linking forest edge structure to edge function: mediation of herbivore damage

Linking forest edge structure to edge function:

mediation of herbivore damage

M. L. CADENASSO and S. T. A. PICKETT

Institute of Ecosystem Studies, Box AB, Millbrook, NY 12545, USA

Summary

1 Forest edges, which are prominent features in the north-eastern United States

landscape, may control the ¯ux of organisms between forest and non-forest habi-

tats. Previous studies have described edge structure rather than function, as deter-

mined by interaction with such ¯uxes.

2 The function of the forest edge may be linked to the structure of its vegetation.

We tested this hypothesis by experimentally altering the structure of the vegetation

at two deciduous forest edges in Millbrook, New York, USA. Intact and thinned

plots were established at each edge and we determined whether the structure of the

edges in¯uenced the ¯ux of herbivores, as measured by herbivore damage to trans-

planted tree seedlings.

3 Herbivore damage to seedlings at site 1 was a�ected by edge vegetation structure

and by distance from the edge. The edge structure e�ect was due to herbivory by

voles, which was signi®cantly greater in the intact than in the thinned treatment.

Regardless of treatment, voles damaged seedlings only on the edge and 30±40m

from the edge and did no damage in the forest interior (90±100m), whereas deer

damaged signi®cantly more seedlings in the forest interior than on the edge. At site

2, where vole damage was concentrated on the edge, damage to seedlings was

a�ected only by distance from the edge, not edge structure.

4 The two dominant herbivores, white-tailed deer and meadow voles, preferentially

damaged di�erent seedling species. In addition, tree seedlings browsed by deer

resprouted more frequently than those clipped by voles. Our results suggest that

both edge structure and distance from the edge in¯uence herbivore activity and, as

a result, in¯uence the spatial arrangement, density and composition of populations

of tree seedlings during regeneration in forest fragments.

Keywords: edge permeability, fragmentation, meadow voles, tree seedlings, white-

tailed deer

Journal of Ecology (2000) 88, 31±44

Introduction

In the north-eastern United States, as elsewhere,

fragmentation of landscape structure has increased

both the prominence of forest edges and the propor-

tion of forest area that lies close to an edge. While

processes characteristic of the forest interior, such as

tree regeneration, plant±plant interactions and

plant±animal interactions, still occur in forest

patches, their dynamics may be in¯uenced by factors

originating from outside the patch boundary

(Saunders et al. 1991; Angelstam 1992). The impact

of exogenous factors on internal forest dynamics

may depend on the permeability of the edge to those

factors (Wiens et al. 1985; Stamps et al. 1987;

Forman & Moore 1992), and this study represents

the ®rst experimental test of whether the ¯ux of one

such factor, tree seedling herbivores, is indeed

a�ected by the structure of the forest edge.

The importance of forest edges has been acknowl-

edged and investigated by ecologists for a long time,

although the empirical approach has been predomi-

nantly static and descriptive (Murcia 1995). Leopold

(1936) ®rst suggested that edges bene®t game man-

agement. Later, ecologists recognized that there are

both positive and negative e�ects of edges, depend-

ing on the organism or scale of study (Harris 1988).Correspondence: M. L. Cadenasso (fax 914 6775976;

e-mail [email protected]).

Journal of

Ecology 2000,

88, 31±44

# 2000 British

Ecological Society

In the context of the plant community, the focus of

edge research has been on quantifying abiotic gradi-

ents (Geiger 1965; Wales 1967, 1972; Matlack 1993;

Weathers et al. 1995; Cadenasso et al. 1997) and bio-

tic structure (Ranney et al. 1981; Williams-Linera

1990; Brothers & Spingarn 1992) across edges,

allowing comparison between edges that di�er in

age (Matlack 1994; Camargo & Kapos 1995), aspect

(Wales 1972; Matlack 1994) or adjacent land use

(Moran 1984; Chen et al. 1992). Functional signi®-

cance is often inferred from these largely descriptive

patterns of plant community structure: for example,

the use of edge to interior ratios assumes that zones

within a certain distance from the edge have a parti-

cular function (Levenson 1981; Laurance & Yensen

1991). The link is, however, largely untested except

for the e�ect of edges on nest predation and parasit-

ism in birds (AndreÂ n & Angelstam 1988; AndreÂ n

1995), where results are often contradictory (Paton

1994). This research tests the assumption by examin-

ing how edge structure mediates herbivore damage

to tree seedlings, and thus assesses the functional

impact of the edge on the interior forest community

and plant population dynamics.

The call for more research on the functioning of

forest edges has been justi®ed by their potential to

mediate ¯ows between forest and non-forest habitats

(Wiens et al. 1985; Forman & Moore 1992; Hansson

1992; Wiens 1992), depending on the characteristics

of both the two habitats and the edge zone and on

the nature of the ¯ow (Wiens 1992; Wiens et al.

1993). There are several externally originating pro-

cesses that can ¯ow across the landscape and

through forest edges (Saunders et al. 1991; Forman

& Moore 1992; Wiens 1992). These ¯ows of organ-

isms, material and energy link habitat patches in the

landscape and may a�ect landscape pattern, popula-

tion dynamics and nutrient cycling (Wiens 1992).

The further hypothesis that the dynamics within

each patch will be a�ected by the existence of edges

(Wiens et al. 1993) has not been tested experimen-

tally.

We adopted a conceptual model that integrates

structure and function and illustrates the potential

functions of forest edges (Pickett & Cadenasso

1995). This model incorporates ideas from a variety

of sources (Forman & Moore 1992; Wiens 1992;

Wiens et al. 1993; Forman 1995) and comprises

three distinct zones ± the forest interior, the forest

edge and the surrounding non-forest habitat. Most

organisms, material and energy moving from the

forest exterior into the interior must pass through

the forest edge (exceptions include birds or seeds

that can travel over the edge and deposit directly in

the interior, and ¯uxes in ground water). Depending

on the situation, an edge may inhibit or enhance

movement across the boundary or it may have no

e�ect.

Our experimental test of the link between struc-

ture and function of forest edges considered this

model for the particular case of the ¯ux of tree seed-

ling herbivores between deciduous forests and adja-

cent old ®elds released from agriculture. Edges

between these contrasting land covers are structu-

rally and compositionally abrupt, and biotic and

abiotic changes across these edges are steep.

The meadow vole (Microtus pennsylvanicus, Ord

1815) is the primary herbivore in the old ®eld, and

the white-tailed deer (Odocoileus virginianus,

Zimmermann 1780) is the main forest herbivore.

Herbivory is important in determining tree seedling

composition and density in both forests (Alverson

et al. 1988; Tilghman 1989; Gill 1992) and old ®elds

(Rankin & Pickett 1989; Gill & Marks 1991; Ostfeld

& Canham 1993). For example, proximity to the

forest edge is critical to the establishment of woody

species in adjacent old ®elds because it provides a

seed source (Gill & Marks 1991) and in¯uences her-

bivore activity (Williamson & Hirth 1985; Myster &

McCarthy 1989; Ostfeld et al. 1997). Here, we con-

sidered the e�ect of edge on tree regeneration in the

forest, which has been less well studied.

The structure of the edge is hypothesized to in¯u-

ence how it mediates any ¯ux. Edge structure can be

viewed from a geographical perspective: a forest

edge represents a physical disjunction in the land-

scape at a scale of kilometres. We therefore consid-

ered how herbivore activity di�ered with distance

from the forest edge. Alternatively, the ecological

structure of an edge is represented by the complex

of vegetation layers that make up the edge zone and

varies over a scale of metres. We tested the function

of the edge at this scale by experimentally altering

the structure of the vegetation on the edge and mea-

suring how herbivore activity di�ered with vegeta-

tion structure.

Two questions were posed. First, how does the

structure of the vegetation on the forest edge med-

iate herbivory in the forest? To determine the direct

e�ects of edge structure on a key herbivore, small

mammals were trapped. Secondly, what is the net

e�ect of that mediation on tree regeneration in the

forest?

Site description

Two 1-ha sites were located at the Institute of

Ecosystem Studies (IES) in Millbrook, Dutchess

County, New York, USA (41�500N, 73�45

0W).

Both were embedded in large (>40ha) upland

mesic deciduous forests that are approximately 60

years old, and had similar canopy composition

(dominated by several species including Quercus

rubra, Q. alba, Q. prinus, Acer rubrum, A. sac-

charum, Fagus grandifolia, Betula lenta and Carya

spp., with Ostrya virginiana and Carpinus caroliniana

32Linking forest

edge structure to

edge function

# 2000 British

Ecological Society

Journal of Ecology,

88, 31±44

as mid-canopy trees and Hammemalis virginiana and

Viburnum acerifolium in the understorey). The ®elds

adjacent to each site had been released from hay

production or grazing in the 1960s. The ®eld at site

1 had been mowed periodically, there was no woody

establishment and it was dominated by several spe-

cies of Solidago, Schizachyrium scoparium, Poa spp.

and other grass and forb species (Armesto et al.

1991). The forest at site 2 was separated from the

®eld by a 3-m wide paved road, accessible to only

the IES. This ®eld had not been mowed except

along the road margins and, in addition to the her-

baceous species found at site 1, had small patches of

Rhus glabra and Cornus racemosa and two indivi-

duals of Acer rubrum approximately 5m tall. Both

sites had relatively straight and structurally abrupt

edges. Site 1 faced north-east (21� from true north)

and site 2 had a west aspect (275� from true north)

(Fig. 1). (Taxonomy is according to Gleason &

Cronquist 1991.)

EXPERIMENTAL MANIPULATION OF EDGE

STRUCTURE

Plots were established at each stand such that the

external boundary approximately followed the

canopy dripline and the sites extended 100m into

the forest interior (Fig. 1). Each of the sites was

divided into two 40-m plots separated by a 20-m

bu�er zone, and intact and thinned treatments were

allocated at random (Fig. 2). In autumn 1994 the

woody vegetation lower than half canopy height

was removed from the outermost 20m of the

thinned plot at each site. This included the lateral

branches of the canopy trees that were lower than

half canopy height, complete trees where they were

shorter than half the canopy height, and shrubs; the

herbaceous layer was not cut. Although we altered

the physical structure of the edges of the thinned

plots, but no canopy trees were removed, the shape

and location of these abrupt edges, as drawn on a

map, were not therefore altered. In other words, we

altered the ecological but not the geographical struc-

ture of the edges. Our manipulation produced a

structure similar to a newly created forest edge

before colonization by shrubs and saplings or devel-

opment of lateral branches by the newly exposed

canopy trees.

Methods

HERBIVORY EXPERIMENTAL DESIGN

Five pairs of caged and uncaged quadrats were

established in a strati®ed random design in each of

three distance bands from the edge of each treat-

ment plot (0±10m, 30±40m and 90±100m) (60

quadrats per site) (Fig. 2). Caging was accomplished

by constructing a four-sided exclosure measuring

1.5� 0.75m and made of 61-cm wide square-weave

`hardware cloth' with 1.27-cm mesh. The perimeter

was buried 4±6 cm to discourage animals from bur-

rowing under, and the cages were regularly checked

for signs of disturbance. During burial, damage to

litter and vegetation was avoided as much as possi-

ble. Twenty-centimetre wide aluminium ¯ashing was

riveted to the top of the hardware cloth around the

Fig. 1 The two ®eld sites used in the experiment. Each site occupied 100m of forest edge and extended 100m into the forest

interior and contained a thinned and a control (intact) plot allocated at random.

33M.L. Cadenasso

& S.T.A. Pickett

# 2000 British

Ecological Society

Journal of Ecology,

88, 31±44

entire cage perimeter, to prevent small mammals

from using the mesh to climb up the sides of the

cage and enter the cage through the top. Hexagonal-

weave `chicken wire' (2.54-cm mesh) was secured

over the top of the cage to prevent deer browsing

inside the exclosure. An uncaged quadrat of the

same size was located approximately 3m away from

the caged quadrat with which it was paired.

In the spring of 1995, all (caged and uncaged)

quadrats were planted with 12 seedlings of each of

Betula lenta, Quercus rubra and Ailanthus altissima.

All three species are found in these forests and

represent an early and a late successional species

and a species invasive in the Hudson Valley, respec-

tively. The seedlings were grown from seed either

collected on the IES grounds or bought from F.W.

Schumacher Co. (Sandwich, MA). Seeds were ger-

minated in February and March and seedlings were

maintained in the IES greenhouse until planted in

the ®eld in early June. Immediately after planting

seedlings were watered generously. The three species

were located randomly in the quadrats.

Seedlings were monitored weekly for the ®rst

10weeks then every 2 weeks until leaf drop in the

autumn. They were resurveyed in the spring of 1996.

Seedlings not surviving the ®rst 2 weeks after plant-

ing due to shock or stress were replaced only once.

Each seedling was scored as undamaged, damaged

by herbivores, mechanically damaged or dead from

other causes. Each herbivore damages seedlings in a

unique way, allowing for easy ®eld scoring of

damage by a speci®c herbivore. Voles clip seedlings

at the base, approximately 2 cm from the soil,

cleanly severing the stem. Deer remove biomass

from the top of the seedling and, occasionally,

remove only the apical bud. Due to their lack of

upper incisors, deer leave a very jagged cut on the

remaining seedling stem. Slugs were observed on the

plants and their slime trails were apparent on the

seedling stem. Insect defoliation was incremental

and the defoliation could be tracked until seedling

mortality. Slug and insect damage were combined

into an invertebrate class for the analyses. All seed-

ling damage observed could be attributed to one of

these classes of herbivores.

SMALL MAMMAL TRAPPING

Small mammals were trapped using Sherman live

traps placed in a regular grid extending from 20m

beyond the edge to 50m into the forest. Eight traps

were placed 10m apart along three transects in each

intact and thinned plot. Each site was trapped every

third week for three consecutive nights. Because

traps were moved between the two sites, traps were

placed on the trap station, left closed, and baited at

least 3 days prior to the actual trapping period, to

ensure that animals were familiar with the traps.

This strategy was used to prevent inaccuracies in the

capture data that may have occurred if a lag time

existed for the small mammals to `®nd' the traps.

Each site was trapped on seven occasions between

13 June and 26 October 1995, the period during

which herbivory was measured. A site was not

trapped in the week immediately following seedling

planting so that the herbivores would have access to

Fig. 2 Experimental design. Sites were embedded within deciduous forests (light shading) and a 20-m bu�er zone (hatched)

separated the two experimental plots. At three distances (0±10, 30±40 and 90±100m) on each plot, ®ve pairs of caged (&)

and open (&) quadrats were established randomly.

34Linking forest

edge structure to

edge function

# 2000 British

Ecological Society

Journal of Ecology,

88, 31±44

the seedlings used in the experiment. Traps were set

in the late afternoon, baited with rolled oats, and

checked the following morning within 2 h of sunrise.

STATISTICAL ANALYSES

All statistical analyses were done separately for data

from both site 1 and site 2. Because parametric and

non-parametric statistical approaches yielded the

same results, we only present the parametric ana-

lyses.

We used a three-factor nested multivariate analy-

sis of variance (MANOVA) together with univariate

three-factor nested ANOVAs to analyse the e�ects of

edge vegetation structure, distance from the edge

and herbivore exclusion cages on the response vari-

able, and damage to seedlings due to herbivory vs.

damage due to all other causes. Distance from the

edge was nested within edge structure and within

cage e�ect. Damage was calculated as the percen-

tage of the 36 individual seedlings planted in each

caged or uncaged quadrat that was damaged either

by a herbivore or by other means (i.e. mechanical

damage and other causes combined). ANOVA results

for a particular factor (edge structure, cage, distance

nested within edge structure or distance nested

within cage) were not considered unless MANOVA

results for that factor were signi®cant.

The e�ects of edge vegetation structure and dis-

tance from the edge nested within edge structure on

damage to seedlings caused by each of the three her-

bivore classes (deer, voles, invertebrates) were ana-

lysed with a two-factor nested MANOVA. If the

MANOVA results for a factor were signi®cant, then

two-factor nested ANOVAs were used to evaluate

which variable (herbivore class) contributed to the

signi®cant di�erences detected by the multivariate

tests. Damage was calculated for each open quadrat

as a percentage of the 36 planted seedlings that had

been subjected to herbivory by each of the three

classes. Invertebrates did not damage seedlings at

site 2 and were excluded from the analyses for this

site.

We also tested for patterns in damage among

seedling species. A two-factor nested MANOVA was

used to analyse the e�ects of edge vegetation struc-

ture and distance from edge nested within edge

structure on damage to tree seedlings caused by her-

bivory for each of the three tree species used.

Damage was calculated as a percentage of the 12

individuals of each species in each open quadrat

that had been a�ected. Again, two-factor nested

ANOVA results were considered for each factor sig-

ni®cant in the MANOVA tests to evaluate which of

the response variables (seedling species) contributed

to the signi®cant di�erences detected by the multi-

variate tests.

To test the net e�ect of herbivore damage on (i)

the mortality and (ii) the composition of the seedling

community, we analysed (i) overall seedling response

to damage caused by each of the herbivores and (ii)

damage caused by each of the herbivores to each

seedling species to determine if a herbivore damaged

seedling species di�erentially. A chi-square fre-

quency analysis was used to test the e�ect of herbiv-

ory by deer and voles on the resprouting frequency

of seedlings following damage. The assumption of

this analysis was that the ability of the damaged

seedling to resprout would be determined by the

identity of the herbivore because of the characteris-

tic manner in which each herbivore damages seed-

lings. Edge structure and distance from the edge

may in¯uence which herbivore encounters the quad-

rat, but were not expected to in¯uence the frequency

of resprout by seedlings following damage.

Therefore, the location of the seedling was not con-

sidered in this analysis. Damage was calculated as

the percentage of seedlings damaged by each herbi-

vore that resprouted in each open quadrat. For

example, if deer and voles damaged seedlings in a

quadrat and all those damaged by deer resprouted

and none damaged by voles resprouted, the response

value for deer was 100% and for voles 0%. Because

the analysis was done to test the net e�ect of herbiv-

ory on seedling community mortality, quadrats with

no herbivore damage were not used in the analysis.

The chi-square test determined whether the fre-

quency of resprout of seedlings damaged by deer

and damaged by voles di�ered from an expected

equal frequency.

A similar test with a separate analysis for each

herbivore class was used to determine whether each

species of seedlings was damaged equally by each

herbivore. Location of the seedling with respect to

edge structure and distance from the edge was again

assumed not to in¯uence the preference of the herbi-

vore. Twelve individuals of each seedling species

were exposed to herbivory in each open quadrat.

The percentage of each species in each quadrat

damaged by a particular herbivore was calculated.

Because the analysis was to test the net e�ect of her-

bivory on the composition of the seedling commu-

nity, quadrats in which the particular herbivore

caused no damage were excluded from the analysis.

A chi-square test was performed for each herbivore

to test whether the herbivore damaged seedling spe-

cies di�erentially. Because invertebrates only

damaged seedlings at site 1, the analysis of inverte-

brate preference was performed only for this site.

Results

HERBIVORE EXCLUSION CAGES AND

DAMAGE TO SEEDLINGS

Herbivore exclusion cages a�ected damage to tree

seedlings at both site 1 and site 2 (Fig. 3 and

Table 1). The signi®cant e�ect of cages in the

35M.L. Cadenasso

& S.T.A. Pickett

# 2000 British

Ecological Society

Journal of Ecology,

88, 31±44

MANOVA permitted univariate analyses conducted

separately on each of two damage classes to be used

to determine which damage class contributed to the

signi®cant cage e�ect. At both site 1 and site 2, her-

bivore damage was signi®cantly greater in the open

quadrats than within the exclusion cages, and uni-

variate analyses showed that this accounted for the

signi®cant cage e�ect in the MANOVA (Table 1);

cages had no e�ect on mortality due to all causes

other than herbivory (Table 1). Damage due to

causes other than herbivory was similar for all com-

binations of edge structure, distance from edge and

caging (Fig. 3).

HERBIVORE DAMAGE

At site 1, both edge structure and distance from the

edge nested within edge structure a�ected herbivore

damage to seedlings. The two edge treatments eli-

cited di�erent patterns of herbivory. Voles were the

dominant herbivore on the intact plot, where they

clipped 40% of the planted seedlings and caused

96% of all observed herbivore damage; deer browse

was minimal (Fig. 4). In contrast, in the thinned

plot, browse by deer and defoliation by inverte-

brates were the dominant herbivore activities, while

voles clipped only 2.8% of the planted seedlings

(Fig. 4). Univariate analyses showed that the

response of voles was the predominant driver of the

signi®cant e�ect of edge structure on seedling

damage (Table 2), although invertebrate damage

also tended to be higher on the thinned plot (Fig. 4

and Table 2). The e�ect of distance from the edge

was due to both voles and deer (Table 2). Regardless

of edge structure, voles damaged seedlings on the

edge and 30±40m into the forest but not in the for-

est interior (Fig. 4). In the intact plot, deer damage

to seedlings increased markedly with distance from

the edge and was su�cient to give an overall dis-

tance e�ect despite similar browsing throughout the

forest in the thinned plot (Fig. 4).

There was no e�ect of edge structure on herbivory

(Table 2) at site 2, but herbivory was signi®cantly

greater on the edge than at other distances for both

plot types (Fig. 4). The signi®cant e�ect of herbivory

was due to voles being limited to the edge and 30±

40m into the forest; deer browsed throughout this

site, but there was no invertebrate damage.

DAMAGE TO SEEDLINGS ACCORDING TO

TREE SPECIES

The patterns in herbivore damage to Q. rubra seed-

lings accounted for the signi®cant e�ect of distance

from the edge on damage to tree seedlings (Table 3).

Herbivory was signi®cantly greater on the edge than

at any other distance on the intact plot, and was

concentrated on the edge and 30±40m from the

Fig. 3 Damage to tree seedlings planted in herbivore exclusion cages and open quadrats in two edge structure treatments,

intact and thinned, at two sites. Damage to seedlings due to herbivores and to other causes in caged and open quadrats are

represented by di�erent shading patterns. Each value is the mean of ®ve replicates 2 1 SE.

36Linking forest

edge structure to

edge function

# 2000 British

Ecological Society

Journal of Ecology,

88, 31±44

edge of the thinned plot (Fig. 5). The trends towards

greater damage to both Q. rubra and B. lenta seed-

lings on the intact plot compared with the thinned

plot were responsible for the nearly signi®cant e�ect

of edge type in this MANOVA (Table 3). At site 2,

neither edge structure nor distance from edge

a�ected the amount of damage to seedlings when

separated by tree species (Table 3).

SEEDLING RESPROUT FOLLOWING DAMAGE

Seedlings damaged by deer and voles did not

resprout with equal frequency (Fig. 6 and Table 4).

At both sites, signi®cantly more seedlings resprouted

following browse by deer than after clipping by

voles.

HERBIVORE PREFERENCE FOR TREE

SEEDLING SPECIES

None of the herbivore classes damaged seedling spe-

cies with equal frequency (Fig. 7 and Table 5). At

both sites, deer damaged seedlings of B. lenta at a

higher frequency than either Q. rubra or A. altis-

sima, while voles exhibited a preference for Q. rubra

and B. lenta. Defoliation of seedlings by inverte-

brates, which only occurred at site 1, was concen-

trated on A. altissima seedlings (Fig. 7 and Table 5).

Table 1 MANOVA and univariate ANOVAs for e�ects of edge vegetation structure, herbivore exclusion cages and distance

from edge (nested within each) on tree seedling damage

Source d.f. Wilks' l F P

Site 1

(a) Multivariate analysis

Edge 2, 50 0.9099 2.475 0.0944

Cage 2, 50 0.4489 30.689 0.0001

Distance (edge) 8, 100 0.7689 1.755 0.0950

Distance (cage) 4, 100 0.8889 1.517 0.2030

Source d.f. ss F P

(b) Univariate analyses

Herbivory damage Edge 1 383.9528 2.94 0.0926

Cage 1 8076.8483 61.79 0.0001

Distance (edge) 4 868.7633 1.66 0.1733

Distance (cage) 2 318.2013 1.22 0.3045

Error 51 6666.6972

Other damage Edge 1 108.2458 2.09 0.1547

Cage 1 46.4816 0.90 0.3484

Distance (edge) 4 425.1937 2.05 0.1014

Distance (cage) 2 201.6613 1.94 0.1537

Error 51 2646.1783


Site 2


Edge 2, 50 0.9360 1.7098 0.1913

Cage 2, 50 0.5930 17.1592 0.0001

Distance (edge) 8, 100 0.8401 1.1379 0.3449

Distance (cage) 4, 100 0.8359 2.3432 0.0599

Source d.f. ss F P


Herbivory damage Edge 1 62.2813 1.40 0.2424

Cage 1 1285.7510 28.88 0.0001

Distance (edge) 4 338.4449 1.90 0.1246

Distance (cage) 2 427.6227 4.80 0.0123

Error 51 2270.7142

Other damage Edge 1 157.5612 2.72 0.1051

Cage 1 108.2458 1.87 0.1774

Distance (edge) 4 182.5961 0.79 0.5378

Distance (cage) 2 3.3490 0.03 0.9715

Error 51 2951.1223

37M.L. Cadenasso

& S.T.A. Pickett

# 2000 British

Ecological Society

Journal of Ecology,

88, 31±44

Fig. 4 Herbivore damage to tree seedlings at three distances from intact and thinned treatment edges at two sites separated

by herbivore class. Each value is the mean of ®ve replicates 2 1 SE.

Table 2 MANOVA and univariate ANOVAs for e�ects of edge vegetation structure and distance from edge nested within edge

structure on tree seedling damage by herbivores


Site 1


Edge 3, 22 0.4515 8.9090 0.0005

Distance (edge) 12, 58.5 0.1407 5.3565 0.0001

Source d.f. ss F P


Deer Edge 1 50.4663 0.45 0.5067

Distance (edge) 4 2371.7083 5.34 0.0032

Error 24 2666.0335

Voles Edge 1 1408.2231 23.01 0.0001

Distance (edge) 4 4618.0465 18.86 0.0001

Error 24 1469.0088

Invertebrates Edge 1 173.8095 3.69 0.0666

Distance (edge) 4 176.9157 0.94 0.4579

Error 24 1129.4816


Site 2


Edge 2, 23 0.9103 1.1339 0.3391

Distance (edge) 8, 46 0.4414 2.9048 0.0104

Source d.f. ss F P


Deer Edge 1 160.7767 1.82 0.1902

Distance (edge) 4 516.4095 1.46 0.2455

Error 24 2123.0323

Voles Edge 1 1.0267 0.27 0.6104

Distance (edge) 4 71.9391 4.67 0.0063

Error 24 92.4742

38Linking forest

edge structure to

edge function

# 2000 British

Ecological Society

Journal of Ecology,

88, 31±44

VOLE CAPTURES

The species trapped included meadow voles, white-

footed mice (Peromyscus leucopus), shrews (Blarina

brevicauda), eastern chipmunk (Tamias striatus) and

meadow jumping mice (Zapus hudsonius) but, of

these species, only meadow voles are herbivorous

(Ostfeld & Canham 1993). As expected, all vole cap-

tures were in the adjacent ®eld (ÿ 20, ÿ 10m) andthe forest edge (0m) rather than the forest interior.

To illustrate the data, we calculated the number of

captures at each of the three distances in each plot

over a three-night trapping period, resulting in the

number of captures per 27 trap nights per week. The

data were temporally pseudoreplicated (Hurlbert

1984), and were not therefore subjected to analysis.

Fig. 5 Herbivore damage to each of three species of tree seedlings in di�erent edge treatments and distances. Each value is

the mean of ®ve replicates 2 1 SE.

Table 3 MANOVA and univariate ANOVAs for e�ects of edge vegetation structure and distance from edge nested within edge

structure on herbivore damage to seedlings by seedling species


Site 1


Edge 3, 7 0.5000 3.3582 0.0847

Distance (edge) 12, 18.8 0.0661 2.8101 0.0219

Source d.f. ss F P


Ailanthus altissima Edge 1 477.5233 1.02 0.3389

Distance (edge) 4 2652.1138 1.42 0.3042

Error 9 4212.7593

Betula lenta Edge 1 3175.7963 4.17 0.0717

Distance (edge) 4 9247.5648 3.03 0.0770

Error 9 6862.3242

Quercus rubra Edge 1 1131.8125 4.61 0.0604

Distance (edge) 4 5380.0857 5.47 0.0163

Error 9 2211.0464


Site 2


Edge 3, 7 0.8233 0.5006 0.6937

Distance (edge) 12, 18.8 0.3496 0.7644 0.6777

39M.L. Cadenasso

& S.T.A. Pickett

# 2000 British

Ecological Society

Journal of Ecology,

88, 31±44

However, at site 1, vole captures were consistently

greater on the thinned than on the intact plot; no

di�erences were apparent between treatments at site

2 (Fig. 8 and Table 6).

Discussion

Is the structure of the vegetation on the edge linked

to its function as re¯ected by herbivore ¯ux?

Herbivore damage to seedlings inside the cages was

minimal, showing that exclusion was successful,

while seedling mortality due to causes other than

herbivory was similar in the caged and open quad-

rats, indicating that cages did not introduce any

additional stresses. Further analyses of the responses

to herbivores were limited to the open quadrats.

ECOLOGICAL EDGE STRUCTURE AND

HERBIVORE DAMAGE

At site 1, the ecological structure of the edge had a

signi®cant e�ect on the amount of herbivore damage

to tree seedlings. This was primarily due to voles,

which were the dominant herbivore on the intact

plot but damaged signi®cantly fewer seedlings on

the thinned plot. We had expected vole activity to

be less on the thinned plot because the experimental

manipulation removed vegetation cover and might

therefore make voles more vulnerable to predation.

However, although voles reach higher densities in

herbaceous communities when low-statured vegeta-

tion cover is dense, and tend to avoid areas of

decreased vegetation cover (Birney et al. 1976; Peles

& Barrett 1996), the experimental thinning did not

alter ground layer vegetation. In addition, more

voles were captured outside the thinned treatment

but damage was greater in the intact plot. This

apparent contradiction may be explained by a com-

pensatory response of the ground layer to the

experimental manipulation. Removal of lateral

branches of the canopy trees and of small trees and

shrubs may have increased light in the thinned plot.

Although the resulting increase in herbaceous cover

may have encouraged voles, the production of more

herbaceous stems may have made tree seedlings on

Fig. 6 The percentage of seedlings damaged by deer and

voles that resprouted following damage at site 1 and site 2.

Damage represents the mean value for those open quadrats

that experienced damage by deer or voles 2 1 SE. The

number of quadrats used in the analysis can be found in

Table 4.

Fig. 7 The percentage of each species of seedlings that (a)

deer, (b) voles and (c) invertebrates damaged at site 1 and

site 2. Values shown are the mean of those for open quad-

rats in which each herbivore damaged a particular seedling

species, 2 1 SE. Species that were damaged in only one

quadrat were not included in the ®gure. The number of

quadrats used in the analyses can be found in Table 5.

Table 4 Chi-square analysis for departure from equal e�ect of deer and vole on seedling resprout after damage

n Frequency w2 statistic d.f. P

Site 1

Deer 23 1506.3 555.81 1 0.001

Voles 18 460.7

Site 2

Deer 19 1034.7 891.33 1 0.001

Voles 10 51.0

40Linking forest

edge structure to

edge function

# 2000 British

Ecological Society

Journal of Ecology,

88, 31±44

the thinned plot less obvious to predators (Birney

et al. 1976). Further tests are necessary to con®rm

the detailed mechanism by which the ecological

structure of the edge mediates the impact of voles as

herbivores on tree seedlings.

At site 2, the ecological structure of the edge vege-

tation did not a�ect herbivore damage. The number

of seedlings damaged may have been too small rela-

tive to the number of experimental treatment combi-

nations for a signi®cant e�ect of the ecological

structure to be detected by the multivariate analysis.

We did not expect the road bordering this site to

impact vole activity. The road is infrequently used

by vehicle tra�c and is only 3m wide, and Oxley

et al. (1974) concluded that roads inhibited the

movement of small mammals from forest habitats

Fig. 8 Frequency of vole captures in the ®eld adjacent to and in the intact and thinned treatment edges at site 1 and site 2.

Table 5 Chi-square analyses for whether the frequency of damage of a particular herbivore to each of the three seedling

species is signi®cantly di�erent from the expected equal frequency

n Frequency w2 statistic d.f. F

Site 1

Deer

A. altissima 13 158.3 944.49 2 0.001

B. lenta 17 883.3

Q. rubra 7 125.0

Vole

A. altissima 3 33.3 305.45 2 0.001

B. lenta 7 358.3

Q. rubra 16 400.0

Invertebrate

A. altissima 9 208.3 236.39 2 0.001

B. lenta 1 8.3

Q. rubra 3 58.3

Site 2

Deer

A. altissima 4 66.7 592.36 2 0.001

B. lenta 16 558.3

Q. rubra 6 116.7

Vole

A. altissima 1 8.3 107.27 2 0.001

B. lenta 2 25.0

Q. rubra 9 100.0

41M.L. Cadenasso

& S.T.A. Pickett

# 2000 British

Ecological Society

Journal of Ecology,

88, 31±44

but not those characteristic of more open environ-

ments. However, voles were trapped only on the

®eld side of the road, suggesting that avoidance of

the road may prevent voles from responding to dif-

ferent edge treatments. Although there was an eco-

logical e�ect only at site 1 and herbivore damage

was low at site 2, both sites showed a strong geogra-

phical e�ect.

GEOGRAPHICAL EDGE STRUCTURE AND

HERBIVORE DAMAGE

The response of herbivores to the geographical

structure of the edge was addressed by testing for

patterns in herbivore damage to seedlings with dis-

tance from the plot edge. Voles are restricted to her-

baceous habitats but do use forest edges (Grant

1971), and the decrease of their damage with dis-

tance from edge at both sites was therefore expected.

At site 1, the geographical structure also a�ected

deer damage to seedlings. On the intact plot they

caused more damage farther from the edge, and the

shift from voles as the primary herbivore close to

the ®eld to deer in the forest was as expected from

their habitat preference (Grant 1971; Tilghman

1989). In the thinned treatment, however, deer

damaged seedlings consistently over distance from

the edge. The thinned structure was maintained

throughout the growing season and therefore deer

were not attracted to the edge by resprouting stems,

as these were periodically removed. However, a

greater number of seedlings may have been available

to deer for a longer period of time because of the

reduced vole herbivory on the thinned plot. The

geographical-scale response of deer damage to edge

structure may therefore be dependent on the ecolo-

gical-scale response of voles.

NET EFFECTS ON TREE REGENERATION

The spatial patterns of damage caused by each her-

bivore will contribute to the net e�ect of herbivory

on the composition and density of the seedling com-

munity, but it is also necessary to consider which

species each herbivore damages and how seedlings

respond to the damage.

Distance from the edge a�ected damage to the

three seedling species di�erentially. Greater damage

to Q. rubra seedlings close to the edge could be

explained by the preference for this species shown

by voles, whose habitat is limited to the edge.

Distance from the edge did not in¯uence damage to

either B. lenta or A. altissima seedlings. Both deer

and voles showed some preference for B. lenta and

damage therefore occurred throughout the forest.

Although invertebrates preferred A. altissima seed-

lings, they caused minimal damage and any in¯u-

ence of either edge structure or distance from the

edge was masked by damage to this species by the

other herbivores.

Both deer and voles are known to be seedling her-

bivores, and their di�erences in damage pattern over

space in the forest and in species preference will

result in the seedling community being di�erentially

a�ected by herbivory through space. Thus regenera-

tion of the forest may depend on patterns of herbi-

vore activity as well as on other, more commonly

recognized, spatially di�erentiated factors such as

seed source (Bjorkbom 1979; Sork 1983; Houle

1994) and the availability of light (Oliver & Larson

1990; Macdougall & Kellman 1992).

The identity of the herbivore may also a�ect the

density of seedlings of each tree species because

seedlings respond di�erently to damage by each her-

bivore. The mode of damage may explain why more

seedlings resprout following deer browse than

resprout following clipping by voles. Regardless of

species, deer typically leave several leaves and, occa-

sionally, only the apical bud is removed, whereas

voles clip seedlings very close to the ground and

only a small portion of the stem remains. The e�ect

of damage by speci®c herbivores in addition to their

preferences must therefore be considered when

investigating the mechanism by which herbivory

a�ects composition and mortality of seedling popu-

lations during forest regeneration.

Understanding how forest edges in¯uence herbi-

vore damage to seedlings is important because an

Table 6 t-test analyses of the e�ect of edge structure on vole captures. Variance are equal

at both sites

n Mean SE t d.f. P

Site 1

Intact edge 7 4.4286 0.6494 ÿ5.5018 12 0.0001

Thinned edge 7 12.8571 1.3875

Site 2

Intact edge 7 4.0000 1.0911 ÿ0.2222 12 0.8279

Thinned edge 7 4.2857 0.6801

42Linking forest

edge structure to

edge function

# 2000 British

Ecological Society

Journal of Ecology,

88, 31±44

increasing proportion of the forested landscape is in

close proximity to edges. Data from sightings of

deer in spotlights has provided a conservative popu-

lation estimate for white-tailed deer on the IES

property at 18 kmÿ 2 (Winchcombe 1993), and

because this is considerably higher than that sug-

gested to inhibit forest regeneration in Wisconsin (4

kmÿ 2) (Alverson et al. 1988), deer may strongly

in¯uence seedling density and composition at our

sites. Deer traverse forest edges every dawn and

dusk (Montgomery 1963) and their interaction with

edge structure and its in¯uence on forest dynamics

may therefore be much greater than expected from

the proportion of space occupied by edges.

This is the ®rst experimental test of the function

of forest edges on plant community regeneration. It

con®rms the suggested importance of forest edge

function as a mediator of herbivore impacts

(Alverson et al. 1988) and suggests hypotheses for

more detailed mechanistic studies. In addition, the

technique of altering the ecological structure of a

forest edge while keeping the geographical scale con-

®guration of the edge intact may be a useful strategy

for studying di�erent landscape ¯uxes and how they

interact with di�erent types of edges to determine

edge functions.

Acknowledgements

We would like to thank Julie E. Hart and M.

Michael Traynor for extensive ®eld assistance in

cage construction, seedling planting and monitoring.

Dave Bulkeley and the IES Greenhouse sta� helped

grow and maintain the seedlings until they were

planted in the ®eld. The cutting of vegetation on the

forest edge was done by Brad Roeller, Alan Kling

and the IES Grounds crew. Peter Morin provided

valuable statistical advice. The manuscript has been

greatly improved by comments from Charlie Nilon,

Rick Ostfeld, John Wiens and Richard Forman.

This research was funded by the NSF, grant DEB

9307252.

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Received 29 October 1998

revision accepted 13 July 1999

44Linking forest

edge structure to

edge function

# 2000 British

Ecological Society

Journal of Ecology,

88, 31±44

linking forest edge structure to edge function: mediation of herbivore damage

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