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RESEARCH ARTICLE

Learned recognition and avoidance of invasive mosquitofish by the shrimp, Paratya australiensis

Joshua D. Bool A , Kristen Witcomb A , Erin Kydd A and Culum Brown A B
+ Author Affiliations
- Author Affiliations

A Department of Biological Sciences, Macquarie University, Sydney, NSW 2109, Australia.

B Corresponding author. Email: Culum.Brown@mq.edu.au

Marine and Freshwater Research 62(10) 1230-1236 https://doi.org/10.1071/MF11140
Submitted: 17 June 2011  Accepted: 16 August 2011   Published: 29 September 2011

Abstract

Little is known about the learning ability of crustaceans, especially with respect to their anti-predator responses to invasive species. In many vertebrates, anti-predator behaviour is influenced by experience during ontogeny. Here, predator-naïve glass shrimp (Paratya australiensisis) were exposed to a predatory, invasive fish species, Gambusia holbrooki, to determine whether shrimp could learn to: (1) avoid the scent of Gambusia via classical conditioning; and (2) restrict their activity patterns to the night to reduce predatory encounters. Conditioned shrimp were placed in containers in aquaria containing Gambusia for 3 days during which time they could be harassed but not consumed by Gambusia. When tested in a Y-maze, conditioned shrimp showed a long delay before making a choice between Gambusia scented water and aged tap water but chose an arm at random. Control shrimp showed a brief delay in emergence and also chose at random. In a second experiment, we housed shrimp with a single Gambusia and observed their activity patterns. In the presence of Gambusia, shrimp switched from diurnal to nocturnal foraging. These results show that naïve shrimp learn to recognise novel predatory species via chemical cues and adjust their activity patterns to coincide with periods when Gambusia are inactive.

Additional keywords: conditioning, crustacean, Gambusia, learning, predator, shrimp.


References

Ache, A., and Case, J. (1969). An analysis of antennular chemoreception in two commensal shrimps of the genus Betaeus. Physiological Zoology 42, 361–371.
| 1:CAS:528:DyaE3cXlt1ersg%3D%3D&md5=edf3ec1262ad248870d3b8cd89477898CAS |

Ache, B. W., Fuzessery, Z. M., and Carr, W. E. S. (1976). Antennular chemosensitivity in the spiny lobster, Panulirus argus: comparative tests of high and low molecular weight stimulants. The Biological Bulletin 151, 273–282.
Antennular chemosensitivity in the spiny lobster, Panulirus argus: comparative tests of high and low molecular weight stimulants.Crossref | GoogleScholarGoogle Scholar |

Acquistapace, P., Hazlett, B. A., and Gherardi, F. (2003). Unsuccessful predation and learning of predator cues by crayfish. Journal of Crustacean Biology 23, 364–370.
Unsuccessful predation and learning of predator cues by crayfish.Crossref | GoogleScholarGoogle Scholar |

Arthington, A. H. (1991). Ecological and genetic impacts of introduced and translocated freshwater fishes in Australia. Canadian Journal of Fisheries and Aquatic Sciences 48, 33–43.
Ecological and genetic impacts of introduced and translocated freshwater fishes in Australia.Crossref | GoogleScholarGoogle Scholar |

Brown, G. E., Ferarri, M. C. O., and Chivers, D. P. (2011). Learning about danger: chemical alarm cues and threat sensitive assessment of predation risk by fishes. In ‘Fish Cognition and Behaviour, 2nd edition’. (Eds C. Brown, K. Laland and J. Krause.) pp. 59–80. (Blackwell: Oxford.)

Carey, C., Ching, M., Collins, S., Early, A., Fetzer, W., Chai, D., and Hairston, N. (2011). Predator-dependent diel migration by Halocaridina rubra shrimp (Malacostraca: Atyidae) in Hawaiian anchialine pools. Aquatic Ecology 45, 35–41.
Predator-dependent diel migration by Halocaridina rubra shrimp (Malacostraca: Atyidae) in Hawaiian anchialine pools.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsFyru78%3D&md5=015d6639a49434c52f318addc87b5582CAS |

Carr, W. E. S., and Gurin, S. (1975). Chemoreception in the shrimp, Palaemonetes pugio: comparative study of stimulatory substances in human serum. The Biological Bulletin 148, 380–392.
Chemoreception in the shrimp, Palaemonetes pugio: comparative study of stimulatory substances in human serum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2MXksFGru7o%3D&md5=d4acca5d2adf144471c61b24e796b824CAS |

Crowl, T. A., and Covich, A. P. (1994). Responses of freshwater shrimp to chemical and tactile stimuli from a large decapod predator. Journal of the North American Benthological Society 13, 291–298.
Responses of freshwater shrimp to chemical and tactile stimuli from a large decapod predator.Crossref | GoogleScholarGoogle Scholar |

Csanyi, V., and Doka, A. (1993). Learning interactions between prey and predator fish. Marine Behaviour and Physiology 23, 63–78.
Learning interactions between prey and predator fish.Crossref | GoogleScholarGoogle Scholar |

Darwish, T. L., Mirza, R. S., Leduc, A. O. H. C., and Brown, G. E. (2005). Acquired recognition of novel predator odour cocktails by juvenile glowlight tetras. Animal Behaviour 70, 83–89.
Acquired recognition of novel predator odour cocktails by juvenile glowlight tetras.Crossref | GoogleScholarGoogle Scholar |

Dupuch, A., Magnan, P., and Dill, L. M. (2004). Sensitivity of northern redbelly dace, Phoxinus eos, to chemical alarm cues. Canadian Journal of Zoology 82, 407–415.
Sensitivity of northern redbelly dace, Phoxinus eos, to chemical alarm cues.Crossref | GoogleScholarGoogle Scholar |

Griffin, A. S. (2008). Socially acquired predator avoidance: is it just classical conditioning? Brain Research Bulletin 76, 264–271.
Socially acquired predator avoidance: is it just classical conditioning?Crossref | GoogleScholarGoogle Scholar |

Hancock, M. A., and Bunn, S. E. (1999). Swimming response to water current in Paratya australiensis Kemp, 1917 (Decapoda, Atyidae) under laboratory conditions. Crustaceana 72, 313–323.
Swimming response to water current in Paratya australiensis Kemp, 1917 (Decapoda, Atyidae) under laboratory conditions.Crossref | GoogleScholarGoogle Scholar |

Hazlett, B. A., Acquistapace, P., and Gherardi, F. (2002). Differences in memory capabilities in invasive and native crayfish. Journal of Crustacean Biology 22, 439–448.
Differences in memory capabilities in invasive and native crayfish.Crossref | GoogleScholarGoogle Scholar |

Howe, E., Howe, C., Lim, R., and Burchett, M. (1997). Impact of the introduced poeciliid Gambusia holbrooki (Girard, 1959) on the growth and reproduction of Pseudomugil signifer (Kner, 1865) in Australia. Marine and Freshwater Research 48, 425–434.
Impact of the introduced poeciliid Gambusia holbrooki (Girard, 1959) on the growth and reproduction of Pseudomugil signifer (Kner, 1865) in Australia.Crossref | GoogleScholarGoogle Scholar |

Keller, K., and Brown, C. (2008). Behavioural interactions between the introduced plague minnow Gambusia holbrooki and the vulnerable native Australian ornate rainbowfish Rhadinocentrus ornatus, under experimental conditions. Journal of Fish Biology 73, 1714–1729.
Behavioural interactions between the introduced plague minnow Gambusia holbrooki and the vulnerable native Australian ornate rainbowfish Rhadinocentrus ornatus, under experimental conditions.Crossref | GoogleScholarGoogle Scholar |

Kelley, J. L., and Magurran, A. E. (2011). Learned defences and counter defences in predator–prey interactions. In ‘Fish Cognition and Behaviour, 2nd edition’ (Eds C. Brown, K. Laland and J. Krause.) pp. 36–58. (Blackwell: Oxford.)

Kusch, R. C., Mirza, R. S., and Chivers, D. P. (2004). Making sense of predator scents: investigating the sophistication of predator assessment abilities of fathead minnows. Behavioral Ecology and Sociobiology 55, 551–555.
Making sense of predator scents: investigating the sophistication of predator assessment abilities of fathead minnows.Crossref | GoogleScholarGoogle Scholar |

Leyse, K. E., Lawler, S. P., and Strange, T. (2004). Effects of an alien fish, Gambusia affinis, on an endemic California fairy shrimp, Linderiella occidentalis: implications for conservation of diversity in fishless waters. Biological Conservation 118, 57–65.
Effects of an alien fish, Gambusia affinis, on an endemic California fairy shrimp, Linderiella occidentalis: implications for conservation of diversity in fishless waters.Crossref | GoogleScholarGoogle Scholar |

Lima, S. L., and Bednekoff, P. A. (1999). Temporal variation in danger drives antipredator behaviour: the predation risk allocation hypothesis. American Naturalist 153, 649–659.
Temporal variation in danger drives antipredator behaviour: the predation risk allocation hypothesis.Crossref | GoogleScholarGoogle Scholar |

Lindén, E. (2007). The more the merrier: swarming as an antipredator strategy in the mysid Neomysis integer. Aquatic Ecology 41, 299–307.
The more the merrier: swarming as an antipredator strategy in the mysid Neomysis integer.Crossref | GoogleScholarGoogle Scholar |

Lindén, E., Lehtiniemi, M., and Viitasalo, M. (2003). Predator avoidance behaviour of Baltic littoral mysids Neomysis integer and Praunus flexuosus. Marine Biology 143, 845–850.
Predator avoidance behaviour of Baltic littoral mysids Neomysis integer and Praunus flexuosus.Crossref | GoogleScholarGoogle Scholar |

Lloyd, L. N., and Tomasov, J. F. (1985). Taxonomic status of the mosquitofish, Gambusia affinis (Poeciliidae), in Australia. Australian Journal of Marine and Freshwater Research 36, 447–451.
Taxonomic status of the mosquitofish, Gambusia affinis (Poeciliidae), in Australia.Crossref | GoogleScholarGoogle Scholar |

Magurran, A. E. (1990). The inheritance and development of minnow anti-predator behaviour. Animal Behaviour 39, 834–842.
The inheritance and development of minnow anti-predator behaviour.Crossref | GoogleScholarGoogle Scholar |

Magurran, A. E., and Seghers, B. H. (1990). Population differences in the schooling behaviour of newborn guppies, Poecilia reticulata. Ethology 84, 334–342.
Population differences in the schooling behaviour of newborn guppies, Poecilia reticulata.Crossref | GoogleScholarGoogle Scholar |

March, J. G., Benstead, J. P., Pringle, C. M., and Ruebel, M. W. (2001). Linking shrimp assemblages with rates of detrital processing along an elevational gradient in a tropical stream. Canadian Journal of Fisheries and Aquatic Sciences 58, 470–478.
Linking shrimp assemblages with rates of detrital processing along an elevational gradient in a tropical stream.Crossref | GoogleScholarGoogle Scholar |

March, J. G., Pringle, C. M., Townsend, M. T., and Wilson, A. I. (2002). Effects of freshwater shrimp on assemblages of benthic communities along an altitudinal gradient of a tropic island stream. Freshwater Biology 47, 377–390.
Effects of freshwater shrimp on assemblages of benthic communities along an altitudinal gradient of a tropic island stream.Crossref | GoogleScholarGoogle Scholar |

Pen, L. J., Potter, I. C., and Calver, M. C. (1993). Comparisons of the food niches of three native and two introduced fish species in an Australian river. Environmental Biology of Fishes 36, 167–182.
Comparisons of the food niches of three native and two introduced fish species in an Australian river.Crossref | GoogleScholarGoogle Scholar |

Pfeiffer, W. (1977). The distribution of fright reaction and alarm substance cells in fishes. Copeia 1977, 653–665.
The distribution of fright reaction and alarm substance cells in fishes.Crossref | GoogleScholarGoogle Scholar |

Pringle, C. M. (1996). Atyid shrimps (Decapoda: Atyidae) influence the spatial heterogeneity of the algal communities over different scales in tropical montane streams, Puerto Rico. Freshwater Biology 35, 125–140.
Atyid shrimps (Decapoda: Atyidae) influence the spatial heterogeneity of the algal communities over different scales in tropical montane streams, Puerto Rico.Crossref | GoogleScholarGoogle Scholar |

Pyke, G. H., and White, A. W. (2000). Factors influencing predation on eggs and tadpoles of the endangered green and golden bell frog Litorea aurea by the introduced plague minnow Gambusia holbrooki. Australian Zoologist 31, 496–505.

Richardson, A. J., Growns, J. E., and Cook, R. A. (2004). Distribution and life history of caridean shrimps in regulated lowland rivers in southern Australia. Marine and Freshwater Research 55, 295–308.
Distribution and life history of caridean shrimps in regulated lowland rivers in southern Australia.Crossref | GoogleScholarGoogle Scholar |

Rincón, P. A., Correas, A. M., Morcillo, F., Risueño, P., and Lobón-Cerviá, J. (2002). Interaction between the introduced eastern mosquitofish and two autochthonus Spanish toothcarps. Journal of Fish Biology 61, 1560–1585.
Interaction between the introduced eastern mosquitofish and two autochthonus Spanish toothcarps.Crossref | GoogleScholarGoogle Scholar |

Roh, E., Mirza, R. S., and Brown, G. E. (2004). Quality or quantity? The role of donor condition in the production of chemical alarm cues in juvenile convict cichlids. Behaviour 141, 1235–1248.
Quality or quantity? The role of donor condition in the production of chemical alarm cues in juvenile convict cichlids.Crossref | GoogleScholarGoogle Scholar |

Tamaki, A., Ingole, B., Ikebe, K., Muramatsu, K., Taka, M., and Tanaka, M. (1997). Life history of the ghost shrimp, Callianassa japonica Ortmann (Decapoda: thalassinidea), on an intertidal sandflat in western Kyushu, Japan. Journal of Experimental Marine Biology and Ecology 210, 223–250.
Life history of the ghost shrimp, Callianassa japonica Ortmann (Decapoda: thalassinidea), on an intertidal sandflat in western Kyushu, Japan.Crossref | GoogleScholarGoogle Scholar |

Walsh, C. J., and Mitchell, B. D. (1995). The freshwater shrimp Paratya australiensis (Kemp, 1917) (Decapoda: Atyidae) in estuaries of south-western Victoria, Australia. Marine and Freshwater Research 46, 959–965.
The freshwater shrimp Paratya australiensis (Kemp, 1917) (Decapoda: Atyidae) in estuaries of south-western Victoria, Australia.Crossref | GoogleScholarGoogle Scholar |

Warburton, K., and Madden, C. (2003). Behavioural responses of two native Australian fish species (Melanotaenia duboulayi and Pseudomugil signifer) to introduced poeciliids (Gambusia holbrooki and Xiphophorus helleri) in controlled conditions. Proceedings of the Linnean Society of New South Wales 124, 115–123.

Wisenden, B. D. (2000). Olfactory assessment of predation risk in the aquatic environment. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 355, 1205–1208.
Olfactory assessment of predation risk in the aquatic environment.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3M7psF2luw%3D%3D&md5=d9394d4b5d70538b15e34ee6e5e4afd8CAS |