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Confounding Factors in the Detection of Species Responses to Habitat Fragmentation

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Confounding Factors in the Detection of Species Responses to Habitat Fragmentation Biol. Rev. (2006), 81, pp. 117–142. f 2005 Cambridge Philosophical Society 117 doi:10.1017/S1464793105006949 Printed in the United Kingdom Confounding factors in the detection of species responses to habitat fragmentation Robert M. Ewers1,2,3* and Raphael K. Didham1 1 School of Biological Sciences, University of Canterbury, Private Bag 4800, Christchurch, New Zealand (E-mail: [email protected]) 2 Smithsonian Tropical Research Institute, Apartado 0843-03092, Balboa, Panama´, Republic of Panama´ 3 Current address: Institute of Zoology, Zoological Society of London, Regents Park, London NW14RY, UK, and Department of Zoology, Cambridge University, Downing Street, Cambridge CB23EJ, UK (Received 9 November 2004; revised and accepted 19 September 2005) ABSTRACT Habitat loss has pervasive and disruptive impacts on biodiversity in habitat remnants. The magnitude of the ecological impacts of habitat loss can be exacerbated by the spatial arrangement – or fragmentation – of remaining habitat. Fragmentation per se is a landscape-level phenomenon in which species that survive in habitat remnants are confronted with a modified environment of reduced area, increased isolation and novel ecological boundaries. The implications of this for individual organisms are many and varied, because species with differing life history strategies are differentially affected by habitat fragmentation. Here, we review the extensive literature on species responses to habitat fragmentation, and detail the numerous ways in which confounding factors have either masked the detection, or prevented the manifestation, of predicted fragmentation effects. Large numbers of empirical studies continue to document changes in species richness with decreasing habitat area, with positive, negative and no relationships regularly reported. The debate surrounding such widely contrasting results is beginning to be resolved by findings that the expected positive species-area relationship can be masked by matrix-derived spatial subsidies of resources to fragment-dwelling species and by the invasion of matrix-dwelling species into habitat edges. Significant advances have been made recently in our understanding of how species interactions are altered at habitat edges as a result of these changes. Interestingly, changes in biotic and abiotic parameters at edges also make ecological processes more variable than in habitat interiors. Individuals are more likely to encounter habitat edges in fragments with convoluted shapes, leading to increased turnover and variability in population size than in fragments that are compact in shape. Habitat isolation in both space and time disrupts species distribution patterns, with consequent effects on metapopulation dynamics and the genetic structure of fragment-dwelling populations. Again, the matrix habitat is a strong determinant of fragmentation effects within remnants because of its role in regulating dispersal and dispersal- related mortality, the provision of spatial subsidies and the potential mediation of edge-related microclimatic gradients. We show that confounding factors can mask many fragmentation effects. For instance, there are multiple ways in which species traits like trophic level, dispersal ability and degree of habitat specialisation influence species- level responses. The temporal scale of investigation may have a strong influence on the results of a study, with short-term crowding effects eventually giving way to long-term extinction debts. Moreover, many fragmentation effects like changes in genetic, morphological or behavioural traits of species require time to appear. By contrast, synergistic interactions of fragmentation with climate change, human-altered disturbance regimes, species interactions and other drivers of population decline may magnify the impacts of fragmentation. To conclude, we emphasise that anthropogenic fragmentation is a recent phenomenon in evolutionary time and suggest that the final, long-term impacts of habitat fragmentation may not yet have shown themselves. * Address for correspondence: Department of Zoology, Cambridge University, Downing Street, Cambridge CB2 3EJ, UK (Tel: (+44) 1223 336675; Fax: (+44) 1223 336676; E-mail: [email protected]). 118 Robert M. Ewers and Raphael K. Didham Key words: area effects, edge effects, habitat fragmentation, habitat loss, invertebrate, isolation, matrix, shape index, synergies, time lags. CONTENTS I. Introduction ................................................................................................................................................. 118 (1) Causes of habitat fragmentation ......................................................................................................... 118 (2) Approaches to the study of fragmentation ........................................................................................ 119 (3) Structure of this review ........................................................................................................................ 119 II. Habitat area ................................................................................................................................................. 119 (1) Species-area relationships: predicting extinction rates from habitat loss ...................................... 120 (2) Landscape and extinction thresholds ................................................................................................. 122 (3) The population consequences of small habitat area ........................................................................ 122 III. Edge effects ................................................................................................................................................... 123 (1) Community composition at habitat boundaries ............................................................................... 123 (2) Edges as ecological traps ...................................................................................................................... 123 (3) Edges alter species interactions ........................................................................................................... 124 (4) Variability and hyperdynamism at edges .......................................................................................... 124 IV. Shape complexity ........................................................................................................................................ 124 V. Isolation ........................................................................................................................................................ 125 VI. Matrix effects ................................................................................................................................................ 125 (1) Can matrix quality mitigate fragmentation effects? ......................................................................... 126 (2) Matrix and dispersal ............................................................................................................................. 126 (3) Matrix and edge effects ........................................................................................................................ 127 VII. Confounding factors in the detection of fragmentation impacts .......................................................... 127 (1) Trait-mediated differences in species responses to fragmentation ................................................. 127 (2) Time lags in the manifestation of fragmentation effects .................................................................. 129 (a) Time lags in population responses to fragmentation ................................................................. 129 (b) Biogeographic factors controlling fragmentation responses ...................................................... 130 (c) Altered selection pressures and developmental instability ......................................................... 131 (3) Synergies magnify the impacts of fragmentation .............................................................................. 131 (a) Fragmentation and pollination ...................................................................................................... 131 (b) Fragmentation and disease ............................................................................................................. 132 (c) Fragmentation and climate change .............................................................................................. 132 (d ) Fragmentation and human-modified disturbance regimes ........................................................ 133 VIII. Implications for fragmentation research .................................................................................................. 133 IX. Conclusions .................................................................................................................................................. 134 X. Acknowledgements ...................................................................................................................................... 134 XI. References .................................................................................................................................................... 134 I. INTRODUCTION (1) Causes of habitat fragmentation Fragmentation, as an expression of the size and spatial The magnitude of habitat fragmentation reflects the per- arrangement of habitat patches, is not a purely anthro- vasive influence of humans
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