Untapped potential of physiology, behaviour and immune markers to predict range dynamics and marginality

From Wiley via Jisc Publications RouterHistory: received 2021-03-04, rev-recd 2021-09-09, accepted 2021-10-14, pub-electronic 2021-11-11Article version: VoRPublication status: PublishedFunder: Royal Society; Id: http://dx.doi.org/10.13039/501100000288; Grant(s): UF160725Funder: Natural Environment Research Council; Id: http://dx.doi.org/10.13039/501100000270; Grant(s): NE/L002469/1Abstract: Linking environmental conditions to the modulators of individual fitness is necessary to predict long‐term population dynamics, viability, and resilience. Functional physiological, behavioral, and reproductive markers can provide this mechanistic insight into how individuals perceive physiological, psychological, chemical, and physical environmental challenges through physiological and behavioral responses that are fitness proxies. We propose a Functional Marginality framework where relative changes in allostatic load, reproductive health, and behavior can be scaled up to evidence and establish causation of macroecological processes such as local extirpation, colonization, population dynamics, and range dynamics. To fully exploit functional traits, we need to move beyond single biomarker studies to develop an integrative approach that models the interactions between extrinsic challenges, physiological, and behavioral pathways and their modulators. In addition to providing mechanistic markers of range dynamics, this approach can also serve as a valuable conservation tool for evaluating individual‐ and population‐level health, predicting responses to future environmental change and measuring the impact of interventions. We highlight specific studies that have used complementary biomarkers to link extrinsic challenges to population performance. These frameworks of integrated biomarkers have untapped potential to identify causes of decline, predict future changes, and mitigate against future biodiversity loss

Linking diet switching to reproductive performance across populations of two critically endangered mammalian herbivores

Optimal foraging theory predicts that animals maximise energy intake by consuming the most valuable foods available. When resources are limited, they may include lower-quality fallback foods in their diets. As seasonal herbivore diet switching is understudied, we evaluate its extent and effects across three Kenyan reserves each for Critically Endangered eastern black rhino (Diceros bicornis michaeli) and Grevy’s zebra (Equus grevyi), and its associations with habitat quality, microbiome variation, and reproductive performance. Black rhino diet breadth increases with vegetation productivity (NDVI), whereas zebra diet breadth peaks at intermediate NDVI. Black rhino diets associated with higher vegetation productivity have less acacia (Fabaceae: Vachellia and Senegalia spp.) and more grass suggesting that acacia are fallback foods, upending conventional assumptions. Larger dietary shifts are associated with longer calving intervals. Grevy’s zebra diets in high rainfall areas are consistently grass-dominated, whereas in arid areas they primarily consume legumes during low vegetation productivity periods. Whilst microbiome composition between individuals is affected by the environment, and diet composition in black rhino, seasonal dietary shifts do not drive commensurate microbiome shifts. Documenting diet shifts across ecological gradients can increase the effectiveness of conservation by informing habitat suitability models and improving understanding of responses to resource limitation

Untapped potential of physiology, behaviour and immune markers to predict range dynamics and marginality

Linking environmental conditions to the modulators of individual fitness is necessary to predict long‐term population dynamics, viability, and resilience. Functional physiological, behavioral, and reproductive markers can provide this mechanistic insight into how individuals perceive physiological, psychological, chemical, and physical environmental challenges through physiological and behavioral responses that are fitness proxies. We propose a Functional Marginality framework where relative changes in allostatic load, reproductive health, and behavior can be scaled up to evidence and establish causation of macroecological processes such as local extirpation, colonization, population dynamics, and range dynamics. To fully exploit functional traits, we need to move beyond single biomarker studies to develop an integrative approach that models the interactions between extrinsic challenges, physiological, and behavioral pathways and their modulators. In addition to providing mechanistic markers of range dynamics, this approach can also serve as a valuable conservation tool for evaluating individual‐ and population‐level health, predicting responses to future environmental change and measuring the impact of interventions. We highlight specific studies that have used complementary biomarkers to link extrinsic challenges to population performance. These frameworks of integrated biomarkers have untapped potential to identify causes of decline, predict future changes, and mitigate against future biodiversity loss

Previous assessments of faecal glucocorticoid metabolites in Cape mountain zebra (<i>Equus zebra zebra</i>) were flawed

1. Steroid hormones, especially glucocorticoids (GCs), are widely used to assess physiological responses to stressors. As steroid hormones are heavily metabo lised prior to excretion, it is essential to validate enzyme immunoassays (EIAs) for measuring faecal glucocorticoid metabolites (fGCMs). Although problems with unvalidated assays have been raised repeatedly, their use persists widely. 2. Lea et al. (2017) used an unvalidated corticosterone assay (CJM006) to relate fGCM concentrations to habitat quality, demography and population perfor mance in the Cape mountain zebra (Equus zebra zebra). Here, we revisit their find ings and evaluate the validity of their conclusions using a validated EIA. First, we evaluate the biological sensitivity of six EIAs (three group-specific metabolite assays and three corticosterone assays, including CJM006) through a biologi cal validation experiment (translocation) for two sub-species of mountain zebra, Cape mountain and Hartmann's mountain zebra (E. z. hartmannae). Second, we reanalyse the faecal extracts from Lea et al. (2017) using a validated EIA. 3. fGCM concentrations consistently increased following translocation, when using two 11-oxoaetiocholanolone (lab codes: 72T and 72a) and an 11ß hydroxyaetiocholanolone (69a) EIA, but did not with three different corticoster one EIAs. All corticosterone EIAs (including CJM006) failed to detect an increase in fGCMs within the critical 48–72-h period post translocation. Therefore, the CJM006 EIA utilised in Lea et al. (2017) does not sensitively measure hypotha lamic–pituitary–adrenal (HPA) axis activity in CMZ faeces. 4. Using a validated assay (72T), fGCM concentrations were no longer associated with adult sex ratio or habitat quality (measured by grassiness) and these varia bles were dropped from predictive models. fGCM concentrations now varied be tween seasons and were negatively associated with female fecundity (foal:mare ratio). Consequently, we can conclude that the results of the previous study are unreliable. 5. We introduce the terms “insensitive” and “sub-optimal” to categorise assays that are tested but fail validation, and assays that are comparatively poor at detecting relevant hormone changes, respectively. We discuss how both “insensitive” and “sub-optimal” assays could lead to incorrect inferences about population stress ors and counterproductive conservation recommendationsPeer reviewe

Linking diet switching to reproductive performance across populations of two critically endangered mammalian herbivores

Abstract Optimal foraging theory predicts that animals maximise energy intake by consuming the most valuable foods available. When resources are limited, they may include lower-quality fallback foods in their diets. As seasonal herbivore diet switching is understudied, we evaluate its extent and effects across three Kenyan reserves each for Critically Endangered eastern black rhino (Diceros bicornis michaeli) and Grevy’s zebra (Equus grevyi), and its associations with habitat quality, microbiome variation, and reproductive performance. Black rhino diet breadth increases with vegetation productivity (NDVI), whereas zebra diet breadth peaks at intermediate NDVI. Black rhino diets associated with higher vegetation productivity have less acacia (Fabaceae: Vachellia and Senegalia spp.) and more grass suggesting that acacia are fallback foods, upending conventional assumptions. Larger dietary shifts are associated with longer calving intervals. Grevy’s zebra diets in high rainfall areas are consistently grass-dominated, whereas in arid areas they primarily consume legumes during low vegetation productivity periods. Whilst microbiome composition between individuals is affected by the environment, and diet composition in black rhino, seasonal dietary shifts do not drive commensurate microbiome shifts. Documenting diet shifts across ecological gradients can increase the effectiveness of conservation by informing habitat suitability models and improving understanding of responses to resource limitation