Phytochemical changes in milkweed induced by elevated CO2 alter wing morphology but not toxin sequestration in monarch butterflies
dc.contributor.author | Decker, Leslie E. | |
dc.contributor.author | Soule, Abrianna J. | |
dc.contributor.author | de Roode, Jacobus C. | |
dc.contributor.author | Hunter, Mark D. | |
dc.date.accessioned | 2019-03-11T15:35:23Z | |
dc.date.available | 2020-05-01T18:03:26Z | en |
dc.date.issued | 2019-03 | |
dc.identifier.citation | Decker, Leslie E.; Soule, Abrianna J.; de Roode, Jacobus C.; Hunter, Mark D. (2019). "Phytochemical changes in milkweed induced by elevated CO2 alter wing morphology but not toxin sequestration in monarch butterflies." Functional Ecology 33(3): 411-421. | |
dc.identifier.issn | 0269-8463 | |
dc.identifier.issn | 1365-2435 | |
dc.identifier.uri | https://hdl.handle.net/2027.42/148239 | |
dc.description.abstract | Environmental change has the potential to influence trophic interactions by altering the defensive phenotype of prey.Here, we examine the effects of a pervasive environmental change driver, elevated atmospheric concentrations of CO2 (eCO2), on toxin sequestration and flight morphology of a specialist herbivore.We fed monarch butterfly larvae, Danaus plexippus, foliage from four milkweed, Asclepias, species of varying chemical defence profiles grown under either ambient or eCO2. We also infected a subset of these herbivores with a protozoan parasite, Ophryocystis elektroscirrha, to understand how infection and environmental change combine to alter herbivore defences. We measured changes in phytochemistry induced by eCO2 and assessed cardenolide, toxic steroid, sequestration and wing morphology of butterflies.Monarchs compensated for lower plant cardenolide concentrations under eCO2 by increasing cardenolide sequestration rate, maintaining similar cardenolide composition and concentrations in their wings under both CO2 treatments. We suggest that these increases in sequestration rate are a by‐product of compensatory feeding aimed at maintaining a nutritional target in response to declining dietary quality under eCO2.Monarch wings were more suitable for sustained flight (more elongated) when reared on plants grown under eCO2 or when reared on Asclepias syriaca or Asclepias incarnata rather than on Asclepias curassavica or Asclepias speciosa. Parasite infection engendered wings less suitable for sustained flight (wings became rounder) on three of four milkweed species. Wing loading (associated with powered flight) was higher on A. syriaca than on other milkweeds, whereas wing density was lower on A. curassavica. Monarchs that fed on high cardenolide milkweed developed rounder, thinner wings, which are less efficient at gliding flight.Ingesting foliage from milkweed high in cardenolides may provide protection from enemies through sequestration yet come at a cost to monarchs manifested as lower quality flight phenotypes: rounder, thinner wings with lower wing loading values.Small changes in morphology may have important consequences for enemy evasion and migration success in many animals. Energetic costs associated with alterations in defence and morphology may, therefore, have important consequences for trophic interactions in a changing world.A plain language summary is available for this article.Plain Language Summary | |
dc.publisher | Cornell University Press | |
dc.publisher | Wiley Periodicals, Inc. | |
dc.subject.other | Ophryocystis elektroscirrha | |
dc.subject.other | plant secondary metabolites | |
dc.subject.other | predator‐prey interactions | |
dc.subject.other | environmental change | |
dc.subject.other | Danaus plexippus | |
dc.subject.other | cardenolides | |
dc.subject.other | Asclepias | |
dc.title | Phytochemical changes in milkweed induced by elevated CO2 alter wing morphology but not toxin sequestration in monarch butterflies | |
dc.type | Article | |
dc.rights.robots | IndexNoFollow | |
dc.subject.hlbsecondlevel | Ecology and Evolutionary Biology | |
dc.subject.hlbtoplevel | Science | |
dc.description.peerreviewed | Peer Reviewed | |
dc.description.bitstreamurl | https://deepblue.lib.umich.edu/bitstream/2027.42/148239/1/fec13270-sup-0006-TableS2.pdf | |
dc.description.bitstreamurl | https://deepblue.lib.umich.edu/bitstream/2027.42/148239/2/fec13270-sup-0003-FigS2.pdf | |
dc.description.bitstreamurl | https://deepblue.lib.umich.edu/bitstream/2027.42/148239/3/fec13270-sup-0004-FigS3.pdf | |
dc.description.bitstreamurl | https://deepblue.lib.umich.edu/bitstream/2027.42/148239/4/fec13270-sup-0002-FigS1.pdf | |
dc.description.bitstreamurl | https://deepblue.lib.umich.edu/bitstream/2027.42/148239/5/fec13270-sup-0008-TableS4.pdf | |
dc.description.bitstreamurl | https://deepblue.lib.umich.edu/bitstream/2027.42/148239/6/fec13270-sup-0005-TableS1.pdf | |
dc.description.bitstreamurl | https://deepblue.lib.umich.edu/bitstream/2027.42/148239/7/fec13270-sup-0009-AppendixS1.pdf | |
dc.description.bitstreamurl | https://deepblue.lib.umich.edu/bitstream/2027.42/148239/8/fec13270_am.pdf | |
dc.description.bitstreamurl | https://deepblue.lib.umich.edu/bitstream/2027.42/148239/9/fec13270-sup-0001-Summary.pdf | |
dc.description.bitstreamurl | https://deepblue.lib.umich.edu/bitstream/2027.42/148239/10/fec13270.pdf | |
dc.description.bitstreamurl | https://deepblue.lib.umich.edu/bitstream/2027.42/148239/11/fec13270-sup-0007-TableS3.pdf | |
dc.identifier.doi | 10.1111/1365-2435.13270 | |
dc.identifier.source | Functional Ecology | |
dc.identifier.citedreference | Opitz, S. E. W., & Müller, C. ( 2009 ). Plant chemistry and insect sequestration. Chemoecology, 19 ( 3 ), 117 – 154. https://doi.org/10.1007/s00049-009-0018-6 | |
dc.identifier.citedreference | Malcolm, S. B. ( 1990 ). Chemical defence in chewing and sucking insect herbivores: Plant‐derived cardenolides in the monarch butterfly and oleander aphid. Chemoecology, 1 ( 1 ), 12 – 21. https://doi.org/10.1007/BF01240581 | |
dc.identifier.citedreference | Malcolm, S. B. ( 1994 ). Milkweeds, monarch butterflies and the ecological significance of cardenolides. Chemoecology, 5–6 ( 3–4 ), 101 – 117. https://doi.org/10.1007/BF01240595 | |
dc.identifier.citedreference | Malcolm, S. B., & Brower, L. P. ( 1989 ). Reviews Evolutionary and ecological implications of cardenolide sequestration in the monarch butterfly. Experientia, 45, 284 – 295. https://doi.org/10.1007/BF01951814 | |
dc.identifier.citedreference | Ode, P. J., & Crompton, D. S. ( 2013 ). Compatibility of aphid resistance in soybean and biological control by the parasitoid Aphidius colemani (Hymenoptera: Braconidae). Biological Control, 64 ( 3 ), 255 – 262. https://doi.org/10.1016/J.BIOCONTROL.2012.12.001 | |
dc.identifier.citedreference | Ode, P. J., Johnson, S. N., & Moore, B. D. ( 2014 ). Atmospheric change and induced plant secondary metabolites — are we reshaping the building blocks of multi‐trophic interactions? Current Opinion in Insect Science, 5, 57 – 65. https://doi.org/10.1016/j.cois.2014.09.006 | |
dc.identifier.citedreference | Park, H., Bae, K., Lee, B., Jeon, W. P., & Choi, H. ( 2010 ). Aerodynamic performance of a gliding swallowtail butterfly wing model. Experimental Mechanics, 50 ( 9 ), 1313 – 1321. https://doi.org/10.1007/s11340-009-9330-x | |
dc.identifier.citedreference | 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 ( 3 ), 387 – 393. https://doi.org/10.1111/j.1365-2311.2009.01090.x | |
dc.identifier.citedreference | Pennycuick, C. J. ( 2008 ). Modelling the flying bird, Vol. 5. Burlington, MA: Elsevier. | |
dc.identifier.citedreference | Petschenka, G., & Agrawal, A. A. ( 2016 ). How herbivores coopt plant defenses: Natural selection, specialization, and sequestration. Current Opinion in Insect Science, 14, 17 – 24. https://doi.org/10.1016/J.COIS.2015.12.004 | |
dc.identifier.citedreference | Reichstein, T., von Euw, J., Parsons, J. A., & Rothschild, M. ( 1968 ). Heart poisons in the monarch butterfly. Science, 161, 861 – 866. https://doi.org/10.2307/1724853 | |
dc.identifier.citedreference | Robinson, E. A., Ryan, G. D., & Newman, J. A. ( 2012 ). A meta‐analytical review of the effects of elevated CO 2 on plant–arthropod interactions highlights the importance of interacting environmental and biological variables. New Phytologist, 194, 321 – 336. https://doi.org/10.1111/j.1469-8137.2012.04074.x | |
dc.identifier.citedreference | Ryan, G. D., Rasmussen, S., & Newman, J. A. ( 2010 ). Global atmospheric change and trophic interactions: Are there any general responses? In F. Baluška, & V. Ninkovic (Eds), Plant communications from an ecological perspective (pp. 179 – 214 ). Berlin, Heidelberg: Springer. https://doi.org/10.1007/978-3-642-12162-3_11. | |
dc.identifier.citedreference | Satterfield, D. A., & Davis, A. K. ( 2014 ). Variation in wing characteristics of monarch butterflies during migration: Earlier migrants have redder and more elongated wings. Animal Migration, 2, 2084 – 8838. https://doi.org/10.2478/ami-2014-0001 | |
dc.identifier.citedreference | Satterfield, D. A., Maerz, J. C., & Altizer, S. ( 2015 ). Loss of migratory behaviour increases infection risk for a butterfly host. Proceedings of the Royal Society B: Biological Sciences, 282, 20141734 – 20141734. https://doi.org/10.1098/rspb.2014.1734 | |
dc.identifier.citedreference | Satterfield, D. A., Maerz, J. C., Hunter, M. D., Flockhart, D. T. T., Hobson, K. A., Norris, D. R., … Altizer, S. ( 2018 ). Migratory monarchs that encounter resident monarchs show life‐history differences and higher rates of parasite infection. Ecology Letters, 21, 1670 – 1680. https://doi.org/10.1111/ele.13144 | |
dc.identifier.citedreference | Simpson, S. J., Clissold, F. J., Lihoreau, M., Ponton, F., Wilder, S. M., & Raubenheimer, D. ( 2015 ). Recent advances in the integrative nutrition of arthropods. Annual Review of Entomology, 60 ( 1 ), 293 – 311. https://doi.org/10.1146/annurev-ento-010814-020917 | |
dc.identifier.citedreference | Smilanich, A. M., Dyer, L. A., Chambers, J. Q., & Bowers, M. D. ( 2009 ). Immunological cost of chemical defence and the evolution of herbivore diet breadth. Ecology Letters, 12, 612 – 621. https://doi.org/10.1111/j.1461-0248.2009.01309.x | |
dc.identifier.citedreference | Soto, I. M., Carreira, V. P., Soto, E. M., & Hasson, E. ( 2008 ). Wing morphology and fluctuating asymmetry depend on the host plant in cactophilic Drosophila. Journal of Evolutionary Biology, 21 ( 2 ), 598 – 609. https://doi.org/10.1111/j.1420-9101.2007.01474.x | |
dc.identifier.citedreference | Srygley, R. B., & Thomas, A. L. R. ( 2002 ). Unconventional lift‐generating mechanisms in free‐flying butterflies. Nature, 420 ( 6916 ), 660 – 664. https://doi.org/10.1038/nature01223 | |
dc.identifier.citedreference | Tao, L., Berns, A. R., & Hunter, M. D. ( 2014 ). Why does a good thing become too much? Interactions between foliar nutrients and toxins determine performance of an insect herbivore. Functional Ecology, 28 ( 1 ), 190 – 196. https://doi.org/10.1111/1365-2435.12163 | |
dc.identifier.citedreference | Tao, L., & Hunter, M. D. ( 2015 ). Effects of soil nutrients on the sequestration of plant defence chemicals by the specialist insect herbivore, Danaus plexippus. Ecological Entomology, 40 ( 2 ), 123 – 132. https://doi.org/10.1111/een.12168 | |
dc.identifier.citedreference | Tylianakis, J. M., Didham, R. K., Bascompte, J., & Wardle, D. A. ( 2008 ). Global change and species interactions in terrestrial ecosystems. Ecology Letters, 11 ( 12 ), 1351 – 1363. https://doi.org/10.1111/j.1461-0248.2008.01250.x | |
dc.identifier.citedreference | Urquhart, F. A., & Urquhart, N. R. ( 1978 ). Autumnal migration routes of the eastern population of the monarch butterfly (Danaus p. plexippus L.; Danaidae; Lepidoptera) in North America to the overwintering site in the Neovolcanic Plateau of Mexico. Canadian Journal of Zoology, 56 ( 8 ), 1759 – 1764. https://doi.org/10.1139/z78-240 | |
dc.identifier.citedreference | Vannette, R. L., & Hunter, M. D. ( 2011 ). Genetic variation in expression of defense phenotype may mediate evolutionary adaptation of Asclepias syriaca to elevated CO 2. Global Change Biology, 17 ( 3 ), 1277 – 1288. https://doi.org/10.1111/j.1365-2486.2010.02316.x | |
dc.identifier.citedreference | Zavala, J. A., Nabity, P. D., & DeLucia, E. H. ( 2013 ). An emerging understanding of mechanisms governing insect herbivory under elevated CO 2. Annual Review of Entomology, 58, 79 – 97. https://doi.org/10.1146/annurev-ento-120811-153544 | |
dc.identifier.citedreference | Zehnder, C. B., & Hunter, M. D. ( 2009 ). More is not necessarily better: The impact of limiting and excessive nutrients on herbivore population growth rates. Ecological Entomology, 34 ( 4 ), 535 – 543. https://doi.org/10.1111/j.1365-2311.2009.01101.x | |
dc.identifier.citedreference | Agrawal, A. A., Ali, J. G., Rasmann, S., & Fishbein, M. ( 2015 ). Macroevolutionary trends in the defense of milkweeds against monarchs. In K. S. Oberhauser, K. R. Nail, & S. Altizer (Eds.), Monarchs in a changing world: Biology and conservation of an iconic butterfly (pp. 47 – 59 ). Ithaca, NY: Cornell University Press. | |
dc.identifier.citedreference | Agrawal, A. A., Petschenka, G., Bingham, R. A., Weber, M. G., & Rasmann, S. ( 2012 ). Toxic cardenolides: Chemical ecology and coevolution of specialized plant‐herbivore interactions. New Phytologist, 194 ( 1 ), 28 – 45. https://doi.org/10.1111/j.1469-8137.2011.04049.x | |
dc.identifier.citedreference | Altizer, S., Bartel, R., & Han, B. A. ( 2011 ). Animal migration and infectious disease risk. Science (New York, N.Y.), 331 ( 6015 ), 296 – 302. https://doi.org/10.1126/science.1194694 | |
dc.identifier.citedreference | Altizer, S., & Davis, A. K. ( 2010 ). Populations of monarch butterflies with different migratory behaviors show divergence in wing morphology. Evolution, 64, 1018 – 1028. https://doi.org/10.1111/j.1558-5646.2009.00946.x | |
dc.identifier.citedreference | Altizer, S., Hobson, K. A., Davis, A. K., De Roode, J. C., & Wassenaar, L. I. ( 2015 ). Do healthy monarchs migrate farther? Tracking natal origins of parasitized vs. uninfected monarch butterflies overwintering in Mexico. PLoS ONE, 10 ( 11 ), e0141371. https://doi.org/10.1371/journal.pone.0141371 | |
dc.identifier.citedreference | Anderson, M. J. ( 2001 ). A new method for non parametric multivariate analysis of variance. Austral Ecology, 26 ( 2001 ), 32 – 46. https://doi.org/10.1111/j.1442-9993.2001.01070. pp. x | |
dc.identifier.citedreference | Awmack, C. S., & Leather, S. R. ( 2002 ). Host plant quality and fecundity in herbivorous insects. Annual Review of Entomology, 47 ( 1 ), 817 – 844. https://doi.org/10.1146/annurev.ento.47.091201.145300 | |
dc.identifier.citedreference | Bartel, R. A., Oberhauser, K. S., de Roode, J. C., & Altizer, S. M. ( 2011 ). Monarch butterfly migration and parasite transmission in eastern North America. Ecology, 92 ( 2 ), 342 – 351. https://doi.org/10.1890/10-0489.1 | |
dc.identifier.citedreference | Benítez, H. A., Vargas, H. A., & Püschel, T. A. ( 2015 ). Left–right asymmetry and morphological consequences of a host shift in the oligophagous Neotropical moth Macaria mirthae (Lepidoptera: Geometridae). Journal of Insect Conservation, 19 ( 3 ), 589 – 598. https://doi.org/10.1007/s10841-015-9779-0 | |
dc.identifier.citedreference | Berns, A., Zelditch, M. L., & Hunter, M. D. ( 2014 ). A geometric morphometric analysis of wing shape variation in monarch butterflies Danaus plexippus. Ann Arbor, MI: University of Michigan. | |
dc.identifier.citedreference | Berwaerts, K., Van Dyck, H., & Aerts, P. ( 2002 ). Does flight morphology relate to flight performance? An experimental test with the butterfly Pararge aegeria. Functional Ecology, 16 ( 4 ), 484 – 491. https://doi.org/10.1046/j.1365-2435.2002.00650.x | |
dc.identifier.citedreference | Boggs, C. L., & Freeman, K. D. ( 2005 ). Larval food limitation in butterflies: Effects on adult resource allocation and fitness. Oecologia, 144 ( 3 ), 353 – 361. https://doi.org/10.1007/s00442-005-0076-6 | |
dc.identifier.citedreference | Bowers, M. D., & Collinge, S. K. ( 1992 ). Fate of iridoid glycosides in different life stages of the Buckeye, Junonia coenia (Lepidoptera: Nymphalidae). Journal of Chemical Ecology, 18 ( 6 ), 817 – 831. https://doi.org/10.1007/BF00988322 | |
dc.identifier.citedreference | Bradley, C. A., & Altizer, S. ( 2005 ). Parasites hinder monarch butterfly flight: Implications for disease spread in migratory hosts. Ecology Letters, 8 ( 3 ), 290 – 300. https://doi.org/10.1111/j.1461-0248.2005.00722.x | |
dc.identifier.citedreference | Brower, L. P., & Malcolm, S. B. ( 1991 ). Animal migrations: Endangered phenomena. American Zoologist, 31 ( 1 ), 265 – 276. https://doi.org/10.1093/icb/31.1.265 | |
dc.identifier.citedreference | Camara, M. D. ( 1997 ). Physiological mechanisms underlying the costs of chemical defence in Junonia coenia Hubner (Nymphalidae): A gravimetric and quantitative genetic analysis. Evolutionary Ecology, 11 ( 4 ), 451 – 469. https://doi.org/10.1023/A:1018436908073 | |
dc.identifier.citedreference | Chen, F., Ge, F., & Parajulee, M. N. ( 2005 ). Impact of elevated CO 2 on tri‐trophic interaction of Gossypium hirsutum, Aphis gossypii, and Leis axyridis. Environmental Entomology, 34 ( 1 ), 37 – 46. https://doi.org/10.1603/0046-225X-34.1.37 | |
dc.identifier.citedreference | Crawley, M. J. ( 2012 ). Statistical modelling. The R book. Chichester, UK: John Wiley & Sons, Ltd. https://doi.org/10.1002/9781118448908.ch9 | |
dc.identifier.citedreference | Davis, A. K., & de Roode, J. C. ( 2018 ). Effects of the parasite, Ophryocystis elektroscirrha, on wing characteristics important for migration in the monarch butterfly. Animal Migration, 84 – 93. | |
dc.identifier.citedreference | de Roode, J. C., Chi, J., Rarick, R. M., & Altizer, S. ( 2009 ). Strength in numbers: High parasite burdens increase transmission of a protozoan parasite of monarch butterflies ( Danaus plexippus ). Oecologia, 161 ( 1 ), 67 – 75. https://doi.org/10.1007/s00442-009-1361-6 | |
dc.identifier.citedreference | de Roode, J. C., Gold, L. R., & Altizer, S. M. ( 2007 ). Virulence determinants in a natural butterfly‐parasite system. Parasitology, 134 ( 05 ), 657. https://doi.org/10.1017/S0031182006002009 | |
dc.identifier.citedreference | de Roode, J. C., Pedersen, A. B., Hunter, M. D., & Altizer, S. ( 2008 ). Host plant species affects virulence in monarch butterfly parasites. Journal of Animal Ecology, 77 ( 1 ), 120 – 126. https://doi.org/10.1111/j.1365-2656.2007.01305.x | |
dc.identifier.citedreference | Decker, L. E., de Roode, J. C., & Hunter, M. D. ( 2018 ). Elevated atmospheric concentrations of carbon dioxide reduce monarch tolerance and increase parasite virulence by altering the medicinal properties of milkweeds. Ecology Letters, 21 ( 9 ), 1353 – 1363. https://doi.org/10.1111/ele.13101 | |
dc.identifier.citedreference | Decker, L. E., Soule, A. J., de Roode, J. C., & Hunter, M. D. ( 2018 ). Data from: Phytochemical changes in milkweed induced by elevated CO2 alter wing morphology but not toxin sequestration in monarch butterflies. Dryad Digital Repository https://doi.org/10.5061/dryad.mk3tj78 | |
dc.identifier.citedreference | Docherty, M., Hurst, D. K., Holopainen, J. K., Whittaker, J. B., Lea, P. J., & Watt, A. D. ( 1996 ). Carbon dioxide‐induced changes in beech foliage cause female beech weevil larvae to feed in a compensatory manner. Global Change Biology, 2 ( 4 ), 335 – 341. https://doi.org/10.1111/j.1365-2486.1996.tb00085.x | |
dc.identifier.citedreference | Drake, B. G., Gonzalez‐Meler, M. A., & Long, S. P. ( 1997 ). More efficient plants: A consequence of rising atmospheric CO 2 ? Annual Review of Plant Physiology and Plant Molecular Biology, 48, 609 – 639. https://doi.org/10.1146/annurev.arplant.48.1.609 | |
dc.identifier.citedreference | Drake, B. G., Leadley, P. W., Arp, W. J., Nassiry, D., & Curtis, P. S. ( 1989 ). An open top chamber for field studies of elevated atmospheric CO 2 concentration on saltmarsh vegetation. Functional Ecology, 3 ( 3 ), 363. https://doi.org/10.2307/2389377 | |
dc.identifier.citedreference | Dudley, R. ( 2002 ). The biomechanics of insect flight: Form, function, evolution. Princeton, NJ: Princeton University Press. | |
dc.identifier.citedreference | Dudley, R., & Srygley, R. B. ( 2008 ). Airspeed adjustment and lipid reserves in migratory Neotropical butterflies. Functional Ecology, 22 ( 2 ), 264 – 270. https://doi.org/10.1111/j.1365-2435.2007.01364.x | |
dc.identifier.citedreference | Dyer, L. A., & Deane Bowers, M. ( 1996 ). The importance of sequestered iridoid glycosides as a defense against an ant predator. Journal of Chemical Ecology, 22 ( 8 ), 1527 – 1539. https://doi.org/10.1007/BF02027729 | |
dc.identifier.citedreference | Dyer, L. A., Richards, L. A., Short, S. A., & Dodson, C. D. ( 2013 ). Effects of CO 2 and temperature on tritrophic interactions. PLoS ONE, 8 ( 4 ), e62528. https://doi.org/10.1371/journal.pone.0062528 | |
dc.identifier.citedreference | Facey, S. L., Ellsworth, D. S., Staley, J. T., Wright, D. J., & Johnson, S. N. ( 2014 ). Upsetting the order: How climate and atmospheric change affects herbivore–enemy interactions. Current Opinion in Insect Science, 5, 66 – 74. https://doi.org/10.1016/J.COIS.2014.09.015 | |
dc.identifier.citedreference | Fink, L. S., & Brower, L. P. ( 1981 ). Birds can overcome the cardenolide defence of monarch butterflies in Mexico. Nature, 291, 67 – 70. | |
dc.identifier.citedreference | Flockhart, D. T., Fitz‐gerald, B., Brower, L. P., Derbyshire, R., Altizer, S., Hobson, K. A., … Norris, D. R. ( 2017 ). Migration distance as a selective episode for wing morphology in a migratory insect. Movement Ecology, 5 ( 1 ), 7. https://doi.org/10.1186/s40462-017-0098-9 | |
dc.identifier.citedreference | Garland, M. S., & Davis, A. K. ( 2002 ). An Examination of monarch butterfly ( Danaus plexippus ) autumn migration in coastal Virginia. The American Midland Naturalist, 147 ( 1 ), 170 – 174. https://doi.org/10.1674/0003-0031(2002) 147[0170:AEOMBD]2.0.CO;2 | |
dc.identifier.citedreference | Gibo, D. L. ( 1986 ). Flight strategies of migrating monarch butterflies ( Danaus plexippus L.) in Southern Ontario, 172–184. Proceedings in Life Sciences, 172 – 184. https://doi.org/10.1007/978-3-642-71155-8_12 | |
dc.identifier.citedreference | Gibo, D. L., & Pallett, M. J. ( 1979 ). Soaring flight of monarch butterflies, Danaus plexippus (Lepidoptera: Danaidae), during the late summer migration in southern Ontario. Canadian Journal of Zoology, 57 ( 7 ), 1393 – 1401. https://doi.org/10.1139/z79-180 | |
dc.identifier.citedreference | Gilman, S. E., Urban, M. C., Tewksbury, J., Gilchrist, G. W., & Holt, R. D. ( 2010 ). A framework for community interactions under climate change. Trends in Ecology & Evolution, 25 ( 6 ), 325 – 331. https://doi.org/10.1016/J.TREE.2010.03.002 | |
dc.identifier.citedreference | Greeney, H., Dyer, L., & Smilanich, A. ( 2012 ). Feeding by lepidopteran larvae is dangerous: A review of caterpillars’ chemical, physiological, morphological, and behavioral defenses against natural enemies. ISJ, 9, 7 – 34. | |
dc.identifier.citedreference | Hentley, W. T., Vanbergen, A. J., Hails, R. S., Jones, T. H., & Johnson, S. N. ( 2014 ). Elevated atmospheric CO 2 impairs aphid escape responses to predators and conspecific alarm signals. Journal of Chemical Ecology, 40 ( 10 ), 1110 – 1114. https://doi.org/10.1007/s10886-014-0506-1 | |
dc.identifier.citedreference | Hunter, M. D. ( 2001 ). Effects of elevated atmospheric carbon dioxide on insect‐plant interactions. Agricultural and Forest Entomology, 3 ( 3 ), 153 – 159. https://doi.org/10.1046/j.1461-9555.2001.00108.x | |
dc.identifier.citedreference | Hunter, M. D. ( 2016 ). The phytochemical landscape: Linking trophic interactions and nutrient dynamics. Princeton, NJ: Princeton University Press. | |
dc.identifier.citedreference | Jamieson, M. A., Burkle, L. A., Manson, J. S., Runyon, J. B., Trowbridge, A. M., & Zientek, J. ( 2017 ). Global change effects on plant–insect interactions: The role of phytochemistry. Current Opinion in Insect Science, 23, 70 – 80. https://doi.org/10.1016/J.COIS.2017.07.009 | |
dc.identifier.citedreference | Johnson, H., Solensky, M. J., Satterfield, D. A., & Davis, A. K. ( 2014 ). Does skipping a meal matter to a butterfly’s appearance? Effects of larval food stress on wing morphology and color in monarch butterflies. PLoS ONE, 9 ( 4 ), 1 – 9. https://doi.org/10.1371/journal.pone.0093492 | |
dc.identifier.citedreference | Johnson, S. N., Lopaticki, G., & Hartley, S. E. ( 2014 ). Elevated atmospheric CO 2 triggers compensatory feeding by root herbivores on a C3 but not a C4 grass. PLoS ONE, 9 ( 3 ), e90251. https://doi.org/10.1371/journal.pone.0090251 | |
dc.identifier.citedreference | Kerlinger, P. ( 1989 ). Flight strategies of migrating hawks. Chicago, IL: University of Chicago Press. | |
dc.identifier.citedreference | Klaiber, J., Dorn, S., & Najar‐Rodriguez, A. J. ( 2013 ). Acclimation to elevated CO 2 increases constitutive glucosinolate levels of brassica plants and affects the performance of specialized herbivores from contrasting feeding guilds. Journal of Chemical Ecology, 39 ( 5 ), 653 – 665. https://doi.org/10.1007/s10886-013-0282-3 | |
dc.identifier.citedreference | Klaiber, J., Najar‐Rodriguez, A. J., Dialer, E., & Dorn, S. ( 2013 ). Elevated carbon dioxide impairs the performance of a specialized parasitoid of an aphid host feeding on Brassica plants. Biological Control, 66 ( 1 ), 49 – 55. https://doi.org/10.1016/J.BIOCONTROL.2013.03.006 | |
dc.identifier.citedreference | Kovac, M., Vogt, D., Ithier, D., Smith, M., & Wood, R. ( 2012 ). Aerodynamic evaluation of four butterfly species for the design of flapping‐gliding robotic insects. In 2012 IEEE/RSJ International Conference on Intelligent Robots and Systems (pp. 1102 – 1109 ). IEEE. https://doi.org/10.1109/IROS.2012.6385453 | |
dc.identifier.citedreference | Li, Y., Pierce, A. A., & de Roode, J. C. ( 2016 ). Variation in forewing size linked to migratory status in monarch butterflies. Animal Migration, 3 ( 1 ), 27 – 34. https://doi.org/10.1515/ami-2016-0003 | |
dc.identifier.citedreference | Lincoln, D. E., Sionit, N., & Strain, B. R. ( 1984 ). Growth and feeding response of Pseudoplusia includens (Lepidoptera: Noctuidae) to host plants grown in controlled carbon dioxide atmospheres. Environmental Entomology, 13 ( 6 ), 1527 – 1530. https://doi.org/10.1093/ee/13.6.1527 | |
dc.identifier.citedreference | Littell, R. R., Stroup, W. W., & Freund, R. J. ( 2002 ). SAS for linear models (Fourth). Cary, NC: SAS institute. | |
dc.owningcollname | Interdisciplinary and Peer-Reviewed |
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