Population Ecology

, Volume 51, Issue 1, pp 105–113 | Cite as

Resource-dependent reproductive adjustment and the stability of consumer-resource dynamics

  • Takefumi Nakazawa
  • Takayuki Ohgushi
  • Norio Yamamura
Original Article


This study explored a consumer-resource model including reproductive and nonreproductive subpopulations of the consumer to consider whether resource-dependent reproductive adjustment by the consumer would stabilize consumer-resource dynamics. The model assumed that decreasing (increasing) resource availability caused reproductive suppression (facilitation), and that the reproductive consumer had a higher mortality rate than the nonreproductive one (i.e., a trade-off between reproduction and survival). The model predicted that the variability would be reduced when the consumer had a strong tendency to suppress reproduction in response to low resource availability or when the cost of reproduction was high, although consumer extinction became more likely. Furthermore, when the consumer-resource dynamics converged to limit cycles, reproductive adjustment enhanced the long-term average of the consumer density. It was also predicted that if reproductive suppression enhanced resource consumption efficiency (i.e., a trade-off between reproduction and foraging), then it would destabilize the system by canceling the stabilizing effect of the reproductive adjustment itself. These results suggest that it is necessary not only to identify the costs of reproduction, but also to quantify the changes in individual-level performances due to reproduction in order to understand the ecological consequences of reproductive adjustment.


Breeding suppression Phenotypic plasticity Population cycle Prey–predator interaction Reproductive strategy 



We thank three anonymous referees for their valuable comments. This research was financially supported in part by the Global COE Program A06 to Kyoto University. TN was also supported by a Japan Society for the Promotion of Science Research Fellowship for Young Scientists (1702360).


  1. Abrams PA (2000) The evolution of predator–prey interactions: theory and evidence. Annu Rev Ecol Syst 31:79–105. doi: 10.1146/annurev.ecolsys.31.1.79 CrossRefGoogle Scholar
  2. Abrams PA, Namba T, Mimura M, Roth JD (1997) The relationship between productivity and population densities in cycling predator–prey systems. Evol Ecol 11:371–373. doi: 10.1023/A:1018424605347 CrossRefGoogle Scholar
  3. Abrams PA, Holt RD, Roth JD (1998) Apparent competition or apparent mutualism? Shared predation when populations cycle. Ecology 79:201–212. doi: 10.2307/176875 CrossRefGoogle Scholar
  4. Abrams PA, Brassil CE, Holt RD (2003) Dynamics and responses to mortality rates of competing predators undergoing predator–prey cycles. Theor Popul Biol 64:163–176. doi: 10.1016/S0040-5809(03)00067-4 PubMedCrossRefGoogle Scholar
  5. Bolker B, Holyoak M, Kŕivan V, Rowe L, Schmitz S (2003) Connecting theoretical and empirical studies of trait-mediated interactions. Ecology 84:1101–1114. doi: 10.1890/0012-9658(2003)084[1101:CTAESO]2.0.CO;2 CrossRefGoogle Scholar
  6. Caswell H (1989) Matrix population models: construction, analysis, and interpretation. Sinauer, SunderlandGoogle Scholar
  7. Clutton-Brock TH (1988) Reproductive success. University of Chicago Press, ChicagoGoogle Scholar
  8. Clutton-Brock TH, Guiness FE, Albon SD (1982) Red deer: behavior and ecology of two sexes. University of Chicago Press, ChicagoGoogle Scholar
  9. De Neve L, Soler JJ, Soler M, Pérez-Contreras T, Martín-Vivaldi M, Martínez JG (2004) Effects of a food supplementation experiment on reproductive investment and a post-mating sexually selected trait in magpies Pica pica. J Avian Biol 35:246–251. doi: 10.1111/j.0908-8857.2004.03162.x CrossRefGoogle Scholar
  10. Doughty P, Shine R (1998) Reproductive energy allocation and long-term energy stores in a viviparous lizard (Eulamprus tympanum). Ecology 79:1073–1083. doi: 10.1890/0012-9658(1998)079[1073:REAALT]2.0.CO;2 Google Scholar
  11. Du WG (2006) Phenotypic plasticity in reproductive traits induced by food availability in a lacertid lizard, Takydromus septentrionalis. Oikos 112:363–369. doi: 10.1111/j.0030-1299.2006.13552.x CrossRefGoogle Scholar
  12. Engqvist L, Sauer KP (2003) Influence of nutrition on courtship and mating in the scorpionfly Panorpa cognata (Mecoptera, Insecta). Ethology 109:911–928. doi: 10.1046/j.1439-0310.2003.00937.x CrossRefGoogle Scholar
  13. Erikstad KE, Fauchald P, Tveraa T, Steen H (1998) On the cost of reproduction in long-lived birds: the influence of environmental variability. Ecology 79:1781–1788. doi: 10.1890/0012-9658(1998)079[1781:OTCORI]2.0.CO;2 Google Scholar
  14. Festa-Bianchet M, Jorgenson JT (1998) Selfish mothers: reproductive expenditure and resource availability in bighorn ewes. Behav Ecol 9:144–150. doi: 10.1093/beheco/9.2.136, 10.1093/beheco/9.2.144 CrossRefGoogle Scholar
  15. Ford NB, Seigel RA (1989) Phenotypic plasticity in reproductive traits: evidence from a viviparous snake. Ecology 70:1768–1774. doi: 10.2307/1938110 CrossRefGoogle Scholar
  16. Ghalambor CK, McKay JK, Carroll SP, Reznick DN (2007) Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Funct Ecol 21:394–407. doi: 10.1111/j.1365-2435.2007.01283.x CrossRefGoogle Scholar
  17. Gustafsson L, Sutherland WJ (1988) The costs of reproduction in the collared flycatcher Ficedula albicollis. Nature 335:813–815. doi: 10.1038/335813a0 CrossRefGoogle Scholar
  18. Gwynne DT (1989) Does copulation increase the risk of predation? Trends Ecol Evol 4:54–56. doi: 10.1016/0169-5347(89)90144-4 CrossRefGoogle Scholar
  19. Gyllenberg M, Hanski I, Lindström T (1996) A predator–prey model with optimal suppression of reproduction in the prey. Math Biosci 134:119–152. doi: 10.1016/0025-5564(95)00082-8 PubMedCrossRefGoogle Scholar
  20. Gyllström M, Hansson LA (2004) Dormancy in freshwater zooplankton: induction, termination and the importance of benthic-pelagic coupling. Aquat Sci 66:274–295. doi: 10.1007/s00027-004-0712-y CrossRefGoogle Scholar
  21. Hairston NG Jr, Van Brunt RA, Kearns CM (1995) Age and survivorship of diapausing eggs in a sediment egg bank. Ecology 76:1706–1711. doi: 10.2307/1940704 CrossRefGoogle Scholar
  22. Harshman LG, Zera AJ (2006) The cost of reproduction: the devil in the details. Trends Ecol Evol 22:80–86. doi: 10.1016/j.tree.2006.10.008 PubMedCrossRefGoogle Scholar
  23. Jacobsen KO, Erikstad KE, Sæther BE (1995) An experimental study of the costs of reproduction in the Kittiwake Rissa tridactyla. Ecology 76:1636–1642CrossRefGoogle Scholar
  24. Johnson MTJ, Stinchcombe JR (2007) An emerging synthesis between community ecology and evolutionary biology. Trends Ecol Evol 22:250–257. doi: 10.1016/j.tree.2007.01.014 PubMedCrossRefGoogle Scholar
  25. Kagata H, Ohgushi T (2001) Clutch size adjustment of a leaf-mining moth (Lyonetiidae: Lepidoptera) in response to resource availability. Ann Entomol Soc Am 95:213–217. doi: 10.1603/0013-8746(2002)095[0213:CSAOAL]2.0.CO;2 CrossRefGoogle Scholar
  26. Klemetsen A, Amundsen PA, Dempson JB, Jonsson B, Jonsson N, O’Connell MF, Mortensen E (2003) Atlantic salmon Salmo salar L., brown trout Salmo trutta L. and Arctic charr Salvelinus alpinus (L.): a review of aspects of their life histories. Ecol Freshw Fish 12:1–59. doi: 10.1034/j.1600-0633.2003.00010.x CrossRefGoogle Scholar
  27. Kokko H, Ranta E (1996) Evolutionary optimality of delayed breeding in voles. Oikos 77:173–175. doi: 10.2307/3545599 CrossRefGoogle Scholar
  28. Kokko H, Ruxton GD (2000) Breeding suppression and predator–prey dynamics. Ecology 81:252–260. doi: 10.2307/177148 Google Scholar
  29. Kolluru GR, Grether GF (2004) The effects of resource availability on alternative mating tactics in guppies (Poecilia reticulata). Behav Ecol 16:294–300. doi: 10.1093/beheco/arh161 CrossRefGoogle Scholar
  30. Madsen T, Shine R (1999) The adjustment of reproductive threshold to prey abundance in a capital breeder. J Anim Ecol 68:571–580. doi: 10.1046/j.1365-2656.1999.00306.x CrossRefGoogle Scholar
  31. Marden JH, Rogina B, Montooth KL, Helfand SL (2003) Conditional tradeoffs between aging and organismal performance of Indy long-lived mutant flies. Proc Natl Acad Sci USA 100:3369–3373. doi: 10.1073/pnas.0634985100 PubMedCrossRefGoogle Scholar
  32. McCauley E, Nisbet RM, Murdoch WW, de Roos AM, Gurney WSC (1999) Large-amplitude cycles of Daphnia and its algal prey in enriched environments. Nature 402:653–656. doi: 10.1038/45223 CrossRefGoogle Scholar
  33. McNamara JM, Houston AI (1996) State-dependent life histories. Nature 380:215–221. doi: 10.1038/380215a0 PubMedCrossRefGoogle Scholar
  34. Meijer T, Drent R (1999) Re-examination of the capital and income dichotomy in breeding birds. Ibis 141:399–414CrossRefGoogle Scholar
  35. Miner BG, Sultan SE, Morgan SG, Padilla DK, Relyea RA (2005) Ecological consequences of phenotypic plasticity. Trends Ecol Evol 20:685–692. doi: 10.1016/j.tree.2005.08.002 PubMedCrossRefGoogle Scholar
  36. Moehrlin GS, Juliano SA (1998) Plasticity of insect reproduction: testing models of flexible and fixed development in response to different growth rates. Oecologia 115:492–500. doi: 10.1007/s004420050546 CrossRefGoogle Scholar
  37. Munday PL, Buston PM, Warner RR (2005) Diversity and flexibility of sex-change strategies in animals. Trends Ecol Evol 21:89–95. doi: 10.1016/j.tree.2005.10.020 PubMedCrossRefGoogle Scholar
  38. Murdoch WW, Briggs CJ, Nisbet RM (2003) Consumer-resource dynamics. Princeton University Press, PrincetonGoogle Scholar
  39. Nagy L, Holmes RT (2005) Food limits annual fecundity of a migratory songbird: an experimental study. Ecology 86:675–681. doi: 10.1890/04-0155 CrossRefGoogle Scholar
  40. Naulleau G, Bonnet X (1996) Body condition threshold for breeding in a viviparous snake. Oecologia 107:301–306. doi: 10.1007/BF00328446 CrossRefGoogle Scholar
  41. Nilsson JA, Svensson E (1996) The cost of reproduction: a new link between current reproductive effort and future reproductive success. Proc R Soc B 263:711–714. doi: 10.1098/rspb.1996.0106 CrossRefGoogle Scholar
  42. Norrdahl K, Korpimäki E (1995) Does predation risk constrain maturation in cyclic vole populations? Oikos 72:263–272. doi: 10.2307/3546228 CrossRefGoogle Scholar
  43. Ohgushi T (1991) Lifetime fitness and evolution of reproductive pattern in the herbivorous lady beetle. Ecology 72:2110–2122. doi: 10.2307/1941563 CrossRefGoogle Scholar
  44. Ohgushi T (1996) A reproductive trade-off in an herbivorous lady beetle: egg resorption and female survival. Oecologia 106:345–351. doi: 10.1007/BF00334562 CrossRefGoogle Scholar
  45. Ohgushi T (1998) Bottom-up population regulation of a herbivorous lady beetle: an evolutionary perspective. In: Dempster JP, McLean IFG (eds) Insect populations in theory and in practice. Kluwer, Dordrecht, pp 367–390Google Scholar
  46. Ohgushi T (2005) Indirect interaction webs: herbivore-induced effects through trait change in plants. Annu Rev Ecol Evol Syst 36:81–105. doi: 10.1146/annurev.ecolsys.36.091704.175523 CrossRefGoogle Scholar
  47. Ohgushi T, Sawada H (1985) Population equilibrium with respect to available food resource and its behavioural basis in an herbivorous lady beetle, Henosepilachna niponica. J Anim Ecol 54:781–796. doi: 10.2307/4378 CrossRefGoogle Scholar
  48. Ohgushi T, Sawada H (1997a) A shift toward early reproduction in an introduced herbivorous ladybird. Ecol Entomol 22:90–96. doi: 10.1046/j.1365-2311.1997.00024.x CrossRefGoogle Scholar
  49. Ohgushi T, Sawada H (1997b) Population stability in relation to resource availability in an introduced population of an herbivorous lady beetle. Res Popul Ecol 39:37–45CrossRefGoogle Scholar
  50. Ohgushi T, Sawada H (1998) What changed the demography of an introduced population of an herbivorous lady beetle? J Anim Ecol 67:679–688. doi: 10.1046/j.1365-2656.1998.00225.x CrossRefGoogle Scholar
  51. Ohgushi T, Craig TP, Price PW (2007) Ecological communities: plant mediation in indirect interaction webs. Cambridge University Press, CambridgeGoogle Scholar
  52. Oksanen L, Lundberg P (1995) Optimization of reproductive effort and foraging in mammals: the influence of resource level and predation risk. Evol Ecol 9:45–56. doi: 10.1007/BF01237696 CrossRefGoogle Scholar
  53. Perrin N, Sibly RM (1993) Dynamic models of energy allocation and investment. Annu Rev Ecol Syst 24:379–410. doi: 10.1146/annurev.es.24.110193.002115 CrossRefGoogle Scholar
  54. Pigliucci M (2005) Evolution of phenotypic plasticity: where are we going now? Trends Ecol Evol 20:481–486. doi: 10.1016/j.tree.2005.06.001 PubMedCrossRefGoogle Scholar
  55. Pond D, Harris R, Head R, Harbour D (1996) Environmental and nutritional factors determining seasonal variability in the fecundity and egg viability of Calanus helgolandicus in coastal waters off Plymouth, UK. Mar Ecol Prog Ser 143:45–63. doi: 10.3354/meps143045 CrossRefGoogle Scholar
  56. Reznick DN (1985) Costs of reproduction: an evaluation of the empirical evidence. Oikos 44:257–267. doi: 10.2307/3544698 CrossRefGoogle Scholar
  57. Reznick DN (1992) Measuring the costs of reproduction. Trends Ecol Evol 7:42–45. doi: 10.1016/0169-5347(92)90104-J CrossRefGoogle Scholar
  58. Reznick DN, Yang A (1993) The influence of fluctuating resources on life history: patterns of allocation and plasticity in female guppies. Ecology 74:2011–2019. doi: 10.2307/1940844 CrossRefGoogle Scholar
  59. Römer U, Beisenherz W (1996) Environmental determination of sex in Apistogrammai (Cichlidae) and two other freshwater fishes (Teleostei). J Fish Biol 48:714–725. doi: 10.1111/j.1095-8649.1996.tb01467.x Google Scholar
  60. de Roos AM (1997) A gentle introduction to physiologically structured population models. In: Tuljapurkar S, Caswell H (eds) Structured-population models in marine, terrestrial, and freshwater systems. Chapman & Hall, New York, pp 119–204Google Scholar
  61. Rosenzweig ML, MacArthur RH (1963) Graphical representation and stability conditions of predator–prey interactions. Am Nat 97:209–223. doi: 10.1086/282272 CrossRefGoogle Scholar
  62. Ruxton GD, Lima SL (1997) Predator-induced breeding suppression and its consequences for predator–prey population dynamics. Proc R Soc B 264:409–415. doi: 10.1098/rspb.1997.0058 CrossRefGoogle Scholar
  63. Ruxton GD, Khan QJA, Al-Lawatia M (2002) The stability of internal equilibria in predator–prey models with breeding suppression. IMA J Math Appl Med Biol 19:207–219. doi: 10.1093/imammb/19.3.207 PubMedCrossRefGoogle Scholar
  64. Saitoh T (1989) Effects of added food on some attributes of an enclosed vole population. J Mammal 70:772–782. doi: 10.2307/1381711 CrossRefGoogle Scholar
  65. Schmitz OJ, Adler FR, Agrawal AA (2003) Linking individual-scale trait plasticity to community dynamics. Ecology 84:1081–1082. doi: 10.1890/1051-0761(2003)084[1081:LITPTC]2.0.CO;2 CrossRefGoogle Scholar
  66. Sheldon BC, Verhulst S (1996) Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol Evol 11:317–321. doi: 10.1016/0169-5347(96)10039-2 CrossRefGoogle Scholar
  67. Shine R (1980) “Costs” of reproduction in reptiles. Oecologia 46:92–100. doi: 10.1007/BF00346972 CrossRefGoogle Scholar
  68. Shine R, Madsen T (1997) Prey abundance and predator reproduction: rats and pythons on a tropical Australian floodplain. Ecology 78:1078–1086. doi: 10.2307/2265859 Google Scholar
  69. Siems DP, Sikes RS (1998) Tradeoffs between growth and reproduction in response to temporal variation in food supply. Environ Biol Fish 53:319–329. doi: 10.1023/A:1007407925835 CrossRefGoogle Scholar
  70. Stearns SC (1992) The evolution of life histories. University of Oxford Press, OxfordGoogle Scholar
  71. Stearns SC, Koella JC (1986) The evolution of phenotypic plasticity in life-history traits: predictions of reaction norms for age and size at maturity. Evolution 40:893–913. doi: 10.2307/2408752 CrossRefGoogle Scholar
  72. Via S, Gomulkiewicz R, De Jong G, Scheiner SM, Schlichting CD, Van Tienderen PH (2001) Adaptive phenotypic plasticity: consensus and controversy. Trends Ecol Evol 10:212–217. doi: 10.1016/S0169-5347(00)89061-8 CrossRefGoogle Scholar
  73. Wedekind C (2002) Induced hatching to avoid infectious egg disease in whitefish. Curr Biol 12:69–71. doi: 10.1016/S0960-9822(01)00627-3 PubMedCrossRefGoogle Scholar
  74. Werner EE, Peacor SD (2003) A review of trait-mediated indirect interactions in ecological communities. Ecology 84:1083–1100. doi: 10.1890/0012-9658(2003)084[1083:AROTII]2.0.CO;2 CrossRefGoogle Scholar
  75. Ylönen H (1994) Vole cycles and antipredatory behaviour. Trends Ecol Evol 9:426–430. doi: 10.1016/0169-5347(94)90125-2 CrossRefGoogle Scholar
  76. Young JL, Bornik ZB, Marcotte ML, Charlie KN, Wagner GN, Hinch SG, Cooke SJ (2006) Integrating physiology and life history to improve fisheries management and conservation. Fish Fish 7:262–283. doi: 10.1111/j.1467-2979.2006.00225.x Google Scholar
  77. Zera AJ, Harshman LG (2001) The physiology of life history trade-offs in animals. Annu Rev Ecol Syst 32:95–126. doi: 10.1146/annurev.ecolsys.32.081501.114006 CrossRefGoogle Scholar

Copyright information

© The Society of Population Ecology and Springer 2008

Authors and Affiliations

  • Takefumi Nakazawa
    • 1
  • Takayuki Ohgushi
    • 1
  • Norio Yamamura
    • 2
  1. 1.Center for Ecological ResearchKyoto UniversityShigaJapan
  2. 2.Research Institute for Humanity and NatureKyotoJapan

Personalised recommendations