Clark’s Nutcracker: Impact on the Biology and Ecology of Whitebark Pine
Diana F. Tomback (1/09)
The Clark’s nutcracker (Nucifraga columbiana) and whitebark pine (Pinus albicaulis) have intertwined fates: they participate in a coevolved, mutualistic interaction. Essentially, the whitebark pine has evolved a nearly exclusive dependence on nutcrackers to disperse its large seeds, and, in turn, nutcrackers utilize fresh and stored whitebark pine seeds as an important food source. The key behavior that benefits the whitebark pine is the tendency of nutcrackers to bury thousands of whitebark pine seeds as food stores in small clusters or “seed caches” across diverse forest terrain. These seed caches are retrieved by nutcrackers primarily in spring and summer months as an important food source for themselves and their young. Not all seed caches may be recovered, particularly following a large cone crop. Snow melt and spring rains stimulate seed germination, leading to whitebark pine regeneration. The account that follows summarizes information compiled in Tomback (1983, 1998, 2001, and 2005) and Tomback and Linhart (1990), with additional information from Lanner (1996). The primary references with original data may be found cited in these overview publications.
Roots of interaction: nutcracker and Cembrae pine adaptation and coevolution
There are two nutcracker species worldwide--the Clark’s nutcracker, which ranges throughout the higher mountains of the western United States and Canada, and the spotted or Eurasian nutcracker (Nucifraga caryocatactes), which is widely distributed across the higher mountains of Europe, and north-central, and eastern Asia. Both nutcrackers have highly coevolved relationships with pines historically classified together as Cembrae or “stone pines” within the pine family Pinaceae, and the white pine (soft pine) subgenus Strobus. The Eurasian Cembrae pines include four species--Swiss stone pine (P. cembra), Siberian stone pine (P. sibirica), Korean pine (P. koraiensis), and Japanese stone pine (P. pumila). In North America, the sole Cembrae pine is whitebark pine. Fossil evidence indicates that the Cembrae pines may be the most recent pines to evolve. New genetic evidence suggests that these pines may not form a related (monophyletic) group, but rather evolved similar traits through convergence, perhaps selected in part by nutcracker seed dispersal.
All Cembrae pines share several distinctive features considered “derived” or departures from the ancestral state for pines, including relative large and wingless seeds and indehiscent cones—cones that remain closed after seeds ripen. This combination of seed and cone features makes seed dispersal by wind, considered the ancestral condition, impossible, and promotes seed dispersal by nutcrackers. Furthermore, four Cembrae pines share a distinctive “candelabra” growth form, the result of profuse branching and a flat-topped, shrub-like canopy. The upper branches are vertically-oriented, with horizontally-directed cones at the tips, which make cones more visible and accessible to nutcrackers. Japanese stone pine, the exception, assumes a mat-like, dwarf form similar to treeline conifers.
The nutcrackers belong to the avian family Corvidae (along with ravens, crows, and jays), whose members tend to hide food for future use and are distinguished by superior cognitive abilities. Nutcrackers have specialized traits for foraging on conifer seeds: a bill that is long, sturdy, and pointed, and used to remove the scales of closed cones, peck or crack open seeds, and store and recover seed caches; a well-developed spatial memory that enables each bird to retrieve thousands of seed caches each year; a functional incubation patch in males as well as in females (unlike most corvids), enabling males to incubate eggs or brood nestlings while females recover seed caches; an early nesting strategy, so that young are independent by late summer in time to cache their own seeds; and, the sublingual pouch, a sac-like structure developed from the floor of the mouth with an opening under the tongue, which is used to transport conifer seeds and other nuts. For Clark’s nutcrackers, the filled pouch may hold as many as 100 or more whitebark pine seeds.
The nutcracker-Cembrae pine interaction is believed to have evolved initially in Eurasia. According to Lanner, the greater number of Cembrae pines in Eurasia and the number of nutcracker subspecies throughout Europe and Asia argues this case. Based on genetic distance calculations from allozyme studies, Krutovskii et al. estimated the time of separation between whitebark pine and the other
Eurasian stone pines to 0.6 to 1.3 million years ago, which may correspond to formation of a Bering Strait land bridge connecting Eurasia and western North America. An ancestral Cembrae pine and nutcracker would have expanded their range across the bridge, eventually evolving into whitebark pine and Clark’s nutcracker.
Clark’s nutcracker expanded its range beyond that of whitebark pine, through the ranges of other large-seeded white pines, including limber (Pinus flexilis), southwestern white (P. strobiformis), Colorado piñon (P. edulis), and singleleaf piñon (P. monophylla). The seeds of these pines are dispersed by Clark’s nutcrackers as well, but importance of the interaction varies with the pine and geographic area. Nutcrackers also use the seeds of other conifers, including ponderosa (P. ponderosa), Jeffrey (P. jeffreyi), the bristlecone (P. aristata, P. longaeva) pines, and Douglas-fir(Pseudotsuga menziesii). In fact, the more widespread and frequent cone producers, such as ponderosa and Douglas-fir, may represent stable, if less preferred, food sources for nutcrackers. Similarly, the Eurasian nutcrackers use a variety of relatively large-seed pines and hazelnuts (Corylus avellena) beyond the Cembrae pines; and seed use also varies geographically.
There is clearly a difference in “specificity” between whitebark pine and nutcrackers, which has probably accounted for the success of this interaction—until now. Whitebark pine is an “obligate” mutualist of Clark’s nutcracker, which means it is dependent on the bird for seed dispersal, whereas the nutcracker can survive without whitebark pine. This fact has implications regarding the current widespread decline of whitebark pine (see Threats) from white pine blister rust (Cronartium ribicola), mountain pine beetle (Dendroctonus ponderosae), and successional replacement. In areas where the numbers of living whitebark pine have diminished, nutcrackers may be infrequent visitors, thus no longer providing seed dispersal “services.”
Annual cycle of nutcrackers
Photos by D. F. Tomback
The following is based on observations from the Sierra Nevada and Rocky Mountains. When cones are produced by whitebark pine, nutcrackers begin to harvest seeds as early as mid-July, removing pieces of unripe seeds from resinous cones, to feed themselves or their dependent juveniles. At this time, the nutcrackers are acting as seed predators, and the lost seeds are a price the trees pay for seed dispersal services later in the summer. Throughout the summer, nutcrackers also retrieve whitebark pine seed caches made the previous year. By mid to late August, nutcrackers are able to harvest intact seeds with brown seed coats; this appears to be the stimulus for caching seeds. In a good cone crop year, nutcrackers continue to store whitebark pine seeds until October or November. When cone crops are low to moderate, nutcrackers are in a race for access to seeds against the pine squirrels—the Douglas squirrel or chickaree (Tamiasciurus douglasii) of the Pacific ranges and widely-distributed red squirrel (T. hudsonicus)—which rapidly cut down cones as a winter food supply. During fall, most nutcrackers move down to lower elevations or travel to other areas where they search for cones in other large-seeded conifers. Some birds spend the winter at lower elevations or moving up and down in elevation, retrieving caches and foraging in cones for remaining seeds, insects, and other foods. Nutcrackers begin courting as early as December and nesting-building in March or earlier; young generally fledge in April or May. Most nutcrackers may breed at mid-elevations, although some breed within the subalpine zone. Adults feed young seeds retrieved from caches and some insect material. From May to early July, depending on snowpack depth, nutcrackers return to subalpine elevations, many in family groups, and retrieve caches made in previous years.
Seed dispersal
Nutcrackers typically place from 1 to 15 seeds within a cache, although rare caches with more than 30 seeds have been observed; average cache sizes are 3 to 5 seeds. Nutcrackers select diverse microsites for caching, burying caches 1 to 3 cm under various substrates, such as forest litter, mineral soil, gravel, or pumice. Nutcrackers place many caches at the base of trees, near the trunk or exposed roots; these microsites tend to experience early snowmelt. Nutcrackers also cache next to fallen trees and rocks; in fallen trees; in open terrain; among plants; on rocky ledges; and in rock fissures. They place some of their caches in trees, tucking seeds in cracks, holes, and under the bark. They will also cache whitebark pine seeds at and above treeline, among patches of conifers and in small depressions in open areas.
Whitebark pine seeds may be cached near source trees or transported 12 km or farther, often to higher or to lower elevations, where whitebark pine cannot grow. Other studies have indicated that nutcrackers may transport seeds even longer distances, e.g., for piñon pine, 22 km (Vander Wall and Balda 1977); and, for ponderosa pine, 30 km (Lorenz 2008). Nutcrackers appear to cache across a variety of terrain within their home range but also within communal storage areas, which are steep and south-facing slopes used by a local population of nutcrackers for caching. These slopes tend to be within 3 to 4 km of source trees.
Estimates of the numbers of whitebark pine seeds stored per bird within one season have been based on different assumptions and for different geographic regions, but vary from 35,000 seeds in about 9,500 caches in the eastern Sierra Nevada, California (Tomback) to 98,000 seeds in 30,600 caches in the Absaroka Mountains, Wyoming (Hutchins and Lanner). With these estimates, a population of 25 nutcrackers would store from 95,000 to 750,000 caches.
Seed morphology and delayed germination
The seeds in unretrieved nutcracker caches germinate following snow melt and spring and summer rains, resulting in single seedlings and clusters of seedlings appearing throughout whitebark pine communities. However, the nutcracker caching mode of seed dispersal has exerted selection pressure on both the seed structure and timing of germination in whitebark pine, as well as in other Cembrae pines. Both planting and natural experiments indicate that whitebark pine seeds typically require two or more winter dormancy cycles before they germinate. Therefore, seeds do not usually germinate within the next growing season following seed caching, but rather two or more growing seasons later, and germination seems to correspond to higher moisture availability. Rarely, the seeds within a cache may germinate in different years. Delayed germination may result from the short growing season in the subalpine zone coupled with the fact that nutcrackers are caching a proportion of seeds before seed development is complete, resulting in underdeveloped embryos. Seeds may also have physiological resistance to germination until available moisture is sufficient, an adaptation to increase survival.
There is evidence that seed structure and physiology in Cembrae pines have been shaped by selection pressure from nutcrackers for a seed caching mode of dispersal. Specifically, the seed structures and physiology of whitebark and Siberian stone pines, the two Cembrae pines examined to date, are similar to each other but very different from the structures of wind-dispersed conifer seeds and may facilitate continued viability of seeds and further maturation under soil (Tillman-Sutela et al. 2008). Thus, the seeds appear to be adapted to remaining within a seed soil bank created by nutcrackers.
Ecological and population impact of seed dispersal by nutcrackers
Seed dispersal by nutcrackers has diverse influences on the ecology of whitebark pine. For example, the sites selected by nutcrackers for seed caching, along with the environmental suitability of these sites for seed germination and seedling survival, determine where whitebark pine occurs on the landscape. The tendency of nutcrackers to cache seeds below and above the current elevational distribution of whitebark pine enables whitebark pine to respond rapidly to climate cooling or warming with changes in elevational and even latitudinal distribution. This influence is particularly important now, with climate warming predicted to cause an upward and northward shift in whitebark pine distribution.
Secondly, seed dispersal by nutcrackers is responsible for the genetic population structure of whitebark pine at several spatial scales. At the local level, the seed caching mode of seed dispersal results in a unique fine-scale genetic population structure. Because two or more whitebark pine seeds are often cached together, several seedlings from a cache may survive and produce a “tree cluster” growth form. This growth form appears to be a single tree with multiple stems, which are tightly clustered or fused at the base or part way up the stem. Genetic studies confirm that most of these tree cluster growth forms contain distinct individuals, each arising from a different seed within a cache. Also, because nutcrackers harvest from several seeds to an entire pouchload of seeds from a single tree, there is a high probability that the seeds within a cache are genetically related. Finally, within a given area, nutcrackers cache at random with respect to caches already present, and with seeds from different source trees. Consequently, the seedlings among neighboring caches are usually unrelated, resulting in a random genetic pattern among clusters. As a result of all these factors, the fine-scale genetic population structure of whitebark pine and other bird-dispersed pines is highly distinctive.
At the landscape and regional scale, we see the influence of nutcracker caching behavior as well on genetic population structure. Nutcrackers often disperse seeds over distances of several kilometers or more, which are far greater than the mean distances traveled by wind-dispersed conifer seeds, and easily move seeds over mountain passes and into adjacent drainages. Wind blows pollen over long distances as well. Consequently, researchers have found very little genetic differentiation among whitebark pine populations at both a landscape level and regional level; this genetic differentiation is lower than found for wind-dispersed conifer seeds.
At a nearly range-wide scale, genetic analysis has revealed population structure likely resulting from whitebark pine range expansion out of three Pleistocene glacial refugia. These refugia represent geographic areas of suitable environmental conditions for whitebark pine when glaciation reached its maximum extent in North America. These three populations, isolated from one another, diverged genetically over time in their mitochondrial DNA, which evolves rapidly. After the glaciers retreated, seed dispersal by nutcrackers enabled whitebark pine populations to expand out of these refugia. The boundaries among these historical populations may be beyond the limits of seed dispersal distances flown by nutcrackers, and so are evident today.
References
Lanner, R M. 1996. Made for each other: A symbiosis of birds and pines. Oxford University Press, New York, New York, USA.
Lorenz, T. 2008. Telemetry study with Clark’s Nutcracker: An update. Nutcracker Notes, Issue No. 15: Autumn/Winter 2008, pp16-19.
Tillman-Sutela, E., A. Kauppi, K. Karppinen, and D. F. Tomback. 2008. Variant maturity in seed structures of Pinus albicaulis (Engelm.) and Pinus sibirica (DuTour): key to a soil seed bank, unusual among conifers? Trees 22: 225-236.
Tomback, D.F. 1983. Nutcrackers and pines: coevolution or coadaption? In: Nitecki, M.H. (Ed.): Coevolution. University of Chicago Press, Chicago, Illinois, USA, 179-223.
Tomback, D. F. 1998. Clark’s Nutcracker (Nucifraga columbiana), No. 331. In: Poole, A. & F. Gill (Eds.): The birds of North America. The Birds of North America, Inc., Philadelphia, Pennsylvania, USA.
Tomback, D.F. 2001. Clark’s nutcracker: Agent of regeneration. In: Tomback, D. F., S.F. Arno, & R.E. Keane (Eds.): Whitebark pine communities: ecology and restoration. Island Press, Washington, D. C., USA, 89-104.
Tomback, D.F. 2005. The impact of seed dispersal by Clark’s nutcracker on whitebark pine: multi-scale perspective on a high mountain mutualism. In: Broll, G.,& B. Keplin, (Eds.): Mountain Ecosystems: Studies in Treeline Ecology. Springer, Berlin, Germany, 181-201.
Tomback, D.F., and Y.B. Linhart. 1990. The evolution of bird-dispersed pines. Evolutionary Ecology 4: 185-219.
