Oecologia

, Volume 170, Issue 1, pp 199–207 | Cite as

The fine line between mutualism and parasitism: complex effects in a cleaning symbiosis demonstrated by multiple field experiments

  • Bryan L. Brown
  • Robert P. Creed
  • James Skelton
  • Mark A. Rollins
  • Kaitlin J. Farrell
Community ecology - Original research

Abstract

Ecological theory and observational evidence suggest that symbiotic interactions such as cleaning symbioses can shift from mutualism to parasitism. However, field experimental evidence documenting these shifts has never been reported for a cleaning symbiosis. Here, we demonstrate shifts in a freshwater cleaning symbiosis in a system involving crayfish and branchiobdellid annelids. Branchiobdellids have been shown to benefit their hosts under some conditions by cleaning material from host crayfish’s gill filaments. The system is uniquely suited as an experimental model for symbiosis due to ease of manipulation and ubiquity of the organisms. In three field experiments, we manipulated densities of worms on host crayfish and measured host growth in field enclosures. In all cases, the experiments revealed shifts from mutualism to parasitism: host crayfish growth was highest at intermediate densities of branchiobdellid symbionts, while high symbiont densities led to growth that was lower or not significantly different from 0-worm controls. Growth responses were consistent even though the three experiments involved different crayfish and worm species and were performed at different locations. Results also closely conformed to a previous laboratory experiment using the same system. The mechanism for these shifts appears to be that branchiobdellids switched from cleaning host gills at intermediate densities of worms to consuming host gill tissue at high densities. These outcomes clearly demonstrate shifts along a symbiosis continuum with the maximum benefits to the host at intermediate symbiont densities. At high symbiont densities, benefits to the host disappear, and there is some evidence for a weak parasitism. These are the first field experimental results to demonstrate such shifts in a cleaning symbiosis.

Keywords

Symbiosis Mutualism Parasitism Context dependence Cleaning behavior 

References

  1. Bauer RT (1998) Gill-cleaning mechanisms of the crayfish Procambarus clarkii (astacidea: cambaridae): experimental testing of setobranch function. Invertebr Biol 117:129–143CrossRefGoogle Scholar
  2. Bishop JE (1968) An ecological study of the branchiobdellid commensals of some mid-western Ontario crayfish. Can J Zool 46:835–843CrossRefGoogle Scholar
  3. Brown BL, Creed RP (2004) Host preference by an aquatic ectosymbiotic annelid on 2 sympatric species of host crayfishes. J North Am Benthol Soc 23:90–100CrossRefGoogle Scholar
  4. Brown BL, Creed RP, Dobson WE (2002) Branchiobdellid annelids and their crayfish hosts: are they engaged in a cleaning symbiosis? Oecologia 132:250–255CrossRefGoogle Scholar
  5. Bshary R, Grutter AS, Willener AST, Leimar O (2008) Pairs of cooperating cleaner fish provide better service quality than singletons. Nature 455:964–966PubMedCrossRefGoogle Scholar
  6. Cheney KL, Côté IM (2003) The ultimate effect of being cleaned: does ectoparasite removal have reproductive consequences for damselfish clients? Behav Ecol 14:892–896CrossRefGoogle Scholar
  7. Cheney KL, Côté IM (2005) Mutualism or parasitism? The variable outcome of cleaning symbioses. Biol Lett 1:162–165PubMedCrossRefGoogle Scholar
  8. Côté IM (2000) Evolution and ecology of cleaning symbioses in the sea. Oceanogr Mar Biol Annu Rev 38:311–355Google Scholar
  9. Ewald PW (1987) Transmission modes and evolution of the parasitism–mutualism continuum. Ann NY Acad Sci 503:295–306PubMedCrossRefGoogle Scholar
  10. Gale KSP, Proctor HC (2011) Diets of two congeneric species of crayfish worm (annelida:clitellata:branchiobdellidae) from western Canada. Can J Zool 89:289–296CrossRefGoogle Scholar
  11. Gelder SR (1999) Zoogeography of branchiobdellidans (annelida) and temnocephalidans (platyhelminthes) ectosymbiotic on freshwater crustaceans, and their reactions to one another in vitro. Hydrobiologia 406:21–31CrossRefGoogle Scholar
  12. Goodnight CJ (1940) The branchiobdellidae of North American crayfishes. Ill Biol Monogr 17:5–75Google Scholar
  13. Grutter AS, Bshary R (2003) Cleaner wrasse prefer client mucus: support for partner control mechanisms in cleaning interactions. Proc R Soc Lond B 270:S242–S244CrossRefGoogle Scholar
  14. Holt PC (1973a) A free-living branchiobdellid (annelida: clitellata)? Trans Am Micros Soc 92:152–153CrossRefGoogle Scholar
  15. Holt PC (1973b) A summary of the branchiobdellid (annelida: clitellata) fauna of Mesoamerica. Smithson Contrib Zool 142:1–40CrossRefGoogle Scholar
  16. Jennings JB, Gelder SR (1979) Gut structure, feeding and digestion in the branchiobdellid oligochaete Cambarincola macrodonta Ellis 1912, an ectosymbiote of the freshwater crayfish Procambarus clarkii. Biol Bull 156:300–314CrossRefGoogle Scholar
  17. Lee J, Kim T, Choe J (2009) Commensalism or mutualism: conditional outcomes in a branchiobdellid–crayfish symbiosis. Oecologia 159:217–224PubMedCrossRefGoogle Scholar
  18. Limbaugh C (1961) Cleaning symbiosis. Sci Am 205:42–49CrossRefGoogle Scholar
  19. Losey GS (1979) Fish cleaning symbiosis: proximate causes of host behavior. Anim Behav 27:669–685CrossRefGoogle Scholar
  20. McManus LR (1960) Some ecological studies of the branchiobdellidae. Trans Am Microsc Soc 79:420–428CrossRefGoogle Scholar
  21. Pellmyr O, Huth CJ (1994) Evolutionary stability of mutualism between yuccas and yucca moths. Nature 372:257–260CrossRefGoogle Scholar
  22. Poulin R, Grutter AS (1996) Cleaning symbioses: proximate and adaptive explanations. Bioscience 46:512–517CrossRefGoogle Scholar
  23. Quaglio F et al (2006) Preliminary investigations of disease-causing organisms in the white-clawed crayfish Austropotamobius pallipes complex from streams of northern Italy. Bull Fr Pêche Piscic 380–381:1271–1290Google Scholar
  24. R Development Core Team (2011) R: A language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  25. Woodhead AE (1950) Life history cycle of the giant kidney worm, Dioctophyma renale (nematoda), of man and many other mammals. Trans Am Microsc Soc 69:21–46CrossRefGoogle Scholar
  26. Young W (1966) Ecological studies of the branchiobdellidae (oligochaeta). Ecology 47:571–578CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Bryan L. Brown
    • 1
    • 3
  • Robert P. Creed
    • 2
  • James Skelton
    • 1
    • 3
  • Mark A. Rollins
    • 2
  • Kaitlin J. Farrell
    • 2
  1. 1.Department of Forestry and Natural ResourcesClemson UniversityClemsonUSA
  2. 2.Department of BiologyAppalachian State UniversityBooneUSA
  3. 3.Department of Biological SciencesVirginia TechBlacksburgUSA

Personalised recommendations