Prey type and foraging ecology of Sanderlings Calidris alba in different climate zones: are tropical areas more favourable than temperate sites?

Study sites

We studied foraging ecology of Sanderlings at Vlieland, an island in the Wadden Sea in the Netherlands (53°16N, 4°55E), and at the beach of Esiama (4°56N, 2°21W), situated 300 km west of Accra, Ghana (Fig. 1). At Vlieland, Sanderlings were studied along a 6 km stretch of the North Sea beach for one season between September and November 2007. In Ghana, we studied Sanderlings for two seasons from mid-January to mid-March (2008) and from January to early February (2009). Round trip migration distances from their arctic breeding sites to non-breeding sites in the Netherlands and Ghana approximate 6,300 km and 16,000 km, respectively. Sanderlings remain at temperate non-breeding sites from mid-July to late May, and at tropical non-breeding sites from mid-August until late April (Reneerkens et al., 2009; Lemke, Bowler & Reneerkens, 2012; Ntiamoa-Baidu et al., 2014). Our study sites differed extensively in climatic and site characteristics (Table 1). The weather in the Netherlands in autumn and winter was unstable and heavy storms were not uncommon during this period. Esiama beach (Ghana) stretches over 13 km and is enclosed by the estuaries of two rivers, and the shore was lined with coconut tree plantations (Ntiamoa-Baidu et al., 2014). Weather in Esiama was stable with few heavy rain showers and little variation in ambient temperature. Day length was very similar between the Netherlands and Ghana during our study period, averaging 11.25 and 11.95 h, respectively. As night foraging is common amongst shorebirds (Robert & McNeil, 1989; Nol et al., 2014), we extrapolated all estimates of foraging time and energy intake over a 24 h period. Foraging efficiency at night may be lower for visual foragers such as Sanderlings, but we could not take this into account, as no estimates are available. We considered our two sites valid for comparison of Sanderling foraging ecology as both consisted of beach habitat (see e.g., Piersma, de Goeij & Tulp (1993) for issues of comparison).

We spent a total of 37 and 36 field days in the Netherlands and Ghana, respectively, covering 274 and 260 h of observation for time budget estimates. Our observations were spread out over the daylight hours, resulting in 41% of observations between 6 am and 12 noon, and 59% between 12 noon and 6 pm. To monitor prey intake, we observed Sanderlings foraging for a total of 520 and 490 min in the Netherlands and Ghana, respectively. All observations were conducted on wild Sanderlings in their natural environment and we did not handle birds for our study. Therefore, no permission from the Animal Ethics Committee of the University of Groningen (DEC-RUG) was required.

Invertebrate sampling

We studied the marine benthic invertebrate community to assess variation and availability of different prey species for Sanderlings. In September/October 2008 (Netherlands) and January 2009/2010 (Ghana), we collected a total of 181 and 614 samples of benthic invertebrates in the upper 20 cm of marine sediment, using sediment cores with inner diameters of 14.9 cm (0.0174 m²) and 12.5 cm (0.0123 m²). We collected benthos at 100 m intervals at the tide line, where Sanderlings forage. In 2008, we sampled over the whole length of both study areas seven times during different stages of the tidal cycle, using the tidal variation to obtain samples at different elevations. We also sampled the Ghanaian study area twice in 2010 to examine inter-annual variation in the benthic invertebrate community. We sieved samples over 1 mm mesh size on site and benthic invertebrates were frozen until further analyses. We extrapolated benthic invertebrate densities and energetic value to m².

To assess invertebrate availability to Sanderlings, we measured burying depths of 300 shellfish in Ghana by extracting a core and systematically scraping off vertical layers of sediment. Depth of shellfish exposed was measured from the top of the core to the middle of the shell. We were unable to measure burying depths of the polychaetes in the Netherlands, because they responded to our presence by quickly retreating deep into the sediment.

Benthic invertebrates were identified to species level, counted and measured to the nearest mm. We dried invertebrate samples at 60 °C for two days, determined ash-free dry mass (AFDM) by subtracting ash weight from dried sample weight and determined ash mass using the end product of processing the samples in a bomb-calorimeter. We used a bomb-calorimeter to estimate energy content of our polychaete and other invertebrate samples. Where possible, samples were processed as duplicates to assess measurement precision, and values were averaged. For shellfish, we used a fixed value of 22 kJ g⁻¹ AFDM, in further analyses due to inconsistencies in energy measurements (Zwarts & Wanink, 1993). We calculated prey quality following Yang et al. (2013), using: ${\displaystyle Q=d\times a\times \frac{\mathrm{AFDMflesh}}{\mathrm{DMshell}}}$ where d is the energetic density of the flesh (22 kJ g⁻¹ AFDM) and a is digestion efficiency (0.82) (Castro et al., 2008; Yang et al., 2013). Size differences between shells were not taken into account, as the majority (>90%) of shells collected measured between 0.5 and 0.7 cm.

Time budgets

We conducted daily surveys covering the entire study area and recorded time, place and behavior of each individual encountered. We categorized time of observations into hours before and after low tide, enabling us to relate behavior to the tidal cycle. Our ethogram included: (1) Foraging: birds were actively foraging and ingesting food; foraging included both probing and pecking, (2) Resting: birds were not foraging, but stood or lied down with little or no apparent movement, (3) Preening: birds actively preened and/or bathed, and (4) Locomotion: birds were actively moving between locations. Locomotion included all running and flying between foraging and roosting sites. Based on the time birds spent exerting different behaviors over the period of each survey, we calculated daily time budgets of Sanderlings at both study sites.

Prey intake

We observed individual Sanderlings for up to 10 min through a spotting telescope to determine food intake rate. To ensure independence of observations among foraging birds, we focused our observations on color-banded individuals and avoided recording measurements from the same individuals within the same flock on the same day. We measured prey intake rate, and identified prey type when possible. We recorded successful ingestion of large-bodied prey by counting swallowing movements of the foraging bird, identified by a fast upward movement of the head. Energy intake was calculated as the weighted average of intake rates observed from Sanderlings foraging during the whole tidal cycle and extrapolated to energy intake/hour, using known energy contents of prey items. Due to distance and the high foraging speed of Sanderlings, prey could only be classified as polychaete or non-polychaete during field observations. We calculated prey intake rates by multiplying the energy values we determined for polychaete and non-polychaete prey by the observed prey ingested during timed foraging observations. For polychaete prey, energetic content estimated we included polychaetes >20 mm in size, as we were unable to observe ingestion of smaller polychaetes. We did not differentiate between polychaetes >20 mm in our calculations, as we could not accurately estimate prey size in the field.

As a gauge for the energy requirements at the two sites, we used the empirical value for DEE measured in Texas in winter (135 kJ/day) by Castro, Myers & Ricklefs (1992) for the Netherlands. Ambient temperature during the Texas winter was comparable to average autumn temperatures in the Netherlands during our study (10 °C and 14 °C, respectively). As an approximation of DEE in Ghana we used 100 kJ/day, which was measured for Sanderlings spending the non-breeding season in Panama. Temperatures between Panama and Ghana are also comparable (27 °C and 32 °C on average) and are above the lower critical temperature of 23 °C estimated for Sanderlings (Kersten et al., 1998).

Statistics

We used a Generalized Linear Model to compare proportion of foraging Sanderlings between sites and at different times of the tidal cycle. Our full model is shown below: ${\displaystyle \%\mathrm{Foraging}\sim \mathrm{Site}+\mathrm{Tide}+{\mathrm{Tide}}^2+\mathrm{Site}\ast \mathrm{Tide}+\mathrm{Site}\ast {\mathrm{Tide}}^2}$ Tide was expressed in hours before and after low tide. We used Tide² because we expected a quadratic relationship between proportion of birds foraging and time in the tidal cycle. All statistical analyses were conducted using the R environment for statistical programming version 3.1.0 (R Development Core Team, 2010). All means are presented ±1SE.

Food availability and quality

Prey type, abundance and energetic content differed extensively between sites. In the Netherlands, 94.5% of the benthic species in our samples consisted of the polychaete Scolelepis squamata, with the amphipod Haustorius arenarius (4.5%) as the second most abundant prey species. The biomass of sanderling prey at the beach in the Netherlands was 7.4 ± 1.6 g AFDM m⁻², and invertebrate distributions were positively correlated with the timing relative to low tide (Fig. 2). The average energy values of these two invertebrate species were 40.5 ± 0.41 kJ g⁻¹ and 20.3 ± 0.04 kJ g⁻¹ AFDM, respectively. For AFDM in the Netherlands, time within the tidal cycle explained 64% of the variation in biomass (R² = 0.64; Fig. 2A). The highest densities of S. squamata were found furthest away from the high tide line, and thus only available during low tide. Average AFDM g⁻¹ sample for polychaetes of different sizes (20 mm–>50 mm) varied between 0.75 and 0.88, with an overall average of 0.83 ± 0.01 g AFDM g⁻¹ sample. These intake rates are only based on the ingestion of polychaetes, as we were unable to identify non-polychaete prey in the field. Average polychaete prey capture rate was 0.075 polychaete s⁻¹ during our 10 min intake observations. The benthic fauna of the Ghana beach was dominated by the bivalve Donax pulchellus which accounted for over 95% in numbers of all organisms found in the samples. Sanderlings were observed to feed almost exclusively on this bivalve. Hydrobia ulvae was the second most abundant species in Ghana with highest densities further away from the shore than D. pulchellus. D. pulchellus were distributed over the whole width of the beach with an average energetic content of 77 g AFDM m⁻², but occurred in highest densities in a 1–3 m wide shell bank (up to 170,000 individuals m⁻²/1,146 g AFDM m⁻²), that was present in both 2008 and 2009 and clearly visible. Although we sampled benthos up to a depth of 20 cm, we only detected invertebrates in the top sediment layer. D. pulchellus had a burying depth of 1.09 ± 0.72 cm, and were thus always available to the Sanderlings, which have bill lengths of 2.5 cm. Sanderlings in the Netherlands were observed to feed on S. squamata and small prey unidentifiable by sight by us. Polychaetes accounted for 45% of successful prey intakes, and the other 55% was composed of small, unidentifiable prey items. Prey quality of D. pulchellus was estimated at 4.59 ± 0.12 kJ g⁻¹ DM_shell, and quality of S. squamata and H. arenarius were 110.6 ± 1.9 and 82.6 kJ g⁻¹ DM_shell, respectively. We processed all H. arenarius in a single sample, thus cannot provide a SE estimate.

Sanderling time budgets and prey intake

Average Sanderling densities were 34 ± 0.7 birds km⁻¹ in the Netherlands and 214 ± 2.6 birds km⁻¹ in Ghana, respectively. We estimated density over a one-dimensional space that covered the length of the beach. In the Netherlands, Sanderlings were spread out on the beach or in small groups (<10 birds) while in Ghana they occurred in large flocks (>50 birds). Time budgets of Sanderlings during the non-breeding period in the Netherlands and Ghana differed predominantly in time spent foraging and resting (Fig. 3). We adjusted time budget calculations to average day lengths in the Netherlands and Ghana during our study period. In the Netherlands, the Sanderlings’ main activity was foraging, which comprised 68.3% (17.8 h) of their time, while in Ghana, Sanderlings foraged 35.1% (9.0 h) of the time. In Ghana, 56.4% of the birds observed were resting, opposed to 13.6% in the Netherlands. The interaction Site*Tide and Site*Tide² in our model were not significant and the model we used for our analyses only included Site and Tide². The proportion of Sanderlings observed to be foraging differed significantly between sites (GLM, t₂₃ = 4.0, p < 0.0007), but no significant correlation between the proportion of foraging birds and the stage in the tidal cycle was found at either site (GLM, t₂₃ = − 0.576, p = 0.57). Preening and locomotion accounted for 4.0–8.1% and 0.5–14.1% of daily effort in the Netherlands and Ghana. Foraging and resting was independent of the tidal cycle in Ghana, but in the Netherlands the percentage of foraging birds appeared to show a slight increase around low tide, though not significant (Fig. 4).

The average caloric intake of Sanderlings was estimated to be 0.13 mg AFDM s⁻¹ (2.28 J s⁻¹) in the Netherlands compared to 1.64 mg AFDM s⁻¹ (36.27 J s⁻¹) in Ghana. For Sanderlings in the Netherlands there was a tendency for a positive correlation between foraging time and benthos availability (ANOVA, F₂ = 3.166, p = 0.105), while in Ghana proportion of foraging birds was independent of the benthos availability (ANOVA, F₂ = 0.004, p = 0.951) (Fig. 5).