Pesq. Vet. Bras. 38(1):183-188, janeiro 2018 DOI: 10.1590/S0100-736X2018000100028

Typology and distribution of antennal sensory organs of adults irritans of the Midwest Region of Brazil1

Fernando de Freitas Fernandes2* and Paulo Filemon Paolucci Pimenta3

ABSTRACT.- Fernandes F.F. & Pimenta P.F.P. 2018. Typology and distribution of antennal sensory organs of adult of the Midwest Region of Brazil. Pesqui- sa Veterinária Brasileira 38(1):183-188. Setor de Artropodologia Médica e Veterinária, Universidade Federal de Goiás, Avenida Esperança s/n, Campus Samambaia, Goiânia, GO 74690-900, Brazil. E-mail: [email protected] Considering the great economic and sanitarian importance of Haematobia irritans development of resistance of this species to the main chemical insecticides used in its con- trol, in several other localities of the world; as well as that different strains of the same − spe the-

was to investigate the typology and distribution of different types of sensillae of H. irritans cies frequently present different types and distribution patterns −, the present aim study- tory sensillae. This study provides new data on the typology and sensillary distribution of adults, from populations of this present in Brazilian Midwest, with emphasis on olfac and ten subtypes of sensilla: long bristles sensillum, long basiconic sensillum, blunt coe- loconicantennal sensillum, sensilla of clavate this fly. coeloconic In the antennal segmentssingle-tip were and found double-tip non-innervated spinulesgroo- ved coeloconic sensillum, long grooved coeloconic sensillum, trichoid sensillum, coeloconic sensillum, and smaller basiconic sensilla − subtypes −, the antennal sensillae of H. irritans. These results provide a morphological basis for future investigations on olfactory-mediated sensillum. behavior A slightof this sexual species, dimorphism and could assistwas observed future stu in-

populations, with less environmental impact. INDEXdies for TERMS: the development Haematobia irritansof alternative, antenna, measures ultrastructure, to the semiochemical, monitoring and olfactory control sensilla. of this fly

RESUMO.- [Tipologia e distribuição de órgãos sensila- tes tipos e subtipos sensilares de adulttos de H. irritans, res de Haematobia irritans adultas do Centro-Oeste do oriunda de populações desta mosca presentes no centro- Brasil.] Considerando a grande importância econômica e -oeste brasileiro, com ênfase nas sensilas olfatórias. Este sanitária de Haematobia irritans, o desenvolvimento de re- estudo apresenta novos dados sobre a tipologia e distri- sistência desta espécie aos principais inseticidas químicos buição sensilar da antenna desta mosca. Em seus segmen- utilizados em seu controle, em diversas outras localidades tos antenais foram observados pilosidades não enervadas do mundo, bem como que diferentes cepas de uma mesma e dez subtipos de sensilas, sendo: long bristles sensillum, espécie frequentemente apresentam diferentes tipos e pa- long basiconic sensillum, blunt coeloconic sensillum, clava- drões de distribuição sensilares, objetivou-se no presente te coeloconic sensilla - single-tip and double-tip subtypes -, trabalho investigar a tipologia e a distribuição dos diferen- grooved coeloconic sensillum, long grooved coeloconic sen- sillum, trichoid sensillum, coeloconic sensillum, e smaller basiconic 1 Received on June 20, 2017. em relação às sensilas antenais de H. irritans. Estes resul- Accepted for publication on August 3, 2017. tados fornecem sensillum. uma Levebase dimorfismomorfológica sexualpara futuras foi observado investi- 2 Setor de Artropodologia Médica e Veterinária, Universidade Federal de gações sobre o comportamento mediado pelo olfato desta Goiás, Cegraf/Editora UFG, Avenida Esperança s/n, Campus Samambaia, espécie, e poderão fomentar futuros estudos para desen- Goiânia, GO 74690-900, Brazil. *Corresponding author: freitasff.ufg@ volvimento de medidas alternativas de monitoramento e gmail.com controle de populações dessa mosca, com menor impacto. 3 Laboratório de Entomologia Médica, Centro de Pesquisas René Ra- chou, Fundação Oswaldo Cruz, Av. Augusto de Lima 1715, Belo Horizonte, TERMOS DE INDEXAÇÃO: Haematobia irritans, antena, ultraes- MG 30190-002, Brazil. CNPq Research Fellow. trutura, semioquímicos, sensilas olfatórias.

183 184 Fernando de Freitas Fernandes and Paulo Filemon Paolucci Pimenta

INTRODUCTION guiding the behaviour of hematophagous winged Haematobia irritans (Linnaeus, 1758) (Diptera: : (Zwiebel & Takken 2004, Mukabana et al. 2012). A promi- Muscinae), commonly known as the - sing and low environmental impact alternative would be red one of the main problems of husbandry in seve- the development of attractant semiochemicals, to be used ral countries. This ectoparasite occurs“horn commonly fly”, is considein Euro- in traps (Pomonis et al. 1993, Furukawa et al. 2002). The electrophysiological investigation of odor response using introduced into Brazil in 1978 in Roraima, and in the cur- the method of Single-Sensillum Recordings (SSR), impor- rentpe, Asia, days Africa, it is disseminated USA and American through Continent. all the Brazilian This fly states, was tant technique for semiochemicals development, becomes and also in Argentina, Paraguay and Uruguay. Males and fe- males of H. irritans are obligate blood-feeding ectoparasite, size of the antenna (Shanbhag et al. 1999). Therefore, the scanninga very difficult electronic task microscopyin , (SEM) due becomes to very an reduced impor-

40feeding times almost a day exclusively of bovine blood.on cattle, While but canfeeding, also parasitizethe “horn horses and sheep. These feed intermittently about 20- (Mitchelltant tool et for al. the 1999). identification and mapping of olfactory same puncture, in a pumping motion. Engorgement usually sensilla,In view based of these on facts, external the purpose morphologic of the characteristics present work requiresfly” inserts 4-10 and min withdraws but feeding its proboscis can take repeatedly as long as into 25-30 the min. This parasitism causes great stress to the cattle and ultrastructure of male and female of H. irritans, and to consequently considerable loss in their production (Honer localizewas to expand and morphofunctionally the knowledge regarding classify the the anatomy differents and & Gomes 1990). types of antennal sensilla of H. irritans, comparing with With infestations varying from 50 to 500 individuals already recognized ones in other insects. with special at- per bovine, H. irritans - per day suffers a blood cause loss of very about significant 2.6 liters losses. of blood It hasper vestigated.tention to olfactory sensilla. In addition, the existence of year,been andestimated consequently that a cowa reduction parasitized in milk by productionabout 500 fliesand sexual dimorphism on the antenna of this fly was also in weight gain. In Brazil the losses caused by this ectoparasite MATERIALS AND METHODS were estimated at about 865 million dollars per year, rela- - - gion of Brazil were studied in the present work. Males and fema- tle infested, created for slaughter and production of meat lesSpecimens without obtained defects or of mutilations the horn fly were population selected of withthe Midwest the aid ofRe a (Bianchinted to the etloss al. of2006). approximately In addition, 10% through of the its weight bites and of cat he- matophagy, this dipteran can transmit disease pathogens feces of naturally infested cattle, originating from ranches, and such as anaplasmosis, leucosis and black leg (Almeida et al. freestereoscope. of insecticidal The flies residues were forobtained at least in 45 laboratory days. starting from 2010). Just in the USA, losses were estimated at between Twenty samples of Haematobia irritans were selected, dissected (were separated from the rest of the body US$700 million and $1 billion, while an additional US$60 with a scalpel blade) and cleaned, as describedheads in Fernandes of both sexes et al. million is spent annually on insecticides to reduce horn (2004): particles of the rearing medium were carefully removed from the specimens using air jet. These were lightly agitated in sa- 2012, Benson et al. 2014). line for 1min to remove water-soluble impurities. This procedure fly populationsResistance of (Byford the H. irritans et al. 1992, to chemical Fitzpatrick insecticides, & Kaufman the main products used in its control, has been widely diagno- specimens were then placed in saline in an ultrasound apparatus sed in the Americas since South America (Argentina) to was repeated five times, changing the saline on each occasion. The- North America (Canada) (Mwangala & Galloway 1993). taraldehyde in 0.1M caccodylate buffer, pH 7.2, at room tempera- for 1h. After this, the samples were fixed overnight with 2.5% glu 2005, 2008). Afterwards, it was washed in buffer, and dehydrated ture and posfixed in 1% osmium tetroxide (Fernandes et al. 2004, regionsAlso in Brazil(Sabatini resistance et al. 2009, of this Barros fly toet al.these 2013). products The resis has- in an increasing series of concentrations of ethanol, alternating been verified, arriving at the Northeast, Midwest and South tance of Horn Fly to many of the insecticides has been de- three times. After this, the samples were dried by the critical point monstrated to occur through several known mechanisms, the concentrations of alcohol at 6h intervals, using 100% ethanol method device with CO2 (Fernandes et al. 2002). including target site insensitivity and thorough metabolic Whole heads, and also dissected antennae from other heads, - zún et al. 2008). Therefore, studies for the development of 10mm, brass), using conductive silver paint. There samples were detoxification of insecticides (Szalanski et al. 1995, Oyar- mountedwere mounted at different on the inclinations Jeol cylinder in SEMorder specimen to allow stubthe visualiza (Ø12.2 x- come appropriate. newOlfactory control andsensilla, monitoring also called measurements chemosensory, of this are fly intri be- ventral part, which usually remain hidden over the ventral sul- guing targets for the development of supplemental control tion of the entire external surface of the antennae, including its- strategies or harmful insects. This is due to the fact that cus of the face of the fly, when in its natural position. The sam these structures, in hematophagous Diptera, as well as JSMples 5600were thenJEOL sputtered scanning withelectron platinum microscope in K550X (Jeol Sputter Ltd., CoaterTokyo, in other parasites and vectors, are employed (Quorum Emitech, Ashford, UK) to be analyze the samples in the in the courtship and mating behavior, in the location of 2004, 2008). In the ultrastructural analysis, the morpho-function host (nutrients source), as well as in the selection of sui- typesJapan), of atH. anirritans accelerating voltage of 5.0-25Kv (Fernandes et al. table sites for oviposition. Field monitoring studies have morphology and observed by SEM (Mitchell et al. 1999, Hallberg indicated that olfactory system plays an important role in & Hansson 1999). sensilla were classified according their cuticle

Pesq. Vet. Bras. 38(1):183-188, janeiro 2018 Typology and distribution of antennal sensory organs of adult Haematobia irritans of the Midwest Region of Brazil 185

RESULTS Figure 1A shows the head of Haematobia irritans, with composed of two large dichoptic eyes without hairs and maxillary palps (mp). The scape (1st antennalmicrotrichia segment) type composed of numerous ommatidia, were observed in both and theby sensilla pedicel of(2nd long antennal bristle type, segment) of various of the sizes in both (Fig.1B). sexes - Figureof fly were 1B also covered shows by longsmaller bristles spinules sensillum, of arranged in a na, implanted beneath of the ptilineal suture, as well as a short median tuft (with about three bristles) on the scape, relativelysexes (Fig.1A). shorter It proboscis also shows (prb), its three-articulatedin contrast to the antenlarger and dispersed in greater numbers on the pedicel.

Fig.1. Eletromicrographs of males and females of Haematobia irritans. (A) Male head showing holoptic eyes, antennae (ant) and a relati- B) Scape (I) and pedicel (II) of the female antenna contai- ning long bristles (lb) and non-innervated spinules of microtrichia type (mct). Scale bar: 42 µm. (C vely(III) shorterwith arista proboscis pectinate (prb), (ars). in contrastScale bar: to 80 the µm. larger (D maxillary palps (mp). ( beside the base of the arista (ars). Scale bar: 15 µm. (E ) Frontalblunt view coeloconic of female sensillumflagellum (bcs) and grooved coeloconic ) Male flagellum with shallowF,G sensory pits (sp) containing distinct sensillar types, showing shallow sensory pits (sp), blunt coeloconic sensillum) Shallow (bcs), sensory and pitslarger in basiconicmale flagellum sensilla containing (lbs). Scale bar: 10 µm. (H) Surface microtrichas sensillum (gcs, (mct) with and “fingers”). larger basiconic Scale bar: sensillum 1.7 µm. ( (lbs),) Surface blunt coeloconic of male and sensillum female flagellum (bcs), grooved respectively, coelo- conic sensillum (gcs) and long grooved coeloconic I,J) Ventral surface of male of male flagellum showing sensillum (lgcs, with long “fingers”). Scale bar: 7 µm. ( flagellum containing clavate coeloconic sensilla (ccs), of double-tip (arrows) and single-tip subtypes (arrowhead). Scale bar: 2.0 μm, 1.5 μm and 1.5μm, respectively. Pesq. Vet. Bras. 38(1):183-188, janeiro 2018 186 Fernando de Freitas Fernandes and Paulo Filemon Paolucci Pimenta

In the antennal segments of H. irritans were found Table 1. Antennal sensilla of adults Haematobia irritans: spinules non-innervated spinules of microtrichia type and subtypes and distribution ten subtypes of sensilla: mechanosensory long bristles sen- Scape and pdicel Long bristles sensilla sillum, larger basiconic sensillum, blunt coeloconic sensil- lum, clavate coeloconic sensilla - single-tip and double-tip (inFlagellum both sexes) or clavateNon-innervated coeloconic sensilla, spinules double-tip of microtrichia subtype type subtypes -, grooved coeloconic sensillum, long grooved coe- funiculus clavate coeloconic sensilla, single-tip subtype loconic sensillum, trichoid sensillum, coeloconic sensillum and smaller basiconic sensillum (Fig.1). Table 1 shows the pattern distribution of the different (in both sexes) blunt coeloconic sensilla grooved coeloconic sensilla (with smaller “fingers”) subtypes of sensilla found in the antennal segments of H. long basiconic sensilla non-innervatedlong grooved coeloconic spinules sensillaof microtrichia (with larger type “fingers”) irritans. Arista trichoid sensilla - in male and female arista. Figure 2 A and B shows the grooved coeloconic sensil- basiconic sensilla - only in female arista coeloconic sensilla - only in female arista la of the “Horn fly” at higher ampliation. Figure 2C and D

Fig.2. Eletromicrographs of antennal sensilla of Haematobia irritans. (A B) female containing grooved coeloconic microtrichia type (mct). Scale bar: 0.8 µm in A and B. (C,D) Female arista, of the pectinate type and with) Surface woody of aspect,flagellum containing of male and trichoid ( (ts), coeloconic (cs), and basiconic (bs) sensillum sensilla. (gcs), Scale with bar: “fingers”, 2.5 µm in blunt C and coeloconic D. (bcs) and non-innervated spinules of shows the female arista, of the pectinate type and with ning mechanisms and closing of pores on the chemosen- woody aspect, containing trichoid (ts), coeloconic (cs), and sors tips, could also be understood through SEM (Van der basiconic (bs) sensilla. Wolk 1978). H. irritans was based DISCUSSION on its cuticular ultrastructure, comparing it with sensilla- The sensillary typology can be constituted on the basis of ry typesThe classification already recognized of the insensilla other insects, supported by morphological criteria, observed by scanning electron mi- studies of ultrastructure and electrophysiology. In this way, croscopy (SEM), such as: distribution; length; grooves on for the analysis of its ultrastructure, the sensilla may be re- the hairs; presence and location of pore(s), etc. Some ope- lated to different types of functions, such as chemoreceptor,

Pesq. Vet. Bras. 38(1):183-188, janeiro 2018 Typology and distribution of antennal sensory organs of adult Haematobia irritans of the Midwest Region of Brazil 187 hygroreceptor, thermoreceptor or mechanoreceptor (Hall- stalk, emerging from a pit and presenting an apical dilation berg & Hansson 1999, Mitchell et al. 1999, Fernandes et al. (bulbous tip). For this reason, it was denominated clavate 2002, 2005, 2008). coeloconic sensillum (Fig. 1I and J). It also presented wall The scape (1st antennal segment) and the pedicel (2nd pores, homogeneously distributed on the surface. Sensilla, presenting wall pores and similar to the clavate by smaller spinules of microtrichia type and by sensilla of coeloconic sensillum and the blunt coeloconic sensillum ob- longantennal bristle segment) type, of variousof the in sizes. both Microtrichias sexes of fly were, as observed covered in H. irritans (Fig.1B), constitute the most abundant pilosi- Stomoxys calcitrans (Linn., 1758) (Diptera: ty type that covers the entire antennal articles of different served in the present work were also previously identified species of Muscomorpha, being frequently designated by inZhang “stable et al. fly” 2013). non-innervated spinules, spines, or trichomes (Shanbhag Muscidae: Stomoxydinae) (Tangtrakulwanich et al. 2011,- et al. 1999, Stocker 2001, Fernandes et al. 2002, 2004). ce of a sensillum with characteristics of sensila olfactory As described here in H. irritans (Fig.1B), mechanosen- in theThe aristae present of study Muscomorpha reveals for - theThis first was time evidenced the existen only sory long bristles sensillum had been previously obser- Dermatobia hominis (L. Jr., 1781) (Diptera: type basiconic and coeloconic type (Fig. 2C and D). Oestridae: Cuterebrinae)17 and Cochliomyia hominivorax in femalesThe trichoid of the sensilla species observedand classified in the as presentsensillum work of the in ved(Coquerel, in the flies1858) (Diptera: : Chrysomyinae) (Fernandes et al. 2004). The long bristles sensilla are tri- similar to the sensilla previously observed in the aristae of choid sensilla, with articulated base, no surface pores, and the in male and female aristaD. hominis of horn, C. hominivorax,fly (Fig. 2C and S. calci D) is- mechanosensory function (Chapman 1991). This sensillum trans and F. hirticeps (Fernandes et al. 2002, 2004; Wang type can be present in several parts of the body of the in- etothers al. 2012) flies,. suchThe absenceas for of pores in this sensilla suggests sects (Fernandes & Linardi 2002) and have frequently been that this types of sensillum may function as mechanore- ceptors. light microscopy observations (Chapman 1991). usedThe in taxonomiclong bristles keys are for mechanosensory species identification, sensilla based that reon- observed in H. irritans (Table 1). Analyses showed that the ceive stimuli originating from contact with surfaces, air sensillaAn slight have sexual a similar dimorphism distribution in the on thesensilla antennae patterns of male was currents or sound waves. Each cuticular projection is as- and female H. irritans, but present a few differences, in re- sociated with a single neurone. Various types of mechano- lation to the sensillary types, described along this manus- receptors also function as propioceptors, that is, they de- cript. This subtle differences probably is due to the need to tect mechanical stimuli produced by the antenna itself. The process different types of stimuli received during the life mechanoreceptors are fundamental, because they provide cycle, involved in mating and oviposition e.g. Differences information about position, degree of distension of parts between the antennal sensilla of males and females have D. such as those involved in ventilation (Chapman 1991, Ca- melanogaster (Shanbhag et al. 1999), D. taláof the 1998). body, monitoring of flight and rhythmic movements hominisbeen also (Fernandes noted in others et al. Muscomorpha,2002), “New World as in “Fruit-fly”Screwworm Sensilla on the antennal funiculus similar to the long ba- C. hominivorax (Fernandes et al. 2004),“American as well ” as in Ne - siconic sensillum (Fig.1F-H) and to the grooved coeloconic Lutzomyia longipalpis (Lutz and sensilla (Fig.1E and H), largest and smallest, observed in fly”Neiva, 1912) (Diptera: : Plebotominae) (Fer- this work, was also previously evidenced in me- matocera,nandes et al.as 2008).in “Sand We fly” believe that the observation of few lanogaster (Fallén, 1823) (Diptera: : Droso- differences between the distribution of sensillary types of philinae). They all present wall pores, in different structure and arrangement, allowing access of volatile substances, - and therefore possessing an olfactory function (Shanbhag dingmales mainly and females on bovine is due blood. to theDifferently, fact that in both the Dipterasexes of spe the- et al. 1999, Stocker 2001, Fernandes et al. 2004). The groo- cies“horn in fly” which have the the feeding same feedingstimuli (andhabits, the the food same itself) hosts, are fee di- ved coeloconic sensilla was shown to be an elevation, emer- ging from a pit, presenting longitudinal grooves and appa- been observed in relation to the patterns of distribution fferent between the sexes, a greater sexual dimorphism has C and D). Sensilla, similar to this grooved coeloconic sensilla rently formed by “cuticular fingers-like projections”Manduca (Fig.2sexta notand bitesensory men types. or . As an example may be mentioned “sand - flies”, in which only females feed on blood, that is, males do sionwere scanning also evidenced electron in microscopy, the “sphinx very moth”, small cuticular po- CONCLUSIONS res(Linn., could 1763) be found (Lepidoptera: at the bottom Sphingidae). of each groove, Using connectingfield-emis This study provides new data on the typology and sen- the inside of the sensillum via cuticular spoke channels ra- sillary distribution of antennal sensilla of Haematobia ther than pore tubules (Shields & Hildebrand 2001). irritans There was also a subtype of coeloconic sensillum, in sensilla. in The the present aristae of study Muscomorpha. reveals for the first time the blunt coeloconic sen- existenceThe presence of a sensillum of different with sensorial characteristics subtypes of olfactorywith ol- sillumthe flagellum (Fig. 1G-H). “horny Another fly” of subtype both sexes, of coeloconic with wall sensillum pores, - wasbut presentingalso observed a blunted in the apex, present called work, as a cylindrical gellum and arista) of H. irritans indicates that the olfaction factory sensory characteristics found in the antennae (fla

Pesq. Vet. Bras. 38(1):183-188, janeiro 2018 188 Fernando de Freitas Fernandes and Paulo Filemon Paolucci Pimenta should play an important role in this species behavior and communication. secondary acetates and a methyl-branched ketone as possible can- Furukawa A., Shibata C. & Mori K. 2002. Syntheses of four methyl-branched The results of this study could assist future electrophy- Cochliomyia hominivorax. Biosci. Biotechnol. Biochem. 66:1164-1169. siological analysis to identify chemosensors, combined didates for the female pheromone of the screwworm fly, Hallberg E. & Hansson B. 1999. Arthropod sensilla: morphology and phy- logenetic considerations. Microsc. Res. Tech. 47:428-439. Such studies would in turn contribute to the develo- Honer M.R. & Gomes A. 1990. O manejo integrado de mosca-dos-chifres, pmentwith behavioral of attractants studies semiochemicals to determine their for monitoringsignificance. and berne e carrapatos em gado de corte. Embrapa Gado de Corte, Campo Grande, MS. 60p. controlAcknowledgements.- of the “horn This fly”. study was supported by the Conselho Nacio- involved in gustation. Microsc. Res. Tech. 47:401-415. - Mitchell B.K., Itagaki H. & Rivet M.P. 1999. Peripheral and central structure Van Loon J.J. & Takken W. 2012. A novel synthetic odorant blend for nal de Desenvolvimento Científico e Tecnológico (CNPq), Brazilian govern Fundação de Amparo a Pesquisas do Estado de Minas Gerais (FAPEMIG); Mukabanatrapping W.R.,of malaria Mweresa and other C.K., Otieno African B., Omusula species. P., Smallegange J. Chem. Ecol. R.C., ment entity which promotes Scientific and Technological Development; to 38:235-244. Ciência e Tecnologia (SECTEC), and to Fundação Oswaldo Cruz (Fiocruz). to Programa de Apoio a Núcleos de Excelência (PRONEX), Secretaria de Mwangala F.S. & Galloway T.D. 1993. Dynamics of pyrethroid resistance Haematobia irritans (L.) (Diptera: Muscidae), popula- Conflict of interest statement.- The authors have no competing inte- tions on tagged and untagged cattle in Manitoba. Can. Entomol. 125: rests. 839-845.in the horn fly, Oyarzún M.P., Quiroz A. & Birkett M.A. 2008. Insecticide resistance in REFERENCES Almeida F.A., Basso F.C., Seno M.C.Z. & Valério Filho W.V. 2010. Population 202. Haematobia irritans) on Guzera cattle breed the horn fly: alternative control strategies. Med. Vet. Entomol. 22:188- and crossbred in Selvíria, MS. Semina, Ciên. Agrárias 31:157-162. dynamics of the horn fly ( Pomonis J.G., Hammak L. &Cochiomyia Hakk H. 1993. hominivorax. Identification J. Chem. of compounds Ecol. 19:985- in & Gonzalez R. 2013. Mechanisms of pyrethroid resistance in Haemato- 1008.an HPLC fraction from female extracts thar elicit mating responses in Barros A.T.M., Schumaker T.T.S., Koller W.W., Klafke G.M., Albuquerque T.A. male screwworm flies, bia irritans (Muscidae) from Mato Grosso do Sul state, Brazil. 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