ADDITIONAL DESCRIPTION OF A NEW SPECIES OF
TUNGA
(SIPHONAPTERA)
FROM ECUADOR
PAMPIGLIONE S.*, TRENTINI M.**, FIORAVANTI ML.*, ONORE G.*** & RIVASI F.****
Summary:
A new species of chigoe flea belonging to the genus Tunga Jarocki, 1 8 3 8 (Siphonaptera, Pulicidae, Tunginae), Tunga
trimamillata, was recently described by Pampiglione et al. (2002). A better description and more details of the epidemiology of the flea are now presented. It is a species found in goats, pigs and cattle in Santa Isabel in Andean Ecuador. This new species differs from its most similar congener, Tunga penetrans (L. 1758), by several features, the most important of which are a) the presence on the anterior extremity of the gravid female of three rounded humps surrounding the head and thorax (which, however, are not visible if viewed in profile), b) slightly larger dimensions and c) the length of the first segment of the maxillary palpi which is longer than each of the other three.
K E Y W O R D S : Siphonaptera, Tunga, chigoes, Ecuador, goats, pigs, cattle.
Résumé : DESCRIPTION COMPLÉMENTAIRE D'UNE NOUVELLE ESPÈCE DE
TUNGA (SIPHONAPTERA) DE L'EQUATEUR
Une nouvelle espèce de chique appartenant au genre Tunga Jarocki, 1838 (Siphonaptera, Pulicidae, Tunginae), Tunga
trimamillata, a été récemment décrite par Pampiglione et al. 12002). les auteurs donnent ici une meilleure description et plusieurs détails de l'épidémiologie de cette nouvelle espèce. La chique a été trouvée dans la localité andine de Santa Isabel, en Equateur, chez des chèvres, des porcs et des bœufs. La nouvelle espèce se différencie de la plus proche espèce de ce genre, Tunga penetrons /(L., 1758), par plusieurs caractères
morphologiques, les plus importants étant constitués par : a) la présence à l'extrémité antérieure de la femelle gravide de trois protubérances encerclant la tête et le thorax qui, toutefois, ne sont pas visibles en observation de profil ; b) des dimensions légèrement plus grandes ; c) le premier segment des palpes maxillaires qui est le plus long des quatre.
MOTS CLES : Siphonaptera, Tunga, chiques, Équateur, chèvre, porc, bœuf.
INTRODUCTION
A
few years a g o , w e e x a m i n e d s o m e s p e c i m e n s of c h i g o e s r e m o v e d from goats and pigs from Ecuador (Trentini et al., 2 0 0 0 , 2 0 0 1 ) and, o n the basis o f s o m e m o r p h o l o g i c a l characteristics, w e w e r e u n a b l e to assign them to any k n o w n s p e c i e s o f the g e n u s Tunga ( T r a u b , 1 9 5 0 ; H o p k i n s ¿4 Rothschild, 1953; Smit, 1 9 6 2 ) . At that time, there w e r e t o o few spe-c i m e n s available to r e a spe-c h a firm spe-c o n spe-c l u s i o n regarding their identity. Since then, o n e o f us ( G . O . ) has collected m o r e c h i g o e s from goats and cattle in the s a m e loca-lity and further study has confirmed that they are a n e w s p e c i e s o f Tunga w h i c h w a s d e s c r i b e d and n a m e dTunga trimamillata n. sp. in a short c o m m u n i c a t i o n
* D i p a r t i m e n t o di S a n i t à P u b b l i c a V e t e r i n a r i a e P a t o l o g i a A n i m a l e , a n d ** D i p a r t i m e n t o di B i o l o g i a E v o l u z i o n i s t i c a S p e r i m e n t a l e , U n i -v e r s i t à di B o l o g n a , Italy. *** F a c u l t a d d e B i o l o g i a , Pontificia U n i v e r s i d a d C a t ó l i c a d e l E c u a d o r , Q u i t o , E c u a d o r . **** D i p a r t i m e n t o di S c i e n z e M o r f o l o g i c h e e M e d i c o Legali, U n i v e r -sità di M o d e n a e R e g g i o E m i l i a , M o d e n a , Italy. C o r r e s p o n d e n c e : Prof. M. T r e n t i n i , D i p a r t i m e n t o di B i o l o g i a e v o l u -z i o n i s t i c a s p e r i m e n t a l e , U n i v e r s i t à di B o l o g n a , via S e l m i 3, 4 0 1 2 6 B o l o g n a , Italy. F a x : 0 0 3 9 0 5 1 2 5 1 2 0 8 - T e l . : 0 0 3 9 0 5 1 2 0 9 4 1 6 2 . E-mail: t r e n t i n i @ a l m a . u n i b o . i t
in the XXII Congress o f the Italian Society o f Parasi-tology ( P a m p i g l i o n e et al., 2 0 0 2 ) . Now, a better des-cription and m o r e details o f its e p i d e m i o l o g y are here presented.
MATERIALS AND METHODS
S
ixty four gravid females in various stages o f deve-lopment and two male Tunga sp. were examined; all w e r e from Santa Isabel in the province o f Azuay in the Ecuadorian Andes ( 3 ° 15' 6 1 . 0 " S and 7 9 ° 18' 6 7 . 4 " W, at 1,400 m. a. s. l.). T h e female s p e c i m e n s w e r e taken from goats ( 4 9 s p e c i m e n s ) , pigs (six spe-c i m e n s ) and spe-cattle ( n i n e s p e spe-c i m e n s ) at a slaughte-rhouse o r from nearby breeding sites. T h e male spe-c i m e n s w e r e spe-captured using humans as bait in a goat shed. Most o f the females w e r e stored in 7 0 % ethanol and e x a m i n e d with a s t e r e o s c o p i c dissecting micro-s c o p e . T o micro-study particular morphological detailmicro-s micro-s o m e s p e c i m e n s w e r e dissected and drawn with a cameralucida. Histological sections w e r e stained with
hae-matoxylin and eosin, PAS and Masson G o l d n e r Tri-c h r o m i Tri-c . T h e males w e r e Tri-cleared and permanently m o u n t e d in Hoyer's medium. S o m e gravid females were dehydrated in an ascending series o f ethanol from
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97 0 % to 100 %, m o u n t e d o n a stub, sprayed with gold and o b s e r v e d under a J E O L 5 2 0 0 scanning electron m i c r o s c o p e (SEM). Another 50 gravid females o f Tunga sp. from pigs from other areas in the Andes o f Ecuador (Pelileo at 2,592 m in the province o f Tungurahua and R i o b a m b a at 2,754 m in the province o f C h i m b o r a z o ) w e r e e x a m i n e d to s e e if the n e w species o f Tunga was also present in localities 2 5 0 - 3 0 0 km north o f Santa Isabel. O u r s p e c i m e n s w e r e c o m p a r e d with males and gravid females o f T. penetrans from Africa and V e n e zuela from humans, pigs and dogs, and with Tunga spp. in the collection of the Natural History Museum, London.
RESULTS
T
he s p e c i m e n s o f Tunga sp. from Santa Isabel collected from goats, pigs and cattle have mor phological characters showing they represent a previously u n d e s c r i b e d s p e c i e s . T h e c h i g o e s fromc
Africa, V e n e z u e l a and other p l a c e s in E c u a d o r w e r e identified as Tunga penetrans.
DESCRIPTION T y p e material
T h e gravid female holotype from Santa Isabel, 3° 15' 6 1 . 0 " S - 7 9 ° 18' 6 7 . 4 " W, 1,400 m.a.s.l., province o f Azuay, Ecuador, from Capra hircus, 15.X. 1 9 9 0 , leg. N. Minerva. Paratypes o f both s e x e s from the s a m e loca lity are deposited in the B i o l o g y Department of the University o f B o l o g n a , Italy.
Adult gravid female (Fig. 1)
Globular, slightly c o m p r e s s e d in an antero-posterior direction (Fig. 1A) with the greatest dimension reaching about 6 mm in width. Anteriorly, there are three humps o n the a b d o m e n (Fig. 1A, C ) easily visible to the n a k e d e y e and surrounding the head and the thorax, r e n d e r i n g the latter structures invisible o n profile (Fig. 2A). T h e three humps, o n e ventral and two
late-1 0 P a r a s i t e , 2 0 0 3 , 10, 9 - 1 5 F i g . 2 . - ( A ) G r a v i d f e m a l e o f Tunga trimamillata in p r o f i l e . ( B ) M a x i l l a r y p a l p i o f Tunga tri mamillata f e m a l e . ( C ) G r a v i d f e m a l e o f Tunga penetrans in p r o file. ( D ) M a x i l l a r y p a l p i o f Tunga penetrans f e m a l e .
N E W S P E C I E S O F TUNGA F R O M E C U A D O I
rodorsal, are similar to e a c h other having a semis¬ pherical form, e a c h with a diameter w h i c h can b e as m u c h as 1.2 m m (Fig. 1A, C); they are semi-transpa rent and s o m e ova are m o r e or less plainly visible within them. T h e e y e is large, pigmented and measures 4 2 x 6 5 m m (Fig. 1 B ) . T h e maxillary palpi are c o v e r e d by numerous, thick, short spines and long bristles and have the first proximal segment clearly longer than the other three; the third is the shortest (Fig. 1D, Fig. 2 B ) . T h e last tarsal segment o f the legs is long and narrow, about eight times longer than its width (Fig. 1 B ) . P o s teriorly, the last a b d o m i n a l s e g m e n t s form a large visible c o n e that is s o m e t i m e s h o l l o w e d in the penul timate segments; the respiratory spiracles o f a b d o minal s e g m e n t s V to VIII are cleary visible (Fig. 1E, F ) . W e don't describe u n e x p a n d e d females, n o n e b e i n g captured.
Male (Fig. 1 G )
T h e length o f the b o d y is about 1 mm. T h e respira tory spiracles, all o f similar size, are visible o n the a b d o m e n . Apparently, the genitalia are similar to those o f T. penetrans. T h e few male s p e c i m e n s presently available are insufficient for a m o r e detailed descrip tion. W e are studying other s p e c i m e n s recently col lected o n the field by o n e o f us (M.L.F.) and they will b e referred to another study.
Diagnosis
T h e most striking morphological feature o f T.
trima¬
millata w h i c h immediately differentiates this s p e c i e s
from the o t h e r nine described s p e c i e s o f the s a m e g e n u s is the p r e s e n c e o f the three h u m p s o f t h e a b d o m e n and the impossibility o f seeing the head and thorax o f the gravid female in profile (Fig. 2A). T h e h u m p s are absent in T. penetrans. T. travassosi Pinto
& Dreyfus, 1927, T. bondari Wagner, 1932 and T.
cae-cata Enderlein, 1901 and the h e a d and thorax are
either visible in profile (T. penetrans, T. travassosi) (Fig. 2C and Fig. 3A, C ) or, w h e n c o n c e a l e d within the a b d o m e n , are invisible (T. bondari, T. caecata). In
T. terasma Jordan, 1937, T. caecigena J o r d a n & Roth
schild, 1 9 2 1 , T. callida Li & Chin, 1957 and T.
mono-situs B a r n e s & Radovsky, 1969, four or eight l o b e s and
h u m p s are present and the h e a d and thorax are either visible in profile (T. terasma) or, w h e n c o v e r e d by the humps, invisible (T. caecigena, T. callida, T. monositus) (Table I ) . T h e e x p a n d e d female o f T. libis Smit, 1962 is at present u n k n o w n .
Tunga trimamillata is similar to T. penetrans in having
the pronotum completely fused dorsally with the m e s o ¬ notum and in having p i g m e n t e d eyes. In addition to the three humps, there are three other features that dis tinguish the n e w s p e c i e s from T. penetrans, namely: a ) size: the b o d i e s o f both m a l e and female T. trima
millata are much larger than those o f T. penetrans;
b ) the maxillary palpi o f T. trimamillata are c o v e r e d with thick, short spines and long bristles c o m p a r e d to only long and short bristles in T. penetrans (Fig. 1D, 3 B , 2 B , 2 D ) ;
c ) the first proximal s e g m e n t o f the maxillary palpi o f
T. trimamillata is longer than the others (Fig. 1D,
Fig. 2 B ) w h e r e a s , in T. penetrans, the s e c o n d is the longest (Fig. 2 D ) ( W e s t w o o d , 1 8 4 0 ; Hopkins & Roth schild, 1 9 5 3 ; Jordan, 1 9 6 2 ) .
Pathology
Macroscopically, the lesions due to Tunga trimamil
lata are m o r e evident than those due to T. penetrans
and, w h e n the parasite is extracted from the skin, w e can s e e with the n a k e d e y e the hump-prints at the b o t t o m o f the "hole" (Fig. 4 A ) .
A b d o m e n H e a d a n d thorax G e o g r a p h i c a l
S p e c i e s s h a p e i n p r o f i l e d i s t r i b u t i o n H o s t
T. trimamillata n. sp. globular not visible, a m o n g 3 h u m p s Ecuador goat, pig, c o w
T penetrans (L. 1758) globular visible Latin America and Africa human, pig, dog, c o w ,
South o f the Sahara horse, donkey, etc.
T. Travassosi Pinto & Dreyfus, 1 9 2 7 globular visible Brazil amardillo
( D a s y p u s novemcinctus)
T. bondari W a g n e r . 1 9 3 2 globular not visible, c o n c e a l e d within Brazil ant-eater
a b d o m e n (Tamandua tetradactyla)
T. terasma J o r d a n , 1 9 3 7 quadrilobate visible Brazil amardillo ( C a b a s s o u s
unicinctus)
T. caecata Enderlein, 1901 globular not visible, c o n c e a l e d within Brazil Rattus rattus. R. nonegicus.
a b d o m e n Mus muscalus
T. caecigena J o r d a n & Rothschild, 1921 elliptical not visible, a m o n g 4 h u m p s China, J a p a n Rattus rattus. R. nonegicus T. callida Li & Chin. 1 9 5 7 globular not visible, a m o n g 4 h u m p s China rodents
T. libis Smit, 1962 (*) not d e s c r i b e d not described Ecuador. Chile Akodon mollis T. monositus B a r n e s & Radovsky, 1969 ovoid not visible, a m o n g 8 h u m p s M e x i c o , USA rodents
(*) Smit ( 1 9 6 2 , 1 9 6 8 ) d e s c r i b e d only o n e m a l e from E c u a d 3r a n d two u n e x p a n d e d females from Chile.
T a b l e I. - S p e c i e s o f t h e g e n u s T u n g a : gravid f e m a l e s c h a r a c t e r i s t i c s .
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PAMPIGLIONE S , TRENTINI M„ FIORAVANTI M.L. ETAL.
Fig. 1. - Tunga trimamillata from g o a t s , E c u a d o r . ( A ) A n t e r i o r e x t r e m i t y of g r a v i d f e m a l e . ( B ) H e a d a n d t h o r a x of g r a v i d f e m a l e s e p a rated f r o m a b d o m e n ( H o y e r ' s m e d i u m ) . ( C ) A n t e r i o r e x t r e m i t y o f gravid f e m a l e , S E M . ( D ) D e t a i l s of h e a d a n d t h o r a x of g r a v i d f e m a l e in frontal v i e w , S E M . ( E ) R e s p i r a t o r y s p i r a c l e s of last a b d o m i n a l s e g m e n t s of g r a v i d f e m a l e ( H o y e r ' s m e d i u m ) . ( F ) R e s p i r a t o r y s p i r a c l e s ( a r r o w s ) o f 5t h, 6, h a n d 7l h a b d o m i n a l s e g m e n t s , S E M . ( G ) M a l e ( H o y e r ' s m e d i u m ) .
Fig. 3. - Tunga penetrans from h u m a n , M a d a g a s c a r . ( A ) G r a v i d f e m a l e . ( B ) F r o n t a l v i e w of h e a d a n d t h o r a x of g r a v i d f e m a l e , S E M . ( C ) A n t e rior e x t r e m i t y of a g r a v i d f e m a l e , S E M .
Fig. 4 . - ( A ) L e s i o n d u e t o Tunga trimamillata from pig. ( B ) H i s t o l o g i c a l s e c t i o n of gravid f e m a l e of Tunga trimamillata e m b e d d e d in s k i n of a b o v i n e ( T r i c h r o m i c M a s s o n G o l d n e r S t a i n ) . N o t e t h e h u m p s ( h ) .
P a r a s i t e , 2 0 0 3 , 10, 9 - 1 5
Mémoire 13
T h e r e are n o apparent differences in the histopatho¬ logical c h a n g e s in the host skin c a u s e d b y T. t r i m a ¬
millata and T. penetrans (Pampiglione et ai, 1998). T h e
parasite is situated in the epithelial tissue c o v e r e d almost c o m p l e t e l y by the considerably thinned horny layer, s o that it is d e e p l y inserted in the basal layers o f the skin o f the host. Communication with the out side is through a small foramen that allows the para site to respire, excrete and oviposit. A moderate inflam matory infiltration, principally consisting o f eosinophilic g r a n u l o c y t e s , neutrophils, l y m p h o c y t e s , and rarely plasmacells and histiocytes, is usually present near the cephalic extremity o f the parasite. T h e epithelial layer frequently s h o w s acanthosis and hyperkeratosis with a marked irregular surface (Fig. 4 B ) .
Seasonality
Tunga trimamillata was c o l l e c t e d exclusively during
the dry season, i.e. from J u n e to O c t o b e r . Local n a m e
Locally, the Santa Isabel c h i g o e is called "Nigua"; this is the s a m e n a m e u s e d for T. penetrans in o t h e r regions o f E c u a d o r and Latin America t o o .
DISCUSSION
The nine d e s c r i b e d s p e c i e s o f c h i g o e s o f the genus Tunga are subdivided into two groups
– penetrans group and caecata group – a c c o r
ding to the p r e s e n c e or a b s e n c e o f e y e s , or e y e pig ment, and w h e t h e r o r not the p r o n o t u m is fused with the m e s o n o t u m (Smit, 1962). T h e s p e c i e s o f the first group are parasites o f edentates, armadillos, h u m a n s and various domestic and wild mammals; t h o s e o f the s e c o n d group afflict, mainly, murine and sigmodontine rodents. Tunga trimamillata b e l o n g s to the penetrans group. T h e geographical distribution, hosts and impor tant morphological characteristics o f e a c h s p e c i e s are s h o w n in T a b l e I.
A male o f Tunga libis, found o n the sigmodontine rodent, Akodon mollis ( T h o m a s , 1 8 9 4 ) , in R i o b a m b a , Ecuador, was described b y Smit (1962). T h e male o f
T. trimamillata differs from that o f T. libis by a ) its
larger size, b ) the claspers, c ) the 5t h tarsal segment and d ) the maxillary palpi. In the original description,
T. libis w a s placed, and it's unquestionably so, in the caecata g r o u p e v e n though the e y e was not des
cribed. T h e e y e was, h o w e v e r , s h o w n in a figure w h e r e it is c l o s e to the dorsal margin o f the head than that o f T. trimamillata (Fig. 1 G ) . It was not possible to c o m p a r e the u n e x p a n d e d female o f T. libis, des cribed b y Smit (1968), b e c a u s e w e didn't capture this stage o f T. trimamillata.
It is interesting to note that, with the e x c e p t i o n o f
T. penetrans, Tunga spp. almost always parasitise a
single s p e c i e s o f vertebrate host, o r a few c l o s e l y related s p e c i e s . T. trimamillata has already b e e n col lected from three different s p e c i e s (goats, pigs and cattle) and it is p r o b a b l e that, like T. penetrans, it can also parasitise other s p e c i e s o f animals, b o t h d o m e s t i c and wild, as well as humans. Pending research is veri fying the hosts and the g e o g r a p h i c distribution. W e c h e c k e d the literature o f the 1 8 0 0 s and early
1900s, w h e n the multiplicity o f Tunga s p e c i e s w a s not k n o w n , to s e e if any early illustrations o f Tunga could be referred to T. trimamillata, but all depicted T. pene
trans. H o w e v e r , in a r e c e n t publication ( G e o r g i &
G e o r g i , 1 9 9 1 ) , w e found p h o t o g r a p h s (Fig. 1.21 and T a b l e s 1-6) o f a gravid f e m a l e classified as Tunga sp. from a pig in E c u a d o r (locality not specified) in w h i c h the p r e s e n c e o f three clearly visible anterior h u m p s suggests the s p e c i m e n w a s T. trimamillata.
ACKNOWLEDGEMENTS
W
e t h a n k N i c o l a M i n e r v a a n d G i u s e p p e Diegoli for kindly providing s o m e s p e c i m e n s o f the c h i g o e s from E c u a d o r and Mario Marini and Salvatore G i a n n e t t o for h e l p with scanning e l e c t r o n m i c r o s c o p y . Finally, w e thank T h e resa H o w a r d for assistance in e x a m i n i n g t h e c o l l e c t i o n o f c h i g o e s in t h e E n t o m o l o g y D e p a r t m e n t , Natural History M u s e u m , L o n d o n , J o a n n a Kapusta o f t h e s a m e department for h e l p with relevant literature, Robert Killick-Kendrick for revision o f our manuscript and Ayodhya P. G u p t a for his v a l u a b l e advices and s u g g e s t i o n s . T h i s i n v e s t i g a t i o n w a s s u p p o r t e d b y grant from t h e MIUR and from the F o u d a z i o n e Cassa di Risparmio in B o l o g n a .REFERENCES
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