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Abundancia y diversidad de semillas dispersadas por el conejo castellano (Sylvilagus floridanus) en una reserva urbana de la Ciudad de México

Yury Glebskiy ^{a, b,} *, Zenón Cano-Santana ^a

a Universidad Nacional Autónoma de México, Facultad de Ciencias, Departamento de Ecología y Recursos Naturales, Laboratorio de Interacciones y Procesos Ecológicos, Circuito Exterior s/n, Ciudad Universitaria, 04510 Ciudad de México, Mexico

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

*Corresponding author: agloti@ciencias.unam.mx (Y. Glebskiy)

Received: 05 February 2025; accepted: 07 October 2025

Abstract

Lagomorphs are potentially important but understudied seed dispersers. In particular, there are no studies about the role of the Eastern Cottontail as a seed disperser. Therefore, the aim of this article is to evaluate the abundance and diversity of seeds dispersed by Sylvilagus floridanus in a conservation reserve within Mexico City. We collected fecal pellets during 2 periods, the highest seed production and the start of seed germination in the Reserva Ecológica del Pedregal de San Ángel. Pellets were subjected to different treatments to end seed dormancy (left in the field, stored in laboratory, and no treatment) and put to germinate in germination chambers and the field. We found that pellets left in the field had the most seeds germinating. Cottontails dispersed up to 0.77 seeds/g of excrete. A total of 15 species were observed, but the Chao estimator suggested that there were 29.8 species. Many of the dispersed seeds belong to rare species, most noticeable Jaegeria hirta. We conclude that cottontails are important dispersers due to the amount of excretes produced and the identity of the plants they disperse.

Keywords: Dormancy; Germination; Jaegeria hirta; Opuntia tomentosa;REPSA

Resumen

Los lagomorfos son dispersores de semillas potencialmente importantes, pero subestudiados. En particular, no existen estudios sobre el papel del conejo castellano como dispersor de semillas; por tanto, el objetivo de este artículo fue evaluar la abundancia y diversidad de semillas dispersadas por Sylvilagus floridanus en una reserva dentro de la Ciudad de México. Colectamos pastillas fecales durante 2 periodos, la temporada de mayor producción de semillas y el inicio de la germinación en la Reserva Ecológica del Pedregal de San Ángel. Las pastillas se sometieron a distintos tratamientos para terminar la dormancia (almacenar en el campo, en laboratorio y sin tratamiento) y fueron puestas a germinar en cámaras y en el campo. Encontramos que las excretas almacenadas en el campo tuvieron más semillas germinadas. Los conejos dispersaron hasta 0.77 semillas/g de excreta. Observamos 15 especies, pero el estimador de Chao sugirió que hubo 29.8 especies dispersadas. Muchas especies dispersadas son raras, en particular Jaegeria hirta. Concluimos que los conejos son importantes dispersores por la cantidad de excretas que producen y la identidad de las plantas diseminadas.

Palabras clave: Dormancia; Germinación; Jaegeria hirta; Opuntia tomentosa; REPSA

Introduction

There is a general consensus among ecologists that seed dispersal by animals is a very important service and that many plant species and even ecosystems could be dependent on this process (Gelmi-Candusso & Hämäläinen, 2019; Godó et al., 2022; Iluz, 2011). And there is an important amount of information on seed dispersal by birds, primates, and ungulates, among other groups (Albert et al., 2015; Beaune et al., 2013; Iluz, 2011); however, information on some other potentially important dispersers, particularly the lagomorphs, is scarce (Godó et al., 2022).

Lagomorphs are a widely distributed and abundant group of mammals that can be found across many ecosystems in all continents, except Antarctica (Chapman & Flux, 2008). Previous studies have shown that lagomorphs are not particularly important seed dispersers when compared to other animals by the number of seeds per gram of excrete (Borchert & Tyler, 2023; Malo & Suárez, 1995). However, they do disperse seeds, and given their abundance and the high amount of fecal matter they produce, they still have the potential to be important seed dispersers. Despite that, there are few studies that evaluate the role of lagomorphs as seed dispersers, and most of them used Oryctolagus cuniculus as the study model (Godó et al., 2022). Therefore, the aim of this study is to describe the diversity and abundance of seeds dispersed by endozoochory by the Eastern cottontail (Sylvilagus floridanus) in an urban reserve in Mexico City.

There are several studies about seed dispersal by the genus Sylvilagus, and they have found that species of this genus can be important seed dispersers of Opuntia (Borchert & Tyler, 2023) and Juniperus (Lezama-Delgado et al., 2016). At the same time, S. floridanus has a diverse diet (Chapman et al., 1980; Hudson et al., 2005). Therefore, our prediction was that Opuntia seeds would be common in excretes, and that the Eastern cottontail will disperse more species than previously reported for the genus. However, to our knowledge, this is the first publication that studies endozoochory by S. floridanus, which is quite surprising given that this is one of the most studied rabbits in North America.

Materials and methods

The Eastern cottontail inhabits a wide variety of environments ranging from deserts to rain forests from southern Canada to Venezuela (Chapman et al., 1980) and has been introduced to other territories like Italy (Rosin et al., 2008). This rabbit produces around 350 fecal pellets/day (Cochran & Stains, 1961), making it a potentially important seed disperser. Its diet consists mainly of grasses and herbaceous plants (Hudson et al., 2005), but it can switch to trees if its preferred food is scarce, for example, during the winter (Chapman et al., 1980). There are also reports of Eastern cottontails consuming fruits and seeds (Lorenzo & Cervantes, 2005); thus, it is a generalist herbivore.

We performed this study in the Reserva Ecológica del Pedregal de San Ángel located in Mexico City (19°18’55” N, 99°11’32” W). The reserve is dominated by a xerophytic scrub with a mean precipitation of 752 mm and an average annual temperature of 18.2 °C (Rzedowski, 1954; SMN, 2025). The reserve has 2 seasons, the wet (from May to October) and the dry (from November to April), and most seeds are only able to germinate during the wet period (Rzedowski, 1954). There is only 1 species of rabbit, S. floridanus, found in this reserve (Hortelano-Moncada et al., 2009).

We collected excretes of S. floridanus twice, the first collection between October 28 and 30, 2016 in 4 locations separated by at least 100 m (we used different locations to capture the variability of the reserve, and it is not the purpose of this study to compare between locations, and after collection, pellets from different locations were mixed together). The second collection was made between May 17 and 22, 2017. We chose those dates because the October collection represents the point of highest seed production in the ecosystem (Cesar-García, 2002) and therefore probably the greatest amount of seeds per excrete, and the second because it’s the beginning of the rainy season and thus germination. After collection, we cleaned the pellets from possible additions of seeds by sieving. The method resulted effective since we observed seeds of Muhlenbergia robusta (Poaceae) fall on the collected pellets, but that plant did not appear in our experiment suggesting, that we were able to get rid of seeds added after defecation.

We performed 2 germination experiments, and the purpose of the first was to determine how many seeds can germinate immediately after the October collection and to compare methods of germination. In the field we observed that fecal pellets could be found entire or disintegrated and could be laying on soil or on rock; therefore, we used 4 treatments: 1) entire pellets in sterilized soil (we sterilized the soil to kill all possible seeds by microwaving before adding the pellets); 2) disintegrated pellets in sterilized soil; 3) entire pellets with no soil, and 4) disintegrated pellets with no soil. This also allowed us to determine the best germination method for the second phase of the experiment. For each treatment we used 1,000 fecal pellets divided among 10 trays. All treatments were put in germination chambers with 12/12 light/dark periods at 25 °C during 3 months. We used the Kruskal-Wallis and post hoc Dunn tests to compare the number of germinated seeds between treatments (using trays as replicas) and calculated the number of seeds per gram of excrete to facilitate comparison with other species.

The purpose of the second germination period was to determine how many seeds can germinate from the October pellets after being stored in different conditions and the pellets collected in May with no storage, in germination chambers, and in the field. In our study location, seeds that are dropped in October cannot germinate in normal field conditions because there is almost no rain, and most seeds in xerophytic shrubs have some type of dormancy to avoid germinating before the rainy season (85% of the seeds have dormancy, according to Baskin and Baskin [2014]). Therefore, we tested 2 methods of pellet storage: laboratory conditions, pellets were dried and stored at room temperature with no exposure to sun. And in the field, pellets were dropped in the field in a location with no rabbits and recollected in May. At the same time, we wanted to test if seeds germinate the same in laboratory and in field conditions; therefore, we put disintegrated pellets in sterilized soil (based on the result of the first experiment) using pellets collected in October and kept in the laboratory, pellets collected in October and kept in the field, and pellets collected in May with no storage in germination chambers (with the same conditions as the previous experiment, we inspected and watered those treatments 3 times a week during 3 months) and in the field (Table 1). The field experiment used the same sterilized soil, but the trays were higher to allow plants to grow and were covered by fabric with 0.04 mm openings to prevent seed addition from the exterior. In this case, the trays were left in the field, and no watering or other treatment was performed. For these experiments we only considered vascular plants. We inspected the field treatments once every week for 3 months. We used Kruskal-Wallis and Dunn tests to compare between treatments (including the disintegrated pellets in the soil treatment from the first experiment) and the Chao estimator for the species richness to estimate the number of species that are dispersed but did not appear in our study.

Results

In the first experiment, we observed the germination of 1.4 ± s.d. 1.3 seeds/100 pellets in the disintegrated pellets in soil treatment, 1.0 ± 0.8 seeds/100 pellets in the entire pellets in soil treatment, and 0.1 ± 0.3 seeds in both treatments with no soil. The Kruskal-Wallis test showed that there are differences between the treatments (p < 0.05), and according to the Dunn test, there are differences between treatments with and without soil but no differences between disintegrated and entire pellets. During this stage we observed 4 morphologically distinctive plants, but they all died early and could not be identified. The main reason plants could not develop was that all pellets were being actively degraded by fungi, which ultimately killed all emerging plants. We also observed that in the treatments with no soil, it was hard to maintain the adequate humidity of the substrate.

In the second experiment, the Kruskal-Wallis test also showed differences between groups (p < 0.05), and according to the Dunn test, the pellets collected in October and left in the field (both the germination cameras and the field) had significantly more seeds germinating from them (Fig. 1, Table 1). Cottontail excretes contained between 1.4 and 8.8 seeds/100 pellets, which equals to 0.12 and 0.77 seeds/g of excrete (considering that the weight of an excrete is 0.115, according to Glebskiy [2016]). We observed 15 species of dispersed seeds, and according to the Chao estimator, there are 29.8 species dispersed (with a 95% confidence interval of ± 13.4). The most common group of dispersed seeds was the Poaceae family (34.5% of all seeds), followed by Opuntia tomentosa (25.9%), Physalis glutinosa (16.4%), and Jaegeria hirta (12.7%). The Poaceae family was composed of Aegopogon tenellus, Eragrostis Mexicana, and Chloris gayana; however, due to their similarities in the initial stages and that some of the plants died, we were unable to determine the exact number of plants for each species (Table 1).

Discussion

The first experiment showed that seeds from both entire and disintegrated pellets can germinate equally well. We used disintegrated pellets in the following experiments because they are easier to homogeneously disperse in the experiment tray. However, germination was very low in the experiments with no soil. This suggests that if the pellets are placed on soil, the seeds inside are able to germinate, but if the cottontail forms a latrine on a rock or some other hard object (as it is commonly observed in our study location; pers. obs.), the pellets are not a good substrate for the plants to develop (at least in the fresh state). An interesting observation that we made was that in the October germination experiment, fungi were an important problem for plant development, but the same did not happen in the following experiment. This could be due to the fact that July-October are the months when most fungi expel their spores and infect the pellets (Valenzuela et al., 2009), but they apparently (at least partially) die before the germination period and by May do not represent an important threat for seeds or seedlings. Therefore, fungi are unlikely to strongly affect the process of seed dispersion by cottontails, since our October germination experiment would never happen in field conditions because of the dry season.

Baskin and Baskin (2014) mention that in xerophitic scrubs, 85% of seeds have some sort of dormancy; this is close to the results of our experiment. If we compare the number of seeds germinated from pellets stored in laboratory and field conditions, we can see that pellets exposed to the field yielded 5.9 (in germination chambers) and 2.9 (in the field) times more plants (Fig. 1). This suggests that most seeds have some sort of dormancy that is broken by the conditions in the field, most likely by heat, as it was shown for Opuntia tomentosa (Olvera-Carrillo et al., 2003). Notice that the Opuntia seeds almost never germinate after being stored in laboratory conditions (Table 1). 

Table 1

Number and identity of the seeds germinated per 1,000 fecal pellets in each treatment. Chao estimator ± 95% confidence interval.

¹Includes: Aegopogon tenellus, Eragrostis Mexicana, and Chloris gayana (the last one is the only exotic species).

The Eastern cottontails showed to be poor seed dispersers if considering the amount of seeds per gram of excretes, 0.77 under the best conditions, compared with the 7.13 seeds/g of excrete dispersed by ringtails in the same location (Peña-Herrera et al., 2024). However, cottontails produce around 350 pellets/day (Cochran & Stains, 1961), which at a weight of 0.115 g/pellet (Glebskiy, 2016) which equals 40 g of excretes and thus up to 31 seeds dispersed per day per cottontail (and their population can rise up to 14 individuals/ha (Glebskiy, 2016). Another important consideration is the identity of the seeds, from the 14 species that we were able to identify; only 2 (Opuntia tomentosa and Buddleja cordata) could be considered dominant in the region (according to the list provided by Cano-Santana [1994]), and the other species are less common or even rare. Most noticeable Jaegeria hirta, which composes 12.7% of all seeds found and is a native but rare species for the location. It has to be noted that of the dispersed species (Table 1), only Chloris gayana is exotic to the location. When comparing to the seeds dispersed by ringtails in the same location (Peña-Herrera et al., 2024), we can see that only 3 species are shared (Opuntia tomentosa, Drymaria laxiflora, and Bidens sp.) and cottontails tend to disperse more Poaceae plants. This suggests that ringtails and rabbits have a complementary role as seed dispersers.

Therefore, we conclude that while being poor dispersers of seeds/g of excrete (the most commonly used estimator to measure dispersion efficiency), cottontails compensate for this by the sheer amount of excretes produced, their high population density, and the fact that they disperse mostly uncommon or even rare plants, and most are native to the region. Thus, cottontails are important seed dispersers and can have a great effect on some rare plants, especially Jaegeria hirta.

Acknowledgements

We are thankful to Díaz Rico A. and Zúñiga Ruíz B. for allowing us to use their germination chambers, Martínez Orea Y. for the plant identification, SEREPSA working team for the permits to collect pellets, List Sánches R. and Godínez Álvarez H. for their useful comments on this project, and Castellanos Vargas I. for technical support. This project was financially supported by PAPIIT grant IV200117 “Análisis ecosocial de una reserva urbana para la sustentabilidad en el campus de Ciudad Universitaria” to ZCS and a scholarship by Conacyt 817316 to YG.

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Vascular epiphyte community of an inland mangrove of Tabasco: composition and similarity with coastal mangroves and adjacent tropical vegetation

Comunidad epífita vascular de un manglar interior de Tabasco: composición y similitud con manglares costeros y vegetación tropical adyacente

Neil Ebeth Meled Morales-Rodríguez ^a, *, Carlos Manuel Burelo-Ramos ^a, José G. García-Franco ^b, Octavio Aburto-Oropeza ^c y María Eugenia Molina-Paniagua ^a

a Universidad Juárez Autónoma de Tabasco, Laboratorio de Manglares Interiores, Carretera Villahermosa-Cárdenas Km. 0.5 s/n, Entronque a Bosques de Saloya, 86150 Villahermosa, Tabasco, Mexico

b Instituto de Ecología, Carretera antigua a Coatepec #351, Col. El Haya, 91073 Xalapa, Veracruz, Mexico 

c Scripps Institution of Oceanography, 9500 Gilman Drive, La Jolla, California 92093, USA

*Corresponding author: nemmr@hotmail.com (N.E.M. Morales-Rodríguez)

Received: 13 December 2024; accepted: 23 October 2025

Abstract

El Cacahuate Lagoon, Tabasco, Mexico, is located 170 km from the current coastline and contains an inland mangrove ecosystem, surrounded by remnants of tropical forest. This inland mangrove is the habitat of an epiphyte community whose species composition and relationship with other epiphyte communities are unknown. This study describes the composition of vascular epiphytes associated with this inland mangrove, evaluates their similarity to epiphyte communities in coastal mangroves and adjacent vegetation within a 220 km radius of the study site, using the Jaccard Index and floristic turnover with β-diversity. We hypothesize that the similarity in the composition of the epiphytes of the inland mangrove should be greater with that of nearby forests than with coastal mangroves, since the seeds of forest epiphytes can easily reach the inland mangrove. The epiphyte community of the Cacahuate mangrove comprises 27 species and is more similar to the epiphyte communities of the coastal mangroves of Tabasco. This affinity could be related to the Pleistocene isolation of this mangrove, or to the long-distance dispersal of epiphytes from coastal mangroves.

Keywords: Biodiversity; Floristics; Red mangrove; Rhizophora mangle; Wanha’ Biosphere Reserve

Resumen

La laguna El Cacahuate, Tabasco, México, se localiza a 170 km de la línea costera actual y contiene un ecosistema de manglar interior, rodeado de remanentes de bosque tropical. Este manglar interior es el hábitat de una comunidad epífita cuya composición de especies y su relación con otras comunidades epífitas se desconocen. El presente estudio describe la composición de epífitas vasculares asociadas con este manglar interior, evalúa su similitud con las comunidades epífitas de los manglares costeros y vegetación adyacente en un radio de 220 km del lugar de estudio, utilizando el índice de Jaccard y su recambio florístico con la diversidad ß. Hipotetizamos que la similitud en la composición de las epífitas del manglar interior debería ser mayor con la de los bosques cercanos que con los manglares costeros, ya que las semillas de las epífitas de los bosques pueden llegar fácilmente al manglar interior. La comunidad epífita del manglar del Cacahuate comprende 27 especies y presenta una mayor similitud con las comunidades epífitas de los manglares costeros de Tabasco. Esta afinidad podría estar relacionada con el aislamiento pleistocénico de este manglar, o con la dispersión a larga distancia de las epífitas provenientes de los manglares costeros.

Palabras clave: Biodiversidad; Florística; Mangle rojo; Rhizophora mangle; Reserva de la Biosfera Wanha’

Introduction

Vascular epiphytic plants (henceforth epiphytes) constitute a functional group that develops on woody species. Unlike parasitic plants, epiphytes obtain water and nutrients from the atmosphere, precipitation, and decomposing organic material, rather than relying physiologically on the host (Krömer & Gradstein, 2016). Within epiphytes, 2 main categories are recognized: true epiphytes, which complete their entire life cycle on the host without producing roots that reach the soil, and hemiepiphytes, which in contrast, exhibit a mixed life cycle, since some germinate on the host and later develop roots that reach the ground (primary hemiepiphytes), whereas others begin their growth in the soil and, as they ascend, establish themselves on the host (secondary hemiepiphytes) (Granados-Sánchez et al., 2003; Zotz, 2016). Epiphytes comprise about 10% of the known plant species worldwide (Zotz et al., 2021). In the Neotropics, epiphytes significantly contribute to the overall diversity of the vegetation, as they can represent up to 50% of the vascular flora in some forests (Carmona-Higuita et al., 2025; Kelly et al., 2004; Taylor et al., 1986). Tree species in the low and mountain forests have different structural characteristics (e.g., greater height, dense canopy, and great diversity of bark textures), which combined with particular environmental conditions (e.g., high humidity), allow the presence of a high number of epiphytic species (Ceja-Romero et al., 2008; Flores-Palacios & García-Franco, 2006; Hietz & Hietz, 1995; Krömer et al., 2007, 2014; Martínez-Meléndez et al., 2011; Rzedowski, 1996). In contrast, mangrove forests generally show a low richness of epiphytes (Benzing, 1990; Carmona-Díaz et al., 2014; Zotz & Reuter, 2009; Zimmerman & Olmsted, 1992), which can be attributed to reduced tree diversity and consequently to low structural complexity of the habitat, but mainly due to environmental stress conditions such as the strong winds, waves, and high salinity present in coastal zones (Gómez & Winker, 1991; Jiménez-López et al., 2017; Zotz & Reuter, 2009). However, epiphytes are frequent in mangrove ecosystems, as several species have been recorded in different studies even though the objectives and sampling efforts are directed toward tree species, which are the dominant physiognomic elements (Aksornkoae, 1993; Cach-Pérez et al., 2013; Carmona-Díaz et al., 2014; De Sousa & Colpo, 2017; García-Luna et al 2024; Jiménez-López et al., 2018; Kupec, 2018; Noguera-Savelli et al., 2021; Rahman et al., 2015; Rohani et al., 2020).

Mangrove ecosystems are primarily distributed in tropical and subtropical regions, generally associated with the coast and brackish water bodies (Leal & Spalding, 2021). However, mangrove ecosystems also have been recorded in freshwater wetlands, away from marine influence, known as inland mangroves. The inland mangroves have been reported in many countries worldwide, such as in Australia, Antigua and Barbuda, the Bahamas, Indonesia, and Pakistan, located 15 to 50 km from the coast, and between 6 and 37 m above sea level (Lugo, 1981; Patel, 2014; Patel & Agoramoorthy, 2012; Stoddart et al., 1973; Taylor, 1986; Tripathi et al., 2013; Woodroffe, 1988). 

Recently, in Mexico, individuals of Rhizophora mangle, along with another 112 coastal affinity species were reported along the banks of the San Pedro Mártir River and El Cacahuate Lagoon in Tabasco, the latter located almost on the border with Guatemala (Aburto-Oropeza et al., 2021). The presence of this inland mangrove is attributed to the global climatic phenomenon that occurred about 120,000 years ago when an increase in global temperatures caused a rise in sea levels, displacing the coastline inland (Aburto-Oropeza et al., 2021). As the planet cooled, the sea retreated to its current position, leaving mangrove trees dispersed along the riverbanks and creating an isolated mangrove ecosystem in the El Cacahuate Lagoon, 170 km from the Tabasco coast (Aburto-Oropeza et al., 2021).

Currently, the El Cacahuate Lagoon is surrounded by a matrix composed of remnants of evergreen tropical forest belonging to the “Cañón del Usumacinta” Flora and Fauna Protection Zone (Conanp, 2015), fragments of several types of tropical forest, and large areas of land used for livestock and agriculture activities. However, despite this mixed landscape, the hydrophytic vegetation surrounding the water body restricts access to the mangrove, which has resulted in minimal human impact. El Cacahuate mangrove is considered a relict area from the Pleistocene and a refuge for biodiversity due to its high degree of conservation (Aburto-Oropeza et al., 2021). This area together with the adjacent forest areas forms part of a core area of the recently designated Wanha’ Biosphere Reserve (Conanp, 2023a; Semarnat, 2023).

Preliminary surveys indicate the presence of several species of epiphytes along the upper San Pedro River (Aburto-Oropeza et al., 2021). However, in El Cacahuate mangrove the epiphyte species composition and its species similarities to the epiphytic communities of the surrounding vegetation or to the coastal mangroves of Gulf of Mexico are unknown. High epiphyte composition similarity with tropical forest would indicate processes of colonization after the sea retired, while high epiphyte composition with coastal mangroves communities should indicate that species arrived together with the mangrove during the interglacial period.

The aims of this study were to determine the richness and composition of the epiphyte community present in the inland mangrove of El Cacahuate Lagoon, and to assess the floristic similarity of the epiphytes of El Cacahuate with coastal mangroves and adjacent tropical forests. We expect that, given the inland Cacahuate mangrove’s location in a freshwater environment and its proximity to tropical forest areas, the similarity of the epiphyte community should be greater than that of the nearest terrestrial vegetation because the seeds of the epiphytes can likely reach the mangrove trees easily.

Materials and methods

The study was conducted in the El Cacahuate Lagoon, located in the “Sueños de Oro” rural community of the Tenosique Municipality, Tabasco State, Mexico (Fig. 1). It is a lentic water body associated with the sub-basin of the San Pedro Mártir River, situated 170 km in a straight line to the coast and over 300 km following the river’s course (17°17’58.949” N, 91°5’13.09” W, elevation 45 m asl). The region has a warm-humid climate with abundant rainfall in the summer (Aceves-Navarro & Rivera-Hernández, 2019). The average temperature is 27 °C, and the average annual precipitation is 2,264 mm, with September being the rainiest month (391 mm) and March the driest (54 mm) (Conanp, 2023a). The lagoon area is approximately 13.7 ha and reaches a depth of up to 24 m. The soils surrounding the lagoon are clayey loam and gleysol (Conanp, 2023a; Palma-López et al., 2017). In the mangrove, there is a surface layer of leaf litter 15 to 40 cm deep, followed by the mineralization of organic matter.

The vegetation present in the lagoon and around it consists of floodable grassland (60%), aquatic vegetation (15%), and mangrove (25%) (Conanp, 2023a). The floodable grasslands are primarily composed of Hydrocotyle umbellata L. (Araliaceae), Eleocharis interstincta (Vahl) Roem. & Schult. (Cyperaceae), Cladium jamaicense Crantz (Cyperaceae), Acrostichum danaeifolium Langsd. & Fisch. (Pteridaceae), and Bletia purpurea (Lam.) DC (Orchidaceae). The aquatic vegetation includes rooted hydrophytes with floating leaves such as H. umbellata and Nymphaea ampla (Salisb.) DC. (Nymphaeaceae), free-floating hydrophytes like Salvinia auriculata Aubl. (Salvinaceae), and submerged free-floating hydrophytes like Cabomba palaeformis Fassett (Cabombaceae), Utricularia foliosa L., and U. purpurea Walter (Lentibulariaceae). The mangrove is in the southwest part of the lagoon, comprising 7 ha of continuous vegetation. In the mangrove vegetation, R. mangle is the most abundant tree species, with rare occurrences of Bucida buceras L. (Combretaceae), Chrysobalanus icaco L. (Chrysobalanaceae), Haematoxylum campechianum L. (Fabaceae), and Pachira aquatica Aubl. (Malvaceae). Additionally, other species are rarely present such as Vanilla insignis (Orchidaceae), Acoelorraphe wrightii (Griseb. & H.Wendl.) H.Wendl. ex Becc. (Arecaceae), Anthurium schlechtendalii Kunth subsp. schlechtendalii (Araceae), Monstera tuberculata Lundell, and Philodendron radiatum Schott. (Araceae). 

Fieldwork was conducted from April 2022 to February 2023. The recording of epiphytes in mangrove vegetation was carried out in 10 rectangular plots of 75 m long by 20 m wide. Plots were oriented perpendicular from the edge of the lagoon to inland spaced 40 m from each other (1,500 m² per plot, 15,000 m² in total; Fig. 1). This design aimed to include as much as possible of the total epiphytic composition present in the mangrove. As R. mangle is the dominant tree species in this mangrove, the recording of epiphyte species focused exclusively on it. Within the sampling plots, we recorded all epiphyte species present on each individual R. mangle tree, excluding hemiepiphytes and parasitic plants. Voucher specimens were collected following standardized methods by Lot and Chiang (1986) and Krömer and Gradstein (2016). For less abundant species, photographic records were obtained instead. All herbarium specimens were deposited in the UJAT herbarium (acronym following Thiers, 2021), and the photographs were stored in the photo archive of the Biological Sciences Division-UJAT.

The identification of the species was carried out with the support of taxonomic keys and specialized literature for the families Bromeliaceae, Cactaceae, and Orchidaceae (Alderete-Chávez & Capello-García, 1988; Ames & Correll, 1985; Beutelspacher, 2011; Campos-Díaz et al., 2020; Conap, 2010; Davidse et al., 1994; Espejo-Serna et al., 2004; Hágsater et al., 2005; Hietz & Hietz-Seifert, 1994; Martínez-Meléndez et al., 2011; Mondragón-Chaparro et al., 2011; Noguera-Savelli & Cetzal-Ix, 2014), as well as Aspleniaceae, Polypodiaceae, and Pteridaceae (Mickel & Smith, 2004). For species identification, original descriptions were reviewed in the Biodiversity Heritage Library (BHL, 2022). Additionally, to determine the conservation status of the recorded epiphyte species in the study area, we consulted the official Mexican environmental protection and species legislation NOM-059-Semarnat-2010 (Semarnat, 2010) and the Red List of Threatened Species by the International Union for Conservation of Nature (IUCN, 2021). 

To determine similarities between the epiphyte species composition of the inland mangrove of El Cacahuate (IM-Cacahuate) and other epiphyte communities, available epiphyte floristic lists from various vegetation types were compiled within a 220 km radius starting from the study area, including sites in Mexico and Guatemala (Fig. 2). Radius length corresponds to the straight-lined distance between El Cacahuate Lagoon and the nearest coastal mangroves of Tabasco, Mexico. It is important to note that most of the studies reviewed were conducted with objectives and sampling efforts not specific to epiphytes, so only the epiphyte species reported were considered (excluding hemiepiphytes).

For the Mexican portion, the compiled lists correspond to coastal mangroves (CM-Paraíso: including localities of Cárdenas, Centla, Comalcalco, Paraíso, Tabasco; Díaz-Jiménez, 2007. CM-Centla: Centla, Tabasco; Jiménez-López et al., 2017, 2018. CM-Nohan: UMA Nohan, Cd. del Carmen, Campeche; Noguera-Savelli et al., 2021); high evergreen tropical forest (HETF-Tenosique: Tenosique, Tabasco, Hernández-Sastré et al., 2014); medium evergreen tropical forest (METF-Macuspana: Macuspana, Tabasco; López-Gómez, 2014; METF-Tenosique: Tenosique, Tabasco; Morales-Damián, 2012); medium subevergreen tropical forest (MSTF-Catazaja: Catazajá, Chiapas; Gutiérrez-Báez, 2004); and tropical dry forest (TDF-Tenosique: Tenosique, Tabasco; Morales-Damián, 2012). Additionally, the riparian flora list of the San Pedro Mártir River was included, which comprises epiphyte records in high, medium, and low evergreen tropical forests with the presence of R. mangle individuals in the riparian vegetation (TF&IM-San Pedro Mártir, Aburto-Oropeza et al., 2021). There are floristic lists that report the presence of epiphyte species for the Calakmul Biosphere Reserve, Campeche, (Conanp, 2023b; Martínez et al., 2001), which were not integrated into the database because this site belongs to the biotic province Yucatán Peninsula (Conanp, 2023b; García-Gil et al., 2002), which reports greater floristic affinity with the districts within the Yucatán Peninsula, Guatemala, and Belize (Duno-de Stefano et al., 2012) and the states of Chiapas, Oaxaca, and Veracruz (Ibarra-Manríquez et al., 2002; Morrone, 2019). 

In Guatemalan territory, only 2 floristic lists within the established distance for the analysis were obtained: one from a disturbed high evergreen tropical forest (TF-Tikal, Hellmuth & D’Angelo-Jerez, 2022), and the second from a high evergreen tropical forest combined with R. mangle from the El Petén area (TF&IM-Peten, Conap, 2010). Appendix presents the list of the recorded species in the present study and the species compiled from the reviewed studies. The classification of the types of vegetation is based on the proposal of Conabio (2013, 2019) for Chiapas and Tabasco, Mexico, and by Melgar (2003) and Conap (2010) for Tikal and El Petén, Guatemala.

A presence-absence data base was constructed, based on the epiphyte species recorded in our study area and the epiphyte species documented from the surrounding sites obtained of literature. The nomenclature was updated and standardized using the electronic database Tropicos (Tropicos, 2023). Subsequently, the similarity between epiphyte communities of the different vegetation types and locations was explored using the data matrix in a hierarchical clustering analysis (UPGMA) based on the Jaccard similarity index (JSI). This index was selected as it uses species presence-absence data, which was the type of data obtained from the reviewed studies. The measure of similarity ranges from 0% (not similar) to 100% (the most similar). Finally, a beta diversity analysis was performed using Cody’s index (Ci) to assess species turnover between communities. If a high index is obtained, it means that the sites are very different, while a low index means that they share most of their species. Both analyses were conducted using the program Past 4.12b (Hammer et al., 2001).

Results

A total of 6 families, 18 genera, and 27 species of epiphytes were recorded (Table 1)in El Cacahuate mangrove, with Orchidaceae and Bromeliaceae being the families with the highest number of species (11 and 10, respectively), followed by Cactaceae and Polypodiaceae (2 species each) and Aspleniaceae and Pteridaceae (1 species each; Fig. 3). The genera with the most species were Tillandsia (Bromeliaceae) with 8 species, and Epidendrum (Orchidaceae) with 3. Among the epiphyte species recorded in El Cacahuate, Asplenium serratum L. is listed as a threatened species under Mexican legislation (Semarnat, 2010), while Tillandsia fasciculata Sw. and Selenicereus grandiflorus (L.) Briton & Rose are cited on the Red List of Threatened Species by IUCN (2021) as species of least concern.

Table 1

List of epiphyte species associated with the mangrove of El Cacahuate Lagoon, Tenosique, Tabasco, Mexico. *New records for the Wanha’ Biosphere Reserve.

Similarities between epiphyte communities. The present study and the review of published studies within the selected surrounding area allowed for the compilation of a total of 119 epiphyte species from sites with coastal mangrove, inland mangrove, tropical forests, and disturbed forests (Appendix). The sites with the highest number of epiphyte species were the high evergreen tropical forest of Tenosique (HETF-Teno, 53 species), the riparian vegetation of the San Pedro River (TF&IM-SPMR, 52 species), the medium evergreen tropical forest of Macuspana (METF-Macus, 45 species), the inland mangrove of El Cacahuate Lagoon (IM-Cac, 27 species), and the coastal mangrove of Centla (CM-Centla, 25 species). In the remaining sites, the number of epiphyte species ranged from 4 to 16, with 14 species recorded in the coastal mangroves of Nohan and Paraíso (CM-Nohan, CM-Paraíso; Appendix).

The clustering analysis (Fig. 4) clearly separated 4 groups (at a similarity level of 0.14). Two groups consisted of a single location: the first being the disturbed evergreen tropical forest of Tikal (TF-Tikal) and the second, the medium subevergreen tropical forest of Catazaja, Chiapas (MSTF-Catazaja). The other 2 groups contained several locations. The first group was made up of different forest types in Tabasco (HETF-Tenosique, METF-Macuspana, TDF-Tenosique, METF-Tenosique), while the second group included sites with coastal mangroves (CM-Nohan, CM-Paraíso, CM-Centla) and tropical forest and inland mangrove vegetation (TF&IM-San Pedro Mártir, TF&IM-Peten, IM-Cacahuate). In this latter group, the inland mangrove of El Cacahuate showed greater similarity in the epiphyte species with the coastal mangroves of Centla (JSI = 0.45, 16 shared species) and Paraíso (JSI = 0.38, 11 shared species), despite being 194 and 220 km away from El Cacahuate, respectively. The tropical forest and mangrove vegetation of the San Pedro River shared a greater number of species (19) with the El Cacahuate mangrove, but the similarity was slightly lower (JSI = 0.23), although the distance between these sites is lower, 59 km. The next ecosystem is the forest with inland mangrove of El Petén, sharing 8 species with El Cacahuate and showing a lower similarity than the previous groups (JSI = 0.18). At last, the coastal mangrove of Nohan, Campeche shared 7 species with El Cacahuate, with the lower similarity inner this group (JSI = 0.15). 

Among all groups, the lowest similarity of the epiphyte community of El Cacahuate was with the medium subevergreen tropical forest of Catazaja (JSI = 0.05) and the disturbed evergreen tropical forest of Tikal (JSI = 0.03), with 2 and 1 species in common, respectively; both located over 100 km from El Cacahuate Lagoon. Among sites with mangrove vegetation, beta diversity analysis (Table 2) shows that the inland mangrove of El Cacahuate presents low species turnover with the coastal mangroves (Centla and Paraíso; Ci= 10 and 9.5, respectively). In contrast, species turnover is higher with the riparian forest and mangrove vegetation of the San Pedro Mártir River (Ci= 19). 

Discussion

As far as we know, our study is the first to be conducted on epiphytic species of inland mangroves in El Cacahuate Lagoon. The epiphyte community of El Cacahuate Lagoon, with 27 records species, is among the richest ever reported in a mangrove ecosystem. Previous studies have reported the presence of fewer species in coastal mangroves (De Sousa & Colpo, 2017; Díaz-Jiménez, 2007; Jiménez-López et al., 2017, 2018; Menéndez-Liguori, 1976; Noguera-Savelli et al., 2021; Rohani et al., 2020). However, it is true that many of these studies did not involve extensive sampling, or they were not specifically focused on epiphyte species. Jiménez-López et al. (2017, 2018), in the mangrove of El Cometa Lagoon, Centla, Tabasco, were specifically focused on epiphytes, recording 25 species. In contrast, the tropical forest sites of Tenosique and Macuspana (Hernández-Sastré et al., 2014; López-Gómez, 2014; Morales-Damián, 2012), and the riparian forest and mangrove of San Pedro Mártir, Tabasco (Aburto-Oropeza et al., 2021), have a higher reported number of epiphyte species than the mangrove of El Cacahuate. However, these differences in the number of species reported are because the forests of Tenosique, Macuspana, and the San Pedro Mártir River were collected in larger areas of vegetation, a greater number of phorophyte species were sampled, and different sampling methods were used. For example: A) in the forests of Tenosique (Morales-Damián, 2012; Hernández-Sastré et al., 2014) sampled 25 × 25 m plots, recording the epiphytes associated with 9 species of phorophytes; B) in the Macuspana forest (López-Gómez, 2014), a representative sampling method of 1 ha was used, sampling epiphytes in 8 plots of 20 × 20 m (400 m²), considering both trees and shrubs present; and finally C) on the San Pedro Mártir River (Aburto-Oropeza et al., 2021), targeted sampling was carried out between 2014 and 2015 with sporadic collections until 2019, covering more than 25 linear km of river and sampling more than 30 species of phorophytes (Burelo-Ramos pers. com.). This shows that floristic lists targeting forests tend to have higher reports of epiphytes than mangrove ecosystems. 

Table 2

Beta-diversity of epiphytes between the inland mangrove of El Cacahuate Lagoon and epiphyte floristic lists of surrounding tropical forest and coastal mangroves. Values above the diagonal represent Cody’s index for each pairwise comparison. Values below the diagonal indicate the number of shared species between sites. The top row displays the total species richness for each location. The first column lists the number of species unique to each site. Site acronyms are defined in the Materials and methods section.

The low richness of epiphytes in coastal mangroves has been associated with the adverse environmental conditions present, such as high temperatures, low precipitation, and excess salinity (Benzing, 1990; Carmona-Díaz et al., 2014; García-Luna et al., 2024; Gómez & Winker, 1991; Zimmerman & Olmsted, 1992; Zotz & Reuter, 2009). Mangrove trees eliminate excess salt through their leaves (Mikolaev et al., 2016; Zotz & Reuter, 2009), so large amounts of salt could be accumulating in some epiphytes (e.g., orchids and bromeliads) due to leaf litter and rainwater falling from the canopy, which is captured in the roots and the rosette leaves of these plants. Salt decreases the osmotic potential of epiphyte cells, reducing their survival by promoting tissue necrosis and leaf loss, especially for species that do not have adaptations to survive under extreme water stress conditions, v.gr., xerophytic habits (Benzing, 2000; Du & Hesp, 2020; Zotz & Reuter, 2009). However, Gómez and Winkler (1991) have pointed out a contrary position suggesting that the high precipitation in some coastal areas may dilute the high salinity that falls from the mangrove’s canopy, allowing for the existence of non-xerophytic epiphytes. Nevertheless, the low presence of epiphyte species in mangrove ecosystems suggests that the physiological limitations in many of these plants may be significant (Cach-Pérez et al., 2018). Considering the distribution of mangroves worldwide, more floristic studies are needed in this ecosystem to identify patterns in other epiphytes species numbers, physiological traits, and functional groups.

The mangrove of El Cacahuate Lagoon presents a less stressful environment compared to coastal mangroves, as it is in a freshwater body with high precipitation (annual average of 2,300 mm) and warm temperatures (annual average of 26 °C) (Aceves-Navarro & Rivera-Hernández, 2019). In coastal mangroves, which are characterized as saline ecosystems (Feller et al., 2010), R. mangle eliminates the excess of salt absorbed by its roots through lenticels on its leaves (Bento et al., 2024). However, although El Cacahuate Lagoon is a freshwater aquatic system (0.4 psu) compared to nearby coastal sites (22 psu), calcium carbonate from mountain runoff has been reported in the area (Aburto-Oropeza et al., 2021; Conanp, 2023a) and the sap salinity of the plants is like that of trees in coastal areas (J. López-Portillo pers. com.). This suggests that the R. mangle trees in El Cacahuate Lagoon still exude salt through the leaves. However, atmospheric humidity and high precipitation could dilute the concentration of salts reaching the epiphytes (J. López-Portillo pers. com.). These conditions seem to favor the presence of orchid, bromeliad, and fern species recorded at this site; it also suggests that the species shared between the inland mangrove and coastal mangroves have adapted to both environmental conditions. Specific ecophysiological studies of the shared and not shared epiphyte species between this inland mangrove and the coastal mangroves will provide a better understanding of the characteristics that limit and promote the distribution of epiphytes in these ecosystems.

Similarities between epiphyte communities. Given the proximity of the Tenosique mountain (ca. 2-32 km), we expected that the species composition of the study area showed greater similarity in epiphyte composition with the surrounding forests (HETF, METF, DTF). It has been recorded that the structure, anatomy, and seed dispersal mechanisms of many epiphytes permit frequent colonization and recolonization processes between nearby tropical sites (Chilpa-Galván et al., 2018; Toledo-Aceves et al., 2012). Nevertheless, we found the highest similarity of El Cacahuate mangrove’s epiphyte species with the epiphyte communities of the coastal mangroves of Centla and Paraíso, located 194-200 km away. These facts suggest 2 possible hypotheses which can help to explain these similarities: the first suggests that when the sea encroached 120,000 years ago, not only R. mangle individuals and other terrestrial coastal species established along the banks of the San Pedro River and El Cacahuate Lagoon, but this process was accompanied by the coastal-affinity epiphytes recorded in the study area; the second one points to contemporary dispersal processes as the reason for the presence of these epiphytes with a coastal distribution. It has been documented that after ca. 30 years, 30% of the original epiphyte species recorded in mangrove trees in the natural part of a canal, colonized juvenile mangroves planted for reforestation in the artificial part of the canal (Kupec, 2018). This suggests that the epiphyte species with coastal affinity may have arrived at the inland mangrove of El Cacahuate Lagoon by seed step-dispersal and colonization events throughout the mangrove established along the San Pedro River, or by long-distance dispersal events of minute seed from the coastal mangroves (Schurr et al., 2009). The other epiphyte species with extensive tropical forest distribution surely have arrived by both dispersal ways.

These 2 processes do not exclude each other, and their success can be highly dependent on the number of viables seeds and habitat availability (Rodríguez-Romero et al., 2011). However, successful establishment also depends on the morphological and anatomical characteristics of the seeds (Arditti & Ghani, 2000; Chilpa-Galván et al., 2018). For instance, some ferns families (e.g., Aspleniaceae, Polypodiaceae, and Pteridaceae) produce many very small spores that are easily dispersed by wind over long distances (Martínez-Salas & Ramos, 2014; Perrie et al., 2010; Shepherd et al., 2009). Similarly, orchid fruits (Orchidaceae) produce millions of tiny seeds, often just a few microns in size and weighing no more than 22 mcg (Arditti & Ghani, 2000; Menchaca-García & Moreno-Martínez, 2011), which are also adapted for long-distance wind dispersal. Many bromeliad species (Bromeliaceae, subfamily Tillandsoideae) have plumose seed appendages that facilitate their movement through the air and their attachment to rough bark surfaces (Einzmann & Zotz, 2017; Mondragón-Chaparro et al., 2011). Meanwhile, some species such as A. bracteata, which produce berry-like fruits, and cacti such as S. grandiflorus and D. testudo, which have pulpy fruits, are dispersed by birds. This suggests that short- or long-distance seed dispersal has contributed to structuring the epiphyte community in the inland mangrove of El Cacahuate Lagoon. Future genetic studies will reveal how closely related the populations of shared epiphyte species are between the inland mangroves of El Cacahuate Lagoon and the coastal mangroves of Tabasco, particularly for those species with a wide distribution range.

Our study clearly shows that the epiphyte community in the inland mangroves of El Cacahuate Lagoon is species-rich. The humid environmental conditions present apparently reduce the salinity concentration exuded by the mangrove trees, allowing the great epiphyte species richness recorded. Also, we have demonstrated that this epiphyte community has a high similarity in composition to the epiphyte communities of the coastal mangroves of Tabasco, suggesting a close genetic relationship between these populations. Future genetic studies will help elucidate the dispersal routes followed by the epiphytes to colonize this mangrove. These and other biological characteristics make this inland mangrove ecosystem one of great biodiversity and conservation value.

Acknowledgments

Special thanks to the UJAT herbarium for access to its facilities and the support provided during the cabinet phase. We are grateful to M. Ferrer, J. Rodríguez, and E. López for their help with the fieldwork. Special thanks to W. Miss and his family for their hospitality and for facilitating access to the study site. Thanks to S. Morales, C. Rodríguez, and I. Morales for providing transportation to the study site. We extend our gratitude to F. Jiménez H. and R. Adams for reviewing early drafts of this manuscript. This study is part of the requirements for obtaining a master’s degree for NEM. The work was supported by the Universidad Juárez Autónoma de Tabasco through the project “Biodiversity and conservation of the inland mangroves of the San Pedro Mártir River as elements for sustainable development in Balancán and Tenosique, Tabasco, Mexico” (No. 20220327), and the Centro para la Biodiversidad Marina y la Conservación, A.C. and Mares Mexicanos. The Consejo Nacional de Humanidades, Ciencia y Tecnología (Conahcyt) granted a scholarship to the first author for his master’s program.

Appendix. Checklist of vascular epiphytes recorded in the inland mangrove of El Cacahuate Lagoon, and compiled data from the floristic studies completed in a radius of 220 km from El Cacahuate Lagoon. Acronyms: IM-Cacahuate, inland mangrove of El Cacahuate, Tenosique, Tabasco; CM-Paraíso, coastal mangrove of Cárdenas, Centla, Comalcalco, Paraíso, Tabasco (Díaz-Jiménez, 2007); CM-Centla, coastal mangrove of Centla, Tabasco (Jiménez-López et al., 2017, 2018); CM-Nohan, coastal mangrove of the UMA Nohan, Cd. del Carmen, Campeche (Noguera-Savelli et al., 2021); HETF-Tenosique, high evergreen tropical forest of Tenosique, Tabasco (Hernández-Sastré et al., 2014); METF-Tenosique, medium evergreen tropical forest of Tenosique, Tabasco (Morales-Damián, 2012); METF-Macuspana: Macuspana, Tabasco; López-Gómez 2014); MSTF-Catazaja: medium subevergreen tropical forest of Catazajá, Chiapas (Gutiérrez-Báez, 2004); TDF-Tenosique: tropical dry forest of Tenosique, Tabasco (Morales-Damián, 2012); TF&IM-San Pedro Mártir: tropical forests with the presence of R. mangle individuals in the riparian vegetation of the San Pedro Mártir River (Aburto-Oropeza et al., 2021); TF-Tikal: disturbed high evergreen tropical forest (Hellmuth and D’Angelo-Jerez, 2022); TF&IM-Peten: high evergreen tropical forest combined with R. mangle from the El Petén area (Conap, 2010).

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Complejo Prorocentrum lima asociado a macrofitas en dos sitios de afloramiento de borde oriental: laguna Estero de Urías (México) y bahía de Paracas (Perú)

Tomasa Cuellar-Martinez ^a, *, Ana Carolina Ruiz-Fernández ^a, Joan Albert Sanchez-Cabeza ^a, Arturo Aguirre-Velarde ^b, Haydeé Felícita López-Cabanillas ^b, Jorge Tam ^c,
Sonia Sánchez ^c, François Colas ^d

a Universidad Nacional Autónoma de México, Instituto de Ciencias del Mar y Limnología, Unidad Académica Mazatlán, Capitán Joel Montes Camarena s/n, Cerro del Vigía, 82040 Mazatlán, Sinaloa, Mexico

b Universidad Nacional Agraria La Molina, Facultad de Pesquería, Av. La Molina s/n, La Molina, Lima, Peru 

c Instituto del Mar del Perú, Esquina Gamarra y General Valle s/n, Chucuito Callao, Lima, Peru

d Institut de Recherche pour le Développement (IRD), Laboratoire LOPS, Institut Universitaire Européen de la Mer (IUEM), 29280 Plouzané, France

*Corresponding author: tcuellar@ola.icmyl.unam.mx (T. Cuellar-Martinez)

Received: 20 November 2024; accepted: 17 September 2025

Abstract

Benthic or epibenthic dinoflagellates (EDs) are a potential risk to the environment and human health due to the production of toxins by some species. This study explored for the first time the presence of EDs mainly associated with macrophytes (macroalgae and seagrass) at 2 sites influenced by upwellings: Estero de Urías Lagoon (EUL), at the entrance of the Gulf of California, and Paracas Bay (PB), on the southern Peruvian coast. Prorocentrum lima complex was present at low abundances: ≤ 25 cells g^-1 wet weight in EUL and ≤ 867 cells g^-1 wet weight in PB. It was recorded in a wide range of temperatures from 22.2 to 31.6 °C in EUL and from 18.0 to 22.2 °C in PB. Despite its low abundance, monitoring the EDs community is essential to detect changes in the distribution patterns of harmful species in the context of climate change.

Keywords: Macroalgae; Caulerpa; Artificial substrate; California Current; Humboldt Current 

Resumen

Los dinoflagelados epibentónicos (DE) representan un riesgo potencial al ambiente y a la salud del ser humano debido a la producción de toxinas por parte de algunas especies. En este estudio, se exploró por primera vez la presencia de DE principalmente asociados a macrofitas (macroalgas y pastos marinos) en 2 sitios con influencia de afloramientos: laguna Estero de Urías (LEU), localizado en la entrada del golfo de California y la bahía de Paracas (BP) en la costa sur de Perú. El complejo Prorocentrum lima estuvo presente con bajas abundancias: ≤ 25 células g^-1 peso húmedo en LEU y ≤ 867 células g^-1 peso húmedo en BP. La especie se registró en un amplio intervalo de temperatura de 22.2 a 31.6 °C en LEU y de 18.0 a 22.2 °C en BP. A pesar de las bajas abundancias encontradas, el monitoreo de la comunidad de DE es importante para detectar cambios en los patrones de distribución de las especies nocivas en un contexto de cambio climático.

Palabras clave: Macroalgas; Caulerpa; Sustrato artificial; Corriente de California; Corriente de Humboldt 

Introduction

Benthic or epibenthic dinoflagellates (EDs) are common in shallow waters. They are frequently attached to many substrate types, such as algal turf, macroalgae, rocks, coral rubble, sand, or seagrasses (Honsell et al., 2013; Yong et al., 2018). Although they prefer substrate attachment, the vegetative cells of free-living species are flagellated and are fully capable of detachment and motility (Durán-Riveroll et al., 2019). The excessive growth of these species, particularly the toxigenic ones, can produce benthic harmful algal blooms, and toxins can be transferred along the food web; in humans, consumption of contaminated seafood with these toxins can cause diarrhetic shellfish poisoning (DSP) or ciguatera fish poisoning (Berdalet et al., 2016). 

Although EDs have a high relative cell abundance and diversity in subtropical and tropical waters, they are found globally, including in temperate, sub-arctic, and polar environments (Álvarez et al., 2022; Tester et al., 2010). In recent decades, evidence suggests a shift in biogeographical distribution patterns for some species (Gobler et al., 2017; Tester et al., 2020), such as Gambierdiscus,previously considered tropical or sub-tropical. Recent studies have shown that it is well established in temperate areas such as Korea, Japan, New Zealand, Australia, the northern Gulf of Mexico, and the Mediterranean Sea (Chinain et al., 2021). Furthermore, there is concern that floating plastics in the ocean can act as global vectors for transporting algal cells and transferring toxins along marine food webs (do Prado-Leite et al., 2022).

In Mexico, about 60 species from 18 EDs genera have been identified. The species that form dense benthic blooms with potentially harmful consequences are Prorocentrum rhathymum, Blixaea quinquecornis, and Amphidinium cf. carterae (Okolodkov et al., 2022). In South America, 31 EDs taxa have been reported (Mafra et al., 2023). The most frequent and widespread species was the P. lima complex (Mafra et al., 2023). On the Peruvian coast, the cold coastal waters of the Humboldt Current System could restrict the presence of these species (Durán-Riveroll et al., 2019). The P. lima complex has been frequently observed over the past ~ 50 years, though studies have primarily focused on the planktonic community (Mafra et al., 2023). 

Benthic microalgae are expected to benefit from climate change conditions, such as warmer waters and changes in marine current patterns, which could promote their invasive colonization and range of expansion (Tester et al., 2010). Estero de Urías Lagoon (EUL) and Paracas Bay (PB) host harbors with high levels of activity (i.e., the harbors of Mazatlán and San Martín, respectively), which may represent a potential risk since ballast waters remain a vector for the introduction of non-native and potentially harmful aquatic species (Lee et al., 2021). This study aimed to explore the EDs associated with macrophytes in Estero de Urías Lagoon, Mazatlán (Mexico), and Paracas Bay, Pisco (Peru), and the environmental variables associated with the presence of these species.

Materials and methods

Estero de Urías Lagoon (EUL; 23.2° N) is located at the entrance to the Gulf of California (Fig. 1) and covers an area of 18 km² with water depths of 1-3 m except in the navigation channel where it is up to 13 m (Montaño-Ley et al., 2008). It is surrounded by the industrialized city and harbor of Mazatlán (Raygoza-Viera et al., 2014). It is influenced by seasonal coastal upwelling events (Herrera-Becerril et al., 2022). EUL does not receive continuous freshwater, for which it exhibits an inverse estuarine circulation, and during the warmest months high salinity occurs in the upper lagoon (Cardoso-Mohedano et al., 2018).

The climate in the area is warm and humid, with a mean annual temperature of 21.4-29.6 °C (1951-2017) and a mean annual precipitation of 372 mm (SMN, 2024). EUL is an anthropized coastal lagoon affected by urban development, shrimp farming, and discharges of domestic, industrial, and wastewater (Hernández-Cornejo & Ruiz-Luna, 2000; Méndez, 2002). The Mazatlán harbor is the second largest on the Mexican Pacific coast, and in 2023 it received almost 500,000 cruise ship passengers from the largest cruise ships navigating the globe (API, 2024). 

Paracas Bay (PB; 13.8° S) is located in Pisco, off South-Central Peru (Fig. 1), with an area of 30 km² and < 15 m of depth (Merma-Mora et al., 2024). The southern part of the bay is included in the Paracas National Reserve (Sernanp, 2019). It is influenced by one of the main upwelling cells of the highly productive Peruvian Upwelling System (Chávez et al., 2008). PB is seasonally influenced by river discharge, and monthly averages range from 0.7 to 282 m³ s⁻¹, with the higher values in austral summer (Cuellar-Martinez et al., 2023). 

The climate in the region is arid, with an average annual rainfall of 1.83 mm and air temperatures ranging from 15 to 22 °C (Reyes, 2009). Anthropogenic activities around the bay include artisanal and industrial fishing, tourism, bay scallop Argopecten purpuratus aquaculture, fish processing industries, non-metallic minerals, and guano extraction (Reyes, 2009). The Terminal Portuario General San Martín, the country’s third most important port for cargo traffic (APN, 2018), is in the surroundings. 

The most abundant macrophytes were collected manually or by diving and placed in polypropylene bags; the macrophyte masses ranged from 5 to 342.2 g in wet weight. The 3 sampling sites at EUL were close to the lagoon mouth, where a greater diversity of macroalgae species is found (Ochoa-Izaguirre et al., 2002). The sites were located in a total area of 0.01 km² with fish cage cultures (~ 8 m depth). The most abundant macroalgae attached to the floating cage frames were collected monthly between August and November 2018 and in January, February, April, and June 2019. A total of 25 samples were collected, including species of Gracilaria sp., Hynea sp., Sargassum sp., Padina sp., Grateloupia sp., and Gelidium sp. In general, 1 to 4 samples were collected per sampling station. In addition, between August and October 2018, artificial substrates consisting of rectangular pieces (3 x 33 cm) of fiberglass screen fixed on a rigid frame were used (Jauzein et al., 2016). The artificial substrates were collected using scissors. For retrieval, 24 hours after installation, the substrate was cut on one side and carefully placed into a plastic bottle filled with 250 ml of ambient seawater. Then, the other side of the substrate was cut and placed inside the bottle, which was capped underwater (Jauzein et al., 2016). 

In PB, the most abundant macrophytes, such as Caulerpa filiformis, Chondracanthus chamissoi, and Ruppia maritima were collected at 5 sites during June and November 2021, and April 2022. The sites were shallow (~ 1 m depth), whereas E1 and EM were 5 m and 10 m deep, respectively. A total of 24 samples were obtained. Additionally, surface water was sampled daily in E1 to evaluate the presence of EDs in the water (cells L^-1), and HOBO data loggers (Onset UA-001-64) recorded surface and bottom temperatures every 20 minutes.

Environmental parameters (temperature, salinity, dissolved oxygen, and chlorophyll a) were measured in both PB and EUL using EXO (YSI) multiparameter sondes. In EUL, the chlorophyll a sensor was calibrated using rhodamine standards according to the manufacture’s guidelines (YSI Inc., 2014), allowing chlorophyll a concentrations to be expressed in absolute units (μg L⁻¹). In contrast, no calibration was performed in PB; thus, chlorophyll a values are reported in RFU (relative fluorescence units), reflecting the raw sensor response. Although not directly comparable to absolute concentrations, RFU values are widely used to identify temporal patterns in relative chlorophyll a concentrations (Foster et al., 2022). In the EUL, measurements were taken near the sampling sites (1-2 km) at stations 3 and 4 for the coastal observatory of global change in Mazatlán (Fig. 1 in Sanchez-Cabeza et al., 2019) and at station E1 for PB. 

In the laboratory, the bags with macrophytes and bottles with artificial substrates were vigorously agitated for 2 minutes. The suspension was filtered through sieves with 250 µm, 150 µm, and 20 µm mesh to remove larger particles. The fraction retained in the 20 µm sieve was concentrated and transferred to a vial of 50 ml filled with seawater filtered through Whatman GF/F filters (nominal pore size ~ 0.7 µm), and preserved with 1% acidic Lugol’s iodine fixative. The EDs counting was performed on 3 replicate subsamples from the same macrophyte sample, using a Sedgwick-Rafter chamber in an optical microscope (LM Leica DMR, Wetzlar, Germany) with 200× magnification. Cell abundances were reported as cells per g w.w. of macrophyte (Reguera et al., 2011). The reported uncertainty is the standard deviation of the mean of 3 replicate counts.

The Shapiro test confirmed that species densities were not normally distributed. Therefore, Kruskal-Wallis one-way ANOVA and Dunn’s multiple comparison post hoc tests were used to assess whether abundances and environmental variables exhibited significant variations during the study period. The significance level (α) was set at < 0.05. All analyses and plots were performed with R version 2024.04.2 (R Core Team, 2024).

Results

Estero de Urías Lagoon

During the study period, the sea surface temperature (SST) varied from 22.2 to 31.6 °C, salinity from 34.0 to 36.1, turbidity from 0.8 to 4.1 NTU, and chlorophyll a from 2.2 to 6.7 mg L^-1. The highest SST was observed in August-September, 2018 (Fig. 2). 

No EDs were observed attached to the artificial substrates in the EUL. Macroalgae were not found in EU2 in November 2018 and June 2019. Dinoflagellates on the EUL macroalgae belonged to the genus Prorocentrum; the highest abundances corresponded to P. micans (Supplementary material; Fig. S1). Prorocentrum lima complex was frequently observed in the samples, with abundances ranging from 0 to 78±45 cells g^-1. No significant differences in the abundances were observed between seasons or among stations (Fig. 3a, b). Spearman’s correlation between the abundances of EDs and environmental variables was not significant. 

Paracas Bay

During the study period, temperatures were from 14.1 to 22.2 °C. The sea surface and bottom temperatures were significantly higher in autumn (surface temperatures: 18.0-22.2 °C; bottom temperatures: 17.5-21.6 °C) than in summer and spring (surface temperatures: 14.5-22.1 °C; bottom temperatures: 14.1-19.7 °C; Fig. 4a). In the 3 seasons, the surface temperatures were significantly higher than the bottom temperatures. When the P. lima complex was observed in the water column and associated with macrophytes (May 14-Jun 04), SST ranged from 18.0 to 22.2 °C. Chlorophyll a ranged from 0.45 to 7.12 RFU. The highest values were observed in autumn, while spring and summer values were similar. The salinity varied between 34.4 and 35.2, with higher values in autumn than in spring and summer (4b).

In Paracas Bay, EDs were absent during most of the study period, and the P. lima complex was detected only in the austral autumn (June 2-4, 2021; Fig. 5, Table 1) with the highest abundances (867±172 cells g^-1 in station E3). The P. lima complex was attached mostly to C. filiformis (Table 1).

According to the high-frequency monitoring of Prorocentrum species in surface water, P. micans was a common dinoflagellate in austral autumn and summer, and its abundances were from 40 to 1,840 cells L^-1 (Supplementary material; Fig. S2). The P. lima complex was observed only in the austral autumn with a maximum abundance (1,360 cell L^-1) on May 14, and between May 17 and June 01, its abundances were ≤ 280 cells L^-1 (Fig. 4c). 

Discussion

Artificial substrates have been successfully used for quantifying and monitoring EDs, particularly in sheltered, shallow, and subtidal sites (Tester et al., 2022). The lack of EDs attached to the artificial substrates in EUL is likely related to the low abundance of these organisms and the lagoon’s turbulent hydrodynamics. Low abundances of EDs were also observed associated with macroalgae. These results agree with observations from the coast of Tonga in an area exposed to high wave action, where Argyle (2018) detected low abundances of Gambierdiscus cells in association with macrophytes, but the artificial substrate failed to collect them. In contrast, Gambierdiscus concentrations were high on natural and artificial substrates deployed at sheltered, shallow, and subtidal sites. Despite EUL mouth having the highest macroalgae diversity (Ochoa-Izaguirre et al., 2002), it is not a sheltered zone. It is influenced by the tidal regime since the energy available for water circulation is primarily provided by tidal pumping, with tidal velocities of up to 0.60 m s^-1 at the main channel (Montaño-Ley et al., 2008). The EDs can be attached by coating mucus or can live freely within the macroalgae interstices, so the turbulence and currents make them vulnerable to cell dispersal. They are mainly found in areas with low to moderately low energy environments (Foden et al., 2005). 

Table 1

Abundance of Prorocentrum species in Paracas Bay in the austral autumn.

* Abundances represent the average of 3 independent counts performed on the same sample. Values are reported as the mean ± standard deviation.

Among the Prorocentrum species associated with macrophytes in this study, only P. lima complex is recognized as a benthic species (Okolodkov et al., 2022), and it is the first time that P. lima complexis reportedattached to macrophytes in EUL and PB. This cosmopolitan taxon is widely distributed in South America (Mafra et al., 2023). Although low abundances were observed in PB, P. lima has been recorded in the water column with abundances of up to 4.5×10⁴ cells L^-1 (Cuellar-Martinez et al., 2023). Caulerpa filiformis is the most representative species in the macroalgae assemblage of PB (Olivas-Valverde, 2013), and the highest abundances of P. lima complex were observed on this species. Although information about the toxicity of P. lima complex is not available in strains from PB or EUL, reports worldwide reveal that all studied P. lima strains produce toxins related to DSP, such as okadaic acid, and several strains produce dinophysistoxins-1 (DTX1; Nishimura et al., 2020). Thus, monitoring this species on different substrates is relevant. 

The presence of P. lima complex in both the water column and on macroalgae in Paracas Bay coincided with the highest temperatures recorded during the study period. Aissaoui et al. (2014) mentioned that this species appears to be eurythermal and euryhaline, as it grows over a wide interval of temperatures and salinities. In this work, P. lima complex was observed over a wide range of temperatures (18.0-31.6 °C), suggesting a remarkable ecological plasticity and ability to colonize diverse niches. Although P. lima complex was previously observed in PB at temperatures ranging from 15 to 25 °C (Mafra et al., 2023), in this study it was detected during autumn, when the highest temperatures reached 17.5-22.2 °C. Aquino-Cruz et al. (2018) highlighted the importance of temperature on cell growth rates, toxin levels, and photosynthetic efficiency. They determined that the optimum growth of P. lima strains from the United Kingdom occurred at 15-25 °C, with an increment in the production of okadaic acid at 15 °C.

Temperatures also affect the range of species distribution. It is expected that warmer temperatures associated with climate change could benefit harmful benthic dinoflagellate species, expanding their geographical distribution range (Tester et al., 2020). Another factor associated with distribution expansion is the artificial introduction of discharged ballast ship water (Park et al., 2021). The sampling period of this study limits the potential for making strong extrapolations regarding the temporal dynamics of the DEs and their ecological dynamics. Nevertheless, the detection of DEs with potential toxin production is a relevant finding that highlights the need for longer-term monitoring to better understand their ecological dynamics and potential harmful implications for environmental health and human activities.

The epibenthic dinoflagellate community was explored at 2 sites influenced by upwellings: Estero de Urías Lagoon, at the entrance to the Gulf of California, and Paracas Bay, off south-central Peru. The Prorocentrum lima complex was commonly found with low abundances, mainly associated with macrophytes in Estero de Urías Lagoon and sporadically detected in Paracas Bay (mainly on Caulerpa filiformis). In the water column of Paracas Bay, the P. lima complex was observed during the period with the highest recorded temperature in the study, suggesting potential environmental influences. These initial findings highlight the need for long-term studies with higher temporal resolution and increased detection frequency to better understand the environmental relationships of the benthic dinoflagellate at the studied sites. Given the known production of diarrhetic shellfish toxins by P. lima, its possible sensitivity to climate-related changes, and the anthropogenic pressures present in both study areas —such as intense marine traffic— further monitoring and multidisciplinary research, including toxicological, physiological, and molecular studies, are strongly recommended to assess the potential risks posed by P. lima to marine ecosystems and public health. 

Acknowledgments

This work was supported by UNAM ICML (#347), IAEA-RLA/7014 and 7028, Project Concytec – World Bank 05-2019-FONDECYT-BM. This is a contribution to the Marine-Coastal Research Stressors Network for Latin America and the Caribbean (REMARCO) www.remarco.org and to the IRN DEXICOTROP of the Institut de Recherche pour le Développement (IRD). The authors thank M. Rangel, O. López Ramos, M. Fregoso-López, B. Yáñez-Chávez, H. Bojórquez-Leyva, and F. Rioual for the help provided in the fieldwork; R. Alonso-Rodríguez, J. A. Cabello Coral, B. Yáñez-Rivera, for microscopy facilities. F. Ramos-Huamaní and L. H. Pérez-Bernal for the laboratory analyses, and M. Ochoa-Izaguirre for the identification of macroalgae from the Estero de Urías Lagoon.

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