Conspecific alarm cues affect interspecific aggression in cichlid fishes

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• 作者：Denis Meuthen ; Sebastian A. Baldauf ; Theo C. M. Bakker ; Timo Thünken
• 关键词：Pelvicachromis taeniatus ; Pelvicachromis kribensis ; Alarm cues ; Interspecific aggression ; Interspecific competition ; Predation risk
• 刊名：Hydrobiologia
• 出版年：2016
• 出版时间：March 2016
• 年：2016
• 卷：767
• 期：1
• 页码：37-49
• 全文大小：633 KB
• 参考文献：Adler, F. R. & C. D. Harvell, 1990. Inducible defenses, phenotypic variability and biotic environments. Trends in Ecology and Evolution 5: 407–410.PubMed CrossRef
  Amarasekare, P., 2002. Interference competition and species coexistence. Proceedings of the Royal Society B 269: 2541–2550.PubMedCentral PubMed CrossRef
  Baldauf, S. A., H. Kullmann, S. H. Schroth, T. Thünken & T. C. M. Bakker, 2009. You can’t always get what you want: size assortative mating by mutual mate choice as a resolution of sexual conflict. BMC Evolutionary Biology 9: 129.PubMedCentral PubMed CrossRef
  Baldauf, S. A., T. C. M. Bakker, H. Kullmann & T. Thünken, 2011. Female nuptial coloration and its adaptive significance in a mutual mate choice system. Behavioral Ecology 22: 478–485.CrossRef
  Barlow, G. W., 2000. The Cichlid Fishes. Perseus Publishing, Cambridge.
  Barreto, R. E., A. Barbosa, A. C. C. Giassi & A. Hoffmann, 2010. The ‘club’ cell and behavioural and physiological responses to chemical alarm cues in the Nile tilapia. Marine and Freshwater Behaviour and Physiology 43: 75–81.CrossRef
  Barreto, R. E., C. A. Miyai, F. H. C. Sanches, P. C. Giaquinto, H. C. Delicio & G. L. Volpato, 2013. Blood cues induce antipredator behavior in Nile tilapia conspecifics. PLoS One 8: e54642.PubMedCentral PubMed CrossRef
  Begon, M., C. R. Townsend & J. L. Harper, 2005. Ecology: From Individuals to Ecosystems. Blackwell Science, Oxford.
  Bengtsson, J., 1989. Interspecific competition increases local extinction rate in a metapopulation system. Nature 340: 713–715.CrossRef
  Berejikian, B. A., R. J. F. Smith, E. P. Tezak, S. L. Schroder & C. M. Knudsen, 1999. Chemical alarm signals and complex hatchery rearing habitats affect antipredator behavior and survival of chinook salmon (Oncorhynchus tshawytscha) juveniles. Canadian Journal of Fisheries and Aquatic Sciences 56: 830–838.CrossRef
  Bierbach, D., M. Schulte, N. Herrmann, M. Tobler, S. Stadler, C. T. Jung, B. Kunkel, R. Riesch, S. Klaus, M. Ziege, J. R. Indy, L. Arias-Rodriguez & M. Plath, 2011. Predator-induced changes of female mating preferences: innate and experiential effects. BMC Evolutionary Biology 11: 190.PubMedCentral PubMed CrossRef
  Bjørnstad, O. N. & B. T. Grenfell, 2001. Noisy clockwork: time series analysis of population fluctuations in animals. Science 293: 638–643.PubMed CrossRef
  Bolnick, D. I., 2004. Can intraspecific competition drive disruptive selection? An experimental test in natural populations of sticklebacks. Evolution 58: 608–618.PubMed CrossRef
  Bourke, P., P. Magnan & M. A. Rodriguez, 1999. Phenotypic responses of lacustrine brook charr in relation to the intensity of interspecific competition. Evolutionary Ecology 13: 19–31.CrossRef
  Brick, O. & S. Jakobsson, 2002. Individual variation in risk taking: the effect of a predatory threat on fighting behavior in Nannacara anomala. Behavioral Ecology 13: 439–442.CrossRef
  Brönmark, C. & J. G. Miner, 1992. Predator-induced phenotypical change in body morphology in crucian carp. Science 258: 1348–1350.PubMed CrossRef
  Brown, G. E., 2003. Learning about danger: chemical alarm cues and local risk assessment in prey fishes. Fish and Fisheries 4: 227–234.CrossRef
  Brown, G. E., D. P. Chivers & R. J. F. Smith, 1995. Fathead minnows avoid conspecific and heterospecific alarm pheromones in the feces of northern pike. Journal of Fish Biology 47: 387–393.
  Brown, G. E., J. C. Adrian, T. Patton & D. P. Chivers, 2001. Fathead minnows learn to recognize predator odour when exposed to concentrations of artificial alarm pheromone below their behavioural-response threshold. Canadian Journal of Zoology 79: 2239–2245.CrossRef
  Brown, G. E., P. E. Foam, H. E. Cowell, P. G. Fiore & D. P. Chivers, 2004. Production of chemical alarm cues in convict cichlids: the effects of diet, body condition and ontogeny. Annales Zoologici Fennici 41: 487–499.
  Brown, G. E., M. A. Vavrek, C. K. Elvidge, R. DeCaire, B. Belland & C. D. Jackson, 2008. Disturbance cues in freshwater prey fishes: do juvenile convict cichlids and rainbow trout respond to ammonium as an ‘early warning’ signal? Chemoecology 18: 255–261.CrossRef
  Brown, G. E., C. D. Jackson, P. H. Malka, M. E. Jacques & M. A. Couturier, 2012. Disturbance cues in freshwater prey fishes: does urea function as an ‘early warning cue’ in juvenile convict cichlids and rainbow trout? Current Zoology 58: 250–259.
  Brown, G. E., M. C. O. Ferrari, C. K. Elvidge, I. Ramnarine & D. P. Chivers, 2013. Phenotypically plastic neophobia: a response to variable predation risk. Proceedings of the Royal Society B 280: 20122712.PubMedCentral PubMed CrossRef
  Brown, G. E., D. P. Chivers, C. K. Elvidge, C. D. Jackson & M. C. O. Ferrari, 2014. Background level of risk determines the intensity of predator neophobia in juvenile convict cichlids. Behavioral Ecology and Sociobiology 68: 127–133.CrossRef
  Bürger, R., K. A. Schneider & M. Willensdorfer, 2006. The conditions for speciation through intraspecific competition. Evolution 60: 2185–2206.PubMed CrossRef
  Chesson, P., 2000. Mechanisms of maintenance of species diversity. Annual Review of Ecology and Systematics 31: 343–366.CrossRef
  Chivers, D. P. & R. J. F. Smith, 1994a. Fathead minnows, Pimephales promelas, acquire predator recognition when alarm substance is associated with the sight of unfamiliar fish. Animal Behaviour 48: 597–605.CrossRef
  Chivers, D. P. & R. J. F. Smith, 1994b. The role of experience and chemical alarm signaling in predator recognition by fathead minnows, Pimephales promelas. Journal of Fish Biology 44: 273–285.CrossRef
  Chivers, D. P. & R. J. F. Smith, 1998. Chemical alarm signalling in aquatic predator–prey systems: a review and prospectus. Ecoscience 5: 338–352.
  Chivers, D. P., G. E. Brown & M. C. O. Ferrari, 2012. The evolution of alarm substances and disturbance cues in aquatic animals. In Brönmark, C. & L. A. Hansson (eds), Chemical Ecology in Aquatic Systems. Oxford University Press, Oxford.
  Chivers, D. P., M. I. McCormick, M. D. Mitchell, R. A. Ramasamy & M. C. O. Ferrari, 2014. Background level of risk determines how prey categorize predators and non-predators. Proceedings of the Royal Society B 281: 20140355.PubMedCentral PubMed CrossRef
  Clark, C. W. & C. D. Harvell, 1992. Inducible defenses and the allocation of resources—a minimal model. American Naturalist 139: 521–539.CrossRef
  Cramer, N. F. & R. M. May, 1972. Interspecific competition, predation and species diversity: a comment. Journal of Theoretical Biology 34: 289–293.PubMed CrossRef
  Crow, S. K., G. P. Closs, J. M. Waters, D. J. Booker & G. P. Wallis, 2010. Niche partitioning and the effect of interspecific competition on microhabitat use by two sympatric galaxiid stream fishes. Freshwater Biology 55: 967–982.CrossRef
  Dodson, S. I., T. A. Crowl, B. L. Peckarsky, L. B. Kats, A. P. Covich & J. M. Culp, 1994. Non-visual communication in freshwater benthos—an overview. Journal of the North American Benthological Society 13: 268–282.CrossRef
  Ferrari, M. C. O., B. D. Wisenden & D. P. Chivers, 2010. Chemical ecology of predator-prey interactions in aquatic ecosystems: a review and prospectus. Canadian Journal of Zoology 88: 698–724.CrossRef
  Foam, P. E., M. C. Harvey, R. S. Mirza & G. E. Brown, 2005. Heads up: juvenile convict cichlids switch to threat-sensitive foraging tactics based on chemosensory information. Animal Behaviour 70: 601–607.CrossRef
  Forsgren, E., 1992. Predation risk affects mate choice in a gobiid fish. American Naturalist 140: 1041–1049.CrossRef
  Genner, M. J., G. F. Turner & S. J. Hawkins, 1999. Resource control by territorial male cichlid fish in Lake Malawi. Journal of Animal Ecology 68: 522–529.CrossRef
  Ghedotti, M. J., 2000. Phylogenetic analysis and taxonomy of the poecilioid fishes (Teleostei: Cyprinodontiformes). Zoological Journal of the Linnean Society 130: 1–53.CrossRef
  Göz, H., 1941. Über den Art- und Individualgeruch bei Fischen. Zeitschrift für vergleichende Physiologie 29: 1–45.CrossRef
  Grether, G. F., N. Losin, C. N. Anderson & K. Okamoto, 2009. The role of interspecific interference competition in character displacement and the evolution of competitor recognition. Biological Reviews 84: 617–635.PubMed CrossRef
  Grether, G. F., C. N. Anderson, J. P. Drury, A. N. G. Kirschel, N. Losin, K. Okamoto & K. S. Peiman, 2013. The evolutionary consequences of interspecific aggression. Annals of the New York Academy of Sciences 1289: 48–68.PubMed CrossRef
  Hesse, S., T. C. M. Bakker, S. A. Baldauf & T. Thünken, 2012. Kin recognition by phenotype matching is family- rather than self-referential in juvenile cichlid fish. Animal Behaviour 84: 451–457.CrossRef
  Holmes, T. H. & M. I. McCormick, 2010. Smell, learn and live: the role of chemical alarm cues in predator learning during early life history in a marine fish. Behavioural Processes 83: 299–305.PubMed CrossRef
  Huisman, J. & F. J. Weissing, 1999. Biodiversity of plankton by species oscillations and chaos. Nature 402: 407–410.CrossRef
  Jackson, D. A., P. R. Peres-Neto & J. D. Olden, 2001. What controls who is where in freshwater fish communities—the roles of biotic, abiotic, and spatial factors. Canadian Journal of Fisheries and Aquatic Sciences 58: 157–170.
  Kats, L. B. & L. M. Dill, 1998. The scent of death: chemosensory assessment of predation risk by prey animals. Ecoscience 5: 361–394.
  Kim, J. W., G. E. Brown & J. W. A. Grant, 2004. Interactions between patch size and predation risk affect competitive aggression and size variation in juvenile convict cichlids. Animal Behaviour 68: 1181–1187.CrossRef
  Kneitel, J. M. & J. M. Chase, 2004. Trade-offs in community ecology: linking spatial scales and species coexistence. Ecology Letters 7: 69–80.CrossRef
  Kohda, M., 1991. Intra- and interspecific social organization among three herbivorous cichlid fishes in Lake Tanganyika. Japanese Journal of Ichthyology 38: 147–163.
  Lakowitz, T., C. Brönmark & P. Nyström, 2008. Tuning into multiple predators: conflicting demands for shell morphology in a freshwater snail. Freshwater Biology 53: 2184–2191.
  Lamboj, A., 2004. Die Cichliden des westlichen Afrikas. Birgit Schmettkamp Verlag, Bornheim.
  Lamboj, A., 2014. Revision of the Pelvicachromis taeniatus-group (Perciformes), with revalidation of the taxon Pelvicachromis kribensis (Boulenger, 1911) and description of a new species. Cybium 38: 205–222.
  Lawrence, B. J. & R. J. F. Smith, 1989. Behavioral response of solitary fathead minnows, Pimephales promelas, to alarm substance. Journal of Chemical Ecology 15: 209–219.PubMed CrossRef
  Leibold, M. A., 1996. A graphical model of keystone predators in food webs: Trophic regulation of abundance, incidence, and diversity patterns in communities. American Naturalist 147: 784–812.CrossRef
  Leibold, M. A., M. Holyoak, N. Mouquet, P. Amarasekare, J. M. Chase, M. F. Hoopes, R. D. Holt, J. B. Shurin, R. Law, D. Tilman, M. Loreau & A. Gonzalez, 2004. The metacommunity concept: a framework for multi-scale community ecology. Ecology Letters 7: 601–613.CrossRef
  Lima, S. L., 1998. Stress and decision making under the risk of predation: Recent developments from behavioral, reproductive, and ecological perspectives. Stress and Behavior 27: 215–290.CrossRef
  Lima, S. L. & L. M. Dill, 1990. Behavioral decisions made under the risk of predation—a review and prospectus. Canadian Journal of Zoology 68: 619–640.CrossRef
  Linke, H. & W. Staeck, 2002. Afrikanische Cichliden I: Buntbarsche aus Westafrika. Tetra Verlag GmbH, Bissendorf.
  Maruyama, A., B. Rusuwa & M. Yuma, 2010. Asymmetric interspecific territorial competition over food resources amongst Lake Malawi cichlid fishes. African Zoology 45: 24–31.CrossRef
  Mathis, A. & R. J. F. Smith, 1993. Chemical labeling of northern pike (Esox lucius) by the alarm pheromone of fathead minnows (Pimephales promelas). Journal of Chemical Ecology 19: 1967–1979.PubMed CrossRef
  Matsumoto, K. & M. Kohda, 2004. Territorial defense against various food competitors in the Tanganyikan benthophagous cichlid Neolamprologus tetracanthus. Ichthyological Research 51: 354–359.CrossRef
  McLennan, D. A., 2004. Male brook stickleback’ (Culaea inconstans) response to olfactory cues. Behaviour 141: 1411–1424.CrossRef
  Mehlis, M., T. C. M. Bakker & J. G. Frommen, 2008. Smells like sib spirit: kin recognition in three-spined sticklebacks (Gasterosteus aculeatus) is mediated by olfactory cues. Animal Cognition 11: 643–650.PubMed CrossRef
  Meuthen, D., S. A. Baldauf, T. C. M. Bakker & T. Thünken, 2011. Substrate-treated water: a method to enhance fish activity in laboratory experiments. Aquatic Biology 13: 35–40.CrossRef
  Meuthen, D., S. A. Baldauf & Thünken, T., 2014. Evolution of alarm cues: a test of the kin selection hypothesis. F1000 Research 1: 27.
  Mirza, R. S. & D. P. Chivers, 2002. Brook char (Salvelinus fontinalis) can differentiate chemical alarm cues produced by different age/size classes of conspecifics. Journal of Chemical Ecology 28: 555–564.PubMed CrossRef
  Mirza, R. S., J. J. Scott & D. P. Chivers, 2001. Differential responses of male and female red swordtails to chemical alarm cues. Journal of Fish Biology 59: 716–728.CrossRef
  Myrberg, A. A. & R. E. Thresher, 1974. Interspecific aggression and its relevance to concept of territoriality in reef fishes. American Zoologist 14: 81–96.CrossRef
  Nosil, P. & B. J. Crespi, 2006. Experimental evidence that predation promotes divergence in adaptive radiation. Proceedings of the National Academy of Sciences 103: 9090–9095.CrossRef
  Oliveira, R. F. & V. C. Almada, 1996. Dominance hierarchies and social structure in captive groups of the Mozambique tilapia Oreochromis mossambicus (Teleostei: Cichlidae). Ethology Ecology and Evolution 8: 39–55.CrossRef
  Parrish, J. D. & S. B. Saila, 1970. Interspecific competition, predation and species diversity. Journal of Theoretical Biology 27: 207–220.PubMed CrossRef
  Peeke, H. V. S. & S. C. Peeke, 1982. Parental factors in the sensitization and habituation of territorial aggression in the convict cichlid (Cichlasoma nigrofasciatum). Journal of Comparative and Physiological Psychology 96: 955–966.PubMed CrossRef
  Peeke, H. V. S., M. J. Herz & J. E. Gallagher, 1971. Changes in aggressive interaction in adjacently territorial convict cichlids (Cichlasoma nigrofasciatum)—study of habituation. Behaviour 40: 43–54.CrossRef
  Peiman, K. S. & B. W. Robinson, 2007. Heterospecific aggression and adaptive divergence in brook stickleback (Culaea inconstans). Evolution 61: 1327–1338.PubMed CrossRef
  Peiman, K. S. & B. W. Robinson, 2010. Ecology and evolution of resource-related heterospecific aggression. The Quarterly Review of Biology 85: 133–158.PubMed CrossRef
  Persson, L., 1990. A field experiment on the effects of interspecific competition from roach, Rutilus rutilus (L.), on age at maturity and gonad size in perch, Perca fluviatilis L. Journal of Fish Biology 37: 899–906.CrossRef
  Pettersson, L. B. & C. Brönmark, 1993. Trading off safety against food: state-dependent habitat choice and foraging in crucian carp. Oecologia 95: 353–357.CrossRef
  Piersma, T. & J. Drent, 2003. Phenotypic flexibility and the evolution of organismal design. Trends in Ecology and Evolution 18: 228–233.CrossRef
  Pimm, S. L., 1984. The complexity and stability of ecosystems. Nature 307: 321–326.CrossRef
  Pollock, M. S., X. X. Zhao, G. E. Brown, R. C. Kusch, R. J. Pollock & D. P. Chivers, 2005. The response of convict cichlids to chemical alarm cues: an integrated study of behaviour, growth and reproduction. Annales Zoologici Fennici 42: 485–495.
  Pomerantz, M. J., W. R. Thomas & M. E. Gilpin, 1980. Asymmetries in population growth regulated by intraspecific competition: empirical studies and model tests. Oecologia 47: 311–322.CrossRef
  Pritchard, J. R. & D. Schluter, 2001. Declining interspecific competition during character displacement: Summoning the ghost of competition past. Evolutionary Ecology Research 3: 209–220.
  R Core Team, 2009. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna.
  Relyea, R. A., 2002. Competitor-induced plasticity in tadpoles: consequences, cues, and connections to predator-induced plasticity. Ecological Monographs 72: 523–540.CrossRef
  Relyea, R. A. & J. R. Auld, 2005. Predator- and competitor-induced plasticity: How changes in foraging morphology affect phenotypic trade-offs. Ecology 86: 1723–1729.CrossRef
  Schluter, D., 1994. Experimental evidence that competition promotes divergence in adaptive radiation. Science 266: 798–801.PubMed CrossRef
  Schoener, T. W., 1973. Population growth regulated by intraspecific competition for energy or time: some simple representations. Theoretical Population Biology 4: 56–84.PubMed CrossRef
  Schoener, T. W., 1982. The controversy over interspecific competition. American Scientist 70: 586–595.
  Schoener, T. W., 1987. Time budgets and territory size: some simultaneous-optimization models for energy maximizers. American Zoologist 27: 259–291.CrossRef
  Schwarzer, J., A. Lamboj, K. Langen, B. Misof & U. Schliewen, 2015. Phylogeny and age of chromidotilapiine cichlids (Teleostei: Cichlidae). Hydrobiologia 748: 185–199.CrossRef
  Seger, J., 1985. Intraspecific resource competition as a cause for sympatric speciation. In Greenwood, P. J., P. H. Harvey & M. Slatkin (eds), Evolution: Essays in Honour of John Maynard Smith. Cambridge University Press, Cambridge.
  Sih, A., R. Ziemba & K. C. Harding, 2000. New insights on how temporal variation in predation risk shapes prey behavior. Trends in Ecology & Evolution 15: 3–4.CrossRef
  Steiger, S., T. Schmitt & H. M. Schaefer, 2011. The origin and dynamic evolution of chemical information transfer. Proceedings of the Royal Society B 278: 970–979.PubMedCentral PubMed CrossRef
  Strobbe, F., M. A. McPeek, M. De Block & R. Stoks, 2011. Fish predation selects for reduced foraging activity. Behavioral Ecology and Sociobiology 65: 241–247.CrossRef
  Taylor, P. W. & R. W. Elwood, 2003. The mismeasure of animal contests. Animal Behaviour 65: 1195–1202.CrossRef
  Teplitsky, C., S. Plenet & P. Joly, 2005. Costs and limits of dosage response to predation risk: to what extent can tadpoles invest in anti-predator morphology? Oecologia 145: 364–370.PubMed CrossRef
  Thünken, T., T. C. M. Bakker, S. A. Baldauf & H. Kullmann, 2007. Active inbreeding in a cichlid fish and its adaptive significance. Current Biology 17: 225–229.PubMed CrossRef
  Thünken, T., N. Waltschyk, T. C. M. Bakker & H. Kullmann, 2009. Olfactory self-recognition in a cichlid fish. Animal Cognition 12: 717–724.PubMed CrossRef
  Thünken, T., D. Meuthen, T. C. M. Bakker & H. Kullmann, 2010. Parental investment in relation to offspring quality in the biparental cichlid fish Pelvicachromis taeniatus. Animal Behaviour 80: 69–74.CrossRef
  Thünken, T., S. A. Baldauf, H. Kullmann, J. Schuld, S. Hesse & T. C. M. Bakker, 2011. Size-related inbreeding preference and competitiveness in male Pelvicachromis taeniatus (Cichlidae). Behavioral Ecology 22: 358–362.CrossRef
  Tilman, D., 2000. Causes, consequences and ethics of biodiversity. Nature 405: 208–211.PubMed CrossRef
  Uriarte, M., C. D. Canham & R. B. Root, 2002. A model of simultaneous evolution of competitive ability and herbivore resistance in a perennial plant. Ecology 83: 2649–2663.CrossRef
  Vøllestad, L. A., K. Varreng & A. B. S. Poleo, 2004. Body depth variation in crucian carp Carassius carassius: an experimental individual-based study. Ecology of Freshwater Fish 13: 197–202.CrossRef
  Wisenden, B. D., 2000. Olfactory assessment of predation risk in the aquatic environment. Philosophical Transactions of the Royal Society B 355: 1205–1208.CrossRef
  Wisenden, B. D. & R. C. Sargent, 1997. Antipredator behaviour and suppressed aggression by convict cichlids in response to injury-released chemical cues of conspecifics but not to those of an allopatric heterospecific. Ethology 103: 283–291.CrossRef
  
• 作者单位：Denis Meuthen (1)
  Sebastian A. Baldauf (1)
  Theo C. M. Bakker (1)
  Timo Thünken (1)
  
  1. Institute for Evolutionary Biology and Ecology, University of Bonn, An der Immenburg 1, 53121, Bonn, Germany
  
• 刊物类别：Biomedical and Life Sciences
• 刊物主题：Life Sciences
  Hydrobiology
  Ecology
  
• 出版者：Springer Netherlands
• ISSN：1573-5117

文摘

Individuals have to respond simultaneously to different environmental factors often making trade-offs between conflicting demands necessary. Many freshwater ecosystems are resource-limited and both intra- and interspecific competitiveness is a common requirement to gain and defend resources necessary for reproduction. Although predation risk is an important selective force affecting behavioral decisions, little is known about the impact of predation risk on interspecific competition. Here, we investigate whether chemically mediated predation risk affects interspecific territorial aggression by the freshwater cichlid Pelvicachromis taeniatus. In our experiments, territorial P. taeniatus males were visually confronted with a territorial intruder: a heterospecific, sympatric cichlid (Benitochromis nigrodorsalis) which generally induced aggression in P. taeniatus. Predation risk for P. taeniatus was simulated by a concurrent release of conspecific chemical alarm cues. In control treatments, no chemical cues, dissolved heterospecific alarm cues, or aliquots of distilled water were provided during these aggressive encounters. The results show that interspecific aggression of territorial male P. taeniatus is significantly decreased under predation risk compared to the control treatments. This suggests that interspecific competition becomes less intense under concurrent predation risk. As this process could hinder competitive exclusion, predation risk may indirectly promote and stabilize biodiversity in natural ecosystems. Keywords Pelvicachromis taeniatus Pelvicachromis kribensis Alarm cues Interspecific aggression Interspecific competition Predation risk