MARINE ECOLOGY PROGRESS SERIESMar Ecol Prog Ser

Vol. 520: 257267, 2015doi: 10.3354/meps11080

Published February 3

INTRODUCTION

The principle of competitive exclusion, a basic tenetof ecology, states that complete competitors cannotcoexist (Gauze 1934, Hutchinson 1959, Schoener1974). That is, the n-dimensional niche hyper-volumebetween any 2 sympatric (and therefore competing)species must differ (Macarthur 1958, Hutchinson1959, Pianka 1969, Wilson 2010). Nonetheless, manyseabird and marine mammal colonies are character-ized by several co-existing species with apparentlysimilar dietary niches (Diamond 1978, Croxall &Prince 1980, Gaston 2004). Competition is likelystrongest during the reproductive period be cause allindividuals are constrained to feed within a limited

radius of the central place and cannot wander entireoceans searching for an optimal foraging patch (Ash-mole 1963, Gaston et al. 2007). Many cliff- or burrow-nesting seabirds are apparently not limited by nest-sites, and competition must occur at sea (Elliott et al.2009b, Masello et al. 2010, Wakefield et al. 2013),presumably leading to differences in their foragingniches over evolutionary time. In support of this the-ory, sympatric seabird species often have differentforaging strategies (Ishtiaq et al. 2010, Barger &Kitaysky 2012; Table 1).

In northern oceans, several auk species coexist atmany colonies and apparently utilize different forag-ing strategies (Gaston 2004, Elliott et al. 2010b, Thax-ter et al. 2010). For instance, common guillemots Uria

The authors 2015. Open Access under Creative Commons byAttribution Licence. Use, distribution and reproduction are un -restricted. Authors and original publication must be credited.

Publisher: Inter-Research www.int-res.com

*Corresponding authors: akikosho@gmail.com; tim.guilford@zoo.ox.ac.uk

Foraging behaviour of sympatric razorbills and puffins

Akiko Shoji1,*, Kyle Elliott2, Annette Fayet1, Dave Boyle1, Chris Perrins1, Tim Guilford1,*

1Department of Zoology, Oxford University, Oxford OX1 3PS, UK2Department of Integrative Biology, University of Guelph, Guelph, ON N1G 2W1, Canada

ABSTRACT: Many marine predators coexist at colonies, creating a zone where there could be sig-nificant inter- and intraspecific competition. To minimize the potential for direct competition,under the principle of competitive exclusion, sympatric predators may differ in their foraging be -haviour at the colony. At Skomer, Wales, razorbills Alca torda and puffins Fratercula arctica bothbreed at the same time of year, forage on sand eels Ammodytes sp. and their populations are sta-ble or declining, meaning that they may be close to carrying capacity and experiencing competi-tion. To examine how they differ in their foraging behaviour, time-depth-temperature recorderswere attached to the legs of chick-rearing individuals of both species. Puffins have lower wing-loading and lower total oxygen stores than razorbills and are therefore expected to invest moretime in flying and less time in diving than razorbills. Mean (1 SE) dive depth was 11.8 0.45 mfor puffins and 8.2 0.21 m for razorbills, while mean dive duration was 40 0.45 s for puffins and24 0.21 s for razorbills. Both species spent most of their dive time making shallow, V-shapeddives during daylight hours. In contrast to our prediction, foraging behaviour was very similarbetween the 2 species, although puffins tended to spend more time both diving and flying. Thehigher diving and flying rates of puffins may be associated with multiple prey loading, as puffinstend to bring back smaller (and therefore more) prey items than do razorbills.

KEY WORDS: Diving behavior Auks Bio-logging Alcids

OPENPEN ACCESSCCESS

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RESULTS

We retrieved TDRs from 7 puffins Fratercula arc-tica and 7 razorbills Alca torda. All un-retrieved birdswere spotted in the colony after deployment, but wefailed to recapture them. No difference was found inbreeding success between our study birds and con-trol birds that are part of the long-term study runby the Edward Grey Institute at the University ofOxford. In total, we recorded 15 383 dives from razor-bills (n = 7 birds) and 3414 dives from puffins (n = 7birds). Dive duration was longer (t12 = 3.17, p =0.008, GLMM with individual as random effect andtime of day: cos[2 hours since solar midnight] as afixed effect) and dive depth tended to be deeper (t12 =1.90, p = 0.08) for puffins than razorbills (Table 3,Fig. 1). Dive duration was longer (t12 = 4.32, p =0.001, GLMM with individual as random effect anddepth as a fixed effect) and surface interval tended tobe shorter for puffins than for razorbills for a givendive depth (t12 = 2.14, p = 0.05, Fig. 1). More than95% of dives were V-shaped for both species. Puffinsspent 5.7 3.3% of the day flying with average flightduration of 7.47 2.91 min, while razorbills spent 4.9 1.4% of the day flying with average flight durationof 6.45 1.20 min. Including species (razorbill/puffin)did not increase the parsimony for models explainingflight duration (AIC = 1.0). The first 3 principal com-ponents (PC) ex plained >77% of the overall vari-ance, and no other axis explained >10% of the vari-ance (Table 4). Dive depth and number of flights perday loaded heavily and negatively on the first axis,while percentage of time diving loaded heavily andpositively on the second axis (Table 5). Razorbillstended to be associated with a positive first PC axisscore, while puffins tended to be associated with apositive second PC axis score.

260

Shoji et al.: Diving in UK alcids 261

Individual Depth (m) Duration (s) Max. Max. No. of dives No. of dives Bout depth (m) duration (s) per day per bout length (s)

Atlantic puffins515 15.7 12.6 52.2 29.9 47.6 123.1 310 19.6 21.2 1320 1368200 9.8 7.4 33.2 19.8 33.7 90.5 460 25.0 18.1 1023 717152 5.9 3.4 28.0 16.4 23.5 93.7 600 26.6 18.6 1105 8171 7.5 5.9 27.9 19.7 23.9 82.7 416 43.6 28.7 1587 1524523 13.8 11.2 42.6 25.6 37.6 95.5 510 23.6 16.8 1320 771518 12.8 13.5 36.6 27.9 46.4 116.6 283 25.6 26.1 1321 871148 9.7 7.6 57.4 25.4 39.4 105.8 283 11.6 12.8 818 904Mean 11.8 4.2 39.7 11.6 36.0 9.7 101.1 14.6 409 123 25.1 20.3 1213 996

Razorbillsk24763 8.9 6.4 26.1 16.2 56 93 417 17.0 22.1 651 749k24909 5.8 3.7 22.4 10.9 25.1 69.8 448 27.0 33.2 776 946k93793 10.3 5.0 31.1 13.6 25.2 71.4 234 17.1 25.4 839 1172m27931 8.6 4.9 24.1 12.8 26.5 68.2 295 20.0 19.5 724 703m93896 8.2 5.8 22.4 16.0 29.3 64.8 362 14.3 4.5 660 208m93998 6.6 3.2 17.8 10.3 21.6 52.3 511 19.2 26.4 638 759m93924 8.8 5.4 23.5 16.1 31.3 73.4 511 26.3 39.4 1052 1288Mean 8.2 1.5 24.0 4.1 30.7 11.6 70.4 12.1 397 105 20.1 24.4 763 832

Table 3. Dive parameters for Atlantic puffins and razorbills breeding on Skomer, including all dives >2.5 m in depth. Values are (where applicable) mean SD

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Fig. 1. Average (a) depth, (b) duration and (c) number of dives per hour relative to time of day, (d) dive duration relative to divedepth, (e) frequency of dives to different depths and (f) average surface interval duration relative to dive depth, for Atlantic

puffins and razorbills

Mar Ecol Prog Ser 520: 257267, 2015

DISCUSSION

Puffin diving behaviour

Puffin Fratercula arctica dive behaviour was quitesimilar to other non-Uria auk species, consisting pri-marily of many shallow (~5 to 20 m) V-shaped divesduring daylight hours. Not surprisingly, dive depthwas apparently limited by visibility as dive depth wasdeeper during the middle of the day and no diving oc-curred at night (Croll et al. 1992, Regular et al. 2011).The number of dives per hour peaked in the morningand evening, which coincides with the peak in feed-ing rates of offspring by parental puffins at Skomer(Bche et al. 2013). Similar peaks in dive rates afterdawn and before dusk were observed with puffins atthe Isle of May (Wanless et al. 1990, Harris & Wanless2012). We speculate that such a relationship reflects aneed to provide food for the offspring before and afterthe nighttime fasting period and perhaps it requiresmore energy and/or investment to feed.

Puffin dive behaviour at Skomer was quite similarto the dive behaviour elsewhere (Table 1), although

dives were shallower than recorded insome cases by capillary tubes (capillarytubing, closed at one end and dustedwith icing sugar, can be used to deter-mine a single maximum depth over thecourse of deployment based on the maxi -mum distance sea water extends into thetube and dissolves the icing sugar; Kooy-man et al. 1971). Capillary tubes can beinaccurate even over short de ployments,leading to erroneously deep maximumdepths for a species (Elliott & Gaston2009). Nonetheless, our maximum depth(48 m) was deeper than that recorded atour study site using capillary tubes (27 m;

Davidson 1994). Both maximum and average depthof puffins at Skomer was deeper than at Isle of May,perhaps because the bathymetry within the foragingrange of the puffin is generally shallower at Isle ofMay than at Skomer (Fig. A1 in the Appendix). Aver-age dive duration was slightly shorter and maximumduration was slightly longer than predicted based onallometric relationships across all auks (predictedaverage duration: 47 s; predicted maximum duration:114 s; Watanuki & Burger 1999).

Puffins dived on average 409 times per day atSkomer compared with 1148 times per day at the Isleof May (Harris & Wanless 2012). Although averagedive duration at Skomer was longer, the averagehours per day submerged at the Isle of May (7.8 h)was higher than at Skomer (4.6 h). The discrepancy ispartially explained by the timing of deployments, asthe puffins observed at Isle of May included puffinswith older offspring, which likely had higher energydemands necessitating more food and higher diverates (Harris & Wanless 2012). If we assume thatpuffins need to capture 447 sand eels per day to feedtheir young and maintain their own body weight

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Variable PC1 PC2 PC3

Percent of variance explained 32% 25% 20%Average dive depth 0.490 0.211 0.300Maximum depth 0.393 0.302 0.257Average surface interval duration 0.282 0.278 0.127Residual of dive duration on dive depth 0.375 0.429 0.464Number of dives per day 0.349 0.370Percent time spent diving 0.131 0.656Number of flights per day 0.480 0.441Percent of time spent flying 0.367 0.222 0.526

Table 4. Loadings for principal components analysis of dive behaviourbased on average values for each individual. Loadings < 0.1 are not shown.

The component with the highest loading is shown in bold

Location Depth Duration Instruments Source

Isle of May, Britain 4 (20) Time-depth recorder Harris & Wanless (2012)Isle of May, Britain 30 (114) Radio telemetry Wanless et al. (1988)Isle of May, Britain (33) Capillary tube Wanless et al. (1990)Petit Manaan, Maine 9.7 (40.7) Time-depth recorder Spencer (2012)Newfoundland (60) Fishing nets Piatt & Nettleship (1985)Newfoundland (68) Capillary tube Burger & Simpson (1986)Norway (45) Capillary tube Barrett & Furness (1990)Labrador (41) Capillary tube Baillie (2001)Skomer, Britain (27) Capillary tube Davidson (1994)Skomer, Britain 11.8 (47.6) 9.7 (40.7) Time-depth recorder Our study

Table 5. Dive behaviour of puffins as recorded at different locations and by different instruments. Average values of dive behaviour (maximum values in parentheses) are presented

Shoji et al.: Diving in UK alcids

(details in Harris & Wanless 2012), then, based on ourdata, puffins at Skomer likely catch just over 1 fishper dive, compared with

Mar Ecol Prog Ser 520: 257267, 2015

rapidly attack schooling fish from below (Burger etal. 1993). Capturing shallow prey also means that itis relatively easy to track the movement of fishschools from the surface, either because the schoolis visible from the surface or because large concen-trations of surface-feeding predators indicate theschool (local en hance ment; Porter & Sealy 1982,Davoren et al. 2003, Elliott et al. 2009a). Finally,oxygen stores are unlikely to be substantially re -duced during short dives, necessitating less time atthe surface and therefore a higher proportion of bot-tom time throughout a dive bout (Croll et al. 1992,Elliott et al. 2008). Apparently, there are manyadvantages to shallow-diving in auks, as with theexception of guillemots (Croll et al. 1992, Mehlumet al. 2001, Falk et al. 2002, Paredes et al. 2008,Thaxter et al. 2010), few auks regularly dive beyond15 m in depth despite having the capability to do so(Burger & Powell 1990, Burger et al. 1993, Kuroki etal. 2003, Paredes et al. 2008, Elliott et al. 2010b,Thaxter et al. 2010, Brown et al. 2012).

In many ways, the foraging behaviour ofrazorbills and puffins was remarkablysimilar given their differences in size.Certainly, there was no evidence for theclear segregation in dive behaviour and/or flight time apparent in many other sea-bird assemblages (Table 1). Althoughpuffins dived ~3.5 m deeper, both speciesused almost exclusively V-shaped dives,implying that, unlike bottom-feeding Eu-ropean shags (Wa ta nuki et al. 2008), nei-ther was ob taining sand eels from theocean floor; V-shaped dives are primarilyassociated with capturing prey in mid- water, at least in guillemots (Elliott et al.2008). In contrast, guillemots have manyfewer V-shaped dives than razorbills andpuffins, and they forage substantially onbenthic fish (Paredes et al. 2008). Bothpuffins and ra zor bills bring back multiple,small items to their young, but puffinstended to bring more, smaller items thanrazorbills, and the longer dives by puffinsmay have resulted from capturing multi-ple prey per dive. Thus, it could be ex-pected that puffins have a longer bottomtime at a fixed depth as they capture mul-tiple prey items within a school. However,the similarity in shape as demonstratedby a high proportion of V-shaped dives forboth species and the similar relationshipbetween depth and duration suggests

that there is little bottom time at fixed depth for eitherspecies. Our sample size is relatively small, and ourstudy was conducted only within 1 season. Segrega-tion in behaviour amongst species could perhaps oc-cur in years of low but not high prey availability. Thus,future studies could benefit from evaluating behaviourover a longer period. Also, as we were unable to sexindividuals within our study, and sex is known to playa strong role in determining dive behavior in auks(Paredes et al. 2005, 2008, Thaxter et al. 2009, Elliottet al. 2010a, Stauss et al. 2012), it is possible that somevariation was missed due to unbalanced or missingdata from one sex for either species. Similarly, theconstraints of accessi bility and disturbance to coloniescan be severe, and therefore, we were unable to pickindividuals randomly. In stead, study birds were cho-sen at locations with a history of successful breedingand no obvious anomalies. As breeding locations areknown to affect foraging behaviour (Soanes et al.2014), the potential role of sub-colony variation mayhave been missed.

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Fig. 2. Principal component analysis of foraging behaviour averaged acrosseach individual. Loadings of different parameters are shown as vectorswithin the principal component space. Parameters included were the aver-age surface interval duration, average (mean) dive depth, maximum divedepth, average percentage of day spent flying, average percentage of dayspent diving, average number of dives per day, average residual of dive

duration on depth and average number of flights per day

Shoji et al.: Diving in UK alcids

One potential explanation for the similarity in div-ing behaviour is that since the diet is similar betweenthe 2 species, they may have used similar conspecificor inter-specific cues to locate food and may have for-aged on the same fish shoals. Unlike deep-divingseabirds, puffins feed at low densities on small, low-density shoals of fish near the surface, sometimesassociated with tidal rips (Piatt 1990, Wanless et al.1990, Harris & Wanless 2012). We suggest that razor-bills and puffins may have used similar oceano-graphic cues to feed on similar shoals near Skomer.Another possibility, as shown in guillemots, is thatforaging niche may be differentiated only duringyears of poor food availability (Barger & Kitaysky2012). When considered together in a multivariateframework, it was clear that many of the parameterswere intercorrelated such that the main differenceappeared to be that puffins worked harder thanrazorbills: they dived deeper and spent more timeflying and diving (Fig. 2). Puffins ability to workharder, possibly associated with a 25% lower wing-loading and therefore lower flight costs leaving moreresidual energy to be expended on diving or addi-tional flying, may lead to higher feeding rates andexplain how they can provision their offspring onland for almost twice as long as razorbills.

Acknowledgements. We thank the staff and volunteers ofSkomer, particularly Jennifer Roberts, and Birgitta Bcheand Ed Stubbings (Skomer wardens). We also thank theWildlife Trust for South and West Wales for permission andgenerous in-kind support. A.S. received financial supportthrough Japan Students Services Organization, Merton Col-lege, Department of Zoology at the University of Oxford andthe American Animal Behavior Society, and K.E. receivedan NSERC Postdoctoral Fellowship. All work was conductedafter approval by Natural Resources Wales, the Skomer andStockholm Islands Advisory Committee and the British Trustfor Ornithology (BTO permits: Guilford, 5311; Perrins, 660;Shoji, 5939).

LITERATURE CITED

Afan I, Navarro J, Cardador L, Ramirez F and others (2014)Foraging movements and habitat niche of two closelyrelated seabirds breeding in sympatry. Mar Biol 161: 657668

Ashmole NP (1963) The regulation of numbers of tropicaloceanic birds. Ibis 103b: 458473

Baillie SM (2001) Atlantic puffin response to changes incapelin abundance in Newfoundland and Labrador: aninter-colony and inter-decade comparison. MS thesis,Memorial University of Newfoundland, St. Johns

Barger CP, Kitaysky AS (2012) Isotopic segregation betweensympatric seabird species increases with nutritionalstress. Biol Lett 8: 442445

Barrett RT, Furness RW (1990) The prey and diving depths

of seabirds on Hornoy, north Norway after a decrease inthe Barents Sea capelin stocks. Ornis Scand 21: 179186

Benvenuti S, DallAntonia L, Lyngs P (2001) Foragingbehaviour and time allocation of chick-rearing razorbillsAlca torda at Graesholmen, central Baltic Sea. Ibis 143: 402412

Brown ZW, Welcker J, Harding AMA, Walkusz W, Kar -novsky NJ (2012) Divergent diving behavior during shortand long trips of a bimodal forager, the little auk Allealle. J Avian Biol 43: 215226

Bche B, Stubbings E, Boyle D, Perrins C, Yates L (2013)Seabird monitoring on Skomer Island in 2013. JNCCContract Report, Joint Nature Conservation Committee,Peterborough

Burger AE, Powell DW (1990) Diving depths and diet ofCassins auklet at Reef Island, British Columbia. Can JZool 68: 15721577

Burger AE, Simpson M (1986) Diving depths of Atlanticpuffins and common murres. Auk 103: 828830

Burger AE, Wilson RP, Garnier D, Wilson MPT (1993) Divingdepths, diet, and underwater foraging of rhinoceros auk-lets in British Columbia. Can J Zool 71: 25282540

Burnham KP, Anderson DR (2002) Model selection andmulti model inference: a practical information-theoreticapproach. Springer, New York, NY

Butler PJ (2006) Aerobic dive limit. What is it and is it alwaysused appropriately? Comp Biochem Physiol A 145: 16

Croll DA, Gaston AJ, Burger AE, Konnoff D (1992) Foragingbehavior and physiological adaptation for diving inthick-billed murre. Ecology 73: 344356

Croxall JP, Prince PA (1980) Food, feeding ecology and eco-logical segregation of seabirds at South Georgia. Biol JLinn Soc 14: 103131

DallAntonia L, Gudmundsson GA, Benvenuti S (2001) Timeallocation and foraging pattern of chick-rearing razor-bills in northwest Iceland. Condor 103: 469480

Davidson F (1994) The ecology of the puffin Fratercula arc-tica. DPhil dissertation, University of Oxford, Oxford

Davoren GK, Montevecchi WA, Anderson JT (2003) Searchstrategies of a pursuit-diving marine bird and the persist-ence of prey patches. Ecol Monogr 73: 463481

Diamond AW (1978) Feeding strategies and population sizein tropical seabirds. Am Nat 112: 215223

Elliott KH, Gaston AJ (2009) Accuracy of depth recorders.Waterbirds 32: 183191

Elliott KH, Hewett M, Kaiser GW, Blake RW (2004) Flightenergetics of the marbled murrelet, Brachyramphus mar-moratus. Can J Zool 82: 644652

Elliott KH, Davoren GK, Gaston AJ (2008) Time allocationby a deep-diving bird reflects prey type and energy gain.Anim Behav 75: 13011310

Elliott KH, Bull RD, Gaston AJ, Davoren GK (2009a) Under-water and above-water search patterns of an Arctic sea-bird: reduced searching at small spatiotemporal scales.Behav Ecol Sociobiol 63: 17731785

Elliott KH, Woo KJ, Gaston AJ, Benvenuti S, DallAntonia L,Davoren GK (2009b) Central-place foraging in an Arcticseabird provides evidence for Storer-Ashmoles halo.Auk 126: 613625

Elliott KH, Gaston AJ, Crump D (2010a) Sex-specific behav-ior by a monomorphic seabird represents risk partition-ing. Behav Ecol 21: 10241032

Elliott KH, Shoji A, Campbell KL, Gaston AJ (2010b) Oxy-gen stores and foraging behavior of two sympatric,planktivorous alcids. Aquat Biol 8: 221235

265

http://dx.doi.org/10.3354/ab00236http://dx.doi.org/10.1093/beheco/arq076http://dx.doi.org/10.1525/auk.2009.08245http://dx.doi.org/10.1007/s00265-009-0801-yhttp://dx.doi.org/10.1016/j.anbehav.2007.09.024http://dx.doi.org/10.1675/063.032.0123http://dx.doi.org/10.1086/283261http://dx.doi.org/10.1890/02-0208http://dx.doi.org/10.1650/0010-5422(2001)103[0469%3ATAAFPO]2.0.CO%3B2http://dx.doi.org/10.1111/j.1095-8312.1980.tb00101.xhttp://dx.doi.org/10.2307/1938746http://dx.doi.org/10.1139/z93-346http://dx.doi.org/10.1139/z90-232http://dx.doi.org/10.1111/j.1600-048X.2012.05484.xhttp://dx.doi.org/10.1111/j.1474-919X.2001.tb04941.xhttp://dx.doi.org/10.2307/3676777http://dx.doi.org/10.1098/rsbl.2011.1020http://dx.doi.org/10.1111/j.1474-919X.1963.tb06766.xhttp://dx.doi.org/10.1007/s00227-013-2368-4

Mar Ecol Prog Ser 520: 257267, 2015

Elliott KH, Ricklefs RE, Gaston AJ, Hatch SA, Speakman JR,Davoren GK (2013) High flight costs, but low dive costs,in auks support the biomechanical hypothesis for flight-lessness in penguins. Proc Natl Acad Sci USA 110: 93809384

Elliott KH, Le Vaillant M, Kato A, Gaston AJ and others(2014) Age-related variation in energy expenditure in along-lived bird within the envelope of an energy ceiling.J Anim Ecol 83: 136146

Falk K, Benvenuti S, DallAntonia L, Gilchrist G, Kampp K(2002) Foraging behaviour of thick-billed murres breed-ing in different sectors of the North Water polynya: aninter-colony comparison. Mar Ecol Prog Ser 231: 293302

Frere E, Quintana F, Gandini P, Wilson RP (2008) Foragingbehaviour and habitat partitioning of two sympatric cor-morants in Patagonia, Argentina. Ibis 150: 558564

Gaston AJ (2004) Seabirds: a natural history. Yale UniversityPress, New Haven, CT

Gaston AJ, Smith SA, Saunders R, Storm GI, Whitney JA(2007) Birds and marine mammals in southwestern FoxeBasin, Nunavut, Canada. Polar Rec 43: 3347

Gauze G (1934) The struggle for existence. Williams &Wilkins, Baltimore, MD

Hansen ES (2003) Ecophysiological constraints on energyprovisioning rate by seabird parents. PhD dissertation,University of Missouri, St. Louis, MO

Harris MP, Wanless S (2012) The puffin. Yale UniversityPress, New Haven, CT

Hutchinson GE (1959) Homage to Santa Rosalia, or Why arethere so many kinds of animals? Am Nat 93: 145159

Ishtiaq F, Javed S, Coulter MC, Rahmani AR (2010) Re -source partitioning in three sympatric species of storks inKeoladeo National Park, India. Waterbirds 33: 4149

Kooyman GL, Elsner R, Campbell WB, Drabek CM (1971)Diving behavior of emperor penguin Aptenodytes for -steri. Auk 88: 775795

Kuroki M, Kato A, Watanuki Y, Niizuma Y, Takahashi A,Naito Y (2003) Diving behavior of an epipelagically feed-ing alcid, the rhinoceros auklet (Cerorhinca monocerata).Can J Zool 81: 12491256

Linnebjerg JF, Fort J, Guilford T, Reuleaux A, Mosbech A,Frederiksen M (2013) Sympatric breeding auks shiftbetween dietary and spatial resource partitioning acrossthe annual cycle. PLoS ONE 8: e72987

Linnebjerg JF, Huffeldt NP, Falk K, Merkel FR, Mosbech A,Frederiksen M (2014) Inferring seabird activity budgetsfrom leg-mounted time-depth recorders. J Ornithol 155: 301306

Lovvorn JR, Watanuki Y, Kato A, Naito Y, Liggins GA (2004)Stroke patterns and regulation of swim speed andenergy cost in free-ranging Brunnichs guillemots. J ExpBiol 207: 46794695

Macarthur RH (1958) Population ecology of some warblersof Northeastern coniferous forests. Ecology 39: 599619

Masello JF, Mundry R, Poisbleau M, Demongin L, Voigt CC,Wikelski M, Quillfeldt P (2010) Diving seabirds share for-aging space and time within and among species. Eco-sphere 1: art19

McMahon TE, Holanov SH (1995) Foraging success of large-mouth bass at different light intensities: implications fortime and depth of feeding. J Fish Biol 46: 759767

Mehlum F, Watanuki Y, Takahashi A (2001) Diving behav-iour and foraging habitats of Brunnichs guillemots (Urialomvia) breeding in the High-Arctic. J Zool 255: 413423

Mori Y, Boyd IL (2004) Segregation of foraging between two

sympatric penguin species: Does rate maximisationmake the difference? Mar Ecol Prog Ser 275: 241249

Mori Y, Yoda K, Sato K (2001) Defining dive bouts usinga sequential differences analysis. Behaviour 138: 14511466

Navarro J, Votier SC, Aguzzi J, Chiesa JJ, Forero MG,Phillips RA (2013) Ecological segregation in space, timeand trophic niche of sympatric planktivorous petrels.PLoS ONE 8: e62897

Paredes R, Jones IL, Boness DJ (2005) Reduced parentalcare, compensatory behaviour and reproductive costs ofthick-billed murres equipped with data loggers. AnimBehav 69: 197208

Paredes R, Jones IL, Boness DJ, Tremblay Y, Renner M(2008) Sex-specific differences in diving behaviour oftwo sympatric Alcini species: thick-billed murres andrazorbills. Can J Zool 86: 610622

Phillips RA, Xavier JC, Croxall JP (2003) Effects of satellitetransmitters on albatrosses and petrels. Auk 120: 10821090

Pianka ER (1969) Sympatry of desert lizards (Ctenotus) inWestern Australia. Ecology 50: 10121030

Piatt JF (1990) The aggregative response of common murresand Atlantic puffins to schools of capelin. Stud Avian Biol14: 3651

Piatt JF, Nettleship DN (1985) Diving depths of four alcids.Auk 102: 293297

Porter JM, Sealy SG (1982) Dynamics of seabird multi-species feeding flocks: age-related feeding behaviour.Behaviour 81: 91109

R Development Core Team (2011) R: a language and envi-ronment for statistical computing. R Foundation for Sta-tistical Computing, Vienna

Raya Rey A, Puetz K, Simeone A, Hiriart-Bertrand L, Reyes-Arriagada R, Riquelme V, Luethi B (2013) Comparativeforaging behaviour of sympatric Humboldt and Magel-lanic penguins reveals species-specific and sex-specificstrategies. Emu 113: 145153

Regular PM, Hedd A, Montevecchi WA (2011) Fishing in thedark: a pursuit-diving seabird modifies foraging behav-iour in response to nocturnal light levels. PLoS ONE 6: e26763

Robertson GJ, Fifield DA, Montevecchi WA, Gaston AJ andothers (2012) Miniaturized data loggers and computerprogramming improve seabird risk and damage assess-ments for marine oil spills in Atlantic Canada. J OceanTechnol 7: 4158

Schoener TW (1974) Resource partitioning in ecologicalcommunities. Science 185: 2739

Shoji A, Owen E, Bolton M, Dean B and others (2014) Flexi-ble foraging strategies in a diving seabird with highflight cost. Mar Biol 161: 21212129

Soanes LM, Arnould JPY, Dodd SG, Milligan G, Green JA(2014) Factors affecting the foraging behaviour of theEuropean shag: implications for seabird tracking studies.Mar Biol 161: 13351348

Spencer SM (2012) Diving behavior and identification of sexof breeding Atlantic Puffins (Fratercula arctica), andnest-site characteristics of alcids on Petit Manan Island,Maine. MS thesis, University of Massachusetts Amherst,Amherst, MA

Stauss C, Bearhop S, Bodey TW, Garthe S and others (2012)Sex-specific foraging behaviour in northern gannetsMorus bassanus: incidence and implications. Mar EcolProg Ser 457: 151162

266

http://dx.doi.org/10.3354/meps09734http://dx.doi.org/10.1007/s00227-014-2422-xhttp://dx.doi.org/10.1007/s00227-014-2492-9http://dx.doi.org/10.1126/science.185.4145.27http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&list_uids=22046348&dopt=Abstracthttp://dx.doi.org/10.1071/MU12040http://dx.doi.org/10.1163/156853982X00094http://dx.doi.org/10.2307/4086771http://dx.doi.org/10.2307/1936893http://dx.doi.org/10.1642/0004-8038(2003)120[1082%3AEOSTOA]2.0.CO%3B2http://dx.doi.org/10.1139/Z08-036http://dx.doi.org/10.1016/j.anbehav.2003.12.029http://dx.doi.org/10.1371/journal.pone.0062897http://dx.doi.org/10.1163/156853901317367690http://dx.doi.org/10.3354/meps275241http://dx.doi.org/10.1017/S0952836901001509http://dx.doi.org/10.1111/j.1095-8649.1995.tb01599.xhttp://dx.doi.org/10.2307/1931600http://dx.doi.org/10.1242/jeb.01331http://dx.doi.org/10.1007/s10336-013-1015-7http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&list_uids=24023663&dopt=Abstracthttp://dx.doi.org/10.1139/z03-112http://dx.doi.org/10.1675/063.033.0105http://dx.doi.org/10.1086/282070http://dx.doi.org/10.1017/S0032247406005651http://dx.doi.org/10.1111/j.1474-919X.2008.00824.xhttp://dx.doi.org/10.3354/meps231293http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&list_uids=23991724&dopt=Abstracthttp://dx.doi.org/10.1073/pnas.1304838110

Shoji et al.: Diving in UK alcids

Stone CJ, Webb A, Barton TR, Gordon JRW (1992) Seabirddistribution around Skomer and Skokholm Islands, June1992. JNCC Report 152, Joint Nature ConservationCommittee, Peterborough

Thaxter CB, Daunt F, Hamer KC, Watanuki Y and others(2009) Sex-specific food provisioning in a monomorphicseabird, the common guillemot Uria aalge: nest defence,foraging efficiency or parental effort? J Avian Biol 40: 7584

Thaxter CB, Wanless S, Daunt F, Harris MP and others(2010) Influence of wing loading on the trade-off be -tween pursuit-diving and flight in common guillemotsand razorbills. J Exp Biol 213: 10181025

Trivelpiece WZ, Trivelpiece SG, Volkman NJ (1987) Ecolog-ical segregation of Adlie, gentoo and chinstrap pen-guins at King George Island, Antarctica. Ecology 68: 351361

Vandenabeele SP, Shepard EL, Grogan A, Wilson RP (2012)When three per cent may not be three per cent; device-equipped seabirds experience variable flight constraints.Mar Biol 159: 114

Wakefield ED, Bodey TW, Bearhop S, Blackburn J and oth-ers (2013) Space partitioning without territoriality in gan-nets. Science 341: 6870

Wanless S, Morris JA, Harris MP (1988) Diving behavior ofguillemot Uria aalge, puffin Fratercula arctica and razor-bill Alca torda as shown by radio-telemetry. J Zool 216: 7381

Wanless S, Harris MP, Morris JA (1990) A comparison offeeding areas used by individual common murres (Uria

aalge), razorbills (Alca torda) and an Atlantic puffin(Fratercula arctica) during the breeding season. ColonWaterbirds 13: 1624

Watanuki Y, Burger AE (1999) Body mass and dive durationin alcids and penguins. Can J Zool 77: 18381842

Watanuki Y, Niizuma Y, Gabrielsen GW, Sato K, Naito Y(2003) Stroke and glide of wing-propelled divers: deepdiving seabirds adjust surge frequency to buoyancychange with depth. Proc R Soc B 270: 483488

Watanuki Y, Daunt F, Takahashi A, Newell M, Wanless S,Sato K, Miyazaki N (2008) Microhabitat use and preycapture of a bottom-feeding top predator, the Europeanshag, shown by camera loggers. Mar Ecol Prog Ser 356:283293

Weimerskirch H, Bartle JA, Jouventin P, Stahl JC (1988) Foraging ranges and partitioning of feeding zones in 3species of southern albatrosses. Condor 90: 214219

Whidden SE, Williams CT, Breton AR, Buck CL (2007)Effects of transmitters on the reproductive success oftufted puffins. J Field Ornithol 78: 206212

White CR, Day N, Butler PJ, Martin GR (2007) Vision andforaging in cormorants: more like herons than hawks?PLoS ONE 2: e639

Wilson RP (2010) Resource partitioning and niche hyper- volume overlap in free-living pygoscelid penguins. FunctEcol 24: 646657

Zimmer I, Wilson RP, Beaulieu M, Ancel A, Ploetz J (2008)Seeing the light: depth and time restrictions in the for -aging capacity of emperor penguins at Pointe Gologie,Antarctica. Aquat Biol 3: 217226

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Fig. A1. Bathymetry maps of puffin colony locations at (A) Isle of May and (B) Skomer Island. Red circle indicates the colonyat Isle of May, and red triangle indicates the colony at Skomer Island. Scale shown is in meters. Average foraging radius is

ca. 8 km and maximum foraging typically 25 km for puffins

Editorial responsibility: Rory Wilson, Swansea, UK

Submitted: July 18, 2014; Accepted: October 15, 2014Proofs received from author(s): January 8, 2015

Appendix.

http://dx.doi.org/10.3354/ab00082http://dx.doi.org/10.1111/j.1365-2435.2009.01654.xhttp://dx.doi.org/10.1371/journal.pone.0000639http://dx.doi.org/10.1111/j.1557-9263.2007.00103.xhttp://dx.doi.org/10.2307/1368450http://dx.doi.org/10.1098/rspb.2002.2252http://dx.doi.org/10.1139/z99-157http://dx.doi.org/10.2307/1521416http://dx.doi.org/10.1111/j.1469-7998.1988.tb02416.xhttp://dx.doi.org/10.1126/science.1236077http://dx.doi.org/10.1007/s00227-011-1784-6http://dx.doi.org/10.2307/1939266http://dx.doi.org/10.1242/jeb.037390http://dx.doi.org/10.1111/j.1600-048X.2008.04507.x

cite10: cite12: cite14: cite23: cite16: cite30: cite25: cite18: cite27: cite41: cite4: cite43: cite36: cite8: cite38: cite50: cite34: cite54: cite47: cite61: cite45: cite29: cite63: cite58: cite70: cite72: cite67: cite1: cite5: cite9: cite11: cite13: cite20: cite22: cite15: cite24: cite17: cite2: cite26: cite40: cite19: cite28: cite42: cite6: cite37: cite51: cite35: cite53: cite33: cite46: cite55: cite48: cite31: cite44: cite57: cite62: cite59: cite64: cite66: cite68: cite71: