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Re-mating between and within breeding seasons in the Greater Flamingo

Phoenicopterus ruber roseus
FRANK CEZILLY & ALAN R. JOHNSON
Station Biologique de la Tour du Valat, Le Sambuc, 13200 Arles, France

Data on re-mating between and within breeding seasons were collected between 1983 and
1994 as part of a long-term study of the Greater Flamingo Phoenicopterus ruber roseus in
the Camargue, southern France. Flamingos have bred in the RhBne delta for centuries
and since 1972 have done so annually on an artificial island in the Etang du Fangassier.
A sample of chicks has been ringed each year since 1977; many of these birds were later
observed back at the breeding site and were used in this study. The mate-switching rate
between consecutivebreeding seasons was 98.3%. This result is contrary to what has been
reported from captive flocks where extensive mate fidelity occurred between consecutive
breeding seasons. Mate-switching also was observed in the Camargue within breeding
seasons, following breeding failure, and seems to be linked to male breeding strategy in
response to the need to synchronize hatching and the limited energy supply of breeding
females. The absence of a long-term pair bond in Greater Flamingos contrasts with current
views on the evolution of mate fidelity in relation to longevity in birds.

In species of birds that survive long enough to breed for
more than one season, or that are able to lay several clutches
within a season, a large part of mate choice is re-mating-
forming a pair for a second or subsequent reproductive effort
(Rowley 1983, Johnston & Ryder 1987). In many monoga-
mous species, some individuals tend to maintain a pair bond
over consecutive breeding attempts, within or between
breeding seasons and re-mating is not a random process.
Some monogamous species typically maintain long-lasting
pair bonds (Tickell 1968.Richdale& Warham 1973),where-
as others experience several different partners during their
reproductive career (Ens et al. 1993. Aebischer et al. 1995).
However, most studies of mate fidelity deal with long-lived
seabirds (Warham 1990). for which tenacity to nest site
tends to be stronger than to the partner (Warham 1990.
Pietz & Parmelee 1994). Thus in seabirds at least, the re-
lationship between long-lived species and mate fidelity may
be the result of the confounding effect of nest-site fidelity.
One way around this potential confounding effect would be
to study the mating patterns of long-lived birds which show
no or little nest-site fidelity. However, quantitative data on
mate fidelity in other groups of long-lived birds (e.g. cicon-
iiforms) either are scarce or come from studies of captive
populations (Studer-Tiersch 1975).
The Greater Flamingo Phoenicopterus ruber roseus breeds
in dense colonies and over a wide range of latitudes (Kahl
1975,A.R. Johnson,unpubl. thesis, Universie de Toulouse).
It is an ideal species to resolve the potential confounding
effect between mate fidelity and nest-site fidelity. It is a long-
lived species, having a 94% annual survival rate (Lebreton
543
et a/. 1992, F. Cezilly et a / . , unpublished data), and shows
no nest-mound fidelity from one breeding attempt to anoth-
er. Flamingos typically form breeding colonies in unstable
habitats which are subject to flooding and drying out (Berry
1972) and often are forced to move several hundred kilo-
metres to find suitable breeding sites. Females lay a single
egg, and both parents share incubation and chick provi-
sioning (Brown 1958, Cezilly 1993, CBzilly et nl. 1994). The
literature on the breeding biology of the Greater Flamingo
inthewildislimited(Brown1958,Rooth1965,CCzilly1993,
CCzilly et al. 1994.1995, A.R. Johnson,unpubl. thesis, Univ-
ersitk de Toulouse), and there is no available information
on the mating system of the family Phoenicopteridae based
on data from the wild. From studies on captive flocks, the
Greater Flamingo was described as monogamous, with pair
bonds extending over consecutive seasons (Studer-Tiersch
1975. Pickering 1992).
Here we report the results so far obtained from a 12-year
field study of the mating system of the Greater Flamingo.
We analyzed data on re-mating both between and within
breeding seasons and discuss the relevance of our results
for recent theories on the evolution of mate fidelity in birds.
STUDY POPULATION AND METHODS
Flamingos have bred intermittently in the saline lagoons of
the Camargue for centuries (A.R. Johnson. unpubl. DPhil
thesis, Universite de Toulouse). Since 1972, they have bred
544 F. C E Z I L L Y & A . R. J O H N S O N
annually on an artificial island constructed in the Etang du
Fangassier, part of the complex of commercial salt pans of
S a l i de Giraud. Breeding flamingos exploit two major for-
aging habitats: the commercial salinas and a complex of
brackish lagoons and temporarily flooded sansouire (low-
lying steppe with sparse halophytic vegetation).The salines
consist of a vast area (11,500 ha) where flamingos find both
nesting and foraging areas. Water levels are held constant
in the salines through management by the salt industry
(Britton & Johnson 1987).
Flamingos begin to return to the vicinity of the breeding
site in December and to visit the island in March. Pair for-
mation takes place during the early breeding season (late
December-May), and there is no evidence of pair-bond re-
tention outside of the breeding season. Between 1983 and
1994, the number of breeding pairs of Greater Flamingos at
the Fangassier colony vaned from 8600 to 19,900.Between-
year variation in the number of breeding birds at the Ca-
margue colony is closely related to the amount of flooded
habitat around the colonies (CCzilly et al. 1995). Due to lim-
itation of space on the breeding island, the Etang du Fan-
gassier is attended during the breeding season by many
‘hopeful’breeders that remain in the immediate vicinity of
the colony. The probability of access to a nest site on the
breeding island increases with age (F. CCzilly et al., unpubl.
data). The first eggs (oneklutch) are usually laid in April,
and the period of egg laying can last 30-74 days. When the
chicks are about 3 weeks old. they form a creche in the
vicinityof the breeding island, where they remain until fledg-
ing 75-90 days after hatching. Each year, from 1977 to date,
samples (518-850 individuals) of the flamingo chicks raised
in the Camargue at the Etang du Fangassierhave been ringed
with plastic leg rings engraved with an alphanumericalcode
(Johnson 1989b) which can be read in the field through a
telescope at distances up to 400 m (Johnson 1989a). In ad-
dition, some adults were ringed in the Camargue in 1985
following a cold spell. A similar ringing programmehas been
developed since 1986 at another colony situated at Fuente
de Piedra (southern Spain). Birds of Spanish origin are ob-
served regularly around the Camargue colony, and some
breed on the island. Data on re-matig between consecutive
breeding seasons were collected between 1983 and 1994. A
tower hide 70 m from the colony is used to keep the colony
under permanent observation. Pairs of ringed birds were
observed at or near the breeding site. In 1991, the breeding
season was characterized by heavy rains and strong winds,
leading to high frequencies of nest desertion, with second
and even third breeding attempts (CBzilly 1993). In 1992,
several nest desertions were also recorded. Those 2 years
allowed the collection of data on re-mating within the same
breeding season.
RESULTS
In view of the relatively small proportion of birds which are
ringed each year, the numbers of pairs of ringed birds form-
IBIS 137
Table 1. Numbers of individually known ringed male and female
Greater Flamingos attempting first, second and third breeding at-
tempts at the Camargue colony in 1991. The diflerence between the
two sexes in the frequency of re-nesting is explained by males chang-
ing mates between consecutive breeding attempts within the breeding
season and many females not relaying
Males Females
First breeding attempt 481 436
Sewnd breeding attempt 170 94
Third breeding attempt 12 1
ing each year are small. Nevertheless, from 1983 to 1993.
2-22 pairs of flamingosof which both partners were ringed
were observed each year at the Camargue colony. Out of
the total of 124 ringed pairs, both partners of 76 of these
were seen back at the Fangassier the following year. Out of
these 76 pairs. in 16 cases neither partner was seen to be
paired; in 40 cases (24 males and 16 females, binomial test,
P = 0.134. n.s.), one pair member was paired to a new
partner (while its former partner was present at the colony
site but was not observed mated or breeding): in 19 cases,
both partners are known to have acquired new mates. Only
in one instance did the two partners re-unite. Thus, the
overall rate of mate switching between seasons was 98.3%
(59 out of 60 cases). During the study period, the produc-
tivity (percentage of young fledgeabreedingpair) at the col-
ony ranged from 12.6% (1987) to 70% (1989 and 1991)
(GziUy et al. 1995). However, the subsequent changes of
mate could not be attributed to breeding failure since at least
18 birds that changed mates had bred successfullythe pre-
vious year.
Table 1 shows the distribution of records of first, second
and third clutches for ringed males and ringed females in
1991. There was no difference between the number of in-
dividuallyknown males and femalesengaged in a first breed-
ing attempt (chi-square goodness-of-fittest, x2] = 2.2, n.s.).
However, the proportions of individually known males and
femalesmaking a second breeding attempt after a first failure
were significantly different from what was expected based
on the observed proportions of individually known males
and females making a first attempt (x21= 15. P < 0.001).
The same was observedfor individuallyknown birds making
a third breeding attempt after two consecutive failures (xzl
= 8.3, P < 0.004).Thus males were significantly more likely
than females to attempt breeding for a second and third time
in the same year. Presumably several of our individually
known males, after breeding failure,took new females which
had not yet bred this year. Our data indicate that at least
29% of males mated with different partners between con-
secutive breeding attempts within a breeding season. The
same pattern was observed in 1992, although more ringed
males (n = 379)than ringed females (n = 256) were observed
making a first breeding attempt (xzl = 23.8, P < 0.001).
1995 RE-MATING I N FLAMINGOS
Among 52 second breeding attempts, 40 were by males h2,
= 6.4, P < 0.02). Thus the Greater Flamingo showed little
mate fidelity over successive breeding attempts whether
considered within or between breeding seasons.
DISCUSSION
In contrast to what has been reported for captive populations
(Studer-Tiersch 1975, Pickering 1992). the mating system
of the Greater Flamingo seems to correspond to seasonal
monogamy. Our results differ markedly from observations
reportingup to 94% mate fidelity in captive buds (F’ickering
1992). This contrast may result partly from the small num-
ber of birds breeding in captive flocks (about 30 pairs) com-
pared with the numbers occurring in the wild (several
thousands of pairs). It is also possible that captivity favours
atypical behaviour. Re-uniting of pairs in three penguin spe-
cies also has been found to be higher in captivity than in
the wild (Bowles et al. 1988). The present study provides
further evidenceof the need for caution when inferring avian
mating systems from captive populations.
The laying of a second clutch following the loss of the first
is common among colonial waterbirds and has been re-
corded previously for captive flamingos (Studer-Tiersch 1975.
Pickering 1992). Data on re-mating between consecutive
breeding attempts within the same breeding season contrast
with previous studies on other colonial waterbird species.
Cuthbert (1985) found that most pairs of Caspian Terns
Sterna caspia which failed to reproduce and initiateda second
nest did not change mates between consecutive breeding
attempts. Ashmole (1963)found no evidenceof mate change
after breeding failure in Sooty Terns Sternafuscata. The same
observation was reported in Little Penguins Eudyptula minor
(Reilly& Balmford 1975).However, previous results (Cezay
1993, CCzilly et al. 1994)have indicated that female flamin-
gos may be very limited in their energeticinvestment in any
year. Time from failure to relaying in Greater Flamingos in
the Camargue varies from 15 to 35 days (this study). Selec-
tion pressure on colonial nesting birds to relay rapidly is
strong because of the need to synchronize hatching in order
to reduce predation. Therefore, given the limited time ho-
rizon available to complete both incubation and the first
stage of chick raising, males, following breeding failure. may
gain an advantage by selecting a new mate from the pool of
available females rather than wait for their initial mate to
recover from energeticstress and be ready to lay again. Cost
of mate change would be minimal as there are large numbers
of hopeful females each year in the vicinity of the breeding
island, sti performing group displays in April or May. Mate
switching within the breeding season thus may correspond
to male reproductive tactics in relation to energetic con-
straints acting upon females and the limited time available
to lay a replacement clutch.
The adaptive significance of mate change (or divorce)has
been highly debated (Coulson 1966, Rowley 1983,Johnston
& Ryder 1987, Ens et al. 1993). Although longevity often is
545
assumed to be the main promoter of mate fidelity, there is
still a lack of agreement on why this is so (Rowley 1983.
Johnston & Ryder 1987, Ens et al. 1993). According to the
‘incompatibilityhypothesis’ (Coulson 1966). divorce is the
fate of incompatiblemates, whereas compatiblemates main-
tain long-lasting pair bonds. Data supporting the incompat-
ibility hypothesis come mainly from a few long-lived seabird
species in which divorce occurs essentially among young
individualsat the onset of their reproductivecareer and often
follows breeding failure (Coulson 1966, Brooke 1978, but
see Coulson & Thomas 1983). This hypothesis does not hold
for flamingos, for which the rate of mate change is inde-
pendent of age (birds as old as 16 years have been observed
changingmates between two consecutive breeding seasons).
According to the ‘better option hypothesis’ (Ens et al. 1993),
the probability of mate change depends highly on the avail-
ability of new mates. Adult mortality is an important factor
regulating the availability of mates. Indeed, Coulson and
Thomas (1985) and Ens et al. (1993) showed that divorce
rates in two species increased following years of high mor-
tality. Rowley (1983)also suggestedthat mate fidelity would
evolve mainly in long-lived species because they would gain
most from maintaining the pair bond and improving their
reproductive technique. This assertion is supported by the
extreme mate fidelity shown by some long-lived seabirds
(Warham 1990).However, a high survival rate is not a pre-
dictor of mate fidelity in the Greater Flamingo.
We suggestthat the mating systemof the Greater Flamingo
may have evolved in response to instability in breeding sites.
Other species of colonial waterbirds combine low mate fi-
delity with low site fidelity. K. S i p s o n (unpubl. MSc thesis,
University of British Columbia, Vancouver) found that all
birds changed mates between consecutive breeding seasons
in the Great Blue Heron Ardea herodias whilst site fidelity
was less than 10%.Low site and mate fidelity occur together
in the Flightless CormorantNannopterurn harrisi (Harris1979),
the Brandt’s Cormorant Phalacrocorax penicillatus (Boekel-
heide & Ainley 1989).the King Cormorant P. albiventer (Der-
enne et al. 1975)and the Shag P. nristotelis (Aebischeret al.
1995)and appear to be related to the instability of the breed-
ing habitat. Cuthbert (1985) found that habitat instability
was also a major determinant of mate change between con-
secutive seasons in the Caspian Tern. We suggest that the
current view on the relationshipbetween longevity and mate
fidelity may be incorrect, at least for colonial waterbirds,
and may result from a taxonomic bias in the study of mate
fidelity. Together with previous studies on ciconiiforms,the
present study suggests that breeding site fidelity may be the
major determinant of mate fidelity in a large number of bird
species. Comparative studies should be performed to assess
the exact influence of survival rate on mate fidelity when
the confounding effect of site fidelity is removed.
We thank the Tour du Valat flamingo team for assistance in the field
and the Compagnie des Salines du Midi et des Salines de 1’Est for
kindly allowing access to their property. Luc-Alain ‘Papa’Giraldeau
546 F . CEZILLY 8 A . R . J O H N S O N
and John Coulson provided helpful comments on an earlier version
of the manuscript.
REFERENCES
Aebischer, N.J.. Potts. G.R. & Coulson. J.C. 1995. Site and mate
fidelity of Shags Phalacrocorax aristotelis at two British colonies.
Ibis 137: 13-28.
Ashmole, N.P. 1963. The biology of the Widewake or Sooty Tern
Sterna juscata on Ascension Island. Ibis 103b 297-364.
Berry, H.H. 1972. Flamingo breeding on the Etosha Pan, South
West Africa. during 1971. Madoqua 5: 5-31.
Boekelheide. R.J. & Ainley, D.G. 1989. Age, resource availability,
and breeding effort in Brandt’s Cormorant. Auk 106: 3 8 9 4 0 1 .
Bowles, A.E., Ellis-Joseph. S.A. & Todd, F.S. 1988. Re-uniting in
three captive penguin species: Perspectives on the factors pro-
moting long-term pair bonds in the wild. Cormorant 16: 121-122.
Britton. R.H. & Johnson, A.R. 1987. An ecological account of a
Mediterranean salina: The SaIin de Giraud, Camargue (s. France).
Biol. Conserv. 42: 185-230.
Brooke. M.de L. 1978. Some factors affecting the laying date. in-
cubation and breeding success of the Manx Shearwater. Puffinus
puffinus. J. Anim. Ecol. 47: 477-495.
Brown, L.H. 1958. The breeding of the Greater Flamingo Phoen-
icopterus ruber at Lake Ehenteita. Kenya colony. Ibis 100: 388-
420.
CCzilly. F. 1993. Nest desertion in the Greater Flamingo, Phoeni-
copterus ruber roseus. Anim. Behav. 45: 1038-1040.
Gzilly. F.. Tourenq. C. & Johnson, A.R. 1994. Variationin parental
care with offspring age in the Greater Flamingo. Condor 96: 809-
812.
Ckzilly, F.. Boy. V.. Green, R., Hirons, G.H.M. & Johnson. A.R. 1995.
Inter-annual variation in Greater Flamingo breeding success in
relation to water levels. Ecology 7 6 2@26.
Coulson. J.C. 1966. The influence of the pair-bond and age on the
breeding biology of the Kittiwake G d Rissa tridactyln. J. Anim.
EcoI. 35: 269-279.
Coulson. J.C. & Thomas. C.S. 1983. Mate choice in the Kittiwake
Gull. Zn Bateson. P. fed.) Mate Choice: 361-376. Cambridge: Cam-
bridge University Press.
Coulson. J.C. & Thomas, C.S. 1985. Changes in the biology of the
Kittiwake Rissa tridactyla: A 31-year study of a breeding colony.
J. Anim. Ecol. 54: 9-26.
Cuthbert. F.J. 1985. Mate retention in Caspian Terns. Condor 87:
74-78.
Derenne. P., Mary. G. & Mougin. J.L. 1975. Le Cormoran a ventre
IBIS 1 3 7
blanc Phalacrocorax albiventer melanogenis (Blyth) de I’Archipel
Crozet. Com. Nat. Franc. Rech. Antarct. Publs. 40: 191-220.
Ens. B., Safriel. U.N. & Harris, M.P. 1993. Divorce in the long-
lived and monogamous Oystercatcher,Haematopus ostralegus: In-
compatibility of choosing the better option? Anim. Behav. 45:
1199-121 7.
Harris, M.P. 1979. Population dynamics of the Flightless Cor-
morant Nannopterum hamsi. Ibis 121: 135-146.
Johnson,A.R. 1989a. Movements of Greater Flamingos in the west-
ern Palearctic. Rev. Ecol. Terre Vie 44: 75-94.
Johnson.A.R. 1989b. Populationstudiesand conservation of Greater
Flamingos in the Camargue. In Spaans. A.L. (ed.) Wetlands en
Watervogels: 49-63. Wageningen: Pudoc.
Johnston, V.H. & Ryder, J.P. 1987. Divorce in larids: A review.
Colonial Waterbirds 1 0 16-26.
Kahl. M.P. 1975. Distribution and numbers: A summary. In Kear.
J. & Duplaix-Hall, N. (eds) Flamingos. Berkhamsted: Poyser.
Lebreton. J.-D.. Burnham, K.P.. Clobert. J. & Anderson, D.R. 1992.
Modeling survival and testing biological hypotheses using marked
animals: A unified approach with case studies. Ecol. Monogr. 62:
67-118.
Pickering, S.P.C. 1992. The comparative breeding biology of Ra-
rningos Phoenicopteridae at The Wildfowl and Wetlands Trust
Centre, Slimbridge. Int. Zoo Yearb. 31: 139-146.
Pietz. P.J. & Parmelee, D.F. 1994. Survival, site and mate fidelity
in South Polar Skuas Catharacta maccormicki at Anvers Island,
Antarctica. Ibis 1 3 6 32-38.
Redly. P.N. & Balmford. P. 1975. A breeding study of the Little
penguin Eudyptula minor in Australia. In Stonehouse,B. (ed.) The
Biology of Penguins: 161-187. London: MacMillan.
Richdale, L.E. & Warham, J. 1973. Survival, pair bond retention
and nest-site tenacity in Buller‘s Mollymawk. Ibis 115: 257-263.
Rooth, J. 1965. The Flamingos on Bonaire (Netherlands Antilles).
Habitat, diet and reproduction of Phoenicopterus ruber ruber. The
Hague: Martinus Nijhoff.
Rowley. I. 1983. Re-matig in buds. In Bateson. P. (ed.) Mate
Choice: 311-360. Cambridge: Cambridge University Press.
Studer-Tiersch. A. 1975. Basle Zoo.In Kear. J. & Duplaix-Hall, N.
(eds) Flamingos: 121-130. Berkhamsted Poyser.
Tickell. W.L.N. 1968. The biology of the Great Albatrosses, Di-
omedea exulans and Diomedea epomorphora. Antarct. Bird Stud. 12:
191-212.
Warham. J. 1990. The Petrels. Theirecology and breedingsystems.
London: Academic Press.
Submitted 16 November 1994; accepted 30 November 1994