Advertisement

Oecologia

, Volume 184, Issue 1, pp 279–291 | Cite as

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

  • Hélène Arambourou
  • Iago Sanmartín-Villar
  • Robby Stoks
Global change ecology – original research

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.

Keywords

Carry-over effects Heat stress Geometric morphometrics Temperature-size rule Wing shape 

Notes

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.

Supplementary material

442_2017_3846_MOESM1_ESM.docx (16 kb)
Supplementary material 1 (DOCX 16 kb)

References

  1. Adams DC, Otárola-Castillo E (2013) Geomorph: an R package for the collection and analysis of geometric morphometric shape data. Methods Ecol Evol 4:393–399CrossRefGoogle Scholar
  2. Alvarez D, Nicieza AG (2002) Effects of induced variation in anuran larval development on postmetamorphic energy reserves and locomotion. Oecologia 131:186–195CrossRefGoogle Scholar
  3. Anholt BR (1992) Sex and habitat differences in feeding by an adult damselfly. Oikos 65:428–432CrossRefGoogle Scholar
  4. 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 484:92–101CrossRefPubMedGoogle Scholar
  5. Atkinson D (1994) Temperature and organism size-a biological law for ectotherms? Adv Ecol Res 25:1–58CrossRefGoogle Scholar
  6. 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 34:32–42CrossRefPubMedGoogle Scholar
  7. Bauerfeind SS, Fischer K (2013) Increased temperature reduces herbivore host-plant quality. Glob Change Biol 19:3272–3282Google Scholar
  8. Beenakkers A, Van der Horst D, Van Marrewijk W (1984) Insect flight muscle metabolism. Insect Biochem 4:243260Google Scholar
  9. 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 113:539–547CrossRefGoogle Scholar
  10. Benard MF, McCauley SJ (2008) Integrating across life-history stages: consequences of natal habitat effects on dispersal. Am Nat 171:553–567PubMedGoogle Scholar
  11. 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 16:587–598CrossRefGoogle Scholar
  12. 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 16:484–491CrossRefGoogle Scholar
  13. Betts CR, Wootton RJ (1988) Wing shape and flight behaviour in butterflies Lepidoptera: Papilionoidea and Hesperioidea. A preliminary analysis. J Exp Biol 138:271–288Google Scholar
  14. 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 277:71–77CrossRefPubMedPubMedCentralGoogle Scholar
  15. Bookstein FL (1991) Morphometric tools for landmark data: geometry and biology. Cambridge University Press, Cambridge/New York/Port Chester/Melbourne/SydneyGoogle Scholar
  16. 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 15:233–251CrossRefPubMedGoogle Scholar
  17. Bouchard SS, O’Leary CJ, Wargelin LJ, Charbonnier JF, Warkentin KM (2015) Post-metamorphic carry-over effects of larval digestive plasticity. Funct Ecol 30:379–388CrossRefGoogle Scholar
  18. Breuker CP, Patterson JS, Klingenberg CP (2006) A single basis for developmental buffering of Drosophila wing shape. PLoS One 1:e7CrossRefPubMedPubMedCentralGoogle Scholar
  19. 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 104:445–452CrossRefGoogle Scholar
  20. 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 95:469–483CrossRefGoogle Scholar
  21. Cooper WE (2000) Effect of temperature on escape behaviour by an ectothermic vertebrate, the keeled earless lizard Holbrookia propinqua. Behaviour 10:1299–1315CrossRefGoogle Scholar
  22. Corbet PS (1999) Dragonflies: behavior and ecology of Odonata. Harley Books, Colchester, p 830Google Scholar
  23. David J, Legout H, Moreteau B (2006) Phenotypic plasticity of body size in a temperate population of Drosophila melanogaster. J Genetics 85:9–23CrossRefGoogle Scholar
  24. De Block M, Stoks R (2003) Adaptive sex-specific life history plasticity to temperature and photoperiod in a damselfly. J Evol Biol 16:986–995CrossRefPubMedGoogle Scholar
  25. De Block M, Stoks R (2005) Fitness effects from egg to reproduction: bridging the life-history transition. Ecology 86:185–197CrossRefGoogle Scholar
  26. Debat V, Béagin M, Legout H, David J (2003) Allometric and nonallometric components of Drosophila wing shape respond differently to developmental temperature. Evolution 57:2773–2784CrossRefPubMedGoogle Scholar
  27. 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 29:1292–1299CrossRefGoogle Scholar
  28. DeVries PJ, Penz CM, Hill RI (2010) Vertical distribution, flight behaviour and evolution of wing morphology in Morpho butterflies. J Anim Ecol 79:1077–1085CrossRefPubMedGoogle Scholar
  29. Diffenbaugh NS, Field CB (2013) Changes in ecologically critical terrestrial climate conditions. Science 341:486–492CrossRefPubMedGoogle Scholar
  30. Dillon ME, Cahn LRY, Huey RB (2007) Life history consequences of temperature transients in Drosophila melanogaster. J Exp Biol 210:2897–2904CrossRefPubMedGoogle Scholar
  31. 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 22:3361–3372CrossRefGoogle Scholar
  32. Dudley R (2000) The biomechanics of insect flight: form, function, evolution. Princeton University Press, PrincetonGoogle Scholar
  33. 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 109:19310–19314CrossRefPubMedPubMedCentralGoogle Scholar
  34. 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 211:2116–2122CrossRefPubMedGoogle Scholar
  35. Gilchrist AS, Azevedo RBR, Partridge L, O’higgins P (2000) Adaptation and constraint in the evolution of Drosophila melanogaster wing shape. Evol Dev 2:114–124CrossRefPubMedGoogle Scholar
  36. 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 28:639–654CrossRefGoogle Scholar
  37. Haenlein MH, Kaplan AM (2004) A beginner’s guide to partial least square analysis. Underst Stat 3:283–297CrossRefGoogle Scholar
  38. Hassall T, Thompson D (2008) The effects of environmental warming on Odonata: a review. Int J Odonatol 11:131–153CrossRefGoogle Scholar
  39. Haunerland NH (1997) Transport and utilization of lipids in insect flight muscles. Comp Biochem Physiol B: Biochem Mol Biol 117:475–482CrossRefGoogle Scholar
  40. Hickling A, Roy DB, Hill J, Thomas CD (2005) A northward shift of range margins in British Odonata. Glob Change Biol 11:502–506CrossRefGoogle Scholar
  41. Hoffmann AA, Shirriffs J (2002) Geographic variation for wing shape in Drosophila serrata. Evolution 56:1068–1073CrossRefPubMedGoogle Scholar
  42. 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 31:965–971Google Scholar
  43. 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 44:233–243CrossRefGoogle Scholar
  44. IPCC (2013) Climate change 2013: The physical science basis. University Press, Cambridge, United Kingdom and New York, CambridgeGoogle Scholar
  45. 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 148:74–82CrossRefPubMedGoogle Scholar
  46. Johnson CG (1966) A functional system of adaptive dispersal by flight. Annu Rev Entomol 11:233–260CrossRefGoogle Scholar
  47. 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 54:1035–1040CrossRefPubMedGoogle Scholar
  48. 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 51:719–732CrossRefPubMedGoogle Scholar
  49. Kingsolver JG, Diamond SE, Buckley LB (2013) Heat stress and the fitness consequences of climate change for terrestrial ectotherms. Funct Ecol 27:1415–1423CrossRefGoogle Scholar
  50. 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 32:59–65CrossRefGoogle Scholar
  51. Krishnan J, Williams LJ, McIntosh AR, Abdi H (2011) Partial least squares (PLS) methods for neuroimaging: a tutorial and review. NeuroImage 56:455–475CrossRefPubMedGoogle Scholar
  52. 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 184:91–109CrossRefPubMedGoogle Scholar
  53. Lake Flake model (2014) Available: http://www.flake.igb-berlin.de/index.shtml. Accessed 20 Mar 2014
  54. Manfreda E, Mitteroecker P, Bookstein FL, Schaefer K (2006) Functional morphology of the first cervical vertebra in humans and nonhuman primates. Anat Record 289B:184–194CrossRefGoogle Scholar
  55. Marden J (1989) Bodybuilding dragonflies: costs and benefits of maximizing flight muscle. Physiol Zool 62:505–521CrossRefGoogle Scholar
  56. McCauley S, Mabry K (2011) Climate change, body size, and phenotype dependent dispersal. Trends Ecol Evol 26:554–555CrossRefPubMedGoogle Scholar
  57. McIntosh AR, Lobaugh NJ (2004) Partial least square analysis of neuroimaging data: applications and advances. NeuroImage 23:250–563CrossRefGoogle Scholar
  58. Meehl G, Tebaldi C (2004) More intense, more frequent, and longer lasting heat waves in the 21st Century. Science 305:994–997CrossRefPubMedGoogle Scholar
  59. 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 93:1340–1352CrossRefPubMedGoogle Scholar
  60. Norberg UM (1995) How a long tail and changes in mass and wing shape affect the cost for flight in animals. Funct Ecol 9:48–54CrossRefGoogle Scholar
  61. 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 277:267–274CrossRefGoogle Scholar
  62. Outomuro D, Johansson F (2015) Bird predation selects for wing shape and coloration in a damselfly. J Evol Biol 28:791–799CrossRefPubMedGoogle Scholar
  63. Outomuro D, Adams DC, Johansson F (2013) Wing shape allometry and aerodynamics in calopterygid damselflies: a comparative approach. BMC Evol Biol 13:118CrossRefPubMedPubMedCentralGoogle Scholar
  64. 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 70–7:1582–1595CrossRefGoogle Scholar
  65. Pechenik JA (2006) Larval experience and latent effects—metamorphosis is not a new beginning. Integr Comp Biol 46:323–333CrossRefPubMedGoogle Scholar
  66. 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 88:327–348CrossRefPubMedGoogle Scholar
  67. 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 269:375–395CrossRefPubMedGoogle Scholar
  68. R Development Core Team (2014) R: a language and environment for statistical computing. Vienna: R foundation for statistical computing. http://www.R-project.org
  69. 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 82:275–285CrossRefPubMedGoogle Scholar
  70. Rohlf F, Corti M (2000) Use of two-block partial least squares to study covariation in shape. Syst Biol 49:740–753CrossRefPubMedGoogle Scholar
  71. Rohlf F, Slice D (1990) Extensions of the Procrustes method for the optimal superimposition of landmarks. Syst Zool 39:40–59CrossRefGoogle Scholar
  72. Roth O, Kurtz J, Reusch T (2010) A summer heat wave decreases the immunocompetence of the mesograzer, Idotea baltica. Mar Biol 157:1605–1611CrossRefGoogle Scholar
  73. Sacktor B (1970) Regulation of intermediary metabolism, with special reference to the control mechanisms in insect flight muscle. Adv Insect Physiol 7:267–347CrossRefGoogle Scholar
  74. Sentis A, Hemptinne JL, Brodeur J (2013) Effects of simulated heat waves on an experimental plant–herbivore-predator food chain. Glob Change Biol 19:833–842CrossRefGoogle Scholar
  75. Seppälä O, Jokela J (2011) Immune defence under extreme ambient temperature. Biol Lett 7:119–122CrossRefPubMedGoogle Scholar
  76. Simmons A, Uppala S, Dee D, Kobayashi S (2007) ERA-interim: new ECMWF reanalysis products from 1989 onwards. ECMWF Newslett 110:25–35Google Scholar
  77. Sokolovska N, Rowe L, Johansson F (2000) Fitness and body size in mature odonates. Ecolo Entomol 25:239–248CrossRefGoogle Scholar
  78. Starmer WT, Wolf MM (1989) Causes of variation of wing loading among Drosophila species. Biol J Linn Soc 37:247–261CrossRefGoogle Scholar
  79. Stoks R, Córdoba-Aguilar A (2012) Evolutionary ecology of Odonata: a complex life cycle perspective. Ann Rev Entomol 57:249–265CrossRefGoogle Scholar
  80. Swillen I, De Block M, Stoks R (2009) Morphological and physiological sexual selection targets in a territorial damselfly. Ecol Entomol 34:677–683CrossRefGoogle Scholar
  81. 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 37:1012–1021CrossRefGoogle Scholar
  82. Thompson R, Beardall J, Beringer J, Grace M, Sardina P (2013) Means and extremes: building variability into community-level climate change experiments. Ecol Lett 16:799–806CrossRefPubMedGoogle Scholar
  83. 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 122:1532–1540CrossRefGoogle Scholar
  84. 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 281:20132612CrossRefPubMedPubMedCentralGoogle Scholar
  85. Wakeling J, Ellington C (1997) Dragonfly flight. III. Lift and power requirements. J Exp Biol 200:583–600PubMedGoogle Scholar
  86. 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 416:389–395CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  1. 1.Irstea, Research Unit MAEP (Freshwater Systems, Ecology and Pollution)Villeurbanne CedexFrance
  2. 2.Laboratory of Aquatic Ecology, Evolution and ConservationUniversity of LeuvenLouvainBelgium
  3. 3.ECOEVO LabUniversidade de VigoPontevedraSpain

Personalised recommendations