Diet Specificity Is Not Associated with Increased Reproductive

Ibis (2009), 151, 255–264

Diet speciﬁcity is not associated with increased reproductive performance of Golden Eagles Aquila chrysaetos in Western Scotland

D. P. WHITFIELD,1*ROBINREID,2 PAUL F. HAWORTH,3 MIKE MADDERS,1 MICK MARQUISS,1 RUTH TINGAY1 & ALAN H. FIELDING3 1Natural Research, Brathens Business Park, Hill of Brathens, Glassel, Banchory, Aberdeenshire AB31 4BY, UK 2Ash Tree Cottage, Riding Mill, Northumberland NE44 6DY, UK 3Biological Sciences, Manchester Metropolitan University, Manchester M1 5GD, UK

Amongst raptor species, individuals with specialized diets are commonly observed to have higher reproductive output than those with general diets. A suggested cause is that foraging efficiency benefits accrue to diet specialists. This diet specificity hypothesis thus predicts that diet breadth and reproductive success should be inversely related within species. We highlight, however, that a prey availability hypothesis also makes the same prediction in some circumstances. Hence, when high diet specificity results from high encounter rates with an abundant, preferred prey, then prey availability may affect reproductive success, with diet specialization as an incidental correlate. Using three insular study areas in western Scotland, we examine diet specificity and reproductive success in Golden Eagles Aquila chrysaetos. Diet breadth and breeding productivity were not negatively related in any of our study areas, even though birds with specific diets did tend to have a higher incidence of preferred prey (grouse and lagomorphs) in the diet. Indeed, in two study areas there was evidence that diet generalists had higher breeding productivity. Our results therefore failed to support the diet specificity hypothesis but were consistent with the prey availability hypothesis. We highlight that although many other studies are superficially consistent with the diet specificity hypothesis, our study is not alone in failing to provide support and that the hypothesis does not provide a generic explanation for all relevant results. Diet specificity in predators can be at least partially a response to prey diversity, availability and distribution, and benefits associated with different prey types, so that being a generalist is not necessarily intrinsically disadvanta- geous. We suggest that the available evidence is more consistent with variation in prey abundance and availability as a more influential factor explaining spatial and temporal variation in breeding productivity of ‘generalist’ species such as the Golden Eagle. Under this argument, prey abundance and availability are the main drivers of variation in reproductive output. Diet specificity is a consequence of variation in prey availability, rather than a substantial cause of variation in reproductive success. Keywords: breeding success, diet breadth, feeding specialization, food abundance, raptor.

Feeding or dietary specialization of individuals is a tion is expected to evolve when heritable variation neglected research field, yet it has profound eco- in food selection behaviour confers a fitness advan- logical, evolutionary and conservation implications tage (MacArthur & Pianka 1966, Partridge & (Lomnicki 1978, Partridge & Green 1985, Durell Green 1985, 1987), as has been observed in birds 2000, Bolnick et al. 2003). Ultimately, specializa- (Partridge & Green 1987, Annett & Pierotti 1999, Golet et al. 2000, although see Woo et al. 2008). *Corresponding author. The metrics by which fitness advantage might be Email: phil.whitfi[email protected] measured, such as foraging efficiency, survival or

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reproductive output, are then expected to be hypothesis), then diet specificity may be a direct greater for specialists than for generalists, at least cause of high reproductive success through the in relation to the preferred food or selection fitness benefits of individual specialization. behaviour of specialists. Variation that may lead to Equally, however, diet specificity may simply be specialization is multi-faceted and may be pro- an incidental correlate of high reproductive suc- moted by differences in phenotype (e.g. morphol- cess of birds whose breeding attempts coincide ogy), spatial or temporal heterogeneity in the with high availability of preferred prey items. In abundance or diversity of foods, and cultural influ- such systems, both diet specificity and prey avail- ence or early experience (Partridge & Green 1985, ability hypotheses make identical predictions on Whitfield 1990, Durell 2000). Alternative special- the relationship between diet and reproductive izations may or may not differ in profitability success. (Whitfield 1990, Annett & Pierotti 1999, Durell The causes of variation in breeding productivity 2000, 2007). are important in understanding the population Research on the fitness consequences of diet var- ecology of raptors (Newton 1979) and other birds iation remains very limited (Bolnick et al. 2003, (Newton 1998), as well as having applications to Woo et al. 2008), although studies of individual population management (Katzner et al. 2005). Fur- variation in diet are frequent, especially in raptors. ther testing of the diet specificity and prey avail- A common finding is that as the abundance of a ability hypotheses is therefore valuable. preferred prey species declines in the environment, In this paper, using a study of three insular dietary breadth increases and reproductive success groups of Golden Eagles in western Scotland, declines (e.g. Steenhof & Kochert 1988, Korpimäki we examine relationships between diet specificity 1992, Steenhof et al. 1997, McIntyre & Adams and reproductive success. First, in each study 1999, Nielsen 1999, Arroyo & Garcia 2006). area we test whether there is an association Watson (1997) confirmed this finding in Golden between breeding productivity and diet breadth. Eagles Aquila chrysaetos, using international results Secondly, we test whether there is an association from several studies, and Katzner et al. (2005) between diet breadth and the prevalence of pre- showed that some measures of breeding density ferred prey in the diet, and whether prevalence and success of Imperial Eagles Aquila heliaca in of preferred prey in diet is associated with Kazakhstan were positively correlated with diet reproductive output. We assume that in Scotland specificity. Both of these authors considered that if preferred prey are lagomorphs (Rabbits and birds specialize on a small number of prey species, hares) and grouse, based on several pieces of this engenders greater foraging efficiency and, ulti- evidence, including previous dietary studies in mately, reproductive success. This is the diet speci- Scotland (Watson 1997), although to our knowl- ficity hypothesis (Watson 1997, Katzner et al. edge no Scottish study has examined if these 2005). However, a positive association between prey are disproportionately captured by Golden diet specificity and reproductive success within a Eagles relative to their abundance. Other evi- population may also occur simply as a function of dence included studies of preferences elsewhere spatial and temporal variation in the availability for ecologically equivalent prey species (e.g. of preferred prey (e.g. Korpimäki 1992, Steenhof Steenhof & Kochert 1988) and Watson’s (1997) et al. 1997, Arroyo & Garcia 2006), irrespective of review, which documented a consistent dietary individual variation in tendency to specialize. In prevalence, across a large number of studies and other words, when there is a high availability of extensive geography, for four prey families: preferred prey, reproductive success may increase Leporidae (Rabbits and hares), Sciuridae (ground because prey capture rates, reflecting greater prey squirrels and marmots), Tetraonidae (grouse) and encounter rates, also increase, and high diet Phasianidae (pheasants and partridges). The most specificity simply reflects these enhanced opportu- common representatives of these families in our nities. This can be termed the prey availability study areas (and across the distribution of hypothesis. Golden Eagles in Scotland: Watson 1997) were So, in systems where variation in individual Rabbit Oryctolagus cuniculus, Mountain Hare foraging behaviour, food abundance and repro- Lepus timidus, and Red Grouse Lagopus lagopus ductive success co-vary (such as those eagle popu- scoticus, so we assumed that these were pre- lations used to develop the diet specificity ferred prey.

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tion purposes and diet-composition analyses we METHODS combined species into higher taxonomic groups, as Our three study areas were in the Hebridean follows: (1) seabirds – Procellariidae, principally islands of western Scotland, involving Mull, in the Northern Fulmar Fulmarus glacialis, and also Inner Hebrides, Lewis and Harris, the northern- Northern Gannet Morus bassanus, Phalacrocoraci- most islands of the Outer Hebrides (Western Isles) dae, Laridae, Alcidae; (2) waterbirds – mostly Grey and the Uists and Benbecula, the southernmost Heron Ardea cinerea, but also divers Gavia spp.; chain of islands of the Outer Hebrides. We studied (3) waterfowl – Anseriformes; (4) waders – Hae- 14 Golden Eagle territories on Mull, 24 territories matopodidae, Scolopacidae and Charadriidae; (5) on Lewis and Harris, and 15 territories on Uists diurnal raptors and owls – Accipitridae, Falconidae (Fig. 1). Diet data were gathered from Mull in and Strigidae; (6) gamebirds – primarily Red 1992 and 1999–2002, from Lewis and Harris in Grouse, but occasionally Common Pheasant Phasi- 2002–2005, and from Uists in 2003–2006. Prey anus colchicus; (7) terrestrial birds – Passeriformes, remains were collected from nests and the immedi- mainly Northern Raven Corvus corax and Hooded ate surroundings once each year after a breeding Crow Corvus cornix, and other birds not covered attempt had finished, typically in August after by other classes; (8) Rabbit; (9) Mountain Hare; eaglets had fledged. (10) deer – Cervidae (almost entirely Red Deer Prey remains were identified to species when- Cervus elaphus); (11) sheep – Ovis aries, mostly ever possible, ensuring that the collected parts of lambs; (12) other mammals – including voles, an item did not result in the same individual being shrews, Brown Rat Rattus norvegicus, Mustelidae counted twice. A total of 106 prey taxa (100 spe- and European Hedgehog Erinaceus europaeus. cies, three genera, three classes) were used in diet Masses of prey species were taken from Cramp breadth estimations, encompassing birds, mam- et al. (1977–1994) and Blackburn and Gaston mals, reptiles, amphibians and fish. For presenta- (1998), subtracting 20% to account for ‘wastage’. According to some authors, ‘end of season’ collections bias diet estimates towards items which are robust (e.g. large bones) and against items which are subject to rapid deterioration (e.g. small mammals and birds, or soft-bodied items) (e.g. Mersmann et al. 1992). Others, however, have suggested that some Golden Eagles may selectively remove remains of large prey items from nests (Tjernberg 1981). Collopy (1983) found that analysis of prey remains produced relatively reliable estimates of Golden Eagle diet, but this was based on frequent collections of remains and not a single collection towards or at the end of breeding. Such single collections, as in the present study, have nev- ertheless been the primary method used by previous studies involved in the hypotheses that we examined (e.g. Watson 1997). Hence, we could exclude any biases inherent in this method, which were common across all our analysis-groups, as influences on our conclusions. We preferred the use of prey remains over regurgitated oral pellets because it allowed a finer degree of taxonomic discrimination (Greene & Jaksic´ 1983) and because pellets of Golden Eagles were subject to a minor degree of confusion with Figure 1. North-west Scotland (inset) showing the locations of pellets of sympatric White-tailed Eagles Haliaeetus the three study areas: Lewis and Harris (1), Uists (2) and albicilla (D.P. Whitfield et al. unpubl. data). Never- Mull (3). theless, as a check that our results were not due to

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bias in prey remains we also used pellets collected Diet breadth was indexed using the formula of in 1998–2002 at 13 Mull territories. Pellets were Levins (1968): collected from April to August at and immediately B ¼ 1=Rp2 around nest-sites and at roost sites known to be i used by the territorial pair in question. Materials in where pi = the proportion of the diet contributed pellets were identified down to the most specific by prey item i. taxonomic level that was practicable. When Levins’ index tends to weight in favour of abun- necessary, feather fragments were classified after dant prey items, andP was preferred over the examination of the downy barbules at 200· magni- Shannon index (H=) [pi · ln (pi)]), which fication, using a reference collection and Brom tends to weight in favour of rare items (Krebs (1986). Mammalian hair was classified using the 1989, Magurran 2003). Both indices were none- medullary pattern, using Teerink (1991). Due to theless highly correlated when applied to our inconsistency between individual pellets in the tax- samples (e.g. for 14 Mull territories, r=0.92). onomic level at which prey could be identified, we Reproductive output measures were obtained by adopted fewer classification categories than for standard monitoring methods, described in detail prey remains. The six categories were: (1) deer, (2) elsewhere (Whitfield et al. 2001, 2007, Hardey sheep and lambs, (3) lagomorphs (i.e. Rabbits and et al. 2006, Eaton et al. 2007), and were the same hares), (4) other mammals, (5) seabirds, (6) other as those used by the studies which developed the birds. The presence in a pellet of any material diet specificity hypothesis. We used breeding pro- which could be assigned to one of the six prey cat- ductivity (number of fledglings per year of territory egories was considered as one item for that prey occupation) as our standard reproductive success category. metric for Mull. For Uists and Lewis ⁄ Harris, data We took the territory as the sampling unit and a were available for 3 years (2003, 2005 and 2006, minimum of 10 items per territory for inclusion of and 2003–2005, respectively), and so we used total a sample in analyses, following Korpimäki (1992). count of fledglings produced as the reproductive We did not use an ‘asymptotic’ method (Pielou success metric. On both Uists and Lewis ⁄ Harris 1975) to determine sample size for diet description there was a new territory established after the first by plotting, for each prey category, sample size year of study, so that one territory in each of these against proportional contribution to diet with the study areas was occupied in only 2 of 3 years. We objective of determining stabilization in the latter omitted these two territories from analysis to avoid parameter’s measures (e.g. Ontiveros et al. 2005). bias because, due to annual variation in breeding This method is sensitive to number of prey productivity, lack of occupation within a short remains categories (Greene & Jaksic´ 1983) and we sample of years probably compromised compara- used a large number. We were more concerned bility across territories in the metric of interest. with potential biases caused by the effect of sam- Although 3 years of breeding productivity data ple size on diet breadth indices, especially the pos- provide relatively reliable estimates of differences sibility that a low sample size might lead to an between territories (Whitfield et al. 2008), for artificially low index of diet breadth. With our cri- Mull we used long-term breeding productivity data terion of n ‡ 10, and after pooling data across years (1990–2006) because they were available (e.g. by territory, there was no correlation between Whitfield et al. 2001), and our sampling of diet sample size and diet breadth (for example for sam- here encompassed a longer period. ple size correlated to Levins (1968) index of diet Age of eagles can affect their reproductive suc- breadth for 14 Mull territories, r=0.08). We com- cess (Newton 1979). We were confident, however, bined annual collections to enhance sample sizes that age effects did not unduly influence results in before deriving indices of diet breadth, so that our this study due to the long-term nature of our study replicate was the territory with all prey remains on Mull, specific data on the rarity of young birds pooled across years (e.g. for Mull, the mean sample in territorial pairs in the study populations, and of prey remains by territory was n = 34). Diet of knowledge that recruitment of young eagles is eagles in western Scotland appears to vary slightly infrequent in western Scotland (Whitfield et al. between years, but pooling data was necessary 2004). because Golden Eagles leave relatively few remains We used ANOVA and MANOVA to examine differ- in their nests (Madders & Marquiss 2003). ences in diet breadth and composition between

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study areas. According to the diet specificity Table 1. Estimated numeric diet composition for summary prey hypothesis, breeding productivity should always item groups according to prey remains by study area (n decline with increasing diet breadth (Watson 1997, territories by study area), based on totals of prey items: Mull = 511, Lewis ⁄ Harris = 597, Uists = 498. Katzner et al. 2005). We tested this hypothesis by treating each study area separately, both to provide Mean % (se) of diet by prey remains replication and to reflect spatial heterogeneity in Golden Eagle diet (Watson et al. 1993, Watson Prey item group Mull (14) Lewis & Harris (24) Uists (15) 1997, see also Penteriani et al. 2005). For Mull, Seabirds 12.2 (5.7) 17.1 (5.7) 14.3 (5.9) due to the long-term continuous availability of Waterbirds 0.3 (0.2) 1.8 (0.6) 2.0 (1.3) annual productivity measures which were normally Waterfowl 1.0 (0.6) 1.8 (0.7) 12.2 (3.6) distributed and did not deviate from linearity Waders 0.6 (0.5) 1.7 (0.5) 2.6 (0.9) assumptions during data explorations, we used a Diurnal raptor 5.5 (2.3) 0.1 (0.1) 3.0 (0.8) Gaussian GLM with identity link function, but for and owl Gamebirds 6.7 (1.2) 28.1 (4.6) 20.5 (5.1) Uists and Lewis ⁄ Harris we used Poisson GLMs Terrestrial birds 12.1 (2.4) 6.6 (1.3) 2.0 (0.7) with log link function because the productivity Rabbit 6.0 (2.2) 3.8 (1.4) 26.3 (3.6) data were effectively counts. We also examined Mountain Hare 33.6 (5.5) 19.6 (4.2) 0.0 (0.0) relationships between the contribution of preferred Deer 2.6 (1.0) 3.1 (1.4) 0.3 (0.3) prey items to diet breadth using Pearson correla- Sheep 12.0 (3.1) 11.7 (2.9) 3.4 (1.0) Other mammals 4.9 (2.0) 3.0 (1.2) 11.2 (2.1) tions, and to breeding productivity with GLMs (Gaussian for Mull, Poisson for Uists and Lewis ⁄ Harris). We expected that higher propor- tions of preferred prey items in the diet would the most frequent seabird prey on Lewis ⁄ Harris generate reduced diet breadth and, under the diet and Uists, but fewer seabirds and a wider range of specificity hypothesis, would be associated with species were evident on Mull (Table 1). The mean higher breeding productivity. (range) proportion of the diet comprising lagomorphs and gamebirds (numerically) was: Mull 0.46 (0.14–0.75), Lewis ⁄ Harris 0.52 (0.00–0.94), RESULTS and Uists 0.47 (0.17–0.76). Breeding productivity was similar across our Descriptions of diet and breeding study areas. Mean (range, n territories) number of productivity fledglings per year per occupied territory was: Mull Mean (range, n) Levins’ index of diet breadth was: 0.57 (0.19–1.0, 14), Lewis ⁄ Harris 0.52 (0–0.67, Mull 4.87 (1.15–9.09, 14), Lewis ⁄ Harris 3.69 20), and Uists 0.51 (0–1.33, 13). (1.14–8.00, 24), and Uists 4.75 (2.09–9.19, 15). There was no difference in diet breadth between Relationships between breeding study areas (ANOVA, F = 1.728, P=0.188). 2,50 productivity and diet breadth Diet composition, however, did vary between study areas (MANOVA, F24,78 = 5.820, P < 0.001), In none of our three study areas was there a signifi- with significant differences in waterfowl cant negative relationship between breeding (P < 0.001), diurnal raptors and owls (P=0.005), productivity and Levins’ index of diet breadth, gamebirds (P=0.005), other terrestrial birds either using prey remains or (Mull only) pellets; (P < 0.001), Rabbits (P < 0.001) hares (P < 0.001) rather, for Lewis ⁄ Harris a positive relationship and other mammals (P < 0.001) (Table 1). In par- approached significance (Table 2). There was also ticular, grouse were uncommon prey items on no indication (cf. Katzner et al. 2005) that territo- Mull, hares were absent on Uists, but Rabbits were ries ⁄ pairs with the highest productivity always had relatively common prey. Ravens and Hooded a specialized diet. As our results may have been Crows were more common prey on Mull than influenced by uneven sampling intensity across ter- elsewhere and waterfowl were more often taken ritories ⁄ pairs we also re-ran our analyses with the on Uists. Brown Rats were taken on Uists but not explanatory variable weighted by the square root elsewhere, whereas on Mull, mustelids and Euro- of sample size (number of prey remains or pellets). pean Hedgehog made up the most common ‘other Again, in no study area was there a significant neg- mammals’ component. The Northern Fulmar was ative relationship between breeding productivity

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Table 2. Results of GLMs (*Gaussian, **Poisson) using Levins’ both according to numbers (r=)0.710, index of diet breadth as an explanatory variable and breeding P=0.004) and mass (r=)0.624, P=0.017), but productivity as response variable, for each study area. was not correlated with breeding productivity Study area df Estimate se t *orz ** P based on numbers in the diet (Gaussian GLM: df = 1, 13, t=0.517, P=0.615). Similarly, basing Mull (remains) 1,13 0.003 0.026 0.124* 0.904 analysis on composition of pellets there was no sig- Lewis ⁄ Harris 1,22 0.126 0.082 1.533** 0.125 nificant relationship between the numeric propor- Uists 1,12 0.092 0.111 0.83** 0.407 tion of lagomorphs in the diet (n=13) and Mull (pellets) 1,12 )0.106 0.115 )0.920* 0.377 breeding productivity (Gaussian GLM: t=1.750, For Mull, GLMs were run with Levins’ index calculated sepa- P=0.108). rately using prey remains and pellets. On Lewis ⁄ Harris, where grouse were apparently slightly more important as prey than on Mull (Table 1), there was no significant correlation between proportion of diet involving lagomorphs and Levins’ index of diet breadth; instead, on both and grouse and diet breadth, either numerically Lewis ⁄ Harris and Uists breeding productivity was (r=)0.327, P=0.119, n=24) or by mass. Nei- positively related to diet breadth (Table 3). These ther were these numeric measures of diet composi- results provided no support for the diet specificity tion correlated with breeding productivity, hypothesis. With the possibility that eagles special- regardless of whether prey species were considered izing on seabirds (as relatively ‘unusual’ prey not in isolation or in combination (Poisson GLMs, in the ‘preferred’ four families of prey: Watson df = 1, 22). On Uists, hares were not present, but 1997) may have confounded support for the diet Rabbits and Red Grouse were the dominant diet specificity hypothesis, we also considered only ter- components. The proportion of diet (by numbers ritories on Lewis ⁄ Harris where pairs nested inland and by mass) comprised by these two species was (nest-site > 2 km from the coast). Again we found negatively correlated with diet breadth (e.g. no supportive evidence of a significant negative numerically: r=)0.617, P=0.014, n=15), but relationship between breeding productivity and these numeric measures were not correlated with Levins’ index of diet breadth (Poisson GLM, breeding productivity either for prey species alone df = 1, 7, z=1.135, P=0.257). or combined (Poisson GLMs, df = 1, 12). We also re-ran all GLMs for potential relationships between diet composition of ‘preferred’ prey and Breeding productivity and prevalence of breeding productivity using prey mass, for all study ‘preferred’ prey in diet areas and for all combinations of prey species. In On Mull, where Mountain Hares constituted the no case was there a statistically significant correla- vast majority of the lagomorph ⁄ grouse diet compo- tion. nent (Table 1), the proportion of diet estimated to be Mountain Hare using prey remains was DISCUSSION negatively correlated with diet breadth (n=14), Although the diet specificity hypothesis originated through an analysis of Golden Eagle diet breadth Table 3. Results of GLMs (*Gaussian, **Poisson) using Levins’ and breeding productivity from a global perspec- index of diet breadth as an explanatory variable (weighted by tive (Watson 1997) and a study of regional param- sample size of prey remains or pellets) and breeding eters in the closely related Imperial Eagle productivity as response variable, for each study area. (Katzner et al. 2005), our analysis involving Study area df Estimate se t *orz ** P Golden Eagles in western Scotland failed to support it. Indeed, we found evidence that in two Mull (remains) 1,13 0.000 0.027 0.000* 0.999 study areas the more reproductively successful Lewis ⁄ Harris 1,22 0.116 0.035 3.359** < 0.001 pairs had broader diets. Our results were thus Uists 1,12 0.084 0.041 2.062** 0.039 more consistent with the prey availability hypoth- Mull (pellets) 1,12 )0.066 0.120 )0.553* 0.592 esis, but because we did not measure prey avail- For Mull, GLMs were run with Levins’ index calculated sepa- ability they cannot be regarded as a definitive rately using prey remains and pellets. discriminatory test.

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Golden Eagle diet in western Scotland has been which have not confirmed the predicted negative characterized as atypically generalist (Watson relationship between diet breadth and reproduc- 1997). However, our analyses illustrated that, as tive output are perhaps more illuminating. For might be expected (Roughgarden 1972, Bolnick instance, in two subsets of an Eagle Owl Bubo bubo et al. 2003, Penteriani et al. 2005), a wide diet population in and around the Luberon massif in breadth across a population reflected the fact that southern France, ‘interior’ pairs showed a propen- some individuals had relatively specialized, but dif- sity to specialize on Rabbits, whereas ‘border’ pairs ferent, diets, whilst others took a wider range of had a broader diet and had higher reproductive prey types. Several pairs in our study areas appar- output (Penteriani et al. 2002). Ontiveros et al. ently conformed to the notion of a ‘typical’ (2005) found no relationship between breeding Scottish Golden Eagle diet (Watson 1997) in pre- productivity of Bonelli’s Eagle Hieraaetus fasciatus dominantly taking Red Grouse and ⁄ or lagomorphs, and the dietary frequency of the main prey species, whereas in other ‘specialist’ pairs, seabirds domi- and Margalida et al. (2009) reported that territo- nated the diet. In two of our three study areas we ries of Bearded Vultures Gypaetus barbatus with a showed that diet breadth and the proportion of wider diet breadth had greater reproductive suc- the supposedly ‘preferred’ prey species were nega- cess. We suggest, therefore, that the diet specificity tively related, as expected from other studies of hypothesis may not have broad utility and that both Golden Eagles (Watson 1997, Pedrini & other more generic explanations should usually be Sergio 2002) and other raptors (e.g. Arroyo & sought to explain the results of studies involving Garcia 2006). The range in our diet breadth diet breadth and breeding productivity. The prey indices between territories ⁄ pairs was wide, and availability hypothesis offers an explanation, or at measures of breeding productivity were also vari- least an alternative consideration that should be able, encompassing most of the values presented in accounted for in some circumstances. Watson’s (1997) global analysis. We therefore can Optimal diet theory has its failings (Sih & see no inherent reasons why our study should have Christensen 2001) but it illustrates the complexity produced atypical results. of factors behind individuals’ foraging decisions if Many authors other than Watson (1997) and it is assumed that decisions over alternative food Katzner et al. (2005) have reported results that can types are governed by selection to maximize a net be interpreted as supporting the diet specificity fitness benefit (which is also an implicit assump- hypothesis because they document a negative relation of the diet specificity hypothesis). Notably, tionship between diet breadth and breeding prey abundance and availability, and their influence productivity (e.g. Steenhof & Kochert 1988, on the net profitability of prey choices by the pred- Korpimäki 1992, Steenhof et al. 1997, Nielsen ator, play a pivotal role. Consequently, the factors 1999, Marchesi et al. 2002, Pedrini & Sergio 2002, leading to feeding specializations can be complex Arroyo & Garcia 2006). Indeed, Watson (1997) and so specialization can have different origins used 24 studies of Golden Eagle diet and breeding (Partridge & Green 1985, Whitfield 1990, Durell success to develop this hypothesis. As we have 2000). While simple theoretical considerations noted, however, the prey availability hypothesis predict that specialists can gain greater net benefits can also predict exactly the same relationship. than generalists (MacArthur & Pianka 1966), pay- Consequently, many of the studies which superfi- offs in practice will depend on, amongst other cially support the diet specificity hypothesis, but things, prey abundance and availability, and prey have also indexed prey availability or abundance, distribution. document covariance between diet breadth and Specialization can pay if efficient exploitation of the abundance of prey which predominate in diet one prey type automatically reduces the ability to during productive breeding (e.g. Steenhof & exploit other prey types efficiently so that general- Kochert 1988, Korpimäki 1992). Other research ist feeding is more costly, perhaps because it has recorded productive breeding coinciding with requires maintenance of more sensory or digestive high measures of selected prey abundance indices facilities (Partridge & Green 1985). But Partridge without reference to diet breadth (e.g. Tjernberg and Green (1985) also note the influence of a 1983, McIntyre & Adams 1999). patchy food supply in governing dietary choices, In light of the lack of exclusivity in the main and that some individuals may specialize because prediction of the diet specificity hypothesis, studies they have a highly restricted choice of prey types

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either through such environmental patchiness or output. The two hypotheses are of course not phenotypic constraints. In this context, a good mutually exclusive, and both mechanisms may example of how specialization may involve territo- have played a part in the results obtained by Katz- rial individuals ‘making the best of a bad job’ is ner et al. (2005) for Imperial Eagles; although this given by Penteriani et al.’s (2002) study of Eagle study did not consider a role of prey availability, it Owls. We speculate that several of the apparent is implied by Katzner et al. (2006). Given the specialists in our study were Golden Eagles faced many studies available, the subject may be appro- with a limited choice of prey at low availability, priate for a meta-analysis (Hedges & Ingram 1985) and that some generalists were birds with access to to tease apart further its complexities, although a wider choice of prey at higher availability. any such future research should be aware of the A positive association between specialized diet potential pitfalls of publication bias (Dickersin and reproductive success should be expected 1990). when the spatial and temporal availability of spe- In relation to conservation management, our cific profitable prey types is predictable or stable study confirms our previous analyses (Whitfield (Sherry 1990, Ward 1992, Šimková et al. 2006). et al. 2001, 2007), and those of Kochert et al. When prey availability is unpredictable or vari- (1999) in emphasizing the importance of indi- able, such as in some systems of the northern vidual differences between Golden Eagle territo- hemisphere (Hanski et al. 1991, Korpimäki et al. ries and the dangers of employing generic 2004), then alternative strategies are either to be management initiatives. For example, in territo- a generalist, or to remain a specialist but either ries where prey species are low in diversity and curtail breeding whenever and wherever preferred abundance, but include preferred species (lago- prey are unavailable, or disperse (Clobert et al. morphs and ⁄ or grouse), then efforts to enhance 2001) to exploit areas of high preferred prey the abundance of these prey would be beneficial. availability. In the northern hemisphere this may However, in those where a diversity of prey explain why some birds (e.g. Long-tailed Skua species is available and eagles are relatively pro- Stercorarius longicaudus or Snowy Owl Bubo scan- ductive, then management emphasis on main- diaca) specializing in eating small mammals with taining or enhancing this diversity may bring highly variable spatial-temporal availability (e.g. greater rewards. Microtus or Dicrostonyx spp.) have low philopatry (e.g. Hanski et al. 1991). In contrast, a generalist We are grateful to the landowners and farmers in our diet might be expected in the highly territorial, study areas for their co-operation and support. We thank philopatric (Watson 1997) and widespread Derek Hayward for assistance in collecting samples on Golden Eagle. In this species, it may not be effi- Mull. Funding of fieldwork and analyses was provided by cient to incur the maintenance costs of specialist Scottish Natural Heritage, Haworth Conservation and Natural Research. Comments from Christian Rutz, Fab- foraging facilities for individuals which may rizio Sergio, John Quinn and Jeremy Wilson improved encounter wide variation in the prey community an earlier draft. Thanks are also due to Antoni Margalida composition on their territory (e.g. Tjernberg for forwarding an ‘in press’ manuscript on Bearded Vul- 1983, McIntyre & Adams 1999), and whose off- ture diet. spring may need to exploit a different suite of prey to obtain a territory and to breed success- REFERENCES fully (e.g. Penteriani et al. 2005). While the cause–effect relationship between Annett, C.A. & Pierotti, R. 1999. Long-term reproductive out- individual foraging specialization and breeding pro- put in Western Gulls: consequences of alternate tactics in diet choice. Ecology 80: 288–297. ductivity inherent in Watson’s (1997) diet specific- Arroyo, B.E. & Garcia, J.T. 2006. Diet composition influ- ity hypothesis may sometimes play a role (e.g. ences annual breeding success of Montagu’s Harriers Partridge & Green 1987, Golet et al. 2000, Circus pygargus feeding on diverse prey. Bird Study 53: although see Woo et al. 2008), we suggest that for 73–78. Golden Eagles and other ‘generalist’ raptors, the Blackburn, T.M. & Gaston, K.J. 1998. The distribution of mammal body masses. Divers. Distrib. 4: 121–133. available evidence is more consistent with the Bolnick, D.I., Svanba¨ck, R., Fordyce, J.A., Yang, L.H., hypothesis that the abundance and availability of Davis, J.M., Hulsey, C.D. & Forister, M.L. 2003. The prey, and preferred prey in particular, is probably ecology of individuals: incidence and implications of individ- far more influential in affecting reproductive ual specialization. Am. Nat. 161: 1–28.

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