Grass and

Forage Science

The Journal of the British Grassland Society The Official Journal of the European Grassland Federation

A meta-analysis of climate change effects on forage

quality in grasslands: specificities of mountain and
Mediterranean areas
B. Dumont*, D. Andueza*, V. Niderkorn*, A. L
uscher, C. Porqueddu and
C. Picon-Cochard
*INRA, UMR1213 Herbivores, Saint-Genes Champanelle, France, Agroscope, Institute for Sustainability
Sciences ISS, Zurich, Switzerland, CNR-ISPAAM, Sassari, Italy, INRA, UR874 Grassland Ecosystem Research,
Clermont-Ferrand, France

Abstract
Atmospheric carbon dioxide (CO2), global mean temperature and interannual variability in temperature
and rainfall are expected to increase significantly by
the end of the 21st century. To review the effects of
these factors on forage quality, we carried out a
meta-analysis of climate manipulation experiments.
The first notable result was a lack of effect of elevated
CO2 on structural carbohydrates and digestibility. Elevated CO2 increased the total non-structural carbohydrates of forage tissues by an average of 25% and
decreased forage nitrogen (N) content by 8%.
Increased legume abundance in multispecies swards
can, however, maintain N concentration in the harvested biomass. There were no consistent effects of
warming on contents of N, water-soluble and structural carbohydrates, or on digestibility. We highlight
the continuum in the effect of water availability, from
drought to irrigation, with a curvilinear increase of
forage N as water availability decreased. Digestibility
increased, on average, by 7% with drought, but with
strong experimental variations. The review places special emphasis on discussion of the specificities of
mountain and Mediterranean grasslands, the former
being limited by low temperature, the latter by
drought and heat. Elevated CO2 decreased forage N
content in mountain areas and in temperate plains
alike. It increased N content by an average of 3% in
Mediterranean areas; this could be due to shifts in
vegetation communities under elevated CO2 or to a
greater concentration of N in plant tissues under

Correspondence to: B. Dumont, INRA, UMR1213 Herbivores,

F-63122 Saint-Genes Champanelle, France.
E-mail: bertrand.dumont@clermont.inra.fr
Received 29 August 2014; revised 6 February 2015

doi: 10.1111/gfs.12169

drought conditions. Further experiments are needed

to investigate the effects of combined factors, including extreme climatic events.
Keywords: elevated CO2, warming, drought, nitrogen,
fibres, digestibility

Background
Global atmospheric change consists of (i) increased
concentrations of the foremost greenhouse gases: CO2,
methane and nitrous oxide and (ii) associated changes
in temperature, precipitation and other climatic elements that are expected over forthcoming decades to
centuries. For the preparation of the Fifth Assessment
Report of the Intergovernmental Panel on Climate
Change (IPCC, 2013a), global projections of the
earths climate have been developed using general circulation models for a set of new emission scenarios,
known as representative concentration pathways
(RCPs). These four projections are referred to as concentration pathways to emphasize that they are not
definitive socio-economic scenarios, but rather internally consistent sets of time-dependent projections of
climate forcing that might be realized with more than
one underlying socio-economic scenario (Collins et al.,
2013).
An increasing concentration of atmospheric CO2 is
the most predictable aspect of global atmospheric
change: between 1980 and 2014 atmospheric CO2
concentration increased from 338 to 398 ppm. According to the four widely varying RCP, by 2100 atmospheric CO2 concentration could reach 421 (RCP2
6,
low), 538 (RCP4
5, mediumlow), 670 (RCP6
0,
mediumhigh) or 936 ppm (RCP8
5, high) (IPCC,
2013b). With respect to RCP4
5, taking into account
the uncertainty within this scenario, the earths mean
annual surface air temperature is expected to increase

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239

240 B. Dumont et al.

by +1
1 to +2
6C relative to 19862005 (Collins et al.,

2013). Maximum warming is expected to occur at
high latitudes of the Northern Hemisphere. In Europe,
warming is projected to be strongest in the north-west
(NW), where it may reach +3 to +7C in winter, while
the hot spot for warming in summer is projected in
the Iberian Peninsula with +3 to +4C (IPCC, 2013c).
Lelievre et al. (2010) reported that in southern France,
the boundaries of Mediterranean climate have moved
to the north and NW at the rate of 3040 km per decade since 1980. However, the majority of models project the winter temperature increase in the
Mediterranean region to be relatively small (+1 to
+2C). Increased intra- and interannual variability
may be another significant aspect of climate change,
and this is of high ecological relevance. Using a regional climate model, Sch
ar et al. (2004) predict that
year-to-year temperature variability for central Europe
will double by 2100. This would lead to more frequent
heat waves and droughts during the growing season.
All climate models suggest that average precipitation
will increase on a larger scale, but regionally this is
not always the case. For 2100 and scenario RCP4
5, a
10-to-20% increase in precipitation, both in winter
and summer, is projected for northern Europe (IPCC,
2013c). For the Mediterranean region, a slight reduction of precipitation (up to 10% in winter and
between 10 and 20% in summer) is projected. The
magnitude of regional precipitation change varies considerably among models, and in many areas, it is less
than the standard deviation of model-estimated natural variability.
The objective of this study is to review current
knowledge of the effects of atmospheric change elevated CO2, increased temperature and drought on a
wide range of forage quality parameters. The basis of
this review is a meta-analysis based on climate manipulation experiments covering a wide range of climatic
conditions and all types of grasslands (permanent
grasslands, temporary grasslands and mixtures) with
some data on shrubs and tree foliage, because they are
occasionally browsed. Data were provided at plant
organ, plant species or plant community levels (grass
legume mixtures or multispecies ecosystems) and
allowed discussion of the direct and indirect effects of
climate change factors on forage quality of harvested
biomass. Special emphasis is also placed on the discussion of the specifics of mountain and Mediterranean
grasslands given that not only the absolute size of
changes (as addressed above) but also the limiting factors of the ecosystems are of importance. We expect a
very different situation for Mediterranean and mountain areas, the former being already limited by
drought and heat, while plant growth in mountain climate areas is limited by low temperature.

Impact of climate change on plant

ecophysiology and livestock digestion
Forage quality depends on nutrient concentration,
which determines digestibility, partitioning of metabolized products in the digestive tract and forage intake;
it thus strongly affects animal performance. Forage
quality is estimated by chemical analyses, such as ash
and nitrogen (N) content, total non-structural carbohydrates (TNC) content [water-soluble carbohydrates
(WSC) and starch] and structural carbohydrates [neutral detergent fibre (NDF), acid detergent fibre (ADF),
acid detergent lignin (ADL)], and by biological analyses, which are mainly based on the estimation of the
organic matter digestibility using ruminal fluid in vitro
(Tilley and Terry, 1963) or enzymes (Aufr
ere and Demarquilly, 1989). Climate change impacts on livestock
digestion in two ways: (i) its effects on the physical
and chemical characteristics of forages and (ii) its
direct effects on animals (intake and digestive
processes).
Physical and chemical changes in plants in
response to heat stress depend on warming level and
drought intensity. Extreme climatic events lead to tissue senescence which strongly decreases forage quality. Under moderate heat stress, plant maturation is
faster, water content of plant tissues decreases, and
there is an increase in WSC. Maturation of plants
increases stem-to-leaf ratio and cell-wall content,
including lignin, which interferes with the digestion of
cell-wall polysaccharides by acting as a physical barrier
to microbial enzymes (Moore and Jung, 2001). High
temperatures amplify the lignification process by
increasing individual cell lignification rather than the
proportion of cells becoming lignified (Wilson et al.,
1991). Consequently, heat stress usually decreases forage digestibility (Lu, 1989). However, under elevated
CO2, an increase of WSC content and a corresponding
decline in cell-wall content can increase DM digestibility (Picon-Cochard et al., 2004), which suggests complex interactions between climatic factors.
Climate change also has direct effects on intake
and digestive processes, which can in turn impair livestock performance (Nardone et al., 2010; OBrien et al.,
2010). It has been well documented that high temperatures decrease voluntary intake by ruminants due to
thermoregulation, as most heat production is due to
rumen fermentation (Beatty et al., 2008). To cope,
animals can adapt their foraging behaviour, such as
reduce feeding-bout duration, and increase night feeding. Advances have also been made in management
and feeding strategies to alleviate heat stress in dairy
cattle. For instance, increasing nutrient density
(because dietary protein degradability may become
critical) and limiting high-fibre diets (to decrease heat

2015 John Wiley & Sons Ltd. Grass and Forage Science, 70, 239254

Climate change effects on forage quality 241

production) can help maintain normal rumen function

(West, 2003). Some direct impacts of heat stress on
digestion have been reported, for example slower passage rate and longer retention time of digesta in the
gastrointestinal tract (Silanikove, 1992). Slower passage rates may partly result from changes in reticular
motility (Miaron and Christopherson, 1992). Reduced
daily intake, associated with a decrease in volatile fatty
acid concentration in the rumen and prolonged retention of feed in the gastrointestinal tract, could increase
forage digestibility (Schneider et al., 1988; Miaron and
Christopherson, 1992). Bernabucci et al. (2009)
reported that variations of diet digestibility in ewes
chronically exposed to heat stress may also result from
adaptation of rumen function to hot environments
with fewer cellulolytic and amylolytic bacteria.

A meta-analysis based on climate

manipulation experiments
To conduct a meta-analysis, we created a database
(references in Table 1 and in Supporting information
published online) of the effects of climate change on
forage quality variables. These included the following
effects: elevated atmospheric CO2 concentration
(CO2), warming (T), drought (D) or irrigation (W),
and their interactions. An extensive search was performed using Web of Science on 15 July 2014. Initial
search terms were climate change combined with
forage quality, forage, grassland, leaf or stem,
and with nitrogen, carbohydrate, fibre, phosphorus, lignin, digestibility, NDF, ADF or ADL. In
the second-round search, terms warming, drought,
water deficit or water stress were combined with
forage or grassland and with nutritive value,
chemical composition or digestibility. A total of
2241 articles were found. Among these, we selected
short-term climate-manipulation experiments that
applied single or combined climate-change factors in
a controlled way and thus allowed for testing various
scenarios. Outdoor experiments with semi-natural or
more intensively managed ecosystems were preferred,
but some experiments that had been performed
under semicontrolled conditions were also selected, as
long as plants were grown in undisturbed soil. We
excluded papers with unavailable data (e.g. where
ANOVA results were given rather than mean values) or
infrequently reported quality variables (e.g. tannins,
macronutrients that were analysed in fewer than six
papers). Some experiments were conducted on multispecies ecosystems, but most of the data came from
grass or legume monocultures. We also included
some data on shrubs and tree foliage as they are
occasionally browsed, especially in Mediterranean
areas.

2015 John Wiley & Sons Ltd. Grass and Forage Science, 70, 239254

In total, seventy-five papers were finally analysed

(Table 1). Of these, there were forty-two papers that
provided data at plant species or plant organ levels,
which accounted for 74% of overall data. Atmospheric
CO2 concentration was increased, on average, by
269  106 ppm (mean  SD, n = 309 observations
from thirty-eight experiments in the database) compared with ambient CO2 (363  15 ppm), which is
slightly less than in the mediumhigh RCP scenario
(IPCC, 2013b). Air or canopy temperature was
increased by an average of 2
2  1
5C (n = 184
observations, twenty-four experiments) during the
growing season compared with ambient temperature
(11
1  5
2C). Precipitation was reduced by
48  22% in drought experiments (n = 131 observations, eighteen experiments). Water supply was
increased by 60  29% in irrigation trials (n = 69
observations, six experiments). Few experiments combined several factors (Table 1).
In some experiments, the effect of climate change
was analysed according to season and year, in which
case we averaged the seasonal data but not the year
data. When measurements were taken at the plant
community level, management data (fertilization vs.
no fertilization, different defoliation regimes, etc.)
were considered as replicates because they could result
in contrasted species assemblages. When measurements were taken at the plant species or plant organ
levels (leaf lamina, sheaths and palatable stems), plant
species and plant organs were considered as replicates.
Plant species were then grouped according to functional group: C3 grasses (GC3), C4 grasses (GC4), Cyperaceae (Cyp), herbaceous legumes (L), herbaceous forbs:
non-N-fixing dicots (F) or woody dicots (woody
legumes and forbs were considered in the same functional group due to the lack of data). For each forage
quality variable, we calculated the ratio of each replicate value in the climate change treatments to that in
the control treatments; 95% confidence intervals (CI)
were then calculated and are represented as horizontal
bars in Figures 1, 2 and 4. The effect of any climate
change factor was considered significant if the 95% CI
of the effect size did not overlap zero. Differences in
the responses between functional groups (Figure 2) or
climatic areas (Figure 4) were also assessed based on
the overlap of 95% CI.
The meta-analysis allowed us to compare the
results from twenty-two climate manipulation experiments under mountain climate conditions with those
from twenty-seven experiments from temperate plains
(Table 1). The classification of mountain was defined
based on sites at elevations of >800 m. Within temperate plains, we considered lowland sites under either
oceanic or continental influence, with mean annual
temperatures above 6C, separating the latter from the

242 B. Dumont et al.

Table 1 Main characteristics of climate manipulation experiments used in the meta-analysis.

Ecosystem/Species*
Semi-arid plains
Native rangeland
Mixed-grass prairie
Mixed-grass prairie
Shortgrass steppe
Shortgrass steppe
Forage crops
Subtropical plains
Tallgrass prairie
Phalaris aquatica, Trifolium subterraneum
Arachis glabrata
Holcus lanatus, Pennisetum clandestinum
Tallgrass prairie
Temperate plains
Deschampsia flexuosa
Temperate grassland
Lolium arundinaceum
Cichorium intybus, M. sativa, T. pratense
Grassland species
Lolium perenne
Lolium perenne
Medicago sativa
Lolium perenne
Trifolium repens
Semi-natural grassland
Medicago sativa
Lolium perenne
Grassland species
Semi-natural heathland
Festuca arundinacea
Temperate grassland
Plantago lanceolata, T. officinale, Elymus repens
F. arundinacea, D. glomerata
Trifolium ambiguum, M. sativa, T. pretense
Perennial grass species
Legume species
Grass and legume species
Alopecurus pratensis
Holcus lanatus
Temperate grassland
Lolium perenne
Subarctic/arctic climate
Bog species
Tundra, wetlands
Semi-arid steppe
Deciduous dwarf shrubs
T. pratense, T. repens
Tundra
Tundra
Mountain climate
Agrostis capillaris, Festuca viviparia, Poa alpine
A. capillaris, F. viviparia, P. alpina

Vegetation type

Quality variables

Treatments

Ref.

GC3, GC4, F
GC3, GC4
GC3, GC4
G, F, Cyp
GC3, GC4
GC3, L

N
N
N/P
N
Dig
N, ADF

CO2
CO2, T, CO2xT
CO2, T
D
CO2
D

[1]
[2]
[3]
[4]
[5]
[6]

GC3,
GC3,
L
GC3,
GC3,

N, C/N
N, TNC, Dig
NDF, Dig, ADF, ADL
N, C/N, ADL
N

T
CO2, T, CO2xT
CO2, T
CO2
T

[7]
[8]
[9]
[10]
[11]

GC3
GC3, GC4, F, L
GC3
F, L
GC3, F
GC3
GC3
L
GC3
L
GC3, F, L
L
GC3
GC3, GC4, F, L
GC3, F
GC3
GC3, GC4, F, L
GC3, F
GC3
L
GC3
L
GC3, L, F
GC3
GC3
GC3, F
GC3

C/N
N, WSC, NDF, Dig, ADF
N, C/N, NDF, ADL
N
N
N
N
TNC, NDF, Dig, ADF, ADL
WSC
N, Dig
N, WSC, NDF, ADF
N, NDF, Dig, ADL
TNC, starch
N, ADL
C/N
N, ADL
N
N, C/N
N, TNC, ADL
N, NDF, Dig, ADF, ADL
N, NDF, ADF, ADL
N, NDF, ADF
N, NDF, Dig
N, C/N
N, C/N, WSC
N
N

CO2, T, D
CO2
CO2, T, D
D
CO2
CO2
CO2
D
CO2
CO2
D(D)
D, W
CO2
CO2
CO2, T, D
CO2
CO2
T
TxD
D
D
D
D
D(D)
D(D)
T, D
CO2

[12]
[13]
[14]
[15]
[16]
[17]
[18]
[19]
[20]
[21]
[22]
[23]
[24]
[25]
[26]
[27]
[28]
[29]
[30]
[31]
[32]
[33]
[34]
[35]
[36]
[37]
[38]

GC3, F
F
GC3
Woody
L
Cyp
Cyp

N, P
N
N
N
N, NDF, Dig, ADL
N
N, C/N

T
T
W
T
CO2
T
T

[39]
[40]
[41]
[42]
[43]
[44]
[45]

GC3
GC3

N, P
TNC, WSC, starch

CO2
CO2

[46]
[47]

GC4, F
L
GC4
F

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Climate change effects on forage quality 243

Table 1 (continued)
Ecosystem/Species*
Festuca paniculata
Perennial grassland
Mixed-grass prairie
Perennial grassland
Glacier forefield species
D. glomerata, L. perenne
Perennial grassland species
Perennial grassland
Shortgrass steppe
Meadow and shrubland
Perennial grassland species
Mixed-grass prairie
Forage barley
Shortgrass steppe
Shortgrass steppe
Shortgrass steppe
Perennial grasses
Perennial grassland
Gentiana straminea, Potentilla anserine
Perennial grassland
Mediterranean climate
Dactylis glomerata, Bromus erectus
Annual grassland
Annual grassland species
Annual grassland
Annual grassland
Grassland and forest trees
Forest and shrubland
Cynodon dactylon

Vegetation type

Quality variables

GC3
GC3, F, L
GC3, GC4
GC3, F, L
GC3, F
GC3
GC3
GC3, F, L, Cyp
GC3, GC4
F, Cyp
F, L, Cyp
GC3, GC4, F
GC3
GC4
GC3, GC4
GC3, GC4
GC4
GC3, F, L
F
GC3, F, L

N,
N
N
N,
N,
N,
N,
N
N
N
N,
N
N,
N,
N,
N
N,
N,
P
N

GC3
GC3, F
GC3, F
GC3, F
GC3, F, L
F, L, Woody
Woody
GC4

N,
N,
N,
N
N
N,
N,
N,

WSC

NDF, ADF
C/N, WSC
NDF, Dig
NDF, Dig

WSC
NDF, Dig, ADF
Dig
WSC, NDF, Dig, ADL
C/N
TNC, NDF, Dig

TNC
ADL
C/N

TNC
C/N
P

Treatments

Ref.

TxD
T, TxD, CO2xTxD
T, CO2, CO2xT
D
CO2
W
W
D
CO2
T
CO2
CO2
D
D
CO2
CO2
CO2
CO2
T
TxD

[48]
[49]
[50]
[51]
[52]
[53]
[54]
[55]
[56]
[57]
[58]
[59]
[60]
[61]
[62]
[63]
[64]
[65]
[66]
[67]

CO2
CO2, T, W
CO2
CO2
D(D)
CO2
D
W

[68]
[69]
[70]
[71]
[72]
[73]
[74]
[75]

*Based on information provided by the authors and on Holdridge classification of biomes: G, grasses (C3 or C4 photosynthetic
types); F, non-N-fixing dicots; L, N-fixing dicots; Cyp, Cyperaceae. Woody dicots were either forbs or legumes: ADF, acid detergent
fibre; ADL, acid detergent lignin; NDF, neutral detergent fibre; Dig, digestibility; WSC, water-soluble carbohydrates; TNC, total
non-structural carbohydrates; CO2, atmospheric CO2 enrichment; T, warming; D, rainfall/irrigation reduction; D(D), increased
precipitation variability; W, irrigation.[1] Dijkstra et al. (2008), [2] Dijkstra et al. (2010), [3] Dijkstra et al. (2012), [4] Evans and
Burke (2013), [5] Morgan et al. (2004), [6] Ul-Allah et al. (2014), [7] An et al. (2005), [8] Lilley et al. (2001), [9] Newman et al.
(2005), [10] Ross et al. (2002), [11] Verburg et al. (2009), [12] Albert et al. (2011), [13] Allard et al. (2003), [14] Brosi et al.
(2011), [15] Brown et al. (2005), [16] Crous et al. (2010), [17] Daepp et al. (2000), [18] Daepp et al. (2001), [19] Deetz et al.
(1996), [20] Fischer et al. (1997), [21] Frehner et al. (1997), [22] Grant et al. (2014), [23] Halim et al. (1989), [24] Hunt et al.
(2005), [25] Knops et al. (2007), [26] Larsen et al. (2011), [27] Newman et al. (2003), [28] Newton et al. (2010), [29] Rodgers
et al. (2012), [30] Sanaullah et al. (2014), [31] Seguin et al. (2002), [32] Sheaffer et al. (1992), [33] Sheaffer and Seguin (2009),
[34] Skinner et al. (2004), [35] Walter et al. (2012a), [36] Walter et al. (2012b), [37] White et al. (2014), [38] Zanetti et al.
(1997), 39] Aerts et al. (2009), [40] Doiron et al. (2014), [41] Gong et al. (2011), [42] Hansen et al. (2006), [43] Muntifering et al.
(2006), [44] Sharp et al. (2013), [45] Welker et al. (2005), [46] Baxter et al. (1994), [47] Baxter et al. (1995), [48] Benot et al.
(2013), [49] Cantarel et al. (2013), [50] Carrillo et al. (2012), [51] Del
eglise et al. (2015), [52] Inauen et al. (2012), [53] Jensen
et al. (2003), [54] Jensen et al. (2010), [55] Jung et al. (2014), [56] King et al. (2004), [57] Klein et al. 2007, [58] K
orner et al.
(1997), [59] LeCain et al. (2012), [60] Maleki Farahani et al. (2013), [61] Milchunas et al. (2004), [62] Milchunas et al. (2005),
[63] Morgan et al. (2001), [64] Newingham et al. (2013), [65] Picon-Cochard et al. (2004), [66] Rui et al. (2012), [67] Zwicke
et al. (2013), [68] Castells et al. (2002), [69] Henry et al. (2005), [70] Hungate et al. (1996), [71] Hungate et al. (1997), [72] Jongen et al. (2013), [73] K
orner and Miglietta (1994), [74] Sardans et al. (2013), [75] Utrillas et al. (1995). The full list of references
is available as Supporting information in the online version of this paper.

2015 John Wiley & Sons Ltd. Grass and Forage Science, 70, 239254

244 B. Dumont et al.

N
C/N
P
TNC
WSC
starch
NDF
Dig
ADF
ADL

29

14

6
2
6

60

40

20

20

40

60

80

60

40

CO2 effect (%)

N
C/N
P
TNC
WSC
starch
NDF
Dig
ADF
ADL

20

20

40

60

80

Warming effect (%)

19
6
1

10
6
8
5

60

40

20

20

40

60

80

Drought effect (%)

subarctic climate in the Holdridge classification (Holdridge, 1967). Only eight experiments from Mediterranean areas were available for the meta-analysis.
Mediterranean climates occur within the latitudes 28
and 45 and are essentially transition zones between
temperate and dry tropical climates. A Mediterranean
climate is characterized by mild wet winters and hot
dry summers, associated with large intra- and interannual variability. More specifically, Buddenhagen
(1990) defined a Mediterranean climate as one where

C3 Grasses

16

C/N

annual precipitation ranges from 275 to 900 mm, with

at least 65% falling during autumn and winter.

General trends
Elevated CO2 effect
An important new result of our meta-analysis is the
lack of effect of elevated CO2 on structural carbohydrates (NDF, ADF, ADL) and digestibility (Figure 1).

C4 Grasses

7
2

TNC

WSC

NDF

Dig

ADF

ADL

C/N

Forbs

Legumes

P
TNC

WSC

NDF

Dig

ADF

ADL

60

Figure 1 The mean effect, as %, of

elevated CO2, warming and drought
on the main forage quality variables:
N: nitrogen: C/N: Carbon/N ratio; P:
phosphorus; TNC: total nonstructural
carbohydrates;
WSC:
water-soluble carbohydrates; NDF:
neutral
detergent
fibre;
Dig:
digestibility; ADF: acid detergent
fibre; ADL: acid detergent lignin.
Error bars represent 95% of
confidence intervals. The sample size
for each variable is shown next to
the Y-axis.

40

20

20

CO2 effect (%)

40

60

80 60

40

20

20

40

CO2 effect (%)

60

80

Figure 2 The mean effect of

elevated CO2 on the main forage
quality variables in C3 grasses, C4
grasses, herbaceous forbs and
herbaceous legumes (abbreviations
are as given for Figure 1). Error bars
represent 95% of confidence
intervals. The sample size for each
variable is shown next to the Y-axis.

2015 John Wiley & Sons Ltd. Grass and Forage Science, 70, 239254

Climate change effects on forage quality 245

Conversely, elevated CO2 decreased the forage N content by an average of 8% and increased the TNC of
forage tissues by about 25%. The content of WSC also
increased, but with very high variability which could
have resulted from the instability of soluble carbohydrates within plant tissues (source/sink relationships
are affected by elevated CO2), time of harvest, or
differences between plant organs or analytical method.
These last responses confirm the conclusions of several
meta-analyses or reviews (Soussana et al., 2002;
L
uscher et al., 2004; Hopkins and Del Prado, 2007;
Soussana and L
uscher, 2007; Wang et al., 2012; Xu
et al., 2013).
Effects of elevated CO2 on digestibility were measured in eight experiments (Table 1; Figure 1), but
only three (Allard et al., 2003; Picon-Cochard et al.,
2004; Milchunas et al., 2005) measured N, TNC and
structural carbohydrates simultaneously (average
ratios of elevated CO2/ambient CO2 were as follows:
TNC = 1
271; N = 0
929; NDF = 0
985; ADF = 0
984;
digestibility = 0
999). These results are perfectly
aligned with the general trend (Figure 1). However, in
a shortgrass steppe, Milchunas et al. (2005) reported a
decline of digestibility, which was related to a slight
decrease in TNC and N contents with a simultaneous
increase in structural carbohydrate content. Differences between experiments could have resulted from
variations in species composition (Allard et al., 2003),
proportion of tissues with contrasting digestibility or
environmental factors (e.g. soil nutrients). Elevated
atmospheric CO2 concentration may affect forage protein-energy balance, and thus microbial synthesis in
the rumen, and digestibility (Soussana et al., 2002).
An increase in forage TNC content (particularly in
WSC) could cause rapid acidification of forages when
making silage, which would be an advantage leading
to little or no required additives (Rotz and Muck,
1994).
For all quality variables, we observed the same
response between functional groups (Figure 2). Within
grasses, only the C/N ratio tended to respond differently between C3 and C4 grasses, with a higher C/N
ratio for C3 grasses (20
6%  9
9 vs. 1
4%  15
9).
This is consistent with the conclusions of Wang et al.
(2012), who compared the responses of C3 and C4 species, including woody species and crops, to elevated
CO2. This more neutral effect of elevated CO2 on the
C/N ratio of C4 grasses results from the fact that photosynthesis and biomass accumulation of C4 species is
less affected by elevated CO2 than those of C3 species.
Apart from a reduction in concentration of N and
an increase in TNC, we did not observe any strong
direct effects of elevated CO2 on forage-quality variables. Nevertheless, shifts in species composition
induced by elevated CO2 could indirectly affect forage

2015 John Wiley & Sons Ltd. Grass and Forage Science, 70, 239254

digestibility in grazed pastures (Morgan et al., 2004;

Milchunas et al., 2005). This is because species strongly
differ in their forage-quality variables, independently
of atmospheric CO2 concentration. The importance of
shifts in species proportion in mixed communities for
the outcome of the CO2 response of forage quality of
the total herbage is demonstrated by results from the
Swiss FACE experiment. While both species Lolium
perenne L. ( 19%) and Trifolium repens L. ( 7%)
showed a reduction in their concentration of N under
elevated CO2 when grown in monocultures, there was
no significant effect on the concentration of N in the
total herbage of their bispecies mixture (Hartwig et al.,
2000; L
uscher et al., 2004). This was mainly due to an
increased proportion of N-rich T. repens (43 g N/kg
DM) at the expense of the N-poorer L. perenne (27 g
N/kg DM) from 21% at ambient CO2 to 33% at elevated CO2 (Hebeisen et al., 1997; Hartwig et al., 2000).
Also, in more complex mixtures containing grasses,
legumes and forbs, the proportion of legumes in the
community increased considerably under elevated CO2
(L
uscher et al., 1996, 1998; Campbell and Stafford
Smith, 2000), especially when the community was frequently cut (Teyssonneyre et al., 2002). These results
demonstrate that the response of plant communities
cannot be predicted from the response of individual
species grown in pure swards and confirm that CO2induced changes in the proportion of species with differing forage quality may be more important than
CO2-induced changes in the quality of individual species (Knops et al., 2007).
Elevated CO2 can also affect forage quality through
an alteration of morphology or heading date of the
species. Picon-Cochard et al. (2004) showed changes
of the laminae fraction of the shoots that could be
mediated by modifications in phenology (Roy et al.,
1996). More recently, Maw et al. (2014) exposed cultivars of L. perenne to the CO2 concentration expected
in 2050 (500 ppm) and found significant changes in
heading date with delays and advances of up to 10 d.
However, in a more complex grassland ecosystem,
flowering phenology showed no significant response
to either elevated CO2 concentration (600 ppm) or
reduction in summer precipitation, while warming
advanced flowering time for the dominant grass
species (Bloor et al., 2010).

Warming effect
Experiments investigating the effect of warming on
forage quality are less common than those manipulating atmospheric CO2. The meta-analysis did not reveal
any clear effects of warming on N, WSC, structural
carbohydrates or digestibility (Figure 1). This contrasts
with results from two meta-analyses (Dieleman et al.,

246 B. Dumont et al.

2012; Bai et al., 2013) and a survey on Medicago sativa

L. (Walgenbach et al., 1981), which concluded that
warming slightly increased plant N content. Higher
mineralization in warmer soils can indeed increase soil
N availability and consequently plant N uptake. However, reduced soil moisture can also lead to highly
stressful conditions that are likely to diminish the
effects of increased soil N availability on plant uptake,
which may explain contrasting trends in the effect of
warming on forage N content.
According to Buxton and Fales (1994), temperature
is the most influential factor on the nutritive value of
forages. This can result from a change in the developmental stage of plants at the time of harvest, e.g.
Bloor et al. (2010) in an upland grassland ecosystem.
Indeed, a rise in temperature increases plant growth,
as well as NDF, ADF and lignin contents, but it
reduces leaf:stem ratios. Consequently, digestibility is
usually reduced. The effect of warming has also been
shown to modify structural carbohydrates and digestibility differently in leaves and in stems (Wilson et al.,
1991). In our meta-analysis, we compared the chemical composition of the same plant organs, plant species
or plant communities under ambient and under elevated temperatures. The absence of clear effects of
warming on plant chemical composition and digestibility could be the result of measurements being carried
out on different plant organs or different functional
groups being mixed. In practice, if an increase of temperature occurs, farmers will harvest earlier, at the
same phenological stage as current harvests, and this
would also buffer the effects of warming on forage
quality.
Indirect effects of warming could, however, arise
from shifts in botanical composition of swards. The
direction and amplitude of these effects has been
assumed to vary according to climatic conditions and
plant communities (Izaurralde et al., 2011; Rodgers
et al., 2012). Simulations in the Aubrac area of Central
France predicted a shift towards exploitative grasses of
higher digestibility as the result of a 1
2C warming
(Picon-Cochard et al., 2013). Cantarel et al. (2013)
observed that an average of 3
5C warming over
4 years decreased grass proportions by 10% in favour
of legumes (mainly Vicia sativa L. and Vicia hirsuta L.),
thereby increasing forage N content in this upland
grassland. Conversely, Sebasti
a (2007) reported shifts
in botanical composition in the Pyrenees as a result of
warming which was also associated with a decrease in
water availability that negatively affected forage quality; in this instance, highly palatable grasses (such as
Festuca nigrescens Lam.) were negatively affected, while
less-palatable forbs (e.g. Potentilla neumanniana Rchb.,
Euphorbia cyparissias L.) became abundant. This last
example illustrates how shifts in community structure

can in some cases accentuate the direct effect of

warming (i.e. increased fibre content of individual
species due to faster development).

Drought effect
In the meta-analysis, nineteen studies analysed the
effects of drought on forage N concentration, 10 on
NDF, eight on ADF, six on C/N and six on digestibility,
with no more than five studies for other parameters
(Figure 1). Water stress led to an average increase of
5% in forage N concentration and to a decrease of 3%
in the plant cell-wall (NDF) content. Digestibility
increased, on average, by 7%, but with high variation
between experiments (Halim et al., 1989; Deetz et al.,
1996; Milchunas et al., 2004; Skinner et al., 2004). The
lack of a clear effect of drought on digestibility could
be the result of the small amplitude of N and NDF
variations, a small increase in lignin content sometimes also buffering the effect of a decrease in NDF.
We have highlighted a continuum in the effect of
variations in precipitation, from reduction (drought)
to irrigation, on plant N response, i.e. the ratio of N
contents between drought (or irrigation) and control
values, with a curvilinear increase in forage N as
water availability decreased (Figure 3). Variability of N
and C/N forage contents was greater in experiments
with varying precipitation compared to those in which
atmospheric CO2 or temperature was manipulated
(Figure 1). Similarly, data from the literature on the
effect of periods of low precipitation on plant N concentration are contradictory, with some authors
reporting a reduction (Hayes, 1985) and others an
increase (Murphy et al., 2002). In multispecies grasslands, one reason for this could be the shifts in species
composition that were observed as a response of grassland ecosystems to drought. Increases in dominant
perennial forbs and decreases in dominant grasses
have, for instance, been reported with warming and
summer drought in the UK (Sternberg et al., 1999).
This shift can be seen as the result of summer drought
as, under wetter conditions during summer, perennial
grasses tended to close the sward, thereby affecting
less-competitive forbs. Deep-rooted chicory (Cichorium
intybus L.) tended to thrive in mixtures when water
availability became limiting (Skinner et al., 2004).
Variations in forage N content can also be expected if
legume abundance varies, as legumes are generally
richer in N than other functional groups. Trifolium repens L. decreases under drought conditions [e.g.
Dumont et al. (2009) in species-rich upland grassland].
Other legume species, such as Onobrychis viciifolia Scop.
and M. sativa, are known to be drought tolerant; their
increased abundance could maintain or even increase
the forage N content. Finally, it is noteworthy that

2015 John Wiley & Sons Ltd. Grass and Forage Science, 70, 239254

N ratio between drought (or irrigation) and control (%)

Climate change effects on forage quality 247

120
100
80
60
40
20
0
20
40
60
150

100

50

50

100

150

Variation in precipitation or irrigation (%)

Figure 3 Effect of variations in precipitation from reduction

(drought, i.e. negative values on the X-axis) to irrigation (positive values) on plant N response, i.e. the ratio of forage N
content between drought (or irrigation) and control. Values
at 0 on the X-axis are drought experiments in which average
precipitation was kept constant but increased in variability
(Walter et al., 2012a,b; Jongen et al., 2013; Grant et al.,
2014). Polynomial regression: Y = 0
3 * X + 0
002 * X
3
192, R2 = 0
43.
legume quality may increase under drought conditions: higher leaf-to-stem ratio, delayed maturity and
higher quality of both the leaf and stem fractions have
been observed as compared to normal conditions (Peterson et al., 1992).

Specificities of mountain and

Mediterranean areas
Mountain areas
The meta-analysis allowed us to compare the effects of
elevated CO2 from twelve climate manipulation experiments under mountain-climate conditions with those
from fourteen experiments from temperate plains
(Table 1). Application of certain climate-change factors
in a controlled way and analysis of their direct effects
on forage quality did not allow for identification of
specific trends in the effects of elevated atmospheric
CO2 in mountain areas (Figure 4). For instance, N
concentration was reduced by 10% (5%), which is
identical to the effect observed in temperate plains:
10% (4%). Water-soluble carbohydrates increased
by 54% in mountain areas, compared to 20% in temperate plains, but with huge experimental variations
that prevented a definitive conclusion about any significant difference. Only Picon-Cochard et al. (2004)
and Milchunas et al. (2005) analysed the effect of elevated CO2 on the NDF content and digestibility of

2015 John Wiley & Sons Ltd. Grass and Forage Science, 70, 239254

upland swards; NDF was, on average, similar to that

in current CO2 conditions, while digestibility occasionally decreased along with forage N content (Figure 4).
A recent experiment revealed a slight but significant
3% decrease in NDF content as a result of elevated
CO2 (+140 ppm) (Niderkorn et al., 2014). Yet, because
forage N content dropped simultaneously by 13%,
digestibility remained unchanged. Perhaps more significant are the theorized shifts in vegetation composition
predicted in future CO2-enriched environments, with
some evidence in mountain areas (Teyssonneyre et al.,
2002; Stampfli and Zeiter, 2004). Rising atmospheric
CO2 concentration thus has the potential to cause significant alterations in grassland structure and function,
leading to grasslands that are more productive but of
lower forage quality for domestic livestock (Campbell
and Stafford Smith, 2000).
There are even fewer studies available that test the
effects of increasing average air temperature (four
experiments) or decreasing precipitation (four experiments) in mountain areas, with both factors being
combined in two further experiments. With only three
experiments to date, forage N content increased by an
average of 9% (10%) in mountain areas compared
with 3% (6%) in temperate plains, and further
research may yield contrasting trends in the direct
effects of increasing air temperature. An increase in
forage N concentration in mountain areas would be
consistent with the results of the meta-analyses by
Dieleman et al. (2012) and Bai et al. (2013), which
suggest non-limiting soil-water conditions in most
mountain areas (at least in those where climate
manipulation experiments have been conducted so
far). Consistent with these findings, Sebasti
a (2007)
reported that productivity in Pyrenean grasslands was
more temperature-limited than water-limited. Shifts in
plant community structure as a result of warming
could have further positive effects on forage quality,
e.g. increased abundance of legumes (Cantarel et al.,
2013) or of exploitative grasses (Picon-Cochard et al.,
2013), but this was not always the case (Sebasti
a,
2007). Effects of an extreme summer event (i.e. a 2week heat wave at +6C combined with a 3-month
summer drought) differed from those of moderate
warming. For instance, Niderkorn et al. (2014) found
that both sward biomass and quality decreased during
the extreme event. However, in autumn, the N content of regrowing tissues increased by 35%, while
NDF decreased by 7%. This led to a significant 8%
increase in the forage in vitro DM digestibility, which
contrasts with the findings reported in Figure 1.
Extreme weather events followed by a rehydration
period may thus be more likely to affect plant tissue
chemistry and forage quality than are the effects of
moderate warming and drought.

248 B. Dumont et al.

N
C/N
P
TNC
WSC
starch
NDF
Dig
ADF
ADL

10

N
C/N
P
TNC
WSC
starch
NDF
Dig
ADF
ADL

Temperate
plain

Mountain

11
2
1

1
1

60

Mediterranean
area

40

20

60

40

20

20

40

60

20

40

CO2 effect(%)

80

CO2 effect(%)

Only four experiments investigated the effect of

reducing water availability on forage quality in mountain grasslands. Consistent with the general trend
reported in Figure 3, the N content of forages
increased with water shortage, whether it was applied
alone or in combination with other factors (Milchunas
et al., 2004; Benot et al., 2013; Cantarel et al., 2013).
WSC increased in subalpine grasslands as the result of
warming and summer drought (Benot et al., 2013). In
vitro DM digestibility of forages also increased in a
shortgrass steppe as the result of water shortage (Milchunas et al., 2004).
More generally, warming and changes in water
availability may modify the boundaries of productivity-defined seasons and seasonal herbage surplus or
shortage. A positive effect of warming in mountain
areas would be the decrease in the length of the winter period. Shorter winters reduce the amount of animal feedstock needed for the winter and also allow an
earlier start of sward growth. This may allow more
intensive exploitation of resources when spring and
summer droughts are not too severe (Nettier et al.,
2010). Environmental factors, however, interact in
complex ways, producing changes in biomass distribution and community structure in subalpine grasslands.
Consequently, high year-to-year variability in temperature and rainfall could threaten the capability of
high-altitude grasslands to provide high-quality forages during summer (Sebasti
a, 2007). Interactions
between climate and management are relevant in this
context. Changes in grazing periods and in cutting
regimes (e.g. early cuts) could buffer the negative
effects of climate change on forage quality, indicating

60

80

Figure 4 The mean effect of

elevated CO2 on the main forage
quality variables in temperate plains
(oceanic or continental with annual
temperature > 6C),
mountains
(>800 m a.s.l.) and Mediterranean
areas (abbreviations are as given for
Figure 1). Error bars represent 95%
of confidence intervals. The sample
size for each variable is shown next
to the Y-axis.

that pasture management offers promising options for

adapting livestock systems to climate change.

Mediterranean areas
Only eight experiments from Mediterranean areas
were available for the meta-analysis, with the effects
of elevated CO2 being the most frequently tested (five
experiments; Table 1). Nitrogen content was recorded
in all the experiments. Forage N content was increased
by an average of 3% (8%) under elevated CO2 compared to 10% (4%) for temperate plains (Figure 4).
This could be the result of either shifts in vegetation
communities under elevated CO2 or a greater concentration of N in plant tissues under drought conditions
(Figure 3). Effects of the different factors could not be
separated due to the lack of data. Water-soluble carbohydrates and TNC increased as a result of elevated
CO2, which is consistent with overall trends reported
in Figure 1. No measurements of digestibility were
taken in any of these climate manipulation experiments. Due to this lack of data, we base our discussion
primarily on measurements of the quality of sown
swards adapted to Mediterranean areas.
Mediterranean grassland quality is often limited by
the absence of legumes. Phosphorus fertilization and
liming of native pastures are effective methods for
increasing legumes, thus promoting N fixation, in
grasslands (Cocks and Gintzburger, 1993). Annual
self-reseeding legumes (e.g. subclovers and medics)
have been extensively used for pasture improvement
in the Mediterranean basin for over forty years; in
resource-poor drylands, they represent a valuable

2015 John Wiley & Sons Ltd. Grass and Forage Science, 70, 239254

Climate change effects on forage quality 249

source of protein that mitigates the negative effects of

drought and warming on forage production (Porqueddu, 2001; Ates et al., 2014). Exploitation of the
genetic resources of perennial legumes such as Sulla
coronaria (L.) Medik. and O. viciifolia, which are able to
escape summer drought and regrow at the seasonal
peak (Sulas et al., 2005; Re et al., 2014), offers an
opportunity to stabilize both production and forage
quality of Mediterranean grasslands. Several breeding
programmes, especially in Australia and New Zealand,
have focused on the production of deep-rooted and
drought-tolerant perennial legumes (e.g. Trifolium ambiguum M. Bieb., Trifolium pratense L., Trifolium tumens
M. Bieb.), which have a high feeding value that
declines slowly with maturity. Recent research indicates that the legume Psoralea bituminosa L. exhibits
potential as a forage species of high nutritive value for
Mediterranean areas (Raeside et al., 2012).
Certain Mediterranean varieties of perennial
grasses, for example of Festuca arundinacea Schreb.,
Dactylis glomerata L. and Phalaris aquatica L., have
adapted to climates that have annual rainfall
>500 mm and an accumulated summer water deficit
<700 mm (Leli
evre et al., 2008). Summer dormancy
and dehydration tolerance are considered to be the
primary drought-tolerance traits of perennial grasses
(Norton and Volaire, 2012). The EU-PERMED Project
(http://cordis.europa.eu/project/rcn/75644_en.html)
allowed the conduct of multisite comparison that
revealed higher digestibility of seven D. glomerata cultivars (except for subsp. hispanica Kasbah) compared
with six F. arundinacea cultivars. Some species, such as
D. glomerata, could thus combine persistence under
long summer drought, early autumn regrowth and
good forage quality (e.g. 23
5% CP for the Sardinian
ecotype Ottava) (Poblaciones et al., 2008; Porqueddu
et al., 2008). Work such as this using P. aquatica and
L. perenne has been limited. According to Gutman
et al. (2001), more information on the effects of defoliation and grazing on biomass partitioning in perennial grasses is also needed to improve the forage
quality and production efficiency in Mediterranean
grasslands.
Most seed mixtures for pastures available in southern Europe consist of a small number of annual
legumes (subclovers, medics, etc.) and sometimes
include low proportions of annual grasses (e.g. Lolium
multiflorum Lam.). However, it is not uncommon to find
complex mixtures that include up to 1520 species
(Porqueddu and Gonzales, 2006). Furthermore, in areas
with higher rainfall, perennial grasses, such as D. glomerata and P. aquatica, are added to mixtures of annual
legumes. Compared with pure stands, grasslegume
mixtures provide higher yields with better seasonal distribution and limit encroachment of unsown species

2015 John Wiley & Sons Ltd. Grass and Forage Science, 70, 239254

(Nyfeler et al., 2009; Finn et al., 2013; L

uscher et al.,
2014). Maltoni et al. (2007) evaluated the feeding values of the different grasslegume mixtures and pointed
out that in mixtures, there is less seasonal variation in
forage quality than in pure stands. According to Norton
and Volaire (2012), it may thus be possible to develop a
stable pasture mixture that contains summer dormant
and summer active species/varieties, such that the
moisture available throughout the year can be utilized
by one or more components of the mixture. Our metaanalysis did not reveal any variations in the response of
grasses, forbs and legumes to elevated CO2, warming or
drought (Figure 2). Climate change is thus not
expected to directly affect the chemical compositions of
grasses and legumes in mixtures, but could shift their
relative abundance according to the previously discussed adaptations of functional types.

Future research needs

In this review, we analysed the effects of elevated
CO2, warming and precipitation change on important
characteristics of forage. While many studies have
investigated changes in N content, less information is
available for TNC. Structural carbohydrates and in vitro
digestibility have been recorded in a very limited
number of climate manipulation experiments and
were usually reported to be present in similar quantities to those found under current climatic conditions.
Apart from changes in N and TNC concentration as a
result of elevated CO2, we did not observe notable
changes in forage quality induced by climate change
factors. Shifts in grassland botanical composition and
phenological stage during harvest times can either
buffer or accentuate the direct effect of a climate factor. We thus identified a need for greater knowledge
about the effects of climate change on the species
composition of grasslands and to separate the effect of
climate-change factors on the plants (at a given phenological stage) from that of a change in the phenological stage (e.g. due to temperature). Our meta-analysis
outputs (e.g. contrasting response of N to each factor
in Figure 1), literature reviews (Dieleman et al., 2012)
and some pioneer experiments testing combinations of
climatic factors (Read and Morgan, 1996; Larsen et al.,
2011; Cantarel et al., 2013) suggest that combined
effects on forage quality cannot be easily predicted
from single-factor responses. Therefore, further experiments should also be carried out that focus on the
combined effects of climate-change factors that have
previously been rarely investigated.
The effects of extreme events have only occasionally
been investigated (Walter et al., 2012a,b; Benot et al.,
2013; Zwicke et al., 2013; Jung et al., 2014; Niderkorn
et al., 2014), despite the fact that pioneer studies suggest

250 B. Dumont et al.

that responses to extreme events can differ from those

obtained under moderate warming and drought (Walter et al., 2012a; Zwicke et al., 2013). Additionally, very
limited data are available for Mediterranean areas,
which prevented any comparison apart from the
response of N forage content to elevated CO2.
The field manipulation experiments we used in the
meta-analysis have a strong predictive power, but
may also exacerbate the effects of natural climatic
changes on plant ecosystem processes (Leuzinger
et al., 2011), which might in turn affect forage quality.
Management options could buffer the effects of
climate change on forage quality. However, they were
only investigated in a limited number of studies with
mown grasslands (e.g. Zanetti et al., 1997; Daepp
et al., 2000; Picon-Cochard et al., 2004) and more
recently in grazed communities (Henkin et al., 2010;
Deleglise C., personal communication). Long-term
experiments that follow vegetation dynamics as a
response to climate variability Long-term Terrestrial
Ecosystem Research (LTER) in the US, Syst
emes
dObservation et dExp
erimentation au long terme
pour la Recherche en Environnement (SOERE) in
France, etc. are closer to natural pedoclimatic conditions and take climate variability into account (gradual natural trends, extreme events). They allow
testing of the effects of grazing management and measurement of induced shifts in plant composition and
phenological stage. It is thus likely that predicting forage quality of grasslands in a changing climate will
require both approaches be pursued in a coordinated
way.

Acknowledgments
This review is an updated version of a paper presented
to the FAO-CIHEAM joint meeting of Mountain Pastures, Mediterranean Forage Resources and Mountain Cheese networks held in Clermont-Ferrand,
2426 June 2014. The study was funded by FP7KBBE-2010-4 project AnimalChange: An integration
of mitigation and adaptation options for sustainable
livestock production under climate change (Project
Number: 266018).

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Supporting Information
Additional Supporting Information may be found in
the online version of this article:
Appendix S1. Full list of articles used in the metaanalysis.

2015 John Wiley & Sons Ltd. Grass and Forage Science, 70, 239254