Distribution and reproductive plasticity of Gyrinicola batrachiensis (Oxyuroidea: Pharyngodonidae) in tadpoles of five anuran species

Abstract

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.

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Funding

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.

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Correspondence to Matthew G. Bolek.

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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.

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Pierce, C.C., Shannon, R.P. & Bolek, M.G. Distribution and reproductive plasticity of Gyrinicola batrachiensis (Oxyuroidea: Pharyngodonidae) in tadpoles of five anuran species. Parasitol Res 117, 461–470 (2018). https://doi.org/10.1007/s00436-017-5723-4

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Keywords

  • Tadpoles
  • Nematodes
  • Pinworms
  • Development
  • Reproductive strategies