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Species traits affect phenological responses to climate change in a butterfly community

  • 1.

    Parmesan, C. Influences of species, latitudes and methodologies on estimates of phenological response to global warming. Glob. Change Biol. 13, 1860–1872. https://doi.org/10.1111/j.1365-2486.2007.01404.x (2007).

    ADS  Article  Google Scholar 

  • 2.

    Peñuelas, J. et al. Evidence of current impact of climate change on life: A walk from genes to the biosphere. Glob. Change Biol. 19, 2303–2338. https://doi.org/10.1111/gcb.12143 (2013).

    ADS  Article  Google Scholar 

  • 3.

    Thackeray, S. J. et al. Trophic level asynchrony in rates of phenological change for marine, freshwater and terrestrial environments. Glob. Change Biol. 16, 3304–3313. https://doi.org/10.1111/j.1365-2486.2010.02165.x (2010).

    ADS  Article  Google Scholar 

  • 4.

    Dapporto, L. et al. Rise and fall of island butterfly diversity: Understanding genetic differentiation and extinction in a highly diverse archipelago. Divers. Distrib. 23, 1169–1181. https://doi.org/10.1111/ddi.12610 (2017).

    Article  Google Scholar 

  • 5.

    Hendry, A. P., Farrugia, T. J. & Kinnison, M. T. Human influences on rates of phenotypic change in wild animal populations. Mol. Ecol. 17, 20–29. https://doi.org/10.1111/j.1365-294X.2007.03428.x (2008).

    Article  PubMed  Google Scholar 

  • 6.

    Devictor, V. et al. Differences in the climatic debts of birds and butterflies at a continental scale. Nat. Clim. Change 2, 121–124. https://doi.org/10.1038/nclimate1347 (2012).

    ADS  Article  Google Scholar 

  • 7.

    Forister, M. L. & Shapiro, A. M. Climatic trends and advancing spring flight of butterflies in lowland California. Glob. Change Biol. 9, 1130–1135. https://doi.org/10.1046/j.1365-2486.2003.00643.x (2003).

    ADS  Article  Google Scholar 

  • 8.

    Altermatt, F. Tell me what you eat and I’ll tell you when you fly: Diet can predict phenological changes in response to climate change. Ecol. Lett. 13, 1475–1484. https://doi.org/10.1111/j.1461-0248.2010.01534.x (2010).

    Article  PubMed  Google Scholar 

  • 9.

    Stefanescu, C., Penuelas, J. & Filella, I. Effects of climatic change on the phenology of butterflies in the northwest Mediterranean Basin. Glob. Change Biol. 9, 1494–1506. https://doi.org/10.1046/j.1365-2486.2003.00682.x (2003).

    ADS  Article  Google Scholar 

  • 10.

    Roy, D. B. & Sparks, T. H. Phenology of British butterflies and climate change. Glob. Change Biol. 6, 407–416. https://doi.org/10.1046/j.1365-2486.2000.00322.x (2000).

    ADS  Article  Google Scholar 

  • 11.

    Diez, J. M. et al. Forecasting phenology: from species variability to community patterns. Ecol. Lett. 15, 545–553. https://doi.org/10.1111/j.1461-0248.2012.01765.x (2012).

    Article  PubMed  Google Scholar 

  • 12.

    Schweiger, O., Settele, J., Kudrna, O., Klotz, S. & Kühn, I. Climate change can cause spatial mismatch of trophically interacting species. Ecology 89, 3472–3479. https://doi.org/10.1890/07-1748.1 (2008).

    Article  PubMed  Google Scholar 

  • 13.

    Glazaczow, A., Orwin, D. & Bogdziewicz, M. Increased temperature delays the late-season phenology of multivoltine insect. Sci. Rep. https://doi.org/10.1038/srep38022 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  • 14.

    van der Kolk, H.-J., WallisDeVries, M. F. & van Vliet, A. J. H. Using a phenological network to assess weather influences on first appearance of butterflies in the Netherlands. Ecol. Indicators 69, 205–212, https://doi.org/10.1016/j.ecolind.2016.04.028 (2016).

  • 15.

    Zografou, K. et al. Signals of climate change in butterfly communities in a mediterranean protected area. PLoS ONE 9, e87245. https://doi.org/10.1371/journal.pone.0087245 (2014).

    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

  • 16.

    Visser, M. Keeping up with a warming world; assessing the rate of adaptation to climate change. Proc. Biol. Sci. R. Soc. 275, 649–659, https://doi.org/10.1098/rspb.2007.0997 (2008).

  • 17.

    Kharouba, H. M., Paquette, S. R., Kerr, J. T. & Vellend, M. Predicting the sensitivity of butterfly phenology to temperature over the past century. Glob. Change Biol. 20, 504–514. https://doi.org/10.1111/gcb.12429 (2014).

    ADS  Article  Google Scholar 

  • 18.

    Roy, D. B. et al. Similarities in butterfly emergence dates among populations suggest local adaptation to climate. Glob. Change Biol. 21, 3313–3322. https://doi.org/10.1111/gcb.12920 (2015).

    ADS  Article  Google Scholar 

  • 19.

    Rapacciuolo, G. et al. Beyond a warming fingerprint: Individualistic biogeographic responses to heterogeneous climate change in California. Glob. Change Biol. 20, 2841–2855. https://doi.org/10.1111/gcb.12638 (2014).

    ADS  Article  Google Scholar 

  • 20.

    Fischer, K. & Fiedler, K. Life-history plasticity in the butterfly Lycaena hippothoe: Local adaptations and trade-offs. Biol. J. Lin. Soc. 75, 173–185. https://doi.org/10.1046/j.1095-8312.2002.00014.x (2002).

    Article  Google Scholar 

  • 21.

    Zografou, K. Who flies first?—Habitat-specific phenological shifts of butterflies and orthopterans in the light of climate change: A case study from the south-east Mediterranean Lepidoptera and Orthoptera phenology change. Ecol. Entomol. 40, 562–574. https://doi.org/10.1111/een.12220 (2015).

    Article  Google Scholar 

  • 22.

    Suggitt Andrew, J. et al. Habitat microclimates drive fine-scale variation in extreme temperatures. Oikos 120, 1–8, https://doi.org/10.1111/j.1600-0706.2010.18270.x (2010).

  • 23.

    Dell, D., Sparks, T. & Dennis, R. Climate change and the effect of increasing spring temperatures on emergence dates of the butterfly Apatura iris (Lepidoptera: Nymphalidae). Eur. J. Entomol. 102, 161–167. https://doi.org/10.14411/eje.2005.026 (2005).

    Article  Google Scholar 

  • 24.

    Zipf, L., Williams, E. H., Primack, R. B. & Stichter, S. Climate effects on late-season flight times of Massachusetts butterflies. Int. J. Biometeorol. 61, 1667–1673. https://doi.org/10.1007/s00484-017-1347-8 (2017).

    ADS  CAS  Article  PubMed  Google Scholar 

  • 25.

    Diamond, S. E., Frame, A. M., Martin, R. A. & Buckley, L. B. Species’ traits predict phenological responses to climate change in butterflies. Ecology 92, 1005–1012. https://doi.org/10.1890/i0012-9658-92-5-1005 (2011).

    Article  PubMed  Google Scholar 

  • 26.

    Melero, Y., Stefanescu, C. & Pino, J. General declines in Mediterranean butterflies over the last two decades are modulated by species traits. Biol. Cons. 201, 336–342. https://doi.org/10.1016/j.biocon.2016.07.029 (2016).

    Article  Google Scholar 

  • 27.

    Stefanescu, C., Peñuelas, J. & Filella, I. Butterflies highlight the conservation value of hay meadows highly threatened by land-use changes in a protected Mediterranean area. Biol. Cons. 126, 234–246. https://doi.org/10.1016/j.biocon.2005.05.010 (2005).

    Article  Google Scholar 

  • 28.

    Sparks, T. H., Huber, K. & Dennis, R. L. H. Complex phenological responses to climate warming trends? Lessons from history. Eur. J. Entomol. 103, 379–386 (2006).

    Article  Google Scholar 

  • 29.

    Wong, M. K. L., Guénard, B. & Lewis, O. T. Trait-based ecology of terrestrial arthropods. Biol. Rev. 94, 999–1022. https://doi.org/10.1111/brv.12488 (2019).

    Article  PubMed  Google Scholar 

  • 30.

    Gutiérrez, D. & Wilson, R. J. Intra- and interspecific variation in the responses of insect phenology to climate. J. Anim. Ecol. https://doi.org/10.1111/1365-2656.13348 (2020).

    Article  PubMed  Google Scholar 

  • 31.

    Zografou, K. et al. Butterfly phenology in Mediterranean mountains using space-for-time substitution. Ecol. Evolut. 10, 928–939. https://doi.org/10.1002/ece3.5951 (2020).

    Article  Google Scholar 

  • 32.

    Steltzer, H. & Post, E. Seasons and life cycles. Science 324, 886–887. https://doi.org/10.1126/science.1171542 (2009).

    Article  PubMed  Google Scholar 

  • 33.

    Hale, R., Morrongiello, J. R. & Swearer, S. E. Evolutionary traps and range shifts in a rapidly changing world. Biol. Let. 12, 20160003. https://doi.org/10.1098/rsbl.2016.0003 (2016).

    Article  Google Scholar 

  • 34.

    Ghalambor, C. K., McKay, J. K., Carroll, S. P. & Reznick, D. N. Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Funct. Ecol. 21, 394–407. https://doi.org/10.1111/j.1365-2435.2007.01283.x (2007).

    Article  Google Scholar 

  • 35.

    Macgregor, C. J. et al. Climate-induced phenology shifts linked to range expansions in species with multiple reproductive cycles per year. Nat. Commun. 10, 4455. https://doi.org/10.1038/s41467-019-12479-w (2019).

    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

  • 36.

    Pau, S. et al. Predicting phenology by integrating ecology, evolution and climate science. Glob. Change Biol. 17, 3633–3643. https://doi.org/10.1111/j.1365-2486.2011.02515.x (2011).

    ADS  Article  Google Scholar 

  • 37.

    Sherry, R. A. et al. Divergence of reproductive phenology under climate warming. Proc. Natl. Acad. Sci. 104, 198. https://doi.org/10.1073/pnas.0605642104 (2007).

    ADS  CAS  Article  PubMed  Google Scholar 

  • 38.

    Wilson, R. J. & Fox, R. Insect responses to global change offer signposts for biodiversity and conservation. Ecol. Entomol. https://doi.org/10.1111/een.12970 (2020).

    Article  Google Scholar 

  • 39.

    Brooks, S. J. et al. The influence of life history traits on the phenological response of British butterflies to climate variability since the late-19th century. Ecography 40, 1152–1165. https://doi.org/10.1111/ecog.02658 (2017).

    Article  Google Scholar 

  • 40.

    Cayton, H. L., Haddad, N. M., Gross, K., Diamond, S. E. & Ries, L. Do growing degree days predict phenology across butterfly species?. Ecology 96, 1473–1479. https://doi.org/10.1890/15-0131.1 (2015).

    Article  Google Scholar 

  • 41.

    Stocker, T. F. et al. Summary for policymakers. In Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change, 3–29 (2013).

  • 42.

    Swengel, A. B. Effects of fire and hay management on abundance of prairie butterflies. Biol. Cons. 76, 73–85 (1996).

    Article  Google Scholar 

  • 43.

    Zografou, K. et al. Severe decline and partial recovery of a rare butterfly on an active military training area. Biol. Cons. 216, 43–50. https://doi.org/10.1016/j.biocon.2017.09.026 (2017).

    Article  Google Scholar 

  • 44.

    Gillingham, P. K., Huntley, B., Kunin, W. E. & Thomas, C. D. The effect of spatial resolution on projected responses to climate warming. Divers. Distrib. 18, 990–1000. https://doi.org/10.1111/j.1472-4642.2012.00933.x (2012).

    Article  Google Scholar 

  • 45.

    Roy David, B. et al. Similarities in butterfly emergence dates among populations suggest local adaptation to climate. Global Change Biol. 21, 3313–3322, https://doi.org/10.1111/gcb.12920 (2015).

  • 46.

    Lemoine, N. P. Climate change may alter breeding ground distributions of eastern migratory monarchs (Danaus plexippus) via range expansion of asclepias host plants. PLoS ONE 10, e0118614. https://doi.org/10.1371/journal.pone.0118614 (2015).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • 47.

    Slansky, F. Phagism relationships among butterflies. J. N. Y. Entomol. Soc. 84, 91–105 (1976).

    Google Scholar 

  • 48.

    Morin, X., Roy, J., Sonié, L. & Chuine, I. Changes in leaf phenology of three European oak species in response to experimental climate change. New Phytol. 186, 900–910. https://doi.org/10.1111/j.1469-8137.2010.03252.x (2010).

    Article  PubMed  Google Scholar 

  • 49.

    Chuine, I., Morin, X. & Bugmann, H. Warming. Photoperiods Tree Phenol. 329, 277–278. https://doi.org/10.1126/science.329.5989.277-e%JScience (2010).

    Article  Google Scholar 

  • 50.

    Luedeling, E., Girvetz, E. H., Semenov, M. A. & Brown, P. H. Climate change affects winter chill for temperate fruit and nut trees. PLoS ONE 6, e20155. https://doi.org/10.1371/journal.pone.0020155 (2011).

    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

  • 51.

    Fu, Y. S. H. et al. Variation in leaf flushing date influences autumnal senescence and next year’s flushing date in two temperate tree species. Proc. Natl. Acad. USA 111, 7355–7360. https://doi.org/10.1073/pnas.1321727111%JProceedingsoftheNationalAcademyofSciences (2014).

    ADS  CAS  Article  Google Scholar 

  • 52.

    Renner, S. S. & Zohner, C. M. Climate change and phenological mismatch in trophic interactions among plants, insects, and vertebrates. Annu. Rev. Ecol. Evol. Syst. 49, 165–182. https://doi.org/10.1146/annurev-ecolsys-110617-062535 (2018).

    Article  Google Scholar 

  • 53.

    Barton, K. E., Edwards, K. F. & Koricheva, J. Shifts in woody plant defence syndromes during leaf development. Funct. Ecol. 33, 2095–2104. https://doi.org/10.1111/1365-2435.13435 (2019).

    Article  Google Scholar 

  • 54.

    Cohen, J. M., Lajeunesse, M. J. & Rohr, J. R. A global synthesis of animal phenological responses to climate change. Nat. Clim. Change 8, 224–228. https://doi.org/10.1038/s41558-018-0067-3 (2018).

    ADS  Article  Google Scholar 

  • 55.

    Altermatt, F. Climatic warming increases voltinism in European butterflies and moths. Proc. R. Soc. B Biol. Sci. 277, 1281–1287. https://doi.org/10.1098/rspb.2009.1910 (2010).

    Article  Google Scholar 

  • 56.

    Illán, J. G., Gutiérrez, D., Díez, S. B. & Wilson, R. J. Elevational trends in butterfly phenology: Implications for species responses to climate change. Ecol. Entomol. 37, 134–144. https://doi.org/10.1111/j.1365-2311.2012.01345.x (2012).

    Article  Google Scholar 

  • 57.

    Nufio, C. R., McGuire, C. R., Bowers, M. D. & Guralnick, R. P. Grasshopper community response to climatic change: Variation along an elevational gradient. PLoS ONE 5, e12977. https://doi.org/10.1371/journal.pone.0012977 (2010).

    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

  • 58.

    Van Dyck, H., Bonte, D., Puls, R., Gotthard, K. & Maes, D. The lost generation hypothesis: Could climate change drive ectotherms into a developmental trap?. Oikos 124, 54–61. https://doi.org/10.1111/oik.02066 (2015).

    Article  Google Scholar 

  • 59.

    Scott, J. A. The Butterflies of North America: A Natural History and Field Guide. (Stanford University Press, 1992).

  • 60.

    Division, E. Final Integrated Natural Resources Management Plan 17003–25002 (The Pennsylvania Department of Military and Veterans Affairs, Annville, 2002).

    Google Scholar 

  • 61.

    Shuey, J. et al. Landscape-scale response to local habitat restoration in the regal fritillary butterfly (Speyeria idalia) (Lepidoptera: Nymphalidae). J. Insect Cons. 20, 773–780. https://doi.org/10.1007/s10841-016-9908-4 (2016).

    Article  Google Scholar 

  • 62.

    Metzler, E., Shuey, J., Ferge, L., Henderson, R. & Goldstein, P. Contributions to the understanding of tallgrass prairie-dependent butterflies and moths (Lepidoptera) and their biogeography in the United States. Ohio Biol. Surv. Bull. New Ser. 15, 1–143 (2005).

    Google Scholar 

  • 63.

    PNHP. PNHP Species Lists. Pennsylvania Natural Heritage Program. http://www.naturalheritage.state.pa.us/Species.aspx (2019).

  • 64.

    Pollard, E. & Yates, T. J. Monitoring Butterflies for Ecology and Conservation (1993).

  • 65.

    Nufio, C. R., McGuire, C. R., Bowers, M. D. & Guralnick, R. P. Grasshopper community response to climatic change: Variation along an elevational gradient. PLoS ONE https://doi.org/10.1371/journal.pone.0012977 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  • 66.

    Glassberg, J. Butterflies through binoculars, the East. A field guide to the butterflies of Eastern North America, 242. (Oxford University Press, Inc., 1999).

  • 67.

    Brock, J. P. & Kaufman, K. Field Guide to Butterflies of North America., 391 (Hillstar Editions L.C, 2003).

  • 68.

    Brakefield, P. M. Geographical variability in, and temperature effects on, the phenology of Maniola jurtina and Pyronia tithonus (Lepidoptera, Satyrinae) in England and Wales. Ecol. Entomol. 12, 139–148. https://doi.org/10.1111/j.1365-2311.1987.tb00993.x (1987).

    Article  Google Scholar 

  • 69.

    de Arce Crespo, J. I. & Gutiérrez, D. Altitudinal trends in the phenology of butterflies in a mountainous area in central Spain. Eur. J. Entomol. 108, 651–658 (2011).

  • 70.

    Moussus, J.-P., Julliard, R. & Jiguet, F. Featuring 10 phenological estimators using simulated data. Methods Ecol. Evol. 1, 140–150. https://doi.org/10.1111/j.2041-210X.2010.00020.x (2010).

    Article  Google Scholar 

  • 71.

    Penny, D. The comparative method in evolutionary biology. J. Classif. 9, 169–172. https://doi.org/10.1007/BF02618482 (1992).

    MathSciNet  Article  Google Scholar 

  • 72.

    Earl, C., Belitz, M. et al. Spatial phylogenetics of butterflies in relation to environmental drivers and angiosperm diversity across North America. BioRxiv:2020.2007.2022.216119, https://doi.org/10.1101/2020.07.22.216119 (2020).

  • 73.

    PRISM. Climate Group, Parameter-elevation Regressions on Independent Slopes Model. Oregon State University, http://prism.oregonstate.edu. Accessed 24 July 2018.

  • 74.

    Daly, C. et al. Physiographically sensitive mapping of climatological temperature and precipitation across the conterminous United States. Int. J. Climatol. 28, 2031–2064. https://doi.org/10.1002/joc.1688 (2008).

    Article  Google Scholar 

  • 75.

    Peñuelas, J. et al. Response of plant species richness and primary productivity in shrublands along a north-south gradient in Europe to seven years of experimental warming and drought: Reductions in primary productivity in the heat and drought year of 2003. Glob. Change Biol. 13, 2563–2581. https://doi.org/10.1111/j.1365-2486.2007.01464.x (2007).

    ADS  Article  Google Scholar 

  • 76.

    McMaster, G. S. & Wilhelm, W. W. Growing degree-days: One equation, two interpretations. Agric. For. Meteorol. 87, 291–300. https://doi.org/10.1016/S0168-1923(97)00027-0 (1997).

    ADS  Article  Google Scholar 

  • 77.

    Walters, E. J., Morrell, C. H. & Auer, R. E. An investigation of the median-median method of linear regression. J. Stat. Educ. https://doi.org/10.1080/10691898.2006.11910582 (2006).

    Article  Google Scholar 

  • 78.

    Theil, H. in Henri Theil’s Contributions to Economics and Econometrics: Econometric Theory and Methodology (eds Baldev Raj & Johan Koerts) 345–381 (Springer Netherlands, 1992).

  • 79.

    Sen, P. K. Estimates of the regression coefficient based on Kendall’s Tau. J. Am. Stat. Assoc. 63, 1379–1389. https://doi.org/10.2307/2285891 (1968).

    MathSciNet  Article  MATH  Google Scholar 

  • 80.

    Siegel, A. F. Robust regression using repeated medians. Biometrika 69, 242–244. https://doi.org/10.2307/2335877 (1982).

    Article  MATH  Google Scholar 

  • 81.

    Schneider, G., Chicken, E. & Becvarik, R. NSM3: Functions and Datasets to Accompany Hollander, Wolfe, and Chicken – Nonparametric Statistical Methods, Third Edition. R Package Version 1.15. https://CRAN.R-project.org/package=NSM3. (2020).

  • 82.

    Patrick Bogaart, Loo, M. v. d. & Pannekoek, J. rtrim: Trends and Indices for Monitoring Data. R Package Version 2.1.1. https://CRAN.R-project.org/package=rtrim. (2020).

  • 83.

    Zografou, K. et al. Stable generalist species anchor a dynamic pollination network. Ecosphere 11, e03225. https://doi.org/10.1002/ecs2.3225 (2020).

    Article  Google Scholar 

  • 84.

    Pinheiro J, Bates D, DebRoy S & D, S. nlme: Linear and Nonlinear Mixed Effects Models. R Package v. 3.1‐117. (www document). https://CRAN.R-project.org/package=nlme. (2015).

  • 85.

    Felsenstein, J. Phylogenies and quantitative characters. Annu. Rev. Ecol. Syst. 19, 445–471. https://doi.org/10.1146/annurev.es.19.110188.002305 (1988).

    Article  Google Scholar 


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