Allies in nature

Jean-François Vayssières (j.vayssières@cgiar.org), Appolinaire Adandonon (adanappo@yahoo.fr), Antonio Sinzogan (a.sinzogan@cgiar.org), and Paul van Mele (p.vanmele@cgiar.org)

<em srcset=Bactrocera invadens adults on a mango” width=”250″ height=”188″ />
Bactrocera invadens adults on a mango

Biocontrol has been around for over 2000 years. The most ancient example of biocontrol use recorded was that of Chinese and Southeast Asian fruit growers, who used weaver ants to protect their citrus crops. Farmers in Asia continue to practice this until today.

Weaver ants (one colony of Oecophylla = several nests) live on trees and defend their territories using chemicals or “pheromones” that they leave on leaves, branches, and fruit. Pheromones are chemicals secreted by insects that strongly influence, in the case of ants, the behavior of others of the same species. The release of these pheromones, which is a form of nonverbal communication, can effectively recruit ants to new food sources or trigger warnings as a protection against intruders.

There are two Oecophylla (Hymenoptera Formicidae) species in the world—the Asian species, Oecophylla smaragdina Fabricius, and the African species, O. longinoda Latreille.

Their successful application as an endemic natural enemy is rising in tropical countries. New research started exploring the mechanisms underlying ant protection of plants against arthropods. Apart from direct control mechanisms, including the predation on or deterrence of insect pests during direct encounters, indirect mechanisms have recently been discovered involving the detection of the territories of enemy ants.

Researchers have demonstrated that the Asian Oecophylla species can deter insect herbivores or plant eaters through info-chemical action. A laboratory test showed that a beetle which this ant preys on was more reluctant to feed on leaves sampled within ant territories than on leaves sampled outside.

In Africa, O. longinoda is being used as a biocontrol agent against agricultural pests. This species defends chemically marked territories at both levels, the intraspecific (within species) and interspecific (between species). Due to their pronounced territoriality, permanent surveillance (all year round, day and night), and very efficient recruitment, O. longinoda respond quickly to any increase in prey numbers.

Nest of <em srcset=O. longinoda on a mango tree” width=”250″ height=”188″ />
Nest of O. longinoda on a mango tree

The use of O. longinoda colonies is suitable for perennial cropping systems in sub-Saharan Africa because they are efficient against fruit fly pests, one of the widespread threats, constantly present in tropical agricultural systems.

Two fruit fly (Diptera Tephritidae) species—Bactrocera invadens Drew Tsuruta & White and Ceratitis cosyra (Walker), were found to be the most important species in terms of fly abundance and fruit damage in Bénin during the 2005 and 2006 seasons. The first is an exotic species from Asia, only recently recorded in West Africa, where it has become a huge threat in main fruit crops, such as mango (Mangifera indica) and citrus. The second species is indigenous.

To control fruit flies, growers sometimes resort to pesticides that are registered for cotton production. This control method is not convenient or effective at all.

Because of the economic importance of fruit flies and the lack of appropriate control methods especially in SSA, research efforts on alternative fruit fly control strategies have received greater attention, including the use of endemic biological control agents.

Making more efficient use of natural means of pest control can greatly benefit planters.

At the beginning of 2008, a Regional Control Program of Mango Fruit Flies called “West African Fruit Fly Initiative” (WAFFI) was launched in West Africa by IITA-CIRAD, with World Bank funding. The program was based in IITA-Bénin. Seven West African countries took part in 2008, and another eight in 2009. A part of the WAFFI research focused mostly on the behavior of economically significant fruit flies and their control with biological control agents, such as weaver ants.

In Bénin, we studied the behavior of fruit flies in both laboratory and field tests over several months. These experiments revealed the fundamental role of info-chemicals of ants in repelling females of two fruit fly species during their oviposition or egg-laying period in mango. Interactions were studied on mango between two frugivorous or fruit-eating fly species (B. invadens and C. cosyra) and the African weaver ant (O. longinoda).

Predation of fruit fly larva third larval instar by weaver ants
Predation of fruit fly larva third larval instar by weaver ants

Results showed that: (1) female flies are strongly attracted to the mango fruit at ripening stages for egg laying; (2) without previous passage of ants on the fruit, the oviposition of tephritids (flies) is very important in mango; (3) once weaver ants have “patrolled” on mango fruit, female oviposition is significantly reduced; (4) C. cosyra seemed twice as sensitive as B. invadens about landing on treated fruit vs. untreated fruit; (5) similar results were found for the time spent on mango fruit; (6) ant-treated fruit had six times less damage from B. invadens and four times less damage from C. cosyra than untreated fruits; (7) B. invadens had significantly more pupae per kilogram fruit than C. cosyra in ant-free mango fruit, whereas no significant difference in ant-treated fruit was detected between the native C. cosyra and the exotic B. invadens.

The presence of weaver ants in mango trees reduced the damage caused by the fruit fly family Tephritidae through predation of adult fruit flies (rare), predation of third-stage larvae (quite frequent) and, especially, the effect of pheromones left by the ants on the fruit so that flies are repelled and are discouraged from egg-laying. Weaver ant presence resulted in a marked reduction in fruit damage.

The influence of info-chemicals from predators such as ants on the foraging behavior of fruit insects and more generally on pests could have crucial consequences for future observations and applications on host selection and consequently in host protection against these pests.

Practical information about the use of weaver ants in fruit fly pest control should be made available to all those involved in the fruit industry at every level, particularly local official producers, pickers, and rural advisors.

This work is also a good example of collaboration among IITA, Africa Rice, and CIRAD on a very important issue about high-value products in West Africa.

References
Adandonon A., J.F. Vayssières, A. Sinzogan, and P. Van Mele. 2009. Density of pheromone sources of the weaver ant Oecophylla longinoda affects oviposition behaviour and damage by mango fruit flies (Diptera: Tephritidae). International Journal of Pest Management. 55 (4), 285 – 292.
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Van Mele P. 2008. A historical review of research on the weaver ant Oecophylla in biological control. Agriculture and Forest Entomology. 10 (1), 13-22.
Van Mele P., J.F. Vayssières, E. Van Tellingen, and J. Vrolijks. 2007. Effects of the African weaver ant Oecophylla longinoda in controlling mango fruit flies (Diptera: Tephritidae). Journal of Economic Entomology. 100 (3), 695-701.
Van Mele P., J.F. Vayssières, A. Adandonon, and A. Sinzogan. 2009. Ant cues affect the oviposition behaviour of fruit flies (Diptera: Tephritidae) in Africa. Physiological Entomology. DOI: 10.1111/j.1365-3032.2009.00685.x
Vayssières J.F., G. Goergen, O. Lokossou, P. Dossa, and C. Akponon. 2005. A new Bactrocera species detected in Bénin among mango fruit flies (Diptera: Tephritidae) species. Fruits. 60 (6), 1-9.
Vayssières J.F. and A. Sinzogan. 2008. The use of weaver ants (Hymenoptera Formicidae) in fruit fly (Diptera: Tephritidae) pest control. Leaflet IITA-CIRAD N°= 5. West African Fruit Fly Initiative (WAFFI). 4 p.
Vayssières J.F., S. Korie, D. Ayegnon, and C. Akponon. 2009. Correlation of fruit fly (Diptera Tephritidae) infestation of major mango cultivars in Borgou (Bénin) with abiotic and biotic factors. Crop Protection. 28, 477-488.
Vayssières J.F., A. Sinzogan, and A. Adandonon. 2009. Principal methods for integrated control of fruit flies in West Africa. Leaflet IITA-CIRAD N°= 6. West African Fruit Fly Initiative (WAFFI). 4 p.