THE
VOL. 67
BOTANICAL
REVIEW
JANUARY-MARCH
2001
NO. 1
The Evolutionary Ecology of Nut Dispersal
STEPHEN B . V A N D E R W A L L
Department of Biology
Ecology, Evolution, and Conservation Biology Program
University of Nevada
Reno, NV89557, U.S.A.
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Abstract . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Synopsis of Nut Genera . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Evolutionary History of Nuts . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
A. Evolution from Wind-Dispersed Diaspores . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
B. Evolution from Frugivore-Dispersed Diaspores . . . . . . . . . . . . . . . . . . . . . . . . .
Evolution of Nut-Dispersing Animals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Nutritional Qualities of Nut Meats . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Nut Development . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Predispersal Predation of Nuts by Insects and Microbes . . . . . . . . . . . . . . . . . . . . . .
Deterrence of Feeding by Vertebrates . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Husk Dehiscence and Nut Fall . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Nut Dispersal . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Mast Seeding: Annual Variation in Nut Production . . . . . . . . . . . . . . . . . . . . . . . . .
Nut Dormancy and Germination . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Seedling Establishment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Effects of Nut Crops on Community Dynamics . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Holocene Migrations of Nut Trees . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Literature Cited . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
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I. Abstract
A v a r i e t y o f n u t - p r o d u c i n g plants h a v e m u t u a l i s t i c s e e d - d i s p e r s a l interactions with anim a l s ( r o d e n t s a n d corvids) that scatter h o a r d their nuts in the soil. T h e g o a l s o f this r e v i e w are
to s u m m a r i z e the w i d e s p r e a d horticultural, botanical, a n d ecological literature p e r t a i n i n g to
n u t d i s p e r s a l in Juglans, Carya, Quercus, Fagus, Castanae, Castanopsis, Lithocarpus, Corylus, Aesculus, a n d Prunus; to e x a m i n e t h e e v o l u t i o n a r y histories o f t h e s e m u t u a l i s t i c interac-
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TheBotanicalReview67(1): 74-117, January-March 2001
9 2001 The New York Botanical Garden
74
ECOLOGY OF NUT DISPERSAL
75
tions; 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. Nut-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 Pinus
(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.
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THE BOTANICAL REVIEW
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 forest 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.
IlL 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 (J. cinerea) of eastern North America, the Japanese walnut ,I. 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 roundto-oval nuts range from 20 to 45 mm in diameter. Large nut crops are produced at intervals of
ECOLOGY OF NUT DISPERSAL
77
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.
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Nuts are generally oval or flattened, 20-50 mm in diameter, and enclosed in a leathery, threevalved 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 (Tiffhey, 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.
A. EVOLUTIONFROM WIND-DISPERSEDDIASPORES
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
modem 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 nu-
ECOLOGY OF NUT DISPERSAL
79
merous features with the Juglandaceae. It had laterally compressed nutlets ~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).
Platyearya, 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 ofnutlets 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 recently derived from Oreomunnea, the bracts are vestigial, and the nut is ~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
(< 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 (~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 (I 986) 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.
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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 modem nuts of these genera evolved from winddispersed nuttets. 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 modem 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.
B. EVOLUTIONFROM FRUGIVORE-DISPERSEDDIASPORES
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 modem, 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 behavior can benefit the plant. If the seeds are scatter hoarded in the soil and ifa
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
ECOLOGY OF NUT DISPERSAL
81
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 coevolutionary 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
82
THE BOTANICAL REVIEW
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 modem 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
modem 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 (Book 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.
ECOLOGY OF NUT DISPERSAL
83
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, 1991 ; 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 & Bums, 1971; Polles et al., 1981). Tannins are thought to
reduce the digestive efficiency of nut predators.
84
THE BOTANICAL REVIEW
Table I
Dry mass and caloric value of various nuts and acorns
Species
Carya glabra
Carya illinoiensis
Carya illinoiensis
Carya illinoiensis
Carya ovata
Corylus avellana
Corylus avellana
Fagus silvatica
Juglans nigra
Juglans regia
Prunus dulcis
Quercus alba
Quercus alba
Quercus macrocarpa
Quercuspetraea
Quercusprinus
Quercus robur
Quercus rubra
Quercus shumardii
Dry mass Percentage
of
of whole
nut meat nut that is
(g)
edible
1.07
3.64
3.36
1.01
1.31
1.55
0.19
2.04
5.77
0.40
0.83
4.66
2.44
1.21
4.21
2.12
2.28
55.6
57.0
33.1
48.8
42.0
66.5
14.3
47.3
49.4
69.6
83.6
85.5
72.4
Caloric value
(kj)i
Per
gram
Per
nut
26.5
32.9
27.5
28.1
34.0
30.2
26.1
26.6
17.4
17.8
18.2
18.7
18.1
19.0
20.4
21.8
28.4
27.8
36.8
52.7
5.7
53.2
153.5
25.0
7.0
14.7
84.8
45.6
21.8
80.0
43.2
49.7
Source
Lewis, 1982
Thompson et al., 1989
Thompson & Baker, 1993
Burns & Viers, 1973
Smith & Follmer, 1972
Mehlenbacher, 1991
Grodzinski & Sawicka-Kapusta,
Grodzinski & Sawicka-Kapusta,
Smith & Follmer, 1972
McGranahan & Leslie, 1991
Kester et al., 1991
Smith & Follmer, 1972
Lewis, 1982
Smith & Follmer, 1972
Grodzinski & Sawicka-Kapusta,
Lewis, 1982
Grodzinski & Sawicka-Kapusta,
Lewis, 1982
Smith & Follmer, 1972
1970
1970
1970
1970
a Caloric values converted to joules.
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).
ECOLOGY OF NUT DISPERSAL
85
Table II
Nutrient composition o f 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).
Species
Aesculus glabra
Caryafloridana
Carya ovata
Castanea dentata
Castanea mollissima
Castanea moltissima
Castanea sativa
Castanea vulgaris
Corylus americana
Corylus avellana
Fagus silvatica
Juglans nigra
Juglans nigra
Juglans regia
Prunus dulcis
Nigrogenfree
Crude
Water Protein Lipids
extract
fiber
52.7
2.2
43.7
44.0
57.6
54.9
33.1
2.6
1.9
5.0
2.9
11.0
3.2
5.0
12.6
9.6
13.3
8.6
7.5
10.4
4.4
6.9
26.5
12.7
30.5
29.3
32.6
14.0
19.0
6.1
34.3
74.4
2.3
2.0
2.1
3.6
3.3
61.4
67.3
49.6
60.2
36.9
71.3
54.0
74.0
45.3
8.8
82.9
84.6
81.6
86.3
84.3
7.2
16.0
7.6
6~7
25.0
3.0
20.0
2.5
9.3
1.5
3.4
2.9
3.3
3.0
2.4
2.2
1.8
7.3
1.0
2.1
9.9
3.0
Ash Source
4.8
1.5
2.0
2.8
3.0
2.6
2.7
3.1
2.7
2.1
4.9
2.8
3.4
1.8
3.0
Wainio&Forbes, 1941
Abrahamson & Abrahamson, 1989
Wainio & Forbes, 1941
McCarthy & Meredith, 1988
McCarthy & Meredith, 1988
Payneetal., 1983
McCarthy & Meredith, 1988
Wainio & Forbes, 1941
Wainio & Forbes, 1941
Mehlenbacher, 1991
Drozdz, 1968
Wainio & Forbes, 1941
Baumgras, 1944
McGranahan & Leslie, 1991
Kester etal., 1991
2.6
2.7
1.1
1.8
1.3
2.4
1.8
2.1
1.9
2.5
2.0
2.2
2.2
1.8
2.1
Wainio & Forbes, 1941
Gysel, 1957
Baumgras, 1944
Abrahamson & Abrahamson, 1989
Abrahamson & Abrahamson, 1989
Ofcarcik & Bums, 1971
Ofcarcik & Bums, 1971
Ofcarcik & Bums, 1971
Abrahamson & Abrahamson, 1989
Drozdz, 1968
Wainio & Forbes, 1941
Smallwood & Peters, 1986
Wainio & Forbes, 1941
Ofcarcik & Bums, 1971
Ofcarcik & Bums, 1971
2.7
2.1
1.4
1.3
1.7
1.6
1.2
1.4
1.3
2.4
2.6
3.1
3.7
1.7
2.0
Ofcarcik & Bums, 1971
Wainio & Forbes, 1941
Ofcarcik & Bums, 1971
Abrahamson & Abrahamson, 1989
Abrahamson & Abrahamson, 1989
Ofcarcik&Bums, 197l
Abrahamson & Abrahamson, 1989
Ofcarcik & Bums, 1971
Ofcarcik & Bums, 1971
Wainio & Forbes, 1941
Gysel, 1957
Baumgras, 1944
Ofcarcik & Bums, 1971
Gysel, 1957
Baumgras, 1944
White oaks (WO)
Quercus alba
Quercus alba
Quercus alba
Quercus chapmanii
Quercus germinata
Quercus lyrata
Quercus macrocarpa
Quercus michauxii
Quercus minima
Quercuspetraea
Quercusprinoides
Quercusprinus
Quercus prinus
Quercus stellata
Quercus virginiana
47.3
24.3
Quercusfalcata
Quercus ilicifolia
Quercus incana
Quercus inopina
Quercus laevis
Quercus marilandica
Quercus myrtifolia
Quercus nigra
Quercusphellos
Quercus rubra
Quercus rubra
Quercus rubra
Quercus shumardii
Quercus velutina
Quercus velutina
8.7
42.0
10.6
11.5
29.5
29.6
16.4
14.2
44.2
50.1
16.5
18.3
6.3
6.5
7.8
4.8
3.9
4.4
3.9
4.4
4.2
5.7
7.6
5.8
6.9
6.2
7.4
6.3
4.8
5,8
4.1
4.7
2.6
11.5
4.6
4.7
6.9
6.3
10.1
5.1
9.4
9.4
6.9
10.3
7.3
5.6
3.7
6.9
4.8
5.4
5.2
6.6
5.3
7.0
7.5
7.0
6.9
31.0
20.0
20.0
24.8
8.1
16.9
26.7
12.7
11.1
20.8
19.3
18.9
24.2
24.1
23.0
82.3
83.3
81.2
87.0
88.7
88.2
80.2
86.4
87.5
80.4
81.7
78.9
83.2
80.2
78.4
2.5
2.7
4.0
2.3
1.4
2.3
2.4
2.5
1.7
4.5
2.4
2.5
2.6
2.4
2.5
Black oaks (BO)
11.4
10.3
38.2
14.9
11.2
9.0
56.5
64.6
68.0
65.8
84.5
72.2
64.6
77.2
79.0
67.1
69.1
68.2
61.4
64.6
65.1
3.0
3.0
3.3
2.5
2.0
2.4
2.7
3.3
3.4
3.1
4.2
2.8
3.1
3.1
3.0
86
THE BOTANICAL REVIEW
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 (I 968) 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 "l-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 coat, 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; Sbuhart, 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 trans-
ECOLOGY OF NUT DISPERSAL
87
located into the cotyledons. In stone fruits (e.g., peaches), which have some similarities to
nut development, there 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 nutbearing 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 oflipids 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
kemels 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
88
THE BOTANICAL REVIEW
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 ~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 squirrels 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 shuckworm (Cydia caryana), the filbertworm (Melissopuslatiferreanus), the pecan nut casebearer
(Acrobasis nuxvorella), the navel orangeworm (Paramyeloistransitella), and codling moths
(Laspeyresiapomonella)(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 ~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 (Leptoglossusphyllopus) (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 (Chromaphisjuglandieola)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
ECOLOGY OF NUT DISPERSAL
89
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 tannins 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 de-
90
THE BOTANICAL REVIEW
signed 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 ofJ. 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 old. 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 weakjawed 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 nut. 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 ofJ. 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 hardshelled 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
ECOLOGY OF NUT DISPERSAL
91
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, tannins 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 (Apodemusflavicollis), 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 (Melanerpesformicivorus), 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 acom woodpeckers. Scrub jays were unable to
maintain their body weight on either Q. agrifolia or Q. lobata acorns (Koenig & Heck, 1988).
Despite the greater potential nutritional value ofQ. 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, bluejays, and grackles (Quiscaius 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.
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THE BOTANICAL REVIEW
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, bluejays 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. S ork
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;
that 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.
ECOLOGY OF NUT DISPERSAL
93
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, food 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 important (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,
94
THE BOTANICAL REVIEW
1968a, 1968b; Sork & Boucher, 1977; Heaney & Thorington, 1978; Monk, 1981; Sork,
1983b; Kikuzawa, 1988; Miyaki & Kikuzawa, 1988; Borchert et al., 1989; W~istljung, 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. K/illander
(1978), for example, estimated that a population of 100-150 rooks (Corvusfrugilegus) 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 Quercuspalustris
acorn crop and cached 54% of the crop. Weevils destroyed 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, 195 l, 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 densitydependent 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
ECOLOGY OF NUT DISPERSAL
95
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;
lida, 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; K/illander, 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). Acoms on the surface of the ground can be damaged by heat and
desiccation (Crow, 1988). lfthe 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 latesuccessional, 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 valu-
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THE BOTANICAL REVIEW
able black walnuts were 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 nutbearing 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 E
(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 intervals; 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 66year 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, 198 l; 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
geographical 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 (O. 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
ECOLOGY OF NUT DISPERSAL
97
probability of cross-pollination (Nilsson & W/istljung, 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 W/istljung (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 &
W~istljung, 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 (Bilsing, 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 nut 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
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THE BOTANICAL REVIEW
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 ofpropagules 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. petraea 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~
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 pericarp 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 of 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
ECOLOGY OF NUT DISPERSAL
99
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 seed 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 con-
100
THE BOTANICAL REVIEW
ditions 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 to 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 2, and seedling production the following spring was 2.2/m 2, a survival rate of 3.7% (Hughes & Fahey, 1988). Seedling production
of Quercuspetraea 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 seedling establishment but become less important as the seedling ages (Korstian, 1927;
Ovington & MacRae, 1960; Brookes et al., 1980; Hoshizaki et al., 1997; Bonfil, 1998). How-
ECOLOGY OF NUT DISPERSAL
101
ever, 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
<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 CO2 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 ofFagus 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
seedlings 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 adequate 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
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THE BOTANICAL REVIEW
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, whitefooted 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 (lxodes 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 crop. 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
broadleaftrees 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).
ECOLOGY OF NUT DISPERSAL
103
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 eastem 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-I 2,000 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 for 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. Bluejays 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.
104
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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.
X V I I . 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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