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Ultrasonic signals from rodents
Ultrasonic signals from rodents G. D. Sewell*
A b r i e f a c c o u n t i s g i v e n of the d i s c o v e r y of the u l t r a s o u n d s p r o d u c e d b y r o d e n t s and the s i t u a t i o n s in which t h e y a r e e m i t t e d . T h e e q u i p m e n t u s e d to s t u d y t h e s e s i g n a l s i s d e s c r i b e d b r i e f l y . R o d e n t s e m i t a wide v a r i e t y of u l t r a s o n i c s i g n a l s and while t h e r e i s s o m e e v i d e n c e t h a t t h e y can h e a r t h e s e s o u n d s , little i s known of how t h e y a r e p r o d u c e d . T h e p h y s i c a l c h a r a c t e r i s t i c s of the s i g n a l s t h e m s e l v e s a r e t h e r e f o r e of g r e a t i n t e r e s t a s t h e y m a y g i v e s o m e c l u e s a s to the m e c h a n i s m of u l t r a s o u n d p r o d u c t i o n . A d e s c r i p t i o n i s give
of the d i f f e r e n t h a r m o n i c s p e c t r a found in t h e s e u l t r a s o n i c s i g n a l s and the v a r i a t i o n s in a m p l i t u d e and p a t t e r n s of f r e ~ q u e n c y c h a n g e t h a t o c c u r within t h e s e s p e c t r a . T h e r e l a t i o n s h i p b e t w e e n the p h y s i c a l c h a r a c t e r i s t i c s of the s i g n a l s and the s i t u a t i o n s in which t h e y a r e e m i t t e d i s d i s c u s s e d , t o g e t h e r with p o s s i b l e r e a s o n s for the u s e of s u c h high f r e q u e n c y s o u n d s . F i n a l l y the p r o b l e m s that h a v e a r i s e n out of t h i s work a r e r e v i e w e d and f u t u r e l i n e s of s t u d y a r e i n d i c a t e d .
It h a s b e e n known for s o m e 30 y e a r s t h a t b a t s p r o d u c e u l t r a sonic s i g n a l s 1 , 2, but it h a s r e c e n t l y b e c o m e known that m a n y r o d e n t s a l s o e m i t u l t r a s o u n d s . In 1954 A n d e r s o n 3 d e t e c t e d ' p u r e t o n e s ' of 23-38kHz f r o m a d u l t r a t s alone in t h e i r c a g e s and l a t e r Z i p p e l i u s and Schleidt (1956) 4 and a l s o N o i r o t (1965) 5 r e p o r t e d t h a t w h e n the young of s e v e r a l s p e c i e s of r o d e n t s w e r e r e m o v e d f r o m the n e s t and i s o l a t e d on a b e n c h top, t h e y e m i t t e d u l t r a s o n i c c r i e s . T h e s e c a l l s w e r e p r o d u c e d at l e a s t until the e y e s of t h e young o p e n e d at the a g e of about 10-15 d a y s . T h e a u t h o r s s u g g e s t e d t h e y w e r e d i s t r e s s c a l l s , which w e r e e m i t t e d by the young u n d e r c o n d i t i o n s of cold a n d h u n g e r and which s e r v e d to e l i c i t the r e t r i e v i n g r e s p o n s e of the m o t h e r a n i m a l and to guide h e r to s t r a y young, out of the nest.
and it w a s found that s h o r t u l t r a s o u n d s , g e n e r a l l y 1 0 - 6 0 m s long at f r e q u e n c i e s of about 50kHz, w e r e often p r o d u c e d during a g g r e s s i v e behaviour. Many s u b m i s s i v e animals prod u c e d long s o u n d s of 22-30kHz which l a s t e d f o r 2 0 0 - 3 4 0 0 m s and could be c o r r e l a t e d with the i r r e g u l a r r e s p i r a t i o n s of the submissive animals.
T h e p r e s e n t s t u d y b e g a n a s a c o m p a r a t i v e s u r v e y of the p r o d u c t i o n of u l t r a s o u n d b y the young of s m a l l m a m m a l s . T h e e x t e n t of the s u r v e y w a s l i m i t e d to the a n i m a l s t h a t could b e a c q u i r e d in t h i s c o u n t r y e i t h e r by live t r a p p i n g B r i t i s h s p e c i e s in the field or by o b t a i n i n g f o r e i g n s p e c i e s f r o m o t h e r r e s e a r c h i n s t i t u t i o n s . A r e c e n t t r i p to E a s t A f r i c a e x p a n d e d the s c o p e of the s u r v e y . So f a r 39 s p e c i e s , i n c l u d i n g 25 s p e c i e s of r o d e n t s , 3 s p e c i e s of p r i m a t e s and 7 s p e c i e s of i n s e c t i v o r e s h a v e b e e n o b s e r v e d in one w a y or a n o t h e r . T h e a n i m a l s t h a t w e r e s t u d i e d in d e t a i l b e l o n g e d to e i t h e r of two f a m i l i e s of the m y o m o r p h g r o u p of r o d e n t s . T h e s e f a m i l i e s w e r e the C r i c e t i d a e w h i c h i n c l u d e s h a m s t e r s , v o l e s and g e r b i l s and the M u r i d a e which i n c l u d e s r a t s , m i c e and t h e i r a l l i e s . T h e p h e n o m e n o n of u l t r a s o u n d e m i s s i o n by young w a s c o n f i r m e d for a l l eight s p e c i e s of C r i c e t i d a e a n d for the s e v e n s p e c i e s of M u r i d a e of which l i t t e r s w e r e e x a m i n e d . W h e r e p o s s i b l e the s i g n a l s w e r e s t u d i e d daily f r o m b i r t h o n w a r d s so that any c h a n g e s with a g e could be d e t e r m i n e d . D u r i n g the c o u r s e of t h i s w o r k it w a s found that u l t r a s o u n d s could be e l i c i t e d f r o m r a t s , long a f t e r the e y e s of the young h a d o p e n e d a n d well into adult life, b y h a n d l i n g the a n i m a l s 6. T h i s i n v o l v e d r o l l i n g the r a t s on to t h e i r b a c k s and r e s t r a i n ing t h e m in a p o s t u r e s i m i l a r to that of the s u b m i s s i v e p o s t u r e of a d u l t s t o w a r d s a n a g g r e s s o r 7. S u b s e q u e n t l y a g g r e s s i v e and s u b m i s s i v e b e h a v i o u r of adult l a b o r a t o r y r a t s w a s s t u d i e d
M i s s G. D. Sewell, D e p a r t m e n t of Zoology, U n i v e r s i t y of London, K i n g ' s C o l l e g e , Strand, London. W.C .2.
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Various other aspects of social behaviour in rodents were then studied. Ultrasounds were detected during aggressive behaviour in several species (see Table 1) and they appeared to be produced by the attacking animals. In gerbils, audible 'retaliation' cries with pronounced ultrasonic components were also emitted, apparently by the subordinate animal as he fended off the attacker. Fully submissive postures were seen only in rats. Ultrasonic signals were detected during mating in all the species in which mating behaviour was observed. Generally these signals could be correlated with the movements of the male but in hamsters,ultrasounds were detected when a female which was on heat nosed other hamsters, either male or female, which were introduced singly into her cage. Ultrasounds were also detected in situations where the a n i m a l s a p p e a r e d to b e e x p l o r i n g - - f o r e x a m p l e , when adult wood m i c e e m e r g e d f r o m the n e s t a f t e r the c a g e had b e e n d i s t u r b e d and a l s o 2 - 3 r a i n a f t e r they had bee,~ put into a new c a g e . S i g n a l s w e r e p r o d u c e d by l a c t a t i n g f e m a l e s of t h r e e s p e c i e s a f t e r t h e i r l i t t e r s had b e e n r e m o v e d f r o m the n e s t s . In yet a n o t h e r s i t u a t i o n , v o c a l s i g n a l s w e r e p r o d u c e d a s a l a c t a t i n g f e m a l e g e r b i l t h u m p e d one hind foot on the g r o u n d after being disturbed. These may r e p r e s e n t warning signals. U l t r a s o u n d s a r e t h u s p r o d u c e d in a wide v a r i e t y of s i t u a t i o n s by r o d e n t s , but if t h e y a r e u s e d for c o m m u n i c a t i o n , the a n i m a l s m u s t be able to h e a r t h e m and t h e r e i s s o m e e v i d e n c e for t h i s . It h a s b e e n r e p o r t e d f r o m v a r i o u s b e h a v i o u r a l r e a c t i o n s that s e v e r a l s p e c i e s of m y o m o r p h r o d e n t s c a n h e a r well into the u l t r a s o n i c r a n g e l o . R e c e n t l y , R a l l s 1~ h a s u s e d e l e c t r o p h y s i o l o g i c a l t e c h n i q u e s to s t u d y the a u d i t o r y s e n s i t i v i t i e s of wild h o u s e m i c e , two s t r a i n s of l a b o r a t o r y m i c e and two s p e c i e s of d e e r m i c e . She h a s shown that the young of t h e s e a n i m a l s at l e a s t a r e s e n s i t i v e to f r e q u e n c i e s up to 70-80kHz. T h e lowest t h r e s h o l d s for a d u l t s w e r e b e t w e e n 10kHz and 30-40kHz in d e e r m i c e and at about 20kHz in wild h o u s e m i c e . In the s t r a i n s of l a b o r a t o r y m i c e , h o w e v e r , s h e found t h a t the a u d i t o r y s e n s i t i v i t i e s to f r e q u e n c i e s above 7-12kHz d e c r e a s e d v e r y r a p i d l y with a g e .
T a b l e 1 O c c u r r e n c e of u l t r a s o u n d e m i s s i o n by r o d e n t s Colloquial name
F o r m a l name
Young
Aggression
Mating
Bank vole
Clethrionomys glareolus
Yes
?
Yes
Other
Family Cricetidae
F i e l d vole
Microtus agrestis
Yes
No
--
Hamster
Mesocricetus auratus
Yes
No
Yes
Mongolian gerbil
Meriones unguiculatus
Yes
--
--
Libyan gerbil
Meriones libycus
Yes
Yes
--
retaliation*
Sand rat or gerbil
Gerbillus species
Yes
Yes
--
retaliation*
Deer mouse
Peromyscus species
Yes*
No
Yes
Steppe lemming
Lagurus lagurus
Yes
No
Yes
Rattus n o r v e g i c u s
Yes
Yes
Yes
Rattus norvegicus
--
Yes
--
Mice: (a) Albino laboratory strain (b) Grey laboratory strain
Mus musculus Mus musculus
Yes Yes
No No
Yes Yes
Minute mouse
Mus minutoides
Yes
No
Yes
Wood mouse
Apodemus sylvaticus
Yes
--
--
exploratory
Spiny mouse
Acomys caharinus
Yes
?
Yes
lactating f e m a l e
Multimammate mouse
Praomys natalensis
Yes
No
Yes
Family Muridae
Rats: (a) L a b o r a t o r y s t r a i n s (b) Wild strain
African forest mouse
Thamnomys species
Yes
Yes
--
Kusu rat
Arvicanthis niloticus
--
Yes
--
submission submission lactating f e m a l e
* = s o m e s i g n a l s with audible and u l t r a s o n i c c o m p o n e n t s
While little i s known of the ability of r o d e n t s to h e a r u l t r a sounds, even l e s s i s known of the m e c h a n i s m by which they a r e p r o d u c e d . So the s t r u c t u r e of the sounds t h e m s e l v e s i s of i n t e r e s t a s it may give s o m e c l u e s a s to the m e c h a n i s m involved. B a t s p r o d u c e u l t r a s o u n d s of 0 . 2 5 - 1 0 0 m s duration with i n t e n s i t i e s of up to 120dB r e 0. 0002~zbar r . m . s . , m e a s u r e d at 10cm f r o m the a n i m a l . T h e s e s i g n a l s may have one o r m o r e h a r m o n i c c o m p o n e n t s and a r e p r o d u c e d in the larynx. 12 P y e 13 has s u g g e s t e d that the l a r y n g e a l wave f o r m i s n o n s i n u s o i d a l and that the h a r m o n i c s it contains a r e influenced b e f o r e e m i s s i o n by the vocal t r a c t s acting a s s i m p l e r e s o n a n c e f i l t e r s . T h i s , he points out, i s c o m p a r a b l e to the phonetic t h e o r y of human vowel production, but in b a t s only one r e s o n a n t peak o r f o r m a t n e e d s to be p o s t u l a t e d i n s t e a d of the four p r e s e n t in human vowel sounds. Griffin 14 adopted the w o r d ' p u l s e ' in connection with the u l t r a s o u n d s p r o d u c e d by b a t s to denote a single u l t r a s o n i c c r y . This word has b e e n u s e d to m e a n many d i f f e r e n t p h e n o m e n a l 5 , but in this account of the u l t r a s o u n d s p r o d u c e d by r o d e n t s the w o r d ' p u l s e ' will be u s e d for a single u l t r a s o n i c sound. R o d e n t s p r o d u c e a wide v a r i e t y of u l t r a s o n i c p u l s e s which r a n g e in d u r a t i o n f r o m 2ms to 3400ms. V a r i a t i o n s in amplitude o c c u r within the sounds and peak i n t e n s i t i e s of up to 106dB have b e e n r e c o r d e d at 10cm. The f r e q u e n c i e s e m i t t e d range f r o m 20kHz (the conventional lower limit of the t e r m ' u l t r a s o u n d ' ) to 150kHz (the p r a c t i c a l upper limit of the r e c o r d i n g a p p a r a t u s ) . Within t h e s e l i m i t s a wide v a r i e t y of f r e q u e n c y s p e c t r a a r e found. M o s t of the sounds that w e r e studied c o n s i s t e d of a single f r e q u e n c y component, but s o m e contained s e v e r a l h a r m o n i c a l l y r e l a t e d components while o t h e r s c o n s i s t e d of many c l o s e l y s p a c e d and a p p a r e n t l y h a r m o n i c a l l y u n r e l a t e d c o m p o n e n t s . O c c a s i o n a l l y all t h e s e t h r e e f r e q u e n c y s t r u c t u r e s w e r e found in one p u l s e and w i t h in any one of them the f r e q u e n c y level often changed in a v a r i e t y of ways, to be c o n s i d e r e d l a t e r . All t h e s e d i f f e r e n t p h e n o m e n a m u s t be accounted for by any m e c h a n i s m that i s s u g g e s t e d for the p r o d u c t i o n of u l t r a s o u n d s by r o d e n t s .
METHOD OF STUDY During this study, u l t r a s o u n d was m o n i t o r e d 16,17 'audibly' using a tunable s u p e r h e t e r o d y n e ' b a t - d e t e c t o r ' and ' v i s i b l y ' by displaying the s i g n a l s on the s c r e e n of a c a t h o d e - r a y o s c i l l o s c o p e . U l t r a s o u n d s p r o d u c e d by young of 12 s p e c i e s of m y o m o r p h r o d e n t s when r e m o v e d daily f r o m the n e s t and p l a c e d on a b e n c h top, and by the adults of 8 s p e c i e s during s o c i a l i n t e r a c t i o n s , w e r e r e c o r d e d on m a g n e t i c tape at 37.5 i . p . s . u s i n g a P r e c i s i o n I n s t r u m e n t s 6100 t a p e - r e c o r d e r . T h i s equipment had a r e a s o n a b l y flat r e s p o n s e up to 100kHz. S p e c i m e n s i g n a l s w e r e then a n a l y s e d with a Kay M i s s i l y s e r 675 s o n o g r a p h by r e p l a y i n g t h e m at o n e - t e n t h of the o r i g i n a l r e c o r d i n g speed. The r e s u l t i n g s o n o g r a m t r a c e had a r e s o lution of about lkHz. The i n t e n s i t i e s of sounds p r o d u c e d by young a n i m a l s w e r e m e a s u r e d s e p a r a t e l y each day using a B r u e l and K j a e r c a l i b r a t e d 1/4in ( 6 . 3 m m ) m i c r o p h o n e type 4135 and displaying the s i g n a l s against a c a l i b r a t e d g r a t i c u l e on the s c r e e n of an o s c i l l o s c o p e . The m i c r o p h o n e w a s held v e r t i c a l l y 10cm above the b e n c h on which the young w e r e p l a c e d . The height in cm r e a c h e d by the m a j o r i t y of p u l s e s was noted and this r e a d i n g w a s then c o n v e r t e d to peak p r e s s u r e in both m i c r o b a r s and d e c i b e l s r e 2 x 10-1Obars r . m . s . Fig 1 shows the o s c i l l o s c o p e t r a c e and s o n o g r a m t r a c e of a s t y l i z e d pulse and i n d i c a t e s the p a r a m e t e r s m e a s u r e d .
AMPLITUDE PATTERNS
The amplitude v a r i e d o v e r the length of each pulse. G e n e r a l ly t h e r e was a g r a d u a l i n c r e a s e in amplitude at the beginning of a p u l s e and a g r a d u a l d e c r e a s e at the end of the p u l s e with s o m e fluctuations in b e t w e e n . Often a s o n o g r a m t r a c e showed one o r m o r e s h o r t b r e a k s along its length and it was not c l e a r w h e t h e r this r e p r e s e n t e d s e p a r a t e p u l s e s o r a single ULTRASONICS J a n u a r y 1970
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C R 0 trace
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f r e q u e n c y of 1 or 2kHz (Fig 4a) to l a r g e c y c l i c a l fluctuations of up to 70kHz o c c u r r i n g within 10ms and m a i n t a i n e d for up to 300ms (Fig 4b).
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Fig 1 Stylized pulse showing the p a r a m e t e r s measured: (a) height of s i g n a l p e a k for intensity m e a s u r e m e n t s (b) p u l s e length (c) initial f r e q u e n c y (d) terrnin:~l f r e quency (e) n m x i m u m frequency (g) m i n i m u m frequency (f) bandwidth (e-g).
Up to four i n s t a n t a n e o u s ' s t e p - l i k e ' f r e q u e n c y changes w e r e found within a single p u l s e and the f r e q u e n c y s t e p s r a n g e d f r o m 2kHz to 50kHz. T h e d i r e c t i o n of the f r e q u e n c y change, u p w a r d s or d o w n w a r d s , a p p e a r e d to be r a n d o m for the s m a l l e r changes but the l a r g e r s t e p s of 20-50kHz w e r e g e n e r a l l y in a d o w n w a r d s d i r e c t i o n . Often t h e s e s t e p s followed an upward f r e q u e n c y drift and the f r e q u e n c i e s on e i t h e r side of t h e s e j u m p s w e r e in or n e a r the s i m p l e r a t i o s 2 : 2 or 3 : 2 (Fig 5). This s u g g e s t e d that a h a r m o n i c jump had o c c u r r e d due to a change in mode of v i b r a t i o n . It is p o s s i b l e that the a n i m a l was i n c r e a s i n g the f r e q u e n c y of the call, but at the higher f r e q u e n c i e s , i n s t e a d of going higher, the note suddenly d r o p p e d to the octave below the note that was being a p p r o a c h e d . This can be d e m o n s t r a t e d in many wind i n s t r u m e n t s , for e x a m p l e the r e c o r d e r . H e r e , by blowing hard into the i n s t r u m e n t (overblowing) the octave above the n o r m a l pitch can be obtained. If, h o w e v e r , one a t t e m p t s to r u n up the s c a l e at the h i g h e r p i t c h e s , with i n s u f f i c i e n t airflow, the s y s t e m may ' c r a c k ' at one point, producing the octave below. This is due to a change of mode in the pipe but Brown 18 has shown that s i m i l a r f r e q u e n c y j u m p s also o c c u r in edge t o n e s without a coupled r e s o n a t o r , when the edge i s g r a d u a l l y withdrawn f r o m the s o u r c e of the jet of a i r that flows o v e r it.
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Fig 2 (a) P u l s e with s l o w drift in frequency and fluctuations in amplitude: s u b m i s s i v e adult rat. (b) Herring-bone appearance of sonogram trace of pulse f r o m adult h~mster.
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F ~ 3 (a) P u l s e with a slow frequency drift first upwards and then downwards: produced by a 15 day old wood m o u s e . (b) Step-like frequency changes in a pulse produced by a 9 day old field vole. p u l s e with d e c r e a s e s in i n t e n s i t y to below the working t h r e s hold of the a p p a r a t u s . F o r convenience, t r a c e s with b r e a k s of l e s s than 5ms and in which the f r e q u e n c y change p a t t e r n a p p e a r e d to be o t h e r w i s e continuous, w e r e c o n s i d e r e d a s a s i n g l e pulse, t h o s e with gaps of m o r e than 5ms w e r e c o n s i dered as separate pulses. A few p u l s e s began with a r a p i d i n c r e a s e in i n t e n s i t y . This was a c c o m p a n i e d by a s h o r t b r o a d , b a n d f r e q u e n c y s t r u c t u r e which may r e p r e s e n t the o n s e t t r a n s i e n t s . Some p u l s e s showed v e r y m a r k e d a m p l i t u d e fluctuations along t h e i r length (Fig 2a). In s e v e r a l of the p u l s e s p r o d u c e d by h a m s t e r s this was so r a p i d that the s o n o g r a m t r a c e had a h e r r i n g b o n e a p p e a r a n c e due to t h i s a m p l i t u d e modulation and c o n s e q u e n t r i n g i n g in the s o n o g r a p h f i l t e r s (Fig 2b).
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PATTERNS OF FREQUENCY CHANGE The f r e q u e n c y s e l d o m r e m a i n e d constant o v e r the length of a p u l s e but g e n e r a l l y changed at l e a s t once. The r a t e s of f r e quency change v a r i e d f r o m a l m o s t z e r o or continuous slow d r i f t s in f r e q u e n c y (Fig 3a) to i n s t a n t a n e o u s ' s t e p - l i k e ' f r e quency c h a n g e s (Fig 3b). F r e q u e n c y d r i f t s often o c c u r r e d as a d e c r e a s e in f r e q u e n c y o v e r m o s t of the length of the pulse, although t h e r e was s o m e t i m e s an initial s h o r t e r i n c r e a s e in f r e q u e n c y . M o r e rapid f r e q u e n c y fluctuations r a n g e d f r o m a few s m a l l changes in 28
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Fig 4 (a) P u l s e with s m a l l rapid frequency changes: produced during an a g g r e s s i v e encounter between adult mule African forest m i c e . (b) P u l s e with marked frequency fluctuations: produced by a 50 day old laboratory rat.
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s e r i e s . The sonograph t r a c e then b e c o m e s indistinct but l a t e r a t h i r d h a r m o n i c family can be d i s t i n g u i s h e d . The o r i g i n a l fundamental X is a p p a r e n t l y the 2nd h a r m o n i c of this s e r i e s , but the t r a c e of Y can no longer be followed. Again the sonograph t r a c e b e c o m e s i n d i s t i n c t but a little f u r t h e r on X e m e r g e s a s the p r o b a b l e fundamental of yet a n o t h e r h a r monic s e r i e s (with Y m i s s i n g ) at the end of the pulse. Not all the h a r m o n i c c o m p o n e n t s of each s e r i e s can be d i s t i n guished but sufficient a r e p r e s e n t to enable this i n t e r p r e t a tion to be made. O t h e r such p u l s e s can be i n t e r p r e t e d in a similar manner. O c c a s i o n a l l y s h o r t f o r m a n t s t r u c t u r e s 5 - 1 5 m s in duration w e r e found (Fig 7). T h e s e c o n s i s t e d of c l o s e l y s p a c e d h a r m o n i c s up to 5kHz a p a r t but the lower h a r m o n i c s and fundam e n t a l of this s e r i e s w e r e a b s e n t . This may indicate e i t h e r that a s e l e c t i v e f i l t e r i n g of the l o w e r h a r m o n i c s had o c c u r r e d , or that s i d e - b a n d s had b e e n p r o d u c e d due to amplitude c h a n g e s within a pulse c o n s i s t i n g of a single f r e q u e n c y c o m ponent. S e v e r a l s p e c i e s of c r i c e t i d r o d e n t s e m i t t e d w i d e - b a n d p u l s e s of up to 200ms d u r a t i o n with many a p p a r e n t l y h a r m o n i c a l l y u n r e l a t e d f r e q u e n c y c o m p o n e n t s (Fig 8). The f r e q u e n c y s p r e a d of t h e s e p u l s e s was b e t w e e n 10 and 60kHz. The lower f r e q u e n c y c o m p o n e n t s w e r e s o m e t i m e s within the human h e a r i n g range and they could be h e a r d a s soft huff-like sounds or a s c r e a k i n g sounds. O c c a s i o n a l l y one f r e q u e n c y c o m ponent was m o r e pronounced than the other.
DISCUSSION F i g 6 P u l s e with marked frequency fluctuations and t h r e e harmonic components. The sonograph trace i s drawn out into intense t a i l - l i k e formant structures. P r o duced by adult spiny mouse during m a t i n g b e h a v i o u r .
HARMONIC STRUCTURES The m a j o r i t y of p u l s e s c o n s i s t e d of a single but changing f r e quency component (Fig 3a). In s o m e p u l s e s the s e c o n d and t h i r d h a r m o n i c s w e r e p r e s e n t (at two and t h r e e t i m e s the fundamental frequency) and o c c a s i o n a l l y up to 12 h a r m o n i c c o m p o n e n t s 2-12kHz a p a r t could be c l e a r l y d i s t i n g u i s h e d . The fundamental was not always the m o s t i n t e n s e component. In many long p u l s e s that initially c o n s i s t e d of two or t h r e e harmonic components, other frequency components, either h a r m o n i c a l l y r e l a t e d to the f i r s t or not, a p p e a r e d for s h o r t i n t e r v a l s along the p u l s e . The p u l s e s p r o d u c e d by spiny m i c e during mating w e r e up to 300ms in duration and many showed m a r k e d c y c l i c a l fluctuations in f r e q u e n c y (Fig 6). T h e s e p u l s e s initially contained two o r t h r e e h a r m o n i c c o m p o n e n t s but often, at c e r t a i n f r e q u e n c i e s the s o n o g r a p h t r a c e b e c a m e i n t e n s i f i e d and d r a w n out for 2 - 3 m s into a ' t a i l ' (Fig 6). Such ' t a i l s ' a p p e a r to be f o r m a n t s t r u c t u r e s with a frequency s p r e a d of 2-30kHz. T h e s e t r a c e s w e r e not caused by the f i l t e r s of the s o n o g r a p h ringing a s they w e r e also s e e n when the s a m e p u l s e s w e r e a n a l y s e d using the m o r e highly damped b r o a d - b a n d f i l t e r s . F o r m a n t s t r u c t u r e s such a s t h e s e w e r e found during all p h a s e s of the modulation of the second h a r monic and s o m e t i m e s w e r e also p r e s e n t at the peaks of the fundamental. The g e r b i l s , ' m e r i o n e s l i b y c u s ' and ' m e r i o n e s unguiculatus, produced s o m e long p u l s e s , up to 200ms, which initially cons i s t e d of two to five h a r m o n i c s . O t h e r c o m p o n e n t s , a p p a r e n t ly h a r m o n i c a l l y r e l a t e d to the f i r s t set but which indicated a lower fundamental, a p p e a r e d f o r s h o r t d i s t a n c e s along the pulse. Noisy w i d e - b a n d s t r u c t u r e s s o m e t i m e s a l s o o c c u r r e d for a s h o r t duration and in many of t h e s e p u l s e s the lowest f r e q u e n c y c o m p o n e n t s w e r e within the human h e a r i n g range and sounded like high pitched ' c r e a k s f. A p o s s i b l e i n t e r p r e t a t i o n of one of t h e s e e x t r a o r d i n a r y p u l s e s i s given a s follows. The two f r e q u e n c y c o m p o n e n t s p r e s e n t at the beginning of the pulse a p p e a r to be the fundamental (X) and i t s second h a r m o n i c (Y). When o t h e r h a r m o n i c a l l y r e l a ted c o m p o n e n t s appear, X and Y can still be followed and can be i n t e r p r e t e d a s the 3rd and 6th h a r m o n i c s of the new
T h e r e a p p e a r e d to be no c l e a r cut d i f f e r e n c e s in the f r e quency p a t t e r n s of the u l t r a s o n i c p u l s e s produced by the diff e r e n t s p e c i e s studied. In g e n e r a l , h o w e v e r , the m u r i d rodents p r o d u c e d sounds with a single f r e q u e n c y component, w h e r e a s many of the c r i c e t i d r o d e n t s p r o d u c e d sounds with two o r m o r e f r e q u e n c y c o m p o n e n t s which, in g e r b i l s and v o l e s at l e a s t , w e r e often h a r m o n i c a l l y r e l a t e d . T h e r e was s o m e indication of a c o r r e l a t i o n b e t w e e n the n a t u r e of the u l t r a sounds and the social s i t u a t i o n s in which they w e r e e m i t t e d . Long p u l s e s with slow f r e q u e n c y d r i f t s w e r e c h a r a c t e r i s t i c of the c a l l s of young a n i m a l s i s o l a t e d on the b e n c h top and t h e s e g e n e r a l l y b e c a m e s h o r t e r , often h i g h e r in f r e q u e n c y and showed m o r e complex f r e q u e n c y p a t t e r n s with the inc r e a s i n g age of the young. In adults, s h o r t h i g h - p i t c h e d sounds of about 45kHz o r m o r e , with a v a r i e t y of f r e q u e n c y
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Fig 7 Short formant structures produced by a one day old rat.
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Fig 8 P u l s e with s e v e r a l apparently harmonically unrelated components: produced by an adult h~mster.
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c h a n g e s , w e r e a s s o c i a t e d with a g g r e s s i v e behaviour while long low f r e q u e n c y sounds with slow d r i f t s in f r e q u e n c y w e r e d e t e c t e d f r o m s u b m i s s i v e r a t s and p r o b a b l y f r o m f e m a l e h a m s t e r s on heat. During mating b e h a v i o u r , c a l l s of up to 700ms with long s t r e t c h e s of p r o n o u n c e d f r e q u e n c y f l u c t u a tions w e r e p r o d u c e d by l a b o r a t o r y r a t s , l a b o r a t o r y m i c e and spiny m i c e , but bank v o l e s e m i t t e d s h o r t e r p u l s e s with f r e quency d r i f t s . All the s p e c i e s which e m i t t e d u l t r a s o u n d s a l s o p r o d u c e d c r i e s that w e r e audible to man, g e n e r a l l y in r e s p o n s e to pain. So f a r t h e r e i s no d e f i n i t e a n s w e r to the q u e s t i o n of why u l t r a s o u n d s may be u s e d for c o m m u n i c a t i o n i n s t e a d of l o w e r f r e q u e n c y sounds. The actual s i z e of the a n i m a l s may be i m p o r t a n t in affecting the f r e q u e n c i e s of the s o u n d s produced. Man p r o d u c e s f u n d a m e n t a l f r e q u e n c i e s of about 66Hz to 1056Hz. Rodents a r e v e r y much s m a l l e r and so the length and m a s s of t h e i r vocal c o r d s and the s i z e of t h e i r vocal t r a c t s a r e a l s o s m a l l e r , giving t h e s e a n i m a l s the ability to p r o d u c e sounds of f r e q u e n c i e s h i g h e r than man can e i t h e r p r o d u c e or h e a r . The ' a u d i b l e ' c r i e s m e n t i o n e d above contained lower f r e q u e n c i e s of 4-6kHz; thus r o d e n t s have a much w i d e r bandwidth a v a i l a b l e to t h e m than h a s man. U l t r a s o u n d s do not a p p e a r to be of s u r v i v a l value to r o d e n t s by being outside the audible f r e q u e n c y r a n g e of t h e i r p r e d a t o r s . It has b e e n shown that c a t s can h e a r sounds of up to 70kHz 2° and it is p r o b a b l e that o t h e r m a m m a l i a n p r e d a t o r s can h e a r s i m i l a r f r e q u e n c i e s , although owls p r o b a b l y cannot h e a r s o u n d s above 20kHz. 21 A n o t h e r p o s s i b l e r e a s o n for the u s e of u l t r a s o u n d s by r o d e n t s i s t e n t a t i v e l y s u g g e s t e d h e r e . High f r e q u e n c y sounds a r e a b s o r b e d very rapidly in a i r 14 and b e c a u s e of t h e i r s h o r t w a v e - l e n g t h s , if e m i t t e d in the field, they would be r e f l e c t e d f r o m s m a l l o b j e c t s such a s b l a d e s of g r a s s and so s c a t t e r e d . Thus although u l t r a s o n i c s i g n a l s could be h e a r d d i s t i n c t l y within a few m e t r e s of t h e i r e m i s s i o n , f u r t h e r away they would be difficult both to h e a r and to l o c a l i s e . If, t h e r e f o r e , u l t r a s o u n d s a r e u s e d f o r c o m m u n i c a t i o n in the social b e haviour of r o d e n t s , they may allow social r e l a t i o n s h i p s to be e s t a b l i s h e d and m a i n t a i n e d b e t w e e n a n i m a l s n e a r to each o t h e r without unduly a d v e r t i s i n g t h e i r p r e s e n c e to p r e d a t o r s . This study of the production of u l t r a s o u n d s in r o d e n t s h a s r e v e a l e d many p o s s i b i l i t i e s f o r the use of u l t r a s o u n d among s m a l l m a m m a l s . F o r e x a m p l e , it s e e m s probable that the sounds p r o d u c e d by s u b m i s s i v e r a t s inhibits the a g g r e s s i o n of a d o m i n a n t a n i m a l and it is p o s s i b l e that the u l t r a s o u n d s p r o d u c e d by the m a l e during mating may affect the behaviour of the f e m a l e . But many q u e s t i o n s have b e e n r a i s e d . Some of t h e s e , such a s the a u d i t o r y s e n s i t i v i t i e s of s m a l l m a m m a l s a s r e v e a l e d by e l e c t r o p h y s i o l o g i c a l s t u d i e s , the motivation f o r the e m i s s i o n of t h e s e sounds in both young and adults, the p o s s s i b l e c o m m u n i c a t i o n value of t h e s e s i g n a l s and the m e c h a n i s m for t h e i r production, a r e at p r e s e n t being i n v e s t i gated by v a r i o u s m e m b e r s of this l a b o r a t o r y . It i s hoped that t h e s e widely v a r y i n g s t u d i e s will r e v e a l m o r e of the ability of r o d e n t s both to p r o d u c e and to use u l t r a s o n i c signals. ACKNOWLEDGEMENTS T h i s r e s e a r c h w a s c a r r i e d out a s p a r t of the work for the d e g r e e of Doctor of P h i l o s o p h y at the U n i v e r s i t y of London. The work was s p o n s o r e d in p a r t by the A i r F o r c e Office of Scientific R e s e a r c h to Dr J. D. Pye. I am indebted to Dr J. D. P y e for much helpful advice and c r i t i c i s m and to Mr S. M. Godson for maintaining the equipment.
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Griffin, D . R . ' L i s t e n i n g in the d a r k ' , Yale U n i v e r s i t y P r e s s , New Haven (1958).
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A n d e r s o n , J . W . 'The production of u l t r a s o n i c sounds by l a b o r a t o r y r a t s and o t h e r m a m m a l s ' , Science. Vol 119 (1954), p 808
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Zippelius, H. M. and Schleidt, W . M . ' U l t r a s c h a l - l a u t e bei jungen M~usen ', N a t u r w i s s e n s c h a f t e n , Vol 43, (1956). p 502
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Noirot, E. ' U l t r a s o n s et c o m p o r t e m e n t s m a t e r n e l s chez l e s petits r o n g e u r s ' , A n n a l e s de la Soci~t~oRoyale Zoologique de B e l g i q u e , V o l 95, (1965), p 47
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Dice, L. and Barto, E. 'The ability of m i c e of the g e n u s P e r o m y s c u s to h e a r u l t r a s o n i c sounds'~ Science Vol 116. (1952), p 110
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Pye, J . D . 'Synthesizing the w a v e f o r m s of b a t s ' p u l s e s ' , Animal Sonar S y s t e m s : Biology and B i o n o m i c s , Symposium at F r a s c a t i 1966. Ed. R.-G. Busnel. L a b o r a t o i r e de P h y s i o l o g i c Acoustique, J o u y - e n - J o s a s . F r a n c e (1967)
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Griffin, D . R . ' S u p e r s o n i c c r i e s of b a t s ', Nature (London), Vol 158, (1946). 46
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Pye, J. D . a n d Flinn, M. 'Equipment f o r detecting a n i m a l u l t r a s o u n d ' , U l t r a s o n i c s , Vol 2 (1964), p 23
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Evans, E . F . ' C o r t i c a l r e p r e s e n t a t i o n in h e a r i n g m e c h a n i s m s in v e r t e b r a t e s ' , Ciba Foundation Symposium. J. and A. Churchill Ltd., London (1968)
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Payne, R. 'Acoustic o r i e n t a t i o n of p r e y by the b a r n owl Tyro alba ', T e c h n i c a l r e p o r t no. 1, Q u a r t e r m a s t e r r e s e a r c h and e n g i n e e r i n g c o m m a n d , US A r m y Office of Naval R e s e a r c h (1961)
'Animal s o n a r in air ', U l t r a s o n i c s , Vol 6 (1968)
A b r i e f a c c o u n t i s g i v e n of the d i s c o v e r y of the u l t r a s o u n d s p r o d u c e d b y r o d e n t s and the s i t u a t i o n s in which t h e y a r e e m i t t e d . T h e e q u i p m e n t u s e d to s t u d y t h e s e s i g n a l s i s d e s c r i b e d b r i e f l y . R o d e n t s e m i t a wide v a r i e t y of u l t r a s o n i c s i g n a l s and while t h e r e i s s o m e e v i d e n c e t h a t t h e y can h e a r t h e s e s o u n d s , little i s known of how t h e y a r e p r o d u c e d . T h e p h y s i c a l c h a r a c t e r i s t i c s of the s i g n a l s t h e m s e l v e s a r e t h e r e f o r e of g r e a t i n t e r e s t a s t h e y m a y g i v e s o m e c l u e s a s to the m e c h a n i s m of u l t r a s o u n d p r o d u c t i o n . A d e s c r i p t i o n i s give
of the d i f f e r e n t h a r m o n i c s p e c t r a found in t h e s e u l t r a s o n i c s i g n a l s and the v a r i a t i o n s in a m p l i t u d e and p a t t e r n s of f r e ~ q u e n c y c h a n g e t h a t o c c u r within t h e s e s p e c t r a . T h e r e l a t i o n s h i p b e t w e e n the p h y s i c a l c h a r a c t e r i s t i c s of the s i g n a l s and the s i t u a t i o n s in which t h e y a r e e m i t t e d i s d i s c u s s e d , t o g e t h e r with p o s s i b l e r e a s o n s for the u s e of s u c h high f r e q u e n c y s o u n d s . F i n a l l y the p r o b l e m s that h a v e a r i s e n out of t h i s work a r e r e v i e w e d and f u t u r e l i n e s of s t u d y a r e i n d i c a t e d .
It h a s b e e n known for s o m e 30 y e a r s t h a t b a t s p r o d u c e u l t r a sonic s i g n a l s 1 , 2, but it h a s r e c e n t l y b e c o m e known that m a n y r o d e n t s a l s o e m i t u l t r a s o u n d s . In 1954 A n d e r s o n 3 d e t e c t e d ' p u r e t o n e s ' of 23-38kHz f r o m a d u l t r a t s alone in t h e i r c a g e s and l a t e r Z i p p e l i u s and Schleidt (1956) 4 and a l s o N o i r o t (1965) 5 r e p o r t e d t h a t w h e n the young of s e v e r a l s p e c i e s of r o d e n t s w e r e r e m o v e d f r o m the n e s t and i s o l a t e d on a b e n c h top, t h e y e m i t t e d u l t r a s o n i c c r i e s . T h e s e c a l l s w e r e p r o d u c e d at l e a s t until the e y e s of t h e young o p e n e d at the a g e of about 10-15 d a y s . T h e a u t h o r s s u g g e s t e d t h e y w e r e d i s t r e s s c a l l s , which w e r e e m i t t e d by the young u n d e r c o n d i t i o n s of cold a n d h u n g e r and which s e r v e d to e l i c i t the r e t r i e v i n g r e s p o n s e of the m o t h e r a n i m a l and to guide h e r to s t r a y young, out of the nest.
and it w a s found that s h o r t u l t r a s o u n d s , g e n e r a l l y 1 0 - 6 0 m s long at f r e q u e n c i e s of about 50kHz, w e r e often p r o d u c e d during a g g r e s s i v e behaviour. Many s u b m i s s i v e animals prod u c e d long s o u n d s of 22-30kHz which l a s t e d f o r 2 0 0 - 3 4 0 0 m s and could be c o r r e l a t e d with the i r r e g u l a r r e s p i r a t i o n s of the submissive animals.
T h e p r e s e n t s t u d y b e g a n a s a c o m p a r a t i v e s u r v e y of the p r o d u c t i o n of u l t r a s o u n d b y the young of s m a l l m a m m a l s . T h e e x t e n t of the s u r v e y w a s l i m i t e d to the a n i m a l s t h a t could b e a c q u i r e d in t h i s c o u n t r y e i t h e r by live t r a p p i n g B r i t i s h s p e c i e s in the field or by o b t a i n i n g f o r e i g n s p e c i e s f r o m o t h e r r e s e a r c h i n s t i t u t i o n s . A r e c e n t t r i p to E a s t A f r i c a e x p a n d e d the s c o p e of the s u r v e y . So f a r 39 s p e c i e s , i n c l u d i n g 25 s p e c i e s of r o d e n t s , 3 s p e c i e s of p r i m a t e s and 7 s p e c i e s of i n s e c t i v o r e s h a v e b e e n o b s e r v e d in one w a y or a n o t h e r . T h e a n i m a l s t h a t w e r e s t u d i e d in d e t a i l b e l o n g e d to e i t h e r of two f a m i l i e s of the m y o m o r p h g r o u p of r o d e n t s . T h e s e f a m i l i e s w e r e the C r i c e t i d a e w h i c h i n c l u d e s h a m s t e r s , v o l e s and g e r b i l s and the M u r i d a e which i n c l u d e s r a t s , m i c e and t h e i r a l l i e s . T h e p h e n o m e n o n of u l t r a s o u n d e m i s s i o n by young w a s c o n f i r m e d for a l l eight s p e c i e s of C r i c e t i d a e a n d for the s e v e n s p e c i e s of M u r i d a e of which l i t t e r s w e r e e x a m i n e d . W h e r e p o s s i b l e the s i g n a l s w e r e s t u d i e d daily f r o m b i r t h o n w a r d s so that any c h a n g e s with a g e could be d e t e r m i n e d . D u r i n g the c o u r s e of t h i s w o r k it w a s found that u l t r a s o u n d s could be e l i c i t e d f r o m r a t s , long a f t e r the e y e s of the young h a d o p e n e d a n d well into adult life, b y h a n d l i n g the a n i m a l s 6. T h i s i n v o l v e d r o l l i n g the r a t s on to t h e i r b a c k s and r e s t r a i n ing t h e m in a p o s t u r e s i m i l a r to that of the s u b m i s s i v e p o s t u r e of a d u l t s t o w a r d s a n a g g r e s s o r 7. S u b s e q u e n t l y a g g r e s s i v e and s u b m i s s i v e b e h a v i o u r of adult l a b o r a t o r y r a t s w a s s t u d i e d
M i s s G. D. Sewell, D e p a r t m e n t of Zoology, U n i v e r s i t y of London, K i n g ' s C o l l e g e , Strand, London. W.C .2.
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ULTRASONICS J a n u a r y 1970
Various other aspects of social behaviour in rodents were then studied. Ultrasounds were detected during aggressive behaviour in several species (see Table 1) and they appeared to be produced by the attacking animals. In gerbils, audible 'retaliation' cries with pronounced ultrasonic components were also emitted, apparently by the subordinate animal as he fended off the attacker. Fully submissive postures were seen only in rats. Ultrasonic signals were detected during mating in all the species in which mating behaviour was observed. Generally these signals could be correlated with the movements of the male but in hamsters,ultrasounds were detected when a female which was on heat nosed other hamsters, either male or female, which were introduced singly into her cage. Ultrasounds were also detected in situations where the a n i m a l s a p p e a r e d to b e e x p l o r i n g - - f o r e x a m p l e , when adult wood m i c e e m e r g e d f r o m the n e s t a f t e r the c a g e had b e e n d i s t u r b e d and a l s o 2 - 3 r a i n a f t e r they had bee,~ put into a new c a g e . S i g n a l s w e r e p r o d u c e d by l a c t a t i n g f e m a l e s of t h r e e s p e c i e s a f t e r t h e i r l i t t e r s had b e e n r e m o v e d f r o m the n e s t s . In yet a n o t h e r s i t u a t i o n , v o c a l s i g n a l s w e r e p r o d u c e d a s a l a c t a t i n g f e m a l e g e r b i l t h u m p e d one hind foot on the g r o u n d after being disturbed. These may r e p r e s e n t warning signals. U l t r a s o u n d s a r e t h u s p r o d u c e d in a wide v a r i e t y of s i t u a t i o n s by r o d e n t s , but if t h e y a r e u s e d for c o m m u n i c a t i o n , the a n i m a l s m u s t be able to h e a r t h e m and t h e r e i s s o m e e v i d e n c e for t h i s . It h a s b e e n r e p o r t e d f r o m v a r i o u s b e h a v i o u r a l r e a c t i o n s that s e v e r a l s p e c i e s of m y o m o r p h r o d e n t s c a n h e a r well into the u l t r a s o n i c r a n g e l o . R e c e n t l y , R a l l s 1~ h a s u s e d e l e c t r o p h y s i o l o g i c a l t e c h n i q u e s to s t u d y the a u d i t o r y s e n s i t i v i t i e s of wild h o u s e m i c e , two s t r a i n s of l a b o r a t o r y m i c e and two s p e c i e s of d e e r m i c e . She h a s shown that the young of t h e s e a n i m a l s at l e a s t a r e s e n s i t i v e to f r e q u e n c i e s up to 70-80kHz. T h e lowest t h r e s h o l d s for a d u l t s w e r e b e t w e e n 10kHz and 30-40kHz in d e e r m i c e and at about 20kHz in wild h o u s e m i c e . In the s t r a i n s of l a b o r a t o r y m i c e , h o w e v e r , s h e found t h a t the a u d i t o r y s e n s i t i v i t i e s to f r e q u e n c i e s above 7-12kHz d e c r e a s e d v e r y r a p i d l y with a g e .
T a b l e 1 O c c u r r e n c e of u l t r a s o u n d e m i s s i o n by r o d e n t s Colloquial name
F o r m a l name
Young
Aggression
Mating
Bank vole
Clethrionomys glareolus
Yes
?
Yes
Other
Family Cricetidae
F i e l d vole
Microtus agrestis
Yes
No
--
Hamster
Mesocricetus auratus
Yes
No
Yes
Mongolian gerbil
Meriones unguiculatus
Yes
--
--
Libyan gerbil
Meriones libycus
Yes
Yes
--
retaliation*
Sand rat or gerbil
Gerbillus species
Yes
Yes
--
retaliation*
Deer mouse
Peromyscus species
Yes*
No
Yes
Steppe lemming
Lagurus lagurus
Yes
No
Yes
Rattus n o r v e g i c u s
Yes
Yes
Yes
Rattus norvegicus
--
Yes
--
Mice: (a) Albino laboratory strain (b) Grey laboratory strain
Mus musculus Mus musculus
Yes Yes
No No
Yes Yes
Minute mouse
Mus minutoides
Yes
No
Yes
Wood mouse
Apodemus sylvaticus
Yes
--
--
exploratory
Spiny mouse
Acomys caharinus
Yes
?
Yes
lactating f e m a l e
Multimammate mouse
Praomys natalensis
Yes
No
Yes
Family Muridae
Rats: (a) L a b o r a t o r y s t r a i n s (b) Wild strain
African forest mouse
Thamnomys species
Yes
Yes
--
Kusu rat
Arvicanthis niloticus
--
Yes
--
submission submission lactating f e m a l e
* = s o m e s i g n a l s with audible and u l t r a s o n i c c o m p o n e n t s
While little i s known of the ability of r o d e n t s to h e a r u l t r a sounds, even l e s s i s known of the m e c h a n i s m by which they a r e p r o d u c e d . So the s t r u c t u r e of the sounds t h e m s e l v e s i s of i n t e r e s t a s it may give s o m e c l u e s a s to the m e c h a n i s m involved. B a t s p r o d u c e u l t r a s o u n d s of 0 . 2 5 - 1 0 0 m s duration with i n t e n s i t i e s of up to 120dB r e 0. 0002~zbar r . m . s . , m e a s u r e d at 10cm f r o m the a n i m a l . T h e s e s i g n a l s may have one o r m o r e h a r m o n i c c o m p o n e n t s and a r e p r o d u c e d in the larynx. 12 P y e 13 has s u g g e s t e d that the l a r y n g e a l wave f o r m i s n o n s i n u s o i d a l and that the h a r m o n i c s it contains a r e influenced b e f o r e e m i s s i o n by the vocal t r a c t s acting a s s i m p l e r e s o n a n c e f i l t e r s . T h i s , he points out, i s c o m p a r a b l e to the phonetic t h e o r y of human vowel production, but in b a t s only one r e s o n a n t peak o r f o r m a t n e e d s to be p o s t u l a t e d i n s t e a d of the four p r e s e n t in human vowel sounds. Griffin 14 adopted the w o r d ' p u l s e ' in connection with the u l t r a s o u n d s p r o d u c e d by b a t s to denote a single u l t r a s o n i c c r y . This word has b e e n u s e d to m e a n many d i f f e r e n t p h e n o m e n a l 5 , but in this account of the u l t r a s o u n d s p r o d u c e d by r o d e n t s the w o r d ' p u l s e ' will be u s e d for a single u l t r a s o n i c sound. R o d e n t s p r o d u c e a wide v a r i e t y of u l t r a s o n i c p u l s e s which r a n g e in d u r a t i o n f r o m 2ms to 3400ms. V a r i a t i o n s in amplitude o c c u r within the sounds and peak i n t e n s i t i e s of up to 106dB have b e e n r e c o r d e d at 10cm. The f r e q u e n c i e s e m i t t e d range f r o m 20kHz (the conventional lower limit of the t e r m ' u l t r a s o u n d ' ) to 150kHz (the p r a c t i c a l upper limit of the r e c o r d i n g a p p a r a t u s ) . Within t h e s e l i m i t s a wide v a r i e t y of f r e q u e n c y s p e c t r a a r e found. M o s t of the sounds that w e r e studied c o n s i s t e d of a single f r e q u e n c y component, but s o m e contained s e v e r a l h a r m o n i c a l l y r e l a t e d components while o t h e r s c o n s i s t e d of many c l o s e l y s p a c e d and a p p a r e n t l y h a r m o n i c a l l y u n r e l a t e d c o m p o n e n t s . O c c a s i o n a l l y all t h e s e t h r e e f r e q u e n c y s t r u c t u r e s w e r e found in one p u l s e and w i t h in any one of them the f r e q u e n c y level often changed in a v a r i e t y of ways, to be c o n s i d e r e d l a t e r . All t h e s e d i f f e r e n t p h e n o m e n a m u s t be accounted for by any m e c h a n i s m that i s s u g g e s t e d for the p r o d u c t i o n of u l t r a s o u n d s by r o d e n t s .
METHOD OF STUDY During this study, u l t r a s o u n d was m o n i t o r e d 16,17 'audibly' using a tunable s u p e r h e t e r o d y n e ' b a t - d e t e c t o r ' and ' v i s i b l y ' by displaying the s i g n a l s on the s c r e e n of a c a t h o d e - r a y o s c i l l o s c o p e . U l t r a s o u n d s p r o d u c e d by young of 12 s p e c i e s of m y o m o r p h r o d e n t s when r e m o v e d daily f r o m the n e s t and p l a c e d on a b e n c h top, and by the adults of 8 s p e c i e s during s o c i a l i n t e r a c t i o n s , w e r e r e c o r d e d on m a g n e t i c tape at 37.5 i . p . s . u s i n g a P r e c i s i o n I n s t r u m e n t s 6100 t a p e - r e c o r d e r . T h i s equipment had a r e a s o n a b l y flat r e s p o n s e up to 100kHz. S p e c i m e n s i g n a l s w e r e then a n a l y s e d with a Kay M i s s i l y s e r 675 s o n o g r a p h by r e p l a y i n g t h e m at o n e - t e n t h of the o r i g i n a l r e c o r d i n g speed. The r e s u l t i n g s o n o g r a m t r a c e had a r e s o lution of about lkHz. The i n t e n s i t i e s of sounds p r o d u c e d by young a n i m a l s w e r e m e a s u r e d s e p a r a t e l y each day using a B r u e l and K j a e r c a l i b r a t e d 1/4in ( 6 . 3 m m ) m i c r o p h o n e type 4135 and displaying the s i g n a l s against a c a l i b r a t e d g r a t i c u l e on the s c r e e n of an o s c i l l o s c o p e . The m i c r o p h o n e w a s held v e r t i c a l l y 10cm above the b e n c h on which the young w e r e p l a c e d . The height in cm r e a c h e d by the m a j o r i t y of p u l s e s was noted and this r e a d i n g w a s then c o n v e r t e d to peak p r e s s u r e in both m i c r o b a r s and d e c i b e l s r e 2 x 10-1Obars r . m . s . Fig 1 shows the o s c i l l o s c o p e t r a c e and s o n o g r a m t r a c e of a s t y l i z e d pulse and i n d i c a t e s the p a r a m e t e r s m e a s u r e d .
AMPLITUDE PATTERNS
The amplitude v a r i e d o v e r the length of each pulse. G e n e r a l ly t h e r e was a g r a d u a l i n c r e a s e in amplitude at the beginning of a p u l s e and a g r a d u a l d e c r e a s e at the end of the p u l s e with s o m e fluctuations in b e t w e e n . Often a s o n o g r a m t r a c e showed one o r m o r e s h o r t b r e a k s along its length and it was not c l e a r w h e t h e r this r e p r e s e n t e d s e p a r a t e p u l s e s o r a single ULTRASONICS J a n u a r y 1970
27
C R 0 trace
,
f r e q u e n c y of 1 or 2kHz (Fig 4a) to l a r g e c y c l i c a l fluctuations of up to 70kHz o c c u r r i n g within 10ms and m a i n t a i n e d for up to 300ms (Fig 4b).
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b Time [ m s ]
Fig 1 Stylized pulse showing the p a r a m e t e r s measured: (a) height of s i g n a l p e a k for intensity m e a s u r e m e n t s (b) p u l s e length (c) initial f r e q u e n c y (d) terrnin:~l f r e quency (e) n m x i m u m frequency (g) m i n i m u m frequency (f) bandwidth (e-g).
Up to four i n s t a n t a n e o u s ' s t e p - l i k e ' f r e q u e n c y changes w e r e found within a single p u l s e and the f r e q u e n c y s t e p s r a n g e d f r o m 2kHz to 50kHz. T h e d i r e c t i o n of the f r e q u e n c y change, u p w a r d s or d o w n w a r d s , a p p e a r e d to be r a n d o m for the s m a l l e r changes but the l a r g e r s t e p s of 20-50kHz w e r e g e n e r a l l y in a d o w n w a r d s d i r e c t i o n . Often t h e s e s t e p s followed an upward f r e q u e n c y drift and the f r e q u e n c i e s on e i t h e r side of t h e s e j u m p s w e r e in or n e a r the s i m p l e r a t i o s 2 : 2 or 3 : 2 (Fig 5). This s u g g e s t e d that a h a r m o n i c jump had o c c u r r e d due to a change in mode of v i b r a t i o n . It is p o s s i b l e that the a n i m a l was i n c r e a s i n g the f r e q u e n c y of the call, but at the higher f r e q u e n c i e s , i n s t e a d of going higher, the note suddenly d r o p p e d to the octave below the note that was being a p p r o a c h e d . This can be d e m o n s t r a t e d in many wind i n s t r u m e n t s , for e x a m p l e the r e c o r d e r . H e r e , by blowing hard into the i n s t r u m e n t (overblowing) the octave above the n o r m a l pitch can be obtained. If, h o w e v e r , one a t t e m p t s to r u n up the s c a l e at the h i g h e r p i t c h e s , with i n s u f f i c i e n t airflow, the s y s t e m may ' c r a c k ' at one point, producing the octave below. This is due to a change of mode in the pipe but Brown 18 has shown that s i m i l a r f r e q u e n c y j u m p s also o c c u r in edge t o n e s without a coupled r e s o n a t o r , when the edge i s g r a d u a l l y withdrawn f r o m the s o u r c e of the jet of a i r that flows o v e r it.
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Fig 2 (a) P u l s e with s l o w drift in frequency and fluctuations in amplitude: s u b m i s s i v e adult rat. (b) Herring-bone appearance of sonogram trace of pulse f r o m adult h~mster.
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F ~ 3 (a) P u l s e with a slow frequency drift first upwards and then downwards: produced by a 15 day old wood m o u s e . (b) Step-like frequency changes in a pulse produced by a 9 day old field vole. p u l s e with d e c r e a s e s in i n t e n s i t y to below the working t h r e s hold of the a p p a r a t u s . F o r convenience, t r a c e s with b r e a k s of l e s s than 5ms and in which the f r e q u e n c y change p a t t e r n a p p e a r e d to be o t h e r w i s e continuous, w e r e c o n s i d e r e d a s a s i n g l e pulse, t h o s e with gaps of m o r e than 5ms w e r e c o n s i dered as separate pulses. A few p u l s e s began with a r a p i d i n c r e a s e in i n t e n s i t y . This was a c c o m p a n i e d by a s h o r t b r o a d , b a n d f r e q u e n c y s t r u c t u r e which may r e p r e s e n t the o n s e t t r a n s i e n t s . Some p u l s e s showed v e r y m a r k e d a m p l i t u d e fluctuations along t h e i r length (Fig 2a). In s e v e r a l of the p u l s e s p r o d u c e d by h a m s t e r s this was so r a p i d that the s o n o g r a m t r a c e had a h e r r i n g b o n e a p p e a r a n c e due to t h i s a m p l i t u d e modulation and c o n s e q u e n t r i n g i n g in the s o n o g r a p h f i l t e r s (Fig 2b).
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PATTERNS OF FREQUENCY CHANGE The f r e q u e n c y s e l d o m r e m a i n e d constant o v e r the length of a p u l s e but g e n e r a l l y changed at l e a s t once. The r a t e s of f r e quency change v a r i e d f r o m a l m o s t z e r o or continuous slow d r i f t s in f r e q u e n c y (Fig 3a) to i n s t a n t a n e o u s ' s t e p - l i k e ' f r e quency c h a n g e s (Fig 3b). F r e q u e n c y d r i f t s often o c c u r r e d as a d e c r e a s e in f r e q u e n c y o v e r m o s t of the length of the pulse, although t h e r e was s o m e t i m e s an initial s h o r t e r i n c r e a s e in f r e q u e n c y . M o r e rapid f r e q u e n c y fluctuations r a n g e d f r o m a few s m a l l changes in 28
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Fig 4 (a) P u l s e with s m a l l rapid frequency changes: produced during an a g g r e s s i v e encounter between adult mule African forest m i c e . (b) P u l s e with marked frequency fluctuations: produced by a 50 day old laboratory rat.
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s e r i e s . The sonograph t r a c e then b e c o m e s indistinct but l a t e r a t h i r d h a r m o n i c family can be d i s t i n g u i s h e d . The o r i g i n a l fundamental X is a p p a r e n t l y the 2nd h a r m o n i c of this s e r i e s , but the t r a c e of Y can no longer be followed. Again the sonograph t r a c e b e c o m e s i n d i s t i n c t but a little f u r t h e r on X e m e r g e s a s the p r o b a b l e fundamental of yet a n o t h e r h a r monic s e r i e s (with Y m i s s i n g ) at the end of the pulse. Not all the h a r m o n i c c o m p o n e n t s of each s e r i e s can be d i s t i n guished but sufficient a r e p r e s e n t to enable this i n t e r p r e t a tion to be made. O t h e r such p u l s e s can be i n t e r p r e t e d in a similar manner. O c c a s i o n a l l y s h o r t f o r m a n t s t r u c t u r e s 5 - 1 5 m s in duration w e r e found (Fig 7). T h e s e c o n s i s t e d of c l o s e l y s p a c e d h a r m o n i c s up to 5kHz a p a r t but the lower h a r m o n i c s and fundam e n t a l of this s e r i e s w e r e a b s e n t . This may indicate e i t h e r that a s e l e c t i v e f i l t e r i n g of the l o w e r h a r m o n i c s had o c c u r r e d , or that s i d e - b a n d s had b e e n p r o d u c e d due to amplitude c h a n g e s within a pulse c o n s i s t i n g of a single f r e q u e n c y c o m ponent. S e v e r a l s p e c i e s of c r i c e t i d r o d e n t s e m i t t e d w i d e - b a n d p u l s e s of up to 200ms d u r a t i o n with many a p p a r e n t l y h a r m o n i c a l l y u n r e l a t e d f r e q u e n c y c o m p o n e n t s (Fig 8). The f r e q u e n c y s p r e a d of t h e s e p u l s e s was b e t w e e n 10 and 60kHz. The lower f r e q u e n c y c o m p o n e n t s w e r e s o m e t i m e s within the human h e a r i n g range and they could be h e a r d a s soft huff-like sounds or a s c r e a k i n g sounds. O c c a s i o n a l l y one f r e q u e n c y c o m ponent was m o r e pronounced than the other.
DISCUSSION F i g 6 P u l s e with marked frequency fluctuations and t h r e e harmonic components. The sonograph trace i s drawn out into intense t a i l - l i k e formant structures. P r o duced by adult spiny mouse during m a t i n g b e h a v i o u r .
HARMONIC STRUCTURES The m a j o r i t y of p u l s e s c o n s i s t e d of a single but changing f r e quency component (Fig 3a). In s o m e p u l s e s the s e c o n d and t h i r d h a r m o n i c s w e r e p r e s e n t (at two and t h r e e t i m e s the fundamental frequency) and o c c a s i o n a l l y up to 12 h a r m o n i c c o m p o n e n t s 2-12kHz a p a r t could be c l e a r l y d i s t i n g u i s h e d . The fundamental was not always the m o s t i n t e n s e component. In many long p u l s e s that initially c o n s i s t e d of two or t h r e e harmonic components, other frequency components, either h a r m o n i c a l l y r e l a t e d to the f i r s t or not, a p p e a r e d for s h o r t i n t e r v a l s along the p u l s e . The p u l s e s p r o d u c e d by spiny m i c e during mating w e r e up to 300ms in duration and many showed m a r k e d c y c l i c a l fluctuations in f r e q u e n c y (Fig 6). T h e s e p u l s e s initially contained two o r t h r e e h a r m o n i c c o m p o n e n t s but often, at c e r t a i n f r e q u e n c i e s the s o n o g r a p h t r a c e b e c a m e i n t e n s i f i e d and d r a w n out for 2 - 3 m s into a ' t a i l ' (Fig 6). Such ' t a i l s ' a p p e a r to be f o r m a n t s t r u c t u r e s with a frequency s p r e a d of 2-30kHz. T h e s e t r a c e s w e r e not caused by the f i l t e r s of the s o n o g r a p h ringing a s they w e r e also s e e n when the s a m e p u l s e s w e r e a n a l y s e d using the m o r e highly damped b r o a d - b a n d f i l t e r s . F o r m a n t s t r u c t u r e s such a s t h e s e w e r e found during all p h a s e s of the modulation of the second h a r monic and s o m e t i m e s w e r e also p r e s e n t at the peaks of the fundamental. The g e r b i l s , ' m e r i o n e s l i b y c u s ' and ' m e r i o n e s unguiculatus, produced s o m e long p u l s e s , up to 200ms, which initially cons i s t e d of two to five h a r m o n i c s . O t h e r c o m p o n e n t s , a p p a r e n t ly h a r m o n i c a l l y r e l a t e d to the f i r s t set but which indicated a lower fundamental, a p p e a r e d f o r s h o r t d i s t a n c e s along the pulse. Noisy w i d e - b a n d s t r u c t u r e s s o m e t i m e s a l s o o c c u r r e d for a s h o r t duration and in many of t h e s e p u l s e s the lowest f r e q u e n c y c o m p o n e n t s w e r e within the human h e a r i n g range and sounded like high pitched ' c r e a k s f. A p o s s i b l e i n t e r p r e t a t i o n of one of t h e s e e x t r a o r d i n a r y p u l s e s i s given a s follows. The two f r e q u e n c y c o m p o n e n t s p r e s e n t at the beginning of the pulse a p p e a r to be the fundamental (X) and i t s second h a r m o n i c (Y). When o t h e r h a r m o n i c a l l y r e l a ted c o m p o n e n t s appear, X and Y can still be followed and can be i n t e r p r e t e d a s the 3rd and 6th h a r m o n i c s of the new
T h e r e a p p e a r e d to be no c l e a r cut d i f f e r e n c e s in the f r e quency p a t t e r n s of the u l t r a s o n i c p u l s e s produced by the diff e r e n t s p e c i e s studied. In g e n e r a l , h o w e v e r , the m u r i d rodents p r o d u c e d sounds with a single f r e q u e n c y component, w h e r e a s many of the c r i c e t i d r o d e n t s p r o d u c e d sounds with two o r m o r e f r e q u e n c y c o m p o n e n t s which, in g e r b i l s and v o l e s at l e a s t , w e r e often h a r m o n i c a l l y r e l a t e d . T h e r e was s o m e indication of a c o r r e l a t i o n b e t w e e n the n a t u r e of the u l t r a sounds and the social s i t u a t i o n s in which they w e r e e m i t t e d . Long p u l s e s with slow f r e q u e n c y d r i f t s w e r e c h a r a c t e r i s t i c of the c a l l s of young a n i m a l s i s o l a t e d on the b e n c h top and t h e s e g e n e r a l l y b e c a m e s h o r t e r , often h i g h e r in f r e q u e n c y and showed m o r e complex f r e q u e n c y p a t t e r n s with the inc r e a s i n g age of the young. In adults, s h o r t h i g h - p i t c h e d sounds of about 45kHz o r m o r e , with a v a r i e t y of f r e q u e n c y
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Fig 7 Short formant structures produced by a one day old rat.
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Fig 8 P u l s e with s e v e r a l apparently harmonically unrelated components: produced by an adult h~mster.
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c h a n g e s , w e r e a s s o c i a t e d with a g g r e s s i v e behaviour while long low f r e q u e n c y sounds with slow d r i f t s in f r e q u e n c y w e r e d e t e c t e d f r o m s u b m i s s i v e r a t s and p r o b a b l y f r o m f e m a l e h a m s t e r s on heat. During mating b e h a v i o u r , c a l l s of up to 700ms with long s t r e t c h e s of p r o n o u n c e d f r e q u e n c y f l u c t u a tions w e r e p r o d u c e d by l a b o r a t o r y r a t s , l a b o r a t o r y m i c e and spiny m i c e , but bank v o l e s e m i t t e d s h o r t e r p u l s e s with f r e quency d r i f t s . All the s p e c i e s which e m i t t e d u l t r a s o u n d s a l s o p r o d u c e d c r i e s that w e r e audible to man, g e n e r a l l y in r e s p o n s e to pain. So f a r t h e r e i s no d e f i n i t e a n s w e r to the q u e s t i o n of why u l t r a s o u n d s may be u s e d for c o m m u n i c a t i o n i n s t e a d of l o w e r f r e q u e n c y sounds. The actual s i z e of the a n i m a l s may be i m p o r t a n t in affecting the f r e q u e n c i e s of the s o u n d s produced. Man p r o d u c e s f u n d a m e n t a l f r e q u e n c i e s of about 66Hz to 1056Hz. Rodents a r e v e r y much s m a l l e r and so the length and m a s s of t h e i r vocal c o r d s and the s i z e of t h e i r vocal t r a c t s a r e a l s o s m a l l e r , giving t h e s e a n i m a l s the ability to p r o d u c e sounds of f r e q u e n c i e s h i g h e r than man can e i t h e r p r o d u c e or h e a r . The ' a u d i b l e ' c r i e s m e n t i o n e d above contained lower f r e q u e n c i e s of 4-6kHz; thus r o d e n t s have a much w i d e r bandwidth a v a i l a b l e to t h e m than h a s man. U l t r a s o u n d s do not a p p e a r to be of s u r v i v a l value to r o d e n t s by being outside the audible f r e q u e n c y r a n g e of t h e i r p r e d a t o r s . It has b e e n shown that c a t s can h e a r sounds of up to 70kHz 2° and it is p r o b a b l e that o t h e r m a m m a l i a n p r e d a t o r s can h e a r s i m i l a r f r e q u e n c i e s , although owls p r o b a b l y cannot h e a r s o u n d s above 20kHz. 21 A n o t h e r p o s s i b l e r e a s o n for the u s e of u l t r a s o u n d s by r o d e n t s i s t e n t a t i v e l y s u g g e s t e d h e r e . High f r e q u e n c y sounds a r e a b s o r b e d very rapidly in a i r 14 and b e c a u s e of t h e i r s h o r t w a v e - l e n g t h s , if e m i t t e d in the field, they would be r e f l e c t e d f r o m s m a l l o b j e c t s such a s b l a d e s of g r a s s and so s c a t t e r e d . Thus although u l t r a s o n i c s i g n a l s could be h e a r d d i s t i n c t l y within a few m e t r e s of t h e i r e m i s s i o n , f u r t h e r away they would be difficult both to h e a r and to l o c a l i s e . If, t h e r e f o r e , u l t r a s o u n d s a r e u s e d f o r c o m m u n i c a t i o n in the social b e haviour of r o d e n t s , they may allow social r e l a t i o n s h i p s to be e s t a b l i s h e d and m a i n t a i n e d b e t w e e n a n i m a l s n e a r to each o t h e r without unduly a d v e r t i s i n g t h e i r p r e s e n c e to p r e d a t o r s . This study of the production of u l t r a s o u n d s in r o d e n t s h a s r e v e a l e d many p o s s i b i l i t i e s f o r the use of u l t r a s o u n d among s m a l l m a m m a l s . F o r e x a m p l e , it s e e m s probable that the sounds p r o d u c e d by s u b m i s s i v e r a t s inhibits the a g g r e s s i o n of a d o m i n a n t a n i m a l and it is p o s s i b l e that the u l t r a s o u n d s p r o d u c e d by the m a l e during mating may affect the behaviour of the f e m a l e . But many q u e s t i o n s have b e e n r a i s e d . Some of t h e s e , such a s the a u d i t o r y s e n s i t i v i t i e s of s m a l l m a m m a l s a s r e v e a l e d by e l e c t r o p h y s i o l o g i c a l s t u d i e s , the motivation f o r the e m i s s i o n of t h e s e sounds in both young and adults, the p o s s s i b l e c o m m u n i c a t i o n value of t h e s e s i g n a l s and the m e c h a n i s m for t h e i r production, a r e at p r e s e n t being i n v e s t i gated by v a r i o u s m e m b e r s of this l a b o r a t o r y . It i s hoped that t h e s e widely v a r y i n g s t u d i e s will r e v e a l m o r e of the ability of r o d e n t s both to p r o d u c e and to use u l t r a s o n i c signals. ACKNOWLEDGEMENTS T h i s r e s e a r c h w a s c a r r i e d out a s p a r t of the work for the d e g r e e of Doctor of P h i l o s o p h y at the U n i v e r s i t y of London. The work was s p o n s o r e d in p a r t by the A i r F o r c e Office of Scientific R e s e a r c h to Dr J. D. Pye. I am indebted to Dr J. D. P y e for much helpful advice and c r i t i c i s m and to Mr S. M. Godson for maintaining the equipment.
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