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 Maranhaõ, 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 Maranhaõ, Imperatriz-MA, Brazil 2Corresponding author, e-mail: [email protected] 3Department of Zoology, Coordenaçaõ 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 Maranhaõ 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 abundance distribution of the calliphorid community conformed to a log series model, characterized by a steep curve that reflects an assemblage 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 sarcophagid 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 Castelloń 1994; Paraluppi 1996; Couri et al. Paraluppi and Castelloń1994). 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, Correâ 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 Castelloń 1994; The Brazilian state of Maranhaõ 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 Maranhaõ (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 Maranhaõ, 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 Maranhaõ (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 Maranhaõ. 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). collection of the Museu Paraense Emı´lio Goeldi (MPEG) in Bele´m, The species were classified in decreasing order of abundance and Para´ (Brazil). these data were compared with four mathematical models of abundance The specimens collected in this study were deposited in the MPEG distribution, i.e., geometric, log series, log-normal, and broken stick, to entomological collection, in the Museu de Zoologia da Universidade determine the best fit of the data collected. The fit was determined using Federal do Para´, also in Bele´m, and in the teaching collection of the Chi-square, considering P < 0.05 (Magurran 1988). These analyses Prof. Cle´sio Fonseca Laboratory of Zoology at the Universidade were run in the program Species Diversity and Richness 3.0 Estadual do Maranhaõ in Imperatriz, Maranhaõ (Brazil). (Henderson and Seaby 2002) and the graphs were produced in Past Data Analysis. The efficiency of the sampling of the calliphorid and (Hammer et al. 2001). sarcophagid species in the study area was verified using cumulative species curves derived from a first-order nonparametric Jackknife pro- Results cedure (Colwell and Coddington 1994), with one thousand randomiza- In total, 18,128 calliphorid specimens were collected during this tions based on the number of study sites (Colwell 2013). The Jackknife study, representing 3 subfamilies (Chrysomyinae, Luciliinae, and 1 estimator is based on the richness of the rarest species, using the Mesembrinellinae), 7 genera, and 14 species, 10 of which were chryso- formula Jackknife ¼ Sobs þ L(n 1/n), where Sobs ¼ the number of myines. The species Hemilucilia semidiaphana (Rondani, 1850) and species observed overall, L ¼ the number of species found in a single Paralucilia paraensis (Mello, 1969) were recorded for the first time in sample, and n ¼ the number of samples (Palmer 1991, Colwell 2013). the state of Maranhaõ (Table 2). C. albiceps and Co. macellaria were

Table 1. Municipalities surveyed in the different mesoregions (Fig. 1) of the Brazilian state of Maranha˜o between 2009 and 2012 Municı´pio Geographic coordinates Mesoregion Study sites Number of traps

South West Carolina 07 12’ 58.8’’ 47 25’ 54.6’’ South Maranhaõ 6 30 Riachaõ 07 25’ 40.1’’ 46 45’ 3.06’’ South Maranhaõ 6 30 Balsas 07 27’ 4.44" 46 24’ 57.02" South Maranhaõ 6 30 Estreito 06 33’ 39" 47 27’ 0.3" South Maranhaõ 9 18 Esperantino´polis 04 55’ 09.02’’ 44 57’ 09.43’’ Central Maranhaõ 6 30 Poçaõ de Pedras 04 49’ 10.95’’ 44 55’ 35.55’’ Central Maranhaõ 6 30 Lago do Junco 04 36’ 14.3’’ 45 01’ 03.44’’ Central Maranhaõ 6 30 Cajari 03 19’ 18.03’’ 44 52’ 13.06’’ North Maranhaõ 6 30 Cajapio´02 50’ 19.98’’ 44 40’ 42.72’’ North Maranhaõ 6 30 Viana 03 12’ 39.7’’ 44 56’ 59.3’’ North Maranhaõ 6 30 Cedral 01 57’ 44.3’’ 44 30’ 41.6’’ North Maranhaõ 6 30 Guimaraes 02 05’ 20.3’’ 44 33’ 11.7’’ North Maranhaõ 6 30 Caˆndido Mendes 01 25’ 54.39’’ 45 30’ 45.12’’ West Maranhaõ 3 15 Turiaçu´01 31’ 07.4’’ 45 25’ 47.2’’ West Maranhaõ 3 15 Centro Novo do Maranhaõ 03 37’ 09.1’’ 46 43’ 22.6’’ West Maranhaõ 9 45 Bom Jardim 04 00’ 53.04’’ 46 46’ 48.99’’ West Maranhaõ 3 15 Cidelaˆndia 05 07’ 39.9’’ 47 45’ 37.0’’ West Maranhaõ 3 15 Vila Nova dos Martı´rios 05 11’ 09.4’’ 47 56’ 41.1’’ West Maranhaõ 3 15 Imperatriz 05 31’ 33’’ 47 28’ 38’’ West Maranhaõ 6 36 Total 105 504 2015 SOUSA ET AL.: DISTRIBUTION AND ABUNDANCE OF NECROPHAGOUS FLIES 3 the most abundant species, and the exotic species of the genus v2 ¼ 995.511; P < 0.05; df ¼ 14), broken stick (Fig. 2c: v2 ¼ 246.508; Chrysomya together contributed more than 50% of total abundance. P < 0.05; df ¼ 14) or log normal (Fig. 2d: v2 ¼ 6.191; P < 0.05; The abundance distribution of the calliphorid community produced df ¼ 12) models. a best fit with the log series distribution (Fig. 2a: v2 ¼ 12.185; The cumulative species curve based on the total sample of the calli- P ¼ 0.430; df ¼ 12). In contrast, the abundance values recorded for the phorids had reached the asymptote by the end of the study (Fig. 3), with species of this family did not adjust to the geometric (Fig. 2b: sampling efficiency (observed species richness divided by estimated

Fig. 1. Location of the municipalities surveyed in the different mesoregions of the Brazilian state of Maranha˜o between 2009 and 2012.

Table 2. Composition and total abundance of the calliphorid species found in the study area in Maranha˜o, Brazil, between 2009 and 2012 Species Frequency index CI Category New occurrencea

AA FI % 1/S %C O CI%C C. albiceps 7,326 40.41 7.14 D 101 96.19 CT Common Co. macellaria 4,787 26.41 7.14 D 99 94.29 CT Common C. megacephala 2,199 12.13 7.14 D 72 68.57 CT Common Ch. idioidea 1,910 10.54 7.14 D 65 61.90 CT Common L. eximia 1,065 5.87 7.14 ND 61 58.10 CT Intermediate C. putoria 363 2.00 7.14 ND 51 48.57 AS Intermediate M. bicolor 242 1.33 7.14 ND 14 13.33 AC Rare H. semidiaphana 190 1.05 7.14 ND 17 16.19 AC Rare X P. paraensis 17 0.09 7.14 ND 8 7.62 AC Rare X Co. hominivorax 11 0.06 7.14 ND 8 7.62 AC Rare L. sericata 10 0.06 7.14 ND 3 2.86 AC Rare H. segmentaria 6 0.03 7.14 ND 4 3.81 AC Rare H. benoisti 1 0.01 7.14 ND 1 0.95 AC Rare M. batesi 1 0.01 7.14 ND 1 0.95 AC Rare Total 18,128 100 2 AA, absolute abundance; FI, Frequency Index; S, observed species richness; C, class; O, occurrence; D, dominant; ND, not dominant; CT, constant; AS, accessory; AC, accidental. aNew occurrence of species in Maranha˜o. 4 JOURNAL OF INSECT SCIENCE VOLUME 15

Fig. 2. Models of the abundance distribution of calliphorid species in Maranha˜o: (a) log series, (b) geometric, (c) broken stick, and (d) log normal.

Mao Tau 25 Jackknife 1

5 Observed (Mao tau) and estimated (Jackknife 1) richness 0 114274053667992105 Samples (Areas) Fig. 3. Cumulative species richness curves (observed, Mao Tau, and estimated, Jackknife 1) for the calliphorids sampled in Maranhaõ, Brazil, 2009–2012. 2015 SOUSA ET AL.: DISTRIBUTION AND ABUNDANCE OF NECROPHAGOUS FLIES 5 richness) of 94%, which indicates that sampling effort was sufficient recorded the highest species richness (26 species), equivalent to 68% of for the reliable measurement of the species richness of the the total found in Brazil. Calliphoridae in the study area. Low species richness of the calliphorid fauna was registered in other Based on the classification of the frequency and constancy of the regions of South America, such as Argentina, where Centeno et al. different species, four calliphorids (28.5% of the total fauna) were con- (2004) recorded 12 species in Hudson, and Mariluis et al. (2008) and sidered to be common in Maranhaõ, two species (14.3%) were classi- Patitucci et al. (2011) recorded four and six species, respectively, in fied as intermediate, and eight (57.2%) as rare (Table 1). The species Patagonia. Beltran et al. (2012) recorded six species in Bogota´, C. albiceps, Co. macellaria, C. megacephala, and Chloroprocta idioi- Colombia. dea (Robineau-Desvoidy, 1830) were all considered to be common, Of the 14 calliphorid species collected in this study, 10 were chryso- given that they were both dominant and constant, being found at more myines, 59% of the 17 species of this subfamily known to occur in than half of the sites surveyed. Brazil (Kosmann et al. 2013). Similarly, of the four species of The species L. eximia and C. putoria were classified as intermediate, Hemilucilia found in Brazil (Dear 1985, Kosmann et al. 2013), three due to the fact that they were not considered to be dominant. The rare (H. semidiaphana, H. segmentaria, and H. benoisti) were recorded in group (nondominant and accidental) included three species of Maranhaõ. In contrast, only one of the four species of the genus the genus Hemilucilia: H. semidiaphana, H. segmentaria (F., 1805), Paralucilia known to occur in Brazil (P. paraensis) was collected in and H. benoisti Se´guy, 1925 and two of the genus Mesembrinella this study. Giglio-Tos 1893: Mesembrinella bicolor (F., 1805) and Mesembrinella In the Neotropical region, the only calliphorid species that is an obli- batesi (Aldrich, 1922). gate parasite of live tissue (i.e., a source of primary myiasis) is Co. hom- In the case of the Sarcophagidae, a total of 14,810 specimens were inivorax (Coquerel, 1858) (Guimara˜es et al. 1983, Dear 1985). Despite collected, all of which were sarcophagines, distributed in 15 genera, this habit, Co. hominivorax also been captured using this type of bait in 11 subgenera, and 52 species. Forty-three of these species had not pre- a number of previous studies (Viana and Pinheiro 1998, Esposito et al. viously been recorded in Maranhaõ and 22 were not known to occur in 2009, Ferraz et al. 2010, Sousa et al. 2010). the Brazilian northeast. Tricharaea (Sarcophagula) occidua (F., 1794) The subfamily Luciliinae was represented by only two species, of and Peckia (Sarcodexia) lambens (Wiedemann, 1830) were the most which, L. eximia is a common species in Brazil, being found in rural abundant species (Table 3). areas and forests (Ferreira 1978, Linhares 1981, Madeira et al. 1982, The best fit for the abundance distribution of the sarcophagids was Sousa et al. 2010). Six species of the genus Lucilia are known to occur the log normal model (Fig. 4a: v2 ¼ 2.289; P ¼ 0.999; df ¼ 13), in Brazil (Carvalho and Ribeiro 2000, Kosmann et al. 2013, Whitworth whereas the data were not consistent with the geometric (Fig. 4b: 2014). v2 ¼ 24,864.8; P < 0.05; df ¼ 50), log series (Fig. 4c: v2 ¼ 40.261; The subfamily Mesembrinellinae was represented by the species P < 0.05; df ¼ 13), or broken stick (Fig. 4d: v2 ¼ 2.153; P < 0.05; M. bicolor and M. batesi. The mesembrinelline flies are found exclu- df ¼ 13) models. sively in the Neotropics, where they are represented by 30 species, The cumulative species curve for the sarcophagids did not reach the 14 of which occur in Brazil (Guimara˜es 1977, Kosmann et al. 2013). asymptote and was still rising at the end of the study period (Fig. 5). These flies are found in natural habitats, such as dense, humid forests However, sampling efficiency (observed species richness divided by (Peris and Mariluis 1984). estimated richness) was 78%, indicating that the sampling effort was The calliphorid fauna recorded in Maranhaõ was similar to that sufficient for the measurement of the species richness of necrophagous found in other Brazilian states, especially given that two of the four sarcophagids in the study area. common species were exotic members of the genus Chrysomya Three sarcophagid species (6% of the total) were considered to be (C. albiceps and C. megacephala), with a third member of this genus common, 5 (9%) intermediate, and the remaining 44 (85%) rare. The (C. putoria) being found among the intermediate species. However, common species, T.(S.) occidua, Pe. (S.) lambens, and Pe. (Peckia) C. albiceps predominated considerably over C. megacephala and chrysostoma (Wiedemann), 1830, were both dominant and constant, C. putoria at most study sites. being not only abundant but also recorded at a high proportion of the The abundance distribution of the calliphorid community con- study sites (Table 2). Even though Oxysarcodexia intona (Curran and formed to a log series model, characterized by a steep curve that reflects Walley, 1934) and O. thornax (Walker, 1849) were dominant species, an assemblage with a high degree of dominance. The log series model they were classified as intermediate due to their accessory status, being (Fisher et al. 1943) implies that the communities are not independent recorded at between 25% and 50% of the study sites. Pe. and require high rates of immigration to maintain their high number of (Squamatodes) ingens (Walker, 1849) and Pe. (Peckia) pexata (Wulp, rare species (Preston 1948). In these communities characterized by a 1895), both considered to be accessory, and Pe. (Euboettcheria) collu- high degree of dominance and low levels of abundance in the majority sor (Curran and Walley 1934), which was constant, were all classified of species, the model predicts a smaller number of species than that as intermediate species because they were not dominant. observed (Magurran 1988). The predominance of C. albiceps in comparison with other Discussion Chrysomya species has been attributed to the feeding behavior of its lar- The known calliphorid fauna of Maranhaõ represents 35% of the vae, which are predators of the immature stages of other dipterans total number of species predicted to occur in Brazil by Mello (2003) (Mello et al. 1997), as well as their short development period, with the and Kosmann et al. (2013). The estimates of the species richness of the larvae incorporating the maximum possible quantity of food during the calliphorids (Jackknife 1 and Mao Tau) indicate that the sampling effort shortest possible period of time (Prado and Guimara˜es 1982). was sufficient for the inventory of the full diversity of necrophagous The species Co. macellaria (common) and L. eximia (intermediate) species present within the study area. The number of species recorded are important components of the necrophilous fly fauna of South was similar to that found in other Brazilian states, such as Para´ America, although the presence of Chrysomya species has been shown (Esposito et al. 2009, 17 species), Amazonas (Sousa et al. 2010, 16 spe- to interfere with their abundance. A number of studies have indicated cies), Rio Grande do Sul (Viana and Pinheiro 1998, 13 species), Saõ that the exotic species C. albiceps may be responsible for the displace- Paulo (Cabrini et al. 2013, 13 species), Roraima (Carvalho and Couri ment or reduction in the abundance of the native species through com- 1991, nine species), Mato Grosso (Esposito and Carvalho-Filho 2009, petition (Guimara˜es et al. 1979, Prado and Guimara˜es 1982, seven species), and Pernambuco (Vasconcelos and Salgado 2014, six D’Almeida and Fraga 2007). The species Ch. idioidea, which is also species). In the state of Rio de Janeiro, however, Ferraz et al. (2010) considered to be common, is also an important component of the 6 JOURNAL OF INSECT SCIENCE VOLUME 15

Table 3. Composition and total abundance of the sarcophagid species found in the study area in Maranha˜o, Brazil, between 2009 and 2012 Species Frequency index CI Category New occurrence (NO)

AA FI % 1/S % C O CI% C NOa NOb Tricharaea (Sarcophagula) occidua 8,452 57.07 1.92 D 70 66.67 CT Common Pe. (Sarcodexia) lambens 2,562 17.30 1.92 D 84 80.00 CT Common Pe. (Peckia) chrysostoma 1,249 8.43 1.92 D 92 87.62 CT Common X O. intona 905 6.11 1.92 D 45 42.86 AS Intermediate Oxysarcoxia thornax 358 2.42 1.92 D 41 39.05 AS Intermediate X Pe. (Euboettcheria) collusor 266 1.80 1.92 ND 53 50.48 CT Intermediate X Pe. (Squamatodes) ingens 146 0.99 1.92 ND 35 33.33 AS Intermediate X Pe. (Pattonella) intermutans 129 0.87 1.92 ND 20 19.05 AC Rare X Sarcofahrtiopsis cuneata 109 0.74 1.92 ND 8 7.62 AC Rare X O. fringidea 105 0.71 1.92 ND 16 15.24 AC Rare Pe. (Peckia) pexata 86 0.58 1.92 ND 28 26.67 AS Intermediate X O. amorosa 67 0.45 1.92 ND 17 16.19 AC Rare X O. modesta 53 0.36 1.92 ND 17 16.19 AC Rare X X O. timida 53 0.36 1.92 ND 18 17.14 AC Rare Ravinia effrenata 49 0.33 1.92 ND 11 10.48 AC Rare X Pe. (Euboettcheria) anguilla 28 0.19 1.92 ND 16 15.24 AC Rare X Helicobia morionella 27 0.18 1.92 ND 12 11.43 AC Rare X Helicobia pilifera 25 0.17 1.92 ND 13 12.38 AC Rare X O. avuncula 14 0.09 1.92 ND 5 4.76 AC Rare X Pe. (Squamatodes) trivittata 13 0.09 1.92 ND 5 4.76 AC Rare X Tricharaea (Sarcophagula) canuta 13 0.09 1.92 ND 2 1.90 AC Rare X Retrocitomyia mizuguchiana 12 0.08 1.92 ND 10 9.52 AC Rare X X Ravinia belforti 9 0.06 1.92 ND 7 6.67 AC Rare X Retrocitomyia urumajoensis 9 0.06 1.92 ND 6 5.71 AC Rare X X Pe. (Peckia) uncinata 8 0.05 1.92 ND 5 4.76 AC Rare X X Argoravinia rufiventris 6 0.04 1.92 ND 3 2.86 AC Rare O. bakeri 6 0.04 1.92 ND 4 3.81 AC Rare X Helicobia rapax 5 0.03 1.92 ND 3 2.86 AC Rare X X Villegasia almeidai 5 0.03 1.92 ND 5 4.76 AC Rare X X O. admixta 4 0.03 1.92 ND 2 1.90 AC Rare X X Titanogrypa (Cucullomyia) larvicida 4 0.03 1.92 ND 2 1.90 AC Rare X Helicobia aurescens 3 0.02 1.92 ND 3 2.86 AC Rare X X Malacophagomyia filamenta 3 0.02 1.92 ND 1 0.95 AC Rare X X O. vilosa 3 0.02 1.92 ND 2 1.90 AC Rare X X Blaesoxipha (Gigantotheca) stallengi 2 0.01 1.92 ND 1 0.95 AC Rare X Dexosarcophaga (Bezzisca) tupinamba 2 0.01 1.92 ND 2 1.90 AC Rare Dexosarcophaga (Farrimyia) carvalhoi 2 0.01 1.92 ND 1 0.95 AC Rare Helicobia pilipleura 2 0.01 1.92 ND 1 0.95 AC Rare X Helicobia setinervis 2 0.01 1.92 ND 2 1.90 AC Rare X X Sarcophaga (Lipoptilocnema) misella 2 0.01 1.92 ND 2 1.90 AC Rare X X Dexosarcophaga hugoi 1 0.01 1.92 ND 1 0.95 AC Rare X X Helicobia borgmeieri 1 0.01 1.92 ND 1 0.95 AC Rare X X O. aurea 1 0.01 1.92 ND 1 0.95 AC Rare X X Oxysarcodexia sp1 1 0.01 1.92 ND 1 0.95 AC Rare Pe. (Euboettcheria) subducta 1 0.01 1.92 ND 1 0.95 AC Rare X X Pe. (Pattonella) pallidipilosa 1 0.01 1.92 ND 1 0.95 AC Rare X X Peckiamyia abnormalis 1 0.01 1.92 ND 1 0.95 AC Rare X X Retrocitomyia retrocita 1 0.01 1.92 ND 1 0.95 AC Rare X X Sarcophaga (Lipoptilocnema) crispula 1 0.01 1.92 ND 1 0.95 AC Rare X Sarcophaga (Neobellieria) polistensis 1 0.01 1.92 ND 1 0.95 AC Rare X X Titanogrypa (Airypel) cryptopyga 1 0.01 1.92 ND 1 0.95 AC Rare X X Titanogrypa (Cucullomyia) luculenta 1 0.01 1.92 ND 1 0.95 AC Rare X X Total 14,810 100 43 22 AA, absolute abundance; FI, frequency index; S, observed species richness; C, class; O, occurrence; D, dominant; ND, not dominant; CT, constant; AS, accessory; AC, accidental. aNew occurrence of species in Maranhaõ. bNew occurrence of species in Northeast Brazil. calliphorid fauna and has been collected at a number of different sites in The number of sarcophagid species recorded in Maranhaõ repre- Brazil (Esposito et al. 2009, 2010; Ferraz et al. 2009; Sousa et al. 2010). sents only around 15% of the total number of species predicted for The rare calliphorid species include two members of the genus Brazil. The estimates of species richness (Jackknife 1 and Mao Tau) Hemilucilia Brauer, 1985, which are typical of forest habitats indicate that the sampling effort was not sufficient for a reliable esti- (D’Almeida and Lopes 1983). The species H. semidiaphana is consid- mate of sarcophagid species richness, based on the criteria of Toti et al. ered to be hemisynanthropic (Viana and Pinheiro 1998). The species (2000). However, the sampling efficiency of 78% indicates that a large M. bicolor and M. batesi and all the other mesembrinellines are consid- proportion of the local species were recorded, at least the necrophagous ered to be asynanthropic, in contrast, due to the fact that they are found species. Even so, given the large number of species known to occur in exclusively in forest and apparently do not breed in any of the decom- the Neotropical region, including Brazil (Pape 1996, Pape et al. 2011), posing substrates so common in anthropogenic environments and the fact that the members of this family occupy an ample diversity (Guimara˜es 1977, Ferreira 1978). They were recorded in the Amazon of habitats and are members of several different guilds (not all species forest zone in this study. are regular visitors of decomposing meat), it seems likely that 2015 SOUSA ET AL.: DISTRIBUTION AND ABUNDANCE OF NECROPHAGOUS FLIES 7

Fig. 4. Models of the abundance distribution of saprophagid species in Maranha˜o: (a) log series, (b) geometric, (c) broken stick, and (d) log normal.

Mao Tau 70 Jackknife 1

10 Observed (Mao tau) and estimated (Jackknife 1) richness 0 1 14274053667992105 Samples (Areas) Fig. 5. Cumulative species richness curves (observed, Mao Tau, and estimated, Jackknife 1) for the sarcophagids sampled in Maranhaõ, Brazil, 2009–2012. 8 JOURNAL OF INSECT SCIENCE VOLUME 15 additional sampling within the study area will result in an increase in fragment: implication for the use of dipteran species as bioindicators. the number of sarcophagid species known to occur in Maranhaõ. The Biodivers. Conserv. 22: 2635–2643. confirmation of new records of 43 species for Maranhaõ and 22 for the Carvalho, C.J.B., and M. S. Couri. 1991. Muscidae, Fanniidae and Calliphoridae (Dı´ptera) do Projeto Maraca´, Roraima, Brasil. Acta Amaz. 21: Brazilian Northeast reinforces the need for further surveys in this 35–43. region. The sarcophagid fauna of the New World is more diverse than Carvalho, C.J.B., and C. A. Mello-Patiu. 2008. Keys to the adults of the most that of the Old World, in terms of the number of species and genera, and common forensic species of Diptera in South America. Rev. Bras. Entomol. the Neotropical region is the most diverse of all (Shewell 1987, Pape 52: 390–406. 1996, Pape et al. 2011). Approximately 800 species have been recorded Carvalho, C.J.B., and P. B. Ribeiro. 2000. Chave de identificaçaõ das in the Neotropics, of which, 350 are known to occur in Brazil (Pape espećies de Calliphoridae (Diptera) do sul do Brasil. Rev. Bras. Parasitol. 9: 255–268. 1996, Amorim et al. 2002). Even so, it seems likely that these numbers Centeno, N., D. Almorza, and C. Arnillas. 2004. Diversity of Calliphoridae will continue to grow as new surveys are conducted. (Insecta: Diptera) in Hudson, Argentina. Neotrop. Entomol. 33: 387–390. Considering that the common sarcophagid species, T. (S.) occidua Colwell, R. K. 2013. Estimates: statistical estimation of species richness and and Pe.(S.) lambens, predominate over all other species, including the shared species from samples. Version 9.0. University of Connecticut. other common species, Pe.(Peckia) chrysostoma, reinforces their Connecticut, USA. (http://purl.oclc.org/estimates). importance as components of the necrophagous sarcophagid fauna of Colwell, R. K., and J. A. Coddington. 1994. Estimating terrestrial biodiversity through extrapolation. Philos. Trans. R. Soc. Lond. B Biol. Sci. 345: Maranhaõ. However, the abundance distribution of the species 101–118. followed a log normal model, with a gentler slope, consistent with a Correa, E. C., W. W. Koller, and A.T.M. Barros. 2010. Abundancia relativa more uniform community. e sazonalidade de espećies de Chrysomya (Diptera: Calliphoridae) no The species Pe.(S.) lambens was also the most abundant sarcoph- Pantanal Sul Mato - Grossense, Brasil. Rev. Bras. Parasitol. Vet. 19: 85–88, agid on Maraca´ Island in the Brazilian state of Roraima (Lopes and 2010. Tibana 1991) and in the Serra do Navio in Amapa´(Couri et al. 2000), Couri, M. S., C.J.E. Lamas, C.C.C.A. Aires, C. A. Mello-Patiu, V. C. Maia, D. M. Pamplona, and P. Magno. 2000. Dı´pteros da Serra do Navio whereas T.(S.) occidua was the most abundant species at the sites sur- (Amapa´, Brasil): Asilidae, Bolbilidae, Calliphoridae, Micropezidae, veyed in Argentina (Mulieri et al. 2008). These two species are able to Muscidae, Sarcophagidae, Stratiomyiidae, Syrphidae, Tabanidae and adapt to a diversity of environments and have been recorded in both Tachinidae. Rev. Bras. Zoocieˆnc. 2: 91–100. open habitats and forests (Mulieri et al. 2008, Sousa et al. 2011). D’Almeida, J. M. 1984. Sinantropia de Sarcophagidae (Diptera) na Regiaõ The sarcophagid species classified as intermediate included Pe.(E.) Metropolitana do Estado do Rio de Janeiro. Arq. Univ. Fed. Rural Rio de collusor and Pe.(S.) ingens, which are capable of adapting to an ample Janeiro 7: 101–110. D’Almeida, J. M, and M. B. Fraga. 2007. Efeito de diferentes iscas na diversity of environments. For example, Pe.(E.) collusor has been atraçaõ de califorı´deos (Diptera) no Campus do Valonguinho, Universidade collected in areas of forest (Linhares 1981, D’Almeida 1984, Dias et al. Federal Fluminense, Niteroí, RJ, Brasil. Rev. Bras. Parasitol. Vet. 16: 1984, Yepes-Gaurisas et al. 2013) as well as more open habitats (Sousa 199-204. et al. 2011). Similarly, Pe.(S.) ingens has been found in both forests D’Almeida, J. M., and H. S. Lopes. 1983. Sinantropia de dı´pteros caliptratos (Vasconcelos et al. 2013) and more open areas, such as clearings (Sousa (Calliphoridae) no Estado do Rio de Janeiro. Arq. Univ. Fed. Rural Rio de et al. 2011). Janeiro 6:39–48. Dear, J. P. 1985. A revision of the new world Chrysomyini (Diptera: The large proportion of rare species (85% of the total) found in the Calliphoridae). Rev. Bras. Zool. 3: 109–169. sample reinforces the need for further surveys, which should increase Dias, E. S., D. P. Neves, and H. S. Lopes. 1984. Estudos sobre a fauna de the number of necrophagous sarcophagid species known to occur in the Sarcophagidae (Diptera) de Belo Horizonte, Minas Gerais. I. Levantamento state of Maranhaõ. taxonoˆmico e sinantro´pico. Mem. Inst. Oswaldo Cruz 79: 83 – 91. Esposito, M. C. 1997. The exotic species of Chrysomya (Diptera, Acknowledgments Calliphoridae) in the Amazonia: why they don’t occur in the Ferreira Penna Cientific Station, pp. 361–367. In P.L.B. Lisboa (ed.), Caxiuana˜. CNPq- We are grateful to the Reforestation Program for the Area of Museu Paraense Emı´lio Goeldi, Bele´m, Para´, Brazil. Permanent Preservation of the Estreito hydroelectric reservoir in the Esposito, M. C., and F. S. Carvalho-Filho. 2009. Moscas Varejeiras, pp. municipality of Estreito in Maranhaõ, coordinated by Dr. Paulo 30–32. In A.C.M. Oliveira, J. B. Santos, and M. C. Santos (eds.), Os Henrique Aragaõ Catunda of the Agronomy course at the Animais da Tanguro Mato Grosso-Diversidade na Zona de Transiçaõ entre Universidade Estadual do Maranhaõ in Imperatriz, Maranhaõ (Brazil). Floresta Amazoˆnica e o Cerrado. Museu Paraense Emı´lio Goeldi, Bele´m, Para´, Brazil. This work was supported by the Fundaçaõ de Pesquisa do estado do Esposito, M. C., J.R.P. Sousa, and F. S. Carvalho-Filho. 2009. Diversidade Maranhaõ, Process: Universal APP-01180/2010. Thanks also to de Calliphoridae (Insecta, Diptera) em ambientes de matas e pro´ximos de Universidade Estadual do Maranhaõ for providing a doctoral stipend habitaço˜es da Estaçaõ Cientı´fica Ferreira Penna (ECFPn), Melgaço/PA, e da to the first author. cidade de Portel/PA, pp. 461–469. In P.L.B. Lisboa (ed.), Caxiuana˜: Desafios para a Conservaçaõ de uma Floresta na Amazoˆnia. 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