1982 (Chapter 13) BELOZEROV Fisiology of Ticks Diapause and Biological Rhythms in Ticks

Prévia do material em texto

C H A P T E R 13 
Diapause and Biological Rhythms in Ticks 
V. N. BELOZEROV 
Biological Institute of the Academy of Sciences, Leningrad University, L·ningrad, USSR 
C O N T E N T S 
13.1. Introduction 469 
13.2. Daily (Circadian) Rhythms in Ixodid and Argasid ticks 470 
13.2.1. Daily Rhythms of Behavioural Activity in Unfed Ticks 470 
13.2.2. Daily Rhythms in Feeding Ticks 473 
13.2.3. Properties and Significance of Daily "Drop-ofF' Rhythms of Engorged 
Ticks 
13.2.4. Regulation of Daily Drop-off Rhythms 476 
13.2.5. Daily Rhythms of Egg-laying in Females 481 
13.2.6. Summary 481 
13.3. Seasonal Rhythms and Diapause in Ticks 481 
13.3.1. The Occurrence of Diapause in Ticks 482 
13.3.2. Physiological Properties of Diapause 485 
13.3.3. Photoperiodic Regulation of Development and Diapause in Ticks 487 
13.3.4. Photoperiodic Regulation of Seasonal Adaptations 492 
13.3.5. Summary 495 
13.4. Conclusions 495 
References 496 
1 3 . 1 . I N T R O D U C T I O N 
T i c k s h a v e c h a r a c t e r i s t i c r h y t h m s w h i c h r e g u l a t e different a spec t s of the i r 
d e v e l o p m e n t a n d ac t iv i ty a n d inf luence every level of the i r o r g a n i z a t i o n . 
O n e of t h e m a i n p r o p e r t i e s of t ick o n t o g e n y is t h e r e g u l a r a l t e r n a t i o n from 
free-l iving to p a r a s i t i c s t ages . T h e r e is a r epe t i t i on in e a c h i n s t a r of t h e 
p rog re s s ion f rom p o s t - m o u l t i n g d e v e l o p m e n t to hos t - f ind ing ac t iv i ty , feeding 
a n d finally m e t a m o r p h o s i s or , in t h e female , egg- lay ing (Ba la shov , 1967) . 
E a c h p h a s e serves a ve ry different func t ion . 
M a n y phys io log ica l p rocesses in t icks a r e a lso r h y t h m i c d u e to t h e r h y t h m i c 
func t ion ing of t h e p a r t i c u l a r o r g a n s . S u c h p h y s i o l o g i c a l r h y t h m s a r e usua l ly 
d i s t i n g u i s h e d b y the i r h i g h e r f requenc ies on t h e o r d e r of s econds a n d m i n u t e s . 
T h e bes t s t u d i e d of t hese a r e t h e r h y t h m s of feeding a n d sa l iva t ion (Ba l a shov , 
1967; G r e g s o n , 1967, 1969; A r t h u r , 1970; S w e a t m a n & G r e g s o n , 1970; 
T a t c h e l l et al., 1972; see C h a p t e r s 3 a n d 4 ) . S o m e phys io log ica l r h y t h m s 
469 
470 V. Ν. Belozerov 
m a t c h the r h y t h m s of d e v e l o p m e n t d u e to t he c o u p l i n g of d iverse p rocesses , 
e.g. t he h a r m o n y b e t w e e n cycles of ecdysone p r o d u c t i o n a n d the m o u l t i n g 
a n d g o n o t r o p h i c cycles . 
E c o l o g i c a l r h y t h m s a r e c h a r a c t e r i s t i c of t icks as well as o t h e r t e r res t r i a l 
A r t h r o p o d a . T h e s e a r e mani fes t a t t h e o r g a n i s m i c level a n d c o - o r d i n a t e t he 
a n i m a l ' s ac t iv i t ies a n d d e v e l o p m e n t w i t h b o t h s ea sona l a n d da i ly ( c i r cad ian ) 
c h a n g e s in t h e e n v i r o n m e n t . T h e s e ecological r h y t h m s h a v e a n obv ious 
a d a p t i v e s ignif icance a n d the i r s t u d y will lead to a n u n d e r s t a n d i n g of t ick 
b i o c h r o n o m e t r y , i n c l u d i n g those m e c h a n i s m s w h i c h m a y be t h e bas i s for 
t e m p o r a l r e g u l a t i o n a n d c o - o r d i n a t i o n in all a n i m a l s . T h i s c h a p t e r is con-
c e r n e d w i t h these da i ly a n d seasona l r h y t h m s in t icks a n d w i t h the i r 
r egu l a t i on . 
1 3 . 2 . D A I L Y ( C I R C A D I A N ) R H Y T H M S I N I X O D I D A N D A R G A S I D T I C K S 
Dai ly r h y t h m s a r e mani fes t b o t h a t i n d i v i d u a l levels (act iv i ty r h y t h m s , 
feeding, a n d egg- lay ing r h y t h m s ) a n d a t p o p u l a t i o n levels ("drop-off ' 
r h y t h m s in e n g o r g e d t icks) . T h e s e r h y t h m s c o n t r i b u t e to t he s y n c h r o n i z a t i o n 
of hos t - seek ing ac t iv i ty , a n d s o m e o t h e r v i ta l func t ions , w i t h p a r t i c u l a r p h a s e s 
of da i ly e n v i r o n m e n t a l r h y t h m s . 
13.2.1. Daily Rhythms of Behavioural Activity in Unfed Ticks 
B e h a v i o u r a l r h y t h m s a r e c h a r a c t e r i s t i c of all t icks a l t h o u g h the i r in tens i t ies 
m a y v a r y a m o n g different spec ies . I n m a n y cases these r h y t h m s h a v e a 
c i r c a d i a n pe r iod ic i ty ( T a b l e 13.1) . 
N o c t u r n a l hos t - seek ing ac t iv i ty r h y t h m s o c c u r in a n u m b e r of nes t -dwe l l ing 
a r g a s i d s (Argas persicus, A. reflexus, A. cooleyi) a n d in s o m e ixod ids w h i c h 
i n h a b i t s t ab le s o r a n i m a l h o u s e s (Hyalomma anatolicum). I n p a s t u r e - d w e l l i n g 
ixod ids t h e da i ly ac t iv i ty r h y t h m s a r e less p r o n o u n c e d a n d a r e usua l ly 
d i u r n a l . 
T h e ma jo r i t y of tick inves t iga to r s , fol lowing the ini t ia l d e d u c t i o n s of Lees 
a n d M i l n e (1951) , a s soc ia te t he r h y t h m i c ver t ica l m i g r a t i o n s of t icks o n the 
vege t a t i on w i t h b e h a v i o u r a l m e c h a n i s m s for t he r egu l a t i on of t ick w a t e r 
b a l a n c e ( C h a p t e r 2 ) . I n a c c o r d a n c e w i t h this idea , da i ly r h y t h m s a r e exogen-
ous in n a t u r e a n d r e p r e s e n t a d i r ec t r e sponse to e n v i r o n m e n t a l fac tors , t he 
m a i n ones b e i n g t e m p e r a t u r e (Khe i s s in , 1953; N a m b a , 1954; B a l a s h o v , 1960, 
1967; B a b e n k o & K h i z h i n s k y , 1964; Kie lczewski & C z a p s k a , 1965; W i l s o n 
& K i n z e r 1972) , h u m i d i t y ( L u t t a & S c h u l m a n , 1958) , o r a c o m b i n a t i o n of 
b o t h ( B o u c k o v a & D y k , 1968; N a s s , 1975) . A n ana lys i s of field d a t a o n t h e 
a b u n d a n c e of Dermacentor variabilis l a r v a e a n d a d u l t s s h o w e d t h a t hos t - seek ing 
ac t iv i ty w a s co r r e l a t ed w i t h t h e in tens i ty of so lar r a d i a t i o n , b u t n o t w i th 
t e m p e r a t u r e ( A t w o o d & S o n e n s h i n e , 1967). B a b e n k o (1974) a lso found t h a t 
TABLE 13.1. DAILY RHYTHMS OF ACTIVITY IN UNFED TICKS. 
Position Leading 
Tick species Stage of maximum factor Authors 
Ixodes ricinus A D Lees and Milne (1951) 
A M + E RH Lutta and Shul'man (1958) 
L, N, A Uncertain T + RH Bouckova and Dyk (1968); 
Nass, (1975) 
L Ε Τ Kielczewski and Czapska, 
(1965) 
Ν E +N SR Babenko (1970, 1974) 
I. persulcatus A M + E Τ Kheissin (1953) 
A E +N Τ Mishin (1956) 
A M + E Τ, W Babenko and Khizhinsky 
(1964); Lykov, (1966). 
Ν E +N SR Babenko, (1970, 1974) 
Dermacentor pictus A D or M + E T + RH Loginovsky, (1972) 
D. marginatus A D or M + E T +RH Loginovsky (1972) 
Haemaphysalis longicornis L M + E Τ Namba (1954) 
Hyalomma asiaticum L, A M + E — Bernadskaya (1938) 
A M + E Τ, L Balashov (1960, 1967) 
H. anatolicum L, N, A E +N Τ Serdyukova (1945, 1960) 
H. plumbeum turanicum ? E+N Τ Serdyukova (I960) 
Amblyomma americanum N, A D Τ Wilson and Kinzer (1972) 
A M + E T +RH Semtner and Hair (1973) 
Ar gas persicus L none — Lounsbury (1906); Galuzo 
(1957) 
N, A Ν — Lounsbury (1906); Hooker et 
al., (1912), Galuzo (1957) 
A. reflexus L, N, A Ν — Galuzo (1957) 
A. vespertilionis L, N, A D — Galuzo (1957) 
A. cooleyi A Ν PhP Howell (1976) 
Ornithodoros savignyi N, A D — Lounsbury (1906) 
Abbreviations. Stage: L, larvae; N, nymphs; A, adults. Position of maximum: D. daytime; E, evening; N, night; M, morning. Leading factor: RH, 
relative humidity; T, temperature; SR, solar radiation; PhP, photoperiod; L, light; W, weather. 
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m V. N. Belozerov 
4 8 12 16 20 24 4 
HOUR OF DAY 
FlG. 13.1. Daily rhythms of activity in unfed nymphs of Ixodes ricinus (I) and / . persulcatus (II) 
under natural conditions. Experiments were conducted during May in Moscow district. Curve 
III shows hourly changes in the intensity of solar radiation. (After Babenko, 1974.) 
c i r c a d i a n r h y t h m s in t h e ac t iv i ty of unfed n y m p h s of Ixodes ricinus a n d / . 
persulcatus w e r e d e t e r m i n e d b y da i ly c h a n g e s in so la r r a d i a t i o n (Fig. 13.1) , 
a n d H o w e l l (1976) d i scove red t h a t p h o t o p e r i o d r e g u l a t e d t h e da i ly r h y t h m 
in t h e b e h a v i o u r of A. cooleyi. 
T h i s l a t t e r a r g a s i d tick is a nes t -dwe l l ing p a r a s i t e of cliff swal lows in 
w e s t e r n N o r t h A m e r i c a a n d its n o c t u r n a l r h y t h m of ac t iv i ty is a r eac t i on to 
a l t e r n a t i o n b e t w e e n l igh t a n d d a r k n e s s . By r e c o r d i n g the l o c o m o t o r ac t iv i ty 
of i n d i v i d u a l unfed a d u l t s , H o w e l l (1976) d e m o n s t r a t e d t h a t ac t iv i ty w a s 
s t i m u l a t e d b y t h e c h a n g e from l ight to d a r k n e s s . Act iv i ty b e g a n d u r i n g t h e 
first 2 h of d a r k n e s s , r e a c h e d p e a k in tens i ty 2 - 3 h la te r , a n d ceased before 
t he onse t of t he l ight p e r i o d o r p h o t o p h a s e . T h e l ight r e g i m e used w a s L D 
1 4 : 1 0 , t h a t is, 14 h of l ight a n d 10 h d a r k n e s s p e r d a y . W h e n the p h o t o p e r i o d 
w a s r eve r sed , w i t h t he d a r k pe r iod or s c o t o p h a s e l e n g t h e n e d to 14 h , t he 
l o c o m o t o r r h y t h m of t h e t icks shifted to co inc ide w i t h t he s c o t o p h a s e of t he 
n e w r e g i m e (Fig . 13 .2A) . T h e r h y t h m e n t r a i n e d by p h o t o p e r i o d s w a s lost 
in c o n s t a n t d a r k n e s s w h e r e n o l o c o m o t o r ac t iv i ty o c c u r r e d for a t leas t 4 d a y s 
(Fig . 13 .2B) . F r o m these d a t a it w a s d e d u c e d t h a t t he r h y t h m h a d a n 
e x o g e n o u s bas i s ( H o w e l l , 1976) , b u t t he resu l t s d id n o t exc lude t he poss ibi l i ty 
t h a t e n d o g e n o u s r e g u l a t o r s , o p e r a t i n g as " i n t e r v a l - t i m e r s " , cou ld be 
" s w i t c h e d - o n " by t h e c h a n g e from p h o t o p h a s e to s c o t o p h a s e . T h e poss ib le 
role of s u c h e n d o g e n o u s c i r c a d i a n processes in t h e con t ro l of tick ac t iv i ty 
r h y t h m s w a s p r o p o s e d by B a b e n k o (1974) . I t is i m p o r t a n t to no t e t h a t t he 
ac t iv i ty r h y t h m of A. cooleyi t icks in H o w e l l ' s e x p e r i m e n t s w a s d e t e r m i n e d 
on ly b y p h o t o p e r i o d a n d n o t by w a t e r b a l a n c e , n o r c h a n g e s in t e m p e r a t u r e 
o r C O 2 c o n c e n t r a t i o n . 
Diapause and Biological Rhythms in Ticks 473 
10 
8-
6 -
4 
2 
I 2 3 
DAYS 
FIG. 13.2. Locomotor activity of unfed adult females of Argas cooleyi at 26° and its dependence 
on light rhythms. A, the shift of activity phase after reversion of photoperiodic regime; B, the 
loss of activity after the photoperiod was changed to constant darkness. (After Howell, 1976.) 
U n d o u b t e d l y t h e fu r the r s t u d y of b e h a v i o u r a l r h y t h m s in i n d i v i d u a l unfed 
t icks (as successfully a p p l i e d by H o w e l l ) w o u l d e n h a n c e o u r k n o w l e d g e of 
t h e r e g u l a t i o n of t ick c i r c a d i a n r h y t h m s . 
13.2.2. Dai ly Rhythms in Feeding Ticks 
Elec t rophys io log ica l r e c o r d i n g s of t h e feeding p a t t e r n s of female Boophilus 
microplus ( T a t c h e l l et al., 1972) s h o w e d da i ly r h y t h m s w h i c h w e r e mani fes t 
b y c h a n g e s in t h e d u r a t i o n of p e r i o d s of inges t ion ( suck ing) , sa l iva t ion , a n d 
r e s t ing (see C h a p t e r 4 ) . A t t h e e n d of t h e s low feeding pe r iod ( 5 - 6 t h d a y ) , 
t he s u c k i n g ac t iv i ty of t h e p h a r y n g e a l p u m p ( low-f requency suck ing , 4 / s a t 
th is s tage) is m a x i m a l a t n i g h t b e i n g 3 2 % of t h e w h o l e cycle, dec reases b y 
m o r n i n g , a n d r e a c h e s a m i n i m u m d u r i n g t h e d a y t i m e ( 1 % of t h e w h o l e 
cycle) a n d inc reases a g a i n b y even ing . A s imi l a r r h y t h m is a lso c h a r a c t e r i s t i c 
of t h e final s t age of feeding (7 th d a y ) w h e n t h e g r e a t e r q u a n t i t i e s of b lood 
a r e inges t ed . T h e m i n i m a l r a t e of inges t ion occu r s d u r i n g t h e d a y (only 3 % 
of t h e w h o l e cyc le ) , i nc reases b y s u n s e t ( 1 8 % of t h e cycle) , a n d r e a c h e s a 
m a x i m u m w i t h d a r k n e s s b e i n g 5 9 - 6 6 % of t h e cycle a n d a lso h i g h e r f requency 
474 V. N. Belozerov 
suck ing (4 /s on d a y 7) . T h i s is ev idence for t he s y n c h r o n i z a t i o n of final 
e n g o r g e m e n t w i t h t h e first ha l f of t he s c o t o p h a s e by m e a n s of the " l igh t s off" 
s ignal . 
13.2.3. Properties and Significance of Daily "Drop-off" Rhythms of 
Engorged Ticks 
T h e da i ly "drop-off" r h y t h m s of e n g o r g e d ticks a r e phys io logica l ly a n d 
ecological ly i m p o r t a n t a n d h a v e b e e n the m o s t in tens ive ly s t u d i e d c i r c a d i a n 
r h y t h m s in t icks. T h e o c c u r r e n c e of s u c h r h y t h m s a n d the i r ecological 
s ignif icance w e r e first i nves t iga t ed by the classical t r ea t i se of H o o k e r et al., 
(1912) . T h e i r d a t a s h o w e d t h a t t he drop-off of e n g o r g e d r a b b i t t icks , Hae-
maphysalis le pons palustris, o ccu r s whi le t he r a b b i t s a r e r e s t ing in the i r n e s t i n g 
forms d u r i n g the d a y ; b u t in t he fowl tick A. persicus (= A. miniatus) drop-off 
occu r s d u r i n g t h e n i g h t whi le t he hos t b i r d s a r e roos t ing . As a resu l t of th is 
s y n c h r o n i z a t i o n , e n g o r g e d t icks drop-off w i t h i n the she l t e r ing p laces of the i r 
hos t s , a n d th is inc reases t h e p r o b a b i l i t y t h a t t he following i n s t a r will find 
a su i t ab l e hos t . 
A da i ly drop-of f r h y t h m h a s b e e n found in a n u m b e r of ixodid a n d a rga s id 
species in t he g e n e r a Ixodes, Haemaphysalis, Dermacentor, Amblyomma, Hyalomma, 
Rhipicephalus, Boophilus, Argas, a n d Ornithodoros ( T a b l e 13.2). S u c h drop-off 
r h y t h m s a r e prec ise ly c o - o r d i n a t e d w i t h r h y t h m s of ac t iv i ty a n d o t h e r b io -
logical p rocesses of t he hos t (Ba l a shov , 1967) . T h e t i m i n g of these r h y t h m s 
h a s a d u a l ecological i m p o r t a n c e ; t he e n g o r g e d tick t e n d s to d r o p in a n a r e a 
w h e r e c o n d i t i o n s a r e f avou rab l e for i ts p o s t - e n g o r g e m e n t d e v e l o p m e n t a n d , 
s u b s e q u e n t l y , w h e r e it is likely to e n c o u n t e r a n e w hos t (Ba la shov , 1967; 
Lees , 1969; Be lozerov , 1975) . M a n y ixodid t icks w h i c h a r e p a r a s i t e s of 
" p a s t u r e " a n i m a l s h a v e a d i u r n a l drop-off r h y t h m , w h i c h pa ra l l e l s t he d i u r n a l 
ac t iv i ty r h y t h m s of the i r hos t s . T h i s h a s b e e n found in the t icks / . ricinus, I. 
persulcatus, I. kazakstani, Haemaphysalis longicornis, Amblyomma hebraeum, D. 
variabilis, a n d B. microplus. I n nes t -dwe l l ing ticks t he drop-off r h y t h m m a y 
be e i the r n o ct u r n a l , in t he cases w h e n hos t s a r e ac t ive d u r i n g t h e d a y a n d 
she l t e r in nes t s a t n igh t , o r d i u r n a l , w h e n hos t s she l te r d u r i n g t h e d a y a n d 
a r e ac t ive a t twi l igh t o r d u r i n g t h e n igh t . Argas persicus a n d Ixodes texanus 
h a v e n o c t u r n a l r h y t h m s whi le / . hexagonus, H. leporispalustns, a n d Ornithodoros 
gurneyi h a v e d i u r n a l drop-off r h y t h m s . S o m e species h a v e a different b e h a v i o u r 
in t h e l a rva l c o m p a r e d w i t h t he fol lowing i n s t a r s . F o r i n s t a n c e , l a rva l 
drop-off is d i u r n a l in H. anatolicum a n d Rhipicephalus sanguineus, wh i l e n y m p h s 
a n d females s h o w n o c t u r n a l drop-off r h y t h m s . O f cour se , t he differences 
b e t w e e n the b e h a v i o u r of different i n s t a r s h a s ecological s ignif icance, reflect-
ing different h a b i t a t r e q u i r e m e n t s d u r i n g p o s t - e n g o r g e m e n t d e v e l o p m e n t 
a n d / o r t he c h a n g i n g hos t p references of s u b s e q u e n t i n s t a r s in t h e t icks 
life-cycle. 
TABLE 13.2. DAILY RHYTHMS OF DETACHMENT OF ENGORGED TICKS. 
Tick species Stage 
Type of 
rhythm Authors 
Ixodes nanus A D Pomerantzev and Alfeev (1935); 
Kheissin and Lavrenenko (1956) 
L D Belozerov and Krutchinina (1979) 
I. persulcatus A D Balashov (1954) 
I. kazakstani L D Babenko and Gal'chenko (1976) 
I. hexagonus L, N, A D Arthur (1962) 
I. texanus L, Ν Ν Darling (1969) 
Haemaphysalis leponspalustns L, N, A D Hooker, et al., (1912); Camin 
(1963); George (1964) 
H. longicornis A D Kitaoka (1962) 
Dermacentor variabilis L, Ν D Amin (1970) 
Hyalomma anatolicum L, N, A Ν Serdyukova (1945, 1960) Hyalomma anatolicum 
L D Hadani and Rechav (1969, 1970); 
Hadani and Ziv, (1974); 
Belozerov and Krutchinina (1979) 
N, A Ν Hadani and Rechav (1969, 1970); 
Hadani and Ziv (1974) 
H. detritum Ν D Galuzo and L'vova (1945) 
Amblyomma hebraeum L, Ν D Rechav (1978) 
Rhipicephalus sanguineus L D Hadani and Rechav (1969) 
R. sanguineus—continued N,A Ν Hadani and Rechav (1969) 
Boophilus microplus A D Hitchcock (1955); Wharton and 
Utech (1969, 1970) 
Argas persicus L Ν Hooker et al. (1912); Hadani and Argas persicus 
Rechav (1969) 
Ornithodoros gurneyi L, Ν D Doube (1975a, b) 
Abbreviations. Stage: A, adults; L, larvae; N, nymph s. Type of rhythm: D, diurnal; N, nocturnal. 
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13.2.4. Regulat ion of Daily Drop-off Rhythms 
Dai ly r h y t h m s in insec ts h a v e e x o g e n o u s a n d e n d o g e n o u s c o m p o n e n t s . 
T h e r e l a t i o n s h i p b e t w e e n the t w o m a y differ, b u t they a lways i n t e r a c t 
(Dan i l evsky et al., 1970; S a u n d e r s , 1976; T y s h c h e n k o , 1977). T i c k biologis ts 
first s t u d i e d t h e e x o g e n o u s c o m p o n e n t in t he r egu l a t i on of da i ly drop-off 
r h y t h m s . A c c o r d i n g to B a l a s h o v (1967) t he d e t a c h m e n t of e n g o r g e d t icks 
occu r s as a r e s p o n s e to c h a n g e s e i the r in t he e n v i r o n m e n t o r t h e hos t ' s 
phys io logy . F ie ld o b s e r v a t i o n s on the ca t t l e t icks / . ricinus a n d / . persulcatus 
conv inc ing ly d e m o n s t r a t e t h e d e p e n d e n c e of tick d e t a c h m e n t r h y t h m s o n 
hos t ac t iv i ty r h y t h m s (e.g. g r a z i n g ) . T h e inc rease in hos t l o c o m o t o r ac t iv i ty 
a p p e a r e d to b e a n i m p o r t a n t s t i m u l u s for tick d e t a c h m e n t (Ba la shov , 1954; 
K h e i s s i n & L a v r e n e n k o , 1956). A m i n (1970) fu r the r s p e c u l a t e d t h a t t he 
m e c h a n i s m r e g u l a t i n g t he r h y t h m of tick d e t a c h m e n t involved the r e s p o n s e 
of feeding t icks to c i r c a d i a n c h a n g e s in the co r t i cos t e rone levels of hos t b lood . 
W o r k i n g w i t h o t h e r tick species in e x p e r i m e n t s u n d e r con t ro l l ed l a b o r a t o r y 
cond i t i ons it h a s b e e n s h o w n t h a t p h o t o p e r i o d , i.e. da i ly c h a n g e s in t he 
l eng th of l ight a n d d a r k p h a s e s , r egu la t e s drop-off r h y t h m s (George , 1964, 
1971; H a d a n i & R e c h a v , 1969, 1970; H a d a n i & Ziv , 1974; D o u b e , 1975a, 
b ; R e c h a v , 1978; Be lozerov & K r u t c h i n i n a , 1979). I n t he cou r se of these 
inves t iga t ions t h e i dea w a s first expressed t h a t d e t a c h m e n t is con t ro l l ed by 
e n d o g e n o u s c i r c a d i a n m e c h a n i s m s of r egu l a t i on w h i c h a r e e n t r a i n e d by 
e x o g e n o u s s igna ls ( G e o r g e , 1964; H a d a n i & R e c h a v , 1969). T h i s h y p o t h e s i s 
h a s b e e n e x p e r i m e n t a l l y tes ted (George , 1971; D o u b e , 1975 a, b ; R e c h a v , 
1978; Be lozerov & K r u t c h i n i n a , 1979) a n d the exogenous s ignals h a v e b e e n 
s h o w n to b e p h o t o p e r i o d i c . T h r o u g h these m e c h a n i s m s , t he d e t a c h m e n t of 
i n d i v i d u a l s is s y n c h r o n i z e d a n d the p o p u l a t i o n shows a s t r o n g c i r c a d i a n 
r h y t h m of d e t a c h m e n t . T a b l e 13.3 i l lus t ra tes t he cha rac t e r i s t i c s of tick 
drop-off r h y t h m s k n o w n to be con t ro l l ed by p h o t o p e r i o d a n d figures 13.3 
a n d 13.4 give ev idence for t he p h o t o p e r i o d i c e n t r a i n m e n t of t w o s u c h 
r h y t h m s . I n th is r e spec t t icks a r e s imi l a r to o t h e r t e r res t r i a l a r t h r o p o d species , 
especia l ly insec ts , a m o n g w h i c h p h o t o p e r i o d i c s ignals a r e t he m o s t i m p o r t a n t 
factors for t he s y n c h r o n i z a t i o n of c i r c a d i a n r h y t h m s . 
T h e c o m p l e x i t y of t he m e c h a n i s m s involved in t he p h o t o p e r i o d i c e n t r a i n -
m e n t of "drop-off" r h y t h m s h a s b e e n s h o w n in de ta i l ed s tud ies o n t h r e e tick 
species , Haemaphysalis leporis palustris (Geo rge , 1964, 1971), 0. gurneyi ( D o u b e , 
1975a) , a n d Amblyomma hebraeum ( R e c h a v , 1978). Reve r sa l of t he p h o t o p e r -
iodic r e g i m e lead to a c o r r e s p o n d i n g shift in t he da i ly p e a k of d e t a c h m e n t 
in all t h r ee t icks. T h i s is i l l u s t r a t ed for 0. gurneyi l a r v a e in F ig . 13.3. T h e 
ex i s tence of a n e n d o g e n o u s c o m p o n e n t in the m e c h a n i s m s of c i r c a d i a n 
r egu l a t i on is m o s t conv inc ing ly d e m o n s t r a t e d by c h a n g i n g the e n t r a i n i n g 
p h o t o p e r i o d i c cycle to a n a p e r i o d i c r eg ime ( c o n s t a n t l ight o r d a r k n e s s ) . 
TABLE 13.3. THE CHARACTERISTICS OF PHOTOPERIODIC REGULATION OF DAILY RHYTHMS OF DETACHMENT IN 
IXODIDS AND ARG AS IDS 
Maintenance 
of rhythms 
Position 
Tick Species Stage of maximum (at LL) (at DD) Authors 
Ixodes ricinus L Ph3 + Belozerov and 
Krutchinina (1979) 
I. kazakstani L Ph3 Babenko and 
Gal'chenko (1976) 
Haemaphysalis leporispalustris L, N, A Ph2-3 + + George (1964, 1971) 
Dermacentor variabilis L, Ν Ph3 — + Amin (1970) 
Amblyomma hebraeum L, Ν Ph3-Sc, + + Rechav (1978) 
Hyalomma anatolicum L Ph2- 3 + + Hadani and Rechav Hyalomma anatolicum 
(1969, 1970) 
L Ph, + Belozerov and 
Krutchinina (1979) 
Ν Sc3 + + Hadani and Rechav 
(1969, 1970) 
A Sei Hadani and Rechav 
(1969, 1970) 
Rhipicephalus sanguineus L Ph3 Hadani and Rechav 
(1969) 
Ν Sc3 Hadani and Rechav 
(1969) 
A Sc2 Hadani and Rechav 
(1969) 
Argas persicus L Sc2 Hadani and Rechav Argaspersicus 
(1969) 
Ornithodoros gurneyi L, Ν Ph2 + Doube (1975a, b) 
Abbreviations. Stage: L, larvae; N, nymphs; A, adults. Position of maximum: Phi, Ph2, Ph3, the beginning, the middle, and the end of photophase; 
Scj, Sc2, Sc3, the same parts of scotophase, respectively. 
D
iapau
se an
d B
iological 
R
h
yth
m
s in
 T
icks 
477 
478 V. N. Belozerov 
R E V E R S E D L IGHT R E G I M E 
I 
σ 10 
I I I I I I I I • I • 11 • 11 
JL 
< 30 
u. 
Ο 
NORMAL LIGHT REGIME 
I 
» H h • 
3 4 
DAY'S 
Iiftiliftil ^
11
 ^
11
 ^ 
FlG. 13.3. The rhythm of detachment in engorged larvae of Ornithodoros gurneyi at reversed 
photoperiods (LD 16:8 and DL 8:16) which are shifted for 12 h about their phases. (After 
Doube, 1975a.) 
FlG. 13.4. The maintenance of the detachment rhythm in engorged larvae of Haemaphysalis 
leponspalustris in constant darkness (after entrainment by five photoperiodic cycles of LD 12:12) 
at 26.5° (After George, 1971.) 
Diapause and Biological Rhythms in Ticks 479 
U n d e r these c o n d i t i o n s t h e c i r c a d i a n r h y t h m of d e t a c h m e n t is still m a i n t a i n e d 
(Fig . 13.4) . Espec ia l ly i m p o r t a n t w e r e e x p e r i m e n t s w h e r e t he feeding of t icks 
took p l a c e u n d e r a p e r i o d i c c o n d i t i o n s w h e n the t icks a n d the i r hos t s h a d 
b e e n p r e c o n d i t i o n e d s e p a r a t e l y so t h a t the i r r h y t h m s w e r e e i the r in o r o u t 
of s y n c h r o n y . T h e resu l t s s h o w e d t h a t a c o m p o n e n t of t he r e g u l a t o r y m e c h -
a n i s m is a c i r c a d i a n r h y t h m w i t h i n t h e t icks t hemse lves . I n o t h e r w o r d s , 
t icks h a v e t he i r o w n e n d o g e n o u s " c l o c k s " w h i c h a r e involved in t he r e g u l a t i o n 
of d e t a c h m e n t r h y t h m s a n d in o t h e r p rocesses . 
T h e s e e x p e r i m e n t s a l so s h o w e d t h a t t he w o r k i n g of t h e e n d o g e n o u s "c lock" 
c a n b e affected b y da i ly phys io log ica l r h y t h m s of t he hos t w h i c h c a n affect 
t h e p rec i s ion of t h e d e t a c h m e n t r h y t h m (George , 1971; D o u b e , 1975a; 
R e c h a v , 1978) a n d , in s o m e cases , shift t he da i ly p e a k of d e t a c h m e n t (Beloz-
e rov & K r u t c h i n i n a , 1979) . T h u s t h e i n t e r a c t i o n of e x o g e n o u s a n d e n d o g e n -
ous c o m p o n e n t s w i t h i n t h e r e g u l a t i o n m e c h a n i s m s m a y c o n t r i b u t e to a 
c e r t a in labi l i ty of t h e d e t a c h m e n t r h y t h m s . T h i s c a n exp la in s o m e of t he 
p h a s e shifts in d e t a c h m e n t r h y t h m s ( H a d a n i & R e c h a v , 1970; H a d a n i & 
Ziv , 1974) , a n d s o m e of t h e a p p a r e n t c o n t r a d i c t i o n s in t he p u b l i s h e d d a t a 
c o n c e r n i n g t h e pos i t ion of t h e da i ly p e a k of d e t a c h m e n t in s o m e t icks , e.g. 
l a r v a e of Hyalomma anatolicum ( S e r d y u k o v a , 1945, 1960; H a d a n i & R e c h a v , 
1969, 1970; Be loze rov & K r u t c h i n i n a , 1979) . U n d o u b t e d l y , t he d e p e n d e n c e 
of p a r a s i t i c r h y t h m s on hos t r h y t h m s is of a d a p t i v e i m p o r t a n c e to t he 
h o s t - p a r a s i t e r e l a t i o n s h i p . 
T h e cr i t ica l t imes o r w i n d o w s d u r i n g w h i c h t h e p h o t o p e r i o d i c e n t r a i n m e n t 
of t h e e n d o g e n o u s c o m p o n e n t r e g u l a t i n g d e t a c h m e n t c a n t ake p l ace n e e d to 
b e clarif ied. S o m e a u t h o r s found t h a t e n t r a i n m e n t w a s poss ib le on ly after 
the i r tick species b e g a n to feed ( G e o r g e , 1971; H a d a n i & Ziv , 1974) , b u t 
o t h e r s found t h a t e n t r a i n m e n t cou ld o c c u r b o t h before a n d d u r i n g feeding 
( D o u b e , 1975a; R e c h a v , 1978; Be lozerov & K r u t c h i n i n a , 1979) . D o u b e 
(1975a) a l so found t h a t r e - e n t r a i n m e n t cou ld o c c u r w i t h i n 2 d a y s . I t is 
poss ib le t h a t t ick species differ in t h e t i m i n g of the i r "sens i t ive s t a g e ( s ) " 
w h e n t h e pos i t ion of t h e da i ly p e a k of d e t a c h m e n t is d e t e r m i n e d . T h e y m a y 
a lso differ in t h e " t o k e n " m e a n i n g of t h e s igna ls de r ived from v a r i o u s 
c o m p o n e n t s of t h e p h o t o p e r i o d . T h u s , in s o m e tick species e n t r a i n m e n t 
resu l t s f rom a s igna l a s soc i a t ed w i t h t h e t r a n s i t i o n from l ight to d a r k (George , 
1971) , wh i l e in o t h e r s it is t h e t r a n s i t i o n f rom d a r k to l ight ( R e c h a v , 1978) 
w h i c h a p p e a r s to be s ignif icant . 
I t is still n o t k n o w n w h e t h e r it is on ly t h e p rocess of d e t a c h m e n t w h i c h 
is r e g u l a t e d by p h o t o p e r i o d o r if t h e b e g i n n i n g of t h e final p h a s e of engo rge -
m e n t is a l so u n d e r p h o t o p e r i o d i c con t ro l ( K i t a o k a , 1962; B a l a s h o v , 1967). 
E l ec t rophys io log ica l r e c o r d i n g s t a k e n f rom female B. microplus d u r i n g t he 
s lower p h a s e s of e n g o r g e m e n t s h o w e d a da i ly r h y t h m in t he in t ens i ty of 
feeding w i t h m i n i m a l s u c k i n g r a t e s ( re la t ive) o c c u r r i n g d u r i n g the d a y a n d 
m a x i m a l r a t e s o c c u r r i n g in t h e e v e n i n g a n d t h r o u g h o u t t he n i g h t ( T a t c h e l l 
480 V. N. Belozerov 
et al., 1972) . I n t h e final s t age of e n g o r g e m e n t , r a p i d feeding (a t a b s o l u t e 
m a x i m a l r a t e s ) b e g a n w i t h t h e onse t of d a r k n e s s , b u t , in s o m e ind iv idua l s , 
e n g o r g e m e n t w a s a l r e a d y c o m p l e t e by t h e m i d d l e of t he n igh t . A t this t i m e 
t h e t icks s t o p p e d feeding b u t d e t a c h m e n t d id n o t occu r un t i l m o r n i n g . 
A c c o r d i n g to these d a t a , t h e r h y t h m of e n g o r g e m e n t a n d t h e onse t of final 
p h a s e of e n g o r g e m e n t a n d d e t a c h m e n t m a y be e n t r a i n e d by different p h o t o -
pe r i od i c s t imul i , t h e s igna l e n t r a i n i n g e n g o r g e m e n t r h y t h m s a p p e a r s to b e 
" l igh t s off" wh i l e d e t a c h m e n t is e n t r a i n e d by " l igh t o n " . A l t e rna t ive ly , o n e 
of these s t imul i m i g h t e n t r a i n b o t h sets of r h y t h m s t h r o u g h the i n t e g r a t i n g 
m e c h a n i s m s of t h e e n d o g e n o u s clock. I t s hou ld be poss ib le to des ign exper i -
m e n t s to tes t these a l t e r n a t i v e h y p o t h e s e s . 
I n s u m m a r y , t h e da i ly r h y t h m s of e n g o r g e d t icks h a v e a n e n d o g e n o u s 
c i r c a d i a n bas i s w h i c h is m a i n l y e n t r a i n e d b y p h o t o p e r i o d i c s igna ls . O t h e r 
e x o g e n o u s s igna l s , a s soc ia t ed w i t h da i ly r h y t h m s in t he phys io logy of t he 
hos t , a l so a p p e a r to b e invo lved b o t h in t h e e n t r a i n m e n t of d e t a c h m e n t 
r h y t h m s a n d in the i r modi f i ca t ion . T h e i n t e r ac t i ons b e t w e e n e n d o g e n o u s 
a n d e x o g e n o u s c o m p o n e n t s inc reases t h e a d a p t i v e va lve of t h e d e t a c h m e n t 
24 12 24 12 24 12 24 12 24 12 
H O U R O F D A Y 
FlG. 13.5. The rhythm of egg-laying in adult females of Haemaphysalis longicornis at different 
photoperiods (LD 12:12), LD 6:18, and DL 12:12) at 25°. The latter photoperiod is a reversal 
of the former. (After Fujisaki et al., 1973.)Diapause and Biological Rhythms in Ticks 481 
r h y t h m b y i n c r e a s i n g t h e p r o b a b i l i t y t h a t t h e e n g o r g e d t icks will d r o p in a n 
e n v i r o n m e n t s u i t a b l e for p o s t - e n g o r g e m e n t d e v e l o p m e n t a n d w h e r e t h e s u b -
s e q u e n t i n s t a r will b e m o r e likely to find a n e w - h o s t . 
13.2.5. Dai ly Rhythms of Egg-laying in Females 
T h e poss ib le effects of p h o t o p e r i o d on ov ipos i t iona l r h y t h m s w e r e inves-
t iga ted b y S n o w a n d A r t h u r (1966) in H. anatolicum a n d by W r i g h t (1969c, 
1971b) in Dermacentor (^Anocentor) nitens a n d Amblyomma maculatum. S u b s e -
q u e n t l y , Fu j i sak i et al. (1973) e s t ab l i shed t h a t t h e da i ly cycle of egg- lay ing 
in b o t h H. longicornis a n d / . persulcatus w a s r e g u l a t e d b y p h o t o p e r i o d i c s t imu l i 
a n d exp re s sed as a p a r t i c u l a r l y s t r o n g r h y t h m w i t h a da i ly p e a k of ov ipos i t ion 
d u r i n g t h e s c o t o p h a s e . T h e r h y t h m is m a i n t a i n e d u n d e r v a r i o u s long a n d 
s h o r t d a y p h o t o p e r i o d s (in L D 1 9 : 6 , 1 2 : 1 2 , a n d 6 : 1 8 ) , a n d w h e n t h e 
p h o t o p e r i o d is r eve r sed ( D L 12 :12 ) a c o r r e s p o n d i n g shift o c c u r s to r e syn-
c h r o n i z e t h e p e a k of egg l ay ing w i t h t h e s c o t o p h a s e (Fig . 13.5) . N o ov ipos i t ion 
r h y t h m w a s o b s e r v e d u n d e r a p e r i o d i c l ight o r d a r k r eg imes , a n d th is e s t a b -
l i shed t h e p r e s e n c e of a n e x o g e n o u s r e g u l a t i n g m e c h a n i s m . Fuj isaki et al. 
(1973) a l so be l ieve t h a t l ight h a s a n a d d i t i o n a l , m o r e d i rec t , i n h i b i t o ry effect 
on egg l ay ing . 
13.2.6. Summary 
I t h a s n o w b e e n e s t ab l i shed t h a t c h a r a c t e r i s t i c t ick b e h a v i o u r p a t t e r n s 
s u c h a s h o s t seek ing , e n g o r g e m e n t , d e t a c h m e n t , a n d egg l ay ing h a v e r h y t h m i c 
cycles w h o s e pe r iod ic i t i e s a r e d e t e r m i n e d n o t on ly b y the d i r ec t effects of 
r h y t h m i c e n v i r o n m e n t a l s t imu l i , b u t a l so b y e n d o g e n o u s r e g u l a t i n g m e c h -
a n i s m s w h i c h h a v e a c i r c a d i a n pe r iod ic i ty . P h o t o p e r i o d i c s t imu l i a r e of 
p r i m a r y i m p o r t a n c e in t h e s y n c h r o n i z a t i o n of these e n d o g e n o u s c i r c a d i a n 
r e g u l a t i n g m e c h a n i s m s w i t h p a r t i c u l a r p h a s e s of o t h e r e n v i r o n m e n t a l 
r h y t h m s . I n th is r e spec t , t icks r e s e m b l e o t h e r t e r res t r i a l a r t h r o p o d s a n d in 
p a r t i c u l a r t h e insec t s (Dan i l evsky et al., 1970; S a u n d e r s , 1976; T y s h c h e n k o , 
1977) . B u t t hese p h o t o p e r i o d i c a l l y e n t r a i n e d r h y t h m s m a y h a v e a g r e a t e r 
a d a p t i v e s igni f icance for t icks t h a n is u s u a l for insec ts (a t leas t for n o n -
p a r a s i t i c spec ies ) , i l l u s t r a t i ng t h e s t a t e m e n t of T y s h c h e n k o (1977) t h a t da i ly 
r h y t h m s a r e especia l ly i m p o r t a n t for t he s y n c h r o n i z a t i o n of in te r - a n d 
in t ra-speci f ic r e l a t i o n s h i p s w h i c h m a i n t a i n t h e l inks in a food c h a i n . 
1 3 . 3 . S E A S O N A L R H Y T H M S A N D D I A P A U S E I N T I C K S 
T i c k s a r e a lso wel l k n o w n for t h e s e a s o n a l per iod ic i t i es of the i r act ivi t ies 
b y w h i c h the i r life-cycles a r e a d a p t e d to c l ima t i c c h a n g e s (Belozerov, 1976a, 
b ) . S e a s o n a l r h y t h m s a r e a l w a y s man i fe s t a t t h e p o p u l a t i o n level a n d a r e 
POT - Q 
482 V. N. Belozerov 
b a s e d on a n a l t e r n a t i o n b e t w e e n p e r i o d s of p e a k ac t iv i ty (host seeking, 
e n g o r g e m e n t , a n d p o s t - e n g o r g e m e n t d e v e l o p m e n t ) a n d pe r iods of d o r m a n c y 
(qu iescence , d i a p a u s e , etc) in s y n c h r o n y w i t h t he a p p r o p r i a t e seasons of 
t he y e a r (Dan i l evsky , 1961; Dav i l evsky et al., 1970). 
T i c k d i a p a u s e , like insec t d i a p a u s e , is a spec ia l ca t ego ry of d o r m a n c y 
( "p rospec t ive d o r m a n c y " in t he t e r m i n o l o g y of U s c h a t i n s k a y a , 1973, 1976) 
w h i c h is m o s t i m p o r t a n t in t h e s ea sona l r egu l a t i on of life-cycles. T h e a d v a n -
t age of d i a p a u s e is t h a t it occu r s as a p r e - a d a p t i v e b e h a v i o u r w h i c h p r ecedes 
t he a c t u a l onse t of u n f a v o u r a b l e e n v i r o n m e n t a l cond i t i ons . T h i s ensu re s tick 
su rv iva l . M o r e o v e r , d i a p a u s e is r e g u l a t e d by i n h e r e n t m e c h a n i s m s a n d is 
no t a d i r ec t r e s p o n s e to u n f a v o u r a b l e cond i t i ons . I n t e m p e r a t e c l ima tes t he 
efficiency of d i a p a u s e lies in its close c o n n e c t i o n w i t h d a y l eng th , s ince 
p h o t o p e r i o d i c s igna ls ( tokens) a c c u r a t e l y foretell s ea sona l c l ima t i c c h a n g e s 
(Lees , 1955; Dan i l evsky , 1961; M ü l l e r , 1965; Beck, 1968; S a u n d e r s , 1976; 
T y s h c h e n k o , 1977) . T h e fol lowing d i scuss ion fu r the r d e m o n s t r a t e s t he 
i m p o r t a n c e of d i a p a u s e a n d p h o t o p e r i o d i s m in t he r egu l a t i on of the seasona l 
r h y t h m s of t icks. 
13.3.1. T h e Occurrence o f Diapause in Ticks 
T i c k s h a v e severa l forms of d i a p a u s e w h i c h s y n c h r o n i z e different s tages 
of the i r d e v e l o p m e n t w i t h s ea sona l c h a n g e s in c l ima te . I n t he first de t a i l ed 
c o n s i d e r a t i o n , Alfeev (1948 , 1954) d i s t i n g u i s h e d four types of tick d i a p a u s e : 
(1) inac t iv i ty of unfed t icks , (2) de l ay in e n g o r g e m e n t , (3) de l ay in m e t a -
m o r p h o s i s of e n g o r g e d l a r v a e a n d n y m p h s , a n d (4) de l ay of oogenes is in 
e n g o r g e d females . A d e l a y in t h e onse t of e m b r y o g e n e s i s in tick eggs w a s 
desc r ibed l a t e r b y S e r d y u k o v a (1951) a n d is a fifth t ype of d i a p a u s e . T h e s e 
types of tick d i a p a u s e h a v e b e e n d e s c r i b e d for a n u m b e r of tick species from 
different c l ima t i c zones , b u t t hey a r e bes t d o c u m e n t e d in t icks from t e m p e r a t e 
reg ions (Belozerov , 1976a) . F r o m a phys io log ica l v i ewpo in t , it h a s b e e n 
s h o w n t h a t n e a r l y all t ypes of d i a p a u s e c a n be classified i n to two bas ic 
f o r m s — b e h a v i o u r a l a n d m o r p h o g e n e t i c . T h e first is cha rac t e r i s t i c of unfed 
t icks a n d the s econd of e n g o r g e d t icks (Belozerov, 1965, 1968, 1973a, b , c ) . 
B e h a v i o u r a l d i a p a u s e is, cha rac t e r i s t i ca l ly , t he s u p p r e s s i o n of hos t -seek-
ing ac t iv i ty in unfed t icks . T h e r e is a b lock in t he specific l inks w i th in the 
c h a i n of r e ac t i ons w h i c h l ead to hos t - seek ing b e h a v i o u r (see C h a p t e r 3) . 
D i s t inc t ive p e a k s of s easona l ac t iv i ty , r e su l t i ng in s easona l p e a k s of tick 
a b u n d a n c e , a r e of p r i m a r y i m p o r t a n c e to s tud ies in m e d i c a l a n d v e t e r i n a r y 
ep idemio logy a n d , therefore , i nves t iga t ions in to t h e m e c h a n i s m s r e g u l a t i n g 
b e h a v i o u r a l d i a p a u s e a r e a l so i m p o rt a n t . T h i s t ype of d i a p a u s e is found in 
v a r i o u s p o s t - e m b r y o n i c s t ages in a w i d e r a n g e of ixodid tick species as s h o w n 
in T a b l e 13.4. T h e w i d e s p r e a d o c c u r r e n c e of b e h a v i o u r a l d i a p a u s e is 
u n d o u b t e d l y c o n n e c t e d w i t h the i r c a p a c i t y for p r o l o n g e d s t a r v a t i o n . 
Diapause and Biological Rhythms in Ticks 483 
TABLE 13.4. D I S T R I B U T I O N OF B E H A V I O U R A L DIAPAUSE IN SOME 
I X O D I D TICKS 
Tick species Diapausing stage(s) Distribution/habitat/host 
Ixodes sp.: 
/. crenulatus L, N, A Palaearctic 
I. hexagonus L, N, A Palaearctic 
I. persulcatus L, N, A Palaearctic 
I. nanus L, N, A Palaearctic 
I. trianguliceps L, N, A Palaearctic 
I. unae (=/. putus) L, N, A Palaearctic 
I. laguri N, A Palaearctic/steppes 
I. redikorzevi N, A Palaearctic/steppes 
I. ceylonensis A Oriental 
I. lividus L Nests 
Haemaphysalis sp: 
H. concinna L, N, A Palaearctic 
H. inermis L, N, A Palaearctic 
H. japonica L, N, A Palaearctic 
H. longicornis* L, N, A Palaearctic-NE USSR 
H. punctata L, N, A Palaearctic 
H. sulcata N, A Palaearctic/steppes 
H. longicornis* (= H. bispinosa) 
H. longicornis* 
A Oriental H. longicornis* (= H. bispinosa) 
H. longicornis* Ν Australia-N. Zealand 
Amblyomma sp: 
A. americanum Ν, A Nearctic 
A. maculatum Ν Nearctic 
Hyalomma sp: 
H. anatolicum A Palaearctic 
H. dromedarii A Palaearctic 
H. marginatum 
(=//. plumbeum) A Palaearctic 
H. scupense L Palaearctic/1 host tick 
Rhipicephalus sp: 
R. turanicus A Palaearctic 
R. schulzei L Nests 
Dermacentor sp: 
D. andersoni L, N, A Nearctic 
D. variabilis L, A Nearctic 
D. marginatus A Palaearctic 
D. nuttalli A Palaearctic 
D. pictus A Palaearctic/winter tick 
D. silvarum A Palaearctic 
D. albipictus L Nearctic/1 host winter tick 
* Species such as Haemaphysalis longicornis (recognized as H. bispinosa by various authors as 
detailed in the Appendix) may exhibit behavioural diapause in different life stages in different 
portions of their geographical range. 
Abbreviations: L, larvae; N, nymphs; A, adults. 
TABLE 13.5. D ISTRIBUTION OF VARIOUS FORMS OF MORPHOGENETIC DIAPAUSE IN SOME PALAEARCTIC 
IXODID TICKS. 
Species Stage* Species Stage Species Stage 
Ixodes sp.: Haemaphysalis sp.: Hyalomma sp.: 
/. hexagonus L, N, A-OvDl H. inermis L, N, A-OvDl H. dromedarii L, N, A-OvDl 
I. ricinus L, N, A-OvDl H. concinna L, Ν H. anatolicum N, A-OvDl 
I. apromophorus L, Ν H. japonica L, Ν H. asiaticum N, A-OvDl 
I. kazakstaini L, Ν H. solcata Ν H. detritum Ν 
I. pavlovski L, Ν H. pospelovashtromae A-OvDl H. plumbeum Ν 
I. persulcatus L, Ν H. punctata A-OvDl 
I. laguri Ν Dermacentor sp.: 
I. redikorzevi Ν D. marginatus A-OvDl 
I. crenulatus A-OvDl D. pictus A-OvDl 
I. uriae A-OvDl 
* Stages of engorged ticks undergoing morphogenetic diapause: L, larva; N, nymph; A-OvDl , delay of oviposition in engorged females. 
484 
V
. Ν
. 
B
elozerov 
Diapause and Biological Rhythms in Ticks 485 
M o r p h o g e n e t i c d i a p a u s e r e su l t s f rom a b lock of s o m e essent ia l s t ep in 
d e v e l o p m e n t . T h e r e m a y b e a d e l a y d u r i n g e m b r y o g e n e s i s , o r in t he m e t a -
m o r p h o s i s of l a r v a e a n d n y m p h s , o r in t h e oogenes i s of e n g o r g e d females . 
M o r p h o g e n e t i c d i a p a u s e m a k e s it poss ib le for t h e a p p e a r a n c e of l a t e r s t ages 
in t he life-cycle to b e s y n c h r o n i z e d w i t h t h e a p p r o p r i a t e season . 
D i a p a u s e of th is t y p e w a s first n o t e d in a u t u m n - f e d l a r v a e of / . ricinus 
( B e y n a r o v i t c h , 1907) a n d h a s b e e n found in l a r v a e a n d n y m p h s of a n u m b e r 
of p a l a e a r c t i c spec ies of ixod id t icks ( T a b l e 13.5) . I t is s u r p r i s i n g t h a t 
m o r p h o g e n e t i c d i a p a u s e h a s b e e n found on ly a m o n g p a l a e a r c t i c ixod ids , 
whi le ixod ids in o t h e r Zoogeographie r eg ions exh ib i t b e h a v i o u r a l d i a p a u s e . 
M o r p h o g e n e t i c d i a p a u s e , p a r t i c u l a r l y exp re s sed as a de l ay in ov ipos i t ion , 
c a n b e d e d u c e d for c e r t a i n Afr ican t icks , i n c l u d i n g Amblyomma nuttalli a n d 
A. sparsum. T h i s r eg iona l d iv i s ion of d i a p a u s e types does n o t a p p l y to a r g a s i d s , 
w h e r e r e p r o d u c t i v e d i a p a u s e is k n o w n in p a l a e a r c t i c species {Argas arboreus, 
Ornithodoras lahorensis), in n e a r c t i c species (0. coriaceus, 0. hermsi), a n d in t h e 
A u s t r a l a s i a n t ick 0. gurneyi. 
M o r p h o g e n e t i c d i a p a u s e of e m b r y o n a t i n g eggs is c o m p a r a t i v e l y r a r e b u t 
o c c u r s in / . ricinus, I. crenulatus, I. hexagonus, I. uriae, a n d H. pospelovashtromae. 
I t is p r o b a b l y a l so found in s o m e Amblyomma f rom Africa (A. hebraeum, A. 
variegatum) a n d f rom A m e r i c a (A. cajennense, A. tuberculatum). 
Fina l ly , a n u n u s u a l fo rm of d i a p a u s e , exp re s sed as a de l ay in e n g o r g e m e n t 
of a t t a c h e d t icks , o c c u r s in s o m e p a l a e a r c t i c species of Dermacentor ( adu l t s 
o f D . silvarum a n d D. marginatus) a n d Hyalomma ( n y m p h s o f / / , detritum a n d 
H. scupense) al l of w h i c h p a r a s i t i z e t h e h o s t in w in t e r . 
I n s u m m a r y , t h e m a n y different fo rms of t ick d i a p a u s e h a v e a c o m m o n 
a d a p t i v e s ignif icance; t h a t is , t h e y s y n c h r o n i z e tick d e v e l o p m e n t a n d ac t iv i ty 
w i t h t he s ea son . All t ypes of t ick d i a p a u s e o p e r a t e b y t e m p o r a r i l y b lock ing 
s o m e v i ta l e v e n t in t h e life-cycle s u c h a s t h e f inding of a hos t , feeding, o r 
m o r p h o g e n e s i s . S o m e tick species h a v e a s ingle d i a p a u s i n g s t age , e.g. t h e 
a d u l t s of p a l a e a r c t i c Dermacentor, t h e n y m p h s of Haemaphysalis longicornis in 
A u s t r a l i a , a n d t h e l a r v a e of / . lividus a n d R. schulzei. I n th is r e spec t they a r e 
s imi l a r to insec t s , b u t t h e m a j o r i t y of d i a p a u s i n g t icks (mos t species of Ixodes, 
Haemaphysalis, Hyalomma, a n d s o m e A m e r i c a n species of Dermacentor) possess 
v a r i o u s c o m b i n a t i o n s of t h e different forms of d i a p a u s e w h i c h m u t u a l l y 
s u p p l e m e n t t h e s e a s o n a l r e g u l a t i o n of d i a p a u s e . T h i s c o m b i n a t i o n of different 
forms of d i a p a u s e is n e c e s s a r y w h e r e t h e life-cycle is p r o l o n g e d for 2 yea r s 
o r m o r e a n d m a y b e c o n s i d e r e d a s a n evo lu t iona r i ly p r imi t i ve fea ture 
(Belozerov, 1976a, 1977) . 
13.3.2. Phys io logica l Properties of Diapause 
D i a p a u s e p r o v i d e s t w o d i s t i nc t a d v a n t a g e s . T h e first of these is s y n c h r o n -
iza t ion of t h e life-cycle w i t h f a v o u r a b l e s ea sons of t he y e a r as a l r e a d y d i s -
486 V. N. Belozerov 
cussed . T h e s econd a d v a n t a g e is r e s i s t ance to u n f a v o u r a b l e cond i t i ons 
( ex t r emes of t e m p e r a t u r e , d r o u g h t , o r lack of food) . T h i s r e s i s t ance d e p e n d s 
on a n a l t e red phys io log ica l s t a t e of t he a n i m a l , a n d the m o s t i m p o r t a n t 
c o n t r i b u t i n g factor is t h e d e c r e a s e d level of m e t a b o l i s m d u r i n g d i a p a u s e . 
D u r i n g the s ea sona l m o r p h o g e n e t i c d i a p a u s e of l a rva l a n d n y m p h a l / . ricinus, 
oxygen c o n su m p t i o n is d e c r e a s e d to 100 -150 m m
3
/ g / h (Belozerov, 
1964b) . D u r i n g t h e r e p r o d u c t i v e d i a p a u s e of D. marginatus females , t he 
d e c r e a s e in r e s p i r a t o r y m e t a b o l i s m is even m o r e p ro found ; oxygen con-
s u m p t i o n in d i a p a u s i n g females is 2 0 - 8 0 m m
3
/ g / h , a n d th is low r a t e c a n be 
m a i n t a i n e d for m a n y m o n t h s , wh i l e in n o n - d i a p a u s i n g females it is as h igh 
as 2 2 0 - 3 6 0 m m
3
/ g / h (Belozerov, 1966b) . M o r e o v e r , unfed a d u l t D. marginatus 
s h o w a d e c r e a s e in r e s p i r a t o r y r a t e of as m u c h as 5 0 - 6 0 m m
3
/ g / h d u r i n g 
b e h a v i o u r a l d i a p a u s e (Belozerov , 1968) . 
D e c r e a s e d m e t a b o l i c r a t e s d u r i n g d i a p a u s e c o n t r i b u t e to a m o r e economica l 
u t i l i za t ion of food reserves as is neces sa ry for su rv iva l d u r i n g p r o l o n g e d 
s t a r v a t i o n . T h i s is p a r t i c u l a r l y t r u e for unfed t icks in b e h a v i o u r a l d i a p a u s e 
w h e r e i nc r ea sed su rv iva l is a l so e n h a n c e d by a dec l ine ( b u t no t full cessa t ion) 
of l o c o m o t o r ac t iv i ty . 
I m a g i n a i ( adu l t ) d i a p a u s e in b l o o d - s u c k i n g A r t h r o p o d a is often c h a r a c -
te r ized by g o n o t r o p h i c d i s soc ia t ion , t h a t is by a n u n c o u p l i n g of the d iges t ive 
a n d r e p r o d u c t i v e p rocesses (Dan i l evsky , 1961; V i n o g r a d o v a , 1969). I n t he 
case of D. marginatus d u r i n g r e p r o d u c t i v e d i a p a u s e , t he u n c o u p l i n g occu r s 
d u r i n g feeding a n d is c h a r a c t e r i z e d by a n inh ib i t i on of n o r m a l oocy te deve l -
o p m e n t a t t he s t age of c y t o p l a s m i c a n d g r e a t e r c y t o p l a s m i c g r o w t h ( L a m a -
nova , 1965). P r e l i m i n a r y s tud ie s of d iges t ion in d i a p a u s i n g a n d n o n - d i a -
p a u s i n g females of th is t ick by s p e c t r o s c o p y (Belozerov & L ikho tk in , 1966) 
a n d e lec t ron m i c r o s c o p y (Belozerov & T y m o p h e e v , 1973) revea led n o specific 
differences e i t he r in t h e r a t e of d iges t ive processes o r in t he u l t r a s t r u c t u r a l 
c h a n g e s in m i d g u t ep i the l i a l cells d u r i n g feeding or after e n g o r g e m e n t . 
U l t r a s t r u c t u r a l c h a n g e s in t h e ep i the l ia l d iges t ive cells of b o t h g r o u p s of 
females w e r e cha rac t e r i s t i c a l l y r e l a t ed to the s tages of feeding. 
A n e l ec t ropho re t i c s t u d y of p r o t e i n s from h a e m o l y m p h a n d g u t ex t r ac t s 
of feeding D. marginatus females s h o w e d t h a t d i a p a u s e h a s a p r o f o u n d effect 
on p r o t e i n m e t a b o l i s m (Belozerov & Luzev , 1977). Differences in d iges t ive 
( m i d g u t p ro t e ins ) o r exc re to ry p rocesses (faecal p ro te ins ) w e r e negl ig ible , 
b u t t he d ivers i ty of h a e m o l y m p h p r o t e i n s in e n g o r g i n g females w h i c h a r e 
c o m m i t t e d to d i a p a u s e d e v e l o p m e n t w a s m u c h less t h a n t h a t of e n g o r g i n g 
females w h i c h will n o t e n t e r d i a p a u s e . After e n g o r g e m e n t , by c o n t r a s t , t he 
h a e m o l y m p h of d i a p a u s i n g females b e c o m e s e n r i c h e d in p r o t e i n s , b o t h q u a n -
t i ta t ively a n d qua l i t a t i ve ly , w h e r e a s in n o n - d i a p a u s i n g females t he oppos i t e 
occu r s as p r o t e i n s a r e u t i l ized for v i te l logenes is . T h e a c c u m u l a t i o n of p r o t e i n 
in t he h a e m o l y m p h of d i a p a u s i n g females m u s t resu l t from the low p inocy to t i c 
ac t iv i ty of t he i n h i b i t e d oocy tes . 
Diapause and Biological Rhythms in Ticks 487 
I n a s imi l a r s i t u a t i o n , D i e h l (1969) o b s e r v e d t h a t a c c u m u l a t i o n of h a e -
m o l y m p h v i te l logen ins in u n m a t e d females of 0. moubata co inc ided w i t h a 
de l ay of o v a r i a n d e v e l o p m e n t . U n d o u b t e d l y , a c c u m u l a t i o n of h a e m o l y m p h 
p ro t e in s r esu l t s f rom t h e syn thes i s of n e w p r o t e i n f rac t ions , a n d th is syn thes i s 
does no t cease d u r i n g d i a p a u s e . S o m e of these h a e m o l y m p h p ro t e in s a r e 
specific for d i a p a u s i n g t icks a n d m a y be invo lved in t he m e c h a n i s m s of 
g o n o t r o p h i c d i s soc ia t ion a n d d e l a y in v i te l logenes is . T h i s de l ay occu r s in 
sp i t e of t h e h i g h c o n t e n t of v i t e l logen ins o r the i r p r e c u r s o r s ( h a e m o p r o t e i n s ) 
in t he h a e m o l y m p h of d i a p a u s i n g females . 
Hopefu l ly , fu r the r s tud i e s o n tick e n d o c r i n o l o g y (see C h a p t e r s 9, 10 a n d 
11 ) a n d m e t a b o l i s m d u r i n g d i a p a u s e will h e l p to e luc ida t e t he m e c h a n i s m s 
w h i c h r e g u l a t e d iges t ion a n d r e p r o d u c t i o n in t icks a n d o t h e r a r t h r o p o d s . 
13.3.3. Photoperiodic Regulat ion o f Deve lopment and Diapause in Ticks 
P h o t o p e r i o d i c r e a c t i o n s to t h e l e n g t h s of d a y a n d n i g h t h a v e a p r i m a r y 
i m p a c t on m e c h a n i s m s r e g u l a t i n g d i a p a u s e in t icks . T h e i m p o r t a n c e of 
p h o t o p e r i o d in t h e con t ro l of t ick s e a s o n a l ac t iv i ty w a s d i scove red by S m i t h 
a n d C o l e (1941) for l a r v a e a n d n y m p h s of D. variabilis (Fig . 13.6) . S u b s e -
q u e n t l y it w a s found t h a t t h e m e t a m o r p h o s i s of/ , ricinus l a r v a e (Loew, 1962, 
1964; Be lozerov , 1964a; B a b e n k o & P l a t o n o v a , 1965) a n d oogenes is in female 
D. marginatus (Be lozerov , 1963) w a s con t ro l l ed b y p h o t o p e r i o d . I t is n o w 
k n o w n t h a t p r ac t i c a l l y every t y p e of t ick d i a p a u s e ( b e h a v i o u r a l a n d m o r -
p h o g e n e t i c ) is r e g u l a t e d by p h o t o p e r i o d ( T a b l e 13.6). I n m a n y cases p h o -
tope r iod i c s igna l s n o t on ly i n d u c e d i a p a u s e b u t a r e a lso i m p o r t a n t in its 
m a i n t e n a n c e a n d t e r m i n a t i o n . 
T i c k s , a s well as insec t s , man i fes t a g r e a t d ivers i ty of r eac t ions to d a y 
l eng th . T h e r e a r e t w o bas i c types : a l o n g - d a y r e a c t i o n ( L D ) , in w h i c h 
ac t ive d e v e l o p m e n t o c c u r s in r e s p o n s e to long d a y s a n d d i a p a u s e is in 
1 0 . X I0.ZI Ι8.ΧΠ 8.Π 2 2 J H 10 .X 10.XC i f lΤΠ 8 .H 22.ΠΙ 
T I M E O F Y E A R 
FlG. 13.6. Changes of aggressiveness of larvae (-Ο-) and nymphs ( - · - ) of Dermacentor variabilis 
under regimes of natural day length (1) and of artificially changed day-length (2). Thick curves 
1 and 2 show the changes of day length at natural and artificial illumination, respectively. 
(Reconstructed from data of Smith & Cole, 1941.) 
TABLE 13.6. PHOTOPERIODIC REGULATION OF SEASONAL ADAPTATIONS IN TICKS 
Processes 
regulated Type of 
Tick species Stage by photoperiod reaction Authors 
Ixodes ricinus L Development LD Loew (1962); Belozerov (1964a, 
1965, 1968) 
L Behaviour LD Belozerov (1968) 
Ν Development SD -LD Belozerov, (1966a, 1968, 1970, 
1972) 
Ν Behaviour LD Belozerov (1966a, 1968) 
A Oogenesis SD Belozerov (1973a) 
Ε Development SD Belozerov (1973a) 
I. persulcatus L Development LD Babenko & Platonova (1965) 
I. kazakstani L Development SD -LD Babenko and Gal'chenko (1976) 
I. trianguliceps L, N DevelopmentLD Bobrovskikh (1966) 
Haemaphysalis concinna L, N Development LD Belozerov (1969) 
L, N Behaviour LD Belozerov (1969) 
H. longicornis L, N Behaviour LD Belozerov and Luzev (1974) 
Dermacentor A Oogenesis SD Belozerov (1963, 1968) 
marginatus A Behaviour SD Belozerov (1967) 
D. pictus A Oogenesis SD Razumova (1965) 
D. silvarum A Feeding SD Belozerov (1973b) 
D. variabilis L, N Behaviour LD Smith and Cole (1941) 
D. albipictus L Behaviour SD Wright (1969a, 1971a) 
Rhipicephalus 
sanguineus (?) L Behaviour SD Sannassi and Subramoniam (1975) 
R. turanicus A Behaviour LD Belozerov (1976b) 
Hyalomma anatolicum N Development LD Belozerov and Mourad (1977) 
A Oogenesis LD Mourad and Belozerov (1976) 
Argas arboreus A Oogenesis LD Khalil (1976) 
Ornithodoros 
gurneyi A Oogenesis SD Doube (1975a) 
Abbreviations. Stages: L, larvae; N, nymphs; A, adults; E, egg. Types of reaction: LD, reaction of long-day type; SD, reaction of short-day type; 
SD-LD, two-step reaction of long-day-short-day type. 
488 
V
. N
. 
B
elozerov 
Diapause and Biological Rhythms in Ticks 489 
ο 6 12 18 2 4 0 6 12 18 2 4 
HOURS LIGHT / DAY HOURS L I G H T / DAY 
FlG. 13.7. Duration of metamorphosis in engorged larvae of Ixodes ricinus (from Leningrad 
district, L, and Moldavia, M) at 18° and different photoperiods. Unfed larvae were maintained 
at LD 12:12. (Belozerov, unpublished.) 
FlG. 13.8. Induction of reproductive diapause in engorged adult females of Dermacentor marginatus 
(K, from Kazakhstan; D, from Dagestan) according to photoperiods (at 18°) before their feeding. 
Diapause is taken as a delay of oviposition beyond 30 days (at 18°) after engorgement of females). 
(After Belozerov, 1968.) 
r e s p o n s e to s h o r t d a y s ; a n d a s h o r t - d a y r e a c t i o n ( S D ) , w h i c h is c h a r a c t e r i z e d 
by a r eve r sa l of t h e r e s p o n s e s (F igs . 13.7 a n d 13.8) . L D - r e a c t i o n s con t ro l t h e 
b e h a v i o u r of unfed l a r v a e , n y m p h s , a n d a d u l t s , d e v e l o p m e n t of e n g o r g e d 
l a r v a e a n d n y m p h s , a n d oogenes i s in s o m e ixodid a n d a r g a s i d species . I n 
o t h e r cases t he se even t s , p l u s female e n g o r g e m e n t a n d egg d e v e l o p m e n t , a r e 
con t ro l l ed b y a S D r e a c t i o n ( T a b l e 13.6) . 
A m o r e c o m p l e x p h o t o p e r i o d i c r e a c t i o n is a l so found in t icks. T h i s is a 
t w o - s t e p r e a c t i o n (Zas l avsky , 1972, 1975) in w h i c h d e v e l o p m e n t p r o c e e d s 
on ly after c e r t a i n i nc reases in p h o t o p e r i o d (e.g. c h a n g e from S D to L D ) , 
wh i l e o t h e r r e g i m e s resu l t in d i a p a u s e (e.g. s t ab l e S D or L D , o r c h a n g e from 
L D to S D ) . N y m p h s of / . ricinus g ive a n exce l len t e x a m p l e of t h e S D to L D 
r e s p o n s e ( S D - L D ) . 
As far a s c a n b e j u d g e d , e a c h species h a s its o w n c h a r a c t e r i s t i c p h o t o -
pe r i od i c r e a c t i o n s w h i c h a r e a d a p t e d to t h e pecu l ia r i t i e s of t he t ick 's life-
cycle. I n t e m p e r a t e c l i m a t i c r eg ions , r e a c t i o n of t h e L D type is c h a r a c t e r i s t i c 
for those t ick spec ies w i t h a life-cycle severa l y e a r s long a n d w i th o n e or 
m o r e unfed i n s t a r s o v e r w i n t e r i n g in a d o r m a n t o r d i a p a u s e s t a t e . T h e S D 
type of r e a c t i o n is m o r e c h a r a c t e r i s t i c of s o u t h e r l y species w h i c h h a v e o n e 
g e n e r a t i o n p e r y e a r a n d a s u m m e r p e r i o d of d o r m a n c y o r d i a p a u s e in unfed 
t icks. T h i s g e n e r a l i z a t i o n , e s t a b l i s h e d ea r l i e r in s tud ies o n t he p h o t o p e r i o d i c 
con t ro l of s e a s o n a l insec t d e v e l o p m e n t (Dan i l evsky , 1961) , app l i e s only to 
t h e tick species w h i c h exh ib i t a b e h a v i o u r a l d i a p a u s e in t h e unfed s tages . I t 
490 V. N. Belozerov 
obvious ly does n o t a p p l y to t hose o n e - h o s t ixodid t icks of t e m p e r a t e c l ima tes 
w h i c h feed on the i r hos t s d u r i n g the w i n t e r (e.g. s o m e Dermacentor spec ies ) . 
M o r e o v e r , m o r p h o g e n e t i c d i a p a u s e in t icks m a y be con t ro l l ed e i the r by L D 
or S D reac t ions , i r r e spec t ive of t h e t icks g e o g r a p h i c a l d i s t r i b u t i o n . L o n g - d a y 
r eac t ions m a y a r r e s t d e v e l o p m e n t in a u t u m n a n d e n s u r e h i b e r n a t i o n of 
e n g o r g e d t icks, b u t S D r eac t i ons m a y a lso a r r e s t d e v e l o p m e n t (pa r t i cu l a r ly 
r e p r o d u c t i v e d e v e l o p m e n t ) d u r i n g the onse t of u n f a v o u r a b l e w a r m (dry?) 
seasons . 
O n e of t he m o s t i m p o r t a n t p a r a m e t e r s of t he t icks r eac t ion to d a y l eng th 
is its c r i t i c a l ( t h r e s h o l d ) p h o t o p e r i o d . A t p h o t o p e r i o d s longer t h a n the 
cr i t ical one , t icks d i s p l a y the i r c h a r a c t e r i s t i c r e sponse ; t h a t is, n o r m a l deve l -
o p m e n t in L D species o r d i a p a u s e in S D species . A t p h o t o p e r i o d s s h o r t e r 
t h a n the cr i t ica l o n e the i r r e s p o n s e is r eversed ; n o r m a l d e v e l o p m e n t occu r s 
in S D species a n d d i a p a u s e in L D species . A t t he cr i t ical p h o t o p e r i o d the 
r a t io of d e v e l o p i n g to d i a p a u s i n g t icks is 1 : 1 . E n t o m o l o g i s t s hypo thes i ze t h a t 
t h e cr i t ical p h o t o p e r i o d is e q u a l o r p r o p o r t i o n a l to s o m e s t a n d a r d pe r iod 
used by insec ts in the i r p r i m a r y e v a l u a t i o n of d a y l eng th . Pe r cep t i on a n d 
e v a l u a t i o n of d a y l e n g t h t h u s a p p e a r s to be t h e first s t ep in all these 
phys io log ica l m e c h a n i s m s ( p h o t o p e r i o d i c r eac t ions ) w h i c h lead to d i a p a u s e 
( T y s h c h e n k o , 1977) . 
T h e g e o g r a p h i c va r i ab i l i t y a n d t e m p e r a t u r e labi l i ty of t he cr i t ical p h o t o -
pe r iod is of g r e a t ecological s ignif icance for t icks, as it is for insects ( D a n i -
levsky, 1961; D a n i l e v s k y et al., 1970) . T h i s va r i ab i l i ty a l lows seasona l deve l -
o p m e n t to be c o - o r d i n a t e d w i t h t h e c l ima t i c r h y t h m in different g e o g r a p h i c a l 
zones , b u t it a l so a l lows t h e r h y t h m of t ick d e v e l o p m e n t to r e s p o n d to 
s ignif icant modi f i ca t ions in t he w e a t h e r from y e a r to yea r . A progress ive 
inc rease in t h e l eng th of t h e cr i t ica l p h o t o p e r i o d m a y o c c u r w i th i nc r ea s ing 
l a t i t u d e (Dan i l evsky , 1961; D a n i l e v s k y et al., 1970) . I n / . ricinus l a rvae , t he 
cr i t ical p h o t o p e r i o d for m o r p h o g e n i c d i a p a u s e va r ies from 15 to 16 h of l ight 
p e r d a y in t icks f rom M o l d a v i a (46.3°N) to 17 -18 h p e r d a y for t icks from 
L e n i n g r a d (59 .6°N) . I n s o m e cases t h e r e is n o g e o g r a p h i c a l v a r i a t i o n in t he 
cr i t ical p h o t o p e r i o d . P o p u l a t i o n s oiD. marginatus f rom D a g h e s t a n , Povo lzhye , 
a n d K a z a k h s t a n , for e x a m p l e , all h a v e a t h r e sho ld of 13 h of l ight p e r d a y 
(a t 13°C) for the i r r e p r o d u c t i v e d i a p a u s e (Belozerov, 1968). 
I n insec ts , a n i nc r ea se in t e m p e r a t u r e m a y lower t he cr i t ica l p h o t o p e r i o d 
for b o t h L D a n d S D r eac t i ons (Dan i l evsky , 1961; T y s h c h e n ko , 1977). Ixodes 
ricinus h a s a t h e r m o l a b i l e p h o t o p e r i o d i c r e s p o n s e (Fig. 13.9) , w i th a fall 
in t h r e s h o l d a t h i g h e r t e m p e r a t u r e s , b u t in D. marginatus t he cr i t ical p h o -
tope r iod is t h e r m o s t a b l e (Fig . 13.10) a l t h o u g h fewer t icks d i a p a u s e a t sho r t 
p h o t o p e r i o d s a t h i g h e r t e m p e r a t u r e s . A m o r e c o m m o n gene ra l i za t i on for 
insec ts a n d t icks is t h a t h i g h e r t e m p e r a t u r e s r e d u c e t he p r o p o r t i o n in d i a p a u s e 
for L D species b u t re inforces d i a p a u s e in S D species . 
P h o t o p e r i o d i c r eac t i ons in a r t h r o p o d s a lso d e p e n d o n the ex is tence of 
Diapause and Biological Rhythms in Ticks 491 
UJ 
ω 
3 
< 
CL 
< 5 0 -
Q 
loo H 
ο-
ο 6 12 18 2 4 Ο 6 12 18 24 
HOURS L I G H T / D A Y HOURS L I G H T / D A Y 
FlG. 13.9. An influence of temperature on the photoperiodic induction of morphogenetic diapause 
in nymphs of Ixodes ricinus (from Leningrad) before their feeding. Diapause is taken as a delay 
of metamorphosis in engorged nymphs beyond 60 days (at 18° and LD 12:12) after their 
engorgement. (After Belozerov, 1970.) 
FlG. 13.10. The photoperiodic induction of reproductive diapause in unfed adult females of 
Dermacentor marginatus (from Dagestan) at 18° and 25°C. Diapause is taken here as a delay of 
oviposition beyond 120 days (at 18°) after engorgement. (After Belozerov, 1965.) 
s e n s i t i v e a n d r e s p o n s i v e s t a g e s . I n s e c t s u sua l ly h a v e a sens i t ive s t age w h i c h 
is fol lowed, o n e o r m o r e i n s t a r s l a te r , by t h e d i a p a u s e r e sponse . O n l y in a 
few cases a r e t h e insec t sens i t ive a n d r e spons ive s t ages c o m b i n e d in t h e s a m e 
i n s t a r (Dan i l evksy 1961; S a u n d e r s , 1976; T y s h c h e n k o , 1977). I n t icks, to t he 
c o n t r a r y , t h e sens i t ive a n d r e spons ive s tages often o c c u r in t he s a m e ins t a r . 
M o r e o v e r , t h e d i a p a u s i n g tick u sua l l y r e t a i n s its sensi t ivi ty to d a y l eng th ; 
p h o t o p e r i o d is therefore invo lved in t h e m a i n t e n a n c e of d i a p a u s e . T h i s is 
o b s e r v e d d u r i n g t h e m o r p h o g e n e t i c d i a p a u s e of l a rva l a n d n y m p h a l / . ricinus 
(Belozerov , 1964a, 1966a, 1968; B a b e n k o , 1970; B a b e n k o & P l a t o n o v a , 1965) , 
a n d Haemaphysalis concinna (Be lozerov , 1969) , d u r i n g the n y m p h a l m o r p h o -
gene t i c a n d a d u l t r e p r o d u c t i v e d i a p a u s e s of Hyalomma anatolicum ( M o u r a d 
& Belozerov , 1976; Be loze rov & M o u r a d , 1977) , a n d in all cases of b e h a v -
iou ra l d i a p a u s e (Belozerov , 1968, 1975) . D i a p a u s e of e n g o r g e d l a r v a e , 
n y m p h s , a n d a d u l t s of m o s t ixod id t icks s t u d i e d is therefore con t ro l l ed by 
p h o t o p e r i o d i c s t imu l i w h i c h a c t before , d u r i n g , a n d after e n g o r g e m e n t 
(Belozerov, 1968) . T w o excep t ions o c c u r d u r i n g the r e p r o d u c t i v e d i a p a u s e 
of female D. marginatus (Be lozerov , 1968) a n d Argas arboreus ( K h a l i l , 1976). 
I n these species t h e p h o t o p e r i o d i c sens i t iv i ty is lost after e n g o r g e m e n t ; 
p h o t o p e r i o d i n d u c e s b u t d o e s n o t m a i n t a i n d i a p a u s e . D i a p a u s e of this n a t u r e 
is h igh ly s t ab l e b e c a u s e it c a n b e b r o k e n on ly by a r e a c t i v a t i o n p r o c e s s 
w h i c h o c c u r s d u r i n g a long p e r i o d of chi l l ing . C o l d r eac t i va t i on in D. 
marginatus females r e q u i r e s 3 - 4 m o n t h s (Belozerov , 1968). 
A n o t h e r d i s t inc t ive fea tu re of p h o t o p e r i o d i c r eac t ion in t icks is t he long 
492 V. N. Belozerov 
d u r a t i o n of t he sens i t ive s t a g e ( s ) . L a r v a l a n d n y m p h a l / . ricinus r e t a i n the i r 
sensi t ivi t ies for 1 5 - 1 6 m o n t h s wh i l e a w a i t i n g a hos t , for a n o t h e r 3 - 5 d a y s 
d u r i n g feeding, a n d for a pe r iod of d a y s o r m o n t h s after feeding. U n f e d 
female D. marginatus r e t a i n the i r sens i t ive p e r i o d t h r o u g h o u t t he pe r iod of 
the i r s t a r v a t i o n for u p to 2 yea r s (Belozerov , 1968) . T h i s i n t r o d u c e s a n o t h e r 
c h a r a c t e r i s t i c of t h e p h o t o p e r i o d i c r e ac t i on w h i c h is specific for t icks. A 
sea sona l r eve r sa l of p h o t o p e r i o d (e.g. L D to S D ) often occu r s d u r i n g the 
p r o l o n g e d sens i t ive s t age , b u t t h e tick c a n still m a k e a r e s p o n s e w h i c h is 
a p p r o p r i a t e to t h e p h o t o p e r i o d it e x p e r i e n c e d j u s t p r i o r to feeding (Belozerov, 
1968). A g e a lso h a s a n effect o n t h e r e g u l a t i o n of d i a p a u s e as first d i scovered 
by R a s u m o v a (1960) in D. pictus. I n c r e a s i n g age usua l ly l eads to a w e a k e n i n g 
of t h e p h o t o p e r i o d i c i n d u c t i o n a n d m a i n t e n a n c e of d i a p a u s e (Belozerov, 
1968) , a n d s o u t h e r n g e o g r a p h i c r aces a r e m o r e affected by th is t h a n n o r t h e r n 
ones . 
T h e p a r a m e t e r s of p h o t o p e r i o d i c r eac t i ons in t e r res t r i a l a r t h r o p o d s a r e 
la rge ly d e t e r m i n e d b y the i r ecological n i c h e , th is b e i n g different for e ach 
species a n d even for e a c h in t raspec i f ic g e o g r a p h i c a l r ace . I n insects th is m a y 
b e s h o w n by differences in t h e l e n g t h of t h e cr i t ica l p h o t o p e r i o d , a n d in t he 
n u m b e r of l i g h t - d a r k cycles r e q u i r e d for t h e i n d u c t i o n of d i a p a u s e ( G o r y s h i n 
& G e y s p i t z , 1975) . T h e s low r e s p o n s e of t icks to the i r cr i t ica l p h o t o p e r i o d 
(a 2 - 3 - w e e k e x p o s u r e is often r e q u i r e d to i n d u c e d i a p a u s e ) m a y b e of 
ecological i m p o r t a n c e as wel l a n d m a y even be r e l a t ed in s o m e w a y to t h e 
l eng th of t h e sens i t ive s t age . I t s l eng th m a y a l so reflect s o m e phys io log ica l 
m e c h a n i s m in t h e p h o t o p e r i o d i c r eac t i on . 
13.3.4. Photoperiodic Regulat ion o f Seasonal Adaptations 
D i a p a u s e r e g u l a t i o n a m o n g insec ts is i n i t i a t ed by p h o t o p e r i o d p e r c e p t i o n , 
a n d th is i n f o r m a t i o n is t r a n s f o r m e d " s t e p - b y - s t e p " i n to phys io log ica l 
r e sponse s . I t h a s b e e n p r o p o s e d t h a t in insec ts t h e r e a r e t h r ee m a i n s t eps 
in t h e t ransfer of i n f o r m a t i o n : 
( 1 ) p e r c e p t i o n a n d e v a l u a t i o n of ex t r ins ic s igna ls by p h o t o r e c e p t o r s a n d 
" p h o t o p e r i o d i c c locks" , b o t h of w h i c h a r e loca ted in t he b r a i n — t h e 
o u t p u t f rom th is s t e p is e i the r a n L D o r S D s igna l ; 
(2) t h e a c c u m u l a t i o n a n d m a i n t e n a n c e of these L D a n d S D s igna ls in t he 
" p h o t o p e r i o d i c m e m o r y " by m e a n s of a p h o t o p e r i o d i c coun t e r ; 
(3) t he r ea l i za t ion of t h e p h o t o p e r i o d i c i n fo rma t ion in t e r m s of d i a p a u s e 
or d e v e l o p m e n t — t h i s is g o v e r n e d by n e u r o s e c r e t o r y cells in the n e r v o u s 
sys t em a n d b y e n d o c r i n e o r g a n s o u t s i d e t h e n e r v o u s sys t em. 
T h e s a m e m e c h a n i s m s p r o b a b l y o c c ur in t icks, a n d a m o d e l h a s b e e n 
dev i sed w h i c h is b a s e d on t h e s h o r t - d a y to l o n g - d a y ( S D - L D ) r eac t i on of 
Diapause and Biological Rhythms in Ticks 493 
n y m p h a l / . ricinus (Be lozerov , 1970, 1972; r ev i ewed by E m e r i t , 1972). A c c o r d -
ing to th is m o d e l , a r a t h e r c o m p l e x r e g u l a t o r y s y s t e m i n t e g r a t e s t he p e r c e p t i o n 
of p h o t o p e r i o d a n d t h e t r ans fe r of i n f o r m a t i o n to t h e e n d o c r i n e g l a n d s (Fig . 
13.11) . T h e first c o m p a r t m e n t is t h e p r i m a r y l ink of p e r c e p t i o n a n d e v a l u a t i o n 
of ex t r ins ic p h o t o p e r i o d i c s t imu l i ( P E E P ) a n d its c o d e d o u t p u t ( S D or L D 
s ignals) affects t h e c e n t r e for p r o d u c t i o n of a c t i v a t i n g h o r m o n e ( P A H ) . T h e 
a c t i v a t i n g h o r m o n e t r iggers t h e ac t iv i ty of a n e n d o c r i n e g l a n d or t i ssue 
( P M H ) w h i c h p r o d u c e s t h e m o u l t i n g h o r m o n e . I n t u r n , t he m o u l t i n g h o r -
m o n e r e a c h e s t h e t a r g e t t i ssues a n d in i t i a t es m e t a m o r p h o s i s . I t is p r o p o s e d 
t h a t t h e r e is a n o t h e r c e n t r e w h i c h p r o d u c e s a n i n h i b i t i n g h o r m o n e ( P I H ) 
FlG. 13.11. A model of neuroendocrine mechanisms in the photoperiodic control of development 
and diapause in nymphs of Ixodes ricinus: ( 1 ) represents the positive stimulating effect of SD 
photoperiods on production of activating hormone (PAH) in fed nymphs; (2) the positive 
stimulating effect of LD on production of inhibiting hormone (PIH) in unfed nymphs; (3) the 
negative efTects of SD on the production of deblocking factor (PDF) in fed nymphs; and (4) the 
positive stimulating efTects of LD on the production of deblocking factor (PDF) in fed nymphs. 
Production of moulting hormone (PMH) is thought to be controlled by these interactions as 
described in the text. (Modified from Belozerov, 1972.) 
to b lock t h e c o n n e c t i o n b e t w e e n p h o t o p e r i o d i c p e r c e p t i o n a n d e v a l u a t i o n 
( P E E P ) a n d t h e p r o d u c e r of a c t i v a t i n g h o r m o n e ( P A H ) . B o t h ( P A H ) a n d 
( P I H ) a r e e n d o c r i n e o r n e u r o e n d o c r i n e o r g a n s w h i c h secre te h o r m o n e after 
r ece iv ing a L D s t i m u l u s f rom t h e p e r c e p t i o n a n d e v a l u a t i o n c e n t r e ( P E E P ) 
in t h e b r a i n . T h e m o d e l se rves to e x p l a i n t w o different fo rms of n y m p h a l 
d i a p a u s e in / . ricinus b o t h of w h i c h a r e exp re s sed as a de l ay in m e t a m o r p h o s i s . 
D i a p a u s e o c c u r s w h e n unfed n y m p h s a r e exposed to t h e s a m e p h o t o p e r i o d i c 
c o n d i t i o n s ( S D or L D ) b o t h before a n d after e n g o r g e m e n t , a n d it c a n be 
b r o k e n b y a r eve r sa l of th i s p h o t o p e r i o d in t h e e n g o r g e d n y m p h s (e i ther by 
S D to L D , o r L D to S D ) . 
T h e S D d i a p a u s e in e n g o r g e d n y m p h s resu l t s f rom t h e S D s igna ls rece ived 
by t h e P A H whi l e t h e L D d i a p a u s e , i n d u c e d p r i o r t o f e e d i n g , is a resu l t 
494 V. N. Belozerov 
of t h e i nh ib i t o ry effect of t he h o r m o n e p r o d u c e d by P I Η w h i c h blocks t he 
s ignals b e t w e e n P E E P a n d P A H in t he unfed n y m p h . T h i s c o n n e c t i o n c a n 
be r e s to red by t h e p r o d u c t i o n of a d e b l o c k i n g h o r m o n a l fac tor (Fig. 13 .11 , 
P D F ) w h i c h is a n t a g o n i s t i c to t h e ac t i on of t he i nh ib i t i ng h o r m o n e . T h i s 
d e b l o c k i n g h o r m o n e is p r o d u c e d in r e s p o n s e to S D s ignals b y fed t icks in 
d i a p a u s e a n d exp la in s h o w p r o l o n g e d S D t r e a t m e n t ( S D sens ib i l iza t ion ; 
Zas l avsky , 1972) c a n r e s to re t he ab i l i ty of t h e n y m p h a l P A H c e n t r e to 
r e s p o n d to L D s igna ls . 
S u c h a n e l a b o r a t e c o m p l e x of n e u r a l , n e u r o e n d o c r i n e , a n d e n d o c r i n e 
i n t e r ac t i ons m a y on ly b e neces sa ry in species sens i t ive to t h e S D to L D 
t r ans i t i on w i t h a t w o - s t e p r eac t i on . F o r s i m p l e r r eac t i ons , on ly o n e e n d o c r i n e 
or n e u r o e n d o c r i n e e l e m e n t m a y b e funct iona l ly i m p o r t a n t a t a n y o n e t ime , 
as in t he p r o d u c t i o n of e i the r a c t i v a t i n g or i n h i b i t i n g h o r m o n e a c c o r d i n g to 
t h e coded o u t p u t of t h e p e r c e p t i o n a n d e v a l u a t i n g cen t res by L D or S D 
species . 
T h e m o d e l is c o m p a t i b l e w i t h w h a t is k n o w n of tick endoc r ino logy (see 
C h a p t e r s 10 a n d 11). I n fact, t icks m a y use s o m e of t h e s a m e h o r m o n e s as 
insec ts , c o n t r a r y to t h e s t a t e m e n t s of S t aa l (1975) a n d desp i t e t he differences 
in a n a t o m i c a l o r g a n i z a t i o n . I t h a s b e e n e s t ab l i shed t h a t ecdysones a n d 
j u v e n i l e h o r m o n e a n a l o g u e s a r e effective in t he t e r m i n a t i o n of tick d i a p a u s e 
( W r i g h t , 1969b; S a n n a s i & S u b r a m o n i a m , 1972; Bassa l & R o s h d y , 1974) 
o r t he d i s t u r b a n c e of d e v e l o p m e n t (Ioffe et al., 1977; see a lso C h a p t e r 11). 
I t is of p a r t i c u l a r in t e res t t h a t n e u r o s e c r e t o r y m a t e r i a l a c c u m u l a t e s in ce r t a in 
cells of t h e b r a i n ( syngang l ion ) d u r i n g d i a p a u s e (Ioffe, 1965), s ince such 
a c c u m u l a t i o n s a r e a lso c h a r a c t e r i s t i c of d i a p a u s i n g insec ts . 
E x p e r i m e n t s o n t h e m e c h a n i s m s of r e p r o d u c t i v e d i a p a u s e in A. arboreus 
h a v e s h o w n t h a t t h e b r a i n in i t i a tes p r o d u c t i o n of t w o a n t a g o n i s t i c 
h o r m o n e s — o n e a g o n a d o t r o p i c a n d t h e o t h e r a d i a p a u s i n g h o r m o n e . 
T o g e t h e r , t hese h o r m o n e s con t ro l t he r e p r o d u c t i v e processes (Kha l i l , 1974, 
1976; S h a n b a k y & K h a l i l , 1975; K h a l i l & S h a n b a k y , 1976). F a c u l t a t i v e 
d i a p a u s e in th is tick is a s y n d r o m e of g o n a d o t r o p i c h o r m o n e deficiency in 
t he p r e s e n c e of t h e d i a p a u s i n g factor (or h o r m o n e ) . T h e l a t t e r is p r o d u c e d 
in unfed females in r e s p o n s e to a S D reac t ion , b u t t h e t a rge t s for the 
d i a p a u s i n g h o r m o n e d o n o t a p p e a r to b e in t h e n e u r a l cen t re s (or s o m e o t h e r 
o r g a n w h e r e g o n a d o t r o p i c h o r m o n e is p r o d u c e d ) b u t in the cells of t he 
r e p r o d u c t i v e a n d / o r t he d iges t ive o r g a n s . 
I t is poss ib le t h a t r e p r o d u c t i v e d i a p a u s e involves a c o m b i n a t i o n of b lock ing 
the a c t i v a t i n g cen t r e s in t he b r a i n a n d i n h i b i t i n g d iges t ive a n d r e p r o d u c t i v e 
o r g a n s , b u t th is will on ly b e e s t ab l i shed by fu r the r inves t iga t ions . T h e r e is 
n o d o u b t t h a t t he n e u r o e n d o c r i n e sys t em (neu rosec re to ry cells a n d e n d o c r i n e 
g l a n d s ) in t icks, as well as insec ts , is t he l ink b e t w e e n p h o t o p e r i o d i c p e r c e p t i o n 
a n d d i a p a u s e , a n d as s u c h its fu r the r s t u d y w o u l d be of g r e a t v a l u e in 
u n d e r s t a n d i n g d i a p a u