Abstract
Invasive species tend to acquire native parasites from their invaded range over time. In these cases, native host-parasite dynamics may be altered as a result of differences in parasite population biology and host competency between invasive and native hosts. Competent invasive hosts are likely to increase transmission to native hosts while incompetent invasive hosts may dilute infection in natives. In this study, we used a freshwater fish system and a survey approach to compare the host competency and population biology of a dominant helminth parasite, Pomphorhynchus tereticollis, between native brown trout (Salmo trutta) hosts and invasive dace (Leuciscus leuciscus) hosts over 2 years at the core and edge of dace’s invasive range in Ireland. Our results show that, although dace acquired P. tereticollis, dace had prevalent and high intensity infections of immature extra-intestinal worms while prevalence of adult worms was consistently higher in brown trout. The majority of parasite individuals infecting dace were immature extra-intestinal forms and, in contrast to brown trout, parasites in dace did not attain sexual maturity. In addition, brown trout from the invasion core where dace have been established the longest had a lower abundance of P. tereticollis, indicating that by taking up but not transmitting infective stages of the parasite, invasive dace may dilute P. tereticollis infection in the native host.
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References
Britton J (2007) Reference data for evaluating the growth of common riverine fishes in the UK. J Appl Ichthyol 23:555–560
Brooks ME, Kristensen K, Benthem KJ, Magnusson A, Berg CW, Nielsen A, Skaug HJ, Maechler M, Bolker BM (2017) glmm TMB balances speed and flexibility among packages for zero-inflated Generalized Linear Mixed Modeling. The R Journal 9:378–400
Brown A, Chubb J, Veltkamp C (1986) A key to the species of Acanthocephala parasitic in British freshwater fishes. J Fish Biol 28:327–334
Bush AO, Lafferty KD, Lotz JM, Shostak AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol 83(4):575–583
Byrne CJ (2000) The parasite community structure of stocked and wild brown trout (Salmo trutta L.). PhD thesis, Trinity College Dublin, pp 283–288
Byrne CJ, Holland CV, Poole R, Kennedy CR (2002) Comparison of the macroparasite communities of wild and stocked brown trout (Salmo trutta L.) in the west of Ireland. Parasitology 124:435–445
Byrne CJ, Holland CV, Kennedy CR, Poole WR (2003) Interspecific interactions between Acanthocephala in the intestine of brown trout: Are they more frequent in Ireland? Parasitology 127:399–409
Byrne CJ, Holland CV, Walsh E, Mulligan C, Kennedy CR, Poole WR (2004) Utilization of brown trout Salmo trutta by Acanthocephalus clavula in an Irish lake: is this evidence of a host shift. J Helminthol 78:201–206
Caffrey JM, Hayden B, Walsh T (2007) Dace (Leuciscus leuciscus L.): an Invasive Fish Species in Ireland. Irish Freshwater Fisheries, Ecology and Management No. 5. Central Fisheries Board, Dublin, Ireland
Caffrey J, Gallagher K, Broughan D, Dick JT (2018) Rapid response achieves eradication–chub in Ireland. Manag Biol Invasions 9:475–482
Chubb JC (1982) Seasonal occurrence of helminths in freshwater fishes Part IV. Adult Cestoda, Nematoda and Acanthocephala. Advances in Parasitology, vol 20. Academic Press, New York, pp 1–292
Conneely JJ, McCarthy TK (1988) The metazoan parasites of trout (Salmo trutta L.) in western Ireland. Polskie Archiwum Hydrobiologii/Polish Arch Hydrobiol 35:443–460
Couso-Pérez S, Cañizo-Outeiriño A, Campo-Ramos R, Ares-Mazás E, Gómez-Couso H (2018) Remarkable differences in the presence of the acanthocephalan parasite Echinorhynchus truttae in brown trout (Salmo trutta) captured in two adjacent river basins in Galicia (NW Spain). Parasitol Open 4
Delanty K, Kelly FL, McLoone P, Matson R, O’ Briain R, Gordon P, Cierpal D, Connor L, Corcoran W, Coyne J, Feeney R, Morrissey E (2017) Fish Stock Assessment of the River Barrow Catchment 2015. Inland Fisheries Ireland, 3044 Lake Drive, Citywest Business Campus, Dublin 24, Ireland
Dezfuli B, Castaldelli G, Bo T, Lorenzoni M, Giari L (2011) Intestinal immune response of Silurus glanis and Barbus barbus naturally infected with Pomphorhynchus laevis (Acanthocephala). Parasite Immunol 33:116–123
Dunn AM, Hatcher MJ (2015) Parasites and biological invasions: parallels, interactions, and control. Trends Parasitol 31:189–199
Emde S, Rueckert S, Palm HW, Klimpel S (2012) Invasive Ponto-Caspian amphipods and fish increase the distribution range of the acanthocephalan Pomphorhynchus tereticollis in the river Rhine. PLoS ONE 7:e53218
Emde S, Rueckert S, Kochmann J, Knopf K, Sures B, Klimpel S (2014) Nematode eel parasite found inside acanthocephalan cysts-a” Trojan horse” strategy? Parasites Vectors 7:1–5
Fitzgerald RD, Mulcahy MF (1983) Parasites of salmon Salmo salar L. and trout Salmo trutta L. in the River Shournagh. Adv Fish Biol Ireland 25:24–31
Gagne RB, Heins DC, McIntyre PB, Gilliam JF, Blum MJ (2016) Mutual dilution of infection by an introduced parasite in native and invasive stream fishes across Hawaii. Parasitology 143:1605
Gendron AD, Marcogliese DJ (2016) Reduced survival of a native parasite in the invasive round goby: evidence for the dilution hypothesis? Aquat Invasions 11:189–198
Gendron AD, Marcogliese DJ (2017) Enigmatic decline of a common fish parasite (Diplostomum spp.) in the St. Lawrence River: evidence for a dilution effect induced by the invasive round goby. Int J Parasitol Parasites Wildl 6:402–411
Goedknegt MA, Feis ME, Wegner KM, Luttikhuizen PC, Buschbaum C, Camphuysen KCJ, van der Meer J, Thieltges DW (2015) Parasites and marine invasions: ecological and evolutionary perspectives. J Sea Res 113:11–27
Gourbière S, Morand S, Waxman D (2015) Fundamental factors determining the nature of parasite aggregation in hosts. PLoS ONE 10:e0116893
Grabner DS, Weigand AM, Leese F, Winking C, Hering D, Tollrian R, Sures B (2015) Invaders, natives and their enemies: distribution patterns of amphipods and their microsporidian parasites in the Ruhr Metropolis, Germany. Parasites Vect 8:419
Hartig (2020) DHARMa: Residual Diagnostics for Hierarchical (Multi-Level / Mixed) Regression Models. R package version 0.2.7. https://florianhartig.github.io/DHARMa/
Hine P, Kennedy C (1974a) Observations on the distribution, specificity and pathogenicity of the acanthocephalan Pomphorhynchus laevis (Müller). J Fish Biol 6:521–535
Hine P, Kennedy C (1974b) The population biology of the acanthocephalan Pomphorhynchus laevis (Müller) in the River Avon. J Fish Biol 6:665–679
Holland CV, Kennedy CR (1997) A checklist of parasitic helminth and crustacean species recorded in freshwater Fish from Ireland. Biol Environ Proc Royal Irish Acad 97B:225–243
Inland Fisheries Ireland (2015) The Economic Contribution of Brown Trout Angling in Ireland. National Strategy for Angling Development. https://www.fisheriesireland.ie/documents/530-the-economic-contribution-of-brown-trout-angling-in-ireland.html. Accessed 22 Oct 2018
Johnson PTJ, Thieltges DW (2010) Diversity, decoys and the dilution effect: how ecological communities affect disease risk. J Exp Biol 213:961–970
Jonsson N, Næsje T, Jonsson B, Saksgård R, Sandlund O (1999) The influence of piscivory on life history traits of brown trout. J Fish Biol 55:1129–1141
Kane MB (1966) Parasites of Irish fishes. Sci Proc Royal Dublin Soc B1(18):205–220
Kelehear C, Brown GP, Shine R (2012) Rapid evolution of parasite life history traits on an expanding range-edge. Ecol Lett 15:329–337
Kelly DW, Paterson RA, Townsend CR, Poulin R, Tompkins DM (2009) Parasite spillback: a neglected concept in invasion ecology? Ecol 90:2047–2056
Kelly FL, Harrison A, Connor L, Matson R, Morrissey E, Feeney R, Wogerbauer C, Rocks K, O’Callaghan R (2011) Sampling Fish for the Water Framework Directive—Summary Report 2010. Inland Fisheries Ireland, Citywest Business Campus, Dublin 24, Ireland
Kelly FL, Connor L, Matson R, Feeney R, Morrissey E, Coyne J, Rocks K (2015) Sampling fish for the water directive framework—Summary Report 2014. Inland Fisheries Ireland, Citywest Business Campus, Dublin 24, Ireland
Kelly-Quinn M, Bracken J (1990) A seasonal analysis of the diet and feeding dynamics of brown trout, Salmo trutta L., in a small nursery stream. Aquacult Res 21:107–124
Kennedy CR (1996) Colonization and establishment of Pomphorhynchus laevis (Acanthocephala) in an isolated English river. J Helminthol 70:27–31
Kennedy CR (2003) Evolution of host-parasite systems in the Acanthocephala: speciation and scale in the genus Pomphorhynchus. In: Combes C, Jourdane J (eds) Taxonomie, Ecologie et Evolution des Métazoaires Parasites, Tome II edn. Presses Universitaires de Perpignan, Perpignan, pp 11–35
Kennedy CR (2006) Ecology of the Acanthocephala. Cambridge University Press, Cambridge, pp 28–278
Kennedy CR (2009) The ecology of parasites of freshwater fishes: the search for patterns. Parasitology 136:1653–1662
Kennedy M, Fitzmaurice P (1971) Growth and food of brown trout Salmo trutta (L.) in Irish waters. Proc Royal Irish Academy. Section B: Biological, Geological, and Chemical Science. Royal Irish Academy, Dublin, pp 269–352
Kennedy CR, Bates R, Brown A (1989) Discontinuous distributions of the fish acanthocephalans Pomphorhynchus laevis and Acanthocephalus anguillae in Britain and Ireland: an hypothesis. J Fish Biol 34:607–619
L’Abée-Lund J, Langeland A, Sægrov H (1992) Piscivory by brown trout Salmo trutta L. and Arctic charr Salvelinus alpinus (L.) in Norwegian lakes. J Fish Biol 41:91–101
Loxton KC, Lawton C, Stafford P, Holland CV (2016) Reduced helminth parasitism in the introduced bank vole (Myodes glareolus): more parasites lost than gained. Int J Parasitol Parasites Wildl 5:175–183
Loxton KC, Lawton C, Stafford P, Holland CV (2017) Parasite dynamics in an invaded ecosystem: helminth communities of native wood mice are impacted by the invasive bank vole. Parasitology 144:1476–1489
Lyndon AR, Kennedy CR (2001) Colonisation and extinction in relation to competition and resource partitioning in acanthocephalans of freshwater fishes of the British Isles. Folia Parasitol 48(1):37–46
Mann R (1974) Observations on the age, growth, reproduction and food of the dace, Leuciscus leuciscus (L.), in two rivers in southern England. J Fish Biol 6:237–253
Médoc V, Rigaud T, Motreuil S, Perrot-Minnot MJ, Bollache L (2011) Paratenic hosts as regular transmission route in the acanthocephalan Pomphorhynchus laevis: potential implications for food webs. Naturwissenschaften 98:825
Molloy S, Holland CV, O’Regan M (1995a) Population biology of Pomphorhynchus laevis in brown trout from two lakes in the west of Ireland. J Helminthol 69:229–235
Molloy S, Holland CV, Poole R (1995b) Metazoan parasite community structure in brown trout from two lakes in western Ireland. J Helminthol 69:237–242
Moriarty C, Fitzmaurice P (2000) Origin and diversity of freshwater fishes in Ireland. Internationale Vereinigung für theoretische und angewandte Limnologie: Verhandlungen 27:128–130
Odening K (1976) Conception and terminology of hosts in parasitology. Adv Parasitol 14:1–93
O’Mahony E, Bradley D, Kennedy C, Holland C (2004a) Evidence for the hypothesis of strain formation in Pomphorhynchus laevis (Acanthocephala): an investigation using mitochondrial DNA sequences. Parasitology 129:341–347
O’Mahony E, Kennedy C, Holland C (2004b) Comparison of morphological characters in Irish and English populations of the acanthocephalan Pomphorhynchus laevis (Müller, 1776). Syst Parasitol 59:147–157
Paterson RA, Rauque CA, Fernandez MV, Townsend CR, Poulin R, Tompkins DM (2013a) Native fish avoid parasite spillback from multiple exotic hosts: consequences of host density and parasite competency. Biol Invasions 15:205–2218
Paterson RA, Lal A, Dale M, Townsend CR, Poulin R, Tompkins DM (2013b) Relative competence of native and exotic fish hosts for two generalist native trematodes. Int J Parasitol Parasites Wildl 2:136–143
Perrot-Minnot M-J (2004) Larval morphology, genetic divergence, and contrasting levels of host manipulation between forms of Pomphorhynchus laevis (Acanthocephala). Int J Parasitol 34:45–54
Perrot-Minnot M-J, Špakulová M, Wattier R, Kotlík P, Düşen S, Aydoğdu A, Tougard C (2018) Contrasting phylogeography of two Western Palaearctic fish parasites despite similar life cycles. J Biogeogr 45:101–115
Perrot-Minnot M-J, Guyonnet E, Bollache L, Lagrue C (2019) Differential patterns of definitive host use by two fish acanthocephalans occurring in sympatry: Pomphorhynchus laevis and Pomphorhynchus tereticollis. Int J Parasitol Parasites Wildl 8:135–144
Poulin R (2017) Invasion ecology meets parasitology: advances and challenges. Int J Parasitol 6:361–363
Poulin R, Valtonen ET (2002) The predictability of helminth community structure in space: a comparison of fish populations from adjacent lakes. Int J Parasitol 32:1235–1243
Poulin R, Paterson RA, Townsend CR, Tompkins DM, Kelly DW (2011) Biological invasions and the dynamics of endemic diseases in freshwater ecosystems. Freshwat Biol 56:676–688
Prenter J, MacNeil C, Dick JTA, Dunn AM (2004) Roles of parasites in animal invasions. Trends Ecol Evol 19:385–390
Reier S, Sattmann H, Schwaha T, Harl J, Konecny R, Haring E (2019) An integrative taxonomic approach to reveal the status of the genus Pomphorhynchus Monticelli, 1905 (Acanthocephala: Pomphorhynchidae) in Austria. Int J Parasitol Parasites Wildl 8:145–155
Ricciardi A, Blackburn TM, Carlton JT, Dick JT, Hulme PE, Iacarella JC, Jeschke JM, Liebhold AM, Lockwood JL, MacIsaac HJ (2017) Invasion science: a horizon scan of emerging challenges and opportunities. Trends Ecol Evol 32:464–474
RStudio Team (2019) RStudio: Integrated Development for R., Version 1.2.5019. RStudio Inc., Boston, MA. http://www.rstudio.com/
Sarabeev V, Balbuena JA, Morand S (2017) Testing the enemy release hypothesis: abundance and distribution patterns of helminth communities in grey mullets (Teleostei: Mugilidae) reveal the success of invasive species. Int J Parasitol 47:687–696
Scherer R (2018) PropCIs: various confidence interval methods for proportions. R package version 0.3-0
Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671
Sherrard-Smith E, Chadwick EA, Cable J (2015) The impact of introduced hosts on parasite transmission: opisthorchiid infections in American mink (Neovison vison). Biol Invasions 17:115–122
Špakulová M, Perrot-Minnot M-J, Neuhaus B (2011) Resurrection of Pomphorhynchus tereticollis (Rudolphi, 1809)(Acanthocephala: Pomphorhynchidae) based on new morphological and molecular data. Helminthologia 48:268–277
Stuart P, Paredis L, Henttonen H, Lawton C, Torres CAO, Holland CV (2020) The hidden faces of a biological invasion: parasite dynamics of invaders and natives. Int J Parasitol 50:111–123
Sures B, Dezfuli BS, Krug HF (2003) The intestinal parasite Pomphorhynchus laevis (Acanthocephala) interferes with the uptake and accumulation of lead (210Pb) in its fish host chub (Leuciscus cephalus). Int J Parasitol 33:1617–1622
Taraschewski H (1985) Experimental transmission of Acanthocephalus anguillae (Palaeacanthocephala). Zeitschrift für Parasitenkunde 71:825–828
Taraschewski H (1989) Acanthocephalus anguillae in intra-and extraintestinal positions in experimentally infected juveniles of goldfish and carp and in sticklebacks. J Parasitol 75:108–118
Telfer S, Lambin X, Birtles R, Beldomenico P, Burthe S, Paterson S, Begon M (2010) Species interactions in a parasite community drive infection risk in a wildlife population. Science 330:243–246
Thieltges DW, Reise K, Prinz K, Jensen KT (2009) Invaders interfere with native parasite–host interactions. Biol Invasions 11:1421–1429
Tinsley RC, Vineer HR, Grainger-Wood R, Morgan ER (2019) Heterogeneity in helminth infections: factors influencing aggregation in a simple host–parasite system. Parasitology 147:65–77
Torchin ME, Lafferty KD, Dobson AP, McKenzie VJ, Kuris AM (2003) Introduced species and their missing parasites. Nature 421:628–630
Vogel S (2018) Update on selected topics in acanthocephalan parasites research. Helminthologia 55:351–352. https://doi.org/10.2478/helm-2018-0023
Warburton EM, Vonhof MJ (2018) From individual heterogeneity to population-level overdispersion: quantifying the relative roles of host exposure and parasite establishment in driving aggregated helminth distributions. Int J Parasitol 48:309–318
Went A (1950) Notes on the introduction of some freshwater fish into Ireland. J Dept Agric 47:119–124
White TA, Perkins SE (2012) The ecoimmunology of invasive species. Funct Ecol 26:1313–1323
Wilson K, Bjørnstad ON, Dobson AP, Merler S, Poglayen G, Randolph SE, Read AD, Skor** A (2002) Heterogeneities in macroparasite infections: patterns and processes. In: Hudson PJ, Rizzoli A, Grenfell BT, Heesterbeek H, Dobson AP (eds) The ecology of wildlife diseases. Oxford University Press, Oxford, pp 6–44
Young RE, MacColl AD (2017) Spatial and temporal variation in macroparasite communities of three-spined stickleback. Parasitology 144:436–449
Acknowledgements
Our thanks to Inland Fisheries Ireland staff for fish collection. We thank M. Williams, R. Byrne, A. Mooney, C. Patmore and S. Wheldon for field assistance and N. Fitzgerald, A. Clark and J. Picard for laboratory assistance. Author P.T was supported by funding from Inland Fisheries Ireland and a Postgraduate Research Studentship from Trinity College Dublin, without which this work could not have been undertaken.
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Electrofishing and euthanasia of fish was carried out by trained Inland Fisheries Ireland staff. This work was approved by the Trinity College Dublin School of Natural Science’s Research Ethics Committee.
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Tierney, P.A., Caffrey, J.M., Vogel, S. et al. Invasive freshwater fish (Leuciscus leuciscus) acts as a sink for a parasite of native brown trout Salmo trutta. Biol Invasions 22, 2235–2250 (2020). https://doi.org/10.1007/s10530-020-02253-1
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DOI: https://doi.org/10.1007/s10530-020-02253-1