Abstract
Allee effects are an important dynamic phenomenon believed to be manifested in several population processes, notably extinction and invasion. Though widely cited in these contexts, the evidence for their strength and prevalence has not been critically evaluated. We review results from 91 studies on Allee effects in natural animal populations. We focus on empirical signatures that are used or might be used to detect Allee effects, the types of data in which Allee effects are evident, the empirical support for the occurrence of critical densities in natural populations, and differences among taxa both in the presence of Allee effects and primary causal mechanisms. We find that conclusive examples are known from Mollusca, Arthropoda, and Chordata, including three classes of vertebrates, and are most commonly documented to result from mate limitation in invertebrates and from predator–prey interactions in vertebrates. More than half of studies failed to distinguish component and demographic Allee effects in data, although the distinction is crucial to most of the population-level dynamic implications associated with Allee effects (e.g., the existence of an unstable critical density associated with strong Allee effects). Thus, although we find conclusive evidence for Allee effects due to a variety of mechanisms in natural populations of 59 animal species, we also find that existing data addressing the strength and commonness of Allee effects across species and populations is limited; evidence for a critical density for most populations is lacking. We suggest that current studies, mainly observational in nature, should be supplemented by population-scale experiments and approaches connecting component and demographic effects.
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References
Ackleh AS, Allen LJS, Carter J (2007) Establishing a beachhead: a stochastic population model with an Allee effect applied to species invasion. Theor Popul Biol 71:290–300. doi:10.1016/j.tpb.2006.12.006
Allee WC (1931) Animal aggregations. University of Chicago Press, Chicago
Allen LJS, Fagan JF, Hognas G, Fagerholm H (2005) Population extinction in discrete-time stochastic population models with an Allee effect. J Differ Equat Appl 11:273–293. doi:10.1080/10236190412331335373
Amarasekare P (1998) Allee effects in metapopulation dynamics. Am Nat 152:298–302. doi:10.1086/286169
Angulo E, Roemer GW, Berec L, Gascoigne J, Courchamp F (2007) Double Allee effects and extinction in the island fox. Conserv Biol 21:1082–1091. doi:10.1111/j.1523-1739.2007.00721.x
Barrowman NJ, Myers RA, Hilborn R, Kehler DG, Field CA (2003) The variability among populations of coho salmon in the maximum reproductive rate and depensation. Ecol Appl 13:784–793. doi:10.1890/1051-0761(2003)013[0784:TVAPOC]2.0.CO;2
Berec L, Angulo E, Courchamp F (2007) Multiple Allee effects and population management. Trends Ecol Evol 22:185–191. doi:10.1016/j.tree.2006.12.002
Boukal DS, Berec L (2002) Single-species models of the Allee effect: extinction boundaries, sex ratios and mate encounters. J Theor Biol 218:375–394. doi:10.1006/jtbi.2002.3084
Campbell MM (1976) Colonization of Aphytis melinus DeBach (Hymenoptera, Aphelinidae) in Aonidialla aurantii (Mask) (Hemiptera, Coccidae) on citrus in south Australia. Bull Entomol Res 65:659–668
Cappuccino N (2004) Allee effect in an invasive alien plant, pale swallow-wort Vincetoxicum rossicum (Asclepiadaceae). Oikos 106:3–8. doi:10.1111/j.0030-1299.2004.12863.x
Chen DG, Irvine JR, Cass AJ (2002) Incorporating Allee effects in fish stock-recruitment models and applications for determining reference points. Can J Fish Aquat Sci 59:242–249. doi:10.1139/f02-005
Clark CW (1976) Mathematical bioeconomics: the optimal management of renewable resources. Wiley, New York
Clutton-Brock TH, Gaynor D, McIlrath GM, Maccoll ADC, Kansky R, Chadwick P, Manser M, Skinner JD, Brotherton PNM (1999) Predation, group size and mortality in a cooperative mongoose, Suricata suricata. J Anim Ecol 68:672–683. doi:10.1046/j.1365-2656.1999.00317.x
Courchamp F, Macdonald DW (2001) Crucial importance of pack size in the African wild dog Lycaon pictus. Anim Conserv 4:169–174. doi:10.1017/S1367943001001196
Courchamp F, Clutton-Brock T, Grenfell B (1999) Inverse density dependence and the Allee effect. Trends Ecol Evol 14:405–410. doi:10.1016/S0169-5347(99)01683-3
Cuthbert R (2002) The role of introduced mammals and inverse density-dependent predation in the conservation of Hutton’s shearwater. Biol Conserv 108:69–78. doi:10.1016/S0006-3207(02)00091-5
Davis HG, Taylor CM, Civille JC, Strong DR (2004a) An Allee effect at the front of a plant invasion: spartina in a Pacific estuary. J Ecol 92:321–327. doi:10.1111/j.0022-0477.2004.00873.x
Davis HG, Taylor CM, Lambrinos JG, Strong DR (2004b) Pollen limitation causes an Allee effect in a wind-pollinated invasive grass (Spartina alterniflora). Proc Natl Acad Sci USA 101:13804–13807. doi:10.1073/pnas.0405230101
Dennis B (1989) Allee effects: population growth, critical density, and the chance of extinction. Nat Resour Model 3:481–538
Dennis B (2002) Allee effects in stochastic populations. Oikos 96:389–401. doi:10.1034/j.1600-0706.2002.960301.x
Dennis B, Patil GB (1984) The gamma distribution and weighted multimodal gamma distributions as models of population abundance. Math Biosci 68:187–212. doi:10.1016/0025-5564(84)90031-2
Deredec A, Courchamp F (2006) Combined impacts of Allee effects and parasitism. Oikos 112:667–679. doi:10.1111/j.0030-1299.2006.14243.x
Drake JM (2004) Allee effects and the risk of biological invasion. Risk Anal 24:795–802. doi:10.1111/j.0272-4332.2004.00479.x
Drake JM, Lodge DM (2006) Allee effects, propagule pressure and the probability of establishment: risk analysis for biological invasions. Biol Invas 8:365–375. doi:10.1007/s10530-004-8122-6
Dulvy NK, Freckleton RP, Polunin NVC (2004) Coral reef cascades and the indirect effects of predator removal by exploitation. Ecol Lett 7:410–416. doi:10.1111/j.1461-0248.2004.00593.x
Elam DR, Ridley CE, Goodell K, Ellstrandt NC (2007) Population size and relatedness affect fitness of a self-incompatible invasive plant. Proc Natl Acad Sci USA 104:549–552. doi:10.1073/pnas.0607306104
Fauvergue X, Malausa JC, Giuge L, Courchamp F (2007) Invading parasitoids suffer no Allee effect: a manipulative field experiment. Ecology 88:2392–2403. doi:10.1890/06-1238.1
Friedenberg NA, Powell JA, Ayres MP (2007) Synchrony’s double edge: transient dynamics and the Allee effect in stage structured populations. Ecol Lett 10:564–573. doi:10.1111/j.1461-0248.2007.01048.x
Gascoigne JC, Lipcius RN (2004) Allee effects driven by predation. J Appl Ecol 41:801–810. doi:10.1111/j.0021-8901.2004.00944.x
Gascoigne JC, Beadman HA, Saurel C, Kaiser MJ (2005) Density dependence, spatial scale and patterning in sessile biota. Oecologia 145:371–381. doi:10.1007/s00442-005-0137-x
Gascoigne J, Berec L, Gregory S, Courchamp F (2009) Dangerously few liaisons: a review of mate-finding Allee effects. Popul Ecol. doi:10.1007/s10144-009-0146-4
Gerber LR, Hilborn R (2001) Catastrophic events and recovery from low densities in populations of otariids: implications for risk of extinction. Mammal Rev 31:131–150. doi:10.1046/j.1365-2907.2001.00081.x
Gerritsen J (1980) Sex and parthenogenesis in sparse populations. Am Nat 115:718–742. doi:10.1086/283594
Hastings A (1996) Models of spatial spread: a synthesis. Biol Conserv 78:143–148. doi:10.1016/0006-3207(96)00023-7
Hays GC (2004) Good news for sea turtles. Trends Ecol Evol 19:349–351. doi:10.1016/j.tree.2004.05.009
Hoddle MS (1991) Lifetable construction for the gorse seed weevil, Apion ulicis (Forster) (Coleoptera, Apionidae) before gorse pod dehiscence, and life-history strategies of the weevil. NZ J Zool 18:399–404
Hopper KR, Roush RT (1993) Mate-finding, dispersal, number released, and the success of biological-control introductions. Ecol Entomol 18:321–331. doi:10.1111/j.1365-2311.1993.tb01108.x
Johnson DM, Liebhold AM, Tobin PC, Bjornstad ON (2006) Allee effects and pulsed invasion by the gypsy moth. Nature 444:361–363. doi:10.1038/nature05242
Jordal BH, Beaver RA, Kirkendall LR (2001) Breaking taboos in the tropics: incest promotes colonization by wood-boring beetles. Glob Ecol Biogeogr 10:345–357. doi:10.1046/j.1466-822X.2001.00242.x
Kent A, Hawkins SJ, Doncaster CP (2003) Population consequences of mutual attraction between settling and adult barnacles. J Anim Ecol 72:941–952. doi:10.1046/j.1365-2656.2003.00762.x
Kramer AM, Sarnelle O, Knapp RA (2008) Allee effect limits colonization success of sexually reproducing zooplankton. Ecology 89:2760–2769. doi:10.1890/07-1505.1
Kuussaari M, Saccheri I, Camara M, Hanski I (1998) Allee effect and population dynamics in the Glanville fritillary butterfly. Oikos 82:384–394. doi:10.2307/3546980
Lamont BB, Klinkhamer PGL, Witkowski ETF (1993) Population fragmentation may reduce fertility to zero in Banksia goodi: a demonstration of the Allee effect. Oecologia 94:446–450. doi:10.1007/BF00317122
Lewis MA, Kareiva P (1993) Allee dynamics and the spread of invading organisms. Theor Popul Biol 43:141–158. doi:10.1006/tpbi.1993.1007
Liebhold A, Bascompte J (2003) The Allee effect, stochastic dynamics and the eradication of alien species. Ecol Lett 6:133–140. doi:10.1046/j.1461-0248.2003.00405.x
Liebhold AM, Tobin PC (2006) Growth of newly established alien populations: comparison of North American gypsy moth colonies with invasion theory. Popul Ecol 48:253–262. doi:10.1007/s10144-006-0014-4
Liermann M, Hilborn R (1997) Depensation in fish stocks: a hierarchic Bayesian meta-analysis. Can J Fish Aquat Sci 54:1976–1984. doi:10.1139/cjfas-54-9-1976
Lundquist CJ, Botsford LW (2004) Model projections of the fishery implications of the Allee effect in broadcast spawners. Ecol Appl 14:929–941. doi:10.1890/02-5325
Martcheva M, Bolker BM (2007) The impact of the Allee effect in dispersal and patch-occupancy age on the dynamics of metapopulations. Bull Math Biol 69:135–156. doi:10.1007/s11538-006-9075-y
McCormick MI (2006) Mothers matter: crowding leads to stressed mothers and smaller offspring in marine fish. Ecology 87:1104–1109. doi:10.1890/0012-9658(2006)87[1104:MMCLTS]2.0.CO;2
Menendez R, Gutierrez D, Thomas CD (2002) Migration and Allee effects in the six-spot burnet moth Zygaena filipendulae. Ecol Entomol 27:317–325. doi:10.1046/j.1365-2311.2002.00404.x
Mooring MS, Fitzpatrick TA, Nishihira TT, Reisig DD (2004) Vigilance, predation risk, and the Allee effect in desert bighorn sheep. J Wildl Manage 68:519–532. doi:10.2193/0022-541X(2004)068[0519:VPRATA]2.0.CO;2
Morozov A, Petrovskii S, Li BL (2004) Bifurcations and chaos in a predator–prey system with the Allee effect. Proc R Soc Lond B Biol Sci 271:1407–1414. doi:10.1098/rspb.2004.2733
Munoz-Duran J (2002) Correlates of speciation and extinction rates in the Carnivora. Evol Ecol Res 4:963–991
Myers RA, Barrowman NJ, Hutchings JA, Rosenberg AA (1995) Population-dynamics of exploited fish stocks at low population-levels. Science 269:1106–1108. doi:10.1126/science.269.5227.1106
Quinn JF, Wing SR, Botsford LW (1993) Harvest refugia in marine invertebrate fisheries: models and applications to the red sea urchin Strongylocentrotus franciscanus. Am Zool 33:537–550
Sæther BE, Ringsby TH, Roskaft E (1996) Life history variation, population processes and priorities in species conservation: towards a reunion of research paradigms. Oikos 77:217–226. doi:10.2307/3546060
Soutullo A, Liminana R, Urios V, Surroca M, Gill JA (2006) Density-dependent regulation of population size in colonial breeders: Allee and buffer effects in the migratory Montagu’s harrier. Oecologia 149:543–552. doi:10.1007/s00442-006-0465-5
Stephens PA, Sutherland WJ (1999) Consequences of the Allee effect for behaviour, ecology and conservation. Trends Ecol Evol 14:401–405. doi:10.1016/S0169-5347(99)01684-5
Stephens PA, Sutherland WJ, Freckleton RP (1999) What is the Allee effect? Oikos 87:185–190. doi:10.2307/3547011
Stephens PA, Frey-Roos F, Arnold W, Sutherland WJ (2002) Model complexity and population predictions: the alpine marmot as a case study. J Anim Ecol 71:343–361. doi:10.1046/j.1365-2656.2002.00605.x
Stoner AW, Ray-Culp M (2000) Evidence for Allee effects in an over-harvested marine gastropod: density-dependent mating and egg production. Mar Ecol Prog Ser 202:297–302. doi:10.3354/meps202297
Taylor CM, Hastings A (2005) Allee effects in biological invasions. Ecol Lett 8:895–908. doi:10.1111/j.1461-0248.2005.00787.x
Tobin PC, Whitmire SL, Johnson DM, Bjornstad ON, Liebhold AM (2007) Invasion speed is affected by geographical variation in the strength of Allee effects. Ecol Lett 10:36–43. doi:10.1111/j.1461-0248.2006.00991.x
Veit RR, Lewis MA (1996) Dispersal, population growth, and the Allee effect: dynamics of the house finch invasion of eastern North America. Am Nat 148:255–274. doi:10.1086/285924
Wallin KF, Raffa KF (2004) Feedback between individual host selection behavior and population dynamics in an eruptive herbivore. Ecol Monogr 74:101–116. doi:10.1890/02-4004
Walters C, Kitchell JF (2001) Cultivation/depensation effects on juvenile survival and recruitment: implications for the theory of fishing. Can J Fish Aquat Sci 58:39–50. doi:10.1139/cjfas-58-1-39
Wang MH, Kot M (2001) Speeds of invasion in a model with weak or strong Allee effects. Math Biosci 171:83–97. doi:10.1016/S0025-5564(01)00048-7
Wittmer HU, Sinclair ARE, McLellan BN (2005) The role of predation in the decline and extirpation of woodland caribou. Oecologia 144:257–267. doi:10.1007/s00442-005-0055-y
Zhou SR, Liu CZ, Wang G (2004) The competitive dynamics of metapopulations subject to the Allee-like effect. Theor Popul Biol 65:29–37. doi:10.1016/j.tpb.2003.08.002
Acknowledgments
We thank Blaine Griffen, Andrea Silletti, Philip Stephens, David Boukal, and three anonymous reviewers for suggestions on an earlier version of this manuscript. Funding for this project was provided by the University of Georgia and a grant from the Great Lakes Protection Fund.
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S2: Supplemental figure. The percentage of studies detecting demographic Allee effects that are strong, weak or unknown strength separated by a) type of study and b) type of evidence.(DOC 35 kb)
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Kramer, A.M., Dennis, B., Liebhold, A.M. et al. The evidence for Allee effects. Popul Ecol 51, 341–354 (2009). https://doi.org/10.1007/s10144-009-0152-6
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DOI: https://doi.org/10.1007/s10144-009-0152-6