Assessing the biology of Bactrocera dorsalis (Hendel) (Diptera: Tephritidae) to understand its invasion potential into the Western Cape of SA

WELMA PIETERSE¹, ARUNA MANRAKHAN², JOHN TERBLANCHE³, PIA ADDISON⁴

¹Department of Agriculture, Forestry and Fisheries, Plant Quarantine Station, Stellenbosch, 7600 SA
²Citrus Research International, P.O.Box 28 Nelspruit 1200, SA
³Centre for Invasion Biology, Department of Conservation Ecology & Entomology, Faculty of AgriSciences, Stellenbosch University, SA
⁴Department of Conservation Ecology & Entomology, Faculty of AgriSciences, Stellenbosch University, SA

The Oriental fruit fly, Bactrocera dorsalis (Hendel) (Diptera: Tephritidae), was discovered on the African continent in 2003 (Lux et al. 2003). As per its common name, the species is of Asian origin and is a notorious pest of a number of commercial fruit. Specimens of B. dorsalis were detected in the northern parts of SA in 2010 and these populations were successfully eradicated (Manrakhan et al. 2011). In subsequent years, there were further detections of B. dorsalis in multiple locations in the north and north east of SA, which led to unsuccessful eradica-tion attempts in regions where it was detected (Manrakhan et al. 2015). In SA, the following provinces are currently declared as infested with B. dorsalis: Limpopo, Mpumalanga, North West, Gauteng, KwaZulu-Natal (excluding the magisterial districts of Amajuba, uMgungundlovu, uMzinyathi, uThukela and Zululand).
The B. dorsalis-free areas of SA are the Western Cape, Eastern Cape, Northern Cape and Free State provinces.

Distribution and niche modelling have shown that parts of the Western Cape Province may be susceptible to B. dorsalis (Hill and Terblanche 2014; De Villiers et al. 2016). Most deciduous fruit grown in the Western Cape Province are readily infested by fruit flies. The Mediterranean fruit fly (Medfly), Ceratitis capitata (Wiedemann), is the predominant fruit fly pest of deciduous fruit in the Western Cape Province.

Questions prevail around whether B. dorsalis will be able to establish successfully in the Western Cape of SA, with its Mediterranean climate, large deciduous fruit growing regions and C. capitata as the dominant fruit fly pest. This has required a three-year study of its temperature tolerances, host specific demography, as well as its competitive ability with C. capitata on various deciduous fruit types.

Physiology:

Because of the characterisation of B. dorsalis as a tropical pest, it was important to determine whether it would be able to persist in the extreme temperatures of a Mediterranean climate. Labora-tory tests were conducted to first determine the ability of B. dorsalis adults to survive extreme high and low temperatures, with and without pre-treatment exposure to non-lethal warm and low temperatures.

The ability of the different life stages of B. dorsalis (eggs, third instar larvae and adults) to survive short-term exposure to extreme temperatures was also tested. Survival of B. dorsa-lis, following exposure to extreme temperatures (high and low), was improved with pre-treatment of the adult flies, with non-lethal warm and low temperatures respectively.

When comparing the survival of different life stages of B. dorsalis, follow-ing a two-hour exposure to extreme temperatures (high and low), the egg stage was found to be more resistant. Compared to indigenous Ceratitis species present in SA – C. capitata and C. rosa – B. dorsalis was found to be less plastic in its ability to rapidly heat and cold-harden. As such, the results of this study suggest that B. dorsalis could have a narrower thermal niche, compared to C. capitata and C. rosa (Pieterse et al. 2017).

Demographic parameters on deciduous fruit:

Very little information was available on the demographic parameters of B. dorsalis on deciduous fruit crops, as well as the suitability of these locally grown crops, to sustain populations of the pest. It was clear from the laboratory experiments on detached fruit that all deciduous fruit types tested were suitable for B. dorsalis to complete its life cycle.

While B. dorsalis and C. capitata were equally successful in utilising most fruits tested, there were differences in the demography between the two species on deciduous fruit. Bactrocera dorsalis adults generally lived longer than those of C. capitata and had a higher net reproductive rate on all deciduous fruit tested, compared to C. capitata (Table 1). Ceratitis capitata had a higher intrinsic rate of increase (faster popula-tion growth) than B. dorsalis on all deciduous fruit types.

The develop-ment of larvae to adults took longer for both species in apple than in any other fruit, making apple suitable as an initial overwintering crop for both species.

Competitive interactions between B. dorsalis and C. capitata:

Since B. dorsalis is known as an aggressive invader, often out-competing C. cosyra and C. capitata on several host plants (Ekesi et al., 2009), it was important to determine its ability to compete with C. capitata on deciduous fruit. In a laboratory study, with B. dorsalis and C. capitata exposed in equal numbers as larvae and adults on nectarine, plum, pear and apple, B. dorsalis was reared in higher numbers than C. capitata from most fruit types tested, except pear (Figure 2 and 3).

This study has provided some insights on the invasive potential of B. dorsalis in the Western Cape Province of SA by quantifying its thermal tolerances, demography on deciduous fruit and competitive ability with C. capitata. In order to fully evaluate the invasive potential of B. dorsalis in the Western Cape Province, further research is needed, in particular on its tolerance to low relative humidity and low rainfall; its tolerance to long periods of cold exposure; as well as on the utilisation of deciduous fruit at different stages of maturity.

It can be conclusively stated in this study that biotic conditions (such as fruit types) in the Western Cape Province would be suitable for B. dorsalis. Temperature extremes, in particular very low temperatures during winter in some areas of the Western Cape, might be limiting factors. When abiotic conditions are suitable, C. capitata, the current dominant fruit fly pest on deciduous fruit, would not be a major competitor for B. dorsalis. In the case of an incursion of B. dorsalis in the Western Cape Province, all efforts would have to be implemented to eradicate this pest.

Summary and actions:

• REGULAR MONITORING TO DETECT POPULATIONS IS ESSENTIAL: Bactrocera dorsalis produced more eggs than C. capitata per female on all deciduous fruit, and the eggs of B. dorsalis hatched sooner (after 32 hours) than those of C. capitata. Bactrocera dorsalis can complete its life cycle in 18-20 days in nectarine.
• QUICK ERADICATION ACTIONS should be taken when B. dorsalis is detected, such as the use of baits, Male Annihilation Technique and regular orchard sanitation.
• ORCHARD SANITATION MEASURES MUST BE STRICTLY ADHERED TO, IN ORDER TO SUPPORT THE ERADICATION ACTIONS. It has been observed in mango orchards in the Lowveld that more of the fallen fruit on the orchard floor are infested with B. dorsalis than fruit still hanging in the tree. Apple is a fruit type that can serve as a bridging host for B. dorsalis to survive the autumn temperatures in the Western Cape. Deciduous fruit on the ground and left over on the tree after harvest, should be collected and either buried at least 1 m below the ground, finely ground or placed in black bags and left in the sun to kill all developing fruit fly larvae.

• Fruit like apple and pear are less effective hosts for C. capitata, but are better hosts for B. dorsalis, since B. dorsalis deposited a significantly higher number of eggs on pear and lived longer on apple. In case of establishment of B. dorsalis, costs of spray programmes might increase as interventions may have to be applied more often to combat the high reproductive potential of B. dorsalis, specifically on apples and pears.

References

DE VILLIERS, M., HATTINGH, V., KRITICOS, D.J., BRUNEL, S., VAYSSIÈRES, J.F., SINZOGAN, A., BILLAH, M.K., MOHAMED, S.A., MWATAWALA, M., ABDELGADER, H. & SALAH, F.E.E.  2016. The potential distribu-tion of Bactrocera dorsalis: considering phenology and irrigation patterns. Bulletin of entomological research 106(1):  19-33.

EKESI, S., BILLAH, M.K., NDERITU, P.W., LUX, A.L. & RWOMUSHANA, I.  2009.  Evidence for Competitive Displacement of Ceratitis cosyra by the Invasive Fruit Fly Bactrocera invadens

(Diptera: Tephritidae) on Mango and Mechanisms Contributing to the Displacement.  Journal of Economic Entomology 102(3): 981-991.

HILL, M.P. & TERBLANCHE, J.S.  2014.  Niche overlap of conge-neric invaders supports a single-species hypothesis and provides insight into future invasion risk: implications for global management of the Bactrocera dorsalis complex. PloS one 9(2):  e90121.

LUX, S.A., COPELAND, R.S., WHITE, I.M., MANRAKHAN, A. & BILLAH, M.K.  2003.  A new invasive fruit fly species from the Bactrocera dorsalis (Hendel) group detected in East Africa. Insect Science and its Application 23(4): 355-361.

MANRAKHAN, A., VENTER, J.H., & HATTINGH, V.  2015.  The progres-sive invasion of Bactrocera dorsalis (Diptera: Tephritidae) in SA.  Biological Invasions 17(10): 2803-2809.

MANRAKHAN, A., HATTINGH, V., VENTER, J.-H. & HOLTZHAUSEN,

2011. 2011. Eradication of Bactrocera invadens (Diptera: Tephritidae) in Limpopo Province, SA. African Entomology 19, 650-659.

PIETERSE, W., TERBLANCHE, J.S. & ADDISON, P.  2017.  Do thermal tolerances and rapid thermal responses contribute to the invasion potential of Bactrocera dorsalis (Diptera: Tephritidae)? Journal of Insect Physiology 98: 1-6.