Abstract
Why are some mammals more vulnerable to extinction than others? Past studies have explored many life history traits as correlates of extinction, but have not been successful at developing a unified understanding of why some species become extinct while other species persist despite living at the same time, under similar conditions, and facing equivalent challenges. I propose that the lens of wildlife behavior may bring into focus a more comprehensive view of why some species have gone extinct while others persist. The fossil record has recorded extinction events over carnivoran history; unfortunately, behavior is not well recorded in the fossil record. As a proxy for behavior, I examine relative encephalization (RE), brain size after controlling for body mass and phylogeny, as it has been found to be biologically relevant in understanding a wide variety of animal behavioral traits. I focus on the data-rich order Carnivora for which there are comprehensive data on brain size and extinction between 40 and 0.012 million years ago. I use Cox proportional-hazards models to assess the role that RE and body size have played on extinction risk for 224 species in the order Carnivora that existed between 40 and 0.012 million years ago. I show generally that carnivoran species with reduced RE had higher relative risks of extinction. Additionally, I find an interaction between RE and body size such that RE had the largest effects on relative extinction risk in the smallest-bodied species. These results suggest that RE is important for understanding extinction risk in Carnivora over geologic time frames.
This is a preview of subscription content, log in via an institution to check access.
Artwork credit: Michael Abelson
Similar content being viewed by others
References
Abelson ES (2016) Brain size is correlated with endangerment status in mammals. Proc R Soc B 283:20152772. https://doi.org/10.1098/rspb.2015.2772
Aiello LC (1997) Brains and guts in human evolution: the expensive tissue hypothesis. Braz J Genet. https://doi.org/10.1590/S0100-84551997000100023
Amiel JJ, Tingley R, Shine R (2011) Smart moves: effects of relative brain size on establishment success of invasive amphibians and reptiles. PLoS One 6:e18277. https://doi.org/10.1371/journal.pone.0018277
Barnosky AD, Matzke N, Tomiya S et al (2011) Has the earth’s sixth mass extinction already arrived? Nature 471:51–57. https://doi.org/10.1038/nature09678
Benson-Amram S, Dantzer B, Stricker G et al (2016) Brain size predicts problem-solving ability in mammalian carnivores. Proc Natl Acad Sci USA 113:2532–2537. https://doi.org/10.1073/pnas.1505913113
Byrne RW, Corp N (2004) Neocortex size predicts deception rate in primates. Proc Biol Sci 271:1693–1699. https://doi.org/10.1098/rspb.2004.2780
Cardillo M, Mace GM, Jones KE et al (2005) Multiple causes of high extinction risk in large mammal species. Science 309:1239–1241. https://doi.org/10.1126/science.1116030
Cardillo M, Mace GM, Gittleman JL et al (2008) The predictability of extinction: biological and external correlates of decline in mammals. Proc R Soc B 275:1441–1448. https://doi.org/10.1098/rspb.2008.0179
Ceballos G, Ehrlich PR, Barnosky AD et al (2015) Accelerated modern human-induced species losses: entering the sixth mass extinction. Sci Adv 1:e1400253. https://doi.org/10.1126/sciadv.1400253
Clark KE, Applegate JE, Niles LJ, Dobkin DS (2006) An objective means of species status assessment: adapting the Delphi technique. Wildl Soc Bull 34:419–425. https://doi.org/10.2193/0091-7648(2006)34%5b419:aomoss%5d2.0.co;2
Cox DR (2018) Analysis of survival data. Routledge, Abingdon
Crozier RH, Dunnett LJ, Agapow P-M (2005) Phylogenetic biodiversity assessment based on systematic nomenclature. Evol Bioinform 1:11–36
Curio E (1996) Conservation needs ethologv. Trends Ecol Evol 11:260–263. https://doi.org/10.1016/0169-5347(96)20046-1
Davidson AD, Hamilton MJ, Boyer AG et al (2009) Multiple ecological pathways to extinction in mammals. Proc Natl Acad Sci USA 106:10702–10705. https://doi.org/10.1073/pnas.0901956106
Dirzo R, Raven PH (2003) Global state of biodiversity and loss. Annu Rev Environ Resour 28:137–167. https://doi.org/10.1146/annurev.energy.28.050302.105532
Ehrlich PR, Blumstein DT (2018) The great mismatch. Bioscience 68:844–846. https://doi.org/10.1093/biosci/biy110
Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125:1–15
Festa-Bianchet M, Apollonio M (2003) Animal behavior and wildlife conservation. Island Press, Washington, DC
Finarelli JA, Flynn JJ (2007) The evolution of encephalization in caniform carnivorans. Evolution 61:1758–1772. https://doi.org/10.1111/j.1558-5646.2007.00131.x
Finarelli JA, Flynn JJ (2009) Brain-size evolution and sociality in Carnivora. Proc Natl Acad Sci USA 106:9345–9349. https://doi.org/10.1073/pnas.0901780106
Garland T, Harvey PH, Ives AR (1992) Procedures for the analysis of comparative data using phylogenetically independent contrasts. Syst Biol 41:18–32. https://doi.org/10.2307/2992503
González-Lagos C, Sol D, Reader SM (2010) Large-brained mammals live longer. J Evol Biol 23:1064–1074. https://doi.org/10.1111/j.1420-9101.2010.01976.x
Green DM (2005) Designatable units for status assessment of endangered species. Conserv Biol 19:1813–1820. https://doi.org/10.1111/j.1523-1739.2005.00284.x
Griffin AS, Blumstein DT, Evans CS (2000) Training captive-bred or translocated animals to avoid predators. Conserv Biol 14:1317–1326. https://doi.org/10.1046/j.1523-1739.2000.99326.x
Holway DA, Suarez AV (1999) Animal behavior: an essential component of invasion biology. Trends Ecol Evol 14:328–330. https://doi.org/10.1016/S0169-5347(99)01636-5
IUCN 2019 IUCN Red List of Threatened Species. Version 2019-1. https://www.iucnredlist.org/en. Accessed 26 Mar 2019
Jerison HJ (1973) Evolution of the brain and intelligence. Academic Press, New York
Kotrschal A, Rogell B, Bundsen A et al (2013) Artificial selection on relative brain size in the guppy reveals costs and benefits of evolving a larger brain. Curr Biol 23:168–171. https://doi.org/10.1016/j.cub.2012.11.058
Kumar D, Klefsjö B (1994) Proportional hazards model: a review. Reliab Eng Syst Saf 44:177–188. https://doi.org/10.1016/0951-8320(94)90010-8
Laughlin SB, van Steveninck RR, Anderson JC (1998) The metabolic cost of neural information. Nat Neurosci 1:36–41. https://doi.org/10.1038/236
Leadley P (2010) Biodiversity scenarios: projections of 21st century change in biodiversity and associated ecosystem services: a technical report for the global biodiversity outlook 3. Renouf Publishing Company Limited, Ottawa
MacFadden BJ (1990) Body size in mammalian paleobiology: estimation and biological implications. Cambridge University Press, Cambridge
Maklakov AA, Immler S, Gonzalez-Voyer A et al (2011) Brains and the city: big-brained passerine birds succeed in urban environments. Biol Lett. https://doi.org/10.1098/rsbl.2011.0341
McKinney ML (1997) Extinction vulnerability and selectivity: combining ecological and paleontological views. Annu Rev Ecol Syst 28:495–516
Miner BG, Sultan SE, Morgan SG et al (2005) Ecological consequences of phenotypic plasticity. Trends Ecol Evol 20:685–692. https://doi.org/10.1016/j.tree.2005.08.002
Nesse RM, Williams GC (1998) Evolution and the origins of disease. Sci Am 279:86–93. https://doi.org/10.1038/scientificamerican1198-86
Niven JE, Laughlin SB (2008) Energy limitation as a selective pressure on the evolution of sensory systems. J Exp Biol 211:1792–1804. https://doi.org/10.1242/jeb.017574
O’Grady JJ, Reed DH, Brook BW, Frankham R (2004) What are the best correlates of predicted extinction risk? Biol Conserv 118:513–520. https://doi.org/10.1016/j.biocon.2003.10.002
Paradis E, Blomberg S, Bolker B et al (2018) Ape: analyses of phylogenetics and evolution. R package version 5.2. https://CRAN.R-project.org/package=ape
R Core Team, R Foundation for Statistical Computing (2019) R 3.5.3: a language and environment for statistical computing. Vienna, Austria
Ratcliffe JM, Fenton MB, Shettleworth SJ (2006) Behavioral flexibility positively correlated with relative brain volume in predatory bats. Brain Behav Evol 67:165–176. https://doi.org/10.1159/000090980
Reader SM, Laland KN (2002) Social intelligence, innovation, and enhanced brain size in primates. Proc Natl Acad Sci USA 99:4436–4441. https://doi.org/10.1073/pnas.062041299
Revell LJ (2009) Size-correction and principal components for interspecific comparative studies. Evolution 63:3258–3268. https://doi.org/10.1111/j.1558-5646.2009.00804.x
Revell LJ (2012) phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol Evol 3:217–223. https://doi.org/10.1111/j.2041-210X.2011.00169.x
Revell LJ (2018) Phytools: phylogenetic tools for comparative biology (and other things). R package version 0.6-60. http://CRAN.R-project.org/package=phytools
Ricotta C, Bacaro G, Marignani M et al (2012) Computing diversity from dated phylogenies and taxonomic hierarchies: does it make a difference to the conclusions? Oecologia 170:501–506. https://doi.org/10.1007/s00442-012-2318-8
Russell GJ, Brooks TM, McKinney MM, Anderson CG (1998) Present and future taxonomic selectivity in bird and mammal extinctions. Conserv Biol 12:1365–1376. https://doi.org/10.1111/j.1523-1739.1998.96332.x
Schuck-Paim C, Alonso WJ, Ottoni EB (2008) Cognition in an ever-changing world: climatic variability is associated with brain size in neotropical parrots. Brain Behav Evol 71:200–215. https://doi.org/10.1159/000119710
Shumway CA (1999) A neglected science: applying behavior to aquatic conservation. Environ Biol Fish 55:183–201. https://doi.org/10.1023/A:1007562023150
Sol D (2009a) The cognitive-buffer hypothesis for the evolution of large brains. Cogn Ecol II:111–134
Sol D (2009b) Revisiting the cognitive buffer hypothesis for the evolution of large brains. Biol Lett 5:130–133. https://doi.org/10.1098/rsbl.2008.0621
Sol D, Lefebvre L, Rodríguez-Teijeiro JD (2005) Brain size, innovative propensity and migratory behaviour in temperate Palaearctic birds. Proc R Soc B 272:1433–1441. https://doi.org/10.1098/rspb.2005.3099
Sol D, Bacher S, Reader SM, Lefebvre L (2008) Brain size predicts the success of mammal species introduced into novel environments. Am Nat 172(Suppl 1):S63–S71. https://doi.org/10.1086/588304
Tear TH, Scott JM, Hayward PH, Griffith B (1993) Status and prospects for success of the endangered species act: a look at recovery plans. Science 262:976–977. https://doi.org/10.1126/science.262.5136.976
Terborgh J (1974) Preservation of natural diversity: the problem of extinction prone species. Bioscience 24:715–722. https://doi.org/10.2307/1297090
The Paleobiology Database (2012) The paleobiology database. http://paleodb.org/cgi-bin/bridge.pl. Accessed 13 May 2012
Therneau TM, Lumley T (2018) Survival: survival analysis. R package version 2.43-3. https://CRAN.R-project.org/package=survival
U.S. Fish and Wildlife Service (1973) Endangered Species Act of 1973. Public Law 93-205-Dec 28, 1973, Statutes at large: 87 Stat. 884. https://en.wikipedia.org/wiki/Endangered_Species_Act_of_1973
van der Bijl W, Thyselius M, Kotrschal A, Kolm N (2015) Brain size affects the behavioural response to predators in female guppies (Poecilia reticulata). Proc R Soc B 282:20151132. https://doi.org/10.1098/rspb.2015.1132
Wilcove DS, Master LL (2005) How many endangered species are there in the United States? Front Ecol Evol 3:414–420. https://doi.org/10.1890/1540-9295(2005)003%5b0414:hmesat%5d2.0.co;2
Acknowledgements
I thank Rodolfo Dirzo, Lucia Jacobs, Deborah Gordon, Gretchen Daily, Amelia Wolf, Maria del Mar Sobral Bernal, Noah Simon, Reuben Youngblom, Stuart Abelson, Minh Chau N. Ho, Erin Kurten, Jonathan Payne, Rachel Vannette, Susumu Tomiya, Leonid Pekelis, Kristen Malinak, and George Michopoulos, for project discussion, manuscript review, and assistance on data processing. I thank Michael Abelson for his artwork in figure two. I also thank J. Finarelli and J. Flynn for collecting and making available brain size and body size used in this study (from their 2009 publication titled “Brain-size evolution and sociality in Carnivora”) and to those who worked to make the Paleobiology Database available and an incredible resource. I am appreciative of the patient and detailed review of this manuscript by Joerg Ganzhorn along with insightful comments from three anonymous reviewers.
Funding
This study was funded by the National Science Foundation Grant #1110332.
Author information
Authors and Affiliations
Contributions
ESA conceived, designed, and executed this study and wrote the manuscript. No other person is entitled to authorship.
Corresponding author
Ethics declarations
Conflict of interest
The author declares that there is no conflict of interest.
Additional information
Communicated by Jörg U. Ganzhorn.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Abelson, E.S. Big brains reduce extinction risk in Carnivora. Oecologia 191, 721–729 (2019). https://doi.org/10.1007/s00442-019-04527-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-019-04527-5