Foragingbehaviour of Terek SandpipersXenus cinereus in Thailand

Biljlsma,R.G. & de Roder,F.E.

Bijlsma,R.G. & de Roder,F.E. (1991). Foraging behaviour of TerekSandpiper Xenus cinereus in Thailand. WaderStudy Group Bull.61: 22- 26.

RobG. Bijlsma,Ooldersummerweg 5, 7983 LD Wapse,The Netherlands FrankE. de Roder,Zwartemeerweg 20a, 8307 RP Ens, TheNetherlands

INTRODUCTION thebill was inserted) and probes (when the billwas fully inserted),number of catches(and whether these were Descriptionsof thefeeding behaviour of TerekSandpipers successfulor not),prey species, prey size, handling time Xenuscinereus are scarce, qualitative and mainly based on (measuredas the timebetween catching and swallowing of stragglersfar outsidetheir normal range of occurrence(Glutz the prey)and intra-and interspecificbehaviour. von Blotzheimet al. 1977;Winkler 1980; Barthel& Krott1982; Cramp& Simmons1983). Quantitative information is only Sinceprey consisted almost exclusively of crabs,prey size knownfrom South Korea (Pierstoa 1986). wasmeasured as the carapacewidth relative to billlength: onetenth of the bill= small,up to 0.25x billlength = medium, Duringa stayon Ko Li Bong(7ø16'N, 99ø20'E) off the west andup to 0.5x billlength -- large.We probablyover-estimated coastof Thailandduring 1-6 December1984, we hadthe carapacewidth, especially in largecrabs, because captured opportunityto observefeeding Terek Sandpipers under crabshold their legs close to the body (Piersma 1986)i This excellentconditions. It is a widespreadwinter visitor to alsoexplains why large crabs recorded as preyin Nord- Thailand(Bijlsma & de Roder1985; Parish & Wells1985). mann'sGreenshank Tringa guttifer (Bijlsma & de Roder1985) exceededgape width.

METHODS Mediumand large sized crabs (>5mm) were abundant, with densitiesat the peakof activityof at least80-145 crabs/m 2. Observationswere made during three low tides from a pier Theseestimates were made by eye anddid nottake into witha lengthof 300 m anda heightof circa2 m,just south of accountsmall (<5ram) sandy coloured crabs. Total densities thevillage Ban Pa Tu Puteon KoLi Bong.The pieris sur- aretherefore much higher than recorded. Some 40 speciesof roundedby sandy mudflats, which are partlycovered with crabswere identified on the easternmudflats of Ko Li Bong, debrisof volcanicrocks, bivalve molluscs and remnantsof themajority of whichbelonged to twospecies of thegenus mangroveforest. Walking on the mudflats was possible Uca(Swennen & Uarteijn1985; C. Swennenpers. comm.). withoutsinking in. Fiddlercrabs Uca sp. were abundant and occupied a burrow ForagingTerek Sandpipers were followed with a telescope whichwas defended against other crabs. Small, sandy (Bushnell20-45 x 60) fromdistances between 15 and60 m. coloured crabs also abounded but did not have burrows. Their Eachbird was watchedfor at leastone minute,but observa- escapestrategy from predators consisted of a sprinttowards tions were switched to other individualswhen the distance the nearestfilm of waterand a quickdisappearance by betweenobserver and bird was considered too large to obtain whirlingsand around themselves; the settlingsand partly reliableinformation. One of uswas following the bird, the coveredthe crab,which was thus pedectly camouflaged. othertook notes and kept an eyeon the clock. The following wererecorded each minute: number of pecks,jabs (when half Theactivities of thefirst fifty or hundredTerek Sandpipers

22 100-- encounteredwhen scanning the mudflatswere categorised eachquarter of an houras resting,preening or foraging (excludingbirds on hightide roosts). For changes in crab abundance,we useda subjectiveindex of density,viz. 0 = none,1 = few, 2 = many,3 = verymany and 4 = super- abundant.

RESULTS

Volcanicoutcrops, and sometimes mangrove forest, were usedas hightide roosts.Here, the birdswere standing close _ together,sleeping and occasionallypreening. Usually, Terek Sandpipersleft their roost two hours after high tide. Most birdswaited along the waterline until the favourite feeding o•o o% placesbecame exposed, normally after one hour (= two hours afterhigh tide). The birds dispersed evenly over the mudflats andstarted foraging atan hectic speed. o • ...... •_...... J__ ForagingTerek Sandpipers intermittently rushed ahead with 2 • 0 the bodyheld more or lesshorizontal and the neckstretched hOUœ_saroun• •'ow fide forward.A sprintingTerek Sandpiper was highlydiagnostic, Figure1. Percentageof foraging (including prey handling) Terek Sandpipers notonly as the embodimentof activity,but also due to the per15 rain (based on samples of 50 or 1O0 birds) and crab abundance per typicalcarriage of the neck,head and bill(see inset in Figure half hour around low tide, o.... e •=•e•, 2=•,a,y3=very many 4=superabundar•t 1, basedon slides).At irregularintervals, the birdssuddenly stoppedand peckedat a fooditem or pushedthe billinto the whenapproached. Moreover, the highdensity of waders substrate.Sprints usually covered 4-6m, partof whichwas resultedin constantdisturbance of crabs, whichwere corre- sometimesflown. Two birds,which were followed non-stop for spondinglydifficult to catch.Towards low tide, a slow-downin ten minuteseach, made on average189 (sd= 31) and 190 feedingwas noticed with a simultaneousincrease in feeding (sd= 17) stepsper minute respectively. efficiency(up to 5 catches/minand circa 30% of attempts successful)(Figure 2). Crabswere very mobile at thisstate of The proportionof foragingTereks was closelyrelated to the thetide, venturing farther away from their burrows. The abundanceof crabs(Figure 1), whichwere at a maximum chanceof catchingcrabs thus increased, and because each between1h30 before, until 0h30 after, low tide. In thisperiod, crabneeded some handling time before being eaten, less the mudflatswere mainlyfrequented by Terek Sandpipers, timecould be spentin catchingcrabs. Half an hourafter low MongolianPlovers Charadrius mongolus, Greater Sand- tide,the percentageof foragingTerek Sandpipers sharply ploversC. leschenaultiiand Greenshanks Tringa nebularia, in dropped,presumably as a resultof decreasingcrab densities densitiesof 10-20, 10, 5 and 1-2 birds/harespectively. All anddeclining feeding efficiency (Figure 1, Figure2). birdsforaged solitarily. Brief aggressive encounters were notedwhen birds intruded into each other's feeding range. Of2,460 feeding movements recorded from 1 h30 before till Kleptoparasiticbehaviour of MongolianPlovers against Terek 0h30after low tide, 43% consistedof pecks,38% of jabsand Sandpipersoccurred frequently, and the samebehaviour was 14%of probes(Figure 3). Althoughpecking at preyitems on seenamong Terek Sandpipers,although less often. the surfacewas the majorfeeding tactic throughout the observationperiod, most hectic feeding was noticed just Feedingactivity, expressed as the numberof pecks,jabs and beforelow tide, when crabs were abundantand active'far' probesper minute, was highestone hourbefore low tide awayfrom their burrows. The increase in jabbing after low (Figure2a). Feedingsuccess during this period was exceed- tidewas consistentwith the tendencyof crabsto returnto inglylow: the numberof capturesaveraged one item/min,and theirburrows as soonas the mudflats'dried up' (Figure1 and lessthan 10% of the catchingattempts were successful Figure3). (Figure2b-c). Most crabs were probably still foraging in the vicinityof theirburrows and couldtherefore escape easily

23 The majorityof crabscaught (63%) was small-sized,29% Number 157 97 318 285 547 524 294 238 weremedium-sized and only7% hada largecarapace width between0.25x and 0.5x billlength. Terek Sandpipers showed a clearpreference for smallcrabs. This became even more pronouncedtowards the endof the feedingperiod (Figure 4). We hadthe impressionthat Terek Sandpipers actively selectedsmall crabs. The crabspecies without burrows, and especiallythe smallsandy coloured crabs, became increas- inglyexposed around low tide. Their chance of escaping detectiondecreased around low tide, becausethe mudflats had'dried up'. Crab abundance greatly decreased towards lowtide (Figure 1) andthe remainingforaging crabs tried to

escapepredation by flatteningon the sandand staying 0 i i i i i i i i i motionlessat theapproach of a predator. -15 -10 -05 0 +05 Feeding Hoursaround low hde mefhd•t Handlingtime of preywas closelyrelated to preysize (Figure 5). Smallcrabs were swallowed immediately after capture, Figure3. Methodsof foragingin relationto the tidalcycle. sometimespreceded by manoeuveringthe preyinto a correct positionin the bill.Medium-sized crabs took more time, especiallywhen the legs were detached. This was done by troublesome.Not only did it take moretime to shakeoff the powerfulshaking. The carapacewas legs,it wasalso necessary to detachall legsbefore the swallowedas soonas mostor all legshad come off; the legs carapacecould be swallowed.This prolonged struggle weresometimes eaten afterwards. Large crabs were clearly attractedkleptoparasitic birds. Only one f'hn 8 3 13 17 32 25 14 9 Terekwas attacked (successfully) when eating small crabs (n=64). 50 Threeattacks were witnessed after the captureof medium- sizedcrabs (n:30), eachtime by MongolianPlovers; one of theseattacks was successful. Whilst handling large crabs (n=8),Terek Sandpipers had to evadepiratical Mongolian

I I i I I I I t I No. crabs 3 11 39 2• 1• 8 8 I 100 %

I I I I I I I

+

1.... -05 •-•_ I 0t I i i i ! i i I Hours around low tide 1.0 05 0 +05 œrabsize Figure2. Numberof catching attempts per min foraging and prey Hours around low fde handling(a), number of crabs caught per min foraging and preyhandling (b)and feeding success of Terek Sandpipers around low tide. Number of Figure4. Sizedistribution of crabscaught around low tide, measured as observation minutes are also shown. widthof carapacein relationto billlength.

24 Ploversand congeners six times; two successful robberies by a MongolianPlover were seen. 10 Small Hedium Larqe Contraryto the findings of Ticehurst(1924), Smaldon (1976) andPiersma (1986), Terek Sandpipers in ourstudy area neverwashed captured crabs before eating, although there o wasample opportunity to do so. However,the onlynon-crab /

/ fooditem -a smallfish- was washed before being swallowed. /

DISCUSSION // /// o Foragingbehaviour of TerekSandpipers on KoLi Bong showedmany similarities with those present in SouthKorea (Piersma1986); small differences infeeding strategies were rare also noticed. lO 20 Carapacewidfh /n mm TerekSandpipers on KoLi Bongforaged almost exclusively oncrabs, presumably mostly Uca sp. (C. Swennenpers. comm.)instead of SandbubblingCrabs Scopimera globosa Figure6. Profitability(mg/sec handling) of small,medium- sized and large as in SouthKorea (Piersma 1986). Tereks are evidently crabs,and feeding rate (mg/sec feeding). Average carapace width of small,medium-sized and large crabs is 2.3mm,8.1mm and 17.9mm adaptedto catchingcrabs: the long,slightly upturned bill is respectively.Corresponding ash free dry weights were calculated from perfectlysuited for catching crabs and the runninggate with Figure2 of Zwarts(1985). abrupthalts- sometimes interspersed with short flights - is particularlysuccessful when pursuing crabs. The stooped Sandpipersduring the two hours around low tide, when crabs stanceof the body,with still lower held neck and head,and emergefrom their burrows to feed on the mudflats.We did theshort legs may be adaptationsto scuttlingcrabs, probably notmeasure burrow depth, but data on Uca tangeftin becausethe carapace is elevated whilst walking. Detecting Guinea-Bissau(Zwarts 1985) and Scopimeraglobosa in andpursuing crabs might be easierwhile looking close to the SouthKorea (Piersma 1986) suggest that the vast majority of ground. crabshave a burrowdepth in excessof 50 mm,thus being justout of reachfor Tereks (bill length 43-52 mm,Cramp & Mostcrab species, including Uca sp., have burrows in which Simmons1983). theyremain for the greater part of theday. The superabun- danceof crabsis thereforeonly accessible for Terek Smallcrabs, with a carapacewidth of on average2.4 mm, wereobviously the preferredfood. The gapewidth of Terek Sandpipers,i.e. on average11.2 mm (Piersma 1986), Small Hedium Large probablydid not allow the birdsto swallowcrabs with cara- pacewidths over 10 mm (see alsoFigure 5). However, accordingto Figure6 smallcrabs are notprofitable because profitability(mg/sec handling) did notexceed the overall feedingrate. On theother hand, large crabs were highly profitable,even if preyslost to kleptoparasiticbirds and time lostin evadingpirates are takeninto account. Why then do Tereksprefer small crabs? Whereas we knowthat small crabswere superabundant, we have no informationon the abundanceof largecrabs. It is conceivablethat largecrabs wereless common and therefore harder to obtain(although I I 10 20 the presenceof WhimbrelsNumenius phaeopus suggests Carapacewdfh in mm otherwise).Moreover, we certainlyoverestimated carapace widthof largecrabs, so thatthe yieldper sec handlingtime willbe lowerthan shown in Figure6. It is alsopossible that Figure5. Handlingtime (including aggressive encounters with kleptoparasiticbirds) for small, medium-sized and large crabs. largecrabs are onlypartly eaten, for examplethe legsbut not

25 the carapace,although we did notwitness such behaviour. Bijlsma,R.G. & de Roder,F.E. 1986.Notes on the Nord- Andfinally, if Terekswould be foragingmostly on largecrabs, mann'sGreenshank Tringa guttiler in Thailand.Forktail 2: 92- theyare boundto attractmore kleptoparasitic birds than they 94. alreadydid, thus increasing their chance of losingprey and time. Cramp,S. & Simmons,K.E.L. 1983. TheBirds of the Western Palearctic.Vol. 3. OxfordUniversity Press, Oxford. The synchronisitybetween crab abundance and foraging TerekSandpipers is striking(Figure 1). The earlypeak in Glutz von Blotzheim,U.N., Bauer, K.M. & Bezzel, E. 1977. foragingmight have been an indicationof the hungrinessof Handbuchder Wgel Mitteleuropas,7 (2. Teil).Akademische Tereks,even though feeding efficiency was relativelylow at Verlagsgesellschaft,Wiesbaden. thisstate of thetide. This was offset by foraging on medium- sizedcrabs (Figure 4). The percentageof foragingTereks Parish,D. & Wells, D. 1985. InterwaderEast Africa/Pacific graduallydecreased with the fallingtide, partly as a resultof ShorebirdStudy Programme, Annual Report 1984. Interwader increasedfeeding efficiency (and more time lost in handling), Publication2. Interwader,Kuala Lumpur. butalso because many birds started to interspersetheir feedingbouts with preening. Piersma's (1986) suggestion that Piersma,T. 1986. Foragingbehaviour of TerekSandpipers gutcontent and rateof digestioncould limit food intake, also Xenuscinereus feeding on SandbubblingCrabs Scopimera seemsto holdin ourstudy. Unlike the feedingbehaviour of globosa.J. Om. 127:475-486. Tereksin SouthKorea, the birdson Ko Li Bongdid not have a secondpeak in the percentageof timespend foraging just Smaldon,R. 1976. TerekSandpiper overwintering in Devon. afterlow tide (Piersma 1986). Instead, foraging decreased Brit. Birds 69: 500-503. withfalling tide, as didcrab abundance (Figure 1). We gotthe impressionthat Tereks had a second,but shorter foraging Swennen,C. & Marteijn,E. 1985.Wader feeding ecology boutcirca one hour before high tide. Many busily feeding studiesin the MalayPeninsula. Interwader Publication 2:13- TerekSandpipers were seen along the waterline with incom- 26. ingtide. Of 50 birdswatched at thistime of theday, 92% were foraging.During five minutes of observation,one birdmade Ticehurst,C.B. 1924. The birdsof Sind. Ibis 11:110-146. 121catching attempts, of which39 weresuccessful. Unfor- tunately,we didnot watch for a longerperiod. Winkler,R. 1980. Zum Nahrungserwerbdes Terekwasserlafers(Xenus cinereus) im Winterquartier. ACKNOWLEDGEMENTS Egretta23: 56-59.

Thisstudy would have been impossible without the grant- Zwarts,L. 1985. The winterexploitation of FiddlerCrabs Uca assistanceby Interwader(East Africa/Pacific Shorebird Study tangeriby waders in Guinea-Bissau.Ardea 73:3-12 Programme).Mogens Henriksen was our companion in Thailand.Advice and information were given by Jon Starks, Phil Round and Cees Swennen. Our enthusiasm for Tereks wasshared by TheunisPiersma, who also commented on a firstdraft of thisarticle. Anne-Marie Blomert suggested many importantimprovements.

REFERENCES

Barthel,P.H. & Krott,N. 1982.Terekwasserl•fer (Xenus cinereus)in S•d-Niedersachsenmir Anmerkungen zu Feldkennzeichen und Auftreten. Faun. Mitt. SQd-Nieders. 4-5:47-51 Bijlsma,R.G. & de Roder,F.E. 1985. Waders along the coast of Thailandduring November and December1984. WlWO- report4.

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