Impact of selective grazing on plant production and qualitythrough floristic contrasts and current-year defoliationin a wet grassland

Nicolas Rossignol • Anne Bonis •

Jan-Bernard Bouzille

Received: 9 April 2010 / Accepted: 4 May 2011 / Published online: 13 May 2011

� Springer Science+Business Media B.V. 2011

Abstract Grazing impacts the structure and func-

tional properties of vegetation through floristic

changes (i.e., long-term effect) and current defolia-

tion (i.e., short-term effect). The aim of this study

was to assess the relative importance of these two

grazing effects on productivity (ANPP) and plant

quality (C/N ratio) among plant patches submitted to

a variety of grazing intensity for several years. Long-

term grazing effect was measured by comparing

ANPP and C/N ratio among plant patches with

contrasting floristic composition. Short-term impact

of grazing was measured by comparing ANPP and

C/N in plant patches, with and without defoliation.

Floristic contrasts led to a lower ANPP in highly

grazed patches than in lightly grazed ones. This result

may be related to the increasing proportion of

grazing-tolerant and grazing-avoiding species with

increasing grazing intensity. Vegetation C/N con-

trasts were recorded among grazed patches but did

not linearly relate to grazing intensity. Short-term

effect of current-year defoliation on ANPP was

limited as vegetation compensated for biomass

removal. No evidence for grazing-enhancement of

ANPP was found even at moderate grazing intensity.

Long-term floristic changes with grazing thus appeared

to be the main driving factor of variations in ANPP. In

contrast, C/N ratio showed no general and consistent

variation along the grazing gradient but varied consis-

tently depending on the community investigated, thus

suggesting an effect of the species pool available.

Keywords ANPP � Defoliation � Floristic

composition � Heterogeneous grazing �Vegetation mosaic � Vegetation quality

Introduction

Large herbivores play a major role in terrestrial

ecosystem functioning (Huntly 1991). The intensity

of grazing exerted by herbivores on grassland veg-

etation impacts the quantity and quality of available

forage. Grazing studies have reported contrasted

effects of herbivores on plant productivity and quality

of herbaceous pastures and the intensity of grazing is

considered as a key driver of change (Milchunas and

Lauenroth 1993; Baron et al. 2002; Louault et al.

2005). Contrasts in grazing intensity may be related

to stocking rates differences among paddocks but can

also occur within paddock, due to herbivore forage

selectivity. Such spatial variations of grazing

N. Rossignol (&) � A. Bonis � J.-B. Bouzille

UMR–CNRS 6553 ECOBIO, Universite de Rennes 1,

Campus de Beaulieu, 35042 Rennes Cedex, France

e-mail: Nicolas.b.rossignol@orange.fr

Present Address:N. Rossignol

INRA, UR1213 Herbivores, Theix,

63122 Saint-Genes-Champanelle, France

123

Plant Ecol (2011) 212:1589–1600

DOI 10.1007/s11258-011-9932-0

intensity typically arise when herbivores recurrently

graze some areas of the grassland whereas other areas

are neglected (Adler et al. 2001). In temperate

herbaceous pastures, selective grazing was shown to

generate and maintain a mosaic of tall lightly grazed

plant patches and short highly grazed plant patches

(Bakker et al. 1984; Berg et al. 1997; Cid and

Brizuela 1998).

The effect of grazing on plant production and

quality is expected to vary between vegetation stands

submitted to different grazing intensities. Indeed, the

net impact of grazing on vegetation results from the

interaction between a long-term impact of grazing,

through herbivore-mediated floristic changes, and a

short-term impact of current defoliation which

induces physiological plant responses as well as

physical damages (Ferraro and Oesterheld 2002).

Both effects can act in similar or in opposite ways on

plant productivity and quality (McIntire and Hik

2005; Olofsson 2006) and it remains difficult to

predict the net effect of grazing on vegetation

properties.

Global studies have shown that grazing generally

promotes N-poor unpalatable species in nutrient-poor

systems (Pastor and Naiman 1992; Milchunas et al.

1995), while in nutrient-rich systems grazing pro-

motes fast-growing species with N-rich tissues

(McNaughton 1985; Holland et al. 1992). Changes

in species composition are driven by grazing intensity

as different plant groups will be promoted by

different grazing intensities and different types of

herbivores (Vesk and Westoby 2001; Diaz et al.

2007). In French temperate sub-humid pastures,

Louault et al. (2005) found that productive species,

competitive for light and with low tissue quality,

dominated in lightly grazed plots, while more inten-

sively grazed plots exhibited increased abundance of

grazing-tolerant and grazing-avoiding species. Such

long-term vegetation shifts with increasing grazing

intensity can also be accompanied by a decrease in

ANPP (Aboveground Net Primary Production)

because species adapted to grazing are generally less

productive (Milchunas and Lauenroth 1993). The

effect of grazing pressure on vegetation quality (e.g.,

N content, digestibility) would be less predictable as

grazing-adapted species could either display low

quality tissues (e.g., grazing-avoiding species) (Loi-

seau et al. 2005; Quetier et al. 2007) or high quality

tissues (e.g., grazing-tolerant species) (Briske 1996).

In contrast, current-year defoliation of herbaceous

plants (i.e., short-term effect of grazing) is expected

to enhance forage quality due to tissue renewal

(Polley and Detling 1989; Milchunas et al. 1995).

ANPP response to short-term impact of grazing (i.e.,

biomass removal) was shown to span from negative

to positive depending on defoliation intensity and

plant species (Ferraro and Oesterheld 2002) and N

resources (Hamilton et al. 1998). Current-year defo-

liation generally induces a positive effect on plant

growth, called compensatory growth. Ritchie et al.

(1998) suggested that increased ANPP is expected

when grazing both stimulates N cycling and promotes

grazing-tolerant plants with strong re-growth ability.

The study of Milchunas and Lauenroth (1993),

however, showed that grazing increased ANPP only

in a very restricted range of conditions and for

moderate intensities of grazing. Evidences for a

positive effect of herbivores on ANPP were also

found by Turner et al. (1993) and McNaughton

(1985).

Testing for multiple levels of grazing intensity is

needed to assess when plant responses to defoliation

counter balance or reinforce the modification of

vegetation properties due to vegetation changes while

such studies remain few (McIntire and Hik 2005).

Moreover, in most grazing studies, neither the

grazing intensity nor the compensatory growth due

to current-year defoliation was quantified (Milchunas

and Lauenroth 1993; McNaughton et al. 1996). In this

study the authors investigated long-term effects of

grazing (i.e., floristic changes) and short-term effects

of current-year defoliation on vegetation quality and

productivity over a range of lightly and highly grazed

patch types generated by selective grazing (Marion

et al. 2010) and found repeatedly within each of the

three plant communities occurring in the wet grass-

lands studied (Amiaud et al. 1998). Grazing intensity

exerted on each patch type was estimated by the

percentage of available forage consumed by herbi-

vores (McNaughton et al. 1996). Aboveground net

primary production (ANPP) of patch types was

estimated and C/N ratio of aboveground plant

biomass was measured as an indicator of vegetation

quality.

The authors hypothesized that (1) floristic con-

trasts will result in lower ANPP in highly grazed

patches than in lightly grazed ones; (2) current-year

defoliation will enhance ANPP in lightly grazed

1590 Plant Ecol (2011) 212:1589–1600

123

patches and decrease it in heavily grazed patches (3)

both long- and short-term grazing effects will have a

positive effect on plant quality which will be

evidenced by a decrease of plant C/N ratio.

Methods

Study area

The study area was a wet grazed grassland, situated in

the Marais Poitevin on the French Atlantic coast

(46�280 N; 1�130 W). The climate is a mild Atlantic

type. This wet grassland was reclaimed from tidal

salt-marshes in the 10th century and has since been

grazed by cattle and horses. The soil is characterized

by a clayey texture and a markedly hydromorphic

character. A topographical gradient consisting of

depressions, higher level flats and intermediate

slopes, with a maximum altitudinal range of 70 cm,

occurs repeatedly within the grassland (Fig. 1). The

length of the flooding period differs depending on

topography and three plant communities with differ-

ent levels of tolerance to flooding are distinguished

(Amiaud et al. 1998). Flats have a mesophilous

(M) vegetation intolerant to flooding and character-

ized by grasses and sedges such as Cynosurus

cristatus, Lolium perenne, Elytrigia repens, and

Carex divisa. Intermediate slopes, flooded a few

weeks each year, have a meso-hygrophilous (Mh)

vegetation and are characterized by a high soil

salinity and sub-halophytic species such as Juncus

gerardi, Alopecurus bulbosus, and Parapholis strig-

osa (Bonis et al. 2005). Depressions, flooded from

winter to early spring, have hygrophilous (H) vegeta-

tion with flood-tolerant species such as Agrostis

stolonifera, Glyceria fluitans, and Eleocharis

palustris.

Surveys were conducted in 2002 on the grassland

common of Magnils-Reignier (250 ha), considering

five paddocks with controlled grazing regime since

1995: two cattle-grazed paddocks (1 ha each, 2

cattle ha-1, 685 kg of live weight ha-1 on average),

two horse-grazed paddocks (2 ha each, 1 horse ha-1,

680 kg of live weight ha-1 on average), and one

ungrazed paddock since 1995, thereafter referred as

‘long-term exclosure’ (4 ha) (Rossignol et al. 2006).

In each paddock, mesophilous, meso-hygrophilous,

and hygrophilous communities occupied about 50,

15, and 35% of the area, respectively, and occurred

repeatedly across all paddocks.

Within each community (M, Mh, and H), tall and

short plant patch types occurred repeatedly due to the

heterogeneous grazing intensity (Fig. 1). Each patch

type distinguished from the others by significant

contrasts in floristic composition and by the species

relative abundance (Marion et al. 2010). The vege-

tation of tall plant patch types was dominated mainly

by perennial species (e.g., E. repens in M, A.

stolonifera in H, and J. gerardi in Mh) as in the

long-term exclosure. Short plant patch types showed

a higher proportion of annual, biennial, and legume

species in the Mh and H patch types compared to the

long-term exclosure, while perennial grasses and

sedges remained highly dominant in the M patch

types along the grazing gradient (Fig. 2).

Sampling design for the assessment of short-

and long-term effects of grazing

The authors selected 16 patch types (Table 1), with

repeated occurrences within the paddocks. Thirteen

patch types occurred within grazed paddocks and

three occurred in long-term exclosure. It was aimed

to disentangle short- and long-term effects of grazing

on plant quality and productivity. Short-term effect of

grazing refers to the effect of the current-year

defoliation (biomass removal) and was investigated

by comparing ANPP and C/N between continuously

grazed situation and short-term grazing exclosures

(no current-year defoliation) for each patch type.

Long-term effect of grazing refers to the floristic

contrasts induced by several years of grazing (con-

trolled grazing regime since 1995) and was investi-

gated by comparing ANPP and C/N among patch

types in short-term exclosures (without current-year

defoliation). The vegetation of the long-term exclo-

sure was used as a standard against which the authors

compared grazed patch types performances (Milch-

unas and Lauenroth 1993).

Plant production in continuously grazed conditions

was measured using the moveable exclosures method

(McNaughton et al. 1996), a method also used by

McNaughton (1985) and Frank (2007). Six represen-

tative stands (about 10 m2 each) were selected across

two replicate paddocks for each of the 13 patch types

studied in grazed paddocks. It was established 13

short-term exclosures, one for a stand of each patch

Plant Ecol (2011) 212:1589–1600 1591

123

70 cm

Flats(Mesophilous)

Slopes(Meso-hygrophilous)

Depressions(Hygrophilous)

Topography Grazed paddock

70 cm

Flats( )

( - )

(Hygrophilous)

Grazed paddock

Fig. 1 Mosaic of patch types in grazed paddock. Left A

topographical gradient consisting of depressions, higher level

flats and intermediate slopes occurs repeatedly within the

grassland. The length of the flooding period differs depending

on topography and three plant communities (black

mesophilous; gray meso-hygrophilous; white hygrophilous).

Right In grazed paddock, tall (plain) and short (hatching) plant

patch types, associated with low and high grazing intensity,

respectively, occurred repeatedly within each topographic

position

100%100%

10%

20%

30%

40%

50%

60%

70%

80%

90%

10%

20%

30%

40%

50%

60%

70%

80%

90%

Cov

er

0%

M0

M-H

1

M-C

1

M-C

2

M-H

2

Mh

0

Mh

-C1

Mh

-H1

Mh

-H2

Mh

-C2

Mh

-H3

H0

H-H

1

H-H

2

H-C

1

H-H

3

0%

M0

M-H

1

M-C

1

M-C

2

M-H

2

Mh

0

Mh

-C1

Mh

-H1

Mh

-H2

Mh

-C2

Mh

-H3

H0

H-H

1

H-H

2

H-C

1

H-H

3

Fig. 2 Cover (% total area)

of perennial monocots

(black), annual monocots

(hatching), dicots (gray),

and legumes (white) in the

different patches

Table 1 Sampled patch types

Mesophilous (flats) Meso-hygrophilous (slopes) Hygrophilous (depressions)

Patches

name

Treatment Height Cover Patches name Treatment Height Cover Patches

name

Treatment Height Cover

M0 Ungrazed Tall 50.0 Mh0 Ungrazed Tall 15.0 H0 Ungrazed Tall 35.0

M-H1 Horses Tall 37.0 Mh-H1 Horses Tall 7.4 H-H1 Horses Tall 21.4

M-H2 Horses Short 4.5 aMh-H2 Horses Short 2.3 bH-H2 Horses Short 18.8

M-C1 Cattle Tall 58.6 aMh-H3 Horses Short 6.0 bH-H3 Horses Short 2.2

M-C2 Cattle Short 1.2 Mh-C1 Cattle Tall 4.6 H-C1 Cattle Short 29.2

Mh-C2 Cattle Short 6.3

a, b Differences of dominant species were used for discriminate between these pairs of patch types

Patch types were sorted depending on the plant community where they occurred (mesophilous vegetation on flats, meso-hygrophilous

on slopes, and hygrophilous on depressions), on the treatment (cattle-grazing, horse-grazing or ungrazed), on vegetation height (short

or tall), and on canopy cover (Loucougaray et al. 2004). The average cover of a patch type is indicated as a percentage cover of a

paddock (ungrazed, cattle-grazed or horses-grazed paddock)

1592 Plant Ecol (2011) 212:1589–1600

123

type and floristic composition of patches was not

affected by the protection from grazing during the

study. Thirteen moveable exclosures were used to

withdraw vegetation from grazing for five successive

2-week periods. For each 2-week period, one stand

per patch type was protected from grazing and five

stands of each patch type were successively protected

during the study.

Aboveground net primary production and grazing

intensity

ANPP was measured for the three patch types in

long-term exclosure and for each of the thirteen

grazed patch types, inside and outside short-term

exclosures over five successive 2-week periods from

mid-April to end of June (i.e., during the main growth

period). In long- and short-term exclosures, ANPP

was calculated as the sum of increments in above-

ground biomass in four randomly located

25 9 25 cm2 quadrats sampled every 2 weeks, over

a 10-week period. In continuously grazed situation,

plant biomass was sampled using four quadrats

located within moveable exclosures that were moved

to new locations after 2 weeks. ANPP was calculated

as the sum of increments in aboveground biomass

during five successive periods of protection by a

moveable exclosure.

These moveable exclosures were also used to

determine the consumption (biomass uptake) by

summing differences in plant biomass measured

inside and outside moveable exclosures during each

2-week period. Grazing intensity was then calculated

as the percentage of available forage consumed over

a 10-week period with:

Grazing intensity ¼ consumption=

initial standing biomassþ ANPPð Þ:

All aboveground plant biomass samples were dried

(65�C, 48 h) before weighing.

C/N ratio

Carbon and nitrogen content of aboveground plant

biomass was measured at the peak standing crop in

grazed condition, in short-term and in long-term

exclosures, for all patch types. Three samples per

patch type were dried, ground, and analysed using a

CHN auto-analyser (Perkin Elmer).

Floristic composition

Plant species cover was recorded in July 2002 for

each patch type, using fifteen 25 9 25 cm2 quadrats.

Similarity of the floristic composition between grazed

patches and long-term exclosure was measured using

the Sørensen similarity index (Is) (Legendre and

Legendre 1998). The fifteen quadrats were averaged

for each patch type to calculate similarity indexes.

Data analysis

ANPP and C/N ratios of the patch types were

analysed using nested ANOVA with community

(M, Mh, H) as first level factor and the patch type

as nested factor (n = 64 for ANPP and n = 48 for

C/N). Datasets were analysed using ANOVA for each

community.

It was tested whether variation rates of C/N and

ANPP with grazing were related to grazing intensity

and whether these variation rates were similar or not

among patch types in the three communities. It was

calculated three indexes of relative changes of ANPP

or C/N with grazing: the net effect of grazing (NEG)

which accounts for both short- and long-term impact,

the long-term effect of grazing (LTEG) related to

floristic contrasts among patch types, and the short-

term effect of grazing (STEG) due to current-year

defoliation.

NEG¼ðcurrently grazed�average value of

long-term exclosureÞ=average value

of long-term exclosure

LTEG¼ðshort-term exclosures�average

value of long-term exclosureÞ=average value

of long-term exclosure

STEG¼ðcurrently grazed�average value of

short-term exclosuresÞ=average value

of short-term exclosure

Relative change indexes were calculated for each

replicate (n = 52 for ANPP and n = 39 for C/N) and

replicates were averaged to obtain one index value

for each patch type. The effects of community on

relative changes of ANPP and C/N ratio were

analysed using ANCOVA with grazing intensity as

covariate. For all analyses, the intensity of grazing

Plant Ecol (2011) 212:1589–1600 1593

123

refers to the value of the current intensity measured

on a patch type.

Floristic similarity between grazed patches and

long-term exclosure was analysed with community as

fixed factor and grazing intensity as covariate. The

sampling design of the study did not allow to

consider a potential effect of the paddocks in

statistical analyses. Analyses were conducted using

MINITAB 13.31 software (MINITAB Inc.).

Results

Heterogeneity of plant patches properties

within the grassland

Grazing intensity, measured as the percentage of

available forage consumed during the study, ranged

from 55 to 88% (Table 2). Hygrophilous patch types

sustained on average less grazing pressure than the

other patches with a maximum of 74% of the

production consumed while, intensively grazed patch

types in Mh and H displayed grazing intensity of 85%

(Mh-H3) and 88% (M-H2), respectively. Floristic

similarity between grazed patches and long-term

exclosure decreased along the grazing gradient

(Fig. 3) for all three communities (R2 = 0.672

F = 22.51 P = 0.001). The peak of standing crop

occurred in mid-June for all patch types and we

considered C/N values of plant biomass at this time.

ANPP and C/N ratios tended to decrease with

increasing grazing intensity, the trend being signifi-

cant for hygrophilous patch types only (Table 3).

Among patches, ANPP varied from 1.3–8.0 g

DM m-2 d-1 and C/N ratio from 17 to 31 (Fig. 4a,

b) with significant effects of the community and

patch type (Nested ANOVA with community as first-

level factor and patch as nested factor; P \ 0.05 for

all analyses and each factor).

Net effect of grazing

Net effect of grazing (NEG) on ANPP of patches was

strongly related to the intensity of grazing exerted on

each patch type (R2 = 0.464, P \ 0.01; Fig. 5c white

squares) without any significant effect of the com-

munities (Table 4). Lightly grazed patches displayed

ANPP values close to the ANPP of the long-term

exclosure vegetation; while intensively grazed

patches were significantly less productive than long-

term exclosure (Fig. 4a).

Although grazing decreased plant C/N (Table 3,

Fig. 4) overall, net effect of grazing on patch types

C/N was not significantly related to grazing intensity

(Table 4). Three mesophilous patch types (i.e., M-C1,

M-C2, and M-H2) displayed decreased C/N ratio

compared to vegetation in long-term exclosure but

had close C/N values within each other (Fig. 4b).

Hygrophilous grazed patch types tend to have lower

C/N than long-term exclosure but without statistical

differences (Fig. 4b). In meso-hygrophilous patch

types, variations of C/N ratio were important between

patch types and it was found both higher and lower

C/N values compared to long-term exclosure.

Although C/N ratios of patches tend to decrease from

lightly grazed patch types to intensively grazed ones,

intensively grazed patch type Mh-H3 did not fit with

this trend and showed a high value of C/N (Fig. 4b).

Table 2 Grazing intensity (% of available forage consumed ±SE) exerted on each patch type for the three plant community

Topography Patches name F

Mesophilous (Flats) M0a M-H1 M-C1 M-C2 M-H2

0 64.9 ± 4.9a 68.9 ± 12.7ab 86.8 ± 8.7b 88.2 ± 0.5b 2.95*

Meso-hygrophilous (Slopes) Mh0a Mh-C1 Mh-H1 Mh-H2 Mh-C2 Mh-H3

0 63.4 ± 2.8a 66.5 ± 3.0a 79.1 ± 6.0b 80.3 ± 4.9b 84.7 ± 4.6b 5.92**

Hygrophilous (Depressions) H0a H-H1 H-H2 H-C1 H-H3

0 55.1 ± 4.2a 63.6 ± 5.4ab 72.9 ± 1.6b 73.8 ± 7.4b 4.01*

a Ungrazed patches M0, Mh0, and H0 were not included in the ANOVAs

* P \ 0.05, **P \ 0.01

The last column indicates F-value of one-way ANOVA for each plant community occurring on distinct topographic position. The

same letters indicate the absence of significant differences within rows for grazing intensity (post-hoc Fisher’s tests)

1594 Plant Ecol (2011) 212:1589–1600

123

Impacts of short- and long-term effects of grazing

on plant patches properties

When protected from current-year defoliation, ANPP

variations among patch types were related to the

floristic contrasts due to long-term effect of grazing

only (LTEG, Fig. 4c). In short-term exclosures, patch

types generated by high intensities of grazing (Mh-

H2, Mh-C2, Mh-H3, and H-H3; Table 2) were found

less productive than vegetation in long-term exclo-

sure (Fig. 4c). Relative changes due to LTEG led to a

linear decrease of ANPP with grazing intensity

(Fig. 5c black squares) for all three communities

(Table 4). Short-term grazing effect linked to current-

year defoliation (STEG) tended to increase ANPP at

light intensity and to decrease it at heavy intensity

(Fig. 5a). This relation was weak (R2 = 0.04;

F = 0.47; P = 0.508) but contributed to accentuate

the linear decrease in ANPP due to long-term impact

of grazing with grazing intensity. Indeed, when

vegetation was continuously grazed, linear decrease

of ANPP with grazing intensity occurred with a

steeper slope than when vegetation was protected by

short-term grazing exclosures (Fig. 5c; white

squares). The limited impact of STEG on ANPP

showed that all patch types displayed good abilities to

compensate for loss of biomass due to current-year

defoliation, whatever its intensity. Full compensation

was mostly observed at low grazing intensity. As

grazing intensity increased, differences between net

effect and long-term effect of grazing grew. This

suggests that plants compensate only partially for

biomass losses at high grazing intensity (Fig. 5c).

Changes in vegetation quality (C/N ratio) with

grazing depended primarily on the plant community

(Table 4). No significant change of C/N ratio was

found with grazing intensity (R2 = 0.132, F = 1.67,

P = 0.223) (Fig. 5d black squares). However, floris-

tic changes with LTGE led to plant quality similar or

higher than vegetation in long-term exclosures

(Fig. 4d) while short-term effect of grazing (STEG,

Fig. 5b) spanned from negative (increased C/N) to

positive at heavy intensity (decreased C/N). The

effect of defoliation (STEG), combined with the

long-term effect of floristic changes, explained that

patch types with high plant quality were more

frequent in intensively grazed situations (Fig. 4b).

Discussion

Previous studies on extensively grazed grasslands of

the Marais Poitevin showed that grazing by large

herbivores generated a spatial heterogeneity of veg-

etation structure (Loucougaray et al. 2004; Marion

et al. 2010) and soil N mineralization rates (Rossignol

et al. 2006). It was shown here that herbivores also

induced spatial heterogeneity in vegetation properties

within the grassland studied. Both ANPP and plant

quality varied between patch types for all three plant

communities studied (M, Mh, and H). These evi-

dences strongly support the view that extensive

grazing promotes functional heterogeneity within

these grasslands.

It was found that selective grazing led to spatial

variations of grazing intensity between patch types

within each topographic position with hygrophilous

vegetation (in flooded depressions) receiving on

average less grazing pressure than the two other

positions. Herbivores were shown to graze preferen-

tially this position early in the season and to switch

toward slopes and flats as the productivity of these

two positions increase (Menard et al. 2002). It was

found a negative and linear relationship between

ANPP and grazing intensity which suggests that

variations of grazing intensity controlled the varia-

tions of ANPP. Grazing led to an overall increase of

Grazing intensity

Flo

rist

ic s

imila

rity

0

0.1

0.2

0.3

0.4

0.5

0.6

0.7

0.8

0.5 0.6 0.7 0.8 0.9 1

M-H1

M-H2

M-C2M-C1

Mh-C1

Mh-H1

Mh-H2

Mh-C2

Mh-H3

H-H1

H-H2H-H3

H-C1

R² = 0.6718p < 0.001

Fig. 3 Floristic similarity (Sørensen index) between grazed

patch types and long-term exclosure along grazing intensity

gradient. Linear regression was calculated among patches of

the three communities: mesophilous (triangles), meso-

hygrophilous (squares), and hygrophilous (circles). The

relation between floristic similarity and grazing intensity did

not differ with plant community: ANCOVA (n = 13) topo-

graphic position (df 2; F 0.47, n.s.) and grazing intensity as

covariate (df 1; F 13.28, P \ 0.01)

Plant Ecol (2011) 212:1589–1600 1595

123

Table 3 Mean ANPP and plant C/N for each topographic position (M, Mh, and H) for different durations of grazing protection

ANPP (g DM m-2 d-1) ± SD C/N Aboveground biomass ± SD

M Mh H M Mh H

Grazed 4.53 ± 2.10 a 3.29 ± 2.64 a 2.78 ± 1.58 a 23.70 ± 4.55 a 24.21 ± 4.78 a 21.21 ± 3.16 a

Short term exclosure 5.87 ± 2.09 ab 3.27 ± 2.24 a 3.05 ± 1.09 a 25.56 ± 7.70 a 21.52 ± 3.65 a 22.18 ± 4.00 a

Long-term exclosure 8.14 ± 0.22 b 7.50 ± 0.60 b 4.05 ± 1.12 a 31.48 ± 0.40 a 23.03 ± 1.20 a 27.12 ± 4.02 b

Grazed situation and short-term exclosure are the means of the patches occurring in each topographic position (The means were not

weighed by the proportion of tall and short plant patches in the area). Within each column, the difference between long- and short-

term exclosures reveals a long-term effect of grazing and the difference between short-term exclosures and grazed situations reveals a

short-term effect of current-year defoliation. The same letters indicate the absence of significant differences within columns (One-

way ANOVAs and post-hoc Tukey’s tests for each topographic position)

0

1

2

3

4

5

6

7

8

9

10

M0

M- H

1

M- C

1

M-C

2

M-H

2

Mh

0

Mh

-C1

Mh

-H1

Mh

- H2

Mh

- C2

Mh

-H3

H0

H-H

1

H-H

2

H-C

1

H-H

3

Tall Short Tall Short Tall Short

M Mh H

cc

a

b

bc

bc

abab

ba

c

c

a

ab

c

b

0

5

10

15

20

25

30

35

40

45

M0

M-H

1

M-C

1

M-C

2

M-H

2

Mh

0

Mh

-C1

Mh

- H1

Mh

-H2

Mh

-C2

Mh

-H3

H0

H-H

1

H-H

2

H-C

1

H-H

3

Tall Short Tall Short Tall Short

M Mh H

b

ab

b

ab

a

n.s.

ab

b

b

a

b

0

1

2

3

4

5

6

7

8

9

10

M0

M-H

1

M-C

1

M-C

2

M- H

2

Mh

0

Mh

-C1

Mh

- H1

Mh

-H2

Mh

-C2

Mh

-H3

H0

H-H

1

H-H

2

H-C

1

H-H

3

Tall Short Tall Short Tall Short

M Mh H

cn.s.

ab

b

a

ab

c

b

a

bb

b

Rat

ioC

/N

Rat

ioC

/N

AN

PP

(g D

M m

- 2d-

1 )A

NP

P(g

DM

m-2

d-1 )

Patch: p< 0.001 Patch: p< 0.001 Patch: p< 0.01 Patch: p< 0.001 Patch: p< 0.01 Patch: p= 0.181

Patch: p= 0.129 Patch: p< 0.001 Patch: p< 0.05 Patch: p< 0.05 Patch: p= 0.806 Patch: p= 0.05

0

5

10

15

20

25

30

35

M0

M-H

1

M-C

1

M-C

2

M-H

2

Mh

0

Mh

-C1

Mh

-H1

Mh

-H2

Mh

-C2

Mh

-H3

H0

H-H

1

H-H

2

H- C

1

H-H

3

Tall Short Tall Short Tall Short

M Mh H

b

aa

a

b

bc

a

bb

c

b

n.s.

0

1

2

3

4

5

6

7

8

9

10

M0

M- H

1

M- C

1

M-C

2

M-H

2

Mh

0

Mh

-C1

Mh

-H1

Mh

- H2

Mh

- C2

Mh

-H3

H0

H-H

1

H-H

2

H-C

1

H-H

3

Tall Short Tall Short Tall Short

M Mh H

cc

a

b

bc

bc

abab

ba

c

c

a

ab

c

b

0

5

10

15

20

25

30

35

40

45

M0

M-H

1

M-C

1

M-C

2

M-H

2

Mh

0

Mh

-C1

Mh

- H1

Mh

-H2

Mh

-C2

Mh

-H3

H0

H-H

1

H-H

2

H-C

1

H-H

3

Tall Short Tall Short Tall Short

M Mh H

b

ab

b

ab

a

n.s.

ab

b

b

a

b

0

1

2

3

4

5

6

7

8

9

10

M0

M-H

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-C1

Mh

- H1

Mh

-H2

Mh

-C2

Mh

-H3

H0

H-H

1

H-H

2

H-C

1

H-H

3

Tall Short Tall Short Tall Short

M Mh H

cn.s.

ab

b

a

ab

c

b

a

bb

b

Rat

ioC

/N

Rat

ioC

/N

AN

PP

(g D

M m

- 2d-

1 )

Grazed

Short-term exclosures

AN

PP

(g D

M m

-2d-

1 )

Patch: p< 0.001 Patch: p< 0.001 Patch: p< 0.01 Patch: p< 0.001 Patch: p< 0.01 Patch: p= 0.181

Patch: p= 0.129 Patch: p< 0.001 Patch: p< 0.05 Patch: p< 0.05 Patch: p= 0.806 Patch: p= 0.05

0

5

10

15

20

25

30

35

M0

M-H

1

M-C

1

M-C

2

M-H

2

Mh

0

Mh

-C1

Mh

-H1

Mh

-H2

Mh

-C2

Mh

-H3

H0

H-H

1

H-H

2

H- C

1

H-H

3

Tall Short Tall Short Tall Short

M Mh H

b

aa

a

b

bc

a

bb

c

b

n.s.

A

C D

B

Fig. 4 ANPP (g Dry Matter m-2 d-1 ± SE), and C/N ratio

(±SE) between patch types in grazed situation (a and b, graybars) or in short-term exclosures (c and d, gray bars) and long-

term exclosure (black bars). Patch types are ranked in relation

to the grazing pressure within each topographic position. For

each topographic position, the differences between patch types

were tested using ANOVA (P-values are indicated on the

figure). The same letters indicate the absence of significant

differences within each topographic position (post-hoc Tukey’s

test)

1596 Plant Ecol (2011) 212:1589–1600

123

vegetation quality as in other grazed grasslands

(Milchunas et al. 1995; Sirotnak and Huntly 2000;

Olofsson and Oksanen 2002; Semmartin and Ghersa

2006) but without linear response to grazing intensity

variations.

Long-term grazing-induced vegetation changes

drive ANPP variations

The relation between ANPP and grazing intensity

appears to mainly result from floristic differences

generated by selective foraging along years. Selective

grazing by herbivores (Menard et al. 2002; Fleurance

et al. 2005) largely drives spatial heterogeneity in

vegetation structure (Adler et al. 2001; Parsons and

Dumont 2003) and can, therefore, influence overall

functioning of the ecosystem. While vegetation of the

-1

-0,8

-0,6

-0,4

-0,2

0

0,2

0,4

0,6

0,8

1

0,5 0,6 0,7 0,8 0,9 1

-1

-0,8

-0,6

-0,4

-0,2

0

0,2

0,4

0,6

0,8

1

0,5 0,6 0,7 0,8 0,9 1

-1

-0,8

-0,6

-0,4

-0,2

0

0,2

0,4

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1

0,5 0,6 0,7 0,8 0,9 1

-1

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-0,6

-0,4

-0,2

0

0,2

0,4

0,6

0,8

1

0,5 0,6 0,7 0,8 0,9 1

Rel

ativ

e ch

ange

sR

elat

ive

chan

ges Short-term effect Short-term effect

Long-term effectNet effect

Long-term effectNet effect

R²= 0.270;p<0.05

R²= 0.464;p<0.01

C D

-1

-0,8

-0,6

-0,4

-0,2

0

0,2

0,4

0,6

0,8

1

0,5 0,6 0,7 0,8 0,9 1

-1

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-0,6

-0,4

-0,2

0

0,2

0,4

0,6

0,8

1

0,5 0,6 0,7 0,8 0,9 1

-1

-0,8

-0,6

-0,4

-0,2

0

0,2

0,4

0,6

0,8

1

0,5 0,6 0,7 0,8 0,9 1

-1

-0,8

-0,6

-0,4

-0,2

0

0,2

0,4

0,6

0,8

1

0,5 0,6 0,7 0,8 0,9 1

Grazing intensity Grazing intensity

Grazing intensity Grazing intensity

Ratio C/NANPPR

elat

ive

chan

ges

Rel

ativ

e ch

ange

s Short-term effectShort-term effect Short-term effectShort-term effect

Long-term effectNet effectLong-term effectNet effect

Long-term effectNet effectLong-term effectNet effect

R²= 0.270;p<0.05

R²= 0.464;p<0.01

A B

Fig. 5 Relative changes of ANPP and C/N with grazing

intensity. Short-term effect of grazing (STEG) on ANPP and

C/N ratio is expressed as the patches performances in grazed

situation compared to patches in short-term exclosures (a and

b). Long-term (c and d, black squares) and net effects (c and d,

white squares) of grazing are expressed as the performance of

patches in short-term exclosures or in grazed situation

compared to vegetation in long-term exclosures. Linear

regressions are indicated on the figures when significant (solidline long-term effect, dotted line net effect). Each point is the

mean of four replicates for the ANPP and the mean of three

replicates for C/N

Table 4 ANCOVA results testing for the changes of ANPP

and C/N of grazed patches relative to vegetation in long-term

exclosure

Source of variation d.f. Relative

changes

of ANPP

Relative

changes

of C/N

Community 2 2.70 6.14**

Grazing exposure 1 0.398 0.06

Community x grazing exposure 2 0.735 0.88

Grazing intensity (covariate) 1 12.09** 0.44

** P \ 0.01

The effects of grazing exposure (short-term exclosures

protected from current-year defoliation and continuously

grazed situations) and of plant community (mesophilous,

meso-hygrophilous or hygrophilous) were tested using

ANCOVA with the grazing intensity exerted on each patch

type as a covariate. F-values are in the table (ANPP: n = 26;

C/N: n = 26)

Plant Ecol (2011) 212:1589–1600 1597

123

three communities showed distinct floristic assem-

blages (Loucougaray et al. 2004), common trends of

vegetation changes with grazing were observed. In

long-term exclosure, all patch types were highly

dominated by tall perennial graminoid species which

are predicted to be strong competitors for light and

very productive in subhumid grasslands (Burke et al.

1998; Pucheta et al. 1998). Grazing was shown, in

various ecosystems, to generally favor annual plants

over perennial, short plants over tall plants, prostrate

over erect plants (McIntyre et al. 1995; Bullock et al.

2001; Diaz et al. 2007). Accordingly, along the grazing

gradient, competitive species were gradually replaced

by grazing-avoiding or grazing-tolerant species

(Briske 1996), like annual species, rosette species,

and legumes, which appeared less productive in this

system. Such floristic shifts could explain the observed

decline of productivity along grazing gradient.

Overall, the shift of species with increasing

grazing intensity, together with productivity changes

recorded for 1–2 ha large paddocks, were similar to

the impacts of grazing reported in larger grasslands

areas (Milchunas and Lauenroth 1993). At the local

scale studied, the authors indeed recorded as much

variation in vegetation structure, composition, and

properties (ANPP and C/N) than in large grasslands

areas.

Impact of in situ defoliation

Contrary to the expectations, ANPP was not signif-

icantly affected by short-term effect of grazing (i.e.,

current-year defoliation) and all patch types dis-

played compensatory growth abilities in response to

grazing. Such a good tolerance to grazing probably

results from the species-pool filtering by the eight

centuries-long history of grazing and most of the

species were thus likely to be grazing-tolerant

(Loucougaray et al. 2004; Bonis et al. 2005).

Ferraro and Oesterheld (2002) have reported that

plant productivity decreased less in grazing experi-

ments than in defoliation experiments conducted

under controlled conditions. Indeed, in grazing

experiments, other effects may counter-balance the

impact of biomass removal on productivity. First,

grazing prevents the canopy closure of vegetation and

then might create better light penetration (Holland

and Detling 1990). Second, compensatory growth of

defoliated plants leads to an increased demand for

nutrients (Hamilton et al. 1998) and can be supported

by nutrient returns through excreta (Maschinski and

Whitham 1989) which fits with the grazing-enhanced

soil N availability previously found in this grassland

(Rossignol et al. 2006). While the lowest effect of

current-year defoliation was found on lightly grazed

patch types, the authors did not find evidence that

plant regrowth after defoliation could enhance pro-

ductivity at moderate intensity of grazing as sug-

gested in previous studies (Milchunas and Lauenroth

1993; Ritchie et al. 1998).

Changes in plant biomass quality

The high abundance of grazing tolerant species in

these grasslands was also supported by Esmaeili et al.

(2009) and Benot et al. (2009) and can explain the

overall enhanced plant biomass quality with grazing

found in this study. However, plant quality of patch

types did not linearly increase with grazing intensity.

This suggests that the increase of plant quality due to

N-rich species was balanced by the presence of

unpalatable species with poorer tissue quality.

The consequences of herbivore-driven floristic

changes on plant biomass quality differed depending

on plant community, which is determined by topog-

raphy and flooding regime. Hence, an increased cover

of legumes occurred in heavily grazed patch types of

winter-flooded depressions and accordingly, high

grazing intensity led to vegetation with low C/N

ratio. In contrast, on slopes, replacement of compet-

itive perennial grasses by annual and dicots with

increasing grazing intensity is accompanied by the

stability in C/N ratio of aboveground biomass. This

result may be explained by the fact that grazed

patches were composed of a mixture of different life

forms showing either tolerant or escaping strategies

for responding to grazing. Accordingly Green and

Detling (2000) and Mikola et al. (2000) reported that

the impact of the grazing intensity on C/N ratio of

plant biomass is highly variable and depends on the

specific tolerance of plant species to grazing (Guitian

and Bardgett 2000).

Conclusions

Overall it was found a decrease in plant productivity

with increasing grazing intensity which resulted

1598 Plant Ecol (2011) 212:1589–1600

123

primarily from long-term effect of grazing through

floristic changes. In contrast, short-term effect of

defoliation was found of minor impact on ANPP,

without evidence of a positive effect of defoliation on

ANPP even at moderate intensities of grazing.

Vegetation, however, displayed a good tolerance to

defoliation along the grazing gradient which may be

explained by faster N cycle.

In the wet grasslands studied, grazing by cattle

and horses promoted the coexistence of tall produc-

tive plant patch types together with low swards with

high nutritive values at the scale of a management

unit (i.e., paddocks). Such grazing heterogeneity led

to functional changes among plant patches which

could contribute to the diversity of the forage

offered, both in quality and quantity. The results

thus highlight the importance of considering the

spatial heterogeneity of vegetation when evaluating

the ecological functioning and the agronomic value

of a pasture.

Acknowledgments This study was funded by the Parc

Interregional du Marais Poitevin. The authors particularly thank

Didier Naudon and Sebastien Cosson for their assistance. This is

part of the program GDR CNRS 2574 ‘‘UTILITERRES’’ and

program ECCO GEOTRAITS. A previous version of this

manuscript was improved by the comments made by Dr. JL Firn

and two anonymous reviewers. Thanks to Stephane Barbier,

Aurelie Josset, and Anthony Pingray for their help in the field.

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