Herpetology Notes, volume 7: 779-781 (2014) (published online on 21 December 2014)

First record of Raillietiella affinis Bovien, 1927 (Arthropoda: Raellietiellidae) as an endoparasite of the Madagascan giant day gecko, grandis Gray, 1870 introduced at Reunion Island

Sébastien Dervin1,*, Mickaël Sanchez1, Charles R. Bursey2 and Stephen R. Goldberg3

Pentastomids are wormlike crustacean endoparasites which displays a territorial behavior and an omnivorous usually found in the respiratory system of vertebrates, diet (Glaw and Vences, 2007). This lizard is also known primarily in carnivorous (Kelehear et al., from Hawaii, Florida, Mauritius and Reunion Island, 2011). These endoparasites are known to have a high where it is considered as an invasive (Kraus, potential for zoonotic diseases (Paré, 2008). Raillietiella 2009; Buckland et al., 2014; Sanchez and Probst, 2014). Sambon, 1910 comprised approximately 39 species From Hawaii, it is known to be the host of several that infect mainly small lizards (Kelehear et al., 2011). parasites, including one cestode, three nematodes and Raillietiella affinis is known from Africa, Indonesia one pentastomid Raillietiella frenatus (Goldberg et al., and Hawaii (Christoffersen and De Assis, 2013), and 2010). was described parasitizing lung of the tokay gecko Here we report the first record of R. affinis as an Gekko gecko (Bovien, 1927). It has been then described endoparasite of P. grandis and a new locality for in geckos, Lepidodactylus lugubris (Self and Kuntz, the parasite. Into Mascarenes archipelago alongside 1957), Gehyra mutilata “as Peropus mutilatus” (Nicoli, Mauritius and Rodrigues islands, Reunion Island 1963), Hemidactylus leschenaulti (Haffner, 1964), lies about 700 km east of Madagascar in the Indian Hemidactylus angulatus “as H. brookii angulatus” Ocean. Like many other islands experiencing (Awachie, 1974), in skinks, Chalcides sepsoides and human colonization, Reunion Island endured several Scincus scincus “as S. officinalis” (Self and Kuntz, introductions of alien species (Cheke and 1957), Eumeces shneideri scneideri “as Eumeces Hume, 2008). Introduced in the middle of the 90’s, the schneiderii” (Brygoo, 1963), in agamids, Stellagama expansion and the impacts of P. grandis on Reunion stellio “as Agama stellio” (Brygoo, 1963), Trapelus Island are closely monitored (e.g. Dervin et al., 2013; mutabilis “as Agama mutabilis” (Ali et al., 1982) and Sanchez and Probst, 2014). in the marine toad Rhinella marina “as Bufo marinus” Eight P. grandis (mean Snout-Vent Length, SVL = (Eldredge, 2000). 98 mm ± 10 SD, range = 76-107 mm) were collected Native from Madagascar, Phelsuma grandis Gray, from five populations around Reunion Island between 1870 (Fig. 1a) is a large diurnal and arboreal gecko September 2010 and May 2013 (four populations in western coast and one population in north east coast; Fig. 2). The lizards were manually caught and, according to a legal destruction agreement, were euthanized by freezing. 1 Association Nature Océan Indien, 6 Lotissement les Endoparasites were removed from trachea and lungs Magnolias, Rivière des Roches 97470 Saint-Benoît, Ile de La (Fig. 1b and 1c). All the eight geckos were parasitized Réunion, France. and 69 parasites, all at adult stage, were found (mean 2 Pennsylvania State University, Shenango University, = 8.62 ± 8.12 SD, range = 1-21). Pentastomids were Department of Biology, Sharon, Pennsylvania 16146, USA. cleared in a few drops of lactophenol on a glass 3 Whittier College, Department of Biology, Whittier, California microscope slide, cover slipped and studied utilizing 90608, USA. *Corresponding author e-mail: [email protected] a binocular microscope (Leica ATC 2000). They were 780 Sébastien Dervin et al.

Figure 1. a) Adult P. grandis on Pandanus utilis; b) ventral dissection of P. grandis where parasites, indicated by dark arrows, are visible through the left lung; c) an extracted parasite. Photos: a) and c) M. Sanchez, b) S. Dervin.

identified as Raillietiella affinis based upon the presence The present paper reports a new host and a new of blunt posterior hooks and the male copulatory spicule distribution for R. affinis. It also emphasizes that exhibiting a flared base devoid of ornamentation. conservation issues could occur in a local context of Raillietiella species have a life cycle which can include biological invasion between P. grandis and endemic two hosts. Eggs are released through the feces of the threatened geckos of Reunion Island (Phelsuma definitive host and they are ingested by the intermediate inexpectata and P. borbonica; UICN France et al., host (Ali and Riley, 1983). In some cases, cockroaches may be used as intermediate host by the parasite (Paré, 2008). On Reunion Island, P. grandis consumes a large amount of Blattidae (Dervin et al., 2013). We suggest that these coprophagous insects could be used as intermediate host by R. affinis on Reunion Island. When the intermediate host is consumed by a suitable definitive host for the parasite, this last one migrates to the respiratory system of its host where it will feed on blood (Paré, 2008). Previous studies have already shown the ability of Raillietiella species for switching its definitive host (e.g. from a gekkonid species, Hemidactylus frenatus to a bufonid species, Rhinella marina), possibly leading to enhance the spread of the parasite (Barton, 2007; Kelehear et al., 2013). The bufonid Amietophrynus gutturalis and the gekkonid H. frenatus are both alien species widely distributed through Reunion Island (Cheke and Hume, 2008). Thus, we believe they could carry the potential for spreading the parasite outside of the current distribution of P. Figure 2. Sampling sites of P. grandis on Reunion Island. The grandis. associated numbers to sites are relative to the quantity of P. grandis that we captured and dissected. First record of Raillietiella affinis as an endoparasite of Phelsuma grandis 781

2013), through the introduction of an endoparasite to Dervin, S., Baret, S., Penin, L., Sanchez, M. (2013): Régime an island possibly free of this parasite. Further studies alimentaire du grand gecko vert de Madagascar, Phelsuma should focus on the natural prevalence of R. affinis in grandis Gray, 1870 sur l’île de La Réunion ( : ). Cahiers scientifiques de l’océan Indien occidental the populations of the native Reunion day geckos, at 4: 29-38. places free of P. grandis. Also, evaluating the presence Eldredge, L.G. (2000): Number of Hawaiian species. Supplement of the parasite in the populations of alien reptiles and 5. Records of the Hawaii Biological Survey for 1999. Bishop amphibians could lead to a better understanding of the Museum Occasional Papers 63: 3-8. spread mechanisms of R. affinis on Reunion Island. Glaw, F., Vences, M. (2007): A Field Guide to the Amphibians and Reptiles of Madagascar, 3rd Edition. Vences & Glaw, Ed., Acknowledgements. The authors would like to thank Matthieu Germany. Le Corre and Lucie Penin for improving an earlier version Goldberg, S.R., Bursey, C.R., Kraus, F. (2010): Helminth records of this paper and Samuel Baret for the specimen collection. for the Madagascan giant day gecko, Phelsuma grandis The study was supported by the Direction de l’Environnement (Gekkonidae) from Hawaii. Bishop Museum Occasional Papers de l’Aménagement et du Logement de La Réunion. Also, we 108: 49-52. would like to thank the two anonymous reviewers for the last Haffner, K.von (1964): Ein Beitrag zur Kenntnis der improvements of this paper. Pentastomidea. Der Hakernapparat, die Hautmuskulatur und die Parapodiallappen von Railietiella affinis Bouvien, 1927. Mitteilungen aus dem Staatsinstitut und Zoologischen Museum References in Hamburg, Kosswig-Festschrift 1964: 51-58. Ali, J.H., Riley, J. (1983): Experimental life-cycle studies of Kelehear, C., Brown, G.P., Shine, R. (2013): Invasive parasites Raillietiella gehyrae Bovien, 1927 and Raillietiella frenatus Ali, in multiple invasive hosts: the arrival of a new host revives a Riley and Self, 1981: pentastomid parasites of geckos utilizing stalled prior parasite invasion. Oikos 122: 1317-1324. insects as intermediate hosts. Parasitology 86: 147-160. Kelehear, C., Spratt, D.M., Dubey, S., Brown, G.P., Shine, Ali, J.H., Riley, J., Self, J.T. (1982): A description of a new species R. (2011): Using combined morphological, allometric and of Raillietiella (Pentastomida: Cephalobaenida) from Egyptian molecular approaches to identify species of the Raillietiella lizards with a reassessment of the taxonomic status of Raillietiella (Pentastomida). PLoS ONE 6(9): e24936. geckonis (Diesing, 1850) Sambon, 1910 and Raillietiella affinis Kraus, F. (2009): Alien reptiles and amphibians: a scientific Bovien, 1927. Systematic Parasitology 4: 169-180. compendium and analysis, 4th Edition. Springer Verlag, Ed., Awachie, J.B.E. (1974): On the pathogenic effects of Raillietiella Germany. affinis Bovien (Pentastomida) on the house wall gecko Nicoli, R.M. (1963): Phylogenèse et systématique. Le phylum des (Hemidactylus brookii angulatus Hallowell) with note on the Pentastomida. Annales de Parasitologie Humaine et Comparée aetiology of human porocephalosis in Africa. Proceedings of the 38: 483-516. Third International Congress in Parasitology 2: 1024-1025. Paré, J.A. (2008): An overview of pentastomiasis in reptiles and Barton, D.P. (2007): Pentastomid parasites of the introduced Asian other vertebrates. Journal of Exotic Pet Medicine 17: 285-294. house gecko, Hemidactylus frenatus (Gekkonidae), in Australia. Sanchez, M., Probst, J.-M. (2014): Distribution and habitat of the Comparative Parasitology 74: 254-259. invasive giant day gecko Phelsuma grandis Gray 1870 (Sauria: Bovien, P. (1927): Ueber einige Pentastomen aus Java. Berichtigung Gekkonidae) in Reunion Island, and conservation implication. Videnskabelige Meddelelser fra den Dansk Naturhistoriske Phelsuma 22: 13-28. Forening i Kjøbenhavn 84: 1-12. Self, J.T., Kuntz, R.E. (1957): Pentastomids from African reptiles Brygoo, E.R. (1963): Contribution à la connaissance de la and mammals and from reptiles of Florida Island, British parasitologie des caméléons malgaches. Annales de Parasitologie Solomon Islands (South Pacific). Journal of Parasitology 43: Humaine et Comparée 38: 149-334, 525-739 [Pentastomida p. 194-200. 195-203]. UICN France, MNHN, SEOR, ARDA, Insectarium de La Réunion, Buckland, S., Cole, N.C., Aguirre-Gutiérrez, J., Gallagher, L.E., GLOBICE, Kélonia (2013): La Liste rouge des espèces menacées Henshaw, S.M., Besnard, A., Tucker, R.M., Bachraz, V., en France - Chapitres Faune de La Réunion. Paris, France. Ruhomaun, K., Harris, S. (2014): Ecological Effects of the Invasive Giant Madagascar Day Gecko on Endemic Mauritian Geckos: Applications of Binomial-Mixture and Species Distribution Models. PLoS ONE 9(4): e88798. Cheke, A., Hume, J. (2008): Lost land of the Dodo – An ecological history of Mauritius, Réunion & Rodrigues. T & Ad Poyser, Ed., London. Christoffersen, M.L., De Assis, J.E. (2013): A systematic monograph of the recent Pentastomida, with a compilation of their hosts. Naturalis Biodiversity Center. Zoologische Accepted by Diogo Provete; Mededelingen Leiden 87: 1-206. Managing Editor: Alessandro Morais