Food Preference Behavior in Birds and Mammals - American

2 Food Preference Behavior in Birds and Mammals STEPHEN A. SHUMAKE

Downloaded by CORNELL UNIV on May 8, 2017 | http://pubs.acs.org Publication Date: February 2, 1978 | doi: 10.1021/bk-1978-0067.ch002

U. S. Fish and Wildlife Service, Wildlife Research Center, Denver, CO 80225

The higher vertebrates survive in the wild through elaborate and eloquent systems of food searching, prey finding, sampling, and selection activities (1, 2). Some omnivorous species have a tremendous adaptive advantage in meeting their energy and nutritional requirements. For example, as one primary food source declines, the omnivores tend to sample new food sources or previously less palatable foods in order to survive (3, 4). Many migratory bird species including the African weaver finch or quelea (5) are able to survive and proliferate in spite of seasonal changes in the abundance of seeds and grains. The behavior and physiology of migratory birds appear to be directly correlated with environmental changes. For example, the quelea lay down fat stores before migrating from dry season areas (6). These birds also migrate with the rainy season to obtain enough food for themselves (seeds and grains) and for their young (green plant material and raw protein from termites and other insects). Certain herbivores such as antelope, mountain sheep, and elk are able to maintain themselves throughout the winter seasons of low food availability by moving to lower elevations (7) or by changing their microflora and microfauna to allow digestion of normally less nutritious plants such as locoweed or sagebrush. These observations point out the physiological and behavioral adaptiveness of wild birds and mammals and their ability to adopt new food habits. Partially for this reason, it is highly unlikely that any commercially available flavoring agents or flavor enhancers that have been developed for humans will have strong and durable flavor preference effects in wild species (8, 9). Instead, most wild animals appear to be adapted or conditioned to associate certain food odors, tastes, and flavors with beneficial effects (i.e., more energy, less nervousness, weight gain, and general health). Other flavors become associated with injurious sublethal poisoning (10) effects such as vomiting, diarrhea, or unconsciousness. Still, there are certain innate flavor preferences that exhibit themselves widely among the omnivores. For example, man, © 0-8412-0404-7/78/47-067-021$10.00/0 Bullard; Flavor Chemistry of Animal Foods ACS Symposium Series; American Chemical Society: Washington, DC, 1978.


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rodents, hogs, and most other mammals (VU 12) a l l show a preference for glucose, sucrose, and even non-nutritive saccharin that is independent of nutritional wisdom or experience. Bitter substances including quinine, sucrose octaacetate, and cyanide are avoided by birds (13), coyotes (14), rodents (1J5) , and herbivores (16). For most species this rejection behavior may be regarded as unlearned. The vast majority of food items consumed by omnivores contain extremely complex mixtures of flavors, and experience with the food is probably the single most important factor controlling preference behavior. Pure flavor sensation and animal preference for i t are extremely d i f f i c u l t to measure. P. T. Young's (V7) approach to this problem of measuring hedonic (pleasurable) or aversive (repellent) taste stimuli has been widely adopted and proposed as a standard method for evaluating taste preference in rats (18). Unfortunately, very few natural flavors have only sensory content. Past associations with flavors can be just as, i f not more, important than their sensory content (3, 19). Birds and mammals do not simply sample a new food item and then either continue or discontinue feeding on the basis of sensory (hedonic) content alone. Typically, the flavors or chemical components of the food items i n i t i a l l y act as signals for either nutritional or toxic effects. Later, palatability may actually be changed (20). In this respect, the chemical senses are similar to the visual or auditory senses. For example, i f gerbils are reared in their natural tunnel systems, they tend to quickly flee and hide from moving visual stimuli. If they are reared, like most laboratory rodents, in wire mesh cages with no opportunity to construct burrow systems, the gerbils show very l i t t l e avoidance of the same stimuli (21_). There are exceptions—if, for example, an animal is hormonally primed and presented with a "super normal" stimulus, the sheer intensity may be enough to evoke a genetically fixed response (22). Regardless of the wild species to be considered or the food flavor under study, the chemist involved in animal food flavor research and development should be aware of the numerous factors that ultimately influence and determine food preference behavior of birds and mammals. This review will not be an attempt to report a l l that is known about food preference behavior of birds and mammals. Such information could be of limited benefit to the chemist working on animal food flavor problems, but, as I will point out to the reader several times, each bird or mammal in a specific habitat is a somewhat unique entity. Laboratory data do not necessarily generalize to f i e l d situations and f i e l d experiments are often d i f f i cult i f not impossible to duplicate in the laboratory. Instead of an exhaustive review, I have elected to cover some important factors that can often influence flavor preference behavior. Next, a brief review is given of attempts to modify preference behavior by the empirical screening approach. Finally, an example of one approach to the problem of intensifying rice flavor to increase

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

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rodent b a i t consumption i s covered i n some d e t a i l . A number o f suggestions i n regard to f u t u r e animal food f l a v o r research are then covered i n the conclusions s e c t i o n .


Factors I n f l u e n c i n g

Food Preference Behavior

N u t r i t i o n a l F a c t o r s . Birds and mammals are e f f i c i e n t at food regulation. Even man, whose f l a v o r preference behavior i s l a r g e l y determined by s o c i a l , economic, and c u l t u r a l patterns (23) tends to g e n e r a l l y increase f a t intake i n c o l d environments, p r o t e i n content i n temperate zones, and carbohydrate content i n t r o p i c a l zones. Much of t h i s food s e l e c t i o n behavior, however, i s d i s t o r t e d by food a v a i l a b i l i t y whether i t be r e l a t e d to socioeconomic status or food crops p r e v a l e n t l y grown i n s p e c i f i c c l i m a t e s . From the standpoint o f animal h e a l t h , n u t r i t i o n a l q u a l i t y o f foods ingested have a d i r e c t bearing on s u r v i v a l of mammals. By d e f i n i t i o n , the f l a v o r q u a l i t i e s of animal foods tend to take on meaning and can lead to n u t r i t i o n a l wisdom. As P. T . Young (24) and M. Kare (25) have often pointed o u t — t h e chemoreceptors stand as guarcls" to the alimentary c a n a l . But, j u s t how e f f i c i e n t are mammals and b i r d s at a c h i e v i n g n u t r i t i o n a l balance? The t a s t e or f l a v o r o f c e r t a i n e s s e n t i a l n u t r i e n t s such as glucose and sodium are immediately sought when a need a r i s e s i n mammals. Morrison and Young (26) and Nachman (27) b e l i e v e there i s an automatic increase i n the p a l a t a b i l i t y f o r s a l t s or sugars as they become d e f i c i e n t i n the d i e t . Some data (28) i n d i c a t e that there may be glucoreceptors i n the l i v e r that send neural information back to feeding and appetite centers i n the b r a i n . Mailer et a l . (29) have proposed a d i r e c t pathway to the b r a i n from the oral-pfiaryngeal area o f rats that regulates intake o f c e r t a i n n u t r i e n t s such as NaCl and glucose. The exact nature o f t h i s pathway and i t s p r o j e c t i o n area i n t o the lower b r a i n centers have not y e t been d e s c r i b e d . Pi 1 cher and Jarman (30) i n attempting to i n v e s t i g a t e t h i s o r i g i n a l f i n d i n g , b e l i e v e tFTat the hepatic system i s more important than the d i r e c t pathway hypothesis. Contreras & Hatton (31) have c i t e d some evidence that the sodium a p p e t i t e and p a l a t a b i l i t y change toward s a l t y t a s t i n g foods or l i q u i d s i n a l b i n o rats may be c o n t r o l l e d by the K/Na r a t i o i n t h e i r b l o o d . Morrison and Young (26) found that r a t s made sodium d e f i c i e n t by formalin i n j e c t i o n drank equal amounts o f e i t h e r 0.3 M NaCl or .03 M Na2CÛ3 s o l u t i o n even though NaCl contains f i v e times more sodium per u n i t volume. A g a i n , they conclude from these data that sodium d e p l e t i o n produces p a l a t a b i l i t y changes and that the amount o f " s a l t y " t a s t i n g s o l u t i o n drunk s i g n a l s s a t i e t y rather than sodium r e p l e t i o n . Thus, f o r some n u t r i e n t s , such as s a l t s or sugars, p a l a t a b i l i t y changes a u t o m a t i c a l l y regulate n u t r i t i o n a l balance i n r a t s . For thiamine (Vitamin B-|) d e f i c i e n c y , Rozin (32, 33) c i t e s r a t h e r convincing evidence t h a t the f l a v o r of the (fiet~Teading to vitamin B] s u f f i c i e n c y i s a s s o c i â t ! v e l y learned by r a t s . Food



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odors may play a dominant r o l e i n vitamin enriched d i e t a r y s e l e c t i o n (3) or glucose i n j e c t i o n (34). T h i s same general f i n d i n g i s i m p l i c a t e d i n the e a r l y reports concerning s p e c i f i c a p p e t i t e f o r e s s e n t i a l vitamins (35, 36). For example, the vitamin d e f i c i e n t rats did not cue i n on the " f l a v o r " of vitamin B. Rather, they s e l e c t e d a new d i e t with a d i s t i n c t i v e (new) f l a v o r when the o l d f l a v o r e d d i e t l e d to continued d e f i c i e n c y symptoms. Diets cont a i n i n g calcium appear to a f f e c t rats i n a s i m i l a r manner (27). Although no s p e c i f i c appetites f o r vitamins A and D have been demonstrated (27), Bernard e t a l . (37) have shown t h a t vitamin A d e f i c i e n c y leads to decreased t a s t e s e n s i t i v i t y . Apparently, vitamin A i s e s s e n t i a l f o r normal t a s t e s e n s i t i v i t y o f the mammalian t a s t e buds (38) and both quinine r e j e c t i o n and NaCl s e l e c t i o n are retarded i n vitamin A d e f i c i e n t r a t s . There appear to be several d i f f e r e n c e s and some s i m i l a r i t i e s between t a s t e preference responses of b i r d s when compared to mammals i n n u t r i t i o n a l d e f i c i e n c y preference t e s t s . For example, Hughes and Wood-Gush (39) were unable to demonstrate any evidence o f s p e c i f i c a p p e t i t e f o r sodium i n chickens fed e i t h e r a sodium d e f i c i e n t d i e t or given formalin i n j e c t i o n s . Young chicks were p a r t i c u l a r l y s u s c e p t i b l e to sodium c h l o r i d e t o x i c i t y . In r a t s , s p e c i f i c a p p e t i t e f o r sodium i s r e a d i l y e s t a b l i s h e d (40, 4 U 4 2 ) , probably because r a t s are more capable o f sodium e x c r e t i o n than most b i r d s , except f o r , perhaps c e r t a i n marine species t h a t possess s p e c i a l i z e d s a l t - s e c r e t i n g glands (43). Hughes and Wood-Gush (39) were able to e a s i l y demonstrate a s p e c i f i c a p p e t i t e f o r t h i a mine i n chickens s i m i l a r to that found i n rats (32). Thus, d i e t a r y d e f i c i e n c i e s can sometimes g r e a t l y i n f l u e n c e preference t e s t r e s u l t s in both birds and mammals. P h y s i o l o g i c a l Influences. Animals i n g e s t foods p r i m a r i l y to s a t i s f y energy requirements, metabolic needs, and f o r reproductive function. In s h o r t , food f l a v o r s become a s s o c i a t e d w i t h , or are c o r r e l a t e d w i t h , adequate d i e t under given environmental c o n d i tions. Animals t h a t do not s e l e c t adequate d i e t s do not s u r v i v e and reproduce. Thus, foods that c o r r e c t p h y s i o l o g i c a l d e f i c i e n c i e s or need s t a t e s are r e i n f o r c e d and food habits are then e s t a b l i s h e d (27). For example, the e f f e c t s o f i n f u s e d n u t r i e n t s i n t o the stomachs of r a t s have a marked i n f l u e n c e on feeding behavior. A d a i r , M i l l e r , and Booth (44) found that amino acids i n f l u s i o n produced an o v e r a l l decreased food consumption by a l b i n o r a t s . D-glucose alone, however, only s p e c i f i c a l l y suppressed consumption o f D-glucose s o l u t i o n s and not o v e r a l l consumption. Thus, the w i l l i n g n e s s o f an animal to eat any a v a i l a b l e food cannot be simply explained by a blood glucose-homeostasis mechanism ( i . e . , the glucostatic theory). Mixtures of c e r t a i n high c a l o r i e n u t r i t i v e and n o n - n u t r i t i v e sweeteners i n water s o l u t i o n can l e a d to excessive d r i n k i n g by l a b o r a t o r y rats (45). When o f f e r e d a mixture o f 3% glucose and 0.125 or 0.250% s a c c h a r i n i n d i s t i l l e d water, the rats consumed



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f l u i d amounts approximately equal to t h e i r body weights every 24 hours. This excessive d r i n k i n g ( p o l y d i p s i a ) was explained as a s y n e r g i s t i c a c t i o n o f the mixture that l e d to a h i g h l y p a l a t a b l e sweet t a s t e without an a s s o c i a t e d high c a l o r i c c o n t e n t , while the s l i g h t l y b i t t e r t a s t e of s a c c h a r i n was masked by glucose. M a i l e r (46) has i n d i c a t e d that w i l d Norway rats (Rattus norvegicus) are c a l o r i c a l l y s e l e c t i v e i n t h e i r food h a b i t s . Thus, p a l a t a b i l i t y f a c t o r s could play a l e s s e r r o l e i n food s e l e c t i o n by w i l d rodents as compared with l a b o r a t o r y r a t s . I have found, however, t h a t w i l d Norway rats e x h i b i t p o l y d i p s i a when o f f e r e d the glucose and s a c c h a r i n mixture. A group o f s i x w i l d Norway r a t s drank an average o f 362 ± 21 ml o f f l u i d per day. Six w i l d r i c e f i e l d rats (Rattus r a t t u s mindanensis), on the other hand, d i d not show such extreme p o l y d i p s i c behavior, d r i n k i n g on the average 78 ± 8 ml of the f l u i d mixture per day. The exact nature o f t h i s species d i f f e r e n c e was not c l e a r from t e s t s with various two-choice combinations o f water, s a c c h a r i n s o l u t i o n , glucose s o l u t i o n , and the mixture. A p p a r e n t l y , both glucose and s a c c h a r i n and t h e i r i n t e r a c t i o n at e i t h e r the r e c e p t o r o r c a l o r i c r e g u l a t i n g l e v e l , c o n t r i b u t e to the species d i f f e r e n c e . As i n d i c a t e d above, w i l d rats do not always s e l e c t c a l o r i c a l l y balanced d i e t s , e s p e c i a l l y under l a b o r a t o r y c o n d i t i o n s . In attempting to f u r t h e r understand c a l o r i c r e g u l a t i n g and feeding systems o f r a t s , Piquard e t a l . (47) have found that a 25% d a i l y c a l o r i e glucose i n f u s i o n i n t o the r a t ' s c i r c u l a t o r y system v i a i n t r a c a r d i a c c a t h e t e r produced an 80% decrease i n intake o f g l u c o s e - t r e a t e d food. Amino a c i d and l i p i d i n f u s i o n produced decreases i n intake o f p r o t e i n s , l i p i d s , and g l u c i d s as w e l l . Booth and Campbell (48) found that i n s u l i n i n f u s i o n i n t o the c i r c u l a t o r y system of rats produced increased food consumption but they could not show that i n f u s i o n s o f f a t t y acids (the breakdown product of f a t s ) had any e f f e c t s on the food intake o f a l b i n o r a t s . Campbell and Davis (28) have shown t h a t both duodenal and portal glucose i n f l u s i o n s w i l l reduce l i c k i n g rates f o r glucose s o l u t i o n s . Thus, at l e a s t f o r glucose, sweet t a s t e p a l a t a b i l i t y and subsequent c a l o r i c r e g u l a t i o n may be c o n t r o l l e d to some degree by chemoreceptors i n the l i v e r . Other p h y s i o l o g i c a l v a r i a b l e s such as circadium rhythms (49), estrus c y c l e (50, 51), sexual hormones (52), and i n s u l i n l e v e l (53) can have i n f l u e n c e s on odor d e t e c t i o n and t a s t e preference or perception i n r a t s . A d e t a i l e d review o f these e f f e c t s i s beyond the scope of t h i s r e p o r t . However, f l a v o r researchers dealing with improving the food acceptance o f l i v e s t o c k , domestic p e t s , or w i l d animals should be aware that these v a r i a b l e s can a f f e c t f l a v o r preference t e s t r e s u l t s . Postingestional factors such as l e v e l of c i r c u l a t i n g blood glucose (54), bulk or f i b e r content o f the food ( 7 ) , and s u b l e t h a l i l l n e s s e f f e c t s (33) a l s o often play some r o l e i n preference t e s t r e s u l t s especially"when the animals are o f f e r e d continuous access or long-term access (>l-2 hrs) to the t e s t food or foods.



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Genetic Factors and the E f f e c t s o f Domestication. Domestic a t i o n of the w i l d Norway r a t has l e d to c e r t a i n s u b t l e changes in f l a v o r preference behavior and the reactions o f d i f f e r e n t r a t s t r a i n s to new foods. M i t c h e l l , Beatty, and Cox ( 5 5 ) found that two d i f f e r e n t w i l d Norway r a t populations produced F] progeny that d i f f e r e d i n t h e i r i n i t i a l acceptance of a new food i n a new feeder. Norway r a t FT progeny from a pig farm a l s o showed a higher incidence o f p o i s o n - e l i c i t e d p i c a a f t e r cyclophosphamide i n j e c t i o n than d i d the progeny from Norway rats captured on a coastal i s l a n d . These d i f f e r e n c e s i n feeding behavior could be the product o f s e l e c t i o n pressure because rats i n farming areas would be much more l i k e l y to contact r o d e n t i c i d e s and traps than rats l i v i n g on an i s o l a t e d i s l a n d . Water, as a p a r t i a l physical b a r r i e r , could have a l s o l e d to more inbreeding among the i s l a n d r a t p o p u l a t i o n . In any event, the r e s u l t s tend to r e i n f o r c e the notion that l o n g i t u d i n a l studies are needed to evaluate domestication e f f e c t s . B r i e f - e x p o s u r e preference t e s t s as described by Young and Kappauf ( 5 6 ) have not demonstrated genetic changes i n t a s t e p r e f erence b e f i â v i o r of Long-Evans hooded versus l a b o r a t o r y b r e d - a n d reared w i l d Norway rats ( 5 7 J . Thus, food f a m i l i a r i t y and r e a r i n g conditions may be, i n some i n s t a n c e s , more important determiners of t a s t e preference behavior and food acceptance than the more s u b t l e g e n e t i c e f f e c t s . Jackson ( 5 8 ) , f o r example, reported that roof rats i n c e n t r a l F l o r i d a feed e x t e n s i v e l y on oranges. Other Southern r o o f rats do not show much acceptance o f c i t r u s as a food item. In the P a c i f i c i s l a n d s , r o o f rats r e a d i l y take coconut on some i s l a n d s and ignore t h i s source o f food on other i s l a n d s . There i s , however, l i t t l e doubt that genetic i n f l u e n c e s can play a r o l e i n determining t a s t e preference behavior. For example, mice o f d i f f e r e n t species show d i f f e r e n t preference responses to 10% glucose versus 1 0 % f r u c t o s e ( 5 9 ) , d i f f e r e n t c o n d i t i o n e d a v e r sion responses to various sugars JEO), and d i f f e r e n t saccharin preference behavior ( 6 1 ) . Wenzel ( 6 2 ) cautions researchers that domesticated and l a b o ratory animals ( a l b i n o r a t s , pigeons, and chickens) may be much less s e n s i t i v e to t a s t e and odor s t i m u l i than are w i l d mammals and birds. For example, domestic chickens are able to compensate f o r reduced c a l o r i c content i n t h e i r d i e t by d r i n k i n g l a r g e r q u a n t i t i e s o f 10% sucrose i n water s o l u t i o n . Normally, however, chickens are i n d i f f e r e n t to sucrose. Kare and M a i l e r ( 6 3 ) found, on the other hand, t h a t Red Jungle fowl tend to p r e f e r sucrose s o l u t i o n s at a l l times and appear to be s u p e r i o r to the domestic chicken i n caloric regulation. Likewise, there i s some evidence ( 4 6 ) that c a l o r i c r e g u l a t i o n i n w i l d rodents i s u s u a l l y s u p e r i o r to t h a t demonstrated by l a b o r a t o r y r a t s . In terms o f animal food f l a v o r development as an a p p l i e d endeavor, these v a r i a b l e s o f domestication and genetic e f f e c t s do not g e n e r a l l y r e q u i r e separate analyses. The reported data do


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imply, however, t h a t the f l a v o r research bioassay should i n c o r p o rate the t a r g e t s p e c i e s , and should d u p l i c a t e c e r t a i n aspects o f the natural ecosystem o f the t a r g e t mammal or b i r d . Behavioral and E c o l o g i c a l I n f l u e n c e s . Much o f the e c o l o g i c a l l i t e r a t u r e r e l a t e d to food h a b i t s , p r e f e r e n c e s , and aversions o f mammals deals with complex predator-prey r e l a t i o n s h i p s . Pearson (64) observed a c y c l i c a l r e l a t i o n s h i p between m i c r o t i ne rodent population l e v e l s and the abundance o f mammalian predators ( e . g . , skunks, foxes, weasels, and f e r a l c a t s ) . Because these predators r e l y on rodents as a primary food source, they tend to delay recovery o f lower rodent population c y c l e s . As rodent populations reach high d e n s i t y l e v e l s , d i s e a s e , p a r a s i t e s , and s t r e s s along with p r é d a t i o n pressure are thought to cause rodent population d e c l i n e s . When the m i c r o t i ne prey population has ebbed, predators w i l l e i t h e r s t a r v e or emigrate. Macdonald (65) has s t u d i e d the prey preference behavior of red foxes (Vulpes vu 1 1 pes) i n great d e t a i l i n the f i e l d . The p a r t i c u l a r prey species taken can depend on several f a c t o r s such as prey a v a i l a b i l i t y and i t s a n t i p r e d a t o r b e h a v i o r , the r e l a t i v e energy costs o f hunting the prey, and the s i z e and n u t r i e n t value of the prey. Foxes took f i e l d mice i n preference to bank voles and wood mice. They a l s o tended to p r e f e r Microtus to Peromyscus. Moles and common shrews tended to be avoided as prey by the red fox. Fresh carcasses o f other carnivores ( e . g . , weasels, badgers, and foxes) were inspected by foxes but were not e a t e n . Instead, foxes would o f t e n mark t h e i r l o c a t i o n s with urine or f e c e s . The general pattern seemed to i n d i c a t e that foxes p r e f e r r e d the f l e s h o f herbivores and avoided the f l e s h o f i n s e c t - and meat-eating animals. The study could provide some clues to the food f l a v o r chemist as to p o s s i b l e s t a r t i n g points i n developing food f l a v o r s f o r f o x e s , dogs, or other c a n i d s . Apfelback (66) has observed that p r e y - c a t c h i n g behavior o f polecats i s highly" dependent on o l f a c t o r y cues. He found that polecats fed e i t h e r dead chicks o r dead rodents f o r t h e i r whole l i v e s showed no i n t e r e s t i n the odor o f the other prey and refused to eat i t . Searching behavior i s apparently only shown by p o l e cats when they contact the odor of the f a m i l i a r prey item. These demonstrated e f f e c t s , although p r i m a r i l y shown i n pen t e s t s , may i n d i c a t e a s e n s i t i v e period ( i . e . , through the fourth month o f l i f e ) during which c e r t a i n carnivores imprint on c e r t a i n prey items as food. With rodents, such o l f a c t o r y or food f l a v o r i m p r i n t i n g i s d i f f i c u l t to demonstrate under both l a b o r a t o r y and s e m i - f i e l d conditions. Some o f the e a r l i e r attempts (15^, 67^, 68) f a i l e d to show any e f f e c t s o f e a r l y feeding experience ( i . e . , post weaning) with l a b o r a t o r y rats or guinea p i g s . More recent reports (69, 70_, 71) have shown that temporary e f f e c t s can be demonstrated f o r food odor and food f l a v o r s i f rats are exposed to the s t i m u l i very



28

FLAVOR

CHEMISTRY

OF ANIMAL

FOODS

e a r l y i n l i f e ( i . e . , preweaning or during the f i r s t postnatal week of l i f e ) . Perhaps more important than p o s s i b l e f l a v o r i m p r i n t i n g e f f e c t s , r e s u l t i n g from the f i r s t foods eaten by newly weaned r a t s , are t h e i r maternal feeding experiences with s p e c i f i c f l a v o r s from l a c t a t i n g dams (72). Galef and Henderson (73) demonstrated that weanling rats would a c t i v e l y seek and p r e f e r e n t i a l l y feed on the d i e t fed to l a c t a t i n g dams during the nursing p e r i o d , even when the d i e t was normally l e s s p a l a t a b l e . Presumably, the f l a v o r o f the dam's d i e t w i l l a f f e c t the f l a v o r of her milk to some degree. Another important f a c t o r t h a t determines which food a r a t pup i s most l i k e l y to eat i s the feeding s i t e s e l e c t e d by parent rats (74). This appears to be a form of s o c i a l i m i t a t i o n that the pups d i s p l a y toward adults that are a c t i v e l y f e e d i n g . A t h i r d f a c t o r t h a t can i n f l u ence r a t pup feeding preference i s the existence o f a maternal pheromone (75, 76). The d i e t o f the l a c t a t i n g r a t can determine the odor a n c T f l a v o r q u a l i t y o f t h i s pheromone ( i . e . , caecotrophe) excreted f o l l o w i n g p a r t u r i t i o n , and r a t pups from such mothers tend to p r e f e r the odor and f l a v o r o f the mother's d i e t . Stimulus f a m i l i a r i t y (77) appears to be the most important aspect of these s o c i a l l y transmitted f l a v o r preference e f f e c t s . F i n a l l y , a fourth f a c t o r t h a t leads to feeding s i t e s e l e c t i o n by r a t pups (78) appears to be other o l f a c t o r y cues that r e s u l t from urine~cTe p o s i t s l e f t by a d u l t r a t s at s p e c i f i c feeding s i t e s . Flavors o f the most f a m i l i a r and normally p r e f e r r e d food items can, of course, determine which foods are most f r e q u e n t l y s e l e c t e d by the adult r a t s . R i c e f i e l d rats (R. r. mindanensis) show r i c e v a r i e t a l preference (79) and tend to p r e f e r Pal ay over Glutenous r i c e i n f i e l d rodent b a i t i n g programs. We have confirmed t h i s r i c e v a r i e t a l preference e f f e c t i n c l o s e d colony s e m i - f i e l d e n v i ronments with small groups o f a d u l t r i c e f i e l d r a t s . As i n d i c a t e d in Table I, the rats showed the highest consumption o f FK-178A r i c e (P < .01) and Milagrosa was p r e f e r r e d to the other two t e s t e d v a r i e t i e s , IR-20 and C-4 (P < .05). Under actual f i e l d c o n d i t i o n s , most rats would only contact one or two s i m i l a r v a r i e t i e s so t h a t these data do not allow f o r p r e d i c t i v e value i n f o r e c a s t i n g damage by the r a t s . However, the data do imply that s u b t l e changes i n the natural r i c e f l a v o r s of b a i t s could p o t e n t i a l l y i n f l u e n c e the extent o f b a i t acceptance. Some food h a b i t studies with stomach content or f e c a l matter analyses as measures take r e l a t i v e food a v a i l a b i l i t y {80, 81) i n t o account. Fellows and Sugihara (82), by t h i s method, were I F l e to determine t h a t Norway and Polynesian r a t s i n and near Hawaiian sugarcane f i e l d s showed high acceptance o f broad-leaved f r u i t s (melastoma, passion f r u i t , guava, thimble b e r r y , and popolo). The young (< 7 mo) of both r a t species showed avoidance o f grass veget a t i o n , whereas adults (7-24 mo) showed some passive acceptance. Such changes i n food acceptance could r e f l e c t e i t h e r ontogenetic ( e . g . , development o f a more adequate d i g e s t i v e system f o r e x p l o i t ing n u t r i e n t s from more food sources) or l e a r n i n g e f f e c t s ( e . g . ,


2.

SHUMAKE

Food Preference

29

Behavior

a s s o c i a t i n g the n u t r i t i v e value o f grasses with t h e i r f l a v o r s ) . F i e l d i n v e s t i g a t i o n s that consider what i s being eaten i n r e l a t i o n to abundance can provide some of the most useful preference data f o r w i l d b i r d s and mammals. However, these s t u d i e s can be extremely time-consuming and undoubtedly r e q u i r e a great deal o f systematic assessment. Table I.


Day 1 2 3 4 5 6 7 8 9 10 11 12

Rice b a i t consumption (g) o f eight r a t c o l o n i e s four v a r i e t i e s o f r i c e (Mean ± S . E . ) .

Milagrosa 18.7 15.1 14.4 8.9 15.6 6.6 4.9 4.0 10.1 6.9 5.0 3.9

+ + + + + + + + + + ± +

4.8 4.2 3.3 1.5 5.2 2.3 2.1 1.4 3.9 2.7 2.6 0.9

Rice v a r i e t y FK-178A IR-20 26.4 34.6 33.9 38.7 37.4 49.9 49.1 49.4 23.5 36.6 34.9 36.6

+ + + + + + + + + + + +

5.7 5.0 7.3 4.2 5.1 6.7 7.5 8.6 3.0 4.8 3.4 5.7

7.4 5.9 10.1 7.8 10.5 4.6 9.1 8.3 9.8 5.6 11.1 8.1

+ + + + + + + + + + + ±

for

C-4 2.4 1.7 2.6 1.6 4.2 1.3 3.1 3.6 4.0 1 .3 3.0 1 .1

7.4 9.4 7.0 8.6 8.8 9.9 6.6 10.2 8.5 12.5 2.5 6.6

+ + + + + + + + + + + +

2.5 1.9 1.5 1.4 1.4 3.2 2.2 3.3 2.0 5.5 1.0 2.5

Behavioral and e c o l o g i c a l e f f e c t s on f l a v o r acceptance or r e j e c t i o n i n b i r d s are more d i f f i c u l t to c h a r a c t e r i z e than those found in mammals. For example, Kare and Ficken (25) reviewed the e a r l y work concerned with t a s t e preference responses o f chickens with t r e a t e d versus untreated water over r e l a t i v e l y long exposure periods. I t was g e n e r a l l y found that chickens were i n d i f f e r e n t to a large number o f carbohydrates ( e . g . , s u c r o s e , glucose, l a c tose) except f o r xylose that was s t r o n g l y r e j e c t e d . Chickens a l s o c o n s i s t e n t l y r e j e c t e d c h l o r i d e s a l t s (ammonium, c a l c i u m , and f e r r i c ) at the higher c o n c e n t r a t i o n s . L i k e w i s e , most sour s o l u tions (organic and i n o r g a n i c acids) were r e j e c t e d by c h i c k e n s . The e f f e c t s of p r i o r experience on t a s t e preference behavior o f the fowl was demonstrated (25) by the f a c t t h a t ascending versus descending s e r i e s o f preference t e s t concentrations y i e l d v a s t l y d i f f e r e n t data. The importance o f p r i o r experience was confirmed by Davidson (83) who reported on preference behavior o f various b i r d species toward b e r r i e s and seeds i n natural s e t t i n g s . He has suggested that low consumption of a new food item by many b i r d species f o r 1-10 days i s o f no p a r t i c u l a r s i g n i f i c a n c e . Thus, c e r t a i n avian species may be extremely slow to change t h e i r normal feeding h a b i t s . D e t a i l e d and systematic l a b o r a t o r y f l a v o r preference e v a l u ations i n w i l d b i r d s are somewhat s c a n t . Working with f e r a l



30

FLAVOR

CHEMISTRY

OF ANIMAL

FOODS

pigeons, Duncan (84) demonstrated that both a c e t i c and hydroc h l o r i c acids (sour to man) produce pronounced r e j e c t i o n even at low concentrations ( e . g . , .005N a c e t i c a c i d ) . With sodium c h l o r i d e , Duncan has i n d i c a t e d that the preference - aversion f u n c t i o n i s s i m i l a r to that found in the r a t . That i s , preference was i n d i c a t e d at wt/vol concentrations below 1.0% and the b i r d s tended to r e j e c t concentrations greater than 1.0%. Some o f the d i s c r e p a n c i e s found f o r preference behavior o f the same general species ( e . g . , c h i c k e n s , q u a i l , pigeons) could be a f u n c t i o n of d i f f e r e n t methods o f measuring p r e f e r e n c e . Gent i l e (85), f o r example, found that chickens p r e f e r r e d c e r t a i n concentrations of sucrose and glucose (1-5%) when b r i e f - e x p o s u r e (< 3 minutes) preference t e s t s are used. G e n t i l e b e l i e v e s that the Kare and Medway (86) preference data f o r carbohydrates r e f l e c t not only t a s t e but a l s o p o s t i n g e s t i o n a l f a c t o r s . As summarized by Wenzel (62), s a l t s and b i t t e r t a s t i n g s t i m u l i ( e . g . , quinine h y d r o c h l o r i d e , sucrose octaacetate) are gene r a l l y r e j e c t e d by the pigeon, q u a i l , c h i c k e n , and Great T i t . Sour s t i m u l i ( a c e t i c and h y d r o c h l o r i c acids) are a l s o r e j e c t e d by most b i r d species t e s t e d except f o r q u a i l that p r e f e r s l i g h t l y sour tastes. The Great T i t and q u a i l a l s o p r e f e r glucose, but the pigeon and chicken are l e s s p r e d i c t a b l e . Using more natural t a s t e s t i m u l i , Yang and Kare (87) reported that c e r t a i n arthropod defensive s e c r e t i o n s could g r e a t l y a f f e c t red-winged b l a c k b i r d preference behavior. Both sal i c y ! a l d e h y d e and p-benzoquinone were r e j e c t e d at very low concentrations (0.025% wt/vol) in water s o l u t i o n s . The data may i n d i c a t e c e r t a i n i n s e c t species gain p r o t e c t i o n from b i r d p r é d a t i o n by v i r t u e of t h e i r chemical s e c r e t i o n s that t a s t e unpleasant or i r r i t a t i n g to b i r d s . Brower's (88) mimicry model o f s e l e c t i v e p r é d a t i o n proposes that b i r d s are i n i t i a l l y i n f l u e n c e d to feed on i n s e c t s by such f a c t o r s as movement, s i g h t , shape, and other nontaste cues. Howe v e r , a f t e r an unpleasant experience with these i n s e c t substances, c e r t a i n aspects o f the food item become avoided. These can i n c l u d e t a s t e as well as c o l o r , shape, t e x t u r e , and s i z e o f s p e c i f i c insects. Some i n t e r e s t i n g p o s s i b i l i t i e s f o r the development o f improved b i r d r e p e l l e n t chemicals are discussed along these l i n e s by Rogers (89). L i t t l e work has been done i n an attempt to i n c r e a s e b a i t acceptance by pest b i r d s . Bui l a r d (90) has provided some evidence that b a i t formulation could be a c r i t i c a l f a c t o r i n b i r d - b a i t i n g programs. Surface-coated grain b a i t s ( c o r n , wheat, or oats) cont a i n i n g a b i r d r e p e l l e n t (methiocarb) were shown to vary g r e a t l y in chemical concentration ( c . v . = 21-48%). Uniformly mixed and t a b l e t e d b a i t s had much l e s s chemical concentration v a r i a b i l i t y ( c . v . = 4.6-8.0%). These data would i n d i c a t e t h a t a more uniform r e p e l l e n t dosage can be achieved with t a b l e t e d m a t e r i a l . Most of the emphasis i n research and development o f b i r d cont r o l agents has been d i r e c t e d at the development of improved r e p e l l e n t s (89). Recent e f f o r t s i n t o t h i s research include an


2.

SHUMAKE

Food Preference

Behavior

31


e v a l u a t i o n of the mode o f a c t i o n o f commercially marketed " b i r d r e s i s t a n t " v a r i e t i e s o f sorghum (91). Although the data are not y e t f u l l y analyzed, i t appears that a rough negative c o r r e l a t i o n e x i s t s between polyphenolic content of the seed v a r i e t y and seed preference by quelea and red-winged b l a c k b i r d s . It i s hoped that the research i n t o the natural secondary plant substances [ e . g . , a l k a l o i d s (92) and a s t r i n g e n t s (93)] w i l l e v e n t u a l l y allow improved crop p r o t e c t i o n from d e s t r u c t i v e b i r d s p e c i e s . It i s a l s o hoped that t h i s research can lead to the development o f improved b i r d r e s i s t a n t grain v a r i e t i e s or the i s o l a t i o n and eventual marketing of extremely s a f e , e f f e c t i v e , and low-cost t a s t e r e p e l l e n t chemicals. Empirical Screening of F l a v o r i n g Agents, Enhancers, and Spices O b v i o u s l y , the f l a v o r chemist and h i s co-workers cannot be expected to research a l l of the f a c t o r s ( n u t r i t i o n a l , p h y s i o l o g i c a l , b e h a v i o r a l , e t c . ) that w i l l a f f e c t the preference behavior of a given b i r d o r mammal. Some researchers have t h e r e f o r e taken an e m p i r i c a l screening approach to the problem. For example, H i l k e r e t a l . (94) attempted to a l t e r food preferences o f rats using a mixture of black pepper, c l o v e s , and cinnamon each at 0.5% concentration. The s p i c e d d i e t was fed to weanling rats f o r 5 weeks followed by a 2-week f r e e - c h o i c e p e r i o d . The young rats consumed s i g n i f i c a n t l y l e s s of the s p i c e d d i e t compared with the untreated d i e t , whereas adults showed no p a r t i c u l a r preference between the d i e t s . Spices and f l a v o r i n g s are thought (95) to stimulate a p p e t i t e and g a s t r o i n t e s t i n a l readiness f o r r e c e i v i n g food. However, a more recent (23) viewpoint on t h i s s u b j e c t i s that the f l a v o r s o f a d d i t i v e s p r i m a r i l y serve as d i s t i n c t i v e t a s t e and odor cues f o r the s a f e t y and f a m i l i a r i t y with c e r t a i n foods eaten by man. I f t h i s viewpoint i s c o r r e c t , the screening of f l a voring agents and spices to increase b a i t consumption by rodents in a g r i c u l t u r a l areas may be v a l u e l e s s . B a i t a d d i t i v e s that enhance n a t u r a l l y p r e f e r r e d food f l a v o r s could o f f e r a p o t e n t i a l means o f improving b a i t i n g programs by a t t r a c t i n g l a r g e r numbers o f rats to the b a i t s and by i n c r e a s i n g t o x i c b a i t consumption. We have not been able to demonstrate that p r o t e i n f l a v o r enhancers ( i . e . , 5 ' - r i b o n u c l e o t i d e s ) (96, 9 7 ) , p o t e n t i a t o r s such as monosodium - L - glutamate, or sweetness enhancers added to ground r i c e b a i t have any p a r t i c u l a r l y strong e f f e c t s on the choice behavior o f r i c e f i e l d r a t s from the P h i l i p pines (Table II). These f i n d i n g s tend to support the views that the t a s t e and odor perceptual systems of man versus rodent are v a s t l y d i f f e r e n t (1, 9 8 ) , and t h a t man's acceptance o f some o f these products may~be, i n large p a r t , c u l t u r a l l y determined (23). Food odors as area a t t r a c t a n t s to rodents f o r c o n t r o l purposes have been postulated f o r many years (99^ 100, 101, 103). R e i f f (99) took a r a t h e r a n a l y t i c approach to the f l a v o r p r e f e r ence prôFlem i n rodents by i n v e s t i g a t i n g c e r t a i n chemical compounds


32

FLAVOR


Table II.

No.

1 2 3 4 5 6 7 8 9 10 11 12

CHEMISTRY

OF ANIMAL

Mean percent preference ± S.E.M. f o r 12 b a i t each t e s t e d at three c o n c e n t r a t i o n s .

Addi t i v e name

Concentrât!on C-j C

a

V-50 Dried humeri Zymino Canned food flavor Cereal f l a v o r Vegamine #1 Vegamine #28 Vegamine #69 V 84T Soy sugar V e l t o l plus Sugar

Control

FOODS

additives

b

C

2

3

47.4±1.0 49.2±1.0 50.3±1.1

47.0±2.7 45.1+5.6 42.0±4.8

45.3±4.2 39.9±5.3 47.3±6.8

29.7±6.5 48.6±4.8 43.H3.8

51.7±1.8 50.0+0.8 48.7±2.0 50.7±1.2 52.1+0.8 48.2±0.8 50.1+1.0 51 .9±1.7 51.7±0.8

42.1±4.2 51.1+1.7 46.3+2.5 43.8±4.7 43.1±6.3 44.1±2.1 46.H5.1 51.8±0.7 57.6±3.2

30.6+7.8 39.4±5.0 50.1+2.9 41.5±6.3 41,4±4.9 38.0±4.0 52.9±2.1 46.1±0.8 51.9+2.6

38.6±4.8 37.7+5.2 38.3±6.6 49.6±5.2 44.6±6.1 42.H3.1 49.8±4.0 44.7±1.7 60.2±3.7

C

A d d i t i v e numbers 1-10 are p r o t e i n h y d r o l y s a t e s ; number 11 i s a sweetness enhancer; number 12 i s a n u t r i t i v e sweetener. A d d i t i v e numbers 1-8 were t e s t e d C = 1.2%; number 9 t e s t e d a t : C-, numbers 10 and 11 t e s t e d a t : Ci = number 12 a t : Cj = 10%, C = 2 0 % ,

b

3

2

c

at: C-j = 0.3%, C = 0.6%, = .15%, Co = 0.3%, Co = 0.75%; .10%, C = 0.2%, Co = 0.4%; C = 40%. 2

2

3

Ρ (C3 > Control) < .05.



2.

SHUMAKE

Food Preference

Behavior

33

commonly found i n food items eaten by rats and mice. C e r t a i n t e r t i a r y amines, e s s e n t i a l o i l s , and aldehydes are found n a t u r a l l y in meats, vegetables, cereal g r a i n s , and d a i r y products known to be r e a d i l y eaten by r a t s . Although these elemental f l a v o r compounds can d i r e c t l y c o n t r i b u t e to the t o t a l f l a v o r o f c e r t a i n food items f o r r a t s , t h e i r combined a c t i o n i s g e n e r a l l y much stronger than the a c t i o n o f any s i n g l e compound. We have found t h i s same general e f f e c t with r i c e f i e l d rats (18). Of 20 candidate food odor compounds evaluated with an automated odor t e s t device (102), none produced as much i n v e s t i g a t i o n as the food odor (Purina Laboratory Chow) a s s o c i a t e d with t h e i r normal l a b o r a t o r y d i e t (see Table III). B u l l (103) came to a s i m i l a r c o n c l u s i o n i n h i s e v a l uation of more general food odors ( f i s h , b e e f , dog f o o d , coconut o i l ) and f l a v o r i n g agents ( r a s p b e r r y , aniseed o i l ) . Even with " r e p e l l e n t " odors, strong odor r e p e l l e n t e f f e c t s were only observed when the a c t i v e agent ( e . g . , Rotran 55) was added to the food i n the hoppers. A g a i n , f a m i l i a r i t y with the food f l a v o r , along with texture and p a r t i c l e s i z e , proved to be more i n f l u e n t i a l on r a t feeding behavior than the presence or absence o f novel food odors. For w i l d rodents, and perhaps o t h e r macro-osmic mammals, food odor a t t r a c t a n t s are h e a v i l y dependent upon the animals' past experience i n t a s t i n g , i n g e s t i n g , and d e r i v i n g n u t r i t i o n a l b e n e f i t s from the food. Hansson (104) noted t h a t f i e l d v o l e s , bank v o l e s , and wood mice showed increased gnawing on s t i c k s impregnated with various vegetable o i l s . Part o f t h i s response appeared to be r e l a t e d to texture changes i n the wood as the o i l s penetrated i t . Some of the response, however, a l s o appeared to be r e l a t e d to the presence of c e r t a i n long-chain f a t t y acids ( e . g . , o l e i c , l i n o l e i c ) i n the oils. We have compared the e f f e c t s o f adding 10% vegetable or g r a i n o i l s to r i c e b a i t with independent groups o f R_. jr. mindanensis. Rats i n a l l groups showed r e l i a b l e preference f o r soybean, c o r n , peanut, l i n s e e d , palm k e r n e l , s a f f l o w e r , coconut, and r i c e o i l over untreated b a i t m a t e r i a l . As can be seen i n Table IV, Freon-11 e x t r a c t e d r i c e o i l produced the most c o n s i s t e n t e f f e c t on r i c e b a i t consumption. A l l o i l s changed the t e x t u r e as well as t a s t e and odor of the b a i t . This texture change e f f e c t was evaluated by comparing the preference responses f o r the s a f f l o w e r o i l ( h i g h - o l e i c type) with the other o i l s s i n c e t h i s material has been reported (105) to be odorless and t a s t e l e s s to man. Supposedly, even with a very low t a s t e or odor component to r a t s , s a f f l o w e r o i l s t i l l produced almost 90% preference a f t e r 6 exposure t e s t days. The r i c e o i l was the most c o n s i s t e n t l y p r e f e r r e d mater i a l , probably because i t acted to i n t e n s i f y the f l a v o r of a n o r mally h i g h l y p r e f e r r e d and f a m i l i a r food ( i . e . , r i c e ) . Intensifying

F l a v o r with Extracted or V o l a t i l i z e d Compounds

The e m p i r i c a l screening approach c a n , at times, lead to s u c c e s s f u l development of improved animal food f l a v o r i n g agents as


34

FLAVOR


Table III.

CHEMISTRY

OF ANIMAL

FOODS

Odor preference test results when 20 candidate mate r i a l s were compared with investigation time toward the familiar food odor (Purina Laboratory Rat Chow).

Candidate food odor attractant Soybean o i l Isovaleric aldehyde N^butyldiethanolamine N-proplyamine Peanut o i l 2-Furaldehyde Linseed o i l Εthy 1 diethanolami ne Sassafrass o i l Dihydroxyethy1 ani1ine Wintergreen o i l Corn o i l Hexanoic acid N^octylamine N-amylamine Isobutylamine Cod l i v e r o i l ( n-p ropy 1 ) -b enzy 1 ami ne Valerone JN-hexylamine

Percent response (mean ± S.E.) 94.6 94.3 87.5 80.0 80.0 77.5 76.2 75.6 74.4 72.5 72.2 67.5 65.9 61.9 60.0 52.4 50.0 40.0 36.4 35.6

+ + ± + + + + + + + + + + + + + + + + +


23.0 21.6 38.6 56.4 18.3 31.3 24.1 11.5 23.9 58.8 16.9 16.3 25.9 26.6 42.9 19.7 19.3 28.1 4.5 3.6


Soybean

54.6±32.8 60.8±29.3 76.6+36.1 75.0±34.2 72.6±35.1 79.3+36.0

69.8±33.9

1 2 3 4 5 6

Mean +S.D.

73.0±36.7

61.8±30.3 67.1+34.8 76.8±38.6 75.3+38.6 78.8±38.9 78.2±39.1

Corn

80.U15.6

55.6±24.9 79.9±12.3 83.0+12.6 84.9±15.0 88.H13.9 89.3±14.8

Peanut

85.4±17.3

71.3+21.6 88.1±14.4 88.4±12.9 90.3±17.2 88.5±18.0 86.0±19.5

Linseed

Oil

74.0+14.9

64.8±19.3 78.8+12.4 77.5+11.7 79.7±10.3 71.0+15.2 72.3+20.2

Palm kernel

81.4±26.0

65.9±38.4 80.2±23.7 82.3±25.0 82.3±25.0 88.3+21.5 89.6+22.2

Higholeicsafflower

64.2±31.2

25.9±32.8 66.8±35.8 71.U38.5 69.9±35.7 87.2± 7.3 64.H37.1

Coconut

94.0± 8.0

83.9± 6.8 97.9+ 2.3 98.3± 3.9 96.2+ 7.0 93.8±14.9 94.U13.1

Freon-11 extractedrice o i l

Mean ± S.D. percent preference o f r i c e f i e l d r a t s f o r r i c e c o n t a i n i n g o i l - t r e a t e d versus untreated r i c e .

Day

Table IV.



36

FLAVOR

CHEMISTRY

OF ANIMAL

FOODS

i n d i c a t e d above. However, a more d i r e c t approach to the problem involves the study of what the animal normally or n a t u r a l l y p r e fers i n i t s native h a b i t a t . This most p r e f e r r e d (or l e a s t p r e f e r r e d ) food i s then chemically analyzed i n conjunction with a s e r i e s of behavioral b i o a s s a y s . To i l l u s t r a t e t h i s approach, I have o u t l i n e d the f o l l o w i n g examples. Rice and Church (106) presented evidence that b l a c k - t a i l e d deer p r e f e r d i s t i l l e d water t r e a t e d with low concentrations o f water or ethanol e x t r a c t s from foods normally accepted by deer ( b i t t e r brush, D o u g l a s - f i r , and hemlock). In response to c e r t a i n organic acids commonly found i n plants browsed by ungulates, there were pronounced sex d i f f e r e n c e s . Bucks s t r o n g l y p r e f e r r e d the intermediate concentrations o f malic a c i d but showed weaker p r e f erence f o r s u c c i n i c and c i t r i c a c i d s . Does, on the other hand, showed weak to strong r e j e c t i o n of these same a c i d c o n c e n t r a t i o n s . This report i n d i c a t e d that e x t r a c t e d f l a v o r compounds found i n natural food sources of b l a c k - t a i l e d deer can g r e a t l y a f f e c t t h e i r consummatory d r i n k i n g behavior. Mugford (107) reported that both the duration and the s i z e of meals eaten by domestic cats can be increased by p e r f u s i n g normally p r e f e r r e d meat odors (cooked r a b b i t ) through t h e i r maintenance d i e t (dry food). Le Magnen (108) and Larue (109) have a l s o noted that food odors can i n f l u e n c e feeding patterns in r a t s . For c e r t a i n predatory mammals such as foxes (65), food odors may e l i c i t food seeking regardless o f experience. For many other mammalian species [ e . g . , Norway rats ( 4 ) , polecats (66), and r o o f rats (58)] food f l a v o r preferences are~highly dependent upon experience with the food or prey s p e c i e s . As another example o f an a l t e r n a t e approach to e m p i r i c a l s c r e e n i n g , B u l l a r d and Shumake (110) evaluated e i g h t p o t e n t i a l f l a v o r components of whole g r a i n , uncooked r i c e with r i c e f i e l d rats in an attempt t o increase the p a l a t a b i l i t y o f ground r i c e baits. Rice bran o i l , the a c e t o n i t r i l e e x t r a c t o f r i c e bran o i l , the ether e x t r a c t of ground r i c e , endosperm, r i c e p o l i s h , r i c e bran, r i c e bran v o l a t i l e s , and whole grain r i c e v o l a t i l e s were evaluated as a d d i t i v e s to ground r i c e with a group o f 12 r a t s . A b r i e f exposure t a s t e preference device (18^, 111) was used i n these evaluations to ensure that p o s t i n g e s t i o n a l f a c t o r s r e l a t e d to c a l o r i c content or d i g e s t a b i l i t y would not confound preference test results. The whole grain r i c e v o l a t i l e s material was the only one found to r e l i a b l y i n c r e a s e both consumption and feeding time. In a l a t e r s e m i - f i e l d pen t e s t , r i c e v o l a t i l e s t r e a t e d b a i t was p r e f e r r e d (P < .05) over w h o l e - g r a i n , granulated, and soy bean o i l (1%) t r e a t e d r i c e . The e f f e c t of the r i c e v o l a t i l e s a d d i t i v e on t o x i c b a i t consumption was then evaluated (110). Two groups o f rats were given a choice between e i t h e r 0.2% z i n c phophide t r e a t e d r i c e and untreated r i c e , or 0.2% z i n c phosphide t r e a t e d r i c e with the r i c e v o l a t i l e s added and untreated r i c e . This l a t t e r group showed almost double the t o x i c r i c e b a i t consumption and a m o r t a l i t y o f


2.

SHUMAKE

Food Preference

Behavior

37

88%. The c o n t r o l group r a t s (without r i c e v o l a t i l e s on t o x i c r i c e b a i t ) showed only 50% m o r t a l i t y (P < .005). This experiment i n d i c a t e d to us that f l a v o r s from a p r e f e r r e d food f o r r a t s could be f u r t h e r i n t e n s i f i e d to increase p a l a t a b i l i t y . T h i s increased p a l a t a b i l i t y had the advantage of i n c r e a s i n g t o x i c b a i t consumpt i o n , presumably because we were working with h i g h l y f a m i l i a r r i c e f l a v o r s p r e f e r r e d by r i c e f i e l d rats (112, 113).


Conclusions I t appears to be u n l i k e l y t h a t food f l a v o r i n g agents, s p i c e s , and enhancers developed f o r humans w i l l e f f e c t strong and l o n g l a s t i n g preference behavior m o d i f i c a t i o n s i n b i r d s and mammals. Food f l a v o r f a m i l i a r i t y may be the s i n g l e , most important f a c t o r c o n t r o l l i n g food preference behavior o f w i l d species (8, £ 3 , 77). Mammals show highest acceptance of f a m i l i a r foods, but they a l s o tend to sample small amounts o f any new food item placed i n t h e i r environment ( 4 ) . Some b i r d species are extremely r e s i s t a n t to changing t h e i r preference behavior f o r c e r t a i n food items (83), but there i s no compelling evidence proving t h a t food f l a v o r i s less important to b i r d s than to mammals (62, 85, 89). For mammals (and p o s s i b l y b i r d s a l s o ) , food t e x t u r e , p a r t i c l e s i z e , and feeder l o c a t i o n can sometimes produce as much, or more, e f f e c t than odor and t a s t e of food (103, 104). Preference t e s t r e s u l t s f o r a given f l a v o r a d d i t i v e and species w i l l vary with methodological f a c t o r s such as: length of t e s t , previous experience of the t e s t animal, and t e s t f l u i d or food base used. In g e n e r a l , t a s t e preference evaluations with standard compounds ( e . g . , NaCl, s u c r o s e , HC1, and quinine) do not y i e l d data that allow p r e d i c t i o n o f the kinds o f food f l a v o r s w i l d animals w i l l most r e a d i l y accept and p r e f e r i n a given ecosystem. Food habit s t u d i e s that take i n t o account the r e l a t i v e abundance of the food items under study, can sometimes y i e l d the most p r o ductive and p r e d i c t i v e i n f o r m a t i o n . Empirical screening as a method of searching f o r animal food a t t r a c t a n t s or r e p e l l e n t s can be an expensive e f f o r t and i s , at times, not worthy o f the r e s e a r c h e r ' s time. Attempts to c o r r e l a t e chemical s t r u c t u r e with r e p e l l e n t e f f e c t s e l i c i t e d by compounds from an e m p i r i c a l s c r e e n ing program i n rodents have l e d to some degree o f p r e d i c t i o n (114), but the e f f o r t and expense o f such a c t i v i t y may not be e a s i l y justified. C o r r e l a t i o n o f chemical s t r u c t u r e with b i o l o g i c a l l y a c t i v e compounds i s o l a t e d from natural sources ( e . g . , secondary plant substances) may be a more f r u i t f u l approach. Our approach to developing an improved and i n t e n s i f i e d r i c e f l a v o r f o r b a i t i n g rats with r i c e has been as f o l l o w s . F i r s t , the natural or normal food habits of the r i c e f i e l d r a t were evaluated under f i e l d c o n d i t i o n s (113). Second, t h i s preference response was then confirmed f o r r i c e under b r i e f - e x p o s u r e , two-choice l a b o r a t o r y t e s t c o n d i t i o n s . T h i r d , the most f a m i l i a r and p r e f e r r e d food, r i c e , was separated i n t o gross chemical components ( e . g . ,


FLAVOR


38

CHEMISTRY

O F ANIMAL

FOODS

bran, endosperm, o i l , f l a v o r v o l a t i l e s , e t c . ) (110), and each o f these was s e p a r a t e l y added back to ground r i c e . A d d i t i o n a l behav i o r a l t e s t s were then conducted to evaluate p o t e n t i a l a p p l i c a t i o n of the most p r e f e r r e d f l a v o r component ( e . g . , i n c r e a s i n g t o x i c b a i t consumption, i n c r e a s i n g b a i t p a l a t a b i l i t y , and a t t r a c t i n g rats from a d i s t a n c e ) . I f a l l l a b o r a t o r y and s e m i - f i e l d e v a l u a tions continue to be p o s i t i v e and c o n s i s t e n t , we w i l l then proceed to s m a l l - and l a r g e - s c a l e f i e l d t e s t i n g . A f t e r some p o s i t i v e con f i r m a t i o n from the f i e l d t e s t s , we w i l l then e i t h e r synthesize the natural r i c e v o l a t i l e s f l a v o r o r devise a commercial e x t r a c t i o n process f o r producing t h i s b a i t a d d i t i v e . The approach to developing improved b i r d r e p e l l e n t s can p r o ceed along these same l i n e s . There are numerous seeds, b e r r i e s , and plants that b i r d s normally a v o i d . Part o f t h i s avoidance could be due to conditioned aversion (89) or to a v e r s i v e t a s t e (93). Regardless o f the p h y s i o l o g i c a l and behavioral mechanisms involved i n the r e p e l l e n t e f f e c t s , I b e l i e v e the trend toward e x p l o i t a t i o n o f natural food items as a source f o r developing more a t t r a c t i v e or r e p e l l e n t animal food f l a v o r s w i l l c o n t i n u e . Acknowledgments Thanks are due to Mr. R. W. Bui l a r d and Dr. R. T . Sterner f o r reviewing e a r l y d r a f t s o f the manuscript. The author i s a l s o g r a t e f u l f o r the t e c h n i c a l a s s i s t a n c e o f Mr. K. A. Crane and Mr. S. E. Gaddis o f the Denver W i l d l i f e Research Center as well as personnel at the Rodent Research Center, Los Banos, The P h i l i p p i n e s . This work was supported, i n p a r t , with funds provided t o the U.S. Fish and W i l d l i f e S e r v i c e by the U.S. Agency f o r I n t e r n a t i o n a l Development under the p r o j e c t "Control o f Vertebrate Pests: Rats, B a t s , and Noxious B i r d s , " PASA RA(ID) 1-67.

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