Hostname: page-component-586b7cd67f-vdxz6 Total loading time: 0 Render date: 2024-11-23T22:42:42.130Z Has data issue: false hasContentIssue false

Patterns of Clinostomum marginatum infection in fishes and amphibians: integration of field, genetic, and experimental approaches

Published online by Cambridge University Press:  04 March 2019

D.M. Calhoun*
Affiliation:
Department of Ecology and Evolutionary Biology, University of Colorado, Ramaley N122 CB334, Boulder, CO 80309, USA
K. L. Leslie
Affiliation:
Department of Ecology and Evolutionary Biology, University of Colorado, Ramaley N122 CB334, Boulder, CO 80309, USA
T.B. Riepe
Affiliation:
Department of Ecology and Evolutionary Biology, University of Colorado, Ramaley N122 CB334, Boulder, CO 80309, USA
T.J. Achatz
Affiliation:
Department of Biology, University of North Dakota, Grand Forks, ND 58202-9019, USA
T. McDevitt-Galles
Affiliation:
Department of Ecology and Evolutionary Biology, University of Colorado, Ramaley N122 CB334, Boulder, CO 80309, USA
V.V. Tkach
Affiliation:
Department of Biology, University of North Dakota, Grand Forks, ND 58202-9019, USA
P.T.J. Johnson
Affiliation:
Department of Ecology and Evolutionary Biology, University of Colorado, Ramaley N122 CB334, Boulder, CO 80309, USA
*
Author for correspondence: D.M. Calhoun E-mail: [email protected]

Abstract

Digenetic trematodes of the genus Clinostomum are cosmopolitan parasites infecting fishes, amphibians, reptiles, and snails as intermediate hosts. Despite the broad geographical distribution of this genus, debate about the number of species and how they vary in host use has persisted. To better understand patterns of infection among host species and across life stages, we used large-scale field surveys and molecular tools to examine five species of amphibians and seven species of fishes from 125 California ponds. Among the 12,360 examined hosts, infection was rare, with an overall prevalence of 1.7% in amphibians and 9.2% in fishes. Molecular evidence indicated that both groups were infected with Clinostomum marginatum. Using generalized linear mixed effects models, host species identity and host life stage had a strong influence on infection status, such that Lepomis cyanellus (green sunfish) (49.3%) and Taricha granulosa (rough skinned newt) (9.2%) supported the highest overall prevalence values, whereas adult amphibians tended to have a higher prevalence of infection relative to juveniles (13.3% and 2.5%, respectively). Experimentally, we tested the susceptibility of two amphibian hosts (Pseudacris regilla [Pacific chorus frog] and Anaxyrus boreas [western toad]) to varying levels of cercariae exposure and measured metacercariae growth over time. Pseudacris regilla was 1.3× more susceptible to infection, while infection success increased with cercariae exposure dose for both species. On average, metacarcariae size increased by 650% over 20 days. Our study highlights the importance of integrating field surveys, genetic tools, and experimental approaches to better understand the ecology of host–parasite interactions.

Type
Research Paper
Copyright
Copyright © Cambridge University Press 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abidi, SMA et al. (1988) Clinostomum complanatum: tegumental surface changes during in vivo development. International Journal for Parasitology 18, 433439.Google Scholar
Adeyemo, AO and Agbede, SA (2008) Histopathology of tilapia tissues harbouring Clinostomum tilapiae parasites. African Journal of Biomedical Research 11, 115118.Google Scholar
Aho, JM (1990) Helminth communities of amphibians and reptiles: comparative approaches to understanding patterns and processes. In Esch, GW, Bush, AO and Aho, JM (eds), Parasite Communities: Patterns and Processes. London: Chapman and Hall, pp. 157195.Google Scholar
Anderson, RC, Chabaud, AG and Willmott, S (2009) Keys to the Nematode Parasites of Vertebrates: Archival Volume. London: CABI.Google Scholar
Bates, D et al. (2015) Parsimonious mixed models. arXiv preprint arXiv:1506.04967.Google Scholar
Bear, J (1933) Note sur un noureau trematode, Clinostomum lophophallum sp. nov. Revue Suisse de Zoologie 40, 312347.Google Scholar
Becker, DA and Cloutman, DG (1975) Parasites of selected gamed fishes of Lake Fort Smith, Arkansas. Journal of the Arkansas Academy of Science 29, 1218.Google Scholar
Belliappa, AB (1944) On a species of Clinostomum in a cat. Indian Veterinary Journal 21, 101102.Google Scholar
Belló, ARR et al. (2000) Lipid peroxidation induced by Clinostomum detruncatum in muscle of the freshwater fish Rhamdia quelen. Diseases of Aquatic Organisms 42, 233236.Google Scholar
Bolker, BM et al. (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends in Ecology & Evolution 24, 127135.Google Scholar
Bonett, RM et al. (2011) Distribution, abundance, and genetic diversity of Clinostomum spp. metacercariae (Trematoda: Digenea) in a modified Ozark stream system. Journal of Parasitology 97, 177184.Google Scholar
Bretz, F, Westfall, P and Hothorn, T (2016) Multiple Comparisons Using R. Boca Raton, FL: CRC Press.Google Scholar
Brown, SP et al. (2003) Field evidence for density-dependent effects in the trematode Microphallus papillorobustus in its manipulated host, Gammarus insensibilis. Journal of Parasitology 89, 668672.Google Scholar
Briosio-Aguilar, R et al. (2018) Morphological and molecular characterization of an enigmatic clinostomid trematode (Digenea: Clinostomidae) parasitic as metacercariae in the body of freshwater fishes (Cichlidae) across Middle America. Journal of Helminthology, https://doi.org/10.1017/S0022149X18000445.Google Scholar
Bruni, G and Angelini, C (2016) No short term effect of Clinostomum complanatum (Trematoda: Digenea: Clinostomatidae) on survival of Triturus carnifex (Amphibia: Urodela: Salamandridae). Acta Herpetologica 11, 7579.Google Scholar
Bullard, SA and Overstreet, RM (2008) Digeneans as enemies of fishes. Fish Diseases 2, 817976.Google Scholar
Caffara, M et al. (2011) Morphological and molecular differentiation of Clinostomum complanatum and Clinostomum marginatum (Digenea: Clinostomidae) metacercariae and adults. Journal of Parasitology 97, 884891.Google Scholar
Caffara, M et al. (2014) Metacercariae of Clinostomum complanatum (Trematoda: Digenea) in European newts Triturus carnifex and Lissotriton vulgaris (Caudata: Salamandridae). Journal of Helminthology 88, 278285.Google Scholar
Caffara, M et al. (2017) A morphological and molecular study of Clinostomid metacercariae from African fish with rediscripton of Clinostomum tilapiae. Parasitology 144, 15191529.Google Scholar
Calhoun, DM, McDevitt-Galles, T and Johnson, PTJ (2018) Parasites of invasive freshwater fishes and the factors affecting their richness. Freshwater Science 37, 134146.Google Scholar
Cort, WW (1913) Notes on the trematode genus Clinostomum. Transactions of the American Microscopical Society 32, 169182.Google Scholar
Crawford, JA and Kuhns, AR (2008) Identifying the distribution and habitat of Jefferson's salamander, Ambystoma jeffersonianum, in Illinois. Illinois Natural History Survey 24, 120.Google Scholar
Crawley, MJ (2002) Statistical Computing. London: John Wiley & Sons.Google Scholar
Crofton, HD (1971) A model of host–parasite relationships. Parasitology 63, 343364.Google Scholar
Duellman, WE and Trueb, L (1994) Biology of Amphibians. New York, NY: McGraw-Hill.Google Scholar
Duszynski, DW, Bolek, MG and Upton, SJ (2007) Coccidia (Apicomplexa: Eimeriidae) of the amphibians of the world. Zootaxa 1667, 177.Google Scholar
Dzikowski, R et al. (2004) Clinostomum complanatum and Clinostomum marginatum (Rudolphi, 1819) (Digenea: Clinostomidae) are separate species based on differences in ribosomal DNA. Journal of Parasitology 90, 413414.Google Scholar
Edney, JM (1940) The longevity of Clinostomum marginatum metacercariae in channel catfish. Journal of the Tennessee Academy of Science 15, 380388.Google Scholar
Elliott, AM and Russert, LR (1949) Some condition characteristics of a yellow perch population heavily parasitized by Clinostomum marginatum. Journal of Parasitology 35, 183190.Google Scholar
Esch, GW, Curtis, LA and Barger, MA (2001) A perspective on the ecology of trematode communities in snails. Parasitology 123, 5775.Google Scholar
Garone, P (2011) The Fall and Rise of the Wetlands of California's Great Central Valley. Berkley, CA: University of California Press.Google Scholar
Gibson, DI, Jones, A and Bray, RA (2002) Keys to the Trematoda. London: CAB International and Natural History Museum.Google Scholar
Gosner, KL (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16, 183190.Google Scholar
Gray, MJ et al. (2007) Influences of agricultural land use on Clinostomum attenuatum metacercariae prevalence in southern Great Plains amphibians. Herpetological Conservation and Biology 2, 2328.Google Scholar
Green, DE et al. (2002) Epizootiology of sixty-four amphibian morbidity and mortality events in the USA, 1996–2001. Annals of the New York Academy of Sciences 969, 323339.Google Scholar
Hara, H et al. (2014) Human laryngitis caused by Clinostomum complanatum. Nagoya Journal of Medical Science 76, 181185.Google Scholar
Hoffman, GL (1999) Parasites of North American Freshwater Fishes. New York, NY: Cornell University Press.Google Scholar
Hopkins, SH (1933) Note on the life history of Clinostomum marginatum (Trematoda). Transactions of the American Microscopical Society 52, 147149.Google Scholar
Hothorn, T et al. (2013) Multcomp: simultaneous inference in general parametric models. R package version 1.2-18. R Foundation for Statistical Computing, Vienna, Austria.Google Scholar
Hunter, WS and Hunter, GW (1935) Studies on Clinostomum. II. The miracidium of C. marginatum (Rud.). Journal of Parasitology 21, 186189.Google Scholar
Jinks, JL and Johnson, JC (1970) Trematodes of Rana catesbeiana from three strip-mine lakes in southeast Kansas. Transactions of the Kansas Academy of Science 73, 519520.Google Scholar
Johnson, PTJ, Kellermanns, E and Bowerman, J (2011) Critical window of disease risk: amphibian pathology driven by developmental changes in host resistance and tolerance. Functional Ecology 25, 726734.Google Scholar
Johnson, PTJ et al. (2012) Living fast and dying of infection: host life history drives interspecific variation in infection and disease risk. Ecology Letters 15, 235242.Google Scholar
Johnson, PTJ et al. (2013) Biodiversity decreases disease through predictable changes in host community competence. Nature 494, 230233.Google Scholar
Jones, A, Bray, RA and Gibson, DI (2005) Keys to the Trematoda. London: CAB International and Natural History Museum.Google Scholar
Kalantan, A and Arfin, M (1987) Seasonal incidence and pathogenicity of the metacercariae of Clinostomum complanatum in Aphanius dispar. Japan Journal of Parasitology 36, 1723.Google Scholar
Kanev, I, Radev, V and Fried, B (2002) Family Clinostomidae Lühe, 1901. In Gibson, GI, Jones, A and Bray, RA (eds), Keys to the Trematoda, Vol 1. New York, NY: CAB Publishing, pp. 113120.Google Scholar
Klaas, EE (1963) Ecology of the trematode Clinostomum marginatum and its hosts in eastern Kansas. Transactions of the Kansas Academy of Science 66, 519538.Google Scholar
Koprivnikar, J et al. (2017) Does spatial heterogeneity in host distribution drive parasite aggregation among hosts? Oikos 127, 99110.Google Scholar
Kudlai, O et al. (2015) A new species of Drepanocephalus Dietz, 1909 (Digenea: Echinostomatidae) from the double-crested cormorant Phalacrocorax auritus (Lesson) (Aves: Phalacrocoracidae) in North America. Systematic Parasitology 90, 221230Google Scholar
Kumar, S, Stecher, G and Tamura, K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 18701874.Google Scholar
Kuperman, BI et al. (2004) Parasites of the African clawed frog, Xenopus laevis, in Southern California, USA. Comparative Parasitology 71, 229232.Google Scholar
Kuznetsova, A, Brockhoff, PB and Christensen, RHB (2017) lmerTest package: tests in linear mixed effects models. Journal of Statistical Software 82, 127.Google Scholar
Lawless, JF (1987) Negative binomial and mixed Poisson regression. Canadian Journal of Statistics 15, 209225.Google Scholar
Lehmann, DL (1954) Some helminths of west coast urodeles. Journal of Parasitology 40, 231238.Google Scholar
Lemke, LB et al. (2008) Infestation of wild-caught American bullfrogs (Rana catesbeiana) by multiple species of metazoan parasites. Journal of the American Association for Laboratory Animal Science 47, 4246.Google Scholar
Lo, CF, Chen, SC and Wang, CH (1985) The study of Clinostomum complanatum (Rud., 1814) V. The influences of metacercaria of Clinostomum complanatum on fish. Fish Pathology 20, 305312.Google Scholar
Locke, SA et al. (2015) A large-scale molecular survey of Clinostomum (Digenea, Clinostomidae). Zoologica Scripta 44, 203217.Google Scholar
Lockyer, AE et al. (2003) The phylogeny of the Schistosomatidae based on three genes, with emphasis on the interrelationships of Schistosoma Weinland, 1858. Parasitology 126, 203224.Google Scholar
McAllister, CT (1990) Metacercaria of Clinostomum complanatum (Rudolphi, 1814) (Trematoda: Digenea) in a Texas salamander, Eurycea neotenes (Amphibia: Caudata), with comments on C. marginatum (Rudolphi, 1819). Journal of the Helminthological Society of Washington 57, 6971.Google Scholar
McAllister, CT et al. (2010) Metacercariae of Clinostomum (Trematoda: Digenea) from three species of Ambystoma (Caudata: Ambystomatidae) from Arkansas and Illinois, USA. Comparative Parasitology 77, 2530.Google Scholar
McDevitt-Galles, T and Johnson, PTJ (2018) Drought attenuates the impact of fish on aquatic macroinvertebrate richness and community composition. Freshwater Biology 63, 14571468.Google Scholar
Miller, DL et al. (2004) Metacercariae of Clinostomum attenuatum in Ambystoma tigrinum mavortium, Bufo cognatus and Spea multiplicata from west Texas. Journal of Helminthology 78, 373376.Google Scholar
Mitchell, CE, Tilman, D and Groth, JV (2002) Effects of grassland plant species diversity, abundance, and composition on foliar fungal disease. Ecology 83, 17131726.Google Scholar
Muzzall, PM (1991) Helminth infracommunities of the frogs Rana catesbeiana and Rana clamitans from Turkey Marsh, Michigan. Journal of Parasitology 77, 366371.Google Scholar
Orlofske, SA et al. (2017) Experimental investigation of alternative transmission functions: quantitative evidence for the importance of non-linear transmission dynamics in host–parasite systems. Journal of Animal Ecology 87, 703715.Google Scholar
Ortlepp, RJ (1963) Clinostomid trematodes as aberrant parasites in the mouth of the domestic cat (Felis catus domesticus). Onderstepoort Journal of Veterinary Research 30, 137143.Google Scholar
Osborn, HL (1911) On the distribution and mode of occurrence in the United States and Canada of Clinostomum marginatum, a trematode parasitic in fish, frogs and birds. The Biological Bulletin 20, 350366.Google Scholar
Osborn, HL (1912) On the structure of Clinostomum marginatum, a trematode parasite of the frog, bass and heron. Journal of Morphology 23, 189229.Google Scholar
Osnas, EE and Lively, CM (2004) Parasite dose, prevalence of infection and local adaptation in a host–parasite system. Parasitology 128, 223228.Google Scholar
Overstreet, RM and Curran, SS (2004) Defeating diplostomoid dangers in USA catfish aquaculture. Folia Parasitologica 51, 153165.Google Scholar
Paperna, I (1991) Diseases caused by parasites in the aquaculture of warm water fish. Annual Review of Fish Diseases 1, 155194.Google Scholar
Pérez Ponce de León, GPP et al. (2016) Species delimitation in trematodes using DNA sequences: Middle-American Clinostomum as a case study. Parasitology 143, 17731789.Google Scholar
Perpiñán, D et al. (2010) Scoliosis in a tiger salamander (Ambystoma tigrinum) associated with encysted digenetic trematodes of the genus Clinostomum. Journal of Wildlife Diseases 46, 579584.Google Scholar
Pinto, HA et al. (2015) Experimental and molecular study of cercariae of Clinostomum sp. (Trematoda: Clinostomidae) from Biomphalaria spp. (Mollusca: Planorbidae) in Brazil. Journal of Parasitology 101, 108113.Google Scholar
Poulin, R and Mouritsen, KN (2003) Large-scale determinants of trematode infections in intertidal gastropods. Marine Ecology Progress Series 254, 187198.Google Scholar
R Core Team (2014) R: A Language and Environment for Statiscial Computing. Vienna: R Foundation for Statistical Computing. http://www.R-project.org.Google Scholar
Roberts, RJ (2012) Fish Pathology. London: John Wiley & Sons.Google Scholar
Rosser, TG et al. (2016) Austrodiplostomum sp., Bolbophorus sp. (Digenea: Diplostomidae), and Clinostomum marginatum (Digenea: Clinostomidae) metacercariae in inland silverside Menidia beryllina from catfish aquaculture ponds, with notes on the infectivity of Austrodiplostomum sp. cercariae in channel catfish Ictalurus punctatus. Parasitology Research 115, 43654378.Google Scholar
Rosser, TG et al. (2017) Clinostomum album n. sp. and Clinostomum marginatum (Rudolphi, 1819), parasites of the great egret Ardea alba L. from Mississippi, USA. Systematic Parasitology 94, 3549.Google Scholar
Rosser, TG et al. (2018) Clinostomum poteae n. sp. (Digenea: Clinostomidae), in the trachea of a double-crested cormorant Phalacrocorax auritus Lesson, 1831 and molecular data linking the life-cycle stages of Clinostomum album Rosser, Alberson, Woodyard, Cunningham, Pote & Griffin, 2017 in Mississippi, USA. Systematic Parasitology 95, 543566.Google Scholar
Sandland, GJ and Goater, CP (2000) Development and intensity dependence of Ornithodiplostomum ptychocheilus metacercariae in fathead minnows (Pimephales promelas). Journal of Parasitology 86, 10561060.Google Scholar
Schell, SC (1985) Handbook of Trematodes of North America North of Mexico. Moscow, ID: University Press of Idaho.Google Scholar
Sereno-Uribe, AL et al. (2013) Using mitochondrial and ribosomal DNA sequences to test the taxonomic validity of Clinostomum complanatum Rudolphi, 1814 in fish-eating birds and freshwater fishes in Mexico, with the description of a new species. Parasitology Research 112, 28552870.Google Scholar
Sereno-Uribe, AL et al. (2018) Three new species of Clinostomum Leidy, 1856 (Trematoda) from Middle American fish-eating birds. Parasitology Research 117, 115.Google Scholar
Sleigh, MA (1991) Protozoa and Other Protists. Cambridge: Cambridge University Press.Google Scholar
Smyth, JD and Smyth, MM (1980) Frogs as Host–Parasite Systems 1. London: Macmillan Press Ltd.Google Scholar
Szalai, AJ and Dick, TA (1988) Helminths of stocked rainbow trout (Salmo gairdneri) with special reference to Clinostomum complanatum. Journal of Wildlife Diseases 24, 456460.Google Scholar
Tkach, VV and Pawlowski, JW (1999) A new method of DNA extraction from the ethanol-fixed parasitic worms. Acta Parasitologica 44, 147148.Google Scholar
Tkach, VV and Snyder, SD (2007) Aptorchis megacetabulus n. sp. (Platyhelminthes: Digenea) from the northern long-necked turtle, Chelodina rugosa (Pleurodira: Chelidae), in Australia. Journal of Parasitology 93, 404408.Google Scholar
Wang, ML, Chen, HY and Shih, HH (2017) Occurrence and distribution of yellow grub trematode (Clinostomum complanatum) infection in Taiwan. Parasitology Research 116, 17611771.Google Scholar
Witenberg, G (1944) What is the cause of the parasitic laryngo-pharyngitis in the Near East (” Halzoun”)? Acta Medica Orientalia 3, 191192.Google Scholar
Yamaguti, S (1933) Studies on the helminth fauna of Japan. Part I. Trematodes of birds, reptiles and mammals. Japanese Journal of Zoology 5, 1134.Google Scholar
Yamashita, J (1938) Clinostomum complanatum, a trematode parasite new to man. Annotationes Zoologicae Japonenses 17, 563566.Google Scholar
Supplementary material: File

Calhoun et al. supplementary material

Calhoun et al. supplementary material 1

Download Calhoun et al. supplementary material(File)
File 178.1 KB