Abstract
Human activities have led to global changes with direct consequences for biodiversity. For this reason, special concerns have arisen, particularly in respect to global threats such as habitat loss and fragmentation, because they decrease population size, promote the loss of species genetic diversity, contract species geographical distribution and facilitate species loss. Interest in the genetic consequences related to habitat changes has increased in the last decades, so it became crucial to understand how genetic diversity changes due to habitat loss and fragmentation and if the degree of genetic losses is related with species traits. Thus, we conduct a metaanalysis to test if genetic diversity of mammalian populations that live in fragments is lower than those living in continuous habitats and we also explore which species traits could be related with the observed patterns. Through this metaanalysis we detected an overall decrease in allelic diversity, allelic richness, observed heterozygosity and expected heterozygosity in mammalian species that live in situations of high habitat fragmentation. However, not all species are affected the same way. We found that species with larger body mass are the most negatively affected by fragmentation; terrestrial and arboreal mammals are more negatively affected than flying species; herbivores suffer consistent negative effect of fragmentation in the four genetic measures analysed; and forestdependent species are the most susceptible to the negative effects of fragmentation. We expected to detect an increase in inbreeding coefficients in fragments when compared to continuous habitats; however, this pattern did not arise, probably because time since fragmentation was not enough and/or species have ways to avoid inbreeding. The patterns here described allow a better understanding of which mammalian species are more susceptible to the negative effects of habitat loss and fragmentation, potentially giving support for the conservation and management of their populations.
Similar content being viewed by others
References
Aguilar, R., Quesada, M., Ashworth, L., Herrerias, D., Lobo, J., 2008. Genetic consequences of habitat fragmentation in plant populations: susceptible signals in plant traits and methodological approaches. Mol. Ecol. 17, 5177–5188.
Arroyo-Rodríguez, V., Mandujano, S., 2006. Forest fragmentation modifles habitat quality for Alouatta palliata. Int.J. Primatol. 27, 1079–1096.
Athrey, G., Barr, K.R., Laňce, R.F., Leberg, P.L., 2012. Birds in space and time: genetic changes accompanying anthropogenic habitat fragmentation in the endangered blackcapped vireo (Vireo atricapiiia). Evol. Appl. 5, 540–552.
Batáry, P., Báldi, A., 2004. Evidence of an edge effect on avian nést success. Conserv. Biol. 18, 389–400.
Biedermann, R., 2003. Body size and areaincidence relationships: is there a general pattern? Glob. Ecol. Biogeogr. 12, 381–387.
Blackburn, T.M., Gaston, K.J., 1999. The relationship between animal abundance and body size: a review of the mechanisms. Adv. Ecol. Res. 28, 181–210.
Cockburn, A., Scott, M., Scotts, D., 1985. Inbreeding avoidance and malebiased natal dispersal in Antechinus spp. (Marsupialia: Dasyuridae). Anim. Behav. 33, 908–915.
Crooks, K.R., 2002. Relative sensitivities of mammalian carnivores to habitat fragmentation. Conserv. Biol. 16, 488–502.
Didham, R.K., Kapos, V., Ewers, R.M., 2012. Rethinkingthe conceptual foundations of habitat fragmentation research. Oikos 121, 161–170.
Dietz, G., Dahabreh, I.J., Gurevitch, J., Lajeunesse, M.J., Schmid, C.H., Trikalinos, T.A., Wallace, B.C., 2014. Open-MEE: Software for Ecological and Evolutionary MetaAnalysis.
Driscoll, D.A., Banks, S.C., Bartoň, P.S., Lindenmayer, D.B., Smith, A.L., 2013. Conceptual domain of the matrix in fragmented landscapes. Trends Ecol. Evol. 28, 605–613.
Dutta, T., Sharma, S., Maldonado, J.E., Wood, T.C., Panwar, H.S., Seidensticker, J., 2013. Gene flow and demographic history of leopards (Panthera pardus) in the centrál Indián highlands. Evol. Appl. 6, 949–959.
Egger, M., Davey Smith, G., Schneider, M., Minder, C., 1997. Bias in metaanalysis detected by a simple, graphical test. Br. Med. J. 315, 629–634.
Ewers, R.M., Didham, R.K., 2006. Confounding factors in the detection of species responsesto habitat fragmentation. Biol. Rev. Camb. Philos. Soc. 81, 117–142.
Fahrig, L., 2003. Effects of habitat fragmentation on biodiversity. Annu. Rev. Ecol. Evol. Syst. 34, 487–515.
Frankham, R., 1996. Relationship of genetic to population relationship variation size in wildlife. Conserv. Biol. 10, 1500–1508.
Gibbs. J.P., 2001. Demography versus habitat fragmentation as determinants of genetic variation inwild populations. Biol. Conserv. 100, 15–20.
Gurevitch, J., Hedges, L.V., 2001. Metaanalysis: combining the results of independent experiments. In: Scheiner, S.M., Gurevitch, J. (Eds.), Design and Analysis of Ecological Experiments. Oxford University Press, oxford, pp. 347–369.
Hanski, I., 2015. Habitat fragmentation and species richness. J. Biogeogr. 42, 989–994.
Harris, R.J., Reed, J.M., 2002. Behavioral barriers to nonmigratory movements of birds. Ann. Zool. Fennici 39, 275–290.
Harrison, F., 2011.Gettingstarted with metaanalysis. Methods Ecol. Evol. 2, 1–10.
Henle, K., Davies, K.F., Kleyer, M., Margules, C., Settele, J., 2004. Predictors of species sensitivity to fragmentation. Biodivers. Conserv. 13, 207–251.
Hoglund, J., 2009. Evolutionary Conservation Genetics. Oxford University Press, New York.
Honnay, O., Jacquemyn, H., 2007. Susceptibility of common and rare plant species to tne genetic consequences of habitat fragmentation. Conserv. Biol. 21, 823–831.
IUCN, 2017. IUCN List Threat. Species, www.iucnredlist.org/.
Joricheva, J., Gurevitch. J., Mengersen, K., 2013. Handbook of MetaAnalysis in Ecology and Evolution. Princeton University Press, Princeton and Oxford.
Keyghobadi, N., 2007. The genetic implications of habitat fragmentation for animals. Can. J. Zool. 85, 1049–1064.
Koskimaki, J., Huitu, O., Kotiaho, J.S., Lampila, S., Makela, A., Sulkava, R., Monkkonen, M., 2014. Are habitat loss, predation risk and climate related to the drastic decline in a Siberian flying squirrel population? A 15-year study. Popul. Ecol. 56, 341–348.
Lancaster, M.L., Cooper, S.J.B., Carthew, S.M., 2016. Genetic consequences of forest fragmentation by agricultural land in an arboreal marsupial. Landsc. Ecol. 31, 655–667.
Lindenmayer, D., Fischer, J., 2006. Tackling the habitat fragmentation panchreston. Trends Ecol. Evol. 22, 127–132.
MacArthur, R.H., Wilson, E.O., 1967. The Theory of Island Biogeography. Princeton University Press, Princeton.
Mills, L.S., 1995. Edge effects and isolation: redbacked voles on forest remnants. Conserv. Biol. 9, 395–403.
Montgelard, C., Zenboudji, S., Ferchaud, A.L., Arnal, V., Vuuren, B.J., van, 2014. Landscape genetics in mammals. Mammalia 78, 139–157.
Morrison, J.C, Sechrest, W., Dinerstein, E., Wilcove, D.S., Lamoreux, J.F., 2007. Persistence of large mammal faunas as indicators of globál human impacts. J. Mammal. 88, 1363–1380.
Murphy, G.E.P., Romanuk, T.N., 2014. A metaanalysis of declines in local species richness from human disturbances. Ecol. Evol. 4, 91–103.
Pabijan, M., Wollenberg, K.C., Vences, M., 2012. Small body size increases the regional differentiation of populations of tropical mantellid frogs (Anura: Mantellidae). J. Evol. Biol. 25, 2310–2324.
Parr, L., Heintz, M., Lonsdorf, E., Wroblewski, E., 2010. Visual kin recognition in nonhuman primates (Pan troglodytes and Macaca muiatta): inbreeding avoidance or male distinctiveness? J. Comp. Psychol. 124, 343–350.
Peakall, R., Ruibal, M., Lindenmayer, D.B., 2003. Spatial autocorrelation analysis offers new insights into gene flow in the Australian bush rat, Rattus fusápes. Evolution 57, 1182–1195.
Potter, S., Eldridge, M.D.B., Cooper, S.J.B., Paplinska, J.Z., Taggart, D.A., 2012. Habitat connectivity, more than species’ biology, influences genetic differentiation in a habitat specialist, the shorteared rockwallaby (Petrogale brachyotis). Conserv. Genet. 13, 937–952.
Prevedello, J.A., Vieira, M.V., 2010. Does the type of matrix matter? A quantitative review of the evidence. Biodivers. Conserv. 19, 1205–1223.
Prugh, LR., Hodges, K.E., Sinclair, A.R.E., Brashares, J.S., 2008. Effect of habitat area and isolation on fragmented animal populations. Proč. Nati. Acad. Sci. U. S. A. 105, 20770–20775.
Purvis, A., Gittleman, J.L., Cowlishaw, G., Mace, G.M., 2000. Predicting extinction risk in declining species. Proč. Biol. Sci. 267, 1947–1952.
Püttker, T., Meyer-Lucht, Y., Sommer, S., 2008. Fragmentation effects on population density of three rodent species in secondary Atlantic Rainforest, Brazil. Stud. Neotrop. Fauna Environ. 43, 11–18.
Quesnelle, P.E., Lindsay, K.E., Fahrig, L., 2014. Low reproductive rate predicts species sensitivity to habitat loss: a metaanalysis of wetland vertebrates. PLoS One 9, e90926.
Quin, D.G., Riek, A., Green, S., Smith, A.P., Geiser, F., 2010. Seasonally constant fleld metabolic rates in freeranging sugargliders (Petaurus breviceps). Comp. Biochem. Physiol. A: Mol. Integr. Physiol. 155, 336–340.
R Core Team, 2013. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
Reis, N.R., Peracchi, A.L, Pedro, W.A., Lima, I.P., 2006. Mamíferos do Brasil, 2nd ed. Universidade Estadual de Londrina, Londrina and Brazil.
Rendall, D., Rodman, P.S., Emond, R.E., 1996. Vocal recognition of individuals and kin in freeranging Rhesus monkeys. Anim. Behav. 51, 1007–1015.
RevMan, 2014. Copenhagen: The Nordic Cochrane Centre, The Cochrane Collaboration, Version 5.3.
Rosenberg, M.S., 2005. The filedrawer problém revisited: a generál weighted method for calculating failsafe numbers in metaanalysis. Evolution 59, 464–468.
Rosenthal, R., 1979. The “filé drawer problém” and tolerance for null results. Psychol. Bull. 86, 638–641.
Sanderson, E.W., Redford, K.H., Chetkiewicz, C.L.B., Medellin, R.A., Rabinowitz, A.R., Robinson, J.G., Taber, A.B., 2002. Planning to savé a species: the jaguár as a model. Conserv. Biol. 16, 58–72.
Strahan, R., 1983. The Australian Museum Complete Book of Australian Mammals. Angus & Robertson Publishers, Sydney, Australia.
Struebig, M.J., Kingston, T., Petit, E.J., Le Comber, S.C., Zubaid, A., Mohd-Adnan, A., Rossiter, S.J., 2011. Parallel declines in species and genetic diversity in tropical forest fragments. Ecol. Lett. 14, 582–590.
Swihart, R.K., Gehring, T.M., Kolozsvary, M.B., Nupp, T.E., 2003. Responses of “resistant” vertebrates to habitat loss and fragmentation: the importance of niche breadth and range boundaries. Divers. Distrib. 9, 1–18.
Thornton, D.H., Branch, L.I., Sunquist, M.E., 2011. The relative influence of habitat loss and fragmentation: do tropical mammals meet the temperate paradigm? Ecol. Appl. 21, 2324–2333.
Tucker, M.A., Bohninggaese, K., Fagan, W.F., Fryxell, J.M., Van Moorter, B., Alberts, S.C., Ali, A.H., Allen, A.M., Attias, N., Avgar, T., Bartlambrooks, H., Bayarbaatar, B., Belant, J.L, Bertassoni, A., Beyer, D., Bidner, L., Van Beest, F.M., Blake, S., Blaum, N., Bracis, C., Brown, D., De Bruyn, P.J.N., Cagnacci, F., Diefenbach, D., Douglashamilton, L., Fennessy, J., Fichtel, C., Fiedler, W., Fischer, C., Fischhoff, I., Fleming, C.H., Ford, A.T., Fritz, S.A., Gehr, B., Goheen, J.R., Gurarie, E., Hebblewhite, M., Heurich, M., Hewison, A.J.M., Hof, C., Hurme, E., Isbell, L.A., Janssen, R., Jeltsch, F., Kaczensky, P., Kane, A., Kappeler, P.M., Kauffman, M., Kays, R., Kimuyu, D., Koch, F., Kranstauber, B., Lapoint, S., Mattisson, J., Medici, E.P., Mellone, U., Merrill, E., Morrison, T.A., Díazmuňoz, S.L., Mysterud, A., Nandintsetseg, D., Nathan, R., Niamir, A., Odden, J., Hara, R.B.O., Oliveirasantos, L.G.R., Olson, K.A., Patterson, B.D., De Paula, R.C, Pedrotti, L., Reineking, B., Rimmler, M., 2018. Moving in the anthropocene: globál reductions in terrrestrial mammalian movements. Science 359, 466–469.
Vetter, D., Hansbauer, M.M., Végvári, Z., Storch, L., 2011. Predictors of forest fragmentation sensitivity in Neotropical vertebrates: a quantitative review. Ecography 34, 1–8.
Villard, M.A., Metzger, J.P., 2014. Beyond the fragmentation debatě: a conceptual model to predict when habitat configuration really matters. J. Appl. Ecol. 51, 309–318.
Waits, L.P., Cushman, S.A., Spear, S.F., 2016. Applications of landscape genetics to connectivity research interrestrial animals. In: Balkenhol, N., Cushman, S.A., Storfer, A.T., Waits, L.P. (Eds.), Landscape Genetics: Concepts, Methods, Applications. West Sussex, pp. 199–219.
Williams, B.L, Brawn, J.D., Paige, K.N., 2003. Landscape scale genetic effects of habitat fragmentation on a high gene flow species: speyeria idalia (Nymphalidae). Mol. Ecol. 12, 11–20.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Lino, A., Fonseca, C., Rojas, D. et al. A meta-analysis of the effects of habitat loss and fragmentation on genetic diversity in mammals. Mamm Biol 94, 69–76 (2019). https://doi.org/10.1016/j.mambio.2018.09.006
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1016/j.mambio.2018.09.006