Global climate change is altering not only average temperatures, but also the distribution and abundance of precipitation. During winter in montane habitats, changing precipitation patterns mean changing snow fall, which will have profound ecological impacts. Snow is an effective insulator and decouples below-snow temperatures from air temperatures, providing a stable environment and determining microclimate conditions in the soil. A wide range of organisms take advantage of stable below-snow winter environments by overwinter in soil. Winter soil microclimate modulates the degree of stress, performance, and ultimately fitness for organisms that overwinter in the soil. During the coldest portions of winter, the insulating effect of snow protects organisms from potentially damaging or even lethal cold stress. However, protection from cold extremes comes at a cost: in ectothermic animals, energy consumption is dependent on body temperature, and so relatively warm below-snow conditions drain energy stores more quickly. In winter resources are limited and energy stores cannot be replenished, and complete depletion of energy stores can cause mortality. Even if organisms survive, post-winter fitness may also be impacted by energy depletion by reducing reserves available for growth and reproduction. We don’t yet understand the impacts of changing winter snow will have on overwintering organisms in montane environments. I hypothesize that winter snow cover, through regulation of winter microclimate, modulates the cause of stress and mortality (cold damage or energy depletion) for montane ectotherms overwintering in soil. By better understanding the impacts of changing winter snow cover on montane ectotherms, we may be better able to identify processes and populations that are vulnerable to climate change.

My dissertation aims to expand our understanding of the impact of snow cover on overwinter stress on insects that overwinter in the soil, by examining the impact of snow cover along elevation gradients, then extending the energy use model developed in Chapter 1 to test for impacts of plasticity. Finally I examine how overwinter conditions alter physiological processes upon emergence from overwintering. This work shows that winter snow cover has far reaching impacts on overwintering ectotherms, which are not equal across elevation, and have effects that can carry over into the growing season, expanding our understanding of changing winters and population impacts of climate change.

Chapter 1 establishes the energetic impacts and thermal challenges of changing snow cover along elevation gradients. Along elevational gradients snow cover increases but air temperature decreases, and it is unknown how these opposing gradients impact performance and fitness of organisms overwintering in the soil. I developed experimentally validated ecophysiological models of cold and energy stress over the past decade for the montane leaf beetle Chrysomela aeneicollis, along five replicated elevational transects in the Sierra Nevada mountains in California. Cold stress peaks at mid-elevations, while high elevations are buffered by persistent snow cover, even in dry years. While protective against cold, snow increases energy stress for overwintering beetles, particularly at low elevations, potentially leading to mortality or energetic trade-offs. Declining snowpack resulting in drier winters, will predominantly impact mid-elevation populations by increasing cold exposure, while high elevation habitats may provide refugia.

Chapter 2 focuses on the impacts of plasticity in metabolic-rate-temperature relationships in dormant organisms and their impacts on energy use estimates, expanding on the model developed in Chapter 1. Ecophysiological energy use models predict long-term energy use from metabolic rates, but we do not know the degree to which plasticity in metabolic intensity or thermal sensitivity impact energy use estimates. I quantified metabolic rate-temperature relationships of dormant willow beetles (Chrysomela aeneicollis) monthly from February to May under constant and variable acclimation treatments. Metabolic intensity increased through time, and acclimation altered both metabolic intensity and the thermal sensitivity. However, incorporating these two types of metabolic plasticity into energy use models did not improve energy use estimates, validated by empirical lipid measurements. Together, this indicates that while metabolic rate temperature relationships are plastic during winter, incorporating this plasticity does not improve prediction of energy use made by ecophysiological models, partly due to large individual variability in energy reserves.

Chapter 3 examines the impact that overwintering environment plays on prioritization of physiological processes upon emergence from dormancy, based on changes in gene expression. During winter, dormant organisms conserve resources through metabolic suppression and minimizing cellular processes. The transition from dormancy to active season requires a quick reversal of these processes and large-scale physiological transitions, enabling organisms to begin exploiting favorable environmental conditions. The impact of overwinter microclimate on the physiological processes involved in transitioning from dormancy to active season in insects are unknown. I conducted a field snow-cover manipulation and then profiled gene expression of willow leaf beetles Chrysomela aeneicollis during the transition out of dormancy using RNA-seq. Upon emergence from dormancy, beetles first prioritize up-regulation of transcripts associated with digestion and nutrient acquisition. The prioritization of nutrient acquisition is followed by investment into reproduction, but the timing is sex-specific with females investing sooner. Winter snow cover impacted the timing of these processes, with beetles that overwintered below snow being several days ahead of beetles that overwintered without snow. This highlights the importance of winter microclimate in regulating critical life history transitions.

Seasonality shapes major life-history strategies and adaptations across the tree of life. The alternating nature of seasons for growth and reproduction and seasons of adverse conditions can put conflicting selective pressures on energy use. Growing seasons often drive evolution of fast-paced processes and activity, while adverse seasons like winter drive evolution of dormancy and energy conservation. Thus, energy use strategies in seasonal environments have profound impacts on fitness. Integrating fitness across seasons and organismal responses to environmental change is key to understanding how populations will respond to ongoing global climate change. Energetics can play two essential roles in mediating organismal fitness in seasonal environments: energy reserves can determine winter survival, and energy at the end of winter can determine reproductive success. Survival and reproduction are both critical components of fitness, and thus energy allocation strategies may favor one over the other, revealing potential trade-offs when energy is limited. However, we do not know how environmental variation and predictability affect energy allocation strategies. Understanding the impacts of environmental change in seasonal environments will help us make better predictions of population responses and vulnerability to climate change.My dissertation aims to expand our understanding of overwintering energy use strategies, then explore how variable environments affect energy allocation strategies under a trade-off between maintenance and future reproduction. Finally, I test my predictions of energy allocation strategies under realistic winter conditions. Winter performance can determine summer performance, linking life cycles in seasonal environments. This work reveals the extent to which stochastic and predictable variation in seasonal environments can affect selective pressures and thus fitness in overwintering organisms. The carry-over effects of winter fitness into the growing season and vice versa expand our understanding of population responses to variable and changing environments. Chapter 1 explores the role of group behavior on energy conservation in overwintering aggregations, a potential energy use strategy that remains widely underexplored. The convergent ladybeetle (Hippodamia convergens) overwinters in massive aggregations, making it an ideal system for testing the effect of aggregation size on metabolic rates in overwintering insects. I measured energy use and thermal sensitivity of beetle aggregations across two ecologically relevant temperatures, and measured locomotor activity as one possible driver of group effects on energy use. Metabolic rates per beetle decreased with increasing aggregation size and scaled hypometrically with mass at both temperatures tested, with responses more pronounced at low temperatures. Activity decreased with aggregation size, but only at low temperatures. These results suggest that individuals within aggregations enter a deeper metabolically inactive state that single individual beetles cannot achieve, which is partly but not completely explained by a reduction in locomotor activity. This behavioral strategy for energy conservation may provide an additional selective advantage for the evolution of large overwintering aggregations. Chapter 2 explores the impact that variation in predictable and stochastic environments has on an energy allocation trade-off between somatic maintenance and future reproduction. Seasonality can modulate selection of energy use strategies, but we currently lack a theoretical framework to generate predictions on energy allocation strategies under changing stochastic conditions. Stochastic extreme events, like heat waves or cold snaps, are increasing in frequency and can have major impacts on population fitness. Overwintering organisms can prepare for harsh conditions by investing energy into stress tolerance (somatic maintenance). However, energy reserves at the end of winter can also influence future reproductive fitness, depending on the relative importance of stored versus recently acquired reserves for reproduction across the capital to income breeding continuum. In this chapter, I develop a general theoretical model that assesses fitness under increasing probability of stochastic lethal events, temporal variation in probability of stochastic events through winter, and how a stochastic end of winter affects optimal allocation strategies in income and capital breeders. Increasing probability of extreme events modulates allocation strategies in capital breeders. Temporal variation in extreme events and stochastic end of the season can alter optimal timing of investments, offering insights on the mismatch costs that changing environments may impose on overwintering organisms. These results highlight the role of end reserves in seasonal transitions and identify capital breeders to be especially susceptible to climate change. Chapter 3 tests the predictions from Chapter 2 by applying it to a case study of a capital breeder, the beetle Chrysomela aeneicollis, and answering how variation in snow cover can affect a trade-off between winter survival and future reproduction in realistic scenarios. Variation in snow cover modulates stochastic cold events and baseline energetic costs for organisms overwintering underground. Winters with deep snow cover have high baseline winter costs while having a low risk of lethal cold events. On the other hand, winters with little or no snow cover have low baseline winter costs but organisms are exposed to a high risk of lethal cold. In this chapter, I build on Chapter 2 by incorporating organism-specific parameters for energy reserves, rates of energy use, and microclimate conditions. I develop a model to systematically explore how cold risk, baseline winter costs, and their interaction under realistic winter scenarios affect energy use, survival, and allocation strategies of the willow leaf beetle (Chrysomela aeneicollis). My results support conclusions from Chapter 2, as increased cold risk and baseline costs can drive allocation strategies, but the response is strongly dependent on starting reserves. Increased cold risk affects future reproduction of beetles starting winter with high reserves, while increased baseline costs affect both reproduction and survival for lean beetles. Under realistic winter conditions, snow cover can modulate the trade-off between winter survival and future reproduction. Overwintering organisms under deep snow cover show high survival at the cost of reproduction, while winters with low snow favored reproduction at the cost of survival. These results show that both starting reserves and winter conditions, in the form of cold risk and baseline costs, drive distinct energy allocation strategies, and offer new insights into population dynamics and predictions under climate change.

Freshwater streams are incredibly variable habitats where abiotic conditions change daily and seasonally. The species that inhabit streams must have the physiological capacity to deal with that variation. Variation that extends outside of the limits of an organism’s tolerance thresholds can cause sub-lethal or lethal stress and dictate which habitats are suitable to the organism. In addition to variation in abiotic conditions, organisms must fit into the ecological interaction web of their habitat and handle variation in biotic conditions. In my dissertation, I focus on two pathways for organisms to encounter new sources of environmental variation: invasion of novel habitats and climate change. Understanding how organisms deal with environmental variation is critical to predicting where they can live now and in the future.

In Chapter 1, I aimed to identify the temperature and oxygen conditions that limit respiration and locomotion in the highly invasive New Zealand mud snail, Potamopyrgus antipodarum. To accomplish this, I generated thermal performance curves for resting respiration rate and voluntary locomotor behaviors under normoxia and hypoxia to find the conditions that limited each performance. I found that extremely high and low temperatures limited respiration and activity, but respiration rate was more sensitive to changes in oxygen at low temperatures. Hypoxia did not significantly decrease activity. Under hypoxic conditions, activity was less thermally sensitive, increased under high temperatures, and may be fueled by anaerobic metabolism. Relying on anaerobic energy is a time-limited survival strategy, so further warming and deoxygenation of freshwater systems may limit the spread of this invasive species.

In Chapter 2, I focused on finding the abiotic and biotic conditions that explain variation in Potamopyrgus antipodarum population density in San Francisco Bay Area streams. P. antipodarum is a prolific invader of freshwater streams in California and worldwide, with the ability to form extremely dense populations that dominate the invaded habitat. To strengthen our ability to predict where this species can thrive, it is critical to understand which abiotic and biotic conditions explain variation in population density. I approached this need by measuring 25 conditions over one year in three streams with varying densities of P. antipodarum populations. The different streams could be distinguished by their water chemistry profiles. Conductivity and filamentous green algae cover were the factors most correlated to population density, but there was only marginal linear statistical support for the response to algae. Overall, P. antipodarum is robust to considerable variation in many ecological factors, and each factor may have a small effect in controlling their population sizes.

In Chapter 3, I focused on the effect that past environmental variation, specifically thermal history, had on the response to different warming regimes in the larval caddisfly Dicosmoecus gilvipes. To accomplish this, I tested the molecular physiology responses of three populations of field-acclimatized D. gilvipes from different eco-regions (mountain, valley, coast) to current and future warming scenarios. I hypothesized that distinct thermal histories could differentiate populations at baseline levels of gene expression and gene expression changes in response to daily warming and heat shock. Population-specific responses were apparent under the control and daily warming conditions, while responses to heat shock were similar across populations. In addition, underlying gene expression patterns in the daily warming and heat shock treatments were different. These results highlight the importance and limitations of measuring the stress response of wild-caught organisms in their natural environment.