Print version ISSN 1519-566X
Neotrop. entomol. vol.40 no.1 Londrina Jan./Feb. 2011
ECOLOGY, BEHAVIOR AND BIONOMICS
JRP de SousaI, II; MC EspositoII; FS Carvalho FilhoII
IDepto de Química e Biologia, Centro de Estudos Superiores de Imperatriz, Univ Estadual do Maranhão, Imperatriz, MA, Brasil
IIInstituto de Ciências Biológicas, Univ Federal do Pará, Belém, PA, Brasil
This study was carried out in the Base Operacional Geólogo Pedro de Moura (BOGPM) in the Urucu River Basin, Coari, state of Amazonas, Brazil, during April, June, and October 2007, in 16 areas, 4 in primary forests (environment MT) and 12 in gaps (environments C1, C2, and C3) at different stages of vegetation recovery, with different plant cover height. We collected 3,547 specimens of flesh flies. The 3,525 individuals identified to species level included 10 genera, 6 subgenera, and 23 species. Sarcodexia lambens (Wiedemann) (47.1%) and Peckia (Peckia) chrysostoma (Wiedemann) (19.1%) were the most abundant species. The abundance patterns and estimated richness differed between the environments, and were separated in two groups, one of the gaps (C1, C2, and C3) and another of forests (MT). Both abundance and estimated richness were higher in the gaps (C1, C2, and C3) than in the forest (MT).
Keywords: Community, ecology, flesh fly, anthropic impact
Flies of the family Sarcophagidae are very common and very similar to certain blowflies (Calliphoridae) in their appearance and habits. Most feed on decomposing organic matter, and some are invertebrate and vertebrate parasites (Guimarães & Papavero 1999). This family comprises about 2,600 described species worldwide, with about 800 species recorded in the Neotropics, 298 of them in Brazil (Pape 1996). They are found in all biogeographical regions, however most occur in tropical and warm-temperate regions (Shewell 1987).
Knowledge on the Amazon flesh flies is fragmentary, and the latest catalog of world species indicated fewer than 60 records for the Brazilian Amazon region (Pape 1996). Studies in specific locations of the Amazon include those of Lopes & Tibana (1991) on Maracá Island in the state of Roraima; Couri et al (2000) in Serra do Navio, state of Amapá; and Esposito & Linhares (2002), in Floresta Nacional Caxiuanã, state of Pará.
The family Sarcophagidae shows different degrees of synanthropy, with some species that live only in natural environments and others that are adapted to live in the human environment, and some species even depend on this kind of enviroment (Linhares 1981, Dias et al 1984a, D'Almeida 1984). This situation and the rapid population responses suggest the possibility that patterns of abundance and richness of Sarcophagidae could be used as indicators of anthropic interference on natural environments.
The Urucu River Basin region, in the Municipality of Coari, contains vast areas of preserved forest, but also forest gaps opened for prospection of oil and natural gas by Petrobrás S.A. Therefore, the region offers a rare opportunity to carry out studies on the effect of vegetation cover on the fauna. The fauna of blowflies in this area was studied by Paraluppi (1996) and Sousa et al (2010). The present study is the first on the fauna of Sarcophagidae in the region.
We studied the composition, abundance, and richness of the flesh fly fauna in the Urucu region, and compared the richness and abundance in environments with different vegetation cover. It was expected that the richness and abundance values for the family and species of Sarcophagidae would be different in the four environments sampled in the present study.
Material and Methods
This study is part of the research network "Evaluation of the bio-ecological dynamics and recomposition of areas altered by oil prospecting", in the area of Urucu, Amazonas, funded by the FINEP/CTPETRO project "Dynamics of forest gaps impacted by oil exploration." It was carried out in the oil exploration area of PETROBRÁS S.A., Base Operacional Geólogo Pedro de Moura (BOGPM) located in the region of the Urucu River Basin, Coari, Amazonas. The area is 600 km west of the city of Manaus, between 4º51'18" and 4º52'16" S and 65º17'58" and 65º20'01" W, altitude between 60 m and 70 m, and is 514,000 ha in extent (Fig 1).
Sixteen study areas were selected, at least 1 km distant from each other (Fig 1). Four of them were in primary forest, and 12 in gaps at different stages of vegetation recovery and differing in their plant cover height, according to Pillar (1996). The four types of environments were: 1) MT, areas of preserved forests; 2) C1, gaps with little recovery, herbaceous vegetation of varying heights from 30 cm to 50 cm; 3) C2, gaps in an intermediate stage of recovery, shrubby vegetation I, height from 50 cm to 2 m; and 4) C3, well recovered gaps, shrubby vegetation II, between 2 m and 5 m in height. The environments were considered as sampling units, and in each environment three collections were made in order to obtain a more representative effort. These three collections were made in April, June, and October 2007.
We utilized flytraps as described by Almeida et al (2003), baited with 50 g of rotting beef lung. The traps were exposed for 48h in the field. We used four traps in each environment, totaling 16 traps per environment, 64 traps per collection, and 192 traps at the end of three collections.
The traps were placed in the center of the gap areas from the north-south and east-west positions, not more than 50 m apart. In the forest areas, the traps were placed in a similar way, but at 300 m from the forest edge.
Flesh-fly identification was based on Lopes (1939, 1946, 1958, 1976, 1989), Lopes & Tibana (1982, 1987), and Pape & Mello-Patiu (2006). Part of the material was deposited at the Entomological Collection of the Museu Paraense Emílio Goeldi (MPEG), Belém, Pará.
In order to assess if the sampling effort was sufficient to sample all available species in this locality, we utilized the following richness estimators: Chao 1, Chao 2, Jack2 (second-order Jackknife), ICE (Incidence-based Coverage Estimator), ACE (Abundance-based Coverage Estimator), and Bootstrap, by using the Estimate S 8.0 software (Colwell 2006a). The non-parametric estimators for species richness that are based on rare species richness use four variables: singletons, doubletons, uniques, and duplicates (Colwell 2006b). These methods of analysis were used because they analyze data with different abundance distributions (Santos 2006).
In order to compare species richness in the 16 environments, we used the rarefaction method based on the number of individuals by specimen, using the BioDiversity Pro 2.0 software (McAleece et al 1997). This relationship of richness to abundance (rarefaction curve) (Magurran 2004) was calculated in order to determine differences between the areas, using a cutoff score equivalent to the lowest abundance found in the areas (18 individuals in the M28 area). According to Ricklefs (1996) and Magurran (2004), this analysis is appropriate when the samples include different numbers of individuals, as in this case; in this way, subsamples of equal size of individuals are taken randomly, and thus an estimate of the richness is obtained that makes the samples comparable to each other.
The four kinds of environment were compared with respect to the estimated richness and abundance pattern for the family and for the more numerous species, with the one-criterion variance analysis (Ayres et al 2007). The abundance of species was processed through the function log n (x + 1) to decrease the influence of numerical range of taxa more abundant. The normality of the data was checked by the Lilliefors test (k samples) (Ayres et al 2007). These analysis were carried out using the BioEstat 5.0 statistical software (Ayres et al 2007), and the results were considered significant when P < 0.05.
Composition and abundance
A total of 3,547 flesh flies were collected, and 3,525 individuals were identified to species level. These represented 10 genera, six subgenera, and 23 species (Table 1). The most abundant species were Sarcodexia lambens (Wiedemann) with 47.1% of the total individuals, followed by Peckia (Peckia) chrysostoma (Wiedemann) with 19.1% (Table 1).
The analysis of species incidence and abundance patterns for the total samples, with observed richness of 23 species and abundance of 3,525 individuals, estimated a minimum of 26 (Bootstrap) and a maximum of 59 species (ICE) (Fig 2). The number of rare species ranged between one and 10, distributed as follows: two doubletons, one duplicate, eight singletons, and 10 uniques (Fig 3).
Comparison between richness and abundance of flesh flies in the different environments
The order of richness observed ranged from three species, in area M25 (MT) to 13, in areas J23 (C2) and R7 (C3). The estimation of richness of species of flesh flies for each area by the rarefaction method indicated the following order of richness: a minimum of three in M25 (MT) for a total of 18 individuals collected and seven in J16 (C3), for the highest estimate with the same number of individuals collected. The forests showed the lowest species richness per individual, with an estimated species number less than five (Fig 4).
The rarefaction analysis indicated the formation of two groups, one formed by four areas of forest (environment MT), with lower richness, and the other by areas of forest gaps (environments C1, C2, and C3), with higher richness (Fig 4).
The estimated richness of flesh flies for the different environments was different as calculated by the rarefaction method (F = 11.6015, DF = 3, P = 0.001). The multiple comparison test showed a significant difference between (C1 - MT), (C2 - MT) and (C3 - MT) (Table 2).
The abundance values for the 16 sampled areas are available as Online Supplementary Material. The abundance differed among the environments (F = 36.5156, DF = 3, P < 0.0001) (Table 3). The comparison among environments indicated significant differences among the pairs (C1 - MT), (C2 - MT) and (C3 - MT) (Table 3). The comparison among the environments (C1 - C2), (C1 - C3), and (C2 - C3) was not significant (Table 3).
The abundance of the eight most numerous species also differed among the environments (Table 4). The comparison of environments showed differences between the pairs: (C1 - MT), (C2 - MT) and (C3 - MT) for the species Oxysarcodexia amorosa (Schiner), Oxysarcodexia fringidea (Curran & Walley), Peckia (Pattonella) intermutans (Walker), P. (P.) chrysostoma, Peckia (Squamatodes) ingens (Walker), S. lambens, and Sa. cuneata (Table 4); and between the pairs: (C1 - MT); (C2 - MT), (C3 - MT) and (C2 - C3), for Oxysarcodexia thornax (Walker) (Table 4).
Composition and abundance
The species Peckia (Euboettcheria) epimelia (Lopes) and Sarcofahrtiopsis cuneata Townsend are new records for the Brazilian Amazon. The former species had been recorded only for the state of São Paulo, and the latter for the states of Ceará, Pernambuco, and Rio de Janeiro (Pape 1996). Helicobia pilifera Lopes and Titanogripa (Cucullomyia) luculenta Lopes are new records for the state of Amazonas. Helicobia pilifera was previously recorded in Pará (Tibana 1981), and T. (C.) luculenta in Amapá (Lopes 1976). Couri et al (2000) reported S. lambens from the Serra do Navio, Amapá; and Esposito & Linhares (2002) reported P. (P.) chrysostoma in the Floresta Nacional Caxiuanã, Melgaço, PA, where both species were also the most abundant ones.
The curve of doubletons and duplicate species showed that they had stabilized. However, the curves of singletons and uniques showed moderate growth, without stabilizing. According to the classification parameters of Toti et al (2000), the estimates for this family did not show good performance, suggesting that the sampling effort was not sufficient to show the richness of the area.
The family Sarcophagidae is very diverse in the Neotropical region, with over 750 described species, over 298 of them recorded from Brazil (Pape 1996). Because of the large number of species and the variety of their habitats, an additional sampling effort is necessary in order to obtain the total species richness in this locality.
Comparison between richness and abundance of flesh flies in the different environments
Although the gaps did not show differences between the abundance and estimated richness patterns, they were different from the forests. The flesh flies did not show sensitivity in relation to types of gaps, as was recorded for blow flies by Sousa et al (2010); but did show differences between gaps and forests.
Ferraz et al (2009) recorded a lower richness of blowflies species at locations near to the entrance (greater anthropic impact) of the Reserva Biológica de Tinguá, Nova Iguaçu, Rio de Janeiro. Sousa et al (2010) found a lower richness of blowflies species in gaps in the Urucu River Basin, Coari, Amazonas.
The occurrence of more species of flesh flies in gap environments may be related to the physical conditions and to the variety of available resources in these environments. The resources in open environments are more exposed to rain and dryness, which makes them more ephemeral. Because the Sarcophagidae are viviparous or ovoviviparous (Shewell 1987), their larvae remain for shorter periods in the substrates where they breed, and they are therefore less exposed to the environmental conditions in the forest gaps. This characteristic may confer an advantage to the Sarcophagidae in exploiting resources in open areas.
The family Sarcophagidae was more abundant in gap environments than in the forests. This may be related to the ample capacity of adaptation to the human-modified environments shown by flesh flies, even becoming dependent on them. The eusynanthropic characteristic of some species of this family has been already recorded (Linhares 1981, Dias et al 1984a, D'Almeida 1984).
In a study in three distinct ecological areas (urban, rural, and forest) in Belo Horizonte, Minas Gerais, Dias et al (1984b) reported that the flesh flies were attracted most by decomposing organic matter, and human feces was the most attractive bait. Antonini et al (2005) found that flesh flies were more abundant in marginal sites of a forest fragment than inside it, in Belo Horizonte.
Peckia (Pa.) intermutans was the most abundant species in the forests (Table 5). According to Linhares (1981) and D'Almeida & Lopes (1983), this is a hemisynanthropic and necrophagous species, which develops in animal carcasses.
The other common species were more abundant in forest gap areas (C1, C2, and C3) (Table 5). Of these species, S. lambens and P. (P.) chrysostoma were considered eusynanthropic by D'Almeida (1984) and Ferraz (1995). Peckia (P.) chrysostoma was more abundant in environments closer to residences than in forested environments at two sites in the Floresta Nacional Caxiuanã, (Base of the Estação Científica Ferreira Pena and Boca do Curuá).
The abundance pattern and estimated richness of flesh flies were not able to separate the gap environments, but did separate gaps from forests. The association with human-impacted environments suggests that this taxon may be appropriate to evaluate anthropic impacts such as deforestation.
Almeida IM, Ribeiro-Costa CS, Marioni L (2003) Manual de coleta, conservação, montagem e identificação de insetos. Série manuais práticos em biologia - 1, Ribeirão Preto, Holos Editora, VIII+78p. [ Links ]
Antonini Y, Accacio GM, Brant A, Cabral BC, Fontenelle JCR, Nascimento MT, Thomazini APBW, Thomazini MJ (2005) Insetos, p.239-273. In Ministério do Meio Ambiente (ed) Fragmentação de ecossistemas: causas, efeitos sobre a biodiversidade e recomendações de políticas públicas. Brasília, MMA/SBF, 2nd ed., 508p. [ Links ]
Ayres M, Ayres Jr M, Ayres DL, dos Santos AS (2007) BioEstat 5.0 - aplicações estatísticas nas áreas das ciências biológicas e médicas. Belém, Sociedade Civil Mamirauá, 364p. [ Links ]
Colwell RK (2006a) Statistical estimation of species richness and shared species from samples. Version 8.0. University of Connecticut, USA. Available at: http://purl.oclc.org/estimates . Accessed on 10 July 2007. [ Links ]
Colwell RK (2006b). EstimateS: statistical estimation of species richness and shared species from samples. Version 8.0. User's guide and application. University of Connecticut, USA. Available at: http://purl.oclc.org/estimates . Accessed on 10 July 2007. [ Links ]
Couri MS, Lamas CJE, Aires CCC, Mello-Patiu CA, Maia VC, Pamplona DM, Magno P (2000) Dípteros da Serra do Navio (Amapá, Brasil): Asilidae, Bolbilidae, Calliphoridae, Micropezidae, Muscidae, Sarcophagidae, Stratiomyiidae, Syrphidae, Tabanidae e Tachinidae. Rev Bras Zoociências 2: 91-100. [ Links ]
D'Almeida JM (1984) Sinantropia de Sarcophagidae (Diptera) na região metropolitana do estado do Rio de Janeiro. Arq Univ Fed Rio J 7: 101-110. [ Links ]
D'Almeida JM, Lopes HS (1983) Sinantropia de dípteros caliptratos (Calliphoridae) no estado do Rio de Janeiro. Arq Univ Fed Rur Rio J 6: 39-48. [ Links ]
Dias ES, Neves DP, Lopes HS (1984a) Estudos sobre a fauna de Sarcophagidae (Diptera) de Belo Horizonte, Minas Gerais. I. Levantamento taxonômico e sinantrópico. Mem Inst Oswaldo Cruz 79: 83-91. [ Links ]
Dias ES, Neves DP, Lopes HS (1984b) Estudos sobre a fauna de Sarcophagidae (Diptera) de Belo Horizonte, Minas Gerais. III. Atratividade das isca. Mem Inst Oswaldo Cruz 79: 413-417. [ Links ]
Esposito MC, Linhares AX (2002) Califorídeos e outros muscóides da Estação Cientifica Ferreira Penna, p.579-585. In Lisboa PLB (ed) Caxiuanã populações tradicionais. meio físico & diversidade biológica. Belém, Conselho Nacional de Pesquisas - Museu Paraense Emílio Goeldi, 734p. [ Links ]
Ferraz ACP, Gadelha B de Q, Aguiar-Coelho VM (2009) Análise faunística de Calliphoridae (Diptera) da Reserva Biológica do Tinguá, Nova Iguaçu, Rio de Janeiro. Rev Bras Entomol 53: 620-628. [ Links ]
Ferraz MV (1995) Larval and pupal periods of Peckia chrysostoma and Adiscochaeta ingens (Diptera: Sarcophagidae) reared under laboratory conditions. Mem Inst Oswaldo Cruz 90: 611-614. [ Links ]
Guimarães JH, Papavero N (1999) Myiasis of man and animals in the Neotropical Region. São Paulo, Editora Plêiade, 380p. [ Links ]
Linhares AX (1981) Synanthropy of Calliphoridae and Sarcophagidae (Diptera) in the city of Campinas, São Paulo, Brasil. Rev Bras Entomol 25: 189-215. [ Links ]
Lopes HS (1939) Contribuição ao conhecimento do genero Helicobia Coquillett (Dipt. Sarcophagidae). Rev Entomol 10: 497-517. [ Links ]
Lopes HS (1946) Contribuição ao conhecimento das espécies do gênero Oxysarcodexia Townsend, 1917 (Diptera Sarcophagidae). Bol Esc Nac Vet 1: 62-134. [ Links ]
Lopes HS (1958) Considerações sobre as espécies de Peckia Desvoidy, 1830 e de gêneros afins. (Diptera-Sarcophagidae). An Acad Bras Cienc 30: 211-239. [ Links ]
Lopes HS (1976) On the holotypes, mostly females of Sarcophagidae (Diptera) described by Francis Walker. Rev Bras Biol 36: 629-146. [ Links ]
Lopes HS (1989) On American Sarcophagidae (Diptera) with revision of Pekiamyia Dodge. Rev Bras Biol 49: 837-845. [ Links ]
Lopes HS, Tibana R (1982) Sarcophagid flies (Diptera) from Sinop, state of Mato Grosso, Brazil. Mem Inst Oswaldo Cruz 77: 285-298. [ Links ]
Lopes HS, Tibana R (1987) On Oxysarcodexia (Diptera, Sarcophagidae), with descriptions of five new species, key, list and geographic distribution of the species. Rev Bras Biol 47: 329-347. [ Links ]
Lopes HS, Tibana R (1991) Sarcophagidae (Díptera) de Roraima, Brasil. Acta Amazonica 21: 151-159. [ Links ]
Magurran AE (2004) Measuring biological diversity. Oxford, Blackwell Science, 256p. [ Links ]
McAleece N, Lambshead PJD, Paterson GLJ (1997) BioDiversity Pro (Version 2). London, The Natural History Museum & The Scottish Association for Marine Science. Available at: http://www. sams.ac.uk/research /software /bdpro.zip/view. Accessed on 12 Nov 2007. [ Links ]
Pape T (1996) Catalogue of Sarcophagidae of the world (Insecta: Diptera). Mem Entomol Int 8: 1-558. [ Links ]
Pape T, Mello-Patiu CA (2006) Revision of Engelimyia Lopes, 1975 (Diptera: Sarcophagidae). Zootaxa 1256: 21-47. [ Links ]
Paraluppi ND (1996) Calliphoridae (Diptera) da Bacia do Alto Rio Urucu, Amazônia Central, Brasil. Rev Bras Zool 13: 553-559. [ Links ]
Ricklefs RE (1996) A economia da natureza. Rio de Janeiro, Guanabara Koogan, 3rd ed., 470p. [ Links ]
Santos AJ (2006) Estimativas de riqueza em espécies, p.19-41. In Cullen Jr L, Rudran, Valladares-Padua C (orgs) Métodos de estudos em biologia da conservação e manejo da vida silvestre. 2 ed. Curitiba, UFPR, 652p. [ Links ]
Sousa JRP de, Esposito MC, Carvalho Filho FS (2010) A fauna de califorídeos (Díptera) das matas e clareiras com diferentes coberturas vegetais da Base de Extração Petrolífera, bacia do Rio Urucu, Coari, Amazonas. Rev Bras Entomol 54: 270-276. [ Links ]
Shewell GE (1987) Sarcophagidae, p. 1159-1186. In McAlpine JF, Peterson BV, Shewell GE, Teskey HJ, Vockeroth JR, Wood DM (eds) Manual of Nearctic Diptera. Vol. 2. Agriculture Canada Monograph, 28. [ Links ]
Tibana R (1981) Estudo sobre 7 espécies de Helicobia Coquillett, 1895 (Diptera, Sarcophagidae). Rev Bras Biol 41: 625-634. [ Links ]
Toti DS, Coyle FA, Miller JA (2000) A structure inventory of appalachian grass bald and heath bald spider assemblages and a test of species richness estimator performance. J Arachnol 28: 329-345. [ Links ]
José RP de Sousa,
Depto de Química e Biologia, Centro de Estudos Superiores de Imperatriz,
Univ Estadual do Maranhão, Rua Godofredo Viana 1300, Bairro União,
65901-430, Imperatriz, MA, Brasil;
Received 29 June 2009 and accepted 07 October 2010
Edited by Og de Souza - UFV