Michael Collins

Aim: The aim of this study was to understand the interplay between local and regional factors as drivers of population physiological diversity in a tropical freshwater crab species. Location: Western Ghats, south‐west India. Taxon: Barytelphusa cunicularis, Brachyura, Crustacea. Methods: We applied an integrative approach combining population genetics and whole animal physiology, using the tropical freshwater crab Barytelphusa cunicularis as our model species. We tested for effects of population location (e.g., latitude, altitude), season (as a proxy for rainfall and water temperature) and/or warming on indices of whole animal respiratory physiology (metabolic rate, MO ₂ ) and hypoxic performance (P _crit , i.e., the PO ₂ at which routine MO ₂ can no longer be sustained) in five widely distributed populations of this species. We also generated population genetic data (mtDNA COI and nDNA histone H3 sequences) to determine the extent of any population genetic structuring and/or cryptic species diversity present to verify that we were investigating a single species. Results: Despite a high level of genetic structuring between the different populations of B. cunicularis examined, the genetic distances observed were consistent with intra‐ and not interspecific differences in freshwater crabs. Populations varied in the diversity of the physiological (MO ₂ ) responses observed. There were significant effects of season and population on respiration in response to temperature and P _crit in response to acute hypoxia. Main Conclusions: We conclude that local environmental factors are important in shaping physiological diversity between populations in tropical freshwater species and systems. This highlights the need to include population‐level responses in any projections we make on how biodiversity will respond to ongoing and future environmental changes, including those caused by climate change.

In the Anthropocene, species are increasingly faced with multiple stressors that are more severe and less predictable than before. While multiple stressors often interact to affect organisms negatively, sometimes these interactions can be beneficial, enhancing resilience through cross-protection. Cross-protection interactions occur when exposure to one stressor, such as elevated temperature, enhances an organism’s tolerance to a different stressor, like hypoxia, through shared protective mechanisms or signaling pathways. Understanding the potential for cross-protection to combat rapid and diverse environmental change is crucial for conservation, as it potentially alters the predicted consequences of such change. Here, we outline 10 key considerations for investigating cross-protection in a conservation context. These considerations include the importance of stressor intensity and timing, recognizing species-specific and sex-specific responses, and embracing temporal variability in environmental stressors. Additionally, predictions will depend upon uncovering the underlying mechanisms of cross-protection by integrating emerging approaches like omics and meta-analyses. By better understanding—and in some cases explicitly leveraging—cross-protective interactions, conservation practitioners may be able to develop more effective management plans to enhance species resilience, potentially mitigating the immediate effects of emerging stressors. These insights are vital for guiding future research directions and informing conservation policies and management practices to preserve biodiversity in the Anthropocene.

Aquatic animals increasingly encounter environmental hypoxia due to climate-related warming and/or eutrophication. Although acute warming typically reduces performance under hypoxia, the ability of organisms to modulate hypoxic performance via thermal acclimation is less understood. Here, we review the literature and ask whether hypoxic performance of aquatic ectotherms improves following warm acclimation. Interpretation of thermal acclimation effects is limited by reliance on data from experiments that are not designed to directly test for beneficial or detrimental effects on hypoxic performance. Most studies have tested hypoxic responses exclusively at test temperatures matching organisms' acclimation temperatures, precluding the possibility of distinguishing between acclimation and acute thermal effects. Only a few studies have applied appropriate methodology to identify beneficial thermal acclimation effects on hypoxic performance, i.e. acclimation to different temperatures prior to determining hypoxic responses at standardised test temperatures. These studies reveal that acute warming predominantly impairs hypoxic performance, whereas warm acclimation tends to be either beneficial or have no effect. If this generalises, we predict that warm-acclimated individuals in some species should outperform non-acclimated individuals under hypoxia. However, acclimation seems to only partially offset acute warming effects; therefore, aquatic ectotherms will probably display overall reduced hypoxic performance in the long term. Drawing on the appropriate methodology, future studies can quantify the ability of organisms to modulate hypoxic performance via (reversible) thermal acclimation and unravel the underlying mechanisms. Testing whether developmental acclimation and multigenerational effects allow for a more complete compensation is essential to allow us to predict species' resilience to chronically warmer, hypoxic environments.

The adaptive value of phenotypic plasticity for performance under single stressors is well documented. However, plasticity may only truly be adaptive in the natural multifactorial environment if it confers resilience to stressors of a different nature, a phenomenon known as cross‐tolerance. An understanding of the mechanistic basis of cross‐tolerance is essential to aid prediction of species resilience to future environmental change. Here, we identified mechanisms underpinning cross‐tolerance between two stressors predicted to increasingly challenge aquatic ecosystems under climate change, chronic warming and hypoxia, in an ecologically‐important aquatic invertebrate. Warm acclimation improved hypoxic performance through an adaptive hypometabolic strategy and changes in the expression of hundreds of genes that are important in the response to hypoxia. These ‘frontloaded’ genes showed a reduced reaction to hypoxia in the warm acclimated compared to the cold acclimated group. Frontloaded genes included stress indicators, immune response and protein synthesis genes that are protective at the cellular level. We conclude that increased constitutive gene expression as a result of warm acclimation reduced the requirement for inducible stress responses to hypoxia. We propose that transcriptional frontloading contributes to cross‐tolerance between stressors and may promote fitness of organisms in environments increasingly challenged by multiple anthropogenic threats.

The prevalence of hypoxic areas in coastal waters is predicted to increase and lead to reduced biodiversity. While the adult stages of many estuarine invertebrates can cope with short periods of hypoxia, it remains unclear whether that ability is present if animals are bred and reared under chronic hypoxia. We firstly investigated the effect of moderate, short-term environmental hypoxia (40% air saturation for one week) on metabolic performance in adults of an estuarine amphipod, and the fitness consequences of prolonged exposure. We then reared the offspring of hypoxia-exposed parents under hypoxia, and assessed their oxyregulatory ability under declining oxygen tensions as juveniles and adults. Adults from the parental generation were able to acclimate their metabolism to hypoxia after one week, employing mechanisms typically associated with prolonged exposure. Their progeny, however, did not develop the adult pattern of respiratory regulation when reared under chronic hypoxia, but instead exhibited a poorer oxyregulatory ability than their parents. We conclude that species apparently hypoxia-tolerant when tested in short-term experiments, could be physiologically compromised as adults if they develop under hypoxia. Consequently, we propose that the increased prevalence of hypoxia in coastal regions will have marked effects in some species currently considered hypoxia tolerant.