Abstract
An ecological theory (HSS hypothesis) predicts that carnivores maintain the terrestrial ecosystem with abundant plants (green world) by regulating herbivore abundance. However, a weak density dependence of herbivores will make the equilibrium unstable and results in population oscillations with a large amplitude. Here, we study a possibility that the dynamics can be stabilized if defence trait by herbivores and offence trait by carnivores change in an adaptive manner. When the cost constraints on adaptation are strong in both the herbivores and the carnivores, the equilibrium is more likely to be stable if the herbivore adapts more quickly than the carnivore. When the constraints on the adaptation are asymmetric between species, the equilibrium is likely to be unstable. We conclude that the green world may be maintained by fast and costly adaptation by the herbivore through mechanisms such as phenotypic plasticity and behavioural change. Plant defence which is poisonous and prickly has been proposed as one of explanations, however, world can be green through adaptation in higher trophic levels even without plant’s defence.
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References
Abrams PA (1982) Functional responses of optimal foragers. Am Nat 120:382–390
Abrams PA (1986) Adaptive responses of predators to prey and prey to predators: the failure of the arms race analogy. Evolution 40:1229–1247
Abrams PA (1992) Adaptive foraging by predators as a cause of predator-prey cycles. Evol Ecol 6:56–72
Abrams PA (2000) The evolution of predator–prey interactions: theory and evidence. Annu Rev Ecol Syst 31:79–105
Abrams PA (2003) Can adaptive evolution or behaviour lead to diversification of traits determining a trade-off between foraging gain and predation risk? Evol Ecol Res 5:653–670
Abrams PA, Matsuda H (1997a) Fitness minimization and dynamic instability as a consequence of predator-prey coevolution. Evol Ecol 11:1–20
Abrams PA, Matsuda H (1997b) Prey evolution as a cause of predator-prey cycles. Evolution 51:1740–1748
Abrams PA, Vos M (2003) Adaptation, density dependence, and the abundances of trophic levels. Evol Ecol Res 5:1113–1132
Abrams PA, Harada Y, Matsuda H (1993) Unstable fitness maxima and stable fitness minima in the evolution of continuous traits. Evol Ecol 7:465–487
Agrawal AA (2001) Phenotypic plasticity in the interactions and evolution of species. Science 294:321–326
Benkman CW, Holimon WC, Smith JW (2001) The influence of a competitor on the geographic mosaic of coevolution between crossbills and lodgepole pine. Evolution 55:282–294
Berenbaum MR, Zangerl AR (1992) Genetics of physiological and behavioural resistance to host furanocoumarins in the parsnip webworm. Evolution 46:1373–1384
Bergelson J, Dawyer G, Emerson JJ (2001) Models and data on plant-enemy coevolution. Annu Rev Genet 35:469–499
Brodie ED Jr, Ridenhour BJ, III Brodie ED (2002) The evolutionary response of predators to dangerous prey: hot spots and cold spots in the geographic mosaic of coevolution between garter snakes and newts. Evolution 56:2067–2082
Buckling A, Rainey PB (2002) Antagonistic coevolution between a bacterium and a bacteriophage. Proc R Soc B 269:931–936
Buckling A, Wei Y, Massey RC, Brockhurst MA, Hochberg ME (2006) Antagonistic coevolution with parasites increases the cost of host deleterious mutations. Proc R Soc B 273:45–49
Chase JM (2000) Are there real differences among aquatic and terrestrial food webs? Trends Ecol Evol 15:408–412
Damman H (1993) Patterns of interaction among herbivore species. In: Stamp NE, Casey TM (eds) Caterpillars ecological and evolutionary constraints on foraging. Chapman and Hall, New York, pp 132–169
Denno RF, McClure MS, Ott JR (1995) Interspecific interactions in phytophagous insects: competition reexamined and resurrected. Annu Rev Entomol 40:297–331
Doebeli M (1997) Genetic variation and the persistence of predator-prey interactions in the Nicholson-Bailey model. J Theor Biol 188:109–120
Forde SE, Thompson JN, Bohannan BJM (2004) Adaptation varies through space and time in a coevolving host–parasitoid interaction. Nature 431:841–844
Forde SE, Thompson JN, Bohannan BJM (2007) Gene flow reverses an adaptive cline in a coevolving host–parasitoid interaction. Am Nat 169:794–801
Frank SA (1994) Coevolutionary genetics of hosts and parasites with quantitative inheritance. Evol Ecol 8:74–94
Friman V-P, Hiltunen T, Laakso J, Kaitala V (2008) Availability of prey resources drives evolution of predator–prey interaction. Proc R Soc B 275:1625–1633
Hairston NG, Smith FE, Slobodkin LB (1960) Community structure, population control, and competition. Am Nat 94:421–425
Halaj J, Wise DH (2001) Terrestrial trophic cascades: how much do they trickle? Am Nat 157:262–281
Hassell MP, May RM (1973) Stability in insect host-parasite models. J Anim Ecol 42:693–736
Ives AR, Dobson AP (1987) Antipredator behaviour and the population dynamics of simple predator-prey systems. Am Nat 130:431–447
Iwasa Y, Pomiankowski A, Nee S (1991) The evolution of costly mate preferences: II. The ‘handicap’ principle. Evolution 45:1431–1442
Kishida O, Mizuta Y, Nishimura K (2006) Reciprocal phenotypic plasticity in a predator–prey interaction between larval amphibians. Ecology 87:1599–1604
Kopp M, Tollrian R (2003) Reciprocal phenotypic plasticity in a predator–prey system: inducible offences against inducible defences? Ecol Lett 6:742–748
Lawton JH (1984) Non-competitive populations, non-convergent communities, and vacant niches: the herbivores of bracken. In: Strong DR, Simberloff D, Abele LG, Thistle AB (eds) Ecological communities: conceptual issues and evidence. Princeton University Press, Princeton, pp 67–99
Lawton JH, Strong DR (1981) Community patterns in folivorous insects. Am Nat 118:317–338
Levin SA (1983) Coevolution. In: Freedman H, Strobeck C (eds) Population biology. Lecture Notes in Biomathematics 52. Springer, Berlin, pp 328–334
Levin SA (1999) Fragile dominion: complexity and the commons. Perseus, Reading
Lima SL (2002) Putting predators back into behavioral predator–prey interactions. Trends Ecol Evol 17:70–75
Lopez-Pascua LDC, Buckling A (2008) Increasing productivity accelerates host–parasite co-evolution. J Evol Biol 21:853–860
May RM, Hassell MP (1981) The dynamics of multi parasitoid–host interactions. Am Nat 117:234–261
Moran N (1992) The evolutionary maintenance of alternative phenotypes. Am Nat 139:971–989
Mougi A, Iwasa Y (2010) Evolution towards oscillation or stability in a predator–prey system. Proc R Soc B 277:3163–3171
Mougi A, Kishida O (2009) Reciprocal phenotypic plasticity can lead to stable predator–prey interaction. J Anim Ecol 78:1172–1181
Mougi A, Kishida O, Iwasa Y (2011) Coevolution of phenotypic plasticity in predator and prey: why are inducible offenses rarer than inducible defenses? Evolution (in press)
Nicholson AJ, Bailey VA (1935) The balance of animal populations. Part I. Proc Zool Soc Lond 1935:551–598
Nuismer SL, Ridenhour BJ, Oswald B (2007) Antagonistic coevolution mediated by phenotypic differences between quantitative traits. Evolution 61:1823–1834
Oksanen L, Fretwell SD, Arruda J, Niemelä P (1981) Exploitation ecosystems in gradients of primary productivity. Am Nat 118:240–261
Polis GA (1999) Why are parts of the world green? Multiple factors control productivity and the distribution of biomass. Oikos 86:3–15
Rosenzweig ML (1971) Paradox of enrichment: destabilization of exploitation ecosystems in ecological time. Science 171:385–387
Rosenzweig ML, MacArthur RH (1963) Graphical representation and stability conditions of predator-prey interactions. Am Nat 97:209–223
Saloniemi I (1993) A coevolutionary predator-prey model with quantitative characters. Am Nat 141:880–896
Sasaki A, Godfray HCJ (1999) A model for the coevolution of resistnace and virulence in coupled host-parasitoid interactions. Proc R Soc B 266:455–463
Schmitz OJ, Krivan V, Ovadia O (2004) Trophic cascades: the primacy of trait-mediated indirect interactions. Ecol Lett 7:153–163
Schultz JC, Baldwin IT (1982) Oak leaf quality declines in response to defoliation by gypsy moth larvae. Science 217:149–151
Shorrocks B, Rosewell J, Edwards K, Atkinson W (1984) Interspecific competition is not a major organizing force in many insect communities. Nature 310:310–312
Shurin JB, Borer ET, Seabloom EW, Anderson K, Blanchette CA, Broitman B, Cooper SD, Halpern BS (2002) A cross-ecosystem comparison of the strength of trophic cascades. Ecol Lett 5:785–791
Smith LD, Palmer AR (1994) Effects of manipulated diet on size and performance of brachyuran crab claws. Science 264:710–712
Soler JJ, Aviles JM, Soler M, Moller AP (2003) Evolution of host egg mimicry in a brood parasite, the great spotted cuckoo. Biol J Linn Soc 79:551–563
Strong DR (1983) Natural variability and the manifold mechanisms of ecological communities. Am Nat 122:636–660
Strong DR (1992) Are trophic cascades all wet? Differentiation and donor-control in speciose ecosystems. Ecology 73:747–754
Takimoto G (2003) Adaptive plasticity in ontogenetic niche shifts stabilizes consumer–resource dynamics. Am Nat 162:93–109
Toju H, Sota T (2006) Imbalance of predator and prey armament: geographic clines in phenotypic interface and natural selection. Am Nat 167:105–117
Tollrian R, Harvell CD (1999) The ecology and evolution of inducible defenses. Princeton University Press, Princeton
Trussell GC (1996) Phenotypic plasticity in an intertidal snail: the role of a common crab predator. Evolution 50:448–454
van Baalen M, Sabelis MW (1993) Coevolution of patch selection strategies og predator and prey and the consequences for ecological stability. Am Nat 142:646–670
Van der Stap I, Vos M, Verschoor AM, Helmsing NR, Mooij WM (2007) Induced defenses in herbivores and plants differentially modulate a trophic cascade. Ecology 88:2474–2481
Verschoor AM, Vos M, Van der Stap I (2004) Inducible defences prevent strong population fluctuations in bi- and tritrophic food chains. Ecol Lett 7:1143–1148
Vos M, Kooi BW, DeAngelis DL, Mooij WM (2004) Inducible defences and the paradox of enrichment. Oikos 105:471–480
Wootton JT (1994) The nature and consequences of indirect effects in ecological communities. Annu Rev Ecol Syst 25:443–466
Yamauchi A, Yamamura N (2005) Effects of defense evolution and diet choice on population dynamics in a one-predator–two-prey system. Ecology 86:2513–2524
Yoshida T, Jones LE, Ellner SP, Fussmann GF, Hairston NG (2003) Rapid evolution drives ecological dynamics in a predator–prey system. Nature 424:303–306
Acknowledgments
We are very grateful to P. A. Abrams, S. P. Ellner and K. Uriu for their valuable advice on this study. This study was supported by a Grant-in-Aid for a Research Fellow from the Japan Society for the Promotion of Science and a Research Fellowship for Young Scientists (no. 20*01655) to A. M. and by a Grant-in-Aid (B) to Y. I.
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Mougi, A., Iwasa, Y. Green world maintained by adaptation. Theor Ecol 4, 201–210 (2011). https://doi.org/10.1007/s12080-011-0114-4
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DOI: https://doi.org/10.1007/s12080-011-0114-4