1982 (Chapter 3) WALADDE Fisiology of Ticks The Sensory Basis of Tick Feeding Behavious

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C H A P T E R 3 
The Sensory Basis of Tick Feeding Behaviour 
S. M. WALADDE 
International Centre of Insect Physiology and Ecology, P.O. Box 30772, Nairobi, Kenya. 
and 
M . J . RICE 
Department of Entomology, University of Queensland, St. Lucia, Qld. 4067, Australia 
C O N T E N T S 
3.1. Introduction to Tick Feeding Behaviour 72 
3.1.1. Tick Feeding as a Behavioural Sequence 72 
3.1.2. General Location of Tick Sense Organs 73 
3.1.3. Tick Chemoreceptor Sensilla 74 
3.1.4. Tick Mechanoreceptors 75 
3.1.5. Tick Photoreceptors 76 
3.1.6. Tick Thermoreceptors, Hygroreceptors, Osmoreceptors, and Radiant 
Heat Receptors 76 
3.2. Host Location by Ticks 78 
3.2.1. Behavioural Studies 78 
3.2.2. Ultrastructure and Electrophysiology of Sensilla on Tarsus I, Including 
Haller's Organ 83 
3.2.2.1. Ultrastructure of the Anterior Pit Sensilla 84 
3.2.2.2. Electrophysiology of the Anterior Pit Sensilla 89 
3.2.2.3. Ultrastructure of the Posterior Capsule Sensilla 90 
3.2.2.4. Electrophysiology of the Posterior Capsule Sensilla 92 
3.2.2.5. Tarsal Receptors Other than those of Haller's Organ 94 
3.3. Attachment of Ticks 95 
3.3.1. Information on Attachment Behaviour 95 
3.3.2. Ultrastructure and Electrophysiology of the Distal Sensilla of the Tarsus 97 
3.3.3. Ultrastructure and Electrophysiology of the Palpal Organ Sensilla 100 
3.4. Engorgement by Ticks 102 
3.4.1. Behavioural Observations 102 
3.4.2. Ultrastructure and Electrophysiology of Cheliceral Receptors 105 
3.4.3. Discussion on Cheliceral Receptor Function 110 
3.5. Conclusions 112 
References 113 
71 
72 S. M. Waladde and M. J. Rice 
3.1. I N T R O D U C T I O N T O T I C K F E E D I N G B E H A V I O U R 
3.1 .1 . Tick Feeding as a Behavioural Sequence 
F e e d i n g is a v i ta l p a r t of t he life of all t icks a n d is t he c a u s e of t he d a m a g e 
they d o to the i r hos t s a n d the m e a n s by w h i c h d i sease o r g a n i s m s a r e 
t r a n s m i t t e d . In t e r f e r ence w i t h p r o p e r feeding m a y b e a poss ib le s t r a t egy for 
tick con t ro l , a n d t icks m a y b e p a r t i c u l a r l y access ib le to con t ro l m e t h o d s 
d u r i n g the i r feeding p h a s e . I n a n y even t , it s eems t h a t a d e e p e r u n d e r s t a n d i n g 
of th is v i ta l funct ion is necessa ry as p a r t of o u r g r o w i n g k n o w l e d g e of t ick 
b io logy . 
W h e r e a s t h e t e r m feeding is often used in t he sense of t he t a k i n g in of 
food, t h a t is ingestion', feeding real ly refers to a c o m p l e x of b e h a v i o u r a l 
p rocesses t h a t s t a r t w i t h h u n g e r a n d e n d w i th sa t i a t i on . I n life, th is c o m p l e x 
of p rocesses is i n t e g r a t e d i n t o a s ingle , mean ing fu l funct ion w h i c h w e c a n 
art if icially resolve by T i n b e r g i a n ana lys i s i n to a s e q u e n c e of n i n e m a i n even t s . 
T h e s e even t s c a n b e ident i f ied by fami l ia r t e r m s , m o s t of w h i c h h a v e b e e n 
used before w i t h a va r i e ty of m e a n i n g s . W e n o w define these for t he p u r p o s e s 
of this c h a p t e r : 
1. APPETENCE L o c o m o t o r y hunting for a hos t o r seeking for o n e from 
a v a n t a g e po in t . 
2. ENGAGEMENT Phys ica l c o n t a c t w i t h a n d a d h e r e n c e to t he h o s t ' s 
pe l age . 
3. EXPLORATION S e a r c h i n g on the hos t for a n a t t a c h m e n t s i te . 
4. PENETRATION I n s e r t i o n of t he m o u t h p a r t s in to t h e h o s t ' s 
i n t e g u m e n t . 
5. ATTACHMENT E s t a b l i s h m e n t of a feeding si te . 
6. INGESTION U p t a k e of hos t b o d y fluids. 
7. ENGORGEMENT U p t a k e of a full m e a l . 
8. DETACHMENT W i t h d r a w a l of t he m o u t h p a r t s from the h o s t ' s 
i n t e g u m e n t . 
9. DISENGAGEMENT L e a v i n g the hos t . 
T h i s feeding s e q u e n c e is found in all t icks. T h e r e a r e , howeve r , c o n s i d e r a b l e 
differences b e t w e e n species . F o r e x a m p l e , in m a n y h a r d t icks ( I x o d i d a e ) 
a t t a c h m e n t a l so involves secre t ion of a c e m e n t cone ( M o o r h o u s e , 1969) b u t 
in soft t icks ( A r g a s i d a e ) , a n d s o m e o t h e r h a r d t icks, n o c e m e n t is sec re ted . 
T h e d iv i s ion of feeding b e h a v i o u r i n to n i n e c lea r -cu t even t s i l lus t ra tes t h e 
need for p rec i s ion in a d i scuss ion of tick feeding. T h e s a m e g e n e r a l t e r m h a s 
b e e n used q u i t e loosely to refer to severa l different p a r t s of the s e q u e n c e . I t 
is b e c a u s e of th is t h a t w e r e c o m m e n d the use of t e r m s t h a t a r e m o r e closely 
def ined. 
The Sensory Basis of Tick Feeding Behaviour 73 
V a r i a t i o n s in feeding b e h a v i o u r b e t w e e n different species of t icks a r e b a s e d 
on differences in t h e w a y t h e y execu te o n e o r m o r e of t he a b o v e n i n e even t s . 
Differences in b e h a v i o u r a t even t s 1—3 form the bas i s of t h e hos t specificity 
of different t ick spec ies . Differences in b e h a v i o u r a t even t s 3 - 5 form t h e bas i s 
of p red i l ec t ion si te se lec t ion . S u c h b e h a v i o u r a l differences b e t w e e n species 
a r e r e g u l a t e d b y t w o m a i n neu ro -b io log ica l f a c t o r s — t h e n a t u r e of t he sensory 
i n p u t o b t a i n e d b y a tick a n d the c e n t r a l n e r v o u s sys t em p roces s ing of t h a t 
i n p u t . W e a r e still a t a n ea r ly s t age in t he inves t iga t ion of c en t r a l p rocess ing , 
b u t r ecen t y e a r s h a v e seen a d v a n c e s in o u r k n o w l e d g e of tick sensory b io logy. 
I t is n o w poss ib le to d e s c r i b e t h e loca t ion a n d m o r p h o l o g y of m o s t of the 
sensory r e c e p t o r s t h o u g h t to be invo lved in feeding b e h a v i o u r , t oge the r w i t h 
t h e u l t r a s t r u c t u r e of the i r s enso ry n e u r o n s . E lec t rophys io log ica l s t u d y of t h e 
r e s p o n s e s p e c t r a of t hese n e u r o n s h a s on ly recen t ly b e g u n a n d m u c h r e m a i n s 
to b e a c c o m p l i s h e d . B e h a v i o u r a l s tud ie s on tick feeding b e h a v i o u r b e g a n 
m a n y yea r s a g o a n d a r e q u i t e ex tens ive b u t , a g a i n , m u c h r e m a i n s to be d o n e , 
p a r t i c u l a r l y in t h e l ight of o u r i m p r o v e d k n o w l e d g e of sensory r ecep to r s . 
T h e ma jo r i t y of s t ud i e s o n tick sensory r ecep t o r s h a v e been of a m o r -
pho log ica l a n d s t r u c t u r a l n a t u r e ; whi le s u c h s tud ie s a r e genera l ly a b l e to 
revea l t h e n a t u r e of m e c h a n o r e c e p t o r s , p h o t o r e c e p t o r s , g u s t a t o r y , a n d olfac-
tory r e c e p t o r s , t hey revea l n o t h i n g of t he r e s p o n s e cha rac t e r i s t i c s of the 
r e c e p t o r s . F r o m m o r p h o l o g y a l o n e it is n o t poss ib le to d i s t i ngu i sh r ecep to r s 
involved in feeding from those w h i c h m a y b e spec ia l ized for de t ec t ion of sex 
or a g g r e g a t i o n p h e r o m o n e s , a v o i d a n c e of p r e d a t o r s , c o - o r d i n a t i o n of loco-
m o t i o n , m o n i t o r i n g g e n e r a l e n v i r o n m e n t a l p a r a m e t e r s , o r in t he loca t ion of 
ov ipos i t ion s i tes . E lec t rophys io log ica l s tud ie s , c o u p l e d w i th prec i se b e h a v -
ioura l a n a l y s e s , a r e n e e d e d to e n a b l e d i s t i nc t ions to be d r a w n b e t w e e n these 
different func t ions . I n ve ry few cases h a s s u c h w o r k even b e g u n , a n d if th is 
c h a p t e r on lyserves to p i n p o i n t th is ve ry fertile a r e a for fu ture w o r k it will 
h a v e b e e n of v a l u e . 
W e h a v e a r r a n g e d t h e c h a p t e r so t h a t t h e even t s w h i c h cons t i t u t e feeding 
b e h a v i o u r a r e d e a l t w i t h in a s e q u e n t i a l m a n n e r . U n d e r t h e h e a d i n g " h o s t 
l o c a t i o n " w e c o n s i d e r a p p e t e n c e a n d e n g a g e m e n t , u n d e r " a t t a c h m e n t " w e 
t r ea t e x p l o r a t i o n , p e n e t r a t i o n , a n d a t t a c h m e n t , a n d , finally, u n d e r the h e a d -
ing " e n g o r g e m e n t " w e cons ide r t h e r e m a i n i n g four even t s of t he feeding 
s e q u e n c e . I n e a c h of t h e m a i n sec t ions , t ick b e h a v i o u r , sensory s t r u c t u r e , 
a n d e l ec t rophys io logy a r e d i scussed in t u r n . W e apo log ize for a n y b i a s 
t o w a r d s t h e ca t t l e t ick Boophilus microplus ( C a n e s t r i n i ) as we h a v e recen t ly 
b e e n w o r k i n g on t h a t species a n d a r e therefore m o s t fami l ia r w i th its sensory 
biology. 
3.1.2. General Location of Tick Sense Organs 
T h e sense o r g a n s k n o w n o r s u s p e c t e d to be involved in tick feeding 
74 S. M. Waladde and M. J. Rice 
b e h a v i o u r a r e c o n c e n t r a t e d a t t h e a n t e r i o r e n d of t he b o d y in four m a i n 
l o c a t i o n s — o n t h e t a r s i of t h e first p a i r of legs; on the p a l p s ; in the che l ice rae ; 
a n d o n the s c u t u m . 
R e c e p t o r s found on the t a r s i of leg I i nc lude t he olfactory c h e m o r e c e p t o r s 
of t he H a l l e r ' s o r g a n c o m p l e x , g u s t a t o r y r ecep to r s , m e c h a n o r e c e p t o r s , a n d 
p r o b a b l y h u m i d i t y a n d r a d i a n t h e a t r ecep to r s (cf. §3 .2 .2) . T h e p a l p a l r e c e p -
tors a p p e a r to b e g u s t a t o r y , a l t h o u g h s o m e of t h e m m a y h a v e a n ol factory 
funct ion a n d nea r ly all of t h e m c o n t a i n m e c h a n o r e c e p t i v e n e u r o n s (cf. §3 .3 .4) . 
T h e che l icera l r e cep to r s a r e m a i n l y g u s t a t o r y a n d m e c h a n o r e c e p t i v e (cf. 
§3 .4 .2) . O n t h e s c u t u m s o m e ticks h a v e well deve loped p h o t o r e c e p t o r s (Fig . 
3 .1) . R e c e p t o r s o n o t h e r p a r t s of leg I , on legs I I - I V , a n d o n the s c u t u m a n d 
a l l o s c u t u m m a y a lso be invo lved in feeding b e h a v i o u r , b u t we h a v e l i t t le 
i n fo rma t ion o n th i s . 
3.1.3. Tick Chemoreceptor Sensil la 
T i c k c h e m o r e c e p t o r s o b s e r v e d so far a r e of two m o r p h o l o g i c a l t y p e s — 
se tae a n d p i t s . C h e m o r e c e p t i v e se tae h a v e b e e n ident if ied from t a r s u s I a n d 
the p a l p a l o r g a n , b u t c h e m o r e c e p t i v e p i ts h a v e b e e n found on the che l icera l 
d ig i t s . T h e m a i n s t r u c t u r a l fea ture t h a t identifies these as c h e m o r e c e p t i v e 
sensi l la is t h e p r e s e n c e of pe r fo ra t ions o r " p o r e s " in the i r cut ic le . S u c h p o r e s 
a r e a n essen t ia l f ea tu re w h i c h p e r m i t chemica l s from the o u t s i d e to p e n e t r a t e 
t he cut ic le a n d g a i n access to t he u n d e r l y i n g sensory cells. G u s t a t o r y c h e -
m o r e c e p t o r p i t s a n d se tae genera l ly h a v e a s ingle t e r m i n a l p o r e , w h e r e a s 
o l f a c t o r y c h e m o r e c e p t o r s e tae genera l ly h a v e m u l t i p l e pe r fo ra t ions in the i r 
wal ls (Figs . 3.11 a n d 3 .20) . O t h e r d i s t i n g u i s h i n g fea tures a r e the gene ra l ly 
th ick wal l a n d p a i r e d i n t e r n a l c h a n n e l s (one c o n t a i n i n g u n b r a n c h e d senso ry 
d e n d r i t e s ) of g u s t a t o r y c h e m o r e c e p t o r s , ve r sus t he genera l ly t h in wal l a n d 
o n e o r m o r e c h a n n e l s (one c o n t a i n i n g b r a n c h i n g d e n d r i t e s ) of ol factory 
c h e m o r e c e p t o r s , a l t h o u g h t h e r e a r e severa l excep t ions to this s imp le s c h e m e . 
T h e bes t w a y of d i f ferent ia t ing b e t w e e n the two types of c h e m o r e c e p t o r is 
to o b s e r v e t he w a y they a r e u sed in b e h a v i o u r a n d to a n a l y s e the i r e lec t ro -
phys io log ica l r e sponses to t h e a p p l i c a t i o n of v a r i o u s s t imul i . I n shor t , olfac-
tory r e c e p t o r s a r e u sed to de t ec t smel ls w h e r e a s g u s t a t o r y r ecep to r s a r e u sed 
for t a s t i ng . F r o m the phys io log ica l v i ewpo in t t he d i s t inc t ion is o n e of 
t h r e sho ld ; m o s t ol factory r ecep to r s r e s p o n d to very low c o n c e n t r a t i o n s of 
c h e m i c a l s in t he v a p o u r s t a t e , w h e r e a s m o s t g u s t a t o r y r ecep to r s gene ra l ly 
r e s p o n d to r a t h e r h i g h e r c o n c e n t r a t i o n s of chemica l s in a l iqu id s t a t e . 
As will b e seen in §§3.2 a n d 3.3 of th is c h a p t e r , olfactory r ecep t o r s h a v e 
a n u m b e r of different u l t r a s t r u c t u r a l f o r m s — s o m e wi th p l u g g e d po re s , s o m e 
w i t h po re s in g rooves , o t h e r s w i th a spoke-whee l a r r a n g e m e n t of l u m i n a 
w i th in the i r se ta l shafts . I t m a y p r o v e poss ib le to co r re l a t e p a r t i c u l a r s t r u c -
tu re s w i t h sens i t iv i ty to specific chemica l s ; howeve r , w o r k of th is t y p e h a s 
The Sensory Basis of Tick Feeding Behaviour 75 
yet to b e d o n e w i t h t icks . P r e d i c t i o n s of func t ion b a s e d o n s t r u c t u r e a lone 
a r e f r augh t w i t h d a n g e r of e r ro r . T h e r e a r e so m a n y excep t ions a l r e a d y 
k n o w n to e a c h e s t ab l i shed s t r u c t u r e - f u n c t i o n co r re l a t ion in insec ts t h a t n o 
ce r t a in t i e s r e m a i n . T h i s is a l so likely to be t r u e of t icks; it h a s ye t to b e 
s h o w n t h a t t h e func t ion of a p a r t i c u l a r m o r p h o l o g i c a l t ype of sens i l lum is 
t he s a m e in t w o different species of tick. G r e a t c a u t i o n is n e e d e d , a n d it 
s h o u l d a l w a y s b e b o r n e in m i n d t h a t t h e a d e q u a t e s t i m u l u s for a p a r t i c u l a r 
sens i l lum is m u c h m o r e t h e p r o p e r t y of its c o n t a i n e d n e u r o n s t h a n of t h e 
c u t i c u l a r c o m p o n e n t s w h i c h a r e so m u c h m o r e easi ly s t ud i ed . 
3.1.4. Tick Mechanoreceptors 
Senso ry se t ae p ro jec t f rom t h e a p p e n d a g e s a n d from the gene ra l b o d y 
surface of all t icks (Figs . 3.1 a n d 3.5.) . S o m e of these a r e c h e m o r e c e p t i v e , 
as d e s c r i b e d in §3.1 .3 a b o v e , b u t m o s t of t h e m a r e t a c t i l e s e n s e o r g a n s 
e n d o w i n g t h e tick w i t h a sense of t o u c h w h e n the se tae a r e m o v e d by c o n t a c t . 
S o m e of t h e se t ae m a y b e v i b r a t i o n r e c e p t o r s r e s p o n d i n g to s o u n d v i b r a t i o n s 
t r a n s m i t t e d t h r o u g h a i r o r s u b s t r a t u m . O t h e r se tae a r e n e i t h e r m e c h a n o -
r ecep to r s n o r c h e m o r e c e p t o r s b u t m a y b e invo lved in d e t e c t i n g o t h e r s t imul i 
s u c h as h e a t . M a n y sensi l la , p a r t i c u l a r l y those w i t h g u s t a t o r y r ecep to r s , 
c o n t a i n t w o types of senso ry n e u r o n w h i c h e n a b l e these sensi l la to h a v e a 
d u a l func t ion a s c h e m o - m e c h a n o r e c e p t o r s . T h e r e a r e a lso non-se t i fo rm 
m e c ha n o r e c e p t o r s o n t h e surface of t h e b o d y ; these a r e t r ad i t i ona l ly referred 
to as a u r i c u l a r s e n s i l l a (cf. p r e v i o u s l i t e r a t u r e , r ev iewed by B a l a s h o v , 1972) , 
b u t t hey a p p e a r so s imi l a r in form to t he fami l ia r c a m p a n i f o r m s e n s i l l a 
of insec ts t h a t w e n o w use t h a t t e r m for t h e m . T h e y a r e d i s t inc t f rom m o s t 
of t h e t ick t r i c h o i d s e n s i l l a , w h i c h cons is t of a se ta p ro jec t ing f rom a socket . 
T i c k c a m p a n i f o r m sensi l la cons is t of t h e socket a lone , c losed off by a p a r t i t i o n 
o r d o m e of cu t ic le w i t h a n i n d e n t a t i o n r u n n i n g ac ross t he m i d d l e (Fig. 3 .4) . 
R e c e n t s t ud i e s of t h e p e r i p h e r a l n e r v o u s s y s t e m of B. microplus w i t h m e t h y l e n e 
b lue s t a i n i n g h a v e s h o w n t h a t t h e tac t i le s e t ae a r e i n n e r v a t e d by t w o n e u r o n s 
w h e r e a s c a m p a n i f o r m sensi l la h a v e on ly o n e ( B i n n i n g t o n , pe r s . c o m m . ) . 
E lec t rophys io log ica l r e c o r d i n g s h a v e ye t to b e m a d e from these r ecep to r s . 
By a n a l o g y w i t h insec t s , h o w e v e r , t h e t r i cho ids a r e likely to m o n i t o r c o n t a c t 
a n d v i b r a t i o n s wh i l e t h e c a m p a n i f o r m s m o n i t o r c u t i c u l a r s t resses a n d s t r a in s . 
As yet , n e i t h e r m u l t i p o l a r s t r e t ch r e c e p t o r s n o r c h o r d o t o n a l sensi l la , b o t h 
c o m m o n in insec t s , h a v e b e e n d e s c r i b e d from t icks. T h e r e is a r e p o r t of 
s t r e t ch r e c e p t o r s in t icks (Bead le , 1973); t he r e c e p t o r figured, howeve r , is 
a c tua l ly t h e b a s a l r eg ion of a typ ica l t r i cho id sens i l lum. 
M a n y of t h e t r i cho id sensi l la of legs a n d p a l p s h a v e b e e n e x a m i n e d by 
e l e c t r o n m i c r o s c o p y a n d found to b e d o u b l y i n n e r v a t e d m e c h a n o r e c e p t o r s , 
h a v i n g t w o n e u r o n s w h o s e d e n d r i t e s t e r m i n a t e in t he socket reg ion of t he 
sensi l la ( R o s h d y et al, 1972; C h u - W a n g & Axte l l , 1973; W a l a d d e ; 1978). 
76 S. M. Waladde and M. J. Rice 
D e n d r i t e s t h a t t e r m i n a t e a t t he b a s e of a se ta a n d h a v e n o c o m m u n i c a t i o n 
w i th t he ex te r io r a r e gene ra l ly cons ide red m e c h a n o r e c e p t o r s . T h e t e r m i n a l s 
of such n e u r o n s c o n t a i n n e u r o t u b u l a r cy toske le tons , w h i c h a r e a lso c h a r -
ac te r i s t i c of all t he m e c h a n o r e c e p t o r s of insects (Rice , 1975). T h e n e u r o t u -
bu les in t he d e n d r i t e t e r m i n a l s a r e often closely p a c k e d a n d b o u n d t oge the r 
w i th d e n s e - s t a i n i n g m a t e r i a l to form " t u b u l a r b o d i e s " , first d e s c r i b e d by 
T h u r m (1964) a n d s u b s e q u e n t l y identif ied from a w i d e r a n g e of m e c h a n o -
r e c e p t o r d e n d r i t e s in insec ts a n d a r a c h n i d s ( rev iewed by M c l v e r , 1975) . T h e 
w a y in w h i c h the cy toske le ton o p e r a t e s is a m u c h - d e b a t e d po in t . T h e t w o 
d e n d r i t e s a t t he b a s e of a typ ica l t r i cho id sens i l lum of the a p p e n d a g e s of B. 
microplus h a v e different cy toske le tons . O n e is often of a d e n s e t u b u l a r b o d y 
type , t he o t h e r h a v i n g a m u c h less d e n s e compos i t i o n ( W a l a d d e , 1978). T h i s 
w o u l d a lso a p p e a r to be t he case in Ar gas arboreus a n d in Amblyomma americanum 
( R o s h d y et ai, 1972; C h u - W a n g & Axte i l , 1973). S u c h a s t r u c t u r a l differ-
en t i a t i on is a lso d i s p l a y e d by the two d e n d r i t e s a t the b a s e of t he che l icera l 
pap i l l a of B. microplus ( W a l a d d e & Rice , 1977) (Fig . 3 .28) . I n t e r m s of 
funct ion, we c o n s i d e r t h a t t he m e c h a n o r e c e p t o r d e n d r i t e s we h a v e e x a m i n e d 
a r e no t sub jec t ed to c o m p r e s s i o n by the socket d u r i n g s t i m u l a t i o n . T h e t w o 
types of cy toske le ton , d e n s e a n d less d e n s e , m a y reflect phys io logica l differ-
ences , s u c h as differences in t h r e sho ld , a d a p t a t i o n r a t e o r d i r ec t i ona l sen-
si t ivity (Rice , 1975). M u c h of this will be resolved w h e n a d d i t i o n a l e lec t ro-
phys io log ica l s tud ie s h a v e b e e n p e r f o r m e d on tick m e c h a n o r e c e p t o r s . 
3.1.5. Tick Photoreceptors 
All t icks t h a t h a v e b e e n e x a m i n e d in de ta i l , even the "eye les s" t icks, h a v e 
b e e n found to h a v e we l l -deve loped p h o t o r e c e p t o r s a n d op t i c gang l i a in t he 
b r a i n ( B i n n i n g t o n , 1972; Panf i lova , 1976; Ioffe, 1976). S o m e of t he Hyalomma 
species (e.g. H. dromedarii a n d H. asiaticum) a n d Ornithodoros savignyi h a v e eyes 
t h a t a r e t h o u g h t to be sufficiently good to a l low these t icks to act ively h u n t 
the i r hos t s by vis ion ( P o m e r a n t z e v , 1950; H o o g s t r a a l , 1956). E v e n those tick 
species t h a t a p p e a r eyeless , r e s p o n d to c h a n g e s in l ight in tens i ty . R e c e n t l y 
t he eyes of A. americanum h a v e b e e n e x a m i n e d by t r a n s m i s s i o n e lec t ron-
m i c r o s c o p y (Phil l is & C r o m r o y , 1977) a n d s h o w n to possess a lens a n d 
3 0 - 4 0 typica l ly r h a b d o m e r i c p h o t o r e c e p t o r s . T h e eyes of B. microplus a r e no t 
well d e v e l o p e d b u t sufficiently so to b e visible by s c a n n i n g e lec t ron m i c r o s c o p y 
(Fig. 3 .1) . T h e r e h a v e b e e n n o e lec t rophys io log ica l s tud ies of t ick vis ion as 
far as we a r e a w a r e . 
3.1.6. Tick Thermoreceptors , Hygroreceptors , Osmoreceptors , and Radiant 
Heat Receptors 
T h e s e r ecep to r s a r e likely to be p r e sen t , as j u d g e d by the b e h a v i o u r a l 
The Sensory Basis of Tick Feeding Behaviour 77 
r e sponses of t icks b u t , as ye t , h a v e n o t b e e n ident if ied as specific s t r u c t u r e s . 
Lees (1948) s t a t e d t h a t t h e sma l l h a i r s o n t he ta rs i of Ixodes ricinus w e r e 
t h e r m o r e c e p t o r s , b u t w e h a v e no t i nves t iga t ed the role of such ha i r s in B. 
microplus. T h e s c u t u m a n d a l l o s c u t u m of B. microplus b e a r two d i s t inc t ly 
different types of se tae ( B i n n i n g t o n , W a l a d d e & Rice , u n p u b l i s h e d ) . T h e 
first t ype a r e longer , w i t h d i s t inc t g rooves in the i r wal ls a n d a cas te l l a ted t ip . 
T h e y a r e p r o b a b l y m e c h a n o r e c e p t o r s (Fig . 3 .2) . T h e second t ype a r e sma l l e r , 
s m o o t h wa l l ed , c u r v e d , a n d t a p e r e d (Fig . 3 .3) . I t is no t k n o w n w h e t h e r these 
sensi l la c o r r e s p o n d to t he t h e r m o r e c e p t o r s d e s c r i b e d by Lees . T h i s r e m a i n s 
to be d e t e r m i n e d by e lec t rophys io log ica l s t u d y . 
FlGS. 3.1-3.4. Boophilus microplus sense organs as revealed by scanning electron microscopy: 3.1, 
the eyes on the scutum (scale equals 200 μιη); 3.2, grooved, tactile seta on the alloscutum (scale 
equals 4 μpiι); 3.3, smooth, tapered seta on the alloscutum (scale equals ΙΟμηι); 3.4, 
companiform-like sensillum on the scutum (scale equals 10 μpiι). 
78 S. M. Waladde and M. J. Rice 
T i c k s r e s p o n d to h u m i d i t y differences, a n d we a n t i c i p a t e t ha t s o m e of 
t he olfactory sensi l la will b e found to c o n t a i n hyg ro recep t i ve n e u r o n s (cf. 
§3 .2 .2 .1) . O s m o r e c e p t o r s m a y be p r e s e n t in t he che l ice rae (cf. §3 .4 .2) . 
R a d i a n t h e a t r e c e p t o r s a r e likely to be p r e sen t , on b e h a v i o u r a l ev idence (cf. 
§3 .2 .1) , b u t n o c a n d i d a t e sens i l lum is yet k n o w n (cf. §3 .2 .2 .1) . O n c e a g a i n 
we c o n c l u d e t h a t a g r e a t dea l of work r e m a i n s to be ca r r i ed o u t before a 
c lear p i c t u r e of t ick sensory biology c a n be p r e s e n t e d . 
3.2 . H O S T L O C A T I O N BY T I C K S 
3.2.1 . Behavioural Studies 
T h e r e h a v e b e e n a n u m b e r of s tud ie s on t he b e h a v i o u r a l r eac t ions of 
v a r i o u s tick species to hos t s t imul i ( H i n d l e & M e r r i m a n , 1912; T o t z e , 1933; 
K r i j g s m a n , 1937; M i r o n o v , 1939; Lees , 1948; W i l k i n s o n , 1953; El Z i a d y , 
1958; C a m i n , 1963; Nevi l le , 1964; Z o l o t a r e v & Sin i tz ina , 1965; M c E n r o e 
& M c E n r o e , 1973; H o w e l l , 1973; E l i za rov & V a s e w t a , 1977). I n a d d i t i o n , 
m a n y c a s u a l o b s e r v a t i o n s o n this sub jec t a r e s ca t t e r ed t h r o u g h o u t the lit-
e r a t u r e , as a d j u n c t s to s tud ie s of tick s t r u c t u r e , life h i s to ry , field ecology, 
a n d l a b o r a t o r y b io logy. I n this sec t ion a n a t t e m p t h a s b e e n m a d e to d r a w 
o u t t h e sa l i en t fea tures of hos t loca t ion b e h a v i o u r , p r e s e n t e d in t he form of 
g e n e r a l s t a t e m e n t s t h a t a r e m o r e or less a p p l i c a b l e to t he ma jo r i t y of tick 
spec ies . O u r p u r p o s e is to give a re la t ively cohe ren t , overa l l p i c t u r e as a n 
i n t r o d u c t i o n to t h e fol lowing sec t ions d e a l i n g w i t h t he s t r u c t u r e a n d phys i -
ology of sensory r ecep to r s u sed in hos t loca t ion . 
A l t h o u g h ce r t a in r e sponses c a n b e r e g a r d e d as c o m m o n to t he ma jo r i t y 
of t icks, different species s h o w a g r e a t dea l of va r i e ty in the i r a p p e t e n c e 
b e h a v i o u r a n d in the i r execu t ion of hos t e n g a g e m e n t . T h e ini t ia l d i s t inc t ion 
is b e t w e e n species t h a t d i s p l a y a p p e t e n c e by ac t ive h u n t i n g of hos t s a n d 
those in w h i c h a p p e t e n c e t akes t he form of p r e p a r i n g a n a m b u s h . H u n t e r s 
m a k e the i r o w n w a y t o w a r d s a sou rce of hos t s t imul i , a m b u s h e r s r e a d y 
t hemse lve s to e n g a g e t h e hos t w h e n it c o m e s w i t h i n r e a c h . C e r t a i n Hyalomma 
species a n d 0. savignyi r e p r e s e n t t he e x t r e m e of t he h u n t e r c lass , ac t ive ly 
r u n n i n g in t h e d i r ec t i on in w h i c h the hos t is seen or sensed ( P o m e r a n t z e v , 
1950); H o o g s t r a a l , 1956) . W i t h t h e d i scovery of tick a t t r a c t i o n to sources of 
C O 2 ( G a r c i a , 1962) , severa l s tud ies h a v e s h o w n t h a t a n u m b e r of o t h e r 
ixod id a n d a r g a s i d species m a y b e a b l e to h u n t over s o m e d i s t a n c e for the i r 
hos t ( the s o u r c e of C O 2 ) . T h e s e species i n c l u d e Ornithodoros coriaceus, 0. 
parken, Dermacentor occidentalis, D. albipictus, D. andersoni, Ixodes pacificus, a n d 
A. amencanum ( G a r c i a , 1965, 1969; Nevi l l , 1964; Mi l e s , 1968; W i l s o n et al., 
1972; H o k a m a & H o w a r t h , 1977). I n s o m e cases C 0 2 t r a p s m o r e effectively 
collect all s t ages of t icks t h a n the t r a d i t i o n a l m e t h o d of " f l agg ing" ( d r a g g i n g 
a c lo th ove r t h e vege t a t i on ) (Wi l son et al., 1972) . T h e s e s a m e w o r k e r s s h o w e d 
The Sensory Basis of Tick Feeding Behaviour 79 
t h a t A. amencanum w e r e a t t r a c t e d by a C O 2 s ou rce from a d i s t a n c e of 21 m . 
T h e exp i r ed b r e a t h of m a m m a l s c o n t a i n s 4 - 5 % C 0 2 in c o m p a r i s o n to a n 
a t m o s p h e r i c c o n t e n t of a b o u t 0 . 0 3 % . R a i s i n g t he a t m o s p h e r i c C O 2 level to 
a b o v e 1 % i n d u c e s a p p e t e n c e b e h a v i o u r in A. americanum, t h e s t r e n g t h of the 
r e sponse i n c r e a s i n g w i t h h i g h e r C O 2 c o n c e n t r a t i o n s u p to a b o u t 8 % ( S a u e r 
et al., 1974) . I n c o n t r a s t , B. microplus is a typ ica l e x a m p l e of a n a m b u s h i n g 
species . L a r v a e a s c e n d v e g e t a t i o n in t he ear ly m o r n i n g a n d a g a i n in t h e 
even ing , r e a c h i n g a h e i g h t a p p r o p r i a t e for c o n t a c t w i th a n y p a s s i n g ca t t l e . 
T h e y r e m a i n q u i e s c e n t o n t he v e g e t a t i o n un t i l a l e r t ed by s t imul i f rom p a s s i n g 
beas t s ; a p p e t e n c e t h e n t ake t h e form of " q u e s t i n g " as t he first p a i r of legs 
a r e w a v e d in t he a i r in t h e d i r ec t i on of hos t s t imu l i (Wi lk inson , 1953). Lees 
(1948) m a d e a c lass ical s t u d y of th is seeking b e h a v i o u r in / . ricinus. 
A n o t h e r d i s t i nc t i on b e t w e e n t h e b e h a v i o u r of tick species in t he field m u s t 
b e b a s e d o n h o s t - c h a n g i n g h a b i t s . I x o d i d t icks gene ra l ly feed for a long t i m e 
a n d they m a y c h a n g e the i r hos t once , twice , o r t h r ee t imes d u r i n g the life-
cycle. O n e - h o s t t icks , like B. microplus, s t ay on the b o d y of a n i n d i v i d u a l hos t 
t h r o u g h o u t t he feeding a n d m o u l t i n g p h a s e s of the i r life-cycle; l a r v a e a r e t h e 
on ly i n s t a r invo lved in hos t loca t ion . T w o - h o s t t icks, such as ce r t a in species 
of Rhipicephalus, in i t ia l ly find hos t s as l a r v a e a n d a g a i n as t he a d u l t s . M o s t 
species of I x o d i d a e a r e t h r e e - h o s t t icks , a n d e a c h i n s t a r ( l a rva , n y m p h , a n d 
a d u l t ) h a s to find its o w n i n d i v i d u a l hos t . I n t w o - a n d th ree -hos t t icks, 
different hos t i n d i v i d u a l s a n d often different hos t species a r e fed u p o n d u r i n g 
the life-cycle. I n c o n t r a s t , e a c h of t h e m a n y d e v e l o p m e n t a l s t ages of a rga s id 
t icks t akes a b lood m e a l of s h o r t d u r a t i o n . A l m o s t all a r g a s i d s s p e n d the i r 
life in hos t nes t s o r in the i r h a b i t u a l roos t ing o r r e s t ing p laces , feeding as 
necessa ry w h e n e v e r the i r hos t s a r e a v a i l a b l e . I n th is s i t ua t ion , hos t - loca t ing 
b e h a v i o u r is ca l led i n t o p l a y m a n y t imes d u r i n g the t ick 's life. T h e r e a r e 
e x c e p t i o n s — t h e a r g a s i d Otobius megnini is a s low feeder a n d r e m a i n s conf ined 
to t he e a r c a n a l of a s ing le -hos t i n d i v i d u a l d u r i n g all feeding s tages of its 
life-cycle. M o r e o v e r , t he ixod id Haemaphysalis inermis is a ve ry r a p i d feeder, 
d r o p p i n g f rom t h e hos t w i t h i n 30 m i n of e n g a g e m e n t — a typica l ly a r g a s i d 
feeding p a t t e r n . N o t w i t h s t a n d i n g these excep t ions , t he g e n e r a l ru le app l i e s 
t h a t h o s t l oca t ion is a re la t ive ly r a r e even t for h a r d ticks a n d a repe t i t ive 
p rocess for soft t icks. 
A t h i r d d i s t i nc t i on m u s t b e b a s e d o n the r a n g e of hos t s t h a t a r e found 
a c c e p t a b l e by v a r i o u s tick spec ies . S o m e ticks a r e confined to a s ingle g r o u p 
of hos t species , w h e r e a s o t h e r t icks pa r a s i t i s e a w i d e r a n g e of hos t s . S o m e 
ticks spec ia l ize in a p a r t i c u l a r t ype of m a m m a l (B. microplus o n b o v i d s ) , 
o t h e r s o n b i r d s ( s o m e Argas spec ies ) , a n d o t h e r s specia l ize o n rept i les ( some 
Aponoma spec ies ) . C e r t a i n t icks d i s p l a y a d i s t inc t p re fe rence for o n e p a r t i c u l a r 
hos t species . W a l t o n (1957) s t a t e s t h a t in E a s t Africa Ornithodoros moubata 
(now recogn ized as 0. porcinus) h a s t h r e e r aces ( n o w subspec ies ) specific for 
w a r t h o g , fowl, a n d h u m a n , respec t ive ly . A t t he o t h e r e x t r e m e a r e s o m e Ixodes 
80 S. M. Waladde and M. J. Rice 
species w h i c h h a v e a very w i d e r a n g e , s p a n n i n g rep t i les , b i rd s , a n d m a m m a l s . 
S u c h t icks often specia l ize on different types of hos t a t different s tages in 
the i r life-cycle. N a r r o w n e s s in hos t r a n g e c a n resu l t from phys io log ica l 
r es t r i c t ion of a t ick species to a p a r t i c u l a r e n v i r o n m e n t w h e r e it on ly e n c o u n -
ters t he " p r e f e r r e d " hos t , e.g. / . canisuga a n d / . nanus (Lees , 1969) . Al t e r -
na t ive ly , r es t r i c t ion m a y resu l t f rom a t r u e b e h a v i o u r a l p re fe rence for a 
p a r t i c u l a r hos t . T r u e b e h a v i o u r a l p re fe rence is d i sp l ayed w h e n a tick will 
no t e n g a g e , a t t a c h , or engo rge on non-p re fe r r ed hos t s . Aponoma concolor 
a p p e a r s to a t t a c h on ly on t w o e c h i d n a species a n d A. uruginas feeds exclus ively 
on w o m b a t s ( R o b e r t s , 1970) . Boophilus microplus does no t d e v e l o p o n m o s t 
of t he w i d e r a n g e of m a m m a l s to w h i c h it will a t t a c h , b u t deve lops well o n 
the p re fe r red bov id s , a n d e n g o r g e d s p e c i m e n s a r e s o m e t i m e s found o n s h e e p . 
H o o g s t r a a l (1956) q u o t e s m a n y e x a m p l e s of t icks w h i c h h a v e b e e n a p p l i e d 
to a r a n g e of hos t s b u t on ly d e v e l o p on " p r e f e r r e d " hos t s . 
A l t h o u g h t h e ex is tence of t h r ee d i s t inc t types of hos t - loca t ing b e h a v i o u r s 
a r e well k n o w n ( h u n t e r ve r sus a m b u s h e r t icks; one -hos t ve r sus m u l t i - h o s t 
t icks; a n d host-specif ic ve r su s h o s t - d i v e r g e n t t icks) , l i t t le is u n d e r s t o o d of 
t he w a y in w h i c h a t ick 's sensory biology is a d a p t e d for such d i s t inc t ly 
different life s tyles . T h e key fea tures t h a t d i s t i ngu i sh t he sensory b io logy of 
a o n e - h o s t host-specif ic a m b u s h e r tick from t h a t of a mu l t i - hos t h o s t - d i v e r g e n t 
h u n t e r t ick, h a v e n o t b e e n d e t e r m i n e d . M o d e r n t e c h n i q u e s used in t h e s t u d y 
of b e h a v i o u r , n e u r o p h y s i o l o g y , a n d u l t r a s t r u c t u r e a r e p r e p a r i n g t h e w a y for 
inves t iga t ions t h a t s h o u l d p r o v i d e these d i s t inc t ions . 
T h e senso ry s t imu l i t h a t evoke a p p e t e n c e a n d e n g a g e m e n t c a n b e classified 
in t h r e e w a y s in t e r m s of t he i n fo rma t ion t h a t t hey could c a r ry : " d i s t a n c e " 
ve r sus " c l o s e " s t imu l i , " d i r e c t i o n a l " ve r sus " n o n - d i r e c t i o n a l " s t imul i , a n d 
" g e n e r a l " ve r sus "speci f ic" s t imul i . C lose s t imul i a r e those t h a t on ly affect 
t icks n e a r to t h e sou rce of s t i m u l a t i o n . T a c t i l e s t i m u l a t i o n is poss ib ly the 
m o s t o b v i o u s of these , t o u c h b e i n g a powerful s t i m u l u s c a u s i n g t icks to 
a t t e m p t to e n g a g e t h e hos t , a n d this is t he bas is of " f l agg ing" as a m e t h o d 
of s a m p l i n g tick p o p u l a t i o n s . W a r m t h , too , is a s t i m u l u s t h a t o p e r a t e s a t 
close q u a r t e r s to c a u s e a p p e t i t i v e b e h a v i o u r a n d is a lso i m p o r t a n t for a t t a c h -
m e n t (see §3 .3 .1) . B o t h t o u c h a n d w a r m t h a r e d i r ec t iona l s t imul i a n d b o t h 
a r e non-specif ic (i .e. t hey a r e no t a s soc ia ted w i t h o n e type of hos t o n l y ) . 
D i s t a n c e s t imu l i a l so evoke a p p e t i t i v e b e h a v i o u r s — h u n t i n g in s o m e species 
a n d seek ing in o t h e r s . V i b r a t i o n s , v i sua l i m a g e s , s h a d o w s , a n d r a d i a n t h e a t 
all a c t a t a d i s t a n c e a n d evoke ac t iv i ty in s o m e tick species . V i b r a t i o n s c a n 
b e specific s t imul i ; s o u n d s p r o d u c e d by swal lows in t he r a n g e of 3 0 0 0 -
8000 H z in i t i a t e t he h u n t i n g b e h a v i o u r of Ornithodoros concanensis ( W e b b et 
ai, 1977) . 
W o r k in o u r l a b o r a t o r y h a s s h o w n t h a t l a r v a e of B. microplus a r e p a r t i c u l a r l y 
sens i t ive to a i r b o r n e v i b r a t i o n s , m a i n l y in t h e 8 0 - 8 0 0 H z r a n g e . T h e s e 
f requencies a r e p r e d o m i n a n t a m o n g the s o u n d s p r o d u c e d by ca t t l e feeding 
The Sensory Basis of Tick Feeding Behaviour 81 
in g r e e n g r a s s (Pa lass i s , u n p u b l i s h e d r e p o r t ) . T h e l a r v a e a r e so sensi t ive to 
s o u n d s of th is f r equency t h a t t hey will r ead i ly seek even w h e n the s o u n d s 
a r e a l m o s t i n a u d i b l e to t h e h u m a n obse rve r . T h e i m p o r t a n c e of s o u n d c a n 
a lso b e d e d u c e d from t h e o b s e r v a t i o n t h a t n y m p h s a n d a d u l t s of Rhipicephalus 
sanguineus e m e r g e from c racks in wal l s a n d beg in to h u n t w h e n a l e r t ed by the 
b a r k i n g of d o g s ( B i n n i n g t o n , p e r s . c o m m . ) . R a d i a n t h e a t from a 1-m d i s t a n t 
sou rce c a u s e s shor t - l ived a p p e t i t i v e b e h a v i o u r in Ixodes persulcatus (E l i za rov 
& V a s e w t a , 1977) a n d in i t i a tes seek ing in B. microplus l a r v a e ( u n p u b l i s h e d 
r e p o r t ) . W o r k in o u r l a b o r a t o r y h a s s h o w n t h a t s h a d o w i n g (i .e. i n t e r r u p t i o n 
of s t e a d y i l l u m i n a t i o n ) , in all co lours of l ight excep t r ed , is a n effective 
a p p e t e n c e s t i m u l u s for B. microplus l a r v a e . I n t icks w i t h we l l -deve loped eyes , 
s u c h as Hyalomma asiaticum a n d H. dromedarii, t h e v i sua l i m a g e of t h e hos t is 
of i m p o r t a n c e in h u n t i n g ( P o m e r a n t z e v , 1950; H o o g s t r a a l , 1956; Z o l o t a r e v 
& S in i t z ina , 1965) . T h e d e g r e e to w h i c h the eyes of such h u n t e r t icks c a n 
resolve i m a g e s r e m a i n s to b e inves t iga t ed . V i s ion m a y a lso b e i m p o r t a n t in 
m a n y species w h i c h h a v e n o o b v i o u s eyes (see §3 .1 .5) . S h a d o w s m a y be 
i m p o r t a n t distance s t imu l i ea r ly in t h e d a y o r l a te in t he even ing , w h e n they 
a r e longes t . A l t h o u g h v i b r a t i o n s a n d v i sua l i m a g e s c a n b e hos t specific, 
s h a d o w s a n d r a d i a n t h e a t a r e gene ra l ly non-specific s t imul i p r o v i d i n g l i t t le 
i n fo rma t ion on t h e t y p e of a n i m a l w h i c h p r o d u c e d t h e m . All four classes of 
s t imul i a r e gene ra l l y directional, c o n t a i n i n g i n fo rma t ion o n the pos i t ion of 
the i r sou rce . 
O d o u r s a r e po t en t i a l l y t h e m o s t specific s t imul i e n c o u n t e r e d by ticks in t he 
field; t hey a r e d i s ta n c e s t imu l i w i t h l i t t le in t r ins i c d i rec t iona l i ty . H o w e v e r , 
o d o u r s a r e u sua l l y ca r r i ed o n a i r c u r r e n t s , w h i c h a d d s a d i r ec t i ona l c o m -
p o n e n t . A l t e rna t i ve ly , a tick m o v i n g t h r o u g h a n o d o u r g r a d i e n t m a y be ab l e 
to m a k e a n a s s e s s m e n t of sou rce pos i t ion . C a r b o n d iox ide , w a t e r v a p o u r , 
a n d vola t i le o r g a n i c c o m p o u n d s , s u c h as b u t y r i c ac id , a r e p r o d u c e d by all 
a n i m a l s a n d a r e n o t host-specif ic in t h e m s e l v e s . H o w e v e r , t he p r o p o r t i o n s 
of v a r i o u s vola t i les in t h e m i x t u r e s e m a n a t i n g from a p a r t i c u l a r hos t species 
a r e likely to b e specific to t h a t hos t . S u c h i n f o r m a t i o n m a y b e of use to t icks 
w i th a n a r r o w r a n g e of hos t r e q u i r e m e n t s . Boophilus annulatus a n d R. sanguineus 
a r e a b l e to di f ferent ia te b e t w e e n t h e o d o u r s of ho r se , cow, a n d h u m a n 
( K r i j g s m a n , 1937) . W h e n p l a c e d in c h a m b e r s w i t h p o r o u s floors, Ornithodoras 
eraticus w a s a b l e to d i f ferent ia te t he o d o u r s of t h e h a i r of gerb i l , g u i n e a - p i g , 
r a b b i t , a n d d o g p e r m e a t i n g u p w a r d s t h r o u g h the floor (El Z i a d y , 1958). 
Ixodes persulcatus s h o w s a p p e t i t i v e b e h a v i o u r to h u m a n o d o u r u p to 1 5 m from 
a d o w n w i n d s o u r c e (E l i za rov & V a s e w t a , 1977) . T h e a p p a r e n t t e n d e n c y to 
u n d e r p l a y t he s ignif icance of o d o u r in t h e p a s t m a y be d u e to t he des ign of 
e x p e r i m e n t s . O d o u r s p r e s e n t e d in a choice c h a m b e r w i t h n o flow-through 
of a i r will soon s a t u r a t e t h e s p a c e o n b o t h s ides of t he c h a m b e r w h i c h t e n d s 
to b lock t h e expres s ion of a n y o d o u r choice b e h a v i o u r . O d o r o u s s t imul i a r e 
often ineffective in t h e a b s e n c e of a n a c c o m p a n y i n g w a r m t h s t i m u l u s , t h a t 
82 S. M. Waladde and M. J. Rice 
is no t , in itself, ve ry effective (Lees , 1948; Nevi l l , 1964). F o r t h e m o s t p a r t , 
q u e s t i o n s of s y n e r g i s m a n d p o t e n t i a t i o n b e t w e e n va r ious s t imul i h a v e b e e n 
left u n a n s w e r e d . M u c h w o r k is n e e d e d on th is sub jec t s ince , u n d e r field 
cond i t i ons , t icks a r e r a re ly p r e s e n t e d w i t h s ingle s t imul i . 
T h e field s i t ua t i on c a n b e s u m m a r i z e d (wi th m a n y excep t ions for p a r t i c u l a r 
species) b y s a y i n g t h a t a p p e t e n c e b e h a v i o u r l e a d i n g to hos t e n g a g e m e n t is 
faci l i ta ted by o d o u r s , v i b r a t i o n s , v i sua l i m a g e s , t o u c h , s h a d o w s , a n d r a d i a n t 
h e a t . B o d y w a r m t h a n d o d o u r will no t b e effective if t h e tick is u p w i n d of 
t he hos t ; in this c i r c u m s t a n c e , v i b r a t i o n , r a d i a n t h e a t , a n d the i m a g e of t h e 
hos t , in s o m e spec ies , m a y b e c ruc ia l . T h i s m a y be especia l ly t r u e if l i gh t ing 
c o n d i t i o n s d o no t t h r o w the h o s t ' s s h a d o w across t he tick. A n a t t e m p t h a s 
b e e n m a d e to r a n k t h e gene ra l i m p o r t a n c e of hos t loca t ion factors for t icks 
( T a b l e 3 .1) , f rom w h i c h it a p p e a r s t h a t o d o u r a n d v i b r a t i o n gene ra l ly h a v e 
t h e m o s t i n fo rma t ion c o n t e n t . P r o v i d e d these s t imul i a r e p r e s e n t e d in t he 
a p p r o p r i a t e con tex t , it is p r o b a b l y t r u e to say t h a t for m o s t t icks o d o u r is 
t he key d o w n w i n d s t i m u l u s , v i b r a t i o n t he key u p w i n d s t i m u l u s , in t he 
in i t i a t ion of a p p e t e n c e b e h a v i o u r ; v is ion ( i nc lud ing s h a d o w i n g ) , t o u c h , a n d 
r a d i a n t h e a t m a y t h e n o p e r a t e in v a r i o u s c o m b i n a t i o n s w i th t he in i t i a t i ng 
s t imu l i to m a i n t a i n a p p e t e n c e a n d p r o m o t e e n g a g e m e n t . 
TABLE 3.1. TICK APPETENCE A N D ENGAGEMENT STIM-
ULI FOR H O S T LOCATION 
Nature of Effective at Directional Host Net information 
stimulus a distance information specificity content rank 
Odour + + + + + + + + + 9 
Vibration + + + + + + + 7 
Vision + + + + + 5 
Touch - + + + + 4 
Radiant heat + + + 3 
+ = possible; + + = known in some cases; + + + = known in many cases. 
Severa l w o r k e r s h a v e d i scove red t h a t p a i n t i n g or a m p u t a t i o n of t h e t a r s i 
on t he first p a i r of legs i m p e d e s t he t ick 's ab i l i ty to loca te hos t s . Lees (1948) 
o c c l u d e d t h e o p e n i n g of t h e c a p s u l e of H a l l e r ' s o r g a n a n d found t h a t th is 
in ter fered w i t h t h e t icks ab i l i ty to r e s p o n d to o d o u r s . C e r t a i n se t ae o n leg 
I h a v e b e e n i m p l i c a t e d (often from li t t le conc re t e ev idence) as tac t i le , 
h u m i d i t y , t h e r m a l , a n d o d o u r r ecep to r s . A good r a n g e of t icks h a s b e e n 
s h o w n to h a v e r e a s o n a b l y c o m p l e x eyes (cf. §3.1.5) c o n t a i n i n g m a n y p h o t o -
r e c e p t o r cells. R e c e n t l y , a n u m b e r of u l t r a s t r u c t u r a l s tud ies , u s i n g s c a n n i n g 
a n d t r a n s m i s s i o n e lec t ron m i c r o s c o p y , h a v e revea led m u c h n e w i n f o r m a t i o n 
a b o u t tick senso ry r e c e p t o r s (Sixl et al., 1971; Foel ix & Axte l l , 1971 , 1972; 
Foel ix & C h u - W a n g , 1972; C h u - W a n g & Axte l l , 1973, 1974; W a l a d d e , 1976; 
L e o n o v i c h , 1977) . H o w e v e r , t h e r e h a v e b e e n few e lec t rophys io log ica l s t ud i e s 
The Sensory Basis of Tick Feeding Behaviour 83 
a n d , un t i l t hese h a v e b e e n c a r r i e d ou t , few firm s t a t e m e n t s c a n be m a d e 
r e g a r d i n g t h e p rec i se s enso ry func t ions of t h e s t r u c t u r e s de sc r ibed by l ight 
a n d e lec t ron m i c r o s c o p y . I n §3.2.2 w e d e s c r i b e s o m e recen t w o r k o n the 
u l t r a s t r u c t u r e a n d e l ec t rophys io logy of t h e sensi l la in H a l l e r ' s o r g a n . T h i s 
c o m p l e x of s enso ry r e c e p t o r s is m o s t likely t he m a i n hos t l oca t ing a n d o d o u r 
sens ing o r g a n in m a n y tick spec ies . I t s h o u l d be e m p h a s i z e d , howeve r , t h a t 
m a n y o t h e r s enso ry r ecep to r s on t a r s u s I , a p a r t f rom H a l l e r ' s o r g a n , a r e 
likely to b e invo lved in hos t loca t ion . T h e s e r ecep to r s a r e , for r e a s o n s of 
c o n v e n i e n c e , d e s c r i b e d in §3 .3 .2 . 
3.2.2. Ultrastructure and Electrophysiology of Sensil la on Tarsus I, 
Inc luding Haller's Organ 
A va r i e ty of sensi l la , m o n i t o r i n g a w i d e r a n g e of e n v i r o n m e n t a l p a r a m e t e r s , 
a r e found on t h e t a r s i of t he first p a i r of legs in all s t ages of t icks. T h e y 
r e p r e s e n t a c o m p l e x of sensory r e c e p t o r s . Ea r l i e r m o r p h o l o g i c a l de ta i l s of 
t a r s u s I sensi l la c a m e from l ight mic roscop ica l inves t iga t ions ( N u t t a l et al., 
1908; Schu lze , 1941; Z o l o t a r e v & S in i t z ina , 1965). S ince t hen , fine s t r u c t u r a l 
s tud ies b y a n u m b e r of w o r k e r s h a v e e l u c i d a t e d t he i n n e r v a t i o n of these 
sensi l la a n d t h e r e l a t i on b e t w e e n thei r r e c e p t o r cells a n d the e n v i r o n m e n t . 
Sixl et al. (1971) u sed s c a n n i n g e lec t ron m i c r o s c o p y ( S E M ) to inves t iga te 
t he olfactory o r g a n s of Ornithodoros papillipes, R. sanguineus, a n d severa l o t h e r 
tick spec ies . Foel ix a n d Axte l l (1971) , u s i n g s c a n n i n g a n d t r a n s m i s s i o n 
e lec t ron m i c r o s c o p y ( T E M ) p e r f o r m e d a c o m p r e h e n s i v e u l t r a s t r u c t u r a l 
ana lys i s of t a r s a l sensi l la i n c l u d i n g those of H a l l e r ' s o r g a n in Amblyomma 
amencanum a n d , ve ry recen t ly , L e o n o v i c h (1977) r e p o r t e d de ta i l s of t h e 
s t r u c t u r e of H a l l e r ' s o r g a n sensi l la in / . persulcatus. R e c h a v et al. (1977) u sed 
S E M to e x a m i n e H a l l e r ' s o r g a n in m a l e Amblyomma hebraeum a n d d e m o n -
s t r a t e d w i t h a cho ice -o l fac tomete r t h a t o l factory r e c e p t o r cells in the sensi l la 
of H a l l e r ' s o r g a n de t ec t t he p r e s e n c e of p h e r o m o n e s . L igh t a n d S E M tech-
n i q u e s w e r e u s e d to inves t iga t e t h e de ta i l s of all t a r sa l sensi l la in B. microplus 
( W a l a d d e , 1976, 1977) . I n a l a t e r s t u d y ( W a l a d d e & Rice , 1982) t he u l t r a -
s t r u c t u r e of s enso ry e l e m e n t s in H a l l e r ' s o r g a n of B. microplus w e r e d e s c r i b e d 
a n d e lec t rophys io log ica l m e t h o d s w e r e u s e d to o b t a i n p r e l i m i n a r y infor-
m a t i o n a b o u t t h e r e s p o n s e of H a l l e r ' s o r g a n sensi l la to factors of p o t e n t i a l 
i m p o r t a n c e in t h e n a t u r a l e n v i r o n m e n t of t he t ick. 
S E M s tud ie s of a d u l t B. microplus s h o w the p r e s e n c e of t h r ee m e d i a l d o r s a l 
sensi l la (Fig . 3.6; m d 1-3 in t h e n o m e n c l a t u r e of W a l a d d e , 1976, 1977) ly ing 
d i s ta l to H a l l e r ' s o r g a n . T h e l i t e r a t u r e o n these sensi l la is confus ing b e c a u s e 
of t he d ivers i ty of n a m e s t h a t h a v e b e e n used . Schu lze (1941) cal led t h e m 
the front h a i r tuft ( V o r d e r e s H a a r b ü s c h e l ) , Lees (1948) used the t e r m a n t e r i o r 
br is t le g r o u p , wh i l e Z o l o t a r e v a n d S in i t z ina (1965) cal led t h e m X3, and t hey 
were cal led t h e d i s t a l br i s t les by Axte l l et al. (1971) . P rox ima l ly , H a l l e r ' s 
84 S. M. Waladde and M. J. Rice 
o r g a n cons is t s of u n i q u e i n d e p e n d a t e g r o u p i n g s of sensi l la , o n e found in t h e 
a n t e r i o r p i t ( ap) a n d the o t h e r in t he pos t e r io r c a p s u l e (cap) (Fig. 3 .6) . I n 
this c h a p t e r , t he H a l l e r ' s o r g a n of a d u l t B. microplus is de sc r ibed as a m o d e l 
for c o m p a r i s o n to o t h e r species . 
3.2.2.1. Ultrastructure of the Anterior Pit Sensilla T h e a n t e r i o r p i t of a d u l t B. 
microplus c o n t a i n s six sensi l la ( r a n g i n g from 5 to 20 μηι long) ; t h e longes t 
m e m b e r of t he g r o u p is a p 1, w h i c h is a p p r o x i m a t e l y 4 t imes longer t h a n 
a n y of t he o t h e r s (F igs . 3.6 a n d 3 .11) . I n A. americanum t he a n t e r i o r p i t g r o u p 
cons is t s of seven sensi l la of w h i c h the long sensi l la , A l a n d A 2 , a r e b l u n t -
t i p p e d , m a r k e d l y c u r v e d a n d w i t h evenly d i s t r i b u t e d po res in the i r cu t i cu l l a r 
wal ls as d e t e c t e d w i t h S E M a t h igh magn i f i ca t ions (Foel ix & Axte l l , 1972) . 
R e p o r t s by v a r i o u s w o r k e r s (E l iza rov , 1963; Leonov ich , 1977) i nd i ca t e t h a t 
a d u l t s of o t h e r h a r d t icks a lso h a v e 6 - 7 sensi l la in t he a n t e r i o r p i t . H o w e v e r , 
the l a r v a of A. americanum h a s five sensi l la (Axtel l et al., 1971) a n d a s imi l a r 
n u m b e r h a s b e e n o b s e r v e d in a d u l t s of t he soft t ick 0. papillipes (Sixl et al., 
1971). A l t h o u g h v a r i a t i o n s in n u m b e r s of a n t e r i o r pi t sensi l la occu r a m o n g 
tick species , t he p r e s e n c e of long a n d shor t sensi l la is a un ive r sa l fea ture . 
F i n e s t r u c t u r a l de ta i l s of t h e a n t e r i o r p i t sensi l la in B. microplus s h o w the re 
a r e a t leas t four s t r u c t u r a l l y different types of sensi l la . 
T h e first t y p e ( a p 1) h a s a th ick-wal led cut ic le ( 0 .8 -1 .3 μηι) pe r fo ra t ed b y 
n u m e r o u s p o r e s (Fig . 3 .7) . E a c h p o r e h a s a n ex t e rna l o p e n i n g of 0.2 μpiι 
d i a m e t e r w h i c h l eads to a p l u g (0.15 μpiι d i a m e t e r ) snug ly fitting in to t h e 
ex t e rna l e n d of a c h a n n e l (Fig . 3 .8.) . T h e c h a n n e l s a r e 0.5 μpiι long a n d l ead 
d i rec t ly i n to t h e l u m e n of t he sens i l lum, w h i c h c o n t a i n s severa l d e n d r i t e 
b r a n c h e s b a t h e d by the sens i l lum l iquor (cf. S t e i n b r e c h t & M u l l e r , 1976) . 
I t c a n be env i saged t h a t the c i r cu la r g a p s a r o u n d the p lugs (Fig. 3.8.) p r o v i d e 
p a t h w a y s for t he diffusion of s t imul i to the recep t ive si tes, p r e s u m a b l y loca ted 
on t h e d e n d r i t e m e m b r a n e s ( S c h n e i d e r et al., 1964; Ka i s s l ing , 1969; Kafka , 
1970; V a r e s c h i , 1971). T h i s be ing the case , t he d i s ta l reg ion of a p 1 is m o r e 
o p e n to rece iv ing s t imul i b e c a u s e it h a s a h i g h e r p o r e dens i ty as well as m o r e 
d e n d r i t i c b r a n c h e s t h a n the p r o x i m a l reg ion of t he sens i l lum. T o w a r d s t h e 
b a s e of t he sens i l l um the wal l s h a v e n o po re s a n d th ree s e p a r a t e sco lopa les 
beg in to a p p e a r ins ide t he l u m e n . T h e a p p e a r a n c e of t he sco lopa les a lso 
m a r k s t he p o i n t w h e r e d e n d r i t i c b r a n c h i n g beg ins (Fig. 3 .9.) . M o r e p rox i -
mal ly , in t he shaft of the sens i l lum, t he r e a r e t h r ee b u n d l e s , e ach of five 
d e n d r i t e s , a n d e a c h c o n t a i n e d in a sco lopa le s h e a t h (Fig. 3 .10) . T h e s e p a r t s 
of the d e n d r i t e s , p lus the i r d i s ta l b r a n c h i n g ex tens ions , r e p r e s e n t t he o u t e r 
s e g m e n t s of t he sensory n e u r o n s . I n A. americanum, sensi l la A l a n d A 2 a r e 
very s imi l a r to t h e t ype de sc r ibed a b o v e . A cross-sect ion t h r o u g h t h e b a s e 
FlGS. 3.5—3.6 Boophilus microplus tarsus I sensilla as revealed by scanning electron microscopy: 
3.5, tarsus I (scale equals 10 μpiι); 3.6, Haller's organ and adjacent sensilla; anterior pit (ap), 
posterior capsule (pc), (scale equals 10 μpiι). 
The Sensory Basis of Tick Feeding Behaviour 85 
POT - D 
86 S. M. Waladde and M. J. Rice 
of these sensi l la s h o w s A 2 is i n n e r v a t e d by five n e u r o n s in a s ingle sco lopa le , 
w h e r e a s A l h a s n i n e n e u r o n s , o n e g r o u p of five a n d a n o t h e r of four, e a c h 
g r o u p enc losed in its o w n sco lopa le (Foel ix & Axte l l , 1972). 
T h e s econd t y p e of a n t e r i o r p i t s ens i l l um ( 1 0 - 2 0 μιτι long) is a th i ck -wa l l ed 
h a i r ( 0 . 6 - 7 μpiι ) w h i c h is finely sca l loped a n d b e a r s 4 - 5 , l o n g i t u d i n a l sur face 
g rooves . T h e r e a r e t h r e e of these h a i r s , t w o c o n t a i n i n g t h r ee d e n d r i t e s ( a p 
2, 3) (Fig . 3.11) a n d o n e c o n t a i n i n g four d e n d r i t e s ( a p 4 ) . I n all of t hese 
sensi l la , o n e o r t w o d e n d r i t e s a p p e a r to r e a c h t h e sensi l lum t ip , t h e o t h e r s 
t e r m i n a t i n g m o r e p r o x i m a l l y . T h e t h r ee u n b r a n c h e d d e n d r i t e s of e a c h sen-
s i l lum a r e b a t h e d b y a n e l ec t ron -dense sens i l lum l iquor c o n t a i n e d in a 
c u t i c u l a r t u b e w h i c h forms t h e c e n t r a l l u m e n . T h i s sens i l lum type h a s a 
" s p o k e - w h e e l a r r a n g e m e n t " w i t h t he d e n d r i t e s o c c u p y i n g t h e " h u b " (Ste in-
b r e c h t , 1969; Foel ix & Axte l l , 1972) . T h e p e r i p h e r a l l u m i n a s e p a r a t i n g t h e 
spokes a r e c o n t i n u o u s w i t h a c o m m o n l u m e n a t t he b a s e (Fig. 3 .11) . F i n e 
cana l s (0.07 μpiι d i a m e t e r ) , filled w i t h t he e l ec t ron -dense sens i l lum l iquor , 
r a d i a t e f rom t h e c e n t r a l l u m e n ( h u b ) t h r o u g h t h e spokes to o p e n in t h e 
l o n g i t u d i n a l g rooves o n t h e sens i l lum surface . T o w a r d s t he t ip of t h e sen-
s i l lum, t h e spoke -whee l s t r u c t u r e s t a r t s to b r e a k d o w n b u t t he c u t i c u l a r t u b e 
w h i c h c o n t a i n s t h e d e n d r i t e s is still p r e sen t . 
T h e t h i r d t y p e of a n t e r i o r p i t s ens i l lum, a p 5, h a s a s m o o t h surface , it is 
7 μpiι l ong a n d is i n n e r v a t e d b y t w o d e n d r i t e s (Fig . 3 .11) . O n e of t h e d e n d r i t e s 
t e r m i n a t e s n e a r t h e t ip , l eav ing t h e o t h e r in t he c u t i c u l a r t u b e . As t h e r e is 
n e i t h e r a d i s t a l o p e n i n g n o r a p o r e s y s t e m in t h e br i s t le shaft of th is s ens i l l um, 
it is n o t k n o w n if i ts d e n d r i t e s c o m m u n i c a t e w i t h t he e x t e r n a l e n v i r o n m e n t . 
T h e four th a n d las t t ype of s ens i l l um in t h e a n t e r i o r p i t is r e p r e s e n t e d b y 
a s ingle ha i r , a p 6 (5 μpiι l o n g ) . I t h a s severa l sha l low grooves ( co r ruga t i ons ) 
r u n n i n g l o n g i t u d i n a l l y a l o n g t h e h a i r shaft; t hese s m o o t h o u t t o w a r d s t h e 
sens i l l um b a s e . T h i s is a th ick-wal led sens i l l um (0.8 μpiι) i n n e r v a t e d b y t h r e e 
d e n d r i t e s (Fig . 3 .11) . N o p o r e s y s t e m h a s b e e n found in t he h a i r shaft , b u t 
t he r e cou ld b e a d i s t a l o p e n i n g t h r o u g h w h i c h the d e n d r i t e s c o m m u n i c a t e 
w i t h t h e e x t e r n a l e n v i r o n m e n t . 
L a r g e p l u g g e d p o r e s a r e n o t on ly found in th ick-wal led sens i l lum a p 1, of 
t he a n t e r i o r p i t , b u t a l so in m d 3 on the m e d i a l d o r s a l surface . I t is i n t e r e s t i ng 
to n o t e t h a t in A.amencanum t h e d i s ta l b r i s t le , d 1 (Foel ix & Axte l l , 1971) , 
r e s e m b l e s m d 3 in B. microplus, wh i l e t h e a n t e r i o r p i t sensi l la , A l a n d A 2 
(Foel ix & Axte l l , 1972) , a r e s imi l a r to t he a p 1 sens i l lum of B. microplus. T h i s 
is t h e on ly s ens i l l um of its k ind in t h e a n t e r i o r p i t of B. microplus. U l t r a s t r u c -
t u r a l de ta i l s of t h e H a l l e r ' s o r g a n of A. amencanum (Foel ix & Axte l l , 1972) , 
FIGS. 3.7-3.10. Boophilus microplus sensillum ap
1
 of the anterior pit as revealed by transmission 
electron microscopy: 3.7, section through the shaft of ap
1
 (scale equals 1 μpiι); 3.8, detail of a 
"plugged" pore (scale equals 0.5 μpiι); 3.9, branching dendrites at sensillum base (scale equals 
0.5 μpiι); 3.10, base arrangement of 3 X 5 dendrites (scale equals 1 μpiι). Note scolopale (s) 
surrounding dendrites (d) and plugged pore (arrow) in thick cuticle (z). 
The Sensory Basis of Tick Feeding Behaviour 87 
88 S. M. Waladde and M. J. Rice 
FIG. 3.11. Diagram of the anterior pit sensilla of Boophilus microplus, showing the numbers and 
arrangement of dendrites and cuticular components in each of the six sensilla. 
/. persulcatus ( L e o n o v i c h , 1977) , a n d those r e p o r t e d h e r e for B. microplus, h a v e 
r evea led t h a t t h e th ick -wa l l ed sensi l la of t he a n t e r i o r p i t m a y c o n d u c t o d o u r 
s t imul i b y a t l eas t t w o different s t r u c t u r e s , e i the r by evenly d i s t r i b u t e d , 
loosely p l u g g e d p o r e s , o r by secret ion-fi l led c a n a l s ( cha rac t e r i s t i c of g r o o v e d , 
spoke -whee l sens i l l a ) . 
T h r e e a n t e r i o r p i t sensi l la , a p 2 - 4 , of B. microplus b e long to t he spoke -
whee l t ype a s a l r e a d y d e s c r i b e d for a n t e r i o r p i t sensi l la A 3 a n d A 5 in A. 
americanum (Foel ix & Axte l l , 1972) . S imi l a r s t r u c t u r e s h a v e b e e n r e p o r t e d in 
t h e a n t e n n a l sensi l la of o t h e r a r t h r o p o d s , i n c l u d i n g t h e g r a s s h o p p e r Locusta 
migratoria migratorioides (S t e inb rech t , 1969) a n d the cock roaches Arenivaga 
( H a w k e & Fa r l ey , 1971a, b) a n d Periplaneta americana (A l tne r et al., 1977) . 
T h e e lec t rophys io log ica l w o r k of W a l d o w (1970) o n locus ts s h o w e d t h a t t h e 
spoke -whee l sensi l la " a r e e i the r p u r e l y olfactory or they r e s p o n d to h u m i d i t y 
a n d t e m p e r a t u r e c h a n g e s " . O t h e r inves t iga to r s (Lof tus , 1968, 1976; A l t n e r 
et al., 1977) h a v e found t h a t t h e g rooved , spoke-whee l sensi l la c o n t a i n 
h y g r o - a n d t h e r m o r e c e p t i v e un i t s as well as c h e m o r e c e p t i v e u n i t s . By a n a l o g y 
it is poss ib le t h a t t h e spoke -whee l sensi l la in t h e a n t e r i o r p i t , a n d t hose o n 
t h e a d j a c e n t r eg ions of t h e t a r s u s , r e s p o n d to h u m i d i t y a n d t e m p e r a t u r e 
The Sensory Basis of Tick Feeding Behaviour 89 
s t imul i . T h e m u l t i p l e i n n e r v a t i o n by b r a n c h i n g d e n d r i t e s of a p 1, howeve r , 
sugges t s t h a t th is is a we l l -deve loped olfactory r ecep to r , ab l e to d i s c r i m i n a t e 
a va r i e ty of o d o u r s . T h e func t ions of a p 5 a n d 6 a r e no t c lear . 
3.2.2.2. Electro physiology of the Anterior Pit Sensilla As s h o w n by T E M , t h e 
a n t e r i o r p i t sensi l la of a d u l t B. microplus a r e a s soc ia t ed w i t h th i r ty n e u r o n s . 
T h i s d e n s i t y of i n n e r v a t i o n impl i e s d ive r se r e spons iveness to a w i d e r a n g e 
of s t imul i . S o m e p r e l i m i n a r y e lec t rophys io log ica l d a t a s u p p o r t t h a t a s s u m p -
t ion. H u m a n b r e a t h a n d c a t t l e w a s h c a n b o t h h a v e e i the r s t i m u l a t i n g o r 
i n h i b i t i n g effects d e p e n d i n g o n t h e pos i t ion of t h e r e c o r d i n g t ip of t he t u n g s t e n 
e l ec t rode a n d t h e n e u r o n s w h i c h a r e r e c o r d e d (Fig . 3 .12) . T h e p a t t e r n s of 
r e s p o n s e (i .e. f r equency , a d a p t a t i o n r a t e , a n d after effects) t h a t a r e t r iggered 
b y t h e a p p l i c a t i o n of vola t i les a l so d e p e n d s o n t h e iden t i ty of n e u r o n s . 
I n a reg ion like t h e a n t e r i o r p i t , w h e r e t h e sensi l la a r e close to e ach o t h e r , 
it is difficult to a s soc ia t e t h e r e c o r d e d un i t s w i t h a p a r t i c u l a r sens i l lum. 
T e c h n i q u e s w h i c h c a n o v e r c o m e th is difficulty h a v e a l r e a d y b e e n successfully 
a p p l i e d in w o r k on a n t e n n a l r e cep to r s of cock roaches (Al tne r et al., 1977) . 
V 
FlG. 3.12. Single unit recording from the anterior pit of a Boophilus microplus adult: a, inhibition 
of firing by dryair; b, response to dry air plus 50% cattlewash; c, response to dry air plus 100% 
cattlewash; d, response to human breath; e, re-application of dry air causes inhibition as in 
trace a (scale equals 0.5 s). 
90 S. M. Waladde and M. J. Rice 
If s u c h m e t h o d s a r e a p p l i e d to t he a n t e r i o r pi t a n d o t h e r t a r sa l sensi l la , it 
m a y be poss ib le in fu ture to p i n p o i n t t h e sensi l la r e spons ib l e for p a r t i c u l a r 
r e s p o n s e p a t t e r n s to o n e or m o r e s t imul i . T h e t races g iven in Fig . 3.12 s h o w 
s o m e of t h e tes ts t h a t h a v e b e e n d o n e a n d d e m o n s t r a t e t he p o t e n t i a l for 
fu r the r work . D r y a i r by itself w a s a n inh ib i to r , whi le d r y a i r p lu s ca t t l e -
w a s h w e r e s t i m u l a t i n g , w i th t h e d e g r e e of s t i m u l a t i o n d e p e n d i n g o n the 
c o n c e n t r a t i o n of t h e c a t t l e w a s h . A p p l i c a t i o n of h u m a n b r e a t h a lso h a d a 
c o m p a r a t i v e l y s t i m u l a t i n g effect, b u t t he r e s u l t a n t p a t t e r n h a d a m u c h lower 
i m p u l s e f r equency t h a n t h a t c a u s e d by c a t t l e w a s h . 
Lees (1948) sugges t ed t h a t t he pos t e r io r c apsu l e is c o n c e r n e d w i t h t h e 
r ecep t ion of smel l ; th is h a d b e e n conf i rmed b y e lec t rophys io log ica l tests in 
B. microplus, w h i c h s h o w t h a t olfactory s t imul i ( ca t t l ewash , h u m a n b r e a t h , 
a n d C O 2 ) d o evoke r e sponses in t he a n t e r i o r p i t ( W a l a d d e , 1978). T h e 
th ick-wa l l ed sens i l l um a p 1 of t he a n t e r i o r p i t is t he only se ta b e a r i n g p l u g g e d 
po res , r e s e m b l i n g t h e t h in -wa l l ed sensi l la in t he pos t e r io r c apsu l e in t h a t 
respec t . Foel ix a n d Axte l l (1972) p r o p o s e d t h a t t he m a t e r i a l s u s p e n d i n g the 
p l u g in t h e p o r e is p e r m e a b l e to o d o u r molecu les , s ince t he m a t e r i a l a l so 
p e r m i t s e n t r y of dyes i n to t he sens i l lum. T h e s e worke r s a lso r e p o r t e d a 
surface c o a t i n g on t h e c a p s u l e sensi l la , w h i c h is poss ib ly s imi la r to surface 
depos i t s occas iona l ly no t i ced on the a n t e r i o r p i t sens i l lum a p 1 of B. microplus. 
S u c h coa t s m a y b e a n e x t e r n a l man i f e s t a t i on of t he sens i l lum l iquor . O n 
s t r u c t u r a l g r o u n d s it is poss ib le t h a t sens i l lum a p 1 m a y h a v e ce r t a in funct ions 
in c o m m o n w i t h t h e c a p s u l e sensi l la (see b e l o w ) . 
T h e u l t r a s t r u c t u r a l d ivers i ty of i n n e r v a t i o n , i n t e r n a l a r r a n g e m e n t , a n d 
poros i ty of t h e four types of a n t e r i o r p i t sensi l la in a d u l t B. microplus, t o g e t h e r 
w i th t he w i d e r a n g e of c h e m i c a l r e spons iveness of the i r n e u r o n s , i nd i ca t e s 
t h a t t hey m o n i t o r d ive r se e n v i r o n m e n t a l p a r a m e t e r s . H u m i d i t y a n d o t h e r 
o d o u r s t imu l i a r e m o s t likely m o n i t o r e d by the p o r o u s sensi l la ( a p 1-4), 
t h o u g h th is w o u l d n o t p r e c l u d e t he poss ibi l i ty t h a t they c o n t a i n t h e r m o -
recep t ive n e u r o n s . M o d e r n u l t r a s t r u c t u r a l a n d e lec t rophys io log ica l t ech-
n i q u e s h a v e led to a n e x p a n d e d ins igh t in to a n t e r i o r p i t funct ion . B a s e d o n 
b e h a v i o u r a l o b s e r v a t i o n s , Lees (1948) h a d s t a t ed t h a t t he a n t e r i o r p i t o f / . 
ricinus func t ions on ly as a h u m i d i t y r ecep to r . T h u s , ini t ia l a p p l i c a t i o n of t h e 
n e w e r t e c h n i q u e s revea l s t h e ex t en t of t he work w h i c h r e m a i n s to b e a c c o m -
p l i shed before t h e func t ions of all t h i r ty n e u r o n s a r e e luc ida t ed . 
3.2.2.3. Ultrastructure of the Posterior Capsule Sensilla T h e capsu l e of H a l l e r ' s 
o r g a n is r ead i ly e x a m i n e d in w h o l e m o u n t s by l ight m ic roscopy . U s i n g this 
p r o c e d u r e t h e c a p s u l e of B. microplus w a s found to c o n t a i n a t leas t twe lve 
se tae ( W a l a d d e , 1976) . T E M h a s revea led t h a t on ly four of t h e se t ae a r e 
i n n e r v a t e d ; t he r e m a i n i n g h a i r s a r e non - senso ry a n d v a r y in n u m b e r f rom 
s p e c i m e n to s p e c i m e n ( W a l a d d e & Rice , 1982). T h e floor of t he c a p s u l e , 
s l a n t i n g a t a 45° ang l e w i th respec t to the l o n g i t u d i n a l axis of t h e t a r s u s , 
b e a r s a s ens i l l um ( c a p 1) a t i ts p r o x i m a l b o r d e r w h i c h s tops j u s t be low t h e 
The Sensory Basis of Tick Feeding Behaviour 91 
FlG. 3.13. Diagram of the four capsular sensilla and their innervation in the adult Boophilus 
micro plus. 
oval o p e n i n g in t h e c a p s u l e d o m e ( W a l a d d e , 1976, 1977). A t a s l ight ly lower 
level, a m o r e p l u m p sens i l l um ( c a p 2) is flanked by t w o re la t ively s l ende r 
sensi l la ( c a p 3 a n d 4) (Fig . 3 .12) . All c a p s u l a r sensi l la a r e of t he t h in -wa l l ed 
t ype (0 .25 μ pi ι ) . E a c h sens i l l um p o i n t s t o w a r d s t he oval o p e n i n g a n d is evenly 
pe r fo ra t ed a t its d i s t a l e n d b y re la t ive ly l a rge p l u g g e d pores (0.2 μpiι d i a m -
e t e r ) . Sens i l l um c a p 2 is s u p p l i e d b y four b u n d l e s c o n t a i n i n g 5, 5, 4, a n d 3 
d e n d r i t e s , respec t ive ly , b u t t h e o t h e r t h r e e sensi l la a r e e ach s u p p l i e d b y four 
d e n d r i t e s . All d e n d r i t e s leave the i r sco lopa les n e a r t he b a s e of t he sensi l la 
a n d b r a n c h u p w a r d s i n to t h e l u m e n (wi th its pe r fo ra t ed wa l l s ) . T h e d e g r e e 
of b r a n c h i n g is m o r e p r o n o u n c e d in sensi l la c a p 1 a n d 2, by c o m p a r i s o n to 
t h a t in sensi l la c a p 3 a n d 4. M o s t of t hese fea tures a r e a lso found in t h e 
c a p s u l e of H a l l e r ' s o r g a n of a d u l t A. americanum w h i c h h a s seven i n n e r v a t e d 
sensi l la s u p p l i e d by 3.5 d e n d r i t e s e a c h . T h e p l u g s , a p p r o x i m a t e l y 500 p e r 
sens i l lum, a r e r e p o r t e d l y s u s p e n d e d b y s o m e fibrous m a t e r i a l f rom the i r 
i n n e r edges (Foel ix & Axte l l , 1972) . M o r p h o l o g i c a l l y , t he c a p s u l e sensi l la 
r e s e m b l e t h e ol factory sens i l la b a s i c o n i c a in insec ts (Slifer, 1954; S t e i n b r e c h t , 
1969; E r n s t , 1969; r ev i ewed by Slifer, 1970) from w h i c h they differ, howeve r , 
in the re la t ive ly l a rge size of the i r p l u g g e d p o r e s . 
92 S. M. Waladde and M. J. Rice 
3.2.2.4. Electrophysiology of the Posterior Capsule Sensilla I n sp i te of t h e c a p s u l a r 
d o m e w h i c h p r o t e c t s t h e four sensi l la of the pos t e r io r capsu l e , it is poss ib le 
to o b t a i n e lec t rophys io log ica l d a t a f rom the t w e n t y - n i n e i n n e r v a t i n g n e u r o n s . 
E lec t r i ca l ac t iv i ty from the pos t e r io r c a p s u l e n e u r o n s , like t h a t f rom the 
a n t e r i o r p i t n e u r o n s , is q u i t e v a r i a b l e , a p a r t i c u l a r s t i m u l u s c a n c a u s e m o r e 
t h a n o n e k ind of r e s p o n s e d e p e n d i n g on the iden t i ty of the un i t r e s p o n d i n g 
( W a l a d d e , 1978) . F u r t h e r m o r e , t he pos t e r io r c apsu l e n e u r o n s c a n de t ec t 
c h a n g e s in t he c o m p os i t i o n a n d c o n c e n t r a t i o n of t he c h e m i c a l s t imul i . 
W i l k i n s o n (1953) o b s e r v e d t h a t a puff of a i r o n t he l a rvae of B. microplus 
in the i r n a t u r a l e n v i r o n m e n t , j u s t sufficient to cause pe rcep t i b l e m o v e m e n t 
of t he g ra s s , p r o d u c e d n o r e s p o n s e in a c lus te r of l a rvae . A v io lent puff of 
a i r p r o d u c i n g a s t r o n g m o v e m e n t of t he g rass i n d u c e d a w e a k r e s p o n s e . 
H o w e v e r , w h e n h u m a n b r e a t h (i.e. o l factory, h u m i d i t y , a n d w a r m t h s t imul i ) 
w a s a p p l i e d , t h e r e w a s a s t r o n g q u e s t i n g r e sponse . T h i s impl ies t h a t b r e a t h 
o d o u r s from g r a z i n g ca t t l e a r e likely to effect s imi la r r eac t ion in t icks t h a t 
"l ie in w a i t " . E lec t rophys io log ica l tests h a v e s h o w n t h a t w h e r e a s puffing of 
r o o m a i r on b o t h reg ions of H a l l e r ' s o r g a n h a s m i n o r effect, s imi la r a p p l i -
ca t ions of h u m a n b r e a t h o r low c o n c e n t r a t i o n s of C 0 2 c a u s e m a r k e d c h a n g e s 
in t h e b a c k g r o u n d i m p u l s e f requencies d e t e c t a b l e from b o t h reg ions of t he 
o r g a n . Senso ry i n p u t s of th is n a t u r e m a y lead , v ia s y n a p t i c c i rcu i t ry in t he 
s y n g a n g l i o n , to a p p r o p r i a t e m o t o r o u t p u t man i fes ted in q u e s t i n g a n d o t h e r 
b e h a v i o u r a l r e sponse s . 
T h e resu l t s g iven h e r e w e r e o b t a i n e d from a d u l t t icks, a n d they d e m o n s t r a t e 
s o m e t h i n g of t he c o m p l e x i t y of t he e lec t rophys io logy of the sensi l la in H a l l e r ' s 
o r g a n . M u c h w o r k r e m a i n s to be d o n e on the sensi l la of l a rva l H a l l e r ' s o r g a n 
if hos t loca t ion is to be u n d e r s t o o d in B. microplus. R e c o r d i n g s n e e d to be 
m a d e from m a n y o t h e r types of t icks if we a r e to u n d e r s t a n d m o r e of t he 
c o m p a r a t i v e phys io logy of hos t loca t ion (cf. §2 .1) . T h e ex is tence of m a n y 
o the r , m u l t i - i n n e r v a t e d sensi l la on t he t a r s i p laces H a l l e r ' s o r g a n in pe r -
spec t ive , as on ly o n e of a va r i e ty of sensi l la involved in hos t loca t ion . 
T h e e lec t rophys io log ica l r e sponses o b t a i n e d so far f rom the H a l l e r ' s o r g a n 
sensi l la of B. microplus a r e in m a n y w a y s s imi la r to those r e c o r d e d from H. 
asiaticum a n d / . persulcatus (E l iza rov , 1963, 1965; S in i tz ina , 1974) in b e i n g 
m a i n l y q u a l i t a t i v e . I t is c lear ly poss ib le to r eco rd i m p u l s e s from s ingle , o r 
severa l , r e c e p t o r cells w h i c h usua l ly h a v e a r e s t ing f requency . H o w e v e r , like 
olfactory n e u r o n s of o t h e r a r t h r o p o d s (Schne ide r , 1969), it is no t k n o w n 
w h e t h e r t h e r e s t ing f requency is a t ru ly s p o n t a n e o u s p h e n o m e n o n o r a n 
FlGS. 3.14—3.15. Other sensilla on tarsus I: 3.14, transverse section through base of sensillum 
md 4 of Boophilus microplus showing two mechanoreceptor endings at the base and seven dendrites 
extending into the shaft (scale equals 1 μιη); 3.15, transverse section through the distal region 
of the "4 group" sensillum of Amblyomma americanum showing the "vase-shaped" channels which 
connect the central lumen to the exterior (scale equals 0.2 μpiι). (From Foelix & Axtell, 1970.) 
The Sensory Basis of Tick Feeding Behaviour 93 
94 S. M. Waladde and M. J. Rice 
ar te fac t c a u s e d b y t h e i n t r o d u c t i o n of t he e lec t rode . S o m e e lec t rophys io log ica l 
i nves t iga t ions o n tick olfactory r ecep to r s h a v e d e a l t w i th t he effects of r epe l l en t 
c o m p o u n d s (E l i za rov , 1963; Z o l o t a r e v & El i za rov , 1964a, b) a n d o t h e r s , to 
a lesser ex t en t , w i t h t ick sex p h e r o m o n e s ( C h o w , 1970, 1974). B e h a v i o u r a l 
s tud ie s h a v e r evea led t h a t b o t h sex a n d a s s e m b l y p h e r o m o n e s p l a y a n 
i m p o r t a n t role in t ick o r i e n t a t i o n . T h i s k n o w l e d g e o u g h t to be s u p p l e m e n t e d 
w i t h q u a l i t a t i v e a n d q u a n t i t a t i v e e lec t rophys io log ica l s tud ie s . All of t h e t a r s a l 
sensi l la a p p e a r to b e idea l for these k i n d s of s t u d y b e c a u s e they h a v e re la t ive ly 
few n e u r o n s w h o s e d i s t r i b u t i o n a m o n g the v a r i o u s sensi l la is n o w k n o w n . 
I n s o m e cases i m p u l s e a m p l i t u d e s from the v a r i o u s sensi l la a r e k n o w n a n d 
m a y b e sufficiently different to p e r m i t r ecogn i t ion of t he cells r e s p o n d i n g to 
g iven s t imu l i . F u r t h e r m o r e , c h a n g e s in t he r e s t ing f requency m a y b e u s e d 
to d i s t i n g u i s h those s t imu l i w i t h i nh ib i t o ry from those w i t h s t i m u l a t o r y 
effects. T h e k n o w l e d g e g a i n e d from this k ind of w o r k m i g h t b e ve ry useful 
w h e n d e v e l o p i n g n e w m e t h o d s of tick con t ro l b a s e d on the m a n i p u l a t i o n of 
tick b e h a v i o u r . 
3.2.2.5. Tarsal Receptors Other than those of Haller's Organ I n all t icks, t he m e d i a n 
d o r s a l sur face of t a r s u s 1 b e a r s a n u m b e r of o t h e r sensi l la w i t h u l t r a s t r u c t u r a l 
fea tures s imi l a r to t hose of sensi l la in H a l l e r ' s o r g a n . P r io r to t he a p p l i c a t i o n 
of T E M a n d S E M t e c h n i q u e s these sensi l la w e r e r e g a r d e d as e i the r p ro t ec t ive 
br is t les o r tac t ic le r e c e p t o r s ( N u t t a l l et al., 1908; Lees , 1948); th is v iew c a n 
n o l onge r b e s u s t a i n e d . 
Sens i l l um m d 3 r e s e m b l e s a p 1, h a v i n g th ick wal ls pe r fo ra ted by p l u g g e d 
p o re s . I n s i d e , five d e n d r i t e s d iv ide i n to severa l b r a n c h e s as they r u n u p 
ins ide t h e l u m e n . A l t h o u g h th is sens i l lum h a s t h e s t r u c t u r e of a n ol factory 
c h e m o r e c e p t o r , e lec t rophys io log ica l i n fo rma t ion is n e e d e d to conf i rm its 
func t ion . 
Sensi l la m d 4 a n d 6 a r e th ick-wal led , w i t h po re s in g rooves ; like a p 2 - 4 
the i r c ross -sec t ions s h o w a n i n t e r n a l spoke-whee l a r r a n g e m e n t . T h e a c t u a l 
func t ion of these sensi l la is n o t ye t k n o w n . M d 4 a n d 6 differ f rom a p 2 - 4 
in h a v i n g p a i r s of m e c h a n o r e c e p t o r s w h i c h t e r m i n a t e a t the i r ba se s a n d in 
h a v i n g seven d e n d r i t e s r u n n i n g u p the i r c e n t r a l l u m i n a , r a t h e r t h a n the t h r e e 
found in t h e a n t e r i o r p i t sensi l la (Fig . 3 .14) . 
Sensi l la m d 9 a n d 10 a r e a lso th ick-wal led b u t h a v e n o a s soc ia t ed 
m e c h a n o r e c e p t o r d e n d r i t e s . M o r e o v e r , two d e n d r i t e s r u n u p the i r c e n t r a l 
l u m i n a . T h e s e sensi l la a r e a lso c h a r a c t e r i z e d by grooves r u n n i n g t h e en t i r e 
l eng th of the i r s e t ae w i t h p o r e s t h a t l ead in to v a s e - s h a p e d c o m p a r t m e n t s off 
t he c e n t r a l l u m e n . T h i s a r r a n g e m e n t m a y faci l i ta te t he p a s s a g e of s t i m u l a t i n g 
molecu le s f rom t h e ex te r io r to t h e d e n d r i t e s in t he l u m e n . T h e loca t ion of 
m d 9 a n d 10 b e h i n d H a l l e r ' s o r g a n a n d the i r u l t r a s t r u c t u r a l fea