Tephritidae and Lonchaeidae (Tephritoidea) are major pests of horticultural crops worldwide. Knowledge of the interactions between these flies and their host plants is needed for rational methods of population control. In the South Pantanal and adjacent areas in Brazil we sampled fruits from 92 plant species (22 orders and 36 families) in natural environments. Fifty-three species of plants were infested, and 39 not infested. Some aspects of the biology and patterns of species diversity, abundance, frequency, pupation period for males and conspecific females, and the interactions among species of frugivorous flies and their host plants were quantified. Twenty-six species of flies from 4 genera and 2 families were reared from the fruits: 17 species of Tephritidae (16 Anastrepha spp. and Ceratitis capitata), and 9 species of Lonchaeidae, comprising 8 species of Neosilba McAlpine, and 1 species of Lonchaea Fallén (Lonchaeidae). The lonchaeids infested 48 species of fruits, and the tephritids 30 species. The most polyphagous species were Neosilba zadolicha McAlpine & Steyskal (36 hosts), Neosilba pendula (Bezzi) (18 hosts), and Neosilba inesperata Strikis & Prado (14 hosts) (Lonchaeidae); and Anastrepha sororcula Zucchi (10 hosts), Ceratitis capitata (Wiedemann) (10 hosts), Anastrepha obliqua (Macquart) (7 hosts), and Anastrepha zenildae (6 hosts) (Tephritidae). All the males of Tephritidae (16 Anastrepha spp. and C. capitata) emerged before their conspecific females. Conversely, all females of the 8 species of Neosilba emerged in advance of their conspecific males.
The polyphagous and oligophagous species of Tephritidae (fruit flies) and Lonchaeidae (lance flies) (Tephritoidea) are the main pests of horticulture in the Neotropical Region. They are the cause of quarantine constraints imposed by many countries to curtail their entry, and they significantly influence commerce inside and outside of the countries producing fruits and vegetables around the world (Uchôa et al. 2002; Uchôa & Nicácio 2010). On the other hand, many stenophagous and monophagous tephritoid species are important as potential biological control agents for invading species of plants (Norrbom & McAlpine 1997), in the decomposition of fruits and cycling of nutrients in the food web, and as alternative hosts for the multiplication of parasitoids, which may reduce the populations of pest flies in orchards.
The Pantanal and Cerrado biomes host important components of Neotropical biodiversity, and the insects are among the taxa most poorly known in both environments (Myers et al. 2000; Junk et al. 2006). Frugivorous Tephritoidea (fruit flies and lance flies) are biodiverse in all Brazilian regions, but their interactions with their host plants are poorly studied, and surveys of the Cerrado and Pantanal biomes are scarce.
The determination of the host plant status for species of fruit flies on commercially important fruits is a controversial topic that frequently causes commercial disputes between countries around the world, and knowledge about the interactions among fruit flies and their host plants is missing for decades. One of the reasons for this delay is a methodological problem (Aluja & Mangan 2008). As pointed out by Aluja & Mangan (2008), first it is necessary to determine if a plant is a natural host, a conditional host (non-natural infestation that occurs when only one species of fruit is offered to a fruit fly species with no option of choice in laboratory conditions), or a non-host (when even in the laboratory under forced conditions the species of fruit fly does not oviposit in the only species of fruit offered as a resource). Some host plant records for fruit flies may be not trustworthy, because inappropriate methodology was applied to study fruit fly and plant interactions.
Aluja & Mangan (2008) classify the species of fruit flies into four types, according to their ability to colonize host plants: the species that infest fruits of different families/orders of plants are polyphagous; those that develop in fruits of the same family are oligophagous; species that infest fruits of a single genus of plants are stenophagous, and finally, monophagous species of fruit flies colonize fruits of only a single species of plant.
The most species rich genera of frugivorous Tephritoidea in Brazil are Anastrepha Schiner (Tephritidae) and Neosilba McAlpine (Lonchaeidae), with 251 (Uramoto et al. 2008; Norrbom & Korytkowski 2009; Canal 2010; Uramoto & Zucchi 2010; Norrbom & Korytkowski 2011; Norrbom & Uchôa 2011), and 17 described species (Strikis & Prado 2005, 2009; Strikis & Lerena 2009), respectively.
No host plant is known for 51 of the 112 species of Anastrepha reported from Brazil, (Zucchi 2008; Garcia et al. 2008; Uramoto & Zucchi 2010; Uchôa & Nicácio 2010; Norrbom & Uchôa 2011). In the genus Anastrepha, some species are of economic importance in the American tropics and subtropics (Calkins & Malavasi 1995) and about half of the species of Neosilba have been associated with fruits and vegetables in the Neotropics.
Knowledge of trophic interactions between frugivorous Tephritoidea and their host plants is important to support strategies for integrated management of fruit fly pests (polyphagous or oligophagous), and for the conservation of stenophagous and monophagous species in their natural environments.
The aims of this study were (1) identify the diversity, abundance and frequency of species of frugivorous Tephritidae and Lonchaeidae (Tephritoidea) in the Pantanal and surrounding areas, (2) study the occurrence and larval viability of the species of fruit flies and lance flies in different naturally infested host fruits in the Pantanal and adjacent areas, and (3) quantify the mean period of pupation (from the exit of larva from the host fruit until adult emergence) for both males and females of the different species of Tephritidae and Lonchaeidae.
MATERIALS and METHODS
Characterization of Climate, Relief and Vegetation
The climate in the state of Mato Grosso do Sul is basically tropical and influenced by cold fronts during the winter (Jun–Sep), when the environment is drier and rainfall vary from 30–60 mm / month. Monthly mean temperature vary from 20–34°C, and the mean annual precipitation ranges from 1300 to 1700 mm. The altitude ranges from 100 to 1000 m above sea level, and vegetation types include savanna, seasonal semideciduous, deciduous, and sub-mountain. In the plateaus near the foothills there are dense shrub-herbaceus strata (1.5–2.0 m high), an intermediate continuous arboreal strata forming a canopy about 10 m above the ground with some trees of 15–25 m (Radam Brasil 1982; Galati et al. 2006).
The biome Pantanal (16–20°S/55–58°W, an environment that resembles the Florida Everglades), is the largest periodically flooded plain in the world, with an area of approximately 160,000 km2 (140,000 km2 in Brazilian territory, 15,000 km2 in Bolivia and 5000 km2 in Paraguay). It is recognized by the United Nations Educational, Scientific and Cultural Organization (UNESCO) as a natural heritage of mankind, biological reserve of the biosphere, and included among the most fragile and threatened biomes of the world (Junk et al. 2006). The Pantanal is connected with the Serra de Maracajú and Cerrado.
The Serra de Maracajú is a plateau that divides the state of Mato Grosso do Sul into 2 distinct biomes: the Cerrado and the Pantanal. To the east of the capital (Campo Grande), Cerrado environments predominate, with soil composed mainly of sandstones, and to the west of Campo Grande, the Pantanal begins (Radam Brasil 1982).
The Cerrado biome, an environment that resembles an African savanna, is located mainly in Central Brazil and occupies approximately 2 million km2 (about 25% of the Brazilian territory). Vegetation varies, but is characterized by its great diversity and high rates of endemism (about 2% of global diversity of plants). Among 26 global biodiversity-hotspots listed for preservation of habitat, it is listed as the sixth most important (Myers et al. 2000; Carvalho et al. 2009).
The original vegetation of the Cerrado biome occupied 1,783,200 km2, but currently only 356,630 km2 remain natural, which represent 20% of the original area. Of this, only 22,000 km2 (6.2%) are located in protected areas, such as National Parks or private reserves. About 10,000 plant species are cataloged in the Cerrado, but for animals only 4 groups of vertebrates are well known (mammals, birds, reptiles and amphibians: 27,298 species). The diversity of invertebrates, totaling more than 95% of living species of animals and represented mainly by insects, is poorly documented (Myers et al. 2000).
Sampling of Plants
A total of 184 trips was made to sample the native fruits of South Pantanal, Cerrado and Serra de Maracajú. Fruits of 92 plant species from 22 orders and 36 families were evaluated for the occurrence of frugivorous tephritoid larvae.
The samples of fruits were taken during the seasons of fruit maturation for angiosperms in the South Pantanal Region (Pott & Pott 1994). Fruits were harvested directly from trees, or occasionally fruits recently fallen to the soil were collected, between Apr 1998 and Aug 2000, in 11 municipalities in the 3 different environments (Pantanal, Cerrado, and Sierra de Maracajú) of the state of Mato Grosso do Sul. The fruits of Ximena americana L. (Olacaceae) also were collected in Oct 2003 and Oct 2004 in the Pantanal.
Sampled Environments
Pantanal: Miranda (20°20′36″S/56°23′49″W, altitude 121 m); Aquidauana: Fazenda Aguapé (20°6′18″S/55°58′11″W, 144 m), Fazenda Rio Negro (19°34′6″S/56°14′44″W, 107 m) and Aquidauana City - Lagoa dos Padres (20°28′46″S/ 55°48′35″W, 141 m); Corrumbá: Passo do Lontra (19°35′32″S/57°32′34″W, 89 m) and Fazenda São Domingos (19°31′24″S/57°2′22″W, 90 m).
Cerrado: Aquidauana (20°28′36″S/55°47′15″W, altitude 151 m);Anastácio (20°29′1″S/55°49′48″W, 148 m) and Fazenda Nossa Senhora Aparecida (20°33′2″S/55°52′45″W, 173 m), Dois Irmãos do Buriti (20°40′47″S/55°17′46″W, 318 m), Terenos (20°27′2″S/55°5′3″W, 263 m), Campo Grande (20°26′34″S/54°38′47″W, 581 m); Nioaque (21°8′7″S/55°49′48″W, 213 m) and Rio Negro (19°26′58″S/54°59′13″W, 261 m).
Serra de Maracajú: Aquidauana - Fazenda Rio Doce: (20°21′52″S/55°36′35″W, altitude 478 m) and Morro do Paxixi (20°28′1″S/55°39′40″W, 192 m), Rochedo (19°57′11″S/54°53′33″W, 257 m), Miranda (20°20′36″S/56°23′49″W, 121 m) and Bodoquena (20°5′19″S/56°46′54″W, 130 m).
Collection of Larvae of Frugivorous Flies
Fruit samples were transported to the Laboratório de Controle Biológico de Insetos, Departmento de Biociências, Universidade Federal de Mato Grosso do Sul (UFMS), Campus de Aquidauana, where fruits were counted and weighed, then held to obtain associated insects according to methodology by Uchôa & Zucchi (1999). Photoperiod was 12h:12h (L:D). The temperature and relative humidity ranged from 15 to 40°C and from 40 to 90%.
Voucher specimens of plants were deposited in the Central Herbarium of the Universidade Federal de Mato Grosso do Sul (UFMS) in Campo Grande-MS, and in the Herbarium of the Departamento de Botânica, Universidade de São Paulo (USP) in São Paulo-SP, Brazil.
Exiting third instar tephritoids (L3) were counted and separated in transparent acrylic containers (300 mL) with sterile sand moistened with distilled water until adult emergence. Each container was labeled to identify the host fruit species and sample date, place, and municipality of collection, fly family, and date of L3 leaving the fruits. The larvae of Lonchaeidae and Tephritidae were differentiated by the shape of the posterior spiracles, body color, and morphology of the mandibles. The posterior spiracles of tephritid larvae (Anastrepha and Ceratitis capitata (Wiedemann)) are yellowish, inconspicuous, and lacking a sclerotized peritreme. The cephalopharyngeal region is shorter, compared to that of lonchaeids. The Lonchaeidae larvae have the posterior spiracles blackish, with a sclerotized peritreme, and more noticeable than those of tephritids, and the body of the lonchaeids is more filiform in shape, whitish, with the cephalopharyngeal region more elongated. Furthermore, the mouth hooks of the Lonchaeidae larvae are darker and more visible than those of tephritids.
The adult flies after emergence, were kept alive for 2 or 3 d to allow full development of color patterns of the body and of the wings of each species. After that, they were killed by exposure to ethyl acetate, and preserved in vials with 70% ethanol.
Identification of Host Plants and Frugivorous Tephritoidea
The plants were identified by the botanists Ubirazilda Maria Rezende from the Herbarium of the Universidade Federal de Mato Grosso do Sul (UFMS) at Campo Grande-MS, and José Rubens Pirani from the Herbarium of the Departamento de Botânica, Universidade de São Paulo (USP, São Paulo), Brazil.
The species of Anastrepha and C. capitata were identified in the Laboratório de Insetos Frugívoros, Faculdade de Ciências Biológicas e Ambientais (FCBA), Universidade Federal da Grande Dourados (UFGD), by M. A. Uchôa using keys and species description (Lima 1934; Stone 1942; Foote 1980; Norrbom & Korytkowski 2009).
The species of Neosilba were identified mainly based on the morphology of the male genitalia (McAlpine & Steyskal 1982) by Pedro Carlos Strikis, UNICAMP, Campinas-SP, Brazil. Voucher specimens of Tephritidae are deposited in the Entomological Collection of the Museu da Biodiversidade (MuBio), FCBA-UFGD, Dourados-MS, Brazil, and voucher specimens of Neosilba (Lonchaeidae) are in the Zoological Collection of Universidade Estadual de Campinas-UNICAMP, Campinas-SP, Brazil.
Definition of Variables, Statistical Analysis and Methods
Statistical analysis was based on 5 qualitative variables: species, orders and families of plants, species and environments of emerged frugivorous flies. Five quantitative variables were evaluated: number of emerged flies, pupal period of the species of fly, number of third instar larvae (L3) / the number of fruit and number of L3 / the mass of fruit (g).
The fruit infestation levels were measured by 2 indexes: average number of third instars (= prepuparial larvae or L3) emerged / fruit, and average number of L3 / mass (g) of fruit. The first index was categorized into 3 intervals of classes: (1) low infestation (<0.1 larvae / fruit);(2) mean infestation (0.1 to 1.0 larvae / fruit); and (3) high infestation (>1.0 larvae / fruit).
The pupal period is defined as the time between the exit of the pre-puparial larva (L3) from the fruit until the emergence of the adult. Four class intervals were established for the average of pupal period: 1 (6–10 d); 2 (10–14 d); 3 (14–18 d); and 4, over 18 d. The averages of pupal period were compared for 13 species of Anastrepha, C. capitata and 6 species of Neosilba. The statistical analysis included only those species that occurred in at least 3 fruit samples.
The viability of the pre-puparial larvae (L3) was calculated by the equation: %V = No. of EA/ L3) × 100, where: %V = Percent of viability), No. of EA = number of emerged adults, and L3 = Total number of pre-puparial larvae; and the quotient was multiplied by 100.
The tests used were chi-square of Pearson (χ2) to test the hypothesis of independence between 2 variables (Dawson & Trapp 2003), and the Kruskal-Wallis Test to compare each 2 variables (Pestana & Gageiro 2008).
We considered α < 1% (highly significant difference), 1% < α < 5% (significant difference), and 5% < α < 10% (marginally significant difference).
Analysis of variance (ANOVA) was used to compare means when assumptions of homogeneity occurred (Levene's Test), and normality (Kolmogorov-Smirnov Test) for dependent variables (Maroco 2007).
RESULTS
From the total of 92 species of fruits sampled, 53 were infested by tephritoid larvae, from which 40 species had not been surveyed previously for Tephritoidea infestation (Uchôa et al. 2002; Zucchi 2007; Uramoto et al. 2008; Garcia et al. 2008; Uchôa & Nicácio 2010) (Table 1). A total of 89,593 fruit were collected weighting 1,141.55 kg, from which 28,714 third-instars (L3) exited.
In all the species of host fruit (except from Duguetia furfuraceae Saint Hilaire) only pulp feeding frugivorous flies were obtained. The Tephritidae comprised 22,505 pre-puparial larvae (L3) and 13,443 adults, and the Lonchaeidae: 6,209 larvae (L3) and 3,770 adults (Table 1).
Thirty-nine species of plants (Aristolochiaceae [Aristolochiales], Bromeliaceae [Bromeliales], Cactaceae [Cactales]; Curcubitaceae [Curcubitales], Erythroxylaceae [Gentianales], Bombacaceae and Malvaceae [Malvales], Smilacaceae [Liliflorae], Meliaceae [Rutales], Sapindaceae [Sapindales], and Verbenaceae [Verbenales] were not infested by the tephritoid larvae (Uchôa & Nicácio 2010).
In this series of samples, 26 species of Neotropical Tephritoidea (16 species of Anastrepha, C. capitata, Tephritidae, and 9 species of Lonchaeidae) were reared from their host fruits (Table 2).
Tephritidae. The tephritids infested 30 species of fruits in 17 families and 13 orders of Angiospermae. Seventeen species emerged (16 Anastrepha and C. capitata), and a single species emerged from 5 hosts. The highest species richness of Tephritidae occurred in the mountainous environment, where 10 species were recovered (Table 2).
TABLE 1.
HOST PLANTS (ANGIOSPERMAE) AND INFESTATION INDICES BY FRUGIVOROUS LARVAE OF FRUIT FLIES AND LANCE FLIES (DIPTERA: TEPHRITOIDEA) IN THE SOUTH PANTANAL REGION, BRAZIL (APR 1998 TO AUG 2000, OCT 2003, AND OCT 2004).
The most ubiquitous species was Anastrepha sororcula Zucchi, which occurred in all 3 environments, followed by Anastrepha zenildae Zucchi in mountainous and cerrado areas. At the other extreme, Anastrepha undosa Stone was characterized as a monophagous species restricted to the swamp environment of the Pantanal (Table 2).
The host fruits Terminalia catappa L., Psidium kennedyanum Morong and Ximenia americana L. had the highest abundance of larvae. The most frequent species were A. sororcula, Anastrepha striata Schiner, and A. zenildae, which occurred in 26, 16, and 15 samples of fruits, respectively (Table 2).
The highest infestation rates (L3/fruit) occurred in Andira cuyabensis Bentham, followed by Terminalia catappa and Ximenia americana, with 9.59, 9.26, and 4.75 larvae per fruit, respectively However, taking into account the rate of infestation number of pre-puparial larvae by fruit mass (L3/g of fruit), the highest rates occurred in T. catappa (0.4 L/g), followed by Andira cuyabensis (0.33 L3 /g), and Psidium kennedyanum (0.31 L3/g) (Table 2).
The percentage of viability for the third instar (L3) was highest in the hosts Sorocea sprucei saxicola (Baillon) J. F. Macbride (95.83%), Licania tomentosa (94.29%), and Andira cuyabensis (94.0%) (Table 2).
The more generalist species of Tephritidae were A. sororcula, C. capitata, Anastrepha obliqua (Macquart), and A. zenildae, which infested 10, 10, 7, and 6 hosts, respectively (Table 2).
Lonchaeidae. Nine lonchaeid species (8 Neosilba spp. and 1 Lonchaea sp.) occurred in fruit of 48 species of plants from 24 families and 15 orders. From 2 hosts (Syagrus flexuosa (Martius) Beccari, and Eugenia pitanga (O. Berg) Kiaerskou, larvae exited but no adults emerged. Only species of Neosilba were obtained from 21 species of plants, and the highest species richness of this genus occurred in the Cerrado environment (S = 8) (Table 3).
The highest rates of fruit infestation by the species of Neosilba occurred in the hosts Duguetia furfuracea Saint Hilaire (10.78 L3/fruit and 0.22 L3/g of fruit), Annona crassiflora Martius (4.97 L3/fruit and 0.01 L3/g of fruit), and Citrus sinensis (L.) Osbeck (1.36 L3/fruit and 0.01 L3/g of fruit) (Table 3).
The highest viability (% of adult emergence from L3 larvae) for the Lonchaeidae occurred in Andira cuyabensis Bentham (100%), Physalis angulata L. (99.55%), Licania tomentosa (96.30%), and Alibertia edulis (Richard) A. Richard (93.75%) (Table 3).
The most abundant, frequent, and ubiquitous species of Lonchaeidae were Neosilba zadolicha McAlpine & Steyskal, Neosilba pendula (Bezzi), and the recently described Neosilba inesperata Strikis & Prado (2009), which colonized 36, 18, and 14 hosts, respectively (Tables 3).
TABLE 2.
TAXONS OF PLANTS (ANGIOSPERMAE), AND PATTERNS OF RELATIONSHIP WITH SPECIES OF FRUIT FLIES (DIPTERA: TEPHRITIDAE) IN 3 ENVIRONMENTS IN SOUTH PANTANAL REGION, BRAZIL (APR 1998 TO AUG 2000, OCT 2003, AND OCT 2004). ENVIRONMENT LEGEND: C = CERRADO, S = SIERRA, P = PANTANAL, AND ORIGIN OF THE SPECIES OF PLANTS: N = NATIVE, E = EXOTIC.
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TABLE 3.
TAXA OF PLANTS (ANGIOSPERMAE), AND PATTERNS OF RELATIONSHIP WITH SPECIES OF LANCE FLIES (DIPTERA: LONCHAEIDAE) IN 3 ENVIRONMENTS IN SOUTH PANTANAL REGION, BRAZIL (APR 1998 TO AUG 2000, OCT 2003, AND OCT 2004). LEGEND: C = CERRADO, S = SIERRA, P = PANTANAL; ORIGIN OF PLNATS: N = NATIVE, E = EXOTIC.
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The infestation rate for the total of larvae (L3) in the 92 species of plants was 78.38% by tephritids and 21.62% by lonchaeids (Table 4).
Larval Viability and Duration of Pupal Period. The relative viability of the larvae from both families of Tephritoidea was 59.73% for the tephritids, and 60.72% for the lonchaeids (Table 4). The pupal period (on average) for Anastrepha species, C. capitata (including male and female), and Neosilba species were 15.85 d, 10.62 d, and 12.21 d, respectively (Table 5). Among Anastrepha species, A. hastata Stone had the longest pupal period (21.92 d), and A. zenildae (mean 13.61 d) the shortest among all species of Anastrepha. The females of C. capitata emerged after 11.03 d. Among the lonchaeids, N. inesperata had the longest pupal period (13.43 d), and Neosilba glaberrima (Wiedemann) the shortest, emerging at 11.48 d (Table 6).
DISCUSSION
From the 53 species of fruits infested by frugivorous larvae of Tephritoidea, 25 were attacked by Tephritidae plus Lonchaeidae, 23 only by Neosilba species (Lonchaeidae), and 5 only by Tephritidae species. The plant species infested by the highest diversity of Tephritoidea species were Psidium guajava (8 spp., 5 of Tephritidae and 3 of Lonchaeidae), Terminalia catappa (8 spp., 3 of Tephritidae and 5 of Lonchaeidae), and Pouteria ramiflora (Martius) Radlkofer (7 spp., 3 of Tephritidae and 4 of Lonchaeidae) (Table 2).
The species Ceratitis capitata, A. sororcula, A. zenildae, and Anastrepha alveatoides Blanchard were the most numerically abundant. The species with the widest host ranges were A. sororcula, C. capitata, and A. zenildae. Ceratitis capitata and A. sororcula both infested 10 species of host fruits. Ceratitis capitata was exclusive in Chrysophyllum gonocarpum and Hancornia speciosa. Anastrepha sororcula was the only species reared from fruits of Casearia sylvestris Swartz, Physalis angulata, and Byrsonima orbignyana A. Jussieu, and A. obliqua irefested 7 species of host fruits (Table 2).
TABLE 4.
INFESTATION RATES BY LARVAE (L3) OF FRUGIVOROUS TEPHRITOIDEA (DIPTERA), VIABILITY (%), AND RELATIVE ABUNDANCE (%) IN HOST FRUITS FROM SOUTH PANTANAL REGION, BRAZIL (APR 1998 TO AUG 2000, OCT 2003, AND OCT 2004)
The highest general infestation rates by larvae occurred in T. catappa (0.41 L3/g of fruit), A. cuyabensis (0.34 L3/g of fruit) and P. kennedyanum (0.31 L3/g of fruit). The viability for all the larvae (Tephritidae plus Lonchaeidae) was 59.95%. The host fruits with highest viability rates were Physalis angulata (99.55%), Licania tomentosa (96.30%), and Andira cuyabensis (94.11%) (Table 2).
The host fruits with the highest rates of infestation (L3/g) were Terminalia catappa (Combretaceae, Afrotropical), A. cuyabensis (Fabaceae, Neotropical), and Psidium kennedyanum (Myrtaceae, Neotropical) (Table 2). Uramoto et al. (2008) also found high levels of infestation by Tephritidae in native Myrtaceae from the Atlantic Forest in the state of Espírito Santo, Brazil. Fruits of Neotropical species of Myrtaceae are known to keep a high diversity of Tephritoidea in natural environments (Uchôa et al. 2002; Uramoto et al. 2008), probably, because their fruits are nutritionally adequate, and some species (e.g., Psidium spp.), produce fruit more than a season during the year.
Tephritidae. The host fruits with highest Tephritidae diversity were Psidium guajava, and P. kennedyanum (Myrtaceae, Neotropical), with 5 spp. each, and L. tomentosa (Chrysobalanaceae, Neotropical), infested by 3 species (Table 2).
The species of Tephritidae were more abundant than those of Lonchaeidae for both number of larvae and adults. However, the Lonchaeidae larvae were more frequently collected. While Tephritidae were obtained on 73 fruit sampling expeditions (Table 2), Lonchaeidae were collected on 85 of 184 sampling trips (Table 3).
TABLE 5.
PUPAL PERIODS FOR GENERA OF FRUGIVOROUS FLIES (DIPTERA: TEPHRITOIDEA) IN HOST FRUITS SAMPLED IN 3 ENVIRONMENTS IN SOUTH PANTANAL REGION, BRAZIL (APR 1998 TO AUG 2000, OCT 2003, AND OCT 2004).
Lonchaeidae. The host fruits with highest diversity of Neosilba species were Pouteria torta (Martius) Radlkofer (5 spp.) and T. catappa (5 spp.). The most abundant species of Lonchaeidae were Neosilba zadolicha Steyskal & McAlpine, and N. pendula (Table 3). Although in a old paper, the species of Neosilba McAlpine, as Silba (Lonchaeidae), were considered as secondary fruit infesters that use the oviposition wounds made by tephritids to gain access to fruit tissue (Souza et al. 1983), results in other papers are in disagree with this information (Malavasi & Morgante 1980; Norrbom & McAlpine 1997; Uchôa & Zucchi 1999; Uchôa et al. 2002; Strikis & Lerena 2009; Uchôa & Nicácio 2010). In fact, in this study a large numbers of fruit/lonchaeid combinations that have no associated tephritids suggest that that generalization can be reconsidered. Of course, Neosilba species have a less sclerotized aculeus in comparation to that of Anastrepha and Ceratitis species (tephritids), but further studies are needed to clarify if the females of Neosilba species are able to use muscular power to insert their eggs inside the fruit pulp or if the newlyhatched larvae are able to bore the fruit peel to reach and feed inside the fruits.
The species of Neosilba were characterized as polyphagous (sensu Aluja & Mangan 2008). Neosilba zadolicha, N. pendula, and N. inesperata were the species with the highest number of host plants (36, 18, and 14 species, respectively). These results show the potential of the species of Neosilba as pests of fruits and vegetables in the Neotropical Region (Uchôa et al. 2002; Strikis & Prado 2005; Strikis & Prado 2009; Strikis & Lerena 2009).
The highest rates of infestation by Lonchaeidae (L3/g) occurred in Duguetia furfuracea (Annonaceae, Neotropical), Physalis angulata (Pantropical), and Solanum sisymbriifolium Lamarck (Solanaceae, Neotropical), respectively D. furfuracea was the only host fruit in which a seed-feeding species, a wasp, Bephratelloides sp. (Eurytomidae, Hymenoptera), was obtained. Species of Bephratelloides are common pests on Annona seeds in the Neotropics (Peña & Bennet 1995).
The general pattern for Lonchaeidae was that the females of all Neosilba species emerged earlier than the conspecific males and on average, the pupal period was 12.21 d, differing significantly from the pupal period of Tephritidae species (Table 4).
Tephritidae versus Lonchaeidae. In this study, Neosilba species (Lonchaeidae) were the only tephritoids infesting species of Annonaceae, Arecaceae, Lauraceae, Loganiaceae, Rubiaceae, Rutaceae, and Passifloraceae. On the other hand, the tephritids were exclusive only in Clusiaceae and Euphorbiaceae. However, this does not mean that the former plant taxa could not be infested by tephritids nor that Clusiaceae and Euphorbiaceae are never adequate host fruits for lonchaeids either. For example, different Neosilba species have been reared from fruits or apical and axilary buds of Manihot esculenta Crantz (Euphorbiaceae), C. capitata and A. turpiniae were reared from fruits of Citrus sinensis (Rutaceae) (Uchôa et al. 2002), and A. fraterculus was reared from fruits of Rollinia laurifolia Schlechtendal (Annonaceae) (Uramoto et al. 2008).
In previous studies, a total of 35 plant species were evaluated for frugivorous insects in areas of Cerrado near the Pantanal, and frugivorous Tephritoidea were found in fruits of 29 species from 16 families. In that study 16 species of Anastrepha, C. capitata (Tephritidae), and 3 species of Lonchaeidae were recovered from their host fruits (Uchôa et al. 2002). Herein, in addition to the species found by Uchôa et al. (2002), 9 different species of Tephritidae were associated with their host plants (Anastrepha alveatoides, A. distincta Greene, A. hastata, A. leptozona Hendel, A. macrura Hendel, A. rheediae Stone, A. serpentina (Wiedemann), A. undosa, and A. zernyi Lima), and new association was found between C. capitata and Hancornia speciosa (Apocynaceae).
TABLE 6.
NUMBER OF HOST FRUIT SAMPLES (ANGIOSPERMAE) FROM THE SOUTH PANTANAL REGION AND NEIGHBORHOOD, BRAZIL, NUMBER AND RELATIVE PERCENT OF REARED FLIES BY GENERA AND SPECIES (TEPHRITOIDEA: DIPTERA), THEIR PUPATION PERIOD (MEAN IN DAYS), STANDARD DEVIATION, AND COMPARISON OF MEANS (APR 1998 TO AUG 2000, OCT 2003, AND OCT 2004).
Anastrepha was the most abundant Tephritoidea genus reared from naturally infested host fruits in this study. A similar pattern was found by Malavasi et al. (1980) in a survey including 55 fruit species sampled in several states of Brazil. Herein, A. sororcula and A. zenildae were the most frequent (percentage of individual of a fly species in relation to the total number of individuals of all fruit fly species) and abundant (relationship of the number of individuals of each species of fruit fly by each species of host fruits) Anastrepha species.
The species of Neosilba were more generalists. They attacked more hosts (48) than the Tephritidae (30). Similar results were obtained in a previous survey in the Cerrado of Mato Grosso do Sul, Brazil (Uchôa et al. 2002).
Larval viability was lower for tephritids (59.73%) than for lonchaeids (60.72%) (Table 4). In this study the larval viability of the tephritids was higher than that reported by Malavasi & Morgante (1980) (10%). This suggests that the methodology herein employed is adequate for obtaining frugivorous insects.
The higher viability of the pre-puparial larvae of Lonchaeidae species is probably due to the lower parasitism rates in this taxon than in Tephritidae species (M. A. Uchôa et al., unpublished data). No adult emerged from 40.05% of the prepuparial larvae of Tephritoidea. Despite of the lower viability (59.73%) of Anastrepha spp. and Ceratitis capitata larvae, their relative abundance in fruit infestation was higher (78.1%), in comparison with Lonchaeidae species (21.9%, Table 4).
The genera of Tephritoidea showed a highly significant difference in their pupation period. The species of Anastrepha had the longest pupation period, followed by Neosilba spp., and C. capitata, respectively The males of all Tephritidae species (16 Anastrepha spp. and C. capitata) emerged before their conspecifics females. Although mating systems of the Lonchaeidae must be more ancient in relation to that of tephritids, because the lonchaeids are among the most primitive Tephritoidea, the opposite pattern was found in the species of Neosilba. All females emerged earlier than the conspecifics males, although the difference was not statistically significant (Table 5).
The average pupation period for the 20 species of frugivorous flies evaluated in this study showed significant differences among 3 groups of species: (Anastrepha hastata Stone to Anastrepha fraterculus (Wiedemann)), (Anastrepha rheediae Stone to Anastrepha striata Schiner), and (Neosilba certa (Walker) to Ceratitis capitata), ranging from 21.92 d for A. hastata to 11.03 d for C. capitata (Table 6). In this analysis, Anastrepha macrura Hendel (22 d) (1♀), Anastrepha n. sp. aff pickeli Lima (18.33 d) (4♀), Anastrepha distincta Greene (13 d) (3 ♀), Lonchaea sp. (7.0 d) (1 ♀), and Neosilba pradoi Strikis & Lerena (16.80 d) (1 ♂), were not included, because each of them occurred in fewer than 3 fruit samples.
Facholi-Bendassolli & Uchôa (2006) studied the reproductive behavior of Anastrepha sororcula and found a marked protandry: males reached sexual maturity at an average of 11.75 d after emergence, and females became sexually mature, on average, 19 d after emergence. There are no reports on the sexual maturation of Neosilba species, but as evidenced in this study, it is probable that the females of Neosilba reached sexual maturity earlier than the conspecific males, a case of protogyny. However, a more specific study is necessary to answer this question satisfactorily. The asynchronous development between males and females of these insects may play an important evolutionary role. If males and females of the same progeny (offspring) reach sexual maturity at different times in nature, the chance of inbred mating decreases, which increases the genetic variability of the species (Futuyma 1992).
The average for the pupal period (interval between L3 exiting from fruits and emergence of adults) showed significant differences between the evaluated genera: Anastrepha (15.85 d), Ceratitis (10.62 d, mean between ♂ ♂ and ♀ ♀) (Tephritidae), and Neosilba (12.21 d, mean between ♂ ♂ and ♀ ♀ (Table 5)). However, when this period was compared between the species of the 3 genera, there is no standard pattern for each genus, because there are strong variations among the congeneric species (Table 6). We do not know if this difference were influenced by the differences in ambient conditions from the sites of fruits collections.
On average, the duration of the pupal period showed highly significant differences between C. capitata and the Anastrepha species. Ceratitis capitata emerged after 10.62 d and the Anastrepha species after 15.85 d. The Tephritidae with the highest mean for pupal period were Anastrepha hastata Stone (21.92 d) and Anastrepha zernyi Lima (20.90 d). Ceratitis capitata (♀♀)and A. zenildae had the shortest pupal periods of 11.03 and 13.61 d, respectively (Table 6). The pupal period for C. capitata obtained in this study (10.62 d) is similar to that found by Papadopoulos et al. (2002), 10 d under laboratory conditions (25°C 2 and 65% 5 RH (relative humidity).
ACKNOWLEDGMENTS
We thank the botanists: Ubirazilda Maria Rezende from the Herbarium of the Universidade Federal de Mato Grosso do Sul (UFMS) at Campo Grande-MS, and José Rubens Pirani from the Herbarium of the Universidade de São Paulo (USP, São Paulo), for identification of plant species; Pedro Carlos Strikis (UNICAMP, Campinas-SP), for identification of Lonchaeidae; Conselho Nacional de Desenvolvimento Cientifíco e Tecnológico (CNPq), for the grant award to J. N Nicácio; Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), for the postdoctoral fellowship (Process N°. 1030/09-4 BEX) to M. A. Uchôa, and Allen L. Norrbom and James L. Nation, for valuable suggestions in the manuscript, making it more comprehensive.
