Journal of Animal Ecology 2011, 80, 307309

doi: 10.1111/j.1365-2656.2011.01805.x

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Response of ecosystems to realistic extinction sequences

Cheetah (Acinonyx jubatus) one of the IUCN Red-Listed species in the Serengeti food web. Photograph by Fredrik Larsson.

de Visser, S., Freymann, B. & Olff, H. (2011) The Serengeti food web: empirical quantication and analysis of topological changes under increasing human impact. Journal of Animal Ecology 80, 465475. Recent research suggests that effects of species loss on the structure and functioning of ecosystems will critically depend on the order with which species go extinct. However, there are few studies of the response of natural ecosystems to realistic extinction sequences. Using an extinction scenario based on the International Union for Conservation of Nature (IUCN) Red List, de Visser et al. sequentially deleted species from a topological model of the Serengeti food web. Under this scenario, large-bodied species like top predators and mega-herbivores go extinct rst. The resulting changes in the trophic structure of the food web might affect the robustness of the ecosystem to future disturbances.
The accelerating and worldwide loss of biodiversity caused by degradation and fragmentation of natural habitats, climate change and overexploitation of natural populations is a matter of growing concern. Owing to the interdependences among species in ecosystems, such human-caused losses of species might in turn unleash cascades of secondary extinctions (Pimm 1980; Borrvall, Ebenman & Jonsson 2000; Dunne, Williams & Martinez 2002; Ebenman, Law & Borrvall 2004; Montoya, Pimm & Sole 2006; Dunn et al. 2009; Fowler 2010) with potentially important consequences for the stability and functioning of those systems (Ives & Cardinale 2004; Raffaelli 2004; Thebault, Huber & Loreau 2007). Recent research suggests that the risk and extent of such extinction
Correspondence author. E-mail: boebe@ifm.liu.se

cascades should depend on the order with which species go extinct as well as on the trophic structure of the affected eco system (Sole & Montoya 2001; Dunne et al. 2002; Dunne & Williams 2009; Staniczenko et al. 2010). Thus, to be able to predict the response of a natural ecosystem to species loss, we need to know the structure of the system as well as which species are likely to go extinct in the rst place (Fig. 1). There are few studies however that have investigated the response of natural ecosystems, especially terrestrial ones, to realistic extinction sequences (Srinivasan et al. 2007). The study by de Visser, Freymann & Olff (2011) represents an important step forward. Based on eld work and literature studies, they have generated a structural (topological) model of the Serengeti food web including vertebrates as well as invertebrates. This is the rst, relatively complete description

2011 The Author. Journal of Animal Ecology 2011 British Ecological Society

308 B. Ebenman
(a) 8
7

Extinction order

6 5 4 3 2 1 0 1 2 3 4 5 6 7 8

Species ranking

(b)

1 09 08 07

06 05 04 03 02 01 0

Network measure

Fig. 1. (a) The order with which species are deleted as a function of their ranking with respect to some trait like, for instance, body size or connectivity (number of direct links to other species). If the trait of interest is body size, then species 1 is the smallest and species 8 the largest species. In this case, the dotted line (squares) represents a deletion sequence where large species are deleted rst, while the hatched line (lled circles) represents a sequence where small species are deleted rst. The solid line (triangles) shows a random deletion sequence no relationship between body size and order of deletion. (b) The robustness of a food web to species deletion as a function of its structure like, for instance, its connectance or species richness, for two different deletion sequences. Robustness could be measured as the proportion of species that must be deleted to cause a loss of 100% of the species in the original community (in this case, the maximum and minimum robustness will be 1 and 1 divided by the number of species, respectively). If the network measure of interest is species richness, then the gure shows that robustness increases with species richness for both deletion scenarios. The crossing of the lines indicates that there is an interaction between species richness and deletion sequence, such that species-poor communities are less robust to one deletion sequence (hatched line), while species-rich communities are less robust to the other deletion sequence (dotted line).

of a natural savanna food web. The web consists of 86 nodes (trophic species) including seven plant resource types, 321 vertebrate species and 29 orders of invertebrates and with animal species ranging in body mass between 10)7 and 104 kg. The web has 547 links, many of which are vertebrate invertebrate feeding interactions. Using in silico experiments, de Visser et al. investigate the robustness of this food web to an extinction scenario based on the Red List of Threatened Species (IUCN 2009). Under this scenario, large-bodied species like top predators and mega-herbivores go extinct rst.

Several studies have shown that large-bodied species and species at the top of food chains tend to be more vulnerable to human-caused disturbances than small-bodied species and species lower down in the food chains (e.g. Cardillo et al. 2005; Duffy 2003). A common measure of the robustness of a food web to species loss is the proportion that must be deleted to cause a loss of a certain proportion (e.g. 50%) of the species in the original web (Dunne et al. 2002). The higher the proportion of species that needs to be deleted, the more robust the web is. The IUCN Red List deletion sequence, which only involves 14 primary extinctions (16% of the nodes), caused no secondary extinctions in the Serengeti food web. Although this deletion sequence caused no secondary extinctions, it led to changes in the topology of the food web and in the distribution of body sizes of species. Link density (average number of links per node) and number of predator nodes over prey nodes decreased, average body mass decreased and predatorprey body mass ratio increased. Species deletions also led to changes in the shape of the degree distribution, that is, the frequency distribution of the number of links per node in the network. All these changes might affect the fragility of the system to future disturbances. Thus, even if a rst sequence of species extinctions does not result in any secondary extinctions, it could still lead to the loss of a large fraction of the functionally important links in the network (Allesina, Bodini & Pascual 2009). A targeted attack on one additional species (removal of the most critical node in the network) might then result in a total network collapse, suggesting the possible presence of tipping points in the collapse of ecological networks. In addition to the Red List deletion scenario, de Visser et al. also explored deletion sequences based on body mass and connectivity of species (number of links to other species). They found that the Serengeti food web was highly robust to decreasing body mass and increasing connectivity deletion sequences (i.e. starting with the largest species and least connected species, respectively), while it was more vulnerable to a decreasing connectivity deletion sequence (i.e. starting with the most connected node). The results with respect to the effects of connectivity are in line with earlier ndings (Sole & Montoya 2001; Dunne et al. 2002; Dunne & Williams 2009). It would also be interesting to compare the outcome of the Red List deletion scenario with that of random deletion sequences. The study of the Serengeti food web, like most other studies of the robustness of food webs to sequential species deletions, is based on so-called topological (structural) analysis. In this kind of analysis, the growth rates and dynamics of populations are not taken into account. The criterion for secondary extinction is simple: a species goes secondarily extinct when it has lost all its prey (in the Serengeti study a species was considered secondarily extinct when it had lost most of its main prey species even if some less important prey species remained). Thus, topological analysis is a bottomup approach and as such gives an estimate of the minimum number of secondary extinctions following the loss of a species in

Robustness

2011 The Author. Journal of Animal Ecology 2011 British Ecological Society, Journal of Animal Ecology, 80, 307309

Response of ecosystems to realistic extinction sequences 309 a community (Allesina et al. 2009). Secondary extinctions because of topdown cascades and disruption of predatormediated coexistence are not revealed in such an analysis. Thus, no secondary extinctions will be predicted even if all top predators in a community are lost. However, empirical studies have shown that loss of top predators can have farreaching consequences for the structure of local communities (e.g. Paine 1966; Estes & Palmisano 1974; Johnson, Isaac & Fisher 2007; Myers et al. 2007; Beschta & Ripple 2009). The inability to reveal topdown extinction cascades is a weak point of the topological approach. Detecting such cascades requires an analysis based on dynamical models, like LotkaVolterra and allometric bioenergetic models, where changes in the abundances of species are followed (Eklof & Ebenman 2006; Petchey et al. 2008; Berlow et al. 2009). However, such a dynamical approach requires much more knowledge about the system rare data on birth and mortality rates of species and on interspecic interaction strengths are needed. The strength of the topological approach taken by de Visser et al. is that it can be used even if data on birth and mortality rates and strengths of interaction between species are not available. Moreover, being purely topological, it makes no assumptions about the dynamics of the system (e.g. type of functional response). By exploring the fragility of a natural ecosystem to an ecologically realistic extinction sequence, de Visser et al. make a major contribution to the research on the response of ecosystems to species loss. Future work might build on this study by using extinction sequences based on both intrinsic biology of species and external impacts (Cardillo et al. 2004). The urgent need for such studies has been pointed out by several ecologists (e.g. Srinivasan et al. 2007). With more studies of this kind, new light will be shed on the relationship between the structure of ecosystems and their robustness to species loss. Bo Ebenman Division of Theoretical Biology, Linko ping University, IFM Theory and Modelling, SE-58183 Linko ping, Sweden
Cardillo, M., Purvis, A., Sechrest, W., Gittleman, J.L., Bielby, J. & Mace, G.M. (2004) Human population density and extinction risk in the worlds carnivores. PLoS Biology, 2, 909914. Cardillo, M., Mace, G.M., Jones, K.E., Bielby, J., Bininda-Emonds, O.R.P., Sechrest, W., Orme, C.D.L. & Purvis, A. (2005) Multiple causes of high extinction risk in large mammal species. Science, 309, 12391241. Duffy, J.E. (2003) Biodiversity loss, trophic skew and ecosystem functioning. Ecology Letters, 6, 680687. Dunn, R.R., Harris, N.C., Colwell, R.K., Koh, L.P. & Sodhi, N.S. (2009) The sixth mass coextinction: are most endangered species parasites and mutualists? Proceedings of the Royal Society B, 276, 30373045. Dunne, J.A. & Williams, R.J. (2009) Cascading extinctions and community collapse in model food webs. Philosophical Transactions of the Royal Society B, 364, 17111723. Dunne, J.A., Williams, R.J. & Martinez, N.D. (2002) Network structure and biodiversity loss in food webs: robustness increases with connectance. Ecology Letters, 5, 558567. Ebenman, B., Law, R. & Borrvall, C. (2004) Community viability analysis: the response of ecological communities to species loss. Ecology, 85, 25912600. Eklof, A. & Ebenman, B. (2006) Species loss and secondary extinctions in sim ple and complex model communities. Journal of Animal Ecology, 75, 239 246. Estes, J.A. & Palmisano, J.F. (1974) Sea otters: their role in structuring nearshore communities. Science, 185, 10581060. Fowler, M.S. (2010) Extinction cascades and the distribution of species interactions. Oikos, 119, 864873. IUCN (2009) The IUCN List of Threatened Species. Available at: http:// www.iucnredlist.org/. Ives, A.R. & Cardinale, B.J. (2004) Food-web interactions govern the resistance of communities after non-random extinctions. Nature, 429, 174177. Johnson, C.N., Isaac, J.L. & Fisher, D.O. (2007) Rarity of a top predator triggers continent-wide collapse of mammal prey: dingoes and marsupials in Australia. Proceedings of the Royal Society B, 274, 341346. Montoya, J.M., Pimm, S.L. & Sole, R.V. (2006) Ecological networks and their fragility. Nature, 442, 259264. Myers, R.A., Baum, J.K., Shepherd, T.D., Powers, S.P. & Peterson, C.H. (2007) Cascading effects of the loss of apex predatory sharks from a coastal ocean. Science, 315, 18461850. Paine, R.T. (1966) Food web complexity and species diversity. American Naturalist, 100, 6575. Petchey, O.L., Eklof, A., Borrvall, C. & Ebenman, B. (2008) Trophically unique species are vulnerable to cascading extinction. American Naturalist, 171, 568578. Pimm, S.L. (1980) Food web design and the effect of species deletion. Oikos, 35, 139149. Raffaelli, D. (2004) How extinction patterns affect ecosystems. Science, 306, 11411142. Sole, R.V. & Montoya, J.M. (2001) Complexity and fragility in ecological networks. Proceedings of the Royal Society B, 268, 20392045. Srinivasan, U.T., Dunne, J.A., Harte, J. & Martinez, N.D. (2007) Response of complex food webs to realistic extinction sequences. Ecology, 88, 671682. Staniczenko, P.P.A., Lewis, O.T., Jones, N.S. & Reed-Tsochas, F. (2010) Structural dynamics and robustness of food webs. Ecology Letters, 13, 891899. Thebault, E., Huber, V. & Loreau, M. (2007) Cascading extinctions and ecosystem functioning: contrasting effects of diversity depending on food web structure. Oikos, 116, 163173. de Visser, S., Freymann, B. & Olff, H. (2011) The Serengeti food web: empirical quantication and analysis of topological changes under increasing human impact. Journal of Animal Ecology, 80, 465475. Received 20 December 2010; accepted 6 January 2011 Handling Editor: Corey Bradshaw

References
Allesina, S., Bodini, A. & Pascual, M. (2009) Functional links and robustness in food webs. Philosophical Transactions of the Royal Society B, 364, 1701 1709. Berlow, E.R., Dunne, J.A., Martinez, N.D., Stark, P.B., Williams, R.J. & Brose, U. (2009) Simple prediction of interaction strengths in complex food webs. Proceedings of the National Academy of Sciences of the United States of America, 106, 187191. Beschta, R.L. & Ripple, W.J. (2009) Large predators and trophic cascades in terrestrial ecosystems of the western United States. Biological Conservation, 142, 24012414. Borrvall, C., Ebenman, B. & Jonsson, T. (2000) Biodiversity lessens the risk of cascading extinction in model food webs. Ecology Letters, 3, 131136.

2011 The Author. Journal of Animal Ecology 2011 British Ecological Society, Journal of Animal Ecology, 80, 307309