Bird assemblages as bio-indicators of water regime

Biological Conservation 106 (2002) 115–127
www.elsevier.com/locate/biocon
Bird assemblages as bio-indicators of water regime management and
hunting disturbance in natural wet grasslands
J.-M. Paillissona,*, S. Reeberb, L. Mariona,b
a
UMR 6553 Ecobio, Laboratoire d’Evolution des Systèmes naturels et modifiés, Université de Rennes I, Campus de Beaulieu,
F-35042 Rennes Cedex, France
b
Réserve naturelle du Lac de Grand-Lieu, Société Nationale de Protection de la Nature, 15 rue de la Châtaigneraie, F-44380 Bouaye, France
Received 11 April 2001; received in revised form 27 July 2001; accepted 24 October 2001
Abstract
Responses of the waterbird community to the management regime of a wet grassland system (primarily small changes in the
water regime but also hunting disturbance) in a large floodplain lake, Grand-Lieu, were studied during three consecutive years
(winter and spring in 1998–2000). These temporarily flooding grasslands (1100 ha) constituted a very important feeding area by
supporting large flocks of waterbird species (52 regular spp., totalling up to 14 250–22 850 birds). A global similar seasonal pattern
in the presence of waterbird species was recorded whatever the year. The March–May period was a key phase with the maximum
species richness (42–48 spp.) and the maximum abundance (30–40% of the total according to year, essentially Anseriformes). Late
in spring Ciconiiformes and to a lesser extent some waders exploit this feeding area. Nevertheless some changes in bird assemblages
were exhibited according to the management regime (a decreasing spring water level from 1998 to 2000, and an exceptional hunting
ban in January 2000, instead of an usual stop in late February). The hunting disturbance clearly limited diurnal accessibility of
ducks to wet grasslands in January and February 1998 and 1999. Also, the duck population in flooding grasslands increased by 55–
65% in January 2000 when hunting was prohibited and in the same time the richness species grew from 14–19 spp. up to 23 spp. in
2000. The overall impact of a high spring water level on waterbirds as in 1998 and to a lesser extent in 1999 (with respectively 54
and 35 cm of mean water level against 25 cm in 2000) was an increase in diving fish-eating birds and larger flocks of resting gulls.
Conversely these conditions, notably a reduced period with a spring water level under 25 cm in spring (20 days in 1998–1999 instead
of 40 days in 2000) were adverse to numerous ground-feeding waterbirds (Ciconiiformes and waders) that require shallow waters.
This study showed that limitation of human disturbance and moderate flooding of wet grasslands can increase their attractiveness
for numerous species of high conservation status. # 2002 Elsevier Science Ltd. All rights reserved.
Keywords: Biodiversity; Community; Multivariate analysis; Water level; Wetland
1. Introduction
Wetlands play an important role in biodiversity
because they are attractive to many species due to their
large habitat diversity and their great productivity providing nutrients and other resources (Weller, 1988;
Elmberg et al., 1994). Birds are among the most conspicuous of wetland animals and various species are
extremely sensitive to large hydrological changes
(Kushlan, 1986a; Crowder and Bristow, 1988; Pyrovetsi
* Corresponding author.
E-mail address: [email protected]
(J.-M. Paillisson).
and Papastergiadou, 1992). Creation of reservoirs
demonstrated immediate effects on waterbird communities (Hunter et al., 1987; Bildstein et al., 1994) and
water conditions are among the main factors affecting
the composition and the abundance of waterbird communities directly and indirectly (Dister et al., 1990;
Briggs et al., 1998; Osiejuk et al., 1999). Water level
fluctuations influence the physical structure of habitats
(zonation of vegetation), the availability and accessibility of food (Clausen, 2000) and the presence of safe
roosting or breeding sites (Green and Robins, 1993;
Guillemain et al., 2000). All these characteristics determine habitat selection by waterbirds (Sanders, 1999)
and especially by migrant birds that depend largely on
the presence of well functioning wetlands along their
0006-3207/02/$ - see front matter # 2002 Elsevier Science Ltd. All rights reserved.
PII: S0006-3207(01)00239-7
116
J.-M. Paillisson et al. / Biological Conservation 106 (2002) 115–127
flyways (Ens et al., 1994; van Eerden, 1997; Madsen,
1998a, b; Ntiamoa-Baidu et al., 1998).
Human disturbances, especially hunting, can interfere
with these factors and limit the accessibility to resources
(e.g. Madsen, 1998a). However, the relative effect of
hunting has not been assessed in relation to other parameters influencing the use of wetlands by waterbirds.
Moreover, the detailed response of different taxonomic
groups of waterbirds to low seasonal changes in water
level has rarely been assessed (Elphick and Oring, 1998).
Indeed, the studies of natural wetlands that have established relationships between water level and bird population changes concerned essentially responses either of
specific groups, Ciconiiformes or ducks (Marion, 1989;
DuBowy, 1996; Dimalexis and Pyrovetsi, 1997; Kingsford and Johnson, 1998; Duncan et al., 1999) or of the
whole community (Hunter et al., 1987; Crivelli et al.,
1995; Briggs et al., 1997; Hertzman and Larsson, 1999)
exclusively to large water depth fluctuations or drainage, while small variations in water level on flooding
surrounding grasslands have been little studied. Also,
most of previous studies have described the responses
on a taxonomic basis rather than on an ecological basis.
The objectives of the present study are to identify
firstly the patterns in the use of a wet grassland system
by the whole waterbird community during a 3-year
period, and secondly the effect of the management
regime of the ecosystem (primarily small changes in the
water regime, but also hunting disturbance) on the species assemblages. We compared the response of the
different species groups, mainly Ciconiiformes, Anseriformes and Charadriiformes, recorded on flooded wet
grasslands over three consecutive years (winter and
spring) with partially controlled water regimes and an
opportunistic exceptional hunting ban imposed during
one of these years. The role of the water level on the
breeding populations of the waterbird community in
the different habitats of the lake will be addressed
in another paper and will complement management
recommendations made in the present study.
Practical management applications are discussed to
define the optimum management regime for preserving
or enhancing the value of the wetland as feeding habitat
for the whole waterbird community and more specifically for some species of high conservation status.
2. Materials and methods
2.1. Study site
The Lac de Grand-Lieu is a shallow, turbid, eutrophic
natural freshwater ecosystem in Western France (47 050
N, 1 390 W). This lake constitutes one of the most
important bird areas in France supporting large numbers of wintering and migrating ducks and Fulica atra
(about 20 000 birds) and breeding populations of ducks
and heron species, the latter representing also one of the
main European breeding populations and the largest
colonies in France for Ardea cinerea, Egretta alba, Platalea leucorodia and Threskiornis aethiopicus (Rocamora
and Yeatman-Berthelot, 1999; Marion et al., 2000). The
whole wetland is designated a Special Protection Areas
under the EC Birds Directive and a Ramsar Site
(Deceuninck et al., 2000).
The wetland is of value because of its diversity of
habitats for waterbirds, with four major complementary
functional units (see Marion et al., 1994, for a more
detailed description). The lake covers 4000 ha in summer and 6300 ha in winter, by flooding adjacent peaty
wet grasslands used mainly as pastures. About 20 km of
the lake margin (2000 ha) are covered by a floating peat
fen, which becomes progressively exposed in summer.
Most of the permanently central flooded area of the
lake is covered from April to October by about 1400 ha
of floating macrophytes. The central open water region
without floating or emergent plants except small patches
of submerged macrophytes covers about 600 ha.
The wet grasslands of the Lac de Grand-Lieu can be
considered as ecotonal habitats, as described by
Dobrowolski (1997), and represent the principal feeding
area of the wetland for wintering and migrating waterbirds. The grassland consists of level fields intersected
by drainage channels. Human activities like mowing
and grazing prevent the growth of trees and have
formed fields with a heterogeneous vegetation structure
dominated by Phalaris arundinacea, Glyceria maxima,
Carex spp. or Eleocharis spp. The present study focuses
on the use of the southwest unit by the waterbird community, the largest and most important part of the wet
grasslands for waterbirds.
2.2. Water regime
A drainage channel flows from the lake to the Loire
estuary 25 km away and a sluice gate regulates the water
level of the lake, essentially during the hydrological
storage period (mainly in winter) by discharging the
water surplus to the outlet. In the past, pressure from
the farming community for land drainage in spring
contributed to reductions in water level and duration of
flooding. During our study, three different water levels
were recorded: a high water level in 1998, a low water
level in 2000 and an intermediate one in 1999 (Fig. 1).
Such a difference, occurring between three consecutive
years in the same site, limits variations due to long term
changes in population dynamics of birds related to
other factors.
The water level is described by using a local depth
measure (Buzay scale=0.47 m above French Geographic Level NGF). The mean level of the wet grasslands is 1.89 m Buzay (Marion and Marion, 1975), with
J.-M. Paillisson et al. / Biological Conservation 106 (2002) 115–127
117
different fixed-observation points at each 5-day interval
to test the overall effect of the two major local descriptors of the management regime (water level and hunting
activity) on the waterbird community.
2.4. Data analysis
Fig. 1. Mean water level in each 5-day interval (from January to July)
on the wet grassland system of the Lac de Grand-Lieu during the 1998–
2000 period. The horizontal line symbolizes the threshold of 25 cm.
a relatively slow variation (SD=0.10 m). Thus a mean
water level of 2.14 m Buzay corresponded to a real
mean water level of 25 cm on the grasslands. For each
year we calculated the length of time that the level was
below this mean threshold of 25 cm commonly defined
as the maximum feeding depth for the majority of
waterbird species, especially Ciconiiformes and Charadriiformes (Owen and Black, 1990; Ntiamoa-Baidu et
al., 1998).
2.3. Bird census
All waterbirds (here defined as Podicipediformes,
Pelecaniformes, Ciconiiformes, Anseriformes, Gruiformes and Charadriiformes) were censused on the
southwest wet grasslands from eight fixed-observation
points covering 1100 ha (the other 300 ha, with many
trees, not being used by large numbers of birds). For
each observation point, waterbird species were counted
individually or in units of 10 when flocks were larger
than 100. When we encountered very large flocks of
resting ducks (> 1000), we first counted them in units
of 100 and then we counted each duck species in units of
10 to control both methods (Reeber, 2000). Given the
open nature of the wet grassland system studied these
counts were likely to estimate absolute abundance
accurately for most species. Nevertheless species for
which this was unlikely to be true (common snipe Gallinago gallinago and little grebe Tachybaptus ruficollis)
are not considered here. Birds seen flying overhead were
not included so that they were not counted again at
another station.
The censuses were conducted at 5-day intervals in
three consecutive years (1998–2000) from the fifth period of 5 days in January, noted Jan V, to the second
period of 5 days in July, noted Jul II. Hunting activity
on the wetland occurred from mid-July to the end of
February in all years except 2000, when an exceptional
ban was imposed in January (due to the Erika disaster)
allowing the effects of disturbance on the waterbird
community to be assessed. We combined data for the
We used standard measures of species diversity to
characterize the patterns of waterbird community in the
wet grassland system: species richness and Shannon
diversity (Guillory, 1999). A mean value of the Shannon diversity was calculated for each month from January to July. Annual frequencies of occurrence (% of
species present in all the 5-day intervals) and monthly
abundance were also defined.
The first step of the assemblage analysis was to classify species into groups, achieving this by a posteriori
analysis of their abundance and distribution to identify
species exhibiting similar patterns (Gawlick et al., 1998,
and literature cited therein). We performed a Foucart’s
Correspondence Analysis (CA) on a series of three contingency tables (one per year, counts at 5-day intervals
for all species). This method (rarely used in ecology)
represents a CA based on an average table called a
compromise table (see Foucart, 1978, and Blanc et al.,
1998, for more details of the method). We used three
graphic representations: a graph linking consecutive 5day intervals linked with a line according to years, a
dendrogram based on a clustering procedure (Euclidian
distances and then UPGMA of factorial coordinates—
Unweighted Pair Group Method Algorithm), and plots
of axes for each annual data set to identify species
assemblages on the compromise plane (convex hull
procedure). Analyses and graphics were performed
using ADE-4 software (Thioulouse et al., 1997) and
species with less than 10 birds recorded for each year
were excluded from the matrices. Numbers of waterbirds were log (x+1) transformed prior to analysis.
We used Wilcoxon signed rank tests (SYSTAT Software, 1998) to compare the mean abundance of each
species between the three years to justify patterns of
waterbird species in 5-day intervals and to determine the
sensitivity of species groups to water regime. For each
species the mean abundance was calculated for the same
period of presence for the 3-year period, rather than the
complete period of census. The comparisons were conducted according to the different water regime phases
(Section 3). Finally some complementary comparisons
of mean abundance were performed on the basis
of numerical proportions of breeding population size of
species feeding on the wet grasslands during the most
variable period identified (Reeber, 2000). These latter
tests were used to minimize the effect of possible variations in biogeographical population sizes, already
reduced by the monitoring during three consecutive
years.
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J.-M. Paillisson et al. / Biological Conservation 106 (2002) 115–127
3. Results
3.1. Water regime
The water level in wet grasslands reached a maximum
value in 1998 in January (Jan V: 117 cm, Fig. 1). In
February, the highest water level was recorded in 2000
(83 cm in Feb IV) while the other years were similar.
The smallest between-year difference occurred in March
(54.5 2.5 cm) despite variable patterns (a stable water
level in 1998, a decreasing water level in 1999 and 2000).
Major prolonged differences were noted from April to
mid-June (phase 2) with a high flooding in 1998 (maximum value of 83.5 cm in May I) and a more moderate
one in 1999 (a peak of 56.0 cm in May I) before grasslands were on average exposed in the second part of
June in all the three years. In spring the mean water
level was 53.5 16.5 cm in 1998, 34.5 10.0 cm in 1999
and 24.5 8.0 cm in 2000. Duration of water levels of
less than 25 cm was thus more limited in 1998 and 1999
(20 days, from May V to June III) and twice as long in
2000 (40 days, from May II to June III).
3.2. Composition and biodiversity indices of the
waterbird community
A total of 52 regular different waterbird species was
recorded in the wet grasslands each year, except in 1999
with no Tringa glareola (Table 1). The most abundant
waterbird species were Charadriiformes (27 species),
Anseriformes (13) and Ciconiiformes (8). The different
taxonomic groups included species that spend part of
their life at the study site, some being always present, as
well as migrant species making more temporary use
of the wet grassland system, especially waders (10
species with a frequency of occurrence of less than
50%). There were great differences in the frequency of
occurrence of waterbirds between the three years, notably among Charadriiforme species, but also among
some Anseriformes.
The monthly species richness patterns were generally
similar between the 3 years (Fig. 2), with a maximum
number of waterbird species from March to May (from
39 to 50) and fewer species in January and in July,
especially in the two first years. The species richness
pattern in 2000 was slightly different because of a high
value in January (23 spp.) during the exceptional hunting ban followed by a resumption of hunting in February. This change in human disturbance induced a
marked difference in curve pattern this year comparatively to the usual curves of the other years (see also
mean abundance). The attractiveness of the wet grasslands was prolonged in 2000 since a larger number of
species was recorded in July (30) than for 1998 (19) and
1999 (14). However the species richness was higher in
February 1998 (35) than during the other years (26).
The mean abundance patterns showed three major
results on the use of the wet grassland system (Fig. 2).
The maximum mean abundance of waterbirds was
observed in March (from 11200 to 14 800 respectively in
1999 and 2000, essentially Anseriformes and Gruiformes, Fig. 3) and represented from 30 (2000) to 40%
(1998 and 1999) of the total annual abundance. The
mean abundance was relatively lower in the other
months, especially in the May–July period whereas the
species richness was still high. At this period the wet
grasslands were however largely used by Charadriiformes (41–46%) and Ciconiiformes (13–31%)
which previously used this habitat little or not at all
when the water level was higher (12–21% together).
Finally the grasslands were more heavily used by the
waterbird community in 2000, with more birds counted
in almost all months (Fig. 2).
The Shannon diversity was relatively constant
between months in 1998 with several similar values
(Fig. 4), whereas this index increased in 1999 and 2000
from low values in the first 2 months (1.06–1.35) to the
highest diversity in the May–July period (2.85–3.31).
During the last 2 years reduced values were linked to
dominance of Fulica atra in January and February,
when it accounted for 65–70% of the total abundance
(Fig. 3). The intermediate values were noted when the
waterbird community was large but also composed of
large flocks of Anseriformes (March and April). Finally
the Shannon diversity reached a peak when the community was again diversified and more equilibrated.
3.3. Definition of species assemblages and responses to
the water regime
The multivariate analysis was performed on contingency tables composed of 40 species, excluding species with less than 10 birds recorded for each year. The
first two axes of the Foucart’s CA accounted for 67% of
the total variation in sample-waterbird composition
in the 3 years. The graph linking subsequent 5-day
intervals and the dendrogram of 5-day intervals confirm
the relative similarity of the use of grasslands by the
waterbird community from January to July in all years
(Fig. 5A, B). However, Jan V (with the influence of the
break in hunting in 2000) and to a lesser extent Feb V in
1998 (with a large species richness, see dendrogram) and
the 5-day intervals from May I to Jul II showed major
differences in waterbird patterns between years. The first
axis accounting for 49% of the total variation arranged
mainly species assemblages along a seasonal gradient
in the use of grasslands (Fig. 5C), from wintering species confined in the negative part of the X-axis to species
recorded in spring with positive values. Two groups
were very similar between years (groups 1 and 3).
Group 1 clumped together some Anseriforme species
(Anas crecca, Anas acuta, Anas penelope and Aythya
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J.-M. Paillisson et al. / Biological Conservation 106 (2002) 115–127
Table 1
Species of waterbirds recorded during census of the wet grassland system of the Lac de Grand-Lieu from 1998 to 2000 (scientific and common
names)a
Scientific name
Common name
Species
code
Frequency of
occurrence (%)
Mean abundance
1998
1999
2000
n
Podicipediforme species
Podiceps cristatus
Podiceps nigricollis*
Great crested grebe
Black-necked grebe
POCR
PONI
91.20–97.05
8.80–47.05
9.202.55
2.851.95
3.851.10
0.450.45
5.25 1.80
0.65 0.85
34
23
Pelecaniforme species
Phalacrocorax carbo*
Great cormorant
PHCA
76.45–100
8.853.10
4.951.75
6.45 1.65
34
Ciconiiforme species
Ardeola ralloides**
Bubulcus ibis
Egretta garzetta*
Egretta alba**
Ardea cinerea
Ardea purpurea**
Threskiornis aethiopicus
Platalea leucorodia**
Squacco heron
Cattle egret
Little egret
Great white egret
Grey heron
Purple heron
Sacred ibis
Spoonbill
ARRA
BUIB
EGGA
EGAL
ARCI
ARPU
THAE
PLLE
38.25–47.05
79.40–88.25
75.55–88.25
100
100
55.88–61.75
73.55–79.40
5.90–61.75
–
23.056.25
37.7013.40
4.600.65
141.2537.05
7.852.45
41.7512.65
1.200.95
–
27.2011.95
24.108.20
6.050.90
102.1524.95
6.852.85
51.4021.00
0.250.40
–
92.1036.20
48.9517.20
15.403.10
117.9530.00
12.104.80
58.5020.35
3.85 1.35
–
34
32
34
34
21
31
24
Anseriforme species
Cygnus olor*
Cygnus atratus
Anser anser
Tadorna tadorna
Anas penelope
Anas strepera*
Anas platyrhynchos
Anas acuta
Anas clypeata*
Anas querquedula*
Anas crecca*
Aythya ferina*
Aythya fuligula*
Mute swan
Black Swan
Grey lag goose
Shelduck
Wigeon
Gadwall
Mallard
Pintail
Shoveler
Garganey
Teal
Pochard
Tufted duck
CYOL
CYAL
ANAN
TATA
ANPE
ANST
ANPL
ANAC
ANCL
ANQU
ANCR
AYFE
AYFU
76.45–100
8.80–64.70
5.90–20.60
11.75–44.10
55.90–61.75
73.55–79.40
94.12–100
44.10–50.00
82.35–88.25
67.35–79.40
20.60–32.35
35.30–52.95
8.80–29.40
11.352.15
–
–
–
343.00219.00
109.0082.00
64.5013.50
132.1592.00
970.00820.50
27.6512.50
5.856.55
7.055.05
1.701.50
8.352.55
–
–
–
357.00249.50
120.0083.50
31.559.00
83.5073.50
1006.50730.70
21.158.85
0.850.65
4.353.90
1.001.65
15.254.30
–
–
–
431.00204.00
151.0096.00
33.007.50
202.50135.00
2077.001403.00
24.9511.00
3.30 2.00
8.35 11.50
5.50 8.95
33
–
–
–
21
30
34
24
33
27
20
29
25
Gruiforme species
Fulica atra
Coot
FUAT
100
1647.50412.80
1809.40456.00
3104.55769.00
34
Charadriiforme species
Himantopus himantopus*
Charadrius dubius
Charadrius hiaticula
Pluvialis apricaria*
Pluvialis squatarola
Vanellus vanellus*
Calidris alpina
Philomachus pugnax*
Limosa limosa*
Numenius arquata
Numenius phaeopus
Tringa erythropus
Tringa totanus*
Tringa nebularia
Tringa ochropus
Tringa glareola
Actitis hypoleucos*
Larus melanocephalus*
Larus ridibundus
Larus minutus*
Larus canus
Black-winged stilt
Little ringed plover
Ringed plover
Golden plover
Grey plover
Lapwing
Dunlin
Ruff
Black-tailed godwit
Curlew
Whimbrel
Spotted redshank
Redshank
Greenshank
Green sandpiper
Wood sandpiper
Common sandpiper
Mediterranean gull
Black-headed gull
Little gull
Common gull
HIHI
CHDU
CHHI
PLAP
PLSQ
VAVA
CAAL
PHPU
LILI
NUAR
NUPH
TRER
TRTO
TRNE
TROC
TRGL
ACHY
LAME
LARI
LAMI
LACA
26.45–67.65
29.40–61.75
23.55–50.00
8.80–26.45
14.70–26.45
97.05–100
38.25–52.95
41.20–64.70
41.20–61.75
8.80–17.65
11.75–23.55
20.60–26.45
70.60–76.45
29.40–50.00
5.90–35.30
0–14.70
14.70–32.35
41.20–58.80
100
17.65–47.05
26.45–55.90
3.401.60
5.307.05
–
5.704.70
–
230.80139.30
1.851.15
32.4536.10
39.1522.60
–
6.909.15
–
17.854.40
12.259.00
–
–
0.850.80
3.451.10
1122.00203.50
5.758.90
–
1.651.35
4.603.25
–
0.250.25
–
88.8038.70
2.751.55
50.3539.75
14.7515.70
–
3.404.75
–
17.054.15
9.307.05
–
–
0.300.25
4.051.20
752.00150.00
0.250.15
–
60.5019.55
18.8013.00
–
0.15 0.15
–
122.1537.20
6.85 2.90
18.7020.20
13.8511.20
–
11.809.35
–
43.7519.60
19.6015.20
–
–
2.80 1.95
4.00 2.55
734.00127.50
12.9016.15
–
24
22
–
22
–
34
20
24
29
–
10
–
27
19
–
–
17
20
34
27
–
120
J.-M. Paillisson et al. / Biological Conservation 106 (2002) 115–127
Table 1 (continued)
Scientific name
Common name
Species
code
Frequency of
occurrence (%)
Mean abundance
1998
Larus argentatus
Larus cachinnans
Larus fuscus
Sterna hirundo*
Chlidonias niger**
Chlidonias hybridus*
Herring gull
Yellow-legged herring gull
Lesser black-backed gull
Common tern
Black tern
Whiskered tern
LAAR
LACA
LAFU
STHI
CHNI
CHHY
64.70–94.10
55.90–67.75
64.70–67.65
5.90–20.60
47.05–52.95
52.95–58.80
3.401.65
–
5.753.65
–
12.454.00
258.8595.40
1999
3.251.95
–
3.801.85
–
13.153.85
81.3068.80
2000
2.25 1.35
–
2.05 0.95
–
14.804.10
417.25129.15
n
34
–
31
–
18
20
a
Four letter acronyms correspond to species codes. Species of high (French list, see Rocamora and Yeatman-Berthelot, 1999; or European ‘Birds’
Directive) or very high (national and European criteria) conservation value are mentioned by one or two asterisks respectively, after the scientific
name. Frequency of occurrence (minimum and maximum values for the 3 years) and mean abundance (number of individuals) are presented for the
shared period of occurrence for each species (n=number of 5-day intervals). The mean abundance was not calculated for the rare species (– : n<10
individuals for each year). A natural breeding population of sacred ibis Threskiornis aethiopicus expands in the present site from escaped birds since
1993 (Marion and Marion, 1994).
fuligula) only observed in the early months (peaks of
abundance near Mar V) and insensitive to the water
levels tested (Table 2). Late migrant Charadriiformes
species (Numenius phaeopus, Tringa nebularia and Actitis hypoleucos whose peaks of abundance were reached
roughly in May I) constituted the second markedly
stable group (group 3) and were relatively unaffected by
fluctuations in water level. On the other hand Fig. 5C
also revealed annual differences related to water conditions for species having intermediate coordinates. The
different patterns of water regime between years resulted
in the formation of group 6 in 1999 and 2000 from the
set of waterbird species forming group 5 in 1998. It
combined the majority of non-sedentary breeding Ciconiiforme species foraging in wet grasslands (Bubulcus
ibis, Egretta garzetta, Ardea purpurea and Threskiornis
aethiopicus) but nesting in the surrounding habitats
(floating peat fen) and breeding Charadriiformes in
grasslands (Tringa totanus and Chlidonias niger). All
these species seemed negatively affected by the spring
flooding in 1998 (significant differences in comparisons
of mean abundance during phase 2, Table 2) except
Chlidonias niger. Platalea leucorodia, Himantopus
himantopus and Chlidonias hybridus were added to this
group only in 2000 because of an increased number of
birds feeding in grasslands this year. In contrast to this
latter group, some sedentary species were always noted
in group 5 whatever the year (Podiceps cristatus, Phalacrocorax carbo, Egretta alba, Ardea cinerea, Cygnus
olor, Anas platyrhynchos, Fulica atra, Vanellus vanellus,
Larus ridibundus, Larus cachinnans and Larus argentatus). Most of these species showed a positive relationship with the high water level in phase 2 in 1998 when
no real trend was noted in phase 1 (Table 2). Finally the
other not previously mentioned waterbird species were
not included in the same groups between years first
because of some pairwise differences in mean abundance
(Anas strepera, Anas clypeata, Anas quequedula, Larus
fuscus) and second because of delayed staging for some
migrant species with either no effect of water fluctuations in the use of wet grasslands (Philomachus pugnax,
Limosa limosa and Larus melanocephalus) or no trend
(Charadrius dubius and Calidris alpina) resulting in
group 7 formed in 1999. In the same time comparisons
of mean abundance, based on numerical proportions
(Table 3), confirmed results on the effect of the water
level variations summarized in Table 4. Tests were performed only for waterbird species nesting in the other
habitats of the lake but foraging onto the wet grasslands
in order to assess the attractiveness of the wet grasslands as feeding areas. Comparisons showed trends
similar to those obtained from Table 2: an increasing
proportion of the population size affected by the high
water level of 1998 (Podiceps cristatus, Phalacrocorax
carbo, Ardea cinerea) or by the low water level of 2000
(Egretta alba, Threskiornis aethiopicus and Platalea leucorodia). In the same time no trend was obtained for the
other breeding species whose population size has
increased during the 3 years (Bubulcus ibis, Egretta garzetta and Ardea purpurea).
The second axis of the factorial planes reflected more
the distribution pattern of presence duration in the
waterbird community. The larger the number of 5-day
intervals in which species were counted the more negative the species ordinates were in each assemblage.
4. Discussion
4.1. The avian conservation value of the wet grasslands
The biological integrity and ecological value of a
wetland can be judged by the occurrence and the number of waterbird species that represent a high nature
conservation value (Owen and Black, 1990; van Eerden,
1997). The presence of 26 species of high conservation
value out of a total of 52 species (Table 1) showed that
the temporarily flooding grasslands of the Lac de
J.-M. Paillisson et al. / Biological Conservation 106 (2002) 115–127
Fig. 2. Mean abundance (histograms) and species richness (lines) of
waterbirds recorded in each month of the three years. Values (with a
95% confidence interval) in 1998, 1999 and 2000 are indicated respectively by light grey, white and dark grey histograms for the mean
abundance and by a solid line with circles, a solid line with squares
and a dashed line with diamonds for the species richness.
Fig. 3. Proportion of each taxonomic group in the total abundance
counted each month during the 1998–2000 period. Podicipediforme
and Pelecaniforme species are excluded since they only accounted for
0.02–0.35% of the total number of waterbirds.
Grand-Lieu are really an important ornithological wetland by supporting numerous wintering, migrating and
breeding waterbird species. These wet grasslands constituted a very important feeding area for wintering
ducks, breeding Ciconiiformes, and a stop over migrating site for waders, while few waterbirds nest on these
marsh grasslands. The March–May period was generally a key phase with the maximum biodiversity (42–
48 spp. from a total of 52 spp.) and the maximum
abundance recorded (30–40% of the total bird sightings,
peaks of 14 250–22 850 birds according to years). However some differences were noted between years, and
2000 was characterized by many waterbirds foraging in
the wet grasslands in most of the months and by a rich
and equilibrated community until summer.
4.2. Relationships between patterns of the waterbird
community and the management regime
The multivariate analysis exhibited a relatively similar
seasonal pattern of use of the flooded grasslands by
121
Fig. 4. Mean Shannon diversity (with a 95% confidence interval) of
each month monitored from 1998 to 2000.
waterbirds whatever the year. Both migrating behaviour
(early vs late species) and breeding behaviour (species
with long breeding season vs short late breeding season
or regular territorial feeding inducing small dispersed
birds vs opportunist social feeding with large flocks
of birds) appear to be the main factors determining
this pattern of use of the habitats. Nevertheless some
changes in bird assemblages, notably the formation of
group 6 in 1999 and 2000 from a large set of species,
associated with comparisons of mean abundance within
and between years, revealed the effect of the management regime (water level and hunting disturbance) of
the wet grasslands.
Although regional and/or continental-wide factors
can influence the fluctuations in abundance recorded
among waterbird populations which is particularly true
for migratory species whose population sizes depend on
survival and reproduction in different geographical
areas, sometimes very far apart (Kushlan, 1986b; Duncan et al., 1999), most of the changes in abundance of
these species could probably be attributed to hunting
and water regime factors. The monitoring during three
consecutive years reduces the effect of possible variations in biogeographical population sizes. In any case
tests performed on numerical proportions of the breeding population on the lake that fed on the wet grasslands avoid this eventual biogeographical device
(Table 3). Moreover habitat selection is known to be
strictly related to the availability and accessibility of
food (Clausen, 2000) and the presence of safe roosting
or breeding sites (Green and Robins, 1993; Guillemain
et al., 2000) which are mainly governed by the hydrological and disturbance conditions in wetlands (Ferns
et al., 1989). The changes in location of 5-day intervals in January 2000 (Fig. 5B,C with an unusual stop
of hunting), corresponding mainly to the presence of
large flocks of Fulica atra, showed the weight of the
hunting disturbance. An optimal use of feeding resources by ducks was prevented when wet grasslands were
insecure during the hunting season (January–February).
122
J.-M. Paillisson et al. / Biological Conservation 106 (2002) 115–127
Fig. 5. Results of the Foucart’s Correspondence Analysis on the three-year contingency tables (5-day intervals-species abundance). (A) Plots of
samples (5-day intervals) on the first two axes of the compromise table identifying trajectories of the 3 years. (B) Dendrogram of 5-day intervals
exhibiting the different levels of clustering. 1998 in dotted line, 1999 and 2000 respectively in black solid plain and bold lines. (C) Coordinates and
grouping of the waterbird species on the compromise plot of the two axes (see Table 1 for species codes).
123
J.-M. Paillisson et al. / Biological Conservation 106 (2002) 115–127
Table 2
Level of significance of the difference between the abundance of species during the three years and for the two different phases of water regime
(respectively Jan V–March VI and Apr I–Jul II) using Wilcoxon’s signed rank testa
Comparison of mean abundance
Phase 1
Phase 2
1998–1999
1998–2000
1999–2000
1998–1999
1998–2000
1999–2000
Podicipediforme species
Podiceps cristatus
Podiceps nigricollis
**
**
nsb
*
ns
ns
**
**
ns
Pelecaniforme species
Phalacrocorax carbo
ns
ns
ns
**
**
+**
Ciconiiforme species
Bubulcus ibis
Egretta garzetta
Egretta alba
Ardea cinerea
Ardea purpurea
Threskiornis aethiopicus
Platalea leucorodia
*
*
+**
ns
ns
ns
ns
+**
ns
+**
ns
ns
ns
ns
+**
+*
+*
ns
ns
ns
+*
+**
+*
ns
*
ns
+*
**
+**
+**
+**
*
+**
+**
+**
+**
+**
+**
ns
+**
+*
+**
Anseriforme species
Cygnus olor
Anas penelope
Anas strepera
Anas platyrhynchos
Anas acuta
Anas clypeata
Anas querquedula
Anas crecca
Aythya ferina
Aythya fuligula
ns
ns
ns
**
ns
ns
*
ns
ns
ns
+**
ns
ns
**
ns
+**
ns
ns
ns
ns
+**
ns
ns
ns
*
ns
+**
+*
ns
ns
**
**
ns
ns
**
ns
*
*
ns
**
ns
*
ns
ns
ns
ns
+*
+*
Gruiforme species
Fulica atra
ns
+**
+**
**
+**
+*
Charadriiforme species
Himantopus himantopus
Charadrius dubius
Pluvialis apricaria
Vanellus vanellus
Calidris alpina
Philomachus pugnax
Limosa limosa
numenius phaeopus
Tringa totanus
Tringa nebularia
Actitis hypoleucos
Larus melanocephalus
Larus ridibundus
Larus minutus
Larus argentatus
Larus fuscus
Chlidonias niger
Chlidonias hybridus
ns
+**
*
**
ns
ns
**
ns
ns
ns
ns
ns
*
+**
ns
ns
ns
ns
+**
+*
*
**
+*
ns
**
ns
ns
ns
ns
ns
*
ns
ns
**
ns
+*
+**
ns
ns
ns
ns
ns
ns
+*
+**
+**
+*
ns
ns
+**
ns
ns
ns
+*
ns
ns
+**
ns
+**
+*
ns
ns
ns
ns
ns
ns
ns
ns
ns
**
ns
**
ns
ns
**
+*
ns
ns
ns
ns
+**
ns
+*
ns
*
ns
*
ns
ns
+*
+**
+**
ns
ns
ns
+**
+*
ns
ns
+*
ns
ns
ns
ns
+**
a
The ‘‘+’’ and ‘‘’’ signs indicate the direction of the difference between two years. No test was performed for some species not recorded during
phase 2.
b
ns, Not significant.
* 0.05< P<0.01.
** P40.01.
124
J.-M. Paillisson et al. / Biological Conservation 106 (2002) 115–127
Table 3
Level of significance of the difference between the abundance of
breeding species nesting outside the wet grasslands but feeding in these
habitats (expressed in proportion of the breeding population) during
the 3 years and for the second phase of the water regime (Apr I–Jul II)
using Wilcoxon’s signed rank test
Comparison of mean numerical
proportion of breeding species (Phase 2)a
Podiceps cristatus
Phalacrocorax carbo
Bubulcus ibis
Egretta garzetta
Egretta alba
Ardea purpurea
Threskiornis aethiopicus
Platalea leucorodia
Ardea cinerea
1998–1999
1998–2000
1999–2000
**
**
ns
ns
ns
ns
ns
*
**
**
**
ns
ns
+**
ns
+**
+**
*
nsb
ns
ns
ns
+**
ns
+**
+**
ns
a
The ‘‘+’’ and ‘‘’’ signs indicate the direction of the difference
between two years.
b
ns, Not significant.
* 0.05< P<0.01.
** P40.01.
In January 1998 and 1999, ducks feeding on the hunted
wet grasslands represented only 0.21% (25) and 0.16%
(27) of the wintering population on the whole wetland,
against 10.56% (1941) in January 2000 when hunting
was prohibited (unpublished data). In February when
hunting occurred, there were only 136, 46 and 227 ducks
on the wet grasslands, respectively, in 1998, 1999 and
2000. The largest flocks were observed only and suddenly in March after the end of the hunting season
(1302, 2385 and 922 birds, respectively, in 1998, 1999
and 2000 in the first days of the month and then up to
13 736, 10 326 and 14 278 birds in the second half of
March), resulting from movements of wintering birds
from the other parts of the lake preserved from disturbance (Reserve Nature status). Dehorter and Tamisier (1997) reported similar results in the Camargue,
where ducks tended to exploit protected brackish habitats even though they are poorer in food resources than
the freshwater habitats which are subject to hunting.
The water regime (period, duration and amplitude)
induced various responses for numerous species (cf.
results summarized in Table 4). Fulica atra (dominating
in January and February) and ducks (dominating in
March and April) were less sensitive to water level fluctuations than Ciconiiformes and Charadriiformes. During the spring period the water regimes were very
contrasted, the mean water level being 30 cm higher
from April to mid-June in 1998 than in 2000 and 10 cm
higher than in 1999, with a maximum difference in May
II (38.5 cm for 1998/1999, 54 cm for 1998/2000 and 15.5
cm for 1999/2000). The overall impact of this rise in
water level on waterbirds was an increase in diving fisheating birds such as Podiceps cristatus and Phalacro-
Table 4
Synthesis of significant effects of changes in the management regime
(water level) from 1998 to 2000 on the use of the wet grasslands by
waterbirds during the phase 2 (April–July)a
Waterbird species
Late breeding species
Bubulcus ibis
Egretta garzetta*
Egretta alba**
Ardea purpurea**
Threskiornis aethiopicus
Platalea leucorodia**
Himantopus himantopus*
Tringa tetanus*
Chlidonias hybridus*
Effect of changes in the
water regime (1998–2000)b
+
+
+
+
+
+
+
+
+
Sedentary, migrant and precocious breeders
Podiceps cristatus
Phalacrocorax carbo
Ardea cinerea
Cygnus olor*
Anas platyrhynchos
Anas clypeata*
Aythya farina*
+
Fulica atra
+
Vanellus vanellus*
+
Larus ridibundus
Larus argentatus
a
Species of high (French list, see Rocamora and Yeatman-Berthelot, 1999; or European ‘Birds’ Directive) or very high (national and
European criteria) conservation value are mentioned by one or two
asterisks respectively, after the scientific name
b
The ‘‘+’’ and ‘‘’’ signs indicate the direction of the effect.
corax carbo and larger flocks of resting gulls. Conversely these conditions were adverse to numerous
ground-feeding waterbirds that require very shallow
waters. The pattern of use of flooding grasslands did not
always correspond to taxonomy but to ecological
responses of well-defined species assemblages. Morphological and behavioural adaptations like the tarsus
length for Ciconiiformes or Charadriiformes (DuBowy,
1996; Ntiamoa-Baidu et al., 1998) or the neck length for
dabbling ducks (Pöysä, 1983) and life history strategies
like the diet composition and the foraging behaviour for
instance for herons (Marion et al., 2000) are the likely
mechanisms explaining variations in the use of the wet
grasslands by birds according to suitability of feeding
habitats.
The increased attractiveness of the wet grasslands as
feeding habitats in 2000 for numerous Ciconiiformes is
all the more true since the population size of these
colonial species nesting in trees in the neighbouring
floating peat fen has increased between years, notably
for Egretta alba and Ardea cinerea (unpublished data).
These long-legged herons are known to be favoured by
high water levels in wetlands (Marion et al., 2000) and
J.-M. Paillisson et al. / Biological Conservation 106 (2002) 115–127
field observations indicated that particularly Egretta
alba was often present in deep waters (about 40 cm).
In the present study, Tringa totanus and Himantopus
himantopus were grouped with the summer migrant
breeding Ciconiiformes. At low water levels, wet grasslands provide suitable habitats (Sanders, 1999). These
two species and Vanellus vanellus nest in wet grasslands
at the Lac de Grand-Lieu contrary to the majority of
Charadriiformes recorded and they are more vulnerable
than migrant species to the water regime since extensive
spring flooding during the breeding season can delay or
prevent waders from breeding as it was recorded elsewhere (Self et al., 1994).
4.3. Recommendations for management regime of wet
grasslands for the waterbird community
Numerous studies have shown large changes in the
use of wetlands by bird populations according to severe
trends in water conditions, from total drought (Kushlan, 1986a; Catsadorakis et al., 1996; Sanders, 1999) to
major flooding such as 2–5 m at Kerkini reservoir (Pyrovetsi and Papastergiadou, 1992; Crivelli et al., 1995).
But when modest water level fluctuations occurred, the
presence and pattern of many species at a site becomes
less predictable (Elphick and Oring, 1998). The present
study shows that, in relation to the semi-natural functioning of the ecosystem, it is essential to use appropriate management strategies to ensure and perhaps to
enhance the value of the wet grassland system of the Lac
de Grand-Lieu as feeding habitat for waterbirds. Any
change in lake water regime needs to be monitored
carefully in view of the rapid response of many species
to the hydrological conditions.
The maintenance of a water regime close to that
recorded in 2000 seems more favourable to the species
of high conservation value (Table 4). A water level
around 50 cm during winter until April ensured suitable
conditions for large flocks of wintering and migrating
Anseriformes. During the following months, the
increased duration of a water level of less than 25 cm
provided feeding areas for long-legged Ciconiiformes
and also for short-legged waders. In this geographical
area, the maintain of grasslands flooded until June is
very important since numerous inland wet grasslands
are exposed and the attractiveness of the wet grasslands of the Lac de Grand-Lieu is likely increased. In
the same way, Fasola and Ruiz (1996 and literature
cited therein) have shown the importance of rice fields in
the Mediterranean Region as valuable replacements for
lost natural habitats for a variety of waterbirds because
of the long duration of flooding through winter and to a
lesser extent as breeding sites.
Finally the water regime applied in 2000 for the Lac
de Grand-Lieu favours early accessibility for livestock
which is essential in maintaining the diversity of habi-
125
tats in wet grasslands (e.g. Colwell and Dodd, 1995),
contrary to either high water levels as in 1998 or
unflooding grasslands from May in the past (Marion
and Marion, 1975).
Although the water conditions in 2000 resulted in
providing suitable areas for exploitation by the majority
of waterbirds, they did not meet the requirements of all
species, notably diving fish-eating species (Table 4). But
most of these species have less conservation value and
above all the wetland is composed of several complementary units and the permanently central flooded
area is the most favourable feeding area for these species.
The water regime is not the only factor influencing the
use of wetlands by waterbirds. The hunting activity, and
more generally all types of disturbance likely predominate. The hunting disturbance was specifically
studied in numerous studies (e.g. Bell and Fox, 1991;
Madsen and Fox, 1995) and a ‘reserve’ effect was often
demonstrated (e.g. Hockin et al., 1992). In the present
study, the impact of the hunting activity depleted the
use of the wet grasslands in January. The total implementation of the European ‘Birds’ and ‘Habitats’
Directives by means of notably the new French law
prohibiting hunting in February from 2001 will probably induce in the future important changes in the use of
wet grasslands by ducks.
This last example emphasizes the need to also define
management guidelines at large spatial scales including multi-wetland sites (Haig et al., 1998). Long-term
and multi-species monitoring of the use of the wet
grasslands of the Lac de Grand-Lieu might elucidate the
response of some waterbird species (essentially Charadriiformes) for which there might be a delay before
possible effect can be detected.
Acknowledgements
This study was supported by grants from the Life
Grand-Lieu Program (European Community, Ministère
de l’Environnement, Agence de l’Eau Loire-Bretagne,
Région Pays de la Loire, Département de Loire Atlantique), directed by L. Marion for the Société Nationale
de Protection de la Nature and the Centre National de
la Recherche Scientifique. We thank two anonymous
referees for comments on a previous draft.
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