Publications by year
2023
Siracusa ER, Pereira AS, Brask JB, Negron-Del Valle JE, Phillips D, Platt ML, Higham JP, Snyder-Mackler N, Brent LJN (2023). Ageing in a collective: the impact of ageing individuals on social network structure.
Philosophical Transactions of the Royal Society B: Biological Sciences,
378(1874).
Abstract:
Ageing in a collective: the impact of ageing individuals on social network structure
Ageing affects many phenotypic traits, but its consequences for social behaviour have only recently become apparent. Social networks emerge from associations between individuals. The changes in sociality that occur as individuals get older are thus likely to impact network structure, yet this remains unstudied. Here we use empirical data from free-ranging rhesus macaques and an agent-based model to test how age-based changes in social behaviour feed up to influence: (i) an individual's level of indirect connectedness in their network and (ii) overall patterns of network structure. Our empirical analyses revealed that female macaques became less indirectly connected as they aged for some, but not for all network measures examined. This suggests that indirect connectivity is affected by ageing, and that ageing animals can remain well integrated in some social contexts. Surprisingly, we did not find evidence for a relationship between age distribution and the structure of female macaque networks. We used an agent-based model to gain further understanding of the link between age-based differences in sociality and global network structure, and under which circumstances global effects may be detectable. Overall, our results suggest a potentially important and underappreciated role of age in the structure and function of animal collectives, which warrants further investigation.
. This article is part of a discussion meeting issue ‘Collective behaviour through time’.
Abstract.
Rosado MRS, Marzan-Rivera N, Watowich MM, Valle ADN-D, Pantoja P, Pavez-Fox MA, Siracusa ER, Cooper EB, Valle JEN-D, Phillips D, et al (2023). Immune cell composition varies by age, sex and exposure to social adversity in free-ranging Rhesus Macaques. GeroScience
Sanchez Rosado MR, Newman L, Watowich M, Pavez-Fox M, Valle JN-D, Phillips D, Skelton M, Siracusa E, Higham J, Brent L, et al (2023). Social Status is Associated with Impaired Anti-Inflammatory Response in Free-Ranging Male Rhesus Macaques. The Journal of Immunology, 210(1_Supplement), 248.13-248.13.
Pavez-Fox MA, De Moor D, Siracusa ER, Ellis S, Kimock CM, Rivera-Barreto N, Valle JEN-D, Phillips D, Ruiz-Lambides A, Snyder-Mackler N, et al (2023). Socioecological drivers of injuries in female and male rhesus macaques (Macaca mulatta).
2022
Siracusa ER, Pereira AS, Brask JB, Negron-Del Valle JE, Phillips D, Platt ML, Higham JP, Snyder-Mackler N, Brent LJN (2022). Ageing in a collective: the impact of ageing individuals on social network structure.
Abstract:
Ageing in a collective: the impact of ageing individuals on social network structure
AbstractAgeing affects many phenotypic traits, but its consequences for social behaviour have only recently become apparent. Social networks emerge from associations between individuals. The changes in sociality that occur as individuals get older are thus likely to impact network structure, yet this remains unstudied. Here we use empirical data from free-ranging rhesus macaques and an agent-based model to test how age-based changes in social behaviour feed up to influence: (1) an individual’s level of indirect connectedness in their network; and (2) overall patterns of network structure. Our empirical analyses revealed that female macaques became less indirectly connected as they aged for some, but not all network measures examined, suggesting that indirect connectivity is affected by ageing, and that ageing animals can remain well integrated in some social contexts. Surprisingly, we did not find evidence for a relationship between age distribution and the structure of female macaque networks. We used an agent-based model to gain further understanding of the link between age-based differences in sociality and global network structure, and under which circumstances global effects may be detectable. Overall, our results suggest a potentially important and underappreciated role of age in the structure and function of animal collectives, which warrants further investigation.
Abstract.
Martinig AR, Karst HJ, Siracusa ER, Studd EK, McAdam AG, Dantzer B, Delaney DM, Lane JE, Pokharel P, Boutin S, et al (2022). Animal personality: a comparison of standardized assays and focal observations in North American red squirrels. Animal Behaviour, 190, 221-232.
Pavez-Fox MA, Kimock CM, Rivera-Barreto N, Valle JEN-D, Phillips D, Ruiz-Lambides A, Snyder-Mackler N, Higham JP, Siracusa ER, Brent LJN, et al (2022). Reduced injury risk links sociality to survival in a group-living primate.
Pavez-Fox MA, Kimock CM, Rivera-Barreto N, Negron-Del Valle JE, Phillips D, Ruiz-Lambides A, Snyder-Mackler N, Higham JP, Siracusa ER, Brent LJN, et al (2022). Reduced injury risk links sociality to survival in a group-living primate. iScience, 25(11), 105454-105454.
Siracusa ER, Higham JP, Snyder-Mackler N, Brent LJN (2022). Social ageing: exploring the drivers of late-life changes in social behaviour in mammals.
Biology Letters,
18(3).
Abstract:
Social ageing: exploring the drivers of late-life changes in social behaviour in mammals
Social interactions help group-living organisms cope with socio-environmental challenges and are central to survival and reproductive success. Recent research has shown that social behaviour and relationships can change across the lifespan, a phenomenon referred to as ‘social ageing’. Given the importance of social integration for health and well-being, age-dependent changes in social behaviour can modulate how fitness changes with age and may be an important source of unexplained variation in individual patterns of senescence. However, integrating social behaviour into ageing research requires a deeper understanding of the causes and consequences of age-based changes in social behaviour. Here, we provide an overview of the drivers of late-life changes in sociality. We suggest that explanations for social ageing can be categorized into three groups: changes in sociality that (a) occur as a result of senescence; (b) result from adaptations to ameliorate the negative effects of senescence; and/or (c) result from positive effects of age and demographic changes. Quantifying the relative contribution of these processes to late-life changes in sociality will allow us to move towards a more holistic understanding of how and why these patterns emerge and will provide important insights into the potential for social ageing to delay or accelerate other patterns of senescence.
Abstract.
Siracusa ER (2022). Social senescence in red deer.
Nat Ecol Evol,
6(8), 1062-1063.
Author URL.
Siracusa ER, Valle JEN-D, Phillips D, Platt ML, Higham JP, Snyder-Mackler N, Brent LJN (2022). Within-individual changes reveal increasing social selectivity with age in rhesus macaques.
Siracusa ER, Negron-Del Valle JE, Phillips D, Platt ML, Higham JP, Snyder-Mackler N, Brent LJN (2022). Within-individual changes reveal increasing social selectivity with age in rhesus macaques.
Proceedings of the National Academy of Sciences,
119(49).
Abstract:
Within-individual changes reveal increasing social selectivity with age in rhesus macaques
Accumulating evidence in humans and other mammals suggests older individuals tend to have smaller social networks. Uncovering the cause of these declines can inform how changes in social relationships with age affect health and fitness in later life. While age-based declines in social networks have been thought to be detrimental, physical and physiological limitations associated with age may lead older individuals to adjust their social behavior and be more selective in partner choice. Greater selectivity with age has been shown in humans, but the extent to which this phenomenon occurs across the animal kingdom remains an open question. Using longitudinal data from a population of rhesus macaques on Cayo Santiago, we provide compelling evidence in a nonhuman animal for within-individual increases in social selectivity with age. Our analyses revealed that adult female macaques actively reduced the size of their networks as they aged and focused on partners previously linked to fitness benefits, including kin and partners to whom they were strongly and consistently connected earlier in life. Females spent similar amounts of time socializing as they aged, suggesting that network shrinkage does not result from lack of motivation or ability to engage, nor was this narrowing driven by the deaths of social partners. Furthermore, females remained attractive companions and were not isolated by withdrawal of social partners. Taken together, our results provide rare empirical evidence for social selectivity in nonhumans, suggesting that patterns of increasing selectivity with age may be deeply rooted in primate evolution.
Abstract.
2021
Rosado MRS, Marzan-Rivera N, Watowich MM, Valle ADN-D, Pantoja P, Pavez-Fox MA, Siracusa ER, Cooper EB, Valle JEN-D, Phillips D, et al (2021). Age, sex, and social environmental effects on immune cell composition in a free-ranging non-human primate.
Fisher DN, Kilgour RJ, Siracusa ER, Foote JR, Hobson EA, Montiglio P, Saltz JB, Wey TW, Wice EW (2021). Anticipated effects of abiotic environmental change on intraspecific social interactions.
Biological Reviews,
96(6), 2661-2693.
Abstract:
Anticipated effects of abiotic environmental change on intraspecific social interactions
ABSTRACTSocial interactions are ubiquitous across the animal kingdom. A variety of ecological and evolutionary processes are dependent on social interactions, such as movement, disease spread, information transmission, and density‐dependent reproduction and survival. Social interactions, like any behaviour, are context dependent, varying with environmental conditions. Currently, environments are changing rapidly across multiple dimensions, becoming warmer and more variable, while habitats are increasingly fragmented and contaminated with pollutants. Social interactions are expected to change in response to these stressors and to continue to change into the future. However, a comprehensive understanding of the form and magnitude of the effects of these environmental changes on social interactions is currently lacking. Focusing on four major forms of rapid environmental change currently occurring, we review how these changing environmental gradients are expected to have immediate effects on social interactions such as communication, agonistic behaviours, and group formation, which will thereby induce changes in social organisation including mating systems, dominance hierarchies, and collective behaviour. Our review covers intraspecific variation in social interactions across environments, including studies in both the wild and in laboratory settings, and across a range of taxa. The expected responses of social behaviour to environmental change are diverse, but we identify several general themes. First, very dry, variable, fragmented, or polluted environments are likely to destabilise existing social systems. This occurs as these conditions limit the energy available for complex social interactions and affect dissimilar phenotypes differently. Second, a given environmental change can lead to opposite responses in social behaviour, and the direction of the response often hinges on the natural history of the organism in question. Third, our review highlights the fact that changes in environmental factors are not occurring in isolation: multiple factors are changing simultaneously, which may have antagonistic or synergistic effects, and more work should be done to understand these combined effects. We close by identifying methodological and analytical techniques that might help to study the response of social interactions to changing environments, highlight consistent patterns among taxa, and predict subsequent evolutionary change. We expect that the changes in social interactions that we document here will have consequences for individuals, groups, and for the ecology and evolution of populations, and therefore warrant a central place in the study of animal populations, particularly in an era of rapid environmental change.
Abstract.
Siracusa ER, Boutin S, Dantzer B, Lane JE, Coltman DW, McAdam AG (2021). Familiar Neighbors, but Not Relatives, Enhance Fitness in a Territorial Mammal. Current Biology, 31(2), 438-445.e3.
2020
Studd EK, Menzies AK, Siracusa ER, Dantzer B, Lane JE, McAdam AG, Boutin S, Humphries MM (2020). Optimisation of energetic and reproductive gains explains behavioural responses to environmental variation across seasons and years.
Ecology Letters,
23(5), 841-850.
Abstract:
Optimisation of energetic and reproductive gains explains behavioural responses to environmental variation across seasons and years
AbstractAnimals switch between inactive and active states, simultaneously impacting their energy intake, energy expenditure and predation risk, and collectively defining how they engage with environmental variation and trophic interactions. We assess daily activity responses to long‐term variation in temperature, resources and mating opportunities to examine whether individuals choose to be active or inactive according to an optimisation of the relative energetic and reproductive gains each state offers. We show that this simplified behavioural decision approach predicts most activity variation (R2 = 0.83) expressed by free‐ranging red squirrels over 4 years, as quantified through accelerometer recordings (489 deployments; 5066 squirrel‐days). Recognising activity as a determinant of energetic status, the predictability of activity variation aggregated at a daily scale, and the clear signal that behaviour is environmentally forced through optimisation of gain, provides an integrated approach to examine behavioural variation as an intermediary between environmental variation and energetic, life‐history and ecological outcomes.
Abstract.
2019
Siracusa ER, Boutin S, Dantzer B, Lane JE, Coltman DW, McAdam AG (2019). Familiar neighbours, but not relatives, enhance fitness in a territorial mammal.
Abstract:
Familiar neighbours, but not relatives, enhance fitness in a territorial mammal
SummaryOne of the outstanding questions in evolutionary biology is the extent to which mutually beneficial interactions and kin-selection can facilitate the evolution of cooperation by mitigating conflict between interacting organisms. The indirect fitness benefits gained from associating with kin are an important pathway to conflict resolution [1], but conflict can also be resolved if individuals gain direct benefits from cooperating with one another (e.g. mutualism or reciprocity) [2]. Owing to the kin-structured nature of many animal societies, it has been difficult for previous research to assess the relative importance of these mechanisms [3–5]. However, one area that might allow for the relative roles of kin-selection and mutualistic benefits to be disentangled is in the resolution of conflict over territorial space [6]. While much research has focused on group-living species, the question of how cooperation can first be favoured in solitary, territorial species remains a key question. Using 22 years of data from a population of North American red squirrels, we assessed how kinship and familiarity with neighbours affected fitness in a territorial mammal. While living near kin did not enhance fitness, familiarity with neighbours increased survival and annual reproductive success. These fitness benefits were strong enough to compensate for the effects of aging later in life, with potential consequences for the evolution of senescence. We suggest that such substantial fitness benefits provide the opportunity for the evolution of cooperation between adversarial neighbours, offering insight into the role that mutually beneficial behaviours might play in facilitating and stabilizing social systems.Graphical Abstract
Abstract.
Siracusa ER, Wilson DR, Studd EK, Boutin S, Humphries MM, Dantzer B, Lane JE, McAdam AG (2019). North American red squirrels mitigate costs of territory defence through social plasticity. Animal Behaviour, 151, 29-42.
2018
Siracusa E, Morandini M, Boutin S, Humphries MM, Dantzer B, Lane J, McAdam AG (2018). Red squirrel territorial vocalizations deter intrusions by conspecific rivals.
Siracusa ER, Wilson DR, Studd EK, Boutin S, Humphries MM, Dantzer B, Lane JE, McAdam AG (2018). Red squirrels mitigate costs of territory defence through social plasticity.
2017
Siracusa E, Boutin S, Humphries MM, Gorrell JC, Coltman DW, Dantzer B, Lane JE, McAdam AG (2017). Familiarity with neighbours affects intrusion risk in territorial red squirrels.
Animal Behaviour,
133, 11-20.
Abstract:
Familiarity with neighbours affects intrusion risk in territorial red squirrels
Interactions with conspecifics are an important aspect of an individual's environment. Although it is well known that the presence of conspecifics can have important effects on behaviour, in general it is also now acknowledged that the composition of the social environment can vary, and that this variation may have profound effects on individual behaviour and fitness. Using a wild population of North American red squirrels, Tamiasciurus hudsonicus, we investigated the importance of the composition of the social environment in a territorial species by assessing whether the risk of intrusion faced by territory owners varied with the degree of relatedness and familiarity in their social neighbourhoods. To test this, we conducted temporary removals of territory owners and observed the time until intrusion and the identity of intruding individuals. We found that individuals in neighbourhoods with low average familiarity faced a higher risk of intrusion and that unfamiliar neighbours were more likely to intrude. Surprisingly, we found that related neighbours also posed a higher risk of intrusion. The results from our study suggest that familiarity with neighbours may be an ecologically and evolutionarily relevant measure of the social environment, even in a species considered to be ‘asocial’. Future studies should consider the potential importance of the social environment, which has heretofore been mostly overlooked, as a relevant selective pressure in asocial, territorial species.
Abstract.
Siracusa E, Morandini M, Boutin S, Humphries MM, Dantzer B, Lane JE, McAdam AG (2017). Red squirrel territorial vocalizations deter intrusions by conspecific rivals.
Behaviour,
154(13-15), 1259-1273.
Abstract:
Red squirrel territorial vocalizations deter intrusions by conspecific rivals
In many species, territory advertisement is thought to be one of the primary functions of acoustic communication. North American red squirrels are a territorial species in which 'rattles' have long been thought to be the principal signal communicating territory ownership. These vocalizations have been assumed to deter intruders, thus reducing energetic costs and the risk of injury associated with direct aggressive interactions. However, this hypothesis has not been directly tested. Here we used a speaker occupation experiment to test whether red squirrel rattles function to deter conspecific rivals. We studied 29 male squirrels and removed each individual from his territory twice in a paired design. During the experimental treatment, we simulated the owner's presence after its removal by broadcasting the owner's rattle from a loudspeaker at the centre of the territory once every 7 min. During the control treatment, the territory was left in silence following the temporary removal of the owner. We found that the presence of a speaker replacement reduced the probability of intrusion by 34% and increased the latency to first intrusion by 7%, providing support for the hypothesis that rattles play an active role in reducing intrusion risk. However, intrusions were not completely averted by the speaker replacement, indicating that for some individuals vocalizations alone are not a sufficient deterrent without other cues of the territory owner.
Abstract.