Abstract
Due to an overlap in the resources used by the flight muscles with the resources used during egg production, it has been hypothesised that an increased dispersal in fragmented landscapes may result in a physiological trade-off between flight and reproduction. In a common garden experiment, we investigated the effects of increased flight on the reproductive output of female speckled wood butterflies (Pararge aegeria, L.) from closed continuous woodland populations versus open highly fragmented agricultural landscapes in central France. Our flight treatment significantly affected resource allocation to egg size, but had no effect on mean daily fecundity. This treatment effect was similar for females from the two landscapes of origin, and suggests that energetic costs associated with increased flight result in a decrease in resource allocation to egg provisioning. There was a landscape-specific effect of flight on longevity: flight reduced longevity by 21% in woodland females, but had no affect on agricultural females. This result suggests that woodland landscape females further compensate for excessive flight by redirecting resources away from somatic maintenance, resulting in reduced life spans. Our results strongly indicate that increased flight caused by changes in landscape structure may impact on key life history traits such as reproductive success and longevity.
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References
Baguette M, Van Dyck H (2007) Landscape connectivity and animal behaviour: functional grain as a key determinant for dispersal. Landsc Ecol. doi:10.1007/s10980-0079108-4
Baguette M, Mennechez G, Petit S, Schtickzelle N (2003) Effect of habitat fragmentation on dispersal in the butterfly Proclossiana eunomia. C R Biol 326:S200–S209
Bauerfeind SS, Fischer K (2008) Maternal body size as a morphological constraint on egg size and fecundity in butterflies. Basic Appl Ecol. doi:10.1016/j.baae.2007.05.005
Benton TG, Plaistow SJ, Beckerman AP, Lapsley CT, Littlejohns S (2005) Changes in maternal investment in eggs can affect population dynamics. Proc R Soc Lond B. doi:10.1098/rspb.2005.3081
Bewaerts K, Matthysen E, Van Dyck H (2008) Take off flight performance in the butterfly Pararge aegeria relative to sex and morphology: a quantitative genetic perspective. Evolution 62:2525–2533
Bink FA (1992) Ecologische atlas van de dagvlinders van Noordwest-Europa. Schultz, Harlem
Braendle C, Davis GK, Brisson JA, Stern DL (2006) Wing dimorphism in aphids. Heredity. doi:10.1038/sj.hdy.6800863
Breuker CJ, Brakefield PM, Gibbs M (2007) The association between wing morphology and dispersal is sex-specific in the Glanville fritillary butterfly Melitaea cinxia (Lepidoptera: Nymphalidae). Eur J Entomol 104:445–452
Chown S, Nicolson S (2004) Insect physiological ecology: mechanisms and patterns. Oxford University Press, Oxford
Cory JS, Goulson D (1993) Flower constancy and learning in foraging preferences of the green-veined butterfly Pieris napi. Ecol Entomol. doi:10.1111/j.1365-2311.1993.tb01107.x
Debinski DM, Holt RD (2000) A survey and overview of habitat fragmentation experiments. Conserv Biol. doi:10.1046/j.1523-1739.2000.98081.x
Dempster JP (1991) Fragmentation, isolation and mobility of insect populations. In: Collins NM, Thomas JA (eds) The conservation of insects and their habitats. Academic, London, pp 143–153
Dempster JP, King ML, Lakhani KH (1976) The status of the swallowtail butterfly in Britain. Ecol Entomol. doi:111/j.1365-231.1976.tb01207.x
Diaz JA, Pérez-Tris J, Telleria JL, Carbonell R, Santos T (2005) Reproductive investment of a lacertid lizard in fragmented habitat. Conserv Biol. doi:10.1111/j.1523-1739.2005.00197.x
Dover J, Sparks T (2000) A review of the ecology of butterflies in British hedgerows. J Environ Manag. doi:10.1006/jema.2000.0361
Dudley R (2000) The biomechanics of insect flight: form, function, evolution. Princeton University Press, Princeton
Engqvist L (2005) The mistreatment of covariate interaction terms in linear model analyses of behavioural and evolutionary ecology studies. Anim Behav 70:967–971
Fahrig L (2003) Effects of habitat fragmentation on biodiversity. Annu Rev Ecol Evol Syst 34:487–515
Gibbs M, Van Dyck H (2009) Reproductive plasticity, oviposition site selection and maternal effects in fragmented landscapes. Behav Ecol Sociobiol. doi:10.1007/s00265-009-0849-8
Gibbs M, Lace LA, Jones MJ, Moore AJ (2005) Egg size-number trade-off and a decline in oviposition site choice quality: female Pararge aegeria butterflies pay a cost of having males present at oviposition. J Insect Sci 5:39. http://insectscience.org/5.39
Gibbs M, Breuker CJ, Van Dyck H (2010) Flight during oviposition reduces maternal egg provisioning and influences offspring development in Pararge aegeria (L.). Physiol Entomol. doi:10.1111/j.1365-3032.2009.00706.x
Hanski I, Ovaskainen O (2000) The metapopulation capacity of a fragmented landscape. Nature. doi:10.1038/35008063
Hanski I, Alho J, Moilanen A (2000) Estimating the parameters of survival and migration of individuals in metapopulations. Ecology 81:239–251
Hanski I, Breuker CJ, Schöps K, Setchfield R, Nieminen M (2002) Population history and life history influence the migration rate of female Glanville fritillary butterflies. Oikos 98:87–97
Hanski I, Saastamoinen M, Ovaskainen O (2006) Dispersal-related life history trade-offs in a butterfly metapopulation. J Anim Ecol. doi:10.1111/j.1365-2656.2005.01024.x
Higgins LG, Riley ND (1993) A field guide to the butterflies of Britain and Europe, 5th edn. Harper Collins, London
Hill JK, Collingham YC, Thomas CD, Blakeley DS, Fox R, Moss D, Huntley B (2001) Impacts of landscape structure on butterfly range expansion. Ecol Lett. doi:10.1046/j.1461-0248.2001.00222.x
Hughes CL, Hill JK, Dytham C (2003) Evolutionary trade-offs between reproduction and dispersal in populations at expanding range boundaries. Proc R Soc Lond B. doi:10.1098/rsbl.2003.0049
Jervis MA, Boggs CL, Ferns PN (2005) Egg maturation strategy and its associated trade-offs: a synthesis focusing on Lepidoptera. Ecol Entomol. doi:10.111/j.0307-6946.2005.00712.x
Jervis MA, Ellers J, Harvey JA (2008) Resource acquisition, allocation, and utilization in parasitoid reproductive strategies. Annu Rev Entomol 53:361–385
Johnson CG (1963) Physiological factors in insect migration by flight. Nature. doi:10.1038/98423a0
Karlsson B (1987) Variation in egg weight, oviposition rate and reproductive reserves with female age in a natural population of the speckled wood butterfly, Pararge aegeria. Ecol Entomol. doi:10.1111/j.1365-2311.1987.tb01029.x
Karlsson B (1994) Feeding-habits and change of body composition with age in 3 Nymphalid butterfly species. Oikos 69:224–230
Karlsson B, Van Dyck H (2005) Does habitat fragmentation affect temperature-related life-history traits? A laboratory test with a woodland butterfly. Proc R Soc B. doi:10.1098/rspb.2005.3074
Lessels CM (1991) The evolution of life histories. In: Krebs JR, Davies NB (eds) Behavioural ecology: an evolutionary approach. Blackwell, Oxford, pp 32–68
Merckx T, Van Dyck H (2006) Landscape structure and phenotypic plasticity in flight morphology in the butterfly Pararge aegeria. Oikos 113:226–232
Merckx T, Van Dyck H, Karlsson B, Leimar O (2003) The evolution of movements and behaviour at boundaries in different landscapes: a common arena experiment with butterflies. Proc R Soc Lond B. doi:10.1098/rspb.2003.2459
Merckx T, Karlsson B, Van Dyck H (2006) Sex- and landscape-related differences in flight ability under suboptimal temperatures in a woodland butterfly. Funct Ecol. doi:10.1016/j.anbehav.2006.12.020
Mole S, Zera AJ (1994) Differential resource consumption obviates a potential flight fecundity trade-off in the sand cricket (Gryllus firmus). Funct Ecol 8:573–580
Murphy DD, Launer AE, Ehrlich PR (1983) The role of adult feeding in egg production and population dynamics of the checkerspot butterfly Euphydryas editha. Oecologia. doi:10.1007/BF00379699
Nijhout FH (1994) Insect hormones. Princeton University Press, Princeton
Norberg U, Enfjall K, Leimar O (2002) Habitat exploration in butterflies—an outdoor cage experiment. Evol Ecol 16:1–14
Nylin S, Gotthard K (1998) Plasticity in life-history traits. Annu Rev Entomol 43:63–83
Ries L, Fletcher RJ Jr, Battin J, Sisk TD (2004) Ecological responses to habitat edges: mechanisms, models, and variability explained. Annu Rev Ecol Evol Syst. doi:10.1146/annurev.ecolsys.35.112202.130148
Roff DA (1992) The evolution of life histories: theory and analysis. Chapman & Hall, New York
Roff DA, Fairbairn DJ (1991) Wing dimorphisms and the evolution of migratory polymorphisms among the Insecta. Am Zool 31:243–251
Roff DA, Fairbairn DJ (2007) Laboratory evolution of the migratory polymorphism in the sand cricket: combining physiology with quantitative genetics. Physiol Biochem Zool. doi:10.1641/B570210
Roland J, Keyghobadi N, Fownes S (2000) Alpine Parnassius butterfly dispersal: effects of landscape and population size. Ecology 81:1642–1653
Saastamoinen M (2007) Mobility and lifetime fecundity in new versus old populations of the Glanville fritillary butterfly. Oecologia. doi:10.1007/s00442-007-0772-5
Schlaepfer MA, Runge MC, Sherman PW (2002) Ecological and evolutionary traps. Trends Ecol Evol. doi:10.1016/S0169-5347(02)02580-6
Schtickzelle N, Mennechez G, Baguette M (2006) Dispersal depression with habitat fragmentation in the bog fritillary butterfly. Ecology 87:1057–1065
Shreeve TG (1984) Habitat selection, mate location, and microclimatic constraints on the activity of the speckled wood butterfly Pararge aegeria. Oikos 42:371–377
Shreeve TG (1986) Egg-laying by the speckled wood butterfly (Pararge aegeria)—the role of female behavior, host plant abundance and temperature. Ecol Entomol. doi:10.1111/j.1365-2311.1986.tb00298.x
Stearns SC (1992) The evolution of life histories. Oxford University Press, Oxford
Steigenga MJ, Hoffmann KH, Fischer K (2006) Effects of the juvenile hormone mimic pyriproxyfen on female reproduction and longevity in the butterfly Bicyclus anynana. Entomol Sci. doi:10.1111/j.1479-8298.2006.00173.x
Svärd L, Wiklund C (1989) Mass and production rates of ejaculates in relation to monandry/polyandry in butterflies. Behav Ecol Sociobiol. doi:10.1007/BF00293267
Taylor PD, Merriam G (1995) Wing morphology of a forest damselfly is related to landscape structure. Oikos 73:43–48
Thomas CD (2000) Dispersal and extinction in fragmented landscapes. Proc R Soc Lond B. doi:10.1098/rspb.2000.0978
Thomas CD, Hill JK, Lewis OT (1998) Evolutionary consequences of habitat fragmentation in a localized butterfly. J Anim Ecol 67:485–497
Van Dyck H, Baguette M (2005) Dispersal behaviour in fragmented landscapes: routine or special movements? Basic Appl Ecol 6:535–545
Wickman PO, Wiklund C (1983) Territorial defense and its seasonal decline in the speckled wood butterfly (Pararge aegeria). Anim Behav 31:1206–1216
Wiklund C, Karlsson B (1984) Egg size variation in satyrid butterflies: adaptive vs. historical, “Bauplan”, and mechanistic explanations. Oikos 43:391–400
Wiklund C, Persson B (1983) Fecundity, and the relation of egg weight variation to offspring fitness in the speckled wood butterfly Pararge aegeria, or why don’t butterfly females lay more eggs? Oikos 40:53–63
Acknowledgments
Hubert Baltus helped with the butterfly rearing. Michel Pirnay, Jean-Pierre Motte and Marc Migon provided technical assistance. Sofie Vandewoestijne assisted with the field collection of butterflies. Casper J. Breuker wrote the software to measure the eggs, provided valuable comments, help with the figures and statistical advice. This is publication number BRC 176 of the Biodiversity Research Centre of the UCL. The research was supported by two research grants to H.V.D. (FSR06-grant of UCL, and FRFC 2.4595.07 and 2.4556.05 of the FNRS Fund for Scientific Research, Wallonia, Belgium). We declare that the experiments comply with the current laws of Belgium.
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Communicated by Roland Brandl.
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Gibbs, M., Van Dyck, H. Butterfly flight activity affects reproductive performance and longevity relative to landscape structure. Oecologia 163, 341–350 (2010). https://doi.org/10.1007/s00442-010-1613-5
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DOI: https://doi.org/10.1007/s00442-010-1613-5