Seed Size, Seed Germination, and Seedling Survival of Brazilian Tropical Tree Species Differing in Successional Status Author(s):

Rogria Pereira de Souza and I. F. M. Vlio Source: Biotropica, Vol. 33, No. 3 (Sep., 2001), pp. 447-457 Published by: The Association for Tropical Biology and Conservation Stable URL: http://www.jstor.org/stable/3593189 . Accessed: 06/06/2013 00:47
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BIOTROPICA33(3): 447-457

2001

Seed Size, Seed Germination, and Seedling Survival of Brazilian Tropical Tree Species Differing in Successional Status1
Rogeria Pereira de Souza2 and I. F. M. Valio Departamento de Fisiologia Vegetal, Instituto de Biologia, C.P. 6109, Universidade Estadual de Campinas, Campinas, SP, 13083-970, Brazil

ABSTRACT
Seed germination and seedling establishment patterns have been used to classify species as shade tolerant or intolerant. The main objective of this researchwas to investigate, under controlled conditions, seed germination of species from different successional positions as well as to follow seed germination and seedling survival under natural shade in the Croton field. The species studied were Solanumgranuloso-leprosum, Tremamicrantha, Cecropia piptocalyx, pachystachya, Bauhiniaforficata subsp. pruinosa, Senna macranthera, Schizolobium parahyba,Piptadeniagonoacantha,Chorisiaspeciosa, Pseudobombax peruiferum,and longifolium,Myroxylon grandiforum, Ficusguaranitica, Esenbeckialeiocarpa,Pachystroma Hymenaea courbaril.Field trials were carried out at Santa Genebra Municipal Reserve, Campinas, SP, Brazil, at the forest edge and in the understory. No significant correlations were detected between successional status and seed size or seed water content. Light-regulated germination was present only in small-seeded species. In field experiments, most species, including the light-sensitive ones, were able to germinate under the canopy, where a low red/far-red ratio predominates. Most species, mainly those of early- and intermediate successional positions, presented low seedling C. survival rates under shade. Myroxylon peruiferumwas the most shade tolerant species, while S. granuloso-leprosum, speciosa,P gonoacantha, E guaranitica, 77 micrantha, and S. parahyba were the most shade intolerant. These latter species showed little or no survival under the shade conditions. tropicalforest;shade;shade tolerance; germination;seedlingsurvival; seed size; semi-deciduous Key words: light-regulated successional species.

KNOWLEDGE

understanding of processesoccurring in plant communities such as establishment, succession, and regeneration (Vazquez-Yanes & Orozco-Segovia 1993). Early researchon the physiological ecology of secondary succession resulted in a series of generalizations about characteristicsof early and late successional species, with particular reference to seeds (Bazzaz 1979, Bazzaz& Pickett 1980, Swaine & Whitmore 1988). Pioneer or early successional, shade intolerant species were thought to have small seeds with low water content. These seeds were often considered to be produced in large quantities all year-round and to have a long life span and specialized dormancy mechanisms that detected changes corresponding to the arrivalof conditions favorablefor seedling establishment. The main triggering factors for germination were likely to be those associatedwith gap formation, such as changes in light quality and temperature fluctuations (Bazzaz& Pickett 1980, Vazquez-Yanes& Orozco-

Segovia 1984, Swaine & Whitmore 1988). In contrast, late successional, shade tolerant species were thought to have larger seeds produced periodically in small quantities, with high water content, brief or no dormancy, and short life span (Bazzaz & Pickett 1980, Vazquez-Yanes & Orozco-Segovia 1984, Swaine & Whitmore 1988). More recent work (Kelly & Purvis 1993), however, has shown that some shade tolerators may have smaller seeds than light demanders, a result that comes up especially when phylogenetically constrained comparisons are made (Metcalfe & Grubb 1995, Grubb & Metcalfe 1996). Additional studies also have demonstrated that germination of some smallseeded species, although not possible in the dark, can occur under conditions of low red/far-red ratios (R/FR) approximating those found in the forest understory (Drake 1993, Metcalfe 1996). Nonetheless, independent of seed size and despite their capacity of germinating in the shaded understory, many species have seedlings that do not survive under this condition, suggesting that they re1 Received28 February 2000; revisionaccepted1 Sep- quire a light gap to become established (Garwood tember2000. 1983). Thus, not only are studies on seed germi2 author: InstitutoAgron6mico de Cam- nation Corresponding needed, but those on seedling survival in de Fie Biofisica,SeCao pinas, Centrode Ecofisiologia 1481, C.P.28, Campinas, different successional environments are also needsiologia.Av. Baraode Itapura, e-mail: SP, 13001-970, Brazil; rpsouza@barao.iac.br. ed. In a study comparing seedling survival of 18
OF SEED BIOLOGY IS FUNDAMENTAL tO

the

447

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448

Souza and Valio der a green safe light (green-painted fluorescent tubes, previously tested for no effect upon germination of several known light-sensitive seeds). In the field, the seeds were placed in shallow trays filled with soil and maintained at one site at the forest edge and another site inside the forest under the closed canopy. The level of photosynthetic active radiation (400-700 nm) inside the forest was ca 0.4-2.4 percent of full sun, and R/ FR ratio (calculated as the ratio of the spectral irradiance values at the wavelength band 656-664 nm to that at 726-734 nm varied from 0.23 to 0.74. This range of values resulted from several measurements taken at different times of day and in the four different seasons of the year. R/FR ratio of full radiation arriving at the forest edge varied from 1.22 to 1.44. All radiation measurements were recorded by a LI-COR spectroradiometer(LI1800). The soil in the trays was always kept wet. In the field germination experiment, B. forficata, S. and S. parahybaseeds were previously macranthera, scarified to assure a fast and synchronous germination under both test conditions; H. courbaril seeds were not scarified because it was observed that this treatment caused the seeds in contact with soil to rot. Nevertheless, although more scattered and in a lower percentage, germination of intact H. courbarilseeds did occur in the field, probably due to the natural temperature fluctuations or to the action of soil microorganisms that may have rendered the hard coat permeable to water. Seeds T micrantha, C. pachysof S. granuloso-leprosum, are and E very small and thereguaranitica tachya, fore were germinated inside plastic transparentboxes containing vermiculite. After germination, these seedlings were transplanted onto soil in trays for survivalevaluation. In the field, seedling emergence was the criterion for germination. Emerged seedlings were labeled. Survivaland the presence of cotyledons were recorded weekly for variable periods, depending on species. Final survivalwas calculated as a ratio between number of survivorsand number of emerged seedlings. Seedling survival was described by linear regression of the log number + 1 of seedlings surviving versus time. The slope of the regressioncan be designated as the survival rate. Survival rate of the seedlings in the shade can be used as an index of shade tolerance, where values close to zero indicate higher shade tolerance (Augspurger 1984). Mean time until germination, mean time until seedling death, or until loss of cotyledons were evaluated according to Labouriau (1983): t = E n(t, - t)2/(-1 + E ni), niti/l ni and s2 =

tropical tree species, Augspurger (1984) found a broad range of survival in shade that representeda continuum of shade tolerance and not a dichotomy between shade tolerant or shade intolerant species. The objective of this research was to investigate, under controlled conditions, seed germination of species from different successional positions, with emphasis on the light control of the process and to study, under experimental conditions, seed germination and seedling survival under natural shade in the field.

MATERIALS AND METHODS

The species studied are listed in Table 1. All species are native of a semi-deciduous tropical forest situated in Campinas, SP, Brazil (22?44'45" S, 47?06'33" W; 670 m elev.). Seeds were characterized by size, mass, and water content (water content % = fresh mass - dry mass/dry mass X 100; dry mass obtained after drying the seeds at least for 48 h at 80? C). Seed size and mass were measured as mean values of 40 seeds of each species, except for the small-seeded species Solanum granuloso-leprosum, Trema micrantha, Cecropiapachystachya, and Ficus guaranitica, which were weighed in four groups of 25 seeds. Seed water content was estimated by using four or five groups of a variable number of seeds-ranging from 5 to 30-depending on species. For the large-seeded species Schizolobiumparahybaand Hymenaeacourbaril,10 and 20 individual seeds, respectively,were used for water content determination. Germination of freshly collected seeds was first recorded under laboratory conditions to test for dormancy mechanisms and then later tested under field conditions. Seed number used in the experiments ranged from 50 to 100 (laboratorytests) or from 60 to 400 (field tests), depending on species (Tables 2 and 3). In the laboratory,the seeds were placed in petri dishes on two sheets of filter paper wetted with distilled water and kept in incubators at 25?C under constant white light (daylight fluorescent tubes, 3.2 W/m2) or darkness (petri dishes inside three opaque black bags). The hard-coated seeds of Bauhinia forficata, Senna macranthera,S. parahyba, and H. courbarilwere mechanically scarified to promote their germination. The scarification was achieved by abrasion of the seed coat in the region opposite the radicle, using sandpaper (for B. forficata and S. macranthera)or an emery wheel (for S. parahyba and H. courbaril). Radicle protrusion was the criterion for germination. Darkness germination was evaluated in a dark room un-

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TABLE 1.

I = intermediate;and L = late successional),and s status (E = early successional; Speciesstudied, their successional ranked, within each successional group, by seed mass values. Successional statusa E E E E E E E E I I L L L L L Seed size (mm) Major axis 2.17 + 0.02 2.24 + 0.03 2.31 + 0.02 6.09 + 0.09 10.06 + 0.16 7.88 12.90
? +

Species Trec. Cecropia pachystachya (Cecropiaceae) Dun. Solanum granuloso-leprosum (Solanaceae) Tremamicrantha(L.) Blum. (Ulmaceae) Senna macranthera (Collad.) Irwin et Barn. (Caesalpiniaceae) Piptadeniagonoacantha(Mart.) Macbr. (Mimosaceae) CrotonpiptocalyxM. Arg. (Euphorbiaceae) Bauhinia forficata Link subsp. pruinosa (Vog.) Fortun. Et Wund. (Caesalpiniaceae) Schizolobiumparahyba (Veil.) Blake (Caesalpiniaceae) Pseudobombax grandiflorum(Cav.) A. Rob. (Bombacaceae) ChorisiaspeciosaSt. Hil. (Bombacaceae) Ficus guaranitica Schodat. (Moraceae) Esenbeckialeiocarpa(Engl.) (Rutaceae) Myroxylon peruiferumL.f. (Fabaceae) Pachystroma longifolium(Nees) I. M. Johns. (Euphorbiaceae) Hymenaea courbarilL. (Caesalpiniaceae)
a

Minor axis 1.18 + 0.02 1.94 + 0.03 1.99 + 0.03 5.19 + 0.09 7.59 + 0.09 5.86 + 0.07 8.95 + 0.10 17.38 + 0.11 4.69 + 0.05 7.98 + 0.06 1.22 + 0.02 6.24 + 0.07 8.41 + 0.17 10.03 + 0.10 18.10 + 0.27

0.10 0.13

29.30 + 0.25 5.88 + .009 9.58 + 0.08 1.64 + 0.02 8.56

+

0.21

14.81 + 0.28 10.99

+

0.12

25.98 + 0.48

Classification according to Gandolfi (1991), Lorenzi (1992), Mantovani (1993), Salis et al. (1994), Rodrigues, (1995), and B

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TABLE 2.

Final percentagesof germination and mean time until germination of seeds under light and darknessconditions at 25 I = intermediate;and L = late successional); N = sampl response.SS = successionalstatus (E = early successional; mechanicalscarification).

Final germinat Category Light-sensitive seeds Species C. pachystachya S. granuloso-leprosum T micrantha E guaranitica S. macranthera B. forficata S. parahyba H. courbaril Light-insensitive seeds P. gonoacantha C. piptocalyx P. grandiflorum C. speciosa E. leiocarpa M. peruiferum P. longifolium SS E E E L E E E L E E I I L L L 100 100 100 100 100 N (4 (4 (4 (4 (4 x X X X x 25) 25) 25) 25) 25) T me me me me Light 84.0a 4.8a 2.5a 86.0a 79.0a 84.0a 93.0a 78.0a 0.0a 65.Oa 30.0a 78.0a 90.0a 2.5a 57.0a 74.0a 93.0a 72.0a 60.0a

Da

Hard-coated, light-insensitive seeds

100 (4 x 25) 60 (4 x 15) 50 (5 x 10) 100 80 100 100 100 100 80 (4 (4 (4 (4 (4 (4 (4 x x X X x X x 25) 20) 25) 25) 25) 25) 20)

a Values

(light x darkness) followed by the same letter are not significantly different at P < 0.05.

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TABLE 3.

Final percentagesof germination and mean time until germination of seeds underfield conditions-forest edge and u status (E = early successional; I = intermediate,and L = late succe SS = successional grouped by categoryof response.

Final germination Category Light-sensitive seeds Species C. pachystachya S. granuloso-leprosum T micrantha E guaranitica S. macrantheraa B. forficataa S. parahybaa H. courbaril P gonoacantha C piptocalyx P grandiflorum C. speciosa E. leiocarpa M. peruiferum SS E E E L E E E L E E I I L L 160 160 160 160 160 160 120 60 160 400 160 160 160 160 N (4 (4 (4 (4 (4 (4 (4 (4 (4 (4 (4 (4 (4 (4 x x x x x x x x x x x x x x 40) 40) 40) 40) 40) 40) 30) 15) 40) 100) 40) 40) 40) 40) Edge 36.5a 38.0a 21.0a 87.8a 10.0b 45.0a 40.8a 20.0a 54.4a 3.8a 48.8a 49.4a 65.6a 17.5a

Unde

Hard-coated, light-insensitive seeds

Light-insensitive seeds

38 41 16 85 18 48 33 14 39 1 53 57 76 8

a
b

Mechanically scarified seeds. Values followed by the same letter are not significantly different at P < 0.05.

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452

Souza and Valio S. parahyba and H. courbarilseeds, since mechanical scarification promoted germination (Table 2). In B. forficata and S. macranthera,although high germination percentages were attained in intact seeds, seed coat scarificationacceleratedthe process because the mean time to germination was greatly reduced in scarified seeds relative to intact ones (Table 2). Under field conditions, all species except C. showed no significant piptocalyxand S. macranthera differences in germination between the forest edge and under the canopy, in spite of the differencesin light quality at these two sites (Table 3). It must be stressed here that even the seeds that showed light-regulated germination under controlled conditions were able to germinate in the shaded understory. On the other hand, the only two species that exhibited differences in germination at the two sites in the field did not respond to light under laboratory conditions. Seedling survivalwas significantly higher at the forest edge for the majority of species, except for M. peruiferum,and S. macranthera, C pachystachya, H. courbaril(Table 4). These four species showed no significant difference in survival in both environments, although for C. pachystachya,the absence of difference in survivalmay have been a consequence of the high mortality rates found under both conditions. Extremely low or zero survivalunder the canopy was observed in S. granuloso-leprosum, T micrantha, S. parahyba, Piptadenia gonoaand E guaranitica.Myroxcantha, Chorisiaspeciosa, was the only species to show 100 ylon peruiferum percent survival in both microsites. Through the analysisof regressioncurves of seedling survivalversus time and by using the slope of regressionas an index for shade tolerance, M. peruiferumappeared as the most shade tolerant species, followed in sequence by S. macranthera,Esenbeckialeiocarpa,B. forficata, H. courbaril, ?Pgrandiflorum, C. piptocaC. spelyx, C. pachystachya,S. granuloso-leprosum, ciosa, P. gonoacantha, F guaranitica, T micrantha, and S. parahyba(Fig.1). The latter six species were the same as those with very low or zero survival under the shade conditions (Table 4). No correlation was found between the percentage of seedling survival under shade and seed mass log values (r = 0.29, not significant, P > 0.05) or mean time until loss of cotyledons (r = 0.11, not significant, P > 0.05). A negative correlation was found between seed mass and mean time until seedling death (r -0.71, P < 0.05), which therefore indicated a shorter longevity in the understory for seedlings borne of larger seeds.

where t = mean time for germination, mortality, or loss of both cotyledons; ti = time in days corresponding to the days of evaluation; ni = number of germinated seeds, number of dead seedlings, or number of surviving seedlings without both cotyledons in each ti interval;and s2 variance of t. Germination and survival data were statistically analyzed (Sokal & Rohlf 1995). Percentagedata were first transformed in arcsine \/p, where p = proportion of germinated seeds or surviving seedlings. The transformed data were then tested for homogeneity of variances by Bartlett'stest and for normal distribution by a Kolmogorov-Smirnov test as modified by Lilliefors (1967). If these requirements for parametrictechniques were achieved by the angular transformation,the data were analyzedby the Student's t-test at the 5 percent level of probability. Otherwise, the original data (number of germinated seeds or surviving seedlings) were analyzed by a X2 test, or when X2test was not applicable, by Fisher's test, both at a 5 percent level of probability.

RESULTS
A wide variation in values of seed size and mass was found (Table 1). The smallervalues were found for S. granuloso-leprosum, T micrantha, C. pachysand E and the largest for seeds, tachya, guaranitica S. parahyba and H. courbaril. Water content of most seeds was below 15 percent. Water content above this value was observed only for T micrantha, Pachystroma longifolium,and Myroxylon peruiferum seeds (Table 1). Light-regulatedgermination was only verified in S. granuloso-leprosum, T micrantha, C. pachystachya,and E guaranitica seeds (Table 2); however, in the first two species, the obtained percentages of germination were very low, probably a consequence of unknown dormancy mechanisms. Crotonpiptocalyxintact seeds also exhibited very low levels of germination, both in light and darkness (2.5 and 7.5%, respectively),also suggesting the presence of a dormancy mechanism. Several treatments were tested in the laboratory to promote the germination of these species. Chemical and thermal scarificationfor 17 micranthaseeds and coat removal for C. piptocalyxseeds were unsuccessful in promoting their germination, while in S. granuloso-leprosum, seed germination was promoted by treatment with gibberellic acid (results not shown). Under treatment with gibberellic acid, the light-regulated germination of S. granuloso-leprosumseeds was confirmed by the higher level obtained under light versus dark conditions. Physical dormancy imposed by the seed coat was verified in

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Germination and Survival of Tropical Species

453

TABLE 4.

Seedlingsurvival at the specifiedtime after germination (T) and mean time after germination until seedling death at theforest edge and understory of Santa GenebraReserve.Speciesare rankedby the calculatedindex of shade tolerance(a), taken as the slope of the regression of seedlingsurvival versustime. SS = successional status (E = earlysuccessional; I = intermediate;and L = late successional). Seedling survivala (%) Mean time until seedling death + SD (days) Edge 29.1 + 23.9 26.2 + 26.4 43.4 + 32.2 55.5 + 51.0 21.0 + 16.4 35.9 47.5 + 25.5 37.8 + 10.5 19.8 - 17.7 42.7 + 19.9 70.6 + 34.1 60.9 + 14.9 14.1 + 7.5 Understory 60.3 59.2 54.4 37.8 42.4 27.9 60.3 75.4 56.5 44.7 75.3 46.1 22.0 + + + + + + + + + + + + + 45.6 31.4 29.4 28.5 28.1 21.8 29.5 27.6 31.3 18.1 16.6 11.1 10.6

~T
Species SS a

Understory (days) Edge M. peruiferum L 100.0a 0.00000 125 100.0a S. macranthera E 46.4a 57.3a -0.00129 174 E. leiocarpa L -0.00204 51.3b 94.5a 125 B. forficata E 91.0a -0.00280 49.8b 125 H. courbaril L 16.2a 38.9a -0.00366 232 P. grandiflorum I 30.2b 75.9a -0.00501 125 C. piptocalyx E 16.7b 91.7a -0.00537 125 E 19.8a 11.9a 171 -0.00777 C. pachystachya S. granuloso-leprosum E -0.01000 47.1a 3.1b 175 C. speciosa I 2.5b 75.9a 125 -0.01195 P gonoacantha 1.lb E 83.8a -0.01599 125 E guaranitica L O.Ob 24.4a 171 -0.02015 T micrantha E 0.0b 36.9a -0.02826 175 S. parahyba 0O.b E 64.6a -0.03099 77 a Values followed by the same letter are not significantly different at P < 0.05.

DISCUSSION
When comparisons of seed size in shade tolerant and shade intolerant species are made without taking phylogenetic constraints into account, a general trend for shade tolerators having large seeds and light demanders having small seeds usually appears (Foster & Janson 1985, Foster 1986, Hodgson & Mackey 1986, Raich & Khoon 1990). In this paT. per, three pioneer species-S. granuloso-leprosum, micrantha and C. pachystachya-were found to have the smallest seeds, while the highest value of seed size or mass was found for H. courbaril, a climax species. Nevertheless, the other species presented intermediate values, and no apparent correlation could be found between seed size and species successional status. Schizolobiumparahyba, an early successional species, had the second greatest value of seed size and mass, while E guaranitica,a late successional species, was among those with the smallest values. Weak correlation between seed size and successional status was also found by Osunkoya et al. (1994). Metcalfe and Grubb (1995) have also demonstrated that despite the general trend for shade tolerators to have larger seeds than shade intolerant species, there are exceptions, both in terms of small-seeded shade toleratorsand largeseeded light demanders. With respect to water content, no correlation was detected with successional status, although higher water contents have been ascribed to seeds of late successional species rather than early successional species (Vazquez-Yanes&

Orozco-Segovia 1984). This generalization may have been based on some studies that included species of the mature forest that have recalcitrantseeds (i.e., seeds that must retain a relatively high moisture content; 35-65% or more in order to remain viable; Vazquez-Yanes & Orozco-Segovia 1993). These seeds are very sensitive to dehydration and lose viability if they are dried or heated by direct insolation. In fact, some studies have shown that these seeds often present very low germination percentages unless they are located on the forest floor under deep shade and high environmental humidity (Vazquez-Yanes & Orozco-Segovia 1993). When considering only orthodox seeds, however, that can attain low moisture contents (as is the case of the present study) the seed water content seems to be a trait of no ecological meaning because it is determined by the intrinsic characteristicsof the species and perhaps also by the microclimatic conditions at the time of seed maturation. Only the small seeds of S. granuloso-leprosum, 77 micrantha, C. pachystachya,and E guaranitica presented light-regulatedgermination, although the occurrence of such behavior in T. micranthaseeds could not be conclusively demonstrated due to their low germination level. Light requirement for germination of small seeds is expected, because these seeds with scarce reserves produce seedlings that must become entirely dependent upon photosynthesis at an early stage of development. In our experiments, it appearedtrue that early successional species exhibited light sensitivity for germination

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454

Souza and Valio

2.0ooooo a= -0.00016 a= -0.00204 1.5 oooo 00 0
*-00*so

a= =.029 a= 0.0

-a='0.,0~

-0.00129
a= -0.00074

1.0 - 1.0 0.5 -

M.peruiferum
2.0- 0 ooo, 8a=-0.00034 a= -0.00280 .

S. macranthera

E. leiocarpa

1.51.0 -

a= -0.00070 .. '> a= -0.00082. ?^

~1.'~0 ^
0.5-

?~

"~

\~8a= -0.00501

L-

::3 U)
Q 1.

-B. forficata
2.0 -

H. courbaril

a= -0.00366

P. grandiflorum

1.50 0000000 op 1.0a=-0,00012 20, -

. a=-0.00482

a= 8 -0.00777

* -0.00201

C:)

0.5 -

*\a=-0.01000 \

0.0 o.0.

C. piptocal 9; .
.5*,
8,,,

a=-0.00537

C. pachystachya
....

. - i

S. granuloso-leprosum

a= -0.00052 '?.

. 5-"a, "~ V; \9

a= -0.00064

1.5 1.0* *4 0.5-

"~
*\

Va=

-0.00474

* -

a=-0.01195

cn 0)
C:
2.01.5

0C. speciosa

C. a=-0.01599 P. gonoacan a

F. guaranitica \a=-0.02015
An Rn lnn1,n4AniRnian2nn22n' *n 4U DU ZU An An

ootA r_>-

a= -0.00102

co

1.0 a= -0.03099

o
*
8= -0.00828

EDGE
UNDERSTOREY

0.5 n U.U .n

T.micrantha
. . . . . ......... . . . . . . .

a= -0.02826
. . . . . . . .

S. parahyba
. . . . . . . . . . . . . . . . . . .

0 20 40 60 80 100120140160180200220240

0 20 40 60 80 100120140160180200220240

Days
FIGURE 1. Seedling survival at the forest edge and understory of Santa Genebra Reserve. Species are arrangedfrom left to right by decreasing values of the slope of the regression (a) in understory shade (top left: more shade tolerant; bottom right: less shade tolerant).

when seeds were small, but this was not necessarily for F guaranitica. Other dormancy mechanisms true when seeds were large. On the other hand, (not light-related) were observed more frequently light-regulated germination can occur in late suc- in early successional species. Solanum granuloso-lecessional species with small seeds, as was observed prosum, T micrantha,and C piptocalyxintact seeds

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and Survivalof TropicalSpecies Germination failed to germinate under the standard laboratory conditions. Solanum granuloso-leprosum seed germination was enhanced by gibberellic acid and when seeds were maintained under greenhouse conditions in which temperaturechanges may have been the stimulus for germination (Souza 1996). Temperature fluctuations or extreme temperatures may also stimulate germination of T micrantha seeds (Souza 1996). In C piptocalyx,the reason for the low germination is still unknown. In some weed species of Croton, dormancy is imposed by the seed coat (Almeida 1988), but seed coat removal had no effect on C piptocalyxgermination. Physical dormancy imposed by the impermeability of the seed coat was observed in S. parahyba, and scarification promoted germination. In S. macrantheraand B. forficata, the presence of a hard coat did not prevent germination but delayed it. Absorption of water by seeds of these species is very heterogeneous, resulting in a scatteredgermination in time (Souza 1996). Among the late successional species studied here, only H. courbarilpresented dormancy imposed by the impermeability of the seed coat to water, confirming that dormancy mechanisms are more frequently found among early successional species (Bazzaz & Pickett 1980). Under natural conditions, these water-impermeable, hard-coated seeds will prevent prompt germination of the species. In the forest soils, these seeds can be rendered permeable by the action of microorganisms that degrade the coat or by the action of natural temperature changes and weathering (Vazques-Yanes& Orozco-Segovia 1993). An ecological meaning has been assigned to this kind of dormancy, because it spreads germination of a seed cohort over a wide interval of time, according to the rate at which the seeds become permeable. This scattered germination can improve the chance of seedlings surviving over time (Vazques-Yanes& Orozco-Segovia 1993). While this behavior may be especially important to early successional species, which are supposed to colonize new and often unpredictable sites, it may also improve the chance of establishment over time for a late species such as H. courbaril. In the field trials, the great majority of the species, including those with small and light-sensitive seeds, germinated similarly at the forest edge and understory, in spite of the low R/FR ratio in the latter. These low R/FR ratios are known to inhibit germination of several species (Valio & Joly 1979, Vazquez-Yanes & Orozco-Segovia 1987). On the other hand, Metcalfe (1996) showed that some small-seeded species were able to germinate, and to

455

a greaterdegree, under a spectral composition similar to canopy shade than in the dark. Germination of some other small-seeded species under far-red light or understory conditions has also been demonstrated elsewhere (Orozco-Segovia & VazquezYanes 1989, Drake 1993). In this study, it is possible that the low R/FR ratios found at the site where the trials were carriedout, although reduced in relation to the external radiation, were enough to trigger germination. Another possibility is that the occurrence of occasional sunflecks, which have R/FR ratios similar to non-filtered radiation (Souza 1996), could have provided the stimulus for germination. In Piper auritum seeds germinating under a forest canopy, however, Orozco-Segovia et al. (1993) showed that germination was probably independent of sunfleck occurrence. Nevertheless, if germination can occur under the canopy, seedling survival is of crucial importance to successful plant establishment. Field observations from Alvarez-Buylla and Martinez-Ramos (1992) for the pioneer Cecropiaobtusifolia suggest that light availabilityaffects seedling establishment more than seed germination. In the present study, most of the species, mainly those of early and intermediate successional positions, presented low survival percentages under shade (B. forficata and S. macranthera being exceptions). Among the late successional species, E. leiocarpaand M. peruiferum displayed the highest survival percentages under shade. Hymenaea courbaril, in spite of the low survival percentage under shade, did not show a statistically higher survival at the forest edge. Also, it fell among the five most shade tolerant species according to the slope of the regression curves for seedling survival. In some studies, the ability to survive in deep shade has been correlatedwith seed size (Leishman & Westoby 1994). In this study, no correlationwas observed between seed mass and final seedling survival under shade. Saverimuttu and Westoby (1996) have stated that a weak correlation should exist between seed reservemass and survivorshipof seedlings at the leaf stage, in contrast to the strong one observed between seed mass and survivorship of seedlings at the cotyledon stage. According to these authors, once the resourcesin seeds have been fully committed to the buildup of the seedlings, seed mass should no longer be relevant to survival. Nevertheless, a positive correlation between seed mass and duration of survivorship under deep shade could be expected, since extra resources in large seeds could assist seedlings to survive longer in deep shade (Saverimuttu & Westoby 1996);

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456

Souza and Valio tolerance shows that responses do not fit a dichotomy of shade tolerant or shade intolerant species but represents a continuum of shade tolerance, a conclusion also reached by Augspurger (1984) working with 18 tropical tree species. In her paper, a Myroxylonspecies, M. balsamum,was also shown to be the most shade tolerant. Augspurger (1984) also found that no species had a higher survival in shade than at the forest edge. This suggests that all species, even the most shade tolerant ones, require a canopy opening for successful establishment. Shade tolerant species may be able to withstand deep shade and wait for a canopy opening, although they may suffer high mortality rates during this waiting period (Pickett 1983). Although seedE. leiocarpa, lings of M. peruiferum,S. macranthera, B. forficata, and H. courbarilshowed the highest indices of shade tolerance, survival was evaluated for a brief period of time, which makes it impossible to predict how long they could survive under the canopy. While M. peruiferum,E. leiocarpa,and H. courbarilare considered late successional species and are able to regenerate under the canopy, B. forficata and S. macrantheraare early successional species with rare occurrence in the forest. Thus, there may be other processes restricting their distribution in the forest community. ACKNOWLEDGMENTS
We thank Dr. JurandirZullo Jr. for measurementsof the

however, a negative correlation between seed mass and mean time until seedling death was found in this study, indicating a shorter longevity for largeseeded species compared to those with small seeds. Because large seedlings originating from large seeds would require more resources for their maintenance, they could be at a disadvantageunder conditions of deep shade, unless they presented other adaptive characteristics (e.g., low relative growth rates) that would allow them to survive longer under irradiance conditions near or below the compensation point. This could explain why S. parahyba, in spite of having large seeds, showed such a rapid seedling death under shade. In another study (Souza 1996), S. parahybawas shown to have the second highest relative growth rate among the 15 studied species. On the other hand, H. courbaril, the other large-seeded species, had the third lowest relative growth rate, consistent with its longer survival under shade. Myroxylon peruiferum,another species with a low relative growth rate, was outstanding among all studied species in view of its 100 percent of survivalunder shade. Grubb and Metcalfe (1996) have emphasized the low position of seed size in the hierarchy of characteristicsenabling plants to become established in the shade, although it may be adaptive in other aspects (e.g., emergence through litter; Seiwa & Kikuzawa 1996, Metcalfe & Grubb 1997). It seems, therefore, that having large seeds does not guarantee longer survival under shade. Osunkoya (1996) has stressed the importance of examining several traits in order to assess the potential for regenerationof species in different forest sites. The ranking of species by the index of shade

for reviewing the English version of the manuscript. We also thank Fundacao Jose Pedro de Oliveira for permission to work at the Santa Genebra Reserve. R. P. Souza was supported by CAPES.

Sodek and Dr. Ladaslav of radiation distribution spectral

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