Living on the edge: morphological and behavioral adaptations to a marginal high-elevation habitat in an arboreal mammal.

Sciurus vulgaris behavioral plasticity marginal edge-habitat morphology personality

Journal

Integrative zoology
ISSN: 1749-4877
Titre abrégé: Integr Zool
Pays: Australia
ID NLM: 101492420

Informations de publication

Date de publication:
Jul 2023
Historique:
medline: 4 7 2023
pubmed: 3 9 2022
entrez: 2 9 2022
Statut: ppublish

Résumé

Habitats are characterized by different local environmental conditions that influence both behavior and morphology of species, which can result in habitat-dependent phenotypic differences among animals living in heterogeneous environments. We studied 3 alpine populations of Eurasian red squirrels (Sciurus vulgaris), 1 living in a marginal high-elevation habitat at the edge of the species' altitudinal distribution, and 2 occurring in higher-quality habitats. Here, we investigated whether squirrels living in the marginal area differed in 2 morphological parameters (body size and body mass) and/or in the expression of 4 personality traits estimated with an open field test and a mirror image stimulation test (activity, exploration, activity-exploration, and social tendency). Furthermore, we tested whether within-individual variance of the traits (behavioral plasticity) was higher in the edge habitat. Male squirrels in the edge habitat were smaller and weighed less than in the other study areas, while among females, size-habitat relationships were less marked. These sex-specific patterns were explained by a strong association between body mass and reproductive success in female squirrels. Squirrels in the marginal habitat were more active, explorative, and had a more social personality than in the other habitats. However, in contrast to our predictions, behavioral plasticity was smaller in the marginal habitat, but only for the trait exploration. Our results suggest that animals choose the habitat that best fits their personality, and that habitat-related differences in selective pressures may shape animals' morphology.

Identifiants

pubmed: 36052941
doi: 10.1111/1749-4877.12679
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

746-761

Informations de copyright

© 2022 The Authors. Integrative Zoology published by International Society of Zoological Sciences, Institute of Zoology/Chinese Academy of Sciences and John Wiley & Sons Australia, Ltd.

Références

Beaman JE, White CR, Seebacher F (2016). Evolution of plasticity: Mechanistic link between development and reversible acclimation. Trends in Ecology & Evolution 31, 237-49.
Bell AM, Hankison SJ, Laskowski KL (2009). The repeatability of behaviour: A meta-analysis. Animal Behaviour 77, 771-83.
Biro PA, Stamps JA (2008). Are animal personality traits linked to life-history productivity? Trends in Ecology & Evolution 23, 361-8.
Bolnick DI, Svanbäck R, Fordyce JA et al. (2003). The ecology of individuals: Incidence and implications of individual specialization. The American Naturalist 161, 1-28.
Boon AK, Réale D, Boutin S (2008). Personality, habitat use, and their consequences for survival in North American red squirrels Tamiasciurus hudsonicus. Oikos 117, 1321-8.
Boone SR, Brehm AM, Mortelliti A (2022). Seed predation and dispersal by small mammals in a landscape of fear: effects of personality, predation risk and land-use change. Oikos 2022, e08232.
Boutin S, Larsen K (1993). Does food availability affect growth and survival of males and females differently in a promiscuous small mammal, Tamiasciurus hudsonicus. Journal of Animal Ecology 62, 364-70.
Boutin S, Wauters LA, McAdam AG, Humphries MM, Tosi G, Dhondt AA (2006). Anticipatory reproduction and population growth in seed predators. Science 314, 1928-30.
Brehm AM, Mortelliti A (2021). Land-use change alters associations between personality and microhabitat selection. Ecological Applications 31, e02443.
Cabrera D, Nilsson JR, Griffen BD (2021). The development of animal personality across ontogeny: A cross-species review. Animal Behaviour 173, 137-44.
Carter AJ, Feeney WE, Marshall HH, Cowlishaw G, Heinsohn R (2013). Animal personality: What are behavioural ecologists measuring? Biological Reviews 88, 465-75.
Cerqueira M, Rey S, Silva T, Featherstone Z, Crumlish M, MacKenzie S (2016). Thermal preference predicts animal personality in Nile tilapia Oreochromis niloticus. Journal of animal ecology 85, 1389-400.
Chmura HE, Zhang VY, Wilbur SM, Barnes BM, Buck CL, Williams CT (2020). Plasticity and repeatability of activity patterns in free-living Arctic ground squirrels. Animal Behaviour 169, 81-91.
Cote J, Clobert J, Brodin T, Fogarty S, Sih A (2010). Personality-dependent dispersal: Characterization, ontogeny and consequences for spatially structured populations. Philosophical Transactions of the Royal Society B 365, 4065-76.
Dall SRX, Houston AI, McNamara JM (2004). The behavioural ecology of personality: Consistent individual differences from an adaptive perspective. Ecology Letters 7, 734-9.
Di Pierro E, Bertolino S, Martinoli A, Preatoni D, Tosi G, Wauters LA (2010). Estimating offspring production using capture-mark-recapture and genetic methods in red squirrels. Ecological Research 25, 395-402.
Di Pierro E, Ghisla A, Wauters LA et al. (2011). The effects of seed availability on habitat use by a specialist seed predator. European Journal of Wildlife Research 57, 585-95.
Dingemanse NJ, Kazem AJN, Réale D, Wright J (2010). Behavioural reaction norms: Animal personality meets individual plasticity. Trends in Ecology & Evolution 25, 81-9.
Dingemanse NJ, Bouwman KM, van de Pol M et al. (2012). Variation in personality and behavioural plasticity across four populations of the great tit Parus major. Journal of Animal Ecology 81, 116-26.
Dingemanse NJ, Wolf M (2013). Between-individual differences in behavioural plasticity within populations: causes and consequences. Animal Behaviour 85, 1031-9.
Edelaar P, Siepielski AM, Clobert J (2008). Matching habitat choice causes directed gene flow: A neglected dimension in evolution and ecology. Evolution 62, 2462-72.
Endler JA (1977). Geographical Variation, Speciation and Clines. Princeton University Press, Princeton, NJ.
Gelman A, Rubin DB (1992). Inference from iterative simulation using multiple sequences. Statistical Science 7, 457-72.
Geweke J (1992). Evaluating the accuracy of sampling-based approaches to the calculation of posterior moments. In: Bernardo JM, Berger AP, Dawid AP, Smith AFM, eds. Bayesian Statistics. Oxford University Press, Oxford, pp. 169-93.
Hadfield JD (2010). MCMC methods for multi-response generalized linear mixed models: The MCMCglmm R package. Journal of Statistical Software 33, 1-22.
Hänninen L, Pastell M (2009). CowLog: Open-source software for coding behaviors from digital video. Behavior Research Methods 41, 472-6.
Hewes ME, Delventhal K, Chaves-Campos J (2017). Behavioral plasticity and consistency in the naked-footed mouse (Peromyscus nudipes) with habitat disturbance. Journal of Ethology 35, 279-92.
Hoffman AA, Merilä J (1999). Heritable variation and evolution under favourable and unfavourable conditions. Trends in Ecology and Evolution 12, 460-1.
Holtmann B, Santos ESA, Lara CE, Nakagawa S (2017). Personality-matching habitat choice, rather than behavioural plasticity, is a likely driver of a phenotype-environment covariance. Proceedings of the Royal Society B 284, 20170943.
Kawecki TJ, Ebert D (2004). Conceptual issues in local adaptation. Ecology Letters 7, 1225-41.
Koprowski J (1994a). Sciurus niger. Mammalian Species 479, 1-9.
Koprowski J (1994b). Sciurus carolinensis. Mammalian Species 480, 1-9.
Lurz PWW, Garson PJ, Wauters LA (2000). Effects of temporal and spatial variations in food supply on the space and habitat use of red squirrels, Sciurus vulgaris L. Journal of Zoology 251, 167-78.
Lurz PWW, Lloyd AJ (2000). Body weights in grey and red squirrels: Do seasonal weight increases occur in conifer woodland? Journal of Zoology 252, 539-43.
Mari V, Martini S, Romeo C et al. (2008). Record litter size in the Eurasian red squirrel (Sciurus vulgaris). Hystrix, the Italian Journal of Mammalogy 19, 61-5.
Martin JGA, Réale D (2008). Animal temperament and human disturbance: Implications for the response of wildlife to tourism. Behavioural Processes 77, 66-72.
Martin JGA, Nussey DH, Wilson AJ, Réale D (2011). Measuring individual differences in reaction norms in field and experimental studies: A power analysis of random regression models: Power analysis of random regression models. Methods in Ecology and Evolution 2, 362-74.
Mazzamuto MV, Cremonesi G, Santicchia F, Preatoni D, Martinoli A, Wauters LA (2019). Rodents in the arena: A critical evaluation of methods measuring personality traits. Ethology Ecology & Evolution 31, 38-58.
McAdam AG, Boutin S, Réale D, Berteaux D (2002). Maternal effects and the potential for evolution in a natural population of animals. Evolution 56, 846-51.
McAdam AG, Boutin S (2003). Effects of food abundance on genetic and maternal variation in the growth rate of juvenile red squirrels. Journal of Evolutionary Biology 16, 1249-56.
Nash DJ, Seaman RN (1977). Sciurus aberti. Mammalian Species 80, 1-5.
R Core Team (2020). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. Available from URL: https://www.R-project.org/
Rabdeau J, Arroyo B, Mougeot F, Badenhausser I, Bretagnolle V, Monceau K (2021). Do human infrastructures shape nest distribution in the landscape depending on individual personality in a farmland bird of prey? Journal of Animal Ecology 90, 2848-58.
Réale D, Reader SM, Sol D, McDougall PT, Dingemanse NJ (2007). Integrating animal temperament within ecology and evolution. Biological Reviews 82, 291-318.
Rodrigues D, Wauters LA, Romeo C et al. (2010). Living on the edge: Can Eurasian red squirrels (Sciurus vulgaris) persist in extreme high-elevation habitats? Arctic, Antarctic, and Alpine Research 42, 106-12.
Romeo C, Wauters LA, Preatoni D, Tosi G, Martinoli A (2010). Living on the edge: Space use of Eurasian red squirrels in marginal high-elevation habitat. Acta Oecologica 36, 604-10.
Royauté R, Dochtermann NA (2021). Comparing ecological and evolutionary variability within datasets. Behavioral Ecology and Sociobiology 75, 127.
Salmaso F, Molinari A, Di Pierro E et al. (2009). Estimating and comparing food availability for tree-seed predators in typical pulsed-resource systems: alpine conifer forests. Plant Biosystems 143, 258-67.
Santicchia F, Gagnaison C, Bisi F et al. (2018). Habitat-dependent effects of personality on survival and reproduction in red squirrels. Behavioral Ecology and Sociobiology 72, 134.
Santicchia F, Romeo C, Ferrari N et al. (2019). The price of being bold? Relationship between personality and endoparasitic infection in a tree squirrel. Mammalian Biology 97, 1-8.
Santicchia F, Wauters LA, Piscitelli AP et al. (2020a). Spillover of an alien parasite reduces expression of costly behaviour in native host species. Journal of Animal Ecology 89, 1559-69.
Santicchia F, Wauters LA, Dantzer B et al. (2020b). Relationships between personality traits and the physiological stress response in a wild mammal. Current Zoology 66, 197-204.
Santicchia F, Van Dongen S, Martinoli A, Preatoni D, Wauters LA (2021). Measuring personality traits in Eurasian red squirrels: A critical comparison of different methods. Ethology 127, 187-201.
Santicchia F, Wauters LA, Tranquillo C et al. (2022). Invasive alien species as an environmental stressor and its effects on coping style in a native competitor, the Eurasian red squirrel. Hormones and Behavior 140, 105127.
Sih A, Bell A, Johnson JC (2004). Behavioral syndromes: An ecological and evolutionary overview. Trends in Ecology & Evolution 19, 372-8.
Sih A, Cote J, Evans M, Fogarty S, Pruitt J (2012). Ecological implications of behavioural syndromes. Ecology Letters 15, 278-89.
Spiegel O, Leu ST, Bull CM, Sih A (2017). What's your move? Movement as a link between personality and spatial dynamics in animal populations. Ecology Letters 20, 3-18.
Stamps JA, Groothuis TGG (2010). Developmental perspectives on personality: Implications for ecological and evolutionary studies of individual differences. Philosophical Transactions of the Royal Society B: Biological Sciences 365, 4029-41.
Stoffel MA, Nakagawa S, Schielzeth H (2017). rptR: Repeatability estimation and variance decomposition by generalized linear mixed-effects models. Methods in Ecology and Evolution 8, 1639-44.
Toscano BJ, Gownaris NJ, Heerhartz SM, Monaco CJ (2016). Personality, foraging behavior and specialization: integrating behavioral and food web ecology at the individual level. Oecologia 182, 55-69.
Tranquillo C, Villa F, Wauters LA et al. (2022). Physiological stress and spatio-temporal fluctuations of food abundance and population density in Eurasian red squirrels. Hystrix, the Italian Journal of Mammalogy 33, 26-32.
Verbeke G, Molenberghs G (2000). Linear Mixed Models for Longitudinal Data. Springer, New York.
Wauters LA, Dhondt AA (1989a). Variation in length and body weight of the red squirrel in two different habitats. Journal of Zoology 217, 93-106.
Wauters LA, Dhondt AA (1989b). Body weight, longevity and reproductive success in red squirrels (Sciurus vulgaris). Journal of Animal Ecology 58, 637-51.
Wauters LA, Dhondt AA, De Vos R (1990). Factors affecting male mating success in red squirrels (Sciurus vulgaris). Ethology Ecology & Evolution 2, 195-204.
Wauters LA, Dhondt AA (1992). Spacing behaviour of red squirrels, Sciurus vulgaris: Variation between habitats and the sexes. Animal Behaviour 43, 297-311.
Wauters LA, Swinnen C, Dhondt AA (1992). Activity budget and foraging behaviour of red squirrels (Sciurus vulgaris) in coniferous and deciduous habitats. Journal of Zoology 227, 71-86.
Wauters LA, Bijnens L, Dhondt AA (1993). Body mass at weaning and juvenile recruitment in the red squirrel. Journal of Animal Ecology 62, 280-6.
Wauters LA, Dhondt AA (1993). Immigration patterns and success in red squirrels. Behavioral Ecology and Sociobiology 33, 159-67.
Wauters LA, Matthysen E, Dhondt AA (1994). Survival and lifetime reproductive success in dispersing and resident red squirrels. Behavioral Ecology and Sociobiology 34, 197-201.
Wauters LA, Dhondt AA (1995). Components of lifetime reproductive success of female Eurasian red squirrels. Oikos 72, 402-10.
Wauters LA, Lens L (1995). Effects of food abundance and density on red squirrel (Sciurus vulgaris) reproduction. Ecology 76, 2460-9.
Wauters LA, Gurnell J, Preatoni D, Tosi G (2001). Effects of spatial variation in food availability on spacing behaviour and demography of Eurasian red squirrels. Ecography 24, 525-38.
Wauters LA, Vermeulen M, Van Dongen S et al. (2007) Effects of spatio-temporal variation in food supply on red squirrel Sciurus vulgaris body size and body mass and its consequences for some fitness components. Ecography 30, 51-65.
Wauters LA, Githiru M, Bertolino S, Molinari A, Tosi G, Lens L (2008). Demography of alpine red squirrel populations in relation to fluctuations in seed crop size. Ecography 31, 104-14.
Wauters LA, Preatoni D, Martinoli A, Verbeylen G, Matthysen E (2011). No sex bias in natal dispersal of Eurasian red squirrels. Mammalian Biology 76, 369-72.
Wauters LA, Mazzamuto MV, Santicchia F, Van Dongen S, Preatoni DG, Martinoli A (2019). Interspecific competition affects the expression of personality-traits in natural populations. Scientific Reports 9, 11189.
Wauters LA, Mazzamuto MV, Santicchia F et al. (2021). Personality traits, sex and food abundance shape space use in an arboreal mammal. Oecologia 196, 65-76.
Wilson AJ, Réale D, Clements MN et al. (2010). An ecologist's guide to the animal model. Journal of Animal Ecology 79, 13-26.
Zhang VY, Buck CL (2022). Seasonal patterns in behavior and glucocorticoid secretion of a specialist Holarctic tree squirrel (Sciurus aberti). Journal of Comparative Physiology B 192, 541-59.
Zong C, Wauters LA, Van Dongen S et al. (2010). Annual variation in predation and dispersal of Arolla pine (Pinus cembra L.) seeds by Eurasian red squirrels and other seed-eaters. Forest Ecology and Management 260, 587-94.

Auteurs

Claudia Tranquillo (C)

Environment Analysis and Management Unit - Guido Tosi Research Group - Department of Theoretical and Applied Sciences, Università degli Studi dell'Insubria, Varese, Italy.

Lucas Armand Wauters (LA)

Environment Analysis and Management Unit - Guido Tosi Research Group - Department of Theoretical and Applied Sciences, Università degli Studi dell'Insubria, Varese, Italy.
Evolutionary Ecology Group, Department of Biology, University of Antwerp, Wilrijk, Belgium.

Francesca Santicchia (F)

Environment Analysis and Management Unit - Guido Tosi Research Group - Department of Theoretical and Applied Sciences, Università degli Studi dell'Insubria, Varese, Italy.

Damiano Preatoni (D)

Environment Analysis and Management Unit - Guido Tosi Research Group - Department of Theoretical and Applied Sciences, Università degli Studi dell'Insubria, Varese, Italy.

Adriano Martinoli (A)

Environment Analysis and Management Unit - Guido Tosi Research Group - Department of Theoretical and Applied Sciences, Università degli Studi dell'Insubria, Varese, Italy.

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