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LINKING LIFE ZONES, LIFE HISTORY TRAITS, ECOLOGY, AND
SPATIAL COGNITION IN FOUR ALLOPATRIC SOUTHWESTERN SEED CACHING CORVIDS:
By
Russell P. Balda, Avian Cognition Laboratory, Department of Biological
Sciences, Northern Arizona University, Flagstaff AZ.
Alan C. Kamil, Center for Avian Cognition, School of Biological Sciences, Department of Psychology, University
of Nebraska, Lincoln NB
INTRODUCTION
Temperate and alpine regions experience large climatic shifts
between summer and winter. To survive, animals must deal with these seasonal changes.
Tactics used to address with these changing conditions include migration, hibernation, laying over-wintering eggs, or Aliving off the land@ (finding food and shelter under changing
conditions). Animals that live off the land, are referred to as permanent
residents. Often these animals have to change the amount and types of foods
they eat to accommodate the energetic and nutritional demands imposed by the
physiological needs of the different seasons of the year. For example, most permanent resident birds eat
insects and arachnids during the summer when these food types are abundant, and
seeds, berries and over-wintering eggs and larvae, during the winter when these
food items may be abundant. Some birds, however, do something quite
different. They Aprepare@ for the upcoming winter by provisioning food in the late summer
and autumn and then recover and consume it during the harsh winter season,
days, weeks, even months after the items were initially stored. In this chapter
we will define the ecological conditions under which these behaviors occur and
the suite of adaptive behaviors used by
the birds in their quest for survival and reproduction.
Food-storing adaptations have been observed in
many avian taxa, including woodpeckers, nuthatches, chickadees and tits (see Vander
Wall 1990 for review of this topic). In this chapter, we will concentrate on a
group of seed caching birds of the family Corvidae, the Clark’s nutcracker (Nucifraga columbiana), pinyon jay (Gymnorhinus cyanocephalus), Western scrub jay (Aphelocoma californica) and Mexican jay (Aphelocoma ultramarine) that co-exist in a relatively small area of
north-central Arizona, the San Francisco Peaks (Figure1.).
These peaks are geographically compact and isolated from other mountainous
areas, thus providing an unusual natural laboratory to study food-storing,
particularly for describing similarities and differences among the four
species.
In the first part of this chapter, we describe
in some detail the habitats occupied and utilized by the seed caching
corvids. In succeeding sections, we use
this background information to illustrate the how and why these conditions, acting
as selective forces, have affected the behavioral patterns of these birds.
The San Francisco Peaks were made famous in the
1880's when they were studied by C. Hart Merriam, an early ecologist and the
first
Director of the present U.S. Fish and Wildlife
Service (Figure 2). He described the distribution of
plants and animals along an elevational gradient
on the sides of the Peaks and compared this distribution to the latitudinal
distribution of plants and animals from temperate to arctic regions of the
eastern U S. He published a famous
monograph on this topic in 1889 (Figure 3). Bands of like plants and animals
that had the same elevational distribution were referred to as LIFE ZONES (Figure
4.).Because the mountain is rather simple, both geologically and
geographically, the zones were relatively easy to identify and describe. It was possible to visit all the life zones on
the Peaks in half a day. This made it easy to record the similarities and
differences in the behaviors of the birds of interest.
A brief
description of the life zones on the San Francisco Peaks, beginning with the
highest elevations and moving downward, will set the stage for understanding
the ecological reasons that these seed caching birds behave as they do.
The San Francisco
Peaks
1. Alpine Tundra. (Figure 5) This zone exists on
the very top of the Peaks, 3,865 m (12,670 ft). Vegetation here is sparse. This
area is above tree line and supports only two small species of shrubs. At tree
line there are small gnarled patches of Engelmann spruce (Picea engelmannii)
and bristlecone pine (Pinus aristata). In winter, the tundra zone is
subjected to strong winds, low temperatures and heavy snow that may be present
in protected pockets well into summer. Summer rains can be torrential. The growing season is short as freezing
temperatures can occur in May and August. The single seed caching corvid that regularly
visits this zone is the Clark’s nutcracker and it does so in late summer and early fall before
the snow flies. Here it can be found with its offspring of the year, foraging,
digging in the soil, catching insects, and caching seeds of bristle cone pine,
limber pine (Pinus flexilis), and southwestern white pine (Pinus
strobiformes) that are carried upward by the adults as the seeds mature at
lower elevations in late summer and early fall. All or most of this activity by
nutcrackers ceases once the zone is covered with snow. Thus, these cached seeds
are not recovered until the area is free of snow the next spring and summer,
some 8-10 months later.
2. Spruce-fir Forest. (Figure 6.) This zone of
dense coniferous trees consisting of Engelmann spruce, alpine fir (Abies
lasiocarpus), limber pine and bristle cone pine exists directly below the
tundra at elevations from about 2,745 m (9,000 ft.) to 3,660 m (12,000 ft).
Forests can be dense with a continuous layer of canopy cover so thick that few
under story plants can thrive in this extreme shade. A thick layer of litter
and duff covers the ground in most areas. Grassy alpine meadows are
interspersed with tree covered areas. This zone is characterized by high winds,
heavy snow fall in winter and rain fall in summer, cold winter temperatures and
cool summer temperatures. Clark=s nutcrackers and Steller=s jays (Cyanocitta stelleri) are common inhabitants of this
zone. Both nest here, extract seeds from the cones of both species of pine, and
readily cache seeds here. (Although Steller’s jays are industrious cachers we have studied them little because
they do not do well in captivity.) Occasionally in late summer and early fall
flocks of pinyon jays can be seen and heard traveling through the area.
Presumably, these birds are searching for pine seeds.
3. Mixed Coniferous Forest. (Figure 7.) This
zone exists at elevations between 2,287 m (7,500 ft) and 2,745 m (9,000 ft). The
principal trees are firs, primarily Douglas fir (Pseudotsuga menziesi)
with occasional white firs (Abies concolor) and ponderosa pines (Pinus
ponderosa) found on warmer exposures. Here, two closely related species of
pine intergrade, the southwestern white pine (Pinus strobiformis) and
the limber pine (Pinus flexilus), and form large stands on the side of
the Peaks. A deciduous tree, Gambel oak
(Quercus gambeli) is present in low numbers. The canopy is complete so
the forest floor is well shaded and contains a thick mat of litter and duff.
Alpine meadows and stands of quaking aspen (Populus tremuloides) are
interspersed among the conifer stands. Winters are cold and windy, with heavy
snows at times and modest amounts of summer rains. Climatic conditions in this
zone are more moderate than in the above spruce-fir zone, but still rather
harsh in winter. Clark=s nutcrackers and Steller=s jays are the principal seed caching corvids
inhabiting this zone with occasional visitations by flocks of pinyon jays.
4. Ponderosa Pine Forest. (Figure 8.) This zone is present from 2,105 m
(6,900 ft) to 2,287 m (7,500 ft) .This forest is a monoculture, as the dominant
and predominant tree is ponderosa pine. In some areas Gambel oak may be present
at modest densities. Ponderosa pine forest form open stands of large trees, in
contrast to the above forests where the canopy is complete. Pine nettles and
cones from past years accumulate on the forest floor and can form a thick mat
of 5-10 cm. In some areas pine trees are dense and small forming Adog-hair thickets@. Winters are modest with snowfall amount below
those experiences in the above zones with summer rains also occurring in
moderation. The growing season extends from late April to early September. In
recent years wild fires have commonly consumed large tracts of this forest. This
is the lowest elevational extension of the coniferous forest on the peaks. Steller=s Jays occur at maximum densities here and readily caches the
seeds of ponderosa pines. These jays also descend to the upper reaches of the
next lower zone to harvest and carry pine seeds up into this forest. Flocks of
pinyon jays roam through portions of this forest, harvesting and caching
ponderosa pine seeds and, like the Steller’s jay descending into the woodland to harvest and carry seeds up
into this zone. Pinyon jays commonly nest in this forest. At the lower edges of
this zone and on drier sites Western scrub-jays and Mexican jays occur. They
also harvest and cache ponderosa pine and pinyon pine seeds here.
5. Pinyon-Juniper Woodland. (Figure 9.) This
extensive zone occupies the base of the mountain and lies between 1,680 m (5,500
ft) and 2,135 m (7,000 ft). This zone occupies the largest amount of area of
all the zones because there is more land mass at the lower elevation where these
trees live. The predominant trees are Colorado pinyon (Pinus edulis) and
a host of junipers (Juniperus osteosperma, J. monophylla, J.
scopulorum, J depppeana). The upper elevations are dominated by pinyon pine and the lower regions may consist
solely of junipers. Because moisture is limiting, trees are spread out with
large openings between them. The under story supports some shrubs, succulents and cacti. The climate is mild in winter and hot in
summer. Modest rains occur in summer and winter moisture is in the form of both
rain and snow. Winter snows melt relatively quickly. Insects and arachnids and
some small mammals are active throughout the year. Populations of western scrub jays and Mexican
jays reached their highest levels here. These jays harvest and cache pinyon
pine seeds when available. Also resident, are flocks of pinyon jays that use
the pinyon pines in great numbers. Steller=s jays and Clark=s nutcrackers descend the mountain and collect large amounts of pine
seeds that they then carry up into their normal habitats. The pinyon pine is
the most heavily sought after pine on the San Francisco Peaks.
Some
important ecological patterns emerge along the Life Zone gradient. At the top
of the mountain it is cold in winter, with heavy snow, but cool in summer with
heavy rains, and frequent clouds that obscure the sun, especially in winter and
mid-summer. Plant and animal productivity is restricted by a short growing
season in late spring and summer. In the higher coniferous forests, tree
density is high and canopies are closed, with a thick layer of decomposing
plant parts on the ground. At lower elevations, it is cool but mild in winter,
with little snow, but hot in summer, with sparse rains. Clouds are much less
frequent than at higher elevations. Plant and animal productivity is spread out
over a 9-10 month period and most animals remain active year round due to the
mild and hospitable climatic conditions. The pine forest and woodland have an
open canopy with sunlight reaching ground level throughout. Almost no plant
decomposition is occurring on the woodland floor and bare ground is often
exposed.
Consequently, each Life Zone has a unique set
of ecological properties and constraints that act as selective forces shaping
the adaptive traits of the creatures inhabiting it. Because of the compactness
of the mountain and the compressed nature of these adaptive zones it was
relatively easy to observe the similarities and differences among the seed
caching corvids.
There is a general trend of increasing numbers
of seed caching corvids species with decreasing elevation throughout the forest
and woodland zones. For example, only
the nutcracker visits the alpine tundra, but all five species (nutcracker,
Steller’s jay, pinyon jay,
western scrub jay, and Mexican jay) visit the pinyon-juniper woodland. In the
high coniferous forests the nutcracker and Steller=s jay are resident whereas in the low woodland
three species of jays (pinyon jay, Western scrub jay and Mexican jay) are
resident. Only the scrub jay apparently uses the grassland which occurs below
the woodland.
The Trees
On the slopes of the San Francisco four species
of pines produce seeds that are harvested, transported, cached and later
recovered by the seed caching corvids. In order of descending importance to the
birds these are: pinyon pine, limber/southwestern pine, ponderosa pine, and
bristlecone pine. A brief description of the characteristics of each that make
them attractive to the seed caching birds follows in order of descending
elevational distribution.
A. Bristlecone pine. This species is the rarest
of the pines and exists at the highest elevations, usually at or near tree line
in the spruce-fir forest. The seeds are tiny, ranging in size of between 10-13
mm (Schopmeyer 1974) and contain a 10-13 mm wing. The seeds are grey to brown
to black. The cone, as the trees name indicates, is armed with narrow, sharp,
pointed needle-like spines to protect the seeds from predators. The cone is
oriented downward on the branch. Bristlecone pine produces some cones most
every year, and seeds readily fall when they open. This pine relies mainly on
wind to disperse its seeds, and little is known about the harvest transport,
caching and recovery of this species by seed caching corvids, primarily Clark=s nutcrackers and Steller=s jays. This pine is probably not a significant
source of food for either of these species.
B. Limber and southwestern white pine complex.
This species complex reaches its high densities in the mixed coniferous forest
with a few individuals extending upward in the spruce-fir forest and down into
the upper edge of the ponderosa pine forest. (On the San Francisco Peaks these
two species interbreed thus we refer to them here as “a species complex”) The wingless seeds are relatively small (10-15 mm in length) and
brown in color. The cone contains either weak spines or no spines at all. Cones
are oriented downward. This pine is prized by nutcrackers and Steller=s jays which work with great industry to harvest
the seeds, which are cached within this forest type and in nearby open meadows
(Benkman et al. 1984). Both Steller’s jays and nutcrackers extract the seeds from open cones. Pinyon jays occasionally visit these trees in
late autumn, harvest seeds and carry them down hill into the ponderosa pine
forest and pinyon-juniper woodland where they are cached.
C. Ponderosa pine. This species exists in almost
pure stands below the mixed coniferous forest. The tree produces some cones in
almost every year and huge crops in some years. The small seeds (3-4 mm in
length) are attached to a wing that may be five times as long as the seed (16
mm in length). The seed coat is brown with occasional dark mottling. Cones
contain many sharp, decurved spines for protective armament. Cones are oriented
downward on the end of branches and seeds are readily released from ripe cones.
All four jays (Steller’s, pinyon, scrub and Mexican) and Clark=s nutcracker harvest, transport, cache, and
recover the seeds from this tree, even though this species relies mainly on
wind for the dispersal of its seeds. Wings are broken off the seeds before they
are transported. Nutcrackers clip them off with their bills while the jays use
a branch or other stationary object to smash the wing with a strong swipe of
the bill.
D. Colorado pinyon pine. (Figure 10.) This
species lives below the ponderosa pine forest. Trees are spaced more openly
than any of the above. This species is the only Amasting@ species of the conifers harvested by the birds. Usually a few
cones are produced on many trees every year but in extreme years no cones are
produced, or just the opposite, with most all trees produce thousands of cones
per tree. When trees produce such a large crop of seeds this is known as a “mast” crop. These extremes occur about once every seven years. (Figure
11.) It has been suggested that masting insures that the seed caching birds and
other seed predators are unable to harvest and consume all available seeds and thus
the predators are ‘swamped”. They cannot build up populations of sufficient
numbers to totally decimate the seed crop (Vander Wall and Balda 1977, Vander
Wall 1990). This species places its cones near the end of branches, where they
are positioned to point outward or upward. Cones open asynchronously on each
tree and in different regions. Seeds are relatively large (10-15 mm) and
wingless and held in deep grooves on the cone scale. The cone scales are
relatively short and contain flanges that act to hold the seeds in the cones so
they are not easily dislodged. The flange disintegrates after the first frost
in autum
n and then the seeds fall out of the cone. Seed
coat color differs drastically between seeds that are full of female
gametophyte material (dark, chocolate brown) and those that are empty (light
yellow) (Figure 12,) All five seed
caching corvids are attracted to the cones pf
pinyon pine to extract seeds.
The Clark=s nutcracker and pinyon jay are able to open tightly closed green
cones, whereas the three other jays must wait for the cones to open naturally.
The scrub-jay may not recognize that the yellow hulled seeds are empty (Vander
Wall & Balda 1981).
This species of tree enjoys the widest
elevational range of any pine on the San Francisco Peaks. Trees grow from 1,680
m (5,500 ft) to over 3,600 m (11,000 ft). These higher stands were most likely “planted” by nutcrackers, as
we have seen them transport seeds to these areas (Vander Wall and Balda 1977).
The Birds
When pine cones are present, the seed caching
corvids expend considerable time and energy harvesting, transporting, and
caching pine seeds each autumn. Each species shows different types of
morphological, ecological and behavioral specializations for this task. Here we
describe these specializations for each species.
A. Clark=s nutcracker. (Figure 13.) This species lives and nests at the
highest elevations on the San Francisco Peaks, of all the seed caching corvids.
They nests in spruce-fir, mixed conifer and ponderosa pine zones. Nutcrackers have
a number of morphological adaptations that are used for the harvest, transport,
caching, and eating of pine seeds. A conspicuous example is the long, heavy,
sharp bill. This bill is used for hacking open green, closed cones, many of
which are covered with pitch. Nutcrackers can open the green cones of most of
the pines mentioned above. The bill is also used to thrust seeds into the
substrate with strong japes of the head and neck. As their name implies,
nutcrackers can open thick-hulled pine seeds by crushing them in their bills
(Johnson et al. 1987).
During
transport, seeds are held in a unique sublingual pouch that is located in the
floor of the mouth in front of the tongue (Bock et al. 1973) (Figure14.). When
full of seeds the sublingual pouch is greatly distended but it is not
conspicuous when empty. This structure can be filled with up to 95 pinyon pine
seeds and weigh up to 13% of the total weight of the bird.
Nutcrackers have
long, pointed wings for strong flight. They often fill their sublingual pouches
with pinyon pine seed and the fly up to 22 km to a caching area (Wander Wall
and Balda 1977, 1981). The also can carry seeds 1,900 m up the side of the
Peaks.
Nutcrackers can distinguish between pinyon pine seeds
that contain female gametophyte material (Anut meat@) and those that are empty by observing the color of the hull or
shell. The other species of pines do not Alabel@ their seeds. Nutcrackers
also use @Bill clicking@, the rapid opening and closing of the mandibles,
to help determine if the seed is full (Ligon and Martin 1974) and also help
determine the thickness of the seed coat (Johnson et al.1987). In an autumn when
the pinyon pines have masted, thousands of discarded cones occur on the ground containing
a large numbers of seeds with yellow hulls.
The daily sequence of events during the autumn
caching season proceeds as follows. Birds open seeds and consume pine seeds at
first light. Then seed collecting begins and pouches are filled. Birds continue
to harvest seeds for the entire day traveling 5-7 times from harvest area to
caching area and back.
Seeds are cached in the substrate at depths of
2-3 cm. (Figure 15.) These caches are totally concealed from view as birds
often place soil, litter, pine needles, pine cones and even small stones on top
of the hidden seeds. These objects seldom remain in place for long due to wind,
water, and gravity. Most likely these objects are placed on top of the cache to
conceal the soil disturbance made by creating caches, not to conspicuously mark
the location of the cache.
Caches are created
in a wide variety of sites, including meadows, tundra, open woodlands, closed
canopy forest, rocky outcrops, thick needle layers, cinders, and bare soil.
Many of these sites experience low amounts of snowfall or early snow melt thus
allowing birds’ ready access to
their caches. Often nutcrackers cache seeds at sites used by numerous other nutcrackers
for caching. However, even though the site may be communal the caches are not,
as birds can only locate the caches they have created (Vander Wall and Balda
1977, Vander Wall 1982).
Nutcrackers often proceed to cache in two
stages. First, when seeds are plentiful birds will extract them and cache them
near the harvest tree. Second, after the cones have been depleted these caches
are recovered and the seeds transported some distance and then recached (Tomback 1998) The former may be a technique
to get as many seeds as possible out of the conspicuous cones and into hidden
sites, the locations of which are known only to the cacher. Later seeds may be moved to more protected
sites or sites with fewer seed predators present.
In a year
with a heavy cone crop a single nutcracker can cache between 22,000 and 33,000
seeds in over 7,000 individual cache sites (Vander Wall and Balda 1977). Birds
may place between one and 14 seeds per cache. Birds continue caching until the
crop is depleted or snow covers the caching areas (Vander Wall and Balda 1977).
Possibly, birds curtail caching after snow remains on the ground because to
cache in these conditions would reveal cache location by their foot prints left
in the snow.
Seed caches may be harvested immediately after the harvest
is finished. Often, birds eat the recovered seeds directly at the site of
recovery, thus providing a measure of recovery accuracy.
Most
workers report that nutcrackers recover seeds from about 80% of their probe
holes (Turek and Kelso 1968, Tomback 1980). This estimate must be low as some
seeds recovered from caches are carried off before consumption, and some sites
must be pilfered by cache robbers. This high estimate is a truly a tribute to
the spatial memory ability of the Clark=s nutcracker when one considers; 1) nutcrackers spend less than 30
sec. making a cache (Kamil et. al.1999): 2) they make thousands of caches each autumn:
3) they returned to accurately recover their caches many months after creating
them: 4) they recover through a substrate that has been greatly altered between
the time of caching and recovery. This means that caches created under one set
of substrate characteristics are recovered under a very different set of
substrate characteristics. For example, caches made in the fall before snow is
present are recovered through snow (Figure 16.). Caches made when green vegetation
is present are recovered after this vegetation has died and disintegrated. This
suggests that these Alocal@ cues or landmarks are not used by the birds as the sole source of
information about the location of their caches.
Nutcrackers are heavily dependent on their
cached seeds for survival in winter and as food for their offspring. Giuntoli
and Mewaldt (1978) found that between 80 and 100% of the winter diet of
nutcrackers was made up of conifer seeds, most likely recovered from caches.
Other foods are consumed, when present, as the nutcracker becomes a feeding
generalist during warmer weather.
Clark=s nutcrackers are among the earliest nesting species of North
American birds initiating nesting at high elevations in the San Francisco Peaks
in February or early March (Tomback 1998). Early breeding may occur because of
having stored enough food to provide the energy and nutrients for this early
reproductive effort. To withstand the cold temperatures, nutcrackers build
large, sturdy, well insulated nests. Both males and females have brood patches
and can thus share in the duties of incubating eggs and brooding nestlings. This
also allows each member of the pair to go off, individually, to locate its own
pine seed caches. The diet of nestling nutcrackers is almost exclusively
conifer seeds (Bendire 1889, Johnson 1900, Mewaldt 1956). This is a highly
unusual food for nestling birds and requires a major adaptive change in the
digestive physiological of the birds to produce specific digestive enzymes to
digest these seeds. After fledging, young birds follow their parents to caching
areas where they are also fed pine seeds. This event normally occurs 9-11
months after the seeds have been stored (Vander Wall and Hutchins 1983).
In late spring and early summer adult nutcrackers
are often seen far from their normal haunts. These birds fly slowly just above the
tips of trees. We suspect these birds are assessing the location and size of
the cone crop that will be harvested in the coming months (RPB, pers. obs.)
In years when cone crops fail nutcrackers leave
their high mountain haunts and fly long distances in search of
alternate foods. These irruptions take birds hundreds of km from their normal
range (Vander Wall et. al 1981, Westcott 1964)
Thus, nutcrackers are highly specialized in
morphology, physiology, and behavior for the extraction, transport, caching and
recovery of conifer seeds and these specializations form a suite of adaptations
that extend into all aspects of the bird=s life history.
B. Pinyon Jay. (Figure 17.)This species, as its
name implies, is closely linked to the pinyon pine which lives that the base of
the San Francisco Peaks. In the San
Francisco Peaks, however, these jays interact with most species of
pines across all Life Zones. They nest in the pinyon-juniper woodland and ponderosa pine zones, where seeds are readily cached. In fall, they also
roam far above these zones in search of seeds.
Pinyon
jays possess a number of adaptations for harvesting, transporting, caching and
recovering seeds. They have a relatively long, sharp bill that is featherless
at its base. Consequently, the bird=s nostrils are exposed and can be a source of heat loss under cold
conditions. However, the loss of these feathers means that the featherless
length of the bill is effectively lengthened, an adaptation especially useful
for extracting seeds from pitch laden pine cones. The trade-off must be in
favor of the longer, feather-free bill compared to the amount of heat
potentially lost. The sharp bill is used to hack open closed pine cones and
also the hulls of pine seeds, thrust seeds into the soil, and probe into the
soil to recover hidden seeds. A special articulation of the jaw allows birds to
absorb the bill=s impact during strong pounding (Zusi 1987).
Seeds are held during transport in an expandable
esophagus which when full, can hold about 40 seeds. This amounts
to about 12% of its body weight (Vander Wall & Balda
1981).
Pinyon jays can distinguish between empty and
full pinyon pine seeds using the color of the seed coat. Pinyon pine seeds are
also “Bill Weighed” and “Bill Clicked” as done by nutcrackers (see above) (Ligon and Martin 1974).
Cones can be opened on the tree branch or broken
off and carried and wedged tightly into a forked branch. When wedged in a fork,
the bird can grip the surrounding branches tightly with both feet and forcibly
hammer the cone open. Shredded cones commonly accumulate under such sites.
Cone opening, seed harvesting, Apouching@, transporting, and caching seeds is a flocking event. These behaviors
are performed by all members of the flock in synchrony. These flocks have permanently mated pairs, stable
membership, contain extended family units, and remain on permanently delineated
home ranges.
Pine seeds are transported to Atraditional@ caching areas that are used year-after-year. Flocks have between
8 -10 of these Atraditional@ caching areas on their home ranges. These “traditional” areas are often located where the substrate is loosely packed,
contains patches of exposed soil, rocks, and cinders, and has a shallow litter
layer. These characteristics indicate a well drained soil (Balda 1987,2002).
Flocks
move in synchronous fashion from harvest to caching area and can make between
5-9 round trips per day from harvesting to caching areas depending on density of
the cones, and distance from the caching areas. Flocks may fly up to 11 km, on
long strong wings, between harvest and caching areas
Pinyon jays seem to favor specific
microhabitats as cache sites. They appear to prefer to cache near objects,
including the base of cliffs, large boulders and especially tree trunks, often
on the south side. These southern exposures are first to melt free of snow or
accumulate less snow following a winter storm (Balda & Bateman 1971, 1972).
Jays however, have been observed digging through a layer of snow 5 cm deep to
recover caches.
Pinyon jays use sites other than the substrate
for caching. Stotz and Balda (1995) found that 86% of 114 above ground cache
sites were crevices in tree bark. Other sites include in rock piles, grass
tuffs, and pine nettle clusters high in trees.
.
Caches are created as the flock walks slowly and
silently over the substrate. Birds continuously thrust their bill into the soil
and litter as they deposit one or more seeds per site (Stotz and Balda 1995). A
single bird can make a dozen caches in less than a minute. Generally, flock members move in a particular
direction during caching but individual birds may move in any direction. Pinyon
jays normally place a single seed in a cache but on occasion they may place up
to seven seeds per cache. At times,
however, birds will thrust their bills into the substrate but not deposit a
seed. This if often referred to as Afalse caching@ (Balda 2002) and may be a technique used to confuse potential
intra- and inter-specific cache pilferers.
In a year when cone crops are dense, a single
bird can cache up to 26,000 seeds in up to 20,000 individual sites (Marzluff
& Balda 1992). Ligon (1978) estimated that a flock of 250 birds in New
Mexico could collectively cache 4.5 million seeds in a single autumn when cone
crops are heavy.
Although caches are made synchronously by the
flock, field observations (Balda and Bateman 1969, 1971) suggest that birds
accurately recover their own caches. This is especially interesting for pinyon
jays because they: 1) cache within the structure of the flock which means birds
move in unison over the terrain when creating caches, so individuals have
little control over the general area where they can cache; 2) have little time
for individual decisions about where to make specific caches because the flock
is always on the move; 3) make caches in rapid succession resembling the needle
of a sewing machine; 4) must be concerned with pilfering.
Young-of-the-year pinyon jays and adult Steller=s jays often watch intently as flock members are
caching and then attempt to locate their caches when they move on. Most
attempts appear to fail, but sometimes the bird that has created the cache will
respond by either chasing the potential pilferer away or digging up the cache
and moving it to a new location (RPB pers. obs.)
Mated pairs of Pinyon jays appear to coordinate
their movements during caching so that they can observe the creation of each
others caches (Shulzitski 1999, Chen 2000). These findings come solely from
laboratory studies. It is difficult to follow individual birds in a flock
because of the sheer numbers and continual movement, thus these observations
have not been confirmed for pairs in the wild.
Pinyon jays nest in late winter and early spring
when cone crops are large. Nests are large and well insulated, and often
constructed on the south side of the tree (Balda and Bateman 1972). The female is the sole
incubator of the eggs as only she possesses a brood patch. Males must feed
their females during the incubation and early brooding phase of nesting because
of low temperatures. Adult jays rely heavily on pine seeds in winter when they
may constitute between 70 and 90 percent of the diet (Ligon 1978). At this
time, seeds are no longer present in cones so these seeds must come from caches
created by the birds. Males must procure and deliver these seeds to the nesting
female. Young pinyon jays are also feed pine seeds as a portion of their diet.
Bateman and Balda (1972) found that pine seeds comprised 11% of the nestling’s diet while Ligon (1978) found pine seeds made
up 32% of the diet. As mentioned for
nutcrackers, the ability of nestlings to digest plant material is a rare
adaptation in song birds, requiring major changes in the digestive enzymes
possessed by the birds.
Juvenile birds first began caching when 3 weeks
post-fledging. For the first 9 weeks of caching young birds cached primarily
non-food items such as rotten pinyon and ponderosa pine seeds, flakes of tree
bark, rabbit scat, dead insects, and a roofing nail. After 12 weeks of age jay
began caching edible pine seeds (Stotz and Balda 1995).
In years when pinyon pine cone crops are low,
pinyon jays cache seeds of the other pines, many of which have large wings.
Birds are efficient at removing the wing by holding the seed in there mouth
with the wing protruding directly outward and then knocking the wing off on a
branch or other object. This behavior differs from that of the nutcracker which
appears to simply bite off the wing (RPB, pers. obs.) No detailed studies are available of the use
of these pines by pinyon jays. However, Balda and Bateman (1971) report that
pinyon jays are highly industrious in the harvest and caching of ponderosa pine
seeds.
When there is a general failure of the pines to
produce cones pinyon jays may irrupt from their normal range and emigrate
hundreds of km in search of food (Westcott 1964). These irruptions may consist
of huge numbers of birds or small bands of birds that scour the country side
for food (RPB pers. obs.).
C. Steller=s Jays. (Figure 18.) This species is a
permanent resident of the coniferous forest zones on the San Francisco Peaks.
It readily caches ponderosa and pinyon pine seeds in autumns when cone crops
are available. Steller’s jays also cache acorns of local oaks. This jay does not have a strong, sharply
pointed bill for opening green cones and thus must wait for cones to open
before it can extract seeds. It does have an expandable esophagus, for about
one-third of its length that can hold up to 20 seeds during transport. Birds
are can carry seeds about 5 km (Vander Wall and Balda 1981) from pinyon pine trees in the woodland and cache
them in the ponderosa pine forest. This jay appears to cache in small family
units or pairs. Steller=s jays appear highly motivated to harvest and cache seeds. A
single bird may make 5-7 trips with seeds per day between woodland and
ponderosa pine forest. Thus, at this intensity one bird can cache about 7,800
seeds per autumn. When pinyon pine seeds
are placed on a feeder Steller=s jays are quick to collect these seeds in their expandable
esophagus (RPB pers. obs.). Few studies have been done on their relationship to
pine seeds and acorns (Abbot 1929, Wander Wall and Balda 1981,
Christensen and Whitham 1991).
At a feeding station where inedible (hollow)
seeds were dyed dark brown to make them look edible, these jays carried them
off. Steller=s jays have never been seen to test the quality
of seeds by Abill-clicking= or Abill weighing@ so it is possible they cannot discriminate seeds as well as the
above two species (Vander wall and Balda 1981).
Steller=s jays may be efficient cache robbers on
nutcrackers and pinyon jays, (Burnell and Tomback 1985). When a flock of pinyon
jays comes through areas inhabited by Steller’s jays they sit silently in trees observing where pinyon jays are
creating caches.
Little is know about the caching and recovery
behavior of Steller=s jays even though they share habitats with humans and readily
come to feeders and picnic tables to collect and carry off seeds (Brown 1994).
In a year of heavy cone production Steller=s jays were observed to cache 46% of the time in soil, 22% of the
time in bark crevices, 18% of the time in rock and stump crevices, and in
ponderosa pine needle clusters 15%. Most often one seed is placed per cache.
(Vander wall and Balda 1981). Around dwellings birds will cache under litter in
gardens, in lawns, in tree crevices, in storm gutters, under roofing shingles,
in depressions and cracks in wood siding and decks, and in cracks in sidewalks
(RPB pers. obs.).
Steller=s jays probably use their cached food solely for winter survival
as there are no reports of them feeding cached seeds or acorns to nestlings.
Possible all cached food is consumed before nesting is initiated. No
observations have been reported on the accuracy of recovery of stored food in
the wild. Observations near homes would suggest the jay is quite accurate when
recovering cached food (RPB pers. obs.).
Steller=s jays nest in late April and early May. Thus, they show no tendency
for unusually early nesting
and do not build bulky, well insulated nests.
This bird has not been studied under closely
controlled laboratory conditions because it is extremely difficult to hold in
cages and aviaries (RPB pers. obs.). Consequently little is known
about its spatial memory abilities. However, the amount of food stored, the
presence of an expandable esophagus, and the amount of time birds spend caching
would suggest that the bird is readily able to find the seeds it caches.
This species does not nest in late winter, does
not build a large nest and does not feed its young pine seeds. Also, it does
not usually undergo huge irruptions when cone crops fail. Thus, many of the
Steller’s jay’s life history traits are not affected by the
presence or absence of pine seeds.
D. Mexican jays. (Figure 19) Western scrub jay.
(Figure 20). These two species, closely related congeners, are permanent
resident species in the pinyon-juniper woodland on and at the base of the San
Francisco Peaks. Both species harvest and cache pinyon pine seeds from open
cones. The western scrub-jay is the most common species in the woodland habitat
and may maintain permanent, year round territories occupied by a single pair of
birds. The Mexican jay is highly social with 5-25 birds occupying permanent
territories (Brown 1994). Neither
species posses any specialized structures for the collecting, transporting,
caching or recovery of pine seeds. Scrub jay bills, for example are relatively
short (x = 19.6 mm, n = 20), rather blunt, and therefore relatively poorly
adapted for opening green cones (Balda 1987).Scrub jays that cache pinyon pine
seeds have slightly more pointed, but rather thin bills, used for extracting
seeds from open pine cones, holding the seeds during transport and thrusting
seeds into the substrate (Peterson 1993).
Neither species is able to open green cones and
must wait for cones to ripen. Scrub jays have been observed silently watching
nutcrackers and pinyon jays opening green cones then flying rapidly at them
while vocalizing loudly. The startled birds drop the partly opened cones and
fly up into the trees. Scrub jays proceed to retrieve the cone and extract the
exposed seeds (Vander wall and Balda 1981).
These
jays have no specialized structure for carry seeds from tree to cache site
except in mouth and bill. Consequently they can only carry 3-5 seeds per trip.
These jays do not have strong long wings, but relatively short rounded ones.
They usually carry pinyon pine seeds no more than 500 m to 1 km. Scrub jays do
possess the buttress complex which makes the lower mandible effective for
pounding open hard shelled seeds. (Zusi 1987).
Both species may be able to distinguish good (dark brown hulled) seeds from empty (yellow hulled)
seeds but they are not known to Abill click@ or Abill weigh@ seeds.
Both species usually cache one seed per cache
and make repeated caches within one m of each other. Cache sites are primarily
along edges of trees and stumps and under dense foliage. Of 62 observed caches
made by scrub jays, 29 were under pinyon pine trees, 8 were under junipers, 8
were near a bush, 3 were near logs, and 14 were out in open meadows (Hall and
Balda, unpublished MS). The majority of caches placed under trees were south of
the trunk. These observations indicate that scrub jays have a set of preferred
caching sites that are frequently used.
Scrub jays and Mexican jays nest in late April
and early May, showing no tendency to nest earlier when cone crops are heavy.
Neither species builds a large well insulated nest, nor is known to feed pine
seeds to its nestlings.
These two species are the most general feeders
in the group and although they store pine seeds in autumn they are not as
motivated as the nutcracker, pinyon and Steller’s jay. Scrub jays store about 6,000 seeds in an autumn when the
cone crop is large. They do not spend every waking moment harvesting,
transporting and caching pine seeds. If the did so they could easily double the
number of seeds cached (Balda 1987). This is so because they transport seeds relatively
short distances compared to the other species, and have many more snow-free
days to cache.
These two jays do not undergo major eruptive
movements when cone crops fail. This may be an indication that these species
are not as heavily dependent on cached food as the nutcracker and pinyon jay.
Summary of Natural
History and Ecology of Caching Behavior
The corvids of the
San Francisco Peak region show an ecological, morphological and behavioral
gradient in their adaptations for the harvest, transport, and storage of pine
seeds. Ecologically, species living in
the harshest environments where winter productivity is nil are most dependent on
cached seeds during winter, whereas species living where winter is milder are
less dependent on cached seeds. Morphological features that show this pattern
include bill size and shape (Figure 21), the structures used to carry seeds,
and variation in wing length and shape
for long, flights. Behaviorally, the number of seeds that can be transported is
highly correlated with the distance they are carried (Figure 22), and the
presence of a specialized structure for doing so. The Clark=s nutcracker and pinyon jay, the two species
living at the highest elevations, cache huge numbers of seeds compared to the
two jays that inhabit the lower, warmer woodlands. Of the five species discussed above only
nestling nutcrackers and pinyon jays are equipped to digest pinyon pine seeds. The scrub jay and Mexican jay do not show the
same levels of intensity to harvest seeds as is shown by the nutcracker and
pinyon jay.
There can
be no doubt that these birds have an adaptive suite of characteristics for the
harvest, transport, and caching of seeds. The components of this adaptive suite
vary depending on the selective forces present in the Life Zones each species
inhabits, and the life history strategy employed by each species. The four
species show a clear specialization gradient from more highly specialized
species, to more generalist species.
Hypothesis and Questions
The phenomenon we described above makes it clear
that there is a complex interaction of natural history and ecology on the one
hand, and behavior and physiology on the other.
While these phenomena strongly suggest that the ability to find stored
food is critical for the survival of these species, they do little to explain
how the different species manage to perform the extraordinary task of
relocating hidden seeds from thousands of sites months after they were created.
However, the pattern in behavioral and
physiological traits strongly suggests a similar pattern may exist in certain
cognitive traits. This led us (Balda and
Kamil 1989, Kamil and Balda 1990) to propose the following hypothesis: Species that are most dependent on cached
seeds for survival in winter and early spring when no other foods are available
will have better spatial memory abilities than those species that are less dependent on stored food
for winter survival.
More specifically,
we predicted that Clark=s nutcrackers and Pinyon Jays have spatial memory abilities that
are superior to those of scrub jays and Mexican jays (Figure 23). Findings to support this
hypothesis will strongly support the suggestion that spatial memory ability is
another trait in the adaptive arsenal employed by species to enhance their fitness.
General
Considerations
Although field observations suggest an accurate
spatial memory in seed cachers, these observations are incomplete because
simply observing the act of recovering a cache is inconclusive. The observer does not know the identity of
the recovering bird, what bird made the cache, how long the cache was present,
if the seeds were visually apparent to the bird, if the soil was disturbed in
such a manner to suggest that a cache of seeds was present at this location,
etc. Also, most birds are highly secretive when creating
caches and avoid making caches when being observed. Pinyon jays are an
exception, but they cache at such a rapid rate it is almost impossible to keep
track of their cache sites. They also create false caches which makes finding
their caches very difficult. Consequently, in order to study the accuracy of
spatial memory for finding cached seeds, it was necessary to develop laboratory
techniques that could control or hold constant many potentially intervening
variables. Below we will describe our methods in detail.
When using controlled laboratory experiments to
explore species differences in mental capabilities there are many potential
problems. Species may respond differently to the experimental apparatus, or to
the stimuli used to elicit a response. Also, some species may simply be able to
adjust to captivity or to the experimental manipulations better than others. In
addition, some species may simply be better Atest takers@ than others. In our attempt to overcome these potential problems
we employed three different experimental paradigms, in a process referred to as
converging operations (Kamil 1988). If the pattern of results across species
remains consistent over these three different tests, we can then be more
confident of the reality of these species differences than we could on the
basis of a single task.
Cache Recovery
Tests of Spatial Memory
A. Introduction and
General Methodology: In order to directly test for accuracy of spatial memory
when recovering caches we conducted a series of experiments in large
free-flying, experimental rooms. These rooms contained raised floors with holes
at regularly spaced distances (Figure 24, 25).
Each hole was 5.5 cm in diameter and could be
filled with a sand-filled cup for caching or a wooden plug to prevent caching.
These rooms contained many landmarks, posters on the wall, observations
windows, a porthole through which the bird entered and
exit the room, a door, and a centrally located feeder. Because the experimental rooms were designed
to enhance the internal validity (Kamil 1988) of our experiments there was a
question if the birds would cache in the sand-filled cups (Figure 26).
Birds
were captured from the wild and tested in numerous experiments. Birds were of
unknown age and sex. Nutcrackers, pinyon jays and Mexican Jays were housed
individually in 0.51 x 0.51 x 0.72 m metal cages. All birds were held on a
10:14 hr light:dark cycle. They were fed a daily diet
of pigeon pellets, meal worms (Tenebrio larva), sunflower seeds, turkey
starter, cracked corn, and a vitamin supplement. They had constant access to
ground oyster shell and fresh water. Between experiments birds were also fed a
ration of pinyon pine seeds. During experiments, however, these seeds were
withheld and used as the experimental stimuli. Before each caching and recovery
session, birds were deprived of all food for 24 hr. Scrub jays, because of
their smaller size were housed in smaller cages but all other conditions were
the same as described.
During experiments birds were allowed to enter
the experimental room directly from their cages through a porthole in the wall.
Before entering the room the cages were darkened and the experimental room was
illuminated. Birds thus flew into the lighted room. After a session was
completed the lights in the room were extinguished and the cage illuminated.
The birds then left the experimental room and flew directly through the
porthole into their cages. Thus, birds
were not handled before, during or after an experiment. For caching sessions a
predetermined number of holes were opened and were filled with sand in a
predetermined pattern. A feeder was placed in the center of the room and
contained a predetermined number of pinyon pine seeds. For recovery sessions
all signs of digging in the sand-filled holes was swept up from the floor, one
seed was placed into cups where caches had been made, and the feeder was empty.
There were no signs of digging or presence of seeds in the cups that the birds
could have used as cues to locate caches.
1. Cache recovery by Clark=s nutcrackers, pinyon jays and scrub jays. (Balda and Kamil 1989)
This test of spatial memory was conducted in a
3.4 x 3.4 m experimental room with 180 holes in the raised floor. The accuracy
of recovery was tested under two conditions. In one condition 90 holes were
available for caching and in the other condition only 15 holes were opened for
caching. The rationale for this two stage design was to assess the accuracy of
the three species after they the birds were given free choice of cache
placement so that a placement strategy could have been employed (90 hole
condition). This accuracy can then be compared to that achieved after severely
limiting the number of available cache sites (15 hole condition). Under this
condition a cache site placement strategy would be severely inhibited. Seven
days after making caches birds were allowed back into the experimental room to
recover their caches. Accuracy was assessed as the proportion of holes probed
that contained a seed.
In most of the
recovery trials birds preformed better than chance (40 out of 42) and all three
species performed better in the 90 hole condition than they did in the 15 hole
condition. Nutcrackers and pinyon jays were significantly more accurate than
scrub jays in both conditions (Figure 27.). There was no significant difference
between nutcrackers and pinyon jays in recovery accuracy. Pinyon jays appeared
to be most affected by the 15 vs. 90 hole condition. During the 90 hole
condition they placed their caches in conspicuous clumps. The average distance
between caches was 0.81 m for pinyon jays, 1.22 m for nutcrackers and 1.5 m for
scrub jays.
These results support our hypothesis that
recovery accuracy is a function of the ecology and natural history of the
species being investigated. Nutcrackers and pinyon jays which have
morphological, and physiological adaptations for this behavior and are also
most dependent on their cached seeds for winter survival and reproduction,
performed significantly better than scrub jays.
However, pinyon jays could have used a
nonmnemonic technique such as area restricted search to find their caches. If
caches are placed in all available cups in a cluster then birds need to only
search in this small restricted area. The clumping of caches may be a result of
the social nature of pinyon jays as they cache as a social unit (Figure 28, 29,
30). Because of this, they may be prone to place caches close together as their
movements may be restricted by the presence of other group members. In nature
pinyon jays appear to place caches close to one another (RPB pers. obs.).
In a follow up
experiment (Romonchuk 1995) allowed nutcrackers and pinyon jays to create 25
caches in 330 sand filled cups in the floor of a large experimental room (9.1 x
15.3 x 2.8m) The mean intercache distance was measured by averaging the
intercache distances between all possible unique pairs of caches. Mean
intercache distance was significantly closer for pinyon jays (mean = 2.66 m)
than for nutcracker (x = 3.86). These results corroborate the findings of the
first experiment.
2. Spacing patterns of Pinyon jays. (Romonchuk, 1995).
This experiment set out to test if pinyon jay
cache recovery accuracy was dependent on placing caches close together so an
area restricted search pattern can be used rather than employing spatial
memory. This was a follow up to A1.
The experiment was
conducted in the large room in which the floor contained 330 holes. This
experiment used two unique sets of holes chosen from the 330 holes available.
In one condition, 72 evenly spaced holes were opened and in the other 36 evenly
spaced holes were opened. Birds were allowed to make 15 caches. In the former
condition the jays could clump caches but the in the latter condition clumping
should have been prevented. If birds use
area restricted search to locate caches than accuracy should be higher during
recovery in the 72-hole condition than in the 36 hole condition. Mean
intercache distances were not significantly different between the two
conditions but was smaller for the 72-hole condition (mean = 3.62) than for the
36-hole condition (mean = 4.01). However, both of these distances are much greater
than the distances found by Balda and Kamil (1989) and described above for all
three species.
Accuracy was measured using a single cache
recovery attempt procedure (SCRAP) developed by Kamil and Balda (1990). During
recovery sessions caches were presented to the bird as a series of clusters.
Each cluster consisted of four holes arranged in a square. The cache was one of
the holes in this square. The other three holes had not been cached in. The
number of probes that were used to find a cache within a cluster could vary from
zero (found cache on first probe) to three (found cache on fourth probe after
probing the three none-caching holes. If a bird was probing at random the mean
number of errors would be 1.5. For each cluster containing a cache site another
cluster was opened but did not contain a cache site. Thus, during recovery
birds had a choice of which cluster to visit (those with a cache site imbedded
and those without cache sites) and which hole to probe within a cluster (hole
with seeds or hole without seed).
Pinyon jays performed impressively under both
conditions making about 0.75 errors per cluster. There was no significant
difference in accuracy between the two conditions. Birds also visited Agood@ clusters significantly sooner than they visited Abad@ clusters. This experiment provides strong evidence that it is not
necessary for pinyon jays to place their caches in clumps and then use area
restricted search to find them. Pinyon jays have precise spatial memories for
the location of their caches.
3. Comparing long-term spatial memory in four species of
seed-caching corvids (Bednekoff et al., 1997) Above we have shown that
nutcrackers and pinyon jays have better spatial memory than scrub jays. These
finding however, are for relatively short durations. In fact, much shorter than
those expected in nature (based on the natural history observations presented
earlier). In this experiment we asked if the duration of memory for cache sites
varied among the four species. Earlier research (Balda & Kamil 1992) indicated
that Clark=s nutcrackers accurately remembered the location
of caches sites for up to 285 days. Here we tested nutcrackers, pinyon jays,
Mexican jays and scrub jays for recovery accuracy at 10, 60, 150,and 250 days
after caching. The
SCRAP procedure (describe above) with cache
sites imbedded in a cluster of 6 open holes in a 2 x 3 rectangle was used.
Chance performance would thus be 2.5 errors per recovery. Nutcrackers and
pinyon jays were highly accurate at the 10 and 60 day interval but only
modestly accurate at intervals of 150 and 250 days. The scrub jays and Mexican
jays performed at above chance levels at all intervals but were generally less
accurate than the former species. (Figure 31.). A species by interval ANOVA of the mean
number of errors, showed that nutcrackers and pinyon
jays did not differ significantly from each other, and the scrub and Mexican
jay did not differ significantly from each other, but the two groups differed
significantly. Thus, these results support the hypothesis that species most
dependent on their caches to survive the winter and for reproduction have more
accurate spatial memory than species less dependent on their caches.
Other tests of spatial memory in seed caching
corvids.
Although the comparative tests of spatial memory
reveal that the species more dependent on their caches for survival and
reproduction than less dependent species, these differences might be due to the
effects of contextual variable that could result in this consistent pattern of species
differences. As mentioned above, one or more species might be better suited for
this type of research paradigm than other species. Also, is this spatial memory
gradient limited to cache recovery or can this ability be generalized to other
tests of spatial memory? To address these potential problems, we conducted a
series of spatial memory experiments using procedures other than direct tests
of cache recovery (Kamil 1988).
A. Spatial memory of seed caching corvids in an
analogue of the radial maze. (Kamil et al. 1994). This experiment was carried
out in a small room (3.6 x 3.2m) where birds could fly free as they searched
for seeds. The raised floor contained 12 holes arranged in a circle (Figure 32).
Numerous
objects were present on the floor and posters were hung on the walls. Birds
entered and exited the room through a porthole in the wall. Members of each
species were habituated to the room and learned to dig for seeds in holes that
were filled with sand. After habituation birds were given 60 acquisition
trials. Each trial consisted of three parts, a preretention stage, a retention
interval, and a post retention stage. During the preretention stage the room
contained four randomly selected open holes. Each hole contained a carefully
buried seed. The bird entered the room and proceeded to harvest and eat the
seeds. This stage continued until the bird found and ate the four food rewards.
The bird then departed the room and the retention interval started. During the
retention interval the room was swept clean of all signs of digging, and four
additional holes were opened and a seed buried in each. After the five minute
retention interval the bird was allows back into the room. The room now
contained eight open holes, the four original holes that the bird had
previously emptied and the four newly opened holes. Only the newly opened holes
contained seeds. During the postretention stage the bird remained in the room
until it located the four food rewards or it made six probes. For each bird to
perform accurately it had to remember the four holes it had visited during the
preretention stage, avoid them, and visit the newly opened holes. A different
set of randomly selected holes were used daily. Trials were run six days per
week. During the 60 acquisition trials, all four species initially had similar
levels of performance, but they rapidly diverged (Figure 33.). Nutcrackers and pinyon jays learned the task faster and performed
more accurately than the western and Mexican jay.
These results
compliment our earlier findings about dependence and spatial memory. They also show that spatial memory is general
and not simply a specialization for finding hidden food caches made by an
individual. What other tasks these
species with highly accurate and robust spatial memory can perform is unknown
at the present time. However, the possibilities are numerous and potentially
exciting.
B. Operant spatial memory and nonspatial memory
test in four species of seed caching corvids (Olson 1991, Olson et al. 1995). Test of spatial memory in an operant chamber
strips away most all environmental influences from the organisms taking the
test, and allows exacting control of the subject and the stimuli. Thus, this
task allows us to enhance and maximize the intrinsic validity of the experiment
(Kamil 1988). For example, birds are rewarded when they peck at the correct
spot when illuminated. This is a huge difference from pecking at a spot in the
ground where a cache has been previously created.
Olson (1991) found that nutcrackers out
performed western scrub jays in this type of task. The present experiment was
designed to extend those findings and also to determine if the species
differences we had observed in other tasks were also present in nonspatial
tasks.
In the
nonspatial task, birds were asked if they could remember a color in order to
receive a food reward. The experiment was conducted in an operant chamber with
a computer monitor at one end and a pecking key and feeder at the other. Trials
were initiated when an illuminated spot appeared in the middle of the monitor.
The spot was either red or green, chosen randomly for each trial. When the bird
pecked this spot, the screen became clear. Now, a yellow light was illuminated behind
the key. The bird now was required to go
to the rear of the chamber and pecked the yellow light causing it to
extinguish. At this time two lights were illuminated on the monitor, one red
and one green. Now, when two pecks were delivered to either color, the trial
was ended. A trial was considered correct, and a food reward given, if the bird
choice the new color. The bird was required to remember what color it had seen
and pecked during the initial part of the trial and then avoid that color and
peck the alternate color during the final stage of the trial. This type of test
is known as a non-matching to sample test.
After the birds learned to perform this test we
wanted to determine how long the birds could remember the color presented
during the first portion of the trial. To do this we introduced a titration
procedure. A retention interval was added between the first peck at the
illuminated color on the monitor and the final choice test. This retention
interval increased when the bird made a correct choice and decreased when the
bird made an incorrect response. A correct response caused the retention
interval to increase by 0.1 seconds and an incorrect response caused the
retention interval to decline by 0.2 seconds.
The results of this experiment were unambiguous
and did NOT correlate with our earlier findings. Species most dependent on
cached food did not perform more accurately than species less dependent on
hidden food. None of the species differences was statistically significant
(Figure 34). However, the speed of
acquisition and retention interval did appear to be correlated with social
organization. The best performance was by pinyon jays and Mexican jays. Both
species live in permanent social groups. The worst performance was by
nutcrackers and scrub jays that have a more solitary life style. Sociality may
require certain types of cognitive abilities not found in non-social species
(Balda et al. 1996).
Immediately after
the above experiment was finished we placed these same birds into another,
almost identical test. This time, however, they were tested for spatial memory
rather than for color memory. All details of the experiment remained the same,
however, when the monitor was first illuminated one of two locations, chosen at
random, lit up. Then during the choice phase of the test two identical spots
were illuminated. One of the spots was at the exact location on the monitor
where the initial spot had appeared. The second spot occurred at a new
location. Again employing the
non-matching to sample paradigm, the novel location was the correct one. This
time very different results emerged. Clark=s nutcrackers were far superior to the three species of jays, thus
duplicating the findings of Olson for nutcrackers and scrub jays. These
findings are consistent with the results from radial maze and cache recovery tests.
It is, however, the first test to demonstrate a difference between nutcrackers
and pinyon jays as the latter specie=s performance could not be separated from that of the scrub and
Mexican jay.
The results of these tests are particularly
important as they allow us to rule out some alternative explanations for the
species differences we found in spatial memory tests. We can eliminate
explanations such as general intelligence or general adaptability or
compatibility to laboratory experimental procedures. If any of the above
factors were involved, then we should have found the same rank order of species
differences in the non-matching to sample color test as we found in spatial
tests. We did not.
C. Comparative
Observational Spatial Memory by pinyon jays, Mexican jays and Clark=s Nutcrackers (Bednekoff et al. 1996a, b). In the wild, pinyon jays and Mexican jays live
in integrated flocks and may cache together as a unit each fall when pine cones
ripen. In contrast, Clark’s nutcrackers cache either as single individuals, pairs, or small
family groups. We asked if the three seed caching species had the ability to
locate caches made by conspecifics. We hypothesized that species differences
may occur that reflect their social life style. If so then pinyon jays and
Mexican jays should be able to locate caches made by flock members but
nutcrackers should not.
To test this hypothesis we used a small caching
room (3.7 x 3.4 m) with 237 holes in a raised floor. Twenty holes contained a
sand-filled cups were available for caching. A bowl with 70 pinyon pine seeds
was placed on the floor. One caged bird was placed on a 1 m high platform in
the center of the room. A second bird was allowed into the room to cache in the
20 holes. After caches were created both birds were removed from the room for
24 hrs. During this time all signs of digging were swept up and one seed was
placed into each cache site. Cachers and observers were now allowed to
individually recover caches in the room.
Pinyon jay and
Mexican jay observers were just as accurate as their respective cachers (Figures 36,
37). Nutcracker observers, however, were not
accurate at locating caches made by the cachers, even though the cachers
themselves were the most accurate of the three species when locating caches
they had made (Figure 38). These results support our hypothesis that social
species may have the ability to locate caches made by conspecifics and
therefore must take special precautions when creating caches to avoid being
detected.
These findings also raised some interesting
mechanistic issues. This experiment demonstrates that neither traveling to a
specific cache site nor creating a particular cache are necessary for locating
that cache. These findings also show that pinyon jays and Mexican jays are not
simply matching the view from the cache site during caching because they never
cached at these sites. Also, birds did not follow a particular route to the
cache site. If so, they would have landed on the platform where their cage was
originally located and then preceded to the cache site. These results suggest
that the evolution of caching behavior may have been different for social and
nonsocial species and suggests a number of studies with other caching species,
i.e. the relatively nonsocial western scrub jays and the closely related but
social Florida scrub jay.
How Do Seed Caching Corvids Recognize the
Locations of Their Caches
Clearly, the ability of Clark=s nutcrackers (and other seed-caching birds) to
relocate their cache sites is remarkable,
and based on spatial memory. But this
raises a very interesting question: When a nutcracker is searching for stored
pine seeds, exactly how does it recognize that a particular location is a cache
site? That is, exactly what is it about
that location that the nutcracker has encoded and remembered? This question is particularly compelling
given the precision with which they return to a specific location that has no
marker or beacon, sometimes even digging through snow to find seeds (Crocq,
1978). Nutcracker caches are often
located in the middle of open meadows with few local features (Tomback, 1977,
1980; Vander Wall & Balda,
1981). There are landmarks (henceforth
abbreviated "LMs"), but many of them are distant from the cache
sites, and there is usually no surface feature identifying the cache site
within the surrounding terrain. Yet the
nutcracker lands on the spot and digs up seeds that it buried months ago. Its bill is a relatively small shovel,
requiring it to dig within a few centimeters of the buried seeds, which are
themselves quite small. Indeed,
Bednekoff and Balda (1997) demonstrated that nutcrackers are extremely accurate
when they use response topography of vertical head movements, with little side‑to‑side
motion, for digging.
Although these characteristics of cache recovery
imply that nutcrackers navigate with exceptional accuracy, little is known
about how the task is accomplished, except that it is based on the location of
LMs. Balda (1980), Vander Wall (1982)
and Balda & Turek (1984) showed that if LMs are either removed or shifted
between caching and recovery, accuracy of seed recovery deteriorates markedly,
to chance levels in some cases. This
suggests that the geometry of the relationships among LMs and cache positions
might affect search behavior.
Kamil, Balda & Good (1999) analyzed
videotapes of caching and recovery to try to understand how movements during
caching were related to those during cache recovery. Among caching behaviors quantified were time spent
and number of probes at individual sites and the compass direction used to
approach and leave the site. There was
no evidence that any of these measures correlated with recovery accuracy. Especially important in its implications for
LM use, birds recovered caches very quickly and accurately when approaching or
probing the cache site from a completely different direction than that used
during caching. Consistency of direction
of approach was completely unrelated to recovery accuracy. Because the birds' view of the LMs in the
room varies with the direction of movement, this suggests that, as implied by
Basil (1993), multiple relationships between goal locations and LM arrays were
being used.
We then began a series of studies using what has
been called the transformational design (Cheng & Spetch, 1998), a powerful technique for investigating LM
use. Animals are first trained to find a
hidden goal (such as a buried piece of food) located at a fixed place relative
to an array of LMs. During training, the
LM array is presented in different locations (but with constant relationships
among the LMs within the array) to ensure that the LM array is the only feature
that accurately predicts goal location.
Once the animal has learned to find the goal, occasional trials are
conducted with the goal absent and the LM array transformed in some way. Response to the transformation is used to
infer how the LM array is being used.
Gould‑Beierle & Kamil (1996) examined
how nutcrackers integrated information when a landmark was located near an
edge. Like the pigeons and black‑capped chickadees studied by Cheng &
Sherry (1992), nutcrackers responded more to shifts in LM position that were
parallel to the edge than to shifts perpendicular to the edge. In two subsequent studies (Gould‑Beierle
& Kamil, 1998, 1999) , we found that global cues had more control over
search when local cues were further from the goal. This
extends previous work suggesting that cues close to a goal location can
exercise more control over search than LMs further away (e.g., Morris, 1981;
Cheng et al, 1987; Spetch, 1995).
The transformational approach has been applied
to the question of how many LMs are remembered.
A location of an object in space can usually be defined in multiple
ways. For example, consider a cache site
located in a meadow within 6 m of three big rocks. The cache location could be defined in terms
of its distance and direction from any one of the rocks, or in terms of its
directional relationship to any two of the rocks, or its distance from one rock
and direction from another, etc. Thus,
it is logically possible to use only a single LM to define and remember a goal
location. And the phenomenon known as
overshadowing suggests that this may be the case, at least under certain
circumstances.
In a typical overshadowing experiment, animals
are trained to find a goal whose position is defined by a set of LMs whose
distance from the goal varies, and are the tested during occasional probe
trials with only a single LM present.
The accuracy of search during the probe trials. Several studies with pigeons have found that
search is most accurate when the LM present during the probe trial is that LM
that was located closest to the goal during training (Cheng, 1988,
Spetch,1995). However, these experiments
employed landmarks that were very close to the goal location and the results
may not generalize to the use of more distant landmarks. Furthermore, the results of several studies
with nutcrackers indicate that these birds remember the spatial relationships
amongst multiple LMs and a goal location.
For example,
Vander Wall (1982) had nutcrackers cache seeds in a large outdoor
aviary. Then, during recovery sessions,
LMs in one part of the aviary were shifted 20 cm east, with seeds remaining in
their original locations. In the area in
which LMs were shifted, the birds' search was also shifted east by 20 cm. But on the edge of that area, where some LMs
had been shifted and others had not, search was intermediate between the
shifted and nonshifted locations. The
birds must have been averaging information from different LMs.
In another instance, Basil (1993) used
nutcrackers with a technique similar to Bennett (1993) with European jays. Birds were trained to find a goal location
defined by a LM array that was presented in many different locations and
orientations within the test room. LMs
in the array varied in size and distance from the goal. Probe trials with some LMs removed showed
that large, close LMs were more important than smaller ones further away from
the goal, as in Bennett (1993). However,
Basil conducted a more extensive set of probe tests than Bennett (1993),
obtaining clear evidence that the nutcrackers learned multiple rules for
locating the goal. Basil had 9 LMs in
her array, and tested for ability to find the goal with various sets of 3 LMs
each. Although the birds performed
better with some arrays than others, they could find the goal regardless of
which set of three LMs was present.
Clearly, they had learned more than one small set of the available goal‑LM
relationships. (This result was
different from that of Bennett, who found that only the two tall LMs nearest
the goal controlled search. This may be
a species difference but is more likely due to Bennett's placing these LMs only
30 cm from the goal, producing an >overshadowing' effect (Spetch, 1995). Basil used distances of 40‑60 cm.)
A recent study by Goodyear and Kamil (2004)
examined overshadowing and the effects of goal-LM distance in nutcrackers. Three groups of Clark=s nutcrackers were
trained to find a goal location defined by a landmark array. Each group was trained with an array of four
LMs, with the goal located in the midst of the array. The different groups were trained with arrays
that varied in the goal-LM distances (Figure 39.).
These goal-LM distances were chosen so that
the effects of both relative and absolute goal-landmark distance could be
assessed. All three groups readily
learned the task and were subsequently tested in probe tests with only single
landmarks from the array available.
Search error in tests with landmarks the same distance away from the
goal was compared across groups where only the relative position of the
landmarks varied. When the LM array was
located relatively close to the goal, overshadowing occurred, and only that LM
closest to the goal resulted in accurate search. As the goal-LM distance of the array
increased, however, this effect diminished.
Thus the results of this study indicate that multiple LMs are more likely
to be simultaneously encoded when goal-LM distances are relatively great.
The next step in
the development of our thinking about the use of LMs during cache recovery was
provided by a study by Kamil and Jones (1997) that suggest that directional
evidence is emphasized when the goal-LM distance is relatively great. Nutcrackers were trained to dig for a seed
hidden halfway between two LMs. Five
interLM training distances were used. The birds readily learned the task,
generalizing to new distances interpolated between training distances. Detailed analysis of the distribution of
search behavior showed the birds were very accurate with both the interLM
distances with which they were trained and the new interLM distances (Figure
40.).
The nutcrackers appeared to have learned a general principle,
although the exact nature of that principle remained to be specified. These results have been extended in several
additional studies (Kamil & Jones, 2000 showed that the birds could learn
and generalize geometric rules other than halfway, while Jones and Kamil (2001)
found that the birds could learn the geometry of arrays that were rotated
during training. However, the most
important result regarding the general use of LMs was an unanticipated feature
of the data from the halfway learning experiment. Error in judging distance from a LM increased
more rapidly than error in judging direction as goal-LM distance increased.
Because the birds had been trained to find a
goal that was located on the line connecting the two LMs, it was possible to
measure distance error and direction error separately. Simply put, error in the axis of the line
from goal to LM reflects error in the estimation of the distance to the LM
while error in the axis perpendicular to that line reflects error in the judgment
of direction from goal to LM.
Furthermore, as the axes are perpendicular, the estimates are
independent. We have repeatedly found
that the funct ions relating search error to goal‑LM distance areions relating search error to goal‑LM distance are
very different for distance and direction estimation (Kamil & Jones, 1997,
2000). The problem of locating a point
on a line has two components: locating the LM‑LM line and finding the
correct position along it. These are
problems in direction and distance estimation, respectively. When the search error of birds trained to
find a point on the LM‑LM line was partitioned into the two appropriate
axes, we have always found that error in each axis increases as goal‑LM
distance increases, but with much steeper slope in the distance than the
direction axis (Fig 41.). This suggests that when the LMs that control search
are far from the goal, information about the direction from goal to LM will
produce more accurate search than information about the distance from the goal
to the LM.
This conclusion raises the question of how
search accuracy can be achieved in the face of error in the compass used for
the estimation of direction. The task of
locating a buried seed calls for a high degree of accuracy. A compass with an
error of measurement of 1% will induce an error of "6.3 cm in search location when the goal is 1 m
from the LM (and an additional "6.3 cm for each additional meter of goal‑LM
distance). Kamil and Cheng (2001) suggested
that the use of multiple LMs provides a powerful way to reduce the effects of
error in directional estimation and achieve precise search. If the direction from the goal to each of a
number of different LMs is the primary information in the representation of the
goal location, these multiple bearings can be used to overcome inaccuracies
caused by compass errors.
Suppose a goal location has been encoded in
terms of n bearings, one to each of n different LMs. What happens to search accuracy as n increases,
given error in the compass used to determine bearings? The information provided by increases in n
can decrease search error. Consider n =
2. In most cases (it depends on the
angular separation of LMs) there will be two intersecting bearings. However, if there is compass error, the point
of intersection will not be at the goal and there will be no information
available about size or direction of the error.
Now consider n = 3. In many cases, the three bearings will describe a
triangle, whose size will contain information about magnitude of the compass error.
Kamil & Cheng (2001) investigated this issue
with a Monte Carlo simulation in which the compass measurement of bearing to
each LM was given a random error of "2%.
Search accuracy decreased significantly as n, the number of LMs encoded,
increased. In fact, search error was reduced by 35% by increasing
the number of LMs being used from two to four.
There can be little doubt that increasing the number of LMs represented
in directionally based encoding can dramatically increase search accuracy.
Based on these empirical results and their
simulation, Kamil & Cheng (2001) proposed the Amultiple-bearings hypothesis=, that goal locations that are relatively far
from LMs will be remembered in terms of the directional bearings from the goal
to each of several LMs. This hypothesis
makes many specific predictions. Search
accuracy should increase as the number of available LMs increases, which was
confirmed by Kamil, Cheng and Goodyear (2001), and should be sensitive to the
detailed geometrical relationships among the available LMs and the goal. As of this writing, several studies are
underway testing predictions of the model in Clark=s nutcrackers.
Evidence from several experiments suggests that
when caching in the field, nutcrackers, pinyon jays and scrub jays do use a
compass based on the sun as one of their sources of directional information. It
is well known that migratory birds use a number of different compasses,
including the sun compass, to find their way during migration (Wiltschko and
Wiltschko 1998) and this ability may also be present in non-migratory seed
caching birds.
Wiltschko
and Balda (1989,), Balda and Wiltschko (1991) and Wiltschko, Balda, Jahnel, and
Wiltschko (1999) studied the role of the sun compass in Clark=s nutcrackers, pinyon jays and scrub jays in a
series of cache recovery experiments. An
octagonal outdoor aviary with a diameter of 4.90 m served as the experimental
chamber. The floor of the aviary was divided into eight pie-shaped segments,
each containing six holes that could be filled with a sand filled cup for
caching or a wooden plug that prevented caching. This aviary was placed within
a courtyard surrounded by four high buildings of different heights and shapes, each
having a unique set of window and door patterns.
Birds were habituated to this aviary and then
allowed to create between one and four caches in 12 holes contained in two adjacent segments of
the floor. These two segments are referred to as the Acaching sectors@ and were varied among birds and tests. After
caching, birds were removed from the aviary and placed in their home cage in a
light-tight holding room. For all
recovery sessions all 48 holes were opened and one seed was placed into each
cup the birds had cached in. The experiments were performed in the following
manner:
1. Control 1: Each bird was allowed to recover
the seeds it had cached 4-7 days earlier. The location of all probes in this
control served as a reference for comparison with the manipulated sessions.
2.
2. Six hr slow clock shift. After caching each
bird was returned to its home cage and its internal clock was reset 6 hrs. slow. Now the artificial
photoperiod began and ended six hours after normal sunrise and sunset. Birds
were confined for at least five days under these conditions. That is, if the
sun normally rose at six am, the lights in the room would go on at 12 noon. If
sunset was a 6 pm the lights in the room would go off at midnight. On the first
sunny day after the birds had experienced the shifted condition for five days
the birds were allowed to recover their caches. All 48 holes were now open and
filled with sand. A single seed was placed in the holes where the bird had
originally cached. In addition, a single seed was also placed in the cups 90
degrees clockwise from the original set. If the birds were using their sun
compass than these 90 degrees clockwise locations would be the probed by the
searching bird.
3. Re-shift to normal photoperiod.
While birds were still in the clock-shifted condition they were again allowed
to cache in the octagonal aviary. After caching, however, the internal clock of
the birds was shifted back to normal, which is a six-hr. fast clock shift. Now
the light would go on and off at the time coinciding with the normal outdoor
light/dark cycle. Recoveries were conducted as in 2. above with both original
and shifted holes containing a seed.
4. Control 2. Same as in Control 1.
Figure 42 gives the vectors indicating the
center of probing activity when recovering caches for individual birds of the
three species. In Control 1, the majority of the vectors are pointed toward the
segment originally cached in. After the six hr. clock shift the majority of the
pinyon jays and scrub jays show the clockwise deflection indicating that the
sun compass is being employed to relocate their caches. The Clark=s nutcracker, however, continued to mainly
search in the original sectors. Under the Reshift condition all three species
show expected counterclockwise deflection. The rather short vectors for the
nutcracker, however, indicate a large amount of scatter. In Control 2, the
pinyon jay and scrub jay showed a tendency to probe left of the caching sector.
These experiments show that resetting the
internal clock influences the location where birds probe for previously hidden
seeds. This strongly suggests that compass information is also involved, in
some manner, in the spatial memory system of these birds. These findings are
especially of interest because the courtyard where the aviary was located was
rich with a diverse set of landmarks.
Species difference in response to the resetting
of the internal clock were evident. Nutcrackers showed a response in only the
reshift condition, and that was weak.
Pinyon jays and scrub jays, on the other hand showed significant responses to
both shift and reshift manipulations. Thus, it appears that the sun compass is
a more important component of spatial memory in these jays and is less
important for nutcrackers. We can suggest some possible reasons for this
difference.
Nutcrackers live at high elevations where the
trees of the coniferous forests often form complete canopies, impeding any
sunlight from reaching the forest floor. In spring, autumn and winter these
high elevation habitats have many cloudy, overcast, rainy days. Also, maybe the
sun compass is not effective when nutcrackers must dig through deep snow to
recover their caches.
The pinyon and scrub jay life at lower
elevations where the canopy of the ponderosa pine forest and pinyon-juniper
woodlands are open as there are fewer trees present. Sunny days are more prevalent at these lower
elevations, and less snow is present in winter, especially in the woodlands.
Therefore the general habitat structure and
prevailing weather conditions in the environments of the two jay species may be
more conducive for sun compass use. For the Clark=s nutcracker the sun compass may represent a
factor not always present, or easy to use, so they rely on other cues to locate
their caches.
The Evolution of Seed Caching In the Clark=s Nutcracker, Pinyon Jay,
Western Scrub Jay and Mexican Jay.
We began this chapter with a description of the
environment within which these four species live, the San Francisco Peaks in
north central Arizona. How did this particular set of species end up on this
mountain?
The origins and dispersal patterns of these
species is well understood. The Clark=s nutcracker is undoubtedly of Old World origin, a close relative
of the Eurasian nutcracker (Nucifraga caryocatactes). It probably
invaded the new World by crossing the Bering Land Bridge about one million
years ago during the Pleistocene. It may even have carried a pouch full of
seeds across the strait (Stegmann 1934, pers. communication, Lanner 1981,
Tomback 1983)! The mountains of Alaska, Canada, and western North American were
covered with alpine coniferous forest. This habitat supplied the early invaders
with the requisites needed for survival and reproduction. The corridor
stretched from Berangia to central Arizona, allowing the nutcracker ease of
passage from north to south. Nutcrackers have strong, long wings for rapid,
long distance flights so latitudinal movements and flights up and down
mountains were probably swift and efficient.
The origin of the
jays in this study probably occurred on the Mexican Plateau located in the
southwestern USA and northern Mexico (Pitelka 1951) The three species are
closely related (de los Monteros and Cracraft 1997) These birds then dispersed
from their ancestral home and were possibly in their present locations by the
end of Pleistocene, about 11,000 years ago. The difference in origin between
the jays and the nutcracker brings a whole series of issues to bear on the
evolution of the seed caching traits (Figure 44,a, b, c).
A reoccurring
pattern in the results from our various experiments was the specialization
gradient whereas species most dependent on their seed caches were most
specialized in morphology, behavior, physiology, and psychology, particularly
in spatial memory ability. In this specialization gradient Clark=s nutcrackers and pinyon jays demonstrated the
most accurate spatial memory, and the Mexican and western scrub jay showed only
modest spatial memory. The evidence reviewed above suggests that the differences
among scrub jays, Mexican jays and pinyon jays represent divergence while the
similarities between nutcracker and pinyon jays represent a case of
convergence. According to this view seed caching behavior has evolved in the
family Corvidae at least twice, once in the Old World and once in the New
World. The pinyon jay appears to be a
nutcracker “want-to-bes”.
The degree of convergence between Clark=s nutcrackers and pinyon jays is intriguing in
terms of the kinds of and degrees of adaptations. The three tables are designed
to show the different types of traits that show divergence and convergence
among the four seed caching species of corvids.
Summary
The cognitive
abilities of the seed caching species reveals some interesting patterns of adaptations.
The responds of the four species to the presence of pinyon pine seeds differs
dramatically. Two species show a major integration of adaptations in all
aspects of their lives, while two other species show only modest adaptations
for this habit. These adaptations all build on one another. For example, the
caching of thousand of seeds would be wasteful if the cacher forgot the
locations of the caches, or placed them were other animals could easily find
them.
Of interest here is the fact that only the nutcracker
has a larger than expected hippocampus. The other seed specialist, the pinyon
jay does not (Basil et al. 1996). Thus, either the hippocampus does extra Aduty@ or other areas of the
brain have been recruited to aid in the memory for seed caches in the pinyon
jay. However, new evidence suggests that hippocampus size does not correlate
with spatial memory ability.
Another example of the integration of these
adaptations is the life history trait of early breeding by nutcrackers and
pinyon jays in response to a large crop of pine seeds. Breeding in February and March would be highly
ineffective if the breeders did not build large well insulated nest to counter
the cold weather, and effectively locate caches (even through deep snow). The
energy from these seeds provides the reproductive energy to form eggs, provides
heat for incubation and brooding, and provides food for the nestlings. To
utilize this food nestlings must have the
physiological ability to digest these pine seeds. Many more examples of this integration
could be given for these seed caching species. In conclusion, cognitive
abilities are interlinked with all other characteristics of the species to form
an integrated adaptive suite of characters that contributes to the biological
fitness of the species possessing these suites.
Acknowledgments
The
findings presented in this chapter are the results of support from the National
Science Foundation and the National Institute of Mental Health. We also thank
our respective institutions for their continuous support and encouragement
during all phases of this research. We are deeply indebted to the hundreds of
students, both graduate and undergraduates that participated in these studies
(obviously there are far too many to list).
Without their help this story could not be told. We must thank the four species of seed caching
corvids for their cooperation and willingness to participate in these studies.
One must see to believe what these birds can accomplish!
Afterword
The
field and laboratory studies described above took place over a 40 year period
starting in the late 1960,s and continue until present. During this time period
many things have changed. Habitat destruction due to human intrusion and
devastating wildfires have caused entire flocks of jays
to shift their home ranges. There has also been an increase in nest predators,
particularly American crows (Corvus brachyrhynchos) and common ravens (Corvus corax) (Marzluff and Balda, 1992). Since
1999 the area where our field studies are
conducted has experienced severe drought. This drought is possibly the most
severe this area has experienced in the past 500 years (T. Whitham pers.
comm.). Trees that are stressed because of low soil moisture are particularly
susceptible to infestation by bark beetles. Due to the combination of moisture
stress and beetle attack, hundreds of thousands
(possibly millions)
of pinyon
and ponderosa pine trees are dying on our study
area (Figure 45, 46). Also, there has been no cone crop in the past four years.
This massive mortality event coupled with the lack of pine cone production in
trees that are still alive, posses a severe selective event for all the
resident birds and could have especially serious fitness consequences for the seed
caching corvids. One could predict, based on the specialization gradient
described above, that the nutcracker and pinyon jays will be most heavily
impacted and the western scrub jay and Mexican jay would be affected to a
lesser extent. This situation is presently being monitored.
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