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The Evolutionary Ecology of Nut Dispersal.

I. Abstract

A variety of nut-producing plants have mutualistic seed-dispersal interactions with animals (rodents and corvids) that scatter hoard their nuts in the soil. The goals of this review are to summarize the widespread horticultural, botanical, and ecological literature pertaining to nut dispersal in Juglans, Carya, Quercus. Fagus, Castanae, Castanopsis, Lithocarpus, Corylus, Aesculus, and Prunus; to examine the evolutionary histories of these mutualistic interactions; and to identify the traits of nut-bearing plants and nut-dispersing rodents and jays that influence the success of the mutualism. These interactions appear to have originated as early as the Paleocene, about 60 million years ago. Most nuts appear to have evolved from ancestors with wind-dispersed seeds, but the ancestral form of dispersal in almonds (Prunus spp.) was by frugivorous animals that ingested fruit.

Nut-producing species have evolved a number of traits that facilitate nut dispersal by certain rodents and corvids while serving to exclude other animals that act as parasites of the mutualism. Nuts are nutritious food sources, often with high levels of lipids or proteins and a caloric value ranging from 5.7 to 153.5 kJ per propagule, 10-1000 times greater than most wind-dispersed seeds. These traits make nuts highly attractive food items for dispersers and nut predators. The course of nut development tends to reduce losses of nuts to insects, microbes, and nondispersing animals, but despite these measures predispersal and postdispersal nut mortality is generally high. Chemical defenses (e.g., tannins) in the cotyledons or the husk surrounding the nut discourage some nut predators. Masting of nuts (periodic, synchronous production of large nut crops) appears to reduce losses to insects and to increase the number of nuts dispersed by animals, and it may increase cross-pollination. Scatter hoarding by rodents and corvids removes nuts from other sources of nut predation, moves nuts away from source trees where density-dependent mortality is high (sometimes to habitats or microhabitats that favor seedling establishment), and buries nuts in the soil (which reduces rates of predation and helps to maintain nut viability). The large nutrient reserves of nuts not only attract animal dispersers but also permit seedlings to establish a large photosynthetic surface or extensive root system, making them especially competitive in low-light environments (e.g., deciduous forest) and semi-arid environments (e.g., dry mountains, Mediterranean climates). The most important postestablishment causes of seedling failure are drought, insufficient light, browsing by vertebrate herbivores, and competition with forbs and grasses. Because of the nutritional qualities of nuts and the synchronous production of large nut crops by a species throughout a region, nut trees can have pervasive impacts on other members of ecological communities. N ut-bearing trees have undergone dramatic changes in distribution during the last 16,000 years, following the glacial retreat from northern North America and Europe, and the current dispersers of nuts (i.e., squirrels, jays, and their relatives) appear to have been responsible for these movements.

II. Introduction

A nut is a dry, one-seeded fruit consisting of an edible kernel enclosed in a hard and woody or tough and leathery, indehiscent shell. Although this definition includes many species that produce relatively small propagules, I restrict its meaning in this review to those relatively large diaspores that are dispersed in the wild by birds and rodents that scatter hoard food items in the soil. Nut-bearing plants are widespread in the temperate and tropical regions of the world. Of primary interest in this review are ten genera: Juglans and Carya (Juglandaceae), Quercus, Lithocarpus, Castanea, Castanopsis, and Fagus (Fagaceae), Corylus (Betulaceae), Aesculus (Hippocastanaceae), and Prunus (Rosaceae). Some members of the genus Pin us (pine nuts) fit this definition but will not be covered here (see Tomback & Linhart, 1990, and Lanner, 1998, for recent reviews). Information on the dispersal of several tropical nut genera (e.g., Hymenaea, Astrocaryum, Gustavia, Dipterxy, Bertholletia, Elaeis) is accumulating (e.g., Hallwachs, 1986; Forget, 1991, 1992, 1993; Peres & Baider, 1997; Peres et al., 1997; Yasuda et al., 2000); no doubt these genera will be important to include in future reviews of this topic.

The literature on nuts comes from three distinct areas. Horticulturalists have conducted extensive and detailed studies on some nut-bearing plants to better understand how they can be cultivated to maximize fruit production for commercial interests. These studies include the biology of nut pests and how they can be controlled, genetic manipulations to produce different cultivars that bear nuts with desirable characteristics, and ecophysiological studies that explore how nutrient application, soil conditions, watering regimes, and harvesting techniques influence yields. Botanists have been concerned with the reproductive biology, morphology, phylogeny, fossil histories, and evolution of these plants. Ecologists, on the other hand, have attempted to understand the role of nut-bearing plants in natural ecosystems. Chief among these interests are the means by which nuts are dispersed and seedlings become established, the benefits that accrue to wildlife species that feed on nuts, and the roles of nut trees in fo rest dynamics. Unfortunately, the ecological literature has developed largely isolated from the horticultural and botanical studies and is very uneven. For example, there is little ecological information on several prominent nut genera (e.g., Lithocarpus, Castanopsis, Prunus). One aim of this review is to integrate the horticultural, botanical, and ecological literature to help better understand the ecological relations of nut-bearing plants in natural environments.

Nut-bearing plants appear to have coevolved, mutualistic relationships with several dozen rodent and bird (jays and related corvids) species that harvest their propagules. The benefit to the plants in these interactions is high-quality seed dispersal. In the process, the animals consume a significant portion of the nut crop, from which they derive sustenance during autumn and winter. Most of these relationships appear diffuse, with several animal species acting as dispersers for several plant species. Other species of birds, mammals, arthropods, and microbes act as parasites in these relationships, feeding on the nuts without providing any benefit to the plants. The mutualists in these interactions have, over millions of years, evolved traits that act to intensify the mutualism and to exclude the parasites. A second major focus of this review is to identify the traits of the nut-bearing plants and the nut-caching rodents and jays that contribute to the success of the mutualisms.

III. Synopsis of Nut Genera

Ten genera of trees and shrubs are conventionally thought of as nut bearers. The following is a brief summary of the biogeography, taxonomy, and nut characteristics of these ten genera.

Juglans. About 21 species of trees and large shrubs in the genus Juglans (walnuts) are distributed in eastern and southern North America, in mountainous regions of Central and South America, and in central and eastern Asia. McGranahan and Leslie (1991) partitioned the genus into three sections. Section Juglans contains the commercially valuable Persian walnut (J. regia) of central Asia. This species is unique in the genus in having a husk that dehisces at maturity, permitting the nut to fall free. Section Cardiocaryon consists of four species, the butternut (.1. cinerea) of eastern North America, the Japanese walnut J. ailantifolia, and two other species restricted to eastern Asia. Section Rhysocaryon contains 16 closely related species of North, Central, and South America. The eastern black walnut (J. nigra), with its hard, grooved shells and strongly flavored kernels, is typical of this section.

Carya. Hickories and pecans (family Juglandaceae) consist of 18 species found in eastern and southern North America, Mexico, and southeastern Asia (Manchester, 1987; Stone, 1989). Nuts are enclosed in a fibrous, four-valved husk that dehisces at maturity in September to December. The thick, woody shell varies from smooth to prominently grooved. The round-to-oval nuts range from 20 to 45 mm in diameter. Large nut crops are produced at intervals of one to five years. The cotyledons vary in taste among species, from sweet to bitter. The pecan (Carya illinoinensis) is one of the most valuable nuts in the commercial nut industry.

The eight genera of the Fagaceae are arranged into three subfamilies: Fagoideae (Fagus and Nothofagus), Quercoideae (Quercus and Trigonobalanus), and Castaneoideae (Castanea, Castanopsis, Chyrsolepis, and Lithocarpus) (Elias, 1971; Kubitzki, 1993). The present center of diversity of the family is southeastern Asia. The following five genera are covered in this review.

Fagus. The ten species of beech trees occur in temperate regions of eastern North America, Europe, and eastern Asia. The relatively small (10-15 mm diameter), ovoid-triangular nuts are produced in a four-valved, leathery cupule that is usually covered with short, recurved appendages. The nutshell is soft and leathery. Large crops occur at intervals of two to five years. Nuts ripen from September to November and often fall after the first frost.

Quercus. About 350-450 species of oak trees and shrubs are found throughout the temperate and tropical regions of North America, northwestern South America, Europe, and Asia, extending into Malaysia. The nut is an acorn partially to almost entirely enclosed in a scaly, cup-shaped cupule. The genus is subdivided into seven subgenera or sections: Erythrobalanus, Protobalanus, and Macrobalanus are restricted to the New World; Lepidobalanus is found in both the Old World and the New World; and Cyclobalanopsis, Cerris, and Mesobalanus are restricted to the Old World (Kubitzki, 1993). Members of the section Erythrobalanus, often referred to as black oaks (BO), and Lepidobalanus, often referred to as white oaks (WO), are common in temperate forests and have received more ecological study than the other sections.

Castanea. The 11 species of chestnuts occur in southern Europe, northern Africa, southwestern to eastern Asia, and eastern North America. Nuts are produced in a spiny cupule or bur that opens at maturity. Nuts are oval, are 20-35 mm long, and have a thin, leathery hull. Nuts fall from August to October. The cotyledons are sweet.

Castanopsis. About 30 species of shrubs and trees are found mostly in southern and southeastern Asia. Plants produce one-four ovoid or triangular nuts in a two- or four-valved, dehiscent, spiny cupule (Kaul, 1986, 1988). Nuts are relatively small (10-15 mm diameter) and have a soft, woody hull. Two members of the group found in the western United States (chinquapins) are sometimes assigned to the genus Chrysolepis (e.g., Kubitzki, 1993).

Lithocarpus. About 300 species are found from eastern India to China and southward through Indonesia to New Guinea. One species, tan oak (L. densiflorus), occurs in the western United States. The nut (an acorn) of some species is superficially similar to Quercus acorns, but these genera are not closely related. The closest relatives of Lithocarpus in the Fagaceae are Castanea and Castanopsis (Nixon, 1989). Acorns are ovoid or turbinate, are 10-50 mm long, and have a smooth or scaly cupule that partially encloses the nut (Kaul, 1987). The nutshell is relatively soft. Nuts ripen in the autumn. Large crops of tan-oak acorns occur in alternate years.

Corylus. The 15 or so species of hazelnuts or filberts (Betulaceae) range in size from large trees to shrubs and inhabit cool regions of Europe, Asia, and North America (Mehlenbacher, 1991). The nuts are nearly round, are 10-15 mm in diameter, and have a thin to very thick, woody hull. The husk is a highly variable involucre, ranging from a narrow, leafy tube constricted below the nut to a short, cup-shaped, spiny bur. Fruits are born in clusters of one to ten and ripen from August to October. The nut meat is sweet. Most nuts grown for the commercial nut industry are those of the European hazel (C. avellana).

Aesculus. Horse chestnuts or buckeyes (family Hippocastanaceae) comprise about 25 species, found in North America, Central America, southeastern Asia, and southeastern Europe. Nuts are generally oval or flattened, 20-50 mm in diameter, and enclosed in a leathery, three-valved capsule with or without weak spines (Hardin, 1955). The soft, leathery hull is a rich chestnut brown. Nuts ripen from September to November. Large crops occur at intervals of one or two years. The nut meat tastes bitter.

Prunus. Members of the genus Prunus (Rosaceae) produce fruits with either a soft, fleshy pericarp (e.g., apricots, plums, cherries) that attracts frugivores or a tough, dry pericarp containing nuts ("almonds") that are dispersed by food-hoarding rodents and birds. The almonds consist of about 25 species found in the deserts, steppes, and dry mountains from central Asia to southeastern Europe (Kester et al., 1991; Browitz & Zohary, 1996), and at least 7 species found in the deserts of western North America (Mason, 1913). The plants, usually small, thorny trees and shrubs, produce small to medium-sized nuts with hard or soft shells. The pericarp dehisces along one side of the nut when mature in midsummer. The nut meat varies from sweet to bitter. The commercial almond is P. dulcis.

IV. Evolutionary History of Nuts

Most of the nut-producing plants described above are found in one of two habitats: mesic forests, where competition for light can be intense, or semiarid regions with a prolonged dry season. Nuts have huge reserves of nutrients that confer a competitive advantage in both situations. The nutrient reserves of nuts permit them to either develop numerous leaves (photosynthetic area) or an extensive root system before they become independent (Baker, 1972; Salisbury, 1974; Reich et al., 1980; Foster, 1986; Bhagat et al., 1993; Hewitt, 1998). The head start afforded seedlings that emerge from nuts increases the probability of establishment relative to seedlings from smaller seeds. The competitive advantage conferred by large seeds is especially important in forest situations; mean seed size increases with increasing woodiness of vegetation and decreasing illumination of the habitat (Baker, 1972; Levin, 1974).

The fossil record shows that relatively large nuts first appeared during the Paleocene (Tiffney, 1986; Crane, 1989; Stone, 1989; Eriksson et al., 2000). The selective forces that caused the evolution of large nuts are complex. If the adaptive explanation offered in the above paragraph is correct, large, animal-dispersed nuts evolved primarily in response to abiotic conditions (low moisture or low light levels). But the emergence of nut-caching animals (primitive rodents and later corvids) also played a fundamental role in this process by providing the plants with an alternative and improved means of dispersal. Some food-caching animals prefer large nuts over small nuts (Bossema, 1979; Jensen, 1985) and preferentially cache large nuts and eat small nuts (Patrick Jansen, unpublished data). It seems likely that abiotic processes in concert with the dispersal services of scatter-hoarding vertebrates are responsible for the increase in nut size and that a combination of establishment requirements, nut dispersers, and nut predators are responsible for how those nuts are designed.

Close inspection of nut morphology and fossil relatives indicates two general patterns of nut evolution.


Most genera of nuts appear to have evolved from ancestors with wind-dispersed diaspores. The Juglandaceae presents the most clear-cut cases (Manning, 1940, 1978; Stone, 1973, 1989; Wing & Hickey, 1984; Tiffney, 1986; Manchester, 1987; Smith & Doyle, 1995). All modern authorities agree that most extinct (and living) relatives of Carya and Juglans had winged nutlets. Caryanthus is an extinct genus from the Paleocene of Sweden that shares numerous features with the Juglandaceae. It had laterally compressed nutlets [approx]1.6 mm long, with a short, apical wing. Details of flower and fruit structure suggest that Caryanthus is most closely related to the tribe Juglandeae, which includes the modern genera Pterocarya, with small nutlets attached to two papery wings, and Juglans (Manchester, 1987). The fossil record of Carya begins in the early Eocene (Manchester, 1987). Based on analysis of chloroplast DNA restriction site variation and morphological data (Smith & Doyle, 1995), Carya is most closely related to the genus Platycarya (see Manchester, 1987, for an alternative phylogeny). Platycarya, which also appeared in the early Eocene, has fruits that are tiny, flattened nutlets with lateral wings about 1-2 mm wide. In Juglans and Carya, the husk is thought to have evolved from bract and bracteoles of the inflorescence (Manning, 1940), the same structures that form the wings of Platycarya and Pterocarya. Casholdia microptera, an extinct species with small nutlets sandwiched between two leafy wings, is the oldest juglandaceous species in the Eurasian fossil record. It dates from the late Paleocene of southern England and France and appears to be related to three modern genera in the Juglandaceae: Engelhardia, Oreomunnea, and Alfaroa (Crane & Manchester, 1982; Manchester, 1987). Engelhardia and Oreomunnea fruits consist of nutlets at the base of three relatively long, leafy bracts that, in modern members of these groups, serve to disseminate the seeds by wind. In Alfaroa, a Central American group that appears to be recen tly derived from Oreomunnea, the bracts are vestigial, and the nut is [approx]30 mm in diameter.

In the Betulaceae (birches, alders, and relatives), fruits vary from small, winged nutlets in some Alnus and Betula, to medium-sized nutlets with a leafy involucre in Carpinus and Ostrya, to large nuts in Corylus (Stone, 1973; Crane, 1989). Fossilized Corylus nuts are known from the Paleocene of Montana, Greenland, and Scotland, but these nuts were relatively small ([greater than]10 mm diameter) compared with those of modern Corylus. The extinct genus Paleocarpinus from the Paleocene of England, France, and western North America produced flattened, ribbed nutlets between two leafy, involucral bracts (Crane, 1989) that may have been wind dispersed. These plants exhibit a number of characteristics that correspond to those predicted for a hypothetical ancestor of the Corylus-Carpinus-Ostrya clade (Crane, 1989).

The evolutionary history of the Fagaceae is less well known. The earliest fossil material comes from the Paleocene/Eocene of western Tennessee and includes a scaly cupule that enclosed three winged nutlets with similarities to Trigonobalanus, a modern relative of oaks, and assigned to the species Trigonobalanoidea americana (Crepet, 1989; Crepet & Nixon, 1989). One of the best-represented fossil members of the family is Fagopsis longifolia, an unusual and extinct species from the lower Eocene of eastern Washington and the Oligocene of Colorado (Manchester & Crane, 1983; Tiffney, 1986). The cupules in Fagopsis were membranous, hairy wedges about 4-6 mm long. Three tiny nutlets ([approx]0.5) mm in diameter) were situated at the base of each cupule. The cupule and enclosed nutlets detached from the infructescence singly or in groups and may have been adapted for wind dispersal. The earliest fossil specimens of nut-producing Fagaceae (Quercus, Castanea, and Trigonobalanus) are from the middle Eocene (Manchester & Crane, 1983; Tiffney, 1986). Tiffney (1986) suggested that the transition from a predominance of abiotically dispersed fruits to a mixture of biotically and abiotically dispersed fruits in the Fagaceae (and Juglandaceae) occurred in the early Tertiary, coeval with the radiation of potential mammal and bird dispersal agents. The differences in fruit morphology between Fagopsis and extant Fagaceae parallels that found between Platycarya and Juglans in the Juglandaceae and between Alnus and Corylus in the Betulaceae (Manchester & Crane, 1983). In most modern Fagaceae, not only are the nuts larger but the cupules, which are thought to have evolved from sterile axes of the inflorescence (Brett, 1964; Forman, 1966; Fey & Endress, 1983), have been greatly modified in one of two general ways. In Castanea, Castanopsis, and Fagus the cupule usually completely encloses the nut. These cupules are usually armed with spines but dehisce at maturity to expose and release the nut. In Quercus and Lithocarpus, the cupules form a cap covering the basal portion of the acorn. Cupules in these genera typically lack spines and are indehiscent, with the apical portion of the acorn exposed (Brett, 1964; Kaul, 1987, 1989). The cupule provides protection to the developing nut through its armature, sclerification, and tannins (Kaul, 1985; Kubitzki, 1993).

It seems reasonable to conclude that modern nuts of these genera evolved from wind-dispersed nutlets. The evolutionary mechanism is probably similar to that suggested for several groups of large, wingless pine seeds that evolved from winged ancestors (Vander Wall & Balda, 1977; Lanner, 1982, 1998; Tomback & Linhart, 1990; Vander Wall, 1992). Animals may have removed the wings from nutlets and cached the nutlets in the soil for later use (just as modern rodents and jays do with some winged pine seeds; e.g., Vander Wall, 1992), and the unrecovered cached nutlets proved to be a more efficient means of dispersal and seedling establishment than did the wind.


Almonds appear to have evolved from plants that produced succulent drupes that were dispersed by fruit-eating mammals or birds. Among cultivated species of the genus Prunus, the closest relative of the almond (P. dulcis) is the peach (P. persica) (Kester et al., 1991; Badenes & Parfitt, 1995). Both almonds and peaches are thought to have originated in the steppes of central Asia. Kester et al. (1991) and Watkins (1995) suggested that the lineages leading to these species split following the uplifting of the Himalayan massif, with almonds evolving in the arid steppes and deserts of southwestern Asia while peaches evolved in the more mesic environs to the east, in China. The ancestor of these species was probably dispersed by frugivorous animals that consumed the entire fruit and then defecated or regurgitated the small, woody nut at some distance from the parent plant, as is the case for modern, fleshy-fruited Prunus (e.g., Herrera & Jordano, 1981). For the animals that disperse these species, the fruit pulp serves as a reward, often of relatively low nutritional value, and the nut is simply ballast to be dumped as soon as possible. Dispersal distances range from a few meters to many kilometers, but the probability of seedling establishment is often low. Many nuts are killed in the digestive tract or are deposited in relatively low quality sites.

The evolution of the nut-bearing Prunus probably occurred through a combination of abiotic and biotic selective pressures. The approximately 25 species of nut-bearing Prunus that range from southwestern Europe to China all occur in arid environments. The same is true of the seven species found in the western United States. The arid environments that these plants occupy probably intensified selection for water economy that may have fostered the evolution of dry fruits. Coupled with this abiotic selection was the effect of food handling by some primitive rodents and birds. To some of these animals, the cotyledons represent a more attractive energy reward than does the fruit pulp. Furthermore, the nut is much less perishable and so can be stored and eaten later, when food is less abundant. After eating a small amount of fruit pulp, some seed-hoarding rodents will strip the pulp away from seeds, discard it, and load the seeds into their cheek pouches (Vander Wall, pers. obs.). Under certain circumstances this be havior can benefit the plant. If the seeds are scatter hoarded in the soil and if a sufficient number of the seeds are neglected, then the cached seeds may experience a higher probability of successful establishment than may seeds dispersed by frugivores. Being cached is an effective way for a seed to become buried, and seed burial is especially important in arid environments, where maintaining high moisture content of the seed during germination can be difficult. Frugivore-dispersed seeds, on the other hand, are deposited on the ground surface and often in dense concentrations under favorite perches, where establishment probabilities may be very low. Dispersal by nut-caching animals also releases plants from having to expend precious water on succulent fruits to attract frugivores.

It appears that the reward for the dispersal services of nut-caching animals was gradually transformed from the pulp surrounding the nut to the nut itself. Along the way, other features of the fruit were also transformed. The pericarp became a dry husk that nurtures and protects the developing nut from various sources of predispersal seed mortality. Chemicals and fibrous tissues in the husk discourage insect attack and premature foraging by potential dispersers. Upon maturity, however, the husk splits open, and, in many species, the nut falls to the ground, where most nut-hoarding animals (rodents and corvids) forage. These traits promote rapid harvest of the nuts by the animals most likely to serve as effective dispersers. The transition to a fruit crop that consisted of fewer, larger nuts served to attract more nut-caching animals and to provide embryos with a larger supply of nutrients to promote the establishment and early growth of seedlings.

Once an incipient mutualistic relationship was established between nutlet-producing plants and nutlet-caching animals, the intensity of the relationship could increase through co-evolutionary interactions among dispersers and plants within the context of strong selection imposed by the abiotic environment. In addition to having their nutlets buried, plants may have benefited from target dispersal, the disproportionate movement of propagules to favorable microhabitats for establishment (Grey & Naughton, 1971; Stapanian & Smith, 1986; Vander Wall, 1993), and long-distance dispersal (Clark, 1998). And because seed-caching corvids and rodents often space caches widely (Stapanian & Smith, 1978, 1984; Clarkson et al., 1986), more seeds are likely to be placed in favorable sites. In contrast, dispersal by the wind and frugivores is arbitrary with respect to safe sites and often results in highly clumped dispersions of seeds.

Nut size increased under these selective pressures. As a consequence, nuts became more attractive to nut dispersers and nut predators alike. In response, some plants evolved nuts with harder shells and enclosed the nuts in thick, fibrous, chemically protected husks to thwart the foraging efforts of many potential seed predators. Synchronous fluctuations in the size of nut crops may have evolved as an additional means of reducing the efficiency of nut predators and increasing the effectiveness of nut dispersers.

V. Evolution of Nut-Dispersing Animals

Animals that are likely to be important dispersers of nuts in temperate Holarctic forests include rodents belonging to Sciurus, Spermophilus, Tamias, Apodemus, and Peromyscus, and corvids belonging to Garrulus, Cyanocitta, Aphelocoma, Nucifraga, and Corvus. Members of all of these genera are known to store large quantities of intact nuts or acorns in the soil at sites where germination of neglected nuts is probable. Some of these genera may be the descendants of those species that dispersed the nutlets of the emerging nut genera early in the Tertiary.

The multituberculates, a diverse and well-represented group of mammals that first appeared in the late Jurassic of North America (Van Valen & Sloan, 1966; Carroll, 1988), were very likely the earliest nut-dispersing mammals. These animals were relatively small, omnivorous, and rodentlike. Among the multituberculates, one of the best-known genera is Ptilodus, from the Paleocene of Saskatchewan, which were similar in many ways to small squirrels. Striations on fossilized teeth suggest that these animals fed on hard food items, such as seeds and nuts (Krause, 1982). Some species of Ptilodus were arboreal and are suspected of having been important dispersers of plant seeds and fruits (e.g., Del Tredici, 1989). Members of the Multituberculata were present for more than 100 million years, from the late Jurassic to the Oligocene (Van Valen & Sloan, 1966; Carroll, 1988). Thus, they came on the scene before nuts evolved and overlapped with the early nut ancestors for about 30 million years.

The earliest known true rodents, the ischyromyids, are from the Paleocene of North America. The modern family Sciuridae (squirrels and relatives), which first appears in the fossil record in the late Eocene, shows clear relationships to the ischyromyids (Carroll, 1988). By the early Miocene, tree squirrels virtually identical to modem members of the genus Sciurus appear in the fossil record (Emry & Thorington, 1984). The family Cricetidae (mice) is represented in the fossil record by the late Eocene of China and the early Oligocene of North America (Carroll, 1988).

The fossil record indicates that first multituberculates and later ischyromyids, squirrels, and mice have coexisted with nut-bearing plants and their ancestors since the Cretaceous, and it appears that these plants and animals may have had strong effects on each other's evolutionary histories. Paleontologists have suggested that the great success of the multituberculates is related to the radiation of angiosperms, which may have provided new food sources that these animals were able to utilize (Clemens & Kielan-Jaworowska, 1979). Paleobotanists, on the other hand, attribute the rapid increase in propagule size of nut-bearing plants in the Paleocene to the emergence of mammalian dispersal agents (Crane, 1989; Tiffney, 1986).

The early evolutionary history of the Corvidae is poorly documented. The oldest corvids date from the Miocene (Brodkorb, 1978). Corvids are related to birds of paradise, Old World orioles, Australian magpies, and other groups (Sibley & Ahlquist, 1990). Only a few of the modern members of these groups store food, and where food hoarding does occur it is poorly developed (Vander Wall, 1990). This suggests that food hoarding evolved in corvids after the corvids split from these other groups. Therefore, it is unlikely that the ancestors of corvids were important in the early evolutionary history of nuts. However, corvids probably became important dispersers of certain nuts after nut genera had become firmly established (perhaps before the Miocene). Since that time they have played an important role in these plant--animal interactions, acting as important evolutionary forces on nut morphology and phenology.

Animals have evolved a variety of morphological structures to handle nuts. Multituberculates had large, slicing premolars and strong jaws that may have been used to open hard seeds (Krause, 1982). Sciurid rodents have very strong jaw musculature and are among the few animals that can open the hard shells of Juglans and Carya nuts (Emry & Thorington, 1984). Among corvids, nutcrackers and some jays have sharp, chisel-shaped bills (Turcek & Kelso, 1968; Vander Wall & Balda, 1981; Zusi, 1987). Some New World jays (e.g., Aphelocoma) have the lower jaw articulation buttressed, which enhances the use of the lower mandible as a chisel (Zusi, 1987). This greatly increases the efficiency of the bill as a tool to open acorns and other soft-shelled nuts.

Animals that transport small nuts (beechnuts, some acorns, hazelnuts) often have specialized structures (cheek pouches, sublingual pouches, or distensible esophagus) in which to carry several items (Bock et al., 1973; Bossema, 1979; Darley-Hill & Johnson, 1981), whereas animals (e.g., squirrels) that scatter hoard large nuts (e.g., walnuts, hickories, horse chestnuts) usually lack specialized structures and carry single nuts in their mouth or between their teeth (Muul, 1970; Stapanian & Smith, 1978). Transporting structures have apparently evolved because animals cannot profitably transport small nuts long distances unless many can be transported simultaneously.

VI. Nutritional Qualities of Nut Meats

The nut meat (cotyledons and endosperm) serves two important functions: as a nutrient and energy supply to finance the early development of a future seedling, and as a potential nutritional reward to entice an animal to gather, transport, and store nuts. For this dual function to work, a portion of the nut crop must serve as the reward for animals to disperse the remainder of the crop (Janzen, 1986). Whatever the ultimate fate of a nut, both objectives can be met by producing relatively large nut meats filled with energy-rich foodstuffs.

Nuts occupy the upper end of the seed-size spectrum. Most species of nuts produce edible nut meats that weigh 1-5 g (Table I), 10-10,000 times larger than the edible portions of seeds that are dispersed by physical processes (e.g., wind) (Grime & Jeffrey, 1965; Grodzinski & Sawicka-Kapusta, 1970). Nut meats typically comprise 33-67% of the intact nut (Table I). The caloric value of nut meats (per gram dry weight) ranges from 26.0 to 34.0 kJ/g in Juglans, Carya, Corylus, Prunus, and Fagus and from 17.5 to 22.0 kJ/g in acorns (Table I). The values for nuts are not much higher than are the caloric values of the edible portions of wind-dispersed seeds (23.0-30.0 kJ/g). However, on a per unit basis, nuts typically contain 10-1000 times more energy than do seeds dispersed by wind (Grime & Jeffrey, 1965; Grodzinski & SawickaKapusta, 1970). Consequently, the value of nuts to wildlife is due mostly to their large size.

Embryos make two demands on the reserve materials within nuts and seeds. They use them as sources of carbon skeleton precursors and as a source of energy to assemble those precursors into metabolic machinery and cell constituents (Levin, 1974). The two most important groups of energy-producing molecules are lipids (in the form of fatty acids) and carbohydrates (in the form of starch or hemicellulose). Lipid content of seeds, like seed mass, is correlated with increasing woodiness and decreasing illumination of the habitat (Levin, 1974). Nuts that are associated with the commercial nut industry are consistently high in fats (54-71%) (Table II). Noncommercial nuts, such as acorns, typically have much lower values for lipids: 11-31% for BO acorns, and 3-12% for WO acorns. The most abundant fatty acids in nuts are the unsaturated oleic and linoleic acids and the saturated palmitic and stearic acids (Stone et al., 1969; Beuchat & Worthington, 1978; Kester et al., 1991; McGranahan & Leslie, 1991; Mehlenbacher, 199 1; Parcerisa et al., 1993, 1994; Senter et al., 1994). Percentage of lipid content is correlated with palatability (Smith & Follmer, 1972), and fatty-acid composition of nuts also may be important, because fatty acids vary in nutritional value, melting point, and effects on storability. Low oil content and unsaturated fatty acids are correlated with short shelf life of nuts (McMeans & Malstrom, 1982). The melting points of fatty acids in nuts are higher in tropical regions than in temperate ones (McNair, 1929).

Carbohydrates (nitrogen-free extract) are highly variable in commercial nuts (3-86%), high in BO acorns (56-79%), and very high in WO acorns (78-89%) (Table II). Carbohydrate content tends to vary inversely with lipid content. Carbohydrates contain approximately half as much energy (kJ/g) as do lipids. This difference in composition accounts for the generally lower weight-specific caloric value of acorns relative to commercial nuts (Table I).

The cotyledons of some nut species contain significant quantities of polyphenols (condensed or hydrolyzable tannins) (e.g., Koenig & Heck, 1988; Fleck & Layne, 1990; Steele et al., 1993). Tannins are secondary compounds that are part of the nitrogen-free extract and so are often lumped in with carbohydrates. Although data are scant, acorns of the BO group are generally high in tannins (5.7-11.3%), acorns of the WO group are intermediate (0.6-5.6%), and other species of nuts typically have low levels of tannins (0.2-1.7%) in the nut meat (Wainio & Forbes, 1941; Ofcarcik & Burns, 1971; Polles et al., 1981). Tannins are thought to reduce the digestive efficiency of nut predators.

The protein reserves in nut meat are not used as an energy source by seedlings but are hydrolyzed to amino acids to make proteins and other nitrogenous cellular components. Most storage proteins in seeds are deposited in subcellular protein bodies in the cotyledons (e.g., Collada et al., 1993). Protein levels in commercial nuts (4-32%) are typically two to four times higher than in acorns (4-8%). WO and BO acorns and chestnuts differ little in protein content (Table II). However, BO acorns are generally high in tannins (polyphenols), which are thought by some researchers to interfere with protein digestion (see sections VIII and IX); as a consequence, BO acorns (and to a lesser extent, WO acorns) may have little available protein.

The kernels of most species of nuts are rich in minerals relative to other plant tissues, including nitrogen (N), phosphorus (P), potassium (K), calcium (Ca), magnesium (Mg), iron, manganese, copper, and zinc (Lewis & Hunter, 1944; Hammar & Hunter, 1946; Kester et al., 1991; Mehlenbacher, 1991; Drossopoulos et al., 1996). Most species of nuts are important sources of minerals for foraging animals (Havera & Smith, 1979).

The water content of nuts can vary widely with age and storage method but still shows some trends. Free water content of mature, dormant, unburied commercial nuts ranges from 2 to 11% but is much higher in BO acorns (9-42%) and WO acorns (16-47%) and is very high in chestnuts and horse chestnuts (33-58%) (Table II). Water content varies inversely with the amount of lipids, which are hydrophobic compounds, and directly with carbohydrates and proteins. Once buried, the water content of nuts varies widely, depending on the moisture content of the soil. The water content of nuts has important implications for nut dormancy and fall germination (see section XI).

From the perspective of vertebrates foragers, nuts are among the most nutritious foods available. Compared with buds, green vegetation, cambium, or fruit, nuts represent fairly rich sources of carbohydrates and/or lipids. Proteins in nut meats range from moderate to low and may be unavailable in acorns because of the effects of tannins, but nuts supplemented with other sources of protein (e.g., insects) can provide a balanced diet. Drozdz (1968) found that small mammals could assimilate 89% of the energy in beechnuts, 91% of the energy in hazelnuts, 79% of the energy in acorns, but only 72% of the energy in green vegetation (forest herbs). Rodents maintained a positive nitrogen balance and gained mass on diets of beech mast or hazelnuts but had a negative nitrogen balance and lost mass on diets of acorns or green vegetation.

VII. Nut Development

Nuts take either one year or two years to develop. In species like almonds, walnuts, hickories, horse chestnuts, hazelnuts, beechnuts, and "1-year oaks," the nut flower primordia form in the autumn and are pollinated and fertilized the next spring; nuts develop during the summer and autumn. In other species like chinquapins, tanoak, and "2-year oaks," the nut flower primordia form in the autumn and are pollinated the next spring. However, the development of these flowers is arrested during the remainder of their first summer. During their second spring, development is reinitiated, fertilization occurs, and the nuts develop during the second summer and autumn. The adaptive significance of these two developmental programs is unclear, but it has implications for the synchronous production of nut crops (e.g., Koenig et al., 1996; see section XII).

The floral biology and early embryo development of nut species have been described by Woodroof and Woodroof (1927), Nast (1935), Manning (1940), Hagerup (1942), Pinney and Polito (1983), Me et al. (1989), and Botta et al. (1995). The general pattern of nut development is similar for most species. Shortly after the egg is fertilized, the ovary contains a globular-shaped embryo surrounded by a small amount of endosperm and a relatively large mass of tissue, the nucellus. Outside this are a thin integument and the ovary wall. As the embryo develops, it becomes torpedo shaped, grows two cotyledons, and absorbs the endosperm and eventually the nucellus to occupy nearly all of the space within the ovary wall. The cotyledons enlarge until they eventually constitute 90-99% of the embryo tissue. The embryonal axis continues to elongate and differentiate, ending at maturity with up to ten leaf primordia around the apical meristem and a root cap covering the root meristem. The integument eventually becomes the seed coa t, a thin layer of tissue that covers the embryonal axis and cotyledons, and the ovary wall becomes the shell. The husk is derived from various tissues, including involucral bracts, bracteoles, and, in almonds, the outer portion of the ovary wall (exocarp and mesocarp).

The development of nuts is characterized by two distinct stages of growth, described for pecans, walnuts, and filberts (Woodroof & Woodroof, 1927; Shuhart, 1932; Thor & Smith, 1935; Hammar & Hunter, 1946; McKay, 1947; Thompson, 1979; Drossopoulos et al., 1996). First, the ovary wall, integuments, and nucellus of the fruit grow rapidly, but with little growth occurring in the embryo, cotyledons, and endosperm. During this stage the fruit assumes its mature shape and nearly reaches mature size. This is often referred to as the water stage because of the high water content of all fruit tissues. During the second, or kernelfilling, stage the embryo, cotyledons, and endosperm grow rapidly to fill the available space within the ovary wall. By the end of this stage the embryo achieves full size, the cotyledons have expanded to fill most of the space within the shell, and reserve materials have been translocated into the cotyledons. In stone fruits (e.g., peaches), which have some similarities to nut development, th ere is a third stage of development, characterized by a resurgence of growth in the ovary wall during which it increases in size and becomes succulent as the fruit reaches maturity (Chalmers & Van den Ende, 1977). In nuts, however, the third stage is missing and instead the pericarp or accessory tissues gradually dry out as the nut matures. The sequence and timing of these events have important consequences for the biology of nut-bearing plants and for the feeding behavior of insects, vertebrates, and other organisms.

During the kernel-filling stage, which for pecans takes more than two months, total dry matter of the kernel increases rapidly during the first month and more gradually during the second month (Woodroof & Woodroof, 1927; Thor & Smith, 1935; Hammar & Hunter, 1946). The ripening date varies from early October to mid-November, depending on weather, cultivar, and locality. The percentage of water content in the embryo declines over the same period. During kernel filling, the dry mass of all nutritional components (protein, carbohydrate, lipid, crude fiber, and ash) increases. However, the proportion of lipids usually increases more rapidly than do those of the other constituents. For example, the percentage of dry mass of lipids in pecans increases from 48% to 68% during development, whereas the percentage of all other constituents decreases (Woodroof & Woodroof, 1927). The rapidity of these changes is illustrated by the fact that 64% of the lipid and 71% of the protein in mature pecans form within a three-week period (Hammar & Hunter, 1946).

In pecans and Persian walnuts, minerals (N, K, P, Mg, and Ca) are rapidly translocated into kernels during the weeks preceding nut maturation (Hammar & Hunter, 1946; Drossopoulos et al., 1996). In pecans this mineral buildup in the cotyledons occurs while the same minerals in the supporting shoots are being depleted (Lewis & Hunter, 1944; Hammar & Hunter, 1946). Later in the autumn there is a measurable return flow of minerals out of the cotyledons and husk back into the supporting twig as the nearly ripe nuts dry out (Drossopoulos et al., 1996).

The endocarp hardens to form a woody or leathery shell during kernel filling through the process of lignification. No further growth of the nut can occur once shell hardening is well under way. The hardened shell serves as a barrier to some foragers at the time that the embryo is becoming increasingly attractive to animals. For ripe pecans, hull color is darker for filled nuts than for faulty nuts (Woodroof & Woodroof, 1927). Foragers may use this difference in shell color to assess nut quality.

VIII. Predispersal Predation of Nuts by Insects and Microbes

Weevils (Curculio spp. and Conotrachelus spp.) are among the most important pests affecting the fruits of nut-bearing plants. Typically, the first damage occurs early in the summer as nuts are developing (water stage) and before the kernel has begun to fill (Brooks, 1922; Moznette et al., 1940; Criswell et al., 1975; Mehlenbacher, 1991; Rutter et al., 1991; Thompson & Grauke, 1991). Weevil larvae tunnel through the husk and kernel tissues, causing the blackened, immature nuts to fall within a few days. More conspicuous damage occurs when later broods feed on the nearly mature kernel or, if the shell has already hardened, on the husks. After several weeks of feeding, the larvae leave the nut and burrow into the soil. Weevil larvae that attack acorns feed on the cotyledons (Gibson, 1971, 1972; Oliver & Chapin, 1984). Damage to acorn crops can be extensive (Kautz & Liming, 1939; Reid & Goodrum, 1958). Levels of weevil-larvae infestation of acorns are correlated with tannin content (Weckerly et al., 1989b). The degree to which individual acorns are injured is related to the number of larvae per acorn, which typically ranges from one to six but can be much higher. When the embryo is consumed or the cotyledons extensively damaged, the acorn is killed, but when consumption of the cotyledons is limited, infested acorns can still germinate and produce viable seedlings (Downs & McQuilkin, 1944; Oliver & Chapin, 1984; Weckerly et al., 1989b; Hubbard & McPherson, 1997). For example, 24% of weevil-infested Quercus virginiana acorns germinated, compared with 80% of uninfested acorns (Oliver & Chapin, 1984). The height of seedlings from these infested acorns after one summer was [approx]70% that of seedlings from uninfested acorns. Nut-caching rodents and jays do not always discriminate between infested and uninfested acorns and nuts (Dennis, 1930; Lloyd, 1968; Stiles & Dobi, 1987; Semel & Andersen, 1988; Weckerly et al., 1989a), although Sork and Boucher (1977), Sork (1983b), and Hubbard and McPherson (1997) found that squirr els and jays efficiently sorted nuts. Consequently, many damaged nuts are cached, and they can germinate in the spring if not recovered.

Several moth larvae infest the husks and cotyledons of nuts, including the hickory shuck-worm (Cydia caryana), the filbertworm (Melissopus latiferreanus), the pecan nut casebearer (Acrobasis nuxvorella), the navel orangeworm (Paramyelois transitella), and codling moths (Laspeyresia pomonella) (Moznette et al., 1940; Michelbacher & Ortega, 1958; Calcote et al., 1984; Nilsson, 1985; McGranahan & Leslie, 1991; Thompson & Grauke, 1991). Larval feeding early in the season causes nut abortion and can greatly reduce the size of the mature nut crop (Moznette et al., 1940; Michelbacher & Ortega, 1958). After the nutshell hardens, larval feeding is restricted to the husk, but the activity of these larvae indirectly affects nut quality by disrupting the flow of nutrients through the husk and into the nut during development. The kernels of pecans with infested husks weigh [approx]20% less than do uninfested nuts (Calcote et al., 1984). Furthermore, the damage caused by larvae delays nut development, accelerates the loss of moisture from the husk, and interferes with the natural abscission of the husk from the shell. This prevents the husk from dehiscing properly and may interfere with nut harvest and dispersal by vertebrates. Similar problems can be caused by walnut husk flies (Rhagoletis completa), which attack the nuts of Persian and black walnuts (Boyce, 1934; Michelbacher & Ortega, 1958).

A number of sucking insects feed on immature nuts. Examples include green stinkbug (Nezara viridula) and leaf-footed bug (Leptoglossus phyllopus) (Moznette et al., 1940). These insects begin to feed on nuts in the water stage and continue until the nuts are nearly mature. Early-season feeding kills the nut, but as the nuts mature, damage is relatively minor, consisting of dark, pithy regions in the cotyledons where nutrients have been depleted. Walnut aphids (Chromaphis juglandicola) suck juices from leaves, not fruits, but, when aphid infections are extensive, they can reduce the size and quality of the nut crop (Michelbacher & Ortega, 1958).

Nut-bearing plants are afflicted by a host of microbes, but only a few of these attack the nuts (e.g., Mirocha & Wilson, 1961). One of the indirect effects of insect damage to nuts is that they act as a vector for fungal, bacterial, and viral infections (e.g., Mehlenbacher, 1991). Rotten acorns and nuts (e.g., Gibson, 1971, 1972) are probably the result of the combined effects of insects and microbes. These microbes can cause a nut that has been slightly damaged by insects to become inviable or unacceptable to a vertebrate nut-dispersal agent.

A number of temporal and spatial patterns in nut infestation are evident from these studies. Geographical variation in the rate of nut infestation within years is considerable, with some populations experiencing heavy infestations while the same species in other regions is virtually untouched (Gibson, 1964, 1971, 1972). Some members of a population suffer heavy infestation, while others are only lightly affected (Gibson, 1971). And different oak species at one site often have widely differing levels of weevil infestation. For example, Quercus alba acorns at one site in Laurel County, Kentucky, had rates of infestation about seven times greater did than Q. stellata acorns (Gibson, 1964). Gibson (1964) found that weevil infestation rates were very low for acorns of the BO group compared with acorns of the WO group. Less than 1% of BO acorns were infested with weevils, whereas several species of the WO group were heavily infested. The proportion of nuts that escape infestation generally increases as the size of the nut crop increases (Brooks, 1922; Gibson, 1972), but Gibson (1971) found the reverse to be true of burr oak (Q. macrocarpa) acorns. In years of heavy nut crops, insects seem to do little more than to effect an unimportant thinning of the crop (Brooks, 1922).

Nut-bearing plants exhibit four traits that appear to reduce the impact of insects and microbes on the nut crop. First, plants are able to detect when a developing nut has been attacked by insects and quickly abort that nut (e.g., Michelbacher & Ortega, 1958; Boucher & Sork, 1979). This apparently has few detrimental effects on the development of the insect larvae, but it serves to conserve energy for other nuts or for tree growth or maintenance. Second, filling of the nut (the major share of energy investment in the embryo) does not begin in earnest until lignification of the shell has begun. The hardened shell prevents most late-season broods from feeding on the cotyledons. In nuts like hickories, pecans, and walnuts, late-season feeding is restricted to the husk, permitting embryo development to proceed, albeit with some disruption. Third, although insects and microbes appear to feed on nut tissue with impunity, the range of pests and the extent of their damage is probably reduced by the presence of tanni ns in the husks (hickories, walnuts, almonds) or in the cotyledons (acorns). Fourth, more nuts escape infestation when the nut crop is large. Annual variation of nut-crop size (discussed in greater detail in section XII) appears to be an essential element in the pest-management strategy of nut-bearing plants.

IX. Deterrence of Feeding by Vertebrates

As nuts mature during the summer and autumn, a host of birds and mammals often partake of the bounty (e.g., Reid & Goodrum, 1958). Nut-bearing plants confront an evolutionary conflict of interest: the nuts must be attractive to nut-caching rodents and corvids (e.g., squirrels, jays) that serve as potential agents of dispersal of the nuts while not being too attractive to a host of other animals (e.g., deer, pigs, grouse, turkeys, acorn woodpeckers) that serve only as predators of nuts. Furthermore, nuts must attract dispersal agents but not be so attractive that these agents of dispersal destroy all of the nuts. Making nuts differentially available to a range of foragers requires that the physical and chemical properties of the nuts and the ways in which they are packaged and presented to foragers be delicately balanced. Several features of nuts appear to be suited to this end.

The husks of several species of nuts are armed with bristly spines. Many species of Castanea and Castanopsis are among the best developed in this regard, having husks (cupules) that are so prickly that they are difficult for a human to handle without gloves. Several species of Corylus have the involucral bracts finely divided to produce a spiny bur that encloses the nut (Crane, 1989). Beechnuts and some species of Aesculus are enclosed in a husk with weak spines (Hardin, 1957; Elias, 1971). At least for Castanea and Castanopsis, these spiny husks are clearly a mechanism to discourage animals from foraging on the nuts; however, their effectiveness in deterring foragers has not been assessed quantitatively. One aspect of the behavior of these spiny husks seems, at first, to be at odds with their presumed protective role. At maturity, the husks or cupules of all of these species dehisce, and the nuts fall to the ground, where nut harvesters have easy access to them. This combination of traits seems designed to protect the nuts during development, when they are attractive and relatively nutritious food items but before they become viable propagules. Once critical stages in embryo development, provisioning of the cotyledons, and lignification of the shell have been achieved, the nuts are released from their spiny husk where their fate is determined by vertebrate foragers.

Among nut species that lack spiny husks, the husks are often impregnated with chemicals or are fibrous and tough, traits that deter some vertebrate foragers. Walnuts and hickories are examples. Like spines, these traits seem designed to reduce the efficiency of vertebrate foragers during early stages of nut development. However, their effectiveness in deterring vertebrate foragers has not been studied quantitatively.

The hulls of nuts range from soft and leathery (Quercus, Lithocarpus, Fagus, Castanopsis, Castanea, and Aesculus) to hard and woody (Carya, Juglans, Corylus, and Prunus). But even within a genus, shell characteristics may vary considerably, and these differences influence foragers' choice of nuts. For example, European jays readily eat the kernels of Q. rubra acorns but prefer whole Q. robur acorns to whole Q. rubra acorns because the husks of the latter are difficult for the jays to open (Bossema, 1979). Varieties of J. regia produce a range of shell morphologies from thick and very hard hulls (e.g., J. regia var. fallax) to thin and fragile hulls (e.g., J. regia var. duclouxiana) (McGranahan & Leslie, 1991). Some varieties of J. regia are referred to as "paper shells" because their shells are so thin. This species has been cultivated in central Asia for about 2000 years, but the variety of nut morphologies found in the wild does not appear to be the result of artificial selection.

The hull serves several general purposes with regard to vertebrate foraging. First, it acts as a barrier, preventing a portion of the granivore community from feeding on the nut meat. For example, the dense, woody hull of Juglans nigra effectively prevents all birds and weak-jawed mammals from eating the nuts. Only gnawing squirrels (e.g., Sciurus spp.) appear to have sufficiently strong jaws to break through the hulls. Second, hull characteristics influence the attractiveness of trees to potential dispersers (Smith & Follmer, 1972). If a tree produces nuts with very thin hulls, dispersers may eat all of the nuts, but if a tree produces nuts with very thick hulls, nut-caching animals may ignore the nut crop. Third, for those animals that can open the nut, the hardness of the hull requires that they invest a certain amount of time and energy handling the nut when they eat it. Jacobs (1992) hypothesized that the time it takes a forager to handle (shell and eat) a nut influences its likelihood of caching that n ut. Animals should cache those items that take longer to eat and should eat immediately those items that require less handling time. She found that the behavior of food-deprived gray squirrels was consistent with this hypothesis: they were more likely to eat hazelnuts without shells and to cache hazelnuts with shells. Hazelnuts with shells require 30% more handling time to eat than do those without shells, and it takes a squirrel less time to cache a nut than to remove the hull and eat it. The convoluted cotyledons of Juglans, which are surrounded by woody hull tissue, may have evolved as a result of this selection pressure. The cotyledons of J. nigra nuts, for example, are so time consuming to extract from the nut relative to acorns and other soft-shelled nuts (Smith & Follmer, 1972) that squirrels are deterred, to some extent, from eating them. However, this trait does not seem to discourage squirrels from caching walnuts. In situations where there are a variety of nuts with different hull characteristics, such as the eastern deciduous forest of North America, food-hoarding animals may be inclined to cache more hard-shelled nuts (e.g., hickories, walnuts) and to eat soft-shelled nuts (e.g., acorns, chestnuts). These differences in behavior may be especially apparent as the seasons change. Smith and Follmer (1972), for example, concluded that gray and fox squirrels prefer walnuts and hickory nuts in the autumn but that they feed primarily on acorns in the winter because they yield energy at a faster rate. By this and other means, the traits of nuts may act to promote tree diversity within the forest.

A number of nut-bearing plants appear to discourage nut consumption with phenolic compounds. The most important among these compounds in nuts are hydrolyzable and condensed tannins, key secondary metabolites present in the cotyledons. The role of tannins in plant tissues is a matter of some controversy (e.g., Haslam, 1988; Steele et al., 1993). This may be at least partially because tannins are highly variable in chemical structure (e.g., Zucker, 1983) and have different effects in different situations (Feeny, 1970; Fleck & Layne, 1990). Tannins may bind with proteins and other molecules and thereby interfere with digestion and the absorption of amino acids (Koenig & Heck, 1988; Koenig, 1991). Consequently, the amount of protein absorbed can be considerably less than the amount of protein present in the diet. Tannins can also bind to digestive enzymes and thereby reduce digestive efficiency of other types of foodstuffs, such as carbohydrates and lipids (Goldstein & Swain, 1965; Zucker, 1983). Furthermore, ta nnins can have a toxic effect on the digestive system, causing severe disability or even death when consumed in high concentrations. And finally, tannins impart a bitter flavor to nut meats, making them less palatable to animals and causing animals to eat less of that food (Haslam, 1988; Servello & Kirkpatrick, 1989; Steele et al., 1993).

Animals have a limited ability to neutralize the effects of tannins, but those animals whose diets are high in tannins often have a greater ability to counter the effects of tannins (Martin & Martin, 1984). For example, Robbins et al. (1987) found that the saliva of mule deer has a greater tannin-binding capacity than does the saliva of sheep and cattle, which have lower levels of tannins in their diets.

Acorns, particularly those of the BO group, are sufficiently high in tannins to cause reduced digestive efficiency in some of the birds and mammals that have been tested. As noted in section VI, high tannin levels in acorns are correlated with high lipid content. This creates a problem for foragers that attempt to select nuts in order to maximize energy gain per unit of foraging effort. Animals that attempt to obtain the energetic lipids in BO acorns must pay a metabolic cost in handling the high tannin levels. Yellow-necked field mice (Apodemus flavicollis), white-footed mice (Peromyscus leucopus), and red squirrels (Sciurus vulgaris) are unable to maintain body mass on a diet of acorns (Drozdz, 1968; Briggs & Smith, 1989; Kenward & Holm, 1993). Even when acorns are abundant, red squirrels are unable to eat more than four to six acorns per day (Wauters et al., 1992). Acorn woodpeckers (Melanerpes formicivorus), an acorn specialist, lost 6% of their body weight when fed high-tannin, high-lipid coast live oak (Quercus agrifolia) acorns for two weeks but were able to maintain their body weight on diets of either low-tannin, low-lipid valley oak (Q. lobata) or canyon live oak (Q. chrysolepis) acorns (Koenig & Heck, 1988). Koenig (1991) found that high lipid content exacerbates the detrimental effects of tannin for acorn woodpeckers. Scrub jays were unable to maintain their body weight on either Q. agrifo1ia or Q. lobata acorns (Koenig & Heck, 1988). Despite the greater potential nutritional value of Q. agrifolia acorns, the subjects received less nutritional benefit from them, presumably because of the digestive interference of the tannins. Scrub jays can maintain body mass on a high tannin diet only if protein levels are also high (Fleck & Tomback, 1996). Blue jays (Cyanocitta cristata) cannot maintain body mass on either BO or WO acorns (Johnson et al., 1993; Dixon et al., 1997a). Steele et al. (1993) found that the tannins in willow oak (Q. phellos) and other species of acorns are concentrated around the embryo in the apical end of the acorn and that gray squirrels, blue jays, and grackles (Quiscalus quiscula) avoid most of the tannins by eating the basal half of the acorns and discarding or caching the apical portion. The tannin levels in other types of nuts do not seem to be sufficiently high to cause digestive problems in animals.

In an effort to explain how nut-caching animals can specialize on acorns whose tannins interfere with digestive efficiency to the extent that foragers cannot maintain body mass, some researchers have suggested that these animals supplement their acorn diets with weevil larvae and other insects that infest the acorns (Johnson et al., 1993). An important implication of this hypothesis is that weevil larvae, rather than damaging oaks, actually benefit oak regeneration over the long term. In support of this hypothesis, blue jays that lost mass on an ad lib pin oak acorn diet were able to maintain weight when fed acorns plus 5 g of weevil larvae per day (Johnson et al., 1993). Weevils represent a significant dietary supplement for free-ranging gray squirrels (Steele et al., 1996). However, in a direct test of this tritrophic relationship among jays, weevils, and oak trees, Hubbard and McPherson (1997) found no evidence that Mexican jays (Aphelocoma ultramarina) preferentially selected weevil-infested acorns. Sork and Boucher (1977) and Semel and Andersen (1988) also found that foraging rodents prefer to feed on uninfested nuts.

A number of studies have examined the preferences of animals for various types of nuts and acorns. These studies seek to discern the interaction among the benefits that accrue from the nutritional qualities of nut meats (e.g., lipid, protein, tannin content), the costs of foraging imposed by the hull on handling time, and the dormancy/germination schedules, which affect the suitability of nuts for long-term storage. The available results do not point to any simple answers to these questions. For example, Smith and Follmer (1972) found that gray and fox squirrels preferred black walnut and shagbark hickory nut meats over acorn nut meats and Quercus shumardii (BO) and Q. macrocarpa (WO) acorns over Q. alba (WO) acorns. These preferences were correlated with lipid content of the nuts but not the rate of ingesting metabolizable energy from whole nuts. Lewis (1982) reported similar results. In contrast, Short (1976) found that fox squirrels preferred the low-lipid, low-tannin acorns of the WO group. In an attempt to disentangle the potentially confounding effects of lipid content, tannin content, and other attributes of nut packaging and physiology, Smallwood and Peters (1986) studied the preferences of gray squirrels using dough balls (artificial "acorns") derived from chestnut oak (WO) acorn meal. They found that adding tannins to dough balls decreased the time squirrels spent feeding on them and that adding lipids to dough balls attenuated the effect of the tannins. They concluded that gray squirrels did not select food to maximize daily energy intake and that tannins at the level used in the experiment had no effect on the digestion of proteins.

A possible explanation for the lack of short-term (e.g., daily) energy maximization in gray squirrels is that their behavior has evolved to maximize energy over a longer time (i.e., during the fall and winter) (Smallwood & Peters, 1986). BO and WO acorns differ in perishability as well as in lipid and tannin content. BO acorns have enforced dormancy during the winter months and do not germinate until spring. WO acorns, on the other hand, germinate soon after falling in the autumn. Once acorns germinate they become less nutritious and less attractive to squirrels. If cached, WO acorns will germinate and rapidly translocate much of their energy and reserve materials from the cotyledons into the woody taproot, leaving the acorn devalued (Fox, 1982). Smallwood and Peters (1986) suggested that squirrels could maximize their long-term energy gain if they ate WO acorns in the autumn and stored the less perishable BO acorns for use later in the winter and spring. The caching of nuts has no effect on tannin levels; t hat is, tannins are not leached from acorns during storage (Dixon et al., 1997a; Koenig & Faeth, 1998). Consequently, the preferences of squirrels in the autumn cannot be predicted directly by their lipid and tannin levels; instead, they are related to germination schedules, for which lipid and tannin may serve as a cue. However, there seem to be few data on the propensity of squirrels or jays to bury versus eat BO and WO acorns under field conditions.

X. Husk Dehiscence and Nut Fall

Most species of nuts develop inside a fleshy husk that is adapted in some way to release the nut at maturity (e.g., Hagerup, 1942). In all members of Carya, Fagus, Castanea, Castanopsis, and Aesculus and in one species of Juglans, the husk splits at maturity, exposing the nut. Sparks and Yates (1995) describe the process of husk abscission in Carya illinoinensis (pecan) as occurring in three phases. First, the inner lining of the husk separates from the surface of the shell, starting at the distal end of the nut. Second, the margins of the valves abscise, again beginning at the distal end of the nut, splitting the husk into four valves. As the valves separate, the distal end of the nut becomes visible. Third, the vascular tissue separates from the inner lining of the husk, beginning at the proximal end of the nut. Following these events, the husk rapidly dries out, shrivels, and turns brown. Nuts may remain loosely attached at the base to the husk, but they usually fall to the ground within a day or so.

Nut drop is a nearly universal trait of nut trees. The behavior is consistent with the fact that most important dispersers of nuts are ground-foraging rodents and corvids. Nut drop usually occurs over a period of several weeks (Downs & McQuilkin, 1944; Boucher & Sork, 1979; Lewis, 1982). Before nuts are ripe and when competition for nuts is intense, animals harvest many nuts from the tree canopy before they have a chance to fall. Also, because of the selective removal of filled nuts from the ground, the quality of nuts in the tree canopy is often better than that on the ground (e.g., Sork, 1983b; Teclaw & Isebrands, 1986).

XI. Nut Dispersal

Food-hoarding animals engage in either larder hoarding or scatter hoarding (Vander Wall, 1990). Larder hoarding occurs when animals place many food items in one or a few sites, typically in or near their nest burrow deep belowground or in a hollow tree or log. Larders are usually poor sites for the emergence and establishment of seedlings, so this form of storage usually ends in nut death (but see Olmsted, 1937, for an exception). Scatter hoarding occurs when animals bury one or a few items at many widely dispersed sites. These sites are usually prepared from the ground surface, the caching animal usually burying items 1-50 mm deep in soil or under plant litter. Sometimes caches occur in the walls of shallow rodent burrows (e.g., Jensen, 1985; pers. obs.). An advantage of scatter hoarding is that the hoarder need not aggressively defend the stored food and is free to engage in other activities. However, the lack of physical defense means that food is vulnerable to pilferage. To minimize this possibility, foo d hoarders typically do two things. First, they are very adept at hiding food so that it cannot be detected easily by a naive forager. Inspection of cache sites by a human seldom reveals any trace of digging or disturbance of the ground surface. Second, food items are spaced sufficiently far apart that the discovery of a buried food item by a naive forager is not likely to lead to the discovery of other buried items nearby. The optimal spacing of caches is thought to be a compromise between minimizing energy and time investment by the animal in transporting items to distant sites and maximizing the number of stored items that the cacher can eventually retrieve (Stapanian & Smith, 1978, 1984; Clarkson et al., 1986; Tamura et al., 1999). Relocation of hidden seeds and nuts by the cacher is possible because of the hoarder's extensive spatial memory of cache sites (Bossema, 1979; Vander Wall, 1982, 1991; Kamil & Balda, 1985; Jacobs & Liman, 1991; Macdonald, 1997), although, for rodents, olfaction may also be impo rtant (Cahalane, 1942; Richards, 1958; Jennings, 1976; Thompson & Thompson, 1980; Vander Wall, 1998, 2000).

Animals can quickly remove a nut crop from beneath productive trees (e.g., Brown & Yeager, 1945; Linsdale, 1946; Cypert & Webster, 1948; Tanton, 1965; Ashby, 1967; Shaw, 1968a, 1968b; Sork & Boucher, 1977; Heaney & Thorington, 1978; Monk, 1981; Sork, 1983b; Kikuzawa, 1988; Miyaki & Kikuzawa, 1988; Borchert et al., 1989; Wastljung, 1989; Pigott et al., 1991; Scarlett & Smith, 1991; Quintana-Ascencio et al., 1992; Crawley & Long, 1995; Herrera, 1995; Sone & Kohno, 1996; but see Sork et al., 1983, for an exception), although there are surprisingly few quantitative data on nut harvest rates. During the harvest, vertebrate foragers are usually proficient at discriminating between filled and empty or insect-infested nuts and scatter hoard mostly filled nuts (Dennis, 1930; Mailliard, 1931; Bossema, 1979; Johnson & Adkisson, 1985; Weckerly et al., 1989a; Dixon et al., 1997b), but in some cases they also store many spoiled nuts (e.g., Stiles & Dobi, 1987). Foragers often prefer large nuts (e.g., Bossema, 1979; Jensen , 1985), but some species prefer small nuts (e.g., Scarlett & Smith, 1991). The quantities of nuts scatter hoarded can be prodigious. Kallander (1978), for example, estimated that a population of 100-150 rooks (Corvus frugilegus) stored 36,000-50,000 Persian walnuts in southern Sweden during a 20-day harvest period, and Chettleburgh (1952) estimated that 35 European jays in Hainault Forest, England, stored 63,000 acorns during a 10-day period at the peak of the harvest. The total number of nuts scatter hoarded is often much greater than these examples illustrate, because the nut harvest generally begins before the nuts are completely ripe and continues until all of the nuts are stored or until winter snows accumulate. Johnson and Adkisson (1985) calculated that a population of blue jays transported 100,000 beechnuts from a woodlot in Wisconsin during a 27-day harvest period. Darley-Hill and Johnson (1981) found that blue jays ate 20% of a Quercus palustris acorn crop and cached 54% of the crop. Weevils destro yed most of the rest of the acorns.

Ecologists have made few quantitative estimates of the number of nuts that rodents cache. Wauters and Casale (1996) estimated that red squirrels (Sciurus vulgaris) in Belgium stored 1.2-1.4 acorns or beechnuts per minute, spent 1920-2050 minutes hoarding food between September and January (4.7-6.7% of their active time), and stored 2323-2768 items each fall. Pigott et al. (1991) used energetic requirements to estimate that gray squirrels require 5400-7200 Quercus robur acorns to fulfill their metabolic needs from September through April. Because squirrels cannot survive on a diet of acorns alone (e.g., Wauters & Casale, 1996), these estimates are probably high. Nevertheless, most of these acorns consumed during this period come from caches.

Most cached nuts are eventually recovered by vertebrates (e.g., Cahalane, 1942; Swanberg, 1951, 1981; Sone & Kohno, 1999; Tamura et al., 1999). Animals use stored nuts for sustenance during the autumn, and winter. Thompson and Thompson (1980), for example, found that rodents removed 85% of a population of 500 experimentally buried horse chestnuts. Of the remaining nuts, 3% spoiled and 12% appeared healthy at the time of germination. Thompson and Thompson (1980) obtained similar results for a smaller sample of rodent caches, However, these and similar data cannot be used uncritically to estimate nut survival rates. Many of the nuts that animals remove from caches are recached elsewhere (Cahalane, 1942; DeGange et al., 1989; Vander Wall & Joyner, 1998; Sone & Kohno, 1999; Vander Wall, 2000), so overall nut survival rates may be considerably higher.

Those stored nuts that are not recovered by animals can germinate as the environment warms in the spring. Several aspects of the behavior of nut-caching animals are potentially beneficial to the nuts that are overlooked. First, animals transport nuts away from source plants. Fallen nuts under a tree or shrub constitute a concentrated food source, where density-dependent mortality is high (e.g., Janzen, 1971; Sork, 1983b). Seed-caching animals respond to these rich food sources by scattering nuts throughout the environment to achieve a lower density and more uniform distribution of nuts as a means of protecting them from competitors (Stapanian & Smith, 1978; Hoshizaki et al., 1997). Dispersal distances range up to about 100 m for squirrels, chipmunks, mice, and other rodents (Stapanian & Smith, 1978; Sork, 1984; Jensen, 1985; Kato, 1985; Jensen & Nielsen, 1986; Stiles & Dobi, 1987; Vander Wall, 1992; Iida, 1996; Sone & Kohno, 1996; Tamura & Shibasaki, 1996; Hoshizaki et al., 1997; Vander Wall & Joyner, 1998; Tamura et al., 1999) but can be several kilometers for corvids (Schuster, 1950; Swanberg, 1951; Chettleburgh, 1952; Kallander, 1978; Bossema, 1979; Purchas, 1980; Darley-Hill & Johnson, 1981; Johnson & Adkisson, 1985). Nearest-neighbor distances between caches are usually several meters (Stapanian & Smith, 1978; Jensen, 1985).

A second advantage of dispersal by nut-hoarding animals is that they bury the nut. As seed size increases, the probability of burial by physical processes rapidly diminishes (Chambers et al., 1991). Burial is a critical step in the regeneration process, and rodents and corvids provide a quick and effective solution. Burial greatly reduces the probability of seed predation by animals such as insects, deer, wood pigeons, chickadees, and turkeys, which act strictly as nut predators (Kautz & Liming, 1939; Downs & McQuilkin, 1944; Higuchi, 1977; Borchert et al., 1989; Crawley & Long, 1995; Herrera, 1995), although some animals, like wild boars, javelina, and pocket gophers are important predators of buried acorns (Griffin, 1971; Borchert et al., 1989; Herrera, 1995). More deeply buried nuts experience lower rates of removal (Watt, 1923; Cahalane, 1942; Barnett, 1977; Bossema, 1979; but see Sork, 1983a). Burial also provides an environment where the viability of nuts can be maintained for a longer period (Griffin, 1971; Jensen, 1985). Acorns on the surface of the ground can be damaged by heat and desiccation (Crow, 1988). If the water content of white oak acorns and chestnuts falls below a certain critical level they lose viability (Korstian, 1927; Gosling, 1989; McCreary, 1989; Finch-Savage, 1992). Successful seed germination requires sustained high moisture content, which becomes increasingly difficult as seed size increases because of diminishing ratio of surface area to volume (Watt, 1919; Shaw, 1968b; Harper et al., 1970). Prompt caching in soil maintains high water content in the embryo and cotyledons. The lack of desiccation tolerance of some acorns and chestnuts can be viewed as a measure of how much these nuts are dependent on animal caching.

Burial also ensures good rooting (Griffin, 1971; Sork, 1983a). Acorns lying on the ground surface can germinate and root, but the probability of establishment is low (Griffin, 1971; Borchert et al., 1989; Nyandiga & McPherson, 1992). Cache depth (at the top of the nut) usually ranges from a few millimeters to several centimeters (e.g., Sviridenko, 1971; Sone & Kohno, 1996, 1999) but has seldom been quantified under natural conditions. Very shallow cache depths (i.e., partially exposed nuts) have been reported (Cahalane, 1942; Thompson & Thompson, 1980; Stiles & Dobi, 1987) in artificial landscapes with compacted soils (e.g., cemeteries, parks, campuses), but cache depths at these sites may not be typical of more natural situations. Acorns buried about 1-5 cm deep generally have the highest probability of establishment (Korstian, 1927; Barrett, 1931).

A third benefit of scatter hoarding is that animals often cache nuts in habitats and microhabitats that favor establishment. Animals often transport acorns and nuts from late-successional, closed-canopy forests to early-successional habitats, such as old fields, disturbed areas, and pine forests (Darley-Hill & Johnson, 1981; Sork, 1983a; Harrison & Werner, 1984; Nilsson, 1985; Paillet & Rutter, 1989; Deen & Hodges, 1991; Johnson et al., 1997; Hoshizaki et al., 1999). One reason for this is that animals can avoid or reduce pilferage of caches by moving nuts out of the forest, where many nut-eating animals live and actively search for nuts (Bossema, 1979; Darley-Hill & Johnson, 1981; Sork, 1983a; Stapanian & Smith, 1986). The greater the value of the nut to the hoarder (e.g., energy or nutritional reward per unit of handling time), the more likely it is that the rodent or corvid will move the nut out of the environment where it was harvested. Stapanian and Smith (1986) found that more valuable black walnuts we re dispersed farther into prairie habitat by fox squirrels than were less valuable acorns. If these nuts survive to the time of germination, they have a high probability of establishing and colonizing a new area. Seedlings in open habitats often experience less competition with mature woody plants and more favorable light environments (Crow, 1988).

XII. Mast Seeding: Annual Variation in Nut Production

Mast seeding is the periodic, synchronous production of large seed crops. Most nut-bearing species produce large crops of nuts at intervals of two to five years, with intermediate or small crops produced in the interim (Waller, 1979; Silvertown, 1980; Kelly, 1994). Large nut crops rarely occur in consecutive years; small nut crops seldom occur in consecutive years but are separated by average or very productive years (Christisen & Korschgen, 1955; Goodrum et al., 1971; Gysel, 1971; Gemoets et al., 1976; Beck, 1977; McQuilkin & Musbach, 1977; Nielsen, 1977; Carmen et al., 1987; Sork et al., 1993; Wood, 1993; Koenig et al., 1994; Chung et al., 1995). Large crops are typically 100-1000 times larger than small crops. For example, annual variation in beechnut production in Belgium ranges from 0.83 to 1273 nuts/[m.sup.2] (Wauters & Casale, 1996). In some data sets, there appears to be periodicity ("cycles") in nut production. For example, over an eight-year period, Quercus rubra produced large crops at four-year i ntervals; black oak (Q. velutina), at two-year intervals; and Q. alba, at three-year intervals (Sork et al., 1993). Over longer periods, however, the timing of large crops of nuts is rarely so regular. Pecans, for example, produced large crops at 2- to 7-year intervals over a 66-year period (Chung et al., 1995). Different tree species may produce nut crops in synchrony (Koenig et al., 1996; Koenig & Knops, 2000), but nut crops are generally asynchronous among species (e.g., Christisen, 1955; Goodrum et al., 1971; Koenig et al., 1991, 1994).

Patterns of variation in nut production are probably the result of interactions between intrinsic (i.e., genetically controlled) physiological processes of the plants and environmental factors. A strong genetic influence is suggested by the consistently good or poor performance of individual plants that appears to be unrelated to site conditions (e.g., soil, slope, aspect) or tree size (Downs & McQuilken, 1944; Christisen, 1955; Gysel, 1956; Sharp & Sprague, 1967; Goodrum et al., 1971; Farmer, 1981; McCarthy & Quinn, 1989, 1992). The physiological basis of variable nut production has not yet been identified. It appears to be related not to periodicity in pistillate flower production but to variation in the rate of abortion of pistillate flowers and developing fruits (Williamson, 1966; Sparks & Heath, 1972; Farmer, 1981; Stephensen, 1981; Feret et al., 1982; Sork, 1983c; Sparks & Madden, 1985; McCarthy & Quinn, 1989; Crawley & Long, 1995). The fact that plants within a local population and even across large g eographical regions usually produce large crops in synchrony indicates that the environment plays a role in setting the timing of large nut crops (Koenig et al., 1996). A large number of proximate factors are likely to be involved. For example, Sharp and Sprague (1967), Sork et al. (1993), and Koenig et al. (1996) found that large crops of WO acorns were correlated with warm temperatures in April, which was the critical period for pollination and ovule fertilization. In two species of California live oaks (Quercus agrifolia and Q. chrysolepis), acorn production was correlated with rainfall prior to acorn production (Koenig et al., 1996). A killing frost during flowering can decimate an acorn crop (Gysel, 1956; Sharp & Sprague, 1967; Goodrum et al., 1971; Nielsen & Wullstein, 1980), high humidity during flowering will reduce fruit set of bear oak (Q. ilicifolia) (Wolgast & Stout, 1977), and water stress during fruit maturation will reduce pecan production (Garrot et al., 1993).

Several non--mutually exclusive hypotheses have been offered to explain the adaptive significance of mast seeding. First, the synchronous, mass production of flowers increases the probability of cross-pollination (Nilsson & Wastljung, 1987; Smith et al., 1990; Sork, 1993; Koenig et al., 1994). Most nut-bearing plants are self-incompatible; self-pollination usually results in empty or undeveloped nuts (e.g., McKay, 1942; Lagerstedt, 1977). The probability of successful pollination and fruit set increases with flower density on conspecific plants. Nilsson and Wastljung (1987) reported 86-94% filled beechnuts during mast years and only 76% filled nuts during nonmast years. It appears to be advantageous for individuals to produce large numbers of flowers when conspecifics are producing large number of flowers. However, Sork (1993) and Koenig and Knops (in press) did not find evidence that oaks had evolved masting in response to pollination efficiency.

Second, the predator-satiation hypothesis suggests that marked annual variation in nut production serves to reduce loss of nuts to specialist insect predators (Silvertown, 1980; Ims, 1990; Koenig et al., 1994). During poor-nut-crop years, insect populations decline because of insufficient resources. Because of their more restrictive food requirements, insects are more vulnerable to temporal shortages of nuts than are vertebrate nut-dispersal agents (Silvertown, 1980; Nilsson, 1985). Then, when plants produce large crops of nuts, the insect predators do not have sufficient time to build up populations to fully exploit the nut crop. Consequently, a larger number of nuts escape predation by insects during mast years. The proportion of a nut crop destroyed by insects either remains nearly constant (Sork, 1983c) or, more often, decreases as the size of the nut crop increases (Beck, 1977; Silvertown, 1980; Nilsson & Wastljung, 1987; Crawley & Long, 1995). However, variation in nut production is not as effective in reducing insect predation on nuts as it might otherwise be because some insects can counteract the plants' defensive measures by producing several generations during mast years, permitting a relatively rapid increase in population size (Busing, 1931; Moznette et al., 1940; Michelbacher & Ortega, 1958), by switching to alternative foods of the same plant species (e.g., twigs, buds) during nonmast years (Brooks, 1922), and by having a portion of the overwintering brood remain dormant for two or more years to bridge short gaps in food supply (Moznette et al., 1940; Dohanian, 1944). The latter phenomenon may result in strong selection on plants for irregular (rather than cyclical) mast production, making it more difficult for insect predators to track nut crops over time.

A third hypothesis, which is a variation of the predator-satiation hypothesis, is that masting increases the number of nuts scatter hoarded and the proportion of those nuts that survive to germinate (Boucher, 1981; Jensen, 1982, 1985; Nilsson, 1985; Smith et al., 1990; Wolff, 1996). Many food-hoarding animals respond to excess food items by hiding them quickly. Unlike feeding, hoarding behavior is not readily satiated. Consequently, when confronted with an abundance of food, animals will typically bury all of the items available even if this is several times more than they could possibly consume (Tomback, 1982; Vander Wall, 1988). The reasons for this overstorage may include the inability of animals to accurately predict how much food they will need to survive the winter and the uncertainty of how much of their stored food will be pilfered by other animals or spoiled by microbes. Overstorage is insurance against environmental uncertainty. Plants exploit this uncertainty when they produce mast crops. Large nu t crops may even promote longer mean dispersal distances if animals are selected to bury nuts at a constant density (Stapanian & Smith, 1978), but this has not been demonstrated. Under these conditions, a disproportionately large number of scatter hoarded nuts survive the winter and germinate in the spring.

A number of other hypotheses have been proposed to explain masting, but they have received little support. For example, there is little support for the notion that the variation in nut production simply reflects fluctuations in the availability of resources from year to year (i.e., resource tracking) (Koenig et al., 1994; Koenig & Knops, in press). There is no support for the hypothesis that the weather conditions that serve as proximate cues for the production of mast crops also predict optimum future conditions for reproductive growth and seedling establishment (Smith et al., 1990). Nor is there support for the

hypothesis that individual trees within a population vary their reproductive effort over time as a means of competing for animal dispersal agents (Koenig et al., 1994), although it seems reasonable that different species of trees may mast in different years in order to avoid competition for dispersers (e.g., Nilsson, 1985).

The weight of the evidence suggests that masting is an evolved strategy of nut-producing plants to minimize the loss of propagules to specialist insect seed predators and to increase the effectiveness of nut dispersal by scatter hoarding rodents and corvids. During masting, plants deplete their nutrient resources, sacrificing growth in favor of reproduction (Koenig & Knops, 1998). As one might predict, plants achieve disproportionately high rates of seedling establishment in mast years (Watt, 1923; Crawley & Long, 1995; Wolff, 1996; Hoshizaki et al., 1997). In contrast, during nonmast years, virtually no seedlings become established (Downs & McQuilkin, 1944; Sork & Boucher, 1977; Jensen, 1985). The fact that different nut-producing species usually produce large crops out of synchrony has important implications. Nut dispersers can have strong preferences for certain nut species. In years when two or more nut-bearing species produce large crops, the plants may compete for dispersers. For example, Quercus robur and Q. pet raea appear to compete with Fagus silvatica for the dispersal services of European jays in southern Sweden (Nilsson, 1985). When oaks and beech produce large nut crops during the same year, jays largely ignore the beech and, instead, harvest and cache acorns (Bossema, 1979; Nilsson, 1985). Only when large beech crops are produced in years of low acorn production do beechnuts receive the dispersal services of the jays. In those years, beechnuts are transported greater distances and into other habitats (e.g., coniferous forests). In the following spring, large numbers of beech seedlings are observed outside the beech forest. The best years for nut dispersal may be those in which a species produces large crops and the nuts of more preferred species are unavailable. Consequently, the preferences of important nut dispersers may create a selective environment that causes less-preferred nut species to use different environmental cues to determine the timing of mast production in order to avoid masting in the same year as a competing species.

XIII. Nut Dormancy and Germination

Most nuts lack long-term dormancy. Under laboratory conditions, for example, most Quercus rubra acorns break innate (inherent) dormancy after about 6-8 weeks of cool (5[degrees]C), moist stratification, although some acorns of this species germinate with 0-4 weeks of stratification (Hopper et al., 1985). Seedlings from Q. rubra acorns that had been stratified for 8-12 weeks grew faster and taller than did those stratified for 0-4 weeks, indicating that afterripening changes occur within the acorn that prepare the embryo for more rapid growth (Hopper et al., 1985). Removal of the pericarp of freshly collected Q. rubra acorns increases the germination percentage of acorns, suggesting that the pericarp of acorns plays a biochemical or physical role in regulating dormancy. In Corylus avellana the seed coat (testa) and the pencarp release inhibitors (probably abscisic acid) that travel via the cotyledons to suppress development of the embryonic axis (Bradbeer, 1968; Jarvis, 1975; Shannon et al., 1983). Chilling o f intact hazelnuts gradually activates gibberellin synthesis, which initiates germination (Ross & Bradbeer, 1968).

About two months of cool, moist conditions are needed to break dormancy in most species of nuts in temperate climates. Under field conditions, dormancy is enforced for longer periods (four to six months) by cold ambient temperatures, usually until conditions ameliorate in the spring. With the breaking of dormancy, the cotyledons imbibe water; the water passes into the axis of the seed, which swells and elongates. In Quercus robur this process appears to be triggered by the decline of abscisic acid in the embryonic axis (Finch-Savage & Clay, 1994). Growth of the axis is directed toward the apex of the fruit, where the radicle (future root) pushes against and breaks through the pericarp. The shell of some nuts has a weak zone near the apex that splits during germination (e.g., Hagerup, 1942). The tip of the radicle is positively geotropic, so it grows downward once it is outside the nut.

Most nuts germinate whether or not other conditions (e.g., light) are appropriate for establishment. This behavior is in marked contrast to most small seeds, which can remain dormant for many years and which break dormancy only under conditions that seem to favor seedling establishment. The reason for the lack of multiyear dormancy in nuts may be that the probability of nut predation is so great that the likelihood of a nut surviving a second year is negligible (Thompson, 1987). Also, nuts lose viability rapidly, and the embryos die if they do not germinate quickly. Under these conditions, the best strategy for nuts is to germinate at the first opportunity.

Acorns of the WO group and a few other types of nuts (e.g., Florida scrub hickory [Carya floridana] [McCarthy & Bailey, 1992]) have taken this strategy to an extreme by having virtually no dormancy at all. These nuts mature early in the autumn and germinate within days or weeks of maturity, sometimes while still on the trees or often while lying on the ground under the parent tree (Griffin, 1971; Barnett, 1977; Fox, 1982; Matsuda & McBride, 1986). The high water content of WO acorns (Table II) may have evolved to facilitate fall germination. Most of the unharvested acorns that germinate die within a few days because their roots are usually unable to penetrate the litter layer. But if nuts dry out on the ground, they will rapidly lose viability. WO acorns appear to require prompt burial in soil, an environment that prevents desiccation and maintains viability. If an animal caches an acorn quickly, the acorn can germinate successfully while the weather is still favorable in the autumn. The storage products in the cotyledons are rapidly translocated through the petioles to a swollen taproot positioned deep below the acorn (Lewis, 1911). The epicotyl or shoot, on the other hand, does not elongate and remains belowground. Once the nutrients have been translocated to the taproot the petioles weaken. In a sense, the seedling abandons the acorn as quickly as possible. In the event that an animal retrieves the acorn, the petioles break with little damage to the seedling. In addition, the first true leaves that emerge in spring are atypical for oaks (Lewis, 1911). It is possible that these atypical leaves serve to camouflage the emerging plant from animals that browse on oak seedlings.

Gray squirrels have evolved behaviors that counteract the autumn germination of WO acorns. Before squirrels cache acorns of the WO group, they often bite into the acorn and excise the embryo, thus preventing germination (Wood, 1938; Fox, 1982; Pigott et al., 1991). The tissue around the embryo is relatively low in tannins, leading some researchers to suggest that the squirrel is not actively removing the embryo but just feeding on the most nutritious portion of the acorn before storing it. But energetic estimates (Fox, 1982) and the fact that squirrels do not excise the embryos of acorns of the red oak group or any other types of nuts that remain dormant suggests that excision of the embryo is the ultimate reason for this feeding behavior. However, the behavior is not uniform across the squirrel population, and some adults and most immature squirrels fail to excise the embryos of most of the WO acorns they cache (Fox, 1982; Pigott et al., 1991). Thus, many WO acorns are successful in escaping postdispersal s eed predators.

The loss of long-term dormancy of nuts may have contributed to the fact that nut-bearing plants are long-lived, perennial woody plants. In a temporally variable environment, dormant seeds provide a means by which annual plants can survive from one period of favorable conditions to another even if these periods are separated by many years. The loss of seed dormancy is likely to occur only if another stage of the plant's life cycle is able to ensure the survival of individuals over long periods of unfavorable conditions. This is accomplished by long-lived trees (e.g., Quercus, Juglans, Carya, Fagus) and by shrubs that can propagate themselves by vegetative reproduction (i.e., Corylus, Prunus). This may help explain why most short-lived forbs do not produce very large seeds.

As I noted above, nuts exhibit great intraspecific variation in size, and this variation has important implications for germination. Larger nuts within a species usually have a higher probability of germination and germinate earlier and with greater vigor than do small nuts (Korstian, 1927; Tripathi & Khan, 1990; Tecklin & McCreary, 1991; Bhagat et al., 1993).

With the exception of Fagus, the nuts considered here have hypogeal germination (i.e., the cotyledons remain belowground). The wind-dispersed relatives of nut genera have smaller seeds and usually exhibit epigeal germination (i.e., with aboveground, photosynthetic cotyledons) (Stone, 1973, 1989). It is generally advantageous to seedlings to have the cotyledons serve as photosynthetic surfaces. The apparent evolutionary transition to hypogeal germination in nuts occurred for two reason. Because nuts are often buried deeply by animals, it is difficult for the elongating embryo axis to push the nut upward through the soil. Consequently, hypogeal germination of nuts could result simply because of increased resistance to movement through soil as nuts evolved larger size. But it is also advantageous for the seedling to keep the cotyledons hidden belowground. If the nutrient-filled cotyledons were deployed aboveground, foraging animals might remove them, damaging or perhaps killing the seedling. Animals are known t o feed heavily on recently germinated seedlings soon after they emerge through the soil (e.g., Cahalane, 1942; Barnett, 1977; Bossema, 1979; Sonesson, 1994), and this damage would probably be worse if the cotyledons were epigeal.

XIV. Seedling Establishment

In temperate regions, seedling emergence occurs from late February to May, depending on climate. Usually only a small proportion of nuts produced in the autumn survive to the seedling stage. For example, the density of Fagus grandifolia nuts in a mast year at Hubbard Brook Experimental Forest, New Hampshire, was 59/[m.sup.2], and seedling production the following spring was 2.2/[m.sup.2], a survival rate of 3.7% (Hughes & Fahey, 1988). Seedling production of Quercus petraea in Wales ranged from 0.3 to 1.5% of filled acorns (Shaw, 1968a, 1968b), and, for Aesculus turbinata in Japan, it ranged from 0.8% to 6.6% (Hoshizaki et al., 1997).

The size of nuts has been found to influence strongly the growth of seedlings (Seiwa & Kikuzawa, 1991). Larger pecans produce taller seedlings (Adams & Thielges, 1979), and larger Indian horse chestnuts (Aesculus indica) have larger seedlings and increased rates of survival (Bhagat et al., 1993). Seedling attributes such as total leaf area, shoot height, shoot diameter, root-system development, and total plant mass at the end of the first growing season all vary in proportion to acorn mass in oaks (McComb, 1934; Jarvis, 1963; Reich et al., 1980; Tripathi and Khan, 1990; Bonfil, 1998). Korstian (1927) found that large Quercus rubra, Q. velutina, Q. alba, and Q. montana acorns produce seedlings with greater percent survival, seedling height, shoot and root mass, and stem diameter at the end of the first growing season relative to medium and small acorns. Removal of cotyledons of oaks and A. turbinata at various times during early seedling growth demonstrates that nutrients in cotyledons are essential for seedl ing establishment but become less important as the seedling ages (Korstian, 1927; Ovington & MacRae, 1960; Brookes et al., 1980; Hoshizaki et al., 1997; Bonfil, 1998). However, Sonesson (1994) reported that by the time Q. robur seedling leaves appear, removal of the acorn has no measurable effect on growth and survival, even though considerable nutrients remain in the cotyledons. One reason for the apparent independence of young seedlings from the acorn in this species is that root development is well under way before the shoot appears aboveground and that the cotyledons may be used primarily for initial development of roots rather than for the shoot (Grime & Jeffrey, 1965). Once the leaves appear in Q. rubra seedlings, current photosynthate makes most of the contribution to the growth of seedlings (Dickson et al., 1990).

The likelihood of successful seedling establishment from Quercus alba and Q. rubra acorns and Juglans regia walnuts is influenced by the orientation of the nut in the soil (Korstian, 1927; Lal et al., 1984). Nuts buried with the embryo oriented vertically and with the radicle pointed downward have the highest probability of seedling establishment; nuts buried with the radicle pointed upward have the lowest likelihood of establishment.

Many factors contribute to seedling failure. The four most prevalent are drought, light conditions, browsing, and competition with other plants. Drought can cause reduced rates of growth or seedling death. For example, drought can reduce photosynthesis by 70-90% in Quercus rubra (Crow, 1988). Desiccation is most likely to be a problem for seedlings growing in open sites, where leaf and soil temperatures can be high (e.g., McCarthy, 1994). Drought-tolerant species, like Q. stellata, have taproots with a great capacity for deep root growth that permit the seedling to explore deeper soils for moisture (Pallardy & Rhoads, 1993). Some species, like Juglans nigra, use stress-induced leaf abscission during summer to increase the root-shoot ratio in order to maintain a more favorable water balance during summer droughts (Parker & Pallardy, 1985; Pallardy & Rhoads, 1993).

The low-light environment experienced under a forest canopy can limit seedling growth (e.g., Shirley, 1929; Quintana-Ascencio et al., 1992). The forest floor has a light intensity [less than]20% of that of open sites. Quercus rubra seedlings benefit from shade because shade moderates temperature and evapotranspiration (Crow, 1988), but under heavy shade daily [CO.sub.2] fixation rates are inadequate to offset seedling respiration. Grubb et al. (1996) reported that very low light levels can cause slow growth and even result in the death of Fagus sylvatica seedlings. The effects of the light environment vary depending on other environmental factors. For example, when moisture is adequate, oak and beech seedlings grow better under bright light conditions, but when moisture is limiting, growth is often better under lower light conditions (Harley, 1939; Ovington & MacRae, 1960). Beech seedlings may not experience nutrient limitation when growing in shade, but nutrients are more likely to be limiting when seedling s grow in full sun (Harley, 1939).

Browsing of seedling leaves, stems, and cotyledons is a leading cause of seedling death or poor performance (Watt, 1919, 1923; Griffin, 1971; Shaw, 1974; Crow, 1988; Callaway, 1992; Herrera, 1995; Madsen, 1995a; Hoshizaki et al., 1997). Seedlings that establish in old fields or near forest edges experience lower rates of whole-plant browsing by mammalian herbivores than do seedlings that establish within the forest (Sork, 1983a; Myster & McCarthy, 1989), but desiccation is more likely to increase in open situations (e.g., McCarthy, 1994). Vertebrates, especially deer, hare, and rodents, are important browsers. Invertebrates are usually unimportant browsers of seedlings (Myster & McCarthy, 1989; McCarthy, 1994), but, at times, insects can cause significant mortality (McPherson, 1993). In some species, like Quercus rubra, resprouting of the shoot from the root collar after browsing is the rule, not the exception (Crow, 1988). The regeneration system seems to be geared toward developing and maintaining an adequ ate root system that can resprout, allowing the seedling to resist repeated browsing until an opportunity to advance to the sapling stage arises. Repeated browsing can kill seedlings quickly (McPherson, 1993) or can keep seedlings in the seedling stage for more than 20 years (Griffin, 1971).

In semiarid environments with dense plant cover, seedlings can experience intense competition for water, light, and nutrients. Competition for water appears to be one of the primary reasons why oak seedlings have low survival rates in oak woodlands (Griffin, 1971; Gordon et al., 1989; McPherson, 1993). Grasses and forbs can deplete the soil of moisture early in the growing season. Madsen (1995b) found that weeds in relatively moist forest openings were not an important factor influencing beech seedling growth, but oak seedlings in wet tropical forests can be harmed by herbaceous cover (Tripathi & Khan, 1990).

XV. Effects of Nut Crops on Community Dynamics

Nuts are among the most nutritious and energy-rich foods produced in natural communities. Consequently, when nuts are produced in abundance they can have dramatic and widespread effects on other community components. These effects are most evident when comparing the numerical and functional responses of animals that feed on nuts during mast and nonmast years. For example, large nut crops are correlated with population increases of numerous species, including squirrels, chipmunks, mice, voles, deer, jays, chickadees, and woodpeckers (Formozov, 1933; Christisen, 1955; Perrins, 1966; Watts, 1969; Goodrum et al., 1971; Flowerdew, 1972; Hansen & Batzli, 1978, 1979; Fox, 1982; Jensen, 1985; Hannon et al., 1987; Koenig & Mumme, 1987; Smith & Scarlett, 1987; Wentworth et al., 1992; McShea & Schwede, 1993; Elkinton et al., 1996; Wolff, 1996; McShea, 2000). Population increases of white-footed mice are caused by increased winter survival and increased reproductive success in the winter and spring following a large nut crop (Elkinton et al., 1996; Wolff, 1996; McShea, 2000). Animals that do not usually associate with nut-bearing plants may be drawn to these habitats to feed on the nuts when they are abundant (e.g., McShea & Schwede, 1993). The species that respond to nut crops include not only a few animals that are potential mutualists (i.e., dispersers) of nuts but also many animals that act strictly as nut predators.

Nut mast is a critical ecosystem component (e.g., Nielsen, 1977) that, when abundant, can have direct and pervasive effects on the structure and functioning of communities. The complexities and extent of these effects have been revealed by studies that show that acorn production in eastern deciduous forests is linked to risk of Lyme disease in humans and to defoliation of oak forests during gypsy moth (Lymantria dispar) outbreaks (Elkinton et al., 1996; Ostfeld et al., 1996; Jones et al., 1998). In years when acorns are abundant, white-footed mice increase in numbers, and white-tailed deer spend more time in oak woods. These changes are associated with an increase in the abundance of black-legged ticks (Ixodes scapularis), which use deer and mice as primary hosts. Some of these ectoparasites also use humans as hosts, which they can infect with Borrelia burgdorferi, a spirochete bacterium that causes Lyme disease. By this chain of events, the risk of Lyme disease to humans increases following a large acorn cr op. Also associated with large acorn crops is a decline in the abundance of gypsy moths because white-footed mice are important consumers of gypsy moth pupae (Ostfeld et al., 1996; Jones et al., 1998). Gypsy moth larvae feed on the leaves of oaks and other broadleaf trees and can defoliate a forest if their populations increase. White-footed mice are an important check on the population size of the moths. But when mast crops of nuts fail, the population of mice declines and rates of predation of moth pupae also decline, events that may initiate moth outbreaks. Defoliation caused by the moth larvae can be sufficient to kill oak trees, reduce the annual growth increment, and reduce the size of acorn crops (Gottschalk, 1990; Ostfeld et al., 1996; Jones et al., 1998).

When nut mast is produced in abundance, it can also have indirect effects on other plant species. For example, when white-tailed deer (Odocoileus virginianus) feed heavily on acorn mast, the browsing of alternative foods, including the seedlings and saplings of shrubs and trees, is often markedly reduced (Christisen, 1955; Reid & Goodrum, 1958; Harlow et al., 1975; Ostfeld et al., 1996), creating opportunities for these plants to become established and grow.

XVI. Holocene Migrations of Nut Trees

Over the past 16,000 years, plant communities in the temperate regions of North America and Europe have undergone dramatic changes. Since the most recent glacial retreat, some tree species have undergone displacement of more than 2000 km (Davis, 1981; Webb, 1981; Huntley, 1988). Nut-bearing trees participated in these movements. Some of these movements have been documented using pollen profiles from lake and pond sediments and plant macrofossils (van der Hammen et al., 1971; Davis, 1981; Delcourt & Delcourt, 1984; Bennett, 1985; Huntley, 1988; Webb, 1988).

The nut-bearing trees in eastern North America that have well-documented migrational histories are Quercus, Fagus, Carya, and Castanea (Davis, 1981; Bennett, 1985; Davis et al., 1986; Webb, 1987; Woods & Davis, 1989). During the Wisconsin glacial maximum, prior to 16,000 years ago, these nut-bearing species were restricted to what is now the southeastern United States and the lower Mississippi River Valley. After the amelioration of climate that initiated the present interglacial period (15,000-12,000 years ago), these trees began to disperse northward. They reached the northern edges of their current geographical ranges between 10,000 and 2000 years ago. Each taxon spread along a different route and moved at a different rate to reach its present distribution. Davis (1981) estimated that Quercus spread the fastest, making the 1200-1600 km range expansion at the rate of about 350 m/yr and that Castanea spread the slowest, at about 100 m/yr. Delcourt and Delcourt (1987) found slower rates of spread: 126 m/yr f or Quercus, and 169 m/yr for Fagus. Comparable rates of spread have been reported for nut-producing genera in Europe (Huntley, 1988). Interestingly, the migration rates of most of these nut-bearing trees (i.e., oaks, beech, hickories) were as fast as or faster than those of some wind-dispersed trees (i.e., maples, firs, hemlock, spruces) that also made the northward migration (Davis, 1981; Webb, 1986; Johnson & Webb, 1989). This suggests that the evolution of large, heavy propagules does not necessarily entail a reduction in dispersibility. In fact, Aizen and Patterson (1990) found a strong positive correlation between acorn size and the size of the geographical range of oak species in North America, suggesting that large acorn size facilitates dispersibility.

Ancestors of those species that disperse these plants today (e.g., jays, chipmunks, squirrels) are assumed to have been important dispersal agents of the nuts during their northward migrations (Johnson & Webb, 1989). The dispersal capacity of these agents is sufficient, in most cases, to account for the rates of dispersal observed. Blue jays in eastern North America, for example, are known to transport beechnuts up to 4 km (Johnson & Adkisson, 1985) and probably move acorns, chestnuts, and pecans similar distances. European jays move nuts comparable distances in Europe. To achieve the rates of dispersal derived from fossil pollen analyses, nut trees had to have moved northward at the rate of 1.2 to 8.0 km per generation (Johnson & Webb, 1989). More data on the maximum nut-transport distances of jays and minimum generation time of nut trees growing in early successional habitats will probably reduce the disparity in these estimated rates of spread. Also, rare but very long range dispersal events (Clark, 1998) may have contributed to the apparent discrepancy.

Food-caching rodents and jays appear to have played an important role in shaping Holocene plant communities in the deciduous forests of North America, Europe, and Asia. These animals effected nut dispersal over a range of distances from meters to kilometers, maintaining populations of nut-bearing plants on a local scale, transporting nuts to new environments, and causing gene flow across a patchy landscape. However, the patchiness of the landscape has increased dramatically over the last several hundred years, as these once nearly continuous forests have been fragmented by agricultural and commercial interests. The dispersal of nuts across these highly fragmented landscapes has been reduced but not eliminated (Johnson et al., 1981; Johnson & Adkisson, 1985). Nut-bearing animals continue their role as dispersers of plant propagules and genes today, but the long-term health and persistence of these plant populations, the forests they constitute, and the many animals that depend on them for food and shelter in the modem fragmented landscape will depend, in part, on how wisely we use our knowledge of plant--animal interactions to manage these resources in the future.

XVII. Acknowledgments

I thank Maurie Beck, Jeanne Chambers, Pierre-Michel Forget, Patrick Jansen, and Walter Koenig for their helpful comments on an earlier draft of the manuscript.

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                 Dry mass and caloric value of various
                            nuts and acorns
                                           Caloric value
                    Dry mass  Percentage     (kJ) [a]
                       of      of whole
                    nut meat  nut that is       Per        Per
Species               (g)       edible         gram        nut
Carya glabra          1.07        --           26.5        28.4
Carya illinoiensis    3.64       55.6           --          --
Carya illinoiensis    3.36       57.0           --          --
Carya illinoiensis     --         --           32.9         --
Carya ovata           1.01       33.1          27.5        27.8
Corylus avellana      1.31       48.8          28.1        36.8
Corylus avellana      1.55       42.0          34.0        52.7
Fagus silvatica       0.19       66.5          30.2         5.7
Juglans nigra         2.04       14.3          26.1        53.2
Juglans regia         5.77       47.3          26.6       153.5
Prunus dulcis          --         --            --         25.0
Quercus alba          0.40       49.4          17.4         7.0
Quercus alba          0.83        --           17.8        14.7
Quercus macrocarpa    4.66       69.6          18.2        84.8
Quercus petraea       2.44       83.6          18.7        45.6
Quercus prinus        1.21        --           18.1        21.8
Quercus robur         4.21       85.5          19.0        80.0
Quercus rubra         2.12        --           20.4        43.2
Quercus shumardii     2.28       72.4          21.8        49.7
Species             Source
Carya glabra        Lewis, 1982
Carya illinoiensis  Thompson et al., 1989
Carya illinoiensis  Thompson & Baker, 1993
Carya illinoiensis  Burns & Viers, 1973
Carya ovata         Smith & Follmer, 1972
Corylus avellana    Mehlenbacher, 1991
Corylus avellana    Grodzinski & Sawicka-Kapusta, 1970
Fagus silvatica     Grodzinski & Sawicka-Kapusta, 1970
Juglans nigra       Smith & Follmer, 1972
Juglans regia       McGranahan & Leslie, 1991
Prunus dulcis       Kester et al., 1991
Quercus alba        Smith & Follmer, 1972
Quercus alba        Lewis, 1982
Quercus macrocarpa  Smith & Follmer, 1972
Quercus petraea     Grodzinski & Sawicka-Kapusta, 1970
Quercus prinus      Lewis, 1982
Quercus robur       Grodzinski & Sawicka-Kapusta, 1970
Quercus rubra       Lewis, 1982
Quercus shumardii   Smith & Follmer, 1972
(a.)Caloric values converted to joules.
                 Nutrient composition of nut meats on a
                 percentage dry-weight basis. The data
                from some sources were recalculated from
                  a wet-weight to a dry-weight basis.
                 Additional data on the composition of
             acorns can be found in Reid and Goodrum (1958)
                                               free     Crude
Species              Water  Protein  Lipids   extract   fiber  Ash
Aesculus glabra      52.7    12.6      6.1     74.0      2.5   4.8
Carya floridana       -       9.6     34.3     45.3      9.3   1.5
Carya ovata           2.2    13.3     74.4      8.8      1.5   2.0
Castanea dentata     43.7     8.6      2.3     82.9      3.4   2.8
Castanea mollissima  44.0     7.5      2.0     84.6      2.9   3.0
Castanea mollissima  57.6    10.4      2.1     81.6      3.3   2.6
Castanea sativa      54.9     4.4      3.6     86.3      3.0   2.7
Castanea vulgaris    33.1     6.9      3.3     84.3      2.4   3.1
Corylus americana     2.6    26.5     61.4      7.2      2.2   2.7
Corylus avellana      1.9    12.7     67.3     16.0      1.8   2.1
Fagus silvatica       5.0    30.5     49.6      7.6      7.3   4.9
Juglans nigra         2.9    29.3     60.2      6.7      1.0   2.8
Juglans nigra        11.0    32.6     36.9     25.0      2.1   3.4
Juglans regia         3.2    14.0     71.3      3.0      9.9   1.8
Prunus dulcis         5.0    19.0     54.0     20.0      3.0   3.0
White oaks (WO)
Quercus alba         47.3     6.3      6.3     82.3      2.5   2.5
Quercus alba          -       6.5      4.8     83.3      2.7   2.7
Quercus alba         24.3     7.8      5.8     81.2      4.0   1.1
Quercus chapmanii     -       4.8      4.1     87.0      2.3   1.8
Quercus germinata     -       3.9      4.7     88.7      1.4   1.3
Quercus lyrata       29.5     4.4      2.6     88.2      2.3   2.4
Quercus macrocarpa   29.6     3.9     11.5     80.2      2.4   1.8
Quercus michauxii    16.4     4.4      4.6     86.4      2.5   2.1
Quercus minima        -       4.2      4.7     87.5      1.7   1.9
Quercus petraea      14.2     5.7      6.9     80.4      4.5   2.5
Quercus prinoides    44.2     7.6      6.3     81.7      2.4   2.0
Quercus prinus        -       5.8     10.1     78.9      2.5   2.2
Quercus prinus       50.1     6.9      5.1     83.2      2.6   2.2
Quercus stellata     16.5     6.2      9.4     80.2      2.4   1.8
Quercus virginiana   18.3     7.4      9.4     78.4      2.5   2.1
Black oaks (BO)
Quercus falcata       8.7     6.9     31.0     56.5      3.0   2.7
Quercus ilicifolia   42.0    10.3     20.0     64.6      3.0   2.1
Quercus incana       10.6     7.3     20.0     68.0      3.3   1.4
Quercus inopina       -       5.6     24.8     65.8      2.5   1.3
Quercus laevis        -       3.7      8.1     84.5      2.0   1.7
Quercus marilandica  11.5     6.9     16.9     72.2      2.4   1.6
Quercus myrtifolia    -       4.8     26.7     64.6      2.7   1.2
Quercus nigra        11.4     5.4     12.7     77.2      3.3   1.4
Quercus phellos      10.3     5.2     11.1     79.0      3.4   1.3
Quercus rubra        38.2     6.6     20.8     67.1      3.1   2.4
Quercus rubra         -       5.3     19.3     69.1      4.2   2.6
Quercus rubra        14.9     7.0     18.9     68.2      2.8   3.1
Quercus shumardii    11.2     7.5     24.2     61.4      3.1   3.7
Quercus velutina      -       7.0     24.1     64.6      3.1   1.7
Quercus velutina      9.0     6.9     23.0     65.1      3.0   2.0
Species              Source
Aesculus glabra      Wainio & Forbes, 1941
Carya floridana      Abrahamson & Abrahamson, 1989
Carya ovata          Wainio & Forbes, 1941
Castanea dentata     McCarthy & Meredith, 1988
Castanea mollissima  McCarthy & Meredith, 1988
Castanea mollissima  Payne et al., 1983
Castanea sativa      McCarty & Meredith, 1988
Castanea vulgaris    Wainio & Forbes, 1941
Corylus americana    Wainio & Forbes, 1941
Corylus avellana     Mehlenbacher, 1991
Fagus silvatica      Drozdz, 1968
Juglans nigra        Wainio & Forbes, 1941
Juglans nigra        Baumgras, 1944
Juglans regia        McGranahan & Leslie, 1991
Prunus dulcis        Kester et al., 1991
White oaks (WO)
Quercus alba         Wainio & Forbes, 1941
Quercus alba         Gysel, 1957
Quercus alba         Baumgras, 1944
Quercus chapmanii    Abrahamson & Abrahamson, 1989
Quercus germinata    Abrahamson & Abrahamson, 1989
Quercus lyrata       Ofcarcik & Burns, 1971
Quercus macrocarpa   Ofcarcik & Burns, 1971
Quercus michauxii    Ofcarcik & Burns, 1971
Quercus minima       Abrahamson & Abrahamson, 1989
Quercus petraea      Drozdz, 1968
Quercus prinoides    Wainio & Forbes, 1941
Quercus prinus       Smallwood & Peters, 1986
Quercus prinus       Wainio & Forbes, 1941
Quercus stellata     Ofcarcik & Burns, 1971
Quercus virginiana   Ofcarcik & Burns, 1971
Black oaks (BO)
Quercus falcata      Ofcarcik & Burns, 1971
Quercus ilicifolia   Wainio & Forbes, 1941
Quercus incana       Ofcarcik & Burns, 1971
Quercus inopina      Abrahamson & Abrahamson, 1989
Quercus laevis       Abrahamson & Abrahamson, 1989
Quercus marilandica  Ofcarcik & Burns, 1971
Quercus myrtifolia   Abrahamson & Abrahamson, 1989
Quercus nigra        Ofcarcik & Burns, 1971
Quercus phellos      Ofcarcik & Burns, 1971
Quercus rubra        Wainio & Forbes, 1941
Quercus rubra        Gysel, 1957
Quercus rubra        Baumgras, 1944
Quercus shumardii    Ofcarcik & Burns, 1971
Quercus velutina     Gysel, 1957
Quercus velutina     Baumgras, 1944
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Publication:The Botanical Review
Date:Jan 1, 2001
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