Hymenolepis ackerti n. sp. (Eucestoda: Hymenolepididae) infecting cricetid rodents from the central Great Plains of North America
DOI:
https://doi.org/10.22201/ib.20078706e.2023.94.4927Keywords:
Konza Prairie, Tallgrass prairie, Expected identification, Host unspecificityAbstract
Hymenolepis ackerti n. sp., parasite of rodents from the tallgrass prairie ecoregion of North America is herein
characterized. This tapeworm occurs in 3 species of rodents including the hispid cotton rat Sigmodon hispidus, the
eastern woodrat Neotoma floridana, and the prairie vole Microtus ochrogaster. A comparison against the other 10
congeneric species known from North America reveals that this species is different based on the size of the scolex,
length of rostellar capsule, testicular arrangement, and the size of cirrus sac, seminal receptacle and eggs. A comparison of mitochondrial DNA reveals that tapeworms present in sympatric mammals share the same mitochondrial haplotype and feature similar morphology, supporting their recognition as a single species. The phylogenetic position of H. ackerti relative to other species is still to be resolved, since there are no homologous sequences available for most species in the genus. Given the pervasiveness of these parasites across rodents in the continent, we recommend diligence among scientists to build public archives of tapeworm specimens collected from mammals across North America, and globally. In the present manuscript, we propose a method to sample DNA while still allowing specimens to be postfixed for staining or fluid-preserved for long term storage.
References
Briggs, J. M., Knapp, A. K., Blair, J. M., Heisler, J. L., Hoch, G. A., Lett, M. S. et al. (2005). An ecosystem in transition. Causes and consequences of the conversion of mesic grassland to shrubland. Bioscience, 55, 243–254.
Bruckerhoff, L., Connell, K., Guinnip, J., Adhikari, E., Godar, A., Gido, K. et al. (2021). Harmony on the prairie? Grassland plant and animal community responses to variation in climate across land-use gradients. Ecology, 102, e02986. https://doi.org/10.1002/ecy.2986
Coggins, J. R., & McDaniel, J. S. (1975). Helminth population dynamics in the cotton rat, Sigmodon hispidus. Proceedings of the Oklahoma Academy of Science, 55, 112–118.
Colella, J. P., Bates, J., Burneo, S. F., Camacho, M. A., Bonilla, C. C., Constable et al. (2021). Leveraging natural history biorepositories as a global, decentralized, pathogen surveillance network. Plos Pathogens, 17, e1009583. https://doi.org/10.1371/journal.ppat.1009583
Dunnum, J. L., Yanagihara, R., Johnson, K. M., Armien, B., Batsaikhan, N., Morgan, L. et al. (2017). Biospecimen Repositories and Integrated Databases as Critical Infrastructure for Pathogen Discovery and Pathobiology Research. Plos Neglected Tropical Diseases, 11, e0005133. https://doi.org/10.1371/journal.pntd.0005133
Faulkner, B. C., & Lochmiller, R. L. (2000). Ecotoxicity revealed in parasite communities of Sigmodon hispidus in terrestrial environments contaminated with petrochemicals. Environmental Pollution, 110, 135–145.
https://doi.org/10.1016/S0269-7491(99)00276-6
Galbreath, K. E., Hoberg, E. P., Cook J. A., Armién, B., Bell, K. C., Campbell, M. L. et al. (2019). Building an integrated infrastructure for exploring biodiversity: field collections and archives of mammals and parasites. Journal of Mammalogy, 100, 382–393. https://doi.org/10.1093/jmammal/gyz048
Gardner, S. L. (1985). Helminth parasites of Thomomys bulbivorus (Richardson) (Rodentia: Geomyidae), with the description of a new species of Hymenolepis (Cestoda). Canadian Journal of Zoology, 63, 1463–1469.
Gardner, S. L., & Campbell, M. L. (1992). Parasites as probes for biodiversity. Journal of Parasitology, 78, 596–600.
Gardner, S. L., Dursahinhan, A. T., Campbell, M. L., & Racz, S. E. (2020). A new genus and two new species of unarmed hymenolepidid cestodes (Cestoda: Hymenolepidiciae) from geomyid rodents in Mexico and Costa Rica. Zootaxa, 4766, 358–376. https://doi.org/10.11646/zootaxa.4766.2.5
Gardner, S. L., Luedders, B. A., & Duszynski, D. W. (2014). Hymenolepis robertrauschi n. sp. from grasshopper mice Onychomys spp. in New Mexico and Nebraska, U.S.A. Occassional Papers of the Texas Tech University Museum, 322, 1–10.
Harkema, R. (1946). The Metazoa parasitic in cotton rats of Wake County. Journal of the Elisha Mitchell Scientific Society, 62, 142–143.
Harkema, R., & Kartman, L. (1948). Observations on the helminths and ectoparasites of the cotton rat, Sigmodon hispidus Say and Ord, in Georgia and North Carolina. Journal of the Elisha Mitchell Scientific Society, 64, 183–191.
Haukisalmi, V., Hardman, L. M., Foronda, P., Feliu, C., & Henttonen, H. (2010). Systematic relationships of Mosgovoyia Spasskii, 1951 (Cestoda: Anoplocephalidae) and related genera inferred from mitochondrial and nuclear sequence data. Systematic Parasitology, 77, 71–79.
Hoberg, E. P., Makarikov, A. A., Tkach, V. V., Meagher, S., Nims, T. N., Eckerlin, R. P. et al. (2016). Insights on the host associations and geographic distribution of Hymenolepis folkertsi (Cestoda: Hymenolepididae) among rodents across temperate latitudes of North America. Parasitology Research, 115, 4627–4638.
Hoberg, E. P., & Soudachanh, K. M. (2021). Diversity of Tetrabothriidae (Eucestoda) among Holarctic Alcidae (Charadriiformes): Resolution of the Tetrabothrius jagerskioeldi cryptic species complex —cestodes of Alcinae— provides insights on the dynamic nature of tapeworm and marine bird faunas under the Stockholm Paradigm. MANTER. Journal of Parasite Biodiversity, 16, 1–76. https://doi.org/10.32873/unl.dc.manter16
Hope, A. G. (2019). Small mammal host-parasite sampling data for 16 linear trapping transects located in 8 LTER burn treatment watersheds at Konza Prairie version 3. Environmental Data Initiative. https://doi.org/10.6073/pasta/69109c56fcf21a30a8d37369cb47f8de
Makarikov, A. A., Galbreath, K. E., Eckerlin, R. P., & Hoberg, E. (2020). Discovery of Arostrilepis tapeworms (Cyclophyllidea: Hymenolepididae) and new insights for parasite species diversity from Eastern North America. Parasitology Research,119, 567–585 https://doi.org/https://doi.org/10.1007/s00436-019-06584-4
Makarikov, A. A., Nims, T. N., Galbreath, K. E., & Hoberg, E. P. (2015). Hymenolepis folkertsi n. sp (Eucestoda: Hymenolepididae) in the oldfield mouse Peromyscus polionotus (Wagner) (Rodentia: Cricetidae: Neotominae) from the southeastern Nearctic with comments on tapeworm faunal diversity among deer mice. Parasitology Research, 114, 2107–2117. https://doi.org/10.1007/s00436-015-4399-x
Miller, M. A., Pfeiffer, W., & Schwartz, T. (2010). Creating the CIPRES Science Gateway for inference of large phylogenetic trees. New Orleans: Gateway Computing Environments Workshop (GCE). https://doi.org/10.1109/GCE.2010.5676129
Mollhagan, T. (1978). Habitat influence on helminth parasitism of the cotton rat in western Texas with remarks on some of the parasites [Article]. Southwestern Naturalist, 23, 401–408. https://doi.org/10.2307/3670248
Morgan, J. A. T., & Blair, D. (1998). Relative merits of nuclear ribosomal internal transcribed spacers and mitochondrial CO1 and ND1 genes for distinguishing among Echinostoma species (Trematoda). Parasitology, 116, 289–297.
Nkouawa, A., Haukisalmi, V., Li, T. Y., Nakao, M., Lavikainen, A., Chen, X. W. et al. (2016). Cryptic diversity in hymenolepidid tapeworms infecting humans. Parasitology International, 65, 83–86. https://doi.org/10.1016/j.parint.2015.10.009
Panti-May, J. A., Rodríguez-Vivas, R. I., García-Prieto, L., Servian, A., & Costa, F. (2020). Worldwide overview of human infections with Hymenolepis diminuta. Parasitology Research, 119, 1997–2004. https://doi.org/10.1007/s00436-020-06663-x
Pfaffenberger, G. S., Kemether, K., & Debruin, D. (1985). Helminths of sympatric populations of kangaroo rats (Dipodomys ordii) and grasshopper mice (Onychomys leucogaster) from the high plains of eastern New Mexico. Journal of Parasitology, 71, 592–595. https://doi.org/10.2307/3281429
Rambaut, A. (2012). FigTree v1. 4. Molecular evolution, phylogenetics and epidemiology. Edinburgh: University of Edinburgh, Institute of Evolutionary Biology.
Ratajczak, Z., Briggs, J. M., Goodin, D. G., Luo, L., Mohler, R. L., Nippert, J. B. et al. (2016). Assessing the potential for transitions from Tallgrass Prairie to Woodlands: are we operating beyond critical fire thresholds? Rangeland Ecology & Management, 69, 280–287. https://doi.org/10.1016/j.rama.2016.03.004
Riley, W. A., & Shannon, W. R. (1922). The rat tapeworm, Hymenolepis diminuta, in man. The Journal of Parasitology, 8, 109–117. https://doi.org/10.2307/3270923
Sasaki, M., Anders, J. L., & Nakao, M. (2021). Cestode fauna of murid and cricetid rodents in Hokkaido, Japan, with assignment of DNA barcodes. Species Diversity, 26, 255–272. https://doi.org/10.12782/specdiv.26.255
Seidenberg, A. J., Kelly, P. C., Lubin, E. R., & Buffington, J. D. (1974). Helminths of cotton rat in southern Virginia, with comments on sex-ratios of parasitic nematode populations [Article]. American Midland Naturalist, 92, 320–326. https://doi.org/10.2307/2424297
Sievers, F., Wilm, A., Dineen, D., Gibson, T. J., Karplus, K., Li, W. et al. (2011). Fast, scalable generation of high‐quality protein multiple sequence alignments using Clustal Omega. Molecular Systems Biology, 7, 539.
Smith, C. S., Jones, F. E., & Eyles, D. E. (1953). Three additional Tennessee cases of Hymenolepis diminuta infection in man. Journal of the Tennessee Academy of Science, 28, 196–197.
