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Negative effects of parasitic lung nematodes on the fitness of a Neotropical toad (Rhinella horribilis)

Published online by Cambridge University Press:  12 March 2019

Crystal Kelehear Open the ORCID record for Crystal Kelehear [Opens in a new window] ,
Kristin Saltonstall  and
Mark E. Torchin
Crystal Kelehear*
Affiliation:
Smithsonian Tropical Research Institute, Apartado 0843-03092, Ancon, Panama, Republic of Panama
Kristin Saltonstall
Affiliation:
Smithsonian Tropical Research Institute, Apartado 0843-03092, Ancon, Panama, Republic of Panama
Mark E. Torchin
Affiliation:
Smithsonian Tropical Research Institute, Apartado 0843-03092, Ancon, Panama, Republic of Panama
*
Author for correspondence: Crystal Kelehear, E-mail: crystal.kelehear@hotmail.com
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Abstract

Pathogens are increasingly implicated in amphibian declines but less is known about parasites and the role they play. We focused on a genus of nematodes (Rhabdias) that is widespread in amphibians and examined their genetic diversity, abundance (prevalence and intensity), and impact in a common toad (Rhinella horribilis) in Panama. Our molecular data show that toads were infected by at least four lineages of Rhabdias, most likely Rhabdias pseudosphaerocephala, and multiple lineages were present in the same geographic locality, the same host and even the same lung. Mean prevalence of infection per site was 63% and mean intensity of infection was 31 worms. There was a significant effect of host size on infection status in the wild: larger toads were more likely to be infected than were smaller conspecifics. Our experimental infections showed that toadlets that were penetrated by many infective Rhabdias larvae grew less than those who were penetrated by few larvae. Exposure to Rhabdias reduced toadlet locomotor performance (both sustained speed and endurance) but did not influence toadlet survival. The effects of Rhabdias infection on their host appear to be primarily sublethal, however, dose-dependent reduction in growth and an overall impaired locomotor performance still represents a significant reduction in host fitness.

Keywords

AmphibiananuranBufoCentral AmericagrowthlocomotionPanamaRhabdias
Type
Research Article
Information
Parasitology , Volume 146 , Issue 7 , June 2019 , pp. 928 - 936
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Copyright
Copyright © Cambridge University Press 2019 

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Footnotes

*

Present address: Department of Biology, Geology & Physical Sciences, Sul Ross State University, Alpine, TX 79832, USA.

References

Acevedo, AA, Lampo, M and Cipriani, R (2016) The cane or marine toad, Rhinella marina (Anura, Bufonidae): two genetically and morphology distinct species. Zootaxa 4103, 574–586.Google Scholar
Anderson, RC (2000) Nematode Parasites of Vertebrates: Their Development and Transmission, 2nd Edn. Wallingford, Oxfordshire: CABI Publishing.Google Scholar
Barton, DP (1998) Dynamics of natural infections of Rhabdias cf. hylae (nematoda) in Bufo marinus (Amphibia) in Australia. Parasitology 117, 505–513.Google Scholar
Berger, L, Speare, R, Daszak, P, Green, DE, Cunningham, AA, Goggin, CL, Slocombe, R, Ragan, MA, Hyatt, AD, McDonald, KR, Hines, HB, Lips, KR, Marantelli, G and Parkes, H (1998) Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America. Proceedings of the National Academy of Sciences of the United States of America 95, 9031–9036.Google Scholar
Biro, PA, Beckmann, C and Stamps, JA (2010) Small within-day increases in temperature affects boldness and alters personality in coral reef fish. Proceedings of the Royal Society B-Biological Sciences 277, 71–77.Google Scholar
Blaustein, AR and Kiesecker, JM (2002) Complexity in conservation: lessons from the global decline of amphibian populations. Ecology Letters 5, 597–608.Google Scholar
Brooks, TM, Mittermeier, RA, Mittermeier, CG, de Fonseca, GAB, Rylands, AB, Konstant, WR, Flick, P, Pilgrim, J, Oldfield, S, Magin, G and Hilton-Taylor, C (2002) Habitat loss and extinction in the hotspots of biodiversity. Conservation Biology 16, 909–923.Google Scholar
Bursey, CR and Brooks, DR (2010) Nematode parasites of 41 anuran species from the Area de Conservación Guanacaste, Costa Rica. Comparative Parasitology 77, 221–231.Google Scholar
Bush, AO, Lafferty, KD, Lotz, JM, Shostak, AW (1997) Parasitology meets ecology on its own terms: Margolis et al. Revisited. Journal of Parasitology 83, 575–583.Google Scholar
Child, T, Phillips, BL, Brown, GP and Shine, R (2008a) The spatial ecology of cane toads (Bufo marinus) in tropical Australia: why do metamorph toads stay near the water? Austral Ecology 33, 630–640.Google Scholar
Child, T, Phillips, BL and Shine, R (2008b) Abiotic and biotic influences on the dispersal behavior of metamorph cane toads (Bufo marinus) in tropical Australia. Journal of Experimental Zoology Part A – Ecological Genetics and Physiology 309A, 215–224.Google Scholar
Child, T, Phillips, BL and Shine, R (2009) Does desiccation risk drive the distribution of juvenile cane toads (Bufo marinus) in tropical Australia? Journal of Tropical Ecology 25, 193–200.Google Scholar
Crawford, AJ, Lips, KR and Bermingham, E (2010) Epidemic disease decimates amphibian abundance, species diversity and evolutionary history in the highlands of Central Panama. Proceedings of the National Academy of Sciences of the United States of America 107, 13777–13782.Google Scholar
Daszak, P, Berger, L, Cunningham, AA, Hyatt, AD, Green, DE and Speare, R (1999) Emerging infectious diseases and amphibian population declines. Emerging Infectious Diseases 5, 735–748.Google Scholar
Dubey, S and Shine, R (2008) Origin of the parasites of an invading species, the Australian cane toad (Bufo marinus): are the lungworms Australian or American? Molecular Ecology 17, 4418–4424.Google Scholar
Easteal, S (1981) The history of introductions of Bufo marinus (Amphibia: Anura); a natural experiment in evolution. Biological Journal of the Linnean Society 16, 93–113.Google Scholar
Espinola-Novelo, JF and Guillen-Hernandez, S (2008) Helminth parasites in Chaunus marinus and Cranopis valliceps (Anura : Bufonidae) from Lagunas Yalahau, Yucatan, Mexico. Journal of Parasitology 94, 672–674.Google Scholar
Espinoza-Jiménez, A, García-Prieto, L, Osorio-Sarabia, D and León-Règagnon, V (2007) Checklist of helminth parasites of the cane toad Bufo marinus (Anura: Bufonidae) from Mexico. Journal of Parasitology 93, 937–944.Google Scholar
Finnerty, PB, Shine, R and Brown, GP (2018) The cost of parasite infection: effects of removing lungworms on performance, growth and survival of free-ranging cane toads. Functional Ecology 32, 402–415.Google Scholar
Goater, CP (1992) Experimental population dynamics of Rhabdias bufonis (Nematoda) in toads (Bufo bufo): density-dependence in the primary infection. Parasitology 104, 179–187.Google Scholar
Goater, CP (1994) Growth and survival of postmetamorphic toads: interactions among larval history, density and parasitism. Ecology 75, 2264–2274.Google Scholar
Goater, CP and Ward, PI (1992) Negative effects of Rhabdias bufonis (Nematoda) on the growth and survival of toads (Bufo bufo). Oecologia 89, 161–165.Google Scholar
Goater, CP, Semlitsch, RD and Bernasconi, MV (1993) Effects of body size and parasite infection on the locomotory performance of juvenile toads, Bufo bufo. Oikos 66, 129–136.Google Scholar
Gosner, KL (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16, 183–190.Google Scholar
Halsey, LG, Matthews, PGD, Rezende, EL, Chauvaud, L and Robson, AA (2015) The interactions between temperature and activity levels in driving metabolic rate: theory, with empirical validation from contrasting ectotherms. Oecologia 177, 1117–1129.Google Scholar
Holterman, M, van der Wurff, A, van den Elsen, S, van Megen, H, Bongers, T, Holovachov, O, Bakker, J and Helder, J (2006) Phylum-wide analysis of SSU rDNA reveals deep phylogenetic relationships among nematodes and acceleratd evolution toward crown clades. Molecular Biology and Evolution 23, 1792–1800.Google Scholar
Hudson, PJ, Dobson, AP and Newborn, D (1998) Prevention of population cycles by parasite removal. Science 282, 2256–2258.Google Scholar
Hudson, PJ, Dobson, AP and Lafferty, KD (2006) Is a healthy ecosystem one that is rich in parasites? Trends in Ecology & Evolution 21, 381–385.Google Scholar
Kelehear, C, Webb, JK and Shine, R (2009) Rhabdias pseudosphaerocephala infection in Bufo marinus: lung nematodes reduce viability of metamorph cane toads. Parasitology 136, 919–927.Google Scholar
Kelehear, C, Brown, GP and Shine, R (2011) Influence of lung parasites on the growth rates of free-ranging and captive adult cane toads. Oecologia 165, 585–592.Google Scholar
Koprivnikar, J, Marcogliese, DJ, Rohr, JR, Orlofske, SA, Raffel, TR and Johnson, PTJ (2012) Macroparasite infections of amphibians: what can they tell us? EcoHealth 9, 342–360.Google Scholar
Kuris, AM, Hechinger, RF, Shaw, JC, Whitney, KL, Aguirre-Macedo, L, Boch, CA, Dobson, AP, Dunham, EJ, Fredensborg, BL, Huspeni, TC, Lorda, J, Mababa, L, Mancini, FT, Mora, AB, Pickering, M, Talhouk, NL, Torchin, ME and Lafferty, KD (2008) Ecosystem energetic implications of parasite and free-living biomass in three estuaries. Nature 454, 515–518.Google Scholar
Kuzmin, Y (2013) Review of Rhabdiasidae (Nematoda) from the Holarctic. Zootaxa 3639, 1–76.Google Scholar
Kuzmin, Y, Tkach, VV and Snyder, SD (2003) The nematode genus Rhabdias (Nematoda: Rhabdiasidae) from amphibians and reptiles of the Nearctic. Comparative Parasitology 70, 101–114.Google Scholar
Kuzmin, Y, Tkach, VV and Brooks, DR (2007) Two new species of Rhabdias (Nematoda: Rhabdiasidae) from the marine toad, Bufo marinus (L.) (Lissamphibia: Anura: Bufonidae), in Central America. Journal of Parasitology 93, 159–165.Google Scholar
Kuzmin, Y, du Preez, LH and Junker, K (2015) Some nematodes of the genus Rhabdias stiles et Hassall, 1905 (Nematoda: Rhabdiasidae) parasitising amphibians in French Guiana. Folia Parasitologica 62, 031.Google Scholar
Lafferty, KD, Allesina, S, Arim, M, Briggs, CJ, De Leo, G, Dobson, AP, Dunne, JA, Johnson, PTJ, Kuris, AM, Marcogliese, DJ, Martinez, ND, Memmott, J, Marquet, PA, McLaughlin, JP, Mordecai, EA, Pascual, M, Poulin, R and Thieltges, DW (2008) Parasites in food webs: the ultimate missing links. Ecology Letters 11, 533–546.Google Scholar
Lever, C (2001) The Cane Toad: The History and Ecology of a Successful Colonist. Otley, West Yorkshire: Westbury Academic and Scientific Publishing.Google Scholar
Lips, KR (1999) Mass mortality and population declines of Anurans at an Upland site in Western Panama. Conservation Biology 13, 117–125.Google Scholar
Lips, KR, Brem, F, Brenes, R, Reeve, JD, Alford, RA, Voyles, J, Carey, C, Livo, L, Pessier, AP and Collins, JP (2006) Emerging infectious disease and the loss of biodiversity in a Neotropical amphibian community. Proceedings of the National Academy of Sciences of the United States of America 103, 3165–3170.Google Scholar
Losos, JB (1990) Thermal sensitivity of sprinting and clinging performance in the Tokay gecko (Gekko gecko). Asiatic Herpetological Research 3, 54–59.Google Scholar
Marr, S, Johnson, SA, Hara, AH and McGarrity, ME (2010) Preliminary evaluation of the potential of the helminth parasite Rhabdias elegans as a biological control agent for invasive Puerto Rican coquis (Eleutherodactylus coqui) in Hawaii. Biological Control 54, 69–74.Google Scholar
Martel, A, Spitzen-van der Sluijs, A, Blooi, M, Bert, W, Ducatelle, R, Fisher, MC, Woeltjes, A, Bosman, W, Chiers, K, Bossuyt, F and Pasmans, F (2013) Batrachochytrium salamandrivorans sp. nov. causes lethal chytridiomycosis in amphibians. Proceedings of the National Academy of Sciences of the United States of America 110, 15325–15329.Google Scholar
Mitchell, MA, Riggs, SM, Singleton, CB, Diaz-Figueroa, O and Hale, LK (2009) Evaluating the clinical and cardiopulmonary effects of clove oil and propofol in tiger salamanders (Ambystoma tigrinum). Journal of Exotic Pet Medicine 18, 50–56.Google Scholar
Moretti, EH, Titon, B Jr, Madelaire, CB, Arruda, R, Alvarez, T and Gomes, FR (2017) Behavioral, physiological and morphological correlates of parasite intensity in the wild Cururu toad (Rhinella icterica). International Journal for Parasitology: Parasites and Wildlife 6, 146–154.Google Scholar
Müller, MI, Morais, DH, Costa-Silva, GJ, Aguiar, A, Ávila, RW and da Silva, RJ (2018) Diversity in the genus Rhabdias (Nematoda, Rhabdiasidae): evidence for cryptic speciation. Zoologica Scripta 47, 595–607.Google Scholar
Nelson, FBL, Brown, GP, Dubey, S and Shine, R (2015) The effects of a nematode lungworm (Rhabdias hylae) on its natural and invasive anuran hosts. Journal of Parasitology 101, 290–296.Google Scholar
Niewiarowski, PH, Lopez, S, Ge, L, Hagan, E and Dhinojwala, A (2008) Sticky gecko feet: the role of temperature and humidity. PLoS ONE 3, e2192.Google Scholar
Pizzatto, L and Shine, R (2011a) Ecological impacts of invading species: do parasites of the cane toad imperil Australian frogs? Austral Ecology 36, 954–963.Google Scholar
Pizzatto, L and Shine, R (2011b) The effects of experimentally infecting Australian tree frogs with lungworms (Rhabdias pseudosphaerocephala) from invasive cane toads. International Journal for Parasitology 41, 943–949.Google Scholar
Pizzatto, L and Shine, R (2012) Lungworm infection modifies cardiac response to exercise in cane toads. Journal of Zoology 287, 150–155.Google Scholar
Pizzatto, L, Child, T and Shine, R (2008) Why be diurnal? Shifts in activity time enable young cane toads to evade cannibalistic conspecifics. Behavioral Ecology 19, 990–997.Google Scholar
Pizzatto, L, Kelehear, C and Shine, R (2013) Seasonal dynamics of the lungworm, Rhabdias pseudosphaerocephala, in recently colonised cane toad (Rhinella marina) populations in tropical Australia. International Journal for Parasitology 43, 753–761.Google Scholar
Pramuk, JB (2006) Phylogeny of South American Bufo (Anura: Bufonidae) inferred from combined evidence. Zoological Journal of the Linnean Society 146, 407–452.Google Scholar
Raffel, TR, LeGros, RP, Love, BC, Rohr, JR and Hudson, PJ (2009) Parasite age-intensity relationships in red spotted newts: does immune memory influence salamander disease dynamics? International Journal for Parasitology 39, 231–241.Google Scholar
Ruiz-Torres, N, García-Prieto, L, Lagunas-Calvo, O, Violante-González, J and Osorio-Sarabia, D (2017) Helminth infracommunity of the cane toad Rhinella marina (Anura: Bufonidae) within its native distribution range. Parasitology International 66, 567–572.Google Scholar
Seebacher, F, Tallis, JA and James, RS (2014) The cost of muscle power production: muscle oxygen consumption per unit work increases at low temperatures in Xenopus laevis. Journal of Experimental Biology 217, 1940–1945.Google Scholar
Selechnik, D, Rollins, LA, Brown, GP, Kelehear, C and Shine, R (2017) The things they carried: the pathogenic effects of old and new parasites following the intercontinental invasion of the Australian cane toad (Rhinella marina). International Journal for Parasitology: Parasites and Wildlife 6, 375–385.Google Scholar
Shine, R (2010) The ecological impact of invasive cane toads (Bufo marinus) in Australia. Quarterly Review of Biology 85, 253–291.Google Scholar
Skerratt, LF, Berger, L, Speare, R, Cashins, S, McDonald, KR and Phillott, AD (2007) Spread of chytridiomycosis has caused the rapid global decline and extinction of frogs. EcoHealth 4, 125–134.Google Scholar
Slade, RW and Moritz, C (1998) Phylogeography of Bufo marinus from its natural and introduced ranges. Proceedings of the Royal Society B-Biological Sciences 265, 769–777.Google Scholar
Sorci, G (1996) Patterns of haemogregarine load, aggregation and prevalence as a function of host age in the lizard Lacerta vivipara. Journal of Parasitology 82, 676–678.Google Scholar
Speare, R (1990) A review of the diseases of the cane toad, Bufo marinus, with comments on biological control. Australian Wildlife Research 17, 387–410.Google Scholar
Tkach, VV, Halajian, A and Kuzmin, Y (2014) Phylogenetic and systematic position of Entomelas sylvestris Baker, 1982 (Nematoda: Rhabdiasidae), a parasite of Breviceps sylvestris FitzSimons (Amphibia: Brevicipitidae) in South Africa. Systematic Parasitology 87, 293–298.Google Scholar
Tompkins, DM, Dunn, AM, Smith, MJ and Telfer, S (2011) Wildlife diseases: from individuals to ecosystems. Journal of Animal Ecology 80, 19–38.Google Scholar
Ujvari, B and Madsen, M (2006) Age, parasites, and condition affect humoral immune response in tropical pythons. Behavioral Ecology 17, 20–24.Google Scholar
Vallinoto, M, Sequeira, F, Sodré, D, Bernardi, JAR, Sampaio, I and Schneider, H (2010) Phylogeny and biogeography of the Rhinella marina species complex (Amphibia, Bufonidae) revisited: implications for Neotropical diversification hypotheses. Zoologica Scripta 39, 128–140.Google Scholar
Wilson, K, Bjørnstad, ON, Dobson, AP, Merler, S, Poglayen, G, Randolph, SE, Read, AF and Skorping, A (2002) Heterogeneities in macroparasite infections: patterns and processes. In Hudson, PJ, Rizzoli, A, Grenfell, BT, Heesterbeek, H and Dobson, AP (eds), The Ecology of Wildlife Diseases. Oxford, UK: Oxford University Press, pp. 6–44.Google Scholar
Zug, GR and Zug, PB (1979) The marine toad, Bufo marinus: a natural history resume of native populations. Smithsonian Contributions to Zoology 284, 1–58.Google Scholar
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