Skip to main content
Log in

Wing shape-mediated carry-over effects of a heat wave during the larval stage on post-metamorphic locomotor ability

  • Global change ecology – original research
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Two key insights to better assess the ecological impact of global warming have been poorly investigated to date: global warming effects on the integrated life cycle and effects of heat waves. We tested the effect of a simulated mild (25 °C) and severe (30 °C) heat wave experienced during the larval stage on the flight ability of the damselfly Ischnura elegans. To get a mechanistic understanding of how heat stress may translate into reduced post-metamorphic flight ability, we evaluated the hypothesized mediatory role of adult size-related traits, and also tested alternative pathways operating through changes in wing shape and two flight-related traits (both relative fat and flight muscle contents). Exposure to a heat wave, and particularly the severe one, shortened the larval stage, reduced adult size-related traits and modified the wing shape but did not significantly affect emergence success, relative fat content and relative flight muscle mass. Notably, the heat wave negatively affected all components of flight ability. Unexpectedly, the heat wave did not reduce flight ability through reducing size. Instead, we identified a novel size-independent mechanism bridging metamorphosis to link larval environment and adult flight ability in males: through affecting wing shape. The present study advances mechanistic insights in the still poorly understood coupling of life stages across metamorphosis. Additionally, our results underscore the need for integrative studies across life stages to understand the impact of global warming.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Adams DC, Otárola-Castillo E (2013) Geomorph: an R package for the collection and analysis of geometric morphometric shape data. Methods Ecol Evol 4:393–399

    Article  Google Scholar 

  • Alvarez D, Nicieza AG (2002) Effects of induced variation in anuran larval development on postmetamorphic energy reserves and locomotion. Oecologia 131:186–195

    Article  Google Scholar 

  • Anholt BR (1992) Sex and habitat differences in feeding by an adult damselfly. Oikos 65:428–432

    Article  Google Scholar 

  • Arambourou H, Beisel JN, Branchu P, Debat V (2014) Exposure to sediments from polluted rivers has limited phenotypic effects on larvae and adults of Chironomus riparius. Sci Total Environ 484:92–101

    Article  CAS  PubMed  Google Scholar 

  • Atkinson D (1994) Temperature and organism size-a biological law for ectotherms? Adv Ecol Res 25:1–58

    Article  Google Scholar 

  • Aytekin S, Aytekin AM, Alten B (2009) Effect of different larval temperature on the productivity (Ro) and morphology of the malaria vector Anopheles superpictus Grassi (Diptera: Culicidae) using geometric morphometrics. J Vector Ecol 34:32–42

    Article  PubMed  Google Scholar 

  • Bauerfeind SS, Fischer K (2013) Increased temperature reduces herbivore host-plant quality. Glob Change Biol 19:3272–3282

    Google Scholar 

  • Beenakkers A, Van der Horst D, Van Marrewijk W (1984) Insect flight muscle metabolism. Insect Biochem 4:243260

    Google Scholar 

  • Beirinckx K, Van Gossum H, Lajeunnesse MJ, Forbes MR (2006) Sex biases in dispersal and philopatry: insights from a meta-analysis based on capture-mark-recapture studies of damselflies. Oikos 113:539–547

    Article  Google Scholar 

  • Benard MF, McCauley SJ (2008) Integrating across life-history stages: consequences of natal habitat effects on dispersal. Am Nat 171:553–567

    PubMed  Google Scholar 

  • Berg MP, Kiers ET, Driessen G, Van der Heijden M, Kooi BW, Kuenen F, Liefting M, Verhoef HA, Ellers J (2010) Adapt or disperse: understanding species persistence in a changing world? Glob Change Biol 16:587–598

    Article  Google Scholar 

  • Berwaerts K, van Dyck H, Aerts P (2002) Does flight morphology relate to flight performance? An experimental test with the butterfly Pararge aegeria. Funct Ecol 16:484–491

    Article  Google Scholar 

  • Betts CR, Wootton RJ (1988) Wing shape and flight behaviour in butterflies Lepidoptera: Papilionoidea and Hesperioidea. A preliminary analysis. J Exp Biol 138:271–288

    Google Scholar 

  • Biro PA, Beckmann C, Stamps JA (2009) Small within-day increases in temperature affects boldness and alters personality in coral reef fish. Proc R Soc B 277:71–77

    Article  PubMed  PubMed Central  Google Scholar 

  • Bookstein FL (1991) Morphometric tools for landmark data: geometry and biology. Cambridge University Press, Cambridge/New York/Port Chester/Melbourne/Sydney

    Google Scholar 

  • Bookstein FL, Streissguth AP, Sampson PD, Connor PD, Barr HM (2002) Corpus calosum shape and neuropsychological deficits in adult males with heavy fetal alcohol exposure. NeuroImage 15:233–251

    Article  PubMed  Google Scholar 

  • Bouchard SS, O’Leary CJ, Wargelin LJ, Charbonnier JF, Warkentin KM (2015) Post-metamorphic carry-over effects of larval digestive plasticity. Funct Ecol 30:379–388

    Article  Google Scholar 

  • Breuker CP, Patterson JS, Klingenberg CP (2006) A single basis for developmental buffering of Drosophila wing shape. PLoS One 1:e7

    Article  PubMed  PubMed Central  Google Scholar 

  • Breuker CP, Brakefield PM, Gibbs M (2007) The association between wing morphology and dispersal is sex-specific in the glanville fritillary butterfly Melitataea cinxia (Lepidoptera: Nymphalidae). Eur J Entomol 104:445–452

    Article  Google Scholar 

  • Brooks RT (2009) Potential impacts of global climate change on the hydrology and ecology of ephemeral freshwater systems of the forests of the northeastern United States. Clim Change 95:469–483

    Article  Google Scholar 

  • Cooper WE (2000) Effect of temperature on escape behaviour by an ectothermic vertebrate, the keeled earless lizard Holbrookia propinqua. Behaviour 10:1299–1315

    Article  Google Scholar 

  • Corbet PS (1999) Dragonflies: behavior and ecology of Odonata. Harley Books, Colchester, p 830

    Google Scholar 

  • David J, Legout H, Moreteau B (2006) Phenotypic plasticity of body size in a temperate population of Drosophila melanogaster. J Genetics 85:9–23

    Article  Google Scholar 

  • De Block M, Stoks R (2003) Adaptive sex-specific life history plasticity to temperature and photoperiod in a damselfly. J Evol Biol 16:986–995

    Article  PubMed  Google Scholar 

  • De Block M, Stoks R (2005) Fitness effects from egg to reproduction: bridging the life-history transition. Ecology 86:185–197

    Article  Google Scholar 

  • Debat V, Béagin M, Legout H, David J (2003) Allometric and nonallometric components of Drosophila wing shape respond differently to developmental temperature. Evolution 57:2773–2784

    Article  PubMed  Google Scholar 

  • Debecker S, Sommaruga R, Maes T, Stoks R (2015) Larval UV exposure impairs adult immune function through a trade-off with larval investment in cuticular melanin. Funct Ecol 29:1292–1299

    Article  Google Scholar 

  • DeVries PJ, Penz CM, Hill RI (2010) Vertical distribution, flight behaviour and evolution of wing morphology in Morpho butterflies. J Anim Ecol 79:1077–1085

    Article  CAS  PubMed  Google Scholar 

  • Diffenbaugh NS, Field CB (2013) Changes in ecologically critical terrestrial climate conditions. Science 341:486–492

    Article  CAS  PubMed  Google Scholar 

  • Dillon ME, Cahn LRY, Huey RB (2007) Life history consequences of temperature transients in Drosophila melanogaster. J Exp Biol 210:2897–2904

    Article  PubMed  Google Scholar 

  • Dinh VK, Janssens L, Stoks R (2016) Exposure to a heat wave under food limitation makes an agricultural insecticide lethal: a mechanistic laboratory experiment. Glob Change Biol 22:3361–3372

    Article  Google Scholar 

  • Dudley R (2000) The biomechanics of insect flight: form, function, evolution. Princeton University Press, Princeton

    Google Scholar 

  • Forster J, Hirst AG, Atkinson D (2012) Warming-induced reductions in body size are greater in aquatic than terrestrial species. Proc Natl Acad Sci USA 109:19310–19314

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Frazier MR, Harrison JF, Kirkton SD, Roberts SP (2008) Cold rearing improves cold-flight performance in Drosophila via changes in wing morphology. J Exp Biol 211:2116–2122

    Article  PubMed  Google Scholar 

  • Gilchrist AS, Azevedo RBR, Partridge L, O’higgins P (2000) Adaptation and constraint in the evolution of Drosophila melanogaster wing shape. Evol Dev 2:114–124

    Article  CAS  PubMed  Google Scholar 

  • Gyulavári H, Therry L, Dévai G, Stoks R (2014) Sexual selection on flight endurance, flight related morphology and physiology in a scrambling damselfly. Evol Ecol 28:639–654

    Article  Google Scholar 

  • Haenlein MH, Kaplan AM (2004) A beginner’s guide to partial least square analysis. Underst Stat 3:283–297

    Article  Google Scholar 

  • Hassall T, Thompson D (2008) The effects of environmental warming on Odonata: a review. Int J Odonatol 11:131–153

    Article  Google Scholar 

  • Haunerland NH (1997) Transport and utilization of lipids in insect flight muscles. Comp Biochem Physiol B: Biochem Mol Biol 117:475–482

    Article  Google Scholar 

  • Hickling A, Roy DB, Hill J, Thomas CD (2005) A northward shift of range margins in British Odonata. Glob Change Biol 11:502–506

    Article  Google Scholar 

  • Hoffmann AA, Shirriffs J (2002) Geographic variation for wing shape in Drosophila serrata. Evolution 56:1068–1073

    Article  PubMed  Google Scholar 

  • Hoffmann AA, Collins E, Woods R (2002) Wing shape and wing size as indicators of environmental stress in Helicoverpa punctigera Lepidoptera: Noctuidae. moths: comparing shifts in means, variances, and asymmetries. Physiol Chem Ecol 31:965–971

    Google Scholar 

  • Hoffmann AA, Woods R, Collins E, Wallin K, White A, McKenzie J (2005) Wing shape versus asymmetry as an indicator of changing environmental conditions in insects. Aust J Entomol 44:233–243

    Article  Google Scholar 

  • IPCC (2013) Climate change 2013: The physical science basis. University Press, Cambridge, United Kingdom and New York, Cambridge

    Google Scholar 

  • Janssens L, Van Dinh K, Stoks R (2014) Extreme temperatures in the adult stage shape delayed effects of larval pesticide stress: a comparison between latitudes. Aquat Toxicol 148:74–82

    Article  CAS  PubMed  Google Scholar 

  • Johnson CG (1966) A functional system of adaptive dispersal by flight. Annu Rev Entomol 11:233–260

    Article  Google Scholar 

  • Karan D, Morin JP, Gibert P, Moreteau B, Scheiner SM, David JR (2000) The genetics of phenotypic plasticity. IX. Genetic architecture, temperature, and sex differences in Drosophila melanogaster. Evolution 54:1035–1040

    Article  CAS  PubMed  Google Scholar 

  • Kingsolver JG, Woods HA, Buckley LB, Potter KA, MacLean HJ, Higgings JK (2011) Complex life cycles and the responses of insects to climate change. Integr Comp Biol 51:719–732

    Article  PubMed  Google Scholar 

  • Kingsolver JG, Diamond SE, Buckley LB (2013) Heat stress and the fitness consequences of climate change for terrestrial ectotherms. Funct Ecol 27:1415–1423

    Article  Google Scholar 

  • Kjærsgaard A, Andersen DH, Pertoldi C, David JR, Loeschcke V (2007) Effects of temperature and maternal and granmaternal age on wing shape in parthenogenetic Drosophila mercatorum. J Therm Biol 32:59–65

    Article  Google Scholar 

  • Krishnan J, Williams LJ, McIntosh AR, Abdi H (2011) Partial least squares (PLS) methods for neuroimaging: a tutorial and review. NeuroImage 56:455–475

    Article  PubMed  Google Scholar 

  • Kuchta SR, Svensson EI (2014) Predator-Mediated natural selection on the wings of the damselfly Calopteryx splendens: differences in selection among trait types. Am Nat 184:91–109

    Article  PubMed  Google Scholar 

  • Lake Flake model (2014) Available: http://www.flake.igb-berlin.de/index.shtml. Accessed 20 Mar 2014

  • Manfreda E, Mitteroecker P, Bookstein FL, Schaefer K (2006) Functional morphology of the first cervical vertebra in humans and nonhuman primates. Anat Record 289B:184–194

    Article  Google Scholar 

  • Marden J (1989) Bodybuilding dragonflies: costs and benefits of maximizing flight muscle. Physiol Zool 62:505–521

    Article  Google Scholar 

  • McCauley S, Mabry K (2011) Climate change, body size, and phenotype dependent dispersal. Trends Ecol Evol 26:554–555

    Article  PubMed  Google Scholar 

  • McIntosh AR, Lobaugh NJ (2004) Partial least square analysis of neuroimaging data: applications and advances. NeuroImage 23:250–563

    Article  Google Scholar 

  • Meehl G, Tebaldi C (2004) More intense, more frequent, and longer lasting heat waves in the 21st Century. Science 305:994–997

    Article  CAS  PubMed  Google Scholar 

  • Nilsson-Örtman V, Stoks R, De Block M, Johansson F (2012) Generalists and specialists along a latitudinal transect: patterns of thermal adaptation in six species of damselflies. Ecology 93:1340–1352

    Article  PubMed  Google Scholar 

  • Norberg UM (1995) How a long tail and changes in mass and wing shape affect the cost for flight in animals. Funct Ecol 9:48–54

    Article  Google Scholar 

  • Orizaola G, Laurila A (2009) Microgeographic variation in the effects of larval temperature environment on juvenile morphology and locomotion in the pool frog. J Zool 277:267–274

    Article  Google Scholar 

  • Outomuro D, Johansson F (2015) Bird predation selects for wing shape and coloration in a damselfly. J Evol Biol 28:791–799

    Article  CAS  PubMed  Google Scholar 

  • Outomuro D, Adams DC, Johansson F (2013) Wing shape allometry and aerodynamics in calopterygid damselflies: a comparative approach. BMC Evol Biol 13:118

    Article  PubMed  PubMed Central  Google Scholar 

  • Outomuro D, Söderquist L, Nilsson-Örtman V, Cortázar-Chinarro M, Lundgren C, Johansson F (2016) Antagonistic natural and sexual selection on wing shape in a scrambling damselfly. Evolution 70–7:1582–1595

    Article  Google Scholar 

  • Pechenik JA (2006) Larval experience and latent effects—metamorphosis is not a new beginning. Integr Comp Biol 46:323–333

    Article  PubMed  Google Scholar 

  • Prather CM, Pelini SL, Laws A, Rivest E, Woltz M, Bloch CP, Del Toro I, Ho CK, Kominoski J, Scott Newbold TA, Parsons S, Joern A (2013) Invertebrates, ecosystem services and climate change. Biol Rev 88:327–348

    Article  PubMed  Google Scholar 

  • Pulcini D, Costa C, Aguzzi J, Cataudella S (2008) Light and shape: a contribution to demonstrate morphological differences in diurnal and nocturnal teleosts. J Morphol 269:375–395

    Article  PubMed  Google Scholar 

  • R Development Core Team (2014) R: a language and environment for statistical computing. Vienna: R foundation for statistical computing. http://www.R-project.org

  • Radchuk V, Turlure C, Schtickzelle N (2013) Each life stage matters: the importance of assessing the response to climate change over the complete life cycle in butterflies. J Anim Ecol 82:275–285

    Article  PubMed  Google Scholar 

  • Rohlf F, Corti M (2000) Use of two-block partial least squares to study covariation in shape. Syst Biol 49:740–753

    Article  CAS  PubMed  Google Scholar 

  • Rohlf F, Slice D (1990) Extensions of the Procrustes method for the optimal superimposition of landmarks. Syst Zool 39:40–59

    Article  Google Scholar 

  • Roth O, Kurtz J, Reusch T (2010) A summer heat wave decreases the immunocompetence of the mesograzer, Idotea baltica. Mar Biol 157:1605–1611

    Article  Google Scholar 

  • Sacktor B (1970) Regulation of intermediary metabolism, with special reference to the control mechanisms in insect flight muscle. Adv Insect Physiol 7:267–347

    Article  CAS  Google Scholar 

  • Sentis A, Hemptinne JL, Brodeur J (2013) Effects of simulated heat waves on an experimental plant–herbivore-predator food chain. Glob Change Biol 19:833–842

    Article  Google Scholar 

  • Seppälä O, Jokela J (2011) Immune defence under extreme ambient temperature. Biol Lett 7:119–122

    Article  PubMed  Google Scholar 

  • Simmons A, Uppala S, Dee D, Kobayashi S (2007) ERA-interim: new ECMWF reanalysis products from 1989 onwards. ECMWF Newslett 110:25–35

    Google Scholar 

  • Sokolovska N, Rowe L, Johansson F (2000) Fitness and body size in mature odonates. Ecolo Entomol 25:239–248

    Article  Google Scholar 

  • Starmer WT, Wolf MM (1989) Causes of variation of wing loading among Drosophila species. Biol J Linn Soc 37:247–261

    Article  Google Scholar 

  • Stoks R, Córdoba-Aguilar A (2012) Evolutionary ecology of Odonata: a complex life cycle perspective. Ann Rev Entomol 57:249–265

    Article  CAS  Google Scholar 

  • Swillen I, De Block M, Stoks R (2009) Morphological and physiological sexual selection targets in a territorial damselfly. Ecol Entomol 34:677–683

    Article  Google Scholar 

  • Therry L, Gyulavári HA, Schillewaert S, Bonte D, Stoks R (2014) Integrating large-scale geographic patterns in flight morphology, flight characteristics and sexual selection in a range-expanding damselfly. Ecography 37:1012–1021

    Article  Google Scholar 

  • Thompson R, Beardall J, Beringer J, Grace M, Sardina P (2013) Means and extremes: building variability into community-level climate change experiments. Ecol Lett 16:799–806

    Article  PubMed  Google Scholar 

  • Travis JMJ, Delgado M, Bocedi G, Baguette M, Barton K, Bonte D, Boulangeat I, Hodgson JA, Kubisch A, Penteriani V, Saastamoinen M, Stevens VM, Bullock JM (2013) Dispersal and species’ responses to climate change. Oikos 122:1532–1540

    Article  Google Scholar 

  • Vasseur DA, DeLong JP, Gilbert B, Greig HS, Harley CDG, McCann KS, Savage V, Tunney TD, O’Connor MI (2014) Increased temperature variation poses a greater risk to species than climate warming. Proc R Soc B 281:20132612

    Article  PubMed  PubMed Central  Google Scholar 

  • Wakeling J, Ellington C (1997) Dragonfly flight. III. Lift and power requirements. J Exp Biol 200:583–600

    PubMed  Google Scholar 

  • Walther GR, Post E, Convey P, Menzel A, Permesan C, Beebee TJC, Fromentin JM, Hoegh-Guldberg O, Bairlein F (2002) Ecological responses to recent climate change. Nature 416:389–395

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank an anonymous reviewer and the associate editor for constructive feedback that improved our manuscript. HA was supported by the French Ministry of Ecology, Sustainable Development and Energy and by the French National Research Institute of Science and Technology for Environment and Agriculture. ISV was supported by a FPI grant of the Spanish Ministry (BES-2012-052005). Financial support for this research came from grants of FWO, Belspo project Speedy and the KU Leuven Centre of Excellence program PF/2010/07 to RS.

Author contribution statement

HA, ISV and RS conceived and designed the experiments. HA and ISV performed the experiments. HA analyzed the data. HA, ISV and RS wrote the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Hélène Arambourou.

Additional information

Communicated by Joel Trexler.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 16 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Arambourou, H., Sanmartín-Villar, I. & Stoks, R. Wing shape-mediated carry-over effects of a heat wave during the larval stage on post-metamorphic locomotor ability. Oecologia 184, 279–291 (2017). https://doi.org/10.1007/s00442-017-3846-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-017-3846-z

Keywords

Navigation