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Necessary Requirements for Oviposition

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Sperm Competition in Butterflies

Part of the book series: Ecological Research Monographs ((ECOLOGICAL))

Abstract

A deposited female egg is tens of thousands of times larger than a male spermatozoon. The highest fecundity found immediately after emergence has suggested that no additional eggs develop throughout the female adult stage. Although the number of eggs actually laid during the female reproductive period is about 500, her abdomen size generally limits the number of mature eggs loaded to fewer than 50. Therefore, females have to continue to lay eggs with developing mature eggs during their lifespan, resulting in a relatively low daily number of eggs laid. Because adult butterflies feed on nectar that contains sugars with little protein, the nutrients used for egg development are those from the fat body accumulated in the abdomen, derived from host plants during larval stage. Because there is no intake of additional nutrients from nectar except sugars throughout the adult stage, using nutrients from the larval host plants appears to be a trade-off relationship between egg development and somatic maintenance. In laboratory experiments, a single mated female pierid butterfly laid eggs every day, and the egg size decreased with each day. However, females could obtain alternative nutrients for egg development and somatic maintenance throughout the adult stage, in which the nutrients are obtained from the ejaculates derived by males when copulating. A spermatophore is a nutrient-rich investment of the males that includes amino acids and sugars. Therefore, females tend to mate more than once to increase the number of eggs actually laid. Because copulating pairs are inactive and can be easily attacked by predators such as birds, multiple matings must increase the mortality risk of the females as well as of the males. Consequently, the optimal number of mating frequencies in females could be the result of a trade-off between the intake of nutrients and mortality risk. In fact, the number of lifetime matings in pierid butterfly females is similar among generations, years and various population densities.

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References

  • Ando S, Watanabe M (1993) Mating frequency and egg load in the white butterfly, Pieris melete Menetries, in a wild environment. Jpn J Ecol 43:111–114. (in Japanese)

    Google Scholar 

  • Baur B, Baur A (1986) Proximate factors influencing egg cannibalism in the land snail Arianta arbustorium (Pulmonata, Helicidae). Oecologia (Berl) 70:283–287

    Article  Google Scholar 

  • Bissoondath CJ, Wiklund C (1995) Protein content of spermatophores in relation to monandry/polyandry in butterflies. Behav Ecol Sociobiol 37:365–371

    Article  Google Scholar 

  • Boggs CL (1981) Selection pressures affecting male nutrient investment at mating in heliconiine butterflies. Evolution 35:931–940

    Article  Google Scholar 

  • Boggs CL, Gilbert LE (1979) Male contribution to egg production in butterflies: evidence for transfer of nutrients at mating. Science 206:83–84

    Article  CAS  PubMed  Google Scholar 

  • Boggs CL, Watt WB (1981) Population structure of pierid butterflies. IV. Genetic and physiological investment in offspring by male Colias. Oecologia (Berl) 50:320–324

    Article  Google Scholar 

  • Charlat S, Reuter M, Dyson EA, Hoenett EA, Duplouy A, Davies N, Roderick GK, Wedell N, Hurst GDD (2007) Male-killing bacteria trigger a cycle of increasing male fatigue and female promiscuity. Curr Biol 17:273–277

    Article  CAS  PubMed  Google Scholar 

  • Courtney SP (1986) The ecology of pierid butterflies: dynamics and interactions. Adv Ecol Res 15:51–131

    Article  Google Scholar 

  • Dunlap-Pianka H, Boggs CL, Gilbert LE (1977) Ovarian dynamics in heliconiine butterflies: programmed senescence versus eternal youth. Science 197:487–490

    Article  CAS  PubMed  Google Scholar 

  • Engebretson JA, Mason WH (1980) Transfer of 65Zn at mating in Heliothis virescens. Environ Entomol 9:119–121

    Article  Google Scholar 

  • Feeny P (1970) Seasonal changes in oak leaf tannins and nutrients as a cause of spring feeding by winter moth caterpillars. Ecology 51:565–581

    Article  Google Scholar 

  • Feltwell J (1986) The natural history of butterflies. Croom Helm, London

    Google Scholar 

  • Honda K, Hayashi N (1995) Chemical factors in rutaceous plants regulating host selection by two swallowtail butterflies, Papilio protenor and P. xuthus (Lepidoptera: Papilionidae). Appl Entomol Zool 30:327–334

    CAS  Google Scholar 

  • Jones JS (1982) Of cannibals and kin. Nature (Lond) 299:202–203

    Article  Google Scholar 

  • Karlsson B. (1996) Male reproductive reserves in relation to mating system in butterflies: a comparative study. Proc R Soc Lond B 263:187–192

    Google Scholar 

  • Karlsson B (1998) Nuptial gifts, resource budgets, and reproductive output in a polyandrous butterfly. Ecology 79:2931–2940

    Article  Google Scholar 

  • Kimura K, Tsubaki Y (1985) Egg weight variation associated with female age in Pieris rapae crucivora Boisduval (Lepidoptera: Pieridae). Appl Entomol Zool 20:500–501

    Google Scholar 

  • Kimura K, Tsubaki Y (1986) Oviposition schedule of the small white butterfly, Pieris melete Menetries (Lepidoptera: Pieridae). Appl Entomol Zool 21:28–32

    Google Scholar 

  • Konagaya T, Watanabe M (2015) Adaptive significance of the mating of autumn-morph females with non-overwintering summer-morph males in the Japanese common grass yellow, Eurema mandarina (Lepidoptera: Pieridae). Appl Entomol Zool 50:41–47

    Article  Google Scholar 

  • Konagaya T, Mutoh N, Suzuki M, Rutowski RL, Watanabe M (2015) Estimates of female lifetime fecundity and changes in the number and types of sperm stored with age and time since mating in the monandrous swallowtail butterfly, Battus philenor (Lepidoptera: Papilionidae) in the Arizona desert. Appl Entomol Zool 50:311–316

    Article  Google Scholar 

  • Labine PA (1966) The population biology of the butterfly, Euphydryas editha. IV. Sperm precedence: a preliminary report. Evolution 20:580–586

    Article  Google Scholar 

  • Labine PA (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

    Article  Google Scholar 

  • Lai-Fook J (1984) The spermatophore of the skipper, Calpodes ethlius (Hesperiidae: Lepidoptera): the sperm sac. Can J Zool 62:1135–1143

    Article  Google Scholar 

  • Lai-Fook J (1991) Absorption of phosphorus from the spermatophore through the cuticle of the bursa copulatrix of the butterfly, Calpodes ethilus. Tissue Cell 23:247–259

    Article  CAS  PubMed  Google Scholar 

  • Lederhouse RC (1981) The effect of female mating frequency on egg fertility in the black swallowtail, Papilio polyxenes asterius (Papilionidae). J Lepid Soc 35:266–277

    Google Scholar 

  • Leong KHL, Yoshimura MA, Williams C (2012) Adaptive significance of previously mated monarch butterfly females (Danaus plexippus (Linnaeus)) overwintering at a California winter site. J Lepid Soc 66:205–210

    Google Scholar 

  • Marshall LD (1982) Male nutrient investment in the Lepidoptera: what nutrients should males invest? Am Nat 120:273–279

    Article  Google Scholar 

  • Marshall LD (1985) Protein and lipid composition of Colias philodice and C. eurytheme spermatophores and their changes over time. J Res Lepid 24:21–30

    Google Scholar 

  • Nakanishi Y, Watanabe M, Ito T (1996) Differences in lifetime reproductive output and mating frequency of two female morphs of the sulfur butterfly, Colias erate (Lepidoptera: Pieridae). J Res Lepid 35:1–8

    Article  Google Scholar 

  • Oberhauser KS (1992) Rate of ejaculate breakdown and intermating intervals in monarch butterflies. Behav Ecol Sociobiol 31:367–373

    Article  Google Scholar 

  • Odendaal FJ, Iwasa Y, Ehrlich PR (1985) Duration of female availability and its effect on butterfly mating systems. Am Nat 125:673–678

    Article  Google Scholar 

  • Ohsaki N (1980) Comparative population studies of three Pieris butterflies, P. rapae, P. melete and P. napi, living in the same area. II. Utilization of patchy habitats by adults through migratory and non-migratory movements. Res Popul Ecol 22:163–183

    Article  Google Scholar 

  • Ohtani T, Yamamoto M (1985) The adult behavior of the Japanese cabbage white (Lepidoptera, Pieridae) in the field. II. Ecological aspects of major behavior patterns. Tyo to Ga 36:43–76

    Google Scholar 

  • Porter K (1992) Eggs and egg-laying. In: Dennis RHD (ed) The ecology of butterflies in Britain. Oxford University Press, Oxford, pp 46–72

    Google Scholar 

  • Prudic KL, Jeon C, Cao H, Monteiro A (2011) Developmental plasticity in sexual roles of butterfly species drives mutual sexual ornamentation. Science 331:73–75

    Article  CAS  PubMed  Google Scholar 

  • Rausher MD (1978) Search image for leaf shape in a butterfly. Science 200:1071–1073

    Article  CAS  PubMed  Google Scholar 

  • Rausher MD (1979) Egg recognition: its advantage to a butterfly. Anim Behav 27:1034–1040

    Article  Google Scholar 

  • Rothschild M, Schoonhoven LM (1977) Assessment of egg load by Pieris brassicae (Lep., Pieridae). Nature (Lond) 266:352–355

    Article  Google Scholar 

  • Rutowski RL (1980) Male scent-producing structures in Colias butterflies—function, localization, and features. J Chem Ecol 6:13–26

    Article  CAS  Google Scholar 

  • Rutowski RL (1984) Sexual selection and the evolution of butterfly mating behavior. J Res Lepid 23:125–142

    Google Scholar 

  • Rutowski RL, Long CE, Marshall LD, Vetter RS (1981) Courtship solicitation by Colias females (Lepidoptera: Pieridae). Am Midl Nat 105:334–340

    Article  Google Scholar 

  • Rutowski RL, Gilchrist GW, Terkanian B (1987) Female butterflies mated with recently mated males show reduced reproductive output. Behav Ecol Sociobiol 20:319–322

    Article  Google Scholar 

  • Shapiro AM (1970) The role of sexual behavior in density-related dispersal of pierid butterflies. Am Nat 104:367–372

    Article  Google Scholar 

  • Shapiro AM (1981) The pierid red-egg syndrome. Am Nat 117:276–294

    Article  Google Scholar 

  • Sharifi S, Zarea N (1970) Biology of the citrus butterfly Papilio demoleus demoleus (Lepidoptera: Papilionidae). Ann Entomol Soc Am 63:1211–1213

    Article  Google Scholar 

  • South A, Lewis SM (2011) The influence of male ejaculate quantity on female fitness: a meta-analysis. Biol Rev 86:299–309

    Article  PubMed  Google Scholar 

  • Stern VM, Smith RF (1960) Factors affecting egg production and oviposition in populations of Colias philodice eurytheme Boisduval (Lepidoptera: Pieridae). Hilgardia 29:411–454

    Article  Google Scholar 

  • Sugawara T (1979) Stretch reception in the bursa copulatrix of the butterfly, Pieris rapae crucivora, and its role in behaviour. J Comp Physiol 130:191–199

    Article  Google Scholar 

  • Suzuki Y (1978) Adult longevity and reproductive potential of the small cabbage white, Pieris rapae crucivora Boisudual (Lepidoptera: Pieridae). Appl Entomol Zool 13:312–313

    Google Scholar 

  • Suzuki Y (1979) Mating frequency in females of the small cabbage white, Pieris rapae crucivora Boisduval (Lepidoptera: Pieridae). Kontyu 47:335–339

    Google Scholar 

  • Svärd L, Wiklund C (1986) Different ejaculate strategies in first versus subsequent matings in the monarch butterfly Papilio machaon L. Behav Ecol Sociobiol 18:325–330

    Article  Google Scholar 

  • Svärd L, Wiklund C (1988) Prolonged mating in the monarch butterfly Danaus plexippus and nightfall as a cue for sperm transfer. Oikos 52:351–354

    Article  Google Scholar 

  • Svärd L, Wiklund C (1989) Mass and production rate of ejaculates in relation to monandry/polyandry in butterflies. Behav Ecol Sociobiol 24:395–402

    Article  Google Scholar 

  • Svärd L, Wiklund C (1991) The effect of ejaculate mass on female reproductive output in the European swallowtail butterfly, Papilio machaon (L.) (Lepidoptera: Papilionidae). J Insect Behav 4:33–41

    Article  Google Scholar 

  • Tigreros N, Sass EM, Lewis SM (2013) Sex-specific response to nutrient limitation and its effects on female mating success in a gift-giving butterfly. Evol Ecol 27:1145–1158

    Article  Google Scholar 

  • Vahed K (1998) The function of nuptial feeding in insects: a review of empirical studies. Biol Rev 73:43–78

    Article  Google Scholar 

  • Välimäki P, Kaitala A, Kokko H (2006) Temporal patterns in reproduction may explain variation in mating frequencies in the green-veined white butterfly Pieris napi. Behav Ecol Sociobiol 61:99–107

    Article  Google Scholar 

  • Välimäki P, Kivelä SM, Mäenpää MI (2011) Mating with a kin decreases female remating interval: a possible example of inbreeding avoidance. Behav Ecol Sociobiol 65:2037–2047

    Article  Google Scholar 

  • Vane-Wright D (2003) Butterflies. The Natural History Museum, London

    Google Scholar 

  • Watanabe M (1979) Natural mortalities of the swallowtail butterfly, Papilio xuthus L., at patchy habitats along the flyways in a hilly region. Jpn J Ecol 29:85–93

    Google Scholar 

  • Watanabe M (1981) Population dynamics of the swallowtail butterfly, Papilio xuthus L., in a deforested area. Res Popul Ecol 23:74–93

    Article  Google Scholar 

  • Watanabe M (1982) Leaf structure of Zanthoxylum ailanthoides Sieb. et Zucc. (Rutales: Rutaceae) affecting the mortality of a swallowtail butterfly, Papilio xuthus L. (Lepidoptera: Papilionidae). Appl Entomol Zool 17:151–159

    Google Scholar 

  • Watanabe M (1983) Radial growth patterns of a pioneer tree, Zanthoxylum ailanthoides Sieb. et Zucc. (Rutales: Rutaceae), related to the population dynamics of a swallowtail butterfly, Papilio xuthus L. (Lepidoptera: Papilionidae). Jpn J Ecol 33:253–261

    Google Scholar 

  • Watanabe M (1988) Multiple matings increase the fecundity of the yellow swallowtail butterfly, Papilio xuthus L., in summer generations. J Insect Behav 1:17–29

    Article  Google Scholar 

  • Watanabe M, Ando S (1993) Influence of mating frequency of lifetime fecundity in wild females of the small white Pieris rapae (Lepidoptera, Pieridae). Jpn J Entomol 61:691–696

    Google Scholar 

  • Watanabe M, Ando S (1994) Egg load in wild females of the small white Pieris rapae crucivora (Lepidoptera, Pieridae) in relation to mating frequency. Jpn J Entomol 62:293–297

    Google Scholar 

  • Watanabe M, Hirota M (1999) Effects of sucrose intake on spermatophore mass produced by male swallowtail butterfly Papilio xuthus L. Zool Sci 16:55–61

    Article  Google Scholar 

  • Watanabe M, Nozato K (1986) Fecundity of the yellow swallowtail butterflies, Papilio xuthus and P. machaon hippocrates, in a wild environment. Zool Sci 3:509–516

    Google Scholar 

  • Watanabe M, Oh’ura T (1997) Egg cannibalism by newly hatched larvae of the small white butterfly, Pieris rapae crucivora (Pieridae), on an artificial diet. J Lepid Soc 51:304–315

    Google Scholar 

  • Watanabe M, Omata K (1978) On the mortality factors of the lycaenid butterfly, Artopoetes pryeri M. (Lepidoptera, Lycaenidae). Jpn J Ecol 28:367–370

    Google Scholar 

  • Watanabe M, Sato K (1993) A spermatophore structured in the bursa copulatrix of the small white Pieris rapae (Lepidoptera, Pieridae) during copulation and its sugar content. J Res Lepid 32:26–36

    Google Scholar 

  • Watanabe M, Yamaguchi H (1993) Egg cannibalism and egg distribution of two Pieris butterflies, Pieris rapae and P. melete (Lepidoptera, Pieridae) on a host plant, Rorippa indica (Cruciferae). Jpn J Ecol 43:181–188. (in Japanese with English summary)

    Google Scholar 

  • Watanabe M, Nozato K, Kiritani K (1986) Studies on ecology and behavior of Japanese black swallowtail butterflies (Lepidoptera: Papilionidae). 5. Fecundity in summer generations. Appl Entomol Zool 21:448–453

    Google Scholar 

  • Watanabe M, Koizumi H, Suzuki N, Kiritani K (1988) Studies on ecology and behavior of Japanese black swallowtail butterflies. 7. Nectar of a glory tree, Clerodendron trichotomum, as a food resource of adults in summer. Ecol Res 3:175–180

    Article  Google Scholar 

  • Watanabe M, Bon’no M, Hachisuka A (2000) Eupyrene sperm migrates to spermatheca after apyrene sperm in the swallowtail butterfly, Papilio xuthus L. (Lepidoptera: Papilionidae). J Ethol 18:91–99

    Article  Google Scholar 

  • Wedell N, Cook PA (1998) Determinants of paternity in a butterfly. Proc R Soc Lond B 265:625–630

    Google Scholar 

  • Wiklund C, Kaitala A, Lindfors V, Abenius J (1993) Polyandry and its effect on female reproductive output in the green-veined white butterfly (Pieris napi L.). Behav Ecol Sociobiol 33:25–33

    Article  Google Scholar 

  • Wiklund C, Kaitala A, Wedell N (1998) Decoupling of reproductive rates and parental expenditure in a polyandrous butterfly. Behav Ecol 9:20–25

    Article  Google Scholar 

  • Yamamoto M (1981) Comparison of population dynamics of 2 pierid butterflies, Pieris rapae crucivora and Pieris napi nesis, living in the same area and feeding on the same plant in Sapporo, northern Japan. J Fac Sci Hokkaido Univ Ser VI Zool 22:202–249

    Google Scholar 

  • Zalucki MP, Kitching RL (1982) Dynamics of oviposition in Danaus plexippus (Insecta: Lepidoptera) in milkweed, Asclepias spp. J Zool (Lond) 198:103–116

    Article  Google Scholar 

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  1. Graduate School of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Ibaraki, Japan

    Mamoru Watanabe

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Watanabe, M. (2016). Necessary Requirements for Oviposition. In: Sperm Competition in Butterflies. Ecological Research Monographs. Springer, Tokyo. https://doi.org/10.1007/978-4-431-55945-0_4

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