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

The social and cultural roots of whale and dolphin brains

Encephalization, or brain expansion, underpins humans’ sophisticated social cognition, including language, joint attention, shared goals, teaching, consensus decision-making and empathy. These abilities promote and stabilize cooperative social interactions, and have allowed us to create a ‘cognitive’ or ‘cultural’ niche and colonize almost every terrestrial ecosystem. Cetaceans (whales and dolphins) also have exceptionally large and anatomically sophisticated brains. Here, by evaluating a comprehensive database of brain size, social structures and cultural behaviours across cetacean species, we ask whether cetacean brains are similarly associated with a marine cultural niche. We show that cetacean encephalization is predicted by both social structure and by a quadratic relationship with group size. Moreover, brain size predicts the breadth of social and cultural behaviours, as well as ecological factors (diversity of prey types and to a lesser extent latitudinal range). The apparent coevolution of brains, social structure and behavioural richness of marine mammals provides a unique and striking parallel to the large brains and hyper-sociality of humans and other primates. Our results suggest that cetacean social cognition might similarly have arisen to provide the capacity to learn and use a diverse set of behavioural strategies in response to the challenges of social living

Social stability in semiferal ponies: networks show interannual stability alongside seasonal flexibility

Long-term relationships that underlie many stable mammalian groups often occur between philopatric kin. Although stable groups of nonrelatives appear to be less common, there is increasing evidence that social bonds between nonkin may confer sufficient intrinsic fitness benefits for these groups to persist. Here we evaluate whether social stability occurs in a bisexually dispersing species where social bonds have been shown to have reproductive benefits: the feral horse, Equus caballus. First, we quantified female social stability by applying a three-level framework to a 3-year data set of associations in semiferal ponies; this tested for stability at the individual, dyadic and subpopulation levels. Despite the relative weakness of these female bonds, we found significant social stability across all levels, as shown by stable association preferences, social networks and individual network positions. Second, we investigated how seasonality impacts on social bond strength and grouping patterns. We found seasonal fluctuations in female gregariousness, with a peak during the mating season. We therefore propose that significant social stability in female horses is coupled with a degree of flexibility that allows for effects of ecological fluctuations. Although social network analysis is widely used in behavioural ecological research, this is one of only a handful of studies to assess the temporal dynamics of networks over a significant timescale. Temporal stability in female relationships suggests that equid social structures are multifaceted: although bonds between stallions and mares are clearly strong, long-term relationships between mares underpin the social network structure. We suggest this framework could be used to assess social stability in other group-living species in order to improve our understanding of the nature of social bonds

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