466 © British Birds 100 • August 2007 • 466–470

Underwater images frombird-borne camerasprovide clue to poorbreeding success of

Shags in 2005Yutaka Watanuki, Akinori Takahashi, Francis Daunt,

Katsufumi Sato, Nobuyuki Miyazaki and Sarah Wanless

ABSTRACT The first underwater digital photographs obtained by camerascarried by Shags Phalacrocorax aristotelis showed the birds diving in areas

dominated by soft coral Alcyonium digitatum and feeding on butterfish Pholis gunnellus, which were brought to the surface before being swallowed.Prey capture rates were markedly lower than previous estimates for birds

feeding on sandeels Ammodytes.This reduced foraging performance probably contributed to the very poor breeding success at the

colony on the Isle of May in 2005.

Recent advances in bio-telemetry haveprovided many exciting insights into theforaging behaviour of seabirds, particu-

larly diving species (Wilson et al. 2002).However, precisely how birds catch their preyunderwater remains largely unknown, owing tothe formidable logistical problems of observingindividuals while they are foraging. This lack ofinformation is becoming critical as concernabout breeding conditions for many commonseabirds in the UK intensifies. Breeding successof Shags Phalacrocorax aristotelis at manycolonies in eastern Britain was below average in2005 (Mavor et al. 2006). Fortuitously, we werecarrying out a pilot study in that year using newbird-borne, miniaturised, still-picture loggersand obtained hundreds of images of Shagswhile they were foraging underwater. Thequality of the images was good enough todescribe the birds’ foraging habitat, prey speciesand foraging behaviour. Previous work using a

range of different techniques (e.g. VHF radiotelemetry, time-depth recorders and wateroffloading; Wanless & Harris 1997, Watanuki etal. 2005) provided extensive background dataon the food and feeding ecology of Shags at thiscolony and indicated that birds made U-shapeddives to the seabed and typically fed on LesserSandeels Ammodytes marinus. The aims of thispaper were as follows: (i) to demonstrate thepotential of the cameras to provide high-qualityimage data of underwater foraging; and (ii) toexamine whether there was any evidence thatpoor breeding success in 2005 was associatedwith changes in foraging performance.

MethodsFieldwork was carried out on the Isle of Maybetween 17th and 20th June 2005. Two maleShags (birds 1 and 2), each with two recentlyhatched chicks, were captured on the nest usinga crook. A digital still-picture logger (DSL) was

attached to the backfeathers with Tesatape, a process thattook less than fiveminutes. After release,each bird went backto its nest andresumed brooding thechicks (plate 196).The birds were recap-tured approximately24 hours later and thelogger removed. TheDSL (DSL-380DTVmanufactured byLittle Leonardo Co.Ltd, Tokyo) was 21mm in diameter and122 mm in length andwas fitted with adepth sensor (1-m accuracy). Depth data wererecorded every second and an image (370×296pixels) was recorded every 15 seconds when thebirds had dived to a depth beyond 2 m.

The mass of the DSL in air was 72 g (c. 4%of the body mass of the male Shags). This com-paratively large size could potentially disruptthe birds’ foraging behaviour. However, valuesfor dive parameters for the two camera-loggerbirds all fell well within the range of valuesreported previously for birds at this colonyfitted with smaller devices (half the cross-sectional area and 22% of mass) (table 1).

Inspection of the dive profiles confirmed thefindings of Watanuki et al. (2005) that birdsmade U-shaped dives, and thus descent, bottomand ascent phases were easily defined usingdepth-change rates. Dives shallower than 5 m

were excluded from the analysis since the imagedata indicated that these were for travelling orwashing rather than feeding.

A total of 265 and 448 images were collectedfrom birds 1 and 2, respectively. By comparingthe time when each picture was taken with thetime-depth profile, images were assigned to thedescent, bottom, and ascent phase of a dive.Because of the time lag in commands and delaybefore data were stored, some images were alsocollected during the surface phase. Images takenduring the bottom phase provided informationon foraging habitat, while those at the surfacegave information on the prey caught and prey-handling behaviour.

ResultsDuring the breeding season, Shags forage solely

Underwater images from bird-borne cameras

467British Birds 100 • August 2007 • 466–470

196. Shag Phalacrocorax aristotelis brooding its young after being fitted with a back-mounted, digital still-picture camera logger, Isle of May, June 2005.

Akin

ori T

akah

ashi

Table 1. Foraging habitat, dive parameters (mean±standard deviation) and foraging success for two ShagsPhalacrocorax aristotelis fitted with digital still-picture loggers, Isle of May, June 2005. Ranges of parameter

values from a previous study using smaller devices (Watanuki et al. 2005) are shown for comparison.

Bird Dive Habitat No. Depth Duration Surface Descent rate Ascent rate No.ID bout dives (m) (s) time (s) (m/s) (m/s) butterfish

1 1 Soft coral 26 30±1 82±17 102±43 1.6±0.1 1.9±0.2 5

1 2 Rocky seaweed 11 22±11 64±21 44±9 1.5±0.1 1.7±0.4 0

1 3 Soft coral 10 29±11 70±27 88±67 1.4±0.2 1.6±0.3 3

1 4 Unknown 4 28±13 85±31 80±51 1.2±0.5 1.5±0.2 0

2 1 Soft coral 48 19±1 59±10 65±27 1.3±0.1 1.9±0.2 5

2 2 Soft coral 19 22±2 66±13 75±31 1.2±0.1 1.9±0.2 0

2 3 Rocky seaweed 64 11±3 42±13 31±11 1.4±0.4 1.8±0.4 1

Previous study 10–41 43–97 not reported 1.2–1.8 1.4–2.2

during the day. Data obtained from the DSLconfirmed that both birds followed this pattern.Bird 1 made a total of 51 dives in four boutsbetween 05.00 hrs and 11.00 hrs (BST) and bird2 made a total of 131 dives in three boutsbetween 07.30 hrs and 19.00 hrs (table 1).

Foraging habitatImages taken during the bottom phase of thedive, showing the area where the bird was for-aging, were obtained for 112 (85%) dives forbird 2, but for only 24 (47%) dives for bird 1.This was because the latter made deeper dives,where the reduced light levels resulted inpoorer-quality images. It was possible to char-acterise the foraging habitat used by the twobirds for six of the seven dive bouts recorded(table 1). In all cases, the birds were feedingclose to the seabed and during four bouts theywere associated with areas where the bottomwas relatively flat and the soft coral Dead Man’sFingers Alcyonium digitatum was extremelyabundant (plate 197a, b). Images from bird 1’sthird dive bout indicated that this soft-coral-dominated habitat occurred close to the Isle ofMay as the island’s cliffs were visible in some ofthe images when the bird was at the surface(plate 197c). Images for the remaining threebouts gave no indication of the location of thesoft-coral areas relative to the colony. Both birds

also foraged in rocky, seaweed-dominated areasduring one of their dive bouts (plate 197d).Dive depths in this habitat tended to be shal-lower than in the Alcyonium areas (3–26 mcompared with 13–30 m).

Prey capture and handlingAlthough the bird’s head was frequently in viewin images taken during the bottom phase of thedive, there was no sign of any prey. However, 13images of the birds at the surface showed thebird holding a single fish, which in every casewas a butterfish Pholis gunnellus (plate 197c, e).Six were wrapped around the bird’s beak sowere probably still alive, suggesting that thebirds had to return to the surface to handle andswallow this species. Twelve (92%) butterfishwere associated with the Alcyonium habitat,only one was taken in the rocky/seaweed area.By classifying the dives as successful (fishpresent in bill on surfacing) and unsuccessful(no fish), the estimated success rates were foundto be 40% of dives (prey capture rate 0.4 fishper dive) and 19% (0.2 fish per dive) for birds 1and 2, respectively.

DiscussionShags on the Isle of May normally feed predom-inantly on Lesser Sandeels (Harris & Wanless1991) and work in which food loads were

468 British Birds 100 • August 2007 • 466–470

Underwater images from bird-borne cameras

197. Examples of images obtained from digital still-picture loggers deployed on Shags Phalacrocorax aristotelisbreeding on the Isle of May, June 2005: (a) bird 2 foraging at 18 m in an area dominated by the soft coral DeadMan’s Fingers Alcyonium digitatum; (b) bird 2 in the same habitat in more detail; (c) bird 1 on the surface with a

small butterfish Pholis gunnellus after a dive to 39 m (the Isle of May is visible in the background); (d) bird 2foraging at 11 m over a rocky bottom among fronds of seaweed Laminaria; (e) bird 2 in rocky habitat showing

starfish Asterias rubens; (f) bird 1 at the surface after a dive to 29 m with a large butterfish in its bill.

a b c

d e f

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Underwater images from bird-borne cameras

obtained from radio-taggedShags has indicated thatmultiple prey capture andingestion on a dive mustoccur regularly (Wanless etal. 1993). However, moni-toring in 2005 showed thatbutterfish was a major com-ponent of the diet (presentin 9 (56%) of 16 regurgita-tions; pers. obs.). Image datafrom the DSLs were consis-tent with this finding interms of both the fish actu-ally captured and the habitatthe birds were using, whichwas completely unsuitablefor sandeels. Our results alsoindicate a marked change inforaging strategy, with amaximum of only one itembeing caught per dive andthe bird returning to thesurface to handle and swallow the prey.Breeding success of Shags on the Isle of Maywas extremely poor in 2005 (0.48 chicks fledgedper laying pair compared to the long-termaverage of 0.86 for the period 1986–2003; per-sonal data). Breeding failures at this colony havebeen linked to stormy weather (Aebischer 1993)and low food availability, particularly ofsandeels (Aebischer 1986; Rindorf et al. 2000).There was nothing to suggest that the weatherwas unusual in 2005. However, the prey capturerate of Shags feeding on butterfish (0.2–0.4fish/dive) in 2005 was markedly lower thanvalues for birds feeding on sandeels (average 2.7fish/dive; Wanless et al. 1993). While compar-ison of prey capture rates obtained using dif-ferent methods should be treated with caution(both techniques probably underestimatesuccess), our results provide circumstantial evi-dence that the low breeding success of Shags in2005 was mediated, at least in part, by poor for-aging performance.

Previous theoretical work has shown thattwo of the most critical relationships betweencomponents of the dive cycle are those betweenbottom time and dive depth, and surface timeand preceding dive time (e.g. Houston &Carbone 1992). However, how these relation-ships are altered by prey capture has rarely beenstudied in wild birds. We used the image data atthe surface to estimate dive success and the

results indicate that, for Shags feeding on but-terfish, bottom time was reduced on successfuldives (fig. 1). In contrast, surface times tendedto be slightly longer after successful dives. Theserelationships accord with those predicted forbirds feeding on prey items that are difficult tofind and handle. Thus a dive ends when prey iscaught, while the time needed to subdue andswallow the prey may extend the surface time.

Underwater animal-borne cameras haveonly recently become small enough to bedeployed on birds and most work has beencarried out on penguins (Spheniscidae). Resultshave been used to determine diet and prey-capture behaviour (Ponganis et al. 2000) and toinvestigate social interactions with other birdsduring foraging (Takahashi et al. 2004). Neitherof the two Shags followed in this study seemedto associate with any conspecifics. Again thismay reflect the fact that birds were feeding onbutterfish, which are territorial, unlike sandeels,which occur at very high densities either inshoals or buried in sandy substrates (Wheeler1978).

Animal-borne cameras offer enormousopportunities for increasing our knowledge ofhow diving birds interact with their prey.Rapidly changing oceanographic conditions inthe North Sea may result in changes of diet forseabird species and camera loggers have thepotential to help to quantify these effects.

0 5 10 15 20 25 30 35 40 45dive depth (m)

Fig. 1. The relationship between time spent at the sea bottom and dive depthfor dives made by two Shags Phalacrocorax aristotelis fitted with digital still-

picture loggers, Isle of May, June 2005. Bottom time for successful dives wherebirds were subsequently recorded at the surface with fish tended to beshorter than that for dives where the bird was apparently unsuccessful.

120

100

80

60

40

20

0

time

spen

t at

the

sea

bot

tom

(s)

SuccessfulUnsuccessful

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Underwater images from bird-borne cameras

Acknowledgments

Mike Harris provided advice at all stages of this project,Alan Osborn helped with identification and ScottishNatural Heritage allowed us to work on the Isle of May.We thank the many people who have helped to collectthe long-term data on Shags and JNCC Support Co forfinancial contributions to the study.The work in 2005 wassuppor ted by grants from the Japanese Society forPromotion of Science to YW (#17370007) and KS(#15255003).

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Yutaka Watanuki, Graduate School of Fisheries Sciences, Hokkaido University, Minato-cho 3-1-1,Hakodate 041-8611, Japan; e-mail ywata@fish.hokudai.ac.jpAkinori Takahashi, National Institute of Polar Research, 1-9-10 Itabashi-ku, Tokyo 173-8515, Japan

Francis Daunt & Sarah Wanless, Centre for Ecology & Hydrology, Banchory, Aberdeenshire AB31 4BW

Katsufumi Sato, International Coastal Research Center, Ocean Research Institute, University of Tokyo,Otsuchi, Iwate 028-1102, Japan

Nobuyuki Miyazaki, Ocean Research Institute, University of Tokyo, 1-15-1 Minamidai, Nakano,Tokyo 164-8639, Japan