Taxonomía y sistemática

Ingrid Yutzil Ruiz-Nuñez ^a, Cristian M. Galván-Villa ^a, *, Omar Domínguez-Domínguez ^b, Rebeca Granja-Fernández ^{a, c}, Miriam Hueytletl-Pérez ^d y Francisco Alonso Solís-Marín ^e

^a Universidad de Guadalajara, Centro Universitario de Ciencias Biológicas y Agropecuarias, Departamento de Ecología Aplicada, Laboratorio de Ecología, Conservación y Taxonomía, Camino Ramón Padilla Sánchez Núm. 2100, 45200 Zapopan, Jalisco, México 

^b Universidad Michoacana de San Nicolás de Hidalgo, Facultad de Biología, Laboratorio de Biología Acuática, Av. Francisco J. Múgica s/n, Ciudad Universitaria, 58030 Morelia, Michoacán, México 

^c Universidad de Guadalajara, Centro Universitario de Ciencias Biológicas y Agropecuarias, Investigación posdoctoral (SECIHTI)-Programa de Maestría en Biosistemática y Manejo de Recursos Naturales y Agrícolas, Camino Ramón Padilla Sánchez Núm. 2100, 45200 Zapopan, Jalisco, México 

^d Instituto Politécnico Nacional, Centro Interdisciplinario de Ciencias Marinas, Programa de Doctorado en Ciencias Marinas, Av. Instituto Politécnico Nacional s/n, Playa Palo de Santa Rita, 23096 La Paz, Baja California Sur, México 

^e Universidad Nacional Autónoma de México, Instituto de Ciencias del Mar y Limnología, Laboratorio de Sistemática y Ecología de Equinodermos, Circuito Exterior s/n, Ciudad Universitaria, Coyoacán, 04510 Ciudad de México, México 

*Autor para correspondencia: cristian.galvan@academicos.udg.mx (C.M. Galván-Villa)

Resumen

Compuesto por 4 islas volcánicas tropicales, el archipiélago de Revillagigedo cuenta con ecosistemas únicos y bien preservados que lo han incluido en la lista de patrimonio mundial de la UNESCO. El objetivo de este trabajo fue dar a conocer un inventario actualizado de equinodermos del Parque Nacional Revillagigedo, incluidos registros nuevos de especies de las clases Asteroidea y Ophiuroidea, y un análisis de su composición. La diversidad de las islas se evaluó mediante análisis ecológicos (riqueza de especies, similitud y distintividad taxonómica). En total, se obtuvieron 94 especies de equinodermos de las cuales 5 son nuevos registros, 2 estrellas de mar (Heliaster kubiniji y Astrometis sertulifera) y 3 ofiuros (Ophiolepis variegata, Ophiopsila californica y Ophiothela mirabilis). La clase con mayor número de especies en todo el parque resultó ser Ophiuroidea con 31, seguida de Asteroidea, Echinoidea y Holothuroidea con 21 cada una. Las islas Clarión (60 spp.) y Socorro (58 spp.) presentaron la mayor riqueza de especies y diversidad taxonómica. Sin embargo, la riqueza de especies en San Benedicto y Roca Partida puede estar subestimada debido a un menor esfuerzo de muestreo histórico realizado en estas islas. 

Palabras clave: Área natural protegida; Pacífico oriental; Similitud; Diversidad taxonómica; Islas oceánicas

Diversity analysis and new records of echinoderms (Echinodermata) for Revillagigedo National Park, Mexico

Abstract

Consisting of 4 tropical volcanic islands, the Revillagigedo Archipelago has unique and well-preserved ecosystems that have placed it on the UNESCO World Heritage List. The objective of this work was to present the updated inventory of echinoderms of Revillagigedo National Park, including new records of species of the classes Asteroidea and Ophiuroidea, and to analyze their composition. The diversity of the islands was evaluated by ecological analysis (species richness, similarity, and taxonomic distinctiveness). A total of 94 records of echinoderm species were obtained, of which 5 are new records, 2 sea stars (Heliaster kubiniji and Astrometis sertulifera) and 3 brittle stars (Ophiolepis variegata, Ophiopsila californica, and Ophiothela mirabilis). The class with the highest number of species in the park was Ophiuroidea with 31, followed by Asteroidea, Echinoidea, and Holothuroidea with 21 each. Clarion (60 spp.) and Socorro (58 spp.) islands had the highest species richness and taxonomic diversity. However, species richness in San Benedicto and Roca Partida may be underestimated due to less historical sampling effort on these islands.

Keywords: Protected Natural Area; Eastern Pacific; Similarity; Taxonomic diversity; Oceanic islands

Introducción

El Parque Nacional Revillagigedo (PNR) es un archipiélago de 4 islas volcánicas tropicales (Clarión, San Benedicto, Socorro y Roca Partida) en el Pacífico mexicano, que están geográficamente aisladas del continente. En 1994, el archipiélago ingresó a la lista de las Áreas Naturales Protegidas de México bajo la categoría de Reserva de la Biosfera. En 2016, sus islas fueron incluidas en la lista del patrimonio mundial de la UNESCO debido a sus ecosistemas únicos y bien preservados. Para asegurar la conservación del área, el 24 de noviembre de 2017 se decretó la creación del PNR, otorgándole la mayor protección posible, y convirtiéndose en el Parque Nacional más grande de América del Norte (DOF, 2017). El aislamiento geográfico y la protección que se le ha dado a la zona la han convertido en un refugio para las distintas especies que la habitan (Becerril-García et al., 2020; Ruiz-Sakamoto et al., 2018). Asimismo, en el Parque se han desarrollado procesos evolutivos que han dado como resultado un alto grado de endemismos, tanto en la parte terrestre como en la marina, reflejando así su relevancia biológica, geológica y ecológica, así como la necesidad de su adecuada protección y manejo (Conanp-Semarnat, 2015; Semarnat-Conanp, 2019).

Los equinodermos son uno de los muchos grupos de fauna marina presentes en el PNR. El primer estudio realizado sobre los equinodermos del PNR data de 1907, cuando H. L. Clark describió al equinoideo Hesperocidaris perplexa, con material recolectado por la expedición Albatrossen isla Clarión (Clark, 1907). Resultado de la misma expedición y en la misma isla, Fisher (1911) reportó el primer registro de un asteroideo, Henricia clarki. Posteriormente, como producto de las recolectas de la expedición Zaca en isla Clarión, se generaron los primeros registros de ofiuroideos (Ophiacantha pyriformis, Ophiactis savignyi, Ophioderma variegatum, Ophiocoma aethiops, Ophionereis annulata y Ophiothrix galapagensis) (Ziesenhenne, 1937) y holoturoideos (Holothuria (Cystipus) inhabilis y Holothuria (Platyperona) difficilis) (Deichmann, 1937).

Algunos trabajos han reportado, de manera particular para cada isla, escasos equinodermos (e.g., Bautista-Romero et al., 1994; Reyes-Bonilla, 1995), y otros se han dado a la tarea de compilar listas más completas para la región del Pacífico mexicano, incluyendo en estas listas el PNR (Granja-Fernández et al., 2015, 2021; Honey-Escandón et al., 2008; Solís-Marín et al., 2013). El inventario más reciente para el PNR es el presentado por Granja-Fernández et al. (2021), quienes incluyeron un total de 85 especies presentes en el archipiélago, de las cuales 19 pertenecen a la clase Asteroidea, 25 a Ophiuroidea, 21 a Echinoidea y 20 a Holothuroidea. Sin embargo, en ninguno de estos trabajos se analiza la diversidad de especies para cada una de las islas que conforman el archipiélago. Además, recientemente y producto de la revisión de ejemplares depositados en colecciones científicas biológicas, se han encontrado nuevos registros para el área. Lo anterior hace necesario una actualización de información, por lo que este trabajo tuvo como objetivo sumar al conocimiento taxonómico de las islas Revillagigedo la incorporación de nuevos registros de especies de las clases Asteroidea y Ophiuroidea, así como realizar un análisis de la diversidad mediante índices cualitativos de similitud y de diversidad taxonómica para cada una de las islas.

Materiales y métodos

El PNR se localiza en el Pacífico mexicano, a unos 400 km de Cabo San Lucas, Baja California Sur y a 540 km del puerto de Manzanillo, Colima (fig. 1). La superficie total del archipiélago es de 14,808,780 ha, de las cuales 14,793,261 ha corresponden a la parte marina y 15,518 ha corresponden a la parte insular. El archipiélago está compuesto por 4 islas: Clarión (20 km²), San Benedicto (6 km²), Socorro (132 km²) y Roca Partida (0.014 km²) (Semarnat-Conanp, 2019). Las islas están compuestas por un conjunto de acantilados, playas rocosas y arenosas, bahías y manantiales (Conabio-Conanp-TNC-Pronatura, 2007). Su origen se asocia con la actividad de 3 placas tectónicas (Pacífico, Rivera y Cocos) y fenómenos volcánicos (Pardo y Suárez, 1995). Las islas tienen un origen volcánico común, pero, cada una de ellas presenta una morfología distinta que a su vez impacta, en mayor o menor grado, a la biodiversidad presente en ellas (Conanp-Semarnat, 2017).

El PNR converge entre 2 extensas regiones biogeográficas: la del Pacífico nororiental templado y la del Pacífico oriental tropical (Spalding et al., 2007). Algunas de las características oceanográficas que se presentan en las aguas cercanas al archipiélago son la influencia de las aguas templadas y ricas en nutrientes de la corriente de California y de las aguas cálidas de la corriente Norecuatorial y corriente costera de Costa Rica; asimismo, se tiene una marea mixta predominantemente semidiurna, un oleaje alto, un intervalo de temperatura de 20-28 °C, la presencia de surgencias estacionales, erupciones volcánicas ocasionales, eventos ENSO, tormentas tropicales y huracanes. En la zona del archipiélago se ha registrado una profundidad máxima de 4,856 m (Conanp-Semarnat, 2017). 

Con la finalidad de conocer la riqueza específica de equinodermos para cada una de las islas del PNR, se llevó a cabo la revisión de literatura histórica, abarcando registros desde 1907 hasta 2024. Posteriormente, se revisó el material depositado en la Colección Nacional de Equinodermos “Dra. Ma. Elena Caso Muñoz” (ICML-UNAM), Ciudad de México, México y Colección Biológica del Laboratorio de Ecología Molecular y Taxonomía (LEMITAX) del Departamento de Ecología Aplicada del Centro Universitario de Ciencias Biológicas y Agropecuarias (CUCBA) de la Universidad de Guadalajara (UdeG), Jalisco, México. La determinación taxonómica de los ejemplares se llevó a cabo con las descripciones originales tomando en cuenta las características morfológicas externas diagnósticas para cada especie (Clark, 1921; Lütken, 1856; Verrill, 1867; Xantus, 1860). El material se examinó utilizando un microscopio estereoscópico Olympus ® SZX7 y revisando, tanto ejemplares preservados en seco, como en alcohol etílico al 70%. 

Con los registros obtenidos para cada una de las islas, se construyó una matriz de incidencia (binaria), ya que los datos provenían de distintas fuentes y métodos de muestreo. Se revisaron y actualizaron los nombres válidos de las especies en WoRMS (2024). La similitud de especies se estimó con el índice de Jaccard, con base en la matriz de incidencia. Se realizó un análisis de escalonamiento multidimensional no métrico (nMDS) y un análisis de clasificación (dendrograma) con la finalidad de identificar agrupaciones entre las islas con base en su riqueza. El dendrograma se construyó con el método de agrupamiento de pares con la media aritmética no ponderada (UPGMA) y la identificación de grupos se hizo con la prueba de perfiles de similitud (Simprof) basada en promedio en 10,000 permutaciones y 9,999 simulaciones con un nivel de significancia de 0.05 (Clarke et al., 2008).

Para medir el grado en el cual las especies están relacionadas taxonómicamente unas con otras y el grado por el cual los taxones están alta o pobremente representados entre las islas, se estimó la distinción taxonómica promedio (Δ⁺) y su variación (Λ⁺) (Clarke y Warwick, 1999). Se usaron 5 categorías taxonómicas jerárquicas: especie, género, familia, orden y clase, las cuales se tomaron con base en la clasificación para equinodermos propuesta en WoRMS (2024). Los niveles taxonómicos fueron ponderados de la siguiente manera: w1, especies dentro del mismo género; w2, especies dentro de la misma familia, pero en diferente género; w3, especies dentro del mismo orden, pero en diferente familia, y así sucesivamente (Warwick y Clarke, 1995). Los embudos de la Δ⁺ y Λ⁺ se crearon con un intervalo de confianza de 95%. Todos los análisis estadísticos se realizaron con el programa PRIMER v6 (Clarke y Gorley, 2006).

Las abreviaturas utilizadas fueron, para asteroideos, R: radio mayor (medida del disco al brazo), r: radio menor (medida del disco al interadio), R/r: radio mayor entre el radio menor, AD: alto del disco. Para ofiuroideos, DD: diámetro del disco, LB: largo del brazo, AB: ancho del brazo (tomando la medida siempre en la vértebra 15).

Descripciones

Nuevos registros

Phylum Echinodermata Klein, 1778

Subphylum Asterozoa Zittel, 1895

Clase Asteroidea de Blainville, 1830

Orden Forcipulatida Perrier, 1884

Familia Asteriidae Gray, 1840

Género Astrometis Fisher, 1923

Astrometis sertulifera (Xantus, 1860)

Fig. 2

Material examinado: 1 individuo. Bahía Eclipse, isla Roca Partida, islas Revillagigedo, México, 19°00’32” N, 112°04’55.9” O: 1 ind. (ICML-UNAM 2.125.5), preservado en seco.

Descripción: R = 20.11 mm; r = 15.4 mm; R/r = 1.30 mm; AD = 16.98 mm. Disco pequeño, bien definido, sobresaliente, delimitado por placas abactinales que soportan cada espina medianamente larga, cónica y lisa. Cuerpo de aspecto espinoso (fig. 2A). El surco ambulacral es amplio, los pies ambulacrales presentan ventosa terminal (fig. 2B). Por cada mandíbula se encuentran 4 espinas orales y 2 suborales (fig. 2C). Del disco salen 5 radios estrechos en su base, angulares, moderadamente cónicos y con punta roma, ornamentados con espinas (fig. 2D). Madreporita redonda, con estrías irregulares. Las espinas abactinales son grandes, con la base más ancha que la punta, de aspecto cónico con punta roma. Las espinas marginales son de menor longitud que todas las demás de la superficie abactinal. Entre las placas abactinales se encuentran las áreas papulares en forma grupal e individualmente entre las espinas ambulacrales y adambulacrales de la superficie actinal. Las espinas adambulacrales se distinguen claramente, son largas, lisas, planas, presentes en 1 sola fila y con punta roma. Las espinas ambulacrales son similares, pero de menor tamaño. Cada espina abactinal y superomarginal se encuentra rodeada en su base o en algún punto longitudinal por un collar de pedicelarios no pedunculados cruzados, de tamaño mediano, bivalbados, dentados en la punta con la base empalmada (fig. 2E, F). Los pedicelarios se encuentran también dispersos en la superficie abactinal, diferenciados por los de alrededor de las espinas principalmente por un mayor tamaño.

Familia Heliasteridae Viguier, 1879

Género Heliaster Gray, 1840

Heliaster kubiniji Xantus, 1860

Fig. 3

Material examinado: 11 individuos. Bahía Eclipse, isla Roca Partida, islas Revillagigedo, México, 19°00’32” N, 112°04’55.9” O: 7 ind. (ICML-UNAM 2.62.2); 4 ind. (ICML-UNAM 2.62.3), preservado en seco.

Descripción: R = 22.24-68.37 mm; r = 12.33-37.43 mm; R/r (x̄) = 1.83 mm; AD = 4.69-25.98 mm. Disco grande con relación a los brazos, no elevado pero abultado en el centro, ornamentado con espinas abactinales cilíndricas robustas y de punta roma, unido a varios radios (de 21 a 24) deprimidos actinalmente, con espinas gruesas, cortas y con espineletas en el extremo distal, dispuestas en 4-6 hileras (fig. 3A, B). Una madreporita pequeña y estriada irregular y onduladamente (fig. 3C). Espinas que ornamentan la placa carinal son las más cilíndricas y gruesas de todas las espinas actinales. Placas marginales soportan espinas de aspecto cilíndrico con la punta aplanada. Superficie actinal plana, con espinas aplanadas en el extremo distal. Espinas ambulacrales en 1 hilera, surco ambulacral más amplio en la base del brazo que en la punta, podios con ventosa terminal (fig. 3D). Cuatro espinas orales por mandíbula, centrales aplanadas, largas, cónicas, con punta aguda, laterales del mismo aspecto, pero de menor longitud (fig. 3E). Pedicelarios en la superficie abactinal; cruzados y rectos, bivalbados, dispersos en todo el disco y más concentrados conforme se acerca la parte distal del radio, algunos cuantos dispersos también entre las espinas orales (fig. 3F).

Clase Ophiuroidea Gray, 1840

Orden Amphilepidida O´Hara, Hugall, Thuy, Stöhr et Martynov, 2017

Familia Ophiolepididae Ljungman, 1867

Género Ophiolepis Müller et Troschel, 1840

Ophiolepis variegata Lütken, 1856

Fig. 4

Material examinado: 2 individuos. Bahía Eclipse, isla Roca Partida, islas Revillagigedo, México, 19°00’32” N, 112°04’559” O: 2 ind. (ICML-UNAM 3.26.3), preservado en seco.

Descripción: DD = 5.36-6.94 mm; LB = 12.00-20.00 mm; AB = 1.21-1.48 mm. Disco pentagonal. Disco dorsal (fig. 4A) cubierto por placas grandes rodeadas por placas más pequeñas, todas con arreglo muy definido; placa central del disco casi redonda, rodeada por 5 placas pentagonales más o menos regulares que forman una roseta; de este sistema de placas centrales irradian 5 hileras que abarcan hasta los márgenes interradiales. Gran placa cuadrangular entre la base de los radios y la parte distal de los escudos radiales. Escudos radiales grandes, en forma de gota. Interradio cubierto por placas grandes de forma y tamaño irregular (fig. 4B). Escudos orales pentagonales con el borde distal alargado, más largos que anchos, angostos en su parte media (fig. 4C). Escudos adorales pequeños, en contacto entre sí (fig. 4C). Cuatro papilas orales triangulares a cada lado de la mandíbula (fig. 4C). Cinco brazos robustos. Placas dorsales trapezoidales con bordes rectos, más anchas que largas (fig. 4D). Placas accesorias pequeñas, segmentadas en 2 piezas. Placas ventrales heptagonales, más anchas que largas (fig. 4E). Dos escamas tentaculares grandes, predominando en tamaño la adradial. De 3 a 4 espinas de los brazos, cortas y puntiagudas. Coloración del disco beige con algunas manchas gris oscuro dispersas; brazos en vista dorsal con bandas beige y gris oscuro, abarcando 1-3 segmentos (fig. 4A).

Famlia Ophiopsilidae Matsumoto, 1915

Género Ophiopsila Forbes, 1843

Ophiopsila californica A. H. Clark, 1921 

Fig. 5

Material examinado: 1 individuo. Isla Roca Partida, islas Revillagigedo, México, 19°00’32” N, 112°04’55” O: 1 ind. (ICML-UNAM 3.102.2), preservado en alcohol al 70%.

Descripción: DD = 6.08 mm; LB = 48.48 mm; AB = 1.48 mm. Disco cubierto dorsal y ventralmente por numerosas escamas pequeñas, redondeadas e imbricadas, con apariencia de piel (fig. 5A, B). Escudos radiales largos y delgados, con aspecto triangular. Escudos orales casi tan largos como anchos, triangulares, ángulos laterales redondeados, ligeramente cóncavos. Escudos adorales pequeños, difíciles de distinguir (fig. 5C). Dos papilas orales puntiagudas a cada lado de la mandíbula, la más distal de mayor tamaño (fig. 5C). Cinco brazos delgados. Placas dorsales de los brazos casi tan largas como anchas, ovaladas, en contacto unas con otras (fig. 5D). Placas ventrales de los brazos más largas que anchas, cuadrangulares (fig. 5E). Dos escamas tentaculares, la adradial con forma de hoja, muy larga, llegándose a cruzar distalmente con la adradial contigua, la abradial de menor tamaño. Cinco espinas de los brazos no tan largas, con punta roma, la de en medio la más larga y robusta. Coloración del disco amarillenta con puntos negros tanto dorsal como ventralmente (fig. 5B). Brazos dorsalmente amarillos con bandas transversales marrón (usualmente compuesto por 3 placas), placas claras; brazo con una línea clara que lo recorre longitudinalmente desde la base hasta la punta (fig. 5B). Algunas placas dorsales y espinas de los brazos presentan puntos.

Familia Ophiotrichidae Ljungman, 1867

Género Ophiothela Verrill, 1867

Ophiothela mirabilis (Verrill, 1867)

Fig. 6

Material examinado: 4 individuos. Caleta Norte, isla Clarión, islas Revillagigedo, México, 19°22’14.3” N, 114°41’40.7” O: 1 ind. (LEMA-EQ 829), 23/abril/2023, 20 m, preservado en alcohol al 96%; 3 ind. (LEMA-EQ 831), Punta Tosca, isla Socorro, islas Revillagigedo, México, 18°46’47.8” N, 111°02’49.7” O, 25/abril/2023, 20 m, preservado en alcohol al 96%.

Descripción: DD = 1.45 mm; LB = 4.54-6.04 mm; AB = 0.20-0.24 mm. Disco rosetado, dorsalmente cubierto con piel y gránulos (fig. 6A). Escudos radiales en contacto, cubriendo casi todo el disco, parcialmente cubiertos por gránulos. Interradio cubierto con piel (fig. 6B). Escudos orales y adorales unidos formando un anillo continuo alrededor de la boca, cubiertos totalmente por piel (fig. 6C). Sin papilas orales (fig. 6C). Cerca de 10 papilas dentales. Seis brazos prensiles. Placas dorsales de los brazos cubiertas por pocos gránulos de tamaño irregular, espacio de piel entre las placas (fig. 6D). Placas ventrales de los brazos cubiertas por piel (fig. 6E). De 5 a 6 espinas de los brazos, aserradas en la punta y en forma de gancho, la más dorsal es la de menor tamaño. Sin escamas tentaculares. Coloración dorsal del disco y brazos morado-rosáceo (fig. 6A).

Riqueza de especies 

Como resultado de la revisión histórica y los nuevos registros previamente mencionados, en total se registraron 94 especies de equinodermos (tabla 1), de las cuales 21 corresponden a la clase Asteroidea, 31 a Ophiuroidea, 21 a Echinoidea y 21 a Holothuroidea (tabla 2). La mayor riqueza de equinodermos se encontró en las islas Clarión (60 spp.) y Socorro (58 spp.), mientras que la menor en Roca Partida (20 spp.) y San Benedicto (10 spp.). El mayor número de especies de crinoideos, asteroideos, ofiuroideos y equinoideos se tuvo en la isla Clarión, y para holoturoideos se presentó en la isla Socorro (tabla 2). 

El 4% de las especies (Asteroidea: Acanthaster planci, Mithrodia bradleyi; Echinoidea: Echinometra vanbrunti y Eucidaris thouarsii) han sido registradas en todas las islas. En contraste, el 51% (49 spp.) habitan en solo 1 de las 4 islas. El 7% (7 spp.) (Asteroidea: Mediaster transfuga;Ophiuroidea: Ophiacantha moniliformis, Ophiopholis bakeri, Ophiothrix (Ophiothrix) rudis y Ophiothrix (Ophiothrix) spiculata;Holothuroidea: Euthyonidiella zacae y Holothuria (Mertensiothuria) hilla)han sido reportadas para el archipiélago, pero no se especifica en qué isla fueron encontradas (Granja-Fernández et al., 2015, 2021; Honey-Escandón et al., 2008; Solís-Marín et al., 2013).

Tabla 1

Lista de especies de equinodermos del Parque Nacional Revillagigedo. IS = Isla Socorro, IC = isla Clarión, IB = isla San Benedicto, IR = isla Roca Partida, NE = isla no especificada. *Nuevos registros para cada isla. Especies en negritas corresponden a registros nuevos para el Parque Nacional Revillagigedo.

Clase	Especie
Asteroidea	Acanthaster planci (Linnaeus, 1758) IS, IC, IB, IR*
	Asteropsis carinifera (Lamarck, 1816) IS, IC
	Astrometis sertulifera(Xantus, 1860) IR*
	Astropecten armatus Gray, 1840 IC
	Heliaster kubinijiXantus, 1860 IR*
	Henricia clarki Fisher, 1910 IC
	Henricia seminudus (A.H. Clark, 1916) IC
	Linckia columbiae Gray, 1840 IS, IC
	Luidia bellonae Lütken, 1864 IC
	Luidia columbia (Gray, 1840) IC
	Mediaster transfuga Ludwig, 1905 NE
	Meridiastra modesta (Verrill, 1867) IS
	Mithrodia bradleyi Verrill, 1867 IS, IC, IB, IR*
	Nearchaster (Nearchaster) aciculosus (Fisher, 1910) IC
	Nidorellia armata (Gray, 1840) IB
	Patiria miniata (Brandt, 1835) IS
	Pauliastra aenigma (Ludwig, 1905) IC
	Pentaceraster cumingi (Gray, 1840) IS, IC, IR*
Tabla 1. Continúa
Clase	Especie
	Pharia pyramidata (Gray, 1840) IS
	Phataria unifascialis (Gray, 1840) IS
	Sclerasterias heteropaes Fisher, 1924 IC
Ophiuroidea	Amphipholis pugetana (Lyman, 1860) IC
	Amphiura seminuda Lütken et Mortensen, 1899 IC
	Astrodictyum panamense (Verrill, 1867) IR
	Ophiacantha diplasia H.L. Clark, 1911 IC
	Ophiacantha moniliformis Lütken et Mortensen, 1899 NE
	Ophiacantha pyriformis Ziesenhenne, 1937 IC
	Ophiactis savignyi (Müller et Troschel, 1842) IS*, IC, IR*
	Ophiactis simplex (Le Conte, 1851) IS*
	Ophiocoma aethiops Lütken, 1859 IS, IC
	Ophiocomella alexandri (Lyman, 1860) IS, IC, IR*
	Ophiocomella schmitti A.H. Clark, 1939 IS, IC
	Ophiocomella sexradia (Duncan, 1887) IC
	Ophioderma aija Humara-Gil, Granja-Fernández, Bautista-Guerrero, Solís-Marín et Rodríguez-Troncoso, 2024 IS Ophioderma bichi Humara-Gil, Granja-Fernández, Bautista-Guerrero, Solís-Marín et Rodríguez-Troncoso, 2024 IR Ophioderma hendleri Granja-Fernández, Pineda-Enríquez, Solís-Marín et Laguarda-Figueras, 2020 IS
	Ophioderma occultum Humara-Gil, Granja-Fernández, Bautista-Guerrero et Rodríguez-Troncoso, 2022 IS*, IR
	Ophioderma panamense Lütken, 1859 IS, IC
	Ophioderma variegatum Lütken, 1856 IS, IC
	Ophiolepis pacifica Lütken, 1856 IS
	Ophiolepis variegataLütken, 1856 IR*
	Ophiomyxa panamensis Lütken et Mortensen, 1899 IS
	Ophionereis annulata (Le Conte, 1851) IS, IC, IR*
	Ophiopholis bakeri McClendon, 1909 NE
	Ophiophragmus papillatus Ziesenhenne, 1940 IS
	Ophiopsila californicaA.H. Clark, 1921 IR*
	Ophiosphalma variabile (Lütken et Mortensen, 1899) IC
	Ophiothela mirabilis(Verrill, 1867) IS*, IC*
	Ophiothrix galapagensis Lütken et Mortensen, 1899 IC
	Ophiothrix (Ophiothrix) rudis Lyman, 1874 NE
	Ophiothrix (Ophiothrix) spiculata Le Conte, 1851 NE
	Ophiuroconis bispinosa Ziesenhenne, 1937 IS
Echinoidea	Astropyga pulvinata (Lamarck, 1816) IS
	Brissopsis pacifica (A. Agassiz, 1898) IS, IC
	Clypeaster europacificus H.L. Clark, 1914 IC
Tabla 1. Continúa
Clase	Especie
	Clypeaster ochrus H.L. Clark, 1914 IC
	Clypeaster rotundus (A. Agassiz, 1863) IC
	Clypeaster speciosus Verrill, 1870 IS, IC
	Diadema mexicanum A. Agassiz, 1863 IS, IC, IB
	Echinometra insularis H. L. Clark, 1912 IS
	Echinometra oblonga (Blainville, 1825) IS, IC
	Echinometra vanbrunti A. Agassiz, 1863 IS, IC, IB, IR*
	Encope micropora insularis H.L. Clark, 1948 IS, IC
	Eucidaris thouarsii (L. Agassiz et Desor, 1846) IS, IC, IB, IR*
	Heterocentrotus mamillatus (Linnaeus, 1758) IS, IC, IB
	Hesperocidaris asteriscus H.L. Clark, 1948 IS
	Hesperocidaris perplexa (H.L. Clark, 1907) IC
	Lovenia cordiformis A. Agassiz, 1872 IS, IC
	Meoma ventricosa grandis Gray, 1851 IS, IC
	Rhyncholampas pacificus (A. Agassiz, 1863) IS, IC
	Toxopneustes roseus (A. Agassiz, 1863) IS, IC
	Tripneustes depressus A. Agassiz, 1863 IS, IC, IB
	Tripneustes gratilla (Linnaeus, 1758) IC
Holothuroidea	Euapta godeffroyi (Semper, 1868) IS, IR*
	Euthyonidiella zacae (Deichmann, 1938) NE
	Holothuria (Cystipus) inhabilis Selenka, 1867 IC
	Holothuria (Halodeima) inornata Semper, 1868 IS, IC
	Holothuria (Halodeima) kefersteinii (Selenka, 1867) IS, IC
	Holothuria (Lessenothuria) coronata Yánez Villanueva, Solís-Marín et Laguarda-Figueras, 2022 IS
	Holothuria (Mertensiothuria) hilla Lesson, 1830 NE
	Holothuria (Mertensiothuria) leucospilota (Brandt, 1835) IS, IC
	Holothuria (Platyperona) difficilis Semper, 1868 IS, IC
	Holothuria (Selenkothuria) lubrica Selenka, 1867 IS, IC, IR*
	Holothuria (Selenkothuria) portovallartensis Caso, 1954 IS, IC
	Holothuria (Semperothuria) imitans Ludwig, 1875 IS, IC, IR*
	Holothuria (Stauropora) fuscocinerea Jaeger, 1833 IS*, IC, IB*
	Holothuria (Theelothuria) paraprinceps Deichmann, 1937 IC
	Holothuria (Thymiosycia) arenicola Semper, 1868 IS, IC
	Holothuria (Thymiosycia) impatiens (Forsskål, 1775) IS, IR*
	Isostichopus fuscus (Ludwig, 1875) IS, IB*, IR*
	Labidodemas americanum Deichmann, 1938 IS*
	Leptosynapta albicans (Selenka, 1867) IS
	Lisacucumis gibber (Selenka, 1867) IS
	Pentamera chierchiae (Ludwig, 1886) IS

Tabla 2

Riqueza de especies para cada clase de equinodermos del Parque Nacional Revillagigedo y para cada una de sus islas. * Registros que no tienen una isla especificada.

Clase	Total	Isla Socorro	Isla Clarión	Isla San Benedicto	Isla Roca Partida	*No especificado
Asteroidea	21	9	13	3	5	1
Ophiuroidea	31	16	18	0	8	4
Echinoidea	21	16	18	5	2	0
Holothuroidea	21	17	11	2	5	3
Total	94	58	60	10	20	8

Similitud entre islas

La comparación de riqueza con los análisis de clasificación y nMDS entre las islas del PNR mostró 2 grupos bien definidos, un primer grupo formado por las islas Socorro y Clarión con 40% de similitud (Simprof, π = 0, p > 0.05) y el segundo formado por San Benedicto y Roca Partida con 20% de similitud (Simprof, π = 0, p > 0.05) (fig. 7A).

Diversidad taxonómica de las islas 

El modelo global de Δ⁺ y Λ⁺ entre las islas del archipiélago mostró que todas las islas poseen una diversidad taxonómica y variación dentro del intervalo de confianza del 95% esperado (p > 0.05) (fig. 7B). Roca Partida tuvo la mayor Δ⁺, a pesar de que Socorro y Clarión son las islas con una mayor riqueza de especies. San Benedicto presentó la menor Δ⁺. Las estimaciones de Λ⁺ para cada una de las islas estuvieron dentro de las estimaciones de probabilidad (fig. 7C).

Discusión 

La revisión taxonómica de los especímenes depositados en colecciones científicas del presente trabajo permitió encontrar 2 nuevos registros de asteroideos (Astrometis sertulifera y Heliaster kubiniji) y 3 de ofiuroideos (Ophiolepis variegata, Ophiopsila californica y Ophiothela mirabilis) para el PNR. Con lo anterior se actualiza el inventario a 94 especies y con los nuevos registros se incrementa la riqueza de especies a 21 para la clase Asteroidea y 31 para Ophiuroidea. Anteriormente, el ofiuroideo Ophioderma teres se reportó para el PNR (Granja-Fernández et al., 2021); sin embargo, la reciente revisión taxonómica de la especie permitió determinar que su identidad corresponde a Ophioderma aija (Humara-Gil et al., 2024), por lo tanto, el registro de O. teres para el PNR se invalida. Al igual que lo reportado por Granja-Fernández et al. (2021), no se encontraron registros verificados de ejemplares de la clase Crinoidea para Revillagigedo. El único registro que se tenía de un crinoideo es el descrito por Roux y Pawson (1999), que corresponde a la especie Hyocrinus foelli, una especie encontrada entre Clarión y la zona de fractura de Clipperton a una profundidad de entre 4,300 y 4,700 m; sin embargo, este no se considera válido, ya que al verificar las coordenadas geográficas del ejemplar recolectado, se encontró distante del límite del parque (Granja-Fernández et al., 2021). La diferencia en riqueza de especies entre trabajos se debe a la actualización del inventario mediante la consulta de literatura, nuevas descripciones y la revisión taxonómica de material depositado en colecciones científicas.

El registro del asteroideo Astrometis sertulifera para Roca Partida corresponde a un nuevo registro para el PNR, así como para el Pacífico central mexicano, ya que la especie solo había sido reportada en México para la costa oeste de Baja California y el golfo de California (Honey-Escandón et al., 2008; Solís-Marín et al., 2005). Por otro lado, Heliaster kubiniji fue reportada por Bautista-Romero et al. (1994) para isla Clarión, sin embargo, al no poder ser confirmado por la falta de un ejemplar que permitiera la validación, no fue incluida en el recuento de Granja-Fernández et al. (2021). La revisión de material depositado en la colección del ICML-UNAM permitió corroborar su presencia en el PNR, específicamente en isla Roca Partida. La distribución de esta estrella es muy amplia, abarcando México, las islas Galápagos y Perú (Solís-Marín et al., 2013). La especie es más común en el golfo de California en México, sin embargo, se ha reportado que se presentan registros ocasionales dispersos hacia el noroeste de Baja California y el sur de California (EUA), los cuales probablemente están asociados a eventos de El Niño (Kerstitch y Bertsch, 2007). 

Tres nuevos registros de ofiuros se lograron identificar con base en ejemplares de las colecciones ICML-UNAM y LEMITAX. Ophiolepis variegata ha sido previamente registrada a lo largo de la costa del Pacífico mexicano (Granja-Fernández et al., 2015) y específicamente en el Pacífico central mexicano, en Nayarit, Jalisco, Colima e islas Marías (Granja-Fernández et al., 2021); sin embargo, su hallazgo en el PNR (isla Roca Partida) corresponde a un registro nuevo para el archipiélago. El caso de Ophiopsila californica es de particular importancia ya que su distribución comprende desde California hasta el norte del Pacífico mexicano (Granja-Fernández et al., 2015). Su recolecta en isla Roca Partida no solo corresponde a un registro nuevo para el Pacífico central mexicano, sino también a una ampliación de su rango de distribución al sur. Finalmente, a pesar de que Ophiothela mirabilis se encuentra ampliamente distribuida en el Pacífico mexicano (Granja-Fernández et al., 2015), esta es la primera vez que se registra en el PNR, específicamente para las islas Clarión y Socorro.

Cabe destacar que el presente trabajo analiza por primera vez la riqueza de equinodermos para cada una de las islas del PNR. Las islas Clarión (61) y Socorro (58), además de poseer la mayor riqueza de equinodermos total y por clases, se agruparon dentro de los análisis nMDS y dendrograma, compartiendo 35 especies. San Benedicto y Roca Partida formaron otro grupo, con una baja similitud, donde comparten solamente 5 especies. Los valores de riqueza de especies pueden estar relacionados con el tamaño de las islas. En este caso, las islas más grandes (Socorro y Clarión) presentan el mayor número de especies y, por el contrario, las islas más pequeñas (San Benedicto y Roca Partida) tienen la menor riqueza de especies. Este patrón puede no estar asociado solamente con el tamaño de las islas, sino también con los hábitats que proporcionan y con la intensidad de muestreo en cada una de ellas. Clarión y Socorro se caracterizan por playas de material calcáreo biogénico asociado con corales, así como con sedimentos (arenas y limos) conformados por moluscos y corales, crecimientos algales, entre otros (Semarnat-Conanp, 2019). Todos estos hábitats son propicios para el establecimiento de larvas (Doll et al., 2022), protección/desarrollo (Hermosillo-Núñez et al., 2015; Herrero-Pérezrul et al., 2015) y alimentación de equinodermos (Siburian et al., 2023). Esta heterogeneidad en la estructura de los hábitats no se presenta en San Benedicto y Roca Partida, ya que la primera está compuesta, principalmente, de rocas volcánicas y la segunda es la cima de un volcán submarino (Semarnat-Conanp, 2019). 

Respecto de la intensidad de muestreo, la exploración de Clarión y Socorro ha llamado la atención de científicos desde 1930 y han sido visitadas desde entonces por expediciones tan importantes como Albatross, Velero y Zaca (Caso, 1962; Deichmann, 1941; Ziesenhenne, 1937). Resultado de lo anterior es que Clarión y Socorro poseen el mayor número de estudios publicados (41 y 47 trabajos, respectivamente) con registros de equinodermos de zonas someras y profundas. En cambio, para San Benedicto solo existen 2 trabajos (Bautista-Romero et al., 1994; Reyes-Bonilla, 1995) en los que se reportan 8 especies de las clases Asteroidea y Echinoidea; con la presente revisión de colecciones científicas, se añaden 2 nuevos registros de holoturoideos para San Benedicto (Holothuria (Stauropora) fuscocinerea e Isostichopus fuscus). Previo a este estudio, el único equinodermo que había sido reportado para la isla Roca Partida era el ofiuro Astrodictyum panamense (Ayala-Bocos et al., 2011), por lo que se aportan 17 nuevos registros para esta isla (5 de la clase Asteroidea, 5 de Ophiuroidea, 2 de Echinoidea y 5 Holothuroidea). A pesar de que San Benedicto y Roca Partida tienen la menor riqueza de equinodermos, no se descarta que con mayor esfuerzo de muestreo se encuentre una mayor riqueza de equinodermos en estas islas. 

A pesar de las diferencias en riqueza entre islas, existen 4 especies que han sido registradas en todas ellas: 2 asteroideos (Acanthaster planci y Mithrodia bradleyi)y 2 equinoideos (Echinometra vanbrunti y Eucidaris thouarsii). Sin embargo, especies como la estrella de mar Pentaceraster cumingi, el ofiuro Ophiocomella alexandri, el erizo Toxopneustes roseus y el pepino I. fuscus, se espera que habiten en todas las islas y sus alrededores, ya que tienen una amplia distribución a lo largo del Pacífico mexicano y americano (Granja-Fernández et al., 2015, 2021; Honey-Escandón et al., 2008; Solís-Marín et al., 2013). También cabe resaltar que, a pesar de las diferencias en riqueza, el análisis de diversidad taxonómica sugiere que la composición de cada isla es un subconjunto al azar del conjunto regional de especies, ya que los valores se encontraron dentro del intervalo de confianza de 95%, es decir, todas las islas son representativas de la diversidad taxonómica del PNR, inclusive San Benedicto y Roca Partida, que tienen la menor riqueza de especies.

La riqueza de especies de equinodermos del PNR representa cerca de 15% de la riqueza registrada en todo México (Solís-Marín et al., 2013, 2014). Si se compara la riqueza de manera particular con las diferentes regiones del Pacífico mexicano como el golfo de California y el Pacífico mexicano, encontramos que el PNR presenta 40.5% y 43.5% de especies, respectivamente. Comparando con la región del Pacífico central mexicano, en el parque se encuentra 50% de estas especies (Granja-Fernández et al., 2021). Esto respalda la importancia de Revillagigedo en términos de conservación, ya que resguarda cerca de la mitad de especies de equinodermos que se pueden encontrar en el Pacífico mexicano.

Para generar un inventario más completo de las especies de equinodermos presentes en el PNR se requiere una búsqueda dirigida al grupo y a los distintos sustratos en los que habitan (e.g., arena, rocas, corales). Se recomienda incrementar el esfuerzo de muestreo principalmente en San Benedicto y Roca Partida. Asimismo, si bien la mayor parte de registros pertenecen a especies someras (< 30 m de profundidad), es necesaria la exploración de aguas profundas del PNR y sus alrededores, ya que poseen un alto potencial de albergar equinodermos por su amplia batimetría que puede alcanzar hasta 5,000 m de profundidad y a la presencia de ventilas hidrotermales (Semarnat-Conanp, 2019). También es necesario dirigir esfuerzos sobre especies crípticas, las cuales regularmente están ocultas y cuya percepción no es tan sencilla en su hábitat (principalmente especies de las clases Ophiuroidea y Holothuroidea), ya que suelen encontrarse bajo rocas o enterradas en el sedimento.

Agradecimientos

Al personal de Conanp del Parque Nacional Revillagigedo por la invitación a CMGV y ODD para participar en la expedición científica 2023. Al personal del Instituto de Biología de la UNAM, Susana Guzmán Gómez y María B. Mendoza Garfias; al personal del ICML de la UNAM, Laura E. Gómez Lizárraga, Alicia Durán González y Carlos A. Conejeros Vargas, por su disposición y colaboración para la realización de este estudio. A Brenda Maya Alvarado por la consulta de referencias bibliográficas que nutren este artículo y a Karla Humara Gil por la corroboración de registros por isla para el género Ophioderma. Agradecemos el apoyo técnico para la captura de imágenes de Alicia Durán González, María B. Mendoza Garfias, Susana Guzmán Gómez y Laura E. Gómez Lizárraga de la UNAM. Al editor y revisores anónimos por sus comentarios invaluables al manuscrito.

Referencias

Ayala-Bocos, A., Reyes-Bonilla, H., Herrero-Perezrul M. D., Walther-Mendoza, M. y Castañeda-Fernández de Lara, V. (2011). New records and range extensions of Astrodictyum panamense (Ophiuroidea: Gorgonocephalidae) in the Eastern Pacific Ocean. Marine Biodiversity Records. Marine Biological Association of the United Kingdom, 4, e46. https://doi.org/10.1017/S175526721100032 

Bautista-Romero, J. J., Reyes-Bonilla, H., Lluch-Cota, D. y Lluch-Cota, S. (1994). Aspectos generales de la fauna marina. En A. Ortega-Rubio y A. Castellanos-Vera (Eds.), La isla Socorro, Reserva de la Biosfera Archipiélago de Revillagigedo (pp. 247–275). La Paz: CIBNOR. 

Becerril-García, E. E., Hoyos-Padilla, E. M., Henning, B. y León, P. S. (2020). Sharks, rays, and chimaeras of the Revillagigedo National Park: An update of new and confirmed records. Journal of Fish Biology, 97, 1228–1232. https://doi.org/10.1111/jfb.14457 

Caso, M. E. (1962). Estudios sobre equinodermos de México. Contribución al conocimiento de los equinodermos de las islas Revillagigedo. Anales del Instituto de Biología, Universidad Nacional Autónoma de México, 33, 293–330.

Clark, A. H. (1921). A new ophiuran of the genus Ophiopsila from Southern California. Proceedings of the Biological Society of Washington, 34, 109–110.

Clark, H. L. (1907). The Cidaridae. Bulletin of the Museum of Comparative Zoology, 7, 165–230.

Clarke, K. R. y Gorley, R. N. (2006). Primer v6: user manual and tutorial. Plymouth, UK: Primer-E.

Clarke, K. R., Somerfield, P. J. y Gorley, R. N. (2008). Testing of null hypotheses in exploratory community analyses: similarity profiles and biota-environment linkage. Journal of Experimental Marine Biology and Ecology, 366, 56–69. https://doi.org/10.1016/j.jembe.2008.07.009 

Clarke, K. R. y Warwick, R. M. (1999). The taxonomic distinctness measure of biodiversity: weighting of step lengths between hierarchical levels. Marine Ecology Progress Series, 184, 21–29.

Conabio (Comisión Nacional para el Conocimiento y Uso de la Biodiversidad)-Conanp (Comisión Nacional de Áreas Naturales Protegidas) -TNC-Pronatura. (2007). Sitios marinos prioritarios para la conservación de la biodiversidad. Escala 1: 1000 000. México: Comisión Nacional para el Conocimiento y Uso de la Biodiversidad, Comisión Nacional de Áreas Naturales Protegidas/ The Nature Conservancy – Programa México, Pronatura, A.C.

Conanp (Comisión Nacional de Áreas Naturales Protegidas)-Semarnat (Secretaría de Medio Ambiente y Recursos Naturales). (2015). Formulario de Nominación del Bien Natural Archipiélago de Revillagigedo para su Inscripción en la Lista del Patrimonio Mundial. México D.F.: Comisión Nacional de Áreas Naturales Protegidas, Secretaría de Medio Ambiente y Recursos Naturales.

Conanp (Comisión Nacional de Áreas Naturales Protegidas)-Semarnat (Secretaría de Medio Ambiente y Recursos Naturales). (2017). Estudio Previo Justificativo para la declaratoria del Parque Nacional Revillagigedo. México: Comisión Nacional de Áreas Naturales Protegidas, Secretaría de Medio Ambiente y Recursos Naturales.

Deichmann, E. (1937). The Templeton Crocker Expedition. IX. Holothurians from the Gulf of California, the West Coast of Lower California and Clarion Island. Zoologica, 22, 161–176.

Deichmann, E. (1941). The Holothuroidea collected by the “Velero III” during the years 1932-1938. Part I. Dendrochirotida. Allan Hancock Pacific Expeditions, 8, 61–195.

Diario Oficial de la Federación (DOF). (2017). Decreto por el que se declara como Área Natural Protegida, con el carácter de Parque Nacional, la región conocida como Revillagigedo, localizada en el Pacífico Mexicano. Publicada en el Diario Oficial de la Federación el 27 de noviembre de 2017. México. Recuperado el 21 de enero, 2024 de: https://www.gob.mx/epn/prensa/comunicado-136165 

Doll, P. C., Caballes, C. F., Hoey, A. S., Uthicke, S., Ling, S. D. y Pratchett, M. S. (2022). Larval settlement in echinoderms: a review of processes and patterns. Oceanography and Marine Biology: An Annual Review, 60, 433–494. https://doi.org/10.1201/9781003288602-9 

Fisher, W. K. (1911). Asteroidea of the North Pacific and adjacent waters, Part I: Phanerozonia and Spinulosa. Bulletin of the United States National Museum, 76, 1–419.

Granja-Fernández, M. R., Herrero-Pérezrul, M. D., López-Pérez, R. A., Hernández-Morales, A. y Rangel-Solís, P. D. (2015). A literature review of the Ophiuroidea (Echinodermata) from the Pacific coast of Mexico. Revista de Biología Tropical, 63, 37–47. http://dx.doi.org/10.15517/rbt.v63i2.23127 

Granja-Fernández, M. R., Maya-Alvarado, B., Cupul-Magaña, A. L., Rodríguez-Troncoso, A. P., Solís-Marín, F. A. y Sotelo-Casas, R. C. (2021). Echinoderms (Echinodermata) from the Central Mexican Pacific. Revista de Biología Tropical, 69, 219–259. http://dx.doi.org/10.15517/rbt.v69isuppl.1.46356 

Hermosillo-Núñez, B. B., Rodríguez-Zaragoza, F. A., Ortiz, M., Galván-Villa, C., Cupul-Magaña A. y Ríos-Jara, E. (2015). Effect of habitat structure on the most frequent echinoderm species inhabiting coral reef communities at Isla Isabel National Park (Mexico). Community Ecology, 16, 125–134. https://doi.org/10.1556/168.2015.16.1.14 

Herrero-Pérezrul, M. D., Ramírez-Ortíz, G., Rosales-Estrada, M. y Reyes-Bonilla, H. (2015). Densidad poblacional y distribución espacial de erizos de mar (Echinodermata: Echinoidea) en la isla Socorro, Archipiélago de Revillagigedo, México. Revista de Biología Tropical, 63, 221–232. https://doi.org/10.15517/rbt.v63i2.23156 

Honey-Escandón, M., Solís-Marín, F. A. y Laguarda-Figueras, A. (2008). Equinodermos (Echinodermata) del Pacífico Mexicano. Revista de Biología Tropical, 56, 57–73. https://doi.org/10.15517/rbt.v56i3.27079 

Humara-Gil, K. J., Granja-Fernández, R., Bautista-Guerrero, E., Solís-Marín, F. A. y Rodríguez-Troncoso, A. P. (2024). Delimitation of Ophioderma teres (Lyman, 1860) and Ophioderma unicolor H.L. Clark, 1940 stat. nov. (Echinodermata: Ophiuroidea), including the description of two new species. European Journal of Taxonomy, 947, 130–174. https://doi.org/10.5852/ejt.2024.947.2625 

Kerstitch, A. y Bertsch, H. (2007). Sea of Cortez marine invertebrates. 2^nd Edition. Monterey, CA: Sea Challengers. 

Lütken, C. F. (1856). Bidrag til kundskab om Slangestjernerne. II. Oversigt over de vestindiske Ophiurer. Videnskabelige Meddelelser fra Dansk Naturhistorisk Förening i Kjøbenhavn 1856, 7, 1–26.

Pardo, M. y Suárez, G. (1995). Shape of the subducted Rivera and Cocos plates in southern Mexico: seismic and tectonic implications. Journal of Geophysical Research, 100, 357–373. https://doi.org/10.1029/95JB00919 

Reyes-Bonilla, H. (1995). Asteroidea and Echinoidea (Echinodermata) of Isla San Benedicto, Revillagigedo Archipiélago, México. Revista de Investigación Científica UABCS, 6, 29–38.

Roux, M. y Pawson, D. L. (1999). Two new Pacific Ocean species of hyocrinid crinoids (Echinodermata), with comments on presumed giant-dwarf gradients related to seamounts and abyssal plains. Pacific Science, 53, 289–298.

Ruiz-Sakamoto, A., Sánchez-Ortiz, C., Stewart, J. D. y Aburto-Oropeza, O. (2018). La Manta Gigante el diamante de Revillagigedo. Biodiversitas, 136, 1–7.

Semarnat (Secretaría de Medio Ambiente y Recursos Naturales)-Conanp (Comisión Nacional de Áreas Naturales Protegidas). (2019). Programa de Manejo Parque Nacional Revillagigedo. México: Semarnat, Conanp.

Siburian, R. H. S., Tapilatu, J. R. y Tapilatu, M. E. (2023). Discovery of habitat preferences and community structure of echinoderms in Kri, Raja Ampat, Indonesia. Biodiversitas, 24, 3968–3976. https://doi.org/10.13057/biodiv/d240735 

Solís-Marín, F. A., Honey-Escandón, M. B. I., Herrero- Pérezrul, M. D., Benítez-Villalobos, F., Díaz-Martínez, J. P., Buitrón-Sánchez, B. E. et al. (2013). The echinoderms of Mexico: biodiversity, distribution and current state of knowledge. En J. J. Alvarado y F. A. Solís-Marín (Eds.), Echinoderm research and diversity in Latin America. Berlín: Springer-Verlag. https://doi.org/10.1007/978-3-642-20051-9_2 

Solís-Marín, F. A., Laguarda-Figueras, A., Durán-González, A., Gust, C. y Torres, J. (2005). Equinodermos (Echinodermata) del Golfo de California, México. Revista de Biología Tropical, 53, 123–137. https://doi.org/10.15517/rbt.v53i3

Solís-Marín, F. A., Laguarda-Figueras, A. y Honey-Escandón, M. (2014). Biodiversidad de equinodermos (Echinodermata) en México. Revista Mexicana de Biodiversidad, 85 (Suplem.),S441–S449. https://doi.org/10.7550/rmb.31805 

Spalding, M. D., Fox, H. E., Allen, G. R., Davidson, N., Ferdaña, Z. A., Finlayson, M. et al. (2007). Marine ecoregions of the world: a bioregionalization of coastal and shelf areas. BioScience, 57, 573–583. https://doi.org/10.1641/B570707 

Verrill, A. E. (1867). Notes on Radiata in the museum of Yale College with descriptions of new genera and species. No. 2. Notes on the echinoderms of Panama and the west coast of America, with descriptions of a new genus. Transactions of the Connecticut Academy of Arts and Sciences, 1, 251–322.

Warwick, R. M. y Clarke, K. R. (1995). New biodiversity measures reveal a decrease in taxonomic distinctness with increasing stress. Marine Ecology Progress Series, 129, 301–305.

WoRMS. (2024). World Register of Marine Species. Recuperado el 01 abril, 2024 de: https://www.marinespecies.org 

Xantus, J. (1860). Descriptions of three new species of starfishes from Cape St. Lucas. Proceedings of the Academy of Natural Sciences of Philadelphia, 12, 568.

Ziesenhenne, F. C. (1937). The Templeton Crocker Expedition. X. Echinoderms from the West Coast of Lower California, the Gulf of California and Clarion Island. Zoology, 22, 209–239. https://doi.org/10.5962/p.184686

Sergio I. Salazar-Vallejo ^a, *, Patricia Salazar-Silva ^b

^a El Colegio de la Frontera Sur, Depto. Sistemática y Ecología Acuática, Unidad Chetumal, Ave. Centenario Km 5.5, 77014 Chetumal, Quintana Roo, Mexico 

^b Tecnológico Nacional de México, Instituto Tecnológico de Bahía de Banderas, Crucero a Punta de Mita, 63734 Bahía de Banderas, Nayarit, Mexico 

*Corresponding author: ssalazar@ecosur.mx (S.I. Salazar-Vallejo)

Abstract 

To clarify the differences between Lepidasthenia Malmgren, 1867 and Lepidametria Webster, 1879, specimens of their type species are redescribed and illustrated. Diagnoses for both genera, a key to species of Lepidasthenia with giant neurochaetae, and a key to species of Lepidametria are included. Lepidasthenia elegans (Grube, 1840), described from the Gulf of Naples, has blocks of black segments alternating with a pale segment, posterior elytrigerous segments blackish; median and posterior segments with elytra every third segment; parapodia without notochaetae; neuropodia with neuropodial pre- and postchaetal lobes with margin entire; median segments with upper single neurochaetae thin, 1-2 giant neurochaetae barely denticulate, and medium-width neurochaetae with tips unidentate (accessory denticle minute). Lepidasthenia digueti Gravier, 1905, described from the Gulf of California living with balanoglossid hemichordates, is redescribed and reinstated. Lepidametria commensalis Webster, 1879, described living with terebellid polychaetes in Virginia, USA, has a brownish transverse segmental band along body; median segments with elytra alternating with dorsal cirri, posterior segments with series of 3-4 elytrigerous interrupted by 1 cirrigerous segment; parapodia with notochaetae; neuropodia elongate with neuropodial prechaetal lobe with upper area lobate, lower one entire, post-chaetal lobe entire; neurochaetae bidentate, median segments with giant neurochaetae barely denticulate.

Keywords: Type-species; Variation; Giant neurochaetae; Prechaetal lobes

Redescripciones de Lepidasthenia elegans, L. digueti y Lepidametria commensalis (Polychaeta: Polynoidae)

Resumen 

Para aclarar las diferencias entre Lepidasthenia Malmgren, 1867 y Lepidametria Webster, 1879, ejemplares de sus especies tipo fueron descritas e ilustradas. Se incluyen diagnosis para ambos géneros, una clave para especies de Lepidasthenia con neurosetas gigantes y una clave para especies de Lepidametria. Lepidasthenia elegans (Grube, 1840), descrita del golfo de Nápoles, tiene bloques negros alternantes con un segmento pálido, elitrígeros posteriores negros; segmentos medios y posteriores con élitros cada tercer segmento; parápodos sin notosetas; neurópodos con lóbulos pre- y postsetales enteros; segmentos medios con neurosetas superiores delgadas, 1-2 neurosetas gigantes apenas denticuladas y neurosetas de grosor medio unidentadas (dentículo accesorio diminuto). Lepidasthenia digueti Gravier, 1905, descrita del golfo de California asociada con balanoglósidos, es redescrita y restablecida. Lepidametria commensalis Webster, 1879, descrita asociada con poliquetos terebélidos en Virginia, EUA, tiene una banda parduzca transversa segmentaria a lo largo del cuerpo; segmentos medios con élitros y cirros alternantes, segmentos posteriores con series de 3-4 elitrígeros y 1 cirrígero; parápodos con notosetas; neurópodos alargados con lógulo presetal con área superior lobulada, inferior entera, lóbulo postsetal entero; neurosetas bidentadas, segmentos medios con neurosetas gigantes apenas denticuladas.

Palabras clave: Especie-tipo; Variación; Neurosetas gigantes; Lóbulos presetales

Introduction

Lepidasthenia Malmgren, 1867, and Lepidametria Webster, 1879 are 2 genera of long-bodied polynoids whose species are commonly found living with other marine invertebrates. Malmgren (1867: 15) added the Greek suffix asthenia which comes from asthenes, meaning “without strength, weak” (Brown, 1954: 348) to emphasize the reduction of elytral size along body. Malmgren (1867: 16) only included Polynoe elegans Grube, 1840, described from the Adriatic Sea, such that it became the type by monotypy. From the original description (Grube, 1840: 85), this species had 2 patterns of sequences for the presence of cirri and elytra: they alternate along anterior and median chaetigers, and from segment 22 or 24, elytra are present singly, and 2 successive segments carry cirri. Malmgren (1867: 15) included the lack of notochaetae, the presence of minute elytra along median and posterior chatigers, and the pattern 2 segments with cirri, one with elytra in median and posterior chaetigers.

Webster (1879: 209-210) proposed Lepidametria, with Lepidametria commensalis from Virginia, USA, as its only species, and diagnosed it by including the presence of notochaetae, elytra not large enough as to cover dorsum, and elytra irregularly arranged in posterior segments. He gave no etymology, but the suffix ametria could be formed by uniting the Greek word metrios, meaning “within measure” (Brown, 521), with the Greek prefix a– meaning “not, without, negative, privative” (Brown, 1954: 62) for indicating the lack of regularity in the elytral pattern along posterior segments. Webster (1879: 210) also noted that Lepidametria differs from Lepidasthenia “by having setae in the dorsal rami”.

Chamberlin (1919: 38) separated the above genera by regarding Lepidasthenia as having elytra in pairs throughout the body, and Lepidametria with some segments having elytra on one side and a cirrus on the other, and he did not include the different sequence of cirri-elytra, or the presence of notochaetae. Seidler (1924: 16) keyed them out after the presence of notochaetae in Lepidametria, and the lack of them in Lepidasthenia (Gardiner, 1976: 85). 

Day (1967: 88) regarded Lepidametria as a junior synonym of Lepidasthenia, but later he changed his mind (Day, 1973: 6). The synonymy, however, had been proposed by Gravier (1905b), Potts (1910), Fauvel (1917), and Hartman (1959: 85) but not by Pettibone (1963: 19).

Pettibone (1989) used the above features, together with the type of parapodia, and elytra for proposing a new subfamily, Lepidastheniinae, and did not include Lepidametria. Consequently, Lepidasthenia and Lepidametria are currently regarded as distinct and different enough, such that they belong to different subfamilies, and there are keys to genera available (Barnich & Fiege, 2004; Salazar-Vallejo et al., 2015). However, the type species of these 2 genera have not been redescribed, and by clarifying their morphological features the affinities of the species in each genus can be clarified, especially because different authors followed the synonymy, whereas others rejected it. These genera differ in the number of species they include; there are 4 species in Lepidametria (Read & Fauchald, 2024a), and over 40 in Lepidasthenia (Read & Fauchald, 2024b).

Materials and methods

During a research visit to the National Museum of Natural History (USNM), Smithsonian Institution, we had the opportunity to study the type material of L. commensalis Webster, 1879, and topotype specimens of L. elegans (Grube, 1840). This completed the previous study of other type specimens in the Muséum National d’Histoire Naturelle, Paris, France (MNHN), such that now we can provide their redescriptions. 

The material is deposited in the Muséum National d’Histoire Naturelle, Paris, France (MNHN), and in the National Museum of Natural History, Smithsonian Institution, Washington, D.C., USA (USNM). Specimens were observed with standard stereo —and compound microscopes; sometimes, some body parts were immersed in Methyl green or Shirlastain-A for increasing the visibility of some morphological features, and this explains their greenish or orange to reddish color in some photos. A series of digital photos in successive focal plains were made for every object; the series of photos were optimized with HeliconFocus and plates were prepared with PaintShop Pro.

Results

Polynoidae Kinberg, 1856

Lepidastheniinae Pettibone, 1989

Lepidasthenia Malmgren, 1867

Type species. Polynoe elegans Grube, 1840, by monotypy.

Diagnosis (after Salazar-Vallejo et al., 2015). Lepidastheniinae with a long body of up to 150 segments. Elytra small, not covering each other, leaving dorsal region mostly uncovered; posterior region with one pair of elytra every 3 segments. Each elytron rounded, margins entire, without tubercles, pale or pigmented. Tentaculophores without chaetae. Notopodia reduced, without notochaetae. Neuropodia projecting with several types of neurochaetae. Ventral surface usually smooth.

Remarks

A key to genera of Lepidastheniinae is available elsewhere (Salazar-Vallejo et al., 2015). Lepidasthenia Malmgren, 1867 resembles Alentiana Hartman, 1942 and Telolepidasthenia Augener & Pettibone in Petibone, 1970 because they have short elytrophores, not transformed into peduncles. However, Lepidasthenia differs by having tiny, non-overlapping elytra in median segments, whereas the 2 other genera have large overlapping elytra in the same body region. Within Lepidasthenia, the presence of giant neurochaetae can separate species into 2 groups; the first group includes those species having giant neurochaetae, including L. elegans, and the larger group includes those species deprived of giant neurochaetae.

Key to species of Lepidasthenia Malmgren, 1867 with giant neurochaetae

(modified after Salazar-Vallejo et al., 2015)

1 Anterior eyes larger than posterior ones …………………………………………………… 2

– Anterior eyes smaller or subequal to posterior ones …………………………………………………… 4

2(1) Dorsal cirri subdistally swollen; ventral cirri digitate …………………………………………………… 3

– Dorsal cirri tapered; ventral cirri basally swollen, tapered …………………………………………………… L. ornata Treadwell, 1937, Western Mexico

3(2) First elytra with innervation …………………………………………………… L. elegans (Grube, 1840), Mediterranean Sea

– First elytra without innervation…………………………………………………… L. izukai Imajima & Hartman, 1964 Japan

4(1) Dorsal cirri subdistally swollen; ventral cirri tapered, surpassing neurochaetal lobe tip; neuraciculae falcate…………………………………………………… L. esbelta Amaral & Nonato, 1982, Brazil

– Dorsal and ventral cirri tapered, ventral cirri short, not reaching neurochaetal lobe tip…………………………………………………… 5

5(4) Palps 2 times as long as lateral antennae; giant neurochaetae unidentate…………………………………………………… L. loboi Salazar-Vallejo, González & Salazar-Silva, 2015 Patagonia

– Palps slightly longer than lateral antennae; giant neurochaetae uni- and bidentate ……………………………………………………L. nuda (Grube, 1870) Red Sea 

Lepidasthenia elegans (Grube, 1840)

Fig. 1

Polynoe elegans Grube, 1840: 85.

Polynoe lamprophthalma von Marenzeller, 1874: 408, Pl. 1, Fig. 1.

Lepidasthenia elegans: von Marenzeller, 1876: 139-141 (syn.); Benham, 1901: 293 (pigm. pattern); Fauvel, 1923: 88, Fig. 33a-g (syn.); Seidler, 1924: 161-162; Barnich & Fiege, 2003: 88-90, Fig. 46; Núñez et al., 2015: 169-170, Fig. 69.

Diagnosis. Lepidasthenia with nuchal lappet smooth; anterior elytra with branching venation, median and posterior elytra minute, transparent; neurochaetae bidentate, including giant barely denticulate, and smaller clearly denticulate ones in median chaetigers; ventral surface of neuropodia smooth. 

Description. Largest non-type specimen (USNM 47901) with body depressed, twisted; dorsum with 3 black longitudinal wide bands progressively paler, forming distinct blocks separated by a white segment, median band narrowest, often discontinuous (Fig. 1A); first block along chaetigers 2-7, then one segment pale, continued with blocks made of 3-4 segments, interrupted by a single pale segment, such that there are 4 blocks of 3 pigmented segments, followed by one with 4 segments, and then median and posterior regions with elytrigerous segments darker, followed by 2 paler cirrigerous segments. Venter pale, blackish along base of parapodia. Cephalic appendages and dorsal cirri white; elytra transparent. Pharynx fully exposed, brownish, 11 pairs of terminal papillae, transparent, some with a blackish core; 2 midlateral round papillae, behind terminal ones. Second largest specimen with pharynx not exposed; anterior elytra, and left parapodia of chaetigers 10 and 40 removed for observation (kept in container).

Prostomium bilobed, sub-hexagonal, slightly wider than long, facial tubercle not visible dorsally, globose. Eyes black, anterior eyes about 2 times as large as posterior ones, in widest prostomial area, directed laterally; posterior eyes close to posterior margin (Fig. 1B); in 3 specimens eyes enlarged, almost fused laterally. Median antenna slightly longer than right lateral one (left one in regeneration), ceratophore slightly wider than laterals; lateral antennae on prostomial anterior extensions; all ceratostyles cylindrical, mucronate. Palps massive, non-papillate, almost as long as median antenna, mucronate. 

Tentacular segment not visible dorsally: tentaculophores long, cirrostyles wide, 3-4 times as long as prostomium; without chaetae. Segment 2 without nuchal lappet; first pair of parapodia and elytrophores directed anteriorly; ventral cirri 5-6 times as long as following ones (3-4 times in smallest specimen); elytrophores short anteriorly, minute along median and posterior rergions.

Elytra 30 pairs (22 in smallest specimen), smooth, without fimbriae, progressively smaller in median and posterior chaetigers; first 13(11) pairs alternating with cirrigerous segments, then present every third segment. First elytra with distinct branching venation from insertion area (Fig. 1C), posterior elytra minute slightly larger than elytrophore (Fig. 1D).

Parapodia sequiramous. Dorsal cirri with cirrophore short, cylindrical along anterior chaetigers, inserted basally (Fig. 1E), truncate conical in posterior chaetigers (Fig. 1F), terete, mucronate, surpassing neurochaetal tips. Notopodium short, round, without chaetae. Neuropodium with pre- and postchaetal lobes of similar size, both with margins smooth, without acicular lobes. Ventral cirri tapered, short, inserted basally. Nephridial lobes from segment 12, digitate.

Anterior chaetigers with neurochaetae barely swollen subdistally (Fig. 1E), pectinate area with petaloid spines, tips bidentate, accessory tooth almost as large as main one (Fig. 1E, inset). Posterior chaetigers with neurochaetae less spinous, of 3 types, superior neurochaetae thin, spinous superior giant neurochaetae darker with tips bidentate or unidentate, and thinner bidentate neurochaetae (Fig. 1F, inset).

Posterior region tapered; pygidium with anus terminal, with 2 small, lateral anal cirri (Fig. 1D.

Variation. Pigmentation pattern fades off in older specimens. Anterior eyes are usually 2 times as large as posterior ones, but they are laterally nearly fused in some specimens, but not in all. The sequence of elytrigerous and cirrigerous segments is constant; first 11-13 elytra alternate with cirri, following ones are in a sequence with one elytron and 2 dorsal cirri, to end of body.

Taxonomic summary

Type material. Polynoe elegans Grube, 1840; 2 syntypes (ZMB 17) from Sicily, 4 syntypes (ZMB 1176) from Palermo, and 2 syntypes (ZMB 1177) from unspecified Mediterranean localities, plus several other specimens in the same museum (Lesina: ZMB 1172; Luisin piccolo: 1173; and Cherso: 1174, 1175); pigmentation faded off. 

Additional material. Three specimens (USNM 5144), Bay of Naples, Italy, 1893, purchased from Stazione Zoologica, Napoli (complete, barely pigmented, better defined in smallest specimen; some parapodia and elytra previously removed (kept in container); eyes better defined in one specimen, anterior eyes about 2 times as large as posterior ones; body 37-80 mm long, 4.5-8.5 mm wide, 65-82 chaetigers). Five specimens (USNM 47900), The Maire, Marseille, France, rocky bottom, 9 Apr. 1971, H. Zibrowius, coll. (3 complete; dorsal pigmentation pattern blackish to brownish, one with pharynx partially exposed, with 4 additional papillae, 2 basal to terminal ones, 2 others irregular; chaetigers 2-7 forming a continuous block, then blocks of mostly 3 segments interrupted by a pale segment anteriorly; one with diffuse pigmentation along medial and posterior regions, 2 others with elytrigerous segments darker than paler cirrigerous ones; anterior eyes 2 times as large as posterior ones, not fused laterally; posterior segments of larger specimens with a white mass inside basal dorsal cirri; body 50-70 mm long, 7.0-7.5 mm wide, 85-94 chaetigers). Four specimens (USNM 47901), Cap l’Abeille. 2 km south of Banyuls, France, corals, 30 m, 6 May 1967, M.H. Pettibone and L. Laubier, coll. (3 complete; body 27.5-50.5 mm long, 4.5-6.5 mm wide, 57-72 chaetigers; used for redescription).

Distribution. Mediterranean Sea, in shallow water coralligenous or rocky bottoms.

Remarks

Hartwich (1993: 96) listed several lots in Berlin and regarded them almost all as syntypes. After the study of many types of species described by Grube, we anticipate his type and non-type specimens should be colorless by now, and this explains why we selected one specimen with bright pigmentation for redescribing the species. The pigmentation pattern was clearly illustrated by Benham (1901: 293), and this is rather consistent in specimens from the Mediterranean Sea. Lepidasthenia elegans (Grube, 1840) has been reported from the Indian Ocean (Day, 1967; Potts, 1910), but those specimens differ in several features from the Mediterranean ones, such as the position of the anterior eyes, the type of dorsal and ventral cirri, and the shape of the giant neurochaetae. These records might belong in L. nuda (Grube, 1870), redescribed by Wehe (2006: 73), which could include L. affinis Horst, 1917.

Hartman (1959: 99) regarded Polynoe blainvillii Audouin & Milne Edwards, 1834 as a synonym of L. elegans (Grube, 1840). However, this publication is the compilation of some earlier publications, and the original proposal was P. blainvillii Audouin & Milne Edwards, 1832. Audouin and Milne-Edwards (1832: 430-431; 1834: 94-95) proposed the new name for a specimen briefly described and illustrated by de Blainville (1828: 459, Pl. 10, Fig. 2), but without locality, and identified as Eumolpe scolopendrina Savigny, 1822. The French specialists noted the differences with P. scolopendrina Savigny, 1822 such as having reduced elytra to the posterior end (larger, but missing in posterior region in P. scolopendrina). Regretfully, probably because it was identified as an already known species, de Blainville provided no morphological details in the description but in his illustrations (2: whole body, dorsal view; 2a: parapodium) the parapodium was depicted with notochaetae. As indicated above, notochaetae are missing in Lepidasthenia species, and if P. blainvillii is a Lepidasthenia, this could be an erroneous observation. The de Blainville specimen was not deposited, such that there is no means to clarify this potential synonymy.

Nevertheless, if P. scolopendrina sensu de Blainville, or P. blainvilli are ever recorded, they should not be retained as senior synonyms of P. elegans Grube, 1840. If they are found, it might be better to regard P. blainvilli as a nomen oblitum, and P. elegans would be a nomen protectum (ICZN 1999, Art. 23.9).

Lepidasthenia digueti Gravier, 1905, reinstated

Lepidasthenia digueti Gravier, 1905a: 177-181; 1905c: 160-173, Textfigs 1-9; Fauvel, 1943: 4-5; Salazar-Silva, 2006: 150.

Diagnosis. Lepidasthenia with nuchal lappet crenate: median and posterior elytra slightly smaller than anterior ones, brown to blackish, non-transparent; neurochaetae unidentate, without giant chaetae.

Description. Syntypes (MNHN POLY TYPE 119, 120; USNM 51613) in poor condition, fragmented, with grayish pigmentation on ceratophores, tentaculophores and on elytral surface (Fig. 2A, C, E), anterior pigmentation faded off in another syntype (USNM 51613) (Fig. 3A); body with small blackish spots dorsally on anterior segments, darker along posterior segments.

Prostomium bilobed, wider than long; facial tubercle reduced. Two pairs of eyes, dark, rounded, of similar size, anterior eyes on widest prostomial area, dorsolateral, posterior eyes dorsal, near posterior prostomial margin (Figs. 2B, D, 3B). Median antenna with ceratophore thin, short, grayish, inserted frontally between prostomial lobes, ceratostyle thick, long, tapering in filiform tip, slightly longer than lateral ceratostyles. Lateral antennae with ceratophores thick, short, grayish, inserted terminally, ceratostyles thinner, long, taper in filiform tip. Palps thin, pale, long, tapered, tip filiform, surface smooth, non-papillate. Pharynx fully exposed in one syntype (MNHN POLY TYPE 119) (Fig. 2A), brownish, with 14 pairs of terminal papillae, and 2 subdistal lateral low tubercles.

Tentacular segment not visible dorsally. Tentaculophores, thick, short, without chaetae, not covered by elytrophores, tentacular cirri long, as long as antennae but thinner. Second segment projected on prostomium as a short nuchal lobe, margin crenate. First pair of elytrophores not expanded dorsally, with some scattered papillae.

Numerous elytra (number indeterminate due to condition of specimens); first elytra present in one syntype (Fig. 2E), slightly larger than following ones, apparently not completely covering anterior end; after pair 12 alternate with 2 dorsal cirri, on the posterior segments elytra alternate with 2 or 3 dorsal cirri. Elytra small, not overlapped middorsal, covering 2 adjacent segments. Elytral margins smooth, without fimbriae; anterior elytra surface with brown area diffuse mainly toward mid-dorsal line, posterior elytra with homogeneous pigmentation.

Parapodia biramous. Notopodia reduced to small lobes. Neuropodia long, thin, with prechaetal and postchaetal lobes rounded, of similar size. Dorsal tubercles absent, elytrophores small, rounded, not directed dorally. Dorsal cirri pale, smooth, cirrophores short, slightly swollen. Ventral cirri long, thick, tapered in filiform tip, cirrophore short, thick. Anterior segments with neuropodia with 3-4 fungiform ventral papilla (Fig. 3D); median and posterior chaetigers with neuropodia ventrally smooth (Fig. 3E). Nephridial papillae from segment 10.

Notochaetae absent. Neurochaetae with pectinate area variably modified along bundle; anterior chaetigers with lower neurochaetae with longer pectinate area (Fig. 3D, inset); median and posterior chaetigers with neurochaetal pectinate area decreasing in size ventrally (Fig. 3E, inset); pectinate area with series of long, petaloid spines; tips bidentate, main tooth short, accessory denticle shorter, almost completely fused to main tooth. No giant neurochaetae present.

Posterior region tapered (Figs 2F, 3F); pygidium with anus terminal, anal cirri short, ventral. 

Taxonomic summary

Type material. Syntypes of Lepidasthenia digueti Gravier, 1905 (MNHN POLY TYPE 119, 120; USNM 51613), La Paz, Baja California, Gulf of California, México, 1904, L. Diguet, coll.

Distribution. Only known from the Gulf of California, associated with an unidentified, intertidal balanoglossid hemichordate.

Remarks

Lepidasthenia digueti Gravier, 1905 is easily recognized as belonging to Lepidasthenia since the original description after the sequence of elytra in posterior segments being present every third segment, the lack of notochaetae, and the elongate neuropodial lobes. This is confirmed despite the fragmented condition of the type specimens. The crenate nuchal hood is very distinctive, although this was not included in the original description, together with the sequence of elytra and cirri along median segments.

The syntype specimens are all fragments, as originally indicated by Gravier (1905a: 179, 1905c: 163), but they include both body ends, and their features correspond to Lepidasthenia. After the type of sequence of elytra-dorsal cirri along median and posterior regions, and after the presence of apparently unidentate neurochaetae (accessory denticle minute), we confirm it belonging in Lepidasthenia. Lepidasthenia digueti belongs in the group of species having apparently unidentate neurochaetae, without giant chaetae, and without ventral papillae along neuropodial surface.

Solís-Weiss et al. (2004: S14) hesitated about the type status of the Paris Museum specimens, probably because they were fragments; we confirm the 2 Paris specimens and the one in Washington are all syntypes. It is enigmatic, however, how a syntype was sent to Washington; there are no indications in the catalogue card for the specimen about how it reached Washington, and it is likely that Dr. Marian Pettibone, after her long-time involvement with polynoid polychaetes, received it as a donation from the Paris museum. 

Read and Fauchald (2024a) have listed L. digueti in Lepidametria after Seidler (1923). This confusion has 2 explanations. First, Gravier (1905a: 180; 1905b: 166) indicated there was a non-exposed notopodial compact bundle of chaetae, but after the study of type specimens, Fauvel (1943: 4) explained they were fibers inserted close to acicular tips, and confirmed L. digueti was a true Lepidasthenia after the lack of notochaetae, but this conclusion was overlooked. Second, Seidler (1923: 258) studied one specimen from Charlestown, and he indicated the locality was in the Pacific coast of Central America. This is wrong. Charlestown is the capital of Nevis Island, in the archipelago of Saint-Kitts and Nevis, in the Caribbean Sea. His specimen might belong to a likely undescribed, western Atlantic species of Lepidametria.We think it is incorrect to incorporate an eastern Pacific species from one genus, into any other on the basis of specimens from a very different ocean basin, or without the study of type material.

The hemichordate was not described soon, as indicated by Gravier (1905a, c), and its identity remains unknown. The hemichordate could be Ptychodera flava Eschscholtz, 1825, a widely distributed species in the Indian and Pacific oceans (Uribe & Larrain, 1992).

Lepidonotinae Willey, 1902

Lepidametria Webster, 1879

Type species. Lepidametria commensalis Webster, 1879, by monotypy.

Diagnosis (after Salazar-Vallejo et al., 2015). Lepidonotinae with a long body with up to 80 segments. Elytrae large, covering body or leaving a narrow dorsal surface uncovered; posterior region with elytra and cirri alternating every other segment. Tentaculophores with chaetae. Notopodia reduced, with fine notochaetae at least along anterior and median segments, rarely absent. Neuropodia projecting with several types of neurochaetae. Ventral surface often papillated.

Remarks

As indicated by Pettibone (1953) and Salazar-Vallejo et al. (2015), Lepidametria differs from Lepidasthenia because it has notochaetae, and alternating elytra and cirri along median and posterior segments, whereas in Lepidasthenia there are no notochaetae, and elytra occur every third segment. The need for a redescription of the type material was indicated elsewhere (Salazar-Vallejo et al. 2015: 26). In a recent contribution (Salazar-Vallejo et al. 2015) we regarded Bouchiria Wesenberg-Lund, 1949, as a junior synonym of Lepidametria; it is a junior synonym but of Lepidasthenia, as indicated by Wehe (2006).

Read and Fauchald (2024) list 4 species in Lepidametria: L. brunnea Knox, 1960; L. commensalis, L. digueti (Gravier, 1905); and L. lactea (Treadwell, 1939). We have shown above that L. digueti belongs in Lepidasthenia, we regard L. brunnea as belonging in Lepidasthenia because it lacks notochaetae, and has elytra every 3 segments along posterior region, and we confirm Hartman (1951) synonymy of L. lactea with L. commensalis. Consequently, there would only be one species in Lepidametria (L. commensalis); however, we think that L. virens (Blanchard in Gay, 1849), and L. gigas (Johnson, 1897) also belong in this genus. A key to species is included below.

Lepidametria commensalis Webster, 1879

Figs. 4, 5

Lepidametria commensalis Webster, 1879: 209-212, Pl. 3, Figs. 23-31; Hartman, 1951: 17 (syn.); Pettibone, 1963: 19-20, Fig. 4k; Day, 1973: 6; Gardiner, 1976: 86-87, Fig. 1k-n.

Lepidasthenia lactea Treadwell, 1939: 3-5, Figs. 13-15. 

Diagnosis. Lepidametria with nuchal lappet smooth: median and posterior elytra slightly smaller than anterior ones, with dark spots, non-transparent; neurochaetae uni- and bidentate, with giant chaetae in median chaetigers.

Description. Syntypes of Lepidametria comensalis (USNM 527) include one beheaded specimen, better preserved (probably used for original description), and a complete specimen; description based on the complete soft syntype. Some parapodia and elytra already dissected (kept in container); no further dissections to avoid additional damage.

Body long, depressed, variably damaged, 70 mm long, 6 mm wide, 71 segments, dorsum with diffuse brownish intersegmental bands (Fig. 4A) [paratype of L. lactea (USNM 20420) 20 mm long, 64 segments; holotype of L. lactea (AMNH 2565) with 50 mm long, 2 mm wide, 62 segments, 34 pairs of elytra]. 

Prostomium bilobed, longer than wide, without facial tubercle (Fig. 4B). Eyes blackish, visible dorsally, small; anterior eyes in widest prostomial area. Median antenna lost, ceratophore cylindrical, long. Lateral antennae lost, on prostomial anterior extensions, ceratophores as long as median one. Palps massive, long, with papillae, tapered into fine tips.

Tentacular segment not visible dorsally; tentaculophores long, cirrostyles wide, 2 times as long as prostomium. Segment 2 with nuchal lappet; first pairs of parapodia and elytrophores perpendicular, not directed anteriorly; ventral cirri about 2 times as long as following ones. Without dorsal tubercles; elytrophores short. 

Elytra 44 pairs, subcircular, thin, transparent, smooth, without fimbriae (Fig. 4C), non-overlapping mid-dorsally, except posterior pair; after pair 12, most alternating with dorsal cirri; elytra pairs 12 and 13, and 14 and 15 contiguous (no dorsal cirri between them). Posterior region with elytra paired along 3-4 segments, then one elytrigerous, followed by one or 2-3 pairs of elytra.

Parapodia biramous, short, about as long as half body width (Fig. 4D). Dorsal cirri thick, short, not surpassing neuropodial tips, subdistally swollen, with long tips, with a brown band in widened area; cirrophore thick, short, swollen basally, inserted basally. Notopodia with notochaetae present along body, missing in far posterior chaetigers. Neuropodia with pre- and postchaetal lobes of similar size, prechaetal lobe lobulate along superior part, continuous along lower part, postchaetal lobe continuous, without acicular lobes. Ventral cirri short, thin, inserted medially in neuropodium. Nephridial lobes cylindrical, long, from segment 8.

Notochaetae scarce, smooth capillaries, not reaching neuropodial tips (Fig. 4D, inset). Neurochaetae most bidentate, a few unidentate, pectinate area slightly wider, rows of spines restricted to wider basal area. Median segments with a single giant unidentate neurochaeta, denticles minute (Fig. 4E, inset).

Posterior end tapered; anus terminal, anal cirri thin.

Variation. A smaller specimen (USNM 52842), mature female, has elytra overlapping completely along middorsum (Fig. 5A), transverse intersegmental bands visible. Prostomium pale, with ceratophores brownish (Fig. 5B); median antenna about 2 times as long as both prostomium and lateral antennae (left one in regeneration), ceratostyles barely swollen, darker than adjacent areas; palps thick, papillate, about 2 times as long as median antenna. Tentaculophores with cirrostyles slightly shorter than median antenna, right one with a single chaeta. Second segment with nuchal lappet.

Elytra oval, wider than long, with brown spots, including insertion areas (Fig. 5C). In posterior chaetigers, elytral sequence is 3 elytrigerous followed by one cirrigerous and then 3 other elytrigerous (Fig. 5D). Dorsal tubercles distinct in cirrigerous segments, at least along posterior region.

Cirrigerous parapodia with dorsal cirri barely swollen subdistally, with brown band, with more abundant notochaetae along anterior region (Fig. 5E), neurochaetae of similar width; posterior parapodia with less notochaetae, and upper giant spine; neurochaetae mostly bidentate, progressively unidentate dorsally (Fig. 5F, inset). Oocytes about 100 µm in diameter.

Two other specimens, complete (USNM 52840, 52841) have elytra overlapping laterally, but leaving a narrow middorsal area uncovered; dorsum with complex pigmentation pattern: the transverse bands are clearly on the posterior part of each segment, not intersegmental, and there is a wide, oval brownish spot along most dorsal surface of each segment, although it can be interrupted medially by a paler area. One specimen (USNM 52841) with pharynx partially exposed, jaws are brownish, and there are 10 upper and 11 lower terminal papillae. Giant neurochaetae from second third of body (chaetigers 23 of 71; 25 of 70 in USNM 52840). One specimen (USNM 52840) with nephridial lobes globose, truncate, from chaetiger 8. Posterior region tapered, anus terminal, anal cirri resembling dorsal cirri.

Another specimen (USNM 56533) rolled ventrally, elytra almost completely brownish, with pale spots in insertion area; posterior segments have 3 elytra in sequence.

Taxonomic summary

Type material. Two syntypes of Lepidametria commensalis (USNM 527), Virginia, USA, Sta. H458, H. E. Webster, coll. Holotype of Lepidasthenia lactea (AMNH 2565), Galveston, Texas, USA Paratype of L. lactea (USNM 20420), Galveston, Texas, USA, O. Sanders, coll. 

Additional material. One specimen (USNM 52840), Banks Channel, Wrightsville Beach, North Carolina, intertidal, in Amphitrite ornata tube, Mar. 1973, S.L. Gardiner, coll. (complete, bent laterally, pharynx partially exposed; body 70 mm long, 5 mm wide, chaetigers). One specimen (USNM 52841), Banks Channel, Wrightsville Beach, North Carolina, intertidal, in Amphitrite ornata tube, 8 Mar. 1974, S.L. Gardiner, coll. (pigmentation pattern indicated in variation; body 50 mm long, 4.5 mm wide, 71 chaetigers). One specimen (USNM 52842), mature female, without posterior end, intracoastal waterway, Wrightsville Beach, North Carolina, intertidal, in Amphitrite ornata tube, 5 Apr. 1974, T. Fox, coll. (pale, with elytra mottled; right elytra 1 and 3, and right parapodia of chaetigers 10 and 45 removed for observation (kept in container); body 66 mm long, 5 mm wide, 66 chaetigers). One specimen (USNM 56533), York River, Virginia, 29 Jul. 1977 (markedly bent ventrally, 2 posterior parapodia and many elytra detached (30 elytra and 2 parapodia in container); not measured for avoiding further damage).

Distribution. Virginia to Texas, USA, in shallow waters, associated with terebellid polychaetes, and with sponges (Dauer 1973).

Remarks

Webster (1879: 211) indicated that the sequence of elytra and cirri was asymmetrical in posterior chaetigers, such that one elytron could be on side, and one dorsal cirri on the other side. This was confirmed in the beheaded syntype, but this is not present in the other non-type specimens. Bergström (1916) noted this same anomaly in other long-bodied polynoids, and it has been recently reported for another species (Salazar-Vallejo, 2024).

Hartman (1951) regarded Lepidasthenia lactea Treadwell, 1939 as a junior synonym of L. commensalis Webster, 1879. The type specimens of L. lactea have a similar shape of prostomium, and share the same type of elytra, noto- and neurochaetae, but they are smaller, such that the specimens might be juveniles.

Webster (1879) found L. commensalis living in tubes of the terebellid Amphitrite ornata (Leidy, 1855), and Hartman (1951) found it living with Thelepus setosus (de Quatrefages, 1866), whereas L. lactea was found in different, unidentified terebellid tubes.

Key to species of Lepidametria Webster, 1879

1 Median and posterior elytra regularly alternating with dorsal cirri …………………… 2

– Median and posterior elytra not regularly alternating …………………… L. virens (Blanchard in Gay, 1849) Chile

2(1) Elytra present along body …………………… L. commensalis Webster, 1879 Northwestern Atlantic

– Elytra not reaching posterior end …………………… L. gigas (Johnson, 1897) California

Acknowledgments

The generous support by curators and collection managers is deeply acknowledged. Karen Osborn and Karen Reed currently, Linda Ward, the late Kristian Fauchald, formerly (USNM), Fredrik Pleijel and Tarik Meziane (MNHN). They all were and have been very supportive of our research activities and provided lab space and facilities for this study. Anabel León-Hernández and Daniel Pech provided some publications. The careful reading by two anonymous referees helped us to improve this final contribution. In her usual high standards, María Antonieta Arizmendi kindly took care of all the formatting issues for this publication. 

References

Amaral, A. C., & Nonato, E. F. (1982). Anelideos poliquetos da costa brasileira. Aphroditidae e Polynoidae. Brasilia: Conselho Nacional de Desenvolvimento Científico e Tecnológico.

Audouin, J. V., & Milne-Edwards, H. (1832). Classification des annélides, et description de celles qui habitent les côtes de la France. Annales des Sciences Naturelles, 27, 337–447. 

Audouin, J. V., & Milne-Edwards, H. (1834). Recherches pour servir à l’histoire naturelle du littoral de la France, ou recueil de mémoires sur l’anatomie, la physiologie, la classification et les mœurs des animaux de nos côtes (Vol. 2, Pt. 1). Paris: Crochard.

Barnich, R., & Fiege, D. (2003). The Aphroditoidea (Annelida: Polychaeta) of the Mediterranean Sea. Abhandlungen der Senckenbergischen Naturforschenden Gesellschaft, 559, 1–170.

Barnich, R., & Fiege, D. (2004). Revision of the genus Lepidastheniella Monro, 1924 (Polychaeta: Polynoidae: Lepidastheniinae) with notes on the subfamily Lepidastheniinae and the description of a new species. Journal of Natural History, 38, 863–876. https://doi.org/10.1080/0022293021000046432

Benham, W. B. (1901). Polychaet worms. In S. F. Harmer & A. E. Shipley (Eds.), The Cambridge natural history (Vol. 2). London: Macmillan. 

Bergström, E. (1916). Die Polynoiden der schwedischen Sudpolarexpedition 1901-1903. Zoologiska Bidrag från Uppsala, 4, 269–304. 

Brown, R. W. (1954). Scientific words: a manual of methods and a lexicon of materials for the practice of logotechnics. Baltimore: George W. King.

Chamberlin, R. V. (1919). The Annelida Polychaeta [Albatross Expeditions]. Memoirs of the Museum of Comparative Zoology at Harvard College, 48, 1–514. 

Dauer, D. M. (1973). Polychaete fauna associated with Gulf of Mexico sponges. Florida Scientist, 36, 193–196. 

Day, J. H. (1967). A monograph on the Polychaeta of South Africa. Part 1. Errantia (Vol. 656). London: British Museum (Natural History). 

Day, J. H. (1973). New Polychaeta from Beaufort, with a key to all species recorded from North Carolina. NOAA Technical Report, National Marine Fisheries Services Circular, 375, 1–153. 

De Blainville, H. M. D. (1828). Vers. Dictionnaire des Sciences Naturelles, 57, 365–625. https://www.biodiversitylibrary.org/page/25316888 [Atlas: https://www.biodiversitylibrary.org/page/24394694]

De Quatrefages, A. (1866). Histoire naturelle des Annelés marins et d‘eau douce. Annélides et Géphyriens (Vol. 2). Paris: Librairie Encyclopédique de Roret. 

Eschscholtz, F. (1825). Berich über die zoologisch Ausbeute der Reise von Kronstadt bis St. Peter und Paul. Isis von Oken, 1825.

Fauvel, P. (1917). Annélides polychètes de l’Australie méridionale. Archives de Zoologie Expérimentale et Générale, 56, 159–277. https://www.biodiversitylibrary.org/page/6322379

Fauvel, P. (1923). Polychètes errantes. Paris: Fédération Française des Sociétés de Sciences Naturelles. 

Fauvel, P. (1943). Annélides polychètes de Californie. Mémoires du Muséum National d’Histoire Naturelle, nouvelle série, 18, 1–32. https://www.biodiversitylibrary.org/page/59784292

Gardiner, S. L. (1976). Errant polychaete annelids from North Carolina. Journal of the Elisha Mitchell Scientific Society, 91, 78–220. 

Gay, C. (1849). Historia física y política de Chile, según documentos adquiridos en esta república durante doce años de residencia en ella. Zoología, Tomo 3, 9–52; Atlas 2, Pls. 1-3. Santiago: Museo de Historia Natural. https://www.biodiversitylibrary.org/page/16438163 [Atlas: https://www.biodiversitylibrary.org/page/55213605]

Gravier, C. (1905a). Sur un Polynoidien (Lepidasthenia digueti nov. sp.) commensal d’un Balanoglosse de Basse-Californie. Bulletin du Muséum d’Histoire Naturelle, Paris, 11, 177–184. 

Gravier, C. (1905b). Sur les genres Lepidasthenia Malmgren et Lepidametria Webster. Bulletin du Muséum d’Histoire Naturelle, Paris, 11, 181–184. 

Gravier, C. (1905c). Sur un polynoïden (Lepidasthenia digueti nov. sp.), commensal d’un balanoglosse de Basse-Californie. Bulletin de la Société Philomatique de Paris, neuvième série, 7, 160–173. 

Grube, A. E. (1840). Actinien, Echinodermen und Würmer des Adriatischen- und Mittelmeers nach eigenen Sammlungen beschrieben. J.H. Bon, Königsberg. https://www.biodiversitylibrary.org/page/10662919

Grube, E. (1870). Bemerkungen über anneliden des Pariser Museums. Archiv für Naturgeschichte, Berlin, 36, 281–352. 

Hartman, O. (1942). A review of the types of polychaetous annelids at the Peabody Museum of Natural History, Yale University. Bulletin of the Bingham Oceanographic Collection, Yale University, 8, 1–98. 

Hartman, O. (1951). The littoral marine annelids of the Gulf of Mexico. Publications of the Institute of Marine Science, Port Aransas, Texas, 2, 7–124.

Hartman, O. (1959). Catalogue of the polychaetous annelids of the world (Occasional paper No. 23). Los Angeles: Allan Hancock Foundation Publications.

Hartwich, G. (1993). Die Polychaeten-Typen des Zoologischen Museums in Berlin. Mitteilungen aus der Zoologischen Sammlung des Museums für Naturkunde in Berlin, 69, 73–154.

Horst, R. R. (1917). Polychaeta Errantia of the Siboga Expedition. Part Ii Aphroditidae and Chrysopetalidae. Siboga Expeditie, 24, 46–143. 

Imajima, M., & Hartman, O. (1964). The polychaetous annelids of Japan (Occasional paper No. 26). Los Angeles: Allan Hancock Foundation. 

International Commission on Zoological Nomenclature (ICZN). (1999). International Code of Zoological Nomenclature. Natural History Museum. https://code.iczn.org

Johnson, H. P. (1897). A preliminary account of the marine annelids of the Pacific Coast, with descriptions of new species. Proceedings of the California Academy of Sciences, 1, 153–194. 

Kinberg, J. G. H. (1856). Nya slägten och arter af Annelider. Öfversigt af Kongl. Vetenskaps-Akademiens Förhandlingar Stockholm, 12, 381–388. 

Knox, G. A. (1960). Biological results of the Chatham Islands 1954 Expedition. Part 3. Polychaeta errantia. New Zealand Department of Scientific and Industrial Research Bulletin, 139, 77–143. 

Leidy, J. (1855). Contributions towards a knowledge of the marine invertebrate fauna of the coasts of Rhode Island and New Jersey. Journal of the Academy of Natural Sciences of Philadelphia, 3, 135–152. 

Malmgren, A. J. (1867). Annulata Polychaeta Spetsbergiæ, Grœnlandiæ, Islandiæ et Scandinaviæ. Hactenus cognita. Helsingforsiae, Ex Officina Frenckelliana. 

Núñez, J., Barnich, R., Brito, M. C., & Fiege, D. (2015). Familias Aphroditidae, Polynoidae, Aceotidae, Sigalionidae y Pholoidae. Fauna Ibérica, 41, 89–257.

Núñez, J., Brito, M. C., & Ocaña, O. (1992). A new species of Lepidasthenia (Polychaeta: Polynoidae) from Canary Islands. Zoologica Scripta, 21, 347–349. https://doi.org/10.1111/j.1463-6409.1992.tb00336.x

Pettibone, M. H. (1953). Some scale-bearing polychaetes of Puget Sound and adjacent waters. Seattle, WA: University of Washington Press.

Pettibone, M. H. (1963). Marine polychaete worms of the New England region, 1. Families Aphroditidae through Trochochaetidae. Bulletin of the United States National Museum, 227, 1–356. 

Pettibone, M. H. (1970). Polychaeta Errantia of the Siboga Expedition. Part IV. Some additional polychaetes of the Polynoidae, Hesionidae, Nereidae, Goniadidae, Eunicidae, and Onuphidae, selected as new species by the late Dr. Hermann Augener with remarks on other related species. Siboga-Expeditie Uitkomsten op Zoologisch, Botanisch, Oceanographisch en Geologisch Gebied verzameld in Nederlandsch Oost-Indië 1899–1900. Siboga – Expedition, 24, 199–270.

Pettibone, M. H. (1989). A new species of Benhamipolynoe (Polychaeta: Polynoidae: Lepidastheniinae) from Australia, associated with the unattached stylasterid coral Conopora adeta. Proceedings of the Biological Society of Washington, 102, 300–304. 

Potts, F. A. (1910). The Percy Sladen Trust Expedition to the Indian Ocean in 1905, under the leadership of Mr. J. Stanley Gardiner: 12. Polychaeta of the Indian Ocean, 2. The Palmyridae, Aphroditidae, Polynoidae, Acoetidae and Sigalionidae. Transactions of the Linnean Society of London, Series 2, Zoology, 16, 325–353. 

Read, G., & Fauchald, K. (Eds.). (2024a). World polychaeta database. Lepidametria Webster, 1879. https://www.marinespecies.org/aphia.php?p=taxdetails&id=236705 (Retrieved on August 20^th, 2024).

Read, G., & Fauchald, K. (Eds.). (2024b). World polychaeta database. Lepidasthenia Malmgren, 1867. https://www.marinespecies.org/aphia.php?p=taxdetails&id=129495 (Retrieved on August 20^th, 2024).

Salazar-Silva, P. (2006). Scaleworms (Polychaeta: Polynoidae) from the Mexican Pacific and some other Eastern Pacific sites. Investigaciones Marinas, Valparaíso, 34, 143–161. 

Salazar-Vallejo, S. I. (2024). Barnichia crialesae gen. nov., sp. nov., from the western Atlantic (Annelida, Polychaeta, Polynoidae, Polynoinae). Bulletin of Marine Science, 100, 439–449. https://doi.org/10.5343/bms.2023.0103

Salazar-Vallejo, S. I., González, N. E., & Salazar-Silva, P. (2015). Lepidasthenia loboi sp. n. from Puerto Madryn, Argentina (Polychaeta, Polynoidae). Zookeys, 546, 21–37. https://doi.org/10.3897/zookeys.546.6175

Savigny, J. C. (1822). Système des annélides, principalement de celles des côtes de l’Égypte, et de la Sirie, offrant les caractères tant distinctifs que naturels des Ordres, Familles et Genres, avec la description des Espèces. Description de l’Égypte, Tome 1. Paris.

Seidler, H. J. (1923). Über neue und wenig bekannte Polychäten. Zoologischer Anzeiger, 61, 254–264. 

Seidler, H. J. (1924). Beiträge zur Kenntnis der Polynoiden 1. Archiv für Naturgeschichte, 89, 1–217. 

Solís-Weiss, V., Bertrand, Y., Helléouet, M. N., & Pleijel, F. (2004). Types of polychaetous annelids at the Muséum national d’Histoire naturelle, Paris. Zoosystema, 26, 377–384. 

Treadwell, A. L. (1937). The Templeton Crocker Expedition. 8. Polychaetous annelids from the west coast of Lower California, the Gulf of California and Clarion Island. Zoologica, Scientific Contributions of the New York Zoological Society, 22, 139–160. 

Treadwell, A. L. (1939). New polychaetous annelids from New England, Texas and Puerto Rico. American Museum Novitates, 1023, 1–7. 

Uribe, M. E., & Larraín, A. P. (1992). Estudios biológicos en el enteropneusto Ptychodera flava Eschscholtz, 1825 de Bahía Concepción, Chile. 1. Aspectos morfológicos y ecológicos. Gayana Zoología, 56, 141–180. 

Von Marenzeller, E. (1874). Zur Kenntnis der adriatischen Anneliden. Sitzungsberichte der Kaiserlichen Akademie der Wissenschaften, Mathematisch-Naturwissenschaftliche Classe, 69, 407–482. 

Von Marenzeller, E. (1876). Zur Kenntniss der adriatischen Anneliden. Zweiter Beitrag. (Polynoinen, Hesioneen, Syllideen). Sitzungsberichte der Kaiserlichen Akademie der Wissenschaften, Wien, Mathematisch-Naturwissenschaftliche Classe, 72, 129–171.

Webster, H. E. (1879). The Annelida Chaetopoda of the Virginian coast. Transactions of the Albany Institute, 9, 202–269. 

Wehe, T. (2006). Revision of the scale worms (Polychaeta: Aphroditoidea) occurring in the seas surrounding the Arabian Peninsula. 1. Polynoidae. Fauna of Arabia, 22, 23–197.

Wesenberg-Lund, E. (1949). Polychaetes of the Iranian Gulf. Danish Scientific Investigations in Iran, 4, 247–400.

Willey, A. (1902). Polychaeta. In B. Sharpe, & J. Bell (Eds.), Report on the Collections of Natural History made in the Antarctic Regions during the Voyage of the “Southern Cross (pp. 262–283). London: British Museum.

Karen Ayala-Galván ^a, *, José Manuel Gutiérrez-Salcedo ^a y Jose Ernesto Mancera-Pineda ^b

^a Instituto de Investigaciones Marinas y Costeras “José Benito Vives de Andréis”, Grupo de Investigación en Taxonomía, Sistemática y Ecología Marina, Calle 25 Núm. 2-55, Playa Salguero, Santa Marta D.T.C.H., Magdalena, Colombia

^b Universidad Nacional de Colombia, Grupo de Investigación en Modelación de Ecosistemas Costeros, Carrera 45 Núm. 26-85, Ciudad Universitaria, Teusaquillo, Bogotá D.C., Colombia

*Autor para correspondencia: ayalakarenc08@gmail.com (K. Ayala-Galván)

Resumen

Para las aguas oceánicas del Caribe colombiano existe un número limitado de publicaciones sobre la composición específica del fitoplancton, la mayoría es literatura gris. Hasta la fecha, se reportan para el Caribe colombiano 328 especies de diatomeas y 185 especies de dinoflagelados, que son principalmente registros en aguas neríticas. Con el fin de ampliar el conocimiento de la riqueza y aumentar el listado taxonómico existente en aguas oceánicas, se analizó la composición fitoplanctónica en la provincia oceánica del Caribe central colombiano, en un área estratégica que comprende 35,874 km², representa 7.5% de las aguas oceánicas y se ubica frente a la influencia del río Magdalena. Para esto, se recolectaron 108 muestras entre 2015 y 2017 con botellas Niskin a 10, 80 y 250 m, y arrastres verticales con redes de 20 µm de poro de malla en los primeros 50 m. Se identificaron 287 taxones pertenecientes a dinoflagelados, diatomeas, cianobacterias, clorofitas, silicoflagelados, cocolitofóridos, criptofitas, carofitas y bigiros, encontrando mayor riqueza de dinoflagelados (61.32%) y diatomeas (30.64%). El listado taxonómico comprende 184 especies, 74 nuevos registros para la cuenca del Caribe colombiano; se incrementa la composición específica para dinoflagelados en 27.03% y para diatomeas en 2.44%.

Palabras clave: Comunidad fitoplanctónica; Mesoescala; Zona oceánica; Listado taxonómico

Phytoplanktonic richness and new records of dinoflagellates, diatoms, coccolithophorids and bigyrids in oceanic waters of the Colombian Caribbean

Abstract

For the oceanic waters of the Colombian Caribbean there is a limited number of publications on the specific composition of phytoplankton, most of which are in gray literature. To date, 328 species of diatoms and 185 species of dinoflagellates have been reported for the Colombian Caribbean, mainly from neritic waters. In order to expand the knowledge of the richness and increase the existing taxonomic list in oceanic waters, the phytoplankton composition was analyzed in the oceanic province of the central Colombian Caribbean, in a strategic area that comprises 35,874 km², represents 7.5% of the oceanic waters and is located in front of the influence of the Magdalena River. For this, 108 samples were collected between 2015 and 2017 with Niskin bottles at 10, 80 and 250 m, and vertical trawls with 20 µm mesh pore nets in the first 50 m. A total of 287 taxa belonging to dinoflagellates, diatoms, cyanobacteria, chlorophytes, silicoflagellates, coccolithophorids, cryptophytes, carophytes and bygira were identified, finding greater richness of dinoflagellates (61.32%), and diatoms (30.64%). The taxonomic list includes 184 species, with 74 new records reported for the Colombian Caribbean basin, increasing the specific composition for dinoflagellates by 27.03% and for diatoms by 2.44%.

Keywords: Phytoplankton community; Mesoscale; Oceanic zone; Taxonomic listing

Introducción

El fitoplancton se ha estudiado a lo largo de la historia en diferentes lugares del mundo y se reconoce como el principal productor primario de los ambientes marinos. Sin embargo, su análisis es un reto debido a que es una comunidad dinámica y su composición, densidad y distribución pueden variar drásticamente con el tiempo, desde variabilidad decenal (Henson et al., 2009), interanual (Westberry et al., 2016), estacional (Holligan y Harbour, 1977), y hasta ciclos de marea (Davidson et al., 2013). A pesar de ser objetivo de muchas investigaciones, su conocimiento en las provincias neríticas y oceánicas de diferentes latitudes es muy irregular, lo que no es ajeno al mar Caribe colombiano. 

Ubicado en la parte más interna de la cuenca semicerrada del Caribe, el mar Caribe colombiano posee aguas de gran extensión, con 30,219 km² de aguas costeras y 501,935 km² de aguas oceánicas (INVEMAR, 2015). Estas últimas tienen un sistema complejo y se ven afectadas en la parte central por una convergencia de procesos como el clima, corrientes y giros marinos, eventos de surgencia, y un dominio costero que incide en las descargas continentales principalmente del río Magdalena, que dan lugar a la modificación de los reguladores ambientales y a la disposición de recursos, los cuales son determinantes en la composición, estructura y biomasa fitoplanctónica (Álvarez-León et al., 1995; Andrade y Barton, 2005; Bernal et al., 2006; Ricaurte-Villota y Bastidas-Salamanca, 2017).

La gran extensión de aguas oceánicas y los diferentes procesos que influyen en ellas dificultan operacionalmente los muestreos y aumentan los costos de estudio, éste es uno de los motivos por los cuales los análisis de fitoplancton marino se encuentran seccionados en diferentes áreas y se encuentran enfocados, principalmente, a una escala local (> 1 km) (Ávila-Silva, 2018; Ayala-Galván et al., 2017, 2018, 2021; Campos-González, 2007; Garay et al., 1988; Garrido-Linares, Alonso-Carvajal, Gutiérrez-Salcedo et al., 2014; Garrido-Linares, Alonso-Carvajal, Rueda et al., 2014; INVEMAR et al., 2017; INVEMAR-ANH, 2012; Ricaurte-Villota et al., 2018; Téllez et al., 1988; Vides y Alonso, 2016); con excepción de algunos análisis que se han realizado a gran escala (> 1,000 km) como los de INVEMAR-ANH (2008), INVEMAR-ANH (2010), Lozano-Duque et al. (2010a), Salón (2013) y Ayala-Galván y Gutiérrez-Salcedo (2019). Aunque los objetivos de estos estudios incluyen caracterizaciones, descripción de los atributos ecológicos e identificación de patrones espaciales o temporales, la información se encuentra restringida debido a que la mayoría de trabajos se encuentran en literatura gris, con algunas excepciones (Ayala-Galván et al., 2022; Garay et al., 1988; Lozano-Duque et al., 2010a). En este contexto, se ha identificado que la mayoría de trabajos del fitoplancton marino en aguas oceánicas provienen de estudios técnicos entre la alianza institucional entre el Instituto de Investigaciones Marinas y Costeras (INVEMAR) y la Agencia Nacional de Hidrocarburos (ANH) de Colombia, por lo que se espera dar mayor visibilidad a esta información, enfocando el objetivo de este trabajo en conocer la riqueza del fitoplancton marino en aguas oceánicas.

Materiales y métodos

El área de estudio comprende 27 sitios de muestreo que se encuentran ubicados en la provincia oceánica de la región central de la cuenca del Caribe colombiano, sobre el abanico sedimentario del Magdalena (Molina et al., 1994), frente al litoral costero comprendido entre los departamentos de Sucre y Magdalena. Tiene un área total de 35,874 km² con una distancia mínima de la costa de aproximadamente 20 km y máxima de 296 km y con una profundidad entre 400 y 4,500 m (fig. 1).

Para la recolecta de muestras y datos se realizaron 3 campañas de muestreo en los años 2015, 2016 y 2017, que para los análisis corresponden a sectores (tabla 1). En cada estación se realizó un arrastre vertical con una red cónica de 2.2 m de longitud, con diámetro de boca de 0.58 m y 20 µm de poro de malla (tabla 2). El material biológico recolectado se almacenó en contenedores de plástico de 500 ml y se fijó con formalina neutralizada con bórax (tetraborato de sodio) quedando una solución final concentrada al 4% (Boltovskoy, 1981). Adicionalmente, en cada estación se muestrearon 3 profundidades, de las cuales 2 pertenecen a la zona epipelágica (ep) y corresponden a las masas de agua: agua superficial del Caribe (ASC) y agua subsuperficial subtropical (ASS); y una pertenece a la zona mesopelágica (mp) que corresponde a la masa de agua ASS (tabla 2). Para ésto, se realizó el lance de una roseta oceanográfica equipada con botellas Niskin de 10 L de capacidad, de los cuales se almacenaron 800 ml de agua en contenedores de plástico forrados con vinipel negro (para evitar la penetración de la luz) y se les adicionó 8 ml de lugol ácido en proporción 1:100. 

Tabla 1

Coordenadas geográficas de las estaciones de muestreo de la comunidad fitoplanctónica en el Caribe central colombiano. Época climática (Pujos et al., 1986): inicio (+) final (–) foco (*).

Sector	Época	Estación	Fecha	Coordenadas decimales de la estación
			(día-mes-año)	Latitud	Longitud
Central	Lluvia (–) Seca (+)	409	19/11/2015	12.0833330	-74.12500000
		412	21/11/2015	12.4166670	-74.37500000
		414	22/11/2015	12.2500000	-74.62500000
		416	24/11/2015	12.0833330	-74.87500000
		418	25/11/2015	12.4166670	-74.87500000
		421	29/11/2015	11.9166670	-75.12500000
		425	01/12/2015	12.0833330	-75.37500000
		431	02/12/2015	11.7500000	-75.62500000
		433	12/12/2015	11.5833330	-75.87500000
Externo	Seca (–)	435	09/04/2016	12.9166670	-74.12500000
		437	10/04/2016	12.5833330	-74.12500000
		444	12/04/2016	12.5833330	-74.62500000
		446	14/04/2016	12.7500000	-74.87500000
		451	15/04/2016	12.4211390	-75.10350000
		456	17/04/2016	12.9166670	-75.37500000
		459	18/04/2016	12.7500000	-75.62500000
		462	19/04/2016	12.4166670	-75.87500000
		466	20/04/2016	12.0833330	-75.62500000
		467	21/04/2016	12.0833330	-75.87500000
Interno	Lluvia (*)	555	23/09/2017	11.3242194	-74.77517500
		557	24/09/2017	11.2579280	-75.31736700
		559	02/10/2017	11.9754720	-74.05918300
		561	03/10/2017	11.8466639	-74.39910556
		564	04/10/2017	11.9823806	-74.99378333
		566	07/10/2017	11.5472722	-75.18444444
		567	26/09/2017	11.7407390	-75.39539700
		570	08/10/2017	11.4804944	-75.83584722

Tabla 2

Información asociada a las 108 muestras en el área de estudio.

Año	Sector	Núm. de estaciones	Análisis	Método	Profundidad (metros)	Núm. de muestras
2015	Central	9	Cualitativo	Red	20 – 0 m	9
			Cuantitativo	Botella	ASC-ep (10 m)	27
					ASS-ep (80 m)
					ASS-mp (250 m)
2016	Externo	10	Cualitativo	Red	20 – 0 m	10
			Cuantitativo	Botella	ASC-ep (10 m)	30
					ASS-ep (80 m)
					ASS-mp (250 m)
2017	Interno	8	Cualitativo	Red	50 – 0 m	8
			Cuantitativo	Botella	ASC-ep (30m)	24
					ASS-ep (80m)
					ASS-mp (250m)

Las muestras de red se revisaron por alícuotas (0.125 ml) mediante una gráfica de morfoespecies acumulada (Ramírez, 1999). Las muestras de botella se revisaron con el método Utermöhl, que se encuentra detallado en el manual de fitoplancton de Edler y Elbrächter (2010). Las células se observaron en un microscopio invertido marca Leica Microsystems modelo DMi1, con objetivos de 20X, 40X y 63X, las fotografías se tomaron con una cámara Leica Microsystems MC120 HD y fueron procesadas con el software de adquisición de imágenes LAS EZ. La identificación se realizó por morfología al nivel más bajo posible siguiendo las claves taxonómicas de Cupp (1943), Wood (1963), Taylor (1976), Balech (1988), Round (1990), Tomas (1997), Vidal (2010), Hoppenrath et al. (2009), entre otras. La información taxonómica se tabuló y actualizó siguiendo la nomenclatura de la base de datos mundial de algas AlgaeBase (Guiry y Guiry, 2025). Luego de la identificación y análisis, todas las muestras biológicas se depositaron en la colección de plancton del Museo de Historia Natural Marina de Colombia MAKURIWA. 

Con el fin de generar una descripción completa a nivel de composición, se unificaron las matrices de presencia de las muestras con red y de botellas Niskin. Se realizó una descripción general de las categorías taxonómicas encontradas y de la riqueza a nivel horizontal. Así mismo, se describió la riqueza por grupo fitoplanctónico y solo en el caso de los 2 géneros más representativos (Tripos Bory, 1823 y Chaetoceros Ehrenberg, 1844) se detalló la variación horizontal. Además, se mencionan las especies frecuentes y raras para el área de estudio. Finalmente, al inventario se le realizó la verificación de registros nuevos de especies basados en listados previos para el Caribe colombiano.

La riqueza de especies (S) se calculó con el programa Primer V7 (Clarke y Gorley, 2015) y las salidas gráficas con el programa Ocean Data View, a las que se les realizó una interpolación de variación de datos DIVA (Schlitzer, 2022). Para esta última se consideró cada estación como una réplica aleatoria, teniendo en cuenta que, las características conservativas que separan las masas de agua oceánicas del Caribe central colombiano se dan de forma estratificada (Dorado-Roncancio et al., 2022).

Resultados

Mediante los muestreos con redes y botellas Niskin, en el Caribe central colombiano se registraron en total 287 taxones fitoplanctónicos, que se distribuyeron en 90 géneros, 60 familias, 37 órdenes, 13 clases y 8 phyla (Dinoflagellata, Heterokontophyta, Cyanobacteria, Chlorophyta, Haptophyta, Cryptista, Charophyta y Bigyra). El listado taxonómico se encuentra detallado en la tabla 3; 89% de las identificaciones se llevó a los 2 niveles taxonómicos más bajos, 64% se identificó a nivel de especie (184 taxones) y 25% a género (71 taxones), mientras que otro 11% estuvo en los demás niveles (32 taxones).

El número de taxones por estación osciló entre 74 y 149. Las mayores riquezas se registraron en las estaciones paralelas y más cercanas a la costa (570, 561, 566, 557, 559, 555), se reconocieron entre 130 y 149 taxones, y se observaron menores riquezas en las estaciones centrales ubicadas al oriente (418, 414, 416, 412, 421), con 74 a 88 taxones (fig. 2).

De los grupos fitoplanctónicos hallados en el Caribe central colombiano, los dinoflagelados y las diatomeas representaron 91.98% de la riqueza total. Los dinoflagelados mostraron mayor riqueza con 61.32% (S = 176), seguido de las diatomeas con 30.66% (S = 88). Con menores riquezas se encontraron las cianobacterias con 4.53% (S = 13), las clorofitas con 1.39% (S = 4), los silicoflagelados con 0.70% (S = 2), mientras que las carofitas, criptofitas, cocolitofóridos y bigiros, presentaron cada uno, una riqueza de 0.35% (S = 1). 

El género con mayor riqueza fue Tripos Bory, 1823 del grupo de los dinoflagelados con 14.29% (S = 41), éste presentó por estación entre 8 y 22 taxones y horizontalmente mostró un aumento de riqueza hacia aguas más oceánicas (fig. 3A). Seguido, se encontró Chaetoceros Ehrenberg, 1844 del grupo de las diatomeas con 7.32% (S = 21), que presentó por estación entre 1 y 6 taxones y horizontalmente mostró una disminución de riqueza hacia aguas más oceánicas (fig. 3B). Otros géneros con riquezas representativas incluyeron a los dinoflagelados Protoperidinium Bergh, 1881con 3.83% (S = 11), Ornithocercus Stein, 1883 con 3.14% (S = 9), Prorocentrum Ehrenberg, 1834 con 3.14% (S = 9), Phalacroma F. Stein, 1883 con 2.79% (S = 8), Histioneis Stein, 1883con 2.79% (S = 8), Dinophysis Ehrenberg, 1839 con 2.79%(S = 8) y las diatomeas Rhizosolenia Brightwell, 1858 nom. et typ. cons., con 2.79% (S = 8), los demás géneros mostraron riquezas inferiores a 2%.

Con una frecuencia superior a 80%, en las estaciones se registraron las especies de diatomeas: Asterolampra marylandica Ehrenberg, 1844 (fig. 4A), Cerataulina pelágica (Cleve) Hendey, 1937 (fig. 4B), Chaetoceros lorenzianus Grunow, 1863, C. peruvianus Brightwell, 1856, Hemiaulus hauckii Grunow ex Van Heurck, 1882 (fig. 4C), H. chinensis Greville, 1865, Pseudosolenia calcar-avis (Schultze) B.G. Sundström, 1986, Thalassionema frauenfeldii (Grunow) Tempère et Peragallo, 1910; los dinoflagelados: Ornithocercus magnificus F. Stein, 1883 (fig. 4D), Oxytoxum laticeps J. Schiller, 1937, Podolampas elegans F. Schütt, 1895, P. palmipes F. Stein, 1883, Prorocentrum compressum (Bailey) T.H. Abé ex J.D. Dodge, 1975, Pyrocystis lunula (F. Schütt) F. Schütt, 1896 (fig. 4E), P. pseudonoctiluca Wyville-Thompson, 1876, Tripos extensus (Gourret) F. Gómez, 2021, T. setaceus (Jørgesen) F. Gómez, 2013, T. teres (Kofoid) F. Gómez, 2013, T. trichoceros (Ehrenberg) Gómez, 2013, Karlodinium sp. J. Larsen, 2000, Gyrodinium sp. Kofoid et Swezy, 1921, nom. cons. y el silicoflagelado Dictyocha fibula Ehrenberg, 1839 (fig. 4F).

Tabla 3

Listado taxonómico y autoridades del fitoplancton marino encontrado en aguas oceánicas del Caribe central colombiano. * Nuevo registro de especie; ** nuevo registro de género; + nuevo registro de categorías superiores (familia, orden, clase, phylum). BT, Recolectada en muestra de botella; RD, recolectada en muestra de red. ^, Estatus taxonómico sin resolver.

Tabla 3 Listado taxonómico y autoridades del fitoplancton marino encontrado en aguas oceánicas del Caribe central colombiano. * Nuevo registro de especie; ** nuevo registro de género; + nuevo registro de categorías superiores (familia, orden, clase, phylum). BT, Recolectada en muestra de botella; RD, recolectada en muestra de red. ^, Estatus taxonómico sin resolver.

Diatomeas céntricas

Asterolampra marylandica Ehrenberg, 1844 | BT | RD

Asteromphalus elegans Greville, 1859 * | BT | RD

Asteromphalus heptactis (Brébisson) Ralfs, 1861 | RD

Bacteriastrum delicatulum Cleve, 1897 | BT | RD

Cerataulina bicornis (Ehrenberg) Hasle, 1985 * | RD

Cerataulina pelagica (Cleve) Hendey, 1937 | BT | RD

Chaetoceros affinis Lauder, 1864 | BT | RD

Chaetoceros atlanticus Cleve, 1873 | BT

Chaetoceros coarctatus Lauder, 1864 | BT | RD

Chaetoceros curvisetus Cleve, 1889 | BT | RD

Chaetoceros dadayi Pavillard, 1913 * | BT | RD

Chaetoceros danicus Cleve, 1889 | BT

Chaetoceros decipiens Cleve, 1873 | BT | RD

Chaetoceros didymus Ehrenberg, 1845 | BT

Chaetoceros diversus Cleve, 1873 | BT | RD

Chaetoceros laciniosus F. Schütt, 1895 | BT | RD

Chaetoceros lorenzianus Grunow, 1863 | BT | RD

Chaetoceros messanensis Castracane, 1875 | BT

Chaetoceros peruvianus Brightwell, 1856 | BT | RD

Climacodium frauenfeldianum Grunow, 1868 * | RD

Coscinodiscus gigas Ehrenberg, 1841| RD

Dactyliosolen blavyanus (H. Peragallo) Hasle, 1975 * | BT | RD

Dactyliosolen mediterraneus (H. Peragallo) H. Peragallo, 1892 | BT

Eucampia cornuta (Cleve) Grunow, 1883 | BT

Guinardia cylindrus (Cleve) Hasle, 1996 | BT | RD

Guinardia flaccida (Castracane) H. Peragallo, 1892 | BT | RD

Guinardia striata (Stolterfoth) Hasle, 1996 | BT | RD

Hemiaulus hauckii Grunow ex Van Heurck, 1882 | BT | RD

Hemiaulus membranaceus Cleve, 1873 | BT | RD

Hemiaulus chinensis Greville, 1865 | BT | RD

Leptocylindrus danicus Cleve, 1889 | BT | RD

Melosira inflexa (Roth) Guiry, 2019 | BT | RD

Neocalyptrella robusta (G. Norman ex Ralfs) Hernández-Becerril et Meave, 1997 | BT | RD

Planktoniella sol (G. C. Wallich) Schütt, 1892 | BT | RD

Pseudoguinardia recta Stosch, 1986 * | BT | RD

Pseudosolenia calcar-avis (Schultze) B. G. Sundström, 1986 | BT | RD

Rhizosolenia clevei Ostenfeld, 1902 | BT | RD

Rhizosolenia debyana H. Peragallo, 1892 * | RD

Skeletonema costatum (Greville) Cleve, 1873 | BT | RD

Trieres chinensis (Greville) Ashworth et E. C. Theriot, 2013 | RD

Cyclotella sp. (Kützing) Brébisson, 1838, nom. et typ. cons. | BT

Lithodesmium sp.Ehrenberg, 1839 | BT | RD

Bacteriastrum spp. Shadbolt, 1853 | BT | RD

Chaetoceros spp. Ehrenberg, 1844 | BT | RD

Coscinodiscus spp. Ehrenberg, 1839, nom. et typ. cons. | BT | RD

Proboscia spp. Sundström, 1986 | BT | RD

Rhizosolenia spp. Brightwell, 1858, nom. et typ. cons. | BT | RD

Diatomeas pennadas

Asterionellopsis glacialis (Castracane) Round, 1990 | BT | RD

Cylindrotheca closterium (Ehrenberg) Reimann et J. C. Lewin, 1964 | BT | RD

Haslea wawrikae (Husedt) Simonsen, 1974 | BT | RD

Lioloma pacificum (Cupp) Hasle, 1996 | BT | RD

Mastogloia rostrata (Wallich) Hustedt, 1933 * | BT | RD

Thalassionema frauenfeldii (Grunow) Tempère et Peragallo, 1910 | BT | RD

Thalassionema nitzschioides (Grunow) Mereschkowsky, 1902 | BT | RD

Diploneis sp. Ehrenberg ex Cleve, 1894 | BT

Fragilaria sp. Lyngbye, 1819 | BT | RD

Gyrosigma sp. Hassall, 1845, nom. cons. | BT

Pseudo-nitzschia sp. H. Peragallo, 1900 | BT | RD

Tryblionella sp. W. Smith, 1853 | BT

Haslea sp. Simonsen, 1974 | BT | RD

Navicula spp. Bory, 1822 | BT | RD

Nitzschia spp. Hassall, 1845, nom. cons. | BT | RD

Dinoflagelados tecados

Amphisolenia bidentata B. Schröder, 1900 | RD

Amphisolenia bifurcata G. Murray et Whitting, 1899 | RD

Amphisolenia globifera F. Stein, 1883 | RD

Amphisolenia schauinslandii Lemmermann, 1899 * | BT | RD

Amphisolenia schroederi Kofoid, 1907 * | RD

Centrodinium maximum Pavillard, 1930 * | ** | RD

Centrodinium punctatum (Cleve) F. J. R. Taylor, 1976 * | ** | RD

Ceratocorys armata (Schütt) Kofoid, 1910 | RD

Ceratocorys horrida Stein, 1883 | RD

Citharistes apsteinii F. Schütt, 1895 * | RD

Citharistes regius Stein, 1883 * | RD

Cladopyxis brachiolata F. Stein, 1883 | RD

Corythodinium biconicum (Kofoid) F. J. R. Taylor, 1976 * | BT | RD

Corythodinium constrictum (F. Stein) F. J. R. Taylor, 1976 * | BT | RD

Corythodinium milneri (G. Murray et Whitting) F. Gómez, 2017 | BT | RD

Corythodinium tesselatum (F. Stein) Loeblich Jr. et Loeblich III, 1966 * | BT | RD

Corythodinium robustum (Kofoid et J. R. Michener) F. Gómez, 2017 * | RD

Dinophysis apicata (Kofoid et Skogsberg) Abé, 1967 * | RD

Dinophysis capitulata Balech, nom. inválido. 1967 ^ | RD

Dinophysis exigua Kofoid et Skogsberg, 1928 * | BT | RD

Dinophysis hastata F. Stein, 1883 | RD

Dinophysis hindmarchii (G. Murray et Whitting) Balech, 1967 * | RD

Dinophysis ovum F. Schütt, 1895 * | RD

Dinophysis parvula (F. Schütt) Balech, 1967 * | BT | RD

Dinophysis schuettii G. Murray et Whitting, 1899 * | BT | RD

Dinophysis caudata Kent, 1881 | RD

Gonyaulax birostris Stein, 1883 * | BT | RD

Gonyaulax pacifica Kofoid, 1907 * | RD

Histioneis biremis F. Stein, 1883 * | RD

Histioneis costata Kofoid et J. R. Michener, 1911 * | RD

Histioneis crateriformis Stein, 1883 * | RD

Histioneis depressa J. Schiller, 1928 * | RD

Histioneis longicollis Kofoid, 1907 * | RD

Histioneis mediterranea J. Schiller, 1928 * | RD

Histioneis milneri G. Murray et Whitting, 1899 * | RD

Histioneis paraformis (Kofoid et Skogsberg) Balech, 1971 * | RD

Ornithocercus carolinae Kofoid, 1907 * | RD

Ornithocercus heteroporus Kofoid, 1907 | RD

Ornithocercus magnificus F. Stein, 1883 | BT | RD

Ornithocercus quadratus Schütt, 1900 | RD

Ornithocercus skogsbergii T. H. Abé, 1967 * | RD

Ornithocercus splendidus F. Schütt, 1892 | RD

Ornithocercus steinii Schütt, 1900 | RD

Ornithocercus thumii (A. W. F. Schmidt) Kofoid et Skogsberg, 1928 | RD

Oxytoxum elongatum E. J. F. Wood, 1963 * | BT | RD

Oxytoxum laticeps J. Schiller, 1937 * | BT

Oxytoxum mitra (F. Stein) Schröder, 1906 * | BT | RD

Oxytoxum sceptrum (F. Stein) Schröder, 1900 * | BT | RD

Oxytoxum scolopax F. Stein, 1883 | BT | RD

Phalacroma circumcinctum Kofoid et J. R. Michener, 1911 * | RD

Phalacroma cuneus F.Schütt, 1895 | RD

Phalacroma doryphorum F. Stein, 1883 | BT | RD

Phalacroma expulsum (Kofoid et J. R. Michener) Kofoid et Skogsberg, 1928 * | RD

Phalacroma mitra F. Schütt, 1895 | RD

Phalacroma oxytoxoides (Kofoid) F. Gomez, P. Lopez-Garcia et D. Moreira, 2011 | BT | RD

Phalacroma rapa F. Stein, 1883 | RD

Phalacroma scrobiculatum (Balech) Díaz-Ramos et G. J. Estrella, 2000 * | RD

Podolampas bipes F. Stein, 1883 | RD

Podolampas elegans F. Schütt, 1895 | BT | RD

Podolampas palmipes F. Stein, 1883 | BT | RD

Podolampas reticulata Kofoid, 1907 | RD

Podolampas spinifera Okamura, 1912 | BT | RD

Prorocentrum compressum (Bailey) T. H. Abé ex J. D. Dodge, 1975 | BT | RD

Prorocentrum concavum Y. Fukuyo, 1981 * | BT | RD

Prorocentrum dentatum F. Stein, 1883 | BT

Prorocentrum micans Ehrenberg, 1834 | RD

Prorocentrum rostratum F. Stein, 1883 * | BT

Protoperidinium cf. cassum (Balech) Balech, 1974 | RD

Protoperidinium cf. oviforme (P. J. L. Dangeard) Balech, 1974 | RD

Protoperidinium cf. sphaeroideum (Mangin) Balech, 1974 | RD

Protoperidinium elegans (Cleve) Balech, 1974 | RD

Protoperidinium oceanicum (Vanhöffen) Balech, 1974 | RD

Pyrocystis fusiformis C. W. Thomson, 1876 | RD

Pyrocystis hamulus var. Inaequalis Schröder, 1906 | RD

Pyrocystis lanceolata Schröder, 1900 * | RD

Pyrocystis lunula (F. Schütt) F. Schütt, 1896 * | BT | RD

Pyrocystis pseudonoctiluca Wyville-Thompson, 1876 * | BT | RD

Pyrocystis robusta Kofoid, 1907 | RD

Pyrophacus steinii (Schiller) Wall et Dale, 1971 | RD

Schuettiella mitra (Schütt) Balech, 1988 * | ** | RD

Spiraulax jolliffei (G. Murray y Whitting) Kofoid, 1911 | RD

Triadinium polyedricum (Pouchet) J. D. Dodge, 1981 | RD

Tripos arcuatus (Gourret) F. Gómez, 2021 | RD

Tripos arietinus (Cleve) F. Gómez, 2021 | RD

Tripos azoricus (Cleve) F. Gómez, 2013 | BT | RD

Tripos belone (Cleve) F. Gómez, 2021 | RD

Tripos bigelowii (Kofoid) F. Gómez, 2013 | RD

Tripos brevis (Ostenfeld et Johannes Schmidt) F. Gómez, 2021 | RD

Tripos candelabrum (Ehrenberg) F. Gómez, 2013 | RD

Tripos carriensis (Gourret) Hallegraeff et Huisman, 2013 | BT | RD

Tripos dens (Ostenfeld et Johannes Schmidt) F. Gómez, 2013 | RD

Tripos digitatus (F.Schütt) F. Gómez, 2013 | RD

Tripos extensus (Gourret) F. Gómez, 2021 | RD

Tripos falcatus (Kofoid) F. Gómez, nom. inval. 2013 ^ | RD

Tripos furca (Ehrenberg) F. Gómez, 2013 | BT | RD | RD

Tripos fusus (Ehrenberg) F. Gómez, 2013 | BT | RD

Tripos geniculatus (Lemmermann) F. Gómez, 2021 | RD

Tripos gibberus (Gourret) F. Gómez, 2021 | RD

Tripos gracilis (Pavillard) F. Gómez, 2013 | RD

Tripos gravidus (Gourret) F. Gómez, 2013 | RD

Tripos hexacanthus (Gourret) F. Gómez, 2013 | RD

Tripos inflatus (Kofoid) F. Gómez, 2013 | RD

Tripos karstenii (Pavillard) F. Gómez, 2021 | RD

Tripos lanceolatus (Kofoid) F. Gómez, 2013 * | RD

Tripos limulus (Pouchet) F. Gómez, 2021 | RD

Tripos longirostrum (Gourret) Hallegraeff et Huisman 2020 | RD

Tripos lunula (Schimper ex Karsten) F. Gómez, 2013 | RD

Tripos macroceros (Ehrenberg) Hallegraeff et Huisman, 2020 | BT | RD

Tripos massiliensis (Gourret) F. Gómez, 2021 | RD

Tripos muelleri Bory, 1826 | RD

Tripos pentagonus (Gourret) F. Gómez, 2021 | BT | RD

Tripos pulchellus (Schröder) F. Gómez, 2021 | RD

Tripos ranipes (Cleve) F. Gómez, 2013 | RD

Tripos reflexus (Cleve) F. Gómez, 2013 | RD

Tripos robustus (Ostenfeld et Johannes Schmidt) F. Gómez, 2021 | RD

Tripos schroeteri (B.Schröder) F. Gómez, 2013 * | RD

Tripos setaceus (Jørgesen) F. Gómez, 2013 | BT | RD

Tripos tenuis (Ostenfeld et Johannes Schmidt) Hallegraeff et Huisman, 2020 | RD

Tripos teres (Kofoid) F. Gómez, 2013 | BT | RD

Tripos trichoceros (Ehrenberg) Gómez, 2013 | BT | RD

Tripos volans (Cleve) F. Gómez, 2021 | RD

Tripos vultur Cleve, 1900 | RD

Alexandrium sp. Halim, 1960 | RD

Blepharocysta sp. Ehrenberg, 1873 | RD

Heterocapsa sp. F. Stein, 1883 | BT | RD

Scrippsiella sp. Balech, 1965, nom. cons. | BT | RD

Amphidoma sp. F. Stein, 1883 ** | BT | RD

Azadinium spp. Elbrächter et Tillmann, 2009 ** | BT | RD

Prorocentrum spp. Ehrenberg, 1834 | BT | RD

Ornithocercus spp. Stein, 1883 | RD

Protoperidinium spp. Bergh, 1881 | BT | RD

Gonyaulax spp. Diesing, 1866 | BT | RD

Tripos sp. Bory, 1823 | RD

Dinoflagelados atecados

Asterodinium gracile Sournia, 1972 * | BT

Brachidinium capitatum F. J. R. Taylor, 1963 * | ** | BT

Ceratoperidinium margalefii A. R. Loeblich III, 1980 * | ** | BT

Karenia papilionacea A. J. Haywood et K. A. Steidinger, 2004 * | BT

Kofoidinium pavillardii J. Cachon et M. Cachon, 1967 * | ** | RD

Pronoctiluca spinifera (Lohmann) Schiller, 1932 | BT

Pseliodinium fusus (F. Schütt) F. Gómez, 2018 | BT

Torodinium robustum Kofoid et Swezy, 1921 * | BT

Torodinium teredo (Pouchet) Kofoid et Swezy, 1921 * | BT

Gyrodinium sp. Kofoid et Swezy, 1921, nom. cons. | BT

Karlodinium sp. J. Larsen, 2000 ** | BT

Cucumeridinium spp. F. Gómez, P. López-García, H. Takayama et  D. Moreira, 2015 ** | RD

Karenia spp. Gert Hansen et Moestrup, 2000 | BT | RD

Kofoidinium sp. Pavillard, 1929 ** | BT

Cianobacterias

Merismopedia elegans A. Braun ex Kützing, 1849 | RD

Oscillatoria limosa C. Agardh ex Gomont, 1892 | RD

Richelia intracellularis J. Schmidt, 1901 | BT | RD

Komvophoron sp. Anagnostidis et Komárek, 1988 | RD

Planktothrix sp. Anagnostidis et Komárek, 1988 | RD

Pseudanabaena sp. Lauterborn, 1915 | RD

Trichodesmium sp. Ehrenberg ex Gomont, 1892, nom. cons. | BT | RD

Clorófitas

Pyramimonas longicauda L.Van Meel, 1969 | BT

Tetradesmus lagerheimii M. J. Wynne et Guiry, 2016 | RD

Desmodesmus sp. (Chodat) S. S. An, T.Friedl et E. Hegewald, 1999 | BT | RD

Pediastrum sp. Meyen, 1829 | RD

Silicoflagelados

Dictyocha fibula Ehrenberg, 1839 | BT | RD

Octactis octonaria (Ehrenberg) Hovasse, 1946 | BT | RD

Carófita

Staurastrum sp. Meyen ex Ralfs, 1848 | RD

Cocolitofórido

Scyphosphaera apsteinii Lohmann, 1902 * | BT | RD

Criptófita

Cryptomonadaceae Ehrenberg, 1831 | BT

Bigiro

Solenicola setigera Pavillard, 1916 * | ** | + | BT

Por su parte, se registraron 36 taxones raros (registrados en una sola estación) dentro de los que se encuentran los dinoflagelados Amphisolenia bifurcata G. Murray et Whitting, 1899, Brachidinium capitatum F.J.R. Taylor, 1963, Centrodinium maximum Pavillard, 1930, Ceratoperidinium margalefii A.R. Loeblich III, 1980, Citharistes apsteinii F. Schütt, 1895, Corythodinium robustum (Kofoid et J.R. Michener) F. Gómez, 2017, Dinophysis hastata F. Stein, 1883 (fig. 5A), Histioneis biremis F. Stein, 1883, H. crateriformis Stein, 1883, Phalacroma circumcinctum Kofoid et J.R. Michener, 1911, Phalacroma mitra F. Schütt, 1895 (fig. 5B), Prorocentrum rostratum F. Stein, 1883, Pyrocystis lanceolata Schröder, 1900, Tripos arietinus (Cleve) F. Gómez, 2021 (fig. 5C), T. belone (Cleve) F. Gómez, 2021, T. bigelowii (Kofoid) F. Gómez, 2013 (fig. 5D), T. digitatus (F. Schütt) F. Gómez, 2013, T. lanceolatus (Kofoid) F. Gómez, 2013, T. longirostrum (Gourret) Hallegraeff et Huisman, 2020, Kofoidinium sp. Pavillard, 1929, 2 morfoespecies del género Cucumeridinium F. Gómez, P. López-García, H. Takayama et D. Moreira, 2015, y 3 taxones posiblemente del orden Gymnodiniales; también se encontraron las diatomeas Cerataulina bicornis (Ehrenberg) Hasle, 1985, Chaetoceros messanensis Castracane, 1875 (fig. 5E), Trieres chinensis (Greville) Ashworth et E.C. Theriot, 2013 (fig. 5F), Gyrosigma sp. Hassall, 1845, nom. cons.;las cianobacterias Merismopedia elegans A. Braun ex Kützing, 1849, Planktothrix sp. Anagnostidis et Komárek, 1988, Pseudanabaena sp. Lauterborn, 1915, Komvophoron sp. Anagnostidis et Komárek, 1988; las clorofitas Tetradesmus lagerheimii M.J. Wynne et Guiry, 2016,y Pediastrum sp. Meyen, 1829y la carofita Staurastrum sp. Meyen ex Ralfs, 1848.

Con la revisión de los listados de Lozano-Duque et al. (2010b, 2011) y los trabajos publicados posteriormente por Lozano-Duque et al. (2010a), Vidal y Lozano-Duque (2011), Dimar-CIOH (2011), Ayala et al. (2011), Hoyos-Acuña et al. (2019), De la Hoz y Betancur (2019) y Córdoba-Mena et al. (2020) se calcularon en total 328 especies de diatomeas y 185 especies de dinoflagelados; se identificaron en el presente trabajo 74 registros nuevos para el Caribe colombiano que corresponden a 50 especies y 9 géneros de dinoflagelados, 8 especies de diatomeas, 1 especie de cocolitofóridos y 1 phylum, 1 clase, 1 orden , 1 familia, 1 género y 1 especie de bigiros (tabla 3; fig. 6). Se encontró que los géneros con mayor número de nuevos registros para el Caribe colombiano fueron Histioneis Stein, 1883 con 8 especies (fig. 7A-H), Dinophysis Ehrenberg, 1839con 6 especies, Corythodinium Loeblich et A.R. Loeblich, 1966; Oxytoxum Stein, 1883 y Phalacroma F. Stein, 1883con 4 especies cada uno, Pyrocystis Wyville-Thompson, 1876con 3 especies y Tripos (Ehrenberg) F. Gómez, 2013; Torodinium Kofoid et Swezy, 1921; Ornithocercus Stein, 1883; Gonyaulax Diesing, 1866; Citharistes Stein, 1883; Prorocentrum Ehrenberg, 1834; Centrodinium Kofoid, 1907y Amphisolenia Stein, 1883con 2 especies cada uno.

Discusión

La composición específica de las masas de agua reflejó las condiciones del medio, mostrando a las diatomeas y a los dinoflagelados como los grupos representativos, estos últimos los que presentaron mayor riqueza de especies. Estos 2 grupos fitoplanctónicos son dominantes en el mar Caribe y en el Caribe colombiano (Lozano-Duque, Medellín-Mora et al., 2010; Lozano-Duque et al., 2011; Okolodkov, 2003). Las especies de dinoflagelados son consideradas comunes en aguas oceánicas (Okolodkov, 2003), ya que gracias a su fisiología presentan bajos requerimientos de nutrientes y una nutrición variada (autótrofa, heterótrofa y mixotrófica), que les permite adaptarse a aguas oligotróficas (Gamboa-Márquez et al., 1994; Licea et al., 1995), como son las aguas oceánicas del Caribe colombiano (Corredor, 1979); por su riqueza y distribución, reflejan su adaptación a las condiciones del mar abierto (López y Caballero, 1997; Margalef, 1969). Así mismo, diferentes trabajos lo han reportado como el grupo dominante en aguas oceánicas del Caribe colombiano (Ayala-Galván et al., 2018, 2021; Garrido-Linares, Alonso-Carvajal, Rueda et al., 2014; INVEMAR et al., 2017; Lozano-Duque et al., 2010a; Ricaurte-Villota et al., 2018).

Por su parte, las diatomeas son consideradas más comunes en aguas neríticas (Castillo, 1984; Corchuelo y Moreno, 1983), ya que requieren mayor cantidad de nutrientes y carecen de estructuras especializadas para movilizarse activamente, dependiendo así de los cambios fisicoquímicos diarios de la columna del agua para modificar su posición (Torres y Estrada, 1997). Por ello, han sido reportadas como el grupo dominante en la provincia nerítica de diferentes países (Delgado y Chang, 2010; Loza-Álvarez et al., 2018; Troccoli-Ghinaglia et al., 2004) al igual que en el Caribe colombiano (Franco-Herrera, 2006; Franco-Herrera y Torres-Sierra, 2007; Franco-Herrera et al., 2006; Gavilán et al., 2005; Ramírez-Barón et al., 2010), reflejando su adaptación a condiciones de mayor turbulencia, ya que las favorece a disminuir su sedimentación, y a su vez, se benefician por el aumento en la concentración de nutrientes (Margalef, 1978).

Del grupo de los dinoflagelados, el género Tripos presentó la mayor riqueza, con especies que formaron cadenas de 2 hasta 14 células, como es el caso de algunas especies recolectadas con red como: T. gibberus (Gourret) F. Gómez, 2021 (2 células), T. dens (Ostenfeld et Johannes Schmidt) F. Gómez, 2013 (3 células), T. ranipes (Cleve) F. Gómez, 2013 (4 células) y T. vultur Cleve, 1900(14 células). La formación de cadenas les permite mayor flotabilidad en la zona fótica, generando cadenas más largas en zonas donde la turbulencia es menor (Vargas-Montero et al., 2008). Por lo que estas formaciones están reflejando la estabilidad de la columna de agua, principalmente en el sector externo donde fueron más comunes. La riqueza de Tripos fue mayor hacia aguas más oceánicas, confirmando lo planteado por Lozano-Duque et al. (2010a), quienes teniendo en cuenta estaciones ubicadas a lo largo de un transecto del suroccidente al nororiente a la costa Caribe colombiana, mostró que las aguas oceánicas favorecían la presencia de dinoflagelados, principalmente de este género.

La presencia de otros géneros de dinoflagelados tecados como Protoperidinium, Ornithocercus, Prorocentrum, Phalacroma, Histioneis y Dinophysis es común en aguas tropicales (Hallegraeff y Jeffrey, 1984; López y Caballero, 1997). Además, indica las estrategias de adaptación que presentan algunos de estos géneros como el tamaño, cuernos y aletas, para asegurar una mayor superficie de absorción, disminuyendo la velocidad de caída y creando dificultad de pastoreo por niveles tróficos superiores (Garay et al., 1988; Hallegraeff y Jeffrey, 1984). Por su parte, aunque el reporte de géneros de dinoflagelados atecados se ve limitado a nivel de caracterización (por su coraza débil) debido a que las técnicas de fijación como formol y lugol dificultan su preservación e identificación (Lalli y Parsons, 1997), se lograron registrar 11 géneros para este grupo. Los géneros de dinoflagelados atecados son conocidos en aguas tropicales, con estudios que se enfocan en análisis moleculares, morfológicos y ecológicos (Escobar-Morales y Hernández-Becerril, 2015; Gómez, 2003, 2005; Gómez y Furuya, 2007; Gómez et al., 2015; Maciel-Baltazar y Hernández-Becerril, 2013), sin embargo, este grupo es mucho menos conocido y estudiado en comparación con los dinoflagelados tecados. Para el Caribe colombiano se encuentran pocos registros resaltando los reportes de los géneros Torodinium Kofoid et Swezy, 1921, Asterodinium Sournia, 1972, Karenia Gert Hansen et Moestrup, 2000, Gyrodinium Kofoid et Swezy, 1921, nom. cons. (Ayala-Galván et al., 2022) y Pronoctiluca Fabre-Domergue, 1889 (Ayala-Galván et al., 2022; Hoyos-Acuña et al., 2019).

Por otra parte, del grupo de las diatomeas, el género Chaetoceros expuso la mayor riqueza;esta diatomea planctónica es un género ampliamente distribuido, es común en ambientes marinos en todo el mundo, ya sea en aguas neríticas u oceánicas, con solo unas pocas especies de ambientes continentales o estuarinos (Sunesen et al., 2008), algunas de sus especies son cosmopolitas (Li et al., 2017) y la mayoría son euritérmicas, eurihalinas y producen hipnosporas (Calderón, 1986), lo que les otorga amplias posibilidades de supervivencia incluso en condiciones adversas (Pitcher, 1990). En este estudio, Chaetoceros disminuyó su riqueza hacia aguas más oceánicas, mostrando que se ven favorecidas con la cercanía hacia aguas neríticas, lo que puede reflejar como esta diatomea se beneficia a mayor turbulencia y concentración de nutrientes (Margalef, 1978), que en este caso estarían dadas en la parte interna del área de estudio, por las descargas continentales del río Magdalena (Restrepo, 2014; Restrepo et al., 2006, 2015).

También se observó la presencia de otros géneros de diatomeas con formas coloniales unidas por prolongacionescomo Skeletonema Greville, 1865, nom. et typ. cons., Pseudo-nitzschia H. Peragallo, 1900, Hemiaulus Heiberg, 1863, nom. cons.y géneros con formas cilíndricas y alargadas como Rhizosolenia; estas formaciones son estrategias que permiten aumentar la relación superficie-volumen mejorando la flotabilidad y favoreciendo la resistencia al hundimiento haciendo que se mantengan en la capa superficial de la columna de agua (Garay et al., 1988).

Con menor riqueza se encontró al grupo de las cianobacterias, con representantes coloniales y filamentosas como: Richelia intracellularis J. Schmidt, 1901, Merismopedia elegans, Oscillatoria limosa C. Agardh ex Gomont, 1892, Planktothrix sp. Anagnostidis et Komárek, 1988, Pseudanabaena sp. Lauterborn, 1915 y Trichodesmium sp.Ehrenberg ex Gomont, 1892, nom. cons.Este grupo es considerado con baja riqueza y frecuencia en aguas marinas en comparación con aguas continentales (Margalef, 1991); sin embargo, estas algas son de gran importancia en ecosistemas oligotróficos (Campos-González, 2007), ya que son capaces de fijar nitrógeno molecular (N₂) (Rippka et al., 1979; Stewart, 1980). Las cianobacterias han representado menos de 2% de la composición específica frente al mar Caribe centro de Colombia (Franco-Herrera y Torres-Sierra, 2007), destaca también su baja riqueza en la región insular, pero con altas densidades del género Oscillatoria Vaucher ex Gomont, 1892 (Campos-González, 2007; Garay et al., 1988; INVEMARANH, 2012; Téllez et al., 1988). Este grupo ha mostrado en la provincia nerítica mayor densidad durante la época lluviosa, con representantes estuarinos como Merismopedia Meyen, 1839, Anabaena Bory ex Bornet et Flahault, 1886, nom. cons., Nostoc Vaucher ex Bornet et Flahault, 1886y Oscillatoria Vaucher ex Gomont, 1892(Franco-Herrera et al., 2006).

El género Trichodesmium sp. (fig. 4G) y la especie Richelia intracellularis (fig. 4H, I) presentaron en este estudio una frecuencia de aparición de 78% y 55%, respectivamente,y se consideran relevantes en la composición que presenta el Caribe central colombiano debido a que éstos son los organismos fijadores de N₂ (diazótrofos) más importantes de los ambientes pelágicos en los océanos del mundo, pues son responsables de ~ 63% de la fijación de N₂ en la zona pelágica (Kulkarni et al., 2010).

Por otra parte, se registraron grupos del fitoplancton marino menos representativos en cuanto a diversidad como los cocolitofóridos (Sournia, 1995; Young et al., 2003), los silicoflagelados (Hernández-Becerril y Bravo-Sierra, 2001; Throndsen, 1997) y grupos más comunes en aguas continentales como las clorofitas (Ehrenberg, 1841), las criptofitas (Cerino y Zingone, 2007) y las carofitas (Brook, 1965). En el área solo se registró a Scyphosphaera apsteinii Lohmann, 1902como representante de los cocolitofóridoscon una frecuencia de aparición de 52% y más común hacia aguas más oceánicas. Los cocolitofóridos pueden encontrarse tanto en aguas neríticas como oceánicas, y la mayoría de sus especies se dan en mares cálidos; mientras que los silicoflagelados, con pocas especies conocidas, generalmente son más abundantes en aguas frías (Lalli y Parsons, 1997). Los cocolitofóridos han mostrado mayor riqueza en aguas oceánicas de otros países como Cuba, donde se encontraron 20 especies (Loza-Álvarez y Lugioyo-Gallardo, 2009) o en el golfo de México con 29 taxones (Gaarder y Hasle, 1971). Para los silicoflagelados solo se registraron 2 representantes, Dictyocha fibula con una frecuencia de aparición de 100% y Octactis octonaria (Ehrenberg) Hovasse, 1946,con 22%, aunque esta última no estuvo presente en el sector externo. Estas especies también han sido registradas para el Pacífico colombiano (Peña y Pinilla, 2002).

Por su parte, las clorofitas y las carofitas son grupos normalmente de aguas continentales o estuarinas que se encontraron en bajas frecuencias y densidades en la provincia oceánica, reflejando la influencia de aguas continentales por corrientes locales principalmente en el sector interno, donde, la especie más común fue la clorofita Pyramimonas longicauda L. Van Meel, 1969. Estos grupos también se han registrado en aguas neríticas y oceánicas del Caribe colombiano con baja representatividad, como se ha demostrado en los estudios de Tigreros (2001) y Franco-Herrera y Torres-Sierra (2007).

En este estudio se encontraron asociaciones simbióticas como la de Solenicola setigera Pavillard, 1916con Dactyliosolen mediterraneus (H. Peragallo) H. Peragallo, 1892, la cualno había sido reportada para el Caribe colombiano. El bigiro S. setigera frecuentemente se encuentra adherido a las valvas de D. mediterraneus, sin embargo, también se puede encontrar formando colonias aisladas (Gómez, 2007; Valencia, 2013), lo que indicaría en ciertos momentos limitaciones de compuestos nitrogenados, especialmente de nitratos (Meave-del Castillo et al., 2012). Otras asociaciones encontradas fueron las de Richelia intracellularis con Guinardia cylindrus (Cleve) Hasle, 1996,o R. intracellularis con Rhizosolenia clevei Ostenfeld, 1902, las cuales ya habían sido reportadas para el Caribe colombiano en el Área de Régimen Común Colombia – Jamaica (INVEMAR-ANH, 2012), Cayo Serranilla (Ricaurte-Villota et al., 2018) y al norte de La Guajira (Ayala-Galván et al., 2018). Se conoce que los hospedadores más comunes de R. intracelularis son diatomeas de los géneros Rhizosolenia, Hemiaulus y Guinardia H. Peragallo, 1892 (Kulkarni et al., 2010). Sin embargo, esta simbiosis es más frecuente con las especies R. clevei y G. cylindrus que se encuentran en aguas tropicales (Hallegraeff y Jeffrey, 1984), así como se pudo observar en este estudio donde fue común encontrar a R. intracellularis con R. clevei. En general, este tipo de asociaciones simbióticas son conocidas y han sido registradas en los mares mundiales (Gárate-Lizárraga y Muñetón-Gómez, 2009; Gómez et al.,2005; Hallegraeff y Jeffrey, 1984; Margalef, 1961; Taylor, 1982; Valencia, 2013). La importancia de éstas en el ambiente marino radica en que pueden beneficiar tanto al huésped como al simbionte mediante el intercambio mutuo de nutrientes orgánicos e inorgánicos (Hallegraeff y Jeffrey, 1984).

La frecuencia de algunas especies encontradas se relaciona con su distribución y amplios rangos de tolerancia, Chaetoceros lorenzianus, C. peruvianus, Cerataulina pelágica, Pseudosolenia calcar-avis, Pyrocystis lunula, Ornithocercus magnificus, Tripos extensus, T. teres, T. trichoceros y Podolampas elegans se consideran cosmopolitas de aguas templadas y cálidas; Hemiaulus hauckii y H. chinensis cosmopolitas de aguas cálidasy Dictyocha fibula cosmopolita euroica(Margalef, 1961). Por su parte, los taxones raros o poco comunes representaron 12.54% de las especies identificadas, 25 de los 36 taxones con un solo registro fueron de dinoflagelados, y mostraron una mayor diversidad en aguas oceánicas, generando un aporte significativo a la estructura fitoplanctónica del Caribe central colombiano.

Al comparar el número de taxones encontrados (176 dinoflagelados y 88 diatomeas) con los registros del Gran Caribe, donde se encuentran alrededor de 1,083 especies de diatomeas (305 diatomeas céntricas y 778 diatomeas pennadas) (Navarro y Hernández-Becerril, 1997) y 404 especies de dinoflagelados (Wood, 1968), el presente trabajo representa, aproximadamente, 17.75% del total de especies conocidas de estos 2 grupos en el Gran Caribe. Al compararlos con los registros del mar Caribe colombiano, donde se han encontrado para aguas oceánicas y costeras un total de 312 especies de diatomeas pertenecientes a 106 géneros y 169 especies de dinoflagelados de 32 géneros (Lozano-Duque et al., 2010b, 2011), el presente trabajo representa aproximadamente 51.46% del total de especies registradas en estudios del mar Caribe colombiano. De lo anterior, si se tiene en cuenta la composición específica, este trabajo generó un aumento para los dinoflagelados de 27.03% (50 especies) y para las diatomeas de 2.44% (8 especies). Cabe anotar que las especies de dinoflagelados Tripos falcatus (Kofoid) F. Gómez, nom. inval. 2013 y Dinophysis capitulata Balech, nom. inválido. 1967, hasta la fecha tampoco se han registrado en el Caribe colombiano, sin embargo, no se incluyeron como nuevos registros debido a que sus estatus taxonómicos están bajo evaluación (Guiry y Guiry, 2025).

Uno de los registros más relevantes fue el de Solenicola setigera, debido a que es un registro nuevo desde la categoría taxonómica de phylum (Bigyra). Este phylum comprende generalmente organismos parásitos o simbiontes. Para aguas oceánicas del Caribe colombiano no se encontraron artículos científicos que confirmen la presencia de éstos. Sin embargo, para Colombia se encontró el registro del phylum asociado con la especie parásita Blastocystis hominis Brumpt 1912 en 2 conjuntos de datos en GBIF (Global Biodiversity Information Facility), publicados por el Instituto Nacional de Salud (Duque et al., 2022, 2023). En cuanto a S. setigera, esun protista marino colonial distintivo y muy extendido (Buck y Bentham, 1998) que no tenía definida su posición filogenética, la cual fue aclarada por Gómez et al. (2011).

Respecto al hallazgo de Scyphosphaera apsteinii, cabe mencionar que esta especie no se encontró registrada en artículos científicos para el Caribe colombiano. Sin embargo, se registra previamente en 2 conjuntos de datos en GBIF que pertenecen a las expediciones de Seaflower del Proyecto Colombia BIO (Ayala-Galván, 2018; Ayala-Galván y Dorado-Roncancio, 2021). Además, el género se encuentra en el listado para aguas oceánicas del Caribe colombiano realizado por Ayala-Galván et al. (2022).

Los resultados obtenidos sugieren que aún queda mucho por explorar respecto a la riqueza de especies en el Caribe colombiano. La información limitada disponible en aguas oceánicas puede estar relacionada con que la mayoría de estudios realizados proviene de cruceros ocasionales. Esta falta de estudios persistentes impide un conocimiento detallado de la composición específica del fitoplancton marino de aguas oceánicas, ya que estas comunidades pueden variar en diferentes escalas temporales (Davidson et al., 2013; Henson et al., 2009; Holligan y Harbour, 1977; Westberry et al., 2016).

El alto número de registros nuevos encontrados podría atribuirse, en parte, a que los resultados de este trabajo respondieron a un análisis a mesoescala, el cual no se había realizado antes para este grupo biológico en un área que representó 7.5% de las aguas oceánicas del Caribe colombiano. Así como a la ubicación del área de estudio, ya que, aunque en su totalidad pertenece a la zona oceánica, abarca estaciones en un gradiente latitudinal que se extiende desde cercanías con la zona nerítica hacia aguas más oceánicas (factor horizontal), con lo que se incrementó la probabilidad de detectar especies raras y menos frecuentes. Además, el esfuerzo de muestreo a 3 profundidades (factor vertical) permitió una mayor captura de organismos, incluyendo aquellos que habitan en diferentes masas de agua como el ASC y el ASS.

En conclusión, estos hallazgos revelan de forma general una alta riqueza fitoplanctónica en aguas oceánicas del Caribe colombiano, la cual fue mayor hacia el sector interno en aguas más cercanas a la costa, probablemente por la influencia del río Magdalena. La riqueza también se vio reflejada en los nuevos registros de dinoflagelados, diatomeas, cocolitofóridos y bigiros, que contribuyeron significativamente al conocimiento de la biodiversidad en el área, especialmente por el primer reporte del phylum Bigyra, así como el alto porcentaje de nuevos registros de dinoflagelados, que confirman su relevancia en aguas costa afuera. Estos resultados destacan la importancia de realizar estudios de composición taxonómica, análisis espaciales a mayor escala (mesoescala > 100 km y macroescala > 1,000 km), que permitan un mayor conocimiento de las comunidades fitoplanctónicas en este complejo ecosistema marino.

 Agradecimientos

Se agradece a al Instituto de Investigaciones Marinas y Costeras (INVEMAR) y a la Agencia de Nacional de Hidrocarburos (ANH) de Colombia, por la financiación de los proyectos “Línea base ambiental de los bloques COL 1 y COL 2 en la cuenca sedimentaria del Caribe colombiano fase II temática 1 (convenios 290-2015 y 167 -2016)” y “Estudio técnico ambiental de línea base en el área de evaluación COL 3 sobre la cuenca sedimentaria del Caribe colombiano (convenio 379-2017)”. Esta publicación corresponde a la contribución Núm. 1399 del INVEMAR. Además, damos un sentido agradecimiento al profesor Luis Alfonso Vidal Velásquez (Q. E. P. D.), por su asesoría en la confirmación de las identificaciones. Finalmente, agradecemos a los revisores anónimos por sus valiosos comentarios y sugerencias, los cuales contribuyeron a mejorar este manuscrito.

Referencias 

Álvarez-León, R., Aguilera-Quiñones, J., Andrade-Amaya, C. A. y Nowak, P. (1995). Caracterización general de la zona de surgencia en la Guajira colombiana. Revista de la Academia Colombiana de Ciencias Exactas Físicas y Naturales, 19, 679–694.

Andrade, C. A. y Barton, E. D. (2005). The Guajira upwelling system. Continental Shelf Research, 25, 1003–1022. https://doi.org/10.1016/j.csr.2004.12.012

Ávila-Silva, M. Y. (2018). Caracterización del ensamblaje de dinoflagelados en un sector oceánico del Caribe colombiano en la época de lluvias mayor (2015) y seca mayor (2016) (Tesis, Biología). Facultad de Ciencias Básicas, Universidad del Magdalena. Santa Marta, Colombia.

Ayala, C., Martínez, P. A., Méndez, A. y Vidal, L. A. (2011). Primer registro del dinoflagelado Neoceratium digitatum (Schütt) Gómez, Moreira y López-García 2009 (Dinophyceae), en aguas del Caribe colombiano. Biota Colombiana, 12, 145–148.

Ayala-Galván, K. (2018). Composición del fitoplancton en Isla Cayo de Serranilla en la Reserva de Biosfera – Seaflower (Versión 1) [Conjunto de datos]. Instituto de Investigaciones Marinas y Costeras. https://doi.org/10.15472/2bekzn

Ayala-Galván, K. y Dorado-Roncancio, F. (2021). Composición del fitoplancton en la Isla Cayos de Serrana en la Reserva de Biosfera – Seaflower [Conjunto de datos]. Instituto de Investigaciones Marinas y Costeras. https://doi.org/10.15472/hna7kq

Ayala-Galván, K., Dorado, F. y Escarria, E. (2018). Caracterización de comunidades biológicas A. Plancton. En M. Vides y D. Alonso (Eds.), Estudio técnico ambiental de línea base en el área de evaluación COL 10, extremo norte del Caribe colombiano. Informe Técnico Final(pp. 103–173). Agencia Nacional de Hidrocarburos/ Instituto de Investigaciones Marinas y Costeras José Benito Vives de Andréis (Convenio 340-2018).

Ayala-Galván, K., Dorado, F. y Escarria, E. (2021). Plancton. En M. Vides y D. Alonso (Eds.), Estudio técnico ambiental en áreas de interés del Caribe y Pacífico colombiano como apoyo al crecimiento sostenible del sector de hidrocarburos costa afuera – fase 2021. Informe Técnico Final(pp. 121–196). Agencia Nacional de Hidrocarburos/ Instituto de Investigaciones Marinas y Costeras José Benito Vives de Andréis (Convenio 265-2021).

Ayala-Galván, K., Dorado, F., Escarria, E., Gutiérrez, J., Contreras, K., Cárdenas, A. et al. (2017). Caracterización de comunidades biológicas. En M. Vides, M. Santos-Acevedo y D. Alonso (Eds.), Estudio técnico ambiental de línea base en el área de evaluación COL 3 sobre la cuenca sedimentaria del Caribe colombiano. Informe Técnico Final (pp. 98–260). Agencia Nacional de Hidrocarburos/ Instituto de Investigaciones Marinas y Costeras José Benito Vives de Andréis (Convenio 379-2017).

Ayala-Galván, K. y Gutiérrez-Salcedo, J. M. (2019). Comunidades biológicas: plancton. En M. Vides y D. Alonso (Eds.), Integración, análisis y diagnóstico de información de línea base ambiental de la cuenca Caribe como apoyo a nuevas a fronteras del desarrollo del sector de hidrocarburos costa afuera. Informe Técnico Final (pp. 209–256). Agencia Nacional de Hidrocarburos/ Instituto de Investigaciones Marinas y Costeras José Benito Vives de Andréis (Convenio 399-2019).

Ayala-Galván, K., Gutiérrez-Salcedo, J. M. y Montoya-Cadavid, E. (2022). Fitoplancton de la provincia oceánica del mar Caribe colombiano. Diez años de historia. Biota Colombiana, 23, e903. https://doi.org/10.21068/2539200X.903

Balech, E. (1988). Los dinoflagelados del Atlántico sudoccidental. Publicación especial del Instituto Español de Oceanografía. Consejo Regional de Asturias.

Bernal, G., Poveda, G., Roldan, P. y Andrade, C. (2006). Patrones de variabilidad de las temperaturas superficiales del mar en la Costa Caribe colombiana. Revista de la Academia Colombiana de Ciencias Exactas, Físicas y Naturales, 30, 195–208. https://doi.org/10.18257/raccefyn.30(115).2006.2240

Boltovskoy, D. (1981). Atlas del zooplancton del Atlántico sudoccidental y métodos de trabajo con el zooplancton marino. Mar del Plata, Argentina: INIDEP (Instituto Nacional de Investigación y Desarrollo Pesquero). 

Brook, A. J. (1965). Planctonic algae as indicators of lakes types with special reference to the Desmidiaceae. Limnology and Oceanography, 10, 403–411. https://doi.org/10.4319/lo.1965.10.3.0403

Buck, K. R. y Bentham, W. N. (1998). A novel symbiosis between a cyanobacterium, Synechococcus sp., an aplastidic protist, Solenicola setigera, and a diatom, Leptocylindrus mediterraneus, in the open ocean. Marine Biology, 132, 349–355. https://doi.org/10.1007/s002270050401 

Calderón, E. (1986). Las diatomeas en el plancton de los esteros de la rada de Tumaco (Pacífico colombiano), con observaciones ecológicas y biogeográficas (Tesis, Biología Marina). Facultad de Ciencias Naturales e Ingeniería, Universidad de Bogotá Jorge Tadeo Lozano.

Campos-González, E. (2007). Fitoplancton de las islas de Providencia y Santa Catalina, Caribe colombiano (Tesis, Biología Marina) Facultad de Ciencias Naturales Ingeniería, Universidad de Bogotá Jorge Tadeo Lozano.

Castillo, F. (1984). Fitoplancton del Pacífico colombiano como indicador de masas de agua (ERFEN IV). Biología Pesquera, 13, 67–70.

Cerino, F. y Zingone, A. (2007). Decrypting cryptomonads: a challenge for molecular taxonomy. En J. Brodie y J. Lewis (Eds.), Unravelling the algae: the past, present, and future of algal systematics (pp. 197–214). Systematics Association Special Volume Series, 75. Boca Raton: CRC Press.

Clarke, K. y Gorley, R. N. (2015). PRIMER (Plymouth routines in multivariate ecological research) v7. User manual/tutorial. PRIMER-E, Plymouth Marine Laboratory.

Corchuelo, M. y Moreno, G. (1983). Contribución al conocimiento del fitoplancton y algunos tintínidos del Pacífico colombiano (Tesis, Biología Marina). Facultad de Ciencias Naturales e Ingeniería, Universidad de Bogotá Jorge Tadeo Lozano.

Córdoba-Mena, N., Florez-Leiva, L., Atehortúa, L. y Obando, E. (2020). Changes in phytoplankton communities in a tropical estuary in the Colombian Caribbean Sea. Estuaries and Coasts, 43, 2106–2127. https://doi.org/10.1007/s12237-020-00750-z

Corredor, J. E. (1979). Phytoplankton response to low level nutrient enrichment through upwelling in the Columbian Caribbean Basin. Deep Sea Research Part A: Oceanographic Research Papers, 26, 731–741. https://doi.org/10.1016/0198-0149(79)90010-4

Cupp, E., (1943). Marine plankton diatoms of the west coast of North America. Bulletin of the Scripps Institution of Oceanography of the University of California, 5, 1–238.

Davidson, K., Gilpin, L. C., Pete, R., Brennan, D., McNeill, S., Moschonas, G. et al. (2013). Phytoplankton and bacterial distribution and productivity on and around Jones Bank in the Celtic Sea. Progress in Oceanography, 117, 48–63. https://doi.org/10.1016/j.pocean.2013.04.001

De la Hoz, L. A. y Betancur, S. P. (2019). Nuevo registro de la especie Cladopyxis hemibrachiata del grupo dinoflagelado para la reserva de la biosfera de Seaflower, Caribe colombiano. Boletín Científico CIOH, 38, 41–43. https://doi.org/10.26640/22159045.2019.466

Delgado, L. E. y Chang, F. (2010). La comunidad microalgal durante el verano 2006. Instituto del Mar Perú, 36, 3–4.

Dimar-CIOH. (2011). Catálogo de fitoplancton de la Bahía de Cartagena, Bahía Portete y Agua de Lastre. Dirección General Marítima Centro de Investigaciones Oceanográficas e Hidrográficas del Caribe. Serie de Publicaciones Especiales CIOH, 5. https://doi.org/10.26640/52.2011

Dorado-Roncancio, E. F., Medellín-Mora, J., Mancera-Pineda, J. E. y Pizarro-Koch, M. (2022). Copepods of the off-shore waters of Caribbean Colombian Sea and their response to oceanographic regulators. Journal of the Marine Biological Association of the United Kingdom, 101, 1129–1143. https://doi.org/10.1017/S0025315422000133

Duque, S., Arévalo-Jamaica, A., Gunturiz-Albarracín, M. L., Figueroa-Velandia, S. y López-Hernández, R. G. (2022). Colección de giardiasis del Instituto Nacional de Salud (Versión 1.1) [Conjunto de datos]. Instituto Nacional de Salud. Dataset/ Occurrence. https://doi.org/10.15472/68g8jh

Duque, S., Arévalo-Jamaica, A., Gunturiz-Albarracín, M. L., Figueroa-Velandia, S. y López-Hernández, R. G. (2023). Biobanco de parásitos intestinales del Instituto Nacional de Salud (Versión 1.2) [Conjunto de datos]. Instituto Nacional de Salud. Dataset/Occurrence. https://doi.org/10.15472/zoth79

Edler, L. y Elbrächter, M. (2010). The Utermöhl method for quantitative phytoplankton analysis. Microscopic and Molecular Methods for Quantitative Phytoplankton Analysis, 110, 13–20.

Ehrenberg, C. G. (1841). Verbreitung und Einflus des mikroskopischen Lebens in Sud-und Nord-Amerika. Abhandlungen der Königlichen Akademie der Wissenschaften zu Berlin, Physik. Kl., 1841, 291–445.

Escobar-Morales, S. y Hernández-Becerril, D. U. (2015). Free-living marine planktonic unarmoured dinoflagellates
from the Mexican tropical Pacific. Acta Botanica Mexicana, 110, 93–123. https://doi.org/10.1515/bot-2014-0049

Franco-Herrera, A. (2006). Variación estacional del fitoplancton y mesozooplancton e impacto de herbivoría de Eucalanus subtenuis, Giesbrecht, 1888 (Copepoda: Eucalanidae) en el Caribe colombiano (Tesis doctoral, en Oceanografía). Facultad de Ciencias Naturales y Oceanográficas, Universidad de Concepción. Chile.

Franco-Herrera, A., Castro, L. y Tigreros, P. (2006). Plankton dynamics in the south-central Caribbean Sea: strong seasonal changes in the Coastal Tropics Sytems. Caribbean Journal of Science, 42, 24–28.

Franco-Herrera, A. y Torres-Sierra, E. A. (2007). La comunidad fitoplanctónica en el evento de surgencia frente al mar Caribe centro de Colombia. Actualidades y Divulgación Científica, 10, 159–172. https://doi.org/10.31910/rudca.v10.n1.2007.578

Gaarder, K. R. y Hasle, G. R. (1971). Coccolithophorids of the Gulf of Mexico. Bulletin of Marine Science, 21, 519–544.

Gamboa-Márquez, J. F., Sánchez-Suárez, I. G. y La Barbera-Sánchez, A. (1994). Dinoflagelados (Pyrrophyta) del Archi-
piélago Los Roques (Venezuela): familias Prorocentraceae y Ostreopsidaceae. Acta Científica Venezolana, 45, 140–152.

Gárate-Lizárraga I. y Muñetón-Gómez M. (2009). Primer registro de la diatomea epibionte Pseudohimantidium pacificum y de otras asociaciones simbióticas en el golfo de California. Acta Botanica Mexicana, 88, 31–45. https://doi.org/10.21829/abm88.2009.311 

Garay, J., Castillo, F., Andrade, C., Aguilera, J., Niño, L., De La Pava, M. et al. (1988). Estudio oceanográfico del área insular y oceánica del Caribe colombiano – archipiélago de San Andrés y Providencia y cayos vecinos. Boletín Científico CIOH, 9, 3–73. https://doi.org/10.26640/01200542.8.3_73

Garrido-Linares, M., Alonso-Carvajal, D., Gutiérrez-Salcedo, J. M., Montoya-Cadavid, E., Rodríguez, A., Bastidas, M. et al. (2014). Línea base ambiental preliminar del bloque de exploración de hidrocarburos Guajira Offshore 3 en el Caribe colombiano. Informe técnico Final. Agencia Nacional de Hidrocarburos/ Instituto de Investigaciones Marinas y Costeras José Benito Vives de Andréis (Convenio 171–2013).

Garrido-Linares, M., Alonso-Carvajal, D., Rueda, M., Ricaurte, C., Polanco, A., Cárdenas, A. et al. (2014). Línea base ambiental preliminar de los bloques de exploración de hidrocarburos Caribe colombiano: fase COL 4 y COL 5. Informe técnico Final Agencia Nacional de Hidrocarburos/ Instituto de Investigaciones Marinas y Costeras José Benito Vives de Andréis (Convenio 188–2014).

Gavilán, M., Cañón, M. y Tous, G. (2005). Comunidad fitoplanctónica de la Bahía de Cartagena y en las aguas de lastre de buques de tráfico internacional. Boletín Científico CIOH, 23, 60–75. https://doi.org/10.26640/01200542.23.60_75

Gómez, F. (2003). New records of Asterodinium Sournia (Brachidiniales, Dinophyceae). Acta Botanica Croatica, 62, 85–92. https://doi.org/10.1127/0029-5035/2003/0077-0331

Gómez, F. (2005). Is Karenia a synonym of Asterodinium-Brachidinium (Gymnodiniales, Dinophyceae)? Vie et Milieu, 55, 237–242.

Gómez, F. (2007). The consortium of the protozoan Solenicola setigera and the diatom Leptocylindrus mediterraneus in the Pacific Ocean. Acta Protozoologica, 46, 15–24.

Gómez, F. y Furuya, K. (2007). Kofoidinium, Spatulodinium and other kofoidiniaceans (Noctilucales, Dinophyceae) in the Pacific Ocean. European Journal of Protistology, 43, 115–124. https://doi.org/10.1016/j.ejop.2006.12.002

Gómez, F., Furuya, Y. y Takeda, S. (2005). Distribution of the Cyanobacterium Richelia intracellularis as an epiphyte of the diatom Chaetoceros compresssus in the Western Pacific Ocean. Journal of Plankton Research, 27, 323–330. https://doi.org/10.1093/plankt/fbi007

Gómez, F., López-García, P., Takayama, H. y Moreira, D. (2015). Balechina and the new genus Cucumeridinium gen. nov. (Dinophyceae), unarmored dinoflagellates with thick cell coverings. Journal of Phycology, 51, 1088–1105. https://doi.org/10.1111/jpy.12346

Gómez, F., Moreira, D., Benzerara, K. y López-García, P. (2011). Solenicola setigera is the first characterized member of the abundant and cosmopolitan uncultured marine stramenopile group MAST-3. Environmental Microbiology, 13, 193–202. https://doi.org/10.1111/j.1462-2920.2010.02320.x

Guiry, M. D. y Guiry, G. M. (2025). AlgaeBase. Publicación electrónica mundial, Universidad Nacional de Irlanda, Galway. Consultado el 24 de febrero de 2025 en https://www.algaebase.org 

Hallegraeff, G. M. y Jeffrey, S. W. (1984). Tropical phytoplankton species and pigments of continental shelf waters of north and north-west Australia. Marine Ecology Progress Series, 20, 59–74.

Henson, S. A., Dunne, J. P. y Sarmiento, J. L. (2009). Decadal variability in North Atlantic phytoplankton blooms. Journal of Geophysical Research: Oceans, 114, C04013. https://doi.org/10.1029/2008JC005139

Hernández-Becerril, D. U. y Bravo-Sierra, E. (2001). Planktonic silicoflagellates (Dictyochophyceae) from the Mexican Pacific. Botanica Marina, 44, 417–423. https://doi.org/10.1515/BOT.2001.050

Holligan, P. M. y Harbour, D. S. (1977). The vertical distribution and succession of phytoplankton in the western English Channel in 1975 and 1976. Journal of the Marine Biological Association of the United Kingdom, 57, 1075–1093. https://doi.org/10.1017/S002531540002614X

Hoppenrath, M., Elbrächter, M. y Drebes, G. (2009). Marine phytoplankton. Stuttgart:Kleine SenckenbergReihe. 

Hoyos-Acuña, J. J., Salón-Barros, J. C. y Mancera-Pineda, J. E. (2019). Aspectos morfológicos y primer registro del dinoflagelado Pronoctiluca spinifera en el Caribe colombiano. Acta Biológica Colombiana, 24, 264–274. https://doi.org/10.15446/abc.v24n2.70179

INVEMAR (Instituto de Investigaciones Marinas y Costeras José Benito Vives de Andréis). (2015). Informe del estado de los ambientes y recursos marinos y costeros en Colombia: Año 2014. Serie de Publicaciones Periódicas Núm. 3. Santa Marta, Colombia: INVEMAR.

INVEMAR (Instituto de Investigaciones Marinas y Costeras José Benito Vives de Andréis)-ANH (Agencia Nacional de Hidrocarburos). (2008). Especies, ensamblajes y paisajes de los bloques marinos sujetos a exploración de hidrocarburos. Informe técnico final. Santa Marta, Colombia: Agencia Nacional de Hidrocarburos/ Instituto de Investigaciones Marinas y Costeras José Benito Vives de Andréis. 

INVEMAR (Instituto de Investigaciones Marinas y Costeras José Benito Vives de Andréis)-ANH (Agencia Nacional de Hidrocarburos). (2010). Especies, ensamblajes y paisajes de los bloques marinos sujetos a exploración de hidrocarburos – Fase II – Caracterización de la megafauna y el plancton del Caribe colombiano. Informe Técnico Final. Santa Marta, Colombia: Agencia Nacional de Hidrocarburos/ Instituto de Investigaciones Marinas y Costeras José Benito Vives de Andréis.

INVEMAR (Instituto de Investigaciones Marinas y Costeras José Benito Vives de Andréis)-ANH (Agencia Nacional de Hidrocarburos). (2012). Línea base ambiental en el Área de Régimen Común Jamaica – Colombia como aporte al aprovechamiento sostenible de los recursos marinos compartidos. Informe técnico final. Santa Marta, Colombia: Agencia Nacional de Hidrocarburos/ Instituto de Investigaciones Marinas y Costeras José Benito Vives de Andréis.

INVEMAR (Instituto de Investigaciones Marinas y Costeras José Benito Vives de Andréis), CORALINA (Corporación para el Desarrollo Sostenible del Archipiélago de San Andrés, Providencia y Santa Catalina), UNIANDES (Universidad De Los Andes) y UPB (Universidad Pontificia Bolivariana). (2017). Evaluación física y biológica de los ambientes profundos de la isla Cayos de Serrana en la Reserva de Biósfera – Seaflower. Informe Técnico Final. Expedición Científica Seaflower en Isla Cayo Serrana. Santa Marta, Colombia: Instituto de Investigaciones Marinas y Costeras José Benito Vives de Andréis.

Kulkarni, V. V., Chitari, R. R., Narale, D. D., Patil, J. S. y Anil, A. C. (2010). Occurrence of cyanobacteria-diatom symbiosis in the Bay of Bengal: implications in biogeochemistry. Current Science, 99, 6–25.

Lalli, C. y Parsons, T. R. (1997). Biological oceanography: an introduction (2nd Ed.). Elsevier Butterworth-Heinemann. 

Li, Y., Boonprakob, A., Gaonkar, C. C., Kooistra, W. H., Lange, C. B., Hernández-Becerril, D. et al. (2017). Diversity in the globally distributed diatom genus Chaetoceros (Bacillariophyceae): three new species from warm-temperate waters. Plos One, 12, e0168887. https://doi.org/10.1371/journal.pone.0168887

Licea, S., Moreno, J. L., Santoyo, H. y Figueroa, G. (1995). Dinoflagelados del golfo de California. La Paz, México:Universidad Autónoma de Baja California Sur. 

López, N. O. y Caballero, O. G. (1997). Dinoflagelados del mar peruano como indicadores de masas de agua durante los años 1982 a 1985. Boletín Instituto del Mar del Perú, 16, 1–60.

Loza-Álvarez, S., Benavides-Morera, R., Brenes-Rodríguez, C. L. y Saxon, D. B. (2018). Phytoplankton structure in dry and rainy seasons in the gulf of Papagayo, Costa Rica. Journal of Marine and Coastal Sciences, 10, 9–30. https://doi.org/10.15359/revmar.10-2.1

Loza-Álvarez, S. y Lugioyo-Gallardo, G. M. (2009). Diversidad del microfitoplancton en las aguas oceánicas alrededor de Cuba. Revista Ciencias Marinas y Costeras, 1, 29–47. https://doi.org/10.15359/revmar.1.2

Lozano-Duque, Y., Medellín-Mora, J. y Navas, G. R. (2010). Contexto climatológico y oceanográfico del mar Caribe colombiano. Biodiversidad del margen continental del Caribe colombiano. Santa Marta, Colombia:Serie de publicaciones especiales INVEMAR.

Lozano-Duque, Y., Vidal, L. A. y Navas, G. R. (2011). Lista de especies de dinoflagelados (Dinophyta) registrados en el mar Caribe colombiano. Boletín de Investigaciones Marinas y Costeras-INVEMAR, 40, 361–380. 

Lozano-Duque, Y., Vidal, L. A. y Navas, G. R. (2010a). La comunidad fitoplanctónica en el mar Caribe colombiano. Biodiversidad del margen continental del Caribe colombiano. Serie de publicaciones especiales INVEMAR Núm. 20.

Lozano-Duque, Y., Vidal, L. A. y Navas, G. R. (2010b). Listado de diatomeas (Bacillariophyta) registradas para el Mar Caribe colombiano. Boletín de Investigaciones Marinas y Costeras-INVEMAR, 39, 83–116. 

Maciel-Baltazar, E. y Hernández-Becerril, D. U. (2013). Especies de dinoflagelados atecados (Dinophyta) de la costa de Chiapas, sur del Pacífico mexicano. Revista de Biología Marina y Oceanografía, 48, 245–259. https://doi.org/10.4067/S0718-19572013000200005

Margalef, R. (1961). Distribución ecológica y geográfica de las especies del fitoplancton marino. Investigación Pesquera, 19, 81–101.

Margalef, R. (1969). Estudios sobre la distribución a pequeña escala del fitoplancton marino. Memorias de la Real Academia de Ciencias y Artes de Barcelona, 40,3–22.

Margalef, R. (1978). Life-forms of phytoplankton as survival alternatives in an unstable environment. Oceanologica Acta, 1, 493–509.

Margalef, R. (1991). Ecología. Barcelona, España: Omega. 

Meave-del Castillo, M. E., Zamudio-Reséndiz, M. E. y Castillo-Rivera, M. (2012). Riqueza fitoplanctónica de la bahía de Acapulco y zona costera aledaña, Guerrero, México. Acta Botanica Mexicana, 100, 405–487. https://doi.org/10.21829/abm100.2012.41

Molina, A., Molina, C., Giraldo, L., Parra, C. y Chevillot, P. (1994). Dinámica marina y sus efectos sobre la geomorfología del golfo de Morrosquillo. Boletín Científico CIOH, 15, 93–113. https://doi.org/10.26640/22159045.74

Navarro, J. N. y Hernández-Becerril, D. U. (1997). Check-list of marine diatoms from the Caribbean Sea. Listados Florísticos de México, 15, 1–48.

Okolodkov, Y. B. (2003). A review of Russian plankton research in the Gulf of Mexico and the Caribbean Sea in the 1960-1980s. Hidrobiológica, 13, 207–221.

Peña, V. y Pinilla, G. A. (2002). Composición, distribución y abundancia de la comunidad fitoplanctónica de la ensenada de Utría, Pacífico colombiano. Revista de Biología Marina y Oceanografía, 37, 67–81. http://dx.doi.org/10.4067/S0718-
19572002000100008

Pitcher, G. (1990). Phytoplankton see populations of the Cape Peninsula upwelling plume, with particular reference to resting spores of Chaetoceros (Bacillariophyceae) and their role in seeding upwelling waters. Estuarine, Coastal and Shelf Science, 31, 283–301. https://doi.org/10.1016/0272-7714(90)90105-Z

Ramírez, A. (1999). Ecología aplicada: diseño y análisis estadístico. Bogotá: Fundación Universidad de Bogotá Jorge Tadeo Lozano. 

Ramírez-Barón, J. S., Franco-Herrera, A., García-Hoyos, L. M. y López, D. A. (2010). La comunidad fitoplanctónica durante eventos de surgencia y no surgencia, en la zona costera del departamento del Magdalena, Caribe colombiano. Boletín de Investigaciones Marinas y Costeras-INVEMAR, 39, 233–263.

Restrepo, J. C. (2014). Dinámica sedimentaria en deltas micromareales-estratificados de alta descarga: delta del río Magdalena (Colombia-Mar Caribe) (Tesis doctoral, en Ciencias del Mar). Facultad de Ciencias Básicas, Universidad del Norte. Colombia.

Restrepo, J. C., Ortiz, J. C., Otero, L. y Ospino, S. R. (2015). Transporte de sedimentos en suspensión en los principales ríos del Caribe colombiano: magnitud, tendencias y variabilidad. Revista de la Academia Colombiana de Ciencias Exactas, Físicas y Naturales, 39, 527–546. https://doi.org/10.18257/raccefyn.209

Restrepo, J. D., Kjerfve, B., Hermelín, M. y Restrepo, J. C. (2006). Factors controlling sediment yield in a major South American drainage basin: the Magdalena River, Colombia. Journal of Hydrology, 316, 213–232. https://doi.org/10.1016/j.jhydrol.2005.05.002

Ricaurte-Villota, C. y Bastidas-Salamanca, M. L. (Eds.). (2017). Regionalización oceanográfica: una visión dinámica del Caribe. Serie de Publicaciones Especiales Núm.14. Santa Marta, Colombia: Instituto de Investigaciones Marinas y Costeras José Benito Vives De Andréis. 

Ricaurte-Villota, C., Murcia-Riaño, M., Ayala-Galván., K., Dorado, E. F., Escarria, E. y Alonso, D. A. (2018). Evaluación física y biológica de los ambientes profundos de la isla cayo de Serranilla en la Reserva de la Biosfera – Seaflower. Expedición Científica Seaflower 2017 Isla Cayo Serranilla. Santa Marta, Colombia: Informe Técnico Final del Instituto de Investigaciones Marinas y Costeras José Benito Vives De Andréis para la Comisión Colombiana del Océano.

Rippka, R. Deruelles, J., Waterbury, J. B., Herdman, M. y Stanier, R. Y. (1979). Generic assignments, strain histories and properties of pure cultures of cyanobacteria. Microbiology, 111, 1–61. https://doi.org/10.1099/00221287-111-1-1

Round, F. (1990). Diatoms: the biology and morphology of the genera. Cambridge: Cambridge University Press. https://doi.org/10.1017/S0025315400059245

Salón, J. C. (2013). Caracterización de la comunidad fitoplanctónica en áreas oceánicas del Caribe colombiano durante la época seca del año 2011 (febrero y marzo) (Tesis, Biología). Facultad de Ciencias Básicas, Universidad del Magdalena. Santa Marta, Colombia.

Schlitzer, R. (2022). Ocean data view. https://odv.awi.de

Sournia, A. (1995). Red tide and toxic marine phytoplankton of the world ocean: and inquiry into biodiversity. En P. Lassus et al. (Eds.), Harmful marine algal blooms (pp. 103–112). París, Francia: Lavoisier.

Stewart, W. D. P. (1980). Some aspects of structure and function in N2-fixing cyanobacteria. Annual Review of Microbiology, 34, 497–536. https://doi.org/10.1146/annurev.mi.34.100180.002433

Sunesen, I., Hernández-Becerril, D. U. y Sar, E. A. (2008). Marine diatoms from Buenos Aires coastal waters (Argentina). V. Species of the genus Chaetoceros. Revista de Biología Marina y Oceanografía, 43, 303–326. https://doi.org/10.4067/S0718-19572008000200009

Taylor, F. J. R. (1976). Dinoflagellates from the International Indian Ocean Expedition. A material collected by the R.V.” Anton Bruun” 1963-1964. Stuttgart, Alemania: Biblioteca Botánica. 

Taylor, F. J. R. (1982). Symbioses in marine microplankton. Annales de l’Institut Océanographique, 58, 61–90.

Téllez, C., Márquez, G. y Castillo, F. (1988). Fitoplancton y ecología pelágica en el archipiélago de San Andrés y Providencia: Crucero Océano VI en el Caribe colombiano. Boletín Científico CIOH, 8, 3–26. https://doi.org/10.26640/22159045.26

Throndsen, J. (1997). The planktonic marine flagellates. En C. R. Tomas (Ed.), Identifying marine phytoplankton (pp. 591–729). San Diego, EUA: Academic Press.

Tigreros, P. (2001). Biodiversidad y valoración bioquímica del fitoplancton marino en ambientes costeros mesotróficos y oligotróficos tropicales, Caribe colombiano (Tesis, Biología Marina), Facultad de Ciencias Naturales e Ingeniería, Universidad de Bogotá Jorge Tadeo Lozano.

Tomas, C. (1997). Identifying marine phytoplankton. San Diego, EUA: Academic Press. https://doi.org/10.1017/S0025315400038959

Torres, R. y Estrada, M. (1997). Patrones de migración vertical en el plancton de un lago tropical. Hidrobiológica, 7, 33–40.

Troccoli-Ghinaglia, L., Herrera-Silveira, J. A. y Comín, F. A. (2004). Structural variations of phytoplankton in the coastal seas of Yucatan, Mexico. Hydrobiologia, 519, 85–102. https://doi.org/10.1023/B:HYDR.0000026487.78497.b6

Valencia, V. J. (2013). Variación estacional del fitoplancton en una estación nerítica del Canal de Mallorca (Mediterráneo occidental): 2000-2001 (Tesis doctoral). Departamento de Bioloxía Celular e Molecular de la Facultade de Ciencias, Universidad da Coruña. España.

Vargas-Montero, M., Bustamante, E. F., Guzmán, J. C. y Vargas, J. C. (2008). Florecimientos de dinoflagelados nocivos en la costa Pacífica de Costa Rica. Hidrobiológica, 18, 15–23.

Vidal, L. A. (2010). Manual del fitoplancton hallado en la ciénaga Grande de Santa Marta y cuerpos de agua aledaños. Fundación Universidad de Bogotá Jorge Tadeo Lozano. Bogotá, Colombia.

Vidal, L. A. y Lozano-Duque, Y. (2011). Revisión de los taxones del género Neoceratium F. Gómez, D. Moreira et P. Lópezgarcía (Dinophyceae) y primer registro de N. dens en el mar Caribe colombiano. Boletín de Investigaciones Marinas y Costeras – INVEMAR, 40, 143–183.

Vides, M. y Alonso, D. (Eds.) (2016). Línea base ambiental de los bloques COL 1 y COL 2 en la cuenca sedimentaria del Caribe colombiano – Temática 1. En M. Vides, y D. Alonso (Eds.), Levantamiento de información ambiental de sistemas marinos y costeros sobre el Caribe colombiano Fase II. Informe Técnico Final (pp. 75–160). Santa Marta, Colombia: Agencia Nacional de Hidrocarburos/ Instituto de Investigaciones Marinas y Costeras José Benito Vives de Andréis(Convenios 290-2015 y 167–2016).

Westberry, T. K., Schultz, P., Behrenfeld, M. J., Dunne, J. P., Hiscock, M. R., Maritorena, S. et al. (2016). Annual cycles of phytoplankton biomass in the subarctic Atlantic and Pacific Ocean. Global Biogeochemical Cycles, 30, 175–190. https://doi.org/10.1002/2015GB005276

Wood, F. (1963). Dinoflagellates in the Australian Region. Australian Journal of Marine and Freshwater Research, 5, 171–352. https://doi.org/10.1071/MF9540171

Wood, F. (1968). Dinoflagellates of the Caribbean Sea and adjacent areas. Coral Gables, FL: University of Miami Press. 

Young, J. R., Geisen, M., Cros, L., Kleijne, A., Probert, I. y Ostergaard, J. B. (2003). A guide to extant coccolithophore taxonomy. Journal of Nannoplankton Research, Special Issue, 1, 1–132. https://doi.org/10.58998/jnr2297

Alejandro Lizama-Hernández ^a, Ma Ventura Rosas-Echeverría ^a, *, M. Guadalupe del Rio ^b

^a Universidad Autónoma del Estado de Morelos, Escuela de Estudios Superiores del Jicarero, Laboratorio de Sistemática y Evolución de Insectos, Carretera Galeana-Tequesquitengo s/n, Colonia El Jicarero, 62909 Jojutla, Morelos

^b Museo de La Plata, División Entomología- Consejo Nacional de Investigaciones Científicas y Técnicas, Paseo del Bosque s/n, 1900 La Plata, Buenos Aires, Argentina

*Corresponding author: mvrosase@gmail.com (M.V. Rosas-Echeverría)

Received: 01 October 2024; accepted: 27 January 2025

Abstract

The first phylogenetic analysis of the weevil genus Megalostylus endemic to Mexico(Entiminae, Naupactini) is presented, based on a data matrix of 37 morphological characters of adults and 21 terminal taxa. The ingroup comprises 9 species, 4 varieties, and 5 specimens of Megalostylus whose identification at the species level is doubtful. The outgroup includes species representing closely related genera: Pantomorus albosignatus, Naupactus cervinus, and Megalostylodes hirsutus. The objectives were to test the monophyly of Megalostylus, to explore its species relationships, and to determine which synapomorphies allow its identification and differentiation from other genera. The analysis yielded a single cladogram of 61 steps, showing the following phylogenetic sequence: (Pantomorus albosignatus (Naupactus cervinus (Megalostylodes hirsutus (Megalostylus rhodopus (M. morpho 2(M. macrophthalmus (M. tomentosus (M. dilaticollis (M. albicans (M. brevipilis, M. fusiformis (M. splendidus – M. sturmi))))))))))).The results support the monophyly of Megalostylus based on the following synapomorphies: protibia with a prominence opposite to mucro, elytra almost flat, sternite VIII subrhomboidal very elongated, and aedeagus smooth. They also support its sister-group relationship with Megalostylodes.

Keywords: Systematics; Naupactini; Morphology; New species; New varieties; Megalostylodes

Filogenia del género de gorgojos Megalostylus (Coleoptera: Curculionidae: Entiminae), endémico de México

Resumen

Presentamos el primer análisis filogenético del género de gorgojos Megalostylus endémico de México(Entiminae, Naupactini)basado en una matriz de datos de 37 caracteres morfológicos de adultos y 21 taxones terminales. El grupo interno comprende 9 especies, 4 variedades y 5 especímenes de Megalostylus de dudosa identificación a nivel de especie. El grupo externo está formado por 3 especies representantes de géneros relacionados cercanamente: Pantomorus albosignatus, Naupactus cervinus y Megalostylodes hirsutus. Los objetivos fueron poner a prueba la monofilia de Megalostylus, explorar sus relaciones interespecíficas y determinar qué sinapomorfías lo identifican y diferencian de otros géneros. El análisis produjo un solo cladograma de 61 pasos, que muestra la siguiente secuencia filogenética: (Pantomorus albosignatus (Naupactus cervinus (Megalostylodes hirsutus (Megalostylus rhodopus (M. morpho 2(M. macrophthalmus (M. tomentosus (M. dilaticollis (M. albicans (M. brevipilis, M. fusiformis (M. splendidus – M. sturmi))))))))))). Los resultados avalan la monofilia de Megalostylus con base en las siguientes sinapomorfías: protibias con una prominencia opuesta al mucro, élitros casi planos en vista lateral,  esternito VIII subromboidal muy elongado y aedeago liso. También respaldan su estrecha relación con Megalostylodes.

Palabras clave: Sistemática; Naupactini; Morfología; Especie nueva; Variedades nuevas; Megalostylodes

Introduction 

Megalostylus Schoenherr, 1840 (Entiminae, Naupactini) is a genus of broad-nosed weevils distributed in the Mexican states of Durango, Guanajuato, Guerrero, Michoacán, Morelos, Oaxaca, Puebla and Veracruz (Champion, 1911; Muñiz-Vélez et al., 2015; Ordóñez- Reséndiz et al., 2008). It was described by Schoenherr (1840) in his monumental work Genera et species curculionidum, cum synonymia hujus familiae, specie novae aut hactenus minus cognitae based on the type species M. sturmi Boheman, 1840 and has been traditionally characterized by the presence of a short antennal scape comparatively stouter at apex than in other genera (Champion, 1911; Figs. 1-3). The most complete treatment of Megalostylus was conducted by Champion (1911), who recognized 9 species and assigned this genus to “Otiorhynchinaealatae”, group “Cyphina”. He also provided a taxonomic key based on 32 morphological characters of adults and the complete distribution records of the species until then. 

The classification of Megalostylus proposed by Champion (1911) more than a century ago needs a revision of the status of the species, the infraspecific varieties, and a phylogenetic analysis, to test the monophyly, species relationships, and synapomorphies that support the genus.

Materials and methods 

We examined 347 adult specimens obtained from the following entomological collections: IBUNAM, Instituto de Biología, Universidad Nacional Autónoma de México, Mexico City, Mexico; INECOL, Instituto de Ecología, A. C., Xalapa, Veracruz, Mexico; USNM, National Museum of Natural History, Washington DC, USA; NHRS, Swedish Museum of Natural History, Stockholm, Sweden; and BMNH, Natural History Museum, London, England. Moreover, we included material collected by the working team at the Laboratorio de Sistemática y Evolución de Insectos (LabSei) of the ESSJicarero, UAEM.

Taxon sampling. The outgroup comprises 3 species: Megalostylodes hirsutus Champion, 1911, Naupactus cervinus (Boheman, 1840), and Pantomorus albosignatus Boheman, 1840, the former representing the most closely related genus. The ingroup includes 9 species (Figs. 1-3): M. sturmi Boheman,1840, M. rhodopus Boheman, 1840, M. albicans (Lacordaire, 1876), M. splendidus Chevrolat, 1878, M. brevipilis Champion, 1911, M. dilaticollis Champion, 1911, M. fusiformis Champion, 1911, M. macrophthalmus Champion, 1911, and M. tomentosus Champion, 1911 (Table 1). Additionally, 4 described varieties and 5 specimens of doubtful identification at species-level were included as morphospecies1-5.

A list of 37 discrete characters (29 binary and 8 multistate) was recorded from adults, including 33 characters from the external morphology, 2 of the female genitalia, and 2 of the male genitalia (Table 2). The selection of characters was based on previous analyses of the tribe Naupactini (del Río, 2009; Lanteri & del Río, 2017; Rosas et al., 2011). 

For the preparation of genital structures, we followed the methodology described in Rosas et al. (2011) and Lanteri and del Río (2017). A Carl Zeiss Stemi 2000 stereomicroscope, equipped with a reticle eyepiece was used for observations and measurements of the external and internal morphology. Photographs were taken with a Nikon D750 camera equipped with a SIGMA 150 mm 1:2.8 (macro) lens, and drawings were made with Corel Draw (2020 version 22.0.0412). Most characters were illustrated by photographs and drawings, to facilitate the recognition of character states (Figs. 4, 5). They were highlighted with arrows, with indication of character numbers and character states between parentheses. 

A data matrix of 21 terminal groups and 37 morphological characters was compiled (Table 3). Character states that could not be examined (due to insufficient material) were scored with a “?” and character states with inapplicable entries on various terminals were scored with a “–”. Species or varieties showing 2 or more characters were coded as polymorphic characters. To facilitate the coding, Mesquite software version 3.70 was used (Maddison & Maddison, 2021). An implicit enumeration search was performed in the program TNT version 1.5 (Goloboff & Catalano, 2016). The characters were treated as unordered or non-additive, and under equal weights. The species Pantomorus albosignatus was used to root the trees. To evaluate branch support (BS), a standard Bootstrap with 1000 replicates was calculated in TNT. Branch support values greater than 50 were mapped in the cladogram. The resulting cladogram and character state transformations were examined in WINCLADA under fast optimization. All records were georeferenced, and maps created in ArcMap version 10. 4.1 (ESRI, 2015).

Results 

The search for the most parsimonious trees under equal weights yielded one most parsimonious tree (Fig. 6) (L = 63, IC = 0.73, IR = 0.83), showing the following phylogenetic sequence: (Pantomorus albosignatus (Naupactus cervinus (Megalostylodes hirsutus (Megalostylus)))). 

Megalostylodes was found to be sister to the genus Megalostylus based on 12 synapomorphies: epistome scales similar in size, density, and color to those on the rest of the rostrum (0:0), dorsal surface of rostrum slightly to strongly depressed (1:1), absence of pair of dorsolateral carinae (2:0), scape very wide in males and thin in females (3:1), width of scape at apex greater than club width in males (4:1), shape of scape strongly clavate (5:1), color brown to black of the verticillate setae of funicle (9:1), slight lateral projection of pronotum (14:1), absence of a row of denticles on inner margin of protibia (20:0), vestiture of scutellum present, consisting of white scales or seta-like scales (25:1), presence of medial longitudinal depression of ventrites 1 and 2 on males (32:1), and subspherical body shape of spermatheca (33:1). There are also 2 homoplastic characters that support this relationship: pronotum subconical, with sides curved and strongly divergent from apex to base (11:1) and width of base of scutellum wider than interestria 2 (24:2). 

Megalostylus was recovered as monophyletic based on 4 synapomorphies: presence of prominence opposite to mucro in protibia (21:1), elytra in lateral view almost flat (23:1), plate of sternite VIII, subrhomboidal very elongated (34:0), and sculpture of aedeagus smooth (35:1).

The sister genus Megalostylodes is characterized by 3 autapomorphies: pronotum narrower with respect to elytral base (13:0), very long elytral setae, longer than width of elytral interstriae 2 at middle (27:2), and presence of deeply excavated metafemur near apex (31:1), and 3 non-exclusive synapomorphies: presence of glabrous areas in midline of pronotum (12:1), erect disposition of elytral setae (26:1), and slightly convex interestriae (29:1). 

Table 1

List of species included in the cladistic analysis of the genus Megalostylus and their geographic distributions (countries and states).

Species names	Geographic distributions
Pantomorus albosignatus Boheman	Mexico (Aguascalientes, Chihuahua, Coahuila, Mexico City, Durango, Guanajuato, Guerrero, Hidalgo, Monterrey, Oaxaca, Puebla Querétaro, San Luis Potosí, Veracruz, Zacatecas)
Naupactus cervinus (Boheman)	Argentina (Buenos Aires, Catamarca, Córdoba, Corrientes, Entre Ríos, Jujuy, Mendoza, Misiones, Salta, Santa Fe, Tucumán), Brasil (Paraná, Río Grande do Sul, Santa Catarina, São Paulo), México (Distrito federal), Uruguay (Artigas, Canelones, Colina, Durazno, Maldonado, Montevideo, Rio Negro, Treinta y Tres)
Megalostylodes hirsutus Champion	Mexico (Oaxaca)
Megalostylus albicans (Lacordaire)	Mexico (Colima, Estado de México, Guanajuato, Guerrero, Jalisco, Michoacán, Morelos, Nayarit, Oaxaca, Puebla)
Megalostylus brevipilis Champion	Mexico (Colima, Guerrero, Oaxaca)
Megalostylus dilaticollis Champion	Mexico (Guerrero, Michoacán, Morelos, Jalisco)
Megalostylus fusiformis Champion	Mexico (Morelos, Guerrero)
Megalostylus macrophthalmus Champion	Mexico (Oaxaca)
Megalostylus rhodopus Boheman	Mexico (Oaxaca)
Megalostylus splendidus Chevrolat	Mexico (Durango, Guerrero, Morelos, Puebla)
Megalostylus sturmi Boheman	Mexico (Guerrero, Michoacán)
Megalostylus tomentosus Champion	Mexico (Oaxaca)

Table 2 

List of 37 morphological characters, character states and codes. 

Character	Character states
0. Shape, size, density and color of epistome scales compared to those on the rest of the rostrum	Similar in size, density and color (0); smaller, scarcer and generally different in color (1)
1. Dorsal surface of rostrum	Flat (0); slightly to strongly depressed (1)
2. Pair of dorsolateral carinae	Absent (0); present (1)
3. Sexual dimorphism in antennae	Scape width subequal in males and females (0); scape very wide in males and thin in females (1)
4. Width of scape at apex with respect to width of club, in males	Less than club width (0); greater than club width (1)
5. Shape of scape	Capitate (0); strongly clavate (1)
6. Vestiture of scape	Absent to almost absent (0); scales dispersed leaving integument exposed (1); dense, space between scales reduced or absent, not leaving integument exposed (2)
7. Length of funicular antennomeres 1 and 2	Antennomere 2 slightly shorter than 1 or both sub-equal (0); antennomere 2 longer than 1 (1)
8. Antennae, scales on funicular antennomere 2	Absent (0); present (1)
9. Color of verticillate setae of funicle	Whitish or golden (0); brown to black (1)
10. Convexity of eyes	Convex, pronounced curvature, hemispherical shape (0); slightly convex, less pronounced curvature, small elevations (1)
Table 2. Continued
11. Shape of pronotum	Subcylindrical, curved sides and maximum width about half (0); subconical, with sides moderately to strongly curved and strongly divergent from apex to base (1); subconical, with sides slightly curved to straight and strongly divergent from apex to base (2); bell-shaped (3); subtrapezoidal, with sides slightly concave at anterior half and progressively expanding towards lateral sides at posterior half (4)
12. Glabrous areas at midline of pronotum	Absent (0); present (1)
13. Width of pronotum with respect to elytral base	Narrower (0); subequal (1); wider (2)
14. Lateral projection of pronotum	Absent or indistinct (0); slightly projected (1); strongly projected (2)
15. Shape of lateral projections of posterior margin of pronotum	Extended towards sides (0); strongly extended backwards, towards elytral base (1)
16. Sides at basal third of pronotum	Not depressed (0); strongly depressed (1)
17. Shape of posterior margin of pronotum	Straight to slightly bisinuate (0); strongly bisinuate (1)
18. Bulging surface beneath intercoxal granule, at anterior margin of prothorax	Indistinct or absent (0); present (1)
19. Color of legs integument	Light tones, reddish or orange (0); dark tones, black or brown (1)
20. Row of denticles on inner margin of protibia	Absent (0); present (1)
21. Prominence opposite to mucro in protibia	Absent (0); present (1)
22. Elytral anterior margin	Straight (0); bisinuate (1)
23. Shape of elytra in lateral view	Moderately convex (0); almost flat (1)
24. Width of base of scutellum with respect to width of interstria 2	Reduced to indistinct (0); subequal to width of interstria 2 (1); wider than interstria 2 (2)
25. Scutellum vestiture	Scales similar in color to those covering whole surface of elytra (0);  Scales similar, consisted of white scales or seta-like scales (1)
26. Disposition of elytral setae	Recumbent to suberect (0); erect (1)
27. Size of elytral setae	Short (0); long, almost as long as width of interstria 2 at middle (1); very long, longer than width of elytral interestriae 2 at middle (2)
28. Arrangement of elytral setae	Uniform throughout elytral disc (0); only on lateral edges of elytral disc, dorsally without setae (1)
29. Convexity of interstriae	Flat (0); slightly convex (1)
30. Vestiture on legs	Absent or almost absent (0); inconspicuous, scales are scattered leaving integument exposed (1); conspicuous, space between scales is reduced or absent, and covered the integument (2)
31. Deep excavation on metafemur, near apex	Absent (0); present (1)
32. Medial longitudinal depression of ventrites 1 and 2, on males	Indistinct or absent (0); present (1)
33. Spermatheca, body shape	Subcylindrical, slender (almost as wide as base of cornu) (0); subspherical (1)
34. Shape of plate of sternite VIII	Subrhomboidal very elongated, with basal part much longer than apical part (0); subrhomboidal slightly elongated, with basal part as long as apical part (1)
35. Aedeagus, sculpture of median lobe	Granulose (0); smooth (1)
36. Aedeagus, shape of apex of median lobe	Acute to slightly acute (0); truncated (1); arrow shape (2)

Table 3

Data matrix of 21 taxa and 37 morphological characters of Megalostylus and outgroups used for the cladistic analysis. Inapplicable characters are indicated with a dash (-), and missing characters with a question mark (?).

Taxa	Characters
	0-4	5-9	10-14	15-19	20-24	25-29	30-36
Pantomorus albosignatus	101?0	00000	00010	00000	10000	-0100	00?01??
Naupactus cervinus	10100	00100	00010	00000	10100	00000	00001?2
Megalostylodes hirsutus	01011	10001	01101	00000	00102	11201	0111100
Megalostylus albicans	01011	12010	02012	00101	01111	00000	1011010
Megalostylus albicans var. expansus	01011	12010	02022	00101	01111	00000	101??10
Megalostylus albicans var. farinosus	01011	120?0	02012	00101	01111	00000	101????
Megalostylus brevipilis	010?1	120?0	03011	10101	01111	00000	101??10
Megalostylus dilaticollis	01011	12000	04022	01001	01111	00000	10110??
Megalostylus fusiformis	010?1	120?0	03011	10101	01111	00000	10?????
Megalostylus macrophthalmus	01011	100?	12011	00000	01112	10000	00?10??
Megalostylus splendidus	01011	12010	01011	10101	01112	00000	1011010
Megalostylus splendidus var.	01011	12010	01011	10101	01112	00000	1011010
Megalostylus sturmi	01011	12010	0100&11	10111	01112	01100	1011?11
Megalostylus sturmi var. villosus	01011	12010	0100&11	10111	01112	01100	1011011
Megalostylus rhodopus	01011	12001	01111	00000	01112	10010	0011010
Megalostylus tomentosus	01011	110?0	02011	00000	01112	01100	00110??
Morphospecies 1	010?1	12001	01111	10000	0111?	10010	001??10
Morphospecies 2	010?1	11000	01011	10100	01112	10000	001??10
Morphospecies 3	010?1	10001	02011	00000	01112	10011	001??10
Morphospecies 4	010??	11000	02011	00000	01112	01100	00?10??
Morphospecies 5	010?1	12000	04011	00001	01111	00000	101??10

Two main clades were found within Megalostylus: clade I, including Megalostylus rhodopus and morphospecies 1 and 3 (considered belonging to M. rhodopus), is supported by 1 exclusive synapomorphy: elytral setae only present on the lateral edges of elytral disc (28:1). Clade II is supported by 1 exclusive synapomorphy and 1 non-exclusive synapomorphy: scales of scape separate, leaving integument exposed (6:1) and whitish or golden color of the verticillate setae of funicle (9:0), respectively. Within clade II, morphospecies2 is sister to the remaining species, which form a clade supported by 1 non-exclusive synapomorphy: pronotum subconical, sides slightly curved to straight and strongly divergent from apex to base (11:2). Megalostylus macrophthalmus is the sister species of M. tomentosus–M. sturmi var. villosus based on 1 non-exclusive synapomorphy: vestiture of scutellum present, scales similar in color to those covering the whole surface of elytra (25:0). Megalostylus tomentosus (along with morphospecies4) is the sister of a supported clade (BT 58) M. dilaticollis–M. sturmi var. villosus clade, which is supported by 3 exclusive synapomorphies and 1 non-exclusive synapomorphy: integument of legs with dark tones, black or brown (19:1), and width of base of scutellum reduced to indistinct (24:1), vestiture on legs inconspicuous, scales are scattered leaving integument exposed (30:1), and scales separated leaving integument of scape exposed (6:2). Within this clade M. dilaticollis (along with morphospecies 5) is sister to a subclade supported by 1 exclusive synapomorphy and 1 non-exclusive synapomorphy: presence of scales on the second funicular antennomere (8:1) and posterior margin of pronotum strongly bisinuate (17:1) that includes M. albicans and its varieties, M. albicans var. expansus, and var. farinosus sister to M. brevipilis to M. sturmi var. villosus clade supported by 1 exclusive synapomorphy and 1 non-exclusive synapomorphy: pronotum flared or bell-shaped (11:3) and lateral projections of posterior margin of pronotum strongly extended backward, towards elytral base (15:1). Within this clade, M. brevipilis and M. fusiformis are sisters to the M. splendidus–M. sturmi var. villosus clade which is supported by 2 non-exclusive synapomorphies: pronotum subconical, sides curved and strongly divergent from apex to base (11:1), and width of base of scutellum wider than interestria 2 (24:2). The clade M. splendidus–M. sturmi var. villosus also has unresolved relationships between M. splendidus and his variety, both sister to the M. sturmi + M. sturmi var. villosus clade. 

Geographic distribution. The maps (Figs. 7, 8) indicate that the species of Megalostylus are mostly distributed along the Pacific coast, with the greatest richness in the central and southern parts of the country. Megalostylus albicans shows the largest distribution,ranging from Oaxaca to Sinaloa. Six species are distributed in the central states of the country (Guanajuato, Guerrero, Michoacán, Morelos, and Puebla): M. albicans, M. brevipilis, M. dilaticollis, M. fusiformis, M. splendidus, and M. sturmi. The species M. rhodopus, M. macrophthalmus, and M. tomentosus are restricted to Oaxaca, and M. rhodopus reaches the southernmost distribution extending to the Isthmus of Tehuantepec. 

Discussion 

The sister group relationship between Megalostylodes and Megalostylus is well supported by 12 exclusive synapomorphies, and the monophyly of Megalostylus is supported by a combination of 4 exclusive synapomorphies of the protibiae, elytra, and female and male genitalia. Champion (1911) distinguished Megalostylus based on the presence of a prominence opposite to mucro (or toothed tibiae at the external apical angle), and Lanteri and del Río (2017) recovered this character state (car 69[1]) as an apomorphy of Megalostylus.

Within Megalostylus most of the relationships are not well supported nevertheless, it is clear the position of M. rhodopus (including morphospecies 1 and 3) as sister species of the remaining, and it was recovered a well-supported group including M. dilaticollis (= morphospecies 5), M. albicans, M. brevipilis, M. fusiformis, M. splendidus, and M. sturmi. Megalostylus macrophthalmus and M. tomentosus (= morphospecies 4) would be basal regarding this clade. Morphospecies2 is considered a probable new species, however, this status needs further studies. 

The species of Megalostylus are very variable in scale color, size and pronotum shape, and due to that intraspecific variation, some nominal species have been synonymized: M. farinosus Chevrolat, 1878 [junior synonym of M. albicans (Lacordaire, 1876)], M. expansus Pascoe, 1881 [junior synonym of M. albicans (Lacordaire, 1876)] and M. villosus Chevrolat, 1878 [junior synonym of M. sturmi Boheman, 1840]. Our analysis explored the relationships among intraspecific varieties of the genus Megalostylus, and the results support the previously established synonymies. In the case of M. albicans with its varieties (M. albicans var. expansus and M. albicans var. farinosus) there is no reason to consider them as different species. Characters with the greatest contribution to the species relationships are those referring mainly to the vestiture of antennae, legs, elytra, shape, and characteristics of the pronotum, scutellum, and apex of aedeagus.

Acknowledgments 

We thank all curators, institutions, collection managers, technicians, and collectors that provided specimens. We also thank Miguel Menéndez-Acuña, Elizabeth Arellano-Arenas, and anonymous reviewers for their helpful suggestions to improve the manuscript. The authors would like to express their sincerest gratitude to Santiago Zaragoza Caballero and María Cristina Mayorga Martínez for their invaluable assistance in providing material for examination. 

References 

Champion, G. C. (1911). Insecta. Coleoptera. Vol. IV, Parte 3. Rhynchophora. Curculionidae. Attelabinae, Pterocolinae, Allocoryninae, Apioninae, Thecesterninae, Otiorhynchinae. In D. Sharp, & G. Champion (Comps.), Biologia Centrali-Americana (pp. 241–246). London: R.H. Porter.

del Río, M. G. (2009). Estudio taxonómico y cladístico de los géneros de la tribu Naupactini (Coleoptera: Curculionidae) distribuidos en la subregión Páramo-Puneña o Zona de Transición Sudamericana (Ph.D. Thesis). Universidad Nacional de la Plata, La Plata, Argentina.

ESRI (2015). ArcGIS Desktop: Versión 10.4.1 Redlands, CA: Environmental Systems Research Institute.

Goloboff, P. A., & Catalano, S. A. (2016). TNT version 1.5, including a full implementation of phylogenetic morphometrics. Cladistics, 32, 221–238. https://dx.doi.org/10.1111/cla.12160 

Lanteri, A. A., & del Río, M. G. (2017). Phylogeny of the tribe Naupactini (Coleoptera: Curculionidae) based on morphological characters. Systematic Entomology, 42, 429–447. https://doi.org/10.1111/syen.12223 

Maddison, W. P., & Maddison, D. R. (2021). Mesquite: a modular system for evolutionary analysis. Versión 3.70. http://www.mesquiteproject.org 

Muñiz-Vélez, R., Burgos-Dueñas, A., Burgos-Dueñas, O., López-Martínez, V., & Burgos-Solorio, A. (2015). Nuevas aportaciones a los Curculionoidea del estado de Morelos, Folia Entomológica Mexicana, 1, 25–49.

Ordóñez-Reséndiz, M. M., Muñíz-Vélez R., & Gama-Rojas, F. (2008). Curculiónidos (Coleópteros). In S. Oceguera, & J. Llorente-Bousquets (Coords.), Catálogo taxonómico de especies de México, en Capital natural de México, vol. L. Conocimiento actual de la biodiversidad. CD1. Mexico City. Conabio.

Rosas, M. V., Morrone, J. J., del Río, M. G., & Lanteri, A. A. (2011). Phylogenetic analysis of the Pantomorus-Naupactus complex (Coleoptera: Curculionidae: Entiminae) from North and Central America. Zootaxa, 2780, 1–19. https://doi.org/10.11646/zootaxa.2780.1.1 

Schoenherr, C. J. (Ed). (1840). Genera et species curculionidum, cum synonymia hujus familiae; species novae aut hactenus minus cognitae. Paris: Roret.

Oscar Iván González-Romero ^a, Xochitl G. Vital ^{a, b,} *

^a Universidad Nacional Autónoma de México, Facultad de Ciencias, Circuito Exterior s/n, Ciudad Universitaria, Coyoacán, 04510 Ciudad de México, México

^b Universidad Nacional Autónoma de México, Posgrado en Ciencias Biológicas, Facultad de Ciencias, Circuito Exterior s/n, Ciudad Universitaria, Coyoacán, 04510 Ciudad de México, México 

*Corresponding autor: vital@ciencias.unam.mx (X.G. Vital)

Received: 18 August 2024; accepted: 5 February 2025

Abstract

While the diversity of sea slugs in the northern area of the Pacific coast of Mexico has been studied thoroughly in the last decades, little is known about the composition of species in the southern states of Mexico. Several field trips were made in 5 localities of Bahías de Huatulco, Oaxaca, where specialized sampling methods focused on sea slugs were carried out. Herein, we documented 49 species of sea slugs, including 37 new records for the state, which increases to 58 species the total sea slug richness known for Oaxaca. This study updates the inventory of sea slugs for the Mexican Pacific coast and contributes to the knowledge of the marine fauna of the Natural Protected Area “Parque Nacional Huatulco”.

Keywords: Bahías de Huatulco; Coral reefs; Molluscs; Nudibranchia; Tropical Eastern Pacific

Babosas marinas (Gastropoda: Heterobranchia) de Huatulco: nuevos registros y ampliaciones de distribución para Oaxaca, México

Resumen

Mientras que la diversidad de babosas marinas en la zona norte de la costa del Pacífico mexicano ha sido estudiada de forma exhaustiva en las últimas décadas, poco se sabe acerca de la composición de especies en los estados del sur de México. Se realizaron diversas visitas a 5 localidades de las bahías de Huatulco, Oaxaca, donde se llevaron a cabo métodos de muestreo especializados con enfoque en babosas marinas. Aquí censamos 49 especies de babosas marinas, con 37 nuevos registros para el estado, lo que incrementa la riqueza de babosas marinas conocida para Oaxaca a 58 especies. Este estudio actualiza el inventario de babosas marinas para la costa del Pacífico mexicano y contribuye al conocimiento de la fauna marina del Área Natural Protegida “Parque Nacional Huatulco”.

Palabras clave: Bahías de Huatulco; Arrecifes de coral; Moluscos; Nudibranchia; Pacífico este tropical

Introduction

Heterobranch sea slugs are gastropods with more than 8,400 described species distributed in all the oceans of the planet, from the intertidal zone to deep waters (Behrens et al., 2022; Camacho-García et al., 2005). Some of these molluscs can do some of the most exceptional processes in the metazoans, such as the incorporation of functional chloroplasts or nematocysts into their tissues (Goodheart & Bely, 2017; Händeler et al., 2009). Furthermore, sea slugs can be important model organisms in several study areas from neuroscience to global climate change (Kandel, 1979; Ziegler et al., 2014); a source of biomedical compounds used for creating novel drugs (Dean & Prinsep, 2017; Fisch et al., 2017) and an attractive target to professional and amateur underwater photographers worldwide (Behrens, 2005). 

More than 370 species of sea slugs have been recorded in the Eastern Pacific from Alaska to Central America (Behrens et al., 2022), of which around 234 have been found on the Mexican Pacific coast (Hermosillo et al., 2006). Although several studies on sea slugs have been performed in this region (e.g., Angulo-Campillo, 2005; Bertsch, 2014; Flores-Rodríguez et al., 2017; Hermosillo, 2009, 2011; Hermosillo & Behrens, 2005; Hermosillo & Gosliner, 2008; Verdín-Padilla et al., 2010), most of them are focused on the northern coast of Mexico, whereas the composition of species of the southern coast, corresponding to the states of Oaxaca and Chiapas, has been poorly recorded in faunal inventories. The current knowledge of Oaxaca’s sea slug fauna comes from 2 checklists of intertidal molluscs on rocky shores of the state (Holguín-Quiñones & González-Pedraza, 1989; Rodríguez-Palacios et al., 1988), a review of the sea slugs preserved at Colección Nacional de Moluscos (CNMO) from Universidad Nacional Autónoma de México (UNAM) (Zamora-Silva & Naranjo-García, 2008), and an ecological analysis of the richness and abundance of molluscs associated with coral ecosystems in the Tropical Eastern Pacific (Barrientos-Luján et al., 2021). Altogether, these studies sum up to 10 known species of Heterobranch sea slugs on the coastal shore of Oaxaca.

Biological inventories are a fundamental base that provides essential information for conservation strategies, such as establishing natural protected areas or monitoring their condition inside them (Alexander et al., 2009; Schejter et al., 2016). Marine molluscs are useful in rapid biodiversity assessments (Benkendorff & Davis, 2002), and they could serve as indicators of the total biological richness in marine reserves (Gladstone, 2002), which possibly extrapolates to different areas and types of habitats. Sea slugs are one of the most diverse groups within the marine molluscs. Nonetheless, they are apparently “rare in space and time” (Schubert & Smith, 2020), as they are not always recorded in the biological inventories due to their small size, their camouflage strategies and inadequate collecting methods applied on the field. This work aims to provide information on the diversity of sea slugs in the southern region of the Mexican Pacific coast, based on surveys conducted in different coral communities in Oaxaca. 

Materials and methods

Five localities of the bay complex known as Bahías de Huatulco, Oaxaca were selected for field studies: San Agustín (hereafter Agustín), La Entrega (hereafter Entrega), El Arrocito (hereafter Arrocito), Isla Montosa (hereafter Montosa) and Playa Conejos (hereafter Conejos). Agustín is located within the Natural Protected Area in the category of National Park “Parque Nacional Huatulco (PNH)” (Conanp, 2003) (Fig. 1, Table 1). This locality has a large and compact homogenous platform of coral colonies dominated by Pocillopora damicornis with patches of dead corals and rocks, similar to Entrega, which additionally has shallow zones of algal turf (López-Pérez & Hernández-Ballesteros, 2004; Ramírez-González, 2005). Arrocito’s substrate is composed of rocks overgrown by algal turf and dead coral fragments mostly in shallow environments, with few coralline formations and a high abundance of sponges. Conejos has big rocks with a sandy bottom and low presence of corals at shallow depths (Ramírez-González, 2005). Finally, Montosa is an island with mixed patches of corals, sand and large boulders as a dominant substrate (López-Pérez & Hernández-Ballesteros, 2004).

A total of 17 field trips were conducted between May 2017 and March 2018, 4 at each locality (except on Montosa, where we searched only once). Using snorkelling and SCUBA diving at maximum depths of 18 m, searches were conducted in subtidal environments on different substrates (Table 1). Most of the specimens were collected in all localities, when necessary, except in Agustín where photos, identification and measuring of the organisms were taken in situ. Additionally, different algal morphotypes where sea slugs may potentially be found were collected in all localities, excluding Agustín. The algae collected were placed in trays with low seawater level, then they were examined after 2 to 3 hours to find specimens attached to the tray walls (Urbano et al., 2019). All organisms were measured and photographed while they were alive and identified according to sea slug identification guides for the Pacific east coast (Behrens et al., 2022; Camacho-García et al., 2005; Hermosillo et al., 2006). Afterwards, the collected specimens were narcotized with magnesium chloride (MgCl₂), preserved with ethanol (96º) (Urbano et al., 2019) and deposited in Colección Nacional de Moluscos (CNMO), Instituto de Biología, UNAM. The nomenclature used in this work follows Bouchet et al. (2017) for supra-family and family categories and World Register of Marine Species (Horton et al., 2024) for genus and species categories. We present the new records for Oaxaca: number of organisms found per locality, their size, their collection number, distribution in the Pacific east coast and remarks of the species, as well as a brief description of undetermined species. 

Table 1

Collecting sites in Bahías de Huatulco: San Agustín, La Entrega, El Arrocito, Isla Montosa, Playa Conejos. Sampling technique: snorkelling (S), scuba diving (SD).

Locality	Latitude (N)	Longitude (W)	Sampling technique	Substrate composition
San Agustín	15°41.185’	96°14.254’	S	Compact coral colonies, rocks and dead coral patches
La Entrega	15°44.642’	96°07.732’	S, SD	Compact coral colonies, rocks, algae and dead coral patches
El Arrocito	15°45.672’	96°06.008’	S, SD	Rocks with algal turf, coral, sponges and dead coral patches
Isla Montosa	15°45.725’	96°05.120’	SD	Boulders, sand and corals
Playa Conejos	15°46.722’	96°03.853’	S	Boulders, sand and corals

Results

A total of 298 specimens belonging to 49 species (38 determined to species level, 10 to genus and 1 to family) were recorded from 5 localities in Bahías de Huatulco; the species were distributed in 22 families and 6 orders/superorders. Nudibranchia had the highest number of species (27), followed by Sacoglossa (10), Aplysiida (6), Pleurobranchida (3), and Cephalaspidea (2), while Umbraculida was represented only by 1 species. A list of the sea slugs recorded from Bahías de Huatulco in this study, complemented with the previous records from Oaxaca, is given in Table 2. 

Class Gastropoda Cuvier, 1795

Subclass Heterobranchia Gray, 1840

Infraclass Euthyneura Spengel, 1881

Cohort Ringipleura Kano, Brenzinger, Nützel, Wilson and Schrödl, 2016

Subcohort Nudipleura Wägele and Willan, 2000

Order Pleurobranchida Pelseneer, 1906

Family Pleurobranchidae Gray, 1827

Berthellina ilisima Ev. Marcus and Er. Marcus, 1967

(Fig. 2A) 

Material examined: 1 organism (18 mm), Entrega (CNMO8025).

Distribution: from Santa Barbara, California to Islas Galapagos, Ecuador (Behrens et al., 2022).

Remarks: animals with nocturnal habits and spongivorous diet (Valdés, 2019).

Berthella sp.

(Fig. 2B)

Material examined: 2 organisms (5, 8 mm), Arrocito (CNMO8274).

Distribution: El Arrocito, Bahías de Huatulco, Oaxaca (this study).

Diagnosis: translucent whitish body with numerous small opaque white dots and low rounded brown tubercles on the dorsum. Small translucent internal shell. The foot protrudes posteriorly from the mantle. The oral velum is triangular and the rolled rhinophores are partially fused. 

Remarks: organisms were found under rocks near white sponges. The observed characters in the specimens allowed their identification only to the genus level. Berthella andromeda, B. strongi and B. martensi are also distributed in the Pacific east coast; however, our specimens had a more translucent and white body than B. strongi and they did not present the opaque white transverse bar of B. andromeda (Ghanimi et al., 2020); the dots on the notum also were darker and more regular compared with B. martensi, which has a band along the edge of the mantle (Behrens et al., 2022).

Pleurobranchus digueti Rochebrune, 1895

(Fig. 2C)

Material examined: 3 organisms (15-20 mm), Entrega (CNMO8020); 1 organism (35 mm), Arrocito (CNMO8006); 1 organism (10 mm), Montosa (CNMO7965).

Distribution: from Santa Barbara, California to Islas Galapagos, Ecuador (Behrens et al., 2022).

Remarks: nocturnal animals hide under rocks during the day (Valdés, 2019).

Order Nudibranchia Cuvier, 1817

Family Dorididae Rafinesque, 1815

Dorididae sp.

(Fig. 2D)

Material examined: 1 organism (6 mm), Conejos (CNMO8261).

Distribution: Playa Conejos, Bahías de Huatulco, Oaxaca (this study).

Diagnosis: yellowish body, with an oval orange-brownish patch covering the dorsum and divided by a cream-whitish band that runs through the middle of the rhinophores all the way to the branchial area. The lamellated rhinophores and the gills are the same colour as the body.

Remarks: the specimen was found under rocks at approximately 3 m depth. The observed characters in the organism did not resemble any recorded species in the literature, but they allowed its identification up to the family level.

Doris sp.(Risbec, 1928)

(Fig. 2E)

Material examined: 1 organism (6 mm), Conejos (CNMO8260).

Distribution: Playa Conejos, Bahías de Huatulco, Oaxaca (this study).

Diagnosis: pale yellowish body with discontinued purple band between the rhinophores and the posterior area of the body. The animal had big tubercles in the central area of the dorsum with visible translucent spicules. Rhinophores were lamellated.

Remarks: specimen found on algae of the genus Caulerpa. This specimen resembles the organism illustrated in Behrens et al. (2022) as Doris immonda; however, the previous authors mention that this identification might not be valid due to its geographical distribution, as D. immonda was originally described for the Indo-Pacific. Also, the diagnosis of D. immonda in Gosliner et al. (2018) does not mention the purple band observed in this individual, these authors described a white opaque marking across the body instead. Therefore, we decided to include this species as Doris sp. until a further review of this taxon is made.

Family Discodorididae Bergh, 1891

Diaulula nayarita (Ortea & Llera, 1981)

(Fig. 2F)

Material examined: 1 organism (4 mm), Arrocito (CNMO7974).

Distribution: from Punta Eugenia, Baja California to Panama (Camacho-García et al., 2005).

Remarks: found under rocks near sponges of the same colour as the specimen.

Discodoris ketos (Marcus & Marcus, 1967)

(Fig. 2G)

Material examined: 1 organism (8 mm), Arrocito (CNMO8028).

Distribution: Gulf of California. Mexico to Islas Galapagos, Ecuador (Behrens et al., 2022).

Remarks: it is still unclear whether this species is the same as the circumtropical species Tayuva lilacina (Behrens et al., 2022). Discodoris ketos has a highly specialised diet, feeding on the sponge Haliclona caerulea (Verdín-Padilla et al., 2010).

Geitodoris mavis (Marcus & Marcus, 1967)

(Fig. 2H) 

Material examined: 1 organism (15 mm), Entrega (CNMO7964). 1 organism (13 mm), Arrocito (CNMO8029).

Distribution: from Rosarito, Baja California to Islas Galapagos, Ecuador (Behrens et al., 2022).

Remarks: live specimens darkened their gills when disturbed.

Family Polyceridae Alder and Hancock, 1845

Polycera anae Pola et al., 2014

(Fig. 2I)

Material examined: 2 organisms (8, 10 mm), Conejos (CNMO7981). 

Distribution: from Mexico to Costa Rica (Pola et al., 2014).

Remarks: found on algae of the genus Padina. Specimens found in this work exceed the maximum length of 5 mm reported for the species by Pola et al. (2014).

Polycera cf. hedgpethi Er. Marcus, 1964

(Fig. 2J)

Table 2

Sea slug fauna recorded from Oaxaca state based on this study and the literature. Localities: Puerto Ángel (PA), San Agustín (SA), El Maguey (EM), La Entrega (LE), El Arrocito (EA), Isla Montosa (IM), Playa Conejos (PC), Santa Cruz (SC), Not available data (ND). New records for the state (*). Only determined species in literature were included. References: ¹Holguín-Quiñones and González-Pedraza (1989); ²Rodríguez-Palacios et al. (1988); ³Zamora-Silva and Naranjo-García (2008); ⁴Barrientos-Luján et al. (2021); ⁵This study.

Family	Species	PA	SA	EM	LE	EA	IM	PC	SC	ND	Reference
Pleurobranchidae	Berthellina ilisima*				•						5
	Berthella sp.					•					5
	Pleurobranchus digueti*				•	•	•				5
Dorididae	Dorididae sp.							•			5
	Doris sp.							•			5
Discodorididae	Diaulula nayarita*					•					5
	Diaulula sandiegensis	•									2
	Discodoris ketos*					•					5
	Geitodoris mavis*				•	•					5
Polyceridae	Polycera anae*							•			5
	Polycera cf. hedgpethi*						•				5
	Tambja abdere*						•				5
Chromodorididae	Felimida sphoni*				•	•		•			5
	Chromolaichma dalli*		•				•	•			5
	Chromolaichma sedna*					•	•				5
	Felimare agassizii*		•		•	•	•				5
Cadlinidae	Cadlina sp.				•	•		•			5
Dendrodorididae	Dendrodoris krebsii			•							2
	Doriopsilla janaina*		•		•			•			5
Tritoniidae	Tritonia festiva	•									2
Hancockiidae	Hancockia californica*					•					5
Flabellinidae	Coryphellina marcusorum*						•				5
	Samla telja*		•		•	•	•				5
Cuthonidae	Cuthona divae	•									2
	Cuthona sp. 1					•					5
	Cuthona sp. 2		•								5
Aeolidiidae	Bulbaeolidia sulphurea*					•					5
	Anteaeolidiella chromosoma*					•		•			5
	Anteaeolidiella ireneae*				•						5
	Baeolidia moebii*		•								5
	Limenandra confusa*		•			•					5
	Spurilla braziliana*					•					5
Facelinidae	Favorinus elenalexiarum*				•	•					5
	Phidiana lascrucensis*		•		•	•	•	•			5
Tylodinidae	Tylodina fungina*					•					5
Table 2. Continued
Bullidae	Bulla punctulata									•	1
	Bulla gouldiana									•	4
Haminoeidae	Haminoea sp.		•			•					5
	Aliculastrum exaratum									•	4
Aglajidae	Navanax aenigmaticus*		•		•	•					5
Aplysiidae	Aplysia cf. cedrosensis*							•			5
	Aplysia californica				•						2
	Aplysia hooveri*		•		•	•		•			5
	Dolabella cf. auricularia*		•		•						5
	Dolabella californica				•						2
	Dolabrifera nicaraguana*				•						5
	Phyllaplysia padinae*							•			5
	Stylocheilus rickettsi*				•	•					5
Oxynoidae	Lobiger cf. souverbii*				•			•			5
	Oxynoe aliciae*				•						5
Plakobranchidae	Elysia diomedea		•		•	•		•	•		3, 5
	Elysia cf. pusilla*					•		•			5
	Elysia sp. 1					•	•	•			5
	Elysia sp. 2		•		•	•		•			5
Limapontiidae	Placida cf. dendritica*				•						5
Hermaeidae	Polybranchia mexicana*							•			5
	Caliphylla sp.				•						5
	Hermaea sp.				•						5
	Total	3	14	1	25	27	10	18	1	3

Material examined: 1 organism (14 mm), Montosa. Photographic record only.

Distribution: from Puerto Peñasco, Mexico to Islas Galapagos, Ecuador (Behrens et al., 2022).

Remarks: found on rocks with bryozoan colonies. Behrens et al. (2022) treat this species as Polycera gnupa; however, it is unclear if this nudibranch is different from the widespread species P. hedgpethi.

Tambja abdere Farmer, 1978

(Fig. 3A) 

Material examined: 1 organism (42 mm), Montosa (CNMO7966).

Distribution: from the Gulf of California, Mexico to Costa Rica (Behrens et al., 2022).

Remarks: the specimen was found on rocks at approximately 13 m depth. According to Hermosillo (2007), T. abdere feeds on the bryozoan Sessibugula translucens which lives in zones with low currents.

Family Chromodorididae Bergh, 1891

Felimida sphoni Ev. Marcus, 1971

(Fig. 3B)

Material examined: 1 organism (5 mm), Entrega (CNMO8270). Three organisms (8-14 mm), Arrocito (CNMO8262, CNMO8272). Three organisms (9-12 mm), Conejos (CNMO8263, CNMO8265). 

Distribution: from the Gulf of California, Mexico to Ecuador (Behrens et al., 2022).

Remarks: animals were found under rocks near to different unidentified sponges.

Chromolaichma dalli (Bergh, 1879)

(Fig. 3C)

Material examined: 5 organisms (17-32 mm), Montosa (CNMO8259). One organism (5 mm), Conejos (CNMO8264).

Distribution: from Islas San Benito, Baja California to Islas Galapagos, Ecuador (Behrens et al., 2022).

Remarks: larger specimens were found at approximately 15 m depth. Matsuda and Gosliner (2018) categorized C. dalli under a temporal nomenclatural name that needs further taxonomic analysis. 

Chromolaichma sedna (Ev. Marcus & Er. Marcus, 1967)

(Fig. 3D)

Material examined: 1 organism (31 mm), Montosa (CNMO8278).

Distribution: from the Gulf of California, Mexico to Ecuador (Behrens et al., 2022).

Remarks: Verdín-Padilla et al. (2010) reported that C. sedna is a polyphagous species that may feed on 16 sponge species. 

Felimare agassizii (Bergh, 1894)

(Fig. 3E)

Material examined: 2 organisms (9, 32 mm), Entrega (CNMO8276, CNMO8281). Four organisms (32-55 mm), Arrocito (CNMO8279, CNMO8280, CNMO8282, CNMO8283). One organism (14 mm), Montosa (CNMO8275).

Distribution: from the Gulf of California, Mexico to Islas Galapagos, Ecuador (Behrens et al., 2022).

Remarks: Verdín-Padilla et al. (2010) reported that F. agassizii has a polyphagous diet feeding on 9 sponge species.

Family Cadlinidae Bergh, 1891

Cadlina sp.

(Fig. 3F)

Material examined: 5 organisms (4-5 mm), Entrega. One organism (3 mm), Arrocito. Two organisms (4 mm), Conejos. Photographic record only.

Distribution: from Baja California, Mexico to Panama (Behrens et al., 2022).

Diagnosis: oval translucent white body with 4-5 rounded yellow glands around the mantle at each side of the body, simulating an inner semi-oval. The rhinophores are white with a red band in the centre. 

Remarks: the specimens were found on white sponges. Specimens resemble Cadlina sp. in Camacho-García et al. (2005), Bertsch and Aguilar Rosas (2016) and Behrens et al. (2022). This undescribed species has been reported in several locations for the Pacific east coast such as Islas Tres Marías (Hermosillo, 2009), Revillagigedo (Hermosillo & Gosliner, 2008), Bahía de Banderas (Hermosillo, 2011), Acapulco (Flores-Rodríguez et al., 2017) and Costa Rica (Camacho-García et al., 2005).

Family Dendrodorididae O’Donoghue, 1924 (1864)

Doriopsilla janaina Er. Marcus and Ev. Marcus, 1967

(Fig. 3G)

Material examined: 1 organism (18 mm), Entrega (CNMO8022). Two organisms (13, 28 mm), Conejos (CNMO8014, CNMO7985). 

Distribution: from Baja California, Mexico to Islas Galapagos, Ecuador (Behrens et al., 2022).

Remarks: 1 specimen was found on brown algae. Although there are reports of the gregarious behaviour of these animals (Hermosillo et al., 2006), they were found individually in our surveys. 

Suborder Cladobranchia

Family Hancockiidae MacFarland, 1923

Hancockia californica MacFarland, 1923

(Fig. 3H)

Material examined: 3 organisms (5-11 mm), Arrocito (CNMO7968).

Distribution: from Big Lagoon, California to Costa Rica (Behrens et al., 2022).

Remarks: the specimens were found on green algae. Even though the 3 specimens were collected on the same algae, they presented colour variations in their bodies, from transparent brown to reddish-brown. 

Family Flabellinidae Bergh, 1889

Coryphellina marcusorum (Gosliner & Kuzirian, 1990)

(Fig. 3I)

Material examined: 6 organisms (6-18 mm), Montosa (CNMO7976).

Distribution: from Isla San Diego, Baja California to Islas Galapagos, Ecuador (Behrens et al., 2022).

Remarks: specimens were observed at more than 15 m depth. Animals feed on hydroids of the genus Eudendrium (Camacho-García et al., 2005).

Samla telja (Ev. Marcus & Er. Marcus, 1967)

(Fig. 4A)

Material examined: 1 organism (9 mm), Arrocito (CNMO7971). One organism (8 mm), Montosa (CNMO7967).

Distribution: from Puerto Peñasco, Mexico to Islas Galapagos, Ecuador (Behrens et al., 2022).

Remarks: organisms found on hydroids during daytime as reported by Behrens (2022).

Family: Cuthonidae Odhner, 1934

Cuthona sp. 1

(Fig. 4B)

Material examined: 1 organism (3 mm), Arrocito. Photographic record only.

Distribution: from Puerto Vallarta, Mexico to Islas Catalinas, Costa Rica (Camacho-García et al., 2005).

Diagnosis: translucent whitish body with several opaque white spots. The cerata are globose and have longitudinal yellowish lines with a reddish colour on the base. The smooth rhinophores and the oral tentacles are white coloured on the tips and have a reddish-brown band on the base.

Remarks: juvenile specimen found on hydroids with S. telja individuals. Our species diagnosis match Cuthona sp. 3 in Camacho-García et al. (2005). Before this work, this undescribed species had been reported only in 2 localities that correspond to its geographic distribution limits. 

Cuthona sp. 2

(Fig. 4C)

Material examined: 1 organism (5 mm), Agustín. Photographic record only.

Distribution: San Agustín, Bahías de Huatulco, Oaxaca (this study).

Diagnosis: light orange body with multiple little white spots. The pericardial area is swollen and has a distinctive white patch. The cerata colour base is brown with several little yellow dots. The smooth rhinophores have orange freckles and an orange band near the tips. The oral tentacles are shorter than the rhinophores and have 2 distinctive orange bands, 1 on the base and the other near the centre.

Remarks: the animal was found near egg masses, possibly just laid by the observed specimen. The observed characters in the organism allowed its identification only to the genus level. Specimen diagnosis did not match any recorded species in the literature.

Family Aeolidiidae Gray, 1827

Bulbaeolidia sulphurea Caballer and Ortea, 2015

(Fig. 4D)

Material examined: 4 organisms (4-12 mm), Agustín (CNMO7975, CNMO7995, CNMO8001).

Distribution: from Puerto Vallarta, Mexico to Islas Galapagos, Ecuador (Behrens et al., 2022).

Remarks: 1 specimen was found on green algae. This species feeds on anemones (Behrens et al., 2022).

Anteaeolidiella chromosoma (Cockerell & Eliot, 1905)

(Fig. 4E)

Material examined: 8 organisms (15-22 mm), Agustín (CNMO7973, CNMO8002, CNMO8005).

Distribution: from Morro Bay, California to Islas Galapagos, Ecuador (Camacho-García et al., 2005).

Remarks: specimens were found under rocks and near coral polyps.

Anteaeolidiella ireneae Carmona et al., 2014

(Fig. 4F)

Material examined: 1 organism (21 mm), Entrega (CNMO8017).

Distribution: from Isla Socorro, Mexico to Panama (Carmona et al., 2014a).

Remarks: feeds on anemones (Behrens et al., 2022).

Baeolidia moebii Bergh, 1888

(Fig. 4G)

Material examined: 1 organism (27 mm), Agustín. Photographic record only.

Distribution: from the Gulf of California, Mexico to Panama (Hermosillo et al., 2006).

Remarks: found under bivalve shells in shallow water (2 m).

Limenandra confusa Carmona et al., 2014

(Fig. 4H)

Material examined: 2 organisms (16, 18 mm), Arrocito (CNMO8033).

Distribution: from the Gulf of California, Mexico to Costa Rica (Carmona et al., 2014c).

Remarks: Carmona et al. (2014c) report that this species feeds on small anemones.

Spurilla braziliana MacFarland, 1909

(Fig. 4I)

Material examined: 1 organism (24 mm), Arrocito. Photographic record only.

Distribution: from Baja California Sur, Mexico to Colombia (Behrens et al., 2022).

Remarks: Carmona et al. (2014b) confirmed that S. braziliana is a widespread species and its presence in the Pacific east coast is probably due to human introduction. 

Family Facelinidae Bergh, 1889

Favorinus elenalexiarum García and Troncoso, 2001

(Fig. 5A)

Material examined: 1 organism (4 mm), Entrega. 1 organism (12 mm), Arrocito. Photographic record only.

Distribution: from the Gulf of California, Mexico to Islas Galapagos, Ecuador (Behrens et al., 2022).

Remarks: specimens found near Aplysia egg masses.

Phidiana lascrucensis Bertsch and Ferreira, 1974

(Fig. 5B)

Material examined: 1 organism (9 mm), Entrega (CNMO7998). Two organisms (8, 12 mm), Arrocito (CNMO7969, CNMO8003). One organism (24 mm), Montosa (CNMO8036). Five organisms (10-21 mm), Conejos (CNMO7980, CNMO8035). 

Distribution: from Baja California, Mexico to Panama (Behrens et al., 2022).

Remarks: organisms found under rocks, often observed near specimens of Chiton albolineatus. 

Cohort Tectipleura Schrödl, Jörger, Klussmann-Kolb and Wilson, 2011

Subcohort Euopisthobranchia Jörger, Stöger, Kano, Fukuda, Knebelsberger and Schrödl, 2010

Order Umbraculida, Odhner, 1939

Family Tylodinidae Gray, 1847

Tylodina fungina Gabb, 1865

(Fig. 5C)

Material examined: 2 organisms (6, 8 mm), Arrocito (CNMO7994, CNMO8030).

Distribution: from Baja California, Mexico to Islas Galapagos, Ecuador (Hermosillo et al., 2006).

Remarks: Tylodina fungina has a highly specialist diet, feeding on the sponge Aiolochroia thiona and Aplysina gerardogreeni (Behrens et al., 2022; Verdín-Padilla et al., 2010).

Order Cephalaspidea Fischer, 1883

Family Haminoeidae Pilsbry, 1895

Haminoea sp. 

(Fig. 5D)

Material examined: 2 organisms (8, 10 mm), Arrocito (CNMO7958). 

Distribution: from Bahía de Banderas, Mexico to Peru (Behrens et al., 2022).

Diagnosis: body oval. White cream body, with irregular dark brown patches. The animals have an inverted “V” stain in the cephalic area between the eyes. The body is surrounded by multiple orange and light brown dots.

Remarks: specimens found on marine brown cyanobacteria. This species was firstly identified as the Indo-Pacific species Lamprohaminoea ovalis by Valdés and Camacho-García (2004). However, recently phylogenetic analysis has shown that the specimens in the Pacific east coast are an undescribed species more related to the Atlantic and Pacific species of the genus Haminoea (Oskars & Malaquias, 2019, 2020).

Family Aglajidae Pilsbry, 1895

Navanax aenigmaticus (Bergh, 1893)

(Fig. 5E)

Material examined: 5 organisms (30-44 mm), Entrega (CNMO7996, CNMO7999, CNMO8007). Two organisms (21, 33 mm), Arrocito (CNMO8032). 

Distribution: from Baja California, Mexico to Chile (Behrens et al., 2022).

Remarks: collected specimens presented different body colour variations from black, brown, and pink with cream or whitish spots. According to Ornelas-Gatdula et al. (2012), colouration differences on N. aenigmaticus could be probably influenced by environmental factors.

Order Aplysiida

Family Aplysiidae Lamarck, 1809

Aplysia cf. cedrosensis

(Fig. 5F)

Material examined: 1 organism (22 mm), Conejos (CNMO7978).

Distribution: from Bahía de los Angeles, Baja California to Playa Conejos, Bahías de Huatulco, Oaxaca.

Remarks: juvenile specimen found under rocks near red algae. Our diagnosis matched the species A. cedrosensis in Hermosillo et al. (2006). However, Behrens et al. (2022) state that this species might be a synonym of the California black sea hare Aplysia vaccaria. Before this work, the southern distribution of A cedrosensis in the Pacific east coast was reported for Parque de la Reina, Acapulco (Flores-Rodríguez et al., 2017), approximately 440 km northeast from Playa Conejos, Oaxaca.

Aplysia hooveri Golestani et al., 2019

(Fig. 5G)

Material examined: 72 organisms (3-16 mm), Entrega (CNMO7961-7963, CNMO7986, CNMO8010, CNMO8021, CNMO8026, CNMO8034). Two organisms (6, 7 mm), Arrocito (CNMO7972). Five organisms (5-12 mm), Conejos (CNMO7982, CNMO7993). 

Distribution: from Baja California, Mexico to Islas Galapagos, Ecuador (Valdés, 2019).

Remarks: this species was highly abundant in some localities of the study area; it was usually associated with red and brown algae. 

Dolabella cf. auricularia (Lightfoot, 1786)

(Fig. 5H)

Material examined: 1 organism (180 mm), Agustín. One organism (210 mm), Entrega. Photographic record only.

Distribution: from the Gulf of California, Mexico to Ecuador (Zamora-Silva & Naranjo-García, 2008).

Remarks: found on algae at approximately 10 m depth. According to Behrens et al. (2022) there is molecular evidence that confirms that Dolabella auricularia is a species complex.

Dolabrifera nicaraguana Pilsbry, 1896

(Fig. 5I)

Material examined: 1 organism (14 mm), Entrega (CNMO7960).

Distribution: from Bahía de las Cruces, Baja California to Tumbes, Peru (Valdés et al., 2018).

Remarks: cryptic specimen found on rhodolith beds. 

Phyllaplysia padinae Williams and Gosliner, 1973

(Fig. 6A) 

Material examined: 4 organisms (8-18 mm), Conejos (CNMO8277, CNMO8268, CNMO8269).

Distribution: from the Gulf of California, Mexico to Islas Galapagos, Ecuador (Camacho-García et al., 2005).

Remarks: the specimens were found attached to algae of the genera Padina and Caulerpa.

Stylocheilus rickettsi (MacFarland, 1966)

(Fig. 6B)

Material examined: 29 organisms (5-29 mm), Entrega (CNMO7959, CNMO7997, CNMO8008, CNMO8018, CNMO8023, CNMO8024, CNMO8027). Five organisms (6-38 mm), Arrocito (CNMO7957, CNMO7970). 

Distribution: from Baja California, Mexico to Islas Galapagos, Ecuador (Bazzicalupo et al., 2020).

Remarks: the specimens were found on rocks and on different unidentified green, red, and brown algae. 

Subcohort Panpulmonata Jörge et al., 2010

Superorder Sacoglossa Ihering, 1876

Family Oxynoidae Stoliczka, 1868 (1847)

Lobiger cf. souverbii Fischer, 1857

(Fig. 6C)

Material examined: 1 organism (6 mm), Entrega (CNMO8015). One organism (9 mm), Conejos (CNMO7983). 

Distribution: Baja California Sur, Mexico to Islas Galapagos, Ecuador (Behrens et al., 2022). 

Remarks: specimens were found associated with algae of the genus Caulerpa as mentioned in the literature (Behrens et al., 2022; Camacho-García et al., 2005). Due to the original description of L. souverbii in the Caribbean region, this sacoglossan is suspected to be a different species.

Oxynoe aliciae Krug et al., 2018

(Fig. 6D)

Material examined: 6 organisms (4-9 mm), Entrega (CNMO8009, CNMO8016).

Distribution: from Baja California Sur, Mexico to Islas Galapagos, Ecuador (Behrens et al., 2022).

Remarks: specimens found as hosts on the algae Caulerpa as mentioned by Krug et al. (2018). 

Family Plakobranchidae Gray, 1840

Elysia cf. pusilla (Bergh, 1871)

(Fig. 6E)

Material examined: 3 organisms (8-11 mm), Arrocito (CNMO8004). Ten organisms (8-10 mm), Conejos (CNMO7977, CNMO8000, CNMO8013). 

Distribution: from Mexico to Costa Rica (Behrens et al., 2022).

Remarks: cryptic specimens were found attached to algae of the genus Halimeda as mentioned in the literature (Behrens et al., 2022; Camacho-García et al., 2005). This species is presumed to be different from E. pusilla, which was originally described in the Indo-Pacific region (Behrens et al., 2022).

Elysia sp. 1

(Fig. 6F)

Material examined: 4 organisms (6-10 mm), Arrocito. Twenty-seven organisms (5-14 mm), Conejos. Photographic record only.

Distribution: from Bahía de Banderas, Mexico to Panama (Hermosillo et al., 2006).

Diagnosis: elongated olive-greenish body. The rolled rhinophores are yellow whitish with light brown patches. The parapodia are strongly folded with an opening in the centre. Some specimens have a white spot in the base of the rhinophores. 

Remarks: specimens were found associated with algae of the genus Halimeda. Our diagnosis resembles the species Elysia sp. 1 in Camacho-García et al. (2005) and Hermosillo et al. (2006). There are numerous records of this undescribed species in the Pacific east coast: Bahía de Banderas (Hermosillo, 2011), Ixtapa, Guerrero (Hermosillo & Behrens, 2005), Papagayo and Parque de la Reina, Acapulco (Flores-Rodríguez et al., 2017), Playa Avellanas and San Pedrillo, Costa Rica (Camacho-García et al., 2005) and Panama (Hermosillo et al., 2006). 

Elysia sp. 2

(Fig. 6G)

Material examined: 4 organisms (13-24 mm), Entrega. Two organisms (19, 22 mm), Arrocito. 8 organisms (12-24 mm), Conejos. Photographic record only.

Distribution: from Islas Revillagigedo, Mexico to Costa Rica (Behrens et al., 2022).

Diagnosis: elongated light-greenish body with several white and dark green specks. The rhinophores are smooth, large, and rolled. The convoluted parapodia are folded with several rounded whitish papillae on the edges. Adult specimens have a purple-pinkish colouration along the margin of the parapodia and in the basis of the rhinophores.

Remarks: some specimens were found on red and green algae of the genus Halimeda and Caulerpa. Our diagnosis matched the species Elysia sp. 2 in Camacho-García et al. (2005) and Elysia sp. in Behrens et al. (2022). This undescribed species was previously documented in multiple locations in the Pacific east coast: Bahía de Banderas (Hermosillo, 2011), Islas Revillagigedo (Hermosillo & Gosliner, 2008), Isla Clipperton (Kaiser, 2007), Ixtapa, Guerrero (Hermosillo & Behrens, 2005) and Costa Rica (Camacho-García et al., 2005). 

Family Limapontiidae Gray, 1847

Placida cf. dendritica (Alder and Hancock, 1843)

(Fig. 6H)

Material examined: 3 organisms (3-5 mm), Entrega (CNMO8019).

Distribution: from the Gulf of California to La Entrega, Bahías de Huatulco, Oaxaca.

Remarks: specimens were found on algae of the genus Bryopsis. Before this work, the southern distribution of P. dendritica in the Pacific east coast was known for Bahía de Banderas, Nayarit (Hermosillo, 2011), approximately 1,200 km northeast from La Entrega, Oaxaca. It is suspected that P. dendritica might be a species complex that encompasses 2 different species in the region (Behrens et al., 2022).

Family Hermaeidae H. Adams and A. Adams, 1854

Polybranchia mexicana Medrano et al., 2018

(Fig. 6I)

Material examined: 1 organism (48 mm), Conejos (CNMO7992).

Distribution: from Baja California, Mexico to Islas Galapagos, Ecuador (Medrano et al., 2018).

Remarks: specimen found under rocks at daylight supporting the reports of the nocturnal habits of the species (Behrens et al., 2022).

Caliphylla sp.

(Fig. 6J)

Material examined: 4 organisms (5-14 mm), Entrega. Photographic record only.

Distribution: from La Entrega, Mexico to Islas Galapagos, Ecuador.

Diagnosis: elongated translucent green body with multiple little dark green and white dots. The bifid rhinophores, the head and the cerata have visible dark green ramified digestive branches. The elongated cerata are flattened and pointed. Some specimens may have a white speck between the eyes and in the posterior part of the head.

Remarks: some specimens were found on algae of the genus Bryopsis. Our diagnosis coincides with the undescribed species Caliphylla sp. in Camacho-García et al. (2005), which has been previously reported in a few localities from Costa Rica and Ecuador.

Hermaea sp.

(Fig. 6K)

Material examined: 1 organism (5 mm), Entrega. Photographic record only.

Distribution: from La Entrega, Oaxaca, Mexico to Playa Real, Guanacaste, Costa Rica.

Diagnosis: cream coloured body with multiple dark green flecks. Rhinophores are auriculate. The arrow-head shape cerata are covered with several white dots and red-brownish ramified digestive branches are visible throughout.

Remarks: the specimen was found on filamentous red algae. Our diagnosis resembles the species Hermaea sp. 3 in Camacho-García et al. (2005), which has been previously reported in Costa Rica.

Discussion

In this study we added 48 sea slug records, increasing by 83% the knowledge of sea slugs’ diversity for Oaxaca, from 10 to 58 species (Table 2). Also, the records presented in this study represent almost 11% of the total sea slug species previously known for the Eastern Pacific, from Alaska to Peru (Behrens et al., 2022). Among the sea slug fauna from Oaxaca, the order Nudibranchia is the most diverse encompassing more than half of the registered species, which is a general trend observed worldwide and in other localities from the Tropical Eastern Pacific (TEP) (García-Méndez & Camacho-García, 2016; Gosliner, 1991; Hermosillo, 2004; Spalding et al., 2007), and might be explained due to phylogenetic, historical and functional variables within the group (Bertsch, 2010). In contrast with other localities on the Pacific coast of Mexico (Table 3), the total number of species recorded in Oaxaca is similar to those reported for Isla Tres Marías, Nayarit (52 spp.), which is a relatively lower species richness compared with other works that involve higher sampling effort and/or more extensive study areas (Angulo-Campillo, 2005; Bertsch, 2014; Hermosillo, 2011; Hermosillo & Behrens, 2005). Moreover, the percentage of shared species between Revillagigedo, Colima and Oaxaca is higher (57.1%) than in other localities; however, this amount could be inaccurate due to the underestimated sea slug diversity in Islas Revillagigedo pointed out by Hermosillo and Gosliner (2008).

Overall, almost all the new sea slug records in this study are endemic to the Panamic biogeographic province (Briggs & Bowen, 2012), with some exceptions previously remarked that are also distributed on the Western Atlantic and/or the Indo-Pacific regions. Most of these exceptions belong to species complex that have not been resolved yet (Behrens et al., 2022), but others have a widespread natural distribution, or they have been introduced possibly by humans’ influence, as it has been suggested for S. braziliana (Carmona et al., 2014b). Interestingly, all the species previously reported for Oaxaca by Rodríguez-Palacios et al. (1988) (see Table 2) are not distributed in the Panamic province nor any warm waters of the Pacific east coast. Therefore, these records should be treated with caution as these species might have been misidentified due to the lack of specific field guides and accessible literature related with the sea slug fauna for this region in the past. 

Coral reef communities, including those inhabiting the TEP, are one of the most thriving habitats for sea slugs, as they encompass a net of biological associations that increase their diversity and inherent productivity (Sanvicente-Añorve et al., 2012; Sreeraj et al., 2013). In general, we found a higher species richness in localities with greater heterogeneity in their substrate composition (Table 1), possibly providing more habitats for sea slugs to succeed in this area. San Agustín, which is inside a Natural Protected Area, did not show a higher species richness compared to other localities. However, the number of species in this locality is underestimated, as we could not perform algae collection as an indirect search method; additionally, other variables need to be analysed to determine whether there is a significant difference in the sea slug diversity between protected and non-protected areas.

The continuous discovery of undescribed sea slug species in the TEP, such as the ones reported in this work: Berthella sp., Dorididae sp., Doris sp., and Cuthona sp. 2 has been a common issue, even in recent years. Phylogenetic and systematic studies have helped to elucidate the status of certain sea slug taxa (e.g., Bazzicalupo et al., 2020; Golestani et al., 2019; Krug et al., 2018; Medrano et al., 2018; Valdés et al., 2018), and represent important efforts to better understand the diversity of the sea slug fauna in the TEP. Nonetheless, there are species recorded more than a decade ago, such as Cadlina sp., Cuthona sp. 1, Elysia sp. 1, Elysia sp. 2, Caliphylla sp. and Hermaea sp. that remain undescribed. In the same way, some studies have found uncertainties in described species related to their geographic distribution. For instance, Behrens et al. (2022) state that Aplysia cf. cedrosensis and Placida cf. dendritica are given names that belong to 2 or more undescribed species that inhabit different biogeographic provinces. The extension of the distribution for those species reported in this work could confirm that they are different species indeed, and further taxonomic studies regarding the description and distribution of each species need to be done.

Table 3

Studies on sea slug diversity from the Pacific coast of Mexico. Shared species refer to those species present in other localities and this study (Huatulco).

Locality	Number of species	Number of shared species (%)	Reference
Bahía de los Angeles, Baja California	117	26 (22.2)	Bertsch (2014)
Baja California Sur	117	31 (26.4)	Angulo-Campillo (2005)
Bahía de Banderas, Nayarit-Jalisco	146	44 (30.1)	Hermosillo (2011)
Islas Tres Marías, Nayarit	52	27 (51.9)	Hermosillo (2009)
Revillagigedo, Colima	42	24 (57.1)	Hermosillo and Gosliner (2008)
Colima, Michoacán and Guerrero	76	38 (50)	Hermosillo and Behrens (2005)
Acapulco, Guerrero	63	27 (42.8)	Flores-Rodríguez et al. (2017)

This study updates the knowledge of the sea slug fauna of Oaxaca and the southern Pacific coast of Mexico; however, many unexplored localities in this region still need to be studied. Since this region could be a potential hotspot of marine biodiversity (Bastida-Zavala et al., 2013), further efforts to find sea slugs are needed. Future samplings involving SCUBA diving on different habitats such as lagoons, mangroves, and rocky shores at different times of the day may help to increase this inventory. This work also contributes to the biological inventory of Parque Nacional Huatulco, which is essential to determine future perspectives in the conservation planning and management of this and other Natural Protected Areas (Bezaury-Creel & Gutiérrez, 2009).

Acknowledgements

We thank Parque Nacional Huatulco for allowing us the entrance to perform the surveys in the locality of San Agustín; OGR acknowledges Comisión Nacional de Becas de Educación Superior, SEP for the financial support as an undergraduate student; XGV acknowledges Consejo Nacional de Ciencia y Tecnología (Conacyt) her PhD scholarship (CVU: 564148). We thank A. Valdés, P. Krug and S. Medrano, who helped with the identification of some organisms, and E. Naranjo-García for providing a space to work in her laboratory. We thank F. Pérez, M. Pérez, and M. A. Arriaga for their hospitality and support in performing this study; to the staff of “Buceo Anfibios Huatulco” and all the people who helped us in the surveys, especially E. Molina, L. Jiménez, A. García and A. Barrera.

References

Alexander, T. J., Barrett, N., Haddon, M., & Edgar, G. (2009). Relationships between mobile macroinvertebrates and reef structure in a temperate marine reserve. Marine Ecology Progress Series, 389, 31–44. https://doi.org/10.3354/meps08210

Angulo-Campillo, O. (2005). A four-year survey of the opisthobranch fauna (Gastropoda, Opisthobranchia) from Baja California Sur. Vita Malacologica, 3, 43–50.

Barrientos-Luján, N. A., Rodríguez-Zaragoza, F. A., & López-Pérez, A. (2021). Richness, abundance and spatial heterogeneity of gastropods and bivalves in coral ecosystems across the Mexican Tropical Pacific. Journal of Molluscan Studies, 87, eyab004. https://doi.org/10.1093/mollus/eyab004 

Bastida-Zavala, J. R., García-Madrigal, M. S., Rosas-Alquicira, E. F., López-Pérez, R. A., Benítez-Villalobos, F., Meraz-Hernando, J. F. et al. (2013). Marine and coastal biodiversity of Oaxaca, Mexico. Check List, 9, 329–390. https://doi.org/10.15560/9.2.329 

Bazzicalupo, E., Crocetta, F., Gosliner, T. M., Berteaux-Lecellier, V., Camacho-García, Y. E., Sneha Chandran, B. K. et al. (2020). Molecular and morphological systematics of Bursatella leachii de Blainville, 1817 and Stylocheilus striatus Quoy & Gaimard, 1832 reveal cryptic diversity in pantropically distributed taxa (Mollusca: Gastropoda: Heterobranchia). Invertebrate Systematics, 34, 535–568. https://doi.org/10.1071/IS19056 

Behrens, D. W. (2005). Nudibranch behaviour. Jacksonville, FL: New World Publications.

Behrens, D. W., Fletcher, K., Hermosillo, A., & Jensen, G. C. (2022). Nudibranchs and sea slugs of the Eastern Pacific. Bremerton, Washington: MolaMarine.

Benkendorff, K., & Davis, A. R. (2002). Identifying hotspots of molluscan species richness on rocky intertidal reefs. Biodiversity and Conservation, 11, 1959–1973. https://doi.org/10.1023/A:1020886526259 

Bertsch, H. (2010). Biogeography of Northeast Pacific opisthobranchs: comparative faunal province studies between Point Conception, California, USA, and Punta Aguja, Piura, Perú. In L. J. Rangel-Ruiz, J. Gamboa-Aguilar, S. L. Arriaga-Weiss, & W. M. Contreras Sánchez (Eds.), Perspectivas en malacología mexicana (pp. 219–259). Villahermosa: División Académica de Ciencias Biológicas, Universidad Juárez Autónoma de Tabasco.

Bertsch, H. (2014). Biodiversity in the Reserva de la Biosfera Bahía de los Ángeles y Canales de Ballenas y Salsipuedes: naming of a new genus, range extensions and new records, and species list of Heterobranchia (Mollusca: Gastropoda), with comments on biodiversity conservation within marine reserves. The Festivus, 46, 158–177. https://doi.org/10.54173/f465158 

Bertsch, H., & Aguilar-Rosas, L. E. (2016). Invertebrados marinos del noroeste de México / Marine invertebrates of Northwest Mexico. Ensenada, Baja California: Instituto de Investigaciones Oceanológicas, UABC.

Bezaury-Creel, J., & Gutiérrez, D. (2009). Áreas naturales protegidas y desarrollo social en México. In R. Dirzo, R. González, & I. J. March (Eds.), Capital natural de México: estado de conservación y tendencias de cambio, Vol. II. Estado de conservación y tendencias de cambio (pp. 385–431). Ciudad de México: Comisión Nacional para el Conocimientos y Uso de la Biodiversidad. 

Bouchet, P., Rocroi, J. P., Hausdorf, B., Kaim, A., Kano, Y., Nützel, A. et al. (2017). Revised classification, nomenclator and typification of gastropod and monoplacophoran families. Malacologia, 61, 1–526. https://doi.org/10.4002/040.061.0201 

Briggs, J. C., & Bowen, B. W. (2012). A realignment of marine biogeographic provinces with particular reference to fish distributions. Journal of Biogeography, 39, 12–30. https://doi.org/10.1111/j.1365-2699.2011.02613.x 

Camacho-García, Y. E., Gosliner, T. M., & Valdés, Á. (2005). Guía de campo de las babosas marinas del Pacífico este tropical. San Francisco, CA: California Academy of Sciences.

Carmona, L., Bhave, V., Salunkhe, R., Pola, M., Gosliner, T. M., & Cervera, J. L. (2014a). Systematic review of Anteaeolidiella (Mollusca, Nudibranchia, Aeolidiidae) based on morphological and molecular data, with a description of three new species. Zoological Journal of the Linnean Society, 171, 108–132. https://doi.org/10.1111/zoj.12129 

Carmona, L., Lei, B. R., Pola, M., Gosliner, T. M., Valdés, Á., & Cervera, J. L. (2014b). Untangling the Spurilla neapolitana (Delle Chiaje, 1841) species complex: a review of the genus Spurilla Bergh, 1864 (Mollusca: Nudibranchia: Aeolidiidae). Zoological Journal of the Linnean Society, 170, 132–154. https://doi.org/10.1111/zoj.12098 

Carmona, L., Pola, M., Gosliner, T. M., & Cervera, J. L. (2014c). The end of a long controversy: Systematics of the genus Limenandra (Mollusca: Nudibranchia: Aeolidiidae). Helgoland Marine Research, 68, 37–48. https://doi.org/10.1007/s10152-013-0367-y 

Conanp (Comisión Nacional de Áreas Naturales Protegidas). (2003). Programa de Manejo Parque Nacional Huatulco, México. Dirección General de Manejo para la Conservación, Ciudad de México: Conanp. https://www.conanp.gob.mx/que_hacemos/pdf/programas_manejo/huatulco.pdf 

Dean, L. J., & Prinsep, M. R. (2017). The chemistry and chemical ecology of nudibranchs. Natural Product Reports, 34, 1359–1390. https://doi.org/10.1039/c7np00041c 

Fisch, K. M., Hertzer, C., Böhringer, N., Wuisan, Z. G., Schillo, D., Bara, R. et al. (2017). The potential of Indonesian heterobranchs found around Bunaken Island for the production of bioactive compounds. Marine Drugs, 15, 384. https://doi.org/10.3390/md15120384 

Flores-Rodríguez, P., Flores-Garza, R., García-Ibáñez, S., Valdés-González, A., Martínez-Ríos, B., Mora-Marín, Y. et al. (2017). Riqueza, composición de la comunidad y similitud de las especies bentónicas de la subclase Opisthobranchia (Mollusca: Gastropoda) en cinco sitios del litoral de Acapulco, México. Revista de Biología Marina y Oceanografía, 52, 67–80. https://doi.org/10.4067/s0718-19572017000100005 

García-Méndez, K., & Camacho-García, Y. E. (2016). New records of heterobranch sea slugs (Mollusca: Gastropoda) from Isla del Coco National Park, Costa Rica. Revista de Biología Tropical, 64, 205–279. https://doi.org/10.15517/rbt.v64i1.23449 

Gladstone, W. (2002). The potential value of indicator groups in the selection of marine reserves. Biological Conservation, 104, 211–220. https://doi.org/10.1016/S0006-3207(01)00167-7 

Golestani, H., Crocetta, F., Padula, V., Camacho-García, Y., Langeneck, J., Poursanidis, D. et al. (2019). The little Aplysia coming of age: from one species to a complex of species complexes in Aplysia parvula (Mollusca: Gastropoda: Heterobranchia). Zoological Journal of the Linnean Society, 187, 279–330. https://doi.org/10.1093/zoolinnean/zlz028 

Goodheart, J., & Bely, A. (2017). Sequestration of nematocysts by divergent cnidarian predators: mechanism, function, and evolution. Invertebrate Biology, 136, 75–91. https://doi.org/10.1111/ivb.12154 

Gosliner, T. M. (1991). The opisthobranch gastropod fauna of the Galápagos Islands. In M. J. James (Ed.), Galápagos marine invertebrates: taxonomy, biogeography and evolution in Darwin’s islands (pp. 281–305). Boston, MA: Springer. https://doi.org/10.1007/978-1-4899-0646-5_14 

Gosliner, T., Valdés, Á., & Behrens, D. (2018). Nudibranch and sea slug identification: Indo-Pacific. Jacksonville, FL: New World Publications.

Händeler, K., Grzymbowski, Y. P., Krug, P. J., & Wägele, H. (2009). Functional chloroplasts in metazoan cells – a unique evolutionary strategy in animal life. Frontiers in Zoology, 6, 28. https://doi.org/10.1186/1742-9994-6-28 

Hermosillo, A. (2004). Opisthobranch mollusks of Parque Nacional De Coiba, Panama (Tropical Eastern Pacific). The Festivus, 36, 105–117.

Hermosillo, A. (2007). Historia natural y ecología de Tambja abdere (Marcus y Marcus, 1967) (Mollusca: Opisthobranchia) de Bahía de Banderas. In E. Ríos-Jara, M. C. Esqueda-González, & C. M. Galván-Villa (Eds.), Estudios sobre la malacología y conquiliología en México (pp. 179–180). Guadalajara: Universidad de Guadalajara, México.

Hermosillo, A. (2009). The opisthobranch fauna of Islas Tres Marías, Mexican Pacific. The Festivus, 41, 3–9.

Hermosillo, A. (2011). Species list of opisthobranch mollusks for Bahía de Banderas (Jalisco-Nayarit), Pacific Coast of México. The Festivus, 43, 39–49.

Hermosillo, A., & Behrens, D. W. (2005). The opisthobranch fauna (Gastropoda, Opisthobranchia) of the Mexican states of Colima, Michoacán and Guerrero: filling in the faunal gap. Vita Malacologica, 3, 11–22.

Hermosillo, A., Behrens, D. W., & Ríos-Jara, E. (2006). Opistobranquios de México: guía de babosas marinas del Pacífico, golfo de California y las islas Oceánicas. Guadalajara, Jalisco: Conabio.

Hermosillo, A., & Gosliner, T. M. (2008). The opisthobranch fauna of the Archipiélago de Revillagigedo, Mexican Pacific. The Festivus, 40, 25–34.

Horton, T., Kroh, A., Ahyong, S., Bailly, N., Boyko, C. B., & Brandão, S. N. (2024). World register of marine species. Accessed on 2024-06-05. http://www.marinespecies.org 

Holguín-Quiñones, O., & González-Pedraza, A. (1989). Moluscos de la franja costera del estado de Oaxaca, México. Atlas No. 7 CICIMAR, Instituto Politécnico Nacional.

Kaiser, K. L. (2007). The recent molluscan fauna of Île Clipperton. The Festivus, 39, 1–162.

Kandel, E. (1979). Behavioral biology of Aplysia: a contribution to the comparative study of opisthobranch mollusks. San Francisco, CA: W. H. Freeman.

Krug, P. J., Berriman, J. S., & Valdes, A. (2018). Phylogenetic systematics of the shelled sea slug genus Oxynoe Rafinesque, 1814 (Heterobranchia: Sacoglossa), with integrative descriptions of seven new species. Invertebrate Systematics, 32, 950–1003. https://doi.org/10.1071/IS17080 

López-Pérez, R., & Hernández-Ballesteros, L. (2004). Coral community structure and dynamics in the Huatulco area, western Mexico. Bulletin of Marine Science, 75, 453–472.

Matsuda, S. B., & Gosliner, T. M. (2018). Molecular phylogeny of Glossodoris (Ehrenberg, 1831) nudibranchs and related genera reveals cryptic and pseudocryptic species complexes. Cladistics, 34, 41–56. https://doi.org/10.1111/cla.12194 

Medrano, S., Krug, P. J., Gosliner, T. M., Kumar, A. B., & Valdés, Á. (2018). Systematics of Polybranchia Pease, 1860 (Mollusca: Gastropoda: Sacoglossa) based on molecular and morphological data. Zoological Journal of the Linnean Society, 186, 76–115. https://doi.org/10.1093/zoolinnean/zly050 

Ornelas-Gatdula, E., Camacho-García, Y., Schrödl, M., Padula, V., Hooker, Y., Gosliner, T. M. et al. (2012). Molecular systematics of the “Navanax aenigmaticus” species complex (Mollusca, Cephalaspidea): coming full circle. Zoologica Scripta, 41, 374–385. https://doi.org/10.1111/j.1463-6409.2012.00538.x 

Oskars, T. R., & Malaquias, M. A. E. (2019). A molecular phylogeny of the Indo-West Pacific species of Haloa sensu lato gastropods (Cephalaspidea: Haminoeidae): Tethyan vicariance, generic diversity, and ecological specialization. Molecular Phylogenetics and Evolution, 139, 1–21. https://doi.org/10.1016/j.ympev.2019.106557 

Oskars, T. R., & Malaquias, M. A. E. (2020). Systematic revision of the Indo-West Pacific colourful bubble-snails of the genus Lamprohaminoea Habe, 1952 (Cephalaspidea: Haminoeidae). Invertebrate Systematics, 34, 727–756. https://doi.org/10.1071/is20026 

Pola, M., Sánchez-Benítez, M., & Ramiro, B. (2014). The genus Polycera Cuvier, 1817 (Nudibranchia: Polyceridae) in the eastern Pacific Ocean, with redescription of Polycera alabe Collier & Farmer, 1964 and description of a new species. Journal of Molluscan Studies, 80, 551–561. https://doi.org/10.1093/mollus/eyu049 

Ramírez-González, A. (2005). Las bahías de Huatulco, Oaxaca, México: ensayo geográfico ecológico. Ciencia y Mar, 9, 3–20.

Rodríguez-Palacios, C., Mitchell-Arana, L., Sandoval-Díaz, G., Gómez, P., & Green, G. (1988). Los moluscos de las bahías de Huatulco y Puerto Ángel, Oaxaca. Distribución, diversidad y abundancia. Universidad y Ciencia, 5, 85–94.

Sanvicente-Añorve, L., Hermoso-Salazar, M., Ortigosa, J., Solís-Weiss, V., & Lemus-Santana, E. (2012). Opisthobranch assemblages from a coral reef system: the role of habitat type and food availability. Bulletin of Marine Science, 88, 1061–1074. https://doi.org/10.5343/bms.2011.1117 

Schejter, L., Rimondino, C., Chiesa, I., Díaz-de Astarloa, J. M., Doti, B., Elías, R. et al. (2016). Namuncurá Marine Protected Area: an oceanic hot spot of benthic biodiversity at Burdwood Bank, Argentina. Polar Biology, 39, 2373–2386. https://doi.org/10.1007/s00300-016-1913-2 

Schubert, J., & Smith, S. D. A. (2020). Sea slugs “rare in space and time” but not always. Diversity, 12, 1–14. https://doi.org/10.3390/d12110423

Spalding, M. D., Fox, H. E., Allen, G. R., Davidson, N., Ferdaña, Z. A., Finlayson, M. et al. (2007). Marine ecoregions of the World: a bioregionalization of coastal and shelf areas. Bioscience, 57, 573–583. https://doi.org/10.1641/b570707

Sreeraj, C. R., Sivaperuman, C., & Raghunathan, C. (2013). Species diversity and abundance of opisthobranch molluscs (Gastropoda: Opisthobranchia) in the coral reef environments of Andaman and Nicobar Islands, India. In K. Venkataraman, C. Sivaperuman, & C. Raghunathan (Eds.), Ecology and conservation of tropical marine faunal communities (pp. 81–106). Heidelberg, Berlin: Springer Berlin Heidelberg. https://doi.org/10.1007/978-3-642-38200-0_6 

Urbano, B., Ortigosa, D., Garcés-Salazar, J., Aristeo, J., González-Liano, M., Álvarez-Cerrillo, L. et al. (2019). Evaluación de la antropización usando a los moluscos como parámetro. In C. P. Ornelas-García, F. Álvarez, & A. Wegier (Eds.), Antropización: primer análisis integral (pp. 199–219). Ciudad de Mexico: IBUNAM/ Conacyt.

Valdés, Á. (2019). Northeast Pacific benthic shelled sea slugs. Zoosymposia, 13, 242–304. https://doi.org/10.11646/zoosymposia.13.1.21 

Valdés, Á., Breslau, E., Padula, V., Schrödl, M., Camacho, Y., Malaquias, M. A. E. et al. (2018). Molecular and morphological systematics of Dolabrifera Gray, 1847 (Mollusca: Gastropoda: Heterobranchia: Aplysiomorpha). Zoological Journal of the Linnean Society, 184, 31–65. https://doi.org/10.1093/zoolinnean/zlx099 

Valdés, Á., & Camacho-García, Y. E. (2004). “Cephalaspidean” heterobranchs (Gastropoda) from the Pacific coast of Costa Rica. Proceedings of the California Academy of Sciences, 55, 459–497.

Verdín-Padilla, C., Carballo, J. L., & Camacho, M. L. (2010). A qualitative assessment of sponge-feeding organisms from the Mexican Pacific Coast. The Open Marine Biology Journal, 4, 39–46. https://doi.org/10.2174/1874450801004010039 

Zamora-Silva, A., & Naranjo-García, E. (2008). Los opistobranquios de la Colección Nacional de Moluscos. Revista Mexicana de Biodiversidad, 79, 333–342. https://doi.org/10.22201/ib.20078706e.2008.002.568 

Ziegler, M., FitzPatrick, S. K., Burghardt, I., Liberatore, K. L., Leffler, A. J., Takacs-Vesbach, C. et al. (2014). Thermal stress response in a dinoflagellate-bearing nudibranch and the octocoral on which it feeds. Coral Reefs, 33, 1085–1099. https://doi.org/10.1007/s00338-014-1204-8

José Alan Herrera-García ^a, Mahinda Martinez ^{a, b,} *, Pilar Zamora-Tavares ^c, Ofelia Vargas ^c, Luis Hernández-Sandoval ^{a, b}

^a Universidad Autónoma de Querétaro, Facultad de Ciencias Naturales, Av. de las Ciencias, s/n, 76230 Juriquilla, Querétaro, Mexico 

^b Universidad Autónoma de Querétaro, Facultad de Ciencias Naturales, Biología, Laboratorio Nacional de Identificación y Caracterización Vegetal, Av. de las Ciencias, s/n, 76230 Juriquilla, Querétaro, Mexico 

^c Universidad de Guadalajara, Centro Universitario de Ciencias Biológicas y Agropecuarias, Instituto de Botánica, Departamento de Botánica y Zoología, Laboratorio Nacional de Identificación y Caracterización Vegetal, Av. Ing. Ramón Padilla Sánchez, 45200 Zapopan, Jalisco, Mexico 

*Corresponding author: mahinda@uaq.mx (M. Martínez)

Received: 20 May 2024; accepted: 19 February 2025

Abstract

Some bromeliads form a compact rosette that accumulates detritus and water, known as phytotelma. The phytotelma is a lentic ephemeral aquatic environment that forms diverse communities with complex trophic levels. Pseudalcantarea grandis, a saxicolous plant, forms a phytotelma. To understand the importance of P. grandis as a eukaryotic diversity reservoir in arid zones, we collected water samples from 5 plants growing in a dry canyon in Zimapán, Hidalgo, Mexico. We analyzed them through metabarcoding of the ITS1 (Internal Transcribed Spacer) and the partial 5.8S gene. We used the Ion Torrent PGM platform for the sequencing, and the taxonomic assignation for the amplicons was made with BLAST in Genbank at NCBI. We found 26 phyla and 543 genera, 80% of which belonged to Ascomycota, Basidiomycota, Blastocladiomycota Chytridiomycota, Glomeromycota, Mucoromycota, and Zoopagomycota phyla. The remaining 20% was composed of 19 phyla belonging to other kingdoms. Photosynthetic organisms were represented by the phyla Bacillariophyta, Charophyta, Chlorophyta, and Ochrophyta. The vascular plants do not live in the tank but constitute the debris sustaining the large number of decomposers. The trophic levels in the tank were detritus, micro- and macro-decomposers, filter feeders, photosynthesizers, micro-predators, aquatic volume predators, surface predators, and parasites.

Keywords: Aquatic; Ephemeral; Arid zone; Phytotelma

Diversidad de eucariotes y niveles tróficos dentro de la bromelia tanque Pseudalcantarea grandis en una zona árida detectados por metabarcoding de ADN ambiental

Resumen

Algunas bromelias forman rosetas compactas que acumulan detritus y agua. Esta acumulación se conoce como fitotelma, un hábitat acuático léntico y efímero con comunidades diversas y niveles tróficos complejos. Psedalcantarea grandis es una planta saxícola y forma un fitotelma. Para entender la importancia de P. grandis como reservorio de diversidad acuática en una zona árida, colectamos muestras de agua de 5 plantas en un cañón de Zimapán, Hidalgo, México y las analizamos por metabarcoding del ITS1 (Internal Transcribed Spacer) y una región parcial del gen 5.8S. La secuenciación se hizo en la plataforma Ion Torrent PGM. Asignamos la identidad taxonómica de los amplicones utilizando BLAST de Genbank. Encontramos 26 phyla y 543 géneros, 80% pertenecen a los phyla fúngicos Ascomycota, Basidiomycota, Blastocladiomycota Chytridiomycota, Glomeromycota, Mucoromycota, y Zoopagomycota. El 20% restante está compuesto por 19 phyla de otros reinos. Los organismos fotosintéticos estuvieron representados por los phyla Bacillariophyta, Charophyta, Chlorophyta y Ochrophyta. Otros organismos fotosintéticos que corresponden a plantas vasculares no viven dentro del tanque, pero forman la hojarasca que mantiene a los descomponedores. Los niveles tróficos en el tanque fueron detritus, micro y macrodescomponedores, filtradores, fotosintetizadores, microdepredadores, depredadores del volumen de agua, depredadores de superficie y parásitos.

Palabras clave: Acuático; Efímero; Zona árida; Fitotelma

Introduction

The Bromeliaceae family is comprised of almost 3,700 species distributed mostly in tropical areas of the Americas (Gouda et al., 2024). They are herbaceous perennial monocots with leaves arranged in rosettes, many of which are epiphytes (Ramírez-Murillo et al., 2004; Rzedowski, 2006). There are 442 species in Mexico (Espejo-Serna & López-Ferrari, 2018) that frequently grow in nutrient and mineral-deficient environments (Bernal et al., 2006; Ramírez-Murillo et al., 2004). Some species form compact rosettes with absorbent trichomes in their interior that allow the accumulation of solids rich in nutrients and water, known as phytotelma (Benzing, 2000; Goffredi et al., 2011).

Phytotelmata are lentic aquatic environments, mostly ephemeral that last less than 3 months (Mogi, 2004). They are freshwater habitats for diverse communities including viruses, Archaea, and bacteria (Brouard et al., 2013, Goffredi et al., 2011). Among the eukaryotes, aquatic mosses, green algae, diatoms, protists, fungi, insects, amphibians, and crustaceans have been documented (Benzing, 2000; Brandt et al., 2017; Kitching, 2001; Ramos & do Nascimento Moura, 2019; Rodríguez-Núñez et al., 2018; Simão et al., 2020). 

Bromeliads that form phytotelma accumulate essential mineral elements, which are the main nitrogen source for the plant (Kitching, 2001). The presence of detritivores and predators is related to the nitrogen concentration in the leaves. Predators increase nutrient flux from the leaf litter of nearby plants to the bromeliad (Benzing & Renfrow, 1974; Ngai & Srivastava, 2006; Nievola et al., 2001; Takahashi & Mercier, 2011).

Unlike terrestrial and aquatic communities in which plants and algae are the main nutrient resources, in the phytotelma leaf litter and invertebrate remains play that role. In trophic networks inside the phytotelma, protists and rotifers are considered as micro-predators that also consume organic particles. Macroinvertebrates can consume the detritus, filter feeders, aquatic predators, and surface predators, whereas bacteria and fungi are the main decomposers that obtain energy directly from the detritus (Brouard et al., 2012; Mogi, 2004).

Gomes et al. (2015) characterized the enzymatic activity of the fungal community inside the bromeliad tank of Vriesea minarum in Brazil. Using cultivation techniques they identified 36 species, 22 of which were Basidiomycota and 14 were Ascomycota. The most relevant genera were Cryptococcus, Candida, and Aureobasidium. These organisms contain enzymes that degrade vegetal material. 

Nutrient intake for the plant is further facilitated by insects (Ngai & Srivastava, 2006). For example, odonatan larvae ingest detritivores, contributing to the nitrogen cycle within the bromeliad by defecating. Leachates from defecation release nitrogen in a form available to the bromeliad and create a suitable niche for other microorganisms providing substrata (Benzing & Renfrow, 1974).

Pseudalcantarea grandis (Schltdl.) Pinzón & Barfuss (Fig. 1A) is a saxicolous tank bromeliad that reaches 2.5 m in height and forms a highly ramified inflorescence in March and April. It is distributed from Central Mexico (Guanajuato, Querétaro, Hidalgo) toward the south (Puebla, Oaxaca, and Chiapas) and into Honduras. It is considered a MegaMexico II endemic species (Espejo-Serna et al., 2010). At the locality of Las Adjuntas, in Hidalgo, the plant is known as “tinaja”, “jarilla”, and “soluche de agua” because its tank can store water. The species grows in crags of the main rivers in the northeastern portion of the region known as Bajío. It grows at elevations ranging from 400 to 1,600 m asl (Espejo-Serna et al., 2010; Rzedowski, 2006). 

Metabarcoding studies describing the communities associated with phytotelma have mostly focused on specific groups such as vertebrates (Brozio et al., 2017), ciliates (Simão et al., 2017), or bacteria (Louca et al., 2017; Rodríguez-Núñez et al., 2018). In Pseudalcantarea grandis, 297 bacteria genera were found, with Proteobacteria (37%), Actinobacteria (19%), and Firmicutes (15%) comprising the highest percentage (71%). The main metabolic functions were aerobic chemoheterotrophy and fermentation. However, rare biosphere bacteria were also found, which could favor micro-ecosystem resilience and resistance (Herrera-García et al., 2022). Comprehensive sequencing of the eukaryotic diversity inside tank bromeliads has been performed in tropical zones (Simão et al., 2020), but not arid areas. The objectives of our study were to describe the eukaryotic diversity in Pseudalcantarea grandis phytotelma to understand which vascular plants form the litter, and to infer the putative trophic levels of the phytotelmata in an arid zone.

Materials and methods

Water samples were collected during the 2018 rainy season at Las Angosturas Canyon, Zimapán, Hidalgo, Mexico (20°50.933’ N, 99°26.7’ W, 900 m asl, see Herrera-García et al. [2022] for a location map) within the Queretano-Hidalguense arid zone, which has been described as a high-diversity and endemicity area (Hernández-Magaña et al., 2017; Hernández & Bárcenas, 1995; Rojas et al., 2013). This arid zone is considered the southernmost portion of the Chihuahuan Desert floristic province. It consists mostly of arid valleys and depressions surrounded by mountains (Hernández & Gómez-Hinostrosa, 2005). 

Las Angosturas Canyon is approximately 12 km long with a mixture of xerophytic scrub and tropical deciduous forest (Fig. 1B). Bromeliads grow on vertical crags with different amounts of the surrounding vegetation. Therefore, the tanks are frequently filled with leaf litter. We selected individuals that were accessible enough to be collected by a rappel and were more than 50 cm in diameter. The associated plants are listed in Table 1. To collect the water inside the bromeliads we used Nest® cell scrapers to scratch the inside of each tank, and the water in the bromeliads was vigorously shaken to obtain a homogeneous sample. Water volumes of 50 to 100 ml were collected using 10 ml sterile serological pipettes. The samples were stored in 50 ml conical Falcon tubes, transported on dry ice, and stored at -79 °C until processing. Physicochemical water parameters were not determined.

Table 1

Las Angosturas Canyon floristic inventory. Plants directly above the sampled individuals are noted in the second column. Vouchers and photographs are noted in the third column.

Family	Species	Association	Reference at QMEX
Amaryllidaceae	Zephyranthes clintiae Traub		A. Herrera 30
Amaryllidaceae	Zephyranthes concolor (Lindley) Bentham & Hook.		A. Herrera 7
Anacardiaceae	Rhus terebinthifolia Schltdl. & Cham.		A. Herrera 21
Anacardiaceae	Pseudosmodingium virletii (Baill.) Engl.		L. Hernández 5029
Apocynaceaea	Asclepias curassavica L.		A. Herrera 20
Apocynaceaea	Vallesia glabra (Cav.) Link		A. Herrera 4
Arecaceae	Brahea dulcis (Kunth) Mart.		Photographic record
Asparagaceae	Agave xylonacantha Salm-Dyck	surrounding	A. Vega 50
Asparagaceae	Dasylirion longissimum Lem.		L. Hernández 4511
Asparagaceae	Yucca filifera Chab.		L. Hernández 4828
Asparagaceae	Yucca queretaroensis Piña		Photographic record
Asteraceae	Baccharis salicifolia (Ruiz y Pav.) Pers.		M. Martínez 6056
Asteraceae	Cirsium sp.		A. Herrera ND
Asteraceae	Gnaphalium luteo-album L.		A. Herrera ND
Asteraceae	Gochnatia hypoleuca (DC.) A. Gray	surrounding	A. Herrera ND
Bignoniaceae	Tecoma stans (L.) Juss.		Photographic record
Boraginaceae	Cordia boissieri A. DC.		M. Martínez 7144
Bromeliaceae	Hechtia glomerata Zucc.	surrounding	S. Zamudio 14469
Bromeliaceae	Hechtia tillandsioides (André) L. B. Smith	surrounding	Photographic record
Table 1. Continued
Family	Species	Association	Reference at QMEX
Bromeliaceae	Pseudalcantarea grandis (Schltdl.)Pinzón & Barfuss		A. Herrera 1
Bromeliaceae	Tillandsia recurvata L.	surrounding	M. Martínez 8220
Burseraceae	Bursera morelensis Ram.	surrounding	Photographic record
Cactaceae	Astrophytum ornatum (DC.) Britton & Rose		Photographic record
Cactaceae	Cylindropuntia imbricata (Haw.) F. M. Knuth ssp. cardenche (Griffiths) U. Guzmán		A. Herrera 12
Cactaceae	Coryphanta sp.		Photographic record
Cactaceae	Echinocereus pentalophus Lem.		Photographic record
Cactaceae	Echinocactus platyacanthus Link & Otto		M. Figueroa 12
Cactaceae	Ferocacutus histrix (DC.) G.E.Linds.		Photographic record
Cactaceae	Mammilaria elongata DC.	surrounding	Photographic record
Cactaceae	Mammillaria longimamma DC.		Photographic record
Cactaceae	Myrtillocactus geometrizans (Mart. ex Pfeiff.) Console	surrounding	Photographic record
Cactaceae	Neobuxbaumia polylopha (DC.) Backeberg		Photographic record
Cactaceae	Opuntia imbricata (Haw.) F. M. Kunth		Photographic record
Cactaceae	Opuntia microdasys (Lehm.) Pfeiff.		Photographic record
Cactaceae	Opuntia rastrera F.A.C. Weber	surrounding	Photographic record
Cactaceae	Stenocereus queretaroensis (F.A.C.Weber ex Mathes.) Buxb.		Photographic record
Cactaceae	Strombocactus disciformis (DC.) Britton & Rose		Photographic record
Cannabaceae	Celtis pallida Torr.		A. Herrera 2
Capparaceae	Capparis incana Kunth		A. Herrera 5
Convolvulaceae	Ipomoea rzedowskii E. Carranza		A. Herrera 17
Crassulaceae	Echeveria secunda Booth	surrounding	A. Herrera 26
Crassulaceae	Pachyphytum sp.		A. Herrera ND
Crassulaceae	Sedum sp.	surrounding	A. Herrera ND
Euphorbiaceae	Cnidoscolus tubulosus (Muell. Arg.) I.M. Johnst.		A. Herrera 9
Euphorbiaceae	Acalypha monostachya Cav.		A. Herrera 15
Euphorbiaceae	Croton ciliato-glandulifer Ort.		L. Hernández 5029
Euphorbiaceae	Jatropha dioica Sessé ex Cerv.		A. Herrera ND
Euphorbiaceae	Ricinus communis L.		A. Herrera ND
Fabaceae	Acacia berlandieri Benth.	surrounding	Photographic record
Fabaceae	Albizia occidentalis Brandegee		Photographic record
Fabaceae	Bauhinia sp.		Photographic record
Fabaceae	Lysiloma microphylla Bentham		A. Herrera 36
Fabaceae	Mimosa leucaenoides Bentham	surrounding	Photographic record
Fabaceae	Mimosa martindelcampoi F. G. Medrano		Photographic record
Fabaceae	Mimosa puberula Bentham		A. Herrera 3
Fabaceae	Pithecellobium dulce (Roxb.) Bentham		Photographic record
Fabaceae	Neltuma laevigata (Humb. & Bonpl. ex Willd.) Britton & Rose		M. Martínez ND
Fabaceae	Vachellia farnesiana (L.) Willd. & Arn.		A. Herrera 10
Table 1. Continued
Family	Species	Association	Reference at QMEX
Fouquieriaceae	Fouquieria splendens Engelm.	surrounding	Photographic record
Lentibulariaceae	Pinguicula aff. moctezumae Zamudio & R.Z. Ortega		Photographic record
Lythraceae	Heimia salicifolia (Kunth) Link		A. Herrera 13
Onagraceae	Hauya elegans DC.	surrounding	A. Herrera 14
Malpighiaceae	Mascagnia macroptera (Moc. & Sessé ex DC.) Nied.		A. Herrera 8
Malvaceae	Pseudobombax ellipticum (Kunth) Dugand		A. Herrera ND
Malvaceae	Malvaviscus arboreus Cav.		M. Martínez 5317
Myrtaceae	Psidium guajava L.	surrounding	Photographic record
Papaveraceae	Argemone ochroleuca Sweet		M. Martínez 6713
Plantaginaceae	Rusellia polyedra Zucc.		A. Herrera 27
Platanaceae	Platanus mexicana Moric.		A. Herrera 16
Poaceae	Arundinaria sp.		A. Herrera ND
Poaceae	Cenchrus sp.		A. Herrera ND
Poaceae	Cynodon dactylon (L.) Pers.		M. Martínez 3197
Poaceae	Eragrostis sp.		E. Carranza 5251
Primulaceae	Samolus ebracteatus Kunth		A. Herrera 11
Pteridaceae	Argyrochosma formosa (Liebm.) Windham		A. Herrera 23
Pteridaceae	Notholaena affinis (Mett.) T. Moore		A. Herrera 24
Pteridaceae	Notholaena jacalensis Pray		A. Herrera 25
Pteridaceae	Pellaea sp.		A. Herrera 34
Ranunculaceae	Clematis drummondii Torr. & A.Gray		M. Martínez 4434
Rhamnaceae	Karwinskia subcordata Schlecht.		A. Herrera 22
Rubiaceae	Nernstia mexicana (Zucc. & Mart. ex DC.) Urb.		A. Herrera 32
Salicaceae	Neopringlea integrifolia (Hemsl.) S. Watson		A. Herrera 19
Salicaceae	Salix humboldtiana Willd.		Photographic record
Sapindaceae	Dodonaea viscosa (L.) Jacq.		A. Herrera ND
Sapindaceae	Sapindus saponaria L.		A. Herrera ND
Sapindaceae	Serjania sp.		A. Herrera ND
Selaginellaceae	Selaginella lepidophylla (Hook. & Grev.) Spring.	surrounding	Photographic record
Selaginellaceae	Selaginella ribae Valdespino		A. Herrera 29
Selaginellaceae	Selaginella selowii Hieron.		A. Herrera 28
Solanaceae	Datura inoxia Miller		V. Martínez 1
Solanaceae	Nicotiana glauca Graham		Photographic record
Solanaceae	Nicotiana trigonophylla Dunal		O. García 434
Solanaceae	Physalis cinerascens (Dunal) Hitch.		L. Hernández 3769
Solanaceae	Physalis philadelphica Lam.		A. Herrera 38
Solanaceae	Solanum lycopersicon L.		Photographic record
Taxodiaceae	Taxodium mucronatum Ten.		M. Martínez 3237
Urticaceae	Urera sp.		H. Rubio 302
Zygophyllaceae	Morkillia acuminata Rose & Painter	surrounding	A. Herrera 18

DNA extraction

Water samples were homogenized and 100 ml was filtered through a 0.22 µm Millipore® nitrocellulose membrane. The membrane was frozen and macerated in liquid nitrogen. We extracted total DNA using the QIAmp DNA Extraction® kit following the manufacturer’s instructions by duplicate to obtain pseudoreplicates and verify reproducibility. DNA quality and concentration were evaluated using NanoDrop® spectrophotometry. 

Amplicon sequencing

To characterize eukaryotic diversity, we amplified a portion of the 5.8 S Internal Transcibed Spacer (ITS) with the ITS1 and ITS2 primers designated by White et al. (1990). The PCR reaction consisted of a final volume of 25 µl, that contained 2 mM of dNTP´s, 2mM µl of each primer, 0.4% DMSO, 0.4 % BSA, 2.5 mM MgCl2, 1.2 mM Buffer, 1.25 U Platinum Taq, 60ng/µl DNA and H2O. Thermocycler conditions were an initial step at 95 °C for 3 min, followed by 30 cycles at 95 °C for 1 min; 52 °C, 45 s, and 72 °C, 2 min, with a final extension step at 72 °C for 5 min. Amplicons were purified with Agencourt® AMPure® XP.

To construct the libraries, we used the Ion Plus Fragment Library kit. The presence, size, and concentration of the fragment were analyzed using Bioanalyzer 2100 with high-sensitivity DNA assay (Agilent). Libraries were quantified using real-time PCR to obtain an equimolar dilution factor to mix the 3 libraries. The template was prepared using a PCR emulsion in the Ion One Touch 2 System (Life Technologies) and quantified by fluorometry in Qubit® 3.0 (Thermo Fisher Scientific). Finally, the template was loaded onto the PGM 318TM chip using the 400-pair base fragment sequencing kit, according to the Ion PGM™ Hi‑Q™ View Sequencing Kit protocol.

We sampled the vascular plants growing at the canyon, directly above the bromeliad, and also the surrounding vegetation. Voucher specimens were deposited at QMEX herbarium. We compared the similarity of the plant inventory obtained by sequencing against the floristic list obtained by field sampling through a Sorensen coefficient analysis at the family level.

Sequencing quality was evaluated using the FastQC program. Sequences were filtered by the quality value of Phred > 20. We selected sequences larger than 100 bp in the CLC Genomic Workbench v.11.01 (QIAGEN Bioinformatics, Aarhus, Denmark) platform. In the Microbial Genomics module application, we performed an analysis based on the amplicons to aggregate the sequences in operational taxonomic units (OTUs) considering only 99% similarity among them. We deleted unique reads and chimeras. Taxonomic assignation of the amplicons was performed with BLAST in 2023 via the Genbank at NCBI database (Altschul et al., 1990). Over 90% of the OTUs had identity percentages higher than 95% and only 54 OTUs had lower percentages, ranging from 75 to 80%. We manually reviewed them and corroborated the genus of each one. Since BLAST provides determinations at the genus and species levels, we used MEGAN Community Edition V. 6.24.4 to assign kingdom, phylum, class, order, and family. We loaded the BLAST results using the lowest basal common ancestor assignation algorithm (LCA). The analysis is based on the taxonomic hierarchies recognized by NCBI and the results are displayed as a phylogenetic tree that allows simple observation of taxonomic diversity (Huson et al., 2016). We manually reviewed the classifications and to corroborate the taxonomic assignations we used the classification proposed by Simpson (2006) for plants, and Tree of Life (2022) for the other eukaryotic marine taxa (such as Cnidaria). The OTUs at the genus level were used to define the total eukaryotic group diversity present in our sample.

We assigned the ecological function of each genus following the criteria of Mogi (2004) and Brouard et al. (2012). We considered 9 categories: 1) detritus formed by leaf litter and vegetal matter that serves as the main resource for the trophic network; 2) micro decomposers integrated by bacteria (Herrera-García et al., 2022); 3) macro decomposers formed by saprobiotic fungi; 4) filter feeders that use small particles including microorganisms that are in turn consumed by aquatic and surface predators; 5) photosynthetic organisms that require sunlight and serve as food for predators; 6) micro predators that feed on photosynthetic organisms, filter feeders, and micro-decomposers; 7) aquatic predators which are macroinvertebrates that live in the water column and feed mostly on algae and bacteria; 8) surface predators which are restricted to the uppermost portion of the water column and feed on protists, bacteria, and algae; and 9) parasites which are obligate vertebrate parasites that use arthropods as vectors.

Results

The 5 sampled plants had volumes that varied from 50 to 100 ml. The 2 pseudoreplicates were compared and considered as a single pool due to the similarity of the resulting OTUs. We obtained a total of 3,276,538 lectures. After quality and size filtration, the number of useful lectures was reduced to 1,284,998 representing a total of 23,948 OTUs, 762 of which could not be assigned to the species or genus taxonomic category provided by BLAST. 

The diversity of organisms living in the tank consisted of 26 phyla and 543 genera. See Supplementary material T1 for a list of assigned taxa. Fungi were dominant, as 80% of the genera belonged to Ascomycota, Basidiomycota, Blastocladiomycota Chytridiomycota, Glomeromycota, Mucoromycota, and Zoopagomycota phyla. The remaining 20% was composed of 19 phyla: Apicomplexa, Apusozoa, Arthropoda, Bacillariophyta, Bryophyta, Cercozoa, Charophyta, Chlorophyta, Ciliophora, Cnidaria, Colponemidia, Heterolobosea, Hyphochytriomycota, Metamonada, Myxomycota, Ochrophyta, Oomycota, Platyhelminthes, and Tracheophyta (Fig. 2). We identified 25 genera of photosynthetic algae from the phyla Bacillariophyta (with the genera Pseudo-nitzschia, Navicula, and Stephanodiscus), Charophyta (Staurastrum), Chlorophyta (Leskea, Didymogenes, Meyerella, Dolichomastix, Bathycoccus, Mychonastes, Trebouxia, Chamaetrichon, Hazenia, Chloroidium, and Pleurastrum), and Ochrophyta (Nannochloropsis). The other photosynthetic organisms were Bryophyta (Fontinalis, Leskea, and Thuidium).

Protists were represented by 44 genera, 4 of which are relevant to human health: Plasmodium (Apicomplexa) which causes paludism, Giardia (Metamonada) which is responsible for giardiasis, Neobalantidium (Cilliophora) that causes balantidiosis, and Spirometra (Plathelmyntes) which is responsible for sparganosis. 

Tracheophyta (vascular plants) do not live in the phytotelma but do constitute the debris that accumulates in the bromeliad. They comprised 11% of the identified genera. We found a Sorensen coefficient of 45% similarity among the methods in which 14 taxa at the family level were shared (Supplementary material F1). Arthropoda were represented by 13 genera of the Coleoptera, Diptera, Hymenoptera, Lepidoptera, Odonata, and Pocopodia orders. 

Of the eukaryotic organisms, 79% were classified as decomposers, and 7% were classified as micro-predators. In the tank, 3% were photosynthetic organisms, 2% were parasites, and the remaining 9% corresponded to the vascular plants that constitute the detritus. Tracheophyta and Bryophyta constituted the vegetal resources available to micro- and macro-decomposers, and filter feeders. Cercozoa, Apusozoa, Heterolobosea, and Colponemidia were considered micro-predators because they consume some photosynthetic organisms, filter feeders, and micro-decomposers. Ciliophora and 2 Arthropoda genera (Cyprideis and Notodromas) were some of the filter feeders. Apicomplexa, Chytridiomycota, Metamonada, Myxomycota, and Zoopagomycota were the parasites. Aquatic predators were mostly metazoans (Cnidaria and Platyhelminthes) that use filter feeders, photosynthesizers, and macro decomposers as resources. The arthropods Coleoptera, Diptera, Hymenoptera, Lepidoptera, and Odonata were part of the uppermost categories of the trophic network (surface predators). However, their exoskeletons and/or excretions become part of the tank resource or contribute to the nutrient cycling of the microecosystem (Figs. 3, 4). 

Discussion

Eukaryotic composition of the Pseudalcantarea grandis community

The abundance of fungi in the Pseudalcantarea tank appeared to correlate with their function in the trophic network. Fungi are the most important degrading group, responsible for organic decomposition and nutrient recycling in forests, aquatic ecosystems, and the phytotelma (Costa & Gusmão, 2015; Grossart et al., 2019; Grothjan et al., 2019). Fungi also have multiple functions in aquatic environment interactions that favor antagonistic and symbiotic members of the community. They can be predators, parasites, or food for heterotrophic protists. Some can use organic matter, pollen, or zooplankton exoskeletons (Zoopagomycota, Chytridiomycota) (Grossart et al., 2019). Vegetal matter decomposition enhances detritus quality for detritivores degrading vegetal polysaccharides into monosaccharides through enzymatic reactions which are then easily digested by microorganisms (Krauss et al., 2011). Fungi and protist interactions for vegetal matter transformation are poorly documented. A symbiotic relationship between them is unknown and difficult to study because of the microscopic scale at which they occur (Grossart et al., 2019).

The fungal diversity found in the Pseudalcantarea grandis tank was high compared to that reported in previous studies of other Bromeliaceae species. We found 436 genera, whereas Gomes et al. (2015) identified 36 genera using cultivation techniques. Other papers already pointed out that metagenomic studies detect higher diversity levels than other techniques (Simão et al., 2020). The 36 genera found by Gomes et al. (2015) were also found in P. grandis. Cryptococcus, Candida, and Aureobasidium have specific enzymatic activity in plant material degradation, which suggests that degradation reactions by these organisms are frequent in the phytotelma. The primers used in our study were developed for fungi (White et al., 1990), therefore they might be overrepresented.

We found 44 protist genera in the phytotelma. Some have mixotrophic nutrition, in that they obtain their energy through photo- and heterotrophy depending on the environmental conditions in which they grow (Jones, 2000). In aquatic environments where light is available but dissolved organic carbon (DOC) is scarce, photosynthetic organisms are better represented. Low light and high DOC favor heterotrophic organisms (Jones, 2000). The latter condition is what was present in the sampled tanks. Therefore, the development of photosynthetic protists is not favored because of the large and abundant bacterial community that competes for elements such as phosphorus (Brouard et al., 2012; Herrera-García et al., 2022). In the rainy season, the tank of P. grandis is surrounded by vegetation that intercepts light and deposits leaf litter, therefore favoring the conditions for fungi and decomposers (Grossart et al., 2019; Herrera-García et al., 2022, Kitching, 2000).

Direct observations and sampling of the phytotelma of tropical zones have revealed Diptera, Odonata, Oligochaeta, Ostracoda, beetles, copepods, pseudoscorpions, scorpions, isopods, Lepidoptera, hemipterans, homopterans, orthopterans, and arachnids in tank bromeliads (Cutz-Pool et al., 2016; Marino et al., 2013). Using environmental DNA with specific primers, amphibians (Brozio et al., 2017) and ciliates (Simão et al., 2017) have been found in tank bromeliads with high water availability. These results suggest that aridity and strong water seasonality in our study area were responsible for the lack of amphibians and the low arthropod and ciliate diversity we found.

Phytotelma seasonality is an important factor. In a rainy forest, the annual precipitation is 3,000 mm and rain is present for 280 days, therefore the water in the tank lasts longer (Brouard et al., 2012). In contrast, in our location, the annual precipitation is 391 mm and the phytotelma is available only through the rainy season from May to June (INFAED, 2012). The presence of Plasmodium is relevant since its most common vector is Aedes, suggesting that at some point during the phytotelma duration, the mosquito is in contact with the water, completing the parasite life cycle (Williams, 2007).

The absence of vertebrates is characteristic of phytotelma communities (Mogi, 2004). One exception is in rainforest bromeliad, where bromeliad tadpoles can be found. We did not find vertebrates. Strong seasonality was probably the reason for their absence. Not all OTUs could be assigned to the species or genus taxonomic category at 99% identity level we used. We did not find an identity for 762 of the 23,984 sequences, possibly because the sequences of these organisms are not available in the NCBI database, or because the organisms have not yet been described.

The tracheophytes found in the phytotelma could not be identified at the generic level. There are 2 possible explanations: the reads were short (150 bp) and therefore insufficient, or the genera growing at the canyon are not in the GenBank NCBI (National Center for Biotechnology Information) database. However, 30 families of vascular plants were detected, 16 of which correspond to the families found by field collection.

Trophic structure of the Pseudalcantarea grandis tank

We propose 9 trophic levels for tank bromeliads in arid zones, —2 more than those suggested by Mogi (2004), and 3 more than those suggested by Brouard et al. (2012). Detritus is the main nutrient source. Macrodecomposers process leaf litter into small organic matter particles, including their waste. The particles are then stored in the phytotelma where filterers and invertebrates process them. Dead organisms, feces, and leaf litter stored at the bottom of the tank are used by bacteria and other microorganisms such as fungi to assimilate nutrients (Brouard et al., 2012). We found that 48 plant genera (45 Tracheophyta, and 3 Bryophyta) constitute the detritus, and although Brouard et al. (2012) recognized organic litter as a resource, they did not identify the organisms that provided it. The large amount of detritus was due to the type of surrounding vegetation, which was a tropical deciduous forest in this study. In P. grandis macro decomposers are fungi of the Ascomycota, Basidiomycota, and Myxomycota phyla. We concur with Brouard et al. (2012) that ciliates are filterers. Mogi (2004) did not consider microorganisms to be autotrophs, but Brouard et al. (2012) included that category, and in P. grandis algae constitute this level. Insects were categorized as surface predators in their diagram; they include the odonate family Coenagrionidae, which includes the 2 genera we found in P. grandis, Ischnura, and Agriocnemis (Brouard et al., 2012). Neither Mogi (2004) nor Brouard et al. (2012) included parasites at a trophic level, but some of the genera found in P. grandis are obligate parasites, mostly from the Alveolata kingdom, which has birds and mammals as hosts but uses arthropods as vectors.

We found 26 phyla with 543 genera in the phytotelma of P. grandis growing in an arid zone. The identified diversity suggested that the organisms that inhabit these small ephemeral water bodies are adapted to prolonged dry spells and develop quickly when the phytotelma has water. The biota was mostly composed of fungi (over 80% of the diversity) that specialize in plant detritus degradation. Water bodies shelter aquatic groups that cannot exist in areas outside the P. grandis phytotelma. It is easier to assess the diversity of organisms within a tank than to comprehend their interactions. The trophic network proposed for eukaryotes indicates that they fulfill different functions.

As final considerations, we conclude that the analyzed phytotelma had a large detritus accumulation, and water was present briefly. Most of the diversity belonged to fungi (80%) because of the large amount of plant detritus in the tank. Photosynthesizers were scarce but included 25 algal genera and 3 Bryophyta. We found 45% Sorensen coefficient similarity between the plant detritus and the specimens collected with herbarium specimens. We also found a low arthropod and ciliate diversity, and the tank also harbors protist genera, some of which have medical implications. We found 9 trophic levels in the tank. Unlike tropical areas, in which algal production can support non-detrital food webs, in our arid zone system, detritus degradation was the main energy source. 

Acknowledgments

Funding was provided by Conahcyt through grant 293833 for the Laboratorio Nacional de Identificación y Caracterización Vegetal. Diana Velázquez designed and executed Figure 3. Two anonymous reviewers helped to improve the manuscript with their comments.

References

Altschul, S. F., Gish, W., Miller, W., Myers, E. W., & Lipman, D. J. (1990). Basic local alignment search tool. Journal of Molecular Biology, 215, 403–410. https://doi.org/10.1016/S0022-2836(05)80360-2 

Benzing, D. H., & Renfrow, A. (1974). The mineral nutrition of Bromeliaceae. Botanical Gazette, 135, 281–288. https://doi.org/10.1086/336762 

Benzing, D. H. (2000). Bromeliaceae: profile of an adaptive radiation. Cambridge, U.K.: Cambridge University Press. 

Bernal, R., Valverde, T., & Hernández-Rosas, L. (2006). Habitat preference of the epiphyte Tillandsia recurvata (Bromeliaceae) in a semi-desert environment in Central Mexico. Canadian Journal of Botany, 83, 1238–1247. https://doi.org/10.1139/b05-076 

Brandt, F. B., Martinson, G. O., & Conrad, R. (2017). Bromeliad tanks are unique habitats for microbial communities involved in methane turnover. Plant and Soil, 410, 167–179. https://doi.org/10.1007/s11104-016-2988-9 

Brouard, O., Céréghino, R., Corbara, B., Leroy, C., Pelozuelo, L., Dejean, A. et al. (2012). Understorey environments influence functional diversity in tank-bromeliad ecosystems. Freshwater Biology, 57, 815–823. https://doi.org/10.1111/j.1365-2427.2012.02749.x 

Brozio, S., Manson, C., Gourevitch, E., Burns, T. J., Greener, M. S., Downie, J. R. et al. (2017). Development and application of an eDNA method to detect the critically endangered Trinidad golden tree frog (Phytotriades auratus) in bromeliad phytotelmata. Plos One, 12, 1–8. https://doi.org/10.1371/journal.pone.0170619 

Costa, L. A., & Gusmão, L. F. P. (2015). Characterization saprobic fungi on leaf litter of two species of trees in the Atlantic Forest, Brazil. Brazilian Journal of Microbiology, 46, 1027–1035. https://doi.org/10.1590/S1517-838246420140548

Cutz-Pool, L. Q., Ramírez-Vázquez, U. Y, Castro-Pérez, J. M, Puc-Paz, W. A., & Ortiz-León, H. J. (2016). La artropo-
dofauna asociada a Tillandsia fasciculata en bajos inundados de tres sitios de Quintana Roo, México. Entomología Mexicana, 3, 576–581. 

Espejo-Serna, A., & López-Ferrari, A. R. (2018). La familia Bromeliaceae en México. Botanical Sciences, 96, 533–554. https://doi.org/10.17129/botsci.1918 

Espejo-Serna, A., López-Ferrari, A., & Ramírez-Murillo, I. (2010). Bromeliaceae. Flora del Bajío y Regiones Adyacentes, 165, 1–82.

Goffredi, S. K., Kantor, A. H., & Woodside, W. T. (2011). Aquatic Microbial Habitats Within a Neotropical Rain-
forest: Bromeliads and pH-Associated Trends in Bacterial Diversity and Composition. Microbial Ecology, 61, 529–542. https://doi.org/10.1007/s00248-010-9781-8 

Gomes, F. C. O., Safar, S. V. B., Marques, A. R., Medeiros, A. O., Santos, A. R. O., Carvalho, C. et al. (2015). The diversity and extracellular enzymatic activities of yeasts isolated from water tanks of Vriesea minarum, an endangered bromeliad species in Brazil, and the description of Occultifur brasiliensis f.a., sp. nov. Antonie van Leeuwenhoek, International Journal of General and Molecular Microbiology, 107, 597–611. https://doi.org/10.1007/s10482-014-0356-4 

Gouda, E. J., Butcher, D., & Dijkgraaf, L. (2024) Encyclopaedia of Bromeliads, Version 5. Utrecht University Botanic Gardens, online (accessed: 02-10-2024): http://bromeliad.nl/encyclopedia/ 

Grossart, H. P., Van den Wyngaert, S., Kagami, M., Wurzbacher, C., Cunliffe, M., & Rojas-Jimenez, K. (2019). Fungi in aquatic ecosystems. Nature Reviews Microbiology, 17, 339–354. https://doi.org/10.1038/s41579-019-0175-8 

Grothjan, J. J., & Young, E. B. (2019). Diverse microbial communities hosted by the model carnivorous pitcher plant Sarracenia purpurea: Analysis of both bacterial and eukaryotic composition across distinct host plant populations. PeerJ, 2019, e6392. https://doi.org/10.7717/peerj.6392 

Hernández, H. M., & Bárcenas, R. T. (1995). Endangered Cacti in the Chihuahuan Desert: I. Distribution Patterns. Conservation Biology, 9, 1176–1188. https://doi.org/10.1046/j.1523-1739.1995.9051169.x-i1 

Hernández, H. M., & Gómez-Hinostrosa, C. (2005). Cactus diversity and endemism in the Chihuahuan Desert Region. EnJ. L. Cartron, G. Ceballos, & R. Felger (Eds.), Biodiversity, ecosystems and conservation in Northern Mexico (pp264–275). New York: Oxford University Press.

Hernández-Magaña, R., Hernández-Oria, J. G., & Chávez, R. (2017). Datos para la conservación florística en función de la amplitud geográfica de las especies en el Semidesierto Queretano, México. Acta Botanica Mexicana, 140, 105. https://doi.org/10.21829/abm99.2012.22 

Herrera-García, J. A., Martínez, M., Zamora-Tavares, P., Vargas-Ponce, O., Hernández-Sandoval, L., & Rodríguez-Zaragoza, F. A. (2022). Metabarcoding of the phytotelmata of Pseudalcantarea grandis (Bromeliaceae) from an arid zone. PeerJ, 10, e12706. https://doi.org/10.7717/peerj.12706 

Huson, D. H., Beier, S., Flade, I., Górska, A., El-Hadidi, M., Mitra, S. et al. (2016). MEGAN Community Edition – Interactive Exploration and Analysis of Large-Scale Microbiome Sequencing Data. Plos Computational Biology, 12, 1–12. https://doi.org/10.1371/journal.pcbi.1004957 

INAFED (Instituto Nacional para el Federalismo y el Desarrollo Municipal). (2012). Zimapán. Enciclopedia de los municipios y Delegaciones de México. http://www.inafed.gob.mx/work/enciclopedia/EMM13hidalgo/municipios/13084a.html 

Jones, R. I. (2000). Mixotrophy in planktonic protists: an overview. Freshwater Biology, 45, 219–226. https://doi.org/10.1046/j.1365-2427.2000.00672.x 

Kitching, R. (2000). Food webs and container habitats: the natural history and ecology of phytotelma. Cambridge, U.K.: Cambridge University Press. https://doi.org/10.1017/CBO9780511542107 

Kitching, R. L. (2001). Food webs in phytotelmata: “Bottom-Up” and “Top- Down’” Explanations for Community Structure. Annual Review of Entomology, 46, 729–760. https://doi.org/10.1146/annurev.ento.51.110104.151120 

Krauss, G. J., Solé, M., Krauss, G., Schlosser, D., Wesenberg, D., & Bärlocher, F. (2011). Fungi in freshwaters: Ecology, physiology and biochemical potential. FEMS Microbiology Reviews, 35, 620–651. https://doi.org/10.1111/j.1574-6976.20
11.00266.x 

Louca, S., Jacques, S. M. S., Pires, A. P. F., Leal, J. S., González, A. L., Doebeli, M. et al. (2017). Functional structure of the bromeliad tank microbiome is strongly shaped by local geochemical conditions. Environmental Microbiology, 19, 3132–3151. https://doi.org/10.1111/1462-2920.13788 

Marino, N. A. C., Srivastava, D. S., & Farjalla, V. F. (2013). Aquatic macroinvertebrate community composition in tank-bromeliads is determined by bromeliad species and its constrained characteristics. Insect Conservation and Diversity, 6, 372–380. https://doi.org/10.1111/j.1752-4598.2012.00224.x 

Mogi, M. (2004). Phytotelmata: hidden freshwater habitats supporting unique faunas. In C. M. Yule, & H. S. Yong (Eds.), Freshwater invertebrates of the Malaysian region (pp. 13–22). Kuala Lumpur, Malaysia: Academy of Sciences Malaysia.

Ngai, J. T., & Srivastava, D. S. (2006). Predators accelerate nutrient cycling in a bromeliad ecosystem. Science, 314, 963. https://doi.org/10.1126/science.1132598 

Nievola, C. C., Mercier, H., & Majerowicz, N. (2001). Levels of Nitrogen assimilation in bromeliads. Journal of Plant Nutrition, 24, 1387–1398. https://doi.org/10.1081/PLN-100106989 

Ramírez-Murillo, I., Carnevali-Fernández, G., & Chi-May, F. (2004). Guía ilustrada de las Bromeliaceae de la porción mexicana de la península de Yucatán. Yucatán: Centro de Investigación Científica de Yucatán. 

Ramos, G. J. P., & do Nascimento Moura, C. W. (2019). Algae and cyanobacteria in phytotelmata: diversity, ecological aspects, and conservation. Biodiversity and Conservation, 28, 1667–1697. https://doi.org/10.1007/s10531-019-01771-2 

Rodríguez-Núñez, K. M., Rullan-Cardec, J. M., & Ríos-Velázquez, C. (2018). The metagenome of bromeliads phytotelma in Puerto Rico. Data in Brief, 16, 19–22. https://doi.org/10.1016/j.dib.2017.10.065 

Rojas, S., Castillejos-Cruz, C., & Solano, E. (2013). Florística y relaciones fitogeográficas del matorral xerófilo en el valle de Tecozautla, Hidalgo, México. Botanical Sciences, 91, 273–294. https://doi.org/10.17129/botsci.8 

Rzedowski, J. (2006). Vegetación de México. México D.F.: Conabio.

Simão, T. L. L., Borges, A. G., Gano, K. A., Davis-Richardson, A. G., Brown, C. T., Fagen, J. R. et al. (2017). Characterization of ciliate diversity in bromeliad tank waters from the Brazilian Atlantic Forest. European Journal of Protistology, 61, 359–365. https://doi.org/10.1016/j.ejop.2017.05.005 

Simão, T. L. L., Utz, L. R. P., Dias, R., Giongo, A., Triplett, E. W., & Eizirik, E. (2020). Remarkably complex microbial community composition in bromeliad tank waters revealed by eDNA metabarcoding. Journal of Eucaryotic Microbiology, 67, 593–607. https://doi.org/10.1111/jeu.12814 

Simpson, M. G. (2006). Plant systematics. Amsterdam: Elsevier/Academic Press.

Takahashi, C. A., & Mercier, H. (2011). Nitrogen metabolism in leaves of a tank epiphytic bromeliad: characterization of a spatial and functional division. Journal of Plant Physiology, 168, 1208–1216. https://doi.org/10.1016/j.jplph.2011.01.008 

Tree of Life Web Project, (2019). Tree of life. Website. http://tolweb.org/tree/ 

White, T. J., Bruns, T., Lee, S., & Taylor, J. (1990). Amplification and direct sequencing of fungal ribosomal RNA genes for Phylogenetics. In M. A. Innis, D. H. Gelfand, J. J. Sninsky, T. J. White (Eds.), PCR Protocols (January) (pp. 315–322). San Diego, CA: Academic Press. https://doi.org/10.1016/b978-0-12-372180-8.50042-1 

Williams, D. D. (2007). Other temporary water habitats. The Biology of temporary waters. Oxford, UK: Oxford University Press. https://doi.org/10.1093/acprof:oso/9780198528128.001.0001

César Marco Aurelio Jurado-Vargas ^a, *, José Cruz-de León ^b, José Tulio Mendez-Montiel ^c

^a Universidad Michoacana de San Nicolás de Hidalgo, Facultad de Biología, Laboratorio de Investigación en Invertebrados, Ciudad Universitaria, Av. Fco. J. Mujica s/n, 58030 Morelia, Michoacán, México

^b Universidad Michoacana de San Nicolás de Hidalgo, Facultad de Ingeniería en Tecnología de la Madera, Laboratorio de Conservación y Preservación de la Madera, Ciudad Universitaria, Av. Fco. J. Mujica s/n, 58030 Morelia, Michoacán, México 

^c Universidad Autónoma Chapingo, Dirección de Ciencias Forestales, Carretera Federal México-Texcoco Km 38.5, 56230 Texcoco, Estado de México, México

*Autor para correspondencia: cjurado@umich.mx (C.M.A. Jurado-Vargas)

Recibido: 02 abril 2024; aceptado: 11 marzo 2025

http://zoobank.org/urn:lsid:zoobank.org:pub:4737516A-ED56-4106-B714-86B23F67BCF4 

Resumen

A partir de un análisis morfológico y taxonómico de adultos del género Calymmaderus Solier, 1849 (Ptinidae: Dorcatominae), se describen y proponen 2 nuevas especies para el Neotrópico en México: C. robustus sp. nov. y C. semioblongus sp. nov. Ellas se distinguen de las 7 especies reportadas y reconocidas actualmente para México con base en su coloración, pubescencia y estrías elitrales laterales. Se describe la estructura genital de machos.

Palabras clave: Carcoma; Edificios históricos; Xilófagos

Two new Neotropical species of the genus Calymmaderus (Coleoptera: Ptinidae), associated to structural wood in Taretan, Michoacán, Mexico

Abstract

Through morphological and taxonomic analysis of adults of the genus Calymmaderus Solier, 1849 (Ptinidae: Dorcatominae), 2 new Neotropical species in Mexico are described and proposed: C. robustus sp. nov. and C. semioblongus sp. nov. They are distinguished from the 7 species currently reported and recognized for Mexico based on their coloration, pubescence and lateral elitral striae. The genital structure of males is described.

Keywords: Woodworm; Historic buildings; Xylophages

Introducción

El género Calymmaderus incluye especies de escarabajos xilófagos de distribución mundial, para el cual se reconocen 89 especies americanas (Blackwelder, 1945; Lüer y Honour, 2017; Toskina, 2000; White, 1974, 1982, 1983, 1984), de las que 7 especies se encuentran en México: C. dejeani (Pic, 1905), C. donckieri (Pic, 1904), C. oblongus (Gorham, 1883), C. pupatus (Gorham, 1883), C. semirufus (Champion, 1913), C. sharpi (Gorham, 1886) y C. subvestitus (Champion, 1913) (White, 1983; Zaragoza et al., 2016). El estudio de las especies de este género es complicado debido a la falta de revisiones taxonómicas, lo limitado de sus descripciones diagnósticas y la carencia, en la mayoría de los casos de ilustraciones de los órganos genitales, estudio que le da mayor robustez a la determinación de especies (Bercedo et al., 2008; Lüer y Honour, 2017; Viñolas, 2018). Los miembros de Calymmaderus se distinguen de las demás especies de Ptinidae por su cuerpo alargado y oblongo, antenas con los 2 últimos segmentos de la clava estrechamente unidos, coxas protorácicas expuestas ventralmente, un lóbulo metasternal bifurcado que aloja al último segmento antenal cuando el cuerpo está en reposo y el número de suturas elitrales laterales (Arango, 2012; Español, 1992; White, 1971). Las especies de este género son de importancia económica al dañar la madera estructural de edificios históricos y bienes culturales. La especie más conocida en México es C. oblongus (Gorham, 1883), a la que varios autores señalan como asociada al deterioro de la madera (Bercedo et al., 2008; Cibrián et al., 1995; Jurado-Vargas, 2020; Jurado-Vargas y Cruz, 2010, 2020; Jurado-Vargas et al., 2003; Pichardo et al., 2017; White, 1974).

El presente estudio tiene como objetivo describir 2 especies nuevas de Calymmaderus, que fueron encontradas en la localidad de Taretan, Michoacán, México, ubicada en la Zona de Transición Mexicana, que es un área de alta diversidad y endemismos de artrópodos y presenta la mayor mezcla biótica entre elementos neárticos y neotropicales (Halffter, 2017). Ambas especies representan taxones morfológicamente diferentes a las especies descritas en la literatura conocida para este grupo. White fue el último investigador que publicó datos sobre especies de Calymmaderus y otros géneros de escarabajos de la familia Ptinidae americanas entre 1981 y 1984, dejando pendientes algunos ejemplares con estatus incierto aún por resolver. En este trabajo presentamos la descripción y propuesta de las 2 nuevas especies de Calymmaderus referidas.

Materiales y métodos

El área de estudio corresponde a la localidad de Taretan, Michoacán, México (1,140 m snm, 19°20’3.32” N, 101°55’3.02” O) (fig. 1), que presenta un clima cálido A (w), con precipitación media anual de 1,240 mm y temperatura media anual 25° C (INEGI, 2010).

Se recolectaron 463 ejemplares del género Calymmaderus de la techumbre de madera del templo de San Ildefonso por medio de 2 trampas de luz blanca, durante el periodo de emergencia de los adultos en los meses de junio-agosto del 2017 y 2018. Los ejemplares se fijaron en una solución de alcohol al 80%. La determinación de los ejemplares se realizó usando descripciones y claves de identificación para el género y especies de Calymmaderus (Arango, 2012; White,1971, 1974, 1982, 1983, 1984). En el proceso, la preparación de los órganos se realizó mediante la técnica de montaje permanente en laminillas con resina sintética (Gaviño et al., 2004). 

La descripción de los caracteres morfológicos de los ejemplares adultos se realizó mediante un microscopio estereoscópico Nikon a 45 aumentos. Se obtuvieron imágenes de los ejemplares en posición dorsal, lateral y ventral, además de metasterno, abdomen y antenas, mediante un microscopio estereoscópico Carl Zeiss (modelo Axio Zoom V16). Las imágenes de las preparaciones de la estructura genital se lograron a través de un microscopio compuesto Marca Leica a 100 aumentos y una cámara Panasonic adaptada a la distancia focal del ocular. Para obtener detalles adicionales de la morfología externa de los ejemplares, se tomaron imágenes por medio del microscopio electrónico de barrido modelo JSM-6400.

Se determinaron las medidas de largo y ancho de 30 ejemplares de cada una de las especies que se describen con un vernier digital, con las que se realizó un análisis estadístico descriptivo básico de los parámetros utilizados para su descripción. La fenología de emergencia de adultos se determinó mediante gráficos de los registros mensuales de captura de los ejemplares adultos en los periodos de trabajo. Los holotipos y paratipos de las 2 especies se depositaron en la Colección de Invertebrados (Insectos Xilófagos) de la Facultad de Biología de la Universidad Michoacana (CIFBUM-XIL).

Resultados

Descripciones

Calymmaderus robustus Jurado-Vargas sp. nov. (figs. 2-7, 14)

http://zoobank.org/urn:lsid:zoobank.org:act:1C158DC5-F92E-4A6C-A089-09DC362DFC6E 

Diagnosis. Cuerpo robusto en vista lateral, 1.9 veces más largo que ancho, color negro uniforme mate, pubescencia blanquecina decumbente y abundante, separada menos de su longitud, élitros paralelos después de la base hasta 3/4 partes; antenas desde la base de café rojizo a café negruzco en los últimos segmentos; metasterno con menos pubescencia que resto del cuerpo. Lóbulo mestasternal con muesca profunda en forma característica de U.

Holotipo ♂, largo 3.8 mm, ancho 2.1 mm. Cuerpo robusto en vista lateral, 1.9 veces más largo que ancho (figs. 2, 3), color negro mate, excepto en palpos maxilares y labiales, que presentan el segmento basal café oscuro y los otros segmentos café rojizo. Tarsos de color café rojizo. Pubescencia decumbente blanquecina, abundante, uniforme en todo el cuerpo. Puntuaciones elitrales de la superficie ampliamente distribuidas, no alineadas e intercaladas con otras puntuaciones diminutas en todo el cuerpo y separadas 1.0 veces su diámetro. Cabeza: ojos grandes y abultados, distancia interocular 1.1 veces el diámetro vertical de un ojo. Clava antenal ligeramente mayor (1.1 veces) que el resto de los segmentos; 9º segmento de la clava antenal ligeramente más largo que los segmentos 10º y 11º (fig. 6). Pronoto: acampanado, 1.9 veces más ancho que largo; borde anterior curvo y márgenes laterales redondeados. Superficie densamente punteada y pilosa, con las puntuaciones laterales equidistantes y separadas en general el equivalente a su diámetro; en el disco las puntuaciones son más separadas (1-2 veces su diámetro). Élitro: puntuaciones del disco y laterales separadas de 1 a 2 veces su diámetro (algunas veces un poco más separadas y alargadas); puntuaciones más cercanas a la base elitral más aglutinadas y puntuaciones laterales hacia la parte distal del élitro más alargadas; ranura lateral visible después de la base del tercer esternito hasta el ápice (fig. 4), abarcando menos de la mitad del élitro. Metasterno: convexo, más ancho que largo, carinas bien delimitadas; puntuaciones cercanas al proceso metasternal más pequeñas, separadas 1.0 veces su diámetro; puntuaciones se agrandan más hacia la parte media y a los lados, separadas de 1.0 a 1.5 veces su diámetro; en la parte media y hasta el borde posterior son más pequeñas y menos densas; surco longitudinal corto y no muy marcado (fig. 5). Abdomen: primero, segundo y quinto esternitos más o menos del mismo largo; segundo con borde posterior ligeramente curvo en centro; tercero un poco más corto que anteriores, y cuarto más corto que el resto (fig. 3). Edeago: longitud: 1.1 mm; anchura 0.48 mm. Parámeros bifurcados apicalmente, con borde apical redondeado; piezas accesorias de los parámeros 4.2 veces más largos que su ancho, con pilosidad larga desde la mitad hasta su extremo. Endófalo: ápice más esbelto que la base, terminando en punta con un diente curvo en forma de gancho, saco interno provisto de por lo menos doce espinas transversales a lo largo; las 2 más cercanas a la base 2 veces más largas que las demás y de posición paralela; 2 espinas al centro más pequeñas y entrecruzadas con las espinas basales más largas (fig. 14).

Paratipo ♀. Aspecto general del cuerpo similar al macho. Largo 4.1 ancho 2.3 mm, ojos evidentemente más grandes y abultados que el macho, distancia interocular 1.3 veces el diámetro vertical de un ojo. Tercera y cuarta sutura de los esternitos curvada a los lados.

Resumen taxonómico

Etimología. El epíteto de la especie robustus deriva de la forma robusta del tórax en vista lateral (mucho más alta que el abdomen), que caracteriza y diferencia a los ejemplares de esta especie en comparación con las especies conocidas.

Material examinado. Holotipo ♂: CIFBUM-XIL Núm. 224. México: Michoacán. Taretan. 19.VII.2017. C. Jurado Col. Trampa de luz blanca, madera estructural de pino. 19°20’3.32” N. 101°55’3.02” O. 1,140 m snm. Paratipos: 28; 13 ♂, 17 ♀. CIFBUM-XIL Núms. 226-252, con los mismos datos del holotipo. 

Comentarios taxonómicos

Variabilidad: largo 3.1-4.2 mm (media 3.72) ancho 1.7-2.3 mm (media 2.08). Macho más pequeño que la hembra (de 3.1 a 3.7 mm; tabla 1). Ojos más pequeños, distancia interocular de 1.0 a 1.1 veces del diámetro vertical del ojo; último esternito normal, con sutura recta. Hembra: 3.8 a 4.2 mm, ojos más grandes y abultados que el macho, distancia interocular de 1.2 a 1.3 veces el diámetro vertical de un ojo; último esternito con sutura ligeramente curvada en el centro. Especie con morfología poco variable; color general negruzco mate, pubescencia blanquecina uniforme, algunas veces con pubescencia menos abundante en el metasterno.

Especie de hábitos nocturnos asociada con madera estructural de Pinus sp.; los ejemplares se capturaron en el interior de la techumbre de madera del templo de “San Ildefonso” Taretan, con trampa de luz. La emergencia de adultos inicia la última semana de junio, con máximo a mediados de julio y disminuye la última semana de julio; la emergencia es rara en agosto. Cohabita con otras especies de Ptinidae y termes, reinfestando durante muchos años la madera del mismo sitio (fig. 7). 

Tabla 1

Medidas y variación de largo y ancho de machos y hembras adultos de Calymmaderus robustus sp. nov. 

Medidas	Promedio (mm)	Error estándar	Rango (mm)
N (hembras) = 13 N (machos) = 17	Machos	Hembras	Machos	Hembras	Machos	Hembras
Longitud	3.438	3.947	0.055	0.032	3.1 – 3.7	3.8 – 4.2
Ancho	1.931	2.194	0.036	0.020	1.2 – 2.1	2.1 – 2.3

De acuerdo con la clave de identificación usada para especies de Calymmaderus (White, 1983), los ejemplares son definitivamente diferentes a las descripciones de las especies mexicanas descritas, considerando la variación en el conjunto de los siguientes caracteres. Todas las especies citadas para México presentan cuerpo oblongo o semiesférico (C. sharpi) en vista lateral; en cuanto al color, los ejemplares descritos de todas las especies van de café rojizo o café oscuro a casi negro, mientras que la coloración del integumento de la especie que se describe es negro mate uniforme. En cuanto a la pubescencia, a diferencia de las especies conocidas en las que tiene tonalidades amarillentas a grisáceas, la especie propuesta presenta pubescencia blanquecina, que contrasta fuertemente con el color del cuerpo. La mayoría de las poblaciones de las especies comparten un tamaño de longitud y ancho similares, excepto C. donckieri y C. subvestitus, que son notablemente más pequeñas. La carencia de información acerca de la armadura genital de las especies no permite hacer comparaciones al respecto. Sin embargo, se presenta la comparación de la armadura genital del macho de las 2 especies propuestas en este documento y C. oblongus, especie mejor conocida de amplia distribución en México (figs. 14-16), lo que respalda la diferenciación entre ellas. 

Calymmaderus semioblongus Jurado-Vargas sp. nov. (figs. 8-13, 15)

http://zoobank.org/urn:lsid:zoobank.org:act:7170D451-739D-4507-96C3-A826C5BA4E13 

Diagnosis. Forma oblonga, esbelto en vista dorsal, 2.1 veces más largo que ancho, élitros paralelos después de la base hasta 3/4 partes de su extensión; superficie del cuerpo de coloración homogénea de café oscuro a casi negro; pubescencia amarillenta densa y decumbente, separada menos del largo de su longitud; puntuaciones laterales de élitros más agrandadas en la base que en el resto del élitro.

Holotipo ♂, largo 3.8 mm, ancho 1.8 mm. Coloración de café oscuro a casi negro; superficie brillante; antenas y tarsos con la misma coloración del cuerpo; palpos labiales y palpos maxilares café rojizo. Cuerpo oblongo y alargado, 2.1 veces más largo que ancho (figs. 8, 9). Vestidura: pubescencia amarillenta, densa, decumbente y abundante en todo el cuerpo, puntuaciones uniformes en todo el cuerpo, excepto las puntuaciones laterales del élitro que se presentan de forma aglutinada e irregular (fig. 10). Cabeza: ojos pequeños separados 1.4 veces el diámetro vertical de un ojo. Clava antenal 1.3 veces más larga que el resto de los segmentos, noveno segmento de la clava antenal del mismo largo que el décimo y undécimo (fig. 12). Pronoto: acampanado 1.6 veces más largo que ancho, convexo dorsalmente; margen lateralmente redondeado, con un reborde lateral y borde anterior regularmente curvo, no proyectado; disco no prominente; pubescencia uniforme, superficie densamente punteada. Élitro: puntuaciones elitrales irregulares, no alineadas en hileras, separadas de 1 a 2 veces su diámetro, en el disco elitral también a la misma distancia; puntuaciones laterales de la base un poco más grandes y algunas están separadas el equivalente a su diámetro; en el tercio posterior del élitro las puntuaciones son más pequeñas; puntuaciones basales laterales aglutinadas formando una estría a la altura del segundo esternito, que continua hasta el ápice ya bien marcada como ranura basal; por encima otra línea no muy marcada forma otra estría también a nivel del segundo esternito, la ranura ocupa ligeramente más de la mitad del élitro hasta el ápice. Metasterno: ancho del lóbulo metasternal, escasamente mayor que su longitud, muesca profunda, ápice del lóbulo muy arqueado en forma de V; puntuaciones más grandes cerca del lóbulo y a lo largo del borde anterior del metasterno, separadas el equivalente a su diámetro; a los lados las puntuaciones son más espaciadas de 1.0 a 1.5 veces su diámetro, algunas separadas hasta 2 veces su diámetro; del centro hasta el borde posterior, las puntuaciones son más pequeñas y escasas, separadas de 1.0 a 2.0 veces su diámetro; surco longitudinal ligeramente marcado y extendido hasta la mitad del metasterno (fig. 11). Abdomen: segundo ventrito más largo que el resto; el primero y tercero de largo similar, el cuarto es el más estrecho, el quinto presenta una concavidad paralela al ventrito cerca del borde posterior (fig. 9). Edeago: longitud 0.65 mm; anchura 0.41 mm, parámeros bifurcados apicalmente, el más grande de apariencia bilobulada en el extremo; piezas accesorias de los parámeros 4.5 veces más largos que anchos, con pilosidades desde la mitad hasta el ápice. Endofalo: ápice redondeado, saco interno con un par de dientes paralelos al endofalo en la base; sobre estos dientes, hay 2 dientes adicionales curvos con aspecto de media luna (fig. 15).

Paratipo ♀. Aspecto general del cuerpo similar al macho. Largo 4.1 mm. Ancho 1.9 mm. Distancia interocular 1.4 veces el diámetro vertical del ojo, segunda y tercera suturas abdominales curvadas en el centro, quinta sutura ligeramente curvada a los lados.

Resumen taxonómico

Etimología. El epíteto semioblongus es aplicado por la similitud morfológica externa con la especie oblongus, conocida para varias localidades de México.

Material examinado. Holotipo ♂: CIFBUM-XIL No. 253, Michoacán, Taretan. 18.VIII.2017. C. Jurado Col. Trampa de luz blanca, madera estructural de pino. Col. C. Jurado. 19°20’3.32” N. 101°55’3.02” 0. 1,150 m.snm. Paratipos: 29 individuos CIFBUM-XIL Núms. 255 a 282 (14 ♂ y 14 ♀), mismos datos que el holotipo.

Comentarios taxonómicos

Variabilidad: largo: 3.0-4.8 mm; ancho 1.4- 2.1 mm. Especie muy homogénea. Los machos notablemente menores que las hembras, con tamaño que varía de 3.0 a 3.7 mm (a veces hasta 3.8 mm), con ojos más pequeños y menos separados que en las hembras (distancia interocular de 0.8 a 1.2 el diámetro vertical de un ojo); área frontal algo más aplanada que la hembra, surco longitudinal del metasterno más largo que en la hembra.

Tabla 2

Medidas y variación de largo y ancho de machos y hembras adultos de Calymmaderus semioblongus sp. nov. 

Medidas	Promedio (mm)	Error estándar	Rango (mm)
N (machos) = 15  N (hembras) = 15	Machos	Hembras	Machos	Hembras	Machos	Hembras
Longitud	3.507	4.133	0.059	0.070	3.0-3.8	3.8-4.8
Ancho	1.627	1.886	0.025	0.026	1.4-1.7	1.7-2.1

Tabla 3. Medidas y variación de largo y ancho de machos y hembras adultos de Calymmaderus oblongus de la localidad de Tacícuaro, Michoacán.

Medidas	Medidas	Promedio (mm)	Error estándar	Rango (mm)
N (machos) = 15  N (hembras) = 15	n♂= 15 n♀= 15	♂	♀	♂	♀	♂	♀
Longitud	Longitud	3.507	4.133	0.060	0.070	3.0-3.8	3.8-4.8
Ancho	Ancho	1.627	1.887	0.025	0.026	1.4-1.7	1.7-2.1

Hembra: cuerpo más grande que el macho, de 3.9 a 4.8 mm, ojos más grandes y separados que el macho (distancia interocular de 1.4 a 1.6 veces el diámetro vertical del ojo), última sutura esternal más curva a los lados que en el macho. 

Especie de hábitos nocturnos asociada con madera estructural de Pinus sp. Se capturó en el interior de la techumbre de madera del templo de San Ildefonso en Taretan, Michoacán, con trampa de luz. La emergencia de los adultos inicia la última semana del mes de junio, en el mes de julio se registra la máxima emergencia con el inicio del verano, hasta disminuir en agosto con pocos ejemplares y en septiembre su emergencia es rara. Cohabita con otras especies xilófagas de Ptinidae y de termitas. Reinfesta las estructuras de madera por muchos años en el mismo sitio (fig. 13).

Calymmaderus semioblongus sp. nov. es una especie diferente a las otras especies mexicanas del género (White, 1983). Muestra similitud morfológica con la especie oblongus, pero con diferencias evidentes como la coloración del integumento (café oscuro en la especie descrita, a diferencia de oblongus que tiende más a café rojizo; sus medidas de longitud y ancho del cuerpo son menores (3.0 a 4.5 mm de longitud y ancho 1.4 a 2.1 mm, tabla 2), en comparación con C. oblongus (de 3.3 a 5.2 mm de largo y ancho de 1.6 a 2.4 mm, tabla 3). Ambas especies presentan de 2 a 3 hileras de puntuaciones laterales desde la base elitral que forman estrías; en oblongus, la estría más externa y cercana a la ranura elitral es más corta y las otras 2 estrías son menos marcadas que en la especie que se describe. La comparación de la estructura genital de machos de C. oblongus y C. semioblongus sp. nov. también mostró diferencias claras en el número y posición de espinas en el endofalo de estas 2 especies; C. oblongus presenta 2 espinas en forma de cornamenta en la parte más alejada de la base (figs. 14-16). 

Agradecimientos

Al Laboratorio de Investigación en Invertebrados de la Facultad de Biología y a la División de Estudios de Posgrado de la Facultad de Ingeniería en Tecnología de la Madera de la UMSNH, por apoyar el proyecto de insectos xilófagos en madera estructural en Michoacán. A Mauricio Quesada, jefe del laboratorio Nacional de Síntesis Ecológica, ENES, UNAM, Unidad Morelia, por facilitar el uso del microscopio Axiostar Zoom V16, para la toma de imágenes de ejemplares. A las autoridades eclesiásticas del Templo de la “Asunción” de Taretan (en especial al párroco Francisco Javier Valencia Durón), por permitir el trabajo de campo en el inmueble. A Roberto Sibaja por la elaboración y ubicación del mapa del sitio. Finalmente agradecer a José Fernando Villaseñor Gómez, de la Facultad de Biología, quien colaboró en la última revisión del texto, con sugerencias acertadas y positivas.

Referencias

Arango, R. A. y Young, D. K. (2012). Death-watch and spider beetles of Wisconsin—Coleoptera: Ptinidae. USDA Forest Service, Forest Products Laboratory, General Technical Report FPL-GTR-209. https://doi.org/10.2737/FPL-GTR-209 

Bercedo, P., García, B. R. y Arnaiz, L. (2008). El género Calymmaderus Solier, 1849 nuevo para Canarias y descripción de una nueva especie (Coleoptera: Ptinidae: Dorcatominae). Boletín de la Sociedad Entomológica Aragonesa, 42, 33–35.

Blackwelder, R. E. (1945). Checklist of the coleopterous insects of México, Central America, The West Indies, and South America (Ptinidae, Gnostidae and Anobiidae). Bulletin of the United States National Museum, 185, 401–406. https://doi.org/10.5479/si.03629236.185.3 

Cibrián, T. D., Méndez M. J. T., Campos, B. R., Harry, O. Y. y Flores, L. J. (1995). Insectos forestales de México. Texcoco, Estado de México: Universidad Autónoma Chapingo.

Español, C. F. (1992). Coleoptera: Anobiidae. Fauna Ibérica, Vol. 2. Museo Nacional de Ciencias Naturales. Madrid: CSIC.

Gaviño, G., Juárez, L. C. y Figueroa, T. H. (2004). Técnicas biológicas selectas de laboratorio y campo. México D.F.: Limusa.

Halffter, G. (2017). La Zona de Transición Mexicana y la megadiversidad de México: del marco histórico a la riqueza actual. Dugesiana, 2, 77–89. https://doi.org/10.32870/dugesiana.v24i2.6572

INEGI (Instituto Nacional de Geografía y Estadística). (2010). Compendio de información geográfica municipal. Taretan, Michoacán de Ocampo. Clave geoestadística 16087. Instituto Nacional de Geografía y Estadística. Recuperado el 17 diciembre, 2024 de: https://www.inegi.org.mx/contenidos/app/mexicocifras/datos_geograficos/16/16087.pdf

Jurado-Vargas, C. M. A. (2020). Incidencia y daño de insectos en la techumbre de madera de cinco edificios históricos (Templos) de Michoacán (Tesis doctoral). Facultad de Ingeniería en Tecnología de la madera, Universidad Michoacana de San Nicolás de Hidalgo. Morelia, Michoacán.

Jurado-Vargas, C. M. A., Campos, B. R. y Cruz-de León, J. (2003). Anóbidos asociados a la madera en uso en dos monumentos históricos de Michoacán. Entomología Mexicana, 2, 803–806.

Jurado-Vargas, C. M. A. y Cruz-de León, J. (2010). Insectos que dañan la madera de edificios históricos de Morelia, Michoacán. Entomología Mexicana, 9, 103–110.

Jurado-Vargas, C. M. A. y Cruz-de León, J. (2020). Evaluación de la incidencia de insectos xilófagos en la madera estructural del Templo de Ucareo en Michoacán. Entomología Mexicana, 7, 389–395.

Lüher, A. H. y Honour, R. (2017). Descripción de dos especies nuevas de Calymmaderus Solier, 1849 (Coleoptera: Ptinidae) de Chile. Boletín de la Sociedad Entomológica Aragonesa, 60, 105–110.

Pichardo, S. L., San Marino, C. A., Jiménez, Q. E. y Torres, H. B. (2017). Familia Ptinidae. En D. Cibrian-Tovar (Ed.), Fundamentos de entomología forestal (pp. 268–272). Texcoco, Estado de México: Universidad Autónoma Chapingo. 

Toskina, I. N. (2000). New wood-boring beetles (Coleoptera: Anobiidae) from Paraguay. Russian Entomological Journal, 9, 199–240.

Viñolas, A. (2018). Nuevos datos sobre la validez específica de Ernobius vinolasi Novoa y Baselga, 2000 (Coleoptera: Ptinidae: Ernobiinae). Arquivos Entomoloxicos, 19, 75–80. https://doi.org/10.5281/zenodo.12767756 

White, R. E. (1971). Key to North American genera of Anobiidae, with phylogenetic and synonymic notes (Coleoptera). Annals of the Entomological Society of America, 64, 179–191. https://doi.org/10.1093/aesa/64.1.179 

White, R. E. (1974). The Dorcatominae and Tricoryninae of Chile (Coleoptera: Anobiidae). Transactions of the American Entomological Society, 100, 191–253.

White, R. E. (1982). A catalog of the Coleoptera of America North of Mexico. Family Anobiidae. Systematic Entomology Laboratory, Agricultural Research Service, U.S. Dept. of Agriculture, U.S.A.

White, R. E. (1983). Keys to Neotropical species of Calymmaderus Solier and species of Calytheca White, taxonomic notes (Coleoptera: Anobiidae). Proceedings of the Entomological Society of Washington, 85, 229–250.

White, R. E. (1984). Eight new species of Anobiidae (Coleoptera) from Jamaica. The Coleopterists Bulletin, 38, 240–248.

Zaragoza, S., Navarrete-Heredia, J. L. y Ramírez, G. E. (2016). Temolines. Los coleópteros entre los antiguos mexicanos. Ciudad de México: Instituto de Biología, UNAM. Disponible: http://www.ibiologia.unam.mx/barra/publicaciones/Temolines.pdf

Francisco Lorea-Hernández*

Instituto de Ecología, A.C., Carretera antigua a Coatepec 351, Col. El Haya, 91073 Xalapa, Veracruz, Mexico 

*Corresponding author: francisco.lorea@inecol.mx (F. Lorea-Hernández)

Received: 27 February 2024; accepted: 21 January 2025

Abstract

Following a detailed morphological survey of the Licaria collections in several herbaria, various taxonomic entities not recognized before were detected. Here, 11 new species of Licaria from Mesoamerica are described and illustrated. Possible relations to other species in the genus are commented.

Keywords: Lauraceae of Central America; Lauraceae of Mexico; Licaria of Central America; Licaria of Mexico

Nuevas especies de Licaria (Lauraceae) de Mesoamérica

Resumen

Como resultado de un análisis morfológico detallado de las colecciones del género Licaria en diferentes herbarios, se detectaron varias entidades taxonómicas no reconocidas previamente. Aquí se describen e ilustran 11 especies nuevas del género Licaria de la región mesoamericana. Se comentan además las posibles relaciones con otras especies del género.

Palabras clave: Lauraceae de Centroamérica; Lauraceae de México; Licaria de Centroamérica; Licaria de México

Introduction

Licaria is an endemic genus to the Americas represented mostly by medium-sized to large tree species that grow principally in the intertropical region of this part of the world. The hermaphrodite, perigynous flowers with only the third whorl of stamens fertile, whose anthers are bisporangiate, as well as the fruit often seated on a double rimmed cupule, constitute the combination of characters that distinguishes the genus among the Lauraceae. Licaria was last revised by Kurz (2000), who recognized 38 species, including 12 in the Mesoamerican area. That work is an adaptation with minor changes of Kurz doctoral dissertation (Kurz, 1983). Since then, in the lapse of 40 years, subtracting new combinations and synonyms, 31 new species have been described, adding 9 to the flora of Mesoamerica (Burger & van der Werff, 1990; Gómez-Laurito & Cascante, 1999; Gómez-Laurito & Estrada, 2002; Hammel, 1986; van der Werff, 1988, 2009). The impulse given to field work with the onset of the Flora Mesoamericana project resulted in a significant increment of herbarium specimens during the last 2 decades of the past century, but Kurz did not see most of them; those specimens have been frequently the source of new species described afterwards in Licaria. Furthermore, the expanded collections have improved our knowledge about variation of morphology within species and consequently have led to better circumscriptions of them. On the other hand, it is important to say that Kurz missed part of the diversity of Licaria because he relied mainly on what the big museums of Europe and the USA have, but did not search in several of the smaller regional herbaria; some of which preserve important specimens that support the recognition of several species that have elsewhere been synonymized or validate larger geographic distributions of taxa.

Contrary to what is found in most American genera of the Lauracae, Licaria presents a rather wide variation in flower morphology, e.g., in orientation of tepals, extent of stamens fusion, presence and extent of fusion of glands, presence of staminodes, and shape and position of anther openings. These features, together with the presence and type of hairiness on flower parts, as well as position and structure of inflorescence, constitute the basis for the recognition of species in the genus (Kostermans, 1937; Kurz, 2000; Mez, 1889). In the course of the revision of Licaria for the Flora Mesoamericana project, a number of herbarium specimens with distinctive character combinations were found, which had not been recorded previously in the genus. Differences are mainly in flower morphology, but complementary vegetative features or other data emphasize their singularity. In several cases, there are no additional specimens, but the collection on which the description is based. This situation has not been considered a drawback since, as is discussed in every case, the peculiarity of the plants is so patent that there is little chance to think they represent part of the variability of any other known species. The case strengthens the idea that we have as yet an incomplete picture of the extent of diversity and distribution in many taxa. Field work is still important and necessary.

Materials and methods

Specimens identified as Licaria (as well as unidentified, putative lauraceous material) collected in the Mesoamerican area from different herbaria (A, CAS, DS, ENCB, F, GH, HEM, K, MEXU, MICH, MO, NY, P, TEX, US, XAL) were carefully analyzed, both for vegetative and reproductive morphology. Particular attention was paid to floral characters; flowers were dissected using a Zeiss, Stemi DV4 stereomicroscope. Information of vegetative characters was collected directly from dry specimens, while floral morphology was surveyed in rehydrated material. Groups of specimens sharing similar morphology were matched with keys and descriptions of currently accepted species, in order to apply the correct names to them. To prevent misinterpretations, all available type specimens (either from herbaria cited above or accesible on Global Plants database (http://plants.jstor.org/search?plantNam) were also considered during the process of identification. Specimens that did not fit any of the known species were evaluated to determine their singularity; those whose floral and vegetative features combined do not overlap with that of accepted taxa are here proposed as new species. Following the methodology mentioned above, description of vegetative characters is based on dry specimens, while floral characters are described as they look in rehydrated material. In order to apply a standardized nomenclature to characters, applicable information in Radford et al. (1974) was used; particularly, base and apex of leaves, pubescence, tridimensional form of flowers, and shape of tepals were described according to that text.

Descriptions

Licaria breedlovei Lorea-Hern. sp. nov. (Figs. 1, 3)

Diagnosis. Trees similar to L. alata Miranda, but different because of the convex flanks of the base of the leaves, sparsely sericeous lower leaf surface, obloid flowers, densely tomentose tepals abaxially, partially pubescent staminal filaments abaxially and adaxially, densely tomentose hypanthium outside, densely hirsute-tomentose inside, and sparsely puberulent style.

Trees up to 15 m tall; twigs sericeous, soon glabrate, brownish gray or dark brown, lenticellate, conspicuously ridged, the ridges narrow, wing-like (at least when dry), each ridge originates at one extreme of petiole insertion, acropetal. Buds densely sericeous-tomentose. Leaves alternate, petioles 9-10.5(-12) mm long, bi-marginate above, glabrous, round below, sericeous, glabrescent, blades (17.5-)23-28 × (3.5-)4.5-7 cm, narrowly elliptic, pinninerved, secondary veins 11-13 pairs, upper leaf surface glabrous, lower surface sparsely sericeous, glabrescent, leaf apex acuminate, leaf base obtuse, somewhat conduplicate, the basal flanks of the blade convex and projected above the midvein. Inflorescences (7.5-)10-16.5 cm long, axillary to tiny, deciduous bracts, on the proximal section of new twigs, paniculate, sericeous-tomentose, peduncle (2.5-)4-6.5 cm long, sometimes glabrescent, pedicels 0.5-1.2(-2.5) mm long, densely tomentose, hairs yellowish-gray to yellowish-brown. Flowers obloid, tepals conspicuously inflexed, outer tepals 0.8-1 × 1.7-2 mm, very widely ovate, densely tomentose abaxially, slightly papillose toward the apex, glabrous or sometimes with scattered sericeous hairs at the base adaxially, inner tepals 0.6 × 1-1.1 mm, ovate or elliptic, tomentose abaxially, glabrous adaxially, staminodes of whorls I and II absent, stamens of whorl III 1-1.1 mm long, fused throughout, filaments pubescent at the base abaxially, glabrous adaxially or pubescent on the upper section, anthers 0.2-0.3 mm long, glabrous, with apical openings, glands ca. 0.2 mm, free, compressed, glabrous, sometimes reduced or absent, hypanthium ca. 0.8 mm deep, densely tomentose outside, hirsute-tomentose inside, pistil 1.3-1.4 mm long, ovary 0.8-1 mm long, glabrous, style sparsely puberulent. Fruits unknown.

Taxonomic summary

Type. Mexico. Chiapas: municipality of Petalcingo (actually municipality of Tila), steep slope of Ahk’ulbal Nab above Petalcingo, 1,700 m, 28 March 1981, D. E. Breedlove 50394 (holotype CAS; isotype MO 6485834).

Etymology. This species is dedicated to Dr. Dennis E. Breedlove, who spent so much effort in field work documenting the flora of Chiapas, pursuing the aim of elaborating a plant species compendium for that region of Mexico.

Distribution and habitat. So far the species is known only from the type collection, in an area covered by montane rain forest which, according to Breedlove (data from label of type specimen), had a canopy layer reaching 25 – 35 m, and species of the genera Alfaroa, Brunellia, Calatola, Hedyosmum, Matudea, Meliosma, Nectandra, Oreopanax, Quercus, and Turpinia, among others. 

Phenology. Regarding the date when the plant was collected, it must have flowers around the end of winter and early days of spring; fruit season is not known, but possibly occurs during winter, for it has been observed that maturation of fruits in most Lauraceae takes around a year after flowering. It seems that the species is not deciduous.

Conservation status. Given the deep environmental degradation that currently prevails in the region where the species is only known, it is suspected that it is critically endangered.

Remarks

The presence of erect, concave tepals, and stamens with extrorse sporangia places L. breedlovei in subgenus Licaria. It is one element in the group (here called Licaria excelsa species group) constituted by L. alata, L. excelsa Kosterm., L. minutiflora (here described), L. pergamentacea W. C. Burger, L. sarukhanii (here described), and L. tomentulosa (here described), as it shares with them morphological features like ridged twigs, large narrow-elliptic leaves (frequently reaching 28-30 cm long), and anthers with sporangia opening apically. Within the group, L. breedlovei is distinguished from the other species by the combination of somewhat conduplicate leaf-base, lower leaf surface persistently sericeous, stamens fused throughout, and sparsely pubescent style. In addition, it differs particularly from L. alata for the obloid flowers (vs. ellipsoid), tepals densely tomentose abaxially (vs. tepals glabrous abaxially), filaments pubescent abaxially and adaxially (vs. filaments glabrous), and hypanthium densely tomentose outside and inside (vs. hypanthium glabrous on both faces).

Licaria dolichopoda Lorea-Hern. sp. nov. (Figs. 2, 3)

Diagnosis. Trees, similar to L. misantlae (Brandegee) Kosterm., glabrous throughout, leaves mostly caudate, inflorescences botryoid, flowers long-pedicellate, without staminodes, and fruit cupule thick, deeply crateriform, its outer rim slightly lobed.

Trees up to 25 m; twigs glabrous, smooth or slightly ribbed, reddish-brown or grayish-brown, sparsely lenticellate. Buds glabrous. Leaves alternate, petioles (3.5-)6.5-9(-11) mm long, slightly sulcate above, rounded and smooth or slightly ribbed below, glabrous, blades (4.5-)7-11(-13) × (1.5-)2.5-4(-5) cm, elliptic or narrowly elliptic, pinninerved, secondary veins 6-11 pairs, both upper and lower leaf surfaces glabrous, leaf apex caudate, sometimes acuminate, base cuneate to obtuse. Inflorescences 2.5-5 cm long, axillary to tiny, decidous bracts, disposed on very short shoots axillary to leaves, botryoid, or apparently paniculate, due to suppression of terminal bud of the floriferous branchlet, glabrous throughout, peduncle 0.2-1.7 cm long, pedicels (6-)10-13(-16) mm long, glabrous. Flowers widely obovoid to turbinate, greenish-yellow, tepals concave, conspicuously inflexed, outer tepals 0.9-1.3 × 1.1-1.7 mm, widely ovate, blunt cuspidate, glabrous abaxially and adaxially, short-ciliate, inner tepals 0.75-1.1 × 1.1-1.2 mm, ovate to widely ovate, glabrous abaxially and adaxially, short-ciliate, staminodes of whorls I and II absent, stamens of whorl III 0.6-1 mm long, fused throughout, filaments glabrous abaxially and adaxially, sometimes with a few hairs at the base abaxially, anthers ca. 0.1 mm, glabrous, with apical openings, glands ca. 0.4 mm, free, oblong, sometimes almost square, obtuse or sub-acute, glabrous, hypanthium 0.6-0.9 mm deep, glabrous outside and inside, pistil ca. 1.5 mm long, glabrous throughout, ovary 0.7-0.9 mm long. Fruits ca. 27 × 21 mm, ovoid or ellipsoid, cupule ca. 15 × 20 mm, crateriform, clearly bimarginate, inner margin ca. 2 mm tall, erect, outer margin ca. 3.5 mm tall, oblique to slightly reflexed, shallowly lobed, thick, pedicel ca. 5.5 × 4.5 (at the base) and 7 (at the apex) mm, obconic, continuous with the cupule.

Taxonomic summary

Type. Costa Rica. Puntarenas: Reserva Forestal Golfo Dulce, Osa Peninsula, Rancho Quemado, 8°44’ N, 83°36’ W, 200-300 m, 2 May 1988, B. Hammel et al. 16790 (holotype MO; isotypes MEXU, TEX).

Paratypes. Costa Rica. Guanacaste: Cantón de Tilarán, San Gerardo Abajo, río Caño Negro, Fincas Quesada y Arce, 10°18’40’’ N, 84°50’02’’ W, 1,100-1,200 m, 5 December 1991, E. Bello & E. Cruz 4262 (XAL). Puntarenas: Cantón de Osa, Rincón, filas al margen izquierdo de Quebrada Vaquedano, 8°38’45’’ N, 83°35’25’’ W, 400 m, 21 July 1990, G. Herrera 4000 (XAL); Cantón de Osa, Aguabuena, cuenca media y superior de Quebrada Orito, Rincón, 8°42’40’’ N, 83°31’40’’ W, 400 m, 25 October 1990, G. Herrera 4510 (MEXU); Cantón de Osa, Rancho Quemado, sector oeste, Sierpe, 8°41’00’’ N, 83°35’40’’ W, 350 m, 25 August 1982, J. Marín & G. Marín 499 (MO, XAL).

Etymology. The name of this species alludes to the distinctive long pedicels that bear the flowers.

Distribution and habitat. Currently the species is known from 2 rather distant areas in Costa Rica that differ in ecological conditions. One of them, in the province of Guanacaste, is located in the Pacific foothills of the southern end of the Sierra de Guanacaste, while the other, in the province of Puntarenas, is in the lowlands of the Peninsula de Osa toward the southeastern extreme of the country. The first one is covered by pre-montane humid forest, and the second by humid tropical forest. 

Phenology. Flowering is apparently distributed in 2 peaks: May-July and October-December. Fruits are only known from October.

Conservation status. There is no information about the abundance of the species in the places where it has been collected, neither about the ecological conditions of the vegetation there. However, the distribution range in the southeast is embedded in the Reserva Forestal Golfo Dulce, by the boundaries with the Parque Nacional Corcovado. Thus, there might not be problems with the persistence of the species in that region. The other point of the species distribution is, according to satellite images, within a region with deeply transformed vegetation, although not too far from the Parque Nacional Volcán Arenal, which could hold the species in its flora.

Remarks

Because of the erect, concave tepals, and extrorse sporangia of stamens in the flowers, L. dolichopoda must be also considered in the subgenus Licaria. The glabrous condition found in every structure of the plant body (stem, leaves, and flowers), as well as the apical openings of stamens, and the lack of staminodes found in this species places it beside L. eurypaniculata (here described), from which it differs in the botryoid architecture of the inflorescence, and the conspicuous caudate leaves. Collection duplicates of L. dolichopoda have been previously distributed as L. cufodontisii Kosterm. (Herrera 4000), and as L. misantlae (Herrera 4510).

Licaria eurypaniculata Lorea-Hern. sp. nov. (Figs. 4, 6)

Diagnosis. Among the species with glabrous leaves, inflexed tepals, lacking staminodes, as well as apical anther openings, this species is distinguished by paniculate inflorescences where the flowers are not aggregate on the floriferous axes, orbicular flowers, tepal surface glabrous abaxially and adaxially, fused stamens throughout, glabrous hypanthium outside and inside, and glabrous pistil.

Trees 6-7 m tall; twigs glabrous, smooth or slightly ribbed, reddish-brown, sparsely lenticellate. Buds glabrous. Leaves alternate, petioles (5.5-)7-9(-10.5) mm long, slightly sulcate above, glabrous, blades (7-)11-16(-19.5) × (2-)3-4.5(-6) cm, narrowly elliptic to lanceolate or elliptic, pinninerved, secondary veins 7-9 pairs, both upper and lower leaf surfaces glabrous, leaf apex acuminate to short caudate, base obtuse to cuneate. Inflorescences 10-11 cm long, apparently terminal, if it is axillary to a bract, this one is inconspicuous, paniculate, basal axes longer than the peduncle, glabrous throughout or sparsely puberulent toward the end of the secondary axes, flowers spaced, not aggregate on the axes, peduncle ca. 3 cm long, pedicels 2-3.2 mm long, glabrous or sparsely puberulent. Flowers spheroidal, greenish, tepals conspicuously inflexed, outer tepals ca. 0.5 × 0.9-1.0 mm, widely ovate to depressed ovate, glabrous abaxially and adaxially, inner tepals ca. 0.4 × 0.6-0.7 mm, ovate or almost orbicular, glabrous abaxially and adaxially, staminodes of whorls I and II absent, stamens of whorl III 0.5-0.6 mm long, fused throughout, filaments glabrous outside, sparsely tomentose inside, anthers ca. 0.1 mm, glabrous, with apical openings, glands ca. 0.1 mm, free, widely elliptic or orbicular, glabrous, hypanthium ca. 0.7 mm deep, glabrous outside, glabrous or sparsely pubescent on the distal section inside, pistil ca. 1.1-1.2 mm long, glabrous throughout, ovary ca. 0.6-0.7 mm long. Fruits (not wholly ripe) 15-17 × 12-12.5 mm, ovoid or ellipsoid, cupule 10-11 × 14-15 mm, crateriform, clearly bimarginate, inner margin 1.1-1.3 mm tall, erect, outer margin 0.5-0.7 mm tall, perpendicular to the inner one, pedicel 3-3.6 × 2-2.2 (at the base) and 3.6-4 (at the apex) mm, obconic.

Taxonomic summary

Type. Panama. Bocas del Toro: along road to Chiriquí Grande, c. 10 road miles from continental divide and about 2 miles along road east of highway, 8°45’ N, 82°15’ W, 300 m, 15 April 1987, G. McPherson 10830 (holotype MO; isotype XAL 124596).

Paratype. Panama. Bocas del Toro: along road to Chiriquí Grande, 10 road-miles from continental divide, ca. 2 road-miles along road east of highway, 8°55’04’’ N, 82°10’04’’ W, 300 m, 9 February 1987, G. McPherson 10453 (MO 5048286).

Etymology. The name of this species alludes to the very long basal secondary axes of the inflorescence, which give a broad triangular profile to the panicle.

Distribution and habitat. The only 2 known collections of the species come from the same area in the Atlantic lowlands of western Panama. No information about the vegetation found at the site was recorded, but considering the geographical factors of the place, it is expected to be tropical rain forest. 

Phenology. Flowers in spring, and fruits mature in winter or early spring. The plant is not deciduous.

Conservation status. It seems that the species is not frequent in the area where it was found, for it has been collected only twice. On the other hand, the view of the area from satellite images shows that most of the original vegetation has been cleared; therefore, the species might be endangered.

Remarks

There are no species that come close morphologically to L. eurypaniculata. The other species with a general glabrous condition almost throughout the plant body, L. dolichopoda, is very different, in the shape of the leaves and the structure of the inflorescence. Given the erect, concave tepals, and stamens with extrorse sporangia that L. eurypaniculata presents, it is also a member of the subgenus Licaria. 

Licaria gibbitepala Lorea-Hern. sp. nov. (Figs. 5, 6)

Diagnosis. Trees similar to L. excelsa, but distinguished by the obovate to oblanceolate leaves, densely yellowish to orange-brown puberulent inflorescences, tepals with basal half conspicuously swollen, puberulent abaxial surface, sericeous adaxial surface at the base, apically pubescent ovary, and pubescent style.

Trees 15-20 m tall, trunk ca. 25 cm DBH, bark smooth, fragrant; twigs hollow, inhabited by ants, glabrous, sparsely lenticellate, slightly ridged, each ridge originating at one extreme of petiole insertion, acropetal. Buds glabrous or partially pubescent. Leaves alternate, petioles 10-12(-14) mm long, bimarginate above, glabrous, blades (20-)24-30 × (9-)11-13 cm, obovate or oblanceolate, sometimes elliptic, pinninerved, secondary veins (12)14-16 pairs, leaf surface glabrous above and below, leaf apex apiculate, sometimes apiculate-acuminate, leaf base obtuse or rounded. Inflorescences 9-15 cm, seemingly terminal, but actually axillary to tiny, deciduous bracts, on the proximal section of new twigs, paniculate, conspicuously puberulent along all axes, hairs yellowish to orange-brown, peduncle (1-)3.5-4.5 cm, sparsely puberulent, glabrescent, pedicels 2.5-5.5(-7) mm, densely puberulent. Flowers widely obovoid, yellowish-green, fragrant, perianth thick, coriaceous, tepals clearly inflexed, their base conspicuously swollen, outer tepals 1.2-1.4 × 1.6-1.9 mm, widely ovate, puberulent abaxially, sericeous-tomentose at the base and toward the margins adaxially, hairs orange-brown, inner tepals 0.8-1 × 1-1.2 mm, ovate, puberulent abaxially, sericeous-tomentose at the base and tomentose at the middle adaxially, staminodes of whorls I and II absent, stamens of whorl III 0.7-0.8 mm long, fused along their filaments, filaments tomentose at the base outside, tomentose throughout inside, hairs orange-brown, anthers ca. 0.2 mm, free or fused just at the base, glabrous, with apical openings, glands ca. 0.3 mm, only 3 given the fusion of adjoining glands, widely oblong, glabrous, hypanthium 1-1.2 mm deep, obconic, densely puberulent outside, hairs yellowish to orange-brown, sericeous-tomentose inside, hairs reddish-brown, pistil 1.6-1.8 mm long, top of the ovary and style pubescent, ovary 0.8-1.2 mm long. Fruits (nearly ripe) 19-23 × 15.5-16.5 mm, ellipsoid, cupule ca. 16.5 × 18.5 mm, cotyliform, sparsely lenticellate, seemingly tri-margined, the 2 regular margins plus the swollen projections of the tepals, inner margin ca. 1.6 mm tall, erect, outer margin 2.2-2.5 mm tall, erect, pedicel 4.5-7 mm long, continuous with the base of the cupule, 3.5 mm diam. at the base.

Taxonomic summary

Type. Costa Rica. Limón: Reserva Biológica Hitoy Cerere, 300 m aguas abajo de la confluencia del río Hitoy con el río Cerere, margen izquierda por la fila que lleva al cerro Bobócora, 9°39’00’’ N, 83°02’45’’ W, 200 m, 20 February 1989, G. Herrera & A. Chacón 2427 (holotype MO, isotype XAL 124445).

Etymology. The name is derived from the conspicuous swollen condition of the base of the tepals; the feature is distinctive. 

Distribution and habitat. So far, this species is known only from the southwestern end of Costa Rica. Although no information about the habitat was recorded, there is no doubt that the place lies within the tropical rain forest territory.

Phenology. With flowers and ripe fruits around the end of winter. The species has perennial leaves.

Conservation status. There is no information about the abundance or extent of distribution of the species, but as it is known to grow in the grounds of a nature reserve, it can be expected that it is not under high risk of extinction but certainly endangered.

Remarks

Licaria gibbitepala seems to be closely related to L. tomentulosa and, at the same time, to the group of species around L. excelsa. All of them have ridged twigs, large leaves, flowers with erect, concave tepals, no staminodes, and sporangia with apical openings. The hollow twigs, along with the obovate to oblanceolate leaves, and the conspicuous gibbous base of the tepals distinguish L. gibbitepala.

Licaria gracilis Lorea-Hern. sp. nov. (Figs. 7, 9)

Diagnosis. Small trees with glabrous leaves, botryoid, few-flowered inflorescences, glabrous, erect tepals, lacking staminodes, free stamens, anther openings elliptic, lateral, strongly oblique, glands present, glabrous hypanthium outside and inside, glabrous pistil.

Trees to 6 m tall; twigs smooth, dark brown to reddish brown, pruinose, puberulent, glabrescent, sparsely lenticellate. Buds glabrous. Leaves alternate, petioles (4-)8-11 mm long, puberulent, soon glabrous, canaliculate above, blades 8.5-13 × 3.5-5.5 cm, elliptic or narrowly elliptic, pinninerved, secondary veins 5-7 pairs, leaf surface glabrous above and below, but the lower surface puberulent in the beginning, leaf apex caudate, sometimes just acuminate, base obtuse to cuneate. Inflorescences 2.5-3.5 cm long, axillary to leaves and to tiny, deciduous bracts, on the proximal section of new twigs, botryoid, racemiform, few-flowered (less than 10 flowers), glabrous throughout or with some hairs toward the end of the peduncle, peduncle 1.8-2 cm long, pedicels 3-4.5 mm long, glabrous. Flowers obovoid, pale yellow, tepals erect to slightly inflexed, concave, outer tepals ca. 0.8 × 1.3 mm, very widely ovate to depressed ovate, glabrous abaxially, with some long, appressed hairs ascending from the base adaxially, inner tepals ca. 0.5 × 0.8 mm, ovate or widely ovate, glabrous abaxially, adaxially like the outer tepals, staminodes of whorls I and II absent, stamens of whorl III ca. 0.7 mm long, free, but very close one to each other, widely ovate in outline, filaments sparsely tomentulose outside and inside, anthers ca. 0.4 mm, tomentulose at the base outside, tomentulose inside along the central line, openings lateral, oblique, glands ca. 0.4 mm, rounded, glabrous, hypanthium ca. 0.7 mm deep, obconic, glabrous inside and outside, pistil ca. 1.7 mm long, glabrous, ovary ca. 0.8 mm long. Fruit unknown.

Taxonomic summary

Type. Panama. Chiriquí: Punta Burica, El Chorogo, alrededores de la finca de Fernando Chavarría, adyacente al límite fronterizo, cabecera del río San Bartolo, 8°17’07’’ N, 82°58’56’’ W, 395 m, 15 May 2007, J. E. Aranda et al. 3912 (holotype MO 6456198).

Etymology. The name of the species is derived from the attractive view that the slender inflorescences give to the plant.

Distribution and habitat. The species is known only from the location where it was first and last collected. No information about the habitat is mentioned in the data-label of the specimen, except that was collected nearby a ranch. The original vegetation must have been tropical evergreen forest or semi-evergreen forest.

Phenology. Flowers during spring; ripe fruits expected during winter or early spring, since maturation of fruits in most Lauraceae takes around a year after flowering.

Conservation status. The species might be (critically) endangered, for most of the land in the area where it was collected has been transformed for diverse agricultural purposes.

Remarks

The few-flowered, botryoid inflorescence, tiny flowers, and very oblique, lateral openings of the sporangia distinguish this species straightaway. There is no species whose general morphology indicates association with L. gracilis. The singular way that the openings of the stamens are displayed resemble that found in Licaria cogolloi van der Werff, and L. caribaea Gómez-Lau. & Cascante, but besides this, there is no other feature that might suggest a relationship to those species. For the features of its flowers, Licaria gracilis belongs to subgenus Licaria.

Licaria minutiflora Lorea-Hern. sp. nov. (Figs. 8, 9)

Diagnosis. Trees similar to L. pergamentacea, but distinct by the presence of hollow twigs, glabrous buds, abaxially densely tomentulose tepals, internally pubescent hypanthium, apically pubescent ovary, and pubescent style.

Trees up to 20 m tall, trunk ca. 30 cm DBH; twigs hollow, inhabited by ants, glabrous, smooth or slightly ridged, each ridge originates at one extreme of petiole insertion, acropetal, sparsely lenticellate. Buds glabrous. Leaves alternate, petioles (7-)15-20(-30) mm, glabrous, bimarginate above, blades (11-)20-28(-34.5) × (3-)5-9(-13) cm, narrowly elliptic or narrowly ovate, pinninerved, secondary veins 9-12 pairs, leaf surface glabrous on both sides, leaf apex acute, slightly apiculate, base acute or obtuse. Inflorescences (6-)9-12(-15) cm long, axillary to tiny, deciduous bracts, on the proximal section of new twigs or axillary to leaves, paniculate, tomentulose, peduncle (0.5-)1.5-3(-4) cm long, pedicels (1.2-)2.5-4(-6) mm long, densely tomentulose. Flowers obovoid or ellipsoid, yellowish-green, tepals inflexed, outer tepals 0.5-0.8 × 0.8-1 mm, widely ovate, densely tomentulose abaxially, tepal surface concealed or almost so by hairs, glabrous adaxially, inner tepals 0.5-0.7 × 0.5-0.6 mm, ovate, densely tomentulose abaxially, glabrous adaxially, staminodes of whorls I and II absent, stamens of whorl III 0.5-0.6 mm long, free or barely united by filament base, filaments tomentose at base outside, glabrous or sparsely pubescent along the medial line inside, anthers ca. 0.2 mm, glabrous, openings apical, glands ca. 0.2 mm, free, rounded, hypanthium 0.6-0.8 mm deep, obconic, densely tomentulose outside, sericeous on upper half inside, hairs yellowish or reddish, pistil ca. 1.4 mm long, top of the ovary and style pubescent, ovary 0.8-1 mm long. Fruits ca. 19.5 × 15-16.5 mm, ellipsoid, cupule 15-16 × 18-20 mm, urceolate, lenticellate, conspicuously bimarginate, inner margin 1.2-1.5 mm tall, outer margin 1-1.2 mm, extended, pedicel 6.5-9 mm long, continuous with the cupule, 2.8-3.6 mm diameter at base.

Taxonomic summary

Type. Costa Rica. Alajuela: camino entre la estación de la Reserva Forestal de San Ramón y el camino a la colonia Palmareña, finca de don Bolívar Ruiz, margen derecha río San Lorencito, 10°12’53’’ N, 84°36’28’’ W, February 1987, G. Herrera 500 (holotype MO 3587621; isotypes MEXU 638804, TEX).

Paratypes. Costa Rica. Alajuela: Reserva Biológica Monteverde, Poco Sol, La Cutacha de San Bosco, 10°22’ N, 84°40’ W, 900 m, 1 April 1989, E. Bello 784 (MEXU 1304162; MO 6142952; XAL 124442); Bosque Eterno de los Niños, Reserva de Arenal, río Peñas Blancas, Quebrada Agua Gata, Finca Villalobos, 10°23’ N, 84°42’ W, 1,000 m, 20 April 1990, E. Bello 2208 (MO 6130824; XAL 124446); Cantón de Upala, Colonia La Libertad, 10°52’ N, 85°17’ W, 300 m, 3 August 1991, Q. Jiménez & G. Rivera 1011 (MO 6117397; XAL 124597). Guanacaste: Parque Nacional Guanacaste, Estación Pitilla, 10°00’15’’ N, 85°25.2’ W, 500 m, 27 May 1989, G. Herrera et al. 2942 (MO; XAL 124428).

Etymology. The very small flowers, whose tepals are less than 1 mm long, is the feature on which the species name is based.

Distribution and habitat. This species is known from the northern hills of the Cordillera de Guanacaste (Guanacaste Mountain Range) and the western part of the Cordillera Central (Central Mountain Range), between 200 and1,000 m asl. Prevailing vegetation in the region is tropical evergreen forest and montane rain forest. The species has been collected also in pasture fields. There is a fruiting specimen from the Osa Peninsula (Hammel et al. 16984) that seems to belong to L. minutiflora but until confirmed with a flowering specimen, the presence of the species in this part of the country remains uncertain.

Phenology. Flowers toward the end of winter and early spring; fruits must be ripe around the end of autumn or early winter.

Conservation status. Most specimens of this species have been collected within nature reserves. Therefore, it is considered not threatened, even though its abundance is still unknown.

Remarks

As has been mentioned elsewhere in this paper, Licaria minutiflora is part of the L. excelsa species group. Its general appearance resembles that of L. pergamentacea, for the size and shape of the leaves, structure and hairiness of the inflorescence, and for having small oblong-ellipsoid, not coriaceous flowers. However, besides the presence of hollow twigs, it differs by having flowers with the upper part of the hypanthium homogeneously pubescent inside, and a pubescent pistil.

Licaria ochracea Lorea-Hern. sp. nov. (Figs. 10, 12)

Diagnosis. Trees similar to L. multinervis H. W. Kurz, but differing by lower surface indument of leaves composed by 2 types of hairs, the most numerous tomentulose, the fewer sericeous, long inflorescences, terminal or axillary to leaves, with rachis up to 15 cm, fully exserted anthers, clearly stalked glands, conspicuous hypanthium tube projected beyond the insertion point of stamens. 

Trees up to 22 m tall, twigs smooth, densely tomentose, hairs initially yellowish-brown, then greysh, sparsely and inconspicuously lenticellate. Buds tomentose. Leaves alternate, petioles (10-)15-20 mm long, tomentose, glabrescent, channeled above, blades 12.5-18.5 × (2.5)3.5-4.5 cm, narrowly elliptic, sometimes narrowly oblanceolate, pinninerved, secondary veins (9)10-13 pairs, leaf surface glabrous above, tomentose below, most hairs sinuous, rather appressed, or patent, fewer hairs straight, appressed, leaf apex acuminate, base narrowly cuneate. Inflorescences (7-)10-18 cm long, axillary to leaves, less frequently terminal, paniculate, densely tomentose, hairs like on twigs, flowers agglomerate at the end of terminal axes, peduncle 0.2-1.5(-3.5) cm long, pedicels (1-)1.5-2 mm long, tomentose. Flowers narrowly oblong, tepals erect, concave, outer tepals, 1-1.3(-1.5) × (1-)1.1-1.3 mm, widely ovate, tomentose abaxially, glabrous adaxially, except for a few long, appressed hairs, coming from the base, inner tepals 1-1.1(-1.4) × 0.8-0.9 mm, ovate, with a pattern of pubescence similar to that of outer tepals, staminodes of whorls I and II absent, stamens of whorl III 3-3.3(-3.8) mm long, coherent along their filaments or even at the base of the anthers, easily separable, filaments tomentose on both faces, anthers 0.9-1.1 mm long, free or coherent at the base, glabrous, completely exserted, openings dorsolateral, glands 0.7-0.8 mm, free, oblanceolate, glabrous, clearly stalked, stalk pubescent, hypanthium 1.2-1.3(-1.6) mm deep, extended 0.3 mm beyond the insertion point of stamens, tomentose outside, densely hirsute-tomentose inside, hairs golden-brown, pistil 3.6-3.9 mm long, sparsely pubescent, at least some hairs on the upper half of the ovary and lower half of the style, ovary 0.9-1.1 mm long. Fruits unknown.

Taxonomic summary

Type. Nicaragua. Matagalpa (according to current maps it should be Jinotega): pasture and small woods, tropical premontane forest, Hacienda Santa María del Ostuma, 10 km N of Matagalpa, 1,300 m, 17 July 1978, P. C. Vincelli 756 (holotype MO 2984723; isotypes LL, MEXU 691292).

Etymology. The name refers to the conspicuous orange-brown pubescence of the species on young twigs and main axes of inflorescences.

Distribution and habitat. Only known from the place of type collection, where the Cordillera Isabelia and Cordillera Dariense meet.

Phenology. Flowers in summer; fruit season is not known, but since it has been observed that maturation of fruits in most Lauraceae takes around a year after flowering, possibly ripe fruits are present during spring or early summer.

Conservation status. There is no certainty on the conditions that might be affecting the survival of the species. The type was collected in a private property that used to be preserved for ecotourism activities, but its current situation is unknown. However, since the species has not been collected again, it is suspected to be endangered.

Remarks

The collection on which the description of this species is based was initially identified by Kurz (2000) as L. multinervis; actually it is cited as a paratype of this species. But the impression of being conspecific with this taxon disappears with a detailed survey of the morphology. Important differences are the pubescence on the lower surface of the leaves (simple in L. multinervis vs. made of 2 types of hairs in L. ochracea), position of the inflorescences (axillary to small bracts in the proximal section of new branches in L. multinervis vs. axillary to leaves or terminal in L. ochracea), length of inflorescences (up to 3.5 cm long in L. multinervis vs. 5-7 times longer in L. ochracea), protrusion of anthers (partially exserted in L. multinervis vs. fully exerted in L. ochracea), and projection of hypanthium tube beyond the insertion point of stamens (short in L. multinervis vs. conspicuous in L. ochracea). However, L. multinervis and L. ochracea seem to be more closely related to each other than to the rest of species in the area that present fully exserted stamens, namely L. agglomerata van der Werff, L. capitata (Schltdl. et Cham.) Kosterm., L. nitida van der Werff, and L. vanderwerffii (here described).

Licaria rufotricha Lorea-Hern. sp. nov. (Figs. 11, 12)

Diagnosis. Small trees, distinct for the conspicuously obovoid flowers, aggregate toward the end of the secondary floriferous axes, with inflexed tepals, glabrous abaxially, reddish-brown hirsute-sericeous adaxially, lacking staminodes, stamens fused throughout, reddish-brown hirsute, anther openings apical, hypanthium mostly glabrous outside, reddish-brown hirsute inside, and ovary distally pubescent. 

Trees to 12 m tall; twigs smooth or inconspicuously ridged, each ridge originating at one extreme of petiole insertion, acropetal, lenticellate, grayish, densely puberulent, glabrescent. Buds glabrous. Leaves alternate, petioles 10-13 (-17) mm long, slightly channeled above, puberulent, blades (14.5-)16.5-20(-23) × 4-5.5(-9) cm, elliptic or narrowly elliptic, pinninerved, secondary veins 6-7 pairs, leaf surface densely puberulent above when young, glabrescent, rather persistently puberulent below, leaf apex acuminate, base cuneate, sometimes obtuse or narrowly cuneate to indistinctly attenuate. Inflorescences (3-)5-8(-10.5) cm, axillary to tiny, deciduous bracts, on the proximal section of new twigs, or axillary to new leaves, paniculate, flowers aggregate at the end of secondary axes, densely puberulent on peduncle and rachis, glabrate toward the ultimate axes, peduncle (2-)3.5-5.5(-7.5) cm long, pedicels 2-3.5(-4.5) mm long, glabrous or sparsely puberulent. Flowers obovoid or obconic, pale yellow, tepals conspicuously inflexed, outer tepals 1-1.2 × 2-2.4 mm, widely ovate, glabrous abaxially, hirsute-sericeous adaxially, hairs reddish-brown, inner tepals 0.8-1 × 0.8-0.9 mm, ovate or elliptic, glabrous abaxially, generally mostly hirsute adaxially, hairs reddish-brown, surpassing the apical margin of the tepals, making them appear fimbriate, staminodes of whorls I and II absent, stamens of whorl III, 0.6-0.7 mm long, fused throughout, filaments hirsute on both faces, hairs reddish-brown, anthers ca. 0.2 mm, pubescent, except around the margin of the openings, hairs like those of the filaments, glands ca. 0.4 mm, free, rounded or oblate, glabrous, hypanthium 0.8-0.9 mm deep, glabrous or sparsely puberulent outside, hirsute inside, hairs like those of the filaments, pistil 1.7-2 mm long, ovary ca. 0.8 mm long, sparsely pubescent distally, hairs whitish. Fruits unknown.

Taxonomic summary

Type. Panama. Panama: 5-10 km NE of Altos de Pacora, on trail at end of road, ca. 750 m, 7 March 1975, S. Mori & J. Kallunki 4977 (holotype MO 2992664).

Etymology. The name given to this species refers to the dense red-brown pubescence in the interior of the flowers, covering the adaxial surface of tepals, stamen filaments, anthers, and hypanthium inside.

Distribution and habitat. Just known from the place where the type was collected (around 25-30 km NE of Panama City), with tropical evergreen forest or semi-evergreen forest as original vegetation.

Phenology. Flowers around the end of winter or early spring; ripe fruits expected during winter, since maturation of fruits in most Lauraceae takes around a year after flowering.

Conservation status. Probably the species is endangered. Most of the vegetation in the surroundings of the place where the species was collected has been cut down for cattle raising or agricultural purposes. But the southern boundary of the Parque Nacional Chagres (Chagres National Park) is very close to that place, and the Nature Reserve Cocobolo is a few kilometers ENE of it as well. So, even it has not been collected again, it is hoped the species is still around there.

Remarks

There is no other species in the Mesoamerican area with the distinctive reddish-brown pubescence found in the interior of the Licaria rufotricha flowers. Yellowish to reddish-brown pubescence is present on the filaments of stamens and/or inside the hypanthium of several species, like L. agglomerata, L. excelsa, L. gibbitepala, and L. tomentulosa, but it is never found on the tepals surface. In fact, its general morphology does not suggest a relation to any species in the region. 

Licaria sarukhanii Lorea-Hern. sp. nov. (Figs. 13, 15)

Diagnosis. Trees similar to L. alata, but differing by terminal, subsessile inflorescences, longer pedicels (up to 10.5 mm), flowers widely ellipsoid, abaxial tepal surface tomentose at the base and papillose toward the apex, hypanthium densely tomentose outside, sericeous-tomentose inside, and style pubescent.

Trees to 20 m tall, twigs glabrous, grayish to grayish-brown, slightly ridged, each ridge originating at one extreme of petiole insertion, acropetal, sparsely lenticellate. Buds glabrous or pubescent at the apex of the bud scales. Leaves alternate, petioles (11-)13-17(-20) mm long, slightly bimarginate, glabrous, blades (12.5-)20-32(-37) × (5-)7-10(11.5) cm, narrowly elliptic, occasionally oblanceolate, pinninerved, secondary veins (12)14-18 pairs, leaf surface glabrous on both sides, leaf apex acuminate, sometimes acute, base obtuse or acute. Inflorescences 12-22 cm long, terminal, paniculate, tomentose, soon glabrescent, hairs patent or oblique, grey or yellowish-grey, peduncle 0.2-0.4 cm long, pedicels (3-)5-8(-10.5) mm long, glabrous or sparsely tomentose. Flowers broadly ellipsoid, pale green, tepals inflexed, outer tepals 0.8-0.9 × 1.8-2 mm, very widely ovate, concave, tomentose over the basal half, and papillose-pubescent over the distal half abaxially, glabrous or with few straight hairs at base adaxially, inner tepals 0.7-0.9 × 0.4-0.8 mm, ovate, pubescence pattern abaxially like that of outer tepals, but less papillose, glabrous adaxially, staminodes of whorls I and II absent, stamens of whorl III 0.7-0.9 mm long, fused along their filaments, filaments tomentose along the central line on both faces, anthers 0.2-0.4 mm long, glabrous, openings apical, glands ca. 0.4 mm, oblong, flattened, frequently reduced or absent, glabrous or tomentose on the base abaxially, hypanthium ca. 1 mm deep, densely tomentose outside, hairs sinuous, sericeous-tomentose inside, pistil 1.3-1.6 mm long, ovary 0.8-1.2 mm long, glabrous, style rather densely pubescent. Fruits 27-30 × 17-18 mm, ellipsoid, cupule 15-17.5 × 18-19.5 mm, urceolate, bimarginate, but the margins barely discernible, ca. 0.5 mm, erect, pedicel 4-5 × 3.5-4.5 mm.

Taxonomic summary

Type. Mexico. Chiapas: municipio de Ángel Albino Corzo, Reserva de la Biosfera El Triunfo, aprox. 1.5 km al E de Campamento El Triunfo, sobre el Sendero Bandera, 15°36’ N, 92°50’ W, 1,850 m, 27 April 1993, F. Lorea 5522 (holotype XAL 151063; isotypes [to be distributed]).

Paratypes. Mexico. Chiapas: municipio de Ángel Albino Corzo, Polígono I de la Reserva de la Biosfera El Triunfo, 15°39’ N, 92°48’ W, 1,900 m, 21 February 1993, S. Solórzano 67 (MEXU 754117); Reserva El Triunfo, camino a Cerro de la Bandera, 25 March 1986, M. L. Ávila and V. H. Hernández s/n (MEXU 877857, TEX 146383); Reserva de la Biosfera El Triunfo, sendero Palo Gordo, 15°40’10’’ N, 92°48’42’’ W, 1,990 m, 22 March 2006, F. González-García s/n (XAL 113841).

Etymology. The species is dedicated to José Sarukhán, a Mexican plant ecologist who has played an important role in making a huge amount of information about Mexico’s biodiversity, ecosystem conservation, and sustainable development accessible to the public.

Distribution and habitat. So far, the species is known only from the central region of the Sierra Madre de Chiapas, from 1,800 to 2,000 m asl where the montane rain forest is the dominant type of vegetation.

Phenology. Flowers toward the end of winter and early spring; ripe fruits were found in the same interval of time.

Conservation status. All the collections of the species come from the nature reserve El Triunfo, located in the Sierra Madre de Chiapas, which has persisted largely undisturbed for its almost forty years of existence. Thus, considering the size of the area covered with montane rain forest in the reserve, the species might be regarded as vulnerable.

Remarks

Licaria sarukhanii is part of the L. excelsa species group, with a closer relation to L. breedlovei, because they share tomentose inflorescences and flowers rather widely ellipsoid to obloid. They differ by the conduplicate leaf bases, sparsely sericeous lower leaf surface, conspicuously pedunculate inflorescences axillary to small bracts or leaves, fused anthers, and style sparsely pubescent present in L. breedlovei, in contrast to flat leaf base, glabrous lower leaf surface, terminal, sub-sessile inflorescences, free anthers, and conspicuously pubescent style in L. sarukhanii. 

Licaria tomentulosa Lorea-Hern. sp. nov. (Figs. 14, 15)

Diagnosis. Trees similar to L. excelsa, but distinguished by presenting hollow twigs, inflorescences yellowish-brown tomentulose, flowers conspicuously obovoid, tepals densely tomentulose abaxially, and apex of the ovary and style conspicuously pubescent.

Trees up to 25 m tall, and trunk 50 cm DBH, twigs hollow, inhabited by ants, smooth or slightly ridged, glabrous, grayish-brown, sparsely lenticellate. Buds glabrous. Leaves alternate, petioles (14-)17-22(-24) mm long, bimarginate above, glabrous, blades (22-)25-30(-34) × (6-)8-10(-12) cm, narrowly elliptic or elliptic, pinninerved, secondary veins (9)11-13 pairs, leaf surface glabrous on both sides, leaf apex acute or short acuminate, base obtuse, rounded or shortly attenuate, particularly in leaves close to the twig tips. Inflorescences 6.5-9.5(13.5) cm long, axillary to tiny, deciduous bracts, on very short branches axillary to leaves, paniculate, tomentulose, hairs yellowish-brown, peduncle 2.5-4 cm long, pedicels (1-)2-3.5 mm long, densely tomentulose. Flowers obovoid, thick, coriaceous, greenish-yellow, tepals inflexed, concave, outer tepals 0.7-1 × 1.4-1.7 mm, widely ovate, densely tomentulose abaxially, hairs almost concealing the surface, marginal tomentose bands and some long, appressed hairs at the base adaxially, inner tepals 0.6-0.9 × 0.8-0.9 mm, ovate, sometimes slightly conduplicate, densely tomentulose abaxially, pattern of pubescence adaxially like in the outer tepals, staminodes of whorls I and II absent, stamens of whorl III 0.8-1.1 mm long, fused throughout, filaments tomentose outside on lower half, densely tomentose all over the inner face, hairs reddish-brown, anthers ca. 0.2 mm, glabrous outside, densely tomentose inside, openings apical, glands 0.3-0.4 mm, frequently fused between adyacent stamens, transversely oblong, oblong when free, hypanthium 1-1.2 mm deep, densely tomentulose outside, tomentulose inside, sometimes only in the upper half, hairs mainly reddish-brown, pistil 2-2.3 mm long, ovary 1.1-1.4 mm long, apex of the ovary and style conspicuously pubescent. Fruits (not fully ripe) ca. 13 × 13 mm, spheroidal, cupule 13-14 × 17-18 mm, crateriform, lenticellate, bimarginate, inner margin 0.7-1 mm tall, erect, outer margin 0.5-0.7 mm, erect to spreading, pedicel 4-6 × 3-4 (apex) and 2 mm (base).

Taxonomic summary

Type. Costa Rica. Limón: Cordillera de Talamanca, Matina, intersección de río Barbilla y quebrada Cañabral, por la fila al norte, 10°01’ N, 83°24’ W, 100-200 m, 11 October 1988, G. Herrera 2165 (holotype MO 3693485; isotypes MEXU 529888, 529889, 717774, and 718334; TEX).

Paratypes. Costa Rica. Alajuela: Upala, Bijagua, El Pilón, Cerro La Carmela, entre río Celeste y cabeceras del río Chimurria, 10°43’15’’ N, 84°59’45’’ W, 1,000 m, 11 July 1988, G. Herrera 2056 (MEXU 529875, 717781; MO 3693486; US 3655515). Limón: Reserva Biológica Hitoy Cerere, Valle de la Estrella, sendero a Cerro Bobócara, 9°41’00’’ N, 83°04’20’’ W, 798 m, 17 August 1990, G. Herrera 4115 (MEXU 1304090; MO 6142953; XAL 124444); Reserva Indígena Talamanca, camino a Soki entre la Quebrada Amubri, margen izquierda de río Lari, 9°29’40’’ N, 82°89’40’’ W, 200 m, 29 June 1989, A. Chacón 25 (MO; XAL 124437).

Etymology. The name is for the abundant tomentulose pubescence that covers the axes of the inflorescence, as well as the abaxial surface of tepals and hypanthium. 

Distribution and habitat. Known only from Costa Rica, along the Atlantic lowlands adjacent to the Sierra de Talamanca, and the Sierra de Guanacaste. Tropical rain forest used to be the predominant vegetation there, but currently a big amount of land has been changed to agricultural activities or other affairs.

Phenology. Flowers in summer and early autumn; ripe fruits in summer.

Conservation status. Given the deterioration of the habitat, the species might be considered vulnerable or endangered, in spite of its wide range of distribution. 

Remarks

Licaria excelsa and L. tomentulosa are much alike. Considering the available material, distinguishing characters seem to work well to separate both species; hollow twigs, as well as type and distribution of pubescence on vegetative and floral parts, are consistently present in all the specimens considered as L. tomentulosa, making it a clear morphological unit, distinct from L. excelsa.

Licaria vanderwerffii Lorea-Hern. sp. nov. (Figs. 16, 17)

Diagnosis. Similar to L. agglomerata, but different by the free stamens, white pubescence of stamens, hypanthium densely white tomentose inside, and pistil glabrous.

Shrubs or small trees 1-3 m tall, twigs hollow, smooth, sparsely lenticellate, glabrous, reddish-brown. Buds glabrous. Leaves alternate, petioles ca. 12.5-15 mm long, slightly channeled and bimarginate above, glabrous, blades ca. 15-23 × 6-7.5 cm, narrowly elliptic, pinninerved, secondary veins 9-11 pairs, leaf surface glabrous on both sides, leaf apex acuminate, base obtuse or cuneate. Inflorescences ca. 1.5-2 cm long, axillary to leaves, axillary to tiny, deciduous bracts, on the proximal sections of new twigs too, paniculate, but strongly condensed, with very short rachis and secondary axes, peduncle ca. 0.5 cm long, glabrous, pedicels (1.2-)1.5-2.5(-3) mm long, glabrous. Flowers ellipsoid, slightly swollen in the middle of the hypanthium, greenish, tepals erect, outer tepals 0.5-0.6 × 0.5-0.6 mm, ovate, glabrous abaxially, glabrous adaxially except for some sericeous hairs at the base, inner tepals 0.4-0.5 × 0.2-0.3 mm, ovate, glabrous abaxially, glabrous adaxially or with some sericeous hairs at the base, staminodes of whorls I and II absent, stamens of whorl III 1-1.2 mm long, free, filaments white-tomentose throughout, denser on inside, anthers 0.3-0.4 mm, wholly exserted, glabrous or sparsely tomentose at the base outside, tomentose on lower half inside, openings dorsal, glands absent, hypanthium 1.1-1.3 mm deep, narrowly rhomboid, extending a little beyond the insertion point of stamens, glabrous outside, densely white-tomentose inside, pistil 2-2.3 mm long, glabrous, ovary 1-1.2 mm. Fruit unknown.

Taxonomic summary

Type. Panama. Darién: Cerro Tacarcuna S slope, 1,250-1,450 m, 26 January 1975, A. Gentry & S. Mori 13920 (holotype MO 2300651; isotype F 1763407).

Etymology. The species is named after Hendrik (Henk) Hessel van der Werff, a prolific scholar of the family Lauraceae in the Neotropics.

Distribution and habitat. So far, only known from the type collection, in the mountains of the southeastern edge of Panama, where premontane rain forest prevails.

Phenology. Flowers in winter; probably ripe fruits expected during autumn or early winter, since maturation of fruits in most Lauraceae takes around a year after flowering.

Conservation status. The place of the type collection is within the boundaries of the nature reserve Parque Nacional del Darién, but the altitudinal range within which the specimen was collected stretches barely for 40 km along the reserve. So, the species should be considered endangered.

Remarks

The collection on which the description of L. vanderwerffii is based was cited by Kurz (2000) as L. triandra, but there are several features that separate the former from this species. Whereas L. triandra presents branchlets solid, paniculate inflorescences (up to 6 cm long), stamens fused throughout (or almost so), glands at the base of filaments, anthers partially exserted, and hypanthium glabrous inside, L. vanderwerffii has hollow branchlets, sub-capitate inflorescences (up to 2 cm long), stamens free, no glands at the base of filaments, anthers wholly exserted, and hypanthium densely white tomentose inside.

This species is closely related to L. agglomerata; both present small, glomerate inflorescences, ellipsoid to narrowly rhomboid flowers with erect tepals, no staminodes, fully exserted stamens, no glands on filaments, pubescent stamens, and hypanthium tomentose within. However, L. vanderwerffii differs by having stamens free throughout, white tomentum on stamens and (densely on) inner face of hypanthium, and glabrous pistil, against stamens fused by their filaments, brownish-orange tomentum on stamens and upper part of hypanthium inside (sometimes completely glabrous), and puberulent style in L. agglomerata. It is worth to mention that they differ in ecological conditions as well; while L. agglomerata grows in lowland habitats (200-700 m), L. vanderwerffii is a mountain dweller above 1,200 m.

Acknowledgements

I would like to thank the curators of the herbaria cited in the Materials and methods section for allowing the study of specimens of Licaria in their collections. I also thank Jens Rohwer and an anonymous reviewer for their comments and calling my attention to several slips and wrong phrasing in some paragraphs. Eva Piedra assisted me with the preparation of figures. Phil Brewster kindly reviewed the final english version of the manuscript. I thank one of the reviewers who suggested to include the following exsiccata as part of the studied material for several of the species described here, however, it was not possible to see the specimens. So even they correspond to duplicates of the studied material, they are cited here just as a reference for researchers who might need to study them.

L. breedlovei; D. Breedlove 50394, isotype TEX 472525.

L. dolichopoda; B. Hammel et al. 16790, isotypes CR 147811 and CR 2918355; E. Bello & E. Cruz 4262, paratype CR 1596155; G. Herrera 4000, paratype CR 1596509; G. Herrera 4510, paratypes CR 159602, CR 176525 and CR 1561583; J. Marín & G. Marín 499, paratype CR 1596363.

L. gibbitepala; G. Herrera & A. Chacón 2427, isotype CR 1596536.

L. minutiflora; G. Herrera 500, isotype CR 151205; E. Bello 784, paratype CR 1513414; E. Bello 2208, paratype CR 1596135; Q. Jiménez & G Rivera 1011, paratypes CR 1561584 and CR 157780; G. Herrera 2942, paratype CR 1596539.

L. tomentulosa; G. Herrera 2165, isotypes CR 146925 and CR 2921047; G. Herrera 2056, paratypes CR 147034, and CR 2920969; G. Herrera 4115, paratypes CR 1596519, and CR 207025; A. Chacón 25, paratype CR 1596195.

References

Burger, W., & van der Werff, H. (1990). Flora Costaricensis. Family 80 Lauraceae. Fieldiana, Botany, n. s., 23, 1–129.

Gómez-Laurito, J., & Cascante, A. (1999). Licaria caribaea (Lauraceae): a new species from the Caribbean lowlands of Costa Rica. Novon, 9, 199–201. https://doi.org/10.2307/3391798 

Gómez-Laurito, J., & Estrada, A. (2002). Licaria leonis (Lauraceae), una nueva especie del Pacífico costarricense, y algunas notas sobre Licaria multinervis H. Kurz. Lankesteriana, 3, 5–9. https://doi.org/10.15517/lank.v2i1.23136

Hammel, B. E. (1986). New species and notes on Lauraceae from the Caribbean lowlands of Costa Rica. Journal of
the Arnold Arboretum, 67, 123–136. https://doi.org/10.5962/bhl.part.27389 

Kostermans, A. J. G. H. (1937). Revision of the Lauraceae II. The genera Endlicheria, Cryptocarya (American species) and Licaria. Recueil des Travaux Botaniques Néerlandais, 34, 500–609.

Kurz, H. W. (1983). Fortpflanzungsbiologie einiger Gattungen neotropischer Lauraceen und Revision der Gattung Licaria (Lauraceae) (Ph.D. Thesis). University of Hamburg, Germany.

Kurz, H. W. (2000). Revision der Gattung Licaria (Lauraceae). Mitteilungen aus dem Institut für Allgemeine Botanik in Hamburg, 28/29, 89–221.

Mez, C. (1889). Lauraceae americanae. Jahrbuch des Königlichen Botanischen Gartens und des Botanischen Museums zu Berlin, 5, 1–556.

Radford, A. E., Dickison, W. C., Massey, J. R., & Bell, C. R. (1974). Vascular plant systematics. New York: Harper & Row.

Van der Werff, H. (1988). Eight new species and one new combination of Neotropical Lauraceae. Annals of the Missouri Botanical Garden, 75, 402–419. https://doi.org/10.2307/2399431 

Van der Werff, H. (2009). Nine new species of Licaria (Lauraceae) from tropical America. Harvard Papers in Botany, 14, 145–159. https://doi.org/10.3100/025.014.0206