Abstract
There is a strong trend of declining populations in many species of both animals and plants. Dwindling numbers of species can eventually lead to their functional extinction. Functional, or ecological, extinction occurs when a species becomes too rare to fulfill its ecological, interactive role in the ecosystem, leading to true (numerical) extinction of other depending species. Recent theoretical work on food webs suggests that the frequency of functional extinction might be surprisingly high. However, little is known about the risk of functional species extinctions in networks with other types of interactions than trophic ones. Here, we explore the frequency of functional extinctions in model ecological networks having different proportions of antagonistic and mutualistic links. Furthermore, we investigate the topological relationship between functionally and numerically extinct species. We find that (1) the frequency of functional extinctions is higher in networks containing a mixture of antagonistic and mutualistic interactions than in networks with only one type of interaction, (2) increased mortality rate of species having both mutualistic and antagonistic links is more likely to lead to extinction of another species than to extinction of the species itself compared to species having only mutualistic or antagonistic links, and (3) trophic distance (shortest path) between functionally and numerically extinct species is, on average, longer than one, indicating the importance of indirect effects. These results generalize the findings of an earlier study on food webs, demonstrating the potential importance of functional extinction in a variety of ecological network types.
Similar content being viewed by others
References
Allesina S, Tang S (2012) Stability criteria for complex ecosystems. Nature 483:205–208. doi:10.1038/nature10832
Altermatt F, Pearse IS (2011) Similarity and specialization of the larval versus adult diet of European butterflies and moths. Am Nat 178:372–382
Anderson SH, Kelly D, Ladley JJ et al (2011) Cascading effects of bird functional extinction reduce pollination and plant density. Science 331:1068–1071. doi:10.1126/science.1199092
Barnosky AD, Matzke N, Tomiya S et al (2011) Has the earth’s sixth mass extinction already arrived? Nature 471:51–57. doi:10.1038/nature09678
Baum JK, Worm B (2009) Cascading top-down effects of changing oceanic predator abundances. J Anim Ecol 78:699–714. doi:10.1111/j.1365-2656.2009.01531.x
Baum JK, Myers RA, Kehler DG et al (2003) Collapse and conservation of shark populations in the northwest atlantic. Science 299:389–392. doi:10.1126/science.1079777
Berlow E, Neutel A-M, Cohen J et al (2004) Interaction strengths in food webs: issues and opportunities. J Anim Ecol 73:585–598
Berlow EL, Dunne JA, Martinez ND et al (2009) Simple prediction of interaction strengths in complex food webs. Proc Natl Acad Sci 106:187–191. doi:10.1073/pnas.0806823106
Brodie JF, Aslan CE, Rogers HS et al (2014) Secondary extinctions of biodiversity. Trends Ecol Evol 29:664–672
Brummitt N, Bachman SP, Moat J (2008) Applications of the IUCN Red List: towards a global barometer for plant diversity. Endanger Species Res 6:127–135. doi:10.3354/esr00135
Butchart SHM, Walpole M, Collen B et al (2010) Global biodiversity: indicators of recent declines. Science 328:1164–1168. doi:10.1126/science.1187512
Casini M, Hjelm J, Molinero J-C et al (2009) Trophic cascades promote threshold-like shifts in pelagic marine ecosystems. Proc Natl Acad Sci 106:197–202. doi:10.1073/pnas.0806649105
Christianou M, Ebenman B (2005) Keystone species and vulnerable species in ecological communities: strong or weak interactors? J Theor Biol 235:95–103
Cohen JE, Newman CM (1985) A stochastic theory of community food webs: I. Models and aggregated data. Proc R Soc Lond B Biol Sci 224:421–448. doi:10.1098/rspb.1985.0042
Collen B, Loh J, Whitmee S et al (2009) Monitoring change in vertebrate abundance: the living planet index. Conserv Biol 23:317–327. doi:10.1111/j.1523-1739.2008.01117.x
Colwell RK, Dunn RR, Harris NC (2012) Coextinction and persistence of dependent species in a changing world. Annu Rev Ecol Evol Syst 43:183–203
Cury PM, Boyd IL, Bonhommeau S et al (2011) Global seabird response to forage fish depletion—one-third for the birds. Science 334:1703–1706. doi:10.1126/science.1212928
De Ruiter P, Neutel A-M, Moore JC (1995) Energetics, patterns of interaction strengths, and stability in real ecosystems. Science 269:1257–1260
De’ath G, Fabricius KE (2000) Classification and regression trees: a powerful yet simple technique for ecological data analysis. Ecology 81:3178–3192. doi:10.1890/0012-9658(2000)081[3178:CARTAP]2.0.CO;2
Di Marco M, Boitani L, Mallon D et al (2014) A retrospective evaluation of the global decline of carnivores and ungulates. Conserv Biol 28:1109–1118. doi:10.1111/cobi.12249
Dirzo R, Young HS, Galetti M et al (2014) Defaunation in the anthropocene. Science 345:401–406. doi:10.1126/science.1251817
Ebenman B, Law R, Borrvall C (2004) Community viability analysis: the response of ecological communities to species loss. Ecology 85:2591–2600
Estes JA, Duggins DO, Rathbun GB (1989) The ecology of extinctions in kelp forest communities. Conserv Biol 3:252–264
Estes JA, Tinker MT, Bodkin JL (2010) Using ecological function to develop recovery criteria for depleted species: sea otters and kelp forests in the Aleutian archipelago. Conserv Biol 24:852–860. doi:10.1111/j.1523-1739.2009.01428.x
Estes JA, Terborgh J, Brashares JS et al (2011) Trophic downgrading of planet earth. Science 333:301–306. doi:10.1126/science.1205106
Fontaine C, Guimarães PR, Kéfi S et al (2011) The ecological and evolutionary implications of merging different types of networks. Ecol Lett 14:1170–1181. doi:10.1111/j.1461-0248.2011.01688.x
Fowler M (2010) Extinction cascades and the distribution of interactions. Oikos 119:864–873
Frank KT, Petrie B, Choi JS, Leggett WC (2005) Trophic cascades in a formerly cod-dominated ecosystem. Science 308:1621–1623. doi:10.1126/science.1113075
Galetti M, Guevara R, Côrtes MC et al (2013) Functional extinction of birds drives rapid evolutionary changes in seed size. Science 340:1086–1090. doi:10.1126/science.1233774
Gaston KJ, Blackburn TM, Goldewijk KK (2003) Habitat conversion and global avian biodiversity loss. Proc Biol Sci 270:1293–1300
Haydon D (1994) Pivotal assumptions determining the relationship between stability and complexity—an analytical synthesis of the stability-complexity debate. Am Nat 144:14–29
Hong Y (2013) On computing the distribution function for the Poisson binomial distribution. Comput Stat Data Anal 59:41–51. doi:10.1016/j.csda.2012.10.006
Jackson JBC, Kirby MX, Berger WH et al (2001) Historical overfishing and the recent collapse of coastal ecosystems. Science 293:629–637. doi:10.1126/science.1059199
James A, Plank MJ, Rossberg AG et al (2015) Constructing random matrices to represent real ecosystems. Am Nat 185:680–692
Joppa LN, Roberts DL, Pimm SL (2010) How many species of flowering plants are there? Proc R Soc Lond B Biol Sci. doi:10.1098/rspb.2010.1004
Kaneryd L, Borrvall C, Berg S et al (2012) Species-rich ecosystems are vulnerable to cascading extinctions in an increasingly variable world. Ecol Evol 2:858–874
Kokkoris G, Jansen VAA, Loreau M et al (2002) Variability in interaction strength and implications for biodiversity. J Anim Ecol 71:362–371
Kondoh M, Mougi A (2015) Interaction-type diversity hypothesis and interaction strength: the condition for the positive complexity-stability effect to arise. Popul Ecol. doi:10.1007/s10144-014-0475-9
Loh J, Green RE, Ricketts T et al (2005) The living planet index: using species population time series to track trends in biodiversity. Philos Trans R Soc B Biol Sci 360:289–295. doi:10.1098/rstb.2004.1584
May RM (1972) Will a large complex system be stable? Nature 238:413–414. doi:10.1038/238413a0
McCann K (2000) The diversity-stability debate. Nature 405:228–233
McCann K, Hastings A, Huxel GR (1998) Weak trophic interactions and the balance of nature. Nature 393:794–798
McConkey KR, Drake DR (2006) Flying foxes cease to function as seed dispersers long before they become rare. Ecology 87:271–276. doi:10.1890/05-0386
Melián CJ, Bascompte J, Jordano P, Krivan V (2009) Diversity in a complex ecological network with two interaction types. Oikos 118:122–130. doi:10.1111/j.1600-0706.2008.16751.x
Mougi A, Kondoh M (2012) Diversity of interaction types and ecological community stability. Science 337:349–351. doi:10.1126/science.1220529
Mougi A, Kondoh M (2014) Stability of competition–antagonism–mutualism hybrid community and the role of community network structure. J Theor Biol 360:54–58. doi:10.1016/j.jtbi.2014.06.030
Neutel A-M, Thorne MAS (2014) Interaction strengths in balanced carbon cycles and the absence of a relation between ecosystem complexity and stability. Ecol Lett 17:651–661. doi:10.1111/ele.12266
Neutel A-M, Heesterbeek JAP, de Ruiter PC (2002) Stability in real food webs: weak links in long loops. Science 296:1120–1123. doi:10.1126/science.1068326
Pereira HM, Leadley PW, Proença V et al (2010) Scenarios for global biodiversity in the 21st century. Science 330:1496–1501. doi:10.1126/science.1196624
Pimm SL, Jenkins CN, Abell R et al (2014) The biodiversity of species and their rates of extinction, distribution, and protection. Science 344:1246752. doi:10.1126/science.1246752
Redford K, Feinsinger P (2001) The half-empty forest: sustainable use and the ecology of interactions. In: Reynold D, Mace G, Redford K, Robinson J (eds) Conservation of exploited species. Cambridge University Press, UK, pp 370–399
Ripple WJ, Estes JA, Beschta RL et al (2014) Status and ecological effects of the world’s largest carnivores. Science 343:1241484. doi:10.1126/science.1241484
Säterberg T, Sellman S, Ebenman B (2013) High frequency of functional extinctions in ecological networks. Nature 499:468–470. doi:10.1038/nature12277
Sauve AMC, Fontaine C, Thébault E (2014) Structure–stability relationships in networks combining mutualistic and antagonistic interactions. Oikos 123:378–384. doi:10.1111/j.1600-0706.2013.00743.x
Sauve AMC, Fontaine C, Thébault E (2015) Stability of a diamond-shaped module with multiple interaction types. Theor Ecol. doi:10.1007/s12080-015-0260-1
Schipper J, Chanson JS, Chiozza F et al (2008) The status of the world’s land and marine mammals: diversity, threat, and knowledge. Science 322:225–230. doi:10.1126/science.1165115
Sekercioğlu ÇH, Daily GC, Ehrlich PR (2004) Ecosystem consequences of bird declines. Proc Natl Acad Sci 101:18042–18047. doi:10.1073/pnas.0408049101
Smith ADM, Brown CJ, Bulman CM et al (2011) Impacts of fishing low–trophic level species on marine ecosystems. Science 333:1147–1150. doi:10.1126/science.1209395
Soulé ME, Estes JA, Berger J, Del Rio CM (2003) Ecological effectiveness: conservation goals for interactive species. Conserv Biol 17:1238–1250. doi:10.1046/j.1523-1739.2003.01599.x
Soulé ME, Estes JA, Miller B, Honnold DL (2005) Strongly interacting species: conservation policy, management, and ethics. Bioscience 55:168–176. doi:10.1641/0006-3568(2005)055[0168:SISCPM]2.0.CO;2
Stouffer DB, Bascompte J (2011) Compartmentalization increases food-web persistence. Proc Natl Acad Sci 108:3648–3652. doi:10.1073/pnas.1014353108
Suweis S, Grilli J, Maritan A (2014) Disentangling the effect of hybrid interactions and of the constant effort hypothesis on ecological community stability. Oikos 123:525–532. doi:10.1111/j.1600-0706.2013.00822.x
Tang S, Pawar S, Allesina S (2014) Correlation between interaction strengths drives stability in large ecological networks. Ecol Lett. doi:10.1111/ele.12312
Thébault E, Huber V, Loreau M (2007) Cascading extinctions and ecosystem functioning: contrasting effects of diversity depending on food web structure. Oikos 116:163–173. doi:10.1111/j.2006.0030-1299.15007.x
Therneau T, Atkinson B, Ripley B (2014) RPART: recursive partitioning and regression trees. R package version 4.1-8
Acknowledgments
We thank two anonymous reviewers for their valuable comments. This work was financed through a Faculty grant from Linköping University.
Author information
Authors and Affiliations
Corresponding author
Appendix
Appendix
Rights and permissions
About this article
Cite this article
Sellman, S., Säterberg, T. & Ebenman, B. Pattern of functional extinctions in ecological networks with a variety of interaction types. Theor Ecol 9, 83–94 (2016). https://doi.org/10.1007/s12080-015-0275-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12080-015-0275-7