Distribution and reproductive plasticity of Gyrinicola batrachiensis (Oxyuroidea: Pharyngodonidae) in tadpoles of five anuran species
Previous studies on Gyrinicola batrachiensis indicate that these pinworms have distinct reproductive strategies dependent on the development time to metamorphosis of their anuran tadpole hosts. In tadpoles of amphibian species with short developmental periods (a few weeks), female nematodes reproduce parthenogenetically, and only produce thick-shelled eggs used as transmission agents from tadpole to tadpole. In contrast, nematodes in tadpoles with longer larval developmental periods (months to years) reproduce by haplodiploidy, and females produce thick-shelled as well as autoinfective thin-shelled eggs. However, recent investigations on the haplodiploidy strain of G. batrachiensis indicate that plasticity exists in the ability of these nematodes to produce thin-shelled autoinfective eggs when these nematodes infect tadpoles of co-occurring amphibian species. Yet, little information is available on the potential mechanism for this reproductive plasticity because few co-occurring amphibian species have been examined for the reproductive strategies of these nematodes. Therefore, our goals were to document field host specificity and reproductive strategies of nematode populations in tadpoles of five co-occurring amphibian species that varied in their larval developmental periods. Additionally, we evaluated adult worm morphology from each infected amphibian species to assess any differences in worm development and reproductive strategy of pinworm populations in different amphibian species. Of the five amphibian species examined, four were infected with the haplodiploid strain of G. batrachiensis. Prevalence of G. batrachiensis ranged from a high of 83% in Acris blandchardi to a low of 15% in Pseudacris clarkii; whereas mean intensity was highest for Rana sphenocephala (10 ± 10.36) and lowest for Hyla chrysoscelis (3.23 ± 3.35). Prevalence appeared to be controlled by tadpole ecology and life history, while mean intensity appeared to be controlled by tadpole physiology and worm reproductive strategy, but not necessarily the developmental period of each anuran species. G. batrachiensis observed in long developing tadpoles of R. sphenocephala had high mean intensities and conformed to the haplodiploidy reproductive strategy with both male and female worms being present, and females produced thick-shelled and thin-shelled eggs. In contrast, tadpoles of A. blanchardi, H. chrysoscelis, and P. clarkii, which varied in their developmental times from long to short, had relatively low mean intensities and contained both male and female G. batrachiensis. However, female worms only produced thick-shelled eggs in these hosts. Importantly, morphological differences existed among female worms recovered from R. sphenocephala and female worms recovered from A. blanchardi tadpoles with long developmental periods. These data strongly suggest that when the haplodiploidy strain of G. batrachiensis is shared by tadpoles of different amphibian species, species-specific differences in interactions between these nematodes and their development in different amphibian host species have a strong influence on the reproductive plasticity of these nematodes.
KeywordsTadpoles Nematodes Pinworms Development Reproductive strategies
Partial support for this project was made possible with student research grants from the Southwestern Association of Parasitologists to C.C.P. and by the National Science Foundation award numbers DEB-0949951 to M.G.B.
Compliance with ethical standards
This research was conducted under the Oklahoma State University Institutional Animal Care and Use Committee protocols AS-13-6, and AS-11-14; all animals were collected under the Oklahoma Department of Wildlife Conservation Special License numbers 6609 to M.G.B. and 6626 to C.C.P.
- Altig R, McDiarmid RW (2015) Handbook of larval amphibians of the United States and Canada. Comstock PublishingAssociates, Cornell University Press, 345 pGoogle Scholar
- Altig R, McDiarmid RW, Nichols KA, Ustach PC (2008) Tadpoles of the United States and Canada: a tutorial and key. http://www.pwrc.usgs. gov/tadpole/
- Araujo P, Artigas PT (1982) Gyrinicola chabaudi n. sp. (Nematoda, Pharyngodonidae), oxiudídeo encontrado en girinos. Mem. Inst. Butantan (São Paulo) 44(45):383–390Google Scholar
- Bursey CR, Dewolf FW (1998) Helminths of the frogs, Rana catesbeiana, Rana clamitans, and Rana palustris, from Coshocton County, Ohio. Ohio J Sci 98:28–29Google Scholar
- Bush AO, Lafferty KD, Lotz JM, Shostak AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol 96:724–735Google Scholar
- Childress JN, Rogers SC, Bolek MG, Langford GJ (2017) Reproductive plasticity in the nematode Gyrinicola batrachiensis: does an intermediate reproductive strategy exist in sexually reproducing, didelphic pinworms? J Parasitol 103. https://doi.org/10.1645/17-30
- Dinnik JA (1930) Data on the fauna of the freshwater parasitic worms in the Caucasus. Raboty Severo-Kavkazskoi gidrobiologicheskoi stantsii pri Gorskom sel’sko-khoziaistvennom Institute 3:87–90Google Scholar
- Dodd KC Jr (2013) Frogs of the United States and Canada. The Johns Hopkins University Press, Baltimore, 982 pGoogle Scholar
- Gosner KL (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16:183–190Google Scholar
- Grimm LG, Yarnold PR (1995) Reading and understanding multivariate statistics. American Psychological Association, Washington, DC, 373 pGoogle Scholar
- Heyer WR (1976) Studies in larval amphibian habitat partitioning. Smithson Contrib Zool 242:1–36Google Scholar
- McDiarmid RW, Altig R (1999) Tadpoles: the biology of anuran larvae. The University of Chicago press, Chicago, 444 pGoogle Scholar
- Planade B, Bain O, Lena MP, Joly P (2008) Gyrinicola chabadamsoni n. sp. and G. tba (Dinnik 1933) (Nematoda, Oxyuroidea) from tadpoles of the hybridogenetic complex Rana lessonae-esculenta (Amphibia, Ranoidea). Zootaxa 1764:25–40Google Scholar
- Sokal RR, Rohlf JF (1981) Biometry, Second edn. W. H. Freeman and Company, New York, 859 pGoogle Scholar
- StatSoft Inc. (2011) STATISTICA data analysis software system (v 10). http://www.statsoft.com
- Stigge HA, Bolek MG (2016b) Evaluating the biological and ecological factors influencing transmission of larval digenetic trematodes: a test of second intermediate host specificity of two North American Halipegus species. J Parasitol 102(6):613–621. https://doi.org/10.1645/15-891 CrossRefPubMedGoogle Scholar
- Yuan ZH, Zhou WW, Chen X, Jtr PNS, Chen HM, Jang-Liaw NH, Chou WH, Matzke NJ, Iizuka K, Min MS, Kuzmin SL, Zhang YP, Cannatella DC, Hillis DM, Che J (2016) Spatiotemporal diversification of the true frogs (genus Rana): a historical framework for a widely studied group of model organisms. Syst Biol 65(5):824–842. https://doi.org/10.1093/sysbio/syw055 CrossRefPubMedGoogle Scholar
- Yamaguti S (1938) Studies on helminth fauna of Japan. Two new species of amphibian nematodes. Jap J Zool 7:603–607Google Scholar