Anastrepha species ( Diptera : Tephritidae ) , their host plants and parasitoids ( Hymenoptera ) in the state of Roraima , Brazil : state of the art

The aim of this review was to update the available information on Anastrepha species in the state of Roraima, Brazil, with emphasis on distribution, host plants and parasitoids. In total, 25 species of Anastrepha and 27 host plant species have been recorded to date in Roraima. Anastrepha striata and A. obliqua are widely distributed in the state. Anastrepha obliqua is the most polyphagous species, where it is associated with 13 hosts. Six species of parasitoids of Anastrepha have been reported in Roraima. Of these, Doryctobracon areolatus is the most abundant and has been associated with the largest number of Anastrepha species.


Introduction
The state of Roraima is located in the extreme north of the Brazilian Amazon, occupying an area of 224,299 km 2 between latitudes 5°16ʼN and 1°25ʼS; and longitudes 58°55ʼW and 64°48ʼW (IBGE, 2010a), corresponding to 2.6% of the Brazilian territory and 5.3% of the Amazon biome (FUNCATE, 2006).It is the Brazilian state with the smallest number of municipalities (15), although some of them cover large territories, such as the municipality of Caracaraí (47,411 km 2 ).Roraima has international borders with Venezuela and Guyana.Within Brazil, it borders the states of Amazonas and Pará.
In Roraima, there are three climate groups according to the Köppen classiication system: Aw, Af, and Am.
The Aw climate region corresponds to the savannas in central-eastern and northeastern Roraima.This type of climate is characterized by a marked, well-deined dry period, which is between the months of December and March.Mean annual rainfall in this region is 1,655 ± 408 mm.Approximately 9% of this total occurs at the peak of the dry season (December-March), and 70% at the peak of the rainy season (May-August) (BARBOSA, 1997;ARAÚJO et al., 2001).The Af climate is observed in the forest systems of the extreme south and northwest parts of the state.These regions are predominantly covered by dense ombrophilous forests, with mean annual rainfall exceeding 2,000 mm.The Am type climate is found in the contiguous forests and grassland regions of the state, where mean annual rainfall ranges from 1,700 to 2,000 mm.] Fruit farming is a very important source of revenue and employment in Roraima.The main fruit crops are banana, papaya, orange, lime, pineapple, melon and watermelon (IBGE, 2010b).In addition to these crops, a wide variety of native and exotic fruit trees can be found in home orchards, many of which are known to be or are potential hosts of fruit lies (MARSARO JÚNIOR et al., 2011b).
Fruit lies (Diptera: Tephritidae) are among the most important pest species in the world, due to their direct economic impact and the severe quarantine restrictions enforced by many countries to prevent their entry into their territories (AlUJA, 1994;AlUJA;MANGAN, 2008).The family Tephritidae is composed of approximately 4,541 valid species grouped into 493 genera (NORRBOM, 2010).Anastrepha Schiner is considered the most economically relevant fruit ly genus in tropical America, with over 250 described species and the highest recorded number of pest species (NORRBOM, 2004a;2004b;NORRBOM et al., 2014).To date, 120 species of Anastrepha have been reported in Brazil (ZUCCHI, 2008).Six of these are particularly important from an economic standpoint: Anastrepha striata Schiner, A. obliqua (Macquart), A. fraterculus (Wiedemann), A. grandis (Macquart), A. pseudoparallela (loew), and A. zenildae Zucchi (URAMOTO;ZUCCHI, 2009).
The irst survey of Anastrepha species in Roraima was conducted in the 1990s by Rafael (1991), who recorded three species at the time: A. leptozona Hendel, A. hamata (loew), and A. serpentina (Wiedemann).In that study, the only reported host plant was Pouteria caimito, hosting A. leptozona.No parasitoid species were reported.In 2000, Malavasi andZucchi (2000) published a book gathering all the available information on fruit lies in Brazil.In the chapter dedicated to northern Brazil, Silva and Ronchi-Teles (2000) reported that eight species of Anastrepha, only i ve species of host plants and no species of parasitoids had been registered in Roraima.In addition, only localized collection efforts had been conducted in the state, covering only four municipalities.
Starting in 2007, through the project known as the Amazonian Network for Research on Fruit Flies, coordinated and funded by the Brazilian Agricultural Research Corporation (Embrapa), a new series of surveys was initiated with the goal of investigating the diversity of Anastrepha species, as well as their host plants and parasitoids in Roraima.When the project was completed, all available information on fruit l ies in the Brazilian Amazon was consolidated in a book (SIlVA et al., 2011b).In that work, Marsaro Júnior et al. (2011b) updated the number of Anastrepha species recorded in Roraima ( 17).New studies conducted after that time (MARSARO JÚNIOR et al., 2011a;2012;2013a;2013b;ZUCCHI et al., 2011a;ADAIME et al., 2012;lIMA et al., 2012;TRASSATO et al., 2015) expanded the existing knowledge about fruit l ies in Roraima, where 25 species of Anastrepha, 27 species of host plants and six species of parasitoids have been reported to date.
The aim of this review was to update current knowledge of Anastrepha species in Roraima, with emphasis on their distribution, host plants and parasitoids.

Anastrepha species richness and distribution
As shown in Figure 1, the number of Anastrepha species recorded in Roraima since the earliest studies by Rafael (1991) has risen from three in 1991 to 25 today, with the recent publications by lima et al. (2012) andMarsaro Júnior et al. (2013a;2013b).This leap in the number of reported species was unquestionably the result of the surveys conducted during the Amazonian Network for Research on Fruit Flies project, initiated in 2007.
Anastrepha striata is the most widely distributed species in Roraima (Table 1).This species is very well adapted to conditions found in the state and can be collected both at low altitudes -such as the state capital

Boa Vista (approximately 100 m above sea level [masl])
-and at higher elevations, such as Pacaraima, located above 900 masl (MARSARO JÚNIOR et al., 2012).According to Aluja (1994), the level of dominance of a species is inluenced by ecological bases (host plant, richness and diversity) and by altitudinal gradients.In Mexico, for example, in mango orchards at 1,100 masl, 30% of all collected individuals were A. ludens (loew), out of 14 species captured in traps.At lower altitudes (680 m), among 12 captured species, only 4% of individuals were A. ludens.Therefore, given that A. striata is well adapted to different altitudes in Roraima and provided that host plants are available, this species may be present in every municipality in the state, and has indeed been reported in 13 of 14 municipalities already sampled.Anastrepha striata is also the most widely distributed species in the state of Amapá (SIlVA et al., 2011a) and is present in every state of the Brazilian Amazon (ZUCCHI et al., 2011b).
Anastrepha obliqua, also widely distributed in Roraima, has been reported in 12 municipalities within the state (Table 1).This distribution can be explained by the polyphagous habits of the species, whose main hosts are fruits of Anacardiaceae and Myrtaceae, which are very common in Roraima, as shown by Marsaro Júnior et al. (2011a).Anastrepha obliqua is also present in every  Anastrepha species, their host plants and parasitoids state within the area known as the "Legal Amazon."It is able to adapt to a variety of biomes and occurs practically throughout Brazil, except in the state of Sergipe, where it has not been reported to date (ZUCCHI et al., 2011b).
Fruit fly surveys have been conducted in the central (Boa Vista and neighboring municipalities), northern, northeastern and southern regions of Roraima (Figure 2).The municipalities with the highest species richness are those where surveying has been most intense and frequent, including Boa Vista, Amajari and Pacaraima, whereas the lowest richness levels were found at locations where only localized collection efforts were made (Table 1; Figure 2).Figure 2 shows that surveys have been performed in 14 out of 15 municipalities in Roraima, and new information has recently been obtained regarding the distribution of Anastrepha species in municipalities located in the southern part of the state, expanding their known distribution ranges.However, for an accurate view of Anastrepha distribution and richness throughout the state of Roraima, new surveys should be completed in the less studied municipalities, and particularly in Alto Alegre, which has not been sampled to date.
The state capital Boa Vista has the highest known richness of Anastrepha (17 species), followed by Amajari ( 14) and Pacaraima (11).The lowest richness levels are found in Caroebe and Uiramutã, with a single species each (Table 1).The high richness of Anastrepha species observed in Boa Vista is mainly due to the fact that the majority of surveys conducted in Roraima, with fruit sampling and McPhail traps, have focused mainly on the capital, as shown by the works of Marsaro Júnior et al. (2011a;2012;2013a;2013b) andlima et al. (2012).
The number of Anastrepha species in Boa Vista is likely to be even higher; the faunistic analysis conducted in this municipality by Marsaro Júnior et al. ( 2012) showed that the observed species richness was lower than expected, since the cumulative species curves indicated moderate growth, suggesting that the collection effort was not suficient to produce an accurate description of species richness in Boa Vista.This shows that surveying should be continued in all municipalities in Roraima, to improve the accuracy of available data on Anastrepha species richness throughout the state.

Host plants of Anastrepha
The state of Roraima features a wide diversity of native and exotic fruit trees, many of which are known to be or are potential hosts of Anastrepha (MARSARO JÚNIOR et al., 2011b).To date, 27 plant species have been reported as hosts of Anastrepha spp., across 12 botanical families (Table 2).
Families Myrtaceae and Anacardiaceae account for over 50% of all known hosts of Anastrepha in Roraima (Figure 3).Anastrepha obliqua is the most polyphagous Anastrepha, having been associated with 13 host plants from four botanical families (Table 2).However, Anastrepha obliqua has a marked preference for Anacardiaceae and Myrtaceae hosts, and the main host plant of this species is Spondias spp.(MARSARO JÚNIOR et al., 2011a;2011b).In Roraima, S. mombin has shown one of the highest rates of infestation by A. obliqua, with up to 345 puparia/kg of fruit (MARSARO JÚNIOR et al., 2011a).the most abundant fruit ly in the state of Tocantins (BOMFIM et al., 2007) and the most relevant in the state of Amazonas (RONCHI-TElES;SIlVA, 2005).
Anastrepha striata is the second most polyphagous Anastrepha species in Roraima, having been associated with 10 host plant species from ive botanical families (Table 2).However, it has a strong preference for Myrtaceae host plants, with Psidium guajava as its main host (MARSARO JÚNIOR et al., 2011a;2013b).The same has been observed in the state of Amapá (SIlVA et al., 2011a;JESUS-BARROS et al., 2012).Anastrepha striata has been considered dominant in Bonim and Pacaraima and super-dominant in Boa Vista (MARSARO JÚNIOR et al., 2012).In the state of Amapá, A. striata is believed to be the most polyphagous and widely distributed fruit ly and, therefore, one of the top three in terms of economic importance (DEUS; ADAIME, 2013).This means that, in terms of distribution, dominance and polyphagy, A. obliqua and A. striata are the most economically important Anastrepha species in the state of Roraima.Some species of Anastrepha can be classii ed as specialists, infesting one specii c host.One example is A. manihoti, whose larvae develop exclusively in fruits of Manihot esculenta (Euphorbiaceae) (Table 2).As a result, A. manihoti has a more limited distribution and has been reported only at locations where fruits of its only known host are present.To date in the Brazilian Amazon, A. manihoti has been observed only in the states of Amazonas and Rondônia (RONCHI-TElES, 2000) and Roraima (MARSARO JÚNIOR et al., 2011b).
Polyphagous species are more widely distributed than specialist ones and they often show niche overlap, with multiple species using the same host plant (MAlAVASI; MORGANTE, 1980).This strategy can be viewed in Table 2, which shows multiple species of Anastrepha occurring on the same host plants.
Eleven species of Anastrepha in Roraima have had no hosts reported thus far (Table 3).Six of these species are exclusive to the Amazon and one of them, A. zucchii, only occurs in the state of Roraima (ZUCCHI et al., 2011b).In other states in the Amazon region, hosts of A. atrigona, A. fractura, A. fraterculus and A. turpiniae have been known for some time, as listed by Zucchi et al. (2011b) and shown in Dutra et al. (2013).But for some other species, such as A. l avipennis, a host plant in the Amazon region (Pouteria glomerata, Sapotaceae) has been reported only recently (CORRÊA et al., 2011).  . ethalea, A. hamata, A. longicauda, A. rafaeli, A. zernyi, and A. zucchii, have no known hosts in the Brazilian Amazon (ZUCCHI, 2008;ZUCCHI et al., 2011b).To identify the host plants of these Anastrepha species, new studies should therefore be conducted not only in Roraima, but across the entire Brazilian Amazon.Some hosts of Anastrepha in Roraima are exotic species (Table 2) grown mainly in urban areas.The most extensive areas of the Amazon Forest in Roraima, with their huge diversity of native fruits, are found mostly in the southern part of the state, where few fruit ly surveys have been conducted.Studies conducted in this region could lead to new reports of Anastrepha species and their host plants.We therefore suggest that any new surveys of Anastrepha in Roraima should focus on this poorly studied part of the state.

Natural enemies of Anastrepha spp.
The irst study into the diversity of parasitoids of Anastrepha spp. in Roraima was conducted by Ronchi-Teles (2000), who reported two species: Doryctobracon areolatus (Szépligeti) and Doryctobracon brasiliensis (Szépligeti).A number of additional studies were subsequently conducted and new species were reported, making up a current total of six known parasitoid species (Table 4).Doryctobracon areolatus is the most abundant parasitoid of Anastrepha and has been associated with the highest number of Anastrepha species (eight) (Table 4).Doryctobracon crawfordi (Viereck), which has been reported in Brazil only in the states of Amapá and Roraima so far (ZUCCHI et al., 2011a), has been associated with two species in Roraima, namely A. coronilli and A. serpentina (Table 4).
With regard to D. brasiliensis (Szépligeti), reported in Roraima by Ronchi-Teles (2000), additional studies are needed to conirm if this species is associated with A. leptozona or A. serpentina, since these two fruit lies emerged from the same host fruit.The only known parasitoid of Anastrepha belonging to the family Figitidae, Aganaspis pelleranoi (Brèthes), is associated with A. obliqua (Table 4).
The highest rate of parasitism of Anastrepha observed in Roraima (62.3%) was seen in fruits of the native plant Loreya mespiloides (Melastomataceae) (MARSARO JÚNIOR et al., 2010).That study showed the importance of native plants in preserving and multiplying the populations of these agents of biological control of fruit lies, and further highlights the need for conserving the native plant species of the Amazon, the natural habitat of these parasitoids.
Predators, especially spiders, are also important natural enemies of fruit lies in Roraima, as reported by Marsaro Júnior et al. (2011b), who observed the predation of A. amita by the spider Phiale crocea (Salticidae).
Therefore, in light of the sparseness of studies conducted in southern Roraima, more intensive surveys conducted in that region are likely to report new parasitoids or predators of Anastrepha, or may even reveal new species of Anastrepha and their natural enemies that are yet to be discovered, described and preserved.

Final considerations
Knowledge about fruit lies in the state of Roraima has seen major progress since the initial study on the topic was published in the early 1990s.The number of reported Anastrepha species in the state jumped from three to 25, the number of parasitoids from zero to six, and the number of host fruits from one to 27.Species distribution across the state is also better known now, with information currently available for 14 of the 15 municipalities of Roraima.
As previously mentioned, the state of Roraima features multiple types of plant formations (savannas, Amazon Forest and grasslands) and has borders with two Brazilian states (Amazonas and Pará) and two South American countries (Venezuela and Guyana).
This geographic area as a whole is the site of reports of fruit lies of quarantine importance, a large number of preserved areas (conservation areas and indigenous reserves) and a wide variety of native and exotic fruit trees.Due to these peculiar characteristics, Roraima has major potential for studies on the bioecology of fruit lies, and the research conducted to date is still insuficient to fully express the existing richness of Anastrepha, parasitoids and host plants in the state.Fruit fly surveying should therefore continue (in already studied areas) and be extended to unsurveyed areas, to more accurately characterize the richness and distribution of fruit ly species, their host plants and parasitoids in the state of Roraima.
On the other hand, to ensure the success of additional fruit ly surveys in Roraima, human resources must be trained to perform these activities in the different plant formations found in the state.Access to these plant formations is dificult due to lack of supporting infrastructure, inadequate conservation and absence of roads in the interior of Roraima, not to mention the high volume of rain from May to August, which makes certain regions inaccessible in that period.However, these dificulties should not discourage fruit ly surveying in Roraima, especially in less studied areas.Creativity, effort and perseverance in inding solutions to overcome these access impediments will be rewarded through the wealth of knowledge that is waiting to be revealed in these regions of the state.
In recent years, several municipalities in Roraima have invested in the production of native and exotic fruits for local consumption and for distribution to other Brazilian states.This creates a need for studies oriented towards a more adequate management of tephritids that infest fruits of commercial interest.
Therefore, due to the importance of fruit farming for Roraima and the damages caused by tephritids to fruits in the state, further studies on fruit lies in the region are needed.

FIGURE 1 :
FIGURE 1: Cumulative curve of number of Anastrepha species recorded in Roraima, considering reports up to and including the respective years shown.

FIGURE 2 :
FIGURE 2: Number of Anastrepha species recorded in municipalities of the state of Roraima.
In a report by Marsaro Júnior et al. (2012), Anastrepha obliqua was considered a dominant species in the municipalities of Bonim and Pacaraima, and super-dominant in Boa Vista.It is also believed to be A. L. Marsaro Júnior et al.

FIGURE 3 :
FIGURE 3: Number of hosts of Anastrepha in each botanical family and respective percentages in relation to total number of hosts.

TABlE 1 :
Anastrepha species and their distribution in 14 municipalities of the state of Roraima.

PA CC BO CA NO MU IR RO SJ SL CR UI Anastrepha
amita Zucchi, 1979

TABlE 2 :
Anastrepha species associated with their host plants in the state of Roraima.
*Considering only the irst record of Anastrepha species in the host. 1 Exotic species; 2 Native species; 3 Origin unknown.

TABlE 3 :
Anastrepha without known host plants in the state of Roraima.

TABlE 4 :
Parasitoid species associated with Anastrepha spp. in the state of Roraima.