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Shorebirds Forage Disproportionately in Horseshoe Crab NestDepressionsAuthor(s): James D. Fraser, Sarah M. Karpanty and Jonathan B. CohenSource: Waterbirds, 33(1):96-100. 2010.Published By: The Waterbird SocietyDOI: http://dx.doi.org/10.1675/063.033.0111URL: http://www.bioone.org/doi/full/10.1675/063.033.0111

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96

Shorebirds Forage Disproportionately in Horseshoe Crab Nest Depressions

JAMES D. FRASER*, SARAH M. KARPANTY AND JONATHAN B. COHEN

Department of Fisheries and Wildlife Sciences, Virginia Tech, Blacksburg, VA, 24061-0321, USA

*Corresponding author; E-mail: Fraser@vt.edu

Abstract.—Horseshoe Crab (Limulus polyphemus) eggs are an important shorebird food during the Delaware Bayspring stopover, and shorebird management plans aim to increase and monitor this resource. If shorebirds focustheir foraging on Horseshoe Crab nesting depressions they may find richer food supplies than if they forage ran-domly on the beach. The amount of shorebird sign in quadrats centered on Horseshoe Crab nest depressions wascompared with the amount of sign in paired beach areas with no Horseshoe Crab nests. Horseshoe Crab nest de-pressions had more pecks, probes, digit marks, Ruddy Turnstone excavations, Horseshoe Crab eggs and a greatercoverage by shorebird sign than paired beach plots with no Horseshoe Crab nests. Foraging disproportionatelywithin Horseshoe Crab nesting depressions may facilitate the rapid mass gain needed to prepare shorebirds fortheir flight to the breeding grounds. Horseshoe crab egg monitoring currently estimates mean egg abundance perbeach. However, birds are able to find patches with high egg densities even when foraging on beaches with loweraverage densities. Received 27 January 2009, accepted 29 November 2009.

Key words.—Arenaria interpres, Calidris alba, Calidris alpina, Calidris canutus, foraging, Horseshoe Crab, Limuluspolyphemus, Red Knot, Ruddy Turnstone, shorebirds.

Waterbirds 33(1): 96-100, 2010

During northward migration, tens ofthousands of shorebirds stop in DelawareBay in May and June and feed primarily oneggs of spawning Horseshoe Crabs (Limuluspolyphemus). Semipalmated Sandpipers(Calidris pusilla), Ruddy Turnstones (Arenar-ia interpres), Red Knots (Calidris canutus),Sanderlings (Calidris alba) and Dunlin(Calidris alpina) are the most common spe-cies (Clark et al. 1993).

Most Horseshoe Crabs come ashore dur-ing the night high tide near the full and newmoons. Female crabs dig nest burrows anddeposit egg masses containing an average of3,650 2-3 mm-diameter eggs at 0-20 cm be-low the beach surface (Shuster and Botton1985; Brockman 1990; Botton et al. 1994).They depart, leaving a semi-circular depres-sion in the sand. On most days after spawn-ing, a line of nest depressions stretchesacross the beach just below the high watermark, parallel to the water’s edge. Some crabeggs are distributed on the beach becausethey are dislodged from the egg mass by thelaying female, because a laying female exca-vates the eggs of another crab, or due toscouring by waves, while others remain bur-ied (Botton et al. 1994; Kraeuter and Fegley1994; Jackson et al. 2002).

Food intake rate is important to shore-birds stopping in Delaware Bay because theyhave a limited time to store the fat requiredfor their flight onto the breeding grounds(Atkinson et al. 2007). Gillings et al. (2007)showed that birds can ingest surface eggsfaster than buried eggs, and that ingestionrate is positively correlated with egg density.Using functions derived from feeding exper-iments, they predicted that Red Knots couldmeet their daily energy requirements byfeeding for 15 h d-1 on surface eggs at 360eggs m-2 or buried eggs at 19,200 eggs m-2.They referred this to mean egg densities oneleven beaches and noted that only sevenbeaches had mean egg densities

≥19,200eggs m-2, and concluded that “the opportuni-ties for feeding on buried eggs are limited.”

We agree that this conclusion is warrant-ed if eggs are distributed uniformly or ran-domly and if birds cannot detect patches ofhigh egg density. But if high density patchesexist, and birds can readily detect thosepatches, birds may be able to forage in highegg densities more often than suggested bybeach average densities. One place wherebirds may be able to find high egg densitiesis Horseshoe Crab nest depressions. We test-ed the hypothesis that shorebirds preferen-

SHOREBIRD FORAGING PATTERNS 97

tially foraged in Horseshoe Crab nest depres-sions in comparison to nearby beach areaswithout visible crab nest depressions.

METHODS

The hypothesis that shorebirds use Horseshoe Crabnest depressions preferentially was examined by com-paring evidence of shorebird foraging activity (birdfootprints, peck and probe marks, and Ruddy Turn-stone excavations) in nest depressions with similar evi-dence in paired control plots. Control plots had noevidence of crab nesting, were the same distance fromthe water as the nesting depression, and were

≥ 75 cmfrom the nest plot. If shorebirds were not using Horse-shoe Crab nests preferentially, the number of bird foot-prints and peck, probe, and excavation marks should besimilar in nest depressions and control plots.

The study was conducted on six Delaware Bay beach-es (Cook’s, Kimble’s, Pierce’s Point, Reed’s, Slaughter,and Ted Harvey Beaches) known for Horseshoe Crabspawning and shorebird use (Smith and Michels 2006).On each sampling occasion, a crab nesting depressionwas randomly selected for examination. Thereafter, ev-ery fifth crab nest depression on a path parallel to thewater was examined. Sampled nest depressions werespaced such that all nest depression quadrats were > 2 mapart. After examining a crab nest depression, weplaced a control plot 2 m away at the same distance fromthe water as the nest. If there was a crab nesting depres-sion at the 2-m mark, the control quadrat was placedfurther down the beach so that it was at least 0.75 mfrom the edge of the nearest crab nesting depression. Amaximum of ten nesting depressions and ten controlswere examined on any beach on any day.

A 0.75 m

× 0.75 m quadrat was centered on each nestdepression and control point. Within this quadrat, eachhole in the substrate that was made by a digging, peck-ing, or probing shorebird was counted. Because bill-cre-ated holes and holes created by shorebird toes weresometimes indistinguishable, we summed all holes andassumed they constituted an index to shorebird activityin the quadrats. In addition to probing in the sand, Rud-dy Turnstones often excavate holes. We counted theseseparately. The percent of the quadrat covered by signsof bird activity (bird footprints, pokes, and excavations)was visually estimated. Two people independently as-sessed each site at the same time. The independent as-sessments of number of holes and excavations and totalcoverage by bird sign were averaged. We excavated a cy-lindrical hole 25 cm in diameter in the center of the de-pression or control quadrat and recorded the numberof Horseshoe Crab eggs in the top 5 cm of the excavatedcylinder.

Statistical Analyses

We estimated mean responses using generalized lin-ear mixed models where the fixed effects were treat-ment (nest vs. control) and block (sampling occasion,i.e. a beach on a particular day) and the random effectwas plot (the nest-control pair). The block variable wasincluded to control for variance associated with envi-ronmental variables (e.g. tidal stage, time of day, weath-er, intensity of crab spawning, density of foraging birds).Analyses were performed in SAS version 9.1.3 (SAS In-

stitute 2004). Continuous data that conformed to as-sumptions of normality and heteroscedasity wereanalyzed with a linear model, and count data were ana-lyzed with a Poisson model, except for the number ofeggs in the top 5 cm of sand, which was analyzed with anegative binomial model because the negative binomialwas a better fit (AICc negative binomial model = 860 vs.AICc mixed Poisson model = 1677) due to many zerovalues that led to overdispersion.

RESULTS

Sixty-six pairs of Horseshoe Crab nest de-pressions and controls were examined dur-ing eight sampling occasions between 12May and 1 June, 2005. All sample plots wereavailable to birds from first light until sam-pling began. Sample collection began 3.3-5.2(mean = 4.1 hours) hours after sunrise.From sunrise to the beginning of samplingthe plots were exposed for 0.0-5.1 h of fallingtide (mean = 2.4 h) and 0.0-3.7 h of risingtide (mean = 1.3 h).

We found egg masses in 55 of 66 nestplots and 34 of 66 control plots (

χ21 = 15.2, P

< 0.01). Compared to control plots, nestplots had more shorebird-created holes,Ruddy Turnstone digs and Horseshoe Crabeggs in the top 5 cm (Table 1). Compared tocontrol plots, a higher percentage of nestplots were covered by shorebird holes andruddy turnstone excavations (Table 1).

DISCUSSION

The greater concentration of shorebirdactivity sign in the Horseshoe Crab nest plotscompared to the control plots supports thehypothesis that shorebird foraging activitywas higher in crab nest depressions thanelsewhere on the beach. The greater num-ber of eggs in the top 5 cm of the crab nestscompared to control plots indicates thatbirds foraging in Horseshoe Crab nest de-pressions were likely to find richer food sup-plies than birds foraging on random beachplots. The range of Ruddy Turnstone excava-tion depths in nest plots was sufficient forthem to find entire egg masses, an energeticreward that may offset the cost of deep exca-vations.

Our observations each day took placewell after the beginning of shorebird forag-

98 WATERBIRDS

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Num

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the

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(16

77).

SHOREBIRD FORAGING PATTERNS 99

ing. Because foraging birds favored Horse-shoe Crab nest depressions, the differenceswe observed in egg numbers between nestdepressions and control quadrats were prob-ably less than the differences that existed atthe beginning of the foraging day at twilight.Thus, the benefits conveyed by the foragingpattern described here are understated.

Migrating shorebirds arrive on the Dela-ware Bay in early May and must depart fortheir nesting areas by early June to arrive intime for the short northern breeding season(Clark et al. 1993; Atkinson et al. 2007). Thus,they must gain weight rapidly during theDelaware Bay stopover. Foraging rates ofshorebirds ingesting Horseshoe Crab eggsare positively related to egg densities at thechosen foraging sites (Gillings et al. 2007).The condition of birds arriving at theirnorthern breeding sites may influence theirability to survive early summer inclemencyand to transform their physiological statefrom a migration state to a breeding state(Morrison et al. 2005). Thus, the ability tofind areas with the highest egg densities, asindicated in this study, is likely an adaptivetrait.

We did not check nests before shorebirdsarrived to forage, so we do not know howmany eggs were visible on the surface at thattime. Whether birds are initially attracted bythe morphology of the nest depression or byvisible surface crab eggs within the depres-sions remains to be discovered. Likewise, therole of social facilitation (sensu Pomara et al.2003) in promoting disproportionate use ofthe crab nest depressions is unknown. We of-ten observed Red Knots and Sanderlings for-aging in and around Ruddy Turnstone exca-vations as the Turnstones were actively dig-ging. Gillings et al. (2007) experimentallymanipulated Horseshoe Crab egg densitiesin trays, and found that the number of shore-birds using trays and the bird-time spent onthe trays was positively correlated with trayegg density. Since the area and dimensionsof their trays were similar across egg densi-ties, this suggests that individual bird deci-sions to enter, stay on, or leave trays werebased either on individual experiences withegg densities or on information gained from

watching other birds, not on the images ofthe trays themselves.

Birds may not be able to take advantageof the high density of crab eggs in nests everyday. On windy days, the depressions quicklyfilled in. On such days the value of eggsfound in the swash zone or in windrows onthe beach may be relatively more importantthan on calm days. However, the same windsthat cover nest depressions may also createwaves that unearth buried eggs (Kraeuterand Fegley 1994; Jackson et al. 2002; Nord-strom et al. 2006). The annual variation inthis phenomenon is unknown. In this studyyear, 2005, the Horseshoe Crab spawn waslargely delayed because of stormy weather(Smith and Michels 2006), and peak Horse-shoe Crab spawning did not occur until afterthis study was completed. Thus, there werelikely fewer crab eggs on the study beachesthan in other years (Kraeuter and Fegley1994). In years with more abundant Horse-shoe Crab spawning, there might be moreeggs on the surface, and the preferential useof nest depressions for foraging might be lesspronounced.

The clumped distribution of crab eggs inthe swash zone and windrows and the fo-cused nature of shorebird foraging on crabnest depressions, wrack lines and the swashzone (Nordstrom et al. 2006; this study), sug-gest that even when mean densities on abeach are low, birds may be able to find andforage in very high-density patches. Thus,while random sampling of beaches (Pooler etal. 2003) can provide useful data on large-scale trends in overall egg abundance towhich the availability of eggs to birds may becorrelated, assessment of whether birds areable to forage on egg densities high enoughto meet their daily energy requirements(Gillings et al. 2007) requires an assessmentof the distribution and abundance of highegg-density patches, and the density of eggstherein.

ACKNOWLEDGMENTS

We thank the National Marine Fisheries Service forfunding. We thank N. Avissar, C. Olfenbuttel, J. Ber-cume, D. Fraser, J. Trivett, M. Davis, D. Hata, S. Melvinand C. Hitchens for field assistance. We thank S. Melvin

100 WATERBIRDS

for assistance with project design. Discussion and collab-oration with P. Atkinson, K. Bennett, D. Carter, K. Clark,N. Clark, K. Cole, A. Dey, S. Gillings, B. Harrington, K.Kalasz, S. Michels, R. Miller, C. Minton, G. Moore, L.Niles, K. Reynolds, H. Sitters, D. Smith and R. Weber fa-cilitated and improved the work.

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