Syst Parasitol (2011) 78:117–122 DOI 10.1007/s11230-010-9280-9
A new species of Caryospora Le´ger, 1904 (Apicomplexa: Eimeriidae) from the endangered Round Island boa Casarea dussumieri (Schlegel) (Serpentes: Bolyeridae) of Round Island, Mauritius: an endangered parasite? Peter Daszak • Stanley J. Ball • Daniel G. Streicker • Carl G. Jones Keith R. Snow
•
Received: 1 July 2010 / Accepted: 19 October 2010 Ó Springer Science+Business Media B.V. 2010
Abstract A new species of Caryospora Le´ger, 1904 (Apicomplexa: Eimeriidae), C. durelli n. sp., is described from the endangered Round Island boa Casarea dussumieri (Schlegel) (Serpentes: Bolyeridae) from Round Island, Mauritius. Six of 11 hosts were infected. Oo¨cysts are spherical to subspherical, 19.2 9 18.2 (17.5–21 9 16–21) lm, n = 20, and have a shape index (mean length/mean width) of 1.05 (1.02–1.09). The bi-layered wall is composed of an outer layer of c.0.6 lm thick and an inner layer of c.0.4 lm thick. A micropyle, oo¨cyst residuum and P. Daszak (&) EcoHealth Alliance, 460 West 34th Street, 17th Floor, New York, NY 10001, USA e-mail:
[email protected] S. J. Ball School of Life Sciences, Kingston University, Kingston-upon-Thames, Surrey KT1 2EE, UK D. G. Streicker Odum School of Ecology, University of Georgia, Athens, GA 30602, USA C. G. Jones Mauritian Wildlife Foundation, Black River, Mauritius C. G. Jones Durrell Wildlife Conservation Trust, Les Augre`s Manor, Trinity, Jersey, Channel Islands, UK K. R. Snow School of Health and Bioscience, University of East London, London E15 4LZ, UK
polar granule are absent. Sporocysts are ellipsoidal, 14.7 9 11.0 (13–16 9 9.5–11.5) lm, n = 20, and have a shape index of 1.33. Both Stieda and substieda bodies are present. The sporocyst residuum measures c.12 9 4.5 lm, is surrounded by sporozoites and composed of numerous granules. Refractile bodies are present but not clearly visible. This is the first coccidian parasite reported from the family Bolyeridae and the first species of Caryospora reported from the Mascarenes. Conservation issues concerning parasites of endangered host species are discussed.
Introduction The island of Mauritius is located in the Indian Ocean, 850 km east of Madagascar, and is the home to an important relict endemic flora and fauna (Cheke, 1987). The introduction of exotic species, habitat degradation and direct predation following colonisation by humans in the 1700s led to the rapid extirpation of many endemic species, including the dodo Raphus cucullatus and a number of endemic reptiles, such as the giant Mauritian skink Leiolopisma mauritiana and the gecko Phelsuma gigas, the largest known species of the genus Phelsuma (see Arnold, 1980; Vinson & Vinson, 1969). Relict populations of the Mauritian flora and fauna survive in extremely small areas of remnant endemic habitat, such as montane forest on mainland Mauritius and palm savannah on small satellite islands. One of these satellites, Round Island,
123
118
has an area of only 150 hectares, yet harbours four endemic species of reptiles that originally occurred throughout Mauritius: Telfair’s skink Leiolopisma telfairii, the Round Island boa Casarea dussumieri, Durrell’s night gecko Nactus durrelli and the Round Island gecko Phelsuma guentheri (see Arnold, 1980; Arnold & Jones, 1994; Austin et al., 2004; Vinson, 1953, 1975; Vinson & Vinson, 1969). Historically, the habitat of Round Island consisted of palm forest on the lower slopes and a hardwood forest on the summit consisting of dwarf ebony and other trees (Lloyd, 1846; Pike, 1870). The anthropogenic introduction of rabbits and goats led to overgrazing of tree seedlings and eventual loss of forest and soil cover (Vinson, 1964). An international conservation project, initiated in the 1970s, has focused on habitat restoration, eradication of introduced species, captive breeding of endangered taxa and surveys of biodiversity on Mauritius and its surrounding islands (Bell, 2002; Bloxam, 1986; Bloxam & Vokins, 1978; Jones, 1993; Merton et al., 1989; Tonge & Barlow, 1985). During expeditions to these islands faecal samples from wild-caught reptiles were surveyed for parasites (Daszak, 1995; Leinwand et al., 2005). The aims were twofold: to assess the potential threat these parasites may represent to small relict host populations and to assess the biodiversity of the parasites. During these surveys, a new species of Caryospora Le´ger, 1904 was discovered in the faeces of Casarea dussumieri. This snake is restricted to Round Island, Mauritius, where it is the sole remaining representative of the family Bolyeridae. The other member of this family, the Round Island burrowing boa Bolyeria multocarinata, was last seen in 1975 (Bullock, 1986) and is now listed as extinct on the IUCN Red List (http://www.redlist.org). Apart from a prevalence paper resulting from these surveys (Daszak, 1995), there are no previous reports of parasites in this species of snake nor in the family Bolyeridae.
Materials and methods Animals were collected on two expeditions to Round Island: the first organised by Raleigh International (August 1st–September 15th, 1993) and the second organised by Kingston University (October 12th– November 15th, 1995) (Daszak, 1994, 1996). Animals were collected from the wild and kept individually in
123
Syst Parasitol (2011) 78:117–122
uncontaminated snake bags immediately after capture and up to the point of the collection of faeces for the present study. Animals were released within 48 hours of capture. Fresh faecal samples were placed in 2.5% potassium dichromate and examined by direct, wet mounts. Oo¨cysts were measured six weeks later and photographed under oil using a Zeiss photomicroscope III using DIC optics. Mean oo¨cyst lengths and widths are given with standard deviations; all ranges are in parentheses, and all measurements in micrometres. Oo¨cyst morphology of our new species of Caryospora was compared with all Caryospora spp. previously described from the superfamily Henophidia (Boidea—boas and pythons) (Lainson et al., 1991; Matuschka, 1984; Upton et al., 1990). Due to the rarity of the host animals, no specimens were available for studies of the endogenous stages of the coccidia described herein and no specimens were available for deposition as symbiotypes.
Caryospora durrelli n. sp Type-host: Casarea dussumieri (Schlegel); the Round Island boa or keel-scaled boa (Serpentes: Bolyeridae). Adult (sex unknown) collected 28th August, 1993. Type-locality: Western slopes of Round Island, 21 km NNE of Mauritius; 19°500 1600 S, 57°460 3400 E. Type-material: Photosyntype deposited at the Pathology Museum of the Institute of Zoology, Zoological Society of London, Regent’s Park, London NWI 4RY, UK. Accession number: ZSL 008. Site of infection and sporulation: Unknown; oo¨cysts recovered from faeces and not examined for 4 days after collection due to lack of microscope access. Other hosts and localities: None identified. Prevalence: 6/11 individuals; 1993 expedition, 6/10 individuals (including 1 immature specimen); 1995 expedition, 0/1 individuals. Pathogenicity: There were no grossly visible clinical signs of infection. Etymology: The specific name is given for the late conservationist, author and founder of the Durrell Wildlife Conservation Trust (formerly the Jersey Wildlife Preservation Trust), Gerald Durrell, whose popular writings and documentaries acted as a catalyst for the restoration of Round Island, for the conservation of the Mascarene flora and fauna, and for the global conservation movement.
Syst Parasitol (2011) 78:117–122
Fig. 1 DIC micrograph of a sporulated oo¨cyst of Caryospora durrelli n. sp. from the Round Island boa. Abbreviations: R, sporocyst residuum; S, sporozoite. Scale-bar: 10 lm
Description (Figs. 1–4) Oo¨cysts spherical to subspherical, 19.2 9 18.2 (17.5–21 9 16–21) lm, n = 20; shape index (SI; mean length/mean width) 1.05 (1.02–1.09). Bi-layered wall composed of outer layer of c.0.6 thick and inner layer c.0.4 thick. Micropyle, oo¨cyst residuum and polar granule absent. Sporocysts ellipsoidal, 14.7 9 11.0 (13–16 9 9.5–11.5) lm, n = 20; SI 1.33. Stieda body present, c.0.4 high 9 1.6 wide; substieda body present, c.1.2 high 9 2 wide. Sporocyst residuum present, c.12 9 4.5, surrounded by sporozoites and composed of numerous granules. Refractile bodies present but not clearly visible.
Discussion The family Bolyeridae consists of only two species, Casarea dussumieri and Bolyeria multocarinata (Boie´), both of which are endemic to Mauritius; the latter is presumed extinct. To date, no species of coccidia has been described from either bolyerids,
119
and only two species of Caryospora have been described from the Boidae. Oo¨cysts of Caryospora corallae Matuschka, 1984 from the emerald tree boa Corallus caninus (L., 1758) in French Guiana are typically spherical and larger than Caryospora durrelli n. sp. and contain a polar granule. C. corallae is further distinguished by its larger, ovoidal sporocysts, which do not overlap in size ranges of length or width with C. durrelli and contain a clustered, rather than scattered, sporocyst residuum (Matuschka, 1984). Oo¨cysts of C. epicratesi Lainson, Paiva do Nascimiento & Shaw, 1991 from Epicrates cenchria cenchria L. in Brazil are larger and contain a characteristic polar granule often observed adhering to the sporocyst wall. Sporocysts of C. epicratesi are broadly ellipsoidal (SI = 1.4), but are larger and do not overlap with C. durrelli in ranges of length or width. Finally, sporocysts of C. epicratesi contain a ‘stopperlike’ structure, composed of the Stieda and substieda bodies, and a prominent sporocyst residuum which contrasts with the small, indistinct substieda bodies and scattered sporocyst residuum of C. durrelli (see Lainson et al., 1991). Caryospora spp. from reptiles have been shown to have heteroxenous development (Koudela, 1993; Modry´ et al., 2005; Upton et al., 1986; Duszynski & Upton, 2009). Dietary analysis of wild-collected and captive C. dussumieri shows that it feeds on all four endemic Mauritian lizards found on Round Island, i.e. Phelsuma ornata, Leiolopisma telfairii, Scelotes bojerii and Nactus durrelli (see Bullock, 1986; Jones, 1988; Vinson, 1949, 1975), any of which could act as an intermediate host of C. durrelli if it has a heteroxenous life-cycle. One of the aims of this study was to assess whether potentially pathogenic parasites are present in these highly endangered species. There is no evidence in the literature that intestinal Caryospora spp. infections of snakes are pathogenic. However, it is worth noting that under captive conditions a Sarcocystis sp. infection was identified as the cause of death in a bullsnake Pituophis melanoleucus sayi, which had been captured during hibernation and kept at high temperatures (Daszak & Cunningham, 1995). Thus, C. durrelli should be considered as a possible pathogen when attempting differential diagnoses for Casarea dussumieri in captive breeding programmes. The last remaining location for C. dussumieri, Round Island, is an internationally renowned refuge
123
120
Syst Parasitol (2011) 78:117–122
Figs. 2–3 DIC micrographs of a sporulated oo¨cyst of Caryospora durrelli n. sp. from the Round Island boa. Abbreviations: R, sporocyst residuum; SB, Stieda body; S, sporozoite. Scale-bar: 10 lm
Fig. 4 Line drawing of a sporulated oo¨cyst of Caryospora durrelli n. sp. from the Round Island boa. Scale-bar: 10 lm
for Mascarene endemic flora and fauna (Merton et al., 1989). Consequently, significant conservation efforts have been directed at preserving the boa and its
123
habitat (Jones & Hartley, 1995). These have included successful captive-breeding of the snake (Bloxam, 1986), complete eradication of invasive vertebrates (Bell, 2002) and continuing efforts to weed out invasive plants (North et al., 1994). The wild Round Island boa population was estimated at 75 in 1978 (Bullock et al., 1979), with no reliably-determined increase in population up to 1982 (Bullock et al., 1983). The population estimates in 1989 (three years after the removal of rabbits) were of a total Round Island population larger than 185 (Bullock & North, 1991). However, the species remains critically endangered (EN, D on the IUCN Red List; http://www. redlist.org) due to its small population size. The global population of mature adults is likely less than 200 and confined to the single site of Round Island, with a single, small captive colony. Our finding of a new species of likely endemic parasite in this host species highlights two important conservation issues. First, that the parasite Caryospora durrelli is also an endangered species. Snake Caryospora are a fairly host-specific group, apart from some experimental cross-infections (Upton et al., 1986), and the phylogenetic and geographical distance between the Bolyeridae and their nearest
Syst Parasitol (2011) 78:117–122
relatives is large (Cundall & Irish, 1989). This strongly suggests that C. durrelli is, like its host, confined to Round Island and has a total global population that is very small for a coccidian. In fact it is likely that the parasite is under a far greater threat of extinction than its host. Modelling and empirical studies of host-parasite ecology show that, for parasites transmitted in a density-dependent manner (e.g. faecal-oral route), as host populations decline, they reach a threshold density below which the parasite is unable to be transmitted and becomes extinct (McCallum & Dobson, 1995). If the remaining population of Casarea dussumieri undergoes a continued decline, it is possible that Caryospora durrelli will become extinct, even though the snake may remain extant. This situation appears to have occurred for an unidentified Eimeria sp. from the black-footed ferret, which was present when the last few remaining individuals were captured for a captive breeding programme, but has not been seen since (Gompper & Williams, 1998). Furthermore, the proposed reintroduction of Casarea dussumieri to other islands in Mauritius, or to the mainland will likely involve low numbers of founding individuals, with a risk that these do not contain the parasite. It is therefore proposed that Caryospora durrelli should be entered on the IUCN Red List, with the same classification as its host, i.e. critically endangered (EN, D). The conservation of parasites has been largely ignored by conservation organisations, although it has been highlighted in a number of publications (Daszak & Cunningham, 1999; Daszak et al., 2000; Harris, 1983; Stork & Lyal, 1993; Windsor, 1990, 1998). Such discrimination may be a critical error. Conservation of a host without consideration of its endemic parasites may disrupt the often poorly understood ecological interaction between host and parasite in natural populations. It may also leave satellite populations of released individuals vulnerable to the future introduction of the parasite should they lose herd immunity. Finally, as well as being considered by many as a key driver of evolution (Hamilton et al., 1990), parasites are organisms with fascinating life-cycles and evolutionary adaptations that deserve conservation status in their own right. Acknowledgements This work was funded by Fauna and Flora International, The Royal Geographical Society, The
121 Percy Sladen Memorial Fund, The Godman Fund, The Appleyard Fund, Leica Cameras, Kodak Cameras (UK) and the V. Kann Rasmussen Foundation. We are grateful to: the Mauritian Government National Parks and Conservation Service (Director, Yousoof Mungroo) for fieldwork permits; Kirsty Swinnerton, Eshan Dulloo and Peirre de Boucherville Baissac (Mauritius Project of the Durrell Wildlife Conservation Trust); Brian Bell (Wildlife Management International Ltd.); Mike Bell (New Zealand Department of Conservation); Jos Bhuiyan, Jock Marfell, Roger Jackon, Sue Belbin, Jonathan Cook and other volunteers on Raleigh International expedition 93F (teams ‘‘Sharkbait’’, ‘‘Dodo commitments’’, ‘‘Geckoes’’ and ‘‘Weeds’’); John G.E. Lewis, Sheila Lewis, Janet D. Cottingham and Esther Wenman (1995 expedition members); Dr Ralph Manly (Kingston University); Richard Gibson, Simon Tonge, Paul Pearce-Kelly, Dave Clarke and Elspeth Chaplin (Zoological Society of London); John Hartley and Quentin M. Chumley Bloxam (Durrell Wildlife Conservation Trust); Steven North (Scottish Natural Heritage); David Bullock (English Nature); and Nick Arnold (Natural History Museum, London, UK).
References Arnold, E. N. (1980). Recently extinct reptile populations from Mauritius and Reunion, Indian-Ocean. Journal of Zoology, 191, 33–47. Arnold, E. N., & Jones, C. O. (1994). The night geckos of the genus Nactus in the mascarene islands with a description of the distinctive population on Round Island. Dodo, Journal of the Wildlife Preservation Trusts, 30, 119–131. Austin, J. J., Arnold, E. N., & Jones, C. O. (2004). Reconstructing an island radiation using ancient and recent DNA: the extinct and living day geckos (Phelsuma) of the Mascarene Islands. Molecular Phylogenetics and Evolution, 31, 109–122. Bell, B. D. (2002). The eradication of alien mammals from five offshore islands, Mauritius, Indian Ocean. In: L Veitch, C. R., & Clout, M. N. (Eds) Turning the tide: the eradication of invasive species. Gland, Switzerland: IUCN, pp. 40–45. Bloxam, Q. M. C. (1986). The Round Island boa Casarea dussumieri breeding program at the Jersey Wildlife Preservation Trust. Dodo, Journal of the Jersey Wildlife Preservation Trust, 23, 101–107. Bloxam, Q. M. C., & Vokins, A. M. A. (1978). Breeding and maintenance of Phelsuma guentheri (Bouleger, 1885) at the Jersey Zoological Park. Dodo, Journal of the Jersey Wildlife Preservation Trust, 15, 82–91. Bullock, D. J. (1986). The ecology and conservation of reptiles on Round-Island and Gunner Quoin, Mauritius. Biological Conservation, 37, 135–156. Bullock, D. J., & North, S. G. (1991). Leicester Polytechnic Round Island expedition 1989. Leicester Polytechnic, Leicester, UK. Unpublished Report. Bullock, D. J., North, S. G., & Alexander, J. B. (1979). Report of the 1975 and 1978 Edinburgh University expeditions to Round Island (Mauritius). Edinburgh University. Unpublished Report.
123
122 Bullock, D. J., North, S., & Greig, S. (1983). Round Island Expedition 1982. University of St. Andrews. Unpublished Report. Cheke, A. S. (1987). An ecological history of the Mascarene Islands, with particular reference to extinctions and introductions of land vertebrates. In: Diamond, A. W. (Ed.), Studies of Mascarene island birds. Cambridge: Cambridge University Press, pp. 5–90. Cundall, D., & Irish, F. J. (1989). The function of the intramaxillary joint in the Round Island boa, Casarea dussumieri. Journal of Zoology, London, 217, 569–598. Daszak, P. (1994). Report of the Raleigh International expedition to Round Island, 1993. Kingston University, Kingston-upon-Thames, Surrey, UK. Unpublished Report. Daszak, P. (1995). Prevalence of endoparasites in Round Island reptiles. Herpetological Journal, 5, 195–199. Daszak, P. (1996). The 1995 Kingston University expedition to Mauritius - preliminary report. Kingston University, Kingston-upon-Thames, Surrey, UK. Unpublished Report. Daszak, P., & Cunningham, A. A. (1995). A report of intestinal sarcocystosis in the bullsnake (Pituophis melanoleucus sayi) and a re-evaluation of Sarcocystis sp. from snakes of the genus Pituophis. Journal of Wildlife Diseases, 31, 400–403. Daszak, P., & Cunningham, A. A. (1999). Extinction by infection. Trends in Ecology & Evolution, 14, 279. Daszak, P., Cunningham, A. A., & Hyatt, A. D. (2000). Emerging infectious diseases of wildlife - threats to biodiversity and human health. Science, 287, 443–449. Duszynski, D. W., & Upton, S. J. (2009). The biology of the Coccidia (Apicomplexa) of snakes of the world. A scholarly handbook for identification and treatment. CreateSpace; a DBA of On-Demand Publishing LLC, Amazon. Com Inc., 430pp. Gompper, M. E., & Williams, E. S. (1998). Parasite conservation and the black-footed ferret recovery program. Conservation Biology, 12, 730. Hamilton, W. D., Axelrod, R., & Tanese, R. (1990). Sexual reproduction as an adaptation to resist parasites: a review. Proceedings of the National Academy of Sciences, USA, 87, 3566–3573. Harris, E. A. (1983). Helminths in danger: the forgotten few. Parasitology, 87, R29. Jones, C. G. (1988). Round Island boa eats Serpent Island gecko. Oryx, 22, 180. Jones, C. G. (1993). The ecology and conservation of Mauritian skinks. Proceedings of the Royal Society of Arts and Sciences, Mauritius, 5, 71–95. Jones, C. G., & Hartley, J. (1995). A conservation project on Mauritius and Rodrigues: An overview and bibliography. Dodo, Journal of the Wildlife Preservation Trusts, 31, 40–65. Koudela, B. (1993). Experimental transmission of Caryospora bigenetica Wacha et Christiansen, 1982 (Apicomplexa: Eimeriidae) from a rattlesnake, Crotalus atrox, to rodents and pigs. Folia Parasitologica, 40, 81–84. Lainson, R., Paiva do Nascimento, F., & Shaw, J. J. (1991). Some new species of Caryospora (Apicomplexa, Eimeriidae) from Brazilian Snakes, and a re-description of C. jararacae Carini, 1939. Memo´rias do Instituto Oswaldo Cruz, 86, 349–364.
123
Syst Parasitol (2011) 78:117–122 Leinwand, I., Kilpatrick, A. M., Cole, N., Jones, C. G., & Daszak, P. (2005). Patterns of coccidial prevalence in endemic and introduced lizards of Mauritius. Journal of Parasitology, 91, 1103–1108. Lloyd, J. A. (1846). Relation d’un voyage a` 1’Iˆle Ronde et a` 1’Iˆle aux Serpents en de´cembre 1844. Proce`s-Verbaux de la Socie´te´ d’Histoire Naturale de ‘Iˆle Maurice, October 1842 - August 1846, pp. 154–162. Matuschka, F. R. (1984). Caryospora corallae n. sp. (Apicomplexa, Sporozoea, Eimeriidae) from the emerald tree boa Corallus caninus (Serpentes, Boidae). Journal of Protozoology, 31, 358–359. McCallum, H., & Dobson, A. (1995). Detecting disease and parasite threats to endangered species and ecosystems. Trends in Ecology & Evolution, 10, 190–194. Merton, D. V., Atkinson, I. A., Strahm, W., Jones, C. G., Empson, R. A., Mungroo, Y., Dulloo, E., & Lewis, R. (1989). A management plan for the restoration of Round Island, Mauritius. Jersey Wildlife Preservation Trust (currently The Durrell Wildlife Conservation Trust). Unpublished Report. Modry´, D., Sˇlapeta, J. R., & Koudela, B. (2005). Mice serve as paratenic hosts for the transmission of Caryospora duszynskii (Apicomplexa: Eimeriidae) between snakes of the genus Elaphe. Folia Parasitologica, 52, 205–208. North, S. G., Bullock, D. J., & Dulloo, M. E. (1994). Changes in the vegetation and reptile populations on Round-island, Mauritius, following eradication of rabbits. Biological Conservation, 67, 21–28. Pike, N. (1870). A visit to Round Island. Transactions of the Royal Society of Arts and Sciences, Mauritius, N.S., 4, 11–22. Stork, N. E., & Lyal, C. R. C. (1993). Extinction or ‘‘coextinction’’ rates? Nature, 366, 307. Tonge, S. J., & Barlow, S. C. (1985). Aspects of the biology of the Round Island skink, Leiolopisma telfairii. Dodo, Journal of the Jersey Wildlife Preservation Trust, 22, 97–109. Upton, S. J., Current, W. L., & Barnard, S. M. (1986). A review of the genus Caryospora Le´ger, 1904 (Apicomplexa: Eimeriidae). Systematic Parasitology, 8, 3–2 1. Upton, S. J., Freed, P. S., Burdick, D. A., & McAllister, C. T. (1990). Seven new species of coccidia (Apicomplexa, Eimeriorina) from reptiles in Madagascar. Canadian Journal of Zoology, 68, 2368–2375. Vinson, J. (1949). L’Iˆle Ronde et 1’Iˆle aux Serpents. Proceedings of the Royal Society of Arts and Sciences, Mauritius, 1, 32–52. Vinson, J. (1953). Some recent data on the fauna and flora of Round and Serpent Islands. Proceedings of the Royal Society of Arts and Sciences, Mauritius, 1, 253–257. Vinson, J. (1964). Sur la disparation progressive de la faune de 1’Iˆle Ronde. Proceedings of the Royal Society of Arts and Sciences, Mauritius, 2, 247–263. Vinson, J.-M. (1975). Notes on reptiles of Round Island. Bulletin of the Mauritius Institute, 8, 49–67. Vinson, J., & Vinson, J.-M. (1969). The saurian fauna of the Mascarene Islands. 1. A revision of the fauna. Bulletin of the Mauritius Institute, 6, 203–320. Windsor, D. A. (1990). Heavenly hosts. Nature, 348, 104. Windsor, D. A. (1998). Equal rights for parasites. Bioscience, 48, 244.
