ARTICLE

Marbled Murrelets (Brachyramphus marmoratus) foraging withgray whales (Eschrichtius robustus) off Vancouver Island, BritishColumbiaK.A. Muirhead, C.D. Malcolm, and D.A. Duffus

Abstract: Seabirds are known to associate with marine mammals to facilitate prey capture. These occur when mammals eitherforce prey near the surface or provide small scraps of larger prey victims. Gray whales (Eschrichtius robustus (Lilljeborg, 1861)) havebeen observed to provide invertebrate prey to a variety of seabird species; however, there are no published reports of MarbledMurrelets (Brachyramphus marmoratus (Gmelin, 1789)) feeding in association with gray whales. We observed Marbled Murreletsforaging within several metres of gray whales off Vancouver Island, British Columbia, feeding on epibenthic zooplankton in2006 and 2008. Join-count statistics identified significant clustering (p = 0.1) of 258 Marbled Murrelets within 300 m of 39 feedinggray whales in June of 2006, and no association between 3 gray whales and 34 Marbled Murrelets in June and July of 2008,marking a foraging association conditional on the abundance of both gray whales and their prey, but potentially significant toMarbled Murrelet survival and fecundity.

Key words: Marbled Murrelet, Brachyramphus marmoratus, gray whale, Eschrichtius robustus, feeding association, join-count statistic.

Résumé : Il est déja établi que des oiseaux marins s’associent a des mammifères marins pour faciliter la capture de leurs proies.Dans de telles associations, les mammifères marins forcent les proies vers la surface ou fournissent aux oiseaux de petitsrestes de proies. S’il a déja été observé que les baleines grises (Eschrichtius robustus (Lilljeborg, 1861)) fournissent des proiesinvertébrées a différentes espèces d’oiseaux marins, aucun cas n’avait encore été publié de guillemots marbrés (Brachyramphusmarmoratus (Gmelin, 1789)) s’alimentant en association avec des baleines grises. En 2006 et 2008, nous avons observé, au large del’île de Vancouver (Colombie-Britannique), des guillemots marbrés qui se nourrissaient de zooplancton épibenthique a quelquesmètres de baleines grises. La statistique de comptage a permis de définir un groupement significatif (p = 0,1) de 258 guillemotsen deça de 300 m de 39 baleines grises en quête de nourriture, en juin 2006, mais aucune association entre 3 baleines et34 guillemots en juin et juillet 2008. Ces observations indiquent que cette association d’alimentation potentiellement impor-tante pour la survie et la fécondité des guillemots marbrés est conditionnée par l’abondance tant des baleines grises que de leursproies. [Traduit par la Rédaction]

Mots-clés : guillemot marbré, Brachyramphus marmoratus, baleine grise, Eschrichtius robustus, association d’alimentation, statistiquede jointure compte.

IntroductionMany species of marine birds forage in association with other

marine predators, including fish (Colblentz 1985; Au and Pitman1986; Safina 1990) and marine mammals (Evans 1982; Au andPitman 1986; Pitman and Balance 1992; Vermeer et al. 1992). Inthese associations, seabirds benefit from access to small fish orinvertebrates forced to the surface, or by retrieval of scraps fromlarger prey torn apart by the predators. This potentially commen-sal association (e.g., Rossi-Santos and Flores 2009), where marinebirds take advantage of the feeding activities of cetaceans thatfrighten, dislodge, or disorient prey (Brockman and Barnard 1979;Harrison 1979; Au and Pitman 1986), may provide the benefit of anincreased rate of prey capture for the marine birds.

Foraging relationships with cetaceans have been identified innumerous marine bird species (Au and Pitman 1986; Mehlum et al.1998; Camphuysen and Webb 1999; Camphuysen et al. 2006). Inthe Bering Sea, Harrison (1979) documented nine species of ma-

rine birds, including four species of alcid (Parakeet Auklet, Aethiapsittacula (Pallas, 1769); Crested Auklet, Aethia cristatella (Pallas,1769); Least Auklet, Aethia pusilla (Pallas, 1811); Horned Puffin,Fratercula corniculata (J.F. Naumann, 1821)), feeding on zooplanktonin mud plumes of foraging gray whales (Eschrictius robustus (Lilljeborg,1861)). Surf Scoters (Melanitta perspicillata (L., 1758)) have been ob-served in Puget Sound, Washington, taking advantage of foraginggray whales that dislodge ghost shrimp (Neotrypaea californiensis(Dana, 1852)) from the subtidal benthic sediments (Anderson andLovvorn 2008). Martin (1986) documented shearwaters (Aves: Pro-cellaridae) responding to the presence of Atlantic spotted dol-phins (Stenella frontalis (G. Cuvier, 1829)) off the Azores Islands withincreased feeding effort and aggressiveness in circling and diving forprey. Rossi-Santos and Flores (2009) described a feeding associationbetween seabirds and Guiana dolphins (Sotalia guianensis (P.-J. vanBénéden, 1864)) in Santa Catarina, Brazil, between 1993 and 1997.Evans (1982) reviewed published accounts of seabird–cetacean feed-

Received 14 February 2013. Accepted 9 October 2013.

K.A. Muirhead* and D.A. Duffus. Whale Research Lab, Department of Geography, University of Victoria, P.O. Box 3050, Station CSC, Victoria,BC V8W 3P5, Canada.C.D. Malcolm. Department of Geography, Brandon University, Fourth Floor, John R. Brodie, Science Centre, 270 - 18th Street, Brandon, MB R7A 6A9,Canada.Corresponding author: K.A. Muirhead (e-mail: kylemuirhead@gmail.com).*Present address: 19 South Place, Altona, MB R0G 0B2, Canada.

847

Can. J. Zool. 91: 847–852 (2013) dx.doi.org/10.1139/cjz-2013-0033 Published at www.nrcresearchpress.com/cjz on 10 October 2013.

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ing interactions and made two important observations: (1) seabirdsare likely to benefit from such interactions and (2) any incident offeeding association is likely to be opportunistic.

Marbled Murrelets (Brachyramphus marmoratus (Gmelin, 1789))feed on a variety of prey, including euphausiids, mysids, and smallfish (Sealy 1975). Different prey types are linked to season andlocation. In British Columbia, Pacific sand lance (Ammodyteshexapterus Pallas, 1814) dominates the diet in late spring and sum-mer, while euphausiids (family Euphausiidae) dominate duringthe winter and early spring (Sealy 1975; Carter and Sealy 1984;Vermeer et al. 1992). Marbled Murrelets also forage opportunisti-cally (Evans 1982; Burkett 1995), but their feeding in associationwith gray whales has not been well documented.

In Clayoquot Sound (Fig. 1), gray whales forage primarily onswarms of hyperbenthic mysids (Mysidae) (Dunham and Duffus2001, 2002). During the summer months, these foraging boutsoccur around shallow, nearshore kelp beds and rocky reefs, hab-itat that is also important for foraging Marbled Murrelets. Here,we investigate a potential feeding association between graywhales and Marbled Murrelets by examining the density and dis-

tribution of feeding Marbled Murrelets in the presence of graywhales.

Materials and methods

Study areaClayoquot Sound is located on the west coast of Vancouver

Island (Fig. 1), extending up to 35 km inland and comprising265 000 ha of land and 85 000 ha of narrow inlets. Data werecollected in Cow Bay, along the southwest coast of Flores Island(49°15=N, 126°10=W) between Siwash Point in the west and theFitzpatrick Islands to the east (Fig. 2). The coastline is character-ized by rocky shores, kelp (Nereocystis luetkeana (K. Mertens) Postels& Ruprecht) beds interposed with sandy beaches and cobble bays.

Data collectionSurveys along a 600 m fixed-width transect (i.e., to 300 m from

either side of the vessel) were oriented along the 10 m depthcontour, as this depth represents an important attribute to graywhale foraging habitat in this area (Laskin 2007; Laskin et al. 2010).

Fig. 1. Research study area, Clayoquot Sound, British Columbia, Canada.

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When a whale was located, the distances and bearings of all Mar-bled Murrelets within 300 m of the vessel were recorded. Beyond300 m, we found the ability to detect murrelets with confidencebecame too low (cf. Bibby et al. 2000). Distances were estimated;observers participated in field testing with known landmarks andcontrol buoys prior to surveys. When possible, laser range finderswere used on nearby landmarks (e.g., rocky outcrops) to increaseaccuracy and confirm estimates. Gray whale position was re-corded at the location of its feeding dive, identified by a largerbreath and increased lift from the surface, and often followingone to several ventilations. Distances between murrelets andwhales were calculated as the difference, in metres, between UTMcoordinates of the individuals.

Observations in 2006 were recorded during gray whale identi-fication and habitat-use surveys, using a 6.5 m aluminum open-deck vessel. Gray whales were observed on three of three surveysbetween 5 June and 24 June of 2006, zero of nine surveys between26 May and 21 July of 2007, and two of eight surveys between23 May and 28 July of 2008. Marbled Murrelets were recorded ateach gray whale sighting.

Data analysisWe used a point pattern analysis to analyze the spatial relation-

ship between Marbled Murrelets and gray whales. Local spatialautocorrelation was measured by a join-count statistic (Alstadtet al. 2008), which assesses spatial patterns in binary data fromadjacent sampling units or regions (Upton and Fingleton 1985).The observed join-count statistic enumerates the number of adja-cent points in the data set (i.e., Marbled Murrelets (M) and graywhales (G)), with values greater than zero signifying more cluster-ing in points of the same category than would be randomly ex-pected and values less than zero signifying higher clustering inpoints of opposing categories than would be randomly expected(Fortin et al. 2002). Calculations were done at 100 and 300 mthresholds to evaluate the extent of influence of the whales.

ResultsMarbled Murrelet observations were classified into “resting”

and “feeding” categories based on their observed behaviours dur-ing the survey. In each case, if the Marbled Murrelet was observeddiving or carrying prey at the surface, then it was classified as

feeding. Marbled Murrelets that displayed no foraging activitywere classified as resting. Only those Marbled Murrelets engagedin active feeding near gray whales were considered for statisticalanalysis to reduce bias associated with the incidental presence ofboth species in the area. In 2006, we recorded 39 gray whales, and258 Marbled Murrelets feeding within 300 m of whales and88 birds feeding in areas with no whale activity (Figs. 3a, 3b, 3c). In2008, 34 Marbled Murrelets were feeding within 300 me of fivegray whales and 102 birds were feeding in areas of no whale activ-ity (Figs. 3d, 3e). In 2007, we found no instances where the MarbledMurrelets fed with gray whales. In this year, only three whaleswere observed in the area, and the likelihood of observing anyrelationship was low because these whales were rarely seen.

Based on the distribution of point data (Figs. 3a–3e), join-countstatistics for all Marbled Murrelets in the study area showed sig-nificant positive spatial autocorrelation between murrelet andwhale points in 2006 at both 100 and 300 m thresholds (Tables 1,2), indicating a greater relationship between murrelets andwhales than would be expected under complete spatial random-ness. The significantly negative statistic on these dates indicates apositive spatial autocorrelation between points of opposite val-ues, that is, gray whales and Marbled Murrelets. No significantspatial autocorrelation was found in 2008 (Tables 1, 2), suggestingno correlation between points of opposite values, that is, graywhales and Marbled Murrelets in that year of study.

DiscussionIn 2006, Marbled Murrelets foraged in clusters centred on gray

whale feeding sites. This fine-scale spatial association suggeststhat the whales acted as a cue to the presence of prey and (or)actually provided increased access to prey. Whales may help birdslocate dense prey patches, as they forage in the densest patches inthe bay (Feyrer and Duffus 2011), and through their feeding, theymay bring mysids closer to the surface or disorient the zooplank-ton making them easier to acquire. Seventy-five percent (n = 346)of the observations of murrelets in 2006 were in conjunction withforaging whales, suggesting an increased return for murrelet for-aging effort in the presence of whales in that year.

Results for 2008 failed to show the significant correlation be-tween murrelets and whales observed in 2006. This foraging rela-

Fig. 2. Cow Bay, along the south coast of Flores Island, British Columbia, Canada, and the foraging habitat of both Marbled Murrelets(Brachyramphus marmoratus) and gray whales (Eschrichtius robustus).

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tionship was observed during the spring and early summer, whengray whales tend to feed heavily on mysids and often in closeproximity with each other. In 2008, there were fewer whales inthe study area and significantly lower densities of mysid prey(Feyrer 2010). Of the total observations in 2008, 26% (n = 136) of

murrelets were seen feeding within 300 m of whales, which is a67% decrease from 2006. This lack of consistency between years ofmurrelets taking advantage of feeding gray whales suggests thatadditional underlying factors drive resource selection and forag-ing behaviour, such as the availability of other prey. The fewer

Fig. 3. Distribution of gray whales (Eschrictius robustus) and Marbled Murrelets (Brachyramphus marmoratus) across the study area, 8 June2006 (a), 9 June 2006 (b), and 12 June 2006 (c), 26 June 2008 (d), and 14 July 2008 (e). Maps depict the distribution of foraging gray whales andforaging and resting Marbled Murrelets observed along a single survey that was conducted from east to west.

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number of whales found foraging in the study area in 2008 dem-onstrates that murrelets may be more likely to respond to a preycue, but only when mysid abundance is high enough to make thisforaging behaviour energetically efficient, such as years wherefinfish abundance is low.

Gray whales in the Bering Sea are known to bring food fromdepths that would otherwise be unavailable to seabirds, and sev-eral species of seabird have been identified foraging in associationwith these whales. Correlations between gray whale locations andforaging seabirds found in studies by Harrison (1979) and Obst andHunt (1990) suggest that gray whales may act as cues to the pres-ence of large quantities of invertebrate prey. Gray whales feedingin groups create these ephemeral opportunities for the murreletsby disorienting and (or) bringing large quantities of mysids closerto the surface, allowing murrelets easier access to prey (Obst andHunt 1990) and improving breeding conditions, as well as eggproduction in female murrelets (Janssen et al. 2009) and increas-ing net energy gain for the Marbled Murrelets during chick-provisioning.

Statistically significant evidence of this feeding associationwas found in only 1 year of our study, suggesting a plasticopportunistic feeding strategy. So, although further research isrequired, mysids disturbed by feeding gray whales may repre-sent a seasonal ecological variable that can influence murreletfeeding behaviour in this area during chick-rearing. Later inthe summer when the mysid population is depleted and whalesdisperse (Dunham and Duffus 2001), this relationship is lesslikely to occur.

Previous observations involving marine birds feeding in largegroups (100s) near cetaceans often involve multiple bird speciesmassing around large prey disturbances at the surface, such asbait balls (e.g., Rossi-Santos and Flores 2009) or mud plumes (e.g.,Harrison 1979). Our study suggests that feeding associations canalso exist at smaller, more localized scale, and future marine birdand marine mammal studies should consider these potential re-lationships.

AcknowledgementsThis research was conducted through the University of Victoria

Whale Research Lab. Funding was provided by the Society for

Ecological and Coastal Research (SEACR), the Natural Sciences andEngineering Research Council of Canada (NSERC) PostgraduateScholarship program, and (in 2006) the Brandon University Re-search Council (BURC). Thanks to all of the University of VictoriaWhale Lab staff, research assistants, and volunteers that aided inthe data-collection process. Thanks also to the Ahousaht First Na-tion, as well as Hugh Clarke and family of the Ahousaht GeneralStore, for their support.

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Table 1. Results of the join-count statistics, with a 100 m threshold,between Marbled Murrelets (Brachyramphus marmoratus) and graywhales (Eschrichtius robustus).

Total number Join count

DateMarbledMurrelets

Graywhales Observed Expected Z

8 June 2006 117 10 47 98.667 −1.53579 June 2006 128 16 30 58.110 −1.155712 June 2006 101 13 23 42.991 −1.164426 June 2008 50 3 4 6.6248 −0.416714 July 2008 67 2 4 7.1174 −0.4338

Note: Z values in boldface type are significant (p = 0.1).

Table 2. Results of the join-count statistics, with a 300 m threshold,between Marbled Murrelets (Brachyramphus marmoratus) and graywhales (Eschrichtius robustus).

Total number Join count

DateMarbledMurrelets

Graywhales Observed Expected Z

8 June 2006 117 10 81 167.71 −1.53579 June 2006 128 16 94 129.38 −1.155712 June 2006 101 13 83 117.80 −1.164426 June 2008 50 3 15 13.333 0.068714 June 2008 67 2 24 42.179 −0.0741

Note: Z values in boldface type are significant (p = 0.1).

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