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OF THE AUSTRALIAN SLEEPY LIZARD TILIQUA RUGOSA BELONGS TO THE GENUS HEMOLIVIA

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T H E TICK-TRANSMITTED HAEMOGREGARINID

OF THE AUSTRALIAN SLEEPY LIZARD TILIQUA RUGOSA BELONGS TO THE GENUS HEMOLIVIA

SMALLRIDGE C.* & PAPERNA I.**

Summary :

Nymphae of Amblyomma limbatum Neumann, engorged on the Australian sleepy lizard Tiliqua rugosa Gray infected with haemogregarine blood-stage gametocytes, were studied by light and electron microscope 3-57 days after detachment. Examined ticks demonstrated haemogregarine oocysts and sporogonic stages. Oocysts found in the intestinal epithelium, were three to five arm star-shaped, and divided into numerous sporokinetes. The sporokinetes spread to various tissues and, after transforming into hard-walled sporocysts, divided into sporozoites. This course of development in the vector is characteristic of the genus Hemolivia Petit, Landau, Baccam & Lainson, 1 9 9 0 reported earlier from toads and ticks. The reported haemogregarinid is therefore described as Hemolivia mariae n. sp.

KEY WORDS : Hemolivia mariae n. sp., haemogregarine, Amblyomma limbatum, Tiliqua rugosa, Australia, development, ultrastructure.

Résumé : L'HÉMOGRÉGARINE TRANSMISE PAR LA TIQUE DU LÉZARD AUSTRALIEN TILIQUA RUGOSA APPARTIENT AU GENRE HEMOLIVIA Des nymphes d'Amblyomma limbatum Neumann, gorgées sur le lézard australien Tiliqua rugosa Gray infecté avec des gamétocytes d'hémogrégarine au stade sanguin, sont étudiés en microscopie optique et électronique 3 à 57 jours après leur détachement. On retrouve chez les tiques examinées des oocystes d'hémogrégarine et des stades sporogoniques. Les oocystes trouvés dans l'épithélium intestinal ont la forme d'étoiles à trois à cinq branches, et se divisent en de nombreux sporokinètes. Les sporokinètes gagnent différents tissus et, après leur transformation en sporocystes à paroi épaisse, se divisent en sporozoïtes. Cette séquence de développement au sein du vecteur est caractéristique du genre Hemolivia Petit, Landau, Baccam & Lainson, 1990, précédemment rapporté chez les crapauds et les tiques.

L'hémogrégarine rapportée est donc décrite sous le nom de Hemolivia mariae n. sp.

MOTS CLÉS : Hemolivia mariae n. sp., hémogrégarine, Amblyomma limbatum, Tiliqua rugosa, Australie, développement, ultrastructure.

S

l e e p y lizards Tiliqua rugosa Gray ( S c i n c i d a e ) from Mt Mary, S o u t h Australia w e r e f o u n d infected with haemogregarinids occurring in the circulating erythrocytes. T h e population is c o m m o n l y infested with the tick Amblyomma limbatum Neu- mann. N y m p h a e o f A. limbatum w e r e a l l o w e d to e n g o r g e o n h a e m o g r e g a r i n e i n f e c t e d lizards a n d e n g o r g e d ticks w e r e dissected 3-57 days after sponta- n e o u s detachment. T h e c o u r s e o f d e v e l o p m e n t in e n g o r g e d n y m p h a e and newly moulted adult ticks w a s established from examination o f G i e m s a stained smears from internal organs by light m i c r o s c o p e and from a study by transmission e l e c t r o n m i c r o s c o p y ( Т Е М ) . Tick viscera w e r e fixed in 2.5 % glutaralde- hyde in c a c o d y l a t e buffer (0.1M, pH 7 . 4 ) for 24 h at 4.0 °C, rinsed repeatedly in the s a m e buffer, post-fixed in 1.0 % o s m i u m tetroxide in the s a m e buffer for 1 h and, after rinsing in the s a m e buffer, dehydrated in

* Flinders University of South Australia, School of Biological Sciences, GPO Box 2100, Adelaide, 5001, Australia.

** Department of Animal Sciences of the Hebrew University of Jeru­

salem, Rehovot. 76-100. Israel.

Correspondence : Ilan Paperna.

graded alcohols and e m b e d d e d in Agar 1 0 0 ® resin (Agar C o . U K ) . T h i n s e c t i o n s , cut o n a R e i c h e r t

« Ultracut » with a diamond knife, were stained on-grid with uranyl acetate and lead citrate and e x a m i n e d in a J e o l 100 CX ТЕМ.

H a e m o g r e g a r i n e o o c y s t d e v e l o p m e n t and s p o r o g o n y in the tick t a k e s p l a c e in the gut epithelial cells.

Y o u n g o b l o n g oocysts 7-8 x 3 μm in size, lodged in a parasitophorous vacuole ( P V ) filled with d e n s e mate­

rial, contained nuclei o f h o m o g e n o u s granular n u c l e o ­ plasm with a large c o n s p i c u o u s nucleolus, few e l e c ­ tron-dense rhoptries and a few m i c r o n e m e s (Fig. 1 ) . Older oocysts, reaching 1 8 x 7 µm in size w e r e lodged in an e x p a n d e d PV with an undulated and folded wall (Fig. 2 ) . Cytoplasmic contents in such oocysts b e c a m e loaded with r i b o s o m e s and aggregates o f a granular substance, intersected by e n d o p l a s m i c reticulum, and also with lipid v a c u o l e s and amylopectin granules. At this stage, oocysts still retained a nucleus with large nucleolus and a fair n u m b e r o f m i c r o n e m e s (Fig. 2 ) . Smears from tick gut, e x a m i n e d b y light m i c r o s c o p e (LM) demonstrated three-arm stellate oocysts (Fig. 3 ) typical to the toad (Bufo marinus) h a e m o g r e g a r i n e H. stellata w h i c h d e v e l o p s in the tick Amblyomma rotondatimi (Petit et al., 1 9 9 0 ) . In addition to the c o m - Article available athttp://www.parasite-journal.orgorhttp://dx.doi.org/10.1051/parasite/1997044359

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SMALLRIDGE G. & PAPERNA I.

Fig. 1. Ultra-thin crosss ection through early stage oocyst, scale 1 µm, ТЕМ χ 15,100. Fig. 2. Young oocysts within an expanded PV. scale 1 pm, ТЕМ χ 9,500. Fig. 3. Stellate oocyst ( O o ) Giemsa stained smear, χ 235. Fig. 4. Differentiating stellate oocysts filled with crystalline bodies, around some of which sporokinete primordia (ps) start consolidating, scale 2 pm, ТЕМ χ 2,700. Fig. 5. Stellate oocyst, ripe filled with sporokinetes (sk), Giemsa stained smear, X 1,533.

Abbreviations to figures 1-10 : A, amylopectin granule; a, apical complex; c, crystalline body; hT, Tick's gut epithelial cell; L, lipid vacuole;

m, micronemes; mt. mitochondrion; n, nucleus; Oo, oocyst: PV, parasitophorous vacuole; r. rhoptry; rl, rhoptry-like organelle; S, sporo­

kinete; z., sporozoite.

3 6 0 Note de recherche Parasite, 1997, 4, 359-363

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HAEMOLIVIA МАМАЕ N. SP.

monly occurring three-arm oocysts there w e r e s o m e with four or five arms, the length o f e a c h arm m e a ­ suring from 142 to 201 pm. T h e granular aggregates s e e n in the y o u n g e r o o c y s t s c o u l d have b e e n the analgen for the crystalline b o d i e s which fill the cyto­

plasm o f the older (stellate) o o c y s t s ; around these b o d i e s w e r e consolidating the division p r o g e n y o f these oocysts (Fig. 4 ) . T h e end-product o f the o o c y s t e n d o g e n o u s division (Fig. 5 ) w e r e o b l o n g motile stages, 1 5 - 1 6 x 5-6 p m in size, w h i c h r e s e m b l e d the s p o r o k i n e t e s w h i c h are formed b y the H. stellata oocysts. Newly formed s p o r o k i n e t e s had an apical c o m p l e x a c c o m p a n i e d b y r h o p t r y - l i k e o r g a n e l l e s consisting o f fine granular substance with a superficial layer o f electron dense material. A crystalline substance filled almost the entire s p o r o k i n e t e body, o n both sides o f the h o m o g e n o u s nucleus. Older sporokinetes found scattered throughout the tick intestine as well as in extra-intestinal organs w e r e o f variable sizes (from 1 5 - 1 8 χ 5-11 pm to 19-24 x 8-14 pm, apparently prior e n c a p s u l a t i o n ) and altogether differed from the early o n e s in the texture and contents o f their cyto­

plasm; they also c o n t a i n e d many minute m i c r o n e m e s , and had their crystalline mass subdividing. All sporo­

kinetes w e r e intracellular, l o d g e d within either an e x p a n d e d PV with wavy wall or a narrow space b o u n d by a single lamella (Fig. 7 ) . Differentiation o f s p o r o ­ kinetes into sporocysts lead to the thickening o f their walls w h i c h resulted in their increased resistance to fixation and infiltration (Figs. 8 and 9 ) . Division in these hard-walled, 2 9 - 3 3 x 1 4 - 1 8 pm s p o r o c y s t s yielded n u m e r o u s ( 8 - 2 0 ) sporozoites (Fig. 1 0 ) .

T h e life cycle in the tick has b e e n found to b e very similar to the d e v e l o p m e n t cycle o f the toad parasite H. stellata d e s c r i b e d from the tick A. rotundatum (Petit et al, 1 9 9 0 ) , with the formation inside the gut epithelial cells o f stellate oocysts. T h e s e oocysts like­

wise formed, through e n d o g e n o u s division, mobile s p o r o k i n e t e s w h i c h spread into other gut cells before transforming into sporocysts containing sporozoites. In the presently d e s c r i b e d s p e c i e s , s p o r o k i n e t e s w e r e found spreading throughout the tick tissue also into extra-intestinal locations. This cycle differs from many haemogregarines o f the genus Hepatozoon developing in m o s q u i t o e s ' h a e m o c o e l (Mackerras, 1 9 6 2 ; Ball &

Oda, 1 9 7 1 ; Bashtar et al, 1 9 8 4 ; W o z n i a k & Telford, 1 9 9 1 ) . In Hepatozoon the p r o g e n y o f sporocysts, divi­

ding into sporozoites remained often located within the parent o o c y s t wall (Bashtar et al, 1 9 8 4 ; Lowichik et al, 1 9 9 3 ) . Hemolivia sporokinetes, unlike the sporo­

cysts formed in Hepatozoon retain a distinct apical c o m p l e x , fine structural features o f mobile stages (such as the ookinete o f haemosporidians, Paterson & Desser, 1 9 8 9 ) . D e v e l o p m e n t o f oocysts in the vector's gut cells

have b e e n also reported in Hepatozoon mauritanicus o f the land tortoise transmitted via the tick Hyalomma aegyptium (Brumpt, 1 9 3 8 ; Michel, 1 9 7 3 ) and a skink's Hepatozoon lygosomarum transmitted via mites (Allison

& D e s s e r , 1 9 8 1 ) , stellate o o c y s t s in these s p e c i e s , h o w e v e r , w e r e not found. Their t a x o n o m i e status is presently revised ( s e e Landau & Paperna, s a m e issue).

S p o r o g o n i e d e v e l o p m e n t o f Hepatozoon o c t o s p o r e i from skinks, in mites was shown, however, to o c c u r in the h a e m o c o e l ( R a m a n a d a n Shanavas & Rama- chandran, 1 9 9 0 ) . Sporogonie d e v e l o p m e n t in the hae­

m o c o e l has b e e n a l s o r e p o r t e d in m a m m a l i a - h o s t Hepatozoon: H. canis in the tick Haemophysalis lon- gicornis (Murata et al, 1 9 9 5 ) , and Η. balfourí in the mite Haemolaelaps aegyptius (Hoogstraal, 1961). Worth consideration also is the similarity b e t w e e n Hemolivia and Karyolysus. O o g e n e s i s and sporulation o f the latter h a e m o g r e g a r i n e takes p l a c e in the lumen or the epithelium o f the gut o f dermanyssid mites, and simi­

larly leads to the formation o f sporokinetes. T h e s e , unlike those o f Hemolivia, penetrate mite's eggs and are transovarially transmitted to the vector's offspring ( R e i c h e n o w , 1 9 2 1 ; Svahn, 1 9 7 5 ) .

TAXONOMIC STATUS Hemolivia mariae n. sp.

Hosts: Tiliqua rugosa Gray and Amblyomma limbatum N e u m a n n

G e o g r a p h i c locality: Mount Mary, South Australia.

Etymology: Named by its type locality.

T y p e material: D e p o s i t e d in t h e S o u t h Australian Museum.

Paratypes: D e p o s i t e d in Muséum National d'Histoire Naturelle, Paris.

DESCRIPTION

In Giemsa stained b l o o d smears, mature, e n c a p s u ­ lated g a m e t o c y t e s reach 1 8 x 5 pm. Oocysts develo­

ping in the ticks gut epithelium are stellate, with three to five arms, each 142-201 ( m e a n 1 7 7 ) pm in size. T h e latter divide into mobile sporokinetes ( 1 5 - 2 3 . 8 x 5.6- 14 pm in size) w h i c h spread T H R O U G H O L I T the tick tis­

sues w h e r e they b e c o m e established as hard-walled oval sporocysts (29-34 x 14-18 pm in size), divided into 8-20 sporozoites ( 1 2 - 1 4 χ 1.4-2.1 pm in size).

DIFFERENTIAL DIAGNOSIS

Conspecificity with H. stellata is unlikely o n a c c o u n t s o f differences in host taxa (skink vs. toad), and g e o ­ graphic location. B. marinus ( c a n e toads) the natural hosts o f H. stellata have b e e n introduced into Australia, but, thus far n o n e have b e e n found infected with either H. stellata nor ticks ( S p e a r e , 1 9 9 0 ) , and an attempt to e x p e r i m e n t a l l y infect c a n e toads failed

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SMAI.LRIDGE С. & PAPERNA I.

Fig. 6. Newly formed sporokinetes inside the oocyst, scale 1 ц т , ТЕМ χ 6,200. Fig. 7. Variable size sporokinetes inside gut epithelial cell, filled with fragmented crystalline body ( c ) , scale pm, ТЕМ χ 5,775. Figs. 8 and 9. Hard-walled sporocyst before division to sporozoites, scales 1 pm, ТЕМ x 8,700 and x 8,800. Fig. 10. Sporocysts (S) containing sporozoites (z), Giemsa stained smear X 1,000.

Abbreviations to figures 1-10 : A, amylopectin granule; a, apical complex; c, crystalline body; hT, Tick's gut epithelial cell; L, lipid vacuole;

m, micronemes; mt, mitochondrion; n, nucleus; Oo, oocyst; PV, parasitophorous vacuole; r. rhoptry; rl. rhoptry-like organelle; S, sporo- kinete; z, sporozoite.

3 6 2 Note de recherche Parasite, 1997, 4, 359-363

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НAEMOLIVIA MARIAE N.SP.

(Smallridge, unpublished). Infection with both orga­

nisms in native toads in Brazil is highly prevalent (Lainson & Paperna, unpublished).

REFERENCES

ALLISON B. & DESSER S.S. Developmental stages of Hepatozoon lygosomarum (Dore, 1919) comb. n. (Protozoa: Haemo- gregarinidae). a parasite of a New Zealand skink leiolo- pisma nigra. Journal of Parasitology, 1981, 67, 852-858.

BALL G.H. & ODA S.N. Sexual stages in the life history of the hemogregarine Hepatozoon rarefaciens (Sambon &

Seligman, 1907). Journal of Protozoology, 1971, 18, 697- 700.

BASHTAR A.R., BOULOS R. & MEHLIIORN, R. Hepatozoon aegypti nov. sp. 1. Life cycle. Zeitscbriftfur Parasitenkunde, 1984,

70, 29-41.

BRUMPT E. Formes évolutives d'Haemogregarina mauritanica chez la tique Hyalomma syriacum. Annales de Parasito­

logie Humaine et Comparée, 1938, 16, 350-361.

HOOGSTRAAI. H . The life cycle and incidence of Hepatozoon balfouri (Laveran, 1905) in Egyptian Jerboas (Jaculus spp.) and mites (Haemolaelaps aegyptius Keegan, 1956). Journal

of Parasitology, 1961, 8, 231-248.

LowicHiK Α., LANNERS Η.Η., LOWRIE R.C. & MEINERS N.E. Game- togenesis and sporogony of Hepatozoon mocassini (Api- complexa: Adeleina: Hepatozoidae) in an experimental mosquito host, Aedes aegypti. Journal ofEukaryotic Micro­

biology, 1993, 40, 287-297.

MACKERKAS J. The life history of a Hepatozoon (Sporozoa: Ade- leidea) of varanid lizards in Australia. Australian Journal of Zoology, 1962, 10, 55-44.

MICHEL J.-C. Hepatozoon mauritanicum (Et. et Ed. Sergent, 1904) η. comb., parasite de Testudo graeca-. redescription de la sporogonie chez Hyalomma aegyptium et de la schi­

zogony tissulaire d'après le matériel d'E. Brumpt. Annales de Parasitologie humaine et comparée, 1973, 48, 11-21.

MURATA T., INOUE M . , TAURA Y . , ABE H . & FUHLSAKI К . Detec­

tion of Hepatozoon cani oocysts from ticks collected from infected dogs. Journal of Veterinary and Medical Sciences, 1995, 57, 111-112.

PATERSON W.B. & DESSER S.S. The polar ring complex in ooki­

netes of Leucocytozoon simondi (Apicomplexa: Haemo- sporina) and evidence for a conoid in haemosporidian ookinetes. European Journal of Protistology, 1989, 24, 244-251.

PETIT G., LANDAU I., BACCAM D. & LAINSON R . Description et cycle biologique â'Hemolivia stellata η. g., η. sp., hemo­

gregarine de crapauds brésiliens. Annales de Parasitologie Humaine et Comparée, 1990, 65, 3-15.

RAMANANDAN SHANAVAS K. & RAMACHANDRAN P . Life history of Hepatozoon octosporei sp. п., a new hemogregarine from the skink, Mabuya cannata (Schneider), with notes on the in vitro excystment of its oocysts. Archiv fiir Protisten- kunde, 1990, 138, 127-137.

REICHENOW E. Die hamococcidien der Eidechsen. Vorbemer- kungen und I. Teil: Die Entwicklungsgeschichte von Karyolysus. Archiv fur Protistenkunde, 1921, 42, 179-291.

SPEARE R. A review of the diseases of the Cane Toad, Bufo marinus, with comments on biological control. Australian Wildlife Research, 1990, 17, 387-410.

SVAHN K. Blood parasites of the genus Karyolysus (Coccidia, Adeleidae) in Scandinavian lizards. Description and life cycle. Norwegian Journal of Zoology, 1975, 23, 277-295.

WOZNIAK E. & TELFORD S.R. Jr. The fate of Hepatozoon spe­

cies naturally infecting Florida black racers and water snakes in potential mosquito and soft tick vectors and his­

tological evidence of pathogenicity in unnatural host spe­

cies. International Journal for Parasitology, 1991, 21, 511- 516.

R e ç u le 10 juin 1 9 9 7 A c c e p t é l e 17 juillet 1 9 9 7

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