Maternal effects mechanism of population cycling: A formidable competitor to the traditional predator-prey view

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 364, Issue 1520, 2009, Pages 1117-1124

  Inchausti, Pablo ^a   Ginzburg, Lev R ^b  

^a CNRS   (France)

^b STONY BROOK UNIVERSITY   (United States)

Author keywords

Delayed density dependence; Individual quality; Maternal effects; Population cycles; Predator prey dynamics; Reproductive allocation

Indexed keywords

DENSITY DEPENDENCE; FOOD CHAIN; HOST-PARASITE INTERACTION; LOTKA-VOLTERRA MODEL; MATERNAL EFFECT; POPULATION CYCLE; POPULATION GROWTH; PREDATOR-PREY INTERACTION; RESOURCE ALLOCATION;

ANIMAL; BIOLOGICAL MODEL; BREEDING; ENVIRONMENT; FEMALE; GROWTH, DEVELOPMENT AND AGING; MALE; MATERNAL BEHAVIOR; PARASITE; PHYSIOLOGY; POPULATION DENSITY; POPULATION DYNAMICS; POPULATION GROWTH; PREDATION; REPRODUCTION; REVIEW;

ANIMALS; BREEDING; ENVIRONMENT; FEMALE; MALE; MATERNAL BEHAVIOR; MODELS, BIOLOGICAL; PARASITES; POPULATION DENSITY; POPULATION DYNAMICS; POPULATION GROWTH; PREDATORY BEHAVIOR; REPRODUCTION;

EID: 65649108099     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2008.0292     Document Type: Article

References (70)

1. Baltensweiler, W. & Fischlin, A. 1989 The larch budmoth in the Alps. In Dynamics of forest insect populations, patterns, causes, implications (ed. A. Berryman), pp. 331-351. New York, NY: Plenum Press.
2. Banks, P. & Powell, F. 2004 Does maternal condition or prédation risk influence small mammal population dynamics? Oikos 106, 176-184. (doi:10.1111/j.0030-1299.2004.12679.x)
3. Beckerman, A., Benton, T. G., Ranta, E., Kaitala, V. & Lundberg, P. 2002 Population dynamic consequences of delayed life history effects? Trends Ecol. Evol. 17, 263-270. (doi: 10.1016/S0169-5347 (02)02469-2)
4. Beckerman, A., Benton, T., Lapsley, C. & Koesters, N. 2003 Talkin' 'bout my generation: environmental variability and cohort effects. Am. Nat. 162, 754-767. (doi: 10.1086/381056)
5. Beckerman, A. P., Benton, T. G., Lapsley, C. T. & Koesters, N. 2006 How effective are maternal effects at having effects? Proc. R. Soc. B 273, 485-493. (doi:10.1098/rspb. 2005.3315)
6. Begon, M. J., Harper, L. & Townsend, C. R. 2006 Ecology, 3rd edn. London, UK: Blackwell.
7. Benton, T. G., Ranta, E., Kaitala, V. & Beckerman, A. P. 2001 Maternal effects and the stability of population dynamics in noisy environments. J. Anim. Ecol. 70, 590-599. (doi:10.1046/j.1365-2656.2001.00527. x)
8. Benton, T. G., Plaistow, S. G. & Coulson, T. N. 2006 Complex population dynamics and complex causation, devils, details and demography. Proc. R. Soc. B 273, 1173-1181. (doi:10.1098/rspb.2006.3495)
9. Benton, T. G., St Clair, J. J. H. & Plaistow, S. J. 2008 Maternal effects mediated by maternal age, from life 7histories to population dynamics. J. Anim. Ecol. 77, 1038-1046. (doi:10.1111/j.1365-2656.2008.01434. x)
10. Berryman, A. 1995 Population cycles, a critique of the maternal and allometric hypothesis. J. Anim. Ecol. 64, 290-293. (doi:10.2307/5763)
11. Bjornstad, O. & Hansen, T. 1994 Individual variation and population dynamics. Oikos 69, 167-171. (doi:10.2307/3545298)
12. Boonstra, R., Hik, D., Singleton, G. R. & Tinnikov, A. 1998 The impact of predator-induced stress on the snowshoe hare cycle. Ecol. Monog. 68, 371-394. (doi:10.1890/0012-9615(1998)068[0371: TIOPIS]2.0.CO;2)
13. Brommer, J. 2000 The evolution of fitness in life-history theory. Biol. Rev. 75, 377-404. (doi:10.1017/S00063231 000055IX)
14. Calder, W. 1983 Size, function and life history. Mineola, NY: Dover.
15. Chitty, D. 1960 Population processes in the vole and their relevance to general theory. Can. J. Zool. 38, 98-113. (doi:10.1139/z60-011)
16. Conner, M. & White, G. 1999 Effects of individual heterogeneity in estimating the persistence of small populations. Nat. Res. Modelling 12, 109-127.
17. Demastes, J., Hafner, M. S., Hafner, D. J. & Spradling, T. A. 2003 Pocket gophers and chewing lice, a test of the maternal transmission hypothesis. Mol. Ecol. 7, 1065-1069. (doi:10.1046/j.1365-294x.1998.00383.x)
18. Elton, C. & Nicholson, M. 1942 The ten-year cycles in numbers of the lynx in Canada. J. Anim. Ecol. 11, 215-244. (doi:10.2307/1358)
19. Ergon, T., MacKinnon, J. L., Stenseth, N. C., Boonstra, R. & Lambin, X. 2001 Mechanisms for delayed density dependent reproductive traits in field voles, Microtus agrestis, the importance of inherited environmental effects. Oikos 95, 185-197. (doi:10.1034/j.1600-0706. 2001.950201.x)
20. Finnerty, J. 1980 The population cycles of small mammals. New Haven, CT: Yale University Press.
21. Fox, C. & Savalli, U. 1998 Inheritance of environmental variation in body size, superparasititsm of seeds affects progeny and grandprogeny body size via a monogenetic maternal effect. Evolution 52, 172-182. (doi:10.2307/2410932)
22. Ginzburg, L. 1998 Inertial growth, population dynamics based on maternal effects. In Maternal effects as adaptations (eds T. Mousseau & C. Fox), pp. 42-53. New York, NY: Oxford University Press.
23. Ginzburg, L. & Colyvan, M. 2004 Ecological orbits. New York, NY: Oxford University Press.
24. Ginzburg, L. & Jensen, C. 2004 Rules of thumb for judging ecological theories. Trends Ecol. Evol. 19, 121-126. (doi:10.1016/j.tree. 2003.11.004)
25. Ginzburg, L. & Taneyhill, D. 1994 Population cycles of forest Lepidoptera, a maternal effects hypothesis. J. Anim. Ecol. 63, 79-92. (doi:10.2307/5585)
26. Ginzburg, L. & Taneyhill, D. 1995 Higher growth rate implies shorter cycle, whatever the cause. J. Anim. Ecol. 64, 294-295. (doi:10.2307/5764)
27. Giron, D. & Casas, J. 2003 Mothers reduce egg provisioning with age. Ecol. Lett. 6, 273-277. (doi:10.1046/j.1461- 0248.2003.00429.x)
28. Groothuis, T. G. G., Müller,W., von Engelhardt, N., Carere, C. & Eising, C. M. 2005 Maternal hormones as tool to adjust offspring phenotype in avian species. Neurosci. Biobehav. Rev. 29, 329-352. (doi:10.1016/j.neubiorev. 2004.12.002)
29. Hanski, I., Henttonen, H., Korpimäki, E., Oksanen, L. & Turchin, P. 2001 Small rodent dynamics and predation. Ecology 82, 1505-1520. (doi:10.1890/0012-9658(2001) 082[1505:SRDAP]2.0.CO;2)
30. Hercus, M. & Hoffmann, A. 2000 Maternal and grandmaternal age influence offspring fitness in Drosophila. Proc. R. Soc. B 267, 2105-2110. (doi:10.1098/rspb.2000. 1256)
31. Hörnfeldt, B. 2004 Long-term decline in numbers of cyclic voles in boreal Sweden, analysis and presentation of hypotheses. Oikos 107, 376-392. (doi:10.1111/j.0030- 1299.2004.13348.x)
32. Inchausti, P. & Ginzburg, L. 1998 Small mammals cycles in Northern Europe, patterns and evidence for a maternal effects hypothesis. J. Anim. Ecol. 67, 180-194. (doi:10. 1046/j.1365-2656.1998.00189.x)
33. Keith, L. 1963 Wildlife's ten year cycle. Madison, WI: University of Wisconsin Press.
34. Keith, L. 1990 Dynamics of snowshoe hare populations. In Current mammalogy (ed. H. Genoways), pp. 119-195. New York, NY: Plenum Press.
35. Kendall, B. E., Prendergast, J. & Bjørnstad, O. N. 1998 The macroecology of population dynamics, taxonomic and biogeographic patterns in population cycles. Ecol. Lett. 1, 160-164. (doi:10.1046/j.1461- 0248.1998. 00037.x)
36. Kendall, W., Briggs, C. J., Murdocb, W. W., Turchin, P., Ellner, S. P., Mccauley, E., Nisbet, R. M. & Wood, S. N. 1999 Why do populations cycle? A synthesis of statistical and mechanistic modeling approaches. Ecology 80, 1789-1805.
37. Krebs, C. 1996 Population cycles revisited. J. Mammal. 77, 8-24. (doi:10.2307/1382705)
38. Krebs, C. J., Boutin, S., Boonstra, R., Sinclair, A. R. E., Smith, J. N. M., Dale, M. R. T., Martin, K. & Turkington, R. 1995 Impact of food and predation on the snowshoe hare cycle. Science 269, 1112-1115. (doi:10.1126/science. 269.5227.1112)
39. Krukonis, G. & Schaffer, W 1991 Population cycles in mammals and birds, does periodicity scale with body size? J. Theor. Biol. 148, 469-493. (doi:10.1016/S0022-5193 (05)80232-2)
40. Kruuk, L. & Hadfield, J. 2007 How to separate genetic and environmental causes of similarity between relatives. J. Evol. Biol. 20, 1890-1903. (doi:10.1111/j.1420-9101. 2007.01377.x)
41. Leslie, P. 1948 Some further notes on the use of matrices in population dynamics. Biometrika 35, 213-245.
42. Leslie, P. 1959 The properties of a certain lag of population growth and the influence of an external random factor on a number of such population. Physiol. Zool. 32, 151-159.
43. Leslie, P. 1966 The intrinsic rate of increase and overlap of successive generations in a population of guillemots Una aalge Pont. J. Anim. Ecol. 35, 291-301. (doi:10.2307/2396)
44. Lindstrom, J. 1999 Early development and fitness in birds and mammals. Trends Ecol. Evol. 14, 343-348. (doi: 10. 1016/S0169-5347 (99)01639-0)
45. Lindström, J. & Kokko, H. 2002 Cohort effects and population dynamics. Ecol. Lett. 5, 338-344. (doi: 10. 1046/j.1461-0248.2002. 00317.x)
46. Marshall, D. & Ulier, T. 2007 When is a maternal effect adaptive? Oikos 116, 1957-1963. (doi:10.1111/j.2007. 0030-1299.16203.x)
47. Marshall, T. C., Slate, J., Kruuk, L. & Pemberton, J. M. 2002 Statistical confidence for likelihood-based paternity inference in natural populations. Mol. Ecol. 7, 639-655. (doi: 10.1046/j.1365-294x. 1998.00374.x)
48. Martinez-Padilla, J. 2006 Prelaying maternal condition modifies the association between egg mass and T cell-mediated immunity in kestrels. Behav. Ecol. Sociol. 60, 510-515. (doi:10.1007/s00265-006-0193-l)
49. Matthiopolous, J., Moss, R. & Lambin, X. 2002 The kin facilitation hypothesis for red grouse population cycles, territorial dynamics of the family cluster. Ecol. Model 47, 291-307. (doi:10.1016/S0304-3800 (01)00420-3)
50. McNamara, J. & Houston, A. 1996 State-dependent life histories. Nature 380, 215-221. (doi:10.1038/380215a0)
51. Moss, R., Watson, A. & Parr, R. 1996 Experimental prevention of a population cycle in red grouse. Ecology 77 1512-1530. (doi: 10.2307/2265548)
52. Mousseau, T. A. & Fox, C. W 1998 Maternal effects as adaptations. Oxford, UK: Oxford University Press.
53. Murdoch, W W., Briggs, C. J. & Nisbet, R. M. 2002 Consumer resource dynamics. Princeton, NJ: Princeton University Press.
54. Norrdahl, K. & Korpimäki, E. 1995 Effects of predator removal on vertebrate prey populations, birds of prey and small mammals. Oecologia 103, 241-248. (doi:10.1007/BF00329086)
55. Peckarsky, B. et al. 2008 Revisiting the classics, considering nonconsumptive effects in textbook examples of predator-prey interactions. Ecology 89, 2416-2425. (doi:10.1890/07-1131.1)
56. Plaistow, S. J., Lapsley, C. T. & Benton, T. G. 2006 Context-dependent intergenerational effects, the interaction between past and present environments and its effect on population dynamics. Am. Nat. 167, 206-215. (doi:10. 1086/499380)
57. Plaistow, S. J., St Clair, J. J., Grant, J. & Benton, T. G. 2007 How to put all your eggs in one basket, empirical patterns of offspring provisioning throughout mother's lifetime. Am. Nat. 170, 520-529. (doi: 10. 1086/521238)
58. Räsänen, K. & Kruuk, L. 2007 Maternal effects and evolution at ecological time scales. Func. Ecol. 21, 408-421. (doi:10. 1111/j.1365-2435.2007.01246.x)
59. Räsänen, K., Laurila, A. & Merilä, J. 2005 Maternal investment in egg size: environment-and-population-specific effects on offspring performance. Oecologia 4, 546-553. (doi: 10.1007/s00442-004-1762-5)
60. Redpath, S. M., Mougeot, F., Leckie, F. & Hudson, P. J. 2006 Testing the role of parasites in driving the cyclic population dynamics of a gamebird. Ecol. Lett. 9, 410-441. (doi:10.1111/j.1461-0248.2006.00895.x)
61. Rossiter, M. 1996 Incidence and consequences of inherited environmental effects. Annu. Rev. Ecol. Syst. 27, 451-476. (doi:10.1146/annurev. ecolsys.27.1.451)
62. Royama, T. 1992 Analytical population dynamics. New York, NY: Chapman and Hall.
63. Sinclair, A. R. E., Chitty, D., Stefan, C. I. & Krebs, C. J. 2003 Mammal population cycles, evidence for intrinsic differences during snowshoe hare cycles. Can. J. Zool. 81, 216-220. (doi:10.1139/z03-006)
64. Turchin, P. 2003 Complex population dynamics. Princeton, NJ: Princeton University Press.
65. Turchin, P. & Batzli, G. 2001 Availability of food and the population dynamics of arvicoline rodents. Ecology 82, 1521-1534. (doi: 10.2307/2679797)
66. Turchin, P. & Hanski, I. 1997 An empirically-based model for the latitudinal gradient in vole population dynamics. Am. Nat. 149, 842-874. (doi: 10.1086/286027)
67. Turchin, P. & Hanski, I. 2002 Contrasting alternative hypotheses about rodent cycles by translating them into parameterized models. Ecol. Lett. 4, 267-276. (doi: 10. 1046/j.1461-0248.2001.00204.x)
68. Ulier, T. 2008 Developmental plasticity and the evolution of parental effects. Trends Ecol. Evol. 23, 432-436. (doi: 10. 1016/j.tree.2008.04. 005)
69. Weitz, J. & Levin, S. 2006 Size and scaling of predator prey dynamics. Ecol. Lett. 9, 548-557. (doi:10.111 l/j.1461-0248.2006. 00900.x)
70. Wellington, W. 1960 Qualitative changes in natural populations during changes in abundance. Can. J. Zool. 38, 290-314. (doi:10.1139/z60-036)