rain forest fragmentation and the structure of amazonian liana communities

12 Pages·2001·0.15 MB·English

Ecology,82(1),2001,pp.105–116
(cid:113)2001bytheEcologicalSocietyofAmerica
RAIN FOREST FRAGMENTATION AND THE STRUCTURE
OF AMAZONIAN LIANA COMMUNITIES
WILLIAM F. LAURANCE,1,2DIEGO PE´REZ-SALICRUP,3PATRICIA DELAMOˆNICA,1PHILIP M. FEARNSIDE,4
SAMMYA D’ANGELO,1ADRIANO JEROZOLINSKI,1LUCIANO POHL,1 AND THOMAS E. LOVEJOY5
1BiologicalDynamicsof ForestFragmentsProject,NationalInstitutefor AmazonianResearch(INPA),
C. P.478, Manaus,AM 69011-970, Brazil
2Smithsonian TropicalResearchInstitute,Apartado 2072, Balboa,Panama
3Harvard Forest,HarvardUniversity,Cambridge,Massachusetts02138 USA
4Departmentof Ecology,INPA,C. P. 478, Manaus,AM 69011-970, Brazil
5Counselor to the Secretaryfor Biodiversityand Conservation,SmithsonianInstitution,Washington,D.C.20560 USA
Abstract. Intropicalforests,lianas(woodyvines)areimportantstructuralparasitesof
trees. We assessed the effects offorest fragmentation,treefalldisturbance,soils,andstand
attributesonlianacommunitiesincentralAmazonianrainforests.Over27500lianastems
((cid:36)2cmdiameteratbreastheight[dbh])wererecordedin271-haplotsincontinuousforest
and 42 plots in 10 forest fragments ranging from 1 to 100 ha in area. For each plot, an
indexofforestdisturbancewasdeterminedfroma20-yrstudyoftree-communitydynamics,
and 19 soil-texture and chemistry parameters were derived from soil surface samples(top
20 cm).
Liana abundance was 187–701 stems/ha, and liana aboveground dry biomass varied
from3.7to12.3Mg/ha.Lianaabundanceincreasedsignificantlynearforestedgesandwas
significantly positively associated with forest disturbance and significantly negatively as-
sociated with tree biomass. Liana biomass was similarly associated with disturbance and
tree biomass but also increased significantly alongsoil-fertilitygradients.Plotsnearforest
edges had a significantly higher proportion of small (2–3 cm dbh) lianas and relatively
fewer large ((cid:36)4 cm dbh) lianas than did sites in forest interiors.
Liana communities were further assessed by comparing their species richness, com-
position,climbingguilds,andfrequencyoftreeinfestationinthree10-hafragments.Within
each fragment, data were collected in 24 small (400-m2) plots, with half of the plots near
edges and half in interiors. Significantly more trees were infested on fragment edges than
ininteriors.Allthreemajorguilds(branch-twiners,mainstem-twiners,tendril-twiners)were
significantly more abundant on edges. Species diversity oflianas (asmeasuredbyFisher’s
diversity index) also was significantly higheron edges, and this wasnotsimplyanartifact
of increased liana abundance on edges.
We conclude that many aspects of liana community structure are affected by habitat
fragmentation, and we suggest that lianas can have important impacts on forest dynamics
and functioning in fragmented rain forests. By creating physical stresses on trees and
competingforlightandnutrients,heavylianainfestationsappearpartlyresponsibleforthe
dramatically elevated rates of tree mortality and damage observed near fragment edges.
Keywords: Amazon;biomass;edgeeffects;forestdynamics;habitatfragmentation;lianacom-
munities;treeinfestation;tropicalrainforest;tree mortality;vines.
INTRODUCTION Lianas are diverse and abundant in many tropical
forests.OnBarroColoradoIsland,Panama,45%ofall
Lianas (woody vines) are a conspicuous feature of
plant species (cid:46)10 m tall are lianas (Croat 1978). In
tropical rain forests and important structural parasites
of trees. Occasionally growing to (cid:46)40 cm in diameter both neotropical and southeast Asian forests,40–60%
of all large ((cid:36)10 cm diameter) trees typically bear at
and several hundred meters in length, lianas exploit
leastoneliana(Putz1983,PutzandChai1987,Camp-
trees for physical support in order to reach the forest
bell and Newbery 1993, Pe´rez-Salicrup 1998). Al-
canopy. By creating structural stresses on trees and
though they comprise less than one tenth of above-
competingforlight,moisture,andsoilnutrients,lianas
groundbiomass,lianasproduceupto40%ofallleaves
can reduce tree growth (Putz 1984, Whigham 1984,
intheforest(Ogawaetal.1965,KlingeandRodriguez
Pe´rez-Salicrup1998)andreproduction(Stevens1987),
1974,Katoetal.1978,Putz1983,AvalosandMulkey
and increase rates of tree felling and limb breakage
1999). Many lianas propagate vegetatively as well as
(Lowe and Walker 1977, Putz 1980, 1984).
by seed (Putz 1984), enhancing their ability to prolif-
erate under favorable conditions.
Manuscriptreceived22 September1999;revised10January
2000;accepted12January2000. Mostlianaspeciesarelightlovingandrespondpos-
105
106 WILLIAMF.LAURANCEET AL. Ecology,Vol.82,No.1
itively to forest disturbance (Webb 1958, Putz 1984). 37mtall,withemergentsto55m.Speciesrichnessof
Treefallgapsprovidebothincreasedlightandabundant treesisveryhighandcanexceed280species((cid:36)10cm
smalltreesandlianastemsthatprovidecrucialsupports dbh) per hectare (de Oliveira and Mori 1999).
forclimbinglianas.Astheycolonizegaps,lianasoften The study area is surrounded by large expanses ((cid:46)
inhibit the regeneration of small trees via shading and 200 km) of continuous forest to the west, north, and
mechanical damage (Nicholson 1958, Dawkins 1961, east. In the early 1980s, 11 1-, 10-, and 100-ha frag-
Fox1968,Putz1984).Lianainfestationsalsopromote ments (Fig. 1) were isolated by distances of 70–1000
formation of large treefall gaps by entangling the m from surrounding forest by clearing theintervening
crowns of adjoining trees; in peninsular Malaysia, li- vegetation to establish pastures in three large ((cid:59)5000
ana-laden trees dragged down nearly twice as many ha) cattle ranches. Fragments were fenced to prevent
neighbors when felled as did similarly sized treesthat encroachment by cattle. Nine reserves ranging from 1
were liana-free (7.2 vs. 3.9; Appanah and Putz 1984). to1000hainareaweredelineatedinnearbycontinuous
Lianastendtoproliferateinloggedforests(Pinardand foresttoserveasexperimentalcontrols.Regrowthfor-
Putz 1994) and are loathed by foresters because they ests have regenerated in some cleared areas and are
suppress tree growth, deform boles, and increase tree dominated by Cecropia spp. or Vismia spp.
mortality (Putz 1991). Thedominantsoilsinthestudyareaarexanthicfer-
Lianas have been shown to increase in fragmented ralsols (using the FoodandAgriculturalOrganization/
forests in tropical Queensland (Laurance 1991, 1997) UnitedNationalEducationalScientificandCulturalOr-
andsoutheasternBrazil(Oliveira-Filhoetal.1997,Ta- ganizationsystem;Beinroth1975).Ferralsolsarewide-
banez et al. 1997, Viana et al. 1997), apparently in spread in the Amazon basin, heavily weathered, and
response to increased treefalls and lateral light pene- usuallyhavealowbasesaturation.Theyoftenarewell
tration near forest edges. In the Amazon, rates of tree aggregated,porous,andfriable,withvariableclaycon-
mortalityanddamagerisesharplyinfragmentedforests tents.Clayparticlesinferralsolscanformverydurable
(Lovejoyetal.1986,FerreiraandLaurance1997,Laur- aggregations, giving the soil poor water-holding char-
ance et al. 1998b), causing many ecological changes acteristics, even with high clay contents (Richter and
andasubstantiallossoflivingtreebiomass(Laurance Babbar 1991). Xanthic ferralsols in the Manaus area
etal.1997,1998a).Quantitativemodelsincorporating are derived from Tertiary deposits and are typically
these data suggest that biomass losses in fragmented acidic and very poor in nutrients such as P, Ca, and K
tropical forests could be a globally significant source (Chauvel et al. 1987).
of greenhouse gases, releasing up to 150 million Mg
Network of permanent plots
of C emissions annually (Laurance et al. 1998d). To
date, however, the role of lianas in fragmented Ama- Since 1980, a long-term study of tree-community
zonian forests is unknown, and there have been very dynamics, biomass, and composition has been con-
few ecologicalstudiesofAmazonianlianas(e.g.,Rol- ducted in fragmented and continuous forests in the
let 1969, Putz 1983). study area. Over 62000 trees ((cid:36)10 cm dbh) are being
Here we present a large-scale integrative study of monitoredatregular(typically4–6yr)intervalswithin
liana communities in fragmented and continuous Am- 69permanent,square,1-haplotsspanninganextensive
azonian forests. Our study combines extensive liana ((cid:59)1000 km2) experimental landscape (Fig. 1). Forty-
surveysatlandscapeandlocalscales,withamajordata twooftheplotsarelocatedwithinfive1-hafragments
set on forest soils and a 20-yr investigation of forest (5 plots), three 10-ha fragments (18 plots), and two
dynamicsanddisturbance.Wefocusonfourquestions: 100-hafragments(19plots).Theremaining27control
(1) Do the abundance and biomass of lianas increase plots are arrayed in nine reserves that roughly mimic
in fragmented forests? (2) Does fragmentation affect the spatial arrangement of fragment plots, but in con-
liana species richness, composition, size distributions, tinuous forest. Plots within fragments and continuous
or climbing guilds? (3) Do soils, forest disturbances, forestarestratifiedsothatedgeandinteriorareaswere
and stand features influence liana communities? (4) both sampled. Becausefragmentationeffectsonforest
Howdolianasaffectthedynamicsandbiomassoffrag- dynamics in these recently isolated forests ((cid:44)20 yr)
mented forests? arestronglyinfluencedbythedistanceofplotstoforest
edge (cf. Lovejoy et al. 1986, Ferreira and Laurance
METHODS 1997,Lauranceetal.1997,1998a,b,c,d),thepresent
studyfocusesonedgedistanceasakeylandscapevar-
Study area
iable. The effects of additional soil and habitat vari-
The study area is located in the central Amazon,80 ables on lianas are also assessed.
km north of Manaus, Brazil (2(cid:56)30(cid:57) S, 60(cid:56) W), at 50–
Liana abundance and biomass
100 m elevation (Lovejoy et al. 1986). Rain forestsin
the area are not seasonally inundated. Rainfall ranges From 1997 to 1999, liana abundance, biomass, and
from 1900–3500 mm annually with a pronounced dry size distributions were estimated within all 69 1-ha
seasonfromJunetoOctober.Theforestcanopyis30– plots. Liana abundance was estimated by counting all
January2001 LIANASIN AMAZONIANFORESTS 107
FIG.1. LocationofthestudyareaincentralAmazonia.Unshadedareasindicateprimaryrainforest,whilestippledareas
showcattlepasturesorregrowthforest.Darkwavylinesareaccessroads.Darklyshadedblocksindicateexperimentalforest
fragmentsand controlsitesin continuousforest.
liana stems ((cid:36) 2 cm dbh) within each plot, following wereconvertedtobiomassestimateswithanallometric
the method of Putz (1983, 1984). It was not feasible model derived by destructively sampling 319 trees in
to excavate each stem to determine whether it was nearby rain forests (Santos 1996). Total AGBM esti-
linked to nearby stems (vegetatively propagated) or a mates for each plot were adjusted upward by 12% to
distinctive individual (genet). The diameter of each accountfortreesof(cid:44)10cmdbh(JordanandUhl1978).
stem at 1.3 m height was measured with a dbh-tapeto For each plot, AGBM values for all censuses werere-
the nearest 0.1 cm, then converted to an estimate of gressed against time (months since January 1980) in
aboveground dry biomass using an allometricformula order to estimate the mean rate of biomass change
developed in an Amazonian rain forest in Venezuela (Laurance et al. 1997). Plots near forest edges ((cid:44)100
(Putz 1983): m from edge) often lost considerable biomass (mean
3–14 Mg·ha(cid:50)1·yr(cid:50)1), especially if several large trees
Log biomass (kg)(cid:53) 0.12 (cid:49) 0.91log([dbh]2). (1)
died, whereas plots in forest interiors were usually
more stable (Laurance et al. 1997).
Forest disturbance Soil parameters
An index of past forest disturbance was derived by Within 40 of the 1-ha plots, we measured 19 soil
calculating the mean annual rate of change in above- parameters. These 40 plots spanned the width and
ground tree biomass in each plot, based on long-term breadth of the study area (including eight of 11 frag-
(14–20 yr) data on tree-community dynamics (Laur- mentsandsevenofninereservesincontinuousforest),
anceetal.1997,1998a,b).Inmatureforest,thisindex and varied greatly in distance to forestedge (53–3000
provides a more realistic indication of forest distur- m).Fieldandlaboratorymethodsusedforsoilanalyses
bancethantree-mortalityrates,becauseitplacesgreat- aredetailedelsewhere(Lauranceetal.1999,Fearnside
er emphasis on deaths of large trees. andLeal-Filho,inpress),andbrieflysummarizedhere.
All plots were initially censused between January Each 1-ha plot was divided into 25 quadrats of 20 (cid:51)
1980 and January 1987, then recensused 3–5 times, 20 m each. Within each plot, 9–13 quadrats were se-
with the most recent recensus completed in June1999 lectedforsampling,usinganalternatingpatterntopro-
(mean(cid:53)4.0censuses/plot).Estimatesofaboveground vide good coverage of the plot. In each quadrat, 15
dry biomass (AGBM) for each plot were derived by samples were collected at haphazard locations with a
carefullymeasuring(tothenearest1mm)thediameters soil auger (2 cm diameter, 20 cm deep cores), then
of all trees (cid:36)10 cm dbh. Buttressed trees were mea- bulked and subsampled. Composite samples for each
sured just above the buttresses. Measurements of dbh quadrat were oven-dried, cleaned by removing stones
108 WILLIAMF.LAURANCEET AL. Ecology,Vol.82,No.1
and charcoal fragments, then passed through 20 mm nerability to edge effects, and soils that could poten-
and2mmsieves.Inallcases,valuesforsoilparameters tially influence liana communities: (1) the number of
were derived separately for each quadrat, then com- trees((cid:36)10cmdbh)perplot;(2)abovegroundbiomass
bined to yield a mean value for each 1-ha plot. oftreesineachplot;(3)theindexofforestdisturbance;
Textural analyses were conducted to separate sam- (4)logdistancetothenearestforestedge;and(5)two
ples into clay (particles (cid:44)0.002 mm diameter), silt ordination axes that described major gradients in soil
(0.002–0.05mm),andsand(0.05–2mm)fractions,us- fertilityandtexture.Thesoilordinationwasperformed
ingthepipettemethod.Water-holdingcapacity,amea- using Principal Components Analysis (PCA) on the
sureoftheamountofwaterthesoilcanholdinaform PC-ORD package (McCune and Mefford 1995). Soil
extractable by plant roots, was estimated as the dif- parameterswereequallyweightedbeforeanalysiswith
ference between the field capacity (moisture content thestandardizationbymaximummethod(Noy-Meiret
retained in soil under a suction of 0.33 atmospheres) al. 1975).
and the wilting point (moisture content retained at 15 Theefficacyofthesixpredictorswasassessedusing
atmospheres), using a pressure membrane apparatus. best-subsetsandmultiplelinearregressions(Sokaland
As is standard practice, samples were dried, sieved, Rohlf 1995). None of the predictors were strongly in-
and rewetted before determining water-holdingcapac- tercorrelated (R2(cid:44) 27%). Performance of the finalre-
ity,makingtheresultsonlyanindexofwateravailable gression model was assessed by comparing the stan-
to plants in the field. dardized residuals to the fitted values and to each sig-
A pH meter was used to measure soil pH in water. nificant predictor (Crawley 1993).
Total N was determined by Kjeldahl digestion (Par-
Local-scale comparisons
kinson and Allen 1975) and total organic C by dry
combustion. Total P was determined by digestion in In addition to landscape-scale data, detailed infor-
HNO , HClO , and HF (Lim and Jackson 1982), and mationonlocallianacommunitieswascollectedJuly–
3 4
reaction with ammonium molybdinate. We measured August1997byD.Pe´rez-Salicrupinthree10-hafrag-
PO 3(cid:50) in an autoanalyzer using the molybdenum blue ments in the study area. The fragments (BDFFPnum-
4
method(Jorgenson1977).K(cid:49)wasdeterminedbyatom- bers 1202, 2206, and 3209) were located on threedif-
ic emission spectroscopy at the Brazilian Center for ferentcattleranchesandseparatedbydistancesof11–
Nuclear Energy and Agriculture (CENA), Piracicaba, 28km.Lianadatawerecollectedinatotalof72small
Sa˜o Paulo, Brazil, while Ca2(cid:49), Mg2(cid:49), Al3(cid:49), and H(cid:49) in (20 (cid:51) 20 m) plots, with 12 plots near fragment edges
soil were measured by atomic absorption spectropho- (plot margin 10–30 m from the nearest edge) and 12
tometryatCENAafterdigestioninHClO ,HNO ,and intheinterior((cid:46)100mfromthenearestedge)ofeach
4 3
H SO (Jorgenson1977).Organic(Walkley-Black)car- fragment.Tominimizeeffectsofedgeaspect,theedge
2 4
bon to total nitrogen (C:N) ratios were calculated to plots were divided equally among 3–4 differentedges
provide an index of N availability; if C:N (cid:46) 15, there of each fragment. Precise positions of all plots were
is very little N available for plant growth (Fearnside determinedusingrandomx–ycoordinates.Becausethe
and Leal-Filho, in press). samples were intended to assess fine-scale variation
Cation measures were derived without Na(cid:49), which withintheseparticularfragments,concernsaboutpseu-
isgenerallyaminorconstituentofexchangeablebases. doreplication (Hurlbert 1984) are irrelevant, but the
These measures included cation exchange capacity reader should be aware that the results may not be
(CEC), which is the sum of K(cid:49), Ca2(cid:49), Mg2(cid:49),Al3(cid:49),and typical of other Amazonian fragments.
H(cid:49); total exchangeable bases (TEB), the sum of K(cid:49), The following data were collected in each plot for
Ca2(cid:49), and Mg2(cid:49); and aluminum saturation, which is lianas of (cid:36)2 cm dbh: (1) number of liana stems; (2)
((Al3(cid:49) (cid:49) H(cid:49))/CEC) (cid:51) 100. Samples were digested in number of liana taxa; (3) number of living trees ((cid:36)10
0.0025mol/LHCland0.005mol/LH SO ,andextracts cm dbh); (4) frequency of infestation (percentage of
2 4
for cation determination were buffered to pH 7.0, the trees with at least one liana); (5) median number of
standard practice in Brazil (Serv´ıcioNacionaldeLev- lianas per infested tree (medians were used because
antamentoeConservac¸a˜odeSolos–EmpresaBrasileira liana counts per tree could not be normalized by data
de Pesquisa Agropecua´ria 1979). We also measured transformations); and (6) number of lianas in each of
DpH (the difference between soil pH in KCl and in threeclimbingguilds.Lianataxawereidentifiedinthe
water),whichindicatesthechargestatusofthesoiland field to species level or, for some genera andfamilies,
is a useful indicator of organic matter concentration to morphospecies level, usually on the basis of sterile
(Fearnside and Leal-Filho, in press). features.Vouchersforeachtaxonwerelatercompared
tospecimensintheINPAHerbarium,andthevouchers
Landscape-scale comparisons
arepermanentlylodgedthere.Becauselianaabundance
Sixvariablesweretestedaspredictorsoflianaabun- varied considerably among plots, we calculated liana
dance and biomass in the same 40 1-ha plots used for diversityusingFisher’slogseries(cid:97),anindexofspecies
soil analysis. These variables were chosen to reflect diversity that is insensitive to sample size (Magurran
key features of tree stands, treefall disturbance, vul- 1988).
January2001 LIANASIN AMAZONIANFORESTS 109
LianaclimbingguildsfollowedtheschemesofPutz
(1984) and Hegarty (1991), as follows: (1) Tendril-
twiners have modified leaves, leaflets, inflorescences,
or stipules that twine around supports. Such species
often favor smaller ((cid:44)7 cm diameter) supports. (2)
Mainstem-twinersusethemainstemaxistocoilaround
thehost,andtendtofavorintermediate-sizedsupports
((cid:44)16 cm diameter). (3) Branch-twiners use leaf-bear-
ing branches to twine around the host, and generally
use the largest supports ((cid:46)12 cm diameter).
An ordination analysis was used to identify major
gradientsinlianaspeciescomposition.Nonmetricmul-
tidimensionalscaling(NMS)wasused,withSorensen’s
distance metric (Ludwig and Reynolds 1988), on the
PC-ORD package. Uncommon species (detected at
(cid:44)10 plots), which can seriously distort ordinations
(McCune and Mefford 1995), were deleted prior to
analysis. Species used in the analysis were weighted
equallywiththestandardizationbymaximummethod.
A two-way multivariate analysis of variance (MAN-
OVA)wasusedtocompareedgevs.interior,site(frag-
ment), and interaction effects for all ordination axes
simultaneously (Sokal and Rohlf 1995).
For all other liana community parameters, two-way
ANOVAs were used to compare edge vs. interior, site
(fragment),andinteractioneffects,followedwhereap-
propriate by Tukey’s HSD tests to contrast sample FIG. 2. Relationship between liana abundance (above)
means. To minimize heteroscedasticity and improve andabovegrounddrybiomassoflianas(below)asafunction
normality of samples, abundance and species-richness of distanceof plotsfromthenearestforestedge.
data were log-transformed, while infestation data and
guildproportionswerearcsine-squareroottransformed
(Sokal and Rohlf 1995). Bartlett’s tests were used to Liana biomass (Fig. 2) also was high in many edge
test for heteroscedasticity. plots but, unlike liana abundance, did not differ sig-
In comparing the three 10-ha fragments, both the nificantlybetweenforestedgesandinteriors(t(cid:53)1.05,
ANOVAandMANOVAanalysesweredesignedtoas- df (cid:53) 67, P(cid:53) 0.30; ttest).Severalforest-interiorplots
sess site (fragment), edge vs. interior, and interaction also had high biomass, and as a result the correlation
effects separately. This approach was clearly justified between distance to edge and biomass was nonsignif-
because there were considerable differences in liana icant (r (cid:53) 0.070, n (cid:53) 69, P (cid:53) 0.57; Spearman rank
s
communitiesamongfragments,whichmightotherwise correlation).
confound direct comparisons of fragment edges and Liana size distributions.—Lianas ranged from2–43
interiors. However, because there were very few sig- cm dbh, but most (97.1%) were (cid:44)10 cm in diameter.
nificantinteractioneffects,andbecausethesiteeffects Sizedistributionsoflianasdifferedbetweenforestedg-
are not of general interest, only the edge vs. interior es and interiors (Fig. 3). Plots near edges had more
contrasts are reported here. small(2–3cmdbh)lianasandrelativelyfewermedium
and large ((cid:36)4 cm dbh) lianas, than did those in forest
RESULTS interiors ((cid:46)100 m from edge). This difference was
highly significant (X2 (cid:53) 113.0, df (cid:53) 9, P (cid:44) 0.0001;
Landscape-scale comparisons
chi-square test for independence).
Liana abundance and biomass.—A total of 27590 Ordination of soil variables.—The ordination anal-
lianasweremeasuredinthe691-haplots.Lianaabun- ysisrevealedtwomajorsoilgradientsinthestudyarea
dance(Fig.2)wassignificantlyhighernearforestedges (Table1).Axis1,whichcaptured48%ofthevariation
((cid:44)100 m from edge) than further (145–3000 m) from in the data set, described a continuum between rela-
edges (t (cid:53) 2.20, df (cid:53) 67, P (cid:53) 0.032; t test). There tively fertile sites with high clay content (havinghigh
was, however, no simple, monotonic relationship be- total C, N, CEC, and exchangeable bases), and less
tween distance from edge and liana abundance (r (cid:53) fertile sites with high sand content (having high alu-
s
(cid:50)0.079,n(cid:53)69,P(cid:53)0.52;Spearmanrankcorrelation), minumsaturation).Axis2,whichcaptured18%ofthe
because several plots in deep forest interiors ((cid:46)1000 totalvariation,describedagradientbetweenlessacidic
m from edge) also had many lianas. siteswithmoretotalP,andmoreacidicsiteswithsome-
110 WILLIAMF.LAURANCEET AL. Ecology,Vol.82,No.1
TABLE1. Pearsoncorrelationsbetween19soilvariablesand
three ordination axes produced by principal components
analysis.
Variable Axis 1 Axis 2 Axis 3
Percentagesof soiltexturecomponents
Clay 0.969§ (cid:50)0.025 (cid:50)0.047
Silt 0.631§ (cid:50)0.239 (cid:50)0.555§
Sand (cid:50)0.953§ 0.076 0.167
Water-holdingcapacity 0.424 (cid:50)0.430 (cid:50)0.421
Carbon
OrganicC (%) 0.789§ 0.183 0.255
C:N ratio (cid:50)0.321 0.471 0.303
Acidity
pH in water 0.030 (cid:50)0.920§ 0.275
Primarynutrients
TotalN (%) 0.960† (cid:50)0.133 0.051
TotalP (%) 0.456 (cid:50)0.809§ (cid:50)0.053
PO(cid:50)3† (cid:50)0.013 (cid:50)0.235 0.684§
K2(cid:49)4† 0.685§ (cid:50)0.537§ 0.308
Secondarynutrients
Ca2(cid:49)† 0.673§ 0.580§ 0.018
Mg2(cid:49)† 0.899§ 0.097 0.254
Otherions
Al3(cid:49)† 0.617§ 0.675§ (cid:50)0.100
H(cid:49)† 0.729§ (cid:50)0.212 (cid:50)0.220
Cationmeasures
FIG.3. Sizedistributionsoflianasinforestedgeandin- Cationexchangecapacity 0.799§ 0.464 (cid:50)0.114
terior plots (edge plots are (cid:44)100 m from the nearest edge; Aluminumsaturation (cid:50)0.797§ (cid:50)0.032 (cid:50)0.351
interiorplotsare(cid:46)100 m fromedge). Totalexchangeablebases 0.927§ 0.208 0.205
DpH‡ 0.025§ (cid:50)0.068 (cid:50)0.150
Variationexplainedby 47.7 18.3 8.6
ordinationaxis(%)
what higher Al3(cid:49) and Ca2(cid:49). Axis 3 captured (cid:44)9% of
†Expressedin (cid:109)molesof charge/kgof fine earth.
the total variation, and is not considered further. ‡DifferencebetweensoilpH in KCl and in water.
Multiple regressions.—We assessed the effects of §Correlations significant with a Bonferroni-corrected al-
soils, disturbance, treestands, and distancetoedgeon phavalue(P(cid:44)0.002).Thiswasusedtoreducethelikelihood
of spuriouscorrelations.
lianadistributionsusingmultipleregressions.Forliana
abundance there were three significant predictors,
yieldingahighlysignificantmultipleregressionwhich soil axis 2 (slope negative), and tree biomass (slope
explained56%ofthevariationinlianaabundance(F3,36 negative), yielding a highly significant multiple re-
(cid:53) 14.98, P (cid:44) 0.0001). The first predictor was tree gression (F (cid:53) 8.78, R2 (cid:53) 65%, P (cid:53) 0.0016). For
2,15
biomass, which was negatively associated with liana liana biomass, there were two predictors, soil axis 2
abundance (Fig. 4), followed by the index of forest (slopenegative)andforestdisturbance(slopepositive),
disturbance(positiveslope)anddistancetoforestedge again producing a highly significant multiple regres-
(negative slope). sion (F (cid:53) 13.06, R2 (cid:53) 64%, P (cid:53) 0.0005). These
2,15
For liana biomass there were four predictors, pro-
ducingahighlysignificantmultipleregression(F (cid:53)
4,35
11.89, P (cid:44) 0.0001) which explained 58% of the total
variation.ThefirstpredictorwassoilPCAaxis2(neg-
ativeslope),followedbytreebiomass(negativeslope),
forest disturbance (positive slope), and soil PCA axis
1 (positive slope). Thus, in addition to tree biomass
and disturbance, gradients in soil fertility appeared to
influence liana biomass, with higher biomass associ-
ated with less acidic soils with higher P, clay, and ex-
changeable bases.
Forest-interiorplots.—Contrarytoourexpectations,
some forest-interiorplots hadmanylianas(Fig.2).To
furtherassessthefactorsresponsible,wetestedeffects
of five predictors (tree density, tree biomass, forest-
disturbanceindex,andsoilPCAaxes1and2)onliana
abundance and biomass in 18 forest-interior plots
((cid:46)100 m from edge). For liana abundance, therewere ofFrIaGin. 4f.oreRsteltaretieosnsahnidplbiaentwaeaebnunadbaonvceegrionunpdermdraynebniotm1-ahsas
three predictors, forest disturbance (slope positive), plots.
January2001 LIANASIN AMAZONIANFORESTS 111
TABLE2. ResultsofANOVAscomparingattributesofAmazonianlianacommunitiesbetween
edges and interiorsof three10-harainforestfragments.
Attribute F P Tukey’stests(P)
1,66
Lianaabundanceand diversity
Abundance 9.84 0.003 Edge (cid:46) Interior((cid:44)0.01)
Speciesrichness 14.82 (cid:44)0.001 Edge (cid:46) Interior((cid:44)0.01)
Speciesdiversity† 6.17 0.016 Edge (cid:46) Interior((cid:44)0.05)
Treeinfestations
Percentoftreesinfested 8.61 0.005 Edge (cid:46) Interior((cid:44)0.01)
Medianno.lianas/infest- 0.32 0.573 …
ed tree
Abundancesof lianasin threeclimbingguilds
Branchtwiners 3.91 0.052 Edge (cid:46) Interior(0.053)
Mainstemtwiners 5.32 0.024 Edge (cid:46) Interior((cid:44)0.05)
Tendriltwiners 4.39 0.040 Edge (cid:46) Interior((cid:44)0.05)
Proportionsof lianasin threeclimbingguilds
Branchtwiners 3.30 0.074 Interior(cid:46) Edge (0.08)
Mainstemtwiners 2.01 0.161 …
Tendriltwiners 1.91 0.172 …
Note:Dataonlianaabundanceandspeciesrichnesswerelog -transformed,whileinfestation
10
data and guild proportionswerearcsine-transformed.
†Using Fisher’s(cid:97), a robustindex of speciesdiversitythatis insensitiveto samplesize.
results are generally concordant with the regressions was no significant difference overall (F (cid:53) 2.40, P
2,34
involving all 40 plots; forest-interior plots with high (cid:53)0.11;one-wayANOVA).Resultsweresimilarwhen
lianaabundanceandbiomassweremoredisturbedand distance to edge was included as a covariate.
occurredonbetter(higherPandlessacidic)soils,while Edge aspect.—Our study area receives prevailing
liana abundance also was negatively associated with easterly winds that might increase forest disturbance
tree biomass. andmicroclimaticchangesoneast-facingforestedges.
Numberofnearbyedges.—Todeterminewhetherli- We therefore compared liana abundance in plots near
anaabundancewasinfluencedbythenumberofnearby edges with eastern aspects (n (cid:53) 12) versus all other
forest edges ((cid:44)100 m away), we compared plots with aspects (n (cid:53) 18), but liana abundance did not vary
one nearby edge (n (cid:53) 21), two nearby edges (i.e., on significantly(t(cid:53)0.92,df(cid:53)8,P(cid:53)0.36;ttest)between
thecornerofafragment;n(cid:53)9),andfournearbyedges eastern (387 (cid:54) 105 stems/ha) and non-eastern (429 (cid:54)
(i.e., in a 1-ha fragment; n (cid:53) 5). Although plots with 131) aspects.
fouredgeshadsomewhathigherlianaabundances(526
(cid:54) 134 stems/ha; mean (cid:54) 1 SD) than did those with Local-scale comparisons
only one (431 (cid:54) 129) or two (377 (cid:54) 91) edges, there
Liana abundance and tree infestation.—We found
1023lianas((cid:36)2cmdbh)inthe72small(400-m2)plots
inthethree10-hafragments(Table2).Whencompared
to a Poisson distribution (Fig. 5), there were signifi-
cantly more trees than expected with no lianas, and
manymoretreesthanexpectedwithheavyinfestations
(4–17 lianas). Thus, lianas were strongly aggregated,
with some trees bearing very heavy infestations.
Lianasweresignificantly(P(cid:44)0.01)moreabundant
onfragmentedges(413(cid:54)211stems/ha)thaninteriors
(298 (cid:54) 222; Table 2). Lianas also infested a signifi-
cantly higher (P (cid:44) 0.01) proportion of trees ((cid:36)10 cm
dbh) near edges (40.5 (cid:54) 9.7%) than in interiors (34.2
(cid:54)10.3%),althoughtherewasnosignificantdifference
inthemediannumberoflianasperinfestedtree(Table
2).
Lianaguilds.—Ofthe1023lianas,overhalf(59.6%)
were branch-twiners, followed by mainstem-twiners
(21.7%) and tendril-twiners (18.2%). A small number
oflianas(0.5%)ascendedviamodifiedspines,andare
FIG. 5. Numbers of lianas borne by rain forest trees in
centralAmazonia(bars),comparedtoexpected(random)val- not considered further.
ues fromthe Poissondistribution(circlesand lines). Allthreemajorclimbingguildsbecamesignificantly
112 WILLIAMF.LAURANCEET AL. Ecology,Vol.82,No.1
(cid:44) 0.007) to reduce the likelihood of experiment-wise
errors. Of 34 common taxa, three increased signifi-
cantlyinabundanceonedges(Cheiocliniumcognatum
[Celastraceae]; Bignoniaceae 1 and 4), whilenonede-
clined on edges.
DISCUSSION
Our findings suggest that rain-forest fragmentation
alters many aspects of liana community structure. Li-
anasinfragmentsweremoreabundantanddiverse,and
infested a higher proportion of trees than in forest in-
teriors.Lianacommunitiesnearforestedgescontained
many small lianas, and relatively few large lianas.All
three major climbing guilds of lianas (branch-twiners,
mainstem-twiners, tendril-twiners) increased signifi-
FIG.6. Meanabundancesofmajorlianaclimbingguilds cantly near edges. These patterns are quite similar to
onedgesandinteriorsofthree10-haforestfragments(error those found in 20–40-yr-old regrowth forests in Pan-
bars indicate(cid:54) 1 SE). ama, which also had elevated liana abundance and di-
versity, but not biomass, relative to mature forests
(DeWalt et al. 2000). For lianas, forest fragments and
(P (cid:44) 0.05) more abundant on fragment edges (Table regrowth may be similar ecologically in that each has
2).Branch-twinersincreasedby28%onaverage,while anabundanceoftreefallgapsandsmalltrees(Laurance
mainstem-twiners rose by 52% and tendril-twiners by etal.1997),whichprovidemanytrellisesandincreased
55%(Fig.6).Theproportionsofeachguildalsovaried light for actively climbing lianas.
somewhat, with branch-twining lianas becoming rela- On a broad landscape scale, there was considerable
tively less abundant (P (cid:44) 0.08) on edges than in in- variationinlianaabundanceandbiomass.Asrevealed
teriors (Table 2). by our multiple regression models, the abundanceand
Lianaspeciesdiversity.—Atotalof83lianaspecies biomass of lianas were affected somewhat differently
ormorphospecieswereidentifiedinthethreefragments byfragmentation,soils,andforestdisturbance,despite
(total area sampled (cid:53) 2.88 ha). About a quarterofthe the fact that liana abundance and biomass were quite
taxa(22species)canbeconsideredrare(meandensity strongly and positively correlated (R2 (cid:53) 53%).
of (cid:59)(cid:35)1 stem/ha). Liana species richness was signifi-
cantly (P (cid:44) 0.01) higher on fragment edges than in- Landscape-scale variation in liana abundance
and biomass
teriors (Table 2). The high species richness on edges
resultedinpartfromelevatedlianaabundanceinthese Onalandscapescale,therelationshipbetweenliana
areas;therewasastrong,positiverelationshipbetween abundance and distance to forest edgewassignificant,
liana richness and the number of lianas per plot (R2(cid:53) but weaker than expected. While lianas were often
77.2%,df(cid:53)70,P(cid:44)0.0001).However,theedgeplots abundant near edges, several plots in deep forest in-
also had significantly higher Fisher’s (cid:97) values (18.06 teriors also had high abundances (Fig. 2). We had hy-
(cid:54) 12.89) than did the interior plots (12.80 (cid:54) 8.36), pothesizedthatedgedistancewouldbeakeycorrelate
suggesting that liana species diversity at edges was oflianaabundancebecausetreemortality(Ferreiraand
elevated irrespective of variation in liana abundance Laurance1997,Lauranceetal.1998b)andlaterallight
(Table 2). penetration (Kapos et al. 1997, Didham and Lawton
Liana species composition.—The nonmetric multi- 1999)increasesharplyinAmazonianforestfragments,
dimensional scaling (NMS) analysis was based on the especially within 60–100 m of edges. Although edge
29 most prevalentliana speciesormorphospecies(de- distancewasoneofthreesignificantpredictorsofliana
tectedat(cid:36)10plots).Theanalysisrevealedthreemajor abundance, tree biomass and the index of forest dis-
gradients in species composition, with the axes cap- turbance were more important.
turing 19.3%, 18.7%, and 10.1% of the total variation Thestrongnegativeassociationbetweenlianaabun-
in the data set, respectively. A comparison of the or- dance and tree biomass (Fig. 3) could arise for three
dination scores, using a two-way MANOVA,revealed reasons. First, sites with high tree biomass may have
that floristic composition did not differ significantly been infrequently disturbed in the past. Such stable
between fragment edges and interiors (F (cid:53) 0.36, P conditionswouldallowtreestogrowlargerandwould
3,64
(cid:53) 0.78). providefewopportunitiesforlianastoproliferate.Sec-
We also compared abundances of the mostcommon ond, lianas may actively depress tree biomass, by in-
liana taxa ((cid:36)10 individualsoverall)betweenfragment creasing mortality and damage (Putz 1980, 1984) and
edgesandinteriors,usingaseriesoftwo-wayANOVAs suppressing growth (Lowe and Walker 1977, Putz
with a stringent, Bonferroni-corrected alpha value (P 1984, Whigham 1984, Viana et al. 1997). Finally, li-
January2001 LIANASIN AMAZONIANFORESTS 113
anas and trees could be negatively correlated if they ourforest-interiorplots,abovegroundbiomassoflianas
responded in opposite ways to soils or other edaphic waslower,andcomprisedasmallerpercentageoftotal
factors. This latter proposition seems least likely, be- forest biomass, than in other tropical rain forests in
cause in the very poor, heavily weathered soils of our Brazil (Klinge and Rodriguez 1974), Venezuela (Putz
study area, both lianas and trees respond positively 1983),Bolivia(Pe´rez-Salicrup1998),Thailand(Ogawa
(increasedbiomass)tosoilfertility(cf.Lauranceetal. et al. 1965), Malaysia (Kato et al. 1978), and Ghana
1999 for data on soil–tree biomass relationships).The (Greenland and Kowai 1960). This is consistent with
firsttwopropositions,however,areveryplausible:for- theobservationthat,inintactforestsofourstudyarea,
est disturbancesbegetlianainfestations,whichinturn mortality rates of trees are naturally quite low (1.2 (cid:54)
maybegetfurtherdisturbances.Thisviewissupported 0.4%/yr; W. F. Laurance, unpublished data). Putz
bythefactthattheindexofforestdisturbancealsowas (1983) has argued that on a geographic scale, differ-
a significant predictor of liana abundance, and is con- ences in disturbance regimes affecting tree mortality
sistent with several earlier studies (e.g., Putz 1984, maybethemostimportantfactordeterminingtheabun-
HegartyandCaballe´ 1991,Oliveira-Filhoetal.1997). dance of lianas. The very acidic, heavily weathered
Distance to forest edge had no significant effect on soils prevalent in the central Amazon (Laurance et al.
liana biomass, but this result was less surprising. A 1999, Fearnside and Leal-Filho, in press) could also
preponderance of large ((cid:46)10 cm diameter) lianas ap- depresslianaabundance.Thus,theobservedeffectsof
pearstobeanindicatorofprimaryforestorareassub- lianasinthisstudyarelikelytobelessthaninregions
jectedtofewdisturbances(EmmonsandGentry1983, with greater disturbance (e.g., cyclonic and hurricane
Peixoto and Gentry 1990, Hegarty and Caballe´ 1991). forests;Webb1958)ormorefertilesoils.Insuchareas,
Areas prone to frequent perturbations apparentlyhave liana infestations in fragmented forests may become
many small, actively climbing lianas, asdemonstrated even more severe.
by our comparison ofliana sizedistributionsonforest Liana diversity in our study area appears moderate.
edges and interiors (Fig. 3). OnBarroColoradoIsland,Panama,Putz(1984)found
Of the factors tested, liana biomass appeared most 65 liana species ((cid:36)2 cm dbh) in 1.0 haof plots,while
strongly influenced by soil fertility. The gradient de- usingnearlyidenticalmethodsweidentified83species
scribingvariationintotalPandpHwasmostimportant, ormorphospeciesin2.88haofplotsspanningalarger
whichisconsistentwiththesuggestionthatintropical geographic area (random subsamples of our plots to-
lowland soils, P availability is often criticallylimiting taling 1.0 ha averaged 69.6 species). This moderate
to plant growth (Sollins 1998). Liana biomassalsoin- richness of lianas is in stark contrast to tree diversity
creasedalongagradientfromsandytoclaysoils,with in our study area (averaging (cid:59)280 species of (cid:36)10 cm
thelatterhavingloweraluminumsaturationandhigher dbhperhectare),whichisseveraltimeshigherthanon
N, organic matter, cation exchange capacity, and ex- Barro Colorado Island and among the highest in the
changeable bases. The notion that soil factors are im- world (de Oliveira and Mori 1999).
portant to lianas accords with Gentry (1991), who Although fragmentation caused diverse changes in
found that Amazonian sites on very poor white-sand liana communities, there were only limited shifts in
soilshadlowerlianadensities(andthuslowerbiomass) guild and species composition. All three majorclimb-
than did nearby sites with less extreme soils. Proctor ing guilds increased in abundance near edges, but the
et al. (1983) and Putz and Chai (1987) also suggested proportions of each guild did not change greatly (al-
that liana densities are higher on richer soils. though there were somewhat fewer branch-twining li-
The above results were generally supported when we anas [P (cid:44) 0.08], which use the largest supports). We
analyzed only plots in forest interiors ((cid:46)100 m from had particularly expected tendril-twining species,
edge).Althoughcautionisneededbecauseofthelimited which use the smallest trellises (Putz 1984, Hegarty
samplesize(n(cid:53)18plots),theregressionmodelssuggest 1991),toincreaseproportionallyonedges.Inaddition,
forest-interiorplotswithmanylianasweremoredisturbed none of the ordination axes describing gradients in li-
and had relatively high soil fertility (higher Pandlower ana composition differed significantly between edges
acidity) and lower tree biomass. In intact forests of the andinteriors,andonlythreespeciesincreasedonedges
central Amazon, periodic disturbances are caused by whilenonedeclined(withoutthestringentBonferroni-
windstorms (Nelson et al. 1994, Foster and Terborgh corrected P values, seven species increased on edges
1998), small floods (Mori and Becker 1991), lightning [P(cid:44)0.05]andnonedeclined).Thefactthatnospecies
strikes(Magnussonetal.1996),andpathogenoutbreaks. declined on edges is perhaps not surprising; although
Such disturbances, along with natural heterogeneity in somelianaspeciesthatattainlargediametersareshade
soils, apparently generate considerable variability in the tolerant (Gentry 1991), many primary-forest plants
local abundance of lianas. benefit from increased light availability (Clark 1994,
Sizer and Tanner 1999), such as occurs near edges. It
Amazonian liana communities
is also possible that the forest edges in our study area
It is important to emphasize that in our study area, arestillinadynamicstateoftransition.Ourfragments
the abundance and biomass of lianas are modest. In were only 13–17-yr-old during the study, and some
114 WILLIAMF.LAURANCEET AL. Ecology,Vol.82,No.1
authorshavearguedthatrain-forestedgesmayrequire Gentry 1983, Gentry 1991), but their abundance in
20–80 yr to fully equilibrate in structure and floristic fragmented forests can become unnaturally high, se-
composition (Oliveira-Filho et al. 1997). If this view riously affecting forest structure and functioning. In
is valid, then the age of forest edges could also have many tropical regions, lianas will play a key role in
a significant effect on liana communities. the ecology and dynamics of fragmented forests.
Implications for fragmented forests ACKNOWLEDGMENTS
WethankFrancisPutz,SaaraDeWalt,DeborahClark,Ru-
Proliferatinglianascanhavediverseimpactsonfrag- dolfoDirzo,EdTanner,ClaudeGascon,HeraldoVasconcelos,
mented forests. Forest fragments are especially prone ScottWilson,andtwoanonymousrefereesforinsightfulcom-
to windstorms (Laurance 1991, 1997, Laurance et al. ments on drafts of the manuscript, and our field technicians
for invaluable help with data collection. A list of lianataxa
1998b) and fire (Laurance 1998, Nepstad et al. 1999),
used in the analysis is located in the Appendix. The study
andliana-infestedtreesaremuchmorepronetodamage
was supported by the Conservation, Food and HealthFoun-
fromwindandfirethanareliana-freetrees(Putz1991). dation,NationalAeronauticsandSpaceAdministrationLong-
Heavy liana infestations can inhibit successional pro- termBiosphere–AtmosphereExperimentintheAmazon,An-
cesses near forest edges and reduce tree biomass and drewW.MellonFoundation,WorldWildlifeFund–U.S.,Mac-
Arthur Foundation, National Institute for Amazonian Re-
density (Tabanez et al. 1997, Viana et al. 1997). In a
search,andSmithsonianInstitution,andstudysiteaccesswas
positivefeedbackloop,lianasrespondpositivelytofor- provided by SUFRAMA (Superintend´ıncia da Zona Franca
est disturbance and then appear to promote and exac- de Manaus; the Manaus free-trade authority). This is publi-
erbate subsequent disturbances. cationnumber297 in the BDFFPtechnicalseries.
Lianasmayalsohelpdrivefloristicchangesinfrag- LITERATURECITED
ments.Becausetheyaregenerallylonglivedandslow Appanah, S., and F. E. Putz. 1984. Climber abundance in
growing, old-growth tree species are often prone to virgindipterocarpforestandtheeffectofpre-fellingclimb-
liana infestations (Laurance et al. 2000). Pioneertrees ercuttingonloggingdamage.MalaysianForester47:335–
342.
such as Cecropia spp. and Trema spp. are, however,
Avalos, G., and S. S. Mulkey. 1999. Seasonal changes in
lessvulnerabletolianasbecauseoftheirrapidgrowth,
lianacoverintheuppercanopyofaneotropicaldryforest.
monopodalform,largeleaves,andflexibletrunks,and Biotropica31:186–192.
also sometimes because of the activity of ants (Putz Beinroth, F. H. 1975. Relationships between U.S. soil tax-
1984). In our study area, the abundance of Cecropia onomy, the Brazilian system, and FAO (Food and Agri-
cultural Organization)/UNESCO (United National Educa-
sciadophylla, an ubiquitous pioneer, has increased33-
tional Scientific and Cultural Organization) units. Pages
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Laurance, unpublished data), and its ability to limit managementintropicalAmerica.NorthCarolinaStateUni-
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of 36.1 Mg/ha of dry tree biomass (Laurance et al. of a neotropical rain forest. University of Chicago Press,
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