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Mating behaviour of female Tuta absoluta (Lepidoptera: Gelechiidae): polyandry increases reproductive output

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Abstract

Tuta absoluta (Meyrick) is an important pest of tomato. Mass trapping of males has seldom proved an effective control measure, probably due to the pest’s reproductive biology. There are few studies on female mating behaviour. For this reason, this study aimed to determine female mating frequency and its effects on reproductive output and female longevity; the effects of male mating status on female reproductive output and longevity and the fate of the spermatophore inside the bursa copulatrix. The studied population of T. absoluta mated only once a day at the beginning of the photophase, females remated frequently and can be classified as polyandrous. The refractory period of both T. absoluta males and females was very short and was not observed in many cases. The lack of refractory period could be due to the female’s rapid metabolism of the spermatophore thus allowing the female to reduce the intermating interval and mate again. Remating had direct benefits for T. absoluta females increasing their fecundity, fertility and longevity. These benefits were greater when females could remate to virgin males instead of to the same male. In this species, therefore, polyandry has direct benefits for the female. The occurrence of polyandry together with other known or unknown reasons can explain the failure of control methods based on pheromones in the open greenhouses in some tomato-growing areas.

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References

  • Abbes K, Harbi A, Chermiti B (2012) Comparative study of 2 protection strategies against Tuta absoluta (Meyrick) ina late open field tomato crops in Tunisia. Bull OEPP/EPPO Bull 42:297–304

    Article  Google Scholar 

  • Arnó J, Gabarra R (2011) Side effects of selected insecticides on the Tuta absoluta (Lepidoptera: Gelechiidae) predators Macrolophus pygmaeus and Nesidiocoris tenuis (Hemiptera: Miridae). J Pest Sci 84:513–520

    Article  Google Scholar 

  • Arnqvist G, Nilsson T (2000) The evolution of polyandry: multiple mating and female fitness in insects. Anim Behav 60:145–164

    Article  PubMed  Google Scholar 

  • Attygalle AB, Jham GN, Svatos A, Frighetto RTS et al (1995) Microscale, random reduction-application to the characterization of (3E,8Z,11Z)-3,8,11-tetradecatrienyl acetate, a new Lepidopteran sex-pheromone. Tetrahedron Lett 36:5471–5474

    Article  CAS  Google Scholar 

  • Balzan MV, Wackers FL (2013) Flowers to selectively enhance the fitness of a host-feeding parasitoid: Adult feeding by Tuta absoluta and its parasitoid Necremnus artynes. Biol Control 67:21–31

    Article  Google Scholar 

  • Batalla-Carrera L, Morton A, Garcia-del-Pino F (2010) Efficacy of entomopathogenic nematodes against the tomato leafminer Tuta absoluta in laboratory and greenhouse conditions. Biocontrol 55:523–530

    Article  Google Scholar 

  • Benvenga SR, Fernandes OA, Gravena S (2007) Tomada de decisão de controle da traça-do-tomateiro através de armadilhas com feromônio sexual. Hortic Bras 25:164–169

    Article  Google Scholar 

  • Bergström J, Wiklund C (2002) Effects of size and nuptial gifts on butterfly reproduction: can females compensate for a smaller size through male-derived nutrients? Behavior Ecol Sociobiol 52:296–302

    Article  Google Scholar 

  • Biondi A, Desneux N, Siscaro G, Zappalà L (2012a) Using organic-certified rather than synthetic pecticides may not be safer for biological control agents: Selectivity and side effects of 14 pesticides on the predator Orius laevigatus. Chemosphere 87:803–812

    Article  CAS  PubMed  Google Scholar 

  • Biondi A, Mommaerts V, Smagghe G, Vinuela E et al (2012b) The non-target impact of spinosyns on beneficial arthropods. Pest Manag Sci 68:1523–1536

    Article  CAS  PubMed  Google Scholar 

  • Biondi A, Desneux N, Amiens-Desneux E, Siscaro G, Zappalà L (2013) Biology and developmental strategies of the Palaearctic parasitoid Bracon nigricans (Hymenoptera: Braconidae) on the Neotropical moth Tuta absoluta (Lepidoptera: Gelechiidae). J Econ Entomol 106:1638–1647

    Article  PubMed  Google Scholar 

  • Bompard A, Jaworski CC, Bearez P, Desneux N (2013) Sharing a predator: can an invasive alien pest affect the predation on a local pest? Pop Ecol 55:433–440

    Article  Google Scholar 

  • Caballero-Mendieta N, Cordero C (2013) Male mating cost in a butterfly that produces small ejaculates. Physiol Entomol. doi:10.1111/phen.12037

    Google Scholar 

  • Cabello T, Gallego JR, Fernandez FJ, Gamez M et al (2012) Biological control strategies for the South American tomato moth (Lepidoptera: Gelechiidae) in greenhouse tomatoes. J Econ Entomol 105:2085–2096

    Article  PubMed  Google Scholar 

  • Cagnotti CL, Viscarret MM, Riquelme MB, Botto EN et al (2012) Effects of X-rays on Tuta absoluta for use in inherited sterility programmes. J Pest Sci 85:413–421

    Article  Google Scholar 

  • Calvo FJ, Soriano D, Bolckmans K, Belda JE (2013) Host instar suitability and life-history parameters under different temperature regimes of Necremnus artynes on Tuta absoluta. Biocontrol Sci Techn 23:803–815

    Article  Google Scholar 

  • Caparros-Megido R, Haubruge E, Verheggen FJ (2012) First evidence of deuterotokous parthenogenesis in the tomato leafminer, Tuta absoluta (Meyrick) (Lepidoptera: gelechiidae). J Pest Sci 85:409–412

    Article  Google Scholar 

  • Caparros-Megido R, Brostaux Y, Haubruge E, Verheggen FJ (2013a) Propensity of the tomato leafminer, Tuta absoluta (Lepidoptera: gelechiidae), to develop on four potato plant varieties. Am J Potato Res 90:255–260

    Article  Google Scholar 

  • Caparros-Megido R, Brostaux Y, Haubruge E, Verheggen FJ (2013b) Pheromone-based management strategies to control the tomato leafminer, Tuta absoluta (Lepidoptera: gelechiidae). A review. Biotechnol Agron Soc Environ 17:475–482

    Google Scholar 

  • Centurion Statgraphics (2009) Statgraphics® Centurion XVI user manual. StatPoint Technologies Inc, Warrenton

    Google Scholar 

  • Chailleux A, Desneux N, Seguret J, Hong DTK et al (2012) Assessing European egg parasitoids as a mean of controlling the invasive South American tomato pinworm Tuta absoluta. PLoS ONE 7:e48068. doi:10.1371/journal.pone.0048068

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Chailleux A, Bearez P, Pizzol J, Amiens-Desneux E et al (2013) Potential for combined use of parasitoids and generalist predators for biological control of the key invasive tomato pest Tuta absoluta. J Pest Sci 86:533–541

    Article  Google Scholar 

  • Chermiti B, Abbes K (2012) Comparison of pheromone lures used in mass trapping to control the tomato leafminer Tuta absoluta (Meyrick, 1917) in industrial tomato crops in Kairouan (Tunisia). Bull OEPP/EPPO Bull 42:241–248

    Article  Google Scholar 

  • Cocco A, Deliperi S, Delrio G (2012) Potential of mass trapping for Tuta absoluta management in greenhouse tomato crops using light and pheromone traps. IOBC-WPRS Bulletin 80:319–324

    Google Scholar 

  • Cocco A, Deliperi S, Delrio G (2013) Control of Tuta absoluta (Meyrick) (Lepidoptera: gelechiidae) in greenhouse tomato crops using the mating disruption technique. J Appl Entomol 137:16–28

    Article  CAS  Google Scholar 

  • Coelho MCF, França FH (1987) Biologia, quetotaxia da larva e descrição da pupa e adulto da traça-do-tomateiro. Pesq Agropec Bras 22:129–135

    Google Scholar 

  • de Medeiros MA, Sujii ER, Rasi GC, Liz RS, de Morais HC (2009) Padrão de oviposição e tabela de vida da traça-do-tomateiro Tuta absoluta (Meyrick) (Lepidoptera, Gelechiidae). Rev Bras Entomol 53:452–456

    Article  Google Scholar 

  • Desneux N, Decourtye A, Delpuech JM (2007) The sublethal effects of pesticides on beneficial arthropods. Annu Rev Entomol 52:81–106

    Article  CAS  PubMed  Google Scholar 

  • Desneux N, Wajnberg E, Wyckhuys KAG, Burgio G et al (2010) Biological invasion of European tomato crops by Tuta absoluta: ecology, geographic expansion and prospects for biological control. J Pest Sci 83:197–215

    Article  Google Scholar 

  • Desneux N, Luna MG, Guillemaud T, Urbaneja A (2011) The invasive South American tomato pinworm, Tuta absoluta, continues to spread in Afro-Eurasia and beyond: the new threat to tomato world production. J Pest Sci 84:403–408

    Article  Google Scholar 

  • Ferracini C, Ingegno BL, Navone P, Ferrari E et al (2012) Adaptation of indigenous larval parasitoids to Tuta absoluta (Lepidoptera: gelechiidae) in Italy. J Econ Entomol 105:1311–1319

    Article  PubMed  Google Scholar 

  • Foster SP, Ayers RH (1996) Multiple mating and its effects in the lightbrown apple moth, Epiphyas postvittana (Walker). J Insect Physiol 42:657–667

    Article  CAS  Google Scholar 

  • Franco K, Jauset A, Castañé C (2011) Monogamy and polygamy in two species of mirid bugs: a functional-based approach. J Insect Physiol 57:307–315

    Article  CAS  PubMed  Google Scholar 

  • Gabarra R, Arno J, Lara L, Verdu MJ et al (2014) Native parasitoids associated with Tuta absoluta in the tomato production areas of the Spanish Mediterranean Coast. Biocontrol 59:45–54

    Article  Google Scholar 

  • Gontijo PC, Picanço MC, Pereira EJG, Martins JC et al (2013) Spatial and temporal variation in the control failure likelihood of the tomato leaf miner, Tuta absoluta. Ann Appl Biol 152:50–59

    Article  Google Scholar 

  • Gonzalez-Cabrera J, Molla O, Monton H, Urbaneja A (2011) Efficacy of Bacillus thuringiensis (Berliner) in controlling the tomato borer, Tuta absoluta (Meyrick) (Lepidoptera: gelechiidae). Biocontrol 56:71–80

    Article  Google Scholar 

  • Guedes NNC, Picanço MC (2012) The tomato borer Tuta absoluta in South America: pest status, management and insecticide resistance. Bull OEPP/EPPO Bull 42:211–216

    Article  Google Scholar 

  • Hickel ER, Vilela EF (1991) Comportamento de chamamento e aspectos do comportamento de acasalamento de Scrobipalpula absoluta (Lep., Gelechiidae), sob condicoes de campo. Ann Soc Entomol Bras 20:173–182

    Google Scholar 

  • Imenes SDL, Uchôa-Fernandes MA, Campos TB, Takematsu AP (1990) Aspectos biológicos e comportamentais da traça-do-tomateiro Scrobipalpula absoluta (Meyrick, 1917) (Lepidoptera: gelechiidae). Arq Inst Biol 57:63–68

    Google Scholar 

  • Jamoussi K, Sellami S, Nasfi Z, Krichen-Makni S, Tounsi S (2013) Efficiency and midgut histopathological effect of the newly isolated Bacillus thuringiensis KS delta-endotoxins on the emergent pest Tuta absoluta. J Microbial Biotech 23:1099–1106

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Kawagoe T, Suzuki N, Matsumoto K (2001) Multiple mating reduces longevity of females of the windmill butterfly Atrophaneura alcinous. Ecol Entomol 26:258–262

    Article  Google Scholar 

  • Knight AL (2007) Multiple mating of male and female codling moth (Lepidoptera: tortricidae) in apple orchards treated with sex pheromone. Environ Entomol 36:157–164

    Article  CAS  PubMed  Google Scholar 

  • Maluf WR, Silva VD, Cardoso MD, Gomes LAA et al (2010) Resistance to the South American tomato pinworm Tuta absoluta in high acylsugar and/or high zingiberene tomato genotypes. Euphytica 176:113–123

    Article  CAS  Google Scholar 

  • Michereff Filho M, Vilela EF, Jham GN, Attygalle A et al (2000) Initial studies of mating disruption of the tomato moth, Tuta absoluta (Lep., Gelechiidae) using synthetic sex pheromone. J Brazil Chem Soc 11:621–628

    Article  CAS  Google Scholar 

  • Molla O, Gonzalez-Cabrera J, Urbaneja A (2011) The combined use of Bacillus thuringiensis and Nesidiocoris tenuis against the tomato borer Tuta absoluta. Biocontrol 56:883–891

    Article  Google Scholar 

  • Monserrat A (2011) La polilla del tomate Tuta absoluta en la region de Murcia: bases para su control. Consejería de Agricultura y Agua, Región de Murcia. http://archives.eppo.int/MEETINGS/2011_conferences/tuta/Monserrat_Murcia_monografia_Tuta.pdf Accessed 9 January 2014

  • Nuñez P, Zignago A, Paullier J, Nuñez S (2009) Feromonas sexuales para el control de la polilla del tomate Tuta absoluta (Meyrick) (Lep., Gelechiidae). Agrociencia 13:27–35

    Google Scholar 

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

    Article  Google Scholar 

  • Ouye MT, Garcia RS, Graham HM, Martin DF (1965) Mating studies on the Pink Bollworm, Pectinophora gossypiella (Lepidoptera: gelechiidae), based on presence of spermatophores. Ann Ent Soc Am 58:880–882

    Google Scholar 

  • Pereyra PC, Sanchez NE (2006) Effect of two solanaceous plants on developmental and population parameters of the tomato leaf miner, Tuta absoluta (Meyrick) (Lepidoptera: gelechiidae). Neotrop Entomol 35:671–676

    Article  PubMed  Google Scholar 

  • Seth RK, Kaur JJ, Rao DK, Reynolds SE (2002) Sperm transfer during mating, movement of sperm in the female reproductive tract, and sperm precedence in the common cutworm Spodoptera litura. Physiol Entomol 27:1–14

    Article  Google Scholar 

  • Silva SS (2008) Fatores da biologia reprodutiva que influenciam o manejo comportamental de Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). Dissertation, Universidade Federal Rural de Pernambuco

  • Siqueira HAA, Guedes RNC, Fragoso DB, Magalhaes LC (2001) Abamectin resistance and synergism in Brazilian populations of Tuta absoluta (Meyrick) (Lepidoptera: gelechiidae). Int J Pest Manag 47:247–251

    Article  Google Scholar 

  • Solomon JD (1962) Characters for determining sex in elm span worm pupae. J Econ Entomol 55:269–270

    Google Scholar 

  • Stjernholm F, Karlsson B (2000) Nuptial gifts and the use of body resources for reproduction in the green-veined white butterfly Pieris napi. Proc Royal Soc B-Biol Sci 267(1445):807–811

    Article  CAS  Google Scholar 

  • Svärd L, McNeil JN (1994) Female benefit, male risk: polyandry in the true armyworm Pseudaletia unipuncta. Behav Ecol Sociobiol 35:319–326

    Article  Google Scholar 

  • Torres-Vila LM (2013) Polyandry-fecundity relationship in insects: methodological and conceptual problems. J Evol Biol 26:325–334

    Article  CAS  PubMed  Google Scholar 

  • Torres-Vila LM, Jennions MD (2005) Male mating history and female fecundity in the Lepidoptera: do male virgins make better partners? Behav Ecol Sociobiol 57:318–326

    Article  Google Scholar 

  • Torres-Vila LM, Rodriguez-Molina MC, Jennions MD (2004) Polyandry and fecundity in the Lepidoptera: can methodological and conceptual approaches bias outcomes? Behav Ecol Sociobiol 55:315–324

    Article  Google Scholar 

  • Tropea Garzia G, Siscaro G, Biondi A, Zappalà L (2012) Tuta absoluta, an exotic invasive pest from South America now in the EPPO region: biology, distribution and damage. Bull OEPP/EPPO Bull 42:205–210

    Article  Google Scholar 

  • Uchôa-Fernandes MA, Della Lucia TMC, Vilela EF (1995) Mating, oviposition and pupation of Scrobipalpula absoluta (Meyrick) (Lepidoptera: gelechiidae). An Soc Entomol Bras 24:159–164

    Google Scholar 

  • Vacas S, Alfaro C, Primo J, Navarro-Llopis V (2011) Studies on the development of a mating disruption system to control the tomato leafminer, Tuta absoluta Povolny (Lepidoptera: gelechiidae). Pest Manag Sci 67:1473–1480

    Article  CAS  PubMed  Google Scholar 

  • Walters JR, Stafford C, Hardcastle TJ, Jiggins CD (2012) Evaluating female remating rates in light of spermatophore degradation in Heliconius butterflies: pupal-mating monandry versus adult-mating polyandry. Ecol Entomol 37:257–268

    Article  Google Scholar 

  • Wedell N, Wiklund C, Cook PA (2002) Monandry and polyandry as alternative lifestyles in a butterfly. Behav Ecol 13:450–455

    Article  Google Scholar 

  • Xu J, Wang Q (2009) A polyandrous female moth discriminates against previous mates to gain genetic diversity. Anim Behav 78:1309–1315

    Article  Google Scholar 

  • Zappalà L, Bernardo U, Biondi A, Cocco A et al (2012) Recruitment of native parasitoids by the exotic pest Tuta absoluta (Meyrick) in Southern Italy. Bull Insectol 65:51–61

    Google Scholar 

  • Zappalà L, Biondi A, Alma A, Al-Jboory IJ et al (2013) Natural enemies of the South American moth, Tuta absoluta, in Europe, North America and Middle East, and their use in pest control strategies. J Pest Sci 86:635–647

    Article  Google Scholar 

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Acknowledgments

We wish to thank Dr. C López for help with the experiments, Dr. A Jauset and J Goñi who helped with the microphotographs, Dr. R Gabarra for her advice and guidance to establish the first Tuta absoluta rearing in our laboratory, R Berruezo for supplying the insects and J Clariana and JM Forcades for letting us use their farms.

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Correspondence to Marina S. Lee.

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Communicated by N. Desneux.

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Lee, M.S., Albajes, R. & Eizaguirre, M. Mating behaviour of female Tuta absoluta (Lepidoptera: Gelechiidae): polyandry increases reproductive output. J Pest Sci 87, 429–439 (2014). https://doi.org/10.1007/s10340-014-0576-4

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