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BY-NC-ND 4.0 license Open Access Published by De Gruyter Open Access December 13, 2018

Alternate migration strategies of eastern monarch butterflies revealed by stable isotopes

Hannah B. Vander Zanden, Carol L. Chaffee, Antonio González-Rodríguez, D.T. Tyler Flockhart, D. Ryan Norris and Marta L. Wayne
From the journal Animal Migration

Abstract

Alternative life history strategies are mechanisms by which organisms are able to maximize fitness across a range of environmental conditions. Fitness is maximized by different strategies depending on context, resulting in trade-offs between life history strategies. Monarch butterflies (Danaus plexippus) employ both migratory and resident life history strategies. Since residents breed throughout the year, but migrants overwinter in reproductive diapause, there are fitness trade-offs between the two strategies. We used stable isotope analysis to evaluate the geographic origins of monarchs in a yearround population in south Florida. Based on stable isotope profiles of hydrogen and carbon (δ2H and δ13C values), we found that 48% (16/33) of monarchs collected in south Florida are migrants that originated from outside the sampling region. Migrants had a larger wing length than residents; thus, switching to a resident strategy could alter their probability of reproductive success. Further work is needed to investigate the mechanism underlying this pattern, but these findings show that alternate life history strategies and sex-specific behaviors are underexplored factors influencing monarch migration and evolution.

References

[1] Grönroos J., Green M., Alerstam T., To fly or not to fly depending on winds: shorebird migration in different seasonal wind regimes, Anim. Behav., 2012, 83, 1449-145710.1016/j.anbehav.2012.03.017Search in Google Scholar

[2] Vande Velde L., Van Dyck H., Lipid economy, flight activity and reproductive behaviour in the speckled wood butterfly: on the energetic cost of territory holding, Oikos, 2013, 122, 555-56210.1111/j.1600-0706.2012.20747.xSearch in Google Scholar

[3] Judge K.A., Ting J.J., Gwynne D.T., Condition dependence of male life span and calling effort in a field cricket, Evolution, 2008, 62, 868-87810.1111/j.1558-5646.2008.00318.xSearch in Google Scholar

[4] Leary C.J., Fox D.J., Shepard D.B., Garcia A.M., Body size, age, growth and alternative mating tactics in toads: satellite males are smaller but not younger than calling males, Anim. Behav., 2005, 70, 663-67110.1016/j.anbehav.2004.12.013Search in Google Scholar

[5] Greenfield M.D., Shelly T.E., Alternative mating strategies in a desert grasshopper: evidence of density-dependence, Anim. Behav., 1985, 33, 1192-121010.1016/S0003-3472(85)80180-9Search in Google Scholar

[6] Smith M.D., Schrank H.E., Brockmann H.J., Measuring the costs of alternative reproductive tactics in horseshoe crabs, Limulus polyphemus, Anim. Behav., 2013, 85, 165-17310.1016/j.anbehav.2012.10.021Search in Google Scholar

[7] Hews D.K., Knapp R., Moore M.C., Early exposure to androgens affects adult expression of alternative male types in tree lizards, Horm. Behav., 1994, 28, 96-11510.1006/hbeh.1994.1008Search in Google Scholar PubMed

[8] Páez D.J., Brisson-Bonenfant C., Rossignol O., Guderley H.E., Bernatchez L., Dodson J.J., Alternative developmental pathways and the propensity to migrate: a case study in the Atlantic salmon, J. Evol. Biol., 2011, 24, 245-25510.1111/j.1420-9101.2010.02159.xSearch in Google Scholar PubMed

[9] Chapman B.B., Brönmark C., Nilsson J.-Å., Hansson L.-A., The ecology and evolution of partial migration, Oikos, 2011, 120, 1764-177510.1111/j.1600-0706.2011.20131.xSearch in Google Scholar

[10] Semmens B.X., Semmens D.J., Thogmartin W.E., Wiederholt R., López-Hoffman L., Diffendorfer J.E., et al., Quasi-extinction risk and population targets for the Eastern, migratory population of monarch butterflies (Danaus plexippus), Sci. Rep., 2016, 6, 2326510.1038/srep23265Search in Google Scholar PubMed PubMed Central

[11] Flockhart D.T.T., Pichancourt J.-B., Norris D.R., Martin T.G., Unravelling the annual cycle in a migratory animal: breedingseason habitat loss drives population declines of monarch butterflies, J. Anim. Ecol., 2015, 84, 155-16510.1111/1365-2656.12253Search in Google Scholar PubMed

[12] Pleasants J.M., Oberhauser K.S., Milkweed loss in agricultural fields because of herbicide use: effect on the monarch butterfly population, Insect Conserv. Divers., 2013, 6, 135-14410.1111/j.1752-4598.2012.00196.xSearch in Google Scholar

[13] Pleasants J., Milkweed restoration in the Midwest for monarch butterfly recovery: estimates of milkweeds lost, milkweeds remaining and milkweeds that must be added to increase the monarch population, Insect Conserv. Divers., 201610.1111/icad.12198Search in Google Scholar

[14] Inamine H., Ellner S.P., Springer J.P., Agrawal A.A., Linking the continental migratory cycle of the monarch butterfly to understand its population decline, Oikos, 2016, 125, 1081-109110.1111/oik.03196Search in Google Scholar

[15] Agrawal A.A., Inamine H., Mechanisms behind the monarch’s decline, Science, 2018, 360, 1294-129610.1126/science.aat5066Search in Google Scholar PubMed

[16] Oberhauser K., Wiederholt R., Diffendorfer J.E., Semmens D., Ries L., Thogmartin W.E., et al., A trans-national monarch butterfly population model and implications for regional conservation priorities, Ecol. Entomol., 2017, 42, 51-6010.1111/een.12351Search in Google Scholar

[17] Goehring L., Oberhauser K.S., Effects of photoperiod, temperature, and host plant age on induction of reproductive diapause and development time in Danaus plexippus, Ecol. Entomol., 2002, 27, 674-68510.1046/j.1365-2311.2002.00454.xSearch in Google Scholar

[18] Urquhart F.A., Urquhart N.R., Overwintering areas and migratory routes of the monarch butterfly (Danaus p. plexippus, Lepidoptera: Danaidae) in North America, with special reference to the western population, Can. Entomol., 1977, 109, 1583-158910.4039/Ent1091583-12Search in Google Scholar

[19] Pyle R.M., Chasing Monarchs: Migrating with the Butterflies of Passage, Houghton Mifflin Co., 1999Search in Google Scholar

[20] Dockx C., Directional and stabilizing selection on wing size and shape in migrant and resident monarch butterflies, Danaus plexippus (L.), in Cuba, Biol. J. Linn. Soc., 2007, 92, 605-61610.1111/j.1095-8312.2007.00886.xSearch in Google Scholar

[21] Knight A., Brower L.P., The influence of Eastern North American autumnal migrant monarch butterflies (Danaus plexippus L.) on continuously breeding resident monarch populations in southern Florida, J. Chem. Ecol., 2009, 35, 816-82310.1007/s10886-009-9655-zSearch in Google Scholar PubMed

[22] Howard E., Aschen H., Davis A.K., Citizen science observations of monarch butterfly overwintering in the southern United States, Psyche J. Entomol., 201010.1155/2010/689301Search in Google Scholar

[23] Zalucki M.P., Rochester W.A., Estimating the effect of climate on the distribution and abundance of Danaus plexippus: a tale of two continents, In: Hoth, J., Merino, L., Oberhauser, K.S., Pisanty, I., Price, S., Wilkinson, T. (Eds.), Proceedings of the North American Conference on the Monarch Butterfly, Commission for Environmental Cooperation, Montreal, Canada, 1999, 151-163Search in Google Scholar

[24] Zhan S., Zhang W., Niitepõld K., Hsu J., Haeger J.F., Zalucki M.P., et al., The genetics of monarch butterfly migration and warning colouration, Nature, 2014, 514, 317-32110.1038/nature13812Search in Google Scholar PubMed PubMed Central

[25] Brower L.P., Studies on the migration of the monarch butterfly I. Breeding populations of Danaus plexippus and D. gilippus berenice in south central Florida, Ecology, 1961, 42, 76-8310.2307/1933269Search in Google Scholar

[26] Urquhart F.A., Urquhart N.R., Aberrant autumnal migration of the eastern population of the monarch butterfly, Danaus plexippus plexippus (Lepidoptera: Danaidae) as it relates to the occurrence of strong westerly winds, Can. Entomol., 1979, 111, 1281-128610.4039/Ent1111281-11Search in Google Scholar

[27] Knight A., A Population Study of Monarch Butterflies in North- Central and South Florida, Master thesis, : University of Florida, Gainesville, FL, 1998.Search in Google Scholar

[28] Dockx C., Migration of the North American Monarch, Danaus plexippus, to Cuba, Dissertation, : University of Florida, Gainesville, FL, 2002.Search in Google Scholar

[29] Hobson K.A., Wassenaar L.I. (Eds.), Tracking animal migration with stable isotopes, Elsevier, Amsterdam, 2008Search in Google Scholar

[30] Wassenaar L.I., Hobson K.A., Natal origins of migratory monarch butterflies at wintering colonies in Mexico: New isotopic evidence, Proc. Natl. Acad. Sci., 1998, 95, 15436-1543910.1073/pnas.95.26.15436Search in Google Scholar PubMed PubMed Central

[31] Hobson K.A., Wassenaar L.I., Taylor O.R., Stable isotopes (δD and δ13C) are geographic indicators of natal origins of monarch butterflies in eastern North America, Oecologia, 1999, 120, 397-40410.1007/s004420050872Search in Google Scholar PubMed

[32] Bowen G.J., Statistical and geostatistical mapping of precipitation water isotope ratios, In: West, J.B., Bowen, G.J., Dawson, T.E., Tu, K.P. (Eds.), Isoscapes: Understanding Movement, Pattern, and Process on Earth through Isotope Mapping, Springer, New York, 2010, 139-160Search in Google Scholar

[33] Suits N.S., Denning A.S., Berry J.A., Still C.J., Kaduk J., Miller J.B., et al., Simulation of carbon isotope discrimination of the terrestrial biosphere, Glob. Biogeochem. Cycles, 2005, 1910.1029/2003GB002141Search in Google Scholar

[34] Altizer S., Davis A.K., Populations of monarch butterflies with different migratory behaviors show divergence in wing morphology, Evolution, 2010, 64, 1018-102810.1111/j.1558-5646.2010.00946.xSearch in Google Scholar PubMed

[35] Li Y., Pierce A.A., de R.J.C., Variation in forewing size linked to migratory status in monarch butterflies, Anim. Migr., 2016, 3, 27-3410.1515/ami-2016-0003Search in Google Scholar

[36] Hobson K., Plint T., Serrano E.G., Alvarez X.M., Ramirez I., Longstaffe F., Within-wing isotopic (δ2H, δ13C, δ15N) variation of monarch butterflies: implications for studies of migratory origins and diet, Anim. Migr., 2017, 4, 8-1410.1515/ami-2017-0002Search in Google Scholar

[37] Wassenaar L.I., Hobson K.A., Comparative equilibration and online technique for determination of non-exchangeable hydrogen of keratins for use in animal migration studies, Isotopes Environ. Health Stud., 2003, 39, 211-21710.1080/1025601031000096781Search in Google Scholar

[38] Bowen G.J., Wassenaar L.I., Hobson K.A., Global application of stable hydrogen and oxygen isotopes to wildlife forensics, Oecologia, 2005, 143, 337-34810.1007/s00442-004-1813-ySearch in Google Scholar

[39] Flockhart D.T.T., Wassenaar L.I., Martin T.G., Hobson K.A., Wunder M.B., Norris D.R., Tracking multi-generational colonization of the breeding grounds by monarch butterflies in eastern North America, Proc. R. Soc. B Biol. Sci., 2013, 280, 2013108710.1098/rspb.2013.1087Search in Google Scholar

[40] Miller N.G., Wassenaar L.I., Hobson K.A., Norris D.R., Monarch butterflies cross the Appalachians from the west to recolonize the east coast of North America, Biol. Lett., 2011, 7, 43-4610.1098/rsbl.2010.0525Search in Google Scholar

[41] R Core Team, R: A language and environment for statistical computing, R Foundation for Statistical Computing, Vienna, Austria, 2016Search in Google Scholar

[42] Flockhart D.T.T., Brower L.P., Ramirez M.I., Hobson K.A., Wassenaar L.I., Altizer S., et al., Regional climate on the breeding grounds predicts variation in the natal origin of monarch butterflies overwintering in Mexico over 38 years, Glob. Change Biol., 2017, 23, 2565-257610.1111/gcb.13589Search in Google Scholar

[43] Dockx C., Brower L.P., Wassenaar L.I., Hobson K.A., Do North American monarch butterflies travel to Cuba? Stable isotope and chemical tracer techniques, Ecol. Appl., 2004, 14, 1106-111410.1890/03-5128Search in Google Scholar

[44] Dockx C., Differences in phenotypic traits and migratory strategies between eastern North American monarch butterflies, Danaus plexippus (L.), Biol. J. Linn. Soc., 2012, 106, 717-73610.1111/j.1095-8312.2012.01916.xSearch in Google Scholar

[45] Lack D., The problem of partial migration, Br. Birds, 1943, 37, 122-130Search in Google Scholar

[46] Lundberg P., The evolution of partial migration in Birds, Trends Ecol. Evol., 1988, 3, 172-17510.1016/0169-5347(88)90035-3Search in Google Scholar

[47] Mysterud A., Loe L.E., Zimmermann B., Bischof R., Veiberg V., Meisingset E., Partial migration in expanding red deer populations at northern latitudes - a role for density dependence?, Oikos, 2011, 120, 1817-182510.1111/j.1600-0706.2011.19439.xSearch in Google Scholar

[48] Chapman B.B., Skov C., Hulthén K., Brodersen J., Nilsson P.A., Hansson L.-A., et al., Partial migration in fishes: definitions, methodologies and taxonomic distribution, J. Fish Biol., 2012, 81, 479-49910.1111/j.1095-8649.2012.03349.xSearch in Google Scholar PubMed

[49] Daniels J.C., Seasonal variation in the little sulphur butterfly, Eurema lisa lisa, in central Florida: how it compares to other sympatric Eurema species (Lepidoptera: Pieridae), Holarct. Lepidoptera, 1995, 2, 59-65Search in Google Scholar

[50] Ladner D.T., Altizer S., Oviposition preference and larval performance of North American monarch butterflies on four Asclepias species, Entomol. Exp. Appl., 2005, 116, 9-2010.1111/j.1570-7458.2005.00308.xSearch in Google Scholar

[51] Atterholt A.L., Solensky M.J., Effects of larval rearing density and food availability on adult size and coloration in monarch butterflies (Lepidoptera: Nymphalidae), J. Entomol. Sci., 2010, 45, 366-37710.18474/0749-8004-45.4.366Search in Google Scholar

[52] Brower L.P., Fink L.S., Walford P., Fueling the fall migration of the monarch butterfly, Integr. Comp. Biol., 2006, 46, 1123-114210.1093/icb/icl029Search in Google Scholar

[53] Flockhart D.T.T., Fitz-gerald B., Brower L.P., Derbyshire R., Altizer S., Hobson K.A., et al., Migration distance as a selective episode for wing morphology in a migratory insect, Mov. Ecol., 2017, 5, 710.1186/s40462-017-0098-9Search in Google Scholar

[54] Yang L.H., Ostrovsky D.M., Rogers M.C., Welker J.M., Intrapopulation variation in the natal origins and wing morphology of overwintering western monarch butterflies (Danaus plexippus), Ecography, 2015, 39, 998-100710.1111/ecog.01994Search in Google Scholar

[55] Davis A.K., Cope N., Smith A., Solensky M.J., Wing color predicts future mating success in male monarch butterflies, Ann. Entomol. Soc. Am., 2007, 100, 339-34410.1603/0013-8746(2007)100[339:WCPFMS]2.0.CO;2Search in Google Scholar

[56] Van Hook T., Monarch butterfly mating ecology at a Mexican overwintering site : proximate causes of non-random mating, Dissertation, University of Florida, Gainesville, FL, 1996.Search in Google Scholar

[57] Alonso-Mejía A., Rendon-Salinas E., Montesinos-Patiño E., Brower L.P., Use of lipid reserves by monarch butterflies overwintering in Mexico: implications for conservation, Ecol. Appl., 1997, 7, 934-94710.1890/1051-0761(1997)007[0934:UOLRBM]2.0.CO;2Search in Google Scholar

[58] Oberhauser K.S., Male monarch butterfly spermatophore mass and mating strategies, Anim. Behav., 1988, 36, 1384-138810.1016/S0003-3472(88)80208-2Search in Google Scholar

[59] Oberhauser K.S., Effects of spermatophores on male and female monarch butterfly reproductive success, Behav. Ecol. Sociobiol., 1989, 25, 237-24610.1007/BF00300049Search in Google Scholar

[60] Altizer S.M., Oberhauser K.S., Brower L.P., Associations between host migration and the prevalence of a protozoan parasite in natural populations of adult monarch butterflies, Ecol. Entomol., 2000, 25, 125-13910.1046/j.1365-2311.2000.00246.xSearch in Google Scholar

[61] McLaughlin R.E., Myers J., Ophryocystis elektroscirrha sp. n., a neogregarine pathogen of the monarch butterfly Danaus plexippus (L.) and the Florida queen butterfly D. gilippus berenice Cramer, J. Protozool., 1970, 17, 300-30510.1111/j.1550-7408.1970.tb02375.xSearch in Google Scholar

[62] Leong K.L.H., Yoshimura M.A., Kaya H.K., Williams H., Instar susceptibility of the monarch butterfly (Danaus plexippus) to the neogregarine parasite, Ophryocystis elektroscirrha, J. Invertebr. Pathol., 1997, 69, 79-8310.1006/jipa.1996.4634Search in Google Scholar PubMed

[63] Altizer S.M., Oberhauser K.S., Geurts K.A., Transmission of the protozoan parasite, Ophryocystis elektroscirrha, in monarch butterfly populations: implications for prevalence and population-level impacts, In: Oberhauser, K.S., Solensky, M. (Eds.), The Monarch Butterfly: Biology and Conservation, Cornell University Press, Ithaca, NY, 2004, 203-218Search in Google Scholar

[64] Altizer S.M., Oberhauser K.S., Effects of the protozoan parasite Ophryocystis elektroscirrha on the fitness of monarch butterflies (Danaus plexippus), J. Invertebr. Pathol., 1999, 74, 76-8810.1006/jipa.1999.4853Search in Google Scholar PubMed

[65] Mongue A.J., Tsai M.V., Wayne M.L., Roode J.C. de, Inbreeding depression in monarch butterflies, J. Insect Conserv., 2016, 20, 477-48310.1007/s10841-016-9880-zSearch in Google Scholar

[66] Altizer S., Bartel R., Han B.A., Animal migration and infectious disease risk, Science, 2011, 331, 296-30210.1126/science.1194694Search in Google Scholar PubMed

[67] Flockhart D.T.T., Dabydeen A., Satterfield D.A., Hobson K.A., Wassenaar L.I., Norris D.R., Patterns of parasitism in monarch butterflies during the breeding season in eastern North America, Ecol. Entomol., 2018, 43, 28-3610.1111/een.12460Search in Google Scholar

[68] Bartel R.A., Oberhauser K.S., Roode J.C. de, Altizer S.M., Monarch butterfly migration and parasite transmission in eastern North America, Ecology, 2011, 92, 342-35110.1890/10-0489.1Search in Google Scholar PubMed PubMed Central

[69] Satterfield D.A., Maerz J.C., Altizer S., Loss of migratory behaviour increases infection risk for a butterfly host, Proc. R. Soc. Lond. B Biol. Sci., 2015, 282, 2014173410.1098/rspb.2014.1734Search in Google Scholar PubMed PubMed Central

[70] Monarch Watch: Dedicated to Education, Conservation & Research. Monarch Watch, 2016Search in Google Scholar

[71] Howard E., Davis A.K., Documenting the spring movements of monarch butterflies with Journey North, a citizen science program, In: Oberhauser, K.S., Solensky, M.J. (Eds.), The Monarch Butterfly: Biology & Conservation, Cornell University Press, Ithaca, NY, 2004, 105-114Search in Google Scholar

[72] Lyons J.I., Pierce A.A., Barribeau S.M., Sternberg E.D., Mongue A.J., De Roode J.C., Lack of genetic differentiation between monarch butterflies with divergent migration destinations, Mol. Ecol., 2012, 21, 3433-344410.1111/j.1365-294X.2012.05613.xSearch in Google Scholar PubMed

[73] Taborsky M., Brockmann H.J., Alternative reproductive tactics and life history phenotypes, In: Kappeler, P. (Ed.), Animal Behaviour: Evolution and Mechanisms, Springer Verlag, Berlin, 2010, 537-586.Search in Google Scholar

Received: 2018-06-08
Accepted: 2018-10-30
Published Online: 2018-12-13
Published in Print: 2018-12-01

© by Hannah B. Vander Zanden, et al., published by De Gruyter

This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 License.

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