Male reproductive strategy explains spatiotemporal segregation in brown bears

1. Spatiotemporal segregation is often explained by the risk for offspring predation or by differences in physiology, predation risk vulnerability or competitive abilities related to size dimorphism. 2. Most large carnivores are size dimorphic and offspring predation is often intraspecific and related to nonparental infanticide (NPI). NPI can be a foraging strategy, a strategy to reduce competition, or a male reproductive strategy. Spatiotemporal segregation is widespread among large carnivores, but its nature remains poorly understood. 3. We evaluated three hypotheses to explain spatiotemporal segregation in the brown bear, a size-dimorphic large carnivore in which NPI is common; the ‘NPI – foraging/competition hypothesis', i.e. NPI as a foraging strategy or a strategy to reduce competition, the ‘NPI – sexual selection hypothesis’, i.e. infanticide as a male reproductive strategy and the ‘body size hypothesis’, i.e. body-size-related differences in physiology, predation risk vulnerability or competitive ability causes spatiotemporal segregation. To test these hypotheses, we quantified spatiotemporal segregation among adult males, lone adult females and females with cubs-of-the-year, based on GPS-relocation data (2006–2010) and resource selection functions in a Scandinavian population. 4. We found that spatiotemporal segregation was strongest between females with cubs-of-the-year and adult males during the mating season. During the mating season, females with cubs-of-the-year selected their resources, in contrast to adult males, in less rugged landscapes in relative close proximity to certain human-related variables, and in more open habitat types. After the mating season, females with cubs-of-the-year markedly shifted their resource selection towards a pattern more similar to that of their conspecifics. No strong spatiotemporal segregation was apparent between females with cubs-of-the-year and conspecifics during the mating and the postmating season. 5. The ‘NPI – sexual selection hypothesis’ best explained spatiotemporal segregation in our study system. We suggest that females with cubs-of-the-year alter their resource selection to avoid infanticidal males. In species exhibiting NPI as a male reproductive strategy, female avoidance of infanticidal males is probably more common than observed or reported, and may come with a fitness cost if females trade safety for optimal resources.

[1]  D. Bates,et al.  Output Analysis and Diagnostics for MCMC , 2015 .

[2]  Stéphane Dray,et al.  Reciprocal modulation of internal and external factors determines individual movements. , 2013, The Journal of animal ecology.

[3]  A. Zedrosser,et al.  Resource selection by sympatric free-ranging dairy cattle and brown bears Ursus arctos , 2011 .

[4]  Guiming Wang,et al.  Despotism and Risk of Infanticide Influence Grizzly Bear Den-Site Selection , 2011, PloS one.

[5]  Alessandro Massolo,et al.  Human Activity Helps Prey Win the Predator-Prey Space Race , 2011, PloS one.

[6]  M. Delibes,et al.  Predators or prey? Spatio-temporal discrimination of human-derived risk by brown bears , 2011, Oecologia.

[7]  J. Nel Handbook of the Mammals of the World , 2010 .

[8]  D. Allainé,et al.  Coping with human disturbance: spatial and temporal tactics of the brown bear (Ursus arctos) , 2010 .

[9]  Navinder J. Singh,et al.  Sexual segregation in Eurasian wild sheep , 2010 .

[10]  Jarrod D. Hadfield,et al.  MCMC methods for multi-response generalized linear mixed models , 2010 .

[11]  F. Zachos Handbook of the Mammals of the World , 2009 .

[12]  Edzer J. Pebesma,et al.  Real-time automatic interpolation of ambient gamma dose rates from the Dutch radioactivity monitoring network , 2009, Comput. Geosci..

[13]  Olivier Gimenez,et al.  The magnitude and selectivity of natural and multiple anthropogenic mortality causes in hunted brown bears. , 2009, The Journal of animal ecology.

[14]  A. Zedrosser,et al.  The effects of primiparity on reproductive performance in the brown bear , 2009, Oecologia.

[15]  S. Creel,et al.  Relationships between direct predation and risk effects. , 2008, Trends in ecology & evolution.

[16]  A. Kitchener,et al.  Family Ursidae (Bears) , 2008 .

[17]  M. Main Reconciling competing ecological explanations for sexual segregation in ungulates. , 2008, Ecology.

[18]  J. Berger Fear, human shields and the redistribution of prey and predators in protected areas , 2007, Biology Letters.

[19]  K. Ruckstuhl Sexual segregation in vertebrates: proximate and ultimate causes. , 2007, Integrative and comparative biology.

[20]  J. Swenson,et al.  Importance of diel behaviour when studying habitat selection : examples from female Scandinavian brown bears (Ursus arctos) , 2007 .

[21]  M. Adamič,et al.  Brown bear body mass and growth in northern and southern Europe , 2007, Oecologia.

[22]  P. Richard,et al.  Segregation of Beaufort Sea beluga whales during the open-water season , 2006 .

[23]  K. Rode,et al.  Sexual dimorphism, reproductive strategy, and human activities determine resource use by brown bears. , 2006, Ecology.

[24]  L. Edenius,et al.  Spatial Heterogeneity and Hierarchical Feeding Habitat Selection by Reindeer , 2006 .

[25]  P. Taberlet,et al.  Mating Strategies in Relation to Sexually Selected Infanticide in a Non‐Social Carnivore: the Brown Bear , 2006 .

[26]  S. Creel,et al.  Elk alter habitat selection as an antipredator response to wolves , 2005 .

[27]  B. Mclellan Sexually selected infanticide in grizzly bears: the effects of hunting on cub survival , 2005 .

[28]  Rosie Woodroffe,et al.  People and Wildlife, Conflict or Co-existence? , 2005 .

[29]  N. Pettorelli,et al.  Using the satellite-derived NDVI to assess ecological responses to environmental change. , 2005, Trends in ecology & evolution.

[30]  A. Mysterud,et al.  Ageing and reproductive effort in male moose under variable levels of intrasexual competition , 2005 .

[31]  Owen T Nevin,et al.  Measuring the cost of risk avoidance in brown bears: further evidence of positive impacts of ecotourism. , 2005 .

[32]  Owen Nevin,et al.  Perceived risk, displacement and refuging in brown bears:positive impacts of ecotourism? , 2005 .

[33]  Burt P. Kotler,et al.  Hazardous duty pay and the foraging cost of predation , 2004 .

[34]  A. Mysterud,et al.  Patterns of reproductive effort in male ungulates , 2004 .

[35]  D. Macdonald,et al.  Promiscuous females protect their offspring. , 2004, Trends in ecology & evolution.

[36]  K. Titus,et al.  Consumption of salmon by Alaskan brown bears: a trade-off between nutritional requirements and the risk of infanticide? , 2004, Oecologia.

[37]  Jon E Swenson,et al.  Seasonal range size in relation to reproductive strategies in brown bears Ursus arctos. , 2003, The Journal of animal ecology.

[38]  David R. Anderson,et al.  Model selection and multimodel inference : a practical information-theoretic approach , 2003 .

[39]  Roger Pradel,et al.  A Proposal for a Goodness‐of‐Fit Test to the Arnason‐Schwarz Multisite Capture‐Recapture Model , 2003, Biometrics.

[40]  M. Boyce,et al.  Evaluating resource selection functions , 2002 .

[41]  S. Forbes Infanticide by males and its implications , 2002 .

[42]  J. Clobert,et al.  Estimating effects of adult male mortality on grizzly bear population growth and persistence using matrix models , 2001 .

[43]  F. Bunnell,et al.  Possible negative effects of adult male mortality on female grizzly bear reproduction , 2000 .

[44]  S. L. Lima,et al.  Temporal Variation in Danger Drives Antipredator Behavior: The Predation Risk Allocation Hypothesis , 1999, The American Naturalist.

[45]  Andrew Gelman,et al.  General methods for monitoring convergence of iterative simulations , 1998 .

[46]  S. Engen,et al.  ASSESSING THE VIABILITY OF SCANDINAVIAN BROWN BEAR, URSUS ARCTOS, POPULATIONS : THE EFFECTS OF UNCERTAIN PARAMETER ESTIMATES , 1998 .

[47]  L. Ebensperger Strategies and counterstrategies to infanticide in mammals , 1998 .

[48]  J. Craighead,et al.  The Grizzly Bears of Yellowstone: Their Ecology in the Yellowstone Ecosystem, 1959-1970 , 1997 .

[49]  J. Swenson,et al.  Infanticide caused by hunting of male bears , 1997, Nature.

[50]  S. Farley,et al.  Lactation, hibernation, and mass dynamics of American black bears and grizzly bears , 1995 .

[51]  D. Mattson,et al.  Influences of cutthroat trout (Oncorhynchus clarki) on behaviour and reproduction of Yellowstone grizzly bears (Ursus arctos), 1975 – 1989 , 1995 .

[52]  F. Bunnell,et al.  Tests of hypotheses for sexual segregation in grizzly bears , 1995 .

[53]  F. Bunnell,et al.  Sexual segregation and female grizzly bear avoidance of males , 1994 .

[54]  B. Manly,et al.  Resource selection by animals: statistical design and analysis for field studies. , 1994 .

[55]  B. L. Boeuf,et al.  Reproductive effort of male northern elephant seals: estimates from mass loss , 1990 .

[56]  T. Clutton‐Brock,et al.  Fitness costs of gestation and lactation in wild mammals , 1989, Nature.

[57]  L. Partridge,et al.  The Ecological Context of Life History Evolution , 1988, Science.

[58]  Liping Xu,et al.  [Response of maize emergence rate and yield to soil water stress in period of seeding emergence and its meteorological assessment in central area of Jilin Province]. , 1988, Ying yong sheng tai xue bao = The journal of applied ecology.

[59]  S. Hrdy,et al.  Infanticide among animals: A review, classification, and examination of the implications for the reproductive strategies of females , 1979 .

[60]  A. M. Pearson,et al.  Helminths of the grizzly bear, Ursus arctos L., in northern Canada. , 1969, Canadian journal of zoology.

[61]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[62]  A. Zedrosser,et al.  The mating system of the brown bear Ursus arctos , 2012 .

[63]  S. Steyaert The mating system of the brown bear in relation to the sexually selected infanticide theory , 2012 .

[64]  Henrik Andrén,et al.  Biomedical Protocols for Free-ranging Brown Bears, Gray Wolves, Wolverines and Lynx Editors , 2007 .

[65]  Sterling Miller,et al.  Effects of hunting on brown bear cub survival and litter size in Alaska , 2003 .

[66]  Burt P. Kotler,et al.  Ecology of fear : Foraging games between predators and prey with pulsed resources , 2001 .

[67]  Van Schaik,et al.  Infanticide by males and its implications: Vulnerability to infanticide by males: patterns among mammals , 2000 .

[68]  戎兵,et al.  ERDAS IMAGINE——遥感业界的先驱 , 1996 .

[69]  S. Stearns Trade-offs in life-history evolution , 1989 .

[70]  B. Mclellan,et al.  Grizzly bears and resource-extraction industries: effects of roads on behaviour, habitat use and demography , 1988 .