Phenotypic plasticity is a common defensive strategy in species experiencing variable predation risk, such as habitat generalists. Larvae of generalist dragonflies can elongate their abdominal spines in environments with fish, but long spines render larvae susceptible to invertebrate predators. Long-spined specialists adapted to fish-heavy habitats are not expected to have phenotypic plasticity in this defence trait, but no empirical studies have been undertaken. Moreover, in comparison to prey responding to multiple predators that induce similar phenotypes, relatively little is known regarding how species react to combinations of predators that favour opposing traits. We examined plasticity of larval dragonfly Sympetrum depressiusculum, a long-spined habitat specialist. In a rearing experiment, larvae were exposed to four environments: (i) no predator control, (ii) fish cues (Carassius auratus), (iii) invertebrate cues (Anax imperator), as well as (iv) a combination of (ii) and (iii). Compared with the control, fish but not invertebrate cues resulted in longer spines for two (one lateral, one dorsal) of the six spines measured. Interestingly, the combined-cue treatment led to the elongation of all four dorsal spines compared with the fish treatment alone, whereas lateral spines showed no response. Our experiment provided evidence of morphological plasticity in a long-spined specialist dragonfly. We showed that nearly all spines can elongate, but also react differently under specific predator settings. Therefore, while spine plasticity evolved in direct response to a single predator type (fish), plasticity was maintained against invertebrate predators as long as fish were also present. Selective spine induction under the combined condition suggests that S. depressiusculum can successfully survive in environments with both predators. Therefore, phenotypic plasticity may be an effective strategy for habitat generalists and specialists. Although more studies are necessary to fully understand how selection shapes the evolution of phenotypic plasticity, we demonstrated that in dragonflies, presence or absence of a specific predator is not the only factor that determines plastic defence responses.

Department of Biology and Ecology Faculty of Science University of Ostrava Ostrava Czech Republic

Institute of Environmental Technologies Faculty of Science University of Ostrava Ostrava Czech Republic

Zobrazit více v PubMed

Kerfoot WC, Sih A. Predation. Direct and indirect impacts on aquatic communities. London: University Press of New England; 1987.

van Buskirk J. Interactive effects of dragonfly predation in expermental pond communities. Ecology. 1988;69: 857–867. 10.2307/1941035 DOI

Crowl TA, Covich AP. Predator-induced life-history shifts in a freshwater snail. Science. 1990;247: 949–951. 10.1126/science.247.4945.949 PubMed DOI

Skelly DK, Werner EE. Behavioral and life-historical responses of larval American toads to an odonate predator. Ecology. 1990;71: 2313–2322. 10.2307/1938642 DOI

Relyea RA. Morphological and behavioral plasticity of larval anurans in response to different predators. Ecology. 2001;82: 523–540.

Tseng M. Life-history responses of a mayfly to seasonal constraints and predation risk. Ecol Entomol. 2003;28: 119–123. 10.1046/j.1365-2311.2002.00482.x DOI

Michels E, De Meester L. Inter-clonal variation in phototactic behaviour and key life-history traits in a metapopulation of the cyclical parthenogen Daphnia ambigua: The effect of fish kairomones. Hydrobiologia. 2004;522: 221–233. 10.1023/B:HYDR.0000029988.02195.35 DOI

Lima SL, Dill LM. Behavioral decisions made under the risk of predation: A review and prospectus. Can J Zool. 1990;68: 619–640. 10.1139/z90-092 DOI

Benard MF. Predator-induced phenotypic plasticity in organisms with complex life histories. Annu Rev Ecol Evol Syst. 2004;35: 651–673. 10.1146/annurev.ecolsys.35.021004.112426 DOI

Moran NA. The evolutionary maintenance of alternative phenotypes. Am Nat. 1992;139: 971–989. 10.1086/285369 DOI

Lively CM, Hazel WN, Schellenberger MJ, Michelson KS. Predator-induced defense: Variation for inducibility in an intertidal barnacle. Ecology. 2000;81: 1240–1247. 10.1890/0012-9658(2000)081[1240:PIDVFI]2.0.CO;2 DOI

Agrawal AA. Phenotypic plasticity in the interactions and evolution of species. Science. 2001;294: 321–326. 10.1126/science.1060701 PubMed DOI

Dicke M, Sabelis MW. Infochemical terminology: Based on cost-benefit analysis rather than origin of compounds? Funct Ecol. 1988;2: 131–139. 10.2307/2389687 DOI

Hettyey A, Tóth Z, Thonhauser KE, Frommen JG, Penn DJ, van Buskirk J. The relative importance of prey-borne and predator-borne chemical cues for inducible antipredator responses in tadpoles. Oecologia. 2015;179: 699–710. 10.1007/s00442-015-3382-7 PubMed DOI

Mitchell MD, Bairos-Novak KR, Ferrari MCO. Mechanisms underlying the control of responses to predator odours in aquatic prey. J Exp Biol. 2017;220: 1937–1946. 10.1242/jeb.135137 PubMed DOI

Tollrian R, Harvell CD. The ecology and evolution of inducible defenses. Princeton, New Jersey: Princeton University Press; 1999.

van Buskirk J. The costs of an inducible defense in anuran larvae. Ecology. 2000;81: 2813–2821. 10.1890/0012-9658(2000)081[2813:TCOAID]2.0.CO;2 DOI

Auld JR, Agrawal AA, Relyea RA. Re-evaluating the costs and limits of adaptive phenotypic plasticity. Proc R Soc B Biol Sci. 2010;277: 503–511. 10.1098/rspb.2009.1355 PubMed DOI PMC

von Elert E, Pohnert G. Predator specificity of kairomones in diel vertical migration of Daphnia: a chemical approach. Oikos. 2000;88: 119–128. 10.1034/j.1600-0706.2000.880114.x DOI

van Buskirk J, Arioli M. Dosage response of an induced defense: How sensitive are tadpoles to predation risk? Ecology. 2002;83: 1580–1585. 10.2307/3071977 DOI

Kishida O, Trussell GC, Mougi A, Nishimura K. Evolutionary ecology of inducible morphological plasticity in predator–prey interaction: Toward the practical links with population ecology. Popul Ecol. 2010;52: 37–46. 10.1007/s10144-009-0182-0 DOI

Pfennig DW, Wund MA, Snell-Rood EC, Cruickshank T, Schlichting CD, Moczek AP. Phenotypic plasticity’s impacts on diversification and speciation. Trends Ecol Evol. 2010;25: 459–467. 10.1016/j.tree.2010.05.006 PubMed DOI

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. 1993;15: 1309–1318. 10.1093/plankt/15.11.1309 DOI

Tollrian R. Fish-kairomone induced morphological changes in Daphnia lumholtzi (Sars). Arch Für Hydrobiol. 1994;130: 69–75.

Laforsch C, Tollrian R. Embryological aspects of inducible morphological defenses in Daphnia. J Morphol. 2004;262: 701–707. 10.1002/jmor.10270 PubMed DOI

Gyssels F, Stoks R. Behavioral responses to fish kairomones and autotomy in a damselfly. J Ethol. 2006;24: 79–83. 10.1007/s10164-005-0165-3 DOI

Weiss LC, Leimann J, Tollrian R. Predator-induced defences in Daphnia longicephala: Location of kairomone receptors and timeline of sensitive phases to trait formation. J Exp Biol. 2015;218: 2918–2926. 10.1242/jeb.124552 PubMed DOI PMC

Shaffery HM, Relyea RA. Dissecting the smell of fear from conspecific and heterospecific prey: Investigating the processes that induce anti-predator defenses. Oecologia. 2016;180: 55–65. 10.1007/s00442-015-3444-x PubMed DOI

Heynen M, Bunnefeld N, Borcherding J. Facing different predators: adaptiveness of behavioral and morphological traits under predation. Curr Zool. 2017;63: 249–257. 10.1093/cz/zow056 PubMed DOI PMC

Smith AD, Houde ALS, Neff B, Peres-Neto PR. Effects of competition on fitness-related traits. Oecologia. 2017;183: 701–713. 10.1007/s00442-017-3816-5 PubMed DOI

Polačik M, Janáč M. Costly defense in a fluctuating environment-sensitivity of annual Nothobranchius fishes to predator kairomones. Ecol Evol. 2017;7: 4289–4298. 10.1002/ece3.3019 PubMed DOI PMC

Dahl J, Peckarsky BL. Induced morphological defenses in the wild: Predator effects on a mayfly, Drunella coloradensis. Ecology. 2002;83: 1620–1634. 10.1890/0012-9658(2002)083[1620:IMDITW]2.0.CO;2 DOI

Ball SL, Baker RL. Predator-induced life history changes: Antipredator behavior costs or facultative life history shifts? Ecology. 1996;77: 1116–1124. 10.2307/2265580 DOI

Jourdan J, Baier J, Riesch R, Klimpel S, Streit B, Müller R, et al. Adaptive growth reduction in response to fish kairomones allows mosquito larvae (Culex pipiens) to reduce predation risk. Aquat Sci. 2016;78: 303–314. 10.1007/s00027-015-0432-5 DOI

Johansson F, Samuelsson L. Fish-induced variation in abdominal spine length of Leucorrhinia dubia (Odonata) larvae? Oecologia. 1994;100: 74–79. 10.1007/BF00317132 PubMed DOI

Mikolajewski DJ, Rolff J. Benefits of morphological defence demonstrated by direct manipulation in larval dragonflies. Evol Ecol Res. 2004;6: 619–626.

Mikolajewski DJ, Johansson F. Morphological and behavioral defenses in dragonfly larvae: Trait compensation and cospecialization. Behav Ecol. 2004;15: 614–620. 10.1093/beheco/arh061 DOI

Arnqvist G, Johansson F. Ontogenetic reaction norms of predator-induced defensive morphology in dragonfly larvae. Ecology. 1998;79: 1847–1858. 10.1890/0012-9658(1998)079[1847:ORNOPI]2.0.CO;2 DOI

McCauley SJ, Davis CJ, Werner EE. Predator induction of spine length in larval Leucorrhinia intacta (Odonata). Evol Ecol Res. 2008;10: 435–447.

Flenner I, Olne K, Suhling F, Sahlén G. Predator-induced spine length and exocuticle thickness in Leucorrhinia dubia (Insecta: Odonata): A simple physiological trade-off? Ecol Entomol. 2009;34: 735–740. 10.1111/j.1365-2311.2009.01129.x DOI

Petrin Z, Schilling EG, Loftin CS, Johansson F. Predators shape distribution and promote diversification of morphological defenses in Leucorrhinia, Odonata. Evol Ecol. 2010;24: 1003–1016. 10.1007/s10682-010-9361-x DOI

Mikolajewski DJ, Johansson F, Wohlfahrt B, Stoks R. Invertebrate predation selects for the loss of a morphological antipredator trait. Evolution. 2006;60: 1306–1310. 10.1111/j.0014-3820.2006.tb01208.x PubMed DOI

McPeek MA. Behavioral differences between Enallagma species (Odonata) influencing differential vulnerability to predators. Ecology. 1990;71: 1714–1726. 10.2307/1937580 DOI

Mikolajewski DJ, De Block M, Rolff J, Johansson F, Beckerman AP, Stoks R. Predator-driven trait diversification in a dragonfly genus: Covariation in behavioral and morphological antipredator defense. Evolution. 2010;64: 3327–3335. 10.1111/j.1558-5646.2010.01078.x PubMed DOI

Mikolajewski DJ, Rüsen L, Mauersberger R, Johansson F, Rolff J. Relaxed predation results in reduced phenotypic integration in a suite of dragonflies. J Evol Biol. 2015;28: 1354–1363. 10.1111/jeb.12658 PubMed DOI

Johansson F. Reaction norms and production costs of predator-induced morphological defences in a larval dragonfly (Leucorrhinia dubia: Odonata). Can J Zool. 2002;80: 944–950. 10.1139/z02-073 DOI

Pettersson LB, Nilsson PA, Brönmark C. Predator recognition and defence strategies in crucian carp, Carassius carassius. Oikos. 2000;88: 200–212. 10.1034/j.1600-0706.2000.880122.x DOI

Turner AM, Bernot RJ, Boes CM. Chemical cues modify species interactions: The ecological consequences of predator avoidance by freshwater snails. Oikos. 2000;88: 148–158. 10.1034/j.1600-0706.2000.880117.x DOI

Relyea RA. Trait-mediated indirect effects in larval anurans: Reversing competition with the threat of predation. Ecology. 2000;81: 2278–2289. 10.1890/0012-9658(2000)081[2278:TMIEIL]2.0.CO;2 DOI

Relyea RA. How prey respond to combined predators: a review and an empirical test. Ecology. 2003;84: 1827–1839. 10.1890/0012-9658(2003)084[1827:HPRTCP]2.0.CO;2 DOI

Sternberg K, Buchwald R. Die Libellen Baden-Württembergs. Band 2: Großlibellen (Anisoptera). Stuttgart: Verlag Eugen Ulmer Gmbh & Co.; 2000.

Kalkman VJ, Boudot J-P, Bernard R, Conze K-J, De Knijf G, Dyatlova E, et al. European red list of dragonflies. Luxembourg: Publications Office of the European Union; 2010.

Kalkman VJ, Boudot J-P, Bernard R, De Knijf G, Suhling F, Termaat T. Diversity and conservation of European dragonflies and damselflies (Odonata). Hydrobiologia. 2018.

Dolný A, Harabiš F, Bárta D. Vážky (Insecta: Odonata) České republiky. Praha: Academia; 2016.

Dolný A, Harabiš F, Mižičová H. Home range, movement, and distribution patterns of the threatened dragonfly Sympetrum depressiusculum (Odonata: Libellulidae): A thousand times greater territory to protect? PLoS ONE. 2014;9: e100408 10.1371/journal.pone.0100408 PubMed DOI PMC

Šigutová H, Šigut M, Dolný A. Intensive fish ponds as ecological traps for dragonflies: An imminent threat to the endangered species Sympetrum depressiusculum (Odonata: Libellulidae). J Insect Conserv. 2015;19: 961–974. 10.1007/s10841-015-9813-2 DOI

Gerken B, Sternberg K. Die Exuvien Europäischer Libellen (Insecta, Odonata)/The exuviae of European dragonflies. Höxter: Huxaria Druckerei GmbH; 1999.

Dijkstra K-DB, Lewington R. Field guide to the dragonflies of Britain and Europe including western Turkey and northwestern Africa. Gillingham: British Wildlife Publishing; 2006.

Kottelat M, Freyhof J. Handbook of European freshwater fishes. Cornol, Switzerland: Publications Kottelat; 2007.

Akkas SB, Kepenek AO, Beklioglu M, Severcan F. Molecular approach to the chemical characterization of fish-exuded kairomone: A Fourier transform infrared spectroscopic study. Aquat Sci. 2010;72: 71–83. 10.1007/s00027-009-0114-2 DOI

Benke AC, Benke SS. Comparative dynamics and life histories of coexisting dragonfly populations. Ecology. 1975;56: 302–317. 10.2307/1934962 DOI

Suhling F, Sahlén G, Gorb SN, Kalkman VJ, Dijkstra K-DB, van Tol J. Order Odonata In: Thorp J, Rogers DC, editors. Ecology and general biology: Thorp and Covich’s freshwater invertebrates. Academic Press; 2015. pp. 893–932.

Benke AC. A method for comparing individual growth rates of aquatic insects with special reference to Odonata. Ecology. 1970;51: 328–331. 10.2307/1933673 DOI

R Development Core Team. R: A language and environment for statistical computing. The R Foundation for Statistical Computing, Vienna, Austria; 2015. https://www.r-project.org.

Anderson MJ. Distance-based tests for homogeneity of multivariate dispersions. Biometrics. 2006;62: 245–253. 10.1111/j.1541-0420.2005.00440.x PubMed DOI

Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, et al. vegan: Community ecology package. R package version 2.4-; 2016. https://CRAN.R-project.org/package=vegan.

Ter Braak CJF, Šmilauer P. Canoco reference manual and user’s guide: Software for ordination, version 5.0. Ithaca, USA: Microcomputer Power; 2012.

Pinheiro J, Bates D, Debroy S, Sarkar D, R Core Team. nlme: Linear and nonlinear mixed effects models. R package version 3.1–131; 2017. https://CRAN.R-project.org/package=nlme.

Schoeppner NM, Relyea RA. Damage, digestion, and defence: the roles of alarm cues and kairomones for inducing prey defences. Ecol Lett. 2005;8: 505–512. 10.1111/j.1461-0248.2005.00744.x PubMed DOI

Schoeppner NM, Relyea RA. Interpreting the smells of predation: How alarm cues and kairomones induce different prey defences. Funct Ecol. 2009;23: 1114–1121. 10.1111/j.1365-2435.2009.01578.x DOI

Hoverman JT, Relyea RA. Prey responses to fine-scale variation in predation risk from combined predators. Oikos. 2016;125: 254–261. 10.1111/oik.02435 DOI

Hoverman JT, Cothran RD, Relyea RA. Generalist versus specialist strategies of plasticity: Snail responses to predators with different foraging modes. Freshw Biol. 2014;59: 1101–1112. 10.1111/fwb.12332 DOI

McPeek MA. Trade-offs, food web structure, and the coexistence of habitat specialists and generalists. Am Nat. 1996;148: 124–138. 10.1086/285906 DOI

McIntosh AR, Peckarsky BL. Criteria determining behavioural responses to multiple predators by a stream mayfly. Oikos. 1999;85: 554–564. 10.2307/3546705 DOI

Lima SL. Life in a multi-predator environment: some considerations for anti-predatory vigilance. Ann Zool Fenn. 1992;29: 217–226.

Matsuda H, Hori M, Abrams PA. Effects of predator-specific defence on biodiversity and community complexity in two-trophic-level communities. Evol Ecol. 1996;10: 13–28. 10.1007/BF01239343 DOI

Teplitsky C, Plenet S, Joly P. Hierarchical responses of tadpoles to multiple predators. Ecology. 2004;85: 2888–2894. 10.1890/03-3043 DOI

Hoverman JT, Relyea RA. The rules of engagement: How to defend against combinations of predators. Oecologia. 2007;154: 551–560. 10.1007/s00442-007-0847-3 PubMed DOI

Bourdeau PE. Prioritized phenotypic responses to combined predators in a marine snail. Ecology. 2009;90: 165–1669. 10.1890/08-1653.1 PubMed DOI

Pigliucci M. Phenotypic plasticity: Beyond nature and nurture. Baltimore, MD: Johns Hopkins University Press; 2001.

Relyea RA. Integrating phenotypic plasticity when death is on the line In: Pigliucci M, Preston K, editors. Phenotypic integration studying the ecology and evolution of complex phenotypes. Oxford: Oxford University Press; 2004. pp. 176–190.

DeWitt TJ, Sih A, Hucko JA. Trait compensation and cospecialization in a freshwater snail: Size, shape and antipredator behaviour. Anim Behav. 1999;58: 397–407. 10.1006/anbe.1999.1158 PubMed DOI

Cornwallis CK, Birkhead TR. Plasticity in reproductive phenotypes reveals status-specific correlations between behavioral, morphological, and physiological sexual traits. Evolution. 2008;62: 1149–1161. 10.1111/j.1558-5646.2008.00346.x PubMed DOI

Bourdeau PE, Johansson F. Predator-induced morphological defences as by-products of prey behaviour: A review and prospectus. Oikos. 2012;121: 1175–1190. 10.1111/j.1600-0706.2012.20235.x DOI

Snell-Rood EC, van Dyken JD, Cruickshank T, Wade MJ, Moczek AP. Toward a population genetic framework of developmental evolution: The costs, limits, and consequences of phenotypic plasticity. BioEssays. 2010;32: 71–81. 10.1002/bies.200900132 PubMed DOI PMC

Relyea RA. Fine-tuned phenotypes: Tadpole plasticity under 16 combinations of predators and competitors. Ecology. 2004;85: 172–179. 10.1890/03-0169 DOI