Skip to main content
SpringerLink
Log in

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

  • Original Article
  • Published:
Behavioral Ecology and Sociobiology Aims and scope Submit manuscript

Abstract

Personality traits overlap in behavioral syndromes that are assumed to be related to physiology and life history traits, shaping pace-of-life syndromes. Boldness and explorative behavior are frequently associated with higher parasite loads, increased resource acquisition, less efficient antipredator behavior, and reduced survival (e.g., through predation). We explored how personality is related to these biological traits using an invasive species—Atlantoxerus getulus in Fuerteventura island—as a model system with reduced parasitism and low predation pressure. We used breath rate during handling, open field tests, and escape trials to test for the existence of interindividual differences in boldness, explorative behavior, and escape speed, respectively. We also tested whether the personality traits were related and formed behavioral syndromes in A. getulus. At the same time, we explored how personality is related to ectoparasite load, body condition, and survival in the species. We found strong between-individual differences in breath rate, readiness to get in the open field arena, and escape speed. We found a behavioral syndrome, linking open field entrance and escape speed, in A. getulus. However, personality was not related to parasite load or body condition and survival was higher for bolder individuals. As a whole, our results suggest reduced parasites and predator pressures on Fuerteventura may have potentially neutralized the typical drawbacks of a fast pace-of-life in the introduced population of A. getulus.

Significance statement

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Altizer S, Nunn CL, Thrall PH, Gittleman JL, Antonovics J, Cunningham AA, Dobson AP, Ezenwa V, Jones KE, Pedersen AB, Poss M, Pulliam JRC (2003) Social organization and parasite risk in mammals: integrating theory and empirical studies. Annu Rev Ecol Evol S 34:517–547

    Article  Google Scholar 

  • Barber I, Dingemanse NJ (2010) Parasitism and the evolutionary ecology of animal personality. Phil Trans R Soc B 365:4077–4088

    Article  PubMed  Google Scholar 

  • Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effect models using lme4. J Stat Softw 67:1–48

    Article  Google Scholar 

  • Bergeron P, Montiglio P-O, Réale D, Humphries MM, Gimenez O, Garant D (2013) Disruptive viability selection on adult exploratory behaviour in eastern chipmunks. J Evol Biol 26:766–774

    Article  PubMed  CAS  Google Scholar 

  • Bijleveld AI, Massourakis G, van der Marel A, Dekinga A, Spaans B, van Gils JA, Piersma T (2014) Personality drives physiological adjustments and is not related to survival. Proc R Soc B 281:20133135

    Article  PubMed  Google Scholar 

  • Biro PA, Stamps JA (2008) Are animal personality traits linked to life-history productivity? Trends Ecol Evol 23:361–368

    Article  PubMed  Google Scholar 

  • Blackburn TM, Pyšek P, Bacher S, Carlton JT, Duncan RP, Jarošík V, Wilson JRU, Richardson DM (2011) A proposed unified framework for biological invasions. Trends Ecol Evol 26:333–339

    Article  PubMed  Google Scholar 

  • Blight O, Josens R, Bertelsmeier C, Abril S, Boulay R, Cerdá X (2017) Differences in behavioural traits among native and introduced colonies of an invasive ant. Biol Invasions 19:1389–1398

    Article  Google Scholar 

  • Blumstein DT, Flores G, Munoz NE (2015) Does locomotor ability influence flight initiation distance in yellow-bellied marmots? Ethology 120:1–8

    Google Scholar 

  • Blumstein DT, Lea AJ, Olson LE, Martin JGA (2010) Heritability of anti-predatory traits: vigilance and locomotor performance in marmots. J Evol Biol 23:879–887

    Article  PubMed  CAS  Google Scholar 

  • Boon AK, Réale D, Boutin S (2007) The interaction between personality, offspring fitness and food abundance in North American red squirrels. Ecol Lett 10:1094–1104

    Article  PubMed  Google Scholar 

  • Boon AK, Réale D, Boutin S (2008) Personality, habitat use, and their consequences for survival in North American red squirrels Tamiasciurus hudsonicus. Oikos 117:1321–1328

    Article  Google Scholar 

  • Boyer N, Réale D, Marmet J, Pisanu B, Chapuis J-L (2010) Personality, space use and tick load in an introduced population of Siberian chipmunks Tamias sibiricus. J Anim Ecol 79:538–547

    Article  PubMed  Google Scholar 

  • Brommer JE, Kluen E (2012) Exploring the genetics of nestling personality traits in a wild passerine bird: testing the phenotypic gambit. Ecol Evol 2:3032–3044

    Article  PubMed  PubMed Central  Google Scholar 

  • Bush AO, Lafferty KD, Lotz JM, Shostak AW (1997) Parasitology meets ecology on its own terms. Margolis et al. revisited. J Parasitol 83:575–583

  • Cabrera D, Andres D, McLoughlin PD, Debeffe L, Medill SA, Wilson AJ, Poissant J (2017) Island tameness and the repeatability of flight initiation distance in a large herbivore. Can J Zool 95:771–778

    Article  Google Scholar 

  • Careau V, Thomas D, Humphries MM, Réale D (2008) Energy metabolism and animal personality. Oikos 117:641–653

    Article  Google Scholar 

  • Careau V, Thomas DW, Humphries MM (2010) Energetic cost of bot fly parasitism in free-ranging eastern chipmunks. Oecologia 162:303–312

    Article  PubMed  Google Scholar 

  • Carere C, van Oers K (2004) Shy and bold great tits (Parus major): body temperature and breath rate in response to handling stress. Physiol Behav 82:905–912

    Article  PubMed  CAS  Google Scholar 

  • Carter AJ, Goldizen AW, Tromp SA (2010) Agamas exhibit behavioral syndromes: bolder males bask and feed more but may suffer higher predation. Behav Ecol 21:655–661

    Article  Google Scholar 

  • Chapple DG, Simmonds SM, Wong BBM (2012) Can behavioral and personality traits influence the success of unintentional species introductions? Trends Ecol Evol 27:57–64

    Article  PubMed  Google Scholar 

  • Class B, Brommer JE (2016) Senescence of personality in a wild bird. Behav Ecol Sociobiol 70:733–744

    Article  Google Scholar 

  • Corti M, Bazzi G, Costanzo A, Podofillini S, Saino N, Rubolini D, Romano A (2017) Behavioural stress response and melanin-based plumage colouration in barn swallow nestlings. Behaviour 154:853–874

    Article  Google Scholar 

  • Cote J, Clobert J, Brodin T, Fogarty S, Sih A (2010) Personality-dependent dispersal: characterization, ontogeny and consequences for spatially structured populations. Phil Trans R Soc B 365:4065–4076

    Article  PubMed  CAS  Google Scholar 

  • David M, Auclair Y, Dechaume-Moncharmont F-X, Cézilly F (2012) Handling stress does not reflect personality in female zebra finches (Taeniopygia guttata). J Comp Psychol 126:10–14

    Article  PubMed  Google Scholar 

  • del Arco Aguilar M-J, González-González R, Garzón-Machado V, Pizarro-Hernández B (2010) Actual and potential natural vegetation on the Canary Islands and its conservation status. Biodivers Conserv 19:3089–3140

    Article  Google Scholar 

  • Dingemanse NJ, Both C, Drent PJ, Tinbergen JM (2004) Fitness consequences of avian personalities in a fluctuating environment. Proc R Soc Lond B 271:847–852

    Article  Google Scholar 

  • Dingemanse NJ, Dochtermann NA (2013) Quantifying individual variation in behaviour: mixed-effect modelling approaches. J Anim Ecol 82:39–54

    Article  PubMed  Google Scholar 

  • Dingemanse NJ, Dochterman NA, Nakagawa S (2012) Defining behavioural syndromes and the role of ‘syndrome deviation’ in understanding their evolution. Behav Ecol Sociobiol 66:1543–1548

    Article  Google Scholar 

  • Dubuc-Messier G, Réale R, Perret P, Charmantier A (2017) Environmental heterogeneity and population differences in blue tits personality. Behav Ecol 28:448–459

    PubMed  Google Scholar 

  • Ezenwa VO, Archie EA, Craft ME, Hawley DM, Martin LB, Moore J, White L (2016) Host behaviour-parasite feedback: an essential link between animal behaviour and disease ecology. Proc R Soc B 283:20153078

    Article  PubMed  CAS  Google Scholar 

  • Ferrari C, Pasquaretta C, Carere C, Cavallone E, von Hardenberg A, Réale D (2013) Testing for the presence of coping styles in a wild mammal. Anim Behav 85:1385–1396

    Article  Google Scholar 

  • Gelman A, Rubin DB (1992) Inference from iterative simulation using multiple sequences. Stat Sci 7:457–511

    Article  Google Scholar 

  • Hadfield JD (2010) MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R package. J Stat Softw 33:1–22

    Article  Google Scholar 

  • Haigh A, Butler F, O’Riordan R, Palme R (2017a) Managed parks as a refuge for the threatened red squirrel (Sciurus vulgaris) in light of human disturbance. Biol Conserv 211:29–36

    Article  Google Scholar 

  • Haigh A, O’Riordan R, Butler F (2017b) Variations in aggression and activity levels amongst squirrels inhabiting low and high density areas. Ecol Res 32:931–941

    Article  Google Scholar 

  • Hall ML, van Asten T, Katsis AC, Dingemanse NJ, Magrath MJL, Mulder RA (2015) Animal personality and pace-of-life syndromes: do fast-exploring fairy-wrens die young? Front Ecol Evol 3:28

    Google Scholar 

  • Hillegass MA, Waterman JM, Roth JD (2008) The influence of sex and sociality on parasite loads in an African ground squirrel. Behav Ecol 19:1006–1011

    Article  Google Scholar 

  • Hillegass MA, Waterman JM, Roth JD (2010) Parasite removal increases reproductive success in a social African ground squirrel. Behav Ecol 21:696–700

    Article  Google Scholar 

  • Houston AI, McNamara JM, Hutchinson JMC (1993) General results concerning the trade-off between gaining energy and avoiding predation. Phil Trans R Soc B 341:375–397

    Article  Google Scholar 

  • Husak JF (2006a) Does survival depend on how fast you can run or how fast you do run? Funct Ecol 20:1080–1086

    Article  Google Scholar 

  • Husak JF (2006b) Does speed help you survive? A test with collared lizards of different ages. Funct Ecol 20:174–179

    Article  Google Scholar 

  • Jones KA, Godin J-GJ (2010) Are fast explorers slow reactors? Linking personality type and anti-predator behaviour. Proc R Soc Lond B 277:625–632

    Article  Google Scholar 

  • Khokhlova IS, Krasnov BR, Kam M, Burdelova NI, Degen AA (2002) Energy cost of ectoparasitism: the flea Xenopsylla ramesis on the desert gerbil Gerbillus dasyurus. J Zool 258:349–354

    Article  Google Scholar 

  • Kiffner C, Stanko M, Morand S, Khokhlova IS, Shenbrot GI, Laudisoit A, Leirs H, Hawlena H, Krasnov BR (2013) Sex-biased parasitism is not universal: evidence from rodent-flea associations from three biomes. Oecologia 173:1009–1022

    Article  PubMed  Google Scholar 

  • Kight CR, David M, Dall SRX (2013) The evolution of animal personality variation. In: eLS. John Wiley & Sons ltd., Chichester, http://www.els.net

  • Kluen E, Siitari H, Brommer JE (2014) Testing for between individual correlations of personality and physiological traits in a wild bird. Behav Ecol Sociobiol 68:205–213

    Article  Google Scholar 

  • Koprowski JL (2002) Handling tree squirrels with a safe and efficient restraint. Wildlife Soc Bull 30:101–103

    Google Scholar 

  • Kortet R, Hedrick AV, Vainikka A (2010) Parasitism, predation and the evolution of animal personalities. Ecol Lett 13:1449–1458

    Article  PubMed  Google Scholar 

  • Krams IA, Vrublevska J, Sepp J, Abolins-Abols M, Rantala MJ, Mierauskas P, Krama T (2014) Sex-specific associations between nest defence, exploration and breathing rate in breeding pied flycatchers. Ethology 120:492–501

    Article  Google Scholar 

  • Krasnov BR, Morand S, Hawlena H, Khokhlova IS, Shenbrot GI (2005) Sex-biased parasitism, seasonality and sexual size dimorphism in desert rodents. Oecologia 146:209–217

    Article  PubMed  Google Scholar 

  • Lande R, Arnold SJ (1983) The measurement of selection on correlated characters. Evolution 37:1210–1226

    Article  PubMed  Google Scholar 

  • Le Coeur C, Thibault M, Pisanu B, Thibault S, Chapuis J-L, Baudry E (2015) Temporally fluctuating selection on a personality trait in a wild rodent population. Behav Ecol 26:1285–1291

    Article  Google Scholar 

  • Le Galliard J-F, Paquet M, Mugabo M (2015) An experimental test of density-dependent selection on temperament traits of activity, boldness and sociability. J Evol Biol 28:1144–1155

    Article  PubMed  Google Scholar 

  • Lemaître J, Fortin D, Montiglio P-O, Darveau M (2009) Bot fly parasitism of the red-backed vole: host survival, infection risk, and population growth. Oecologia 159:283–294

    Article  PubMed  Google Scholar 

  • López-Darias M (2007) Ecología de una invasión: el caso de la ardilla moruna (Atlantoxerus getulus) en la isla de Fuerteventura (Islas Canarias). University of La Laguna, San Cristóbal de La Laguna

  • López-Darias M, Lobo JM (2008) Factors affecting invasive species abundance: the Barbary ground squirrel on Fuerteventura island, Spain. Zool Stud 47:268–281

    Google Scholar 

  • López-Darias M, Nogales M (2008) Effects of the invasive Barbary ground squirrel (Atlantoxerus getulus) on seed dispersal systems of insular xeric environments. J Arid Environ 72:926–939

    Article  Google Scholar 

  • López-Darias M, Ribas A, Feliú C (2008) Helminth parasites in native and invasive mammal populations: comparative study on the Barbary ground squirrel Atlantoxerus getulus L. (Rodentia, Sciuridae) in Morocco and the Canary Islands. Acta Parasitol 53:296–301

    Article  Google Scholar 

  • Machado A (1979) The introduction of the Getulian squirrel (Atlantoxerus getulus L. 1758) in Fuerteventura, Canary Islands. Egypt J Wildl Nat Res 2:182–203

    Google Scholar 

  • Machado A, Domínguez F (1982) Estudio sobre la presencia de Ardilla Moruna (Atlantoxerus getulus L.) en la isla de Fuerteventura; su introducción, su biología y su impacto en el medio. Ministerio de Agricultura, Pesca y Alimentación, Instituto Nacional para la Conservación de la Naturaleza, San Cristóbal de La Laguna

  • Macleod R, Barnett P, Clark JA, Cresswell W (2005) Body mass change strategies in blackbirds Turdus merula: the starvation-predation risk trade-off. J Anim Ecol 74:292–302

    Article  Google Scholar 

  • Malange J, Izar P, Japyassú H (2016) Personality and behavioural syndrome in Necromys lasiurus (Rodentia: Cricetidae): notes on dispersal and invasion processes. Acta Ethol 19:189–195

    Article  Google Scholar 

  • Marras S, Killen SS, Claireaux G, Domenici P, McKenzie DJ (2011) Behavioural and kinematic components of the fast-start escape response in fish: individual variation and temporal repeatability. J Exp Biol 214:3102–3110

    Article  PubMed  Google Scholar 

  • Marzol-Jaén MV (1988) La Lluvia: un recurso natural para Canarias. Servicio de Publicaciones de la Caja General de Ahorro de Canarias, Santa Cruz de Tenerife

  • Monceau K, Dechaume-Montcharmont F-X, Moreau J, Lucas C, Capoduro R, Motreuil S, Moret Y (2017) Personality, immune response and reproductive success: an appraisal of the pace-of-life syndrome hypothesis. J Anim Ecol 86:932–942

    Article  PubMed  Google Scholar 

  • Montiglio P-O, Garant D, Pelletier F, Réale D (2012) Personality differences are related to long-term stress reactivity in a population of wild eastern chipmunks, Tamias striatus. Anim Behav 84:1071–1079

    Article  Google Scholar 

  • Mortola JP, Lanthier C (2005) Breathing frequency in ruminants: a comparative analysis with non-ruminant mammals. Respir Physiol Neurobiol 145:265–277

    Article  PubMed  Google Scholar 

  • Mutascio HE, Pittman SE, Zollner PA (2017) Investigating movement behavior of invasive Burmese pythons on a shy–bold continuum using individual-based modeling. Perspect Ecol Conserv 15:25–31

    Article  Google Scholar 

  • Nakagawa S, Schielzeth H (2010) Repeatability for Gaussian and non-Gaussian data: a practical guide for biologists. Biol Rev 85:935–956

    PubMed  Google Scholar 

  • Oufiero CE, Garland T (2009) Repeatability and correlation of swimming performances and size over varying time-scales in the guppy (Poecilia reticulata). Funct Ecol 23:969–978

    Article  Google Scholar 

  • Patterson JEH, Neuhaus P, Kutz SJ, Ruckstuhl KE (2013) Parasite removal improves reproductive success of female North American red squirrels (Tamiasciurus hudsonicus). PLoS One 8:e55779

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Peig J, Green AJ (2009) New perspectives for estimating body condition from mass/length data: the scaled mass index as an alternative method. Oikos 118:1883–1891

    Article  Google Scholar 

  • Perals D, Grif S, Bartomeus I, Sol D (2017) Revisiting the open-field test: what does it really tell us about animal personality? Anim Behav 123:69–79

    Article  Google Scholar 

  • Perez VJ, Eatwell JC, Samorajski T (1980) A metabolism chamber for measuring oxygen consumption in the laboratory rat and mouse. Physiol Behav 24:1185–1189

    Article  PubMed  CAS  Google Scholar 

  • Phillips BL, Suarez AV (2012) The role of behavioural variation in the invasion of new areas. In: Candolin U, Wong BBM (eds) Behavioural responses to a changing world. Oxford University Press, Oxford, pp 190–200.

    Chapter  Google Scholar 

  • Phillips MA, Waterman JM (2014) Anti-snake behaviour in a facultative cooperative breeder, the cape ground squirrel. Behaviour 151:1735–1758

    Article  Google Scholar 

  • Quinn JL, Cresswell W (2005) Personality, anti-predation behaviour and behavioural plasticity in the chaffinch Fringilla coelebs. Behaviour 142:1377–1402

    Article  Google Scholar 

  • R Development Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna http://www.R-project.org

    Google Scholar 

  • Réale D, Garant D, Humphries MM, Bergeron P, Careau V, Montiglio P-O (2010) Personality and the emergence of the pace-of-life syndrome concept at the population level. Phil Trans R Soc B 365:4051–4063

    Article  PubMed  Google Scholar 

  • Réale D, Reader SM, Sol D, McDougall PT, Dingemanse NJ (2007) Integrating animal temperament within ecology and evolution. Biol Rev 82:291–318

    Article  PubMed  Google Scholar 

  • Rödel HG, Zapka M, Talke S, Kornatz T, Bruchner B, Hedler C (2014) Survival costs of fast exploration during juvenile life in a small mammal. Behav Ecol Sociobiol 69:205–217

    Article  Google Scholar 

  • Rodríguez-Prieto I, Martín J, Fernández-Juricic E (2011) Individual variation in behavioural plasticity: direct and indirect effects of boldness, exploration and sociability on habituation to predators in lizards. Proc R Soc Lond B 278:266–273

    Article  Google Scholar 

  • Rózsa L, Reiczigel J, Majoros G (2000) Quantifying parasites in samples of hosts. J Parasitol 86:228–232

    Article  PubMed  Google Scholar 

  • Schulte-Hostedde AI, Millar JS (2002) Effects of body size and mass on running speed of male yellow-pine chipmunks (Tamias amoenus). Can J Zool 80:1584–1587

    Article  Google Scholar 

  • Sih A, Bell AM (2008) Insights for behavioral ecology from behavioral syndromes. Adv Stud Behav 38:227–281

    Article  Google Scholar 

  • Sih A, Bell A, Johnson JC (2004a) Behavioral syndromes: an ecological and evolutionary overview. Trends Ecol Evol 19:372–378

    Article  PubMed  Google Scholar 

  • Sih A, Bell AM, Johnson JC, Ziemba RE (2004b) Behavioral syndromes: an integrative overview. Q Rev Biol 79:241–277

    Article  PubMed  Google Scholar 

  • Sih A, Cote J, Evans M, Fogarty S, Pruitt J (2012) Ecological implications of behavioural syndromes. Ecol Lett 15:278–289

    Article  PubMed  Google Scholar 

  • Sikes RS, Gannon WL (2011) Guidelines of the American Society of Mammalogists for the use of wild mammals in research. J Mammal 92:235–253

    Article  Google Scholar 

  • Šimková O, Frýdlová P, Žampachová B, Frynta D, Landová E (2017) Development of behavioural common boa (Boa imperator): repeatable independent traits of personality? PLoS One 12:e0177911

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Smith BR, Blumstein DT (2007) Fitness consequences of personality: a meta-analysis. Behav Ecol 19:448–455

    Article  Google Scholar 

  • Stamps JA (2007) Growth-mortality tradeoffs and “personality traits” in animals. Ecol Lett 10:355–363

    Article  PubMed  Google Scholar 

  • Stamps J, Groothuis TGG (2010) The development of animal personality: relevance, concepts and perspectives. Biol Rev 85:301–325

    Article  PubMed  Google Scholar 

  • Stoffel MA, Nakagawa S, Schielzeth H (2017) RptR: repeatability estimation and variance decomposition by generalized linear mixed-effect models. Methods Ecol Evol (published online, https://doi.org/10.1111/2041-210X.12797)

  • Thorlacius M, Hellström G, Brodin T (2015) Behavioral dependent dispersal in the invasive round goby Neogobius melanostomus depends on population age. Curr Zool 61:529–542

    Article  Google Scholar 

  • Torchin ME, Lafferty KD, Dobson AP, McKenzie VJ, Kuris AM (2003) Introduced species and their missing parasites. Nature 421:628–630

    Article  PubMed  CAS  Google Scholar 

  • van Oers K, Drent PJ, de Goede P, van Noordwijk AJ (2004) Realized heritability and repeatability of risk-taking behaviour in relation to avian personalities. Proc R Soc Lond B 271:65–73

    Article  Google Scholar 

  • Wolf M, van Doorn GS, Leimar O, Weissing FJ (2007) Life-history trade-offs favour the evolution of animal personalities. Nature 447:581–584

    Article  PubMed  CAS  Google Scholar 

  • Závorka L, Aldvén D, Näslund J, Höjesjö J, Johnsson JI (2015) Linking lab activity with growth and movement in the wild: explaining pace-of-life in a trout stream. Behav Ecol 26:877–884

    Article  Google Scholar 

  • Zohdy S, Bisanzio D, Tecot S, Wright PC, Jernvall J (2017) Aggression and hormones are associated with heterogeneity in parasitism and parasite dynamics in the brown mouse lemur. Anim Behav 132:109–119

    Article  Google Scholar 

Download references

Acknowledgments

We would like to thank E. Koole and T. Dorta Morales for their help during fieldwork. We acknowledge all constructive comments regarding data analyses from R. Dorta. We are thankful to A. Martín, M. Molina Borja, and J. María Fernández-Palacios, as their comments during the master thesis of JCP have been incorporated into this manuscript. Special thanks to the Cabildo de Fuerteventura for the kindness of its staff and for providing allocation and facilities on Fuerteventura that greatly contributed to this work. Particular thanks as well to Instituto de Productos Naturales y Agrobiología (Consejo Superior de Investigaciones Científicas) and its previous director (Dr. Cosme García), by providing a vehicle to accomplish the fieldwork. The excellent reviews by two anonymous reviewers from BES contributed significantly to the improvement of the final version of this manuscript.

Funding

This study was also supported by the National Research Council of Canada, the Canadian Foundation for Innovation, and a university research grant from the University of Manitoba to JMW. AvdM was also supported by the University of Manitoba, Faculty of Science graduate studentships and the Faculty of Graduate Studies Graduate Enhancement of the Tri-Council Stipend. JCP was supported with a student grant from Ministerio de Educación, Cultura y Deporte while doing his master’s thesis. ML-D was funded by the Program Agustín de Betancourt, under the identification mark “Tenerife 2030” (P. INNOVA 2016–2021).

Author information

Authors and Affiliations

  1. Island Ecology and Evolution Research Group, Instituto de Productos Naturales y Agrobiología (IPNA-CSIC), Astrofísico Francisco Sánchez no. 3, 38206, La Laguna, Tenerife, Canary Islands, Spain

    Julien C. Piquet, Marta López-Darias & Manuel Nogales

  2. Department of Biological Sciences, University of Manitoba, Winnipeg, MB, R3T 2N2, Canada

    Annemarie van der Marel & Jane Waterman

Authors
  1. Julien C. Piquet
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Marta López-Darias
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Annemarie van der Marel
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Manuel Nogales
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jane Waterman
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Julien C. Piquet.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and institutional guidelines for the care and use of animals were followed. All procedures were made in accordance with the American Mammal Association guidelines (Sikes et al. 2011), and were approved by the University of Manitoba’s Animal Care and Use Committee (#F14–032).

Additional information

Communicated by A. I. Schulte-Hostedde

Electronic supplementary material

ESM 1

(DOC 29 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Piquet, J.C., López-Darias, M., van der Marel, A. et al. Unraveling behavioral and pace-of-life syndromes in a reduced parasite and predation pressure context: personality and survival of the Barbary ground squirrel. Behav Ecol Sociobiol 72, 147 (2018). https://doi.org/10.1007/s00265-018-2549-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00265-018-2549-8

Keywords

Search

Navigation