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