2024

Individual behavioral variation does not affect social organization or reproductive success in a cooperative small mammal

van der Marel A, Johnson NE, Grillo S, Riquelme J, Vásquez RA, Gilliam EH, Ebensperger LA, Hayes LD. 

Accepted in Behaviour. 

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We studied the common degu, Octodon degus, a social rodent, to evaluate whether individual behavioral variation (personality) underlies social organization and the reproductive success of individuals within groups. We examined social groups in a population in central-north Chile during one breeding season, tested 67 adults in an open field test (i.e., the propensity to explore an unfamiliar environment) and 62 adults in a poke test (i.e., the propensity to charge an object) to quantify individual behavioral variation, determined assortment based on individual behavioral differences across 19 social groups, and performed genetic analyses to assess reproductive success. We found that the response to the poke test was repeatable, while none of the behaviors from an open field test were. The repeatable behavior during the poke test was not associated with components of social organization (group composition), or reproductive success. These findings imply that individual behavioral variation did not affect grouping patterns or direct fitness in this degu population. 

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2023    

Size is not everything: Nuanced effects of female multiple mating and annual litter number on testes size in terrestrial mammal

van der Marel A, Warrington MH, Waterman JM. 2023

Journal of Zoology DOI

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We examined the relationship between testes size and mating systems, litter size, and litter rate while considering male lifespan and investment in paternal care in 224 terrestrial mammalian species in 15 orders. Relative testes size was larger in species where females mated with multiple males. Furthermore, in species with multiple-mating females, species with higher litter rates had larger testes compared to species with fewer litters per year while in monogamous species we found the opposite pattern. Neither longevity nor paternal care influenced testes size. Our results elucidate the effect of female reproductive strategies on relative testes size is nuanced and varies between mating systems, suggesting that the interplay between male and female reproductive investment may be different within similar social mating systems.

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Perturbations highlight importance of social history in parakeet rank dynamics

van der Marel A, Francis X, O’Connell CL, Estien C, Carminito CE, Kluever BM, Hobson EA. 2023

Behavioral Ecology 34(3):457–467. DOI - published data and code.

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           Dominance rank can influence many aspects of an individual’s biology across many species. We manipulated 

group membership to determine whether rank is the product of a group’s social history or bodyweight in monk parakeets. After reintroducing removed individuals, no top-ranked individuals could re-take their rank, and bodyweight was inconsistently correlated with rank across all birds. Our results show that rank is more likely an outcome of social history rather than being driven by individual characteristics.

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2022

Preprint: Perturbations of key individuals trigger shifts in group-level dominance patterns

van der Marel A, Francis X, O’Connell CL, Estien C, Carminito CE, Hobson EA. 2022

EcoEvoRxiv July 20. DOI  

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Dominance hierarchies direct and structure aggression in many species. Recent computational approaches detected aggression patterns within dominance hierarchies based on relative rank differences between individuals. Within species, groups can follow different dominance patterns, indicating that these patterns are not species-specific, but rather group-specific characteristics. We used perturbation experiments in monk parakeets to study how and why a particular social dominance pattern emerges within a group or if intragroup variation in patterns exists. Perturbation experiments assessed the impact of key individuals on group-level aggression and identified conditions associated with shifts in the group’s social dominance pattern. Understanding the conditions under which a group may shift patterns provides insight into group-level behavioral plasticity.

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Playback experiments elicit temporary group repulsion, not attraction, in a globally distributed pest parrot

Estien C, O’Connell CL, Francis X, Smith-Vidaurre G, Kluever BM, Hobson EA, van der Marel A. 2022

Animal Behavior and Cognition, 9(4):363-384. DOI

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We conducted playback experiments with a captive population of monk parakeets to evaluate auditory cues that may be useful for designing management protocols. Our experiment evaluated the efficacy of two stimuli that we expected to either repulse or attract parakeets: predator vocalizations and conspecific vocalizations, respectively. In the repulsion playbacks, monk parakeets were repelled by predator vocalizations in 80% of trials and took longer to cease vigilance and return to baseline behavior compared to attraction playbacks. In the attraction playbacks, monk parakeets exhibited vigilant behavior and weak or no attraction to the stimulus, with attraction only being observed in 10% of trials. Our results demonstrate that predator playbacks may be particularly useful for completing management objectives, such as temporary removal from a location.

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A comparison of low-cost behavioral observation software applications for handheld computers and recommendations for use

van der Marel A, O'Connell CL, Prasher S, Carminito C, Francis X, Hobson EA. 2022

Ethology 128:275-284. DOI

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In the field of animal behavior and behavioral ecology, many standardized methods to observe animal behavior were established in the last decades. While the protocols remained similar, behavioral researchers can take advantage of technological advancements to enter observations directly onto a handheld computer (phone, tablet, etc.), saving time and potentially increasing fidelity of recordings. However, we now have the choice between many different platforms for recording behavioral observations. Our challenge is choosing the most appropriate platform that fits a particular study question, research design, budget, and desired amount of preparatory time. Here, we review six low-cost software applications for handheld computers that are available for real-time entry of behavioral observations: Animal Behaviour Pro, Animal Observer, BORIS, CyberTracker, Prim8, and ZooMonitor. Our goal is to help researchers make calculated decisions about what behavioral observation platform is best for their study system and question.

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2021

Barbary ground squirrels do not have a sentinel system but instead synchronise vigilance                

van der Marel A, Waterman JM, López-Darias M. 2021 

Behavioral Ecology and Sociobiology 75:153, DOI - published data and code

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Animals must balance eating and avoid being eaten. Species can reduce the cost of this trade-off – increased predation risk and reduced foraging – by performing low-quality vigilance (foraging and vigilant at the same time) instead of high-quality vigilance (completely focused on vigilance), by synchronizing vigilance or taking turns acting as sentinels. Invasive Barbary ground squirrels may synchronize their vigilance 1) to perform an optimal activity when satiated, and, 2) to watch each other’s back.

 

Exploring the role of life history traits and introduction effort in understanding invasion success in mammals: A case study of Barbary ground squirrels

van der Marel AM, Waterman JM, López-Darias M. 2021

Oecologia 195:327-339. DOI - Published data and code

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Introduction effort (i.e., number of founders and times introduced) is one of the main factors that explain invasion success. Although life history traits are also associated with invasion success, where a fast life history (large and frequent litters, small body size, short lifespan) favors invasion success in mammals. We first investigated life history traits of the Barbary ground squirrel, Atlantoxerus getulus, a species with a very low introduction effort, and studied whether their exceptional invasion success is due to a very fast life history profile through a comparison of these traits to other successful mammal invaders. We then examined whether number of founders and/or a fast life history influences invasion success of squirrels. We found that Barbary ground squirrels were on the fast end of the “fast-slow continuum”, but their life history is not the only contributing factor to their invasion success, as the life history profile is comparable to other invasive species that do not have such a low introduction effort. We also found that neither life history traits nor number of founders explained invasion success of introduced squirrels in general. These results contradict the concept that introduction effort is the main factor explaining invasion success, especially in squirrels. Instead, we argue that invasion success can be influenced by multiple aspects of the new habitat or the biology of the introduced species.      

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2020

Preprint: Evidence for an extreme founding effect in a highly successful invasive species

Kratzer K, van der Marel A, Garroway C, López-Darias M, Petersen SD, Waterman JM. 2020

bioRxiv 2020.08.04 DOI 

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The adaptive potential of invasive species is thought to decrease during founding events due to reduced genetic diversity, limiting the new population’s ability to colonize novel habitats. Barbary ground squirrels (Atlantoxerus getulus) were purportedly introduced as a single breeding pair to the island of Fuerteventura but have expanded to over a million individuals spread across the island in just over 50 years. Our results suggest that A. getulus has undergone an intense genetic bottleneck during their colonization of the island as they have a small effective population size, low levels of heterozygosity, and high levels of inbreeding, supporting a founding population size of two to three individuals. They are one of the few species where introduction effort does not explain invasion success, although further investigation may explain how they have avoided the worst expected effects following an extreme genetic bottleneck.

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A framework to evaluate whether to pool or separate behaviors in a multilayer network

van der Marel A, Prasher S, Carminito C, O'Connell C, Phillips A, Kluever BM, Hobson EA. 2020

Current Zoology 67(1):101–111. DOI - Published data and code

       

As behavioral ecologists, we often collect data on multiple behaviors. These behaviors may be variations that occur within the same social context, like multiple types of aggression or affiliation. We do not currently have a  framework for evaluating the implications of deciding whether to keep these behaviors separate or pooling them together. We propose a data-driven approach that allows researchers to follow 3 questions to evaluate whether the combined evidence supports pooling behaviors before performing other analyses.

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Social organization in a North African ground squirrel

van der Marel A, Waterman JM, López-Darias M. 2020 

Journal of Mammalogy 101(3):670–683. DOI

 

Patterns of group living are often explained through kinship, but such a pattern is not necessarily universal because unrelated individuals may be social due to other benefits. In Barbary ground squirrels Atlantoxerus getulus, adult females primarily live with related females, while males live in groups with unrelated adult males and subadults of either sex. Thus, females live with family and males live with friends. These results suggest that kinship is not the only determinant for cooperation in this species. Barbary ground squirrels’ social organization resembles that of the closely related Cape ground squirrel rather than that of the temperate ground-dwelling sciurids, which have seasonal breeding in common with Barbary ground squirrels. In addition to describing the social organization of a previously unstudied species, this paper sheds light on the ecological drivers of sociality, and the evolution of distinct social organizations in ground-dwelling sciurids.

 

2019

Group-enhanced predator detection and quality of vigilance in a social ground squirrel  

van der Marel AM, López-Darias M, Waterman JM. 2019

Animal Behaviour 151:43–52. DOI

 

• Collective high-quality vigilance increased with larger group size.

• Individual low- and high-quality vigilance did not decrease as group size increased.

• Repeated alarm calls communicate a terrestrial threat to group members.

• Collective detection is one of the grouping benefits in Barbary ground squirrels.

 

2018

Unraveling behavioral and pace-of-life syndromes in a reduced parasite and predation pressure context: personality and survival of the Barbary ground squirrel

Piquet JC, López-Darias M, van der Marel A, Nogales M, Waterman J. 2018

Behavioural Ecology and Sociobiology 72:147. DOI

 

Research on the interactions of animal personality with other ecological and evolutionary factors, such as parasitism and selection gradients, has yielded some intriguing perspectives about many ecological and evolutionary processes. However, our understanding of the eco-evolutionary consequences of animal personality and how it interacts with other relevant biological processes is still limited. Invasive species often experience specific ecological conditions that can allow testing of the general assumptions related to animal personality. The present contribution explores if and how personality traits are related to key ecological and evolutionary factors, such as parasitism and survival, in the context of an invasive population subjected to reduced parasite and predation pressure. Unlike other studies conducted under different ecological contexts, our results suggest Barbary ground squirrels from the assessed population with fast pace-of-life syndromes have higher survival chances than their counterparts.

 

2014

Personality drives physiological adjustments and is not related to survival

Bijleveld AI, Massourakis G, van der Marel A, Dekinga A, Spaans B, van Gils JA, Piersma T. 2014

Proceedings of the Royal Society B 281:20133135. DOI

 

The evolutionary function and maintenance of variation in animal personality is still under debate. Variation in the size of metabolic organs has recently been suggested to cause and maintain variation in personality. Here, we examine two main underlying notions: (i) that organ sizes vary consistently between individuals and cause consistent behavioural patterns, and (ii) that a more exploratory personality is associated with reduced survival. Exploratory behaviour of captive red knots (Calidris canutus, a migrant shorebird) was negatively rather than positively correlated with digestive organ (gizzard) mass, as well as with body mass. In an experiment, we reciprocally reduced and increased individual gizzard masses and found that exploration scores were unaffected. Whether or not these birds were resighted locally over the 19 months after release was negatively correlated with their exploration scores. Moreover, a long-term mark–recapture effort on free-living red knots with known gizzard masses at capture confirmed that local resighting probability (an inverse measure of exploratory behaviour) was correlated with gizzard mass without detrimental effects on survival. We conclude that personality drives physiological adjustments, rather than the other way around, and suggest that physiological adjustments mitigate the survival costs of exploratory behaviour. Our results show that we need to reconsider hypotheses explaining personality variation based on organ sizes and differential survival.