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Estuarine, Coastal and Shelf Science 89 (2010) 97e106

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Estuarine, Coastal and Shelf Science

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High Arctic sea ice conditions influence marine birds wintering in LowArctic regions

Laura McFarlane Tranquilla a,*, April Hedd a, Chantelle Burke a, William A. Montevecchi a,Paul M. Regular a, Gregory J. Robertson b, Leslie Ann Stapleton a, Sabina I. Wilhelm b, David A. Fifield a,b,Alejandro D. Buren a

aCognitive and Behavioural Ecology, Memorial University of Newfoundland, St. John’s, Newfoundland, Labrador, AIB 3X9, CanadabCanadian Wildlife Service, Environment Canada, 6 Bruce Street, Mount Pearl, Newfoundland and Labrador, A1N 4T3, Canada

a r t i c l e i n f o

Article history:Received 23 September 2009Accepted 1 June 2010Available online 10 June 2010

Keywords:Arctic sea iceocean climate changeweathermortalitystarvationThick-billed MurreUria lomviaCanada

* Corresponding author.E-mail address: lat@alumni.sfu.ca (L. McFarlane Tr

0272-7714/$ e see front matter � 2010 Elsevier Ltd.doi:10.1016/j.ecss.2010.06.003

a b s t r a c t

Ocean climate change is having profound biological effects in polar regions. Such change can also havefar-reaching downstream effects in sub-polar regions. This study documents an environmental rela-tionship between High Arctic sea ice changes and mortality events of marine birds in Low Arctic coastalregions. During April 2007 and March 2009, hundreds of beached seabird carcasses and moribundseabirds were found along the east and northeast coasts of Newfoundland, Canada. These seabird“wrecks” (i.e. dead birds on beaches) coincided with a period of strong, persistent onshore winds andheavily-accumulated sea ice that blocked bays and trapped seabirds near beaches. Ninety-two percent ofwreck seabirds were Thick-billed Murres (Uria lomvia). Body condition and demographic patterns ofwreck murres were compared to Thick-billed Murres shot in the Newfoundland murre hunt. Averagebody and pectoral masses of wreck carcasses were 34% and 40% lighter (respectively) than shot murres,indicating that wreck birds had starved. The acute nature of each wreck suggested that starvation andassociated hypothermia occurred within 2e3 days. In 2007, first-winter murres (77%) dominated thewreck. In 2009, there were more adults (78%), mostly females (66%). These results suggest that spatialand temporal segregation in ages and sexes can play a role in differential survival when stochasticweather conditions affect discrete areas where these groups aggregate. In wreck years, southwardmovement of Arctic sea ice to Low Arctic latitudes was later and blocked bays longer than in most otheryears. These inshore conditions corresponded with recent climate-driven changes in High Arctic icebreak-up and ice extent; coupled with local weather conditions, these ice conditions appeared to be thekey environmental features that precipitated the ice-associated seabird wrecks in the Low Arctic region.

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1. Introduction

Many studies of biological responses to climate change havebeen concentrated in high-latitude polar areas where effects havebeen dramatic (Wilson et al., 2001; Croxall et al., 2002; Mallory andForbes, 2007; Regehr et al., 2007; Laidre et al., 2008). Yet theimplications of polar climate change for ocean ecosystems andmarine animals at lower latitudes are less certain. Current climatechange models predict an increase in environmental variability andextreme weather events (Bates et al., 2008). Extreme weatherevents can impose significant ecological and demographic conse-quences on marine birds (Irons et al., 2008; Jenouvrier et al., 2009),

anquilla).

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which in turn provide robust signals of the biological effects ofclimate change (Ainley et al., 2005; Boyd et al., 2006). In this study,we document relationships among extreme weather, localized iceconditions linked to High Arctic sea ice changes, and marine birdmortality events in the Low Arctic.

Anomalous oceanographic conditions and stormy weather canhave negative impacts on seabird populations (Harris and Wanless,1996; Piatt and van Pelt, 1998; Baduini et al., 2001a; Davoren andMontevecchi, 2003; Parrish et al., 2007; Lavers et al., 2008).Severe weather events can lead to mass mortalities, or “wrecks” ofseabirds, particularly in winter (Harris and Wanless, 1996;Stenhouse and Montevecchi, 1996; Baduini et al., 2001a;Schreiber, 2002). Such winter mortality at sea can occur due toexposure to inclement conditions (Harris et al., 2007) but is moregenerally attributed to starvation after prey becomes unavailable orinaccessible (Stenhouse and Montevecchi, 1996; Finney et al., 1999;

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Baduini et al., 2001a; Schreiber, 2002; Barrett et al., 2004; Sandviket al., 2005). Weather anomalies can cause changes in abundanceand distribution of key prey, forcing diet shifts and foraging atlower trophic levels (Schreiber, 2002). Anomalous ice cover is alsoknown to alter access to prey, exacerbating the energetic strain ofinclement conditions (Wilson et al., 2001; Vincent and Marsden,2001; Ballerini et al., 2009). Encountering extreme weatherduring non-breeding periods, when adults need to build andmaintain body reserves for reproduction, can also influencebreeding success. Birds arriving at colonies with low body reservesmay have difficulty attaining breeding condition even after theweather perturbation subsides (Harris and Wanless, 1996;Sorensen et al., 2009). Other effects of poor weather, consistentwith food shortage, include later returns to colonies, less stagingand reduced nesting activity during pre-breeding, delayedbreeding, and changes in availability or type of prey delivered tonestlings (Harris and Wanless, 1996; Barrett et al., 2004).

Given that extreme weather events are predicted to increase infrequency with climate change (Bates et al., 2008), it is important tounderstand the effects of environmentally-driven mortality onmarine animal populations (Frederiksen et al., 2007; Sandvik et al.,2008). For example, an understanding of environmental influenceson immature seabirds is critical because their recruitment canbuffer declines in breeding populations following stochasticecosystem events, causing demographic shifts (Votier et al., 2008).Through combined effects on adult and juvenile survival, andreduced breeding activity or success at colonies (Sandvik et al.,2005; Votier et al., 2008), anomalous weather events can influ-ence population dynamics at scales ranging from a local colony toglobal populations (Harris andWanless, 1996; Baduini et al., 2001b;Irons et al., 2008).

During early April 2007 and late March 2009, sustained north-easterly winds pushed the seasonal Arctic ice pack against thenortheast Newfoundland coast, resulting in a heavy build-up of icevery close to shore (Environment Canada, 2007a,b, 2009b). Duringthese environmental conditions, 209 (2007) and 215 (2009) seabirdcarcasses were collected on beaches (hereafter referred to as theseabird “wreck”) along the east and northeast Newfoundland coast,andmanymore seabirds appearing weak and listless were reportedin bays near shore in both years. Beached seabird carcasses duringthese two events occurred at a much higher density (ca. 10e100birds/km; Canadian Wildlife Service unpubl. data) compared toregional winter beached bird surveys (0.1 bird/km; Wilhelm et al.,2009). Almost all of the birds were identified as Thick-billedMurres, Uria lomvia, though three Common Murres, Uria aalge, twoBlack Guillemots, Cepphus grylle, and a Long-tailed Duck, Clangulaharenguswere also found in 2007 and 26 Common Murres and oneBlack Guillemot were collected in 2009. Upon examination, wreckcarcasses were emaciated, suggesting starvation as the cause ofdeath.

Thick-billed Murres are pursuit-diving, Arctic-breedingseabirds that associate with sea ice and generally overwinter inwaters close to ice edges (Gaston and Jones, 1998). Such ice-associated birds forage on a diversity of fish and zooplankton,taking advantage of physical processes that concentrate cold,slow-moving prey at the ice margins (Gaston and Jones, 1998;Mehlum, 2001). Their high-latitude overwintering areas arecold, harsh environments, where air temperature and windsstrongly influence sea ice cover (Prinsenberg et al., 1997) and itstransport from high to low latitude regions (Vincent andMarsden, 2001). In turn, ice cover and resulting surface watertemperature influence the type, composition, and availability ofprey in winter diets of murres and their southern ocean coun-terparts, the penguins (Elliot et al., 1990; Ainley et al., 1998).Variation in distribution, thickness, and extent of ice cover

strongly affects seabird winter distribution, diet, survival andsubsequent breeding (Wilson et al., 2001; Ainley et al., 2005;Ballerini et al., 2009; Gaston, 2003, Gaston et al., 2009). Thick-billed Murres respond to dynamic ice cover by shifting theirdistribution throughout the year, usually southward as the winterprogresses (Gaston, 1980). Similar to penguins, murres possessthe behaviour and morphology to exploit ice-associated foragingopportunities (Ainley et al., 1994), despite the potentially harshconditions associated with high latitude areas in winter.

Due to tissue-specific metabolic processes, comparing theisotopic signatures of various body tissues can provide insight intorecent dietary shifts (Hobson and Clark,1992b). For example, recentdietary changes will be first detected in tissues such as blood andliver, which have rapid turnover (Evans-Ogden et al., 2004; Phillipsand Eldridge, 2006). To interrogate the extent of dietary restrictionpreceding the wreck event (i.e., if birds were having trouble findingfood), we used stable isotope analyses (SIA) to investigate differ-ences in trophic associations according to three (competing) ideas:wreck birds would exhibit (1) relative nitrogen enrichment in bodytissues, as starving birds catabolize protein from their muscle tissue(Hobson et al., 1993; Cherel et al., 2005; but see Kempster et al.,2007; Williams et al., 2007), or (2) a shift toward lower trophiclevels (and subsequent decline in 15N enrichment) to be detectablein body tissues, particularly liver, as birds begin to feed on any preyitem encountered, presumably including a wider range of lowertrophic levels, in order tomeet life-saving energy requirements (c.f.Baduini et al., 2001b). We also investigated whether spatialmovements and spatial segregation of birds from offshore toinshore marine areas could be detectable via relative enrichment of13C (c.f. Hobson et al., 1994; Forero et al., 2005; Phillips andEldridge, 2006).

When seabird wrecks occur, it is difficult to pinpoint a singleunderlying cause (Harris and Wanless, 1996). We investigated theseabird wreck using multiple approaches, including carcass andSIA analyses, and assessment of environmental conditions thatmay have led to thewreck. In this paper, we (1) describe the extentof the ice-induced mortality events, (2) compare the age class andsex composition of the wreck birds with those expected in thepopulation at large, (3) contrast the body mass and stable isotopesignatures of wreck birds with apparently healthy hunter-killedmurres, (4) examine the environmental conditions that createdthe coastal ice accumulations and resulted in the seabird mortalityevents, (5) assess past patterns of inshore sea ice and occurrencesof wreck events, and (6) consider the implications of ongoingocean climate change on seabird mortality events. We integratethese results to infer the causes and implications of the mortalityevents, and appraise the implications of Arctic Ocean climatechange on marine birds wintering in mid-latitude Low Arcticregions.

2. Methods

2.1. Murre carcass analyses

Seabird carcasses were collected from coastal sites in easternNewfoundland on 5e6 April 2007 and 26e31 March 2009 (Fig. 1).Due to a rapid response to numerous public reports of dead birdsonshore (by Environment Canada Canadian Wildlife Service, EC-CWS), birds were likely beach-cast for only a day or two beforeretrieval. Carcasses were weighed and examined for speciesidentification, age, sex, and sampled for avian influenza. A sub-sample of birds (N ¼ 11) had detailed post-mortem and histopa-thology examinations to determine cause of death by VeterinaryPathologists at the Atlantic Veterinary College, Canadian Cooper-ative Wildlife Heath Centre (2007) and the Newfoundland and

Fig. 1. Map of distribution and numbers of wreck Thick-billed Murres (Uria lomvia) along the eastern Newfoundland coast in 2007 (top) and 2009 (bottom).

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Labrador Department of Natural Resources’ Animal Health Divi-sion (2009).

For comparison with wreck Thick-billed Murres, we determinedmass, age and sexofpresumablyhealthy Thick-billedMurres killedbyhunters from January through March 2004e05 (N ¼ 55), 2005e06(N ¼ 13) and 2007e08 (N ¼ 56). A sub-sample of hunted birds(N¼39), taken in late February 2008 inSt.Mary’s Bay (see Fig.1)were

available for detailed carcass analyses. These birds were sexed andassigned to one of two age classes, first winter or older, based onfeatures including size of bursae and gonads, color of greatersecondarycoverts (Camphuysen,1995;Wilhelmet al., 2008), and sizeand ossification of supra-orbital ridges (Gaston, 1984). For conve-nience, the term “adult” is used to describe birds older than firstwinter, including younger birds in their second winter.

Table 1Comparisons of body mass (overall, adult, and juvenile; g � SD) and pectoral musclemass (g � SD) of shot and wreck Thick-billed Murres (Uria lomvia).

Mass Shot (N) Wreck 2007 (N) Wreck 2009 (N) OverallLoss

Pooled Body 958 � 87 (113) 622 � 72 (74) 639 � 56 (108) 34%Adult 997 � 85 (59) 641 � 76 (15) 645 � 51 (84) 35%Juvenile 915 � 66 (54) 617 � 70 (59) 618 � 67 (24) 33%Pectoral Muscle 71 � 3.02 (12) 43 � 6.05 (53) n/a 40%

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Age and sex ratios of wreck Thick-billed Murres were alsocompared to those expected in the population at-large. Weassumed juveniles represented 15% of the population offNewfoundland in spring (Gaston, 1980; Elliot, 1991; Wiese et al.,2004). Females and males were expected to be in equal numbers,as there is no obvious sex bias in the population (Tuck, 1961; Wieseet al., 2004).

Muscle mass and SIA were collected for the 2007 wreck groupand the 2008 shot group only. Pectoralis and supracoracoideusmuscles from both sides of the carcass of each bird were excisedand weighed. Mass of both pectoral muscles was averaged perindividual to produce a single measure of pectoral muscle for bothwreck and shot birds. Pectoral muscle (N ¼ 13 shot; N ¼ 29 wreck)and liver (N ¼ 33 shot; N ¼ 29 wreck) were sub-sampled for SIA.Scavenged wreck birds (i.e. pectoral muscle damaged) wereexcluded from mass analyses.

2.2. Tissue preparation and stable isotope (SI) analyses

Liver and muscle tissue samples were prepared according tostandard SIA sample preparation methods described in Hobsonet al. (2002). Samples were analyzed at the Stable Isotope Facility,University of California Davis, USA. Replicate measurement oflaboratory standards (2 standards for every 12 unknowns) indi-cated measurement errors of approximately 0.16 and 0.06& fornitrogen and carbon, respectively. Specific metabolic processeswithin different body tissues result in slightly different isotopicvalues in those tissues as animals change diets or foraging locations(Phillips and Eldridge, 2006). These tissue differences are generallyaccounted for using “fractionation” equations (Hobson and Clark,1992). Standard equations were used to present delta (d) notationfor the SI values, to incorporate diet-tissue fractionation factors(Hobson and Clark, 1992; but see Bond and Jones, 2009), and toconvert SI values for pectoral tissue to their liver equivalent fordirect comparison of the isotopic values from these two differenttissues (Moody and Hobson, 2007).

2.3. Sea ice conditions and climate

Sea ice conditions in the Arctic, Northwest Atlantic andNewfoundland and Labrador coasts were evaluated using CanadianIce Service (CIS) online Ice Graph Tool and online data requestservices (http://ice-glaces.ec.gc.ca/IceGraph/IceGraph-GraphdesGlacesjsf?id¼11874&lang¼eng). Sea ice conditions were compiledacross seasons and years by CIS using all available ice data fromsatellite data, ship, and shore reports, and most recently, fromRADARSAT-1/2 and NOAA-x satellites (Bernard Duguay,Environment Canada, pers. comm).

2.4. Statistical analyses

Standard general linear models (GLM) were used to test rela-tionships between mean body mass and group (wreck or shot), ageand sex, and their interactions. GLMs were also used to examineeffects of age, group (shot or wreck), tissue (pectoral or liver, cor-rected for discrimination factors) and their interactions on SIsignatures. When results from GLM were significant, we usedANOVA with Tukey post-hoc tests to discriminate differencesbetween groups. Pectoral masses were assessed in a separate GLM,indicating that group (2007 wreck or shot) was the only signifi-cantly influence (F1,59 ¼ 100.47, P � 0.001), so we pooled ages andsexes to compare pectoral masses of wreck and shot birds. Averagemass of wreck birds did not differ between 2007 and 2009(F1,180 ¼ 3.08, P ¼ 0.081), so years were pooled for analyses. Like-wise, average mass of shot birds from the murre hunt (2005e2008)

did not vary annually (F2,110 ¼ 0.95, P ¼ 0.39), so years were pooledin subsequent analyses. Age ratios between wreck and shot groupswere compared using chi-square tests; sex ratios were assessedusing CI for one proportion (within group) and chi-square tests(between groups). Specific model results described in the resultssection are presented in Table 2. Means are reported �1 SE, exceptfor body and tissue masses which are reported with SD. Minitab(version 13.32) statistical software was used for data analysis.

3. Results

3.1. Extent of wreck

Ninety-two percent of wreck carcasses collected were Thick-billed Murres (years pooled). 168 wreck Thick-billed Murres werecollected on 5e7 April 2007, and 187 were collected on 26e31March 2009, mainly along the eastern Newfoundland coast, withhighest numbers occurring in 2007 at English/Trinity Harbours,Holyrood, and Portugal Cove South; and in 2009 at Holyrood,Conception Bay (Fig.1). Other beached bird surveys on the southernAvalon Peninsula through the 2000s report a background mortalityrate of about 0.1 bird/km of beach surveyed, with relatively littlevariation among years (Wilhelm et al., 2009).

3.2. Laboratory results and body condition

All examined wreck murres were extremely emaciated, with nodiscernable subcutaneous or visceral fat. The stomachs of all birdswere empty and carcasses were otherwise unremarkable. Inabsence of infectious agents or other causes, starvation was themost probable cause of death (S. McBurney, L. Rogers, AtlanticVeterinary College, pers. comm.). Intact wreck birds were muchlighter than shot birds (F1,293 ¼ 1383.5, p � 0.001; Table 1), andaverage pectoral muscle mass in wreck birds (2007) was lighterthan that of shot birds (F1,63 ¼ 213.0, p � 0.001; Table 1).

Both group and age explained significant variation in body mass(F1,197¼ 530.97, p� 0.001; F1,197¼ 9.94, p¼ 0.002, respectively), butnot sex (F1,197 ¼ 0.08, p ¼ 0.781) nor any interactions (p > 0.2 in allcases). Wreck adults were significantly heavier than wreck juve-niles (years pooled; F1,180 ¼ 8.30, p ¼ 0.004) and shot adults weresignificantly heavier than shot juveniles (F1,111 ¼ 32.86, p � 0.001;Table 1).

3.3. Age and sex composition

First-year murres comprised the bulk of the wreck sample in2007 (Table 2). This is significantly different from the proportion ofjuveniles expected in the population at-large (c2 ¼ 97.5, DF ¼ 1,P � 0.001), and also significantly different from the proportion inthe sample of shot birds (c12 ¼ 27.4, P � 0.001). An opposite patternoccurred in 2009 with most of the wreck birds being adults, closerto the age ratio expected in the population at-large (c12 ¼ 1.56,P ¼ 0.211; Table 2).

Table 2Number and sex ratios of adult and juvenile Thick-billed Murres (Uria lomvia) in theshot and wreck groups, compared to that estimated in the population at-large.“Juvenile” indicates birds in their first winter; “adult” includes all birds over one yearold, including immatures and non-breeders. A hypothetical population (n ¼ 100) isused to indicate relative age and sex ratios.

Group N Adult Male: Female Juvenile Male: Female

Shot 124 65 1.1:1.0 59 1.8:1.0Wreck 2007 167 38 1.0:1.3 129 1.0:1.4Wreck 2009 185 146 1.0:2.4 39 1:1Population 100 85 1:1 15 1:1

Fig. 2. Adjusted carbon (d13C � SE) isotopes in liver and pectoral tissues of shot (darksymbols) and wreck (light symbols) Thick-billed Murres (Uria lomvia), separated by agegroups (adults denoted by squares, juveniles denoted by circles). Increasing carbonenrichment indicates feeding closer to inshore areas or on more benthic prey; differentenrichment in tissues indicates recent dietary change.

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In 2007, our sample of wreck Thick-billed Murres was slightly,but not significantly, female-biased (c12 ¼ 1.54, P ¼ 0.214) and notdifferent to the sex ratio in the shot sample (c12 ¼ 2.69, P¼ 0.101). In2009, wreck birds were mostly females (Table 2), significantlybiased from the 1:1 ratio anticipated in the population at-large(c12 ¼ 5.95, P¼ 0.015) and significantly different than the proportionof females in our shot sample (c12 ¼ 6.12, P ¼ 0.013).

3.4. Trophic association

We found no variation in d15N between shot or wreck individuals(F1,88 ¼ 0.39, P ¼ 0.532), between tissues (F1,88 ¼ 1.28, P ¼ 0.261),between age classes (F 1,88 ¼ 2.42, P ¼ 0.095), between sexes(F 1,88 ¼ 0.50, P ¼ 0.481) or in any interactions. However, d13C valuesvaried significantly (Fig. 2), with pooled d13C being more enriched inwreck versus shot birds (F 1,88 ¼ 194.46, P � 0.001), in liver versuspectoral tissues (corrected for discrimination factors; F 1,96 ¼ 140.69,P � 0.001), and in juveniles versus adults (F2,88 ¼ 7.28, P ¼ 0.008;Fig. 2) but not according to sex (F 1,88 ¼ 0.66, P ¼ 0.418) and with nosignificant interactions (all p > 0.3). In analyses separating wreckfrom shot groups, these patterns remained in shot birds, with d13Csignificantly more enriched in liver versus pectoral tissue and injuveniles versus adults; but for wreck birds, only isotopic differencesbetween tissue type (not age) was significant (Fig. 2). Unadjusted SIsignatures of pectoral and liver tissues in shot and wreck birds arepresented in Table 3 for comparison with other studies.

3.5. Sea ice conditions

Investigating the environmental conditions around the time ofthe wreck required post-hoc data collection from various sources.During 1e5 April 2007 and 24e31 March 2009, high-density packice and sustained northeasterly winds combined to block coastalleads and create strong ice pressure blocking the northeastNewfoundland coast (Environment Canada, 2007a, 2009b), causingbirds to be restricted to narrow inner reaches of coastal inlets andbays. The ice conditions in 2007 and 2009 stand out as unusual inthree ways. First, there was more sea ice, nearer the shore thanusual during April 2007 and March 2009 (Fig. 3). Second, theappearance of coastal ice blocking the inshore bays for manyconsecutive days (>3) occurred later in thewreck years of 2007 and2009 than in all other years since 1999 (Fig. 4). Ice often blocksinshore bays around Newfoundland waters, but the inshore iceblockage usually occurs earlier in the year (JaneFeb) and has begunto retreat by March/April. Third, in 2007 and 2009, the progression

Table 3Mean raw muscle and liver values (�SE) of d15N and d13C in Thick-billed Murres (Uria lo

Group N Pectoral muscle d15N Pect

Wreck 29 13.93 � 0.07 �18Shot 13 13.74 � 0.16 �20Moody and Hobson 2007 89 14.8 � 0.1 �1

of the leading ice edge along the Newfoundland-Labrador coast wasfarther south than usual, and later in the season, compared to thelong-term average (Fig. 5). Usually, the ice edge has begun to retreatnorthward again by early March (1969e2000 average, Canadian IceService; see Fig. 5).

4. Discussion

4.1. Mortality and body condition

Based on detailed necropsies and very low body and musclemass, Thick-billed Murres found dead along the easternNewfoundland coast in April 2007 and March 2009 undoubtedlystarved. The starvation coincided with a period of sustainednortheasterly winds and coastal sea ice blocking coastal bays laterthan usual. Starvation likely occurred because ice restricted accessto or altered the distribution of coastal food sources, in combinationwith extremely reduced physical ability of starving birds to catchfood or move elsewhere. The wreck event affected mostly inexpe-rienced first-year birds in 2007 and adult females in 2009. Theacute nature of the wreck events suggests that Thick-billed Murresstarved rapidly, within 2e3 days.

Wreck Thick-billed Murres’ body and muscle mass was 34%reduced compared to healthy birds during the same time of year.This percentage is consistent with other seabird starvation reports,with reduced body mass (Piatt and van Pelt, 1998; Baduini et al.,2001a; Barrett et al., 2004), reduced organ mass, lipid depletion,and protein catabolism soon followed by death (Oka and Okuyama,2000; Baduini et al., 2001a). The mass of wreck murres was also36% lighter than that of chick-rearing Thick-billed Murres at CoatsIsland (Gaston and Hipfner, 2006).

Undoubtedly, their extremely poor physical condition wouldhave prevented murres from moving elsewhere. During severe

mvia), this study (wreck, shot), compared with Moody and Hobson (2007).

oral muscle d13C N Liver d15N Liver d13C

.91 � 0.06 29 15.251 � 0.07 �18.77 � 0.07

.00 � 0.08 33 15.257 � 0.06 �19.91 � 0.079.8 � 0.1 n/a n/a

Fig. 3. Ice anomaly around coastal Newfoundland during the wreck events in April 2007 (top) and March 2009 (bottom). Figures courtesy of Canadian Ice Service, EnvironmentCanada.

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weather, seabirds may be incapable of relocating to productiveforaging areas, due to the lack of body reserves to support the highflight costs of travelling elsewhere (Baduini et al., 2001b; Elliottet al., 2008). Increased foraging effort is necessary to supporthigher energy requirements in winter (Fort et al., 2009), but

successful foraging may not be possible in stormy conditions(Daunt et al., 2006) or when food access is restricted by ice cover(Wilson et al., 2001). The energetic strain imposed by harsh envi-ronmental conditions coupled with limited access to food and lackof sufficient body reserves could push seabirds to starvation in

Fig. 4. Wreck events (where wreck ¼ yes or no) according to the earliest date that icefirst blocked for �3 days between 15 Marche15 April in northeast Newfoundland(Bonavista, Trinity and Conception Bays; see Fig. 1), from 1999 to 2009. Wrecksoccurred when bays were first blocked later in the season.

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a few days (Grémillet et al., 2005; Fort et al., 2009). Energeticallycompromised murres will be more susceptible to hypothermia, tobeing driven landward during severe weather (see Stenhouse andMontevecchi, 1996), or to aggregating ashore to reduce thermalconductance at sea (Piatt and van Pelt, 1998).

4.2. Age and sex ratios

A common element in both the 2007 and 2009 wreck eventsseems to have been spatial segregation inwinter distribution by ageand sex. This is not unusual, as band recoveries of overwinteringmurres have shown temporal and spatial segregation by age, colonyof origin, and month (Gaston, 1980; Elliot, 1991; Donaldson et al.,1997; Harris et al., 2005). A juvenile mortality bias in theNewfoundland murre hunt has been attributed to inexperience inrisk avoidance and to age-related differences in temporal and

Fig. 5. Timing of latitudinal progression of the ice edge along the Newfoundland and Labradedge begins to retreat northward again (denoted by red symbols) in early March; in 2007 anencompassing wreck study area (between 47 and 48� N); arrows denote wreck periods in 20courtesy of the Canadian Ice Service, Environment Canada).

spatial distribution (Elliot, 1991; Donaldson et al., 1997), both ofwhich likely contributed to the prevalence of wreck juveniles in2007. Survival of immature auks varies more and/or is reducedcompared to adults (Harris et al., 2007; Sandvik et al., 2008), andimmature birds are commonly over-represented in seabird wrecksfollowing extreme weather (Harris and Wanless, 1996). The agebias in the 2007 wreck suggests that juveniles were more suscep-tible to starvation during anomalous ice conditions, similar to thatseen in the Southern Ocean, where extensivewinter sea ice reducessurvival of subadult Adelie Penguins (Wilson et al., 2001). Weather-induced mortality is likely a significant contributor to age-specificsurvival rates (Wilson et al., 2001), when localized weatherconditions affect areas in which age groups aggregate.

The population sex ratio of Thick-billed Murres is presumedequal (Tuck, 1961; Wiese et al., 2004; Robertson et al., 2006). Theprevalence of females in the 2009 wreck suggests sex-relateddifferences in spatial distribution and/or increased susceptibility toenergetic stress during harsh environmental conditions. Weathermay contribute to sex differences in survival when sex-specificbehaviour determines spatial distribution, such as in the Thick-billed Murre males, which accompany chicks to sea during post-breeding dispersal. Yet we are aware of mortality events only whenthey occur nearshore, where dying seabirds are more likely to befound; what happens offshore during extreme weather events isunknown.

4.3. Trophic associations

We found no variation in d15N stable isotopes, rejecting ourhypotheses that wreck birds had been feeding at a lower trophiclevel to fulfill energetic requirements, and that they had beenstarving over a longer time. The brief duration of strong onshorewinds prior to murres coming ashore in 2007 and 2009 suggeststhat the wreck unfolded rapidly as have other seabird wrecks (Piattand van Pelt, 1998; Barrett et al., 2004). Any event limiting access tofood during harsh conditions would have the potential to causerapid starvation and hypothermia (c.f. Grémillet et al., 2005; Fort

or coast, historically (1969e2000) and for the wreck years (2007 and 2009). Usually, iced 2009, ice retreat was much later than normal. Horizontal shaded bar denotes latitude07 and 2009. Latitude of the nearshore ice edge estimated to the nearest degree (data

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et al., 2009), before a change in diet could be incorporated into theseabird tissues. Therefore SI response and turnover time was likelyinsufficient to register either a trophic-level dietary change or foodabsence before the birds died (Hobson et al., 1993). d13C has beenused to assess the distance of seabird foraging areas from shore(inshore vs. offshore) and their links with benthic food webs(Hobson et al., 1994; Forero et al., 2005). As well, recent changes indiet or foraging areas can be detected because tissues incorporatedietary isotopes at different turnover rates (Evans-Ogden et al.,2004; Phillips and Eldridge, 2006). In contrast to our d15N results,we found consistent patterns in d13C signatures indicative of spatialand temporal segregation among wreck and juvenile groups(Fig. 2). We found greater 13C enrichment in (1) wreck murres thanshot murres overall, and (2) liver than pectoral muscle, across agesand groups. The first finding suggests spatial segregation of wreckand shot groups, where a more inshore distribution of wreck birdscompared to shot birds may have increased the susceptibility of thewreck group to entrapment by inshore ice. This spatial segregationwould have had to occur over a longer time in order for both liverand pectoral tissues of the wreck group to register the changetoward inshore/benthic food sources. These samples were taken indifferent years, so we cannot preclude the possibility that thedifferences may be due to inter-annual variation in d13C signaturesof marine food webs (Moody and Hobson, 2007). Within years,consistent 13C enrichment in juveniles versus adults also suggestsage-specific spatial distribution (however, age-specific metabolicprocesses may fractionate diet differently; c.f. Williams et al., 2007;Bond and Jones, 2009). The second finding indicated a consistentdifference between liver and pectoral muscle among ages andgroups, with liver tissue having the highest enrichment, comparedto pectoral tissue of its age and study group. Isotopic ratios of thetissues would be nearer equilibrium (Phillips and Eldridge, 2006), ifthe animal was not shifting from inshore/benthic to offshore/pelagic sources. The increased enrichment of liver tissue, which hasa faster isotopic turnover (Evans-Ogden et al., 2004), may reflectthe temporal scale of inshore movement, with recent movementtoward inshore occurring in both the shot and the wreck groups;the shot birds moved inshore and were hunted, whereas the wreckbirds moved inshore and became ice-entrapped.

4.4. Local sea ice conditions

During March/April 2007 and late March 2009, sea ice washeavily and densely packed along the Newfoundland coast in thedays preceding the wreck. For 4e5 days, sea ice blocked bays andextended 100 km or more offshore. This ice occurrence wasunusually late and protracted in 2007 and 2009. The Arctic ice mayhave reduced the temperature and salinity in southward-flowingwater, both of which influence the distribution and abundance ofseabird prey. Since Thick-billed Murres forage at sea ice edges(Gaston and Jones,1998), the coastal ice in 2007 and 2009may haveattracted them. It is also possible that strong windsmoved the birdsinshore ahead of sea ice. Either way, the inshore distributionbecame a trap as strong winds rapidly closed coastal leads,precluded access to food and prevented birds from relocating.

Historically, sea ice from the Arctic moves southward down theLabrador Current to the northeast Newfoundland coast in Januar-yeFebruary, reaches its full extent in early March, and then breaksup and moves offshore by late MarcheMay. Coinciding with thissouthward ice movement is the northward migration of over-wintering murres from the marine area around Newfoundland,back to Arctic colony areas (Gaston, 1980). In previous heavy iceyears during 1970se1990s, the ice edge reached the Newfoundlandcoast (48� N latitude) early in the year and remained through April.In those years, Thick-billed Murres migrating through coastal areas

would not become trapped if the bays were already blocked by ice.The main difference in ice conditions during 2007 and 2009 wasthe late southward penetration of Arctic sea ice into bays (Figs. 4and 5), which coincided with northward pre-breeding migrationof Thick-billed Murres (Gaston, 1980). In more than 60 years ofrecorded natural history, there have been no reports of similar ice-related wrecks of Thick-billed Murres (Tuck, 1961; P. Ryan, Cana-dian Wildlife Service, pers. comm.; WAM, unpubl. data); thissuggests that there have been relatively recent changes in theconditions that influence ice and in turn, ice-associated seabirds.

4.5. Regional atmospheric & sea ice conditions

Atmospheric systems (e.g. North Atlantic Oscillation [NAO],Antarctic Oscillation) influence ice cover (Prinsenberg et al., 1997;Strong et al., 2009), and often the relationship is synergistic, thevariability of one affecting the other (Ainley et al., 2005; Vincentand Marsden, 2001). The strength of seasonal winds and theirinfluence on ice break-up and ice conditions influences polar-breeding species such as Thick-billed Murres and Adelie penguinson breeding and wintering grounds (Wilson et al., 2001; Gaston2003, Gaston et al., 2009; Ainley et al., 2005). Positive NAO aretypically characterized by increased winds, more frequent storms,and colder temperatures, causing sea ice concentrations to beanomalously high southwest of Greenland (Strong et al., 2009).Positive NAO indices have been common in the Northwest Atlanticduring FebruaryeApril over the last 30 years (US National Centrefor Atmospheric Data, 1995), and have been associated withwinter survival and breeding parameters in some seabirds (Votieret al., 2005; Gaston et al., 2009; Wanless et al., 2009) but notothers (Harris et al., 2005; Regular et al., 2008; Wanless et al.,2009). With only two datapoints (2007 and 2009), we lackedpower for a robust comparison of NAO indices and the probabilityof seabird wrecks. However, as seen in the Antarctic, variation inatmospheric systems causing unusual sea ice conditions can haveadverse effects on seabirds (Wilson et al., 2001; Ainley et al., 2005).

Coastal ice conditions around Newfoundland in 2007 and 2009coincided with unusual ice conditions in the High Arctic, leading usto hypothesize that the regional seabird wrecks were the result ofchanging High Arctic ice conditions. The Nares Strait, usually frozenthrough the winter, usually restricts the southward flow of Arcticsea ice until summer break-up. Biological effects of changes inwindand ice conditions in Nares Strait include the variation in timingand location of seasonally-occurring polynyas (e.g. the NorthWaterPolynya, Vincent andMarsden, 2001; Hobson et al., 2002). Since the1950s, there have only been three years when ice in Nares Strait hasnot consolidated e 1993, 2007, and 2009 (Environment Canada,2009a). Examination of ice charts through the winter and springof 2007 and 2009 (Canadian Ice Service Online Ice Graph tool,http://ice-glaces.ec.gc.ca/IceGraph/IceGraph-GraphdesGlacesjsf?id¼11874&lang¼eng) depict anomalous bands of ice sweepingsouth through the Labrador Sea as spring progresses. The variabilityin extent and distribution of ice cover is governed by winds andcurrents (Vincent and Marsden, 2001; Ainley et al., 2005), sug-gesting the link between recent changes in High Arctic ice condi-tions and biophysical consequences in Low Arctic regions in theNorthwest Atlantic. In April 2007, the influx of older multi-yearArctic ice into coastal Newfoundland trapped more than 200 seal-ing vessels and launched the most intensive marine rescue opera-tion in Canadian history (Environment Canada, 2007a). In 2009, anunusual tongue of arctic-origin ice extended eastward from theNewfoundland and Labrador coasts to the shelf edge ca. 350 kmeast of Newfoundland. In addition to the physical impact of iceitself, large ice exports during the winters of 2004/05, 2007/08 and2008/09 through Fram Strait and Nares Strait on the east and west

L. McFarlane Tranquilla et al. / Estuarine, Coastal and Shelf Science 89 (2010) 97e106 105

coasts of Greenland have created freshwater anomalies along theLabrador/Newfoundland coast, with a 1e3 year lag (T. Wohlleben,Canadian Ice Service, pers. comm.). The areas “downstream” ofNares Strait, particularly Baffin Bay, the Davis Strait and LabradorSea are important wintering areas for Thick-billed Murres, and thepresence and southward movement of ice and salinity changesthrough these regions likely influence the distribution of birds andtheir prey (Gaston, 1980). Thus, we suggest that the ice-associatedwrecks observed in 2007 and 2009 are not just localizedphenomenon, but are likely to reflect large-scale climate changesaffecting the region.

5. Conclusion

We have suggested that temporal, spatial, and physical sea icechanges can sweep from High to Low Arctic regions, catalyzingecosystem changes and biological responses such as seabird wintermortality. To date, biological responses to climate change in iceecosystems (c.f. Croxall et al., 2002; Gaston et al., 2009; Ainley et al.,2005) have mostly been reported in polar regions where sea icechange has been most notable. The present study describes onepossible consequence of climate-related changes in ice ecosystemson animals living “downstream” from Arctic regions. Thick-billedMurres from colonies throughout the High and Low Arcticconcentrate at important wintering areas in the Northwest Atlantic(Gaston, 1980; Donaldson et al., 1997), where environmentalconditions are likely critical to their survival. Events in winteringareas can carry over to the breeding season, in the form of reducednumbers, differential survival of sexes, or fewer juveniles or pre-breeders that might otherwise buffer population declines (Gaston,2003; Votier et al., 2008; Sorensen et al., 2009). Any increase inenvironmental anomalies during winter as predicted by climatechange models could have widespread demographic and pop-ulation consequences for seabirds and other marine animals inregions far-removed from the poles.

Acknowledgements

We thank Drs. H. Whitney and L. Rogers at the Newfoundlandand Labrador Department of Natural Resources, Animal HealthDivision, and Dr. S. McBurney at the Atlantic Veterinary College,Canadian Cooperative Wildlife Health Centre, for their promptpost-mortem and histopathology examinations. Logistic supportwas provided by Environment Canada - Canada Wildlife Serviceand the Newfoundland and Labrador Department of NaturalResources, with special thanks to A. Blundon, P. Ryan, P. Thomas.We thank T.D. Williams for discussions about stable isotopes.S. Gilliland and P. Ryan kindly provided access to harvested birds.Carcasses were collected under Canadian Wildlife Service permitno. SS2505. Research was supported by International Polar Year,NSERC Discovery, Memorial University Career Experience Programgrants to WAM, and an NSERC scholarship to LMT.

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