Sex-related seasonal differences in the foraging strategy of the Kentish Plover

BioOne sees sus ainable schola ly publishing as an inhe en ly collabo a i e en e p ise connec ing au ho s, nonp o i publishe s, academic ins i u ions, esea ch lib a ies, and esea ch unde s in he common goal o maximizing access o c i ical esea ch. Sex-Rela ed Seasonal Di e ences in he Fo aging S a egy o he Ken ish Plo e Au ho (s): MacA ena Cas o, Jose A. Mase o, Alejand o Pé ez-Hu ado, Juan A. Ama , and Cesa Megina Sou ce: The Condo , 111(4):624-632. 2009. Published By: Coope O ni hological Socie y URL: h p://www.bioone.o g/doi/ ull/10.1525/cond.2009.080062 BioOne (www.bioone.o g) is a nonp o i , online agg ega ion o co e esea ch in he biological, ecological, and en i onmen al sciences. BioOne p o ides a sus ainable online pla o m o o e 170 jou nals and books published by nonp o i socie ies, associa ions, museums, ins i u ions, and p esses. 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En especies de a es con cuidado bipa en al, cada sexo puede ene sus p opios eque imien os de ene gía y/o esquema de iempo pa a la alimen ación, lo cual pod ía conduci a di e encias en las es a egias de alimen ación en e ambos sexos. En los es ua ios, las especies de playe os como Cha ad ius alexand inus pueden o ajea en angos in e ma eales y en hábi a s sup ama eales adyacen es an o du an e el in ie no así como du- an e la época ep oduc i a. Aquí, analizamos la die a, el uso de hábi a de o ajeo, la asa de inges ión (biomasa inge ida po unidad de iempo) y el iempo dedicado al o ajeo po el macho y la hemb a de C. alexand inus du- an e ambas empo adas en una zona es ua ina donde los angos in e ma eales y las salinas adyacen es son las p incipales á eas de alimen ación. La p incipal p esa pa a C. alexand inus ue un polique o (Ne eis di e sicolo ), una p esa in e ma eal que suplió más del 80% de la biomasa consumida en cada es ación. Ambos sexos inc emen- a on sus asas de alimen ación du an e la época ep oduc i a, y disminuye on sus iempos diu nos de o ajeo. Po el inc emen o de la asa de inges ión du an e la época ep oduc i a, las a es minimiza on el iempo que pasa on en los angos in e ma eales, lo que les pe mi ió maximiza el iempo dedicado a las ac i idades de ep oducción en las salinas adyacen es. Po lo an o, el conflic o en e alimen a se en los angos e sus el desa ollo de las ac- i idades de ep oducción (en las salinas), ue esuel o aco ando el iempo en los angos, minimizando el iempo ue a de las zonas de nidada. Hubo di e encias elacionadas con el sexo en el iempo diu no dedicado al o ajeo: las hemb as dedica on dos ho as menos a la alimen ación y concen a on su ac i idad de alimen ación en las ho as cen ales de la ma ea baja. SEX-RELATED SEASONAL DIFFERENCES IN THE FORAGING STRATEGY OF THE KENTISH PLOVER Di e encias Es acionales Relacionadas con el Sexo en la Es a egia de Alimen ación de Cha ad ius alexand inus Abs ac . In species o bi ds wi h bipa en al ca e, each sex may ha e i s own ene gy equi emen s and/o schedule o eeding, possibly leading he sexes o di e in o aging s a egy. In es ua ies, sho ebi ds such as he Ken ish Plo e (Cha ad ius alexand inus alexand inus) may o age on in e idal mudfla s and in adjacen su- p a idal habi a s du ing win e as well as du ing he b eeding season. In his s udy, we analyzed he die , use o o aging habi a , ood-in ake a e (biomass inges ed pe uni ime), and ime alloca ed o o aging by male and emale Ken ish Plo e s a bo h seasons in an es ua y nea Cádiz, Spain, whe e in e idal mudfla s and adjacen sal wo ks a e he main habi a s o o aging. The plo e s’ main p ey was he agwo m (Ne eis di e sicolo ), an in e idal polychae e ha supplied mo e han 80% o he biomass consumed a each season. Du ing he b eeding season, bo h sexes inc eased hei in ake a e and dec eased hei dayligh o aging ime. By inc easing he diu nal in ake a e du ing he b eeding season, he bi ds minimized hei ime spen o aging on he in e idal mudfla s, allowing hem o maximize he ime o ac i i ies associa ed wi h b eeding in he adjacen sal wo ks. The e o e, he plo e s sol ed he conflic be ween o aging on he mudfla s and b eeding in he sal wo ks by sho ening he o aging ime on he mudfla s, minimizing ime away om he nes ing a eas. The sexes di e ed in he dayligh ime alloca ed o o aging, wi h emales spending 2 h less on o aging and concen a ing hei eeding ac i i y in o he cen al hou s o low ide. 4Cu en add ess: Cen o de In es igación en Ecosis emas de la Pa agonia, Bilbao 449, Coyhaique, Chile. E-mail: maca ena.cas [email protected] MACARENA CASTRO 1,4, JOSE A. MASERO 2, ALEJANDRO PÉREZ-HURTADO 1, JUAN A. AMAT 3, AND CESAR MEGINA 1 1Depa amen o de Biología Animal, Facul ad de Ciencias del Ma y Ambien ales, Uni e sidad de Cádiz, E-11510 Pue o Real, Spain 2G upo de In es igación en Conse ación, Á ea de Zoología, Facul ad de Ciencias, Uni e sidad de Ex emadu a, A enida de El as s/n, E-06071 Badajoz, Spain 3Es ación Biológica de Doñana, Consejo Supe io de In es igaciones Cien íficas, Apdo 1056, E-41080 Se illa, Spain Manusc ip ecei ed 23 Oc obe 2008; accep ed 4 Augus 2009. Key wo ds: Cha ad ius alexand inus, o aging, habi a use, in ake a e, sal wo ks, sex di e ence, Ken ish Plo e , sho ebi ds. SEASONAL VARIATION IN THE KENTISH PLOVER’S FORAGING STRATEGY 625 INTRODUCTION Di e en beha io s equi e ime and/o ene gy and canno be ca ied ou simul aneously. This conflic may lead o ade- o s among di e en ac i i ies. Fo ins ance, eeding is no compa ible wi h any o he ene gy-demanding ac i i y (Cu hill and Hous on 1997). Such ade-o s a e likely o be mo e ap- pa en du ing he b eeding season, when esou ce alloca ion can a ec ecundi y, su i al, and ime de o ed o ep oduc- ion s ongly (Sibly and Calow 1986, Williams 1996). In many species o bi ds, success ul b eeding equi es bipa en al ca e. In hese species, bo h pa en s spend a subs an ial ac ion o each day on he nes , educing he ime a ailable o o ag- ing. Du ing incuba ion, ex ended absences om he nes may esul in changes in egg empe a u es ha can a ec emb yo de elopmen nega i ely (Webb 1987, Ama and Mase o 2007) as well as inc ease he ime o exposu e o p eda o s (Tulp and Schekke man 2006). The e o e, he wo sexes should no o - age a he same ime so ha he nes can be almos con inu- ously a ended by an adul . Many mig a o y sho ebi ds (Cha ad ii) ely on in e idal habi a s o o aging du ing bo h he win e and he b eeding season. Owing o hei small size and hei high mass-specific me abolic a es, sho ebi ds ha e a limi ed capaci y o s o e en- e gy be o e he onse o b eeding and a e he e o e obliged o eed du ing incuba ion (Tulp and Schekke man 2006). The in e idal habi a is a ailable o only pa o each day, and du ing he b eeding season males and emales mus al e na e lea ing he nes o he in e idal a eas o sa is y hei equi e- men s o bo h ood and nes a endance. None heless, sea- sonal di e ences in sho ebi ds’ o aging beha io ha e been s udied only in equen ly (Du ell 2001). The Ken ish/Snowy Plo e (Cha ad ius alexand inus) is a mig a o y sho ebi d wi h bipa en al incuba ion, emales incu- ba ing by day, males by nigh (Wa ine e al. 1986, F aga and Ama 1996). In es ua ies, i can eed in in e idal mudfla s as well as in adjacen sup a idal habi a s (Pie sma 1996, Mase o e al. 2000). In his s udy we compa ed he o aging s a egies o male and emale Ken ish Plo e s in he win e and b eeding season in an es ua y in which in e idal mudfla s and adjacen sal wo ks (salinas o sal pans) a e he main o aging g ounds (Mase o e al. 2000, Cas o 2001). Because he Ken ish Plo- e can nes only in he sup a idal habi a , we expec ed an in- c ease du ing he b eeding season in he use o sal wo ks o o aging as a esul o , o example, e i o ial beha io . The o aging beha io o ypical plo e s is highly s e eo yped, and sho -billed species such as he Ken ish Plo e all o age isu- ally in a un–s op–sea ch manne (Mase o e al. 2007). The en- e ge ic demands o b eeding Ken ish Plo e s may di e by sex, explaining di e ences in o aging pa e ns. Howe e , Ama e al. (2000) ound no changes in body mass du ing incuba ion and ea ly chick ea ing o ei he males o emales, and nei he did hey find sex- ela ed di e ences in he ene ge ic cos s o in- cuba ion. Ne e heless, di e en oles du ing ep oduc ion may s ill lead o di e ences be ween he sexes in pa e ns o o ag- ing. Because emales incuba e by day and males by nigh , we expec ed sexual di e ences in pa e ns o habi a use, die , in- ake a e (biomass inges ed pe uni ime), and ime alloca ed o eeding du ing he b eeding season. In bo h Eu ope and he Ame icas Cha ad ius alexand i- nus is su e ing sha p popula ion declines (B own e al. 2000, Delany and Sco 2006), and many ini ia i es o hal his de- cline ha e in ol ed habi a - es o a ion plans (La e y e al. 2006). Because popula ions o mig a o y bi ds can be influ- enced by e en s du ing win e , mig a ion, o b eeding (Sil- le e al. 2000), e ec i e sho ebi d conse a ion equi es an unde s anding o when and how popula ions a e limi ed and egula ed (Skagen 2006). In his con ex , in ake a e is used by modele s o es ima e ene gy budge s, p eda o –p ey in e - ac ions, he quali y o eeding g ounds, and o he ac o s ha may a ec fi ness, such as he isk o being aken by a p eda- o , and ood- ela ed ep oduc i e success (Goss-Cus a d e al. 2006). Acco dingly, ou esul s o seasonal a ia ion in in- ake a e may bea significan ly on he success o conse a ion plans o C. alexand inus. METHODS STUDY SITE We chose an indus ial sal wo ks o 400 ha in he no h o Cádiz Bay Na u al Pa k (36n 23` N, 6n 8` W), sou hwes e n Spain, as he s udy a ea, oge he wi h 20–30 ha o adjacen in e idal mudfla s a a dis ance o 50–800 m (Fig. 1). Abou 400 Ken ish Plo e s egula ly win e in his sal wo ks, while du ing b eeding he e a e abou 120 indi iduals (Mase o e al. 2000, his s udy). The in e idal mudfla s a e exposed (i.e., a ailable o sho ebi ds) o 7–9 h daily (semidiu nal ides). The s udy a ea (sal wo ks and adjacen in e idal mud- fla s) is su ounded by an h opogenic habi a s unsui able o sho ebi ds, hus cons i u ing an isola ed we land in he no h o Cádiz Bay (Fig. 1). O e all, he s udy a ea unc ions as a closed sys em o o e win e ing sho ebi ds. Small sho ebi ds such as he Ken ish Plo e es a high ide in he sal wo ks and o age in he adjacen in e idal mudfla s a low ide, wi h no appa en mo emen s be ween his isola ed we land and he es o he bay h oughou he win e (Ho as 1997, Mase o e .al. 2000, Mase o e al. 2001). A Cádiz Bay, Ken ish Plo e s ha e been banded since 1994 wi h bo h me al and colo bands (e.g., Pé ez-Hu ado e al. 1994, To ija 2005). Du ing ou s udy, 36% o he Ken ish Plo e s b eeding in he s udy a ea we e colo -banded (pe s. obs.), and we no ed ha a leas 44% o hese colo -banded Ken ish Plo e s b eeding in he sal - wo ks had win e ed in he same a ea p e iously (pe s. obs.). Sex ecogni ion was possible in mos cases by plumage dimo phism (males ha e a black ba on he on o hei o e- heads, emales do no ; see Hayman e al. 1995 o plumage de- sc ip ions). We could dis inguish he sexes ~86% o he ime e en in win e when he plumage is mo e c yp ic (Table 1). 626 MACARENA CASTRO ET AL. USE OF FORAGING HABITAT Ou field obse a ions ex ended om Decembe 1996 o June 1997. The numbe o male and emale Ken ish Plo e s o - aging and es ing (including p eening) in he sal wo ks was eco ded once pe week (excep one week in win e in which wea he condi ions made i impossible), a bo h high and low ides, in Decembe and Janua y (win e ) and in May and June (b eeding season). The maximum numbe s o ac i e nes s and adul bi ds eco ded in he sal wo ks du ing his b eed- ing season we e 57 and 113, espec i ely. Du ing he obse a- ions o o aging in he sal wo ks a high ide, we no ed ha all hese Ken ish Plo e s we e engaged in ypical b eeding beha io s such as nes a endance, dis ac ion displays, o e i o ial figh s (on a e age, 80% o he pai s we e in ol ed in nes a endance and less han 10% we e ca ing o chicks; pe s. obs.). Acco dingly, we assumed ha all adul Ken ish Plo e s eco ded du ing he o aging s udies in he s udy a ea in May and June we e b eeding bi ds (ju eniles can be dis in- guished by he na ow bu inges on hei co e s and scapu- la s; Hayman e al. 1995). Diu nal ac i i y. We assumed he coun in he sal wo ks a high ide o be he o al numbe o Ken ish Plo e s in he s udy a ea and he di e ence be ween he o al coun ed in he sal wo ks a high and low ides o be he pa o he popula ion isi ing he mudfla s. We eco ded ac i i y o plo e s on he in e idal mudfla s a low ide on he day a e he census in he FIGURE 1. S udy a ea, showing in e idal mudfla s (in e idal channel) and adjacen sal wo ks (sup a idal a ea). The s udy a ea cons i- u es an isola ed we land in he no h o Cádiz Bay, sou hwes e n Spain. TABLE 1. Numbe s o male and emale Ken ish Plo e s eco ded in he sal wo ks (high and low ide) and on he in e idal mudfla s du ing win e and he b eeding season. Mean o aging ac i i y (pe cen age o bi ds o aging o 1 SD) is gi en in pa en heses. Sal wo ks High ide Low ide In e idal mudfla s Win e ing Females 139 (26.43 o 10.41) 12 (100) 152 (95.61 o5.66) Males 150 (10.35 o5.29) 21 (100) 135 (96.82 o8.63) Sex unknown 45 (32.51 o 10.22) 4 (100) 10 (95.41 o7.45) B eeding Females 48 (19.38 o1.03) 28 (3.6 o 2.42) 15 (52.3 o 36.19) Males 65 (25.22 o6.04) 38 (7.89 o 3.64) 20 (74.76 o 34.62) Sex unknown 4 (40.03 o5.82) 4 (15.22 o 4.04) 1 (100) SEASONAL VARIATION IN THE KENTISH PLOVER’S FORAGING STRATEGY 627 sal wo ks and unde simila condi ions. Ken ish Plo e s eed- ing and es ing on he in e idal mudfla s we e coun ed e e y hou du ing low ide (7–9 h ). Fo aging ac i i y on he mud- fla s, exp essed as he pe cen age o Ken ish Plo e s o aging, was calcula ed o each coun , and he pe cen ages we e la e a e aged o he en i e low- ide pe iod (Zwa s e al. 1990). Noc u nal ac i i y. Du ing he b eeding season, we used a ligh in ensifie (Canon; 6.5 magnifica ion, ligh -in ensi- ying ac o 70 000 ) o eco d he bi ds’ numbe and ac i - i y a nigh , always a a dis ance o 10 o 50 m om he ocal indi iduals. E e y 14 days we ca ied ou noc u nal coun s in he same a ea as ou diu nal coun s bu du ing he pe iod be- ween 2 h be o e and 2 h a e low ide. Noc u nal o aging ac i i y on in e idal mudfla s was calcula ed by compa ing he numbe s o indi iduals eeding by nigh and by day a he same si e (Zwa s e al. 1990). Nigh censuses in he sal wo ks we e ca ied ou in he same way as he dayligh censuses. Ligh om a nea by illage acili a ed iden ifica ion o bi ds and hei o aging ac i i y, al hough sexing indi iduals was no possible. Fo win e , da a on noc u nal ac i i y we e de- i ed om a s udy ca ied ou a he same si e he same yea (Mase o e al. 2000). Fo aging- ime alloca ion. The daily ime spen o aging was de i ed om he p opo ions o males and emales o ag- ing in each habi a (in e idal mudfla s o sal wo ks) ela i e o hei o al numbe s, numbe o minu es ha habi a was a ail- able, and p opo ion ime he plo e s spen o aging. Fo his calcula ion, we conside ed he du a ion o he low- ide pe iod in he sal wo ks he same as he pe iod du ing which he in- e idal mudfla s we e exposed; he es , up o he comple ion o he idal cycle, was conside ed o be high ide (Mase o and Pé ez-Hu ado 2001). We could no dis inguish he plo e s’ sex a nigh , so we assumed he sex a io o bi ds o aging a nigh was simila . DIET AND INTAKE RATE P ey iden ifica ion and size. We andomly selec ed ac i ely o aging indi iduals, 30m om he obse e , and obse ed hem o 1 min wi h a 20–60 zoom elescope. A e 1 min, a new ocal indi idual a leas 10 m om he p e ious indi- idual was chosen o a oid pseudo eplica ion (Hu lbe 1984). In e e y sequence, we eco ded he ollowing da a: bi d’s sex, eeding a e (success ul pecks min−1), ype and size o p ey i ems cap u ed, and ime since low ide. In he sal wo ks, plo- e s o aged on small p ey i ems a ailable a high densi ies along he sho e o he pans, and we assumed ha a p ey i em was inges ed e e y ime he bi d pecked (pe s. obs.; see simi- la p ocedu e in Mase o and Pe ez-Hu ado 2001). P ey size was es ima ed in ela ion o a e age bill leng h. A Cádiz Bay he e we e no significan di e ences be ween males and emales in bill leng h ( 43  0.37, P 0.72; unpub- lished da a), so we used an a e age leng h o 16 mm (15.56 o 0.82 mm; n 45 indi iduals, bo h sexes combined). Visual obse a ions we e con as ed wi h analyses o ecal samples (32 eces in win e and 30 in he b eeding pe iod, collec ed in oos ing a eas o when eeding bi ds we e obse ed exc e - ing). Mase o e al. (1999) and Cas o (2001) p o ided in o - ma ion abou he species composi ion, size dis ibu ion, and biomass o he p ey a ailable o sho ebi ds in he s udy a ea. Acco ding o hose s udies, on he mudfla s he plo e ’s po- en ial p ey we e he polychae e agwo m Ne eis di e sicolo , he bi al es Ce s ode ma edule and Sc obicula ia plana, he gas opod Hyd obia ul ae, and he isopod Cya hu a ca i- na a, while in he sal wo ks hey we e he b ine sh imp (A - emia spp.), adul s and la ae o he coleop e an Och hebius spp., and la ae o he dip e ans Chi onomus salina ius and Ephyd a spp. All hese po en ial p ey lea e ecognizable ha d pa s a e passing h ough a plo e ’s diges i e ac (Cas o 2001). Following he me hod o Zwa s and Blome (1992), we used he cumula i e equency dis ibu ion o p ey sizes ound in eces o co ec isual es ima es o p ey sizes. Biomass inges ed. We con e ed he leng h o each p ey i em in o biomass by he equa ions in Mase o e al. (1999) and Mase o and Pe ez-Hu ado (2001). We we e no able o es i- ma e accu a ely in he field he species and he leng h o poly- chae e wo ms sho e han hal a plo e ’s bill leng h (which co esponded o 12 mm a e co ec ion o he isual es- ima es; see abo e). Fo his size class o p ey, we assumed as a e age biomass he a e age biomass o he polychae es smalle han 12 mm a ailable in he in e idal mud (da a om Mase o e al. 1999 and Cas o 2001; see p e ious sec ion). Finally, we es ima ed in ake a e (mg o ash- ee d y mass sec−1) by mul iplying he numbe o each size class aken pe minu e by he ash- ee d y mass o ha size class. The e a e no published da a on seasonal a ia ion in he condi ion o in e eb a es in Cádiz Bay. The e o e, ou es i- ma es o in ake a es du ing he b eeding season may be con- side ed conse a i e gi en ha wa me empe a u es may a ec he a ailabili y and condi ion o in e eb a es (Zwa s and Wanink 1993). Likely, i he e a e seasonal o sex- ela ed di e ences in in ake a e, hey may be sligh ly highe han hose we epo . STATISTICAL ANALYSES We used a co a iance analysis (ANCOVA) o explo e sex- ela ed di e ences in he pe cen age o indi iduals using he mudfla s and sal wo ks a each season. In his analysis, sex (male/ emale), season (win e /b eeding), and si e (mudfla s/ sal wo ks) we e fixed ac o s. Since he numbe o o aging indi iduals could be influenced by he o al numbe o bi ds in he a ea, we included he o al numbe o indi iduals o each sex as co a ia e. Seasonal changes in o aging ac i i y (pe - cen age o eeding bi ds), o aging ime, and sex- ela ed di - e ences in eeding a e and in ake a e we e e alua ed also by ANCOVA wi h sex, season, and si e as fixed ac o s and 628 MACARENA CASTRO ET AL. densi y o bi ds as a co a ia e. Densi y o bi ds (ha−1) was in- cluded as co a ia e because a s udy in he same in e idal zone sugges ed ha a high densi y o sho ebi ds influences he be- ha io o he in e eb a e p ey, possibly a ec ing he bi ds’ in ake a e nega i ely (Mase o and Pé ez-Hu ado 2001). We assessed di e ences in mean diu nal and noc u nal ac- i i y wi h S uden ’s - es . The da a we e inspec ed o no - mali y and homoskedas ici y and we e no malized by a csine ans o ma ion i needed. When analyses showed significan di e ences, a pos -hoc Tukey es was used. Unless s a ed o he wise, mean alues a e p esen ed wi h o SD, and he sig- nificance le el o all es s was se a A 0.05. All s a is i- cal analyses we e pe o med wi h S a is ica 7.0 (S a So , Inc., 2004). RESULTS FORAGING The pe cen age o indi iduals mo ing o he in e idal zone a low ide dec eased om 88% in win e o 30% in he b eed- ing season (F1, 25  74.93, P 0.05). Mean o aging ac i i y on in e idal mudfla s dec eased om win e o he b eeding season o bo h sexes (F1,24  65.44, P 0.05), pa icula ly o emales (F1,24  25.20, P 0.05; Table 1). This change was because emales sho ened hei ime o aging on he mud- fla s, du ing he b eeding season concen a ing hei o aging mainly be ween 2 h be o e and 1 h a e he maximum low ide (Fig. 2). The a io o indi iduals o aging a nigh inc eased om 0.37 in win e o 0.51 in he b eeding season ( 6 −7.02 P 0.05). Th oughou he s udy pe iod he e was no noc u nal o aging in he sal wo ks a nigh . Du ing he b eeding season emales alloca ed less ime o o aging han did males (614.75 o 27.65 and 282.28 o 37.11 min day−1 o emales; 627.86 o 19.26 and 405 o 40.54 minu es pe day o males, du ing he win e and b eeding season, e- spec i ely; F1,12  11.64, P 0.05). DIET Combining da a om isual obse a ions, eces collec ed in each habi a , and he knowledge o a ailable p ey yielded a eliable es ima e o he plo e ’s p ey and hei sizes. On he mudfla s he main p ey was he polychae e wo m Ne eis di e - sicolo , which appea ed in 100% o eces analyzed and 100% o isual obse a ions, supplying mo e han he 80% o he biomass he plo e s consumed a bo h seasons (Fig. 3). The aqua ic bee le Och hebius sp. appea ed in mos eces (70%) a bo h seasons, bu i supplied less han 10% o he biomass he plo e s inges ed (Fig. 3). The emaining p ey i ems ap- pea ed in 30% o eces and supplied less han 10% and 20% o he inges ed biomass in win e and he b eeding season, e- spec i ely (Fig. 3). A bo h seasons Ken ish Plo e s inges ed p edominan ly polychae es ~10 cm long (Fig. 4). We could no assess he leng h o he Och hebius bee les inges ed, bu he leng h o hose a ailable in he sal wo ks anged om 1 o 3 mm a bo h seasons (Cas o 2001). To calcula e in ake a e, we collec ed a andom sample o 60 indi iduals o his bee le om he pans o calcula e he a e age biomass pe indi idual (mean biomass pe indi idual: 6.67 10−5 g ash- ee d y mass). INTAKE RATE Al hough eeding a es we e significan ly highe in he sal wo ks han on he mudfla s (F1,164  42.99, P 0.05, Table 2), in ake a es we e significan ly highe (a ound 10 highe ) on he mud- fla s han in he sal wo ks (F1,164  70.95, P 0.05; Table 2). The plo e s inc eased hei in ake a e om win e o he b eeding season significan ly on he mudfla s (F1,164  4.45, P 0.05; Ta- ble 2) bu no in he sal wo ks (F1,164  0.07, P 0.79; Table 2), al hough he e we e no significan di e ences be ween he sexes a ei he season o in ei he habi a (F1,164  0.07, P 0.79; Table 2). The densi y o eeding bi ds on he mudfla s had no significan e ec on in ake a e (F1,164  0.78, P 0.38). FIGURE 2. Mean hou ly o aging ac i i y o male and emale Ken ish Plo e s du ing dayligh on in e idal mudfla s in ela ion o ides du ing he win e (a) and b eeding season (b). SEASONAL VARIATION IN THE KENTISH PLOVER’S FORAGING STRATEGY 629 DISCUSSION The o aging s a egy o Ken ish Plo e s, as measu ed by habi a use, in ake a e, and ime alloca ed o eeding, shi ed seasonally. Bo h sexes inc eased hei in ake a e du ing he b eeding season and dec eased hei dayligh eeding ime, so ha he conflic o o aging on he mudfla s (whe e he main p ofi able p ey we e a ailable) wi h nes ing (which necessa - ily akes place on he adjacen sup a idal habi a ) was esol ed by sho ening he o aging ime on he mudfla s and he e o e minimizing ime away om he nes ing a eas. Acco ding o ene gy-maximiza ion p inciples (S ephens and K ebs 1986), he sal wo ks we e a subop imal o aging habi a o he plo e s, which ob ained en imes less biomass (ene gy) pe uni ime in his habi a han on he in e idal mudfla s. Indeed, acco ding o Zwa s and Wannik’s (1993) equa ion o assessing minimum p ofi able in ake a e as a unc ion o a sho ebi d’s body mass, he plo e s’ in ake a e FIGURE 3. Occu ence (a) and biomass (b) o he p ey eco ded in he eces o Ken ish Plo e s du ing he win e (n = 32) and b eeding season (n = 30). 630 MACARENA CASTRO ET AL. in he sal wo ks was only 27% o he minimum in ake a e ex- pec ed o i . Use o he sal wo ks a low ide du ing he b eed- ing season inc eased. Because no densi y-dependen ac o s we e appa en ly ope a ing in he in e idal mudfla s, he FIGURE 4. Compa ison o he leng h classes o he agwo m Ne eis di e sicolo a ailable on he in e idal mudfla s (solid line) and in he eces o Ken ish Plo e s (b oken line) du ing he win e (a) and b eeding season (b). Da a on leng h classes a ailable on mud- fla s a e om Cas o (2001). TABLE 2. Mean (o 1 SD) eeding a e and in ake a e o male and emale Ken ish Plo e s o aging on he in e idal mudfla s and in he adjacen sal wo ks du ing he win e and b eed- ing season. In e idal mudfla s Sal wo ks Feeding a e In ake a e nFeeding a e In ake a e n Win e Males 13.77 o 6.58 0.20 o 0.10 20 19.89 o 4.49 0.03 o 0.01 12 Females 13.59 o 5.57 0.22 o 0.11 23 23.72 o 5.49 0.03 o 0.02 17 B eeding Males 13.39 o 8.10 0.33 o 0.20 43 26.54 o 17.28 0.04 o 0.03 18 Females 12.35 o 7.11 0.34 o 0.31 27 19.09 o 6.91 0.03 o 0.01 13 longe ime ha he bi ds spen in he sal wo ks du ing he b eeding season was likely no due o hei being displaced om he mudfla s by o he indi iduals. The esul s sugges ha he bi ds emain in he sal wo ks du ing low ide because o hei b eeding. By inc easing hei in ake a es du ing he b eeding sea- son, he plo e s ob ained mo e ene gy in a sho e ime han in win e , hus minimizing o aging ime and inc easing ime a ailable o o he ac i i ies. Females alloca ed almos 2 h less o o aging du ing dayligh in he b eeding sea- son, mo ing on o he mudfla s o eeding jus du ing maxi- mum mud exposu e, when, a p io i, mo e p ey a e a ailable (Esselink and Zwa s 1989). Males also dec eased hei eed- ing on he mudfla s, al hough he dec ease was no as sha p as o emales. Depending on he phase o b eeding, each sex’s ime con- s ain o eeding is g ea e o lesse . Females incuba e mainly du ing dayligh , males mos ly a nigh (Wa ine e al. 1986, F aga and Ama 1996, Kosz olányi and Székely 2002). The e- males usually dese he b ood when chicks a e 7–20 days old (Wa ine e al. 1986, Székely and Lessells 1993, Ama e al. 1999). The e o e, du ing incuba ion emales a e mo e ime- cons ained o eeding han a e males, al hough he opposi e is he case a e ha ching. We did no ollow indi idual bi ds, and ou es ima es a e popula ion-based, so ha emales and males we s udied may ha e been in di e en s ages o b eed- ing. Howe e , we measu ed all a iables when we ound he g ea es numbe o ac i e nes s, implying ha mos indi idu- als eco ded du ing ou obse a ions we e a a simila s age. Mul iplying he daily ime alloca ed o eeding by he in- ake a e, and assuming an assimila ion e ficiency o 80% o Ne eis di e sicolo (Cas o e al. 2008) and 70% o Och he- bius (Bell 1990), one can es ima e he plo e s’ daily ene gy consump ion. Using he equa ion o Nagy e al. (1999) o es i- ma e he daily heo e ical ene gy consump ion o wild bi ds, one can compa e he ene gy consump ion we es ima e wi h he heo e ical alue. Acco ding o ou es ima es, males consumed 131.42 kJ day−1 and 121.58 kJ day−1, emales 141.02 kJ day−1 and 97.98 kJ day−1 du ing he win e and b eeding season, e- spec i ely. Acco ding o he heo e ical es ima es, he ene gy SEASONAL VARIATION IN THE KENTISH PLOVER’S FORAGING STRATEGY 631 sho ebi d conse a ion assessmen : sho ebi d conse a ion s a- us, conse a ion uni s, popula ion es ima es, popula ion a ge s, and species p io iza ion. Manome Cen e o Conse a ion Sci- ences. h p://www.Manome .o g/p og ams/sho ebi ds (10 Ap il 2009). CASTRO, M. 2001. Ecología de la alimen ación del Cho li ejo Pa ine- g o Cha ad ius alexand inus: exis e plas icidad compo amen- al o fisiológica asociada al sexo?. Ph.D. disse a ion, Uni e si y o Cádiz, Cádiz, Spain. CASTRO, M., J. A. MASERO,C. MEGINA, J. A. AMAT,AND A. PÉ- REZ-HURTADO. 2008. Ene gy and mac onu ien assimila ion e ficiencies o Snowy Plo e (Cha ad ius alexand inus) eed- ing on he polychae e agwo m (Ne eis di e sicolo ). Auk 125: 368–373. CUTHILL,I.C., AND A. I. HOUSTON. 1997. Managing ime and ene gy, p. 97–120. In J. R. K ebs and N. B. Da ies [EDS.], Beha iou al ecology: an e olu iona y app oach, 4 h ed. Blackwell Science, Ox o d, UK. DELANY,S., AND SCOTT,D. [EDS.]. 2006. Wa e bi d popula ion es i- ma es, 4 h ed. We lands In e na ional, Wageningen, he Ne he - lands. DURRELL,S.E.A.LE V. DIT. 2001. Indi idual eeding specialisa ion in sho ebi ds: popula ion consequences and conse a ion impli- ca ions. Biological Re iews 75:503–518. ESSELINK, P., AND L. ZWARTS. 1989. Seasonal end in bu ow dep h and idal a ia ion in eeding ac i i y o Ne eis di e sicolo . Ma ine Ecology P og ess Se ies 56: 243–254. FRAGA, R. M., AND J. A. AMAT. 1996. B eeding biology o a Ken ish Plo e (Cha ad ius alexand inus) popula ion in an inland saline lake. A deola 43:69–85. GOSS-CUSTARD, J. D., A. D. WEST, M. G. YATES,R.W.G.CAL- DOW,R.A.STILLMAN,L. BARDSLEY, J. CASTILLA, M. CAS- TRO, V. DIERSCHKE, S. E. A. LE V. DIT DURELL, G. EICHHORN, B. J. ENS,K. M. EXO, P. U. UDAYANGANI-FERNANDO, P. N. FERNS, P. A. R. HOCKEY, J. A. GILL, I. JOHNSTONE, B. KALEJ- TA-SUMMERS, J. A. MASERO, F. MOREIRA,R. V. NAGARAJAN, I. P. F. OWENS,C. PACHECO,A. PÉREZ-HURTADO,D.ROGERS, G. SCHEIFFARTH, H. SITTERS,W. J. SUTHERLAND, P. TRIPLET, D. H. WORRALL,Y.ZHARIKOV,L.ZWARTS,AND R. A. PETTIFOR. 2006. In ake a es and he unc ional esponse in sho ebi ds (Cha ad ii o mes) ea ing mac o-in e eb a es. Biological Re iews 81:1–29. HAYMAN, P., J. MARCHANT,AND T. PRATER. 1995. Sho ebi ds: an iden ifica ion guide o he wade s o he wo ld. A. & C. Black, London. HORTAS, F. 1997. E olución de las comunidades de a es limícolas (O den Cha ad ii o mes) en salinas del su oes e de España. Es uc u a espacio- empo al de las poblaciones y uso del hábi a . Ph.D. disse a ion, Uni e sidad de Cádiz, Cádiz, Spain. HURLBERT, S.H. 1984. Pseudo eplica ion and design o ecological field expe imen s. Ecological Monog aphs 54:187–211. KOSZTOLÁNYI,A., AND T. SZÉKELY. 2002. Using a ansponde sys- em o moni o incuba ion ou ines in Snowy Plo e s. Jou nal o Field O ni hology 73:199–205. KUWAE,T. 2007. Diu nal and noc u nal eeding a e in Ken ish Plo- e s Cha ad ius alexand inus on an in e idal fla as eco ded by elescopic ideo sys ems. Ma ine Biology 151:663–673. LAFFERTY, K. D., D. GOODMAN,AND C. SANDOVAL. 2006. Res o a ion o b eeding by Snowy Plo e s ollowing p o ec ion om dis u - bance. Biodi e si y and Conse a ion 15:2217–2230. MASERO, J. A., M. PÉREZ-GONZÁLEZ, M. BASADRE,AND M. OTERO- SAAVEDRA. 1999. Food supply o wade s (A es: Cha ad ii) in an es ua ine a ea o he Bay o Cádiz (SW Ibe ian Peninsula). Ac a Oecologica 20:429–434. inges ed should be 138.03 kJ day−1 and 147.53 kJ day−1 du ing hese wo pe iods, espec i ely (we used a mean body mass o 39.55 o 3.95 o win e and 43.13 o 3.78 o he b eeding season—da a om bi ds cap u ed in he sal wo ks. In ou s udy a ea he masses o males and emales we e simila : 13  −0.83, P 0.43, and 21  1.59, P 0.13, o win e ing and b eeding bi ds, espec i ely). Females’ appa en ly low en- e gy consump ion could be a consequence o he assump ions we made abou noc u nal o aging. Following Zwa s e al. (1990), we measu ed noc u nal ac i i y wi hin 2 h o low ide and assumed ha he e we e nei he sex- ela ed di e ences in in ake a e no di e ences in o aging bi ds’ sex a io. None- heless, a nigh , emales’ in ake a e should be highe (Kuwae 2007) o hei ac i i y should be highe han we ound in his s udy, wi h emales o aging h oughou he low- ide pe iod. Die did no change by season, wi h he polychae e wo m Ne eis di e sicolo being he plo e ’s p ima y p ey. B eeding is conside ed o be an ac i i y wi h a g ea equi emen o p o ein (Mu phy 1994). Ne eis di e sicolo is a p o ein- ich in e eb a e wi h a p o ein con en 50% (Cas o e al. 2008), sugges s ha i p o ides he plo e he p o ein i equi es o b eeding, so ha i does no need o shi i s die du ing he b eeding season. The Ken ish and Snowy Plo e s a e unde going a sha p nume ical decline in Eu ope and he Ame icas (B own e al. 2000, Delany and Sco 2006). To he bes o ou knowledge, no p e ious s udies ha e es ima ed he seasonal a ia ion in his species’ in ake a es. Ou esul s indica e ha , o ealis- ic assessmen s o p ey acquisi ion, ene gy budge s, o habi a quali y, he species’ conse a ion plans should ake in o ac- coun hese a ia ions in in ake a es. ACKNOWLEDGMENTS We a e g a e ul o Gonzalo Muñoz and S. Ma in o hei field assis- ance and o Isabel To ija and Angeles Muñoz o hei help wi h iden i ying in e eb a es. We also hank he s a o he en i onmen- al o fice o Cádiz Bay Na u al Pa k o acili a ing all he pe mis- sions and he company Unión Saline a o allowing us o s udy a he Salinas La Tapa. LITERATURE CITED AMAT, J. A., R. M. FRAGA,AND G. M. ARROYO. 1999. B ood dese - ion and polygamous b eeding in he Ken ish Plo e Cha ad ius alexand inus. Ibis 141:596–607. AMAT, J. A.,G. H. VISSER, A. PÉREZ-HURTADO,AND G. M. ARROYO. 2000. B ood dese ion by emale sho ebi ds: a es o he di e - en ial pa en al capaci y hypo hesis on Ken ish Plo e s. P oceed- ings o he Royal Socie y o London B 267:2171–2176. AMAT, J. A., AND J. A. MASERO. 2007. The unc ions o belly-soaking in Ken ish Plo e Cha ad ius alexand inus. Ibis 149:91–97. BELL,G. P. 1990. Bi ds and mammals on an insec die : a p ime on die composi ion analysis in ela ion o ecological ene ge ics. S udies in A ian Biology 13:416–423. BROWN,S., C. HICKEY, B. GILL,L.GORMAN,C.GRATTO-TREVOR, S. HAIG, B. HARRINGTON, C. HUNTER, G. MORRISON, G. PAGE, P. SANZENBACHER,S.SKAGEN,AND N. WARNOCK. 2000. Na ional