Ann. Rev. Ecol. Syst. 1987. 18:431-51 Copyright © 1987 by Annual Reviews Inc. All rights reserved

TROPICAL RAINFOREST GAPS AND

TREE SPECIES DIVERSITY

Julie Sloan Denslow

Department of Biology, Tulane University, New Orleans, Louisiana 70118

INTRODUCTION

Evolutionary hypotheses about how so many species of tropical rainforest trees might have arisen include (a) genetic drift (71), (b) habitat specialization (8) in benign environments, or (c) repeated geographic isolation followed by remixing of species during Pleistocene climatic fluctuations (144). Ecological hypotheses about how these species continue to coexist are often cast into equilibrium or non-equilibrium frameworks: Do tropical forests comprise" . . . sets of highly coevolved niche-differentiated tree species in stable or semi­stable floristic assemblages," or do they consist of" .. . diffusely coevolved, broadly generalist species which slowly drift in relative abundance within a few large life-history guilds" (67, 102)? In this context, there has been considerable recent interest in the role of adaptations by species to different regeneration sites in structuring plant assemblages in general (83, 84, 86, 141), and tropical tree communities in particular (62, 89, 90, 150). The immediacy of this interest is

' heightened by rising rates of deforestation

throughout the tropics and a critical need for management strategies of the remaining preserves, for ecologically sound harvesting procedures, and for the tools with which to restore degraded forests.

Openings in the forest canopy are widely recognized as important for the establishment and growth of rainforest trees (5, 33, 62, 90). Hartshorn (89) suggests that perhaps 75% of the tree species at La Selva Biological Station, Costa Rica are dependent on canopy opening for seed germination or for growth beyond sapling size. Similar statements are found in descriptions of forest dynamics in Queensland, Australia (185), Malaysian dipterocarp for­ests (195), and West African rain forest (108). Demographic studies demon-

431 0066-4162/87/1120-0431 $02.00

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strate greater growth, survival, and reproduction when plants occur in or near canopy openings (32,35,36,42,49, 142, 158, 162). These examples include canopy, subcanopy, and understory species across the spectrum of shade­tolerant to light-demanding physiologies. Canopy openings clearly have an important influence on sapling growth, survival, and the probability that a tree will attain canopy stature (21, 33, 122, 152, 153, 189). Beyond this generalization, however, the patterns and processes by which fallen trees are replaced in the canopy are not well understood; current hypotheses fall between the following alternatives.

Occupancy of canopy space is determined in part by interactions among establishing saplings in the forest understory and within treefall gaps (11, 62,

90, 135, 150, 193). Habitats in the gap-understory mosaic represent a com­plex environment that varies temporally and spatially, partitioned among species exploiting different resources through physiological, morphological, and life-history adaptations (46). Species not competitively superior for some resources at least some of the time are eventually eliminated from the commu­nity (47, 66, 96).

Alternatively, community composition is seen as a function of chance and historical accident. Capture of canopy space is determined by the presence of seedlings and saplings in place when the gap is formed and is primarily a function of the relative abundance and distribution of this advance regenera­tion. Competitive interactions prior to or after gap formation are not thought to play an important role under this scenario. Like coral reef fish communities (155), species composition in tropical tree communities is largely determined by a lottery process (e.g. 95, 98, 100, 103, 104, 143, 195). Species diversity does not gradually decline as this model would predict (98) because (a) local extinctions are slow; (b) new species are continually added to the pool from outside (e.g. 98, 100); (c) disturbance rates are such that progression toward dominance by a few species is interrupted (55, 105); and/or (d) density dependent mortality rates prevent few-species dominance (48, 54, 57, 157,

160). This is in effect a null model for forest dynamic processes. These two schemes lie at the extremes of a continuum. Some species will

grow only in very large canopy openings (32). These species, however, account for only a small proportion of the tree flora in most tropical rain forests (64, 103). Most species have some degree of shade tolerance but also respond positively to canopy opening. Do these species finely partition environmental variation or does this guild comprise ecologically equivalent species? Likewise, the importance of advance regeneration in filling small gaps is well established (19, 149, 191), but the processes determining its composition are little studied. The central question remains, to what degree do adaptive specialization and competition among seedlings and saplings influence canopy occupancy?

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TROPICAL TREEFALL GAPS 433

To address this question, I first summarize recent information on the nature of gap-understory habitats in tropical rainforest environments and the patterns

of seedling and sapling growth. I then examine evidence regarding habitat specialization by tropical trees. These findings take two principle forms: (a) data on the distribution of adult and juvenile trees, and (b) data on the relative performances of similar species along gap-understory gradients.

GAP AND UNDERSTORY ENVIRONMENTS

Light

The immediate and perhaps most important effect of canopy opening is an increase in the duration and intensity of direct sunlight to lower strata of the forest (43). During a sunny day, the center of a large gap receives higher intensity radiation a greater proportion of the time than does the center of a small gap or the forest floor under closed canopy. Chazdon & Fetcher (44) estimated that the majority of 10 min averages of photosynthetic photon flux

density (PPFD) in a large (400 m2) gap were at intensities greater than 500 Mmol m -2 s -I. In contrast, most 10 min averages in a smaller clearing (200 m2) were between 100 and 200 Mmol m-2 S-I. Over 70% of the 10 min averages in the understory were below 10 /Lmol m-2 S-I. Total PPFD at the center of a gap is a function of gap size, shape, and orientation; local topography; and the height of the surrounding forest. The 400 m2 gap received about 20--35% PPFD of full sunlight in comparison to 9% full sunlight in a 200 m2 gap and 1-2% full sunlight in adjacent forest understory (44). Comparable measurements from understories of other rain forests range between about 0.4% (Queensland, Australia, 26; the Tai Forest, Ivory Coast, 4), 2.4% (Oahu, Hawaii, 138), and 3.0% (Pasoh, Malaysia, 6).

The low intensity diffuse radiation in the forest understory is deficient in photosynthetically active wavelengths (300--700 nm) (26). However, on a clear day, the majority of total PPFD in the understory is received as short duration, direct light in sunflecks-61-77% (44); 80% ( l38)-and plant growth rates are more closely correlated with the estimated amount of direct than diffuse sunlight received (130). At PPFDs typical of understory environ­ments, photosynthetic responses to increased light levels are steeply linear (27, 42, 114, 132, 133, 139, 159, 162), suggesting that small differences in light levels at the forest floor may have important effects on the carbon balance of seedlings. At seedling heights, measured PPFD is spatially hetero­geneous (42) and likely affected by the distribution of understory plants. At La Selva, large-leaved species in the families Cyclanthaceae, Palmae,

Araceae, Heliconiaceae, and Marantaceae are an important component of the

understory vegetation. The dense shade cast by such species may affect the abundance and distribution of tree seedlings (31, but see 121). The conse-

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quences of such heterogeneity in light availability will be greater for seedling than for sapling size classes.

Although the centers of large gaps generally receive more total PPFD than do the centers of small gaps, within-gap heterogeneity is high. Gap orienta­tion, gap-forest edge effects, and the presence of surviving trees and shrubs within the clearing area all modify local conditions. Total PPFD at the edge of a large gap may approximate that in the center of a small gap. Total PPFD in the centers and edges of four gaps (100-600 m2) in Costa Rica was measured at 8.6-23.3% full sunlight in gap centers and 2.8-11.1 % at the gap edges (J. S. Denslow, N. Fetcher, J. C. Schultz, B. R. Strain, P. M. Vitousek, unpublished data). Moreover, the light environments of saplings growing in the forest understory may be strongly influenced by oblique light from crown gaps that does not reach to the forest floor (49, 103). However, in general, differences in gap and understory light levels are less at small than at large gap sizes, at gap edges than at gap centers, and on cloudy than on sunny days. Direct measurements of light availability with PAR (photosynthetically active radiation), sensors (44), or simulations of direct beam radiation from canopy photographs (138) give better estimates of plant environments than approx­imations based on gap size or plant habitat.

Soil Nutrient Availability

Increased soil and air temperatures can be found in gaps (73, 160) associated with high PPFD and large quantities of leaf and wood litter, and these suggest that gaps should be hot spots of nutrient availability (e.g. 33, 135). However, comparisons of soil nutrient availability in recent gaps and under intact canopy have not demonstrated a strong pulse in nutrient enrichment in gaps smaller than about 300 m2 (137; 162; 178; c. Uhl, K. Clark, N. Dezzeo, P. Maquirino, unpublished). Consistent but small and nonsignificant differences in extractable P were detected in surface soils from the crown zones of recent (1-12 months after treefall) Costa Rican gaps. However, there were no detectable increases in soil N (178), and (in another study) there was no increase in the levels of NOTN, K, Mg, or Ca in soil water at 70 em depth (137). There were, however, increases in these nutrients in soil water samples from two gaps larger than 500 m2 (137). High N availability in the Costa Rican soils, rapid nutrient uptake by intact roots of standing vegetation, and rapid adsorption of P onto variable charge clays (168) may account for the absence of an important or sustained nutrient pulse in small gaps on these soils. In large gaps, only a small portion of the gap area is reached by the fine roots from surrounding vegetation, and more of the nutrients may be washed through the upper soil layers (137).

With the exception of nutrient poor subsoils brought to the surface by uprooted trees or animal activity, there does not appear to be important

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TROPICAL TREEFALL GAPS 435

variation in nutrient availability among microhabitats within gaps (crown zone, bole zone, gap edge) (177; 178; C. Uhl, K. Clark, N. Dezzeo, P. Maquirino, unpublished), nor is there any associated with the small gaps typical of many rain forests.

Soil Moisture

Moisture levels in the upper 10 cm of soil are consistently and significantly higher in gaps than in the adjacent forest understory (178). In Costa Rica these differences were present in small as well as large ( l1�OO m2) gaps and in both rainy and dry seasons. High moisture levels are likely associated with a lower transpirational load on the clearing soils.

GAP DYNAMICS

Gap Size-Frequency Distributions

To the degree that gap size is a good index of resources and microclimates, the gap size-frequency distribution of a forest can be a useful basis for comparing ecosystems. Brokaw (29) suggests that a gap should be measured as the areal projection of any canopy opening reaching within 2 m of the ground. This definition seems an unambiguous basis for comparing canopy topographies.· A more realistic estimate of resource availability may be the area in expanded gaps, i.e. that area of the surrounding understory affected by, but not directly under, the canopy opening; the area and resource charact­eristics of expanded gaps can be calculated from data on gap size, canopy height, latitude, slope, and exposure (37).

Important differences in gap size-frequency distributions among sites appear to be primarily due to variation in sources of multiple-tree gaps. Surveys at La Selva and Barra Colorado Island (neither of which is subject to hurricanes or landslides) suggest that most gaps (76% and 95% respectively) are <200 m2 in size, although a substantial portion of total gap area (>21 % at La Selva) may occur in gaps >400 m2 (30, 157). At San Carlos de Rio Negro, Venezuela, most gaps are < 100 m2; trees there are slow growing and small statured (171) and therefore make smaller openings in the canopy. The old growth forest on Barro Colorado has more large gaps (> 150 m2) than the second growth forest because the younger forest there has few large canopy trees or emergents (75).

Topographic and edaphic variation similarly may produce local variation in gap sizes and formation rates 079, 180). For example, forests on ridge tops buffeted by strong winds (e.g. 183) or on unstable soils are likely to have different gap characteristics than forests on more stable soils. At La Selva the mean gap area on two poorly drained sites was 104 m2 and 120 m2 in comparison to 87 m2 in an upland site on steeper topography (89, also see

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103). Very large gaps (gap diameter> canopy height) are more common in forests subject to large-scale disturbances (e.g. cyclones and hurricanes, 58, 188; elephants, 108; and landslides, 80). Tree species that have a high demand for light are a larger proportion of the flora in such forests (64, 65, 188, 192).

Forest Turnover Rates

In old growth forests, long-term monitoring of gap formation in permanent plots yields estimates of forest turnover rates (as the mean time interval between successive gaps) that range between 80 and 136 years. Thus, 0.7 to 1.2% of forest area converted to gaps each year (30, 89, 152, R. Lawton and F. E. Putz unpublished). Although they are scarce, available estimates of year-to-year (R. Lawton, F. E. Putz, unpublished) or within-site (89) varia­tion in gap formation frequencies on the same site are of the same order of magnitude as variation among sites.

Other bases for forest turnover estimates necessitate assumptions of un­known accuracy. For example, data from one-time surveys of gap size distributions may be used to estimate turnover if gap closure rates are known (e.g. 143, 157, 171). Closure rates, however, likely vary with gap size. Small-tree and branch-fall gaps close primarily through lateral canopy growth, whereas the tree canopy of large gaps is closed through both ingrowth and the upward growth of saplings. When a gap enlarges with the fall of bordering trees (103), not only is the spatial extent of the gap increased, but high light levels in the preexisting clearing are also prolonged. Although turnover rates based on single surveys should be interpreted with caution, most estimates fall within the same range as those from permanent plot data (except 143).

Permanent plot data on tree mortality are also used to estimate stand turnover rates (e. g. 112, 115, 117, 147, 165). These estimates are not equivalent to estimates made from gap formation rates, since gap size can be greatly influenced by the circumstances surrounding tree death. Trees that die standing produce very small gaps over an extended period of time, whereas the fall of a canopy emergent can open a gap sufficiently large for the establishment of high light demanding species. Forest turnover times based on tree mortality are about half those based on gap formation in the same area (30, 115, 117). Like gap-based estimates, comparability of turnover times in different forests depends on sampling protocol, in this case on minimum tree diameters since small trees may experience higher mortality rates than do large trees (e.g. 32, 35, 170, but see 117).

Striking similarities in turnover rate estimates among forest types as dis­parate as northern coniferous forest (91), eastern deciduous forest (154), tropical cloud forest (R. Lawton, F. E. Putz, unpublished) and tropical rain

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TROPICAL TREEFALL GAPS 437

forest raise questions about the usefulness of the gap-based turnover rate per se as an index of stand dynamics. Size-specific estimates of gap return times are better estimates of available resources, which will likely affect sapling growth and forest structure.

PATTERNS OF GROWTH AND MORTALITY

The patch of light created by a gap on the forest floor is an ephemeral one. With the growth of surviving shrubs and establishing saplings, light availabil­ity soon declines to levels that are no longer sufficient for germination of light-requiring seeds. Micrometerological measurements at seedling levels suggest that temperature and humidity return to pre-gap levels within two years of treefall (73). Growth rates are higher and mortality lower for plants establishing before or soon after treefall (32). Seedlings and propagules present at tree fall or establishing soon after treefall thus account for the majority of saplings surviving beyond the first few years. In Venezuela, advance regeneration accounted for 95% of all trees> 1 m tall surviving in small gaps after 4 yr (c. Uhl, K. Clark, N. Dezzeo, P. Maquirino, un­published). More shade-tolerant species, however, may be able to establish or survive as seedlings for a longer period of time (35).

Canopy opening triggers the germination of seeds present in the forest soil and the release of seedlings already established in the understory. However, the timing of establishment and sources of mortality vary among species of different light requirements. In many tropical tree floras, light-demanding species generally have smaller seeds than do more shade-tolerant species (76, 126). The small seeds of many light-demanding species are able to maintain dormancy for long periods of time in the soil under an intact forest canopy (45, 87, 93, 94, 120, except see 126), but they germinate in response to increases in incident radiation, in the ratio of red to far-red wavelengths, and in temperature (25, 34, 60, 88, 173, 174, 190). Current seed rain apparently accounts for only a small proportion of seeds germinating from forest top soils (45; c. Uhl. K. Clark. N. Dezzeo. P. Maquirino. unpublished; F. E. Putz. S. Appanah, unpublished). As might be expected, the sapling density of light­demanding, but not shade-tolerant species is strongly correlated with gap area (32). Seedling establishment on tip-up mounds is sparse-presumably due in part to low nutrient availability ( 178) and small soil stocks of viable seeds­and is confined primarily to species demanding high light (145. 148. 151). Survival of advance regeneration and seedling establishment are likewise sparse under the fallen crowns of new treefalls (C. Uhl, K. Clark, N. Dezzeo, P. Maquirino, unpublished).

In contrast, large-seeded, shade-tolerant species germinate in response to rainfall ( 12, 77, 79, 163) rather than canopy opening. Most treefalls also

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occur during the rainy season (30, 32). These species have shorter dormancy capacities as seeds (most germinating within 4 months of dispersal; 79; also see 126, 127, 191), but high shade tolerance as seedlings (24, 187). Since large seeds are not incorporated into the upper soil layers, they are more susceptible to herbivory and dessication than are small seeds, but they pro­duce larger, more persistent seedlings in low light environments (76, 97, 126). In contrast to light-demanding species, sapling density of shade-tolerant species is generally constant acroSS a wide range of gap sizes, suggesting that most were present as suppressed saplings in the understory when treefall occurred (32; 152; c. Uhl, K. Clark, N. Dezzeo, P. Maquirino, unpublished).

Mortality of seedlings, high in any case (48, 50), is likely lower in gaps than under intact canopy where mortality due to fungal pathogens is high, especially to small seedlings (13-17). Other sources of seedling mortality include falling litter (especially palm fronds, 172), ground foraging mammals (61, 110), and insect herbivory (48, except 23).

Leaf damage due to insect herbivores is most closely correlated with leaf tissue quality. Leaves high in N, protein, and water, and low in fiber, phenols, and toughness experience higher rates of herbivory than do tougher, low quality leaves (51, 52, 113). Young leaves suffer more herbivore damage than do mature leaves, and the short-lived leaves of high-light species are eaten more than are the tougher, long-lived leaves of shade-tolerant species (52, except see 125). For example, in Panama saplings of persistent, shade­tolerant species show significantly lower levels of herbivory than do saplings of high light-demanding species (51, 52). These patterns suggest that although herbivory levels should be higher in gaps than in the understory, the consequences may be less; plants growing in high-carbon gap environments may produce more phenols (125; I. T. Baldwin, J. C. Schultz, unpublished; but see 52) and may more easily replace lost leaf tissue (53). The extended availability of growth support from large endosperms may partially com­pensate for low photosynthetic rates in shade-tolerant plants (55, 63, 76, 96).

Gap size and light availability affect not only seedling establishment but also the survival and growth of saplings. Sapling stem densities begin to decline as gaps close and establishing saplings compete for space and re­sources (32, 78). Species requiring large gaps in particular suffer high mortal­ity in small gaps (35). In small gaps, the growth of shade-tolerant species declines as the gap closes (C. Uhl, K. Clark, N. Dezzeo, P. Maquirino unpublished). As in shade-tolerant temperate species, it is likely that these plants experience alternating periods of slow and more rapid growth as they are exposed to successive gaps throughout their lifetimes (38). Vigorous liana growth at the edges of large clearings may also retard growth and increase the mortality of slow-growing tree saplings (146, 191).

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TROPICAL TREEFALL GAPS 439

Physiological correlates of growth responses by high-light and shade­tolerant species have been reviewed elsewhere (20,21,22,28,92, 124, 140). In brief, tropical shade-tolerant species obtain a large proportion of their photosynthetic energy from short-duration, direct-beam radiation in the form of sunflecks (27, 42, 138). The photosynthetic apparlJtus of such species is able to respond rapidly to a sunfleck, often within seconds of exposure (27, 138). In shade-tolerant species this response is correlated with low con­centrations of carboxylase enzyme, low light-saturated photosynthetic rates, saturation at low-light levels, low respiration rates, low light compensation points, and generally slow growth even under favorable light levels (27, 140). Where comparisons are controlled for soil nutrient availability (85), specific leaf weights are lower and leaf longevities higher in shade-tolerant than in high Iight-ctemanding species (72, 124, 116). High rates of leaf production and leaf turnover in light-demanding species may facilitate rapid acclimation to increased light levels through production of sun leaves. At the light and temperature conditions of a large gap, the growth of shade-tolerant species is often inhibited (42, 140 except 114), seed germination diminished (129), and establishing seedlings injured (128).

HABIT AT SPECIALIZATION AMONG TROPICAL

RAINFOREST TREES

Data from Tree Distributions

Great tropical tree species diversity is associated with high spatial heterogene­ity in the distribution of species. With the exception of forests in extreme habitats (e.g. swamps) or those subject to frequent large-scale disturbances (cyclones and hurricanes, 58, 181, 188, 196; landslides, 80; river meanders, 74, 156), the slopes of species-area curves do not markedly decline at large sample sizes (e.g. 10, 68, 100, 111, 131, 136). The populations of most species are aggregated, often at more than one spatial scale (e.g. 7, 98, 99). Rare species are more likely to be clumped than are common species (101, 143) whose distributions are sometimes indistinguishable from random (e.g. 18, 101).

Large-scale pattern in species distributions is often associated with dis­turbance history or edaphic variation, such as physiography (7a, 9, 18, 99, 118, 194); soil depth, texture, or nutrient content (7a, 9, 18, 182, 184); drainage (l18, 184); and exposure to windthrow and canopy breakage (111, 181, 183, 187, 188). The associated environmental variation is sometimes impressively slight. Indeed, sampling sites are often chosen specifically for their apparent uniformity. For example, slopes on the upland portion of a 50-ha mapped plot on Barro Colorado Island ranged from 0-21 % and soil

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depths from 100 cm to <50 cm. The distribution of Poulsenia armata (Mig.) StandI. (Moraceae) is typical of species whose distributions coincide with the slight topography of thc area; it occurs commonly in one habitat (in this case on the slopes) and more rarely over the rest of the plot (e.g. on the upland flat area) (99). Similar species distribution patterns are described from the Old World tropics (7a, 18). Distribution boundaries are most sharply defined where soils are periodically flooded or drainage impaired (e.g. 118).

Other studies have been unable to document an association between species distributions and environmental pattern such as topographic or soil variation (111, 143, 160, 195). In some instances the sampling design was apparently insufficient to detect existing pattern (e.g. 143, 195), or other variables influencing vegetation structure confounded the environmental pattern (e.g. disturbance history, Il l ). In others, aggregations have no consistent associa­tion with obvious environmental variation. They are apparently related to the local regeneration history of the species, for example a single establishment event associated with a large clearing (80) or the establishment of poorly dispersed offspring in the vicinity of large parent trees (131). The latter pattern is especially characteristic of large-seeded, wind-dispersed diptero­carps (143) but is associated with other large-seeded species as well (17,98). The mosaic of canopy patches comprising trees in gap, building, and mature phases has been used to describe the spatial effects of treefalls on forest structure ( 134, 167).

Studies of rainforest spatial structure thus suggest that in topographically heterogeneous environments, the value of adult tree distributions for detection of species differences in regeneration requirements is limited to well-defined, large-scale phenomena such as landslides (80) or river meanders (156). Although the distributions of tropical trees are sometimes associated with relatively slight topographic and edaphic variation, habitat differences at the small scales typical of most rainforest gaps « 200 m2) are difficult to detect and to interpret in the distribution of adult trees.

Sapling distributions should likewise be used with caution to assess such gap-related phenomena as tree replacement probabilities, habitat requirements for regeneration, and the long-term stability of tree communities (e.g. 1, 98, 102- 104). With the exception of high light requiring species whose distribu­tions are restricted to large gaps, most rainforest trees are both shade tolerant and gap dependent. Their distributions are therefore unlikely to reflect present gap configurations. Moreover, the use of sapling abundances to estimate future forest composition assumes equal growth and survival rates among species, an assumption that is probably unwarranted (186). In the final analysis, long life spans of trees and high species diversity of tropical forests limit our ability to evaluate the compositional stability of rainforest com­munities (56).

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TROPICAL TREEFALL GAPS 44 1

Data from Comparative Studies of Species

The few detailed comparative studies of co-occurring species demonstrate considerable overlap in species distributions along gap-understory environ­mental gradients. Nevertheless, morphologically and ecologically similar species often show fine-scaled performance differences with consequences for their distributions and abundances--e.g. shrubs in the genus Piper (Piper­aceae), 81, 124; Amazonian palms, 109. The following are examples.

Chazdon (40-42) examined the patterns of photosynthesis, growth, and distribution of two understory palm species in Costa Rica. Asterogyne mar­

tiana Wend!. and Geonoma cuneata H. Wend! . ex Spruce are morphological­ly and physiologically similar dwarf palms with long, undissected leaves. Photosynthetic light response curves were characteristic of highly shade­tolerant species; photosynthetic rates at light saturation for shade-grown plants was 3-4 Momol CO2 m-2 S-I, and light compensation points were 3-4 J,l,ffiol m-2 S-I (42). Both regularly flowered and fruited in the understory although productivity increased at gap edges . However, Geonoma reproduced as smaller individuals « I m taJl) at lower light levels than Asterogyne (> 1.5 m tall as reproducing adults) (42). By virtue of a smaller leaf area, less investment in support tissue per unit leaf area, fewer pendant leaves, and less self-shading , Geonoma had a higher light interception efficiency and was thus able to grow and reproduce in more shaded environments than Asterogyne (41, 42).

In Hawaiian rain forest, the photosynthetic capacities of two understory

trees were similar at low light levels but diverged at high light levels. The compensation point of Euphorbiaforbesii Sherff (Euphorbiaceae, a C4 plant) was similar to that of Claoxylon sandwicense Muell. Arg. (Euphorbiaceae, a C3 plant), but Euphorbia had higher light-saturated photosynthetic rates and greater acclimation capacities. Both occupied similar habitats in the rainforest

understory , but Euphorbia was only able to reproduce in gaps or as large individuals in the upper strata of the forest. Claoxylon flowered and fruited as a small tree under intact forest canopy (138, 139).

At the other end of the spectrum, Brokaw (35) followed the growth and survival of saplings of three high light demanding species growing in tree fall clearings on Barro Colorado Island: Trema micrantha (L.) Blume (Ul­maceae), Cecropia insignis Liebm. (Moraceae), and Miconia argentea (Swartz) DC (Melastomataceae). All three required gaps for seed germination and growth to reproductive size and were common early colonists of large new treefalls. Careful monitoring over an 8-9-yr period following gap forma­

tion, however, revealed differences in shade tolerance and growth rates with consequences for the distribution of adults.

Saplings (> 1 m tall) of all three species appeared early following gap formation and accounted for the majority of saplings alive after 8 yr. The

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slower growing Miconia saplings recruited as late as 7 yr after gap formation,

whereas few Trema saplings entered the I-m-size class beyond the first year.

Cecropia was intermediate. Moreover, mortality of Miconia saplings in small gaps was less than that of either Cecropia or Trema. At the end of 8-9 years,

Trema survived only in those gaps larger than 376 m2; Cecropia occurred in gaps larger than 215 m2; and Miconia occurred in gaps as small as 102 m2. In

50 ha of mapped forest on Barro Colorado, ranked abundances of the three species paralleled their habitat breadths; Miconia was the most abundant and Trema the least, since it was able to survive in only about 5% of the clearings formed (30).

DISCUSSION AND CONCLUSIONS

Life-History Attributes in a Gap-Understory Mosaic

Seedling establishment and sapling growth of tropical rainforest trees and shrubs appear to be limited primarily by the total incident radiation and its temporal duration. Accordingly, the life-history characteristics of tropical rainforest species can be arrayed along a continuum characterized by patterns of light availability from high light requiring, shade-intolerant, ruderal spe­cies, through light-requiring species with some shade tolerance, to highly shade-tolerant, slow-growing species (103, 119, 169, 188, also 176). These categories conform roughly to the ruderal, competitive, and stress-tolerant categories of Grime (83), although in the present case the resource (incident light level) is disturbance related in all cases.

As in Grime's scheme, tropical ruderal species (RS) occupy relatively permanent open areas. Typical examples include large multiple treefall gaps;

river margins (74, 156) and abandoned agricultural land (70), whieh have a history of repeated disturbances; and severely disturbed habitats such as

landslides (80, 175). A continuous tree canopy is slow to develop on these sites because vegetation regrowth on depauperate soils is slow, seed stocks have been depleted through repeated grazing, burning, or loss of topsoil, and because species intolerant of repeated disturbance have been eliminated (2, 59, 169). Species occupying these habitats are characterized by traits classi­cally ascribed to pioneer species (e.g. 20,21). They have high light-saturated

photosynthetic and respiration rates, saturate at high light levels, and are shade intolerant. Seeds of RS have good dormancy capacity and forest seed stocks are also augmented by seed rain from deforested areas bordering intact forests (107). Within the gap mosaic of an old-growth forest, seedlings may germinate but not survive to reproductive size except in very large gaps. Hence RS are rare in most rain forests not subject to large-scale disturbance. Trema micrantha (187), Trema guineensis (3), and Vismia spp. (Guttiferae,

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169) are examples. Because RS are also likely to survive well on degraded soils, they are good species to use to establish a tree cover on degraded pasture or farm land.

Like RS, large gap species (LOS) require the high light intensities and temperatures of large gaps for germination and seedling establishment. Early

growth is rapid, and saplings are able to reach the upper forest strata during the lifetime of a single gap. This growth pattern may in part account for the scarcity of sapling size classes in these species and the absence of the classic "J" shaped size-frequency distribution in their populations (19, 89, 103, 111, 160). Light-saturated photosynthetic rates are high, but respiration rates are

low. LOS are thus plastic in their growth responses to varying light availabil­ity and able to tolerate lower light levels than do ruderal species. Populations of LOS are maintained through mUltiple treefall gaps or the fall of large­crowned emergent trees. They are thus more common in primary or very old growth forest than in secondary forest (75, I I I) and include many canopy or emergent trees described as long-lived pioneers�.g. Cavanillesia platanifo­

lia HBK (Bombacaceae), 89; Hampea appendiculata Standley (Stercu­liaceae), Dipteryx panamensis Record and Mell. (Leguminosae), 132; Mico­

nia argentea (Swartz) DC (Melastomataceae), 35. LOS are often components of secondary vegetation following logging, although they fail to survive severe or repeated disturbance. The combination of fast maximum growth rates, large adult sizes, and tolerance of a wide range of light conditions make these species good candidates for reforestation of cleared land that has not been severely degraded.

Small gap species (SGS) germinate in the understory or in small clearings. Saplings are able to survive understory light conditions owing to low respira­tion rates and low light requirements at saturation, but they are dependent on some canopy opening for substantive growth and reproduction. Ught satura­tion occurs at relatively low PPFD levels, and SOS grow slowly in even favorable light conditions. High light levels damage leaves and meristems in such a way that maximum growth is attained in small gaps or on edges of large gaps. Examples include Pentaclethra macroloba (Willd. ) Kuntze (Leguminosae) and Virola koschnyi Warb. (Myristicaceae), 132, 133; Agathis

macrophylla Mast. (Aracariaceae), 187; and many understory tree species, 119. Many valuable timber species fall into this group, and their stocks are rapidly being mined from old-growth forests. Commercial propagation of SGS is difficult because the seeds have poor storage capacities; reforestation strategies are largely based on the preservation of advance regeneration (130).

Only a small portion of the variation in sapling composition among gaps can be accounted for by gap-related environmental variation and differences in species establishment requirements. High species diversity, low pre-

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dictability of gap formation, small gap size, and temporal and spatial variabil­ity in propagule availability (especially SGS) all contribute to the high

sampling error. However, persistence largely may be assured if a species is competitively superior for some resource at least some of the time (46, 47).

The long life spans of most tropical trees (46, 119), the variable competitive

environments, and fine-scale differences in reproductive and regeneration

requirements increase the probability that such competitive superiority will occur with sufficient frequency to' maintain the presence of a species in a community.

SUMMARY

Several points are emphasized by this scheme and by the foregoing review. First, both amount and duration of light are important determinants of es­tablishment success. Tree speCies can be arrayed along a continuum of adaptive responses to the availability and duration of incident radiation.

Species and successional processes characteristic of very large clearings and repeatedly disturbed areas are different from those of large but shorter-lived gaps.

Second, most tropical rainforest trees are in some sense gap-dependent in that most depend for growth and reproduction on locally enhanced light levels and show positive growth responses to canopy opening (except see 188). Although some species are highly shade tolerant and growth-inhibited by high light levels, so far none has been described that grows best under an intact forest canopy.

Third, sources of mortality in gap and understory habitats are diverse. Although photosynthetic and growth rates are important components of spe­cies adaptations, patterns of resource allocation to herbivore and pathogen

deterrence, leaf structure and turnover, and the production and dispersal of seeds may have equally important consequences for the distribution and the long-term presence of the species in the community.

Finally, comparisons of closely related or ecologically similar species reveal performance differences associated with a gap-understory environmen­tal mosaic, although there remains much apparent overlap 'in regeneration requirements. Nevertheless, a scenario which couples adaptive diversification

with high temporal and spatial unpredictability in the distribution of both gaps and propagules .is consistent with much of the currently available data.

ACKNOWLEDGMENTS

I am grateful to A. Bradburn, P. Neal, and C. Uhl for critical comments on the manuscript, to J. Reed for bibliographic assistance, and to S. Appanah, R. Lawton, F. E. Putz, J. C. Schultz, and C. Uhl for permission to cite

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TROPICAL TREEFALL GAPS 445

unpublished manuscripts. This paper has profited from discussions with D. A. Clark, D. B. Clark, G. Orians, J. Schultz, P. Vitousek, and the researchers at the Estacion Biologica La Selva. Support for this work was provided by NSF

grants BSR-8306923 and BSR-8605106 to Duke University on behalf of the

Organization for Tropical Studies.

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