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ECOSYSTEMS • An. Acad. Bras. Ciênc. 97 (1) • 2025 • https://doi.org/10.1590/0001-3765202520240561 linkcopy

Open-access Spatial distribution and habitat preference of sarcosaprophagus Calliphoridae (Diptera) in the Brazilian Northeast, with notes on the utilization of different animal baits

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Abstract

Brazil is a country with one of the greatest biodiversities in the world, in addition to the high diversity of biomes that directly influences the composition of fauna and flora. In this context, the analysis of the potential distribution of calliphorids in the Northeast can generate important information for forensic entomology and conservation biology. This study aims to identify the current and potential distribution of the main species of flies from the family Calliphoridae of forensic interest in the Northeast region of Brazil. For this purpose, field and bibliographic data were collected and analyzed. The obtained data were used to develop ecological models based on the MaxEnt model. The analyses showed that the exotic species Chrysomya albiceps (Wiedemann, 1819) and Chrysomyia megacephala (Fabricius, 1794) are the most common species in Northeast environments, presenting a wide spatial distribution. On the other hand, native taxa have a more restricted distribution, except for the species Cochliomyia macellaria (Fabricius, 1775). The variables that most influenced the models were precipitation and wind. The ecological models presented in this study demonstrate an overlap in the distribution of exotic and native species, which may pose a risk of competition and future homogenization of assemblies.

Key words
Sarcosaprophagus insects; ecological modeling; blow flies; ephemeral resources

INTRODUCTION

Calliphoridae is a family of sarcosaprophagus dipterans with great potential for forensic, medical, and environmental research. The taxon comprises more than 1,500 species distributed across 97 genera (Pape et al. 2011), whose specimens are common and highly abundant among the first colonizers of a cadaver (Catts & Goff 1992), making them targets of forensic research. In the forensic scope, in addition to aiding in the estimation of the post-mortem interval (PMI), dipterans can also be used to obtain evidence of cadaver movement (Greenberg 1985, Catts & Goff 1992); however, this applicability depends on the knowledge of the spatial distribution of the taxa.

Considering that the composition and structure of assemblies, as well as the distribution of species, are influenced by seasonality, habitat type and food resources, anthropogenic disturbances, and microclimatic conditions (Patitucci et al. 2011, Vasconcelos et al. 2015, Sousa et al. 2014, Dufek et al. 2019, Barbosa et al. 2017, Hodecek & Jakubec 2022), it is essential to know the local distribution and habitat preferences. This is because the family includes species with a broader geographical distribution (e.g., Chrysomya Robineau-Desvoidy, 1830 and Lucilia Robineau-Desvoidy, 1830), while others are more restricted to certain types of environments, including groups sensitive to anthropogenic changes (e.g., Hemilucilia Brauer, 1895) (Whitworth 2010, Cabrini et al. 2013, Sousa et al. 2014).

In this context, predictive models of spatial distribution are important tools for studies related to ecology, conservation, and the management of resources and invasive species (Arasato & Amaral 2013, Yang et al. 2013). These models of geographic distribution also help to fill gaps in knowledge about the geographical boundaries of the studied species, helping to understand which climatic and environmental characteristics influence their distribution (Carvalho et al. 2017). This approach consists of a computational process capable of combining species occurrence data with environmental/ecological variables (biotic and abiotic factors, temperature, precipitation, elevation, geology, and vegetation), generating representations of the necessary conditions for species occurrence (Giannini et al. 2012, Anderson et al. 2003).

The predictive approach is fundamental to determining the likely distribution of a taxon in countries or regions that are megadiverse and have many gaps in fauna mapping. This is the case of the Northeast region of Brazil, consisting of nine states: Alagoas (AL), Bahia (BA), Ceará (CE), Maranhão (MA), Paraíba (PB), Pernambuco (PE), Piauí (PI), Rio Grande do Norte (RN), and Sergipe (SE), and a complex diversity of habitats and/or biomes, including the main ones: Amazon, Caatinga, Cerrado, and Atlantic Forest (Figure 1) (IBGE 2022).

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Figure 1
Biome type (Amazon, Caatinga, Cerrado, and Atlantic Forest) and spatial location of Northeastern Brazil, composed of the states of Alagoas (AL), Bahia (BA), Ceará (CE), Maranhão (MA), Paraíba (PB), Pernambuco (PE), Piauí (PI), Rio Grande do Norte (RN), and Sergipe (SE).

These sub-regions present distinct geo-environmental characteristics, which can influence the presence or absence of calliphorids. The Meio-Norte region exhibits a transition zone between the Sertão and the Amazon Rainforest, with rainfall, perennial rivers, and a large amount of groundwater. This sub-region encompasses the biomes of Cerrado, Caatinga, and Amazon Rainforest (Silva & Coutinho 2018), as observed in the state of Maranhão. The Agreste is the transition between the northeastern coast and the hinterland, presenting characteristics of both geo-environments. In this domain, the climate is sub-humid, and the typical vegetation is Caatinga, but with elements of Atlantic Forest and Cerrado (Rebouças 1997, Veloso 1964). It extends from Rio Grande do Norte to Bahia. The Sertão, also referred to as semi-arid, is characterized by periodic droughts, sandy soils, saline, and nutrient-poor. Occupying from parts of Rio Grande do Norte to Bahia, Ceará, and part of Piauí, the basic vegetation is Caatinga, which presents a great variety of formations adapted to long dry seasons (Rebouças 1997). Finally, the Zona da Mata is the coastal strip that extends from Rio Grande do Norte to the southern region of Bahia, represented by the Atlantic Forest (Rebouças 1997, Silva & Coutinho 2018).

In the last two decades, the number of studies with flies in northeastern environments has been increasing, with records in different biomes of the region: Amazon Rainforest and Cerrado (Sousa et al. 2015, Nascimento et al. 2021, Leite et al. 2023, Santos et al. 2024, Silva et al. 2023a, b, c), Caatinga (Alves et al. 2014, Oliveira & Vasconcelos 2020), Atlantic Forest (Vasconcelos et al. 2015, Carmo et al. 2017, Barbosa et al. 2020), and coastal and urban environments (Vasconcelos et al. 2015, Barbosa et al. 2017, Medeiros et al. 2023). However, there is still a significant gap, especially in the Caatinga areas and states such as Alagoas, Sergipe, and Piauí. Therefore, this study aims to generate predictive models of the potential spatial distribution of flies from the Calliphoridae family using a predictive approach. Additionally, the use of animal baits and habitats will be analyzed to understand the scenarios of distributions of exotic vs. native species.

MATERIALS AND METHODS

Species data

A dataset on the spatial distribution, habitat preference, and feeding behavior of Calliphoridae species commonly associated with animal baits, carcasses, and cadavers was compiled from major scientific journal platforms (Periódicos Capes; PubMed; Scientific Electronic Library Online (Scielo); and Science Direct). The database was constructed from 67 publications and data from field studies conducted by the Insect and Vector Laboratory of the Universidade Federal do Rio Grande do Norte (Live-UFRN). Data from 18 species distributed across seven genera were compiled, resulting in 840 collection records from different states, with missing data for Alagoas and Piauí.

This study’s database was built from scientific articles published between 2000 and 2024, using the keywords: Calliphoridae, Califorídeos, Nordeste, Brasil, Moscas, Entomologia Forense, Blow flies, Calliphorids, Northeast, Brazil, Flies, Forensics Entomology. During the searches, the collected data were organized into a table, and the geographic coordinates (latitude and longitude) were transformed into decimal degrees (datum SIRGAS2000) for analysis. Inconsistent data or data lacking geographical references were corrected by comparing with the information contained in the respective publications.

Data analysis and ecological modeling

For the analysis and construction of graphs on feeding preference, the pivot table tool in Microsoft Office Excel (https://www.office.com/) was used. The spatial distribution of Calliphoridae species in Northeastern Brazil was performed using ArcGIS 10.4 software (https://www.arcgis.com).

Ecological models using the MaxEnt (Maximum Entropy) method (Phillips et al. 2006) were used to estimate the potential distribution of species, utilizing MaxEnt 3.4.4 software (https://biodiversityinformatics.amnh.org/open_source/maxent/). MaxEnt is used to infer and/or predict distribution from incomplete data, being suitable for any presence data set and considered efficient for modeling small samples. This algorithm generates probabilities of distribution for a given species in a specific region, based on different variables, such as temperature (minimum, maximum and average temperature), variation, solar radiation, wind speed, water vapor pressure and environmental variations (vegetation and topography) (Phillips et al. 2006, Martínez-Calderas et al. 2015).

WorldClim climatic variables, version 2.1 (https://www.worldclim.org), and the main components obtained from them (Honorato et al., 2021) were obtained from the Ambdata project website (http://www.dpi.inpe.br/Ambdata/) and used to estimate the potential distribution of species.

RESULTS

Habitat distribution and feeding preference

The publications used were primarily from the states of Maranhão, Pernambuco and Rio Grande do Norte (Table I). Only three states did not have Calliphoridae collection records: Alagoas and Piauí. The species Chrysomya albiceps (Wiedemann, 1819) and Chrysomya megacephala (Fabricius, 1794) were found in the six states that has previous studies in the Northeast region of Brazil, being the only species with more than 100 records (Table I, Appendix). The species Hemilucilia benoisti Séguy 1925, Hemilucilia townsendi Shannon, 1926, and Paralucilia paraenses (Mello, 1969) are restricted to Maranhão, while the species Calliphora lopesi Mello 1962, Hemilucilia souzalopesi Mello 1972 and Paralucilia fulvinota (Bigot, 1877) occurs only in the state of Pernambuco (Table I).

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Table I
Number of blow flies’ species records by state in the Northeast, Brazil (2000-2024). BA - Bahia; CE - Ceará; MA - Maranhão; PB - Paraíba; PE - Pernambuco, RN - Rio Grande do Norte and SE - Sergipe.

On the other hand, Calliphora vicina Robineau-Desvoidy, 1830 occurs in the state of Ceará and Pernambuco, while Lucilia sericata (Meigen, 1826) appears in Maranhão and Pernambuco. Regarding biomes and habitats, 14 different environments were recorded, and the abundance of species and records were compared. It was observed that records are more common in Cerrado, Caatinga, and Atlantic Forest areas, as well as in the abundance of specimens.

Regarding the feeding preference of species, the database evidenced a wide diversity of baits used for fly collection (Figure 2, Appendix). Among them, bovine substrate was the most used in collections, representing about 46% of the records. Swine substrate was the second most used (15%), followed by fish, chicken, human, and others (Figure 2).

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Figure 2
Ephemeral resources (baits and carcasses) used in the capture of Calliphoridae, characterized by published articles for the Northeast region, Brazil. *Rat, liver (unspecified origin), cat, goat, dog and ostrich.

Ecological modeling

The ecological modeling of Calliphoridae species obtained using the MaxEnt method is visualized in Figure 3. The study revealed that the exotic species (C. albiceps, C. megacephala, and Chrysomya putoria (Wiedemann, 1818) have a wide distribution throughout the region, with a spatial pattern similar to the native species most common in the studies (Chloroprocta idioidea (Robineau-Desvoidy, 1830), Lucilia eximia (Wiedemann, 1819), and Cochliomyia macellaria (Fabricius, 1755). On the other hand, H. benoisti and P. paraensis show more restricted distributions in the Mid-North region compared to other Calliphoridae species.

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Figure 3
Maximum entropy probability distribution of Calliphoridae species in Northeastern Brazil, based on geographic data from Calliphoridae specimen collection. The color gradient indicates the probability of the species’ presence at the location: redder colors indicate a higher chance of presence, and bluer colors indicate absence of presence.

Hemilucilia species present a distribution closer to the coast and Mid-North region, however Hemilucilia semidiaphana (Rondani, 1850) has a wider distribution compared to Hemilucilia segmentaria (Fabricius, 1805) (Figure 3). It is also worth noting that the predator species, C. albiceps, presents distribution overlap with all other species (Figure 3). Cochliomyia hominivorax (Coquerel, 1858) also exhibited a wide distribution, with higher intensity in the Mid-North and semiarid areas (Figure 3).

Of the variables used, precipitation and wind speed were the most significant for the creation of the maps. Precipitation had a higher contribution rate to the modeling of the species C. idioidea, C. albiceps, C. megacephala, C. putoria, C. hominivorax, C. macellaria, H. benoisti, H. segmentaria, and L. eximia. Wind, on the other hand, showed higher contribution rates to the species C. idioidea, C. albiceps, C. megacephala, C. putoria, C. hominivorax, C. macellaria, H. segmentaria, H. semidiaphana, and L. eximia (Table II).

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Table II
Variables with the highest contribution rates to the ecological modeling of the species. BA - Bahia; CE - Ceará; MA - Maranhão; PB - Paraíba; PE - Pernambuco and RN - Rio Grande do Norte.

The analyses also showed that P. paraenses was the only species that presented a distribution influenced by other variables (one biological and solar radiation). Additionally, H. semidiaphana and P. paraenses were the only species without direct influence of the best variables for model construction (precipitation and wind speed) from precipitation, although the biological variables of MaxEnt are derived from monthly temperatures and rainfall, meaning that precipitation can be inferred as the main variable of the ecological model, directly or indirectly.

DISCUSSION

Historical data collected from scientific platforms revealed that Calliphoridae specimens are widely distributed across various habitats in Northeastern Brazil. However, it is difficult to determine the true spatial distribution due to gaps or absence of studies in some areas. Historically, research on sarcosaprophagus flies in the region has focused on the states of Pernambuco, Paraíba, Rio Grande do Norte, and Maranhão, with more sporadic records in other states (Vasconcelos & Araújo 2012, Sousa et al. 2015, Alves et al. 2014, Jales et al. 2020). Additionally, the frequent use of baits in studies may be associated with difficulties and ethical concerns regarding the use of carcasses or cadavers, as well as the ease of greater replicability in ecological studies and good representation of the dipterofauna (Farinha et al. 2014).

Based on the maximum entropy ecological model, it can be observed that exotic (C. albiceps, C. megacephala, and C. putoria) and native (C. idioidea, C. macellaria, P. paraenses, H. segmentaria, and H. semidiaphana) species exhibit overlapping distribution and potentially ecological niches. This could pose a risk of competition and future homogenization of assemblages, mainly due to the fact that Chrysomya species are voracious competitors and predators of native species (e.g., C. macelaria and L. eximia) (Faria et al. 2004, Carmo et al. 2018, Barbosa et al. 2021). Furthermore, the modeling results demonstrate that this distribution overlap occurs across different habitats, being more pronounced in the coastal, sertão, and Mid-North regions. This similarity can be explained by the proximity of spatially recorded points in the literature, as some studies show that the closer geographically groups are to each other, the greater the tendency for them to be similar, favoring coexistence between communities (Menezes et al. 2016).

The adaptation of Chrysomya species to the characteristics of new habitats is remarkable. Within less than a century of their introduction into Brazil, the modeling showed that this taxon will be present in all states and environments of the Northeast. This is a warning for environmental agencies, as some cases have empirically shown that Chrysomya species can displace native species that share similar ecological niches (Mello et al. 2007, Carmo 2016). Mello et al. (2007) emphatically state that in the past four decades, the population dynamics and spatial distribution of Calliphoridae species in Brazil have been modified by the introduction of the Chrysomya genus and by anthropogenic modifications. Native species such as L. eximia and C. macellaria have experienced a decrease in population density due to lower success in competition, fecundity rate, and development time in the presence of Chrysomya (Spindola 2017, Galindo 2009, unpublished data).

However, the spatial distribution models presented here are based on geographic occurrence data for species crossed with environmental data, generating predictive data for areas with a higher degree of environmental suitability. Thus, this predictive distribution may differ in future analyses that take into account the interactions between taxa. Here we consider the idea of the fundamental niche, described by Grinnell (1917), which refers to the set of environmental conditions in which a species is capable of maintaining its populations without migration processes (Peterson & Vieglais 2001).

Among the environmental conditions, wind and precipitation were the variables that most contributed to the species’ distribution pattern. Wind can generate positive responses in Calliphoridae populations, as it facilitates the dispersion of decomposition odors in the environment, which are important in locating ephemeral resources suitable for feeding and development sites (Mohr & Tomberlin 2014). Vogt et al. (1983), Gennard (2012), and Mohr & Tomberlin (2014) have also shown that variations in wind speed can affect the flight capacity and consequently the dispersal of Calliphoridae species, justifying the high contribution of the wind variable. Such an effect of wind on the flight of flies may also be related to the shape of the wings, since the three-dimensional undulation of fly wings can alter the distribution of wind forces during flight, although the rectangular-shaped wings of blowflies, an ideal wing for rotation (eg. Calliphora), exhibit good aerodynamics (Krishna et al. 2020).

In the tropics, blow fly population peaks are directly linked to different rainy seasons (Gennard 2012). Works such as those by Dias et al. (2009), Gonçalves et al. (2011), and Mello et al. (2007) have shown that species such as C. megacephala and C. albiceps have higher abundance with increased precipitation, which is consistent with the data obtained from ecological modeling. This can support the wider distribution of these species in regions where biomes have higher precipitation rates, such as the Atlantic Forest and Amazon, when compared to drier biomes such as the Caatinga. On the other hand, this may still be associated with a greater supply of food, since during the dry season, the ephemeral resource dries out faster and loses its attractiveness (Vasconcelos et al. 2023, Leite et al. 2023).

Furthermore, chronological data reveal the need for more studies in the diverse environments of the Northeast, although the number of records and studies has been increasing recently. The works used present collection data from the past two decades, which can naturally undergo changes over time, either due to ecological interactions of the species studied, anthropogenic actions, or global climate change. Besides having experienced an El Niño, which modulated precipitation indices in northern South America, where rainfall accumulations were close to or below average in most of the Northern and Northeastern regions of Brazil (Andrade et al. 2023, INMET 2024).

One of the greatest threats to biodiversity arises from the occupation of natural landscapes by anthropogenic actions, with habitat removal and the formation of smaller and isolated fragments being the most direct consequences (Tôrres & Vercillo 2012). In recent years, there has been deforestation of a large part of the native vegetation of the Amazon and Cerrado biomes, especially in the Amazon region, which presents high rates of degradation and deforestation (Strassburg et al. 2017, Carvalho et al. 2023), leading to a depletion of the region’s biodiversity and changes in the hydrological cycle, which can cause suppression of rainfall in nearby areas (Soares et al. 2019).

The loss of forest poses an extinction risk for H. benoisti and P. paraenses, which appear to be more restricted to this type of environment. Furthermore, the more restricted distribution of some species of Calliphora, Hemilucilia and Paralucilia may reflect a preference for more preserved forest areas, since Hemilucilia species with strong preference for preserved environments (Cabrini et al. 2013).

Besides the environmental concerns, the data from this study have forensic and sanitary implications, as Calliphoridae are associated with cases of animal and human myiasis in the Northeast (Barbosa & Vasconcelos 2015, Martins et al. 2021), especially C. hominivorax, which also has a wide distribution in the Northeast, particularly in the Maranhão region and states in semiarid areas. In the Neotropical region, the genera Cochliomyia Townsend, 1915, Lucilia, Calliphora Townsend, 1908 and Chrysomya are the species most often cited as etiological agents of myiasis (Moretti & Thyssen 2006). From a forensic perspective, this probability of species distribution can support future studies on the movement of bodies between areas, especially those species with restricted spatial distribution. However, more studies are needed to confirm the distribution predicted by ecological models.

Another curious fact is the information gap identified here for some northeastern states, reflecting the recent interest in dipterans in the region, especially within the scope of Forensic Entomology. The lack of data for the states of Alagoas and Piauí may have limited the models and the actual distribution of species, although the characteristics of these states are similar to those of other Northeastern states. Furthermore, we previously believe that many species occur in these states, however, to confirm this hypothesis, future faunal surveys in these areas are necessary.

Ecological models confirm the pattern observed in many inventories, showing the probable niche overlap between exotic and native species, i.e., competition within the same sample (Alves et al. 2014, Sousa et al. 2015, Carmo et al. 2017, Jales et al. 2020). It is expected that the models presented in this study can support future ecological research and assist environmental and health surveillance agencies. Although they correspond to models based on the fundamental niche of species, the presented distribution maps can direct new samplings in areas with a high probability of occurrence for the species.

ACKNOWLEDGMENTS

We are grateful to the students of the Insect and Vector Laboratory- LIVe for their assistance in field work and/or laboratory. We thank CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior) for the scholarship to TMB and ABLA.

REFERENCES

  • ALVES ACF, SANTOS WE, FARIAS RCAP & CREÃO-DUARTE AJ. 2014. Blowflies (Diptera, Calliphoridae) associated with pig carcasses in a Caatinga area, Northeastern Brazil. Neotrop Entomol 43: 122-126.
  • ANDERSON RP, LEW D & PETERSON AT. 2003. Evaluating predictive models of species’ distributions: criteria for selecting optimal models. Ecol Modell 162: 211-232.
  • ANDRADE FM, GODOI VA & ARAVÉQUIA JA. 2023. Why above-averagerainfall occurred in northern northeast Brazil during the 2019 El Niño?. Meteorology 2(3): 307-328.
  • ARASATO LS & AMARAL S. 2013. Geoprocessamento e biodiversidade: contribuições para a modelagem da distribuição de palmeiras Amazônicas. Anais XVI Simpósio Brasileiro de Sensoriamento Remoto, Foz do Iguaçu, PR, Brasil, p. 6767-6774.
  • BARBOSA TM, CARMO RFR, SILVA LP, SALES RG & VASCONCELOS SD. 2017. Diversity of sarcosaprophagous calyptratae (Diptera) on sandy beaches exposed to increasing levels of urbanization in Brazil. Env Entomol 46: 460-469.
  • BARBOSA TM, JALES JT, MEDEIROS JR, VASCONCELOS SD & GAMA RA. 2021. Behavioural aspects of the prey-predator interaction among necrophagous Diptera: implications for cadaveric colonization. Neotrop Entomol 50: 303-311.
  • BARBOSA TM, JALES JT, VASCONCELOS SD & GAMA RA. 2020. Differential ability of necrophagous Diptera to colonize concealed resources: empirical evidence from a field experiment in Brazil. J Forensic Sci 65(5): 1594-1600.
  • CABRINI I, GRELLA MD, ANDRADE CFS & THYSSEN P. 2013. Richness and composition of Calliphoridae in an Atlantic Forest fragment: implication for the use of dipteran species as bioindicators. Biodivers Conserv 22: 2635-2643.
  • CARMO RFR, OLIVEIRA DL, BARBOSA TM, SOARES TF, SOUZA JRB & VASCONCELOS SD. 2017. Visitors versus colonizers: an empirical study on the use of vertebrate carcasses by Necrophagous Diptera in a rainforest fragment. Ann Entomol Soc Am 110: 492-500.
  • CARMO RFR & VASCONCELOS SD. 2016. Assemblage of necrophagous diptera in atlantic insular environments and response to different levels of human presence. Neotrop Entomol 45: 471-481.
  • CARMO RFR, VASCONCELOS SD, BRUNDAGE AL & TOMBERLIN JK. 2018. How do invasive species affect native species? Experimental evidence from a carrion blowfly (Diptera: Calliphoridae) system. Ecol Entomol 43: 483-493.
  • CARVALHO RL ET AL. 2023. Pervasive gaps in Amazonian ecological research. Current Biol 33: 3495-3504.
  • CARVALHO MES, MENDONÇA FA & SANTOS SSC. 2017. Variabilidade climática e a modelagem ecológica da Biomphalaria glabrata: cenários futuros (2050 e 2070) para o hospedeiro intermediário da esquistossomose no Brasil. In: Perez Filho A & Amorim RR (Eds.), Os desafios da Geografia Física na fronteira do conhecimento. Campinas: Instituto de Geociências, UNICAMP, p. 1579-1589.
  • CATTS EP & GOFF ML. 1992. Forensic entomology in criminal investigations. Annu Rev Entomol 37: 253-272.
  • DIAS LS, SANTARÉM VA, ALMEIDA MSR, MEDINA AO & SILVA AV. 2009. Biodiversidade de moscas Calliphoridae no lixão urbano de Presidente Prudente, São Paulo, Brasil. Arq Inst Biol 76: 659-663.
  • DUFEK MI, OSCHEROV EB, DAMBORSKY MP & MULIERI PR. 2019. Calliphoridae (Diptera) in human-transformed and wild habitats: diversity and seasonal fluctuations in the Humid Chaco Ecoregion of South America. J Med Entomol 56: 725-736.
  • FARIA LDB, GODOY WAC & REIS SF. 2004. Larval predation on different instars in blowfly populations. Braz Arch Biol Tech 47: 887-894.
  • FARINHA A, DOURADO CG, CENTEIO N, OLIVEIRA AR, DIAS D & REBELO MT. 2014. Small bait traps as accurate predictors of dipteran early colonizers in forensic studies. J Insect Sci 14: 77.
  • GENNARD D. 2012. Forensic entomology: an introduction, 2nd ed, Wiley-Blackwell.
  • GIANNINI TC, SIQUEIRA MF, ACOSTA AL, BARRETO FCC, SARAIVA AM & ALVES-DOS-SANTOS I. 2012. Desafios atuais da modelagem preditiva de distribuição de espécies. Rodriguésia 63: 733-749.
  • GONÇALVES L, DIAS A, ESPINDOLA CB & ALMEIDA FS. 2011. Inventário de Calliphoridae (Diptera) em manguezal e fragmento de Mata Atlântica na região de Barra de Guaratiba, Rio de Janeiro, Brasil. R Bras Bioci 9: 50-55.
  • GREENBERG B. 1985. Forensic Entomology: Case Studies. Bull Entomol Soc Am 31: 25-28.
  • GRINNELL J. 1917. The niche-relationships of the California thrasher. Auk 34: 427-433.
  • HODECEK J & JAKUBEC P. 2022. Spatio-temporal distribution and habitat preference of necrophagous Calliphoridae based on 160 real cases from Switzerland. Int J Legal Med 136: 923-934.
  • HONORATO NRM, SILVA ANB, NEGREIROS CCA, AGUIAR LMA, MARLIÉRE NP, SOUZA RCM, GUIMARÃES RJPS, GALVÃO LMDC & CÂMARA ACJ. 2021. Triatomine and Trypanosoma cruzi discrete typing units distribution in a semi-arid area of northeastern Brazil. Acta Trop 220: 105950.
  • IBGE - INSTITUTO BRASILEIRO DE GEOGRAFIA E ESTATÍSTICA. 2022. Brasil: Informações ambientais. Available in: https://www.ibge.gov.br/geociencias/cartas-e-mapas/informacoes-ambientais.html
    » https://www.ibge.gov.br/geociencias/cartas-e-mapas/informacoes-ambientais.html
  • INMET – INSTITUTO NACIONAL DE METEOROLOGIA. 2024. El Niño: saiba como foi a atuação do fenômeno no Brasil. Available in: https://portal.inmet.gov.br/noticias/el-ni%C3%B1o-saiba-como-foi-a-atua%C3%A7%C3%A3o-do-fen%C3%B4meno-no-brasil
    » https://portal.inmet.gov.br/noticias/el-ni%C3%B1o-saiba-como-foi-a-atua%C3%A7%C3%A3o-do-fen%C3%B4meno-no-brasil
  • JALES JT, BARBOSA TM, SANTOS LC, RACHETTII VPS & GAMA RA. 2020. Carrion decomposition and assemblage of necrophagous dipterans associated with Terbufos (Organophosphate) intoxicated rat carcasses. Acta Trop 212: 105652.
  • KRISHNA S, CHO M, WEHMANN HN, ENGELS T & LEHMANN FO. 2020. Wing Design in flies: properties and aerodynamic function. Insects 11: 466.
  • LEITE RC, BARBOSA TM, SANTOS-JUNIOR EG, GAMA RA & SOARES TF. 2023. Sarcophagidae (Diptera) do Cerrado Sul Maranhense: expansão na distribuição geográfica de Sarcophaga (Neobelleria) libera Aldrich, 1916. Entomol Commun 5: ec05032-ec05032.
  • MARTÍNEZ-CALDERAS JM, HERNÁNDEZ-SAINTMARTÍN AD, ROSAS-ROSAS OC, PALACIO-NUÑEZ J, VILORDO-GAVÁN JA & OLIVERA-MÉNDEZ A. 2015. Distribución potencial del tigrillo (Leopardus wiedii, Schinz 1821) en el noreste de México, 2nd ed, Therya, p. 241-255.
  • MARTINS LGV, BARBOSA TM & GAMA RA. 2021. Myiasis in humans: case reports in Northeastern Brazil including multispecies co-infestation by Sarcophagidae. Parasitol Int 85: 102436.
  • MEDEIROS JR, TEIXEIRA-JALES J, GAMA RA & BARBOSA TM. 2023. Diversity of sarcosaprophagous dipterans (Insecta: Diptera) associated with street markets in the semiarid of northeastern Brazil. Rev Chil Entomol 49(4): 747-759.
  • MELLO RDS, QUEIROZ MMC & AGUIAR-COELHO VM. 2007. Population fluctuations of calliphorid species (Diptera, Calliphoridae) in the Biological Reserve of Tinguá, State of Rio de Janeiro, Brazil. Iheringia - Ser Zool 97: 481-485.
  • MENEZES BS, MARTINS FR & ARAÚJO FS. 2016. Montagem de comunidades: Conceitos, domínio e estrutura teórica. Oecol Aust 20: 1-17.
  • MOHR RM & TOMBERLIN JK. 2014. Environmental factors affecting early carcass attendance by four species of blow flies (Diptera: Calliphoridae) in Texas. J Med Entomol 51: 702-708.
  • MORETTI TC & THYSSEN PJ. 2006. Miíase primária em coelho doméstico causada por Lucilia eximia (Diptera: Calliphoridae) no Brasil: relato de caso. Arq Bras Med Vet Zootec 58: 28-30.
  • NASCIMENTO RFO, SILVA JOA & CARVALHO-FILHO FS. 2021. Scavengers flesh flies (Diptera, Sarcophagidae) from two phytophysiognomies in the state of Maranhão, Northeastern of Brazil. Biota Neotrop 24(4): e20211192.
  • OLIVEIRA DL & VASCONCELOS SD. 2020. Do native and invasive blow fly (Diptera: Calliphoridae) species differ in their preferential time of flight? Empirical evidence from a seasonally dry tropical forest. J Arid Environ 174: 103985.
  • PAPE T, BLAGODEROV V & MOSTOVSKI MB. 2011. Order Diptera Linnaeus, 1758. In: Zhang ZQ (Ed.), Animal Biodiversity: An outline of higher-level classification and survey of taxonomic richness. Zootaxa 3148: 237.
  • PATITUCCI LD, MULIERI PR, SCHNACK JA & MARILUIS JC. 2011. Species composition and heterogeneity of blowflies’ assemblages (Diptera: Calliphoridae) in urban–rural gradients at regional scale in Argentinean Patagonia. Stud Neotrop Fauna E 46: 49-58.
  • PETERSON AT & VIEGLAIS DA. 2001. Predicting species invasions using ecological niche modeling: new approaches from bioinformatics attack a pressing problem. BioScience 51: 363-371.
  • PHILLIPS SJ, ANDERSON RP & SCHAPIRE RE. 2006. Maximum entropy modeling of species geographic distributions. Ecol Modell 190: 231-259.
  • REBOUÇAS AC. 1997. Água na região Nordeste: desperdício e escassez. Estudos Avançados 11: 127-154.
  • SANTOS MFCR, NASCIMENTO RFO & SILVA JOA. 2024. Moscas varejeiras (Diptera: Calliphoridae) do estado do Maranhão, Brasil, com destaque para as espécies do Parque Estadual do Mirador. Vivências 20: 125-139.
  • SILVA JOA, BRASIL LS & CARVALHO-FILHO FS. 2023a. Flesh flies (Diptera: Sarcophagidae) of forensic importance collected from pig carcasses in the Cerrado of Northeastern Brazil. J Med Entomol 60: 272-281.
  • SILVA JOA, CÂMARA JT, CARVALHO-FILHO FS. 2023b. Muscídeos (Diptera, Muscidae) de importância forense visitantes de carcaças de suínos em áreas de Cerradão no Nordeste do Brasil. Rev Bras Crimin 12: 113-117.
  • SILVA JOA, CARVALHO-FILHO FS, JUEN L & ESPOSITO MC. 2023c. Ecological succession of blow flies (Diptera: Calliphoridae) in the decomposition of pig carcasses in Cerrado areas of Brazil. J Med Entomol 60: 1297-1304.
  • SILVA RC & COUTINHO SFS. 2018. Biomas Nordestinos: um estudo no âmbito da mata atlântica e da caatinga. Anais V CONEDU. Campina Grande: Realize Editora. Available in: <https://editorarealize.com.br/artigo/visualizar/46627>. Acessed in: 30/04/2024.
    » https://editorarealize.com.br/artigo/visualizar/46627
  • SOARES TO, ALMEIDA AA, MORAES AEF, SOUSA MCBC & LEITE TSA. 2019. Impactos ambientais causados pelo desmatamento: uma revisão sistemática da literatura. RESMA 9: 66-73.
  • SOUSA JRP, CARVALHO-FILHO FS, JUEN L & ESPOSITO MC. 2016. Evaluating the effects of different vegetation types on necrophagous fy communities (Diptera: Calliphoridae: Sarcophagidae): implications for conservation. PLoS ONE 11: e0164826.
  • SOUSA JRP, CARVALHO-FILHO FS & ESPOSITO MC. 2015. Distribution and abundance of necrophagous flies (Diptera: Calliphoridae and Sarcophagidae) in Maranhão Northeastern Brazil. J Insect Sci 15: 70.
  • SOUSA JRP, ESPOSITO MC, CARVALHO-FILHO FS & JUEN L. 2014. The potential use of sarcosaprophagous flesh flies and blowflies for the evaluation of the regeneration and conservation of forest clearings: A case study in the amazon forest. J Insect Sci 14: 1-5.
  • SPINDOLA AF, ZHENG L, TOMBERLIN JK, THYSSEN PJ. 2017. Attraction and oviposition of Lucilia eximia (Diptera: Calliphoridae) to resources colonized by the invasive competitor Chrysomya albiceps (Diptera: Calliphoridae). J Med Entomol 54(2): 321-328. DOI: 10.1093/jme/tjw170.
  • STRASSBURG BBN ET AL. 2017. Moment of truth for the Cerrado hotspot. Nat Ecol Evol 1: 1-3.
  • TÔRRES NM & VERCILLO UE. 2012. Como ferramentas de modelagem de distribuição de espécies podem subsidiar ações de governo? Nat Conserv 10: 228-230.
  • VASCONCELOS SD & ARAUJO MCS. 2012. Necrophagous species of Diptera and Coleoptera in Northeastern Brazil: state of the art and challenges for the forensic entomologist. Rev Bras Entomol 56: 7-14.
  • VASCONCELOS SD, BARBOSA TM & OLIVEIRA TPB. 2015. Diversity of forensically-important dipteran species in different environments in Northeastern Brazil, with notes on the attractiveness of animal baits. Fla Entomol 98: 770-775.
  • VASCONCELOS SD, SILVA AM & BARBOSA TM. 2023. Differential colonization of ephemeral resources by sarcosaprophagous Diptera in the Brazilian Caatinga and its implications for forensic entomology in arid environments. J. Arid Environ 214: 1049966.
  • VELOSO HP. 1964. Os grandes clímaces do Brasil: IV - Considerações gerais sobre a vegetação da região nordeste. Mem Inst Oswaldo Cruz 62: 204-223.
  • VOGT WG, WOODBURN TL, MORTON R & ELLEM BA. 1983. The analysis and standardization of trap catches of Lucilia cuprina (Wiedemann) (Diptera: Calliphoridae). Bull Ent Res 73: 609-617.
  • YANG XQ, KUSHWAHA SPS, SARAN S, XU I & ROY PS. 2013. Maxent modeling for predicting the potential distribution of medicinal plant, Justicia adhatoda L. in Lesser Himalayan foothills. Ecol Eng 51: 83-87.
  • WHITWORTH T. 2010. Keys to the genera and species of blow flies (Diptera: Calliphoridae) of the West Indies and description of a new species of Lucilia Robineau-Desvoidy. Zootaxa 2663: 1-35.

APPENDIX

List of consulted references to generate Figure 2 and Table I.

  1. ALMEIDA MAO ET AL. 2008. Ocorrência de ectoparasitos em avestruzes (Struthio camelus) criadas no semi-árido baiano. Rev Bras Parasitol Vet 17(3): 155-157.

  2. ALVES ACF, SANTOS WE, FARIAS RCAP & CREÃO-DUARTE AJ. 2014. Blowflies (Diptera, Calliphoridae) associated with pig carcasses in a Caatinga area, Northeastern Brazil. Neotrop Entomol 43: 122-126.

  3. ANDRADE HTA, VARELA-FREIRE AA, BATISTA MJA & MEDEIROS JF. 2005. Calliphoridae (Diptera) coletados em cadáveres humanos no Rio Grande do Norte. Neotrop Entomol 34: 855-856.

  4. BAIA TC, GAMA RA, SILVA DE LIMA LA & LIMA KMG. 2016. FTIR microspectroscopy coupled with variable selection methods for the identification of flunitrazepam in necrophagous flies. Anal Methods 8: 968-972.

  5. BARBOSA TM, CARMO RFR, SILVA LP, SALES RG & VASCONCELOS SD. 2017. Diversity of Sarcosaprophagous calyptratae (Diptera) on sandy beaches exposed to increasing levels of urbanization in Brazil. Env Entomol 46: 460-469.

  6. BARBOSA TM, JALES JT, MEDEIROS JR, VASCONCELOS SD & GAMA RA. 2021. Behavioural aspects of the prey-predator interaction among necrophagous Diptera: implications for cadaveric colonization. Neotrop Entomol 50: 303-311.

  7. BARBOSA TM, JALES JT, VASCONCELOS SD & GAMA RA. 2020. Differential ability of necrophagous Diptera to colonize concealed resources: Empirical evidence from a field experiment in Brazil. J Forensic Sci 65(5): 1594-1600.

  8. CARMO RFR, BARBOSA TM, TORRIS AF, BEZERRA MS & VASCONCELOS SD. 2021. Diversity of sarcosaprophagous Diptera (Calliphoridae, Sarcophagidae) in organic and conventional mango plantations in the Brazilian semi-arid region. Rev Bras Entomol 65: 2-5.

  9. CARMO RFR & VASCONCELOS SD. 2016. Assemblage of necrophagous diptera in atlantic insular environments and response to different levels of human presence. Neotrop Entomol 45: 471-481.

  10. CARMO RFR, OLIVEIRA DL, BARBOSA TM, SOARES TF, SOUZA JRB & VASCONCELOS SD. 2017. Visitors versus colonizers: an empirical study on the use of vertebrate carcasses by Necrophagous Diptera in a rainforest fragment. Ann Entomol Soc Am 110: 492-500.

  11. CAVALCANTE ANP, DAL BÓ D, CREÃO-DUARTE AJ & FARIAS RCAP. 2015. Espécies de Calliphoridae (Diptera) associadas a carcaças de Sus scrofa Linnaeus, 1758 em área de restinga na Paraíba, Brasil, e espécies de importância forense para a estimativa do Intervalo Pós-Morte (IPM). Entomotropica 30: 150-159.

  12. CRUZ TM, BARBOSA TM, THYSSEN PJ & VASCONCELOS SD. 2021. Diversity of Diptera species associated with pig carcasses in a Brazilian city exposed to high rates of homicide. Pap Avulsos Zool 61: 1-7.

  13. CRUZ JD, SILVA CC & RAPOSO-FILHO JR. 2014. Dipterofauna associada a cadáver de porco doméstico Sus scrofa domesticus (Linnaeus, 1758) na cidade de Itabaianinha, estado de Sergipe. Cad Grad 2: 155-173.

  14. ERNESTO MV, LIBERAL CN, FERREIRA AS, ALVES ACF, ZEPPELINI D, MARTINS CF, PEREIRA-COLAVITE A, CREÃO-DUARTE AJ & VASCONCELLOS A. 2018. Hexapod decomposers of Serra de Santa Catarina, Paraíba, Brazil: an area with high potential for conservation of Caatinga biodiversity. Biota Neotrop 18: 1-13.

  15. FREIRE O. 1923. Fauna cadavérica brasileira. Revista de Medicina 3: 15-40.

  16. GUIMARÃES SEF, MELO DMP, BARBOSA TM, FARIAS RCAP & BICHO CL. 2022. First report of Peckia (Squamatodes) ingens (Walker, 1849) (Diptera: Sarcophagidae) colonizing human corpse in the Neotropical region. Pap Avulsos Zool 62: e202262020.

  17. JALES JT, BARBOSA TM, SANTOS LC, RACHETTII VPS & GAMA RA. 2020. Carrion decomposition and assemblage of necrophagous dipterans associated with Terbufos (Organophosphate) intoxicated rat carcasses. Acta Trop 212: 105652.

  18. MARTINS LGV, BARBOSA TM & GAMA RA. 2021. Myiasis in humans: Case reports in Northeastern Brazil including multispecies co-infestation by Sarcophagidae. Parasitol Int 85: 102436.

  19. MARTINS G, SANTOS WE, CREAO-DUARTE AJ, SILVA LBG & OLIVEIRA AAF. 2013. Estimativa do intervalo pós-morte em um canino (Canis lupus familiaris Linnaeus 1758) pela entomologia forense em Cabedelo-PB, Brasil: relato de caso. Arq Brasil Med Veter Zoot 65: 1107-1110.

  20. MEDEIROS JR, TEIXEIRA-JALES J, GAMA RA & BARBOSA TM. 2023. Diversity of sarcosaprophagous dipterans (Insecta: Diptera) associated with street markets in the semiarid of northeastern Brazil. Rev Chil Entomol 49(4): 747-759.

  21. MEIRA LMR, BARBOSA TM, JALES JT, SANTOS AN & GAMA RA. 2020. Insects associated to crime scenes in the Northeast of Brazil: consolidation of collaboration between entomologists and criminal investigation Institutes. J Med Entomol 20: 1012-1020.

  22. MONTEIRO TT, DA SILVA EM & BRAVO FR. 2014. Levantamento taxonômico e sazonalidade de Calliphoridae, Muscidae e Fanniidae (Insecta: Diptera) em Feira de Santana, Bahia, Brasil. EntomoBrasilis 7: 171-177.

  23. NASCIMENTO EMF, OLIVEIRA JB, PAES MJ, LOBO AP, SILVA ALA, SANTOS JÚNIOR ER, LEAL JLF & MOYA-BORJA GE. 2005. Miíases humanas por Cochliomyia hominivorax (Coquerel, 1858) (Diptera, Calliphoridae) em hospitais públicos na cidade do Recife, Pernambuco, Brasil. Entomol Vectores 12: 37-51.

  24. OLIVEIRA DL, BARBOSA TM, MAIA ACD & VASCONCELOS SD. 2019. Development and field evaluation of a novel, inexpensive passive trap for monitoring dispersal of necrophagous dipteran larvae. J Economic Entomol 112: 2497-2501.

  25. OLIVEIRA TC & VASCONCELOS SD. 2010. Insects (Diptera) associated with cadavers at the Institute of Legal Medicine in Pernambuco, Brazil and its implications for Forensic Entomology. Forensic Sci Int 198: 97-102.

  26. OLIVEIRA DL & VASCONCELOS SD. 2018. Diversity, Daily flight activity and temporal occurrence of necrophagous Diptera associated with decomposing carcasses in a semi-arid environment. Neotrop Entomol 47: 470-477.

  27. OLIVEIRA DL & VASCONCELOS SD. 2020. Do native and invasive blow fly (Diptera: Calliphoridae) species differ in their preferential time of flight? Empirical evidence from a seasonally dry tropical forest. J Arid Environ 174: 103985.

  28. OLIVEIRA DL, SOARES TF & VASCONCELOS SD. 2015. Effect of bait decomposition on the attractiveness to species of Diptera of veterinary and forensic importance in a rainforest fragment in Brazil. Parasit Res 115: 449-455.

  29. PAMPONET F, LOPES D, VÉRAS T, FONSECA P, VASCONCELOS S, TORRES M & OLIVEIRA-COSTA J. 2019. Análise temporal de Calliphoridae (Diptera: Cyclorrhapha) no processo de decomposição em carcaças de suínos (Sus scrofa Linnaeus) em Salvador, Bahia, Brasil. EntomoBrasilis 12: 63-69.

  30. SANTOS MFCR, NASCIMENTO RFO & SILVA JOA. 2024. Moscas varejeiras (Diptera: Calliphoridae) do estado do Maranhão, Brasil, com destaque para as espécies do Parque Estadual do Mirador. Vivências 20: 125-139.

  31. SILVA AV. 2024. Avaliação da distribuição de espécies nativas e exóticas de potencial forense da família Calliphoridae (Diptera) em um fragmento de Mata Atlântica no estado de Pernambuco. Trabalho de Conclusão de Curso Ciências Biológicas Bacharelado - Universidade Federal de Pernambuco, Recife.

  32. SILVA JOA, CARVALHO-FILHO FS, JUEN L & ESPOSITO MC. 2023. Ecological succession of blow flies (Diptera: Calliphoridae) in the decomposition of pig carcasses in Cerrado areas of Brazil. J Med Entomol 60: 1297-1304.

  33. SOARES TF & VASCONCELOS SD. 2016. Diurnal and nocturnal flight Activity of blow flies (Diptera: Calliphoridae) in a rainforest fragment in Brazil: implications for the colonization of homicide victims. J Forensic Sci 61: 1571-1577.

  34. SOUSA JRP, CARVALHO-FILHO FS & ESPOSITO MC. 2015. Distribution and abundance of necrophagous flies (Diptera: Calliphoridae and Sarcophagidae) in Maranhão Northeastern Brazil. J Insect Sci 15: 70.

  35. SOUSA JRP, CARVALHO-FILHO FS, JUEN L & ESPOSITO MC. 2016. Evaluating the effects of different vegetation types on necrophagous fy communities (Diptera: Calliphoridae; Sarcophagidae): implications for conservation. PLoS ONE 11: e0164826.

  36. SOUSA LL & COSTA PW. 2019. Abundância e flutuação populacional do gênero Chrysomya (Robineau-Desvoidy, 1830) (Díptera: Calliphoridae) durante as fases de decomposição da carcaça de Sus scrofa (Linnaeus, 1758) na região Nordeste do Brasil. Rev Brasil Zoociências 20: 1-11.

  37. SOUSA JRP, MENDES TP, CARVALHO-FILHO FS, JUEN L & ESPOSITO MC. 2021. Diversity of necrophagous flies (Diptera: Calliphoridae, Mesembrinellidae, and Sarcophagidae) in anthropogenic and preserved environments of five different phytophysiognomies in Northeastern Brazil. Neotrop Entomol 50: 537-550.

  38. VASCONCELOS SD, BARBOSA TM & OLIVEIRA TPB. 2015. Diversity of forensically-important dipteran species in different environments in Northeastern Brazil, with notes on the attractiveness of animal baits. Fla Entomol 98: 770-775.

  39. VASCONCELOS SD, COSTA DL & OLIVEIRA DL. 2019. Entomological evidence in a case of a suicide victim by hanging: first collaboration between entomologists and forensic police in north-eastern Brazil. Australian J Forensic Sci 51: 231-239.

  40. VASCONCELOS SD, CRUZ TM, SALGADO RL & THYSSEN PJ. 2013. Dipterans associated with a decomposing animal carcass in a rainforest fragment in Brazil: notes on the early arrival and colonization by necrophagous species. J Insect Sci 13: 1-11.

  41. VASCONCELOS SD & SALGADO RL. 2014. First record of six Calliphoridae (Diptera) species in a seasonally dry tropical forest in Brazil: evidence for the establishment of invasive species. Fla Entomol 97: 814-816.

  42. VASCONCELOS SD, SALGADO RL, BARBOSA TM & SOUZA JRB. Diptera of medico-legal importance associated with pig carrion in a Tropical Dry Forest. J Medical Entomol 53: 1131-1139.

  43. VASCONCELOS SD, SILVA AM & BARBOSA TM. 2023. Differential colonization of ephemeral resources by sarcosaprophagous Diptera in the Brazilian Caatinga and its implications for forensic entomology in arid environments. J. Arid Environ 214: 1049966.

  44. VASCONCELOS SD, SOARES TF & COSTA DL. 2014. Multiple colonization of a cadaver by insects in an indoor environment: first record of Fannia trimaculata (Diptera: Fanniidae) and Peckia (Peckia) chrysostoma (Sarcophagidae) as colonizers of a human corpse. Int J Legal Med 128: 229-233.

Publication Dates

  • Publication in this collection
    07 Feb 2025
  • Date of issue
    2025

History

  • Received
    27 May 2024
  • Accepted
    13 Nov 2024
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