12 that Pose a Threat to Florida: B. carambolae and B. invadens

Aldo Malavasi,1 David Midgarden2 and Marc De Meyer3 1Medfly Rearing Facility – Moscamed Brasil, Juazeiro, Bahia, Brazil; 2USDA/APHIS, Guatemala City, Guatemala; 3Royal Museum for Central Africa, Tervuren, Belgium

12.1 Introduction point, (e.g., a backyard or garden tree) to adjacent areas and commercial groves. is one of the largest families of 2. High natural ability of dispersion. Some fru- Diptera and contains more than 500 genera and givorous fruit species are good flyers and can 4000 species, divided into three subfamilies disperse quickly and in large number when suita- (White and Elson-Harris, 1992; Norrbom et al., ble host trees are not available or are out of sea- 1999). Tephri­tidae pests are particularly impor- son. Well-fed adults – males and females – can fly tant because of their ability to invade regions large distances in search of reproductive and ovi- far from their native distribution. Introduced position sites or just for shelter. Experiments populations attack commercial fruit species, using the mark-release-recapture methodology which causes ­countries imp­orting fruit to have shown that either males or females can impose quarantine regulations (McPheron and travel many kilometers when the environment is Steck, 1996). These restrictions can inhibit the inadequate. In addition, being physically strong, sale of produce and the development or expan- the adults can be carried large distances by wind, sion of fruit production in the areas in which the hurricanes and masses of warm air, a fairly com- pest species are established. mon phenomenon in the atmosphere. Because of As their name implies, many members of such events, Japan keeps a trapping network in the family are frugivorous (feed on fruit), and the the southernmost island of its archipelago, close most important pest species have a high capacity to Taiwan. The distance between Taiwan and the to disperse to and colonize new areas. There are Yonaguni Island is 180 km. Japan is a fruit fly- three major characteristics that give Tephritidae free country as it had conducted a large eradica- a status of good potential invasive species: tion program some decades ago and Taiwan remains infested by some species of Bactrocera. 1. A large and rapid rate of population growth. Although the distance is large the Japanese This allows many Tephritid species to increase Ministry of Agriculture, Forestry and Fisheries their population size dramatically in a short trapping system occasionally captures Bactrocera period of time. In addition to the increase in den- adults in the islands close to the strait. sity, one or few gravid females can rapidly infest a 3. High anthropogenic dispersion. In fruit fly large number of hosts, expanding the geographic species, the egg and larval stages are necessarily distribution of the population from a single inside a fresh fruit. It is not always possible to

214 © CAB International 2013. Potential Invasive Pests of Agricultural Crops (ed. J. Peña) Bactrocera Species that Pose a Threat to Florida 215

distinguish when a fruit is infested with eggs or APHIS would carry out 100% of inspections at Los larvae of fruit fly. Some fruits, such as guavas Angeles International Airport for all arriving inter- (Psidium guajava L.), carambolas (Averrhoa caram- national flights for at least 1 day. The result was boa L.) and oranges (Citrus spp.) usually do not that in 24 h of full inspection, 73 fruit fly larvae reveal any external evidence that they are infested were intercepted. Considering this number for one unless in advanced ripe stage. Others, such as full year, it is estimated that more than 25,000 lar- apple Malus × domesticum, peaches Prunus persica vae are brought into California every year. L. and papayas Carica papaya L. show in early stages that they are infested. 12.2 Host Range and Colonization Due to these characteristics, many infested Ability fruits can be carried by people traveling large dis- tances. In some cultures (e.g., Latin America, South-East Asia and sub-Saharan Africa), it is Tephritids can be categorized by the number of quite common for people to carry fresh fruit as an fruit species that they attack. Monophagy refers easy source of food, since it is ready for consump- to attacks on a single fruit species; oligophagy tion at any time. Therefore, fruit infested with refers to attacks on different host plants belong- fruit fly eggs or larvae can travel very large dis- ing to the same plant family; polyphagous tances, because the cultural habit of people is infest many fruit species belonging to different associated with the modern transportation sys- families. Polyphagous flies have the potential to tem, allowing a large number of immature invade new territory when compared with mono- to move distances that would be impossible by or oligophagous flies. For example, the medfly, natural flight. This was the case for B. carambolae, C. capitata, is now a cosmopolitan species that the carambola fruit fly (CFF) (Fig. 12.1), intro- infests more than 300 host plants (Liquido et al., duced in Suriname in the north of South America 1991). The origin of medfly is sub-Saharan Africa in the early 1970s, and discussed in Section 12.3, and it was probably brought to Europe by naviga- as well as for the introduction of the invasive tors in the 17th or 18th centuries. fruit fly B. invadens into Africa. B. dorsalis, the Oriental fruit fly, and Many outbreaks of fruit flies follow a similar B. cucurbitae, the melon fruit fly, occur in the pattern. Every year, Mediterranean fruit fly or med- Hawai’ian Archipelago and are categorized as fly (Ceratitis capitata) and B. dorsalis, the oriental being polyphagous and oligophagous, respec- fruit fly (OFF) are brought into California, USA, by tively. The record of outbreaks of these two travelers bringing fruits from infested countries. ­species in California, USA, is around 10:1, giving Either returning US tourists or foreigners bringing a good measure of the relative aggressiveness of their preferred fruits to the USA are the most com- both species. mon sources of fruit fly detections in California. In 1993, it was suggested by a Scientific Advisory Panel of the Medfly Program in California that 12.3 Carambola Fruit Fly,

The carambola fruit fly (CFF) (Fig. 12.1), is a native of Indonesia, Malaysia and Thailand, and was first collected in South America in 1975 in Paramaribo, Suriname. The flies collected were not identified and CFF was not found again until 1981 when specimens were sent to the US Department of Agriculture and identified as Dacus dorsalis, the OFF. Although the OFF is one of the world’s most serious pests, no action was taken at that time. In 1986, the international community realized that the presence of OFF in Fig. 12.1 Bactrocera carambolae adults. Suriname would represent an important threat 216 A. Malavasi et al.

to the production and marketing of fruit through- small infestations of several B. dorsalis complex out tropical and subtropical America and the species have been found in Chile and the USA in Caribbean Basin Region. The fly was later found California and Florida, but action by respective to be a separate but closely related species from federal and state authorities prevented perma- the OFF, B. carambolae, the CFF. nent establishment. Unsurprisingly, there are direct ties between For much of the 20th century, the OFF has Suriname and the native area of CFF, as both been held responsible for enormous losses to Suriname and Indonesia are former colonies of fruit and vegetable crops throughout Asia and The Netherlands. Today the country has an esti- South-East Asia (Drew and Hancock, 1994). mated 450,000 inhabitants, 15% of whom are Doubts about the singularity of this species began descending from Indonesian colonizers from Java in the 1950s and 1960s (Hardy, 1969) and Drew in the early 20th century. Suriname maintains and Hancock (1994) have now identified 52 mor- strong ties with The Netherlands and > 90% of phologically and behaviorally similar species in trade and travel is with that country. During the what they term the B. dorsalis complex. Forty of colonial period and even after the independence these species are newly described. CFF is the in 1972, the Dutch KLM was the only airline to member of this complex (Drew, 1989) that has operate flights to and from Suriname. established in South America. When Drew and Hancock reviewed the tephritids in Asia, the OFF in Suriname was iden- tified as a species that occurred in Thailand and 12.3.2 Biology Indonesia and which attacked carambola, and was classified as B. carambolae. Mating By 1998 it was clear (Malavasi et al., 2000) that the route of CFF introduction into South There are two basic strategies that have been America was a traveler from Indonesia flying identified in tephritid mating (Prokopy, 1980; from Djakarta to Amsterdam and then from Shelly and Kaneshiro, 1991): (i) resource guard- Amsterdam to Paramaribo in a 12,000-km jour- ing, where the males stake out territory on a ney. The distance between South-East Asia resource such as a host fruit, and (ii) lekking, a (where CFF occurs naturally), and the north of grouping of males of a species for the purpose of South America, does not allow an introduction by attracting females (Sivinski and Burk, 1989; the regular maritime shipping lines. Drew, 1987). Females are attracted to these leks Lack of funding and coordination among the when they are physiologically prepared for mat- international community allowed the fly to ing. Mating in B. carambolae occurs just before expand its geographic distribution. CFF was first dark when the light intensity becomes less than found in French Guyana in the late 1980s and in 1000 lux (McInnis et al., 1999) and commonly Brazil in March, 1996. occurs on host plants. In Suriname, the first mat- ing by female B. carambolae usually takes place 18 days after emergence.

12.3.1 Taxonomic status Oviposition

The subfamily (Christenson and Foote, Females puncture the unripe, healthy fruit with 1960; Fletcher, 1987; White and Elson-Harris, their ovipositors, making cavities in which they 1992) are Old World in origin, principally tropical lay their eggs. Females can lay as many as 3000 Asia and Africa, and are represented by over 800 eggs over their lifetime in the laboratory, though species (including Bactrocera and Ceratitis spp.). some consider 1200–1500 to be the usual life- Until the population in the Guyanas region of time production under field conditions. South America was found (Hancock, 1990; van Sauers-Muller, 1991), no member of the B. dorsalis Adult feeding complex of fruit fly was permanently established in the New World (Bateman, 1972; Drew et al., B. dorsalis complex adults require a rich diet 1978; Vargas et al. 1990). Isolated specimens and that is high in amino acids, vitamins, minerals, Bactrocera Species that Pose a Threat to Florida 217

carbohydrates and water to survive and repro- the government of France. As a result of the pro- duce (Fletcher, 1987). Both males and females gram interruption, the CFF returned to its origi- must feed daily, and they forage on non-host as nal distribution and spread toward the north and well as host trees. Their diet has been observed to west in the Republic of Guyana and toward the include honeydew, plant exudates, extrafloral south and east in Amapa (Brazil), reaching nectaries, pollen, fruit juice, ripe fruits, microor- Macapa, the state capital. The present distribu- ganisms and bird droppings (Hendrichs and tion of CFF in South America includes all Hendrichs, 1990; Hendrichs and Prokopy, 1994). Suriname and French Guyana; west, central and Both sexes appear to respond equally well to pro- south of Guiana; and the State of Amapa in Brazil. tein baits, though hypothetically, females should The host list for the northern part of South be more attracted because of their need for pro- America is presented in Table 12.1. tein for egg production.

Life stages 12.3.3 Sampling and monitoring The life stages of B. carambolae are egg, larvae techniques (three instars), pupa and adult; they complete the cycle from egg to reproductive adult in 30–40 Most members of the Dacinae complex are days. Some experiments have shown that the strongly attracted to methyl eugenol, cue lure adult flies can remain alive as long as 125 days; [4-(p-acetoxypheyl)-2-butanone] and/or Wilson’s generally, however, lifespan varies with tempera- lure (which is the hydroxy derivative of cue-lure) ture and availability of food. In mountainous (Cunningham, 1989). These chemicals are termed regions of Hawai’i, for example, adult B. dorsalis pseudo- or parapheromones because they attract can live up to 1 year (Vargas et al., 1984). Once only one sex and are found in the environment the larvae hatch, they begin to feed and burrow rather than being produced by the opposite sex. into the pulp of the fruit. During development, A trap baited with methyl eugenol is the most fre- the larvae tunnel in the fruit and feed on the tis- quently used method of sampling for B. dorsalis sues and associated bacteria. When mature, lar- complex species. Both males and females can be vae leave the fruit and burrow several centimeters trapped using McPhail traps that are baited with into the soil, where they pupate. a protein diet and water. This method of sam- pling has advantages over the male-only traps, Host range and geographic distribution but the results are variable and highly dependent on rainfall and humidity. The host range and geographic distribution of Two types of traps are used to detect CFF in B. dorsalis complex is very broad, with more than South America: 150 varieties of fruit attacked throughout 1. Jackson traps, impregnated with a minimal ­tropical and subtropical Asia. The host range of amount of a methyl eugenol-malathion mixture B. dorsalis complex species in Malaysia is more and with a density of 10 traps per km2, and limited. van Sauers-Muller (1991) has reported checked biweekly to detect the presence of that the host range of the B. carambolae in male CFF. Suriname is very similar to that of CFF in 2. McPhail traps, baited with 300 ml of protein Indonesia and Malaysia. hydrolyzate food lure, placed with a density of A regional CFF eradication program was two units per km2, and checked every week to established in Paramaribo in 1997 with aim of determine the presence of both male and female eradicating the species from South America. In CFF, as well as other fruit flies. 3 years the distribution of CFF was reduced in 80% in Suriname, it was eradicated from Guiana Larvae surveys are performed upon fruits and kept the population only in Oiapoque in the collected from the host plants. Naked eye, micro- French–Brazilian border (Fig. 12.2). scopic inspection and pupae recovery of the fruits In 2002 when CFF was present in the urban are used to determine the presence of larvae, areas of French Guiana as well as in isolated agri- helping to qualify the state of infestation of a cultural areas, the program was terminated by given area. 218 A. Malavasi et al.

Venezuela Atlantic Ocean

Guyana

Suriname French Guiana

Boa Vista

Brazil

Fig. 12.2 Geographical distribution of Bactrocera carambolae in South America as of 2009.

12.3.4 Economic importance current trade patterns of the newly infested countries. Economic losses would occur due to a CFF is listed along with other species in the decrease in value of the produce of the fruit crops B. dorsalis complex on the list of quarantine that serve as host to the pest (caused by fruit insects for the European Economic Community damage and reduced yield); and export earnings (EPPO, 2011). The presence of CFF in Suriname, would be drastically affected, as fruit exports French Guiana, Guyana and Brazil represents a from newly infected countries would rejected or threat to the production and marketing of fruit subjected to restrictions in the international and vegetables throughout tropical and subtro­ markets. pical South and Central America and the An economic analysis conducted by Sanchez Caribbean. Lack of action to control CFF when (1998) showed that accumulated benefits on pro- it was first detected allowed it to become estab- duction over the twelve years projected a range lished as a pest of significant economic impor- from US$239 million to US$359 million, of which tance (Vo and Miller, 1995; Sanchez, 1998). Brazil obtains the larger share, US$194–291 mil- Discovery of this pest resulted in the imposition lion. Venezuela, Cuba and Colombia, in that of quarantine restrictions by importing countries order, also profit substantially from the program. in 1986, reducing the exports of fruits and vege- As expected, there is a close correlation between tables from Suriname and preventing the devel- the proportion of the value of fruit produced and opment and improvement of fruit exports in the value of the benefits obtained. Upon the com- Suriname and French Guiana. pletion and success of the eradication program, Spread of the CFF beyond its present benefits will also be derived from the avoidance ­territory would bring about dramatic changes in of export restrictions. Exports benefits are mark- the fruit production levels and value, and in the edly larger than those for production. They range Bactrocera Species that Pose a Threat to Florida 219

Table 12.1. Host list for the northern part of South America.

Hosts Scientific name English French

Primary Oxalidaceae Averrhoa carambola L. Carambola Carambole Myrtaceae Syzygium samarangense (Blume) Java apple Pomme rosa Merr. and Perry Secondary Anacardiaceae Mangifera indica L. Mango Mangue Malpighiaceae Malpighia punicifolia L. West indian cherry Cerises pays Myrtaceae Psidium guajava L. Guava Goyave Sapotaceae Manilkara achras (Mill.) Fosberg Sapodilla Sapotille Occasional Sapotaceae Chrysophyllum cainito L. Star apple Rhamnaceae Zizyphus mauritiana (jujuba) Lam. Indian jujube Jujube Myrtaceae Syzygium malaccense (L.) Merr. Malay apple Pomme de madagascar and Perry Pomme d’amour Myrtaceae Eugenia uniflora L. Surinam cherry Cerise du Suriname Rutaceae Citrus aurantium L. Sour orange Orange amere Citrus reticulata Blanco Mandarin Mandarine Citrus sinensis (L.) Osbeck Orange Orange Citrus paradisi Macfad. Grapefruit Pamplemousse Combretiaceae Terminalia catappa L. Tropical almond Anacardiaceae Anacardium occidentale L. Cashew Noix de cajou Spondias mombin L. Hogplum Clusiaceae Garcinia dulcis (Roxb.) Kurz Guttiferae Mammea americana L. Mamey apple

from a minimum of US$1604 million to a maxi- ­widespread distribution of bait stations impreg- mum of US$1848 million. The proportion nated with methyl eugenol and the insecticide between value of total fruit exports and benefits malathion. The lure attracts males to the stations derived from the eradication of the pest is again where they feed, ingest the insecticide and die high. Brazil receives the larger share of the quickly. For the technique to be effective, bait sta- ­benefits, which range from US$1192 million to tions must be evenly distributed throughout the US$1362 million in the twelve years encom- whole infested area. passed, while Cuba, exporting a high proportion Over a period of time, progressive reduction of its fruit production, ranks second with of the male fly population results in fewer and ­advantages ranging from US$262 million to fewer fertile females, until eventually the popula- US$315 million. tion reaches a very low level and may be com- pletely eradicated (Koyama et al., 1984). The technique is highly specific to a small number of 12.3.5 Control tactics fruit fly species, is environmentally benign and presents minimal health risks to human and ani- Two primary control tactics are used in the CFF mals. The male annihilation technique, MAT, is eradication campaign: male annihilation and foli- the basic method of eradication when an out- age baiting. break occurs in free areas. In South America two kinds of bait stations Male annihilation technique are used for MAT. One is a wooden fiber block that is soaked in the malathion methyl-eugenol CFF strongly responds to the male lure mixture; the other uses a 5–10 ml spot sprayed methyl eugenol. Male annihilation involves the onto a tree or electricity pole. In the spray, 220 A. Malavasi et al.

the methyl eugenol and insecticide are mixed Based on the above facts, the risk of intro- toget­her with Min-U-Gel® (ITC Industrials- duction of CFF into Florida is considered low. Floridin, Hunt Valley, Maryland). This is a pow- der that, when mixed in the right proportions, makes a type of jelly or grease. This gel lasts longer 12.4 Bactrocera invadens after being sprayed than the liquid by itself. More recently a combination of methyl-eugenol and The first specimens of B. invadens (Bi) (Fig. 12.3) spinosad, an organic insecticide, has been used to were found along the Kenyan coast during surveys control the outbreaks in areas free from Bactrocera. conducted in 2003 within the framework of the African Fruit Fly Initiative (an international pro- Protein baiting technique gram co-ordinated by the International Centre of Protein (hydrolyzed yeast protein), mixed with Physiology and Ecology, Nairobi, Kenya) the insecticide malathion or the new generation (Lux et al., 2003). A few months later, the species of insecticides (spinosad) is used to spray the foli- was found in Tanzania (Mwatawala et al., 2004), age, preferably of fruiting host plants. The protein and was subsequently reported from countries acts as a food attractant to both males and throughout the African continent. Although the females, particularly immature females which genus Bactrocera occurs in Africa, the indigenous need protein to develop eggs. Flies feed on the species belong to different subgenera and Bi does protein, ingest the insecticide and die quickly. All not have any close relatives in this zoogeographi- fruit fly species, not just CFF, are attracted to pro- cal region (White, 2006). Taxonomists recognized tein baits. Where protein baiting and male annihi- the specimens as being an alien species, belong- lation can be carried out at the same time in ing to the B. dorsalis complex (Lux et al., 2003). infested areas, control of the CFF can be achieved Drew et al. (2005) concluded that the African more quickly and with greater efficiency. Where specimens belonged to a hitherto undescribed trap catches or larva surveys in fruit indicate a sig- species and that identical specimens were col- nificant localized breeding population (i.e. a ‘hot lected in Sri Lanka. They described the new spot’), a protein-bait strategy is also employed. ­species as B. invadens. Although previously unknown and appar- ently of no economic significance in its region of origin, Bi has made a tremendous impact in Africa 12.3.6 Potential risk of introduction into Florida

To make an assessment on the risk of introduc- tion, the following points should be considered: •• CFF has already been present in the north of South America for almost 40 years. •• There are no records of CFF presence in Venezuela and the Caribbean. •• The control program carried out in Brazil, if not achieving eradication, has at least suc- cessfully kept the species in a containment area. •• There is no evidence of CFF presence in the Amazon forest. •• Few new hosts have been reported after the first wave of invasion. •• There are no direct flights between Paramaribo and Miami. •• Agricultural products exported from Fig. 12.3 Bactrocera invadens (copyright R.S. Suriname to the USA are negligible. Copeland, reproduced by permission). Bactrocera Species that Pose a Threat to Florida 221

since it was first introduced. The species has dem- ­confirmed that the former belongs to the native onstrated an unprecedented dispersal rate and is range (Khamis et al., 2009). The pathway by currently considered one of the major pest spe- which Bi entered Africa is not clear, nor is there cies, especially for the horticultural industry of any definite evidence that eastern Africa was the tropical fruits such as mangoes. It is also a strong original port of entry. The East African coast has competitor displacing indigenous pest species of historical ties with the Middle East and Central fleshy fruits, mainly representatives of the genus Asia, dating back several centuries (Gilbert, Ceratitis. It further aggravates the problems that 2004) when there was a thriving trading busi- local growers are facing because of both the indig- ness with sailing boats (dhows) transporting enous pests and the exotic fruit flies such as merchandise between the regions. However, no B. cucurbitae and B. zonata, which were introduced specimens of Bi could be found in any historical to the continent earlier. Because of its economic collection from the 20th century or before. significance and invasive behavior, it is consid- Between 1999 and 2000, the African Fruit Fly ered a potential threat for many other regions Initiative occasionally deployed methyl eugenol with significant fruit-producing economies. traps in Kenya, Tanzania and Uganda (Lux et al., 2003) and an intensive fruit sampling and rear- ing program ran in Kenya between 1999 and 12.4.1 Taxonomic status 2003 (Copeland et al., 2006). No specimens were detected in that period. Similarly, fruit fly sur- veys were conducted in different countries in B. invadens belongs to the subgenus Bactrocera s.s. western Africa from 2000 onwards (Vayssières (White, 2006) and is very similar to B. dorsalis and et al., 2005) but the species was not reported. related taxa. At first, it was identified as being an All this seems to indicate that it was not present aberrant form of B. dorsalis (Lux et al., 2003), but (or at very low abundance) prior to 2003. Since was later recognized as a distinct species (Drew its first detection, however, numbers have risen et al., 2005) belonging to the B. dorsalis complex sharply. In addition, within a timespan of 2 years as described by Drew and Hancock (1994). (February 2003–January 2005), the species was Specimens of Bi, however, demonstrate a high recorded in very high numbers in no fewer than variability in thoracic and abdominal patterns 11 countries ranging from Senegal in the west to (Drew et al., 2005), and morphological differences Ethiopia and Tanzania in the east (Drew et al., to unambiguously differentiate it from allied spe- 2005; De Meyer and White, 2008) (Fig. 12.4). cies are minor (White, 2006; Drew et al., 2008) Currently, it is known from more than 20 coun- and not easy to recognize by non-specialists. tries throughout the continent, as well as from Recent studies regarding hybridization (Jessup Madagascar and the Comoro Islands in the et al., 2010), nucleotide sequences of mitochon- Indian Ocean. drial COI (cytochrome oxidase region I), morpho- Most remarkable is the fact that, only metrics (Schutze et al., 2012) and rectal volatiles 9 months after its first detection in Kenya, (Tan et al., 2010) do not provide any evidence of specimens were collected in Nigeria in western distinct separation between particular species of Africa (Umeh et al., 2008). It is unlikely that the complex, leading to assump- the species dispersed by natural means over tions that Bi and other species within the complex this distance in such a short time. Khamis et al. could be identical to B. dorsalis (Tan et al., 2010; (2009) showed that the population subdivis­ Schutze et al., 2012). However, the extreme com- ion in Africa is not on a geographical basis plexity of species boundaries within the B. dorsalis but that three distinct African clusters are species complex and the actual taxonomic status apparent, which can be interpreted as different of Bi should be investigated further. invasion bursts or outbreaks. One of these ­originated from Nigeria. It is, therefore, not unlikely that the Nigerian detection represents 12.4.2 Invasion history an introduction event independent of those in East Africa. However, more studies are required Bi has an Asian origin, and a genetic study of to resolve the invasion history of the species in Sri Lankan and African populations have Africa further. 222 A. Malavasi et al.

Fig. 12.4 Distribution of Bactrocera invadens.

12.4.3 Distribution southernmost part of Africa. The occurrence southwards is more restricted, with data from the Knowledge of the distribution of Bi in its region northern parts of Namibia, Botswana and of origin is fragmentary. The species seems to be Mozambique. In the latter country, the spread of widespread in Sri Lanka (De Meyer et al., 2010) the fly has been surveyed since the first record in but records from other parts of the Indian sub- 2007 (Correia et al., 2008), using an extensive continent are rare. Some specimens from south- network of methyl eugenol-baited traps along the east India were recognized as Bi (Sithanantham major transportation routes and in horticultural et al., 2006), while a few specimens were found areas (Cugala et al., 2011). It is abundant and per- among a large series of B. dorsalis from Bhutan manently established in the northern provinces, (Drew et al., 2007). Again, confusion with other while still absent from the south. The area roughly species of the B. dorsalis complex might disturb between the Zambezi and Save Rivers has so far a correct observation of the distribution pattern shown irregular occurrences of the fly, but the of Bi. Several closely related species, such as number of interceptions has been increasing in B. kandiensis, B. dorsalis s.s., or B. rubigina occur in this region over the last years. It is not clear the region, and a more in-depth study and survey whether these records reflect true natural disper- should be conducted in order to establish the sal of the fly, or if they are the result of (increased) exact range of Bi in Central Asia. accidental introductions by human activities. Because of the absence of congeners (species De Meyer et al. (2010) developed an ecologi- within the genus Bactrocera) in Africa, the distri- cal niche model, based on associations between bution of the species is well known there. As known occurrence data and a set of environmen- mentioned earlier, the species became widespread tal variables. The results of this modeling suggest throughout the continent in a fairly short time. It that Bi prefers hot and humid environments with is currently officially reported from most coun- high – although not necessarily continuous – tries south of the Sahara, but excluding the annual precipitation. This preference is indirectly Bactrocera Species that Pose a Threat to Florida 223

supported by the relative abundance of Bi along indices of Citrus were also observed in Kenya altitudinal transects. Observations in eastern (Rwomushana et al., 2008). Host preference, Africa have shown that its presence is lower at therefore, seems to be influenced by factors other higher elevations that often also have high humid- than just presence or absence of the host. ity but lower temperatures (Ekesi et al., 2006; Mwatawala et al., 2006a). The majority of known occurrence sites of Bi in Africa coincides with the 12.4.5 Biology predicted areas. Those sites outside the predicted areas might be due to anthropogenic microcli- Development mates, such as the observed high abundance in irrigated regions along the Nile River in Sudan. Ekesi et al. (2006) provide data on the ­development of Bi immature stages on a yeast–­ carrot-based artificial diet at 28°C. They showed 12.4.4 Host list that immature development takes on average 25 days (egg incubation 1.2 d; larval stage 11.1 d; Bi is a truly polyphagous species, attacking a wide pupa to adult 12.4 d) with 55% survival, and the variety of fleshy fruits. All known host data origi- mean generation time is 31 days. Life expectancy nate from rearing experiments in Africa. No host at pupal eclosion is lower for females (75.1 d) records are available from the area of origin. An than for males (86.4 d). Females were observed to overview of all host records reported so far can be have a net fertility of 608 eggs. A further study by found on the Invasive Fruit Fly Pests in Africa Rwomushana et al. (2008) showed that develop- websitei which is updated at regular intervals. So mental times for all stages is affected by tempera- far, 65 species belonging to 26 families have been ture, with the shortest at 30°C (17.76 d) gradually listed. This includes most tropical, subtropical becoming longer under colder temperatures and temperate climate fruits that are grown com- (75.74 d at 15°C). Lower developmental thresh- mercially in Africa, but also a number of orna- olds, based on linear regression equations, were mental exotics and wild indigenous fruits. In between 8.7 and 9.4°C for the different immature addition, some records are known from plants life stages, while 35°C proved to be the higher categorized as vegetables, such as solanaceous threshold for adult emergence. and cucurbitaceous crops. With regard to incidence and infestation Temporal and spatial abundance rates, the impact of Bi on the different hosts is very varied. Some hosts seem to be infested pref- Bi shows distinct seasonal fluctuations in abun- erentially while others are only rarely attacked. dance. Mwatawala et al. (2006b) and Vayssières Also, the number of emerging flies per unit of et al. (2005, 2009) demonstrated that a distinct fruit (e.g. weight) can differ widely. Mwatawala peak period coincides with the mango fruiting et al. (2006b, 2009) present an in-depth study on season. In both regions, this also marks the onset the host range and utilization of Bi and co-­ of the rainy season (unimodal in Benin, bimodal occurring fruit flies in Tanzania, while Vayssières in Central Tanzania, with the mango fruiting sea- et al. (2009) present extensive data for Benin in son falling in the short rainy season). In Tanzania, western Africa. Both studies show a high prefer- a second peak occurs with the onset of the guava ence of Bi for the following hosts (only those fruiting season. However, the relative abundance occurring in both areas): mango, guava and tropi- strongly declines along an altitudinal transect, cal almond. Other commercial crops such as and there are indications that presence at higher ­avocado, banana or carambola (starfruit) are non- elevations is the result of dispersal from lower preferential hosts with limited infestation in regions during high abundance. both regions. On the other hand, while most cit- rus species show relatively low infestation rates Interspecific competition in Tanzania and the drier Sudanian areas of Benin, they are considered more preferential Duyck et al. (2004) state that life-history strate- hosts in the Guinean area of Benin (Vayssières gies play a role in determining the competitive et al., 2009). Similar differences in infestation interactions between invasive species and the 224 A. Malavasi et al.

pre-established species. Many invasive Bactrocera world, mainly in tropical areas, are at least species, including Bi, demonstrate K traits, such ­climatically suitable for the survival of Bi. Other as large adult size, that seem to favor both exploi- regions, therefore, are anxious to avoid the tation and interference competition. The com- introduction of this invasive pest in their petitive displacement of other fruit flies by regions. Several alerts have been issued, such as Bactrocera species has been demonstrated in a the quarantine order by the USA,ii or the A1 list- number of cases (Duyck et al., 2004, 2007). In ing by EPPO. EPPO also developed a pest risk Kenya, evidence for such displacement of the analysis to evaluate the different pathways indigenous mango fruit fly (Ceratitis cosyra) by Bi along which Bi can enter the region. Because of has been shown by Ekesi et al. (2009) and the similar environmental conditions with areas Rwomushana et al. (2009). This plays an impor- where Bi occurs in Africa, the Ministry of tant role in evaluating the potential impact of Agriculture of Brazil has set up a detection sys- Bi in new areas. tem in those Brazilian cities with direct flights from infested areas in Africa. Florida is potentially at risk. GARP, one of 12.4.6 Control tactics the ecological niche models developed by De Meyer et al. (2010), indicates southern Florida as suitable for establishment of the pest, with regard As with several other species of the B. dorsalis to prevailing climate conditions only. Considering species complex, Bi is also strongly attracted to that Bi is attracted to methyl eugenol, the trap- methyl eugenol. This parapheromone is the opti- ping system in the state will allow early detection mal tool for surveillance and monitoring activi- of any invasion. It is considered that the eradica- ties, but only attracts males. Both sexes can be tion plan developed for B. dorsalis will also be trapped using protein bait or other food baits applicable for Bi. such as three-components lure, but the attrac- tiveness is much lower than methyl eugenol, as demonstrated by Mwatawala et al. (2006a). The Notes use of methyl eugenol has shown its effectiveness in surveillance programs in South Africa, where it i www.africamuseum.be/fruitfly/AfroAsia.htm, is intensively used for early detection (Venter accessed 26 July 2012. et al., 2010). ii www.aphis.usda.gov/import_export/plants/plant_ Control strategies are very similar to those imports, accessed 28 July 2012. outlined earlier in this article for the Carambola fruit fly. MAT, in combination with protein bait spraying and other possible eradication actions such as fruit stripping, are considered the appro- References priate plan of action. South Africa has developed an action plan along these lines to combat any Bateman, M.A. (1972) The ecology of fruit flies. possible detection (Manrakhan et al., 2010). Annual Review of Entomology 12, 493–519. Christenson, L.D. and Foote, R.H. (1960) Biology of fruit flies. Annual Review of Entomology 5, 171–192. 12.4.7 Economic importance Copeland, R.C., Wharton, R.A., Luke, Q., De Meyer, M., Lux, S., Zenz, N., Machera, P. et al. (2006) The economic impact of Bi in Africa cannot be Geographic distribution, host fruit, and parasi- underestimated. Although the horticultural toids of African fruit fly pests Ceratitis anonae, industry had already suffered considerable Ceratitis cosyra, Ceratitis fasciventris, and Ceratitis rosa (Diptera: Tephritidae) in Kenya. losses due to indigenous fruit fly pests such as Annals of the Entomological Society of medfly (Ceratitis capitata), mango fruit fly America 99, 262–278. (C. cosyra) and Natal fruit fly (C. rosa), the prob- Correia, A.R.I., Rega, J.M. and Olmi, M. (2008) lem has become dramatic since Bi spread A pest of significant economic importance throughout the continent. De Meyer et al. detected for the first time in Mozambique: (2010) showed that many other parts of the Bactrocera invadens Drew, Tsuruta & White Bactrocera Species that Pose a Threat to Florida 225

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