Synanthropy of Sarcophagidae (Diptera) in La Pintada, Antioquia-Colombia

Sinantropía de Sarcophagidae (Diptera) en La Pintada, Antioquia- Colombia
Daniela Yepes-Gaurisas¹*, Juan David Sánchez-Rodríguez¹, Cátia Antunes de Mello-Patiu²*  & Marta Wolff Echeverri¹

*^{Dirección para correspondencia:}
Abstract

Recently, populations of flies have increased in numbers given the elevated levels of organic matter waste produced by anthropic activities and domestication of animals. Such increase represents a worldwide health concern, since flies can be vectors of human diseases. The great variety of feeding and  developmental habits of flies of the family Sarcophagidae taking place on animal corpses, feces and decomposed organic matter make them potential vectors of pathogens. Herein, we evaluated the synanthropic index (SI), as well as other ecological aspects of this family, through simultaneous monthly samplings in three areas with  different degrees of human disturbance (urban, rural and forest). Each area had four  van Someren Rydon traps, each one with a different bait (i.e., human feces, chicken viscera, fish and decomposing onion). Traps were active during 48 hours each month, and specimen collection was made every 12 hours. A total of 7 446 Sarcophagidae individuals were collected (1 275 males and 6 171 females), belonging to 27 species and nine genera. Tricharaea (Sarcophagula) canuta (SI=+96.67), Oxysarcodexia taitensis (SI=+93.85), Peckia (Peckia) chrysostoma (SI=+90.00) and Tricharaea (Sarcophagula)  occidua (SI=+88.76) exhibited the highest values of synanthropy index, revealing a  strong preference for human settlements. The most abundant species were Oxysarcodexia conclausa (21.80%), Ravinia effrenata (18.67%), Oxysarcodexia bakeri (11.45%) and Oxysarcodexia taitensis (10.20%), all of which exhibited preference for urban environments. Additionally, we are reporting seven new records of Sarcophagid flies for Colombia: Oxysarcodexia angrensis, Oxysarcodexia bakeri, Oxysarcodexia diana, Oxysarcodexia similata, Oxysarcodexia timida, Peckia (Peckia) pexata and Titanogrypa (Cucullomyia) placida.

Key words: Flesh flies, synanthropic index, ecology, tropical dry forest, biodiversity, life history.

Resumen

La  población de moscas se ha visto  incrementada recientemente por la proliferación de residuos de materia orgánica  proveniente de la actividad antrópica, así  como por la domesticación de animales. Este aumento constituye una gran alerta de salud a nivel mundial, ya que algunas moscas  son  vectores de enfermedades al humano. Los Sarcophagidae cuentan con una gran  variedad de hábitos de alimentación y  desarrollo, los cuales tienen lugar en cadáveres de animales, excrementos y materia orgánica en descomposición; haciéndolos posibles vectores de patógenos. En este estudio se evaluó el índice de sinantropía, al igual que otros aspectos ecológicos de esta familia median- te muestreos mensuales simultáneos en tres zonas (urbana, rural y bosque), usando trampas van Someren Rydon ceba- das con excremento humano, vísceras  de pollo, pescado y cebolla en descomposición. En cada zona se instalaron cuatro trampas (una por atrayente), durante 48 horas cada mes, realizando recolectas cada 12 horas. Se recolectaron 7 446 individuos de Sarcophagidae (1 275 machos y 6 171 hembras),  de  27  especies  y  nueve  géneros.  Tricharaea (Sarcophagula)  canuta (+96.67), Oxysarcodexia taitensis (+93.85), Peckia (Peckia) chrysostoma  (+90.00)  y  Tricharaea (Sarcophagula) occidua (+88.76) presentaron los índices de sinantropía más altos del estudio, lo que refleja una  fuerte  preferencia  por  asentamientos  humanos.  Las especies más abundantes fueron: Oxysarcodexia conclausa (21.80%), Ravinia effrenata (18.67%),   Oxysarcodexia bakeri  (11.45%)  y   Oxysarcodexia  taitensis  (10.20%), todas  exhibiendo preferencia por ambientes  urbanizados. Se reportan siete nuevos registros para Colombia: Oxysarcodexia angrensis,  Oxysarcodexia bakeri, Oxysarcodexia diana, Oxysarcodexia similata, Oxysarcodexia timida, Peckia (Peckia) pexata y Titanogrypa (Cucullomyia) placida.

Palabras clave: índice de sinantropía, Sarcofágidos, ecología, bosque seco tropical, biodiversidad, historia de vida.

The Sarcophagidae Hagen, 1881, are a family of Calyptratae flies present in all geo- graphic regions of the world, from which nearly 2 600 species have been described. They are distributed in three subfamilies: Miltogramminae, Paramacronychiinae and Sarcophaginae (Pape 1996). Sarcophagidae show the highest richness in the Neotropical region and it is strongly dominated by Sarcophaginae, with few members of the other subfamilies (Pape & Dahlem 2010). In Colombia, there are 78 species reported: six Miltogramminae and 72 Sarcophaginae, the latter grouped in 24 genera, with some of the most notorious being: Oxysarcodexia Townsend, 1917, Peckia Robineau-Desvoidy, 1830,RaviniaRobineau-Desvoidy, 1863 and LepidodexiaBrauer & Bergenstamm, 1891 (Papeet al. 2004).

Sarcophaginae have a wide variety of habits, some species being scavengers, coprophages, hosts of ant and termite nests, some cause myasis to amphibians and mammals, others are predators on arachnid eggs, butterfly larvae and bee pupae. They can even be highly specialized parasitoids in other arthropods (Papeet al. 2004). This variety of habits is what allows several species to be associated with human environments and domestic animals, becoming a great threat to public health, due to their capacity to become vectors of pathogenic organisms such as protozoa, helminthes, bacteria and virus (Greenberg 1973).

The transformation of natural environments into urban and rural areas, radically changes local fauna and flora, however, some species of flies can adapt to these new conditions; this association is called synanthropy and can be calculated for different ecological regions according to the formula proposed by Nuorteva (Ferreira 1979, Linhares 1981, Diaset al. 1984, D’Almeida 1984, Ferreira & Lacerda 1993, Gomes & Von Zuben 2005, Montoyaet al. 2009, Uribe et al. 2010), who considers synanthropy as “the capacity of some animals to make use of favorable conditions created by men” (Nuorteva 1963).

Calculation of synanthropy index (SI) is based on the comparison of flies species collected in urban, rural and forest areas. This index ranges from -100 and +100; positive values show a preference for areas with human settlements and negative values show intolerance to ecological changes resulting from urbanization. The degree and nature in which synanthropy occurs is different depending on the species, the geographical and weather conditions of the place, and the characteristics of the human groups that modify the habitat in a determined way, with their culture, traditions and habits (Nuorteva 1963). Furthermore, the environmental impact caused by a poor management of residuals, increases densities of synanthropic flies populations, and in consequence, the potential of disease transmissions (Paraluppi & Castellón 1994, Lomônaco & Almeida 1995, Ferreira & Barbola 1998).

Sarcophagidae are an important component of synanthropic fauna in South America, however, there are few works done under this perspective, which have been developed mainly in some regions of Brazil as Curitiba (Ferreira 1979), Campinas (Linhares 1981), Belo Horizonte (Diaset al. 1984), Rio de Janeiro (D’Almeida 1984) and Goiânia (Ferreira & Lacerda 1993). In Colombia, there are only two studies on synanthropy, one for the family Calliphoridae (Montoyaet al. 2009) and another for Muscidae (Uribeet al. 2010) with none on Sarcophagidae associated to anthropic environments. This way, the present work is a contribution to the ecology, natural history and general knowledge of the Sarcophagidae.

Materials and Methods

Study site:La Pintada is located in the Southwest of the department of Antioquia, Colombia, at 5º44’ N - 75º36’ W at an aver- age altitude of 600masl. Annual average temperature is 27°C, relative humidity is 76% and average annual precipitation is 1 000mm, the latter having a bimodal distribution characterized by two wet periods (April-May and September-November) and two with less precipitation (December-March and June-August). The municipality has an area of 55km²with a population of 10 450 inhabitants and an urban area of 6.5km²(Velásquezet  al. 2006). All sampling areas belong to Tropical Dry Forest (T-df) (Holdridge 1967).

Sampling:The study was simultaneously done in three areas with different ecological characteristics: 1. Urban area: located in the village (5º44’48” N - 75º36’34” W) at an altitude of 610masl. There are drinkable water, sewer- age system and periodical waste collection. 2. Rural area: grasslands located 5km away from the urban area (5º43’25” N - 75º37’26” W) at an altitude of 770masl. Drinkable water is collected from a spring, it also has a septic tank and waste is burned. The site provides ecotourism services with approximately 150 visitors each month and holds four permanent residents, beef cattle and horses. 3. Forest area: it is characterized by low human intervention, located in Farallón de la Paz (5º43’24” N - 75º37’15” W) 5.5km away from the urban area and at an altitude of 850masl.

Four van Someren Rydon traps (Villarealet al. 2004) were installed in each area, placed one meter high from the ground and separated from each other by a distance of 50m. Each trap was baited with about 150g of a bait type: human faeces, fish, chicken viscera or rotting onion. The traps were left for 48 hours each month, and obtained material was collected in Falcon vials containing 70% ethanol every 12 hours (06:00 and 18:00h). Samples were taken every month for a total period of six months, from February to July 2007. The total sampling effort in each area was 1 152 hours. Precipitation data were provided by the Colombian Meteorogical Institute (Instituto de Hidrología, Meteorología y Estudios Ambientales de Colombia-IDEAM).

Preservation and identification:Only the males were identified, since there are not descriptions and keys for the females; nonetheless these were considered for some analyses. Males were set in entomological pins with their external genitalia exposed, in order to observe the structures that allow species identification. They were identified following the keys of Carvalho & Mello-Patiu (2008), Buenaventuraet al. (2009) and Pape & Dahlem (2010), the cata- logue by Pape (1996), some descriptions and redescriptions (e.g. Lopes 1946, 1962, 1975, Leite & Lopes 1989, Lopes & Leite 1991, Lopes & Tibana 1991, Guimarães 2004, Girouxet al. 2010) and through the revision of the Sarcophagidae reference collection deposited in the Entomological Collection of University of Antioquia (Colección de Entomología de la Universidad de Antioquia - CEUA), identified by Thomas Pape and Cátia Antunes de Mello- Patiu, specialists on this family. The nomenclature adopted was from Pape (1996). All material was deposited in the Entomological Collection of University of Antioquia (CEUA, Collection National Register No.036).

The SI was calculated according to the formula by Nuorteva (1963), SI=(2a+b-2c)/2, where a. is the percentage of individuals of a given species collected in the urban area, b. is the percentage of the same species collected in the rural area, and c. the percentage of the same collected in the forest. For this analysis, only species with a number equal or higher to 15 individuals were considered.

Results

A total of 7 446 individuals were collected (1 275 males and 6 171 females). Males were 17.1% of the sample, distributed in nine genera and 27 species.OxysarcodexiaandPeckia were the most diverse genera with 11 and six species respectively,Ravinia and Tricharaea with two species, and Argoravinia,Helicobia, Sarcodexia, Sarcofahrtiopsis and Titanogrypa were represented by only one species (Fig. 1). The complete results for all species are in the^appendixsection.

From all the species found, only Peckia (Squamatodes) ingens (Walker, 1849) were reported for Antioquia; the remaining species are new records for this department, and seven of them were also new records for Colombia:Oxysarcodexia angrensis(Lopes, 1933),O. bakeri(Aldrich, 1916),O. diana (Lopes, 1933),O. similata (Lopes & Tibana, 1987), O. timida(Aldrich, 1916),P. (Peckia) pexata(Wulp, 1895) andTitanogrypa (Cucullomyia) placida(Aldrich, 1925), which totalizes 85 species for the country (Fig. 1).

Oxysarcodexia conclausa (Walker, 1861),Ravinia effrenata (Walker, 1861),O. bakeriandOxysarcodexia  taitensis (Schiner, 1868) were the most abundant species respectively, representing 62.07% of the total number of males collected (Fig. 1). These species were scarcely found in the forest area. Consequently, the urban and rural areas had the highest proportions of individuals: 71.69% and 23.22% respectively (including all the species found) (Fig. 2, ³ 3 Fig.  3 ).

Titanogrypa placida, Oxysarcodexia cyaniforceps (Hall, 1933), O. diana, Peckia pexata and Sarcofahrtiopsis cuneata(Townsend, 1935) were the most scarce species with only two individuals forT. placida and one individual for each of the remaining species; however, three of these species were new records for Colombia (^Appendix).

Most of the collected individuals were found in May, which coincides with the wettest month; on the other hand, the least number of sarcophagid flies were collected during February when the precipitation was very low. Therefore the monthly species abundance was possibly related to rainfall (Figs. 2, ⁴ 4 ).

Chicken viscera was the most effective bait in all three areas (41.82%), followed by fish (39.86%), human faeces (16.47%) and onion (1.85%) (Fig.  3). However, a difference was found between the preference of males and females for the baits, being chicken viscera the most effective to capture males (33.80%) (Fig. 5), and fish and viscera had a very similar effect in females (41.11% and 39.88% respectively).

The species with the highest synanthropic indices wereTricharaea (Sarcophagula) canuta(Wulp, 1896) andOxysarcodexia taitensiswith 96.67 and 93.85 respectively, showing a very strong preference for human settlements. In contrast,Oxysarcodexia angrensis and Peckia (Pattonella) intermutans(Walker, 1861) with -42.31 and -100.00 respectively, were not found in urban areas andP. intermutans was found exclusively in the forest area, showing a complete avoidance for human settlements. The remaining species showed different degrees of association with human settlements, most of them preferring habited areas (Table 1and^Appendix).

Discussion

With this study we have reported seven new records for Colombia, many of them previously recorded for other countries in the Neotropical and Neartic regions (Lopes 1975, Lopes & Tibana 1991, Pape 1996, Oliveiraet al. 2002, Papeet al. 2004). These results allow us to resume a total of 85 species of this family for Colombia.

The most abundant genus in this study wasOxysarcodexia, represented mainly byO. conclausa, which was observed through- out the study showing a preference for human settlements and exhibited a strong necrophagous behavior.

Tricharaea canutawas the most eusy- nanthropic species with a strong preference for dense human settlements, it was main- ly attracted by human faeces, for which it could be considered as a potential vector of pathogens to humans.

Peckia (Peckia) chrysostoma(Wiedemann, 1830), Tricharaea (Sarcophagula) occidua(Fabricius, 1794),O. bakeri and O. timidashowed a strong preference for human settlements, having high synanthropic indexes (from 90 to 65).Tricharaea occiduawas collected in chicken viscera, fish and human faeces in similar proportions, and therefore it could be considered a potential vector of human diseases, it has also been registered in previous studies as one of the most abundant species in corpses (Barroset al. 2008). Peckia chrysostomawas mainly found in the urban area and being absent in forests; this coincides with observations in Rio de Janeiro, where it was commonly found inside houses, SI=60.97 (D’Almeida 1984), while in Belo Horizonte it was more common in uninhabited areas, SI=-32.4 (Diaset al. 1984) and inCampinas it showed independence of human settlements, SI=13.90 (Linhares 1981). This species revealed a necrophagous behavior, also evidenced in Rio de Janeiro and Campinas, in a similar way (Linhares 1981, D’Almeida 1984). It has been collected in decomposing fish (Leandroet al. 2005), pig corpses (Barroset al.2008, Barbosaet al. 2009) and human corpses (Oliveira-Costaet al. 2001) in Brazil, where is of great forensic importance.

Oxysarcodexia similata, Sarcodexia lambens (Wiedemann, 1830) and P. ingensrevealed a preference for human settlements, being present in all three sampling areas, with a similar abundance in urban and rural areas.Sarcodexia lambensshowed a strong attraction for fish and chicken viscera, in accordance to other studies where this species has been found in a large proportion in corpses (Barroset al. 2008). However, it is an opportunistic species and it has been attracted by a variety of substrata, such as pig and human corpses (Oliveira-Costaet al. 2001, Barros et al. 2008, Barbosaet al. 2009), and even causing myasis in humans (Queiroz de Leãoet al. 1996, Fernandes et al. 2009) and frogs (Hagmanet al. 2005).

Linhares (1981) reportedHelicobia morionella(Aldrich, 1930) attracted by chicken viscera, mouse corpses and human faeces, showed the highest abundance in the latter; it also resulted in a synanthropic index that reveals a complete rejection for human settlements. These results contrast with those found in this study, since the few individuals collected of this species were caught in the urban area being attracted by fish and chicken viscera, with no individuals in human faeces.

Peckia pexata and P. (Euboettcheria) anguilla(Curran & Walley, 1934) were considered an asynanthropic species by Diaset al(1984), differing from the herein presented results, sinceP. anguillashowed its highest abundance in the rural area, also being present in the urban and forest areas. However, both species exhibit necrophagous habits and have been previously associated to corpses’ decomposition (Barroset al. 2008). Peckia pexatais represented in this study by only one individual collected in the rural area, for this reason, nothing could yet be concluded. In Brazil, this species has been recorded as one of the most abundant in corpses in the Cerrado biome being present in several phases of decomposition, and therefore, having forensic importance (Barroset al. 2008).

Oxysarcodexia avunculashowed dominance in the forest of Belo Horizonte (Diaset al. 1984), while in the present study it was found in the rural area and the forest in equal proportions, being collected in fish and chicken viscera. This species has been attracted by corpses in Brazil (Barroset  al. 2008), and in this study 75.0% of its individuals were attracted by fish and the other 25.0% by chicken viscera.

The species that showed preference for uninhabited areas wereOxysarcodexia sarcinata(Lopes, 1953) andPeckia (Euboettcheria) collusor (Curran & Walley, 1934). The latter showed complete rejection for human settle- ments in Campinas, SI=-71.10 (Linhares 1981), Belo Horizonte, SI=-93.00 (Diaset al. 1984) and Rio de Janeiro, SI=-80.99 (D’Almeida 1984), with most individuals collected in the forest, it was classified as an asynanthropic species. In La Pintada, it showed a necrophagous behavior being attracted in a larger proportion by fish and chicken viscera, what coincides with the other studies (D’Almeida 1984, Barroset al. 2008, D’Almeida & Lima 1994), while in Campinas it has been also reported in human faeces (Linhares 1981).

Oxysarcodexia angrensiswas collected in all baits, being fish the most successful. This species exhibited a very low synanthropic index (-42.31) indicating a complete rejection for human settlements, which is in accordance to observations in Campinas where it was present in chicken viscera, mouse carcass and human faeces, SI=-58.90 (Linhares 1981).

Peckia intermutanspresented the lowest synanthropic index (-100.00), since this spe- cies was recorded only in the forest, showing a complete rejection for urbanized areas, which make it an asynanthropic species. This result is similar to the behavior found in Campinas, SI=-94.30 (Linhares 1981) and Rio de Janeiro, SI=-60.1 (D’Almeida 1984); but it significantly differs from the results of Belo Horizonte, SI=4.2 (Diaset al. 1984) where P. intermutansshowed independence from inhabited areas and was found in the three areas, with a lower proportion in the urban area. This species showed a necrophagous behavior, also exhibited in other studies (Linhares 1981, D’Almeida 1984, D’Almeida & Lima 1994), for this reason several taxonomists have remarked its importance in forensic entomology (Carvalhoet al. 2000, Oliveiraet al. 2002, Barroset al. 2008).

The great abundance of females in each environment can be explained by the need of appropriate substrata for laying larvae, being necrophagy the most abundant habit, while onion did not have a significant importance as bait. A deeper knowledge on the ecology of Sarcophagidae will help to better understand the dynamics of its species and their effect on the ecosystem, which in turn opens the possibility to use the asynanthropic species as indicators of healthy environments, and even synanthropic species could be implemented in the forensic entomology field in Colombia.

Acknowledgments

We want to thank to the family compensation fund Comfenalco-Antoquia for founding this project. To the Laboratorio de Colecciones Entomológicas de la Universidad de Antioquia (CEUA) and the Grupo de Entomología de la Univesidad de Antioquia (GEUA) for their great help during the field sampling. Finally we want to thank Elena Ricaurte Yepes for her kindly and invaluable help in translating this manuscript and to Juliana Cardona-D for her valuable comments.

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