Medical and Veterinary Entomology (2014) 28, 228–231
doi: 10.1111/mve.12043
SHORT COMMUNICATION
Seasonal abundance of livestock-associated Culicoides species in northeastern Brazil L. P. C. C A R V A L H O and F. S. S I L V A Laboratory of Medical Entomology, Center for Agrarian and Environmental Sciences, Federal University of Maranh˜ao, Chapadinha, Maranh˜ao, Brazil
Abstract. Culicoides biting midges (Diptera: Ceratopogonidae) are of great medical and veterinary importance because the haematophagous females of some species can transmit diseases to humans and animals. In order to determine the presence and seasonal abundance of the bluetongue virus (BTV) vector Culicoides insignis Lutz at domestic animal sheds in northeastern Brazil, insects were collected once a month between January and December 2010. Light traps were set from 18.00 to 06.00 hours at a pigsty, chicken coop and bovine corral. Culicoides insignis accounted for 81% of the 22 316 specimens collected. Other well-represented species were: Culicoides paucienfuscatus Barbosa (3246 individuals), Culicoides diabolicus Hoffman (308), Culicoides leopoldoi Ortiz (224) and Culicoides duartei Tavares and Luna Dias (221). The remainder accounted for 4% of the total sample. Culicoides insignis occurred mostly at the cattle corral, 98.2% in the rainy season. This study confirms the presence and close association of C. insignis with cattle in Maranh˜ao state, northeastern Brazil and emphasizes the risk of bluetongue infections spreading in the area. Key words. Culicoides insignis, bluetongue, cattle.
The genus Culicoides, known as ‘maruim’ in Brazil, is of medical and veterinary importance because the bloodsucking females of some species can transmit viruses that cause diseases such as Oropouche fever, affecting humans in the Amazon basin, and bluetongue (BT), affecting wild and domestic animals in several countries (Mellor et al., 2000). Bluetongue is a non-contagious viral disease affecting many wild and domesticated ruminants in several countries, including Brazil. Clinical disease manifests most often in sheep (Antoniassi et al., 2010) and is less frequently in cattle; however, in the latter, highly susceptible animals may be severely affected (Kettle, 1995). The disease has an economic impact on cattle farming owing to production losses in the affected herds and on the international trade of animals and their products. The main insect vectors of bluetongue virus (BTV) are Culicoides sonorensis Wirth and Jones in North America, Culicoides imicola Kieffer in Africa and Southern Europe, Culicoides fulvus Sen and Gupta and Culicoides brevitarsis Kieffer in Australia, Culicoides pusillus Lutz, and Culicoides
insignis Lutz in South USA, Central and South America (Mellor et al., 2000). The Culicoides obsoletus group and probably the Culicoides pulicaris group have recently been implicated as potential vectors of BTV in Northern Europe (Carpenter et al., 2009). In Brazil, serological surveys have detected BTV infection in the states of Minas Gerais (Konrad et al., 2003), Rio Grande do Sul (Costa et al., 2006), Paraíba (Alves et al., 2009) and Bahia (Dorneles et al., 2012). Information regarding Culicoides abundance and distribution in Brazil is however limited to a few surveys done in some parts of the country (Silva & Rebˆelo, 1999; Silva et al., 2001; Laender et al., 2004). However, to date, clinical manifestations of BT with isolation of viral serotypes have only been recorded in the south of Brazil (Antoniassi et al., 2010). In spite of the fact that 6 million cattle, 24% of the effective cattle herd in north-eastern Brazil, are present in Maranh˜ao state, no research on BTV circulation has been conducted. In addition, as mentioned above, only a relative few Culicoides midge surveys, especially in cattle breeding areas, have been
Correspondence: Francinaldo S. Silva, Laboratory of Medical Entomology, Center for Agrarian and Environmental Sciences, Federal University of Maranh˜ao, Chapadinha, Maranh˜ao 65500–000, Brazil. Tel/Fax.: + 55 98 3471 1201; E-mail: [email protected] 228
© 2013 The Royal Entomological Society
Livestock-associated Culicoides species done in Brazil. Therefore, the main purpose of this study was to investigate the association of the BTV vector C. insignis with livestock in northeastern Brazil. Culicoides biting midges were sampled once a month from January to December 2010, between 18.00 and 06.00 hours, with CDC incandescent light traps. Twelve collections were made at each of three sites. The collections were carried out on a farm located at the margins of BR-222 highway (3◦ 44 17 S and 43◦ 20 29 W), in Northeastern Maranh˜ao. The region has a hot, semi-humid climate with the annual average temperature ranging from 28 to 30 ◦ C. The mean annual rainfall ranges from 1600 to 2000 mm. The region has two distinct seasons, a rainy season from January to June and a dry season from July to December. Three light traps, one each in a pigsty, chicken coop and a bovine corral, were set in the peridomiciliary area of the farm. Several species of domestic animals such as chickens, geese, turkeys, dogs and pigs were present on the farm during the study. Chickens roamed freely in the peridomiciliary area during the day and roosted inside the chicken coop at night. The chicken coop was 12 m away from the principal dwelling. Pigs were in a 20 × 10-m enclosure next to a forested area, about 50 m from the principal dwelling. The bovine corral, with 50–100 head of cattle, was 600 m from the principal dwelling. The light trap at the chicken coop was 40 m from the trap at the pigsty. These two traps were 600 m from the bovine corral. After sampling, the insects were killed using ethyl acetate vapours and preserved in 70% alcohol. Collections were identified to the species level using the keys provided by Wirth and Blanton (1973) and Wirth et al. (1988). All voucher specimens are lodged in the collection of the Laboratory of Medical Entomology, Center for Agrarian and
229
Environmental Sciences, Federal University of Maranh˜ao, Chapadinha, Maranh˜ao, Brazil. Species richness was evaluated by summing the number of species in each animal shed. Midge diversity was assessed according to Shanon-Wiener indices using DivEs, Version 2.0 (Lizaro Soft, Brazil; Rodrigues, 2005) Software. The Kruskal–Wallis test was used to compare the abundance of individuals in the three animal sheds and the Mann–Whitney test for assessing the differences between males and females, both using the software Prism (GraphPad, San Diego, CA, U.S.A.). Each sampling date was a replication when the Kruskal–Wallis and the Mann–Whitney tests were conducted. A total of 22 316 individuals distributed in 17 species was found. The most abundant species were C. insignis, Culicoides paucienfuscatus Barbosa, Culicoides leopoldoi Ortiz, Culicoides duartei Tavares and Luna Dias, Culicoides diabolicus Hoffman, Culicoides. foxi Ortiz and Culicoides ignacioi Forattini (Table 1). Females predominated over males, with 22 211 individuals against 105 males. Culicoides insignis was the most abundant species (18 071 individuals) accounting for 80.9% of the total sample. Of these, 98.2% were captured in the corral. This result was statistically significant (P < 0.05). In the pigsty, the most abundant species were C. insignis and C. paucienfuscatus, with 38% and 28%, respectively. In the chicken coop, C. paucienfuscatus was the prevailing species (89.8%). Of the seven most abundant species, four (C. insignis, C. diabolicus, C. foxi and C. ignacioi ) were sampled mostly in the corral and three (C. paucienfuscatus, C. leopoldoi and C. duartei ) in the chicken coop. No species was found preferentially in the pigsty. Culicoides pusillus, considered an important BTV vector in Central and South America, was
Table 1. Species of Culicoides biting midges captured in CDC light traps and their relative abundance and per cent in Northeastern Brazil from January to December 2010. Corral
Chicken coop
Pigsty
Total
Species
N
%
N
%
N
%
N
%
C. insignis C. paucienfuscatus C. diabolicus C. leopoldoi C. duartei C. foxi C. ignacioi C. lutzi C. paraensis C. pusillus C. limai C. ruizi C. flavivenula C. lahillei C. neoparaensis Individuals Richness Diversity
17 744 201 208 11 35 140 14 5 — 4 — 1 — 1 — 18 364 11 H’: 1.0940
98.2 6.2 67.5 4.9 15.8 68.6 70 71.4
12 2805 2 191 108 1 — — 3 — — — — — — 3122 7 H’: 1.6419
0.1 86.4 0.6 85.3 48.9 0.5 — — 75 — — — — — — 13.9
315 240 98 22 78 63 6 2 1 — 3 — 1 — 1 830 12 H’: 2.2202
1.7 7.4 31.9 9.8 35.3 30.9 30 28.6 25 — 100 — 100 — 100 3.7
18 071 3246 308 224 221 204 20 7 4 4 3 1 1 1 1 22 316 15 H’: 4.9561
100 100 100 100 100 100 100 100 100 100 100 100 100 100 100 100
100 — 100 — 100 — 82.3
© 2013 The Royal Entomological Society, Medical and Veterinary Entomology, 28, 228–231
230
L. P. C. Carvalho and F. S. Silva
Table 2. Seasonal distribution of Culicoides biting midges captured in CDC light traps in Northeastern Brazil from January to December 2010. Rainy season is January to June; dry season is July to December. Corral
C. insignis C. paucienfuscatus C. diabolicus C. leopoldoi C. duartei C. foxi C. ignacioi C. lutzi C. paraensis C. pusilus C. limai C. ruizi C. flavivenula C. lahillei C. neoparaensis Total Total
Chicken coop
Pigsty
Rainy
Dry
Rainy
Dry
Rainy
Dry
15 850 200 208 10 35 135 13 5 — 4 — 1 — — — 16 461 18 364
1894 1 — 1 — 5 1 — — — — — — 1 — 1903
2 2749 1 148 50 — — — 3 — — — — — — 2953 3122
10 56 1 43 58 1 — — — — — — — — — 169
298 230 95 17 78 62 5 1 1 — — — 1 — — 788 830
17 10 3 5 — 1 1 1 — — 3 — — — 1 42
only collected in the corral and was among the least abundant species in the present survey. Culicoides species were found all year round, with peaks of abundance in the rainy season (> 90%) (Table 2). The relative abundance of C. insignis reached 89% in the corral in the second trimester of the year, just over halfway through the rainy season. The close association found between C. insignis and cattle in Northeastern Brazil in the present study is in agreement with previous studies (Saenz & Greiner, 1994). The muddy substrate found in a corral favours the immature development of C. insignis (Kettle, 1977) and the mammophilic behaviour of this species contributed to the occurrence of a high numbers of adults in light traps in both the corral and pigsty and low concentration in the chicken coop. Rainfall contributed to the increase in the abundance of midges by providing a muddy and humid environment for larval development. The epidemiology of BT may be affected by weather as well as vector distribution. As the annual temperature does not vary substantially, rainfall rather than temperature will play a more important role in governing the seasonal abundance of Culicoides midges in this part of the country. Because C. paucienfuscatus, the second most abundant species in the present survey, is usually found in higher concentrations at chicken coops than in animal baited traps, it is considered to be an ornithophilic species (Castell´on, 1990; Silva & Carvalho, 2013). Culicoides paraensis, the vector of Oropouche fever in Amazonian areas, is of interest to public health in Northeastern Brazil (Mellor et al., 2000). Culicoides paraensis is a diurnal man-biting insect usually found in urban areas (Hoch et al., 1990, Silva & Carvalho, submitted), and the relative low numbers collected in the present study may be related with this behavioural aspect and because the light
traps is ineffective for collection of diurnal species. A banana plantation, a very important environment for C. paraensis larval development (Hoch et al., 1990), near the chicken coop and the pigsty possibly favoured the occurrence of this species at these two collection sites. Culicoides pusillus, considered a secondary vector of BTV in Central and South America, is also of interest (Mo et al., 1994). The fact that this species was only captured in the corral supports its potential role in the transmission cycle of BTV. This species together with C. insignis has been captured in corral areas previously (Greiner et al., 1993). The global distribution of BT follows the insect vector distribution and most of Brazil is within the BT endemic zone where infection is common and the disease is not. Given that C. insignis feed on cattle and the high numbers collected near cattle, the risk of BTV spreading in Northeastern Brazil might be high and require special attention.
Acknowledgements We would like to thank Mr Bena and family for allowing insect collections on their farm and the anonymous referees for most useful comments on the manuscript.
References Alves, F.A.L., Alves, C.J., Azevedo, S.S., Silva, W.W., Silva, M.L.C.R., Lobato, Z.I.P. & Clementino, I.J. (2009) Soroprevalˆencia e fatores de risco para a língua azul em carneiros das mesorregi˜oes do Sert˜ao e da Borborema, semi´arido do Estado da Paraíba, Brasil. Ciˆencia Rural , 39, 484–489. Antoniassi, N.A.B., Pavarini, S.P., Henzel, A., Flores, E. & Driemeier, D. (2010) Aspiration pneumonia associated with oesophageal
© 2013 The Royal Entomological Society, Medical and Veterinary Entomology, 28, 228–231
Livestock-associated Culicoides species myonecrosis in sheep due to BTV infection in Brazil. Veterinary Record , 166, 52–53. Carpenter, S., Wilson, A. & Mellor, P.S. (2009) Culicoides and the emergence of bluetongue virus in northern Europe. Trends in Microbiology, 17, 172–178. Castell´on, E.G. (1990) Culicoides (Diptera: Ceratopogonidae) na Amazˆonia brasileira. II. Esp´ecies coletadas na reserva florestal Ducke, aspectos ecol´ogicos e distribuic¸a˜ o gegr´afica. Acta Amazˆonica, 20, 83–93. Costa, J.J.R., Lobato, Z.I.P., Herrmann, G.P., Leite, R.C. & Haddad, J.P.A. (2006) Prevalˆencia de anticorpos contra o vírus da língua em bovinos e ovinos do sudoeste e sudeste do Rio Grande do Sul. Arquivo Brasileiro de Medicina Veterin´aria e Zootecnia, 58, 273–275. Dorneles, E.M.S., Morcati, F.C., Guimar˜aes, A.S. et al. (2012) Prevalence of bluetongue virus antibodies in sheep from Distrito Federal, Brazil. Semina: Ciˆencias Agr´arias, Londrina, 33, 1521–1524. Greiner, E.C., Claudette, L., Mo, E., Homan, J., Gonzalez, J. & Marco-Tulio, O. (1993) Epidemiology of bluetongue in Central America and the Caribbean: initial entomological findings. Medical and Veterinary Entomology, 7, 309–315. Hoch, A.L., Roberts, D.R. & Pinheiro, F.P. (1990) Host-seeking behaviour and seasonal abundance of Culicoides paraensis (Diptera: Ceratopogonidae) in Brazil. Journal of the American Mosquito Control Association, 6, 110–114. Kettle, D.S. (1977) Biology and bionomics of bloodsucking ceratopogonids. Annual Review of Entomology, 22, 33–51. Kettle, D.S. (1995) Medical and Veterinary Entomology, 2nd edn. CAB International, Wallingford. Konrad, P.A., Rodrigues, R.O., Chagas, A.C.P., Paz, G.F. & Leite, R.C. (2003) Anticorpos contra o vírus da Língua Azul em bovinos leiteiros de Minas Gerais e Associac¸o˜ es com problemas reprodutivos. Revista da FZVA, 10, 117–125. Laender, J.O., Ribeiro, E.S., Gouveia, A.M.G., Lobato, Z.I.P. & Felippe-Bauer, M.L. (2004) Levantamento das esp´ecies de Culicoides Latreille, 1809 (Diptera: Ceratopogonidae) encontradas nas Mesorregi˜oes Norte de Minas, Jequitinhonha e Vale do Mucuri, Minas Gerais, Brasil. Entomologia & Vectors, 11, 145–157.
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Mellor, P.S., Boorman, J. & Baylis, M. (2000) Culicoides Biting Midges: their role as arbovirus vectors. Annual Review of Entomology, 45, 307–340. Mo, C.L., Thompson, L.H., Homan, E.J., Oviedo, M.T., Greiner, E.C., Gonz´alez, J. & S´aenz, M.R. (1994) Bluetongue virus isolations from vectors and ruminants in Central America and the Caribbean. American Journal of Veterinary Research, 55, 211–215. Rodrigues, W.C. (2005) DivEs – Diversidade de esp´ecies – guia do usu´ario. Serop´edica: Entomologistas do Brasil, 9p. http://www.ebras.bio.br/dives/ [accessed on 10 June 2011]. Saenz, M.R. & Greiner, E.C. (1994) Culicoides aspirated from cattle in Costa Rica, Honduras, Panama and Puerto Rico, and their role as potential vectors of bluetongue viruses. Regional Bluetongue Team. Medical and Veterinary Entomology, 8, 15–19. Silva, F.S. & Rebˆelo, J.J.M. (1999) Esp´ecies de Culicoides Latreille (Diptera, Ceratopogonidae) da ilha de S˜ao Luis, Maranh˜ao, Brasil. Boletim do Museu Paraense Emilio Goeldi , 15, 169–179. Silva, C.S., Felippe-Bauer, M.L., Almeida, E.H.G. & Figueiredo, L.R. (2001) Culicoides (Diptera: Ceratopogonidae) do estado do Rio de Janeiro, Brasil. I. Regi˜ao Norte: Município de Campos do Goytacazes. Entomologia & Vectores, 8, 349–358. Silva, F.S. & Carvalho, L.P.C. (2013) A Population Study of the Culicoides Biting Midges (Diptera: Ceratopogonidae) in Urban, Rural, and Forested Sites in a Cerrado Area of Northeastern Brazil. Annals of Entomological Society of American, 106, 463–470. Wirth, W.W. & Blanton, F.S. (1973) A review of the maruins or biting midges of the genus Culicoides (Diptera: Ceratopogonidae) in the Amazon Basin. Amazoniana, 4, 405–470. Wirth, W.W., Dyce, A.L. & Spinelli, G.R. (1988) An atlas of wing photographs, of a summary of the numerical characters of the Neotropical species of Culicoides (Diptera: Ceratopogonidae). Contributions of the American Entomological Institute, 25, 1–72. Accepted 22 May 2013 First published online 30 December 2013
© 2013 The Royal Entomological Society, Medical and Veterinary Entomology, 28, 228–231
doi: 10.1111/mve.12043
SHORT COMMUNICATION
Seasonal abundance of livestock-associated Culicoides species in northeastern Brazil L. P. C. C A R V A L H O and F. S. S I L V A Laboratory of Medical Entomology, Center for Agrarian and Environmental Sciences, Federal University of Maranh˜ao, Chapadinha, Maranh˜ao, Brazil
Abstract. Culicoides biting midges (Diptera: Ceratopogonidae) are of great medical and veterinary importance because the haematophagous females of some species can transmit diseases to humans and animals. In order to determine the presence and seasonal abundance of the bluetongue virus (BTV) vector Culicoides insignis Lutz at domestic animal sheds in northeastern Brazil, insects were collected once a month between January and December 2010. Light traps were set from 18.00 to 06.00 hours at a pigsty, chicken coop and bovine corral. Culicoides insignis accounted for 81% of the 22 316 specimens collected. Other well-represented species were: Culicoides paucienfuscatus Barbosa (3246 individuals), Culicoides diabolicus Hoffman (308), Culicoides leopoldoi Ortiz (224) and Culicoides duartei Tavares and Luna Dias (221). The remainder accounted for 4% of the total sample. Culicoides insignis occurred mostly at the cattle corral, 98.2% in the rainy season. This study confirms the presence and close association of C. insignis with cattle in Maranh˜ao state, northeastern Brazil and emphasizes the risk of bluetongue infections spreading in the area. Key words. Culicoides insignis, bluetongue, cattle.
The genus Culicoides, known as ‘maruim’ in Brazil, is of medical and veterinary importance because the bloodsucking females of some species can transmit viruses that cause diseases such as Oropouche fever, affecting humans in the Amazon basin, and bluetongue (BT), affecting wild and domestic animals in several countries (Mellor et al., 2000). Bluetongue is a non-contagious viral disease affecting many wild and domesticated ruminants in several countries, including Brazil. Clinical disease manifests most often in sheep (Antoniassi et al., 2010) and is less frequently in cattle; however, in the latter, highly susceptible animals may be severely affected (Kettle, 1995). The disease has an economic impact on cattle farming owing to production losses in the affected herds and on the international trade of animals and their products. The main insect vectors of bluetongue virus (BTV) are Culicoides sonorensis Wirth and Jones in North America, Culicoides imicola Kieffer in Africa and Southern Europe, Culicoides fulvus Sen and Gupta and Culicoides brevitarsis Kieffer in Australia, Culicoides pusillus Lutz, and Culicoides
insignis Lutz in South USA, Central and South America (Mellor et al., 2000). The Culicoides obsoletus group and probably the Culicoides pulicaris group have recently been implicated as potential vectors of BTV in Northern Europe (Carpenter et al., 2009). In Brazil, serological surveys have detected BTV infection in the states of Minas Gerais (Konrad et al., 2003), Rio Grande do Sul (Costa et al., 2006), Paraíba (Alves et al., 2009) and Bahia (Dorneles et al., 2012). Information regarding Culicoides abundance and distribution in Brazil is however limited to a few surveys done in some parts of the country (Silva & Rebˆelo, 1999; Silva et al., 2001; Laender et al., 2004). However, to date, clinical manifestations of BT with isolation of viral serotypes have only been recorded in the south of Brazil (Antoniassi et al., 2010). In spite of the fact that 6 million cattle, 24% of the effective cattle herd in north-eastern Brazil, are present in Maranh˜ao state, no research on BTV circulation has been conducted. In addition, as mentioned above, only a relative few Culicoides midge surveys, especially in cattle breeding areas, have been
Correspondence: Francinaldo S. Silva, Laboratory of Medical Entomology, Center for Agrarian and Environmental Sciences, Federal University of Maranh˜ao, Chapadinha, Maranh˜ao 65500–000, Brazil. Tel/Fax.: + 55 98 3471 1201; E-mail: [email protected] 228
© 2013 The Royal Entomological Society
Livestock-associated Culicoides species done in Brazil. Therefore, the main purpose of this study was to investigate the association of the BTV vector C. insignis with livestock in northeastern Brazil. Culicoides biting midges were sampled once a month from January to December 2010, between 18.00 and 06.00 hours, with CDC incandescent light traps. Twelve collections were made at each of three sites. The collections were carried out on a farm located at the margins of BR-222 highway (3◦ 44 17 S and 43◦ 20 29 W), in Northeastern Maranh˜ao. The region has a hot, semi-humid climate with the annual average temperature ranging from 28 to 30 ◦ C. The mean annual rainfall ranges from 1600 to 2000 mm. The region has two distinct seasons, a rainy season from January to June and a dry season from July to December. Three light traps, one each in a pigsty, chicken coop and a bovine corral, were set in the peridomiciliary area of the farm. Several species of domestic animals such as chickens, geese, turkeys, dogs and pigs were present on the farm during the study. Chickens roamed freely in the peridomiciliary area during the day and roosted inside the chicken coop at night. The chicken coop was 12 m away from the principal dwelling. Pigs were in a 20 × 10-m enclosure next to a forested area, about 50 m from the principal dwelling. The bovine corral, with 50–100 head of cattle, was 600 m from the principal dwelling. The light trap at the chicken coop was 40 m from the trap at the pigsty. These two traps were 600 m from the bovine corral. After sampling, the insects were killed using ethyl acetate vapours and preserved in 70% alcohol. Collections were identified to the species level using the keys provided by Wirth and Blanton (1973) and Wirth et al. (1988). All voucher specimens are lodged in the collection of the Laboratory of Medical Entomology, Center for Agrarian and
229
Environmental Sciences, Federal University of Maranh˜ao, Chapadinha, Maranh˜ao, Brazil. Species richness was evaluated by summing the number of species in each animal shed. Midge diversity was assessed according to Shanon-Wiener indices using DivEs, Version 2.0 (Lizaro Soft, Brazil; Rodrigues, 2005) Software. The Kruskal–Wallis test was used to compare the abundance of individuals in the three animal sheds and the Mann–Whitney test for assessing the differences between males and females, both using the software Prism (GraphPad, San Diego, CA, U.S.A.). Each sampling date was a replication when the Kruskal–Wallis and the Mann–Whitney tests were conducted. A total of 22 316 individuals distributed in 17 species was found. The most abundant species were C. insignis, Culicoides paucienfuscatus Barbosa, Culicoides leopoldoi Ortiz, Culicoides duartei Tavares and Luna Dias, Culicoides diabolicus Hoffman, Culicoides. foxi Ortiz and Culicoides ignacioi Forattini (Table 1). Females predominated over males, with 22 211 individuals against 105 males. Culicoides insignis was the most abundant species (18 071 individuals) accounting for 80.9% of the total sample. Of these, 98.2% were captured in the corral. This result was statistically significant (P < 0.05). In the pigsty, the most abundant species were C. insignis and C. paucienfuscatus, with 38% and 28%, respectively. In the chicken coop, C. paucienfuscatus was the prevailing species (89.8%). Of the seven most abundant species, four (C. insignis, C. diabolicus, C. foxi and C. ignacioi ) were sampled mostly in the corral and three (C. paucienfuscatus, C. leopoldoi and C. duartei ) in the chicken coop. No species was found preferentially in the pigsty. Culicoides pusillus, considered an important BTV vector in Central and South America, was
Table 1. Species of Culicoides biting midges captured in CDC light traps and their relative abundance and per cent in Northeastern Brazil from January to December 2010. Corral
Chicken coop
Pigsty
Total
Species
N
%
N
%
N
%
N
%
C. insignis C. paucienfuscatus C. diabolicus C. leopoldoi C. duartei C. foxi C. ignacioi C. lutzi C. paraensis C. pusillus C. limai C. ruizi C. flavivenula C. lahillei C. neoparaensis Individuals Richness Diversity
17 744 201 208 11 35 140 14 5 — 4 — 1 — 1 — 18 364 11 H’: 1.0940
98.2 6.2 67.5 4.9 15.8 68.6 70 71.4
12 2805 2 191 108 1 — — 3 — — — — — — 3122 7 H’: 1.6419
0.1 86.4 0.6 85.3 48.9 0.5 — — 75 — — — — — — 13.9
315 240 98 22 78 63 6 2 1 — 3 — 1 — 1 830 12 H’: 2.2202
1.7 7.4 31.9 9.8 35.3 30.9 30 28.6 25 — 100 — 100 — 100 3.7
18 071 3246 308 224 221 204 20 7 4 4 3 1 1 1 1 22 316 15 H’: 4.9561
100 100 100 100 100 100 100 100 100 100 100 100 100 100 100 100
100 — 100 — 100 — 82.3
© 2013 The Royal Entomological Society, Medical and Veterinary Entomology, 28, 228–231
230
L. P. C. Carvalho and F. S. Silva
Table 2. Seasonal distribution of Culicoides biting midges captured in CDC light traps in Northeastern Brazil from January to December 2010. Rainy season is January to June; dry season is July to December. Corral
C. insignis C. paucienfuscatus C. diabolicus C. leopoldoi C. duartei C. foxi C. ignacioi C. lutzi C. paraensis C. pusilus C. limai C. ruizi C. flavivenula C. lahillei C. neoparaensis Total Total
Chicken coop
Pigsty
Rainy
Dry
Rainy
Dry
Rainy
Dry
15 850 200 208 10 35 135 13 5 — 4 — 1 — — — 16 461 18 364
1894 1 — 1 — 5 1 — — — — — — 1 — 1903
2 2749 1 148 50 — — — 3 — — — — — — 2953 3122
10 56 1 43 58 1 — — — — — — — — — 169
298 230 95 17 78 62 5 1 1 — — — 1 — — 788 830
17 10 3 5 — 1 1 1 — — 3 — — — 1 42
only collected in the corral and was among the least abundant species in the present survey. Culicoides species were found all year round, with peaks of abundance in the rainy season (> 90%) (Table 2). The relative abundance of C. insignis reached 89% in the corral in the second trimester of the year, just over halfway through the rainy season. The close association found between C. insignis and cattle in Northeastern Brazil in the present study is in agreement with previous studies (Saenz & Greiner, 1994). The muddy substrate found in a corral favours the immature development of C. insignis (Kettle, 1977) and the mammophilic behaviour of this species contributed to the occurrence of a high numbers of adults in light traps in both the corral and pigsty and low concentration in the chicken coop. Rainfall contributed to the increase in the abundance of midges by providing a muddy and humid environment for larval development. The epidemiology of BT may be affected by weather as well as vector distribution. As the annual temperature does not vary substantially, rainfall rather than temperature will play a more important role in governing the seasonal abundance of Culicoides midges in this part of the country. Because C. paucienfuscatus, the second most abundant species in the present survey, is usually found in higher concentrations at chicken coops than in animal baited traps, it is considered to be an ornithophilic species (Castell´on, 1990; Silva & Carvalho, 2013). Culicoides paraensis, the vector of Oropouche fever in Amazonian areas, is of interest to public health in Northeastern Brazil (Mellor et al., 2000). Culicoides paraensis is a diurnal man-biting insect usually found in urban areas (Hoch et al., 1990, Silva & Carvalho, submitted), and the relative low numbers collected in the present study may be related with this behavioural aspect and because the light
traps is ineffective for collection of diurnal species. A banana plantation, a very important environment for C. paraensis larval development (Hoch et al., 1990), near the chicken coop and the pigsty possibly favoured the occurrence of this species at these two collection sites. Culicoides pusillus, considered a secondary vector of BTV in Central and South America, is also of interest (Mo et al., 1994). The fact that this species was only captured in the corral supports its potential role in the transmission cycle of BTV. This species together with C. insignis has been captured in corral areas previously (Greiner et al., 1993). The global distribution of BT follows the insect vector distribution and most of Brazil is within the BT endemic zone where infection is common and the disease is not. Given that C. insignis feed on cattle and the high numbers collected near cattle, the risk of BTV spreading in Northeastern Brazil might be high and require special attention.
Acknowledgements We would like to thank Mr Bena and family for allowing insect collections on their farm and the anonymous referees for most useful comments on the manuscript.
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