MORPHOLOGY, SYSTEMATICS, EVOLUTION
A New Species of Tunga (Siphonaptera: Tungidae) From Brazil With a
Key to the Adult Species and Neosomes
DANIEL M. DE AVELAR,1 ARÍCIO X. LINHARES,2
AND
PEDRO M. LINARDI1,3
J. Med. Entomol. 49(1): 23Ð28 (2012); DOI: http://dx.doi.org/10.1603/ME11111
ABSTRACT Tunga bossii new species of tungid sand ßea belonging to the caecata group is described
with illustrations of the adult female, parasitizing the wild rodent Delomys dorsalis (Hensel) from
Brazilian Atlantic Forest. Tunga bossii differs from the ten other known species of Tunginae by the
size of the Þrst segment of the maxillary palp and the presence of two bristles at the base of the maxilla.
Tunga bossii also can be differentiated from other species of the T. caecata group by the eye
morphology. A key to the adult species and neosomes of the genus Tunga also is included.
KEY WORDS Siphonaptera, Tungidae, Tunga bossii sp. nov., sand ßea, neosome
Tunga Jarocki, 1838, is the most specialized genus of
the order Siphonaptera because adult females penetrate into the skin of their hosts, causing serious ectoparasitosis and harmful infections (Hopkins and
Rothschild 1953, Linardi and Guimarães 2000,
Pampiglione et al. 2009). After mating, gravid females
undergo hypertrophy, becoming a neosome 5Ð13 mm
in size, deÞned as an entire organism of signiÞcant
enlargement formed of new morphological structure,
accompanied by growth of new tissue, during a single
active stadium of an invertebrate (Audy et al. 1972,
Rothschild 1992).
Currently the genus includes 10 species of sand
ßeas, parasitizing armadillos, anteaters, rodents, pigs,
human and other domestic animals, distributed in the
New World tropics, Sub-Saharan Africa, China, and
Japan (Lewis 1998).
According to Barnes and Radovsky (1969) the center of distribution of the genus Tunga is within the
Neotropical region, considering that of the 10 described species, six are restricted to South America
and another, Tunga penetrans (L., 1758), exhibits a
wide Neotropical distribution, being now permanently established in much of tropical Africa (Lewis
1998).
Based on morphology and host afÞnities, Smit
(1962) divided Tunga into two species groups, penetrans and caecata. Currently, the penetrans group includes T. penetrans; T. trimamillata Pampiglione, Trentini, Fioravanti, Onore, and Rivasi, 2002 (Ecuador);
and three Brazilian species: T. travassosi Pinto and
Dreyfus, 1927, T. bondari Wagner, 1932 and T. terasma
Jordan, 1937, all of them associated primarily with
1
Departamento de Parasitologia, Instituto de Ciências Biológicas
da Universidade Federal de Minas Gerais, Caixa Postal 486, Avenida
Antônio Carlos, 6627, Campus UFMG, Minas Gerais, 31270-901, Brazil.
2 Departamento de Parasitologia, Instituto de Biologia, Universidade Estadual de Campinas.
3 Corresponding author, e-mail: [email protected].
edentates. The caecata group, found exclusively on
rodents, includes T. caecata (Enderlein 1901) (Brazil),
T. caecigena Jordan and Rothschild, 1921 (China and
Japan); T. callida Li & Chin, 1957 (China); T. libis
Smit, 1962 (Ecuador); and T. monositus Barnes and
Radovsky, 1969 (Mexico and United States). Another
proposal that includes the two Chinese species in a
distinct subgenus (Brevidigita) was presented by
Wang (1976).
However, in spite of morphological differences between the groups, some difÞculties are found when
identifying species. The hypertrophial female is the
most frequently observed form in hosts and after oviposition, the neosome involutes with the dead parasite
being absorbed or sloughed from the host epidermis
by tissue repair mechanisms (Lavoipierre et al. 1979,
Eisele et al. 2003). More often the legs are missing after
Þxation in the hosts (Rothschild 1992) and some characteristics cannot be seen in the most dissected specimens. With the exception of T. libis, all gravid females
are known. However, only Þve species have known
males: T. penetrans, T. terasma, T. libis, T. monositus,
and T. trimamillata.
The current study describes a new species of
Tunga of the caecata group parasitizing the tail base
of the striped rat Delomys dorsalis and collected
during the course of the interrelationship ßea-host
studies from Atlantic Forest areas in southeastern
Brazil (Bossi 2003, de Moraes et al. 2003). A key for
Tunga adult species and respective neosomes also is
included.
Materials and Methods
Delomys dorsalis harboring specimen of Tunga
was collected in one area of the Itatiaia National
Park (Itatiaia, RJ 22⬚ 26.187⬘ S, 44⬚ 37.511⬘ W) and
taken to the laboratory of the Department of Parasitology, State University of Campinas, where two
0022-2585/12/0023Ð0028$04.00/0 䉷 2012 Entomological Society of America
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Vol. 49, no. 1
Fig. 1. T. bossii sp. nov., neosomes. A. Two neosomes located on the base of the tail of a specimen of D. dorsalis collected
from Serra do Itatiaia, Rio de Janeiro, Brazil. Bar: 10 mm. B. Dorsal view of the neosome. Bar: 5 mm. C.) Ventral view of the
neosome, where it is possible to visualize a small, medially located opening. Bar: 2 mm.
neosomes were removed from its tail base and Þxed
in 70% ethanol. After identiÞcation the host specimen was released at the same trap site. The neosomes subsequently were sent to the Department of
Parasitology of the Federal University of Minas
Gerais, where they were measured and dissected.
Only the head, thorax, spermatheca, and caudal disk
of one of the neosomes was recovered (in the second neosome these structures already were deteriorated by dying of the ßea), diaphanized in 10% cold
potash, dehydrated in an ethanol series, clariÞed in
creosote, and mounted on slides in Canada balsam
(Linardi and Guimarães 2000). Morphometric parameters were measured using an Olympus binocular microscope (Japan) Þtted with ocular and
stages micrometers. Except for the neosome, all
measurements are in micrometers, including the
units cited in parentheses.
Morphologic comparisons were performed with
species deposited in collections from the Zoology
Museum of the University of São Paulo and the
Department of Parasitology of the Federal University of Minas Gerais, Brazil.
A female holotype was deposited in the Collection
of Ectoparasites of the Department of Parasitology of
the Federal University of Minas Gerais, Brazil.
Results
Tunga bossii, sp. nov.
(Figs. 1Ð 4)
Hypertrophied Female. Globular neosome (9-mm
length, 8-mm width, and 7-mm height) without lobes,
located at the base of the tail of the host (Fig. 1A).
Head and thorax completely invaginated within the
abdomen. Caudal disk forming a circular opening of 2
mm (Fig. 1B). Anterior extremity of the neosome with
a small, medially localized opening in the same position of the head (Fig. 1C). Head (Fig. 2): rounded
dorsal margin with a slightly pronounced frontal tubercle and six small bristles in a slight depression,
posterior to the frontal tubercle. Pre and postantennal
regions with 10 bristles each not organized in welldeÞned rows. Preoral internal sclerotization similar to
that of T. monositus, with the posterior arm (41.8 ␮m)
nearly two times longer than the anterior arm (22.1
␮m). Rounded ventral and dorsal genal lobes extending to the antennal fossa covering more than half of the
segment II but not reaching the antennal segment III.
Eye without black pigment and recess into its internal
margin with the greatest diameter (36.9 ␮m) exceeding half of its distance to the dorsal margin of the head
(60 ␮m). Antennal segment II with a single long bristle
January 2012
DE
AVELAR ET AL.: T. bossii NEW SPECIES
25
Fig. 2. T. bossii sp. nov., female holotype. Bar: 120 ␮m.
posterodorsally. Antennal clava with six antennomeres on its posterior margin (Fig. 3A). Laciniae strong,
heavily serrated, and slightly exceeding the distal part
of the anterior trochanter and exhibiting a total length
of 233.7 ␮m. Maxillary palps reaching the base of
anterior trochanter and increasing in length in the
following order: I ⬍ II ⬍ III ⬍ IV (Fig. 3B). Segment
I is very small (9.8 by 12.3 ␮m) when compared with
the rest of the segments, which have the following
length and width measurements: II: 49.2 by 17.2 ␮m;
III: 61.5 by 22.1 ␮m; IV: 71.3 by 22.1 ␮m. A complete
division between the segments III and IV of maxillary
palp was not observed in the specimen studied. Base
of the maxilla anteriorly with two bristles. Thorax:
Pronotum and mesonotum not completely fused dorsally, each with two bristles on their ventral halves.
Proepimeron with a small and rounded posterodorsal
lobe (Fig. 2). Legs: Mesocoxa with a complete oblique
external break. Metacoxa with an anterodistal angle
projecting down like a wide tooth (Fig. 2) and exhibiting on its median surface, two irregular rows with 15
bristles in total near to the anterior margin. Other two
apical bristles, four submarginals, and three tiny submarginals located posteroproximally. As is often the
case in gravid females of Tunga, the other segments of
the legs are not found. Spermatheca (Fig. 4A): Bulga
approximately globular measuring 61.5 ␮m long and
66.4 ␮m wide. Hilla with length of 41.8 ␮m and width
of 12.3 ␮m. Caudal disk (Fig. 4B): Tergite VIII divided
into two halves, each having one functional spiracle
located dorsally in the spiracular fossa. Bristles only in
the ventral region, being four each laterally on the
internal surface. Segment X with eight trichobothria
on each side and a plate projecting around the sensilium, exhibiting three robust bristles and two microbristles on the sides and two medium-length bristles.
Another plate below with a row of four bristles.
Type Material. HOLOTYPE: one female, BRAZIL:
Serra do Itatiaia, RJ (22⬚ 26.187⬘ S, 44⬚ 37.511⬘ W),
17-XII-2000, on Delomys dorsalis, Leandro B. de Moraes.
Etymology. The new species is named in honor of
the late David Eduardo Paolinetti Bossi, a Brazilian
entomologist.
Discussion
The pronotum of Tunga bossii is not completely
fused with the mesonotum, which is a characteristic
of the caecata group (Smit 1962). Tunga bossii can be
differentiated from all other known species of Tunga
by the size of the segment I of the maxillary palps,
which is greatly reduced compared with other species (segment IV is at least seven times longer than
segment I). In other Tunga species, the segment III
is always the smallest segment. In addition, it is the
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Vol. 49, no. 1
Fig. 3. T. bossii sp. nov., female holotype. A. Maxillary palp. Bar: 72 ␮m. B. Antenna. Bar: 25 ␮m. C. Posterodorsal lobe
of proepimeron. Bar: 50 ␮m.
only species that possesses two bristles at the base
of the maxilla. Still, it differs from the other species
of the “caecata” group by its eye morphology (the
eyes are large and nonpigmented, whereas those of
T. libis are pigmented, those of T. caecata and T.
monositus are small, and T. caecigena and T. callida
have no eyes) (Pinto and Dreyfus 1927, Wagner
1932, Jordan 1937, Hopkins and Rothschild 1953,
Johnson 1957, Smit 1962, Linardi and Guimarães
2000, Pampiglione et al. 2002).
The majority of species belonging to the caecata
group are parasites of the auricular region of rodents
(except T. libis, which is not known to form a neosome and T. callida, parasitizing the rear end of the
body) (Li and Chin 1957, Smit 1962, Barnes and
Radovsky 1969). This is the Þrst time that a Tunga
specimen has been found to parasitize the base of
the tail of a sigmodontine rodent. This site of infestation in rodents also represents the Þrst record in
the New World, up until now restricted to the external base of the ear pinna.
Key for Adult Species and Neosomes of the
Genus Tunga
1. Pronotum and mesonotum not completely fused
dorsally (caecata group) . . . . . . . . . . . . .
Pronotum and mesonotum fused dorsally (penetrans group) . . . . . . . . . . . . . . . . . . . .
2. Eye absent . . . . . . . . . . . . . . . . . . . . . .
Eye present
. . . . . . . . . . . . . . . . . . . . .
3. Occipital region with 8 Ð10 bristles. Preoral internal sclerotization with anterior arm extend-
2
7
3
4
ing to half the distance between frontal tubercle and base of maxillary palp. Lacinia as long
as maxillary palp. Elliptical neosome, with dorsal and ventral portions of similar dilatation,
measuring: 7Ð10-mm length, 5-mm width, and
6-mm height . . . . . . . . . . . . . . . . . . . . .
. . . . T. caecigena Jordan and Rothschild, 1921
Occipital region with 3Ð5 bristles. Preoral internal sclerotization with anterior arm extending
near to the base of maxillary palp. Lacinia
longer than maxillary palp. Spherical neosome,
with the dorsal portion more swelled than the
ventral portion, measuring: 4.5-mm length,
4.5-mm width, and 4.5-mm height. . . . . . . .
. . . . . . . . . . . . . T. callida Li & Chin, 1957
4. Eye pigmented. Gravid female unknown. . . . .
. . . . . . . . . . . . . . . . . . . . libis Smit, 1962
Eye without black pigment. Gravid female with
diverse forms . . . . . . . . . . . . . . . . . . . . 5
5. Posterodorsal lobe of proepimeron large,
strongly projecting. Base of maxilla with no
bristles. Lacinia as long as maxillary palp.
Gravid female with eight lobes, arranged as
four large outer lobes and four small inner
lobes . . . . . . . . . . . . . . . . . . . . . . . . . .
. . . . . T. monositus Barnes & Radovsky, 1969
Posterodorsal lobe of proepimeron small,
rounded. Base of maxilla with one or two bristles. Lacinia longer than maxillary palp. Gravid
female globular . . . . . . . . . . . . . . . . . . . 6
6. Preoral internal sclerotization with posterior arm
more than eight times the length of anterior
arm. Segment III is the smallest among the four
January 2012
DE
AVELAR ET AL.: T. bossii NEW SPECIES
27
Fig. 4. T. bossii sp. nov., female holotype. A. Spermatheca. Bar: 32 ␮m. B) Neosome: central region of the caudal disk.
Bar: 190 ␮m.
segments of maxillary palp. Segment IV of the
maxillary palp about twice length of segment
I. Spermatheca with the bulga longer than
wide and hilla two times longer than wide.
Neosome with length, width, and height measuring 7 ⫻ 6 ⫻ 6 mm . . . . . . . . . . . . . . .
. . . . . . . . . . . . T. caecata (Enderlein, 1901)
Preoral internal sclerotization with posterior arm
less than four times the length of anterior arm.
Segment I is the smallest among the four segments of maxillary palp. Segment IV of the
maxillary palp as long as segment III. Spermatheca with the bulga wider than long and
hilla about four times longer than wide. Neosome with length, width, and height measuring
9 ⫻ 8 ⫻ 7 mm . . . . . . . . . . . . . . . . . . . .
. . . . . . . . . . . . . . . . . . . . T. bossii sp. nov.
7. Eye without black pigment. Base of maxilla
with only a micro-bristle. Neosome with
head invaginated within abdomen, measuring: 12Ð13-mm length, 8-mm width, and
10-mm height . . . . . . . . . . . . . . . . . . . .
. . . . . . T. travassosi Pinto and Dreyfus, 1927
Eye pigmented. Base of maxilla with two or more
bristles. Neosome with head not invaginated
within abdomen or laterally visible . . . . . . 8
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8. Eye small, its greatest diameter only slightly exceeding half the distance from eye to dorsal
margin of head. Dorsal genal lobe covering
part of antennal segment III. Spermatheca
with bulga wider than long. Neosome measuring: 6-mm length, 6-mm width, and 5-mm
height . . . . . . . . . . . . . . . . . . . . . . . . .
. . . . . . . . . . . . . . T. bondari Wagner, 1932
Eye large, its greatest diameter nearly equal to
the distance from eye to dorsal margin of head.
Dorsal genal lobe not covering the antennal
segment III. Spermatheca with bulga longer
than wide . . . . . . . . . . . . . . . . . . . . . . . 9
9. Antennal segment II with only two bristles. Maxillary palp with few bristles. Hypertrophied
female not globular and containing four prominent subcylindrical lobes, measuring: 10-mm
length, 9-mm width, and 13-mm height . . . .
. . . . . . . . . . . . . . . T. terasma Jordan, 1937
Antennal segment II with more than two bristles.
Maxillary palp with numerous bristles. Hypertrophied female globular without lobes or exhibiting three anterior lobes . . . . . . . . . . 10
10. Anteromedial surface of posterior tibia with
row of 9 Ð12 bristles. Anterior base of maxilla
with 6 Ð7 bristles. Segment I of maxillary palp
longer than segment II. Spermatheca with
hilla 2.5 times longer than wide. Bulga nearly
Þve times longer than hilla. Hypertrophied
female with three lobes located anteriorly,
measuring: 12-mm length, 5-mm width, and
5-mm height . . . . . . . . . . . . . . . . . . . .
. . . . . T. trimamillata Pampiglione, Trentini,
Fioravanti, Onore, and Rivasi, 2002
Anteromedial surface of posterior tibia without
bristles. Anterior base of maxilla with three
thick bristles. Segment II of maxillary palp
longer than segment I. Spermatheca with
hilla as long as wide. Bulga ⬇3.5 times longer
than hilla. Globular hypertrophied female
without projections or lobes, measuring:
6-mm length, 5-mm width, and 5-mm height.
. . . . . . . . . . . . . . . T. penetrans (L., 1758)
Acknowledgments
The research forms part of the Ph.D. thesis of D.M.A.
produced under the auspices of the Programa de Pós-graduação em Parasitologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais (UFMG), Brasil. We
thank the Conselho Nacional de Desenvolvimento CientṍÞco
e Tecnológico (CNPq) for research fellowships to P.M.L. and
A.X.L.
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Received 27 May 2011; accepted 12 October 2011.