Anastrepha fraterculus (Wiedemann) is an insect pest commonly referred to as the South American fruit fly, which occurs from the southern United States to Argentina (Figure 1). Recent research has revealed this species to be a complex of at least eight cryptic species (yet unnamed), currently described as morphotypes, rather than a single biological species (Hernández-Ortiz et al. 2004, 2012, 2015).
Overall, the morphotypes in the complex are highly polyphagous with the potential to infest at least 110 host plants, including economically important fruit crops, such as guava, citrus, and apples (Zucchi 2016). However, depending on their distribution, each fly morphotype may have its own host range, which is still unknown. Uncertainties around the taxonomic status of the complex represent a huge challenge to plant protection authorities (Hendrichs et al. 2015). Because of the economic importance of this group of flies, it is crucial to know which species within the complex are indeed insect pests in order for plant protection authorities to establish quarantine barriers and prevent the introduction of pest species across countries and spread within each country.
The suspicion that Anastrepha fraterculus was a complex of multiple species was initially raised by Stone in 1942. Subsequently, the status of cryptic species within Anastrepha fraterculus was confirmed by multiple lines of evidences, such as isozymes (enzymes with different amino acid sequences that catalyze the same reactions), karyotypes, molecular cytogenetics, morphometry, chemical profiles, and behavioral studies (Morgante et al. 1980; Steck 1991; Selivon and Perondini 1998; Smith-Caldas et al. 2001; Hernández-Ortiz et al. 2004, 2012, 2015; Selivon et al. 2005; Canal et al. 2015; Vera et al. 2006; Cáceres et al. 2009; Rull et al. 2013; Devescovi et al. 2014; Vanicková et al. 2015; Dias et al. 2016). These cryptic species of the Anastrepha fraterculus complex are often called morphotypes, representing groups of similar organisms.
Currently, eight morphotypes are recognized in the Neotropics as part of the nominal species Anastrepha fraterculus: Andean, Brazilian-1, Brazilian-2, Brazilian-3, Ecuadorian, Mexican, Peruvian, and Venezuelan morphotypes (Hernández-Ortiz et al. 2004, 2012, 2015). Those eight morphotypes are related to three distinct and directly unrelated phenotypic lineages, Andean, Brazilian, and Meso-Caribbean, suggesting the non-monophyly of the Anastrepha fraterculus complex (Hernández-Ortiz et al. 2015). However, to date, all phenotypes from the Anastrepha fraterculus complex remain named Anastrepha fraterculus.
The following synonyms for Anastrepha fraterculus are listed by the Integrated Taxonomic Information System (ITIS 2017):
Dacus fraterculus (Wiedemann 1830) (original designation)
Tephritis mellea (Walker 1837)
Trypeta unicolor (Loew 1862)
Anthomyia frutalis (Weyenbergh 1874)
Anastrepha peruviana (Townsend 1913)
Anastrepha braziliensis (Greene 1934)
Anastrepha costarukmanii (Capoor 1954)
Anastrepha scholae (Capoor 1955)
Anastrepha pseudofraterculus (Capoor 1955)
Anastrepha lambayecae (Korytkowski & Ojeda 1968)
Species of the Anastrepha fraterculus complex are native to and most common in South America (Argentina, Brazil, Colombia, Ecuador, Peru, Venezuela), but can also be found in Central America (Guatemala, Panama) and North America (Mexico and the United States).
In general, the Anastrepha fraterculus eggs are creamy white, elongate, averaging 1.35 mm to 1.42 mm, have a conspicuous micropyle (opening for sperm entry) as well as a short chorionic extension in the egg apex, and are bluntly rounded in the egg end (Figure 2) (Murillo and Jirón 1994; Selivon and Perondini 1998). Eggs from different morphotypes within the Anastrepha fraterculus complex may differ in length, position of the micropyle, structure of papilla, pattern of sculpturing of the chorion, size, and number of aeropyles (respiratory channels) (Selivon et al. 1997; Selivon and Perondini 1998). Females deposit eggs inside the fruit through sclerotized ovipositors. The eggs hatch into larvae within two days.
In order for Anastrepha fraterculus larvae to reach maturity, they must molt three times. Usually, the first instar occurs from 1 to 3 days old, the second instar from 4 to 6 days old, and the third instar (Figure 3) from 7 to 12 days old (Nieuwenhove and Ovruski 2011). The average body length of the third instar ranges from 8.77 mm to 10.02 mm across morphotypes (Canal et al. 2015). Several larval traits can be used to identify the different morphotypes within the Anastrepha fraterculus complex, particularly mandible shape, as shown in Figure 4 (Canal et al. 2015).
The pupal stage is inert, but extremely important due to the intensive level of cellular differentiation. Pupae of the Anastrepha fraterculus complex are cylindrical and brownish, becoming darker when the insect is fully developed (Figure 5A), but still inside of the pupae as a pharate adult (Figure 5B). In nature, pupae can usually be found buried in the ground. Pupae hatch into adults within two to three weeks.
The adults in the Anastrepha fraterculus complex are colorful, usually yellowish brown, ranging from 12 to 14 mm. Although they are highly variable, aspects of wings, genitalia (particularly female genitalia), and thorax (mesonotum) constitute important characteristics to identify the species within the complex (Hernández-Ortiz et al. 2004, 2012, 2015) (Figure 6). According to Greene (1934), Anastrepha fraterculus adults can be distinguished from other species of the genus by the shape of the ovipositor (females) and wing pattern. There is no sexual dimorphism, except in the sexual characteristics and size (females are usually larger than males) (Figure 7). For instance, one of the characteristics exclusive to females is the ovipositor, which can measure 2 mm long.
Sexual behavior of these insects is complex, variable, and very interesting. Males from the Anastrepha fraterculus complex exhibit a lek mating system in which calling individuals get together on trees (usually under the leaves) to attract, court, and mate with receptive females (Morgante et al. 1983) (Figure 8).
Multiple signals, such as visual (symmetry of structures), acoustical (buzzing), and chemical (pheromones), are used by males to court females (Segura et al. 2007; Gomez-Cendra et al. 2011; Brizová et al. 2013; Dias et al. 2016) (Figure 9).
The species within the Anastrepha fraterculus complex infest at least 110 host plants, including several families, such as Anacardiaceae, Annonaceae, Myrtaceae, and many others (Zucchi 2016):
Anastrepha fraterculus is an important pest in South America. For instance, attack by females from the Brazilian-1 morphotype to apple orchards in southern Brazil can result in economic losses estimated at US $110 million (about 5% of the production or approximately 60,000 tons). In the same region, it is estimated that the losses in peaches can reach around 40% of the total production. Grapes can also be attacked, but the larvae cannot complete their development in grapes (Figure 10).
Besides pesticides and toxic baits, more environmental friendly techniques can be applied to reduce the population of insects from the Anastrepha fraterculus complex. One of those approaches is the Sterile Insect Technique (SIT), a method of control based on the reduction of fertility in a target population through the mating of sterile males (released from the laboratory) and fertile females (wild females from the target pest population) (Lance and McInnis 2005).
The successful implementation of SIT programs depends on correctly understanding species boundaries within the Anastrepha fraterculus complex because sexual compatibility is a requirement for the success of the technique (Hendrichs et al. 2015). In addition, biological control and mating disruption are other promising strategies that can be used in integrated pest management programs to control Anastrepha fraterculus populations.
The authors would like to thank Vicente Hernández-Ortiz, Instituto de Ecología AC—Mexico, Nelson Canal,Universidad del Tolima—Colombia, and Silvana Caravantes, International Atomic Energy Agency, for reviewing this article and contributing with helpful suggestions.
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