Is our understanding of aquatic ecosystems sufficient to quantify ecologically driven climate feedbacks?

The Earth functions as an integrated system-its current habitability to complex life is an emergent property dependent on interactions among biological, chemical, and physical components. As global warming affects ecosystem structure and function, so too will the biosphere affect climate by altering atmospheric gas composition and planetary albedo. Constraining these ecosystem-climate feedbacks is essential to accurately predict future change and develop mitigation strategies; however, the interplay among ecosystem processes complicates the assessment of their impact. Here, we explore the state-of-knowledge on how ecological and biological processes (e.g., competition, trophic interactions, metabolism, and adaptation) affect the directionality and magnitude of feedbacks between ecosystems and climate, using illustrative examples from the aquatic sphere. We argue that, despite ample evidence for the likely significance of many, our present understanding of the combinatorial effects of ecosystem dynamics precludes the robust quantification of most ecologically driven climate feedbacks. Constraining these effects must be prioritized within the ecological sciences for only by studying the biosphere as both subject and arbiter of global climate can we develop a sufficiently holistic view of the Earth system to accurately predict Earth's future and unravel its past.

La Terre fonctionne comme un système intégré­son habitabilité pour une vie complexe est une propriété émergente qui dépend des interactions entre les composantes biologiques, chimiques et physiques. Le réchauffement climatique affecte la structure et la fonction des écosystèmes, et en retour, la biosphère affecte également le climat en modifiant la composition des gaz atmosphériques et l'albédo planétaire. Il est essentiel de quantifier ces rétroactions entre les écosystèmes et le climat afin de prédire avec précision les changements futurs et élaborer des stratégies d'atténuation; cependant, l'interaction entre les processus écologiques complique l'évaluation de leurs impacts. Dans cet article, nous examinons l'état des connaissances sur la façon dont les processus écologiques et biologiques (par exemple, la concurrence, les interactions trophiques, le métabolisme, l'adaptation) affectent la directionnalité et l'ampleur des rétroactions entre les écosystèmes et le climat à l'aide d'exemples issus du monde aquatique. Nous soutenons que, malgré les nombreuses preuves de l'importance de plusieurs de ces rétroactions, notre compréhension limitée des effets additifs des processus écosystémiques empêche de faire une quantification robuste de la plupart des rétroactions climatiques d'origine écologique. Circonscrire ces effets doit être une priorité pour les sciences aquatiques, car ce n'est qu'en étudiant la biosphère en tant que sujet et arbitre du climat planétaire que nous pourrons développer une vision suffisamment holistique du système terrestre pour prédire avec précision l'avenir de la Terre et élucider son passé.

Starvation reduces thermal limits of the widespread copepod Acartia tonsa.

Organismal thermal limits affect a wide range of biogeographical and ecological processes. Copepods are some of the most abundant animals on the planet and play key roles in aquatic habitats. Despite their abundance and ecological importance, there is limited data on the factors that affect copepod thermal limits, impeding our ability to predict how aquatic ecosystems will be affected by anthropogenic climate change. In a warming ocean, one factor that may have particularly important effects on thermal limits is the availability of food. A recently proposed feedback loop known as "metabolic meltdown" suggests that starvation and exposure to high temperatures interact to drastically reduce organismal thermal limits, increasing vulnerability to warming. To investigate one component of this feedback loop, we examined how starvation affects thermal limits (critical thermal maxima: CTmax) of Acartia tonsa, a widespread estuarine copepod. We found that there was no effect of short-duration exposure to starvation (up to 2 days). However, after 3 days, there was a significant decrease in the CTmax of starved copepods relative to the fed controls. Our results provide empirical evidence that extended periods of starvation reduce thermal limits, potentially initiating "metabolic meltdown" in this key species of coastal copepod. This suggests that changes in food availability may increase the vulnerability of copepods to increasing temperatures, amplifying the effects of climate change on coastal systems.

Parasitism does not reduce thermal limits in the intermediate host of a bopyrid isopod.

Parasitism has strong effects on community dynamics. Given the detrimental effects parasites have on host health, infection or infestation might be expected to reduce upper thermal limits, increasing the vulnerability of host species to future climate change. Copepods are integral components of aquatic food webs and biogeochemical cycles. They also serve as intermediate hosts in the life cycle of parasitic isopods in the family Bopyridae. As both copepods and isopod parasites play important roles in aquatic communities, it is important to understand how the interaction between parasite and host affects thermal limits in order to better predict how community dynamics may change in a warming climate. Here we examined the effect of infestation by larvae of a bopyrid isopod on the cosmopolitan copepod Acartia tonsa to test the hypothesis that infestation reduces thermal limits. To aid with this work, we developed an affordable, highly portable system for measuring critical thermal maxima of small ectotherms. We also used meta-analysis to summarize the effects of parasitism on critical thermal maxima in a wider range of taxa to help contextualize our findings. Contrary to both our hypothesis and the results of previous studies, we observed no reduction of thermal limits by parasitism in A. tonsa. These results suggest that life history of the host and parasite may interact to determine how parasite infestation affects environmental sensitivity.

Naupliar exposure to acute warming does not affect ontogenetic patterns in respiration, body size, or development time in the cosmopolitan copepod Acartia tonsa.

Short-term, acute warming events are increasing in frequency across the world's oceans. For short-lived species like most copepods, these extreme events can occur over both within- and between-generational time scales. Yet, it is unclear whether exposure to acute warming during early life stages of copepods can cause lingering effects on metabolism through development, even after the event has ended. These lingering effects would reduce the amount of energy devoted to growth and affect copepod population dynamics. We exposed nauplii of an ecologically important coastal species, Acartia tonsa, to a 24-hour warming event (control: 18°C; treatment: 28°C), and then tracked individual respiration rate, body length, and stage duration through development. As expected, we observed a decrease in mass-specific respiration rates as individuals developed. However, exposure to acute warming had no effect on the ontogenetic patterns in per-capita or mass-specific respiration rates, body length, or development time. The lack of these carryover effects through ontogeny suggests within-generational resilience to acute warming in this copepod species.

Limited plasticity in thermally tolerant ectotherm populations: evidence for a trade-off.

Many species face extinction risks owing to climate change, and there is an urgent need to identify which species' populations will be most vulnerable. Plasticity in heat tolerance, which includes acclimation or hardening, occurs when prior exposure to a warmer temperature changes an organism's upper thermal limit. The capacity for thermal acclimation could provide protection against warming, but prior work has found few generalizable patterns to explain variation in this trait. Here, we report the results of, to our knowledge, the first meta-analysis to examine within-species variation in thermal plasticity, using results from 20 studies (19 species) that quantified thermal acclimation capacities across 78 populations. We used meta-regression to evaluate two leading hypotheses. The climate variability hypothesis predicts that populations from more thermally variable habitats will have greater plasticity, while the trade-off hypothesis predicts that populations with the lowest heat tolerance will have the greatest plasticity. Our analysis indicates strong support for the trade-off hypothesis because populations with greater thermal tolerance had reduced plasticity. These results advance our understanding of variation in populations' susceptibility to climate change and imply that populations with the highest thermal tolerance may have limited phenotypic plasticity to adjust to ongoing climate warming.

Negative relationship between thermal tolerance and plasticity in tolerance emerges during experimental evolution in a widespread marine invertebrate.

Whether populations can adapt to predicted climate change conditions, and how rapidly, are critical questions for the management of natural systems. Experimental evolution has become an important tool to answer these questions. In order to provide useful, realistic insights into the adaptive response of populations to climate change, there needs to be careful consideration of how genetic differentiation and phenotypic plasticity interact to generate observed phenotypic changes. We exposed three populations of the widespread copepod Acartia tonsa (Crustacea) to chronic, sublethal temperature selection for 15 generations. We generated thermal survivorship curves at regular intervals both during and after this period of selection to track the evolution of thermal tolerance. Using reciprocal transplants between ambient and warming conditions, we also tracked changes in the strength of phenotypic plasticity in thermal tolerance. We observed significant increases in thermal tolerance in the Warming lineages, while plasticity in thermal tolerance was strongly reduced. We suggest these changes are driven by a negative relationship between thermal tolerance and plasticity in thermal tolerance. Our results indicate that adaptation to warming through an increase in thermal tolerance might not reduce vulnerability to climate change if the increase comes at the expense of tolerance plasticity. These results illustrate the importance of considering changes in both a trait of interest and the trait plasticity during experimental evolution.

Adaptation to simultaneous warming and acidification carries a thermal tolerance cost in a marine copepod.

The ocean is undergoing warming and acidification. Thermal tolerance is affected both by evolutionary adaptation and developmental plasticity. Yet, thermal tolerance in animals adapted to simultaneous warming and acidification is unknown. We experimentally evolved the ubiquitous copepod Acartia tonsa to future combined ocean warming and acidification conditions (OWA approx. 22°C, 2000 µatm CO2) and then compared its thermal tolerance relative to ambient conditions (AM approx. 18°C, 400 µatm CO2). The OWA and AM treatments were reciprocally transplanted after 65 generations to assess effects of developmental conditions on thermal tolerance and potential costs of adaptation. Treatments transplanted from OWA to AM conditions were assessed at the F1 and F9 generations following transplant. Adaptation to warming and acidification, paradoxically, reduces both thermal tolerance and phenotypic plasticity. These costs of adaptation to combined warming and acidification may limit future population resilience.

Genetic differentiation underlies seasonal variation in thermal tolerance, body size, and plasticity in a short-lived copepod.

Organisms experience variation in the thermal environment on several different temporal scales, with seasonality being particularly prominent in temperate regions. For organisms with short generation times, seasonal variation is experienced across, rather than within, generations. How this affects the seasonal evolution of thermal tolerance and phenotypic plasticity is understudied, but has direct implications for the thermal ecology of these organisms. Here we document intra-annual patterns of thermal tolerance in two species of Acartia copepods (Crustacea) from a highly seasonal estuary, showing strong variation across the annual temperature cycle. Common garden, split-brood experiments indicate that this seasonal variation in thermal tolerance, along with seasonal variation in body size and phenotypic plasticity, is likely affected by genetic polymorphism. Our results show that adaptation to seasonal variation is important to consider when predicting how populations may respond to ongoing climate change.

Integrating patterns of thermal tolerance and phenotypic plasticity with population genetics to improve understanding of vulnerability to warming in a widespread copepod.

Differences in population vulnerability to warming are defined by spatial patterns in thermal adaptation. These patterns may be driven by natural selection over spatial environmental gradients, but can also be shaped by gene flow, especially in marine taxa with high dispersal potential. Understanding and predicting organismal responses to warming requires disentangling the opposing effects of selection and gene flow. We begin by documenting genetic divergence of thermal tolerance and developmental phenotypic plasticity. Ten populations of the widespread copepod Acartia tonsa were collected from sites across a large thermal gradient, ranging from the Florida Keys to Northern New Brunswick, Canada (spanning over 20° latitude). Thermal performance curves (TPCs) from common garden experiments revealed local adaptation at the sampling range extremes, with thermal tolerance increasing at low latitudes and decreasing at high latitudes. The opposite pattern was observed in phenotypic plasticity, which was strongest at high latitudes. No relationship was observed between phenotypic plasticity and environmental variables. Instead, the results are consistent with the hypothesis of a trade-off between thermal tolerance and the strength of phenotypic plasticity. Over a large portion of the sampled range, however, we observed a remarkable lack of differentiation of TPCs. To examine whether this lack of divergence is the result of selection for a generalist performance curve or constraint by gene flow, we analyzed cytochrome oxidase I mtDNA sequences, which revealed four distinct genetic clades, abundant genetic diversity, and widely distributed haplotypes. Strong divergence in thermal performance within genetic clades, however, suggests that the pace of thermal adaptation can be relatively rapid. The combined insight from the laboratory physiological experiments and genetic data indicate that gene flow constrains differentiation of TPCs. This balance between gene flow and selection has implications for patterns of vulnerability to warming. Taking both genetic differentiation and phenotypic plasticity into account, our results suggest that local adaptation does not increase vulnerability to warming, and that low-latitude populations in general may be more vulnerable to predicted temperature change over the next century.

Complex interactions between local adaptation, phenotypic plasticity and sex affect vulnerability to warming in a widespread marine copepod.

Predicting the response of populations to climate change requires an understanding of how various factors affect thermal performance. Genetic differentiation is well known to affect thermal performance, but the effects of sex and developmental phenotypic plasticity often go uncharacterized. We used common garden experiments to test for effects of local adaptation, developmental phenotypic plasticity and individual sex on thermal performance of the ubiquitous copepod, Acartia tonsa (Calanoida, Crustacea) from two populations strongly differing in thermal regimes (Florida and Connecticut, USA). Females had higher thermal tolerance than males in both populations, while the Florida population had higher thermal tolerance compared with the Connecticut population. An effect of developmental phenotypic plasticity on thermal tolerance was observed only in the Connecticut population. Our results show clearly that thermal performance is affected by complex interactions of the three tested variables. Ignoring sex-specific differences in thermal performance may result in a severe underestimation of population-level impacts of warming because of population decline due to sperm limitation. Furthermore, despite having a higher thermal tolerance, low-latitude populations may be more vulnerable to warming as they lack the ability to respond to increases in temperature through phenotypic plasticity.

Adaptation to a latitudinal thermal gradient within a widespread copepod species: the contributions of genetic divergence and phenotypic plasticity.

Understanding how populations adapt to heterogeneous thermal regimes is essential for comprehending how latitudinal gradients in species diversification are formed, and how taxa will respond to ongoing climate change. Adaptation can occur by innate genetic factors, by phenotypic plasticity, or by a combination of both mechanisms. Yet, the relative contribution of such mechanisms to large-scale latitudinal gradients of thermal tolerance across conspecific populations remains unclear. We examine thermal performance in 11 populations of the intertidal copepod Tigriopus californicus, ranging from Baja California Sur (Mexico) to British Columbia (Canada). Common garden experiments show that survivorship to acute heat-stress differs between populations (by up to 3.8°C in LD50 values), reflecting a strong genetic thermal adaptation. Using a split-brood experiment with two rearing temperatures, we also show that developmental phenotypic plasticity is beneficial to thermal tolerance (by up to 1.3°C), and that this effect differs across populations. Although genetic divergence in heat tolerance strongly correlates with latitude and temperature, differences in the plastic response do not. In the context of climate warming, our results confirm the general prediction that low-latitude populations are most susceptible to local extinction because genetic adaptation has placed physiological limits closer to current environmental maxima, but our results also contradict the prediction that phenotypic plasticity is constrained at lower latitudes.