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First record of the blow fly Chrysomya megacephala (Diptera: Calliphoridae) on a southern Atlantic island: implications for disease transmission in a protected environment

2014; Wiley; Volume: 39; Issue: 1 Linguagem: Inglês

10.1111/j.1948-7134.2014.12093.x

1948-7134

Rodrigo Felipe Rodrigues do Carmo, Simão Dias Vasconcelos,

Climate Change and Health Impacts

Flies from the family Calliphoridae comprise a cosmopolitan group of approximately 1,500 species, many of which are reported as colonizers of human and animal corpses (Carvalho and Mello-Patiu 2008). Some species, such as those from the genus Chrysomya Robineau-Desvoidy, 1830, have medical relevance as vectors of pathogens, including bacteria, protozoans, and helminthes, and as causal agents of myiasis (Greenberg 1973). A study performed in Ethiopia showed that Chrysomya rufifacies acted as a vector of at least five helminthes parasites, including Ascaris lumbricoides, and four species of protozoan parasites: Entamoeba histolytica/dispar, Entamoeba coli, Giardia lamblia, and Cryptosporidium sp. (Getachew et al. 2007). Three Chrysomya species, C. albiceps (Wiedemann 1819), C. megacephala (Fabricius 1874), and C. putoria (Wiedemann 1818), originally restricted to the Old World, were accidentally introduced in the Neotropical region in the late 1970s. Since their first detection in southern Brazil, Chrysomya species, including a fourth species, C. rufifacies, have been reported in several countries in the Americas (Mariluis and Mulieri 2003, Montoya et al. 2009, Kosmann et al. 2013). A recent review on necrophagous Diptera in northeastern Brazil indicates that Chrysomya species have spread along diverse ecosystems with varying degrees of anthropogenic impact (Vasconcelos and Araujo 2012). The current understanding of the dispersion of Chrysomya species in South America, however, is limited to mainland areas of Argentina, Brazil, Colombia, and Peru (Mariluis and Mulieri 2003, Montoya et al. 2009, Kosmann et al. 2013, Vasconcelos and Araujo 2012). So far, there are few records on the arrival and establishment of these species in insular environments despite their medical importance. As part of a study on insect ecology in the archipelago of Fernando de Noronha, a conservation site located on the coast of Brazil, we aimed to detect the presence of non-exotic, medically important Calliphoridae species. We report here the first evidence of the establishment of a non-native Chrysomya species on islands in the southern Atlantic Ocean and discuss the implications of this finding to local disease transmission. The archipelago of Fernando de Noronha (3°52’S; 32º26’W, total area 18.4 km2), is located 545 km northeast of the Brazilian mainland. It is composed of 21 islands and islets, of which the only inhabited one, also called Fernando de Noronha, has a population of 2,630 and total area of 16.9 km2 (Brasil 2012). The archipelago is legally protected and human activities are limited or prohibited in a great portion of its territory (Freitas and Vasconcelos 2008). The climate is tropical, mean temperatures range from 23.5° C to 31.5°C, with an annual mean of 27.0° C, relative humidity is high with an annual average of 78%, and rainfall of approximately 1,420 mm/year. Native flora are mostly represented by seasonal deciduous vegetation, with several introduced plant species. Overall, the island suffers from a persistent shortage of water, as there are no permanent freshwater reservoirs (Freitas and Vasconcelos 2008). To draw inferences regarding the relationship between the diversity of blow flies and anthropogenic activities, sampling was performed in June, 2012 in six sites to represent different levels of exposure to human activities. The sites under Low Anthropogenic Impact (LAI) included Ponta da Sapata (PS) located at the extreme west of the island, a small peninsula restricted to scientific and management activities partially covered with native vegetation and is part of the Marine National Park, and Praia de Atalaia (PA), a restricted beach located at the northeastern area of the island, open to controlled tourist visits two h per day and also part of the National Marine Park. The sites under Moderate Anthropogenic Impact (MAI) were Mangue do Sueste (MS), a mangrove area located in the southern portion of the island with limited human presence and it is an area used for egg-laying by marine turtles, Baía dos Golfinhos (BG), a bay situated in the northwest of the island, with predominantly shrubby vegetation that belongs to the Marine National Park but is open to small groups of tourists during the day. Two sites were classified as under High Anthropogenic Impact (HAI), Urban Area (UA): the village where approximately 70% of the population of the island lives, and that has litter in several areas, and Praia do Cachorro (PC), a beach near the inhabited part of the island with unlimited access and only a few bars and small amounts of litter present. Insects were collected using a suspended trap containing chicken liver or sardine (ca. 200 g, after 24 h at room temperature) as bait (Oliveira and Vasconcelos 2010). In each environment, a grid of six traps, three containing chicken liver and three containing sardine, was placed with 20 m between the traps. A total of 108 independent traps were used throughout the study. Each trap was exposed for 48 h in each environment. Adult flies collected from traps were placed in 70% alcohol until identification using the taxonomic keys of Carvalho and Mello-Patiu (2008), Carvalho and Ribeiro (2000), and Kosmann et al. (2013). Species from the Calliphoridae assemblage were classified as constant when present in >50% of the samples, accessory when collected in 25% to 50% of the samples and accidental when present in <25% of the samples. Dominance was calculated using Simpson's index (Primer® 6.0), which takes into account not only species richness and abundance but also the proportion of the occurrence of each species. The abundances of the codominant species were compared by analysis of variance (ANOVA), and a Chi-square test was used to compare the abundance of C. megacephala in the three types of environment. A significance level of 5% was used in all analyses. A total of 41,683 adult dipterans belonging to four species of Calliphoridae were registered from the samples across all sites. Two species are reported for the first time for the archipelago (Table 1). Chrysomya megacephala was the most abundant species (58.0% of all insects), followed by Cochliomyia macellaria. The combined abundance of the two species reached 98%, showing a marked dominance over the remaining calliphorids (Figure 1). All species were collected in all sampling sites, irrespective of the degree of preservation. Simpson's diversity indices were low and did not differ markedly in the three types of environments (SLAI = 0.506; SMAI = 0.498; SHAI = 0.473). C. megacephala and Co. macellaria were classified as codominant species (Table 1) and no significant differences were observed in their dominance across the three types of environment (F(2;3) = 2.90; P = 0.19). Regarding constancy, Lucilia eximia and Lucilia sp. were categorized as accessory species, while C. megacephala and Co. macellaria were classified as constant. Relative frequencies of C. megacephala across the sites varied little; when the abundances of C. megacephala in each type of environment were compared, a significantly higher abundance was reported in areas under moderate anthropogenic impact (χ2 =1,915; P < 0.0001, d.f. = 2), a pattern that was similar for the remaining species. The only reference to Calliphoridae in the island was based on samples taken in the early 1970s, when only C macellaria and L. eximia were reported (Couri et al. 2008). The fact that C. megacephala has become a dominant species less than 40 years after the first survey supports the conclusion that this species has potential to achieve stronger medical importance in a near future. In that sense, Wells (1991) alerts for the invasive potential of the species and highlights the need for the development of integrated control measures. The Oriental latrine fly Chrysomya megacephala is a medically and forensically important blow fly species that has been demonstrated to occupy a wide variety of habitats since its introduction in the American continent, ranging from the Amazon forest to semi-arid regions, including the rainforest, agroecosystems, coastal environments, and urban areas (Montoya et al. 2009, Vasconcelos and Araujo 2012). Its dominance in areas exposed to diverse levels of human impact suggests that the species is expanding its geographical distribution, which may have direct effects on the dispersal of pathogens and parasites. For example, Monzon et al. (1991) compared the role of Musca domestica and C. megacephala as vectors in an area exposed to anthropogenic impact in Manila and concluded that the latter was associated with a significantly higher frequency of helminthes eggs. Fernando de Noronha suffers from increasing tourism and cargo, which increases the production of domestic litter far above the capacity of the local composting plant to process. The poor sanitary conditions, including the lack of a sewage system, favors the establishment of C. megacephala. Since their larvae can feed on decomposing organic matter, an additional negative effect is the proliferation of pathogens on litter, several of which can be mechanically transmitted to humans (Greenberg 1973). For example, in fresh food markets in Thailand, C. megacephala was shown to exhibit high levels of contamination by bacteria, at even higher frequencies than Musca domestica (Sukontason et al. 2007), with all the medical risks associated. The legal protection does not seem to cover subtle threats to human and animal health, as the constant flux of tourists, cargo, and supplies to-from the continent may promote passive transport of medically important species, such as mosquitoes and blow flies. From 2001 to 2011, 501 cases of dengue were identified by the local authorities, which is outstanding given the small population (Brasil 2012). To reinforce that, a medically important, non-native, scorpion species, Tityus stigmurus, was also recorded recently which poses questions about the fragility of the quarantine system (Freitas and Vasconcelos 2008). The medical relevance of C. megacephala is increasingly associated with its forensic importance, as the species was shown to be frequent in cadaver colonization (Kumara et al. 2012, Vasconcelos et al. 2014). Lastly, the concept that C. megacephala is highly synanthropic needs to be regarded with caution. None of the areas in the island can be classified as strongly “urban” and no significant differences in the frequency of occurrence of C. megacephala were observed between preserved and human occupied areas. The dominance of C. megacephala in all types of environments in Fernando de Noronha underlines the need for rigorous inspection of cargo and human visitors to the island and the development of monitoring strategies. We thank the following people and/or institutions: Fundação de Amparo à Ciência e Tecnologia do Estado de Pernambuco (Facepe) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for financial support; the staff from the Instituto Chico Mendes de Conservação da Biodiversidade for legal authorization, the Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis and the Government of Pernambuco State for logistical help, and Dr. Trevor Williams (Inecol, Mexico) for critical reading of the manuscript. The corresponding author has a productivity grant from CNPq.