Rendón et al.  1
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Assessing sex-related chick provisioning in greater flamingo
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Phoenicopterus roseus parents using capture-recapture
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models
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Miguel A. Rendón* a, Araceli Garrido b, Manuel Rendón-Martos c, José M.
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Ramírez b and Juan A. Amat a
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a
Department of Wetland Ecology, Estación Biológica de Doñana (EBD-CSIC), calle
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Américo Vespucio s/n, 41092 Sevilla, Spain
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b
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Ambiente y Agua de Andalucía, Consejería de Agricultura, Pesca y Medio Ambiente,
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Junta de Andalucía, Parque Comercial Málaga Nostrum, Edificio Galia Center, calle
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Jaén 9-3ª, 29004 Málaga, Spain
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c
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Medio Ambiente, Junta de Andalucía, Apartado 1, 29520 Fuente de Piedra, Spain
Programa de Actuaciones de Aves Acuáticas en Andalucía, Agencia de Medio
Reserva Natural Laguna de Fuente de Piedra, Consejería de Agricultura, Pesca y
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*
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Corresponding author: ma_rendon@ebd.csic.es
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Word count: 8596
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Running head: Provisioning movements in greater flamingos
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Summary
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1.
In sexually dimorphic species, the parental effort of the smaller sex may be
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reduced due to competitive exclusion in the feeding areas by the larger sex,
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or physiological constraints. However, to determine gender effects on
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provisioning patterns other intrinsic and extrinsic factors affecting parental
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effort should be accounted for.
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2.
Greater flamingos (Phoenicopterus roseus) exhibit sexual size dimorphism.
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In Fuente de Piedra colony the lake dries out almost completely during the
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breeding season and both parents commute between breeding and foraging
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sites distant >130 km during the chick rearing period.
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3.
Applying multistate capture-recapture models to daily observations of
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marked parents, we determined the effects of sex, and their interactions with
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other intrinsic and extrinsic factors, on the probability of chick desertion and
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sojourn in the colony and feeding areas. Moreover, using stable isotopes in
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the secretions that parents produce to feed their chicks we evaluated sex-
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specific use of wetlands.
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4.
The probability of chick attendance (complementary to chick desertion) was
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>0.98. Chick desertion was independent of parental sex, but decreased with
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parental age. Females stayed in the feeding areas for shorter periods (mean:
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7.5 [95% CI: 9.4–6.0] days) than males (9.2 [11.8–7.3] days). Isotopic
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signatures of secretions did not show sex differences in δ13C, but males’
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secretions were enriched in δ15N, suggesting they fed on prey of higher
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trophic levels than females. Both parents spent approximately one day in the
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colony, but females prolonged their mean stay when the lake dried out.
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Females also allocated more time to foraging in the flooded areas remaining
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in the colony, likely because they were energetically more stressed than
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males.
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5.
The results indicate that sex-specific provisioning behaviour in greater
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flamingo is related to differential effects of both intrinsic and extrinsic
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factors. Males seem forage less efficiently than females, whereas females
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body condition seem to be lower after fed the chick. Our methodology may
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be extended to species that feed on distant food sources, and that do not visit
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their offspring daily, to elucidate patterns of chick provisioning behaviour.
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Key-words: Foraging ecology, multistate capture-recapture models, parental care,
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sexual size dimorphism, sexual segregation, stable isotopes, waterbirds.
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Rendón et al.  4
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Introduction
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Chick rearing entails high energetic expenditures (Drent & Daan 1980; Monaghan &
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Nager 1997). The time and energy that adults allocate to obtain resources for their
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offspring are limited by both adult and offspring requirements (Ydenberg et al. 1992).
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Therefore, studying provisioning patterns is important for the understanding of the
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factors that limit parental investment and variations in the life-history of species (Sæther
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1994).
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The frequency of parental provisioning is one of the most important factors affecting
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chick body condition (Gray et al. 2005). The patterns of provisioning may be affected
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by the interaction of both extrinsic (e.g. resources and time) and intrinsic (e.g. body
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condition, age) factors (Tinbergen & Verhulst 2000; Weimerskirch & Lys 2000;
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Zimmer et al. 2011). Adult sex, for instance, may restrict parental effort due to
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differences in foraging efficiency or dominance in dimorphic species (González-Solís et
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al. 2000; Lewis et al. 2005; but see Lewis et al. 2002), as well as physiological
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restrictions (e.g. nutrient limitation, Nisbet 1997) or sex differences in energy efficiency
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(Barbraud et al. 1999). In sexually dimorphic species, pair members may reduce sexual
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competition by using different environments (González-Solís et al. 2000; Quillfeldt et
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al. 2011) or feeding on different prey (Forero et al. 2002; Quillfeldt et al. 2011). These
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strategies may affect foraging patterns (Lewis et al. 2005), and consequently
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provisioning behaviour (Weimerskirch & Lys 2000; Kato et al. 2001). In addition, sex
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differences in parental investment at different breeding stages (egg production,
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incubation, etc.) together with other intrinsic (Nol & Smith 1987; McGraw et al. 2001)
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and extrinsic (Dawson & Bortolotti 2003; Hamer et al. 2005) conditioning factors may
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lead to male and female parents adopting different decisions.
Rendón et al.  5
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Besides parental sex, provisioning is influenced by age at breeding (Nol & Smith 1987;
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Forest & Gaston 1996; González-Solís et al. 2004), probably due to older individuals
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being more experienced/efficient in acquiring resources. Also, as chick requirements
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increase during growth, so should increase parental effort. In long-lived birds it has
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been shown both flexible (Weimerskirch et al. 1997a; Hamer et al. 2005) and fixed
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levels of parental effort to satisfy chicks’ requirements (Sæther et al. 1993; Navarro &
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González-Solís 2007). These two strategies may not be mutually exclusive, however, as
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adults may switch between them depending on food availability (Erikstad et al. 1998;
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Granadeiro et al. 1998; Weimerskirch et al. 2001).
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Here we investigate the effect of sex on offspring desertion and parental provisioning
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strategies in the greater flamingo Phoenicopterus roseus. The greater flamingo is a
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colonial nester, long-lived and sexually dimorphic bird (males are 20% larger than
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females), which lays a single egg that is incubated by both parents (Johnson & Cézilly
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2007). The chicks are fed with a secretion produced by their parents (Lang 1963;
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Ziswiler & Farner 1972). Once chicks are in crèches, the parents move to forage in
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wetlands distant up to 400 km from the breeding site, remaining several days foraging
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in them (Amat et al. 2005). Male greater flamingos exhibit a greater effort in nest
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defence prior to egg laying (Johnson & Cézilly 2007), as well as in incubation (Rendón-
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Martos et al. 2000), but females are more likely to desert the nest (Cézilly 1993).
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During incubation, nest attendance also depends on flooding around the colonies
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(Rendón-Martos 1996), and parental age (Johnson & Cézilly 2007; Schmaltz et al.
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2011). In the few days after hatching, parental care equalise between sexes (Rendón-
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Martos et al. 2000). However, both chick provisioning and the factors that control it
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have been little studied in flamingos. Previous studies have determined that chick
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survival do not depend on parental age (Johnson & Cézilly 2007; Schmaltz et al. 2011),
Rendón et al.  6
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but the effect of parental sex on provisioning patterns remains unknown. Furthermore,
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as colonial birds are central place foragers during breeding, their provisioning tactics are
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expected to vary with environmental conditions (Tremblay & Cherel 2005). This may
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be especially critical when foraging on spatially and/or temporally unpredictable
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resources, and the food sources are distant from the colony, as in the case of greater
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flamingos (Amat et al. 2005).
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We applied multistate capture-recapture models to resightings of individually marked
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adults attending a colony to analyse the effect of the interaction of adult sex with other
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intrinsic (laying date, parent age, chick age) and extrinsic (observation date) factors on
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chick provisioning. The analysis of resighting data from marked individuals by means
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of capture-recapture methods may be an alternative to the study of animal movements
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(Kendall & Nichols 2004). In particular, the use of multistate models with unobservable
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states (Kendall & Nichols 2002; Fujiwara & Caswell 2002; Schaub et al. 2004) allowed
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determining periodicities of reproductive events in species with temporal emigrations.
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Though these models have been mainly used to study interannual demographic patterns,
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multistate models have also been applied to document variations in reproductive effort
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within a breeding season (Schmaltz et al. 2011).
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A comprehensive analysis of parental investment takes body condition changes besides
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reproductive effort by the parents into account (Weimerskirch et al. 1997b; Granadeiro
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et al. 1998; Weimerskirch & Lys 2000). For this reason we also studied the effect of
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intrinsic and extrinsic factors on the foraging patterns of parents. In addition, we
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investigated whether male and female parents used different habitats and/or prey during
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chick provisioning, by analysing stable isotopes (δ13C and δ15N) in secretions of parents
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(i.e. chick food).
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Materials and methods
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STUDY SITES AND BREEDING PHENOLOGY
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The study was conducted at Fuente de Piedra lake (FP; 37º07’N, 4º46’W; Fig. 1), a
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seasonal wetland in which the size of breeding colonies of greater flamingos varies
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annually depending on rainfall (Rendón-Martos 1996). The main foraging areas (FA) of
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adults during chick provisioning are in the wetlands of Doñana National Park and
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nearby zones, mainly the seasonal marshes (Guadalquivir marshes, GM), and Veta la
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Palma fish-farm (VP) (Amat et al. 2005).
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Laying dates in 2001 spanned from late February until mid-May, and colony size was
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17700 nests. There were three waves of breeders (cohorts: c) (Fig. 2A): 9th (fourth week
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of February) to 11th weeks (c1), 13th-15th weeks (c2) and 17th-19th weeks (c3). The
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number of flamingos in GM increased in line with chick hatching in FP, whereas in VP
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remained more or less stable. However, as GM dried out, there was a greater use of VP,
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which coincided with the maximum number of chicks at FP (Fig. 2B).
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OBSERVATIONS OF BREEDING ADULTS AND CHICKS
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Since 1977 in Camargue (France), and since 1986 in Fuente de Piedra, about 10% of
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greater flamingo chicks have been ringed using individually-coded leg-rings (Johnson
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& Cézilly 2007). The breeding behaviour of marked adults was recorded using a
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spotting scope located 250 m from the breeding colony. The sex of adults was
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determined based on their relative size and sex-specific behaviour from multiple
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observations. This sexing procedure was very accurate, as 96% of adults for which sex
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was determined using molecular methods were correctly classified when sex was
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assigned using phenotypic and behavioural characteristics (Appendix S1). The age of
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adults (Aa) was known, as they were individually marked as chicks. To investigate
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whether seasonal trends in joining the colony by breeding adults were predicted by their
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age (c), we used a linear model that included the interaction with the sex of adults
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(c*sex).
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When a parent was attending a chick, the age of the latter was allocated as a function of
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both its size relative to the adult, and the development of its plumage. When a parent
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was only recorded incubating, we assumed that it was in mid-incubation (incubation
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lasts 28-30 days; Johnson & Cézilly 2007). Thus, we estimated for each parent both
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laying and hatching dates. Laying dates were grouped according to each one of the three
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cohorts (c1, c2 and c3; see above). Chick age was estimated based on four categories
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(ac4), depending on their ability to forage by themselves and to fly (Allen 1956; Zweers
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et al. 1995): chicks that (1) cannot fly and are provisioned by their parents (1-6 weeks),
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(2) may forage by themselves but cannot fly (7-12 weeks), (3) may perform short flights
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and forage by themselves (13-16 weeks), and (4) are able to fly and forage by
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themselves (>16 weeks)
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PRESENCE OF ADULTS IN THE BREEDING COLONY
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After hatching, the presence of individually marked adults in FP was recorded daily
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during two periods (p): p1, 30 May–23 June (25 days), and p2, 25 July–19 August (26
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days). Observations were carried out from 08:00 h to 12:00 and from 18:00 h to 21:00 h
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(GMT+2h), and average time of observation was 4.3 ± (SD) 1.8 hours/day, though
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resighting effort (E) varied between days (range 2-8 h). We chose these two time-
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periods in order to avoid the hottest hours, when individuals were resting far from the
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lake shore (Rendón-Martos 1996). We carried out observations at the mouth of a stream
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at which the adults congregate during diurnal hours (Fig. 1). A total of 1934
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individually marked greater flamingos were identified, of which 367 (188 males and
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179 females) were selected because they were recorded incubating or attending chicks.
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PROBABILITIES OF CHICK DESERTION AND COMMUTING
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The analysis of the probability of chick desertion and commuting between FP and FA
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was considered as a case of temporary emigration, for which we used multistate
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capture-recapture models with unobservable states (Fujiwara & Caswell 2002; Schaub
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et al. 2004). Multistate capture-recapture models include three kinds of parameters:
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recapture probability Pt, survival rate St, and conditional transition probability ψt
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(Nichols et al.1994). When emigration processes dominate on mortality, St may be
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interpreted as probability of leaving the study area (Pradel et al. 1997). Survival
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probability in greater flamingos is >0.9 (Cézilly et al. 1996; Tavecchia et al. 2001), 97%
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of the individuals in this study were re-sighted in subsequent years after the study,
Rendón et al.  10
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therefore, St was considered as the probability of chick attendance, which is
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complementary to the probability of desertion.
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From the transition matrices both the probability of an individual commuting from FP to
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FA (ψtFPFA) and its probability of returning from FA to FP (ψtFAFP) were calculated
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(see Appendix S2 for model description). For an equally spaced discrete-time Markov
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chain, the mean residence or sojourn time ( ti ) for the chain in a state i is the length of
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time it stays there during a single visit (Guttorp 1995). As the expected sojourn time in
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stage i is geometrically distributed with parameter 1-ψi→i (probability of leaving the
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estate), we transformed transition probabilities in sojourn time for FP and FA, using the
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expressions tFP =1/(1-ψFP→FP) and tFA =1/(1-ψFA→FA), respectively.
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In order to estimate parameters values recapture probabilities for FA were fixed to 0,
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and survival probabilities were constrained to be the same for FP and FA (Kendall &
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Nichols 2002). Thus, the starting model considered the additive effects of sex, p and E
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on the probability of recapture at FP (Psex+p+E), the effect of the interaction of sex with
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ac4, Aa, c and p on the probability of residence (Ssex*(ac4+Aa+c+p)), and the effect of the
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interaction of sex with age of chick (excluding the category >16 weeks old: ac3), Aa, c
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and p on the probability of commuting between FP and FA (ψFPFAsex*(ac3+Aa+c+p)) and
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vice versa (ψFAFPsex*(ac3+Aa+c+p)). Given the chicks >16 weeks old are no longer fed by
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their parents (Rendón-Martos et al. 2000), its effect on commuting probability was not
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included in the models. Capture-recapture models were analysed using MARK (White
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& Burnham 1999).
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Because no formal test exists to check the goodness-of-fit (GOF) in multistate models
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with unobservable states, the data were fitted to a Cormack–Jolly–Seber model
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St*sexPt*sex (Lebreton et al. 1992). Selection of more parsimonious models was done
Rendón et al.  11
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using Akaike’s information criterium corrected for finite sample size (AICc). When the
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difference in AICc values among several models was <2, the model with the lowest
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number of significant parameters was retained as the final model. In Results only a
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selection of models are shown. All generated models are presented in Table S1.
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FORAGING BEHAVIOUR
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Abdominal profile index (API), a semi-quantitative index of abdominal roundness, was
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used as a surrogate of the time that adults allocated to forage. In the greater flamingo
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there are considerable variations in the abdominal roundness, not only related to body
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fat stores, but also to the time devoted to drinking and feeding. APIs were estimated
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based on six categories (Fig. 5 in Rendón et al. 2009). APIs of individually marked
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individuals (654 observations from 286 individuals) were recorded both at FP and VP at
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the same time period the continuous observations were carried out at FP colony. Using
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mixed ordinal logistic models API was related to the interaction of sex with ac3, Aa, p
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and locality of observation (l) as fixed factors (sex*[ac3+Aa+p+l]), and bird identity and
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observer as random factors. Analyses were conducted with R package ordinal2
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(Christensen 2010). Generated models are presented in Table S2.
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STABLE ISOTOPES IN SECRETIONS
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In 2006 and 2007, parental secretions were collected from chicks ringed at FP (n=100
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and n=118 chicks, respectively). By softly massaging the crops, the chicks were induced
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to regurgitate their content (i.e. the secreted food by its parent). Samples were then kept
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in vials at 4ºC during transportation and until analysis. Blood samples (1 ml) from a
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tarsal vein were taken and stored in 70% ethanol for sex determination of chicks. Cells
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extracted from crop content were used for molecular sex determination. As these cells
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may originate either from the parent that fed the chick or from the chick itself, parental
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sex was assigned only when molecular sexing based on secretion cells were different
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from chick sex based on blood sample. This resulted in unambiguous sex identification
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of 37 (25 and 12) female and 29 (6 and 23) male parents (in 2006 and 2007,
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respectively).
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The analysis of stable isotopes of the feeding secretions was conducted at the Iso-
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Analytical Ltd. Laboratory (Sercon Ltd., Crewe, U.K.), using mass spectrometry to
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obtain isotope ratios for carbon (13C/12C) and nitrogen (15N/14N), both relative to
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reference material, and expressed in delta notation (δ13C and δ15N) as
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δX(‰)=[(Rsample/Rreference)-1]*1000, where X is the heavier isotope and R is the isotopic
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proportion (13C/12C, 15N/14N) in the sample or reference material.
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Variations between individuals in δ13C and δ15N values were related to parental sex and
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tarsus length of chicks, indicative of chick age, using a mixed model in which year was
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included as random factor, and parental sex, tarsus length of chicks and their interaction
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as fixed factors.
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Results
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EFFECT OF ADULT AGE ON LAYING DATE
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There was no significant effect of the interaction between sex and cohort on the mean
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age of breeders (F2, 415=0.219; P=0.803). Sex had no additive effect on parental age (F1,
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415=0.001;
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joined the colony earlier (c1) were older (14±[SE] 0.54 years, n=45) than those that
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joined later (c2: 12.2±0.23 years, n=242 and c3: 11.3±0.29 years, n=149) (Tukey-
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Kramer test: P<0.05), but there was no difference in parental age between c2 and c3
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(P>0.05).
P=0.972) after controlling for cohort (F2, 415=37.9; P<0.001). Parents that
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MULTISTATE MODELS
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GOF tests
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The 3.SR component was not significant neither for males (229=19.7, P=0.902) nor
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females (231=7.5, P=1). The 2.CT component was not significant for males (246=22.0,
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P=0.999), but it was significant for females (248=72.0, P=0.014) because the
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observation of females in FP was more likely when they were recorded the previous day
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(trap dependence: Z=-1.98, P=0.048). The variance factor was ĉ=0.87, indicating minor
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underdispersion, and therefore a value of ĉ=1 was applied (Burnham & Anderson
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2002).
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Probability of recapture
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The best model of recapture probability included resighting effort (Table 1: M07). The
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model that also included the additive effect of observation period (Table 1: M04) had
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slightly higher relative AIC values (ΔAICc=0.5), however, the 95% CI of p included the
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0 value (βp1=-1.272; [SE: 1.142; 95% CI: -3.511 – 0.966]). Model M07 indicates that the
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probability of recapture increased with resighting effort (βE=0.444; [0.151; 0.148 –
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0.741]) from 0.53 (0.36 – 0.70) to 0.90 (0.63 – 0.99) in the range between 2 and 8 hours
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of observation.
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Probability of chick attendance
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The lowest AICc value was due to the additive effect of chick and parental age on the
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probability of chick attendance (Table 2: M17). Models M13 and M16 had ΔAICc=1.8.
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Nevertheless, the 95% CI of the coefficients of interactions between sex and both
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parental age and observation period in model M13 included the 0 value (-0.838 − 0.086
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and -0.088 − 2.486, respectively), as well as observation period coefficient in model
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M16 (-0.531 − 0.321). Therefore, we selected model M17 as the best model. Probability
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of chick attendance was very high for parents attending chicks <16 weeks old (weeks 1-
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6: 0.993 [95% CI: 0.990 − 0.995]; 7-12 weeks: 0.981 [0.972 – 0.987]; 13–16 weeks:
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0.982 [0.966 – 0.991]), and decreased for chicks >16 weeks old (0.794 [0.643 – 0.892])
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(Fig. 3A). In addition, older parents were less prone to desert from chick care than
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younger parents (Fig. 3B; βAa=0.197 [SE: 0.101]).
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Commuting between the colony and foraging areas
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The model estimating the probability of commuting from FP to FA with the lowest
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AICc value (Table 3: M27) included the interaction of sex with observation period and
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the additive effect of parental age. The AICc value of the model M25, that in addition
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considers the interaction between parental sex and age, differs by 1.5 with respect to
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model M27, but the interaction term was not significant (βsex*Aa=0.215; [SE: 0.278];
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[95% CI: -0.760 – 0.331]). Given than the probabilities of transition of males and
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females in model M27 were rather similar in period p1 (0.958; [0.927 – 0.977] and
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0.955; [0.923 – 0.974], respectively), we tested whether there were no significant
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intersex differences in such transition for p1. The new model (M33) provided a better fit
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to data (AICc=6348.5), and the probability of commuting from FP to FA during p1 was
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0.956 (0.934 – 0.971), corresponding to mean sojourn time in FP of 1.1 (1.01 – 1.00)
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days (Fig. 4A). During p2 the probability of parents moving from FP to FA was lower,
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(Fig. 4A), and it was lower for females (0.675; [0.569 – 0.765]) than for males (0.885;
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[0.814 – 0.948]), corresponding to mean sojourn time in FP of 1.5 (1.8 – 1.3) days for
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females and 1.1 (1.2 – 1.1) days for males (Fig. 4B). Independently of the observation
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period, older parents spent less time than younger parents in FP between consecutive
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visits to FA (βAa=0.322; [SE: 0.134]).
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The probability of remaining in FA is best explained by a model including parental sex
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as the only explanatory variable (Table 3: M44). A model that also included the additive
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effect of the observation period (M43) had ΔAICc<2 compared to model M44, but the
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coefficient of observation period term was not significant (95% CI: -0.139 – 0.331).
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Daily probability of parents in FA moving to FP was greater in females (0.134 [95% CI:
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0.106 – 0.168]) than in males (0.109 [0.085 – 0.765]), which implied a mean sojourn
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time of 7.5 (9.4 – 6.0) and 9.2 (11.8 – 7.3) days in FA for females and males (Fig. 4C),
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respectively.
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FORAGING BEHAVIOUR OF ADULTS
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Four models relating API values in FP and VP (Table S2: Mvii, Mx, Mxii y Mxiii) had
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ΔAIC values <2, all being submodels of Mvii (sex*[Aa+l]+p). The interaction between
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parental sex and age for this last model was not significant (z=1.577; P=0.115), neither
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the additive effects of parental age (z=-0.310; P=0.757) and observation period
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(z=1.033; P=0.302), so that model Mviii including the interaction between parental sex
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and locality of observation (βsex[males]*l[VP]=1.032 [SE: 0.432]; P=0.017) was selected.
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During the stay in FP (Fig. 5) males had lower API (API2: 67%) than females (API3:
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54%), suggesting that females spent probably more time foraging in the colony. When
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males and females were in VP, there were no sex differences in API, and both sexes
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exhibited greater APIs than when they were in FP (API4: 63% and 64%, for males and
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females, respectively), likely because both sexes spent similar time foraging and spent
384
more time foraging in VP than in FP.
385
386
387
STABLE ISOTOPES IN SECRETIONS
388
389
There were no significant effects of the interaction of parental sex*chick tarsus length
390
(F1, 58.06=1.11; P=0.297), chick tarsus length (F1, 58.32=0.686; P=0.411), or parental sex
391
(F1, 35.34=0.06; P=0.804) on δ13C values. δ15N was related neither to the interaction of
392
adult sex*chick tarsus length (F1, 59=0.75; P=0.391), nor to chick tarsus length (F1,
393
59=0.04;
394
(15.11±SE: 0.54‰) than secretions of female parents (13.22±0.5‰; F1, 59=5.11;
395
P=0.028).
396
397
398
399
400
401
402
403
404
P=0.844) although secretions of male parents had higher levels of δ15N
Rendón et al.  18
405
Discussion
406
407
Our results show that both intrinsic (sex, parental age, and chick age), and extrinsic
408
factors (observation date) affected chick provisioning effort by parents. In contrast to
409
most breeding colonies of greater flamingos in Europe, the Fuente de Piedra colony is
410
located in a temporal natural wetland that usually dries out in early summer, and
411
therefore breeding adults have to move to other wetlands for foraging. These conditions
412
must be similar to those faced by the greater flamingo in other natural wetlands, and
413
thus our study may be representative of the environmental conditions that have shaped
414
the provisioning strategies in the species.
415
416
417
CHICK ATTENDANCE BY PARENTS
418
419
Both incubation and chick rearing require considerable energy expenditure by parents
420
(Monaghan & Nager 1997). In the greater flamingo the main limiting of breeding
421
success is desertion during incubation (Rendón-Martos 1996). Indeed, Schmaltz et al.
422
(2011) showed that incubation acts as a bottleneck in the greater flamingo, eliminating
423
individuals of lower quality (i.e. younger breeders), while the remaining parents are
424
equally able to assume chick rearing. We have shown that the probability of chick
425
attendance is very high during chick provisioning (>0.98), suggesting that after chick
426
hatching, most parents could afford paying the costs of parental care. This is in line with
427
Johnson & Cézilly (2007) reporting that parental age does not affect chick survival.
Rendón et al.  19
428
Despite having demonstrated a significant effect of parental age on chick desertion,
429
such an effect is minimal while chicks are dependent on parental care (<16 weeks), and
430
increases when chicks are able to fly, with an average occurrence of >10% for the rank
431
of parental ages that we have analysed (Fig. 3B). This result suggests that the
432
prolongation of parental care depends mainly on parental age, and that only older
433
individuals are able of assuming such an effort during chick rearing. Similar patterns in
434
prolongation of parental care by older adults have been reported in gulls (Pugesek
435
1990). The prolongation of parental care before the chicks leave the natal colony likely
436
to have important consequences on their body condition that may affect survival (Nur
437
1984; Tinbergen & Boerlijst 1990), as well as their dispersal capabilities (Barbraud et
438
al. 2003). In years when parental age of the FP colony is highly structured (older
439
individuals start breeding earlier than younger ones), chick survival before fledging is
440
lower in younger chicks, and this may be partly due to chick desertion by younger
441
parents who initiate breeding later than older parents (M.A. Rendón et al., unpubl.).
442
We did not detect seasonal changes, neither on the probability of chick desertion, nor on
443
the frequency of chick provisioning, once the remaining explanatory factors were
444
controlled for. Differences in parental effort of individuals breeding in different dates
445
would have been due to environmental factors related to seasonal changes (e.g. food
446
availability) and/or differences in quality/experience of breeders.
447
Neither did we found a sex-related effect on the probability of chick desertion by
448
parents. The main factors that affect sexual conflict over parental care in birds depend
449
on chick precocity and on new mating opportunities of adults during the same breeding
450
season (Olson et al. 2008). Despite mate switching have been observed within the
451
breeding season (Cézilly & Johnson 1995), adults abandoning at chick stage may have
452
low chances to successfully complete a new breeding attempt. There is age-related
Rendón et al.  20
453
assortative mating in the greater flamingo (Cézilly et al. 1997), and this may further
454
limit the opportunities for a sexual conflict over chick care. It is unlikely that one parent
455
would increase its fitness by reducing its effort and thus inducing its mate to
456
compensate for loss (Pärt et al. 1992), given that the residual reproductive value of both
457
parents would be similar. Therefore, it is expected that chick desertion by one of the
458
parents may determine desertion by the other parent, determining a rather similar
459
investment in chick care by both pair members during the provisioning period.
460
461
462
PROVISIONING MOVEMENTS
463
464
Sojourn time in foraging areas
465
466
In general, in dimorphic species the smaller sex feeds in more distant sites and has a
467
lower foraging efficiency than the larger sex during chick provisioning, and as a
468
consequence the smaller sex exhibits a lower level of parental care (Wearmouth & Sims
469
2008, for a review on marine species). Contrary to this pattern, female greater flamingos
470
remained in FA shorter periods than males between consecutive visits to the colony (7.5
471
vs. 9.2 days). This would allow the females to feed the chicks more frequently than
472
males. Central place foraging theory predicts that the time that individuals spend in
473
foraging areas increases with the distance to foraging patches from the central site, or
474
when energy gain in the patch diminishes (Orians & Pearson 1979). Accordingly, we
475
would expect that females forage in wetlands closer to the colony, or exploit more
476
efficiently than males the trophic resources. Nevertheless, satellite tracking of some
Rendón et al.  21
477
individuals did not support this (Amat et al. 2005). Neither do δ13C values in secretions
478
indicate sexual differences in wetland use during chick provisioning. δ15N values in
479
male secretions, however, suggest that males feed on prey of higher trophic levels than
480
those of females (e.g. Bearhop et al. 2006).
481
Food availability may affect provisioning movements, as food searching time may vary
482
and this may determine variations in the quantity of food received by chicks
483
(Granadeiro et al. 1998; Weimerskirch et al. 2001). In southern Spain there is a dramatic
484
seasonal decrease in wetland availability from late spring due to the drying out of
485
temporal marshes in the Doñana area, so that the number of flamingos in permanent
486
wetlands increased threefold during our study. However, we did not find a relationship
487
between sojourn times in FA and observation period, suggesting that resource
488
availability did not directly affect foraging efficiency of parents during chick rearing.
489
490
491
Sojourn time in the colony
492
493
In contrast to the pattern of sojourn time in FA, the duration of stays by parents in FP
494
increased throughout the chick rearing period. However, this was affected by gender
495
differences: during p1 both members remained one day in FP, but during p2 females
496
remained longer (1.5 days) than males (1.1 days) in FP between consecutive visits to
497
FA. Given that females remained for shorter periods in FA than males, foraged on prey
498
of apparently lower quality, and both parents provisioning their chick with similar meal
499
sizes (M.A. Rendón et al. unpubl., but see Cézilly et al. 1994), the amount of parental
500
effort might have decreased female body condition more than male body condition
Rendón et al.  22
501
(with more expressed differences with advance of the season due to the cumulative
502
effort). These, in turn, might have resulted in females spending more time foraging than
503
males late in the chick provisioning period when visiting the breeding site.
504
Older parents remained for shorter periods in FP between consecutive visits to FA than
505
younger ones. This pattern could mean that older parent spent less time to regain body
506
condition before returning to FA. Due to higher residual reproductive value, young
507
parents should invest less in chick rearing than older ones if investment in reproduction
508
affects survival. However, female flamingos <7 years old breeding for the first time
509
have lower survival than those breeding later, although this pattern is not found in males
510
(Tavecchia et al. 2001). Alternatively, as older individuals could be more
511
experienced/efficient in acquiring food resources (Bildstein et al. 1991), sojourn time in
512
FP would decrease with parental age because older parent spend less time to restore
513
their body condition before leaving the colony.
514
515
516
IS THERE REGULATION OF CHICK PROVISIONING?
517
518
Chick age did not affect commuting behaviour by parents, at least for the range of chick
519
ages that we studied. This indicates that parents may not vary their effort in response to
520
chick requirements. However, there are other aspects of parental effort besides
521
frequency of visits to the colony, for instance, food quantity/quality (Weimerskirch et
522
al. 1997b; Weimerskirch & Lys 2000). Parent males of greater flamingos vary the
523
duration of their feedings according to chick age (Cézilly et al. 1994). On the other
524
hand, the number of feedings received daily by chicks also varies with chick age
Rendón et al.  23
525
(Rendón et al. 2012). Therefore, additional studies are necessary to determine whether
526
parental effort is fixed or varies according to chick needs.
527
528
529
SEX-RELATED PROVISIONING PATTERNS
530
531
Sex-related differences in commuting patterns suggest that females make a greater
532
parental investment than males during chick rearing. Commuting periods are shorter for
533
females than males, in spite of females being smaller and foraging on prey of apparently
534
lower quality than males. An explanation to the greater effort of females in chick
535
provisioning may be due to different gender allocation of effort in different phases of a
536
reproductive attempt. Thus, the cumulative effects of such effort would affect the body
537
condition of individuals investing more in previous phases, and this would affect
538
parental care decisions in latter phases (Heaney & Monaghan 1996). However, despite
539
male's greater effort in the first phases of breeding, it is more likely that females desert
540
the nest, and, therefore, males should invest less than females in incubation (Cézilly
541
1993).
542
In the present study a significant variation in isotopic signatures between sexes has been
543
shown. The higher δ15N values in male's secretions suggest segregation between sexes
544
by their selection for different prey size/type (e.g. Forero et al. 2002; Bearhop et al
545
2006). Sex difference in provisioning patterns is probably not due to competitive
546
exclusion from feeding areas, because according to this hypothesis we would expect
547
longer permanency of females in FA to compensate for their lower foraging efficiency.
548
Alternatively, sojourn time at FA could be consequence of size-mediated differences in
Rendón et al.  24
549
sex-specific foraging behaviour and microhabitat use. Sex differences in bill size
550
(Cramp & Simmons 1977) would determine males filtering larger prey items than
551
females because of their larger bill, and thus secretions had higher δ15N values. On the
552
other hand, sexual dimorphism can promote sex-specific niche segregation by
553
exploiting different feeding microhabitats, reducing intersexual-competition. Using
554
satellite telemetry, J.A. Amat et al. (unpubl.) found that females foraged in shallow
555
water near the shore of wetlands, whereas males were spread over the wetlands using
556
deeper, open waters. This spatial segregation between sexes must determine differences
557
in both foraging behaviour (e.g. stamp-feeding vs. walk-feeding, Johnson & Cézilly
558
2007) and prey selection. Varo et al. (2011) found that brine shrimp (Artemia
559
parthenogenetica), a potential prey for greater flamingo, are larger and occur at higher
560
density at the bottom of the water column. Therefore, if males exploit larger but more
561
dispersed prey than females, which are restricted to shallower water where exploit more
562
benthonic preys (e.g. Chironomus larvae), optimum foraging duration at FA could be
563
longer for males because more time is needed to maximise energy gained per unit time
564
(Stephen & Krebs 1986).
565
566
567
Conclusions
568
569
By analysing resightings of individually marked flamingos we were able to study
570
commuting patterns during chick rearing. Our study provides further empirical evidence
571
that capture-recapture models can be successfully applied to estimate probabilities of
572
desertion and commuting when parents do not visit their chicks daily and the marking
Rendón et al.  25
573
of adults to track their movements (e.g. telemetry) is difficult. Our results indicate that
574
sex differences in provisioning behaviour in the greater flamingo may arise due to both
575
gender-specific foraging behaviour and energy constraints. In foraging areas, males
576
seem to be less efficient than females in replenish body reserves. However, when
577
parents return to fed the chick, females must restoring their body condition staying
578
longer time periods than males in the colony, before returning to adult foraging areas.
579
580
581
Acknowledgements
582
583
The Consejería de Medio Ambiente of Junta de Andalucía authorised our study and
584
provided many facilities. We thank Juan Rubio for assistance during field work.
585
Pesquerías Isla Mayor S.A. granted access to Veta la Palma fish-farm. Logistical
586
support was provided by Laboratorio de Ecología Molecular, Estación Biológica de
587
Doñana, CSIC (LEM-EBD), where sexing of cells extracted from crop content was
588
performed by Mónica Gutiérrez. Sex determination of chicks was carried out at the
589
laboratory of Centro de Análisis y Diagnóstico de la Fauna Silvestre, Consejería de
590
Medio Ambiente, Junta de Andalucía. Data on counts of greater flamingos and water
591
levels in the National Park of Doñana were provided by Equipo de Seguimiento de
592
Procesos Naturales-EBD. The authors would like to thank the anonymous referees for
593
their valuable comments. We were supported by research grants BOS2002-04695 and
594
CGL2005-01136BOS from Ministerio de Educación y Ciencia of Spain, both with EU-
595
ERDF support.
596
Rendón et al.  26
597
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796
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800
801
Rendón et al.  35
802
Supporting Information
803
The following Supporting Information is available for this article online.
804
Appendix S1. Phenotypic sexing of adult greater flamingos.
805
Appendix S2. Description of the multistate capture-recapture models.
806
Table S1. Results of the model fitting for the selection of the more parsimonious model
807
for probabilities of residence and movement between the breeding site and foraging
808
areas.
809
Table S2. Results of the mixed-effects ordinal logistic models predicting abdominal
810
profile index values in adults grater flamingos.
811
812
Rendón et al.  36
813
FIGURE LEGENDS
814
815
Figure 1. Location of the study area at Fuente de Piedra lake, and the two main feeding
816
areas for breeding flamingos during the chick-rearing period in Doñana National Park.
817
818
Figure 2. (A) Weekly variation (week 1 is the first week of January) of the numbers of
819
adult flamingos at the colony and dispersed along the lake, and water depth at FP in
820
2001. Three waves of breeding (c) were recorded in 2001. Daily resightings of marked
821
adults were conducted in two periods (p). (B) Monthly variation of greater flamingos in
822
GM and VP in 2001. Water depth in the GM is also shown.
823
824
Figure 3. Chick (A) and parent (B) age effects on the mean (±95% CI) daily probability
825
of chick attendance by parents (S) in FP according to the M17-model (table 2). For
826
chick age effect, only the predicted values for categories 7-12 and >16 weeks old are
827
shown.
828
829
Figure 4. Mean daily probabilities (±95% CI) of movements by parent greater flamingos
830
(ψ) form FP to FA and vice versa, predicted by M44-model (table 3). The right axis
831
indicates the mean sojourn time in FP and FA. (A) Observation period and sex effects
832
on movement probabilities from FP to FA. (B) Effects of parental age and (C) sex on
833
the probability of movements are also shown for foraging displacements from FA to FP.
834
835
Figure 5. Predicted probabilities for API categories in greater flamingos relative to sex
836
(males: black bars; females: white bars) and locality of observation (FP: upper graph;
837
VP: lower graph), resulting from the ordinal logistic model: sex*l.
838
Rendón et al.  37
839
840
FIGURE 1
841
842
Doñana
National Park
Fuente de
Piedra Lake
0
100 km
Guadalquivir
Marshes
Breeding
Colony
Surveyed
Area
Veta la Palma
0
843
844
10 km
0
1 km
Rendón et al.  38
845
846
FIGURE 2
847
848
p1
A
p2
16000
14000
0.5
12000
0.4
10000
8000
0.3
c2
6000
c3
4000
0.2
Depth (m)
Nº of individuals
Adults dispersed
Adults at colony
Chicks
Breeding waves
Depth
0.6
c1
0.1
2000
0
0
0.0
8
B
10
12
14
16
18
20
22
24
28
30
32
34
36
25000
1.0
GM
VP
Depth
0.9
0.8
0.7
15000
0.6
0.5
10000
0.4
0.3
0.2
5000
0.1
0.0
0
8
849
850
851
852
10
12
14
16
18
20
22
Weeks
24
28
30
32
34
36
Depth (m)
Nº of individuals
20000
Rendón et al.  39
853
854
855
856
857
858
859
FIGURE 3
Rendón et al.  40
860
861
862
863
FIGURE 4
Rendón et al.  41
864
865
FIGURE 5
866
0,7
0.7
0,6
0.6
0,5
0.5
0,4
0.4
0,3
0.3
Probability
0,2
0.2
0,1
0.1
0,0
0.0
1
1
2
2
3
3
4
4
5
5
1
1
2
2
3
3
4
4
5
5
0.7
0,7
0.6
0,6
0.5
0,5
0.4
0,4
0.3
0,3
0.2
0,2
0.1
0,1
0.0
0,0
867
868
869
API
Rendón et al.  42
870
871
Table 1. Model selection for daily recapture probability for greater flamingos at FP
872
colny. AICc, ΔAICc, number of parameters (k), and deviance are shown. Variables in
873
uppercase letters are continuous. Most parsimonious model is highlighted in bold.
874
Model
M01: sex+p+E
M02: sex+p
M03: sex+E
M04: p+E
M05: sex
M06: p
M07: E
M08: .
875
876
877
878
879
880
881
AICc ΔAICc k Deviance
6371.2
2.3 52
6262.6
6403.6
34.7 51
6273.5
6371.0
2.1 51
6264.6
6369.4
0.5 51
6263.0
6374.5
5.6 50
6270.2
6375.6
6.7 50
6271.4
6368.9
0 50
6264.6
6373.5
4.6 49
6271.4
Abbreviations
sex: parental sex; p: resighting period (p1 and p2); E: resighting effort (hours); .:
constant; +: additive effect.
Rendón et al.  43
882
883
Table 2. Model selection for daily probability of chick attendance for greater flamingos
884
at FP colony. AICc, ΔAICc, number of parameters estimated (k), and deviance are
885
shown. Variables starting with uppercase letters are continuous. Most parsimonious
886
model is highlighted in bold.
887
M09:
M10:
M11:
M12:
M13:
M14:
M15:
M16:
M17:
M18
M19
M20:
888
889
890
891
892
893
894
Model
sex*(ac4+Aa+c+p)
sex*(Aa+c+p)+ac4
sex*(Aa+c+p)
sex*(Aa+p)+ac4+c
sex*(Aa+p)+ac4
sex*(p)+ac4+Aa
sex+ac4+Aa+p
ac4+Aa+p
ac4+Aa
ac4
Aa
.
AICc ΔAICc k Deviance
6368.9
10.5 50
6264.6
6363.6
5.2 47
6265.8
6370.5
12.1 44
6279.1
6363.4
5.0 45
6269.9
6360.2
1.8 43
6271.0
6360.7
2.3 42
6273.7
6362.1
3.8 41
6277.3
6360.2
1.8 40
6277.4
6358.4
0.0 39
6277.8
6361.4
3.0 38
6282.9
6375.9
17.5 36
6301.7
6378.7
20.3 35
6306.6
Abbreviations
sex: parental sex; ac4: chick age (1-6 weeks, 7-12 weeks, 13-16 weeks, and >16 weeks);
Aa: age of breeders (years); c: waves of breeding (c1, c2, and c3); p: resighting period
(p1 and p2); .: constant; +: additive effect; *: interaction among variables.
Rendón et al.  44
895
896
Table 3. Model selection for daily movements between FP and FA (ψ FP→FA and ψ
897
FA→FP
898
Variables starting with uppercase letters are continuous. Most parsimonious models are
899
highlighted in bold.
). AICc, ΔAICc, number of parameters estimated (k), and deviance are shown.
900
901
902
903
904
905
906
907
908
Transition
ψFP→FA
M21
M22
M23
M24
M25
M26
M27
M28
M29
M30
M31
M32
M33
Model
sex*(ac3+Aa+c+p)
sex*(Aa+c+p)+ac3
sex*(Aa+c+p)
sex*(Aa+p)+c
sex*(Aa+p)
sex*(Aa)+p
sex*(p)+Aa
sex*(p)
sex+p
sex
p
.
p1(.), p2(sex)+Aa
AICc ΔAICc k Desviación
6358.4
9.9 39
6277.8
6356.1
7.6 37
6279.8
6355.3
6.8 35
6283.2
6354.9
6.4 33
6287.0
6352.0
3.6 31
6288.4
6357.2
8.7 30
6295.7
6350.5
2.1 30
6289.0
6354.3
5.8 29
6294.9
6359.5
11.0 28
6302.1
6418.1
69.6 27
6362.9
6368.6
20.1 27
6313.4
6431.8
83.3 26
6378.6
6348.5
0.0 29
6289.0
ψFA→FP
sex*(ac3+Aa+c+p)
sex*(ac3+Aa+p)+c
sex*(ac3+Aa+p)
sex*(Aa+p)+ac3
sex*(Aa+p)
sex*(Aa)+p
sex*(p)+Aa
sex*(Aa)
sex*(p)
sex+p
sex
p
.
6348.5
6344.9
6342.7
6339.3
6340.3
6338.4
6338.4
6337.0
6336.8
6334.9
6333.5
6339.8
6338.1
M34
M35
M36
M37
M38
M39
M40
M41
M42
M43
M44
M45
M46
15.0
11.5
9.2
5.8
6.8
4.9
4.9
3.5
3.3
1.4
0.0
6.3
4.6
29
27
25
23
21
20
20
19
19
18
17
17
16
6289.0
6289.7
6291.6
6292.3
6297.5
6297.7
6297.7
6298.4
6298.2
6298.3
6299.0
6305.3
6305.6
The most parsimonious model for ψ was determined departing from the model:
FA
FAFP
Sap4, Aa PEFP ψ FP
sex*(ap3 Aac p) ψ sex*(ap3 Aac p) . In the first place we established the best model for the
FP→FA transition and, once determined, we selected the best model for the FP→FA
transition.
Abbreviations as in the table 3.