Biological Conservation 100 (2001) 335±343

www.elsevier.com/locate/biocon

Are rice®elds a good alternative to natural marshes for waterbird

communities in the Camargue, southern France?
Christophe Tourenq a,b,*, Robert E. Bennetts a, Hubert Kowalski c, Emmanuel Vialet d,
Jean-Laurent Lucchesi e, Yves Kayser a, Paul Isenmann b
a
Station Biologique de la Tour du Valat, le Sambuc, 13200 Arles, France
b
CEFE/CNRS, 1919 route de Mende, 34293 Montpellier Cedex 5, France
c Âserve
Re Nationale de Camargue, La CapellieÁre, 13200 Arles, France
d
Domaine La Palissade, Conservatoire du Littoral, 13129 Salin de Giraud, France
e
Marais du Vigueirat, Conservatoire du Littoral, Mas Thibert, 13104 Arles, France

Received 22 June 2000; received in revised form 17 November 2000; accepted 19 December 2000

Abstract
Rice cultivation has frequently been suggested to provide an important wetland habitat for waterbirds. However, in contrast to
most other regions of the Mediterranean, the Camargue still has a substantial amount of surface area of natural marshes. Thus, we
compared the abundance, species richness, and community composition of waterbirds in rice®elds and natural marshes of the
Camargue, during a one-year study. Based on surveys conducted at 4±7 day intervals in 1997±1998, our results suggest that natural
marshes had substantially greater abundance of waterbirds, with ca. 99% of the individuals having been observed in natural mar-
shes. Estimates of species richness and associated parameters further indicated that rice®elds were clearly less rich than natural
marshes. Although our results were rather striking for the Camargue, they may not be applicable to other regions because of the
relatively high availability of natural marshes and di€erences in management of rice®elds. # 2001 Elsevier Science Ltd. All rights
reserved.
Keywords: Agricultural wetlands; Camargue; Habitat selection; Rice®elds; Waterbirds

1. Introduction fauna (e.g. waterbirds) has been frequently discussed. In

The increased loss of natural wetlands throughout the
World may be in the form of: (1) a complete loss (e.g.
drainage for urbanization or dry cultivation); (2) a
degradation in quality (e.g. contamination or alteration
of hydrologic regimes); or (3) a conversion of land to
aquatic agriculture, which changes the structure and the
function of the habitat, but retains the area as a wet-
land. Of the latter, rice (Oryza sp.) cultivation is by far
the most common and 40% of the world population
now depends on this food source (Fasola and Ruiz,
1997). As a consequence, in many regions, natural wet-
lands have now virtually disappeared and rice®elds have
become the primary wetland habitat. Given the near
complete loss of natural wetlands in these areas, the
value of rice®elds as an alternative habitat for local
* Corresponding author. Fax:+33-4-90-97-20-19.
E-mail address: tourenq@tour-du- valat.com (C. Tourenq).
0006-3207/01/$ - see front matter # 2001 Elsevier Science Ltd. All rights reserved.
PII: S0006-3207(01)00037-4
regions of intensive rice cultivation, it has been sug-
gested that rice®elds may provide suitable habitat for
waterbirds during wintering and migrating (e.g.
Hobaugh et al., 1989; TreÂca, 1994; Elphick and Oring,
1998) or during breeding (e.g. Hohman et al., 1994;
Acosta et al., 1996; Lane and Fujioka, 1998).
The Mediterranean Region is a case in point: rice
cultivation is widespread, and has been suggested to
provide an extremely important habitat for waterbirds
(e.g. Fasola and Ruiz, 1996, 1997; Fasola et al., 1996).
Furthermore, in many parts of the Mediterranean, nat-
ural marshes have been greatly reduced (Fasola and
Ruiz, 1997), which may alter the relative importance of
rice®elds as an alternative habitat. In contrast to most
other parts of the northern Mediterranean, the Camar-
gue still has a substantial amount of surface area of
natural marshes (Table 1), although it too has been
rapidly disappearing for these last 40 years (Tamisier
and Grillas, 1994). In this study, we compared the
336 C. Tourenq et al. / Biological Conservation 100 (2001) 335±343

abundance and species richness of waterbird commu-
nities in rice®elds and natural marshes in the Camargue.
2. Study area
The Camargue is the delta of the RhoÃne river located
on the Mediterranean coast of southern France
(43 300 N, 4 300 E; Fig. 1). This deltaic complex, covering
an area of about 1450 km2, is one of the most important
wintering and breeding site for waterbirds in Europe
(Heath and Evans, 2000). The habitat is a mosaõÈc of
fresh, brackish and saline wetlands interspersed with
areas of intensive agriculture (Tamisier and Grillas,
1994). Rice currently is the primary crop of the Camar-
gue; with alternative species being limited by high salt
loads (Barbier and Mouret, 1992).
In the Camargue, rice is traditionally cropped in ¯at
areas, which are typically ¯ooded just before sowing
(late April±early May). Germination takes place 7±15

Table 1
Proportion of area occupied by rice, wetlands and other habitats in the main northern Mediterranean rice cultivation regions (from Tamisier, 1996;
Fasola and Ruiz, 1997; Mathevet, 2000)

Region

Ebro Delta (Spain) Camargue (France) Padania (Italy)

Total surface area (ha) 32,000 145,000 538,000

Percentage of surface area comprised of rice®elds 66 16 41
Percentage of surface area comprised of wetlandsa 23 59 1
Percentage of surface area comprised of dry landsb 11 25 58
Percentage of wetland surface area comprised of rice®elds 74 22 98
a
Including marshes, rivers, lagoons, salt pans and wet pastures.
b
Including urban and industrial habitats, dry crops, woodlands.

Fig. 1. Study area, showing the Camargue delta and the Fumemorte Basin (dashed line). Inset shows the location of the study area in France. Sites
cited in the text are indicated with stars (P, Palissade; S, Salin de Badon; T, Tour du Valat; V, Vigueirat).
 C. Tourenq et al. / Biological Conservation 100 (2001) 335±343
days later and rice plants emerge from water ca. 30 days
after sowing. They attain maximum height in August,
and harvest takes place in September±October. Once
seedlings are rooted, water levels (20±30 cm) are peri-
odically reduced (5±10 cm) several times during the
season for agricultural operations (herbicides and pesti-
cides spraying, or fertilisation). Rice®elds are com-
pletely dried some days before harvesting, and the post-
harvest (October±March) stubble is generally burned
and ploughed. Some farmers ¯ood their rice®elds and
maintain water levels at  10 cm to attract wildfowl for
hunting but most rice®elds remain dry or only partially
¯ooded by rainfall throughout the winter. Moreover,
since the middle 1980s, due to growing use of mechan-
isation practices, changes in water management have
occurred: ®elds are now dried actively by pumping in
late December±January to allow land preparation
(laser-levelling) in March (Barbier and Mouret, 1992;
Mathevet, 2000).
3. Methods
3.1. Bird counts
We counted waterbirds, as de®ned by Rose and Scott
(1997), at ca. 4±7 day intervals in rice®elds and natural
marshes between March 1997 through March 1998 in
the eastern part of the Camargue. Each survey lasted ca.
5 h starting at sunrise. Upon arrival at each wetland a
scan-sampling of 10 min was conducted. We then
walked around each habitat block along dikes and
canals to count birds that may have been concealed
from view by vegetation. Birds disturbed and ¯ushing
from a ®eld were included in our counts but individuals
only seen just passing overhead were not. Terns and
gulls seen foraging on ¯ying insects or emergent larvae
were included.
We distinguished four seasons according to the pat-
terns of spring and autumn migration and breeding of
waterbirds species observed in the Camargue (Blondel
and Isenmann, 1981; Isenmann, 1993; Thibault et al.,
1998): spring (March±April; SM), breeding (May±July;
BRE), autumn (August±October; FM) and winter
(November±February; WIN).
3.2. Habitats
Surveys in rice®elds were conducted on a random
selection of 47 out of 1978 ®elds (94 ha, mean=2
ha  1.17). While rice®elds only occur in fresh water and
have a temporary hydrologic regime (i.e. seasonally
¯ooded), in contrast, natural marshes in the Camargue
can be quite variable. They can range in salinity from
highly saline lagoons (salinity more than 15 g l 1) to
freshwater marshes (salinity of less than 1 g l 1). They
337
also have a wide variety of hydrologic regimes, ranging
from temporary rainfall-dependent marshes to perma-
nent lakes and lagoons. Our intention here was not to
test the e€ects of all the potential environmental factors
on bird communities within natural marsh systems but
was to compare the use of natural marshes and rice-
®elds. Consequently, to reduce the potential for our
results to be an artifact of the greater diversity of nat-
ural habitats, we restricted our initial analyses to tem-
porary freshwater marshes. For this restricted subset,
we included surveys in natural wetlands conducted in
the same part of the Camargue in the Marais du Vig-
ueirat (507 ha) and on marshes within the Tour du
Valat Reserve, including the Marais du Saint Seren
(61.5 ha), Baisse SaleÂe (50.8 ha) and Grenouillet (78 ha).
However, for a few comparisons (only where speci®cally
noted), we included surveys conducted on all natural
marshes, regardless of salinity or hydrologic character-
istics. These additional surveys included marshes of the
Salin de Badon (National Reserve of Camargue, 90 ha)
and La Palissade (French Coast Conservancy; 184 ha,
Fig. 1).
3.3. Data analysis
To compare species richness between rice®elds and
natural marshes, we used the program COMDYN
(Hines et al., 1999). The estimators of COMDYN are
described in detail by Boulinier et al. (1998) and Nichols
et al. (1998). Because not all species have an equal
probability of detection, their approach uses species
richness in a capture-resighting context where detect-
ability of a given species can be explicitly incorporated
into the estimates of richness. In this context, a matrix is
built where a given species is assigned a 1, if it was
observed on a given survey, and a 0, otherwise. In much
the same way that probability of detecting individuals
can be estimated from this matrix in a survival context
using maximum-likelihood estimation (e.g. Lebreton et
al., 1992), the probability that a given species is detected
in this context (Burnham and Overton, 1979). Thus,
species richness is estimated using the jackknife esti-
mator which assumes that detection probabilities are
heterogeneous among species (Burnham and Overton,
1979; Boulinier et al., 1998; Nichols et al., 1998).
The parameters considered here are de®ned as: Ri,
raw numbers of species observed in habitat i; Ni, esti-
mated numbers of species present in habitat i; l, the
relative species richness estimated as Ni/Nj or Nj/Ni; l0 ,
an alternative form of l, estimated as Ri/Rj, or Rj/Ni,
used when the detection probabilities do not di€er
among the comparison groups; and Bi,j, the number of
species present in habitat i but not in habitat j.
Associations between the frequency of observations
for each species in natural marshes and rice®elds were
determined using adjusted residuals (Haberman, 1973)
338 C. Tourenq et al. / Biological Conservation 100 (2001) 335±343

from a chi-squared test of independence. Unadjusted the little bittern (Ixobrychus minutus), only one time
residuals are highly in¯uenced by the expected values during our surveys, although both species usually occur
and are therefore dicult to interpret. Adjusted resi- in natural freshwater marshes (Blondel and Isenmann,
duals are standardized to account for the expected 1981; Hafner et al., 1982). The third species, the whim-
values in such a way that they are distributed as brel (Numenius phaeopus) was observed only four times,
approximately standard normal (i.e. a residual of 1.96 is and is more commonly associated with coastal brackish
approximately equal to an  of 0.05). or saltwater marshes, rather than either rice®elds or
natural freshwater marshes (Blondel and Isenmann,
1981). In contrast, 28 species were recorded exclusively
4. Results in natural marshes. If we take into account detection
probabilities, the estimated number of species exclusive
4.1. Species abundance to natural marshes (Bn,r) ranged from 18 species during
the breeding season to 37 in autumn (Fig. 3). In con-
We carried out a total of 154 bird surveys, of which 69 trast, the estimated number of species found exclusively
were conducted in temporary freshwater natural mar- in rice®elds (Br,n) ranged from 1.6 during the breeding
shes and 85 in rice®elds. We recorded a total of 299,573 season and autumn to 2.9 during winter. Many of these
bird observations involving 59 species (Table 2). Of
these 2801 (1%) were in rice®elds and 296,772 (99%)
were in natural marshes. This extreme disparity occurs
even though a greater number of surveys were con-
ducted in rice®elds and natural marshes were limited to
temporary freshwater marshes. When expressed per
survey the number of individuals observed in natural
marshes compared to rice®elds was 4301 per survey for
natural marshes compared to 33 per survey for rice-
®elds. Further, this overall higher abundance of birds in
natural marshes occurred for all taxonomic orders,
although some orders in particular (e.g. Anseriformes)
contributed largely to the extreme disparities (Table 2).

4.2. Specied richness

Both the raw number of species observed (Ri) and the

estimated number of species (Ni) were substantially Fig. 2. Relative species richness (li 95% C.I.) of natural marshes
and rice®elds during each season. A value of 1.0 indicates no di€erence
lower in rice ®elds than in natural marshes during all in species richness between the habitats. Values >1.0 indicate higher
seasons (Table 3). If all natural marshes are considered, species richness in natural marshes, and values <1.0 indicate higher
rather than the subset restricted to temporary fresh- species richness in rice®elds.
water marshes, the relationship becomes even stronger.
Our results indicated an unequal probability of
detection between habitats in spring (P<0.001) and
winter (P=0.003). Thus, for testing relative species
richness (li), we used the estimator based on unequal
detection probabilities (Nichols et al., 1998, Hines et al.,
1999). However, it is worth noting that the choice of
estimator used did not alter our results. Estimates of
relative species richness (li) further con®rmed higher
richness in natural marshes compared to rice®elds dur-
ing all seasons (Fig. 2). Disparity between the habitats
was greatest in winter and autumn, and lowest in spring
and summer.

4.3. Species composition

Fig. 3. Estimated number of exclusive species (Bi  S.E.) during each
Only three species were observed exclusively in rice- season found in natural marshes, but not in rice®elds (NM), and the
®elds during our surveys (Table 2). The squacco heron number exclusive species found in rice®elds, but not in natural mar-
(Ardeola ralloides), was observed only seven times and shes (RF).
 C. Tourenq et al. / Biological Conservation 100 (2001) 335±343 339

Table 2
Number of birds observed and the number per survey of each species in rice®elds and natural marshes in the Camargue

Species Scienti®c name Number observed Number/survey

Natural marshes Rice Total Natural marshes Rice

Podicipediformes
Great crested grebe Podiceps cristatus 75 0 75 1.09 0.00
Black-necked grebe Podiceps nigricollis 10 0 10 0.14 0.00
Little grebe Tachybaptus ru®collis 120 0 120 1.74 0.00
Pelecaniformes
Great cormorant Phalacrocorax carbo 675 4 679 9.78 0.04

Ciconiiformes
Great white egret Egretta alba 69 2 71 1.00 0.02
Grey heron Ardea cinerea 476 151 627 6.90 1.77
Purple heron Ardea purpurea 53 49 102 0.77 0.57
Squacco heron Ardea ralloides 0 7 7 0.00 0.08
Little egret Egretta garzetta 1307 49 1356 18.94 0.57
Cattle egret Bubulcus ibis 904 494 1398 13.10 5.81
Black-crowned night heron Nycticorax nycticorax 30 3 33 0.43 0.03
Little bittern Ixobrychus minutus 0 1 1 0.00 0.01
Great bittern Botaurus stellaris 3 0 3 0.04 0.00
White stork Ciconia ciconia 1 0 1 0.01 0.00
Phoenicopteriformes
Greater ¯amingo Phoenicopterus ruber 5928 117 6045 85.91 1.37
Anseriformes
Mute swan Cygnus olor 39 0 39 0.57 0.00
Greylag goose Anser anser 6409 0 6409 92.88 0.00
Northern shoveler Anas clypeata 31,863 0 31,863 461.78 0.00
Northern pintail Anas acuta 7671 0 7671 111.17 0.00
Common teal Anas crecca 89,290 0 89,290 1294.06 0.00
Eurasian wigeon Anas penelope 1026 0 1026 14.87 0.00
Mallard Anas platyrhynchos 63,918 313 64,231 926.25 3.68
Garganey Anas querquedula 182 0 182 2.64 0.00
Gadwall Anas strepera 37,548 0 37,548 544.17 0.00
Common pochard Aythya ferina 133 0 133 1.93 0.00
Tufted duck Aythya fuligula 184 0 184 2.67 0.00
Red-crested pochard Netta ru®na 7125 0 7125 103.26 0.00
Common shelduck Tadorna tadorna 494 24 518 7.16 0.28
Gruiformes
Common coot Fulica atra 22,869 0 22,869 331.43 0.00
Common moorhen Gallinula choloropus 6 13 19 0.96 0.15
Charadriiformes
Black-winged stilt Himantopus himantopus 502 0 502 7.28 0.00
Northern lapwing Vanellus vanellus 6857 178 7035 99.38 2.09
European golden plover Pluvialis apricaria 9 0 9 0.13 0.00
Kentish plover Charadrius alexandrinus 14 0 14 0.20 0.00
Little ringed plover Charadrius dubius 132 4 136 1.91 0.04
Greater ringed plover Charadrius hiaticula 6 0 6 0.09 0.00
Dunlin Calidris alpina 717 0 717 10.39 0.00
Common sandpiper Actitis hypoleucos 10 15 25 0.14 0.17
Spotted redshank Tringa erythropus 31 7 38 0.45 0.08
Wood sandpiper Tringa glareola 128 66 194 1.86 0.77
Common greenshank Tringa nebularia 53 31 84 0.77 0.36
Green sandpiper Tringa ochropus 33 8 41 0.48 0.09
Marsh sandpiper Tringa stagnatilis 2 0 2 0.03 0.00
Common redshank Tringa totanus 2 16 18 0.03 0.18
Common snipe Gallinago gallinago 398 13 411 5.77 0.15
Bar-tailed godwit Limosa limosa 2670 0 2670 38.70 0.00
Eurasian curlew Numenius arquata 4 0 4 0.06 0.00
Whimbrel Numenius phaeopus 0 4 4 0.00 0.04
Ru€ Philomachus pugnax 634 2 636 9.19 0.02
Jack snipe Lymnocryptes minimus 1 0 1 0.01 0.00
(continued on next page)
340 C. Tourenq et al. / Biological Conservation 100 (2001) 335±343

Table 2 (continued)
Species Scienti®c name Number observed Number/survey

Natural marshes Rice Total Natural marshes Rice

Yellow-legged gull Larus cachinnans 2230 225 2455 32.32 2.64

Mediterranean gull Larus melanocephalus 2 2 4 0.03 0.02
Little gull Larus minutus 1 0 1 0.00 0.01
Black-headed gull Larus ridibundus 3850 977 4827 55.80 11.49
Caspian tern Sterna caspia 2 0 2 0.03 0.00
Common tern Sterna hirundo 2 0 2 0.03 0.00
Gull-billed tern Sterna nilotica 71 23 94 1.03 0.27
Whiskered tern Chlidonis hybrida 1 2 3 0.01 0.02
Black tern Chlidonis niger 2 1 3 0.03 0.11

species are not known to occur commonly in rice®elds
of the Camargue.
A similar pattern emerges if we consider the frequency
of counts for each species, rather than the presence or
absence of a given species. During each season, species
showed a higher frequency of observations in one habi-
tat or another. Of those that signi®cantly departed from
expected values (at =0.05) an overwhelming number
were observed in higher than expected frequencies in
natural marshes compared to rice®elds (Fig. 4). In every
season except spring, only one species was found in
higher than expected frequencies in rice®elds, although
it was a di€erent species for each season. These were
cattle egret (Bubulcus ibis) during winter (P=0.022),
common redshank (Tringa totanus) during the breeding
season (P=0.007), and purple heron (Ardea purpurea)
during autumn (P<0.001). During spring, ®ve species
showed higher than expected frequencies in rice®elds:
whimbrel (P=0.026), common sandpiper (Actitis hypo-
leucos; P=0.003), wood sandpiper (Tringa glareola;
P=0.022), gull-billed tern (Sterna nilotica; P<0.001)
and black-headed gull (Larus ridibundus; P<0.001). In
contrast, the number of species showing a signi®cant
selection of natural marshes ranged from 27 during the
breeding season to 34 during spring.
5. Discussion
The number of species observed, estimates of species
richness and relative species richness, and the number of
species present in natural marshes but not in rice®elds,
all indicated that natural marshes had a greater abun-
dance, species richness, and number of exclusive species.
The greatest di€erences we observed in species richness
between natural marshes and rice®elds was during
autumn and winter seasons. The estimate of relative
species richness (li) showed that these di€erences
decreased during spring and breeding seasons.
Although both habitat types included in our analysis
were seasonally inundated, there was a di€erence in
timing of inundation. Rice®elds are typically ¯ooded
from spring to autumn, whereas temporary freshwater
marshes are ¯ooded with autumn±winter rains. If not
¯ooded naturally by autumn±winter rains or by active
pumping for game hunting after the harvest time, rice-
®elds remain dry during winter. This di€erence in timing
may explain the exceptionally higher use of natural
wetlands by wintering waterbirds populations in the
Camargue, even though higher use of natural marshes
occurs during all seasons.
Rice®elds are intensively used in spring by some larids
and shorebird species because of the coincidence of
arrival of pre-nuptial migrants (whimbrel, wood sand-
piper and common sandpiper) and breeders (gull-billed
tern, black-headed gull) with the ¯ooding of rice®elds in
March±April (Blondel and Isenmann, 1981; Isenmann,
1993; Thibault et al., 1998; this study). Flooding dra-
matically enhances the surface appearance of earth-
worms and emergence of aquatic insects (Viala, 1980;
Suhling et al., 2000; personal observation) and, at this
time, rice®elds are most similar to mud-¯ats and wet

Table 3
Observed number of species (Ri) and estimated number of species (Ni S.E.) for natural marshes and rice®elds

Habitat Winter Spring Breeding Autumn

Ri Ni ( S.E.) Ri Ni ( S.E.) Ri Ni ( S.E.) Ri Ni ( S.E.)

Rice®elds 11 12.5 (1.3) 24 33.3 26 36.1 (5.4) 13 18.3 (3.6)

Natural (temporary freshwater marshes)a 35 37.1 (2.8) 45 51 39 50.4 (5.2) 43 53.7 (5.5)
Natural (all)b 43 44.2 (2.2) 54 57.9 59 68.4 (4.8) 61 63.1 (1.6)
a
Restricted subset of natural marshes (temporary freshwater) that most closely represented the hydrologic conditions of rice®elds.
b
Includes all natural marshes, regardless of hydrology or salinity characteristics.
 C. Tourenq et al. / Biological Conservation 100 (2001) 335±343
meadows typically used for foraging by these species in
the Camargue (Blondel and Isenmann, 1981; Isenmann,
1993; Sadoul, 1996). However, this use occurs over a
relatively short time period, and after the rice crops
germinate in May±June, gulls, terns and shorebirds
often desert rice®elds for natural marshes.
In autumn, rice®elds were selected by purple herons.
This may re¯ect the post-breeding dispersion of local
populations and the arrival of individuals from north-
ern populations (northwest France, Netherlands) in the
Camargue (Cramp and Simmons, 1977; Hafner, perso-
nal communication). Since temporary freshwater mar-
shes are often dry at the end of the summer, rice®elds
may provide valuable alternative foraging habitats for
this migrant species, necessary to build their fat reserves
before migration. Cattle egrets showed a strong pref-
erence for rice ®elds in winter. This period of high use is
associated with post-harvest ploughing (by tractors)
which can result in important surges of prey availability
(Bredin, 1983; Lombardini et al., 2001).
Seasonal changes are not the only temporal e€ect on
habitat use. Some species (e.g. several species of water-
fowl, ¯amingos, and night herons) forage extensively at
night (Tamisier, 1971; Cramp and Simmons, 1977,
Blondel and Isenmann, 1981; Pirot et al., 1984). Thus,
the use of rice®elds by nocturnally foraging species may
be under-represented in our daily counts, and our abil-
ity to derive inferences for this segment of the avian
fauna is consequently limited.
Elphick (2000) suggested recently that if managed
appropriately, rice®elds may provide valuable foraging
habitats, replacing the function of natural wetlands on
which rice®elds were cultivated. Although our results
were quite dramatic indicating much higher use of nat-
ural marshes by waterbirds, our ®ndings are not readily
extendable to other ecosystems. First, unlike many
Fig. 4. Number of species that showed a signi®cant association at
=0.05 during each season between the number of individuals coun-
ted and the habitat type. Associations where higher than expected
values were found in natural marshes are shown in solid bars and
associations where higher than expected values were found in rice®elds
are shown in open bars.
341
other regions, particularly throughout the northern
Mediterranean, natural marshes are still relatively
available in the Camargue. Most of them are protected
areas or managed for game hunting (Tamisier and
Grillas, 1994; Tamisier, 1996), providing either suitable
foraging grounds, breeding or resting places for water-
birds. In regions where they are not available (e.g. Ebro
delta, Padania), rice®elds may o€er the only wetland
habitat available for waterbirds. Thus, bene®ts of rice-
®elds may be much greater in such regions than are
apparent in the Camargue. A second factor limiting our
inference to other regions, is that management practices
of rice®elds di€ers greatly among regions. In contrast to
the Camargue, rice®elds are kept ¯ooded through the
winter in many regions for game hunting (mainly
waterfowl). During this season, they may be extensively
used by waterbirds for foraging on rice grains left over
from the harvest, and on aquatic vegetation and/or
invertebrates that would otherwise be absent (Ferrer,
1986; Llorente et al., 1986; Hobaugh et al., 1989; Beck
et al., 1999; Elphick, 2000). In the Camargue, only
about 10% of rice®elds are managed for game hunting
(Mathevet, 2000) and in our study area, we observed
this practice on only 6% of our study ®elds (Tourenq et
al., unpublished data). Hafner et al. (1986) also reported
a considerable decline in recent years in the use of rice-
®elds in the Camargue by little egrets (Egretta garzetta)
which they attributed to increased use of certain pesti-
cides since the 1980s. Thus, although our data indicated
substantially higher use of natural marshes by water-
birds in the Camargue, the disparity between use of
these habitats might be reduced if management of rice-
®elds takes into account use by waterbirds.
Disturbance may also in¯uence the use of habitats by
waterbirds. However, it is not clear in the Camargue,
how this factor in¯uences use of di€erent habitats. On
the one hand, the activities associated with growing rice
(e.g. spraying), may induce a periodic disturbance (in
addition to any e€ects from the spraying itself). How-
ever, such areas are also not generally open to public
access and are therefore less disturbed on a daily basis.
This study was not designed to test for the e€ects of
disturbance, although it is clearly one element that
needs to receive further attention, not only in the con-
text of agricultural habitats.
Finally, the importance of rice®elds for waterbirds may
be most pronounced during extremely dry years when
natural marshes are dry. Our study included a relatively
dry year (total annual rainfall=414.60 mm, compared to
the mean annual rainfall of 625.40 mm for the 1963±1999
period), although more extreme years (e.g. 252 and 325.6
mm for 1989 and 1992, respectively) have been recorded in
the Camargue (P. Chauvelon, personal communication).
Thus, our results are reasonably applicable to relatively
dry years, but do not allow us to extend reliable inference
to extreme conditions which may periodically occur.
342 C. Tourenq et al. / Biological Conservation 100 (2001) 335±343
Acknowledgements
We are grateful to the farmers of the Fumemorte
Basin who allowed us to collect data in their property.
We thank J.C. Bri€aud, Conseratoire du Littoral-La
Palissade, E. Coulet, ReÂserve Nationale de Camargue,
the Station Biologique de la Tour du Valat, especially P.
Chauvelon, F. MesleÂard and N. Sadoul, for their sup-
port in this study. We are indebted to N. Beck, J. Ber-
tagne, E. Didner, L. Durieux, N. Hecker, K.
Lombardini, G. Massez, A. Mora, D. Tatin, D. Vernet,
who helped us to collect data in the ®eld. This study was
funded by the Station Biologique de la Tour du Valat,
the SansouõÈre Foundation, the MAVA Foundation, and
the Centre FrancËais du Riz.
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