Abstract
The freshwater pearl mussel (Margaritifera margaritifera) is an endangered bivalve with an obligate parasitic stage on salmonids. Host suitability studies have shown that glochidial growth and load vary significantly between host strains as well as among individuals of a suitable strain. Variation in host suitability has been linked to environmental conditions, host age and/or size, genetic composition of the host and parasite, or a combination of these factors. In our study, we wanted to investigate if brown trout (Salmo trutta) displayed an age-dependent response to glochidial infestation. We hypothesised that 1+ naive brown trout hosts tolerate glochidial infestation better than 0+ hosts. In order to test our hypothesis, we infested 0+ and 1+ hatchery reared brown trout with glochidia from closely related mothers and kept them under common garden conditions. This allowed us to observe a pure age dependent host response to infestation, as we eliminated the confounding effect of genotype-specific host interactions. We analysed the interaction between glochidial load and host condition, weight and length, and observed a significant age-dependent relationship. Glochidial load was negatively correlated to host condition in 0+ fish hosts and positively correlated in 1+ hosts. These contradictory findings can be explained by a change in host response strategy, from resistance in young to a higher tolerance in older fish. In addition, we also examined the relationship between glochidial load and haematocrit values in the 1+ hosts and observed that haematocrit values were significantly higher in heavily infested hosts. Our results have important conservation implications for the management of wild pearl mussel populations, as well as for captive breeding programmes.
Similar content being viewed by others
References
Adelman JS, Hawley DM (2017) Tolerance of infection: a role for animal behaviour, potential immune mechanisms, and consequences for parasite transmission. Horm Behav 88:79–86. https://doi.org/10.1016/j.yhbeh.2016.10.013
Ahtiainen JJ, Alatalo RV, Kortet R, Rantala MJ (2005) A trade-off between sexual signalling and immune function in a natural population of the drumming wolf spider Hygrolycosa rubrofasciata. J Evol Biol 18:985–991. https://doi.org/10.1111/j.1420-9101.2005.00907.x
Araujo R, Ramos MA (2000) Status and conservation of the giant European freshwater pearl mussel (Margaritifera auricularia) (Spengler, 1793) (Bivalvia: Unionoidea). Biol Conserv 96:233–239. https://doi.org/10.1016/S0006-3207(00)00075-6
Arey LB (1932a) The formation and structure of the glochidial cyst. Biol Bull 62:212–221. https://doi.org/10.2307/1537553
Arey LB (1932b) The nutrition of glochidia during metamorphosis. A microscopical study of the sources and manner of utilization of nutritive substances. J Morphol 53:201–221. https://doi.org/10.1002/jmor.1050530108
Arnott SA, Barber I, Huntingford FA (2000) Parasite-associated growth enhancement in a fish-cestode system. Proc R Soc Lond B Biol Sci 267:657–663. https://doi.org/10.1098/rspb.2000.1052
Awakura T (1968) The ecology of parasitic glochidia of the freshwater pearl mussel, Margaritifera laevis (Haas). Scientific Reports of the Hokkaido Fish Hatchery, No. 23
Barribeau SM, Sadd BM, du Plessis L, Schmid-Hempel P (2014) Gene expression differences underlying genotype-by-genotype specificity in a host-parasite system. PNAS 111:3459–3501. https://doi.org/10.1073/pnas.1318628111
Bauer G (1979) Untersuchungen zur Fortpflanzungsbiologie der Flussperlmuschel (Margaritifera margaritifera) im Fichtelgebirge. Arch Hydrobiol 85:152–165
Bauer G (1987) The parasitic stage of the freshwater pearl mussel (Margaritifera margaritifera L.) II. Susceptibility of brown trout. Arch Hydrobiol Suppl 76:403–412
Bauer G, Vogel C (1987) The parasitic stage of the freshwater pearl mussel (Margaritifera margaritifera L.) I. Host response to glochidiosis. Arch Hydrobiol Suppl 76:393–402
Bauer G, Hochwald S, Silkenat W (1991) Spatial distribution of freshwater mussels: the role of host fish and metabolic rate. Freshw Biol 26:377–386. https://doi.org/10.1111/j.1365-2427.1991.tb01405.x
Beasley CR (1996) The distribution and ecology of the freshwater pearl mussel, Margaritifera margaritifera L. 1758, in County Donegal, Ireland and implications for its conservation. Unpublished Ph.D. Thesis, Queen’s University of Belfast
Best A, White A, Boots M (2014) The coevolutionary implications of host tolerance. Evolution 68:1426–1435. https://doi.org/10.1111/evo.12368
Bonneaud C, Mazuc J, Gonzalez G, Haussy C, Chastel O, Faivre B, Sorci G (2003) Assessing the cost of mounting an immune response. Am Nat 161:367–379. https://doi.org/10.1086/346134
Brommer JE (2004) Immunocompetence and its costs during development: an experimental study in blue tit nestlings. Proc R Soc Lond B Biol Sci 271:S110–S113. https://doi.org/10.1098/rsbl.2003.0103
Carius HJ, Little TJ, Ebert D (2001) Genetic variation in a host-parasite association: potential for coevolution and frequency-dependent selection. Evolution 55:1136–1145. https://doi.org/10.1111/j.0014-3820.2001.tb00633.x
Carlsson J (2008) Effects of microsatellite null alleles on assignment testing. J Hered 99:616–623. https://doi.org/10.1093/jhered/esn048
Chowdhury MMR, Salonen JK, Marjomäki TJ, Taskinen J (2017) Interaction between the endangered freshwater pearl mussel Margaritifera margaritifera, the duck mussel Anodonta anatina and the fish host (Salmo): acquired and cross immunity. Hydrobiologia 810:273–281. https://doi.org/10.1007/s10750-017-3114-6
Cunjak RA, McGladdery SE (1991) The parasite-host relationship of glochidia (Mollusca: Margaritiferidae) on the gills of young-of-the-year Atlantic salmon (Salmo salar). Can J Zool 69:353–358. https://doi.org/10.1139/z91-055
Dakin EE, Avise JC (2004) Microsatellite null alleles in parentage analysis. Heredity 93:504–509. https://doi.org/10.1038/sj.hdy.6800545
Davidson J, Bebak J, Mazik P (2009) The effects of aquaculture production noise on the growth, condition factor, feed conversion, and survival of rainbow trout, Oncorhynchus mykiss. Aquaculture 288:337–343. https://doi.org/10.1016/j.aquaculture.2008.11.037
Denic M, Taeubert JE, Geist J (2015) Trophic relationships between the larvae of two freshwater mussels and their fish hosts. Invertebr Biol 134:129–135. https://doi.org/10.1111/ivb.12080
Dodd BJ, Barnhart MC, Rogers-Lowery CL, Fobian TB, Dimock RV (2005) Cross-resistance of largemouth bass to glochidia of unionid mussels. J Parasitol 91:1064–1072. https://doi.org/10.1645/GE-511R.1
Filipsson K, Brijs J, Näslund J, Wengström N, Adamsson M, Závorka L, Österling ME, Höjesjö J (2017) Encystment of parasitic freshwater pearl mussel (Margaritifera margaritifera) larvae coincides with increased metabolic rate and haematocrit in juvenile brown trout (Salmo trutta). Parasitol Res 116:1353–1360. https://doi.org/10.1007/s00436-017-5413-2
Fustish CA, Millemann RE (1978) Glochidiosis of salmonid fishes. II. Comparison of tissue response of Coho and Chinook salmon to experimental infection with Margaritifera margaritifera (L.) (Pelecypoda: Margaritiferidae). J Parasitol 64:155–157. https://doi.org/10.2307/3279631
Gallaugher P, Farrell AP (1998) Hematocrit and blood oxygen-carrying capacity. In: Perry SF, Tufts BL (eds) Fish physiology: fish respiration. Academic Press, New York, pp 185–227
Geist J (2010) Strategies for the conservation of endangered freshwater pearl mussels (Margaritifera margaritifera L.): a synthesis of conservation genetics and ecology. Hydrobiologia 644:69–88. https://doi.org/10.1007/s10750-010-0190-2
Geist J, Kuehn R (2005) Genetic diversity and differentiation of central European freshwater pearl mussel (Margaritifera margaritifera L.) populations: implications for conservation and management. Mol Ecol 14:425–439. https://doi.org/10.1111/j.1365-294X.2004.02420.x
Geist J, Kuehn R (2008) Host-parasite interactions in oligotrophic stream ecosystems: the roles of life history strategy and ecological niche. Mol Ecol 17:997–1008. https://doi.org/10.1111/j.1365-294X.2007.03636.x
Geist J, Porkka M, Kuehn R (2006) The status of host fish populations and fish species richness in European freshwater pearl mussel (Margaritifera margaritifera L.) streams. Aquat Conserv Mar Freshwat Ecosyst 16:251–266. https://doi.org/10.1002/aqc.721
Geist J, Rottmann O, Schroder W, Kuehn R (2003) Development of microsatellite markers for the endangered freshwater pearl mussel Margaritifera margaritifera L. (Bivalvia: Unionoidea). Mol Ecol 3:444–446. https://doi.org/10.1046/j.1471-8286.2003.00476.x
Geist J, Wunderlich H, Kuehn R (2008) Use of mollusc shells for DNA-based molecular analyses. J Molluscan Stud 74:337–343. https://doi.org/10.1093/mollus/eyn025
Gustafsson L, Nordling D, Andersson MS, Sheldon BC, Qvarnström A (1994) Infectious-diseases, reproductive effort and the cost of reproduction in birds. Philos Trans: Biological Sciences 346:323–331. https://doi.org/10.1098/rstb.1994.0149
Haag WR (2012) North American freshwater mussels: natural history, ecology, and conservation. Cambridge, UK: Cambridge University Press
Hastie LC, Young MR (2001) Freshwater pearl mussel (Margaritifera margaritifera) glochidiosis in wild and farmed salmonid stocks in Scotland. Hydrobiologia 445:109–119. https://doi.org/10.1023/A:1017588222480
Hämäläinen A, Raharivololona B, Ravoniarimbinina P, Kraus C (2015) Host sex and age influence endoparasite burdens in the gray mouse lemur. Front Zool 12:1–14. https://doi.org/10.1186/s12983-015-0118-9
Horky P, Douda K, Maciak M, Zavorka L, Slavik O (2014) Parasite-induced alterations of host behaviour in a riverine fish: the effects of glochidia on host disperal. Freshw Biol 59:1452–1461. https://doi.org/10.1111/fwb.12357
Ieshko EP, Geist J, Murzina SA, Veselov AE, Lebedeva DI, Ziuganov VV (2016) The characteristics of the infection of juvenile Atlantic salmon with glochidia of the freshwater pearl mussel in rivers of Northwest Russia. Knowl Manag Aquat Ecosyst 417:1–10. https://doi.org/10.1051/kmae/2015039
Ilmonen P, Taarna T, Hasselquis D (2000) Experimentally activated immune defence in female pied flycatchers results in reduced breeding success. Proc R Soc Lond B Biol Sci 267:665–670. https://doi.org/10.1098/rspb.2000.1053
Izhar R, Ben-Ami F (2015) Host age modulates parasite infectivity, virulence and reproduction. J Anim Ecol 84:1018–1028. https://doi.org/10.1111/1365-2656.12352
Jackson JA, Hall AJ, Friberg IM, Ralli C, Lowe A, Zawadzka M, Turner AK, Stewart A, Birtles RJ, Paterson S, Bradley JE, Begon M (2014) An immunological marker of tolerance to infection in wild rodents. PLoS Biol 12:1–13. https://doi.org/10.1371/journal.pbio.1001901
Jacot A, Scheuber H, Brinkhof MWG (2004) Costs of an induced immune response on sexual display and longevity in field crickets. Evolution 58:2280–2286. https://doi.org/10.1111/j.0014-3820.2004.tb01603.x
Karlsson S, Larsen BM, Hindar K (2014) Host-dependent genetic variation in freshwater pearl mussel (Margaritifera margaritifera L.). Hydrobiologia 735:179–190. https://doi.org/10.1007/s10750-013-1679-2
Karna D, Millemann RE (1978) Glochidiosis of salmonid fishes. III. Comparative susceptibility to natural infection with Margaritifera margaritifera (Pelecypoda: Magaritanidae) and associated histopathology. J Parasitol 64:528–537. https://doi.org/10.2307/3279799
Kat PW (1984) Parasitism and the Unionacea (Bivalvia). Biol Rev 59:189–207. https://doi.org/10.1111/j.1469-185X.1984.tb00407.x
Klemme I, Karvonen A (2016) Vertebrate defence against parasites: interactions between avoidance, resistance and tolerance. Ecology and Evolution 7:561–571. https://doi.org/10.1002/ece3.2645
Kutzer MAM, Armitage SAO (2016) Maximising fitness in the face of parasites: a review of host tolerance. Zoology 119:281–289. https://doi.org/10.1016/j.zool.2016.05.011
Lagrue C, Kelly DW, Hicks A, Poulin R (2011) Factors influencing infection patterns of trophically transmitted parasites among a fish community: host diet, host-parasite compatibility or both? J Fish Biol 79:466–485. https://doi.org/10.1111/j.1095-8649.2011.03041.x
Lambrechts L, Halbert J, Durand P, Gouagna LC, Koella JC (2005) Host genotype by parasite genotype interactions underlying the resistance of anopheline mosquitoes to Plasmodium falciparum. Malar J 4:1–8. https://doi.org/10.1186/1475-2875-4-3
Larsen BM (2005) Handlingsplan for elvemusling Margaritifera margaritifera i Norge. Innspill til den faglige delen av handlingsplanen. NINA Rapport 122
Lefèvre T, Roche B, Poulin R, Renaud F, Thomas F (2008) Exploiting host compensatory responses: the ‘must’ of manipulation? Trends Parasitol 24:435–439. https://doi.org/10.1016/j.pt.2008.06.006
Loot G, Poulin R, Lek S, Guegan JF (2002) The differential effects of Ligula intestinalis (L.) plerocercoids on host growth in three natural populations of roach, Rutilus rutilus (L.). Ecol Freshw Fish 11:168–177. https://doi.org/10.1034/j.1600-0633.2002.00006.x
Lopes-Lima M, Sousa R, Geist J, Aldridge DC, Araujo R, Bergengren J, Bespalaya Y, Bódis E, Burlakova L, Van Damme D, Douda K, Froufe E, Georgiev D, Gumpinger C, Karatayev A, Kebapçi Ü, Killeen I, Lajtner J, Larsen BM, Lauceri R, Legakis A, Lois S, Lundberg S, Moorkens E, Motte G, Nagel KO, Ondina P, Outeiro A, Paunovic M, Prié V, von Proschwitz T, Riccardi N, Rudzitis M, Scheder C, Seddon M, Sereflisan H, Simic V, Sokolova S, Stoeckl K, Taskinen J, Teixeira A, Thielen F, Trichkova T, Varandas S, Vicentini H, Zajac K, Zajac T, Zogaris S (2017) Conservation status of freshwater mussels in Europe: state of the art and future challenges. Biol Rev 92:572–607. https://doi.org/10.1111/brv.12244
Machordom A, Araujo R, Erpenbeck D, Ramos MA (2003) Phylogeography and conservation genetics of endangered European Margaritiferidae (Bivalvia: Unionoidea). Biol J Linn Soc 78:235–252. https://doi.org/10.1046/j.1095-8312.2003.00158.x
Martin LB II, Scheuerlein A, Wikelski M (2003) Immune activity elevates energy expenditure of house sparrows: a link between direct and indirect costs? Proc R Soc Lond B Biol Sci 270:153–158. https://doi.org/10.1098/rspb.2002.2185
Marwaha J, Jensen KH, Jakobsen JJ, Geist J (2017) Duration of the parasitic phase determines subsequent performance in juvenile freshwater pearl mussels (Margaritifera margaritifera). Ecol Evolution 7:1375–1383. https://doi.org/10.1002/ece3.2740
Meyers TR, Milleman RE (1977) Glochidiosis of salmonid fishes. I. Comparative susceptibility to experimental infection with Margaritifera margaritifera (L.)(Pelecypoda: Margaritanidae). J Parasitol 63:728–733. https://doi.org/10.2307/3279583
Meyers TR, Milleman RE, Fustish CA (1980) Glochidiosis of salmonio fishes. IV. Humoral and tissue responses of Coho and Chinook salmon to experimental infection with Margaritifera margaritifera (L.) (Pelecypoda: Margaritanidae). J Parasitol 66:274–281. https://doi.org/10.2307/3280818
Milinski M (1985) Risk of predation of parasitized sticklebacks (Gasterosteus aculeatus L.) under competition for food. Behaviour 93:203–216 https://www.jstor.org/stable/4534442. Accessed 10 Jan 2019
Mollusc Specialist Group (1996) Margaritifera margaritifera. The IUCN Red List of Threatened Species 1996: e. T12799A3382532.en
Moreno J, Sanz JJ, Arriero E (1999) Reproductive effort and T-lymphocyte cell-mediated immunocompetence in female pied flycatchers Ficedula hypoleuca. Proc R Soc Lond B Biol Sci 266:1105–1109. https://doi.org/10.1098/rspb.1999.0750
Morton A, Routledge RD (2006) Fulton’s condition factor: is it a valid measure of sea lice impact on juvenile salmon? N Am J Fish Manag 26:56–62. https://doi.org/10.1577/M05-068.1
Museth J (2001) Effects of Ligula intestinalis on habitat use, predation risk and catchability in European minnows. J Fish Biol 59:1070–1080. https://doi.org/10.1111/j.1095-8649.2001.tb00172.x
Nezlin LP, Cunjak RA, Zotin AA, Ziuganov VV (1994) Glochidium morphology of the freshwater pearl mussel (Margaritifera margaritifera) and glochidiosis of Atlantic salmon (Salmo salar): a study by scanning electron microscopy. Can J Zool 72:15–21. https://doi.org/10.1139/z94-003
Nordling D, Andersson M, Zohari S, Gustafsson L (1998) Reproductive effort reduces specific immune response and parasite resistance. Proc R Soc B Biol Sci 265:1291–1298. https://doi.org/10.1098/rspb.1998.0432
Norris K, Evans MR (2000) Ecological immunology: life history trade-offs and immune defence in birds. Behav Ecol 11:19–26. https://doi.org/10.1093/beheco/11.1.19
O’Connell MT, Neves RJ (1999) Evidence of immunological responses by a host fish (Ambloplites rupestris) and two non-host fishes (Cyprinus carpio and Carassius auratus) to glochidia of a freshwater mussel (Villosa iris). J Freshw Ecol 14:71–78. https://doi.org/10.1080/02705060.1999.9663656
Ondracková M, Reichard M, Jurajda P, Gelnar M (2004) Seasonal dynamics of Posthodiplostomum cuticola (Digenea, Diplostomatidae) metacercariae and parasite-enhanced growth of juvenile host fish. Parasitol Res 93:131–136. https://doi.org/10.1007/s00436-004-1123-7
Österling ME, Larson BJ (2013) Impact of origin and condition of host fish (Salmo trutta) on parasitic larvae of Margaritifera margaritifera. Aquat Conserv Mar Freshwat Ecosyst 23:564–570. https://doi.org/10.1002/aqc.2320
Österling EM, Wengström N (2015) Test of the host fish species of a unionoid mussel: a comparison between natural and artificial encystment. Limnologica 50:80–83. https://doi.org/10.1016/j.limno.2014.11.005
Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295. https://doi.org/10.1111/j.1471-8286.2005.01155.x
Råberg L (2014) How to live with the enemy: understanding tolerance to parasites. PLoS Biol 12:1–4. https://doi.org/10.1371/journal.pbio.1001989
Råberg L, Graham AL, Read AF (2009) Decomposing health: tolerance and resistance to parasites in animals. Philos Trans R Soc B 364:37–49. https://doi.org/10.1098/rstb.2008.0184
Raymond M, Rousset F (1995) Genepop (version-1.2) population genetics software for exact tests and ecumenicism. J Hered 86:248–249. https://doi.org/10.1093/oxfordjournals.jhered.a111573
Rousset F (2008) GENEPOP’007: a complete re-implementation of the GENEPOP software for Windows and Linux. Mol Ecol Resour 8:103–106. https://doi.org/10.1111/j.1471-8286.2007.01931.x
Rogers-Lowery CL, Dimock RV Jr (2006) Encapsulation of attached ectoparasitic glochidia larvae of freshwater mussels by epithelial tissue on fins of naive and resistant host fish. Biol Bull 210:51–63. https://doi.org/10.2307/4134536
Rogers-Lowery CL, Dimock RV Jr, Kuhn RE (2007) Antibody response of bluegill sunfish during development of acquired resistance against the larvae of the freshwater mussel Utterbackia imbecillis. Dev Comp Immunol 31:143–155. https://doi.org/10.1016/j.dci.2006.05.011
Poulin R (1993) Age-dependent effects of parasites on anti-predator responses in two New Zealand freshwater fish. Oecologia 96:431–438. https://doi.org/10.1007/BF00317516
Salonen JK, Marjomäki TM, Taskinen J (2016) An alien fish threatens an endangered parasitic bivalve: the relationship between brook trout (Salvelinus fontinalis) and freshwater pearl mussel (Margaritifera margaritifera) in northern Europe. Aquat Conserv Mar Freshwat Ecosyst 26:1130–1144. https://doi.org/10.1002/aqc.2614
Salonen JK, Luhta PL, Moilanen E, Oulasvirta P, Turunen J, Taskinen J (2017) Atlantic salmon (Salmo salar) and brown trout (Salmo trutta) differ in their suitability as hosts for the endangered freshwater pearl mussel (Margaritifera margaritifera) in northern Fennoscandian rivers. Freshw Biol 62:1346–1358. https://doi.org/10.1111/fwb.12947
Sandland GJ, Minchella DJ (2003) Costs of immune defense: an enigma wrapped in an environmental cloak? Trends Parasitol 19:571–574. https://doi.org/10.1016/j.pt.2003.10.006
Schmid-Hempel P (2011) Evolutionary parasitology: the integrated study of infections, immunology, ecology, and genetics. Oxford University Press, Oxford
Sheldon BC, Verhulst S (1996) Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol Evol 11:317–321. https://doi.org/10.1016/0169-5347(96)10039-2
Simkova A, Lafond T, Ondracková M, Jurajda P, Ottová E, Morand S (2008) Parasitism, life history traits and immune defence in cyprinid fish from Central Europe. BMC Evol Biol 8:1–11. https://doi.org/10.1186/1471-2148-8-29
Siva-Jothy MT, Tsubaki Y, Hooper RE (1998) Decreased immune response as a proximate cost of copulation and oviposition in a damselfly. Physiol Entomol 23:274–277. https://doi.org/10.1046/j.1365-3032.1998.233090.x
Soler JJ, de Neve L, Perez-Contreras T, Soler M, Sorci G (2003) Trade-off between immunocompetence and growth in magpies: an experimental study. Proc R Soc Lond B Biol Sci 270:241–248. https://doi.org/10.1098/rspb.2002.2217
Strayer DL, Downing JA, Haag WR, King TL, Layzer JB, Newton TJ, Nichols JS (2004) Changing perspectives on pearly mussels. North America’s most imperiled animals. BioScience 54:429–439. https://doi.org/10.1641/0006-3568(2004)054[0429:CPOPMN]2.0.CO;2
Taeubert JE (2014) Host-parasite interactions in aquatic ecosystems—the relationship between fishes and endangered freshwater mussels. Ph.D thesis, Technischen Universität München
Taeubert JE, Geist J (2013) Critical swimming speed of brown trout (Salmo trutta) infested with freshwater pearl mussel (Margaritifera margaritifera) glochidia and implications for artificial breeding of an endangered mussel species. Parasitol Res 112:1607–1613. https://doi.org/10.1007/s00436-013-3314-6
Taeubert JE, Geist J (2017) The relationship between the freshwater pearl mussel (Margaritifera margaritifera) and its hosts. Biol Bull 44:67–73. https://doi.org/10.1134/S1062359017010149
Taeubert JE, Denic M, Gum B, Lange M, Geist J (2010) Suitability of different salmonid strains as hosts for the endangered freshwater pearl mussel (Margaritifera margaritifera). Aquat Conserv Mar Freshwat Ecosyst 20:728–734. https://doi.org/10.1002/aqc.1147
Taeubert JE, Gum B, Geist J (2013) Variable development and excystment of freshwater pearl mussel (Margaritifera margaritifera L.) at constant temperature. Limnologica 43:319–322. https://doi.org/10.1016/j.limno.2013.01.002
Taylor LH, Matthews L, Shaw DJ, Haydon DT (2005) Competitive suppression in mixed-clone parasite cultures. Biol Lett 1:108–111. https://doi.org/10.1098/rsbl.2004.0256
Thomas F, Guégan J-F, Michalakis Y, Renaud F (2000) Parasites and host life-history traits: implications for community ecology and species co-existence. Int J Parasitol 30:669–674. https://doi.org/10.1016/S0020-7519(00)00040-0.
Thomas GR, Taylor J, Garcia de Leaniz C (2014) Does the parasitic freshwater pearl mussel M. margaritifera harm its host? Hydrobiologia 735:191–201. https://doi.org/10.1007/s10750-013-1515-8
Thomas GR (2011) Conservation ecology of the endangered Freshwater Pearl Mussel, Margaritifera margaritifera. Ph.D. thesis, University of Swansea, Wales
Treasurer JW, Turnbull T (2000) The pathology and seawater performance of farmed Atlantic salmon infected with glochidia of Margaritifera margaritifera. J Fish Biol 57:858–866. https://doi.org/10.1111/j.1095-8649.2000.tb02197.x
Treasurer JW, Hastie LC, Hunter D, Duncan F, Treasurer CM (2006) Effects of (Margaritifera margaritifera) glochidial infection on performance of tank-reared Atlantic salmon (Salmo salar). Aquaculture 256:74–79. https://doi.org/10.1016/j.aquaculture.2006.02.031
Tschirren B, Richner H (2006) Parasites shape the optimal investment in immunity. Proc R Soc Lond B Biol Sci 273:1773–1777. https://doi.org/10.1098/rspb.2006.3524
van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538. https://doi.org/10.1111/j.1471-8286.2004.00684.x
Veiga JP, Salvador A, Merino S, Puerta M (1998) Reproductive effort affects immune response and parasite infection in a lizard: a phenotypic manipulation using testosterone. Oikos 82:313–318. https://doi.org/10.2307/3546971
Wächtler K, Dreher-Mansur MC, Richter T (2001) Larval types and early postlarval biology in naiads (Unionoida). In: Bauer G, Wächtler K (eds) Ecology and evolution of the freshwater mussels unionoida, vol 145. Springer-Verlag, The Series Ecological Studies Berlin, Germany, pp 93–126
Watters GH, O’Dee SH (1999) Glochidia of the freshwater mussel Lampsilis overwintering on fish hosts. J Molluscan Stud 65:453–459. https://doi.org/10.1093/mollus/65.4.453
Wilson K, Bjørnstad ON, Dobson AP, Merler S, Poglayen G, Randolph SE, Read AF, Skorping A (2002) Heterogeneities in macroparasite infections: patterns and processes. In: Hudson PJ, Rizzioli A, Grenfell BT, Heesterbeek H, Dobson AP (eds) Ecology of wildlife diseases. Oxford University Press, Oxford, pp 6–44
Young M, Purser GJ, Al-Mousawi B (1987) Infection and successful reinfection of brown trout (Salmo trutta L) with glochidia of Margaritifera margaritifera (L). Am Malacol Bull 5:125–128
Young M, Williams J (1984) The reproductive biology of the freshwater pearl mussel Margaritifera margaritifera (Linn.) in Scotland. I. Field studies. Arch Hydrobiol 99:405–422
Ziuganov VV, Zotin A, Nezlin L, Tretiakov V (1994) The freshwater pearl mussels and their relationships with salmonid fish. VNIRO Publishing House, Moscow, Russia
Acknowledgements
We would like to thank the staff at the Laboratory of Unit of Molecular Zoology, Technische Universität München and also the staff at the mussel rearing facility in Austevoll for all their help.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflicts of interest
The authors declare that there is no conflict of interest.
Additional information
Section Editor: Stephen A. Bullard
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Marwaha, J., Aase, H., Geist, J. et al. Host (Salmo trutta) age influences resistance to infestation by freshwater pearl mussel (Margaritifera margaritifera) glochidia. Parasitol Res 118, 1519–1532 (2019). https://doi.org/10.1007/s00436-019-06300-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-019-06300-2