J. Avian Biol. 40: 388�399, 2009

doi: 10.1111/j.1600-048X.2008.04620.x# 2009 The Authors. J. Compilation # 2009 J. Avian Biol.

Received 2 June 2008, accepted 20 October 2008

Flexibility in the bimodal foraging strategy of a high Arctic alcid, thelittle auk Alle alle

Jorg Welcker, Ann M. A. Harding, Nina J. Karnovsky, Harald Steen, Hallvard Strøm andGeir W. Gabrielsen

J. Welcker (correspondence), H. Steen, H. Strøm and G. W. Gabrielsen, Norwegian Polar Inst., Polarmiljøsenteret, 9296 Tromsø, Norway.E-mail: jorg.welcker@npolar.no. � A. M. A. Harding, Alaska Pacific Univ., Environm. Sci. Dept., 4101 Univ. Drv., Anchorage, AK 99508,USA. � N. J. Karnovsky, Pomona Col., Dept. of Biol., 175 W. 6th St., Claremont, CA 91771, USA.

A bimodal foraging strategy has previously been described for procellariiform seabird species and is thought to haveevolved in response to local resource availability being too low for adult birds to meet chick requirements andsimultaneously maintain their own body condition. Here, we examine the dual foraging trip pattern of an alcid, the littleauk Alle alle, at five colonies with contrasting oceanographic conditions. In spite of large variation in local conditions,little auks at all colonies showed the same general pattern of alternating a single long-trip with several consecutive short-trips. However, we found that the foraging pattern was flexible and could be adjusted at three levels: (1) the length oflong-trips, (2) the frequency of short-trips, and (3) the total time spent foraging. Birds facing unfavorable conditionsincreased the duration of long-trips and reduced the number of short-trips. These adjustments resulted in reducedprovisioning rates of chicks despite the fact that birds also increased the time allocated to foraging. Travel times duringforaging trips were positively correlated to the total duration of the trip suggesting that differences in trip length amongcolonies were partly driven by variation in the distance to foraging areas. Most birds spent substantially more timetraveling during long compared to short-trips, indicating that they accessed distant foraging areas during long-trips butremained close to the colony during short-trips. However, the difference in travel times was small at the site with the mostfavorable conditions suggesting that bimodal foraging in the little auk may be independent of the existence of high-quality areas at distance from the breeding ground.

As central place foragers, breeding seabirds often faceenergetic constraints due to high travel costs incurred bythe need to frequently return to the colony to feed theoffspring, and the sparse, patchy and unpredictable dis-tribution of food resources in the marine environment (e.g.Ashmole 1971, Ricklefs 1990). If resource availability closeto the breeding colony is limited, parents may be unable tosimultaneously meet chick requirements and maintain theirown body condition by use of these near-shore food sourcesalone. Several seabird species facing such conditionsrespond by adopting a bimodal foraging strategy wherebythey alternate feeding trips of long duration to utilize highlyprofitable foraging areas at distance to the breeding groundwith a single or several consecutive trips of short durationin resource-poor near-shore areas (e.g. Chaurand andWeimerskirch 1994, Weimerskirch et al. 1997, Catardet al. 2000). Short-trips serve to increase the feedingfrequency of the chick but yield a negative energy balanceto the parents. In contrast, during long-trips birds pre-dominately feed for themselves restoring body reserveswhich are then expended during subsequent short-trips(e.g. Weimerskirch 1998). The decision to initiate eithera long or short-trip is thereby thought to be under the

control of adult body condition. It has been suggested thatlong-trips are triggered by the proximity of a lower bodymass threshold below which mortality risks are increased(Weimerskirch et al. 1999, 2003). Thus, the dual strategycan be interpreted as a compromise between the need of theoffspring to be fed frequently and that of the adults toforage efficiently to enhance their own survival and futurefecundity.

In some seabird species, the bimodal foraging strategy isthought to be a facultative response to annual or geographicvariation in trophic conditions. In years when local resourceavailability is high, adult birds exhibit a unimodal strategybased on the utilization of local resources alone, whereasthey adopt the bimodal strategy when local conditions arepoor (Granadeiro et al. 1998). In the same way, the modeof foraging may differ spatially between colonies of the samespecies, presumably due to geographic variation in localfood availability (Waugh et al. 2000, Congdon et al. 2005).Although bimodal foraging is generally linked to poor localforaging conditions little information is available on howvariation in resource availability affects the behavior of dualforagers. There is some evidence that the alternate strategymay be adjusted to deteriorating conditions by decreasing

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the number of short-trips and increasing the length of long-trips (Duriez et al. 2000). By doing so, parents may be ableto mitigate higher foraging costs and maintain their ownbody condition at the cost of reduced chick provisioning(Duriez et al. 2000).

There is mounting evidence that bimodal foragingbehavior is a general feature of the life-history strategy ofprocellariiform seabirds (e.g. Weimerskirch et al. 1994,Granadeiro et al. 1998, Booth et al. 2000, Waugh et al.2000). However, indication of dual feeding outside thistaxon is very limited (Benvenuti et al. 1998, Clarke 2001).One exception is the little auk Alle alle, a small, high Arcticalcid, for which a bimodal foraging strategy has recentlybeen described (Steen et al. 2007). Although the bimodalpattern of foraging trips of little auks is similar to that of thesmaller Procellariiformes (e.g. Congdon et al. 2005), thetemporal and spatial scale of their feeding behavior differssubstantially. In contrast to procellariiform dual foragers,little auks usually provision their chicks several times a day(Stempniewicz and Jezierski 1987, Harding et al. 2004).Also, their maximum foraging range is thought to extend nomore than 100 to 150 km from the colony (Brown 1976),an order of magnitude less than that of many Procellar-iiformes (e.g. Catard et al. 2000).

Little auks are zooplanktivorous, with three calanoidcopepod species accounting for up to 90% of their diet(Mehlum and Gabrielsen 1993, Karnovsky et al. 2003,Wojczulanis et al. 2006). The quality of little auk foragingareas is to a large extent determined by ocean temperaturebecause the distribution and abundance of Calanus cope-pods and water temperature are closely linked (Falk-Petersen2007, Loeng and Drinkwater 2007). Calanus speciesassociated with cold water are up to 25% higher in lipidand total energy content than species associated with warmerwater masses (Scott et al. 2000), and accordingly little auksprefer cold water masses as their foraging habitat (Weslawskiet al. 1999, Karnovsky et al. 2003).

In this study we examine spatial variation in the foragingbehavior of the little auk over a wide range of local foragingconditions. We examine: (1) foraging trip durations at fivedifferent breeding sites located across a large part of thespecies’ global distribution to determine whether bimodalfeeding is an intrinsic feature of the foraging strategy of thisnon-procellariiform species or a facultative response togeographic variation in local food availability, (2) assess howforaging trip patterns are adjusted with respect to localoceanographic conditions and how these modificationsaffect chick provisioning rates, and (3) use activity dataobtained from miniature time-depth recorders to investigatewhether the dual feeding strategy in this species isdetermined by the distance of foraging areas from thebreeding sites.

Material and methods

Study area and species

Field work for this study was conducted at five differentbreeding sites of little auks adjacent to the Greenland andBarents Sea in the Arctic zone of the Atlantic. Data wascollected during the chick-rearing period in July and earlyAugust 2007 at Kap Hoegh on the east coast of Greenland(708 43?N, 218 38?W; hereafter called ‘‘East Greenland’’),Ellasjøen on Bear Island between mainland Norway andSpitsbergen (748 23?N, 198 01?E; hereafter called ‘‘BearIsland’’), and at Hornsund (778 00?N, 158 22?E), Isfjorden(788 12?N, 158 20?E) and Kongsfjorden (798 01?N, 12825?E), all three located on the west coast of Spitsbergen (seeFig. 1).

Oceanographic conditions differ substantially betweenthese study sites. The east coast of Greenland is character-ized by cold water masses of polar origin which are carriedsouthward along the coast by the East Greenland Current

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Figure 1. Map showing the location of the five little auk colonies and the areas for which sea surface temperature was obtained (indicatedby black boxes). The main ocean currents are illustrated (warm currents are indicated by dark arrows, cold currents by light arrows).

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(Bourke et al. 1987, see Fig. 1). In contrast, the west coastof Spitsbergen is influenced by both cold and warm watermasses of Arctic and Atlantic origin, respectively. ColdArctic water originating from the Barents Sea is transportedby the South Cape Current northwards on the shelf, whilerelatively warm Atlantic water is brought to the area by anextension of the North Atlantic current (Aagaard et al.1987, Saloranta and Svendsen 2001; Fig. 1). The extent towhich these two main currents affect local hydrographyvaries between the three study sites on Spitsbergen.Oceanographic conditions at Hornsund are mainly domi-nated by cold Arctic derived water masses (Karnovsky et al.2003, and references therein), whereas Isfjorden andespecially Kongsfjorden are to a larger degree influencedby warm Atlantic water (Svendsen et al. 2002, Cottier et al.2005).

Little auks breed almost exclusively on the Arctic islandsof Greenland, Svalbard and Franz Josef Land, so thelocation of our five study sites encompasses a large andimportant part of their geographic breeding range. Littleauks lay their single egg in rock crevices in talus slopes. Thechick is brooded for the first 3�5 d, after which it is leftmostly alone in the nest with parents only visiting briefly tofeed (Stempniewicz 2001). During the post-broodingperiod, parents spend most of their time foraging at sea,diving up to 35 m deep to feed themselves and collect foodfor the chick (Falk et al. 2000). The chick meal is broughtback to the colony in an expandable gular pouch which cancontain up to 4,000 prey items (Karnovsky et al. 2003).The chick is fed regularly by both parents until the end ofthe chick-rearing period when females tend to reduce theirprovisioning effort and leave the colony prior to fledging(Harding et al. 2004). Chicks normally fledge at a mean ageof 25�28 d when they have reached about 2/3 of the bodymass of the adults (Stempniewicz 2001). Little auks haveshort wings as an adaptation for wing-propelled diving, andtheir low wing length/body mass ratio consequently resultsin high energy expenditure during flight (Pennycuick 1987,Gabrielsen et al. 1991).

Foraging trip duration

To determine feeding trip duration and pattern weconducted direct behavioral observations of individuallymarked birds at the study site in East Greenland and thethree colonies in Spitsbergen. Observations at each of thefour colonies took place during the mid chick-rearingperiod, when chicks were no longer being brooded andbefore females started to leave the colony. Median chick ageat the time of observation varied only slightly between thestudy sites (East Greenland�13 d, Hornsund�11 d,Isfjorden�16 d and Kongsfjorden�19 d).

At each site, a suitable part of the colony was chosenwhere several entrances of active nests could simultaneouslybe observed without affecting the behavior of the birds. Inorder to enhance the visibility of nest sites, blinds were usedat Kongsfjorden and East Greenland. Birds were eithermarked during the previous breeding season or several daysprior to the observations by individual combinations ofthree plastic color leg bands or with temporary colormarkings by marker pen on the breast feathers. At least

two observers took shifts of 6�8 h, recording time of colonyarrival and departure of all marked birds and whether or notadults returned with food for the chick. The duration of aforaging trip was defined as the time between the colonydeparture of an individual with an empty gular pouch andits return to the colony with a full pouch. Observationswere conducted continuously for 48 h, starting July, 25th inHornsund and Isfjorden, and July, 26th in Kongsfjordenand East Greenland. At East Greenland, a second observa-tion period was conducted starting August, 9th. In total,foraging trip lengths were recorded for 17 (East Greenland),25 (Hornsund), 23 (Isfjorden) and 15 (Kongsfjorden)individuals, respectively.

At Bear Island, an automatic passage recording systemwas used to determine the pattern of foraging trips. Thetube-shaped system, consisting of a PIT (passive integratedtransponder) tag antenna (see Steen et al. 2007, for details)and a photoelectric switch was placed at six nest entrances.At each passage of a PIT-tagged bird, the date, time and theindividual identification number were logged as well as thetime the bird passed the photoelectric switch. By thechronological sequence of the two events the direction ofthe movement of the bird in or out of the nest wasdetermined. Data from six individuals were collectedcontinuously for 6�18 d starting July, 25th (mean chickage�10 d). Using this system, the length of a foraging tripwas defined as the time period between nest departure andthe subsequent re-arrival at the nest. This measurementcomprised both the time spent at sea and the time spent atthe colony outside the nest (Steen et al. 2007), andestimates of trip duration from Bear Island were thereforenot directly comparable to estimates derived from directobservations. Consequently, data from Bear Island wereonly used to examine the pattern of foraging trips but wereexcluded from all analyses of inter-colony variation of thedual foraging strategy.

Travel time and foraging ranges

The foraging trips of little auks usually consist of three mainactivities: flying, resting at sea and active diving. Todetermine the amount of time birds spent flying during agiven foraging trip we used miniature time-depth recorders(hereafter abbreviated TDR) at three of the study sites (EastGreenland, Hornsund and Kongsfjorden).

Birds were caught on the nest or with a mist net duringthe first half of the chick-rearing stage (median chick ageat deployment of devices: 5 d (East Greenland), 3 d(Hornsund) and 4 d (Kongsfjorden)), and fitted with G5data storage tags (Cefas, Suffolk). The tags (2.7 g in air,31�Ø 8 mm, 8 Mb memory) weighed less than 2% of thebody mass of the birds and were programmed to recordtemperature and depth every 5 s for up to 5 d. Its sensorsallowed for a 12 bit resolution (resulting in a depthresolution ofB0.04 m and a temperature resolution of0.038 C) and an accuracy of 91 m (depth) and 90.18 C.The devices were attached ventrally to the body feathers atapproximately the midpoint of the center-line of the birds’body, using cyanoacrylate adhesive. The position of thedevice ensured that the loggers were in permanent contactwith seawater whenever the birds landed at sea (Tremblay

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et al. 2003). Birds were recaptured within 2 to 5 d afterdeployment, the TDRs were removed and the data down-loaded to a computer. Thus, we were able to collect a totalof 1,654 h of data of 6, 11 and 7 individuals in EastGreenland, Hornsund and Kongsfjorden, respectively.

By visual inspection of the temperature and depth curvesof the dataset of each individual we determined 3 main typesof behavior � colony attendance, flight and time on the water(Tremblay et al. 2003, 2005; see also Fig. 2). Colony arrivalwas unambiguously characterized by a sudden and steepincrease in temperature as the proximity of the device to thebody of the bird resulted in a temperature rise ofapproximately 15�208 C above air temperature. Tempera-ture decreased rapidly again upon colony departure,approaching a level characteristic for flying. This level variedslightly between individuals and was typically somewhathigher than air temperature presumably depending on theexact location of the logger on the bird. As air temperature atall study sites was mostly higher than ocean temperature,landing at sea was normally followed by a rapid decrease intemperature whereas take-off from the water was associatedby a prompt increase in temperature. Finally, time on thewater was characterized by relatively stable temperatureswith slight fluctuations during active diving.

The amount of time an individual spent traveling withina given foraging trip was calculated as the sum of all flyingbouts from colony departure to subsequent re-arrival at thecolony. Time on the water was defined as total trip lengthminus the time spent flying and comprised both resting atthe sea surface and active diving. To classify a foraging trip aseither long or short we applied the cut-off values we derivedfrom observational data (see below). We estimated the site-specific maximum foraging range for long and short-tripsbased on mean flight times divided by two and multiplied byan estimated flight speed of 20 m s�1 (Pennycuick 1987,Elliott et al. 2004). Our estimates of foraging range imply adirect line of flight between the breeding site and the feedingarea and must therefore be regarded as an upper bound ofthe potential foraging distance.

Sea surface temperature

To characterize local oceanographic conditions and evaluateforaging conditions for little auks during the study periodwe calculated the mean sea surface temperature (SST, 8 C)for July 2007 for an area of about 4,000 km2 adjacent to thecolonies in East Greenland, Hornsund, Isfjorden andKongsfjorden (see Fig. 1). Satellite data with a spatialresolution of 10�10km and a temporal resolution of 12 hwas provided by the EUMETSAT Ocean and Sea IceSatellite Application Facility (OSI SAF). Due to restrictionsimposed by cloud cover, data was available for 7 to 13 d atthe different sites. We derived the mean July SST for eachsite by averaging daily means based on all data pointsavailable within the selected areas.

Data analysis

The frequency distribution of the foraging trip lengths wasbimodal at all five colonies (see results). However, theclassification of single trips as either long or short based onthe frequency distribution alone was not straightforward inall cases. To obtain an unbiased data driven cut-off value forseparating the two types of trips we applied the followingmethod: The bimodal distribution of the full datasets canbe considered as two separate log-normal distributions ofshort and long-trips, respectively. We regarded the cut-offvalue to be best that minimized the sum of the variances ofboth trip types given their log-normal distribution. First, wearbitrarily set the cut-off point at a trip length of 4 h, avalue well within the range of short-trips, and calculated thevariance of both short and long-trips given that cut-offpoint. We then repeated the procedure by stepwiseincreasing the cut-off value at 0.1 h intervals to 9 h, a valuewell within the range of long-trips, and selected the cut-offpoint that resulted in the lowest sum of the variances. Thiswas done separately for each study site. The derived cut-offpoints varied slightly between sites, ranging from 5.4 h atHornsund to 7.6 h at Kongsfjorden (see also Fig. 3) and

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Figure 2. Determination of three main types of little auk behavior (flight (light-gray bar), at sea (dark-gray bar) and colony attendance(black bar)) determined from continuous temperature (bold black line) and depth (gray line) measurements derived from time-depthrecorders (see text for details). The illustrated example is based on 6.5 h of data from one individual at Hornsund, Spitsbergen.

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were applied to classify all trips as either short or long forsubsequent analyses.

To examine geographic variation in foraging trip lengthsand their relationship with sea surface temperature we usedlinear mixed effects models (LME) with location and seasurface temperature, respectively, as fixed effects. Toaccount for repeated measurements of the same individuals,‘‘individual’’ was included in the models as a random factor.Separate models were fitted for long and short-trips.Likewise, linear mixed effects models were used to test forspatial variation in travel time and the time spent at sea, andto test for differences in trip time estimates betweenobservational and TDR data. To test for a possible diurnalpattern in the timing of foraging trips we fitted a general-ized linear model with quasipoisson error distribution andlogarithmic link function on the number of trips initiated inrelation to time of day (split in four 6 h periods: 01:00�06:59, 07:00�12:59, 13:00�18:59, 19:00�00:59, localtime). We included ‘‘location’’, ‘‘trip type’’ (long vs. short)and their interaction in this model. Simple analysis ofvariance (ANOVA), and covariance (ANCOVA), wereapplied to examine inter-colony differences in the frequencyof short-trips, the chick feeding rate and in time allocation.

The frequency of short-trips was defined as the number ofshort-trips an individual performed in between two long-trips. Individuals for which only one long-trip was recordedduring the observation period were excluded from theanalysis. The chick feeding rate was assumed to be reflectedby the number of times per day an individual returned tothe colony with a filled gular pouch. Data from Bear Islandwere not included in these analyses as the data collectedwith PIT tags were not directly comparable to theobservational data (see above).

To meet the condition of normality data were trans-formed when necessary. All statistical analyses were done inR 2.2.1 (R Development Core Team 2006). Throughoutthis paper we report mean values 91 SE unless otherwisestated. Tests are two-tailed and PB0.05 is regarded asstatistically significant.

Results

Sea surface temperature

The mean July sea surface temperature varied significantlybetween study sites (ANOVA, F3,41�51.38, PB0.001;

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Figure 3. Frequency distribution of little auk foraging trip durations. Short-trips are indicated by dark bars and long-trips by gray bars.Lower right panel shows the sequence of long and short foraging trips over 48 h, exemplarily illustrated by one individual from each studysite.

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Fig. 4). SST was lowest at the East Greenland colony (0.068C,90.34), and increased in Spitsbergen from Hornsund(1.968C, 90.50), to Isfjorden (4.998C, 90.27), andKongsfjorden (5.648C, 90.17).

General foraging trip pattern

In total, we determined the duration of 738 foraging tripsof 86 individuals. The frequency distribution of foragingtrip lengths was clearly bimodal in all five colonies, with aclear distinction between trips of long and short duration.Short-trips lasted between about 0.4 and 6 h, long-tripsranged from about 7 to 35 h (Fig. 3).

Birds from all study sites showed the same distinctivepattern of alternating long and short-trips, in which a longfeeding trip was followed by a succession of several, usually2�6, short-trips (Fig. 3). This pattern was universal; none ofthe observed individuals went on only short or long-trips.Additionally, in only 8 out of the 738 (1.1%) observedcases, birds performed two consecutive long-trips beforeinitiating a short-trip cycle.

We did not find evidence of a diurnal pattern in thetiming of either long or short-trips. The number of initiatedforaging trips was independent of the time of day (GLM:x2�1.20, df�3, P�0.753), and this relationship did notdiffer between long and short-trips (GLM: x2�1.02, df�3, P�0.796), nor between colonies (GLM: x2�8.83,df�9, P�0.453).

Geographic variation in trip length and pattern

The length of long-trips varied significantly among colonies(Fig. 4, LME: F3,58�15.93, PB0.001). The duration oflong-trips was shortest at East Greenland (9.57 h90.485)and increased on Spitsbergen from Hornsund (11.68 h90.773) to Isfjorden (13.94 h90.973) and Kongsfjorden(17.04 h91.181), where little auks spent on average 78.1%more time on a long-trip than at East Greenland (Table 1).Accordingly, long-trip length was strongly positively relatedto sea surface temperature (LME: F1,60�44.20, PB0.001). In contrast, there was only slight variation in thelength of short-trips between study sites (Fig. 4; LME:F3,67�2.27, P�0.088). Mean duration of short-tripsranged from 2.03 h90.110 (Hornsund) to 2.41 h90.106(Kongsfjorden, Table 1). Moreover, there was no significantrelationship between short-trip length and sea surfacetemperature (LME: F1,69�2.13, P�0.149).

Despite the stereotyped alternation of the two types oftrips there was large individual variation in the number ofshort-trips birds performed in-between long-trips, with ashort-trip cycle consisting of between 1 to 10 trips (mean�3.2490.262). The frequency of short-trips was negativelyrelated to the mean length of the long-trips amongindividuals, e.g. little auks performing extended long-tripscarried out fewer short-trips before the subsequent long-trip than birds with shorter mean long-trip duration(ANCOVA: F1,47�6.12, P�0.017). This relationship

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Figure 4. Inter-colony variation in the duration of long and short foraging trips (mean91 SE; upper panel) of little auks and sea surfacetemperature (SST, mean91 SE; lower panel) for an area of approx. 4,000 km2 adjacent to each colony in July 2007. Note that data fromBear Island were collected by a different method and are therefore not directly comparable to the other four study sites (see Material andmethods section for details).

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did not differ between colonies (ANCOVA: factor ‘‘loca-tion’’ and all interaction terms P�0.05).

Accordingly, the mean number of short-trips per long-trip tended to be higher at colonies where birds performedlong-trips of shorter duration (Table 1). However, thistendency was statistically not significant (ANOVA: F3,64�0.53, P�0.664). On average, little auks at East Greenland,the site with the shortest long-trip duration, completedapproximately one short-trip more between long-trips thanbirds at Kongsfjorden where the number of short-trips wasthe least (Table 1).

Time allocation and chick feeding rate

The proportion of time little auks spent on foraging tripsvaried significantly between study sites (arcsine transformeddata, ANOVA: F3,55�13.46, PB0.001, see Table 1)and increased with increasing sea surface temperature(ANCOVA: F1,57�35.79, PB0.001). Hence, birds atcolonies with high sea surface temperature allocated moretime to foraging and spent less time in the colony than birdsat colonies with low sea surface temperature.

The number of feedings a parent little auk deliveredto its chick was mainly determined by the duration of itslong-trips and the frequency of short-trips. Chick feedingrates decreased with increasing duration of long forage tripsand increased with increasing frequency of short-trips(ANCOVA: ‘‘LT duration’’: F1,46�54.02, PB0.001;‘‘ST per LT’’: F1,57�8.68, P�0.005). These relationshipsdid not differ among study sites (ANCOVA: factor‘‘location’’ and all interaction terms P�0.05).

The mean number of chick feedings per day at thedifferent colonies reflected these relationships (Table 1). AtKongsfjorden, birds completed on average 1.2 fewer feedingtrips per day than at East Greenland and hence, chicks atKongsfjorden received approximately 25% fewer feedingsper day than their conspecifics at East Greenland. Indivi-duals at Hornsund and Isfjorden conducted intermediatenumbers of foraging trips per day (Table 1).

Travel times during foraging trips

The time little auks spent flying during a given foraging tripwas strongly positively correlated to the total duration ofthe trip (LME: F1,135�322.52, PB0.001; TDR data).Surprisingly, travel time did not differ significantly betweenlong and short-trips at all the three colonies studied.Foraging birds spent significantly more time travelingduring long-trips than during short-trips at Hornsund(LME: t��2.71, df�134, P�0.008) and Kongsfjorden(LME: t��4.84, df�134, PB0.001), but not at EastGreenland (LME: t��1.82, df�134, P�0.071, seeTable 2).

During long-trips, the time spent traveling differedsignificantly amongst the three colonies where TDRs weredeployed (Fig. 5, LME: F2, 19�6.21, P�0.008). Indivi-duals at Kongsfjorden spent more than three times as longtraveling than their conspecifics at East Greenland(6.09 h90.481 vs. 1.91 h90.304). Birds at Hornsundhad intermediate travel times (3.60 h90.448). Flightduration corresponded to a maximum potential foragingrange of 69, 130 and 219 km for East Greenland,Hornsund and Kongsfjorden, respectively (Table 2). How-ever, differences in travel times alone did not fully accountfor the variation in the duration of long-trips amongcolonies as the time spent on the water (resting and activediving) also differed significantly between sites (Fig. 5,LME: F2,19�5.82, P�0.011).

Comparison of observational and TDR data

Estimates of the mean duration of long-trips did not differbetween the two methods applied in this study (Fig. 6; LME:F1,61�2.88, P�0.095). However, mean length of short-trips was significantly affected by the method of datacollection (LME: F1,71�20.88, PB0.001). Separate mod-els for each site revealed that estimated short-trip durationdiffered between observational and TDR data in Hornsund(LME: F1,31�22.30, PB0.001), but not in East Greenland

Table 1. Provisioning parameters of little auks from four different colonies (mean91 SE). Sample size (number of observed foraging trips (LTand ST duration) and number of individuals, respectively) is given in parentheses.

East Greenland Hornsund Isfjorden Kongsfjorden

LT duration (h) 9.5790.49 (20) 11.6890.77 (22) 13.9490.97 (20) 17.0491.18 (19)ST duration (h) 2.0990.14 (98) 2.0390.11 (79) 2.0390.10 (128) 2.4190.11 (79)ST per LT 3.7590.60 (12) 3.5390.50 (11) 3.0390.49 (20) 2.8790.50 (12)Foraging trips/d 4.8790.46 (15) 4.0590.28 (15) 4.3790.32 (23) 3.7190.26 (15)Time spent on foraging trips (%) 80.192.03 (15) 86.591.70 (15) 92.990.96 (23) 91.091.26 (15)

Table 2. Time spent traveling and time on the water, and estimated maximum foraging ranges associated with foraging trips of long (LT) andshort (ST) duration at three little auks colonies (mean91 SE). Sample size is given in parentheses.

East Greenland Hornsund Kongsfjorden

n (Individuals) 6 11 7Travel time (h) LT 1.9190.30 (7) 3.6090.45 (37) 6.0990.48 (20)

ST 0.6490.08 (12) 0.3290.02 (55) 0.9290.11 (30)Time on water (h) LT 7.9090.64 (7) 9.4190.68 (37) 13.6791.32 (20)

ST 1.2990.39 (12) 1.0390.14 (55) 1.5890.25 (30)Maximum foraging range (km) LT 68.61910.93 (7) 129.46916.14 (37) 219.11917.32 (20)

ST 22.8093.00 (12) 11.6090.90 (55) 32.9693.83 (30)

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(LME: F1,20�0.78, P�0.389) and Kongsfjorden (LME:F1,20�1.86, P�0.189).

Discussion

Foraging conditions

Sea surface temperature varied significantly among studysites and corroborated the expected differences in oceano-graphic conditions associated with the main ocean currentsof the study area (Fig. 1). Sea surface temperatures of 58 Cand more as measured in Isfjorden and especially Kongsf-jorden reflect a strong inflow of Atlantic water, whereas thelower sea surface temperatures at Hornsund and EastGreenland indicate a predominance of Arctic water massesat these sites (e.g. Svendsen et al. 2002, Cottier et al. 2005).

These differences in oceanographic conditions are likely tohave had a strong effect on the foraging conditions of littleauks. Cold, Arctic water masses are characterized by anabundance of the large and energy-rich calanoid copepodspecies Calanus glacialis and C. hyperboreus (Hirche et al.1994), the preferred prey species of little auks (Karnovsky etal. 2003). In contrast, warm Atlantic water masses containlarge quantities of the smaller and energetically less profit-able Calanus finmarchicus. It can therefore be expected thatlittle auks at sites with high sea surface temperature weresubject to inferior local foraging conditions compared tosites with low temperature.

Bimodal pattern

The results of the present study indicate that a bimodalforaging strategy is a general feature of the feeding behaviorof little auks during the chick rearing period. Individualsfrom five colonies located across a large part of the species’geographic breeding range showed a similar bimodalpattern of alternating trips of short and long durationdespite large inter-colony variation in local oceanographicconditions. The bimodal foraging behavior of little auksresembled the dual foraging strategy described for a numberof procellariiform seabirds, such as shearwaters and smallpetrel species (Weimerskirch 1998, Weimerskirch et al.1999, Catard et al. 2000, Congdon et al. 2005). Evidencefor bimodal foraging outside the order of Procellariiformesis very limited. A bimodal distribution of foraging trips withrespect to duration and/or feeding area has been reportedfor adelie penguins Pygoscelis adeliae (Clarke et al. 1998,Ropert-Coudert et al. 2004), and thick-billed murres Urialomvia (Benvenuti et al. 1998). However, the extent towhich the bimodality in these cases resulted from a dualforaging strategy or from a tendency of individuals toperform either long or short-trips remains unknown. Toour knowledge the little auk is the only non-procellariiformspecies for which the strategy of alternating short and long-trips has yet been described (Steen et al. 2007; this study).

The bimodal strategy is thought to be facultative inprocellariiform species that are exposed to high variability inlocal conditions (Granadeiro et al. 1998, Waugh et al. 2000,Congdon et al. 2005). When local food availability is high,these species use a unimodal foraging mode during whichthey are believed to utilize near-shore areas only. Bi-modalityis adopted when conditions deteriorate and local resourceavailability does not suffice to sustain both breeding and self-maintenance. In the present study, local oceanographicconditions varied substantially amongst colonies, andoceanographic conditions are known to largely determinethe food availability of little auks (Weslawski et al. 1999,Karnovsky et al. 2003). However, the general dual patternwas similar at all colonies and we did not find any indicationof little auks using a unimodal strategy at sites with favorablelocal conditions. These results suggest that bimodal feedingis not facultative in this species.

Explanations for the dual strategy in Procellariiformesgenerally imply that during long-trips birds access foragingareas at distance from the breeding ground that areconsiderably and consistently more productive than near-colony waters. In accordance with this explanation, travel

East Greenland Hornsund Kongsfjorden

Tim

e (h

)

0

5

10

15

Figure 5. Total amount of time spent flying (dark bars) and timespent on the water (light bars) during foraging trips of longduration at three different little auk colonies (mean91 SE).

Tim

e (h

)

0

5

10

15

20

25

East Greenland Hornsund Kongsfjorden

Figure 6. Comparison of the mean duration of long and shortforaging trips of little auks at three different colonies estimated byobservational and TDR data. Estimates of long-trip length did notdiffer between observations (black bars) and TDR data (dark graybars) while estimates of short trip length differed in Hornsund butnot the other two sites (observations: light gray bars, TDR: whitebars; see Results).

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times and corresponding maximum foraging ranges of littleauks were significantly longer during long-trips than duringshort-trips at Hornsund and Kongsfjorden suggesting thatbirds from these colonies frequented different areas duringlong and short-trips, respectively. Although we do not havedirect evidence on the direction of flight during foragingtrips, temperature data obtained from TDRs indicates thatflight during long-trips was indeed directed away/towardsthe colony. For example, in Kongsfjorden ocean tempera-ture declined constantly and considerably between flightbouts of long-trips until the foraging area was reached andflight activity almost completely ceased (Karnovsky et al.unpubl. data). The reversed pattern was visible on thereturn travel indicating a close correlation between flightduration and foraging range. Also, a number of studies havefound a strong positive relationship between foraging triplength and foraging distance (e.g. Weimerskirch et al. 1997,Hamer et al. 2000, 2001) further supporting the notionthat little auks foraged at distant areas during long-trips.Long travel distances were unexpected because the energeticcosts of flight are thought to be high in little auks(Gabrielsen et al. 1991), and consequently may reduceforaging efficiency substantially. Foraging areas reachedduring long-trips therefore need to be higher in foodabundance and/or quality than near-shore areas to allowbirds to compensate for high travel costs. These areas havenot yet been identified, but are likely to be characterized bya constant inflow of cold Arctic water masses that are highin energy-rich mesozooplankton species (Weslawski et al.1999, Karnovsky et al. 2003).

In contrast, differences in mean flight duration betweenlong and short-trips at the East Greenland site were slightand statistically not significant. Moreover, local foragingconditions at this colony were presumably favorable asindicated by low sea surface temperatures. Hence, the twomain conditions thought to lead to the development of abimodal foraging strategy, poor near-shore feeding condi-tions and utilization of distant foraging areas, did not applyto East Greenland birds. Although little auks at this colonywould therefore be expected to conduct foraging trips ofunimodal length, birds remained close to the colony andstill conducted foraging trips of bimodal length.

An alternative explanation recently proposed by Con-gdon et al. (2005) may account for this apparent contra-diction. Congdon et al. (2005) suggested that a bimodalstrategy may help birds to minimize travel costs andtherefore be advantageous even when birds remain closeto the colony during long-trips. The ability to minimizetravel costs may be especially important for the little auk.The flight costs of an individual with a given wingmorphology are mainly determined by its body mass(Pennycuick 1989). For instance, a 10% decrease in thebody mass of little auks results in a similar reduction offlight costs (Harding et al. 2009). Little auks have high fieldmetabolic rates and therefore need to consume foodequivalent to about 80% of their body mass per day inorder to cover their own energy requirements (Gabrielsen etal. 1991). In fact, only 15% of the total daily energy gainsare delivered to the offspring, even at times when chickrequirements are highest (Konarzewski et al. 1993).

Given the duration of time required for digestion, littleauks using a unimodal strategy would likely be required to

travel with large amounts of food ingested, therebyincreasing their body mass and flight costs substantially.Conversely, remaining at sea for extended periods mayenable birds to acquire, process and excrete the amount offood needed for self-maintenance completely before com-muting to the colony, reducing flight costs in the process(Gabrielsen 1996). Hence, energetic requirements for travelusing a bimodal strategy may be less compared to aunimodal strategy, thus making dual foraging profitablein this species irrespective of travel distances.

The two explanations for bimodal foraging are notmutually exclusive and may both, as our results indicate,account for the observed behavior in little auks.

Geographic variation in the bimodal pattern

We found strong indication that the dual strategy of littleauks was adjusted in response to spatial variation in seasurface temperature. Modifications took place at threedifferent levels: the length of long-trips, the frequency ofshort-trips and the total time spend foraging. The durationof long foraging trips varied substantially between differentbreeding sites, increasing dramatically with increasing seasurface temperature. Mean long-trip length at Kongsfjorden,the site with the highest sea surface temperature, was approx.70% longer than at East Greenland, the site with the lowestsea surface temperature. A similar adjustment of long-tripduration has been found in two small petrel species, theAntarctic prion Pachyptila desolata, and the thin-billed prionPachyptila belcheri (Weimerskirch et al. 1999, Duriez et al.2000). In years with unfavorable conditions individuals ofthese species increased the length of long-trips, which wasthought to be the result of an increase in the distance toprofitable feeding areas (Weimerskirch et al. 1999). Inaccordance, we found that differences in trip duration inlittle auks were partly driven by variation in travel times.Time spent flying increased more than three-fold betweenthe site with the shortest to the site with the longest meantrip duration. This indicates a positive relationship betweentrip duration and the distance to preferred feeding areas.However, inter-colony variation in trip length resulted notonly from differences in the distance to foraging areas butalso from different amounts of time spent in foraging areasonce they were reached. Birds may have to spend more timeforaging to compensate for additional energetic costsincurred by longer travel distances.

We found only little inter-colony variation in the lengthof short-trips in spite of large variation in local oceano-graphic conditions. Based on our observational data, meanduration of short-trips was approx. 2 h at all sites. Twoexplanations may account for this. Firstly, because parentspresumably forage solely to provision the chick duringshort-trips, the effect of variation in food availability on thetime required to collect one chick meal might be small andmay have remained undetected given our sample size.Higher variation in short-trip length among TDR-birdssupports this idea.

Alternatively, the length of short-trips may be deter-mined by an endogenous rhythm of the adults optimizingthe feeding frequency of chicks. A regular and frequentprovisioning rate is likely to enhance chick development

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(Schaffner 1990). In little auks, a feeding rate of roughlyevery two h may be optimal for chicks to process andassimilate food and hence facilitate maximum chick growth.This is supported by the fact that it takes approx. 1.5 � 2 hto process a full meal in thick-billed murres (Hawkins et al.1997). However, a stable chick feeding frequency under abimodal foraging regime would imply coordinated provi-sioning among partners of a pair. Evidence of coordinatedswitching of foraging modes has recently been reported inthe wedged-tailed shearwater Puffinus pacificus (Congdon etal. 2005). In this species, individuals of a pair terminated acycle of short-trips at about the same time their partnerreturned from a long-trip. However, coordinated foragingremains to be tested in little auks.

While the length of short-trips was similar at thedifferent colonies, the frequency of short-trips was not.The number of short-trips little auks completed during ashort-trip cycle was negatively correlated to long-tripduration and consequently there was a tendency for themean frequency of short-trips to decrease with increasinglong-trip duration among colonies. The decision to performanother short-trip or initiate a long-trip after completing ashort-trip is believed to be mainly under the control of adultbody mass (Chaurand and Weimerskirch 1994, Weimers-kirch et al. 1995, Weimerskirch 1998, but see Congdon etal. 2005). When individuals reach a lower mass thresholdthey terminate the short-trip cycle and perform a long-tripto regain body reserves and avoid the risk of starvation.Hence, the number of short-trips individuals are capable ofconducting is determined by the ability to store resourcesduring long-trips and the energetic costs, i.e. the rate ofdepletion of body reserves associated with short-trips. Forinstance, Duriez et al. (2000) found that thin-billed prionswere able to increase the number of short-trips when theirnutritional status was high, i.e. under favorable foragingconditions.

In the present study we did not measure body masschanges. However, it seems likely that the distance littleauks have to travel to profitable foraging areas during long-trips affects the amount of body reserves with which theyreturn. Long distance travelers may partially use the energystored during their return flight and therefore mayapproach the lower mass threshold after fewer short-trips.

Chick feeding rate and resource allocation

The observed inter-colony variation in the bimodal foragingstrategy had strong implications on the number of mealsreceived by the chicks. The increase of long-trip durationand the decrease of short-trip frequency at sites withunfavorable conditions led to a considerable reduction ofthe chick provisioning rate. This was apparent althoughparents also increased their total amount of time allocatedto foraging and reduced the time spent in the colony. Thisflexibility in time allocation is likely to benefit the chicksand buffer the effects of variable conditions (e.g. Litzow andPiatt 2003, Harding et al. 2007). The buffering effect offlexible time budgets is supported by the fact that theobserved inter-colony differences in chick feeding rate weresmaller than expected based on differences in long-tripduration and short-trip frequency. However, our data

suggests that increased foraging effort did not allow birdsto fully compensate for variation in foraging conditions,and chicks at Kongsfjorden received approx. 25% fewerfeedings per day than their conspecifics at East Greenland.This difference is likely to have a strong impact on chickgrowth and/or survival (e.g. Hamer et al. 1991, Kitaysky etal. 2000, Davis et al. 2005).

The dual foraging strategy can be viewed as the result ofan allocation conflict, with birds alternating their resourceallocation between self-maintenance (long-trips) and repro-duction (short-trips). Our study demonstrates that littleauks can adjust their feeding strategy in response todeteriorating foraging conditions through reduced timeallocation to short-trips and increased time allocation tolong-trips. These results indicate that under poor foragingconditions parent little auks redirect resources to them-selves. Additional costs associated with longer traveldistances were at least partly shunted to the chicks asindicated by the decrease in chick feeding frequency.

Acknowledgements � We thank all fieldworkers at the five sites andthe staff of the Polish Polar Station at Hornsund (Institute ofGeophysics, Polish Academy of Science), Sverdrup Station(Norwegian Polar Institute) at Kongsfjorden and NANU travelat Ittoqqortoormiit for their invaluable help in the field. Manythanks to S. Eastwood and O. Pavlova for the preparation of theSST data and to Z. Brown, K. Kampp and an anonymous refereefor constructive comments on an earlier draft of the manuscript.JW, GWG, HS and H. Strøm were supported by the ResearchCouncil of Norway (MariClim, 165112/S30), the Norwegianseabird monitoring project SEAPOP and the Norwegian PolarInstitute. AMAH and NJK were funded by the National ScienceFoundation (grant 0612504). Fieldwork in Greenland wasadditionally supported by the French Polar Institute (Grant388). All field work was conducted with the permission of theGovernor of Svalbard and the Greenland Home Rule Government(Permit 512�240).

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