Abstract
The natural history and mating behavior of a species of tephritid fruit fly in the poorly studied genus Haywardina are described for the first time. Haywardina cuculi Hendel larvae were recovered over four field seasons from infested fruit of Vassobia breviflora (Sendtn.) Hunz, which constitutes a new host plant record for this species. Recovered pupae emerged as adults over 183 days on average, suggesting that most individuals became dormant. Adult flies engaged in sexual activity as soon as two days after emergence, were highly promiscuous, and displayed large variability in copulation duration. As for most tephritid species in the subtribe Carpomyini, H. cuculi exhibited a resource defense mating system. Fly activity peaked around noon. Copulation could last from 9 min to 17 h, with most copulations beginning in the afternoon and lasting until the following day. We discuss the potential significance of copulation duration variability in light of mate guarding and sperm competition hypothesis and outline future research to understand the evolution of life history and these behavioral strategies.




References
Abraham S, Rull J, Mendoza M, Liendo MC, Devescovi F, Roriz AK, Kovaleski A, Segura DF, Vera MT (2014) Differences in sperm storage and remating propensity between adult females of two morphotypes of the Anastrepha fraterculus (Diptera: Tephritidae) cryptic species complex. Bull Entomol Res 104:376–382
Alcock J (1994) Postinsemination associations between males and females in insects: the male guarding hypothesis. Annu Rev Entomol 39:1–21
Alonso-Pimentel H, Papaj DR (1996) Operational sex ratio versus gender density as determinants of copulation duration in the walnut fly, Rhagoletis juglandis (Diptera: Tephritidae). Behav Ecol Sociobiol 39:171–180
Aluja M, Piñero J, Jácome I, Díaz-Fleischer F, Sivinski J (2000) Behavior of flies in the genus Anastrepha (Trypetinae: Toxotrypanini). Fruit flies (Tephritidae): Phylogeny and Evolution of Behavior. CRC Press, Boca Raton, pp 375–408
Andrés JA, Cordero Rivera A (2000) Copulation duration and fertilization success in damselfly: an example of female cryptic choice? Anim Behav 59:695–703
Averill AL, Prokopy RJ (1987) Intraspecific competition in the tephritid fruit fly Rhagoletis pomonella. Ecology 68:878–886
Bernacki FG (2014) Biología floral y frutal de Vassobia breviflora (Sedtn.) Hunz. (Solanaceae) en el noroeste argentino [dissertation]. San Miguel de Tucumán: Universidad Nacional de Tucumán
Bernacki FG, Albornoz P, Valoy M, Ordano M (2015) Anatomía de flor y fruto de Vassobia breviflora (Solanaceae) en el sur de las Yungas australes (Argentina). Phyton-Revista Internacional de Botánica Experimental 84:478–487
Boller EF, Prokopy RJ (1976) Bionomics and management of Rhagoletis. Annu Rev Entomol 21:223–246
Brévault T, Quilici S (2000) Diel patterns of reproductive activities in the tomato fruit fly, Neoceratitis cyanescens. Physiol Entomol 25:233–241
Costello MJ, Wilson S, Houlding B (2012) Predicting total global species richness using rates of species description and estimates of taxonomic effort. Syst Biol 61:871–883
Danks HV (2002) The range of insect dormancy responses. Eur J Entomol 99:127–142
Danks HV (2007) The elements of seasonal adaptations in insects. Can Entomol 139:1–44
Dayton PK (2003) The importance of the natural sciences to conservation. Am Nat 162:1–13
Dickinson JL (1986) Prolonged mating in the milkweed leaf beetle Labidomera clivicollis clivicollis (Coleoptera: Chrysomelidae): a test of the “sperm-loading” hypothesis. Behav Ecol Sociobiol 18:331–338
Dodson GN (1997) Resource defense mating system in antlered flies, Phytalmia spp. (Diptera: Tephritidae). Ann Entomol Soc Am 90:496–504
García-González F, Gomendio M (2004) Adjustment of copula duration and ejaculate size according to the risk of sperm competition in the golden egg bug (Phyllomorpha laciniata). Behav Ecol 15:23–30
Headrick DH, Goeden RD (1994) Reproductive behavior of California fruit flies and the classification and evolution of Tephritidae (Diptera) mating systems. Stud Dipterol 1:194–252
Headrick DH, Goeden RD (1998) The biology of nonfrugivorous tephritid fruit flies. Annu Rev Entomol 43:217–241
Jaldo HE, Gramajo MC, Willink E (2001) Mass rearing of Anastrepha fraterculus (Diptera: Tephritidae): a preliminary strategy. Fla Entomol 84:716–718
Koštál V (2006) Eco-physiological phases of insect diapause. J Insect Physiol 52:113–127
Masetevach Becerra M, Barboza GE (2013) Vassobia. In: Zuloaga FO et al (eds) Flora Fanerogámica Argentina: Programa ProFlora. Dicotyledoneae, Solanaceae, Córdoba, Museo Botánico, IMBIV, pp 148–150
May RM (1988) How many species are there on earth? Science 241:1441–1449
Miller PL (1987) An examination of prolonged copulation of Ischnura elegans (Van der Linden) (Zygoptera: Coenigronidae). Odonatologica 16:201–207
Norrbom AL (1994) New species and phylogenetic analysis of Cryptodacus, Haywardina, and Rhagoletotrypeta (Di ptera: Tephritidae). Insecta Mundi 288
Norrbom AL (2004) Updates to biosystematic database of world Diptera for Tephritidae through 1999. Diptera Data Dissemination Disk (CD-ROM) 2
Norrbom AL, Castillo-Meza AL, Garcia-Chavez JE, Aluja M, Rull J (2014) A new species of Anastrepha (Diptera: Tephritidae) from Euphorbia tehuacana (Euphorbiaceae) in Mexico. Zootaxa 3780:567–576
Nufio CR, Papaj DR (2001) Host marking behavior in phytophagous insects and parasitoids. Entomol Exp Appl 99:273–293
Opp SB, Prokopy RJ (2000) Multiple mating and reproductive success of male and female apple maggot flies, Rhagoletis pomonella (Diptera: Tephritidae). J Insect Behav 13:901–914
Opp SB, Spisak SA, Telang A, Hammond SS (1996) Comparative mating systems of two Rhagoletis species: the adaptive significance of mate guarding. Fruit fly pests: a world assessment of their biology and management. St. Lucie Press, Delray Beach, pp 43–49
Ovruski SM, Schliserman P, Aluja M (2016) Occurrence of diapause in neotropical parasitoids attacking Anastrepha fraterculus (Diptera: Tephritidae) in a subtropical rainforest from Argentina. Austr Entomol 55:274-283
Palacio FX, Valoy M, Bernacki FG, Sánchez MS, Núñez-Montellano MG, Varela O, Ordano M (2015) Bird fruit consumption results from the interaction between fruit-handling behaviour and fruit crop size. Ethol Ecol Evol 28:00–00. doi:10.1080/03949370.2015.1080195 [Published online: 29 Sep 2015]
Papadopoulos NT, Katsoyannos BI, Carey JR (1998) Temporal changes in the composition of the overwintering larval population of the Mediterranean fruit fly (Diptera: Tephritidae) in northern Greece. Ann Entomol Soc Am 91:430–434
Perez-Staples D, Weldon CW, Radhakrishnan P, Prenter J, Taylor PW (2010) Control of copula duration and sperm storage by female Queensland fruit flies. J Insect Physiol 56:1755–1762
Prokopy RJ, Papaj DR (2000) Behavior of flies of the genera Rhagoletis, Zonosemata, and Carpomya (Trypetinae: Carpomyina). Fruit flies (Tephritidae): Phylogeny and Evolution of Behavior. CRC Press, Boca Raton, pp 219–252
Rull J, Abraham S, Kovaleski A, Segura DF, Mendoza M, Liendo M, Vera MT (2013) Evolution of pre-zygotic and post-zygotic barriers to gene flow among three cryptic species within the Anastrepha fraterculus Complex. Entomol Exp Appl 148:213–222
Silverman J, Goeden RD (1980) Life history of a fruit fly, Procecidochares sp., on the ragweed, Ambrosia dumosa (gray) Payne, in southern California (Diptera: Tephritidae). Pan Pac Entomol 56:283–288
Sivinski J (1999) Breeding habits and sex in families closely related to the Tephritidae: opportunities for comparative studies of the evolution of fruit fly behavior. Fruit flies (Tephritidae): Phylogeny and Evolution of Behavior. CRC Press, Boca Raton, pp 23–37
Smith JJ, Bush GL (1999) Phylogeny of the subtribe Carpomyina (Trypetinae), emphasizing relationships of the genus Rhagoletis. Fruit Flies (Tephritidae): Phylogeny and Evolution of Behavior. CRC Press, Boca Raton, pp 187–217
Stork NE, McBroom J, Gely C, Hamilton AJ (2015) New approaches narrow global species estimates for beetles, insects, and terrestrial arthropods. Proc Natl Acad Sci 112:7519–7752
Thomas DB (1997) Degree-day accumulations and seasonal duration of the pre-imaginal stages of the Mexican fruit fly (Diptera: Tephritidae). Fla Entomol 80:71–78
Thornhill R, Alcock J (1983) The evolution of insect mating systems. Harvard University Press, Cambridge
Wilkinson GS, Johns PM (2005) Sexual selection and the evolution of mating systems in flies. The Biology of the Diptera. Columbia University Press, New York, pp 312-339
Acknowledgements
We are grateful to Felipe and Eliseo Rull for keeping us awake during odd ours of the night for behavioral observations. This study was funded by PIP CONICET n° 1353 to Pablo Schlisermann and a CONICET fellowship to Sergio Ovruski and Juan Rull.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Rull, J., Abraham, S., Schlisermann, P. et al. Mating Behavior and Basic Biology of Haywardina cuculi (Diptera: Tephritidae), a Poorly Known Species Exhibiting High Variability in Copulation Duration. J Insect Behav 30, 439–453 (2017). https://doi.org/10.1007/s10905-017-9629-x
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10905-017-9629-x