Distribution and host data of Lonchaeidae species (Diptera: Tephritoidea) in the state of Amapá, Brazil, are presented. Adults of 10 species in the genera Neosilba, Dasiops, and Lonchaea were reared from 23 plant species in 18 families. Neosilba laura Strikis and Neosilba parapeltae Strikis are reported for the first time in the Amazon, and Dasiops inedulis Steyskal and Neosilba perezi Romero & Ruppel are reported for the first time in Amapá State. Additionally, 24 new host associations are documented.
Lonchaeids (Diptera: Lonchaeidae), commonly known as lance flies, are minute insects (3-6 mm long) with glossy, dark blue bodies and hyaline or very pale brown wings, found mainly in humid or shaded places. Larvae are associated with decomposing organic matter, mainly wood, flowers, and fruits. However, some species are primary invaders of fruits and flower buds (McAlpine 1961; Norrbom & McAlpine 1997) and may have a significant economic impact on fruit crops (MacGowan & Okamoto 2013).
Lonchaeidae contain approximately 545 species, grouped into 2 subfamilies (Dasiopinae and Lonchaeinae) and 8 genera (Chaetolonchaea Czerny, Dasiops Rondani, Earomyia Zetterstedt, Lamprolonchaea Bezzi, Lonchaea Fallén, Neosilba McAlpine, Protearomyia McAlpine, and Silba Macquart). The subgenus Setisquamalonchaea Morge is currently considered synonymous with Silba (MacGowan & Okamoto 2013; MacGowan 2015).
Tephritidae and Lonchaeidae are the most and second-most, respectively, economically important dipteran families in South America, and some species of Dasiops and Neosilba are primary pests of fruit crops. For plant species of economic importance, including citrus (Citrus species; Sapindales: Rutaceae), ambarella (Spondias dulcis Soland. ex Forst. f.; Sapindales: Anacardiaceae), and passionfruit (Passiflora species; Malpighiales: Passifloraceae), lonchaeids can be more abundant and more important as pests than Tephritidae (Uchôa 2012).
Although infestations of fruits of economic importance by lonchaeids have been reported in Brazil since the 1930s, these insects generally were neglected in surveys of fruit flies, mainly due to a lack of taxonomic knowledge. In the 1990s, the large number of lonchaeid puparia obtained in these surveys renewed interest in lonchaeid research, especially in southeastern Brazil (Araújo & Zucchi 2002). Recently, a number of studies on Lonchaeidae species have been conducted in Brazil, motivated by advances in taxonomic knowledge of Brazilian species. The species reported in Brazil belong to the genera Dasiops, Lonchaea, and Neosilba.
These studies have revealed that species of Neosilba are primary pests of certain crops, including cassava (Manihot esculenta Crantz; Malpighiales: Euphorbiaceae) (Lourenção et al. 1996); acerola (Malpighia emarginata [Moc. & Sessé] ex. DC; Malpighiales: Malpighiaceae) (Araújo & Zucchi 2002); citrus (Citrus species) (Uchôa-Fernandes et al. 2002, 2003); coffee (Coffea arabica L.; Gentianales: Rubiaceae) (Aguiar-Menezes et al. 2007); and tangerine (Citrus reticulata Blanco; Sapindales: Rutaceae) (Lopes et al. 2008). Dasiops frieseni Norrbom & McAlpine has been reported to damage fruits of sour passionfruit (Passiflora edulis Sims; Malpighiales: Passifloraceae) (Souza-Filho et al. 2002), and Dasiops inedulis Steyskal has been reported to damage passionfruit flower buds (Lunz et al. 2006).
Lonchaeids were first reported in the Brazilian Amazon in the state of Amazonas by Silva (1993), who reported species of Neosilba associated with 19 fruit-bearing species. Costa (2005) subsequently reported Neosilba major (Malloch), Neosilba zadolicha McAlpine & Steyskal, and Neosilba sp. in a study conducted at the Adolpho Ducke Forest Reserve, in the city of Manaus. New studies were completed more recently, contributing significantly to knowledge on Lonchaeidae in the Amazon (Querino et al. 2010; Strikis et al. 2011; Adaime et al. 2012; Deus et al. 2013).
Lonchaeids have numerous native and exotic hosts in the Brazilian Amazon, many species of which are found exclusively in forest environments. Neosilba glaberrima (Wiedemann) and N. zadolicha are the most polyphagous and widely distributed lonchaeid species in this region (Strikis et al. 2011). Despite an increase in research, little is known about the ecology and biology of lonchaeids. This study reports new findings on the distribution of Lonchaeidae species and their hosts in the Brazilian Amazon.
Materials and Methods
STUDY SITE
We conducted this study on 3 farms located in the municipalities of Mazagão, Porto Grande, and Santana, state of Amapá, Brazil (Fig. 1). All 3 properties contained commercial orchards with adjoining areas of native forest.
The area in Mazagão (0.1°S, 51.25°W) exhibits native floodplain forest vegetation, which undergoes daily flooding due to tides. Common species include Platymiscium duckei Huber (Fabales: Fabaceae), Virola surinamensis (Rolander) Warb. (Magnoliales: Myristicaeceae), Calycophyllum spruceanum (Benth.) Hook,f. ex K. Schum. (Gentianales: Rubiaceae), and Carapa guianensis Aubl. (Sapindales: Meliaceae). The commercial orchard area occupies an area of approximately 10 ha, with cultivated fruit trees including tahiti lime (Citrus aurantifolia Swingle var. ‘Tahiti'; Sapindales: Rutaceae), passionfruit (P. edulis), and soursop (Annona muricata L.; Magnoliales: Annonaceae), grown for the manufacture of fruit concentrate or to be sold in natura.
The area in Porto Grande (0.6°N, 51.45°W) exhibits dense forest vegetation, with numerous tree species, including Protium species (Sapindales: Burseraceae), Caryocar villosum (Aubl.) Pers. (Malpighiales: Caryocaraceae), and Dipteryx odorata (Aubl.) Willd. (Fabales: Fabaceae). The property is approximatly 100 ha, of which 30% is used for the cultivation of fruit trees, mainly hog plum (Spondias mombin Jacq.; Sapindales: Anacardiaceae), araza (Eugenia stipitata McVaugh; Myrtales: Myrtaceae), and soursop (A. muricata).
The area in Santana (0.03°S, 51.21°W) exhibits secondary forest vegetation, with Eschweilera tenuifolia Miers (Ericales: Lecythidaceae), Ficus pertusa L.f., (Rosales: Moraceae), and Pourouma guianensis Aubl. (Rosales: Urticaceae) as predominant species. The commercial orchard is approximately 20 ha, and the main species are acerola (M. emarginata), guava (Psidium guajava L.; Myrtales: Myrtaceae), and passionfruit (P. edulis). As classified by Köppen, the climate type at the study sites is Am, characterized as hot and humid with a short dry season in the spring. Rainfall is distributed bewteen 2 well-defined periods: a rainy season (Jan to Jul), which receives about 80% of all annual rainfall in the area, and a dry season (Aug to Dec). Temperatures are elevated throughout the year, with an annual average of 25 to 27 °C (low of 22 °C and high of 34 °C) (IBGE 2010).
FRUIT COLLECTION AND PROCESSING
Every fruit tree species in the orchards was sampled. Within the native vegetation areas, 1 parcel of 40 × 250 m (1 ha) was delimited in each area. Once per month from Jan to Dec 2012, fruits were collected from various plant species, either directly from the plant or by retrieving recently fallen fruit. Samples were transported in stackable plastic crates to the Entomology Laboratory at Embrapa Amapá, where the fruits were weighed on a digital scale. For preparation of the samples, the fruits were processed and individualized according to the sample size criterion established by Silva et al. (2011): 15 units, for small fruit; 10 units, for medium-sized fruit; and 3 units, for large or elongated fruit. In each sample, each individual fruit was considered as 1 subsample.
The collected fruits were placed either individually into tubular, transparent plastic vials (8 cm diameter ×× 6 cm height), with vented lids lined with organza; or, in the case of large or elongated fruit, on rectangular plastic trays (33 × 18 ×× 6 cm LWH), also covered with organza held in place by rubber bands. Both types of containers included a thin layer of sterilized sand as a substrate for pupation.
ACQUISITION OF PUPARIA AND ADULT INSECTS
Every 3 d, the sand was examined and lonchaeid puparia were removed with spatulas. The puparia were transferred into transparent plastic vials (8 cm diameter), with vented lids covered with organza, containing a thin layer of moistened vermiculite. The adult insects that emerged were killed, transferred to Eppendorf tubes containing 70% ethanol, and labeled for subsequent identification.
Identification of Insects
Specimens obtained were identified according to McAlpine & Steyskal (1982) and Strikis (2011).
Identification of Botanical Material
Branches with attached reproductive structures (flowers and/or fruits), were collected and vouchered as herbarium specimens using typical mounting and preservation techniques (Fidalgo & Bononi 1984). Plant species was identified with identification keys and by comparison with specimens available at the Herbário Amapaense, the herbarium at the Amapá State Institute for Scientific and Technological Research.
Results
In total, 412 plant samples were collected (78 plant species in 32 families, 4,554 fruits, 323.4 kg) (Table 1). Infestation was observed in 50 of the samples (12.1%), representing 23 plant species (18 families; Table 1). In total, 856 Lonchaeidae puparia were obtained, from which emerged specimens of 10 species in the genera Neosilba, Dasiops, and Lonchaea.
MAZAGÃO
In total, 129 samples were collected, consisting of 1,495 fruits of 42 species (20 families; Table 1). Infestation by lonchaeids was observed in 15 samples: 59 fruits of 7 plant species (7 families), from which 457 puparia were obtained (Tables 1 and 2). Metrodorea flavida K. Krause (Sapindales: Rutaceae) showed the highest percentage of infested fruits (70.0%), and A. muricata had the highest infestation load (39 puparia/fruit) (Table 2).
Seven species of Lonchaeidae were obtained: N. glaberrima, N. laura Strikis, N. pendula (Bezzi), N. pseudozadolicha Strikis, N. zadolicha, D. inedulis, and 1 Lonchaea species (Table 2) that was in poor condition and unidentifiable. Neosilba zadolicha was the most abundant species (66 specimens), occurring from Apr to Jul and infesting 5 host species (Table 2).
PORTO GRANDE
In total, 154 samples were collected, consisting of 1,524 fruits of 41 species (24 families). Infestation by lonchaeids was observed in 16 samples: 41 fruits of 8 plant species (7 families), from which 176 puparia were obtained (Tables 1 and 3). Artocarpus altilis (Parkinson) Forsberg (Rosales: Moraceae) showed the highest percentage of infested fruits (66.7%), and A. muricata had the highest infestation load (11 puparia/fruit) (Table 3).
Six species were reared: N. glaberrima, N. laura, N. pendula, N. pseudozadolicha, N. zadolicha, and 1 unidentified Lonchaea species (Table 3). Neosilba glaberrima infested the greatest number of hosts (6), followed by N. zadolicha and N. pseudozadolicha (3). Neosilba zadolicha was the most abundant species (31 specimens). In total, 44 specimens of Neosilba were obtained from E. stipitata, specifically 20 specimens of N. zadolicha, 3 of N. glaberrima, 1 of N. pseudozadolicha, and 20 females (Table 3). Except for Oct and Nov, specimens were obtained from at least 1 sampled host in all other months (Table 3).
SANTANA
In total, 129 samples were collected, consisting of 1,535 fruits of 40 plant species (23 families). Infestation was observed in 19 samples: 43 fruits of 12 plant species (12 families), from which 223 puparia were obtained (Tables 1 and 4). Inga edulis Mart. (Fabales: Fabaceae) showed the highest percentage of infested fruits (100%) (Table 4). The highest infestation load was observed on shoots of M. esculenta (11puparia/ shoot) (Table 4).
Eight species were reared: Neosilba bella Strikis, N. glaberrima, N. parapeltae Strikis, N. pendula, N. perezi Romero & Ruppel, N. pseudozadolicha, N. zadolicha, and D. inedulis. Neosilba zadolicha infested the greatest number of hosts (5), followed by N. glaberrima (4). Neosilba zadolicha was the most abundant species (59 specimens). The fruits of P. guajava yielded specimens from 3 species of Neosilba (N. glaberrima, N. pseudozadolicha, and N. zadolicha) in 6 mo of the year (Table 4).
Table 1.
Number of samples and fruits collected and infested by Lonchaeidae in 3 municipalities of the state of Amapá, Brazil, Jan to Dec 2012.
Continued
Table 2.
Lonchaeidae host plants, infestation rates of fruits, and months of occurrence in Mazagão, Amapá, Brazil, Jan to Dec 2012.
Table 3.
Lonchaeidae host plants, infestation rates of fruits, and months of occurrence in Porto Grande, Amapá, Brazil, Jan to Dec 2012.
Table 4.
Lonchaeidae host plants, infestation rates of fruits, and months of occurrence in Santana, Amapá, Brazil, Jan to Dec 2012.
Discussion
Our results contribute significantly to the knowledge of Lonchaeidae species that occur in the Amazon and their plant hosts, and we document 2 new records in the Amazon (N. laura and N. parapeltae) and 2 records in the state of Amapá (D. inedulis and N. perezi). We also report 24 new associations between lonchaeid species and hosts in the Amazon (Table 5), contributing towards a better understanding of Lonchaeidae-host relationships in this region of Brazil.
Neosilba species are polyphagous, and Uchôa (2012) reported that 5 species of Neosilba were of economic importance to the continent: N. zadolicha, N. pendula, N. glaberrima, N. perezi, and N. inesperata Strikis & Prado. In our study, the species that infested the greatest numbers of hosts were N. zadolicha (11 plant species in 9 families) and N. glaberrima (10 plant species in 9 families). These are the most polyphagous and most widely distributed lonchaeids in the Amazon region (Strikis et al. 2011), and are among the species with the highest economic importance for South America (Uchôa 2012).
Table 5.
Lonchaeidae species and their hosts in 3 municipalities of the state of Amapá, Brazil, Jan to Dec 2012.
Neosilba laura and N. parapeltae were described only recently (Strikis 2011), and there is no information about their biology. Neosilba laura was obtained from a fruit of M. flavida in Mazagão, a lonchaeid- host association reported for the first time here (Table 2). Neosilba parapeltae was obtained from a flower bud of E. tenuifolia in Santana, and this is possibly the first report of this host plant being used by the lonchaeid species (Table 2).
Neosilba perezi was obtained from sprouts of M. esculenta in Santana (Table 4). Neosilba perezi is a pest of cassava crops, with occurence varying by region and time of year (Lourenção et al. 1996). In the Amazon, N. perezi has been reported in the state of Rondônia (Oliveira 1987), under the name Silba pendula. Cassava is a significant social and economic species as a food staple and source of family income, but damage from this pest has not yet been quantified; this is the first report of N. perezi in the state of Amapá.
Dasiops inedulis was obtained from flower buds of P. edulis, a new distribution record for this species in the state of Amapá. Dasiops inedulis is an important pest of Passiflora flower buds in South America (Peñaranda et al. 1986; Uchôa-Fernandes et al. 2002). In the state of Pará, it is considered the most important pest of passionfruit plants, causing production losses of up to 100% (Lemos 2009).
Specimens of Lonchaea sp.1 were reared from fruits of A. muricata only. An additional unidentfied of Lonchaea species has already been reported in the states of Amazonas and Amapá. In Brazil, only localized reports of Lonchaea have been made, with no information about its biology and ecology, indicating a need for new surveys to discover additional potential hosts (Strikis et al. 2011).
Infestation rates varied widely (Tables 2–4). The greatest percentages of infested fruits were observed on fruits of native species, such as I. edulis, in Santana (Table 4). In previous studies conducted in the Amazon region, Silva et al. (2010) and Deus et al. (2013) reported infestation by lonchaeids of this plant species. The largest infestation (i.e., number of puparia/fruit) was observed on fruits of A. muricata in Mazagão (Table 2). This plant species represents a significant source of income for inhabitants of the Amazon region, who use it to make soursop concentrate.
We did not rear any parasitoids in this work, although 8 species of parasitoid Eucoilinae (Figitidae) are associted with larvae of Neosilba in Brazil (Uchôa 2012). Figitid parasitoids search for host larvae located inside fruits that have already fallen to the ground and that have an orifice for entry, as the females of these parasitoids have short ovipositors (Uchôa 2012). Because fruits were collected directly from host palnts, figitid parasitoids may not have had an opportunity to parasitize larvae. An interesting finding in this study was the wide diversity of Lonchaeidae host plants sampled in native forest areas. Of the 10 species we reared, 6 were associated with hosts located in native forest areas. In addition, the 2 new reports for the Brazilian Amazon were associated with native hosts (Table 5).
Because some lonchaeid species are pest species, researchers have become increasingly interested in studying these flies. However, little is known about the ecology and biology of lonchaeid flies in Brazil. This work identifies the state of Amapá as a region with the greatest recorded lonchaeid species richness in the Amazon, and suggests that additioanl survey and rearing work be conducted.
Acknowledgments
We dedicate this paper to Cheslavo A. Korytkowski, science doctor at the University of Panama, who sadly passed away on 12 May 2015, for his great scientific contribution to knowledge on Lonchaeidae species. We thank the students Danilo Baia do Nascimento, Maria do Socorro Miranda de Sousa, Luana dos Santos Pinheiro, Francisco Andrew Pacheco, Oziel Barroso Baía, Sarron Feliphe, and Jonh Carlo Reis. We also thank our colleagues at Embrapa Amapá: Felipe Galdino Machado, Carlos Alberto Moraes, Manoel Jonas de Jesus Viana, and Marcelo Luiz de Oliveira. We gratefully acknowledge the Brazilian Council for Scientific and Technological Development—CNPq, for the Research Productivity Fellowship granted to R. Adaime.
