Taxonomía y sistemática

Roberto Arce-Pérez, Andrés Ramírez-Ponce *

Instituto de Ecología, A.C., Red de Biodiversidad y Sistemática, Carretera Antigua a Coatepec Núm. 351, El Haya, 91073 Xalapa, Veracruz, Mexico

*Corresponding author: andres.ramirez@inecol.mx (A. Ramírez-Ponce)

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Abstract

A bibliographic and museum review is carried out on the Cybistrinae species of Mexico, as well as comparative analysis with species from South America, concluding that Trifurcitus fallax (Aubé, 1838) has been wrongly cited for Mexico. Additionally, 2 new species are described as the first country-specific records, Trifurcitus mexicanus sp. nov. from the state of Chiapas, and T. maya sp. nov. from the state of Yucatán. Also, new state records are provided for Bifurcitus lherminieri (Guérin-Méneville, 1829) in Mexico. Future reviews of specimens under the names Bifurcitus, Cybister, Metaxydytes, and Trifurcitus are recommended as this could likely uncover more new species.

Keywords: Coleoptera; Dytiscidae; Cybistrinae; Trifurcitus; Bifurcitus; Mexico; New species

Notas sobre Cybistrinae de México (Coleoptera: Dytiscidae), con la descripción de 2 especies nuevas de Trifurcitus

Resumen

Se realiza una revisión bibliográfica y museística de las especies de Cybistrinae de México, así como un análisis comparativo con especies de Sudamérica, concluyendo que Trifurcitus fallax (Aubé, 1838) ha sido citada erróneamente para México. Adicionalmente, se describen 2 especies nuevas como los primeros registros específicos para el país, Trifurcitus mexicanus sp. nov. del estado de Chiapas, y T. maya sp. nov. del estado de Yucatán. También se proporcionan registros nuevos estatales para Bifurcitus lherminieri (Guérin-Méneville, 1829) para México. Se recomiendan revisiones futuras de especímenes bajo los nombres Bifurcitus, Cybister, Metaxydytes y Trifurcitus, ya que éstos, probablemente, podrían incluir más especies nuevas.

Palabras clave: Coleoptera; Dytiscidae; Cybistrinae; Trifurcitus; Bifurcitus; México; Especies nuevas

Introduction

Until recently, the subfamily Cybistrinae Sharp, 1880 included 1 tribe, 7 genera, 8 subgenera and 129 species with 10 subspecies worldwide (Nilsson & Hájek, 2023), including 2 genera from the New World: Megadytes Sharp, 1880, with 21 species in 4 subgenera, and Cybister Curtis, 1827, with 6 species in 2 subgenera and additional species without subgeneric assignment (Arce-Pérez et al., 2021; Nilsson & Hájek, 2023; Trémouilles, 1984, 1989a, b; Trémouilles & Bachmann, 1980). A phylogenetic study (Miller et al., 2024) based on morphological characters, focused on reclassifying the genera of Cybistrinae, updated the information including 1 tribe, 12 genera, 4 subgenera and 130 species with 10 subspecies (Miller et al., 2024). In this work, for the New World 7 genera were included: Bifurcitus Brinck, 1945 (3 species), Cybister Curtis, 1827 (5 species in 2 subgenera), Megadytes Sharp, 1882 (2 species), Metaxydytes Miller et al., 2024 (9 species), Nilssondytes Miller et al., 2024 (1 species), Paramegadytes Trémouilles & Bachmann, 1980 (2 species), and Trifurcitus Brinck, 1945 (6 species).

Of the 7 genera cited for the New World, 4 are reported for Mexico, Bifurcitus (2 species), Cybister (3 species), Metaxydytes (2 species), and Trifurcitus (1 species) (Arce-Pérez et al., 2021; Miller et al., 2024; Nilsson & Hájek, 2023). The only species of Trifurcitus cited for Mexico by Sharp (1882a, b), T. fallax (Aubé, 1838), was described from French Guyana. Dejean (1836: 60) lists it as Trochalus fallax from Cayenne. This name was made available by Aubé (1838: 54) as Cybister fallax. Sharp (1882a: 710 and 1882b: 47) placed the species in his new genus Megadytes, and Brinck (1945: 8) in his new subgenus Trifurcitus of Megadytes. Currently the species is classified in the genus Trifurcitus (Miller et al., 2024). Sharp (1882a, b) studied a female from the Edwin Brown collection reported it from Mexico without a precise locality. Wilke (1920: 247) cited 1 specimen from the British Museum from “Mexico” and another from “Orizaba-Mexico” (State of Veracruz). Zimmermann (1920: 256) listed Sharp’s specimen but cited it incorrectly from Central America. Trémouilles and Bachmann (1980: 125) and Trémouilles (1989b: 161) cited the species for Argentina, Bolivia and Brazil. Libonatti et al. (2013: 164) were the last to provide a new record of the species (Chaco province, Argentina). The larval stages of T. fallax were described by Ferreira (1995: 315) and Michat (2010: 381). Arce-Pérez et al. (2021: 331) provided a key for all the New World Cybistrinae species found north of Belize and Guatemala, including T. fallax.

For Mexico, there are no records later than those of Sharp (1882a, b) and Wilke (1920). Now, 104 years after, while reviewing Cybistrinae material from different Mexican collections, some specimens were found identified as T. fallax. However, while undertaking a comparative analysis with specimens from Argentina, Bolivia, Brazil and México housed in different museums, Sharp’s opinions stand out: “I have seen only two individuals of this species, one of them, from Dejean’s collection, was there labelled “Trochalus fallax mihi, h. in Cayenne, D. Lacordaire”: the other was in Edwin Brown’s collection and labelled in his handwriting “Cybister flavocinctus, Chev., Mexico.” The determination being wrong it is probable that the locality also of this latter specimen may be erroneous. Cayenne.; 1 Mexico. 1107” (Sharp, 1882a). “This little-known species is represented in Salle’s collection by a single female labelled “Trogus flavocinctus”, this determination, however, was erroneous and the specimen, a very fine one, agrees with the 2 other female, these being all that we know of the species” (Sharp, 1882b).

Based on the above, we consider that T. fallax is only distributed in South America (Argentina, Bolivia, Brazil and French Guiana), and therefore, the Mexican specimens correspond to another species, whose description is the objective of the present work.

Materials and methods

Type material and other specimens of Trifurcitus fallax (Aubé, 1838) were requested in different national and foreign museums. Four male specimens from Mexico were examined (CNIN), plus another dissected one and housed at BMNH by photographic comparison. The 4 Mexican specimens were hydrated in a humid chamber for 2 days, their genitals were removed and cleaned in hot water. The median lobe and parameres were disarticulated and mounted with the specimens. Two male specimens dissected from Argentina (MACN) determined by Trémouilles and Bachmann (1980) were reviewed in photographs as well as undissected specimens from Brazil and Bolivia deposited in collections in Germany (ZSM) (MZSP) and Brazil, that were used for comparison.

The Mexican specimens were studied with a LEICA MZ8 stereomicroscope and photographed with a Zeiss Stemi SV6 stereomicroscope, stacking several photographs into a final image. The final plates were edited in Photoshop CS6. The reviewed specimens come from the following collections —specimens reviewed directly: Colección Nacional de Insectos (CNIN), Instituto de Biología, Universidad Nacional Autónoma de México, Mexico City, Mexico (S. Zaragoza); Colección de Insectos del INECOL (IEXA), Instituto de Ecología A.C., Xalapa, Veracruz, Mexico (R. Arce-Pérez). Specimens reviewed by photographs: Museo Argentino de Ciencias Naturales (MACN), Buenos Aires, Argentina (P. Mulieri); Muséum National d’Histoire Naturelle (MNHN), Paris, France (website); Museu de Zoologia da Universidade de São Paulo (MZSP), Sao Paulo, Brazil (S. Casari); The Natural History Museum (BMNH), London, UK (M. Geiser); and Zoologische Staatssammlung München (ZSM), Germany (M. Balke). 

Results

Historiographical analysis allowed us to trace the depository of type material from Cayenne (French Guiana). Unfortunately, the specimens are lost, as it is the material from Bolivia (MNHN) identified by Trémouilles and Bachmann (1980). Only 1 female syntype was compared from the website of MNHN, and dissected males were also used from Mexico (BMNH) and Argentina (MACN), and specimens from Brazil (MZSP) and Bolivia (ZSP) (not dissected) for comparison via photographs.

When trying to compare the diagnostic characters presented in the original description made by Aubé (1838), the diagnosis of Sharp (1882a, b), and the diagnosis of Trémouilles and Bachmann (1980), the identity of Mexican specimens of T. fallax could not be confirmed. This was also observed in studies that addressed with the larva of T. fallax; when describing the third stage (1 from Brazil and another from Argentina), they appear as different species (Fig. 1a, b) (Ferreira, 1995; Michat, 2010), probably because the associated adults were different species, but were identified with the key of Trémouilles and Bachmann (1980) arriving to M. (T.) fallax.

The larva illustrated by Michat (2010) is now recognized as T. fallax (Miller et al., 2024). Also by making the determination by photographic comparison with specimens determined by specialists (determination labels of Guignot [1955, 1958], Bachmann [1979] and Trémouilles [1985]) deposited in several museums (MZSP, ZSM, BMNH) (Fig. 2a, f), among them a syntype female (MNHN), and by morphological comparison with the specimens 7715 and 7725 of the Museo Argentino de Ciencias Naturales, where it was observed that they are generally similar to the specimens from Mexico (length, shape, color, punctures) but differ in the diameter of the dorsal puncture and of ventrites III to V, being slightly thicker and denser in the South American specimens (Fig. 3a, h).

The specimens from Argentina, Bolivia and Brazil have transverse rows on ventrites III to V, plus a slight central accumulation of points in ventrite III (Fig. 3b, d, f, h); while the Mexican specimens present finer punctuations, with a transverse row in ventrites IV and V, and few central punctuations in ventrite III (Figs. 5b, 8b). The basal impression of the prosternal process in the specimens from Argentina (MACN) is variable, being present in specimen 7715 and completely absent in specimen 7725 (Fig. 3b), while in the specimens from Mexico it is present in Trifurcitus mexicanus nov. sp. (Fig. 5b, d), and absent in T. maya nov. sp. (Fig. 8b), also visible in the Bolivian specimen (Fig. 3d) and not observable in the Brazilian specimen (Fig. 3h).

Furthermore, the shape of the median lobe of the male genital in the Argentinean specimens and in the illustrations by Trémouilles and Bachmann (1980) is narrower and sharper at the apex (Fig. 4a, b, d, e) while in Mexican specimens it is slightly to moderately wider (Figs. 6a-f; 8c-e), In addition, the distance between the apex of the ventral sclerite and the apex of the median lobe appears to be smaller in South American specimens (these measurements may vary due to dehydration) (Figs. 4b, e, 6a, e, f, 8d, e).

The distribution of the species of Trifurcitus is Neotropical (Argentina, Bolivia, Brazil, French Guiana, and Panama), with T. fallax being recorded from Argentina, Bolivia, Brazil, and French Guiana (Nilsson & Hájek, 2023; Trémouilles & Bachmann, 1980), making its presence in Mexico unlikely. Historical analysis, morphological comparison and communication with specialists of the group allow us to support what was mentioned by Sharp (1882a, b), that T. fallax does not reach Mexico, and to report 2 new species of this genus for Mexico, T. mexicanus nov. sp. Arce-Pérez & Ramírez-Ponce for Chiapas, and T. maya nov. sp. Arce-Pérez & Ramírez-Ponce for Yucatán, representing the first records of the genus Trifurcitus Brinck for Mexico.

Descriptions

Trifurcitus mexicanus Arce-Pérez & Ramírez-Ponce, sp. nov.

(Figs. 5a-d, 6a-g)

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Differential diagnosis. The new Mexican species can be differentiated from the South American ones by the diameter of the dorsal punctuation, and of ventrites III to V (Fig. 5a, b), being slightly thicker and denser in the South American specimens (Fig. 3a-h). In addition, the shape of the middle lobe of the male genital in South American specimens is narrower and sharper at the apex (Fig. 4a, b, d, e), while in Mexicans it is slightly to moderately wide (Fig. 6a, b, d, e).

Description. Holotype (male, IEXA).Habitus and general surface structure: dorsal (Fig. 5a); body oval, maximum width behind of the half of the elytral length. Length 29 mm, maximum width 18 mm. Dorsal coloration dark olive green shiny, with wide reddish-yellow stripe along the lateral margins of the pronotum and elytra, near the elytral apex the olive-green coloration is interspersed with yellow punctuation of the lateral stripe; clypeus anteriorly and labrum reddish-yellow. Ventral coloration (Fig. 5b) black, with reddish-yellow palps and antennae, yellowish-reddish front and middle legs, black hind legs. Sculpture on dorsum and venter largely smooth; with punctuations of variable diameter and faint wrinkles and striae; the setation is minute, slender and sparse, present in punctuations and often almost imperceptible. Median lobe wider in its basal half (0.55 mm), narrowing apically, apex slightly rounded (Fig. 6a, e). Dorsal surface (Fig. 5a, c), head: clypeus with almost straight anterior margin, labrum with slightly sinuous anterior margin, with small central concavity. Clypeal line incomplete, widely interrupted medially. Two small, punctuate grooves transverse, immediately posterior to anterior margin. Strongly punctuate oval longitudinal depression on each side posterior to incomplete clypeal line. Short row of small punctures along the posterior half of inner margin of eyes (Fig. 5c). Antennae filiform. Both palps are slender, but slightly thicker than the reddish-yellow antennae. Setae very short, sparse in the grooves of the clypeus; thicker and denser in the concavity of the labrum; slightly longer in the longitudinal depression posterior to the interrupted clypeal line; very short and sparse on the inner margins of the eyes. Surface of the vertex with slight longitudinal wrinkles. Pronotum: anterior margin with short rows of small punctures interrupted medially; line of punctures slightly thicker, extending laterally reaching inner margin of reddish-yellow stripe; inner margin of stripe with scattered row of thicker punctures extending from base to apex. Surface with faint longitudinal striations and wrinkles, mainly in the posterior region, and a slight accumulation of punctures on each side of the disc. Lateral margin without edge, with complete yellowish-reddish band, which exceeds the yellowish-reddish border of the hypomeron. Short setae on the punctuation of the anterior edge, lateral margins and on the yellowish-reddish band. Elytra:3 longitudinal lines defined by broad and widely separated punctuations; first line with slightly elongated punctuations reaching near the apex; second and third lines with circular punctuations; third line at inner edge of reddish-yellow stripe. Elytral margins with a thick, complete border and minute, irregular punctuation; dark olive-green margins in anterior half. Reddish-yellow band along the margin of the elytra, not reaching the margin or the epipleura, more or less of equal width throughout its length, defined as a network of irregular polygonal pigments, which mixes with the dorsal olive-green colour as scattered dots. Very sparse setiferous punctuation on the yellow stripe and lateral edge; very short setae. Ventral surface (Fig. 5b, d), head:shiny black; mouthparts dark reddish; antennae and palps reddish-yellow. Prothorax:shiny black; hypomeron yellowish-reddish. Prosternal process subrectangular in anterior half, flat surface, anterior edge not notched, continuing into an oval depression with rounded apex; posterior half widened and lanceolate, pointed, reaching the deeply triangular anteromedial process of the metaventrite; lanceolate region with a lateral rim, and the apex acute with transverse striations (Fig. 5d), length 4.1 mm long by 1.3 mm wide. Pterotorax: epipleuron reddish-yellow, broad, with slight mesial narrowing. Suture between metaventrite and metacoxal plates weakly marked. Metaventrite with conspicuous curved row punctuationss in anteromedial region. Metacoxal lines strongly divergent anteriorly, not reaching anterior margin of metaventrite; with row of broad punctures extending beyond metacoxal lines to suture of metaventrite. Posterior margin of metacoxal processes with deep central triangular incision; lobes of processes broadly rounded. Abdomen: colour: shiny black, with a semicircular reddish-yellow spot on lateral margin of ventrites III to V; with a slight lateral depression in ventrites II to VI, deeper and expanded in ventrites V and VI; suture between ventrites I and II clearly marked; ventrite III with few, tiny punctures and wrinkles on middle and parallel wrinkles on distal margin; ventrites IV and V with transverse line of small punctures and superficial wrinkles (evident in ventrite V); ventrite VI with uniformly rounded apex, with a slight transverse depression, with the lateral depression deeper and more extended, with few, tiny scattered punctures. Setiferous puncture, with very short yellowish setae. Legs:front and middle legs reddish-yellow, hind legs black, with a light reddish trochanter in its apical half. Protarsomere I-III enlarged, oval-shaped; 1.3 mm long by 1.9 mm wide; protarsomere I with numerous minute sucking setae at base and a row of large sucking setae at apex, protarsomere II with only 1 row of large sucking setae, protarsomere III with 2 rows of large sucking setae, protarsomere V with a pair of long, black, curved, sharp claws; anterior claw longer and thicker. Mesotarsomeres dark; mesotarsomeres I-IV with a series of setae near apical margin (posteroventrally); mesotarsomeres I-II with abundant ventral rows of long pale-yellow setae; claws sharp and curved, the anterior one longer and thicker; both longer and thicker than the protarsal claws. Metafemur with rounded dorso-distal angle, weakly acute (almost straight), not pointed. Metatibia with 2 apical spurs, the outer one noticeably thinner than the inner one and with trifid apex. Last metatarsomere with 2 straight and sharp claws of equal length, the outer one slightly wider. Male genitalia (Fig. 6a-g). Median lobe wider in its basal half (0.55 mm), narrowing apically, apex slightly rounded (Fig. 6a, e). Median lobe in lateral view, length 4 mm (Fig. 6d, f); ventral, with maximum width 0.55 mm (Fig. 6e); ventrolateral (oblique view) 4 mm (Fig. 6f), and median sclerite 3 mm (Fig. 6e). Distance between the apex of the median sclerite and the apex of the median lobe 1 mm (Fig. 6e); Left paramere 4 mm, with row of external ridges, in oblique view, the ridges that reach the ventral margin in the apical 3/3 simulate small teeth (Fig. 6g).

Variation. A male specimen like the holotype (without genitalia) from Chiapas, Municipality of Cintapala (16°37’ N, 93°46’ W), 28.III.1985, Col. M.L. Lozano. “Small (length 27 mm, width 16.5 mm), dorsally, slightly brownish coloration; surface on the pronotum with more wrinkles on the disk; more evident stippling and wrinkles on ventricles III to V.” 

Females. Not present in the material studied. According to Trémouilles and Bachmann (1980), females present sexual sculpture formed by curved, anastomosing lines, or without sexual sculpture, and according to Aubé (1838), the females differ only by the simplicity of the front legs.

Taxonomic summary

Type locality:Mexico, Chiapas, Municipality of Concordia, km 17 carretera Jaltenango-Revolución Mexicana, 15°58’ N, 92°48’ W, elevation 575 m asl.

Type material:holotype: ♂, México: Chiapas/Municipio de Concordia, 15°58’ N, 92°48’ W/18-V-2012, Col. D. Reynoso-Velasco [typed, white label], “holotipo/Trifurcitus mexicanus nov. sp./Arce-Pérez & Ramírez-Ponce 2024” [typed, red label] (IEXA).

Habitat: Megadytes species have been reported to be associated with open, sunny environments in permanent and temporary lentic waters with dense vegetation; however, detailed habitat preferences are unknown for most species (Miller & Bergsten, 2016), except for Bifurcitus iherminieri (Hendrich et al., 2019). The specimen from Chiapas (Municipality of Concordia), was collected in a sunny and exposed area, on the banks of a permanent, slow-flowing stream, with an average depth of 80 cm, among grasses that grow on the riverbank (Fig. 7a, b) (Daniel Reynoso Velasco, personal communication).

Distribution: this species is known from Mexico, Chiapas, but being a species of a Neotropical genus, it is likely that it is also distributed in Oaxaca and Guatemala on the Pacific coast.

Etymology: because it is the first corroborate record of the genus Trifurcitus Brinck for the country, this species is named mexicanus.

Remarks

Trifurcitus mexicanus sp. nov. can be differentiated from Trifurcitus maya sp. nov. by the following characters (Trifurcitus maya nov. sp. [in brackets]). Trifurcitus mexicanus presents an oval depression with rounded apex in the anterior half of the prosternal process (Fig. 5d) [without depression (Fig. 8b)]; ventrites IV and V with a transverse line of small punctures and superficial wrinkles (Fig. 5b) [ventrite IV without apparent punctuation or wrinkles (Fig. 8b)]; Male genitalia in ventral view with broad median lobe in its basal half (0.55 mm), slightly narrowing apically and with rounded apex (Figs. 6a, e) [median lobe slender in basal half (0.53 mm), narrowing apically and with apex acute (Fig. 8d)].

Trifurcitus maya Arce-Pérez & Ramírez-Ponce, sp. nov.

(Fig. 8a-f)

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Differential diagnosis. In Trifurcitus mexicanus Arce-Pérez & Ramírez-Ponce.

Description. Habitus and general surface structure: dorsal (Fig. 8a): bodyoval, maximum width behind the half of the elytral length. Length 29 mm, 17 mm wide. Coloration bright dark olive green, with a broad reddish-yellowish stripe along the lateral margins of the pronotum and elytra, near the elytral apex interspersed with the yellow punctuation of the lateral band; clypeus anteriorly and labrum reddish-yellowish. Ventral (Fig. 8b): black coloration with reddish-yellow palps and antennae, dark reddish front and middle legs, black hind legs. Sculpture dorsal and ventral largely smooth, with punctuations of variable diameter and faint wrinkles and striae; the setation is minute, slender and sparse, present only at punctuations and often almost imperceptible. in ventral view, with median lobe slender in its basal half (0.53 mm), narrowing apically, with apex slightly acute (Fig. 8c-e). Dorsal surface (Fig. 8a), head: clypeus with almost straight anterior margin, labrum with slightly sinuous anterior margin, with small central concavity. Clypeal line incomplete, widely interrupted medially. Two small, punctuations grooves transverse, posterior to anterior margin. A punctuate oval depression on each side, posterior to incomplete clypeal line. A short line of small punctures along posterior half of inner margin of eyes. Antennae filiform. Both palps thin, like the antennae, reddish-yellow. Setae very short, sparse in the grooves of the clypeus; denser and thicker in the concavity of the labrum; slightly longer in the oval depression posterior to the interrupted clypeal line; very short and sparse on the inner margins of the eyes. Front surface with slight longitudinal wrinkles on the posterior half. Pronotum: anterior margin with short rows of small punctures interrupted medially; line of slightly thicker punctures extending laterally, reaching inner margin of reddish-yellowish stripe; inner margin of stripe with scattered row of thicker punctures extending from base to apex. Surface with faint dark longitudinal wrinkles, mainly in posterior region, and a slight accumulation of punctures on each side of disc. Lateral margin without border, with complete reddish-yellowish stripe, extending beyond reddish-yellowish border of hypomeron. Short setae on anterior margin puncture, lateral margins and on reddish-yellowish stripe. Elytra: 3 longitudinal lines defined by wide and widely separated punctuation; first line with slightly elongated punctuations reaching close to the apex; second and third lines with circular punctuations; third line on the inner edge of the reddish-yellowish stripe. Elytral margins with a thick complete border and tiny, irregular punctuations; dark olive-green margins in their anterior half. Reddish-yellowish stripe along the margin of the elytra that does not reach the margin or the epipleura, more or less of equal width throughout its length, defined as a network of irregular polygonal pigments, which mixes with the dorsal olive-green color as scattered dots. Very sparse setiferous punctuations on the reddish-yellowish stripe and lateral edge; very short setae. Ventral surface (Fig. 8b), head: shiny black; mouthparts dark reddish; antennae and palps dark yellowish reddish. Prothorax: shiny black; hypomeron dark reddish-yellowish. Prosternal process subrectangular in anterior half, smooth and flat surface, anterior edge not notched or depressed; posterior half widened and lanceolate, pointed, reaching the deeply triangular anteromedial process of the metaventrite; lanceolate region with a lateral rim, and the apex acute with transverse striations. Pterothorax: epipleuron dark reddish-yellow, broad, with slight mesial narrowing. Suture between metaventrite and metacoxal plates weakly impressed. Metaventrite with a curved row of small punctuations in the anteromedial region. Metacoxal lines strongly diverging anteriorly, not reaching anterior margin of metaventrite; with row of broad punctuations extending beyond metacoxal lines to suture of metaventrite. Posterior margin of metacoxal processes with deep central triangular incision; lobes of processes broadly rounded.

Abdomen: glossy black, with a slight reddish-yellow semicircular macule on the lateral margin of ventrites III to V; a slight lateral depression in ventrites II to VI, slightly deeper and expanded in ventrites V and VI; suture between ventrites I and II clearly marked; surface of ventrite II with faint parallel wrinkles on distal margin; ventrite III with few and tiny punctures in the center and parallel wrinkles in the distal region; ventrite IV without apparent puncture, but with scattered faint surface striae; ventrite V with a transverse line of few punctures and elongated wrinkles that do not reach the lateral depression; ventrite VI with uniformly rounded apex; with a slight transverse depression, and with lateral depression surrounded by slight striae, with scattered small subapical punctures. Setiferous punctuation with very short yellowish setae. Legs: fore and middle legs dark yellowish reddish, hind legs black, with pale reddish trochanter at apical half. Fore and middle legs dark yellowish reddish, hind legs black, with pale reddish trochanter at apical half. Protarsomere I with numerous tiny sucking setae at base and a row of large sucking setae at apex; protarsomere II with only 1 row of large sucking setae; protarsomere III with 2 rows of large sucking setae; protarsomere V with a pair of long, black, curved, sharp claws, the anterior 1 longer and thicker. Mesotarsomeres dark. Mesotarsomeres I-IV with a series of setae near the apical margin (posteroventrally); mesotarsomeres I-II with abundant ventral rows of long pale-yellow setae. Claws sharp and curved, the anterior 1 longer and thicker; both longer and thicker than the protarsal claws. Metafemur with rounded dorso-distal angle, weakly acute (almost straight), not pointed. Metatibiae with 2 apical spurs, the outer 1 noticeably thinner than the inner one, with trifid apex. Last metatarsomere with 2 straight and sharp claws of equal length, the outer 1 slightly wider. Male genitalia (Fig. 8c-f): parameres and median lobe; c-e) medial lobe in lateral, ventral and almost lateral (oblique) views; f) paramere in lateral view. c) Median lobe in lateral view (4.23 mm), and median sclerite (2.25 mm); d) median lobe in ventral view (maximum width 0.53 mm); e) median lobe in oblique ventrolateral view (4.26 mm), and median sclerite (3 mm); distance between median sclerite and apex of lobe 1.23 mm; f) left paramere (3.98 mm), with row of external ridges; the ridges reaching the ventral margin in the apical 3/3 (depending on the angle of inclination), simulate small teeth.

Variation. Paratype small. Length 27.5 mm, width 14.5 mm, dorsal and ventral punctures slightly smaller (less obvious). Median lobe in lateral view 4.15 mm; in ventral view, with maximum width 0.50 mm, and median sclerite 2 mm; ventrolateral (oblique) 4.20 mm, and median sclerite 2.95 mm; distance between the median sclerite and the apex of the lobe 1.20 mm; left paramere with row of external ridges, 3.95 mm; the ridges that reach the ventral margin in the apical 3/3 simulate small teeth. Another male from Mexico: total length 28.5 mm, width 14.5 mm. Dorsal and ventral punctuations slightly smaller (less evident). Median lobe in ventral view 4.20 mm, with maximum width 0.51 mm, and median sclerite 2.95 mm. Left paramere with row of external ridges 3.95 mm.

Taxonomic summary

Type locality: Mexico, Yucatán, km 90, ruta 295, Río Lagartos, 21°31’ N, 88°08’ W, elevation 10 m asl. 

Type material: holotype (♂, IEXA): “Mexico: Yucatán/21°31’ N, 88°08’ W, 18-vi-1985/Col.: H. Velasco” [typed, white label], “holotype/Trifurcitus maya nov. sp./Arce-Pérez & Fery 2024” [typed, red label] (CNIN). Paratypes: 1 ♂, same data as holotype (CNIN), and 1 ♂ without precise location (collected in Mexico) (BMNH). Both paratypes with the following label: “paratype/Trifurcitus maya nov. sp./Arce-Pérez & Fery 2024” [typed, yellow label].

Distribution: this species is known from northern Yucatán, but it is very likely that it is also distributed in Quintana Roo and Campeche, between the states of the Gulf of Mexico and Yucatán. 

Etymology: the specific name “maya” is assigned because it is the first record of the genus Trifurcitus for the region where the indigenous Maya people originated and developed in Mexico.

New state records:the giant diving beetle Bifurcitus lherminieri (Guérin-Méneville, 1829) is widely distributed in Mexico, recorded for the states of Campeche, Chihuahua, Jalisco, Oaxaca, Quintana Roo, Sinaloa, Veracruz and Yucatán, at elevations up to 1,480 m asl in cloud forests and temperate forests (Arce-Pérez & Reynoso-Velasco, 2022). It is now reported for the first time for the state of Nayarit, Tepic, 28-xi-1989, A. Cadena col. 1♂; and with reservation for the states of Guerrero, Acapulco, 5-xi-1970, J. Hendrichs col. (junto al mar) (1♀) and Tabasco, Villa Hermosa, Macultepec, 15/30-iv-1953, J. Hendrichs col. (1♀); Tonalá, Chico Zapote, 10-x-1953, J. Hendrichs col. (1♀) (CNIN).

Discussion

The fact that only 4 specimens of the genus Trifurcitus have been found in Mexico, a few others in South America and very few in the most important collections in the world, confirms what Miller (2013: 401) stated: “It is an interesting feature of dytiscid systematics that often the largest species are among the lesser-known taxa, while many of the smaller dytiscids have been revised using modern methods” (see also Short and McIntosh [2015: 671] for members of the family Hydrophilidae, and Arce-Pérez et al. [2021: 331] for other members of Cybisterinae, Dytiscidae). This also highlights the lack of collection activities (e.g. by using bottle traps as explained in Hendrich et al. [2019: 530] and faunal studies in aquatic environments in Mexico, as well as the need to restore, conserve and protect water bodies in various ecosystems in protected areas (and to the extent possible also in non-protected areas) to ensure the permanence of these beetles and other aquatic invertebrates.

Finally, it is evident that there is a need to review the material stored in collections under the generic names of Bifurcitus, Cybister, Metaxydytes (previously Megadytes and Cybister) to detect whether specimens of Trifurcitus mexicanus sp. nov., or Trifurcitus maya sp. nov. and other undescribed species may be hidden among them.

Acknowledgments

We thank the curators who kindly provided images, specially to Juan Carlos Urcola (University of Buenos Aires), and additional information: Santiago Zaragoza Caballero and Cristina Mayorga (CNIN); Pablo Mulieri and Gastón Zubarán (MACN), Sonia Casari and Gabriel Biff (MZSP), Michael Balke (ZSM) and Keita Matssumoto, Michael Geiser, and Max Barclay (BMNH). Special thanks to Daniel Reynoso-Velasco (INECOL), who donated the male from Chiapas and provided information and photos of the collecting site. Eder M. Mora (INECOL) took the photographs of the Mexican specimens. Finally, thanks to Emmanuel Arriaga Varela (INECOL) and an anonymous reviewer for their insightful comments to improve the work.

References

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Arce-Pérez, R., & Reynoso-Velasco, D. (2022). New state records for Megadytes lherminieri (Guérin-Méneville, 1829) (Coleoptera: Dytiscidae: Cybistrinae) in Mexico. Proceedings of the Entomological Society of Washington, 124, 359–361. https://doi.org/10.4289/0013-8797.124.2.359

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Ferreira, Jr. N. (1995). Description of the larvae of Megadytes fallax (Aubé) and M. marginithorax (Perty) (Coleoptera: Dytiscidae). The Coleopterists Bulletin, 49, 313–318.

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Hamid Nazari ^a, Farrokh Ghahremaninejad ^b, *

^a Bu-Ali Sina University, Department of Biology, 6517838695, Hamedan, Iran

^b Kharazmi University, Faculty of Biological Sciences, Department of Plant Sciences, 4911-15719, Tehran, Iran

*Corresponding author: fgh@khu.ac.ir (F. Ghahremaninejad)

Received: 07 November 2024; accepted: 21 March 2025

Abstract

Leaf trichomes are vital for plant physiology, defense, and ecological interactions. This study utilized scanning electron microscopy to examine the leaf trichomes of 7 species in the family Cordiaceae, including 5 species from the genus Cordia and 2 from Varronia. Various types of trichomes, including glandular, non-glandular, and stellate, were observed. Our findings highlight differences in trichome types, density, and distribution both within and between genera. This research enhances the understanding of anatomical diversity and the significance of leaf trichomes in Cordiaceae, providing a foundation for future studies in plant biology. The high diversity of trichome structure in the studied species indicates their importance for their classification. Therefore, the results of this study provide a useful insight into the diversity of trichomes and their potential as a taxonomic tool.

Keywords: Indumentum; Glandular; Non-glandular; Stellate trichomes; Taxonomy 

Resumen

Los tricomas de las hojas son vitales para la fisiología, la defensa y las interacciones ecológicas de las plantas. Este estudio utilizó microscopía electrónica de barrido para examinar los tricomas de las hojas de 7 especies de la familia Cordiaceae; se incluyeron 5 de los géneros Cordia y 2 de Varronia. Se observaron varios tipos de tricomas, incluidos glandulares, no glandulares y estrellados. Nuestros hallazgos resaltan las diferencias en los tipos de tricomas, la densidad y la distribución tanto dentro como entre géneros. Esta investigación mejora la comprensión de la diversidad anatómica, resalta la importancia de los tricomas de las hojas en Cordiaceae y proporciona una base para futuros estudios en biología vegetal. La gran diversidad de la estructura de los tricomas en las especies estudiadas indica su importancia para su clasificación. Por lo tanto, los resultados de este estudio proporcionan una buena visión de la diversidad de tricomas y su potencial como herramienta taxonómica.

Palabras clave: Indumento; Glandular; No glandular; Tricomas estrellados; Taxonomía

Contribución al valor sistemático de los tricomas foliares en las Cordiaceae (Boraginales)

Introduction

The family Cordiaceae in Boraginales includes 2 large genera, Cordia L. and Varronia P. Browne with a total of 368 accepted species (POWO, 2024) or 350 (APG 4, 2016). Its members are usually shrubs or trees that are distributed in tropical and subtropical regions (Luebert et al., 2016). The classification of this family and its subfamilies has been debated by botanists for years. In most references Cordiaceae has been recognized as a family or as part of Heliotropiaceae and Boraginaceae. Finally, based on the results of Luebert et al. (2016), this family was accepted as a separate family in Boraginales. Cordiaceae is the only family in Boraginales with plicate cotyledons and generally a twice-dichotomous style with 4 stigmatic branches (Luebert et al., 2016). Johnston (1951) introduced the genus Cordia with 5-7 sections for Cordiaceae and molecular work placed Varronia as the sister genus of Cordia (Miller & Gottschling, 2007). Species of Cordia are found principally in tropical and subtropical regions of the American, Asian, and African continents. In this genus, there are many species cultivated as ornamentals, and for wood and medicinal applications, with extensive use by traditional communities (Matias et al., 2015). Varronia is a Neotropical genus with most of its species naturally distributed in Brazil (Silva & Melo, 2019).

Leaf trichomes are specialized structures that grow on the epidermis of leaves. They play an important role in how plants adapt to their environment and interact with it (Wagner, 1991); also, they are a powerful tool in solving taxonomic problems (e.g., Ghahremaninejad et al., 2012). Trichomes play a significant role in the leaf texture of Cordiaceae species, contributing to their diagnostic value within the family. Studies have shown that the family possesses both glandular and non-glandular leaf trichomes, which influence their rough texture (Amer et al., 2016). Notably, in some regions, the abrasive surface of these leaves (including those of Cordia sebestena L.) has led to their traditional use as natural sandpaper (Flowers of India, 2025). Cordiaceae exhibits a wide range of leaf trichome morphologies, yet comprehensive studies elucidating their diversity and functional significance remain limited. Trichome morphology, density, and distribution are known to vary extensively even within closely related taxa, reflecting adaptation to diverse ecological niches and selective pressures (Rodríguez & Healey, 2000). In addition to their functional roles, the structural and functional diversity of leaf indument in Cordiaceae are indispensable taxonomic tools. Trichome characteristics often serve as apomorphic characters that assist botanists in resolving complex taxonomic issues (e.g., Beilstein et al., 2006; Ghahremaninejad, 2004; Kong & Hong, 2019; Steyn & Van Wyk, 2021). However, many studies within this family have paid insufficient attention to trichome features (e.g., Amer et al., 2016; Taroda, 1984).

Trichome morphology exhibits remarkable diversity across the plant kingdom, playing a significant role in the taxonomy and ecology of various plant families, including the Boraginaceae and Cordiaceae (Selvi & Bigazzi, 2001). Limited studies on Cordiaceae trichomes reveal a high diversity of trichomes both among closely related species (Tölke et al., 2013) and at the genus level (Silva et al., 2023). This diversity in trichome morphology suggests intricate evolutionary adaptations that may serve various ecological functions.

Given the existing literature on Cordia and Varronia, trichomes have critical taxonomic features in Cordiaceae, particularly for differentiating closely related genera. This study aims to examine the trichome morphology of both genera using SEM to clarify their taxonomic relationships. Scanning electron microscopy enhances trichome trait comparison by providing greater detail (Gonçales et al., 2023). We anticipated identifying distinct trichome characteristics to resolve existing taxonomic ambiguities. By focusing on these morphological characters, we seek to enhance the understanding of Cordiaceae taxonomy.

Material and methods

Samples were obtained from Herbarium specimens of the Naturhistorisches Museum Wien (W) and Botanical Museum Berlin-Dahlem (B), acronyms according to Thiers (2025). Trichome morphology was studied using SEM at the Natural History Museum (NHM), Vienna. Leaves were soaked in 40-degree water for 10 minutes to restore trichomes and then air-dried for 1 hour. Leaf samples were attached to SEM stubs with conductive adhesive tabs and coated with a thin layer of gold for conductivity, applied with a sputter coater. Imaging was performed with a JEOL JXA 6610LV SEM at the Vienna Museum. Digital images from various regions were captured, documenting trichome characteristics such as type, shape, size, density, and distribution for each species. Additionally, a voucher table listing the information and codes of the specimens used was prepared (Table 1).

Table 1 

The voucher table of studied specimens. 

No.	Species	Locality	Collector and number	QR code	Herbarium acronym	Type of trichome
1	Cordia africana Lam.	Ethiopia	U. i. 285	W0254121	W	Non-glandular
2	Cordia alliodora (Ruiz & Pav.) Oken	Brazil	s.c. 893	W0058028	W	Non-glandular
3	Cordia bicolor A.DC.	Brazil	Schomburgk 678	W0010617	W	Stellate
4	Cordia decandra Hook. & Arn.	Chile	K.H. & Rechinger 63378	W0254122	W	Non-glandular
5	Cordia myxa L.	Greece	Rainer KARL	W0254123	W	Non-glandular
6	Varronia bullata L.	–	–	W0254157	W	Glandular, non-glandular
7	Varronia guanacastensis (Standl.) J.S.Mill.	Costa Rica	Zamora et al. 6340	B101137807	B	Glandular, non-glandular (short pyramidal shape)

Results

Electron microscopy studies of 5 species of Cordia and 2 species of Varronia illustrate the diversity in the size, shape, and distribution of trichomes in Cordiaceae. Variation was observed both within and between genera. Two main types of trichomes were identified among the studied species, glandular and non-glandular. Glandular trichomes were observed only in Varronia species, while non-glandular were observed in species of both genera. In addition, a special type of stellate trichome, which mostly has more than 10 arms, as a first-time report, was observed in Cordia bicolor A. DC.

Among the investigated species, glandular trichomes with a size of 100 to 120 μm were observed only in Varronia bullata L. and V. guanacastensis (Standl.) J.J. Mill. (Fig. 1). A type of trichome was observed in Cordia myxa L., which is bag-like and different from non-glandular trichomes. The samples used in this research were herbarium specimens, but for accurate diagnosis of this trichome, fresh material is needed. 

In all 7 studied species, non-glandular trichomes were observed on both adaxial and abaxial leaf surfaces. In Cordia africana Lam., the upper surface of the leaf has scattered short trichomes that exist in the form of small protrusions distant from one another, while the back surface of the leaf in this species (Fig. 2A) has depressions where different trichomes are densely present in these depressions. In C. alliodora (Ruiz & Pav.) Oken., simple trichomes are observed on both surfaces. On the abaxial surface of the leaf, in addition to this type of trichome, there are smaller and curved trichomes that do not have small projections on their surface (Fig. 2B). On the abaxial surface of C. decandra Hook. & Arn. leaves, in addition to short and long simple trichomes, which are smooth and sometimes curved, horn-shaped hard trichomes are also observed (Fig. 2C). In C. myxa, in addition to the specific type of trichomes mentioned (referring to glandular trichomes), very small trichomes that include a widened base and a protrusion (Fig. 2D) are observed in nearly regular rows on the adaxial surface of the leaf. On the abaxial surface, long trichomes with small projections are observed. Varronia bullata also has simple trichomes, which are similar to the trichomes of the mentioned species, except that on the adaxial surface, trichomes are completely dormant (Fig. 3A), but on the abaxial surface, in addition to greater diversity and density, some standing or twisted trichomes are also seen (Fig. 3B). In Varronia guanacastensis, a special type of trichome was observed, which covered the adaxial surface of the leaf in addition to many glandular trichomes. These trichomes are short and have a conical end (Fig. 3C). On the abaxial surface, a type of horn-like non-glandular trichome is also seen (Fig. 3D).

Stellate trichomes are a type of branched trichome that have several arms arising from a common base (either stalked or sessile). This type of trichome was observed only in Cordia bicolor. The number of arms of these trichomes is between 10 and 17, and the length of each arm is between 50 and 100 μm. Figure 4 shows the studied specimen and the observed stellate trichome. The distribution and density of trichomes on the surface of the leaf can be seen with the naked eye most of the time. Figure 5 shows the leaves of the studied species where trichome density can be seen on their surface.

Microscopic examination of these 7 species revealed that the adaxial leaf surface generally has a lower density of trichomes compared to the abaxial surface, which has a higher density. On the adaxial surface of the leaf of Cordia africana, there are trichomes in the form of small protrusions that are sparse, while on the abaxial surface, the trichomes have a different shape and are densely placed inside the depressions, while long trichomes are rarely seen. In Cordia alliodora, C. bicolor, C. decandra, and C. myxa the type of trichome is similar on both surfaces, with the difference that they are scattered on the adaxial side and dense on the abaxial side. In the case of the 2 Varronia species, the trichomes are scattered on the adaxial surface of V. bullata and dense on the abaxial surface, but in V. guanacastensis, the trichomes are dense on both leaf surfaces, with the difference being that the type of trichome is different between the surfaces. Figure 6 shows the difference between trichome distribution on adaxial and abaxial leaf surfaces in all studied species.

Discussion

Our study on leaf trichomes within Cordiaceae highlights significant morphological diversity, underscoring the diagnostic value of trichomes in taxonomy. Trichomes were categorized as either glandular (exclusively in Varronia species) or non-glandular (present in both genera), establishing clear taxonomic distinctions between the 2 genera. The restriction of glandular trichomes to Varronia supports the value of trichomes as reliable taxonomic markers, reinforcing molecular evidence that separates Varronia from Cordia. Despite the limited number of species examined, these findings offer a foundation for further studies across Cordiaceae. A notable finding was the discovery of stellate trichomes in Cordia bicolor, a first report for this species and probably rare within Boraginales. Stellate trichomes, characterized by multiple arms emerging from a common base, were observed solely in Cordia bicolor after an examination of over 100 Boraginales species (details in preparation). Figure 5 illustrates this unique stellate trichome, underscoring its taxonomic significance and its potential adaptive function.

Previous studies align with our findings on trichome diversity. Silva et al. (2023) examined leaf anatomy in 10 Varronia species from Brazil, identifying secretory and non-secretory trichomes as key taxonomic indicators. Similarly, Tölke et al. (2013) demonstrated variation in glandular and non-glandular trichomes among V. globosa Jacq. and V. leucocephala (Moric.) J.S. Mill., with unique glandular types and micropapillae-covered trichomes distinguishing each species. Demétrio et al. (2020) reported distinctive non-glandular trichomes and a single glandular type in V. polycephala Lam., a medicinal species, which also contained cystoliths and crystal sand idioblasts. These variations highlight trichomes as valuable taxonomic features and adaptive characters. While this study suggests a difference between Varronia and Cordia, the limited scope relative to the genera’s size precludes definitive conclusions. Further sampling of more species is needed to confirm this distinction in leaf trichomes.

Moreover, the distribution of trichomes, denser on the abaxial leaf surfaces, suggests adaptations to environmental pressures and provides additional taxonomic insight. Consistent trichome types on particular leaf surfaces across species indicate conserved characters, useful for classification within the family. This diversity, particularly in non-glandular trichomes that vary in shape, size, and density, emphasizes the evolutionary lability of trichomes and their dual roles in adaptation and taxonomy.

Our use of SEM enabled detailed trichome analysis, offering precise structural insights and enhancing taxonomic resolution. Nazari and Ghahremaninejad (2024, 2025) also found that trichome examination can verify generic separations within Boraginales, as demonstrated in their study on Heliotropiaceae. Collectively, these findings underscore the morphological and taxonomic significance of trichomes, establishing them as key indicators in botanical classification.

Acknowledgments

We sincerely thank all the invaluable contributors to this work. Special thanks to Heimo Rainer, head of the Botany Department at the Natural History Museum of Vienna, for his extensive support. Additionally, we appreciate Astrid Hille, Andreas Berger, Tanja Schuster, and Johannes Walter from the same department for their assistance. We are also grateful to Wenke Wegner, a SEM specialist, for supervising the microscopic imaging of the fragments. Our thanks extend to W herbarium and B herbarium for sharing their extensive botanical resources.

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Eduardo Reyes-Grajales ^{a, b,} *, Christian Rico ^c, John Iverson ^d, Luis Díaz-Gamboa ^e, Marco A. López-Luna ^f, Wilfredo A. Matamoros ^g

^a El Colegio de la Frontera Sur, Departamento Conservación de la Biodiversidad, Doctorado en Ciencias en Ecología y Desarrollo Sustentable, Carretera Panamericana y Periférico Sur s/n, Barrio María Auxiliadora, 29290 San Cristóbal de Las Casas, Chiapas, Mexico 

^b Turtle Survival Alliance, 1030 Jenkins Road, Charleston, 29407 South Carolina, USA

^c Universidad de Ciencias y Artes de Chiapas, Instituto de Ciencias Biológicas, Maestría en Ciencias en Biodiversidad y Conservación de Ecosistemas Tropicales, Libramiento Norte Poniente, 1150, Lajas Maciel, 29039 Tuxtla Gutiérrez, Chiapas, Mexico

^d Earlham College, Department of Biology, 801 National Road West, 47374 Richmond, Indiana, USA 

^e Red para la Conservación de los Anfibios y Reptiles de Yucatán, Km. 5.5 Carr. Sierra Papacal-Chuburná Pto. Tablaje, 31257 Sierra Papacal, Yucatán, Mexico

^f Universidad Juárez Autónoma de Tabasco, División Académica de Ciencias Biológicas, Carretera Villahermosa-Cárdenas Km 0.5, 86039 Villahermosa, Tabasco, Mexico 

^g Universidad de Ciencias y Artes de Chiapas, Instituto de Ciencias Biológicas, Libramiento Norte Poniente, 1150, Lajas Maciel, 29039 Tuxtla Gutiérrez, Chiapas, Mexico

*Corresponding author: eduardo.reyes.grajales@gmail.com (E. Reyes-Grajales)

Abstract

Mexico has the second highest species richness of turtles in the world. However, there are several research gaps within this group compared to other reptiles, especially in the southeastern region, which has been described as the area with the highest herpetofaunal diversity. These data deficiencies have led to much uncertainty regarding the identification, occurrence, and status of the area’s turtles. Given this context, we provide an update for all the native turtle taxa present in each state in southeastern Mexico. We include maps with historical and unpublished distribution records for each taxon, along with a dichotomous key based on external morphology. We discuss the native turtle taxa documented in southeastern Mexico, the possible presence of some species in certain states, the identification of the turtles in this region, and their conservation status according to national, historical and current contexts.

Keywords: Conservation priorities; Freshwater turtles; Neotropical region; Reptiles; Testudines

Tortugas continentales del sureste de México: una actualización sobre la identificación, composición, distribución y conservación

Resumen

México tiene la segunda mayor riqueza de especies de tortugas en el mundo. Sin embargo, en este país existen varios vacíos de investigación dentro de este grupo en comparación con otros reptiles, especialmente en la región sureste, que ha sido descrita como el área con mayor diversidad herpetofaunística. Esta deficiencia de datos ha generado mucha incertidumbre en cuanto a la identificación, distribución y estado de las tortugas en la región. Dado este contexto, proporcionamos una actualización de todos los taxones nativos de tortugas presentes en cada estado del sureste de México. Incluimos mapas con registros históricos y no publicados de distribución para cada taxón, junto con una clave dicotómica basada en la morfología externa. Discutimos los taxones de tortugas nativas documentados en el sureste de México, la posible presencia de algunos taxones en ciertos estados, la identificación de las tortugas en esta región y su estado de conservación según los contextos nacional, histórico y actual.

Palabras clave: Prioridades de conservación; Tortugas dulceacuícolas; Región neotropical; Reptiles; Testudines

Introduction 

The order Testudines includes 2 extant suborders, comprising 14 families, 97 genera, 7 marine turtle species, and 346 continental land and freshwater turtles (TTWG, 2021). Mexico supports the second richest turtle fauna per country in the world (after the USA) with 7 families, 13 genera, and 49 species of continental terrestrial and freshwater turtles (Hurtado-Gómez et al., 2024; Loc-Barragán et al., 2020; López-Luna et al., 2018; TTWG, 2021). When subspecies are included, a total of 63 distinct taxa are recognized in Mexico, with nearly half (49%, 31 taxa) being endemic (Hurtado-Gómez et al., 2024; Loc-Barragán et al., 2020; López-Luna et al., 2018; TTWG, 2021). Of those, 5 taxa have been described since 2010: Gopherus evgoodei, G. morafkai, Kinosternon cora, K. vogti, and Trachemys venusta iversoni (Edwards et al., 2016; Loc-Barragán et al., 2020; López-Luna et al., 2018; McCord et al., 2010; Murphy et al., 2011), and 5 taxa were taxonomically rearranged: K. cruentatum, K. mexicanum, K. stejnegeri, Terrapene mexicana, and T. yucatana (Hurtado-Gómez et al., 2024; Iverson & Berry, 2024; Martin et al., 2013; McCord, 2016;). It is noteworthy to mention that ~ 50% of Mexican continental turtles lack basic natural history data, which makes it cumbersome to comprehensively assess their actual conservation status (Flores-Villela & García-Vázquez, 2014; Macip-Ríos et al., 2015). Legler and Vogt (2013) stated that to solve “Mexican turtle conservation issues”, an integrative conservation research approach is necessary, to build knowledge about life history and ecology of these organisms. 

Within Mexico, the southeastern region (Campeche, Chiapas, Oaxaca, Quintana Roo, Tabasco, Veracruz, and Yucatán) is characterized by high turtle endemism, with high presence of human induced alterations at different ecosystem levels (Ennen et al., 2020). Historically, many indigenous cultures in this region incorporated turtles (e.g., Dermatemys mawii, and those in the genera Trachemys and Kinosternon) into their diets as ceremonial or complementary foods (Beauregard et al., 2010; González-Porter et al., 2011; Legler & Vogt, 2013; Velázquez-Nucamendi et al., 2021). More recently, southeastern Mexico has become one of the hotspots where turtles are extracted for illegal trade worldwide, especially from Chiapas, Tabasco, and Veracruz (Legler & Vogt, 2013; Macip-Ríos et al., 2015; TTWG, 2021). In response to these actions, standards have been established at both the national level (e.g., the list of Mexican federal government protected species of flora and fauna) and international levels (e.g., the CITES appendices) to regulate the use of turtles. However, the application of protocols for the study or protection of this group of vertebrates in southeastern Mexico has shown inconsistencies in the processes of identification and/or systematization of information on their distribution (Flores-Villela & García-Vázquez, 2014; Legler & Vogt, 2013; Macip-Ríos et al., 2015). Therefore, there is a recognized need to design tools and update information on these aspects to safeguard these turtles.

To contribute to the resolution of this situation, in this study we set 2 main goals: 1) to provide an up-to-date checklist, with general comments on the distribution of the continental turtles occurring in southeastern Mexico, and 2) to present a practical dichotomous key for their identification that encompasses the current turtle taxonomy in southeastern Mexico. Our findings can be implemented immediately in activities related to the study and protection of continental turtles in this region of Mexico.

Materials and methods

We define southeastern Mexico as the states of Campeche, Chiapas, Oaxaca, Quintana Roo, Tabasco, Veracruz, and Yucatán (Fig. 1). The region is delimited by the Isthmus of Tehuantepec as the initial dividing line, given its significance as a major biogeographic barrier (Huidobro et al., 2006; Quiroz-Martínez et al., 2014). However, considering that several turtle taxa extend west and north just beyond this barrier, we chose to include Mexican states that comprise part of the isthmus region. This region comprises ~ 415,000 km² originally vegetated with tropical evergreen forest and tropical deciduous forest with warm humid and warm subhumid climates (Leopold, 1950). In this region, turtles typically occur from sea level to approximately 1,200 m (Legler & Vogt, 2013). Major geographic features of the region are: the Gulf Coastal Plain, Sierra Madre de Oaxaca, Sierra Madre del Sur, Pacific Coastal Plain, Isthmus of Tehuantepec, Chiapas Highlands, Sierra Madre de Chiapas, Chiapas Coastal Plain, Central Depression of Chiapas, and the Yucatán Peninsula (Contreras-Balderas et al., 2008; Legler & Vogt, 2013). The main rivers are: Candelaria, Usumacinta, Grijalva, Tonalá, Coatzacoalcos, Papaloapan, Jamapa, Tehuantepec, and Ometepec (INEGI, 2021) (Fig. 1).

Georeferenced point locations were obtained for native continental turtles of southeastern Mexico from a combination of our own fieldwork records, the Turtle Taxonomy Working Group (TTWG, 2021, TTWG, 2025), and data repositories, including the Global Biodiversity Information Facility (GBIF, 2024), Sistema Nacional de Información sobre la Biodiversidad (SNIB-Conabio, 2024), Áreas Naturales y Vida Silvestre of the Secretaría del Medio Ambiente e Historia Natural (Semahn), iNaturalist (2024), and published scientific literature (Supplementary material: Table S1).

We used a systematic approach, establishing the TTWG shapefile (2021, 2025) as our base dataset. All newly identified occurrence points from additional sources were stored in a georeferenced database for the subsequent creation of maps using QGIS 3.34.2 (QGIS, 2024). Distribution polygons were based on TTWG (2025) and were expanded to include extralimital records verified through our compilation.

To ensure spatial accuracy, only points that provided open, non-obscured coordinates with reported location uncertainties of ≤ 10 km were incorporated. In the case of iNaturalist data, we exclusively used “research-grade” observations and excluded any records with obscured or low-precision coordinates (e.g., obscured within ~ 400 square miles). Records without supporting metadata or located significantly outside of known ranges were critically assessed, and when appropriate, excluded from analyses.

Special attention was given to isolated or potentially non-native records. For instance, we included K. flavescens from Veracruz based on the report of Auth et al. (2000) and the corroboration of voucher specimens (BCB 7489) by JBI at the Strecker Museum. We also carefully evaluated records of other species commonly subject to anthropogenic translocation, considering only those that plausibly represent native occurrences based on geographic and ecological context (see Discussion section). This rigorous validation process aimed to minimize the inclusion of records originating from village collections, pet trade, or other human-mediated movements, unless justified by the locality’s proximity to known native ranges or supporting documentation.

Our checklist includes valid names, authorities, and year of publication as in TTWG (2025). The dichotomous key we created based initially on the taxon descriptions provided in Legler and Vogt (2013). We then updated the key with the taxa recognized subsequent to Legler and Vogt (2013), and verified and added pertinent meristic and morphometric characters, and pigmentation patterns from specimens deposited in the Herpetology Section at the Zoológico Regional Miguel Álvarez del Toro (ZooMAT, Tuxtla Gutiérrez, Chiapas), the Colección herpetológica of El Colegio de la Frontera Sur (ECOSUR, San Cristóbal, Chiapas), and our own field data. 

We refer to the plastral formula as the relative lengths of the midline sutures of each plastral scute (Supplementary material: Fig. S1). Due to inconsistencies (conventional vs. new) in the nomenclature of plastral scutes (Hutchison & Bramble, 1981; Legler & Vogt, 2013), we followed the recommendation of Legler and Vogt (2013) to use the numerical nomenclature for the plastral formula, where the counts start anteriorly (Supplementary material: Fig. S1). For the nomenclature of the head stripes, we followed Ernst (1978) for Rhinoclemmys spp., and Legler (1990) for Trachemys spp. We used the term “tomiodonts” according to Moldowan et al. (2015), and “tubercles” according to Winokur (1982).

For conservation criteria at the national level, we consulted the Mexican Government list in the NOM-059 (Semarnat, 2010, 2025), and for international criteria, we referred to the IUCN Red List of threatened species (IUCN, 2024) and the CITES appendices (CITES, 2024). Additionally, we used the EDGE metrics, as it prioritizes species based on their evolutionary distinctiveness (ED), which measures the relative contribution of a species to the total evolutionary history of their taxonomic group, and global endangerment (GE), or extinction risk (Gumbs et al., 2018). This metric has been recognized as useful to meaningful priorities for conservation. 

Results

Native continental turtles in southeastern Mexico are represented by 5 families, 8 genera and 22 species with 9 recognized subspecies, for a total of 25 extant continental taxa (Table 1). The most speciose families in southeastern Mexico are the Kinosternidae, with a total of 13 taxa and Emydidae with 6 taxa (Table 1). The states with the greatest species richness are Oaxaca (16 taxa), followed by Chiapas (15), and Veracruz (13), and those with the least species richness were Quintana Roo (11), Tabasco (9) and Yucatán (7) (Table 2). Ten continental turtles in 4 genera are endemic to the region, as follows: Kinosternon (4 taxa), Terrapene (2 taxa), Trachemys (2 taxa) and Rhinoclemmys (2 taxa) (Table 3). The states with the highest number of Mexican endemic taxa are Oaxaca (2 species and 2 subspecies), Quintana Roo (2 species and 1 subspecies), Veracruz (2 species and 1 subspecies), and Yucatán (2 species and 1 subspecies) (Tables 1, 3). 

Table 1

Diversity of continental turtles in southeastern Mexico. Ca = Campeche, Ch = Chiapas, Oa = Oaxaca, QR = Quintana Roo, Ta = Tabasco, Ve = Veracruz, Yu = Yucatán; CSP = count of states present; % S = percentage considering all the taxa distributed in southeastern Mexico; X = presence; – = undocumented.

Family

Genus

Species

Subspecies

Ca

Ch

Oa

QR

Ta

Ve

Yu

CSP

% S

Chelydridae

Chelydra

C. rossignonii

X

X

X

–

–

X

–

5

71.4

Dermatemydidae

Dermatemys

D. mawii

X

X

–

X

X

X

–

5

71.4

Emydidae

Terrapene

T. mexicana

–

–

–

–

–

X

–

1

14.3

T. yucatana

X

–

–

X

–

–

X

3

42.9

Trachemys

T. grayi

T. g. grayi

–

X

X

–

–

–

–

2

28.6

T. venusta

T. v. cataspila

–

–

–

–

–

X

–

1

14.3

T. v. iversoni

–

–

–

X

–

–

X

2

28.6

T. v. venusta

X

X

X

X

X

X

–

6

85.7

Geoemydidae

Rhinoclemmys

R. areolata

R. areolata

X

X

X

X

X

X

X

7

100

R. pulcherrima

R. p. incisa

–

X

X

–

–

–

–

2

28.6

R. p. pulcherrima

–

–

X

–

–

–

–

1

14.3

R. rubida

R. r. rubida

–

X

X

–

–

–

–

2

28.6

Kinosternidae

Claudius

C. angustatus

X

X

X

X

X

X

X

7

100

Kinosternon

K. abaxillare

–

X

–

–

–

–

–

1

14.3

K. acutum

X

X

X

X

X

X

–

6

85.7

K. creaseri

X

–

–

X

–

–

X

3

42.9

K. cruentatum

X

X

X

X

X

X

X

7

100

K. flavescens

–

–

–

–

–

X

–

1

14.3

K. herrerai

–

–

–

–

–

X

–

1

14.3

K. integrum

–

–

X

–

–

–

–

1

14.3

K. leucostomum

X

X

X

X

X

X

X

7

100

K. mexicanum

–

X

X

–

–

–

–

2

28.6

K. oaxacae

–

–

X

–

–

–

–

1

14.3

Staurotypus

S. salvinii

–

X

X

–

–

–

–

2

28.6

S. triporcatus

X

X

X

X

X

X

–

6

85.7

Totals by state

11

15

16

11

9

13

7

Table 2

Summary of taxonomic diversity of continental turtles by state in southeastern Mexico. The number of continental turtles found in Mexico was established according to TTWG (2021, 2025). Hurtado-Gómez et al. (2024), and Iverson and Berry (2024). The percentage with respect to diversity at the national level (left) and in southeastern Mexico (right) is in parentheses.

Place	Families	Genera	Species	Taxa
Mexico	7	13	50	65
Southeastern Mexico	5 (71.4)	8 (61.5)	22 (45)	25 (39.7)
Campeche	5 (71.4 / 100)	8 (61.5 / 100)	11 (22.4 / 50)	11 (17.5 / 44)
Chiapas	5 (71.4 / 100)	7 (53.8 / 87.5)	15 (30.6 / 68.2)	15 (23.8 / 60)
Oaxaca	4 (57.1 / 80)	6 (46.2 / 75)	15 (30 / 68.2)	16 (25.4 / 64)
Quintana Roo	4 (57.1 / 80)	6 (46.2 / 75)	10 (20 / 45.5)	11 (17.5 / 44)
Tabasco	5 (71.4 / 100)	7 (53.8 / 87.5)	9 (18.4 / 40.9)	9 (14.3 / 36)
Veracruz	5 (71.4 / 100)	8 (61.5 / 100)	13 (26.5 / 59.1)	14 (22.2 / 56)
Yucatán	3 (42.9 / 60)	4 (30.8 / 50)	5 (10.2 / 22.7)	5 (7.9 / 20)

Dichotomous key to the general and plastron view of each turtle (Fig. 2), the plastral nomenclature and the names of the head stripes (Supplementary material: Figs. 1S, S2). The Spanish translation is presented in Supplementary material.

1A. Posterior plastral lobe ends in a point …………………………………… 2 (Fig. 2A)

1B. Posterior plastral lobe does not end in a point …………………………………… 5 (Fig. 2B)

2A. Reduced bridge almost the same length size as plastral scute 2. Kinosternidae: Staurotypus, …………………………………… 3

2B. Extremely narrow, reduced bridge shorter than the length of plastral scute 2 …………………………………… 4

3A. Top and sides of head boldly marked with irregular dark and pale reticulations; 3 distinctive carapace keels, well developed posteriorly, especially the middle keel ……………………………………S. triporcatus (Fig. 2Y)

3B. Top of head dark, usually unicolored, lacking bold pattern; 3 distinctive carapace keels of similar size, anterior to posterior ……………………………………S. salvinii (Fig. 2X)

4A. Three pointed tomiodonts on the upper tomium; neck not ornamented with cutaneous tubercles; tail not as long as the plastron …………………………………… Kinosternidae: Claudius angustatus (Fig. 2M) 

4B. One medial pointed extension on the upper tomium; neck ornamented with long, flat, pointed cutaneous tubercles; tail about as long as the plastron …………………………………… Chelydridae: Chelydra rossignonii (Fig. 2A)

5A. Interdigital membranes not present on forefeet or hind feet …………………………………… 6

5B. Interdigital membranes present on fore and hind feet ……………………………………11

6A. One plastral hinge, allowing movement of anterior and posterior plastral lobes; the posterior end of the plastron rounded ……………………………………Emydidae: Terrapene, 7

6B. A transverse plastral hinge is absent; the posterior end of the plastron is notched …………………………………… Geoemydidae: Rhinoclemmys, 8

7A. Plastral scute 5 averaging 15% the straight-midline length of the posterior plastral lobe; plastral scute 3 averaging 23% the straight-midline length of the anterior plastral lobe ……………………………………T. mexicana (Fig. 2C)

7B. Plastral scute 5 averaging 21% the straight-midline length of the posterior plastral lobe; plastral scute 3 averaging 33% the straight-midline length of the anterior plastral lobe …………………………………… T. yucatana (Fig. 2D)

8A. Yellow markings predominate on the forefeet, hind feet, neck and/or head ……………………………………9

8B. Red markings predominate on the forefeet, hind feet, neck and/or head …………………………………… 10

9A. Red/orange dorsolateral head stripes continuous or discontinuous; each costal scute uniformly colored ……………………………………R. areolata (Fig. 2I)

9B. Red/orange dorsolateral head stripes are absent; each lateral scute with 1 pale areolar spot with a dark outline, possibly with obvious light-colored concentric rings around it ……………………………………R. rubida rubida (Fig. 2L)

10A. Carapace is elevated; inferior surface of each marginal scute with 1 transverse pale mark ……………………………………R. pulcherrima incisa (Fig. 2J)

10B. Carapace is depressed; inferior surface of each marginal scute with 2 transverse, dark-bordered pale marks ……………………………………R. p. pulcherrima (Fig. 2K)

Table 3

Conservation status of the continental turtles of southeastern Mexico. NOM-059 = List of Mexican federal government protected species of flora and fauna; P = endangered (in danger of extinction), Pr = under special protection, A = threatened; Red List = the IUCN Red list of threatened species; CITES = Convention on International Trade in Endangered Species of Wild Fauna and Flora; En = national endemism; Y = endemic to Mexico; N = not endemic to Mexico; EDGE = EDGE score (Gumbs et al., 2018; higher threat = higher score).

Taxa	NOM-059	Red List	CITES	EDGE	En
Chelydra rossignonii	Pr	Vulnerable A2d	–	5.22	N
Dermatemys mawii	P	Critically endangered A2abd+4d	II	7.15	N
Terrapene mexicana	Pr	Vulnerable A2bcde+4bcde	II	4.19	Y
Terrapene yucatana	Pr	Vulnerable A2bcde+4bcde	II	4.19	Y
Trachemys grayi grayi	–	–	–	–	N
Trachemys venusta cataspila	–	–	–	–	Y
Trachemys venusta iversoni	–	–	–	–	Y
Trachemys venusta venusta	–	–	–	–	N
Rhinoclemmys areolata	A	Near threatened	II	3.77	N
Rhinoclemmys pulcherrima incisa	A	–	II	–	N
Rhinoclemmys pulcherrima pulcherrima	A	–	II	–	Y
Rhinoclemmys rubida rubida	Pr	Near threatened	II	3.87	Y
Claudius angustatus	P	Near threatened	II	4.36	N
Kinosternon abaxillare	–	Vulnerable A2cd+4cd	II	–	N
Kinosternon acutum	Pr	Near threatened	II	4.36	N
Kinosternon creaseri	–	Least concern	II	3.67	Y
Kinosternon cruentatum	–	–	II	–	N
Kinosternon flavescens	–	Least concern	II	3.67	N
Kinosternon herrerai	Pr	Near threatened	II	4.36	Y
Kinosternon integrum	Pr	Least concern	II	3.67	Y
Kinosternon leucostomum	Pr	–	II	–	N
Kinosternon mexicanum	–	–	II	–	N
Kinosternon oaxacae	Pr	–	II	4.36	Y
Staurotypus salvinii	Pr	Near threatened	II	4.69	N
Staurotypus triporcatus	A	Near threatened	II	4.69	N
Total of taxa in the categories considered	15	15	20	15

11A. There are no transversely oriented plastral hinges allowing plastral movement ……………………………………12

11B. There are 1 or 2 transversely oriented plastral hinges, allowing 1 or both plastral lobes to move around the scute 4…………………………………… Kinosternidae: Kinosternon, 16

12A. The head typically has a pale-colored patch that covers part or all of the dorsal region of the head but is never striped ……………………………………Dermatemydidae: Dermatemys mawii (Fig. 2B)

12B. The head is colored with obvious yellow stripes…………………………………… Emydidae: Trachemys, 13 

13A. Carapace ocelli centered on each costal scute and occupying most of scute…………………………………… 14

13B. Carapace ocelli not centered on costal scutes ……………………………………15 

14A. Carapace ocelli have an obvious large dark center to each ocellus ……………………………………T. venusta iversoni (Fig. 2G)

14B. Carapace ocelli lack an obvious dark center to each ocellus ……………………………………T. v. venusta (Fig. 2H)

15A. No light-colored ocelli on carapace; most of the central secondary orbitocervical stripes are narrow, of roughly equal width, and lacking black borders…………………………………… T. grayi grayi (Fig. 2E)

15B. Ocelli not centered in lateral scutes or broken; The postorbital stripe is thin where it contacts the orbit, then widens to about the diameter of the orbit; the central secondary orbitocervical stripes vary in width ……………………………………T. v. cataspila (Fig. 2F)

16A. Only the anterior plastral lobe is movable ……………………………………K. herrerai (Fig.2S)

16B. Both plastral lobes are movable relative to plastral scute 4 ……………………………………17

17A. Axillary scutes absent ……………………………………K. abaxillare (Fig. 2N)

17B. Axillary scutes present ……………………………………18 (see Fig. 2P)

18A. Moveable plastral lobes do not close the shell opening completely ……………………………………19

18B. Moveable plastral lobes close the shell opening completely ……………………………………20

19A. Plastral formula is 6 < = > 4 > 2 > 1 > 5 > 3 ……………………………………K. flavescens (Fig. 2R)

19B. Formula plastral is 4 > 6 > 1 > 5 > 2 > 3 ……………………………………K. oaxacae (Fig. 2W)

20A. Eyes with red pigment ……………………………………K. acutum (Fig. 2O)

20B. Eyes do not have red pigment…………………………………… 21

21A. Tricarinate carapace (less obvious in older individuals) ……………………………………22

21B. Unicarinate carapace ……………………………………23

22A. Plastral formula is 4 > 6 ……………………………………K. integrum (Fig. 2T)

22B. Plastral formula is 6 > 4 ……………………………………24

23A. Plastral formula is 1 > 2 ……………………………………K. creaseri (Fig. 2P)

23B. Plastral formula is 2 > 1 ……………………………………K. leucostomum (Fig. 2U)

24A. Maximum carapace width averages 77.1% (standard deviation [S.D.] 2.8%) of maximum plastron length in females and 74.6% (S.D. 2.8%) in males; the length of the plastral suture 4 averages 55.3% (S.D. 3.9%) of maximum shell height in females and 61.7% (S.D. 4.9%) in males ……………………………………K. mexicanum (Fig. 2V)

24B. Maximum carapace width averages 69.8% (S.D. 3.5%) of maximum plastron length in females and 68.9% (S.D. 2.8%) in males; the length of the plastral suture 4 averages 61.7% (S.D. 4.9%) of maximum shell height in females and 64.4% (S.D. 4.5%) in males ……………………………………K. cruentatum (Fig. 2Q)

Distributions of continental turtles of southeastern Mexico

In this section the abbreviations are: Ca = Campeche, Ch = Chiapas, Oa = Oaxaca, QR = Quintana Roo, Ta = Tabasco, Ve = Veracruz, Yu = Yucatán.

Chelydra rossignonii (Bocourt, 1868; Figs. 2A, 3A): along the Gulf of Mexico versant from the Jamapa River (Ve) to the Usumacinta River (Ta and Ch), including Laguna de Terminos (Ca). Other rivers include the Papaloapan, Coatzacoalcos (both in Oa and Ve), and lower Grijalva (Ch).

Dermatemys mawii Gray, 1847 (Figs. 2B, 3B): from the Jamapa River (Ve) to Champoton River (Ca) on the Gulf of Mexico versant, including the Usumacinta (Ca, Ch and Ta) and Lacantun Rivers (Ch). In Chetumal Bay (QR) the distribution extends to and beyond the Belize border.

Terrapene mexicana (Gray, 1849; Figs. 2C, 3C): from the Tamesi River to the Jamapa River, including the Tamiahua Lake area; on the Gulf of Mexico versant in Veracruz and northward into Tamaulipas. 

Terrapene yucatana (Boulenger, 1895; Figs. 2D, 3C): most of the western Yucatán Peninsula (primarily Yucatán and Campeche), with rare and localized occurrences in the northern region of Quintana Roo.

Trachemys grayi grayi (Bocourt, 1868; Figs. 2E, 3D): from La Arena River (Oa) to the Suchiate River on the Pacific versant (Ch), and southward to El Salvador.

Trachemys venusta cataspila (Günther, 1885; Figs. 2F, 3D): from the Jamapa River to the Panuco River (both in Ve) on the Gulf of Mexico versant, and northward in Tamaulipas.

Trachemys venusta iversoni McCord, Joseph-Ouni, Hagen, and Blanck, 2010 (Figs. 2G, 3D): most of the northern portions of Yucatán and Quintana Roo.

Trachemys venusta venusta (Gray, 1856; Figs. 2H, 3D): from the Jamapa River (Ve) to the Champoton River (Ca) on the Gulf of Mexico versant, including the Usumacinta (Ca, Ch and Ta) and Lacantun Rivers (Ch). In Chetumal Bay (QR) the distribution continues across the border into Belize and Guatemala.

Rhinoclemmys areolata (Duméril and Bibron in Duméril and Duméril, 1851; Figs. 2I, 3E): from the Jamapa River eastward (Ve) on the Gulf of Mexico versant throughout the north portions of Oaxaca and Chiapas and extended across Tabasco and the Yucatán peninsula (Ca, Yu and QR), and into Guatemala and Belize. 

Rhinoclemmys pulcherrima incisa (Bocourt, 1868; Figs. 2J, 3F): from the west portion of the Copalita River (Oa) to the Suchiate River (Ch) on the Pacific versant, and southeast to Nicaragua. 

Rhinoclemmys pulcherrima pulcherrima (Gray, 1856; Figs. 2K, 3F): from the Tehuantepec River (Oa) westward on the Pacific versant to the Balsas River, Guerrero.

Rhinoclemmys rubida rubida (Cope, 1870; Figs. 2L, 3E): from the Ometepec River (Oa) to the Suchiate River (Ch) on the Pacific versant, including the Atoyac and Tehuantepec basins (both in Oa).

Claudius angustatus Cope, 1865 (Figs. 2M, 3G): from the Jamapa River (Ve) to the western and southern Yucatán peninsula on the Gulf of Mexico versant, including the Usumacinta (Ca, Ch and Ta) and Lacantun Rivers (Ch), and southward into Guatemala and Belize.

Kinosternon abaxillare Baur in Stejneger, 1925 (Figs. 2N, 3H): restricted to the Grijalva River basin in the Central Depression and Plateau of Chiapas. 

Kinosternon acutum Gray, 1831 (Figs. 2O, 3H): from the Jamapa River (Ve) to the Champoton River (Ca) on the Gulf of Mexico versant, including the Papaloapan, Coatzacoalcos (both in Oa and Ve) and lower Grijalva Rivers (Ch), and Laguna de Terminos (Ca). Also found on the southern Yucatán peninsula (Ca and QR), northern Guatemala and Belize. 

Kinosternon creaseri Hartweg, 1934 (Figs. 2P, 3H): from the Champoton River (Ca) across the Yucatán peninsula (QR and Yu).

Kinosternon cruentatum Duméril and Bibron in Duméril and Duméril, 1851 (Figs. 2Q, 3I): from the Pánuco River (Ve) across the Tabasco lowlands to the entire Yucatán Peninsula on the Gulf of Mexico versant and into Guatemala and Belize.

Kinosternon flavescens Agassiz, 1857 (Figs. 2R, 3J): in southeastern Mexico it is restricted to the Panuco River basin (Ve) but ranges north across the Great Plains of the USA.

Kinosternon herrerai Stejneger, 1925 (Figs. 2S, 3K): from the Jamapa to the Panuco River (both in Ve) and northward on the Gulf of Mexico versant.

Kinosternon integrum Le Conte, 1854 (Figs. 2T, 3J): in southern Mexico from the Atoyac (Oa and Ve) and Tlapaneco River basins westward (Oa). 

Kinosternon leucostomum Duméril and Bibron in Duméril and Duméril, 1851 (Figs. 2U, 3K): from the Jamapa River (Ve) to the Champoton River (Ca) on the Gulf of Mexico versant, including the Usumacinta (Ca, Ch and Ta) and Lacantun rivers (Ch). Also found from Chetumal Bay through eastern Quintana Roo, and southward through Central America.

Kinosternon mexicanum Le Conte, 1854 (Figs. 2V, 3J): restricted to the Pacific versant from the Tehuantepec River (Oa) to the Suchiate River (Ch), and southeast to El Salvador.

Kinosternon oaxacae Berry and Iverson, 1980 (Figs. 2W, 3J): restricted to the Ometepec, La Arena, Colotepec and Copalita River basins on the Pacific versant in Oaxaca; also, westward into Guerrero.

Staurotypus salvinii Gray, 1864 (Figs. 2X, 3L): from the Copalita River (Oa) to the Suchiate River (Ch) on the Pacific versant, and southeast to El Salvador.

Staurotypus triporcatus (Wiegmann, 1828; Figs. 2Y, 3L): from the Jamapa River (Ve) to Campeche state on the Gulf of Mexico versant, including the Usumacinta (Ca, Ch and Ta) and Lacantun River (Ch). Also, in southern Quintana Roo to Chetumal Bay and into Guatemala, Belize and northwestern Honduras. Insertar fig 3:12cm

There was a wide range of conservation status for most of the native turtle taxa under national and international criteria. For example, the Mexican Government list (NOM-059 list; Semarnat, 2010) includes 16 species (64% of all turtle taxa found in southeastern Mexico), the IUCN Red List includes 18 (72%), and 20 are CITES listed (80%; Table 3). The turtles listed by NOM-059 and IUCN Red List as most threatened are D. mawii, C. angustatus, and those within the genus Terrapene (Table 3). However, the taxa whose conservation status is totally unknown includes all species in the genus Trachemys (Table 3). The average EDGE score for southeastern Mexican turtle taxa was 4.41 with a minimum value of 3.67 (K. creaseri, K. flavescens, and K. integrum), and a maximum of 7.15 (D. mawii) (Table 3).

Discussion

This is the first dichotomous key based on external characteristics to consider all native continental turtles that are distributed in southeastern Mexico, in accordance with advances in turtle taxonomy. Other dichotomous keys, although effective, are based on the review of internal characteristics that require the sacrifice of the organisms —e.g., for cranial measurements (Legler & Vogt, 2013). These criteria may not be useful when carrying out population ecology studies, or when required in forensic procedures, as for the identification of confiscated turtles. The inclusion of a Spanish translation may facilitate the work of early-career professionals and local authorities in the preparation of expert reports on seized specimens, contributing to a more accurate assessment of the extent of illegal trade affecting certain taxa. Generally, when there are national reports of seizures involving mud turtles, this is limited to filing a report at the genus level (Profepa, 2020).

According to our results, southeastern Mexico supports 3/4 of the families —and more than half of the genera— found nationwide in Mexico (Table 2). These findings highlight southeastern Mexico as a region of high importance for the composition of land and freshwater turtles at the national level. This fact is consistent with studies focused on analyzing the composition of the Mexican herpetofauna (Flores-Villela & García-Vazquez, 2014; Johnson et al., 2017; Ramírez-Bautista et al., 2023). In addition to this, Oaxaca, Chiapas, and Veracruz stand out as the states with the highest species richness and/or endemism, respectively. These 3 states are located within the region considered the richest in total herpetofauna, a result of complex orography, diverse habitats and environments, and the biogeographic history of Mexico (Ramírez-Bautista et al., 2023).

Previously published checklists of reptile diversity in Mexico often included taxonomic and distributional inconsistencies for turtles, possibly due to the disposition of the taxonomic status at that time (e.g., Flores-Villela & García-Vazquez, 2014; Hernández-Ordoñez et al., 2015; Johnson et al., 2015; Wilson et al., 2013). For example, Johnson et al. (2015) reported the presence of T. ornata in Chiapas, but according to the TTWG (2021, 2025) this species occurs only in western Mexico, from Culiacan, Sinaloa to Puerto Vallarta, Jalisco. Likewise, R. areolata and C. serpentina have been reported from the southeastern part of the Lacandona rainforest, Chiapas (Hernández-Ordoñez et al., 2015). However, experts agree that there is no evidence for native populations of R. areolata in that region (TTWG, 2021, 2025). Velázquez-Nucamendi et al. (2021) suggested that the records might involve animals transported from Tabasco to this region of Chiapas. Furthermore, the closely related C. serpentina and C. rossignonii are commonly confused in southeastern Mexico, despite the former species being found only in the United States and Canada (TTWG, 2021, 2025). 

It is important to note that the Berlandier’s tortoise (Testudinidae: Gopherus berlandieri) has been reported from the northern portion of Veracruz in recent checklists (Torres-Hernández et al., 2021; Vásquez-Cruz et al., 2021) and in virtual repositories (GBIF, 2024; iNaturalist, 2024; SNIB-Conabio, 2024). However, the inclusion of this turtle in these reports is not confirmed by collection data, and in the case of virtual repositories, it is based on individuals in captivity near the state border with Tamaulipas, where G. berlandieri is known to occur naturally. As no wild populations have been reported, and no wild individuals have been formally collected in the northern portion of Veracruz, we do not consider this species native to Veracruz. However, this issue needs to be addressed in the future to clarify the total richness of continental turtles in southeastern Mexico.

Southeastern Mexico has been categorized globally as an area with high to moderate endemism (Ennen et al., 2020). Our data indicates that this region contains 33% of the endemic continental turtle taxa at the national level within the genera Terrapene, Trachemys, Rhinoclemmys, and Kinosternon (Table 3). However, there are suggestions that in this region the probability remains high for potential new taxonomic discoveries or upgrades from subspecies to species, especially within Trachemys and Kinosternon, 2 genera that have been poorly studied in Mexico (Flores-Villela & García-Vázquez, 2014; Legler & Vogt, 2013). The T. venusta complex has historically presented many inconsistencies in its taxonomic relationships. Despite prominent color pattern differences among species, genetic divergences within this complex are shallow, and the taxonomic diversity of each species with several currently recognized subspecies could be overestimated (Fritz et al., 2011, 2023; Parham et al., 2013; Seidel & Ernst, 2017). Another scientific priority is to clarify the genetically distinct group of D. mawii located in the Papaloapan River in Veracruz (González-Porter et al., 2011), and into the Lacandona rainforest (Martínez Gómez et al., 2017). 

Historically, turtles in southeastern Mexico have been widely exploited at unsustainable rates, resulting in negative repercussions on their populations and pushing some species to the brink of near local extinctions (Legler & Vogt, 2013). Examples include C. angustatus and D. mawii, both recognized as most threatened by national criteria (Table 3). For the first species, in a study conducted in Lerdo de Tejada, Veracruz (Mexico), Espejel-González (2004) reported a capture of 254 individuals. However, due to the high rates of extraction per year (Espejel-González, 2004), Reynoso et al. (2016) found no individuals in the same locality. For D. mawii in the Lacandona rainforest (Chiapas), a systematic evaluation that started in the 1980s and concluded 20 years later inferred a reduction of ~ 80% of the native population in the area (Guichard-Romero, 2006; Legler & Vogt, 2013). Other current events that provide a glimpse of the crisis facing Mexican turtles include 2 trade confiscations in 2020. In just 2 seizures, approximately 30,000 Mexican turtles were confiscated, mainly Trachemys, Kinosternon, Claudius, and Staurotypus (Profepa, 2020; Excelsior, 2020). 

We found that D. mawii, T. mexicana, and T. yucatana were the only species in which their risk categories were consistent under national and international criteria. For the remainder of the turtles distributed in southeastern Mexico, these categorizations were inconsistent or nonexistent (Table 3). The genus Trachemys is the one that is not under any national or international protection criteria (Table 3). The absence of protection criteria does not indicate a lesser concern for the conservation of these turtles, but rather a potential neglect of an approach to diagnose the conservation status through their distribution, even though these turtles are highly demanded for local consumption and the illegal pet trade (Beauregard-Solís et al., 2010; Profepa, 2020; Velázquez-Nucamendi et al., 2021). One main problem for the conservation of turtles in Mexico is the lack of concordance between the lists issued by the national Government and those by international organizations (Macip-Ríos et al., 2015). This leads to confusion by the Mexican public administration regarding the data available for decisions related to management and permitting, especially for species poor studied and highly demanded as Trachemys and Kinosternon (Macip-Ríos et al., 2015; Profepa, 2020).

Mexico is an active country in the trade of wild species. Just in the period 2007-2011, Mexico was the second-largest exporter worldwide, with approximately 750,000 specimens of live reptiles removed, of which continental turtles stood out (Semarnat, 2012). Therefore, agreement between national and international standards is a high priority to conserve Mexican turtle species. More research and data are needed on least Rhinoclemmys, K. cruentatum, K. herrerai, K. leucostomum, K. oaxacae, K. mexicanum, and S. salvinii. The need for updates in national and international legal regulations is recognized as essential to the protection of the different species of turtles that are distributed in southeastern Mexico. We encourage the assessment of population trends and potential threats to provide a more comprehensive conservation status for these turtles under national and international criteria. 

The information provided in this work should help to improve and focus future research and conservation in southeastern Mexico. However, we recognize that more information is required on the population status of the turtles in each state to face the new challenges that we need to consider for their conservation. Indeed, addressing the remaining gaps in the distribution and systematics of certain turtle species would be a valuable avenue for future research. Continued efforts to enhance our understanding of these aspects will contribute to more accurate assessments of conservation status. Finally, we encourage the resolution of the discrepancies between international and Mexican conservation priorities to ensure the protection of the turtles that occur in this region. Aligning priorities will help create more unified and impactful strategies, ensuring better protection for these turtles and their habitats (Macip-Ríos et al., 2015). This underscores the importance of international collaboration and coordination to address conservation challenges comprehensively.

Acknowledgments 

Fieldwork was conducted under the Mexican Federal Government permit numbers: SGPA/DGVS/01156/19 and SGPA/DGVS/06570/21 issued by Semarnat. We thank the authorities of the Áreas Naturales y Vida Silvestre from SEMAHN for providing essential information on turtle locations; Carlos A. Guichard Romero and Antonio Ramirez for providing access to the ZooMAT facilities; Antonio Muñoz Alonso for providing access to the reptile collection from ECOSUR, and Anders G. J. Rhodin for providing all Mexican turtle localities from the Turtle Taxonomy Working Group’s distributional database (TTWG 2021, 2025). For photographs in Fig. 2, we thank Ernesto Eduardo Perera Trejo (A, general view and plastron), Julio Gonzalez (C, plastron), Mike Jones (D and P, general view and plastron), Taggert Butterfield (L plastron), Alejandra Monsivais (K general view and plastron), Antonio Ramírez (M, general view), and Erasmo Cázares (S, general view and plastron). Anders G. J. Rhodin, Peter Paul van Dijk, Oscar Flores-Villela, Taggert Butterfield, Jacobo Reyes-Velasco and Donald McKnight made important comments to improve this manuscript. We thank the Turtle Survival Alliance, Mohamed bin Zayed Species Conservation Fund (242536595), Turtle Conservation Fund, Chelonian Research Foundation (TCF-0790), and Turtle Taxonomy Fund for their support during field work and laboratory analysis. Finally, ERG is grateful to the scholarship “Becas de Preparación de Posgrado” from El Colegio de la Frontera Sur for support during the writing of this work.

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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.

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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. 

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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.

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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.

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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 

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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.

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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.

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