Hostname: page-component-78c5997874-lj6df Total loading time: 0 Render date: 2024-11-10T16:47:21.709Z Has data issue: false hasContentIssue false
  • English
  • Français

Effect of fruit and host fly species on the associative learning by Fopius arisanus

Published online by Cambridge University Press:  26 February 2019

A. Monsia ,
G.S.B. Mègnigbèto ,
D. Gnanvossou  and
M.F. Karlsson Open the ORCID record for M.F. Karlsson [Opens in a new window]
A. Monsia
Affiliation:
Department of Zoology, University of Abomey-Calavi (UAC), BP 215, Godomey, Benin International Institute of Tropical Agriculture (IITA), 08 BP 0932 Tri Postal, Cotonou, Benin
G.S.B. Mègnigbèto
Affiliation:
International Chair in Mathematical Physics and Applications (ICMPA) (CIPMA-Chaire UNESCO), University of Abomey-Calavi (UAC), 03 BP 2819, Cotonou
D. Gnanvossou
Affiliation:
International Institute of Tropical Agriculture (IITA), 08 BP 0932 Tri Postal, Cotonou, Benin
M.F. Karlsson*
Affiliation:
International Institute of Tropical Agriculture (IITA), 08 BP 0932 Tri Postal, Cotonou, Benin Department of Plant Protection Biology, Swedish University of Agricultural Sciences (SLU), SE-230 53 Alnarp, Sweden
*
*Author for correspondence Phone: +229 21350188 ext 470 Fax: +229 21350556 E-mail: Miriam.Karlsson@slu.se
Get access Rights & Permissions [Opens in a new window]

Abstract

Parasitoids, released in augmentative biological control programmes, which display a rapid host-location capacity, have a higher likelihood of successfully controlling target pest species. By learning to associate sensory cues to a suitable oviposition site, might parasitoids used as biological control agents, locate hosts more rapidly, and perhaps increase the efficacity of e.g. Tephritidae fruit fly management. We studied associative learning of Fopius arisanus (Hymenoptera: Braconidae) and tested its range of learning in natural and conditional hosts and host fruits, i.e. Bactrocera dorsalis, Zeugodacus cucurbitae, Ceratitis capitata and Ceratitis cosyra (Diptera: Tephritidae) and on fruits (papaya, tomato, banana). Naïve female F. arisanus were compared with experienced wasps, which had been offered infested and non-infested fruit, and been allowed to oviposit. Preferences for olfactory cues from infested fruits were thereafter assessed in a two-choice olfactometer. Naïve and trained parasitoids preference differed in general and non-responders to infested fruits were higher among naïve parasitoids. The trained wasps preferred the fruit infested in the training more than the control fruit, for all combination, except when C. cosyra infested the fruits, hence avoidance behavioural response was observed towards the odour of the infested fruit. Fopius arisanus was capable of behaviourally respond to the learned information, e.g. associative odour learning was achieved, yet limited depending on interaction level, fruit fly and fruit combination. To create F. arisanus preference of an associated odour, it might hence be needed to ensure oviposition in perceived suitable host and host fruit, for the parasitoid learning to become favourable in a biological control setup.

Keywords

BraconidaeTephritidaepreferencebehaviourconditioning
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 109 , Issue 5 , October 2019 , pp. 649 - 658
Check for updates
Copyright
Copyright © Cambridge University Press 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Altuzar, A., Montoya, P. & Rojas, J.C. (2004) Response of Fopius arisanus (Hymenoptera: Braconidae) to fruit volatiles in a wind tunnel. Florida Entomologist 87, 616–618.Google Scholar
Aluja, M., Sivinski, J., Ovruski, S., Guillén, L., López, M., Cancino, J., Torres-Anaya, A., Gallegos-Chan, G. & Ruíz, L. (2009) Colonization and domestication of seven species of native New World hymenopterous larval-prepupal and pupal fruit fly (Diptera: Tephritidae) parasitoids. Biocontrol Science and Technology 19, 49–79.Google Scholar
Ayelo, P.M., Sinzogan, A.C., Bokonon-Ganta, A.H. & Karlsson, M.F. (2017) Host species and vegetable fruit suitability and preference by the parasitoid wasp Fopius arisanus. Entomologia Experimentalis et Applicata 163, 70–81.Google Scholar
Bautista, R.C., Harris, E.J., Vargas, R.I. & Jang, E.B. (2004) Parasitization of melon fly (Diptera: Tephritidae) by Fopius arisanus and Psyttalia fletcheri (Hymenoptera: Braconidae) and the effect of fruit substrates on host preference by parasitoids. Biological Control 30, 156–164.Google Scholar
Benelli, G. & Canale, A. (2012) Learning of visual cues in the fruit fly parasitoid Psyttalia concolor (Szpligeti) (Hymenoptera: Braconidae). BioControl 57, 767–777.Google Scholar
Benelli, G., Stefanini, C., Giunti, G., Geri, S., Messing, R.H. & Canale, A. (2014) Associative learning for danger avoidance nullifies innate positive chemotaxis to host olfactory stimuli in a parasitic wasp. Naturwissenschaften 101, 753–757.Google Scholar
Canale, A., Geri, S. & Benelli, G. (2014) Associative learning for host-induced fruit volatiles in Psyttalia concolor (Hymenoptera: Braconidae), a koinobiont parasitoid of tephritid flies. Bulletin of Entomological Research 104, 774–780.Google Scholar
Carmichael, A.E., Wharton, R.A. & Clarke, A.R. (2005) Opiine parasitoids (Hymenoptera: Braconidae) of tropical fruit flies (Diptera: Tephritidae) of the Australian and South Pacific region. Bulletin of Entomological Research 95, 545–569.Google Scholar
Carrasco, M., Montoya, P., Cruz-Lopez, L. & Rojas, J.C. (2005) Response of the Fruit Fly Parasitoid Diachasmimorpha longicaudata (Hymenoptera: Braconidae) to mango fruit volatiles. Environmental Entomology 34, 576–583.Google Scholar
Chinajariyawong, A., Clarke, A.R., Jirasurat, M., Kritsaneepiboon, S., Lahey, H.A., Vijaysegaran, S. & Waiter, G.H. (2000) Survey of opiine parasitoids of fruit flies (Diptera: Tephritidae) in Thailand and Malaysia. The Raffles Bulletin of Zoology 48, 71–101.Google Scholar
Costa, A., Ricard, I., Davison, A.C. & Turlings, T.C.J. (2010) Effects of rewarding and unrewarding experiences on the response to host-induced plant odors of the generalist parasitoid Cotesia marginiventris (Hymenoptera: Braconidae). Journal of Insect Behavior 23, 303–318.Google Scholar
De Meyer, M., Delatte, H., Mwatawala, M., Quilici, S., Vayssieres, J.-F. & Virgilio, M. (2015) A review of the current knowledge on Zeugodacus cucurbitae (Coquillett) (Diptera, Tephritidae) in Africa, with a list of species included in Zeugodacus. ZooKeys 540, 539–557.Google Scholar
De Rijk, M., Cegarra Sánchez, V., Smid, H.M., Engel, B., Vet, L.E.M. & Poelman, E.H. (2018) Associative learning of host presence in non-host environments influences parasitoid foraging: associative learning in parasitoid foraging. Ecological Entomology 43, 318–325.Google Scholar
Desouhant, E., Navel, S., Foubert, E., Fischbein, D., Théry, M. & Bernstein, C. (2010) What matters in the associative learning of visual cues in foraging parasitoid wasps: colour or brightness? Animal Cognition 13, 535–543.Google Scholar
Dukas, R. (2008) Evolutionary biology of insect learning. Annual Review of Entomology 53, 145–160.Google Scholar
Dukas, R. & Duan, J.J. (2000) Potential fitness consequences of associative learning in a parasitoid wasp. Behavioral Ecology 11, 536–543.Google Scholar
Ekesi, S., De Meyer, M., Mohamed, S.A., Virgilio, M. & Borgemeister, C. (2016) Taxonomy, ecology, and management of native and exotic fruit fly species in Africa. Annual Review of Entomology 61, 219–238.Google Scholar
Ero, M.M. & Clarke, A.R. (2012) Host location by the fruit fly parasitoid Diachasmimorpha krausii: role of fruit fly species, life stage and host plant. Agricultural and Forest Entomology 14, 101–110.Google Scholar
García-Medel, D., Sivinski, J., Díaz-Fleischer, F., Ramirez-Romero, R. & Aluja, M. (2007) Foraging behavior by six fruit fly parasitoids (Hymenoptera: Braconidae) released as single- or multiple-species cohorts in field cages: influence of fruit location and host density. Biological Control 43, 12–22.Google Scholar
Giunti, G., Canale, A., Messing, R.H., Donati, E., Stefanini, C., Michaud, J.P. & Benelli, G. (2015) Parasitoid learning: current knowledge and implications for biological control. Biological Control 90, 208–219.Google Scholar
Giunti, G., Benelli, G., Flamini, G., Michaud, J.P. & Canale, A. (2016) Innate and learned responses of the tephritid parasitoid Psyttalia concolor (Hymenoptera: Braconidae) to olive volatiles induced by Bactrocera oleae (Diptera: Tephritidae) infestation. Journal of Economic Entomology 0, 1–9.Google Scholar
Gnanvossou, D., Hanna, R., Bokonon-Ganta, A.H., Ekesi, S. & Mohamed, S.A. (2016) Release, establishment and spread of the natural enemy Fopius arisanus (Hymenoptera: Braconidae) for control of the invasive oriental fruit fly Bactrocera dorsalis (Diptera: Tephritidae) in Benin, West Africa. pp. 575–600 in Ekesi, S., Mohamed, S.A. & DeMeyer, M. (Eds) Fruit fly Research and Development in Africa – Towards A Sustainable Management Strategy to Improve horticulture. Switzerland, Springer.Google Scholar
Gonçalves, R.S., Manoukis, N.C. & Nava, D.E. (2017) Effect of Fopius arisanus oviposition experience on parasitization of Bactrocera dorsalis. BioControl 62, 595–602.Google Scholar
Hagen, K. (1953) A premating period in certain species of the genus Opius (hymenoptera: Braconidae). Proceedings of the Hawaiian Entomological Society 15, 115–116.Google Scholar
Harris, E.J. & Bautista, R.C. (1996) Effects of fruit fly host, fruit species, and host egg to female parasitoid ratio on the laboratory rearing of Biosteres arisanus. Entomologia Experimentalis et Applicata 79, 187–194.Google Scholar
Harris, E., Bautista, R., Vargas, R.I. & Jang, E. (2007) Rearing Fopius arisanus (Sonan) (Hymenoptera: Braconidae) in Mediterranean fruit fly (Diptera: Tephritidae). Proceedings of the Hawaiian Entomological Society 39, 121–126.Google Scholar
Harris, C.M., Ruberson, J.R., Meagher, R. & Tumlinson, J.H. (2012) Host suitability affects odor association in Cotesia marginiventris: implications in generalist parasitoid host-finding. Journal of Chemical Ecology 38, 340–347.Google Scholar
Kambura, C.W. (2016) Diversity and host preference of tephritid fruit fly species infesting cucurbit and major horticultural crops in costal Kenya. MSc Thesis, University of Nairobi, p. 97.Google Scholar
Kroder, S. & Messing, R.H. (2010) A new parasitoid from Kenya, Fopius ceratitivorus, complements the extant parasitoid guild attacking Mediterranean fruit fly in Hawaii. Biological Control 53, 223–229.Google Scholar
Lewis, W.J. & Takasu, K. (1990) Use of learned odours by a parasitic wasp in accordance with host and food needs. Nature 348, 635–636.Google Scholar
Li, X. & Lui, S.S. (2003) Learning in host foraging the parasitoid Diadegma semiclausum (Hymenoptera: Ichneumonidae). Acta Entomologica Sinica 46, 749–754.Google Scholar
Liquido, N.J.N. (1991) Effect of ripeness and location of papaya fruit on the parasitization rates of oriental fruit flies and melon fruit (Diptera: Tephritidae) by braconid (Hymenoptera) parasitoid. Environmental Entomology 20, 1732–1736.Google Scholar
Liquido, N.J., Cunningham, R.T. & Nakagawa, S. (1990) Host Plants of Mediterranean fruit fly (Diptera: Tephritidae) on the Island of Hawaii (1949–1985 Survey). Journal of Economic Entomology 83, 1863–1878.Google Scholar
Liquido, N., McQuate, G., Kurashima, R., Hanlin, M., Birnbaum, A. & Marnell, S. (2015) Provisional list of suitable host plants of Oriental fruit fly, Bactrocera dorsalis (Hendel) (Diptera: Tephritidae), USDA Animal and Plant Health Inspection Services, p. 47.Google Scholar
Lucchetta, P., Bernstein, C., Théry, M., Lazzari, C. & Desouhant, E. (2008) Foraging and associative learning of visual signals in a parasitic wasp. Animal Cognition 11, 525–533.Google Scholar
Masry, A., Clarke, A.R. & Cunningham, J.P. (2018) Learning influences host versus nonhost discrimination and postalighting searching behavior in the Tephritid Fruit Fly Parasitoid Diachasmimorpha kraussii (Hymenoptera: Braconidae). Journal of Economic Entomology 111, 787–794.Google Scholar
Mcquate, G.T., Liquido, N.J. & Nakamichi, K.A.A. (2017) Annotated world bibliography of host plants of the melon fly Bactrocera cucurbitae (Coquillett) (Diptera: Tephritidae). Insecta Mundi 527, 1–339.Google Scholar
Minoli, S., Kauer, I., Colson, V., Party, V., Renou, M., Anderson, P., Gadenne, C., Marion-Poll, F. & Anton, S. (2012) Brief exposure to sensory cues elicits stimulus-nonspecific general sensitization in an insect. PLoS ONE 7, e34141.Google Scholar
Mohamed, S.A., Ekesi, S. & Hanna, R. (2010) Old and new host-parasitoid associations: parasitism of the invasive fruit fly Bactrocera invadens (Diptera: Tephritidae) and five African fruit fly species by Fopius arisanus, an Asian opiine parasitoid. Biocontrol Science and Technology 20, 183–196.Google Scholar
Montoya, P., Liedo, P., Benrey, B., Cancino, J., Barrera, J.F., Sivinski, J. & Aluja, M. (2000) Biological control of Anastrepha spp. (Diptera: Tephritidae) in mango orchards through augmentative releases of Diachasmimorpha longicaudata (Ashmead) (Hymenoptera: Braconidae). Biological Control 18, 216–224.Google Scholar
Müller, C., Collatz, J., Wieland, R. & Steidle, J.L.M. (2006) Associative learning and memory duration in the parasitic wasp Lariophagus distinguendus. Animal Biology 56, 221–232.Google Scholar
Ndiaye, O., Ndiaye, S., Djiba, S., Ba, C.T., Vaughan, L., Rey, J.-Y. & Vayssieres, J.-F. (2015) Preliminary surveys after release of the fruit fly parasitoid Fopius arisanus Sonan (Hymenoptera Braconidae) in mango production systems in Casamance (Senegal). Fruits 70, 91–99.Google Scholar
Ngumbi, E., Jordan, M. & Fadamiro, H. (2012) Comparison of associative learning of host-related plant volatiles in two parasitoids with different degrees of host specificity, Cotesia marginiventris and Microplitis croceipes. Chemoecology 22, 207–215.Google Scholar
Nishida, T. & Haramoto, F. (1953) Immunity of Dacus cucurbitae to attack by certain parasites of Dacus dorsalis. Journal of Economic Entomology 46, 61–64.Google Scholar
Papaj, D.R. & Vet, L.E.M. (1990) Odor learning and foraging success in the parasitoid, Leptopilina heterotoma. Journal of Chemical Ecology 16, 3137–3150.Google Scholar
Quilici, S. & Rousse, P. (2012) Location of host and host habitat by fruit fly parasitoids. Insects 3, 1220–1235.Google Scholar
Quimio, G.M. & Walter, G.H. (2001) Host preference and host suitability in an egg-pupal fruit fly parasitoid, Fopius arisanus (Sonan) (Hym., Braconidae). Journal of Applied Entomology 125, 135–140.Google Scholar
Raine, N.E. & Chittka, L. (2008) The correlation of learning speed and natural foraging success in bumble-bees. Proceedings of the Royal Society B 275, 803–808.Google Scholar
Ramadan, M.M., Wong, T. & Beardsley, J. (1992) Reproductive behavior of Biosteres arisanus (Sonan) (Hymenoptera: Braconidae), an egg-larval parasitoid of the oriental fruit fly. Biological Control 2, 28–34.Google Scholar
R Development Core Team. (2009) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. <http://www.R-projec.t.org>>Google Scholar
Rendon, P., Sivinski, J., Holler, T., Bloem, K., Lopez, M., Martinez, A. & Aluja, M. (2006) The effects of sterile males and two braconid parasitoids, Fopius arisanus (Sonan) and Diachasmimorpha krausii (Fullaway) (Hymenoptera), on caged populations of Mediterranean fruit flies, Ceratitis capitata (Wied.) (Diptera: Tephritidae) at various sites. Biological Control 36, 224–231.Google Scholar
Rousse, P., Gourdon, F. & Quilici, S. (2006) Host specificity of the egg pupal parasitoid Fopius arisanus (Hymenoptera: Braconidae) in La Réunion. Biological Control 37, 284–290.Google Scholar
Rousse, P., Chiroleu, F., Veslot, J. & Quilici, S. (2007) The host- and microhabitat olfactory location by Fopius arisanus suggests a broad potential host range. Physiological Entomology 32, 313–321.Google Scholar
Segura, D.F., Viscarret, M.M., Carabajal Paladino, L.Z., Ovruski, S.M. & Cladera, J.L. (2007) Role of visual information and learning in habitat selection by a generalist parasitoid foraging for concealed hosts. Animal Behaviour 74, 131–142.Google Scholar
Segura, D.F., Nussenbaum, A.L., Viscarret, M.M., Devescovi, F., Bachmann, G.E., Corley, J.C., Ovruski, S.M. & Cladera, J.L. (2016) Innate host habitat preference in the parasitoid Diachasmimorpha longicaudata: functional significance and modifications through learning. PLoS ONE 11, 1–18.Google Scholar
Seino, H. & Kainoh, Y. (2008) Associative learning and discrimination of 10 plant species by the egg-larval parasitoid, Ascogaster reticulata Watanabe (Hymenoptera: Braconidae). Applied Entomology and Zoology 43, 83–90.Google Scholar
Sime, K.R., Daane, K.M., Wang, X.G., Johnson, M.W. & Messing, R.H. (2008) Evaluation of Fopius arisanus as a biological control agent for the olive fruit fly in California. Agricultural and Forest Entomology 10, 423–431.Google Scholar
Sivinski, J. & Aluja, M. (2012) The roles of parasitoid foraging for hosts, food and mates in the augmentative control of tephritidae. Insects 3, 668–691.Google Scholar
Sivinski, J.M., Calkins, C.O., Baranowski, R., Harris, D., Brambila, J., Diaz, J., Burns, R.E., Holler, T. & Dodson, G. (1996) Suppression of a Caribbean Fruit Fly (Anastrepha suspensa (Loew) Diptera: Tephritidae) population through augmented releases of the parasitoid Diachasmimorpha longicaudata (Ashmead) (Hymenoptera: Braconidae). Biological Control 6, 177–185.Google Scholar
Steck, G.J. (2015) Mango fruit fly, Ceratitis cosyra (Walker) (Insecta: Diptera: Tephritidae). pp. 1–3 in Gillett-Kaufman, J.L. (Ed.) Entomology and Nematology Department. Gainesville, UF/ IFAS Extension, University of Florida, EENY286.Google Scholar
Steidle, J.L.M. & Van Loon, J.J.A. (2003) Dietary specialization and infochemical use in carnivorous arthropods: testing a concept. Entomologia Experimentalis Et Applicata 108, 133–148.Google Scholar
Takasu, K. & Lewis, W.J.J. (1996) The role of learning in adult food location by the larval parasitoid, Microplitis croceipes (Hymenoptera: Braconidae). Journal of Insect Behavior 9, 265–281.Google Scholar
Takasu, K. & Lewis, W.J. (2003) Learning of host searching cues by the larval parasitoid Microplitis croceipes. Entomologia Experimentalis et Applicata 108, 77–86.Google Scholar
Thiel, A. & Hoffmeister, T.S. (2009) Decision-making dynamics in Parasitoids of Drosophila. pp. 45–66 in Prévost, G. (Ed.) Advances in Parasitology, Vol. 70. Burlington, Academic Press, Elevier Ltd.Google Scholar
Turlings, T.C.J., Wäckers, F.L., Vet, L.E.M., Lewis Joseph, W. & Tumlinson, J.H. (1993) Learning of host-finding cues by hymenopterous parasitoids. pp. 51–78 in Papaj, D.R. & Lewis, A.C. (Eds) Insect Learning. US, Springer.Google Scholar
Vargas, R.I., Long, J., Miller, N.W., Delate, K., Jackson, C.G., Uchida, G.K., Bautista, R.C. & Harris, E.J. (2004) Releases of Psyttalia fletcheri (Hymenoptera: Braconidae) and sterile flies to suppress melon fly (Diptera: Tephritidae) in Hawaii. Journal of Economic Entomology 97, 1531–1539.Google Scholar
Vargas, R.I., Leblanc, L., Putoa, R. & Eitam, A. (2007) Impact of Introduction of Bactrocera dorsalis (Diptera: Tephritidae) and classical biological control releases of Fopius arisanus (Hymenoptera: Braconidae) on economically important fruit flies in French Polynesia. Journal of Economic Entomology 100, 670–679.Google Scholar
Vargas, R.I., Piñero, J.C., Mau, R.F.L., Jang, E.B., Klungness, L.M., McInnis, D.O., Harris, E.B., McQuate, G.T., Bautista, R.C. & Wong, L. (2010) Area-wide suppression of the Mediterranean fruit fly, Ceratitis capitata, and the oriental fruit fly, Bactrocera dorsalis, in Kamuela, Hawaii. Journal of Insect Science 10, 1–17.Google Scholar
Vargas, R.I., Leblanc, L., Harris, E.J. & Manoukis, N.C. (2012) Regional suppression of Bactrocera fruit flies (Diptera: Tephritidae) in the Pacific through biological control and prospects for future introductions into other areas of the world. Insects 3, 727–742.Google Scholar
Wei, K., Tang, Y.L., Wang, X.Y., Yang, Z.Q., Cao, L.M., Lu, J.F., Liu, E.S. & Liu, G.J. (2013) Effects of learning experience on behaviour of the generalist parasitoid Sclerodermus pupariae to novel hosts. Journal of Applied Entomology 137, 469–475.Google Scholar