Acknowledgements
We thank the many iNaturalist users who are recording and identifying
insect biodiversity. We also thank those who have collected, curated,
and digitized insect specimen records. MWB was partially supported by a
University of Florida Biodiversity Institute (UFBI) fellowship. CJ
Campbell provided valuable feedback. No direct funding supported this
study, but MWB, EAL, and RPG developed phenological tools and concepts
used in this study that were supported by the National Science
Foundation DEB # 1703048 and DEB # 1702664.
References
Altermatt, F. (2010a). Climatic warming increases voltinism in European
butterflies and moths.Proc Biol Sci277, 1281–1287. doi:10.1098/rspb.2009.1910.
Altermatt, F. (2010b).
Tell me what you eat and I’ll tell you when you fly: diet can predict
phenological changes in response to climate change. Ecology
Letters 13, 1475–1484.
doi:https://doi.org/10.1111/j.1461-0248.2010.01534.x.
Bartomeus, I., Ascher,
J. S., Wagner, D., Danforth, B. N., Colla, S., Kornbluth, S., et al.
(2011). Climate-associated phenological advances in bee pollinators and
bee-pollinated plants. PNAS 108, 20645–20649.
doi:10.1073/pnas.1115559108.
Belitz, M. W. (2021). InsectDuration: Code for Manuscript Submission
(Version v1.0). Zenodo . http://doi.org/10.5281/zenodo.4574261
Belitz, M. W., Larsen, E. A., Ries, L., and Guralnick, R. P. (2020). The
accuracy of phenology estimators for use with sparsely sampled
presence‐only observations. Methods in Ecology and
Evolution , 11 (10), 1273-1285.
doi:10.1111/2041-210X.13448
Center for International Earth Science Information
Network-CIESIN-Columbia University (2017). Gridded population of the
world, Version 4 (GPWv4): Population Density, Revision 11.
doi:10.7927/H49C6VHW.
Chick, L. D.,
Strickler, S. A., Perez, A., Martin, R. A., and Diamond, S. E. (2019).
Urban heat islands advance the timing of reproduction in a social
insect. Journal of Thermal Biology 80, 119–125.
doi:10.1016/j.jtherbio.2019.01.004.
Cleland, E. E.,
Chuine, I., Menzel, A., Mooney, H. A., and Schwartz, M. D. (2007).
Shifting plant phenology in response to global change. Trends in
Ecology & Evolution 22, 357–365. doi:10.1016/j.tree.2007.04.003.
Cohen, J. M.,
Lajeunesse, M. J., and Rohr, J. R. (2018). A global synthesis of animal
phenological responses to climate change. Nature Climate Change8, 224–228. doi:10.1038/s41558-018-0067-3.
Crossley, M. S.,
Meier, A. R., Baldwin, E. M., Berry, L. L., Crenshaw, L. C., Hartman, G.
L., et al. (2020). No net insect abundance and diversity declines across
US Long Term Ecological Research sites. Nature Ecology &
Evolution 4, 1368–1376. doi:10.1038/s41559-020-1269-4.
Damgaard, C. (2019). A
Critique of the Space-for-Time Substitution Practice in Community
Ecology. Trends in Ecology & Evolution 34, 416–421.
doi:10.1016/j.tree.2019.01.013.
Danks, H. V. (2007). The elements of seasonal adaptations in
insects. The Canadian Entomologist , 139 (1), 1-44.
doi.org/10.4039/n06-048
Denlinger, D. L.
(2002). Regulation of diapause. Annual review of entomology 47,
93–122.
Diamond, S. E., Dunn,
R. R., Frank, S. D., Haddad, N. M., and Martin, R. A. (2015). Shared and
unique responses of insects to the interaction of urbanization and
background climate. Current Opinion in Insect Science 11, 71–77.
doi:10.1016/j.cois.2015.10.001.
Diamond, S. E., Frame,
A. M., Martin, R. A., and Buckley, L. B. (2011). Species’ traits predict
phenological responses to climate change in butterflies. Ecology92, 1005–1012. doi:https://doi.org/10.1890/10-1594.1.
Diamond, S. E.,
Cayton, H., Wepprich, T., Jenkins, C. N., Dunn, R. R., Haddad, N. M., et
al. (2014). Unexpected phenological responses of butterflies to the
interaction of urbanization and geographic temperature. Ecology95, 2613–2621. doi:10.1890/13-1848.1.
Edwards, M., and
Richardson, A. J. (2004). Impact of climate change on marine pelagic
phenology and trophic mismatch. Nature 430, 881–884.
doi:10.1038/nature02808.
Fisogni, A.,
Hautekèete, N., Piquot, Y., Brun, M., Vanappelghem, C., Michez, D., et
al. (2020). Urbanization drives an early spring for plants but not for
pollinators. Oikos 129, 1681–1691.
doi:https://doi.org/10.1111/oik.07274.
Forrest, J. R. (2016).
Complex responses of insect phenology to climate change. Current
Opinion in Insect Science 17, 49–54. doi:10.1016/j.cois.2016.07.002.
GBIF. (2020a). GBIF Occurrence download.
https://doi.org/10.15468/dl.6y59tz
GBIF. (2020b). GBIF Occurrence download.
https://doi.org/10.15468/dl.vkunmd
GBIF. (2020c). GBIF Occurrence download.
https://doi.org/10.15468/dl.yz7uuv
GBIF. (2020d). GBIF Occurrence download.
https://doi.org/10.15468/dl.n5f8hv
GBIF. (2020e). GBIF Occurrence download.
https://doi.org/10.15468/dl.jp9fd3
Gilbert, N., and
Raworth, D. A. (1996). Forum: Insects and temperature – A general
theory. The Canadian Entomologist 128, 1–13.
doi:10.4039/Ent1281-1.
Hallmann, C. A.,
Zeegers, T., Klink, R. van, Vermeulen, R., Wielink, P. van, Spijkers,
H., et al. (2020). Declining abundance of beetles, moths and caddisflies
in the Netherlands. Insect Conservation and Diversity 13,
127–139. doi:https://doi.org/10.1111/icad.12377.
Heinrich, B. (1972).
Physiology of Brood Incubation in the Bumblebee Queen, Bombus
vosnesenskii. Nature 239, 223–225. doi:10.1038/239223a0.
Hodgson, J. A.,
Thomas, C. D., Oliver, T. H., Anderson, B. J., Brereton, T. M., and
Crone, E. E. (2011). Predicting insect phenology across space and time.Global Change Biology 17, 1289–1300.
doi:10.1111/j.1365-2486.2010.02308.x.
Ives, A. R., and Li,
D. (2018). ‘rr2‘: An R package to calculate R2s for regression models.Journal of Open Source Software 3, 1028.
doi:10.21105/joss.01028.
Jochner, S., and
Menzel, A. (2015). Urban phenological studies – Past, present, future.Environmental Pollution 203, 250–261.
doi:10.1016/j.envpol.2015.01.003.
Jones, J. C., and
Oldroyd, B. P. (2006). “Nest Thermoregulation in Social Insects,” inAdvances in Insect Physiology, ed. S. J. Simpson (Academic
Press), 153–191. doi:10.1016/S0065-2806(06)33003-2.
Kerr, N. Z., Wepprich,
T., Grevstad, F. S., Dopman, E. B., Chew, F. S., and Crone, E. E.
(2020). Developmental trap or demographic bonanza? Opposing consequences
of earlier phenology in a changing climate for a multivoltine butterfly.Global Change Biology 26, 2014–2027. doi:10.1111/gcb.14959.
Kumar, S., Stecher,
G., Suleski, M., and Hedges, S. B. (2017). TimeTree: A Resource for
Timelines, Timetrees, and Divergence Times. Mol Biol Evol 34,
1812–1819. doi:10.1093/molbev/msx116.
Kuznetsova, A.,
Brockhoff, P. B., and Christensen, R. H. B. (2017). lmerTest Package:
Tests in Linear Mixed Effects Models. Journal of Statistical
Software 82, 1–26. doi:10.18637/jss.v082.i13.
Larsen, E., and
Shirey, V. (2021). Method matters: pitfalls in analyzing phenology from
occurrence records. Authorea.
doi:10.22541/au.161001475.56669645/v1.
Li, D., Barve, N.,
Brenskelle, L., Earl, K., Barve, V., Belitz, M. W., et al. (2021).
Climate, urbanization, and species traits interactively drive flowering
duration. Global Change Biology 27, 892–903.
doi:https://doi.org/10.1111/gcb.15461.
Li, D., Dinnage, R.,
Nell, L. A., Helmus, M. R., and Ives, A. R. (2020). phyr: an R package
for phylogenetic species-distribution modelling in ecological
communities. Methods in Ecology and Evolution 11, 1455–1463.
Li, D., and Ives, A.
R. (2017). The statistical need to include phylogeny in trait-based
analyses of community composition. Methods in Ecology and
Evolution 8, 1192–1199. doi:https://doi.org/10.1111/2041-210X.12767.
Li, D., Stucky, B. J.,
Deck, J., Baiser, B., and Guralnick, R. P. (2019). The effect of
urbanization on plant phenology depends on regional temperature.Nature Ecology & Evolution 3, 1661–1667.
doi:10.1038/s41559-019-1004-1.
Losey, J. E., and
Vaughan, M. (2006). The Economic Value of Ecological Services Provided
by Insects. BioScience 56, 311–323.
doi:10.1641/0006-3568(2006)56[311:TEVOES]2.0.CO;2.
Macgregor, C. J.,
Thomas, C. D., Roy, D. B., Beaumont, M. A., Bell, J. R., Brereton, T.,
et al. (2019). Climate-induced phenology shifts linked to range
expansions in species with multiple reproductive cycles per year.Nature Communications 10, 4455. doi:10.1038/s41467-019-12479-w.
Menzel, F., and
Feldmeyer, B. (2021). How does climate change affect social insects?Current Opinion in Insect Science.
doi:10.1016/j.cois.2021.01.005.
Michielini, J. P.,
Dopman, E. B., and Crone, E. E. (2021). Changes in flight period predict
trends in abundance of Massachusetts butterflies. Ecology Letters24, 249–257. doi:https://doi.org/10.1111/ele.13637.
Michonneau, F., Brown,
J. W., and Winter, D. J. (2016). rotl: an R package to interact with the
Open Tree of Life data. Methods in Ecology and Evolution 7,
1476–1481. doi:10.1111/2041-210X.12593.
Middleton-Welling, J.,
Dapporto, L., García-Barros, E., Wiemers, M., Nowicki, P., Plazio, E.,
et al. (2020). A new comprehensive trait database of European and
Maghreb butterflies, Papilionoidea. Scientific Data 7, 351.
doi:10.1038/s41597-020-00697-7.
Miller-Rushing, A. J.,
Høye, T. T., Inouye, D. W., and Post, E. (2010). The effects of
phenological mismatches on demography. Philos Trans R Soc Lond B
Biol Sci 365, 3177–3186. doi:10.1098/rstb.2010.0148.
Neil, K., and Wu, J.
(2006). Effects of urbanization on plant flowering phenology: A review.Urban Ecosyst 9, 243–257. doi:10.1007/s11252-006-9354-2.
Ooms, J., and
Chamberlain, S. (2019). phylocomr: Interface to “Phylocom.”Available at: https://CRAN.R-project.org/package=phylocomr.
Park, D. S.,
Breckheimer, I., Williams, A. C., Law, E., Ellison, A. M., and Davis, C.
C. (2019). Herbarium specimens reveal substantial and unexpected
variation in phenological sensitivity across the eastern United States.Phil. Trans. R. Soc. B 374, 20170394.
doi:10.1098/rstb.2017.0394.
Parmesan, C. (2007).
Influences of species, latitudes and methodologies on estimates of
phenological response to global warming. Global Change Biology13, 1860–1872. doi:10.1111/j.1365-2486.2007.01404.x.
Pöyry, J., Leinonen,
R., Söderman, G., Nieminen, M., Heikkinen, R. K., and Carter, T. R.
(2011). Climate-induced increase of moth multivoltinism in boreal
regions. Global Ecology and Biogeography 20, 289–298.
doi:https://doi.org/10.1111/j.1466-8238.2010.00597.x.
R Core Team. (2020). R: A language and environment for statistical
computing. Version 4.0.0 “Arbor Day”. Vienna, Austria: R Foundation
for Statistical Computing.
Renner, S. S., and
Zohner, C. M. (2018). Climate Change and Phenological Mismatch in
Trophic Interactions Among Plants, Insects, and Vertebrates.Annual Review of Ecology, Evolution, and Systematics 49,
165–182. doi:10.1146/annurev-ecolsys-110617-062535.
Robinson, R. A.,
Crick, H. Q., Learmonth, J. A., Maclean, I. M., Thomas, C. D., Bairlein,
F., et al. (2009). Travelling through a warming world: climate change
and migratory species. Endangered species research 7, 87–99.
Roy, D. B., Oliver, T.
H., Botham, M. S., Beckmann, B., Brereton, T., Dennis, R. L. H., et al.
(2015). Similarities in butterfly emergence dates among populations
suggest local adaptation to climate. Global Change Biology 21,
3313–3322. doi:10.1111/gcb.12920.
Rue, H., Martino, S.,
and Chopin, N. (2009). Approximate Bayesian inference for latent
Gaussian models by using integrated nested Laplace approximations.Journal of the Royal Statistical Society: Series B (Statistical
Methodology) 71, 319–392. doi:10.1111/j.1467-9868.2008.00700.x.
Scott, J. A., and
Epstein, M. E. (1987). Factors affecting phenology in a temperate insect
community. American Midland Naturalist, 103–118.
Seress, G., Hammer,
T., Bókony, V., Vincze, E., Preiszner, B., Pipoly, I., et al. (2018).
Impact of urbanization on abundance and phenology of caterpillars and
consequences for breeding in an insectivorous bird. Ecological
Applications 28, 1143–1156. doi:10.1002/eap.1730.
Shirey, V., Belitz, M.
W., Barve, V., and Guralnick, R. (2021). A complete inventory of North
American butterfly occurrence data: narrowing data gaps, but increasing
bias. Ecography n/a. doi:https://doi.org/10.1111/ecog.05396.
Steltzer, H., and
Post, E. (2009). Seasons and Life Cycles. Science 324, 886–887.
doi:10.1126/science.1171542.
Stemkovski, M.,
Pearse, W. D., Griffin, S. R., Pardee, G. L., Gibbs, J., Griswold, T.,
et al. (2020). Bee phenology is predicted by climatic variation and
functional traits. Ecology Letters 23, 1589–1598.
doi:https://doi.org/10.1111/ele.13583.
Tauber, M. J., and
Tauber, C. A. (1976). Insect seasonality: diapause maintenance,
termination, and postdiapause development. Annual review of
entomology 21, 81–107.
Thompson, R., and
Clark, R. M. (2006). Spatio-temporal modelling and assessment of
within-species phenological variability using thermal time methods.Int J Biometeorol 50, 312–322. doi:10.1007/s00484-005-0017-4.
Thornton, M.M., Thornton, P.E., Wei, Y., Mayer, B.W., Cook, R.B., and
Vose, R.S. (2016a). Daymet: Annual Climate Summaries on a 1-km Grid for
North America, Version 3. ORNL DAAC, Oak Ridge, Tennessee, USA.
https://doi.org/10.3334/ORNLDAAC/1343
Thornton, M.M., Thornton, P.E., Wei, Y., Mayer, B.W., Cook, R.B., and
Vose, R.S. (2016b). Daymet: Monthly Climate Summaries on a 1-km Grid for
North America, Version 3. ORNL DAAC, Oak Ridge, Tennessee, USA.
https://doi.org/10.3334/ORNLDAAC/1345
van Klink, R., Bowler,
D. E., Gongalsky, K. B., Swengel, A. B., Gentile, A., and Chase, J. M.
(2020). Meta-analysis reveals declines in terrestrial but increases in
freshwater insect abundances. Science 368, 417–420.
doi:10.1126/science.aax9931.
Villalobos-Jiménez,
G., and Hassall, C. (2017). Effects of the urban heat island on the
phenology of Odonata in London, UK. Int J Biometeorol 61,
1337–1346. doi:10.1007/s00484-017-1311-7.
Wagner, D. L. (2020).
Insect Declines in the Anthropocene. Annual Review of Entomology65, 457–480. doi:10.1146/annurev-ento-011019-025151.
Wagner, D. L., Grames,
E. M., Forister, M. L., Berenbaum, M. R., and Stopak, D. (2021). Insect
decline in the Anthropocene: Death by a thousand cuts. PNAS 118.
doi:10.1073/pnas.2023989118.
Warren, M. S., Maes,
D., Swaay, C. A. M. van, Goffart, P., Dyck, H. V., Bourn, N. A. D., et
al. (2021). The decline of butterflies in Europe: Problems,
significance, and possible solutions. PNAS 118.
doi:10.1073/pnas.2002551117.
Welti, E., Joern, A.,
Lightfoot, D. C., Record, S., Rodenhouse, N., Stanley, E. H., et al.
(2020). Meta-analyses of insect temporal trends must account for the
complex sampling histories inherent to many long-term monitoring
efforts.
While, G. M., and
Uller, T. (2014). Quo vadis amphibia? Global warming and breeding
phenology in frogs, toads and salamanders. Ecography 37,
921–929. doi:https://doi.org/10.1111/ecog.00521.
Zeuss, D., Brunzel,
S., and Brandl, R. (2017). Environmental drivers of voltinism and body
size in insect assemblages across Europe. Global Ecology and
Biogeography 26, 154–165. doi:https://doi.org/10.1111/geb.12525.
Zografou, K., Swartz,
M. T., Adamidis, G. C., Tilden, V. P., McKinney, E. N., and Sewall, B.
J. (2021). Species traits affect phenological responses to climate
change in a butterfly community. Scientific Reports 11, 3283.
doi:10.1038/s41598-021-82723-1.