Generalist parasites have the capacity to infect multiple hosts. The temporal pattern of host specificity by generalist parasites is rarely studied, but is critical to understanding what variables underpin infection and thereby the impact of parasites on host species and the way they impose selection on hosts. Here, the temporal dynamics of infection of four species of freshwater mussel by European bitterling fish (Rhodeus amarus) was investigated over three spawning seasons. Bitterling lay their eggs in the gills of freshwater mussels, which suffer reduced growth, oxygen stress, gill damage and elevated mortality as a result of parasitism. The temporal pattern of infection of mussels by European bitterling in multiple populations was examined. Using a Bernoulli Generalized Additive Mixed Model with Bayesian inference it was demonstrated that one mussel species, Unio pictorum, was exploited over the entire bitterling spawning season. As the season progressed, bitterling showed a preference for other mussel species, which were inferior hosts. Temporal changes in host use reflected elevated density-dependent mortality in preferred hosts that were already infected. Plasticity in host specificity by bitterling conformed with the predictions of the host selection hypothesis. The relationship between bitterling and their host mussels differs qualitatively from that of avian brood parasites.

Bell Pettigrew Museum of Natural History University of St Andrews Bute Building St Andrews Fife KY16 9TS UK

Institute of Vertebrate Biology Academy of Sciences of the Czech Republic Brno Czech Republic

School of Biology University of St Andrews St Andrews UK

See more in PubMed

Bauer G. The adaptive value of offspring size among freshwater mussels (Bivalvia; Unionoidea) J Anim Ecol. 1994;1:933–944. doi: 10.2307/5270. DOI

Briskie JV, Sealy SG, Hobson KA. Differential parasitism of least flycatchers and yellow warblers by the brown-headed cowbird. Behav Ecol Sociobiol. 1990;27:403–410. doi: 10.1007/BF00164066. DOI

Briskie JV, Sealy SG, Hobson KA. Behavioral defenses against avian brood parasitism in sympatric and allopatric host populations. Evolution. 1992;46:334–340. doi: 10.2307/2409854. PubMed DOI

Brooker LC, Brooker MG. Why are cuckoos host specific? Oikos. 1990;57:301–309. doi: 10.2307/3565958. DOI

Bryja J, Smith C, Reichard M. Range-wide population genetic structure of the European bitterling based on microsatellites and mtDNA. Mol Ecol. 2010;19:4708–4722. doi: 10.1111/j.1365-294X.2010.04844.x. PubMed DOI

Burnham KP, Anderson DR. P values are only an index to evidence: 20th-vs. 21st-century statistical science. Ecology. 2014;95:627–630. doi: 10.1890/13-1066.1. PubMed DOI

Chang C-H, Li F, Shao K-T, Lin Y-S, Morosawa T, Kim S, Koo H, Kim W, Lee J-S, He S, Smith C, Reichard M, Miya M, Chen W-J, Mayden RL. Phylogenetic relationships of Acheilognathidae (Cypriniformes: Cyprinoidea) as revealed from evidence of both nuclear and mitochondrial gene sequence variation: evidence for necessary taxonomic revision in the family and the identification of cryptic species. Mol Phylogenet Evol. 2014;81:182–194. doi: 10.1016/j.ympev.2014.08.026. PubMed DOI

Davies N. Cuckoo: cheating by nature. London: Bloomsbury; 2015.

Detwiler JT, Minchella DJ. Intermediate host availability masks the strength of experimentally-derived colonisation patterns in echinostome trematodes. Int J Parasitol. 2009;39:585–590. doi: 10.1016/j.ijpara.2008.10.008. PubMed DOI

Feeney WE, Welbergen JA, Langmore NE. Advances in the study of coevolution between avian brood parasites and their hosts. Ann Rev Ecol Evol Syst. 2014;45:227–246. doi: 10.1146/annurev-ecolsys-120213-091603. DOI

Giorgi MS, Arlettaz R, Guillaume F, Nusslé S, Ossola C, Vogel P, Christe P. Causal mechanisms underlying host specificity in bat ectoparasites. Oecologia. 2004;138:648–654. doi: 10.1007/s00442-003-1475-1. PubMed DOI

Honza M, Taborsky B, Taborsky M, Teuschl Y, Vogl W, Moksnes A, Røskaft E. Behaviour of female common cuckoo Cuculus canorus, in the vicinity of host nests before and during egg laying: a radiotelemetry study. Anim Behav. 2002;64:861–868. doi: 10.1006/anbe.2002.1969. DOI

Hoover JP, Brittingham MC. Regional variation in cowbird parasitism of wood thrushes. Wilson Bull. 1993;105:228–238.

Hornbach DJ, Deneka T. A comparison of a qualitative and a quantitative collection method for examining freshwater mussel assemblages. J N Am Benthol Soc. 1996;1:587–596. doi: 10.2307/1467809. DOI

Ieno EN, Zuur AF. Data exploration and visualisation with R. Newburgh: Highland Statistics Ltd; 2015.

Kaltz O, Shykoff JA. Local adaptation in host–parasite systems. Heredity. 1998;81:361–370. doi: 10.1046/j.1365-2540.1998.00435.x. DOI

Karplus I. Symbiosis in fishes: the biology of interspecific partnerships. Oxford: Wiley-Blackwell; 2014.

Kawamura K, Ueda T, Arai R, Smith C. Phylogenetic relationships of bitterling fishes (Teleostei: Cypriniformes: Acheilognathinae), inferred from mitochondrial cytochrome b sequences. Zool Sci. 2014;31:321–341. doi: 10.2108/zs130233. PubMed DOI

Kitamura J, Nagata N, Nakajima J, Sota T. Divergence of ovipositor length and egg shape in a brood parasitic bitterling fish through the use of different mussel hosts. J Evol Biol. 2012;25:566–573. doi: 10.1111/j.1420-9101.2011.02453.x. PubMed DOI

Kruschke JK. Doing Bayesian data analysis. London: Academic Press; 2015.

Liu H, Yurong Z, Reichard M, Smith C. Evidence of host specificity and congruence between phylogenies of bitterlings and freshwater mussels. Zool Stud. 2006;45:428–434.

Lopes-Lima M, Teixeira A, Froufe E, Lopes A, Varandas S, Sousa R. Biology and conservation of freshwater bivalves: past, present and future perspectives. Hydrobiologia. 2014;735:1–13. doi: 10.1007/s10750-014-1902-9. DOI

Lopes-Lima M, Froufe E, Ghamizi M, Mock KE, Kebapçi Ü, Klishko O, Kovitvadhi S, Kovitvadhi U, Paulo OS, Pfeiffer JM, Raley M, Riccardi N, Şereflişan H, Sousa R, Teixeira A, Varandas S, Wu X, Zanatta DT, Zieritz A, Bogan AE. Phylogeny of the most species rich freshwater bivalve family (Bivalvia: Unionida: Unionidae): Defining modern subfamilies and tribes. Mol Phyl Evol. 2017;106:174–191. doi: 10.1016/j.ympev.2016.08.021. PubMed DOI

Mason P. Brood parasitism in a host generalist, the shiny cowbird: II. Host selection. Auk. 1986;103:61–69.

Medina I, Langmore NE. The evolution of host specialisation in avian brood parasites. Ecol Lett. 2016;19:1110–1118. doi: 10.1111/ele.12649. PubMed DOI

Mendlová M, Šimková A. Evolution of host specificity in monogeneans parasitizing African cichlid fish. Parasit Vectors. 2014;7:69. doi: 10.1186/1756-3305-7-69. PubMed DOI PMC

Miller AC, Payne BS. Qualitative versus quantitative sampling to evaluate population and community characteristics at a large-river mussel bed. Am Midl Nat. 1993;1:133–145. doi: 10.2307/2426282. DOI

Pateman-Jones C, Rasotto MB, Reichard M, Liao C, Liu H, Zięba G, Smith C. Variation in male reproductive traits among three bitterling fishes (Acheilognathinae: Cyprinidae) in relation to mating system. Biol J Linn Soc. 2011;103:622–632. doi: 10.1111/j.1095-8312.2011.01648.x. DOI

Patten MA, Reinking DL, Wolfe DH. Hierarchical cues in brood parasite nest selection. J Ornithol. 2011;152:521–532. doi: 10.1007/s10336-010-0608-7. DOI

Payne RB. Avian brood parasitism. Host-parasite evolution: general principles and avian models. In: Clayton DH, Moore J, editors. Host-parasite evolution: general principles and avian models. Oxford: Oxford University Press; 1997. pp. 338–369.

Poulin R. Evolutionary ecology of parasites. Princeton: Princeton University Press; 2011.

Poulin R, Krasnov BR, Mouillot D. Host specificity in phylogenetic and geographic space. Trends Parasitol. 2011;27:355–361. doi: 10.1016/j.pt.2011.05.003. PubMed DOI

R Development Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

Reichard M, Ondračková M, Przybylski M, Liu H, Smith C. The costs and benefits in an unusual symbiosis: experimental evidence that bitterling fish (Rhodeus sericeus) are parasites of unionid mussels in Europe. J Evol Biol. 2006;19:788–796. doi: 10.1111/j.1420-9101.2005.01051.x. PubMed DOI

Reichard M, Liu H, Smith C. The co-evolutionary relationship between bitterling fishes and freshwater mussels: insights from interspecific comparisons. Evol Ecol Res. 2007;9:1–21.

Reichard M, Przybylski M, Kaniewska P, Liu H, Smith C. A possible evolutionary lag in the relationship between freshwater mussels and European bitterling. J Fish Biol. 2007;70:709–725. doi: 10.1111/j.1095-8649.2007.01333.x. DOI

Reichard M, Smith C, Bryja P. Seasonal change in the opportunity for sexual selection. Mol Ecol. 2008;17:642–651. doi: 10.1111/j.1365-294X.2007.03602.x. PubMed DOI

Reichard M, Ondračová M, Bryjova A, Smith C, Bryja J. Breeding resource distribution affects selection gradients on male phenotypic traits: experimental study on lifetime reproductive success in the bitterling fish (Rhodeus amarus) Evolution. 2009;63:377–390. doi: 10.1111/j.1558-5646.2008.00572.x. PubMed DOI

Reichard M, Polačik M, Tarkan AS, Spence R, Gaygusuz Ö, Ercan E, Ondračková M, Smith C. The bitterling–mussel coevolutionary relationship in areas of recent and ancient sympatry. Evolution. 2010;64:3047–3056. PubMed

Reichard M, Vrtílek M, Douda K, Smith C. An invasive species causes role reversal in a host-parasite relationship. Biol Lett. 2012;8:601–604. doi: 10.1098/rsbl.2011.1234. PubMed DOI PMC

Reichard M, Douda K, Przybylski M, Popa OP, Karbanová E, Matasová K, Rylková K, Polačik M, Blažek R, Smith C. Population-specific responses to an invasive species. Proc R Soc Lond B. 2015;282:20151063. doi: 10.1098/rspb.2015.1063. PubMed DOI PMC

Shimizu A, Aida K, Hanyu I. Effects of photoperiod and temperature on gonadal activity and plasma steroid levels in an autumn-spawning bitterling, Acheilognathus rhombea, during different phases of its annual reproductive cycle. Gen Comp Endocrinol. 1994;93:137–150. doi: 10.1006/gcen.1994.1016. PubMed DOI

Smith JN, Myers-Smith IH. Spatial variation in parasitism of song sparrows by brown-headed cowbirds. Oxf Ornithol Ser. 1998;9:296–312.

Smith C, Reichard M. A sperm competition model for the European bitterling (Rhodeus amarus) Behaviour. 2013;150:1709–1730. doi: 10.1163/1568539X-00003116. DOI

Smith C, Reynolds JD, Sutherland WJ. Adaptive host choice and avoidance of superparasitism in the spawning decisions of bitterling (Rhodeus sericeus) Behav Ecol Sociobiol. 2000;48:29–35. doi: 10.1007/s002650000212. DOI

Smith C, Reynolds JD, Sutherland WJ, Jurajda P. The population consequences of reproductive decisions. Proc R Soc Lond B. 2000;267:1327–1334. doi: 10.1098/rspb.2000.1146. PubMed DOI PMC

Smith C, Rippon K, Douglas A, Jurajda P. A proximate cue for oviposition site choice in the bitterling (Rhodeus sericeus) Freshw Biol. 2001;46:903–911. doi: 10.1046/j.1365-2427.2001.00725.x. DOI

Smith C, Reichard M, Jurajda P, Przybylski M. The reproductive ecology of the European bitterling (Rhodeus sericeus) J Zool. 2004;262:107–124. doi: 10.1017/S0952836903004497. DOI

Smith C, Warren M, Rouchet R, Reichard M. The function of multiple ejaculations in bitterling. J Evol Biol. 2014;27:1819–1829. doi: 10.1111/jeb.12432. PubMed DOI

Soler M. Long-term coevolution between avian brood parasites and their hosts. Biol Rev Camb Philos Soc. 2014;89:688–704. doi: 10.1111/brv.12075. PubMed DOI

Soler JJ, Møller AP, Soler M, Martínez JG. Interactions between a brood parasite and its host in relation to parasitism and immune defence. Evol Ecol Res. 1999;1:189–210.

Spence R, Smith C. Rose bitterling (Rhodeus ocellatus) embryos parasitise freshwater mussels by competing for nutrients and oxygen. Acta Zool. 2013;94:113–118. doi: 10.1111/j.1463-6395.2011.00532.x. DOI

Stadnichenko AP, Stadnichenko YA. On the effect of bitterling larvae on the lamellibranchid mollusc Unio rostratus gentilis Haas. Gidrobiol Zhurnal. 1980;1980:57–61.

Su Y-S, Yajima M (2012) R2jags: a package for running JAGS from R. http://CRAN.R-project.org/package=R2jags

Van Damme D, Bogutskaya N, Hoffmann RC, Smith C. The introduction of the European bitterling (Rhodeus amarus) to West and Central Europe. Fish Fish. 2007;8:79–106. doi: 10.1111/j.1467-2679.2007.00239.x. DOI

van Dijken MJ, Waage JK. Self and conspecific superparasitism by the egg parasitoid Trichogramma evanescens. Entomol Exp Appl. 1987;43:183–192. doi: 10.1111/j.1570-7458.1987.tb03604.x. DOI

Wand MP, Ormerod JT. On semiparametric regression with O’Sullivan penalized splines. Aust NZ J Stat. 2008;50:179–198. doi: 10.1111/j.1467-842X.2008.00507.x. DOI

Ward D, Smith JNM. Interhabitat differences in parasitism frequencies by brown-headed cowbirds in the Okanagan Valley, British Columbia. In: Smith JNM, Cook TL, Rothstein SI, Robinson SK, Sealy SG, editors. Ecology and management of cowbirds and their hosts. Austin: University of Texas Press; 2000. pp. 210–219.

Wiepkema PR. An ethological analysis of the reproductive behaviour of the bitterling (Rhodeus amarus Bloch) Arch Neerl Zool. 1961;14:103–199. doi: 10.1163/036551661X00052. DOI

Wootton RJ, Smith C. Reproductive biology of teleost fishes. Oxford: Wiley-Blackwell; 2015.

Zaki SAH, Jordan WC, Reichard M, Przybylski M, Smith C. A morphological and genetic analysis of the European bitterling species complex. Biol J Linn Soc. 2008;95:337–347. doi: 10.1111/j.1095-8312.2008.01050.x. DOI

Zuur A, Ieno EN, Walker N, Saveliev AA, Smith GM. Mixed effects models and extensions in ecology with R. New York: Springer; 2009.

Zuur AF, Ieno EN, Elphick CS. A protocol for data exploration to avoid common statistical problems. Methods Ecol Evol. 2010;1:3–14. doi: 10.1111/j.2041-210X.2009.00001.x. DOI

Zuur AF, Saveliev AA, Ieno EN. A beginner’s guide to generalised additive mixed models with R. Newburgh: Highland Statistics Ltd; 2014.