797

Conservation Biology, Pages 797–801Volume 11, No. 3, June 1997

Effects of Forest Fragmentation on Mortality and Damage of Selected Trees in Central Amazonia

LEANDRO V. FERREIRA AND WILLIAM F. LAURANCE

Biological Dynamics of Forest Fragments Project, National Institute for Research in the Amazon (INPA), C.P. 478, Manaus, AM 69011-970, Brazil

Introduction

Tropical forests are being cleared at a rate of over150,000 km

2

per year (Whitmore 1997), causing exten-sive loss and fragmentation of existing wildlife habitats.Fragmentation has myriad impacts on the dynamics oftropical ecosystems (e.g., Laurance & Bierregaard 1997)but its effects on plant communities have received onlylimited attention (e.g., Williams-Linera 1990; Laurance1991, 1997; Malcolm 1994; Turner et al. 1996).

We describe the frequency of mortality and damage intrees of the family Myrtaceae in fragmented and continu-ous Amazonian rainforests. By assessing the relative im-portance of edge and area effects and fragment age, wecan better understand the mechanisms of ecologicalchange in recently fragmented forests.

Methods

Study Area

This study is part of the Biological Dynamics of ForestFragments Project (Fig. 1), a long-term experimentalstudy of Amazonian forest fragmentation (Lovejoy et al.1986; Bierregaard et al. 1992). The study area is located70 km north of Manaus in central Amazonia (2

8

30

9

S,60

8

W), at 100–150 m elevation. Local soils are nutrient-poor. Rainfall ranges from 1900–2500 mm annually witha pronounced dry season from June to October. The for-est canopy is 30–37 m tall, with emergents to 55 m. Thelocal flora is remarkably diverse in tree species (Rankin-de Merona et al. 1992).

The study area is surrounded by large expanses of con-tinuous forest. In the early 1980s, a series of 1-, 10-, and100-ha fragments (Fig. 1) were isolated by distances of70–1000 m from surrounding forest by clearing and of-ten by burning the intervening vegetation to establish

cattle pastures. Reserves ranging from 1–1000 ha in areawere delineated in nearby continuous forest to serve asexperimental controls.

Study Design

From 1980 to 1986 floristic inventories of all trees (

$

10cm diameter at breast height) were conducted in 66square, 1-ha plots in the study area (Rankin-de Merona etal. 1992). Trees in each plot were marked with num-bered aluminum tags and mapped, with leaves, fruits,and/or flowers collected for every individual. From Feb-ruary to May 1987, one of the authors (LVF) revisited 56of the plots to assess mortality and damage level to treesin the family Myrtaceae, for which taxonomic identifica-tions were especially reliable. Every individual was relo-cated, and any changes in its condition since the initialinventory were assessed.

A total of 632 Myrtaceae trees of 59 identified speciesor morphospecies were examined, averaging 11.3

6

5.3trees (

6

SD) per plot. Dead or damaged trees weregrouped into three categories: (1) standing dead trees;(2) physically damaged or fallen trees; and (3) all dead ordamaged trees. We distinguished the first two categoriesbecause standing dead trees may result from altered mi-croclimatic conditions near forest edges (Lovejoy et al.1986), whereas fallen or damaged trees commonly resultfrom wind disturbance (Laurance 1991).

Of the 56 plots (Fig. 1), 30 were located in forest frag-ments and 26 in continuous forest (controls). The frag-ment plots were in four 1-ha fragments (4 plots); three10-ha fragments (17 plots); and one 100-ha fragment (9plots). The control plots were in five 1-ha (5 plots); one10-ha (3 plots); one 100-ha (9 plots); and one 1000-ha (9plots) reserves. Plots within fragments were stratified sothat edge and interior areas were both sampled.

We devised four landscape predictors for each plot:(1) distance to the nearest forest edge; (2) distance tothe nearest east-facing edge (edge aspect

5

70–110

8

);(3) fragment area; and (4) fragment age (number of years

x

Paper submitted May 17, 1996; revised manuscript accepted October23, 1996.

798

Fragmentation and Tree Mortality Ferreira & Laurance

Conservation BiologyVolume 11, No. 3, June 1997

since isolation). We contrasted the two edge-distance pre-dictors because our study area receives prevailing easterlywinds (V. Kapos, personal communication) that couldcause increased windthrow along east-facing edges. Edge-distances were measured from the center of each plot.

Plots were pooled into discrete categories to facilitatestatistical analysis. There were four categories for theedge-distance measures (1

5

#

60 m; 2

5

61–100 m; 3

5

101–500 m; 4

5

.

500 m) and for fragment area (1

5

1 ha;2

5

10 ha; 3

5

100 ha; 4

5

control) and three categoriesfor fragment age (1

5

3 years; 2

5

4 years; 3

5

7 years).The rationale for the edge-distance categories is that mi-croclimatic changes can occur within 60 m of forestedges in the study area (Kapos 1989), whereas wind-dis-turbance may be pronounced within 100–200 m ofedges and detectable up to 500 m from edges, at least insome Australasian forests (Laurance 1991).

Statistical Analysis

Tree mortality and damage were patchy in nature, yield-ing a strongly positively skewed (approximately nega-tive binomial) data distribution. We ranked the depen-dent variables, which reduced both skewness andheteroscedasticity among samples. Ranked data werecompared between treatments using one-way ANOVAs,followed where appropriate by Tukey’s tests to contrastsample means.

The factors describing fragment area and edge-dis-tance were intercorrelated (

r

s

5

0.66–0.87; Spearmanrank correlations). To assess effects of area indepen-dently of edge effects, all plots

,

150 m from any edgewere excluded, and the remaining plots were used tocontrast damage levels in fragmented and continuousforest. The two edge-distance measures also were inter-

correlated (

r

s

5

0.68) but their efficacy as predictors iscompared here as alternative explanations for the ob-served variation in tree damage.

The interval between the initial tree inventory and ourresurvey of each plot varied from 1–7 years. Plots withlonger intervals should accrue more dead trees via natu-ral mortality processes, independent of other factors. Toassess the importance of this effect, we used data from27 non-edge plots to estimate the “natural” mean mortal-ity rate (

M

) of Myrtaceae trees in the study area, using alogarithmic model (

M

5

ln(

S

)/

t

, where

S

5

proportionof individuals surviving the interval and

t

5

time inyears; Lieberman et al. 1985). The expected natural mor-tality was calculated for each plot (expected mortality

5

[1

2

M

]

t

), and expected and observed values were com-pared using least-squares regression analysis.

A mathematical “core-area model” (Laurance 1991;Laurance & Yensen 1991) was used to predict the im-pacts of edge effects on fragments of varying sizes andshapes. The model generates accurate (

.

99%) predic-tions of the size of unaffected core-area for any fragment,using three parameters: a fragment shape-index (

SI

), frag-ment area (

TA

), and empirical knowledge of the distance(

d

) to which edge effects penetrate into fragments.

Results

Nearly half (25/56) of the plots had no damage, whereasthe remainder had 6–57% dead or damaged trees. Annualmortality rates were low (0.56

6

0.26%,

6

SE) in forest-interior plots (

.

100 m from edge) but were nearly seventimes higher (3.85

6

0.72%) in edge plots. Annual ratesof tree damage were over eight times higher in edge(2.96

6

1.06%) than interior (0.32

6

0.32%) plots.

x

Figure 1. Map of study area in central Amazonia showing locations of 1-, 10-, and 100-ha forest frag-ments and continuous for-est reserves (controls). Fragments and controls used in the study are shaded, whereas stippled areas indicate cattle pas-tures or young regrowth, and unstippled areas are primary rainforest.

Conservation BiologyVolume 11, No. 3, June 1997

Ferreira & Laurance Fragmentation and Tree Mortality

799

Variation in census interval appeared to have little ef-fect on mortality and damage estimates. When bothdead and damaged trees were considered, the length ofthe sampling interval accounted for only 5.3% of the to-tal variation in the data set (

F

5

3.03,

p

5

0.087; least-squares regression analysis).

One-way ANOVAs revealed highly significant effectsof edge-distance on most mortality and damage parame-ters (Table 1). Edge effects appeared to have a major in-fluence on tree mortality and damage (Fig. 2). Distanceto the nearest east-facing edge, however, was not a bet-ter predictor than simple edge-distance. For overall mor-tality and damage, edge-distance accounted for more ofthe variation in the data set (45.3%) than did distance tonearest eastern edge (26.9%; based on sums of squaresfrom the ANOVAs).

Tukey’s tests suggested tree mortality and damagewere significantly elevated within 100 m of fragmentmargins. When total mortality and damage were consid-ered, samples from both 0–60 m and 61–100 m fromedges had significantly (

p

,

0.01) higher values thanthose farther from edges. Results were identical whenstanding dead and fallen or damaged trees were ana-lyzed separately (Fig. 2).

Fragment area effects per se appeared weak. Whenonly sites

.

150 m from edges were compared betweenfragmented and continuous forest, the analysis was non-significant (Table 1), accounting for only 3.9% of thevariation in overall damage and mortality (ANOVA sumsof squares). Although this test was conservative becausethere were only four non-edge sites in fragments, totaldamage and mortality was virtually identical in frag-mented (2.5

6

4.3%) and continuous (2.8

6

5.8%) forest.Fragment age also had limited effects on tree damage

and mortality (Table 1). The effects of age were signifi-cant only for fallen and damaged trees, and the trendwas actually opposite to that expected, with more fallenand damaged trees in younger (3- or 4-year-olds) thanolder (7-year-olds) fragments (

p

,

0.05; Tukey’s test).Fragment age accounted for 16.7% of the variation in totalmortality and damage (ANOVA sums of squares).

To generate the core-area model, we used a value of

d

5

100 m because tree mortality and damage were sig-nificantly increased within 100 m of edges (Fig. 2). Themodel (Fig. 3) suggests edge effects may have a substan-tial impact on Amazonian forest remnants, even uponlarger (500–1000 ha) remnants. This is especially appar-ent when “realistic” fragment shapes (i.e.,

SI

5

2–4) areused in the model, rather than a square fragment (

SI

5

1.13), which is unusual in real landscapes. For example,using realistic shapes (Fig. 3), a fragment of 1000 ha ispredicted to have 22–42% of its total area influenced byedge effects, whereas a fragment of 500 ha would have30–58% of its area influenced.

Discussion

Edge and Area Effects

Our findings suggest edge effects can cause sharply ele-vated tree mortality and damage in recently fragmentedforests, at least among species of Myrtaceae in Amazo-nia. Rates of tree death and damage were seven to eighttimes higher in edge than non-edge sites. When all deador damaged trees were considered, nearly half (45%) of

Table 1. Summaries of one-way ANOVAs used to assess effects of landscape features on tree mortality and damage in fragmented and continuous forests in central Amazonia.

Factor tested

*

All dead ordamaged trees

Standing deadtrees only

Fallen ordamaged trees

F p F p F p

Dist. nearest edge 14.39

,

0.0001 6.33 0.0010 12.87 0.0003Dist. eastern edge 6.38 0.0009 8.56 0.0001 2.46 0.0730Fragment area 0.00 0.9920 0.77 0.3900 1.33 0.2600Fragment age 2.71 0.0840 1.09 0.3490 8.24 0.0016

*

Sample sizes varied between treatments and comparisons, but were reasonably large (

n

5

7–30 plots) for all treatments except non-edge plotsin fragments (

n

5

4).

Figure 2. Effects of edge-distance on tree damage and mortality ( 6 SE) in central Amazonia.x

800

Fragmentation and Tree Mortality Ferreira & Laurance

Conservation BiologyVolume 11, No. 3, June 1997

the total variation in the data set (using ranked data) wasexplained by the distance of plots to forest edge (Fig. 2).

The distance of plots to the nearest easterly-facingedge (which receives persistent tradewinds) was a lesseffective predictor, explaining 27% of the total variation.This may occur because windstorms that damage treescan come from virtually any direction (V. Kapos, pers.comm.) and may cause complex patterns of forest dis-turbance (Boose et al. 1994) that obviate any simple rela-tionship between edge aspect and tree mortality. In ad-dition, microclimatic changes in fragments, such asreduced humidity and increased temperature variabilitynear edges, may not vary greatly between easterly edgesand those with other aspects.

Edge and area effects are rarely discriminated in stud-ies of fragmented ecosystems (Temple 1986; Laurance &Yensen 1991; Didham 1997), but in this study we dem-onstrated that area effects per se had little apparent ef-fect on tree mortality and damage, accounting for only4% of variation in the data set. Area effects that might in-fluence tree persistence in fragments include popula-tion-level processes, such as losses of small populationsvia random genetic or demographic events (Shafer 1981),and community-level phenomena, such as declines in re-production following losses of specialized pollinators orseed-dispersers (Powell & Powell 1987; Aizen & Feinsinger1994). In general, however, we suspect such changes re-quire longer time-scales to be manifested than in the re-cent (3- to 7-year-olds) fragments examined in this study.At least for this data-set, edge effects apparently swampedarea effects as the proximate cause of tree damage andmortality.

Causes of Tree Mortality

There are two likely causes of elevated tree mortalityand damage near fragment margins. The first is microcli-matic changes. Working in newly created forest frag-ments in the same study area, Kapos (1989) demon-strated that hotter, drier conditions more typical ofoutside areas penetrated at least 40–60 m into fragmentinteriors. Microclimatic changes are often lessened inolder edges which become “sealed” by pioneer and sec-ondary vegetation (Williams-Linera 1990; Kapos et al.1993), but they are probably an important cause of treemortality in new fragments (Lovejoy et al. 1986). Thelarge numbers of standing dead trees near edges (Fig. 2)may have been killed by sudden shifts in temperature,relative humidity, or soil moisture that exceeded theirphysiological tolerances. The observation that leaf-fall in-creases dramatically near recent edges (Lovejoy et al.1986; Sizer 1992) suggests affected trees experiencedsevere water-stress.

A second likely cause of tree damage is wind turbu-lence. When forests are cleared and fragmented, theedges of remnants are exposed to increased windspeed,turbulence, and vorticity, which often lead to elevatedwindthrow (Chen et al. 1992) and forest-structural dam-age (Laurance 1991, 1997). Winds striking an abrupt for-est edge cause an increase in downwind turbulence, re-sulting in pronounced wind-eddies for at least 2–10times the height of the forest edge (Savill 1983). In trop-ical Queensland, Australia, a region subjected to occa-sional cyclones, Laurance (1991, 1997) suggested thatwind forces caused detectable increases in forest dam-age up to 500 m from fragment edges and marked dam-age within 200 m of edges. Unlike microclimatic changes,wind damage is unlikely to lessen over time as fragmentedges become less permeable because downwind turbu-lence usually increases as edge permeability is reduced(Bull & Reynolds 1968; Savill 1983).

Conservation Implications

Our results suggest that in central Amazonia, edge ef-fects in tree mortality and damage penetrate about100 m into fragment interiors (Fig. 2). Our study was notexplicitly designed to measure the penetration-distance(

d

) of edge effects, however, which can be assessedmost precisely using replicated edge-interior transects(Laurance & Yensen 1991). Thus our estimate of

d

5

100 m should be regarded as approximate.The core-area model (Fig. 3) suggests edge effects

should increase rapidly in intensity as fragment area fallsbelow about 500 ha. Fragments below this size-rangemay still have important conservation values (Turner &Corlett 1996), but their ecological characteristics arelikely to differ markedly from those in intact forest. Suchdifferences may include the decline of wind- and drought-

Figure 3. A core-area model for rainforest fragments in central Amazonia. The empirical estimate for the penetration-distance of edge effects (d 5 100 m) was based on observed patterns of tree mortality and dam-age. According to the model, fragments with realistic shapes (SI 5 2–4) are expected to become increasingly vulnerable to edge effects once fragment area falls be-low about 500 ha.

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Ferreira & Laurance Fragmentation and Tree Mortality

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sensitive tree species near forest edges and a generalshift toward disturbance-adapted vegetation in frag-ments (Laurance 1991, 1997). A sudden increase in treemortality could potentially cause “ecological distortions”that drive initial species losses in fragments (Terborgh etal. 1997), especially among animals that have mutualisticrelationships with vulnerable tree species.

Acknowledgments

C. Gascon, S. Lewis, W. Magnusson, J. Chambers, andthree anonymous referees commented on earlier draftsof the manuscript. This study was supported by WorldWildlife Fund-U.S., National Institute for Research in theAmazon, Ministerio de Ciencia e Tecnologia (MCT-Bra-zil), Smithsonian Institution, and the Mellon Foundation.This is publication number 175 in the BDFFP technicalseries.

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