Abstract
Lateralization is a fundamental principle of the brain organization widespread among vertebrates but rather unknown in invertebrates. Evidences of lateralized courtship and mating behavioral traits in parasitic wasps are extremely rare. Here, courtship and mating sequences and the presence of mating lateralization in Anagyrus sp. near pseudococci, one of the most effective biological control agents of mealybugs, were investigated. Courtship and mating behavior in A. sp. near pseudococci consisted in the male chasing of the female, pre-copula, copula, and post-copula phases. Males mating success was not related to the duration of chasing and pre-copula. High-speed videos showed population-level lateralization in A. sp. near pseudococci during courtship. Most the wasps used the right antenna to start antennal tapping and this led to a higher mating success, although lateralization had no impact on the frequency of the antennal tapping. Both females and males displayed this behavior. Higher mating success was detected when females displayed antennal tapping during sexual interaction, though male tapping was performed with a slightly higher frequency. To the best of our knowledge, this report on behavioral asymmetries of mating traits in A. sp. near pseudococci represents a quite rare evidence of lateralized behavior in parasitic wasps of economic importance. Our findings add basic knowledge on the behavioral ecology of this biocontrol agent with potential implications on the optimization of mass-rearing procedures aimed at using this parasitoid in Integrated Pest Management.
Similar content being viewed by others
References
Ades C, Ramires EN (2002) Asymmetry of leg use during prey handling in the spider Scytodes globula (Scytodidae). J Insect Behav 15:563–570. doi:10.1023/A:1016337418472
Anfora G, Frasnelli E, Maccagnani B, Rogers LJ, Vallortigara G (2010) Behavioural and electrophysiological lateralization in a social (Apis mellifera) but not in a non-social (Osmia cornuta) species of bee. Behav Brain Res 206:236–239. doi:10.1016/j.bbr.2009.09.023
Backwell PRY, Matsumasa M, Double M, Roberts A, Murai M, Keogh JS, Jennions MD (2007) What are the consequences of being left-clawed in a predominantly right-clawed fiddler crab? Proc R Soc B Biol Sci 274:2723–2729. doi:10.1098/rspb.2007.0666
Benelli G, Canale A (2012) Learning of visual cues in the fruit fly parasitoid Psyttalia concolor (Szépligeti) (Hymenoptera: Braconidae). Biocontrol 57:767–777. doi:10.1007/s10526-012-9456-0
Benelli G, Romano D (2017) Does indirect mating trophallaxis boost male mating success and female egg load in Mediterranean fruit flies? J Pest Sci. doi:10.1007/s10340-017-0854-z
Benelli G, Canale A, Bonsignori G, Ragni G, Stefanini C, Raspi A (2012) Male wing vibration in the mating behavior of the olive fruit fly Bactrocera oleae (Rossi) (Diptera: Tephritidae). J Insect Behav 25:590–603. doi:10.1007/s10905-012-9325-9
Benelli G, Donati E, Romano D, Stefanini C, Messing RH, Canale A (2015a) Lateralization of aggressive displays in a tephritid fly. Sci Nat Naturwiss 102(1–2):1–9. doi:10.1007/s00114-014-1251-6
Benelli G, Romano D, Messing RH, Canale A (2015b) First report of behavioural lateralisation in mosquitoes: right-biased kicking behaviour against males in females of the Asian tiger mosquito, Aedes albopictus. Parasitol Res 114:1613–1617. doi:10.1007/s00436-015-4351-0
Benelli G, Romano D, Messing RH, Canale A (2015c) Population-level lateralized aggressive and courtship displays make better fighters not lovers: evidence from a fly. Behav Process 115:163–168. doi:10.1016/j.beproc.2015.04.005
Benelli G, Romano D, Stefanini C, Kavalieratos NG, Athanassiou CG, Canale A (2017a) Asymmetry of mating behaviour affects copulation success in two stored product beetles. J Pest Sci. doi:10.1007/s10340-016-0794-z
Benelli G, Romano D, Kavallieratos N, Conte G, Stefanini C, Mele M, Athanassiou C, Canale A (2017b) Multiple behavioural asymmetries impact male mating success in the khapra beetle, Trogoderma granarium. J Pest Sci 90:901–909. doi:10.1007/s10340-017-0832-5
Bisazza A, Sovrano VA, Vallortigara G (2001) Consistency among different tasks of left–right asymmetries in lines of fish originally selected for opposite direction of lateralization in a detour task. Neuropsychologia 39:1077–1085. doi:10.1016/S0028-3932(01)00034-3
Briscoe AD, Chittka L (2001) The evolution of colour vision in insects. Annu Rev Entomol 46:471–510. doi:10.1146/annurev.ento.46.1.471
Bugila AA, Branco M, Silva EBD, Franco JC (2014) Host selection behaviour and specificity of the solitary parasitoid of mealybugs Anagyrus sp. nr. pseudococci (Girault)(Hymenoptera, Encyrtidae). Biocontrol Sci Technol 24(1):22–38
Cohen J (1960) A coefficient of agreement for nominal scales. Educ Psychol Meas 20:37–46
Daane KM, Almeida RPP, Bell VA, Walker JTS, Botton M, Fallahzadeh M, Mani M, Miano LL, Sforza R, Walton VM, Zaviezo T (2012) Biology and management of mealybugs in vineyards. In: Bostanian NJ, Vincent C, Isaacs R (eds) Arthropod management in vineyards. Springer, Dordrecht, pp 271–307. doi:10.1007/978-94-007-4032-7_12
Fortuna TM, Franco JC, Rebelo MT (2015) Morphology and distribution of antennal sensilla in a mealybug parasitoid, Anagyrus sp. near pseudococci (Hymenoptera, Encyrtidae). Microsc Microanal 21(S6):8–9
Franco JC, Silva EB, Cortegano E, Campos L, Branco M, Zada A, Mendel Z (2008) Kairomonal response of the parasitoid Anagyrus spec. nov. near pseudococci to the sex pheromone of the vine mealybug. Entomol Exp Appl 126(2):122–130
Frasnelli E, Iakovlev I, Reznikova Z (2012) Asymmetry in antennal contacts during trophallaxis in ants. Behav Brain Res 232(1):7–12
Ghirlanda S, Vallortigara G (2004) The evolution of brain lateralization: a game theoretical analysis of population structure. Proc R Soc B Biol Sci 271:853–857
Ghirlanda S, Frasnelli E, Vallortigara G (2009) Intraspecific competition and coordination in the evolution of lateralization. Philos Trans R Soc Lond B 364:861–866
Giunti G, Canale A, Messing RH, Donati E, Stefanini C, Michaud JP, Benelli G (2015) Parasitoid learning: current knowledge and implications for biological control. Biol Control 90:208–219
Güleç G, Kilinçer AN, Kaydan MB, Ülgentürk S (2007) Some biological interactions between the parasitoid Anagyrus pseudococci (Girault) (Hymenoptera: Encyrtidae) and its host Planococcus ficus (Signoret) (Hemiptera: Coccoidea: Pseudococcidae). J Pest Sci 80(1):43–49
Gwet KL (2014) Handbook of inter-rater reliability: The definitive guide to measuring the extent of agreement among raters. Advanced Analytics LLC, Stataxis Publishing Company, Gaithersburg
Hädicke CW, Ernst A, Sombke A (2016) Sensing more than the bathroom: sensilla on the antennae, cerci and styli of the silverfish Lepisma saccharina Linneaus, 1758 (Zygentoma: Lepismatidae). Entomol Gen 36:71–89
Heidari M, Jahan M (2010) A study of ovipositional behaviour of Anagyrus pseudococci a parasitoid of mealybugs. J Agr Sci 2:49–53
Kamimura Y (2006) Right-handed penises of the earwig Labidura riparia (Insecta, Dermaptera, Labiduridae): evolutionary relationships between structural and behavioral asymmetries. J Morphol 267:1381–1389
Rigosi E, Haase A, Rath L, Anfora G, Vallortigara G, Szyszka P (2015) Asymmetric neural coding revealed by in vivo calcium imaging in the honey bee brain. Proc R Soc Lond B Biol Sci 282(1803):20142571
Rogers LJ, Vallortigara G (2008) From antenna to antenna: lateral shift of olfactory memory in honeybees. PLoS ONE 3(6):e2340. doi:10.1371/journal.pone.0002340
Rogers LJ, Vallortigara G (2015) When and why did brains break symmetry? Symmetry 7:2181–2194
Rogers LJ, Vallortigara G, Andrew RJ (2013a) Divided brains: The biology and behaviour of brain asymmetries. Cambridge University Press, Cambridge
Rogers LJ, Rigosi E, Frasnelli E, Vallortigara G (2013b) A right antenna for social behaviour in honeybees. Sci Rep 3:2045. doi:10.1038/srep02045
Rogers LJ, Frasnelli E, Versace E (2016) Lateralized antennal control of aggression and sex differences in red mason bees, Osmia bicornis. Sci Rep 6:29411
Romano D, Canale A, Benelli G (2015) Do right-biased boxers do it better? Population-level asymmetry of aggressive displays enhances fighting success in blowflies. Behav Process 113:159–162
Romano D, Kavallieratos NG, Athanassiou CG, Stefanini C, Canale A, Benelli G (2016a) Impact of geographical origin and rearing medium on mating success and lateralization in the rice weevil, Sitophilus oryzae (L.) (Coleoptera: Curculionidae). J Stored Prod Res 69:106–112
Romano D, Donati E, Canale A, Messing RH, Benelli G, Stefanini C (2016b) Lateralized courtship in a parasitic wasp. Laterality 21(3):243–254
Sokal RK, Rohlf FJ (1981) Biometry. Freeman and Company, New York
Suma P, Mansour R, La Torre I, Ali Bugila AA, Mendel Z, Franco JC (2012) Developmental time, longevity, reproductive capacity and sex ratio of the mealybug parasitoid Anagyrus sp. nr. pseudococci (Girault) (Hymenoptera: Encyrtidae). Biocontrol Sci Technol 22(7):737–745
Tingle CCD, Copland MJW (1989) Progeny production and adult longevity of the mealybug parasitoids Anagyrus pseudococci, Leptomastix dactylopii, and Leptomastidea abnormis [Hym.: Encyrtidae] in relation to temperature. Entomophaga 34(1):111–120
Triapitsyn SV, Gonzàlez D, Vickerman DB, Noyes JS, White EB (2007) Morphological, biological, and molecular comparisons among the different geographical populations of Anagyrus pseudococci (Hymenoptera: Encyrtidae), parasitoids of Planococcus spp. (Hemiptera: Pseudococcidae), with notes on Anagyrus dactylopii. Biol Control 41:14–24
Vallortigara G (2000) Comparative neuropsychology of the dual brain: a stroll through animals’ left and right perceptual worlds. Brain Lang 73(2):189–219
Vallortigara G (2006) The evolutionary psychology of left and right: costs and benefits of lateralization. Dev Psychobiol 48(6):418–427
Vallortigara G, Rogers LJ (2005) Survival with an asymmetrical brain: advantages and disadvantages of cerebral lateralization. Behav Brain Sci 28:575–633
Vallortigara G, Versace E (2017) Laterality at the neural, cognitive, and behavioral levels. In: Call J (ed) APA handbook of comparative psychology: vol. 1. basic concepts, methods, neural substrate, and behavior. American Psychological Association, Washington DC, pp 557–577
Vallortigara G, Chiandetti C, Sovrano VA (2011) Brain asymmetry (animal). Wiley Interdiscip Rev Cogn Sci 2:146–157. doi:10.1002/wcs.100
Versace E, Vallortigara G (2015) Forelimb preferences in human beings and other species: multiple models for testing hypotheses on lateralization. Front Psychol 6:233. doi:10.3389/fpsyg.2015.00233
Acknowledgements
We are grateful to Andrea Sala (BioPlanet, Cesena, Italy) for providing the mass-reared parasitoids tested in this study. We would like to thank Alice Bono for her kind assistance during high-speed video recordings. Giovanni Benelli is funded by BIOCONVITO P.I.F. “Artigiani del Vino Toscano” (Regione Toscana, Italy). This study was partially supported by the H2020 Project “Submarine cultures perform long-term robotic exploration of unconventional environmental niches” (subCULTron) [640967FP7]. Funders had no role in the study design, data collection and analysis, decision to publish or preparation of the manuscript.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflicts of interest.
Ethical standards
All applicable international and national guidelines for the care and use of animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted.
Additional information
Communicated by M. Traugott.
Rights and permissions
About this article
Cite this article
Romano, D., Benelli, G., Stefanini, C. et al. Behavioral asymmetries in the mealybug parasitoid Anagyrus sp. near pseudococci: does lateralized antennal tapping predict male mating success?. J Pest Sci 91, 341–349 (2018). https://doi.org/10.1007/s10340-017-0903-7
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10340-017-0903-7