Long, dry scientific article about importance of unripe seed

For all your questions about diet and food for your finches
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mattymeischke
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Anyone who doesn't like boring sciencey stuff, stop reading now; you have been warned.

This is a long review article about the significance of unripe seeds and animal tissues in the protein nutrition of herbivores. I was going to excerpt the bits about birds, but I found the whole article interesting and thought others might.
I made it it's own topic because I didn't want to clutter the green seed vs. sprouted seed topic, and because it doesn't cast much light on that debate.
I typed it all out because BrettB is not the only one who doesn't have access to many biology journals.

It is by Thomas White from the University of Adelaide; if someone knows him they could perhaps ask his opinion on the green seed versus sprouted seed question. It is reproduced here for the purpose of private study is and is not to be further reproduced, please. The full reference is:
White, T.C.R, 2011, The significance of unripe seeds and animal tissues in the protein nutrition of herbivores. Biological Reviews 86:217-224.

I: INTRODUCTION
Herbivorous animals usually struggle to acquire their minimum requirement of protein for successful reproduction and the growth of their young. This has resulted in the evolution of behavioural and physiological adaptations that increase their access to nitrogen in a form that can be absorbed and used for these functions (White, 1993). One of these adaptations is the preferential eating of flowers and unripe seeds. Evidence has now emerged that this behaviour is widespread although its significance is still largely unrecognised or its occurrence is dismissed as a chance event of no ecological significance. The behaviour is particularly common among seed- or fruit-eating mammals, birds and insects. Some, like most seed-eating insects, eat only developing flowers or seeds. Mature seeds alone, while usually providing sufficient nitrogen for adult animals to maintain body condition, mostly are not adequate to support the higher protein demands of breeding and growth of neonates (Allen & Hume, 1997). The common denominator throughout all examples of this behaviour is access to an enriched supply of soluble nutrients, in particular amino acids, flowing from the plant's stored reserves to its flowers and developing seeds or pollen. The concentration of amino acids in this flow to the reproductive parts is higher than that in the phloem to newly growing leaves that are preferentially eaten by flush-feeding herbivores (White, 1993, 2009).

The importance of this mobilisation and transport of a plant's nutrients to the success of herbivores has been shown by a study that specifically investigated this relationship. Furthermore, it showed that eating any part of a plant that carries increased supplies of nutrients to the reproductive organs will be of benefit. Miller, Tyre & Louda (2006) studied a coreid bug, Narnia pallidicornis, that feeds on a tree cactus, Opuntia imbricata, in the Chihuahuan Desert of New Mexico. The bugs will feed on all parts of the cactus, but prefer the reproductive structures. Miller et al. (2006) found a direct relationship between the proportion of resources allocated by the plant to reproduction and the number of young bugs produced, and hence the size of the coreid's population. Significantly, the growth of the population began before complete differentiation and ripening of the fruit. The population dynamics of this insect herbivore are driven predominantly from the “bottom-up” by the nutrient quality of its food plant via the amount of resources the plant allocates to reproduction. Neither predators nor competition from other herbivores had a significant influence on the bugs' abundance (Miller, 2008).


II. EATING UNRIPE SEEDS
This preference for, and dependence upon, plant tissues bearing enhanced levels of nitrogen to its reproductive tissues is now known to occur in many herbivorous birds, mammals, reptiles and arthropods, and also in some omnivores. The following examples illustrate how widespread this behaviour is. It is likely that many more examples will be found once attention is focused on it. Thus, White's (2002) suggestion that access to ripening grain might be the key to outbreaks of feral house mice (Mus domesticus) is supported by the experimental demonstration that juvenile house mice fed on ripening wheat grew faster than those fed on mature grains (Mutze, 2007).


(1) Mammals
The Siberian chipmunk (Eutamias sibiricus lineatus) eats the buds, flowers and unripe seeds of a wide range of plants during its breeding season (Kawamichi, 1980). In Europe the red squirrel (Sciurus vulgaris) consumes seeds from freshly formed cones of Pinus sylvestris and partly mature acorns (Quercus robur) and beechnuts (Fagus sylvaticus) (Wauters & Lens, 1995). Gestating females of the edible dormouse, Glis glis, “avidly consume” unripe beechnuts as soon as they start to form (Fietz et al., 2005), and both the edible (Adamik & Kral, 2008a) and the common dormouse, Muscardinus avellanarius, (Juskaitis, 2007) eat flowers, pollen and immature seeds of a variety of plants.

K. Kuhn (personal communication 2007) records that the American squirrel, Tamiasciurus douglasii, feeds extensively on the buds, flowers, pollen cones and immature seeds of Pinus jefferyi and P. contorta, and that the many unripe seeds they drop on the ground are eagerly harvested by chipmunks (Tamias amoenus and T. quadrimaculatus) and ground squirrels (Spermophilus lateralis). She also records these latter sciurids eating the buds, flowers, pollen and immature seeds of a variety of grasses and shrubs.

Red-backed voles (Clethrionomys spp.) in North America may show a similar response to access to unripe seeds. Boonstra & Krebs (2006) found that the fruiting of small, berry-producing shrubs was the major factor influencing the abundance of C. rutilus in the Yukon, and that increased winter snowfall provided higher moisture in spring that benefited the flowering and seed-setting of these shrubs. The ensuing burst of good food in the spring would allow full expression of the voles' capacity to produce five or six consecutive litters of five or six young per litter during the short breeding season, far swamping other potential influences on the size of their population. The red-backed voles' density did not respond to seed masts of white spruce (Picea glauca) and their predators were shown to be “irrelevant as a limiting factor” (Boonstra & Krebs, 2006, p.1269). The authors concluded that some other food must explain fluctuations in these populations. The voles' body mass increased significantly during the season ahead of a mast and they lost weight when fed a pure diet of spruce seed. The developing reproductive tissues of the small shrubs may well be the other food that is key to the increase of the red-backed voles (White, 2007).

This influence was via increased survival of the young that usually die before they are trappable. This highlights an important fact that is often overlooked in ecological studies; it is normally through its impact on the very young that food limits the abundance of animals. Neonates mostly die at an early stage because of a lack of adequate nutrition, so their fate is never witnessed and they are never registered as part of the population. In mammals they may be reabsorbed, aborted, cannibalised, abandoned or quickly starve. In birds poor-quality eggs produce non-viable young, eggs or nestlings are abandoned, or nestlings starve long before they could fledge. Most newly hatched insects die and disappear, unseen, as mere specks of dust.

Recent work with the bank vole, Clethrionomys glareolus has confirmed earlier findings (reviewed in White, 1993, Section 6.2.3) that successful breeding in this species, like many other voles, requires access in spring to herbs that are actively growing, flowering and fruiting. They also seek out ripening acorns in the autumn and germinating ones in the spring. A diet of acorns alone, and especially of ripe ones, is not sufficient even to maintain the voles' body mass, let alone support successful breeding. Similarly they cannot survive on a diet of mature herbs in the autumn (Wereszczynska et al., 2007).

Observations of herbivorous and fruit-eating primates preferentially eating flowers and unripe seed have, to date, been sparse and largely unrecorded because such feeding was considered to be unimportant. For example, olive baboons (Papio anubis) were recorded eating only unripe seeds of just one of the many plant species in their diet (Barton & Whiten, 1994). However, Milton (1980) found that howler monkeys (Alouatta spp.) ate unripe Ficus yoponensis, particularly when young leaves were less abundant, and that these contained higher levels of protein than the ripe fruit. Howler monkeys also eat great quantities of flowers (K. Milton, personal communication 2009) and unripe fruit (J. C. Bicca-Marques, personal communication 2009).

Furthermore, studies involving very meticulous daily observations sustained over one or more years are changing this belief, often to the expressed surprise of the authors! Hamilton & Galdikas (1994) found that orangutans (Pongo pygmaeus) selectively ate the flowers and unripe fruit of a number of species of plants. Of these, they spent the longest time foraging on the fruit of Irvingia malayana, stripping virtually all the fruit from the trees. They bit the end off the 5 cm × 3 cm unripe fruit, used their molar teeth to squeeze the gelatin-like contents of the seed into their mouth, and discarded the flesh.

More recently Lappan (2009) found that the fruit-eating Sumatran gibbon, Symphalangus syndactylus spends up to 40% of its time feeding on flowers, specifically on the male flowers of just one dioecious tree species. She also records that gibbons and orangutans in Borneo are known to eat large quantities of flowers.

Proboscis monkeys mostly eat young leaves, and like all colobine monkeys they have a large sacculated fore-stomach similar to ruminants for digesting this herbivorous diet. Yet Matsuda, Tuuga & Higahsi (2009) found in Malaysian Sabah that the proboscis monkey, Nasalis larvatus, also eats flowers and spends 30% of its time eating fruit, 90% of which is unripe and eaten preferentially even when new foliage and ripe fruit is abundant. In fact, all colobines prefer unripe fruit and seeds. Only a few species, on rare occasions, take ripe fruit (I. Matsuda, personal communication 2009).

Felton et al. (2008) expressed surprise to discover that in Peru, spider monkeys, Ateles chamek, that had always been assumed to be “ripe fruit specialists”, spend 23% of their feeding time all year round eating unripe fruits of Ficus boliviana, and that these provide more available protein per minute of feeding time than do the ripe figs. Furthermore, these monkeys feed on such food so as to supply a fixed minimum amount of protein in their diet, regulating intake of protein more tightly than that of energy-rich carbohydrates and fats (Felton et al., 2009).


(2) Reptiles
Some reptiles, in addition to those discussed in White (1993), are known to eat flowers. The large omnivorous Australian skinks, the blue-tongued (Tiliqua spp.) and the sleepy or shingle-back lizards (Trachydosaurus rugosus) eat quantities of flowers as well as developing fruit (T.C.R. White, personal observations). In North America all four tortoises (Gopherus spp.), the chuckwalla lizard, Sauromalus sp. and the desert iguana (Dipsosaurus sp.) all seek out wildflowers, especially yellow ones (K. Nagy, personal communication).

A more specific example is that of the sand dune lizard, Meroles anchietae, in the Namib Desert. It is an omnivore, with the bulk of its food comprising arthropods. However, on average its diet includes 37% immature seeds of grasses and herbs and individuals may have nothing else in their stomachs. These seeds are so immature as to be barely more than ovules. And when fed ripe seeds the lizards were unable to digest them (Nagy & Shemanski, 2009).

(3) Birds
Examples of feeding on developing reproductive tissues in birds are discussed in White (1993, Section 7.3). Particularly striking among these examples is the preferential feeding by bullfinches (Pyrrhula pyrrhula) on the flower buds of only some individual trees. In this and similar cases, the individual trees, or tree varieties that are favoured have been found to be those with the highest levels of amino acids in their tissues. Successful breeding for the goldfinch (Carduelis carduelis) and an Australian parrot, the galah (Eolophus roseicapillus) similarly depend on access to unripe seeds (White,1993 Section 7.3).

In more recent work, Allen & Hume (1997) demonstrated a similar dependence of successful breeding of the Australian zebra finch (Taeniopygia guttata). Zebra finches breed in the dry interior of the continent only after good rains produce abundant growth of grasses. The feeding of the young finches coincides with the peak of the flush of unripe grass seeds. Adult birds can maintain body condition on ripe seed alone, but cannot breed. Here again, the tissues on which feeding is concentrated are those with the highest levels of soluble amino acids. Allen & Hume (1997) clearly demonstrated what earlier studies had not, that access to these otherwise unavailable amino acids in unripe seeds is the essential key to successful breeding in this species.

An interesting consequence of this search for amino acids is the extent to which birds have learnt to preferentially seek out the developing flower buds and ripening seeds of non-native plants, in many cases becoming serious pests of grain and fruit crops. Thus the bullfinch can become a pest on crops and fruit trees, and displays intense selection for only some varieties and even individual trees. The Australian galah has expanded its range and numbers enormously feeding on seeds of introduced weeds and grain crops (White, 1993, Section 7.3.2 and 7.3.4). Adaptation to foreign food sources has become widespread and common in many Australian parrots. Once a population has discovered even a single tree, the birds return year after year, with impeccable timing, to harvest unripe seeds. The sulphur-crested cockatoo (Cacatua galerita) has become particularly adept at this, attacking green walnuts, barley crops and daffodil flowers (White, 2002), as well as barley-grass, and green Cupressus spp. and Pinus spp. cones. They also eat the unripe seeds of some varieties of citrus, extracting and peeling the seed, and discarding the fruit (V.B. White, personal communication 2008). Galahs, not normally seen in my garden in New South Wales happened upon a lone almond tree I planted. Thereafter they returned unerringly each year just in time to strip all the green fruit from it. I have observed rainbow lorikeets (Trichoglossus haematodus) extracting the unripe seeds from soft green cones of an ornamental cypress shrub in an Adelaide garden. So engrossed in their feeding were these usually nervous birds that I was able to approach and watch from within half a metre. Adelaide rosellas (Platycercus elegans adelaidae) attack green apples, and cotoneaster berries in suburban gardens, eating only the unripe seeds. They also became a major pest in cherry orchards in the Adelaide Hills of South Australia. Here they first attack fruiting buds, ignoring the vegetative ones, and then select out just the primordia from within these buds. Later they return to attack the ripening cherries, but selecting the fruit from only certain varieties (Reynolds, 2003). Every year, yellow-tailed black cockatoos (Calyptorhynchus funereus), along with sulphur-crested cockatoos, avidly strip green cones from the many pine trees growing in the suburbs of Adelaide and tear them open to eat the soft unripe seeds.

It seems likely that this preference for unripe seeds is widespread, including those of the birds' native food plants. Recently I was viewing an exhibition of wildlife photography and came upon the image of an Australian king parrot (Alisterus scapularis) with the green seed pod of a wattle in its beak. The photographer, M. Maconachie, recorded the bird “feeding on unripened Acacia seeds”. There are undoubtedly many more such examples - not recorded because their significance is not realised. Certainly examples from other parts of the world suggest that this is so.

Green fruit of rimu (Dacrydium cupressinum) and other podocarps make up the major component of the diet of breeding females of the New Zealand flightless parrot, the kakapo (Strigops habroptilus), which breed only in mast years of these trees (Raubenheimer & Simpson 2006). The unripe fruit is present during the winter/spring when breeding female kakapo consume significant quantities of it and feed it to their young (Fidler, Lawrence & McNatty, 2008). The importance of this food lies in its content of amino acids rather than as a source of energy (Houston et al., 2007). Also, like its Australian cousins, the kakapo will selectively eat unripe walnuts and pine seeds (Trewick, 1999).

Another New Zealand parrot, the kaka (Nestor meridionalis) also attempts to breed only in a year when native beech (Nothofagus spp.) trees produce a mast crop. They commence to nest before and when the trees are flowering, six months before seed fall. By the time the nestlings' demand for food is at a maximum, they are fed on the swelling green Nothofagus seeds (Wilson et al., 1998). The adults also feed on the flowers and fruit of rata (Metrosideros umbellata) and mistletoes (Perexilla spp.).

Unripe seeds predominate in the diet of nestlings of the Central America scarlet macaw (Ara macaro), and in Mexico the lilac-crowned parrot (Amazona finschi) consumes seeds that are mostly unripe (Renton, 2001, 2006). In Venezuela the green-rumped (Forpus passerinus) and dusky-billed (F. modestus) parrotlets both eat unripe seeds of a variety of plants, while the former feeds its nestlings exclusively on unripe seed of the high-nitrogen euphorb, Croton hirtus (Pacheco et al., 2004; M.A. Pacheco personal communication 2008). In Africa many species of Poicephalus parrots preferentially feed on unripe seeds of high-nitrogen legumes, manipulate flowers from which they selectively remove and eat the embryos, and can become pests attacking fruit crops, including unripe grapes and citrus blossoms (Selman, Hunter & Perrin, 2002; Boyes, 2008; Boyes, & Perrin, 2009).

Such dietary selectivity is likely much more widespread than realised, principally because investigators are not expecting and therefore not looking for it. Ninety per cent of the diet of adult Californian acorn woodpeckers (Melanerpes formicivorus) is acorns of five species of Quercus. Like so many other seed-eating birds they eat them as they are ripening, and then store ripe ones as winter/spring food (Koenig et al., 2008).

The painted honeyeater, Grantiella picta, a specialist feeder on the nectar and fruit of the mistletoe, Amyema maidenii, in Australia, spends up to 50% of its foraging time eating the fruit when it is green. This behaviour was only mentioned in passing because it was assumed the birds were using the green fruit as a measure of the future abundance of ripe fruit (Barea & Watson, 2007; Oliver, Chambers & Parker, 2003).


(4) Insects
The larvae of insects from diverse orders are known to feed entirely on or in developing seeds (White, 1993). The widespread and often very complex association of larvae of tephritid flies feeding on flowers and developing seeds of a wide range of plant species is particularly well documented (e.g. Straw, 1989). Yet new examples continue to be reported, including those demonstrating strong bottom-up limitation of numbers by food, and the absence of any significant influence of predators or interspecific competitors (Solbreck & Ives, 2007).

Another recent example is that of the larvae of the cecidomyiid Eucalyptodiplosis chionochloae (Kolesik et al., 2007). Along with larvae of a chloropid fly (Diplotoxa similis) and a gelechiid moth (Megacraspedus calamogonus), it attacks the inflorescences of tussock grasses of the genus Chionochloa in New Zealand. All three species complete their larval development either by the time flowering is completed or before any uninfested seed has ripened (McKone et al., 2001).

In addition to these seed predators there are, like the cactus bug discussed above (Miller, 2008), other examples of preferential feeding on developing reproductive tissues.

It has long been known that aphids congregate on parts of trees that are flowering (Perrins, 1966). A recent study confirmed this preference by quantifying the numbers of the aphids Dysaphis sorbi and Rhopalosiphum insertum on the leaves of mountain ash, Sorbus aucuparia, in Germany. Both aphids were found to be much more abundant on the trees that produced the greatest number of ripening fruit (Schaefer & Rolshausen, 2006).

The first and early second instar larvae of Pieris brassicae feed on the small leaves of the flower branches of their wild cruciferous host plants. But from late second instar, and for the remainder of the larval period, they feed exclusively on the flower buds and flowers themselves. There they sustain a significantly higher growth rate than larvae experimentally fed on leaves alone, in spite of the flowers containing up to five times higher levels of glucosinolates than the leaves (Smallegange et al., 2007).

Similarly, first and early second instars of the arctiid moth Utetheisia ornatrix feed on the tips of young leaves before entering the pods of several species of Crotalaria, where they feed on their developing seeds, even although they contain higher levels of alkaloids than the leaves. Again, they grow faster and bigger than larvae confined to feeding on leaves (Ferro, Guimaraes & Trigo, 2006). This behaviour is well known to farmers and gardeners from many species of noctuid cutworms (Helicoverpa spp.) which all enter the fruit to feed on the unripe seeds of plants as diverse as cotton, maize, tomatoes and green beans.

The first instar larvae of the autumnal moth, Epirrita autumnata, feed preferentially on the male catkins of the mountain birch, Betula pubescencs ssp. czerepanovii. When fed experimentally with these catkins more of them survived and grew faster to become heavier pupae (Klemola, Kaitaniemi & Ruohomaki, 2009).

An even more unusual example is that of females of the burrowing bug, Adomerus triguttulus, that feed on developing seeds of the mint, Lamium purpureum, before moving into the soil to lay their eggs. They then care for the hatching nymphs by bringing them developing seeds to feed on (Kudo & Nakahira, 2005).


III. EATING GERMINATING SEEDS
The amino acids locked into the protein of seeds are released and transported to the new growing plants when the seeds germinate. Here again, the benefit of feeding on such tissues comes from accessing the flow of amino acids, this time out of the seed into the plant. There are relatively few recorded examples of animals preferentially eating germinating seeds, probably because the observer did not recognise the significance of such behaviour. House mice are known to do so, selectively eating just the endosperm and cotyledons where the amino acids are concentrated (Bomford, 1987).

Wereszczynska et al. (2007) record bank voles eating germinating acorns in the spring, and K. Milton (personal communication 2009) records that baboons in Africa and capuchins in Panama dig up sprouting seeds from the soil and eat them. Sulphur-crested cockatoos have been recorded attacking a crop of germinating barley, eating just the meristematic tissues of the elongating stalks (White, 2002). Australian galahs exhibit a preference for meristematic tissues; they systematically dig up and eat the underground runners of kikuyu (Cynodon sp.) grass in Adelaide parks and gardens. The European nutcracker, Nucifaga caryocatactes, is known to bury the large seeds of stone (Pinus pumila) and edible (P. cembra) pines in the autumn, and return to harvest them once the snow melts in the spring. Then they selectively eat those seeds that are germinating (A. Battisti, personal communication 1998). European jays, Garrulus g. glandarius, store acorns in the soil in autumn and, when they germinate in the spring, feed extensively on the cotyledons (and feed them to their nestlings together with insects and the eggs of smaller birds) (Bossema, 1979).


IV. EATING ANIMAL TISSUES
As this last example illustrates, there are many apparently obligate herbivores that also eat animal tissues. I have previously discussed a number of examples where this behaviour seems to be necessary for successful breeding (White, 1993, Sections 10.4, 10.5, and Chapter 12), and, in particular, that virtually all neonate herbivores must eat some animal protein if they are to survive (White, 1985). Animal tissues apparently frequently provide key protein food required for otherwise herbivorous animals to be able to breed successfully. However, this, too, is a behaviour largely unreported in animals believed to be obligate herbivores. Here I discuss further examples.


(1) Mammals
Herbivorous mammals have evolved many other ways of supplementing dietary nitrogen (White, 1993), but including animal protein in the diet appears to be most prevalent in frugivorous and granivorous mammals. Many small seed-eating mammals eat insects during the breeding season (Fietz et al., 2005; White, 2007). Some, like the common (M. avellanariuus), forest (Dryomys nitedula) and edible (G.glis) dormice, also eat the eggs and young of hole-nesting birds (Juskaitis 2007; Adamik & Kral, 2008a,b). Squirrels will eat various small vertebrates as well as insects, and North American granivorous rodents of the genera Peromyscus, Tamius and Sciurus are well-known predators of birds' eggs (McShea, 2000).

The Djungarian hamster, Phodopus sungorus, which lives in the Siberian steppes, eats insects and stores large amounts of them in its burrows during the breeding season. In captivity these hamsters will not breed unless their diet of laboratory rodent chow is supplemented with animal protein (T. Ruf, personal communication 2007).

In Japan three species of variously folivorous and granivorous rodents, the wood mice Apodemus speciosus and A. argenteus, and the grey-sided vole, Clethrionomys rufocanus, all eat insects. Interestingly, A. speciosus is a specialist feeder on the acorns of Quercus crispula and the only one of the three whose abundance tracks that of oak masts. Yet when these mice were fed solely on an ad libitum supply of these acorns they died in 15 days (Saitoh et al., 2007).

Acorns alone cannot sustain the breeding of the white-footed mouse, Peromyscus leucopus. Insects are known to form a large proportion of their diet. Marcello, Wilder & Meikle (2008) recorded that mouse numbers increased dramatically during an emergence of periodic cicadas (Magicicada spp.) - the same response, said the authors, to a perishable pulsed resource as to a cacheable pulsed acorn mast.

The same story emerges for voles both in North America (Elias, Whitham & Hunter, 2006) and Europe (Wereszczynska et al., 2007; White, 1993, Section 6.2.3 and Chapter 17). Many species, including those usually assumed to be obligate herbivores, eat insects, especially before and during the breeding season. For example, Wereszczynska et al., (2007) found that if bank voles were kept in captivity in the autumn or spring on a diet of acorns alone, they lost weight. When fed a mix of their preferred herbs in autumn they also lost condition. However, when given freshly growing herbs in the spring they put on body mass. Clearly while flushing and fruiting tissues can sustain them in the spring, during autumn they must have access to some better food than mature herbs and acorns. Insects are the obvious candidates.

The red-backed vole, C. gapperi regularly eats insects (Elias et al., 2006), and its close relative, C. rutilus (Boonstra & Krebs, 2006), may also be getting the necessary nutritional boost from eating invertebrates that feed on the same reproductive tissues of their food plants.

It was once thought that primates were obligate folivores and/or frugivores, but increasingly careful study is revealing that this is not the case. The hunting and meat-eating habits of chimpanzees (Pan troglodytes) are now well known. Chimpanzees also regularly eat termites. Significantly, sharing of these animal foods favours breeding females and their young (Newton-Fischer, 1999).

Meticulous observations of the feeding habits of various species of monkeys have established that many of them also regularly eat animal tissues. Howler monkeys have long been considered to be “strictly vegetarian” (Bicca-Marques et al., 2009). However, Marcio Ayres recorded howlers (and other species of monkeys) in Brazil converging on trees with an outbreak of caterpillars and feeding on these insects until they were all consumed, before returning to their usual vegetarian diets (K. Milton, personal communication 2009). And Bicca-Marques et al. (2009) have now recorded repeated observations of two howler species, Alouatta caraya and A. guariba clamitans, eating birds eggs. Felton et al. (2008) recorded spider monkeys spending “long periods of time” concentrating on eating caterpillars in the foliage, and that they selectively feed to maintain a stable intake of protein by varying their total intake of energy (Felton et al., 2009). Similarly Lappan (2009) and Matsuda et al. (2009) respectively observed gibbons and proboscis monkeys eating termites, the latter consuming whole arboreal nests on a daily basis throughout the year. Such feeding on insects, while comprising only 1 to 2 per cent of total feeding time, is of much greater importance than is generally believed because it represents a greater intake of high quality protein per unit time than does the same time spent ingesting leaves or fruit.


(2) Birds
The New Zealand kaka, breeds only when there is a seed mast, yet eats quantities of honeydew from scale insects (Ultracoelostoma assimile) living on the bark of beech trees (Beggs & Wilson, 1991). It also spends 35% of its feeding time digging out from the trunks of the beech trees and eating large (up to 180 gm) larvae of the wood-boring kanuka longhorn beetle (Ochrocydus huttoni) (Wilson et al., 1998).

The Californian acorn woodpecker (M. formicivorus) specialises in eating acorns. Nevertheless it supplements this low-protein diet with a wide range of food, including the “occasional vertebrate”. In the spring it depends heavily on insects, feeding nestlings during their first two weeks on a diet that is 85% insects (Koenig et al., 2008).

The same is true for nectivorous and frugivorous birds. Tropical hummingbirds, Australian lorikeets and honeyeaters all eat insects and especially feed them to their nestlings (White, 1993 Section 7.2; Oliver, 1998; Oliver et al., 2003). Few if any frugivorous birds, and especially their young, could get adequate protein without eating insects (Herrera, Rodriguez & Hernandez, 2009).

In Africa, Meyer's and Ruppell's parrots (Poicephalus meyeri and P. rueppellii), like other Poicephalus parrots, preferentially eat unripe seeds. However, they also selectively forage for a variety of insects that can make up to 60% of the diet of females during egg-laying, incubation and nesting, and 100% of the regurgitate they feed to their nestlings (Selman et al., 2002; Boyes, 2008; Boyes & Perrin, 2009).

Across hundreds of kilometres of central Europe the fluctuations in abundance of populations of the great tit (Parus major) and the blue tit (Cyanistes caeruleus) are closely correlated with masting of European beech (F. sylvaticus) and with North Atlantic Oscillation-driven weather patterns (Saether, et al., 2007). These authors repeatedly state that the fluctuations in abundance of the tits are caused by the beech masts. However, in the case of the great tit, while this correlation between numbers of birds and beech masts has long been known, simultaneous fluctuations in the abundance of these birds also occur in areas where there are no beech trees (Perrins, 1966). Furthermore, their numbers increase when more young survive in the spring of years when there is going to be a mast crop in the succeeding autumn - that is before the seed becomes available (Perrins, 1966). So, there has to be some other factor in the environment that simultaneously improves the reproductive success of the trees and the tits. These birds eat a variety of tree seeds to sustain them through winter, but in the breeding season they are exclusively carnivorous, eating, and feeding to their fast growing young, the Lepidopterous larvae that feed on the new growth of deciduous trees. Perrins (1966) observed that there were more aphids on parts of trees that were flowering, so suspected a link between survival of young birds and the prevalence of animal food in the spring of those years when more seed is going to be produced in winter. White (1993, p. 226) suggested that this could well be the case because the mobilisation of nutrients into developing seeds in a mast year would also improve the plants' tissues as food for the caterpillars that in turn provide an increased supply of food for the breeding birds.


(3) Insects
In addition to examples discussed in White (1993), Whitman, Blum & Slansky (1994) record that facultative predation (and often cannibalism) by supposed herbivores is widespread in insects from at least seven orders and is most commonly encountered among newly hatched individuals and breeding females.

Seed harvester ants in the Chihuahuan Desert take small numbers of termites while foraging for seeds, but this was assumed to be opportunistic behaviour. However, Whitford & Jackson (2007) have found that Pogonomymex rugosus regularly eats termites and observed them selectively preying upon dense concentrations of grass cicadas (Beameria vanosa) as they emerge synchronously from the soil; behaviour reminiscent of that of white-footed mice.

The attendant parents of the burrowing bug (A. triguttulus) supplement the diet of unripe seed they feed to their young with animal protein in the form of trophic eggs (Kudo & Nakahira, 2005). As discussed in White (1993), the provision of unfertilised trophic eggs is a not uncommon method of supplementing the high protein needs of growing young of both invertebrates and vertebrates.


V. CONCLUSIONS
1. There appear to be sufficient examples to suggest that the eating of developing reproductive plant tissues and/or the tissues of other animals by herbivores is more than an occasional or chance behaviour.
2. The successful breeding of many animals may depend upon such food, and such additions to the diet are probably much more general and widespread than is realised, and spread across different taxonomic groups and feeding guilds.
3. The adaptive advantage of this behaviour is that animals gain increased access to the essential amino acids that are necessary to support successful production and subsequent growth of young.
4. There are likely to be many more cases than those listed here simply because nobody has looked. What is not looked for is not seen - even although it is clearly visible!
5. It is my hope that this review will alert ecologists to look for and investigate these behaviours that until now have never been considered, or have been dismissed as merely chance acts of no ecological significance.

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Avid amateur aviculturalist; I keep mostly australian and foreign finches.
The art is long, the life so short; the critical moment is fleeting and experience can be misleading, crisis is difficult....... (Hippocrates)
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Mortisha
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On the flip side, it is a dynamic that turns up regularly in commercial horticulture.

Overfertilization with nitrogen fertilizer increases the plant available nitrates, which in turn increases pest and disease damage.
Which makes growers spray more, and on and on it goes...
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BrettB
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Thank you for that, it makes interesting reading.

I was struck by how specific some of the feeding behaviours of the animals was. Different species targeting different parts of plants/types of insects depending on the time of year, breeding status, etc. I guess there are no real surprises in that, but it does highlight how complex this whole nutrition business is.

Whilst the author suggested various protein differences as the most likely explanation, there is no reason it could not be any one of numerous other nutritional components.
Allen, L. R. & Hume, I. D. (1997). The importance of green seed in the nitrogen nutrition of the zebra finch Taeniopygia guttata. Australian Journal of Ecology 22, 412–418.
concludes with the following statement
Results from this study, together with the argument developed above, indicate that the benefit of green seed vs ripe seed in the diet of breeding Zebra Finches is twofold. Soft unripe seed facilitates an increased throughput of digesta and thus an ingestion rate that allows extraction of more of the limiting essential amino acids lysine, threonine and methionine. As predicted by Moir (1994), green seed contains a higher proportion of lysine, the most limiting essential amino acid in ripe seeds.
This article is probably the most relevant from a finch keepers perspective. It again concentrates on the proteins and particularly the potential role of lysine.

Cheers
Brett
"We don't see things as they are, we see things as we are ." Anais Nin
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Tiaris
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What is meant by "limiting" & "most limiting" when referring to the amino acids? What is being limited? Please enlighten me.
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SamDavis
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Thanks for posting the article Matty - most interesting. I'd love to read Allen, L. R. & Hume, I. D. (1997) if it's available.
Tiaris wrote:What is meant by "limiting" & "most limiting" when referring to the amino acids? What is being limited? Please enlighten me.
Just did a bit of googling to try to get a handle on this limiting amino acid business.
1. I think we're only talking about essential amino acids (ones the body can't manufacture itself).
2. It seems the proportion of each essential amino acid absorbed by the body is fixed. Therefore the total diet must include all amino acids in correct proportion if they are all to be absorbed.
3. A limiting amino acid is one found in lower proportion than required which means it limits the absorption of all essential amino acids.
I maybe totally off the mark so please correct me all you medical/vet people.
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mattymeischke
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That's about right, Sam.

The amino acids are the necessary ingredients to build protein.
Protein includes a lot of the physical structure of a body, as well as enzymes, which are the chemical machinery that builds all the other proteins and handles all metabolic processes.
Building baby creatures requires a lot of protein, so breeding animals have to get enough for the demands of growth.
The amount of protein that can be made is limited by the availability of amino acids; your body can synthesise many, but not all, of the amino acids.
The amino acids that your body can't synthesise are called "essential" amino acids, as in it is essential to get them in your diet because you can't make them yourself.
The total amount of protein that can be synthesised is limited by the dietary availability of these essential amino acids.

An analogy:
If you are making pancakes, and you have 20L of milk, 30kg of flour and 6 eggs, the number of pancakes you make will be limited by the eggs.
If you had 20L milk, 200g flour and 12 eggs, then the limiting ingredient would be flour.

Hope that makes sense.
Avid amateur aviculturalist; I keep mostly australian and foreign finches.
The art is long, the life so short; the critical moment is fleeting and experience can be misleading, crisis is difficult....... (Hippocrates)
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Thanks very much guys. Another penny drops.
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claudicles
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SamDavis wrote:Thanks for posting the article Matty - most interesting. I'd love to read Allen, L. R. & Hume, I. D. (1997) if it's available.
Tiaris wrote:What is meant by "limiting" & "most limiting" when referring to the amino acids? What is being limited? Please enlighten me.
Just did a bit of googling to try to get a handle on this limiting amino acid business.
1. I think we're only talking about essential amino acids (ones the body can't manufacture itself).
2. It seems the proportion of each essential amino acid absorbed by the body is fixed. Therefore the total diet must include all amino acids in correct proportion if they are all to be absorbed.
3. A limiting amino acid is one found in lower proportion than required which means it limits the absorption of all essential amino acids.
I maybe totally off the mark so please correct me all you medical/vet people.
You've missed the point with 2 a bit samdavis. The abosorption of certain amino acids isn't the issue. The body absorbs what ever amino acids it can get its hands on, so to speak. If there is excess it can either be used to make other aminos acids, in the case of the essential amino acids, or used as a fuel source. The issue is more the amount of certain amino acids that is availble from certain sources. Lysine and methionine are both scarce from vegetable sources and more abundant from non veg sources. The key thing is not how much the body can use but how much the food source can supply. Then mattymeischkes pancake anaolgy comes into play. Great analogy btw. Wish i'd thought of it.

Liz
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