seed and seedling ecology of tree species in neotropical secondary forests: management implications

145

Ecological Applications, 10(1), 2000, pp. 145–154q 2000 by the Ecological Society of America

SEED AND SEEDLING ECOLOGY OF TREE SPECIES IN NEOTROPICALSECONDARY FORESTS: MANAGEMENT IMPLICATIONS

MANUEL R. GUARIGUATA1

Center for International Forestry Research (CIFOR), Box 6596 JKPWB, Jakarta 10065, Indonesia, andUnidad de Manejo de Bosques Naturales, Centro Agronomico Tropical de Investigacion y Ensenanza (CATIE),

Turrialba 7170, Costa Rica

Abstract. In spite of the growing importance of neotropical secondary forests assources of timber and environmental services, the baseline information needed to developsilvicultural options is still limited. In this paper I describe interspecific patterns of seedlongevity in the soil, germination, and survival and growth of transplanted seedlings underclosed canopy of nine tree species that are common in secondary forest stands in wet,lowland Costa Rica and most of which are timber species in the region: Cordia alliodora,Hampea appendiculata, Jacaranda copaia, Laetia procera, Rollinia microsepala, Simarou-ba amara, Stryphnodendron microstachyum, Trichospermum grewiifolium, and Vochysiaferruginea. Many of these species also occur throughout the lowland neotropics. Experi-ments were carried out in three replicate secondary-forest stands (20–30 yr old after pastureabandonment) located at La Selva Biological Station in northeastern Costa Rica. Longevityof experimental seed cohorts differed markedly among species, from ,3 mo (Cordia,Hampea, Simarouba, Vochysia), to .1 yr (Stryphnodendron). Similarly, germination ofrecently dispersed seeds in the understory ranged from 0% in Laetia to .75% in Cordiaand Vochysia. In contrast, seedling survival was uniformly low (,10% survival one yearafter transplanting except for Stryphnodendron, which showed ;20% survival).

The implications of these findings for the management of secondary forest stands fortimber production are varied and depend on the species of interest. First, all study speciesappear to require nearly complete canopy opening to regenerate as they show limitedcapacity either to germinate or to survive as seedlings in the understory. Second, somespecies that can germinate at high levels in the shade can be managed at the seedling stageby opening up the canopy a few months after germination (e.g., Cordia, Simarouba, Voch-ysia). Third, species that show little or no germination under closed canopy (e.g., Jacaranda,Laetia, Rollinia) will need canopy removal simply to germinate in adequate amounts. Dueto rapid declines in seed viability and seedling survivorship, however, any canopy manip-ulation must be performed not beyond 6 mo in order to guarantee adequate levels of soil-stored seeds or seedlings for future stand development. Site-preparation techniques mayneed implementation, given the potential of competing vegetation to interfere with seedlingsafter canopy opening, as suggested by the high abundance of herbs and shrubs present inthe soil seed bank in the study stands. This ecological scenario is likely to occur in secondarystands elsewhere in the region as secondary stands are usually located within agriculturalland. Finally, the results of this study suggest that ecological classifications of trees solelybased on light preferences for stem growth may fail to account for important differencesamong species in their regeneration mode. This is of particular importance for refiningsilvicultural guidelines in neotropical secondary forests.

Key words: Costa Rica; forest management; neotropical secondary forests; secondary succession;seed germination, interspecific variation; seedling survival; soil seed bank; stand dynamics; timberspecies, seed ecology; tree seed biology, silvicultural implications; tropical forest trees, life-history.

INTRODUCTION

Recent interest in the role that neotropical secondaryforests can play as sources of timber and environmentalservices (e.g., Wadsworth 1987, Finegan 1992, Fearn-side and Guimares 1996) calls for strengthening theecological basis for their management. Although abun-

Manuscript received 14 September 1998; revised 8 March1999; accepted 11 March 1999.

1 Present address: CATIE 7170, Turrialba 33102, CostaRica. E-mail: [email protected]

dant information exists on the pattern and process ofsecondary forest succession (see review by Brown andLugo [1990]), this knowledge is largely confined to theearly stages of forest development while less is knownof ecological processes in older successional stands(Finegan 1996). Generally, the tree species that dom-inate secondary forests are apparently unable to re-generate under their own shade, as suggested by theabsence of small size classes in stem-diameter distri-butions (Knight 1975), by examining changes in treespecies composition across a forest chronosequence

146 MANUEL R. GUARIGUATA Ecological ApplicationsVol. 10, No. 1

(Saldarriaga et al. 1988), and by monitoring tree re-cruitment over long periods (Lang and Knight 1983).Thus, timber-management guidelines targeted at sec-ondary forests should include recommendations for‘‘drastic’’ canopy opening to facilitate regenerationfrom seed. However, further research on the seed ecol-ogy of timber species is warranted for assuring long-term forest productivity in these successional forestsand for adding flexibility to management prescriptions.

Early studies on tropical-forest succession openedthe way for classifying tree species based on their lightpreferences for germination, establishment, and growth(e.g., Budowski 1965), a topic that still attracts forestecologists (e.g., Swaine and Whitmore 1988, Weldenet al. 1991, Clark and Clark 1992). Management ofthese ecological groups (as opposed to targeting indi-vidual species) has been proposed as a practical optionin species-rich tropical forests (Panayotou and Ashton1992). Yet, even among those tree species that domi-nate the canopies of secondary forests (which usuallyinclude species classified as either ‘‘pioneer’’ or as‘‘late successional’’ or ‘‘long-lived pioneer’’), no con-sistent patterns in terms of seed dormancy and disper-sibility seem to emerge based on their seed biology(e.g., Dalling et al. 1997, 1998). Discerning furtherdifferences in the regeneration from seed within thisecological group should help in designing sound sil-vicultural systems.

In Costa Rica, high deforestation rates for cattle rais-ing during the 1970s, followed by pasture abandonmentdue to a drop in export meat prices one decade later(Butterfield 1994), have resulted in the development ofsecondary forests, particularly in the wet, Caribbeanlowlands. As the agricultural frontier closes in this re-gion, secondary forests have the potential to serve asa low-cost source of timber, at least at the farm level(e.g., Schelhas 1996), especially because high-valuetimber from primary forests is diminishing (Kishor andConstantino 1993, Sanchez-Azofeifa and Quesada-Ma-teo 1995). As is the case elsewhere throughout the low-land neotropics, secondary forests in northeastern Cos-ta Rica are characterized by a low number of canopy-tree species but in high relative dominance (Fineganand Sabogal 1988, Guariguata et al. 1997), two attri-butes that are assumed to facilitate their management(Ewel 1979). Thus the purpose of this study was todevelop baseline information on regeneration fromseed for nine coexisting tree species that commonlyoccur in secondary forests in northeastern Costa Rica,many of which have local commercial value for con-struction and furniture (Carpio 1992). Because most ofthese species range throughout Central and SouthAmerican moist and wet lowlands (Croat 1978, Maury-Lechon 1982, Faber-Langendoen 1992, Gentry 1993,Killeen et al. 1993) the outcome of this research hasthe potential to be generalizable to similar ecologicalregions elsewhere. Specifically, I asked the followingquestions: (1) How do patterns of seed longevity in the

soil vary? (2) Are there differences in the capacity oftheir seeds to germinate under closed canopy and oftheir seedlings to tolerate shade? and (3) What is thenumerical contribution of their seeds to the seed bank?Because many of the study species are currently beingextracted selectively from primary forest in the region,their abundance is likely to remain low under this har-vesting scheme. Thus, their management appears botheconomically and ecologically more attractive in high-density, secondary stands (Wadsworth 1997).

METHODS

Study site

The study was conducted between late 1996 and mid-1998 at La Selva Biological Station, owned by the Or-ganization for Tropical Studies (OTS) and located inthe Sarapiquı region, Heredia Province, NortheasternCosta Rica (108269 N, 848009 W). The natural vege-tation is classified as ‘‘tropical wet forest’’ (sensu Hold-ridge et al. 1975; see Hartshorn and Hammel [1994]for vegetation descriptions), and annual rainfall andtemperature average 3800 mm and 268C, respectively(Sanford et al. 1994). A mild dry season occurs duringJanuary–April, but no month receives on average lessthan 100 mm of precipitation. The landscape is of vol-canic origin, and the topography varies from flat, al-luvial terraces to moderately undulating hills. Approx-imately 63% of the total area of La Selva (;1500 ha)is covered by primary and lightly logged forest, whilesecondary forests account for about 11% of the totalarea (Hartshorn and Hammel 1994).

I selected three replicate secondary forest stands,which are ;4–5 ha in size, separated from each other;2 km. These stands regrew after the abandonment ofpasture that was used for not more than 10 yr afterforest conversion to agriculture. One secondary stand(‘‘Holdridge,’’ ;30-yr-old at the time of study and lo-cated on the easternmost part of La Selva) rests onalluvial soils. The other two secondary stands (‘‘Lin-dero’’ and ‘‘Peje,’’ ;18–20-yr-old at the time of studyand located on central and western La Selva, respec-tively) are underlain by residual soils derived fromPleistocene lava flows (Sollins et al. 1994). The can-opies of the three study stands are floristically andstructurally similar to others in the region with com-parable age and land-use history. Stem density and bas-al area of individuals $10 cm in diameter at breastheight d.b.h. range between 500 and 600 stems/ha and20–25 m2/ha, respectively (Finegan and Sabogal 1988,Guillen 1993, Guariguata et al. 1997, Herrera and Fine-gan 1997), while those of old-growth forest range be-tween 350 and 550 stems/ha and 25–30 m2/ha, respec-tively (Lieberman and Lieberman 1994, Guariguata etal. 1997). The three study stands are surrounded atsome point either by pasture or open, successional veg-etation. All experiments described below were carriedout at least 300 m away from any of these habitats.

February 2000 147TREE REGENERATION IN SECONDARY FORESTS

TABLE 1. Characteristics of the nine study species at La Selva Biological Station, Costa Rica.Nomenclature follows Wilbur (1994).

Species (Family)Commercial

status†

Seedmass(mg)

Dispersalmode Fruiting peak

Cordia alliodora (Ruiz & Pavon) Oken(Boraginaceae)

C 40 Wind Feb.–Mar.

Hampea appendiculata (J. D. Sm.)Standley(Malvaceae)

NC 68 Vertebrates Dec.–Jan.

Jacaranda copaia (Aubl.) D. Don(Bignoniaceae)

C 9 Wind Aug.–Sep.

Laetia procera (Poeppig) Eichl.(Flacourtiaceae)

C 7 Vertebrates Jul.–Aug.

Rollinia microsepala Standley(Annonaceae)

C 40 Vertebrates June–July

Simarouba amara Aubl.(Simaroubaceae)

C 370 Vertebrates Mar.–Apr.

Stryphnodendron microstachyumPoeppig & Endl.(Mimosoideae)

C 80 Vertebrates Jan.–Feb.

Trichospermum grewiifolium (A. Rich.)Kosterm.(Tiliaceae)

NC 3 Wind Feb.–Mar.

Vochysia ferruginea Martius(Vochysiaceae)

C 32 Wind Aug.–Sep.

† C 5 commercial; NC 5 noncommercial. Data are from Camacho and Finegan (1997).

Study species

I selected the study species (see Table 1) on the basisof their observed canopy ocurrence in the area and theiravailability of seeds at the time the study was initiated.Only Trichospermum grewiifolium is uncommon insecondary stands at La Selva but it was included be-cause it is abundant elsewhere in the area ( personalobservation). In contrast, the widespread tree speciesGoethalsia meiantha (J.D.Sm.) Burret (Tiliaceae) wasexcluded because its freshly collected seeds were verydifficult to germinate under controlled conditions (cf.Gonzalez 1991), and therefore estimates of initial seedviability proved unreliable.

For each species (hereafter referred to by genus),seeds were collected from at least four parental indi-viduals. Seed collections started in September 1996 andfinished in July 1997 due to phenological differencesamong species (Table 1); therefore, seeds of each ofthe study species were not sown simultaneously in thefield (see next section). After collection, seeds werepooled and either unfilled or damaged seeds were dis-carded. The two following experiments described be-low were performed within each replicate stand in twoparallel 20 3 20 m plots, each subdivided into a 1 31 m grid. Plots were separated by ;10 m, and bothwere haphazardly laid out under closed canopy. Theexact locations of these plots in each stand are refer-enced on the La Selva Biological Station 50 3 100 mreserve-wide grid (data not reported).

Seed longevity and seed germination in theunderstory

This experiment was designed to assess seed lon-gevity in the soil for a period of one year by burying

a known amount of seeds in nylon mesh bags (1 3 1mm mesh size) and retrieving them at fixed time in-tervals. For each species at each stand, a total of 25bags, each containing 50 seeds, were buried 0–3 cmdeep at random locations within one of the 20 3 20 mplots. A total of 3750 seeds per species were used (50seeds per bag 3 25 bags per stand 3 3 stands). Foreach species at the time of burial, initial seed viabilitywas determined by placing one batch of 250 seeds inshallow plastic trays filled with alluvial soil. Each batchwas left to germinate on an open bench that was pro-tected from the rain but received direct sunlight for atleast 3–4 h/d. They were watered every other day, andobservations were terminated if germination (definedas emergence of a 2-mm-long radicle) did not occurover four consecutive weeks. Not more than 2 wkpassed between the time of seed collection and burialof the mesh bags for any species. Values of initial seedviability for each species were also used as a compar-ison for assessing their ability to germinate underclosed canopy (see below).

Every 3 mo after the date of burial, five replicatebags per species were retrieved from each stand. If atthe time of retrieval any bag showed obvious signs ofdecomposition or holes, it was discarded and anotherwas retrieved (this happened only in a very few casesand it was independent of the species involved). Ger-minated, rotten, or otherwise-missing seeds from with-in the bags were not differentiated. Seeds inside theretrieved bags were germinated under the same con-ditions as described above. No pregermination treat-ment was applied to any species, with the sole excep-tion of the hard-coated seeds of Stryphnodendron,where a slight incision was made at the seed tip tofacilitate water entrance.


To determine the capacity of seeds of the study spe-cies to germinate in the forest understory, I placed (con-currently with the burial of the mesh bags) seeds insidepots under the canopy. For each species two replicatesper stand (50 seeds per replicate) were prepared, eachconsisting of 10-cm-diameter plastic pots filled withthe same substrate (alluvial soil) as above. Pots wereattached to a wooden bench that was leveled 0.5 mabove the forest floor to avoid seed predation. Eachpot was placed inside a larger one (20-cm diameter),in order to retain any seed that might have been carriedaway due to splashing raindrops. Germination was fol-lowed weekly for each species over nine consecutivemonths. Falling leaf litter was removed at each census.

Seedling transplant experiment

Additional batches of seeds of six of the study spe-cies—Cordia, Hampea, Jacaranda, Simarouba,Stryphnodendron, and Vochysia—were collected toraise seedlings in order to evaluate among-speciesseedling performance (growth and survival) in under-story conditions. Species selection was based on pre-vious observations in the study area that suggestedsome capacity to persist under closed canopy followinggermination. However, how long these seedlings areable to tolerate shade under natural conditions had re-mained unexplored. Recently germinated seeds weretransferred to plastic containers (3-cm diameter, 15 cmdeep) filled with alluvial soil and grown under shad-ecloth for at least 3–4 mo before transplanting. Foreach species in each stand, 100 seedlings were trans-planted in 10 random locations witin the adjacent 203 20 m plot (300 seedlings total per species). Removalof existing vegetation was kept to a minimum. At eachrandom location, I demarcated a 1 3 1 m subplot andtransplanted 10 seedlings of the same species, spaced15–20 cm from each other. Seedlings were transplantedduring 3 d during mid-June 1997 (one day for eachstand) and censused for survival at 2, 4, 7, and 12 mo.The height growth of surviving seedlings was measuredonly at 12 mo. At each stand, seedling survival wascalculated from each of the 10 subplots as the numberof seedlings that were alive at census time divided bythe initial number (10) of transplants. Thus, each spe-cies had a total of 10 observations per census time perstand. I assessed the understory light environment atthe transplant plots through black-and-white (ASA400) hemispherical photographs (with a Nikkor 8-mmlens) taken 1 m above the ground in forty randomlyselected points 1 wk before transplanting. The photo-graphic negatives were analyzed with the CANOPYsoftware (Rich 1990), and weighted canopy openness(indirect site factor) was averaged at each stand. Thesevalues were similar across the three stands, and aver-ages ranged from 5.8 to 7.7 (coefficients of variationranged from 24% to 30%).

Natural seed banks

I determined the density and composition of the seedbank by taking core samples (10-cm diameter 3 3 cmdeep) at 5-m intervals along a transect that started fromthe northernmost corner of the plot used for the ex-perimental seed banks (see previous section). To detectpotential seasonal variations in seed input to the soil,sampling was spaced over 6 mo: May 1997 and No-vember 1997, roughly corresponding to the beginningand end of the wet season. The second sampling wasdone in a parallel fashion, 1 m away from the first. Soilsamples were thinly spread (#5 mm, following Dallinget al. [1995]) in plastic trays over a 2-cm-deep heat-sterilized sand layer, and watered every 2–3 d in a shadehouse located in a clearing (;20% full sunlight). Seed-ling emergence was followed for 6 wk. Three controltrays with sterilized soil were used to check for poten-tial airborne-seed contamination. Species morphotypeswere transplanted and allowed to grow (2–3 mo) forfurther identification. Species identification of treeseedlings was assisted by the local expert, Orlando Var-gas (OTS). All other emergents were identified at thelife-form level only (sedge/herb, shrub, liana).

Data analysis

Longevity of experimental cohorts (percentage ger-mination) and seedling transplants (percentage surviv-al) was analyzed for each species with two-way ANO-VA with time and forest stand as fixed main effects.Among-species comparisons in percentage seedlingsurvival were performed with one-way ANOVA onlyat 12 mo following transplanting. Interspecific com-parisons were not possible for both the seed longevityand germination experiments because of species-spe-cific differential seed availability over time (see above,Study species). Percentages were subjected to arcsinetransformations to improve normality, and graphicanalyses of residuals were assessed to check for ho-mogeneity-of-error variances. To test for seasonal dif-ferences within sites in germinant density from the seedbank, Mann-Whitney U tests were performed. Repli-cated goodness-of-fit G tests (Sokal and Rohlf 1981)were performed to test both for seasonal differences inthe absolute abundance of germinants of different life-forms across stands, and for within-species differencesin seed germination in the understory across stands.Statistical significance was fixed at a 5 0.05. Post-hoccomparisons follow the Tukey procedure (Neter et al.1985). All analyses were run on SYSTAT (Wilkinsonet al. 1992).

RESULTS

Seed longevity and seed germination in theunderstory

Over a 1-yr period, experimental seed cohorts of thestudy species showed three distinctive longevity pat-terns in the soil (Fig. 1). Seeds of Cordia, Hampea,


FIG. 1. Changes in seed viability over oneyear of artificial cohorts of nine tree speciestypical of secondary forest (see Table 1), sownin mesh bags in three replicate secondary standsat La Selva Biological Station, Costa Rica. Dataare means 6 1 SE, averaged across stands. Seedcohorts were sown at different time periods dueto phenological differences among species.

FIG. 2. Percentage germination of the ninestudy species (see Table 1) in pots under thecanopy of three replicate secondary stands atLa Selva Biological Station, Costa Rica. Valuesare averaged across stands; data are means and1 SE. Circles on top of each bar represent per-centage germination under open conditions (seeMethods: Seed longevity and seed germinationin the understory).

Simarouba, and Vochysia showed no capacity to remainviable for more than 3 mo following burial; seeds werefound either decomposed or germinated within thebags. Two other species, Jacaranda and Rollinia,reached 0% germination at 9 mo after burial. Of theremaining species whose artificial seed cohorts did notdecline to zero 1 yr after burial, Stryphnodendronseemed to retain the highest germination percentage(;40%) compared to Laetia and Trichospermum (;9%and ;5%, respectively). Only three species showed astatistically significant effect of forest stand on per-centage germination of the retrieved seeds: Jacaranda(ANOVA, P , 0.05), Laetia (ANOVA, P , 0.01), andTrichospermum (ANOVA, P , 0.05). However, no sta-tistical interaction between forest stand and census timewas significant for any species (ANOVA, P . 0.2),suggesting that seed decay over time was similar forall species in all three stands.

Germination percentages under closed canopy werealso very different, ranging from 0 to .75% (Fig. 2).Nine months after sowing seeds in pots for each spe-

cies, no germination was recorded in Laetia, and seedsof Rollinia and Hampea germinated poorly (,25% onaverage). The highest percentages were recorded inCordia, Simarouba, and Vochysia, whose seeds alsogerminated quickly (completed in ,1 mo). The hard-coated seeds of Stryphnodendron were the only onesthat showed prolonged germination, recorded up to 8mo after sowing. The remaining species did not showany germination beyond 4 mo after sowing.

Seedling transplant experiment

Overall, few seedlings survived under shade one yearpost-transplanting (Fig. 3); Stryphnodendron survivor-ship was highest (Tukey, P , 0.01). In contrast, seed-lings of Jacaranda and Simarouba reached nearly zerosurvival at 7 mo after transplanting. A statistical effectof forest stand on seedling survival was detected forSimarouba, Stryphnodendron, and Vochysia (ANOVA,P , 0.01) but as with the seed-longevity experiment,no statistical interaction between forest stand and cen-sus time was evident for any species (ANOVA, P .


FIG. 3. The percentage of seedlings of six of the ninestudy species (see Table 1) that survived over one year at theforest understory of three replicate secondary stands at LaSelva Biological Station, Costa Rica. Data are means and 1SE, averaged across stands. Survival curves for Cordia, Si-marouba, and Vochysia fell between Hampea and Jacarandaafter 7 mo post-transplanting. Seedlings were sown duringMay 1997. The black line on the top right roughly corre-sponds to the dry season.

TABLE 2. Number and composition of tree seedlings thatemerged over a period of 6 wk from twenty 0.0079-m2

paired soil samples taken at 3 cm depth from three replicatesecondary stands at La Selva Biological Station, CostaRica. Nomenclature follows Wilbur (1994).

Species (Family)

Sampling date

May1997

November1997

Apeiba membranacea Spruce ex Benth(Tiliaceae)

1 0

Casearia arborea (L.C. Rich) Urban(Flacourtiaceae)

1 0

Cecropia spp.(Cecropiaceae)

40 33

Goethalsia meiantha (J. D. Sm.) Burret.(Tiliaceae)

18 6

Laetia proceraMiconia multispicata Naudin

(Melastomataceae)

1624

26

Rollinia microsepalaTrema sp.

(Ulmaceae)

—22

10

Vitex cooperi Standley(Verbenaceae)

1 0

Total 123 48

FIG. 4. Average seedling height of those in-dividuals that survived one year after trans-planting, in five of the nine study species (seeTable 1) in the forest understory of three rep-licate secondary stands at La Selva BiologicalStation, Costa Rica. Data are means 6 1 SE.Post hoc comparisons among species in 1-yrheight growth were: Stryphnodendron . Cordia5 Hampea 5 Simarouba 5 Vochysia. The num-ber of surviving individuals after one year foreach species were: Cordia, n 5 8; Hampea, n5 27; Simarouba, n 5 6; Stryphnodendron, n5 42; Vochysia, n 5 18.

0.4). Annual height growth was also higher for Stryph-nodendron seedlings compared to the other study spe-cies (Tukey, P , 0.01; Fig. 4).

Natural seed banks

In all three stands, mean densities of seeds that ger-minated from the seed bank ranged from ;1000 to4000 seedlings/m2, but the relative abundance of treegerminants was remarkably low, not exceeding 14%(Fig. 5). Of all tree species recorded, Cecropia spp.dominated (Table 2). Emerging seedlings from onlytwo of the study species, Laetia and Rollinia, were

observed in much lower numbers. Only at the ‘‘Lin-dero’’ stand was seed density higher in May 1997 (ini-tial census) than 6 mo later (Mann-Whitney U, P ,0.01); seed density did not differ within this time in-terval at the ‘‘Holdridge’’ and ‘‘Peje’’ stands (Mann-Whitney U, P 5 0.36 and 0.11, respectively). However,when plant life-form is taken into account, absoluteabundance of shrub germinants as well as of sedge/herb germinants was not consistent across stands onboth census dates (replicated goodness-of-fit G, P ,0.001 in both cases), suggesting seasonal changes inseed output of these life-forms. In contrast, no seasonalshifts in the absolute abundance of tree and liana ger-minants were statistically significant across stands (rep-licated goodness-of-fit G, P 5 0.9 and P 5 0.5, re-spectively). Relative abundance of shrub germinantsappeared slightly lower in May than in November (45%


FIG. 5. Average number of seedlings from different life-forms that emerged from soil-stored seeds during 6 wk fromtwenty 0.0079-m2 surface soil samples taken at 3 cm depthin three replicate secondary stands at La Selva BiologicalStation, Costa Rica, during middle and late 1997.

vs. 55%, respectively), while it showed an oppositetrend for sedges and herbs (82% vs. 18%, respectively).

DISCUSSION

Seeds of the nine study species showed wide vari-ation in seed longevity and their capacity to germinateunder closed canopy. Less pronounced interspecific dif-ferences, however, were found in the ability of theirseedlings to survive in the understory (there was ,10%average survival 12 mo post-transplanting for five spe-cies), perhaps with the exception of Stryphnodendron,which had the highest survival (;20%, 12 mo post-transplanting). Although the study species can be ro-bustly classified as ‘‘light demanders’’ based on qual-itative observations throughout the study area (e.g.,Guariguata et al. 1997), diameter growth rates (e.g.,Camacho and Finegan 1997), and the results presentedhere, this study demonstrates that nevertheless theyshow contrasting patterns in their early regenerationrequirements. Seed longevity in Simarouba, Cordia,and Vochysia declined to zero in ,3 mo, but thesespecies showed moderate-to-high capacity to germinateunder closed canopy. In contrast, seeds of Laetia andRollinia showed zero or minimal capacity to germinateunder closed canopy, and their germinability declinedto ,10% one year after burial. Moreover, seeds ofStyphnodendron showed moderate capacity to germi-nate under closed canopy, and retained the highest(;40%) germinability of all species 1 yr after burial.Thus no obvious correlation seems to emerge in this

study between seed longevity in the soil and the ca-pacity to germinate in the forest understory. High di-versity in tree life histories was also recently reportedat the seed stage for a suite of pioneer tree species thatcoexist in seasonally moist tropical forest in CentralPanama (Dalling et al. 1997). The available evidencepoints out that ecological classifications of trees basedsolely on light preferences for growth and survival mayfail to account for important differences among speciesin their early regeneration requirements (cf. Dalling etal. 1998, see also Metcalfe and Grubb [1995]).

My findings also shed some light on factors thateither determine initial floristic composition after pas-ture abandonment in the area, or influence tree replace-ment patterns in secondary forest stands. On one hand,for those species whose seeds possess very little dor-mancy, such as Cordia, Hampea, Simarouba, andVochysia, site colonization may be possible only a fewweeks after seed dispersal. Species such as Jacaranda,Laetia, and Stryphnodendron appear less constrainedby timing of seed dispersal to colonize open areas dueto their greater seed longevity. On the other hand, theability of some of the study species to germinate andgrow for limited periods in the understory makes themcapable of self-replacement within their stands perhapsonly if canopy gaps occur. This is expected to be par-ticularly important only beyond intermediate (20–50yr) successional stages, however, as localized canopygaps appear to be infrequent in secondary stands at thisage class (e.g., Saldarriaga et al. 1988). At La SelvaBiological Station, 18–20 yr old secondary standsshowed smaller and more evenly distributed canopyopenings (based on sensor- and hemispherical photo-graphs-based techniques) when compared to neighbor-ing old-growth stands (Nicotra et al. 1999).

This study also bears important practical implica-tions for the management of secondary stands for sus-tained timber production. For the study species as awhole, almost complete canopy removal may be nec-essary either for stimulating seed germination or forsustaining seedling growth and survival. A ‘‘mono-cyclic’’ system (i.e., where tree cutting takes place onlyonce during the stand rotation period) that relies oncreating a future, even-aged stand by opening the mid-dle and upper canopy shortly before tree harvesting(i.e., clearcutting) is perhaps the most amenable (seeWadsworth [1997] for a detailed account of this sil-vicultural system). Managers should keep in mind,however, that timing of this management prescriptionis critical for all species studied, and that the impor-tance of phenology-based knowledge to the manage-ment of secondary forests should not be overlooked.First, due to phenological constraints, the time at whichany canopy manipulation is performed will inevitablyfavor the regeneration of some species at the expenseof others, especially if seeds are not produced annually.Second, for those species that show little or no capacityto germinate under shade (e.g., Laetia, Jacaranda, Rol-


linia), canopy removal should be performed within 6mo post-dispersal in order to guarantee adequateamounts of viable seeds in the soil for germination.Third, for species that are able to germinate and es-tablish as seedlings in the understory (e.g., Cordia,Simarouba, Vochysia), canopy removal should also notoccur later than a few months after germination in orderto guarantee adequate densities for management pur-poses. In contrast to the above-mentioned species, how-ever, features of the seed ecology of Stryphnodendronmake this species not very attractive for managementbased on natural regeneration. The delayed germinationof the hard-coated seeds may preclude the build up ofsubstantial amounts of seedlings either before or aftercanopy manipulation. This is supported to some extentby the fact that although locally common, Stryphno-dendron is rarely abundant in secondary stands in thearea, as opposed to other study species such as Cordia,Laetia, Simarouba, and Vochysia (Guillen 1993, Guari-guata et al. 1997, Herrera and Finegan 1997).

In addition to the above recommendations, formalexperiments are further warranted to test directly howdifferent management techniques may affect early re-generation of the study species. Small-seeded, shade-intolerant species such as those in this study are gen-erally negatively affected during germination and es-tablishment by the presence of leaf litter (e.g., Vazques-Yanes et al. 1990, Guzman-Grajales and Walker 1991).However, the magnitude of the affect varies with thespecies considered and their developmental stage. Intropical moist forest in Central Panama, Molofsky andAugspurger (1992) found that for one of my study spe-cies, Cordia alliodora, surface leaf litter had an effectonly at postgermination emergence compared to otherlight-demanding tree species for which seed germi-nation was more affected. Removal of litter by soilscarification and controlled burning enhance germi-nation and seedling survival of some timber species inthe understory of secondary forests with respect to un-manipulated areas (e.g., Baur 1964, Granados 1995).This practice may be suitable for species that can es-tablish in the shade such as Cordia, Simarouba, andVochysia. Extensive seedling ‘‘carpets’’ of these spe-cies usually appear in the understory a few weeks afterdispersal around fruiting trees (personal observation),and their densities could be further enhanced by ap-plying these substrate-preparation techniques at the on-set of seed dispersal. In contrast, species whose seedsshow limited germination in the shade, such as Laetia,Jacaranda, and Rollinia, may not be suitable for thesesubstrate-preparation techniques unless light levels areconcurrently enhanced, a prescription that may becomeimpractical.

In any case, regardless of the species targeted formanagement, I hypothesize that their seedlings areprone to experiencing competition once the canopy isopened. Irrespective of time of sampling, more than90% of all germinants that emerged from soil-stored

seeds in the study stands were sedges, herbs, andshrubs. This dominance of ‘‘weedy’’ seeds is a commonphenomenon in forest stands surrounded by agriculturalor early successional vegetation (e.g., Cheke et al.1979, Young et al. 1987, Quintana-Asencio et al. 1996,Dupuy and Chazdon 1998). Again for Cordia allio-dora, competition by weeds reduces seedling growthand survival, even when substrate conditions in theopen are suitable for seed germination (Tschinkel1965). Because the large majority of secondary standsin the region (and across neotropical lowlands) are sur-rounded by agricultural or pasture land, research onsite-preparation techniques that aim to control the ef-fect of competing vegetation with tree establishmentseems justified. Interestingly, 20–100 yr old secondaryforests in Central Panama that have been historicallysurrounded by primary forests or spatially isolatedfrom agricultural fields showed a very low proportionof forbs and grasses in their seed banks (Dalling andDenslow 1998).

Decades ago, the Trinidad Tropical Shelterwood Sys-tem (Baur 1964) opened up the way in the neotropicsfor experimental forestry on secondary stands basedon a monocyclic approach. Yet silvicultural knowledgeat the seed level of many tree species still needs to berefined if we are to fully utilize the potential that sec-ondary forests offer as timber sources. In particular,knowledge of seed biology has been largely overlookedfrom a forest-management perspective (at least in theneotropics), except for developing strategies for ex situconservation of germplasm. To date, most silviculturalguidelines in moist and wet neotropical forests narrow-ly focus on increasing stem-growth rates, and few takeinto account the ecological requirements at the seedand seedling stage (but see Stanley and Gretzinger[1996]). Because in Costa Rica in particular (and even-tually in other neotropical countries) many tree speciesthat occur in secondary forests are becoming usable,the time is ripe to encourage research on monocyclictimber management with a solid knowledge base onthe seed and seedling ecology of their component spe-cies.

ACKNOWLEDGMENTS

I thank Bernal Paniagua for his assistance in both seed anddata collection throughout this study and Leo Campos andWilliam Miranda for assistance in hemispherical photo anal-ysis. Giselle Arroyo and Carolina Gonzalez also helped dur-ing various stages of this work. I am grateful to the Orga-nization for Tropical Studies, and especially to Bruce Youngfor permission to carry out this study and for facilitating mywork at La Selva. Partial support was provided by the SwissInternational Cooperation (COSUDE) through CATIE, CostaRica, where thanks are also due to William Vazquez at theseed laboratory. Robin Chazdon, James Dalling, Kathy Ewel,Bryan Finegan, Rebecca Ostertag, Michelle Pinard, and twoanonymous reviewers provided helpful comments and sug-gestions on an earlier version of the manuscript.

LITERATURE CITED

Baur, G. N. 1964. The ecological basis of rain forest man-agement. Forestry Commission of New South Wales, Syd-ney, Australia.


Brown, S., and A. E. Lugo. 1990. Tropical secondary forests.Journal of Tropical Ecology 6:1–32.

Budowski, G. 1965. Distribution of tropical American rainforest species in the light of successional processes. Tur-rialba 15:40–42.

Butterfield, R. P. 1994. The regional context: land coloni-zation and conservation in Sarapiquı. Pages 299–306 in L.A. McDade, K. S. Bawa, H. A. Hespenheide, and G. S.Hartshorn, editors. La Selva: ecology and natural historyof a neotropical rain forest. University of Chicago Press,Chicago, Illinois, USA.

Camacho, M., and B. Finegan. 1997. Efectos del aprove-chamiento forestal y el tratamiento silvicultural en unbosque humedo del noreste de Costa Rica. Informe tecnico295. Centro Agronomico Tropical de Investigacion y En-senanza (CATIE), Costa Rica.

Carpio, I. M. 1992. Maderas de Costa Rica. Editorial de laUniversidad de Costa Rica, San Jose, Costa Rica.

Cheke, A. S., W. Nanakorn, and C. Yankoses. 1979. Dor-mancy and dispersal of seeds of secondary forest speciesunder the canopy of a primary tropical rain forest in North-ern Thailand. Biotropica 11:88–95.

Clark, D. A., and D. B. Clark. 1992. Life history diversityof canopy and emergent trees in a neotropical rain forest.Ecological Monographs 62:315–344.

Croat, T. B. 1978. Flora of Barro Colorado Island. StanfordUniversity Press, Stanford, California, USA.

Dalling, J. W., and J. S. Denslow. 1998. Soil seed bankcomposition along a forest chronosequence in seasonallymoist tropical forest, Panama. Journal of Vegetation Sci-ence 9:669–678.

Dalling, J. W., S. P. Hubbell, and K. Silvera. 1998. Seeddispersal, seedling establishment, and gap partitioningamong tropical pioneer trees. Journal of Ecology 86:674–689.

Dalling, J. W., M. D. Swaine, and N. C. Garwood. 1995.Effect of soil depth on seedling emergence in tropical soilseed-bank investigations. Functional Ecology 9:119–121.

Dalling, J. W., M. D. Swaine, and N. C. Garwood. 1997.Soil seed bank community dynamics in seasonally moistlowland tropical forest, Panama. Journal of Tropical Ecol-ogy 13:659–680.

Dupuy, J. M., and R. L. Chazdon. 1998. Long-term effectsof forest regrowth and selective logging on the seed bankof tropical forests in NE Costa Rica. Biotropica 30:223–237.

Ewel, J. J. 1979. Secondary forests: the tropical resource ofthe future. Pages 53–60 in M. Chavarria, editor. Simposiointernacional sobre las ciencias forestales y su contribucional desarrollo de la America Tropical. CONICIT/Intercien-cia/SCITEC, San Jose, Costa Rica.

Faber-Langendoen, D. 1992. Ecological constraints on rainforest management at Bajo Calima, Western Colombia. For-est Ecology and Management 53:213–244.

Fearnside, P. M., and W. M. Guimaraes. 1996. Carbon uptakeby secondary forests in Brazilian Amazonia. Forest Ecol-ogy and Management 80:35–46.

Finegan, B. 1992. The management potential of neotropicalsecondary lowland rain forest. Forest Ecology and Man-agement 47:295–321.

Finegan, B. 1996. Pattern and process in neotropical sec-ondary rain forests: the first 100 years of succession. Trendsin Ecology and Evolution 11:119–124.

Finegan, B., and C. Sabogal. 1988. El desarrollo de sistemasde produccion sostenible en bosques tropicales humedosde bajura: un estudio de caso en Costa Rica. El Chasquı17:3–24.

Gentry, A. H. 1993. A field guide to the families and generaof woody plants of Northwest South America. Conserva-tion International, Washington, D.C., USA.

Gonzalez, E. 1991. Recoleccion y germinacion de semillasde 26 especies arboreas del bosque humedo tropical. Re-vista de Biologıa Tropical 39:47–51.

Granados, J. 1995. Efecto de los tratamientos del suelo sobrela regeneracion natural en un bosque secundario. Thesis.Centro Agronomico Tropical de Investigacion y Ensenanza(CATIE), Turrialba, Costa Rica.

Guariguata, M. R., R. L. Chazdon, J. S. Denslow, J. M. Du-puy, and L. Anderson. 1997. Structure and floristics ofsecondary and old-growth forest stands in lowland CostaRica. Plant Ecology 132:107–120.

Guillen, L. 1993. Inventario comercial y analisis silviculturalde bosques humedos secundarios en la region Huetar Nortede Costa Rica. Thesis. Instituto Tecnologico de Costa Rica,Cartago, Costa Rica.

Guzman-Grajales, S. M., and L. R. Walker. 1991. Differ-ential seedling responses to litter after Hurricane Hugo inthe Luquillo Experimental Forest, Puerto Rico. Biotropica23:407–414.

Hartshorn, G. S., and B. Hammel. 1994. Vegetation typesand floristic patterns. Pages 73–89 in L. A. McDade, K. S.Bawa, H. A. Hespenheide, and G. S. Hartshorn, editors.La Selva: ecology and natural history of a neotropical rainforest. University of Chicago Press, Chicago, Illinois, USA.

Herrera, B., and B. Finegan. 1997. Substrate conditions, fo-liar nutrients and the distributions of two canopy tree spe-cies in a Costa Rican secondary rain forest. Plant and Soil191:259–267.

Holdridge, L. R., W. G. Grenke, W. H. Hatheway, T. Liang,and J. A. Tosi, Jr. 1975. Forest environments in tropicallife zones. Pergamon Press, New York, New York, USA.

Killeen, T. J., E. Garcıa, and S. G. Beck. 1993. Guıa dearboles de Bolivia. Editorial Quipus, La Paz, Bolivia.

Kishor, N. M., and L. F. Constantino. 1993. Forest manage-ment and competing land uses: an economic analysis fromCosta Rica. LATEN Dissemination Note 7. The WorldBank, Washington D.C., USA.

Knight, D. H. 1975. A phytosociological analysis of species-rich tropical forest on Barro Colorado Island, Panama. Eco-logical Monographs 45:259–284.

Lang, G. E., and D. H. Knight. 1983. Tree growth, mortality,recruitment, and canopy gap formation during a 10-yearperiod in a tropical moist forest. Ecology 64:1075–1080.

Lieberman, M., and D. Lieberman. 1994. Patterns of densityand dispersion of forest trees. Pages 106–119 in L. A.McDade, K. S. Bawa, H. A. Hespenheide, and G. S. Hart-shorn, editors. La Selva: ecology and natural history of aneotropical rain forest. University of Chicago Press, Chi-cago, Illinois, USA.

Maury-Lechon, G. 1982. Regeneration forestiere en GuyaneFrancaise: recru sur 25 ha de coupe papetiere en foret densehumide (Arbocel). Bois et Forets des Tropiques 197:3–21.

Metcalfe, D. J., and P. J. Grubb. 1995. Seed mass and lightrequirements for regeneration in Southeast Asian rain for-est. Canadian Journal of Botany 73:817–826.

Molofsky, J., and C. K. Augspurger. 1992. The effect of leaflitter on early seedling establishment in a tropical forest.Ecology 73:68–77.

Neter, J., W. Wasserman, and M. H. Kutner. 1985. Appliedlinear statistical models. Richard D. Irwin, Homewood, Il-linois, USA.

Nicotra, A. B., R. L. Chazdon, and S. V. B. Iriarte. 1999.Spatial heterogeneity of light and woody seedling regen-eration in tropical wet forests. Ecology 80:1908–1926.

Panayotou, T., and P. S. Ashton. 1992. Not by timber alone:economics and ecology for sustaining tropical forests. Is-land Press, Washington D.C., USA.

Quintana-Asencio, P. F., M. Gonzalez-Espinosa, N. Ramırez-Marcial, G. Domınguez-Vazquez, and M. Martınez-Ico.1996. Soil seed banks and regeneration of tropical rain


forest from milpa fields at the Selva Lacandona, Chiapas,Mexico. Biotropica 28:192–209.

Rich, P. M. 1990. Characterizing plant canopies with hemi-spherical photographs. Remote Sensing Reviews 5:13–29.

Saldarriaga, J. G., D. C. West, M. L. Tharp, and C. Uhl. 1988.Long-term chronosequence of forest succession in the up-per Rio Negro of Colombia and Venezuela. Journal of Ecol-ogy 76:938–958.

Sanchez-Azofeifa, A. G., and C. Quesada-Mateo. 1995. De-forestation, carbon dynamics, and sustainable mitigationmeasures in Costa Rica. Interciencia 20:396–400.

Sanford, R. L., Jr., P. Paaby, J. C. Luvall, and E. Phillips.1994. Climate, geomorphology, and aquatic systems. Pages19–33 in L. A. McDade, K. S. Bawa, H. A. Hespenheide,and G. S. Hartshorn, editors. La Selva: ecology and naturalhistory of a neotropical rain forest. University of ChicagoPress, Chicago, Illinois, USA.

Schelhas, J. 1996. Land-use choice and forest patches inCosta Rica. Pages 258–284 in J. Schelhas and R. Green-berg, editors. Forest patches in tropical landscapes. IslandPress, Washington D.C., USA.

Sokal, R. R., and F. J. Rohlf. 1981. Biometry. W. H. Freeman,New York, New York, USA.

Sollins, P., F. Sancho, R. Mata, and R. L. Sanford. 1994.Soils and soil process research. Pages 34–53 in L. A.McDade, K. S. Bawa, H. A. Hespenheide, and G. S. Hart-shorn, editors. La Selva: ecology and natural history of aneotropical rain forest. University of Chicago Press, Chi-cago, Illinois, USA.

Stanley, S. A., and S. P. Gretzinger. 1996. Timber manage-ment of forest patches in Guatemala. Pages 343–365 in J.Schelhas and R. Greenberg, editors. Forest patches in trop-ical landscapes. Island Press, Washington, D.C., USA.

Swaine, M. D., and T. C. Whitmore. 1988. On the definitionof ecological species groups in tropical rain forests. Ve-getatio 75:81–86.

Tschinkel, H. M. 1965. Algunos factores que influyen en laregeneracion natural de Cordia alliodora (Ruiz & Pav.)Cham. Turrialba 15:317–324.

Vasquez-Yanes, C., A. Orozco-Segovia, E. Rincon, M. E.Sanchez-Coronado, P. Huante, J. R. Toledo, and V. L. Ba-rradas. 1990. Light beneath the litter in a tropical forest:effect on seed germination. Ecology 71:1952–1958.

Wadsworth, F. H. 1987. A time for secondary forestry intropical America. Pages 189–198 in J. Figueroa, F. H.Wadsworth, and S. Branham, editors. Management of theforests of tropical America: prospects and technologies.USDA Forest Service, Institute of Tropical Forestry, PuertoRico, USA.

Wadsworth, F. H. 1997. Forest production for Tropical Amer-ica. Agriculture Handbook 710. USDA Forest Service,Washington, D.C., USA.

Welden, C. W., S. W. Hewett, S. P. Hubbell, and R. B. Foster.1991. Sapling survival, growth, and recruitment: relation-ship to canopy height in a neotropical forest. Ecology 72:35–50.

Wilbur, R. L. 1994. Vascular plants: an interim checklist.Pages 350–378 in L. A. McDade, K. S. Bawa, H. A. Hes-penheide, and G. S. Hartshorn, editors. La Selva: ecologyand natural history of a neotropical rain forest. Universityof Chicago Press, Chicago, Illinois, USA.

Wilkinson, L., M. Hill, S. Miceli, P. Howe, and E. Vang.1992. SYSTAT for Macintosh. Version 5.2. SYSTAT, Ev-anston, Illinois, USA.

Young, K. R., J. J. Ewel, and B. J. Brown. 1987. Seed dy-namics during forest succession in Costa Rica. Vegetatio71:157–173.

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