From Tortuguero National Park, Costa Rica

J. Parasitol., 92(6), 2006, pp. 1202–1206 ᭧ American Society of Parasitologists 2006

DIGENETIC TREMATODE COMMUNITY IN NESTING GREEN SEA TURTLES (CHELONIA MYDAS) FROM TORTUGUERO NATIONAL PARK, COSTA RICA

Mario Santoro, Ellis C. Greiner*, Juan Alberto Morales, and Beatriz Rodrı´guez-Ortı´z† Departamento de Patologı´a, Escuela de Medicina Veterinaria, Universidad Nacional, P.O. Box 86, Heredia 3000, Costa Rica. e-mail: [email protected]

ABSTRACT: The digenetic community of 40 green sea turtles (Chelonia mydas) was investigated at Tortuguero National Park, Costa Rica. In total, 24,270 trematodes belonging to 29 species and 6 families including Clinostomidae 1, Microscaphidiidae 5, Paramphistomidae 2, Pronocephalidae 15, Rhytidodidae 2, and Spirorchiidae 4 were recorded from chelonians examined. Turtles harbored a mean of 7.63 Ϯ 3.5 SD species. Only 3 species, i.e., Learedius learedi, Microscaphidium reticulare, and Pyelosomum cochlear, infected more than 50% of the hosts sampled. Learedius learedi was the most prevalent (97.5%) and the second most abundant species with a mean of 25.6 Ϯ 21.6 SD. Only 1 core species, M. reticulare, was recovered from the gastrointestinal tract; it was the most abundant parasite, with a mean intensity of 477 Ϯ 1,180 SD, and the second most prevalent (77.5%). Diversity values ranged from 0.10 to 2.10, with a mean of 1.00 Ϯ 0.43 SD for the total component community and from 0.10 to 1.84, with a mean of 0.79 Ϯ 0.41 SD, for the gastrointestinal component community. Species richness was the highest recorded from a sea turtle species. All digenetic species were recorded from Costa Rica for the ﬁrst time. This represents the ﬁrst report on the helminth community of the green turtle.

The green turtle (Chelonia mydas) is a widely distributed owing to the haphazard and irregular sampling, it has not been herbivore in the Atlantic, Pacific, and Indian oceans. The Ca- possible to accurately estimate the population or community ribbean Sea constitutes a very important feeding area for a large parameters of parasites in these turtles. population of resident green turtles and for migrant individuals Here, we report on the parasite community of 40 nesting that periodically use this area to graze, breed, and nest (Mor- green turtles from Tortuguero National Park, Costa Rica. This timer, 1995; Troe¨ng et al., 2005). Tortuguero National Park on represents the first report of sea turtle trematodes from Costa the northern Caribbean coast of Costa Rica is the most impor- Rica. tant green turtle nesting ground of the Atlantic Ocean. Here, the nesting season occurs annually from June to October. Tur- MATERIALS AND METHODS tles spend up to 3 mo offshore from the park coastline to complete their reproductive cycle, coming ashore only to nest. From June to September of the 2003 and 2004 nesting seasons, 40 When the reproductive cycle ends, the turtles return to a pasture female green turtles were collected on a 26 km beach of Tortuguero Њ Ј Љ Њ Ј Љ Њ Ј Љ Њ Ј Љ resident area (approximately 512 km away) in the western Ca- National Park (10 32 27 N, 83 29 59 W–10 21 17 N, 83 23 29 W). Necropsy methods followed those of Wolke and George (1981). Turtles ribbean off the Nicaraguan coast (Meylan, 1995; Troe¨ng et al., were found freshly dead, killed during the night by jaguar (Panthera 2005). onca) attack while they were coming ashore to nest. All carcasses used Among the reptiles, turtles possess the richest and largest in this study were complete turtles collected at dawn under appropriate helminth communities (Aho, 1990). The published literature on permits from the Costa Rican government. Organs, including the heart, sea turtle helminth communities includes only 2 studies, 1 on great vessels, lungs, esophagus, stomach, upper and lower intestine, spleen, liver, gall bladder, kidneys, and urinary bladder, were carefully the olive ridley (Lepidochelys olivacea) of the Pacific coast of examined for parasites following the methods described by Greiner et Mexico (Pe´rez-Ponce De Leoń et al., 1996) and 1 on the log- al. (1980). Trematodes were collected alive, placed in tap water, refrig- gerhead (Caretta caretta) of the western Mediterranean Sea erated overnight, and fixed in AFA (alcohol–formalin–acetic acid so- (Aznar et al., 1998). Results of these studies showed the hel- lution) or 70% ethanol, then stained with Mayer’s acid carmine and minth parasite communities as isolationist, poor, and of low mounted in Canada balsam. Specimens were deposited in the Coleccioń Helmintolo´gica de Costa Rica (accession numbers CHCR 168/283), diversity. Universidad de Costa Rica, San Jose´, Costa Rica, and the Harold W. Owing to the opportunistic nature surrounding the collection Manter Laboratory of Parasitology (accession numbers P-2005-797 and of the turtles, it has not been possible to generate data regarding P-2005-800), Nebraska State Museum, Lincoln, Nebraska. species richness, prevalence, abundance, and intensity of the Prevalence, intensity, and abundance for each species were recorded parasite community in a Caribbean green turtle population. To according to definitions by Bush et al. (1997). A helminth species was our knowledge, the only published data regarding trematodes considered to be common (core species as defined by Aho, 1990) if it had a prevalence Ͼ50%. A specialist species was defined as one recov- in green turtles from the Caribbean Sea have been obtained ered only from a sea turtle species (for example specialist in green from Jamaica (Stephens, 1911), Trinidad (Gupta, 1961), an un- turtle). A generalist species was a parasite found in 2 or more turtle named Caribbean site (Gupta, 1962), Cuba (Groschaft, 1977; species (generalist in sea turtles) or in other vertebrate species. An al- Groschaft et al., 1977; Groschaft and Tenora, 1978), and Puerto logenic species was defined as one that uses fish or other aquatic ver- Rico (Dyer et al., 1991, 1995; Williams et al., 1994). These tebrate as an intermediate host and that matures in birds (Esch et al., 1990). studies, however, included a single turtle, or just a few. Thus, To describe the infracommunity structure, the number of helminth species per turtle (richness) and the number of worms per turtle, including uninfected hosts (abundance), were used. Brillouin’s index of Received 13 February 2006; revised 5 April 2006; accepted 16 May diversity was applied to calculate infracommunity diversity (Magurran, 2006. 1988). Analysis of the component community using all organs was cal- * Department of Pathobiology, College of Veterinary Medicine, Uni- culated first. Then gastrointestinal helminth community (worms from versity of Florida, Gainesville, Florida 32611. the esophagus, stomach, and intestine) was calculated separately to † Laboratorio de Helminthologıá, Facultad de Microbiologıá, Univer- compare our data with previously published studies (Pe´rez-Ponce De sidad de Costa Rica, San Jose´, Costa Rica. Leoń et al., 1996; Aznar et al., 1998).

1202 SANTORO ET AL.—DIGENETIC TREMATODE COMMUNITY OF CHELONIA MYDAS 1203

TABLE I. Prevalence, mean abundance, and infection intensity of digenetic trematodes in 40 green turtles (Chelonia mydas) from Tortuguero National Park, Costa Rica.*

Intensity of infection Prevalence Mean Trematode species (location in host)† (%) abundance x¯ Range

Angiodictyidae Microscaphidium reticulare van Beneden, 1859 (I)‡§ 77.5 477.0 Ϯ 1179.6 615.1 Ϯ 1311.8 1–6410 Deuterobaris intestinalis Mehrotra, 1973 (I)§ 45 22.2 Ϯ 63.4 49.4 Ϯ 88.3 2–369 Polyangium linguatula Looss, 1899 (I)࿣ 27.5 0.5 Ϯ 1.2 2.0 Ϯ 1.6 1–6 Octangium hiphalum Blair, 1987 (LI)‡§ 5 1.5 Ϯ 6.8 29.5 Ϯ 12.0 21–38 Microscaphidium warui Blair, 1986 (UB)‡§ 2.5 NA 2 — Clinostomidae Clinostomum complanatum Rudolphi, 1814 (E)‡࿣ 2.5 NA 1 — Paramphistomidae Schizamphistomoides erratum Blair, 1983 (LI)࿣ 45 4.7 Ϯ 7.4 10.5 Ϯ 7.8 2–24 Schizamphistomoides scleroporum Creplin, 1844 (I/S)࿣ 32.5 9.2 Ϯ 27.2 28.3 Ϯ 42.6 1–165 Pronocephalidae Pyelosomum cochlear Looss, 1899 (UB)࿣ 57.5 1.0 Ϯ 1.2 1.8 Ϯ 1.1 1–4 Cricocephalus resectus Looss, 1902 (E/S)࿣ 47.5 15.8 Ϯ 44.7 33.3 Ϯ 61.0 1–262 Desmogonius desmogonius Stephens, 1911 (E/S)§ 45 4.7 Ϯ 8.1 10.4 Ϯ 9.4 1–33 Cricocephalus megastomus Looss, 1902 (E/S)࿣ 35 9.5 Ϯ 22.9 27.0 Ϯ 32.6 1–99 Cricocephalus albus Kuhl and van Hasselt, 1822 (E/S)࿣ 30 8.6 Ϯ 22.9 28.6 Ϯ 35.1 1–103 Pronocephalus obliquus Looss, 1899 (HI)§ 30 7.2 Ϯ 17.8 24.1 Ϯ 26.1 1–91 Charaxicephaloides sp. (S)§ 27.5 7.6 Ϯ 21.4 28 Ϯ 34.2 6–127 Pleurogonius longiusculus Looss, 1901 (I)§ 20 0.6 Ϯ 1.7 3.2 Ϯ 2.7 1–8 Charaxicephalus robustus Looss, 1901 (E/S)§ 15 2.4 Ϯ 10.6 16.3 Ϯ 24.7 1–66 Pleurogonius sindhii Mehra, 1939 (I)§ 15 0.1 Ϯ 0.3 1.0 Ϯ 0.0 1 Rameshwarotrema uterocrescens Rao, 1975 (E)࿣ 10 0.6 Ϯ 1.8 5.7 Ϯ 1.9 3–7 Pleurogonius sp. (LI) 5 0.3 Ϯ 1.5 5.5 Ϯ 6.3 1–10 Pleurogonius linearis Looss, 1901 (I)࿣ 5 0.1 Ϯ 0.4 2.0 Ϯ 0.0 2 Pleurogonius solidus Looss, 1901 (I)࿣ 5 0.1 Ϯ 0.3 1.5 Ϯ 0.7 1–2 Himasomum lobatus Looss, 1901 (I)࿣ 2.5 NA 1 — Rhytidodidae Rhytidodoides similis Price, 1939 (GB/L)§ 25 2.6 Ϯ 7.1 10.6 Ϯ 11.3 1–34 Rhytidodoides intestinalis Price, 1939 (GB)§ 15 0.2 Ϯ 0.4 1.2 Ϯ 0.4 1–2 Spirorchiidae Learedius learedi Price, 1934 (GV/H/E/GB/L/I)࿣ 97.5 25.6 Ϯ 21.6 26.2 Ϯ 21.5 3–78 Hapalotrema postorchis Rao, 1976 (GV/H)§ 20 3.4 Ϯ 20.8 19.9 Ϯ 45.4 1–132 Monticellius indicum Mehra, 1939 (H)§ 12.5 0.2 Ϯ 0.5 1.6 Ϯ 0.6 1–2 Amphiorchis solus Simha and Chattopadhyaya, 1970 (I)§ 2.5 NA 1 —

* Mean abundance and infection intensity were reported with mean followed by standard deviation. † Abbreviations: E, esophagus; GB, gall bladder; GV, great vessels; H, heart; HI, high intestine; I, intestine; L, liver; LI, lower intestine; S, stomach; UB, urinary bladder. ‡ Only immature ﬂukes. § Specialist parasites. ࿣ Generalist parasites.

RESULTS 6,614. Altogether, 22,926 flukes were recovered from the gastrointestinal tract, which harbored a mean of 5.40 Ϯ 2.90 SD Forty of 40 (100%) nesting female green turtles (curved car- apace length ranging from 92 to 111 cm) were parasitized by species, ranging from 2 to 13. The number of flukes per host Ϯ only digenetic trematodes. In total, 24,270 flukes belonging to varied from 17 to 6,512, with a mean of 573.2 1,219.8 SD. 29 species and 6 families, including Clinostomidae 1, Micro- Only 3 species, i.e., Learedius learedi, M. reticulare, and Pye- scaphidiidae 5, Paramphistomidae 2, Pronocephalidae 15, Rhy- losomum cochlear, infected more than 50% of the hosts sam- tidodidae 2, and Spirorchiidae 4, were recovered (Table I). Only pled. Only 1 core species, M. reticulare, was recovered from immature specimens of Microscaphidium reticulare, Micro- the gastrointestinal tract; it accounted for 77.3% of total flukes scaphidium warui, Octangium hiphalum, and Clinostomum found. It was the most abundant with a mean of 477 Ϯ 1,180 complanatum were found. Turtles harbored a mean of 7.63 Ϯ SD worms and the second most prevalent (77.5%). Learedius 3.5 SD species, ranging from 3 to 17; the mean number of learedi was the most prevalent (97.5%) and the second most worms per host was 606.7 Ϯ 1,224.8 SD, ranging from 46 to abundant species, with a mean of 25.6 Ϯ 21.6 SD. Brillouin’s 1204 THE JOURNAL OF PARASITOLOGY, VOL. 92, NO. 6, DECEMBER 2006

TABLE II. General statistical data of gastrointestinal helminth communities of sea turtles.*

Olive ridley turtle, n ϭ 32 (Lepidochelys olivacea), Loggerhead turtle, n ϭ 54 Green turtle, n ϭ 40 Pe´rez-Ponce De Leo´n (Caretta caretta), (Chelonia mydas), this study et al. (1996) Aznar et al. (1998)

Geographical site Tortuguero, Caribbean coast of Costa Rica Oaxaca, Paciﬁc coast of Mexico Western Mediterranean Species richness 5.40 Ϯ 2.90 (2–13) 1.8 Ϯ 1.4 (1–2) 1.60 Ϯ 0.60 (1–3) Abundance 573.2 Ϯ 1,219.8 (17–6,512) 49.9 Ϯ 88.7 (1–365) 131.4 Ϯ 143.9 (1–683) Brillouin’s index 0.79 Ϯ 0.41 (0.10–1.84) 0.42 Ϯ 0.47 (0.37–1.6) 0.21 Ϯ 0.30 (0–1.04)

* Data were reported with mean followed by standard deviation and the range in parentheses. diversity index ranged from 0.10 to 2.10, with a mean of 1.00 tode. This fluke is a specialist in green turtles, where it occurs Ϯ 0.43 SD for overall component community and from 0.10 to in the esophagus, intestine, pseudocecum, and large intestine 1.84 with a mean of 0.79 Ϯ 0.41 SD for the gastrointestinal (Blair, 1986). Fischthal and Acholonu (1976) also recorded M. component community. reticulare from hawksbill turtles in Puerto Rico. Blair (1986) All digenean species collected were recorded from Costa reexamined deposited material from Puerto Rico and concluded Rica for the first time. New geographical locality records for that ‘‘for the very bad condition their specimens cannot be iden- the Atlantic Ocean included Amphiorchis solus, Charaxice- tified with certainty, even to genus.’’ phalus robustus, Cricocephalus resectus, Deuterobaris intestin- The presence of an immature C. complanatum was consid- alis, Hapalotrema postorchis, M. warui, Monticellius indicum, ered accidental. This is a cosmopolitan parasite in the buccal O. hiphalum, Pleurogonius sindhii, Rhytidodoides intestinalis, cavity and esophagus of piscivorous birds (Kanev et al., 2002). and Rhytidodoides similis. New geographical locality records The beach of Tortuguero National Park is located between an for the Caribbean Sea included Pleurogonius longiusculus and intricate series of channels and rivers, and it is possible that Pronocephalus obliquus. Clinostomum complanatum was re- this infection was acquired accidentally by ingesting an infected corded from a sea turtle for the first time. intermediate host being dragged by the river current to sea. Green turtles from Tortuguero had higher gastrointestinal DISCUSSION mean species richness and higher abundance when compared to Pacific olive ridleys (Pe´rez-Ponce De Leoń et al., 1996) and Green turtles from Tortuguero National Park were parasitized Mediterranean loggerheads (Aznar et al., 1998) (Table II). This exclusively by a rich fauna of digenetic trematodes. Helminths difference in the patterns between the marine turtle helminth other than trematodes are rarely recorded in free-ranging green infracommunities may be related to different foraging habits turtles. Only occasional nematodes have been found in the gas- and the habitat conditions in which the 3 turtle species live. The trointestinal tract (Freitas and Lent, 1946; Lichtenfels et al., diet of the host, habitat, population density, and seasonal move- 1978). Of the 29 species observed in the present study, 15 were ments have been cited as the factors determining the nature of specialists in green turtles (Table I). The remaining species were generalists in sea turtles, except for C. complanatum, a common the parasite fauna (Ginetsinskaya, 1988; Aho, 1990; Marcog- generalist in birds. However, Cricocephalus albus has occa- liese, 2002). Loggerheads and olive ridleys are omnivorous sionally been recovered from the marine French angelfish Po- generalists, foraging principally on fish, crustaceans, and mol- macanthus arcuatus (Pe´rez-Ponce De Leoń and Brooks, 1995), lusks. Caribbean green turtles graze primarily on the sea grass, C. resectus from a star tortoise Testudo elegans (Yamaguti, Thalassia testudinum, which constitutes almost 90% of their 1971), and Polyangium linguatula from kidneys of the avian diet (Bjorndal, 1997). Studies of sea turtle movements showed host, the arctic loon Colymbus arcticus (ϭGavia arctica) (Po- that loggerheads and olive ridleys are highly migratory and no- che, 1925). The exceptional finding of an immature C. com- madic species that disperse and move great distances through planatum constituted the only allogenic species we recovered. the pelagic habitat (Musick and Limpus, 1997; Plotkin, 2003). The presence of 15 specialist species in nesting green turtles Green turtles nesting in Tortuguero find their resident foraging confirms that its digenean fauna has high degree of specificity, habitat in the western Caribbean off the Nicaraguan coast, in contrast with other sea turtles (Pe´rez-Ponce De Leoń et al., where waters are shallow and currents are weak (Meylan, 1995; 1996; Aznar et al., 1998), where helminth communities were Troe¨ng et al., 2005). Generally, it is agreed that a geographi- dominated by generalists. We found 3 core species, constituting cally widespread generalist feeder is exposed to a greater num- 10.3% of the entire component community, but only 1 core ber of potential intermediate host species, resulting in a greater species, M. reticulare, with immature specimens in the gastro- helminth richness compared to a specialized consumer with a intestinal tract. narrower geographic range (Kennedy et al., 1986; Marcogliese, The most prevalent species was the cardiovascular fluke L. 2002). With the exception of a few marine sanguinicolids that learedi (97.5%) reported to date from green turtles, black turtles use annelids, flukes require mollusks as obligate intermediate (Chelonia mydas agassizii), and hawksbill turtles (Eretmochelys hosts (Esch et al., 2001). Habitat conditions of the Caribbean imbricata) from the Atlantic, Pacific, and Indian oceans (Smith, feeding area (warm and shallow water with weak currents) fa- 1997; Inohuye-Rivera et al., 2004). Microscaphidium reticulare vor the occurrence of trematodes, molluscan intermediate hosts, was the second most prevalent and the most abundant trema- and vegetation growth (Ginetsinskaya, 1988; Marcogliese, SANTORO ET AL.—DIGENETIC TREMATODE COMMUNITY OF CHELONIA MYDAS 1205

2002; Prieto et al., 2003), while the pelagic habitat of the other ESCH, G. W., L. A. CURTIS, AND M. A. BARGER. 2001. A perspective on sea turtle species probably reduces the transmission possibilities the ecology of trematode communities in snails. Parasitology 123: 57–75. for trematodes (Holmes, 1990; Marcogliese, 2002). ———, A. W. SHOSTAK,D.J.MARCOGLIESE, AND T. M . G OATER. 1990. Of the 5 species of Microscaphidiidae collected in this study, Patterns and processes in helminth parasite communities: An over- M. reticulare, M. warui, and O. hiphalum were the only im- view. In Parasite communities: Patterns and processes, G. W. Esch, mature worms present. We hypothesize that recruitment of these A. O. Bush, and J. M. Aho (eds.). Chapman and Hall, New York, p. 1–19. infections may have occurred during the breeding migration to FISCHTHAL,J.H.,AND A. D. ACHOLONU. 1976. Some digenetic trema- Tortuguero nesting beach. In some aquatic bird and fish popu- todes from the Atlantic hawksbill turtle, Eretmochelys imbricata lations, it has been shown that trematode fauna may be affected imbricata (L.) from Puerto Rico. Proceedings of the Helminthol- by seasonal movements. For birds and marine fishes, it is be- ogical Society of Washington 43: 174–185. lieved that intensity of infection decreases during the migration FREITAS,J.F.T.,AND H. LENT. 1946. ‘‘Porrocaecum sulcatum’’ (Ru- dolphi, 1819) (Nematoda, ascaroidea). Revista Brasileira de Biol- and reaches its maximum at the breeding grounds (Erasmus, ogia 6: 235–238. 1972; Esch et al., 1990). Also it is suggested that stress in GINETSINSKAYA, T. A. 1988. Problems of trematode ecology. In Trem- female reptiles during the breeding and nesting seasons may atodes, their life cycles, biology and evolution, T. A. Ginetsinskaya affect the immune system and make hosts more susceptible to (ed.). Amerind Publishing Co. Pvt. Ltd., New Delhi, India, p. 318– 346. infection, favoring a higher prevalence and abundance (Eras- GREINER, E. C., J. J. FORRESTER, AND E. R. JACOBSON. 1980. Helminths mus, 1972; Saad and El Deeb, 1990). of mariculture-reared green turtles (Chelonia mydas) from Grand Caribbean green turtle habitat, together with the grazing hab- Cayman, British West Indies. Proceedings of the Helminthological its and breeding migration of the turtles, were likely the most Society of Washington 47: 142–144. important factors influencing the composition and richness of GROSCHAFT, J. 1977. Microscaphidium caballeroi sp. n. from marine turtle (Chelonia mydas) and a revision of the subfamily Micro- nesting green turtle parasite community from Tortuguero Na- scaphidiinae Looss 1900 (Trematoda: Microscaphidiidae). Excerta tional Park, which was dominated in species number by pron- Parasitologica 1977: 169–176. ocephalids. Unfortunately, no data exist regarding helminth ———, A. C. OTERO, AND F. T ENORA. 1977. Trematodes (Trematoda) communities in other green turtle populations for comparison from Cuban turtles Chelonia mydas mydas (L.) and Eretmochelys imbricata imbricata (L.) (Testudinata-Cheloniidae). Acta Univer- with our data. sitatis Agriculturae, Facultas Agronomica 25: 155–167. ———, AND F. T ENORA. 1978. Charaxicephaloides polyorchis gen. ACKNOWLEDGMENTS nov., sp. nov. (Trematoda: Charaxicephalinae) from Chelonia mydas mydas (Testudinata) in Cuba. Vestnik Ceskoslovenske Spolec- We are grateful to Tortuguero Conservation Area and the Park Rang- nosti Zoologicke 42: 108–111. ers for logistic support and for facilitating the sampling on the beach. GUPTA, S. P. 1961. On some trematodes from the intestine of the marine We would also like to thank Gerardo Chavez, Universidad de Costa turtle, Chelone mydas from the Caribbean Sea. Canadian Journal Rica, who assisted with the statistical analyses. 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