Species Diversity of Frugivorous Flies (Diptera: Tephritoidea) from Hosts in the Cerrado of the State of Mato Grosso do Sul, Brazil

Diversidade de Espécies de Moscas Frugívoras (Diptera: Tephritoidea) em Hospedeiros do Cerrado do Estado de Mato Grosso do Sul

ECOLOGY, BEHAVIOR AND BIONOMICS

Species Diversity of Frugivorous Flies (Diptera: Tephritoidea) from Hosts in the Cerrado of the State of Mato Grosso do Sul, Brazil

MANOEL A. UCHÔA-FERNANDES¹, ISAIAS DE OLIVEIRA¹, ROSA M.S. MOLINA¹ AND ROBERTO A. ZUCCHI²

¹Depto. Ciências Biológicas, Universidade Federal de Mato Grosso do Sul (UFMS). Rodovia Dourados-Itahum, km 12

79804-970, Cidade Universitária, Dourados, MS, Brasil, e-mail: [e-mail]

²Depto. Entomologia, Fitopatologia e Zoologia Agrícola, ESALQ/USP, C. postal 9, 13418-900, Piracicaba, SP, Brasil

e-mail: [e-mail]

Diversidade de Espécies de Moscas Frugívoras (Diptera: Tephritoidea) em Hospedeiros do Cerrado do Estado de Mato Grosso do Sul

RESUMO - Neste trabalho foram amostradas 35 espécies de frutos do cerrado em sete municípios do estado de Mato Grosso do Sul (janeiro de 1993 a março de 1997) para avaliar a infestação por moscas frugívoras. Ocorreram espécies de seis gêneros de Tephritoidea - Anastrepha Schiner, Ceratitis MacLeay (Tephritidae); Dasiops Rondani, Lonchaea Fallén, Neosilba McAlpine (Lonchaeidae) e Notogramma Loew (Otitidae), em 29 espécies de frutos. As moscas-das-frutas (Tephritidae) colonizaram 19 hospedeiros e foram representadas por 11 espécies: Anastrepha fraterculus (Wied.), A. grandis (Macquart), A. montei Lima, A. obliqua (Macquart), A. pickeli Lima, A. sororcula Zucchi, A. striata Schiner, A. turpiniae Stone, A. zenildae Zucchi, Anastrepha sp. n. e Ceratitis capitata (Wied.). De Lonchaeidae foram obtidos: Dasiops inedulis Steyskal, Dasiops spp., Lonchaea spp., Neosilba zadolicha McAlpine e Neosilba spp. As espécies de Neosilba foram as mais abundantes moscas frugívoras, ocorrendo em 22 hospedeiros. Notogramma foi o único gênero de Otitidae obtido. É discutida a associação entre moscas frugívoras e frutos hospedeiros.

PALAVRAS-CHAVE: Biodiversidade, mosca-das-frutas, Lonchaeidae, frugivoria, Brasil-Central

ABSTRACT - Thirty-five fruit species were sampled in seven municipalities located in the cerrado of the state of Mato Grosso do Sul (January 1993 to March 1997) in a study to evaluate the infestation by frugivorous flies. Species of six genera of Tephritoidea were reared from 29 host fruits: Anastrepha Schiner, Ceratitis MacLeay (Tephritidae); Dasiops Rondani, Lonchaea Fallén, Neosilba McAlpine, (Lonchaeidae) and Notogramma Loew (Otitidae). Fruit flies (Tephritidae) were found in 19 host fruits and were represented by 11 species: Anastrepha fraterculus (Wied.), A. grandis (Macquart), A. montei Lima, A. obliqua (Macquart), A. pickeli Lima, A. sororcula Zucchi, A. striata Schiner, A. turpiniae Stone, A. zenildae Zucchi, Anastrepha n. sp. and Ceratitis capitata (Wied.). From Lonchaeidae were reared: Dasiops inedulis Steyskal, Dasiops spp., Lonchaea spp., Neosilba zadolicha McAlpine and Neosilba spp. The species of Neosilba were the most abundant, occourring in 22 host fruits. Notogramma was the only genus of Otitidae obtained. The association between frugivorous flies and the fruit species is discussed.

KEY WORDS: Biodiversity, fruit fly, frugivory, Lonchaeidae, Mid-Western Brazil

Pomiculture is a relatively new economic activity in the state of Mato Grosso do Sul, Brazil, but with great potential. The climatic condition in this state is favorable for growing fruits and vegetables, with no interruption throughout the year, for several species of agricultural importance. The most cultivated fruits are: banana, citrus, watermelon, melon, pineapple, and mango, but there are also commercial orchards of avocado, Barbados cherry, cashew, guava, papaya, passion fruit, peach, and grape, among others. According to IBGE (1996) the area under cultivation with citrus (orange, lime and tangerine) in 1993-1994 was 777 ha. The largest producers are in the municipalities of Terenos and Coxim.

Fruit flies of the genus Anastrepha and Ceratitis capitata (Tephritidae) are the most important pests to the Brazilian pomiculture (Zucchi 2000). In Mid-Western Brazil, at least in the states of Mato Grosso do Sul and Goiás, besides tephritids, species of the genera Dasiops and Neosilba (Lonchaeidae) are also important pests in citrus, guava, papaya, Barbados cherry, passion fruit and other commercial fruits (Veloso et al. 1994, Uchôa-Fernandes & Zucchi 1999). Integrated pest management has been more difficult by the lack of basic studies on taxonomy, biology and ecology. In Brazil, records on the genera of Lonchaeidae associated with fruits are scarce. Regional surveys are very important because they can provide basic information for managing insect pest populations and their natural enemies.

The objective of this paper is to assess the diversity of fruit fly species and lonchaeids occurring in wild and cultivated fruits in the cerrado of the state of Mato Grosso do Sul.

Material and Methods

Colecting Host Fruits. Fruits, pods or flowers from 35 species (Table 1) were collected, from January 1993 to March 1997, in the cerrado of the municipalities of Anastácio (20º 31' 36'' S, 55º 50' 12'' W, 170 m), Aquidauana (20º 39' S, 55º 19' 50'' W, 173 m), Coxim (18º 30' 12'' S, 54º 45' W, 205 m), Dois Irmãos do Buriti (20º 39' S, 55º 19' 50'' W, 315 m), Nioaque (21º 20' S, 55º 49' 45'' W, 205 m), Rochedo (19º 57' 30'' S, 54º 53' 10'' W, 398m) and Terenos (20º 26' 12'' S, 54º 04' 54'' W, 308m). These cities are located in the major fruit producing areas in the state of Mato Grosso do Sul. Collecting fruits, and fruit fly and lonchaeid rearings were done according to Uchôa-Fernandes & Zucchi (1999).

Fly Identification. The adults were identified in the Departamento de Entomologia, Fitopatologia e Zoologia Agrícola, Escola Superior de Agricultura "Luiz de Queiroz" (ESALQ), Universidade de São Paulo (USP), Piracicaba-SP, by the first author. For Anastrepha Schiner, mainly characteristics of the female aculeus and the chromatic patterns of the body and wings were considered (Lima 1934, Stone 1942, Blanchard 1961, Steyskal 1977, Zucchi 2000).

Ceratitis capitata (Wied.) is the only species of this genus in Brazil and, it is easily recognized by the diagnosis discussed by Foote (1980). The genera of Lonchaeidae were identified using keys and original descriptions (Korytkowski & Ojeda 1971, McAlpine & Steyskal 1982, McAlpine 1987, Norrbom & McAlpine 1997) and Notogramma cimiciforme Loew (Otitidae) was identified by Dr. Allen L. Norrbom (National Museum of Natural History, Washington-D.C., USA). Neosilba zadolicha McAlpine was identified by means of morphology and male terminalia (McAlpine & Steyskal 1982) and Dasiops inedulis Steyskal, based on aculeus shape (Norrbom & McAlpine 1997).

Plant species were identified by botanists at the Herbário Central da Universidade Federal de Mato Grosso do Sul (UFMS) and Departamento de Botânica, Universidade de São Paulo (USP) in São Paulo. Voucher specimens of the insects were deposited at Coleção Zoológica (ZUFMS), Universidade Federal de Mato Grosso do Sul (UFMS) in Campo Grande-MS and at Coleção Entomológica do Departamento de Entomologia, Fitopatologia e Zoologia Agrícola, ESALQ-USP in Piracicaba-SP. Voucher specimens of host plants were deposited at the Herbário Central da UFMS in Campo Grande-MS and at Coleção de Botânica, Departamento de Botânica, USP, in São Paulo-SP.

Results and Discussion

Host Fruits. Species of six genera of frugivorous Tephritoidea were reared: Anastrepha, Ceratitis (Tephritidae), Dasiops, Lonchaea, Neosilba (Lonchaeidae), Notogramma and other unidentified genera of Otitidae. The highest number of specimens belong to Neosilba and Anastrepha (Table 2). Out of 35 fruit species sampled in 18 families, were obtained frugivorous flies from 29 plant species (Tables 1 and ³). Only in six fruit species no adult flies were collected: Melicoccus lepidopetalus, Rollinia sp., Dipterix alata, Ficus sp., Ricinus communis and Tamarindus indica (Tables 1 and ⁴).

Tephritidae. Ten Anastrepha species were collected: A. fraterculus (Wied.), A. grandis (Macquart), A. montei Lima, A. obliqua (Macquart), A. pickeli Lima, A. sororcula Zucchi, A. striata Schiner, A. turpiniae Stone, A. zenildae Zucchi and Anastrepha n. sp. (^{Table 3}). The ocurrence of these species besides C. capitata (Wied.) was reported recently in the state of Mato Grosso do Sul (Uchôa-Fernandes & Zucchi 2000).

The tephritids (Anastrepha spp. and C. capitata) were reared from 19 host fruits. In the genus Anastrepha, whose identification is based on the female, A. sororcula was the species with the largest abundance (1,315), followed by A. obliqua (951) and A. turpiniae (165). The largest number of individuals of those three species was obtained from two hosts: guava (Psidium guajava L.), for A. sororcula and A. turpiniae, and hog plum (Spondias lutea L.), for A. obliqua (^{Table 3}). A. sororcula was more common than A. fraterculus in four municipalities sampled: Anastácio, Aquidauana, Coxim and Terenos (Table 1), where only nine specimens of A. fraterculus were collected, in spite of the fact that it is a common species in guava orchards in other Brazilian regions (Nascimento et al. 1982).

A. sororcula, followed by A. turpiniae and A. striata, were more common in guava than A. zenildae, which infests largely guava in the semi-arid Northeast of Brazil (Araújo et al. 2000, Canal et al. 1998a). Also, in Nova Soure (BA), in a transition between Atlantic forest and the caatinga, most specimens of Anastrepha caught in traps were A. sororcula (A.S. Nascimento, pers. comm.). Similar to other Brazilian regions (Bressan & Teles 1991, Zahler 1991, Morgante 1991, Aguiar-Menezes & Menezes 1996), A. obliqua also prefers Anacardiaceae fruits in the cerrado of Mato Grosso do Sul.

Mediterranean fruit fly, C. capitata, is widespread in Brazil: Bahia, Minas Gerais, Rio de Janeiro, São Paulo, Paraná, Santa Catarina, Rio Grande do Sul, Maranhão, Pernanbuco, Ceará, Rio Grande do Norte, Espírito Santo, Goiás (Malavasi et al. 2000), Mato Grosso do Sul (Uchôa-Fernandes & Zucchi 2000), Rondônia (Ronchi-Teles & Silva 1996), Pará (Silva et al. 1998), and Amapá (Silva & Ronchi-Teles 2000). This species is distributed throughout Brazil and it was the fruit fly species with the largest number of individuls reared from the fruits (^{Table 3}). For C. capitata the major host was tropical almond (Terminalia catappa L.), native to the Malay Peninsula (Liquido et al. 1991), to which medfly seems to present strong adaptation. The infestation by medfly of T. catappa also occurred in several Brazilian regions (Morgante 1991, Ronchi-Teles & Silva 1996, Canal et al. 1998b, Veloso et al. 1994) and around the world (Liquido et al. 1991). Medfly shows strong colonization in guava, P. guajava (native) but also in orange, C. sinensis, (exotic) as well.

The ocurrence of many individuals of medfly in guava shows a good adaptation also in Mid-Western Brazil. Medfly had higher infestation in guavas than the native species A. fraterculus and A. zenildae. However, it should be pointed out that most of the samples were collected in urban areas. It is known that C. capitata in urban areas tends to overcome the native species of the genus Anastrepha (Haji et al. 1991, Harris 1993, Canal et al. 1998b).

The occurrence of C. capitata in Inga laurina is a new record. In Brazil species of Inga are usually attacked by A. distincta Greene, which occurs in the surveyed region and was caught in McPhail traps (Uchôa-Fernandes & Zucchi 2000), but has not been reared from fruits yet. However, the pods of I. laurina attacked by medfly were collected in urban areas of Anastácio and Aquidauana. Only species of Neosilba emerged from I. laurina pods sampled in the forests.

Guava was the host with the largest tephritid diversity: six species of Anastrepha and C. capitata from which emerged the largest number of Anastrepha specimens (Table 1). A. obliqua and C. capitata, followed by A. sororcula, infested the largest number of host fruit species. Surprisingly, A. fraterculus, a generalist species with wide geographical range in south of Brazil, was obtained only from two host fruits (^{Table 3}).

Lonchaeidae. The species of Neosilba had an absolute predominance over all frugivorous flies, mainly in the orange, Citrus sinensis (L.), tangerine, C. reticulata (L.) and "pequi", Caryocar brasiliense Camb. Species of Neosilba occurred in 22 host fruit species (^{Table 3}), in the seven municipalities sampled (Table 2). The species of the other genera were rarely reared from fruits. Except for Dasiops inedulis and Neosilba zadolicha, other species of Lonchaeidae were not identified due to the lack of taxonomic reviews for the neotropical lonchaeids. Only one specimen of Dasiops sp. emerged from Spondias purpurea (red mombim) and 11 individuals of Lonchaea spp. were reared in wild cassava fruits - Manihot sp. (Tables 1 e ³).

In spite of the economic importance of some species of Lonchaeidae that occur as pests on fruit and vegetables in several countries, such as Colombia (Steyskal 1978, 1980, Chacon & Rojas 1984, Peñaranda et al. 1986), Peru (Korytkowski & Ojeda 1971), Porto Rico (Romero & Ruppel 1962), Costa Rica (Sánchez et al. 1991) and USA (Moffitt & Yaruss 1961, Norrbom & McAlpine 1997), the knowledge of these dipterous is still incipient. Also in Brazil, research on the damage in fruits and vegetables by lonchaeids is very scarce.

The number of Neosilba reared from citrus fruits in the sites surveyed is quite superior (3,360 adults) to the number of Anastrepha (2) and C. capitata (66) (Table 1). These results suggest the economic importance of Neosilba sp. as a pest in citrus fruits. Other authors also reported infestation by lonchaeids in oranges (Malavasi & Morgante 1980, Raga et al. 1997) and in coffee berries (Raga et al. 1996) in the state of São Paulo. Studies should be made to evaluate the importance of Neosilba for pomiculture in Brazil.

Larvae of N. zadolicha attack fruits of a wild species of passion fruit (Passiflora sp., Passifloraceae) and larvae of Dasiops inedulis Steyskal infest floral buds of that same species (Table 1). According to Norrbom & McAlpine (1997), at least 12 species of Dasiops feed in plants of the genus Passiflora. D. inedulis is considered an important pest in P. edulis and P. quadrangularis L., sweet passion fruit, in the USA (Norrbom & McAlpine 1997) and Colombia (Peñaranda et al. 1986). Its larvae develop in floral buds, feeding in the ovaries of the flowers, causing the fall of the floral buds and new fruits (Peñaranda et al. 1986).

Otitidae. Some 319 otitids were reared (Table 2), but only Notogramma cimiciforme Loew was identified. It feeds on sour passion fruit, P. edulis and in a wild Passiflora sp., representing 28% of all Otitidae obtained (^{Table 3}). N. cimiciforme presents a wide geographical distribution, occurring in the USA, from Mexico to Panama, Cuba, Jamaica, Guyana, Venezuela, Colombia, Brazil, Ecuador, Peru and, according to Steyskal (1968), it was introduced in Oceania.

Infestation Indices and Larval Viability. The highest infestation indices, when considering the number of third instar larvae (L3) by fruit, were obtained in squash (Cucurbita moschata) infested exclusively by A. grandis; mango (Mangifera indica) - infested by A. obliqua, A. turpiniae, C. capitata and Neosilba spp.; "pequi"(Caryocar brasiliense) attacked almost exclusively by Neosilba spp. and the tropical almond (Terminalia catappa), highly infested by C. capitata (^{Tables 3} and ⁴). In mango the losses can be attributed mainly to A. obliqua, because 82% of all frugivorous flies in this fruit belong to the West Indian fruit fly (Table 1). If the index L3/kg of fruits is considered, the largest infestation levels occurred in hog plum (Spondias lutea), tropical almond (T. catappa), cassava (Manihot esculenta), "cagaita" (Eugenia dysinterica), red mombim (Spondias purpurea) and "araçá" (Psidium sp.), respectively. In that last case, there is a tendency of high indices in fruit of lower biomass (^{Table 4}), according to Malavasi & Morgante observations (1980).

Although the biomass of floral buds of wild passion fruit has been very low, only 0.116 g, a very high index of infestation was verified (448.27 L3/kg), with low larval viability (9.6%), and all D. inedulis. The largest rates of larval viability occurred in sugar apple (A. squamosa) infested by Neosilba spp.; in squash by A. grandis; in "juá" by species of Neosilba; in sour passion fruit by the otitid N. cimiciforme; in tangerine by Neosilba spp. and in guava by several Anastrepha species (^{Table 4}), with the predominace of A. sororcula. In guava, C. capitata and Neosilba spp. also occurred (^{Table 3}).

New Records. This is the first large survey of frugivorous flies in the state of Mato Grosso do Sul (MS). Before this work, as published in Uchôa-Fernandes & Zucchi (2000), only A. rheediae was recorded in MS (Malavasi et al. 1980). Including also the state of Mato Grosso (MT), because the split from that state occurred in 1977, the number of Anastrepha species recorded for the whole region was nine: one in MS (A. rheediae) and eight in MT - A. grandis, A. punctata (as A. minor), collected in Fazenda Murtinho - MS, A. dissimilis, A. leptozona and A. mixta, collected in the district of Utiariti, municipality of Diamantino - MT; A. sororcula, A. obliqua and A. daciformis (without record of locality, Uchôa-Fernandes & Zucchi 2000). These are all the records on frugivorous Tephritoidea and its hosts in these two Brazilian states. There was no record of medfly in MS until the beginning of this work (1992).

A. sororcula in jambolan plum (Syzygium cumini) and in "pequi" (Caryocar brasiliense) and A. turpiniae in red mombim (S. purpurea); mango (M. indica) and orange (C. sinensis) are the first records of hosts for these species (Table 1). Also it was observed that species of three genera: Dasiops, Lonchaea and Neosilba (Lonchaeidae) are associated with host fruits in Mato Grosso do Sul, with predominance of the species of Neosilba.

Larvae of Neosilba spp. were found in a larger number of host fruit species than fruit fly larvae. The diversity of fruit fly species in the cerrado of MS is high in relation to that of other areas studied in Brazil.

Eleven species of parasitoids were detected attacking larvae or pupae of frugivorous flies. Five species of Braconidae parasitize tephritids; four Eucoilinae species (Figitidae) attack larvae of Neosilba (Lonchaeidae), including a new species of Trybliographa (T. infuscata Gallardo, Díaz & Uchôa-Fernandes), and two pteromalid species are associated with pupae of both families of Tephritoidea (Uchôa-Fernandes et al. in prep.).

Acknowledgments

We thank MSc. Ubirazilda Maria Resende (Herbário Central, Universidade Federal de Mato Grosso do Sul (UFMS), Campo Grande-MS and Dr. José Rubens Pirani (Departamento de Botânica, Universidade de São Paulo (USP), for the identification of the plants and Dr. Allen L. Norrbom (National Museum of Natural History, Washington-D.C., USA), for the identification of N. cimiciforme and for the confirmation of the identities of D. inedulis and N. zadolicha, and Professor Elsbeth A. Flunker (WI, USA) for the revision of the version in English.

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Received 22/10/01. Accepted 20/09/02.

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Publication Dates

• Publication in this collection
  20 Feb 2003
• Date of issue
  Oct 2002

History

• Accepted
  20 Sept 2002
• Received
  22 Oct 2001