Tritrophic relations and spatial distribution of fruit flies (Diptera: Tephritidae) in the Cerrado and Caatinga regions in Piauí, Brazil

ABSTRACT

Knowledge about the spatial distribution of fruit flies (Diptera: Tephritidae) and tritrophic interactions (fruit-fruit fly parasitoid) contributes to the monitoring and maintenance of the numerical density at a level lower than economic damage. The purpose of this study was to identify the spatial distribution and associations of fruit flies with their parasitoids and host plants in the municipality of Bom Jesus-PI. The flies were obtained from fruit collection from July 2018 to May 2019. A total of 1,711 individuals were obtained, represented by six species: Anastrepha obliqua (Macquart, 1835), An. fraterculus (Wiedemann, 1830), An. alveata Stone, 1942, An. sororcula Zucchi, 1979, An. zenildae Zucchi, 1979 and Ceratitis capitata (Wiedemann, 1824). Anastrepha obliqua was the species with the widest distribution throughout the ecotone area. Ceratitis capitata is distributed only in the urban perimeter. A tritrophic relationship occurred between four species of parasitoids, Asobara anastrephae (Muesebeck, 1958) or Opius sp. associated with An. obliqua in Spondias mombin or S. tuberosa fruits. Opius sp. has also been associated with An. alveata in Ximenia americana. Pachycrepoideus vindemiae was obtained from C. capitata in Malpighia emarginata, in addition to An. obliqua in Averrhoa carambola. Therefore, fruit flies are associated with native fruit trees (S. tuberosa, S. mombin, S. purpurea, P. acutangulum, Inga laurina, X. americana) and exotic fruits (M. emarginata, A. carambola, P. guajava). Ceratitis capitata was recorded for the first time in the state of Piauí infesting I. laurina (Sw.) Willd. This is the first record of the parasitoid genus Spalangia. in An. obliqua in Piauí and in the semiarid region of Brazil.

Keywords:
Ceratitis capitata; Anastrepha; Faunal inventory; GIS geographic information system

Introduction

Knowledge about the tritrophic relations and spatial distribution of insects provides a basis for defining the management strategy of insect populations of economic importance (Soberón, 2010; Teixeira et al., 2021). The interactions involving fruit flies and parasitoids have been largely studied worldwide due to their economic importance and the possibility of using their parasitoids as biological control agents, and the study of interactions between insects and fruits is one of the main challenges for understanding the reproductive success of many angiosperms because the damage caused by insects can cause loss of productivity in a wide variety of fruits. Fruit-eating insects can influence the production due to direct damage and by indirect damage through biochemical changes that cause premature ripening of the fruit or increased protein levels (Aluja, 1999; Ovruski et al., 2000, 2004; Schliserman et al., 2016; López-Ortega et al., 2020). Fruit flies of the Tephritidae family are among the most harmful insects to commercial fruits because the larval stage develops within the fruit (Garcia et al., 2017).

Studies evaluating the population distribution of fruit flies associated with host plants are useful to understand the real biotic potential of these species (Zucchi, 2000; Midgarden et al., 2014; Enkerlin et al., 2015; Arbab and Mirphakhar, 2016; Nicácio et al., 2019; Teixeira et al., 2021). It is important to understand these introductions in ecotonal areas, whose relationships are mixed and with high structural complexity, provide locational and behavioral information for insect management tactics of economic importance (Costa-Coutinho et al., 2019).

One of the main forms of control of fruit flies is the use of integrated insect management. However, to establish this sustainable system, it is essential to know the natural enemies as their parasitoids, especially Hymenoptera, considered by many researchers to be the most efficient natural enemies of fruit flies in various parts of the world (Aluja et al., 2014). The composition of parasitoid species in a region can vary considerably, depending on several factors, such as climate, fruit fly species diversity, and infested fruit trees (Araujo et al., 2015). Information on the diversity and geographical distribution of parasitoids and their hosts is scarce in fragmented ecotonal habitats.

In Piauí, the most recent reports include 23 described species of Anastrepha (Zucchi and Moraes, 2022); for the city of Bom Jesus, however, there is currently one known species of Anastrepha in addition to C. capitata (Coelho et al., 2020). There is only one article published, which was carried out in the urban area of Bom Jesus on the occurrence of fruit fly parasitoid species (Coelho et al., 2020). The identification of native parasitoids requires an intensive analysis of native and exotic fruits in order to verify the association between fly and parasitoid species and their host plants (Silva et al., 2010; Deus et al., 2013).

The aim of this study was to evaluate the interaction of fruit flies with their parasitoids in host plants and their distribution in the municipality of Bom Jesus-state Piaui, Brazil, which has Cerrado, Caatinga vegetation, and transition vegetation (Ecotonal).

Materials and methods

Study area

This study was conducted from July 2018 to May 2019 in the municipality of Bom Jesus-Piauí Brazil (09°04'28 ” S, 44°21'31 ” W; 277 m), which integrates the Piauí semiarid region (Fig. 1). It has a territory of 5,469 km². The climate is warm and humid, classified by Köppen as Awa, tropical rain with a dry season in winter, with average rainfall between 900 and 1.200 mm/year-1 and average temperature of 26.2 °C (INMET, 2019).

Figure 1
Inventory area on fruit flies, showing the distribution of sampling points and the main characteristic environments of the region in the municipality of Bom Jesus-PI, July 2018 to May 2019.

In this region, the high spatial and environmental heterogeneity presents itself as a complex mosaic of vegetation types, ranging from the driest, such as the Caatinga, with small vegetation, trees and thorny shrubs, in addition to Cactaceae, Euphorbiaceae, Bromeliaceae, and Fabaceae plants adapted to withstand water deficit. It has areas of Cerrado, with large shrubs and sparse trees, with twisted branches and deep roots (Souza et al., 2017; Costa-Coutinho et al., 2019). It includes a wide range of Cerrado-Caatinga transition vegetation due to environmental heterogeneity, and its vegetation cover forms a complex mosaic of vegetation types (Macedo et al., 2019). In the transition vegetation ecotone area, there is a current of the Matões Stream microbasin and the Gurguéia River Basin, with riparian forest throughout its course (Paula Filho et al., 2012).

For interpretation purposes, the collected areas were subdivided into: Caatinga - a region of difficult access where the Viana Canyons (rock formations) are located, bordering the Serra das Confusões; Cerrado - a region with intense expansion of deforestation, where the main cultivation areas (soybean, corn) are located; transition vegetation (Ecotone) - central strip of the municipality with the current of the Matões stream, Gurguéia River and the urban perimeter (Fig. 1). Inventory regarding fruit fly species in this region are still scarce (Araújo et al., 2014; Coelho et al., 2018; Vieira et al., 2019; Coelho et al., 2020).

Fruit collection

The fruits were collected weekly at different points in the municipality, which were georeferenced (we tried to cover the entire area of the municipality, excluding areas of difficult access). The fruits were collected according to availability at each point, and each point was sampled only once. Each plant species, georeferenced, from a total of 27 sampled, was named by a numeral to facilitate its spatial identification on the map (Fig. 1).

The fruits were placed in plastic trays and transported to the Plant Protection Laboratory of the Federal University of Piauí (UFPI/CPCE), quantified, weighed individually, labeled and placed in plastic containers containing autoclaved sand and closed. The trays were kept in a room at room temperature (25 ± 2 °C and 70 ± 5% RH). The fruits and sand were sorted between 10 and 15 days, and the pupae were transferred to transparent plastic cups containing sterilized sand for adult emergence for a period of 20 days. The emerged insects were placed in properly labeled glass vials containing 70% ethanol for subsequent identification.

Identification of fruit flies, parasitoids, and host plants

The fruit flies were identified based on the morphological characteristics of the females, mainly in the ventral examination of the aculeus, according to Zucchi (2000).

The parasitoids were identified by morphological characteristics, such as coloration of the antenna apex, tibia, and mandibles, by the researcher Dr. Jorge Anderson Guimaraes from Embrapa de Hortaliças - DF. The specimens of fruit flies and parasitoids were deposited in the Zoology Laboratory of the Federal University of Piauí (UFPI/CPCE).

For the identification of plant species, branches containing reproductive structures (flowers and fruits) were collected. The material was kept as complete as possible and subsequently herborized. According to usual assembly and preservation techniques (Mori et al., 1989; Judd et al., 2009). Plant identification was performed by Prof. Dr. Marcelo Sousa Lopes, Federal University of Piauí-UFPI/CPCE. The identification of unknown individuals was provided through the collection of the Graziela Barroso Herbarium (TEPB), as well as the INCT (2019) website, using analytical keys (Joly, 1975; Barroso, 1984; Luz et al., 2020).

The classification system adopted for the plants was that of APG IV (2016) and abbreviation of the names of the authors of the species, following the same method used on the website of the Botanical Garden of Rio de Janeiro (The Brazil Flora Group, 2018). After proper identification, the specimens were recorded in the SISGEN (National System of Management of Genetic Heritage and Associated Traditional Knowledge) taxon database, as well as in the collection of exsiccates from the herbarium of the UFPI Campus in Bom Jesus and Teresina.

Data analysis

Each sampled group of fruits of each species was weighted. For each sample, fruit infestation levels were calculated by dividing the total number of pupae obtained from the fruit sample by its total weight. The indexes of infestation by flies and of parasitism were obtained by dividing the total number of adult flies and/or parasitoids that emerged from the pupae by the total number of pupae obtained from the sample and multiplied by 100.

The spatial distribution patterns of the fruit fly species were evaluated by the Voronoi Diagram method, which is a partition of a plane into regions close to each of a given set of objects. In the simplest case, these objects are just a finite number of points in the plane (called plants, sites, or generators). For each plant, there is a corresponding region called a Voronoi cell, which consists of all points in the plane closer to that plant than to any other. The Voronoi diagram of a set of points is dual to its Delaunay triangulation. (Feng and Murray, 2018). A map was generated with the definitions of the areas at each sampling point for each variable analyzed. The cross-summation of the factors in the map determined the locations of occurrence of fruit flies, parasitoids, host plants and the relationship between them using ArcGis software (Esri Inc, 2020).

Results

Fruit fly host plant interactions

We examined fruit samples from 27 plant species of 15 botanical families, which summed to a total of 73,333 Kg. We documented the presence of five species of the genus Anastrepha infesting 10 fruit species belonging to seven families and the presence of C. capitata infesting four fruit species belonging to four families (Table 1).

Table 1
- Fruit flies (Diptera: Tephritidae), parasitoids (Hymenoptera) and host fruit trees (native and exotic) sampled in different environments of the municipality of Bom Jesus-PI (July 2018 to May 2019).

Plant Families	Plant Species	Sample Weight (Kg)	Infested Fruit Yes/No	Species of fruit flies	Species of parasitoids	Occurrence Environments
Anacardiaceae	Spondias purpurea	1.43	Yes	Anastrepha obliqua Ceratitis capitata	- -	Transition Vegetation
	Spondias tuberosa	3.55	Yes	Anastrepha obliqua	Asobara anastrephae Opius sp.	Transition Vegetation
	Spondias mombin	7.17	Yes	Anastrepha obliqua	Asobara anastrephae Opius sp.	Transition Vegetation
	Anacardium occidentale	22.50	Yes	Anastrepha obliqua	- -	Transition Vegetatione
	Mangifera indica	0.21	No	- -	- -	Transition Vegetation
Apocynaceae	Hancornia speciosa	0.02	No	- -	- -	Cerrado
Annonaceae	Annona squamosa	0.02	No	- -	- -	Cerrado
Cactaceae	Cereus jamacaru	0.13	No	- -	- -	Transition Vegetation
	Cereus gounellei	0.14	No	- -	- -	Transition Vegetation
Euphorbiaceae	Manihot piauhyensis	0.47	No	- -	- -	Cerrado
Fabaceae	Inga laurina	0.23	Yes	Ceratitis capitata	- -	Transition Vegetation
	Andira sp.	0.61	Yes	Anastrepha zenildae	- -	Transition Vegetation
	Dipteryx lacunifera	0.10	No	- -	- -	Cerrado
	Copaifera langsdorffii	0.02	No	- -	- -	Cerrado
Myrtaceae	Psidium guajava	7.56	Yes	Anastrepha fraterculus	- -	Transition Vegetation
	Psidium acutangulum	12.39	Yes	Anastrepha sororcula Anastrepha fraterculus	- -	Transition Vegetation
	Psidium sp.	0.56	No	- -	- -	Caatinga
Malpigiaceae	Malpighia emarginata	4.80	Yes	Ceratitis capitata	Pachycrepoideus vindemiae	Transition Vegetation
Malvaceae	Guazuma ulmifolia	0.02	No	- -	- -	Cerrado
Melastomataceae	Mouriri pusa	1.51	Yes	Anastrepha fraterculus	- -	Transition Vegetation
	Muriri elliptica	0.19	No	- -	- -	Cerrado
Rubiaceae	Tocoyena sp.	2.20	No	- -	- -	Cerrado
	Alibertia edulis	2.64	No	- -	- -	Cerrado
Rutaceae	Citrus sinensis	1.28	No	- -	- -	Transition Vegetation
Solanonaceae	Physalis angulata	0.01	No	- -	- -	Transition Vegetation
Olacaceae	Ximenia americana	1.75	Yes	Anastrepha alveata	Opius sp.	Transition Vegetation
Oxalidaceae	Averrhoa carambola	1.81	Yes	Ceratitis capitata Anastrepha obliqua	- - Pachycrepoideus vindemiae Spalangia sp.	Transition Vegetation

Of the fruit flies sampled, An. obliqua, and C. capitata had greater infestation rates. The least representative species were An. alveata and An. zenildae. The plants with the highest occurrence of the collected fruit fly species were Malpighia emarginata, Spondias mombin and S. tuberosa (Table 2). Of the fruit flies, An. obliqua had a frequency of 45.7%, and Ceratitis capitata had a frequency of 39.3%. The other species had a low percentage of occurrence during the collections, with An. fraterculus (2.8%), An. sororcula (1.5%), An. alveata (1.1%) and An. zenildae (0.5%).

Table 2
- Abundance of species of fruit flies (Diptera: Tephritidae) sampled in native and exotic hosts (municipality of Bom Jesus-PI, July 2018 to May 2019).

Fruit plants	C. capitata	An. alveata	An. fraterculus	An. obliqua	An. sororcula	An. zenildae	Total
Malpighia emarginata	461(5)	- -	- -	- -	- -	- -	461
Ximenia americana	- -	22(2)	- -	- -	- -	- -	22
Psidium acutangulum	- -	- -	19(1)	- -	10(2)	- -	29
Spondias mombin	- -	- -	- -	412(13)	- -	- -	412
Anacardium occidentale	- -	- -	- -	3(1)	- -	- -	3
Averrhoa carambola	160(3)	- -	- -	29(2)	- -	- -	189
Psidium guajava	- -	- -	5(1)	- -	- -	- -	5
Inga laurine	11(1)	- -	- -	- -	- -	- -	11
Mouriri pusa	- -	- -	24(2)	- -	- -	- -	24
Andira sp.	- -	- -	- -	- -	- -	3(1)	3
Spondias purpurea	106(2)	- -	- -	57(2)	- -	- -	163
Spondias tuberosa	- -	- -	- -	389(4)	- -	- -	389
Grand Total	738	22	48	890	10	3	1711
No. of infested hosts	4	1	3	5	1	1	-
Infestation rates	1.0236	0,0172	0.9978	3.045	1.970	0.0064	- -

• () = frequency in which it occurred

Our sampling efforts resulted in the first records of C. capitata infesting Inga laurina in the state of Piauí.

Anastrepha obliqua was widely distributed: S. mombin L., S. tuberosa L., Averrhoa carambola L., Anacardium occidentale L., S. purpurea L. and Psidium guajava L. (Figs. 2B and 2A). The other species of fruit flies occurred at restricted sites: An. zenildae in an area of Cerrado, infesting Andira sp.; An. sororcula in the transition vegetation (ecotonal), infesting P. acutangulum DC.; An. alveata in the transition vegetation, infesting Xinemia americana L. Anastrepha fraterculus was obtained from three fruit species: Mouriri pusa, P. acutangulum and P. guajava, all in the transition vegetation (Figs. 2A and 2B). Of all the fruit fly species, An. obliqua exhibited the highest number of hosts in the region, exploiting up to five host species.

Figure 2
(A) Spatial distribution of fruit plants, (B) fruit flies (Diptera: Tephritidae), (C) parasitoids Hymenoptera and (D) tritrophic relationship in sampling of native and exotic fruits (municipality of Bom Jesus -PI, July 2018 to May 2019).

With respect to host plant phenology, the highest availability of fruits was generally observed in the period of August and September 2018 and February and March 2019 (8 species), with the highest number and abundance of fruits recorded during March. We observed that the fruits of A. occidentale were the most abundant, but only with the record of An. abliqua, already S. purpurea, with a lower amount of fruit, we recorded three species of fruit flies (Tables 1 and 3).

Table 3
- Distribution of the fructification period of plant species sampled from the municipality of Bom Jesus state Piauí, Brazil. (July 2018 - May 2019). Darker shading indicates greater availability of fruits; lighter shading denotes a decrease in fruit availability, generally occurring before and after the rainy season. Asterisks indicate new host plant records for fruit flies.

Host Family	Host Scientific Name	Fruit Fly Species	Jul	Aug	Sep	Oct	Nov	Dec	Jan	Feb	Mar	Apr	May
Anacardiaceae	Spondias purpurea	Anastrepha obliqua
		Anastrepha fraterculus
		Ceratitis capitata
	Spondias tuberosa	Anastrepha obliqua
	Spondias mombin	Anastrepha obliqua
	Anacardium occidentale	Anastrepha obliqua
	Mangifera indica	- -
		- -
Apocynaceae	Hancornia speciosa	- -
Annonaceae	Annona squamosa	- -
Cactaceae	Cereus jamacaru	- -
	Cereus gounellei	- -
Euphorbiaceae	Manihot piauhyensis	- -
Fabaceae	Inga laurina*	Ceratitis capitata
	Andira sp.*	Anastrepha zenildae
	Dipteryx lacunifera	- -
	Copaifera langsdorffii	- -
Myrtaceae	Psidium guajava	Anastrepha fraterculus
		Anastrepha obliqua
	Psidium acutangulum	Anastrepha sororcula
		Anastrepha fraterculus
	Psidium sp.	- -
Malpigiaceae	Malpighia emarginata	Ceratitis capitata
Malvaceae	Guazuma ulmifolia	- -
Melastomataceae	Mouriri pusa	Anastrepha fraterculus
	Muriri elliptica	- -
Rubiaceae	Tocoyena sp.	- -
	Alibertia edulis	- -
Rutaceae	Citrus sinensis	- -
Solanonaceae	Physalis angulata	- -
Olacaceae	Ximenia americana	Anastrepha alveata
Oxalidaceae	Averrhoa carambola	Ceratitis capitata
		Anastrepha obliqua

Anastrepha obliqua occurred from August 2018, with predominance in the months of January to April 2019 and higher population density in March due to the increased availability of S. mombin and S. tuberosa fruits in the host plants, a consequence of rainfall accumulation. in this period of the year. Anastrepha fraterculus occurred in November, January and March. Ceratitis capitata occurred in August, September and October 2018 and January to April 2019, and in August, there was a greater number of individuals collected from M. emarginata and A. carambola plants (Table 3).

Fruit infestation and parasitism rates

Fruit infestation rates were highly variable between the different hosts, ranging between 0.006 and 3.04 fruit flies/kg of sampled fruit. The highest infestation levels occurred in M. emarginata, S. tuberosa and S. mombin, and the lowest infestation rate was observed in Andira sp.

Four species of parasitoids associated with fruit flies were identified: Asobara anastrephae Muesebeck, 1958 (Hymenoptera: Braconidae) Opius sp. (Hymenoptera: Braconidae), Pachycrepoideus vindemiae Rondani, 1875 (Hymenoptera: Pteromalidae) and Spalangia sp. (Hymenoptera: Pteromalidae), (Table 1 and Table 4). Among these species, Opius sp. and As. anastrephae occurred in the transition vegetation and Caatinga area. The other species were distributed in transition vegetation (Fig. 2C). The occurrence of parasitoids was more restricted to the transition vegetation in the vicinity of the Gurguéia River basin and the current of the Matões stream, located in the ecotonal region (Fig. 2C).

Table 4
- Parasitoid species and levels of parasitism of fruit fly species in their hosts sampled from the municipality of Bom Jesus state Piauí, Brazil. (July 2018 - May 2019).

Family	Host Plant	Fruit fly species	Recovered Fruit Fly Pupae	Parasitoid Species	Total No. Parasitoids	% Parasitism
Anacardiaceae	Spondias tuberosa	Anastrepha obliqua	474	Asobara anastrephae	28	1.8
				Opius sp.	12	0.78
	Spondias mombin	Anastrepha obliqua	690	Asobara anastrephae	51	3.24
				Opius sp.	64	4.03
Malpigiaceae	Malpighia emarginata	Ceratitis capitata	161	Pachycrepoideus vindemiae	10	0.65
Olacaceae	Ximenia americana	Anastrepha alveata	163	Opius sp.	12	0.78
Oxalidaceae	Averrhoa carambola	Anastrepha obliqua	34	Pachycrepoideus vindemiae	3	0.19
				Spalangia sp.	2	0.13

Of the parasitoid species, the parasitism percentage were 3.24%. and 1.8% for As. anastrephae. The other species presented a low frequency, Spalangia sp. (0.13%) and P. vindemiae (0.19%). The fruit hosts of fruit flies with greater association with parasitoids, were S. purpurea and S. monbin and A. carambola in An. Obliqua (Table 1 and Table 4). In the case of species An. sororcula, An. zenilde and An. fraterculus, we did not observe any parasitism.

Tritrophic interactions: fruit flies, parasitoids, and host plants

Of the parasitoid species, As. anastrephae is restricted to An. obliqua collected from S. mombin and S. tuberosa plants; Opius sp. occurred in An. obliqua in fruits of S. mombin and S. tuberosa and in An. alveata associated with X. americana; Spalangia sp. occurred only in An. obliqua in A. carambola fruits; P. vindemiae was recorded in C. capitata, in fruits of M. emarginata, and An. obliqua in S. purpurea. Of the four parasitoid species recorded, all parasitized An. obliqua, two of which were obtained from the same host plants: As. anastrephae and Opius sp. in S. mombin and Spalangia sp. and P. vindemiae in A. carambola fruits (Table 1 and Fig. 2D).

Of the twenty-seven (27) fruit trees sampled, twelve (12) were colonized by fruit flies. Of these, eight (8) were infested exclusively by Anastrepha species, and two (2) were infested exclusively by C. capitata. Malpighia emarginata and A. carambola are introduced fruit plants, while S. purpurea and I. laurina are native. Anacardiaceae had the highest number of species with infested fruits, followed by Myrtaceae and Malpighiaceae (Table 1).

Discussion

Previous studies reported 128 species of Anastrepha in Brazil, of which 23 species are recorded from the state of Piauí (Zucchi and Moraes, 2022); for the city of Bom Jesus, however, there are currently one known species of Anastrepha (An. obliqua) in addition to C. capitata (Coelho et al., 2020).

The distribution of fruit flies was more frequent in the transition vegetation area (ecotone) (Figs. 1 and 2B), which is related to the occurrence of different fruit plants, some of which are considered the preferred host of fruit flies, such as S. mombin (Sousa et al., 2017). This area is characterized by being a humid region due to the presence of the Gurguéia River and the Current of the Matões stream, consequently providing a greater availability of resources. Fruit flies occur in different fruit trees, such as A. carambola and S. tuberosa, which are considered endemic plants of the Caatinga (Santos et al., 2012).

Fruit flies have a relationship closely linked to the hosts of certain plant taxa. Anacardiaceae fruits, for example, have been reported as preferential hosts of An. obliqua. Species of this family have fruits rich in nutrients, which probably provide a higher nutritional quality for An. obliqua larvae. The production period (fruits), for example, of S. mombin, occurs between the months of February and June (Araujo et al., 2005; Souza et al., 2006), which may explain the greater abundance of this fruit flies infesting these hosts in this study due to its soon fruiting period, providing the development of the life cycle of these flies.

This preference of An. obliqua for fruit trees of the genus Spondias is not restricted to the state of Piauí (Araújo et al., 2014) but was also reported in other states and geographic regions of Brazil, such as Rio de Janeiro (Leal et al., 2009), Minas Gerais (Pirovani et al., 2010), Bahia (Bittencourt et al., 2012), Mato Grosso do Sul (Uchôa-Fernandes et al., 2002) and Amapá (Deus and Adaime, 2013).

The distribution of C. capitata (Mediterranean fly or medfly) was restricted to the urban perimeter of the municipality of Bom Jesus Piauí, associated with four fruit species. This species is a key pest in fruit crops in many tropical, subtropical, and temperate areas. It was possible to observe C. capitata infestation in M. emarginata and A. carambola but also infested native fruits, S. purpurea and I. laurina. This shows the high adaptive capacity of this species and is in constant population increase due to the invasion of new geographic areas, infesting different hosts (Zucchi and Moraes 2012; Sciarretta et al., 2018). In Piauí, there is a record of this species in A. carambola fruits (Feitosa et al., 2007), S. mombin (Araújo et al., 2014) and S. purpurea (Coelho et al., 2020). Ceratitis capitata was recorded for the first time in I. laurina pods in the state of Piauí. Inga fruits were sampled in an urban area (riparian forest). The family Fabaceae is widely distributed in Brazil, from the states of the Amazon to Paraná, as well as in other parts of South America, Central America, and the Caribbean Islands. Inga laurina was recorded as a host of An. distincta (Uramoto et al., 2008) and An. striata (Souza et al., 2018).

In the urban area, transition vegetation, of the sampled region, there are several species of fruit trees, used both in the afforestation of the city and cultivated in backyards. These sites become a reservoir of C. capitata, favoring its population increase. According to Alvarenga et al. (2009), in urban orchards, fruits maturing in different seasons of the year provide excellent food conditions for fruit flies, enabling the dispersal and exploitation of different niches (Alvarenga et al., 2009).

In studies on P. guajava plantations, Lopes et al. (2015) observed that C. capitata did not coexist with Anastrepha species. In this study, the occurrence of C. capitata in native fruit trees in both S. purpurea and I. laurina was observed, which shows the aggressiveness and adaptation of this species in search of new hosts. The presence of C. capitata in urban areas is related to urbanization, where there is a greater presence of introduced fruits, favoring the presence of this species, which competes directly with Anastrepha species for resources (Garcia et al., 2017). However, the correct management of native plant species that serve as natural reservoirs of fruit flies is necessary, which is essential to avoid the displacement of their populations to commercial orchards.

The Opius genus is one of the largest in the Braconidae family, and all opiine braconids are koinobiont endoparasitoids of Cyclorrhapha diptera, has the potential to reduce the populations of fruit flies is a genus of parasitoids that predominates in areas of native vegetation (Costa et al., 2009). Most likely, the characteristics of host plants (Anacardiaceae) favored parasitism by native parasitoids in Anastrepha species. López-Ortega et al. (2020) report Opius hirtus (Fisher) in five new fruit fly-parasitoid associations, all occurring in native tree species infested by different fly species. This highlights the preference of this parasitoid for monophagous fly species attacking comparatively small-sized fruits.

Asobara anastrephae obtained from An. obliqua in S. tuberosa and S. mombin fruits; Opius sp. obtained from An. alveata associated with X. americana and An. obliqua associated with S. tuberosa and S. mombin, both parasitoid species are native and have small ovipositors, which favors success in their parasitism in smaller fruits with shallow pulps (Zucchi, 2000; Sousa et al., 2016).

In addition, we document the first report of Spalangia sp. parasitizing An. obliqua in the State Piaui. The occurrence of Spalangia sp. in this survey shows that these parasitoids can be common in semiarid environment. Species of parasitoids of the genus Spalandia are generalists and parasitize pupae of various dipteran families, such as Muscidae, Calliphoridae, Sarcophagidae, Drosophilidae, and Tephritidae. In Brazil, there are records of Spalangia parasitizing Anastrepha in the southeastern and center-west regions and parasitizing C. capitata in the semiarid region of Brazil (Uchôa-Fernandes et al., 2003; Gibson, 2009; Nicácio et al, 2011; Beitia et al., 2016; Silva et al., 2020). Therefore, these are the first reports of Spalangia sp. species associated with An. obliqua in a semiarid region of Brazil.

Based on the observed associations, further studies should be conducted on the diversity of parasitoid species that attack fruit flies in southwestern Piauí. Future research should focus on the biology and ecology of these parasitoids, which are promising biological control agents of fruit flies. Parasitism in frugivorous tephritid larvae is quite variable in natural environments (Nicácio et al., 2011). It can be affected by several factors, such as the occurrence of host frugivorous larvae and host fruit characteristics.

Asobara anastrephae was associated with An. obliqua in S. tuberosa and S. mombin fruits. This species has been reported by other authors parasitizing tephritid species in Brazil (Uchôa-Fernandes et al., 2003) and in the semiarid region in a study by Sá et al. (2012), parasitizing Anastrepha species in S. tuberosa fruits, corroborating what was observed in this study. Asobara anastrephae is considered a species adapted to the northeast region and to several native hosts, such as umbuzeiro, endemic to the Caatinga. This parasitoid was also observed attacking the same species An. obliqua in the Amazon region in S. mombin fruits (Sousa et al., 2016).

Studies on the tritrophic interactions between fruit flies, their host plants and parasitoids are scarce. The results described here contribute to the understanding of the relationships between native parasitoids and species of fruit flies. Parasitoids are particularly important because of interactions for long periods of time with their hosts and may be effective in reducing pest populations in orchards, keeping the outbreaks of Tephritidae under control without decreasing local biodiversity (Sugayama and Malavasi, 2000; Zucchi, 2000; Uchôa-Fernandes et al., 2003; Cancino et al., 2009; Araujo et al., 2015).

This study was conducted in an ecotonal region, which has a heterogeneity of microenvironments, and the vegetation cover has a floristic mixture, where species from the Cerrado and Caatinga biomes coexist (Souza et al., 2017), with greater availability of resources for fruit flies in the ecotone area (Garcia et al., 2017). S. tuberosa, for example, is endemic to the Caatinga biome (Santos et al., 2012), and M. pusa is characteristic of Cerrado regions (Borges, 2012). Other host fruit trees in this region, such as P. guajava, A. occidentales, P. acutangulum, wild X. americana, S. mombin, and S. purpurea, were all infested by species of the genus Anastrepha.

Fruit flies can persist in different types of environments. Generalist species can thrive in a matrix of human use with commercial and backyard fruit orchards, while a part of the population remains and survives within the natural forest. This would be the case for C. capitata in I. laurina, a plant species that maintains viable populations of this fruit fly within its natural habitat. Because 70 percent of herbivore species exhibit a high level of specialization (Bernays and Chapman, 1994), knowledge of wild plant species that serve as hosts for fruit flies is relevant.

These results highlight the importance of increasing our knowledge about fruit fly/host plant interactions in natural environments.

Conclusions

Our findings shed light into host plant association for species of fruit flies and their parasitoids in natural environments and highlight the importance of tropical rainforests for the conservation of biodiversity. The areas of the Cerrado and Caatinga in Bom Jesus, that still preserve a great part of its original composition and structure exhibit a higher richness of wild fruits, such as those collected in this study. Consequently, represents a highly important reservoir for the diversity of fruit fly and native parasitoids spatially and temporally.

Acknowledgments

Federal University of Piauí (Universidade Federal do Piauí - UFPI) for providing transportation and some of the laboratory facilities necessary for this study and Coordination for the Improvement of Higher Education Personnel (CAPES). The authors would like to thank researcher Dr. Jorge Anderson Guimaraes for identifying the parasitoid species and researcher Dr. Marcelo Sousa Lopes for identifying the plant species.

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Edited by

Associate Editor: Ricardo Siqueira da Silva

Publication Dates

• Publication in this collection
  18 July 2022
• Date of issue
  2022

History

• Received
  22 Nov 2021
• Accepted
  14 June 2022