S37.3: Effects of plant secondary metabolites on diet choice and digestion

1Department of Zoology, University of Florida, Gainesville, Florida, 32611-8525, USA,  fax 352 392 3704, e-mail DLEVEY@zoo.ufl.edu; ²Department of Biology, Berry College, Mt. Berry, Georgia, 30149, USA.

Studies of diet selection in birds have typically focused on nutritional contents and availability of food items. Two realisations have recently forced a reevaluation this focus. First, the way in which a food item is internally processed by a bird may have a major impact on the bird's behavior and ecology (Karasov & Diamond 1988). Because different birds can process dietary constituents in radically different ways (e.g. Grajal et al. 1989; Martínez del Rio & Stevens 1989), an approach that fails to take digestive physiology into account can be seriously misguided (Martínez del Rio & Restrepo 1993). Second, it is possible that coevolutionary interactions between birds and plants can explain patterns of diet selection among birds that consume plant parts (Snow 1971). In particular, the consequences to both birds and plants when foliage is consumed is vastly different than when a fruit is consumed.

Here we review the influence of plant secondary metabolites on diet choice in birds. Note that this topic lies at the intersection of the two new emphases we described above. Secondary metabolites not only have a potentially large impact on avian physiological processes (e.g. Guglielmo et al. 1996) but many are likely the result of plant-animal interactions, as well (Rosenthal & Janzen 1979).

In general, seeds are energy-rich and many are of a size easily handled by birds (0.01 - 0.0001g; Harper et al. 1970). Furthermore, they are often extremely abundant, reaching densities in some habitats of 31,000 seeds m^-2 (Leck et al. 1989) and 188 kg/ha (Pulliam & Brand 1975). From the perspective of avian ecology, seeds are a crucial resource. From the perspective of plant ecology, seeds represent a life history stage at which mortality is generally highest and chemical protection is common (Janzen 1971; Harper 1977). Given these two perspectives, it is puzzling that the influence of secondary chemistry on seed choice and nutrition in birds is so poorly understood. Research on diet selection in granivorous birds has instead focused on morphological and energetic factors (Stephens & Krebs 1986; Díaz 1996). Yet, seeds that are high in energetic content and of an appropriate size are often avoided by birds, suggesting the presence and importance of secondary compounds (Pulliam 1980). Even more convincing is an analysis by Diaz (1996) in which the diets of finch species were compared world-wide. He found that seeds of several plant families (Leguminosae, Malvaceae, and Convolvulaceae) are consistently avoided by birds and seeds of one family, Poacae, are consistently taken. Seeds of the avoided families are significantly more likely to contain tannins and alkaloids than seeds of the preferred family.

Essentially the only set of experimental studies examining the influence of secondary compounds on seed-eating birds in an evolutionary context is with woodpeckers and jays that consume acorns. (Agricultural studies on birds and secondary metabolites in grains are noted in the final section of this manuscript.) In several species, acorns comprise a major portion of the diet and can be especially important for winter survival and breeding success (Smith 1986; Koenig & Mumme 1987; Smith & Scarlett 1987). Many species of acorns, including those frequently consumed, are high in tannins (Koenig 1991). Tannins are water-soluble phenolic compounds that occur widely among plant families. Their toxic properties are multi-faceted and depend upon the type of tannin and the species of consumer. In general, tannins bind with protein and form insoluble precipitates, thereby reducing protein availability of ingested food and hydrolytic activity of proteinaceous enzymes (Goldstein & Swain 1965; Feeny 1969; Short 1976; Swain 1979). In addition, they can be directly toxic by damaging gut epithelia and causing liver necrosis (Bernays et al. 1989). The extent to which tannins influence nutrient digestibilities is a focus of current debate (e.g. Elkin et al. 1996).

Interest in acorn consumption by birds was aroused by the apparent lack of avian physiological adaptations to counteract tannins. How can Acorn Woodpeckers Melanerpes formicivorus, Scrub Jays Aphelocoma californica, and Blue Jays Cyanocitta cristata rely so heavily on acorns? Considering that acorns are inherently low in protein content (Koenig 1991), binding by tannins of what little protein is present would seem especially detrimental to the nutritional state of the bird. As demonstrated with domestic fowl, tannins can have pronounced negative effects on growth and digestive efficiency, even when dietary protein is relatively high (Marquart & Ward 1979; Chami et al. 1980; Elkin et al. 1990).

Experiments with captive Scrub Jays, Blue Jays, and Acorn Woodpeckers have demonstrated, with one exception, that these species lose body mass on diets of exclusively acorns and that acorns containing higher levels of tannins usually result in more rapid loss of body mass (Koenig & Heck 1988; Koenig 1991; Johnson et al. 1993; Dixon et al. 1997a). The one exception was with Acorn Woodpeckers, which were able to maintain body mass when fed acorns containing relatively low levels of tannins (Koenig & Heck 1988). Yet, such studies are difficult to interpret with respect to secondary chemistry because the evidence is correlative (Bernays et al. 1989) -- covarying levels of lipids or other nutrients may account for the patterns.

Koenig (1991) experimentally examined the effect of added tannin on metabolizable energy coefficients of Acorn Woodpeckers. Two types of tannins, tannic acid (a hydrolysable tannin) and quebracho (a condensed tannin), were varied within limits of their natural occurrence. Quebracho significantly reduced metabolizable energy coefficients, whereas at comparable concentrations tannic acid did not. However, tannic acid did significantly reduce metabolizable energy coefficients when lipid levels were increased. Despite these detrimental effects of tannins on digestion, Acorn Woodpeckers displayed similar metabolizable energy coefficients on acorn meal and crickets, which are low in tannins. This lack of difference led Koenig (1991) to conclude that Acorn Woodpeckers appear well-suited to dealing with the physiological effects of tannins in their diet.

Fleck & Tomback (1996) experimentally manipulated lipid, protein, and tannin levels in the diets of Western Scrub Jays. The birds lost most body mass on a low-protein, low-lipid, high tannin diet that most closely matched the nutritional composition of a type of acorn they commonly consume. More generally, the amount of tannin in the diet was positively correlated with the amount of body mass lost during trials. Furthermore, jays were able to detect differences in tannin levels and preferred diets low in tannin.

The effect of tannins on the nutritional state of acorn-consuming birds is not simple -- both of the above studies found significant interactions between tannin and nutrient levels. Koenig (1991) found that tannic acid significantly reduced metabolizable energy coefficients when lipid levels were high but not when they were low. Fleck & Tomback (1996) found that the effect of tannic acid on body mass loss was eliminated when protein levels were high, a result corroborated with domestic ducks fed high tannin, high amino acid diets (Elkin et al. 1991). Presumably, binding by tannins is saturated at high protein concentrations, thereby allowing assimilation of the 'excess' protein.

The ameliorating effect of high protein levels on tannic acid raises the possibility that acorn-consuming birds may behaviourally counter the detrimental effects of tannins by increasing their consumption of protein. In fact, an 'extra' protein source -- cuculionid larvae -- is naturally present in many acorns. Perhaps by consuming these larvae, birds can compensate for high levels of tannins. Indeed, Johnson et al. (1993) found that Blue Jays did not lose body mass when feed acorn diets supplemented by 5 g d^-1 of cuculionid larvae. However, a more recent study revealed that Blue Jays prefer acorns without cuculionid larvae, that they rarely ingest the larvae when encountered, and that the number of larvae required to total 5 g d^-1 is prohibitively high (Dixon et al. 1997b).

A final means by which acorn-consuming birds may lessen effects of tannin is to store acorns under conditions that facilitate natural decomposition of the tannins. This hypothesis is bolstered by the fact that jays and woodpeckers commonly cache acorns for long periods. Dixon et al. (1997a) mimicked such caches and compared performance of Blue Jays fed cached versus uncached acorns. They found no difference in weight loss between birds on the two diets and thus rejected the hypothesis.

Whereas seeds are generally high in nutrients because they must supply sufficient resources for seedling establishment, leaves tend to be low in nutrients and high in bulk (Robbins 1993; Van Soest 1994). This means that herbivorous birds must consume large quantities to satisfy their nutritional requirements. At least two factors are thought to constrain their ability to do so: gut volume is tightly restricted due to requirements of flight (Morton 1978; Dudley & Vermeij 1992) and secondary metabolites, which are common in leaves, may reach toxic levels. Not surprisingly, relatively few extant bird species (ca. 3%) rely heavily on foliage (Morton 1978). For those that do, diet selection is thought to be especially important (Sedinger 1997).

Much work has focused on the importance of nutrients and secondary metabolites in diet choice of herbivorous birds. Yet, few studies have examined the influence of both. In a recent review of 51 studies on diets in waterfowl and grouse, Sedinger (1997) found that 17 examined nutrient content of diet, four examined secondary metabolites, and only one examined both. That study, by Buchsbaum et al. (1984), aroused controversy.

Based on feeding experiments and field observations, Buchsbaum et al. concluded that diet selection in Canada Geese Branta canadensis is based on a hierarchical system of feeding cues (Buchsbaum et al. 1984; Buchsbaum & Valiela 1987). Nutrients, fibre, and secondary metabolites all appeared influential, but secondary metabolites (primarily phenols) played the greatest role. Gauthier & Bedard (1990) extended these studies by simultaneously manipulating phenol and protein content of grass in feeding experiments with Snow Geese Chen caerulescens. They found that ferulic acid but neither tannic nor p-coumaric acids depressed feeding and that the effect of ferulic acid depended upon the protein content of the diet. When ferulic acid was absent, protein content did not influence feeding behavior but when ferulic acid was present, protein content enhanced feeding, thereby countering the deterrent effect of ferulic acid.

An important lesson emerges from the above studies: numerous nutritional and chemical characteristics of browse influence diet selection and because none of these characteristics occur in isolation, all need to be considered simultaneously. Put another way, interactions among nutritional and chemical factors may explain more variation in avian feeding behavior than any factor singly. In fact, such interactions render invalid any interpretation based on consideration of a single factor (Sokal & Rohlf 1981). Numerous studies that clearly demonstrated effects of nutrient content or secondary metabolites on diet choice (e.g. Moss 1972; Sedinger & Raveling 1984; Remington & Braun 1985; Jakubas et al. 1989) thus need reevaluation.

A new generation of studies examine diet choice among herbivorous birds in a multifactorial context. For example, Gauthier & Hughes (1995) asked why Snow Geese consume willow only during a narrow period of leaf development. They concluded the behavior is best explained by the ratio of phenol to protein content, which is minimal during the stage of leaf development when geese consume the leaves. Neither protein content nor phenol content are especially high or low during this stage.

By far the most complete set of 'new generation' studies is that on patterns and consequences of diet selection in Ruffed Grouse Bonasa umbellus. During the winter, a large proportion of the grouse's diet is composed on Quaking Aspen Populus tremuloides buds. Birds are highly selective, feeding only from certain trees (Doerr et al. 1974). Preference for these trees is correlated with lower than average levels of coniferyl benzoate (a phenylpropanoid ester found in their flower buds; Jakubas et al. 1989) and best explained by both coniferyl benzoate and crude protein content (Jakubas & Guillion 1991). Grouse preference for other winter browse is likewise influenced by both nutritional content and plant secondary metabolites (Guglielmo & Karasov 1995).

What makes the work on Ruffed Grouse especially powerful is its focus on mechanisms by which coniferyl benzoate affects feeding behavior. Traditionally, such plant secondary metabolites have been viewed either as toxic or as detrimental to nutrient assimilation. Coniferyl benzoate, however, does not appear toxic, even when ingested in fairly high concentrations (Jakubas et al. 1993a). And, birds can quickly habituate to its irritant properties (Jakubas et al. 1993b).

Negative effects of consuming coniferyl benzoate appear to take place only after absorption. In general, biotransformation (the means by which foreign compounds are converted into other compounds and excreted) may result in molecules being lost via conjugation with xenobiotics and may also threaten pH homeostasis (Foley 1992; Foley et al. 1995; Illius & Jessop 1995). In either case, substantial amounts of energy and nitrogen could be lost via detoxification processes on diets high in coniferyl benzoate. Indeed, such losses appear important. As coniferyl benzoate concentrations in the diet increased, grouse showed increased excretion of glucoronic acid and ornithine (both detoxification conjugates), increased excretion of ammonium (suggesting problems with pH homeostasis), had up to 90% higher nitrogen requirements, and had increased energetic costs of 10-14% (Guglielmo et al. 1996).

The influence on birds of secondary metabolites in fruits is more controversial than is the influence of secondary metabolites in seeds and foliage. At the heart of the controversy lies the recognition that unlike other plant parts, fruits 'are made to be eaten' (Snow 1971). Whereas compounds that deter consumption are expected in seeds and foliage, their presence in ripe fruit presumably reduces consumption of the fruit and hinders seed dispersal, thereby decreasing plant fitness. Thus, one would expect such compounds to be broken down during fruit ripening. (Presence of secondary metabolites in unripe fruit is easily explained: consumption of unripe fruits is detrimental to plant fitness because it usually means destruction of immature seeds.) Although concentrations are almost always lower in ripe than unripe fruit, many species of ripe fruit contain toxic levels of secondary metabolites in their pulp (see reviews by Herrera 1982; Barnea et al. 1993; Cipollini & Levey 1997a). In the case of some Solanum species, concentrations of glycoalkaloids are high enough to kill a 1-2 kg mammal after consumption of less than 10 fruits (Cipollini & Levey 1997b). In this section, we discuss the effect of secondary metabolites on fruit consumption by birds and summarise explanations for the occurrence of these compounds.

Secondary metabolites found in fruit are commonly found elsewhere in the parent plant (Ehrlen & Eriksson 1993). In general, they seem to have a detrimental effect on fruit consumption. Birds typically avoid or do not prefer species known to contain high levels of secondary metabolites (Kear 1968; Sherburne 1972; Jordano 1988; Cipollini & Stiles 1993a; Cipollini & Levey 1997b; Levey & Cipollini 1998). Likewise, fewer species of both birds and mammals feed on fruits from genera with toxic fruits than from genera with non-toxic fruits (Herrera 1982).

By the same token, many fruits containing high levels of secondary metabolites are consumed by birds (Heiser 1969; Herrera 1982; Jordano 1988; Cipollini & Levey 1997a). Some secondary metabolites even stimulate fruit consumption and promote gain in body mass in frugivorous birds (Bairlein 1996). These observations have led to suggestions that fruit-eating birds possess adaptations to detoxify or avoid detrimental effects of fruit secondary compounds. Examples include especially large livers (Pulliainen et al. 1981; Eriksson & Nummi 1982; ; but see Herrera 1984) and biochemical processing of the compounds in such a way as to avoid their detrimental effects (Struempf & Martínez del Rio, unpublished manuscript). Whatever the mechanism, it appears that fruit-eating birds have a greater tolerance of secondary compounds than non-fruit-eating birds. Witness Herrera's (1985) observation that frugivorous birds consume more aposematically coloured insects than non-frugivorous species, presumably because they are better able to deal with toxic compounds (many derived or sequestered from plants).

The extent to which fruit secondary metabolites may force birds to diversify their diet has been the focus on much debate. Izhaki & Safriel (1989) hypothesised that secondary metabolites reduce digestibility of protein in fruit pulp, thereby forcing birds to forage on insects to attain sufficient protein. They pointed out that this would benefit the plant via increased seed dispersal when birds leave the plant to forage elsewhere. And, they demonstrated that birds lost body mass on exclusive fruit diets, even when nitrogen intake appeared sufficient. Apparently, secondary metabolites greatly reduced the availability/digestibility of fruit protein. Mack (1990), however, pointed out that it makes little evolutionary sense to both provide protein as a reward for fruit consumption and simultaneously make it less available (see also Cipollini & Levey 1997a)

Two other hypotheses address the proposed link between secondary metabolites and the broad diets of frugivorous birds. First, birds may be forced to consume many types of fruits to avoid ingesting too much of a particular type of secondary compound (Jordano 1988; Levey & Karasov 1989; Mack 1990; Izhaki 1992). Alternatively, birds may diversify their diets simply to gain sufficient amounts of particular fruit constituents (e.g. uncommon amino acids). A challenge for future research is tease apart these hypotheses: Do birds consume many types of fruits and insects because they are balancing their diet or because they are avoiding toxic doses of specific secondary metabolites? This issue is currently controversial. Evidence summarised in the next two paragraphs supports both hypotheses. Ultimately, the answer is likely to lie somewhere between the two extremes.

Work with captive birds has shown that few species can maintain body mass on pure fruit diets (Berthold 1976; Moermond & Denslow 1985; Levey & Karasov 1989; Izhaki & Safriel 1990; Izhaki 1992), although some can (see review by Bairlein 1996). Because fruit pulp is notoriously low in protein (Moermond & Denslow 1985; Herrera 1987; Jordano 1992), the interpretation has been that frugivorous birds must diversify their diet to maintain nitrogen balance. This interpretation is bolstered when one considers that the protein content of fruit may be over-estimated by current methods of analysis (Izhaki 1993), protein may be made unavailable by secondary metabolites (Izhaki & Safriel 1989), and the amino acid composition is non-balanced (Izhaki 1998).

It is important to keep in mind that fruit secondary metabolites can affect fruit choice in ways not related to their potential toxicity. In experiments with Garden Warblers Sylvia borin fed artificial diets with an without an extract from black elder berries, Bairlein (1996) found that the birds lost body mass on the diet without the extract (i.e. without any plant secondary metabolites). In contrast, they consumed more of the diet with the extract and were able to maintain or gain body mass. Furthermore, they preferred the extract-containing diet in choice trials. Cipollini & Stiles (1993a) also found that addition of fruit secondary metabolites increased consumption of artificial diets by frugivorous birds in some trials.

Understanding why and how secondary metabolites influence bird feeding behavior holds promise for ecologically-based pest management. In particular, naturally-occurring repellents can be used to deter crop damage by birds in a preventative, not reactionary, way (Van Vuren & Smallwood 1996). Current agricultural research focuses on how bird-resistant and non-bird-resistant strains of crops differ in type and quantity of secondary metabolites (e.g. Muellerharvey & Reed 1992; Bullard & York 1996) and how use of deterrent compounds with low toxicity may help protect crops and stored products in situations where pesticides would be hazardous (e.g. Crocker et al. 1993). An alternative approach is to determine the relationship between repellency and chemical structure of a secondary metabolites and then genetically engineer crops to produce biologically active analogues of naturally-occurring compounds (Jakubas et al. 1992).

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