Density-dependent adjustment of inducible defenses

Ralph Tollrian; Sonja Duggen; Linda C. Weiss; Christian Laforsch; Michael Kopp

doi:10.1038/srep12736

journal article Open Access Aug 03, 2015

Density-dependent adjustment of inducible defenses

Ralph Tollrian Sonja Duggen Linda C. Weiss Christian Laforsch

Michael Kopp

Scientific Reports Vol. 5 No. 1 · Springer Science and Business Media LLC

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Abstract

AbstractPredation is a major factor driving evolution and organisms have evolved adaptations increasing their survival chances. However, most defenses incur trade-offs between benefits and costs. Many organisms save costs by employing inducible defenses as responses to fluctuating predation risk. The level of defense often increases with predator densities. However, individual predation risk should not only depend on predator density but also on the density of conspecifics. If the predator has a saturating functional response one would predict a negative correlation between prey density and individual predation risk and hence defense expression. Here, we tested this hypothesis using six model systems, covering a taxonomic range from protozoa to rotifers and crustaceans. In all six systems, we found that the level of defense expression increased with predator density but decreased with prey density. In one of our systems, i.e. in Daphnia, we further show that the response to prey density is triggered by a chemical cue released by conspecifics and congeners. Our results indicate that organisms adjust the degree of defense to the acute predation risk, rather than merely to predators’ densities. Our study suggests that density-dependent defense expression reflects accurate predation-risk assessment and is a general principle in many inducible-defense systems.

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References

49

[1]

Tollrian, R. & Harvell, C. D. The ecology and evolution of inducible defenses. (Princeton University Press 1999). 10.1515/9780691228198

[2]

Kats, L. B. & Dill, L. M. The scent of death: chemosensory assessment of predation risk by prey animals. Ecoscience. 5, 361–394 (1998). 10.1080/11956860.1998.11682468

[3]

Bertram, B. C. R. Living in groups: predators and prey in Behavioural Ecology: an Evolutionary Approach. (ed. Krebs, J. R. & Davies, N. B. ) pp. 64–96 (Blackwell Scientific, Oxford 1978).

[4]

Hamilton, W. D. Geometry for the selfish herd. J Theor Biol. 31, 295–311 (1971). 10.1016/0022-5193(71)90189-5

[5]

Peacor, S. D. Phenotypic modifications to conspecific density arising from predation risk assessment. Oikos. 100, 409–415 (2003). 10.1034/j.1600-0706.2003.12043.x

[6]

Jeschke, J. M. Density-dependent effects of prey defenses and predator offenses. J Theor Biol. 242, 900–907 (2006). 10.1016/j.jtbi.2006.05.017

[7]

Ale, S. B., Brown, J. S. The contingencies of group size and vigilance. Evol Ecol Res. 9, 1263–1276 (2007).

[8]

Hanazato, T. Influence of food density on the effects of a Chaoborus-released chemical on Daphnia ambigua. Freshw Biol. 25, 477–483 (1991). 10.1111/j.1365-2427.1991.tb01390.x

[9]

Anholt, B. R. & Werner, E. E. Interaction between food availability and predation mortality mediated by adaptive behavior. Ecology. 76, 2230–2234 (1995). 10.2307/1941696

[10]

Pettersson, L. B. & Brönmark, C. Density-dependent costs of an inducible morphological defense in crucian carp. Ecology. 78, 1805–1815 (1997). 10.1890/0012-9658(1997)078[1805:ddcoai]2.0.co;2

[11]

Fyda, J. & Wiackowski, K. Benefits and costs of predator-induced morphological changes in the ciliate Colpidium kleini (Protozoa, Ciliophora). Europ J of Protozool. 34, 118–123 (1998). 10.1016/s0932-4739(98)80021-7

[12]

Wiackowski, K. & Starońska, A. The effect of predator and prey density on the induced defence of a ciliate. Funct Ecol. 13, 59–65 (1999). 10.1046/j.1365-2435.1999.00282.x

[13]

McCoy, M. W., Conspecific density determines the magnitude and character of predator-induced phenotype. Oecologia. 153, 871–878 (2007). 10.1007/s00442-007-0795-y

[14]

Van Buskirk, J., Ferrari, M., Kueng, D., Näpflin, K. & Ritter, N. Prey risk assessment depends on conspecific density. Oikos. 120, 1235–1239 (2011). 10.1111/j.1600-0706.2010.19311.x

[15]

Burns, C. W. Crowding-induced changes in growth, reproduction and morphology of Daphnia. Freshw Biol. 43, 19–29 (2000). 10.1046/j.1365-2427.2000.00510.x

[16]

Jeschke, J. M., Kopp, M. & Tollrian, R. Predator functional responses: discriminating between handling and digesting prey. Ecolog Monogr. 72, 95–112 (2002). 10.1890/0012-9615(2002)072[0095:pfrdbh]2.0.co;2

[17]

Jeschke, J. M., Kopp, M. & Tollrian, R. Consumer-food systems: why type I functional responses are exclusive to filter feeders. Biol Rev Camb Philos Soc. 79, 337–349 (2004). 10.1017/s1464793103006286

[18]

Jeschke, J. M. & Tollrian, R. Density-dependent effects of prey defences. Oecologia. 123, 391–396 (2000). 10.1007/s004420051026

[19]

Stankowich, T. & Blumstein, D. T. Fear in animals: a meta-analysis and review of risk assessment. Proc R Soc B. 272, 2627–2634 (2005). 10.1098/rspb.2005.3251

[20]

Laforsch, C., Beccara, L. & Tollrian, R. Inducible defenses: The relevance of chemical alarm cues in Daphnia. Limnol Oceanogr. 51, 1466–1472 (2006). 10.4319/lo.2006.51.3.1466

[21]

Wilson, K., Thomas, M. B., Blanford, S., Doggett, M., Simpson, S. J. & Moore, S. L. Coping with crowds: density-dependent disease resistance in desert locusts. Proc Natl Acad Sci. 99, 5471–5475 (2002). 10.1073/pnas.082461999

[22]

Elliot, S. L. & Hart, A. G. Density-dependent prophylactic immunity reconsidered in the light of host group living and social behavior. Ecology. 91, 65–72 (2010). 10.1890/09-0424.1

[23]

Yin, M., Laforsch, C., Lohr, J. N. & Wolinska, J. Predator-induced defense makes Daphnia more vulnerable to parasites. Evolution. 65, 1482–1488 (2011). 10.1111/j.1558-5646.2011.01240.x

[24]

Tollrian, R. & Harvell, D. H. The evolution of inducible defenses: current ideas in the ecology and evolution of inducible defenses. (eds Tollrian, R., Harvell, D. C. ). pp. 307–321 (Princeton University Press 1999). 10.1515/9780691228198

[25]

Relyea, R. A. & Auld, J. R. Having the guts to compete: how intestinal plasticity explains costs of inducible defences. Ecol Lett. 7, 869–875 (2004). 10.1111/j.1461-0248.2004.00645.x

[26]

Relyea, R. A. & Auld, J. R. Predator-and competitor-induced plasticity: how changes in foraging morphology affect phenotypic trade-offs. Ecology. 86, 1723–1729 (2005). 10.1890/04-1920

[27]

Wiackowski, K. & Szkarlat, M. Effects of food availability on predator-induced morphological defence in the ciliate Euplotes octocarinatus (Protista). Hydrobiol. 321, 47–52 (1996). 10.1007/bf00018676

[28]

Spaak, P. & Boersma, M. Tail spine length in the Daphnia galeata complex: costs and benefits of induction by fish. Aqu Ecol. 31, 89–98 (1997). 10.1023/a:1009935100804

[29]

Cipollini, D. Stretching the limits of plasticity: can a plant defend against both competitors and herbivores? Ecology. 85, 28–37 (2004). 10.1890/02-0615

[30]

Relyea, R. A. F.ine-tuned phenotypes: tadpole plasticity under 16 combinations of predators and competitors. Ecology. 85, 172–179 (2004). 10.1890/03-0169

[31]

Izaguirre, M. M., Mazza, C. A., Biondini, M., Baldwin, I. T. & Ballaré, C. L. Remote sensing of future competitors: impacts on plant defenses. Proc Natl Acad Sci. 103, 7170–7174 (2006). 10.1073/pnas.0509805103

[32]

Gilbert, J. Kairomone induced morphological changes in rotifers in the ecology and evolution of inducible defenses. (eds Tollrian, R. & Harvell, D. C. ) pp. 177–202 (Princeton University Press 1999). 10.1515/9780691228198-010

[33]

Barry, M. J. The costs of crest induction for Daphnia carinata. Oecologia. 97, 278–288 (1994). 10.1007/bf00323161

[34]

Tollrian, R., Dodson, S. D. Inducible defenses in Cladocera: Constraints, Costs and multipredator environments in the ecology and evolution of inducible defenses. (eds Tollrian, R. & Harvell, D. C. ) pp.177–202 (Princeton University Press 1999). 10.1515/9780691228198-013

[35]

Tollrian, R. Predator-induced morphological defenses: costs, life history shifts and maternal effects in Daphnia pulex. Ecology. 76, 1691–1705 (1995). 10.2307/1940703

[36]

Chornesky, E. A. Induced development of sweeper tentacles on the reef coral Agaricia agaricites: a response to direct competition. Biol Bull. 165, 569–581 (1983). 10.2307/1541466

[37]

Relyea, R. A. Competitor-induced plasticity in tadpoles: consequences, cues and connections to predator-induced plasticity. Ecol Monogr. 72, 523–540 (2002). 10.1890/0012-9615(2002)072[0523:cipitc]2.0.co;2

[38]

Gilbert, J. J. Specificity of crowding response that induces sexuality in the rotifer Brachionus. Limnol Oceanogr. 48, 1297–1303 (2003). 10.4319/lo.2003.48.3.1297

[39]

Lürling, M. The effect of substances from different zooplankton species and fish on the induction of defensive morphology in the green alga Scenedesmus obliquus. J Plankton Res. 25, 979 (2003). 10.1093/plankt/25.8.979

[40]

Werner, E. E. & Peacor, S. D. A review of trait-mediated indirect interactions in ecological communities. Ecology. 84, 1083–1100 (2003). 10.1890/0012-9658(2003)084[1083:arotii]2.0.co;2

[41]

Miner, B. G., Sultan, S. E., Morgan, S. G., Padilla, D. K. & Relyea, R. A. Ecological consequences of phenotypic plasticity. Trends Ecol Evol. 20, 685–692 (2005). 10.1016/j.tree.2005.08.002

[42]

Gilbert, J. J. Rotifer ecology and embryological induction. Science. 151, 1234–1237 (1966). 10.1126/science.151.3715.1234

[43]

Tollrian, R. Predator-induced helmet formation in Daphnia cucullata (Sars). Arch f Hydrobiol. 119, 191–196 (1990). 10.1127/archiv-hydrobiol/119/1990/191

[44]

Krueger, D. A. & Dodson, S. I. Embryological induction and predation ecology in Daphnia pulex. Limnol and Oceanogr. 26, 219–223 (1981). 10.4319/lo.1981.26.2.0219

[45]

Grant, J. W. G. & Bayly, I. A. E. Predator induction of crests in morphs of the Daphnia carinata King Complex. Limnol and Oceanogr. 26, 201–218 (1981). 10.4319/lo.1981.26.2.0201

[46]

Tollrian, R. Fish-kairomone induced morphological changes in Daphnia lumholtzi (Sars). Arch f Hydrobiol. 130, 69–69 (1994). 10.1127/archiv-hydrobiol/130/1994/69

[47]

Tollrian, R. Neckteeth formation in Daphnia pulex as an example of continuous phenotypic plasticity: morphological effects of Chaoborus kairomone concentration and their quantification. J Plankton Res. 15, 1309–1318 (1993). 10.1093/plankt/15.11.1309

[48]

Laforsch, C. & Tollrian, R. Cyclomorphosis and phenotypic defences in Encyclopedia of Inland waters (ed Edited by Liekens, G. E. ) Vol. 3 pp. 643–650 (Elsevier, 2009). 10.1016/b978-012370626-3.00150-2

[49]

Fyda, J. Predator-induced morphological changes in the ciliate Colpidium (Protozoa, Ciliophora). Europ J Protozool. 34, 111–117 (1998).

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Published: Aug 03, 2015
Vol/Issue: 5(1)
License: View

Authors

Animal Ecology I and BayCEER University of Bayreuth Bayreuth Germany

M

Michael Kopp

Cite This Article

Ralph Tollrian, Sonja Duggen, Linda C. Weiss, et al. (2015). Density-dependent adjustment of inducible defenses. Scientific Reports, 5(1). https://doi.org/10.1038/srep12736

Density-dependent adjustment of inducible defenses

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