COMMENTARY

Seasonal climate change and demography COMMENTARY Nigel G. Yoccoza,1

Seasons strongly influence the life cycles of many spe- of the study has now increased by 50 d, with the grow- cies on Earth, and it is therefore not surprising that ing season in some recent years being as long as some of the best evidence we have of the ecological 200 d. Surprisingly this very large change did not ap- response to recent climate change comes from stud- pear to be among the major drivers of marmot sur- ies of phenology, the timing of seasonal events (1). We vival, in either winter or summer, despite expectations know, however, less about the demographic impacts that should benefit from a prolonged access of climate change within each season, how consistent to food before hibernating. Cordes et al. (2) provide those effects are across seasons and age groups, and different explanations for this unexpected result, from if they could compensate or, on the contrary, amplify increased during extended summers to each other. Cordes et al. (2) provide a detailed analysis lower quality of food at critical times such as pup of seasonal demographic changes in an alpine mam- emergence. This illustrates a common issue in many mal, the yellow-bellied marmot (Marmota flaviventer), ecological studies of the impacts of climate change— which reveals the complexity of responses to climatic that there are many potential mechanisms linking change. For example, increasing summer drought a given change in climate, in this case decreased severity led to a decrease in pup and adult winter snowfall and increased temperature leading to a survival, whereas an increase in summer maximum longer growing season—and demography. We are temperatures and length of the growing season seldom able to measure all relevant covariates, which tended to increase yearling and adult summer sur- leaves us with different interpretations of the causal vival. Overall, negative effects dominated across the pathways. multiple impacts of climate change, as the winter season is a critical bottleneck for these hibernating Winter and Summer Variation . Nevertheless, the many pathways linking Yellow-bellied marmots are medium-lived mammals, climate change and marmot demography and the with a generation time of 4 to 5 y (3). We expect that uncertainty associated with projected seasonal cli- adult survival would vary less in response to environ- matic changes make predictions of the marmots’ fu- mental variation than other demographic traits such as ture very uncertain. Integrating refined projections pup survival (4). This is partly what Cordes et al. (2) of seasonal climates and models of demographic found, with large effects of environmental covariates changessuchasCordesetal.(2)doisanimportant on summer and winter pup survival and small effects, challenge for future work. often not statistically significant, on adult survival. We Cordes et al. (2) used 40 y (1979 to 2018) of high- do not have, however, clear predictions regarding quality, individual data collected at high-elevation these seasonal effects: Do we expect different sensi- (2,700 to 3,100 m above sea level) sites in Colorado. tivities to seasonal variation depending on the age They used advanced capture–recapture statistical classes? How does seasonal sensitivity change be- models to relate female survival within each season tween short- and long-lived species, that is, could to environmental covariates measured at the same short-lived species be more sensitive to winter vari- site. Overall, the observed climatic changes were con- ability than long-lived species, but could the reverse sistent with expectations: decreasing total snowfall, be true for summer variability? Consider annual sur- earlier snowmelt date, increasing summer maximum vival, the parameter that has been the focus of com- temperatures, and more intense drought. One of the parative ecological and evolutionary studies; it is the most striking potential ecological consequences of product of winter and summer survival. A proportional relevance to the marmots is the extended growing change in winter or summer survival will then have the season, which from being 115 d long at the beginning same proportional effect on annual survival. Winter

aDepartment of Arctic and Marine Biology, UiT The Arctic University of Norway, N-9037 Tromsø, Norway Author contributions: N.G.Y. wrote the paper. The author declares no competing interest. Published under the PNAS license. See companion article, “Contrasting effects of climate change on seasonal survival of a hibernating ,” 10.1073/pnas.1918584117. 1Email: [email protected]. First published July 24, 2020.

www.pnas.org/cgi/doi/10.1073/pnas.2012792117 PNAS | August 11, 2020 | vol. 117 | no. 32 | 18921–18923 Downloaded by guest on September 27, 2021 and summer survival have the same elasticities (elasticities quan- affect the whole life, and such cohort effects, determined by tify how a proportional change in survival leads to a proportional conditions experienced early in life, are known to be important change in population growth rate) and we expect no difference in drivers of life-history variation in many species, including marmots relative variability if the negative consequences of demographic (13). Statistically, it is challenging to distinguish between age, variation are compensated across demographic rates and seasons cohort, and time effects, as when we know the age and time we (4). However, this does not mean that the effects of seasonal en- also know when an individual was born, that is, the cohort (14). vironmental variation will be the same for winter and summer, as Simplifying assumptions about the age, cohort, and time effects some seasons may be more variable than others (5), and patterns must be made—for example, that they are additive, or that one of seasonal variability may change over time and differ among effect is ignored—but results can be sensitive to these assump- continents (6). As studies accumulate on seasonal demographic tions at the same time as there is often not information in the data changes, we will be able to test refined hypotheses about the to robustly assess the assumptions. As data accumulate, one can interplay between environmental variation at different time scales look forward to even more refined analyses that will robustly at- and the evolution of life-history traits. tribute observed demographic variation to intrinsic (age and co- hort) and extrinsic (environment) variation. Seasonal Effects May Differ between Mountain Ranges Can the results of Cordes et al. (2) be extrapolated to other spe- Value of Long-Term Studies cies and sites? Marmots hibernate in a and the main lim- The important results obtained in Cordes et al. (2) show once iting factor in winter is available reserves and thermoregulatory more the importance of long-term studies using marked individ- loss, not access to resources or predation. Cordes et al. (2) found uals (15). Environmental covariates as well as survival rates in this that drought severity had a consistent negative effect on pup and study showed consistent trends but also large variation—growing adult winter survival, because dry summers limit body mass gain season by nearly a factor of 2, and total snowfall even more, from during the summer, and body mass drives variation in winter 5 m to 16 m. Obtaining reliable estimates of the effects of envi- survival. Drought has increased recently in the western United ronmental variation implies that we have a big enough sample of States, particularly around 2000 to 2010 (7), and drought there- years with various combinations of environmental factors. How- fore affects even high-elevation species. However, long-term ever, even 40 y of data represents a small sample if many factors studies of the European cousin of the yellow-bellied marmot, have an effect, and sampling and model uncertainty might explain the alpine marmot (Marmota marmota), have found that the in part the disparate effects found in Cordes et al. (2), for example dominant effect in the was through winter climate: Cold and that yearling winter survival was not affected by environmental dry winters, with little protective snow cover, led to lower winter variation whereas pup and adult survival were. More than real survival (8) and decreasing litter size through an effect on body ecological differences, one may suspect that such differences in mass in the spring (9). The main difference between the two sys- statistical models supported by the data reflect sampling tems lies in the different snow depths during the winter, with shallower snow cover in the European Alps than in Colorado (8). variation. Yellow-bellied marmots in Colorado are well insulated from winter Despite the importance of seasonal variation for life-history temperature variation, whereas alpine marmots are not, but this traits (16) and population dynamics (17), we surprisingly lack a might change if winter snowfall continues to decrease in Colorado good roadmap to study, analyze, and predict consequences of and yellow-bellied marmots become more susceptible to the di- seasonal changes on species and ecosystems. Season length has rect effect of winter climate. Alpine marmots, on the other hand, been the focus of both theoretical and empirical studies, and it might become more susceptible to drought, which is increasing in can have major influences on, for example, small mammal pop- – frequency in the Alps (10). Knowledge acquired from one system ulation cycles (18) or predator prey dynamics (19). However, such may become relevant to other systems as climatic change may studies assume that winter and summer stay the same, except for lead to a shift from one state—mainly summer climate effects on their length. Species-specific phenology changes and the match– winter survival—to another—mainly winter climate effects on mismatch hypothesis have been thoroughly studied (20), but survival. these studies focus on one specific time of the year. Such periods Interestingly, the effect of summer conditions on winter sur- might be critical for reproduction and survival and often corre- vival found by Cordes et al. (2) represents a short-term carryover spond to conspicuous events (budburst or molt). However, with- effect (11), mediated by body mass, and carryover effects have out long-term, year-round studies investigating variations within been found in many species; for example, cold winters may have a and between seasons of demographic traits (2, 21) we might miss direct negative effect on survival, but this effect may extend to the consequences of changes in other seasons, and how events in one following summer in oystercatchers (12). Carryover effects can season may carry over to the next season and the whole lifespan.

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