Network structure and biodiversity loss in food webs: robustness increases with connectance

Food-web structure mediates dramatic effects of biodiversity loss including secondary and ‘cascading’ extinctions. We studied these effects by simulating primary species loss in 16 food webs from terrestrial and aquatic ecosystems and measuring robustness in terms of the secondary extinctions that followed. As observed in other networks, food webs are more robust to random removal of species than to selective removal of species with the most trophic links to other species. More surprisingly, robustness increases with food-web connectance but appears independent of species richness and omnivory. In particular, food webs experience ‘rivet-like’ thresholds past which they display extreme sensitivity to removal of highly connected species. Higher connectance delays the onset of this threshold. Removing species with few trophic connections generally has little effect though there are several striking exceptions. These findings emphasize how the number of species removed affects ecosystems differently depending on the trophic functions of species removed.

[1]  R. Macarthur Fluctuations of Animal Populations and a Measure of Community Stability , 1955 .

[2]  J. Lawton,et al.  On feeding on more than one trophic level , 1978, Nature.

[3]  R. May,et al.  Stability and Complexity in Model Ecosystems , 1976, IEEE Transactions on Systems, Man, and Cybernetics.

[4]  Stuart L. Pimm,et al.  Complexity and stability: another look at MacArthur's original hypothesis , 1979 .

[5]  Stuart L. Pimm,et al.  Food web design and the effect of species deletion , 1980 .

[6]  G. B. Williamson,et al.  High temperature of forest fires under pines as a selective advantage over oaks , 1981, Nature.

[7]  Joel E. Cohen,et al.  Community food webs have scale-invariant structure , 1984, Nature.

[8]  Robert M. May,et al.  The Search for Patterns in the Balance of Nature: Advances and Retreats , 1986 .

[9]  Philip H. Warren,et al.  Spatial and temporal variation in the structure of a freshwater food web , 1989 .

[10]  R. Ulanowicz,et al.  The Seasonal Dynamics of The Chesapeake Bay Ecosystem , 1989 .

[11]  Neo D. Martinez Artifacts or Attributes? Effects of Resolution on the Little Rock Lake Food Web , 1991 .

[12]  Joel E. Cohen,et al.  Food web patterns and their consequences , 1991, Nature.

[13]  G. Polis,et al.  Complex Trophic Interactions in Deserts: An Empirical Critique of Food-Web Theory , 1991, The American Naturalist.

[14]  S. Hall,et al.  Food-web patterns : lessons from a species-rich web , 1991 .

[15]  S. Levin THE PROBLEM OF PATTERN AND SCALE IN ECOLOGY , 1992 .

[16]  Jerry C. Blackford,et al.  Self-assembling food webs : a global viewpoint of coexistence of species in Lotka-Volterra communities , 1992 .

[17]  R. Paine,et al.  Food-web analysis through field measurement of per capita interaction strength , 1992, Nature.

[18]  Neo D. Martinez Constant Connectance in Community Food Webs , 1992, The American Naturalist.

[19]  K. Havens,et al.  Scale and Structure in Natural Food Webs , 1992, Science.

[20]  S. Levin The problem of pattern and scale in ecology , 1992 .

[21]  Neo D. Martinez,et al.  Effect of scale on food web structure. , 1993, Science.

[22]  J. Roughgarden,et al.  Construction and Analysis of a Large Caribbean Food Web , 1993 .

[23]  Richard Law,et al.  Alternative Permanent States of Ecological Communities , 1993 .

[24]  J. Downing,et al.  Biodiversity and stability in grasslands , 1996, Nature.

[25]  P. Warren Making connections in food webs. , 1994, Trends in ecology & evolution.

[26]  J. Lawton,et al.  Declining biodiversity can alter the performance of ecosystems , 1994, Nature.

[27]  Neo D. Martinez Scale-Dependent Constraints on Food-Web Structure , 1994, The American Naturalist.

[28]  M. Huxham,et al.  Do Parasites Reduce the Chances of Triangulation in a Real Food Web , 1996 .

[29]  J. Castilla,et al.  Challenges in the Quest for Keystones , 1996 .

[30]  P. Vitousek,et al.  The Effects of Plant Composition and Diversity on Ecosystem Processes , 1997 .

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

[32]  Robert B. Waide,et al.  The food web of a tropical rain forest , 1997 .

[33]  J. Lawton,et al.  POSITIVE AND NEGATIVE EFFECTS OF ORGANISMS AS PHYSICAL ECOSYSTEM ENGINEERS , 1997 .

[34]  McIntosh,et al.  Disturbance, resource supply, and food-web architecture in streams , 1998 .

[35]  Duncan J. Watts,et al.  Collective dynamics of ‘small-world’ networks , 1998, Nature.

[36]  A. Hastings,et al.  Weak trophic interactions and the balance of nature , 1998, Nature.

[37]  D. Wilcove,et al.  QUANTIFYING THREATS TO IMPERILED SPECIES IN THE UNITED STATES , 1998 .

[38]  Neo D. Martinez,et al.  TROPHIC RANK AND THE SPECIES-AREA RELATIONSHIP , 1999 .

[39]  E. Berlow,et al.  Strong effects of weak interactions in ecological communities , 1999, Nature.

[40]  Bradford A. Hawkins,et al.  EFFECTS OF SAMPLING EFFORT ON CHARACTERIZATION OF FOOD-WEB STRUCTURE , 1999 .

[41]  Robert R. Christian,et al.  Organizing and understanding a winter's seagrass foodweb network through effective trophic levels , 1999 .

[42]  H E Stanley,et al.  Classes of small-world networks. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[43]  Tomas Jonsson,et al.  Biodiversity lessens the risk of cascading extinction in model food webs , 2000 .

[44]  Veijo Kaitala,et al.  Species loss leads to community closure , 2000 .

[45]  Albert-László Barabási,et al.  Error and attack tolerance of complex networks , 2000, Nature.

[46]  Neo D. Martinez,et al.  Predators, parasitoids and pathogens: species richness, trophic generality and body sizes in a natural food web , 2000 .

[47]  Neo D. Martinez,et al.  Simple rules yield complex food webs , 2000, Nature.

[48]  R. Albert,et al.  The large-scale organization of metabolic networks , 2000, Nature.

[49]  Andrew D. Huberman,et al.  Finger-length ratios and sexual orientation , 2000, Nature.

[50]  K. McCann The diversity–stability debate , 2000, Nature.

[51]  J. Jackson,et al.  Measuring Past Biodiversity , 2001, Science.

[52]  A. Barabasi,et al.  Lethality and centrality in protein networks , 2001, Nature.

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

[54]  Ricard V. Solé,et al.  Complexity and fragility in ecological networks , 2000, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[55]  K. Bjorndal,et al.  Historical Overfishing and the Recent Collapse of Coastal Ecosystems , 2001, Science.

[56]  J. E. Cohen,et al.  Global stability, local stability and permanence in model food webs. , 2001, Journal of theoretical biology.

[57]  S. Strogatz Exploring complex networks , 2001, Nature.

[58]  Albert-László Barabási,et al.  Statistical mechanics of complex networks , 2001, ArXiv.

[59]  J. H. Brown,et al.  Complex species interactions and the dynamics of ecological systems: long-term experiments. , 2001, Science.

[60]  J. P. Grime,et al.  Biodiversity and Ecosystem Functioning: Current Knowledge and Future Challenges , 2001, Science.

[61]  Neo D. Martinez,et al.  Food-web structure and network theory: The role of connectance and size , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[62]  Neo D. Martinez,et al.  Two degrees of separation in complex food webs , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[63]  J. Montoya,et al.  Small world patterns in food webs. , 2002, Journal of theoretical biology.

[64]  Jennifer A. Dunne,et al.  Small Networks but not Small Worlds: Unique Aspects of Food Web Structure , .