O N EIMERIA BRAGANCAENSIS N . SP. (APICOMPLEXA: EIMERIIDAE) A N D TISSUE-CYSTS OF A N UNIDENTIFIED PROTOZOAN
I N THE BAT PEROPTERYX MACROTIS (CHIROPTERA: EMBALLONURIDAE) FROM A M A Z O N I A N BRAZIL
LAINSON R.* & NAIFF R.D.**
Summary:
A description is given of the mature oocysts and endogenous stages of Eimeria bragancaensis n. sp., from the small intestine of the bat Peropteryx macrotis from north Brazil. Oocysts are spherical to sub-spherical, 15.9 x 14.6 µm (range 14-17 x 14-
17.7). The wall is of two layers: an outer, thicker one which is of a brownish-yellow colour and striated (pitted), and an inner one which is thin and colourless. The outer layer is frequently lost. No micropyle or oocyst residuum present, but the oocyst usually contains one or two polar bodies. Sporocysts 8.4 x 5.3 µm (range 6.25-9 x 4-6) with inconspicuous Stieda and substiedal bodies. Endogenous stages are intracytoplasmic in the epithelial cells of the small intestine, above the host-cell nucleus. Stages of merogony and gametogony are described. Abundant tissue-cysts of an unidentified protozoan, containing from 1-4 zoites, were found in the parenchyma cells of the liver and, less frequently, in the lamina propria of the small intestine. Their possible nature is discussed.
KEY WORDS : Eimeria bragancaensis n. sp., oocysts, endogenous stages, Peropteryx macrotis, Chiroptera, bat, unidentified protozoan, tissue-cysts, Brazil.
Résumé :
EIMERIA BRAGANCAENSIS N. SP. (APICOMPLEXA : EIMERIIDAE) ET KYSTES VISCÉRAUX D'UN PROTOZOAIRE NON IDENTIFIÉ CHEZPEROITERYX MACROTIS (CHIROPTERA : EMBALLONURIDAE) DE L'AMAZONIE BRÉSILIENNE
Description des oocystes matures et du stade de développement endogène d'Eimeria bragancaensis n. sp. au niveau de l'intestin grêle de la chauve-souris Peropteryx macrotis du nord du Brésil.
Les oocystes sont sphériques ou subsphériques : 15,9 x 14,6 µm (14-17 x 14-17,7). La paroi comporte deux couches : l'externe, la plus épaisse, de couleur jaune-brun, est striée; l'interne, plus fine, est incolore. La couche externe est souvent absente. Les oocystes comportent habituellement un ou deux corps polaires. Les sporocytes mesurent 8,4 x 5,3 µm (6,25-9 x 4-6). Les stades de développement endogène sont intracytoplasmiques dans les cellules épithéliales de l'intestin grêle, au-dessus du noyau de la cellule hôte. Les stades de mérogonie et de gamétogonie sont décrits. De nombreux kystes viscéraux d'un protozoaire non identifié et contenant de un à quatre zoïtes, ont été observés dans les cellules du parenchyme hépatique et moins souvent dans la lamina propria du grêle, leur nature est discutée.
MOTS CLÉS :
Eimeria bragancaensis n. sp., oocystes, développement endogène, Peropteryx macrotis, chiroptère, protozoaire sans identité, kystes viscéraux, Brésil.INTRODUCTION
A
s far as w e are aware, only e l e v e n valid spe- cific n a m e s have b e e n given to Eimeria s p e - cies o f bats (Lainson & Naiff, 1 9 9 8 ) , in spite o f the w i d e range o f genera and s p e c i e s within the order Chiroptera and the h u g e b i o m a s s they represent. F o r this reason descriptions o f additional chiropteran e i m e - riids are particularly w e l c o m e .Coccidial oocysts found in the faeces o f o n e o f three s p e c i m e n s o f the bat Peropteryx macrotis from north Brazil are c o n s i d e r e d to b e t h o s e o f a previously unre- c o r d e d Eimeria s p e c i e s , and descriptions are given o f the mature o o c y s t s in the f a e c e s and the e n d o g e n o u s stages o f the parasite as s e e n in histological sections
* Department of Parasitology, Instituto Evandro Chagas, Caixa Postal 1128, Belém, Para, Brazil.
** Instituto Nacional de Pesquisa da Amazonia, Caixa Postal 478, Manaus, Amazonas, Brazil.
Correspondence: R. Lainson.
Tel.: (55.91) 211.4453 - Fax: (55.91) 226.1284.
o f the small intestine. O c c a s i o n a l tissue-cysts, contai- ning from 1-4 zoites, w e r e found in the lamina pro- pria o f the small intestine and, m o r e abundantly, in the p a r e n c h y m a cells o f the liver. W e consider t h e s e not to b e an extra-intestinal stage o f the n e w Eimeria sp., but part o f the life-cycle o f s o m e other unidenti- fied parasite. T h e i r possible nature is discussed.
MATERIALS AND METHODS
T
hree s p e c i m e n s o f P. macrotis w e r e captured in primary forest n e a r B r a g a n ç a , Para, north Brazil ( 1 ° 0 3' S , 4 6 ° 4 6 ' W ) in August, 1998: o n e w a s taken from a h o l l o w tree-trunk and two from the b r a n c h e s o f a nearby tree. Abundant oocysts w e r e detected in faeces removed from the rectum o f the first bat a n d this material was s u s p e n d e d in a small quan- tity o f 2 % ( w / v ) a q u e o u s p o t a s s i u m d i c h r o m a t e ( K , C r , 07) and maintained at room temperature ( 2 3 - 2 4 ° C ) . No o o c y s t s could b e detected in faeces from the o t h e r t w o animals. Further e x a m i n a t i o n o f theParasite, 2000, 7, 123-129 Mémoire 123
LAINSON R. & NAIFF R.D.
Figs 1-13- - Endogenous stages of Eimeria bragancaensis n. sp., in the epithelial cells of the small intestine of the bat, Peropteryx macrotis.
Figs 1, 2. Developing and segmented meronts. Figs 3-5. Growing microgamonts. Figs 6, 7. Mature microgamonts shedding microgametes.
Fig. 8. Young macrogamonts. Figs 9,10. Growing macrogamonts: note large numbers of cytoplasmic inclusions, probably amylopectin gra
nules. Fig. 11. Mature macrogamont. Fig. 12. Young oocyst. Fig. 13. Sloughing of epithelial cells and parasites (arrowed) into the gut lumen.
Figs 14-16. - Mature oocysts in the faeces.
P = polar bodies; R = microgamont residuum; SS = Stieda and substiedal bodies; W = inner oocyst wall layer; WFB 1 = small type 1 wall- forming bodies; WFB 2 = large type 2 wall-forming bodies. Bars = 10 um. That in Fig. 9 also applies to Figs 1-12.
124 Mémoire Parasite, 2000, 7, 123-129
F i g s 1 7 - 2 7 . - L i n e - d r a w i n g s o f t h e e n d o g e n o u s s t a g e s o f Eimeria bragancaensis n. s p . in t h e s m a l l i n t e s t i n e o f t h e b a t Peropteryx macrotis.
Fig. 1 7 . S e g m e n t e d m e r o n t . F i g s 1 8 , 1 9 . D e v e l o p i n g m a c r o g a m o n t s . Fig. 2 0 . M a t u r e m a c r o g a m o n t . F i g s 2 1 , 2 2 . Y o u n g o o c y s t s , w i t h thin, i n n e r l a y e r o f t h e o o c y s t w a l l . F i g s 2 3 - 2 5 . D e v e l o p i n g m i c r o g a m o n t s . F i g s 2 6 , 2 7 . M a t u r e m i c r o g a m o n t s s h e d d i n g m i c r o g a m e t e s a n d l e a v i n g a r e s i d u u m o f v a r i a b l e s i z e .
P a r a s i t e , 2 0 0 0 , 7, 1 2 3 - 1 2 9 125
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positive material was only possible several w e e k s later, b y w h i c h time most o f the oocysts w e r e fully sporu- lated. W e w e r e unable, therefore, to record the s p o - rulation time.
Twenty-five oocysts and 3 5 sporocysts were measured by normal light-microscopy with a x 100 neofluar objec
tive, x 10 eyepieces and an ocular micrometer. T h e entire intestine w a s removed and fixed in 10 % neutral buf
fered formalin, together with pieces o f liver, spleen and lung. Tissues w e r e paraffin-wax e m b e d d e d and sec
tions, cut at 5 pm, w e r e stained with haematoxylin and eosin. Photomicrographs w e r e prepared using a Zeiss P h o t o m i c r o s c o p e III and K o d a k T M X 100 film. All measurements are given in pm: for the oocysts these are given as m e a n s , with the range in parentheses, fol
l o w e d b y the shape-index (ratio o f length/width).
DESCRIPTIONS
EIMERIA BRAGANCAENSIS N. SP. (Figs 1-29)
J — " d e s c r i p t i o n of the oocyst (Figs 14-16; 2 8 , 2 9 ) . With M J t h e characters o f the genus. Mature oocysts
spherical ( 5 0 % ) to subspherical, 15.9 x 14.6 (1 i- 17.7 x 14-17.7), shape-index 1.0 (1-1.2). Intact oocyst wall about 1.0 thick and o f two layers (Figs 14, 2 8 ) . The outer layer is prominently striated (pitted), yellow- b r o w n in colour and approximately 0.75 thick. It is fre
quently lost, leaving only the thin, colourless and non- striated inner layer (Fig. 2 9 ) . T h e r e is n o micropyle or oocyst residuum, but o n e or t w o polar b o d i e s . T h e s e are rather irregular in s h a p e and m e a s u r e approxima
tely 1-2 x 1, Sporocysts pear-shaped, 8.4 x 5.3 ( 6 . 2 5 - 9 x 4 - 6 ) , s h a p e i n d e x 1.6 ( 1 . 2 - 1 . 9 ) , and with i n c o n s picuous Stieda and substiedal bodies. Sporocyst residuum c o m p o s e d o f a relatively small n u m b e r o f globules and finer granules. Sporozoites with anterior (smaller) and posterior (larger) refractile bodies.
Endogenous stages (Figs 1-13). M e r o g o n y and g a m e t o - g o n y stages are intracytoplasmic in the epithelial cells o f the small intestine, a b o v e the host-cell nucleus. Seg
m e n t e d meronts (Figs 2, 17) averaged 10 x 8: from cross-sections it was estimated that they produce only from 10-20 merozoites measuring approximately 5 x 1.5, and that little or n o residuum remains. Y o u n g m a c r o - g a m o n t s measuring about 4 x 4 are recognizable by their voluminous nucleus containing a prominent karyo- s o m e (Figs 8, 9, 18, 19). Mature macrogamonts are about 11 x 10 and, with growth, contain the usual eimeriid small (type I) and large (type II) wall-forming bodies:
the latter are particularly conspicuous (Figs 11, 2 0 ) . T h e cytoplasm o f the growing m a c r o g a m o n t s and zygotes (or y o u n g o o c y s t s ) b e c o m e s p a c k e d with small, ovoid, colourless bodies (Figs 10, 20-22) which probably repre
sent the amylopectin granules c o m m o n l y r e c o r d e d in
the m a c r o g a m o n t s and zygotes o f other eimeriids.
Early microgamonts (Figs 3, 2 3 , 2 4 ) are readily diffe
rentiated from young schizonts and m a c r o g a m o n t s by their intensely staining and frequently angular nuclei, located around the periphery o f the parasite. T o w a r d s maturity the microgamonts m e a s u r e approximately 10, and p r o d u c e a large n u m b e r o f m i c r o g a m e t e s measu
ring about 3 x 0.5. T h e r e is a c o n s p i c u o u s residuum, o f variable size (Figs 6, 7 , 2 6 , 2 7 ) .
Host: the bat Peropteryx macrotis (Wagner, 1 8 4 3 ) (Chi- roptera: Emballonuridae).
Location in host: in the cytoplasm o f the epithelial cells of the small intestine.
Type locality: primary forest, near Braganca, Para State, north Brazil (1° 0 3 ' S 4 6 ° 4 6 ' W ) .
Spontlation time: not ascertained.
Prevalence: uncertain. O n e o f three P. macrotis e x a m i n e d w a s infected.
Pathology: there was considerable sloughing o f the intes
tinal epithelium in the major d e v e l o p m e n t a l regions o f E. bragancaensis in the small intestine, with dissociated cells and parasites present in the gut lumen (Fig. 1 3 ) . T h e infected bat, h o w e v e r , a p p e a r e d to b e in g o o d health.
Etymology: T h e specific n a m e is derived from the type locality o f the parasite in B r a g a n c a , Para, north Brazil, w h e r e the infected bat was captured.
Figs 2 8 , 2 9 . - L i n e - d r a w i n g s o f m a t u r e o o c y s t s o f Eimeria bragan
caensis n. sp., in f a e c e s o f t h e b a t Peropteryx macrotis. Fig. 2 8 . O o c y s t with intact, t w o - l a y e r e d wall. Fig. 2 9 . O o c y s t , h a v i n g lost t h e t h i c k e r , o u t e r striated w a l l layer.
TLSSUE-CYSTS OF AN UNIDENTIFIED PARASITE
IN THE LIVER AND lamina propria
OF THE BAT Peropteryx macrotis
During our e x a m i n a t i o n o f histological sections o f tis
sues from the bat infected with E. bragancaensis n.sp., w e noted the o c c a s i o n a l p r e s e n c e o f cysts in the
lamina propria o f the small intestine (Figs 3 0 - 3 3 ) , and similar b o d i e s w e r e abundant in p a r e n c h y m a cells o f the liver (Figs 3 4 - 3 7 ) . T h e y m e a s u r e d approximately
126 Mémoire P a r a s i t e , 2 0 0 0 , 7, 1 2 3 - 1 2 9
Figs 30-33- - Developing tissue-cysts of an unidentified protozoan (probably Hepatozoori) in the lamina propria of the small intestine of the bat Peropteryx macrotis, containing from 2-4 endozoites. Figs 34-37. - Similar cysts in the parenchyma cells of the liver. Sections stained with haematoxylin and eosin. Bar = 10 pm.
16.7 x 13.7 (12.5-22.5 x 8.7-16.2), s h a p e - i n d e x 1.2 ( 1 - 1.6) for 30 cysts e x a m i n e d , and c o n t a i n e d either an undivided parasite with a single nucleus (Figs 34, 35) or stages in the division to form from 2-4 zoites (Figs 30- 33, 36, 37). Fully separated zoites measured approxi
mately 12.5 x 2.5.
DISCUSSION
T
a b l e I lists the generally a c c e p t e d s p e c i e s o f Eimeria previously described from bats. A m o n g a n u m b e r o f features, Eimeria bragancaensis n.sp. can b e differentiated from these as follows. From E. andamanensis Mandal & Nair 1 9 7 3 , E. dukei Lavier 1927 and E. levinei Bray 1 9 5 8 by the a b s e n c e o f a micropyle a n d / o r an oocyst residuum: from E. eumopsMarinkelle 1968, E. molossi Lainson & Naiff 1 9 9 8 , E. rbynchonycteridis Lainson 1 9 6 8 , E. vespertilii Mus- saiev & Weissov 1 9 6 1 , E zakirica Mussaiev 1967 and E. mehelyi Mussaiev & Gauzer 1971 b y its much smaller oocysts.
Morphologically, the oocysts o f E. bragancaensis n. sp., are closest to t h o s e o f E. macyi W h e a t 1 9 7 5 a n d E. hessei Lavier 1924. T h e oocyst o f E. macyi is only slightly larger ( 1 9 x 17.6, range 16-21 x 1 5 - 1 9 ) , has a striated wall (but which is described as unilayered) and further resembles E. bragancaensis n. sp. in having n o oocyst residuum, but 1-2 polar bodies. Its sporocysts, however, are considerably larger ( 1 1 x 7, range 10-
1 2 x 6 - 8 versus 8.4 x 5.3, range 6.2-9 x 4-6). In addi
tion, t h e sporocysts have "prominent" Stieda and s u b - stiedal b o d i e s , w h i c h contrast m a r k e d l y with t h e i nconspi cuous o n e s o f E. bragancaensis n. sp. T h e
P a r a s i t e , 2 0 0 0 , 7, 1 2 3 - 1 2 9
Mémoire 127
LAINSON R. & NAIFF R.D.
Measurements (um), Measurements (um),
Species Host morphology3, oocyst Sporocystb
E. andamanensis Taphozous melanopogon M, OR Mandai & Nair 1973
E. dukei Nyctinomous limbatus, 20-24, S; 23-25 X 18-22, O; OR, Wl 7-9 x 6-7
Lavier 1927 N. pumilus
E. eumopos Eumops trumbulli 34.9 x 28 ( 3 4 - 3 6 x 27-28), O-S; PP, W2 11 x 7.9 (10.5-11.8 x 6.5-8.1), St Marinkelle 1968
E. hessei Rhinolophus hipposideros 16-22, S ¿4 15-18 x 13-15, O; Wl 11 x 5.5 Lavier 1924
E. levinei Tadarida bemmelini 21.6 x 18.2 (19-24 x 17-19), O, M, Wl 8.5 x 7.4 (8-9 x 7-8) St Bray 1958
E. maeyi Pipistrelli^ subflavus 19 x 17.6 (16-21 x 15-19), E, P, Wl 1 1 x 7 (10-12 x 6-8) St, Sb Wheat 1975
E. mehelyi Rhinolophus mehelyi Larger than 19 x 17.6 (Wheat, 1975) •>
Mussaiev & Gauzer 1971
E. molossi Molossus ater 23.4 x 17.5 (18-30 x 15-22.5), E, PP, W3 10.2 x 7.5 (10-12.5 x 7.5), St Lainson & Naiff 1998
E. rhynchonyeteridis Rhynchonycteris naso 25.5, S; Wl 15.2 x 8.1; St, Sb Lainson 1968
E. vespertini Vespertilio kuhlii 25.1 x 22 (20-27 x 18-25), S-SS; O, W2, P 6 - 1 0 x 4-6, St Mussaiev & Weissov 1961
E. zakirika Vespertilio kuhlii 25 x 22.5 (20-30 x 16-26), O; P, Wl 11.2 x 7.6 (8-14 x 6-10), St Mussaiev 1967
E. bragancaensis Peropteryx macrotis 15.9 x 15.2 (14-17.7 x 12.5-17.7), S-SS; W2 8.4 x 5.3 (6.2-9 x 4-6), St, Sb n. s p . ( t h i s p a p e r )
a E = ellipsoidal; M = with micropyle; O = ovoid; OR = with oocyst residuum; P/PP = with polar body (ies); S = spherical; SS = subsphe- rical; W = number of oocyst wall layers.
b St = with Stieda body; Sb = with substiedal body.
Table I. - Eimeria species recorded in bats.
e n d o g e n o u s stages o f E. macyi w e r e not described.
T h e o o c y s t o f E. hessei has the large size range o f 16- 22 for spherical forms and 1 5 - 1 8 x 13-15 for those des- cribed as "ovoid". According to Lavier's description and illustrations, there is a single-layered, non-striated wall, and the oocyst contains n o polar bodies. Measurements o f sporocysts are not given in text, but from the pm scale a c c o m p a n y i n g the illustrations they are approxi- mately 11 x 5.5 and larger, therefore, than those o f E. bragancaensis n. sp: n o Stieda or substiedal b o d i e s are figured. Additional differential features could not b e found w h e n c o m p a r i n g the e n d o g e n o u s stages o f the t w o parasites.
T h e mature o o c y s t s o f E. bragancaensis n. sp. are fra- gile and s o o n b e c o m e considerably deformed (Fig. 1 5 ) . In m a n y c a s e s the thicker, striated wall b e c o m e s deta- c h e d , with the resulting impression that there are two different oocysts: o n e with a two-layered, b r o w n and striated wall, and a n o t h e r with a single, thin and colourless wall w h i c h has n o striations (Figs 2 8 , 2 9 ) . T h e frequent loss o f o n e or m o r e layers o f the oocyst wall o f a given coccidian may create difficulties or even errors in diagnosis, as the nature o f the wall is a c h a - racter c o m m o n l y used to separate species (e.g. "rough"
versus "smooth"; W h e a t , 1 9 7 6 ) . W h e n such modifica- tions o f the oocyst wall are suspected, particular atten- tion n e e d s to b e given to all additional m o r p h o l o g i c a l characters.
W e are o f the o p i n i o n that t h e tissue-cysts p r e s e n t in the lamina propria o f the small intestine and, m o r e frequently, in the p a r e n c h y m a cells o f t h e liver, are n o t extra-intestinal s t a g e s o f E. bragancaensis n. sp., but that t h e y b e l o n g to a n o t h e r unidentified p r o t o - zoan parasite. T h e y b e a r a striking r e s e m b l a n c e to the latent cysts ( "kystes e n d o g e n i q u e s " ) o f Hepatozoon, found in various o r g a n s o f s n a k e a n d lizard hosts, particularly the liver (Landau et al, 1972). In the lizard, t h e s e cysts arise w h e n the animal ingests an infected a r t h r o p o d v e c t o r ( e . g . a m o s q u i t o ) and s p o - r o z o i t e s invade cells o f the liver and o t h e r organs.
H e r e t h e y e n c y s t and p r o d u c e a small n u m b e r o f e n d o z o i t e s (usually from 2 - 6 ) b y the p r o c e s s o f e n d o - d y o g e n y . T h e s e latent infective forms t h e n s e r v e as a s o u r c e o f i n f e c t i o n for s n a k e s p r e y i n g o n t h e lizards.
T h e a b s e n c e o f h a e m o g r e g a r i n e s in the b l o o d o f the bat u n d e r study suggests that it is not the definitive mammalian host, and that the cysts and c o n t a i n e d
128 Mémoire Parasite, 2000, 7, 123-129
e n d o z o i t e s m a y represent a "dead-end" for the para- site. Hepatozoon, probably H. didelphydis (d'Utra e Silva & Arantes, 1 9 1 6 ) , has b e e n recorded in a n u m b e r o f neotropical marsupials including Didelphis marsu- pialis, Philander opossum, a n d Metachirus nudicau- datus (d'Utra e Silva & Arantes, 1916; R e g e n d a n z &
Kikuth, 1928; Garnham & Lewis, 1958; D e a n e & D e a n e , 1961; Ayala et al, 1 9 7 3 ) : in addition, another u n n a m e d s p e c i e s h a s b e e n n o t e d in s p e c i m e n s o f the cricetid rodents Holochilus brasiliensis a n d Oryzomys capito from Amazonian Brazil (Lainson, 1 9 7 4 ) , and unidenti- fied haemogregarines have also b e e n recorded in Ama- zonian birds (Lainson et al, 1 9 7 0 ) All o f these hosts are abundant in north Brazil, a n d as P. macrotis is an insectivorous bat, its infection may well have originated following the ingestion o f mosquitoes o r another insect vector carrying the sporozoites o f a n y o n e o f these parasites. Oocysts containing mature sporocysts, typical o f the g e n u s Hepatozoon have b e e n e n c o u n t e r e d in a freshly dissected p h l e b o t o m i n e sandfly, Lutzomyia sp., from Para (unpublished o b s e r v a t i o n ) . Finally, if the parasite c a n tolerate the c h a n g e from a c o l d - b l o o d e d to a w a r m - b l o o d e d host there c o u l d b e a snake-bat- s n a k e life-cycle for t h e parasite. T h e infected bat w a s resting in a hollow tree-trunk - a favourite retreat for s o m e snakes.
A C K N O W L E D G E M E N T S
T
his work w a s supported b y a grant from the W e l l c o m e Trust, London ( t o RL) a n d financed, in part, by the Instituto Nacional d e Pesquisas da Amazonia, Brazil ( t o RDN). W e thank Constancia Maia Franco, Francisco Lima Santos a n d Walter M Campos for technical assistance, a n d Dra. Suely Marques o f the Museu Paraense Emilio Goeldi, B e l e m , for identification of the bat.REFERENCES
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Reçu le 17 février 2000 Accepté le 13 mars 2000
Parasite, 2000, 7, 123-129
Mémoire 129
