Abstract
The majority of African fruit fly species are controlled using behavioural methods (e.g. attract and kill). Sterile Insect Technique (SIT) has also been successfully used for a few African fruit fly pests, mostly outside of the African region. A thorough understanding of the feeding and mating behaviour of fruit fly pests is required when using behavioural control methods and SIT for fruit fly control. The feeding and mating behaviour of key African fruit fly pests are reviewed. Feeding and mating behaviours have been elucidated for only a few species with a wider global distribution. For the remaining Ceratitis, Bactrocera and Dacus species with a limited worldwide distribution, there are still important knowledge gaps in their behavioural ecology. With horticulture expanding in Africa and increasing trade of horticultural produce from the region, it is important that these knowledge gaps are filled so that control methods can be optimised.
Access provided by Autonomous University of Puebla. Download chapter PDF
Similar content being viewed by others
Keywords
1 Introduction
African fruit fly pests are mainly monitored and controlled using attractive food baits and male lures (Ekesi et al. 2007; Manrakhan 2006). For control, food baits and male lures are combined with a toxin or pathogen in an attract and annihilate approach; adult fruit flies are attracted to the bait/ lure and killed by the toxin or pathogen (Cunningham 1989; Roessler 1989). Such behavioural control methods are effective and limit insecticide use, but their efficacy can be influenced by a number of intrinsic (e.g genetic and physiological factors) and extrinsic (e.g climate, host abundance) factors (Foster and Harris 1997). As such, a thorough understanding of the feeding and mating behaviour of each pest species is essential for the optimisation of control methods.
For some fruit fly pests, the Sterile Insect Technique (SIT) has also been successfully used worldwide as a method for prevention, containment, suppression and eradication (Enkerlin 2005). To date the use of SIT in Africa is still limited. Effectiveness of SIT programmes are dependent on successful mating of sterile males with wild-type females and the subsequent induction of reproductive failure (Perez-Staples et al. 2012). Given that most tropical and subtropical fruit flies have complex mating systems (Burk 1981), a detailed understanding of each mating system is crucial for successful development and optimisation of SIT (Hendrichs et al. 2002).
Here I review the current status of knowledge on the feeding and mating behaviour of key fruit fly pest species in Africa grouped under four genera: Ceratitis, Bactrocera, Zeugodacus and Dacus. Future research needs required to fill the gaps in our understanding of feeding and mating behaviour of these African fruit fly pests are also discussed.
2 Feeding Behaviour of African Fruit Flies
Fruit flies only feed during the larval and adult stages (Christenson and Foote 1960). Frugivorous fruit fly larvae feed on the fruit pulp while adult flies have been reported feeding on various sources including extra-floral glandular secretions from plants, plant leachates, fruit juices, bacteria, honeydew and bird faeces in order to acquire sufficient carbohydrate and protein for survival and reproduction (Christenson and Foote 1960; Hendrichs and Hendrichs 1990; Manrakhan and Lux 2009; McQuate et al. 2003; Nishida 1958; Warburg and Yuval 1997). Studies on the mouthparts of adult Bactrocera and Ceratitis species have revealed that adult flies have a fluid-centered mode of feeding and a labellar-filter-feeding mechanism allowing them to ingest fluids and particles that are less than 0.5 μm in size (Vijaysegaran et al. 1997; Coronado-Gonzalez et al. 2008). All frugivorous female fruit flies are anautogenous, that is they need to feed on protein to realise their reproductive potential (Drew and Yuval 2001). Furthermore, nutrition plays an important role in both the regulation of oocyte maturation and male accessory gland development (Williamson 1989). Foraging behaviour of adult flies occurs at different hierarchical levels: the habitat (fruit-growing area), the patch (host trees or non-host trees) and the specific food item (Hassell and Southwood 1978; Prokopy and Roitberg 1989). The initial identification of a potential food item by a fly is largely achieved through olfaction (Dethier 1976). Olfactory receptors on the antennae and on the palps of fruit flies are sensitive to the gaseous products of amino acid breakdown, mainly ammonia (Rice 1989; Tsiropoulos 1992). The attraction of fruit flies to protein-based odours is exploited in the use of poisoned food baits for fruit fly control (Roessler 1989).
A thorough understanding of adult feeding behaviour has direct implications in optimising control of fruit fly pests using food baits (Hendrichs and Prokopy 1994). In relation to the application of food baits, knowing what attracts flies to food and understanding the factors that influence feeding behaviour can improve the efficacy of control strategies using food baits.
2.1 Ceratitis Species
Research on the feeding behaviour of Ceratitis species has largely been restricted to a few of the key pest species: the Mediterranean fruit fly (medfly), Ceratitis capitata (Wiedemann); Ceratitis fasciventris Bezzi; the Natal fruit fly, Ceratitis rosa Karsch; and the mango fruit fly, Ceratitis cosyra (Walker). Some of these fruit fly pests prefer to reside on host trees compared with non-host trees, and for this reason most of their food foraging activities are likely to occur within host patches (Manrakhan 2009; Hendrichs and Hendrichs 1990).
The type of food ingested influences survival and the reproductive activity of Ceratitis species. Survival of some pest species of Ceratitis was poor without a sugar source (Hendrichs and Hendrichs 1990; Hendrichs et al. 1991; Manrakhan and Lux 2006). Calling, mating, egg laying and egg fertility was greater in adult Ceratitis species feeding on a protein-rich diet than on a protein-poor diet (Kaspi et al. 2000; Kaspi and Yuval 2000; Papadopoulos et al. 1998; Manrakhan and Lux 2006; Taylor and Yuval 1999; Shelly et al. 2002; Hendrichs et al. 1991). The effect of protein on longevity of C. capitata varied amongst different studies. Some studies reported better survival of flies maintained on a constant diet of sugar and protein compared with flies maintained on only sugar sources (Cangussu and Zucoloto 1995; Manrakhan and Lux 2006). Other studies showed a reduced mortality in C. capitata flies when they were deprived of protein (Carey et al. 1998; Hendrichs et al. 1991; Kaspi and Yuval 2000).
Temporal patterns of feeding have been described for a number of Ceratitis species. With respect to time of the day, male Ceratitis fasciventris (Bezzi) and male C. capitata fed mainly in the morning and late afternoon respectively, after having engaged in reproductive activities (Hendrichs and Hendrichs 1990; Manrakhan and Lux 2006; Warburg and Yuval 1997). With respect to the age of flies, for C. cosyra, C. fasciventris and C. capitata, sugar consumption was greater soon after emergence whilst protein feeding usually occurred either in or after the first week of adult life depending on species and sex (Manrakhan and Lux 2009). Nutritional state had a significant influence on the responses of C. cosyra, C. fasciventris and C. capitata to food odours. Sugar deprivation increased responses of young flies to food odours but there was no preference for particular types of odours in young sugar-deprived flies (Cohen and Voet 2002; Manrakhan and Lux 2008). Protein deprivation in mature flies enhanced their response to protein odours (Barry et al. 2003; Manrakhan and Lux 2008; Prokopy et al. 1992). Not all protein odours are equally attractive to adult Ceratitis species. For example, amongst different animal droppings that form part of the natural food complex of C. capitata, a preference for droppings from birds and lizards compared with droppings from mammals was shown for this species (Prokopy et al. 1993). Moreover for C. capitata and other Ceratitis species, natural food sources were more attractive than artificial food baits (Manrakhan and Lux 2008; Prokopy et al. 1992). Variation in fly responses to different artificial proteinaceous baits has also been recorded (Katsoyannos et al. 1999; Manrakhan and Kotze 2011). The degree of response to protein baits differed between Ceratitis species (Manrakhan and Kotze 2011); this has important implications as baits that are effective for control of one Ceratitis species may not be as effective for other Ceratitis species. Differences in responses to protein odours amongst Ceratitis species could be linked to their protein requirement and therefore their sensitivity to volatiles emanating from protein sources.
2.2 Bactrocera Species
The three most important Bactrocera pest species in the African region include the oriental fruit fly, Bactrocera dorsalis (Hendel) previously known as B. invadens Drew, Tsuruta and White (Schutze et al. 2014); the peach fruit fly, Bactrocera zonata (Saunders); and the solanum fruit fly, Bactrocera latifrons (Hendel); they are all of Asian origin and only recently introduced in to the African region (De Meyer et al. 2014; Ekesi and Muchugu 2006). There is generally a lack of information on the feeding behaviour and food bait preferences of B. zonata and B. latifrons. In the island of Mauritius, investigations found that B. zonata responded equally well to a commercially available protein hydrolysate and processed brewery yeast waste (Gopaul et al. 2000). In contrast to most Bactrocera species, more information is available on the feeding behaviour of B. dorsalis. Early studies by Bess and Haramoto (1961) in Hawaii suggested that B. dorsalis foraged for food and shelter on plants other than one of its preferred host plants, guava. However, subsequent studies in Hawaii have shown that B. dorsalis prefers to forage on guava (Vargas et al. 1990). In laboratory studies under controlled conditions, B. dorsalis engaged in feeding behaviour during the morning (Arakaki et al. 1984). As with Ceratitis species, reproduction of B. dorsalis was affected by the type of food ingested. A protein source in the adult diet of B. dorsalis was important for reproduction (Shelly et al. 2005). For example, B. dorsalis males deprived of protein had fewer matings that those that had access to protein (Shelly et al. 2005). Protein feeding decreased attraction of mature adult B. dorsalis females to protein odours whilst immature protein-fed B. dorsalis females were equally attracted to fruit and protein odours (Cornelius et al. 2000). In studies conducted recently in Kenya, B. dorsalis showed preferences for particular protein baits, and females were more attracted to protein baits than males (Ekesi et al. 2014). In studies conducted in Hawaii, young female B. dorsalis had stronger positive responses to protein baits than older females (Barry et al. 2006; Pinero et al. 2011). The results of studies on food bait preferences for B. dorsalis have been at times conflicting. For example, in studies done in Tanzania and Kenya, the three-component Biolure (ammonium acetate, putrescine, trimethylamine) was less attractive to B. dorsalis than liquid protein baits such as Torula yeast (Ekesi et al. 2014; Mwatawala et al. 2006). However, current trials in South Africa have found that the three-component Biolure is more attractive to B. dorsalis than liquid protein baits such as Torula yeast (Manrakhan et al., unpublished data). A more in depth understanding of the responses of B. dorsalis to food attractants is required for optimisation of monitoring and control efforts against this pest.
2.3 Zeugodacus Species and Dacus Species
In Africa, the melon fly, Zeugodacus cucurbitae (Coquillet) previously known as Bactrocera cucurbitae (Coquillet) (Virgilio et al. 2015) and a number of Dacus fruit fly species are economically important pests of vegetables in the family Cucurbitaceae (Ekesi and Muchugu 2006). Studies on a few cucurbit-infesting fruit fly pests have shown that flies preferred to congregate on non-host plants while host plants were only visited by gravid females for oviposition (Nishida and Bess 1950; Atiama-Nurbel et al. 2012). For this reason control efforts targeted at these species and based on food baits have been done on non-host plants rather than host plants (Prokopy et al. 2003). Other than studies on the distribution of cucurbit-infesting fruit flies within a habitat, there is very little information on their feeding behaviour. Zeugodacus cucurbitae; the lesser pumpkin fly, Dacus ciliatus (Loew); and Dacus demmerezi (Bezzi) respond to protein baits, although the degree of response differed between species and within some species in respect to age and starvation status depending on bait type (Barry et al. 2006; Deguine et al. 2012; Nestel et al. 2004; Pinero et al. 2011). There is a lack of information on the temporal feeding patterns of these species. Moreover, for some Dacus species, such as D. ciliatus, which do not respond well to commercially available protein baits (Deguine et al. 2012), detailed studies on their feeding requirements and habits are urgently required.
3 Mating Behaviour of African Fruit Flies
Afrotropical fruit flies, in particular those that are polyphagous, have complex mating systems which involve the formation of leks (Sivinski and Burk 1989). Leks are male communal display aggregations, with the purpose of attracting females (Sivinski and Burk 1989). An understanding of the mating behaviour of key African fruit fly pests is important in the development of SIT for control of these pests (Hendrichs et al. 2002). Male lures used for monitoring and control of African fruit fly species are known to influence the mating behaviour of some species (Khoo and Tan 2000; Shelly and Dewire 1994; Tan and Nishida 1998). The use of male lures in combination with insect growth regulators (IGRs) or pathogens will require a better understanding of the effect of these male lures on the mating behaviour of the flies since it is essential that lure-fed males interact and mate with wild females if sterilisation or transmission of pathogens is to be effective.
3.1 Ceratitis Species
The mating behaviour of C. capitata has been studied extensively over the years (see review by Eberhard [2000]). However, very little is known about the mating behaviour of other Ceratitis species. The courtship behaviour of C. rosa, C. cosyra, C. fasciventris and Ceratitis catoirii Guérin-Mèneville has been studied in laboratory and field cages (Manrakhan and Lux 2009; Quilici et al. 2002; Myburgh 1962). Unlike C. capitata and C. catoirii which are day mating species, C. rosa, C. fasciventris and C. cosyra began mating activity at dusk, staying in copula until day break (Manrakhan and Lux 2009; Quilici et al. 2002). In studies conducted under laboratory conditions in Kenya, protein in the adult food diet influenced the calling and mating behaviour of C. fasciventris and C. cosyra (Manrakhan and Lux 2006). Frequency of calling in C. fasciventris males, and mating in C. fasciventris and C. cosyra, was higher when the flies were fed on a protein-rich diet as compared to a protein-poor diet (Manrakhan and Lux 2006). For Ceratitis species other than C. capitata, the factors affecting their mating behaviour, remating habits and sperm transfer have yet to be elucidated. This lack of research on Ceratitis species other than C. capitata may be due to limited interest in developing SIT for control of those pests in Africa. However for other regions in the world which are still free of important polyphagous Ceratitis pests such as C. rosa, C. cosyra and C. fasciventris, the development of SIT targeting those species is still relevant and needs to be pursued since SIT can be used either as a preventative control measure against introduction of these pests, or as an eradication tool.
3.2 Bactrocera Species
Bactrocera species that are pests in the African continent are dusk-mating species, a characteristic of the majority of dacine fruit flies (Fletcher 1987). There is evidence for male-produced sex pheromones in B. dorsalis (Kobayashi et al. 1978). The rectal glands of male fruit flies produce and store sex pheromones (Fletcher 1987) and are present in male B. dorsalis (Schultz and Boush 1971). Sexually mature virgin B. dorsalis females were highly attracted to mature males and to the excised rectal glands of the males, particularly around dusk (Kobayashi et al. 1978). In B. dorsalis, mating begins at dusk when the light intensity falls to 280 Lux and continues until day break (Arakaki et al. 1984). Pairs of B. dorsalis remain in copula for ~10 h and copulation was found to be more successful in males that engaged in wing vibration (Arakaki et al. 1984). Under laboratory conditions adults only begin mating on the 11th day after emergence (Arakaki et al. 1984). Under field conditions, leks of 2–12 male B. dorsalis were found on host plants with each male defending an individual leaf; when a female arrived on a leaf the male mounts her and copulation proceeds (Shelly and Kaneshiro 1991). Female visits were not influenced by the sizes of leks suggesting a less intense female choice in the mating system of B. dorsalis compared with that of C. capitata (Shelly 2001). A different facet of female choice was demonstrated by Poramarcom and Boakes (1991), who showed that female B. dorsalis preferred dominant males and those that mated twice. Mating success was also greater in B. dorsalis males with previous exposure to methyl eugenol and protein (Shelly 2000; Shelly and Dewire 1994; Shelly et al. 2005; Tan and Nishida 1998). This may be because male B. dorsalis (reported as Bactrocera papaya Drew and Hancock in the publication) are known to convert methyl eugenol to other derivatives, particularly phenyl propanoids, which then act as sex pheromones to attract females during courtship (Hee and Tan 1998; Tan and Nishida 1998); one phenylpropanoid coniferyl alcohol was highly attractive to B. dorsalis females (Hee and Tan 1998).
Bactrocera latifrons, another important pest species in Africa, has a similar mating system to B. dorsalis. Jackson and Long (1997) described the mating behaviour of this pest species in field cages on coffee trees; leks of 4–9 calling males were observed and mating occurred between 1 h before sunset and 15 min after sunset (Jackson and Long 1997). Bactrocera latifrons, like other Bactrocera species, sequester male–specific attractants in their rectal glands (Nishida et al. 2009).
In contrast to B. dorsalis and B. latifrons, information on the mating behaviour of B. zonata is largely lacking. Bactrocera zonata males have a strong attraction to methyl eugenol (Tan et al. 2010). In the rectal glands of B. zonata, methyl eugenol is synthesised to form a blend of phenylpropanoid volatiles that are different to that produced by B. dorsalis (Tan et al. 2010).
3.3 Zeugodacus Species and Dacus Species
Zeugodacus cucurbitae is a dusk-mating species (Suzuki and Koyama 1980), similar to the Bactrocera pest species in Africa. Laboratory strains have shorter pre-mating periods and initiate mating at higher light intensities than their wild counterparts (Suzuki and Koyama 1980). Lek formation has been suggested for Z. cucurbitae (Kuba et al. 1984; Kuba and Koyama 1985). Raspberry ketone (a derivative of Cuelure which is a known male lure of Z. cucurbitae) increased the production of female-attracting sex pheromone, male-aggregation pheromone and was also an allomone (Khoo and Tan 2000).
The mating behaviour of other cucurbit infesting fruit flies has been poorly studied. Rempoulakis et al. (2015) recently described the mating behaviour of D. ciliatus but the mating habits of the other Dacus species remain undescribed. For Dacus species that do not respond to commercially available protein baits, the use of male lures with toxins and pathogens as well as SIT could still be viable control tools. The development of these techniques will, however, require an in depth investigation of the mating behaviour of Dacus species.
4 Conclusion
Within the African fruit fly pest complex, feeding and mating behaviours have been elucidated for only a few species with a wider global distribution. For the remaining Ceratitis, Bactrocera and Dacus species with a limited worldwide distribution, there are still important knowledge gaps in their behavioural ecology. With horticulture expanding in Africa and increasing trade of horticultural produce from the region, it is important that these knowledge gaps are filled so that control methods can be optimised.
References
Arakaki N, Kuba H, Soemori H (1984) Mating behaviour of the Oriental fruit fly, Dacus dorsalis Hendel (Diptera: Tephritidae). Appl Entomol Zool 19(1):42–51
Atiama-Nurbel T, Deguine J-P, Quilici S (2012) Maize more attractive than Napier grass as non-host plants for Bactrocera cucurbitae and Dacus demmerezi. Arthropod Plant Interact 6:395–403
Barry JD, Vargas RI, Miller GT, Morse JG (2003) Feeding and foraging of wild and sterile Mediterranean fruit flies (Diptera: Tephritidae) in the presence of spinosad bait. J Econ Entomol 96(5):1405–1411
Barry JD, Miller NW, Pinero JC, Tuttle A, Mau FL, Vargas RI (2006) Effectiveness of protein baits on melon fly and Oriental fruit fly (Diptera: Tephritidae): attraction and feeding. J Econ Entomol 99(4):1161–1167
Bess HA, Haramoto FH (1961) Contributions to the biology and ecology of the Oriental fruit fly, Dacus dorsalis Hendel (Diptera: Tephritidae), in Hawaii, vol 44. Hawaii Agricultural Experiment Station, University of Hawaii, Technical Bulletin, Honolulu, pp 5–30
Burk T (1981) Signalling and sex in acalyptrate flies. Fla Entomol 64(1):30–43
Cangussu JA, Zucoloto FS (1995) Self-selection and perception threshold in adult females of Ceratitis capitata (Diptera, Tephritidae). J Insect Physiol 41(3):223–227
Carey JR, Liedo P, Muller HG, Wang JL, Vaupel JW (1998) Dual modes of aging in Mediterranean fruit fly females. Science 281:996–998
Christenson LC, Foote RH (1960) Biology of fruit flies. Annu Rev Entomol 5:171–192
Cohen H, Voet H (2002) Effect of physiological state of young Ceratitis capitata females, on resource foraging behaviour. Entomol Exp Appl 104:345–351
Cornelius ML, Nergel L, Duan JJ, Messing RH (2000) Responses of female Oriental fruit flies (Diptera:Tephritidae) to protein and fruit odors in field cage and open field tests. Environ Entomol 29(1):14–19
Coronado-Gonzalez PA, Vijaysegaran S, Robinson AS (2008) Functional morphology of the mouthparts of the adult Mediterranean fruit fly, Ceratitis capitata. J Insect Sci 8(73):1–11. doi:10.1673/031.008.7301
Cunningham RT (1989) Male Annihilation. In: Robinson AS, Hooper G (eds) Fruit flies: their biology, natural enemies and control, vol 3B. Elsevier, Amsterdam, pp 345–351
De Meyer M, Mohamed S, White IM (2014) Invasive fruit fly pests in Africa. http://www.africamuseum.be/fruitfly/AfroAsia.htm. Accessed 30 Nov 2012
Deguine J-P, Douraguia E, Atiama-Nurbel T, Chiroleu F, Quilici S (2012) Cage study of spinosad-based bait efficacy on Bactrocera cucurbitae, Dacus ciliatus, and Dacus demmerezi (Diptera: Tephritidae) in Reunion Island. J Econ Entomol 105(4):1358–1365
Dethier VG (1976) The hungry fly. Harvard University Press, Cambridge, MA/London
Drew RAI, Yuval B (2001) The evolution of fruit fly feeding behavior. In: Aluja M, Norrbom AL (eds) Fruit flies (Tephritidae): phylogeny and evolution of behaviour. CRC Press, Boca Raton, pp 731–749
Eberhard WG (2000) Sexual behavior and sexual selection in the medfly, Ceratitis capitata. In: Aluja M, Norrbom A (eds) Fruit flies (Tephritidae): phylogeny and evolution of behavior. CRC Press, Boca Raton, pp 459–489
Ekesi S, Muchugu E (2006) Tephritid fruit flies in Africa- fact sheets of some economically important species. In: Ekesi S, Billah MK (eds) A field guide to the management of economically important Tephritid fruit flies in Africa, 2nd edn. icipe Science Press, Nairobi, pp B-1–B-19
Ekesi S, Mohamed SA, Hanna R, Lux SA, Gnanvossou D, Bokonon-Ganta A (2007) Fruit fly suppression- purpose, tools and methodology. In: Ekesi S, Billah MK (eds) A field guide to the management of economically important Tephritid fruit flies in Africa. International Centre of Insect Physiology and Ecology, Nairobi, pp D1–D15
Ekesi S, Mohamed S, Tanga CM (2014) Comparison of food-based attractants for Bactrocera invadens (Diptera: Tephritidae) and evaluation of mazoferm-spinosad bait spray for field suppression in mango. J Econ Entomol 107(1):299–309
Enkerlin WR (2005) Impact of fruit fly control programmes using the sterile insect technique. In: Dyck VA, Hendrichs J, Robinson AS (eds) Sterile insect technique. Principles and practice in area-wide integrated pest management. Springer, Dordrecht, pp 651–676
Fletcher BS (1987) The biology of dacine fruit flies. Annu Rev Entomol 32:115–144
Foster SP, Harris MO (1997) Behavioural manipulation methods for insect pest management. Annu Rev Entomol 42:123–146
Gopaul S, Price NS, Soonoo R, Stonehouse J, Stravens R (2000) Local production of protein bait: Mauritius. Technologies of fruit fly monitoring and control in the Indian Ocean region. Indian Ocean Commission Regional Fruit Fly Programme, Reduit
Hassell MP, Southwood TRE (1978) Foraging strategies of insects. Annu Rev Ecol Syst 9:75–78
Hee AK-W, Tan KH (1998) Attraction of female and male Bactrocera papayae to conspecific males fed with methyl eugenol and attraction of females to male sex pheromone components. J Chem Ecol 24(4):753–764
Hendrichs J, Hendrichs MA (1990) Mediterranean fruit fly (Diptera: Tephritidae) in nature: location and diel pattern of feeding and other activities on fruiting and nonfruiting hosts and nonhosts. Ann Entomol Soc Am 83(3):632–641
Hendrichs J, Prokopy RJ (1994) Food foraging behaviour of frugivorous fruit flies. In: Calkins CO, Klassen W, Liedo P (eds) Fruit flies and the sterile insect technique. CRC Press, Boca Raton, pp 37–55
Hendrichs J, Katsoyannos BI, Papaj DR, Prokopy RJ (1991) Sexual differences in movement between natural feeding and mating sites and tradeoffs between food consumption, mating success and predator evasion in Mediterranean fruit flies (Diptera: Tephritidae). Oecologia 86:223–231
Hendrichs J, Robinson AS, Cayol JP, Enkerlin W (2002) Medfly areawide sterile insect technique programmes for prevention, suppression or eradication: the importance of mating behaviour studies. Fla Entomol 85(1):1–13
Jackson CG, Long JP (1997) Mating behaviour of Bactrocera latifrons (Diptera: Tephritidae) in field cages. Ann Entomol Soc Am 90(6):856–860
Kaspi R, Yuval B (2000) Post-teneral protein feeding improves sexual competitiveness but reduces longevity of mass-reared sterile male Mediterranean fruit flies (Diptera:Tephritidae). Ann Entomol Soc Am 93(4):949–955
Kaspi R, Taylor PW, Yuval B (2000) Diet and size influence sexual advertisement and copulatory success of males in Mediterranean fruit fly leks. Ecol Entomol 25:279–284
Katsoyannos BI, Heath RR, Papadopoulos NK, Epsky ND, Hendrichs J (1999) Field evaluation of Mediterranean fruit fly (Diptera:Tephritidae) female selective attractants for use in monitoring programs. J Econ Entomol 92(3):583–589
Khoo CCH, Tan KH (2000) Attraction of both sexes of melon fly, Bactrocera cucurbitae to conspecific males – a comparison after pharmacophagy of cue-lure and a new attractant – zingerone. Entomol Exper Appl 97:317–320
Kobayashi RM, Ohinata K, Chambers DL, Fujimoto MS (1978) Sex pheromones of the Oriental fruit fly and the melon fly: mating behaviour, bioassay method, and attraction of females by live males and by suspected pheromone glands of males. Environ Entomol 7(1):107–112
Kuba H, Koyama J (1985) Mating behaviour of wild melon flies, Dacus cucurbitae Coquillett (Diptera: Tephritidae) in a field cage: courtship behaviour. Appl Entomol Zool 20(4):365–372
Kuba H, Koyama J, Prokopy RJ (1984) Mating behaviour of wild melon flies, Dacus cucurbitae Coquillett (Diptera: Tephritidae) in a field cage: distribution and behaviour of flies. Appl Entomol Zool 19(3):367–373
Manrakhan A (2006) Fruit fly monitoring – purpose, tools and methodology. In: Ekesi S, Billah MK (eds) A field guide to the management of economically important Tephritid fruit flies in Africa. icipe Science Press, Nairobi, pp c1–c17
Manrakhan A (2009) Diel and lifetime patterns of activities of African fruit flies (Diptera:Tephritidae) (unpublished data)
Manrakhan A, Kotze C (2011) Attraction of Ceratitis capitata, C. rosa and C. cosyra (Diptera: Tephritidae) to proteinaceous baits. J Appl Entomol 135:98–105
Manrakhan A, Lux SA (2006) Contribution of natural food sources to reproductive behaviour, fecundity and longevity of Ceratitis cosyra, Ceratitis fasciventris and Ceratitis capitata (Diptera: Tephritidae). Bull Entomol Res 96:259–268
Manrakhan A, Lux SA (2008) Effect of food deprivation on attractiveness of food sources, containing natural and artificial sugar and protein, to three African fruit flies: Ceratitis cosyra, Ceratitis fasciventris and Ceratitis capitata. Entomol Exper Appl 127:133–143
Manrakhan A, Lux SA (2009) Diel and lifetime patterns of feeding and reproductive activities of three African fruit flies, Ceratitis cosyra, Ceratitis fasciventris and Ceratitis capitata (Diptera: Tephritidae) in semi-field cages of different spatial scales. Afr Entomol 17(1):8–22
McQuate GT, Jones GD, Sylva CD (2003) Assessment of corn pollen as food sources for two Tephritid fruit fly species. Environ Entomol 32(1):141–150
Mwatawala MW, De Meyer M, Makundi RH, Maerere AP (2006) Biodiversity of fruit flies (Diptera: Tephritidae) in orchards in different agro-ecological zones of the Morogoro region, Tanzania. Fruits 61(5):321–332
Myburgh AC (1962) Mating habits of the fruit flies Ceratitis capitata (Wied.) and Pterandus rosa (Ksh.). South Afr J Agric Sci 5(3):457–464
Nestel D, Nemny-Lavy E, Zilberg L, Weiss M, Akiva R, Gazit Y (2004) The fruit fly PUB: a phagostimulation unit bioassay system to quantitatively measure ingestion of baits by individual flies. J Entomol 128:576–582
Nishida T (1958) Extrafloral glandular secretions, a food source for certain insects. Proc Hawaiian Entomol Soc 16(3):379–386
Nishida T, Bess HA (1950) Applied ecology in melon fly control. J Econ Entomol 43:877–883
Nishida R, Enomoto H, Shelly TE, Ishida T (2009) Sequestration of 3-oxygenated α-ionone derivatives in the male rectal gland of the solanaceous fruit fly, Bactrocera latifrons. Entomol Exper Appl 131:85–92
Papadopoulos NK, Katsoyannos BI, Kouloussis NA, Economopoulos AP, Carrey JR (1998) Effect of adult age, food, time of day on sexual calling incidence of wild and mass-reared Ceratitis capitata males. Entomol Exper Appl 89:175–182
Perez-Staples D, Shelly TE, Yuval B (2012) Female mating failure and the failure of ‘mating’ in sterile insect programs. Entomol Exper Appl 146:66–78
Pinero JC, Mau RFL, Vargas RI (2011) A comparative assessment of the response of three fruit fly species (Diptera: Tephritidae) to a spinosad-based bait: effect of ammonium acetate, female age, and protein hunger. Bull Entomol Res 101(4):373–381
Poramarcom R, Boakes CRB (1991) Behavioural influences on male mating success in the Oriental fruit fly, Dacus dorsalis Hendel. Anim Behav 42:453–460
Prokopy RJ, Roitberg BD (1989) Fruit fly foraging behaviour. In: Robinson AS, Hooper G (eds) Fruit flies: their biology, natural enemies and control, vol 3A, World crop pests. Elsevier, Amsterdam, pp 293–304
Prokopy RJ, Papaj DR, Hendrichs J, Wong TTY (1992) Behavioural responses of Ceratitis capitata flies to bait spray droplets and natural food. Entomol Exper Appl 64:247–257
Prokopy RJ, Hsu CL, Vargas RI (1993) Effect of source and condition of animal excrement on attractiveness to adults of Ceratitis capitata (Diptera: Tephritidae). Environ Entomol 22(2):453–458
Prokopy RJ, Miller NW, Pinero JC, Barry JD, Tran LC, Oride L, Vargas RI (2003) Effectiveness of GF-120 fruit fly bait spray applied to border area plants for control of melon flies (Diptera: Tephritidae). J Econ Entomol 96(5):1485–1493
Quilici S, Franck A, Peppuy A, Dos Reis CE, Mouniama C, Blard F (2002) Comparative studies of courtship behaviour of Ceratitis spp. (Diptera: Tephritidae) in Reunion Island. Fla Entomol 85:138–142
Rempoulakis P, Nemny-Lavy E, Castro R, Nestel D (2015) Mating behaviour of Dacus ciliatus (Loew) [Diptera: Tephritidae]: comparisons between a laboratory and a wild population. J Appl Entomol 140:250–260. doi:10.1111/jen.12252
Rice MJ (1989) The sensory physiology of fruit flies: conspectus and prospectus. In: Robinson AS, Hooper G (eds) Fruit flies, their biology, natural enemies and control, vol 3A. Elsevier, Amsterdam, pp 249–272
Roessler Y (1989) Insecticidal bait and cover sprays. In: Robinson AS, Hooper G (eds) World crop pests, fruit flies: their biology, natural enemies and control, vol 3B. Elsevier, Amsterdam, pp 329–335
Schultz GA, Boush GM (1971) Suspected sex pheromone glands in three economically important species of Dacus. J Econ Entomol 64(2):347–349
Schutze MK, Mahmood K, Pavasovic A, Bo W, Newman J, Clarke AR, Krosch MN, Cameron SL (2014) One and the same: integrative taxonomic evidence that Bactrocera invadens (Diptera: Tephritidae) is the same species as the Oriental fruit fly Bactrocera dorsalis. Syst Entomol 40:472–486. doi:10.1111/syen.12114
Shelly TE (2000) Fecundity of female Oriental fruit flies (Diptera: Tephritidae): effects of methyl-eugenol fed and multiple mates. Ann Entomol Soc Am 93(3):559–564
Shelly TE (2001) Lek size and female visitation in two species of tephritid fruit flies. Anim Behav 62:33–40
Shelly TE, Dewire AM (1994) Chemically mediated mating success in male Oriental fruit flies (Diptera: Tephritidae). Ann Entomol Soc Am 87(3):375–382
Shelly TE, Kaneshiro KY (1991) Lek behaviour of the Oriental fruit fly. Dacus dorsalis, in Hawaii (Diptera: Tephritidae). J Insect Behav 4:235–241
Shelly TE, Kennelly SS, McInnis DO (2002) Effect of adult diet on signalling activity, mate attraction, and mating success in male Mediterranean fruit flies (Diptera: Tephritidae). Fla Entomol 85(1):150–155
Shelly TE, Edu J, Pahio E (2005) Influence of diet and methyl eugenol on the mating success of males of the Oriental fruit fly, Bactrocera dorsalis (Diptera: Tephritidae). Fla Entomol 88(3):307–313
Sivinski J, Burk T (1989) Reproductive and mating behaviour. In: Robinson AS, Hooper G (eds) Fruit flies, their biology, natural enemies and control, vol 3A. Elsevier, Amsterdam, pp 343–351
Suzuki Y, Koyama J (1980) Temporal aspects of mating behavior of the melon fly, Dacus cucurbitae Coquillett (Diptera: Tephritidae): a comparison between laboratory and wild strains. Appl Entomol Zool 15(3):215–224
Tan KH, Nishida R (1998) Ecological significance of male attractant in the defence and mating strategies of the fruit fly, Bactrocera papayae. Entomol Exper Appl 89:155–158
Tan KH, Tokushima I, Ono H, Nishida R (2010) Comparison of phenylpropanoid volatiles in male rectal gland after methyl eugenol consumption, and molecular phylogenetic relationship of four global pest fruit fly species: Bactrocera invadens, B. dorsalis, B. correcta and B. zonata. Chemoecology 21(1):25–33
Taylor PW, Yuval B (1999) Postcopulatory sexual selection in Mediterranean fruit flies: advantages for large and protein-fed males. Anim Behav 58:247–254
Tsiropoulos GJ (1992) Feeding and dietary requirements of the tephritid fruit flies. In: Anderson TE, Leppla NC (eds) Westview studies in insect biology: advances in insect rearing for research and pest management. Westview Press, Boulder, pp 93–118
Vargas RI, Stark JD, Nishida T (1990) Population dynamics, habitat preference, and seasonal distribution patterns of Oriental fruit fly and melon fly (Diptera: Tephritidae) in an agricultural area. Environ Entomol 19(6):1820–1828
Vijaysegaran S, Walter GH, Drew RAI (1997) Mouthpart structure, feeding mechanisms, and natural food sources of adult Bactrocera (Diptera: Tephritidae). Ann Entomol Soc Am 90(2):184–201
Virgilio M, Jordaens K, Verwimp C, White IM, De Meyer M (2015) Higher phylogeny of frugivorous flies (Diptera, Tephritidae, Dacini): localised partition conflicts and a novel generic classification. Molecular phylogenetics and evolution. doi:http://dx.doi.org/10.1016/j.ympev.2015.01.007
Warburg MS, Yuval B (1997) Circadian patterns of feeding and reproductive activities of Mediterranean fruit flies (Diptera: Tephritidae) on various hosts in Israel. Ann Entomol Soc Am 90(4):487–495
Williamson DL (1989) Oogenesis and spermatogenesis. In: Robinson AS, Hooper G (eds) Fruit flies: their biology, natural enemies and control, vol 3A, World crop pests. Elsevier, Amsterdam, pp 141–151
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2016 Springer International Publishing Switzerland
About this chapter
Cite this chapter
Manrakhan, A. (2016). Feeding and Mating Behaviour of African Fruit Flies. In: Ekesi, S., Mohamed, S., De Meyer, M. (eds) Fruit Fly Research and Development in Africa - Towards a Sustainable Management Strategy to Improve Horticulture. Springer, Cham. https://doi.org/10.1007/978-3-319-43226-7_8
Download citation
DOI: https://doi.org/10.1007/978-3-319-43226-7_8
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-43224-3
Online ISBN: 978-3-319-43226-7
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)