Abstract
Adaptive autotomy is the self-amputation of an appendage in response to external stimuli that benefits survival. Variation in the ease of appendage removal among populations suggests that autotomy performance is under selection, evolves, or is phenotypically plastic, although the latter has never been experimentally tested. We model an autotomy threshold that optimally balances how the benefits of surviving predator attack versus the costs of losing an appendage vary with predator presence. We test for functional plasticity in autotomy threshold in the caudal lamellae of Enallagma damselfly larvae by experimentally manipulating non-lethal cues from predatory dragonfly larvae. Predator cues lead to functional plastic responses in the form of smaller lamellar joints that required lower peak breaking force. This is the first experimental demonstration of functional plasticity in autotomy to cues from a grasping predator, a novel form of indirect predator effects on prey, realized through plasticity in morphological traits that govern the autotomy threshold. This supports the model of optimized autotomy performance and provides a novel explanation for variation in performance among populations under different predator conditions. Plastic autotomy responses that mitigate costs in the face of variation in mortality risks might be a form of inducible defense.
This is a preview of subscription content, access via your institution.



Change history
23 March 2020
In the original publication of the article, the sample size reported in the article differs from the sample size in the Electronic Supplementary material 2 dataset. The corrections in the text and the revised supplementary data set are provided in this correction.
23 March 2020
In the original publication of the article, the sample size reported in the article differs from the sample size in the Electronic Supplementary��material 2��dataset.��The corrections in the text and the��revised supplementary data set are provided in this correction.
References
Anholt BR, Werner EE (1995) Interaction between food availability and predation mortality mediated by adaptive behavior. Ecology 76:2230–2234. https://doi.org/10.2307/1941696
Arnold SJ (1983) Morphology, performance, and fitness. Integr Comp Biol 23:347–361. https://doi.org/10.1093/icb/23.2.347
Arnold EN (1984) Evolutionary aspects of tail shedding in lizards and their relatives. J Nat Hist 18:127–169. https://doi.org/10.1080/00222938400770131
Arnold EN (1988) Caudal autotomy as a defense. In: Gans C, Huey RB (eds) Biology of the Reptilia. John Wiley & Sons, New York, pp 235–273
Arnqvist G, Johansson F (1998) Ontogenetic reaction norms of predator-induced defensive morphology in dragonfly larvae. Ecol 79:1847–1858. https://doi.org/10.1890/0012-9658(1998)079%5b1847:ORNOPI%5d2.0.CO;2
Baker RL, Dixon SM (1986) Wounding as an index of aggressive interactions in larval Zygoptera (Odonata). Can J Zool 64:893–897. https://doi.org/10.1139/z86-134
Bateman PW, Fleming PA (2009) To cut a long tail short: a review of lizard caudal autotomy studies carried out over the last 20 years. J Zool 277:1–14. https://doi.org/10.1111/j.1469-7998.2008.00484.x
Bellairs A, Bryant SV (1985) Autotomy and regeneration in reptiles. In: Gans C, Huey RB (eds) Biology of the Reptilia. John Wiley & Sons, New York, pp 301–410
Benard MF (2004) Predator-induced phenotypic plasticity in organisms with complex life histories. Annu Rev Ecol Evol Syst 35:651–673. https://doi.org/10.1146/annurev.ecolsys.35.021004.112426
Berrigan D, Scheiner SM (2004) Modeling the evolution of phenotypic plasticity. In: DeWitt TJ, Scheiner SM (eds) Phenotypic plasticity: Functional and conceptual approaches. Oxford University Press, Oxford, pp 82–89
Bose APH, Robinson BW (2013) Invertebrate predation predicts variation in an autotomy-related trait in larval damselfly. Evol Ecol 27:27–38. https://doi.org/10.1007/s10682-012-9581-3
Bright E, O’Brien MF (1999) Odonata larvae of Michigan: keys for, and notes on, the dragon and damselfly larvae found in the State of Michigan. http://insects.ummz.lsa.umich.edu/MICHODO/test/HOME.HTM (Accessed June 2011)
Brodin T, Mikolajewski DJ, Johansson F (2006) Behavioural and life history effects of predator diet cues during ontogeny in damselfly larvae. Oecologia 148:162–169. https://doi.org/10.1007/s00442-005-0334-7
Brown AL, Robinson BW (2016) Variation in behavioural plasticity regulates consistent individual differences in Enallagma damselfly larvae. Anim Behav 112:63–73. https://doi.org/10.1016/j.anbehav.2015.11.0180003-3472
Burnside CA, Robinson JV (1995) The functional morphology of caudal lamellae in coenagrionid (Odonata: Zygoptera) damselfly larvae. Zool J Linn Soc 114:155–171. https://doi.org/10.1006/zjls.1995.0022
Chivers DP, Smith RJF (1998) Chemical alarm signaling in aquatic predator-prey systems: a review and prospectus. Ecoscience 5:338–352. https://doi.org/10.1080/11956860.1998.11682471
Chivers DP, Wisenden BD, Smith RJF (1996) Damselfly larvae learn to recognize predators from chemical cues in the predator’s diet. Anim Behav 52:315–320. https://doi.org/10.1006/anbe.1996.0177
Clarac F, Wales W, Laverack MS (1971) Stress detection at the autotomy plane in the decapod crustacea. J Comp Physiol 73:383–407. https://doi.org/10.1007/BF00297954
Clause AR, Capaldi EA (2006) Caudal autotomy and regeneration in lizards. J Exp Zool 305A:965–973. https://doi.org/10.1002/jez.a.34
Congdon JD, Vitt LJ, King WW (1974) Geckos: adaptive significance and energetics of tail autotomy. Science 184:1379–1380. https://doi.org/10.1126/science.184.4144.1379
Cooper WE, Frederick WG (2010) Predator lethality, optimal escape behavior, and autotomy. Behav Ecol 21:91–96. https://doi.org/10.1093/beheco/arp151
Cooper WE, Vitt LJ (1991) Influence of detectability and ability to escape on natural selection of conspicuous autotomous defenses. Can J Zool 69:757–764. https://doi.org/10.1139/z91-109
Cooper WE, Pérez-Mellado V, Vitt LJ (2004) Ease and effectiveness of costly autotomy vary with predation intensity among lizard populations. J Zool 262:243–255. https://doi.org/10.1017/S095283690300462X
Dial BE, Fitzpatrick LC (1981) The energetic costs of tail autotomy to reproduction in the lizard Coleonyx brevis (Sauria: Gekkonidae). Oecologia 51:310–317. https://doi.org/10.1007/BF00540899
Dixon SM, Baker RL (1988) Effects of size on predation risk, behavioural response to fish, and cost of reduced feeding in larval Ischnura verticalis (Coenagrionidae: Odonata). Oecologia 76:200–205. https://doi.org/10.1007/BF00379953
Eriksen CH (1986) Respiratory roles of caudal lamellae (gills) in a Lestid damselfly (Odonata: Zygoptera). J N Am Benthol Soc 5:16–27. https://doi.org/10.2307/1467744
Fleming PA, Muller D, Bateman PW (2007) Leave it all behind: a taxonomic perspective of autotomy in invertebrates. Biol Rev 82:481–510. https://doi.org/10.1111/j.1469-185X.2007.00020.x
Flenner I, Olne K, Suhling F, Salen G (2009) Predator-induced spine length and exocuticle thickness in Leucorrhinia dubia (Insecta: Odonata): a simple physiological trade-off? Ecol Entomol 34:735–740. https://doi.org/10.1111/j.1365-2311.2009.01129.x
Gleason JE, Fudge DS, Robinson BW (2014) Eco-mechanics of lamellar autotomy in larval damselflies. J Exp Biol 217:185–191. https://doi.org/10.1242/jeb.091827
Gyssels FGM, Stoks R (2005) Threat-sensitive responses to predator attacks in a damselfly. Ethology 111:411–423. https://doi.org/10.1111/j.1439-0310.2005.01076.x
Hopkins TL, Kramer KJ (1992) Insect cuticle sclerotization. Annu Rev Entomol 37:273–302. https://doi.org/10.1146/annurev.en.37.010192.001421
Ingram BR, Jenner EE (1976) Life histories of Enallagma hageni (Walsh) and E. aspersum (Hagen) (Zygoptera: Coenagrionidae). Odonatologica 5:331–345
Johansson F (2002) Reaction norms and production costs of predator-induced morphological defences in a larval dragonfly (Leucorrhinia dubia: Odonata). Can J Zool 80:944–950. https://doi.org/10.1139/Z02-073
Johansson F, Stoks R (2005) Adaptive plasticity in response to predators in dragonfly larvae and other aquatic insects. In: Fellowes MDE, Holloway GJ, Rolff J (eds) Insect evolutionary ecology. CABI Publishing, Cambridge, pp 347–368
Johnson DM (1991) Behavioural ecology of larval dragonflies and damselflies. TREE 6:8–13. https://doi.org/10.1016/0169-5347(91)90140-S
Koperski P (1997) Changes in feeding behaviour of the larvae of the damselfly Enallagma cyathigerum in response to stimuli from predators. Ecol Entomol 22:167–175. https://doi.org/10.1046/j.1365-2311.1997.00058.x
Kormondy EJ, Gower JL (1965) Life history variation in an association of Odonata. Ecology 46:882–886
Legrand J (1974) Étude comparative de l’autotomie chez les larves de zygoptères (Odon.). Ann Soc Entomol Fr 10:635–646
Lima SL, Dill LM (1990) Behavioural decisions made under the risk of predation: a review and prospectus. Can J Zool 68:619–640. https://doi.org/10.1139/z90-092
Maginnis TL (2006) The costs of autotomy and regeneration in animals: a review and framework for future research. Behav Ecol 17:857–872. https://doi.org/10.1093/beheco/arl010
Matthews LM, McKnight AE, Avery R, Lee KT (1999) Incidence of autotomy in New England populations of green crabs, Carcinus maenas, and an examination of the effect of claw autotomy on diet. J Crustac Biol 19:713–719. https://doi.org/10.2307/1549295
McCauley SJ, Rowe L, Fortin M (2011) The deadly effects of “nonlethal” predators. Ecology 92:2043–2048. https://doi.org/10.1890/11-0455.1
McGuffin MA, Baker RL, Forbes MR (2006) Detection and avoidance of fish predators by adult Enallagma damselflies. J Insect Behav 19:77–91. https://doi.org/10.1007/s10905-005-9013-0
McPeek MA (1989) Differential dispersal tendencies among Enallagma damselflies (Odonata) inhabiting different habitats. Oikos 56:187–195. https://doi.org/10.2307/3565335
McPeek MA (1990a) Behavioural differences between Enallagma species (Odonata) influencing differential vulnerability to predators. Ecology 71:1714–1726. https://doi.org/10.2307/1937580
McPeek MA (1990b) Determination of species composition in the Enallagma damselfly assemblages of permanent lakes. Ecology 71:83–98. https://doi.org/10.2307/1940249
McPeek MA (1997) Measuring phenotypic selection on an adaptation: lamellae of damselflies experiencing dragonfly predation. Evolution 51:459–466. https://doi.org/10.1111/j.1558-5646.1997.tb02433.x
McPeek MA (2004) The growth/predation risk trade-off: So what is the mechanism? Am Nat 163:88–111. https://doi.org/10.1086/382755
McPeek MA, Schrot AK, Brown JM (1996) Adaptation to predators in a new community: swimming performance and predator avoidance in damselflies. Ecology 77:617–629. https://doi.org/10.2307/2265635
McPeek MA, Grace M, Richardson JML (2001) Physiological and behavioural responses to predators shape the growth/predation risk trade-off in damselflies. Ecology 82:1535–1545. https://doi.org/10.1890/0012-9658(2001)082%5b1535:PABRTP%5d2.0.CO;2
McVean AR (1973) Autotomy in Carcinus maenas (Decapoda: Crustacea). J Zool 169:349–364. https://doi.org/10.1111/j.1469-7998.1973.tb04561.x
McVean AR (1976) The incidence of autotomy in Carcinus maenas (L.). J Exp Mar Biol Ecol 24:177–187. https://doi.org/10.1016/0022-0981(76)90102-7
Mortenson L, Richardson JML (2008) Effects of chemical cues on foraging in damselfly larvae, Enallagma antennatum. J Insect Behav 21:285–295. https://doi.org/10.1007/s10905-008-9125-4
Naya DE, Veloso C, Muñoz JLP, Bozinovic F (2007) Some vaguely explored (but not trivial) costs of tail autotomy in lizards. Comp Biochem Phys A 146:189–193. https://doi.org/10.1016/j.cbpa.2006.10.014
Pressier EL, Bolnick DI, Benard MF (2005) Scared to death? The effects of intimidation and consumption in predator-prey interactions. Ecology 86:501–509. https://doi.org/10.1890/04-0719
Robinson MH, Abele LG, Robinson B (1970) Attack autotomy: a defense against predators. Science 169:300–301
Robinson JV, Hayworth DA, Harvey MB (1991a) The effect of caudal lamellae loss on swimming speed of the damselfly Argia moesta (Hagen) (Odonata: Coenagrionidae). Am Midl Nat 125:240–244. https://doi.org/10.2307/2426228
Robinson JV, Shaffer LR, Hagemeier DD, Smatresk NJ (1991b) The ecological role of lamellae loss in the larval damselfly, Ischnura posita (Hagen) (Odonata: Zygoptera). Oecologia 87:1–7. https://doi.org/10.1007/BF00323773
Sapolsky RM (2002) Endocrinology of the stress-response. In: Becker JB, Breedlove SM, Crews D, McCarthy MM (eds) Behavioral endocrinology. MIT Press, Cambridge, pp 409–450
Seifert A, Kiama SG, Seifert MG, Goheen JR, Palmer TM, Maden M (2012) Skin shedding and tissue regeneration in African spiny mice (Acomys). Nature 489:561–565. https://doi.org/10.1038/nature11499
Slos S, Stoks R (2008) Predation risk induces stress proteins and reduces antioxidant defense. Funct Ecol 22:637–642. https://doi.org/10.1111/j.1365-2435.2008.01424.x
Smith DL (1990) Patterns of limb loss in the blue crab, Callinectes Sapidus Rathbun, and the effects of autotomy on growth. Bull Mar Sci 46:23–36
Sokolova IM, Frederich M, Bagwa R, Lannig G, Sukhotin AA (2012) Energy homeostasis as an integrative tool for assessing limits of environmental stress tolerance in aquatic invertebrates. Mar Environ Res 79:1–15. https://doi.org/10.1016/j.marenvres.2012.04.003
Sorensen JG, Kristensen TN, Loeschcke V (2003) The evolutionary and ecological role of heat shock proteins. Ecol Lett 6:1025–1037. https://doi.org/10.1046/j.1461-0248.2003.00528.x
Stoks R (1998) Effect of lamellae autotomy on survival and foraging success of the damselfly Lestes sponsa (Odonata: Lestidae). Oecologia 117:443–448. https://doi.org/10.1007/s004420050679
Stoks R (1999a) The effect of lamellae autotomy and sexual size dimorphism on startle-response performance in larvae of a lestid damselfly (Odonata). J Zool 247:269–273. https://doi.org/10.1111/j.1469-7998.1999.tb00990.x
Stoks R (1999b) Autotomy shapes the trade-off between seeking cover and foraging in larval damselflies. Behav Ecol Sociobiol 47:70–75. https://doi.org/10.1007/s002650050651
Stoks R (2001) Food stress and predator-induced stress shape developmental performance in a damselfly. Oecologia 127:222–229. https://doi.org/10.1007/s004420000595
Stoks R, De Block M, Van Gossum H, Valck F, Lauwers K, Verhagen R, Matthysen E, De Bruyn L (1999) Lethal and sublethal costs of autotomy and predator presence in damselfly larvae. Oecologia 120:87–91. https://doi.org/10.1007/s004420050836
Stoks R, De Block M, McPeek MA (2005) Alternative growth and energy storage responses to mortality threats in damselflies. Ecol Lett 8:1307–1316. https://doi.org/10.1111/j.1461-0248.2005.00840.x
Strobbe F, McPeek MA, De Block M, Stoks R (2011) Behav Ecol Sociobiol 65:241–247. https://doi.org/10.1007/s00265-010-1032-y
Turgeon J, McPeek MA (2002) Phylogeographic analysis of a recent radiation of Enallagma damselflies (Odonata: Coenagrionidea). Mol Ecol 11:1989–2001. https://doi.org/10.1046/j.1365-294X.2002.01580.x
Wasson K, Lyon BE, Knope M (2002) Hair-trigger autotomy in porcelain carbs is a highly effective escape strategy. Behav Ecol 13:481–486. https://doi.org/10.1093/beheco/13.4.481
Whitman DW, Agrawal AA (2009) What is phenotypic plasticity and why is it important? In: Whitman DW, Ananthakrishnan TN (eds) Phenotypic plasticity of insects: mechanism and consequences. Science Publishers, Enfield, pp 1–63
Wisenden BD, Chivers DP, Smith RJF (1997) Learned recognition of predation risk by Enallagma damselfly larvae (Odonata, Zygoptera) on the basis of chemical cues. J Chem Ecol 23:137–150. https://doi.org/10.1023/B:JOEC.0000006350.66424.3d
Acknowledgements
J. Gleason advised on tensile testing and SEM, and A. Brown, V. Corbin, N. Deveau, C. Rosa, E. Matczak, M. Tregenza, J. Seery, and J. Stiles assisted field sampling or provided for animal care during the experiment. We are grateful for discussions with R. McLaughlin, A. McAdam, C. Axelrod and D. Gislason that assisted model development, and to comments from two anonymous reviewers that improved the manuscript. This study was supported by Discovery Grants from the Natural Sciences and Engineering Research Council of Canada [RGPIN-2014-04455 to BWR, and RGPIN-2016-04967 to DSF].
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflicts of interest.
Ethical approval
Animals were cared for in accordance with animal use and welfare standards administered by the University of Guelph under Canadian government guidelines (UAREB No. 1500).
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Black, K.L., Fudge, D., Jarvis, W.M.C. et al. Functional plasticity in lamellar autotomy by larval damselflies in response to predatory larval dragonfly cues. Evol Ecol 33, 257–272 (2019). https://doi.org/10.1007/s10682-019-09979-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10682-019-09979-y
Keywords
- Autotomy
- Self-amputation
- Enallagma damselflies
- Predator indirect effects
- Inducible-defense
- Phenotypic plasticity
- Evolution