Reactive stress-coping styles show more variable reproductive expenditure and fitness outcomes

Sih, A., Bell, A. & Johnson, J. C. Behavioural syndromes: an ecological and evolutionary overview. TREE 19, 372–377, https://doi.org/10.1016/j.tree.2004.04.009 (2004).

Article  PubMed  Google Scholar 

Biro, P. A. & Stamps, J. A. Are animal personality traits linked to life-history productivity? TREE 23, 361–368, https://doi.org/10.1016/j.tree.2008.04.003 (2008).

Article  PubMed  Google Scholar 

Duckworth, R. A. Evolution of personality: developmental constraints on behavioural flexibility. The Auk 127, 752–758, https://doi.org/10.1525/auk.2010.127.4.752 (2010).

Article  Google Scholar 

Wolf, M. & Weissing, F. J. An explanatory framework for adaptive personality differences. Philos. Trans. R. Soc. B 365, 3959–3968, https://doi.org/10.1098/rstb.2010.0215 (2010).

Article  Google Scholar 

Carere, C. & Maestripieri, D. editors. 2013. Animal personalities. Behavior, physiology, and evolution. Chicago (IL): The University of Chicago Press.

Dochtermann, N. A. & Dingemanse, N. J. Behavioral syndromes as evolutionary constraints. Behav. Ecol. 24, 806–811, https://doi.org/10.1093/beheco/art002 (2013).

Article  Google Scholar 

Réale, D., Gallant, B. Y., Leblanc, M. & Festa-Bianchet, M. Consistency of temperament in bighorn ewes and correlates with behaviour and life history. Anim. Behav. 60, 589–597 (2000).

Article  Google Scholar 

Adriaenssens, B. & Johnsson, J. I. Shy trout grow faster: exploring links between personality and fitness-related traits in the wild. Behav. Ecol. 22, 135–143, https://doi.org/10.1093/beheco/arq185 (2011).

Article  Google Scholar 

Smith, B. R. & Blumstein, D. T. Fitness consequences of personality: A metaanalysis. Behav. Ecol. 19, 448–455, https://doi.org/10.1093/beheco/arm144 (2008).

Article  Google Scholar 

Dingemanse, N. J., Both, C., Drent, P. J. & Tinbergen, J. M. Fitness consequences of avian personalities in a fluctuating environment. Proc. R. Soc. Lond. B 271, 847–852 (2004).

Article  Google Scholar 

Both, C., Dingemanse, N. J., Drent, P. J. & Tinbergen, J. M. Pairs of extreme avian personalities have highest reproductive success. J. Anim. Ecol. 74, 667–674, https://doi.org/10.1111/j.1365-2656.2005.00962.x (2005).

Article  Google Scholar 

Monestier, C. et al. Is a proactive mum a good mum? A mother’s coping style influences early fawn survival in roe deer. Behav. Ecol. 26, 1395–1403, https://doi.org/10.1093/beheco/arv087 (2015).

Article  Google Scholar 

May, T. M., Page, M. J. & Fleming, P. A. Predicting survivors: animal temperament and translocation. Behav. Ecol. 27, 969–977, https://doi.org/10.1093/beheco/arv242 (2016).

Article  Google Scholar 

Archard, G. A. & Braithwaite, V. A. The importance of wild populations in studies of animal temperament. J. Zool. 281, 149–160, https://doi.org/10.1111/j.1469-7998.2010.00714.x (2010).

Article  Google Scholar 

Ferrari, C. et al. Testing for the presence of coping styles in a wild mammal. Anim. Behav. 85, 1385–1396, https://doi.org/10.1016/j.anbehav.2013.03.030 (2013).

Article  Google Scholar 

Herborn, K. A. et al. Personality in captivity reflects personality in the wild. Anim. Behav. 79, 835–843, https://doi.org/10.1016/j.anbehav.2009.12.026 (2010).

Article  Google Scholar 

Twiss, S. D., Cairns, C., Culloch, R. M., Richards, S. A. & Pomeroy, P. P. Variation in female grey seal (Halichoerus grypus) reproductive performance correlates to proactive-reactive behavioural types. Plos One 7, e49598, https://doi.org/10.1371/journal.pone.0049598 (2012).

ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

Blaszczyk, M. B. Boldness towards novel objects predicts predator inspection in wild vervet monkeys. Anim. Behav. 123, 91–100, https://doi.org/10.1016/j.anbehav.2016.10.017 (2017).

Article  Google Scholar 

Ward‐Fear, G. et al. The ecological and life history correlates of boldness in free‐ranging lizards. Ecosphere 9, e02125, https://doi.org/10.1002/ecs2.2125 (2018).

Article  Google Scholar 

DeRango, E. J. et al. Intrinsic and maternal traits influence personality during early life in Galápagos sea lion (Zalophus wollebaeki) pups. Anim. Behav. 154, 111–120, https://doi.org/10.1016/j.anbehav.2019.06.011 (2019).

Article  Google Scholar 

Benson-Amram, S. & Holekamp, K. E. Innovative problem solving by wild spotted hyenas. Proc. R. Soc. B. 279, 4087–4095, https://doi.org/10.1098/rspb.2012.1450 (2012).

Article  PubMed  Google Scholar 

Carter, A. J., Marshall, H. H., Heinsohn, R. & Cowlishaw, G. How not to measure boldness: novel object and antipredator responses are not the same in wild baboons. Anim. Behav. 84, 603–609, https://doi.org/10.1016/j.anbehav.2012.06.015 (2012).

Article  Google Scholar 

Arvidsson, L. A., Adriaensen, F., van Dongen, S., De Stobbeleere, N. & Matthysen, E. Exploration behaviour in a different light: testing cross-context consistency of a common personality trait. Anim. Behav. 123, 151–158, https://doi.org/10.1016/j.anbehav.2016.09.005 (2017).

Article  Google Scholar 

Yuen, C. H., Schoepf, I., Schradin, C. & Pillay, N. Boldness: are open field and startle tests measuring the same personality trait? Anim. Behav. 128, 143–151, https://doi.org/10.1016/j.anbehav.2017.04.009 (2017).

Article  Google Scholar 

Sih, A., Cote, J., Evans, M., Fogarty, S. & Pruitt, J. Ecological implications of behavioural syndromes. Ecol. Letts. 15, 278–289, https://doi.org/10.1111/j.1461-0248.2011.01731.x (2012).

Article  Google Scholar 

Réale, D., Reader, S. M., Sol, D., McDougall, P. T. & Dingemanse, N. J. Integrating animal temperament within ecology and evolution. Biol. Rev. 82, 291–318, https://doi.org/10.1111/j.1469-185X.2007.00010.x (2007).

Article  PubMed  Google Scholar 

Wolf, M. & Weissing, F. J. Animal personalities: consequences for ecology and evolution. TREE 27, 452–461, https://doi.org/10.1016/j.tree.2012.05.001 (2012).

Article  PubMed  Google Scholar 

Sgoifo, A. et al. Incidence of arrhythmias and heart rate variability in wild-type rats exposed to social stress. Am. J. Physiol. 273, 1754–60 (1997).

Google Scholar 

Koolhaas, J. M. et al. Coping styles in animals: current status in behavior and stress physiology. Neurosci. Biobehav. Rev. 23, 925–935 (1999).

CAS  Article  Google Scholar 

Koolhaas, J. M., De Boer, S. F., Coppens, C. M. & Buwalda, B. Neuroendocrinology of coping styles: Towards understanding the biology of individual variation. Front. Neuroendocrinol. 31, 307–321, https://doi.org/10.1016/j.yfrne.2010.04.001 (2010).

CAS  Article  PubMed  Google Scholar 

Visser, E. K. et al. Heart rate and heart rate variability during a novel object test and a handling test in young horses. Physiol. Behav. 76, 289–296, https://doi.org/10.1016/S0031-9384(02)00698-4 (2002).

CAS  Article  PubMed  Google Scholar 

von Borell, E. et al. Heart rate variability as a measure of autonomic regulation of cardiac activity for assessing stress and welfare in farm animals: a review. Physiol. Behav. 92, 293–316 (2007).

Article  Google Scholar 

Jonckheer-Sheehy, V. S. M., Vinke, C. M. & Ortolani, A. Validation of a Polar® human heart rate monitor for measuring heart rate and heart rate variability in adult dogs under stationary conditions. J. Vet. Behav. 7, 205–212, https://doi.org/10.1016/j.jveb.2011.10.006 (2012).

Article  Google Scholar 

Øverli, Ø. et al. Evolutionary background for stress-coping styles: relationships between physiological, behavioral, and cognitive traits in non-mammalian vertebrates. Neurosci. Biobehav. Rev. 31, 396–412, https://doi.org/10.1016/j.neubiorev.2006.10.006 (2007).

CAS  Article  PubMed  Google Scholar 

Rödel, H. G., Monclús, R. & von Holst, D. Behavioral styles in European rabbits: social interactions and responses to experimental stressors. Physiol. Behav. 89, 180–188, https://doi.org/10.1016/j.physbeh.2006.05.042 (2006).

CAS  Article  PubMed  Google Scholar 

Bubac, C. M. et al. Repeatability and reproductive consequences of boldness in female gray seals. Behav. Ecol. Sociobiol. 72, 100, https://doi.org/10.1007/s00265-018-2515-5 (2018).

Article  Google Scholar 

Shuert, C. R., Pomeroy, P. P. & Twiss, S. D. In press. Coping styles in capital breeders modulate behavioural trade-offs in time allocation: assessing fine-scale activity budgets in lactating grey seals (Halichoerus grypus) using accelerometry and heart rate variability. Behav. Ecol. Sociobiol. 74, 8, https://doi.org/10.1007/s00265-019-2783-8.

Carere, C., Caramaschi, D. & Fawcett, T. W. Covariation between personalities and individual differences in coping with stress: Converging evidence and hypotheses. Curr. Zool. 56, 728–740 (2010).

Article  Google Scholar 

Coppens, C. M., de Boer, S. F. & Koolhaas, J. M. Coping styles and behavioural flexibility: Towards underlying mechanisms. Philos. Trans. R. Soc. B 365, 4021–4028, https://doi.org/10.1098/rstb.2010.0217 (2010).

Article  Google Scholar 

Kontiainen, P. et al. Aggressive Ural owl mothers recruit more offspring. Behav. Ecol. 20, 789–796, https://doi.org/10.1093/beheco/arp062 (2009).

Article  Google Scholar 

Pomeroy, P. P., Fedak, M. A., Rothery, P. & Anderson, S. Consequences of maternal size for reproductive expenditure and pupping success of grey seals at North Rona, Scotland. J. Anim. Ecol. 68, 235–253, https://doi.org/10.1046/j.1365-2656.1999.00281.x (1999).

Article  Google Scholar 

Santicchia, F. et al. Habitat-dependent effects of personality on survival and reproduction in red squirrels. Behav. Ecol. Sociobiol. 72, 134, https://doi.org/10.1007/s00265-018-2546-y (2018).

Article  Google Scholar 

Ruiz-Gomez, M. et al. Response to environmental change in rainbow trout selected for divergent stress coping styles. Physiology and Behavior 102, 317–22, https://doi.org/10.1016/j.physbeh.2010.11.023 (2011).

CAS  Article  Google Scholar 

Boness, D. J., Anderson, S. S. & Cox, C. R. Functions of female aggression during the pupping and mating season of grey seals, Halichoerus grypus (Fabricius). Can. J Zool. 60, 2270–2278, https://doi.org/10.1139/z82-293 (1982).

Article  Google Scholar 

Anderson, S. S. & Harwood, J. Time budgets and topography – how energy reserves and terrain determine the breeding behaviour of grey seals. Anim. Behav. 33, 1343–1348, https://doi.org/10.1016/S0003-3472(85)80196-2 (1985).

Article  Google Scholar 

Twiss, S. D., Caudron, A., Pomeroy, P. P., Thomas, C. J. & Mills, J. P. Finescale topographical correlates of behavioural investment in offspring by female grey seals, Halichoerus grypus. Anim. Behav. 59, 327–338, https://doi.org/10.1006/anbe.1999.1320 (2000).

CAS  Article  PubMed  Google Scholar 

Redman, P., Pomeroy, P. P. & Twiss, S. D. Grey seal maternal attendance patterns are affected by water availability on North Rona, Scotland. Can. J. Zool. 79, 1073–1079, https://doi.org/10.1139/z01-081 (2001).

Article  Google Scholar 

Twiss, S. D., Thomas, C. J., Poland, V. F., Graves, J. A. & Pomeroy, P. P. The impact of climatic variation on the opportunity for sexual selection. Biol. Letts. 3, 12–15, https://doi.org/10.1098/rsbl.2006.0559 (2007).

Article  Google Scholar 

Stephenson, C. M., Matthiopoulos, J. & Harwood, J. Influence of the physical environment and conspecific aggression on the spatial arrangement of breeding grey seals. Ecol. Inform. 2, 308–317, https://doi.org/10.1016/j.ecoinf.2007.09.001 (2007).

Article  Google Scholar 

Stewart, J. E., Pomeroy, P. P., Duck, C. D. & Twiss, S. D. Finescale ecological niche modeling provides evidence that lactating gray seals (Halichoerus grypus) prefer access to fresh water in order to drink. Mar. Mamm. Sci. 30, 1456–72, https://doi.org/10.1111/mms.12126 (2014).

Article  Google Scholar 

Pomeroy, P. P., Anderson, S. S., Twiss, S. D. & McConnell, B. J. Dispersion and site fidelity of breeding female grey seals (Halichoerus grypus) on North Rona, Scotland. J. Zool. 233, 429–447, https://doi.org/10.1111/j.1469-7998.1994.tb05275.x (1994).

Article  Google Scholar 

Bijleveld, A. I. et al. Personality drives physiological adjustments and is not related to survival. Proc. R. Soc. B. 281, 20133135, https://doi.org/10.1098/rspb.2013.3135 (2014).

Article  PubMed  Google Scholar 

de Witt, T. J., Sih, A. & Wilson, D. S. Costs and limits of phenotypic plasticity. TREE 13, 77–91 (1998).

Google Scholar 

Ruiz-Gomez, M. D. E. L. et al. Behavioral plasticity in rainbow trout (Oncorhynchus mykiss) with divergent coping styles: When doves become hawks. Hormones and Behavior 54, 534–538, https://doi.org/10.1016/j.yhbeh.2008.05.005 (2008).

CAS  Article  Google Scholar 

Hulme, M. et al. Climate Change Scenarios for the United Kingdom: The UKCIP02 Scientific Report, Tyndall Centre for Climate Change Research, School of Environmental Sciences, University of East Anglia, Norwich, UK. 120pp (2002).

Post, E S. & Mann, M. Acceleration of phenological advance and warming with latitude over the past century. Sci. Rep. 8, https://doi.org/10.1038/s41598-018-22258-0 (2018).

Bolnick, D. I. et al. The Ecology of Individuals: Incidence and Implications of Individual Specialization. Am.Nat. 161, 1–28, https://doi.org/10.1086/343878 (2003).

MathSciNet  Article  PubMed  Google Scholar 

Violle, C. et al. The return of the variance: intraspecific variability in community ecology. TREE 27, 244–252, https://doi.org/10.1016/j.tree.2011.11.014 (2012).

Article  PubMed  Google Scholar 

Carrete, M. & Tella, J. L. Inter-Individual Variability in Fear of Humans and Relative Brain Size of the Species Are Related to Contemporary Urban Invasion in Birds. Plos One 6, e18859, https://doi.org/10.1371/journal.pone.0018859 (2011).

ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

Zidar, J. et al. A comparison of animal personality and coping styles in the red junglefowl. Anim. Behav. 130, 209–220, https://doi.org/10.1016/j.anbehav.2017.06.024 (2017).

Article  Google Scholar 

Dingemanse, N. J., Kazem, A. J. N., Réale, D. & Wright, J. Behavioural reaction norms: Animal personality meets individual plasticity. TREE 25, 81–89, https://doi.org/10.1016/j.tree.2009.07.013 (2010).

Article  PubMed  Google Scholar 

Twiss, S. D., Poland, V. F., Graves, J. A. & Pomeroy, P. P. Finding fathers: Spatio-temporal analysis of paternity assignment in grey seals (Halichoerus grypus). Mol. Ecol. 15, 1939–1953, https://doi.org/10.1111/j.1365-294X.2006.02927.x (2006).

CAS  Article  PubMed  Google Scholar 

Smout, S., King, R. & Pomeroy, P. Environment‐sensitive mass changes influence breeding frequency in a capital breeding marine top predator. J. Anim. Ecol. 00, 1–13, https://doi.org/10.1111/1365-2656.13128 (2019).

Article  Google Scholar 

Hiby, L. et al. Analysis of photo‐id data allowing for missed matches and individuals identified from opposite sides. Methods Ecol. Evol. 4, 252–259, https://doi.org/10.1111/2041-210x.12008 (2013).

Article  Google Scholar 

Bennett, K. A., Speakman, J. R., Moss, S. E. W., Pomeroy, P. P. & Fedak, M. A. Effects of mass and body composition on fasting fuel utilisation in grey seal pups (Halichoerus grypus Fabricius): an experimental study using supplementary feeding. J. Exp. Biol. 210, 3043–3053, https://doi.org/10.1242/jeb.009381 (2007).

Article  PubMed  Google Scholar 

Langton, S. D., Moss, S. E., Pomeroy, P. P. & Borer, K. E. Effect of induction dose, lactation stage and body condition on tiletamine-zolazepam anaesthesia in adult female grey seals (Halichoerus grypus) under field conditions. Vet. Rec. 168, 457, https://doi.org/10.1136/vr.d1047 (2011).

CAS  Article  PubMed  Google Scholar 

Marchant-Forde, R. M., Marlin, D. J. & Marchant-Forde, J. N. Validation of a cardiac monitor for measuring heart rate variability in adult female pigs: accuracy, artefacts and editing. Physiol. Behav. 80, 449–458 (2004).

CAS  Article  Google Scholar 

Hopster, H. & Blokhuis, H. K. Validation of a heart-rate response monitor for measuring a stress response in dairy cows. Can. J. Anim. Sci. 74, 465–474 (1994).

Article  Google Scholar 

Parker, M., Goodwin, D., Eager, R. A., Redhead, E. S. & Marlin, D. J. Comparison of Polar® heart rate interval data with simultaneously recorded ECG signals in horses. Comp. Exercise Physiol. 6, 137–142, https://doi.org/10.1017/S1755254010000024 (2010).

Article  Google Scholar 

Ille, N., Erber, R., Aurich, C. & Aurich, J. Comparison of heart rate and heart rate variability obtained by heart rate monitors and simultaneously recorded electrocardiogram signals in nonexercising horses. J. Vet. Behav. 9, 341–346, https://doi.org/10.1016/j.jveb.2014.07.006 (2014).

Article  Google Scholar 

Essner, A. et al. Comparison of Polar® RS800CX heart rate monitor and electrocardiogram for measuring inter-beat intervals in healthy dogs. Physiol. Behav. 138, 247–253, https://doi.org/10.1016/j.physbeh.2014.10.034 (2015).

CAS  Article  PubMed  Google Scholar 

Brannan, N. B. L. Investigating the physiological underpinnings of proactive and reactive behavioural types in grey seals (Halichoerus grypus): Trial deployment of a minimally invasive data logger for recording heart rate and heart rate variability in a wild free-ranging breeding pinniped species, Durham theses, Durham University. Available at Durham E-Theses Online, http://etheses.dur.ac.uk/11980/ (2017).

Berntson, G. G. et al. Heart rate variability: Origins, methods, and interpretive caveats. Psychophysiology 34, 623–648, https://doi.org/10.1111/j.1469-8986.1997.tb02140.x (1997).

CAS  Article  PubMed  Google Scholar 

Saalasti, S., Seppänen, M. & Kuusela, A. Artefact correction for heart beat interval data. In: Advanced Methods for Processing Bioelectrical Signals; 1st Probisi 2004 Proceedings. Jyväskylä, Finland: University of Jyväskylä (2004).

Martínez, C. A. G. et al. Heart Rate Variability Analysis with the R Package RHRV, Springer (2017).

Penttila, J., Helminen, A., Jartti, T. & Kuusela, T. Time domain, geometrical and frequency domain analysis of cardiac vagal outflow: effects of various respiratory patterns. Clin. Physiol. 21, 365–376, https://doi.org/10.1046/j.1365-2281.2001.00337.x (2001).

CAS  Article  PubMed  Google Scholar 

Pohlin, F. et al. Seasonal variations in heart rate variability as an indicator of stress in free-ranging pregnant Przewalski’s horses (E. ferus przewalskii) within the Hortobágy National Park in Hungary. Front. Physiol. 8, 664, https://doi.org/10.3389/fphys.2017.00664 (2017).

Article  PubMed  PubMed Central  Google Scholar 

Altmann, J. Observational study of behavior: sampling methods. Behav. 49, 227–267 (1974).

CAS  Article  Google Scholar 

Shuert, C. R., Pomeroy, P. P. & Twiss, S. D. Assessing the utility and limitations of accelerometers and machine learning approaches in classifying behaviour during lactation in a phocid seal. Anim. Biotelem. 6, 14, https://doi.org/10.1186/s40317-018-0158-y (2018).

Article  Google Scholar 

Kovacs, K. M. & Lavigne, D. Growth of grey seal (Halichoerus grypus) neonates: Differential maternal investment in the sexes. Can. J. Zool. 64, 1937–1943, https://doi.org/10.1139/z86-291 (1986).

Article  Google Scholar 

Kovacs, K. M. Maternal behaviour and early behavioural ontogeny of grey seals (Halichoerus grypus) on the Isle of May, UK. J. Zool. 213, 697–715, https://doi.org/10.1111/j.1469-7998.1987.tb03735.x (1987).

Article  Google Scholar 

Anderson, S. S. & Fedak, M. A. Grey seal, Halichoerus grypus, energetics: females invest more in male offspring. J. Zool. 211, 667–679, https://doi.org/10.1111/j.1469-7998.1987.tb04478.x (1987).

Article  Google Scholar 

Haller, M. A., Kovacs, K. & Hammill, M. O. Maternal behaviour and energy investment by grey seals (Halichoerus grypus) breeding on land-fast ice. Can. J. Zool. 74, 1531–1541, https://doi.org/10.1139/z96-167 (1996).

Article  Google Scholar 

Mellish, J. A. E., Iverson, S. J. & Bowen, W. D. Variation in milk production and lactation performance in grey seals and consequences for pup growth and weaning characteristics. Physiol. Biochem. Zool. 72, 677–90, https://doi.org/10.1086/316708 (1999).

CAS  Article  PubMed  Google Scholar 

R Core Team. 2018. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, https://www.R-project.org/.

Bell, A. M., Hankison, S. J. & Laskowski, K. L. The repeatability of behaviour: A meta-analysis. Anim. Behav. 77, 771–783, https://doi.org/10.1016/j.anbehav.2008.12.022 (2009).

Article  PubMed  PubMed Central  Google Scholar 

Nakagawa, S. & Schielzeth, H. Repeatability for Gaussian and non-Gaussian data: A practical guide for biologists. Biol. Rev. 85, 935–956, https://doi.org/10.1111/j.1469-185X.2010.00141.x (2010).

Article  PubMed  Google Scholar 

Stoffel, M. A., Nakagawa, S. & Schielzeth, H. rptR: Repeatability estimation and variance decomposition by generalized linear mixed-effects models. Methods Ecol. Evol. 8, 1639–1644, https://doi.org/10.1111/2041-210X.12797 (2017).

Article  Google Scholar 

Bates, D., Maechler, M., Bolker, B. & Walker, S. Fitting Linear Mixed-Effects Models Using lme4. J. Stat. Softw. 67, 1–48, https://doi.org/10.18637/jss.v067.i0 (2015).

Article  Google Scholar 

Bolker, B. M. et al. Generalized linear mixed models: a practical guide for ecology and evolution. TREE 24, 127–135, https://doi.org/10.1016/j.tree.2008.10.008 (2009).

Article  PubMed  Google Scholar 

Dingemanse, N. J. & Dochtermann, N. A. Quantifying individual variation in behaviour: Mixed-effect modelling approaches. J. Anim. Ecol. 82, 39–54, https://doi.org/10.1111/1365-2656.12013 (2013).

Article  PubMed  Google Scholar 

Zuur, A. F., Ieno, E. N. & Elphick, C. S. A protocol for data exploration to avoid common statistical problems. Methods Ecol. Evol. 1, 3–14, https://doi.org/10.1111/j.2041-210X.2009.00001.x (2010).

Article  Google Scholar 

Bartón, K. MuMIn: multi-model inference. R package version 1.10.0. 2014. Available online at, http://cran.r-project.org/package=MuMIn (2014).

Richards, S. A. Dealing with overdispersed count data in applied ecology. J. Appl. Ecol. 45, 218–227, https://doi.org/10.1111/j.1365-2664.2007.01377.x (2008).

Article  Google Scholar 

Richards, S. A., Whittingham, M. J. & Stephens, P. A. Model selection and model averaging in behavioural ecology: the utility of the IT-AIC framework. Behav. Ecol. Sociobiol. 65, 77–89, https://doi.org/10.1007/s00265-010-1035-8 (2011).

Article  Google Scholar 

Nakagawa, S. & Schielzeth, H. A general and simple method for obtaining R² from generalized linear mixed-effects models. Methods Ecol. Evol. 4, 133–142, https://doi.org/10.1111/j.2041-210x.2012.00261.x (2013).

Article  Google Scholar