Abstract
The macadamia nut borer, Gymnandrosoma aurantianum Lima (Lepidoptera: Tortricidae), is the main pest of Macadamia integrifolia Maiden & Betche (Proteales: Proteaceae) in Central America. Despite its importance, there is little information on its reproductive behavior. We studied the calling behavior and effect of age on female sex pheromone production and male antennal response to the pheromone. Calling behavior of G. aurantianum females occurred at the onset of scotophase, between 17:00 and 20:00 h. The mean time spent calling was 64 min. It was observed that 30% of the 50 females exhibited a calling posture characterized by extrusion of the pheromone gland from the tip of the abdomen and they spread their wings slightly. Female age had no influence on the sex pheromone production, while male antennal response increased with age and pheromone dosage. The information obtained in this work contributes to understanding the sexual behavior of G. aurantianum and thus to the creation of strategies to control this important pest in macadamia.
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References
Almeida ÂA, Lima ER, Reis R (2008) Pupal period affects calling behavior of the wheat moth, Pseudaletia sequax (Lepidoptera: Noctuidae). Ethology 114:499–503. https://doi.org/10.1111/j.1439-0310.2008.01492.x
Altesor P, Horas VR, Arcia MP et al (2010) Reproductive behaviour of Crocidosema (=Epinotia) aporema (Walsingham) (Lepidoptera: Tortricidae): Temporal pattern of female calling and mating. Neotrop Entomol 39:324–329
Ambrogi BG, Fonseca MG, Coracini MDA, Zarbin PHG (2009) Calling behaviour and male response towards sex pheromone of poplar moth Condylorrhiza vestigialis (Lepidoptera: Crambidae). J Pest Sci 82:55–60. https://doi.org/10.1007/s10340-008-0219-8
Aranda-Arguello R, Rojas JC, Malo EA et al (2022) Male attraction of Gymnandrosoma aurantianum (Lepidoptera : Tortricidae), from Guatemala, to its sex pheromone major component is not affected by the addition of secondary components. Can Entomol 154:1–13. https://doi.org/10.4039/tce.2022.37
Baker TC, Cardé RT (1979) Endogenous and exogenous factors affecting periodicities of female calling and male sex pheromone response in Grapholitha molesta (Busck). J Insect Physiol 25:943–950. https://doi.org/10.1016/0022-1910(79)90107-0
Bento JMS, Parra JRP, Vilela EF et al (2001) Sexual behavior and diel activity of citrus fruit borer: Ecdytolopha aurantiana. J Chem Ecol 27:2053–2065. https://doi.org/10.1023/A:1012294921058
Blanco-Metzler H, Watt A, Cosens D (1993) Ciclo de vida y comportamiento de oviposición de Ecdytolopha torticornis (Lepidoptera: Tortricidae) barrenador de la nuez de macadamia. Manejo Integr Plagas 29:36–39
Blanco-Metzler H (1994) The biology and ecology of the macadamia nutborer Ecdytolopha torticornis in Costa Rica. PhD Thesis, University of Edinburgh, Scotland, p 131
Cardé RT, Haynes KF (2004) Structure of the pheromone communication channel in moths. In: Cardé RT, Millar JG (eds) Advances in the chemical ecology of insects. Cambridge University Press, Cambridge, pp 283–332
Cardé AM, Baker TC, Cardé RT (1979) Identification of a four-component sex pheromone of the female oriental fruit moth, Grapholitha molesta (Lepidoptera: Tortricidae). J Chem Ecol 5:423–427. https://doi.org/10.1007/BF00987927
Castrejon-Gómez VR, Rojas JC (2006) Calling behavior of Zamagiria dixolophella (Lepidoptera: Pyralidae). Florida Entomol 89:83–84. https://doi.org/10.1653/0015-4040(2006)89[83:CBOZDL]2.0.CO;2
Cruz-Esteban S, Rojas JC, Malo EA (2017) Calling behavior, copulation time, and reproductive compatibility of corn-strain fall armyworm (Lepidoptera: Noctuidae) from populations in Mexico. Environ Entomol 46:901–906. https://doi.org/10.1093/ee/nvx120
Del Mazo-Cancino A, Malo EA, Cruz-López L, Rojas JC (2004) Diel periodicity and influence of age and mating on female sex pheromone titre in Estigmene acrea (Lep., Arctiidae). J Appl Entomol 128:459–463. https://doi.org/10.1111/j.1439-0418.2004.00872.x
Delisle J, Royer L (1994) Changes in pheromone titer of oblique-banded leafroller, Choristoneura rosaseana virgin females as a function of time of day, age, and temperature. J Chem Ecol 20:45–69
Eiras ÁE (2000) Calling behaviour and evaluation of sex pheromone glands extract of Neoleucinodes elegantalis Guenée (Lepidoptera: Crambidae) in wind tunnel. An Soc Entomol Bras 29:453–460
Fatzinger CW (1973) Circadian rhythmicity of sex pheromone release by Dioryctria abietella (Lepidoptera: Pyralidae (Phycitinae)) and the effect of a diel light cycle on its precopulatory behavior. Ann Entomol Soc Am 66:1147–1153
Foster SP, Anderson KG (2022) Some factors influencing calling behavior and mass emission rate of sex pheromone from the gland of the moth Chloridea virescens. J Chem Ecol 48:141–151. https://doi.org/10.1007/s10886-021-01334-2
Garcia MS, Parra JRP (1999) Comparação de dietas artificiais, com fontes protéicas variáveis, para criação de Ecdytolopha aurantiana (Lima) (Lepidoptera: Tortricidae). An Soc Entomol Bras 28:219–232. https://doi.org/10.1590/s0301-80591999000200004
Giebultowicz JM, Webb RE, Raina AK, Ridgway RL (1992) Effects of temperature and age on daily changes in pheromone titer in laboratory-reared and wild gypsy moth (Lepidoptera: Lymantriidae). Environ Entomol 21:822–826. https://doi.org/10.1093/ee/21.4.822
Gorsuch CS, Karandinos MG, Koval CF (1975) Daily rhythm of Synanthedon pictipes (Lepidoptera: Aegeriidae) female calling behavior in Wisconsin: temperature effects. Entomol Exp Appl 18:367–376. https://doi.org/10.1111/j.1570-7458.1975.tb00409.x
Itagaki H, Conner WE (1988) Calling behavior of Manduca sexta (L.) (Lepidoptera: Sphingidae) with notes on the morphology of the female sex pheromone gland. Ann Entomol Soc Am 81:798–807. https://doi.org/10.1093/aesa/81.5.798
Kamimura M, Tatsuki S (1993) Diel rhythms of calling behavior and pheromone production of oriental tobacco budworm moth, Helicoverpa assulta (Lepidoptera: Noctuidae). J Chem Ecol 19:2953–2963
Kawazu K, Tatsuki S (2002) Diel rhythms of calling behavior and temporal change in pheromone production of the rice leaffolder moth, Cnaphalocrocis medinalis (Lepidoptera: Crambidae). Appl Entomol Zool 37:219–224. https://doi.org/10.1303/aez.2002.219
Kawazu K, Adati T, Tatsuki S (2011) The effect of photoregime on the calling behavior of the rice leaf folder moth, Cnaphalocrocis medinalis (Lepidoptera: Crambidae). Japan Agric Res Q 45:197–202. https://doi.org/10.6090/jarq.45.197
Leal WS, Bento JMS, Murata Y et al (2001) Identification, synthesis, and field evaluation of the sex pheromone of the citrus fruit borer: Ecdytolopha aurantiana. J Chem Ecol 27:2041–2051. https://doi.org/10.1023/A:1012242904220
Levi-Zada A, Byers JA (2021) Circadian rhythms of insect pheromone titer, calling, emission, and response: A review. Sci Nat 108:1–20. https://doi.org/10.1007/s00114-021-01746-w
Liu H, Zhao W, Yang M et al (2013) Diel rhythms of sexual behavior and pheromone titers in Isoceras sibirica Alpheraky (Lepidoptera, Cossidae). Arch Insect Biochem Physiol 84:15–26. https://doi.org/10.1002/arch.21109
López-Guillén G, Ruiz JG, Brown JW et al (2021) First records of Lepidoptera damaging Macadamia integrifolia (Proteaceae) fruits in Guatemala. Proc Entomol Soc Washingt 123:341–349. https://doi.org/10.4289/0013-8797.123.2.341
Ma T, Zhang Y, Wang S et al (2018) Reproductive behavior and sex pheromone production in Eutectona machaeralis (Lepidoptera: Crambidae). Florida Entomol 101:189–194. https://doi.org/10.1653/024.101.0206
Malo EA, Renou M, Guerrero A (2000) Analytical studies of Spodoptera littoralis sex pheromone components by electroantennography and coupled gas chromatography-electroantennographic detection. Talanta 52:525–532. https://doi.org/10.1016/S0039-9140(00)00401-X
Nascimento ES, Ambrogi BG, Pinto-Zevallos DM, Sousa-Souto L (2016) Age-dependent pattern of calling behavior in Atheloca subrufella (Hulst) (Lepidoptera: Phycitidae). J Insect Behav 29:190–198. https://doi.org/10.1007/s10905-016-9552-6
Pires CSS, Vilela EF, Viana PA (1994) Comportamento de fêmeas de Elasmopalpus lignosellus (Zeller) (Lepidoptera: Pyralidae) associado à liberação de feromônio sexual. An Soc Entomol Bras 23:1–12. https://doi.org/10.37486/0301-8059.v23i1.901
R Core Team (2022) R: a language and environment for statistical computing. R Core Team, Vienna, Austria
Raina AK, Klun JA, Stadelbacher EA (1986) Diel periodicity and effect of age and mating on female sex pheromone titer in Heliothis zea (Lepidoptera: Noctuidae). Ann Entomol Soc Am 79:128–131. https://doi.org/10.1093/aesa/79.1.128
Raina AK, Davis JC, Stadelbacher EA (1991) Sex pheromone production and calling in Helicoverpa zea (Lepidoptera: Noctuidae): Effect of temperature and light. Environ Entomol 20:1451–1456. https://doi.org/10.1093/ee/20.5.1451
Rehermann G, Altesor P, McNeil JN, González A (2016) Conspecific females promote calling behavior in the noctuid moth, Pseudaletia adultera. Entomol Exp Appl 159:362–369. https://doi.org/10.1111/eea.12448
Royer L, McNeil JN (1991) Changes in calling behaviour and mating success in the european corn borer (Ostrinia nubilalis), caused by relative humidity. Entomol Exp Appl 61:131–138. https://doi.org/10.1111/j.1570-7458.1991.tb02405.x
Seabrook WD, Linn CE, Dyer LJ, Shorey HH (1987) Comparison of electroantennograms from female and male cabbage looper moths (Trichoplusia ni) of different ages and for various pheromone concentrations. J Chem Ecol 13:1443–1453. https://doi.org/10.1007/BF01012290
Soofbaf M, Nouri G, Goldansaz SH, Asghari-Zakaria R (2007) Effects of age and temperature on calling behavior of carob moth, Ectomyelois ceratoniae, Zell. (Lepidoptera: Pyralidae) under laboratory conditions. Pakistan J Biol Sci 10:2976–2979. https://doi.org/10.3923/pjbs.2007.2976.2979
Stelinski LL, Il’ichev AL, Gut LJ (2006) Antennal and behavioral responses of virgin and mated oriental fruit moth (Lepidoptera : Tortricidae) females to their sex pheromone. Ann Entomol Soc Am 99:898–904
Triana MF, Nogueira ASPC, França PHB et al (2020) Sexual behavior of the sugarcane hairy borer, Hyponeuma taltula (Lepidoptera: Erebidae): Evidence for a female-released sex pheromone. Neotrop Entomol 49:739–744. https://doi.org/10.1007/s13744-020-00774-x
Valles SM, Heath RR, Capinera JL (1992) Production and release of sex pheromone by Diaphania nitidalis (Lepidoptera: Pyralidae): Periodicity, age, and density effects. Ann Entomol Soc Am 85:731–735. https://doi.org/10.1093/aesa/85.6.731
Webster RP (1988) Modulation of the expression of calling by temperature in the omnivorous leafroller moth, Platynota stultana (Lepidoptera: Tortricidae) and other moths: a hypothesis. Ann Entomol Soc Am 81:138–151. https://doi.org/10.1093/aesa/81.1.138
Webster RP, Cardé RT (1982) Relationships among pheromone titre, calling and age in the omnivorous leafroller moth (Platynota stultana). J Insect Physiol 28:925–933. https://doi.org/10.1016/0022-1910(82)90108-1
Xiang YY, Yang MF, Li ZZ (2010) Calling behavior and rhythms of sex pheromone production in the black cutworm moth in China. J Insect Behav 23:35–44. https://doi.org/10.1007/s10905-009-9193-0
Acknowledgements
The authors would like to thank Pedro Zaldaña Morales for allowing the development of this research at his Buena Vista Farm (San Marcos, Guatemala) and Julio C. Rojas for his suggestions on an earlier draft of the manuscript.
Funding
Funding for this work was provided by Consejo Nacional de Ciencia y Tecnología (CONACYT) through a scholarship granted to Rutver Aranda-Arguello for his doctoral studies (CVU: 641600).
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All authors contributed to the study conception and design. Rutver Aranda-Arguello conducted experiments and wrote first draft of the manuscript. Leopoldo Cruz-López reviewed chemical analysis and examined field data. Leopoldo Cruz-López, Edi A. Malo, and Guillermo López-Guillén reviewed and improved the manuscript. All authors read and approved the manuscript.
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Aranda-Arguello, R., Malo, E.A., López-Guillén, G. et al. Gymnandrosoma aurantianum (Lepidoptera: Tortricidae): Calling Rhythm and Effect of Age on Female Sex Pheromone Titer and Male Antennal Responses. Neotrop Entomol 53, 75–82 (2024). https://doi.org/10.1007/s13744-023-01101-w
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DOI: https://doi.org/10.1007/s13744-023-01101-w