Seed Selectivity: Crop Size, Predispersal Predation, and Seed Characteristics

Variation in seed characteristics within and among tree species can affect seed dispersal because corvids are selective when choosing seeds for hoarding. When seed crops are large and seeds are not limiting, birds selectively forage on, and therefore disperse, trees with seed characteristics that they prefer. For example, arthropods and fungi often damage pine cones and acorns during maturation (Espelta et al. 2009). Within trees, many birds inspect seeds and avoid ones with obvious damage caused by insects whose larvae eat the cotyledons, which are often the most nutritious part of the seed (Bossema 1979, Darley-Hill and Johnson 1981, Fleck and Woolfenden 1997, Hubbard and McPherson 1997). Despite low availability (11%) of viable seeds on American beech (Fagus grandifolia) trees, Blue Jays (Cyanocitta cristata) transported and cached viable seeds only (Johnson and Adkisson 1985). After visual inspection, the birds assess seeds by handling them with their bill, lifting and rattling them in the process, which also allows them to exclude seeds that have been compromised by arthropods but show no exterior traces (Vander Wall and Balda 1977, Dixon et al. 1997, Hubbard and McPherson 1997, Langen and Gibson 1998, Langen 1999). Similarly, Clark's Nutcrackers (Nucifraga columbiana) discarded ≥4.5% of pinyon pine seeds, many of which were subsequently determined to be spoiled (Vander Wall and Balda 1977). Birds not only ignore damaged seeds within a tree; sometimes they avoid trees and entire stands with low-quality cones or those affected by insects (Christensen and Whitham 1991, 1993, Christensen et al. 1991). The avoidance of damaged seeds by scatter-hoarding birds enhances the quality of seed dispersal, because the proportion of viable seeds that are dispersed is higher than the proportion present on the tree.

Size and chemical composition affect corvid preferences for acorns of different oak species. Darley-Hill and Johnson (1981) reported that Blue Jays in Virginia removed the seeds from pin oak (Q. palustris), black oak (Q. velutina), willow oak (Q. phellos), and American beeches while ignoring nearby white oaks (Q. alba) and northern red oaks (Q. borealis) that were also carrying large acorn crops; they speculated that the large diameter of red oak acorns and the early germination of white oak acorns may have deterred the birds. Scarlett and Smith (1991) found a similar pattern in Blue Jays in Arkansas, which avoided the large acorns of white, red, and English oaks (Q. robur) while foraging on smaller acorns of willow, pin, black, and post oaks (Q. stellata). In subsequent experiments, the Blue Jays showed the same avoidance of large acorns and preferred small acorns from pin and willow oaks. Interestingly, preferred acorns also had higher tannin content (Scarlett and Smith 1991). By contrast, Moore and Swihart (2006) showed, on the basis of experiments with different acorn types, that Blue Jays will eat less-preferred acorns when other options are unavailable; they also found that Blue Jays preferred acorns with lower tannin content when the size was similar and argued that these factors were confounded in other studies. In summary, when multiple species of oaks are present in a community, the effects of the birds' seed selectivity can be positive for trees with preferred seed characteristics, and negative for trees with less-preferred seeds (Lichti et al. 2014).

Seed selectivity by corvids directly results in high seed dispersal quality, but other dispersers are less discriminatory or damage acorns during harvest. Eastern gray squirrels (Sciurus carolinensis) readily eat and disperse acorns infested by weevils (Curculionidae), the most common arthropods found in acorns (Steele et al. 1996). Similarly, seed-dispersing rodents in Spanish woodlands exhibited a weak preference for healthy acorns but still dispersed large numbers of acorns with weevil damage or weevils inside (Perea et al. 2012). Some squirrels also prevented germination of acorns by excising the embryo before caching the seeds (Steele et al. 2001). Nevertheless, rodents play an important role in dispersal communities and move large proportions of seeds where they are present (Gómez et al. 2008, Siepielski and Benkman 2008).

Transportation Distance and Frequency

Scatter-hoarding rodents and marsupials are often important dispersers of large seeds in tropical areas, but corvids are the dominant dispersers for large-seeded plants in many northern temperate communities (Table 1; Forget and Vander Wall 2001, Jansen et al. 2004, Russo 2005, Purves et al. 2007, Whelan et al. 2008, García and Martínez 2012). Rodents that compete with birds for seeds rarely disperse them over distances >100 m, but they often dominate local dynamics in those same communities (Howe and Smallwood 1982, Siepielski and Benkman 2007, Gómez et al. 2008). However, there have been few explicit comparisons of different dispersers and their dispersal distances for the same tree (Gómez 2003, Thayer and Vander Wall 2005, Gómez et al. 2008).

After selecting seeds at the tree, corvids transport them in their bill, crop, or sublingual pouch, the latter an adaptation evolved specifically for efficient seed transportation over potentially extensive distances (Bock et al. 1973). Transportation distances can range from a simple hop from the source tree to flights that are tens of kilometers in length (Table 1). Equally important is the fact that seeds are often moved among patches of habitat, differentiating corvids from scatter-hoarding rodents that rarely cross open patches and generally disperse seeds over shorter distances (Vander Wall 1990).

The longer the maximum dispersal distance by any given vector, the more likely the plants are to benefit from such colonization events (Nathan et al. 2008). North American oaks and beeches, for example, experienced rapid northward range expansion of several hundred meters per year after the Last Glacial Maximum; this was likely driven largely by corvid seed dispersal (Johnson and Webb 1989). As temperature and precipitation patterns change globally, such dispersal will play a crucial role in the ability of plants to shift the altitude and latitude of their ranges (Parmesan 2006, Montoya et al. 2008, Engler and Guisan 2009).

Corvids gather seeds at high rates while they are available and may gather many per visit, depending on seed size. Pinyon Jays (Gymnorhinus cyanocephalus), for example, transport ≤56 pine seeds visit⁻¹, and nutcrackers regularly cache >500 seeds day⁻¹ (Vander Wall and Balda 1977, Marzluff and Balda 1992, Hutchins et al. 1996). Over a fruiting season, nutcrackers cache tens of thousands of pine seeds, often more than twice as many as necessary to feed them through the subsequent winter (Tomback 1982, 2016, Tomback and Linhart 1990). Acorns are generally not transported in such large numbers, perhaps because they are much larger, but jays can carry as many as 3 at a time and cache ≤5,000 yr⁻¹, often recovering fewer than half of them (Bossema 1979, Darley-Hill and Johnson 1981, DeGange et al. 1989, Gómez 2003, Carmen 2004, Pesendorfer 2014).

Seed Deposition and Directed Dispersal

Corvids store food items by thrusting them into the substrate with their bill, positioning them in a way that they cannot be seen, and covering them with materials from the surrounding area. Depending on the substrate, the item is lodged into a crack or crevice, or the birds use their bill to create the space before placing the food (Brown 1970, Bossema 1979, Vander Wall 1990). The seeds are usually positioned at a depth of 1–5 cm, which inhibits dehydration and often protects them from vertebrate predators (Bossema 1979, Vander Wall and Balda 1981, Tomback 1982, Borchert et al. 1989, Greenberg et al. 2012).

Corvids do not hide seeds with the intention of cultivating seedlings. In some areas, Clark's Nutcrackers cache a majority of pine seeds in areas that are unsuitable for germination, such as tree bark or rock crevices, and only a small proportion is cached in locations that allow seedlings to germinate (Lorenz et al. 2011, Neuschulz et al. 2015). Elsewhere, however, birds place seeds in areas that are well suited for seedling establishment, and most other corvids hide a majority of items in the ground, where germination is possible (Vander Wall 1990, Tomback et al. 2001). This positioning of a large number of seeds in safe sites is one of the unique aspects of scatter-hoarding seed dispersers (Vander Wall and Beck 2012).

Directed dispersal occurs when seeds are placed in areas that favor germination and seedling establishment. This behavior is performed by a considerable number of corvids and provides an important advantage in the first steps of establishment (Johnson et al. 1997, Wenny and Levey 1998, Wenny 2001, Whelan et al. 2008). In habitat degraded by human activity and drought in the Mediterranean Basin, animal-dispersed trees exhibit stronger resilience to habitat fragmentation and destruction than wind-dispersed species; this effect is likely a consequence of long-distance seed dispersal, as well as of directed dispersal to areas with increased likelihood of seedling establishment and survival (Montoya et al. 2008). Corvid-mediated seed dispersal can thus have profound effects on the community structure of the patch in which seeds have been placed (Johnson et al. 1997, Culliney et al. 2012, Lenda et al. 2012).

Both Old World and New World jays perform directed dispersal by hiding seeds below other plants, at the transition zone between vegetation types, or in recently disturbed areas (Bossema 1979, Tomback 1982, Borchert et al. 1989, Lenda et al. 2012). For seeds and seedlings, such areas can serve as nurse environments by reducing water stress and ungulate herbivory (Callaway and D'Antonio 1991, Broncano et al. 1998, Leiva et al. 2013). In North America, for example, several species of corvids frequently cache in recently burned or disturbed areas, allowing oaks and pines to colonize newly available habitat (Johnson et al. 1997, Lenda et al. 2012). In Spanish woodlands and managed (agroforestry) dehesas, oak seedling recruitment is limited to areas with oak canopy cover and to years with increased precipitation (Mendoza et al. 2009). Fifty percent of holly oak (Q. ilex) acorns planted below shrubs to mimic jay caches survived 8 mo as seedlings, whereas only 16% of acorns planted in the open or below artificial shade survived over that time (Smit et al. 2008). The degree of directed dispersal can vary strongly with habitat. Morán-López et al. (2015a) showed that acorns harvested in oak forests are more likely to arrive in suitable habitat than acorns from dehesas. The topic of context dependence of directed dispersal by corvids thus requires more research.

Masting: Seed Dispersal Insurance for Oaks and Pines?

Many large-seeded trees dispersed by scatter-hoarders have spatially synchronized seed production with cyclical bumper crops, a phenomenon termed “masting” or “mast-fruiting” (Koenig and Knops 2000). Masting appears to be an evolved strategy that interacts with environmental factors to produce synchronous bumper crops over large geographic areas that can be hundreds or thousands of square kilometers in size (Kelly and Sork 2000, Koenig et al. 2003, Koenig and Knops 2013). Masting leads to strong temporal pulses in resources, which reverberate through the whole ecosystem (Ostfeld and Keesing 2000). Seed predators and dispersers such as insects, rodents, and birds respond functionally to mast years with increased reproductive success (Ostfeld and Keesing 2000, Espelta et al. 2009, Koenig et al. 2009). The effect of masting on the scatter-hoarding behavior of corvids, however, is not fully understood.

Two non–mutually exclusive hypotheses make predictions about the effect of masting on seed fate. The “predator satiation hypothesis,” arguably the best-established hypothesis for the functional significance of masting, proposes that seed consumer populations are overwhelmed in bumper crop years, resulting in a larger proportion of seeds that survive until reproduction (Kelly and Sork 2002). This hypothesis, however, makes no clear predictions about the dispersal of the surviving seeds. The “predator [or animal] dispersal hypothesis” proposes that, in addition to predator satiation, mast years improve seed dispersal benefits that plants receive from scatter-hoarders (Vander Wall 2002, 2010). The latter hypothesis is still controversial, and the details of how seed dispersal is affected by masting need to be addressed in future research.

Evidence supporting the predator dispersal hypothesis as a selective advantage of masting mostly comes from rodents. Red acouchis (Myoprocta acouchy), medium-sized rodents that scatter-hoard seeds of Carapa procera, a large-seeded rainforest tree, increased seed dispersal effectiveness in years of bumper crops by increasing seed removal rates and distances, as well as by hoarding larger seeds that were more likely to germinate (Jansen et al. 2004). Jeffrey pines (P. jeffreyi), dispersed by multiple rodent species, experienced seed removal rates that were 4–8 times faster and dispersal distances that were ~25% farther in mast years than in a regular crop year (Vander Wall 2002). While the increase in dispersal rates in mast years may be explained by a functional or numerical response of foraging animals to seed availability, the mechanisms that lead to increased dispersal distances are unclear (Vander Wall 2002, 2010). Bumper crops can also increase plant fitness by affecting other dispersal parameters. Rodents dispersing Prunus armeniaca in China, for example, increased the proportion of seeds that were scatter-hoarded rather than placed in a single larder during a mast year (Li and Zhang 2007). Masting can therefore function to ensure high-quality seed dispersal by increasing the mutualistic benefit the trees receive from scatter-hoarding rodents (Vander Wall 2010).

Bumper crops may affect scatter-hoarding in corvids in ways similar to the effect on rodents, but few studies have addressed this issue. Johnson et al. (1997) noted that scatter-hoarding rates by Blue Jays were significantly reduced in a year of low crop production. Similarly, dispersal rates and distances of acorns scatter-hoarded by Island Scrub-Jays (Aphelocoma insularis) were positively correlated with acorn crop size in local oaks (Pesendorfer 2014). Finally, Siepielski and Benkman (2008) demonstrated that Clark's Nutcrackers showed greater selectivity among trees during bumper crop years. Given that these birds tend to prefer trees with large individual crops of sizable, healthy seeds (Christensen et al. 1991), this may also affect the fitness benefits that the trees receive from seed dispersal. Although the response of scatter-hoarding by corvids to masting of trees still requires more research, its role as a long-distance dispersal mechanism that enables plants to colonize new habitat and change ecosystem dynamics is well established.

Dispersal, Colonization, and Ecosystem Engineering

Bird dispersal of seeds is often a major driver of vegetation succession and land reclamation after disturbance. If the area surrounding the disturbed site provides enough bird habitat and seeds to disperse, birds will accelerate plant succession on disturbed patches (Robinson and Handel 1993, 2000, Neilan et al. 2006, Howe and Martínez-Garza 2014). Directed dispersal by corvids can have large-scale effects on the geographic expansion and resilience of tree populations and their associated ecosystems (Lankau et al. 2011). Driven by long-distance seed dispersal, tree populations can quickly respond to changes in climate and habitat availability despite the immobility of the adult plants (Johnson and Webb 1989, Kollmann and Schill 1996). For example, old fields in Poland were quickly colonized by black walnuts (Juglans regia) because Rooks (Corvus frugilegus) and Carrion Crows (C. corone) preferentially cached nuts in such disturbance zones. Consequently, the range of J. regia has undergone rapid expansion over the past 50 yr in this region (Lenda et al. 2012).

Colonization of new areas by oaks and pines not only changes the species interactions in a patch; it also changes the concentrations of carbon, nitrogen, and soil nutrients as well as soil moisture retention and other abiotic conditions (for a broader discussion of oak effects on ecosystems, see Campos et al. 2013). Oak and pine trees create “fertility islands” through organic-matter incorporation and nutrient cycling. Soils beneath the canopy have lower bulk density, higher pH, and greater concentrations of organic carbon, nitrogen, and total and available phosphorus than soils of neighboring grassland (Dahlgren et al. 1997, Quideau et al. 1998, 2001). Oaks in Texas savannas ameliorate conditions for shrubby plants, initially favoring their establishment by providing shade, but potentially limiting their access to water as the understory plants increase in size (Anderson et al. 2001). Forest patches can expand by facilitating establishment of understory shrubs and conspecifics that are competing with surrounding grasses. Increased shade, water, and soil nitrogen availability allow trees to become established at the edge of forest fragments, creating a positive feedback loop (Li and Wilson 1998).

Such engineering is central to ecosystem restoration because it provides long-lasting changes that extend beyond an individual plant's area and life span (Byers et al. 2006, Crain and Bertness 2006, Hastings et al. 2007). As keystone hardwood species, oaks are major drivers of biodiversity and affect abiotic variables over extended periods (McShea and Healy 2003, Johnson et al. 2009). Similarly, pines change the soil chemistry of patches and facilitate establishment of understory plants in alpine and subalpine habitats (Quideau et al. 1998, Baumeister and Callaway 2006). In coastal California, tall vegetation such as oaks and pines captures moisture from fog, producing an important water input into the ecosystem (Dawson 1998, Fischer et al. 2009). Establishment and expansion of oak and pine stands can thus change the resource availability of the surrounding environment, which can facilitate the subsequent arrival of other plants and animals. This process is often enabled by long-distance seed dispersal by corvids, which suggests that the impact of the birds as a dispersal vector can affect the dynamics of whole ecosystems (see Tomback 2016).

Below, we provide examples of the mutualism between corvids and oak or pine trees that span different habitat types and broad geographic regions (Table 1 and Figure 2). We also highlight case studies of how corvid scatter-hoarding behavior can be utilized in habitat restoration efforts. The value of ecosystem services provided by birds is increasingly recognized and can provide a cost-effective enhancement or alternative to existing restoration methods (Whelan et al. 2008, Wenny et al. 2011).

Eurasian Jays and Oaks

Eurasian Jays (Garrulus glandarius) are associated with oak and pine habitat throughout their range, extending from England to Japan (Figure 2). These birds eat acorns, fruits, invertebrates, and vertebrates, and store acorns throughout the fall (Bossema 1979). The jays are selective between acorns of different species and sizes, preferentially selecting larger acorns unless they are too large for their gape (Pons and Pausas 2007b). Acorns are dispersed as long as they are available, even when presented out of season (Pons and Pausas 2007a).

In heterogeneous landscapes, Eurasian Jays disperse seeds unevenly among available habitat (Morán-López et al. 2015a). Because the birds have strong habitat preferences, habitat composition affects the spatial distribution of caches (Pons and Pausas 2007a); they disproportionatey cache seeds in disturbed areas such as recently abandoned fields and roadside areas, but also in mowed grass (Kollmann and Schill 1996), in the transition zone between vegetation types (Bossema 1979), and in areas with low densities of oaks (Gómez 2003). These are often the microhabitats that favor oak recruitment and yield the highest seedling densities (Pausas et al. 2004, Pons and Pausas 2007a). Habitat preferences, both when foraging and caching, can vary significantly between managed areas, such as dehesas, and continuous forest. Morán-López et al. (2015a) recently demonstrated that acorns from dehesa oaks are less likely to be cached in ways that promote recruitment than acorns from oak forests.

Eurasian Jays are the predominant dispersers of acorns over large distances (Perea et al. 2011), but other animals, such as wood mice (Apodemus spp.), red squirrels (S. vulgaris), and even dung beetles (Thorectes lusitanicus) also cache acorns (den Ouden et al. 2005, Goméz et al. 2008, Pérez-Ramos et al. 2013, Morán-López et al. 2015b). Rodent dispersal plays an important role in within-patch dynamics, but rodents often hesitate to cross open spaces. In fragmented, heterogeneous landscapes, model simulations of oak woodland dynamics in Spain suggest that directed dispersal by jays enhances regional abundance of large-seeded trees (Purves et al. 2007). In fact, jay-dispersed plants show stronger resilience in the face of habitat destruction and fragmentation than other plants that are dispersed by wind (Montoya et al. 2008). Thus, as habitat fragmentation and climate change affect European hardwoods, Eurasian Jays are likely to be an increasingly valuable ally for the oaks (Montoya and Raffaelli 2010).

While much is known about the role of Eurasian Jays as oak dispersers in Western and Central Europe, little is known about European Jay dispersal of oaks and other plant species over most of the jay's range (Figure 2). Because seed dispersal dynamics and scatter-hoarding by corvids are highly context dependent, more research is needed to explore the generality of the ecological role of Eurasian Jays in oak woodland dynamics.

Nutcrackers and Pines

Nutcrackers (Europe: N. caryocatactes; North America: N. columbiana), renowned scatter-hoarders that spend a majority of the fall harvesting and caching pine seeds, carry as many as 150 pine seeds at a time in their sublingual pouch (Bock et al. 1973, Tomback 1978). Nutcrackers transport seeds as far as 32 km and place them in caches of 1–15 seeds (Vander Wall and Balda 1977, 1981, Tomback 1978, 1982, Lorenz et al. 2008, 2011). As a consequence, nutcracker-dispersed pines in the Old World and the New World regularly show a “tree cluster” or “multi-genet” growth form that consists of genetically different individuals (Tomback and Linhart 1990, Tomback et al. 1993, 2001, Tomback 2005).

Lesser and Jackson (2013) showed that repeated long-distance dispersal events by nutcrackers were necessary to establish and stabilize a population of ponderosa pines in the Rocky Mountains, USA. Various substrates and habitats serve as cache locations, ranging from leaf litter in closed-canopy forests to rock crevices and the bark of other pine trees (Lorenz et al. 2011). When placed in the ground, nutcracker caches are usually found 2.5 cm below the surface, an optimal depth for pine seed germination (Tomback 1982). Clearly, not all cache sites are suitable for seed germination and recruitment by pines, but the sheer number and distribution of dispersed seeds across the landscape enables trees to colonize new habitats, providing the trees with mutualistic benefits (Tomback et al. 2001).

In the fall, nutcrackers often fly to lower elevations to gather pine seeds that are then transported back to their territories. Nutcrackers therefore have a strong influence on pine population structure and may allow the plants to track elevational shifts of suitable habitat as the climate changes (Richardson et al. 2002, Tomback 2005, Lesser and Jackson 2013). The birds also exert selection on pine characteristics, choosing pines with more rewarding cones and larger seeds (Siepielski and Benkman 2008). A fifth of all pines—species whose seeds have lost their wings—rely on this mutualism as their dispersal mode (Tomback and Linhart 1990).

Other plant species benefit from this keystone mutualism. Pines ameliorate harsh environmental conditions by changing abiotic factors, such as soil moisture and temperature, as well as exposure to wind and sun. On harsh sites, nutcracker-dispersed pines often act as nurse trees for seedlings of some shrubs and trees (Callaway 1998, Baumeister and Callaway 2006). Nutcrackers disperse whitebark pine seeds to the treeline; there, dwarfed (krummholz) whitebark pines may act as nurse trees, leading to the formation of tree-island conifer communities (Resler and Tomback 2008, Tomback 2016).

New World Jays, Oaks, and Pines

North and South America are home to a diverse group of jays, the New World jays. While little is known about the scatter-hoarding of Neotropical jay taxa, the behavior of temperate North American jays is comparatively well studied. These birds are associated with oak or pine habitat throughout their range (Figure 2) and typically scatter-hoard seeds (Pitelka 1951, Vander Wall 1990, Peterson 1993). An exception is the Gray Jay (Perisoreus canadensis), a sister group to the Old World Siberian Jay (P. infaustus) found throughout Canada and in alpine areas of the United States, which occasionally scatter-hoards seeds but mostly stores arthropods, berries, and fungi in aboveground caches along tree trunks (Waite 1988).

Pinyon Jays are strong fliers and cache seeds as far as 11 km from their harvest location (Vander Wall and Balda 1981, Marzluff and Balda 1992). This long-distance dispersal likely contributes to high levels of heterozygosity in pockets of twoneedle pinyon (Pinus edulis) woodland at the northern edge of the tree's distribution, contrasting with the homozygosity indicative of founder effects common to peripheral stands of many other tree species (Betancourt et al. 1991). This points to repeated dispersal into the area, likely due to Pinyon Jay and nutcracker caches placed there over the past 500–1,000 yr. Seed dispersal activity by Pinyon Jays has probably not only expanded the range of pinyon pines, but also helped maintain pine genetic diversity and population health.

Individual Florida Scrub-Jays (Aphelocoma coerulescens), Western Scrub-Jays (A. californica), and Island Scrub-Jays (A. insularis) cache 5,000–6,000 acorns yr⁻¹ when the acorn crop is good and have been shown to enhance oak habitat recovery (DeGange et al. 1989, Carmen 2004, Pesendorfer 2014). For example, blue oak (Q. douglasii) acorns that were manually planted to mimic caches created by scrub-jays were twice as successful in establishing seedlings as acorns simply placed on the surface, even when ungulates were excluded. The effect was even stronger in areas exposed to seedling predators (Borchert et al. 1989). Aphelocoma caching behavior also contributes to postfire habitat recovery because their ground caches are likely to survive the high temperatures and the acorns face little competition when sprouting after fire (Pase 1969, Borchert et al. 2003, Borchert and Tyler 2010). Despite an abundance of research on scatter-hoarding by Aphelocoma, however, comparatively little is known about their role as seed dispersers.

Blue Jays forage on most oak species in their range, where they are the dominant avian dispersers of acorns (Johnson and Webb 1989, Johnson et al. 1997). In a single fruiting season, Blue Jays collectively transported >130,000 acorns from a stand of 11 pin oaks and 91% of the observed caches were placed in areas suitable for germination, thus promoting colonization of new habitat by the oaks (Darley-Hill and Johnson 1981). Blue Jays increase their caching effort after fires and tend to select canopy gaps and habitat transition zones as their caching sites; these areas also have the most oak seedlings (Johnson et al. 1997). Most remarkable, though, are the distances over which acorns are transported by Blue Jays: up to 4 km, with averages around 1 km (Darley-Hill and Johnson 1981, Johnson and Adkisson 1985, Johnson et al. 1997). In addition to acorns, Blue Jays also disperse the seeds of beeches (Fagus spp.) and American chestnut (Castanea dentata) (Johnson and Adkisson 1985, Heinrich 2014). The combination of intense harvesting effort and cache placement highlights the role of these corvids as a keystone species in the life history of many oaks in eastern North America.

Oak Woodland Restoration in Western Europe

Land managers in Western Europe have long recognized the role of seed dispersal by Eurasian Jays in maintaining and restoring oak habitat. Although many foresters considered corvids a pest that steal valuable acorn crops and kill other passerines, early discussions in forestry journals reveal that they also recognized their contribution to oak regeneration (Stimm and Knoke 2004, Madden et al. 2015). For example, Krebs (1889) wrote that “It is unnecessary to seed oaks, because the jays do so in abundance” (translated from German). Similarly, Stimm and Knoke (2004) cited examples dating back as far as 1653 in which poets described the hoarding activity of the birds, as well as the positive impact on oak regeneration.

German foresters are actively taking advantage of the ecosystem services provided by jays. In an approach termed “ecological silviculture,” large old oaks that serve as a seed source are conserved and wooded areas are thinned to increase oak seedling growth. Mosandl and Kleinert (1998) estimated the contribution of jays as amounting to 2,000–4,000 young oaks ha⁻¹ in an eastern German forest. If seed crops are low, large baskets of seeds are offered, and, in combination with the exclusion of seedling predators, such “jay-oaks” (German Hähereichen) can contribute significantly to the profitability of forested lands (Stimm and Knoke 2004).

Restoration efforts can also profit by saving on the costs of planting trees in public space. For an urban forest in Stockholm, Sweden, Hougner et al. (2006) calculated that replacing “planting” efforts performed yearly by Eurasian Jays with human labor would cost $2 acorn⁻¹, or as much as $9,400 ha⁻¹ of forest annually. A fraction of such replacement costs could be invested in maintaining or creating optimal jay habitat, resulting in similar forest maintenance. In Spain, managers tasked with oak habitat restoration plant small areas of seed-source trees that attract scatter-hoarders to deposit caches at the edge of the vegetation (Rey Benayas et al. 2008). This habitat-islet strategy has been successfully applied to Mediterranean old fields as a cost-effective alternative between full afforestation and simple abandonment of agricultural fields (Rey Benayas and Bullock 2012). An analysis of jay nesting and habitat use pattern also suggests that clearing of brush and maintenance of diverse and complex habitat structure may increase jay densities and consequent oak restoration (Pons and Pausas 2008). More recently, however, Morán-López et al. (2015a) demonstrated that the jays' hoarding behavior can vary tremendously between continuous forest and dehesas. Dispersal rates, distances, and habitat selectivity all varied between the 2 habitat types, illustrating that the birds prefer to forage on and cache acorns from forest trees, and that those acorns are also cached in ways that are more likely to result in oak regeneration, than is the case for acorns from dehesas (Morán-López et al. 2015a). Restoration strategies thus need to be adjusted to site-specific needs in order to maximize the ecosystem services provided by the birds.

Still, many corvids are culled regularly under the assumption that they are only a crop pest and significantly reduce populations of other passerines. A recent analysis, however, revealed that such detrimental impacts are often minute at worst (Madden et al. 2015). Stimm and Böswald (1994) therefore made a strong argument against the culling of corvids, especially Eurasian Jays, by highlighting their useful attributes, such as the silvicultural and restoration benefits described above. Supplementing acorns, maintaining jay-friendly habitat, and restricting jay hunting within target areas can thus positively affect oak habitat restoration.

Whitebark Pine Restoration in the Rocky Mountains

Whitebark pine, a keystone species in the Rocky Mountains of western North America (Tomback 2005), has declined throughout its range as a result of blister rust infestation, mountain pine beetle (Dendroctonus ponderosae) attacks, and fire suppression (Tomback et al. 2001, Scott and McCaughey 2006, Tomback and Achuff 2010). Clark's Nutcrackers are the main seed dispersers of whitebark pine (P. albicaulis; Tomback 1982), and they forage less frequently in trees that have reduced cone crops due to tree damage and mortality by blister rust and bark beetles. In fact, cone abundance thresholds identified for nutcracker foraging are now used to categorize areas for restoration efforts (McKinney and Tomback 2007, McKinney et al. 2009, Barringer et al. 2012).

Managers use multiple methods to enhance the nutcracker–pine mutualism. Catering to nutcracker caching preference, suitable areas have been created by prescribed fire and silvicultural practices (Keane and Parsons 2010). Such areas attract nutcracker caching but, for unknown reasons, have resulted in little regeneration of pines. Meanwhile, other areas may comprise trees that are resistant to the fungal infestation that causes blister rust. Consequently, recovery plans also include the propagation of seed from resistant trees in areas that are still largely intact (Schoettle and Sniezko 2007); but in highly degraded areas, different tactics are necessary (Tomback and Achuff 2010, Tomback 2016). Combined with site preparation to enhance survival of seedlings and young trees, managers could take advantage of seed dispersal by nutcrackers to distribute seeds of resistant trees throughout the landscape.

Recovery of Oak Chaparral and Pine Woodland in Channel Islands National Park

Oak and pine vegetation on the 2 largest islands, Santa Cruz and Santa Rosa, in southern California's Channel Islands National Park are recovering from 150 yr of grazing by introduced livestock (Van Vuren and Coblentz 1987, Morrison 2011). The extent of these habitats on Santa Cruz Island has more than doubled since livestock removal began in the late 1980s, likely aided by the endemic Island Scrub-Jay (Morrison et al. 2011). Furthermore, the spatial patterns of vegetation expansion suggest that Island Scrub-Jay seed dispersal was an important driver of the island's passive recovery (Beltran et al. 2014, Dahlin et al. 2014). This corvid is one of the rarest and most range-restricted passerine species in the United States, with an estimated total population of <3,000 individuals (Sillett et al. 2012). Nonetheless, because each individual jay is estimated to disperse ~4,500 acorns yr⁻¹, this population may transport ~7 million acorns yr⁻¹ (Pesendorfer 2014). On Santa Rosa Island, which lacks Island Scrub-Jays, the recovery of oak and pine habitats has been slow. Oaks and pines experienced little apparent recruitment until nonnative ungulates were fully eradicated in 2011.

Restoration of oak and pine habitats on Santa Rosa Island, in the absence of a scatter-hoarding jay, will require either an enormous investment of capital and human labor or many decades to centuries of time. Island Scrub-Jays, however, formerly occurred on Santa Rosa Island, perhaps into the 19th-century ranching era (Collins 2009). Translocation of Island Scrub-Jays to Santa Rosa Island is a potential strategy to both abate threats associated with the jays' small population size and restricted range and accelerate restoration of the island's oak and pine habitats (Morrison et al. 2011). Island Scrub-Jays would likely rapidly disperse Santa Rosa Island's oaks (Q. pacifica, Q. agrifolia, and Q. tomentella) and Bishop pines (P. muricata), as well as seeds from the small endemic population of Torrey pine (P. torreyana), a range-restricted species that, like the jay, is considered vulnerable (IUCN 2012). Both the island endemic jay and its mutualistic partners could benefit from proactive conservation action while providing a cost-effective alternative to human labor (Hougner et al. 2006, Morrison et al. 2011).