Red squirrels use territorial vocalizations for kin discrimination

doi:10.1016/j.anbehav.2015.06.011

Animal Behaviour

Volume 107, September 2015, Pages 79-85

https://doi.org/10.1016/j.anbehav.2015.06.011 Get rights and content

Highlights

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Red squirrels use rattle vocalizations during territory defence.
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Rattle acoustic structure is repeatable, suggesting rattles are individually distinctive.
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Squirrels do not respond differently to the rattles of neighbours and non-neighbours.
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Squirrels rattle more frequently in response to the rattles of nonkin versus kin.
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Red squirrels use individually distinctive rattles to discriminate kin from nonkin.

The ability to discriminate among individuals, or among classes of individuals, can provide animals with important fitness benefits. Although several mechanisms for discrimination are possible, most require animals to show stable phenotypic variation that reflects their identity or their membership in a particular class (e.g. sex, mate, kin). For territorial animals that rarely interact physically, vocalizations could serve as long-distance signals that facilitate discrimination. In this study, we tested whether the territorial rattle vocalizations of North American red squirrels, Tamiasciurus hudsonicus, are repeatable, and whether they could hence provide the basis for multiple types of discrimination. We measured four structural features from two rattles from each of 76 marked squirrels. All four features were repeatable, which is consistent with territorial rattles being individually distinctive. We then conducted a playback experiment to determine whether squirrels use rattles for discrimination. Specifically, we tested whether squirrels discriminate between the rattles of neighbours and non-neighbours, and kin (coefficient of relatedness, r ≥ 0.25) and non-kin (r < 0.125). Following a 2 × 2 factorial design, we broadcast a rattle from a non-neighbouring nonkin individual to 15 subjects, from a neighbouring nonkin individual to 14 subjects, from a non-neighbouring kin individual to 11 subjects, and from a neighbouring kin individual to 13 subjects. Subjects did not discriminate between the rattles of neighbours and non-neighbours, but did respond differently to the rattles of kin and nonkin. Specifically, squirrels were significantly more likely to produce a rattle of their own in response to the broadcasted rattles of nonkin versus the broadcasted rattles of kin. This result demonstrates that red squirrels can use territorial vocalizations for kin discrimination. It also suggests that they are more tolerant of territorial intrusions by kin.

Section snippets

Subjects

Subjects were derived from a marked population of North American red squirrels (T. hudsonicus; Erxleben, 1777) that has been studied annually in the southwest Yukon Territory of Canada (61°N, 138°W) since 1989 (McAdam, Boutin, Sykes, & Humphries, 2007). All individuals in the population were marked with numbered metal eartags when first captured (usually just after birth when in the natal nest) and were then live-trapped each year throughout their lifetime. We also attached a unique combination

Acoustic Analysis

We recorded one unsolicited territorial rattle from each of 172 individually marked red squirrels. Rattles had an average ± SD duration of 3.0 ± 1.4 s (range 0.4–10.0 s), an average call rate of 19.1 ± 2.0 pulses/s (range 12.6–25.2 pulses/s), an average dominant frequency of 1124 ± 152 Hz (range 770–1460 Hz) and an average entropy of 6.5 ± 0.3 bits (range 5.6–7.1 bits). None of the acoustic features differed significantly between females and males (unpaired t tests: all |t₁₇₁| < 1.64, all P ≥ 0.10), between adults

Discussion

Red squirrels produced territorial vocalizations with repeatable acoustic structure, and they used these vocalizations to discriminate between kin and nonkin. We found no evidence that squirrels use rattles to discriminate between neighbours and non-neighbours.

Our acoustic analysis showed that red squirrels produce territorial rattles that reflect the signaller's identity. The ICCs of the four structural features that we measured were each significantly greater than zero, which is consistent

Acknowledgments

We thank the many field technicians who helped collect the data, A. Sykes and E. Anderson who served as head technicians during the duration of the study, Agnes Moose and her family for long-term access to her trapline, and J. Slate and M. R. Gunn who helped to develop the paternal pedigree. The McAdam lab group and two anonymous referees provided helpful comments on an earlier version of the manuscript. This is paper number 81 in the Kluane Red Squirrel Project. This project was supported by

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Furthermore, preplayback rattle rates in our current study were noticeably higher than those previously reported in both Wilson et al. (2015) and Shonfield et al. (2017). The exact reason for the discrepancies seen between the results of Wilson et al. (2015), Shonfield et al. (2017) and our study is unknown. Statistical power cannot account for these discrepancies, as the patterns we observed relating to playback context and relatedness were in the opposite direction of those observed by Shonfield et al. (2017).
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Red squirrels are arboreal rodents in which both sexes defend exclusive territories year-round.15 Territories are important for overwinter survival16 and are defended through vocalizations called “rattles”17, which are uniquely identifiable.18 Juveniles typically disperse 100 m on average and females sometimes bequeath all or part of their territory to offspring.19
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For territorial species, the ability to be behaviourally plastic in response to changes in their social environment may be beneficial by allowing individuals to mitigate conflict with conspecifics and reduce the costs of territoriality. Here we investigated whether North American red squirrels, Tamiasciurus hudsonicus, are able to minimize costs of territory defence by adjusting behaviour in response to the familiarity of neighbouring conspecifics. Since red squirrels living in familiar neighbourhoods face reduced intrusion risk, we predicted that increasing familiarity among territorial neighbours would allow squirrels to spend less time on territorial defence and more time in the nest. Longitudinal behavioural data (1995–2004) collected from the same squirrels across several different social environments indicated that red squirrels reduced rates of territorial vocalizations and increased nest use in response to increasing familiarity with neighbours. In contrast, cross-sectional data (2015–2016), which provided observations from each individual in a single social environment, did not provide evidence of this plasticity. Post hoc analyses revealed that evidence of social plasticity in this system is primarily due to within-individual changes in behaviour, which we were unable to estimate in the cross-sectional data. Our results demonstrate that red squirrels respond to changes in their social environment by adjusting their behaviour in a manner that reduces the costs of territoriality. However, our results also suggest that estimating plasticity by comparing behaviour among individuals (i.e. cross-sectional analyses) may not always be reliable. Our ability to detect these effects may therefore depend on having data with multiple observations from the same individuals across different social environments.
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Because the Sciuridae family frequently uses acoustic communication, they are suitable for studying the diversity of sound characteristics. Sciurids produce sounds in various situations, such as predator alerts (e.g., Balph and Balph, 1966; Sherman, 1977; Owings and Leger, 1980; Blumstein and Armitage, 1997); territory defense (e.g., Lair, 1990; Digweed et al., 2012; Wilson et al., 2015); mother-infant interactions (e.g., Emmons, 1978, Lishak, 1982; Tamura and Ohba, 1993) and mating activities (e.g., Farentinos, 1972; Thompson, 1977; Grady and Hoogland, 1986; Tamura, 1993). Both inter-specific and inter-population differences in acoustic characteristics have been reported in various genera of squirrels, including Cynomys (Waring, 1970), Spermophilus (Fagerstone, 1987; Eiler and Banack, 2004), Tamias (Brand, 1976; Blankenship and Brand, 1987), Tamiasciurus (Smith, 1978), Paraxerus (Viljoen, 1983), Callosciurus (Tamura and Yong, 1993) and Glaucomys (Eisinger et al., 2016).
Vocal communication plays an important role in the mating behaviour of arboreal squirrels. Callosciurus is a genus of tree squirrels that includes 15 species distributed in Southeast Asia, and congeneric species often inhabit the same forest. As closely related species of Callosciurus have the potential to interbreed, species recognition from mating calls may be a fundamental reproductive barrier. We compared seven acoustic characteristics of male mating calls in six Callosciurus species and estimated whether the species differences were clear enough to function as a cue. Discriminant function analyses (DFA) classified 87.4% of mating calls to the correct species. All of the calls by C. notatus, C. nigrovittatus and C. caniceps, and 88% of the calls by C. prevostii, were assigned to the correct species, while the percentage of correct classifications was lower in C. finlaysonii (71%) and C. erythraeus (63%). We compared these results with the genetic relationships to determine whether interspecific acoustic differences are caused by adaptive selection (habitat selection and body size) or by a stochastic process (drift). The genetic relationships among the six species were coincident with the differences in mating calls, which supports the stochastic divergence. Species-specific mating calls may be a useful cue for species recognition in Callosciurus, and thus these calls could be an effective trait for phylogenetic analysis in Callosciurus.

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View full text

Red squirrels use territorial vocalizations for kin discrimination

Highlights

Section snippets

Subjects

Acoustic Analysis

Discussion

Acknowledgments

Animal Behaviour

Journal of Theoretical Biology

Trends in Ecology & Evolution

Animal Behaviour

Animal Behaviour

Animal Behaviour

Trends in Ecology & Evolution

Animal Behaviour

Animal Behaviour

Trends in Ecology & Evolution

Breeding dispersal in female North American red squirrels

Ecology

Kin recognition mechanisms: phenotype matching or recognition alleles?

American Naturalist

Social sounds: vocal learning and development of mammal and bird calls

Behavioral responses of territorial red squirrels to natural and experimental variation in population density

Behavioral Ecology and Sociobiology

Who's your neighbour? Acoustic cues to individual identity in red squirrel Tamiasciurus hudsonicus rattle calls

Current Zoology

Intraspecific cache pilferage by larder-hoarding red squirrels (Tamiasciurus hudsonicus)

Journal of Mammalogy

Evolution and bird sociality

Food pilfering in larder-hoarding red squirrels (Tamiasciurus hudsonicus)

Journal of Mammalogy

Adopting kin enhances inclusive fitness in asocial red squirrels

Nature Communications