Identifying species' characteristics associated with natural population die‐offs in mammals

Extreme natural events such as cold waves, droughts, floods or hurricanes can drastically impact wildlife populations and are expected to become more frequent and more intense in the coming decades. When populations experience abnormally high declines within a short time interval due to such phenomena, the losses can be referred to as natural population die‐offs (NPDOs). Although such events have been observed and population declines have been recorded, there is currently little known about which species might be most affected. Using a database of 72 NPDOs from 31 terrestrial herbivorous mammals, we modelled the effects of four biological traits (adult body mass, foraging strategy, home‐range area and territoriality) on the degree of population loss (severity) caused by extreme natural events. We found that the susceptibility to large NPDOs decreases with increased home‐range size for a given body mass. Foraging strategy was also found to be significantly associated with NPDO severity, with grazers and mixed feeders experiencing larger declines than browsers. Our analyses moreover suggested that wide‐ranging browsers might be less susceptible to large NPDOs than browsers with small home ranges. Identifying the traits shaping high biological sensitivity and/or limited adaptive capacity to extreme natural events can help us to identify those populations most likely to become increasingly vulnerable to NPDOs, allowing tailored interventions to be implemented to avoid local extinctions. This will be of the utmost importance for those populations already experiencing high levels of anthropogenic impact and distributed in regions where exposure to extreme natural events is expected to increase in the coming decades.

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

[2]  N. Pettorelli,et al.  Assessing exposure to extreme climatic events for terrestrial mammals , 2013 .

[3]  Mabelle Chedid,et al.  Water Stress in Small Ruminants , 2013 .

[4]  N. Pettorelli,et al.  Reassessing the Determinants of Breeding Synchrony in Ungulates , 2012, PloS one.

[5]  Guy Cowlishaw,et al.  Natural population die-offs: causes and consequences for terrestrial mammals. , 2012, Trends in ecology & evolution.

[6]  P. Leadley,et al.  Impacts of climate change on the future of biodiversity. , 2012, Ecology letters.

[7]  T. Stocker,et al.  Managing the Risks of Extreme Events and Disasters to Advance Climate Change Adaptation. A Special Report of Working Groups I and II of IPCC Intergovernmental Panel on Climate Change , 2012 .

[8]  Ben Collen,et al.  Predicting how populations decline to extinction , 2011, Philosophical Transactions of the Royal Society B: Biological Sciences.

[9]  R. Freckleton,et al.  Comparative Methods as a Statistical Fix: The Dangers of Ignoring an Evolutionary Model , 2011, The American Naturalist.

[10]  F. Jiguet,et al.  Community responses to extreme climatic conditions , 2011 .

[11]  G. Mace,et al.  Beyond Predictions: Biodiversity Conservation in a Changing Climate , 2011, Science.

[12]  D. Nyariki,et al.  The perfect drought? Constraints limiting Kalahari agro-pastoral communities from coping and adapting , 2011 .

[13]  M. Uriarte,et al.  Anthropogenic and environmental drivers of modern range loss in large mammals , 2011, Proceedings of the National Academy of Sciences.

[14]  Andy Purvis,et al.  Selectivity in Mammalian Extinction Risk and Threat Types: a New Measure of Phylogenetic Signal Strength in Binary Traits , 2010, Conservation biology : the journal of the Society for Conservation Biology.

[15]  J. Lamarque,et al.  Global Biodiversity: Indicators of Recent Declines , 2010, Science.

[16]  Tim Hirsch,et al.  Global biodiversity outlook 3 , 2010 .

[17]  Clinton N. Jenkins,et al.  Extinctions and the practice of preventing them , 2010 .

[18]  Paul R. Ehrlich,et al.  The Sixth Extinction Crisis Loss of Animal Populations and Species , 2010 .

[19]  Kate E. Jones,et al.  PanTHERIA: a species‐level database of life history, ecology, and geography of extant and recently extinct mammals , 2009 .

[20]  F. Geiser,et al.  Hibernation and daily torpor minimize mammalian extinctions , 2009, Naturwissenschaften.

[21]  James H Brown,et al.  Multiple ecological pathways to extinction in mammals , 2009, Proceedings of the National Academy of Sciences.

[22]  Susanne A. Fritz,et al.  Geographical variation in predictors of mammalian extinction risk: big is bad, but only in the tropics. , 2009, Ecology letters.

[23]  N. Cooper,et al.  Modelling extinction risk in multispecies data sets: phylogenetically independent contrasts versus decision trees , 2009, Biodiversity and Conservation.

[24]  Heikki Mannila,et al.  Lower Extinction Risk in Sleep‐or‐Hide Mammals , 2008, The American Naturalist.

[25]  A. Purvis Phylogenetic Approaches to the Study of Extinction , 2008 .

[26]  Kate E. Jones,et al.  The predictability of extinction: biological and external correlates of decline in mammals , 2008, Proceedings of the Royal Society B: Biological Sciences.

[27]  G. Mace,et al.  SPECIES SUSCEPTIBILITY TO CLIMATE CHANGE IMPACTS , 2008 .

[28]  Luke J. Harmon,et al.  GEIGER: investigating evolutionary radiations , 2008, Bioinform..

[29]  R. G. Davies,et al.  Methods to account for spatial autocorrelation in the analysis of species distributional data : a review , 2007 .

[30]  T. Waite,et al.  Sanctuary in the City: Urban Monkeys Buffered against Catastrophic Die-off during ENSO-related Drought , 2007, EcoHealth.

[31]  J. L. Gittleman,et al.  Hunting to extinction: biology and regional economy influence extinction risk and the impact of hunting in artiodactyls , 2007, Proceedings of the Royal Society B: Biological Sciences.

[32]  Barbara R. Holland,et al.  Analysis of Phylogenetics and Evolution with R , 2007 .

[33]  Kate E. Jones,et al.  The delayed rise of present-day mammals , 1990, Nature.

[34]  Michael J. Crawley,et al.  The R book , 2022 .

[35]  J. Lee-Thorp,et al.  Nutritional content of savanna plant foods: implications for browser/grazer models of ungulate diversification , 2007, European Journal of Wildlife Research.

[36]  L. Tejera,et al.  Unusual mass mortality of feral horses during a violent rainstorm in Parque Provincial Tornquist, Argentina , 2006 .

[37]  R. G. Davies,et al.  Human impacts and the global distribution of extinction risk , 2006, Proceedings of the Royal Society B: Biological Sciences.

[38]  J. L. Gittleman,et al.  Latent extinction risk and the future battlegrounds of mammal conservation. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[39]  A. Jentsch Extreme climatic events in ecological research , 2006 .

[40]  C. Bradshaw,et al.  The devil in the (demographic) detail (Letter to the editor) , 2006 .

[41]  Kate E. Jones,et al.  Multiple Causes of High Extinction Risk in Large Mammal Species , 2005, Science.

[42]  Robert S. Chen,et al.  Natural Disaster Hotspots: A Global Risk Analysis , 2005 .

[43]  Millenium Ecosystem Assessment Ecosystems and human well-being: synthesis , 2005 .

[44]  Richard M. Heiberger,et al.  Statistical Analysis and Data Display: An Intermediate Course with Examples in S-Plus, R, and SAS , 2004 .

[45]  G. Cowlishaw,et al.  How species respond to multiple extinction threats , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[46]  Aaron M. Ellison,et al.  A Primer of Ecological Statistics , 2004 .

[47]  O. Phillips,et al.  Extinction risk from climate change , 2004, Nature.

[48]  N. Owen‐Smith,et al.  Foliage acceptability to browsing ruminants in relation to seasonal changes in the leaf chemistry of woody plants in a South African savanna , 1988, Oecologia.

[49]  Richard M. Heiberger,et al.  Statistical Analysis and Data Display , 2004 .

[50]  Simon P Blomberg,et al.  Extrinsic versus intrinsic factors in the decline and extinction of Australian marsupials , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[51]  E. F. Robertson,et al.  Population decline of tsessebe antelope (Damaliscus lunatus lunatus) on a mixed cattle and wildlife ranch in Zimbabwe , 2003 .

[52]  G. Daily,et al.  Population diversity and ecosystem services , 2003 .

[53]  D. H. Reed,et al.  The frequency and severity of catastrophic die‐offs in vertebrates , 2003 .

[54]  Kate E. Jones,et al.  Biological Correlates of Extinction Risk in Bats , 2003, The American Naturalist.

[55]  M. Pagel,et al.  Phylogenetic Analysis and Comparative Data: A Test and Review of Evidence , 2002, The American Naturalist.

[56]  B. Simmen,et al.  A major increase in the population of brown lemurs on Mayotte since the decline reported in 1987 , 2002, Oryx.

[57]  John F. McLaughlin,et al.  Climate change hastens population extinctions , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[58]  F J Rohlf,et al.  COMPARATIVE METHODS FOR THE ANALYSIS OF CONTINUOUS VARIABLES: GEOMETRIC INTERPRETATIONS , 2001, Evolution; international journal of organic evolution.

[59]  I. Gordon,et al.  Relationships between oral morphology and feeding style in the Ungulata: a phylogenetically controlled evaluation , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[60]  W. Ekaya Nutritional Characteristics of Selected Grass and Browse Species From Kenya’s Pastoral Ecosystems , 2001 .

[61]  Tim K. Keyes,et al.  Applied Regression Analysis and Multivariable Methods , 2001, Technometrics.

[62]  L. Shipley Grazers and Browsers : How Digestive Morphology Affects Diet Selection , 2001 .

[63]  J. L. Gittleman,et al.  Predicting extinction risk in declining species , 2000, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[64]  G. Meehl,et al.  Climate extremes: observations, modeling, and impacts. , 2000, Science.

[65]  J. Leeuw,et al.  Population trends of large non‐migratory wild herbivores and livestock in the Masai Mara ecosystem, Kenya, between 1977 and 1997 , 2000 .

[66]  I. Owens,et al.  Quantifying Biodiversity: a Phenotypic Perspective , 2000 .

[67]  M. Pagel Inferring the historical patterns of biological evolution , 1999, Nature.

[68]  Michael M. McKinney,et al.  Present and Future Taxonomic Selectivity in Bird and Mammal Extinctions , 1998 .

[69]  H. Mooney,et al.  Human Domination of Earth’s Ecosystems , 1997, Renewable Energy.

[70]  T. F. Hansen,et al.  Phylogenies and the Comparative Method: A General Approach to Incorporating Phylogenetic Information into the Analysis of Interspecific Data , 1997, The American Naturalist.

[71]  T. Young Natural Die‐Offs of Large Mammals: Implications for Conservation , 1994 .

[72]  M. Pagel,et al.  The comparative method in evolutionary biology , 1991 .

[73]  G. Haynes Mass deaths and serial predation: Comparative taphonomic studies of modern large mammal death sites , 1988 .

[74]  R. Lande,et al.  Extinction Thresholds in Demographic Models of Territorial Populations , 1987, The American Naturalist.

[75]  N. Owen‐Smith,et al.  PALATABILITY OF WOODY PLANTS TO BROWSING RUMINANTS IN A SOUTH AFRICAN SAVANNA , 1987 .

[76]  T. Struhsaker A Further Decline in Numbers of Amboseli Vervet Monkeys , 1976 .

[77]  R. Nowak,et al.  Walker's mammals of the world , 1968 .