Download Competition Among Insects, Birds and Mammals for Conifer Steeds

AMF.R. ZOOL., 19:1065-1083(1979).
Competition Among Insects, Birds and Mammals for Conifer Steeds
CHRISTOPHER C. SMITH
AND
Department of Biology,
Museum of Northern Arizona,
Route 4, Box 720,
Flagstaff, Arizona 86001
RUSSELL P. BALDA
Department of Biological Sciences,
Northern Arizona University,
Flagstaff, Arizona 86011
SYNOPSIS. Species of at least 5 orders of insects, 6 families of birds, and 2 orders of mammals,
in various combinations, can exploit the cones and seeds of most species of conifers.
Lodgepole pine is the exception to this pattern of broad taxonomic diversity of seed
predators in that only pine squirrels and coreid bugs attack its serotinous cones. The contrast
between lodgepole pine and other conifers demonstrates that large intrinsic variation in the
abundance of a resource fosters the evolution of a broad range of taxonomic groups to
exploit the resource. The diverse groups'are limited by different predators and alternate
resources when conifer seeds independently decrease in abundance.
INTRODUCTION
Because conifers are such an important
source of lumber, a great amount of effort
has been put into the study of their biology
(Fowells, 1965), their seeds (USDA, 1974),
and the predators of their seeds (Keen,
1958). People concerned with the lumber
industry are interested in how many seeds
escape predation to allow reforestation of
logged or burned areas. Questions of general biological interest that do not relate
directly to reforestation may go unasked
even though pertinent information is available. In this paper, we use the extensive
literature on conifer seeds and their predators to outline the nature of these seeds as a
food resource and the manner in which the
various seed predators use this resource.
The information can then be used as a basis
for answering three questions: 1) Why are
there many different distantly related taxa
of animals exploiting a distinctive and easily
delimited resource? 2) How do the various
taxa interact in using the resource? 3) How
do the different taxa avoid competitive ex-
elusion? Our personal experience is mainly
limited to the conifers of western North
America and our discussion will be concentrated on those, although some of the patterns probably apply generally to conifers
in the Northern Hemisphere (Bock and
Lepthien, 1976).
THE RESOURCE
As a food resource, single viable eonifer
seeds are highly uniform as to size (weight
of female gametophyte and embryo) and
quality (caloric value of female gametophyte and embryo) within an individual
cone, tree or species population (Table 1).
The total number of viable seeds in single
cones within a single annual crop for one
tree or a species population is more variable
than seed size or quality, especially in
lodgepole pine (Pinus contorta Dougl.) (Table 1). The sizes of annual cone crops for
single trees or species populations are by far
the most variable feature of conifer seeds in
all western North American species, except
lodgepole pine (Table 1).
The variation in caloric value of seeds
given in Table 1 is probably an underestiWe wish to thank Jim Reichman forstimulatingusto mation because 5 to 10 seed kernels were
think about competition between distantly related burned to derive each value thus masking
taxa. Gary Bateman and Gilbert Schubert made helpful comments in reviewing the manuscript. Anne the variation between individual seeds. The
Slobodchikoff was very helpful in editing and typing similar variations between samples from
the manuscript.
the same cone, cones from the same tree,
1065
TABLE l. l he source oj variation in conij
'er seeas as ajooa resource.
Species
Source of units
Number
Range
o
Mean
Coefficient of variation
<y>
Caloric value of female gametophyte and embryo (Cal/g dry weight):
Lodgepole pine
Lodgepole pine
Lodgepole pine
groups of 6 to 10 seeds from one cone
groups of 6 to 10 seeds from one tree
groups of 5 to 10 seeds from one
population
Engelmann spruce
Lodgepole pine
Lodgepole pine
seeds from one cone
seeds from one cone
10 means of seeds from 10 cones
r ff~l fTT\ t~\ n ^A t *" ^~» *~i
irom one tree
6 means of seeds from 6 cones from
different trees
5
6
7
6.55-6.91
6.63-7.04
6.54-6.96
6.74
6.79
6.83
2.0%
2.3%
2.2%
Weight of female gametophyte and embryo (mg/seed):
Lodgepole pine
40
25
10
1.6-2.0
1.7-2.3
2.01-3.27
1.91
1.88
2.49
7.5%
9.5%
14.8%
6
1.88-3.63
2.53
24.0%
H
Filled seed content of cones (filled seeds/cone):
Lodgepole pine
Lodgepole pine
Ponderosa pine
Ponderosa pine
cones from one tree
10 means of cones from 10 trees
cones from one tree
7 means of cones from 7 trees
5
10
5
7
9-23
4.4-18.8
53-89
39.0-70.4
15.8
11.6
70.4
53.5
40.4%
39.5%
22.9%
20.6%
Annual cone crops (cones/tree or cones/acre):
Douglas-fir
Ponderosa pine
11 annual means for several trees
(cones/tree)
10 annual crops (cones/acre)
11
10
0-14,244
316-7521
Ponderosa pine
Lodgepole pine
smaller crop/larger crop x 100 for 10
pairs of successive years
smaller crop/larger crop x 100 for 9
pairs of successive years
smaller crop/larger crop x 100 for 4
pairs of successive years
z
O
4219
124.6%
2437
93.1%
Ratios of successive cone crops (%):
Douglas-fir
p
p
(*>
10
0.0-67.2
6.9
9
4.2-94.4
40.2
4
50.8-73.5
62.4
>
COMPETITION FOR CONIFER SEEDS
1067
and trees from the same population indi- equal in size (Table 1), and the variation is
cate, however, that differences between not significantly greater in numbers of
cones and trees add little or nothing to the seeds per cone in cones taken from several
variance in seed quality (Smith, 1968). The annual crops than in cones taken from one
coefficient of variation differs from 5.5% to crop (C. C. Smith, unpublished data).
14.9% for seed weight within 15 different
The selective pressures influencing the
individual lodgepole pine cones. The cone evolution of these resource patterns have
with the median value was used as the become increasingly clear in the past few
example in Table 1. The seeds from one decades. The adaptive basis of these patcone of Engelmann spruce (Picea engelman- terns will help in understanding the extent
nii Parry) had a coefficient of variation to which interactions between seed predawithin the range found for cones of lodge- tors have influenced the nature of their
pole pine (Table 1). A median value for 10 seed resources. Smith and Fretwell (1974)
trees was also used for the value of the have argued that there is an optimum balcoefficient of variation for seeds/cone ance between size and number of offspring
within a tree for lodgepole pine. The values which tends to set narrow limits to the
for cones/tree were taken from large, dom- amount of energy invested in individual
inant Douglas-firs (Pseudotsuga menziesii offspring (seeds). Baker (1972) has proMirb.) left exposed as seed trees after the vided evidence that in climax communities
surrounding forest was logged (Garman, soil moisture stress is the main environmen1951). The cone production in these trees tal variable influencing the amount of enwould not be suppressed by competition. ergy reserves a species is selected to deposit
The values for cones/acre were taken from in seeds to allow the seedlings to develop a
an uncut mixed-age stand of ponderosa root system which can gather sufficient wapine (Pinus ponderosa Laws) (Larson and ter. Franklin (1964) has shown that the
Schubert, 1970). In 4 different years, C. C. moisture content of germination sites of
Smith sampled cone production in lodge- two conifer species in a climax community
pole pines by cutting down trees in the early does fit their seed sizes, with the smaller
summer and counting the two immature species being limited to moist microhabicone crops on each tree. The ratio between tats. In the coevolution of Clark's Nutthe two crops on all trees felled for each of crackers (Nucifraga columbiana Wilson) with
the 4 years can be compared to the ratios white-barked pine (Pinus albicaulis Engbetween successive crops for Douglas-fir elm.) (Tomback, 1977), and Pirion Jays
and ponderosa pine data (Table 1).
(Gymnorhinus cyanocephalus Wied) with pinyon
pine (Pinus edulis Engelm.) (Balda and
The large variation in the size of annual
Bateman,
1971; Ligon, 1978), large seed
cone crops causes an even greater variation
in the annual crops of seeds (C. C. Smith, size in the pine is coupled with birds caching
unpublished data). When trees produce seeds in dry, exposed soils.
their smallest female cone crop, they also
The number of seeds per cone is influproduce their smallest pollen crop (Allen enced by at least two factors: 1) As menand Owens, 1972). This results in less pol- tioned earlier, the annual variation in cone
len, a lower frequency of cross-pollination and pollen production leads to a correlation
and fertilization, and a lower number of between cone crop size and the frequency
viable seeds per cone when the cone crop is of viable seeds within a cone. The selective
smaller. This pattern of lower frequency of pressure influencing the variation in anviable seeds and fewer viable seeds per cone nual cone crops is discussed below. 2) The
in smaller cone crops has been reported for potential number of viable seeds per cone,
Douglas-fir (Garman, 1951), Sitka spruce as determined by the number of fertile cone
(Piceasitchensis (Bong.) Cam), western hem- scales, is influenced by selective pressures
lock (Tsuga heterophylla (Raf.) Sarg.) (Ruth from squirrels (Smith, 1970; Elliott, 1974)
and Berntsen, 1955), and ponderosa pine and probably other seed predators. Seed
(Larson and Schubert, 1970). Lodgepole predators also influence the amount of enpine has annual cone crops more nearly ergy in the cone scales, bracts and axis to the
1068
C. C. SMITH AND R. P. BALDA
extent that these structures protect seeds
from predation (Smith, 1970, 1975).
The large annual variation in cone crops
applies not only to individual trees but to
whole species populations and even groups
of species growing together locally (Garman, 1955), and over large areas (Lowry,
1966; Bock and Lepthien, 1976). For this
pattern to exist, individual trees within and
between species must be cuing their reproduction from the same proximate environmental factors. Root grafting between
neighboring trees (Bormann, 1966) could
help to coordinate single species in local
stands. Proximate factors which statistically
correspond to large cone crops in Douglas-fir in coastal forests of Washington and
Oregon are a warm January the year before crop maturation, a wet March and April 1.5 years before crop maturation, and
a cool July 2 years before crop maturation
(Lowry, 1966). Garman (1951) found that
large crops of Douglas-fir followed a dry
April 0.5 years before crop maturation in
coastal British Columbia and that one very
large crop never followed another.
There may be as many as four ultimate
selective advantages for the large fluctuation in size of annual cone crops: 1) The
physiological processes required for reproduction may work better under some weather regimes than others. 2) Weather may
affect the germination conditions for seed
crops in some predictable pattern. Smith
(1970) suggested that dry weather in the
spring before a crop matures may lead to a
die-back of the surface roots of established
trees and create a minimum of root competition for the seedlings resulting from germination of the seed crop the following
spring. 3) Because both male and female
cone crops very in phase, the density of
pollen experienced by the average female
cone is greater in variable crops than would
be the case with uniform annual crops (C.
C. Smith, unpublished data). Therefore,
variable cone crops result in a higher mean
frequency of viable seeds than would uniform crops. Eiset al. (1965) have shown that
for trees with variable cone crops in damp
coastal forests of the Pacific Northwest, the
cost of large cone crops is derived from
photosynthesis of the same year, and that it
results in a reduced increment of trunk
growth. Such a pattern does not require
energy storage or extra transport of material which would result in an energetic cost
for varying the size of cone crops. Slower
growing species, such as pinyon pine, may
require more energy for a large cone crop
than for a one-year growth increment in
trunk and limbs. Consequently, they may
have no alternative but to store energy for
mast years. 4) Having crop failures between
mast years leads to decimation of seed
predators and allows a large fraction of the
seeds in the mast crops to go uneaten (Garman, 1955; Keen, 1958; Smith, 1968, 1970;
Janzen, 1971). The average number of
seeds surviving predation is greater than if
the trees had annual crops of a uniform size
or if trees varied their crops out of phase
with each other.
The ultimate advantages gained from
variable cone crops in terms of physiological conditions for reproduction (1) and frequency of pollination (3) would only cause
the individuals of one species of tree to
vary their reproduction in phase with each
other. The advantages gained in terms of
improved germination conditions (2) and
predator escape (4) would cause the individuals of different species to be in phase
provided that germination conditions, such
as low competition for moisture, applied to
all species, and that some predators could
feed on different species of conifers, as is
true for some insects and most birds and
mammals.
Female pine cones require two or three
years to mature, depending on the species,
while all other conifers require only one
year for cone maturation. As a result of this
difference, pines cannot cue the variation in
their cone crops off the same weather factors as other conifers. Garman's (1955) data
show that the sizes of cone crops in western
white pine (Pinus monticola Dougl.) do not
correlate well with those in grand fir (Abies
grandis (Dougl.) Lindl.) and Douglas-fir.
Nonetheless, Garman (1955) and Schubert
and Adams (1971) find numerous years in
which both groups of conifers fail. The synchronous variation in the size of cone crops
1069
COMPETITION FOR CONIFER SEEDS
in most pines seems to be limited to small
geographical areas and to be of a smaller
magnitude than in other conifers.
Local weather patterns in the mountainous western U. S. appear to be-governed, to
a large extent, by local or regional topographic features. This may be especially
true in the lower, drier habitats where most
western pines are found. There is little
doubt, however, that at least some species of
pines produce cones in synchrony with
their conspecifics in the same habitat. Pinyon pines (Ligon, 1971, 1978; Balda and
Bateman, 1972; Vander Wall and Balda,
1977) produce a large cone crop on the
average of once every 6— 7 yr. In some of
the intervening years, virtually all trees will
lack cones. This variation is not only of a
local nature, but may exist over hundreds
of square kilometers in Arizona, New Mexico, Colorado, and Utah (Balda and Ligon,
unpublished data).
An additional factor that must be considered in a discussion of seed predation and
competition is the difference in dispersal
strategies of the pines. Some pines have
their seeds dispersed by wind, whereas
others rely almost solely on animals for seed
dispersal. These latter species of pine have
developed a constellation of morphological
adaptations that not only allows animals
easy access to their seeds, but may actually
entice the dispersal agents which appear to
be birds of the family Corvidae.
Table 2 compares an enticer pine to a
non-enticer in terms of 7 morphological
features. All enticers allow seeds to be easily
located, extracted from cones, eaten and
cached for future use. The two best studied
enticer species are Pinus albicaulis (Tom-
back, 1978) and Pinus edulh (Vander Wall
and Balda, 1977; Ligon, 1978). In both
cases the dispersal agent is also a seed predator, but it caches far more seeds than it
uses in years of high cone crops.
The amplitude and frequency of synchronized cone crops may be different between enticer and non-enticer pines. Larson
and Schubert (1970) report for ponderosa
pine in north-central Arizona that over' a
52-yr period, this species produced large
crops (greater than 3,000 cones per acre)
every 5 yr. The interval between large cone
crops is thus 1 or 2 yr less in ponderosa
than in pinyon pine. In addition, the
amplitude may be different. The above authors report a low of 316 cones to a high of
7,521 cones/acre over a 10-yr span. Although this is a 2200% increase in cone
production, pinyon pines show an even
greater difference. Some years, pinyon
pines produce absolutely no mature cones/
acre (Balda, unpublished data), whereas
other years they can produce as many as
1800 cones/tree (Ligon, 1971).
A final important consideration for the
use of conifer seeds as a resource is the ease
of their location by seed predators. While
still in the cone on the tree, seeds are
clumped in predictable and easily discovered locations. The visible development
time of cones lasts from 6 mo to 2.5 yr in
some pines. Even before the cone crop matures, some birds can adjust molting time
(Ligon, 1978) and some mammals (Smith,
1968) can initiate reproduction and adjust
litter size to the size of the seed crop. Once
seeds are shed from the cone, they are
much less clumped and their location is
much less predictable. In most conifer
TABLE 2. Features ojpines with different dispersal strategies.
Characteristics:
1.
2.
3.
4.
5.
Seed size
Wings present on seeds
Seed quickly released from cone
Seed coat indicates seed quality
Cone positioned for easy vision
of seed and/or access to seed
6. Spines present on cone scales
7. Seed coat thickness
Non-enticer pine
Enticer pine
generally small
generally larger
yes
yes
no
no
no
no
yes
yes
yes
no
relatively thick
relatively thin
1070
C. C. SMITH AND R. P. BALDA
forests, freezing weather predominates between the time seeds are shed and the time
when they germinate and this precludes
their use by insects after they are shed.
In summary, conifer seeds in cones are
an easily located, clumped resource that is
generally uniform in size and quality, but
extremely variable in abundance through
time. Predators of conifer seeds experience
either feast or famine. Lodgepole pine is an
exception to this pattern and should serve
as a control for the effects of annual variation in cone crops.
their long mouth parts to exude an enzyme
to digest portions of the cone scales and
seed coat (Koerber, 1963; Krugman and
Koerber, 1969). Coreid bugs do attack the
nonserotinous races of lodgepole pine, but
no one has reported seeing them on the
serotinous race. The pentatomid bug, Tetyra bipunctata (Herrick-Schaeffer), can attack Pinus banksiana Lamb. (Gilbert et al.,
1967), the serotinous ecological equivalent
of lodgepole pine in eastern North America. The hole pierced in the seed coat by the
bug is not visible to the naked eye. The
empty seed coats with shriveled female
gametophytes are similar to those resulting
THE COMPETITORS
from lack of fertilization after pollination
Effective seed predators are found in at (Krugman and Koerber, 1969); this exleast 5 orders of insects, 6 families of birds, plains why seed damage caused by these
and 2 orders of mammals (Table 3). Each bugs went so long undetected (Koerber,
group is characterized by its method of 1963).
exploiting conifer seeds and its means of
Flies in the genera Oscinella Becker and
escaping starvation during years of low Hylemya Robineau-Desroidy and moths in
seed production (Table 3). In this section, the genera Eupithecia Crt., Barbara H. Edwe will summarize some of the literature on wards, Eucosma Hbn., Laspey resia Hbn. and
the biology of seed predators as a basis for Dioryctria Zell. lay their eggs between scales
understanding the nature of competition or on the surface of conifer cones of many
between groups.
genera. The larvae mine their way through
the scales of nearly mature cones, eating
several ripe seeds in the process. The larvae
Insects
may pupate in the cone or on the ground.
Insects have four general methods of at- The cone is very seldom killed before the
tacking conifer cones as described by Keen seeds mature, and some seeds in most cones
(1958) and Krugman and Koerber (1969). escape predation. Adults do not feed on
Adult cone beetles (genus Conophthorus seeds.
Hopkins) chew into the stem or base of a
Flies in several genera of the family
developing pine cone to enter the axis of Itonididae and the genus Euromyia Zetthe cone where they chew several galleries terstedt and wasps in the genusMegastigmus
in which to lay their eggs. The adult activity Dalman oviposit their eggs between the
usually kills the cone before the larvae scales of young cones of many genera of
hatch out of the eggs and continue to mine conifers. Each larva develops in one seed,
the axis, scales and seeds of the immature the contents of which it consumes as its sole
cone. The larvae pupate in the galleries and source of energy. Adults do not feed on
metamorphose into adults in August. The seeds. Megastigmus causes the seed coat of
adults feed and overwinter in the cone, ponderosa pine to grow into and fuse with
emerging to attack new immature cones the its subtending cone scale, but cone develfollowing May or June. The beetles destroy opment is otherwise unaffected.
whole cones before the seeds mature and
Insects use four general patterns of esare available for other animals.
cape from starvation or lack of reproducBoth nymphal and adult stages of the tion that comes with very small cone crops.
coreid bug, Leptoglossus occidentalis Heide- Moths of the genus Dioryctria can develop as
man, digest and suck the liquified contents larvae in the buds and young twigs of the
out of developing and mature seeds of same species of conifers whose cones they
western Noth American conifers by using mine. These young tissues are used as an
TABLE 3. Outline of the biology of conifer seed predators.
Taxonomic group
of seed predators
INSECTS:
Order: Coleoptera
cone beetles
Genera of trees exploited
Leptoglossus occidentals
Order: Diptera
small cone maggot
genus: Oscinella
resin and gall midges
family: Itonididae
seed maggots
genus: Earomyia
large cone maggot
genus: Hylemya
Order: Hymenoptera
seed chalcids
genus: Megastigmus
Order: Lepidoptera
cone loopers
genus: Eupithecia
fir cone moths
genus: Barbara
pine cone moths
genus: Eucosma
seed moths
genus: Laspeyresia
coneworms
genus: Dioryctria
Method of escaping starvation
during cone crop failure
Pinus L.
adults and larvae mine immature
cones before seeds mature
exploiting cones before competitors,
alternate food for adults
Pinus
nymphs and adults suck seed
contents out of maturing cones
emigration
Abies, Picea A. Dietr. Pinus
larvae mine several seeds
emigration?
Abies, Picea, Pinus, Thuja L.
Pseudotsuga
Abies, Larix Mill., Picea, Pinus,
Pseudotsuga, Thuja
Abies, Picea, Tsuga
larval development in one seed
variable diapause
larvae mine through one or two
seeds
larvae mine several seeds
variable diapause
3
variable diapause
n
o
Abies, Picea, Pinus, Tsuga,
Pseudotsuga
larval development in one seed
variable diapause
Abies, Picea, Pinus, Pseudotsuga,
Tsuga
larvae mine several seeds
emigration?
Abies, Picea, Pseudotsuga
larvae mine several seeds
variable diapause
Pinus
larvae mine several seeds
emigration?
A bies, Picea, Pinus,
Pseudotsuga
Abies, Larix, Picea Pinus,
Pseudotsuga
larvae mine several seeds
variable diapause
larvae mine several seeds
twigs and buds as alternate food
for larvae
genus: Conophthorus
Order: Hemiptera
seed bugs
Method of conifer exploitation
o
o
H
5
z
z
F1
SO
<*>
w
o
NO
TABLE 3. continued
Taxonomic group
of seed predators
Genera of trees exploited
Method of conifer exploitation
Method of escaping starvation
during cone crop failure
BIRDS:
Family: Psittacidae
parrots
genus: Rhynchopsitta
Family: Picidae
Hairy Woodpecker
White-headed Woodpecker
genus: Picoides
Family: Corvidae
Pifion Jay
genus: Gymnorhinus
Clark's Nutcracker
genus: Nucifraga
Gray Jay
genus: Perisoreus
Steller'sjay
genus: Cyanocitta
Scrub Jay
Mexican Jay
genus: Aphelocoma
Black-billed Magpie
genus: Pica
Family: Paridae
Mountain Chickadee
Pinus
extracted seeds from closed and
open cones
emigration, nomadic
Pinus
extracted seeds from closed and
open cones eaten by adults
andjuveniles
alternate foods
Pinus
cache seeds extracted from closed
and open cones to feed young
and adults
cache seeds extracted from open
and closed cones to feed young
and adults
may extract seeds from open cones
or retrieve from ground to eat
and store as boli
cache seeds from open cones to
feed adults
cache seeds from open cones and
ground to feed adults
alternate foods, emigration
Pinus
Abies, Picea
Pinus
Pinus
H
alternate foods, emigration
>
D
alternate foods, territorial
alternate foods, territorial, emigration
alternate foods, territorial
Pinus
cache seeds from open cones and
ground to feed adults
alternate foods, territorial
A bies, Picea, Pseudotsuga, Pinus
cache seeds from open cones and
ground to feed adults
cache seeds from open cones and
ground to feed adults
cache seeds from open cones and
ground to feed adults
alternate foods
Boreal Chickadee
Abies, Picea, Pseudotsuga
Plain Titmouse
genus: Parus
Pinus
alternate foods
alternate foods, territorial
o
Family: Sittidae
White-breasted Nuthatch
Red-breasted Nuthatch
Pygmy Nuthatch
genus: Sitta
Family: Fringillidlae
crossbills
genus: Loxia
Pine Siskins
genus: Carduelis
uses and makes cache of seeds and
finds seeds on ground
Abies, Picea, Pinus, Pseudotsuga, seeds from open cones cached and
Tsuga
eaten by adults
Abies, Picea, Pseudotsuga, Pinus seeds from open cones cached and
eaten by adults
Pinus
Abies, Larix, Picea, Pinus,
Pseudotsuga, Tsuga
Abies, Larix, Picea, Pinus,
Pseudotsuga, Tsuga
seeds from closed and open cones
fed to young and adults
seeds from open cones and the
ground fed to young and adults
alternate foods
alternate foods, emigration
alternate foods
O
nomadic nesters, emigrate to
alternate foods
emigration, alternate foods
MAMMALS:
Order: Rodentia
pine squirrels
genus: Tamiasciurus
tree squirrels
genus: Sciurus
chipmunks
genus: Eutamias
golden-mantled ground
squirrel
Spermophilus Interalis
deer mice
genus: Peromyscus
red-backed voles
genus: Clethrionomys
Order: Insectivora
shrews
genus: Sorex
o
•o
PI
3
5
3
JO
Abies, Larix, Picea, Pinus,
Pseudotsuga, Tsuga
Pinus
cache and feed from whole closed
cones
seeds from closed cones
territoriality, emigration, alternate
foods
alternate foods
Abies, Larix, Picea, Pinus,
Pseudotsuga, Tsuga
Pinus
cache and eat seeds from closed or
open cones
forage for single seeds
alternate foods
Larix, Picea, Pinus, Pseudotsuga,
Tsuga
Larix, Picea, Pinus, Pseudotsuga,
Tsuga
forage for single seeds and
cache seeds
forage for single seeds and
cache seeds
alternate foods
Larix, Picea, Pinus, Pseudotsuga,
Tsuga
forage for single seeds
alternate foods
alternate foods
alternate foods
O
OS
1074
C. C. SMITH AND R. P. BALDA
alternate food during years when cone
crops are small or absent. Cone bettles have
also been observed to invade young twigs,
which the adults use as an energy source to
survive a second winter when cone crops
fail, but not for reproduction.
In some flies (Family: Itonididae, genera:
Euromyia and Hylemya), wasps (Megastigmus), and moths {Barbara and Laspeyresia)
individuals have been observed to diapause
over 1,2, and in some species, 3 winters.
These individuals emerge from the same
cones kept in storage, and presumably can
be the offspring of one parent, although
this relationship has not been established
conclusively (Keen, 1958). Having all diapause periods found in an optimum proportion in the offspring of each parent
would allow a larger population to be maintained than if the offspring inherited the
diapause period of their parents. The average parent with the varied offspring would,
therefore, leave more surviving offspring
than the average parent with only one type
of offspring.
Some bugs (Leptoglossus occidentalis), flies
(Oscinella), and moths (Eupithecia,Eucosma),
which lack both the above means of surviving very small cone crops, must be able to
either emigrate to areas of larger crops or
be highly successful in competing for the
few cones available. One would expect
these groups to be stronger fliers than the
others, but we know of no evidence to support that prediction. The coreid bugs do
attack pine cones at an earlier stage than
some seed predators, and by killing the
seeds before they mature, they eliminate
them from use by other predators.
Birds
sitta pachyrhyncha (Swainson)) has been
known to invade the coniferous forests of
southern Arizona in summer and autumn
and consume large quantities of pine seeds.
This large-billed bird can extract seeds
from green cones as well as from ripe ones.
The bird is reported to pull or twist off the
heavy cone scales to procure seeds (Wetmore, 1935). Wetmore also states that in
1917 this species consumed the entire cone
crop of Chihuahua pine (Pinus leiophylla
Schiede and Deppe) in the Chiricahua
Mountains! It is also known to eat large
quantities of pinyon pine and ponderosa
pine seeds (Vorhies, 1934). This species is
highly gregarious and may wander long
distances to find cone crops.
In the family Picidae two species of woodpeckers are known to make extensive use of
ponderosa pine seeds. Stallcup (1968,
1969) reported that Hairy Woodpeckers
(Picoides villosus L.) spend about 65% of
their foraging time extracting and eating
ponderosa pine seeds from mid-October
through February, the very time they form
mixed flocks with Pinon Jays (Balda et al.,
1972) which are doing much the same
thing. The woodpecker can perch on ponderosa pine cones and extract seeds by
probing between the cone scales and also
hammering these to shreds.
The White-headed Woodpecker (Picoides
albolarvatus Cassin) also extracts seeds from
pine cones (Tevis, 1953), and may subsist
for long periods of the year solely on vegetable matter, especially ponderosa pine
seeds (Beal, 1911). This species can tear
open hard, tightly closed cones and extract
seeds. During some portions of the year, it
may spend more than 60% of its time foraging on pine cones (Ligon, 1973). Ligon suggests that competition with Pygmy Nuthatches (Sitta pygmaea Vigors), Hairy
Woodpeckers, and Red Crossbills (Loxia
curvirostra L.), all conifer seed eaters, may
be extensive during cold spring months
when insects are still rare.
In the North American Corvidae, Clark's
Nutcrackers have co-evolved with whitebarked pine and possibly limber pine (Pinus
flexilis), and Pinon Jays with species of pin-
Six families of birds include species that
use and specialize on conifer seeds to varying degrees. The degree of specialization
ranges from simply eating seeds found on
the ground, to searching through open
cones and extracting seeds, to opening
closed cones with a specialized bill, to extracting seeds and caching them for future
use in sites that may favor germination.
Of the New World parrots (family Psit- yon pines (P.edulis,P. monophylla Torr. and
tacidae), the Thick-billed Parrot (Rkynchop- Freim.,P.quadrifolia Parl. exSudw.), (Balda
COMPETITION FOR CONIFER SEEDS
1075
and Bateman, 1972; Tomback, 1977; Van- ests, harvest seeds from open cones and
der Wall and Balda, 1977; Ligon, 1978). carry them back to be cached in the coniferBoth species of corvids cache thousands of ous forest. Scrub Jays (Aphelocoma coerulesseeds per bird in many small subterranean cens Bose) harvest seeds from open cones in
caches on areas that are relatively dry, the pinyon pine woodlands and cache them
snow-free, or where snow melt is early. The there. In parts of Utah where Steller's Jays
number of seeds cached per bird is esti- are absent, their role seems to be filled by
mated to be from 18,000 to 33,000 (Balda, the Black-billed Magpie (Pica pica L.) (Van1979). Vander Wall and Balda (1977) esti- der Wall and Balda, unpublished data).
mate that each Clark's Nutcracker stored
These five species of corvids vary morbetween 2.2 and 3.3 times the number of phologically, physiologically and behaviorseeds needed to survive the cold, insect-free ally in their ability to exploit the seed crop
period of the fall, winter and spring. The and respond to it (Vander Wall and Balda,
nesting season of these two species is usually unpublished data). The most specialized
in the winter or very early spring, and its morphological structure is the sublingual
timing is dependent on the amount of seeds pouch of the Clark's Nutcracker which can
cached the previous autumn (Ligon, 1971, hold about 19 g of seeds (Bocketal., 1973).
1978; Balda and Bateman, 1972). These Although this diverticulum of the floor of
seeds stimulate gonadal development, are the oral cavity appears (when full) as a
used for reproductive energy before and major morphological modification, its apduring nesting, and are fed to the young pearance is made possible by surprisingly
(Mewaldt, 1956; Ligon, 1971, 1978; Bate- minor modifications of the musculature of
man and Balda, 1973). Pinon Jays in some the mouth and throat.
areas may nest in the autumn, using seeds
As food storage is widespread in corvids,
harvested directly from pinyon pine trees further investigation will probably reveal
(Ligon, 1971). The presence of green cones many more interesting interactions beprovides the proximal cue for such breed- tween corvids and conifers. Species for
ing (Ligon, 1974).
which fragmentary information exists are
These two species are quite social during the Gray Jay (Perisoreus canadensis L.) which
the seed harvest period and flocks of up to may store conifer seeds in the form of pel300 Pinon Jays may work through pinyon lets (boli) covered with saliva (Dow, 1965;
pines together. Nutcrackers often harvest Ritter, 1969) and the Mexican Jay {Apheloin groups of 3 to 10. When all pine crops fail coma ultramarina Bonaparte) which eats and
and alternate foods are not available, these stores seeds oiPinus cembroides (Zucc.) when
species respond by emigrating either to abundant (Brown, personal communicaareas where crops are present, or to areas tion).
far from their normal breeding range
Nuthatches (Family Sittidae) with long,
where alternate foods are available (Davis slender, strong bills used for probing for
and Williams, 1964; Westcott, 1964). Some insects in bark crevices and needle clusters,
of these emigrants return to their original are also adept at probing between the scales
home ranges when conditions turn favor- of open conifer cones to remove seeds. All
able in the spring (Vander Wall and Balda, are omnivorous.
unpublished data).
The Pygmy Nuthatch, a bird of the pine
These corvids and others also eat and and mixed coniferous forests, consumes becache the smaller, wind-dispersed seeds of tween 86 and 98% vegetable matter during
ponderosa pine and Jeffrey pine (P.jeffereyi the fall and winter months. A large portion
Grev. and Balf.), (Balda and Bateman, of this is undoubtedly conifer seeds (Norris,
1971, 1972; Tomback, 1977). In northern 1958). This proportion varies significantly
Arizona and Utah when bumper crops of with size of the cone crop and climate. In
pinyon pine occur, three additional species areas of relatively mild winters, Pygmy
of corvids industriously harvest and cache Nuthatches concentrate on insect prey
the seeds. Steller's Jays (Cyanocitta stelleri (Anderson, 1976). When cones are abunGmelin) descend from the coniferous for- dant this species actively probes between
1076
C. C. SMITH AND R. P. BALDA
cone scales for seeds by perching either nuthatches, however, is probably cued to
right-side-up or up-side-down on a cone their summer diet of insects.
and pulling out the wings which they inIn the family Paridae, the Boreal Chickspect for seeds (Stallcup, 1968; personal ob- adee (Partis hudsonicus Forster), the Mounservation). In ponderosa pine, a single bird tain Chickadee (Parus gambeli Ridgway), the
can pull out about one wing every second Mexican Chickadee (Parus sclateri Kleinand search through an entire cone in less schmidt) and the Plain Titmouse (Parus inthan one minute (personal observation). ornatus Gambeli) all consume large quanThis species also consumes or caches seeds tities of conifer seeds when available
that it finds on the ground. Occasionally it (Haftorn, 1974; personal observation).
will cache conifer seeds in crevices in dead These species are all omnivorous and pertrees, stumps or under bark scales of live manent residents of coniferous forests. The
trees. Sometimes these seeds are later lo- Boreal Chickadee also stores seeds of
cated and eaten by conspecifics as well as spruce in crevices on thick branches close to
other bark gleaning and probing birds the main trunk or on the main trunk where
(personal observation).
they are available during periods of heavy
snow.
Seeds are fixed in place with the aid
T h e White-breasted Nuthatch (Sitta
carolinensis Latham), the most general for- of spider webbing and downy materials
ager and dietarily least specialized of the from plants (Haftorn, 1974). In coniferous
nuthatches, appears to spend less time forests Mountain Chickadees eat and store
foraging on cones than the other nuthatch pine seeds for future use. Chickadees exspecies. Occasionally, it discovers cached tract seeds from cones on trees and forage
seeds or seeds on the ground that have been for them singly on the ground. Seed caches
recently released from cones. This species made in bark crevices are sometimes covalso caches pine seeds in crevices and often ered. Plain Titmice, even with their short
covers these cached seeds with a piece of bills, can extract seeds from Pinus edulis
bark, twig or lichen (Kilham, 1974; per- cones because of the short cone scales. This
bird searches vigorously for edible seeds on
sonal observation).
In north-central Arizona, Red-breasted the ground below trees, and it caches them
Nuthatches (Sitta canadensis L.) eat and for future use (personal observation). In
cache seeds of spruce, fir and pine. Seeds light of work by many Europeans on memare obtained by bill probing between cone bers of this genus, it is probable that most, if
scales in a manner similar to the Pygmy not all, North American parids eat conifer
Nuthatch. Caches are often covered as de- seeds when available.
scribed for the White-breasted Nuthatch.
In the Family Fringillidae, the crossbills
Although it takes considerable time (and (Loxia L.) are most highly adapted to expresumably energy), this species can ham- ploiting conifer seeds. They can pry open
mer open the hull oiPinus edulis seeds. The closed cones with their specialized crossed
Red-breasted Nuthatch is primarily a bird mandibles and remove seeds with their
of the mixed coniferous forest, but it will tongue (Robbins, 1932). They will either
invade lower elevations in years of high pick cones and hold them with their feet
pinyon pine cone production (Vander Wall while extracting seeds, or work around the
and Balda, unpublished data).
cone while it is attached to the tree. They do
Of the above three species, only the not cache seeds, but will nest at any time of
Red-breasted Nuthatch seems to be so heav- the year, feeding their incubating and
ily dependent on conifer seeds for winter brooding mate and the nestlings with confood that it undergoes periodic irruptions ifer seeds from large cone crops (Tordoff
into other habitats and regions when all and Dawson, 1965). They escape the probconifers in its breeding habitat fail to pro- lem of poor cone crops by being very
duce a cone crop. It is one of 9 North nomadic, nesting wherever and whenever
American boreal species that undergo syn- they find a large crop (Austin, 1968). The
chronous eruptive emigrations (Bock and more boreal species (Loxia leucoptera GmeLepthien, 1976). The breeding season of all lin) participates in synchronous eruptive
COMPETITION FOR CONIFER SEEDS
emigrations along with other seed-eating
species (Bock and Lepthien, 1976).
Pine Siskins (Carduelis pinus Wilson) lack
adaptations for opening closed cones and
are limited to pulling seeds out of opened
cones or foraging for them on the ground.
Like the crossbills and corvids, they are
highly social and can nest in early spring by
having one member of the mated pair provide seeds and insects for the other during
incubation and brooding. The young are
fed seeds and insects by the brooding
female (Austin, 1968). Siskins also escape
seed shortages by eruptive emigration
(Bock and Lepthien, 1976).
Some grosbeaks (Hesperiphona vespertina
Cooper, Pinicola enucleator L.) and finches
(Carpodacus purpureus Gmelin, C. cassinii
Baird) and other large-billed fringillids also
include conifer seeds in their diet (Martini
al., 1951). They start nesting late in the
spring, however, when there would be few
or no conifer seeds available. The seeds of
deciduous trees or buds are usually more
important in their diet than conifer seeds,
and they should probably not be considered
conifer specialists (Austin, 1968). Some of
these species do, however, show eruptive
movements in some years (personal observation).
In the above discussion, behavior of caching conifer seeds was mentioned but detailed comments were not provided on its
variety and significance. Members of the
Corvidae usually make subterranean caches
that provide long-term dietary insurance.
They are also committed behaviorally to the
caching of large numbers of seeds each autumn. Nuthatches and tits, by contrast, do
not appear so committed to this behavior
and spend relatively long bouts foraging
for other foods or eating seeds when cone
crops are dense. These smaller species may
be limited by energetic demands that are of
an immediate nature. These birds may
simply not carry around enough energy reserves to devote the necessary time to caching copious amounts of seeds, or they must
forage intensively so that they can withstand the relatively long, cold nights experienced in the coniferous forest during
autumn and winter. Larger birds, such as
the Pifion Jay and nutcracker must be car-
1077
rying enough energy reserves to allow them
to spend considerably more time caching
conifer seeds. Another major difference is
the length of time food items are stored.
During protracted cold weather and/or
early mornings, tits and nuthatches may
deplete their caches so that food storage is
only a short term rather than a long term
phenomenon.
Another interesting question is, why is it
that members of the family Fringillidae do
not cache conifer seeds. Many have heavy,
thick bills specialized for efficiently opening
seeds, and many do consume conifer seeds,
yet to our knowledge no reports exist, nor
have we observed fringillids caching. All
members of this diverse family that breed in
coniferous forests use other strategies to
overwinter. It is possible that the very structure that allows them to be seed-eating
specialists (a short, stocky bill) precludes the
possibility of efficiently caching conifer
seeds. The short, heavy bill is not especially
agile, and seeds could not be buried deeply
in the ground or in crevices.
Mammals
Pine squirrels (Tamiasciurus Trouessart),
chipmunks (Eutamias Trouessart), golden-mantled ground squirrels (Spermophilus lateralis Say), deer mice (Peromyscus
Gloger) and red-backed voles (Clethrionomys
Tilesius) are the five genera of rodents that
exploit conifer seeds in most of the forests
of western North America. Tassel-eared
squirrels (Sciurus aberti Woodhouse) replace
pine squirrels in ponderosa pine forests in
parts of the Southwest. The western gray
squirrel (Sciurus griseus Ord) extracts seeds
from the cones of low elevation pines in the
Pacific Coast states. Shrews (Sorex L.) may
also include conifer seeds as a large fraction
of their diet (Moore, 1942).
The pine and tassel-eared squirrels pick
closed cones and chew off scales to extract
the seeds. Pine squirrels have a territorial
system that allows them to harvest cones
and defend them as a winter food supply in
a central cache (Smith, 1968). Tassel-eared
squirrels are not territorial (Farentinos,
1972), nor do they store large quantities of
cones. Instead they use pine bark and fungi
1078
C. C. SMITH AND R. P. BALDA
as a winter food supply after ponderosa
pine seeds are shed from the cone (Keith,
1965; Golightly and Ohmart, 1978).
Eutamias townsendi Bach man can chew
open small cones (western hemlock, Douglas-fir) (Smith, 1968), but£. amoenus (J. A.
Allen) pulls seeds from large cones (ponderosa pine) as the cones open naturally
(Broadbooks, 1958). Chipmunks harvest
and store the seeds of many herbs and
shrubs (Aldous, 1941; Broadbooks, 1958)
and are probably much less dependent on
conifer seeds than are the tree squirrels.
Golden-mantled ground squirrels, deer
mice, red-backed voles and shrews all forage for individual seeds on the ground.
Shrews use seeds as a supplement to their
main diet of insects and other animal flesh.
Golden-mantled ground squirrels supplement a diet of foliage and fungi with seeds
in the fall before they hibernate (McKeever,
1964). Red-backed voles can supplement a
seed diet with foliage and bark (Hamilton,
1941). Deer mice are probably more dependent on seeds. Both deer mice and
red-backed voles may store seeds in small
scattered caches to help provide a winter
diet (Abbott and Quink, 1970).
Pine squirrels will emigrate tens of kilometers in response to cone crop failures,
and will concentrate in stands of deciduous
trees when there are no alternate conifer
crops available (Smith, 1968; Rusch and
Reeder, 1978). Deer mice will move over
0.5 km in response to changes in local
habitat (Gashwiler, 1959). Chipmunks,
golden-mantled ground squirrels, redbacked voles and shrews should be less
likely to move in response to cone crop failures because their diets typically contain a
larger component of alternate foods. Small
mammals should be less successful than
birds in escaping starvation by emigrating
because of their lower powers of movement.
Rusch and Reeder (1978) found that pine
squirrels maintained the same sized territories over a 3-year period of variable
cone crops in spruce forests. The territories
were large enough to allow them to have
sufficient winter food during the smallest of
the three cone crops. This would indicate
that the territorial system would have the
effect of dampening population fluctuation
while allowing a large proportion of the
large cone crops to go unused.
Birds and insects have different means of
avoiding the detrimental effects of small
cone crops. With their greater mobility,
birds can move further from area to area.
Such movements are most feasible when
mast crops are relatively local and a large
bird population is maintained by switching
to different locales from year to year.
Southern pines have mast crops that tend to
be mostly local in distribution and Pinus is
the only genus for which some bird species,
such as Pygmy Nuthatches and some corvids, seem to be specialized. Insects can
avoid population crashes by variable diapause which allows offspring from one
year to use three crops. Variable diapause,
however, dilutes the product of each reproductive effort over two or three years.
Where cone crops are least variable there
will be less advantage in spreading the maturation of one reproductive effort over two
or three years. It, thus, appears to be significant that 3 of the 5 genera of insects that
lack variable diapause specialize on pine
which have less variable crops than other
conifers.
Mammals lack both the above means of
concentrating their population numbers on
large crops, and consequently may be less
effective than birds and insects at exploiting
mast year crops. None of the three groups
seem to be able to concentrate in large
enough numbers to successfully exploit a
large percentage of the seeds from most
large regional mast crops.
THE COMPETITION
We know of no study that demonstrates
the ecological effects of competition for
conifer seeds by artificially manipulating
the density of some of the competing
species. Conifer seeds are particularly poor
for such manipulations because most predators attack them while they are still in
cones, high up in the canopy, and birds and
insects are too mobile to be easily controlled. That there is severe competition for
conifer seeds during poor cone crops can be
COMPETITION FOR CONIFER SEEDS
inferred from reports that the frequency of
seeds destroyed by insects is highest during
these times (Garman, 1951; Keen, 1958),
reaching levels of 80 and 90%. In addition,
the size of pine squirrel territories is adjusted to food supply (Smith, 1968; Rusch
and Reeder, 1978) and pine squirrels may
harvest the complete cone crop of some
species within their territories during poor
cone crops (Smith, 1968). Jays and nutcrackers eat essentially all seeds from small
crops of pinyon pine without storing and
dispersing any (Vander Wall and Balda,
1977; Ligon, 1978).
The level of exploitative competition
(Birch, 1957, meaning 1) experienced by
the different seed predators should increase with the sequence in which they attack the cones and seeds. All insects start to
exploit cones and seeds at some stage before the cones are mature. Cone beetles
eliminate all competitors by killing the
cones before they reach maturation and can
support animals which depend on mature
seeds. The other groups of insects finish
exploiting the cones and seeds at about the
same time as the cones mature, and therefore, they are ahead of birds and mammals.
Squirrels, Pifion Jays, Clark's Nutcrackers,
crossbills and some chipmunks can extract
seeds from closed cones. Pine squirrels,
however, can exploit cones faster than the
other vertebrates in the fall because they
store whole cones and do not have to spend
time extracting the seeds for external storage or conversion into internal fat storage
(Tomback, 1977). Siskins, nuthatches, Steller's Jays, Scrub Jays, magpies, chickadees,
woodpeckers, and some chipmunks are
next to exploit the seeds after the cones
open naturally, but before the seeds fall to
the ground. Deer mice, red-backed voles
and shrews gain access to the seeds only
after they have fallen to the ground.
Although being first to attack a cone or
seed is a distinct advantage in exploitive
competition, for insects it may lead to predation by competitors who come after; and
for birds and mammals that form caches, it
may lead to a loss of stored food (Birch,
1957, meanings 3 and 2 for competition).
Smith has observed tassel-eared squirrels
eating seed chalcids in the same manner as
1079
they eat seed kernels when chewing open
ponderosa pine cones and biting each seed
coat in half to expose its contents. Pine
squirrels, Pinon Jays and Clark's Nutcrackers, on the other hand, avoid insect infested
cones and seeds, presumably because the
insects have a lower energy content than
seeds, and, in addition, they might already
have escaped or spoiled in storage (Garman, 1955; Smith, 1968; Ligon and Martin,
1974; Vander Wall and Balda, 1977). Mice,
shrews, siskins and nuthatches which eat
each seed at the time when it is found,
would be losing food if they passed up an
insect infested seed.
Insects may have evolved avoidance mechanisms in response to vertebrate seed predators that might attack them. Pine seed
chalcids (Megastigmus albifrons Walker)
cause the seed coat within which they are
developing to fuse to the subtending scale
in ponderosa pine. Therefore, the seed
cannot fall when the cone opens, nor can
the seed be pulled from the cone by a tug on
the seed wing by birds or chipmunks because the chalcid-modified seed is more
firmly attached to the cone scale than to the
wing. The chalcids thus eliminate all predators that cannot tear or peck open cones.
The midge {Phytophaga carpophaga Tripp)
causes the seed in which it develops to swell
more than normal and to remain wedged in
mature, open spruce cones (Tripp, 1955).
Insects that mine their way through several
seeds in a cone either pupate in one of the
galleries or drop to the ground and pupate
there (Keen, 1958). The larvae of the moth,
Dioryctria abietella (D 8c S), form pebble-
covered cocoons in the ground.
There'may also be predation between insect seed predators. In this case, however,
the advantage often goes to the first individual or species to attack the cone. As
many as seven chalcid eggs may be oviposited in one immature seed, but only one
pupa results, presumably^ because of cannibalism between larvae (Keen, 1958). It
seems probable that large larvae that mine
through several seeds could eat the smaller
larvae that develop in one seed. The seed
chalcid lays its eggs on ponderosa pine
cones shortly after the cones are pollinated.
Cone beetles do not attack the cone until a
1080
C. C. SMITH AND R. P. BALDA
year after it is pollinated, and yet they still a comparison between lodgepole pine,
kill the cone before it reaches maturity. which has only one or two predators attackThis would lead to the death of all the seed ing seeds in its cones, and the other species
chalcids that had been developing within of western North American conifers which
the cone.
havt many species attacking their cones.
A vertebrate that caches seeds must The key differences between lodgepole
either defend its caches or place them in pines and other conifers are that serotinous
such a way as to minimize the chance that races of lodgepole pines keep seeds in cones
other organisms will find and use them on the tree for many years as a mechanism
(Stapanian and Smith, 1978). Pine squirrels for reseeding after fires, and have nearly
make concentrated caches of cones which uniform annual seed crops. Lodgepole
they defend against all other organisms that pines provide a more predictable food recan tear open cones (Smith, 1968). Vander source than other conifers and allow their
Wall and Balda (personal observation) have seed predators to maintain a more constant
observed Clark's Nutcrackers stealing lim- population size (Smith, 1970). The coevoluber pine cones from squirrel caches, but tion of pine squirrels with lodgepole pines
that is only possible before the presence of has pushed the pines' defenses to the point
heavy snow cover. Tassel-eared squirrels do that only 2.0% of the weight of a cone is in
not make concentrated caches of pon- seeds, while four other species of conifers in
derosa pine cones, and this may be a con- the same Rocky Mountain region have
sequence of low snow cover and the pres- seeds forming from 7.4 to 25.9% of the
ence of Pirion Jays and Clark's Nutcrackers average cone weight (Smith, 1970). The
evolution of pine squirrels and lodgepole
throughout the squirrel's range.
The spacing of scattered caches by Pirion pine is at an equilibrium such that if pines
Jays and Clark's Nutcrackers is likely to be spent less energy on defense, the squirrels
based on the searching behavior of rodents would leave even fewer surviving seeds,
in much the same way as the spacing pat- and if the trees spent more on defense, they
tern of walnuts cached by fox squirrels (Sci- would produce fewer seeds. That equiliburus niger L.) (Stapanian and Smith, 1978). rium is at a situation where the cone is too
Unlike fox squirrels, the jays and some hard for any other mammal or bird to open,
groups of nutcrackers form and exploit or any insect to chew its way out to avoid
caches as a flock and do not have to space being trapped until the cone opened after
caches to avoid detection by members of the years of weathering.
same species (Balda and Bateman, 1972;
The nonserotinous races of lodgepole
Tomback, 1977; Vander Wall and Balda, pine found along the Pacific Coast and in
1977; Ligon, 1978). Mattes (1978) found the Cascade and Sierra Ranges have softer
that European Nutcrackers (Nucifraga cary- cones with more seeds per cone, and a
ocatactes L.) make caches in local habitats higher percent of the cone's energy is incontaining low rodent densities relative to vested in seeds than in the case of the
other nearby habitats. The spacing of scat- serotinous race (Critchfield, 1957; Elliott,
tered caches by deer mice, red-backed voles 1974). Keen (1958) reports that a species of
and chipmunks is likely to be dependent on cone beetle and two genera of cone moths
the searching behavior of conspecifics and do occasionally attack these nonserotinous
other small mammals.
races. There is some indication that the
There can be little doubt that there is nonserotinous races have a greater annual
severe competition of both an exploitive variation in the size of cone crops than does
and an interference nature during years of the serotinous race (Mowat, 1960).
poor cone crops, which brings us to quesThere appears to be a gradation in the
tions concerning the origin and mainte- strength of evolved structural defenses to
nance of the diversity of conifer seed- seed predators from a high in serotinous
eaters. The best clue to the factors allowing lodgepole pines through nonserotinous
the maintenance of a high diversity of lodgepole pines to a low in other conifers.
predators on one species of conifer seeds is The most effective structural defenses are
COMPETITION FOR CONIFER SEEDS
1081
found in the species with the least variable the resource are each controlled by a differannual cone crops. The variable cone crops, ent set of alternate resources or predators
in fact, reduce the strong selection experi- when the resource goes far below the level
enced by serotinous lodgepole pines for de- required by the various species exploiting
fenses that eliminate all but the most ef- it. The extrinsic causes of resource variaficient predator. The variability in cone tion differ between nutrients for the plankcrops allows many species to exploit the ton and seeds for seed predators, but the
larger cone crops at population densities situations are the same in that an extrinsic
well below carrying capacity for those factor creates the variation in the resource
crops.
rather than density-dependent feedback
The various groups of seed predators do between the resource and the exploiting
not competitively exclude each other be- populations. Nutrient upwelling to the
cause each population is controlled by a plankton has a strictly physical cause and
different set of environmental factors dur- the variation in cone crops is an evolved
ing the years of low cone crops. The verte- adaptation of the trees, but both occur inbrates, especially the smaller birds and dependent of feedback from existing popumammals, have evolved different methods lations of exploiting species.
of foraging for conifer seeds and cones that
Radically different alternate foods, forrelate to different means of using alternate aging techniques and predators are very
foods. The insect groups overlap more than important in allowing the maintenance of a
the vertebrates in their means of escaping high species diversity within a community
poor cone crops, especially in their use that exploits an intrinsically variable reof variable diapause. The diversity of in- source. This situation is clearly demonsect seed predators, however, seems to be strated by the high diversity of distantly
matched by the diversity of species of para- related taxa but the low diversity of closely
sitic wasps that prey upon them (Keen, ralated taxa that exploit conifer seeds. Only
1958). Since the wasps face approximately shrews and deer mice among the mammals
the same problems in finding their prey as and crossbills, woodpeckers and Parids
the insect seed predators face in finding among the birds have two or more species
their food (a cone of a particular species that are sympatric within a habitat (Hall
and stage of development), the number of and Kelson, 1959; Austin, 1968; Smith,
unique ways that the two groups can exploit 1968; Brown, 1971; Heller, 1971; Shep. their resources may be very similar. The pard, 1971). Even the crossbills are separesult of the similarity would be that each rated in western North America, and the
species of insect seed predator would have shrews, woodpeckers and Parids are priits population density controlled by a dif- marily adapted to a less variable diet of
ferent group of parasitic wasps which used insects. Species of Peromyscus separate bea set of clues and adaptations for finding tween ground and arboreal foraging where
and exploiting its food that were similar to two species are sympatric. Each of the
those used by its prey. The high degree of species within the insect genera Conophsimilarity in the attack of insect seed preda- thorus, Megastigmus, Barbara, Eucosma and
tors and their parasites is demonstrated by Laspeyresia is adapted to exploit a different
some species of seed chalcids (Megastigmus) taxonomic group of conifers.
which can be either seed predators or paraOne might expect a relatively stable resites of seed predators (Milliron, 1949).
source to be divided between congeneric
The overall picture of the origin of spe- species on the basis of constant differences
cies diversity in seed predators parallels in size or spatial distribution within the reHutchinson's (1961) analysis of the mainte- source (MacArthur, 1958; Schoener, 1965,
nance of diversity in plankton. Some agent 1974; Rosenzweig, 1966). The territorial
creates so much variation in a basic resource system that pine squirrels use to cache the
that none of the species populations that stable serotinous lodgepole pine crops,
can exploit the resource ever come to an however, precludes an efficient division of
equilibrium density. The species exploiting their niche (Smith, 1968).
1082
C. C. SMITH AND R. P. BALDA
musculature in Clark's Nutcracker. Auk 90:491519.
The maintenance of many distantly re- Bormann, F. H. 1966. The structure, function and
f colijical significance of root grafts in Pinus strolated taxa exploiting the distinctive and easbvs L. Ecol. Monogr. 36:1-26.
ily delimited resource of conifer seeds is the B roadbooks,
H. E. 1958. Life history and ecology of
result of large, intrinsic variation in the rethe ,:hipmunk, Eutamias amoenus, in eastern Washsource. Although there may be severe comington. Misc. Pub. Mus. Zool., Univ. Michigan
103:5-42.
petition of both an exploitive and an interference nature when resources are low, the Brown, J. H. 1971. Mechanisms of competitive exclusion between two species of chipmunks. Ecology
various species using the resource avoid
52:305-311.
competitive exclusion in that each is limited Critchfield, W. B. 1957. Geographic variation in Pinus
by a different predator population or altercontorta. Maria Moors Cabot Foundation Pub. no.
3:1-118.
nate resource when the conifer seed crop is
low. The greater the ecological and taxo- Davis, J. and L. Williams. 1964. The 1961 irruption of
the Clark's Nutcracker in California. Wilson Bull.
nomic differences in the species exploiting
76:10-18.
the variable conifer seed crops, the greater Dow, D. D. 1965. The role of saliva in food storage by
the probability that they will be limited by
the Gray Jay. Auk 82:139-154.
different predators or alternate resources. Eis, S., E. H. Carman, and L. F. Ebell. 1965. Relation
between cone production and diameter increment
of Douglas-fir (Pseudolsuga menziesii (Mirb.) Franco),
grand fir (Abies grandis (Doug.) Lindl.), and western
REFERENCES
white pine (Pinus monticola Dougl.). Can. J. Bot.
43:1553-1559.
Abbott, H. G. and T. F. Quink. 1970. Ecology of east- Elliott, P. F. 1974. Evolutionary response of plants to
ern white pine seed caches made by small forest
seed-eaters: Pine squirrel predation on lodgepole
mammals. Ecology 51:271-278.
pine. Evolution 28:221-231.
Aldous, S. E. 1941. Food habits of chipmunks. J. Farentinos, R. C. 1972. Social dominance and mating
Mamm. 22:18-24.
activity in the tassel-eared squirrel (Sciurus abertiferAllen, G. S. and J. N. Owens. 1972. The life history of
reus). Anim. Behav. 20:316-326.
Douglas-fir. Information Canada, Ottawa.
Fowells, H. A. (ed.) 1965. Silvics of forest trees of the
Anderson, S. H. 1976. Comparative food habits of
United States. Agr. Han'db. No. 271:1-762.
Oregon nuthatches. Northwest Science 50:213-221. Franklin, J. F. 1964. Ecology and silviculture of the
Austin, O. L., Jr. (ed.) 1968. Life histories of North
fir-hemlock forests of the Pacific Northwest. Proc.
American cardinals, grosbeaks, buntings, towhees,
Soc. Amer. Foresters 1964:28-32.
finches, sparrows and allies. U. S. Nat. Mus. Bull. Garman, E. H. 1951. Seed production by conifers in
237:1-602.
the coastal region of British Columbia related to
Baker, H. G. 1972. Seed weight in relation to environdissemination and regeneration. British Columbia
mental conditions in California. Ecology 53:997For. Serv., Tech. Pub. No. T35:1-47.
1010.
Garman, E. H. 1955. Regeneration problems and their
Balda, R. P. 1979. Are seed caching systems cosilvicultural significance in the coastal forests of
evolved? Proc. XVII Internat. Ornith. Congress. (In
British Columbia. British Columbia For. Serv.,
press)
Tech. Pub. No. T41:l-67.
Balda, R. P. and G. C. Bateman. 1971. Flocking and Gashwiler, J. S. 1959. Small mammal study in westannual cycle of the Pinon Jay, Gymnorhinus cyano- central Oregon. J. Mamm. 40:128-139.
cephalus. Condor 73:287-302.
Gilbert, B. L., S. J. Barras, and D. M. Morris. 1967.
Balda, R. P. and G. C. Bateman. 1972. The breeding
Bionomics of Tetyra bipunctata (Hemiptera: Penbiology of the Pinon Jay. Living Bird 11:5-42.
tatomidae: Scutellerinae) as associated with Pinus
Balda, R. P., G. C. Bateman, and G. F. Foster. 1972.
banksiana in Wisconsin. Ann. Entomol. Soc. Am.
Flocking associates of the Pinon Jay. Wilson Bull.
60:698-701.
84:60-76.
Golightly, R. T., Jr. and R. D. Ohmart. 1978. HeteroBateman, G. C. and R. P. Balda. 1973. Growth, develthermy in free-ranging Abert's squirrels (Sciurus
opment and food habits of young Pinon Jays. Auk
aberti). Ecology 59:897-909.
90:39-61.
Haftorn, S. 1974. Storage of surplus food by the
Beal, F. E. L. 1911. Food of the woodpeckers of the
Boreal Chickadee Parus hudsonicus in Alaska with
United States. U. S. Dept. Agr. Biol. Surv. Bull.
some records on the Mountain Chickadee Parus
37:1-64.
gambeli in Colorado. Ornis. Scand. 5:145-161.
Birch, L. C. 1957. The meaning of competition. Amer. Hall, E. R. and K. R. Kelson. 1959. The mammals of
Natur. 91:5-18.
North America. Ronald Press, New York.
Bock, C. E. and L. W. Lepthien. 1976. Synchronous Hamilton, W. J., Jr. 1941. The food of small forest
eruptions of boreal seed-eating birds. Amer. Natur.
mammals in eastern United States. J. Mamm. 22:
110:559-571.
250-263.
Bock, W. J., R. P. Balda, and S. B. Vander Wall. 1973. Heller, H. C. 1971. Altitudinal zonation of chipmunks
Morphology of the sublingual pouch and tongue
(Eutamias): Interspecific aggression. Ecology 52:
CONCLUSIONS
COMPETITION FOR CONIFER SEEDS
1083
312-319.
bles: A note on the American Red Crossbill. Auk
49:159-165.
Hutchinson, G. E. 1961. The paradox of the plankton.
Amer. Natur. 95:137-145.
Rosenzweig, M. L. 1966. Community structure in
Janzen, D. H. 1971. Seed predation by animals. Ann.
sympatricCarnivora.J. Mamm. 47:602-612.
Rev. Ecol. and Syst. 2:465-492.
Rusch, D. A. and W. G. Reeder. 1978. Population
ecology of Alberta red squirrels. Ecology 59:400Keen, F. P. 1958. Cone and seed insects of western
forest trees. U. S. Dept. Agr. Tech. Bull. no. 1169:
420.
1-168.
Ruth, R. H. and C M . Berntsen. 1955. A 4-year record
of Sitka spruce and western hemlock seed fall. U. S.
Keith, J. O. 1965. The Abert squirrel and its dependence on ponderosa pine. Ecology 46:150-163.
D. A. For. Serv. Pacific NW For. and Range Expt.
Kilham, L. 1974. Covering of stores by White-breasted
Sta., Res. Paper No. 12:1-13.
and Red-breasted Nuthatches. Condor 76:108-109. Schoener, T. W. 1965. The evolution of bill size differKoerber, T. W. 1963. Leptoglossus occidentals (Hemip- ences among sympatric congeneric species of birds.
tera, Coreidae), a newly discovered pest of coniferEvolution 19:189-213.
ous seed. Ann. Entomol. Soc. Amer. 56:229-234.
Schoener, T. W. 1974. Resource partitioning in ecological communities. Science 185:27-39.
Krugman, S. L. and T. W. Koerber. 1969. Effects of
cone feeding by Leptoglossus occidentalis on pon-Schubert, G. H. and R. S. Adams. 1971. Reforestation
derosa pine seed development. Forest Sci. 15:104practices for conifers in California. California Dept.
111.
Conservation, Div. Forestry, Sacramento.
Larson, M. M. and G. H. Schubert. 1970. Cone crops Sheppard, D. H. 1971. Competition between two
of ponderosa pine in central Arizona, including the
chipmunk species (Eutamias). Ecology 52:320-329.
influence of Abert squirrels. U. S. D. A. Forest Ser- Smith, C. C. 1968. The adaptive nature of social orvice Research Paper RM-58.
ganization in the genus of tree squirrels TamiasLigon.J. D. 1971. Late summer-autumnal breeding of
ciurus. Ecol. Monogr. 38:31-63.
the Pinonjay in New Mexico. Condor 73.147-153.
Smith, C. C. 1970. The coevolution of pine squirrels
Ligon, J. D. 1973. Foraging behavior of the White(Tamiasciurus) and conifers. Ecol. Monogr. 40:349headed Woodpeckers in Idaho. Auk 90:862-869.
371.
Ligon, J. D. 1974. Green cones of the pinon pine Smith, C. C. 1975. The coevolution of seeds and seed
stimulate late summer breeding in the Pinon Jay.
predators. In I.. E. Gilbert and P. H. Raven (eds.),
Nature 250:80-82.
Coevolution of animals and plants, pp. 53-77. Univ.
Texas Press, Au? in.
Ligon, J. D. 1978. Reproductive interdependence of
Pinon Jays and pinon pine Ecol. Monogr. 48:111
Smith, C. C. and j . D. Fretwell. 1974. The optimal
balance between size and number of offspring.
126.
Amer. Natur. 108:499-506.
Ligon, J. D. and D. J. Martin. 1974. Pinon seed assessment by the Pinonjay. Anim. Behav. 22:421-429.
Stallcup, P. L. 1968. Spatio-temporal relationships of
nuthatches and woodpeckers in ponderosa pine
Lowry, W. P. 1966. Apparent meteorological reforests of Colorado. Ecology 49:831-843.
quirements for abundant cone crop in Douglas-fir.
For. Sci. 12:185-192.
Stallcup, P. L. 1969. Hairy Woodpeckers feeding on
MacArthur, R. H. 1958. Population ecology of some
pine seeds. Auk 86:134-135.
warblers of northeastern conifer forests. Ecology Stapanian, M. A. and C. C. Smith. 1978. A model for
39:599-619.
seed scatterhoarding: Coevolution of fox squirrels
Martin, A. C, H. S. Zim, and A. L. Nelson. 1951.
and black walnuts. Ecology 59:884-896.
American wildlife and plants, a guide to wildlife food Tevis, L. 1953. Effects of vertebrate animals on seed
habits. McGraw-Hill Book Co., New York.
crop of sugar pine. J. Wildl. Mgmt. 17:128-131.
Mattes, H. 1978. Okologische studien Ciber den Tan- Tomback, D. F. 1977. Foraging strategies of Clark's
nenhaher (Nucifraga caryocatactes) im Engadin und Nutcrackers. The Living Bird 16:123-161.
seine Bedeutung fur die verjiingung der Arve Tordoff, H. B. and W. R. Dawson. 1965. The influence
(Pinus cembra). Ph.D. Diss. Universitat Miinster.
of daylength on reproductive timing in the Red
Crossbill. Condor 67:416-422.
McKeever, S. 1964. The biology of the goldenmantled ground squirrel, Citellus lateralis. Ecol. Tripp, H. A. 1955. Descriptions and habits of CecidoMonogr. 34:383-401.
myiidae (Diptera) from white spruce cones. Can.
Mewaldt, L. R. 1956. Nesting behavior of the Clark's
Entomol. 87:253-263.
Nutcracker. Condor 58:3-23.
U.S.D.A. 1974. Seeds of woody plants in the United Stales.
Milliron, H. E. 1949. Taxonomic and biological invesU. S. D. A. For. Serv. Agric. Handbook 450.
tigations in the genus Megastigmus. Amer. Midi. Vander Wall, S. B. and R. P. Balda. 1977. CoadaptaNatur. 41:257-420.
tions of the Clark's Nutcracker and the pinon pine
for efficient seed harvest and dispersal. Ecol. MonoMoore, A. W. 1942. Shrews as a check on Douglas fir
gr. 47:89-111.
reproduction. J. Mamm. 23:37-41.
Mowat, E. L. 1960. No serotinous cones on central Vorhies, C. T. 1934. Arizona records of the thickOregon lodgepole pine. J. Forestry 58:118-119.
billed parrot. Condor 36:180-181.
Norris, R. A. 1958. Comparative biosystematics and Westcott, P. W. 1964. Invasion of Clark Nutcrackers
life history of the nuthatches Sitta pygmaea and Sitta and Pinon Jays into southeastern Arizona. Condor
pusilla. Univ. Cal. Publ. Zool. 56:119-300.
66:441.
Ritter, R. J. 1969. A contribution to the biology of the Wetmore, A. 1935. The thick-billed parrot in southern
Arizona. Condor 37:18-21.
Gray Jay. Canad. Field-Natur. 83:300-316.
Robbins, C. A. 1932. The advantage of crossed mandi-