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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. 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