doi:10.12741/ebrasilis.v10i2.686 e-ISSN 1983-0572 Publication of the project Entomologistas do Brasil www.ebras.bio.br Creative Commons Licence v4.0 (BY-NC-SA) Copyright © EntomoBrasilis Copyright © Author(s) Ecology/Ecologia Seasonality and Relative Abundance of Tabanids (Diptera, Tabanidae) on Marambaia Island, Rio de Janeiro, Brazil

Ronald Rodrigues Guimarães¹, Ronald Rodrigues Guimarães Júnior², Ronald Storti Harlan-Rodrigues³, Roney Rodrigues Guimarães4, Raimundo Wilson Carvalho5 & Roberto de Xerez6

1. Universidade Estácio de Sá, Centro de Ciências Biológicas e da Saúde. 2. Associação Brasileira de Ensino Universitário, Nova Iguaçu, RJ. 3. Centro de Educação e Pesquisas em Medicina Ambiental. 4. Universidade Estácio de Sá/Centro Universitário de Barra Mansa. 5. Escola Nacional de Saúde Pública Sérgio Arouca da Fundação Oswaldo Cruz. 6. Universidade Federal Rural do Rio de Janeiro

EntomoBrasilis 10 (2): 82-88 (2017)

Abstract. Tabanids collections were conducted on Marambaia Island, Atlantic Forest biome, Rio de Janeiro, Brazil. Thirty-one species were identified belonging to 16 genera. Seasonal variation and its relationship with the most important climatic factors during 1981 and 2013 and observations on the bionomics of each species are presented.

Keywords: Atlantic Forest; Biodiversity; Deer ; Horse fly; vector.

Variação sazonal e abundância de tabânidas (Diptera, Tabanidae) na Ilha da Marambaia, Rio de Janeiro, Brasil

Resumo. Coletas de tabânidas foram realizadas na ilha de Marambaia, bioma da Mata Atlântica, Rio de Janeiro, Brasil. Trinta e uma espécies foram identificadas pertencentes a 16 gêneros. São apresentadas a variação sazonal, observações sobre bionomia e a relação com os fatores climáticos mais importantes durante os anos de 1981 e 2013.

Palavras-chave: Biodiversidade; Inseto vetor; Mata Atlântica; Moscas dos veados; Moscas dos cavalos.

The family Tabanidae Latreille comprises about 4,400 essential for the election of control strategies (Fr a n c i s 1919; described species, of which 1,205 are present in the Kl o c k et al. 1973; Kr i n s k y 1976; Fo i l 1989; Ott e & Ab u a b a r a Neotropics (He n r i q u e s et al. 2012). Tabanids are the 1991; Si l v a et al. 1996). Due to the increasing knowledge of largest bloodsucking diptera, reaching up to 2.5 cm, robust body tabanids role in disease transmission, more studies are held in and some with a well-developed proboscis, looks imposing and places of more immediate human interest, such as settlements, awe. Repeatedly attack humans, domestic and wild , farms, pastures, attractions. However, the role of wild areas in among primates, rodents, alligators, snakes, turtles and birds, maintaining natural foci of zoonosis should not be overlooked especially during the drier seasons. They are known worldwide (Pa v l o v s k y 1966). for its painful sting and being mechanical and biological transmission of more than 35 pathogens among helminths, The first studies on tabanids on Atlantic Forest biome were viruses, bacteria and protozoan, etiologic agents of diseases that conducted by Lutz between 1905 and 1914, in which he described can affect humans and wild and domestic animals (Kr i n s k y 1976; 144 species of which 72 are still valid (Lu t z 1905, 1907, 1909, Pe c h u m a n & Te s k e y 1981; Fo i l 1989; Fo i l & Is s e l 1991; Ma r c o n d e s 1910, 1913a, b, 1914; Lu t z & Ne i v a 1909, 1914; Be n c h i m o l & Sá 2001; Lu z -Al v e s et al. 2007; Tu r c a t e l et al. 2007). Around the 2005). Despite the importance of tabanids in transmission of world more and better evidence has been gathered to assess the bovine and equine tripanosomosis in South and southern Brazil, importance of Tabanids in an epidemiological context. the studies of tabanids are mainly conducted for knowledge of ecology (Bo u v i e r 1952, Du t r a & Ma r i n o n i 1994, Ba s s i et al. 2000, Several studies show a correlation between the period of Kr o l o w et al. 2010, Mi l e tt i et al. 2011, Gu i m a r ã e s et al. 2016) greatest activity of tabanids and the appearance of and and (Tu r c a t e l et al. 2007; Kr o l o w & Kr ü g e r 2007). human diseases. The season of year in which these vectors are most common means greater health risk to human and animal This study aimed to know the seasonality of more abundant populations exposed, and information about these facts are tabanid species occurring in Marambaia Island, Rio de Janeiro

Edited by:  Corresponding author: Funding agencies: Jeronimo Augusto Alencar Ronald Rodrigues Guimaraes  CAPES Processo nº 1.383.383, UNESA -

Article History:  [email protected] Pesquisa Produtividade  http://orcid.org/0000-0002-5990-2338 Received: 02.iii.2017 Accepted: 06.v.2017

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state, in southeast coastal Atlantic Forest biome, as well as the 23°02.54’S and 43°57.07’W. At this region, and in Vacaria Velha main climatic factors related. (23°03’47’’S, 43°59’13’’W), specimens were also collected using insect hand net. Tabanids specimens were identified by Drs. MATERIALS AND METHODS GB Fairchild, AL Henriques, IS Gorayeb, and RR Guimarães. Meteorological data of 1981 were provided by a higrothermograph Marambaia Island is a strip of land 42 kilometers long, with an and a pluviometer seated in Armação Beach; and at 2013, data 2 area of approximately 81 km , south of State of Rio de Janeiro, were provided by National Institute of Meteorology, from the in Mangaratiba county, at the entrance of Sepetiba Bay, between Auto-Meteorological Station of Marambaia Island (Rio de 23°0023º06’S and 43º45’44º41’ West (Figure 1). The island Janeiro Station-Marambaia-A602) located on sandbank, near landscape is a mosaic of large areas of originating preserved and the area of research (23°05.00’S and 43°60.00’W). Access to secondary Atlantic Rainforest, sandbank vegetation, little areas the research site was authorized by command of the Assessment of grasslands and mangroves. Center Marambaia Island, Navy of Brazil; for the collection and transport of samples was issued the license nº 33382-1, SISBIO- In 1981, as well as in 2013, monthly collections were made on IBAMA. Marambaia Island, using four Manitoba modified canopy trap seated in an ecotone area between rain forest and dunes. The traps were placed near Armação Beach (Bravo 10), located at

A

B

Figure 1. 1a. Geographic location of Restinga and Marambaia Island, county of Mangaratiba, Rio de Janeiro state, Brazil. 1b. Tabanid sampling sites on Marambaia Island. Sources: (a) - Scielo. Available on: . [Accessed in: 12.iii.2014]. (b) - GoogleMaps. Available on: . [Accessed in: 12.ii.2014].

RESULTS AND DISCUSSION (2.58%), walteri (Guimarães et al.) (1.94%), Phaeotabanus cajennense Fabricius) (1.45%) and During the two periods of study, 3016 specimens belonging to 31 fuscus Wiedemann (1.45%); Chrysops varians Wiedemann, tabanid species were collected by canopy trap, distributed in 16 Rhabdotylus planiventris (Wiedemann), genera of Tabanidae. was the most representative, longicornis (Fabricius), Phaeotabanus litigiosus (Walker), with 16 species in 9 genera, followed by with 9 species Scaptia seminigra Ricardo, Stigmatophtalmus altivagus in 2 genera, Scionini with 2 species in 2 genera, and Pangoniini Lutz, Rhabdotylus viridiventris Macquart were less abundant and Scepsini with 1 species in 1 genus each, and 2 species of than 1% each one (Table 1). During 2013 were captured 2102 Chrysopsini, in 1 genus. In the first period of study (1981), 619 specimens of tabanids, distributed in 12 species listed according specimens were captured by canopy traps, distributed in 15 the order of decreasing number of specimens, and similarly than

species: the most abundant species was bivittatus in 1981, the most abundant species was D. bivittatus (86.25%) 83 Wiedemann (70.44%), followed by Diachlorus distinctus Lutz followed by D. distinctus (4.33%), T. occidentalis (3.90%), T. (7.59%), Tabanus occidentalis Linnaeus (6.62%), Chrysops triangulum (2.19%), D. alcicornis (2.05%), D. walteri (1,14%), variegatus (De Geer) (5.17%), Tabanus triangulum Wiedemann P. cajennensis (0.33%), T. fuscus (0.29%), C. varians (0.24%)

e-ISSN 1983-0572 84 hn curd w pplto pas fauig w annual species. two bivoltine is it that featuring believe to leading species, peaks, the of generations population two occurred December, to when September and May to March from months the during species abundant most is It August. to June from months winter, when the number of captured specimens was lower, at the and 1981 during in year, even the active throughout was 2013, andit respectively, collected specimens total the of 86.25% and 70.44% representing trap, canopy by collected abundant, most by and Bassi 1990 in January 1993. On Marambaia Island November this species was the in Dutra by collected specimens from samples. collected of number total the of 4.08% represented species the March; to November from months the in except 1989, and 1988 in period study the throughout Paraná, Mel, of Island in species made Bahia and (2002). Liechtenberg Grosso Mato Amazonas, at P & ( Santo Espírito in occurs also it 2009) ( Catarina Santa to Janeiro periods of study. This species is distributed in Brazil, from Rio de bivittatus Diachlorus which wasnotdeterminedtheseasonalfluctuation. pungens Wiedemann, (Fabricius), limpidapex inanis (Wiedemann), winthemi lugubris species Others 2). captured in both two periods by (Table insect hand net were specimens collected total the of less altivagus S. and Seasonality andRelativeAbundanceoftabanids(Diptera,Tabanidae)… sandbank forestandAtlanticRainforest,MarambaiaIsland,Mangaratibacounty,RiodeJaneirostate,Brazil. Table 1. Seasonality and relative abundance of species tabanids captured using canopy traps, in 1981, in Armação Beach, in an ecotone area between Tabanus triangulum Tabanus fuscus Tabanus occidentalis Stigmatophtalmus altivagus Rhabdotylus viridiventris Rhabdotylus planiventris Phaeotabanus litigiosus Phaeotabanus cajennensis Dichelacera walteri Diachlorus distinctus Diachlorus bivittatus Acanthocera longicornis Scaptia seminigra Pangoninae Chrysops varians Chrysops variegattus Chrysopsinae a . planiventris R. p o r e v a , Paraná ( Paraná , (Fabricius), idmn, and Wiedemann, (Macquart) T (Wiedemann) Species RA (%) a c r u Total (Wiedemann), 20) at ob o te eod o te species the of records the on doubt cast (2009) and , aau claripennis Tabanus Catachlorops leptogaster aau importunus Tabanus t l e D u

Diachlorus varipes et al. et t . viridiventris R.

01%. tes pce were species Others (0.19%). a r Sess appendiculata Scepsis , a te ot rvln seis n both in species prevalent most the was & D (2007) recorded this species on Paraná on species this recorded (2007) u ,

M t . longicornis A. a r i n o n i r a F aau obsoletus Tabanus c r i a & 3,39 21 8 J 6 2 1 1 1 1 1 quadripunctatus quadripunctatus Poeciloderas h M L d l i 1994; i n o n i r a u (Bigot), ec oe ih .1 or 0.01% with one each , t 4,52 1971; z 28 22 (Rondani), Wiedemann, F & 2 3 1 Barreto, , N B 19) atrd this captured (1994) i s s a C a v i e aahoos flavus Catachlorops 15,19 n ó r a c s o 94 78 M Macquart 6 4 5 1

1909). aau discus Tabanus et al. et idmn, of Wiedemann, Phaeotabanus y Contreras- ​​by 8,24 . litigiosus P. 42 51 & P & 2000), but 2000), A 2 3 3 1 Esenbeckia Months andcollectedspecimens C Tabanus Fidena , n ó r a c s o a p 7,75 o r e v a 48 39 M 4 2 2 1 ,

3,07 19 12 J 2 2 3 the PlanaltoSerrano ofSantaCatarina. record not did (2011) ( season dry in September, to April from occidentalis or driftwood above the water surface or on bathers. onrocks landing collections, orfreshwater streams over flying study, of periods two the throughout observed commonly were al. 2004; & water depth ( on captured and observed commonly also is and environments, savanna in frequent more be to seems it but areas, unsheltered artificial or natural and forests on December, and July between and February. In Central Amazonas the peak of the species occurs throughout the year with peak population occurring in December ( canopy O forest in and activity, anthropic by occidentalis Tabanus ( (15.66%) after (15.40%), species 2010). In Central Amazon region it was the second more prevalent al. and Janeiro de ( Paraná Rio Amazonas, Grosso, Mato in reported was one of the most abundant species in the tropical region: in Brazil to Mexico colleagues, from and Rafael to According Argentina. species, distributed large very a is It study. of period both in August, and July for except year, the over all trap canopy by captured was and 2013), in 3,9% and 1981 in (6.62% occidentalis Tabanus Bassi inNovember1991. T as the period same during prevalent was it behavior; one, and anterior morphology to in both similar species a 2013), in 4.33% and 1981 was in prevalent more species second The a c r u a r i e v i l R 03. n aabi Iln seies of specimens Island Marambaia On 2003). 2000; u a e s s u o 0,65 t F l e 4 J 4 a r i e r r e

R

t al et et al. et B a O 1987; f s o r r a was prevalent all over the year, being more abundant l e a 0,00 a r i e v i l R 20) I Aao rgo te pce i active is species the region Amazon In 2007). . A 0 a (2007) in Paraná, from a specimen collected by collected specimen a from Paraná, in (2007) -K & f D. bivittatus D. l e a 2001; e B C P P i s s a

h & 6,95 t al et r e l 43 34 d o o w l r a S was recorded being active in opened areas opened in active being recorded was 6 1 1 1 T. occidentalis T. C

et al.

a te hr mr peaet species prevalent more third the was h t e H hroaau cinereus Phorcotabanus 2007; . d o o w l r a al s e u q i r n e 2,36 126 2000; . 2010). In Pantanal, Mato Grosso, 75 12 13 O . 9 4 4 5 1 1 1 1 1980; D. distinctus D. , 1980; F 2004; F 2004; 24,88 K a r i e r r e 154 105 16 12 N 8 5 5 1 1 1 w o l o r R in the study of tabanids in tabanids of study the in a H P R e-ISSN 1983-0572 B l e a 5,01 -K d n o m y a

s o r r a 31 was also recorded by recorded also was 19 et al. D a r i e r r e . distinctus D. 4 5 1 1 1 Guimaraes e

et al. et P P H r e l T. occidentalis T. 2010; 2001; Total s e u q i r n e 1986; . occidentalis T. 100 619 436 -K 1991;

32 47 16 41 (Wiedemann) 12 9 9 2 2 2 2 3 5 1 t al. et M e P P e l i et al. H B r e l R s e u q i r n e T T (7.59% s o r r a 2010). B 70,44 2004; d n o m y a 0,48 0,32 0,32 0,32 0,32 6,62 2,58 0,81 100 0,16 7,59 1,94 1,45 1,45 (%) 5,17 (2017) RA i i s s a

et al. et et al.

is T. et et

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Table 2. Seasonality and relative abundance of species tabanids captured using canopy traps, in 2013, in Armação Beach, in an ecotone area between sandbank forest and Atlantic Rainforest, Marambaia Island, Mangaratiba county, Rio de Janeiro state, Brazil.

Months and collected specimens RA Species Total J F M A M J J A S O N D (%) Chrysopsinae Chrysops varians 3 2 5 0,24 Tabaninae Diachlorus bivittatus 55 70 117 113 89 33 18 25 212 348 418 315 1813 86,25 Diachlorus distinctus 4 9 16 8 6 3 6 17 18 4 91 4,33 Dichelacera alcicornis 8 10 1 19 0,9 Dichelacera walteri 1 9 12 2 24 1,14 Phaeotabanus cajennensis 5 2 7 0,33 Phaeotabanus litigiosus 1 1 2 0,1 Rhabdotylus planiventris 2 1 1 4 0,19 Rhabdotylus viridiventris 1 1 0,05 Stigmatophtalmus altivagus 1 1 2 0,1 Tabanus fuscus 6 6 0,29 Tabanus occidentalis 8 6 8 9 8 2 8 8 13 12 82 3,9 Tabanus triangulum 2 12 5 4 2 18 3 46 2,19 Total 78 87 154 135 107 38 18 229 229 493 493 337 2398 100 RA (%) 3,25 3,63 6,42 5,63 4,46 1,58 0,75 9,55 9,55 20,56 20,56 14,05 100

Tabanus triangulum was the fourth more abundant species not caught by cannopy trap in 2013. Although D. walteri was (2.58% in 1981 and 2.19% in 2013) and was prevalent from described in 2015 (Gu i m a r ã e s et al. 2015), the specimens had February to May and from September to December, in both already been collected since 1981. years of study, with regard to probably bivoltine species. This is a southern South America species, ranging from Paraguay, In both years of 1983 and 2013, as a general trend, tabanids were Uruguay, Bolivia and Argentina, and in Brazil, in the states of most active from January to March and September to December, Espírito Santo, Rio de Janeiro, São Paulo, Paraná and Rio Grande i. e., when the rain fall, temperature and air humidity were highest do Sul (Bo u v i e r 1952; Fa i r c h i l d 1971; Ba s s i et al. 2000; Ba r r o s (Figures 1 and 2; Tables 1 and 2). This also occurs in Amazonian 2001; Kr o l o w et al. 2010). At Paraná, Campo Largo, this species region (Go r a y e b 1995), in Pantanal (Ba r r o s et al. 2003) and was was identified as the second most abundant species during the first recorded in southeast region by Bo u v i e r (1952) in São Paulo years 2002-2004, after Dichelacera alcicornis Wiedemann. state. During the two studies periods, tabanids on Marambaia It was present in Mato Grosso Pantanal throughout the year Island demonstrated a low or weak positive correlation between (Ba r r o s 1994). the number of specimens collected by traps and the temperature (ρ temp = 0,28 in 1981; ρ temp = 0,08 in 2013) and humidity (ρ Curiously, C. variegattus reached 5.17% of total collected hum = 0,67 in 1981; ρ hum = 0,03 in 2013) and monthly rainfall species in 1981, but it was not captured by canopy trap in 2013. (ρ pluv = 0,50 in 1981; ρ pluv = 0,01 in 2013). On Marambaia Island this species was more prevalent during October to December; in Central and East Amazon it was Several other studies for diagnosis of tabanids in other regions prevalent during throughout the year of collection (Fe r r e i r a - have used Malaise traps, Shannon, suspended Gorayeb traps, Ke pp l e r et al. 2010; Ra f a e l 1982). It was not captured in the animals or artificial lures, or canopy traps baited with octenol, Planalto Serrano of Santa Catarina, southeast Brazil (Mi l e tt i et carbonic gas, and has brought mixed results, more or less al. 2011). Each one of others species represented less than 2% of satisfactory, both in terms of number and variety of captured total captured specimens. and diagnosed species (Ra f a e l & Go r a y e b 1982; Ta kk e n & Kl i n e 1988; Ra f a e l et al. 1991, Hr i b a r et al. 1991; Ba r r o s et al. 2003; Among the species that was not captured by canopy trap, T. Ol i v e i r a et al. 2007; Kr o l o w et al. 2010). The modified Manitoba importunus is the most important, being considered a pest to canopy trap used in this study is low cost and easy to handle, human and animals, and because the transmission of equine and and may provide subsidies for early studies of tabanofauna, when bovine tripanosomosis in Central and southearn Brazil, Bolivia supplemented with other collection techniques. and Paraguay. In Amazon it was the commonest species during November (Ra f a e l et al. 1991). It also was recorded in Central The species on Marambaia Island, Rio de Janeiro also occur in Amazon (Ra f a e l 1982; He n r i q u e s & Ra f a e l 1999; He n r i q u e s other regions with different characteristics, particularly with 2004). In Mato Grosso Pantanal it was prevalent all over the years respect to the time of appearance and relative abundance of other of collections and it was the most abundant (56%) of the species species present in the same region. These facts may be linked captured by canopy trap (Ba r r o s 2001), and ranged 44.4% when to the limitations imposed by climate, where temperature and it was captured by insect hand net on an equine bait (Ba r r o s et humidity can play important roles as balancing factors between al. 2003). On Marambaia Island it was captured in the months of different tabanids species populations composing the biocenosis October and November. of the different regions.

The number of specimens collected during 1981 (619) was The different behaviors of each species identified in the 2 Marambaia Island compared to the behavior of the same species significantly lower than that collected in 2013 (2398) (X = 6,32; 85 GL = 1; P = 0,5%). But the five most prevalence species in both in other regions, characterize a unique and individualized periods were D. bivittatus, D. distinctus, Tabanus occidentalis, environment, i. e., each of the holarchical systems to which the T. triangulum and D. walteri, excepting C. variegatus that was species belong in different biocenosis. Although climatic factors

e-ISSN 1983-0572 86 enough toknow theseasonalvariation. not case, this in but difficulty, this for compensate to attempt an was bait equine animal an using capture The used. trap the by in exist captured not Certainly were that species region. other several Island Marambaia tabanids endemic enough the have of not diagnosis do but cost, low attractive ability to be used as the only is tool to perform a complete trap canopy Manitoba a for required. is sites studied of tabanofauna of understanding better tools other of use the that such accurate limitations has in study more used our trap The a areas. study to the in biodiversity contributes of knowledge which habitats, different in present in specimens collect to used be can traps Several regions. thespecies different of diagnosis accurate allowing efficient and varied become has tabanids collecting for methodology The factors determinethisphenomenon. also seem to be different, although it is not possible to state what years 30 of intervals at collected populations the from species of in the landscape structure should not be overlooked. The samples involved are that abiotic, and biotic factors, other numerous the behavior, population in differences the in role important an play Seasonality andRelativeAbundanceoftabanids(Diptera,Tabanidae)… (B1, B2,B3),onMarambaiaIsland,Mangaratibacounty,RiodeJaneirostate,Brazil. 2013 and A3) A2, (A1, 1981 years during fall rain and humidity air temperature, mean monthly collected, specimens tabanid of Number 2. Figure A3 A1 B2 ars ATM, 94 Rgsr d Tbndo (itr) em (Diptera) Tabanídeos de Registro 1994. A.T.M., Barros, de Sá. Estácio Universidade from scholarship by Produtividade Pesquisa granted scholarship a by CAPES (#1.383.383). part Currently, the main author is supported by and Arouca Sergio Health from the Post-Graduate Program of scholarship the National School a of Public by part in supported was author main The Navy. between Universidade Federal Rural do Rio de Janeiro Agreement and Brazil Cooperation Technical the of coordinator Xerez, de permission to for access and Brazil, contribution to of the work; Navy to Dr. - Roberto CADIM - Marambaia da Ilha da Avaliação de Centro the of staff and Command to grateful are authors The e aer. euo. i d Jnio UR / nttt de Instituto Biologia /Museu Nacional/SBZ,1994.p.187-188. / UFRJ Janeiro: de Rio Resumos. Janeiro. de Sul-Mato- Pantanal do Grossense. Região na hospedeiros diferentes In ACKNOWLEDGEMENTS Cnrso rslio e olga 2, Rio 20, Zoologia, de Brasileiro Congresso : REFERENCES B3 A2 B1 e-ISSN 1983-0572 Guimaraes et al. (2017) Maio - Agosto 2017 - www.periodico.ebras.bio.br EntomoBrasilis 10 (2): 82-88

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