Distribucion Estacional DeTheileria En La GarrapataHyalomma Anatolicum Anatolicum De Un Area Endemica De Haryana, India

Trop. Anita. Htth Prod, (1994) 26, 241-246

SEASONAL DISTRIBUTION OF THEILERIA IN HYALOMMA ANA TOLICUM ANA TOLICUM TICKS OF AN ENDEMIC AREA OF HARYANA, INDIA A. K. SANGWAN,S. S. CHAUDHRI,N. SANGWANand R. P. GUPTA Haryana Agricultural University, Veterinary Parasitologieal Research Station, Uchani, Karnal-132 001, Haryana, India

SUMMARY

The effect of season on the capacity of Hyalomma anatolicum anatolicum ticks to transmit Theileria was studied by detecting Theileria sporoblasts in the salivary glands of 647 adult ticks moulted in winter (November 1990 to March 1991) and 677 adult ticks moulted in the summer-rainy season (June to August 1991). The intensity (number of infected acini per infected tick) and abundance (number of infected acini per tick examined) of Theileria sporoblasts were significantly (P < 0.05) higher in winter moulted ticks (10.75 and 2.23 respectively) than the summer-rainy season moulted ticks (7"31 and 1"77 respectively). The prevalence of infected moulted ticks was not significantly higher in the summer-rainy season (24"22%) than in the winter (20.71%). A higher percentage of winter moulted ticks had high numbers of infected acini (>11~infected tick) than the summer-rainy season moulted ticks, while the trend was reversed for low numbers of infected acini (5~infected tick), being 47.76% for winter and 73.78%for the summer-rainy season. It was concluded that the winter of Haryana is more favourable to the developing theilerial stages in the ticks than the summer-rainy season. INTRODUCTION

Though bovine tropical theileriosis is a serious challenge to the livestock improvement programme in India, the epidemiological details have not been adequately studied. The detection of Theileria prevalence and intensity in the vector ticks is a component in the study of the epidemiology of theileriosis. Work on this aspect has been initiated with Theileria parva in Kenya (Walker et al., 198t), with Theilera annulata in Sudan (Walker et al., 1983) and in India (Sangwan et al., 1986). The epidemiology of theileriosis differs from one region to another because of different tick vectors and variations in their biology (Uilenberg, 1976). Unfavourable temperature and humidity levels lead to lesser development of Theileria parasites in ticks under field conditions (Young, 1981). While the humidity affects the survival and activity of tick instars, temperature affects both the rate of development and survival of the ticks and their theilerial parasites. Young and Leitch (1981) demonstrated that exposure of pre-moult and post-moult nymphal Rhipicephalus appendiculatus ticks to lower diurnal temperature rhythm (25°C 7°C) produced higher T. parva infection in them than those maintained at higher temperature rhythm (37°C-18°C or 32°C-24°C) or at a constant temperature of either 28°C or 23°C. The variations in temperature between 4°C to 40°C were also seen to affect the moulting rate of Hyalomma anatolicum anatolicum and transmission of theilerial parasites significantly (Das and Sharma, 1991) revealing that a constant temperature of 28°C and 80% relative humidity were most favourable for moulting success and transtadial transmission of T. annulata. To show the 241

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practical implications of such observations in the Theileria endemic state o f Haryana, the comparison of Theileria transmission potential of tick populations existing in winter and summer-rainy seasons representing the 2 generations completed in a year, are presented here. MATERIALS AND METHODS

Tick collection Recently moulted, unfed adult H. a. anatolicum were collected from soil and other hiding places in animal houses in villages endemic for Theileria in Karnal district (29043' N, 76058' E) in Haryana, India, twice during 1991. The first collection was done during late March and April which was the time when adult ticks appeared after 4 winter months (November to February) or more of moulting and diapause. Environmental temperature during this season was low and ticks took longer in moulting and underwent a long diapause. The second period of collection was during July and August which was the rainy season and temperature was quite high (Table I). Engorged nymphs took only 10 to 20 days for moulting during the rainy season without any diapause. Generally 2 life cycles are completed in a year by H. a. anatolicum ticks in this region. Examination of salivary glands for Theileria spiroblasts Hungry adult ticks were prefed for 3 days on rabbits before their salivary glands were removed. The glands were stained by the methyl-green pyronin staining method as described by Walker et al. (1979) and later modified by Irvin et al. (1981). Meteorological data Mean monthly maximum temperature (°C), mean monthly minimum temperature (°C), morning and evening relative humidity (RH%) and morning and evening soil temperature (°C) at 5 cm depth (Table I) were obtained with the courtesy of the Director, Central Soil Salinity Research Institute, Karnal. TABLEI Meteorological data of Karnal ( Haryana, India) for winter (November, 1990 to March, 1991) and summerrainy season (June, 1991 to August, 1991) seasons Temperature (mean)

Relative humidity

Soil temperature (at 5 era depth)

Month

Year

Season 1

Max. (°C)

Min. (°C)

Morning (%)

Evening (%)

Morning (°C)

Evening (oC)

Nov. Dec. Jan. Feb. March

1990 1990 1991 1991 1991

W W W W W

27-9 22-3 19.2 22.7 27.1

12"0 7-6 5.5 9-0 12-6

85 88 92 91 81

39 49 55 53 41

15-0 10.5 8.4 l 1.7 17"1

27"9 22-0 20-1 24.7 30-7

June July August

1991 1991 1991

S-R S-R S-R

36"t 36'0 32.3

24"6 27"3 25-2

74 79 90

49 59 73

28"2 31"6 29.1

40.3 42-5 37.3

W = Winter. S-R = Summer-rainy.

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THEILERIA IN HYALOMMA TICKS TABLE II

Comparison of Theileria infections in winter (November, 1990 to March, 1991) and summer-rainy (June to August, 1991) season moulted Hyatomma anatolicum anatolieurn ticks Moulted ticks

Sample size

Prevalence (%)

Mean intensityI

Winter Summer-rainy Probability

647 677

20-71 24.22 >5%

10-75 7-31 0-05). However, intensity and abundance of TheiIeria infected acini of the 2 tick populations were significantly (P < 0-05) different which could be correlated to the variations in environmental temperatures of winter and summer-rainy seasons. Young and Leitch (1981) demonstrated that the pre-moult and post-moult nymphal R. appendicu[atua ticks, when exposed to natural conditions or to a similar diurnal temperature rhythm (25°C-7°C) in the laboratory, also had higher T. parva infection than those maintained under constant temperature (28°C and 23°C) or at diurnal temperature rhythms of 37°C-18°C or 32°C-24°C. It was suggested that the exposure of nymphs to 25°C-7°C diurnal temperature rhythm lowers their metabolic rate which is suitable for the development and persistence of the sexual

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stages of Theileria. This would also allow the efficient fusion of microgametes and macrogametes resulting in the formation of a large number of zygotes and later stages which are detected in the salivary glands. The winter temperature range (27.9°C-5-5°C) of Karnal (Haryana) provides ideal conditions for the development of Theileria within ticks. In contrast, the temperature range (36.1°C-24.6°C) of the summer-rainy season proved harmful for the developing stages of Theileria, possibly due to rapid digestion of the blood meal by nymphal ticks (Young 1981) which might not have favoured the maximum formation of theilerial zygotes. High constant temperature of 33°C or above for shorter or longer periods was demonstrated to be detrimental for the development of T. parva and for its transmission (Young 1981). In actual field conditions ticks are subjected to the temperature of a few centimetres below the soil (Table I) which is always slightly higher than environmental temperature and often reaches above 37°C in the summer-rainy season thus further damaging the developmental Theileria stages in ticks. This explains the lower intensity and abundance during the summer-rainy season but simultaneously reveals that diurnal changes bring the temperature below 33°C almost daily which probably does not inhibit the development of Theileria completely in ticks. It is intriguing to note the non-significant difference in the prevalence of Theileria in 2 tick populations while there is significant difference in the intensity of infection. The narrow difference between the upper temperature range of winter months and lower temperature of summer-rainy season months are perhaps responsible for the non-significant difference in the prevalence of Theileria in the 2 tick populations. The lower range of temperature during December and January and the upper range of temperature during June and July may cause reduction in moulting success and transtadial transmission of Thefleria but it seems that the lower temperature during winter is not as harmful to the developing theilerial stages as the upper range during the summer-rainy season. In addition to temperature, duration is also important for the success of transtadial transmission of Theileria (Young et al., 1983). The higher abundance of Theileria resulting from longer durations (150 days) of moulting and diapause is similar to higher abundance seen in the present study with comparative period (120 to 150 days). The relative humidity range of Karnal (Haryana) is well suited to H. a. anatolicum ticks and may not have much affect on the rate of development and survival of this semi-arid and arid zone adapted tick and also on its theilerial parasites. Therefore, it would appear that the diurnal temperature rhythm of winter months is more beneficial for the production of high infections of T. annulata in H. a. anatolicum ticks than the temperature rhythm of the summer-rainy season. However, fatal theileriosis is a common occurrence throughout the period (late March to early November) when Hyalomma ticks are found on cattle in Haryana. It makes the integrated use of acaricides, anti-theilerial chemotherapy and live vaccine against theileriosis most important during most of the year in the epidemiological conditions of Haryana. ACKNOWLEDGEMENTS This work was carried out under the scheme Control of Parasitic Diseases in Livestock funded by National Agricultural Research Project of the Indian Council of Agricultural Research. Accepted for publication November 1993

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REFERENCES

CONOVER,W. J. (1980). Practical Nonparametric Statistics. 2nd ed. Wiley, New York. DAS, S. S. & St~AgMA,N. N. ( 1991). Effect of temperature on transtadiat transmission of Theileria annulata in Hyalomma anatolicum anatolicum ticks. Veterinary Parasitology, 40, 155-158. IRVlN, A. D., BOARER,C. D. H., DOSSELAERE,D. A. E., MAHAN,S. M., MASAKE,R. & OCAMA,J. G. R. (1981). Monitoring of Theileria parva infection in adult Rhipicephalus appendiculatas ticks. Parasitology, 82, 137-147. SANGWAN,A. K., CHHABP.A,M. B. & SAMAI,a'ARAY, S. (1986). Theileria infectivity of Hyalomma ticks in Haryana, India. Tropical Animal Health and Production, 18, 149-154. UZL~NSSRG, G. (1976). Tick-borne livestock diseases and their vectors. 2. Epizootiology of tick-borne diseases. World Animal Review, 17, 8-15. WALK~R,A. R., McK~LLAg, S. B., BELL,L. J. & BROWN,C. G. D. (1979). Rapid quantitative assessment of Theileria infection in ticks. Tropical Animal Health and Production, U , 21-26. WALKER,A. R., YOUNG,A. S. & LErrCH, B. L. 098t). Assessment of Theileria infection in Rhipicephatus appendiculatus ticks collected from field. Zeitshrift fur Parasitenkunde, 65, 63-69. WALKER,A. R., LArIF, A. A., MORZARXA,S. P. & JONG~AN,F. (1983). Natural infection rates of Hyalomma anatolicum anatolicum with Theileria in Sudan. Research in Veterinary Science, 35, 87-90. YOUNg3,A. S. (1981). Advances in the Control of Theileriosis. (Eds A. D. Irvin, M. P. Cunningham and A. S. Young). Martinus Nijhoff, The Hague, pp 38-55. YOUNG,A. S. & LErr¢l~, B. L. (1981). Epidemiology of East Coast fever: some effects of temperature on the development of Theileria parva in the tick vector Rhipicephalus appendiculatus. Parasitology, 53, 199-211. YOUNG, A. S, LErrct~, B. L., DOLAN,T. T., NEWSON, R. M., NGUM~, P. N. & OMWOYO,P. L. (1983). Transmission of Theileria parva by a population of Rhipicephalus appendieulatus under simulated natural conditions. Parasitology, 86, 255-267. DISTRIBUTION SAISONNIERE DE THEILERIA CHEZ LES TIQUES HYALOMMA ANATOLICUM ANATOLICUM D'UNE REGION ENDEMIQUE D'HARYANA, INDE Rtsum~mL'influence de la saison sur la capacit6 des tiques" Hyalomma anatolicum anatolicum ~ transmettr~ Theileria a 6t6 6tudi6 par d&ection de sporoblastes de Theileria dans les glandes salivaires de 647 tiques adultes 6closes en hiver (novembre 1990 fi mars 1991) et 677 6closes en saison des ptuies d'tt6 (juin/t aoftt 1991). L'intensit~ (nombre d'acini infectts par tique infect~e) et l'abondance (hombre d'acini infect~s par tique examinee) de sporoblastcs de Theileria 6tait significativement plus 61evtes (P < 0,05) chez les tiqucs prelevtes rhiver (10,75 et 2,23 respectivement) que chez ceres rtcolttes 1"6t6 en saison des pluies (7,31 et 1,77 respectivement). La prtvalence des tiques infecttes parmi les tiques 6:loses en saison des pluies d'&6 (24,22 p. 100) n'&ait pas significativement plus 61ev6 que celle observte parmi les tiques 6closes en hiver (20,71 p.100). Un pourcentage 61ev6de tiques 6closes en hiver montrait un hombre plus 61ev6 d'acini infectts (>11/tique infect&:) que celui des tiques ~¢loscs 1'6t6, alors que l'inverse se produisait avec des nombres peu 6tev~s d'acini infectts (5/tique infectte), soit 47,76 p.100 en hirer contre 73,78 p.100 en 6th. I1 enest dbduit que l'hiver d'Haryana est plus favorable aux stadcs de dtveloppement des theileries chcz les tiqucs que la saison ptuvieuse d'ttt. DISTRIBUCION ESTACIONAL DE THEILERIA EN LA GARRAPATA HYALOMMA ANA TOLICUM ANA TOLICUM DE UN AREA ENDEMICA DE HARYANA, INDIA Resumen--Se estudi6 el efecto de la estaci6n del afio en la capacidad della garrapata Hyalomma anatolicum anatolicum para transmitir Theileria, detectado esporoblastos de Theileria en las gl~indulas salivates de 647 garrapatas adultas que mudaron en invierno (noviembre 1990 a marzo 1991) y de 677 garrapatas adultas que mudaron en la estaci6n lluviosa de verano (junio a agusto de 1991). La intensidad (nftmero de acinos infectados por garrapata infectada) y abundancia (nftmero de acinos infectado por garrapata examinada) de esporoblastos de Theileria fue significtavamente (P < 0.05) mils alta en las garrapatas que mudaron en invierno (10-75 y 2"23, repectivamente) queen aquellas que mudaron en verano (7-31 y 1-77, respectivamente). La prevaliencia de garrapatas infectadas clue mudaron en el verano lluvioso (24-22%), no rue significativamente mils alta que en aqucltas garrapatas que mudaron en invierno (20-71%). Un porcentaje naris alto de garrapatas que mudaron en invierno tuvo el mils alto nfimero de acinos infcctados (>l 1/garrapatas infectadas) que tas garrapatas que mudaron en verano. Lo contrario se encontr6 para un pequefio ntmero de acinos infectados (5/garrapata infectada), siendo 47.76% para el invierno y 73.78% para el verano Uuvioso. S¢ concluye que el invierno de Haryana es n~s thvorable para el desarrollo de los estadi6s de Theileria en las garrapatas que el verano lluvioso.