Germination requirements and seedling shade tolerance are not correlated in a Chilean temperate rain forest

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Research

Blackwell Science Ltd

Germination requirements and seedling shade tolerance

are not correlated in a Chilean temperate rain forest

Javier A. Figueroa

1

and Christopher H. Lusk

2

1

Departamento de Ecología, Facultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile, Casilla 114-D, Santiago, Chile;

2

Departamento de

Botánica, Facultad de Ciencias Naturales y Oceanográficas, Universidad de Concepción, Casilla 160-C, Concepción, Chile

Summary

•

In a comparative study of 26 Chilean temperate woody species, the followingquestions were addressed. Are germination requirements correlated with seedlinglight requirements? Can germination requirements be used to delimit pioneer andnonpioneer guilds?

•

To assess dependence of germination on canopy gaps, germination percentageswere compared experimentally in gap and understorey environments. Seedling lightrequirements were quantified by determining the mean light environment naturallyoccupied by juveniles of each species.

•

Germination was significantly higher in the gap than in the understorey in > 30%of the species, although only one germinated exclusively in the gap. In the under-storey, germination was higher in 19% of species, whereas 50% were indifferent togermination environment. Several light-demanding species germinated abundantlyin the understorey. Both cross-species analysis and phylogenetically independentcontrasts showed that seedling light requirements were not correlated with respon-siveness of germination to the gap environment.

•

Results suggest that germination requirements and seedling light requirements arenot coupled, and that requirement of canopy gaps for germination cannot be usedto delimit pioneer and nonpioneer guilds in a Chilean temperate rain forest.

Key words:

Forest dynamics, germination, LAI-2000, phylogenetically independentcontrasts, pioneer and climax species, shade tolerance, temperate rain forest.

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Author for correspondence:

Javier A. Figueroa Tel: +56 (2) 6862610 Fax: +56 (2) 6862620 Email: [email protected]

Received:

8 May 2001

Accepted:

6 September 2001

Introduction

Much research on tropical rain forest trees has focused on lifehistory variation in relation to successional status. Swaine &Whitmore (1988) suggested that tropical tree species could beclassified into two qualitatively distinct main groups: pioneerand climax or nonpioneer species. Furthermore Swaine &Whitmore (1988) proposed that germination requirementsmay discriminate between these two groups, with pioneerspecies germinating beneath canopy gaps only. However,some subsequent reports are not consistent with this pro-posal. At least some tropical pioneer species are capable ofgerminating under closed canopy, and their association withhigh-light environments only becomes manifest after germina-tion, at the seedling stage (Kyereh

et al.

, 1999; Figueroa &Vazquez-Yanes, 2001).

Few studies have screened large sets of co-occurring tem-perate woody species, to see if Swaine & Whitmore’s postulatecan be applied to temperate forests. Studies of the dynamicsof South American temperate rainforests suggest that anumber of the dominant tree species regenerate mainly orexclusively beneath canopy openings (Veblen

et al.

, 1981;Veblen, 1985; Armesto & Figueroa, 1987; Armesto &Fuentes, 1988). However, at present there are no data thatmight permit an objective classification or ranking of thelight requirements of these species. Neither is much knownabout germination requirements of the woody species ofSouth American temperate rain forests (Figueroa & Armesto,2001).

In the present study, we ask: are germination require-ments correlated with seedling light requirements?; and cangermination requirements be used to delimit pioneer and

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nonpioneer guilds in Chilean temperate rain forest? In orderto answer these questions, we compared the germination of26 woody species in gap and understorey environments, andderived quantitative ratings of the light requirements ofthe seedlings of these 26 taxa by measuring their naturallyoccurring frequency distributions in relation to canopyopenness.

Materials and Methods

Study site and species

Germination assays and seedling shade tolerance measure-ments were carried out under natural conditions at theEstación Biológica Senda Darwin, located 18 km north-eastof Ancud, on Isla Grande de Chiloé, Chile (41

°

50

′

S,73

°

38

′

W). The climate of the study area is maritimetemperate, with an average annual rainfall of

c.

2200 mm, andmean annual temperatures of 9.5

°

C. On Chiloé there is aslight Mediterranean influence that is reflected in a summerrainfall minimum (Di Castri & Hajek, 1976).

We selected 26 common woody species (trees andshrubs) from the temperate forest of Chiloé (Table 1).

The lowland and mid-altitude forests of Chiloé are domin-ated by broadleaved evergreen trees (Veblen & Schlegel,1982). An upper storey up to 40 m tall is variously domin-ated by

Nothofagus nitida

,

Weinmannia trichosperma

,

Laureliopsis philippiana

and

Eucryphia cordifolia

, with asubcanopy of Myrtaceae. Vines, epiphytes and ferns areabundant. Shrubs are common in open site and forestmargins, but are scarce below the canopy (Armesto &Figueroa, 1987).

Seed collection

Seeds were collected from within the Estación BiológicaSenda Darwin, which extends over an area of

c.

100 ha. Withthe exception of

Embothrium coccineum

, whose fruits werecollected during 1999, most species were collected in 1998,during the months of maximum fruit load (Smith-Ramírez &Armesto, 1994; Figueroa

et al.

, 1996). Immediately aftercollection, seeds were extracted manually from the fruits,dried under local ambient conditions of the Senda Darwinlaboratory for 3 d, and then sown immediately. All seedswith blemishes or evidence of fungal or insect attack wererejected.

Table 1 Germination percentages of seeds of 26 Chilean temperate woody species in gap and understory environments, and mean light environments of seedlings. Taxa ordered according to phylogenetic relationships (Soltis et al., 1999). Germination percentages for species with asterisks differ significantly between the two environments (randomization test, P < 0.05)

Species

Germination (%)Seedling light requirements (mean percentage canopy openness)Gap Understorey

Aristotelia chilensis (Mol.) Stuntz* 93 68 13.3Crinodendron hookerianum Gay* 57 91 13.7Eucryphia cordifolia Cav.* 21 54 7.7Caldcluvia paniculata (Cav.) D. Don 60 69 6.4Ovidia pillo-pillo (Gay) Meisn.* 31 0 12.0Amomyrtus luma (Mol.) Legr. et Kaus.* 77 96 3.4Amomyrtus meli (Phil.) Legr. et Kaus. 95 96 6.3Myrceugenia ovata (H. et A) Berg var. ovata 98 91 3.5Myrceugenia ovata var. nannophylla (Burret) Landrum 83 88 5.0Myrceugenia planipes (H. et A) Berg* 82 100 2.4Myrceugenia parvifolia (DC.) Kausel 89 87 4.6Luma apiculata (DC.) Burret 91 84 8.7Tepualia stipularis (H. et A) Griseb 15 21 14.6Rhaphithamnus spinosus (A.L. Juss) Mold.* 79 39 4.4Pseudopanax laetevirens (Gay) Franchet* 70 50 6.2Baccharis patagonica H. et A. 31 17 76.5Gaultheria phillyrerifolia (Pers.) Sleumer* 60 31 10.1Aetoxicon punctatum R. et P. 100 100 2.9Gevuina avellana Mol. 89 98 6.6Embothrium coccineum J.R. et G. Forster* 93 11 25.6Lomatia hirsuta (Lam.) Diels ex Macbr.* 83 57 10.9Berberis darwinii Hook. 95 87 20.6Berberis buxifolia Lam. 98 87 75.8Laureliopsis philippiana (Looser) Schodde 15 10 2.5Drimys winteri J.R. et G. Forster* 75 16 8.8Podocarpus nubigena Lindl.* 0 22 3.5


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Seed germination environments

Germination percentages of each species were obtained in twoenvironments within a secondary forest fragment of

c.

4-haarea at the Senda Darwin: in the center of a gap of

c.

80 m

2

;and under a closed canopy. To prevent rodents and birds fromconsuming the seeds, the trays and pots in both environmentswere enclosed in 1 m

3

cages lined with chicken wire. Theforest fragment was dominated by

Nothofagus nitida

,

Drimyswinteri

, and Myrtaceae, surrounded by a grassland-shrubmatrix.

Two different instruments were used to quantify lightregimes in the gap and understorey environments used for thegermination experiment. A LI-1400 Data Logger and quan-tum sensor (Li-Cor, Lincoln, Nebraska, USA) was used tomeasure photosynthetic photon flux densities at 12 : 00 h on3 d during spring, giving mean figures of

c.

700 µmole m

−

2

s

−

1

in the open outside of the forest,

c.

140 µmole m

−

2

s

−

1

in thecenter of the gap, and 4 µmoles m

−

2

s

−

1

in the understoreysite. Measurements with two LAI-2000 Canopy Analysers(Li-Cor) indicated that diffuse light intensities in the gapand under the canopy were 34 and 1%, respectively, of thoseexperienced at the open site.

Germination experiment

Large seeds (> 0.1 mg) were sown in plastic trays, whilesmaller seeds were sown in plastic pots. For every speciesassayed, three trays or pots were sown with 50 seeds each inthe gap environment, and an equal number of trays wereplaced in the understorey site. Tray and pot positions withinthe protection cage were rerandomized at monthly intervals.The soil used for germination, obtained directly from thestudy site, was sterilized by heating to > 150

°

C. Seeds weresown on the soil surface. To avoid insect predation on seedsand seedlings, the trays and pots were wrapped with whitepolyester mesh (< 0.5 mm aperture), which reduced PPFDby

c.

20%. In order to account for any natural seed fallfrom plants surrounding the sowing site, we included a traycontaining sterile soil but no sown seeds, in both gap andunderstorey environments.

Responsiveness of germination of each species to the gapenvironment was assessed as:

∆

G = G

gap

– G

understorey

/G

max

(G

max

, maximum germination, whether in gap (G

gap

) orunderstorey (G

understorey

) environments.) This index variedbetween 1 and

−

1, higher values indicating greaterdependence of germination on gap environments. Thegermination assays were run for one year, with theexception of

Podocarpus nubigena

that was monitored for2 yr because the seeds presented a long germinationdelay > 1 yr.

Seedling light requirements

A pair of LAI-2000 canopy analysers was used to quantifylight requirements of juvenile woody plants. The percentageof canopy openness above a given point was determined bycomparing simultaneous readings on one LAI-2000 inside theforest, and another stationed at an open site outside of theforest. Measurements of canopy openness with the LAI-2000have been shown to be a good surrogate of variation in totaldaily PPFD in forest understorey environments (Machado &Reich, 1999).

Transects of variable length were run from the center of sec-ond growth stands to well outside the forest margin, encom-passing a wide range of light environments. At random pointsalong each transect, one LAI-2000 was used to take measure-ments immediately above the nearest juvenile, between 0.1and 1.0 m tall, of each woody species present within a radiusof 1.5 m. A minimum of 15 observations per species wereused to calculate the mean light environment (percentagecanopy openness) for each species. As canopy openness datawere strongly skewed, we calculated the geometric mean lightenvironment for each species, instead of the arithmetic mean.

Statistical analyses

A randomization test (Manly, 1992) was used to comparegermination percentages of each species after 12 months inthe gap and the understorey, as there was no true replicationof germination environments. This test compared theobserved difference between germination percentages in thetwo treatments with the distribution of differences arisingfrom 10

4

pairs of random numbers selected from within thesame potential range (0–100).

We used two different methods to analyse the relation-ship between germination and seedling light requirements.In addition to conventional methods that assume species areindependent data points, we used an independent contrastsmethod derived from Felsenstein (1985), and the algorithmsdeveloped by Pagel (1992) and Kelly & Purvis (1993), inorder to correct for phylogenetic relatedness among species.Each contrast tested whether the change in the ‘causal’ vari-able (germination gap requirements) between a pair of taxa isassociated with change of the ‘response’ variable (seedlinglight requirements) of the same pair of taxa, in the directionpredicted by the hypothesis. Each contrast is thus an inde-pendent observation of evolutionary trends.

Independent contrasts were carried out using the ‘Com-pare’ program (Martins, 2001), and were based on a phylo-genetic tree constructed using the angiosperm phylogenyinferred from multiple genes by Soltis

et al

. (1999), and theLandrum (1981) phylogeny for

Myrceugenia

, the most diversetree genus of the temperate forests of Chile. Omission of twospecies responsible for outlier points (

Baccharis patagonica

,

Berberis buxifolia

) was necessary in order to eliminate a



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correlation of seedling light requirement contrasts with meanvalues at nodes (Freckleton, 2000). Attempts to solve thisproblem by data transformation were unsuccessful, but afterelimination of these two species contrast values were not cor-related with mean values at nodes, for either germination data(Pearson

r

=

−

0.16,

P

= 0.45,

n

= 23) or seedling light require-ment data (

r

= 0.04,

P

= 0.85,

n

= 23), indicating complianceof our data with one of the necessary conditions for phylo-genetic independence of contrasts (Freckleton, 2000). Weincluded all possible contrasts within our fully resolved tree,finding no statistical difference between higher and lower levelcontrasts.

Independent contrasts are often analysed by regression ofcontrasts between the two variables under study (Harvey &Pagel, 1991; Beerling & Kelly, 1996). However, in our dataset the germination contrasts were not normally distributed,suggesting evolution following a nonBrownian motion model(Kelly & Southwood, 1999). This led us to prefer a sign test,which was effected by randomization. This test compared thenumber of positive results observed among our 23 contrasts(i.e. those consistent with the hypothesis) with the distribu-tion of positive outcomes for 10

4

sets of 23 random binomialevents. If the number of positive contrasts observed in ourdata set fell within the range expected by chance (assuming

p

= 0.5) then the hypothesis that germination requirements arecorrelated with seedling light requirements would be rejected.

In addition to the analysis of independent contrasts, wecarried out a standard cross-species analysis for all 26 species.The Pearson correlation coefficient was calculated for the cross-species analysis without considering phylogeny, as a descrip-tive statistic measuring the degree of association between thetraits among contemporary taxa (ahistorical correlation).

Results

Germination in gap and under the canopy

After 12 months, 13 (50%) of the species studied presentedsignificantly different germination percentages between gapand understorey environments (Table 1, Fig. 1). Eight speciesgerminated significantly better in the gap environment thanin the understorey, one of these (

O. pillo-pillo

) germinatingbeneath the gap only. By contrast, several species showedsignificantly greater germination under the canopy, with one(

Podocarpus nubigena

) germinating under the canopy only.However, the germination percentage of exactly half of the setof species showed no significant difference between gap andunderstorey environments (Table 1, Fig. 1).

Germination responded most positively to the gap envi-ronment in

Ovidia pillo-pillo

and


(Table 1), both small, short-lived early successional trees. Onthe other hand, germination of all eight species of Myrtaceaewere very unresponsive to the gap environment, most speciesactually germinating slightly better in the understorey.

Seedling light requirements

Most taxa showed some tolerance of shade, with 62% of thespecies studied occupying mean light environments of < 10%canopy openness (Table 1). The four most shade-tolerantspecies of our database appeared to be

Myrceugenia planipes

,

Laureliopsis philippiana

,

Aextoxicon punctatum

and

Amomyrtusluma

, with seedling mean light environments of < 4% canopyopenness. The seedlings of


and

Berberis darwinii

were associated with mean light environ-ments of > 20% canopy openness, and the small shrubs

Berberis buxifolia

and

Baccharis patagonica

stood out asostensibly the most light-demanding species, with mean lightenvironments of 76 and 77% canopy openness, respectively(Table 1).

Relationship between germination response and seedling light requirements

Correlation analysis showed that germination gap require-ments were not significantly associated with seedling lightrequirements (Fig. 2). Neither was any such relationshipdetected by analysis of independent contrasts. Fourteen out of23 independent contrasts showed parallel changes in thesetwo traits in the sense of the hypothesis (Table 2), and arandomization test indicated that this number does not falloutside the range of possibilities to be plausibly expectedunder a under a null model (

P

= 0.20).

Discussion

Our comparison of 26 woody species of the temperate rainforests of southern Chile revealed a wide range of germination

Fig. 1 Breakdown of germination responses to gap and understorey environments for 26 woody species in a Chilean temperate rain forest.


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responses to overstorey density, from species that germinatedpreferentially or exclusively under open conditions, to thosethat germinated better beneath closed canopy (Fig. 1,Table 1). However, only one species germinated exclusively in

the gap environment, and 50% were statistically indifferentto overstorey density. The continuum of responsiveness to thegap vs understorey environments provides little evidence ofdiscrete functional groups for germination characteristics. Asimilar continuum has also been shown for other germinationrequirements of Chilean temperate woody species, such asresponses to chilling ( J. A. Figueroa, unpublished).

Seedling responses to canopy openness also varied widelyand continuously between species. However, most speciesshowed evidence of being able to survive under forest cano-pies, with mean canopy openness values of < 10% for > 60%of the species tested (Table 1). Only four species (15%),including two small

Berberis

shrubs, were associated on aver-age with environments of > 20% canopy openness. This evi-dence of a predominance of shade-tolerant species agrees withprevious studies, which have reported abundant and diverseseedling banks in southern Chilean rainforests (Veblen

et al.

,1981; Armesto & Figueroa, 1987; Armesto & Fuentes,1988). Among the tree species, the relative light requirementssuggested by our results (Table 1) correspond well, in general,with the shade tolerance categories proposed subjectively byDonoso (1989). Our results support previous empirical evid-ence that many of the most shade-tolerant taxa of southernChilean forests belong to the Myrtaceae (Armesto & Fuentes,1988; Lusk & Del Pozo, 2002).

Our results do not support the idea that germination gaprequirements can be used to define pioneer and nonpioneerguilds in a Chilean temperate rain forest. As predicted bySwaine & Whitmore (1988), the germination of most shade-tolerant species was relatively unresponsive to overstoreyconditions, with similar percentages of germination in the gapand beneath canopy (Table 1). However, light-demandingspecies were heterogeneous in their germination require-ments. We found only two species that correspond closely toSwaine & Whitmore’s (1988) concept of a pioneer:

Emboth-rium coccineum

and

Ovidia pillo-pillo

. These small trees, char-acteristic of open sites, forest edges, and old-fields (Donoso,1981, 1989), showed little or no germination beneath a treecanopy and light-demanding seedlings. Most other specieswith high seedling light requirements (e.g.

Berberis

spp.,Lomatia hirsuta) showed moderate to high germination levelsin the understorey (Table 1). The scarcity of the seedlings ofthese species under canopy in the forests of the study areatherefore reflects poor seedling survival, rather than germina-tion failure.

Several studies of tropical trees have also failed to supportSwaine & Whitmore’s (1988) proposal that germinationrequirements delimit pioneer and nonpioneer guilds. A studyof the effect of light on the germination of forest trees inGhana concluded that light-mediated germination is rela-tively rare among tropical pioneers (Kyereh et al., 1999).Other recent work in tropical environments (Clark, 1986;Raich and Gong, 1990; Figueroa & Vazquez-Yanes, 2001;C. Kelly, unpublished) has also questioned this relationship.

1

10

100

−1.0 −0.5 0.0 0.5 1.0

See

dlin

g lig

ht r

equi

rem

ent

(% c

anop

y op

enne

ss)

Germination gap-dependence(Ggap – Gunderstorey / Gmax)

Fig. 2 Ahistorical relationship between seedling light requirements and responsiveness of germination to a gap environment for 26 Chilean rain forest woody species (Pearson correlation, r = 0.32, P = 0.11).

Table 2 Results of 23 independent contrasts of germination gap-dependence and seedling light requirements, for 24 Chilean temperate rain forest woody species. Positive signs indicate that change is in the direction predicted by the initial hypothesis, whereas negative signs indicate contrasts that run counter to the hypothesis

Contrast Sign

Aristotelia chilensis vs. Crinodendron hookerianum = (1) −Eucryphia cordifolia vs. Caldcluvia paniculata = (2) −(1) vs. (2) = (3) +(3) vs. Ovidia pillo-pillo = (4) +Amomyrtus luma vs. A. meli = (5) +Myrceugenia ovata var. nan. vs. M. ovata var. ov. = (6) −(6) vs. Myrceugenia planipes = (7) +(7) vs. Myrceugenia parvifolia = (8) +(8) vs. Luma apiculata = (9) +(5) vs. (9) = (10) +(10) vs. Tepualia stipularis = (11) −(4) vs. (11) = (12) +Rhaphithamnus spinosus vs. Pseudopanax

laetevirens= (13) −

(13) vs. Gaultheria phillyearifolia = (14) +(12) vs. (14) = (15) −(15) vs. Aextoxicon punctatum = (16) +Embothrium coccineum vs. Lomatia hirsuta = (17) +(17) vs. Gevuina avellana = (18) +(16) vs. (18) = (19) −(19) vs. Berberis darwinii = (20) −Laureliopsis philippiana vs. Drimys winteri = (21) +(20) vs. (21) = (22) −(22) vs. Podocarpus nubigena = (23) +


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Nevertheless, Vázquez-Yanes & Orozco-Segovia (1993) havereported that many pioneer trees and shrubs in the tropicalrain forests of México do conform to the pattern proposed bySwaine & Whitmore (1988), accumulating large seed reservesin the soil of primary forests, and showing photoblasticgermination after disturbance.

Overall, the results obtained in this study showed thatgermination behaviour was not correlated with seedling lightrequirements among woody species of the Chilean temperaterain forest. Although the germination responses to the gapthat we studied should not be equated solely with light-dependence, our study suggests that light-mediated germ-ination and seedling shade-tolerance are not coupled. Theincorporation of information on phylogenetic relatednessin this analysis did not greatly alter the result and the phylo-genetic analyses were comparable to correlations calculateddirectly from the species values (Table 2, Fig. 2).

The germination experiment included no true replication,and was carried out in only one gap and one understorey site,therefore we cannot rule out the possibility that uncontrolledfactors influenced our results. In a worst case scenario, uncon-trolled idiosyncracies of our germination sites could conceiv-ably have led us to commit a Type II error in rejecting thehypothesis that germination requirements and seedlingshade-tolerance are coupled. However, this scenario seemshighly unlikely, given that the crucial evidence compelling arejection of the hypothesis is the abundant germinationof some light-demanding species (e.g. Berberis spp., Lomatiahirsuta) at the understorey site. It is very difficult to imaginecircumstances or factors that might stimulate abundantanomalous germination of seeds beneath a dense canopyadmitting only 1% of diffuse light, if the species in questionnormally require gaps to break dormancy.

Seed burial could cause natural germination patterns ofsome of our species to differ from those reported here. Photo-blastic dormancy of some small-seeded tropical rain forestpioneer species is induced by burial in litter or soil (Vázquez-Yanes et al., 1990; Vázquez-Yanes & Orozco-Segovia, 1992),conditions which were not reproduced in our experiment, aswe standardized germination conditions by sowing all seedson the soil surface. This raises the possibility that the abun-dant germination of some light-demanding species in theunderstorey site in our experiment could be an artefact of ourexperimental procedure. However, many of the same tropicalspecies that show dormancy after burial in litter or soil aresimilarly induced to dormancy by the relatively low R : FRratios present beneath dense forest canopies (Vázquez-Yanes& Orozco-Segovia, 1990), suggesting that our understoreytreatment would probably detect any photoblastic dormancyif it were present, as indeed it appeared to be in O. pillo-pilloand E. coccineum (Table 1).

Gap size, shape and orientation influence a variety ofenvironmental parameters such as light quantity and quality,air and soil humidity, and daily temperature range (Denslow,

1980; Collins & Pickett, 1987), all of which are known toinfluence seed bank survival and germination (Washitani &Takenaka, 1987; Vázquez-Yanes et al., 1990). Variation insuch gap parameters could therefore also affect the resultsreported here. Further studies considering responses of ger-mination to environmental variation across a gradient of gapsizes are therefore warranted.

Acknowledgements

We thank Juan-Fernando Hernández, Colleen Kelly and ananonymous referee for their constructive comments on themanuscript, P. Jordano for his help with comparativemethods, and A. Vidal for installing the protection cages inthe field. This research was funded by FONDECYT projectsnos 3980020, 1980084 and 1000367. JAF is supported by aMellon Foundation Fellowship. This article is a contributionto the research programme of Estación Biológica SendaDarwin, Ancud, Chiloé.

References

Armesto JJ, Figueroa J. 1987. Stand structure and dynamics in the rain forest of Chiloé Archipelago. Journal of Biogeography 14: 367–376.

Armesto JJ, Fuentes E. 1988. Tree species regeneration in a mid-elevation rain forest in Isla de Chiloé, Chile. Vegetatio 74: 151–159.

Beerling DJ, Kelly CK. 1996. Evolutionary comparative analyses of the relationship between leaf structure and function. New Phytologist 134: 35–51.

Clark DA. 1986. Regeneration of canopy trees in tropical wet forests. Tree 6: 150–154.

Collins BS, Pickett STA. 1987. Influence of canopy opening on the environment and herb layer in a northern hardwoods forest. Vegetatio 70: 3–10.

Denslow JS. 1980. Gap partitioning among tropical rain forest trees. Biotropica 12: 47–55.

Di Castri F, Hajek ER. 1976. Bioclimatología de Chile. Santiago, Chile: Universidad Católica de Chile.

Donoso C. 1981. Ecología forestal. Santiago, Chile: Editorial Universitaria.Donoso C. 1989. Antecedentes para la silvicultura del tipo forestal

siempreverde. Bosque (Chile) 10: 37–53.Felsenstein J. 1985. Phylogenies and the comparative method. American

Naturalist 125: 1–15.Figueroa JA, Armesto JJ. 2001. Community-wide germination strategies

in a temperate rainforest of Southern Chile: ecological and evolutionary correlates. Australian Journal of Botany 49: 411–425.

Figueroa J, Armesto JJ, Hernandez JF. 1996. Estrategias de germinación y latencia de semillas en especies del bosque templado de Chiloé. Chile Revista Chilena de Historia Natur 69: 243–251.

Figueroa JA, Vazquez-Yanes C. 2001. Efecto de la calidad de la luz sobre la germinación de semillas en el árbol pionero tropical Heliocarpus appendiculatus (Tiliaceae). Revista de Biología Tropical (In press.)

Freckleton RP. 2000. Phylogenetic tests of ecological and evolutionary hypotheses: checking for phylogenetic independence. Functional Ecology 14: 129–134.

Harvey PH, Pagel MD. 1991. The comparative method in evolutionary biology. Oxford, USA: Oxford University Press.

Kelly CK, Purvis A. 1993. Seed size and establishment condition in a tropical trees: on the use of taxonomic relatedness in determining ecological patterns. Oecologia 94: 356–360.


© New Phytologist (2001) 152: 483–489 www.newphytologist.com

Research 489

Kelly CK, Southwood TRE. 1999. Species richness and resource availability: a phylogenetic analysis of insects associated with trees. Proceedings of the National Academy of Sciences, USA 96: 8013–8016.

Kyereh B, Swaine MD, Thompson J. 1999. Effect of light on the germination of forest trees in Ghana. Journal of Ecology 87: 772–783.

Landrum LR. 1981. The phylogeny and geography of Myrceugenia (Myrtaceae). Brittonia 33: 105–129.

Lusk CH, Del Pozo A. 2002. Survival and growth of seedlings of 12 Chilean rainforest trees in two light environments: gas exchange and biomass distribution correlates. Austral Ecology (In press.)

Machado JL, Reich PB. 1999. Evaluation of several measures of canopy openness as predictors of photosynthetic photon flux density in a forest understorey. Canadian Journal of Forest Research 29: 1438–1444.

Manly B. 1992. Randomisation and Monte-Carlo methods in biology. New York, USA: Chapman & Hall.

Martins EP. 2001. COMPARE, version 4.4. Computer programs for the statistical analysis of comparative data. Distributed by the author via the WWW at http://compare.bio.indiana.edu/.Departmentof Biology. Bloomington, IN, USA: Indiana University.

Pagel MD. 1992. A method for the analysis of comparative data. Journal of Theoretical Biology 15: 431–442.

Raich JW, Gong WK. 1990. Effects of canopy openings on tree seed germination in a Malaysian dipterocarp forest. Journal of Tropical Ecology 22: 146–154.

Smith-Ramírez C, Armesto JJ. 1994. Flowering and fruiting patterns in the temperate rainforest of Chiloé, Chile: ecologies and climatic constraints. Journal of Ecology 82: 353–365.

Soltis PS, Soltis DE, Chase MW. 1999. Angiosperm phylogeny inferred from multiple genes as a tool for comparative biology. Nature 402: 402–404.

Swaine MD, Whitmore TC. 1988. On the definition of ecological species groups in tropical rain forest. Vegetatio 75: 81–86.

Vazquez-Yanes C, Orozco-Segovia A. 1990. Ecological significance of light-controlled seed germination in two contrasting tropical habitats. Oecologia 83: 171–175.

Vazquez-Yanes C, Orozco-Segovia A. 1992. Effect of litter from a tropical rainforest on tree seed germination and establishment under controlled conditions. Tree Physiology 11: 391–400.

Vazquez-Yanes C, Orozco-Segovia A. 1993. Patterns of seed longevity and germination in the tropical rainforest. Annual Reviews of Ecology and Systematics 24: 69–87.

Vazquez-Yanes C, Orozco-Segovia A, Rincón E, Sanchez-Coronado ME, Huante P, Toledo JR, Barradas VL. 1990. Light beneath the litter in a tropical forest: effect on seed germination. Ecology 71: 1952–1958.

Veblen TT. 1985. Forest development in tree-fall gaps in the temperate rain forests of Chile. National Geographic Research 19: 365–371.

Veblen TT, Donoso C, Schlegel FM, Escobar B. 1981. Forest dynamics in south-central Chile. Journal of Biogeography 8: 211–247.

Veblen TT, Schlegel FM. 1982. Reseña ecológica de los bosques del sur de Chile. Bosque (Chile) 4: 73–115.

Washitani I, Takenaka A. 1987. Gap-detecting mechanism in the seed germination of Mallotus japonicus (Thunb.) Muell. Arg., a common pioneer tree of secondary succession in temperate Japan. Ecological Research 2: 191–201.


Documents

Germination requirements and seedling shade tolerance are not correlated in a Chilean temperate rain forest