- Email: [email protected]
Poultry Nutrition: A Comparative Approach
2005 Poultry Science Association, Inc.
Poultry Nutrition: A Comparative Approach Department of Animal Science, University of California, Davis, California 95616
Primary Audience: Poultry Nutritionists SUMMARY Although a variety of scholarly papers and books classify chickens and turkeys as granivores, they are omnivores and do not have the food preferences, digestive anatomy, or nutritional strategies that would classify them as granivores. Their wild relatives consume a very wide variety of food items of both plant and animal origin, and seeds are not often a primary component. Intake of insects by jungle fowl chicks and wild turkey poults exceeds 50% of their diet, and adult females increase their intake of insects at the time of reproduction. In the case of jungle fowl, termites and bamboo mast are preferred foods in the area of Southeast Asia where domestication likely occurred. The nutritional strategy of omnivores is a composite of that of faunivores, frugivores, granivores, and herbivores. Appreciating the nutritional strategy of birds that eat diverse types of foods illuminates the potential capabilities and limitations of generalists, like chickens and turkeys. The marriage of comparative genomics with comparative nutrition is likely to be fertile ground for future advancements in applied poultry nutrition. Key words: nutritional strategy, omnivore, Galliformes 2005 J. Appl. Poult. Res. 14:426–436
DESCRIPTION OF PROBLEM The dietary preferences, gastrointestinal anatomy, digestive physiology, biochemical capabilities, and commensal microflora of a bird are collectively known as its nutritional strategy. Nutritional strategies of birds are diverse and permit specialization on foods ranging from nectar to grass to other vertebrates. The specific gastrointestinal anatomy, digestive physiology, and metabolic capabilities of each species have coevolved with the types of foods consumed, so species eating similar food types often have similar nutritional strategies [1, 2]. Poultry nutritionists should have an understanding of the diverse nutritional strategies among birds because it provides an appreciation for the capabilities, limitations, and po1
tentials of chickens and turkeys. The National Institutes of Health, which is devoted to human biology, had the wisdom to fund the sequencing of the avian genome because the comparative approach to biology reveals many secrets that would otherwise not even be known to exist. In a similar manner, the comparative approach to nutrition, including using chicks, rats, and pigs as models, has revealed much about optimum nutrition for humans. A comparative approach to poultry nutrition is likely to have similar benefits. Such a comparative approach requires looking outward from poultry into the diverse avian taxa. The purpose of this paper is to provide an overview of the nutritional strategies of birds and to describe the place of chickens and turkeys in this bigger picture. In order to accomplish this,
To whom correspondence should be addressed: [email protected].
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K. C. Klasing1
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to the Americas, probably sometime around A.D. 500. Two other subspecies remain in Mexico, Rio Grande (M. g. intermedia) and Gould’s (M. g. mexicana) and are likely to be very closely related to M. g. gallopavo. The Ocellated Turkey (Meleagris ocellata) is in the same family as wild turkeys and is found only in eastern central Mexico; more distantly related is the grey partridge (Purdix purdix) [10].
Phylogeny
Dietary Preferences of Birds
Chickens, turkeys, and quail are Galliformes, which is a large order containing more than 200 species, including all of the pheasants, grouse, quail, turkeys, guinea fowl, and partridges. The 200 plus species in this order are all omnivores. Based on morphologic, behavioral, and genetic evidence, the domesticated chickens descend from a single ancestor, the Red Jungle Fowl (Gallus gallus), originating in Southeast Asia, most likely Thailand [3, 4, 5]. The 5 subspecies of Red Jungle Fowl are differentiated by color and subtle differences in morphology. Mitochondrial DNA [3] and microsatellite markers [6] suggest that Gallus gallus gallus was likely the primary ancestor to the diverse breeds of the domesticated chicken (Gallus gallus domesticus); although a contribution by other subspecies, such as G. gallus spadiceus, has not been excluded. Based on cytochrome C gene homology, Gallus appears to be basal to pheasants [7]. The species most closely related to G. gallus are G. varius, G. Lafayettei, and G. sonneratii. More distantly related are peacock-pheasants (Polyplectron) of Southeast Asia, koklass (Pucrasia) of Asia, and chachalaca (Ortalis) of Latin America. Domestic turkeys were domesticated from wild turkeys (Meleagris gallopavo). The wild turkey is indigenous to North America and had an historical range that included much of the eastern and portions of the southwestern US, northern Mexico, and southeastern Canada. Six geographically isolated subspecies are recognized [8]. Spaniards brought back to Europe the southern Mexican subspecies, Meleagris gallopavo gallopavo [9] This subspecies is the ancestor to the modern domestic turkey, not the familiar Eastern Turkey of the US (M. g. sylvestris). The M. g. gallopavo now appears to be extinct in the wild, but its genes are preserved in the domestic turkey. Domestication occurred before Europeans arrived
Across the >9,000 species of birds, there is an almost continuous distribution of dietary preferences (Table 1) and nutritional strategies [1, 2]. The largest numbers of species use their power of flight to select food items with the highest concentration of digestible nutrients and to avoid food items high in roughage (Figure 1). The most nutritious foods are other animals, seeds, fruit, and nectar. The large number of insectivorous, frugivorous, and granivorous avian species account for the fact that there are more than twice as many avian species as mammalian species. The advantage afforded by flight also comes with evolutionary pressure to keep the size of the digestive tract and the weight of its contents to a minimum. These 2 factors make it impractical for flying birds to weigh more than 12 kg. Studies of mammalian herbivores suggest that the size of a digestive tract large enough to digest leaves requires the owner to have a body of at least 15 kg [11, 12]. These constraints prevent flying birds from occupying the niche filled by mammalian bulk-roughage feeders (e.g., cattle, deer, sheep). Thus, the capacity of flight that makes ubiquitous vegetation readily obtainable restricts its digestion. Herbivorous birds capable of flight must always be highly selective and consume plant parts that are relatively high in protein and low in fiber, such as rhizomes, buds, flowers, catkins, very young leaves, and young grasses. Mature leaves, stems, and grass are not selected. Many species are omnivores and consume a wide variety of foods of plant and animal origins. In the wild, their exact choice is determined by a combination of factors, including seasonal availability of food, foraging efficiency, changing nutrient requirements, palatability, and predator patterns. The types of foods consumed by a species can have considerable seasonal variability, espe-
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the phylogenetic position of chickens and turkeys is provided in reference to other species, the dietary preferences of jungle fowl and wild turkeys is detailed in the context of other avian species, and the nutritional strategy of chickens and turkeys is compared with that of others. A second goal is to exemplify ways that the nutritional strategies of birds diverge from that of mammals and to provide rationale, where possible.
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428 TABLE 1. Classification of dietary preferences of birds Category
Chickens, turkeys, some ducks (including domestics), quail, pheasants, grouse, cranes, bustards, crows
Hawks, owls, eagles, falcons, vultures Loons, pelicans, storks, cormorants, mergansers, osprey, kingfishers Woodpeckers, swallows, wrens, flycatchers
Ostriches, some ducks, tinamou Hoatzin Geese, swans Sparrows, finches, some pigeons, some parrots Hummingbirds, sunbirds, lorikeets, honeyeaters Toucans, manikins, tanagers, some pigeons, bulbuls
cially in temperate climates, and the nutritional strategy adjusts accordingly. For example, the mixture of foods consumed by many omnivores is often higher in insects in the summer and higher in foods of plant origin in the winter. Among Galliformes, the winter shift to high fiber foods is matched by increased cecal size, microbial fermentation, and retention time of the digesta [13]. Some species, especially many songbirds, make even more extreme annual shifts. A common dietary pattern is a diet of insects during the summer and a complete switch to fruits during the winter. The change in nutritional strategies, following such switches, can be dramatic [14, 15, 16]. Dietary Preferences of Jungle Fowl Jungle fowl are not granivores. As their name suggests, Red Jungle Fowl are birds of tropical and subtropical forests, not grasslands where seeds and grains would be available. In undisturbed habitats of Southeast Asia, the Red Jungle Fowl prefers to live in bamboo forests [17, 18]. In areas of human habitation and agriculture, jungle fowl prefer the remaining forested areas and forest edges, especially those with an understory with tall herbaceous shrubs [19]. In Southeast Asia and in India, Red Jungle Fowl are most likely to be found in areas with abundant termite populations. All 5 of the jungle fowl species are classified as highly omnivorous, eating a very wide variety of food items of plant and animal origin throughout the year, and seeds are often only a minor component.
A proper quantitative study of the food preferences of jungle fowl in their native habitat has not been conducted. However, field accounts and inspections of crops from birds killed by hunters provide a good picture [17, 19, 20, 21, 22, 23]. Foods of plant origin that are frequently consumed include fruits and berries from trees and herbaceous shrubs, seeds from a variety of plants especially bamboo seeds when available, nuts, young shoots of bamboo and other grasses, leaves, petals, and tubers. When near villages and agriculture, they eat readily available rice, millet, and vetches, but they are not reported to especially pursue these foods. Foods of animal origin that are frequently consumed are termites and their eggs and pupae, winged ants and their eggs and pupae, earthworms, roaches, grasshoppers, spiders, moths and their caterpillars, beetles and their grubs, small crabs, snails, centipedes, and lizards. Invertebrates are obtained by scratching at leaf litter in the forest. Insect communities in elephant droppings may be an important food source in many locations [19]. In adults, foods of plant origin are present in quantitatively greater amounts than those of animal origin, and at many times of the year, fruits are dominant. However, in most of the range of the Red Jungle Fowl, termites and their eggs and pupae appear to be the preferred food and are the most likely food item to be found in the crops of birds, where they are sometimes found in the hundreds [17, 21]. Birds consume adults leaving mounds, but they also scratch mounds to
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Generalist feeder Omnivores Animal matter Faunivores Carnivores Piscivores Insectivores Plant matter Florivores Herbivores Folivores Graminivores Granivores Nectarivores Frugivores
Examples
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expose nurseries. Apparently, the preference for termites is not unique to jungle fowl but is common among most of the pheasant species of Southeast Asia. Foods of animal origin are dominant in the diet of chicks. Again, termites and their eggs and pupae are often the principal type [17, 21]. In one study, the breeding season was matched to the annual cycle of termite availability [19]. Jungle fowl, like most omnivores, are generalists and consume foods on an opportunistic basis and appear to conform to theories on optimal resource allocation [24] and optimal foraging strategies [25]. Red Jungle Fowl spend 90% of the active part of their day in activities associated with foraging for food, especially pecking and scratching at the ground [26]. Young Red Jungle Fowl chicks are able to select among foods to meet their protein requirement [27]. Hatchling chicks in wild populations of partly domesticated chickens choose a diet that is about 60% vertebrates [28]. The innate preferences of domestic chicks for specific colors and sizes of food items and the dependency of this preference on whether the food is perceived to be a fruit or an insect
are likely to be a holdover of foraging strategies of wild jungle fowl [29]. Red Jungle Fowl × White Leghorn crosses have revealed interesting genetic associations with feeding behavior [24], and the quantitative trait loci approach allows mapping specific behaviors to chromosome locations and eventually should permit the identification of sets of genes that control feeding behaviors. Changes in wild populations during domestication illustrate the effects of genetic selection in such a clear way that Darwin [30] devoted the first chapter of his classic book, The Origin of Species, to this topic. Jungle fowl have been kept by humans for about 8,000 yr [31], but during most of this time, selection was for fighting and religious purposes, and selection for agricultural traits was minimal [32]. The idea of selective breeding for productivity (body size or egg production) likely started with the Romans before the time of Aristotle (384 to 322 B.C.), but it was not sustained and appears to have died out, only to be revitalized a few 100 yr ago. An appreciation for the efficiency of feed utilization occurred only about 100 yr ago [33]. The progress in selecting
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FIGURE 1. Proportions of avian and mammalian families feeding on different food categories.
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Dietary Preferences of Turkeys Because the wild turkey is a very important game species that is heavily managed by state and federal agencies, its feeding habits and natural foods have been very well studied. The goal of this extensive literature is to maximize turkey habitat, reproduction, and harvest. Unfortunately, the natural history of the Mexican subspecies M. g. gallopavo, which is the direct ancestor of domestic turkeys, is unknown because it now is apparently extinct. Several excellent reviews on the nutritional biology of M. g. silverstris, M. g. intergrade, and M. g. Merriam found in the US are available [9, 36, 37, 38]. All good turkey hunters know the food and the feeding behavior of wild turkeys, and their wisdom can be readily consulted in a plethora of hunting magazines. Throughout most of their historical range, turkeys live in forested areas and depend heavily on foods produced by the trees [38]. Since the introduction of agriculture, turkeys have increased their consumption of grains, but turkeys are not granivores. Even when plentiful, grains, such as corn, oats, milo, and barley, are not typically a major part of their diet unless their natural foods become unavailable because of drought, snowfall, overpopulation, or loss of habitat due to clearing. Wild turkeys consume a diverse mixture of foods of animal origin and those of plant origin, making them omnivores. The contents of 524 turkey crops and gizzards from Virginia included more than 350 plant species and 300 invertebrate species [39]. Feeding methods include whole ingestion, picking, stripping, clipping, and scratching [38, 39]. Acorns, corn, beechnuts, and other seeds are consumed whole without shelling. Most insects are also consumed whole, although walking sticks and grasshoppers may be battered about to reduce their size before swallowing. Small seeds, such as those from grasses and sedges and the fruiting heads of buttercups and violets, are stripped by
a forceps-like action of the beak. Picking and clipping are used to obtain buds, fruits, and vegetive parts of plants, such as young grass and fern fronds. Scratching is done to locate invertebrates, mast (acorns, beech nuts, pine seeds), fruits, and tubers in the leaf litter of the forest floor. Scratching by turkeys in the leaf litter is methodical and stereotyped leaving a V-shaped scratch. Wild turkeys forage throughout the day, but most feeding activity occurs during the first 2 to 3 h after leaving the roost at daybreak and 2 to 3 h before sunset. Aldo Leopold [40] described why turkeys choose specific food items and provided observations and citations to support his conclusions. Though considerable additional work has been done, Leopold’s work demonstrates that theories on optimal foraging and resource allocation are applicable to turkeys. Wild turkey diets are composed mostly of plants. Depending on the subspecies, location, and season, the percentage of the diet of adult turkeys consisting of animals ranges from 5 to 40%. Of the animals consumed, insects usually predominate, especially grasshoppers, crickets, beetles, ants, ticks, and fly larvae. Spiders, millipedes, snails, salamanders, frogs, toads, lizards, snakes, fiddler crabs, and other small invertebrates are also consumed when encountered [9, 39]. Insects are of critical importance to poults, and survival is low in habitats that do not support large insect populations. The intake of insects by young poults has been estimated to be about 60% of the diet and decreases with age [38, 41]. As stated above, the nutritional biology of the southern Mexican (M. g. gallopavo) subspecies that is the direct ancestor of the domestic turkey is unknown; however, the habitat of east-central Mexico, where it was indigenous, is tropical deciduous forests and mountain pine forests. Acorns would not likely have been a part of their diet in much of their range. The 2 other Mexican subspecies, Rio Grande (M. g. intermedia) and Gould’s (M. g. mexicana), differ from the North American subspecies by eating a greater proportion of insects throughout the year, due to their greater availability, and also consuming fruits of wild tomatoes, junipers, and manzanitas and the seeds of cacti, figs, capulin, acacia, palms, and palmettos [36, 42]. Subspecies of wild turkeys differ in terms of range, appearance, behavior, physiology, and genetic characteristics. Experi-
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for efficiency was rapid, and in the mid-1990s, a 4-wk-old broiler was more than twice as efficient as a jungle fowl of the same age [34, 35]. The basis for this increased efficiency is not due to better digestive efficiency or lower metabolic rate but due to a high rate of food intake and growth rate. This is facilitated by much larger relative intestinal mass, especially the ileum.
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Strategies and Adaptations Poultry are omnivores, and the anatomy and function of their digestive tracts are a composite of all of the specialist species, including faunivores, granivores, and herbivores. Consequently, it is important to have an appreciation for the diversity of digestive strategies and adaptations found in birds that specialize on diverse food items. Distantly related birds eating similar diets often have very similar nutritional strategies and can extract similar nutritional value from their diet [1, 15]. At the morphological level, all birds have their digestive tracts built out of the same units in the same order but with wide variations in design, depending upon the type of diet typically consumed. The avian digestive tract has a greater number of organs than their mammalian counterparts, and there is greater interorgan cooperation. Storage, enzymatic digestion, and mechanical digestion are divided among the crop, proventriculus, and gizzard, respectively. Except for ostriches, the large intestine of birds is considerably smaller than the small intestine. Consequently, the intestine distal to the ileum is usually referred to as the rectum and not the large intestine. When ceca are present, they are paired, whereas mammals have a single cecum. Digestive morphology is extremely variable among species and ranges from very simple, almost tube-like tracts of frugivores and nectarivores to very complex highly convoluted tracts of herbivores. Herbivorous species require symbiotic microflora to aid in digestion (alloenzymatic digestion) and have tracts with large ceca. More subtle functional adaptations are required to accommodate the physical and nutritional characteristics of the food. Adaptation found in various birds include 1) the capacity to egest the exoskeleton of arthropods, the bones of vertebrate prey, or seeds of fruits; 2) the ability to concentrate dietary lipids in the proventriculus; 3) the capacity to sort cell wall components so that only fermentable components enter the ceca and the refractory components move on to the
cloaca; 4) the consumption of feces originating from the ceca in order to obtain microbial protein, energy, and vitamins; 5) and the ability to modulate the rate of passage of digesta to match the type of feedstuff consumed. Poultry utilize strategies 3 to 5 but not the first 2. Figure 2 summarizes 4 typical nutritional strategies. The majority of avian species use their capacity of flight to procure the most nutritious and digestible food items and rely exclusively on autoenzymatic digestion (strategy 1, Figure 2). Nectar is the easiest food to digest, and the digestive tract of nectarivores are very simple, almost a straight tube. Foods of animal origin, such as vertebrates, insects, and mollusks can be almost completely digested if sufficient amounts of time and enzymes are invested. Faunivorous species usually have a large proventriculus and gizzard to accommodate digestion of the high level of protein and fat in these foods. Seeds are also highly digestible, and granivores possess large gizzards for mechanically reducing their structure. Fruits contain relatively high amounts of fiber that cannot be digested autoenzymatically. Most frugivorous species autoenzymatically digest simple sugars and proteins, but digestion of the fiber-containing components of the pulp is often completely lacking. Frugivores compensate for the nutrient-dilute composition of fruits by consuming large amounts and moving them through the digestive tract quickly [44, 45]. This skimming strategy also precludes the digestion of seeds in the fruit. Consequently, the droppings of frugivores are voluminous relative to the droppings of faunivores or granivores, and the retention time of food in the digestive tract is short (Table 2). Nectarivores, faunivores, frugivores, and granivores usually lack ceca, or when present, they are involved in water and nitrogen balance but not fiber digestion [46]. Many species possess enlarged ceca that house microorganisms that aid in the digestion of fibrous components of their food (strategy 2, Figure 2). Not all of the undigested components of food that leaves the ileum move into the ceca. This is particularly well studied in poultry and domestic ducks, in which the anatomy of their ileal-cecal-rectal junction permits sieving of digesta so that only small particulates and water soluble compounds enter the ceca [47, 48, 49]. Digesta that enter the ceca are retained and sub-
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ence of wildlife agencies demonstrates that the nutritional biology of each subspecies determines its suitability for reintroduction into different habitats [43]. The fact that the Rio Grande and Gould’s subspecies have been unable to occupy the former range of the southern Mexican subspecies suggests that their nutritional biology differs.
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jected to microbial fermentation, whereas the digesta that are excluded quickly pass through the rectum and are defecated (rectal feces). The composition of the feces that arises from the ceca (cecal feces) is very different from that of the rectal feces. Cecal feces are enriched in bacteria and have higher levels of protein, fat, and vitamins [13, 48]. Consequently, the cecal feces may be consumed in some species, including chickens and turkeys (strategy 3, Figure 2). Rectal feces, which are excreted frequently throughout the day, often have green-colored streaks when fresh due to the presence of unmetabolized biliverdin. Cecal feces are excreted less frequently (once or twice a day) and microbial metabolism of biliverdin likely eliminates its green color, resulting in light brown to black coloration. Cecal feces are high in ammonia, putrefactive products from microbial metabolism, volatile fatty acids, and hydrophilic dietary fibers that impart a uniform viscous tex-
ture and a distinctive odor [50, 51]. Most omnivores switch between strategies as the availability of food items change. When readily digestible foods are available, they use strategy 1, but when high-fiber plant materials are consumed, strategies 2 or 3 may be used. Consequently, the amount and composition of feces, the rate of passage, and likelihood of coprophagy are dependent on the foods. Terrestrial herbivores, such as tinamou, are not constrained by weight limitations of acrobatic flight and have adapted a different digestive strategy than birds that are adept at flying. They have very large and highly sacculated ceca that allow the retention and fermentation of fiber for long periods of time. Ostriches are among the most efficient birds at utilizing dietary fiber [52, 53]. Their rectum is by far the longest of any bird and accounts for 52% of the length of the gastrointestinal tract. Dietary fiber digestibility in the ostrich
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FIGURE 2. Birds that eat other animals, nectar, grains, and fruits (strategy 1) have guts that lack voluminous ceca that are used for fermentation by herbivores, graminivores, and omnivores (strategies 2 to 4). Strategy 4 is common in mammalian herbivores and folivores but is almost completely absent in birds.
50–300 300–1440 Highly variable
1 1
1
1
2, 3, or 4 2 or 4 1, 2, or 3
Piscivores Insectivores
Granivores
Frugivores Herbivores Flying Terrestrial Omnivores
2
40–100
360–780 30–90
360–600
Very high Very high Highly variable
Very low
Very low
Very low, unless ceca are present Very low
Very low, unless ceca are present
Very low
Microbial activity
Ability to sort fermental fibers into ceca2 Massive ceca Combinations of the above Possess versatile ceca
Ability to process large quantities of water Minimize maintenance requirement for amino acids Ability to eruct fur, feathers, scales, and bones Ability to metabolize large amounts of protein and fat2 Same as above Ability to eruct exoskeletons Produce enzymes with chitenase activity2 Large muscular gizzard2 Lack ceca and alloenzymatic digestion Ability to skim readily available nutrients and excrete fiber without fermenting
Important attributes
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From Klasing [1]. Also used by chickens and turkeys.
1
15–60
1
Carnivores
30–50
1
Nectarivores
Retention time (min)
Nutritional strategy
Consumption category
TABLE 2. Overview of nutritional strategies of birds that consume diverse types of foods1
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size of the gastrointestinal tract, especially the gizzard and the ceca, and its capacity to ferment dietary fiber change throughout the season in conjunction with the quantity and quality of food consumed [13, 62, 63, 64]. For example, in wild turkeys, gizzard and cecal sizes are smallest in the summer, when the birds feed on tender shoots of newly growing herbaceous plants [38]. The gizzard is largest and most muscular, and the ceca are longest and yield the most volatile fatty acids in the winter, when birds feed primarily on woody stems, buds, and leaves. The time required for adaptive hypertrophy appears to be about 2 to 3 mo. The ceca of birds can have many functions, including absorption of water and other nutrients, conservation or detoxification of nitrogen, and fermentation. In chickens, the ceca can be used for any of these purposes, depending upon the diet. The extreme of the metabolic flexibility of chickens is illustrated by their ability to thrive on a 100% meat diet [61]. In other words, they can live the life of a carnivore. Chickens and turkeys can also adopt a pseudoskimming strategy and, at least as adults, maintain on a diet of poorquality herbaceous foods. Modern production practices illustrate that they can also live the life of a granivore, eating virtually only the seeds of corn and soya. The field of nutrition is referred to as a mature field. The glory days of nutrition occurred in the first half of the 20th century and few Nobel Prizeworthy discoveries in the field have occurred in the past 75 yr. These seminal discoveries allowed the previous generation of poultry nutritionists to make rapid progress. Current progress in poultry nutrition is incremental but slow. We could blame this on the lack of new breakthroughs in basic nutrition, but it might also be blamed on our lack of imagination. What future developments will catalyze progress in applied poultry nutrition? The nexus of comparative genomics with comparative nutrition is likely to be fertile ground for future advancements.
CONCLUSIONS AND APPLICATIONS 1. Turkeys and, especially, jungle fowl are omnivores. They are not granivores and do not consume diets that of predominantly grains in their wild environments. 2. The hallmark of omnivores is their morphologic and metabolic flexibility, which is considerably more robust than specialists, like granivores and faunivores.
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approaches that in the horse (cell walls, 47%; hemicellulose, 66%; and cellulose, 38%). Flying herbivores, like Galliformes and Anseriformes (ducks and geese), have limits to which they can utilize dietary fiber, and in some circumstances, a strategy is adopted in which fiber is largely ignored instead of fermented [54, 55]. For example, blue grouse eat conifer needles in the winter and ferment very little of the fiber in their ceca. However, they autoenzymatically digest relatively efficiently nonfiber carbohydrate and protein. High rates of consumption compensate for the low level of autoenzymatically digestible nutrients in their food. Many herbivores can switch between this low-efficiency skimming strategy and a higher-efficiency ceca fermentation strategy, depending on the fiber content of their diet or the quantity of diet available. In fact, geese in the arctic summer can space their feeding bouts over a 24-h period and adopt a strategy of a slow rate of passage and high fermentation. Later in the year, when the days are short and the quality of the grass is poor, their rate of passage increases, and this is accompanied by a marked reduction in the efficiency of fiber digestion. In birds adapted to a high-fiber diet, a skimming strategy markedly lowers the weight of digesta in the gastrointestinal tract and aids flight. The amount of feces is voluminous: geese feeding on grass defecate every 3 to 5 min, with each dropping averaging 5.5 cm in length [56]. A few species have an area for microbial fermentation in their crop, esophagus, and anterior proventriculus (strategy 4, Figure 2). This is taken to the extreme in the hoatzin [57, 58] but also occurs in mousebirds and kakapo. The digestive tract posterior to this fermentation area is relatively simple and resembles that of omnivores. The hallmark of omnivores is their morphologic and metabolic flexibility, which is considerably more robust than specialists, like granivores and faunivores [59, 60, 61]. In many species of Galliformes, including chickens and turkeys, the
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3. Understanding the digestive and metabolic adaptations of birds that are specialists at consuming insects, foliage, grains, and fruits will greatly enhance our understanding of poultry nutrition. 4. Current progress in poultry nutrition is slow relative to the glory days of the early 20th century. Imaginative applications of comparative genomics and comparative nutrition are likely to be fertile ground for renewed advancement.
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20. Collias, N. E., and P. Saichuae. 1967. Ecology of the Red Jungle Fowl in Thailand and Malaya with reference to the origin of domestication. Nat. Hist. Bull. Siam 22:189–209.
3. Fumihito, A., T. Miyake, M. Takada, R. Shingu, T. Endo, T. Gojobori, N. Kondo, and S. Ohno. 1996. Monophyletic origin and unique dispersal patterns of domestic fowls. Proc. Natl. Acad. Sci. 93:6792–6795. 4. Moiseyeva, I. G., M. N. Romanov, A. A. Nikiforov, A. A. Sevastyanova, and S. K. Semyenova. 2003. Evolutionary relationships of Red Jungle Fowl and chicken breeds. Genet. Sel. Evol. 35:403–423. 5. Ohta, N., M. Kajita, S. Kusuhara, and R. Kakizawa. 2000. Genetic differentiation and phylogenetic relationships among species of Gallus (Jungle Fowl) and the chicken. Jpn. Poult. Sci. 37:33–39. 6. Hillel, J., M. A. M. Groenen, M. Tixier-Boichard, A. B. Korol, L. David, V. M. Kirzhner, T. Burke, A. Barre-Dirie, R. P. M. A. Crooijmans, K. Elo, M. W. Feldman, P. J. Freidlin, A. Maki-Tanila, M. Oortwijn, P. Thomson, A. Vignal, K. Wimmers, and S. Weigend. 2003. Biodiversity of 52 chicken populations assessed by microsatellite typing of DNA pools. Genet. Sel. Evol. 35:533–557.
21. Bump, G., and W. H. Bohl. 1961. Red Junglefowl and Kaliji Pheasants. US Fish and Wildlife Service Fish and Wildlife Research Service, Washington, DC. 22. Holdsworth, R. L. 1958. Note on junglefowl shooting. Wild Life Preservation Society of India, Dehradun, UP, India. 23. Johnson, R. A. 1963. Habitat preference and behavior of breeding jungle fowl in central western Thailand. Wilson Bull. 75:270–272. 24. Schutz, K., S. Kerje, O. Carlborg, L. Jacobsson, L. Andersson, and P. Jensen. 2002. QTL analysis of a Red Jungle Fowl × White Leghorn intercross reveals trade-off in resource allocation between behavior and production traits. Behav. Genet. 32:423–433. 25. Andersson, M., E. Nordin, and P. Jensen. 2001. Domestication effects on foraging strategies in fowl. Appl. Anim. Behav. Sci. 72:51–62.
7. Bush, K. L., and C. Strobeck. 2003. Phylogenetic relationships of the Phasianidae reveals possible non-pheasant taxa. J. Hered. 94:472–489.
26. Dawkins, M. S. 1989. Time budgets in red junglefowl as a baseline for the assessment of welfare in domestic fowl. Appl. Anim. Behav. Sci. 24:77–80.
8. Mock, K. E., T. C. Theimer, O. E. Rhodes, Jr., D. L. Greenberg, and P. Keim. 2002. Genetic variation across the historical range of the wild turkey (Meleagris gallopavo). Mol. Ecol. 11:643–657.
27. H. S. Iman Rahayu, A. R. Alimon, M. K. Vidyadaran, and S. A. Babjee. 2001. Responses of choice-fed red jungle fowl and commercial broiler chickens offered a complete diet, corn and soybean. Asian-australas. J. Anim. Sci. 14:1758–1762.
9. Schorger, A. W. 1966. The Wild Turkey: Its History and Domestication. University of Oklahoma Press, Norman, OK. 10. Dimcheff, D. E., S. V. Drovetski, and D. P. Mindell. 2002. Phylogeny of Tetraoninae and other galliform birds using mitochondrial 12S and ND2 genes. Mol. Phylogenet. Evol. 24:203–215. 11. Dudley, R., and G. J. Vermeij. 1991. Do the power requirements of flapping flight constrain folivory in flying animals? Funct. Ecol. 6:101–104. 12. Cork, S. J. 1994. Digestive constraints on dietary scope in small and moderately-small mammals: How much do we really understand? Pages 324–336 in The Digestive System in Mammals: Food, Form and Function. D. J. Chivers and P. Langer, ed. Cambridge University Press, Cambridge. 13. Gasaway, W. C. 1976. Seasonal variation in diet, volatile fatty acid production and size of the cecum of rock ptarmigan. Comp. Biochem. Physiol. 53A:109–114. 14. Levey, D. J., and W. H. Karasov. 1989. Digestive responses of temperate birds switched to fruit or insect diets. Auk. 106:675–686.
28. Savory, C. J., D. G. M. Wood-Gush, and I. J. H. Duncan. 1978. Feeding behaviour in a population of domestic fowls in the wild. Appl. Anim. Behav. Sci. 4:13–27. 29. Gamberale-Stille, G. and B. S. Tullberg. 2001. Fruit or aposematic insect? Context-dependent colour preferences in domestic chicks. Proc. R. Soc. Lond. B Biol. Sci. 268:2525–2529. 30. Darwin, C. 1859. On the Origin of Species. J. Murray, London. 31. West, B. and B.-X. Zhou. 1989. Did chickens go north? New evidence for domestication. Worlds Poul. Sci. J. 45:205–208. 32. Wood-Gush, D. G. 1959. A history of the domestic chicken from antiquity to the 19th century. Poult. Sci. 38:321–326. 33. Armsby, H. P. 1908. The Principles of Animal Nutrition. J. Wiley and Sons, New York. 34. Jackson, S., and J. Diamond. 1996. Metabolic and digestive responses to artificial selection in chickens. Evolution 50:1638–1650.
15. Karasov, W. H. 1990. Digestion in birds: Chemical and physiological determinants and ecological implications. Stud. Avian Biol. 13:391–415.
35. Jackson, S., and J. Diamond. 1995. Ontogenetic development of gut function, growth, and metabolism in a wild bird, the Red Jungle Fowl. Am. J. Physiol. 269:R1163–R1173.
16. Afik, D., and W. H. Karasov. 1995. The trade-offs between digestion rate and efficiency in warblers and their ecological implications. Ecology 76:2247–2257.
36. Leopold, A. 1959. Wildlife of Mexico, The Game Birds and Mammals. University of California Press, Berkeley, CA.
17. Beebe, W. 1990. A Monograph of the Pheasants. Dover Publications, New York. 18. Wells, D. R. 1999. The Birds of the Thai-Malay Peninsula. Vol. 1. Non-Passerines. Academic Press, San Diego, CA.
37. Leopold, A. 1948. The wild turkeys of Mexico. N. Am. Wildl. Conf. 13:393–400. 38. Korschgen, L. J. 1967. Feeding habits and foods. Pages 123– 179 in The Wild Turkey. O. H. Hewitt, ed. The Wildlife Society, Washington DC.
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REFERENCES AND NOTES
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436 39. Mosby, H. S., and C. O. Handly. 1943. The wild turkey in Virginia: Its status, life history and management. VA Comm. Game and Inland Fisheries, Richmond, VA. 40. Leopold, A. 1933. Game Management. Scribner, New York. 41. Rumble, M. A., and S. H. Anderson. 1996. Feeding ecology of Merriam’s turkeys (Meleagris gallopavo merriami) in the Black Hills, South Dakota. Am. Midl. Nat. 136:157–171.
43. Lindzey, J. S. 1967. Highlights of management. Pages 219– 253 in The Wild Turkey. O. H. Hewitt, ed. The Wildlife Society, Washington DC. 44. Martinez del Rio, C. M., and W. H. Karasov. 1990. Digestion strategies in nectar-eating and fruit-eating birds and the sugar composition of plant rewards. Am. Nat. 136:618–637. 45. Levey, D. J., and W. H. Karasov. 1992. Digestive modulation in a seasonal frugivore, the American Robin (Turdus-Migratorius). Am. J. Physiol. 262:G711–G718. 46. Clench, M. H., and J. R. Mathias. 1995. The avian cecum— a review. Wilson Bull. 107:93–121. 47. Duke, G. E. 1982. Gastrointestinal motility and its regulation. Poult. Sci. 61:1245–1256. 48. Bjornhag, G. 1989. Transport of water and food particles through the avian ceca and colon. J. Exp. Zool. 3:32–37. 49. Mahdi, A. H., and J. McLelland. 1988. The arrangement of the muscle at the ileo-caeco-rectal junction of the domestic duck (Anas platyrhynchos) and the presence of anatomical sphincters. J. Anat. 161:133–142.
54. Remmington, T. E. 1989. Why do grouse have ceca? A test of the fiber digestion theory. J. Exp. Zool. 3:87–94. 55. Moss, R. 1989. Gut size and the digestion of fibrous diets by Tetraonid birds. J. Exp. Zool. 3:61–65. 56. Prop, J., and T. Vulink. 1992. Digestion by barnacle geese in the annual cycle—the interplay between retention time and food quality. Funct. Ecol. 6:180–189. 57. Grajal, A., S. D. Strahl, R. Parra, M. G. Dominguez, and A. Neher. 1989. Foregut fermentation in the hoatzin, a neotropical leafeating bird. Science 245:1236–1238. 58. Dominguez-Bello, M. G., M. Lovera, P. Suarez, and F. Michelangeli. 1993. Microbial digestive symbionts of the crop of the Hoatzin: An avian foregut fermenter. Physiol. Zool. 66:374–383. 59. Koutsos, E. A., L. A. Tell, L. W. Woods, and K. C. Klasing. 2003. Adult cockatiels (Nymphicus hollandicus) at maintenance are more sensitive to diets containing excess vitamin A than to vitamin A-deficient diets. J. Nutr. 133:1898–1902. 60. Koutsos, E. A., J. Smith, L. W. Woods, and K. C. Klasing. 2001. Adult cockatiels (Nymphicus hollandicus) metabolically adapt to high protein diets. J. Nutr. 131:2014–2020. 61. Myers, M. R., and K. C. Klasing. 1999. Low glucokinase activity and high rates of gluconeogenesis contribute to hyperglycemia in barn owls (Tyto alba) after a glucose challenge. J. Nutr. 129:1896–1904. 62. Redig, P. T. 1989. The avian ceca—obligate combustion chambers or facultative afterburners—the conditioning influence of diet. J. Exp. Zool. 3:66–69.
50. Zubair, A. K., C. W. Forsberg, and S. Leeson. 1996. Effect of dietary fat, fiber, and monensin on cecal activity in turkeys. Poult. Sci. 75:891–899.
63. Starck, J. M., and G. H. Rahmaan. 2003. Phenotypic flexibility of structure and function of the digestive system of Japanese quail. J. Exp. Biol. 206:1887–1897.
51. Terada, A., H. Hara, J. Sakamoto, N. Sato, S. Takagi, T. Mitsuoka, R. Mino, K. Hara, I. Fujimori, and T. Yamada. 1994. Effects of dietary supplementation with lactosucrose (4G-beta-D-galactosylsucrose) on cecal flora, cecal metabolites, and performance in broiler chickens. Poult. Sci. 73:1663–1672.
64. Starck, J. M. 1999. Phenotypic flexibility of the avian gizzard: Rapid, reversible and repeated changes of organ size in response to changes in dietary fibre content. J. Exp. Biol. 202:3171–3179.
52. Swart, D., F. K. Siebrits, and J. P. Hayes. 1993. Utilization of metabolizable energy by ostrich (Struthio-Camelus) chicks at 2 different concentrations of dietary energy and crude fibre originating from lucerne. S-Afr. Tydskr Veekd. 23:136–141. 53. Swart, D., R. I. Mackie, and J. P. Hayes. 1993. Fermentative digestion in the ostrich (Struthio-Camelus Var Domesticus), a large
Acknowledgments I thank Mamduh Sifri for tirelessly keeping the informative nutrition conference rolling, enthusiastically keeping it relevant, and providing me with a well-placed kick to catalyze the writing of this paper. An National Science Foundation Award (IBN-0212587) provided funding for comparative investigations of avian physiology.
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42. York, D. L., and S. D. Schemnitz. 2003. Home range, habitat use, and diet of Gould’s Turkeys, Peloncillo Mountains, New Mexico. Southwest. Nat. 48:231–240.
avian species that utilizes cellulose. SS-Afr. Tydskr Veekd. 23:127– 135.
Poultry Nutrition: A Comparative Approach Department of Animal Science, University of California, Davis, California 95616
Primary Audience: Poultry Nutritionists SUMMARY Although a variety of scholarly papers and books classify chickens and turkeys as granivores, they are omnivores and do not have the food preferences, digestive anatomy, or nutritional strategies that would classify them as granivores. Their wild relatives consume a very wide variety of food items of both plant and animal origin, and seeds are not often a primary component. Intake of insects by jungle fowl chicks and wild turkey poults exceeds 50% of their diet, and adult females increase their intake of insects at the time of reproduction. In the case of jungle fowl, termites and bamboo mast are preferred foods in the area of Southeast Asia where domestication likely occurred. The nutritional strategy of omnivores is a composite of that of faunivores, frugivores, granivores, and herbivores. Appreciating the nutritional strategy of birds that eat diverse types of foods illuminates the potential capabilities and limitations of generalists, like chickens and turkeys. The marriage of comparative genomics with comparative nutrition is likely to be fertile ground for future advancements in applied poultry nutrition. Key words: nutritional strategy, omnivore, Galliformes 2005 J. Appl. Poult. Res. 14:426–436
DESCRIPTION OF PROBLEM The dietary preferences, gastrointestinal anatomy, digestive physiology, biochemical capabilities, and commensal microflora of a bird are collectively known as its nutritional strategy. Nutritional strategies of birds are diverse and permit specialization on foods ranging from nectar to grass to other vertebrates. The specific gastrointestinal anatomy, digestive physiology, and metabolic capabilities of each species have coevolved with the types of foods consumed, so species eating similar food types often have similar nutritional strategies [1, 2]. Poultry nutritionists should have an understanding of the diverse nutritional strategies among birds because it provides an appreciation for the capabilities, limitations, and po1
tentials of chickens and turkeys. The National Institutes of Health, which is devoted to human biology, had the wisdom to fund the sequencing of the avian genome because the comparative approach to biology reveals many secrets that would otherwise not even be known to exist. In a similar manner, the comparative approach to nutrition, including using chicks, rats, and pigs as models, has revealed much about optimum nutrition for humans. A comparative approach to poultry nutrition is likely to have similar benefits. Such a comparative approach requires looking outward from poultry into the diverse avian taxa. The purpose of this paper is to provide an overview of the nutritional strategies of birds and to describe the place of chickens and turkeys in this bigger picture. In order to accomplish this,
To whom correspondence should be addressed: [email protected].
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to the Americas, probably sometime around A.D. 500. Two other subspecies remain in Mexico, Rio Grande (M. g. intermedia) and Gould’s (M. g. mexicana) and are likely to be very closely related to M. g. gallopavo. The Ocellated Turkey (Meleagris ocellata) is in the same family as wild turkeys and is found only in eastern central Mexico; more distantly related is the grey partridge (Purdix purdix) [10].
Phylogeny
Dietary Preferences of Birds
Chickens, turkeys, and quail are Galliformes, which is a large order containing more than 200 species, including all of the pheasants, grouse, quail, turkeys, guinea fowl, and partridges. The 200 plus species in this order are all omnivores. Based on morphologic, behavioral, and genetic evidence, the domesticated chickens descend from a single ancestor, the Red Jungle Fowl (Gallus gallus), originating in Southeast Asia, most likely Thailand [3, 4, 5]. The 5 subspecies of Red Jungle Fowl are differentiated by color and subtle differences in morphology. Mitochondrial DNA [3] and microsatellite markers [6] suggest that Gallus gallus gallus was likely the primary ancestor to the diverse breeds of the domesticated chicken (Gallus gallus domesticus); although a contribution by other subspecies, such as G. gallus spadiceus, has not been excluded. Based on cytochrome C gene homology, Gallus appears to be basal to pheasants [7]. The species most closely related to G. gallus are G. varius, G. Lafayettei, and G. sonneratii. More distantly related are peacock-pheasants (Polyplectron) of Southeast Asia, koklass (Pucrasia) of Asia, and chachalaca (Ortalis) of Latin America. Domestic turkeys were domesticated from wild turkeys (Meleagris gallopavo). The wild turkey is indigenous to North America and had an historical range that included much of the eastern and portions of the southwestern US, northern Mexico, and southeastern Canada. Six geographically isolated subspecies are recognized [8]. Spaniards brought back to Europe the southern Mexican subspecies, Meleagris gallopavo gallopavo [9] This subspecies is the ancestor to the modern domestic turkey, not the familiar Eastern Turkey of the US (M. g. sylvestris). The M. g. gallopavo now appears to be extinct in the wild, but its genes are preserved in the domestic turkey. Domestication occurred before Europeans arrived
Across the >9,000 species of birds, there is an almost continuous distribution of dietary preferences (Table 1) and nutritional strategies [1, 2]. The largest numbers of species use their power of flight to select food items with the highest concentration of digestible nutrients and to avoid food items high in roughage (Figure 1). The most nutritious foods are other animals, seeds, fruit, and nectar. The large number of insectivorous, frugivorous, and granivorous avian species account for the fact that there are more than twice as many avian species as mammalian species. The advantage afforded by flight also comes with evolutionary pressure to keep the size of the digestive tract and the weight of its contents to a minimum. These 2 factors make it impractical for flying birds to weigh more than 12 kg. Studies of mammalian herbivores suggest that the size of a digestive tract large enough to digest leaves requires the owner to have a body of at least 15 kg [11, 12]. These constraints prevent flying birds from occupying the niche filled by mammalian bulk-roughage feeders (e.g., cattle, deer, sheep). Thus, the capacity of flight that makes ubiquitous vegetation readily obtainable restricts its digestion. Herbivorous birds capable of flight must always be highly selective and consume plant parts that are relatively high in protein and low in fiber, such as rhizomes, buds, flowers, catkins, very young leaves, and young grasses. Mature leaves, stems, and grass are not selected. Many species are omnivores and consume a wide variety of foods of plant and animal origins. In the wild, their exact choice is determined by a combination of factors, including seasonal availability of food, foraging efficiency, changing nutrient requirements, palatability, and predator patterns. The types of foods consumed by a species can have considerable seasonal variability, espe-
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the phylogenetic position of chickens and turkeys is provided in reference to other species, the dietary preferences of jungle fowl and wild turkeys is detailed in the context of other avian species, and the nutritional strategy of chickens and turkeys is compared with that of others. A second goal is to exemplify ways that the nutritional strategies of birds diverge from that of mammals and to provide rationale, where possible.
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428 TABLE 1. Classification of dietary preferences of birds Category
Chickens, turkeys, some ducks (including domestics), quail, pheasants, grouse, cranes, bustards, crows
Hawks, owls, eagles, falcons, vultures Loons, pelicans, storks, cormorants, mergansers, osprey, kingfishers Woodpeckers, swallows, wrens, flycatchers
Ostriches, some ducks, tinamou Hoatzin Geese, swans Sparrows, finches, some pigeons, some parrots Hummingbirds, sunbirds, lorikeets, honeyeaters Toucans, manikins, tanagers, some pigeons, bulbuls
cially in temperate climates, and the nutritional strategy adjusts accordingly. For example, the mixture of foods consumed by many omnivores is often higher in insects in the summer and higher in foods of plant origin in the winter. Among Galliformes, the winter shift to high fiber foods is matched by increased cecal size, microbial fermentation, and retention time of the digesta [13]. Some species, especially many songbirds, make even more extreme annual shifts. A common dietary pattern is a diet of insects during the summer and a complete switch to fruits during the winter. The change in nutritional strategies, following such switches, can be dramatic [14, 15, 16]. Dietary Preferences of Jungle Fowl Jungle fowl are not granivores. As their name suggests, Red Jungle Fowl are birds of tropical and subtropical forests, not grasslands where seeds and grains would be available. In undisturbed habitats of Southeast Asia, the Red Jungle Fowl prefers to live in bamboo forests [17, 18]. In areas of human habitation and agriculture, jungle fowl prefer the remaining forested areas and forest edges, especially those with an understory with tall herbaceous shrubs [19]. In Southeast Asia and in India, Red Jungle Fowl are most likely to be found in areas with abundant termite populations. All 5 of the jungle fowl species are classified as highly omnivorous, eating a very wide variety of food items of plant and animal origin throughout the year, and seeds are often only a minor component.
A proper quantitative study of the food preferences of jungle fowl in their native habitat has not been conducted. However, field accounts and inspections of crops from birds killed by hunters provide a good picture [17, 19, 20, 21, 22, 23]. Foods of plant origin that are frequently consumed include fruits and berries from trees and herbaceous shrubs, seeds from a variety of plants especially bamboo seeds when available, nuts, young shoots of bamboo and other grasses, leaves, petals, and tubers. When near villages and agriculture, they eat readily available rice, millet, and vetches, but they are not reported to especially pursue these foods. Foods of animal origin that are frequently consumed are termites and their eggs and pupae, winged ants and their eggs and pupae, earthworms, roaches, grasshoppers, spiders, moths and their caterpillars, beetles and their grubs, small crabs, snails, centipedes, and lizards. Invertebrates are obtained by scratching at leaf litter in the forest. Insect communities in elephant droppings may be an important food source in many locations [19]. In adults, foods of plant origin are present in quantitatively greater amounts than those of animal origin, and at many times of the year, fruits are dominant. However, in most of the range of the Red Jungle Fowl, termites and their eggs and pupae appear to be the preferred food and are the most likely food item to be found in the crops of birds, where they are sometimes found in the hundreds [17, 21]. Birds consume adults leaving mounds, but they also scratch mounds to
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Generalist feeder Omnivores Animal matter Faunivores Carnivores Piscivores Insectivores Plant matter Florivores Herbivores Folivores Graminivores Granivores Nectarivores Frugivores
Examples
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expose nurseries. Apparently, the preference for termites is not unique to jungle fowl but is common among most of the pheasant species of Southeast Asia. Foods of animal origin are dominant in the diet of chicks. Again, termites and their eggs and pupae are often the principal type [17, 21]. In one study, the breeding season was matched to the annual cycle of termite availability [19]. Jungle fowl, like most omnivores, are generalists and consume foods on an opportunistic basis and appear to conform to theories on optimal resource allocation [24] and optimal foraging strategies [25]. Red Jungle Fowl spend 90% of the active part of their day in activities associated with foraging for food, especially pecking and scratching at the ground [26]. Young Red Jungle Fowl chicks are able to select among foods to meet their protein requirement [27]. Hatchling chicks in wild populations of partly domesticated chickens choose a diet that is about 60% vertebrates [28]. The innate preferences of domestic chicks for specific colors and sizes of food items and the dependency of this preference on whether the food is perceived to be a fruit or an insect
are likely to be a holdover of foraging strategies of wild jungle fowl [29]. Red Jungle Fowl × White Leghorn crosses have revealed interesting genetic associations with feeding behavior [24], and the quantitative trait loci approach allows mapping specific behaviors to chromosome locations and eventually should permit the identification of sets of genes that control feeding behaviors. Changes in wild populations during domestication illustrate the effects of genetic selection in such a clear way that Darwin [30] devoted the first chapter of his classic book, The Origin of Species, to this topic. Jungle fowl have been kept by humans for about 8,000 yr [31], but during most of this time, selection was for fighting and religious purposes, and selection for agricultural traits was minimal [32]. The idea of selective breeding for productivity (body size or egg production) likely started with the Romans before the time of Aristotle (384 to 322 B.C.), but it was not sustained and appears to have died out, only to be revitalized a few 100 yr ago. An appreciation for the efficiency of feed utilization occurred only about 100 yr ago [33]. The progress in selecting
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FIGURE 1. Proportions of avian and mammalian families feeding on different food categories.
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Dietary Preferences of Turkeys Because the wild turkey is a very important game species that is heavily managed by state and federal agencies, its feeding habits and natural foods have been very well studied. The goal of this extensive literature is to maximize turkey habitat, reproduction, and harvest. Unfortunately, the natural history of the Mexican subspecies M. g. gallopavo, which is the direct ancestor of domestic turkeys, is unknown because it now is apparently extinct. Several excellent reviews on the nutritional biology of M. g. silverstris, M. g. intergrade, and M. g. Merriam found in the US are available [9, 36, 37, 38]. All good turkey hunters know the food and the feeding behavior of wild turkeys, and their wisdom can be readily consulted in a plethora of hunting magazines. Throughout most of their historical range, turkeys live in forested areas and depend heavily on foods produced by the trees [38]. Since the introduction of agriculture, turkeys have increased their consumption of grains, but turkeys are not granivores. Even when plentiful, grains, such as corn, oats, milo, and barley, are not typically a major part of their diet unless their natural foods become unavailable because of drought, snowfall, overpopulation, or loss of habitat due to clearing. Wild turkeys consume a diverse mixture of foods of animal origin and those of plant origin, making them omnivores. The contents of 524 turkey crops and gizzards from Virginia included more than 350 plant species and 300 invertebrate species [39]. Feeding methods include whole ingestion, picking, stripping, clipping, and scratching [38, 39]. Acorns, corn, beechnuts, and other seeds are consumed whole without shelling. Most insects are also consumed whole, although walking sticks and grasshoppers may be battered about to reduce their size before swallowing. Small seeds, such as those from grasses and sedges and the fruiting heads of buttercups and violets, are stripped by
a forceps-like action of the beak. Picking and clipping are used to obtain buds, fruits, and vegetive parts of plants, such as young grass and fern fronds. Scratching is done to locate invertebrates, mast (acorns, beech nuts, pine seeds), fruits, and tubers in the leaf litter of the forest floor. Scratching by turkeys in the leaf litter is methodical and stereotyped leaving a V-shaped scratch. Wild turkeys forage throughout the day, but most feeding activity occurs during the first 2 to 3 h after leaving the roost at daybreak and 2 to 3 h before sunset. Aldo Leopold [40] described why turkeys choose specific food items and provided observations and citations to support his conclusions. Though considerable additional work has been done, Leopold’s work demonstrates that theories on optimal foraging and resource allocation are applicable to turkeys. Wild turkey diets are composed mostly of plants. Depending on the subspecies, location, and season, the percentage of the diet of adult turkeys consisting of animals ranges from 5 to 40%. Of the animals consumed, insects usually predominate, especially grasshoppers, crickets, beetles, ants, ticks, and fly larvae. Spiders, millipedes, snails, salamanders, frogs, toads, lizards, snakes, fiddler crabs, and other small invertebrates are also consumed when encountered [9, 39]. Insects are of critical importance to poults, and survival is low in habitats that do not support large insect populations. The intake of insects by young poults has been estimated to be about 60% of the diet and decreases with age [38, 41]. As stated above, the nutritional biology of the southern Mexican (M. g. gallopavo) subspecies that is the direct ancestor of the domestic turkey is unknown; however, the habitat of east-central Mexico, where it was indigenous, is tropical deciduous forests and mountain pine forests. Acorns would not likely have been a part of their diet in much of their range. The 2 other Mexican subspecies, Rio Grande (M. g. intermedia) and Gould’s (M. g. mexicana), differ from the North American subspecies by eating a greater proportion of insects throughout the year, due to their greater availability, and also consuming fruits of wild tomatoes, junipers, and manzanitas and the seeds of cacti, figs, capulin, acacia, palms, and palmettos [36, 42]. Subspecies of wild turkeys differ in terms of range, appearance, behavior, physiology, and genetic characteristics. Experi-
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for efficiency was rapid, and in the mid-1990s, a 4-wk-old broiler was more than twice as efficient as a jungle fowl of the same age [34, 35]. The basis for this increased efficiency is not due to better digestive efficiency or lower metabolic rate but due to a high rate of food intake and growth rate. This is facilitated by much larger relative intestinal mass, especially the ileum.
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Strategies and Adaptations Poultry are omnivores, and the anatomy and function of their digestive tracts are a composite of all of the specialist species, including faunivores, granivores, and herbivores. Consequently, it is important to have an appreciation for the diversity of digestive strategies and adaptations found in birds that specialize on diverse food items. Distantly related birds eating similar diets often have very similar nutritional strategies and can extract similar nutritional value from their diet [1, 15]. At the morphological level, all birds have their digestive tracts built out of the same units in the same order but with wide variations in design, depending upon the type of diet typically consumed. The avian digestive tract has a greater number of organs than their mammalian counterparts, and there is greater interorgan cooperation. Storage, enzymatic digestion, and mechanical digestion are divided among the crop, proventriculus, and gizzard, respectively. Except for ostriches, the large intestine of birds is considerably smaller than the small intestine. Consequently, the intestine distal to the ileum is usually referred to as the rectum and not the large intestine. When ceca are present, they are paired, whereas mammals have a single cecum. Digestive morphology is extremely variable among species and ranges from very simple, almost tube-like tracts of frugivores and nectarivores to very complex highly convoluted tracts of herbivores. Herbivorous species require symbiotic microflora to aid in digestion (alloenzymatic digestion) and have tracts with large ceca. More subtle functional adaptations are required to accommodate the physical and nutritional characteristics of the food. Adaptation found in various birds include 1) the capacity to egest the exoskeleton of arthropods, the bones of vertebrate prey, or seeds of fruits; 2) the ability to concentrate dietary lipids in the proventriculus; 3) the capacity to sort cell wall components so that only fermentable components enter the ceca and the refractory components move on to the
cloaca; 4) the consumption of feces originating from the ceca in order to obtain microbial protein, energy, and vitamins; 5) and the ability to modulate the rate of passage of digesta to match the type of feedstuff consumed. Poultry utilize strategies 3 to 5 but not the first 2. Figure 2 summarizes 4 typical nutritional strategies. The majority of avian species use their capacity of flight to procure the most nutritious and digestible food items and rely exclusively on autoenzymatic digestion (strategy 1, Figure 2). Nectar is the easiest food to digest, and the digestive tract of nectarivores are very simple, almost a straight tube. Foods of animal origin, such as vertebrates, insects, and mollusks can be almost completely digested if sufficient amounts of time and enzymes are invested. Faunivorous species usually have a large proventriculus and gizzard to accommodate digestion of the high level of protein and fat in these foods. Seeds are also highly digestible, and granivores possess large gizzards for mechanically reducing their structure. Fruits contain relatively high amounts of fiber that cannot be digested autoenzymatically. Most frugivorous species autoenzymatically digest simple sugars and proteins, but digestion of the fiber-containing components of the pulp is often completely lacking. Frugivores compensate for the nutrient-dilute composition of fruits by consuming large amounts and moving them through the digestive tract quickly [44, 45]. This skimming strategy also precludes the digestion of seeds in the fruit. Consequently, the droppings of frugivores are voluminous relative to the droppings of faunivores or granivores, and the retention time of food in the digestive tract is short (Table 2). Nectarivores, faunivores, frugivores, and granivores usually lack ceca, or when present, they are involved in water and nitrogen balance but not fiber digestion [46]. Many species possess enlarged ceca that house microorganisms that aid in the digestion of fibrous components of their food (strategy 2, Figure 2). Not all of the undigested components of food that leaves the ileum move into the ceca. This is particularly well studied in poultry and domestic ducks, in which the anatomy of their ileal-cecal-rectal junction permits sieving of digesta so that only small particulates and water soluble compounds enter the ceca [47, 48, 49]. Digesta that enter the ceca are retained and sub-
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ence of wildlife agencies demonstrates that the nutritional biology of each subspecies determines its suitability for reintroduction into different habitats [43]. The fact that the Rio Grande and Gould’s subspecies have been unable to occupy the former range of the southern Mexican subspecies suggests that their nutritional biology differs.
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jected to microbial fermentation, whereas the digesta that are excluded quickly pass through the rectum and are defecated (rectal feces). The composition of the feces that arises from the ceca (cecal feces) is very different from that of the rectal feces. Cecal feces are enriched in bacteria and have higher levels of protein, fat, and vitamins [13, 48]. Consequently, the cecal feces may be consumed in some species, including chickens and turkeys (strategy 3, Figure 2). Rectal feces, which are excreted frequently throughout the day, often have green-colored streaks when fresh due to the presence of unmetabolized biliverdin. Cecal feces are excreted less frequently (once or twice a day) and microbial metabolism of biliverdin likely eliminates its green color, resulting in light brown to black coloration. Cecal feces are high in ammonia, putrefactive products from microbial metabolism, volatile fatty acids, and hydrophilic dietary fibers that impart a uniform viscous tex-
ture and a distinctive odor [50, 51]. Most omnivores switch between strategies as the availability of food items change. When readily digestible foods are available, they use strategy 1, but when high-fiber plant materials are consumed, strategies 2 or 3 may be used. Consequently, the amount and composition of feces, the rate of passage, and likelihood of coprophagy are dependent on the foods. Terrestrial herbivores, such as tinamou, are not constrained by weight limitations of acrobatic flight and have adapted a different digestive strategy than birds that are adept at flying. They have very large and highly sacculated ceca that allow the retention and fermentation of fiber for long periods of time. Ostriches are among the most efficient birds at utilizing dietary fiber [52, 53]. Their rectum is by far the longest of any bird and accounts for 52% of the length of the gastrointestinal tract. Dietary fiber digestibility in the ostrich
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FIGURE 2. Birds that eat other animals, nectar, grains, and fruits (strategy 1) have guts that lack voluminous ceca that are used for fermentation by herbivores, graminivores, and omnivores (strategies 2 to 4). Strategy 4 is common in mammalian herbivores and folivores but is almost completely absent in birds.
50–300 300–1440 Highly variable
1 1
1
1
2, 3, or 4 2 or 4 1, 2, or 3
Piscivores Insectivores
Granivores
Frugivores Herbivores Flying Terrestrial Omnivores
2
40–100
360–780 30–90
360–600
Very high Very high Highly variable
Very low
Very low
Very low, unless ceca are present Very low
Very low, unless ceca are present
Very low
Microbial activity
Ability to sort fermental fibers into ceca2 Massive ceca Combinations of the above Possess versatile ceca
Ability to process large quantities of water Minimize maintenance requirement for amino acids Ability to eruct fur, feathers, scales, and bones Ability to metabolize large amounts of protein and fat2 Same as above Ability to eruct exoskeletons Produce enzymes with chitenase activity2 Large muscular gizzard2 Lack ceca and alloenzymatic digestion Ability to skim readily available nutrients and excrete fiber without fermenting
Important attributes
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From Klasing [1]. Also used by chickens and turkeys.
1
15–60
1
Carnivores
30–50
1
Nectarivores
Retention time (min)
Nutritional strategy
Consumption category
TABLE 2. Overview of nutritional strategies of birds that consume diverse types of foods1
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size of the gastrointestinal tract, especially the gizzard and the ceca, and its capacity to ferment dietary fiber change throughout the season in conjunction with the quantity and quality of food consumed [13, 62, 63, 64]. For example, in wild turkeys, gizzard and cecal sizes are smallest in the summer, when the birds feed on tender shoots of newly growing herbaceous plants [38]. The gizzard is largest and most muscular, and the ceca are longest and yield the most volatile fatty acids in the winter, when birds feed primarily on woody stems, buds, and leaves. The time required for adaptive hypertrophy appears to be about 2 to 3 mo. The ceca of birds can have many functions, including absorption of water and other nutrients, conservation or detoxification of nitrogen, and fermentation. In chickens, the ceca can be used for any of these purposes, depending upon the diet. The extreme of the metabolic flexibility of chickens is illustrated by their ability to thrive on a 100% meat diet [61]. In other words, they can live the life of a carnivore. Chickens and turkeys can also adopt a pseudoskimming strategy and, at least as adults, maintain on a diet of poorquality herbaceous foods. Modern production practices illustrate that they can also live the life of a granivore, eating virtually only the seeds of corn and soya. The field of nutrition is referred to as a mature field. The glory days of nutrition occurred in the first half of the 20th century and few Nobel Prizeworthy discoveries in the field have occurred in the past 75 yr. These seminal discoveries allowed the previous generation of poultry nutritionists to make rapid progress. Current progress in poultry nutrition is incremental but slow. We could blame this on the lack of new breakthroughs in basic nutrition, but it might also be blamed on our lack of imagination. What future developments will catalyze progress in applied poultry nutrition? The nexus of comparative genomics with comparative nutrition is likely to be fertile ground for future advancements.
CONCLUSIONS AND APPLICATIONS 1. Turkeys and, especially, jungle fowl are omnivores. They are not granivores and do not consume diets that of predominantly grains in their wild environments. 2. The hallmark of omnivores is their morphologic and metabolic flexibility, which is considerably more robust than specialists, like granivores and faunivores.
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approaches that in the horse (cell walls, 47%; hemicellulose, 66%; and cellulose, 38%). Flying herbivores, like Galliformes and Anseriformes (ducks and geese), have limits to which they can utilize dietary fiber, and in some circumstances, a strategy is adopted in which fiber is largely ignored instead of fermented [54, 55]. For example, blue grouse eat conifer needles in the winter and ferment very little of the fiber in their ceca. However, they autoenzymatically digest relatively efficiently nonfiber carbohydrate and protein. High rates of consumption compensate for the low level of autoenzymatically digestible nutrients in their food. Many herbivores can switch between this low-efficiency skimming strategy and a higher-efficiency ceca fermentation strategy, depending on the fiber content of their diet or the quantity of diet available. In fact, geese in the arctic summer can space their feeding bouts over a 24-h period and adopt a strategy of a slow rate of passage and high fermentation. Later in the year, when the days are short and the quality of the grass is poor, their rate of passage increases, and this is accompanied by a marked reduction in the efficiency of fiber digestion. In birds adapted to a high-fiber diet, a skimming strategy markedly lowers the weight of digesta in the gastrointestinal tract and aids flight. The amount of feces is voluminous: geese feeding on grass defecate every 3 to 5 min, with each dropping averaging 5.5 cm in length [56]. A few species have an area for microbial fermentation in their crop, esophagus, and anterior proventriculus (strategy 4, Figure 2). This is taken to the extreme in the hoatzin [57, 58] but also occurs in mousebirds and kakapo. The digestive tract posterior to this fermentation area is relatively simple and resembles that of omnivores. The hallmark of omnivores is their morphologic and metabolic flexibility, which is considerably more robust than specialists, like granivores and faunivores [59, 60, 61]. In many species of Galliformes, including chickens and turkeys, the
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3. Understanding the digestive and metabolic adaptations of birds that are specialists at consuming insects, foliage, grains, and fruits will greatly enhance our understanding of poultry nutrition. 4. Current progress in poultry nutrition is slow relative to the glory days of the early 20th century. Imaginative applications of comparative genomics and comparative nutrition are likely to be fertile ground for renewed advancement.
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REFERENCES AND NOTES
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436 39. Mosby, H. S., and C. O. Handly. 1943. The wild turkey in Virginia: Its status, life history and management. VA Comm. Game and Inland Fisheries, Richmond, VA. 40. Leopold, A. 1933. Game Management. Scribner, New York. 41. Rumble, M. A., and S. H. Anderson. 1996. Feeding ecology of Merriam’s turkeys (Meleagris gallopavo merriami) in the Black Hills, South Dakota. Am. Midl. Nat. 136:157–171.
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Acknowledgments I thank Mamduh Sifri for tirelessly keeping the informative nutrition conference rolling, enthusiastically keeping it relevant, and providing me with a well-placed kick to catalyze the writing of this paper. An National Science Foundation Award (IBN-0212587) provided funding for comparative investigations of avian physiology.
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42. York, D. L., and S. D. Schemnitz. 2003. Home range, habitat use, and diet of Gould’s Turkeys, Peloncillo Mountains, New Mexico. Southwest. Nat. 48:231–240.
avian species that utilizes cellulose. SS-Afr. Tydskr Veekd. 23:127– 135.