Helminths from Emoia physicae (Squamata: Scincidae) from Papua New Guinea

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1 Helminths from Emoia physicae (Squamata: Scincidae) from Papua New Guinea By Stephen R. Goldberg*, Charles R. Bursey and Fred Kraus Abstract Twenty-one specimens of the scincid lizard, Emoia physicae, from Papua New Guinea were examined for gastrointestinal helminths. Found were two species of Cestoda, Cylindrotaenia hickmani and Ophiotaenia greeri and five species of Nematoda: Skrjabinodon derooijae, Skrjabinodon sheai, Abbreviata sp., Porrocaecum sp., and Rictulariidae gen. sp. Rictulariidae had the highest prevalence (29%) and Porrocaecum sp. had the greatest mean intensity (21.5 ± 9.2). Emoia physicae are infected by generalist helminths that also infect other species. Three helminth species are endemic to Papua New Guinea (O. greeri. S. derooijae, S. sheai); one is known from Australia, Papua New Guinea and Oceania (C. hickmani); and three are paratenic larvae belonging to widely distributed groups (Abbreviata sp., Porrocaecum sp., Rictulariidae). All are new host records for E. physicae. * Corresponding Author sgoldberg@whittier.edu Pacific Science, vol. 72, no. 3 January 27, 2018 (Early View)

2 Introduction The very rich biodiversity of Papua New Guinea is threatened by a variety of factors including habitat loss, invasion by alien species, harvesting for food, medicine, fuel, and the pet trade; and atmospheric, land and water pollution, all of which imperil the continued existence of much of its fauna (Frazier 2007). In view of these threats it is important to conduct studies to collect biological and ecological information on plants and animals of this region while they remain extant. This would also include gathering information on associated invertebrate biodiversity, including parasites, because it is likely that helminth faunas will also decline, along with their hosts, in some cases, to extinction. A total understanding of the biology of an organism requires knowledge of the parasites it may support. Previous studies on the helminth fauna of large numbers of species, from select areas, for examples: (Bursey et al. 2001) from Peru and (Goldberg et al. 2009a) from Papua New Guinea are valuable as they document the helminth fauna at one point in time. They can thus serve as baseline data for subsequent studies in the same geographic areas under future environmental conditions. Our current study will serve the same purpose. Faunal baselines taken from groups of biological specimens become a permanent record of the biosphere when accessioned into museum collections (Hoberg 2010) The family Scincidae is widespread in the Papuan region (New Guinea and associated offshore islands, Admiralty Islands, Bismarck Islands, and Solomon Islands), with at least 171 species known from there (Allison and Kraus 2011). With the above in mind, we add to the list of helminths already reported from the scincid lizard Emoia physicae, which is known from southeastern New Guinea where it occurs across most of the island (Allison and Kraus 2011). Goldberg et al. (2008) previously reported Nematoda from E. physicae: Abbreviata oligopapillata, Hedruris hanleyae, Meteterakis crombiei, Physalopteroides milnensis, and Pseudorictularia disparilis. Here we supplement that initial helminth list with additional species. 2

3 MATERIALS AND METHODS Twenty-one Emoia physicae from the vicinity of Mount Victory, Oro (= Northern) Province, ( S, E, 530 m elevation), Papua New Guinea were collected by hand, September 2010, killed by an overdose of sodium pentobarbital, fixed in 10% buffered formalin, stored in 70% ethanol, and deposited into the herpetology collection at the Bernice P. Bishop Museum BPBM, Honolulu, Hawaii as BPBM and Body cavities were opened by a longitudinal incision, and the gastrointestinal tract was removed (esophagus to rectum) at the Bishop Museum and shipped to Whittier College, Whittier, California for helminthological examination. The digestive tract was slit longitudinally and examined under a dissecting microscope. Nematodes were cleared in lactophenol, examined under a compound microscope, and identified to genus using keys in Anderson et al. (2009) and Gibbons (2010) and to species by comparison with the original descriptions. Cestodes were regressively stained in hematoxylin, cleared in xylol, mounted in Canada balsam on a glass slide, coverslipped and studied as whole mounts. Helminths were deposited in the Harold W. Manter Laboratory (HWML), University of Nebraska, Lincoln. Reptilian taxonomy follows Uetz et al. (2017). Parasite terminology is in accordance with Bush et al. (1997); prevalence (number infected individuals/number examined X 100), mean intensity is reported as average intensity of a parasite species among infected hosts. RESULTS We obtained a total of 111 helminths representing two species of Cestoda: Cylindrotaenia hickmani (Jones, 1985) (from the small intestine), Ophiotaenia greeri (Bursey, Goldberg and Kraus, 2006) (small intestine), and five species of Nematoda: Skrjabinoptera derooijae Bursey, Goldberg, and Kraus, 2008, (small intestine), Skrjabinoptera sheai Bursey, Goldberg and Kraus, 2008 (small intestine), Abbreviata sp. (stomach wall), Porrocaecum sp. (stomach, small 3

4 intestine), Rictulariidae (stomach wall) were found (Table 1). Accession numbers for these helminths are: Cestoda, Cylindrotaenia hickmani (HWML ); Ophiotaenia greeri (HWML ); Nematoda: Skrjabinodon derooijae (HWML ); Skrjabinodon sheai (HWML ); Abbreviata sp. (HWML ); Porrocaecum sp. (HWML ); Rictulariidae (HWML ). All are new host records for E. physicae. DISCUSSION Emoia physicae is infected by generalist helminths that also infect other species. Cylindrotaenia hickmani (originally Barietta hickmani) was described from the Australian scincid lizards, Lampropholis delicata, L. guichenoti, Anepischetosia maccoyi (as Nannoscincus maccoyi), Saproscincus challengeri and S. mustelinus (Jones M.K 1985, 1987). It was reported from Papua New Guinea in the following skinks: Emoia jakati, E. longicauda, E. obscura, E. pallidiceps, E. popei by Goldberg et al. (2008) and Sphenomorphus aignanus and S. louisiadensis (Goldberg et al. 2009b) as well as E. caruleocauda from the Northern Mariana islands, Oceania (Goldberg et al. 2011). The life cycle of C. hickmani is not known; however, the congener C. americana is believed to have a direct life cycle with embryonated eggs ingested by the definitive host (Joyeux 1927). Ophiotaenia greeri (as Adenobrechmos greeri) was described by Bursey et al. (2006) from the skink Sphenomorphus aignanus from Papua New Guinea. It was moved to Ophiotaenia by de Chambrier et al. (2009). Ophiotaenia greeri was also found in the skinks S. cinereus (Bursey et al. 2015), Carlia eothen, C. luctuosa (Goldberg et al. 2010) and E. obscura, E. pallidiceps, and S. louisadensis (Goldberg et al. 2008). The life cycle of Ophiotaenia greeri is unstudied, but Mead and Olsen (1971) demonstrated the congener O. filaroides to have an indirect life cycle in which copepods serve as intermediate hosts. An intermediate host for O. greeri remains to be determined. 4

5 Skrjabinodon derooijae was described from the skink Papuascincus stanleyanus, and S. sheai was described from another skink, Emoia pallidiceps, both from Central Province, Papua New Guinea, by Bursey et al. (2008). Skrjabinodon sheai was also found in the skinks Emoia caeruleocauda from the Northern Mariana Islands (Goldberg et al. 2011) and Prasinohaema flavipes from Papua New Guinea by Goldberg et al. (2016). Both S. derooijae and S. sheai are members of the Oxyurida which have direct (monoxenous) life cycles (Anderson 2000). Infection presumably results from ingestion of fecal-contaminated substrate during feeding. Individuals of Abbreviata sp. are commonly found encysted as larvae in the stomach walls of snakes, lizards (Jones H.I. 1995) and anurans (McAllister et al. 1995). Reptiles are considered paratenic (= transport) hosts since no further development occurs. Development to the adult takes place when the reptile or amphibian carrying the encysted Abbreviata sp. is eaten by a definitive host. Species of Abbreviata have indirect life cycles in which arthropods are intermediate hosts which was demonstrated for A. hastaspicula in Australian lizards by King and Jones (2016). Although A. oligopapillata was previously identified from adult nematodes taken from Emoia physicae collected in Papua New Guinea (Goldberg et al. 2008), the current individuals (larvae in cysts) cannot be assigned to species because identification to species is based on adult male characters, i.e. spicules and caudal ornamentation surrounding caudal papillae. Roca (1993) suggested that prevalence of encysted larval nematodes in a lizard population indicates their degree of importance as prey because lizards can serve as transport hosts, while unencysted larvae represent a normal infection process. For this reason, we believe the Abbreviata sp. found here is other than A. oligopapillata. Species of Porrocaecum are widely distributed parasites in the intestines of birds (Anderson, 2000). Eggs passed in bird feces hatch when ingested by earthworms. Definitive hosts may become infected by eating infected earthworms or infected vermivores (Anderson 5

6 2000). Reptiles should be considered paratenic (= transport hosts) as further development beyond the larval stage does not occur. Species of Rictulariidae are parasites of aquatic birds that use arthropods as intermediate hosts (Anderson 2000). Reptiles and amphibians serve as paratenic hosts, with development to the adult occurring when the reptile is eaten by a carnivorous bird. In summary, seven additional helminth species are reported from E. physicae. These combined with five different helminth species (Abbreviata oligopapillata, Hedruris hanleyae, Meteterakis crombiei, Physalopteroides milnensis, Pseudorictularia dipsarilis) previously reported in Goldberg et al. (2008), bring the total number of helminth species known to infect E. physicae to twelve. The different helminth species reported in E. physicae (Goldberg et al. 2008) were from three other provinces of Papua New Guinea (Central, Milne Bay, Morobe) and may reflect geographic differences in helminth distributions. With reference to the seven species of helminths reported herein, three are endemic to New Guinea (O. greeri, S. derooijae, S. sheai); one is known from Australia, New Guinea, and Oceania (C. hickmani) and three are widely distributed paratenics from two genera Abbreviata sp., Porrocaecum sp., and one family Rictulariidae (see Anderson 2000). Helminthological examinations of many additional scincids are needed before the helminth diversity of the Scincidae in the Papuan region can be adequately ascertained. 6

7 Literature Cited Allison, A., and F. Kraus Checklist of the Amphibians and Reptiles of the Papuan Region (pbs.bishop museum. org/papuanherps.taxa.html)(accessed 3 October 2017). Anderson, R. C Nematode parasites of vertebrates: Their development and transmission. 2nd ed. CABI Publishing, Oxon, United Kingdom. Anderson, R. C., A. G. Chabaud, and S. Willmott, eds Keys to the nematode parasites of vertebrates. Archival Vol. CABI Publishing, Wallingford, Oxfordshire, United Kingdom. Bursey, C. R., S. R. Goldberg, and J. R. Parmelee Gastrointestinal helminths of 51 species of anurans from Reserva Cuzco Amazónico, Peru. Comp. Parasitol. 68: Bursey, C. R., S. R. Goldberg, and F. Kraus New genus, new species of Cestoda (Proteocephalidae) from the lizard Sphenomorphus aignanus (Squamata: Scincidae) from Papua New Guinea. Comp. Parasitol. 73: Bursey, C. R., S. R. Goldberg, and F. Kraus Gastrointestinal helminths from two species of skink from Papua New Guinea, including two new species of Skrjabinodon (Nematoda, Pharyngodonidae). Acta Parasitol. 53: Bursey, C. R., S. R. Goldberg, and F. Kraus Gastrointestinal helminths of seven species of Sphenomorphus (Squamata: Scincidae) from Papua New Guinea with description of a new species of Entomelas. Comp. Parasitol. 82: Bush, A. O., K. D. Lafferty, J. M.Lotz, and A. W. Shostak Parasitology meets ecology on its own terms: Margolis et al. revisited. J. Parasitol. 83: de Chambrier, A., S. C., Coquille, J., Mariaux, and V. Tkach Redescripton of Testudotaenia testudo (Magath, 1924) (Eucestoda: Proteocephalidea), a parasite of Apalone spinifera (Le Sueur) (Reptilia: Trionychidae) and Amia calva L. (Pisces: 7

8 Amiidae) in North America and erection of the Testudotaeniinae n. subfam. Systematic Parasitol. 73: Frazier, S Threats to Biodiversity.Pages in: A. J. Marshall and B. M. Beehler, eds. The Ecology of Papua, Part two, The Ecology of Indonesia Series, Volume VI. Periplus Editions, Singapore. Gibbons, L. M Keys to the nematode parasites of vertebrates. Supp. Vol. CABI Publishing, Wallingford, Oxon, United Kingdom. Goldberg, S. R., C. R. Bursey, and F. Kraus Gastrointestinal helminths of eleven species of Emoia (Squamata: Scincidae) from Papua New Guinea. J. Nat. Hist. 42: Goldberg, S. R., C. R. Bursey, and F. Kraus. 2009a. Helminths of 26 species of microhylid frogs (Anura: Microhylidae) from Papua New Guinea. J. Nat. Hist. 43: Goldberg, S. R., C. R. Bursey, and F. Kraus. 2009b. Endoparasites in 12 species of Sphenomorphus (Squamata: Scincidae) from Papua New Guinea. Comp. Parasitol. 76: Goldberg, S. R., C. R. Bursey, and F. Kraus Metazoan endoparasites of 14 species of skinks (Squamata: Scincidae) from Papua New Guinea. J. Nat. Hist. 44: Goldberg, S.R., C. R. Bursey, and F. Kraus Helminths of Emoia caeruleocauda (Squamata: Scincidae) from the northern Mariana Islands, Micronesia. J. Nat. Hist. 45: Goldberg, S. R., C. R. Bursey, and F. Kraus Gastrointestinal helminths of two species of skinks: Emoia veracunda and Prasinohaema flavipes (Squamata: Scincidae) from Papua New Guinea. Comp. Parasitol. 83: Hoberg, E. P Invasive processes, mosaic and the structure of helminth parasite faunas. Rev. Sci. Tech. 29:

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10 Table 1. Number (N), Prevalence as percent (P), Mean intensity (MI ± 1 SD) and Range for helminths in 21 Emoia physicae from Papua New Guinea; * = no mean intensity or range for one infected E. physicae. Cestoda N P MI ± 1 SD Range Cylindrotaenia 24 5 * * hickmani Ophiotaenia greeri ± Nematoda Skrjabinodon derooijae ± Skrjabinodon sheai ± Abbreviata sp. 2 5 * * Porrocaecum sp ± Rictulariidae ±