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Adaptive behaviour of chironomid larvae (Chironomus riparius) in response to chemical stimuli from predators and resource density

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Abstract

Chemical-mediated effects of predatory fish on chironomid larvae behaviour have been ignored so far. Sediment-dwelling chironomid larvae inhabit protective burrows from which they extend their bodies only to feed on deposited detritus and microalgae from the surrounding sediment. Here, we performed factorial laboratory experiments to study whether fish-borne chemical cues (kairomones) are responsible for behavioural trait changes of chironomid larvae, and whether chironomid larvae are able to assess the densities of fish predators and food resources and the trade-off between them. We exposed naïve Chironomus riparius larvae to the chemical presence of zero, one, and ten predator fish (Rutilus rutilus) and offered two resource levels (low food, high food) for each treatment. Kairomones induced significant inherent behavioural trait changes in chironomid larvae. During the first 120 min after exposing chironomids to fish-conditioned water, we found a significant increase in digging activity with increasing predator density. After 3 days of exposure, the deepest chironomid burrows were found in treatments with the highest predator density. Chironomid larvae were significantly able to adjust their foraging behaviour to different predator densities and food concentrations and trade off between them; that is, when fish predators were more abundant or when more food resources were available, the foraging activities of larvae were significantly reduced. Our data suggest that chemically mediated trait changes (burrowing and foraging behaviour) may cascade through the littoral food web.

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References

  • Åbjörnsson K, Wagner BMA, Axelsson A, Bjerselius R, Olsén KH (1997) Responses of Acilius sulcatus (Coleoptera: Dytiscidae) to chemical cues from perch (Perca fluviatilis). Oecologia 111:166–171

    Google Scholar 

  • Åbjörnsson K, Hansson LA, Brönmark C (2004) Responses of prey from habitats with different predator regimes: local adaptation and heritability. Ecology 85:1859–1866

    Google Scholar 

  • Abrams AA (1995) Implications of dynamically variable traits for identifying, classifying, and measuring direct and indirect effects in ecological communities. Am Nat 146:112–134

    Article  Google Scholar 

  • Anholt BR, Werner EE (1995) Interaction between food availability and predation mortality mediated by adaptive behavior. Ecology 76:2230–2234

    Google Scholar 

  • Anholt BR, Werner EE, Skelly DK (2000) Effect of food and predators on the activity of four larval ranid frogs. Ecology 81:3509–3521

    Google Scholar 

  • Armitage P, Cranston PS, Pinder LCV (1995) The chironomidae. The biology and ecology of non-biting midges. Chapman and Hall, London

    Google Scholar 

  • Ball SL, Baker RL (1996) Predator-induced life history changes: antipredator behavior costs or facultative life history shifts? Ecology 77:1116–1124

    Google Scholar 

  • Baumgärtner D, Jungbluth A-D, Koch U, von Elert E (2002) Effects of infochemicals on microhabitat choice by the freshwater amphipod Gammarus roeseli. Arch Hydrobiol 155:353–367

    Google Scholar 

  • Berejikian BA, Tezak EP, LaRae AL (2003) Innate and enhanced predator recognition in hatchery-reared chinook salmon. Environ Biol Fishes 67:241–251

    Google Scholar 

  • Bernot RJ, Turner AM (2001) Predator identity and trait-mediated indirect effects in a littoral food web. Oecologia 129:139–146

    Google Scholar 

  • Brooke LT, Ankley GT, Call DJ, Cook PM (1996) Gut content weight and clearance rate for three species of freshwater invertebrates. Environ Toxicol Chem 15:223–228

    Google Scholar 

  • Brown GE (2003) Learning about danger: chemical alarm cues and local risk assessment in prey fishes. Fish Fish 4:227–234

    Article  CAS  Google Scholar 

  • Burks RL, Lodge DM (2002) Cued in: advances and opportunities in freshwater chemical ecology. J Chem Ecol 28:1881–1897

    Google Scholar 

  • Bumann D, Krause J, Rubenstein D (1997) Mortality of spatial positions in animal groups: the danger of being in the front. Behaviour 134:1063–1076

    Google Scholar 

  • Chivers DP, Smith RJF (1994) The role of experience and chemical alarm signalling in predator recognition by fathead minnows, Pimephales promelas. J Fish Biol 44:273–285

    Google Scholar 

  • Chivers DP, Smith RJF (1998) Chemical alarm signalling in aquatic predator-prey systems: a review and prospectus. Écoscience 5:338–352

    Google Scholar 

  • Chivers DP, Mirza RS, Bryer PJ, Kiesecker JM (2001) Threat-sensitive predator avoidance by slimy sculpins: understanding the role of visual versus chemical information. Can J Zool 79:867–873

    Google Scholar 

  • Dahl J, Nilsson PA, Pettersson LB (1998) Against the flow: chemical detection of downstream predators in running waters. Proc R Soc Lond B 265:1339–1344

    Google Scholar 

  • De Meester L (1993) Genotype, fish-mediated chemicals and phototaxis in Daphnia. Ecology 74:1467–1474

    Google Scholar 

  • Dicke M, Sabelis MW (1988) Infochemical terminology: based on cost-benefit analysis rather than origin of compounds? Funct Ecol 2:131–139

    Google Scholar 

  • Gallepp GW (1979) Chironomid influence on phosphorus release in sediment-water microcosms. Ecology 60:547–556

    Google Scholar 

  • Gallie JA, Mumme RL Wissinger SA (2001) Experience has no effect on the development of chemosensory recognition of predators by tadpoles of the American toad, Bufo americanus. Herpetologica 57:376–383

    Google Scholar 

  • Haberlehner E (1988) Comparative analysis of feeding and schooling behaviour of the Cyprinidae Alburnus alburnus (L., 1758), Rutilus rutilus (L., 1758), and Scardinius erythrophthalmus (L., 1758) in a backwater of the Danube near Vienna. Int Rev Gesamt Hydrobiol 73:537–546

    Google Scholar 

  • Hammer C, Temming A, Schubert H-J (1994) Diurnal variations in swimming activity of Rutilus rutilus (Cyprinidae) in a group under tank conditions. Int Rev Gesamt Hydrobiol 79:385–396

    Google Scholar 

  • Hershey AE (1987) Tubes and foraging behavior in larval chironomidae: implications for predator avoidance. Oecologia 73:236–241

    Article  Google Scholar 

  • Helfman GS (1989) Threat-sensitive predator avoidance in damselfish-trumpetfish interactions. Behav Ecol Sociobiol 24:47–58

    Google Scholar 

  • Hölker F, Haertel SS, Steiner S, Mehner T (2002) Effects of piscivore-mediated habitat use on growth, diet and zooplankton consumption of roach: an individual-based modelling approach. Freshw Biol 47:2345–2358

    Google Scholar 

  • Hölker F, Mehner T (2005) Simulation of trait-mediated and density-mediated indirect effects of piscivorous predators on a lake food web. Basic Appl Ecol 6 (in press)

  • Hooper HL, Sibly RM, Hutchinson TH, Maund SJ (2003) The influence of larval density, food availability and habitat longevity on the life history and population growth rate of the midge Chironomus riparius. Oikos 102:515–524

    Google Scholar 

  • Horat P, Semlitsch RD (1994) Effects of predation risk and hunger on the behaviour of two species of tadpoles. Behav Ecol Sociobiol 34:393–401

    Google Scholar 

  • Johnson RK, Boström B, Bund WJ van de (1989) Interactions between Chironomus plumosus L. and the microbial community in surficial sediments of a shallow eutrophic lake. Limnol Oceanogr 34:992–1003

    Google Scholar 

  • Kalmijn AJ (1988) Hydrodynamic and acoustic field detection. In: Atema J, Fay RR, Popper AN, Tavolga WN (eds) Sensory biology of aquatic animals. Springer, Berlin Heidelberg New York, pp 83–130

    Google Scholar 

  • Kats LB, Dill LM (1998) The scent of death: chemosensory assessment of predation risk by prey animals. Écoscience 5:361–394

    Google Scholar 

  • Koperski P (1998) Predator-prey interactions between larval damselflies and mining larvae of Glyptotendipes gripekoveni (Chironomidae): reduction in feeding activity as an induced defense. Freshw Biol 39:317–324

    Google Scholar 

  • Kusch RC, Mirza RS, Chivers DP (2004) Making sense of predator scents: investigating the sophistication of predator assessment abilities of fathead minnows. Behav Ecol Sociobiol 55:551–555

    Google Scholar 

  • Lass S, Spaak P (2003) Chemically induced anti-predator defenses in plankton: a review. Hydrobiologia 491:221–239

    Google Scholar 

  • Macchiusi F, Baker RL (1991) Prey behaviour and size-selective predation by fish. Freshw Biol 25:533–538

    Google Scholar 

  • Macchiusi F, Baker RL (1992) Effects of predators and food availability on activity and growth of Chironomus tentans (Chironomidae: Diptera). Freshw Biol 28:207–216

    Google Scholar 

  • Matisoff G, Wang X (1998) Solute transport in sediments by freshwater infaunal bioirrigators. Limnol Oceanogr 43:1487–1499

    Google Scholar 

  • McIntosh AR, Peckarsky BL, Taylor BW (1999) Rapid size-specific changes in the drift of Baetis bicaudatus (Ephemeroptera) caused by alterations in fish odour concentration. Oecologia 118:256–264

    Google Scholar 

  • Neill WE (1990) Induced vertical migration in copepods as a defense against invertebrate predation. Nature 345:524–526

    Article  Google Scholar 

  • Neumann D, Kramer M, Raschke I, Gräfe B (2001) Detrimental effects of nitrite on the development of benthic Chironomus larvae, in relation to their settlement in muddy sediments. Arch Hydrobiol 153:103–128

    Google Scholar 

  • Osborne S, Hurrell S, Simkiss K, Leidi A (2000) Factors influencing the distribution and feeding of the larvae of Chironomus riparius. Entomol Exp Appl 94:67–73

    Google Scholar 

  • Peacor SD, Werner EE (1997) Trait-mediated indirect interactions in a simple aquatic food web. Ecology 78:1146–1156

    Google Scholar 

  • Peckarsky BL (1980) Predator-prey interactions between stoneflies and mayflies: behavioral observations. Ecology 61:932–943

    Google Scholar 

  • Persson L (1982) Rate of food evacuation in roach (Rutilus rutilus) in relation to temperature, and the application of evacuation rate estimates for studies on rate of food consumption. Freshw Biol 12:203–210

    Google Scholar 

  • Péry ARR, Mons R, Flammarion P, Lagadic L, Garric J (2002) A modeling approach to link food availability, growth, emergence, and reproduction for the midge Chironomus riparius. Environ Toxicol Chem 21:2507–2513

    Google Scholar 

  • Schmitz OJ, Beckerman AP, O’Brian KM (1997) Behaviorally mediated trophic cascades: effects of predation risk on food web interactions. Ecology 78:1388–1399

    Google Scholar 

  • Sih A (1986) Antipredator responses and the perception of danger by mosquito larvae. Ecology 67:434–441

    Google Scholar 

  • Stief P, De Beer D (2002) Bioturbation effects of Chironomus riparius on the benthic N-cycle as measured using microsensors and microbiological assays. Aquat Microbiol Ecol 27:175–185

    Google Scholar 

  • Svensson JM, Leonardson L (1996) Effects of bioturbation by tube-dwelling chironomid larvae on oxygen uptake and denitrification in eutrophic lake sediments. Freshw Biol 35:101–112

    Google Scholar 

  • Van Buskirk J, Arioli M (2002) Dosage response of an induced defense: how sensitive are tadpoles to predation risk? Ecology 83:1580–1585

    Google Scholar 

  • Van de Bund WJ, Goedkoop W, Johnson RK (1994) Effects of deposit-feeder activity on bacterial production and abundance in profundal lake sediment. J N Am Benthol Soc 13:532–539

    Google Scholar 

  • Van de Bund WJ, Groenendijk D (1994) Seasonal dynamics and burrowing of littoral chironomid larvae in relation to competition and predation. Arch Hydrobiol 132:213–225

    Google Scholar 

  • Vilhunen S, Hirvonen H (2003) Innate antipredator responses of Arctic charr (Salvelinus alpinus) depend on predator species and their diet. Behav Ecol Sociobiol 55:1–10

    Google Scholar 

  • Wedemeyer GA (1996) Physiology of fish in intensive culture. Chapman and Hall, New York

    Google Scholar 

  • Wisenden BD (2000) Olfactory assessment of predation risk in the aquatic environment. Philos Trans R Soc Lond B 355:1205–1208

    Google Scholar 

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Acknowledgements

We would like to thank Thomas Mehner and Rita Adrian for valuable comments on the manuscript and Werner Wosniok for statistical assistance. The experiments comply with the current German laws on animal care.

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Authors and Affiliations

  1. Leibniz Institute of Freshwater Ecology and Inland Fisheries, Müggelseedamm 310, 12587, Berlin, Germany

    Franz Hölker

  2. Max Planck Institute for Marine Microbiology, Celsiusstrasse 1, 28359, Bremen, Germany

    Peter Stief

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  1. Franz Hölker
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Correspondence to Franz Hölker.

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Communicated by J. Krause

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Hölker, F., Stief, P. Adaptive behaviour of chironomid larvae (Chironomus riparius) in response to chemical stimuli from predators and resource density. Behav Ecol Sociobiol 58, 256–263 (2005). https://doi.org/10.1007/s00265-005-0932-8

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  • DOI: https://doi.org/10.1007/s00265-005-0932-8

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