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Description of Dichelacera (Dichelacera)

walteri n. sp. (Diptera: Tabanidae) with


a Key to Related Species in the Subgenus
Dichelacera Macquart

R R Guimarães, I S Gorayeb, R
Rodrigues-Guimarães, G S Seppa & R W
Carvalho

Neotropical Entomology

ISSN 1519-566X

Neotrop Entomol
DOI 10.1007/s13744-015-0311-8

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Author's personal copy
Neotrop Entomol
DOI 10.1007/s13744-015-0311-8

SYSTEMATICS, MORPHOLOGY AND PHYSIOLOGY

Description of Dichelacera (Dichelacera) walteri n. sp. (Diptera:


Tabanidae) with a Key to Related Species in the Subgenus
Dichelacera Macquart

RR GUIMARÃES1,2, IS GORAYEB3, R RODRIGUES-GUIMARÃES4,5, GS SEPPA1, RW CARVALHO1


1
Escola Nacional de Saúde Pública Sérgio Arouca, Fiocruz, Rio de Janeiro, RJ, Brasil
2
Centro de Educação e Pesquisas em Medicina Ambiental, CEMA, Nilópolis, RJ, Brasil
3
Museu Paraense Emílio Goeldi, Ministério da Ciência Tecnologia e Inovação, Belém, PA, Brasil
4
Univ de Barra Mansa Barra Mansa, Barra Mansa, RJ, Brasil
5
Univ Estácio de Sá, Rio de Janeiro, RJ, Brasil

Keywords Abstract
Atlantic island, horse fly, Neotropical, Dichelacera (Dichelacera) walteri Guimarães, Gorayeb & Rodrigues-
sandbank forest, tabanid Guimarães n. sp. is described from female specimens collected in
Correspondence Marambaia Island, located in Mangaratiba County, state of Rio de Janeiro,
RR Guimarães, Centro de Educação Brazil. The characterization of the species was based in the following char-
e Pesquisas em Medicina Ambiental, Av. acters: a medium-sized species, more sclerotized than others in the sub-
Dr. Getúlio Vargas, 1797/2, CEP 26525-
023 Olinda, Nilópolis, RJ, Brasil; genus Dichelacera Macquart, the second segment of palp with dark setae
ronaldrguimaraes@gmail.com and longer than the third antennal segment, a brown scutum with
Edited by Roberto A Zucchi – ESALQ/USP pruinescence on the anterior half and posterior edges with white tonality,
yellow dorsum of abdomen with the last three segments brown, white-
Received 21 March 2015 and accepted 8 yellowish venter with yellow setae, narrow frons with dark brown callus,
June 2015
extending just beyond a ridge in the middle of the frons, vertex with ocelli,
* Sociedade Entomológica do Brasil 2015 hyaline wings with three large black bands, and tricolored legs.

Introduction vectors of various etiologic agents among the helminthes,


virus, bacteria, and protozoan (Krinsky 1976, Foil 1989, Foil
Tabanids are the largest bloodsucking Diptera with robust & Issel 1991, Luz-Alves et al 2007, Turcatel et al 2007).
bodies, reaching up to 2.5 cm, belonging to the family The genus Dichelacera Macquart is distributed through-
Tabanidae Latreille. Popularly, the flies of this family are out the Neotropical region, and the majority of the species
known as horse flies and are considered a pest in several inhabit Mexico, Antilles, and Brazil. This genus is represented
regions of the world, attacking humans, domestic, and wild by a group of structurally heterogeneous species, and
animals, and are noticeable in human areas such as settle- regarding the taxonomy and systematics, the coloration
ments, farms, and pastures, especially during the drier sea- characteristics as reported by Fairchild & Philip (1960) are
sons. As ectoparasites, the horse flies are known worldwide generally adopted. The type species is Dichelacera cervicornis
for their painful bite, sometimes known to cause allergies (Fabricius), which was described from specimens collected in
and severe systemic reactions involving generalized urticaria, Guyana. The following features determine the genus
angioedema on the face and, sometimes, on all body, ab- Dichelacera: frontal callus usually as broad as the frons, eyes
dominal pain, nausea, bronchial constriction, dyspnea, and without setae, one or two greenish eye bands, and generally
anaphylactic shock (Frazier 1973, Wilbur & Evans 1975, completely sclerotized labella. Coscarón & Papavero (2009)
Hemmer et al 1998, Quercia et al 2005, Klotz et al 2009). includes 80 species in the genus Dichelacera, grouped into
Furthermore, they have also been mechanical and biological five subgenera: (i) Desmatochelacera Fairchild with two
Author's personal copy
Guimarães et al

species, (ii) Dichelacera representing the majority (62) of the rank correlation coefficient (rs) among the flies with temper-
species described, (iii) Idiochelacera Fairchild with only one ature, rainfall, and humidity using the Biostat 5.3 program
species, (iv) Nothocanthocera Fairchild with 12 species, and (Ayres et al 2007). The statistical significance was set at a p
(v) Orthostyloceras Lutz with three species. Additional species value of <0.05.
were added to the subgenus Dichelacera, including Captures of horse flies were authorized by the Brazilian
Dichelacera corumbaensis Barros & Gorayeb and Dichelacera Institute of Environment and Natural Renewable Resources,
gemmae Limeira-de-Oliveira, Gorayeb & Henriques in the sub- SISBIO-IBAMA no. 33382-1.
genus Dichelacera (Henriques et al 2012).
Dichelacera is the largest subgenus and includes species
characterized by fully sclerotized labella, eyes often with dark Results
diagonal bands, wings with one dark diagonal band plus
others in various forms, and a square-like callus as wide as Genus Dichelacera Macquart, 1838
the frons (Fairchild & Philip 1960). Of the current 64 species Subgenus Dichelacera Macquart, 1838
recognized in this subgenus, four are endemic to the State of Type-species, D. cervicornis (Fabricius, 1805)
Rio de Janeiro, including Dichelacera alcicornis (Wiedemann), Dichelacera (Dichelacera) walteri Guimarães, Gorayeb &
Dichelacera antunesi Fairchild & Philips, Dichelacera januarii Rodrigues-Guimarães n. sp. (Figs 2–12)
(Wiedemann), and this new species Dichelacera walteri n.
sp., described in this manuscript. Moreover, some ecological Diagnosis. Species similar to D. cervicornis and D. alcicornis.
aspects of this new species are discussed, and in addition, a Medium-sized species (length 10–12.4 mm), more sclerotized
key for adults of morphologically related species of subgenus than others in the subgenus Dichelacera. Palp longer than the
Dichelacera is included in order to compare with the new third antennal segment, second segment with dark setae.
species described now. Brown scutum with pruinose anterior half and posterior edges
with white tonality. Yellow dorsum of abdomen with the
last three segments brown; white-yellowish venter with
Material and Methods yellow setae; narrow frons with dark brown callus, extend-
ing just beyond a ridge in the middle of the frons, vertex
In order to know the fauna and bionomics aspects of horse with ocelli. Hyaline wings with three large black bands.
flies, during the year of 2013, four canopy traps were placed Tricolored legs.
in Armação, Marambaia Island, Mangaratiba County, state of
Rio de Janeiro, Brazil (23°02′54″S, 43°57′07″W), at sea level, Description of the female. Body length 12.4 mm (mean
about 86 km east of Rio de Janeiro City and 12 km from the 11.1 mm; range of variation 10.0 to 12.4 mm, no.=14), height
continental coast (Fig 1). Several specimens of the species of frons 2.0 mm (average 1.7 mm), width of frons at vertex
described herein were also captured manually with entomo- 0.5 mm (mean 0.4 mm), width of the frons at the base
logical nets. Afterward, the horse flies were identified at the 0.5 mm (mean 0.4 mm), and frontal index 4.0 (mean 3.8,
Department of Biological Science of Sérgio Arouca National range of variation from 3.3 to 4.2) (Figs 2–4 and 8).
Public Health School (ENSP)-FIOCRUZ, Rio de Janeiro, and the
new species was confirmed at Museum Paraense Emílio Head. Glabrous eyes with two green bands on dark brown
Goeldi (MPEG), Belém, Brazil. background to black, as in Fig 5. Brown frons with white-
The description and measurements were based on the yellowish pruinescence and sparse brown setae; vertex with
holotype considering the average range of variation for spec- black setae and discrete brown sclerotized subtriangular pro-
imens of the typical series. Insects were examined and mea- tuberance, smooth and shiny with ocelli; large slightly inflat-
sured with a stereoscopic microscope Zeiss Stemi SV 11 ed frontal callus, sclerotized, brown, smooth and shiny, as
coupled with a camera lucida and photographed with a wide as the frons, square with upper ridge extending to half
Leica M205 C coupled with Leica DFC 295 camera with the height of the frons; yellow subcallus with bright yellow
“Leica Application Suite” (LAS V3.6) software to process dig- pruinescence (Fig 8). Antenna with yellowish-brown scape
ital images. The photos were taken of the holotype, and the and pedicel with black setae; third segment shorter than
genitalia was prepared from a paratype and kept in glycerin palpi; reddish brown basal plate with dorsal proximal black
in a microtube attached beneath the specimen. The drawings setae; curved elongated spine, dark brown with black setae,
of the genitalia were made by I. S. Gorayeb (EGM). The ter- reaching the second flagellomere; black style with the same
minology complies with Burger (2009) and Cumming & length as the basal plate, with black setae (Fig 6).
Wood (2009). Frontoclypeus slightly inflated with white pruinescence and
Data on richness of horse fly species and absolute abun- sparse fine setae; white-yellowish parafacialia with light yel-
dance of specimens were used to calculate the Spearman’s low setae and pruinescence; gena with pruinescence and
Author's personal copy
Dichelacera walteri: a New Tabanid Species from Brazil

Fig 1 Geographic location (a) and


site of collection (b) of tabanids
on Marambaia Island,
Mangaratiba, state of Rio de
Janeiro, Brazil (Sources: Fig 1a
Souza et al 2007. Available at
http://www.scielo.br/img/
revistas/abb/v21n1/06f1.gif.
Accessed 12 November 2014; Fig
1b Google Maps. Available at
www.google.com.br/maps/@23.
0316476,43.9261133,19073m/
data=!3m1!1e3?hl=pt-BR.
Accessed 12 November 2014).

both white-yellowish and black setae (Fig 5). Slender yellow short black setae (Fig 5). Occiput with brown integument
palp with yellow pruinescence, first segment with both covered with white-yellowish pruinescence and setae.
white-yellowish and light brown setae; second segment lon- Thorax. Brown and white mesonotum with black setae;
ger than the antennal flagellum, with black setae (Fig 7). yellow setae on anterior margin, on notopleura and post-alar
Proboscis and labella fully chitinized, black, shiny, with lobe. Prescutellum with brown-yellowish integument covered

Figs 2–4 Dichelacera walteri n.


sp. 2 Dorsal view of the body
(scale bar=5 mm). 3 Lateral view
of the body (scale bar=5 mm). 4
Wing (scale bar=5 mm).
Author's personal copy
Guimarães et al

Figs 5–8 Dichelacera walteri n.


sp. 5 Lateral view of head,
banded eye, antenna, palpus,
and proboscis (scale bar=
2.0 mm). 6 Antenna (scale bar=
1.0 mm). 7 Palp (scale bar=
1.0 mm). 8 Frons (scale bar=
1.0 mm).

with white pruinescence and black setae, with yellow setae on subcostal cells, and pterostigma all brown; anterior half of the
the anterior margin, on post-pronotal lobe and notopleura. radial basal cell, brown; brown interveinal basal area; anterior
Scutum with brown integument covered with brown part of alula, brown; three large black bands: (i) distal and
pruinescence and black setae, yellow setae on post-alar lobe, anterior portion of the wing, covering the distal third of r1,
on posterior margin of the scutum, and on pre-scutellar lobe. the end of the R1 vein, the distal portion of the r2+3 cell (except
Dark brown scutellum with black setae on the edges, with the apex), and the basal half of the r4 cell; (ii) the second band
white-yellowish posterior border, ventral surface, and covering the center of the r5 cell, the distal third of the discal
pruinescence. Pleura, pleuron, and coxae with yellowish integ- cell, the proximal part of the m1 and m2 cells, most of the distal
ument, pruinescence and setae, black setae on distal end of half of the m3 cell (excluding the anterior tip), and both the
the hind coxae. Wings: length 10.7 mm and width 3.5 mm (alar distal and anterior part of the cua1 cell; and (iii) the third band,
index 3.0), dark brown tegula with setae of same color and more proximal and posterior, covering the distal half of the
dark brown veins, hyaline with black spots; costal basal, costal, cup cell (except the base) and the distal half of the a1 cell
(except the area close to the posterior border) (Fig 4).
Blackish-brown upper calyptra with a fringe of short black
setae on the edge; brown-yellowish lower calyptra with yellow
fringe of short setae; blackish-brown subalar sclerite process
with white tuft of long setae. Tricolored legs, white-yellowish
coxae with white-yellowish pruinescence and setae; anterior
coxae with white-yellowish and black setae on the distal por-
tion; trochanters with black setae; brown-yellowish anterior
femur with black setae; brown-yellowish medium femur with
yellow and black sparse setae concentrated on the distal third;
yellowish-brown hind femur with black setae and yellow
sparse setae more concentrated on the basal half; anterior
and medium tibiae, basal half integument light yellow and
distal half brown; dark brown hind tibiae and tarsi integument
and setae; dark brown to black tarsi with black setae.
Abdomen. Tergite 1 with light yellow integument and yellow
shiny setae; second to fourth tergites with shiny black yellow
setae on lateral and posterior half; fifth to seventh tergites
darker with black setae; sternites with light yellow integument
with shiny yellow setae, with brown setae at the lateral edges
of the fifth and sixth sternites and on the entire seventh ster-
nites (Figs 2 and 3). Terminalia. Cercus with posterior edge
Figs 9–12 Dichelacera walteri n. sp. 9 Tenth tergite and cercus (scale
convex; 10th tergite twice wider than long, eighth sternite with
bar=0.5 mm). 10 Genital fork (scale bar=0.3 mm). 11 Spermatheca (scale
bar=0.3 mm); 12 Eighth sternite and respective gonapophysis (scale round lateral edges and gonapophysis with posterior edge in
bar=0.5 mm). two convex angles. The genital furca has the upper edge
Author's personal copy
Dichelacera walteri: a New Tabanid Species from Brazil

areas of the integument, being brown to brownish-


yellow and yellow to ocher. Setae on the frons ranging
from absent in some specimens to small yellowish setae,
white in the center, and others with white-yellowish and
black setae. Shiny clear setae of the mesonotum more or
less numerous in the examined specimens, easily lost and
some specimens with bare areas. Setae of notopleura all
dark, appearing yellowish-white depending upon the light,
in some specimens all yellowish white. Black setae on the
distal coxae area absent in some specimens, especially on
the fore and mid coxae. Shiny yellow setae on tergites
easily lost on some specimens.

Distribution. Brazil, state of Rio de Janeiro.

Etymology. The species name is a tribute (in memoriam) to


Mr. Walter Rodrigues Guimarães, father of Ronald Rodrigues
Guimarães and Roney Rodrigues Guimarães.

Examined material. Holotype ♀; Brazil, Rio de Janeiro,


Mangaratiba County, Marambaia Island, Armação, 23°
02.54′ S and 43° 57.07′ W, 14-X-2013, entomological net,
forest area of sandbanks, RR Guimarães, RR Guimarães-
Junior and JAS Santana leg., pinned, Entomological
Collection of Instituto Oswaldo Cruz CEIOC-FIOCRUZ,
CEIOC-2693, Rio de Janeiro, Brazil. Paratypes. 13 ♀, same
as holotype. 2 ♀ 15-IX-2012, 4 ♀ 4-5-X-2013, 1 ♀ 14-X-2013,
2♀ 27-X-2013, Guimarães RR leg., CEIOC; 1 ♀ 15-IX-2012,
1 ♀ 14-X-2013, RR Guimarães leg., Museum of Zoology of
University of São Paulo (MZUSP); 1 ♀ 14-X-2013, 1 ♀ 4-5-XII-
2013, RR Guimarães leg., Museu Paraense Emilio Goeldi
(MPEG).

Richness and bionomic remarks

The Tabanidae richness found in coastal zone of the


Marambaia Island, characterized as forest sandbank en-
Fig 13 Monthly averages temperatures (a), humidity (b), monthly cumu-
vironment, was of 18 species and a total of 2102 spec-
lative rainfall (c) and total of specimens of Dichelacera walteri sp. n., imens. D. walteri n. sp. represents the fifth most abun-
collected by ‘canopy’ trap in 2013, Marambaia Island, state of Rio de dant species of horse flies of the island, totalizing 24
Janeiro, Brazil. number of collected specimens; climatic specimens captured (1.1%). D. walteri sp. n. emerges
factor variation. Source: INMET – Instituto Nacional de Meteorologia – Rio
de Janeiro (Estação-Marambaia-A602).
from September to December, in the spring to begin-
ning of the summer, and its seasonal variation shows a
weak negative correlation with temperature (rs=−0.15,
p>0.005), which can be difficult to interpret, because
evenly curved with narrow side flaps, a ventral margin with the species is being recorded as occurring in forest
deep invagination and spermathecal ducts with broad cup-like area of sandbank, which is expected to be related to
expansions, and the spermatheca being fusiform (Fig 11). higher temperatures. This fact may indicate that the
species requires a narrow temperature range for activ-
Male. Unknown. ity. Seasonal variation also demonstrated weak nega-
tive correlation with rainfall (rs = −0.48, p > 0.05) and
Variations. Color variations exist in several areas of the weak positive correlation with the humidity (rs= 0.13,
body, such as the wing veins, the stigma, and some p>0.05) (Fig 13 a, b, c).
Author's personal copy
Guimarães et al

Key to D. walteri n. sp. and similar species of subgenus new species were also compared with those D. antunesi,
Dichelacera recorded in the state of Rio de Janeiro from the collection of the EGM, which differed from the
new species by presenting third antennal segment longer
1. Third antennal segment longer than palpi.....................2 than palpi, the thorax and abdomen broader, general ap-
1′. Third antennal segment shorter than palpi...................4 pearance of a lighter body, yellow anterior pollinose
2. Palpi with white setae; submarginal cell fully dark; mesonotum, and costal cell and stigma black (Figs 2 and 4).
anterior half of mesonotum entirely pale-haired (spe- In the CEIOC, the new species was compared with voucher
cies from Amazonic region)............................................. specimens of D. alcicornis and D. cervicornis, demonstrating
.....................................................D. cervicornis Fabricius the existence of several differences between them.
2′. Palpi with yellowish setae..............................................3 According to Lutz (1915), D. alcicornis is not as light as the
3. Mesonotum with transverse interalar band moderately new species, displaying a yellow color. The frontal index is 3.5
large, pollinose brown and strongly marked; anal cell instead of 3.8 in D. walteri. The frontal callus is light brown
with small dark spot..................D. januari (Wiedemann) and slightly sclerotized, and the scutum features two clear
3′. Mesonotum with transverse interalar band generally bands between the transverse sutures, other than the new
indistinct; anal cell over one-third dark................... species. The scutellum is yellow with an ocher or brown spot
.......................................… D. antunesi Fairchild & Philip on the anterior half, and the second to fourth abdominal
4 Antennal basal plate pale yellowish, with blackish tip tergites possess a distinct, dark brown anterior marginal
and style; scutellum all dark.............. D. intermedia Lutz transversal band. All spots on the wings of D. alcicornis are
4′. Antennal basal plate largely black; scutellum otherwise.... ocher and semitransparent, while on the described species,
..................................................................................................5 they are black and opaque, the transversal spot of anal cells
5. Palpi slender, light brown scutellum, all abdominal seg- being much higher. The voucher specimens of D. alcicornis
ments dark, except the first, pale yellow, without a dis- originate from the Atlantic forest and savannah areas in the
tinct interalar transversal band.............................................. States of Santa Catarina, Paraná, Mato Grosso, Minas Gerais,
.......................................................D. alcicornis (Wiedmann) and Rio de Janeiro.
5′ Palpi more robust proximal half; dark scutellum with Lutz (1915) also pointed out that D. cervicornis has a light
black setae at edges; abdominal tergites 1, 2, 3, and 4 brown callus with a small frontal crest and palpi with clear
yellowish, and the remaining ones dark; with a distinct setae, while the new species has a long frontal crest and palpi
interalar transverse band…..................…D. walteri n. sp. with black setae. Furthermore, D. cervicornis has the third
antennal segment longer than palpi, a light yellow scutum
with yellow setae with a pronounced blackish brown broad
Discussion band with black setae inserted between the wings. The pos-
terior edge of the alar fascia has wider margins, the anal patch
Tabanid fauna diversity and richness studies in Marambaia is restricted to the distal half of the cubital cell, and the ventral
Island were initiated in 1982, when some specimens of the and dorsal abdominal tergites of D. cervicornis are much
species described herein were collected and sent to Dr. GB darker than those of the new species, which has wider wings.
Fairchild who reported that the species resembled The Brazilian Atlantic forest is considered one of the eco-
D. cervicornis, an Amazonian species structurally similar to systems with the highest biodiversity and levels of endemism
D. alcicornis, suggesting the possibility of an undescribed in the planet (Myers et al 2000). There is a remarkable var-
species. In recent studies in the same area during the years of iation in local diversity of areas along its extension. Although
2012 and 2013, new specimens of several species were not many in-depth and specific studies have been conducted,
captured, including new samples of that presumably the information available for some groups of vertebrates and
undescribed species. Therefore, this material was sent to invertebrates is consistent with the idea that in Southeast
Museu Paraense Emílio Goeldi, and this time, it was examined Brazil, more precisely, in the latitudes of the State of Rio de
by Dr. IS Gorayeb, who agreed with the previous diagnosis. Janeiro, there is a high level of diversity of species for several
In the key of Fairchild & Philip (1960) for the Dichelacera groups (Rocha et al 2004, Oliveira et al 2010). Therefore, the
subgenus, the new species has the third antennal segment description of a new species incorporating the inventory of
shorter than palpi which is similar to Dichelacera intermedia the insects in the Atlantic rainforest biodiversity is very im-
Lutz and D. alcicornis and differing from the first species due portant, due to constant losses generated by deforestation
to the absence of the blackish stripe in the mesothoracic disk for wood extraction, pasture, and agriculture.
and the presence of black setae in the notopleuron. It also
differs from second species, D. intermedia, in the third an-
Acknowledgments The authors are sincerely thankful to Márcio
tennal segment staining and the absence of the aforemen- Eduardo Félix and Danielle Cerri from the Entomological Collection of
tioned blackish stripe on the thorax. The specimens of the the Oswaldo Cruz Institute for their help and kindness during our study
Author's personal copy
Dichelacera walteri: a New Tabanid Species from Brazil

to compare the new species with the other voucher specimens in the Henriques AL, Krolow TK, Rafael JA (2012) Corrections and additions to
horse fly collection. The authors are also thankful to the staff of the Catalogue of Neotropical Diptera (Tabanidae) of Coscarón and
Brazilian Navy for the permission and contribution to develop this study Papavero (2009). Rev Bras Entomol 56:277–280. doi:10.1590/
on Marambaia Island. English review and revision by Mitchell Raymond S0085-56262012005000042
Lishon, native of Chicago, IL, USA, UCLA 1969. The study had financial Klotz JH, Klotz SA, Pinnas JL (2009) Stings with animal bites and anaphy-
support by Sérgio Arouca National Public Health School, Post- lactic potential. J Emerg Med 36:148–156. doi:10.1016/j.jemermed.
Graduation Program (CAPES Process Scholarship no. 1383383). 2007.06.018
Krinsky WL (1976) Animal disease agents transmitted by horse flies and
deer flies (Diptera: Tabanidae). J Med Entomol 13:225–275. doi:10.
1093/jmedent/13.3.225
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