Flavor Chemistry of Animal Foods


Flavor Chemistry of Animal Foodshttps://pubs.acs.org/doi/pdf/10.1021/bk-1978-0067.ch001Similarby WW JACOBS - ‎Cited by...

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1 Progress in Animal Flavor Research WILLIAM W. JACOBS, GARY K. BEAUCHAMP, and MORLEY R. KARE

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Monell Chemical Senses Center, University of Pennsylvania, 3500 Market St., Philadelphia, PA 19104

For a terrestrial animal, flavor may be defined as the composite sensation resulting from placing something in the mouth. Therefore, flavor may include taste, olfactory, vomeronasal, trigeminal and other chemical sense inputs as well as tactile, temperature and proprioceptive cues. Thus, the subjective sensation we call flavor is the result of interactions of a complex of receptors. The bulk of experimental work in this field has focussed upon one class of receptors and associated CNS processes, the taste system. There are powerful arguments that the taste system is a uniquely important component in regulating flavor perception and food intake (e.g., 1,2) , but other sensory components significantly influence flavor perception (e.g., 3, 4). Humans regard flavors as qualities which add to the aesthetics of dining. Applied flavor researchers devote most of their efforts toward making foods and beverages more acceptable to humans or domestic animals. However, flavor sensations are not confined to domestic species' analyses of food substances. Examples of non-food-related flavor perception can be found in the responses of male hamsters to female conspecifics' vaginal secretions and the responses of guinea pigs to conspecific and congeneric urines. These secretions are both sniffed and licked (5, 6), and there is evidence for both olfactory and vomeronasal involvement in the case of the hamster (7). Guinea pig urine appears to include a complex of active substances (8) and codes a great deal of information including species, sex, diet of donor and individual identity (5,9,10). The inputs of several chemical sense systems and hence perception of the flavor of the urine may be required for the processing of all of the information present. As yet, however, there is no experimental evidence that the taste system is crucial in the processing of information contained in mammalian secretions and excretions. Instead, taste is apparently rather specifically concerned with food and liquid intake. Consequently, taste responses are emphasized in this paper in a comparative-evolutionary approach toward flavor and its relation to food selection by wild and domestic species.

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Bullard; Flavor Chemistry of Animal Foods ACS Symposium Series; American Chemical Society: Washington, DC, 1978.

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Taste S t i m u l i and Responses t o Them: Overview The sensory r e c e p t i o n and response systems of organisms, l i k e t h e i r other f e a t u r e s , are shaped by s e l e c t i o n f o r c e s and are thus tuned t o meet the pressures of the a n c e s t r a l environment. Chemical d e t e c t i o n systems are found i n very p r i m i t i v e l i f e forms i n c l u d i n g b a c t e r i a , protozoans and c o e l e n t e r a t e s (11, 12, 13, 14). These species respond t o a v a r i e t y of s t i m u l i i n c l u d i n g some of those i d e n t i f i e d by humans as having one of the presumed (15) four b a s i c t a s t e s (sweet, s a l t y , sour and b i t t e r ) . I t i s s t r i k i n g that s i m i l a r c l a s s e s of substances are b e h a v i o r a l l y a c t i v e and that c e r t a i n types o f compounds e l i c i t r a t h e r s i m i l a r responses c r o s s phyletically. Some compounds i n the environment have had great i n f l u e n c e s upon s u r v i v a l of animal l i f e s i n c e i t f i r s t appeared. I t i s r e a sonable t o surmise that receptor systems f o r the d e t e c t i o n of these compounds would be w i d e l y d i s t r i b u t e d i n the animal kingdom. To evaluate t h i s p o s s i b i l i t y f o r compounds f a l l i n g i n t o the four c l a s s i c t a s t e q u a l i t i e s reported i n the human l i t e r a t u r e , a l i s t ing has been made of substances r e p o r t e d l y y i e l d i n g each of these q u a l i t i e s t o humans (Table I ) . Of the n a t u r a l l y o c c u r r i n g chemic a l s , i t can be seen t h a t many sugars, some D-amino a c i d s , as w e l l as L-alanine and g l y c i n e are i d e n t i f i e d as sweet. Such substances are found i n many foods. For example, f r e e sugars ( e s p e c i a l l y g l u cose, f r u c t o s e and sucrose) are present i n s u b s t a n t i a l amounts i n many f r u i t s and vegetables (20). The l i s t of s a l t y t a s t i n g substances contains numerous organi c and i n o r g a n i c s a l t s i n c l u d i n g some t o x i c substances (e.g., l i t h i u m c h l o r i d e ) , but a l s o some n u t r i t i o n a l l y important c a t i o n s and anions. Most abundant of a l l of these compounds i s sodium c h l o r i d e which, i n a d d i t i o n t o i t s p h y s i o l o g i c a l importance, was a l s o part of the medium (sea water) i n which many phyla evolved. For marine and t e r r e s t r i a l animals a l i k e , the most common s a l t y compound i s sodium c h l o r i d e w i t h the t o x i c ones much l e s s common. The d i s t r i b u t i o n of NaCl i s more patchy f o r t e r r e s t r i a l than f o r marine animals, however (21). Since NaCl i s an absolute r e q u i r e ment f o r complex organisms, i t i s not s u r p r i s i n g that n e a r l y a l l species t e s t e d respond t o i t . Sour t a s t i n g substances are a l l a c i d s (but not a l l a c i d s t a s t e sour) and are present i n many p o t e n t i a l food items, n o t a b l y f r u i t s . A c i d s , however, a l s o push the organism toward p h y s i o l o g i c a l a c i d o s i s under experimental c o n d i t i o n s and are not g e n e r a l l y p r e f e r r e d t o water a t any d e t e c t a b l e c o n c e n t r a t i o n . I n the l i q u i d medium i n which most phyla evolved, the a b i l i t y to detect a departure from normal environmental pH could a d a p t i v e l y t r i g g e r the avoidance of c o n d i t i o n s w i t h which many species are not p h y s i o l o g i c a l l y able t o cope. Nevertheless, there are a few s p e c i e s , the chicken f o r example (22), which t o l e r a t e and perhaps p r e f e r s o l u t i o n s of h i g h a c i d i t y .

Bullard; Flavor Chemistry of Animal Foods ACS Symposium Series; American Chemical Society: Washington, DC, 1978.

Bullard; Flavor Chemistry of Animal Foods ACS Symposium Series; American Chemical Society: Washington, DC, 1978.

- 16, 17, 18, 19.

Hydrochloric acid N i t r i c acid Acetic acid Butyric acid Succinic acid L a c t i c acid C i t r i c acid

Sodium c h l o r i d e Lithium chloride Ammonium c h l o r i d e Potassium c h l o r i d e Magnesium c h l o r i d e Sodium f l u o r i d e

Sucrose Glucose Fructose Raffinose Galactose Lactose Maltose Xylose Saccharin (Na) Cyclamate (Na) L-aspartyl-Lphenylalanine L-alanine D-histidine D-phenylalanine D-leucine D-tyrosine Glycine Beryllium chloride Thaumatin Monellin

References

Sour

Salty

Sweet Caffeine Nicotine Quinine compounds Strychnine Other a l k a l o i d s Urea Brucine Theobromine Naringin Glucoside Coumarins Terpene hydrocarbons Terpenoids L-leucine L-tryptophan L-tyrosine L-phenylalanine Magnesium s u l f a t e Denatorium benzoate (Bitrex) Sucrose o c t a a c e t a t e

Bitter

Table I . P a r t i a l l i s t i n g of compounds t a s t i n g sweet, s a l t y , sour o r b i t t e r to humans.

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Many n a t u r a l l y o c c u r r i n g b i t t e r t a s t i n g substances are t o x i c , i n c l u d i n g secondary compounds used as defenses by p l a n t s and a n i mals a g a i n s t depredation. Such substances, when detected, are g e n e r a l l y r e j e c t e d by organisms. I t i s not c l e a r i n every i n s t a n c e that r e j e c t i o n of b i t t e r substances i s independent of t h e i r nonsensory e f f e c t s , however (see l a t e r s e c t i o n s ) . T h i s b r i e f l i s t i n g of compounds f o r which humans r e p o r t one of the four b a s i c t a s t e sensations supports the n o t i o n that these compounds have great e c o l o g i c a l relevance f o r many s p e c i e s . This does not mean that each has equal relevance f o r a l l s p e c i e s , or that other s t i m u l i do not have relevance f o r some species ( c f . , 2^ 23). Indeed, w i t h i n one taxonomic group, the responses of i n d i v i d u a l species to v a r i o u s chemical s t i m u l i may d i f f e r c o n s i d e r a b l y . The degree to which these d i f f e r e n c e s represent adaptat i o n s to the unique e c o l o g i c a l c o n d i t i o n s encountered by each species has not been thoroughly s t u d i e d i n mammals. Taste and food preference s t u d i e s have been conducted on a v a r i e t y of s p e c i e s , f o r a v a r i e t y of reasons and w i t h a v a r i e t y of procedures. The most f r e q u e n t l y used design has been that of R i c h t e r (24) which compares the acceptance of a t e s t s o l u t i o n w i t h that of water f o r a 24-hour p e r i o d . M o d i f i c a t i o n s of t h i s design i n c l u d e s h o r t e n i n g or lengthening the p e r i o d of exposure, changing the composition of the s o l v e n t and r e v e r s i n g the l o c a t i o n of t e s t and standard b o t t l e s i n an attempt to c o n t r o l f o r p o s i t i o n p r e f e r ences. An advantage of long t e s t d u r a t i o n s may be t h a t animals responses over periods of 24, 48, 72 or 96 hours are not subject to b r i e f whims of animals or to time-of-day e f f e c t s . Short t e s t proponents argue t h a t these f a c t o r s can be c o n t r o l l e d somewhat by c a r e f u l design and t h a t the r e s u l t s of s h o r t - d u r a t i o n t e s t s (10 min.- 6 hr.) are l e s s l i k e l y to be confounded by p o s t - i n g e s t i o n a l feedback e f f e c t s (e.g., 25). Some s t u d i e s have presented only one or two c o n c e n t r a t i o n s of a given s t i m u l u s . Others have t e s t e d whole s e r i e s , but may have presented concentrations i n ascending, descending or random o r d e r s , each of which may a f f e c t r e s u l t s d i f f e r e n t l y (26). Common procedures have seldom been used by d i f f e r e n t authors s t u d y i n g d i f f e r e n t s p e c i e s . Thus, c r o s s - s p e c i e s comparisons are d i f f i c u l t at best. The f o l l o w i n g d i s c u s s i o n w i l l center on three species for which data have been c o l l e c t e d on a v a r i e t y of s t i m u l i and under s e v e r a l d i f f e r e n t exposure times. 1

Taste Preferences: Comparisons Among Rats, Cats and Guinea P i g s Summaries of the t a s t e responses of l a b o r a t o r y r a t s (Rattus n o r v e g i c u s ) , domestic cats ( F e l i s c a t t u s ) and domestic guinea pigs (Cavia p o r c e l l u s ) appear i n Table I I . These forms represent three d i s t i n c t feeding types: h e r b i v o r e (guinea p i g ) , c a r n i v o r e (cat) and omnivore ( r a t ) . They are a l s o important research animals; thus there i s need to provide them w i t h acceptable d i e t s . F i n a l l y ,

Bullard; Flavor Chemistry of Animal Foods ACS Symposium Series; American Chemical Society: Washington, DC, 1978.

1.

Animal

JACOBS E T A L .

Flavor

Research

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data are a l s o a v a i l a b l e on t a s t e responses of w i l d r e l a t i v e s o f each o f these s p e c i e s , p r o v i d i n g the o p p o r t u n i t y t o draw a few cautious i n f e r e n c e s concerning the e v o l u t i o n and l a b i l i t y of t a s t e preferences. Sweet Substances. Rats (Table I I ) show preferences f o r many substances t a s t i n g sweet t o humans. ( H e r e a f t e r , such responses w i l l be c a l l e d "sweet preferences" f o r the sake o f b r e v i t y ) . Cav i e s show preference f o r the only sugar (glucose) w i t h which they have been t e s t e d but do not p r e f e r i t a t as h i g h c o n c e n t r a t i o n s as do r a t s . Cats, on the other hand, e i t h e r are i n d i f f e r e n t t o o r r e j e c t sugars under most c o n d i t i o n s o f t e s t i n g ( c f . , d i s c u s s i o n i n 29). This i n d i f f e r e n c e t o sucrose and other sugars makes t h e cat (along w i t h some other s p e c i e s , _2, 41) an exception t o t h e g e n e r a l i t y o f sweet preferences among mammals (42) and i s i n accord w i t h 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 which r e p o r t f i n d i n g very few f i b e r s s e n s i t i v e t o sucrose i n c a t s (43,44,45). We may conclude, t h e r e f o r e , that a sweet t a s t e i s , f o r a l l p r a c t i c a l purposes, i n e r t as an a p p e t i t i v e cue f o r domestic c a t s , whereas r a t s and guinea p i g s can use t h i s cue i n food s e l e c t i o n . The responses to sweets by the domestic forms are very s i m i l a r t o those o f t h e i r w i l d r e l a t i v e s . M a i l e r (46, 47) found very s i m i l a r acceptance percentages (percent o f t o t a l f l u i d i n t a k e that i s t e s t s o l u t i o n i n s o l u t i o n vs. water choice t e s t ) o f s i n g l e conc e n t r a t i o n s of a v a r i e t y o f sugars by w i l d and l a b o r a t o r y Norway r a t s (Rattus n o r v e g i c u s ) . Laboratory r a t s increased f l u i d consumption g r e a t l y during these t e s t s whereas the w i l d type d i d not. Shumake, e t a l (48) found w i l d and l a b o r a t o r y r a t s t o be very simi l a r i n acceptance o f s o l i d d i e t s t r e a t e d w i t h sucrose i n a mechanized design i n which consumption d i f f e r e n c e s appear t o have been " c o n t r o l l e d out." Therefore, the d o m e s t i c a t i o n , o r more p r o p e r l y l a b o r a t o r i z a t i o n , o f Rattus has not a l t e r e d the sweet preferences of t h i s species but has a l t e r e d consumption, a r e l a t e d response. Wild c a v i e s showed higher acceptance and a broader preference range f o r glucose than d i d t h e i r domestic counterparts (33). The domestic c a v i e s acceptances became l i k e the responses o f the w i l d type (which remained c o n s i s t e n t ) upon r e t e s t i n g (34). Between-type consumption d i f f e r e n c e s a l s o were found, p a r t i c u l a r l y d u r i n g the a n i m a l s i n i t i a l exposures t o glucose. However, u n l i k e the s i t u a t i o n w i t h r a t s , i t was the w i l d c a v i e s who showed the g r e a t e r increases i n consumption o f sweet s o l u t i o n . These d i f f e r e n c e s between types a l s o diminished w i t h repeated t e s t i n g . These and other data i n d i c a t e that the w i l d cavy o r i e n t s more q u i c k l y t o s o l u t i o n cues than does the domestic form but f a i l t o provide any evidence f o r sensory d i f f e r e n c e s between them (34). Beauchamp, e t a l (29) have r e c e n t l y t e s t e d t a s t e responses o f twelve w i l d c a t s o f Genus Panthera ( l i o n s , P. l e o ; t i g e r s , _P. t i g r i s ; leopards, P. pardus; j a g u a r s , P. onca) i n short-term preference t e s t s . The r e s u l t s were not s u b s t a n t i a l l y d i f f e r e n t from 1

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Bullard; Flavor Chemistry of Animal Foods ACS Symposium Series; American Chemical Society: Washington, DC, 1978.

Bullard; Flavor Chemistry of Animal Foods ACS Symposium Series; American Chemical Society: Washington, DC, 1978.

C i t r i c acid

Sour

26

f

2 6

27

Rej(.10*-.15M )

t

1

36

35

Pref (.008*-.05M *) Pref(.0092-.052M) 24

Pref(.0067-.61M) Rej(>1.05M)31

Pref(.006*-lM )

f

Pref (.22-1.39M )

31

26

Pref (.055-1.4M)

Pref(.055-1.6M)

Pref(.006*-1.6M) Pref(.011-.9M) Rej(>1.6M)27

Laboratory Rat

2 9

f

Rej(.06*-.48M )

37

Indif(.015*-.12M ) Rej(^.5M) 28

f

37

P r e f ( . l M ) Rej(.5M)28

1

Rej (.60M )

I n d i f 29

I n d i f 29

2 8

lndif > e

Domestic Cat

34

34

Rej(>.031M) 34

Rej(>_.5M)

Pref(.008-.25M) 34

f

3 2 , 3 3

Pref ( . l - . 4 M )

Pref(.2M o n l y )

Domestic Guinea P i g

Summary of responses of three f a m i l i a r mammals to some n a t u r a l sweet, s a l t y , sour and b i t t e r s t i m u l i i n s o l u t i o n v s . water choice t e s t s .

Sodium c h l o r i d e

Salty

Galactose

Maltose

Fructose

Glucose

Sucrose

Sweet

Table I I .

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Bullard; Flavor Chemistry of Animal Foods ACS Symposium Series; American Chemical Society: Washington, DC, 1978. 3 5

38

y

Rej(>.000021M)

Rej(>.000275M)

1

Rej (.000008M* ')

Laboratory Rat

37

Rej (1.000005M*)

Rej (1.00025M*)

Domestic Cat

28

+

Rej(>.002M)

40

I n d i f (. 00016*-.00124M )

Domestic Guinea P i g

3

4

@ A preference f o r .25-.375M sucrose d i s s o l v e d i n .03M NaCl has been reported f o r c a t s . 29 subsequent study f a i l e d to f i n d such a preference.

t Highest concentrations used.

* I n d i c a t e s t h a t these c o n c e n t r a t i o n s were the lowest used i n the study c i t e d ,

5) Exposure times v a r i e d between s t u d i e s c i t e d .

30 A

Assignment of terms i n the l a t t e r case was based upon our experiences w i t h

conducting t h i s s o r t of t e s t i n g .

were l a c k i n g .

i n the c i t e d r e f e r e n c e s or by v i s u a l e v a l u a t i o n of t a b l e s and f i g u r e s i f s t a t i s t i c a l data

4) P r e f e r e n c e , I n d i f f e r e n c e and R e j e c t i o n were determined e i t h e r from s t a t i s t i c a l t e s t s presented

3) Rej = R e j e c t i o n

2) I n d i f = I n d i f f e r e n c e

1) P r e f = Preference

NOTES:

Quinine h y d r o c h l o r i d e

Quinine s u l f a t e

Bitter

Table I I . (continued)

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those w i t h domestic c a t s : Panthera p r e f e r r e d no sweet substances. S a l t y Substances. A l l three domestic species show a p r e f e r ­ ence f o r at l e a s t one hypotonic ( 102, 103, 104) and food s e l e c t i o n ( 2 ) . For e x t e r n a l and i n t e r n a l reasons, animals c o n t i n u a l l y e x e r c i s e t h e i r food s e l e c tion faculties. e

Conclusions This paper has s t r e s s e d f a c t o r s i n v o l v e d i n the e x h i b i t i o n of preferences and aversions by animals to p o t e n t i a l n u t r i e n t s . Perhaps the b i g g e s t advance i n animal f l a v o r research over the past f o r t y years has been the i d e n t i f i c a t i o n and experimental i s o l a t i o n of these f a c t o r s : inherent preferences, c o n d i t i o n e d a v e r s i o n s , neophobia and n e o p h i l i a . While each o f these f a c t o r s has been shown t o a f f e c t c h o i c e s , the manner i n which they i n t e r act f o r a given species must be determined e x p e r i m e n t a l l y i n each case. The i d e n t i f i c a t i o n of these f a c t o r s , however, provides the t o o l s needed to answer a p p l i e d questions concerning the feeding of p e t s , l i v e s t o c k and zoo animals and the c o n t r o l o f animal damage. I n doing such r e s e a r c h , the s u b j e c t s ' phylogenetic and ontogenetic h i s t o r i e s must always be considered.

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LITERATURE CITED

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1. Hankins, W.G., Rusiniak, K.W. and Garcia, J., Behavioral Biology (1976) 18, 345-358. 2. Kare, M.R. and Beauchamp, G.K., In: Swenson, M.J. (ed.) "Dukes' Physiology of Domestic Animals," 713-730, Cornell University Press, Ithaca, N.Y., 1977. 3. Mozell, Μ., Smith, Β., Smith, P., Sullivan, R. and Swender, P., Archives of Otolaryngology (1969) 90, 367-373. 4. Mugford, R.A., In: Kare, M.R. and Maller, O. (eds.) "Chemical Senses and Nutrition, Vol. II," Academic Press, New York, in press. 5. Beauchamp, G.K., Physiology and Behavior (1973) 10, 589-594. 6. Johnston, R.E. and Zahorik, D.M., Science (1975) 189, 893-894. 7. Powers, J.B. and Winans, S.S., Science (1975) 187, 961-963. 8. Beruter, J., Beauchamp, G.K. and Muetterties, E . L . , Biochem­ ical and Biophysical Research Communications (1973) 53, 264-271. 9. Beauchamp, G.K., Nature (1976) 263, 587-588. 10. Beauchamp, G.K., unpublished data. 11. Adler, J., In: Carlile, M.J. (ed.), "Primitive Sensory and Communication Systems," 91-100, Academic Press, London, 1975. 12. Beidler, L.M., In: Denton, D.A. and Coughlan, J.P. (eds.), "Olfaction and Taste: 5th International Symposium," 7176, Academic Press, New York, 1975. 13. Garcia, J . and Hankins, W.G., In: Denton, D.A. and Coughlan, J.P. (eds.) "Olfaction and Taste: 5th International Symposium," 39-45, Academic Press, New York, 1975. 14. Hodgson, E.S., In: Kare, M.R. and Mailer, O. (eds.) "The Chemical Senses and Nutrition," 7-18, Johns Hopkins Press, Baltimore, 1967. 15. McBurney, D., Chemical Senses and Flavors (1974) 1, 17-28. 16. Brand, J . G . , Nairn, M. and Kare, M.R., In: Rechcigl, M. (ed.) "Handbook Series in Nutrition and Food," CRC Press, Cleveland, in press. 17. Furia, T.E. , In: Furia, T.E. and Bellanca, N. (eds.) "Fenaroli's Handbook of Flavor Ingredients, Vol. I . , " 8-11, CRC Press, Cleveland, 1975. 18. Moskowitz, H . , In: Sipple, H.L. and McNutt, K.W. (eds.), "Sugars in Nutrition," 37-64, Academic Press, New York, 1974. 19. Solms, J., Journal of Agricultural and Food Chemistry (1969) 17_, 686-688. 20. Shallenberger, R.S., In: Sipple, H.L. and McNutt, K.W. (eds.), "Sugars in Nutrition," 67-80, Academic Press, New York, 1974. 21. Rozin, P., In: Hinde, R.A., Shaw, E. and Beer, C. (eds.) "Advances in the Study of Behavior, Vol. 6," 21-75 Academic Press, New York, 1976.

Bullard; Flavor Chemistry of Animal Foods ACS Symposium Series; American Chemical Society: Washington, DC, 1978.

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Animal Flavor Research

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Bullard; Flavor Chemistry of Animal Foods ACS Symposium Series; American Chemical Society: Washington, DC, 1978.

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Bullard; Flavor Chemistry of Animal Foods ACS Symposium Series; American Chemical Society: Washington, DC, 1978.

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103. Wade, G.N. and Zucker, I., Journal of Comparative and Physiological Psychology (1969) 69, 291-300. 104. Zucker, I., Physiology and Behavior (1969) 4, 595-602. RECEIVED October 25, 1977.

Bullard; Flavor Chemistry of Animal Foods ACS Symposium Series; American Chemical Society: Washington, DC, 1978.