Factors affecting the length of the post-fledging period ...

Factors affecting the length of the post-fledging period in the Bonelli’s Eagle Hieraaetus fasciatus Javier Balbontín* and Miguel Ferrer Balbontín J. & Ferrer M. 2005. Factors affecting the length of the postfledging period in the Bonelli’s Eagle Hieraaetus fasciatus. Ardea 93(2): ### – ###. We investigated factors associated with the length of the post-fledging dependence period in 28 radio-tagged young Bonelli’s Eagles Hieraaetus fasciatus monitored from 1998 to 2000. Under the assumptions of the Resource Competition Hypothesis (RCH), we predicted that young hatched in high-quality territories would have longer post-fledging dependence periods than young hatched in low-quality territories. As an alternative, we tested the Ontogenetic Switch Hypothesis (OSH), which predicts a better body condition in early dispersing young. For this purpose we measured body condition of young through levels of urea in the blood plasma. We found a weak positive effect of natal habitat quality on the length of the post-fledging dependence period, but no effect of body condition. Siblings were dependent on their parents for a similar number of days, suggesting that habitat and/or parent quality might influence the length of the post-fledging dependence period. Young hatched in 1999 had shorter post-fledging dependence periods than young hatched in 1998 or 2000. The date of independence for young Bonelli’s Eagles was correlated with the timing of breeding (laying date), but not with the length of the post-fledging dependence period. Neither brood size nor sex affected the length of this period. Key words: habitat quality, post-fledging dependence period, Hieraaetus fasciatus, Spain Department of Applied Biology, Estación Biológica de Doñana, Consejo Superior de Investigaciones Científicas, Avda. de María Luisa s/n, Pabellón del Perú, Seville 41013, Spain; *corresponding author ([email protected])

INTRODUCTION

1990, Pusey & Wolf 1996). The decision to move

Natal dispersal is a three-step process involving a decision to leave the natal area (emigration), a transient phase and selection of a breeding site (Clobert et al. 2001). Three major hypotheses have been proposed to explain the ultimate causes of natal dispersal in animal species: competition for resources, competition for mates and avoidance of inbreeding (Greenwood 1980, Johnson & Gaines

may also be provoked by proximate factors. Among the hypotheses explaining dispersal, aggression from conspecifics (Christian 1970) and the need to attain a threshold body condition before dispersal (Holekamp 1986) have attracted much attention. Dispersal and dispersive behaviour most likely depend on interacting factors, and the various hypotheses explaining natal dispersal are not necessarily mutually exclusive (Dobson & Jones 1985).

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Before becoming independent, most birds including raptors show a prolonged period of dependence from their parents (Newton 1979). The time between fledging and dispersal has been called the post-fledging dependence period (Newton 1979). The duration of this period depends on several factors (Bustamante & Hiraldo 1990, Ferrer 1992a). The departure from natal areas might be influenced by a progressively decreasing parental investment in order to save resources for the next breeding season (Ferrer 1992a). On the other hand, young eagles might try to ‘deceive’ parents to extend the period of dependence, thereby increasing the probability of survival. In birds of prey, several factors affect the length of the post-fledging dependence period: timing of breeding (Bustamente & Hiraldo 1990, Donazar & Ceballos 1990, Ferrer 1992a, Pomarol 1994, Arroyo 1995), body condition at fledging (Ferrer 1992a, Dewey & Kennedy 2001), brood size (Ferrer 1992a, Walls & Kenward 1995), gender (Kenward et al. 1993), hatching order (Wood et al. 1998, Ferrer 1992a), and dominance status within the brood (Ellsworth & Belthoff 1999). In Bonelli’s Eagles the post-fledging period has been studied by Morvan & Dobchies (1990), Real et al. (1998), and Minguez et al. (2001). Cadahía et al. (2005) provided information on the onset of dispersal and movements of satellite-tracked juveniles, and Balbontín (2005) identified suitable habitat for immature eagles in southern Spain. The present study extends on the study of Minguez et al. (2001), and provides information on the duration of the post-fledging dependence period for 28 radio-tagged young from 1998 to 2000. Our main objective was to understand the proximate factors that influence the timing of departure from natal areas, especially environmental conditions and body condition. Two opposite interpretations have been proposed to explain the effect of food availability on the onset of dispersal, i.e. the Resource Competition Hypothesis (RCH; Howard 1960, Murray 1967) and the Ontogenetic Switch Hypothesis (OSH; Holekamp 1986). The RCH states that dispersal of young is due to

intraspecific competition for food, mate or territory, and the prediction, therefore, is that during food abundance young stay longer within the natal territory (Kennedy & Ward 1995, Walker 1988). Conversely, the OSH predicts the opposite, i.e. if food is abundant and young reach a good condition earlier in life, the date of dispersal is advanced (Ferrer 1993a, Bustamante 1994, Walls & Kenward 1995, Wood et al. 1998). To test these predictions we collected information on the quality of territories (by quantifying habitat characteristics) and on the body condition of the chicks (from blood profiles). Under the assumptions of the RCH we expected that young hatched in high-quality habitats have longer postfledging dependence periods than young hatched in low-quality habitats. Under the assumptions of OSH we expected a negative correlation between body condition of the young and the length of the post-fledging dependence period. Such a relationship is expected both between and within broods. Both hypotheses hinge on the assumption of a critical role of resources within a territory. Since siblings share the same environmental conditions within their natal areas we tested therefore the similarity of the post-fledging dependence periods and body condition between siblings.

METHODS We studied a breeding population of Bonelli’s Eagles in the province of Cádiz (southern Spain, 36º41'N, 5º32'W), located in the Cordilleras Béticas, the main mountain system of the region which is composed of the Sierras Penibéticas in the south, close to the Mediterranean, and the Sierras Subbéticas further north. Altitude ranges from 80 to 3482 m a.s.l., and the climate is sub-arid Mediterranean (Rivas-Martinez 1986), with a usual annual rainfall of 200–1500 mm. The landscape is characterised by a mosaic of forests (Quercus suber, Q. rotundifolia and Pinus spp.), matorral (Quercus coccifera, Thymus vulgaris and Rosmarinus officinalis), calcareous rock, as well as pastures and fallow land at lower altitudes.

Balbontín & Ferrer: ONSET OF DISPERSAL

The Bonelli’s Eagle is a long-lived raptor that in the Iberian Peninsula breeds between January and June. Maximum life span is 20 years in captivity (Newton 1979). This raptor has a modal clutch size of two eggs (range 1–3) and an age at first reproduction of about 3.5 years (Cramp & Simmons 1980). We collected information on the breeding biology of Bonelli’s Eagle in the Cádiz population in 1998–2000. We checked 14 nesting cliffs three times per year. A ‘nesting cliff’ is a cliff where a pair attempted to breed. Between January and early February, we checked for territory occupancy (territorial display, transportation of nest material), then again from late February to March to record the start or failure of reproduction (e.g. if the female was incubating or not), and once more during April and May to count the number of fledglings. We marked nestlings when between 47 and 53 days old, approximately ten days before fledging.

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Young were ringed and equipped with a 30–35 g transmitter representing 2–3% of their body mass at the time of the first flight (Fig. 1). The radio tags were provided by Biotrack (Wareham, UK) and were fixed on the back of the eagles with a Teflon harness (Kenward 1987). Laying dates were back-calculated from nestlings aged on the basis of plumage development, observations at target nests and other age-related information from the literature (Cramp & Simmons 1980, Torres et al. 1981) and personal experience. Our final sample of young was composed of 14 females and 14 males belonging to 14 different territories marked in three different years, i.e. 10 chicks from double broods and 3 single chicks in 1998, 5 chicks from double broods and 2 single chicks in 1999, and 6 chicks from double broods and 2 single chicks in 2000. To evaluate body condition about 2 ml of blood was taken between 11:00 h and 15:00 h from the brachial vein of the nestlings, and stored

Figure 1. Nestlings were equipped with a transmitter fixed on the back with a Teflon harness (photo José Ramón Benitez).

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in tubes with lithium-heparin. Blood was centrifuged and plasma was separated (10 min at 3000 rpm) within 12 h after the sample was drawn, and both the cellular fraction and the plasma samples were immediately frozen (–80ºC). Analyses were carried out with a Hitachi 705 multichannel automatic analyser, with the reagents recommended by Boehringer-Mannheim (Darmstadt, Germany). Plasma was analysed for urea (urease method) and uric acid (uricase method). In the range of values found in urea and uric acid plasma concentration, the Hitachi 705 analyser showed a coefficient of variation of 6.25% and 2.39% for urea and uric acid respectively. The levels of urea and uric acid in the blood are good indicators of body condition in species with low fat reserves, such as raptors (Ferrer 1993b). The reliability of these parameters as a measure of body condition has been clearly demonstrated in experimental studies involving fasting and re-feeding (García-Rodriguez et al. 1987, Alonso-Alvarez & Ferrer 2001). The time a bird takes to deplete its fat reserves and the moment it starts using its muscle tissues as an energy source essentially varies according to the individual’s initial condition and the species’ capacity for storing fat reserves (Cherel et al. 1987, García-Rodriguez et al. 1987, Balbontín & Ferrer 2002, 2005). As raptors have a poor fat storage capacity (Ferrer 1990), the activation of protein catabolism occurs very quickly. Although urea and uric acid plasma levels are both measures of body condition, we only used urea levels since the two variables were correlated positively (Spearman correlation, rs = 0.74, P < 0.0001, n = 25; from 3 chicks insufficient blood was removed to analyse the urea concentration). The cellular fraction of the blood samples was used to sex the young. For this analysis, primers 2945F, cfR and 3224R were used following Ellegren (1996). After marking, each young eagle was tracked once a week by short-distance triangulation (2 km) with a 100 m tracking resolution, using a Stabo receiver provided by GFT (Horst, Germany) and a three-element Yagi antenna. When the young were 3.5 km from the nest for two succes-

sive observation days, this was used as the date of independence (half the Nearest Neighbour Distance; Penteriani et al. 2003, Balbontín et al. 2003). We used Ranges V software (Kenward & Hodder 1992) and Animal Movement Analysis (an extension for Arcview; Hooge & Eichenlaub 1997) to analyse home range data. We quantified habitat quality with habitat features at the landscape level in 14 territories where radio-tagged eagles had fledged. Using a Geographic Information System (GIS; IDRISI program, Eastman 1997) we measured habitat characteristics related to topography and land cover in natal territories (Table 1). Previous knowledge of habitat requirements indicated that Bonelli’s Eagles prefer open areas, with a high proportion of pastures, non-irrigated crops and edge habitats (Mañosa et al. 1998, Balbontín 2004, Ontiveros et al. 2005). Open areas are high-quality foraging habitats for a number of birds of prey (Pedrini & Sergio 2001, Sergio et al. 2004, Sergio et al. 2005), including Bonelli’s Eagle (Carrete 2002, Penteriani et al. 2003). These habitats abound in European Rabbits Oryctolagus cuniculus and Red-legged Partridges Alectoris rufa, the main prey species of Bonelli’s Eagles (Gil-Sánchez et al. 1994). Rabbit abundance in southern Spain was related to ecotones, non-irrigated mixed crops and natural vegetation (Angulo 2003). Open habitats facilitate prey detection and increase the predators’ hunting efficiency (Carrete 2002). Landscape characteristics were analysed by means of GIS. The analysis of landscape features was based on circular plots with a radius of 3.5 km, centred on active nests and equivalent to half the mean distance between 203 neighbouring nest sites (Balbontín 2004, Penteriani et al. 2003). Variables relating to land cover were calculated from 1:50 000 land-use maps (1995) of the Sistema de Información Ambiental de Andalucía (Andalucian Environmental Information System), which are based on interpretations of Landsat 5 TM 1:60 000 colour aerial photographs (Moreira & Fernández-Palacios 1995). Topography-related variables were measured using a Digital Elevation Model (DEM) with a resolution of 20 m, produced

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Table 1. Contribution of each original habitat variable on PC1 (i.e. factor loadings for PC1) of a PCA used to reduce the original 13 habitat variables (absolute values of loadings > 0.70 in bold). Code

Meaning

DFOREST DSCRUB DPASTURE DISTNON-IRR AVEALT AVESLOPE PNON-IRRI PFOREST PSCRUB PPASTURE SECMAT

Distance to nearest forest 1 Distance to nearest scrubland 2 Distance to nearest pasture Distance to nearest non-irrigate crop Mean altitude within a 3.5 km radii circle Mean slope within a 3.5 km radii circle % non-irrigated crop % Forest % Scrubland % pasture Ecotone (ha) between non-irrigated crop and scrubland within a 3.5 km circle Ecotone (ha) between non-irrigated crop and pasture within a 3.5 km circle Ecotone (ha) between scrubland and pasture within a 3.5 km circle

SECPAS MATPAS 1 2

Loading PC1 0.1956 0.5934 –0.2736 –0.8799 –0.1441 0.2897 0.7882 –0.6180 –0.7983 0.1360 0.4087 0.7697 –0.1929

mainly Quercus suber, Q. rotundifola and Pinus spp. matorral of mainly Quercus coccifera, Thymus vulgaris and Rosmarinus officinalis.

for the Andalucian government (REDIAM 1999). Other variables measured included the distance from the active nest of each territory to the nearest land cover feature. We reduced the original 13 landscape variables running a Principal Component Analysis (Pimental 1979) to produce a habitat gradient. The first component explained 38% of the original variance and arranged the 14 breeding territories along a gradient from less open to more open habitats. Its scores ranged from –1.719 to 1.940. Positive values show habitats with a high proportion of open and edge habitats, indicating good-quality foraging habitats. Negative scores denote habitats with a small proportion of open and edge habitats, indicative of low-quality foraging habitats (Table 1). We used Generalized Linear Mixed Models (GLMM, Littell et al. 1996) with the GLIMMIX macro procedure of SAS package (SAS institute 1996) to investigate factors affecting the length of the post-fledging period. We used a normal distribution of errors and an identity link function. GLIMMIX automatically adjusts overdispersion by

dividing the deviance by the dispersion parameter. Models were tested with F-statistics for fixed effects and Z-statistics for random effects (see Littell et al. 1996 for more details). The explanatory variables were laying date, year, brood size, sex, the scores of the first principal component (as a measure of habitat quality), territory location, and the urea plasma concentration (as a measure of body condition). Starting with a model containing all variables non-significant variables were subsequently dropped. Territory was considered as a random factor, and to control for pseudoreplication this variable was kept in all models tested. We found a correlation in the length of the post-fledging period between siblings (see Results). To check the probability of obtaining a correlation in the length of the post-fledging period between a random sample of seven twins composed by non-siblings chicks, we used a bootstrap method (Matlab 5 code ‘bootstrp.m’). We simulated our data to calculate the probability of obtaining a significant correlation in the length of the post-fledging period between non-siblings sim-

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ilar as we found in siblings. Each simulation randomly extracted seven pairs from our sample of 28 individuals, avoiding pairing of siblings. Subsequently, we calculated the Spearman correlation coefficient rs on the length of the post-fledging period between non-siblings pairs. The program was run 1000 times, each cycle producing one rs. We also used Spearman correlation to test relationships between length of the post-fledging period and date of independence, using the means of broods to avoid pseudoreplication. All tests were two-tailed and statistical significance was set at P < 0.05. Means are given ± 1 SD.

RESULTS Young eagles fledged on average on 14 May (range 29 April–22 June, n = 29, and the mean dispersal date was 30 July (range 25 June–2 October, n = 28). One eagle did not survive the post-fledging dependence period. None of 28 fledglings remained in their natal territory for more than 114 days after fledging. The mean length of the post-fledging period was 77 ± 19 days (range 50–114, n = 28). Independence date was positively correlated with laying date (rs = 0.56, n = 20, P = 0.002). The length of the post-fledging dependence period varied significantly by year (Table 2). In 1999 the post-fledging dependence period was on average 61 ± 11 days, hence shorter than in 1998 (mean 84 ± 17 days) or 2000 (mean 95 ± 14 days), respectively. While controlling for year effects, none of the other parameters measured had a significant effect on the dependence period. However, the effect of the measure of habitat quality (PC1) approached significance, suggesting that the period of dependence was longest in highquality territories. Covariance components associated with the random effect were very close to zero in this model (Z = 0.18, P = 0.42). The length of the post-fledging period was positively correlated between siblings (Fig. 2A). Bootstrapping showed that this positive correlation was unlikely due to chance: the probability of

Table 2. Results of GLMMs for explaining variation in the length of the post-fledging dependence period in Bonelli’s Eagles. Explanatory variables were measures of body condition (urea plasma levels), habitat quality (PC1), laying date, brood size, sex, year, and territory location. The final model included year and territory only (df of error term 11). Estimates of non-significant terms were calculated before they were removed from the model. Effect Intercept Year 1998 1999 2000

Estimate

SE

93.04

5.58

–8.60 –33.9 0

6.88 8.00

Non-significant terms Habitat quality 5.04 Body condition –0.35 Laying date –0.014 Brood size 1 –2.02 2 0 Sex M 5.09 F 0

2.96 0.82 0.73

df

F

P

2

9.51

0.004

1 1 1 1

2.90 0.18 0.04 0.08

0.11 0.68 0.84 0.78

1 6.02

0.72

0.41

7.10

obtaining a similar high rs value from our sample of non-siblings was less than 0.029. Likewise, siblings had similar body condition (Fig. 2B). Within broods there was no relationship discernable between body condition and the length of the dependence period (rs = 0.27, n = 5, P not computable; comparing the differences between body condition and post-fledging periods).

DISCUSSION The dispersal behaviour of young Bonelli’s Eagles was better explained by the Resource Competition Hypothesis (RCH) than by the Ontogenetic Switch hypothesis (OSH), although evidence in favour of the RCH was weak. Young eagles that were raised in territories with more open habitat (high-quality foraging habitat) tended to show a prolonged

length post-fledging period (d, sibling 2)


120

A

100

80

60 60

80

100

120

urea (mg/dl, sibling 2)

length post-fledging period (d, sibling 1) 25

20

15

B

10 10

15

20

25

urea (mg/dl, sibling 1)

Figure 2. Comparing (A) the length of the post-fledging period (rs=0.892, P < 0.05, n = 7) and (B) the body condition (rs = 0.97, n = 5, P not computable) between siblings.

post-fledging period. Body condition had only a marginal effect on the post-fledging period, and its direction (longer periods for individuals in better condition) was more supportive for the RCH than the OSH. Under the OSH young eagles with low levels of urea in plasma (good body condition) should depart earlier from natal areas than young with high levels of urea in plasma. A word of caution is needed on the measurement of body condition (taken approximately ten days before fledging) because we assumed that it was representative for the whole post-fledging period but this needs testing. We found that siblings tended to disperse at similar ages. Siblings share the same territory and are exposed to similar environmental conditions throughout the dependency period. If competition for resources triggers dispersal behaviour, then this outcome should be expected. The within-brood comparison of body condition and the length of

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the post-fledging period did not allow to draw firm conclusions due to the small sample size of twins; moreover the limited variation between siblings hampered the power of the statistical test. It has been stated that late dispersal involves individuals with less competitive abilities (Waser 1985), and individuals dispersing early are supposed to have an adaptive advantage (Lidicker & Stenseth 1992). The cost of early dispersal could be high, however, if the individual has not achieved an appropriate body condition before dispersal. This may be true in particular for longlived species as eagles that have several years to prepare for the first reproductive attempt (Cramp & Simmons 1980). A strategy of staying in the natal territory as long as foraging conditions allow, which is supported by our data, seems therefore more adaptive than minimising the length of the post-fledging period. Surprisingly, we did not find a covariation between habitat quality and body condition of the young. We think the reason was that body condition of young was affected by several factors. For example, young from broods of two were in poorer body condition than singles, but only so during a year of adverse environmental conditions and not in favourable years (Balbontín & Ferrer 2005). Therefore, not only the quality of the territory but multiple factors determine body condition of the young at fledging, and larger sample sizes than we have at this moment are needed to disentangle all effects. We found large variation in the duration of the post-fledging dependence period among years. To what extent this variation was determined by differences in prey abundance or availability we do not know. In contrast, during the eagle’s nesting period rainfall has been established to be an important determinant of food availability. Thus, precipitation was high during the nesting season of 1998, and the inferred food availability was low, whereas during the breeding seasons of 1999 and 2000 the opposite was the case. Certainly, more effort will be needed in future studies to estimate the foraging conditions within territories during the post-fledging period.

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ACKNOWLEDGEMENTS We thank J.A. Gil, E. Minguez, J. R. Benitez, V. Siebering, G. Moreno, C. Aguilar and E. Sáez for their help in the field. We also thank E. Calvo for climbing the nest-cliffs. Thank you very much to my brother Juan Balbontín for his Visual Basic application to build vectorial files needed for the habitat analyses, and to C. Melian for his script in matlab for bootstrap analysis. C. F. Vega and C. AlonsoAlvarez helped with the blood analysis. F. Recio and the lab personal of Valme Hospital kindly allowed the use of their lab equipment. V. Penteriani, Rob Bijlsma, Jouke Prop, F. Sergio and three anonymous referees made helpful comments. Also, we would like to thank A. Ortiz and the personnel of the Andalusia Government (Junta de Andalucia, Consejeria de Medio Ambiente) for giving access to the raster cartography employed in this study.

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SAMENVATTING Jonge Havikarenden Hieraaetus fasciatus zijn na het uitvliegen nog geruime tijd van hun ouders afhankelijk. In deze studie van Havikarenden in Zuid-Spanje werd bekeken of de duur van die afhankelijkheidsperiode werd bepaald door de kwaliteit van de broedplaats (een hoge

kwaliteit zou jonge arenden langer in het territorium kunnen laten vertoeven, en vice versa), dan wel door de conditie van de jongen (een goede conditie zou in snellere dispersie moeten resulteren). Om dit uit te knobbelen werd een aantal relevante habitatvariabelen gekwantificeerd. Als maat voor de voedingstoestand van de jongen werd het ureum- en urinezuurgehalte in het bloedplasma onderzocht. Tussen 1998 en 2000 werden 28 jongen afkomstig van 14 broedplaatsen van een zender voorzien. Daarmee konden ze na het uitvliegen op de voet worden gevolgd. Het moment waarop ze gedurende twee opeenvolgende dagen meer dan 3,5 km van de nestlocatie zaten, werd beschouwd als de start van hun onafhankelijkheid van de ouderlijke zorg. De jonge arenden vlogen gemiddeld op 14 mei uit. Geen enkel jong vertoefde langer dan 114 dagen na het uitvliegen op de broedplaats (spreiding 50–114 dagen, gemiddeld 77 dagen). Hoe vroeger het broedsel was begonnen, des te vroeger ook werden de jongen zelfstandig. Geslacht noch conditie van de jongen speelde een rol bij de duur van de afhankelijkheidsperiode; maar de kwaliteit van het territorium (de gemeten habitatvariabelen) had wel een effect, hoewel amper significant. Jongen in een kwalitatief goed habitat bleven langer in het territorium dan vogels in een ongunstiger gebied. Te verwachten is dat dit doorwerkt op de overlevingskansen van de vogels. (RGB) Corresponding editor: Rob G. Bijlsma Received 15 March 2005; accepted 20 November 2005