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Riolo~ical.Journal a/ l/w Linnenn So&& (1989), 36: 227--249. With 4 figures The tortoise and the hare: ecology of angiosperm dominance and gymnosperm persistence W. J. BOND* Deparlmenl of Biology, Uniuersig of Culzfornin, 1.0s Angeles CA90024, U.S.A. Krceiued 15 SrplemhPr 1988. nrrrpled Jbr puhlzcativtr 6 April I988 Gymnospernis, and conifers in particular, are somctimes vrry productive trees yrt angiosperms dominate most temperate arid tropical vegcAtation. Current explanatioirs for angiosperm success crnphasize the ad\aiitages of insect pollination and seed dispersal by animals for the colonization of isolatccl habitats. DifTcren(.es hctwern gymnospcrm and angiosperm 1-cproductive and vegctativr growth ratcs have bern largely igniircd. Gymnosperms arc all woody, perennial a nd usually have long reproductive cycles. 'l'hcir leavrs arc i i ~ as t fully vascularized as those of angiosperms arid are more stereotyped in shapc and size. Gymnosperm trachcids are gc-ncIally more rcsistant to solute flow than angiosperm vessels. A consequence o f t h e lc-ss eflicicnt transport system is that maximum growth rates of gymnosperms are lower than maximum growth rates of angiosperms i i i well lit, well watered hahitats. Gymnosperm sccdlings may hc particularly uiicompctitive sincc their growth depends on a single cohort of relatively inefficient leaves. Later, some gymnosperms attain a higher productivity than co-occurring aiigiosprrm trees b y accumulating sc-veral cohorts oflcavcs with a higher total leaf arm 'l'ticsc functional constraints o n gymnosperm growth rates suggest that gymnosperms will be restricted to areas wherr growth of angiosperm competitors is reduced, for example, by cold or nu trierit shortages. Biogeographic evidence supports this prediction since conifers are largely confined to high latitudes arid elevations or nutrient-poor soils. Experimental studies show that competition in the regeneration niche (between conifcr seedlings and angiosperm herbs and shrubs) is conimon and significantly allrrts conifer growth and survival. Fast-growing angiosperms, especially herbs and shrubs, may also change the frcquency of disturhancc regimes thereby excluding slower-growing gymnosperms. Shade-tolerant arid early su( .ioiial conifers sharc similar c1iarartrristic.s of slow initial growth aiid tow plasticity t o ;I chaiigr in rcsources. Shade-tolerant gymnosperms would he cxpected to occur only where forest opcnings are small or otherwise urisuitablc for rapid filling by fast-growing angiospcrm trees, lianas o r shrubs. 'I'he limited evidence availahlr suggests that shade-tolerant conifers a r c confined to forests with small gap sizes where large disturbances are very rare. ' I h e regeneration hypothesis for gymnosperm exclusion by angiosperms is consistent with several aspects of the fossil record such as the early disappearance of gymnosperms from early successional mvironnients wherc competition with angiosperms would have heen most scvcre. However there are unresolved dilficulties in intrrprrting process from paleoecological pattern which prevent the testing of alternative hypotheses. KEY WOKDS: ~Angiospcrnievolution ~ gymnosperm evolution - conifcr hiogrography ~ plant conipeti tion. CON'I'EN'I'S Introduction . . . . . , . , . . Characteristics ofangioslicrms versus gymnosperms , Reproductivc ratcs . . . , . , , , , , , , , . . , , . . , . . . . . . . , . . . . 228 . . 232 232 * Present Addrcss: Department of Botany, University of Cape 'l'own, Private Bag, Rondehosch 7700, South Africa. 0024-4066/89/030227 + 23 $03.00/0 227 0 1989 T h e Linnean Society of London W. J. BOND 230 TABLE 1. Net production of angiosperm and gymnosperm forest types measured in the same vicinity (within a radius of a few km). N = Number of stands Forest type Japan (Satoo & Madgwick, 1982) Angiosperm Batula maximowiziana Populus dauidiana Gymnosperm Picea abies Abies Jachalinensis Larix leptolepis Germany (Schulze et al., 1977) Angiosperm Fagus syluatica Gymnospcrm Picea abies N Age Net production (yrs) (ton ha-’ yr I) 3 1 47 40 4.2-6.2 8.7 4 1 1 45-47 26 21 1 120 4.2 1 89 8.4 7.3-12.4 13.0 16.5 American deserts, may dominate diverse geographic areas alongside large genera with many species (e.g. Ceanothus, Arctostaphylos, Opuntia). I n this paper I am concerned only with those features of angiosperms which led to their ecological ascendance, in some habitats, over gymnosperms. The measure of success is relative cover or biomass, rather than number of species. Most recent authors have explained angiosperm advances in the past and the restricted distribution of conifers in the present on the basis of differences in pollination and dispersal potential (Crepet, 1984; Tiffney, 1984; Burger, 1981; Regal, 1977). Many angiosperms are insect-pollinated while nearly all gymnosperms are wind-pollinated. The competitive advantages of insect pollination are said to be: (1) reliable directional pollination which costs less energy, (2) production of outcrossed offspring in sparse populations and (3) successful pollination where wind is ineffective (Crepet, 1984). Insect pollination is thought to be particularly advantageous in sparse populations as insects may carry pollen greater distances more effectively than wind (Whitehead, 1969; 1983; Burger, 1981; Regal, 1977, 1982). Thus insect-pollinated (and animaldispersed) angiosperms ought to be able to maintain gene flow over a wider range of population sizes and structures than wind-pollinated (and winddispersed) conifers. Proponents of the pollination hypothesis explain the widespread persistence of gymnosperms as dominant components of contemporary vegetation by linking site to species diversity. Conifers persist where they do, it is argued, only in dense monospecific stands where wind pollination is as effective as insect pollination. Monospecific stands or low diversity communities, in turn, are caused by ‘stressed’ (cold, nutrient-poor) habitats (Regal, 1977; P. Raven, 1977; Whitehead, 1969). There are several difficulties with this hypothesis. First there is no empirical base for the generalization that gene flow between populations is greater in insect than in wind-pollinated species. Studies of intrapopulation gene flow are common but there are very few studies of gene flow between populations. Ellstrand & Marshall (1985) could find only three, excluding their own, and caution that generalizations on “the importance of gene flow as a cohesive evolutionary force” ANGIOSPERM DOMINANCE AND GYMNOSPERM PERSISTENCE 23 1 between populations cannot be made at present given this limited empirical base. Conifers, like most trees, are usually highly heterozygous (Brown, 1979; Hamrick, Linhart & Mitton, 1979) regardless of whether species ranges are continuous or divided into isolated ‘islands’ (Hiebert & Hamrick, 1983). At first sight this may seem to negate the hypothesis that wind pollination reduces outcrossing. However it can be counter-argued that natural conifer populations are already sufficiently dense to allow adequate gene flow. The only way of studying the hypothesized limitations of wind pollination is by explicitly searching for density dependent effects on gene flow. Some conifers do show density dependent changes in outcrossing rates and greater survivorship of heterozygous seedlings (e.g. Farris & Mitton, 1984), but no studies directly compare the effects of density on heterozygosity in both insect and wind-pollinated species. Nor would it be easy to devise a test which isolated pollination mode from other ecological factors which determine genetic structure (Loveless & Hamrick, 1984). A few conifers are homozygous or nearly so, including both narrow endemics (Pinus torreyana Parry ex Carr) and widespread species (Pinus resinosa Ait., Thujaplicata Donn ex D.Don). Thus some conifers can survive and even thrive despite inbreeding and low genetic variability (Ledig & Conkle, 1983). Even if insect pollination could be shown to maintain greater genetic variation at low densities, it does not follow that heterozygosity necessarily influences survival and distribution of a species as opposed to fitness of genotypes within a species. Biogeographers generally interpret vegetation patterns on the basis of differences in growth rates, deciduosity, rooting patterns, dispersal abilities, longevity, shade tolerance etc. (e.g. Daubenmire, 1978). Relative heterozygosity of competing species has seldom (ever?) been identified as an important factor. While there may, ultimately, be a link between pollination mode, population structure and genetic variation, and even between heterozygosity and ecological dominance, it seems reasonable to look for other more direct causes of conifer distributional limits. Here I argue that the competitive ability of gymnosperms is limited by rates of both vegetative and reproductive processes rather than by access to or selection of mates. The angiosperm innovation of the herbaceous habit (rapid foliage production, minimal expenditure on woody support, short reproductive cycles) allows far more effective exploitation of ephemeral habitats than the woody habit of all gymnosperms. Angiosperms disperse as seeds rather than spores and so escape the ecological constraints of the free-living gametophyte stage of their herbaceous precursors, the homosporous ferns. Angiosperm herbs and shrubs compete directly with gymnosperms regenerating in forest gaps. Although gymnosperm (especially confer) productivity can be very high, the photosynthetic capacity of individual leaves is low. The high productivity of some taxa is due, in part, to a large leaf area resulting from the accumulation of cohorts of leaves over a number of years (Waring & Franklin, 1979; Chabot & Hicks, 1982; Schulze et al., 1986). However the seedlings of conifers possess only a single cohort of leaves with which to compete with angiosperms in the early stages of the life of the tree. I argue that, because of these ontogenetic constraints, conifers are restricted to sites or successional stages which lack intense competition in the regeneration phase. I call this the ‘slow seedling’ hypothesis. The historical implications of the hypothesis are that the Cretaceous and Tertiary retreat of the gymnosperms was caused by the invasion of angiosperms into the gymnosperm regeneration niche. 232 W. J. BOND I first discuss the functional significance of apomorphic features of angiosperms, especially those which influence vegetative growth. I then relate the functional characteristics of modern angiosperms and gymnosperms to the niches they occupy and thus to their biogeography. Finally I discuss whether the “slow seedling” hypothesis is at all compatible with the fossil record of angiosperm advances and gymnosperm declines and what alternative hypotheses successfully explain modern gymnosperm distributions. My argument centres on conifers both because they are by far the most successful modern gymnosperms and because they are the most studied. For the same reasons my discussion centres on conifers with gap-phase regeneration though I briefly consider the ecological implications of the same functional constraints for shade-tolerant gymnosperms. CHARACTERISTICS OF ANGIOSPERMS VERSUS GYMNOSPERMS Reproductive rates Among the seed plants, the potential for prolific reproduction and rapid colonization are pre-eminent angiosperm traits. Many of the reproductive apomorphies which distinguish angiosperms from gymnosperms are associated with a reduction in the costs of reproduction and an increase in the reproductive rate (reviewed by Stebbins, 1974, 1976). The style, for example, facilitates the growth of the pollen-tube while a t the same time selectively filtering pollen parents (Stebbins, 1976; Mulcahy, 1979). The annual herb epitomizes the angiospermous traits of rapid growth and short generation times; some desert annuals complete their entire life cycle in less than a month (Went, 1948). Most angiosperms produce mature seed within a few weeks or months after flowering, though some woody trees take a year or more, for example Quercus spp., Eucahptus regnans (Willson & Burley, 1983; Ashton, 1975). In contrast, most gymnosperms have long reproductive cycles. The period from pollination to fertilization usually exceeds 12 months (Stebbins, 1976; Willson & Burley, 1983). All gymnosperms are perennial and all are woody trees, shrubs or (rarely) vines. Perenniality and woodiness is related to the slower rates and greater costs of reproduction but also to the limitations of the vegetative body (Stebbins, 1976). Vegetative growth rates T h e leaf The vegetative attributes of angiosperms include the capacity for very rapid growth which in turn is associated with a remarkable diversity of foliage form and function. The functional basis for rapid growth lies partly in the evolution of new features related to the conducting system (Carlquist, 1975; see Niklas, 1985; J.A.Raven, 1977 for the importance of the conducting system in early tracheophyte evloution) . The earliest evidence, other than pollen, for angiosperm divergence is the appearance of fossil leaves with complex, branching veins (Doyle & Hickey, 1976; Hickey & Doyle, 1977). Angiosperm, and especially dicot, leaf venation is distinctly different from conifers in the degree of vascularization with anastomosing (closed) systems of veins and a dense network of minor veins ending blindly in small partitions of the leaf (Foster & Gifford, 1974; Esau, 1965). Veins ANGIOSPERM DOMINANCE AND GYMNOSPERM PERSISTENCE 233 increase the rate of solute flow through the leaf by several orders or magnitude relative to an equivalent cross-sectional area of cell wall (Jones, 1983: 74). The enormous conductive capacity of the leaf has been experimentally demonstrated by severing major veins and observing subsequent tissue death in a number of dicot leaves (Fig. 2) (Wylie, 1938; Plymale & Wylie, 1944). Gymnosperm leaves lack the network of anastomosing major and minor veins and presumably, therefore, have lower rates of solute transport than angiosperms*. No comparative physiological work appears to have been done on the topic. The major veins are structurally important in supporting the broad, but very thin, leaf lamina. Givnish (1979) discussed mechanical aspects of leaf venation emphasizing the cost of a vein versus its support function. Thick sclerophyll leaves have few or disorganized veins per unit area since the thickened cell walls are self-supporting. However sclerophylly also enables leaves to resist collapse under highly negative water potentials where an efficient conducting system would be superfluous (Mooney & Dunn, 1970). The slender evidence available thus suggests that the leaf venation of angiosperms makes possible rapid growth and expansion of leaves through efficient supply of water. In addition the support provided by the organized system of major veins permits a much greater diversity of leaf shapes and sizes and greater leaf area per unit carbon expended than those seen in gymnosperms (Doyle & Hickey, 1976). Leaf size, shape and texture in gymnosperms, in contrast, reflect the inability of the transport system to supply rapidly expanding photosynthetic tissue. None of the extant Coniferales, Ginkgoales, Gnetales or Taxales have compound leaves which, in angiosperms, can act as ‘throwaway’ branches for exploiting light gaps in productive environments (Givnish, 1978). T h e only extant gymnosperms with compound leaves, the cycads, have leaves that are slow growing, long-lived and sclerophyllous (Chamberlain, 1934). Conifer leaves are nearly all linear, needle or scale-like so that extension of canopy volume depends on the growth of new shoots rather than deployment of leaves. Conifers with broad leaves (e.g. some species of Agathis, Araucaria, Podocnrpus) are no exception since their leaves are sclerophyllous and long lived. The remarkable survival of Ginkgo, almost unchanged since its origins in the Triassic, seems to have been unexploited by comparative ecophysiologists. Ginkgo has broad deciduous leaves but non-reticulate venation. One would therefore predict slower rates of initial leaf expansion and subsequent solute transport than deciduous broad-leaved angiosperms. This, coupled with its architecture of branches with short shoots, would result in a slow pace of change in Ginkgo canopy geometry which would place it at a competitive disadvantage in broad-leaved angiosperm forests. Gnetum is the single gymnosperm exception with broad leaves and anastomosing veins indistinguishable from a dicot leaf. T h e genus, which has efficient angiosperm-like conducting vessels (Chamberlain, 1934), is also exceptional in including the only gymnosperm lianas and is perhaps the only gymnosperm group which thrives in angiosperm-dominated lowland tropical rainforest (e.g. Gnetum gnetoides). Recent cladistic analysis suggests that the Gnetales are a sister group of * Several Mesozoic gymnosperms, such as the Caytoniaceae (Sqenopleris) and some cycadophytes, show a single order of reticular venation in the leaves. For this reason some have been suggested as angiosperm precursors (Hickey & Doyle, 1977; Doyle, 1977). W. J. BOND 234 A C B D Figure 2. The effects of restricted conduction on deciduous angiosperm leaves (redrawn from Plymale & Wylie, 1944). Dotted lines indicate experimental cuts through the blade. Stippled areas are portions of dead lamina. A, Liriodendron tulipifera; B, Quercus velutina; C , Cercis canadensis; D, Quercus macrocarpa. the angiosperms (Doyle & Donoghue, 1986) and evolved in parallel with (but were never as widespread as) the angiosperms (Upchurch & Crane, 1985). The stem Rapid vegetative growth depends, in part, on the rate of supply of water to leaves and meristems (Waring, 1983). Xylem is specialized into separate support and conductive tissues in angiosperms whereas gymnosperm tracheids serve both functions. The water conducting unit in almost all angiosperms is the vessel whereas the tracheid serves this function in almost all gymnosperms and ferns. Vessels offer less resistance to water flow than tracheids because they lack end walls and are much larger (Carlquist, 1975). T h e lumen diameter of vessels usually exceeds that of tracheids. T h e lumen diameter of conifers seldom exceeds 30-50 microns in diameter whereas diffuse-porous vessels of angiosperms approach 100-200 microns and ring-porous vessels may be as large as 500 microns ANGIOSPERM DOMINANCE AND GYMNOSPERM PERSISTENCE 235 (Zimmermann & Brown, 197 1; Carlquist, 1975). Conductivity is determined by lumen diameter, total conducting area and resistance of the conducting elements to water transport. The significance of the first two can be assessed by the HagenPoiseuille equation. If conducting elements are equivalent to cylindrically shaped capillaries then the rate of flow over a cross section of stem, J, is given by J = (xdi2/8n).(dP/dL) where di is the diameter of vessel i, n is the viscosity of water and dP/dL is the pressure potential gradient (Zimmermann & Brown, 1971; Zimmermann, 1983; Nobel, 1983; Gibson, Calkin & Nobel, 1984). The rate of flow is proportional to the vessel diameter squared so that, for an identical cross-sectional area, a 10-fold increase of vessel diameter (e.g. 10 microns to 100 microns) would increase flow rate 100-fold. The equation also shows that large diameter vessels in a stem will transport most of the water. For example, under the same pressure gradient, a 200 micron diameter vessel adjacent to a 50 micron vessel would carry 94% of the total volume transported through both vessels (Zimmermann, 1978). Wood cells are not ideal capillaries but several studies have shown that the Hagen-Poiseuille equation is a reasonable approximation of relative water flow (Zimmermann & Brown, 1971: 199; Gibson et al., 1984). Discrepancies between predicted and observed hydraulic conductance have been attributed to resistance of the conducting elements. The main components of this resistance in fern tracheids are aperture shape, length of the tapered section and pit membranes all of which vary in relative importance depending on the diameter of the tracheids (Calkin, Gibson & Nobel, 1986). Comparative studies of this nature on gymnosperm and angiosperm conducting elements are needed for determining the hydraulic significance of differences in vascular anatomy. The maximum vessel diameter is constrained by a trade-off between efficiency and safety since a more efficient conducting capacity involves greater risk of accidental embolism (Zimmermann, 1971, 1978; Carlquist, 1985). Not all trees have very large vessels because the failure of a large vessel by accidental embolism would cut off a proportionally very large fraction of the water supply. I n general, therefore, trees with safer, narrower vessels occur in water stressed areas or are evergreens which suffer severe seasonal moisture stress. Large diameter vessels typically occur either in deciduous species which replace the embolized conducting system annually before the flush of new leaves or in evergreen species in non-seasonal humid areas which seldom experience moisture stress (Rury & Dickison, 1984; Zimmermann, 1978, 1983; Carlquist, 1975). I n summary, conifer conducting systems both in the leaf and the wood are less efficient than those of angiosperms. The large vessels and heavily vascularized leaf of angiosperms together allow rapid transpiration and much faster growth of leafy canopies but only where there is no shortage ofwater or the necessary nutrients for production of new leaves. If water is seasonally deficient, temperatures freezing or nutrients limiting, then the gymnospermous combination of narrow tracheids or stress-tolerant, weakly vascularized evergreen leaves is a much safer alternative. Photosynthesis and productivity Conifers, because of the limitations of their transport system, should have lower rates of maximum dry matter production than herbaceous or deciduous W. J. BOND 236 TABLE2. Maximum mean values for relative growth rates of angiosperm herbs and tree seedlings versus conifer seedlings (ex Jarvis & Jarvis, 1964). RGR = relative growth rate = (lnW2 -InWl)/t, where Wi = dry weight at time i, t = time interval RGR Growth form Herb Helianlhus annuus Deciduous broad-leaf Betula verrucosa Pofiulus lremula Conifer Pinus Vlvestris Picea abies (mg g- I) As yo of Helianthus 980 100 513 502 52 51 81 34 8 3 angiosperms under non-limited growing conditions. When measured over short periods, herbaceous angiosperms do have a much higher relative growth rate than either woody angiosperms or gymnosperms (Table 2) (Jarvis & Jarvis, 1964; Grime & Hunt, 1975; Whitmore & Wooi-Khoon, 1983). Conifer seedlings, in turn, have lower relative growth rates than deciduous woody angiosperm seedlings (Jarvis & Jarvis, 1964; Pollard & Wareing, 1968; Whitmore & WooiKhoon, 1983; Krueger & Ruth 1969). These differences in productivity (annual increment of dry matter) can be attributed to differences in four growth parameters: the net photosynthetic rate (Ps), the total area of leaf exposed per unit ground area (LAI, leaf area index), the duration of the leaf crop (LD), and the allocation of photosynthate to leaves or non-photosynthetic tissue (Mooney & Gulmon, 1983j . Much photosynthetic research has focused on Ps. Photosynthetic capacity is generally reported as being lower in conifers than in herbs or broad-leaved trees (90.8-136.2pmol CO,m-*s-' in conifers versus 227-3 17.8 pmol CO,m-'s-' in broad-leaved trees (Larcher, 1980; but see Nelson, 1984 for a dissenting view). However there is no simple relationship between productivity and assimilation rate because the annual rate of carbon gain is a product not only of Ps but also of LA1 and LD. Schulze et al. (1977) made a detailed comparison of Picea abies and Fagus syluatica. Photosynthetic rates were two to four times higher in the leaves of the deciduous Fagus, but Picea, an evergreen, had four or more cohorts of leaves present simultaneously and had a longer growing season. The net result was that Picea stands yielded 14.9 tons C ha-' as opposed to 8.6 for Fagus in an average year. Thus although there is a lower carbon gain per unit leaf mass in the conifer, Picea exceeded the broad-leaved tree in annual carbon gain because the conifer photosynthesized for a longer growing season with a much greater total leaf biomass. Defoliation experiments have confirmed the importance of older cohorts of leaves in evergreen conifers. For example, growth of Pinus radiata saplings was reduced by 51% after removal of 1-2 year old leaves (Rook & Whyte, 1976). Because productivity of evergreen conifers depends on their accumulating a large leaf biomass by adding successive cohorts of leaves, young conifer stands should take longer to reach maximal leaf areas than broad-leaved stands. ANGIOSPERM DOMINANCE AND GYMNOSPERM PERSISTENCE 237 Time Figure 3. Hypothetical growth rate of evergreen (EG) versus deciduous (DD) trees. The two growth forms reverse productivity from juvenile to mature life stages. B = Growth index, e.g. biomass, height. Available evidence suggests this is the case. The maximum leaf area in deciduous forests of the eastern United States is re-established within five years after disturbance while Scottish plantations of Picea sitchenis take 16 years, Swedish plantations of Pinus syluestris take 25 and the leaf area index of newly established conifer stands in the Pacific Northwest continues to rise for 40 years or more Uarvis & Leverenz, 1982: 250). Consequently in the early growth stages juvenile conifers will have less foliage and less carbon income than angiosperm competitors to allocate to shoot growth, root growth and anti-herbivore defences especially in productive habitats. Later, as evergreen leaves accumulate, conifer productivity frequently exceeds that of deciduous angiosperms (Fig. 3 ) . ECOLOGICAL CONSEQUENCES OF SLOW SEEDLING GROWTH We are now in a position to reconsider the question of what limits the distribution and abundance of conifers and how angiosperms might be implicated. If productivity is relevant to interspecific competition then one would expect gymnosperms to be poor competitors as seedlings and juveniles but superior competitors as adults (Fig. 3 ) . Many tree species establish in gaps created by disturbances such as wind throw, fire and flooding or by the senescence of canopy trees (White, 1979; Pickett & White, 1985). T h e environmental conditions encountered by seedlings in such gaps are very different from those experienced by parents in the canopy. The weedy features of angiosperm herbs and shrubs are particularly well suited to quick colonization and space pre-emption in regeneration gaps wherever light, water and nutrients are adequate for rapid vegetative growth. Gymnosperms, by contrast, are ill equipped to survive the seedling stage if they have to compete with weedy forbs, grasses or shrubs. Recruitment bottlenecks have been found to be important constraints on adult distribution and abundance in plants and animals (Werner 1979; Werner & Gilliam, 1984; Goldberg, 1982, 1985; Grubb, 1977). Gymnosperms, too, may be excluded from environments where their seedlings encounter vigorous angiosperm competition-typically sites with abundant water, light and nutrients, and a long growing season. W. J. BOND 238 ECOLOGY OF GYMNOSPERM DISlRIBUTIONS Angiosperms can affect gymnosperms regenerating in gaps in at least four specific ways. First, conifer seedling growth may be suppressed by angiosperms, especially herbs, thereby prolonging the juvenile phase. The longer the seedling remains suppressed, the more vulnerable it will be to death from drought, frost or lethal temperatures (Chapman, 1945; Harper, 1977). Secondly competition at the juvenile phase may prolong exposure of juvenile plants to destructive biotic agents, including herbivores, pathogens and litterfall, when they are least equipped to defend themselves (Vaartaja, 1962; Taher & Cooke, 1975; Grime, 1979). Thirdly, angiosperms may radically alter disturbance cycles so that slower maturing gymnosperms would be eliminated. For example, fires may sweep through grasslands killing juvenile conifers before they can overtop and suppress the herbs (Wells, 1965). Finally, even with unchanged disturbance cycles, conifer regeneration may be suppressed by quick-growing angiosperm herbs or shrubs, and the conifers may fail to reach maturity before the stand is replaced following another disturbance (Fig. 4). I A Time Figure 4. Potential effects of angiosperms on gymnosperm growth and survival. Th e shaded area represents the typical range of disturbance frequencies. T h e dashed line, RT, indicates a sizedependent reproductive threshold. ang = angiosperm competitors present; ang- = no effect from angiosperms. A, No effect or1 disturbance; B, angiosperms alter disturbance frequency. + ANGIOSPERM DOMINANCE AND GYMNOSPERM PERSISTENCE 239 I n all four cases, angiosperm competitors are not directly responsible for the demise of conifers but act through a “third party” (Grubb, 1985) such as drought, fire or fungal pathogens. Thus a conifer seedling regenerating under a dense patch of herbs may survive and slowly overtake its competitors unless some environmental ‘challenge’ intervenes such as drought. However, as a first generalization, the slow seedling hypothesis predicts that conifers should be excluded from environments which support dense, rapid vegetative growth in regenerating patches. They would persist best in sites where vegetative growth is slow or where favourable conditions are too brief for dense swards to develop. Conifers would therefore be least threatened by angiosperms in cold climates, climates with a short growing season, or on nutrient poor soils where vegetative growth is slow to close a regenerating gap. Conifers would also tend to be excluded from communities with short intervals between disturbance, especially if juvenile growth is retarded in any way by angiosperm competitors. Biogeographic evidence The global distribution of conifers seems to be compatible with the prediction that they should occur where conditions for rapid vegetative growth are poorest. Contemporary conifers persist in greatest numbers at high elevations or latitudes-the great northern boreal forests, and montane temperate and tropical forests-where vegetative growth is limited by low insolation, cool temperatures and short growing seasons (Schmithusen, 1960; Florin, 1960; Fowells, 1965; Whitmore, 1975; Regal, 1977; Daubenmire, 1978). These regions support low frequencies of growth forms indicative of the capacity of a site to sustain rapid growth rates, such as deciduous plants and annual herbs (Bliss, 1971; Billings & Mooney, 1968; Cain, 1950; Table 3 ) . Deciduous arctic trees are common only where water and nutrients are abundant during the growing season (Chapin, 198 1 ; Heinselman, 1981a ) . ‘I’ABLE3. T h e incidence of annual herbs (therophytes) in relation to altitude. Values arc annuals as a percent of all species in each area (ex Cain, 1954) Locality Clova, Scotland Poschiavo, Alps Annuals Altitude (m) No. of species 1000+ 900- 1000 800-900 700-800 600-700 500-600 400-500 300-400 < 300 11 44 72 170 206 182 193 21 1 304 0 7 4 4 5 4 4 5 13 2850 + 2550-2850 2250-2550 1900-2250 1550-1900 1200-1550 850-1 200 < 850 51 199 348 492 487 449 604 447 2 4 6 6 8 14 19 21 ,(;( 240 W. J. BOND Outside boreal and montane regions, conifers generally occur on nutrient poor sites, especially sandy, acidic, or waterlogged soils. I n California, for example, conifer ‘islands’ in chaparral and oak woodlands are associated with acid sands, serpentines, diatomaceous earths etc. (Mason, 1946; McMillan, 1956; Gankin & Major, 1964; Wells, 1962; Kruckeberg, 1969, 1985; Vogl, 1973). I n the southeastern United States conifers are also associated with sandy and nutrient poor soils (Forman, 1979; Zobel, 1969). Tropical pines in the Americas and South-East Asia occur on nutrient-deficient podsols quite distinct from rain-forest soils (Whitmore, 1975; Kellman, 1984). I n Australia, Callitris and Actinostrobus (Cupressaceae) form extensive woodlands on infertile sands (Lacey et al., 1982; Page & Clifford, 1981) and in South Africa Widdringtonia (Cupressaceae) is similarly restricted to low fertility heath sites (Kruger, 1977). Tropical lowland conifers including Araucaria, Agathis, and Dacrydium typically occur on heathy sites (kerangas) on infertile sands, acid bogs or occasionally on acid pockets of humus on limestone (Whitmore, 1975; Whitmore & Page, 1983; Regal, 1977; 1982). There is no evidence from either plantation forestry or experimental transplants that edaphically restricted conifers prefer nutrient-poor soils. O n the contrary, studies of Californian conifers restricted to infertile soils show that they nearly always grow better on more fertile soils (McMillan, 1956; Griffin, 1965). These results have led many authors to argue that edaphic endemism is maintained by competition between mature conifers and more vigorous woody species on richer soils (Kruckeberg, 1969, 1954; Gankin & Major, 1964; Grime, 1979). The problem, however, is that edaphically restricted conifers (e.g. Pinus radiata, Pinus merkusii) are not primitive slow growing relicts but highly productive species, some of which form the basis for a plantation forestry industry far beyond their native range, and soon overtop their native competitors. Experimental studies suggest that the basis for edaphic endemism may lie, instead, in release from competitors in the regeneration niche. T h e vegetation of nutrient poor soils is characterized by slow relative growth rates, slow foliage turnover and perenniality (Beadle, 1954; Loveless, 1961; Monk, 1966; Specht, 1979; Chabot & Hicks, 1982). Nutrient-poor soils therefore provide a refuge from competition for slower growing seedlings, including those of conifers, because regenerating patches close more slowly (see Goldberg, 1982, 1985 and Buckley, 1984 for angiosperm examples). Site productivity also influences the disturbance regime. Lacey et al. (1982) suggest that Callitris columellaris (Cupressaceae) is restricted to poor sandy soils because the sparser biomass of herbs on these sites does not carry fire as readily as the better soils. Tree seedlings therefore have more time to become established between fires (Lacey et al., 1982). Experimental evidence- forestry and population studies Although biogeographic patterns support the prediction that conifers are restricted to sites which lack a competitive regeneration niche, Regal’s (1977, 1982) pollination hypothesis has similar predictions. He argues that heterozygosity can only be maintained in dense stands of wind pollinated species in low diversity communities and that low diversity is associated with climatic or nutrient stress (Table 4).Experimental evidence is needed to test the separate explanations for gymnosperm biogeography. ANGIOSPERM DOMINANCE AND GYMNOSPERM PERSISTENCE 24 1 TABLE 4. Comparison of t h e pollination hypothesis and t h e slow seedling hypothesis for angiosperm a d v a n t a g e and gymnosperm limitations ~ ~~ Slow seedling Morphological basis of angiosperm advantage Functional effect Predicted gymnosperm range Explanation of range Assumed mechanism Leaf and vascular anatomy, rate of reproduction Assimilation, productivity Reproductive rates ‘Stressful’ environments e.g. cold, nutrient-poor Refugia for slow-growing juveniles from fast-growing angiosperms (a) Competition leading directly or indirectly to increased mortality. (b) Increased disturbance rates eliminate slow-maturing gymnosperms Pollination Flower/fruit, quality of reproduction Insect pollination Seed dispersal by animals ‘Stressful’ environments e.g. cold, nutrient-poor Wind pollination requires dense populations which occur in speciespoor communities. Low diversity is caused by ‘stress’ conditions Heterozygosity is correlated with interspecific competitive ability. Sparse wind-pollinated populations are more homozygous than sparse insect-pollinated populations There are no experimental tests of the pollination hypothesis. T h e central assumption that wind pollination is inefficient in species rich communities has not been directly tested. There seems to be no data a t all, for example, on pollination of sparsely distributed conifers such as Podocarpus scattered in the broad-leaved southern hemisphere forests or Tuxus in the understory of northern forests. I n the case of the slow seedling hypothesis, however, there is abundant experimental evidence demonstrating the competitive effects of angiosperms on gymnosperms. Conifers have been widely planted by foresters outside their natural ranges. These experimental plantations have repeatedly demonstrated startling capacities for tree growth and survival far beyond natural climatic limits. For example, Pinus ponderosu plantations in the prairies of the Great Plains survived the most severe drought on record and grew to 7 m in 30 years in the arid ‘grassland’ climate (Wells, 1965). Evidently grasses both compete with tree seedlings and carry fires that kill trees before they can overtop and suppress the grasses (Wells, 1965). Conifers are excluded from the Great Plains less by the ‘grassland climate’ than by the effects of grasses on the disturbance cycle and on regenerating tree seedlings (Wells, 1965; Axelrod, 1985). Removal of understory competitors is a n important silvicultural treatment in commercial forestry and has been repeatedly shown to have a major influence on the establishment of many timber species (see references in Tourney & Keinholz, 1931; Fowells, 1965; Stewart, Gross & Honkala, 1984; Sands & Nambiar, 1984; McDonald, 1986). Angiosperm competition with conifers causes either increased seedling mortality, usually in the first year or two of establishment, or decreased growth of saplings. Angiosperm herbs, especially grasses, outgrow and shade the conifers and compete for water and nutrients in the surface layers of the soil (see e.g. Shirley, 1945) (shading can also be beneficial in reducing lethal soil temperatures). Conifers are excluded from many regions by grasses which suppress the growth of tree seedlings (e.g. Pearson, 1942; Johnsen, 1962; Hadley, 1969; Burkhardt & Tisdale, 1976; Sims & Mueller-Dombois, 1968). Although angiosperm competition in the regeneration niche is an important component, the causes of these recruitment bottlenecks are usually complex and 242 W. J . BOND multifactorial. For example, the origin of cohorts of similarly aged junipers in rangelands can often be traced to episodes of' heavy grazing (which leads to decreased competition between grass and tree seedlings), reduced fire frequencies and higher than average precipitation or the coincidence of two or more of them (Johnsen, 1962; Smith, Wright & Schuster, 1975; Madany & West, 1983). The studies cited above refer mostly to seasonally arid woodlands or savannas, but herbs can also severely inhibit seedling establishment after disturbance in other environments, for example in mesic forests such as those of the Pacific Northwest (Strothmann & Roy, 1984), alpine meadows where grasses and forbs inhibit the invasion of coniferous trees (Franklin, Moir, Douglas & Wiberg, 1971; Kotar, 1978), or Mediterranean shrublands where grasses inhibit establishment of Pinus halepensis seedlings (Acherar, Lepart & Debussche, 1984). In addition to herbs, angiosperm shrubs and small trees are also important competitors of juvenile conifers (Conrad & Radosevich, 1982; Hobbs & Wearstler, 1985; McDonald, 1986). In the absence of disturbance, severe droughts or the attack of herbivores or pathogens, suppressed conifers may eventually survive to reach the canopy. For most North American conifers, however, suppressed growth increased the risk of death from periodic drought (Chapman, 1945), fire (Arend, 1950; Burkhardt & Tisdale, 1976; Strothman, 1967) or herbivory, especially by vertebrates. For example Chapman (1945), in a study of Loblolly pine (P. taeda) regeneration, found that the shade of low hardwood shrubs was fatal to pine seedlings. Under high overhead shade, however, and in the absence of low shrubs Loblolly pine survived as suppressed seedlings or saplings for up to 20 years, provided that no severe droughts occurred. These suppressed saplings remained vulnerable to light surface fires at any season whereas seedlings in open sunlight rapidly gained resistance to surface fires. Similar examples occur wherever fire is important in initiating regeneration (Strothmann & Roy, 1984; Wright & Bailey, 1982; Heinselman, 1981a, b). Shade-tolerant conifers The majority of gymnosperms regenerate in large openings created by disturbances such as fire and windstorms (e.g. Fowells, 1965; Whitmore, 1975). A few, however, are shade-tolerant and regenerate in openings created by a single tree or branch fall (e.g. Tsuga canadensis, Podocarpus spp.). Indeed one would expect gymnosperms to persist in such habitats since deep shade would reduce the growth advantages of'angiosperms in the same way as nutrient poor soils and cold climates. Though shade tolerant conifer seedlings do compete with understory angiosperms for the most favourable space on the forest floor (Maguire & Forman, 1983), many survive and persist for years as slow growing, suppressed understory trees. The principles underlying relative abundance and species diversity in forests with tree by tree replacement are still poorly understood (Hubbell & Foster, 1986) but some studies suggest similar processes to those discussed above. Gymnosperms have a more rigid architecture than angiosperm trees and have a lower rate and propensity for reiterating branches (Brown, 1971; Halle, Oldeman & Tomlinson, 1978). Consequently they may be less opportunistic at filling space made available by the death of neighbours (e.g. Hibbs, 1982). Halle et al. (1978) attribute the greater plasticity of angiosperm architecture to the ANGIOSPERM DOMINANCE AND GYMNOSPERM PERSISTENCE 243 more efficient transport system of angiosperms coupled with larger, more productive leaves. If gymnosperms are less able to respond to sudden changes in the canopy environment due to the death of neighbours, then (a) gymnosperm canopy trees will be slower than angiosperms to fill gaps in the forest by lateral growth and (b) gymnosperm saplings will be slower than angiosperm saplings to fill gaps in the canopy by height growth. Hibbs (1982) has provided quantitative data for a north temperate hemlock-hardwood forest. He showed that lateral growth of Tsuga canadensis, a conifer, was the slowest of the five tree species he measured (the rest all angiosperms) while height growth of hemlock saplings in small gaps was also by far the slowest (Hibbs, 1982; see also Runkle & Yetter, 1987). Ifsuch patterns prove general, then shade-tolerant gymnosperms would be restricted to forests where (a) growth rates are slow because of climatic or nutrient limitations on productivity, (b) gaps are small and saplings are shaded and ( c ) there are very long intervals between major stand-destroying disturbances so that the slow growing conifers have sufficient time to reach the canopy. These predictions differ from Regal’s (1977) suggestion that gymnosperms should be confined to “low diversity” forests. Species richness would not be an important factor in gymnosperm distribution. However gymnosperms should be excluded from forests with dense liana growth, a high frequency of compound leaves or other structural attributes indicative of rapid secondary growth or rapid filling of canopy gaps. There are too few studies to test these predictions for shade-tolerant conifers but this is currently a n active area of research (see reviews in Pickett & White, 1985). DISCUSSION The central question I attempt to answer is: what restricts modern gymnosperm distribution? Despite the high productivity of mature conifers, the growth rates of juveniles are low. I argue that competition from angiosperms in the regeneration niche is currently the most plausible hypothesis for the many gymnosperms which regenerate after disturbance. T h e main competing hypothesis is that gymnosperms are limited by the inherent limitations of wind pollination to living in relatively pure stands (P. Raven, 1977; Regal, 1977, 1982; Burger, 1981). Both hypotheses are general-that is they assume a link between functional morphology, ecology and the distribution of major taxa (Table 4).Almost no direct evidence exists to test the pollination hypothesis SO that its breadth of application is unknown. The slow seedling hypothesis, however, is supported by considerable experimental evidence for the importance of angiosperm competition in gymnosperm regeneration and rather less evidence for lethal effects of angiosperms on the disturbance regime. I n the case of shadetolerant gymnosperms (which escape competition as seedlings) populations appear to be limited, by the same growth constraints, to forests with small gap sizes and very infi-equent large-scale disturbances. T h e regeneration niche and the fossil record Does the slow seedling hypothesis explain Cretaceous extinctions of gymnosperms? There are many difficulties in determining process from pattern in the paleobotanical record and the patterns themselves are still controversial 244 W. J BOND (Knoll & Rothwell, 1981; Knoll, 1986; Hickey & Doyle, 1977; Krassilov, 1978). Current interpretations of the fossil record suggest that the angiosperm invasion began from small shrubs in semiarid (Stebbins, 1974) or seasonally dry (Hickey & Doyle, 1977) tropical highlands. T h e weedy attributes of angiosperms were the basis of their initial rapid spread into a variety of unstable depositional environments such as fluvial and deltaic levees and tidal flats (Doyle & Hickey, 1976, Hickey & Doyle, 1977). These temporary habitats were common worldwide because of the breakup of continents and marine transgressions (Retallack & Dilcher, 1981; Frakes 1979). Later, angiosperms diversified into a variety of niches and they began to enter the understory of coniferous forest in more stable landscapes (Doyle & Hickey, 1976; Doyle, 1977; Krassilov, 1978). The first angiosperm trees to reach the canopy only appeared in the beginning of the Late Cretaceous (Doyle, 1977). Indeed some authors have argued that conifers continued to dominate forest canopies until the very end of the Cretaceous with angiosperms merely filling the once-empty understory (Doyle, 1977; Krassilov, 1978). The distinction between enrichment of gymnosperm paleofloras by angiosperms occupying new niches or the replacement of gymnosperms by vigorous angiosperm competitors is often ignored in discussions of the basis of the angiosperm success. Yet the timing of gymnosperm decline is crucial to some explanations, particularly those which invoke coevolution with animal pollinators, dispersers or herbivores ($ Regal, 1977; P. Raven, 1977). Thus Regal (1977) argued that the dispersal of angiosperm seeds by birds was important in early angiosperm radiation yet abiotic dispersal predominated throughout the Cretaceous (Tiffney, 1984). With these uncertainties it seems futile to argue for a single cause of gymnosperm decline. For example, Krassilov (1 978) has suggested that a terminal Cretaceous catastrophe caused the extinction of the Mesozoic conifer overstory. However a catastrophist hypothesis cannot explain the demise of the Cheirolepidiaceae in the mid-Cretaceous nor the relative increase in conifer pollen immediately above the Cretaceous-Tertiary boundary (Saito, Yamanoi & Kaiho, 1986). It is often assumed that direct competition between angiosperms and gymnosperms only commenced when angiosperms evolved canopy trees, that is, when the adult growth forms closely overlapped. The potential importance of angiosperms slowly intruding into the juvenile niche of gymnosperms has been overlooked. Competition between angiosperm shrubs and regenerating trees would have existed early in the Cretaceous with the most severe consequences in regions with periodic drought-such as the seasonal tropics where the Cheirolepidiaceae were the first of the gymnosperms to go extinct (Alvin, 1982). The modern interaction between competition and disturbance cycles could also have occurred early in angiosperm evolution. Early angiosperms were associated with the most frequently disturbed terrain in Cretaceous floodplains (Doyle, 1977; Retallack & Dilcher, 1981) and fires swept through Mesozoic forests creating favourable conditions for weedy, early successional angiosperms (Harris, 1958). Dinosaurs may even have created opportunities for weedy angiosperms as they blundered through Cretaceous conifer forests (Wing & Tiffney, 1987). However, although herbs evolved very early in the Cretaceous (Doyle & Hickey, 1976), grasses only become important in the Oligocene and their effects on conifers may have occurred only as late as the Pleistocene (Axelrod, 1985). ANGIOSPERM DOMINANCE AND GYMNOSPERM PERSISTENCE 245 CONCLUSIONS Gymnosperms, and conifers in particular, are an excellent case-study in the search for generalizations linking functional morphology with ecology. The hypotheses presented here suggest an envelope of possibilities within which gymnosperms can co-occur with angiosperms. Whether they do occur within these bounds depends on many other factors, the random accidents of dispersal, the presence of a particular seed predator, fungal pathogens and their insect vectors and so on. This attempt at a general explanation for the decline of gymnosperms is justified by the perspective it gives to plant evolution. IS, indeed, the giant sequoias retreated because of low weeds interspersed in their understory then the circumstances that change the vegetation of the earth are seen in a rather different light. ACKNOWLEDGEMENTS I benefitted from discussions with P. Grubb, A. Gibson, A. Knoll, P. Nobel, B. Prigge, P. Regal and D. Walker amongst many others while developing these ideas. M. Cody, P. Frost, L. Kohorn, F. Kruger, J. Midgley and P. Rundel made useful comments on the manuscript. An anonymous reviewer pointed out some of the pitfalls awaiting neontologists interested in paleobotany. The research was supported by a Vavra and University of California Research Fellowship. REFERENCES ACHERAR, M., LEPART, J . & DEBUSSCHE, M., 1984. La colonisation des friches par le pin d’Alep (Pinus halepensi5 Miller) e n Languedoc mediterranten. Oecologia Plantae, 5: 179-189. ALVIN, K. L., 1982. Cheirolepidiaceae: Biology, structure and paleoecology. Review of Paleobotany and Paiynology, 37: 55-70. AREND, J. L., 1950. Influence of fire and soil on distribution of eastern red cedar in the Ozarks. Journal of Forestry, 48: 120-130. ASHTON, D. H., 1975. Studies of flowering behavior in Eucalyptus regnans F. Muell. Australian Journal of Botany, 23: 399-41 1. AXELROD, D. I., 1985. Rise of the grassland biome, central North America. Botanical Review, 51: 163-201. BEADLE, N. C. W., 1954. Soil .phosphate and delimitation of plant communities in eastern Australia. I. . Ecology, 35: 370-375. BILLINGS. W. D. L? MOONEY. H. A,. 1968. Bioloeical Review. 43: 481-530. BLISS, L. C., 1971. Arctic and alpine plant life cycles. Annual Reuiew Ecologj and Systematia, 2: 405438. BROWN, C. L., 1971. Secondary growth. In M. H . Zimmermann & C. L. Brown (Eds), Trees: Structure and Function: 67-124. New York: Springer. BROWN, A. H. D., 1979. Enzyme polymorphism in plant populations. Theoretical Population Biology, 15: 1-42. BUCKLEY, G. P., 1984. The uses of herbaceous companion species in the establishment of woody species from seed. Journal of Environmental Management, 18: 309-322. BURGER, W. C., 1981. Why are there so many kinds of flowering plants. Bioscience, 31: 572-581. BURKHARDT, J. W. & TISDALE, E. W., 1976. Causes ofjuniper invasion in southwestern Idaho. Ecology, 57: 472-484. CAIN, S. A,, 1950. Life-forms and phytoclimatc. Botanical Review, 16: 1-32. CALKIN, H. W., GIBSON, A. C. & NOBEL, P. S., 1986. Biophysical model ofxylem conductance in tracheids of the fern Pteris villala. Journal of Experimental Botany, 37: 1054-1064. CARLQUIST, S ., 1975. Ecological Strategies of Xylem Evolution. Berkeley: University of California Press. CARLQUIST, S., 1985. Vasicentric tracheids as a drought survival mechanism in the woody flora ofsouthern California and similar rwions: review of vasicentric tracheids. Aliso, 11: 37-68. CHABOT, B. F. L? HICKS,‘D. J., 1982. The ecology of leaf life spans. jfnnual Review Ecology and Systematics, 13: 229-259. CHAMBERLAIN, C. J., 1934. ~ymnosperms-Structure and Evolution. Chicago. CHAPIN, F. S., 1981. Plant nutrient absorption and retention under differing fire regimes. I n H. A. Mooney & T. M. Bonnicksen (Eds), Fire Regimes and Ecosystem Properties. United States, Department ofrigriculture, Forest Service General Technical Report, WO-26: 30 1-32 1. Y 246 W. J . BOND CHAPMAN, H. H., 1945. 'l'hc effect of overhcad shadc on the survival ol'loblolly pine seedlings. Ecology, 26: 274-282. C:ONKAD, S . G. & RADOSEVICH, S. R . , 1982. Growth responses ofWhite Fir to decreased shading and root competition hy montane chaparral shruhs. Forest Science, 28: 309-320. CREPE?', Mi. L., 1983. 'I'hc role of insrct pollination in the evolution of the angiosperms. In L. Real (Ed.), Pollination BioloLu:29 50. Orlando, Florida: Academic Press. CREPET, W. L., 1984. Advanced (constant) insect pollination mechanisms: pattern of rvolution and implications vis-a-vis angiosperm diversity. Annals of the M i m u r i Botanical Garden, 71: 607-630. DAUBENMIRE, R . , 1978. Plant geography with sperial reference to North America. New York: Academir Prrss. DOYLE, J. A., 1977. Patterns of evt)lution in early angiosperms. I n A. Hallam (Ed.), Patterns qf Ewdulion US illustrated by the F m i l Record: 501-546. Amsterdam: Elsevier. DOYLE, J. A. & D O N O G H U E , M. J , , 1986. Seed plant phylogeny and the origin of angiosperms: an experimental cladistic approach. Butanical Keuiew, 52: 321-402. DOYLE, J. A. & HICKEY, L. J., 1976. Pollen and leaves from the mid-Cretaceous Potomac Group and their hearing on early angiosperm evolution. I n C. B. Beck (Ed.), Ori~qinand Early Evolution ofAngio.rperms: 139-206. New York: Columbia University Prcss. ELLSTRAND, N. C. & MARSHALL, D. L., 1985. Interpopulation gene flow by pollen in wild radish Kaphanus satiuus. American NaturaliJt, 126: 6 0 6 ~6 16. ESAU, K., 196.5. Plant Anatomy. 2nd cdn. New York: Wiley. E'ARRIS, M. A. h MI'I"TON,J. B.., 1984. Population density, outcrossirig rate, and hetcrozygotr superiority in ponderosa pine. Euolulion, 38: 1151-1 154. FLORIN, R. 1960. 'l'he distribution of conifer arid taxad genera in time and space. Acta Horti Bergianz, 20: 1223 14. FORMAN, K.T. 'I., (Ed.), 1979. Pine Barrens: Ecogutem and Landscape. New York: Arademic Prrss. FOWELLS, H. A,, 1965. Siluics qfporest Trees of the United States. Unitrd States, Department OJAgriculture, H i d b o o k No. 271. Washington D.C. FOSTER, A. S. & GIFFORD, F,. M., 1974. Comparative morphology of vascular plants. San Francisco: Freeman. FRANKLIN, J. F.,MOIR, W. H., DOUGLAS, G. W. & WIBERG, C., 1971. Invasion ofsuhalpinr mcadows by trees in the Cascade range, Washington and Oregon. Arctic and Alpine KeJearch, 3: 215-224. FRAKES, L. A,, 1979. Climates through Geolo,qical Time.Amsterdam: Elsevier. GANKIN, R . & MAJOR, J., 1964. ArctostnphyloJ myrt@lia, its biology and relationship to the problem ol' endemism. Ecology, 45: 792-808. GIBSON, A. C., CALKIN, H, W., & NOBEL, P. S., 1984. Xylem anatomy, water flow, and hydraulic conductance in the fern Cyrtomium falcatum. American Journal of Botany, 71: 564-574. GIVNISH, 'I.J., 1978. O n tlic adaptive significance of compound leaves, with particular reference to tropical trees. I n P. B. Tomlinson & M. H . Zimmerman (Eds), Tropzcal Trees as Liuzng ,$ystems: 351-380. London: Cambridgc University Prrss. GIVNISH, T .J., 1979. On the adaptive significance of leaf form. I n 0. Solbrig, P. H. Raven, S. Jain & G. B. Johnson (Eds), Topics in Plant Population Biology: 375-407. New York: Columbia Uriiversity Press. GOLDBERG, D. E., 1982. T h e distribution of evergreen and deciduous trccs relative to soil type: an example from the Sierra Madre, Mexico, and a genrral model. Ecology, 63: 942-951. GOLDBERG, 1). E., 1985. Efyects of soil pH, rompctition, and seed prrdatiori on the distributions of two tree species. L?'colo,gy, 66: 503-5 1 1. CKIE'E'IN, J. R., 1965. Digger pine seedling responsc to serpentinite and uon-serpentinite soil. F o l o ~ 46: , 801807. G R I M E , J. P., 1979. Plant Strateyies and Vegetation Proceues. New York: Wiley. G R I M E , J . P. & H U N T , R., 1975. Relative growth rate: its range and adaptive signiticaricc in a local flora. Journal of Ecology, 63: 393-422. GRUBB, P. J,, 1977. T h e maintenance of species-richness in plant rommunitics: the importance of thc regeneration niche. Bioloyical Reviews, 52: 107-145. GRUBB, P. J., 1986. 'l'hr ecology ol'establishmcnt. I n A. D. Bradshaw, 1). Goodc & E. T h o r p (Eds), E c o ~ J , ~ and Desiyn zn Landscape. Oxford: Blackwell. HADLEY, E. H., 1969. Physiological ecology of Pinusponderosa in Southwestern North Dakota. American Midland Naturalist, 81: 289-314. HAMRICK, J. L., LINHAR'I', Y. B. & MI O N , J. B., 1979. Relationships betwccn life-history characteristics and electrophorctically detectable genctic variation in plants. Annual Reuiew o/ fi;cology and Systematics, 10: 173-200. HALLE, I;., OLDEMAN, R . A. A,, & 'IOMLINSON, P. B., 1978. Tropical Trees and Forests: an Architectural AnalyJiJ. Berlin h New York: Springer Verlag. HARRIS, '1'. M., 1958. Forest firr in the Mesozoic. Journal a/ Ecolo~u,4fi: 447-453. HARPER, J. L., 1977. Popiilation Biolygy of Planh. New York, London: Academic Press. HEINSELMAN, M. L., 1981a. Fire and succession in the conifer forests of northern North America. I n D. (1. West, H . H. Shugart & D. B. Botkin (Eds), Fomt Succession: ConceptJ and Applications: 374 405. Berlin and New York: Springer-Verlag. ANGIOSPERM DOMINANCE AND GYMNOSPERM PERSISTENCE 247 HEINSELMAN, M. L., 1981h. Fire intensity and frequency as factors in the distribution and structure of northern ccosystcms. In H. A. Mooney, T. M. Bonnicksen, N. L. Christensen, J . E. Lotan & W.A. Reiners (Eds), Fire Regimes and Ecocytem Properties. C‘nited StateJ, Department of Agriculture, Forest Seruice General Technical Report, WO-26: 7-57. HIBBS, D. E., 1982. Gap dynamics in a hemlock-hardwood forest. Canadian Journal of’Fnrest Rerearch, 12: 522527. HICKEY, L. J . & DOYLE, J. A., 1977. Early Crctaceous fossil evidence for angiosperm evolution. Botanical Review, 41: 3-103. HIEBERT, R. D. & HAMRICK, J. L., 1983. Patterns arid levels ofgenetic variation in Great Basin Bristlerone Pine, Pinus longaem Eoolution, 37: 302-3 10. HOBBS, S. D. & WEARSTLER, K. A , , 1985. Effects of cutting sclerophyll brush on sprout development and Douglas-Fir growth. Forest Ecoloo and Management, 13: 69-8 1, HUBBELL, S. P. & FOSTER, R . B., 1986. Biology, chance and history and the structure oftropical rain forest tree communities. I n J . Diamond & T. J . Casr (Eds), Communily Ecology: 314-329. New York: Harper & Row. HUGHES, N. F., 1976. Palaeohiology of Angiosperm Ori&s. Cambridge: Cambridgc Univrrsity l’rrss. HUGHES, N. F., 1977. Palaco-succession of earliest angiosperm evolution. Botanical Reuiew, 43: 105-127. JABLONSKI, D., 1986. Background and mass extinctiom: thc alternation of macroevolutionary rcgimrs. Science, 231: 129-133. JARVIS, P. G. & JARVIS, M. S., 1964. Growth rates of woody plants. Physiologia Plantarnm, 17: 654-666. JARVIS, P. G. & LEVERENZ, J. W., 1982. Productivity of temperate, deciduous and evergreen forests. Encyclopaedia o j Plant Physiology, N. S. Vol12B: 233-280. Berlin: Springer-Vcrlag. JOHNSEN, T. N., 1962. One-seed juniper invasion of northern Arizona grasslands. Ecolo,@al Monographs, 32: 187-207. JONES, H. G., 1983. Plant.r and Microclimate. Cambridgc: Cambridge University Prrss. KELLMAN, M., 1984. Synergistic relationships between fire and low soil fertility in rieotropical savannas: a hypothesis. Biotropica, 16: 158-160. R, A. R., LANDE, R . & SCHEMSKE, D. W., 1984. Models of coevolution and sprciation in plants and their pollinators. American Naturalist, 124: 220-243. KNOLL, A. H., 1984. Patterns ofextinction in fossil record ofvascular plants. In M. Nitccki (Ed.), Extinctions: 21-67. Chicago: University of Chicago Press. KNOLL, A. H., 1986. Patterns of change in plant communities through geological time. I n J. Diamond & T. Case (lids), CommuniQ Lcology: 126-141. New York: Harper & Row. KNOLL, A. H. & RO’I‘HWELL,G . W., 1981. Paleobotany: perspectives in 1980. Paleabiolngy, 7: 7-35. KOTAR, J,, 1978. Relationship of carly seedling development to altitudinal distribution of Abies amahilis. Bulletin of the T o r y Botanical Club, 105: 289-295. KRASSILOV, V. A,, 1978. Late Cretaceous gymnosperms from Sakhalin and the terminal Cretaceous event. Palaeontology, 21: 893-905. KRUCKEBERG, A. R., 1954. The ecology of serpentine soils. 111. Plant species in relation to serpentine soils. Ecology, 35: 267-274. KRUCKEBERG, A. R., 1969. Soil diversity and the distribution of plants with examples from western North America. Madrono, 20: 129-154. KRUCKEBERG, A. R., 1985. Cal$mia Serpentines: Flora, Vegetation, G e o l g y , Soilr, and Mana,pment 1’roblem.c. Berkeley: University of California Press. KRUEGER, K. W. & R U T H , R . H., 1969. Comparative photosynthesis of red alder, Douglas-fir, Sitka spruce, and western hemlock seedlings. Canadian Joiirnal of Botany, 47: 5 19-527. KRUGER, F. J., 1977. Ecology of Cape fynhos in relation to fire. Procrcdings of the symposium 011 thc environmental consequences of fire and fuel managcment in meditcrranean ecosystems. In H. A. Mooncy & C. E. Conrad. United States, Department of Agriculture, Foreign Seraire General Technical Report, WO-3: 230 244. LACEY, C. J., WALKER, J. & NOBLE, I . R., 1982. Fire in Australian tropical savannas. I11 B. J . Huntley & B. H. Walker (Eds), EcoloLu of Tropical Savannas: 246-272. Berlin: Springer-Vcrlag. LARCHER, W., 1980. Physiological Plant Ecology. Berlin: Springer-Verlag. LEDIG, F. T. & CONKLE, M. T,, 1983. Gene diversity and genetic structure in a narrow endrmir, Torrey pine (Pinus torreyana Parry ex Carrj. Evolution, 37: 79-85. LEMON, E. R. (Ed.), 1983. CO, and plants. The responsr of plants to rising lrvcls of atmospheric carbon dioxide. Boulder, Colorado: Wrstview Press. LOVELESS, A. R., 1961. A nutritional interpretation of sclerophylly based 011 diffrrcnccs in thr chcmical composition of sclerophyllous arid mesophytir leaves. Anna2.r of Botany, 25: 168-1 84. LOVELESS, M. D. & HAMRICK, J. L., 1984. Ecological determinants of genetic structiire in plant populations. Annual Review of Eco1o.w and ,Qstematics, 15: 65-95. MADANY, M. H. & WEST, N. E., 1983. Livestock grazing-fire regime interactions within montane forests of Zion National Park, Utah. Ecology, 64: 661-667. MAGUIRE, D. A. & FORMAN, R. ’r. T., 1983. Herb cover effects on tree sredling patterns in a mature hrmlork-hardwood forest. Ecology, 64: 1367-1380. MASON, H. L., 1946. ‘Ihe edaphic factor in narrow endrmism. 11. The geographic occurrence of plants of highly restricted patterns of distribution. Madrono, 8: 241-257. 248 W. J. BOND McDONALD, P. M., 1986. Grasses in young conifer plantations- hindrance and help. Northwest Science, 60: 27 I -278. McMILLAN, C., 1956. The edaphic restriction of Cupressus and Pinus in the Coast Ranges of central California. Ecological Monographs, 26: 177-2 12. MONK, C. D., 1966. An ecological significance of evergreenness. Ecolog,~,47: 504-505. MOONEY, H. A. & DUNN, E. L., 1970. Convergent evolution of mediterranean-climate evergreen sclerophyll shrubs. Evolution, 24: 292-303. MOONEY, H. A. & GULMON, S. L., 1983. ' I h e determinants of plant productivity-natural versus manmodified communities. In H. A. Mooney & M. Godron (Eds), Disturbance and Ecosystems: 146-158. Berlin: Springer-Verlag. MULCAHY, D. L., 1979. l h e rise of the angiosperms: a genecological factor. Science, 206: 20-23. NELSON, N. D., 1984. Woody plants are not inherently low in photosynthetic capacity. Photosynthetica, 18: 600605. NIKLAS, K. J., 1985. The evolution of tracheid diameter in early vascular plants and its implications on the hydraulic conductance of the primary xylem strand. Evolution, 39: 11 10-1 12. NOBEL, P. S., 1983. Biophysical Plant Physiology and Ecology. San Francisco: Freeman. OVING'ION, J. D., 1956. The form, weights and productivity of tree species in close stands. N e w Phytologist, 55: 289-304. PAGE, C. N. & CLIFFORD, H . T., 1981. Ecological biogeography ofAustralian conifers and ferns. In A. Keast (Ed.), Ecological Biogeography of Australia: 473-498. The Hague: Junk. PEARSON, G. A., 1942. Herbaceous vegetation, a factor in natural regeneration of' ponderosa pinc in the southwest. Ecological Monographs, 12: 3 15-338. PICKETT, S. T. A. & WHITE, P. S. (Eds), 1985. The Ecology ofNatura1 Disturbance and Patch Dynamics. Orlando: Academic Press. POLLARD, D. F. W. & WAREING, P. F., 1968. Rates ofdry-matter production in forest tree seedlings. Annals of Botary, 32: 573-59 1. PLYMALE, E. L. & WYLIE. R. B. 1944. The major veins of mesomorphic leaves. American Journal of Botany, 31: 99-106. RAUP, 1).M. & SEPKOSKI, J. J., 1986. Periodic extinction of families and genera. Science, 2.71: 833-836. RAVEN, J. A., 1977. The evolution of vascular land plants in relation to supracellular transport processes. Advances in Botanical Research, 5: 153- 2 19. RAVEN, P. H., 1977. A suggestion concerning the Cretaceous rise to dominance of the angiosperms. Evolution, 31: 451-452. REGAL, P. J., 1977. Ecology and cvolution of flowering plant dominance. Science, 196: 622-629. REGAL, P. J., 1982. Pollination by wind and animals: ecology of geographic patterns. Annual Review ofEcology and Systematics, 13: 497-524. KETALLACK, G. & DILCHER, D. L., 1981. A coastal hypothesis for the dispersal and rise to dominance of flowering plants. In K. .J. Niklas (Ed.), Paleobotany, Paleoecology, and Evolutiun: 27-67. New York: Praeger. ROOK, D. A. & WHYTE, A. G. D., 1976. Partial defoliation and growth of 5-year-old Radiata pine. Nem 'reefalls revisited: gap dynamics in thc southern Appalachians. Ecology, 68: 417424. RURY, P. M . & DICKISON, W. C., 1984. Structural correlations among wood, leaves and plant habit. In W. C. Dickison (Ed.), Contemjorary Problems in Plant Anatomy: 495--540. New York: Academic Press. SAITO, l . , YAMANOI, 7'.& KAIHO, K., 1986. End-Cretaceous devastation of trrrestrial flora in the boreal Far East. Nature, 323: 253-255. SANDS, R . & NAMBIAR, E. K. S., 1984. Water relations of radiata pine in competition with weeds. Canadian Journal o j Forest Research, 14: 233-237. SATOO, T. & MADGWICK, H. A. I., 1982. Forest Biomass. The Hague: Martinus Nijhoff. SCHULZE, E. -D., FUCHS, M . & FUCHS, M. I., 1977. Spacial distribution of photosynthetic capacity and performance in a montane spruce forest of Northern Germany. 111. The significance of the evergreen habit. Oecologia, 30: 239-248. SCHULZE, E. D., KUPPERS, M . & MATYSSEK, R., 1986. The roles of carbon balance and branching pattern in the growth of woody species. In T. J . Givnish (Ed.), O n the Economy o f p l a n t Form and Function. London: Cambridge University Press. SCHMITHUSEN,J., 1960. Die Nadelholzer in den Waldgesellschaften der siidlichen Anden. Vegetatio, 9: 313327. SHIRLEY, H. L., 1945. Reproduction ofupland conifers in the Lakc States as affected by root competition and light. American Midland Naturalist, 33: 537-6 12. SIMS, H. P. & MUELLER-DOMBOIS, D. 1968. Effect of grass competition and depth to water table on height growth of coniferous tree seedlings. Ecology, 49: 597-603. SMITH, M. A., WRIGHI', H. A. & SCHUSTEK, J. L., 1975. Reproductive characteristics of redberry juniper. Journal of Range Management, 27: 126-128. SPECHT, R. L., 1979. Heathlands and related shrublands of the world. In R . L. Specht (Ed.), Ecosystems ofthe World, vol. 9A. Heathlands and Related Shrub/ands: Descriptive studies. Amsterdam: Elsevier. ANGIOSPERM DOMINANCE AND GYMNOSPERM PERSISTENCE 249 STEBBINS, G. L., 1974. Flowering Plants: Evolution above the Species Leuel. Harvard University Press: Cambridge, Belknap. STEBBINS, G. L., 1976. Seeds, seedlings, and the origin of angiosperms. I n C. B. Beck (Ed.), Origin and Early Evolution of Angiosperms: 300-3 11. New York: Columbia University Press. STEBBINS, G. L., 1981. Why are there so many species of flowering plants? Bioscience, 31: 573-577. S'I'EWART, W. N., 1983. Paleobotany and the Evolution of Plants. Cambridge: Cambridge University Press. S r E W A R T , R . E., GROSS, L. L. & HONKALA, B. H., 1984. Effects of competing vegctation on forest trres: A bibliography with abstracts. United States, Department of Agriculture, Forest Services General Technical Report, WO-43. Washington D.C. STROTHMANN, R . O., 1967. The influence of light and moisture on the growth of red pine seedlings in Minnesota. Forest Science, 13: 182-191. STROTHMANN, R . 0. & ROY, D. F., 1984. Regeneration ofdouglas fir in the klamath region, California and Oregon. United States, Department of Agriculture, Forest Service General Technical Report, PS W-81. TAHER, M. M . & COOKE, R . C., 1975. Shade induced damping-off in conifer seedlings I. Effects of reduced light intensity on infection by necrotrophic fungi. N e w P/ptologirl, 75: 567-572. 'I'IFFNEY, B. H., 1984. Seed size, dispersal syndromes and the rise of angiosperms: evidence and hypothesis. Annals ofthe Missouri Botanic Garden, 71: 551-576. 'IOUMEY, J. W. & KEINHOLZ, R., 193 1. Trenched plots under forest canopies. Yale UniversiQ School Forestry Bulletin, 30. UPCHURCH, G . R . & CRANE, P. R., 1985. Probable Gnetalean megafossils from the Lower Cretaceous Potomac Group of Virginia. American Journal ofBotary, 72: 903. VAARTAJA, O., 1962. The relationship of fungi to survival of shaded tree seedlings. Ecology, 43: 547-548. VOGL, R. J., 1973. Ecology of knohcone pine in the Santa Ana Mountains, California. Ecological Monographs, 43: 125-143. WARING, R . H., 1983. Estimating forest growth and efficiency in relation to canopy leaf area. Advances in Ecological Research, 13: 327-354. WARING, R . H . & FRANKLIN, J. F., 1979. Evergreen coniferous forests of the Pacific Northwest. Science, 204: 1380-1386. WELLS, P. V., 1962. Vegetation in relation to geological substratum and fire in the San Luis Obispo Quadrangle, California. Ecological Monographs, 32: 79-103. WELLS, P. V., 1965. Scarp woodlands, transported soils and concept of grassland climate in the Great Plains region. Science, 148: 246-249. WENT, F. W., 1948. Ecology of desert plants. I. Observations on germination in the Joshua Tree National Monument. Iicology, 29: 242-253. WERNER, P. A,, 1979. Competition and coexistence ofsimilar specics. In 0. T. Solbrig, S. Jain, G. B. Johnson & P. H. Raven (Eds), Topics in Plant Population Biology: 287-310. New York: Columbia University Press. WERNER, E. E. & GILLIAM, J. F., 1984. The ontogenetic niche and species interactions in size-structured populations. Annual Review of Ecology and Systematics, 15: 393-425. WHITE, P. S., 1979. Pattern, process and natural disturbance in vegetation. Botanical Reuiews, 45: 229-299. WHITEHEAD, D. R., 1969. Wind pollination in the angiosperms: evolutionary and ecological considerations. Evolution, 23: 28-35. WHITEHEAD, D. R., 1983. Wind pollination: some ecological and evolutionary perspectives. I n L. Real (Ed.), Pollination Biology: 97-108. Orlando: Academic Press. WHITMORE, T. C., 1975. Tropical rainforests of the Far East. Oxford: Clarendon Press. WHITMORE, T. C. & PAGE, C. N., 1983. Evolutionary implications of the distribution and ecology of the tropical conifer Agathis. N e w Phytologist, 84: 407-416. WHITMORE, T. C. & WOOI-KHOON, G. 1983. Growth analysis of the seedlings of balsa, Ochroma lagopus. N e w Phytologist, 95: 305-3 11. WILLSON, M. F. & BURLEY, N., 1983. Mate Choice in Plants: Tactics, Mechanisms and Consequences. Princeton, New Jersey: Princeton University Press. WING, S. L. & TIE'FNEY, B. H., 1987. Interactions of angiosperms and herbivorous tetrapods through time. I n E. M. Friis, W. G. Chaloner & P. R. Crane (Eds), T h e origins ofangiosperms and their biological consequences: 203-224. Cambridge: Cambridge University Press. WRIGHT, H. A. & BAILEY, A. W., 1982. Fire Ecology. United States and Southern Canada. New York: Wiley. WYLIE, R. B., 1938. Concerning the conductive capacity of the minor veins of foliage leaves. American Journal of Botany, 30: 273-280. ZIMMERMANN, M. H., 1978. Structural requirements for optimal water conduction in tree stems. I n P. B. Tomlinson & M . H . Zimmermann (Eds), Tropical Trees as Living Systems: 517-532. London: Cambridge University Press. ZIMMERMANN, M. H., 1983. Xylem Structure and the Ascent of Sap. Berlin: Springer-Verlag. ZIMMERMANN, M . H. & BROWN, C. L., 1971. Trees. Structure and Function. New York: Springer. ZOBEL, D. B., 1969. Factors affecting the distribution of Pinus pungens, an Appalachian endemic. Ecological Monographs, 39: 303-333.