COMPARISON OF EFFECTS OF LOW
AND HIGH TICK INFESTATIONS ON ACQUIRED CATTLE TICK RESISTANCE:
HYALOMMA MARGINATUM MARGINATUM
SAHIBI H.*, RHALEM A.* & TIKKI N.*
S u m m a r y :
Three Holstein calves were infested with low numbers of ticks, two or three pairs of adults Hyalomma marginatum marginatum in cloth bag daily for 2 1 days. Infestation was carried out during tick proliferation periods. Two months later, cattle leads were challenged with 1 0 0 pairs of ticks. Another group of three Holstein calves were infested five times with 100 pairs of adult ticks of the same species. The five infestations were performed two weeks from the previous infestation. Three tick characteristics were recorded for each experiment: survival to detachment, females weight at detachment and egg mass weight. Light continuous infestations did not cause a significant change in this parameter, but every parameter declined gradually in the heavy infestations.
Female and egg mass weight reached a significant difference from the first infestation by the fourth infestation. The circulating antibodies anti-salivary glands of Hyalomma m. marginatum showed that light infestation may induce like immuno-suppression.
However, there is an inverse relationship between these antibodies and manifestation of resistance when calves were heavily infested.
This is discussed in relation to a fraction of produced antibodies against protective antigens, and participation of another effector mechanism.
KEY W O R D S : ticks, Hyalomma marginatum marginatum, low and continuous infestations, repeatedly heavy infestations, resistance, humoral response.
Résumé : COMPARAISON DES EFFETS D'INFESTATIONS LÉGÈRES ET MASSIVES, PAR DES TIQUES HYALOMMA MARGINATUM MARGINATUM, SUR L'ACQUISITION D E LA RÉSISTANCE PAR LES BOVINS
Trois bovins de race Holstein ont été infestés par deux à trois paires de tiques adultes de l'espèce Hyalomma m.
marginatum, chaque jour pendant 21 jours. Les infestations ont été réalisés pendant la période d'activité des tiques. Une infestation d'épreuve avec 100 paires de tiques a été faite deux mois après la dernière infestation. Un second groupe de trois bovins de la même race a fait l'objet de cinq infestations massives ( 100 paires de tiques par infestation) à intervalles de 15 jours et cela après gorgement de la dernière tique de l'infestation précédente. Au cours de cette étude trois paramètres ont été suivis : la survie au détachement, le poids des tiques femelles et enfin la masse d'oeufs. Les infestations continues et modérées n'ont pas provoqué de changement significatif des paramètres suivis. Par contre, les infestations massives ont causé une baisse progressive et
significative de ces paramètres. Le poids des tiques femelles et la masse d'œufs marquent une baisse significative à partir de la 4è- 5e infestation. Les anticorps circulant dirigés contre les glandes salivaires de la tique Hyalomma m. marginatum ont montré que les infestations modérées induisent probablement une immuno- suppression. Toutefois, une relation inverse a été constatée entre les anticorps circulants et l'acquisition de la résistance chez les animaux massivement infestés, ceci est discuté en relation avec la fraction des anticorps formée contre les antigènes protecteurs et avec la participation d'un autre mécanisme effecteur.
MOTS CLÉS : tiques, Hyalomma marginatum marginatum, infestations légères et continues, infestations lourdes et répétées, résistance, réponse humorale.
INTRODUCTION
T
icks a n d d i s e a s e s they transmit to animals are o f w o r l d w i d e e c o n o m i c i m p o r t a n c e . T h e cost o f a c a r i c i d e applications, the issue o f environ- mental pollution a n d the d e v e l o p m e n t o f r e s i s t a n c e to a c a r i c i d e s ( B e u g n e t et al, 1994) h a v e m a d e a r e s e a r c h priority to establish c h e a p , effective a n d e n v i r o n m e n - tally a c c e p t a b l e tick c o n t r o l m e t h o d s . T h e r e is a large b o d y o f e v i d e n c e that s h o w s that animals d e v e l o p* Département de Parasitologie et Maladies Parasitaires, Institut Agronomique et Vétérinaire Hassan II, B.P. 6202, Rabat-Instituts, Maroc.
Correspondence : Hamid Sahibi.
Fax : 212 7 68 04 24/7 77 81 35.
resistance against ticks u n d e r laboratory c o n d i t i o n s ( W i k e l , 1 9 8 8 ; Fivaz, 1990; R e c h a v et al, 1991; W i k e l et al, 1994). R e p e a t e d infestations resulted in signifi- cant reduction in the n u m b e r o f ticks that successfully c o m p l e t e d their b l o o d m e a l , a n d in the m e a n w e i g h t o f ticks feeding o n resistant hosts. All studies d e m o n s - t r a t e d t h a t g u i n e a p i g s a n d r a b b i t s s u b j e c t e d t o r e p e a t e d infestations with ticks o f different s p e c i e s a c q u i r e d r e s i s t a n c e (Fivaz, 1990; Fielden et al., 1992;
Losel et al, 1993; R e c h a v et al, 1994; R e c h a v &
Fielden, 1995). Small ruminants also c a n a c q u i r e resis- t a n c e against ticks. I n d e e d , Barriga et al. (1991) found that repeated infestations with 100 pairs o f Amblyomma americanum (L.) i n d u c e strong but i n c o m p l e t e pro- t e c t i o n in s h e e p b y t h e fourth or fifth infestation.
Adamson et al. (1991) demonstrated that goats acquired Article available athttp://www.parasite-journal.orgorhttp://dx.doi.org/10.1051/parasite/1998051069
resistance to larvae o f Amblyomma hebraeum ( K o c h ) after to three infestations. It has long b e e n r e c o g n i z e d that various cattle b r e e d s differed in their r e s p o n s e to tick infestations ( R e c h a v & Kostrzewski, 1 9 9 1 ; Fivaz et al, 1 9 9 1 ; Garris & Hair, 1 9 9 2 , Ali & D e Castro; 1 9 9 3 , Moran et al, 1 9 9 6 ) . At present, acquired resistance o f cattle to natural tick infestation is w e l l - d o c u m e n t e d ( A m o o & D i p e o l u , 1992; Dipeolu et al., 1 9 9 2 ; Barriga et al., 1 9 9 3 ) . However, Sahibi et al. ( 1 9 9 7 a ) recently demonstrated failure due to age and b r e e d to acquire resistance u n d e r field conditions. In this paper, l o w intensity infestation under natural conditions in the field is c o m p a r e d to the effect o f high intensity, repeated infestations with adult ticks Hyalomma m. margi
natum, u n d e r controlled laboratory conditions.
MATERIALS AND METHODS
TICKS
A
c o l o n y o f H. m. marginatum K o c h , 1 8 4 4 ticks w a s maintained at Institut A g r o n o m i q u e Vétérinaire Hassan II, Rabat-Morocco, at 8 5 ± 5 % relative humidity, and 2 8 ° ± 1 °C. Larvae and nymphs w e r e confined to ears o f rabbits using cloth-bags, and adults w e r e fed o n s h e e p using the s a m e m e t h o d . In all experiments, four to five w e e k - o l d adults ticks w e r e used to infest cattle. T o monitor the effect o f host r e s i s t a n c e o n e g g - l a y i n g a n d e g g - h a t c h i n g , t h e e n g o r g e d females w e r e kept individually in glass tubes and maintained at a constant temperature o f 2 8 °C and 8 5 % relative humidity for 3 0 days.
HOSTS
Nine Holstein calves ( m a l e s ) , height to twelve months old weighing 7 0 - 8 0 kg w e r e divided into three groups o f three animals e a c h . T h e animals w e r e carefully e x a mined for e v i d e n c e o f tick infestation as part o f a tho
rough physical e x a m . During the e x p e r i m e n t s , they w e r e kept o n a small plot with bare dry ground which prevented spontaneous n e w tick infestation. T h e calves w e r e fed artificially with cattle pellets and fresh alfalfa, and provided fresh water ad libitum.
• Experiment 1
Effect of low level repeated infestations under laboratory conditions.
Under field conditions, cattle are infested with an ave
rage o f two o r three tick pairs per day. O u r experi
ment c o i n c i d e d with the s e a s o n o f high risk infesta
tion (from J u n e to August ) . Each calf o f the first group r e c e i v e d two or three pairs o f ticks every day for a 21 day period. F e m a l e ticks that had d e t a c h e d w e r e
c o l l e c t e d daily until they all c o m p l e t e d their feeding and detached. T w o months after the e n d o f the last infestation, the cattle w a s c h a l l e n g e d with 100 pairs o f H. m. marginatum adult ticks. Survival to d e t a c h m e n t , e n g o r g e m e n t weight and weight o f the e g g mass w e r e r e c o r d e d to assess resistance.
• Experiment 2
Effect of high intensity infestations on tick characteristics.
Calves o f the s e c o n d group w e r e s u b j e c t e d to five c o n s e c u t i v e infestations with 1 0 0 pairs ( 1 0 0 males and
100 f e m a l e s ) o f H. m. marginatum e a c h . Ticks w e r e deposited in a cloth s a c k and confined to both ears o f the calves. Sacks w e r e e x a m i n e d daily and the n u m b e r o f e n g o r g e d ticks w a s r e c o r d e d until all ticks w h i c h e n g o r g e d had detached. Each female was w e i g h e d and incubated in individual containers ( 8 / 2 . 5 c m ) until the e n d o f the oviposition period, or discarded after 3 0 days if it failed to oviposit. T h e weight o f the egg mass was also recorded. T h e five infestations w e r e d o n e at t w o w e e k intervals, after the last tick from the previous infestation had detached.
SEROLOGY
Calves o f the first e x p e r i m e n t w e r e b l e d b e f o r e infes
tation and every s e v e n days for 17 w e e k s thereafter.
Likewise, cattle o f the s e c o n d e x p e r i m e n t w e r e b l e d at e a c h o f t h e five infestations. A third g r o u p o f three calves was u s e d as a uninfested group, a n d was b l e d during all stages o f the e x p e r i m e n t s . Antibody levels against salivary gland antigens w e r e determined in sera from animals in all e x p e r i m e n t s using the ELISA test.
E L I S A
T h e procedure described by Engvall & Perlman ( 1 9 7 1 ) w a s followed. Ninety-sixwell flat-bottom microplates [Probind ( B e c t o n Dickson)] w e r e coated with 5 pg/well o f protein antigens derived from the p o o l e d salivary glands o f ticks that had fed for five days. Salivary gland extracts w e r e diluted in c a r b o n a t e b i c a r b o n a t e coating buffer, pH = 9-6, and incubated for t w o hours at 37 °C and over night at 4 °C. After three washings with phos
phate buffered saline ( P B S ) containing 0.05 % T w e e n - 20 ( P B S - T 0.05 % ) , the microplates w e r e incubated for o n e hour at 37 °C with P B S - T 2 % in order to inhibit n o n specific binding. After three m o r e P B S - T 0.05 % rinses, 100 pi o f cattle sera diluted to 1 / 1 0 0 in P B S - T 0.05 % w e r e a d d e d (all s a m p l e s w e r e tested in tripli
c a t e ) and plates w e r e i n c u b a t e d for o n e hour at 37 °C.
After o n e washing, 100 pi o f p e r o x i d a s e labelled rabbit anti-bovine IgG (Cappel Lab. W e s t c h e s t e r Pennsyl
vania), diluted 1/1,000 in P B S w e r e added to e a c h well.
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ACQUIRED CATTLE TICK RESISTANCE
T h e plates w e r e i n c u b a t e d for an additional o n e h o u r at 3 7 °C, a n d after a n o t h e r three washings with P B S - T 0.05 %, 100 ul o f substrate solution ( O r t h o p h e n y l e n e diamine ( 1 0 m g ) + 1 ml m e t h a n o l + 100 pi H20> a n d 99 ml water) were a d d e d to the wells. T h e assays w e r e read at an optical w a v e length o f 4 9 2 n m using an automatic ELISA plate reader.
STATISTICAL ANALYSIS
With regard to antibody production, there w a s an i n c r e a s e in the average level from ( 0 . 2 0 ± 0.02 S D ) to ( 0 . 8 7 O D ± 0.07 S D ) by the third w e e k after the first infestations, followed b y a sharp d e c l i n e and fluctua
ting readings ( 0 . 3 7 to 0.25 O D ) for almost nine w e e k s thereafter (Fig. 1 ) . T h r e e w e e k s after the challenge, a n e w antibody peak appeared ( 0 . 5 7 O D ± 0 . 0 5 ) (Fig. 1).
T h e difference b e t w e e n p e a k s w a s statistically signifi
cant (P < 0 . 0 5 ) . Data w e r e analyzed using the general linear model.
Since the m e t h o d o l o g y in this e x p e r i m e n t falls within the principle o f r e p e a t e d m e a s u r e s design (Gill, 1 9 9 0 ) , t h e r e p e a t e d m e a s u r e d ( m u l t i v a r i a t e ) a n a l y s i s o f variance w a s a d o p t e d using the Statistical Analysis Systems (SAS) program. S i n c e the s a m e g r o u p o f ani
mals w a s a n a l y z e d o v e r a time p e r i o d , our main i n t e r e s t w a s to a s c e r t a i n w h e t h e r t h e p r o t e c t i o n afforded by a c q u i r e d resistance increases with suc
c e s s i v e i n f e s t a t i o n s . In all tests, s i g n i f i c a n c e w a s a s s e s s e d at a level o f P < 0 . 0 5 .
RESULTS
EXPERIMENT 1
T
h e effect o f light infestations with H. m. marginatum adult ticks is s h o w n in T a b l e I-A. Low level c o n t i n u o u s intensity infestations c a u s e a d e c l i n e but not significant c h a n g e in the parameters m e a s u r e d for assessing tick viability and feeding suc
c e s s (survival to d e t a c h m e n t , weight o f females at d e t a c h m e n t , weight o f egg m a s s ) . T i c k s in the chal
l e n g e d groups ( 1 0 0 pairs), also did not s h o w any significant differences (P > 0 . 0 5 ) in t h e s e characteris
tics ( T a b l e I - B ) .
Fig. 1. — Antibody level to salivary extracts as determined by KLISA in sera of three calves infested with low rates if Hyalomma m. mar
ginatum. The arrow corresponds to the challenge with 100 pairs of Hyalomma m. marginatum ticks.
A. Result of 21 light infestations with Hyalomma marginatum marginatum in cattle
Tick Characteristics Control Calf 1 Calf 2 Calf 3 Average ± SD
Survival to detachment mg 93 92 86 95 91 ± 3.5
Weight at detachment mg 779 796 618 5-8 664 ± 95
Weight of egg mass (mg) 396 392 272 IR 294 ± 73
Control: mean data of three calves infested one time by 100 pairs of Hyalommma m. marginatum adult ticks.
B. Comparison of the results of 21 light infestations and a heavy challenge on Hyalomma marginatum marginatum of cattle Average 21 infestations
Tick Characteristics Average 21 infestations ± challenge
Survival to detachment (%) 91 ± 3.7 84.5 ± 5.7
Weight at detachment (mg) 664 ± 95 645 ± 88
Weight of egg mass (mg) 294 ± 73 290 ± 37
Table I. — Lack of resistance to low intensity repeated infestations with adult Hyalomma marginatum marginatum (two-three tick pairs added each day for 21 days).
EXPERIMENT 2
During high intensity repeated infestations, the number o f ticks w h i c h survived to detachment and ovipositio- ning declined gradually and r e a c h e d a significant dif
ference from the first infestation only by the fifth infes
tation. D e t a c h m e n t weights s h o w e d a similar trend.
T h e average weight at d e t a c h m e n t was slightly higher by the s e c o n d c o m p a r e d to the first infestation, but all the ticks w e r e significantly smaller (P < 0 . 0 5 ) at the fourth infestation.
Most o f the non-viable ticks (affected ticks) w e r e either dark red-brown with smooth distended cuticles, or light green-yellow and turned dark with time. T h e average weight per egg mass d r o p p e d markedly b y the third infestation to 66 % reduction after the fourth infesta
tion ( T a b l e I I ) . A c o m p a r i s o n r e v e a l e d significant changes in all the parameters measured during the first, fourth and fifth infestations ( T a b l e II).
T h e ELISA test s h o w e d that the first infestation caused an important antibody production reaching a p e a k at Day 15 post infestation (from 0.10 ± 0.02 to 1.07 ± 0 . 0 4 ) and declining thereafter (Fig. 2 ) . During the s e c o n d infestation, the rate o f antibodies increased again and d r o p p e d 15 days thereafter. Each o f the following three infestations, h o w e v e r , resulted in a progressive d e c l i n e in antibody levels. Antibody levels d r o p p e d within a month from the last infestation.
Fig. 2. — Antibodies against an extract of five-day-fed salivary gland of Hyalomma m. marginatum detected by enzyme-linked immunosorbent assay (ELISA) in the sera of three calves taken before infestations and during the first weeks of each infestation by Hya
lomma m. marginatum.
Infestations
Tick characteristics 1st 2nd 3rd 4th 5th
% of females engorged Female weight (mg) Egg mass weight (mg)
68 ± 14 825 ± 31 478 ± 16
74 ± 8 861 ± 17 457 ± 47
80 ± 10 607 ± 87 349 ± 52
53 ± 8 267 ± 23*
164 ± 38*
41 ± 4*
296 ± 23*
129 ± (The value represents an average number; results followed by a symbol were significant.)
Table II. — Tick characteristics during five infestations of three calves with Hyalomma marginatum marginatum.
DISCUSSION
T
he current study investigated the effect o f light and heavy r e p e a t e d infestations o f cattle o n ticks. Simulation o f field conditions in the laboratory using light and c o n t i n u o u s infestations with Hyalomma marginatum marginatum s h o w e d that the following tick parameters (% o f ticks engorged, e n g o r g e d female weight and egg mass weight), w e r e not influenced ( T a b l e I ) . Light intensity infestation did not c o n f e r r e s i s t a n c e u n d e r laboratory c o n d i t i o n s . T h e s e results a p p e a r to closely reflect what o c c u r s under field conditions. Possibly hosts b e c o m e tolerant to the parasite b e c a u s e o f c o n t i n u o u s stimulation with l o w levels o f antigens. Ticks may b e able to e v a d e the host's i m m u n e system b y inoculating i m m u n o g e n i c
materials w h i c h react with antibodies to form i m m u n e c o m p l e x e s that could deflect the i m m u n e r e s p o n s e o f the host to ticks. T h e tick may also inoculate i m m u n e - suppressive materials to abolish the i m m u n e r e s p o n s e (Ribeiro ETAL, 1 9 9 0 ; 1 9 9 2 ; 1 9 9 5 ) .
Heavy repeated infestations induced in cattle partial resistance against Hyalomma marginatum marginatum adult ticks after three infestations. This resistance w a s manifested b y an inhibition o f tick feeding and ferti
lity (Table II). T h e percentage o f engorged females was significantly affected at the forth and fifth infestations c o m p a r e d to the first infestation, dropping to 55 %.
F e m a l e weight w a s also affected from the third to the fifth infestation ( b y 68 % ) . Likewise, e g g mass weight d r o p p e d from the third infestation to reach 66 % b y the fifth infestation. T h e r e is e n o u g h e v i d e n c e to sug-
Mémoire Parasite, 1998, 5, 69-74
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ACQUIRED CATTLE TICK RESISTANCE
gest that frequent reinfestations of cattle can confer a resistance, but the mechanism responsible for main- taining this resistance remain to be investigate. Similar results were found with other species of ticks (Dipeolu et al., 1992). The tick Boophilus microplus (Canestrini) responded basically in the same way (Barriga et al, 1993; 1995). Opdebeeck et al. (1988) found that Here- ford immunized with extracts of tick guts gave a pro- tection of 36 % for seven months.
Circulating antibodies against salivary gland antigens of Hyalomma marginatum marginatum were detected by ELISA. During a low intensity infestation the anti- body titer increased after three weeks, but declined rapidly to remain low. Three weeks after the challenge, the antibody titer increased slightly, and later dropped again. As results we noticed that low intensity infes- tations induced immunosuppression rather than immu- noprotection. However, our results showed that cattle can acquire tick resistance after heavy repeated infes- tations. This resistance could be attributed to the immune response of the host. Circulating antibodies were detected during the five infestations. It seems that the first infestation suppress the occurrence of secon- dary response induced by the second infestation.
However, it did not suppress all antibody production as it occurs in low intensity infestations. Each one of the last three infestations resulted in lower antibody levels and antibody productions declined during the month following the infestations. Around the fifth infestation, the average level was only 30 % of the level found of the first infestation. The same results were found in sheep infested with Amblyomma ameri- canum (L.) (Barriga et al., 199D- Schorderet & Bros- sard (1993) established that heavily infested rabbits pro- d u c e d a h i g h e r titer o f a n t i b o d i e s and t h e lympho-proliferative response was higher compared to lightly infested rabbits.
An inverse relationship between antibody response and manifestation of resistance was observed. Therefore the likelihood of a phenomenon of competition between irrelevant and protective antigens is suspected. Anti- body titers were low when manifestations of resistance became conspicuous at infestation. This suggests that antibodies were not the main effectors of anti-tick protective immunity, or that protective antibodies were only a small fraction of the antibody population formed against tick antigens. Some studies demonstrated that complement and cellular responses were effector mechanisms (Wikel et al., 1978; Wikel, 1979; George etal, 1985; Wikel, 1996). In fact, several investigation related to immunization with tick extracts have high- lighted the existence of a resistance to the host with the development of humoral and cellular response (Banerjee & Momin, 1990; Tembo & Rechav, 1992;
Sahibi et al., 1991b; Sahibi et al., 1997c).
This study showed no relationship between natural resistance and the ability to acquire resistance. The field conditions are propitious for immune-suppression, which probably explains the abundance and wide dis- tribution of ticks. The incomplete immune resistance established after repeated heavy infestations suggests that ticks were able to evade host immunity with their salivary glands secretion (Inokuma et al, 1993; Wikel et al, 1994). This intense antigenic stimulation favors the suppression of specific immune response to ticks.
However, an anti-tick vaccine can be developed, if pro- tective antigens were identified and quantified to induce resistance and to record the time length of such resistance.
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