Secondary extinctions of biodiversity.

Extinctions beget further extinctions when species lose obligate mutualists, predators, prey, or hosts. Here, we develop a conceptual model of species and community attributes affecting secondary extinction likelihood, incorporating mechanisms that buffer organisms against partner loss. Specialized interactors, including 'cryptic specialists' with diverse but nonredundant partner assemblages, incur elevated risk. Risk is also higher for species that cannot either evolve new traits following partner loss or obtain novel partners in communities reorganizing under changing environmental conditions. Partner loss occurs alongside other anthropogenic impacts; multiple stressors can circumvent ecological buffers, enhancing secondary extinction risk. Stressors can also offset each other, reducing secondary extinction risk, a hitherto unappreciated phenomenon. This synthesis suggests improved conservation planning tactics and critical directions for research on secondary extinctions.

[1]  Malcolm L. Hunter,et al.  Paleoecology and the Coarse-Filter Approach to Maintaining Biological Diversity , 1988 .

[2]  J. Terborgh,et al.  Ecological Meltdown in Predator-Free Forest Fragments , 2001, Science.

[3]  E. K. Pikitch,et al.  Trophic Downgrading of Planet Earth , 2011, Science.

[4]  Paul Beier,et al.  Forks in the Road: Choices in Procedures for Designing Wildland Linkages , 2008, Conservation biology : the journal of the Society for Conservation Biology.

[5]  A. Traveset,et al.  Conservation and restoration of plant–animal mutualisms on oceanic islands , 2010 .

[6]  Judith L Bronstein,et al.  Mutualisms in a changing world: an evolutionary perspective. , 2010, Ecology letters.

[7]  J. Brodie,et al.  Functional differences within a guild of tropical mammalian frugivores. , 2009, Ecology.

[8]  P. Ralph,et al.  Coral bleaching: the role of the host. , 2009, Trends in ecology & evolution.

[9]  William F. Morris,et al.  Quantitative conservation biology , 2002 .

[10]  S. Kalisz,et al.  Context-dependent autonomous self-fertilization yields reproductive assurance and mixed mating , 2004, Nature.

[11]  E. Stahl,et al.  Recent speciation associated with the evolution of selfing in Capsella , 2009, Proceedings of the National Academy of Sciences.

[12]  J. Thompson.  The Geographic Mosaic of Coevolution , 2005 .

[13]  J. Kelly,et al.  RAPID EVOLUTION CAUSED BY POLLINATOR LOSS IN MIMULUS GUTTATUS , 2011, Evolution; international journal of organic evolution.

[14]  R. Sukumar,et al.  Waiting for Gajah: an elephant mutualist's contingency plan for an endangered megafaunal disperser , 2013 .

[15]  Richard P. Reading,et al.  The Prairie Dog and Biotic Diversity , 1994 .

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

[17]  Mark A. Hurley,et al.  Relative influence of human harvest, carnivores, and weather on adult female elk survival across western North America , 2013 .

[18]  B. Husband,et al.  EVOLUTION OF THE MAGNITUDE AND TIMING OF INBREEDING DEPRESSION IN PLANTS , 1996, Evolution; international journal of organic evolution.

[19]  Jonathan H. Grabowski,et al.  HABITAT COMPLEXITY DISRUPTS PREDATOR–PREY INTERACTIONS BUT NOT THE TROPHIC CASCADE ON OYSTER REEFS , 2004 .

[20]  A. Shiels,et al.  Are introduced rats (Rattus rattus) both seed predators and dispersers in Hawaii? , 2011, Biological Invasions.

[21]  Nyeema C. Harris,et al.  Coextinction and persistence of dependent species in a changing world , 2012 .

[22]  H. Howe,et al.  Low Recruitment of Trees Dispersed by Animals in African Forest Fragments , 2001 .

[23]  C. A. Howell,et al.  Re-Shuffling of Species with Climate Disruption: A No-Analog Future for California Birds? , 2009, PloS one.

[24]  E. Zavaleta,et al.  Imperfect Replacement of Native Species by Non‐Native Species as Pollinators of Endemic Hawaiian Plants , 2014, Conservation biology : the journal of the Society for Conservation Biology.

[25]  J. Brodie,et al.  Bushmeat poaching reduces the seed dispersal and population growth rate of a mammal-dispersed tree. , 2009, Ecological applications : a publication of the Ecological Society of America.

[26]  Jordi Bascompte,et al.  Non-random coextinctions in phylogenetically structured mutualistic networks , 2007, Nature.

[27]  E. Zavaleta,et al.  Building Taxon Substitution Guidelines on a Biological Control Foundation , 2014 .

[28]  Emmanuelle Porcher,et al.  Plant mating systems in a changing world. , 2010, Trends in ecology & evolution.

[29]  J. Brodie,et al.  Are wolves saving Yellowstone's aspen? A landscape-level test of a behaviorally mediated trophic cascade. , 2010, Ecology.

[30]  Georgina M. Mace,et al.  Synthetic Biology and Conservation of Nature: Wicked Problems and Wicked Solutions , 2013, PLoS biology.

[31]  D. Kelly,et al.  Seed dispersal of matai (Prumnopitys taxifolia) by feral pigs (Sus scrofa). , 2012 .

[32]  D. Kelly,et al.  Cascading Effects of Bird Functional Extinction Reduce Pollination and Plant Density , 2011, Science.

[33]  S. Wright,et al.  Meta‐Analysis of the Effects of Human Disturbance on Seed Dispersal by Animals , 2012, Conservation biology : the journal of the Society for Conservation Biology.

[34]  M. Grube,et al.  Joint Dispersal Does Not Imply Maintenance of Partnerships in Lichen Symbioses , 2009, Microbial Ecology.

[35]  I. Washitani,et al.  Genetic Diversity and Outcrossing Rate between Undisturbed and Selectively Logged Forests of Shorea curtisii (Dipterocarpaceae) Using Microsatellite DNA Analysis , 2002, International Journal of Plant Sciences.

[36]  T. Stuessy,et al.  A survey of floral traits, breeding systems, floral visitors, and pollination systems of the angiosperms of the Juan Fernández Islands (Chile) , 2001, The Botanical Review.

[37]  G. Daily,et al.  Natural Capital: Theory and Practice of Mapping Ecosystem Services , 2011 .

[38]  Jason M Tylianakis,et al.  Specialization and Rarity Predict Nonrandom Loss of Interactions from Mutualist Networks , 2012, Science.

[39]  U. Mueller,et al.  The Origin of the Attine Ant-Fungus Mutualism , 2001, The Quarterly Review of Biology.

[40]  Stefan Sellman,et al.  High frequency of functional extinctions in ecological networks , 2013, Nature.

[41]  Peter Chesson,et al.  Functional tradeoffs determine species coexistence via the storage effect , 2009, Proceedings of the National Academy of Sciences.

[42]  Jordi Bascompte,et al.  Habitat loss and the structure of plant-animal mutualistic networks. , 2006, Ecology letters.

[43]  B. Ebenman,et al.  Using community viability analysis to identify fragile systems and keystone species. , 2005, Trends in ecology & evolution.

[44]  M. Festa‐Bianchet,et al.  Evolutionary rescue in vertebrates: evidence, applications and uncertainty , 2013, Philosophical Transactions of the Royal Society B: Biological Sciences.

[45]  Jane Memmott,et al.  Global warming and the disruption of plant-pollinator interactions. , 2007, Ecology letters.

[46]  J. Bruno,et al.  Cascading effects of predator richness , 2008 .

[47]  C. Dickman,et al.  Keystone effects of an alien top-predator stem extinctions of native mammals , 2009, Proceedings of the Royal Society B: Biological Sciences.

[48]  J. Bascompte,et al.  Global change and species interactions in terrestrial ecosystems. , 2008, Ecology letters.

[49]  Joseph Tzanopoulos,et al.  Long-term observation of a pollination network: fluctuation in species and interactions, relative invariance of network structure and implications for estimates of specialization. , 2008, Ecology letters.

[50]  P. Cox.  Extinction of the Hawaiian avifauna resulted in a change of pollinators for the ieie, Freycinetia arborea. , 1983 .

[51]  William J. Bond,et al.  Do mutualisms matter? Assessing the impact of pollinator and disperser disruption on plant extinction , 1994 .

[52]  G. Bell.  Evolutionary rescue and the limits of adaptation , 2013, Philosophical Transactions of the Royal Society B: Biological Sciences.

[53]  E. Simms,et al.  Pathways to mutualism breakdown. , 2006, Trends in ecology & evolution.

[54]  Elizabeth L. Bennett,et al.  Wild meat: the bigger picture , 2003 .

[55]  Eric Post,et al.  Climate change intensification of herbivore impacts on tree recruitment , 2012, Proceedings of the Royal Society B: Biological Sciences.

[56]  S. Sakai,et al.  Wind and insect pollination (ambophily) of Mallotus spp. (Euphorbiaceae) in tropical and temperate forests , 2013 .

[57]  Anthony J. Giordano,et al.  Lack of trophic release with large mammal predators and prey in Borneo , 2013 .

[58]  E. Zavaleta,et al.  Effects of Native and Non‐Native Vertebrate Mutualists on Plants , 2012, Conservation biology : the journal of the Society for Conservation Biology.

[59]  J. Wilmshurst,et al.  A Megafauna’s Microfauna: Gastrointestinal Parasites of New Zealand’s Extinct Moa (Aves: Dinornithiformes) , 2013, PloS one.

[60]  P. Cheptou.  ALLEE EFFECT AND SELF‐FERTILIZATION IN HERMAPHRODITES: REPRODUCTIVE ASSURANCE IN DEMOGRAPHICALLY STABLE POPULATIONS , 2004, Evolution; international journal of organic evolution.

[61]  J. Biesmeijer,et al.  Global pollinator declines: trends, impacts and drivers. , 2010, Trends in ecology & evolution.

[62]  D. Doak,et al.  Synergy of multiple partners, including freeloaders, increases host fitness in a multispecies mutualism , 2010, Proceedings of the National Academy of Sciences.

[63]  C. Pfister,et al.  Patterns of variance in stage-structured populations: evolutionary predictions and ecological implications. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[64]  Lian Pin Koh,et al.  Species Coextinctions and the Biodiversity Crisis , 2004, Science.

[65]  J. Provan,et al.  Range‐edge effects promote clonal growth in peripheral populations of the one‐sided wintergreen Orthilia secunda , 2008 .

[66]  W. Bond,et al.  Mutualisms matter: pollination rate limits the distribution of oil-secreting orchids , 2011 .

[67]  Paul Beier,et al.  Use of Land Facets to Plan for Climate Change: Conserving the Arenas, Not the Actors , 2010, Conservation biology : the journal of the Society for Conservation Biology.

[68]  Ulf Dieckmann,et al.  Coevolutionary Dynamics and the Conservation of Mutualisms , 2004 .

[69]  Jay P. McEntee,et al.  Disperser limitation and recruitment of an endemic African tree in a fragmented landscape. , 2009, Ecology.

[70]  M. Burgman,et al.  Modelling the persistence of an apparently immortal Banksia species after fire and land clearing , 1999 .

[71]  Nicholas K. Dulvy,et al.  Coral reef cascades and the indirect effects of predator removal by exploitation , 2004 .

[72]  Lian Pin Koh,et al.  The sixth mass coextinction: are most endangered species parasites and mutualists? , 2009, Proceedings of the Royal Society B: Biological Sciences.

[73]  Robert M Ewers,et al.  Interactive effects of habitat modification and species invasion on native species decline. , 2007, Trends in ecology & evolution.

[74]  Michele R. Dudash,et al.  Pollen limitation of plant reproduction: Ecological and evolutionary causes and consequences , 2004 .

[75]  Christopher N. Johnson,et al.  Rarity of a top predator triggers continent-wide collapse of mammal prey: dingoes and marsupials in Australia , 2007, Proceedings of the Royal Society B: Biological Sciences.

[76]  C. Margules,et al.  Predictors of Species Sensitivity to Fragmentation , 2004, Biodiversity & Conservation.

[77]  Matteo Detto,et al.  Consequences of defaunation for a tropical tree community. , 2013, Ecology letters.

[78]  J. Wootton,et al.  ESTIMATES AND TESTS OF PER CAPITA INTERACTION STRENGTH: DIET, ABUNDANCE, AND IMPACT OF INTERTIDALLY FORAGING BIRDS , 1997 .

[79]  John Harte,et al.  Response of complex food webs to realistic extinction sequences. , 2007, Ecology.

[80]  D. H. Reed,et al.  INBREEDING DEPRESSION INCREASES WITH ENVIRONMENTAL STRESS: AN EXPERIMENTAL STUDY AND META‐ANALYSIS , 2011, Evolution; international journal of organic evolution.

[81]  Nigel,et al.  Tree recruitment in an empty forest. , 2008, Ecology.

[82]  P. Brancalion,et al.  Functional Extinction of Birds Drives Rapid Evolutionary Changes in Seed Size , 2013, Science.

[83]  Owen T Lewis,et al.  Structural dynamics and robustness of food webs. , 2010, Ecology letters.

[84]  W. Brockelman,et al.  Nonredundancy in the dispersal network of a generalist tropical forest tree. , 2011, Ecology.

[85]  S. Harris,et al.  Resurrecting Extinct Interactions with Extant Substitutes , 2011, Current Biology.

[86]  J. Iriondo,et al.  Inbreeding at the edge: does inbreeding depression increase under more stressful conditions? , 2012 .

[87]  Charles H. Peterson,et al.  Supporting Online Material for Cascading Effects of the Loss of Apex Predatory Sharks from a Coastal Ocean , 2007 .

[88]  W. Bond,et al.  Ecology of sprouting in woody plants: the persistence niche. , 2001, Trends in ecology & evolution.

[89]  J. P. González‐Varo,et al.  Long-term demographic consequences of a seed dispersal disruption , 2012, Proceedings of the Royal Society B: Biological Sciences.

[90]  Mark G. Anderson,et al.  Incorporating climate change into systematic conservation planning , 2012, Biodiversity and Conservation.

[91]  A. P. Schaffers,et al.  Parallel Declines in Pollinators and Insect-Pollinated Plants in Britain and the Netherlands , 2006, Science.

[92]  A. Lugo,et al.  Natural mixing of species: novel plant–animal communities on Caribbean Islands , 2012 .

[93]  I. C. Machado,et al.  Flowering dynamics and pollination system of the sedge Rhynchospora ciliata (Vahl) Kükenth (Cyperaceae): does ambophily enhance its reproductive success? , 2012, Plant biology.

[94]  Richard T. Corlett,et al.  Climate change in the tropics: The end of the world as we know it? , 2012 .

[95]  E. Zavaleta,et al.  Biodiversity management in the face of climate change: A review of 22 years of recommendations , 2009 .