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Keywords:

  • New World monkeys;
  • sensory ecology;
  • dietary adaptations;
  • taste;
  • taste buds;
  • papillae

Abstract

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. GUSTATORY ANATOMY
  5. MATERIALS AND METHODS
  6. RESULTS
  7. DISCUSSION
  8. Acknowledgements
  9. LITERATURE CITED

Fungiform papillae (FPs) are the only gustatory structures on the anterior tongue. Taste buds (TBs), which are located in FPs, house taste receptors. Each TB has a taste pore (TP) by which tastants are transmitted. In humans, FP and TB densities correlate with taste sensitivity and food preferences. Females have higher FP densities than males in Homo, Pan, and Cebus. Homo, Pan, and Cebus also have larger brains, slower ontogenetic development, and higher maternal investment in offspring compared to most primates. An increase in maternal investment places intense pressure on females to 1) obtain high-quality foods, and 2) detect potential toxins at low levels. This study examines sex differences in FPs and TPs (a TB surrogate) in 11 Cebus apella to test the hypothesis that higher FP density in females may be an adaptation specific to reproductive strategies of females. Tongues were imaged using an environmental scanning electron microscope; from these images FP surface area, FP density, TP count, and TP densities were calculated. We found that there were no significant differences between males and females in the number of TPs per FP. However, we did find that females do have larger FP surface areas and higher FP densities than males. The anatomical evidence indicates that females may have greater taste sensitivity than males because females have more FP than males. Future research on food preference and selection in Cebus is expected to show sex-specific behaviors similar to those observed in Homo and Pan. Anat Rec,, 2011. © 2011 Wiley Periodicals, Inc.


INTRODUCTION

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. GUSTATORY ANATOMY
  5. MATERIALS AND METHODS
  6. RESULTS
  7. DISCUSSION
  8. Acknowledgements
  9. LITERATURE CITED

The sensory systems evolved to assist animals in navigating and interacting with their environment. The function of the gustatory system (taste) is to help determine the chemical contents of foods. In humans, there are sex-based differences in both gustatory anatomy and taste sensitivity. For instance, Hladik and Simmens (1996) found that Mvae and Yassa females in south Cameroon were more sensitive to sucrose (i.e., able to detect sucrose at lower concentrations) than males. Obtaining adequate nutrients from food is critical for both males and females. However, food selection (and rejection) may be more important to the reproductive success of females because their reproductive costs are higher than male reproductive costs. As taste is a very important sense involved with food selection and rejection, females may benefit more from greater taste sensitivity than males.

For primates, studies comparing differences in male and female gustatory sensitivity and anatomy are limited. However, there is some evidence showing sex-based differences in gustatory anatomy in both chimpanzees and Cebus monkeys (Alport,2008,2009). These two nonhuman primates share with humans an increase in brain to body size ratio, slower development, and evidence for an increased maternal investment in their infants (Ghiglieri,1984; Fragaszy and Bard,1997; Di Bitetti and Janson,2001). Thus, it is thought that sex-based differences in gustatory anatomy may reflect a reproductive adaptation in females in these species. In this study, we explore this possibility by examining the variation in the gustatory anatomy of a species of New World monkey, Cebus apella.

GUSTATORY ANATOMY

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. GUSTATORY ANATOMY
  5. MATERIALS AND METHODS
  6. RESULTS
  7. DISCUSSION
  8. Acknowledgements
  9. LITERATURE CITED

In mammals, the dorsum of the tongue is carpeted with four types of papillae: filiform, fungiform, foliate, and circumvallate. Filiform papillae can be found across the entire tongue and are nongustatory, meaning they are not capable of transmitting taste information to the brain. Circumvallate, foliate, and fungiform papillae (FPs) are gustatory and distinct from FPs in their location and anatomy (Purves et al.,1997). Circumvallate are located on the posterior aspect of the tongue, whereas foliate are located on the posterolateral aspect of the tongue (Fig. 1). FPs are the focus of this study and are located on the anterior two-thirds of the tongue. FPs are the first gustatory structures that comes in contact with an ingested chemical (Purves et al.,1997; Buck,2000). Accordingly, FPs are critical in food selection.

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Figure 1. A cross-sectional view of the lingual gustatory papillae and taste buds of the tongue. Fungiform papillae are located at the anterior tip of the tongue and are unique among the papillae in that their taste buds are located superiorly with pores directed upward.

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Taste is the sensation produced when a chemical stimulus (tastant) is applied to a taste cell (Purves et al.,1997). Taste cells are differentiated epithelial cells that cluster together in groups of 50–100 to form a taste bud (TB; Fig. 2). On the tongue, TBs are found in the lingual epithelium of gustatory papillae (Buck,2000). Each TB has a taste pore (TP) that opens to the surface of a gustatory papilla. It is through this pore that molecules and ions taken into the mouth can reach the receptor cells (Segovia et al.,2002). The presence of a pore indicates the presence of functional taste cells (Segovia et al.,2002). Furthermore, the number of pores in a specific region of the tongue provides an indication of taste sensitivity in that region (Miller and Reedy,1990). Accordingly, TPs can be used as a proxy for TB count and location.

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Figure 2. (A) A histological cross section of a Cebus apella fungiform papilla at 10× magnification. (B) A 100× magnification of the taste bud. TB, taste bud; TP, taste pore; TC, taste cell.

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In circumvallate and foliate papillae, TBs and TPs are located on the lateral surface of a papilla; in FPs, they are located superiorly (Figs. 1 and 2). The number of TBs and TPs located in circumvallate, foliate, and FPs varies (Miller and Bartoshuk,1991). TB and TP counts can also vary across different papillae of the same type. For example, TB count can range between 0 and 5 per FP in nonhuman primates (Docherty et al.,2010; Muchlinski et al.,2010). In humans, ∼9% of FPs do not contain TBs. In FPs that contain TBs, TB count can range between 1 and 26, but average around 4.98 TB per FP (Miller and Reedy,1990; Miller and Bartoshuk,1991; Segovia et al.,2002). Furthermore, TB density is positively correlated with FP density, and TB counts decrease in posteriorly located FP (Miller and Reedy,1990). Thus, both FP and TB densities can affect taste sensitivity.

Taste

There are five primary tastes recognized by humans: sweet, umami (i.e., savory or meaty), salty, bitter, and sour. These tastes allow us to evaluate foods for both harmful chemicals and beneficial nutrients (Hladik and Simmen,1996). Sweet, umami, and salty are associated with specific nutrients. Sweet usually indicates a food item that is high in calories and rich in soluble carbohydrates (Hladik and Simmen,1996). Salty foods indicate the presence of sodium, lithium, or potassium (Bartoshuk and Beauchamp,1990), which are vital for ion maintenance and water homeostasis in the body (Lindemann,2001; Sugita,2006). Conversely, sour and bitter tastes usually signal the presence of a harmful compound. Bitter and sour foods are acceptable at low concentrations, but at higher concentrations, both tastants elicit a rejection response. Spoiled foods are high in acid and taste sour; while bitter tasting foods signal the presence of secondary compounds such as alkaloids (e.g., caffeine). Sweet, umami, salty, bitter, and sour may not be universal tastes across the primate order, although behavioral tests show that nonhuman primates will accept and reject foods in a similar way to humans when presented with an oral stimulus (Smith and Margolis,1999).

Based on a misinterpretation of the early work of Hänig (1901), it was thought that the primate tongue had discrete areas on the surface that were designated for a single taste category. For example, it was thought that sweet tastants could only be detected on the tip of the tongue, salty on the anterior and lateral aspect of the tongue, sour posterolaterally, and bitter in the back of the tongue by the circumvallate papillae, for additional details see:(Hladik and Simmen,1996; Lindemann,2001). The tongue taste map as presented above is incorrect because all TBs contain taste cells that respond to tastants from each category (Bradbury,2004). However, some regions of the tongue do show an increased sensitivity to one (or more) of the primary taste categories. This asymmetry in taste sensitivity across the tongue is a result of the density of specific taste cells (e.g., taste cells receptive to sweet tastants) within a TB. For example, the tip of the tongue, where FPs are concentrated, is more sensitive to sweet and umami than stimuli from other taste categories because the receptors for these tastants are in higher concentrations here than in other TBs in other papillae. However, it is important to note that anatomical and electrophysiological data on taste receptor distribution are both contradictory and/or inconclusive (Ninomiya et al.,1993; Adler et al.,2000; Danilova and Hellekant,2003; Inoue et al.,2004). Taste research is still in its infancy and more comparative data are needed to understand better the subtleties of the gustatory system.

Sex Differences

Females have different nutritional needs than males, and these differences are more apparent during gestation and lactation (e.g., Whitten et al.,1983; Boinski,1988; Overdorff,1996; McCabe and Fedigan,2007). For example, female primates in a wide range of species have been shown to feed on more sugar- and protein-rich foods than males (Clutton-Brock,1977; Rodman,1977; Wasser,1977; Gautier-Hion,1980; Whitten et al.,1983; Cords,1986; Boinski,1988; Morland,1991; Byrne et al.,1993; O'Brien and Kinnaird,1997; Isbell,1998; McCabe and Fedigan,2007). Pregnant females must acquire very specific nutrients (e.g., amino acids), but at the same time they must avoid toxins. Thus, female primates are particularly selective when it comes to ingesting high-protein foods such as insects and leaves because these foods are often high in toxins, yet at the same time, these foods are high in amino acids which are essential for reproduction (Sampson and Jansen,1984; Brosnan,1985; National Research Council,2003). They must strike a balance between ingesting too many high-protein foods and very few. Leaves can contain high levels of secondary compounds such as tannins, while one-fifth of an insect's total weight may be comprised of toxins such as aristolochic acids (Schmidt,1979; Milton,1980; Nishida and Uehara,1980; Lambert,1998; Janson and Chapman,1999; Glander,2005). In addition to the secondary compounds that can inhibit digestion (e.g., phenolics) (Glander,1982; Lambert,1998b; Janson and Chapman,1999), many plants also produce steroid hormones, which at even low concentrations can disrupt reproduction (Labov,1977; Wynne-Edwards,2001). For that reason, females, more than males, would benefit from greater taste sensitivity to avoid secondary compounds that might inhibit their reproduction.

Behavioral laboratory experiments on humans and observations of feeding behavior of nonhuman primates strongly support the notion that females are 1) more selective with regard to the foods they ingest and 2) have greater taste sensitivity to certain food items (Keller et al.,2002; Danilova and Hellekant,2003). These differences can be translated into differences in anatomy. Human females have significantly higher FP densities (∼66.6 ± 2.2 FPs/cm2) than males (55.6 ± 2.1 FPs/cm2) (Tepper and Nurse,1997). In humans, higher densities in FPs correlate positively with higher TB densities per FP (Miller and Reedy,1990; Miller and Bartoshuk,1991). The anatomical evidence in humans suggests that individuals with greater FP densities, and therefore, TBs will have greater taste sensitivity. Anatomical sex differences in the gustatory system do appear to affect food preferences and intake. For example, 6-n-propylthiouracil (PROP) and phenylthiocarbamide (PTC) are synthetic compounds that mimic bitter tasting compounds naturally found in vegetables such as cabbage, broccoli, and kale (Keller et al.,2002). Both PROP and PTC are used in taste studies to determine food preferences and taste sensitivity (Keller et al.,2002). If an individual can detect a low concentration of PTC or PROP, he or she would have greater taste sensitivity to bitter tasting foods than an individual who requires higher concentrations of PTC or PROP in registering taste. In the literature, individuals who can detect a compound (or tastant) at lower concentrations are called tasters, while individuals who require high concentrations are generally referred to as nontasters (Kalmus,1971; Miller and Bartoshuk,1991). Among humans, female PROP nontasters preferred sweet tasting and fattier foods then female human tasters (Duffy and Bartoshuk,2000). However, there was no correlation between taste sensitivity to PROP and food preference (Duffy and Bartoshuk,2000). The same results were found in male and female preschool children who are possibly less affected by socioculturally learned behaviors regarding taste preferences (Tepper,1998; Keller et al.,2002).

The gustatory system is better studied in humans than it is in nonhuman primates. However, a few studies have provided evidence for sex-based differences in food preferences and in gross tongue anatomy. Female anthropoid primates are generally smaller in body size and thus require absolutely fewer calories (although relatively more based on metabolic needs) than males to maintain homeostasis. However, during pregnancy and lactation, females require absolutely more calories and are thus documented to 1) spend more time feeding (Alouatta palliata: Smith,1977; Pan troglodytes: Teleki,1977; Cebus capucinus: McCabe and Fedigan,2007); 2) consume a more diverse range of foods (Cebus olivaceus: Fragaszy,1986); 3) consume more fruits and flowers that are high in sugar (C. capucinus: McCabe and Fedigan,2007; Erythrocebus patas: Isbell,1998; Pongo pygmaeus; Rodman,1977); and 4) consume more high protein foods such as leaves and insects (Cercocebus albigena: Wasser,1977; Cercopithecus ascanius: Cords,1986; Erythrocebus patas: Isbell,1998). Nonetheless, there are reports of males spending more time feeding than females. For example, among male Gorilla gorilla beringi, silverbacks spend more time feeding on thistles than females (Fossey and Harcourt,1977). Thistles, which are weeds, have been traditionally used among humans in many cultures to stimulate menstruation and abortion, and are best avoided during pregnancy (Kataria,1995). It appears that female gorillas may be selectively avoiding thistles, and as a result, males appear to be favoring this weed.

Sexual dimorphism in gustatory anatomy has been documented in humans, the common chimpanzee (Pan troglodytes), and the brown capuchin (Cebus apella). FPs are one of the few gustatory gross anatomical structures that have been examined across species and between sexes. Sex-specific FP densities have been quantified in five nonhuman primates (Alouatta palliata, C. apella, Cercopithecus aethiops, Pan troglodytes, Varecia variegata: Alport,2008,2009). All female species sampled had higher FP densities than males—however, statistical significance was reached only in C. apella and Pan troglodytes. Alport (2008) hypothesizes that the sex-based differences observed in FP densities are a result of high offspring investment in these species. Alport (2008) argues that chimpanzees and brown capuchin monkey females may be under more intense selection pressure than males to obtain critical nutrients from foods or to have the capacity to detect toxins at lower levels. Thus, females in these two genera may have adapted to sex-specific reproductive demands by evolving higher FP densities—which may be associated with greater taste sensitivity.

Objectives

Alport (2009) also found significant correlations between FP densities and diet among nonhuman primates, but the observed pattern in nonhuman primates was not always the same as that observed in humans. An underlying assumption of Alport's research was that TB count (and TP count by proxy) remains constant across FP both within and between species. Although there are gross anatomical differences in the density of FP between male and female brown capuchin monkeys, it is not clear if there are intraspecific differences in FP size and TB/TP count. Differences in FP size and TB/TP count may affect overall taste sensitivity. Therefore, in this study, we evaluate similarities and differences between male and female C. apella in FP size and density, as well as evaluating the relationship between TP count (a proxy structure for TB count) and FP size among male and female C. apella. The objectives of our study are twofold. The first is to evaluate the overall relationship between FP size and TP count. The second is to specifically evaluate if males have higher, lower, or equal TP densities compared to females.

MATERIALS AND METHODS

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. GUSTATORY ANATOMY
  5. MATERIALS AND METHODS
  6. RESULTS
  7. DISCUSSION
  8. Acknowledgements
  9. LITERATURE CITED

Sample

Tongues from four female and seven male C. apella were preserved and stored in 10% buffered formalin immediately after euthanasia in a captive facility. No animals were euthanized for the purpose of this study. Samples were obtained from animals euthanized for other purposes. Body mass data were collected for each individual before death (Table 1).

Table 1. Cebus apella sample
SexKGNPapilla densityFungiform papilla area (mm2)Taste pore count
MeanSDMinMaxMeanSDMinMax
  1. Sex, body mass (KG), papillae density (papillae/mm2), and the mean, standard deviations (SD), minimum, and maximum values for fungiform papilla area, and taste pore count for each individual sampled.

F2.2830.910.350.370.080.616.004.2439
F2.6540.580.470.170.310.645.502.3849
F3.2550.460.370.180.180.652.601.6715
F2.3140.520.330.040.290.525.502.0838
M4.0650.240.260.090.130.365.202.1738
M4.2150.440.090.020.070.134.601.5237
M3.2260.210.350.050.280.423.671.7516
M3.9650.560.060.020.040.094.401.1436
M3.580.260.260.050.150.314.751.7528
M3.360.660.080.030.030.115.002.1928
M4.5950.880.100.030.070.155.401.6748

Sample Preparation and Imaging

Each formalin-fixed specimen was sectioned down the midline into right and left halves. The left side of each specimen's tongue was examined using an environmental secondary electron detector (ESED; Hitachi S-3400N) housed at Duquesne University and operated by the author BD. The ESED is similar to other environmental scanning electron microscopes in that it allows specimens to be studied in gaseous environments. Traditional nonenvironmental scanning electron microscopes require specimens to be placed in a vacuum. The ESED is unique because specimens examined are not dehydrated or coated with a conductive layer (gold or carbon coating). Accordingly, ESED is an ideal tool to investigate differences in gustatory anatomy because FP size and shape will not be altered by dehydration. FPs surface area measurements, for example, can be compared to other studies using other methods. Moreover, TB pores are easily seen and will not be masked or clogged by gold and carbon sputter coating (see Docherty et al.,2010). Based on the unique technology of the ESED, tongue samples do not require any additional preparation. Images were taken with an accelerating voltage of 5–20 kV and a working distance of 15 mm. Images were acquired digitally using Princeton Gamma Tech's (PGT) IMIX system and calibrated using an MRS-3 SEM magnification calibration grid. Digital images were used to calculate the density of FPs, FP size, and to count TPs on individual FPs.

To obtain FP density, the number of FPs were counted from the ESED images obtained from the anterior 5 mm of the tongue and that value was divided by the area of the tongue imaged. Low-resolution images were taken of the anterior 5 mm of the tongue, thus in most instances the area sampled was 25 mm2 (Fig. 3). However, to obtain precise area values to calculate FP density, tongue surface area imaged was calculated using NIH ImageJ® software.

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Figure 3. An ESED image of the anterior tip of a female Cebus apella tongue. The fungiform papillae are the mushroom cap-shaped structures. Filiform papillae, the nongustatory papillae, carpet the surface of the tongue and are scattered across the image.

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Environmental secondary electron detector images were also used to obtain FP area measurements and TP count. TP count can be used as a surrogate for TB count. By dividing TP count by FP area, we were able to calculate TP (or TB) density. TP counts and FP area were measured from five randomly selected papillae on the anterior 5 mm of the tongue. Figure 4 shows how easily TPs can be observed and counted using ESED images.

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Figure 4. (A) A fungiform papilla from a male Cebus apella. (B) A close-up image of surface of the fungiform papilla. The white arrows are pointing to individual taste pores (TP) located on the surface.

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Size Adjustments

Alport (2009) found that the density of FPs on the anterior 0.5 cm of the tongue is negatively correlated with body mass. As body size increases, FP density decreases. In Alport's (2009) study, she counted all the FP on the anterior 0.5 cm of the tongue. The use of the entire anterior 0.5 cm of the tongue raises the possibility that body mass and the size of the tongue will affect FP densities. This possibility results from the fact that a half-centimeter is a greater percentage of a smaller tongue, like those of female individuals, than it is for a larger tongue. However, FPs are concentrated toward the tip of the tongue, and their density decreases posteriorly (Fig. 1). In our study, we are looking for intraspecific differences within a sexually dimorphic species. Males in our sample are approximately 1 kg larger than the females sampled (Table 1). In our study, we are only sampling a small portion of the anterior tip of the tongue; thus, body size should not effect density calculations. Nonetheless, to address the potential confounding effects of body size, all tests were conducted using three different methods. First, the raw data were compared between groups. Second, the ratio of the calculated value (e.g., density of TBs) to the cube root of body mass was used to size adjust the data. Finally, residuals of a least square regression of the calculated value and body mass were used to adjust for differences in body size.

Statistical Analysis

In this study, we are exploring both general intraspecific variation as well as purported male/female differences in gustatory anatomy. To accomplish our first objective (see above) a Pearson product-moment correlation was used to test the relationship between TP counts and FP size calculated from ESED images. In addition, a correlation was run to evaluate the relationship between an individual's average TP and FP density. Finally, to evaluate how body size might affect TP and FP density, a least squares regression was run between these variables and an individual's documented body weight.

A Wilcoxon rank-sum test was used to compare differences in gustatory anatomy between males and females. Nonparametric test statistics were selected for intraspecific comparison because of unequal sample sizes between males and females. Thus, more conservative tests were selected to explore variation between males and females. Test statistics were calculated using IBM SPSS Statistics v.19© and JMP 8©.

RESULTS

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. GUSTATORY ANATOMY
  5. MATERIALS AND METHODS
  6. RESULTS
  7. DISCUSSION
  8. Acknowledgements
  9. LITERATURE CITED

Raw FP surface area, TP count, and FP and TP densities were not normally distributed and therefore transformed into naturally logs. Body mass did not correlate with FP density and TP count (Fig. 5). However, a Spearman's rank correlation shows a positive correlation between TP density and body mass (P < 0.0001; Fig. 5) and a significant negative correlation between FP surface area and body mass (P < 0.0001; Fig. 5).

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Figure 5. Scatterplots showing the correlation between (A) ln fungiform papilla surface area, (B) ln fungiform papillae density, (C) ln taste pore count, (D) ln taste pore density and body mass (kg). A positive Spearman's rank correlation was documented for taste pore density and body mass (D: P < 0.0001). There was also a significant negative correlation between fungiform papilla surface area and body mass (A: P < 0.0001). Values obtained from male specimens are labeled M and those from females F.

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TP count and FP surface area was shown to be positively correlated (P < 0.03). However, when male and female TP count and FP surface area values were examined separately, results differed. TP count versus FP surface area remained significant for females (P = 0.002), but not for males (P = 0.10; Fig. 6). However, when each male was examined individually, there was a significant and positive relationship between TP count and FP surface area (Table 2; Fig. 7).

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Figure 6. Scatterplots showing the correlation between ln taste pore count and ln fungiform papilla surface area among all individuals sampled (A), females (B), and males (C). A Spearman's rank correlation test indicates that taste pore count is positively correlated with fungiform papilla surface area among all individuals sampled (A: P = 0.03) and among females (B: P = 0.002), but not among the males sampled. Values obtained from male specimens are labeled M and those from females F.

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Figure 7. A scatterplot of ln taste pore count versus ln fungiform papilla surface area for all male Cebus apella. Each individual male has his own marker (e.g., +). There is no relationship between these two variables across all males sampled (Fig. 6C). Within an individual, however, taste pore count positively correlates with fungiform papilla surface area. Solid and dashed lines were used to illustrate the correlations within each individual. See Table 2 for results.

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Table 2. Individual Spearman's rank correlation results for taste pore count versus fungiform papilla area
Individual IDSexSignificance
1124_166FP < 0.0001
1125_168FP = 0.05
1126_169FP = 0.01
1138_170FP = 0.001
1128_172MP = 0.004
1129_173MP = 0.004
1130_175MP = 0.02
1131_176MP < 0.0001
1132_177MP = 0.004
1137_173MP = 0.02
1127_171MP = 0.001

Results indicate that there are sex-based differences in FP and TP densities and FP surface area. However, there were no significant differences in TP counts between males and females as indicated by a Wilcoxon rank-sum test (Fig. 8). We found that females have a higher density of FPs (Z = 2.36, P = 0.01; Fig. 9) and larger FP (Z = 3.80, P < 0.0001; Fig. 10). These findings did not change when each variable was size adjusted (FP density: Z = 2.75, P = 0.006; FP surface area: Z = 4.43, P < 0.0001). Males, on the other hand, had higher TP densities than females (Z = −4.04, P < 0.0001; Fig. 11). These findings did not change when TP density was size adjusted (Z = 2.36, P = 0.01). These findings were not surprising given that TP count did not differ between males and females, but surface area was larger in females. Figure 12 are ESED images highlighting sex-based differences FPs and TP densities and FP size.

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Figure 8. A box and whisker plot illustrating how ln taste pore counts varies between female and male Cebus apella. Results did not change when taste pore count was size adjusted. The bolded F and M values represent individual fungiform papillae where only one TP was present. There were no significant differences between males and females.

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Figure 9. A box and whisker plot illustrating how ln fungiform papilla density varies and differs significantly between female and male Cebus apella. Results did not change when taste pore count was size adjusted. Significance set at 0.05; * = P ≤ 0.05.

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Figure 10. A box and whisker plot illustrating how ln fungiform papilla surface area varies and differs significantly between female and male Cebus apella. Results did not change when taste pore count was size adjusted. Significance set at 0.05; *** = P ≤ 0.0001.

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Figure 11. A box and whisker plot illustrating how ln transformed taste pore density varies and differs significantly between female and male Cebus apella. Results did not change when taste pore count was size adjusted. Significance set at 0.05; *** = P ≤ 0.0001.

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Figure 12. Environmental SED images obtained from a female (left) and male (right) Cebus apella. Note that females have larger fungiform papillae and more densely packed fungiform papillae. Males have higher taste pore densities than females.

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DISCUSSION

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. GUSTATORY ANATOMY
  5. MATERIALS AND METHODS
  6. RESULTS
  7. DISCUSSION
  8. Acknowledgements
  9. LITERATURE CITED

Gustatory Sexual Dimorphism

FPs have been studied in a number of different mammals, and their gustatory importance is well documented (Murray and Murray,1960; Kobota et al.,1966; Kobota and Iwamoto,1967; Miller and Preslar,1975; Davies et al.,1979; Robinson and Winkles,1990; Mack et al.,1997; Pastor et al.,2008). This study had two major aims. The first was to determine if female C. apella have higher FP densities than males as reported by Alport (2009). The second was to evaluate if TP density or TP count was the likely basis of the proposed higher taste sensitivity in females. In this study, we found that females did have significantly higher FP densities than males. On average, females have 6 FPs/cm2, while males have 4 FPs/cm2 (i.e., females have 50% more FPs than males). These results are similar to those documented by Alport (2009). However, our density values were significantly lower than those reported in Alport's (2009) study. Alport (2009) counted all FPs on the anterior 0.5 cm of the tongue, while we were only able to calculate densities from a 5 mm2 area of the tongue because of imaging restrictions. Regardless, both studies found a significant statistical difference between males and females. Based on previous work in humans that documented both sex-based differences between males and females and a correlation between FP density and taste sensitivity, we hypothesize that females may have greater taste sensitivity than males.

Two factors may confound our inference regarding greater taste sensitivity in Cebus females. First, we assume that FP size remains constant across a species and within an individual. Our second assumption, and perhaps most important, is that TB count (or TP count by proxy) remains constant across FPs. To further explore what intraspecific differences in FP density might indicate functionally, we examine variation in FP surface area and TP count within a single individual and between males and females.

FPs area is an important variable that needs to be considered when drawing conclusions regarding taste sensitivity. Theoretically, larger FPs could house more TBs, which could conceivably increase taste sensitivity. In this study, and in others, females were found to have more FPs than males. Within our limited sample, we also found that females have significantly larger FPs than males. These findings bolster the hypothesis that females have greater taste sensitivity than males because this suggests that females have more room per papilla to house more TBs, which could, in turn, mean a greater number of taste receptors.

Few studies have explored variations in TP density or count in nonhuman primates because TPs are difficult to view except by electron microscopy (Docherty et al.,2010). We found that TP count within a single FP did not differ significantly between males and females. However, there is some variation within a single individual. In our sample, TP count ranged from one to six within a single individual and from one to nine across all individuals sampled. We found at least one TP in every FP we sampled. These findings were surprising given that in humans ∼9% of FPs do not contain TBs (Miller and Reedy,1990; Segovia et al.,2002). A similar lack of TBs has been documented in other primates. Kobota et al. (1966) found that lorises and callitrichines do not have TPs. Muchlinski and colleagues (2010) also found that some FPs in Saimiri and Otolemur lacked TBs and TPs. However, these negative findings may be a result of histological section thickness (>20 μm) or too few serial sections (<15). Although TBs are rarely missed because they range between 10 and 20 μm, it is possible to miss one in intervals between stained sections (Docherty et al.,2010). Because males in the study had smaller FP, but equal number of TPs per FP, males were documented to have significantly higher TP densities than females. There was a significant correlation between FP size and TP count when both male and female data were pooled.

Based on our findings, it appears that FP could be an important variable to consider in evaluating differences in taste sensitivity by anatomical proxy. However, our sample was male biased and relatively small overall, and our results must be interpreted with caution. In addition, two further issues must be considered. Although there was a significant (albeit weak) relationship between FP surface area and TP count across all individuals sampled, no relationship was found when males were examined as a group. This unexpected amount of variability suggests that FP surface area in males is under relaxed selection, and this feature may not play a significant role in enhancing taste sensitivity. Among humans, the size of FPs is negatively correlated with the density of FP (Essick et al.,2003). Whereas the density of FP is positively correlated with taste sensitivity among humans, individuals with higher bitter taste sensitivity have FPs with smaller surface areas (Miller and Reedy,1990; Essick et al.,2003). We found that males had higher TP densities because they had equal numbers of TBs compared to females but smaller FP surface area. Thus, based on previous research and our current findings, it appears that FP density may be a more informative variable when evaluating differences in taste sensitivity both interspecifically and intraspecifically.

To better understand the relationship between TP counts and FP surface area, we need more information on TB size and taste receptor densities. Although our study was able to calculate TP count reliably, we were not able to obtain TB or taste receptor cell densities nondestructively. These data can only be obtained histologically. Differences in receptor neuron size have been identified in olfactory epithelium in several primate species (Smith et al.,2004; Smith and Bhatnagar,2004). Neuroepithelial cell density may even differ significantly between females and males (Segovia and Guillamon,1982). Because of this, Smith and Bhatnagar (2004) assert that the relationship between olfactory epithelium surface area and olfactory receptor neuron densities cannot be assumed constant. Accordingly, future research on gustatory anatomy should explore the interplay between TB size, TC density, and FP surface area. Identifying the relationships between these variables will increase our understanding of the observed differences between males and females identified in this study.

The effects of body size are important to consider in inter- and intraspecific comparisons. Male C. apella are ∼ 1 kg larger than females. Conceivably, males could have larger tongues, which could influence the density of FP, FP size, TP count, or all three variables. In our limited sample, we found that body mass was not significantly correlated with the density of FP or TP count. There was, however, a significant relationship between TP density and FP surface area. As noted above, males in our sample were found to have smaller FPs than females, and thus, a significant negative correlation was found between FP size and body mass. There were no differences in mean TP count, however, between males and females. Accordingly, males had a higher density of TPs than females.

To account for the potential influence of sexual size dimorphism, all data were size adjusted. Size adjusted results did not differ from results run on raw natural log transformed data. Although body size may be an important variable to consider in some interspecific studies, it may not be important in intraspecific studies, and may, in fact, needlessly distort findings (Smith and Bhatnagar,2004). Even if females did have higher FP densities as the result of having a smaller tongue area compared with males, that density should still be associated with higher taste sensitivity, as is seen in humans (Bartoshuk and Beauchamp,1990; Miller and Reedy,1990; Tepper and Nurse,1997; Bartoshuk,2000; Doty et al.,2001; Yakinous and Guinard,2001; Essick et al.,2003). Accordingly, functional in the gustatory system are likely to exist whether those differences result from a greater number of papillae, a smaller tongue area, or both.

Female Sensory Exuberance

The anatomical evidence suggests that female C. apella have greater taste sensitivity than males. The differences in gustatory anatomy, as documented in this study, may be a reproductive adaptation for females who may be under more intense selection pressure than males to obtain critical nutrients in the form of high-quality foods, or to have the capacity to detect potential toxins at low levels. C. apella is a more k-selected species than many of its closest New World monkey relatives (Martin,1990; Fragaszy and Bard,1997). C. apella also has a relatively large brain, the largest per body mass than any other nonhuman primate (Martin,1990). From a bioenergetics perspective, brain tissue is expensive—fueling 1 kg of brain tissue per day requires ∼240 kcal (Holliday,1986; Elia,1992). Large relative brain size is associated with life history parameters such as long periods of infant and juvenile dependency, which lead to a very high cost per offspring (Fragaszy and Bard,1997; Ross,2002; Van Schaik and Deaner,2003). Cebus shares these life history characteristics with chimpanzees and humans (Fragaszy and Bard,1997; Alport,2009).

In addition to life history parameters, Pan and Cebus also show convergence in their feeding behavior. Like many primate species, chimpanzees and capuchins are omnivorous (Teleki,1977; Nishida and Uehara,1983; Fragaszy and Bard,1997; Wrangham et al.,1998). However, unlike most other primates, Pan and Cebus also exhibit relatively high levels of extractive foraging (Goodall,1963,1968; McGrew et al.,1979; Boesch and Boesch,1981; Fedigan,1983; Nishida and Uehara,1983; Fragaszy,1986; Goodall,1986; Boesch and Boesch,1990; Fragaszy et al.,1992; Fragaszy and Bard,1997; Conklin-Brittain et al.,2000; Whiten et al.,2003). Furthermore, capuchin females spend more time engaged in extractive foraging than males. What is notable about extractive foods is that they tend to be high-quality foods that provide a concentrated source of energy and protein (Gibson,1986).

The fact that capuchins show a sex difference in FP density, just as in chimpanzees and humans, suggests that sex differences in lingual anatomy and, perhaps, taste sensitivity are associated with sex differences in the selection of particular food items. There is evidence for sex differences in feeding behavior as well as among females at different reproductive stages (cycling, pregnant, or lactating), in Pan, Homo, and a myriad of other nonhuman primates, little data exists documenting the presence of significant sex differences in diet and foraging in C. apella (see Masterson,1997; Jack,2011). There are differences in cranial morphology (Masterson,1997) and substrate preference (Janson and Boinski,1992) between male and female C. apella, which suggests possible differences in diet, yet the published evidence for sex differences in diet is surprising sparse (Jack,2011). Although data on sex differences in feeding behavior were not found for C. apella, other Cebus species do show sex differences and variation in feeding behavior with reproductive status (Jack,2011). For instance, C. capucinus females spent more time foraging during lactation, and lactating females were observed to ingest more fruit than cycling females during the wet season (McCabe and Fedigan,2007). On the other hand, Rose (1994) found that C. capucinus females spent less time foraging during pregnancy and lactation than when cycling (Rose,1994). C. olivaceus females have been shown to have more dietary diversity and spend more time feeding than males but are thought to be less efficient (Fragaszy,1986; Fragaszy et al.,1992; Fragaszy and Bard,1997).

These sex differences in feeding behavior may be linked to different nutritional needs relating to differential costs of reproduction in females and males. However, effects of sex differences in gustatory sensitivity might be more specific than differences in consumption of fruit or leaves. It may be that females may be avoiding specific plant species and very specific parts of a plant or animals. Testing for sex differences in feeding behavior at this level requires more specific data analyses and is beyond the scope of this project. If the density of FPs, FP size, or TP count is associated with bitter taste sensitivity in Cebus, as it is in humans (Bartoshuk and Beauchamp,1990; Miller and Reedy,1990; Tepper and Nurse,1997; Tepper,1998; Yakinous and Guinard,2001; Essick et al.,2003), Cebus females may benefit specifically from the ability to reject noxious compounds. Ingesting unfamiliar plant species can be especially risky (Freeland and Janzen,1974) and detecting secondary compounds might be particularly beneficial for females with high dietary diversity. Although there is limited evidence supporting behavioral differences in the menus of male and female C. apella in gustatory, our anatomical findings (Fig. 12) suggest that future research on the feeding preferences and behaviors in the wild and captivity in this species will yield results that may shed light on the role of food selectivity and taste as part of the reproductive strategy of C. apella and other species of the genus.

Acknowledgements

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. GUSTATORY ANATOMY
  5. MATERIALS AND METHODS
  6. RESULTS
  7. DISCUSSION
  8. Acknowledgements
  9. LITERATURE CITED

The authors thank Duquesne University Instrumentation Department for granting them access to the environmental scanning electron microscope and Matt Hazzard at the University of Kentucky for illustrating the location and morphology of gustatory papillae in Fig. 1. The authors thank Liza Shapiro, Chris Kirk, Rebecca Lewis, Jason Organ, Russell Hogg, and Deborah Overdorff for comments and feedback during the early stages of this project. Furthermore, The authors thank Drs. Rosenberger and Laitman for inviting them to contribute to their special issue on New World monkeys.

LITERATURE CITED

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. GUSTATORY ANATOMY
  5. MATERIALS AND METHODS
  6. RESULTS
  7. DISCUSSION
  8. Acknowledgements
  9. LITERATURE CITED
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