More info for the terms: competition, cover, density, fresh, litter, mast, phase, phenology, presence, selection, series, shrubs, tree
Clark’s nutcrackers have a complex sequence of foraging patterns that centers on year-round use of pine seeds as a primary food source. Since pine seeds are plentiful for only a brief time in late summer and early fall, an individual Clark’s nutcracker must harvest and store enough seeds to ensure a food supply for the rest of the year. The seed harvest and storage period lasts 50 to 75 days under favorable conditions and depends on size of the seed crop, the number of Clark's nutcrackers, and competition from other animals foraging for seeds [41,167]. Cache recovery occurs during the winter, spring, and much of the summer [167].
Clark's nutcracker with a full sublingual pouch harvesting whitebark pine seeds.
ClarkÂs nutcrackers store food by means of scatter-hoarding: burying many small, discrete clusters (caches) of seeds throughout montane forests (see Caching). The collective supply of pine seeds (thousands of caches) cached by an individual bird during the annual cycle is referred to as its Âseed stores [137,139].
Morphological and behavioral adaptations: ClarkÂs nutcrackers are well adapted to harvest seeds from pine cones. They have long, heavy, sharp bills that they use to break open cones. Many of the conifer species utilized by ClarkÂs nutcrackers have seeds that are retained in the cone after seed ripening. By jabbing and stabbing at cones, ClarkÂs nutcrackers break off cone scales and use their long, tweezer-like bills to extract seeds [72]. They also use their bills to push seeds into the soil one at a time [137].
To collect and transport seeds, the ClarkÂs nutcracker uses a sublingual pouch that is unique to the genus Nucifraga. The sublingual pouch is a saclike extension of the floor of the mouth that opens under the tongue [18]. As it removes seeds from cones, the ClarkÂs nutcracker collects the seeds temporarily in its sublingual pouch, a behavior called "pouching". When its pouch is full, the ClarkÂs nutcracker transports seeds to cache sites, where the seeds are stored until recovered and eaten. The Clark's nutcracker also uses its sublingual pouch to transport cached seeds to nestlings and dependent juveniles [137].
The flight of ClarkÂs nutcrackers is characterized as strong, bold, direct, and generally well above the forest canopy [169]; long, pointed wings are adaptations for strong flight. Use of updrafts and winds to gain lift in mountainous landscapes apparently enables Clark's nutcrackers to conserve energy when hauling heavy pouch loads long distances or to high-elevation cache sites [169]. ClarkÂs nutcrackers can fly with pouch loads that exceed 20% of their body weight [170].
The ClarkÂs nutcracker is described as an optimal forager when harvesting conifer seedspreferring to harvest pine seeds that offer the shortest search and/or handling time [137,155]. When presented with a choice between species, the ClarkÂs nutcracker apparently selects the option with the greatest foraging efficiency, ultimately maximizing the total number of seeds obtained [155]. Selection between preferred species apparently corresponds to cone-ripening phenology; by choosing the pine species that ripens first, ClarkÂs nutcrackers have the opportunity to use preferred species sequentially, prolonging their ability to store seeds [137,160] (see Seed utilization patterns).
Within a selected food species, ClarkÂs nutcrackers forage in a manner that that maximizes the efficiency of the seed harvest, first tending to choose populations that produce the largest seed crops and then discriminating among trees according to cone characteristics and seed crop size [24,167]. Numerous studies describe apparent selection of stands where cones ripen early [137], trees with high cone densities [16,24,155], and cones with high proportion of edible seeds [155,169]. For a further discussion of foraging efficiency, see Tomback and Linhart [156].
Harvestingfeeding and pouching: As the previous yearÂs seed stores become depleted in early summer, ClarkÂs nutcrackers usually begin foraging on fresh seed from the ripening cones of large-seeded pines. Individuals extract seeds for their own immediate consumption and/or for feeding to dependent juveniles. Foraging typically occurs singly, in pairs, or in small loose flocks [169]. Seeds from the ripening seed crop become an increasingly important part of the diet in late summer. On subalpine sites in the Sierra Nevada, ClarkÂs nutcrackers focus on partially ripe whitebark pine seeds by mid-July [137]. Unripe cones are hard to break open because they are tightly closed, so ClarkÂs nutcrackers must shred the pulpy cone scales with their sharp bills to remove seeds. Foraging takes place in tree canopies because cones remain attached to the tree. Cones are clustered at branch tips and are oriented horizontally in relation to the upswept branches, providing a stable platform for ClarkÂs nutcrackers to work from [137]. When foraging on unripe cones of limber pine and singleleaf pinyon (but rarely whitebark pine), Clark's nutcrackers frequently detach unripe cones and fly to a branch near the tree bole, where they hammer the closed scales open [71,169].
When eating unripe seeds, ClarkÂs nutcrackers expend a lot of energy and time for little energy gain [167], but they may be assessing the developing seed crop (seed density and soundness). Early foraging may alert ClarkÂs nutcrackers to an impending seed shortage, allowing time for relocation if necessary [169,171].
During the first 2 to 3 weeks of the whitebark pine harvest season, Clark's nutcrackers eat nearly all seeds they remove from cones [30]. ClarkÂs nutcrackers shift from seed consumption to seed storage as cones mature and foraging efficiency increases. As whitebark pine seeds ripen, cones turn from purple to brown and the cone material dehydrates, causing the scales to loosen and separate slightly [41,42]. Easy removal of whole seeds signals the start of whitebark pine seed storage in the Sierra Nevada [160]. When cones are ripe, ClarkÂs nutcrackers use well-placed bill stabs to detach the upper portions of cone scales along a thin fracture zone, exposing seeds held in the core of the cone. Ripened seeds are firm and encased in woody seedcoats, allowing the ClarkÂs nutcracker to extract seeds and collect them in its sublingual pouch, an indication that these seeds will be cached instead of eaten. The seed coat is usually retained when seeds are pouched [137].
ClarkÂs nutcrackers are highly selective when harvesting seeds for caching; they peer into and probe cones, extracting only edible seeds for the most part. A dark seedcoat is a visual cue of high seed quality in whitebark pine [41,137] and Colorado pinyon seeds [169]. Energy content of fully ripe seeds is nearly optimal; dry mass and caloric value/unit mass generally increase as seeds ripen [167]. Before "pouching" a seed, it is tested for edibility. The ClarkÂs nutcracker rattles the seed between its mandibles, a behavior known as Âbill clicking and also holds it between the mandibles for several seconds, a behavior known as Âbill-weighing [137,169].
ClarkÂs nutcrackers usually feed on pine seeds for several minutes before filling their sublingual pouches [137,169]. When foraging on singleleaf pinyon seeds, ClarkÂs nutcrackers consumed 5 to 15 seeds before beginning to pouch seeds [169]. Seeds are consumed as they are extracted. Clark's nutcrackers typically remove seed hulls prior to swallowing by cracking the seed between the mandibles [137,160]. Once pouching is initiated, feeding does not occur again until the pouch is emptied [167].
When ClarkÂs nutcrackers are transporting seeds they typically make direct, nonstop flights between harvest sites and storage areas [167], although Tomback [137] reported that ClarkÂs nutcrackers frequently rested in the tops of tall trees when making long flights. Caching flights comprised the most energetically demanding phase of the harvesting process [170]. Once pouches are filled, Clark's nutcrackers transport the harvested seed to storage sites. Maximum number of seeds/pouch load depends on seed size and is summarized by Tomback [145] and Lanner [71]. From observations in the Sierra Nevada, Tomback estimated a single pouch load of whitebark pine seeds consisted of 35 to 150 seeds (x=77 (SD 37) seeds; median=58; n=13) [160].
ClarkÂs nutcrackers occur in loose flocks during the summer and fall harvest season and also in early winter before they begin to rely on stored pine seeds [137]. Since food supplies are typically patchy but locally abundant, foraging coloniality allows ClarkÂs nutcrackers to concentrate harvesting efforts in areas where food is most abundant, thereby increasing foraging efficiency [34]. More individuals searching for food increases the likelihood of finding a concentrated patch of preferred seeds. In addition, colonial foraging appears to permit younger and less skilled ClarkÂs nutcrackers to learn about food sources from older, more proficient foragers [30]. In the Washington Cascade Range, Lorenz [85] found that emigrant Clark's nutcrackers foraged and cached in large, vocal flocks of 50 to 200 individuals; by comparison, resident Clark's nutcrackers usually foraged and cached either singly or in small groups of 2 to 10 nutcrackers.
Cones that are worked by Clark’s nutcrackers have a distinct appearance. Frayed cone scales are an indication of harvesting activity on closed cones. Clark’s nutcrackers shred the pulpy scales with their beaks to gain access to the seeds beneath, usually beginning at the proximal end [169]. When extracting seeds from ripe whitebark pine cones, Clark’s nutcrackers typically select cone scales most easily accessed—those facing upward or sideways on the horizontally oriented cone. Because unripe seeds on the underside are often not extracted until later in the season, many cones are only partially harvested and have a hollowed-out appearance [137,142]. In comparison, rodents (chipmunks) most commonly chew off all the cone scales and leave only a core of the cone [137].
Photo courtesy of the Whitebark Pine ecosystem Foundation.
Timing, duration, and size of harvest: Timing of the autumn seed harvest is highly variable from year to year and depends upon the influence of local weather and site conditions on cone-ripening phenology [147]. An indication Clark's nutcrackers have begun harvesting whitebark pine cones is the presence of purple pitch on their bills and faces [30,137].
Dates of initial harvest, initial caching, and the end of the caching season are presented below. Site information and seed crop size for some of these studies are summarized in a review [86].
Timing of Clark's nutcracker seed harvest and caching of food species by geographic location Species Start harvest Start caching Harvest complete Location Whitebark pine 4 August
15-23 >August
late October Wyoming (Absaroka Mountains) [41] first observed caching: 10 August 2006
8 August 2007 Washington (Cascade Range) [85] observed caching 12-14 September Nevada (Jarbidge Mountains) [130] Limber pine ---* 26 August late November Wyoming (Absaroka Mountains) [167] 20 August 28 August late October Colorado (Front Range) [15] 5 September (observed caching) California (Sierra Nevada) [155]
first observed harvesting: 27 July 1985
7 August 1986
first observed caching: early September 1985
26 August 1986
Colorado (Rocky Mountain National Park) [143] observed harvesting from closed cones and caching
9-11 August Nevada (Schell Creek Range) Southwestern white pine started caching 27 August Colorado (San Juan Mountains) [121] Colorado pinyon Late August --- late October Arizona (San Francisco Mountains)[169] Singleleaf pinyon late July 28 August late October Utah (Raft River Mountains) [167] Jeffrey pine --- 18 September 1976
16 October 1975 7 December 1975 California (Sierra Nevada) [160] Ponderosa pine early October --- mid-November Colorado (Front Range) [161] early November early November --- Colorado (Front Range) [15] Rocky Mountain bristlecone pine mid-October --- --- Colorado (Front Range) [15] *No data.
The timing of seed pouching and caching of the year's seed crop vary from year to year within the same locality and depend on many factors. Three consecutive years of observational data for whitebark pine seed harvesting on subalpine sites in the Sierra Nevada indicate the initiation of seed caching varied as much as 2 weeks between years [137].
Beginning dates of whitebark pine seed harvesting by Clark's nutcrackers on sites in the Sierra Nevada [137]
Foraging behavior
Harvesting and consuming unripe seeds Harvesting and caching mature seeds Dates initiated 19 July 1973
1 August 1974
2 August 1975 25 August 1973
29 August 1974
8 September 1975
Clark's nutcrackers harvested and cached pine seeds from closed cones in isolated mountain ranges in Nevada. In the Schell Creek Range, researchers observed limber pine caching from 9 to 11 August; in the Jarbidge Mountains, they observed whitebark pine caching from 12 to 14 September. By these dates, ClarkÂs nutcrackers on the 2 sites had harvested seeds from more than 50% of the trees sampled [130].
The ClarkÂs nutcracker harvests and stores the yearÂs seed crop rapidly, working intensely until the seed resource is depleted. At the height of harvest season, Clark's nutcrackers are highly active, commonly spending almost all daylight hours storing pine seed [137,167]. Hutchins and Lanner [41] observed pronounced seed harvesting and storage occurring approximately 9 hours/day (regardless of day length) on subalpine sites in western Wyoming. On hot upper-subalpine sites in the Sierra Nevada, harvest and storage usually occurred during the cooler portions of the day, typically 2 to 3 hours after sunrise and 2 to 3 hours in the late afternoon and early evening [141,160]. Vander Wall [167] also noted a decline in caching during midday for Clark's nutcrackers using hot pinyon-juniper sites in the Raft River Mountains of Utah.
The size of the Clark's nutcracker harvest depends of the size of the seed crop, with harvesting and caching occurring as long as seeds are available [41]. The effect of seed crop size on the duration of the harvest season is shown below.
Length of Clark's nutcracker harvest season over 3 consecutive years on sites in the eastern Sierra Nevada [30] Year Seed crop size Length of harvest season
(days) Length of caching season
(days) 1989 small 63-70 40-50 1990 large 107 77 1991 medium-large 99 60
During a mast year, a single ClarkÂs nutcracker can store large quantities of seed, estimated at 32,000 [141] to 98,000 seeds [41]. On subalpine sites the Sierra Nevada, one ClarkÂs nutcracker may cache an estimated 850 whitebark pine seeds/day [153]; over a harvest season, one bird may make at least 7,700 separate whitebark pine seed caches. During good seed crop years, cached seeds provide approximately 2.3 to 3 times the energetic requirements of an individual. This extra energy is required for reproduction and feeding nestlings and fledged juveniles [137,169]. Besides ensuring that at least some caches are accessible during all times of the year, excess caching apparently also provides a margin for loss due to rodent predation, seed spoilage, and Âforgetting cache locations [12,141] (see Foraging and caching).
Nonstop caching essentially saturates the subalpine landscape with seed caches in a good seed crop year. A population of 25 ClarkÂs nutcrackers stored an estimated 800,000 seeds within a 120-acre (50 ha) area in the eastern Sierra Nevada [141]; another population of 150 ClarkÂs nutcrackers stored between 3 and 5 million Colorado pinyon seeds in northern Arizona [169].
Caching: Seed caching behavior is fairly consistent throughout the ClarkÂs nutcrackerÂs range. Cache distribution within montane habitatslocal and communal cache placement, distances between harvest trees and caching areas, changes in elevation between harvest trees and cache sites, and cache micrositesappear highly variable and reflect a population's use of the local habitat (see Caching habitat).
Caching behavior: Seed caching is a ritualized behavior and takes about 30 seconds/cache [51]. When caching in forest litter or mineral soil, a ClarkÂs nutcracker digs a shallow trench with sideswipes of its bill, inserts one to several seeds into the soil (one at a time), rakes soil and litter over the cache site, and, in many cases, places a large piece of litter (pine cone, pebbles, leaves, snow) at the site [137,166,169]. If caching in volcanic substrates, ClarkÂs nutcrackers may push seeds into the soil without preliminary preparations [137]. Whitebark pine seeds are buried 0.4 to 1 inch (1-3 cm); cache size ranges from 1 to 15 or more seeds, with a mean cache size of 2.6 to 5.2 seeds/cache [137]. A ClarkÂs nutcracker typically makes several caches in the same area, then flies a short distance to an adjacent area and makes another series of caches, continuing to cache until the sublingual pouch is empty. Tomback [137] reports nearest-neighbor distances ranging from 3.9 to 118 inches (10-300 cm) between caches within a series. See Tomback [137] for detailed information on caching behavior.
ClarkÂs nutcrackers typically work alone while caching [169] but may be part of flocks of up to 150 birds caching concurrently [41]. For example, on Mt Washburn in Yellowstone National Park, groups of 10 to 15 ClarkÂs nutcrackers cached together within a 100-m² area on several different occasions without aggressive interactions [41].
Cache distribution: The ClarkÂs nutcracker typically distributes seed caches in 2 wayscaching locally near source trees or traveling some distance to communal caching areas [41,62,148] (see Arrangement of seed caches).
When caching close to source trees, caches are scattered throughout nearby terrain at distances from 6.6 to 660 feet (2-200 m) [137]. In communal storage areas, however, many ClarkÂs nutcrackers intermix their caches, thus concentrating a high density of caches throughout the communal area. Vander Wall [167] indicates seeds cached near source trees represent only 10% to 20% of the total seeds stores of a ClarkÂs nutcrackers (see Caching habitat for more details on characteristics of cache sites).
Although communal storage areas may be adjacent to large stands of preferred seed trees, Clark's nutcrackers also transport seeds long distances to use communal cache sites. The distance between seed sources and storage areas is highly variable. ClarkÂs nutcrackers may travel up to 18 miles (29 km) to cache seeds; however, shorter distances of up to 1.2 miles (1.9 km) are more common [41,137,167]. Vander Wall and Balda [169] indicate ClarkÂs nutcrackers harvest seeds from trees nearest communal storage sites first; foraging distance from the communal cache site increases as ripe seeds from the closest trees become depleted. Sund [134] reports ClarkÂs nutcrackers tend to bury more seeds/cache when transporting seeds long distances.
Recaching: A portion of the seed cached near source trees may be stored only temporarily. ClarkÂs nutcrackers often make caches within 300 feet (100 m) of the harvest site and later recache seeds on communal storage slopes [41,137]. Recaching appears to increase the number of seeds harvested/individual by reducing time-consuming flights to communal storage areas. Temporary caching may allow ClarkÂs nutcrackers to rapidly store the available seed crop in the ground, where seeds are concealed from direct predation. As the harvest winds down, locally cached seeds can be moved, without loss of harvesting opportunities, to sites with better winter access and where seed predation is less likely [42] (see Seed cache predation). For more information on ClarkÂs nutcracker Foraging behavior during poor seed crop years, see Migration and Irruptions and extralimital wandering.
Retrieving caches: The magnitude of ClarkÂs nutcracker seed caching efforts is remarkable, and the species possesses a noteworthy spatial memory that enables precise and accurate relocation of thousands of seed caches made during the previous harvest season. ClarkÂs nutcrackers recover cached seeds over a 6- to 9-month period extending from winter through late summer [41,137,169].
A ClarkÂs nutcracker remembers the precise location of its seed caches through the use of a large-capacity, well-developed spatial memory [52,139]. Large objects such as rocks, logs, and shrubs serve as visual cues during cache recovery [137,166] (see Cache microsites). ClarkÂs nutcrackers can accurately relocate seed caches up to 9 months after making them [12,166]; accuracy begins to decline between 183 and 285 days after caching [12]. Laboratory research indicates Clark's nutcrackers possess several levels of memory organization to recall information regarding caches. Some research suggests that a ClarkÂs nutcracker remembers some cache locations better than others, and these caches are among the first ones recovered [14]. Apparently ClarkÂs nutcrackers can track which caches have been emptied [53]. Clark's nutcrackers also remember the size of seeds within a cache [100].
Although the location of a cache is remembered in relation to other objects in the landscape, it is unclear how ClarkÂs nutcrackers can retrieve caches from sites that have been visually altered since cache creationfor instance, sites where snow cover removes many visual landmarks or where green vegetation dies back to ground level. Local landmarks are apparently only one factor utilized during cache recovery [13]. For a detailed discussion of research involving the memory capabilities of ClarkÂs nutcrackers, see Balda and Kamil [13] and Lanner [75].
When relocating a seed cache from memory, a ClarkÂs nutcracker first perches on a tree near the cache area and surveys the adjacent terrain, apparently selecting a site for cache retrieval. It then drops to the forest floor and begins probing a spot by thrusting its bill into the soil or by digging a trench with sideswiping motions of its bill. Once a seed is located, sideswiping behavior continues until all seeds within a cache are located and removed. Seeds are either cracked and eaten at the recovery site, leaving behind a pile of seed hulls, or pouched and transported to the nest site to feed young. ClarkÂs nutcrackers usually locate several nearby seed caches before moving on to a new area [137]. See Tomback [137,160] for further information on cache recovery behaviors.
Winter cache retrieval: Studies of winter cache retrieval were uncommon as of 2008. In the Sierra Nevada, ClarkÂs nutcrackers apparently prefer retrieving seed caches from snow-free patches or areas with minimal amounts of snow. Following heavy snowstorms, ClarkÂs nutcrackers rely heavily on seed caches located on steep, wind-swept communal storage slopes [160].
Winter cache retrieval apparently occurs from memory. ClarkÂs nutcrackers access caches by digging through the least snow possible. For instance, on high-elevation meadow sites used year-round by ClarkÂs nutcrackers in Wyoming, Clark's nutcrackers became totally dependent on cached seed by 2 November, when snow blanketed most of the basin. Although snow depths sometimes reached 49.2 feet (15.0 m) at this subalpine location, caches on windswept, rocky moraine ridges and south-facing cliffs remained exposed enough to allow ClarkÂs nutcrackers access. One ClarkÂs nutcracker successfully pecked through 10 inches (25 cm) of snow to retrieve a cache [41].
Winter cache retrieval has been more thoroughly studied in the European nutcracker. Crocq (1990, cited in [90]) reports European nutcrackers leave subalpine habitats when snow depths reach 70 inches (170 cm). European nutcrackers have been documented tunneling through snow to recover caches; successful efforts at cache retrieval occurred over snow tunnel distances of 50 inches (130 cm) and 120 inches (300 cm) (Stern 1994, personal communication cited in [90]).
Spring and summer cache retrieval: As weather moderates and melting snow becomes widespread, Clark's nutcrackers recover seed caches from newly exposed, wet areas near receding snow patches [137]. For example, seeds cached on sites where snow lingers (northeast-facing slopes and under the forest canopy) are used more in summer than in winter [41].
ClarkÂs nutcrackers sometimes continue to recover the previous yearÂs caches while harvesting and caching the current yearÂs crop [41,137]. Occasionally, recovered seeds from the previous crop are cached again, even though many may have already germinated [41]. In a review, Mattes [90] suggests nutcrackers (Nucifraga spp.) sometimes relocate and then recache the previous yearÂs seed caches, particularly if the current seed crop is poor.
Cache retrieval methods may be influenced by a Clark's nutcracker's migratory status. Studies of radio-tagged Clark's nutcrackers in the Washington Cascade Range found resident individuals used memory when locating caches placed within a 120-acre (500 ha) home range (Lorenz and Sullivan 2008, cited in [10]). Emigrant Clark's nutcrackers, however, located whitebark caches by searching for germinating seedlings on communal caching grounds [85].
Other foraging methods: Although ClarkÂs nutcrackers forage primarily on seeds in pine tree crowns, they are opportunistic and employ a variety of foraging methods throughout the year. Versatile bills enable them to probe for insects, kill small vertebrates, and feed on carrion [147]. Clark's nutcrackers glean insects and spiders from vegetation, soil, fallen pine cones, rotten logs, and stumps [147,161]. Other methods include fly-catching, bark-flaking, flying from perch to ground, scavenging, and preying upon other birds and small invertebrates [17,147] (see Diet).
During the winter and early spring, small groups of ClarkÂs nutcrackers forage intensely for unharvested seed in trees and on the ground. On Jeffrey pine sites in the eastern Sierra Nevada, Tomback [160] observed ClarkÂs nutcrackers foraging on fallen Jeffrey pine cones; Clark's nutcrackers first ate seeds that had fallen onto the ground, then ate seeds remaining in open cone scales, and finally opened any closed cone scales to remove remaining seeds.