Keywords: Resource partitioning, competition, dietary specialization, shorebirds, biofilm, microphytobenthos
INTRODUCTION
Dietary specialization – the tendency of individuals to forage on specific prey items that differ from the prey of other individuals in their population – is common in animals and has important implications for individual fitness, inter- and intraspecific competition, and the adaptive potential of a species (Bolnick et al., 2003; Durell, 2000). Age and sex play a particularly important role in influencing dietary specialization, which has been well-studied in the shorebirds and their allies (Charadriiformes; Durell, 2000, 2003; Jehl & Murray, 1986; Székely, Freckleton, & Reynolds, 2004).
Age-related factors including morphology, social status, and acquired skills can influence dietary specialization in shorebirds (Durell, 2000, 2003). Juvenile birds tend to have smaller bodies and shorter bills than adults, and, in some shorebird species, juveniles take smaller prey (Fasola, Canova, & Biddau, 1996; Goss-Custard & Durell, 1987; Puttick, 1978). Juvenile birds may also be excluded from foraging in areas with the most profitable prey because of their subdominant social status (Durell, 2003). In addition, dietary differences between juveniles and adults could arise because juveniles lack the skill needed to acquire and handle certain prey (Durell, 2000, 2003).
Morphological differences between sexes can also influence dietary specialization in shorebirds. Many shorebirds exhibit sexual size dimorphism (SSD) in body size and bill length (Jehl & Murray, 1986; Székely et al., 2004; Székely, Reynolds, & Figuerola, 2000). Sexual size dimorphism in body size is thought to be driven by sexual selection that occurs during the breeding season, but it may also have energetic consequences that impact prey selection because larger-bodied birds require more calories to sustain their greater basal metabolic rates (Jehl & Murray, 1986; Lindström & Klaassen, 2003; Székely et al., 2004, 2000). In contrast, SSD in bill length often exceeds that of other body parts and is thought to be a consequence of competition for food during the non-breeding season (Jehl & Murray, 1986; Székely et al., 2004, 2000). Several studies have demonstrated that bill size dimorphism in shorebirds results in resource partitioning between sexes (Alves, Gunnarsson, Potts, Sutherland, & Gill, 2013; Catry, Alves, Gill, Gunnarsson, & Granadeiro, 2012; Recher, 1966; Stein, Fernández, De La Cueva, & Elner, 2008).
The western sandpiper (Calidris mauri ) is a small (22-35 g) migratory shorebird that exhibits female-biased SSD with a 5% greater body size and a 15% longer bill in females compared to males (Jehl & Murray, 1986; Page & Fearis, 1971). Along the Pacific coast, the non-breeding range of the species extends from British Columbia, Canada to Peru (Franks, Lank, & Wilson, Jr., 2020). The western sandpiper is considered a generalist with a diverse diet that includes benthic invertebrates and biofilm – a thin layer of microphytobenthos, bacteria, and detritus encased in a polysaccharide-rich matrix of extracellular polymeric substances that forms on the surface of mudflats at low tide (Stal, 2003; Underwood & Paterson, 2003). Evidence suggests that sandpipers are able to selectively feed on the microphytobenthic component of biofilm, though they inevitably ingest some whole biofilm (Kuwae et al., 2008).
Previous studies have demonstrated that western sandpipers partition resources among sexes and ages at a broad scale through differential migration and at finer scales through differences in foraging behavior and microhabitat use between sexes (Fernández & Lank, 2008; Mathot & Elner, 2004; Mathot, Smith, & Elner, 2007; Nebel, 2005; Nebel et al., 2002). In adults, shorter-billed males spend a significantly greater proportion of time pecking to consume benthic epifauna, and they winter in northern areas where prey are more abundant at the sediment surface (Fernández & Lank, 2008; Mathot & Elner, 2004; Mathot et al., 2007; Nebel, 2005; Nebel et al., 2002). In contrast, longer-billed females spend more time probing for infauna, and they winter in more southerly areas where deeper prey are more abundant (Fernández & Lank, 2008; Mathot & Elner, 2004; Mathot et al., 2007; Nebel, 2005; Nebel et al., 2002). Juveniles disproportionately occupy northern and southern non-breeding areas, with juveniles from southern areas opting to reduce feather wear and remain in the non-breeding area during their first summer (Nebel et al., 2002; O’Hara, Fernández, Becerril, De La Cueva, & Lank, 2005). The dearth of juveniles in the center of the non-breeding range has been attributed to the alternative migration strategies of juveniles; however, juveniles may also be excluded from the center of the range by adults because of their subdominant social status (Nebel et al., 2002; O’Hara et al., 2005).
Biofilm consumption varies among individuals and may differ among sexes and ages (Jardine, Bond, Davidson, Butler, & Kuwae, 2015). Smaller-bodied shorebird species are better adapted to graze biofilm, and they can obtain a larger portion of their daily energy budget foraging on biofilm compared to larger-bodied species (Kuwae et al., 2012). Further, Elner, Beninger, Jackson, & Potter (2005) suggested that shorebirds with shorter bills should be better mechanically adapted to consume biofilm than shorebirds with longer-bills. These adaptations related to body mass and bill length have facilitated interspecific niche differentiation among shorebird species and may drive intraspecific resource partitioning within western sandpipers (Kuwae et al., 2012). Accordingly, male western sandpipers, with smaller bodies and shorter bills, may be better adapted to biofilm grazing than females. In addition, age-related differences in diet are poorly understood in western sandpipers, but juveniles may be more reliant on biofilm because they have shorter bills, have lesser mass, lack prey handling experience, or are excluded from foraging on more profitable invertebrate prey by dominant adults (Durell, 2000, 2003; Fernández & Lank, 2006).
During the non-breeding season, dietary specialization among western sandpipers would allow sandpipers to partition resources and reduce inter- and intraspecific competition for prey; however, specialization may only be necessary when competitive pressure is intensified by high population densities or increased energetic demands (Svanbäck & Bolnick, 2005). Diet composition in western sandpipers does appear to vary during the non-breeding season. In mid-winter (January/February), Franks, Fernández, Hodkinson, Kyser, & Lank (2013) did not detect resource partitioning between male and female western sandpipers sampled throughout the non-breeding range. In contrast, Beninger, Elner, Morançais, & Decottignies (2011) demonstrated that the trophic position of western sandpipers declined in spring, suggesting that birds shifted their diets to consume more biofilm during their breeding migration. In spring, western sandpipers undergo changes in physiology and organ morphology to prepare for migration (Egeler & Williams, 2000; Guglielmo & Williams, 2003; Stein, Place, Lacourse, Guglielmo, & Williams, 2005; Williams, Warnock, Takekawa, & Bishop, 2007). These changes facilitate hyperphagy, allowing birds to consumer larger quantities of food to cope with the energetic demands of migration. In addition, population densities at some non-breeding areas may increase in spring because sandpipers from southern areas begin their breeding migration earlier than birds from northern areas (Butler, Kaiser, & Smith, 1987; Nebel et al., 2002). Both hyperphagy and increased population densities could lead to prey depletion that would increase competition, and, thus, the need for dietary specialization, at some non-breeding areas in spring.
To evaluate the role of age- and sex-related dietary specialization in driving resource partitioning, we quantified the contribution of biofilm, microphytobenthos, and invertebrates to the diets of western sandpipers of different ages and sexes during mid-winter (January/February) and at the onset of the breeding migration (April). We hypothesized that juvenile males would consume the greatest amount of biofilm and microphytobenthos because males have shorter bills and lesser mass than females, and juveniles are expected to have less prey handling experience than adults. We also hypothesized that biofilm and microphytobenthos consumption would be greater in spring at the onset of migration than during mid-winter based on the expectation that sandpipers consume biofilm and microphytobenthos to help fuel their migration and reduce competition during periods when high densities of birds occupy foraging sites.
MATERIALS AND METHODS