Hostname: page-component-586b7cd67f-t7fkt Total loading time: 0 Render date: 2024-11-20T07:04:22.427Z Has data issue: false hasContentIssue false
  • English
  • Français

Timing and order of exposure to two echinostome species affect patterns of infection in larval amphibians

Published online by Cambridge University Press:  14 July 2020

Logan S. Billet Open the ORCID record for Logan S. Billet [Opens in a new window] ,
Vanessa P. Wuerthner ,
Jessica Hua ,
Rick A. Relyea  and
Jason T. Hoverman
Logan S. Billet*
Affiliation:
Department of Forestry and Natural Resources, Purdue University, West Lafayette, IN47907, USA
Vanessa P. Wuerthner
Affiliation:
Biological Sciences Department, Binghamton University, Binghamton, NY13902, USA
Jessica Hua
Affiliation:
Biological Sciences Department, Binghamton University, Binghamton, NY13902, USA
Rick A. Relyea
Affiliation:
Department of Biological Sciences, Rensselaer Polytechnic Institute, Troy, NY, USA
Jason T. Hoverman
Affiliation:
Department of Forestry and Natural Resources, Purdue University, West Lafayette, IN47907, USA
*
Author for correspondence: Logan S. Billet, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The study of priority effects with respect to coinfections is still in its infancy. Moreover, existing coinfection studies typically focus on infection outcomes associated with exposure to distinct sets of parasite species, despite that functionally and morphologically similar parasite species commonly coexist in nature. Therefore, it is important to understand how interactions between similar parasites influence infection outcomes. Surveys at seven ponds in northwest Pennsylvania found that multiple species of echinostomes commonly co-occur. Using a larval anuran host (Rana pipiens) and the two most commonly identified echinostome species from our field surveys (Echinostoma trivolvis and Echinoparyphium lineage 3), we examined how species composition and timing of exposure affect patterns of infection. When tadpoles were exposed to both parasites simultaneously, infection loads were higher than when exposed to Echinoparyphium alone but similar to being exposed to Echinostoma alone. When tadpoles were sequentially exposed to the parasite species, tadpoles first exposed to Echinoparyphium had 23% lower infection loads than tadpoles first exposed to Echinostoma. These findings demonstrate that exposure timing and order, even with similar parasites, can influence coinfection outcomes, and emphasize the importance of using molecular methods to identify parasites for ecological studies.

Keywords

AmphibianBayesianEchinostomatidaemetacercariaepriority effects
Type
Research Article
Information
Parasitology , Volume 147 , Issue 13 , November 2020 , pp. 1515 - 1523
Check for updates
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

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.)

Footnotes

Present address: 715 W. State Street Room G004, West Lafayette, IN 47907, USA.

References

Allan, F, Rollinson, D, Smith, JE and Dunn, AM (2009) Host choice and penetration by Schistosoma haematobium miracidia. Journal of Helminthology 83, 33–38.CrossRefGoogle ScholarPubMed
Bowles, J and McManus, DP (1993) Rapid discrimination of Echinococcus species and strains using a polymerase chain reaction-based RFLP method. Molecular and Biochemical Parasitology 57, 231–239.CrossRefGoogle ScholarPubMed
Buss, N and Hua, J (2018) Parasite susceptibility in an amphibian host is modified by salinization and predators. Environmental Pollution 236, 754–763.CrossRefGoogle Scholar
Cox, FEG (2001) Concomitant infections, parasites and immune responses. Parasitology 122, S23–S38.CrossRefGoogle ScholarPubMed
Detwiler, JT, Bos, DH and Minchella, DJ (2010) Revealing the secret lives of cryptic species: examining the phylogenetic relationships of echinostome parasites in North America. Molecular Phylogenetics and Evolution 55, 611–620.CrossRefGoogle ScholarPubMed
Detwiler, JT, Zajac, AM, Minchella, DJ and Belden, LK (2012) Revealing cryptic parasite diversity in a definitive host: Echinostomes in Muskrats. Journal of Parasitology 98, 1148–1155.CrossRefGoogle Scholar
Devevey, G, Dang, T, Graves, CJ, Murray, S and Brisson, D (2015) First arrived takes all: inhibitory priority effects dominate competition between co-infecting Borrelia burgdorferi strains ecological and evolutionary microbiology. BMC Microbiology 15, 1–9.CrossRefGoogle Scholar
Dönges, J (1972) Double infection experiments with echinostomatids (Trematoda) in Lymnaea stagnalis by implantation of rediae and exposure to miracidia. International Journal for Parasitology 2, 409–423.CrossRefGoogle ScholarPubMed
Ebert, D, Zschokke-Rohringer, CD and Carius, HJ (2000) Dose effects and density-dependent regulation of two microparasites of Daphnia magna. Oecologia 122, 200–209.CrossRefGoogle ScholarPubMed
Ezenwa, VO (2016) Helminth–microparasite co-infection in wildlife: lessons from ruminants, rodents and rabbits. Parasite Immunology 38, 527–534.CrossRefGoogle ScholarPubMed
Ezenwa, VO, Etienne, RS, Luikart, G, Beja-Pereira, A and Jolles, AE (2010) Hidden consequences of living in a wormy world: nematode-induced immune suppression facilitates tuberculosis invasion in African buffalo. American Naturalist 176, 613–624.CrossRefGoogle Scholar
Fingerut, JT, Zimmer, CA and Zimmer, RK (2003) Patterns and processes of larval emergence in an estuarine parasite system. Biological Bulletin 205, 110–120.CrossRefGoogle Scholar
Fox, J and Weisberg, S (2011) An R Companion to Applied Regression, 2nd Edn. Thousand Oaks, CA: Sage.Google Scholar
Fried, B, Pane, PL and Reddy, A (1997) Experimental infection of Rana pipiens tadpoles with Echinostoma trivolvis cercariae. Parasitology Research 83, 666–669.CrossRefGoogle ScholarPubMed
Fried, B, Frazer, BA and Kanev, I (1998) Comparative observations on cercariae and metacercariae of Echinostoma trivolvis and Echinoparyphium sp. The Journal of parasitology 84, 623–626.CrossRefGoogle ScholarPubMed
Fujino, T, Zhiliang, W, Nagano, I, Takahashi, Y and Fried, B (1997) Specific primers for the detection of genomic DNA of Echinostoma trivolvis and E. caproni (Trematoda: Echinostomatidae). Molecular and Cellular Probes 11, 77–80.CrossRefGoogle Scholar
Gosner, K (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16, 183–190.Google Scholar
Haas, W, Haberl, B, Korner, M, Spengler, Y, Hertel, J and Kalbe, M (2000) Host-finding in Echinostoma caproni: miracidia and cercariae use different signals to identify the same snail species. Parasitology 120, 479–486.Google Scholar
Hechinger, RF and Lafferty, KD (2005) Host diversity begets parasite diversity: bird final hosts and trematodes in snail intermediate hosts. Proceedings of the Royal Society B: Biological Sciences 272, 1059–1066.CrossRefGoogle ScholarPubMed
Holland, MP, Skelly, DK, Kashgarian, M, Bolden, SR, Harrison, LM and Cappello, M (2007) Echinostome infection in green frogs (Rana clamitans) is stage and age dependent. Journal of Zoology 271, 455–462.CrossRefGoogle Scholar
Hothorn, T, Bretz, F and Westfall, P (2008) Simultaneous inference in general parametric models. Biometrical Journal 50, 346–363.CrossRefGoogle ScholarPubMed
Hoverman, JT, Mihaljevic, JR, Richgels, KLDD, Kerby, JL and Johnson, PTJJ (2012) Widespread co-occurrence of virulent pathogens within California amphibian communities. EcoHealth 9, 288–292.CrossRefGoogle ScholarPubMed
Hoverman, JT, Hoye, BJ and Johnson, PTJ (2013) Does timing matter? How priority effects influence the outcome of parasite interactions within hosts. Oecologia 173, 1471–1480.CrossRefGoogle ScholarPubMed
Hua, J, Buss, N, Kim, J, Orlofske, SA and Hoverman, JT (2016) Population-specific toxicity of six insecticides to the trematode Echinoparyphium sp. Parasitology 143, 542–550.CrossRefGoogle ScholarPubMed
Johnson, PTJ and Hoverman, JT (2012) Parasite diversity and coinfection determine pathogen infection success and host fitness. Proceedings of the National Academy of Sciences 109, 9006–9011.CrossRefGoogle ScholarPubMed
Johnson, PTJ and McKenzie, VJ (2008) Effects of environmental change on helminth infections in amphibians: exploring the emergence of Ribeiroia and Echinostoma infections in North America. In Toledo, R and Fried, B (eds), The Biology of Echinostomes: From the Molecule to the Community. New York: Springer, pp. 249–280. doi: 10.1007/978-0-387-09577-6_11.Google Scholar
Johnson, PTJ, Koprivnikar, J, Orlofske, SA, Melbourne, BA and Lafonte, BE (2014) Making the right choice: testing the drivers of asymmetric infections within hosts and their consequences for pathology. Oikos 123, 875–885.CrossRefGoogle Scholar
Johnson, PTJ, De Roode, JC and Fenton, A (2015) Why infectious disease research needs community ecology. Science (New York, N.Y.) 349, 1069–1079.CrossRefGoogle ScholarPubMed
Karvonen, A, Paukku, S, Valtonen, ET and Hudson, PJ (2003) Transmission, infectivity and survival of Diplostomum spathaceum cercariae. Parasitology 127, 217–224.CrossRefGoogle ScholarPubMed
Kleiber, C and Zeileis, A (2008). Applied Econometrics with R. New York: Springer-Verlag. doi: 10.1007/978-0-387-77318-6.CrossRefGoogle Scholar
Knowles, SCL (2011) The effect of helminth co-infection on malaria in mice: a meta-analysis. International Journal for Parasitology 41, 1041–1051.CrossRefGoogle ScholarPubMed
Koprivnikar, J, Forbes, MR and Baker, RL (2007) Contaminant effects on host-parasite interactions: atrazine, frogs, and trematodes. Environmental Toxicology and Chemistry 26, 2166–2170.CrossRefGoogle ScholarPubMed
Koprivnikar, J, Hoye, BJ, Urichuk, TMY and Johnson, PTJ (2019) Endocrine and immune responses of larval amphibians to trematode exposure. Parasitology Research 118, 275–288.CrossRefGoogle ScholarPubMed
Kostadinova, A, Herniou, EA, Barrett, J and Littlewood, DTJ (2003) Phylogenetic relationships of Echinostoma rudolphi, 1809 (Digenea: Echinostomatidae) and related genera re-assessed via DNA and morphological analyses. Systematic Parasitology 54, 159–176.CrossRefGoogle ScholarPubMed
Kumar, S, Stecher, G, Li, M, Knyaz, C and Tamura, K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution 35, 1547–1549.CrossRefGoogle ScholarPubMed
Lafferty, KD, Sammond, DT and Kuris, AM (1994) Analysis of larval trematode communities. Ecology 75, 2275–2285.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
LaFonte, BE and Johnson, PTJ (2013) Experimental infection dynamics: using immunosuppression and in vivo parasite tracking to understand host resistance in an amphibian-trematode system. Journal of Experimental Biology 216, 3700–3708.CrossRefGoogle Scholar
LaFonte, BE, Raffel, TR, Monk, IN and Johnson, PTJ (2015) Quantifying larval trematode infections in hosts: a comparison of method validity and implications for infection success. Experimental Parasitology 154, 155–162.CrossRefGoogle ScholarPubMed
Lenth, R, Singmann, H, Love, J, Buerkner, P and Herve, M (2019). emmeans: Estimated marginal means, aka least-squares means. R Package Version 1, 15–15.Google Scholar
Leung, TLF and Poulin, R (2011) Intra-host competition between co-infecting digeneans within a bivalve second intermediate host: Dominance by priority-effect or taking advantage of others? International Journal for Parasitology 41, 449–454.CrossRefGoogle ScholarPubMed
Maizels, RM, Pearce, EJ, Artis, D, Yazdanbakhsh, M and Wynn, TA (2009) Regulation of pathogenesis and immunity in helminth infections. Journal of Experimental Medicine 206, 2059–2066.CrossRefGoogle ScholarPubMed
Marino, JA, Holland, MP and Werner, EE (2017) The distribution of echinostome parasites in ponds and implications for larval anuran survival. Parasitology 144, 801–811.CrossRefGoogle ScholarPubMed
Miura, O, Kuris, AM, Torchin, ME, Hechinger, RF, Dunham, EJ and Chiba, S (2005) Molecular-genetic analyses reveal cryptic species of trematodes in the intertidal gastropod, Batillaria cumingi (Crosse). International Journal for Parasitology 35, 793–801.CrossRefGoogle Scholar
Pedersen, AB and Fenton, A (2007) Emphasizing the ecology in parasite community ecology. Trends in Ecology and Evolution 22, 133–139.CrossRefGoogle ScholarPubMed
Poulin, R (2010) The scaling of dose with host body mass and the determinants of success in experimental cercarial infections. International Journal for Parasitology 40, 371–377.CrossRefGoogle ScholarPubMed
Preston, DL, Orlofske, SA, Lambden, JP and Johnson, PTJ (2013) Biomass and productivity of trematode parasites in pond ecosystems. Journal of Animal Ecology 82, 509–517.CrossRefGoogle ScholarPubMed
R Core Team (2018). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available online at https://www.R-project.org/.Google Scholar
Richgels, KLD, Hoverman, JT and Johnson, PTJ (2013) Evaluating the role of regional and local processes in structuring a larval trematode metacommunity of Helisoma trivolvis. Ecography 36, 854–863.Google Scholar
Rohr, JR, Raffel, TR, Sessions, SK and Hudson, PJ (2008) Understanding the net effects of pesticides on amphibian trematode infections. Ecological Applications 18, 1743–1753.CrossRefGoogle ScholarPubMed
Ronquist, F, Teslenko, M, Van Der Mark, P, Ayres, DL, Darling, A, Höhna, S, Larget, B, Liu, L, Suchard, MA and Huelsenbeck, JP (2012) Mrbayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539–542.CrossRefGoogle ScholarPubMed
Rozas, J, Ferrer-Mata, A, Sanchez-DelBarrio, JC, Guirao-Rico, S, Librado, P, Ramos-Onsins, SE and Sanchez-Gracia, A (2017) DnaSP 6: DNA sequence polymorphism analysis of large data sets. Molecular Biology and Evolution 34, 3299–3302.CrossRefGoogle ScholarPubMed
Rynkiewicz, EC, Pedersen, AB and Fenton, A (2015) An ecosystem approach to understanding and managing within-host parasite community dynamics. Trends in Parasitology 31, 212–221.CrossRefGoogle ScholarPubMed
Schell, SC (1985) Handbook of trematodes of North America North of Mexico. Moscow, Idaho, USA: University Press of Idaho, pp. 1–263.Google Scholar
Schotthoefer, AM, Cole, RA and Beasley, VR (2003) Relationship of tadpole stage to location of echinostome cercariae encystment and the consequences for tadpole survival. The Journal of parasitology 89, 475–482.CrossRefGoogle ScholarPubMed
Smyth, JD and Halton, DW (1983) The Physiology of Trematodes, 2nd Edn. Cambridge: Cambridge University Press.Google Scholar
Sousa, WP (1993) Interspecific antagonism and species coexistence in a diverse guild of larval trematode parasites. Ecological Monographs 63, 103–128.CrossRefGoogle Scholar
Studer, A and Poulin, R (2012) Seasonal dynamics in an intertidal mudflat: the case of a complex trematode life cycle. Marine Ecology Progress Series 455, 79–93.CrossRefGoogle Scholar
Szuroczki, D and Richardson, JML (2009) The role of trematode parasites in larval anuran communities: an aquatic ecologist's guide to the major players. Oecologia 161, 371–385.CrossRefGoogle ScholarPubMed
Taylor, MD, van der Werf, N and Maizels, RM (2012) T cells in helminth infection: the regulators and the regulated. Trends in Immunology 33, 181–189.CrossRefGoogle ScholarPubMed
Telfer, S, Birtles, R, Bennett, M, Lambin, X, Paterson, S and Begon, M (2008) Parasite interactions in natural populations: insights from longitudinal data. Parasitology 135, 767–781.CrossRefGoogle ScholarPubMed
Telfer, S, Lambin, X, Birtles, R, Beldomenico, P, Burthe, S, Paterson, S and Begon, M (2010) Species interactions in a parasite community drive infection risk in a wildlife population. Science (New York, N.Y.) 330, 243–246.CrossRefGoogle Scholar
Thiemann, GW and Wassersug, RJ (2000) Biased distribution of trematode metacercariae in the nephric system of Rana Tadpoles. Journal of Zoology, London 252, 534–538.CrossRefGoogle Scholar
Vannatta, JT, Knowles, T, Minchella, DJ and Gleichsner, AM (2020) The road not taken: host infection status influences parasite host-choice. Journal of Parasitology 106, 1.CrossRefGoogle Scholar
Venables, WN and Ripley, BD (2002) Modern Applied Statistics with S, 4th Edn. New York: Springer.CrossRefGoogle Scholar
Wickham, H (2016) ggplot2: Elegant Graphics for Data Analysis. New York: Springer-Verlag.CrossRefGoogle Scholar
Wuerthner, VP, Hua, J and Hoverman, JT (2017) The benefits of coinfection: trematodes alter disease outcomes associated with virus infection. Journal of Animal Ecology 86, 921–931.CrossRefGoogle ScholarPubMed