Chapter 2 Nutritional and Digestive Challenges to Being a Gum-Feeding Primate

Transcription

1 Chapter 2 Nutritional and Digestive Challenges to Being a Gum-Feeding Primate Michael L. Power Abstract Gum is an unusual food that presents significant challenges to animals that feed on it. Gum is limited in availability; trees generally secrete it only in response to damage. Gum is a b-linked complex polysaccharide, and as such is resistant to mammalian digestive enzymes and requires fermentation by gut microbes. It contains little or no lipid, low amounts of protein, and no appreciable levels of vitamins. As a food, gum can be characterized as difficult to obtain, potentially limited in quantity, difficult to digest, and primarily a source of energy and minerals. Despite these drawbacks, many primates feed extensively on gums. Among mammals, gum-feeding largely appears to be a primate dietary adaptation. Why are there so many primate gum-feeders and what adaptations have allowed them to make a living on such a problematic food? This is the central question of this book. This chapter examines digestive and nutritional aspects of gum. Specific examples of biological adaptations found in common and pygmy marmosets (Callithrix jacchus and Cebuella pygmaea), small New World primate gum-feeding specialists, will be examined. These marmoset species have many similarities in their behavior, morphology and metabolism, but also some instructive differences in their digestive function. C. pygmaea is the smallest of the marmosets but has the slowest passage rate of digesta. This might represent an adaptation to retain difficult-to-digest material, such as gum, within the gut to allow fermentation. In contrast, C. jacchus has a rapid passage rate. Passage rate in C. jacchus appears adapted more for rapidly excreting indigestible material (e.g., seeds) than for retaining gum within the gut to enable more complete digestion. Fruit is a rare component of C. pygmaea s diet; hence any constraint on feeding caused by filling the gut with ingested seeds is greatly relaxed, apparently enabling digestive kinetics that favor digestive efficiency over maximizing food intake. Interestingly, however, these marmosets share M.L. Power (*) Nutrition Laboratory, Smithsonian Conservation Biology Institute, National Zoological Park, P.O. Box 37012, MRC 5503, Washington, DC , USA and Research Department, American College of Obstetricians and Gynecologists, Washington, DC 20024, USA powerm@si.edu A.M. Burrows and L.T. Nash (eds.), The Evolution of Exudativory in Primates, Developments in Primatology: Progress and Prospects, DOI / _2, Springer Science+Business Media, LLC

2 26 M.L. Power an ability to digest gum despite their differences in gum kinetics. In captivity both species have been shown to be more able to digest Acacia gum than related species that feed less often on gum in the wild. Introduction All life has a common biochemical underpinning. Because of this, everything living potentially is food. Indeed, for every living organism there are other organisms that feed off of it. However, because of the immense amount of time over which life has diverged and radiated, the common biochemical underpinning has accumulated a tremendous amount of variation in specific characteristics among taxa. Everything may be food for something; but for any given organism most of what is in its environment is not food. Animals eat food; they require nutrients. A significant proportion of anatomy and physiology has as its primary purpose the transformation of food that animals select from their environment into the nutrients required for life. These challenges can be external ones such as finding and acquiring food, and they can be internal challenges, such as digesting, assimilating, and metabolizing food, and then finally excreting the associated waste products (Chivers et al. 1984). My research focus is on the internal challenges different foods provide. All foods provide challenges; there is no perfect food. Different foods provide different challenges. For example, carnivores are confronted with very different challenges in obtaining nutrients than are herbivores. Animals and plants share an evolutionary history, and thus are biochemically similar; however, they are also very different, reflecting the billions of years of evolutionary separation. Thus, in general it is assumed that carnivores are faced with a less difficult nutritional challenge than are herbivores. If you are what you eat, then eating other animals should provide fewer difficulties than eating plants. As is true for most generalities in biology, the one above is an oversimplification. Although other animals certainly contain all the nutrients an animal needs to consume, they do not contain them in the correct proportions. Animals contain far more protein than is necessary for another animal to consume, and far less glucose and other carbohydrate than is needed to survive. Strict carnivores must deal metabolically with an excess of protein and insufficient carbohydrate. For herbivores the situation is possibly reversed. Protein can be a limiting nutrient but carbohydrate is usually in plentiful supply, though not always in a readily metabolizable form. Many plant carbohydrates are difficult to digest. Animals that feed largely on plant material generally face greater digestive challenges; for strict carnivores the challenges are primarily metabolic. Of course all plant foods are not alike, and thus provide different digestive and metabolic challenges. This essay concerns the challenges presented by a rather unusual plant food, gum, a type of exudate produced by certain trees and lianas. The number of animals known to regularly feed on tree exudates is not large,

3 2 Nutritional and Digestive Challenges to Being a Gum-Feeding Primate 27 though the list is slowly expanding. Among mammals, the primate order contains a considerable number of species that utilize tree exudates as a food resource, including many that appear to specialize on exudates. The only other (known) exudate-feeding mammals are a guild of small marsupials native to Australia (Hume 1982; Smith and Lee 1984), where there are no native nonhuman primates. Why are there so many primate gum-feeders and what adaptations have allowed them to make a living on such a problematic food? That is the interesting question that has inspired this book. My contribution will be limited to examining the nutritional, digestive and metabolic advantages and challenges from eating gum, and is further constrained by a focus on the biology of the marmosets, small gum-feeding New World primates. Hopefully this chapter will provide a broad enough context that the value of gum as food for other species can be evaluated as well. This chapter will start with a general assessment of gum as food, with some comparison to other plant foods including other exudates. Gum is dietary fiber; as such it presents digestive difficulties. The advantages and disadvantages of foreand hind-gut fermentation for obtaining nutrients from gum are briefly reviewed. The chapter then focuses on marmosets, specifically their digestive function and how that may or may not be adapted to gum-feeding. Exudates as Food There are primate species, our own especially, that incorporate a substantial amount of animal matter in the diet; but in general, primates feed predominantly on plant foods. Plants are complex structures. A tree is composed of many different parts that vary widely in chemical and physical composition. Its wood, bark, leaves, flowers, fruits, and exudates all provide food for something but any given animal species generally will feed only on certain parts and will ignore the rest. A tree may have many species visiting it, each feeding on a different tree product. These are obvious statements; the point is that different plant products need to be categorized in ways that reflect the kind of nutrition they provide in order to explore the dietary adaptations of our subject species. To say that gum is a plant product doesn t help to determine what nutrition it can or cannot provide for a species. Ideally gum should be chemically assayed to determine its constituents, and then fed to animals in controlled trials to determine the bioavailability of those constituents. However, there are general principles that can be used to predict what nutritional category a plant product is likely to occupy. There are many ways to categorize plant foods. For the purposes of this essay I propose two simple categorizations: alive vs. not alive, and primarily reproductive vs. primarily nonreproductive. The first categorization separates exudates from other plant foods such as leaves, flowers, and fruit in a fundamental way. Exudates are created by living things but they themselves are not alive. More to the point, exudates do not contain living cells. Cells, by necessity, contain the required chemical

4 28 M.L. Power components for life. Foods such as leaves, flowers and fruit that are composed predominantly of living cells in theory should provide excellent nutrition. Of course, there might be some difficulty in accessing the cell contents and obtaining the nutrients; but they are there. Exudates are created by living things and therefore it is not surprising that they contain nutrients; however, there is no expectation that exudates will contain all the nutrients necessary for life. And indeed they do not. Gums and other exudates are not complete foods. Plants produce a number of exudates; in this essay I will be primarily concerned with gum; however, the other types of exudates are briefly considered here. Tree exudates are generally categorized as sap, gum, latex, and resin (Nash 1986). In addition, nectar can be considered a plant exudate. All these exudates have different functions, which influence their characteristics as food. Consider nectar, an exudate produced by flowering plants. Flowering plants arose more than a 100 million years ago (Soltis and Soltis 2004), greatly diversified in the Cretaceous, and have been coevolving with animals ever since. Nectar serves as a reward to pollinators. The plant provides food in exchange for assistance in sexual reproduction. Nectar has evolved to be food. Therefore, it is not surprising that nectar has characteristics that make it edible and that it provides some nutrition, in most cases primarily energy. These are characteristics of many, but not all plant parts that primarily serve a reproductive function. Nectar and fruit are the principal examples. In both cases the plant produces a food-like substance to reward animals that assist in the plant s reproduction. But seeds also can provide high quality nutrition. It is true that for many plants it is beneficial if their seeds are ingested; but not if the seeds are actually digested. There are seed dispersers and there are seed predators. For the predators, seeds are food and quite good food for the basic reason that seeds must contain most if not all the molecules necessary for life. They are incipient life. Most exudates other than nectar generally don t serve the reproductive needs of plants, and have not evolved to be food. Sap perhaps is closest to nectar in constitution. Sap contains the simple sugars from photosynthesis, and other nutrients that are required by the plant cells to survive. The main difference between sap and nectar is that nectar is concentrated. There are animals (mainly insects) that feed on sap. The challenges sap presents are mainly related to acquiring it in the first place; however, it is dilute and thus a large quantity of water must be ingested to provide a fairly small amount of nutrition. Cicadas are an insect that feeds on sap; the author has walked through the mist created by millions of cicadas feeding on tree sap, and necessarily excreting large amounts of water into the air. Joly-Radko and Zimmermann (Chap. 7) describe sap eating by proxy in mouse lemurs consuming the excretions produced by hemipteran insects feeding on sap. Resins are phenol and terpene derivatives. They are generally considered noxious and even toxic. There are animals that are tolerant of resins, however. The desert wood rat (Neotoma lepida) feeds extensively on creosote bush leaves, at least in certain areas of its range (Mangione et al. 2000). These leaves can contain as much as 25% of the dry mass as phenolic resin (Rhoades and Cates 1976).

5 2 Nutritional and Digestive Challenges to Being a Gum-Feeding Primate 29 Latex is a chemically complicated exudate that certain plants exude in response to damage. Indeed, as a category it is the most phytochemically diverse exudate (Agrawal and Konno 2009). About 10% of flowering plants produce latex (Agrawal and Konno 2009), which translates to tens of thousands of latex-producing plant species (Farrell et al. 1991). Latex is produced by specialized cells called laticifers, and is released upon damage to the plant. Because latex performs no known metabolic functions in plants it has been suggested to perform a defense function, mainly against herbivorous insects (Agrawal and Konno 2009). In some instances the defense function is related to toxic chemicals in the latex; however, the majority of latex-producing plants have not been found to produce toxic substances in their latex, or to be intrinsically toxic to animals (Konno et al. 2004). Indeed, latex from different species range from highly toxic (e.g., milkweed) to edible (e.g., latex from Brosimum galactodendron, called the milk tree or cow tree in Venezuela). Some researchers have suggested that the sticky nature of latex may serve as a feeding deterrent for insects; a physical defense in addition to any chemical defense (Farrell et al. 1991). Latex is also known to contain proteases. For example, papaya latex contains papain, which is used as a meat tenderizer. Papain has been shown to be toxic to several species of lepidopteran larvae (Konno et al. 2004), though it is unclear how it would affect vertebrates. Latex, as a category, is not very helpful when assessing the potential food value of an exudate, primarily because latex does not appear to have a particular chemical definition. Rather, what unites latex from different species and separates latex from other exudates is that latex is produced and secreted by laticifers, specialized plant cells that respond to tissue damage. Other exudates come from intercellular spaces. Typically latex will be opaque and sticky, and will coagulate upon exposure to air. Latex from many species is milky in appearance; but it can be yellow, orange, red, or even clear (Agrawal and Konno 2009). Thus, for the field ecologists witnessing his focal species feeding on an exudate, being able to distinguish latex from gum would likely require particular botanical knowledge. Latex from certain plants undoubtedly provides significant nutrition to many animals including primates. Latex from other plants probably deters feeding due to the presence of toxic chemicals. Simply labeling an exudate latex gives little insight into its potential nutritional role in an animal s diet. The focus of this chapter is gum as food. Gum is an unusual food that presents significant challenges to animals that feed on it. The amount of gum available to most animals can be limited, since trees generally secrete it only in response to damage and gum usually hardens fairly rapidly to seal the wound site (Nash 1986). Gum is comprised mainly of a b-linked complex polysaccharide (Monke 1941; Booth et al. 1949; Booth and Henderson 1963; Hove and Herndon 1957); complex carbohydrates of this form (e.g., cellulose) require fermentation by gut microbes before the nutrients are available to animals that feed on it. In other words, gum is dietary fiber (Van Soest 1982; Kritchevsky 1988). Dietary fiber is neither inert nor indigestible, and its ingestion has many and varied physiological consequences (Wrick 1979; Van Soest 1982; Kritchevsky 1988). For example, insoluble fiber (e.g., cellulose) generally has a laxative effect on humans and other nonruminant mammals

6 30 M.L. Power (Kritchevsky 1988). In contrast, soluble fiber (e.g., gum, pectin) can slow gastric emptying and the rate of passage through the small intestine by increasing the viscosity of digesta (Johnson et al. 1984). Soluble fiber also has been shown to reduce the rate of glucose absorption (Johnson et al. 1984). Gums are not nutritionally complete, although they can contain significant quantities of mineral salts (e.g., calcium, potassium, magnesium, but not usually phosphorus) (e.g., Génin et al., Chap. 6; Smith 2000; Peres 2000). As a food, gum can be characterized as difficult to obtain, potentially limited in quantity, difficult to digest, and primarily a source of energy and minerals. Despite these drawbacks, many primates feed extensively on gums, as do some birds (e.g., Kori bustards (Ardeotis kori); Skead 1969; Urban et al. 1978; cited in Lichtenberg and Hallager 2008). Among mammals, gum-feeding largely appears to be a primate dietary adaptation, though that might represent a greater knowledge of primate feeding behavior than that of nocturnal arboreal rodents and bats, other taxa that would have access to gum and might benefit from eating gum. Some African rodents eat small quantities of gum in their diets (Emmons 1980). Laboratory rats have been shown to be able to digest gum arabic, i.e., Acacia senegal gum (McLean Ross et al. 1984). In theory, insectivorous bats might benefit from the calcium found in gums, assuming it was biologically available to them. There are some plant products referred to as gums that appear to serve a reproductive function. These are gums produced in seed pods, for example, in the genus Parkia, and appear to act as a food reward to attract potential seed dispersers (Peres 2000; Feldmann and Heymann 2001). Many callitrichid primates (and probably other animals) feed on these pod gums. The chemical structure of these gums is uncertain; but they may be more digestible than other tree gums (Peres 2000). That would certainly be the prediction from an evolutionary perspective. However, the current biochemical evidence does not address this issue with any certainty. The statement in Peres (2000) that the carbohydrates in Parkia pod gum are nonstructural is meaningless. Structural carbohydrates are constituents of cell walls. Since gums do not contain cells of course their carbohydrates are nonstructural. That does not mean that they are not complex b-linked polysaccharides resistant to vertebrate digestive enzymes. The chemical assay technique used to determine the constituent sugars in Parkia pod gum reported in Peres (2000) is also used to determine the sugar constituents of cellulose (e.g., Kajiwara and Maeda 1983). A technique capable of hydrolyzing cellulose into its constituent monosaccharides likely would be successful at breaking a gum into its monosaccharides, regardless of its chemical structure. Interestingly, the monosaccharides identified in Parkia pod gum (arabinose, rhamnose, galactose, and glucuronic acid) are the same sugars that comprise gum arabic (A. senegal gum). Thus, the current evidence indicates that Parkia pod gum has similarities to Acacia gum. The structure of A. senegal gum has been determined; this gum consists of a proline-rich glycoprotein with multiple sugar residues consisting of arabinose (as a mono-, di-, or polysaccharide) or of the four constituent monosaccharides listed above in a complex polysaccharide (Goodrum et al. 2000). A comparison of the relative quantities of sugars reported in Peres (2000) for Parkia pod gum and Goodrum et al. (2000) for A. senegal gum indicates a higher

7 2 Nutritional and Digestive Challenges to Being a Gum-Feeding Primate 31 proportion of arabinose in Parkia pod gum. Assuming similar structure between these gums, this result implies a higher proportion of arabinose sugar residues attached to the gum glycoproteins in Parkia pod gum. If true, then this finding might imply that Parkia pod gum is less resistant to mammalian digestive enzymes; but this is merely conjectural at this time. Fore-Gut and Hind-Gut Digestion The plant constituents that are defined to be dietary fiber are not digested by vertebrate digestive enzymes (Kritchevsky 1988). These include cellulose, hemicellulose, lignin (a non-carbohydrate fiber), and a variety of soluble fibers such as pectins and gums (Van Soest 1982). Many gut microbes do produce enzymes that can break the carbohydrate fibers into simple sugars. Animals that obtain significant amounts of nutrition from the internal fermentation of fiber by symbiotic gut microbes generally have evolved expanded regions of the gut where the digesta is fermented. A detailed discussion of the varied and complex adaptations for fermentation chambers in vertebrates is outside of the scope of this chapter; for those interested an excellent resource is Stevens and Hume (1995) and the computer version of this work is available through the Comparative Nutrition Society website ( For primates, the simplest division is between what are called fore-gut fermenters and hind-gut fermenters. The terms refer to the area of the gut that has been expanded to permit fermentation: the stomach for fore-gut fermenters (colobines) and the cecum and colon for hind-gut fermenters. Most primates are hind-gut fermenters to a greater or lesser extent. The small gummivorous primates are all hind-gut fermenters. Gum is dietary fiber; it shares the biochemical characteristics that make all carbohydrate fibers largely indigestible by endogenous mammalian digestive enzymes. Thus gum needs to be fermented by gut microbes before its nutrients can be used. The ability of gut microbes to ferment a particular fiber depends in part on its water solubility (Cummings 1981). If the gum is water-soluble fermentation will be rapid; water insoluble gums are difficult to ferment, because there is a low surface area to volume ratio. In either case, both fore and hind-gut fermenters are capable of digesting gum. There are differences between fore- and hind-gut fermenters that affect their ability to utilize the nutrients in gum, however. Fore-gut fermenting animals gain significant advantages for certain nutrients (Hume 1989). The microbes in their stomachs produce many essential nutrients, a significant proportion of which escape into the small intestine and are assimilated and utilized by the host animal. In addition, when a microbe dies it will be digested and its constituents will be available to its host. These constituents include many vitamins but also protein. There are some disadvantages to fore-gut fermentation, however, if the diet contains a significant amount of easily digestible carbohydrate. A fore-gut fermenting animal gains energy in the form of short-chain fatty acids from indigestible and difficult-to-digest carbohydrates (e.g., cellulose and hemicellulose) that otherwise would be unavailable, but loses part of the potentially

8 32 M.L. Power available energy from simple sugars and other easily digestible carbohydrates via the same process. A hind-gut fermenting animal can utilize the energy from easily digestible carbohydrates because they are digested and absorbed in the small intestine, before the microbes in the lower gut can feed on them (Hume 1989). The indigestible carbohydrates pass into the hind gut, are fermented and the resulting short-chain fatty acids are absorbed and used by the host animal in metabolism just as in the fore-gut fermenters. However, the hind gut does not absorb all nutrients to the same extent that the small intestine does. Therefore many nutrients (e.g., vitamins, proteins) produced by the gut microbes are not as available to a hind-gut fermenter, unless the animal practices coprophagy. Body Size Body size has several influences on the challenges of utilizing gums as food. Larger animals need absolutely more energy to survive. Due to the relative low availability of gum in the environment gum would be expected to be a smaller proportion of the diet of large animals compared with smaller species, even though an individual from the larger species may eat absolutely more gum than does any individual from the smaller species. Above a certain body size there just wouldn t be enough gum in the environment to sustain an animal. That does not mean that gum will be unimportant to the diets of large primates. On the contrary, gum is an important component for many species of large-bodied primates (e.g., patas monkeys (Erythrocebus patas), baboons (Papio spp.), and chimpanzees (Pan spp.)) But it will be rare that a large primate will be able to obtain the majority of needed energy from gum, unlike the situation for small gum-feeding specialists (e.g., pygmy marmosets, C. pygmaea). However, large body size likely will provide an advantage in digesting gum. Gut capacity generally increases in direct proportion to body mass (Demment and Van Soest 1985). This generally means that the retention time of digesta also increases with body size (Demment 1983), assuming that the digestive strategies of the species being compared are not radically different. A longer retention time in the gut would aid gum digestion; thus larger animals should be better able to digest gum. Humans appear to completely digest gum arabic (McLean Ross et al. 1983; Wyatt et al. 1986). Thus, for large primate species the challenge gum presents as a food is likely more regarding the quantity that can be obtained and not its digestive difficulties. Gums could provide important quantities of minerals for large species, even if the total amount of energy from ingested gum is small relative to requirement (Ushida et al. 2006). Protein Gums contain protein. That isn t surprising, since they are a biological material. Indeed, the chemical properties of economically valuable gums such as gum arabic that are important to their functions (both as a wound-sealing substance in trees and

9 2 Nutritional and Digestive Challenges to Being a Gum-Feeding Primate 33 in human food industry as an emulsifier) derive from the presence of glycoproteins with multiple saccharides (mono, di, and poly) attached (Goodrum et al. 2000). For example, in gum arabic (gum from A. senegal) the glycoprotein is a hydroxyproline-rich peptide with multiple sugar residues consisting of arabinose molecules or the main sugar of gum arabic which is a rhamnoglucuronoarabinogalactan polysaccharide (i.e., a polysaccharide containing rhamnose, glucuronic acid, arabinose, and galactose; Goodrum et al. 2000). So glycoproteins appear to be an intrinsic component of gums. There is a great deal of variation in the amount of protein reported among various gums, ranging from trace amounts to as much as 9 10% on a dry matter basis. So do some gums serve as an important source of protein for primates? Possibly; but certain aspects of gum protein suggest that the answer is not simple. The amount of protein in gum may be overestimated by standard assay techniques; the biological availability of that protein may be problematic for many gum-feeders; and finally, many gum-feeders are also highly insectivorous (e.g., marmosets, Galago senegalensis, Galago moholi), so it is not likely that protein is a limiting nutrient. Biological materials aren t usually assayed for protein per se; usually the assay determines the amount of nitrogen in the sample, and then that value is converted to an estimate called crude protein using an accepted conversion value. For forages used to feed domesticated animals (e.g., alfalfa or hay) that value is 6.25 g protein/g nitrogen; for milk protein the value is Most values of estimated protein in leaves, fruit, and exudates collected from the wild are derived from 6.25 times the amount of nitrogen determined by chemical assay. Other values have been proposed for wild plant materials, usually significantly lower than For example, Milton and Dintzis (1981) found that appropriate conversion factors for many tropical leaves were as low as 70% of Partly that can be explained by the amino acid composition of the proteins; but also, protein is not the sole nitrogenous substance found in plant material. There are amino sugars, lignin, and various plant secondary compounds that contain nitrogen. For example, alkoloids are nitrogenous. These are usually found in relatively low levels in the cultivated forages that are the results of generations of artificial selection to produce efficient feed for domesticated herbivores, and therefore contribute little to the nitrogen content of the plants from which the 6.25 conversion factor was derived. It is not at all certain what conversion factor is appropriate to estimate protein from nitrogen for gums. Thus most estimates of the amount of protein in gums must be considered to be preliminary, and quite possibly inflated. The second issue is bioavailability. If the protein is not incorporated within the indigestible carbohydrate matrix of gum, but is simply dissolved in an aqueous fraction, then the protein should be readily available. However, if the protein is actually incorporated into the chemical structure of the gum, then the gum likely needs to be fermented before that protein is available to the primate that ingests it. Most of the protein in gums probably is in the form of glycoproteins, as described above for A. senegal gum, and thus is incorporated into the polysaccharide structure. However, it is not known to what extent those sugar residues are resistant to cleavage from the peptide, though the sugars themselves are likely resistant to mammalian digestive enzymes. So the bioavailability of gum protein is uncertain.

10 34 M.L. Power If the primate eating the gum is a fore-gut fermenting colobine, then the protein will become available indirectly, regardless of how the protein is incorporated into the carbohydrate structure, through the digestion of fore-gut microbes that pass into the small intestine. For a hind gut fermenting primate, however, if the protein is resistant to digestive enzymes in the upper intestinal tract due to its sugar residues, then the protein will pass into the lower gut to become available to the microbes in the cecum and colon; but unless the animal practices some form of coprophagy, the protein is unlikely to be digested and assimilated by the ingesting primate. Finally, primates that feed on gums all have other sources of protein in their diets, usually insects and other small animals. Primate protein requirements are not particularly high. For most Old World anthropoids, 12% of energy in the diet coming from protein is more than adequate for growth and reproduction (NRC 2003). Even the small New World monkeys, such as common marmosets, can be maintained on diets of 16% of energy from protein and show normal growth and reproduction (Tardif et al. 1998). In the wild, with higher energy expenditures due to activity and thermoregulation, the required percent of energy from protein is likely lower, provided, of course, that sufficient energy to match expenditure can be obtained. Thus it is not clear that most gum-feeding primates are protein limited. This doesn t mean that the protein in gums is irrelevant; it does imply that protein content is unlikely to be the determining factor of whether animals eat a gum or not. Calcium Gums often contain significant amounts of minerals, but not all minerals. Calcium is often found in significant quantities; phosphorus is not. Thus gums have been proposed to be a source of calcium in the diet that may be particularly important to insectivorous gum-feeders (e.g., Bearder and Martin 1980), since insects generally contain significant amounts of phosphorus and little calcium. Assuming that the calcium in gum is bioavailable, which probably requires the gum to be fermented, gums can provide a significant source of calcium for wild animals. The cecum and colon will absorb most minerals, so the calcium in gum is available to hind-gut fermenters. It has been estimated that chimpanzees that feed on Albizia zygia tree gum could obtain their entire daily requirement of calcium and several other minerals from their mean daily intake of gum, even though that amount of gum provides a fairly trivial amount of their daily energy intake (Ushida et al. 2006). Should captive small gum-feeding primates be provided with gum as a calcium source? The levels of calcium in the gums that have been assayed range from below 0.5% to around 1% on a dry matter basis. These are fairly good levels for wild foods but most manufactured primate diets contain % calcium on a dry matter basis. If feeding gum reduces consumption of the nutritionally complete feed that should form the base of any captive animal s diet, then calcium intake may not be increased. In contrast, substituting gum for fruit in the diet may indeed increase

11 2 Nutritional and Digestive Challenges to Being a Gum-Feeding Primate 35 calcium consumption. However that will come at the expense of decreasing the consumption of vitamins in fruit. At present, there are no demonstrated nutritional reasons for including gum in the diet of captive gum-feeding primates. There are hypothetical advantages, such as providing a fermentable substrate that would increase butyrate production in the colon; butyrate is known to enhance colonic health (Wong et al. 2006). However, some starches and pectins in captive callitrichid diets probably already reach the colon to be fermented, providing a source of butyrate. Gum added to the diets of common and pygmy marmosets appeared to slow the passage rate of digesta (Power 1991; Power and Oftedal 1996). Whether a slower passage rate of digesta would have any positive health benefits in captivity is unknown. Based on the lack of evidence that gum has a nutritional purpose in captive callitrichid diets, it should be treated as an enrichment food. Callitrichid Digestive Function The monophyletic primate family Callitrichidae includes marmosets (genera Callithrix, Mico and Cebuella), tamarins (genus Saguinus), lion tamarins (genus Leontopithecus), and Goeldi s monkey (Callimico goeldii). All callitrichids are omnivorous, and feed on fruit, gum, other plant exudates including nectar, invertebrates, and small vertebrates. As a general rule, marmosets are more likely than the other callitrichids to feed extensively on gums. Marmosets have dental adaptations that allow them to gouge trees and stimulate the flow of gum (Coimbra-Filha and Mittermeier 1977), thus reducing the problem of gum availability. This appears to have allowed marmosets to colonize drier forests and small forest fragments where there is little fruit (Fonseca and Lacher 1984). Because wild callitrichids typically feed on a variety of foods they are faced with a variety of digestive challenges. The digestive challenges posed by fruit would appear to favor different digestive adaptations than does those posed by gum. A substantial proportion of the ingested mass of fruits often consists of seeds (Garber 1986; Heymann and Smith 1999), which are passed relatively unchanged through the digestive tract (Garber 1986; Knogge and Heymann 2003). These seeds represent indigestible bulk to marmosets, and could inhibit food intake if they are not eliminated rapidly. In contrast, gums are b-linked polysaccharides that require microbial fermentation; thus their digestion would benefit from an extended residence time within the gut. The optimal digestive strategies for fruit and gum appear to be in conflict. Fruit-eating would favor a rapid passage of digesta through the gut to eliminate the indigestible seeds, while gum digestion would benefit from a slower passage rate, retaining the gum within the gut to allow fermentation to proceed. Previous work on digestive function in five callitrichid species (Power 1991) indicated that, in general, the ability to digest a common diet and the amount of time it took for digesta to pass through the digestive tract were associated with body size. Transit time of particulate digesta (defined as the time to first appearance of

12 36 M.L. Power an indigestible particulate marker) and the apparent digestibility of both dry matter and energy declined with mean body mass for four of the species: golden lion tamarins (Leontopithecus rosalia, ca. 700 g), cotton-top tamarins (Saguinus oedipus, ca. 500 g), common marmosets (Callithrix jacchus, ca. 350 g), and saddle-back tamarins (Saguinus fuscicollis, ca. 300 g). Thus any differences in digestive function between common marmosets and other callitrichids appeared to be explained by allometry. In contrast, the mean value for transit time for the smallest callitrichid species, the pygmy marmoset (Cebuella pygmaea, ca. 125 g), was greater than for any of the other species, and the mean values for apparent digestibility of dry matter and energy were equal to those of Leontopithecus (Figs. 2.1 and 2.2). In addition to being the smallest callitrichid, C. pygmaea is also the marmoset most dependent on gum as a dietary staple in the wild and the least likely to feed on fruit (Ramirez et al. 1977; Soini 1982; Yépez et al. 2005). A comparison of digestive function between C. jacchus, a species that eats a substantial amount of both fruit and gum in addition to animal prey, and C. pygmaea which largely feeds on gum and animal prey, and rarely on fruit, provides instructive insight into the adaptive conflict between digestive strategies for fruit and gum. C. jacchus has rapid passage rates for both solid and liquid markers of digesta (Caton et al. 1996; Power and Myers 2009); indeed C. jacchus does not differ in passage rate from similar-sized tamarins (Power 1991). Passage rate in C. jacchus appears adapted more for rapidly excreting seeds than for retaining digesta within the gut to enable more complete digestion. For wild C. jacchus, seeds represent indigestible bulk, which provide essentially no nutrients, but may inhibit feeding by filling the digestive tract. There is a potential opportunity cost in retaining seeds within the gut and little benefit. Fig. 2.1 Transit time (time to first appearance of a particulate marker) with respect to body mass in five callitrichid species

13 2 Nutritional and Digestive Challenges to Being a Gum-Feeding Primate 37 Fig. 2.2 Apparent digestibility of energy (ADE) with respect to body mass in five callitrichid species (Cp = Cebuella pygmaea; Cj = Callithrix jacchus; Sf = Saguinus fuscicollis; So = Saguinus oedipus; Lr = Leontopithecus rosalia) The adaptive advantage to eliminating seeds rapidly appears to have driven the evolution of a rapid passage rate in most callitrichids (Power 1991; Power and Oftedal 1996). In contrast, wild C. pygmaea feed extensively on gums, and possibly saps, and rarely feed on fruit (Ramirez et al. 1977; Soini 1982; Yépez et al. 2005). C. pygmaea s divergence from the pattern of digestive function exhibited by the other callitrichids may be related to the digestive advantage of retaining gum within the digestive tract for fermentation to occur, as well as to a relaxation of the adaptive constraint from the need to eliminate seeds from the gut (Power 1991; Power and Oftedal 1996). Interestingly, despite their differences in passage rates, the two marmosets did not differ in their ability to digest gum arabic (Power 1991; Power and Oftedal 1996), a highly water-soluble Acacia gum that should ferment relatively rapidly. In contrast, two tamarin (S. oedipus and S. fuscicollis) and one lion tamarin (L. rosalia) species digested this gum poorly (Power 1991; Power and Oftedal 1996). Both marmoset species appear to have adaptations for gum digestion which tamarins and lion tamarins lack (Fig. 2.3). Thus retention of digesta does not appear to be the most important aspect of digestive function in regards to gum digestion in callitrichids. A study of passage rate in C. jacchus using both a particulate (chromium mordanted fiber) and a liquid marker (cobalt EDTA) indicated that the fluid passed through the marmoset digestive tract more slowly than did particulate matter (Caton et al. 1996). Caton and colleagues hypothesized that C. jacchus has a cecal colonic separation mechanism, in which particulate matter is largely excluded from the cecum, flowing directly to the colon, and liquid digesta (e.g., gum) is preferentially retained within the cecum, allowing fermentation to proceed.

14 38 M.L. Power Fig. 2.3 When powdered gum arabic was added to a single-item homogeneous diet at 9% of dry matter, marmosets showed no significant change in digestive efficiency while the tamarin and lion tamarin species all had declines in mean apparent digestibility of energy (ADE). Data from Power (Cp = Cebuella pygmaea; Cj = Callithrix jacchus; Sf = Saguinus fuscicollis; So = Saguinus oedipus; Lr = Leontopithecus rosalia) In contrast to the findings of Caton et al. (1996), Power and Myers (2009) found no difference in the mean retention time (MRT) of solid and liquid markers. The values from the Power and Myers study for MRT of CoEDTA and chromium mordanted fiber were similar to the values in Caton et al.; indeed there was no statistical difference between the values from the two studies (Fig. 2.4). The excretion curves published in Caton et al. (1996) were similar to the excretion curves in Power and Myers (2009); concentrations of both markers were similar over time, and for both markers a majority was excreted before the animals retired for the night. Interestingly, MRT for polystyrene beads in C. jacchus is shorter than the values found for chromium mordanted fiber, even in the Caton et al. study (Power 1991; Fig. 2.4). A cecal colonic separation mechanism is not the only potential strategy to increase gut residence time for gum. Passage rate may vary as a function of physical characteristics of the diet. Both C. jacchus and C. pygmaea fed a diet containing 9% gum arabic on a dry matter basis had longer transit times than when fed the diet without gum (Power 1991; Power and Oftedal 1996). As mentioned earlier, adding gum and other soluble fiber to the diet slows passage rate (Johnson et al. 1984). Wild tamarins and lion tamarins feeding extensively on fruit, and hence swallowing many seeds, often have estimated transit times under 1 h (P. Garber, personal communication). Humans fed plastic pellets have shorter transit times (Tomlin and Read 1988). The mechanical stimulation of the gut from such particles (seeds or plastic pellets) may increase the rate of passage of digesta. Thus, temporally separating gum-feeding from feeding on fruit might allow different residence times for digesta.

15 2 Nutritional and Digestive Challenges to Being a Gum-Feeding Primate 39 Fig. 2.4 Mean retention time (MRT) of liquid and particulate markers for Callithrix jacchus. MRT for cobalt EDTA in Power and Myers (2009) was not different from the results in Caton et al. (1996). MRT for particulate markers were variable, with the mean values being different among all three studies, indicating an effect of the type of particulate marker on the results Heymann and Smith (1999) suggest that the temporal pattern of gum-feeding can be a behavioral mechanism to increase the gut residence time of gum. They found that Saguinus mystax and S. fuscicollis concentrated their gum-feeding in the late afternoon, shortly before retiring. Gum would thus be within the intestinal tract at night, when passage rate may have slowed due to the decreased metabolic rate (Power 1991; Power et al. 2003). Peak gum-feeding and bark gouging bouts in common marmosets are reported to be early in the morning (when guts are likely empty) and at the end of the day (Alonso and Langguth 1989). The same pattern was found in four pygmy marmoset groups in Ecuadorian Amazonia (Yépez et al. 2005). Both of these patterns would be likely to result in longer gut residence time for gum than if it was ingested during the middle of the day. An examination of the temporal pattern of gum-feeding in gum-feeding species is warranted. So what does this all mean? Well, for starters, the MRT of fluid digesta in C. jacchus can be considered to be well established at approximately h (Caton et al. 1996) as confirmed by Power and Myers (2009). This is not a particularly long MRT; it does, however, appear to be sufficient to allow fermentation of water-soluble gums (Power 1991; Power and Oftedal 1996). The MRT for particulate matter in C. jacchus is variable. This is as expected, based on the sizable literature for passage rate and retention time in a large number of species. The retention time of particulate matter in a hind-gut fermenter is inversely proportional to particle size. Small particles are preferentially retained; large particles are more rapidly excreted (Van Soest 1982; Hume 1989; Stevens and Hume 1995). Thus it would appear that large particles, such as seeds, will pass through the marmoset digestive tract more rapidly than will soluble material such as gum. Are seeds actually

16 40 M.L. Power excluded from the cecum? The answer to that question isn t known, though it is reasonable to hypothesize that seeds will be less likely to enter the cecum than will fluid. Do marmosets differ in this fashion from other callitrichids? Again, the answer to that question is not yet known. It is possible that all callitrichids retain soluble digesta longer than large particles. Marmoset Digestive Tracts C. pygmaea has longer retention times for digesta than any other callitrichid so far studied, despite being the smallest species. This lengthened retention time is not accomplished by having a longer than expected digestive tract. The length of the intestinal tract including the cecum is appropriate for its body size, with the same gut proportions as found in C. jacchus (Power 1991). Thus, in C. pygmaea gut kinetics have changed from the common callitrichid pattern of rapid passage through the gut. This adaptation has several benefits, as well as at least one cost. The cost is that total food intake is more likely to be limited in C. pygmaea. They are more likely to fill their guts, and thus be forced to refrain from feeding. This happens to callitrichids in the wild, even with L. rosalia and Saguinus spp., much larger callitrichids with rapid passage rates. An intensive fruit-eating session can come to a halt, with animals resting, grooming or engaged in other nonfeeding behaviors. The resumption of feeding is preceded by a rain of seeds being defecated (P. Garber, personal communication). C. pygmaea would be more likely to experience such a feeding interruption when feeding on fruit; of course C. pygmaea rarely feeds intensively on fruit in the wild (Soini 1982). The main advantage of the longer retention time in C. pygmaea is more complete digestion of ingested food. The longer retention time would likely increase digestion of gums but also of the animal matter in the diet (mainly invertebrates). The data displayed in Figs. 2.1 and 2.2 indicates that if C. pygmaea retained the common callitrichid gut kinetics then time to first appearance of markers (transit time) would be about 100 min, and, more importantly, the apparent digestibility of energy of this captive diet would have been below 65%, in contrast to the mean value of about 84% the animals achieved with their adapted gut kinetics. That is a substantial difference. Mean digestible energy intake (DE) of the five animals in this study was 27.6 kcal/ day (Power 1991). The animals achieved that DE by ingesting a mean of 32.9 kcal of food. To achieve the same DE at 65% ADE the animals would have had to increase food intake by 30% to 42.7 kcal of food. Wild animals would almost certainly require more food to survive than would captive animals. The DE of these captive animals was equal to twice metabolic rate (Power 1991). Small wild animals will often have daily energy expenditures closer to three times metabolic rate. The increased digestive efficiency C. pygmaea achieves with its longer retention time substantially reduces the amount of food needed for survival. Although gut kinetics of C. jacchus did not appear to differ from that of Saguinus and Leontopithecus and did differ from the more dietarily similar C. pygmaea, both

17 2 Nutritional and Digestive Challenges to Being a Gum-Feeding Primate 41 common and pygmy marmosets were similar in being better able to digest gum when it was added to the diet (Fig. 2.3; Power 1991; Power and Oftedal 1996). This implies that there is indeed some difference in digestive function between common marmosets and tamarins and lion tamarins despite their similar gut kinetics. Marmoset gut morphology does differ from that of other callitrichids; both Callithrix spp. and C. pygmaea have a larger proportion of the intestinal tract represented by the cecum and colon than do Saguinus and Leontopithecus (Power 1991; Ferrari and Martins 1992; Ferrari et al. 1993). C. jacchus has a more complex cecum than does L. rosalia (Coimbra-Filha et al. 1980). These are precisely the differences in gut morphology that would be expected if gum fermentation is a more important component of dietary ecology in marmosets compared to tamarins and lion tamarins. These differences are not dramatic, however. The cecum and colon of marmosets is not particularly capacious. It is more a matter of relative proportions. The total length of the digestive tract in callitrichids appears to be strongly correlated with body mass (Power 1991). The larger species had longer total gut length. This correlation held for the small intestine but not for the colon and cecum (Power 1991). After accounting for body mass, total intestinal length did not differ between marmosets (C. pygmaea and C. jacchus), tamarins (S. oedipus), and lion tamarins (L. rosalia and Leontopithecus chrysomelas). However, the ratio of small intestine to the cecum plus colon was significantly lower in the marmoset species (Power 1991). Thus marmoset gut morphology does appear to be adapted more for fermentation. The marmoset cecum may be performing another function in addition to acting as a fermentation chamber. Marmosets likely are cecal-colon fermenters, with gum fermentation taking place in the upper colon as well as within the cecum. Common marmoset ceca are more complex in internal structure than are ceca of lion tamarins (Coimbra-Filha et al. 1980). The strictures within C. jacchus ceca produce multiple small pockets, where bacterial populations may be protected from washout. The smoother walls of Saguinus and Leontopithecus ceca may result in greater bacterial loss due to the passage of digesta. The marmoset ceca may serve as a reservoir of bacteria to recolonize the proximal colon after the resident bacterial populations have been reduced, perhaps due to the passage of large, hard seeds. The human appendix has been recently suggested to perform such a function, harboring a reservoir of gut microbes that can recolonize the colon (Bollinger et al. 2007). The greater ability of marmosets to ferment gums may, in part, derive from an enhanced ability to maintain large microbial populations within the upper colon. Summary Gum is a problematical food; difficult to digest, limited in availability, and likely providing little beyond energy and some minerals. It is not a complete food; but it could complement an insectivorous diet, providing carbohydrate and calcium. Animals that feed extensively on gum would benefit from having a region of the