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Journal of Chemical Ecology [joec]

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Style file version Nov. 19th, 1999

c 2001) Journal of Chemical Ecology, Vol. 27, No. 10, October 2001 (°

GUSTATORY RESPONSIVENESS TO POLYCOSE IN FOUR SPECIES OF NONHUMAN PRIMATES

MATTHIAS LASKA,1,* STEFANIE KOHLMANN,1 HANS-PETER SCHEUBER,2 LAURA TERESA HERNANDEZ SALAZAR,3 and ERNESTO RODRIGUEZ LUNA3 1 Department

of Medical Psychology

2 Department

of Surgery University of Munich Medical School D-80336 Munich, Germany 3 Instituto

de Neuro-Etologia Universidad Veracruzana C.P. 91000 Xalapa, Mexico

(Received October 24, 2000; accepted May 29, 2001)

Abstract—The taste responsiveness of six squirrel monkeys, five pigtail macaques, four olive baboons, and four spider monkeys to polycose, a starchderived polysaccharide, was assessed in two-bottle preference tests of brief duration (2 min). In experiment 1, the monkeys were given the choice between tap water and defined concentrations of polycose dissolved in tap water. In experiment 2, the animals were given the choice between polycose and sucrose, fructose, glucose, lactose, and maltose presented in equimolar concentrations of 100 and 200 mM, respectively. The animals were found to prefer concentrations of polycose as low as 10 mM (pigtail macaques), 30 mM (olive baboons and spider monkeys), and 60 mM (squirrel monkeys) over tap water. Relative taste preferences were stable across the concentrations tested and indicate an order of relative effectiveness (sucrose > polycose ≥ maltose) in squirrel monkeys, spider monkeys, and olive baboons that is similar to the order of relative sweetness in humans. Pigtail macaques, however, displayed an order of relative effectiveness (maltose > polycose ≥ sucrose) that differs markedly from that found in the other primate species tested and is similar to relative taste preferences found in rodents such as rats. Both the high sensitivity of the pigtail macaques to polycose and their vivid predilection for this polysaccharide and its disaccharide constituent maltose suggest that Macaca nemestrina, unlike other primates, but like rodents, may have specialized taste receptors for starch. Key Words—Gustatory preference thresholds, relative taste preferences, polycose. *To whom correspondence should be addressed; e-mail: [email protected]

1997 C 2001 Plenum Publishing Corporation 0098-0331/01/1000-1997$19.50/0 °

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LASKA, KOHLMANN, SCHEUBER, SALAZAR, AND LUNA INTRODUCTION

Carbohydrates, in the form of sugar and starch, represent a major source of metabolic energy for a great number of animal species. With the exception of some fruits, plants usually contain much more starch than sugar (Hizukuri, 1996). However, whereas taste perception of sugars has been the subject of considerable research at both the behavioral and the electrophysiological level in a variety of species (Spector, 2000), studies on the taste of starch have been restricted to the rat. One possible reason for this bias may be the fact that sugars have a highly attractive taste both for humans and many other species, whereas starch has a rather bland taste for humans and has been assumed to be tasteless and, thus, unattractive to other animals as well (Kare, 1971; Pfaffmann, 1977). Comparative studies of sugar taste sensitivity and preference have revealed marked differences among species. With regard to sensitivity, for example, preference thresholds for sucrose may differ by more than two orders of magnitude, even between closely related species belonging to the same order of mammals, such as the spider monkey and the slow loris (Laska et al., 1996; Glaser, 1986). While many species display a strong preference for the taste of sugars, others, such as cats and chickens, are indifferent to soluble carbohydrates (Kare, 1971; Beauchamp et al., 1977). Species have also been found to differ in their relative preference for individual sugars. Among species that prefer sucrose, some, such as rats, spiny mice, and gerbils, show a preference for maltose, while others, such as dogs, armadillos, or cows, are either indifferent or averse to maltose (Kare, 1971; Feigin et al., 1987). In contrast to the wealth of knowledge about differences among species regarding their responsiveness to sugars, little is known as to whether species also differ in their sensitivity and preference for starch and other polysaccharides. In a series of landmark studies, Sclafani and coworkers have shown that rats are strongly attracted to starch and starch-derived polysaccharides such as polycose (Sclafani and Clyne, 1987). Further, they showed that rats have a markedly lower taste preference threshold for polycose than for sugars such as sucrose (Sclafani and Nissenbaum, 1987), and that, at least at concentrations up to 300 mM, they clearly prefer this polysaccharide to sucrose and other mono- or disaccharides (Sclafani and Mann, 1987). These results, along with other findings, led the authors to conclude that rats have two types of carbohydrate taste receptors, one for polysaccharides and one for sucrose, which produce qualitatively distinct gustatory sensations (Nissenbaum and Sclafani, 1987). Recent electrophysiological studies lend support to this idea, as they have demonstrated the neural activity profile of the rat evoked by polycose and other starch-derived polysaccharides to be markedly different from those of other taste stimuli termed sweet by humans (Giza et al., 1991; Sako et al., 1994).

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The presumed function of polysaccharide taste receptors is to facilitate the identification of starch-rich foods (Sclafani, 1991). This latter supposition is supported by findings that showed other rodents, such as gerbils, hamsters, and spiny mice, which also feed on grains and other parts of plants containing high amounts of starch, display similar preferences for polysaccharides as rats (Feigin et al., 1987; Rehnberg et al., 1996). Given the paucity of data on taste sensitivity and preference for polysaccharides in species other than rodents, we decided to test the gustatory responsiveness of four species of nonhuman primates to polycose. This highly water-soluble mixture of glucose chains with α-1,4 linkages (2% glucose, 7% maltose, 55% maltooligosaccharides of 3–10 glucose units, and 36% maltopolysaccharides of >10 glucose units) is produced from an acid enzyme hydrolysis of corn starch and, apart from its frequent use as a taste stimulus in studies of gustatory performance in rodents, it is also used as a dietary supplement in humans. The four primate species employed here, squirrel monkeys, spider monkeys, olive baboons, and pigtail macaques, are known to differ—at least to some degree—in their dietary habits (Clutton-Brock and Harvey, 1977; Caldecott, 1986; Chapman, 1987; Ross, 1992), allowing us to address the question of whether possible differences in taste responsiveness to polysaccharides in nonrodent mammals may reflect an evolutionary adaptation to dietary specialization. Thus, the aims of the present study are threefold: (1), to assess whether different species of nonhuman primates are attracted to polycose; (2), to determine taste preference thresholds for this substance as a first and conservative approximation of gustatory sensitivity; and (3), to assess relative preferences for this polysaccharide in direct comparison with five food-associated mono- and disaccharides. The possibility of including two New World primate species and two Old World primate species in this study allowed us to address additionally the question of whether the degree of phylogenetic relatedness rather than dietary specialization may affect the taste responsiveness of nonhuman primates to polysaccharides.

METHODS AND MATERIALS

Animals. Testing was carried out with six male adult squirrel monkeys (Saimiri sciureus), two male and three female adult pigtail macaques (Macaca nemestrina), two male and two female adult olive baboons (Papio hamadryas anubis), and one male and three female adult spider monkeys (Ateles geoffroyi). Animals of all four species were housed as social groups in enclosures with adjacent single cages that could be closed by sliding doors to allow temporary separation of animals for individual testing [for details of maintenance see Laska (1996, 2000) and Laska et al. (1996, 1999a,b)]. Animals were fed commercial monkey chow, fresh fruit,

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and vegetables ad libitum but were deprived of water overnight before testing on the following morning. The amount of food offered daily to the animals was such that leftovers were still present on the floor the next morning and, thus, it was unlikely that ravenous appetite affected the animals’ ingestive behavior in the tests. Procedure. Gustatory responsiveness to polycose (reagent grade, Ross Products, Columbus, Ohio) was assessed by using a two-bottle preference test of short duration (Richter and Campbell, 1940). Twice each day, approximately 1 and 2 hr before feeding, the animals were separated and allowed 2 min to drink from a pair of simultaneously presented graduated cylinders with metal drinking spouts. In experiment 1, monkeys were given a choice between tap water and defined concentrations of polycose dissolved in tap water. Testing started at a concentration of 200 mM and proceeded in the following steps (100, 50, 20, 10 mM, etc.) until the animals failed to show a significant preference. Subsequently, intermediate concentrations were tested in order to determine the preference threshold value more exactly. To keep up the animals’ motivation and willingness to cooperate, testing did not follow a strict descending staircase procedure but followed a pseudorandomized scheme in which trials with high and, thus, presumably readily perceptible and attractive concentrations of polycose were alternated with low and presumably less attractive concentrations. In experiment 2, monkeys were given a choice between equimolar concentrations of polycose and sucrose, fructose, glucose, maltose, and lactose (reagent grade, Merck, Darmstadt, Germany). In order to assess whether preferences are stable at different concentration levels, two test series were performed at 100 and 200 mM, respectively. In both experiments, each pair of stimuli was presented 10 times, and the position of the stimuli was randomized in order to counterbalance possible position preferences. All animals had served in previous studies using the same method (Laska, 1994, 1996, 1997, 1999, 2000; Laska et al., 1996, 1998, 1999a,b, 2000). They were trained to enter the single cages voluntarily and were completely accustomed to the procedure. The experiments reported here comply with the Guide for the Care and Use of Laboratory Animals (National Institutes of Health Publication no. 86-23, revised 1985) and also with current German and Mexican laws. Data Analysis. For each animal, the amount of liquid consumed from each bottle was recorded, summed for the 10 test trials with a given stimulus combination, converted to percentages (relative to the total amount of liquid consumed from both bottles), and 66.7% (i.e., 2/3 of the total amount of liquid consumed) was taken as the criterion of preference. This rather conservative criterion was chosen for reasons of comparability of data, as the same criterion had been used in previous studies using the same method with the same primate species (Laska, 1994, 1996, 1997, 1999, 2000; Laska et al., 1996, 1998, 1999a,b, 2000), and in order to avoid misinterpretation of data due to a too-liberal criterion.

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Additionally, two-tailed binomial tests (Siegel and Castellan, 1988) were performed, and an animal was only regarded as significantly preferring one of the two stimuli if it reached the criterion of 66.7% and consumed more from the bottle containing the preferred stimulus in at least 8 of 10 trials (binomial test, P < 0.05). Preliminary analysis of the data indicated that there were no reliable differences in choice behavior and liquid consumption between the males and females of a species nor between the first and the second presentation of the day. Intraindividual variability in the amount of liquid consumed across the 10 test trials with a given stimulus combination was low and averaged less than 20%. Thus, a theoretically possible bias in the overall preference score due to excessive drinking in aberrant trials did not occur. Therefore, the data for the males and females of a species obtained in the 10 test trials were combined and are reported as group means and standard deviations. Comparisons of the rank order of preference for the five saccharides tested across species and concentrations, respectively, were made by calculating Spearman rank-order correlation coefficients (rs ), which were tested for significance by computing z scores (Siegel and Castellan, 1988).

RESULTS

Experiment 1. Figure 1 shows the taste preference thresholds for polycose to be 10 mM in the pigtail macaques, 30 mM in the spider monkeys and the olive baboons, and 60 mM in the squirrel monkeys. All animals of a given species significantly discriminated these concentrations from tap water, and in some cases single individuals even scored slightly lower preference threshold values. All animals, however, failed to show a significant preference for the lowest concentrations presented, suggesting that the preference for higher concentrations was indeed based on the chemical nature of the stimulus. In most cases, interindividual variability of scores was low for both sub- and suprathreshold concentrations tested (cf. SDs in Figure 1). Across-species comparisons of the degree of preference for polycose displayed by the four primate species showed that at concentrations of 50, 100, and 200 mM, respectively, the pigtail macaques were more attracted to the polysaccharide than the other species. Experiment 2. Figure 2 shows the mean group preferences of the four primate species given a choice between polycose and maltose, sucrose, fructose, glucose, and lactose, presented at equimolar concentrations of 100 mM. Squirrel monkeys significantly preferred sucrose and fructose over polycose and showed a trend to prefer polycose over maltose, glucose, and lactose that fell short of statistical significance. Spider monkeys significantly preferred sucrose and fructose over polycose, polycose over glucose and lactose, and showed a

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FIG. 1. Taste responsiveness of six squirrel monkeys, five pigtail macaques, four spider monkeys, and four olive baboons to aqueous solutions of polycose tested against tap water. Each data point represents the mean value (±SD) of 10 test trials of 2 min per animal.

nonsignificant trend to prefer polycose over maltose. Olive baboons significantly preferred sucrose over polycose; polycose over maltose, glucose, and lactose; and showed a nonsignificant trend to prefer polycose over fructose. Pigtail macaques significantly preferred maltose over polycose; polycose over fructose, glucose, and maltose; and showed a trend to prefer polycose over sucrose that fell short of statistical significance. Interindividual variability within a given species was remarkably low, as can be inferred from the small SDs, and with only few exceptions all animals of a species either reached the criterion of preference (>66.7% of total consumption, plus binomial test, P < 0.05) in a given task or all failed to do so.

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FIG. 2. Relative taste preferences of six squirrel monkeys, five pigtail macaques, four spider monkeys, and four olive baboons given a choice between aqueous solutions of polycose and sucrose, fructose, glucose, maltose, and lactose presented at equimolar concentrations of 100 mM. The shaded portion of a bar indicates the preference for a given saccharide and the white portion of a bar indicates the preference for polycose. Each bar represents the mean value (±SD) of 10 test trials of 2 min per animal.

Across-species comparisons of the patterns of preferences displayed by the four primate species showed that the preference rankings of squirrel monkeys, spider monkeys, and olive baboons for the five mono- and disaccharides tested against polycose were the same (sucrose > fructose > maltose > glucose > lactose) and, thus, significantly correlate with each other (Spearman, P < 0.05 for all pairs). The preference ranking of pigtail macaques for the same sugars tested against polycose (maltose > sucrose > fructose > lactose > glucose) was markedly different from that of the other three species (Spearman, P > 0.05 for all pairs). Figure 3 shows the mean group preferences of the four primate species given a choice between equimolar concentrations (200 mM) of polycose and maltose, sucrose, fructose, glucose and lactose. Squirrel monkeys significantly preferred sucrose and fructose over polycose and failed to show any preference in the combinations of polycose versus maltose, glucose, and lactose. Spider monkeys significantly preferred sucrose over polycose, polycose over glucose and lactose, and showed a nonsignificant trend to prefer fructose and maltose over polycose. Olive baboons significantly preferred sucrose

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FIG. 3. Relative taste preferences of six squirrel monkeys, five pigtail macaques, four spider monkeys, and four olive baboons given a choice between aqueous solutions of polycose and sucrose, fructose, glucose, maltose, and lactose presented at equimolar concentrations of 200 mM. The shaded portion of a bar indicates the preference for a given saccharide and the white portion of a bar indicates the preference for polycose. Each bar represents the mean value (±SD) of 10 test trials of 2 min per animal.

over polycose, polycose over glucose and lactose, and showed a nonsignificant trend to prefer polycose over maltose and fructose. Pigtail macaques significantly preferred polycose over fructose, glucose, and maltose and showed a trend to prefer maltose and sucrose over polycose that fell short of statistical significance. Interindividual variability within a given species was remarkably low as can be inferred from the small SDs, and, with only few exceptions, all animals of a species either reached the criterion of preference in a given task or all failed to do so. Across-species comparisons of the patterns of preferences displayed by the four primate species revealed that the preference rankings of squirrel monkeys, spider monkeys, and olive baboons for the five mono- and disaccharides tested against polycose were the same (sucrose > fructose > maltose > glucose > lactose) and, thus, significantly correlate with each other (Spearman, P < 0.05 for all pairs), whereas the preference ranking of the pigtail macaques for the same sugars tested against polycose (maltose > sucrose > fructose > lactose > glucose) was markedly different from that of the other three species (Spearman, P > 0.05 for all pairs).

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Within-species comparisons of the patterns of preference across the two concentrations tested revealed that the preference rankings of all four primate species for the five mono- and disaccharides tested against polycose remained the same at 100 mM and 200 mM and thus correlate significantly with each other (Spearman, P < 0.05 for all four pairs). There was, however, a general trend (16 of 20 cases) for the preferences to be less pronounced with the higher concentration tested (200 mM) compared to the lower concentration (100 mM).

DISCUSSION

Table 1 compares the taste preference threshold values for polycose obtained in the present study with those for maltose and sucrose obtained with the same method in the four primate species tested here, with those of other mammalian species obtained by using a similar method, and with detection or recognition threshold values obtained for humans, with psychophysical procedures. A comparison of the preference threshold values for polycose shows Macaca nemestrina to be the most sensitive nonhuman primate species tested so far. Remarkably, their preference threshold value for this polysaccharide is even lower than the recognition threshold value of humans (Hettinger et al., 1996) in which, to the best of our TABLE 1. TASTE PREFERENCE THRESHOLDS FOR POLYCOSE, MALTOSE, AND SUCROSE IN FOUR PRIMATE SPECIES TESTED AND IN OTHER MAMMALIAN SPECIES Threshold (mM) Species

Polycose

Maltose

Sucrose

Saimiri sciureus1,2a Ateles geoffroyi1,3 Papio hamadryas anubis1,4 Macaca nemestrina1,5 Rattus norvegicus6 Rattus norvegicus7 Meriones unguiculatus7 Mesocricetus auratus7 Acomys cahirinus7 Homo sapiens8,9

60 30 30 10 0.1 10 10 38

10 3 10 10 2.6 5 5 >10 >10 10

a1 Present

study, 2 Laska (1996), 3 Laska et al. (1996), 4 Laska et al. (1999), 5 Laska (2000), 6 Sclafani and Nissenbaum (1987), 7 Feigin et al. (1987), 8 Hettinger et al. (1996), study established a recognition threshold for polycose, 9 ASTM (1973) study established detection thresholds rather than preference thresholds for maltose and sucrose.

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knowledge, no proper detection threshold value has been determined. More importantly, pigtail macaques are the only primate species tested so far whose preference threshold value for polycose and maltose is as low as that for sucrose. Thus, they differ from the other primates tested that all, including humans, display lower thresholds for sucrose compared to polycose and its disaccharide constituent maltose. The pattern of preference threshold values displayed by the pigtail macaques for these three saccharides is similar to that reported in rodents such as rats, hamsters, gerbils, and spiny mice, which all have been shown to be at least as sensitive to polycose and maltose as to sucrose (Sclafani and Nissenbaum, 1987; Feigin et al., 1987). The reliability of the preference thresholds established here is supported by one of the few earlier studies that assessed taste responses of nonhuman primates to polycose. Using 24-hr solution versus water tests, Sunderland and Sclafani (1987) reported that squirrel monkeys prefer polycose over water at concentrations of 100 and 200 mM, but not at 10 and 50 mM. Bonnet macaques prefer this polysaccharide over water at all four concentrations. Although all rodent species tested so far show lower preference threshold values for polycose than the pigtail macaques and, thus, all primates tested here, the similarity in the across-substance patterns of sensitivity between Macaca nemestrina and rats, hamsters, gerbils, and spiny mice (cf. Table 1) suggests that this primate species, and perhaps also other members of the genus Macaca, may have specialized taste receptors for starch and starch-derived polysaccharides that other primates are thought to lack (Sclafani, 1991). This supposition is supported by our findings in the second experiment. Table 2 compares the relative taste preferences for suprathreshold concentrations of polycose, maltose, and sucrose in the four primate species tested here with those of other mammalian species obtained with the same or a similar method and with ratings on relative sweetness obtained in humans with psychophysical procedures. Squirrel monkeys, spider monkeys, and olive baboons clearly preferred sucrose over equimolar concentrations of polycose and maltose and, thus, show a pattern of relative preferences that is similar to the ranking of relative sweetness of these three saccharides found in humans (Feigin et al., 1987). Pigtail macaques, in contrast, were at least as attracted to the polysaccharide and its disaccharide constituent as to sucrose. Their pattern of relative preferences is similar to that found in rats. Using solution versus solution tests of brief duration, a method almost identical to the one employed here, Sclafani and Mann (1987) showed that, at concentrations of 30, 100, and 300 mM, Rattus norvegicus prefers polycose and maltose over sucrose and that this ranking of relative preference is reversed only when presenting the saccharides at equimolar concentrations of 500 mM. The reliability of the relative preferences reported here is supported by earlier studies that assessed relative taste preferences for food-associated mono- and disaccharides in squirrel monkeys (Laska, 1997), spider monkeys (Laska et al.,

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TABLE 2. RELATIVE TASTE PREFERENCES FOR POLYCOSE, MALTOSE, AND SUCROSE IN FOUR PRIMATE SPECIES TESTED AND IN OTHER MAMMALIAN SPECIES Species and concentration (mM)

Rank order of preference

sciureus1a

Saimiri 100 200 Ateles geoffroyi1 100 200 Papio hamadryas anubis1 100 200 Macaca nemestrina1 100 200 Rattus norvegicus2 30 100 300 500 Saimiri sciureus3 100 Macaca radiata3 100 Homo sapiens4 100 200

sucrose > polycose ≥ maltose sucrose > polycose = maltose sucrose > polycose ≥ maltose sucrose ≥ maltose ≥ polycose sucrose > polycose > maltose sucrose > polycose ≥ maltose maltose > polycose ≥ sucrose maltose = polycose = sucrose polycose > maltose > sucrose polycose ≥ maltose ≥ sucrose polycose ≥ sucrose ≥ maltose sucrose > maltose ≥ polycose sucrose > maltose = polycose polycose = maltose = sucrose sucrose > maltose = polycose sucrose > maltose > polycose

a1 Present study, 2 Sclafani and Mann (1987), 3 Sunderland and Sclafani (1988), 4 Feigin et al. (1987) study established relative sweetness rather than preference.

1998), and pigtail macaques (Laska, 2000). Using the same method as in the present study, i.e., solution versus solution tests of brief duration, Saimiri sciureus and Ateles geoffroyi preferred sucrose over maltose at equimolar concentrations of 50, 100, 200, and 400 mM, respectively, whereas Macaca nemestrina preferred maltose over sucrose at all four concentrations. In line with these findings, Sunderland and Sclafani (1987) reported that squirrel monkeys showed a significantly higher degree of preference for sucrose than for polycose or maltose in 24-hr solution versus water tests using concentrations of 10, 50, 100, and 200 mM, respectively, whereas bonnet macaques displayed preferences for maltose and polycose that were at least as strong as those for sucrose. The question arises as to possible reasons why the pigtail macaques differ from the other primates tested in their responsiveness to polycose. Old World

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primates and New World primates have been shown to differ in their ability to perceive substances such as aspartame and thaumatin, which both taste sweet to humans, suggesting that phylogenetic relatedness might account for differences or correspondences in taste perception among species (Glaser, 1993). However, in the present study, olive baboons, an Old World primate species like the pigtail macaques, showed the same pattern of relative preferences for polycose as squirrel monkeys and spider monkeys, two New World primate species. Thus, it seems unlikely that membership in one of these taxa is responsible for the observed differences among species. Differences in dietary habits have been shown repeatedly to provide plausible explanations for differences in taste performance among species (Kare, 1971; Pfaffmann, 1977). Among New World primates, for example, the degree of frugivory has been found to correlate positively with sensitivity to food-associated mono- and disaccharides (Laska, 1996). This seems to make sense in terms of optimal foraging theory, as frugivorous species rely on soluble carbohydrates to meet their energy requirements more than nonfrugivores (Laska et al., 1996). Sclafani (1991) proposed that the high sensitivity and preference for polycose and other starch-derived polysaccharides observed in the rat may also be explained by dietary habits. Anatomical features such as teeth and gut morphology suggest that members of the genus Rattus are primarily granivorous, i.e., they feed on a starch-rich diet, lending support to this hypothesis. Although considerable information on the dietary habits of the four primate species employed in the present study are at hand (Clutton-Brock and Harvey, 1977; Caldecott, 1986; Chapman, 1987; Ross, 1992), no definitive conclusions can be drawn at to whether differences in feeding specializations may account for the observed differences in polycose responsiveness, because unfortunately, none of the studies reported the proportion of starch-rich plants in the diet of any species. Furthermore, pigtail macaques do not seem to differ markedly in the proportion of fruits and seeds in their diet (72% of total intake) from olive baboons (63%) and spider monkeys (80%), but only from squirrel monkeys (26%) (Clutton-Brock and Harvey, 1977). Using the proportion of animal matter in the diet as an indicator of the maximally possible proportion of starch-containing plants also shows the squirrel monkey (72%) to be markedly different from the other three species (1–10%), (Clutton-Brock and Harvey, 1977), but nevertheless the squirrel monkeys showed the same pattern of relative preference for polycose as the spider monkeys and the olive baboons. Thus, the ultimate reason for the observed differences in polycose responsiveness between pigtail macaques and olive baboons, spider monkeys, squirrel monkeys, and humans remains elusive. One can speculate, however, as to the possible proximate reason. In addition to behavioral studies measuring voluntary intake of sapid solutions, two lines of evidence lend further support to the idea that rats have specialized taste receptors for starch and stach-derived polysaccharides. Firstly,

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studies using conditioned taste aversion paradigms showed that rats display little cross-generalization between polycose and sucrose, but some degree of crossgeneralization between polycose and its disaccharide constituent maltose (Nissenbaum and Sclafani, 1987; Sako et al., 1994). Similar results were obtained using the same method in the hamster, another rodent species that cross-generalized between glycogen and maltose, but not between glycogen and sucrose (Rehnberg et al., 1996). A more recent study showed cross-generalization between sucrose and polycose in the same rodent species, suggesting that the two substances share common perceptual taste characteristics (Formaker et al., 1998). Secondly, electrophysiological studies have shown that the rat’s chorda tympani responses to sugars were strongly suppressed by gurmarin, an antisweet peptide, whereas this substance had essentially no effect on polycose responses (Sako et al., 1994). Application of KHCO3 onto the rat’s tongue enhanced chorda tympani responses to sugars, but not to polycose (Sako et al., 1994). In line with these findings, single unit activity in the nucleus tractus solitarius of the rat in response to polycose was markedly different from that in response to substances representing the traditional four basic taste qualities (Giza et al., 1991). To the best of our knowledge, studies on conditioned taste aversion using polycose in nonhuman primates have not been performed, but findings from electrophysiological studies in cynomolgus and rhesus macaques lend some support to the idea that members of the genus Macaca might have specialized taste receptors for starch and other polysaccharides. Plata-Salaman et al. (1993) recorded the activity of single neurons in the gustatory cortex of Macaca fascicularis in response to 19 chemicals sweet to humans. They found that all 19 substances formed a coherent cluster in the taste space generated from the correlations among patterns of neural activity evoked by the stimuli, suggesting relative similarity of taste quality across substances. Whereas simple carbohydrates such as glucose, fructose, sucrose, and maltose formed the center of this cluster, polycose was somewhat distant from these sugars, indicating some degree of difference in taste quality. The results of the present study demonstrate that all four species of nonhuman primates employed here are clearly attracted to aqueous solutions of polycose. Further, we showed that pigtail macaques have lower taste preference thresholds for this starch-derived polysaccharide compared to squirrel monkeys, spider monkeys, and olive baboons and that their pattern of relative preference (maltose > polycose ≥ sucrose) differs from that of the other three primate species (sucrose > polcose ≥ maltose). These findings suggest that Macaca nemestrina, unlike other primates, but similar to rodents, may have specialized taste receptors for starch. Acknowledgments—We thank Andreas Russwurm and Alejandra Arango Cessa for help in collecting data, and the Deutsche Forschungsgemeinschaft (La 635/10-1), the Volkswagen Foundation (I/75 354), and Patronato Pro-Universidad Veracruzana for financial support. L.T.H.S. was awarded a grant by Conacyt Mexico (no.124786).

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LASKA, KOHLMANN, SCHEUBER, SALAZAR, AND LUNA REFERENCES

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P1: GKW/RKP

P2: GKW


PP258-344812


September 26, 2001

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2011

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