Abstract
Declines in the abundance and diversity of insects pose a substantial threat to terrestrial ecosystems worldwide. Yet, identifying the causes of these declines has proved difficult, even for well-studied species like monarch butterflies, whose eastern North American population has decreased markedly over the last three decades. Three hypotheses have been proposed to explain the changes observed in the eastern monarch population: loss of milkweed host plants from increased herbicide use, mortality during autumn migration and/or early-winter resettlement and changes in breeding-season climate. Here, we use a hierarchical modelling approach, combining data from >18,000 systematic surveys to evaluate support for each of these hypotheses over a 25-yr period. Between 2004 and 2018, breeding-season weather was nearly seven times more important than other factors in explaining variation in summer population size, which was positively associated with the size of the subsequent overwintering population. Although data limitations prevent definitive evaluation of the factors governing population size between 1994 and 2003 (the period of the steepest monarch decline coinciding with a widespread increase in herbicide use), breeding-season weather was similarly identified as an important driver of monarch population size. If observed changes in spring and summer climate continue, portions of the current breeding range may become inhospitable for monarchs. Our results highlight the increasingly important contribution of a changing climate to insect declines.
This is a preview of subscription content, access via your institution
Access options
Access Nature and 54 other Nature Portfolio journals
Get Nature+, our best-value online-access subscription
$29.99 / 30 days
cancel any time
Subscribe to this journal
Receive 12 digital issues and online access to articles
$119.00 per year
only $9.92 per issue
Buy this article
- Purchase on SpringerLink
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
Data availability
Monarch data from the overwintering grounds and covariate data are available on Zenodo (https://doi.org/10.5281/zenodo.4085906). Monarch data from the summer breeding grounds are proprietary and were obtained from the North American Butterfly Association (https://www.naba.org/), the Iowa Butterfly Survey Network (https://www.reimangardens.com/collections/insects/iowa-butterfly-survey-network/), the Illinois Butterfly Monitoring Network (https://bfly.org/), the Michigan Butterfly Network (https://michiganbutterfly.org/) and the Ohio Lepidopterists (http://www.ohiolepidopterists.org/). These data may be available upon reasonable request to L.R. and with permission from the aforementioned programmes.
Code availability
Code needed to run analyses (R scripts and Stan model files) is available on Zenodo (https://doi.org/10.5281/zenodo.4085906) and Github (https://zipkinlab.github.io/#dataintegration2021Z).
References
van Klink, R. et al. Meta-analysis reveals declines in terrestrial but increases in freshwater insect abundances. Science 368, 417–420 (2020).
Seibold, S. et al. Arthropod decline in grasslands and forests is associated with landscape-level drivers. Nature 574, 671–674 (2019).
Wepprich, T., Adrion, J. R., Ries, L., Wiedmann, J. & Haddad, N. M. Butterfly abundance declines over 20 years of systematic monitoring in Ohio, USA. PLoS ONE 14, e0216270 (2019).
Wagner, D. L., Grames, E. M., Forister, M. L., Berenbaum, M. R. & Stopak, D. Insect decline in the Anthropocene: death by a thousand cuts. Proc. Natl Acad. Sci. USA 118, e2023989118 (2021).
Dirzo, R. et al. Defaunation in the Anthropocene. Science 345, 401–406 (2014).
Winfree, R., Fox, J. W., Williams, N. M., Reilly, J. R. & Cariveau, D. P. Abundance of common species, not species richness, drives delivery of a real-world ecosystem service. Ecol. Lett. 18, 626–635 (2015).
Cardoso, P. et al. Scientists’ warning to humanity on insect extinctions. Biol. Conserv. 242, 108426 (2020).
Brower, L. P. et al. Decline of monarch butterflies overwintering in Mexico: is the migratory phenomenon at risk? Insect Conserv. Divers. 5, 95–100 (2012).
Agrawal, A. A. & Inamine, H. Mechanisms behind the monarch’s decline. Science 360, 1294–1296 (2018).
Schultz, C. B., Brown, L. M., Pelton, E. & Crone, E. E. Citizen science monitoring demonstrates dramatic declines of monarch butterflies in western North America. Biol. Conserv. 214, 343–346 (2017).
Thogmartin, W. E. et al. Monarch butterfly population decline in North America: identifying the threatening processes. R. Soc. Open Sci. 4, 170760 (2017).
Boyle, J. H., Dalgleish, H. J. & Puzey, J. R. Monarch butterfly and milkweed declines substantially predate the use of genetically modified crops. Proc. Natl Acad. Sci. USA 116, 3006–3011 (2019).
Hann, N. L. & Landis, D. A. The importance of shifting disturbance regimes in monarch butterfly decline and recovery. Front. Ecol. Evol. 7, 191 (2019).
Oberhauser, K. S. et al. Temporal and spatial overlap between monarch larvae and corn pollen. Proc. Natl Acad. Sci. USA 98, 11913–11918 (2001).
Pleasants, J. M. & Oberhauser, K. S. Milkweed loss in agricultural fields because of herbicide use: effect on the monarch butterfly population. Insect Conserv. Divers. 6, 135–144 (2013).
Ries, L., Taron, D. J. & Rendón-Salinas, E. The disconnect between summer and winter monarch trends for the eastern migratory population: possible links to differing drivers. Ann. Entomol. Soc. Am. 108, 691–699 (2015).
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 125, 1081–1091 (2016).
Saunders, S. P. et al. Multiscale seasonal factors drive the size of winter monarch colonies. Proc. Natl Acad. Sci. USA 116, 8609–8614 (2019).
Zalucki, M. P. Temperature and rate of development in Danaus plexippus L. and D. chrysippus L. (Lepidoptera: Nymphalidae). Aust. J. Entomol. 21, 241–246 (1982).
Zipkin, E. F., Ries, L., Reeves, R., Regetz, J. & Oberhauser, K. S. Tracking climate impacts on the migratory monarch butterfly. Glob. Change Biol. 18, 3039–3049 (2012).
Saunders, S. P., Ries, L., Oberhauser, K. S., Thogmartin, W. E. & Zipkin, E. F. Local and cross-seasonal associations of climate and land use with abundance of monarch butterflies. Ecography 41, 278–290 (2018).
Batalden, R. V., Oberhauser, K. & Peterson, A. T. Ecological niches in sequential generations of eastern North American monarch butterflies: the ecology of migration and likely climate change implications. Environ. Entomol. 36, 1365–1373 (2007).
Lemoine, N. P. Climate change may alter breeding ground distributions of eastern migratory monarchs via range expansion of Asclepias host plants. PLoS ONE 10, e0118614 (2015).
Vidal, O. & Rendón-Salinas, E. Dynamics and trends of overwintering colonies of the monarch butterfly in Mexico. Biol. Conserv. 180, 165–175 (2014).
Thogmartin, W. E. et al. Density estimates of monarch butterflies overwintering in central Mexico. PeerJ 5, e3221 (2017).
Flockhart, D. T. T., Pichancourt, J.-B., Norris, D. R. & Martin, T. G. Unravelling the annual cycle in a migratory animal: breeding-season habitat loss drives population declines of monarch butterflies. J. Anim. Ecol. 84, 155–165 (2015).
Oberhauser, K. et al. A trans-national monarch butterfly population model and implications for regional conservation priorities. Ecol. Entomol. 42, 51–60 (2017).
Wilcox, A. A. E., Flockhart, D. T. T., Newman, A. E. M. & Norris, D. R. An evaluation of studies on the potential threats contributing to the decline of eastern migratory North American monarch butterflies (Danaus plexippus). Front. Ecol. Evol. 7, 99 (2019).
Chevan, A. & Sutherland, M. Hierarchical partitioning. Am. Stat. 45, 90–96 (1991).
Dai, S., Shulski, M. D., Hubbard, K. G. & Takle, E. S. A spatiotemporal analysis of Midwest US temperature and precipitation trends during the growing season from 1980 to 2013. Int. J. Climatol. 36, 517–525 (2016).
Feng, Z. et al. More frequent intense and long-lived storms dominate the springtime trend in central US rainfall. Nat. Commun. 7, 13429 (2016).
Crimmins, T. M. & Crimmins, M. A. Biologically-relevant trends in springtime temperatures across the United States. Geophys. Res. Lett. 46, 12377–12387 (2019).
Roy, D. B., Rothery, P., Moss, D., Pollard, E. & Thomas, J. A. Butterfly numbers and weather: predicting historical trends in abundance and the future effects of climate change. J. Anim. Ecol. 70, 201–217 (2001).
Nelson, W. A., Bjørnstad, O. N. & Yamanaka, T. Recurrent insect outbreaks caused by temperature-driven changes in system stability. Science 341, 796–799 (2013).
IPCC Climate Change 2014: Impacts, Adaptation, and Vulnerability (eds. Field, C. B. et al.) (Cambridge Univ. Press, 2014).
Diffenbaugh, N. S. & Giorgi, F. Climate change hotspots in the CMIP5 global climate model ensemble. Clim. Change 114, 813–822 (2012).
Cook, K. H., Vizy, E. K., Launer, Z. S. & Patricola, C. M. Springtime intensification of the Great Plains low-level jet and Midwest precipitation in GCM simulations of the twenty-first century. J. Clim. 21, 6321–6340 (2008).
Diffenbaugh, N. S. & Field, C. B. Changes in ecologically critical terrestrial climate conditions. Science 341, 486–492 (2013).
Wagner, D. L. Insect declines in the Anthropocene. Ann. Rev. Entomol. 65, 457–480 (2020).
Forister, M. L. et al. Fewer butterflies seen by community scientists across the warming and drying landscapes of the American West. Science 371, 1042–1045 (2021).
Janzen, D. H. & Hallwachs, W. To us insectometers, it is clear that insect decline in our Costa Rican tropics is real, so let’s be kind to the survivors. Proc. Natl Acad. Sci. USA 118, e2002546117 (2021).
Flockhart, D. T. T. 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. 23, 2565–2576 (2017).
Wassenaar, L. I. & Hobson, K. A. Natal origins of migratory monarch butterflies at wintering colonies in Mexico: new isotopic evidence. Proc. Natl Acad. Sci. USA 95, 15436–15439 (1998).
Oberhauser, K. S. et al. in Monarchs in a Changing World: Biology and Conservation of an Iconic Butterfly (eds. Oberhauser, K. S. et al.) 13–30 (Cornell Univ. Press, 2015).
Pollard, E. A method for assessing changes in the abundance of butterflies. Biol. Conserv. 12, 115–134 (1977).
Saunders, S. P., Ries, L., Obserhauser, K. S. & Zipkin, E. F. Evaluating confidence in climate-based predictions of population change in a migratory species. Glob. Ecol. Biogeogr. 25, 1000–1012 (2016).
Missrie, M. in The Monarch Butterfly: Biology and Conservation (eds. Obserhauser, K. S. & Solensky, M. J.) 141–150 (Cornell Univ. Press, 2004).
García-Serrano, E., Reyes, J. L. & Alvarez, B. X. M. in The Monarch Butterfly: Biology and Conservation (eds. Obserhauser, K. S. & Solensky, M. J.) 129–133 (Cornell Univ. Press, 2004).
Ramírez, M. I., Sáenz-Romero, C., Rehfeldt, G. & Salas-Canela, L. in Monarchs in a Changing World: Biology and Conservation of an Iconic Butterfly (eds. Oberhauser, K. S. et al.) 157–168 (Cornell Univ. Press, 2015).
Howard, E. & Davis, A. K. Investigating long-term changes in the spring migration of monarch butterflies (Lepidoptera: Nymphalidae) using 18 years of data from Journey North, a citizen science program. Ann. Entomol. Soc. Am. 108, 664–669 (2015).
McMaster, G. S. & Wilhelm, W. Growing degree-days: one equation, two interpretations. Agric. Meteorol. 87, 291–300 (1997).
Thornton, P. E. et al. Daymet: Daily Surface Weather Data on a 1-km Grid for North America Version 3 (ORNL DAAC, 2018); https://doi.org/10.3334/ORNLDAAC/1328
Hartzler, R. G. & Buhler, D. D. Occurrence of common milkweed (Asclepias syriaca) in cropland and adjacent areas. Crop Prot. 19, 363–366 (2000).
Hartzler, R. G. Reduction in common milkweed (Asclepias syriaca) occurrence in Iowa cropland from 1999 to 2009. Crop Prot. 29, 1542–1544 (2010).
Homer, C. G. et al. Completion of the 2011 National Land Cover Database for the conterminous United States—representing a decade of land cover change information. Photogramm. Eng. Remote Sens. 81, 345–354 (2015).
Douglas, M. R., Sponsler, D. B., Lonsdorf, E. V. & Grozinger, C. M. County-level analysis reveals a rapidly shifting landscape of insecticide hazard to honey bees (Apis mellifera) on US farmland. Sci. Rep. 10, 797 (2020).
Benbrook, C. M. Trends in glyphosate herbicide use in the United States and globally. Environ. Sci. Eur. 28, 3 (2016).
Pesticide National Synthesis Project (US Geological Survey, 2020); https://water.usgs.gov/nawqa/pnsp/usage/maps/county-level/
Quick Stats (US Department of Agriculture, National Agricultural Statistics Service, 2020); http://quickstats.nass.usda.gov
Crops (Ontario Ministry of Agriculture, Food and Rural Affairs, 2020); http://www.omafra.gov.on.ca/english/crops/
Batalden, R. V. & Oberhauser, K. S. in Monarchs in a Changing World: Biology and Conservation of an Iconic Butterfly (eds. Oberhauser, K. S. et al.) 215–224 (Cornell Univ. Press, 2015).
Alonso-Mejía, A., Rendón-Salinas, E., Montesinos-Patiño, E. & Brower, L. P. Use of lipid reserves by monarch butterflies overwintering in Mexico: implications for conservation. Ecol. Appl. 7, 934–947 (1997).
Brower, L. P., Fink, L. S. & Walford, P. Fueling the fall migration of the monarch butterfly. Integr. Comp. Biol. 46, 1123–1142 (2006).
Tracy, J. L., Kantola, T., Baum, K. A. & Coulson, R. N. Modeling fall migration pathways and spatially identifying potential migratory hazards for the eastern monarch butterfly. Landsc. Ecol. 34, 443–458 (2019).
Feldman, R. E. & McGill, B. J. How important is nectar in shaping spatial variation in the abundance of temperate breeding hummingbirds? J. Biogeogr. 41, 489–500 (2014).
Didan, K. MOD13Q1 MODIS/Terra Vegetation Indices 16-Day L3 Global 250 m SIN Grid V006 [Data set] (NASA EOSDIS Land Processes DAAC, 2015); https://doi.org/10.5067/MODIS/MOD13Q1.006
Vidal, O., López-García, J. & Rendón-Salinas, E. Trends in deforestation and forest degradation after a decade of monitoring in the Monarch Butterfly Biosphere Reserve in Mexico. Conserv. Biol. 28, 177–186 (2013).
Williams, E. H. & Brower, L. P. in Monarchs in a Changing World: Biology and Conservation of an Iconic Butterfly (eds. Oberhauser, K. S. et al.) 109–116 (Cornell Univ. Press, 2015).
Brower, L. P. et al. in The Monarch Butterfly: Biology and Conservation (eds. Obserhauser, K. S. & Solensky, M. J.) 151–166 (Cornell Univ. Press, 2004).
Brower, L. P. et al. Butterfly mortality and salvage logging from the March 2016 storm in the Monarch Butterfly Biosphere Reserve in Mexico. Am. Entom. 63, 151–164 (2017).
Farfán-Gutiérrez, M. et al. Modeling anthropic factors as drivers of wildfire occurrence at the Monarch Butterfly Biosphere. Madera y Bosques 24, e2431591 (2018).
Ramírez, M. I., López-Sánchez, J. G. & Barrasa, S. Mapa de Vegetación y Cubiertas del Suelo, Reserva de la Biosfera Mariposa Monarca Vol. II (CIGA-UNAM, 2019).
Flores-Martínez, J. J. et al. Recent forest cover loss in the core zones of the Monarch Butterfly Biosphere Reserve in Mexico. Front. Ecol. Evol. 7, 167 (2019).
Ramírez, M. I., Gímenez-Azcárate, J. & Luna, L. Effects of human activities on monarch butterfly habitat in protected mountain forests, Mexico. For. Chron. 79, 242–246 (2003).
Ramírez, M. I., Miranda, R., Zubieta, R. & Jiménez, M. Land cover and road network map for the Monarch Butterfly Biosphere Reserve in Mexico 2003. J. Maps 3, 181–190 (2007).
Zuur, A. F. & Ieno, E. N. Beginner’s Guide to Zero-Inflated Models with R (Highland Statistics Ltd, 2016).
Yackulic, C. B., Dodrill, M., Dzul, M., Sanderlin, J. S. & Reid, J. A. A need for speed in Bayesian population models: a practical guide to marginalizing and recovering discrete latent states. Ecol. Appl. 30, e02112 (2020).
Murray, K. & Conner, M. M. Methods to quantify variable importance: implications for the analysis of noisy ecological data. Ecology 90, 348–355 (2009).
Mac Nally, R. Hierarchical partitioning as an interpretative tool in multivariate inference. Austral Ecol. 21, 224–228 (1996).
Gelman, A., Goodrich, B., Gabry, J. & Vehtari, A. R-squared for Bayesian regression models. Am. Stat. 73, 307–309 (2019).
Carpenter, B. et al. Stan: a probabilistic programming language. J. Stat. Softw. 76, 1 (2017).
Stan Development Team. rstan: the R Interface to Stan. R package version 2.17.3 http://mc-stan.org/ (2018).
R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2019); https://www.R-project.org/
Gelman, A. & Rubin, D. B. Inference from iterative simulation using multiple sequences. Stat. Sci. 7, 457–472 (1992).
Gelman, A. & Hill, J. Data Analysis Using Regression and Multilevel/Hierarchical Models (Cambridge Univ. Press, 2007).
Acknowledgements
We thank the many volunteers who contributed to data collection. S. Altizer shared data and insights on the effects of disease and N. Haddad provided comments on the manuscript. This work was supported by NSF grant nos. EF-1702635 (EFZ), DBI-1954406 (EFZ) and EF-1702179 (LR).
Author information
Authors and Affiliations
Contributions
E.R.Z., L.R., K.S.O. and E.F.Z. conceived of the research. L.R., N.N., M.I.R., E.R.-S. and K.S.O. contributed data. E.R.Z, S.P.S., M.T.F. and E.F.Z. constructed the model. E.R.Z. ran analyses. E.R.Z. and E.F.Z. wrote the first drafts of the paper. All authors contributed to the interpretation of results and edits to the paper.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Additional information
Peer review information Nature Ecology & Evolution thanks Diana Bowler and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Extended data
Extended Data Fig. 1 Locations of monarch butterfly surveys on summer breeding grounds between 1994–2018.
Locations of surveys conducted between 14 Jun–15 Aug by the North American Butterfly Association (NABA; blue) and state-specific butterfly monitoring networks (BMNs; red) in a, 1994–2003 and b, 2004–2018. Counties (U.S.) and census districts (Canada) that are included in our delineation of the summer breeding range for the 1994–2003 reduced annual-cycle model and the 2004–2018 full annual-cycle model are outlined in grey.
Extended Data Fig. 2 Model-based index of monarch butterfly population size during peak summer, 1994–2018.
Model-based predictions (posterior medians with 95% credible intervals [CI]) of the expected number of adult monarchs observed per hour on an average NABA survey conducted between 19 Jul–15 Aug, 1994–2018, with linear trend (grey line) and 95% CI (shaded area; slope = –0.15 adults/hr/yr, 95% CI: –0.30, 0.01). Vertical dashed line denotes the break between our 1994–2003 and 2004–2018 analyses.
Extended Data Fig. 3 Changes in summer climate on monarch summer breeding grounds.
Percent change between 1994–2003 and 2004–20018 in a, average temperatures (GDD from 3 May–15 Aug) and b, cumulative precipitation (mm, Apr–Aug) for each U.S. county included in our delineation of the monarch summer breeding range. Temporal trends over a recent 15-year period (2004–2018) in c, GDD (°C/yr), and d, cumulative precipitation (mm/yr). Positive values indicate increases or positive trends in weather variables; negative values indicate decreases or negative trends. Canadian counties were excluded from panels a and b because data limitations prevented us from including these regions in our 1994–2003 model of monarch population dynamics.
Extended Data Fig. 4 Residuals from the winter submodel describing variation in the area occupied by monarch butterflies.
Estimated residuals (posterior medians) from the winter submodel describing the area occupied by monarchs in each of the overwintering supercolonies, when monarchs were present in early winter, 2004–2018. Solid grey line and shaded area represent a linear trend with 95% credible interval (slope= –0.003, 95% CI = –0.014, 0.008).
Extended Data Fig. 5 Effects of summer weather on monarch population size, 1994–2003.
a, Estimated marginal effects (median and 95% credible intervals) of GDD (deviation from county 10-year average) on expected monarch counts during peak summer (expected mean count of adult monarchs per search hour, 19 Jul–25 Jul), for typical cool, average, and warm counties (avgGDDc = 711, 898, and 1033 °C, respectively) within the summer breeding range, 1994–2003. b, Estimated marginal effects of precipitation (deviation from county 10-year average) on expected monarch counts during peak summer, for typical dry, average, and wet counties (avgPCPc = 422, 525, and 578 mm, respectively), 1994–2003.
Supplementary information
Supplementary Information
Supplementary text, references and Tables 1–5.
Rights and permissions
About this article
Cite this article
Zylstra, E.R., Ries, L., Neupane, N. et al. Changes in climate drive recent monarch butterfly dynamics. Nat Ecol Evol 5, 1441–1452 (2021). https://doi.org/10.1038/s41559-021-01504-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/s41559-021-01504-1
This article is cited by
-
Changes in landscape and climate in Mexico and Texas reveal small effects on migratory habitat of monarch butterflies (Danaus plexippus)
Scientific Reports (2024)
-
Mission Monarch: engaging the Canadian public for the conservation of a species at risk
Journal of Insect Conservation (2024)
-
The genome and sex-dependent responses to temperature in the common yellow butterfly, Eurema hecabe
BMC Biology (2023)
-
Survival of eggs to third instar of late-summer and fall-breeding monarch butterflies (Danaus plexippus) and queen butterflies (Danaus gilippus) in north Texas
Journal of Insect Conservation (2023)
-
Integrated Population Models: Achieving Their Potential
Journal of Statistical Theory and Practice (2023)