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Distribution and Abundance of Necrophagous Flies (Diptera: Calliphoridae and Sarcophagidae) in Maranhao, Northeastern Brazil

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Distribution and Abundance of Necrophagous Flies (Diptera: Calliphoridae and Sarcophagidae) in Maranhao, Northeastern Brazil Journal of Insect Science RESEARCH Distribution and Abundance of Necrophagous Flies (Diptera: Calliphoridae and Sarcophagidae) in Maranha˜o, Northeastern Brazil Jose´ Roberto Pereira de Sousa,1,2 Fernando da Silva Carvalho-Filho,3 and Maria Cristina Esposito4 1Department of Chemistry and Biology, Centro de Estudos Superiores de Imperatriz, Universidade Estadual do Maranha˜o, Imperatriz-MA, Brazil 2Corresponding author, e-mail: [email protected] 3Department of Zoology, Coordenac¸a˜o de Zoologia - Entomologia, Museu Paraense Emı´lio Goeldi, Bele´m-PA, Brazil 4Biological Sciences Institute, Universidade Federal do Para´, Bele´m-PA, Brazil Subject Editor: Marc De Meyer J. Insect Sci. (2015) 15(1): 70; DOI: 10.1093/jisesa/iev054 ABSTRACT. This study aimed at surveying the local calliphorid and sarcophagid species in Maranha˜o State (Brazil) to determine their distribution and abundance, as well as the distribution of exotic Chrysomya species. In total, 18,128 calliphorid specimens were collected, distributed in 7 genera and 14 species. The species Hemilucilia semidiaphana (Rondani, 1850) and Paralucilia paraensis (Mello, 1969) were new state records. Chrysomya albiceps (Wiedemann, 1819) and Cochliomyia macellaria (F., 1775) were the most abundant species, and the exotic species of Chrysomya together contributed more than 50% of total blow fly abundance. The abun- dance distribution of the calliphorid community conformed to a log series model, characterized by a steep curve that reflects an assem- blage with a high degree of dominance. For the Sarcophagidae, a total of 14,810 specimens were collected and distributed in 15 genera, 11 subgenera, and 52 species. Tricharaea (Sarcophagula) occidua (F., 1794) and Peckia (Sarcodexia) lambens (Wiedemann, 1830) were the most abundant species. The abundance distribution of the species followed a log normal model, with a gentler slope, consistent with a more uniform community. The cumulative species curve for the sarcophagids did not reach the asymptote. Forty-three sarcoph- agid species were new state records and 22 were new records for the Brazilian northeast, which emphasizes the need for a continued survey in this region. Key Words: blow fly, flesh fly, insect sampling, neotropical region. Flies of the families Calliphoridae and Sarcophagidae are ecologically (Miltogrammatinae, Paramacronychiinae, and Sarcophaginae). and forensically important, due to the fact that the larvae of many spe- Approximately 800 species are known to occur in the Neotropics, and cies feed on dead organic matter, acting as decomposers and potential 350 have been recorded in Brazil (Pape 1996, Amorim et al. 2002). The indicators of the postmortem interval (Rivers and Dahlem 2014). From subfamily Sarcophaginae is the richest in species and the most diverse, in a medical and sanitary viewpoint, the adults are potential vectors of biological terms, with approximately 1,800 known species and 51 gen- pathogens (Greenberg 1971), while the larvae of some species parasit- era, which have been recorded in all biogeographic regions and are com- ize humans and other vertebrates, causing myiasis, known as blowfly mon in the New World (Shewell 1987, Pape 1996, Pape et al. 2006). strike (Zumpt 1965, Hall and Wall 1995, Guimara˜es and Papavero Most species are most effectively identified based on the characteristics 1999). of the male genitalia (Carvalho and Mello-Patiu 2008). There are 1,525 known calliphorid species belonging to 97 genera Most of the available studies of the geographic distribution and (Pape et al. 2011), of which 130 species are known to occur in the occurrence of calliphorid and sarcophagid species in Brazil have Neotropical Region (Carvalho and Mello-Patiu 2008) and 38 in Brazil focused on the southern and southeastern regions (Viana and Pinheiro (Mello 2003, Kosmann et al. 2013). During the 1970s, the composition 1998; Leandro and D’Almeida 2005; Furusawa and Cassino 2006; of the calliphorid fauna of the Americas was affected by the invasion of Ferraz et al. 2009, 2010b; Souza and Von Zuben 2012; Cabrini et al. three exotic species of the genus Chrysomya, originally from the 2013; Ribeiro et al. 2013), as well as the northern region (Carvalho and Old World (Ferreira 1978, Guimara˜es et al. 1978, Linhares 1981, Couri 1991; Paraluppi and Castello´n 1994; Paraluppi 1996; Couri et al. Paraluppi and Castello´n1994). Since this time, these species, Chrysomya 2000; Esposito et al. 2009, 2010; Sousa et al. 2010, 2011), while few albiceps (Wiedemann), C. megacephala (F., 1794), and C. putoria studies are available for the other Brazilian regions, as the midwest (Wiedemann, 1818), have become very abundant in Brazil and have (Gomes et al. 2000, Barros et al. 2008, Correˆa et al. 2010, Koller et al. come to predominate in both urban environments and forest fragments, 2011) and the northeast (Vasconcelos and Araujo 2012, Silva et al. where they have even displaced native species, such as Cochliomyia 2012b, Vasconcelos et al. 2013, Vasconcelos and Salgado 2014) and macellaria (F., 1775) and Lucilia eximia (Wiedemann, 1819) (Ferreira many areas have yet to be surveyed. 1979, 1983; Guimara˜es et al. 1979; Paraluppi and Castello´n 1994; The Brazilian state of Maranha˜o not only covers a vast area but is Esposito 1997). A fourth species of Chrysomya, C. rufifacies (Macquart, also characterized by a remarkable diversity of habitats due to its loca- 1843), has been discovered in Brazil, in the states of Maranha˜o (Silva tion in the transition zone between the Amazon, Cerrado, and Caatinga et al. 2012a) and Rio de Janeiro (Ribeiro et al. 2013). However, Grella biomes (Ab’Saber 1977, Muniz 2006), a scenario that has stimulated et al. (2015) concluded that the specimens identified as C. rufifacies rep- considerable interest from zoologists. Given the lack of data on the resent a polymorphic form of the species C. albiceps and that C. rufifa- fauna of calliphorids and sarcophagids found in Maranha˜o, this study cies does not yet occur in Brazil. aimed to survey the local species and determine their distribution and The sarcophagids are a more diverse group, with a total of 3,094 spe- abundance, as well as the distribution and abundance of the exotic cies, distributed in 173 genera (Pape et al. 2011) and three subfamilies Chrysomya species found in the state. VC The Author 2015. Published by Oxford University Press on behalf of the Entomological Society of America. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact [email protected] 2 JOURNAL OF INSECT SCIENCE VOLUME 15 Materials and Methods The estimates of species richness were calculated in EstimateS, version 9.0 (Colwell 2013). Study Area. The survey was conducted at 105 sites located in The calliphorid and sarcophagid species were classified in three cat- 19 municipalities distributed throughout the state of Maranha˜o (Table egories (common, intermediate, and rare), based on their occurrence at 1; Fig. 1), in northeastern Brazil, between the coordinates 01 01’ to the study sites surveyed in Maranha˜o. The analysis of the records was 10 21’ S and 41 48’ to 48 40’ W. The specimens were collected in based on indices of frequency and constancy (Silveira-Neto et al. traps designed specifically for the capture of saprophagous dipterans, 1976). containing 50 g of cow’s lung as bait (Ferreira 1978). The traps were set The Frequency Index (FI) is the proportion of individuals of a given at three to nine sites in each municipality in July–October 2009, species in relation to the total sample, FI ¼ ni/N, where ni ¼ the number August–October 2010, January, April, and October 2011, and of specimens of species i and N ¼ the total number of specimens col- February, May, and November 2012. Between 15 and 30 traps were set lected. Based on the FI values, the species were classified as dominant at each site, which was considered to be a sampling unit, and were repli- (D) or nondominant (ND). Dominant species were those with a FI value cated at a minimum distance of 2 km from one another. higher than 1/S, where S is species richness, i.e., the total number of The calliphorid specimens were identified using the taxonomic species in the community. keys of Guimara˜es (1977), Dear (1985), Carvalho and Ribeiro The Constancy Index (CI) is the percentage of samples in which a (2000), Mello (2003), Carvalho and Mello-Patiu (2008), and given species was present, CI ¼ p*100/N, where p ¼ the number of Kosmann et al. (2013). The sarcophagid specimens were identified samples in which the species was recorded and N ¼ the total number of using the specific keys for the genera Oxysarcodexia (Lopes 1946, samples. This analysis considered the 105 study sites as individual sam- Lopes and Tibana 1987) and Peckia (Buenaventura and Pape 2013), ples. Based on their CI values, the species were classified as constant as well as other studies, which despite not presenting identification (CT), when present in more than 50% of the samples (CI > 0.50), acces- keys as such, do provide illustrations of the genitalia of some genera, sory (AS) when present in 25–50% of the samples (CI ¼ 0.25–0.50), that permit an accurate identification of the taxa (Lopes 1939, 1958, and accidental (AC) when found in fewer than 25% of samples 1976, 1989; Tibana 1976, 1981; Lopes and Tibana 1982; Tibana and (CI < 0.25). The species were classified based on the combination of Xerez 1985; Guimara˜es 2004). This process was further refined by these two indices, as common (DþCT), intermediate (DþAS; DþAC; comparisons with voucher specimens deposited in the entomological NDþCT; NDþAS), and rare (NDþAC).
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