Stephen B. Vander Wall

SEED REMOVAL, SEED PREDATION, AND SECONDARY DISPERSAL

Many studies of postdispersal seed fate use seed removal as an index of seed predation. However, following primary seed dispersal, some seeds are transported intact by ants, dung beetles, scatter-hoarding animals, or abiotic processes to new microsites (secondary dispersal) where germination is possible. Despite a growing realization that secondary seed dispersal can play an important role in plant recruitment, many researchers continue to use seed removal as a proxy for seed predation and are focused too intently on only the initial step of seed fate. We describe, using examples from the recent literature, how the results of some seed removal studies may have been misinterpreted, present plausible, alternative explanations for the fate of seeds in those studies, and discuss the importance of detailed studies of seed fates. Following the fates of seeds can be difficult, but such studies contribute much more to our understanding of seed dynamics and plant fitness.

The evolutionary ecology of nut dispersal

A variety of nut-producing plants have mutualistic seed-dispersal interactions with animals (rodents and corvids) that scatter hoard their nuts in the soil. The goals of this review are to summarize the widespread horticultural, botanical, and ecological literature pertaining to nut dispersal inJuglans, Carya, Quercus, Fagus, Castanae, Castanopsis, Lithocarpus, Corylus, Aesculus, andPrunus; to examine the evolutionary histories of these mutualistic interactions; and to identify the traits of nut-bearing plants and nut-dispersing rodents and jays that influence the success of the mutualism. These interactions appear to have originated as early as the Paleocene, about 60 million years ago. Most nuts appear to have evolved from ancestors with wind-dispersed seeds, but the ancestral form of dispersal in almonds (Prunus spp.) was by frugivorous animals that ingested fruit.Nut-producing species have evolved a number of traits that facilitate nut dispersal by certain rodents and corvids while serving to exclude other animals that act as parasites of the mutualism. Nuts are nutritious food sources, often with high levels of lipids or proteins and a caloric value ranging from 5.7 to 153.5 kJ per propagule, 10–1000 times greater than most wind-dispersed seeds. These traits make nuts highly attractive food items for dispersers and nut predators. The course of nut development tends to reduce losses of nuts to insects, microbes, and nondispersing animals, but despite these measures predispersal and postdispersal nut mortality is generally high. Chemical defenses (e.g., tannins) in the cotyledons or the husk surrounding the nut discourage some nut predators. Masting of nuts (periodic, synchronous production of large nut crops) appears to reduce losses to insects and to increase the number of nuts dispersed by animals, and it may increase cross-pollination. Scatter hoarding by rodents and corvids removes nuts from other sources of nut predation, moves nuts away from source trees where density-dependent mortality is high (sometimes to habitats or microhabitats that favor seedling establishment), and buries nuts in the soil (which reduces rates of predation and helps to maintain nut viability). The large nutrient reserves of nuts not only attract animal dispersers but also permit seedlings to establish a large photosynthetic surface or extensive root system, making them especially competitive in low-light environments (e.g., deciduous forest) and semi-arid environments (e.g., dry mountains, Mediterranean climates). The most important postestablishment causes of seedling failure are drought, insufficient light, browsing by vertebrate herbivores, and competition with forbs and grasses. Because of the nutritional qualities of nuts and the synchronous production of large nut crops by a species throughout a region, nut trees can have pervasive impacts on other members of ecological communities. 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.

MASTING IN ANIMAL-DISPERSED PINES FACILITATES SEED DISPERSAL

Masting increases the efficiency of wind pollination and satiates seed predators, but there is little evidence that masting facilitates seed dispersal by animals. Masting in pines was studied over three field seasons by simulating seed crops in synchrony (mast years, autumn 1998 and 1999) or out of synchrony (non-mast year, autumn 2000) with the local population. Rodents removed simulated wind-dispersed Jeffrey pine (Pinus jeffreyi) and sugar pine (Pinus lambertiana) seeds significantly more rapidly in mast years than in the non-mast year. Radioisotopes were used to follow the fates of individual pine seeds taken from three source trees. Rodents cached nearly all experimental seeds in mast and non-mast years, making 562 caches in 1998, 510 caches in 1999, and 1034 caches in 2000. Mean dispersal distances of seeds in primary caches were 5.9 and 4.6 m (28.6% and 22.1%) farther in the two mast years than in the non-mast year. Rodents often excavated cached seeds and moved them to new sites (secondary caching). During mast years, some seeds were found in as many as three cache sites, but during the non-mast year, the level of secondary caching approximately tripled, with some seeds being found in five or six separate cache sites. Large seed crops were associated with reduced secondary caching of seeds, reduced seed consumption, and greater seed survival in the following spring. Animal-mediated seed dispersal may be a selective force, along with predator satiation and increased efficiency of wind pollination, driving temporal variation in seed production in some large-seeded pines.

How plants manipulate the scatter-hoarding behaviour of seed-dispersing animals

Some plants that are dispersed by scatter-hoarding animals appear to have evolved the ability to manipulate the behaviour of those animals to increase the likelihood that seeds and nuts will be stored and that a portion of those items will not be recovered. Plants have achieved this in at least four ways. First, by producing large, nutritious seeds and nuts that are attractive to animals and that stimulate hoarding behaviour. Second, by imposing handling costs that cause animals to hoard rather than to eat items immediately. These handling costs can take one of two forms: physical barriers (e.g. hard seed coats) that take time to remove and secondary chemicals (e.g. tannins) that impose metabolic costs. Third, by masting, where a population of plants synchronizes reproductive effort, producing large nut crops at intervals of several years. Mast crops not only satiate seed predators, but also increase the amount of seed dispersal because scatter-hoarding animals are not easily satiated during caching (causing animals to store more food than they can consume) but are satiated during cache recovery. And fourth, by producing seeds that do not emit strong odours so that buried seeds are less likely to be discovered. These, and perhaps other, traits have increased the relative success of plant species with seeds dispersed by scatter-hoarding animals.

Seed and Seedling Ecology of Pinon and Juniper Species in the Pygmy Woodlands of Western North America

Knowledge of the seed and seedling ecology of the piñon and juniper woodlands of western North America is essential for understanding both the northward migration and expansion of the woodlands during the Holocene (< 11,500 B.P.), and the accelerated expansion of the woodlands since settlement of the West by Anglo-Americans around 200 years ago. We follow the fates of seeds and seedlings of the different piñon and juniper species within the woodlands from seed development to seedling establishment, and discuss the implications of this information for the past and present expansion of the woodlands. While seed development requires about two and one-half years in pinons, it is species-dependent in junipers and can take one, two, or even three years. Substantial seed losses can occur during seed development due to developmental constraints, and before or after seed maturation as a result of insects, pathogens, or predatory animals. In piñon pines, the primary seed dispersers are scatterhoarding birds (corvids) and rodents that harvest seeds from the trees or after seed fall and cache them in the soil. In contrast, most junipers appear to be dispersed primarily by frugivorous birds and mammals that ingest the seeds and defecate them onto the soil surface. We have recently documented that scatter-hoarding rodents also disperse juniper seeds. Disperser effectiveness, or the contribution a disperser makes to the future reproduction of a plant population, may vary among species of piñons and especially junipers. Piñon seeds are short-lived and exhibit little dormancy, and they probably only germinate the spring following dispersal. Juniper seeds are long-lived and seed dispersal can occur over one or more years. Seed germination can be delayed for several years due to impermeable seed coats, embryo dormancy, or the presence of inhibitors. Seedling establishment of piñon pines is facilitated by nurse plants but, while junipers often establish beneath nurse plants, they are capable of establishing in open environments. In the southwestern United States, higher establishment of juniper occurs in open environments due to more favorable precipitation, and competition may be more important than facilitation in determining establishment.When considering the mechanisms involved in the past and present expansion of the woodlands, short-distance dispersal, local population growth, and long-distance dispersal are all important. Different classes of dispersers, some of which appear to have coevolved with the tree species, appear to be responsible for local (short-distance) vs. long-distance dispersal in pinons and junipers. Because ecotones form the interface between the woodlands and adjacent communities, they can provide valuable information on both the seed dispersal and seedling establishment processes responsible for tree expansion.Disturbance regimes and, recently, the effects of humans on those regimes have major effects on the expansion and contraction of the woodlands. Before Anglo-American settlement, fires occurred as frequently as every 50–100 years throughout much of the woodlands. During this century, fire frequencies have been reduced due to the indirect effects of livestock grazing and the direct effects of removing Native Americans from the ecosystem and implementing active fire-prevention programs. The result has been an increase in tree-dominated successional stages at the expense of grass-dominated stages. Various management techniques, including controlled burning and chaining, have been implemented to reduce tree dominance, but their effects depend largely on the life histories of the tree species and the disturbance characteristics. Several areas relating to the seed and seedling ecology of the piñon and juniper require additional research if we are to truly understand the dynamics of the woodlands.

FORAGING SUCCESS OF GRANIVOROUS RODENTS: EFFECTS OF VARIATION IN SEED AND SOIL WATER ON OLFACTION

The ability of yellow pine chipmunks (Tamias amoenus), deer mice (Peromyscus maniculatus), and other rodents to detect buried Jeffrey pine (Pinus jeffreyi) and antelope bitterbrush (Purshia tridentata) seeds using olfaction was investigated during dry and moist conditions at the Whittell Forest and Wildlife Area in Little Valley, Washoe County, Nevada, USA. Removal of cached seeds was monitored on two Jeffrey pine foraging grids (each with 100 caches of five seeds buried 5 mm deep) and on two bitterbrush foraging grids (each with 100 caches of 15 seeds buried at the same depth). Under dry conditions, soil typically contained <0.5% water, whereas Jeffrey pine and bitterbrush seeds contained 4.37 ± 1.46% water (mean ± 1 sd) and 7.45 ± 1.83% water, respectively. Under these conditions, rodents found a mean of 0.33% of available Jeffrey pine seed caches each day and 0.14% of available bitterbrush seed caches each day. After rains, soil moisture increased to as much as 8.5%, and Jeffrey pine and bitterbrush se...

Cache site selection by chipmunks (Tamias spp.) and its influence on the effectiveness of seed dispersal in Jeffrey pine (Pinus jeffreyi)

The effectiveness of Jeffrey pine (Pinus jeffreyi) seed dispersal performed by seed-caching yellow pine chipmunks (Tamias amoenus) and lodgepole chipmunks (Tamias speciosus) was compared to that of wind dispersal in the Sierra Nevada of western Nevada. Wind-dispersed seeds typically fall under or near the parent tree. Chipmunks removed 90 and 97% of 1064 radioactive seeds from each of two simulated wind-dispersed seed shadows in less than 24 h. “Wind-dispersed” seeds were deployed within 12 m of the two “source” trees, but chipmunk caches were found from 2–69 m from the trees. Chipmunks carried nearly all seeds away from source trees, greatly reducing the density of seeds under and near source trees. Caches contained from 1–35 seeds and most were buried 7–21 mm deep. Chipmunks cached in open bitterbrush shrubland with mineral soils much more than expected and cached in closed-canopy Jeffrey pine and lodgepole pine forests with thick needle litter much less than expected. Many Jeffrey pine seedlings and saplings grow in the bitterbrush habitat and few grow in the pine forests. Ten and 20% of the original caches survived until April, the time of seed germination, at the two sites. The movement of wind-dispersed seeds is random relative to environmental variables important in seedling survival, and the wind in coniferous forests cannot quickly bury seeds. The quality of seed dispersal rendered by chipmunks was superior to that provided by the wind because the chipmunks quickly harvested seeds on the ground, moved them away from source trees, and buried them in the ground in habitats and microhabitats where they were more likely to establish new seedlings. The increased quality of seed dispersal provided by animals relative to the wind may help explain why over twenty species of pines have evolved seeds and cones that are adapted for dispersal by seed-caching animals.

Removal of wind-dispersed pine seeds by ground-foraging vertebrates

Nine treatments involving three species of pine (Jeffrey pine, Pinus jeffreyi ponderosa pine, P. ponderosa; and lodgepole pine, P. contorta) seeds were used to test five hypotheses concerning the determinants of seed removal by animals in the field. Each treatment comprised 100 seeds. Winged seeds were tethered so they could not be blown away. Seeds were checked daily for up to 16 d. Animals (primarily chipmunks) removed most seeds within a few days. Winged Jeffrey pine seeds (large) disappeared significantly faster than ponderosa pine seeds (medium) which disappeared faster than lodgepole pine seeds (small) (...)

Forest rodents provide directed dispersal of Jeffrey pine seeds

Some species of animals provide directed dispersal of plant seeds by transporting them nonrandomly to microsites where their chances of producing healthy seedlings are enhanced. We investigated whether this mutualistic interaction occurs between granivorous rodents and Jeffrey pine (Pinus jeffreyi) in the eastern Sierra Nevada by comparing the effectiveness of random abiotic seed dispersal with the dispersal performed by four species of rodents: deer mice (Peromyscus maniculatus), yellow-pine and long-eared chipmunks (Tamias amoenus and T. quadrimaculatus), and golden-mantled ground squirrels (Spermophilus lateralis). We conducted two caching studies using radio-labeled seeds, the first with individual animals in field enclosures and the second with a community of rodents in open forest. We used artificial caches to compare the fates of seeds placed at the range of microsites and depths used by animals with the fates of seeds dispersed abiotically. Finally, we examined the distribution and survival of naturally establishing seedlings over an eight-year period. Several lines of evidence suggested that this community of rodents provided directed dispersal. Animals preferred to cache seeds in microsites that were favorable for emergence or survival of seedlings and avoided caching in microsites in which seedlings fared worst. Seeds buried at depths typical of animal caches (5-25 mm) produced at least five times more seedlings than did seeds on the forest floor. The four species of rodents differed in the quality of dispersal they provided. Small, shallow caches made by deer mice most resembled seeds dispersed by abiotic processes, whereas many of the large caches made by ground squirrels were buried too deeply for successful emergence of seedlings. Chipmunks made the greatest number of caches within the range of depths and microsites favorable for establishment of pine seedlings. Directed dispersal is an important element of the population dynamics of Jeffrey pine, a dominant tree species in the eastern Sierra Nevada. Quantifying the occurrence and dynamics of directed dispersal in this and other cases will contribute to better understanding of mutualistic coevolution of plants and animals and to more effective management of ecosystems in which directed dispersal is a keystone process.

Mechanisms of cache recovery by yellow pine chipmunks

Abstract The mechanisms yellow pine chipmunks, Tamias amoenus , use to retrieve scatter-hoarded food were investigated in an arena using dry sand as a caching substrate and antelope bitterbrush seeds as the hoarded food. When seeds were moist, chipmunks readily found caches using their olfactory sense, but they seldom found air-dried seeds in dry sand by olfaction. Some chipmunks employed extensive exploratory digging to find caches but their success rates (caches found/digs made) were generally less than 4%. When foraging for caches that they themselves had made among the caches of other chipmunks, subjects found significantly more of their own caches. Furthermore, when landmarks near caches were moved, chipmunks searched in the ‘correct’ sites relative to the moved landmarks. This suggests that yellow pine chipmunks remember the locations of caches. Spatial memory of cache sites, olfaction, exploratory digging and perhaps the use of non-remembered visual cues form a highly integrated system for recovering caches and finding hidden food.