Interannual variation in greater flamingo breeding success in relation to water levels
In most wetlands, fluctuations in water depth appear to influence breeding success of waterbirds (Ogden et al. 1980, Frederick and Collopy 1989, Bildstein et al. 1990, Hafner et al. 1994) by strongly affecting food availability. Reduced breeding, or even abstinence from breeding, and low reproductive success during periods of drought have been reported for a number of bird species and explained by the effect of fluctuating water levels on the birds’ food supply (Dusi and Dusi 1968, Ogden et al. 1980, Manry 1985; Kushlan 1986; Frederick and Collopy 1989, Bildstein et al. 1990, Johnson et al. 1991). However previous studies have only considered the relationships between water levels, the number of breeding pairs, and average nest productivity.
The number of chicks raised to fledging per nesting pair is an important parameter of the demography of colonial species. However, in most cases it is difficult to estimate (Erwin and Custer 1982, Nisbet et al. 1990). In addition, even when a reliable measure of fledging success can be obtained, this index may not be closely related to recruitment to the next generation. One way to improve the measurement of overall breeding performance is to consider variation in the body condition of fledglings simultaneously with productivity. Variation in the physical condition of nestlings and fledglings has been observed in various species of birds (Coulson and Porter 1985, Hochachka and Smith 1991, Magrath 1991, Ferrer 1992) and has been shown to have consequences in terms of natal dispersal (Ferrer 1992) and survival (Garnett 1981, Coulson and Porter 1985, Smith et al. 1989, Tinbergen and Boerlijst 1990, Hochachka and Smith 1991, Schmutz 1993, Williams et al. 1993).
An important issue, particularly in species that lay single-egg clutches and thus have no opportunity to trade off the number of offspring against offspring quality, is whether parents are able to buffer their offspring from environmental fluctuations. If this is the case, fledgling condition may not vary with environmental conditions. Alternatively, in poor years the average fledgling condition should be decreased, indicating that adults do not (or only partially) buffer offspring from environmental fluctuations. Although parents may work harder to provide sufficient resources to their offspring, the associated cost in terms of reduced survival may limit the ability of parents to maintain offspring quality under harsh conditions, especially in long-lived species (Pugesek and Diem 1990, Saether et al. 1993). Therefore it is important to produce estimates of both fledging success and fledgling body condition within demographic studies of colonial waterbirds.
In this paper, we examine variation among years in colony size, fledging success, and chick condition at fledging in the Greater Flamingo (Phoenicopterus ruber roseus) in relation to local hydrological conditions in the Camargue (southern France) to determine whether variation in water levels, through potential decrease in food availability and increased competition between foragers, affects the number of breeding pairs and their breeding success. We use data on water levels of the local hydrological network, the Vaccares system, to test this hypothesis. First, we analyze the variation in the number of breeding pairs in relation to the water levels in potential foraging sites at the time when breeding takes place over eight consecutive years (1984-1991). Second, we analyze the variation in colony productivity and in the body condition of young in relation to the extent of flooded area used by breeding flamingos for foraging around the colony. We also consider differences in recruitment between two cohorts as a potential consequence of variation in the average body condition at fledging in a given year.
Study area and species
Flamingos have bred intermittently in the saline lagoons of the Camargue for centuries (Gallet 1949, Johnson 1983). In every year since 1974, they have successfully bred on an artificial island constructed for them in the Etang du Fangassier, part of the large complex of commercial salt pans of Salin de Giraud [ILLUSTRATION FOR FIGURE 1 OMITTED]. Depending on years and colony size, birds may also nest on a nearby dike. Flamingos begin to visit the breeding site in March. The first eggs (one per clutch) are usually laid in April and the period of egg laying can last 30-74 d. Both sexes incubate (Johnson 1983, Cezilly 1993) and feed the chick. Incubation lasts 29 d. When they are about 3 wk old, the chicks form a creche (assemblage of chicks not yet independent) in the vicinity of the breeding island where they remain until fledging, 75-90 d after hatching.
Water levels and the Vaccares system
Two major foraging habitats are used by breeding flamingos in the Camargue [ILLUSTRATION FOR FIGURE 1 OMITTED], the commercial salines (a network of shallow lagoons and ponds varying in salinity from that of the sea through to salt-saturated brine) and a complex of brackish lagoons and temporarily flooded “sansouire” (low-lying steppe with sparse halophytic vegetation) in the south of the Vaccares system (Johnson 1983; G. Hirons, unpublished data). The salines cover a large area ([approximately equal to]12 000 ha) and provide both nesting and foraging habitat for the flamingos (Johnson 1983, Britton and Johnson 1987). Management of the salines by the salt industry results in the maintenance of fairly constant water levels. However during the study period a strike in 1989 delayed by 10 d the pumping of water, resulting in a late flooding that year of many lagoons, including the Etang du Fangassier.
The Vaccares system includes two major components: the Etang du Vaccares, a brackish lagoon of [approximately equal to]6400 ha, and the Etangs du Sud, a complex of interconnecting lagoons covering [approximately equal to]4500 ha [ILLUSTRATION FOR FIGURE 1 OMITTED]. There are several communications between the two components and water flows between the Etang du Vaccares and the Etangs du Sud. Wind is a major factor in the transport of water between the two components of the system. Studies of variation in salinity of the Vaccares system reveal that the transfer of water from the Etang du Vaccares to the Etangs du Sud can be active until the end of spring and during summer, preventing complete drying and excessive salinity in the latter (Heurteaux 1992). Flamingos exploit the sansouire as foraging habitat when flooded, which is when water levels are high in the Etangs du Sud, or after heavy rains. Following conclusions from Heurteaux (1992), we used data on water levels in the Etang de Malagroy, one of the major permanent lagoons in the Etangs du Sud, as an index of flooded surface in the Etangs du Sud and the flooded sansouire for the period 1984 to 1991. Water levels were obtained from an automatic recording system (Heurteaux 1992). Daily measurements of water levels (expressed as relative values to the general level in France) were transformed into monthly averages for the period March to July, for each year from 1984 to 1991. Significant correlations were observed between consecutive monthly estimates of water levels across years.
Census of the breeding population and assessment of productivity
We estimated the productivity of the colony from counts of the number of breeding pairs and of chicks in the creche just prior to fledging. The creche system of flamingos facilitates the determination of annual productivity since most of the predation on chicks takes place on the breeding island before a creche is formed (Salathe 1983). Chicks form a creche when they are about 3 wk of age and remain in it until they fledge. Each year the colony was photographed from a plane in May, when peak numbers were incubating nests (see Green and Hirons 1988 for the limits associated with this method). The creche was photographed in a similar way shortly before fledging when the chicks are no longer vulnerable to predation by herring gulls (Salathe 1983).
Ringing and body measurements
Since 1977, a sample of the creche (10-30% or 552-838 chicks) has been marked each year with engraved plastic rings that allow individual recognition in the field (Johnson 1983). Originally, the larger chicks were selected for ringing, but since 1984 chicks of all ages have been marked (Green et al. 1989). Body mass and tarsus length were recorded for each ringed individual. These measurements allow estimation of body condition of chicks prior to fledging. Only one marking operation is organized each year. As the duration of egg laying in the colony can vary between 30 and 74 d, depending primarily on weather conditions, inter-individual variation in tarsus length and mass is due partly to the difference in age between chicks.
Estimating average body condition of chicks
To relate annual variation in the body condition of chicks to annual variation in water levels, we used an index of the average body condition of chicks for each cohort between 1984 and 1991. As it was not possible to control for variation in age structure in the creche, we used the ratio of mass to tarsus length. The ratio used was the slope of a linear regression of chick mass on chick tarsus length.
For each year from 1984 to 1991, we first modeled mass (M) as a function of tarsus length (T) by the allometric equation:
M = a[T.sup.b]. (1)
The parameters a (intercept) and b (slope) were then estimated by linear regression based on logarithms:
log M = log a + b log T. (2)
The slope of regression 2 was used as a measure of the average body condition of chicks.
From 1984 to 1991, 4473 chicks were ringed and measured. The regression of mass on tarsus length after logarithmic transformation (log M = 1.524 log T – 0.375, [r.sup.2] = 0.689, N = 4473, P [less than] 0.001) provided a slightly better fit to the data than the direct linear regression of mass on tarsus length ([r.sup.2] = 0.663).
Observations of the adult size and behavior of marked birds in subsequent years allowed sex determination of a subsample (N = 317 birds) of the ringed population. Significant differences were found between males and females in tarsus length at ringing (females: mean [+ or -] 1 SD = 204 [+ or -] 25 mm, N = 124; males: 227 [+ or -] 28 mm, N = 193; one-way analysis of variance with unequal sample size, [F.sub.1, 313] = 55.353, P [less than] 0.001) and in the mean body mass (females: 2262 [+ or -] 478 g, N = 124; males: 2734 [+ or -] 593 g, N = 193; one-way analysis of variance with unequal sample size, [F.sub.1, 313] = 55.387, P [less than] 0.001). The regression of log(mass) on log(tarsus length) was significant for both sexes (males: [r.sup.2] = 0.714, n = 193; females: [r.sup.2] = 0.672, n = 124; P [less than] 0.001 in both cases). However, there was no significant difference between sexes in the slopes of the regression of mass on tarsus length (analysis of covariance: [F.sub.1, 313] = 0.243). Therefore we assumed that no variation linked with sex would affect the use of the slope of the regression as an estimator of the mean body condition for each year.
Recruitment into the breeding population
Observations from a tower situated 70 m from the colony allowed us to record breeding attempts by birds of known age. Access to reproduction is progressive in flamingos; no breeding attempt by a bird younger than 3 yr has ever been observed, and breeding by birds of 3 and 4 yr old is very rare (Johnson et al. 1993). In 1989, 1990, and 1991 we recorded several breeding attempts by birds hatched in 1984 or 1985 and thus aged 5 or 6 yr.
The analysis concentrates on the 1984-1991 period, in which both random samples of chicks were ringed and reliable estimates of water levels in the Vaccares system were available. From March 1984 to July 1991, the water levels in the Etang de Malagroy ranged from -19 cm (May 1990) to +29 cm (March 1986). During the same period, the annual breeding population of flamingos ranged from 8600 to 19926 pairs and the colony fledging success ranged between 12.6 and 69.6% of young fledged.
In 1987, a balloon drifted into the colony scaring birds and causing two-thirds of the colony to abandon. However, even after eliminating 1987 data, there was no significant relationship between the number of fledglings in the creche and the number of breeding pairs (r = 0.601, n = 7 yr, P = 0.150). There was a strong correlation among years between the numbers of breeding pairs and the water levels in the Vaccares system in March, when birds start visiting the breeding island ([ILLUSTRATION FOR FIGURE 2 OMITTED]; r = 0.894, n = 8 yr, P [less than] 0.001). However there was no correlation between the productivity of the colony and water levels in May (r = 0.624, n = 8 yr, P = 0.099) or June (r = 0.292, P = 0.483), the start of chick raising [ILLUSTRATION FOR FIGURE 3 OMITTED]. Excluding 1987 data did not result in significant correlations between colony fledging success and water levels in May (r = 0.632, n = 7 yr, P = 0.127) or June (r = 0.126, n = 7 yr, P = 0.435).
The regression of log(mass) and log(tarsus length) was significant for each year (Table 1). There were significant differences among years in the slopes of the regression of mass on tarsus length, irrespective of sex (analysis of covariance, [F.sub.7, 4457] = 11.698, P [less than] 0.001). These slopes, our estimate of fledgling condition, were significantly correlated with the mean monthly water level in the Etang de Malagroy for the March to July period ([ILLUSTRATION FOR FIGURE 4 OMITTED]; r = 0.918, P [less than] 0.001).
TABLE 1. Regression of log (mass) on log (tarsus length) for Greater
Flamingo fledglings, for each year from 1984 to 1991.
TABLE 2. Comparison of the proportion of birds recruited at age 5
and 6 yr between the two cohorts 1984 and 1985.
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