It Takes Guts (And More) to Eat Fruit: Lessons From Avian Nutritional Ecology

Many studies in the last 20 years have examined the basis of fruit choice in birds. It is somewhat frustrating that results of those studies are often inconsistent. Different species and even different individuals of the same species can prefer different fruits (e.g. Johnson et al. 1985, Whelan and Willson 1994, Willson 1994, Young 1992). Although it is clear that birds' preferences are not random (Moermond and Denslow 1985), it is equally clear that generalizations about what underlies their choices are premature even after two decades of research. We rarely understand why birds eat the particular fruits they do. Conversely, we understand even less about why birds do not eat many species of fruit they encounter frequently. In fact, the more one ponders the question, “Why don't more birds eat more fruit?”, the more perplexing it becomes. After all, fruits are “made to be eaten.” Unlike most other dietary items, they represent a mutualistic link—their consumption presumably benefits both the bird and the plant (Snow 1971). Fruits are comparatively easy to find, easy to capture, and often easy to digest. Why, then, do most species of birds rarely or never consume fruits? And, of those species that do consume fruit, why do they not consume more fruit and a larger suite of fruit species? Hidden and consequently neglected keys to unlocking the mystery of why animals eat what they do is how food is processed after it is ingested. The processes by which nutrients in food are assimilated and metabolized can be as important as preingestional factors as determinants of food choice (Bozinovic and Martínez del Rio 1996, Karasov 1990, Karasov and Diamond 1988). In the case of fruit-eating birds, it is becoming clear that processing in the gut varies within and among species in important ways. In addition, we are slowly learning that there might be interspecific differences in ability to catabolize nutrients after they have been absorbed and in ability to tolerate secondary metabolites in fruits. Such differences may frequently entail trade-offs that carry ecological and behavioral consequences (Karasov and Levey 1990, Witmer and Van Soest 1998). In this paper, we summarize nine lessons learned from the study of nutritional ecology of fruit-eating birds. Taken together, those lessons stretch beyond the bounds of fruit-eating birds. They form a foundation for understanding one of the most basic interactions between an animal and its environment—the fueling of life and it physiological underpinnings. The lessons have been divided into two broad sections. The first section summarizes how studying digestive function has yielded new insights about frugivory. The second section focuses on physiological processes other than digestion that can influence fruit choice. Our view of wildlife nutrition has been influenced by a misguided anthropocentric perspective. We unconsciously assume that a bird's digestive and metabolic processes are similar to ours and to those of laboratory rats. However, the digestive traits of birds are not only different from ours, they are also remarkably heterogeneous among species. That heterogeneity can translate into large variation in ability to assimilate food that at a first glance is chemically similar. Even minor chemical differences can have a major influence on fruit preferences and assimilation efficiency. For example, fruit pulp of many species contains the disaccharide sucrose and the hexoses, glucose and fructose. These sugars are essentially identical in terms of energy content per unit gram and are very similar in terms of chemical structure. Most human nutritionists would see no reason for birds to distinguish among them. Yet they do—sometimes very strongly. All birds in the sturnid-muscicapid lineage that have been examined lack expression of the intestinal enzyme sucrase, which breaks down sucrose into its constituent monosaccharides, glucose and fructose. Consequently, those birds are unable to hydrolyze sucrose. When given a choice between isocaloric diets containing hexoses or sucrose, they strongly prefer hexose diets. Because sucrose at high concentrations causes osmotic diarrhea (Martínez del Rio et al. 1997), that sugar is worse than useless for those species (Malcarney et al. 1994, Martínez del Rio and Stevens 1989). Even some species that have sucrase activity prefer isocaloric hexose diets over sucrose (Martínez del Rio et al. 1989). Those observations come as a surprise to us because sucrose is extremely palatable to humans. It is easily assimilated and is distinctively ubiquitous in human contemporary cuisine (Mintz 1986). Although the mechanisms remain unclear, similarly subtle differences in lipid structure can affect frugivore preferences (Bairlein 1991). The physical processing of fruit also can influence preferences and may be a determinant of assimilation efficiencies. In particular, fruit-eating birds can encounter digestive bottlenecks when the volume of indigestible seeds in fruit is high (Levey and Grajal 1991, Murray et al. 1993, but see Witmer 1998a). Like other species that feed on abundant but bulky foods (Diamond et al. 1986, Sibley 1981), the rate at which birds can consume fruit may be limited by the rate at which their guts can process the fruit. Tightly controlled experiments with captive birds have shown that one apparent consequence of that bottleneck is a preference for fruits containing seeds that can be defecated or regurgitated rapidly (Levey and Grajal 1991, Murray et al. 1993). Another consequence is thought to be rapid passage of pulp and seeds through the gut (Walsberg 1975, Karasov and Levey 1990, Jordano 1992, Levey and Karasov 1994, Afik and Karasov 1995). Short retention times, in turn, are hypothesized to result in low assimilation efficiencies (Karasov 1990, Martínez del Rio and Karasov 1991), a seemingly common feature of fruit-eating birds. Herrera (1981) suggested that high competition for dispersers favored low seed loads in Smilax aspera. The implicit assumption of Herrera's (1981) suggestion, and one that must receive more experimental attention, is that frugivores prefer fruit with lower seed loads because those permit higher ingestion and higher nutrient assimilation efficiencies and rates. This assumption, relating a bulky diet with lowered retention time and assimilation efficiency, has been questioned (Witmer 1998a, Witmer and Van Soest 1998, Witmer 1999). More experimental data are clearly needed to resolve this issue. We hypothesize that the degree to which seeds influence ingestion and assimilation is related not only to seed load, but also by the size and geometry of seeds and by mechanisms used by birds to get rid of them. As we have learned more about different types of fruits and frugivores, generalizations about frugivory have become more elusive. Carbohydrate-rich, lipid-poor fruits, for example, are no longer viewed as the avian equivalent of junk food, containing sugar but little else and “snacked” on as a source of energy by omnivorous birds (McKey 1975, Morton 1977). Although those fruits are indeed consumed in small quantities by an astounding assortment of taxa (Levey et al. 1994, Moermond and Denslow 1985, Willson 1986), they also constitute the major dietary item of other taxa (Walsberg 1975, Moermond and Denslow 1985, Loiselle and Blake 1990, Stiles and Rosselli 1993, Witmer 1996a). Far from being junk food, the nutritional content of those fruits appears ideally suited for the digestive traits of birds that specialize on them. In particular, short retention times and low digestive efficiencies may have selected for easily absorbed nutrients in fruit pulp, resulting in the “predigested” monosaccharides and free amino acids that typify fleshy fruits (Jordano 1992, Levey and Grajal 1991). In contrast to carbohydrate-rich fruits are lipid-rich, carbohydrate-poor fruits (Moermond and Denslow 1985, Jordano 1992). A more thorough understanding of digestive processing has altered our view of those fruits as well. Because lipids are assimilated more slowly than carbohydrates (Karasov and Hume 1997), gut retention times of birds that specialize on lipid-rich fruits are relatively long (Bosque and de Parra 1992, Place and Stiles 1992, Zurovchak et al. 1999). The incompatibility of long and short retention times provides a functional explanation of why lipid-rich fruits are primarily consumed by some birds (e.g. insectivorous taxa with long retention times), whereas carbohydrate-rich fruits are primarily consumed by others (e.g. small-bodied omnivorous taxa with short retention times; McDiarmid et al. 1977, Stiles 1980, 1993; Herrera 1984a, Loiselle and Blake 1990, Fuentes 1994). Indeed, such a trade-off between digestive strategies designed either for efficient utilization of lipids or for rapid processing of carbohydrates (Afik and Karasov 1995, Witmer and Van Soest 1998) may underlie the bimodal distribution of percentage of lipid in fruit pulp revealed in at least six studies (Herrera 1984b, Moermond and Denslow 1985, Debussche et al. 1987, White 1989, Fuentes 1994, Witmer 1996a). The negative correlation between lipid and carbohydrate content of fruit pulp across many species (Herrera 1987, Jordano 1992) may be the result of selective pressures imposed on the two digestive strategies outlined above and schematically characterized as sugar- and lipid-processors. Witmer and Van Soest (1998) and Witmer and Martínez del Rio (2001) sketched some of the characteristics that may typify those strategies in Cedar Waxwings (Bombycilla cedroroum), which feed almost exclusively on sugar-dominated fruits (Witmer 1996a), and North American thrushes, which include a significantly higher fraction of lipid-dominated fruits in their diet (Wheelwright 1986). Briefly, ability to emulsify, hydrolyze, absorb, and metabolize lipids should be prevalent in birds that eat lipid-dominated fruit, whereas traits that allow rapid processing of a bulky and watery diet should be prevalent in birds eating sugar-dominated fruits (Witmer and Martínez del Rio 2001). Testing for such a dichotomy in frugivores requires extending the comparison between North American thrushes and Cedar Waxwings to include tropical birds that specialize on lipid-dominated fruit, such as Oilbirds (Steatornis caripensis; Bosque and de Parra 1992) and bellbirds (Snow 1982). In addition, a more detailed look at the digestive traits that allow feeding on lipid-rich fruit is needed. The details and comparative physiology of lipid digestion and metabolism in birds has been relatively neglected (Zurovchak et al. 1999). We predict that a comparative study will reveal higher levels of bile production and higher expression levels of pancreatic lipases and intestinal esterases in birds that specialize on lipid-dominated fruits (Place and Stiles 1992). In addition, birds feeding on lipid-rich fruit should have higher expression of the mechanisms used to transport lipids from the gut into tissues (e.g. higher levels of synthesis of the apoproteins involved in the formation of chylomicrons and lipoproteins) and to catabolize lipids (e.g. high levels of endothelial lipoprotein lipase; Dietschy et al. 1993). The hypotheses that have guided in the nutritional ecology of frugivores by observations of tropical 1993, and It is that those hypotheses have been examined in most in and North American species. (Bosque and de Parra we very little about the digestive and metabolic traits of tropical species. We are of the most basic physiological traits of of birds. that come to as of comparative studies because they are and include are the fruit and the is to the of on species to the less but important and tropical birds. The digestive of birds are remarkably They can in structure and function in to in diet or consumption and can do over a of time (Karasov Many birds a in diet from in to fruit in et al. That is because fruit and are different in nutritional content different digestive strategies (Afik and Karasov 1995, Moermond and Denslow digestive factors which birds can the and the of the what a bird's ability to become or The ability or of birds to digestive processes is important in such (Karasov for example, a bird is unable to retention enzyme or to the of a new it may be unable to to that on the other those traits can be it will be to the is what traits are the of and the time over which The of digestive and gut retention time has been examined in fruit-eating birds in Karasov by transport are in birds (Levey and Karasov 1992, Karasov et al. 1996, Afik et al. in (Karasov and Diamond Karasov 1992). of at least one amino on the other is in the to or in dietary (Levey and Karasov 1992, Karasov et al. 1996, Afik et al. for of intestinal are similar. In small intestinal activity not with carbohydrate content of the diet (Afik et al. 1995, Martínez del Rio et al. 1995, et al. but the activity of an content (Afik et al. 1995, Martínez del Rio et al. 1995, et al. 1998, Levey et al. 1999). gut retention time in the birds eating diets have higher retention times than those eating fruit diets (Karasov and Levey 1990, Levey and Karasov 1992, Afik and Karasov 1995, Karasov gut retention time can be within see Afik and Karasov 1995, Levey and Martínez del Rio 1999). The that is that some digestive are and others are Those that are may have ecological or behavioral For example, the of and to on high diets is to their to intestinal (Afik et al. 1995, Afik and Karasov 1995, Martínez del Rio et al. 1995). A is that and with digestion more than those with birds on a fruit diet do not digestive to assimilate because is more to than are carbohydrates (Afik et al. the time for and for diet may among dietary that do not such differences into et al. 1998). It is that of digestive processes examined (Karasov and Diamond and Diamond 1989, Karasov 1992). do birds to a similarly clear (Karasov is that about avian digestive function is of at least some digestive For example, glucose in primarily transport (Karasov and Hume 1997), but that is the in birds (Karasov and 1994, and Karasov 1996, Levey and 1996, Afik et al. et al. 2001). has and It requires little energy and rate of to the for of nutrient 1993). A major is that will be absorbed is et al. (2001) that to have important behavioral and It may for example, of in which consume large quantities of secondary metabolites in fruits and seeds (Diamond et al. 1999). Such consequences digestion can a between physiology and feeding birds an to such a because their digestive processes are relatively guts and chemically and because their feeding is relatively by the between digestion and more than in most other from chemical and 1987, Martínez del Rio and Karasov have to new insights about digestive function and its behavioral consequences in fruit-eating birds. Those digestive to gut retention nutrient and volume (Karasov 1990, Martínez del Rio et al. 1994, Karasov 1996, and Martínez del Rio 1999). A of the first of those is that retention time and digestive are related to sugar of fruit pulp (Martínez del Rio et al. 1994). The basis for that is that birds can rate of energy by pulp is the gut with a broad of interspecific the to with the that fruit-eating birds eat quantities of fruit that of their per digestion of what they seeds and and gut passage than insectivorous birds Moermond and Denslow 1985, and 1989, Martínez del Rio et al. 1994). However, at the laboratory of the have to that (Karasov and 1996, et al. Levey and Martínez del Rio digestive is not by hexose and retention time either or with hexose of other have to the and Karasov 1998a, Taken together, those results into the of rate of energy or its physiological is that birds do not rate of energy but as to feeding time by digestive efficiency. In other they their to of by they Another is that a assumption of digestion in animals can assimilation a high of and as in the lower gut may osmotic diarrhea and ability to and (Levey and Martínez del Rio 1999). and Martínez del Rio used a that the almost sugar assimilation to gut function in used in data on enzyme and data on gut volume to predict food at sugar They a remarkably between and food and the The of and Martínez del to gut function in frugivores is that feed primarily on many frugivores feed on fruit (Martínez del Rio et al. 1992). gut function in those frugivores requires the rate at which hexoses are in the that we have no of The most used in the the intestinal (Karasov and Diamond may to intestinal tissues and to large of in et al. as in the intestinal of sugar may have a Although many of the of the of have been we have learned in the Levey and Martínez del Rio suggested of gut function in frugivores and Martínez del Rio et al. (2001) and of those in birds. We that the new of gut function in frugivores will not energy but will efficient gut such as levels of expression and distribution of and the that permit digestive processes to at the rate by metabolic The nutritional ecology of frugivores to a large nutrient The reason for that is the of relatively data on the content of such as sugars and lipids in fruit (e.g. Herrera 1987, et al. 1998). we a less about and secondary content of fruit. Yet those may fruit and preferences by or through interactions with metabolites and may even the influence of on fruit preferences and nutrient We that the in on nutritional ecology of fruit-eating birds beyond the gut into the secondary are and into the are and and are or We our of and secondary metabolites by at a content in foods is most from of is by a from animal to percentage from with that as a for has two major to of in fruits can be 1993, Bosque and Levey et al. not only is content of fruit pulp frugivores less than is but that can be is as secondary are to be Those new on the about why most fruit-eating birds on a diet of only fruits and 1989, Levey and Karasov 1989, 1990, 1996, Witmer The on one on content of fruit fruit-eating birds consume to Moermond and Denslow 1985, Bosque and the other most experiments with captive birds on fruit diets that they are not in and that their diet with to and Denslow et al. 1987, Those different are one between and on content of fruit will and assimilation such are because we lack on both fruit and data on content of fruit is and we about assimilation and of birds. to that is the that amino of fruit pulp may be more important than content per because in a amino may a fruit 1998). The to which that and the by which fruit-eating birds the of a diet are as for (Witmer Bosque and et al. 2001). The between fruit secondary metabolites and and is by (2001) study of consumption of fruit by Cedar The fruits of in the but remain through the In the of rapidly the fruit from After a of hypotheses to this Witmer (2001) in the that only fruit when they also from which are only in the In the that and a only when they on both fruit and the They when they with only fruit or only fruit energy to the but little and high levels of a The metabolism of some secondary such as and acids that must to et al. 1995). of the mechanisms for is production of and from amino by of is in et al. 1995). The ingestion of fruit on a for that is by We have on (2001) study because it the of observations with physiological experiments in the laboratory to perplexing More to the it that it may be to to understand the of fruit secondary metabolites to the ecological of between fruits and their The anthropocentric assumption that the study of assimilation in birds has often been to secondary et al. 1993). that are to and laboratory are to be to birds, However, some of those such as that and some have no apparent or on birds and Stiles 1993, et al. and 2001). metabolites in fruit pulp are and have on avian frugivores (Herrera and 1989, and Levey secondary metabolites fruit consumption and Levey Levey and 1997), whereas some it and Stiles 1993, and 1995). gut retention time et al. 1994, but see Witmer whereas some it et al. 1998). may assimilation and 1989, but see some may entail to (e.g. et al. and many are in large The and of secondary metabolites for about and ecology of fruit-eating most fruit-eating birds on They may not be to consume fruits because to do would to of particular secondary metabolites (Levey and Karasov 1989). as secondary fruit may a on a bird's do fruit-eating birds consume species of fruits over a short than one that is such may result from the of of a given secondary are there exclusively species of The physiological to with large of and may carry The of secondary metabolites in fruits is and the of to such almost an important that must be are the of secondary metabolites on frugivores and can we a that related of (e.g. and with on It may be that of can be with different hypotheses of function and Levey metabolites are in fruit, but they also because of production by and More than 20 years have why fruits seeds and least for fruit, and the hypotheses remain For example, we have not nutrient and and production by influence seed Consequently, the function of the of by of one of the by for of humans. hypothesized that of by in contemporary may a of an an between frugivory and consumption and that a as an and in fruit-eating there is for that We little about levels of in fruit, about levels that and in frugivores, and about the of different species to A but as of is that frugivores will have higher of than will The of fruit-eating birds with the of to study metabolism in and and a to may a to the of the is about in fruit. Even less is about for among fruit-eating birds. and have shown that some can have very low levels of and that many plant to relatively abundant but little The of appears suited to in the of a high of et al. 1999). Indeed, to remarkably and Martínez del Rio fruit pulp and are fruit-eating birds We predict that many fruit-eating birds are We also predict that avian frugivores that feed on and watery fruit will traits similar to those by birds with and ability to et al. (2001) used a comparative to that with They that an in diet from to both frugivory and with a in the and a in the the plant we hypothesize that some have of a ecological In particular, they may a of seed dispersers by an but (e.g. et al. 1998). It has long been that many birds to a diet presumably to energy for et al. and Willson is how that can be within individuals and among Even some to on fruits to 1986, 1998). In that fruit in diets of most species thought to be insectivorous (e.g. and than of fruit species more to than also Jordano and 1995). of fruit in the diet with in Those strongly that fruit is important to birds. only do birds easily carbohydrates and lipids from fruit pulp, but because in fruit can be very abundant and they also may less energy for fruits than for our no study has the physiological efficient from fruit sugars and from the ecological and of of frugivory in are to in which However, for more than studies that must also be and that those must be and 1994, Karasov and 1998, and 1998, and birds for are with the of and two nutrients that are by feeding on two fruit and on captive birds fruit and have shown that in is on a diet of fruit and and 1994). will be to and factors that the of fruit and used in the by birds. We have why of nutritional ecology is to understanding and of fruit-eating birds. Most of the lessons are not new 1998) and are to other taxa of and their It will guts to in some and in It is a to our and our in digestive physiology of birds and to We also and Witmer for and