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PLOS ONE  2014 

Does Skipping a Meal Matter to a Butterfly's Appearance? Effects of Larval Food Stress on Wing Morphology and Color in Monarch Butterflies

DOI: 10.1371/journal.pone.0093492

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In animals with complex life cycles, all resources needed to form adult tissues are procured at the larval stage. For butterflies, the proper development of wings involves synthesizing tissue during metamorphosis based on the raw materials obtained by larvae. Similarly, manufacture of pigment for wing scales also requires resources acquired by larvae. We conducted an experiment to test the effects of food deprivation in the larval stage on multiple measures of adult wing morphology and coloration of monarch butterflies (Danaus plexippus), a species in which long-distance migration makes flight efficiency critical. In a captive setting, we restricted food (milkweed) from late-stage larvae for either 24 hrs or 48 hrs, then after metamorphosis we used image analysis methods to measure forewing surface area and elongation (length/width), which are both important for migration. We also measured the brightness of orange pigment and the intensity of black on the wing. There were correlations between several wing features, including an unexpected association between wing elongation and melanism, which will require further study to fully understand. The clearest effect of food restriction was a reduction in adult wing size in the high stress group (by approximately 2%). Patterns observed for other wing traits were ambiguous: monarchs in the low stress group (but not the high) had less elongated and paler orange pigmentation. There was no effect on wing melanism. Although some patterns obtained in this study were unclear, our results concerning wing size have direct bearing on the monarch migration. We show that if milkweed is limited for monarch larvae, their wings become stunted, which could ultimately result in lower migration success.


[1]  Hahn DA (2005) Larval nutrition affects lipid storage and growth, but not protein or carbohydrate storage in newly eclosed adults of the grasshopper Schistocerca americana. Journal of Insect Physiology 51: 1210–1219. doi: 10.1016/j.jinsphys.2005.06.011
[2]  Scott DE (1994) The effect of larval density on adult demographic traits in Ambystoma opacum. Ecology 75: 1383–1396. doi: 10.2307/1937462
[3]  Telang A, Wells MA (2004) The effect of larval and adult nutrition on successful autogenous egg production by a mosquito. Journal of Insect Physiology 50: 677–685. doi: 10.1016/j.jinsphys.2004.05.001
[4]  Tigreros N (2013) Linking nutrition and sexual selection across life stages in a model butterfly system. Functional Ecology 27: 145–154. doi: 10.1111/1365-2435.12006
[5]  Awmack CS, Leather SR (2002) Host plant quality and fecundity in herbivorous insects. Annual Review of Entomology 47: 817–844.
[6]  Pellegroms B, Van Dongen S, Van Dyck H, Lens L (2009) Larval food stress differentially affects flight morphology in male and female speckled woods (Pararge aegeria). Ecological Entomology 34: 387–393. doi: 10.1111/j.1365-2311.2009.01090.x
[7]  Boggs CL, Freeman KD (2005) Larval food limitation in butterflies: effects on adult resource allocation and fitness. Oecologia 144: 353–361. doi: 10.1007/s00442-005-0076-6
[8]  Brower LP (1995) Understanding and misunderstanding the migration of the monarch butterfly (Nymphalidae) in North America: 1857–1995. Journal of the Lepidopterists' Society 49: 304–385.
[9]  Howard E, Davis AK (2004) Documenting the spring movements of monarch butterflies with Journey North, a citizen science program. In: Oberhauser K, Solensky M, editors. The monarch butterfly Biology and Conservation. Ithaca, NY: Cornell University Press. pp. 105–114.
[10]  Altizer S, Davis AK (2010) Populations of monarch butterflies with different migratory behaviors show divergence in wing morphology. Evolution 64: 1018–1028. doi: 10.1111/j.1558-5646.2010.00946.x
[11]  Davis AK, Farrey B, Altizer S (2005) Variation in thermally-induced melanism in monarch butterflies (Lepidoptera: Nymphalidae) from three North American populations. Journal of Thermal Biology 30: 410–421. doi: 10.1016/j.jtherbio.2005.04.003
[12]  Sander SE, Altizer S, De Roode JC, Davis AK (2013) Genetic factors and host traits predict spore morphology for a butterfly pathogen. Insects 4: 447–462. doi: 10.3390/insects4030447
[13]  Davis AK, Chi J, Bradley CA, Altizer S (2012) The redder the better: wing color predicts flight performance in monarch butterflies. PloS One 7: e41323 doi:41310.41371/journal.pone.0041323.
[14]  Hanley D, Miller NG, Flockhart DT, Norris DR (2013) Forewing pigmentation predicts migration distance in wild-caught migratory monarch butterflies. Behavioral Ecology 24: 1108–1113. doi: 10.1093/beheco/art037
[15]  Dmitriew C, Rowe L (2011) The effects of larval nutrition on reproductive performance in a food-limited adult environment. Plos One 6: 6. doi: 10.1371/journal.pone.0017399
[16]  Barros-Bellanda HCH, Zucoloto FS (2002) Effects of intraspecific competition and food deprivation on the immature phase of Ascia monuste orseis (Lepidoptera, Pieridae). Iheringia, Série Zoologia 92: 93–98. doi: 10.1590/s0073-47212002000100009
[17]  Kemp DJ (2008) Resource-mediated condition dependence in sexually dichromatic butterfly wing coloration. Evolution 62: 2346–2358. doi: 10.1111/j.1558-5646.2008.00461.x
[18]  Flockhart DTT, Martin TG, Norris DR (2012) Experimental examination of intraspecific density-dependent competition during the breeding period in monarch butterflies (Danaus plexippus). Plos One 7: 8. doi: 10.1371/journal.pone.0045080
[19]  Knuttel H, Fiedler K (2001) Host-plant derived variation in ultraviolet wing pattern influences mate selection by male butterflies. Journal of Experimental Biology 204: 2447–2459.
[20]  Talloen W, Van Dyck H, Lens L (2004) The cost of melanization: butterfly wing coloration under environmental stress. Evolution 58: 360–366. doi: 10.1554/03-250
[21]  Pleasants JM, Oberhauser KS (2012) Milkweed loss in agricultural fields because of herbicide use: effect on the monarch butterfly population. Insect Conservation and Diversity: Online Early doi:10.1111/j.1752-4598.2012.00196.x.
[22]  Altizer SM, Oberhauser K, Brower LP (2000) Associations between host migration and the prevalence of a protozoan parasite in natural populations of adult monarch butterflies. Ecological Entomology 25: 125–139. doi: 10.1046/j.1365-2311.2000.00246.x
[23]  Davis AK (2009) Wing color of monarch butterflies (Danaus plexippus) in eastern North America across life stages: migrants are ‘redder’ than breeding and overwintering stages. Psyche 2009 doi:10.1155/2009/705780.
[24]  Davis AK, Cope N, Smith A, Solensky MJ (2007) Wing color predicts future mating success in male monarch butterflies. Annals of the Entomological Society of America 100: 339–344. doi: 10.1603/0013-8746(2007)100[339:wcpfms];2
[25]  Satterfield DA, Wright AE, Altizer S (2013) Lipid reserves and immune defense in healthy and diseased migrating monarchs Danaus plexippus. Current Zoology 59: 393–402.
[26]  Statistica (2003) Statistica version 6.1, Statsoft Inc.
[27]  Bauerfeind SS, Fischer K (2009) Effects of larval starvation and adult diet-derived amino acids on reproduction in a fruit-feeding butterfly. Entomologia Experimentalis et Applicata 130: 229–237. doi: 10.1111/j.1570-7458.2008.00814.x
[28]  Nijhout HF, Grunert LW (2010) The cellular and physiological mechanism of wing-body scaling in Manduca sexta. Science 330: 1693–1695. doi: 10.1126/science.1197292
[29]  Lafont R, Mauchamp B, Blais C, Pennetier JL (1977) Ecdysones and imaginal disk development during last larval instar of Pieris brassicae. Journal of Insect Physiology 23: 277–283. doi: 10.1016/0022-1910(77)90042-7
[30]  Tigreros N, Sass EM, Lewis SM (2013) Sex-specific response to nutrient limitation and its effects on female mating success in a gift-giving butterfly. Evolutionary Ecology Online Early- doi:10.1007/s10682-013-9647-x.
[31]  Ethier J, Despland E (2012) Effects of polymorphic melanism and larval diet on life history traits of Malacosoma disstria moths. Journal of Insect Physiology 58: 67–74. doi: 10.1016/j.jinsphys.2011.09.018
[32]  Atterholt AL, Solensky MJ (2010) Effects of larval rearing density and food availability on adult size and coloration in monarch butterflies (Lepidoptera: Nymphalidae). Journal of Entomological Science 45: 366–377.
[33]  Lindsey E, Mehta M, Dhulipala V, Oberhauser K, Altizer S (2009) Crowding and disease: effects of host density on response to infection in a butterfly-parasite interaction. Ecological Entomology 34: 551–561. doi: 10.1111/j.1365-2311.2009.01107.x
[34]  Van Dyck H, Matthysen E, Wiklund C (1998) Phenotypic variation in adult morphology and pupal colour wintin and among families of the speckled wood butterfly Pararge aegeria. Ecological Entomology 23: 465–472. doi: 10.1046/j.1365-2311.1998.00151.x
[35]  Trullas SC, van Wyk JH, Spotila JR (2007) Thermal melanism in ectotherms. Journal of Thermal Biology 32: 235–245. doi: 10.1016/j.jtherbio.2007.01.013
[36]  Ellers J, Boggs CL (2004) Functional ecological implications of intraspecific differences in wing melanization in Colias butterflies. Biological Journal of the Linnean Society 82: 79–87. doi: 10.1111/j.1095-8312.2004.00319.x
[37]  Gibo DL, Pallett MJ (1979) Soaring flight of monarch butterflies, Danaus plexippus (Lepidoptera: Danaidae), during the late summer migration in southern Ontario. Canadian Journal of Zoology 57: 1393–1401. doi: 10.1139/z79-180
[38]  Bowlin MS, Wikelski M (2008) Pointed wings, low wingloading and calm air reduce the cost of migratory flight in songbirds. Plos One 3: e2154. doi: 10.1371/journal.pone.0002154
[39]  Copete JL, Marine R, Bigas D, Martinez-Vilalta A (1999) Differences in wing shape between sedentary and migratory Reed Buntings Emberiza schoeniclus. Bird Study 46: 100–103. doi: 10.1080/00063659909461119
[40]  Gibo DL, McCurdy JA (1993) Lipid accumulation by monarch butterflies (Danaus plexippus L.). Canadian Journal of Zoology 71: 76–82. doi: 10.1139/z93-012
[41]  McCord JW, Davis AK (2010) Biological observations of monarch butterfly behavior at a migratory stopover site: results from a long-term tagging study in coastal South Carolina. Journal of Insect Behavior 23: 405–418. doi: 10.1007/s10905-010-9224-x
[42]  Satterfield DA, Davis AK (In Press) Variation in wing characteristics of monarch butterflies during migration: Earlier migrants have redder and more elongated wings. Animal Migration


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