Egg maturation strategy and its associated trade-offs: A synthesis focusing on Lepidoptera

Ecological Entomology

Volumn 30, Issue 4, 2005, Pages 359-375

  Jervis, Mark A ^a   Boggs, Carol L ^b   Ferns, Peter N ^a  

^a CARDIFF UNIVERSITY   (United Kingdom)

^b STANFORD UNIVERSITY   (United States)

Author keywords

Capital and income breeding; Lepidoptera; Reproduction survival trade off; Resource allocation and acquisition; Synovigeny and pro ovigeny

Indexed keywords

FECUNDITY; LIFE HISTORY; MATURATION; REPRODUCTIVE EFFORT; RESOURCE ALLOCATION; SURVIVAL; TRADE-OFF;

HEXAPODA; HYMENOPTERA; INSECTA; LEPIDOPTERA; TRICHOPTERA;

EID: 27144512530     PISSN: 03076946     EISSN: 13652311     Source Type: Journal    
DOI: 10.1111/j.0307-6946.2005.00712.x     Document Type: Review

References (180)

1. Barbosa, P., Krischik, V. & Lance, D. (1989) Life-history traits of forest-inhabiting flightless Lepidoptera. American Midland Naturalist, 122, 262-274.
2. Barnes, A.I. & Partridge, L. (2003) Costing reproduction. Animal Behaviour, 66, 199-204.
3. Bejer, B. (1988) The nun moth in European Spruce forests. Dynamics of Forest Insect Populations (ed. by A. A. Berryman), pp. 211-231. Plenum Press, New York.
4. Bell, G. & Koufopanou, V. (1986) The cost of reproduction. Oxford Surveys in Evolutionary Biology, 3, 83-131.
5. Bishop, J.A. (1972) An experimental study of the cline of industrial melanism in Biston betularia (L.) (Lepidoptera) between urban Liverpool and rural North Wales. Journal of Animal Ecology, 41, 209-243.
6. Blackburn, T.M. (1991a) A comparative examination of life span and fecundity in parasitoid Hymenoptera. Journal of Animal Ecology, 60, 151-164.
7. Blackburn, T.M. (1991b) Evidence for a 'fast-slow' continuum of life-history traits among parasitoid Hymenoptera. Functional Ecology, 5, 65-71.
8. Boggs, C.L. (1979) Resource allocation and reproductive strategies in several heliconiine butterflies. PhD Dissertation, University of Texas at Austin, Texas.
9. Boggs, C.L. (1981) Nutritional and life-history determinants of resource allocation in holometabolous insects. American Naturalist, 117, 692-709.
10. Boggs, C.L. (1986) Reproductive strategies of female butterflies: variation in and constraints on fecundity. Ecological Entomology, 11, 7-15.
11. Boggs, C.L. (1987) Within population variation in the demography of Speyeria mormonia (Lepidoptera: Nymphalidae). Holarctic Ecology, 10, 175-184.
12. Boggs, C.L. (1990) A general model of the role of male-donated nutrients in female insects' reproduction. American Naturalist, 136, 598-617.
13. Boggs, C.L. (1992) Resource allocation: exploring connections between foraging and life history. Functional Ecology, 6, 508-518.
14. Boggs, C.L. (1994) The role of resource allocation in understanding reproductive patterns. Individuals, Populations and Patterns in Ecology (ed. by S. R. Leather. A. D. Watt, N. J. Mills and K. E. A. Walters), pp. 25-33. Intercept Press, Andover, U.K.
15. Boggs, C.L. (1995) Male nuptial gifts: phenotypic consequences and evolutionary implications. Insect Reproduction (ed. by S. R. Leather and J. Hardie), pp. 215-242. CRC Press, Boca Raton, Florida.
16. Boggs, C.L. (1997a) Reproductive allocation from reserves and income in butterfly species with differing adult diets. Ecology, 78, 181-191.
17. Boggs, C.L. (1997b) Dynamics of reproductive allocation from juvenile and adult feeding: radiotracer studies. Ecology, 78, 192-202.
18. Boggs, C.L. (2003) Environmental variation, life histories, and allocation. Butterflies: Ecology and Evolution Taking Flight (ed. by C. L. Boggs, W. B. Watt and P. R. Ehrlich), pp. 185-206. University of Chicago Press, Chicago.
19. Boggs, C.L. & Gilbert, L.E. (1979) Male contribution to egg production in butterflies: evidence for transfer of nutrients at mating. Science, 206, 83-84.
20. Boggs, C.L. & Jackson, L.A. (1991) Mud puddling by butterflies is not a simple matter. Ecological Entomology, 16. 123-127.
21. Boggs, C.L. & Murphy, D.D. (1997) Community composition in mountain ecosystems: climatic determinants of montane butterfly distributions. Global Ecology and Biogeography Letters, 6, 39-48.
22. Boggs, C.L. & Nieminen, M. (2004) Checkerspot reproductive biology. On the Wings of Checkerspots: a Model System for Population Biology (ed. by P. R. Ehrlich and I. Hanski), pp. 92-111. Oxford University Press. Oxford.
23. Boggs, C.L. & Ross, C.L. (1993) The effect of adult food limitation on life history traits in Speyeria mormonia (Lepidoptera: Nymphalidae). Ecology, 74, 433-441.
24. Bonnet, X., Bradshaw, D. & Shine, R. (1998) Capital versus income breeding: an ectothermic perspective. Oikos, 83, 333-342.
25. Braby, M.F. (1995) Reproductive seasonality in tropical satyrine butterflies: strategies for the dry season. Ecological Entomology, 20, 5-17.
26. Braby, M.F. (2002) Life history strategies and habitat templets of tropical butterflies in north-eastern Australia. Evolutionary Ecology, 16, 399-413.
27. Braby, M.F. & Jones, R.E. (1995) Reproductive patterns and resource allocation in tropical butterflies: influence of adult diet and seasonal phenotype on fecundity, longevity and egg size. Oikos, 72, 189-204.
28. Brower, L.P. (1985) New perspectives on the migration biology of the monarch butterfly, Danaus plexippus L. Migration: Mechanisms and Adaptive Significance (ed. by M. A. Rankin), pp. 748-785. University of Texas Contributions to Marine Science, Austin, Texas.
29. Brown, I. & Ehrlich, P.R. (1980) Population biology of the checkerspot butterfly Euphydryas chalcedona: structure of the Jasper Ridge colony. Oecologia, 47, 239-251.
30. Carroll, A.L. & Quiring, D.T. (1993) Interactions between size and temperature influence fecundity and longevity of a tortricid moth, Zeiraphera canadensis. Oecologia, 93, 233-241.
31. Carvalho, M.C., Queiroz, P.C.D. & Ruszczyk, A. (1998) Protandry and female size - fecundity variation in the tropical butterfly Brassolis sophorae. Oecologia, 116, 98-102.
32. Casas, J., Pincebourde, S., Mandon, N., Vannier, F., Poujol, R. & Giron, D. (2005) Lifetime nutrient dynamics reveal simultaneous capital and income breeding in a parasitoid. Ecology, 86, 545-554.
33. Chapman, R.F. (1998) The Insects: Structure and Function. Cambridge University Press, Cambridge.
34. Cheng, H.H. (1972) Oviposition and longevity of the dark-sided cutworm, Euxoa messoria (Lepidoptera: Noctuidae), in the laboratory. Canadian Entomologist. 104, 919-925.
35. Chew, F.S. & Robbins, R.K. (1984) Egg-laying in butterflies. The Biology of Butterflies (ed. by R. I. Vane-Wright and P. R. Ackery), pp. 65-79. Academic Press, London.
36. Cole, L.R. (1967) A study of the life-cycles and hosts of some Ichneumonidae attacking pupae of the green oak-leaf roller moth, Tortrix viridana (L.) (Lepidoptera: Tortricidae) in England. Transactions of the Royal Entomological Society of London, 119, 267-281.
37. Common, I.F.B. (1990) Moths of Australia. E.J. Brill, Leiden.
38. Dunlap-Pianka, H., Boggs, C.L. & Gilbert, L.E. (1977) Ovarian dynamics in heliconiine butterflies: programmed senescence versus eternal youth. Science, 197, 487-490.
39. Eidmann, H. (1931) Morphologische und physiologische Untersuchungen am weiblichen Genitalapparat der Lepidopteren. II. Physiologischer Teil. Zeitschift für angewandte Entomologie, 18, 57-112.
40. Elkinton, J.S. & Liebhold, A.M. (1990) Population dynamics of Gypsy Moth in North America. Annual Review of Entomology, 35, 571-596.
41. Ellers, J. & Jervis, M. (2003) Body size and the timing of egg production in parasitoid wasps. Oikos, 102, 164-172.
42. Ellers, J. & Jervis, M.A. (2004) Why are so few parasitoid wasp species pro-ovigenic? Evolutionary Ecology Research, 6, 993-1002.
43. Ellers, J., Sevenster, J.G. & Driessen, G. (2000) Egg load evolution in parasitoids. American Naturalist, 156, 650-665.
44. Ellers, J. & van Alphen, J.J.M. (1997) Life history evolution in Asobara tabida: plasticity in allocation of fat reserves to survival and reproduction. Journal of Evolutionary Biology, 10, 771-785.
45. Fadamiro, H.Y. & Baker, T.C. (1999) Reproductive performance and longevity of female European corn borer, Ostrinia nubilalis: effects of multiple mating, delay in mating, and adult feeding. Journal of Insect Physiology, 45, 385-392.
46. Feldman, T.S. & Haber, W.A. (1998) Oviposition behaviour, host plant use, and diet breadth of Anthanassa butterflies (Lepidoptera: Nymphalidae) using plants in the Acanthaceae in a Cost Rican community. Florida Entomologist, 81, 396-406.
47. Feltwell, J. (1982) Large White Butterfly: The Biology, Biochemistry and Physiology of Pieris brassicae (Linnaeus). W. Junk, The Hague.
48. Fenemore, P.G. (1977) Oviposition of potato tuber moth, Phthorimaea opercullela Zell. (Lepidoptera: Gelechiidae); fecundity in relation to mated state, age, and pupal weight. New Zealand Journal of Zoology, 4, 187-191.
49. Flanders, S.E. (1950) Regulation of ovulation and egg disposal in the parasitic Hymenoptera. Canadian Entomologist, 82, 134-140.
50. Gage, M.J.G. (1995) Continuous variation in reproductive strategy as an adaptive response to population density in the moth Plodia interpunctella. Proceedings of the Royal Society of London B, 261, 25-30.
51. Gage, M.J.G. (1998) Influences of sex, size and symmetry upon ejaculate size in a moth. Behavioral Ecology, 9, 592-597.
52. Garcia-Barros, E. (2000) Body size, egg size, and their interspecific relationships with ecological and life history traits in butterflies (Lepidoptera: Papilionoidea, Hesperoidea). Biological Journal of the Linnean Society, 70, 251-284.
53. Gardiner, B.O.C. (1982) A Silkmoth Rearer's Handbook. The Amateur Entomologist's Society, Hanworth, U.K.
54. Gilbert, F.S. & Jervis, M.A. (1998) Functional, evolutionary and ecological aspects of feeding-related mouthpart specializations in parasitoid flies. Biological Journal of the Linnean Society, 63, 495-535.
55. Gilbert, L.E. (1972) Pollen feeding and reproductive biology of Heliconius butterflies. Proceedings of the National Academy of Sciences of the United States of America, 69, 1403-1407.
56. Graf, J.E. (1917) The potato tuber moth. US Department of Agriculture Bulletin, 427, 1-56.
57. Greenfield, M.D. & Karandinos, M.G. (1976) Fecundity and longevity of Synanthedon pictipes under constant and fluctuating temperatures. Environmental Entomology, 5, 883-887.
58. Gunn, A. & Gatehouse, A.G. (1985) Effects of the availability of food and water on reproduction in the African armyworm, Spodoptera exempta. Physiological Entomology. 10, 53-63.
59. Hanski, I., Erälahti, C., Kankare, M., Ovaskainen, O. & Sirén, H. (2004) Variation in migration propensity among individuals maintained by landscape structure. Ecology Letters, 7, 958-966.
60. Heimpel, G.E., Mangel, M. & Rosenheim, J.A. (1998) Effects of time limitation and egg limitation on lifetime reproductive success of a parasitoid in the field. American Naturalist, 152, 273-289.
61. Heimpel, G.E. & Rosenheim, J.A. (1998) Egg limitation in parasitoids: a review of the evidence and a case study. Biological Control. 11, 160-168.
62. Heinrich, B. (1993) The Hot-Blooded Insects: Strategies and Mechanisms of Thermoregulation. Springer, Berlin.
63. Hellmann, J.J., Weiss, S.B., McLaughlin, J.F., Ehrlich, P.R., Murphy, D.D. & Launer, A.E. (2004) Structure and dynamics of Euphydryas editha populations. On the Wings of Checkerspots: A Model System for Population Biology (ed. by P. R. Ehrlich and I. Hanski), pp. 34-62. Oxford University Press, Oxford.
64. Herman, W.S. & Tatar, M. (2001) Juvenile hormone regulation of longevity in the migratory monarch butterfly. Proceedings of the Royal Society of London B, 268, 2509-2514.
65. Herz, A. & Heitland, W. (2002) Comparison of the fat allocation patterns in female pine sawflies (Hymenoptera; Diprionidae). European Journal of Enlomology, 99, 117-120.
66. Hill, C.J. & Pierce, N.B. (1989) The effect of diet on the biology of butterflies. 1. The common imperial blue, Jalmenus evagoras. Oecologia, 81, 249-257.
67. Huang, F. & Subramanyam, B. (2003) Effects of delayed mating on reproductive performance of Plodia interpunctella (Hübner) (Lepidoptera: Pyralidae). Journal of Stored Products Research, 39, 53-63.
68. Jaenike, J. (1990) Host specialization in phytophagous insects. Annual Review of Ecology and Systematics, 21, 243-273.
69. Janzen, D.H. (1984) Two ways to be a tropical big moth: Santa Rosa saturniids and sphingids. Oxford Surveys in Evolutionary Biology, 1, 85-140.
70. Jervis, M. A. (1998) Functional and evolutionary aspects of mouth-part structure in parasitoid wasps. Biological Journal of the Linnean Society, 63, 461-493.
71. Jervis, M.A. & Ferns, P.N. (2004) The timing of egg maturation in insects: ovigeny index and initial egg load as measures of fitness and of resource allocation. Oikos, 107, 449-460.
72. Jervis, M.A., Ferns, P.N. & Heimpel, G.E. (2003) Body size and the timing of egg production: a comparative analysis. Functional Ecology, 17, 375-383.
73. Jervis, M.A., Heimpel, G.E., Ferns, P.N., Harvey, J.A. & Kidd, N.A.C. (2001) Life-history strategies in parasitoid wasps: a comparative analysis of 'ovigeny'. Journal of Animal Ecology, 70, 442-458.
74. Jervis, M.A. & Kidd, N.A.C. (1986) Host-feeding strategies in hymenopteran parasitoids. Biological Reviews of the Cambridge Philosophical Society, 61, 395-434.
75. Jervis, M.A. & Kidd, N.A.C. (1999) Parasitoid adult nutritional ecology: implications for biological control. Theoretical Approaches to Biological Control, (ed. by B. A. Hawkins and H. V. Cornell), pp. 131-151. Cambridge University Press, Cambridge.
76. Jervis, M.A., Kidd, N.A.C., Fitton, M.G., Huddleston, T. & Dawah, H.A. (1993) Flower-visiting by hymenopteran parasitoids. Journal of Natural History, 27, 67-105.
77. Jervis, M.A. & Vilhelmsen, L.B. (2000) Mouthpart evolution in adults of the basal, 'symphytan' hymenopteran lineages. Biological Journal of the Linnean Society, 70, 121-146.
78. Johnson, C.G. (1969) Migration and Dispersal of Insects by Flight. Methuen, London.
79. Jones, R.E., Gilbert, N., Guppy, M. & Nealis, V. (1980) Long distance movement of Pieris rapae. Journal of Animal Ecology, 49, 629-642.
80. Jönsson, K.I. (1997) Capital and income breeding as alternative tactics of resource use in reproduction. Oikos, 78, 57-66.
81. Kaitala, A. (1988) Wing muscle dimorphism: two reproductive pathways of the waterstrider Gerris thoracicus in relation to habitat instability. Oikos, 53, 222-228.
82. Karlsson, B. (1994) Feeding habits and change of body composition with age in three nymphalid butterfly species. Oikos, 69, 224-230.
83. Karlsson, B. (1995) Resource allocation and mating systems in butterflies. Evolution, 49, 955-961.
84. Karlsson, B. (1998) Nuptial gifts, resource budgets, and reproductive output in a polyandrous butterfly. Ecology, 79, 2931-2940.
85. Kemp, D.J. & Rutowski, R.L. (2004) A survival cost to mating in a polyandrous butterfly, Colias eurytheme. Oikos, 105, 65-70.
86. Kidd, N.A.C. & Jervis, M.A. (1989) The effects of host feeding behaviour on the dynamics of parasitoid - host interactions, and the implications for biological control. Researches on Population Ecology, 31, 235-274.
87. Kingsolver, J.G. (1999) Experimental analysis of wing size, flight, and survival in the western white butterfly. Evolution, 53, 1479-1490.
88. Kopper, B.J., Shu, S.Q., Charlton, R.E. & Ramaswamy, S.B. (2001) Evidence for reproductive diapause in the fritillary Speyeria idalia (Lepidoptera: Nymphalidae). Annals of the Entomological Society of America, 94, 427-432.
89. Labine, P.A. (1964) Population biology of the butterfly, Euphydryas editha. I. Barriers to multiple inseminations. Evolution, 18, 335-336.
90. Labine, P.A. (1968) The population biology of the butterfly, Euphydryas editha. VIII. Oviposition and its relation to patterns of oviposition in other butterflies. Evolution, 22, 799-805.
91. Launer, A.E., Murphy, D.D., Boggs. C.L., Baughman, J.F., Weiss, S.B. & Ehrlich, P.R. (1993) Puddling behavior by Bay checkerspot butterflies (Euphydyras editha bayensis). Journal of Research on Lepidoptera, 32, 45-52.
92. Leahy, T.C. & Andow, D.A. (1994) Egg weight, fecundity and longevity are increased by adult feeding in Ostrinia nubilalis (Lepidoptera: Pyralidae). Annals of the Entomological Society of America, 87, 342-349.
93. Leather, S.R. (1984) The effect of adult feeding on the fecundity, weight loss, and survival of the pine beauty moth, Panolis flammea (D. and S.). Oecologia, 63, 70-74.
94. Leather, S.R. & Bernand, A.C. (1987) Factors affecting life-history parameters of the pine beauty moth, Panolis flammea (D. and S.): the hidden costs of reproduction. Functional Ecology, 1, 331-338.
95. Leverton, R. (2001) Enjoying Moths. T. & A.D. Poyser, London.
96. Majerus, M. (2002) Moths. HarperCollins, London.
97. Marden, J.H. (2000) Variability in the size, composition and function of insect flight muscles. Annual Review of Physiology, 62, 157-178.
98. Marks, R.J. (1976) Mating behavior and fecundity of the red bollworm Diparopsis castanea Hmps (Lepidoptera, Noctuidae). Bulletin of Entomological Research, 66, 145-158.
99. Mayhew, P.J. (1997) Adaptive patterns of host-plant selection by phytophagous insects. Oikos, 79, 417-428.
100. Mayhew, P.J. & Blackburn, T.M. (1999) Does development mode organise life-history traits in the parasitoid Hymenoptera? Journal of Animal Ecology, 68, 906-916.
101. Meitner, C.J., Brower, L.P. & Davis, A.K. (2004) Migration patterns and environmental effects on stopover of monarch butterflies (Lepidoptera, Nymphalidae) at Peninsular Point, Michigan. Environmental Entomology, 33, 249-256.
102. Mell, R. (1922) Beitrage zur Fauna Sinica II. Biologie und Systematik der Sudchinesischen Sphingiden. R. Friedlander & Sohn, Berlin.
103. Mell, R. (1940) Beitrage zur Fauna sinica XX. Eiproduktion bei Lepidopteren in tropenrandgebieten. Zeitschrift für angewandte Entomologie, 27, 503-539.
104. Miller, T.A. (1978) Oviposition behaviour of colonized Hyalophora gloveri (Saturniidae). Journal of the Lepidoplerist's Society, 32, 233-234.
105. Miller, T.A. & Cooper, W.J. (1977) Oviposition behaviour of colonized Callisamia promethea (Saturniidae). Journal of the Lepidopterist's Society, 31, 282-283.
106. Miller, W.E. (1996) Population behaviour and adult feeding capability in Lepidoptera. Environmental Entomology, 25, 213-226.
107. Miller, W.E. (1997) Diversity and evolution of tongue length in hawkmoths (Sphingidae). Journal of the Lepidopterists' Society, 51,9-31.
108. Murata, M. & Tojo, S. (2002) Utilization of lipid for flight and reproduction in Spodoptera litura (Lepidoptera: Noctuidae). European Journal of Entomology, 99, 221-224.
109. Murphy, D.D., Launer, A.E. & Ehrlich, P.R. (1983) The role of adult feeding in egg production and population dynamics of the Checkerspot Butterfly Euphydryas editha. Oecologia, 56, 257-263.
110. Nakanishi, Y., Watanabe, M. & Ito. T. (2000) Differences in lifetime reproductive output and mating frequency of two female morphs of the sulfur butterfly, Colias erate (Lepidoptera: Pieridae). Journal of Research on the Lepidoptera, 35, 1-8.
111. Norris, M.J. (1932) Contributions towards the study of insect fertility. I. The structure and operation of the reproductive organs of the genera Ephestia and Plodia (Lepidoptera, Phycitidae). Proceedings of the Zoological Society of London, 1932, 39-611.
112. Norris, M.J. (1934) Contributions towards the study of insect fertility. III. Adult nutrition, fecundity, and longevity in the genus Ephestia (Lepidoptera, Phycitidae). Proceedings of the Zoological Society of London, 1934, 333-360.
113. Norris, M.J. (1936) The feeding habits of the adult Lepidoptera Heteroneura. Transactions of the Royal Entomological Society of London, 85, 61-90.
114. Novak, K. & Sehnal, F. (1963) The development cycle of some species of the genus Limnephilus (Trichoptera). Casopsis Ceskoslovenske Spolencnosti Entomologicke, 60, 68-80.
115. Oberhauser, K.S. (1997) Fecundity, lifespan and egg mass in butterflies: effects of male-derived nutrients and female size. Functional Ecology, 11, 166-175.
116. O'Brien, D.M., Fogel, M.L. & Boggs, C.L. (2002) Renewable and non-renewable resources: Amino acid turnover and allocation to reproduction in Lepidoptera. Proceedings of the National Academy of Sciences USA, 99, 4413-4418.
117. O'Brien, D.M., Boggs, C.L. & Fogel, M.L. (2003) Pollen feeding in the butterfly Heliconius charitonia: isotopic evidence for essential amino acid transfer from pollen to eggs. Proceedings of the Royal Society of London B, 270, 2631-2636.
118. O'Brien, D.M., Boggs, C.L. & Fogel, M.L. (2004) Making eggs from nectar: Connections between butterfly life history and the importance of nectar carbon in reproduction. Oikos, 105, 279-291.
119. O'Brien, D.M., Boggs, C.L. & Fogel, M.L. (in press) The dietary sources of amino acids used in reproduction by butterflies: a comparative study using compound specific stable isotope analysis. Physiological and Biochemical Zoology.
120. Odendaal, F. (1989) Mature egg number influences the behaviour of female Battus philenor butterflies. Journal of Insect Behavior, 2, 15-25.
121. Odendaal, F. & Rauscher, M.D. (1990) Egg load influences search intensity, host selectivity, and clutch size in Battus philenor butterflies. Journal of Insect Behavior, 3, 183-193.
122. Oldroyd, H. (1964) The Natural History of Flies. Weidenfeld & Nicholson, London.
123. Ostaff, D.P. & Quiring, D.T. (1994) Seasonal distribution of adult eclosion, oviposition, and parasitism and predation of eggs of the spruce bud moth, Zeiraphera canadensis (Lepidoptera, Tortricidae). Canadian Entomologist, 126, 995-1006.
124. Papaj, D.R. (2000) Ovarian dynamics and host use. Annual Review of Entomology, 45, 423-448.
125. Peck, S.L., Gould, F. & Ellner, S.P. (1999) Spread of resistance in spatially extended regions of transgenic cotton: implications for management of Heliothis virescens (Lepidoptera: Noctuidae). Journal of Economic Entomology, 92, 1-16.
126. Penz, C.M. & Krenn, H.W. (2000) Behavioural adaptations to pollen-feeding in Heliconius butterflies (Nymphalidae: Heliconiidae): an experiment using Lantana flowers. Journal of Insect Behavior, 13, 865-880.
127. Pivnick, K.A., Janvis, B.J., Gillott, C., Slater, G.P. & Underbill, E.W. (1990) Daily patterns of reproductive activity and the influence of adult density and exposure to host plants on reproduction in the Diamondback Moth (Lepidoptera: Plutellidae). Environmental Entomology, 19, 587-593.
128. Prinzing, A. (2003) Are generalists pressed for time? An interspecific test of the time-limited disperser model. Ecology, 84, 1744-1755.
129. Proshold, F.I. (1996) Reproductive capacity of laboratory-reared Gypsy Moths (Lepidoptera: Lymantriidae): effect of age of female at time of mating. Journal of Economic Entomology, 89, 337-342.
130. Proshold, F.I., Karpenko, C.P. & Graham, C.K. (1982) Egg production and oviposition in the tobacco budworm: Effect of age at mating. Annals of the Entomological Society of America, 75, 51-55.
131. Quintero, H.E. (1988) Population dynamics of the butterfly Heliconius charitonius L. in Puerto Rico. Caribbean Journal of Science, 24, 155-160.
132. Rau, P. & Rau, N.L. (1913) The fertility of cecropia eggs in relation to the mating period. Biological Bulletin, 24, 245-250.
133. Richards, O.W. (1940) The biology of the small white butterfly (Pieris rapae), with special reference to the factors controlling its abundance. Journal of Animal Ecology, 9, 243-288.
134. Rivero, A., Giron, D. & Casas, J. (2001) Lifetime allocation of juvenile and adult nutritional resources to egg production in a holometabolous insect. Proceedings of the Royal Society of London B, 268, 1231-1237.
135. Roff, D.A. (2002) Life History Evolution. Sinauer Associates. Sunderland, Massachusetts.
136. Roitberg, B. (2000) Threats, flies, and protocol gaps: can evolutionary ecology save biological control? Parasitoid Population Biology (ed. by M. E. Hochberg and A. R. Ives), pp. 254-265. Princeton University Press, Princeton, New Jersey.
137. Romanowski, H.P. (1991) Population Ecology of Pleuroptya ruralis (Scopoli) (Pyralidae: Pyraustinae). PhD thesis, University of Leeds. UK.
138. Rosenheim, J.A. (1996) An evolutionary argument for egg limitation. Evolution, 50, 2089-94.
139. Rosenheim, J.A. (1999a) Characterizing the cost of oviposition in insects: a dynamic model. Evolutionary Ecology, 13, 141-165.
140. Rosenheim, J.A. (1999b) The relative contributions of time and eggs to the cost of reproduction. Evolution, 53, 376-385.
141. Rosenheim, J.A., Heimpel, G.E. & Mangel, M. (2000) Egg maturation, egg resorption, and the costliness of transient egg limitation in insects. Proceedings of the Royal Society of London B, 267, 1565-1573.
142. Rutowski, R.L. & Gilchrist, G.W. (1987) Courtship, copulation and oviposition in the chalcedon checkerspot, Euphydryas chalcedona (Lepidoptera: Nymphalidae). Journal of Natural History, 21, 1109-1117.
143. Saito, H. (1992) Oviposition patterns in Samia silkmoths (Lepidoptera, Saturniidae). Japanese Journal of Applied Entomology and Zoology, 37, 163-167.
144. Sandlan, K.P. (1979) Host-feeding and its effects on the physiology and behaviour of the ichneumonid parasitoid, Coccygomimus turionellae. Physiological Entomology, 4, 383-392.
145. Sattler, K. (1991) A review of wing reduction in Lepidoptera. Bulletin of the British Museum (N.H.) Entomology, 60, 43-288.
146. Scoble, M.J. (1995) The Lepidoptera: Form, Function and Diversity. Natural History Museum/Oxford University Press, London/Oxford.
147. Sculley, C.E. & Boggs, C.L. (1996) Mating systems and sexual division of foraging effort affect puddling behaviour by butterflies. Ecological Entomology, 21, 193-197.
148. Showier, A.T. & Moran, P.J. (2003) Effects of drought stressed cotton, Gossypium hirsutum L., on beet armyworm, Spodoptera exigua (Hübner), oviposition, and larval feeding preferences and growth. Journal of Chemical Ecology, 29, 1997-2011.
149. Sibly, R.M. & Calow, P. (1984) Direct and absorption costing in the evolution of life cycles. Journal of Theoretical Biology, 111, 463-473.
150. Sibly, R.M. & Calow, P. (1986) Physiological Ecology of Animals. Blackwell Scientific, Oxford,.
151. Šmits, A., Larsson, S. & Hopkins, R. (2001) Reduced realised fecundity in the pine looper Bupalus pinarius caused by host plant defoliation. Ecological Entomology, 26, 417-424.
152. Spradbery, J.P. (1973) Wasps: an Account of the Biology and Natural History of Solitary and Social Wasps, with Particular Reference to Those of the British Isles. Sidgwick & Jackson, London.
153. Spradbery, J.P. & Sands, D.P.A. (1981) Larval fat body and its relationship to protein storage and ovarian development in adults of the screw-worm fly Chrysomya bezziana. Entomologia experimentalis et applicata, 30, 116-122.
154. Stearns, S.C. (1992) The Evolution of Life Histories. Oxford University Press, Oxford.
155. Stern, V.M. & Smith, R.F. (1960) Factors affecting egg production and oviposition in populations of Colias philodice eurytheme Boisduval (Lepidoptera: Pieridae). Hilgardia, 29, 411-454.
156. Stevens, D.J., Hansell, M.H., Freel, J.A. & Monaghan, P. (1999) Developmental trade-offs in caddis flies: increased investment in larval defence alters adult resource allocation. Proceedings of the Royal Society of London B, 266, 1049-1054.
157. Stevens, D.J., Hansell, M.H. & Monaghan, P. (2000) Developmental trade-offs and life histories: strategic allocation of resources in caddis flies. Proceedings of the Royal Society of London B, 267, 1511-1515.
158. Stjernholm, F. & Karlsson, B. (2000) Nuptial gifts and the use of body resources for reproduction in the green-veined white butterfly, Pieris napi. Proceedings of the Royal Society of London B, 267, 807-811.
159. Stjernholm, F., Karlsson, B. & Boggs, C.L. (in press) Flight muscle breakdown: a possible route to increased reproductive potential in butterflies? Biological Journal of the Linnean Society.
160. Sutcliffe, O.L., Thomas, C.D. & Moss, D. (1996) Spatial synchrony and asynchrony in butterfly population dynamics. Journal of Animal Ecology, 65, 85-95.
161. Svärd, L. & Wiklund, C. (1988) Fecundity, egg weight and longevity in relation to multiple ma tings in females of the monarch butterfly. Behavioral Ecology and Sociobiology, 23, 39-43.
162. Tammaru, T., Esperk, T. & Catellanos, I. (2002) No evidence for costs of being large in females of Orgyia spp. (Lepidoptera, Lymantriidae): larger is always better. Oecologia. 133, 430-438.
163. Tammaru, T. & Haukioja, E. (1996) Capital breeders and income breeders in Lepidoptera - consequences for population dynamics. Oikos, 77, 561-564.
164. Tisdale, R.A. & Sappington, T.W. (2001) Realized and potential fecundity, egg fertility, and longevity of laboratory-reared female beet armyworm (Lepidoptera: Noctuidae) under different adult diet regimes. Annals of the Entomological Society of America, 94, 415-419.
165. Torres-Vila, L.M., Carmen Rodriguez-Molina, M., Gragera, J. & Bielza-Lino. P. (2001) Polyandry in Lepidoptera: a heritable trait in Spodoptera exigua Hübner. Heredity, 86, 177-183.
166. Tweedie, M.W.F. (1976) A note on moths with flightless females. Entomologist's Gazette, 27, 2-3.
167. Van Noordwijk, A.J. & De Jong, G. (1986) Acquisition and allocation of resources: their influence on variation in life history tactics. American Naturalist, 128, 137-142.
168. Waller, D.A. & Gilbert, L.E. (1982) Roost recruitment and resource utilization: observations on a Heliconius charitonia roost in Mexico (Nymphalidae). Journal of the Lepidopterist's Society, 36, 178-184.
169. Ward, A.A. (1986) Optimal habitat selection in time-limited dispersers. American Naturalist, 129, 568-579.
170. Watanabe, M. (1988) Multiple matings increase the fecundity of the yellow swallowtail butterfly, Papilio xuthus L., in summer generations. Journal of Insect Behavior, 1, 17-24.
171. Weinert, B.T. & Timiras, P.S. (2003) Physiology of aging. Invited review: theories of aging. Journal of Applied Physiology, 95, 1706-1716.
172. Wheeler, D. (1996) The role of nourishment in oogenesis. Annual Review of Entomology, 41, 407-431.
173. Wheeler, D., Tuchinskaya, I., Buck, N.A. & Tabashnik, B. (2000) Hexameric storage proteins during metamorphosis and egg production in the diamondback moth, Plutella xylostella (Lepidoptera). Journal of Insect Physiology, 46, 951-958.
174. Wiklund, C., Karlsson, B. & Leimar, O. (2001) Sexual conflict and cooperation in butterfly reproduction: a comparative study of polyandry and female fitness. Proceedings of the Royal Society of London B, 268, 1661-1667.
175. Wilcox, B.A., Murphy, D.D., Ehrlich, P.R. & Austin, G.T. (1986) Insular biogeography of montane butterfly faunas in the Great Basin: a comparison with birds and mammals. Oecologia, 69. 188-194.
176. Willers, J.L., Schneider, J.C. & Ramaswamy, S.B. (1987) Fecundity, longevity and caloric patterns in female Heliothis virescens - changes with age due to flight and supplemental carbohydrate. Journal of Insect Physiology, 33, 803-805.
177. Xingquan, K., Calvin, D.D., Knapp, M.C. & Poston, F.L. (2004) Female European corn borer (Lepidoptera: Crambidae) ovarian development stages: their association with oviposition and use in a classificatory system. Journal of Economic Entomology, 97, 828-835.
178. Young, A.M. (1972) Breeding success and survivorship in some tropical butterflies. Oikos, 23, 318-326.
179. Yusoh, M.R.M. (1999) Adult foods of the diamondback moth, Plutella xylostella L. (Lepidoptera: Yponomeutidae): their effects on some fitness parameters. PhD thesis, University of Wales.
180. Zera, A.J. & Harshman, L.G. (2001) The physiology of life history trade-offs in animals. Annual Review of Ecology and Systematics, 32, 95-126.