Abstract
The males of butterflies transfer a spermatophore to the female during mating that can contain nutrients enhancing the reproductive potential of their partners. The nutrients transferred by males can be derived from both larval and adult feeding. These nutrients may be depleted by multiple matings. An apparent difference in adult feeding behaviour between the sexes is puddling on mud, dung and carrion, which in most butterfly species is exclusively a male behaviour. A possible explanation for this division in feeding behaviour is that nutrients derived from puddling by males are transferred to the female during mating. Here, we test this hypothesis in the African fruit-feeding butterfly Bicyclus anynana. We varied the male nuptial gift by (1) feeding males either a diet with or without sodium, and (2) varying the number of previous successful copulations by remating males up to five times on consecutive days. The results show both a strong effect of order of mating on the mating duration, and an individual effect with some males typically copulating for a shorter time than others. The effects on female reproduction were, however, minimal. The total number of eggs per female and the sodium content of the eggs did not differ significantly between diets, nor were they affected by the mating histories of the males. Eggs showed a non-significant lower hatching for females partnered by a male who had already mated several times. There was an indication of an interaction with male diet: the sodium treatment showing a decline in egg hatchability with order number of male mating, whilst the control treatment showed a constant hatchability. The results are discussed in relation to determinants of male gift-giving strategy and to other potential explanations for a restriction of puddling to males in butterflies.
Similar content being viewed by others
References
Andersson J, Borg-Karlson AK, Wiklund C (2000) Sexual cooperation and conflict in butterflies: a male-transferred anti-aphrodisiac reduces harassment of recently mated females. Proc R Soc Lond B Biol Sci 267:1271–1275
Arms K, Feeny P, Lederhouse RC (1974) Sodium: stimulus for puddling behaviour by tiger swallowtail butterflies, Papilio glaucus. Science 185:372–374
Arnqvist G (1989) Sexual selection in a water strider: the function, mechanism of selection and heritability of a male grasping apparatus. Oikos 56:344–350
Arnqvist G (1992) Pre-copulatory fighting in a water strider: inter-sexual conflict or mate assessment. Anim Behav 43:559–567
Bailey SW, Buso DC, Likens GE (2003) Implications of sodium mass balance for interpreting the calcium cycle of a forested ecosystem. Ecology 14:471–484
Beck J, Mühlenberg E, Fiedler K (1999) Mud-puddling behavior in tropical butterflies: in search of proteins or minerals? Oecologia 119:140–148
Bissoondath CJ, Wiklund C (1995) Protein-content of spermatophores in relation to monandry polyandry in butterflies. Behav Ecol Sociobiol 37:365–371
Bissoondath CJ, Wiklund C (1996a) Effect of male mating history and body size on ejaculate size and quality in two polyandrous butterflies, Pieris napi and Pieris rapae (Lepidoptera: Pieridae). Funct Ecol 10:457–464
Bissoondath CJ, Wiklund C (1996b) Male butterfly investment in successive ejaculates in relation to mating system. Behav Ecol Sociobiol 39:285–292
Bissoondath CJ, Wiklund C (1997) Effect of male body size on sperm precedence in the polyandrous butterfly Pieris napi L. (Lepidoptera: Pieridae). Behav Ecol 8:518–523
Boggs CL, Jackson LA (1991) Mud puddling by butterflies is not a simple matter. Ecol Entomol 16:123–127
Brakefield PM, Kesbeke F (1995) Raised adult lifespan and female fecundity in tropical fruit-feeding Bicyclus butterflies. Proc Exp Appl Entomol 6:93–98
Brakefield PM, El Filali E, Van der Laan R, Breuker CJ, Saccheri IJ, Zwaan BJ (2001) Effective population size, reproductive success and sperm precedence in the butterfly, Bicyclus anynana, in captivity. J Evol Biol 14:148–156
Ciereszko A, Dabrowski K, Piros B, Kwasnik M, Glogowski J (2001) Characterization of zebra mussel (Dreissena polymorpha) sperm motility: duration of movement, effects of cations, pH and gossypol. Hydrobiologia 452:225–232
Cook PA, Wedell N (1996) Ejaculate dynamics in butterflies: a strategy for maximizing fertilization success? Proc R Soc Lond B Biol Sci 263:1047–1051
Cook PA, Wedell N (1999) Non-fertile sperm delay female remating. Nature 397:486–486
Delisle J, Bouchard A (1995) Male larval nutrition in Choristoneura rosaceana (Lepidoptera, Tortricidae): an important factor in reproductive success. Oecologia 104:508–517
Delisle J, Hardy M (1997) Male larval nutrition influences the reproductive success of both sexes of the spruce budworm, Choristoneura fumiferana (Lepidoptera: Tortricidae). Funct Ecol 11:451–463
Ehrlich AH, Ehrlich PA (1978) Reproductive strategies in the butterflies: mating frequency, plugging, and egg number. J Kans Entomol Soc 51:666–697
Engebretson JAM, Mason WH (1981) Depletion of trace elements in mated male Heliothis virescens and Drosophila melanogaster. Comp Biochem Physiol 68:323–325
Gonzalez A, Rossini C, Eisner M, Eisner T (1999) Sexually transmitted chemical defense in a moth (Utetheisa ornatrix). Proc Natl Acad Sci USA 96:5570–5574
Gwynne DT (1984) Sexual selection and sexual differences in Mormon crickets (Orthoptera: Tettigoniidae, Anabrus simplex). Evolution 38:1011–1022
Hou ML, Sheng CF (1999) Fecundity and longevity of Helicoverpa armigera (Lepidoptera: Noctuidae): effects of multiple mating. J Econ Entomol 92:569–573
Jones KN, Odendaal R, Francois J, Ehrlich P (1986) Evidence against the spermatophore as paternal investment in checkerspot butterflies (Euphydryas: Nymphalidae). Am Midl Nat 116:1–6
LaMunyon CW, Huffman TS (2001) Determinants of sperm transfer by males of the noctuid moth Heliothis virescens. J Insect Behav 14:187–199
Littell RCM GA, Stroup WW, Wolfinger RD (1996) SAS system for mixed models. SAS Institute, Cary, N.C.
Liu WY, Fox JED, Xu ZF (2003) Nutrient budget of a montane evergreen broad-leaved forest at Ailao Mountain National Nature Reserve, Yunnan, southwest China. Hydrol Process 16:1119–1134
Marshall LD (1982) Male nutrient investment in the Lepidoptera: what nutrients should males invest? Am Nat 120:273–279
Marshall LD, McNeil JN (1989) Spermatophore mass as an estimate of male nutrient investment: a closer look in Pseudaletia-Unipuncta (Haworth) (Lepidoptera, Noctuidae). Funct Ecol 3:605–612
Milner R (2000) Butterfly antiaphrodisiac. Nat Hist 109:79
Miyatake T, Chapman T, Partridge L (1999) Mating-induced inhibition of remating in female Mediterranean fruit flies Ceratitis capitata. J Insect Physiol 45:1021–1028
Norris MJ (1936) The feeding-habits of the adult lepidoptera heteroneura. Trans R Entomol Soc Lond 85:61–90
Oberhauser KS (1989) Effects of spermatophores on male and female monarch butterfly reproductive success. Behav Ecol Sociobiol 25:237–246
Oberhauser KS (1997) Fecundity, lifespan and egg mass in butterflies: effects of male-derived nutrients and female size. Funct Ecol 11:166–175
Pivnick KA, McNeil JN (1987) Puddling in butterflies: sodium affects reproductive success in Thymelicus lineola. Physiol Entomol 12:461–472
Pliske TE (1973) Factors determining mating frequencies in some new world butterflies and skippers. Ann Entomol Soc Am 66:164–169
Poulton EB (1917) Salt (chloride of sodium) probably sought by the Hesperidae. Proc Entomol Soc Lond 1:76–80
Rossato M, Balercia G, Lucarelli G, Foresta C, Mantero F (2002) Role of seminal osmolarity in the regulation of human sperm motility. Int J Androl 25:230–235
Ryne C, Zhu JW, Van Dongen S, Lofstedt C (2001) Spermatophore size and multiple mating: effects on reproductive success and post-mating behaviour in the Indian meal moth. Behaviour 138:947–963
Sculley CE, Boggs CL (1996) Mating systems and sexual division of foraging effort affect puddling behaviour by butterflies. Ecol Entomol 21:193–197
Seastedt TR, Crossley DA (1980) Sodium dynamics in forest ecosystems and the animal starvation hypothesis. Am Nat 117:1029–1034
Simmons LW (1988) The contribution of multiple mating and spermatophore consumption to the lifetime reproductive success of female field crickets (Gryllus bimaculatus). Ecol Entomol 13:57–69
Simmons LW (1990) Nuptial feeding in tettigoniids: male costs and the rates of fecundity increase. Behav Ecol Sociobiol 27:43–47
Simmons LW, Gwynne DT (1993) Reproductive investment in bush-crickets: the allocation of male and female nutrients to offspring. Proc R Soc Lond B Biol Sci 5:1–5
Smedley SR, Eisner T (1996) Sodium: a male moth’s gift to its offspring. Proc Natl Acad Sci USA 93:809–813
Svard L, Wiklund C (1986) Different ejaculate delivery strategies in first versus subsequent matings in the swallowtail butterfly Papilio machaon. Behav Ecol Sociobiol 18:325–330
Svard L, Wiklund C (1988) Fecundity, egg weight and longevity in relation to multiple matings in females of the monarch butterfly. Behav Ecol Sociobiol 23:39–43
Svard L, Wiklund C (1989) Mass and production-rate of ejaculates in relation to monandry polyandry in butterflies. Behav Ecol Sociobiol 24:395–402
Svard 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
Tiedemann AR, Clary WP (1996) Nutrient distribution in Quercus gambelii stands in central Utah. Great Basin Nat 10:119–128
Vahed K (1998) The function of nuptial feeding in insects: review of empirical studies. Biol Rev Camb Philos Soc 73:43–78
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
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 Lepidoptera 32:26–36
Wedell N (1991) Sperm competition selects for nuptial feeding in a bush-cricket. Evolution 45:1975–1978
Wedell N (1993a) Mating effort or paternal investment: incorporation rate and cost of male donations in the wartbiter. Behav Ecol Sociobiol 32:239–246
Wedell N (1993b) Spermatophore size in bush-crickets: comparative evidence for nuptial gifts as a sperm protection device. Evolution 47:1203–1212
Wedell N, Cook PA (1998) Determinants of paternity in a butterfly. Proc R Soc Lond B Biol Sci 265:625–630
Wedell N, Cook PA (1999) Butterflies tailor their ejaculate in response to sperm competition risk and intensity. Proc R Soc Lond B Biol Sci 266:1033–1039
Wedell N, Wiklund C, Cook PA (2002) Monandry and polyandry as alternative lifestyles in a butterfly. Behav Ecol 13:450–455
Wiklund C, Karlsson B, Leimar O (2001) Sexual conflict and cooperation in butterfly reproduction: a comparative study of polyandry and female fitness. Proc R Soc Lond B Biol Sci 268:1661–1667
Zijlstra WG, Kesbeke F, Zwaan BJ, Brakefield PM (2002) Protandry in the butterfly Bicyclus anynana. Evol Ecol Res 4:1229–1240
Acknowledgements
We thank Fanja Kesbeke, Rinny Kooi and Tim Brakefield for assistance with counting eggs, Bert de Winter, Els Schlatmann, Niels Wurzer and Mariël Lavrijsen for maize cultivation, Tom van Doorn for statistical advice, Jos van Brussel for the sodium analyses, and Małgorzata Arlet, Christer Wiklund and Andreas Erhardt for helpful comments on an earlier version of the manuscript. The funding was provided by the Netherlands Foundation for the Advancement of Tropical Research (WOTRO), (W80-82-238 to P.M.B.) and NWO (811-34-005 to B.J.Z.). The experiments comply with the current laws in the Netherlands.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by M.A. Elgar
Rights and permissions
About this article
Cite this article
Molleman, F., Zwaan, B.J. & Brakefield, P.M. The effect of male sodium diet and mating history on female reproduction in the puddling squinting bush brown Bicyclus anynana (Lepidoptera). Behav Ecol Sociobiol 56, 404–411 (2004). https://doi.org/10.1007/s00265-004-0789-2
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00265-004-0789-2