As Epibiont of Crocodylus Moreletii (Duméril and Bibron, 1851) in Southern Mexico (Crocodylia: Crocodylidae)

Home , Epibiont, Hebetancylus, Hebetancylus excentricus

Herpetology Notes, volume 13: 627-629 (2020) (published online on 05 August 2020)

First record of the freshwater limpet Hebetancylus excentricus (Morelet, 1851) as epibiont of Crocodylus moreletii (Duméril and Bibron, 1851) in southern Mexico (Crocodylia: Crocodylidae)

Pierre Charruau1,*, Carlos Iván Flores-Escalona1, Marcos Antonio Morales Garduza1, and Everardo Barba-Macías2

The Morelet´s crocodile, Crocodylus moreletii (Duméril and research on health of these populations should and Bibron, 1851), is a medium-sized crocodilian that be taken into account (Ryser-Degiogis, 2013). One inhabits the Atlantic lowlands of the Gulf of Mexico particular aspect of health in Morelet´s crocodiles that and the Yucatan Peninsula (Platt et al., 2010). During has been poorly studied is parasitology. There are a few the early-mid 20th century, populations were severely records describing the various ectoparasites (leeches depleted due to overexploitation for the international and ticks) and endoparasites (gastrointestinal helminths) skin trade. Despite near extinction, the implementation of C. moreletii (Casas-Andreu et al., 2013; Charruau et of conservation and management laws directed towards al., 2016; Cory-Roberts et al., 2017), but overall there their protection has assisted species recovery in most of is a lack of data on the prevalence of those parasites its range. The Morelet’s crocodile is considered as Least in wild populations and if and how they are affecting Concern by the IUCN Red List of threatened species those populations. Furthermore, as far as we know, no (Cedeño-Vázquez et al., 2012) and is now recognised as epibiont have been formally identified in C. moreletii a species for sustainable management with a ranching to date. Those organisms have a different relationship program under development in southern Mexico (Platt with their host (basibiont) than parasites do. Epibionts et al., 2010; Barrios and Cremieux, 2018). usually do not harm the basibionts and the interaction The aquatic ecosystems of the Yucatan Peninsula and usually benefits the epibiont while the result can be Mexican lowlands of the Gulf of Mexico are strongly neutral (commensalism) or also beneficial (mutualism) affected by natural and anthropogenic disturbances for the basibiont. Moreover, epibiosis relationships (Metcalfe et al., 2011; Calderon-Aguilera et al., 2012; can be used as bioindicators (Violente-Huerta, 2018). Islebe et al., 2015), and their quality would likely Thus, any research on parasite and epibiont occurrence affect the health of populations of C. moreletii. As and their effect on C. moreletii would be valuable in the establishment of sustainable commercialisation understanding the host-parasite/epibiont dynamic, in of the Morelet´s crocodile progresses, the increase addition to providing cryptic data about the environment. deterioration of the environment, and the monitoring Herein, we report the first observation of the freshwater limpet Hebetancylus excentricus (Morelet, 1851), on a Morelet´s crocodile in southern Mexico. On 29 April 2019, we captured Morelet´s crocodiles in drains of rice fields for an ecotoxicological study in the ejido of Nuevo Pochote, Municipality of Emiliano 1 Centro del Cambio Global y la Sustentabilidad A.C., Calle Zapata, in the State of Tabasco (17.8718°N, 91.6726°W; Centenario del Instituto Juarez SN, Colonia Reforma, Datum WGS84; 8 m elevation). After obtaining the Villahermosa, Tabasco 86080, México. measures and samples, crocodiles were released at 2 Laboratorio Manejo Sustentable de Cuencas y Zonas Costeras, their capture sites. One subadult male of 129 cm total Departamento de Ciencias de la Sustentabilidad, El Colegio length (measured with a measuring tape, ± 0.1 cm) was de la Frontera Sur, Unidad Villahermosa, Carr. Reforma Km. 15.5 s/n Ra. Guineo 2.a Sección, Villahermosa, Tabasco parasitised by limpets on scales 11 (n = 2) and 13 (n = 86280, México. 1) of its simple caudal crest (Fig. 1) and on its groin * Corresponding author. E-mail: [email protected] (n = 2). We collected three of the five detected limpets, 628 Pierre Charruau et al.

on their skin (Cupul-Magaña and Cortés-Lara, 2005). We frequently observe algae on Morelet´s crocodiles we captured in Southern Mexico, including Nuevo Pochote, and H. excentricus could thus feed on these algae growing on the crocodiles. The limpet does not represent a threat to the health of crocodiles, but could help them to control the growth of algae on their skin, which would correspond to a mutualistic relationship.

Acknowledgements. We are grateful to Marisa Tellez for her comments on the first version of the manuscript. This work was funded by Project FORDECyT 273646: Cambio global y sustentabilidad en la cuenca del Usumacinta y zona marina de influencia: Bases para la adaptación al cambio climático desde la ciencia y la gestión del territorio. The study was realised with permit number SGPA/DGVS/03983/19 authorised by the Secretaria de Medio Ambiente y Recursos Naturales (SEMARNAT) of Mexico. Figure 1. The limpet Hebetancylus excentricus observed on a caudal scale of a Crocodylus moreletii specimen from the ejido References of Nuevo Pochote, Municipality of Emiliano Zapata, State of Tabasco, southern Mexico. Photo by Pierre Charruau. Barrios, G., Cremieux, J. (2018): Protocolo de rancheo para cocodrilo de pantano (Crocodylus moreletii) en México. Ciudad de México, México, Comisión Nacional para el Conocimiento y Uso de la Biodiversidad (CONABIO). Calderon-Aguilera, L.E., Rivera-Monroy, V.H., Porter-Bolland, L., and stored them in alcohol 96° for species identification Martínez-Yrízar, A., Ladah, L.B., Martínez-Ramos, M., et al. in the laboratory. The specimens collected were (2012): An assessment of natural and human disturbance effects identified as Hebetancylus excentricus, the excentric on Mexican ecosystems: current trends and research gaps. ancylid (Gastropoda: Heterobranchia: Planorbidae). Biodiversity Conservation 21: 589–617. The individual limpets were measured with a Vernier Casas-Andreu, G., Barrios-Quiroz, G., Escobedo-Galván, A.H., Digital Lion Tools (precision 0.05 mm) and have mean Aguilar-Miguel, X. (2013): Sinopsis de datos biológicos y dimensions of 4.23 ± 0.31 mm in shell length and 1.93 ecológicos del Cocodrilo de Pantano (Crocodylus moreletii). D.F., México, Instituto de Biología, Universidad Nacional ± 0.15 mm in shell width. We deposited the specimen Autonóma de Mexico. in the Aquatic Collection of Reference in the southeast: Cedeño-Vázquez, J.R., Platt, S.G., Thorbjarnarson, J. (IUCN macroinvertebrates and fish, ECOSUR, Villahermosa Crocodile Specialist Group) (2012): Crocodylus moreletii. The campus, with voucher number CRMT (Reference IUCN Red List of Threatened Species 2012: e.T5663A3045579. Collection of Mollusk from Tabasco) 19500–19502. Available at: https://dx.doi.org/10.2305/IUCN.UK.2012.RLTS. Hebetancylus excentricus is a freshwater limpet, T5663A3045579.en. Accessed on 10 June 2020. widely distributed across North and Central America and Charruau, P., González-Muñoz, R. (2016): Epibiont sea anemones the Caribbean islands (Thompson, 2011). The species is inhabiting the American crocodile Crocodylus acutus. Marine Biodiversity 46(1): 1–12. well distributed in the freshwater ecosystems of Tabasco Charruau, P., Pérez-Flores, J., Cedeño-Vázquez, J.R., González- and in Usumacinta river basin (Mellado-Hernández Solis, D., González-Desales, G.A., Monroy-Vilchis, O., Desales- et al., 2015; Trinidad-Ocaña et al., 2018). Although Lara, M.A. (2016): Occurrence of Amblyomma dissimile on several epibionts and ectoparasites have been recorded wild crocodylians in southern Mexico. Diseases of Aquatic in crocodilians (Huchzermeyer, 2003; Cupul-Magaña Organisms 121: 16 –171. et al., 2011; Charruau and González-Muñoz, 2016), to Cory-Roberts, C., Brianne, D., Tellez, M. (2017): Crocodylus our knowledge this is the first observation of limpets moreletii (Duméril & Bibron, 1851). Ectoparasitism. in crocodilians. The excentric ancylid is an herbivorous Mesoamerican Herpetology 4(4): 923–925. Cupul-Magaña, F., Cortés-Lara, M.C. (2005) First record of gastropod that feeds on aquatic plants during the day epibionts in Crocodylus acutus juvenile individuals in the wild. (Thorp and Covich, 2010). Thus, this species likely does Caldasia 27(1): 147–149. not exhibit a parasitic relationship with C. moreletii but Cupul-Magaña, F.G., Rubio-Delgado, A., Escobedo Galván, A.H., more a commensalistic or mutualistic relation. In aquatic Reyes-Núñez, C. (2011): First report of the marine barnacles eutrophic ecosystems, crocodiles illustrate algae growth Lepas anatifera and Chelonibia testudinaria as epibionts on First record of Hebetancylus excentricus as epibiont of Crocodylus moreletii 629

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Accepted by Pedro Pinna