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Internal Heterogeneity of Gaps and Species Richness in Costa Rican Tropical Wet ForestAuthor(s): Aldo Brandani, Gary S. Hartshorn and Gordon H. OriansSource: Journal of Tropical Ecology, Vol. 4, No. 2 (May, 1988), pp. 99-119Published by: Cambridge University PressStable URL: http://www.jstor.org/stable/2559652 .

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Journal of Tropical Ecology (1988) 4:99-119. With 4 figures

Internal heterogeneity of gaps and species richness in Costa Rican tropical wet forest

ALDO BRANDANI*, GARY S. HARTSHORNt, and GORDON H. ORIANS

Institute for Environmental Studies and Department of Zoology, University of Washington, Seattle, WA 98195, USA

ABSTRACT. In Costa Rican tropical wet forest the distribution of seedlings of most tree species colonizing 51 tree-fall gaps is clumped, probably because of differences in the proximity of gaps to fruiting trees. Different gap zones (root, bole and crown) are more similar to one another, in terms of their species composition, than they are to other zones in the same gap. This non- random pattern is established soon after gap formation, indicating that mortality of young seedlings is both high and related to gap zones. Some tree species are strongly positively associated with one of the gap zones, whereas others are associated with the age of the gap at the time the census was taken or the species of tree whose fall caused the gap. Root zones are dominated by fewer species than are bole or crown zones. Results are consistent with the assumption that an initial random distribution of seedlings is quickly changed to a strongly non-random pattern by selective mortality of seedlings of different tree species in the different gap zones. The internal heterogeneity of gaps is probably one of the factors helping to maintain the high tree species richness characteristic of tropical wet forests.

KEY WORDS: Costa Rica, disturbance, diversity, gaps, La Selva, patchy environments, species richness, tree-falls, tropical forests.

INTRODUCTION

The fact that small areas of some tropical forests contain more species of most taxa than temperate forests stimulated the development of theories to explain latitudinal gradients in species richness. Some theories deal with the origins of the large numbers of species in the tropics (Baker 1970, Brown & Ab'Saber 1979, Dobzhansky 1950, Haffer 1969, Simpson-Vuilleuimier 1971). Other theories deal with the problem of ecological coexistence of large numbers of similar species (Clark& Clark 1984, Connell 1971, 1978, Connell & Orias 1964, Diamond 1972, Fleming 1973, Janzen 1970, 1971a, b, 1978, MacArthur 1965, 1969, Paine 1966, Pianka 1966). Among the factors that might help to explain coexistence of tree species is the environmental heterogeneity created by physical and biological processes. Perturbations are frequent in all parts of the tropics, and they differ in type, intensity, frequency, and predictability (White 1979). In tropical wet forests, the disturbance created by tree falls is known to Present addresses: * PO Box 722, Universidad Nacional de Mar del Plata, Mar del Plata, Argentina 7600. t Tropical science Center, Apartado 8-3870, San Jose, Costa Rica.

(99)



100 ALDO BRANDANI, GARY S. HARTSHORN AND GORDON H. ORIANS

be important for the regeneration of many tree species (Brokaw 1985, Harts- horn 1978, Knight 1975, Ricklefs 1977, Whitmore 1978). The scale of this particular disturbance type ranges from small openings created by the fall of single branches or trees, to large gaps produced by the simultaneous or sequen- tial falls of several to many trees. Still larger gaps are produced by major catastrophes such as hurricanes, landslides, earthquakes, and fires (Garwood et al. 1979).

Knowing that disturbances are important for seedling establishment does not, however, provide an explanation for tree species richness. What is required are processes that favour different phenotypes in different parts and sequences of the disturbance mosaic. In the absence of such processes a single, very suc- cessful invader could dominate those patches, depending on the rate of formation and predictability of disturbed patches and dispersal abilities of trees (Hartshorn 1978, Slatkin 1974). Some evidence of this possibility has been presented for other space-competing organisms (Paine 1969, Sutherland 1974).

Elsewhere, one of us (Orians 1983) presented a theory of how processes of tree-fall gap formation might enhance tree species richness. Orians proposed a three-part division of single tree gaps into root, bole and crown zones, each with strikingly different initial environmental conditions. Gaps also differ according to the species of trees that fell, the breakage mode, and in size and time of their formation. Heterogeneity within and among gaps may also be caused by selective uptake of minerals by individuals of different tree species which thereby differentially deplete soils in their root zones and selectively release nutrients when they decay. Such variability is yet to be conclusively demonstrated, but it is expected because tree species have wood, leaves, and fruits with different chemical compositions (Bultman & Southwell 1976, Pease & Macdonald 1981), and because the materials produced by trees that are typically deposited outside the root zone of their producer, such as nectar, pollen, seeds, and fruits, all differ markedly among species in their chemical compositions (Baker & Baker 1975).

Based on these processes, Orians (loc. cit.) postulated that germination and survival of seeds and seedlings should vary with gap zone, gap size, and species of trees that fell. In this paper we test these predictions, plus some additional ones that follow from the general theory, but which were not previously expli- citly formulated, with data gathered in 51 tree fall gaps in a tropical wet forest at the La Selva Biological Station, Costa Rica.

Predictzions Our basic postulate is that species composition, structure and characteristics

of the community of seedlings that colonizes gaps are influenced by environmental conditions found in gaps after the fall of a canopy tree. These general conditions probably differ systematically among the three zones of gaps in the following ways. In root zones, the soil is highly disturbed, much light reaches



Gaps and tree species richness 101

the bare mineral soil, existing roots are broken and torn from the ground, few seedlings survive the disturbance, and little or no nutrients fall into the zone. In bole zones, the soil, roots and existing understorey vegetation are largely undisturbed except where the bole lands. The bole is the primary source of nutrient input but those nutrients are released slowly as the bole decays. In the crown zones a large mass of leaves, branches and epiphytes smothers most seedlings and saplings growing there but also provides high levels of nutrients that are released relatively rapidly. We did not directly measure these attributes in our gaps, but for the present purposes, all that is required is that there are consistent differences among gap zones in conditions favouring germination and early survival of seedlings.

In this paper we test the following predictions: Differences in species composition. Seeds are probably not randomly distri-

buted over different gaps because seed rain depends on the proximity of the gaps to fruiting trees during the first months or years following its formation. However, seed deposition within gaps should be approximately random with respect to zone type, the number of seeds landing being a direct function of zone size. Moreover, seeds that arrived prior to formation of gaps should also be distributed randomly with respect to the eventual gap zones if a large number of gaps is sampled. If so, differences in species compositions among the zones of gaps would constitute strong circumstantial evidence of non-random sur- vivorship.

Dynamic differences. Initial colonizers of a gap encounter higher light levels and less competition from neighbours than do later arrivals. As individuals increase in size, the extent of their above and below ground interference with neighbours also increases. Therefore, species that do best as initial invaders of a gap zone may be competitively inferior to other species a short time later. As a result, successional changes are expected during the gap closure process. These changes should be more marked where disturbance is more severe, i.e. in root and crown zones, than in bole zones where disturbance is, in general, less (except where the bole lands). Such changes are best identified by following marked seedlings over time, but in our study we must infer possible changes by comparing species composition in gaps of differing age.

Differences in species richness and species density. Densities of seedlings, which depend on seed banks in the soil at the time of the tree fall and on subsequent arrival rates of new seeds, are likely to be highly variable. However, other things being equal, they should be positively correlated with nutrient levels and with the extent to which competition with established plants is reduced by disturbance caused by the fall of the tree. If so, seedling densities are expected to be higher in crown and root zones than in bole zones. Species richness of seedlings is expected to be highest in crown zones because these zones are generally larger than the other two and because they have high internal variability in patterns of nutrient inputs.




METHODS

Our data set consists of complete censuses of seedlings and saplings in 51 tree- fall gaps. No single gap was censused more than once, but gaps differ in age. Therefore, all conclusions we draw from our data concerning patterns in time are inferred from point samples. Such samples can provide powerful indirect evidence of underlying processes and can help identify those processes that are most likely to yield interesting results if they receive more time-intensive investigations.

Field methods. Our study site is the La Selva Biological Station (1330 ha) owned and administered by the Organization for Tropical Studies. La Selva is in north-eastern Costa Rica (10? 26' N and 83? 59' W) where the physio- graphy changes from the steep foothills of the Central Volcanic Cordillera to the extensive coastal plain. Elevations range from 35 to 135 m, with short, steep slopes up to 60%. Approximately 64% of La Selva is primary forest, dominated by the mimosoid legume Pentaclethra macroloba, with importance values of 18-23% (Hartshorn 1983). Despite such dominance, the La Selva primary forest averages 96 species per hectare for trees and lianas 10 cm or more in diameter at breast height (Lieberman et al. 1985). More detailed site, soil and vegetation descriptions are found in Bourgeois et al. (1972), Frankie et al. (1974), Hartshorn (1983), Holdridge et al. (1971) and Lieberman et al. 1985).

In April 1978 we censused the 51 study gaps to record seedlings (<50 cm in height) and saplings of tree species in root, bole and crown zones. For each individual seedling or sapling we recorded its species, size, and zone of the gap, i.e. root, bole or crown, in which it was growing. We also determined if it was already present at the moment of gap formation, i.e. a survivor, or if it was a subsequent colonizer. A seedling or sapling was judged to have been a survivor if it showed signs of having been bent or broken by objects falling on it and if it was too large to have reached its size in the time available since the formation of the gap. Boundaries between gap zones were determined from patterns of disturbance and location of parts of the tree that fell. The limit between root and bole zones was taken as an imaginary line running at right angles to the juncture of the bole and roots of the fallen tree. The boundary between bole and crown zones was taken as a line crossing the bifurcation point of the lowest crown branch of the tree. The gap border was defined as the edge of the canopy opening or the edge of disturbances created by the tree fall. If the crown of the fallen tree swung under the intact canopy, the zone where the crown fell was considered part of the gap even though the canopy was above it.

Analytical procedures. From our census of gaps, we obtained information about the size of each gap zone, the numbers of seedlings and saplings of each tree species in each gap zone, and which of those individuals appeared to have survived the fall of the tree and which had germinated thereafter. We grouped




the data in several different ways, each pertinent to a different set of predictions.

Pooled analysis. Each gap zone was considered a separate sample unit. Sample size was 140 units rather than 153 (51 gaps X 3 zones each) because not all gaps had three zones. We pooled these units by zone type to establish whether root, bole and crown zones could be differentiated based on the abundance of colonizing species.

Zonal analysis. The units were grouped into three subsets, each consisting of all root (N = 42), bole (N = 47), and crown (N = 51) zones respectively. Analyses were performed to compare species compositions between and among gap zones and to determine the influences of features of the zones such as their size, and abundance of colonizing species.

Gap-by-gap analysis. Each gap was treated as a unit, yielding a sample of 51 units. This allowed us to study major colonization patterns as functions of gap size, age, or adult species that fell, regardless of internal heterogeneity of the gaps.

RESULTS

Pattern of gap formation Most gaps at La Selva are formed by the fall of a single canopy tree. Incom-

plete gaps, formed by breakage of the bole or a large branch, are less frequent, smaller, and lack root zones. In some cases adjoining trees fell a few months after the initial gap, enlarging the gap and sometimes superimposing one zone on another. One of our sample gaps was formed by the fall of two trees of different species. In this case we added together the areas of the zones of each of the fallen trees to yield one composite gap.

The causes of gap formation are varied (Brokaw 1985). Weak soil structure, high rainfall, superficial rooting, and prevalence of heavy epiphyte loads (Strong 1977) are important, especially during storms or periods of strong winds. Indeed, at La Selva, most gaps are formed during wet seasons (Table 1) as is the case in many wet-forested areas (Brokaw 1985). Hartshorn (1978) calculated a turnover rate of 118 ? 27 years for the virgin forest on the La Selva plots. This is comparable to turnover rates calculated for other Neo- tropical forests: 104 years for tierra firme forest in Amazonian Venezuela (Uhl Table 1. Seasonal distribution of gap formation at La Selva from 1970-1976 in relation to rainfall. The wettest periods of the year are indicated by '*'. Mean monthly rainfall averages calculated from daily data collected and provided by OTS.

Months: June* July* Aug.* Sept. Oct. Nov.* Dec.* Jan.* Feb. Mar. April May

27 yr mean 440 503 396 324 355 429 426 275 175 156 220 328 rainfall (mm)

Mean rainfall 441 529 369 376 294 434 446 318 193 128 204 292 (7 yrs) 70-76

Number of gaps 7 7 2 0 1 3 9 18 3 0 0 1




& Murphy 1981); 114 years for old forest on Barro Colorado Island, Panama (Brokaw 1982).

Of the 32 gaps for which we know the identity of the principal canopy tree, 21 were caused by Pentaclethra macroloba (Wild) Kuntze (Mimosaceae), the dominant canopy tree in the La Selva primary forest. Two gaps were formed by Dipteryx panamensis (Pitt.) Record (Fabaceae), and one gap each was formed by Apeiba membranacea Spruce (Tiliaceae), Ocotea hartshorniana Hammel (Lauraceae), Pterocarpus hayesii Hemsl. (Fabaceae), Tabernaemon- tana arborea Rose (Apocynaceae), Veconcibea pleiostemona (D.-Sm.) Pax. & Hoffm. (Euphorbiaceae), Aspidosperma megalocarpon Muell.-Arg. (Apocyna- ceae) and Jacaratia costaricensis I. M. Johnston (Caricaceae). Interestingly, the last two species are very rare in La Selva (Hartshorn & Poveda 1983) and were not found as seedlings in these 51 gaps. We found seedlings of 273 tree species in these 51 gaps, approximately 87% of the total number recorded for La Selva in 1978.

General patterns among gaps. Data on sizes of gap zones, age of gaps (from date of formation to date of inventory), total numbers of species and individuals, and diversity of survivors and colonizers are summarized in Table 2. Complete data on sizes of individual gaps, numbers of species and individuals found in them and the numbers of individuals of each species found in each gap zone are available from the authors on request. As shown in Table 2, crown zones are the largest and root zones the smallest parts of gaps. Nonetheless, the zones overlap in size so that the largest root zones are larger than the smallest crown zones. Crown zones are the most variable in size, measured both as total size range and variance.

There is no reason to expect understorey seedlings and saplings to be distributed other than at random with respect to where the different gap zones will be formed, but probability of surviving the tree fall is greater in bole zones than elsewhere because of the lack of disturbance except where the bole falls. Even here, however, more species were recorded as colonizers than as survivors, and overall more than four times as many individuals were colonizers than survivors (Table 2). Thus, at La Selva the community that recolonizes gaps develops primarily after the gaps are formed. Our hypotheses are directed toward the effects of conditions after gap formation and how they may affect survival of colonizing individuals, and our analyses are confined to colonizing individuals.

Species richness and species density. The absolute number of colonizers is highest in crown zones and lowest in root zones, but densities are the reverse. We examined abundances as functions of size of gap zones using four different models:

(a) linear: Y= a+ bX (b) exponential: Y= aebX

(c) potential: Y=aXb (d) log Y-log a + b log X




Table 2. Pooled data on 51 gaps, gap zones, and seedlings and saplings found in them. Sample sizes, enclosed in parentheses, do not always equal 51 because of missing data, incomplete gaps, or because there were no seedlings or saplings in some zones.

Root zone Bole zone Crown zone Total

Age: range 13-197 (51) average 60 (51)

Area (mi): range 2-66 (42) 15-471 (46) 16-735 (51) 25-1273 (51) average 11.5 (40) 74.3 (41) 103.0 (49) 177.4 (51) Standard Deviation 12.5 (40) 82.0 (44) 125.9 (49) 205.0 (51) total 465 (40) 3021 (44) 5048 (49) 9047 (51)

Survivors Number of species:

range 0-5 (42) 0-27 (46) 0-35 (51) 2-65 (51) average 1.2 (42) 8.7 (46) 6.5 (51) 3.4 (51) total 42 (42) 119 (46) 142 (51) 174 (51)

Number of individuals: range 0-6 (42) 0-45 (46) 0-45 (51) 5-170 (51) average 1.4 (42) 12.4 (46) 10.1 (51) 23.5 (51) total 72 (42) 614 (46) 513 (51) 1199 (51)

Number of individuals m-2: 0.1 (42) 0.2 (46) 0.1 (49) 0.1 (51) Diversity* 0.67 (27) 19.7 (46) 1.56 (49) 1.40 (51)

Colonizers

Number of species: range 0-26 (42) 0-71 (46) 6-96 (51) 16-124 (51) average 6.5 (42) 17.6 (46) 25.1 (51) 45.5 (51) total 113 (41) 204 (46) 223 (51) 253 (51)

Number of individuals: range 0-69 (42) 0-308 (46) 10-496 (51) 22-873 (51) average 12.5 (42) 47.3 (46) 67.3 (51) 127.0 (51) total 637 (42) 2412 (46) 3424 (51) 6478 (51)

Number of individuals m72: 1.5 (40) 0.7 (46) 0.7 (49) 0.7 (51) Diversity* 1.58 (40) 2.34 (46) 2.63 (51) 2.20 (51)

* Measured using Brillouin Index: H = 1/n log (n!/n1 !n2 ! . . . ns) where: n = total number of individuals, n1, n2 . . . ns= number of individuals of species 1, 2, ... s. Sample size is the total number of zones with at least one individual.

In each equation X is the area of the gap zone and a and b are parameters. These models are frequently used to measure species-area and individual-area relationships, with Y representing the number of species or number of individuals. The best fit (P<0.01) to our species-area data was obtained using the potential model for all three gap zones (Figure 1). Root zones, although smaller and with fewer species, have the highest number of species per unit area. The individual-area relationships for root and crown zones are at best approximated by power functions while a linear relationship holds for bole zones (P<0.01, Figure 2). This difference might be due to rapid colonization of the highly disturbed root and crown zones, leading to the great densities recorded there. Power functions reflect saturation of available space by colonizers, probably




70 o-0oROOT ZONE

BOL E ZONE 60 -*--.CROWN ZONE

(/) 50-

40 -

40 80 120 160 200 240 280 320 360 400

AREA M2

Figure 1. Species-area relationships for root, bole and crown zones. The best fit models, all power functions, are presented.

240

o-o ROOT ZONE

<200 B BOLE ZONE

- CROW/V ZOWE

16 0

~80-

40

0 40 80 120 160 200 240 280 320 360 400

AREA M 2 Figure 2. Abundance vs size in each gap zone, together with the best fit mnodels.




20- *- ROOT ZONE (a)

A BOLE ZONE

10 CnRaCROWN ZONE

_j 8-

6-

<2-

0

ww

5 0o 5 20 25 30

ABUNDANCE RANK Figure 3. Plot of the abundance of colonizing species with more than 1%o of total abundance vs rank. (a) All species; (b) same as (a) after eliminating the three dominant species (see text).

because highly disturbed zones provide better conditions for regrowth. It follows that, in an environment saturated by colonizers, interference among seedlings is high. In bole zones, on the other hand, disturbance is low and the density of colonizers is also low. Hence, little interference occurs among bole zone colonizers, allowing abundances to rise linearly with zone area.

The distributions of abundances of colonizing species in all three gap zones are shown in Figure 3a. Root zones tend to be dominated by fewer species than are bole or crown zones. For instance, it takes only nine species to exceed 50% of the total number of individuals in root zones, whereas 14 species are needed in crown zones to reach a similar value. Although the majority of species is represented by no more than a few individuals in our sample, three species are notably abundant and widespread; Anaxagorea crassipetala Hemsl. (Anno- naceae), Pentaclethra macro loba and Welfia georgii Wendl. (Palmae) are found in 33, 49 and 49 gaps, respectively, and together they comprise over 31% of all individuals counted. If these species are excluded (Figure 3b), concentration of dominance among the remaining species in root zones is almost double that in bole or crown zones. Hence, fewer species are common under root zone conditions than under bole and crown zone conditions. Nonetheless, colonizers of




root zones are found at the highest densities, indicating that conditions are generally suitable for seedling establishment.

Occurrence of species in different zones of a single gap Differences among gap zones in densities of individuals and species richness

of colonizers do not, by themselves, indicate whether species are non-randomly distributed among zones. The patterns we have so far shown could be the result of factors influencing success in germination and survival that affect all species equally. If germination and survival of seedlings of all tree species were random with respect to gap zone, we would expect that: (1) zones within a gap will have individuals of each species present in numbers proportional to the size of the zones , and (2) zones within a gap will be more similar to one another in species composition than a zone of one gap is to the same zone in another gap. The opposite pattern would constitute strong evidence of differential establishment or mortality of species in different gap zones.

Of the 253 tree species we found as colonizers, 64 (27%) occurred in only one of the three zones. Of these, 41 species were represented by a single individual only and, hence, could have been found in only one zone. Ninety-two (36%) species were found in two zones, 16 of which are represented by only two individuals, while 9 7 species (3 7%) occurred in all three gap zones. Although the number of species found in only a single zone is positively correlated with the total area available for colonization in each zone type (see Table 3), this is not true for species found in more than one gap zone. However, it is inappro- priate to use the entire sample for an analysis of distribution because the total sample is dominated by rare species (91 species out of 253 are represented by three or fewer individuals). Therefore, we performed an analysis using only the 30 most abundant species, each with at least 51 colonizing individuals, represented Table 3. Actual and expected distribution of the 30 most common tree species within gaps. Expected values are calculated assuming that species had been distributed randomly among zones of the gaps in which they occurred.

Young (< 36 months) Old (> 36 months) All

Random Actual Random Actual Random Actual

Age of gap N %0 N % N % N % N % N %

Found in: Root zone 0 0 12 5.1 0 0 20 4.9 0 0 31 4.8 Bole zone 24 10.3 54 23.1 54 13.3 46 11.3 78 12.2 100 15.6 Crown zone 59 25.2 57 24.4 140 34.5 190 46.8 199 31 247 38.6 Root +bole 0 0 13 5.6 0 0 15 3.7 0 0 29 4.5 Root + crown 0 0 1 1 4.7 1 0.2 16 3.9 1 0.2 27 4.2 Bole +crown 112 47.9 56 23.9 167 41.1 79 19.5 279 43.6 135 21.1 Root +bole + 39 16.7 31 13.2 44 10.8 40 9.8 83 13 71 11.1

crown

Totals 234 234 406 406 640 640

X'= 395.8 X'(= 254.3 2282




in our samples. Our procedure was to use the actual number of individuals of each of these species found in each gap in which it occurred as a base for pre- dicting an expected distribution if those individuals had been distributed randomly among the zones of those gaps. The expectations were calculated according to the actual sizes of the three zones in each gap. If a species did not occur in a given gap, that gap was not used for calculating the expected distribution of that species. These expected abundances for each species were then added together to yield a composite expected distribution of individuals among the zones. That is, we obtained a distribution of the number of individuals expected to occur in every zone in all combinations of zones in the gaps in which the species was actually found. A simple numerical example using two species and three gaps is shown in Appendix A. The expected number of individuals was rounded to the nearest integer. The null model we use is that individuals of each species are distributed in proportion to zone size. Thus, for very small zones (e.g. root zones) expected values may be zero.

The results of this analysis using actual data are shown in Table 3. Several predictions generated by a hypothesis of zone-specific mortality rates for different species are supported by the data. Specifically, there are too many cases in which a species is found in only one zone of a gap and too few cases in which a species is found in all three zones of a gap than expected if individuals were randomly distributed among the gap zones, adjusted for differences in sizes of the zones. Non-randomness is most marked in root zones where soils are highly disturbed and where high seedling densities should lead to stronger competition for light than is the case elsewhere. Finally, differences increase with age in crown zones, in accordance with the delays in seedling establishment caused by the presence of large amounts of debris in that zone.

Several other patterns not predicted by our hypotheses are shown by these data. For example, there are too many species found in root and bole zones only and in root and crown zones only. In both cases the effect decreases with time. In these two cases, the predicted numbers are small due to the small sizes of most root zones, and the statistical effect we found in our sample is due to a strong initial bias in the distribution of seedlings in root zones. In addition, there are far too few species found in bole and crown zones only, and this pattern is strong in gaps of all ages. The general pattern may be the result of the striking differences between bole and crown zones in conditions for seedling colonization. Studies through time with marked seedlings are needed to test this idea.

Most of the species included in this analysis (24 of 30) are over- or under- represented in one or more zones (Table 4). The most common pattern is for a species to be over-represented in the root zone. Usually, this is associated with under-representation in one of the other zones. The species in this table are the ones that will be subjected to special analysis to test whether the morpholo- gical features predicted to confer success in each of the zones (Orians 1983) are, in fact, associated statistically with over-representation in that zone.




Table 4. Actual and expected number of individuals in each gap zone for the 30 most common tree species in our sample. Expected numbers were calculated based on actual size of gap zones of gaps where each species was present. Small differences in total number of individuals between actual and expected figures is caused by rounding to the nearest integer. The significance of differences between actual and expected values was tested through a x2 test with P=95%. The zones where over-representation and under-representation of individuals are statistically significant are also indicated, (*) indicates significant differences by the x2 test (P >95%). For species with zero individuals expected in root zones, a value of one was assumed for x2 calculations.

Root zone Bole zone Crown zone Representation

Species Actual Expected Actual Expected Actual Expected x2 Over Under

Ocotea atirrensis 7 1 13 17 31 33 37.1* Root None Guarea rhopalocarpa 3 1 18 20 30 30 2 - - Cecropia obtusifolia 5 1 14 20 33 30 18.1* Root None Cassipourea elliptica 5 0 19 22 31 34 16.7* Root None Faramea suerrensis 2 2 20 16 33 36 1.2 Dipteryx panamensis 4 2 19 19 38 37 1.4 Simarouba amara 10 2 14 25 34 35 36.9* Root Bole Perebea angustifolia 2 1 24 27 39 36 1.6 Parathesis chrysophylla 4 0 4 5 57 59 9.3* Root None Ampelocera hottlei 4 2 6 26 58 39 6.5* Crown Bole Virola sebifera 3 0 27 22 38 46 6.5* Root Crown Guatteria inuncta 7 1 24 29 41 43 37.0* Root None Apeiba membranacea 19 1 32 24 23 40 333.9* Root, Crown

bole Castilla elastica 3 4 9 27 63 44 20.4* Crown Bole Pourouma aspera 6 2 20 26 50 48 9.5* Root None Rauvolfia purpurascens 3 4 47 29 26 43 18.1* Bole Crown Casearia arborea 20 2 28 33 34 46 173.3* Root Crown Miconia multispicata 13 2 29 35 43 48 62.1* Root Bole Virola koschnyi 9 1 30 35 50 52 64.8* Root None Inga thibaudiana 13 4 31 35 47 51 21.0* Root None Guarea bullata 10 3 28 36 62 61 18.1* Root Bole Rinorea pubipes 13 2 37 36 62 74 62.5* Root Crown Hampea appendiculata 5 4 37 42 75 71 1.1 Prestoea decurrens 3 5 57 47 67 75 3.8 Goethalsia meiantha 11 6 57 48 70 82 7.6* Root, Crown

bole Laetia procera 41 7 59 51 38 79 187.7* Root Crown Socratea durissima 28 7 72 91 116 119 67.0* Root Bole Welfia georgii 67 22 190 204 303 333 95.7* Root Crown,

bole Anaxagorea crassipetala 72 35 345 223 192 352 178.6* Root, Crown

bole Pentaclethra macroloba 57 54 365 325 459 503 8.9* Bole Crown

Species composition of gap zones. To test our prediction that species compositions of gap zones of one type are more similar to one another than expected if species were randomly distributed, we analysed distributions of only those 104 species represented by 10 or more individuals. This reduces the number of gap zones in the sample to 137. To test whether different gap zones differ in species composition, we treated each zone as an independent sample unit. The 137 units were than classified into three groups on the basis of the abundances of the 104 species in them. These groups were analysed to determine if they actually corresponded to gap zones, using a x2 test where classifi-




cation of units by zone type was the 'expected' distribution and the clustering using actual abundances of colonizers was the 'observed' situation.

To classify the groups, we used clustering analysis and Multiple Discriminant Analysis. For both methods we tested final differences by introducing colonizing species in direct and stepwise calculations (Nie et al. 1975, Pielou 1977, Zenio & Simmons 1981). The results obtained with both methods were essen- tially equivalent. Therefore, we confine our discussion to the results of the Multiple Discriminant Analysis (MDA) because it provides precise statistics for evaluating the results.

The result of this MDA (Figure 4) shows that three different groups are clearly separated by the first and second discriminant scores of each unit. Centroids are well separated and very little overlap exists among the units belonging to each group, clearly illustrating that species abundances are significant variables for the discrimination of units. Moreover, in 94.9% of cases, a zone sample was clustered with others from the same zone type (X2 = 233.6, P >0.99).

-5.0 -2.5 0 2.5 5.0 50 p 150

3.75- - 3.75 I I 13

I I I N 2.5- 1 -2.5

k ~~~~~~111 :1

(, 1.25- 1 1 1 3 3 -1 25 J 3 33 3

i. 3 3 33 ZZ 0 - 2 3 22 33 33 33 3 33

2; 3 3 3 3 223 2 3 3 3 3

2 12 Z -1.25 - 2 2 3 1.25

2 2

2 2 2 2 22 20W2

-2.5 2 2 3 -2.5 2 22

22 2 22 2 2

2 2 2

-3752 2 -3.75 2 2 2

2

-5.0 - , -5.0 -3.75 -1.25 1.25 3.75

DISCRIM/NANT SCORE / Figure 4. Plot of the two scores from discriminant analysis for each gap zone. (1) Root zones, (2) bole zones, (3) crown zones. Solid circles indicate the centroids of each cluster of zones. Ninety-five per cent of the zones were correctly classified as being root, bole or crown zones by the discriminant analysis based on recolonizing species composition (x2= 233.6).




These results are not artifacts of differences in the sizes of the zones because, if size were the only factor affecting species distribution, units of similar size would cluster together regardless of their topographical position within gaps. This is clearly not the case even though there is substantial overlap in sizes of individual gap zones of the three types (Table 2).

The MDA results are particularly interesting because different zones within a gap are close to one another in space and were formed at the same time. Never- theless, based on their seedling compositions, samples from the same zone type are grouped together even though they are separated in space and in the time of their formation. Evidently, the environmental features shared by zones of a given type affect germination and survival strongly enough to override the influence of spatial and temporal contiguity that should result in similar species compositions among zones of a single gap.

Factors affecting the distribution of species within gaps We have shown that colonizing species are heterogeneously distributed within

gaps, and that gap zones differ in species composition. To investigate which of the three factors for which we have data (gap age, gap size, and species of tree that fell) most strongly influence the colonization patterns in each zone type, we performed a canonical correlation between our set of independent variables (the three factors) and the set of dependent ones (the abundances of the 104 colonizing species). A more detailed description of these calculations can be found in several statistical texts (e.g. Pielou 1977, Orloci et al. 1979).

The species of tree that fell as an independent variable was transformed into a binary variable: gaps formed by P. macroloba vs. gaps formed by some other species because, whereas 21 gaps were formed by the fall of Pentaclethra macroloba, most other species contributed only a single gap, and we did not know what tree formed 19 of the gaps.

The canonical correlation was performed for each gap zone and, because we have three independent variables, up to three pairs of canonical variates are possible. The results show that the first, second and third independent canonical variates are most highly correlated with different factors for each zone: root and age; bole and size; crown and species (Table 5). The significance of each canonical variate is produced by a sub-set of species whose abundances are correlated, positively or negatively, with each factor (Table 6). Twenty-four colonizing species show a direct correlation with zone size in at least one zone type.

Within root zones, some species, such as Apeiba membranacea, are more abundant in older gaps, while others, such as Guarea rhopalocarpa Radlk. (Meliaceae) and Faramea suerrensis Donn.-Smith (Rubiaceae), are more characteristic of younger gaps. An analogous situation is found among bole zones, although the species characteristic of young and old gaps, respectively, are not the same as for root zones (Table 6). In addition, more species are over-represented in young gaps than in older ones, especially in crown zones where no species is




Table 5. Canonical correlation coefficients for each zone type between first, second and third canonical variates (linear functions of recolonizing species abundances) and gap factors: Age: Age of gap; Size: Size of gap; Species: Species that formed gap.

New dependent variables (canonical variates)

Independent variables Zone (gap factors) type First Second Third

Age Root 0.874* 0.484 0.041 Bole 0.441 -0.294 0.848* Crown 0.195 -0.166 0.967*

Size Root 0.596 0.791* -0.135 Bole -0.843* 0.061 -0.534 Crown 0.137 -0.948 -0.288

Species Root 0.031 -0.381 -0.924* Bole -0.067 0.978 -0.199 Crown -0.997* 0.059 0.047

* Indicates significant correlations (P < 0.05).

particularly common in older gaps. Moreover, species characteristics of younger crown zones are more common in older root zones than in younger ones. Taken together, these results suggest that early colonizers are replaced by seedlings of other species, especially in root zones, whereas in crown zones early colonists decrease in abundance without being replaced by individuals of other species. These results indicate that late colonizers of root zones may play a more important role in canopy closure processes than do late colonizers of other zones.

Different species are positively associated with root and crown zones of gaps formed by the fall of different tree species (Table 6). Of the two types of gaps analysed, the non-Pentaclethra (NP) gaps have more tree species that are over- represented in either root or crown zones than do the Pentaclethra (P) gaps. Within the same gap type, no species is significantly over-represented in both root and crown zones. In addition, canonical correlation results show no association between colonizers and bole zones of either group of gaps.

These results are consistent with the view that selective withdrawal of nutrients from the root zone of a growing tree alters the composition of the soil in a species-specific manner. For the same reason, the large quantities of branches and leaves that fall into a crown zone create conditions specific to the species of tree that fell. In the bole zone, however, no conditions are specifically related to the tree that fell because the zone may lie outside the major area where the roots of the tree were extracting nutrients and, except where the bole itself lands, there is little nutrient input from tissues of the fallen tree. If we had longer term data on associations of seedlings with the bole itself and immediately adjacent to it, we might be able to detect an effect of the species of tree that fell in the bole zone too, but our data are not adequate to test this possibility. Similar arguments may apply to microfloral associations.

Conditions found within each zone type of P-gaps should be relatively uni- form because the same species of tree contributes both to nutrient depletion of




Table 6. Colonizing species whose abundances are significantly correlated with the gap factors. Factors are: Size, size of each zone; Age, age of gap; P and NP, gaps formed by the fall of Pentaclethra macroloba and by the fall of some other species respectively. '+' indicates a positive correlation, '-' indicates a negative correlation.

Gap zone

Gap factor Root zones Bole Crown

Guarea bullata Guarea bullata Guarea bullata Brosimum lactescens Brosimum lactescens Brosimum lactescens Casearia arborea Casearia arborea Hernandia didymanthera Hernandia didymanthera

Dendropanax arboreus Dendropanax arboreus Faramea suerrensis Faramea suerrensis Cassipourea elliptica Cassipourea elliptica Colubrina spinosa Colubrina spinosa Dichapetalum donnell-smithii Dichapetalum donnell-smithii

+ Croton schiedeanus Croton schiedeanus Size Guatteria inuncta Guatteria inuncta

Pentaclethra macroloba Anaxagorea crassipetala Hampea appendiculata Jacaratia dolichaula Nephelea mexicana Hernandia stenura Capparis pittieri Guarea rhopalocarpa Cecropia obtusifolia

Cordia nitida Faramea talamancarum Cryosophila albida Hymenolobium pulcherrimum

- none none none

Apeiba membranacea Faramea talamancarum none Casearia arborea

+ Cephaelis elata Goethalsia meiantha

Age Hedyosmum scaberrimum

7 Guarea rhopalocarpa Goethalsia meiantha Apeiba membranacea Faramea suerrensis Jacaratia dolichaula Casearia arborea

Colubrina spinosa Cephaelis elata _ ~~~~~~~~~~~~~~~Cecropia obtusifolia

P gaps Socratea durissima Guarea grandifolia Hernandia didymanthera none Euterpe macrospadix

Castilla elastica Dendropanax arboreus Cecropia ob tusifolia Colubrina spinosa Guarea rhopalocarpa none Croton schiedeanus Simarouba amara Cryosophila albida

NP gaps Guatteria aeruginosa Hernandia didymanthera Alchornea costaricensis Guarea bullata Anaxagorea crassipetala Capparis pittieri Hampea appendiculata Brosimum lactescens

_ Laetia procera Faramea talamancarum

the root zone and nutrient enrichment of the crown zone. In NP-gaps, however, each of many different species of trees contributed its own pattern of nutrient withdrawal and enrichment, and more species are significantly associated with one of the gap zones than is the case with P-gaps. The fact that no species is over-represented in root and crown zones of both types of gaps suggests that Pentaclethra may be unique in the way in which it affects the mineral nutrient




Table 7. Number of tree species falling in each class of Patchiness Index values (P) calculated for those species for which ten or more individuals were recorded.

Patchiness values (P) Percentage of species

0.0 - 0.5 5.8 0.51- 1.50 23.1 1.51- 3.50 27.9 3.51- 5.50 16.3 5.51- 7.50 5.8 7.51- 9.50 5.8 9.51-11.50 2.9

11.51-13.50 1.9 13.51-15.50 1.9 15.51-17.50 1.9 17.51-19.50 1.9 19.51-21.50 1.0 21.51-23.50 1.0 23.51-25.50 1.0 25.51- + 1.9

composition of its root and crown zones or in its microfloral associations. Interestingly, the most abundant species in our total sample, including Penta- clethra itself, are not among those that are over-represented in either P-gaps or NP-gaps.

Differential distribution of species among gaps. Because of the potential importance of seed rain into individual gaps on the eventual composition of the population of colonizing species, we examined the extent to which tree species are clumped among gaps. Because the abundance of species in our sample is highly variable, we use a clumping test that is independent of abundance, Lloyd's Patchiness (P) Index (Pielou 1978). A random distribution of individuals of a species among the maximum number of gaps in which it could have occurred, would give P values close to unity. P values less than one indicate hyperdispersion, while P values larger than one indicate clumping. Because patchiness values are not meaningful for rare species, we limit our discussion to those species for which we found ten individuals or more, the same set we used for the previous multivariate analysis.

Approximately 43% of our species have P values greater than 3.5 (Table 7), the value typically used as the lower limit indicating patchiness. It is significant that a third of the species are crowded into relatively few gaps, even though many of them are common members of the forest canopy. Whereas the more common species are found in more gaps than the rarer ones, no species was recorded in all 51 gaps. Even Pentaclethra macroloba, for which we counted 881 seedlings, was recorded in only 49 gaps.

DISCUSSION

Non-random distributions of seedlings of tree species colonizing tree-fall gaps occur at two different levels - among gaps and within gaps. The major cause of




clumping among gaps is probably the non-random input of seeds associated with the proximity of gaps to fruiting trees. However, seed rain within individual gaps should not be biased in favour of any particular zone. Species with bird dispersed seeds are more likely to land on the edges of gaps than centrally because most birds typically defecate while perched, and most perches are above the periphery of gaps. This pattern should not, however, influence our results because we did not distinguish seedlings according to position within any of the gap zones.

The major cause of non-random distributions within gaps is apparently differential germination success and survival rates of seedlings in the different gap zones. Although we have not measured actual survival rates, it is difficult to explain the clumping of our samples by gap zone type except by assuming non- random survival of seedlings of different species in the different gap zones. Moreover, this mortality must be expressed soon after germination to produce the patterns we found because many of our gaps were less than a few years old. We believe that the critical time for survival is when the seedling exhausts its cotyledonary reserves and must compete with other colonizers and with older individuals that may have survived the fall of the tree. That root competition is an important component of survival is suggested by the rapid decrease of densities of colonizers in bole zones where much of the understorey vegetation survives the tree fall and there is little disturbance to the roots of older plants. The rapidity with which zone-specific patterns are established demonstrates that studies using marked seedlings should yield statistically significant results within a period of relatively few years.

The importance of the species of tree that formed the gap suggests that both nutrient depletion by the adult tree and nutritional differences in crown com- ponents are important in influencing early mortality. Of special interest is the fact that the species of tree that fell does not appear to influence the species composition of bole zones. This zone, with the exception of the ground under the bole itself, is largely unaffected by the identity of the tree that fell. The zone may lie outside the root zone of the falling tree and, hence, should have been minimally influenced by soil depletion caused by that tree. Therefore, of the three zones, the bole zone is the one whose characteristics are expected to be relatively independent of the tree that fell.

Gap size also influences abundances of some of the species in our sample. Larger gaps have higher light and heat inputs in mid-day than do smaller gaps (Denslow 1980), and they also have a large proportion of their total area situa- ted away from the edge. Species with small seeds that are dispersed by wind or small birds that readily move through the low vegetation of newly formed gaps, are more likely to carry propagules to the central parts of gaps, and they should be the species showing the strongest correlation between abundance and gap size.

Root zones are probably subjected to the greatest soil surface disturbance and disruption of pre-existing roots of the three zones. This rather stressful




condition, often associated with high mid-day temperatures, may be why a smaller number of species is able to grow well in root zones than in crown and bole zones. However, for those species able to tolerate the physical conditions in root zones, the diminished competition with survivors should create good germination and early growth-rates after cotyledonary reserves have been exhausted. The high densities of colonizers in root zones, especially in younger gaps, is consistent with this view.

Our results in general support the importance of the internal heterogeneity of tree fall gaps in enhancing species richness. However, studies such as ours, based on static censuses, have limited power to elucidate details of the processes causing differential germination success and seedling survival in different gap zones. Experimental studies and direct measurements of seedling survival are required to complete the picture.

ACKNOWLEDGEMENTS

Help with surveys at La Selva was provided by William H. Hatheway, W. James Erckmann, Genie and Nathaniel Wheelwright. Statistical advice and computa- tional help was given by Tom Crow, Dave Somerton, Steve Willis, Jim Buss, and the Consulting Office of the Academic Computing Center of the Univer- sity of Washington. Lynn Erckmann helped with the graphs, while Betty Hofeditz, Jeanette Pederson, Barbara C. Peterson, and Kathleen Roudybush offered their usual competent services in rendering rough drafts into manu- scripts easier to read. Helpful advice during different states of this work was providided by Peter Ashton, Thomas Zaret, Julie Denslow, Dee Boersma, Rafael Herrera, and Ernesto Medina. Valuable comments on the manuscript were provided by Julie Denslow, Carl Jordan and Christopher Uhl. As usual, logistics and operational support were excellent, thanks to the staff of the OTS office in San Jose, Costa Rica.

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Accepted 1 September 1987

Appendix A. A simple numerical example of the method of calculating expected distributions of individuals among the zones of gaps.

Suppose that we have two species (A and B) whose individuals are distributed among three different gaps (x, y and z) as follows:

Gap

Zone x y z

Species A Root 5 (1) 0 - 4 (1) Bole 7 (6) 0 - 4 (1) Crown 2 (7) 0 - 0 (5)

Species B Root 0 (1) 10 (1) 0 - Bole 0 (4) 6 (1) 0 - Crown 9 (4) 2 (16) 0 -

and that the actual sizes of the zones in the three gaps are as follows:

Area Zone

Root 2 66 30 Bole 15 47 60 Crown 16 735 210

Then, the expected distributions of individuals in the zones of the gaps in which they occurred are given by the figures in parentheses in the upper table. We expect four cases in which one of the species occurred in all three zones and no cases for any of the other combinations. Actually, there were two cases in which one of the species occurred in all three zones of a gap, one case in which it occurred in the root and bole zones only, and one case in which it occurred in the crown zone only. It is these numbers that are entered under the actual and expected values in Table 4. The final table is the result of the iteration of this process for the 30 most abundant species over all gaps in which they actually occurred.



internal heterogeneity of gaps and ... - bgc-jena.mpg.de...journal of tropical ecology (1988)...

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