Evolutionary Ecology

, Volume 24, Issue 5, pp 1003–1016 | Cite as

Predators shape distribution and promote diversification of morphological defenses in Leucorrhinia, Odonata

  • Zlatko Petrin
  • Emily G. Schilling
  • Cynthia S. Loftin
  • Frank Johansson
Original Paper


Predators strongly influence species assemblages and shape morphological defenses of prey. Interestingly, adaptations that constitute effective defenses against one type of predator may render the prey susceptible to other types of predators. Hence, prey may evolve different strategies to escape predation, which may facilitate adaptive radiation of prey organisms. Larvae of different species in the dragonfly genus Leucorrhinia have various morphological defenses. We studied the distribution of these larvae in relation to the presence of predatory fish. In addition, we examined the variation in morphological defenses within species with respect to the occurrence of fish. We found that well-defended species, those with more and longer spines, were more closely associated with habitats inhabited by predatory fish and that species with weakly developed morphological defenses were more abundant in habitats without fish. The species predominantly connected to lakes with or without fish, respectively, were not restricted to a single clade in the phylogeny of the genus. Our data is suggestive of phenotypic plasticity in morphological defense in three of the studied species since these species showed longer spines in lakes with fish. We suggest that adaptive phenotypic plasticity may have broadened the range of habitats accessible to Leucorrhinia. It may have facilitated colonization of new habitats with different types of predators, and ultimately, speciation through adaptive radiation.


Adaptive phenotypic plasticity Aquatic insects Fish predation Odonates Polyphenism Permutation test 



We thank Michael Andersson, Ida Flenner, Karin Olne, Szymon Śniegula, and Laura Toivanen for help in the field and laboratory. We are grateful to Göran Englund for discussing statistical aspects, Folmer Bokma for helping plot the phylogenetic tree, and Frank Drummond, Kevin Simon, Robby Stoks, Sara Helms Cahan, and the anonymous referees for insightful comments on the manuscript. Maxim Teichert kindly helped improving the language. This study was funded by the Swedish Research Council (to FJ), the Maine Department of Inland Fisheries and Wildlife, the Maine Outdoor Heritage Fund, the National Science Foundation, the USGS-Maine Cooperative Fish and Wildlife Research Unit and University of Maine. Mention of trademarks or commercial products does not imply endorsement by the USA Government.

Supplementary material

10682_2010_9361_MOESM1_ESM.doc (104 kb)
(DOC 104 kb)


  1. Agrawal AA (2001) Phenotypic plasticity in the interactions and evolution of species. Science 294(5541):321–326CrossRefPubMedGoogle Scholar
  2. Arnqvist G, Johansson F (1998) Ontogenetic reaction norms of predator-induced defensive morphology in dragonfly larvae. Ecology 79(6):1847–1858CrossRefGoogle Scholar
  3. Brodin T, Johansson F (2002) Effects of predator-induced thinning and activity changes on life history in a damselfly. Oecologia 132(2):316–322CrossRefGoogle Scholar
  4. Crowder LB, Cooper WE (1982) Habitat structural complexity and the interaction between bluegills and their prey. Ecology 63(6):1802–1813CrossRefGoogle Scholar
  5. Davies DAL, Tobin P (1985) The dragonflies of the world: a systematic list of the extant species of Odonata, vol 2. Anisoptera International Odonatological Society (S.I.O.), UtrechtGoogle Scholar
  6. Edmunds M (1974) Defence in animals. Longman, New YorkGoogle Scholar
  7. Ghalambor CK, McKay JK, Carroll SP, Reznick DN (2007) Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Funct Ecol 21(3):394–407CrossRefGoogle Scholar
  8. Good P (1994) Permutation tests: a practical guide to resampling methods for testing hypotheses. Springer, New YorkGoogle Scholar
  9. Grant JWG, Bayly IAE (1981) Predator induction of crests in morphs of the Daphnia carinata King complex. Limnol Oceanogr 26(2):201–218CrossRefGoogle Scholar
  10. Harvell CD (1986) The ecology and evolution of inducible defenses in a marine bryozoan: cues, costs, and consequences. Am Nat 128(6):810–823CrossRefGoogle Scholar
  11. Hovmöller R, Johansson F (2004) A phylogenetic perspective on larval spine morphology in Leucorrhinia (Odonata: Libellulidae) based on ITS1, 5.8S, and ITS2 rDNA sequences. Mol Phylogenet Evol 30(3):653–662CrossRefPubMedGoogle Scholar
  12. Johansson F (2002) Reaction norms and production costs of predator-induced morphological defences in a larval dragonfly (Leucorrhinia dubia: Odonata). Can J Zool-Revue Canadienne De Zoologie 80(5):944–950CrossRefGoogle Scholar
  13. Johansson F, Brodin T (2003) Effects of fish predators and abiotic factors on dragonfly community structure. J Freshw Ecol 18(3):415–423Google Scholar
  14. Johansson F, Mikolajewski DJ (2008) Evolution of morphological defences. In: Córdoba-Aguilar A (ed) Dragonflies and damselflies: model organisms for ecological and evolutionary research. Oxford University Press, New York, pp 127–137Google Scholar
  15. Johansson F, Samuelsson L (1994) Fish-induced variation in abdominal spine length of Leucorrhinia dubia (Odonata) larvae? Oecologia 100(1–2):74–79CrossRefGoogle Scholar
  16. Johansson F, Wahlström E (2002) Induced morphological defence: evidence from whole-lake manipulation experiments. Can J Zool-Revue Canadienne De Zoologie 80(2):199–206CrossRefGoogle Scholar
  17. Kerfoot WC, Sih A (eds) (1987) Predation: direct and indirect impacts on aquatic communities. University Press of New England, HanoverGoogle Scholar
  18. Legendre P, Gallagher ED (2001) Ecologically meaningful transformations for ordination of species data. Oecologia 129(2):271–280CrossRefGoogle Scholar
  19. Lively CM (1986) Predator-induced shell dimorphism in the acorn barnacle Chthamalus anisopoma. Evolution 40(2):232–242CrossRefGoogle Scholar
  20. Mallory ML, Blancher PJ, Weatherhead PJ, McNicol DK (1994) Presence or absence of fish as a cue to macroinvertebrate abundance in boreal wetlands. Hydrobiologia 280:345–351CrossRefGoogle Scholar
  21. Manly BFJ (2007) Randomization, bootstrap and Monte Carlo methods in biology. Chapman & Hall/CRC, London/Boca RatonGoogle Scholar
  22. Marchinko KB (2009) Predation’s role in repeated phenotypic and genetic divergence of armor in threespine stickleback. Evolution 63(1):127–138CrossRefPubMedGoogle Scholar
  23. McCauley SJ, Davis CJ, Werner EE (2008) Predator induction of spine length in larval Leucorrhinia intacta (Odonata). Evol Ecol Res 10(3):435–447Google Scholar
  24. McNicol DK, Mallory ML, Kerekes JJ (1996) The Canadian Wildlife Service LRTAP Biomonitoring Program, Part 3. Site locations, physical, chemical and biological characteristics. Report nr No. 248, Canadian Wildlife SeriesGoogle Scholar
  25. McPeek MA (1995) Morphological evolution mediated by behavior in the damselflies of two communities. Evolution 49(4):749–769CrossRefGoogle Scholar
  26. Meyer JR, Kassen R (2007) The effects of competition and predation on diversification in a model adaptive radiation. Nature 446(7134):432–435CrossRefPubMedGoogle Scholar
  27. Mikolajewski DJ, Johansson F (2004) Morphological and behavioral defenses in dragonfly larvae: trait compensation and cospecialization. Behav Ecol 15(4):614–620CrossRefGoogle Scholar
  28. Mikolajewski DJ, Rolff J (2004) Benefits of morphological defence demonstrated by direct manipulation in larval dragonflies. Evol Ecol Res 6(4):619–626Google Scholar
  29. Mikolajewski DJ, Johansson F, Wohlfahrt B, Stoks R (2006) Invertebrate predation selects for the loss of a morphological antipredator trait. Evolution 60(6):1306–1310PubMedGoogle Scholar
  30. Moran NA (1992) The evolutionary maintenance of alternative phenotypes. Am Nat 139(5):971–989CrossRefGoogle Scholar
  31. Nosil P, Crespi BJ (2006) Experimental evidence that predation promotes divergence in adaptive radiation. Proc Natl Acad Sci USA 103(24):9090–9095CrossRefPubMedGoogle Scholar
  32. Oksanen J, Kindt R, Legendre P, O’Hara B, Simpson GL, Stevens MHH (2008) Vegan: community ecology package.,, R package version 1.11-4
  33. Pajunen VI (1962) Studies on the population ecology of Leucorrhinia dubia v.d. Linden. Ann Zool Soc Zool Bot Fenn Vanamo 24:1–79Google Scholar
  34. Price TD, Qvarnström A, Irwin DE (2003) The role of phenotypic plasticity in driving genetic evolution. Proc R Soc Lond B Biol Sci 270(1523):1433–1440CrossRefGoogle Scholar
  35. R Development Core Team (2008) R: a language and environment for statistical computing R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0,
  36. Reimchen TE (1980) Spine deficiency and polymorphism in a population of Gasterosteus aculeatus: an adaptation to predators? Can J Zool-Revue Canadienne De Zoologie 58(7):1232–1244CrossRefGoogle Scholar
  37. Reimchen TE, Nosil P (2002) Temporal variation in divergent selection on spine number in threespine stickleback. Evolution 56(12):2472–2483PubMedGoogle Scholar
  38. Schilling EG, Loftin CS, Huryn AD (2009) Macroinvertebrates as indicators of fish absence in naturally fishless lakes. Freshw Biol 54(1):181–202CrossRefGoogle Scholar
  39. Stern DL, Orgogozo V (2009) Is genetic evolution predictable? Science 323(5915):746–751CrossRefPubMedGoogle Scholar
  40. Stoks R, McPeek MA (2006) A tale of two diversifications: reciprocal habitat shifts to fill ecological space along the pond permanence gradient. Am Nat 168(6):S50–S72CrossRefPubMedGoogle Scholar
  41. Tollrian R, Harvell CD (1999) The ecology and evolution of inducible defenses. Princeton University Press, PrincetonGoogle Scholar
  42. Vamosi SM (2005) On the role of enemies in divergence and diversification of prey: a review and synthesis. Can J Zool-Revue Canadienne De Zoologie 83(7):894–910CrossRefGoogle Scholar
  43. Van Buskirk J, Relyea RA (1998) Selection for phenotypic plasticity in Rana sylvatica tadpoles. Biol J Linn Soc 65(3):301–328CrossRefGoogle Scholar
  44. Venables WN, Ripley BD (2002) Modern applied statistics. In: Chambers SJ, Eddy W, Härdle W, Sheather S, Tierney L, (eds) Springer, New YorkGoogle Scholar
  45. Woodward G, Jones JI, Hildrew AG (2002) Community persistence in Broadstone Stream (U.K.) over three decades. Freshw Biol 47(8):1419–1435CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Zlatko Petrin
    • 1
    • 2
  • Emily G. Schilling
    • 3
  • Cynthia S. Loftin
    • 4
  • Frank Johansson
    • 1
  1. 1.Department of Ecology and Environmental ScienceUmeå UniversityUmeåSweden
  2. 2.Norwegian Institute for Nature Research, NINATrondheimNorway
  3. 3.Department of Wildlife EcologyUniversity of MaineOronoUSA
  4. 4.US Geological Survey Maine Cooperative Fish and Wildlife Research UnitUniversity of MaineOronoUSA

Personalised recommendations