The costs and benefits in an unusual symbiosis: Experimental evidence that bitterling fish (Rhodeus sericeus) are parasites of unionid mussels in Europe

Journal of Evolutionary Biology

Volumn 19, Issue 3, 2006, Pages 788-796

  Reichard, M ^a,b   Ondrackova M ^a   Przybylski, M ^c   Liu, H ^d   Smith, C ^b  

^a INSTITUTE OF VERTEBRATE BIOLOGY   (Czech Republic)

^b UNIVERSITY OF LEICESTER   (United Kingdom)

^c UNIVERSITY OF LODZ   (Poland)

^d INSTITUTE OF HYDROBIOLOGY   (China)

Author keywords

Brood parasitism; Coevolution; Fitness; Glochidia; Growth; Mutualism; Oviposition; Symbiosis; Unionidae

Indexed keywords

FRESH WATER;

BROOD PARASITISM; COEVOLUTION; COST-BENEFIT ANALYSIS; FISH; MUTUALISM; OVIPOSITION; PARASITE;

ANIMAL; ARTICLE; BIVALVE; CYPRINIFORMES; EGG LAYING; EUROPE; FEMALE; GROWTH, DEVELOPMENT AND AGING; HOST PARASITE INTERACTION; LARVA; PARASITOLOGY; PATHOGENICITY; PHYSIOLOGY; SYMBIOSIS;

ANIMALS; BIVALVIA; CYPRINIDAE; EUROPE; FEMALE; FRESH WATER; HOST-PARASITE RELATIONS; LARVA; OVIPOSITION; SYMBIOSIS;

ASIA; EURASIA; EUROPE;

PISCES; RHODEUS; RHODEUS SERICEUS; UNIONIDAE;

EID: 33646482453     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/j.1420-9101.2005.01051.x     Document Type: Article

References (40)

1. Arai R. 1988. Fish systematic and cladistics. In: Ichthyology Currents 1988 Uyeno T. Okiyama M. eds pp. 4 33. Asakura Shoten.
2. Bauer G. 1994. The adaptive value of offspring size among freshwater mussels (Bivalvia; Unioidea). J. Anim. Ecol. 63 933 944.
3. Bauer G. Wächtler K. 2000. Ecology and Evolution of the Freshwater Mussels Unionoida. Springer-Verlag Berlin.
4. Bogutskaya N.G. Komlev A.M. 2001. Some new data to morphology of Rhodeus sericeus (Cyprinidae: Acheilognathinae) and a description of a new species, Rhodeus colchicus, from west Transcaucasia. Proc. Zool. Inst. 287 81 97.
5. Briskie J.V. Sealy S.G. Hobson K.A. 1992. Behavioral defenses against avian brood parasitism in sympatric and allopatric host populations. Evolution 46 334 340.
6. Bronstein J.L. 2001. The costs of mutualism. Am. Zool. 41 825 839.
7. Bush A.O. Lafferty K.D. Lotz J.M. Schostak A.W. 1997. Parasitology meets ecology on its own terms: Margolis et al. revisited. J. Parasitol. 83 575 583.
8. Cohen J. 1988. Statistical Power Analysis for the Behavioral Sciences. Erlbaum Hillsdale.
9. Compton S.G. Wiebes J.T. Berg C.C. 1996. The biology of fig trees and their associated animals. J. Biogeogr. 23 405 407.
10. Cruz A. Post W. Wiley J.W. Ortega C.P. Nakamura T.K. Prather J.W. 1998. Potential impacts of cowbird range expansion in Florida. In: Parasitic Birds and Their Hosts. Studies in Coevolution Rothstein S. I. Robinson S. K. eds pp. 313 336. Oxford University Press Oxford.
11. Dudgeon D. Morton B. 1984. Site selection and attachment duration of Anodonta woodiana (Bivalvia, Unionacea) glochidia on fish hosts. J. Zool. 204 355 362.
12. Fukuhara S. Nagata Y. Yamada T. 1986. Glochidium parasitic period, host-fish and parasitic site of Anodonta woodiana in small pond. Jpn. J. Malacol. 45 43 52.
13. Guan T.L. Afzelius B.A. 1991. The spermatozoon of the Chinese bitterling, Rhodeus sericeus sinensis (Cyprinidae, Teleostei). J. Submicrosc. Cytol. Pathol. 23 351 356.
14. Hirai K. 1965. Comparative studies on ecology of four species of bitterlings in the Lake Biwa. Physiol. Ecol. Jpn. 12 72 81.
15. Holland J.N. DeAngelis D.L. Schultz S.T. 2004. Evolutionary stability of mutualism: interspecific population regulation as an evolutionary stable strategy. Proc. R. Soc. Lond. B 271 1807 1814.
16. Holčík J. 1978. On the expansion and origin of Carassius auratus in Czechoslovakia. Folia Zool. 27 279 288.
17. Holčík J. 1999. Rhodeus sericeus. In: The Freshwater Fishes of Europe, 5/I Cyprinidae Banarescu P. M. ed. pp. 1 32. AULA-Verlag Wiebelsheim.
18. Hosoi S.A. Rothstein S.I. 2000. Nest desertion and cowbird parasitism: evidence for evolved responses and evolutionary lag. Anim. Behav. 59 823 840.
19. Kadlec D. Šimková A. Jarkovský J. Gelnar M. 2003. Parasite communities of freshwater fish under flood conditions. Parasitol. Res. 89 272 283.
20. Kitamura J. 2005. Factors affecting seasonal mortality of rosy bitterling (Rhodeus ocellatus kurumeus) embryos on the gills of their host mussel. Popul. Ecol. 47 41 51.
21. Kottelat M. 1997. European freshwater fishes. Biológia 52 Suppl. 5 1 271.
22. Kryzhanovsky S.G. 1949. Ecological and morphological features of the development of cyprinid, cobitid and silurid fishes (Cyprinoidei and Silurodei). Tr. Inst. Morfol. Zhivotn. 1 58 332.
23. Mills S.C. Reynolds D.C. 2002. Mussel ventilation rates as approximate cue for host selection by bitterling, Rhodeus sericeus. Oecologia 131 473 478.
24. Mills S.C. Reynolds J.D. 2003. The bitterling-mussel interaction as a test case for co-evolution. J. Fish Biol. 63 S84 S104.
25. Myers T.R. Millemann R.E. 1977. Glochidiosis of salmonid fishes. I. Comparative susceptibility to experimental infection with Margaritifera margaritifera (L.) (Pelycypoda: Margaritanidae). J. Parasitol. 63 728 733.
26. Nagata Y. 1985. The effect of social organization of the bitterling, Rhodeus ocellatus (Kner) and the condition of a bivalve, Anodonta woodiana Lea in a small pond on the number of fish eggs being laid in a bivalve. Mem. Osaka Kyoiku Univ. 34 9 26.
27. Paracer S. Ahmadjian V. 2000. Symbiosis. Oxford University Press Oxford.
28. Reichard M. Jurajda P. Smith C. 2004a. Male-male interference competition decreases spawning rate in the European bitterling (Rhodeus sericeus). Behav. Ecol. Sociobiol. 56 34 41.
29. Reichard M. Smith C. Jordan W.C. 2004b. Genetic evidence reveals density-dependent mediated success of alternative mating tactics in the European bitterling (Rhodeus sericeus). Mol. Ecol. 13 1569 1578.
30. Rothstein S.I. Robinson S.K. 1998. The evolution and ecology of avian brood parasitism: an overview. In: Parasitic Birds and Their Hosts. Studies in Coevolution Rothstein S. I. Robinson S. K. eds pp. 3 56. Oxford University Press Oxford.
31. Smith C. Reichard M. Jurajda P. 2003. Assessment of sperm competition by bitterling, Rhodeus sericeus. Behav. Ecol. Sociobiol. 53 206 213.
32. Smith C. Reichard M. Jurajda P. Przybylski M. 2004. The reproductive ecology of the European bitterling (Rhodeus sericeus). J. Zool. 262 107 124.
33. Smith C. Reynolds J.D. Sutherland W.J. Jurajda P. 2000. Adaptive host choice and avoidance of superparasitism in the spawning decisions of bitterling (Rhodeus sericeus). Behav. Ecol. Sociobiol. 48 29 35.
34. Smith C. Rippon K. Douglas A. Jurajda P. 2001. A proximate cue for oviposition site choice in the bitterling (Rhodeus sericeus). Freshw. Biol. 46 903 911.
35. Tillberg C.V. 2004. Friend or foe? A behavioral and stable isotopic investigation of an ant-plant symbiosis. Oecologia 140 506 515.
36. Thompson J.N. 1994. The Coevolutionary Process. University of Chicago Press Chicago.
37. Thompson J.N. Cunningham B.C. 2002. Geographic structure and dynamics of coevolutionary selection. Nature 417 735 738.
38. Trail P.W. Baptista L.F. 1993. The impact of brown-headed cowbird parasitism on populations of the Nuthall's white-crowned sparrow. Conserv. Biol. 7 309 315.
39. Waters G.T. 1997. A synthesis and review of the expanding range of the Asian freshwater mussel Anodonta woodiana (Bivalvia: Unionidae). Veliger 40 152 156.
40. Wheeler A. 1978. Key to the Fishes of Northern Europe. Warne London.