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Individual variability in diet choices is a common feature among animal populations and may explain a significant amount of variation in a suite of life-history and demographic parameters (Sutherland 1996; Krebs & Davies 1997; Schmitz, Beckerman & Litman 1997). Optimal foraging theory suggests consumers will forage in such a way as to maximize net rate of energy intake (Krebs & McCleery 1984). Hence, when faced with the choice between prey species (all other things being equal), consumers should select the one that will deliver highest energy intake and therefore maximum fitness (Charnov 1976). Although initially thought to be of trivial importance (Pyke, Pulliam & Charnov 1977), recent empirical studies have shown that factors such as nutrient content (McKay, Bishop & Ennis 1994; Hassall, Riddington & Helden 2001), digestibility (Prop & Vulink 1992), or a combination of these factors (Amano et al. 2004; Durant, Fritz & Duncan 2004) may substantially affect resource selection. In addition to intrinsic properties of prey items, other nondietary factors including, predation risk (Inger et al. 2006) disturbance (Madsen 1988; Béchet, Giroux & Gauthier 2004) and local prey density, in terms of biomass in a patch (Vickery et al. 1995) may have a strong effect on dietary choice. Indeed changes in biomass by depletion of preferred prey items can cause animals to switch habitats in search of alternate resources (Rowcliffe et al. 2001), and may be the only factor required to explain habitat switches (Vickery et al. 1995).
Generally, studies of resource usage consider conspecifics, within the same population, as ecological equivalents (Bolnick et al. 2003), and thus ignore any between individual variation. Hence patterns of resource utilization often describe dietary choice only at the population level (Durell 2000; Bolnick et al. 2003). However, consideration of average levels of resource utilization within a population may conceal underlying individual variation, which may have important ecological and evolutionary implications (Smith & Skulason 1996; Bolnick et al. 2002; Bolnick et al. 2003; Urton & Hobson 2005; Bearhop et al. 2006). Indeed many populations that appear to be composed of generalists actually comprise a range of individual specialists (Bolnick et al. 2002). Furthermore, demographic segregation in resource utilization, and the subsequent effects of population dynamics (Newton 1998) will be overlooked by population level studies, but may be quantified by examining intrapopulation variation (Bolnick et al. 2002). Decisions made by individuals ultimately determine the population level response; therefore, it is highly desirable that diet selection studies measure the diet of individuals.
Until recently, methodological constraints often rendered it impractical to determine directly the diet of individuals. Direct observation of individuals’ habitat utilization provides limited information on actual diet, as the community composition of a habitat may not reflect prey selection (Rowcliffe, Sutherland & Watkinson 1999; Stephens et al. 2003). The analysis of gut content, regurgitates or faeces have serious limitations (Bearhop et al. 1999; Votier et al. 2003), and may be biased to particular prey types (Hobson, Piatt & Pitocechelli 1994; Russell et al. 1996). In addition these methods only provide data on resource selection during the study period, or immediately prior to analysis and are typically hard to quantify in a truly objective manner.
However, the measurement of stable isotopic ratios of consumer tissues and food offers an alternative approach and has advanced our knowledge of feeding ecology (e.g. Gannes, Martínez del Rio & Koch 1998; Bearhop et al. 1999; Podlesak, McWilliams & Hatch 2005). Consumer tissues are ultimately derived and dietary sources, and are integrated into tissues in a predictable manner, providing a direct record of dietary choice (Hobson & Clark 1992; Matthews & Mazumder 2004; Bearhop et al. 2002 Bearhop et al. 2004). In particular, there are marked differences in the ratios of the stable isotopes of both carbon (13C and 12C) and nitrogen (15N and 14N) between marine and terrestrial biomes. Thus measuring these two isotope ratios (expressed as δ13C and δ15N) in the tissues of consumers can provide an accurate assessment of marine vs. terrestrial prey in the diet (Bearhop et al. 1999; Ben-David, Titus & Beier 2004). Temporally, incorporation of dietary isotopic ratios is a function of the metabolic turnover rate of the tissue. Hence tissues with different turnover times record diet over different temporal periods.
Here we apply these techniques to evaluate the feeding ecology of wintering East Canadian light-bellied Brent geese Branta bernicla hrota (O.F. Müller), wintering at Strangford Lough, Northern Ireland. The population, along with other Brent goose populations, has dramatically increased in size over the last few decades (Robinson et al. 2004). This rise has in turn led to increased depletion of the preferred prey, a marine angiosperm, Zostera spp. (R. Inger, in press), and has led to the birds seeking alternative food sources in different habitats (Mathers & Montgomery 1997) including agricultural land (Merne et al. 1999). This pattern of habitat usage has occurred in other populations of Brent geese in the UK, often causing conflict with agriculture (Charman 1979; Tubbs & Tubbs 1982; Summer & Critchley 1990; McKay et al. 1993; Vickery et al. 1995). Reduced persecution and the ability to adapt to novel resources are probably the key factors underpinning the recent rises in population sizes (Inger et al. 2006). However, the underlying ecological mechanisms driving variability/changes in habitat utilization remain unclear. Models predict that resource guarding has a strong effect on goose aggregations (Rowcliffe et al. 1999), and hence we suspect that the presence of social dominance hierarchies within goose populations may have a powerful influence on the timing and extent of resource utilization. Furthermore, we predict dominant individuals and groups will have greater access to preferred resources in support of the competition hypotheses proposed to explain differential foraging behaviour among individuals (Monaghan 1980; Goss-Custard et al. 1982; Ekman & Askenmo 1984; Gustafsson 1988; Koivula et al. 1994).
In this study we use stable isotopic ratios coupled with multisource mixing models to quantify the prey choices of individuals throughout the overwintering period. We propose that, in order to explain resource utilization, a number factors in addition to maximizing energy intake must be evoked.
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A population level response is ultimately determined by the choices made by individuals. However, surprisingly few studies consider that individuals are not typically equivalent. Here we provide a rare demonstration of how determining dietary preferences of individuals and quantifying intrapopulation variations reveals patterns of resource utilization that are not apparent from population level results.
Here we apply recent advances in multisource stable isotope mixing models to define the dietary preference of individual animals. This approach has a number of advantages over traditional approaches. The stable isotope ratios of a consumer's tissue reflect its diet in a predictable manner, and represent actual assimilation rather than ingestion. The use of two blood components, red blood cells and plasma, with different turnover rates allows us to quantify the diet over two temporal periods. Blood plasma reflect diet over the previous hours and days, while blood cells represent the diet over the previous weeks, hence we have a continuous record of assimilation, rather than a snapshot of ingestion as provided by traditional methodology (Hobson 2005). Furthermore, by sampling individuals we are able to assign data to the demographic or social level. Consequently, we can quantify dietary choice and differential foraging patterns of groups within the population, rather than an overall population level response. While our methodology offers a number of advantages over traditional techniques it may not to suitable in all circumstances. In order to use stable isotope analysis the individuals must first be captured, which is not always possible. In addition in order to quantify diet, the components must be isotopically distinct.
At the population level, our study was in good agreement with previous studies recording a general movement from feeding in marine habitats early in the winter to terrestrial habitats as the winter progresses. However, in contrast to other studies, we found no evidence for an abrupt habitat switch (between marine and terrestrial habitats), but rather a gradual decrease in the utilization of prey type in one habitat, with a concurrent increase in prey from another habitat. When birds began to utilize a new habitat it is not necessarily coincidental with abandonment of previous habitats. Rather, birds utilized multiple prey types, and multiple habitats within the same temporal period. In addition, by quantifying intrapopulation variability, we identified demographic differences in timing and extent of resource use. Generally, the data describe a strong preference for Zostera spp. in early winter, which declines throughout the winter. By mid-winter, the green algae Enteromorpha spp. and Ulva lactuca became more important, although the results from isosource give a wide distribution of possible contributions to the diet, so that although the quantitative importance of these food sources remains unclear, it is likely to be variable. For the remainder of the winter terrestrial grasses became the most important food source in the diet, accounting for over 80% of the diet by April.
Perhaps of most interest is that not all individuals changed their foraging habitats in the same way. Juvenile individuals had significantly lower (more terrestrial) isotopic ratios than adults, suggesting that throughout the winter juveniles were utilizing terrestrial habitats earlier, and to a greater extent than adult birds. It may be argued that lower isotopic ratios of juveniles may, to some extent, be due to differential fractionation between adults and juveniles, which are still growing. However, this seems unlikely as when birds are purely feeding on Zostera spp. (October 2005) there are no significant differences in either isotopic ratio between adults and juveniles, indicating the absence of any age-related fractionation effect.
That juveniles appear to be utilizing terrestrial prey types earlier than adults, suggest that competitive ability is one factor that may produce patterns of variability in habitat use among individuals, or demographic groups. This is consistent with the finding of Tubbs & Tubbs (1982) who first reported terrestrial feeding in juvenile dark-bellied Brent geese. In this study it was found that terrestrial feeding was stimulated by the presence of juvenile birds in the flock.
The movement of individuals or groups of individuals between habitats and prey choice decisions are likely to be influenced by a number of factors, including the ability to maximize energetic intake, nutritional value of food, protein content (particularly for herbivores), and the suitability of the habitat with regards to predation risk and tradition. Previous studies have suggested a variety of mechanisms influencing diet selection in overwintering Brent geese. Probably the most influential factor is resource depletion (Vickery et al. 1995), which may cause birds to move habitats, although diet selection within habitats may be due to nutritional requirements (Summers et al. 1993; McKay et al. 1994; McKay et al. 2001).
At Strangford Lough, of the four major food types, our results suggest that, in terms of nutritional content, Zostera spp. and terrestrial grass should be the most desirable prey items. Our use of nitrogen and carbon content as proxies for protein and carbohydrate content are consistent with the values of Mathers & Montgomery (1997), who assessed the nutritional value of Brent goose food sources using standard techniques. Indeed, if geese were selecting prey items purely on nutritional content they would select terrestrial grasses over Zostera spp., with terrestrial grasses having a higher carbon and nitrogen content that Zostera spp. In addition, if diet choice were based on biomass we would expect terrestrial grasses to be the preferred dietary item. However, terrestrial grasses have a much higher fibre content, compared with marine food sources (Mathers & Montgomery 1997) decreasing digestibility, which (considering the poor digestive efficiency of geese), may be a major factor in prey selection. Factors other than the intrinsic properties of prey items are also likely to influence prey choice. Zostera spp. is the traditional prey choice for Brent geese, which have historically fed on Zostera spp. beds in preference to other food sources, with terrestrial feeding unreported until the 1970s (Charman 1979; Tubbs & Tubbs 1982). The risk of predation also has a strong influence on the distribution of Brent geese, with intertidal areas that harbour Zostera spp. beds being considered a lower risk habitat than terrestrial habitats (Inger et al. 2006).
That Zostera spp. is the preferred prey choice appears clear, as it constitutes the majority of the diet after migration from their Canadian breeding grounds. The transition from Zostera spp. to alternate food sources can be explained in terms of depletion. Empirical and modelling studies have found a strong relationship between bird numbers and Zostera spp. depletion (Inger et al. in press). In agreement with Vickery et al. (1995), depletion of biomass to levels where foraging becomes unprofitable is likely to be the main cause of changes in prey exploitation. Indeed density dependence appears to take effect very early in the winter, with levels of Zostera spp. falling significantly during October. However, we found no clear switch between habitats or prey items, more a gradual change in diet composition during the winter, the timing of which was strongly influenced demographic factors.
Previous studies have suggested that Brent geese move down a profitability gradient based on food preference or maximizing energy intake (Charman 1979; Mathers & Montgomery 1997). However, since geese started to utilize terrestrial grasses in the 1970s this resource has become increasingly important, representing the main food source during late winter and spring, and the main resource prior to migration and during spring staging in Iceland. Indeed the birds show substantial weight gains in spring due almost exclusively due to terrestrial foraging. Brent geese have clearly adapted well to terrestrial feeding and this is probably an important factor in recent increases in the populations of all races of Brent geese in western Europe. If we are to effectively conserve these populations and reduce the conflict with agriculture it is important that we make decisions based not only on conserving traditional intertidal feeding areas, but also areas of terrestrial grassland utilized by geese.
In conclusion we have demonstrated how resource utilization by individuals can be determined using stable isotope ratios coupled with multisource mixing models. These techniques require some a priori knowledge of the study system, and should therefore build on, not replace traditional methods for determining dietary choice. However, by accurately determining the dietary choice of individuals over predictable time-scales we are able to further our understanding of the complex relationships between consumers and resources, and how the choices made by individuals determine a population level response.