MARINE ECOLOGY PROGRESS SERIESMar Ecol Prog Ser

Vol 501 157ndash168 2014doi 103354meps10670

Published March 31

INTRODUCTION

Food webs are a complex and dynamic network ofinter- and intraspecies interactions across multipletemporal and spatial scales An understanding of howecosystems function requires an understanding offood web (ie predatorminusprey) interactions (May et al1979 Christensen et al 1996 Matthiopoulos et al

2008) However relative to terrestrial fresh water andcoastal marine ecosystems predatorminusprey interactionsin the open ocean are poorly understood due to thedifficulty of sampling free-ranging pre dators andtheir prey and of conducting controlled experiments

Apex and other upper trophic level predators arefundamental in shaping and stabilising ecosystemswith respect to both their abundance and behaviour

copy Inter-Research and Fisheries and Oceans Canada 2014wwwint-rescom

Corresponding author damianlidgarddalca

Predator-borne acoustic transceivers and GPStracking reveal spatiotemporal patterns of encounters with acoustically tagged fish in

the open ocean

D C Lidgard1 W D Bowen2 I D Jonsen1 S J Iverson1

1Department of Biology Dalhousie University Halifax Nova Scotia B3H 4JI Canada2Population Ecology Division Bedford Institute of Oceanography Department of Fisheries and Oceans Dartmouth

Nova Scotia B2Y 4A2 Canada

ABSTRACT Pinnipeds are abundant upper trophic level predators in many marine ecosystemsTop-down effects of their consumption can play important roles in ecosystem structure and func-tioning However interactions between pinnipeds and their prey remain poorly understood due totheir inaccessibility while foraging at sea This uncertainty has fueled debate on the impact of sealpredation on fish stocks of commercial or conservation interest Here we show that a novel com-bination of acoustic (Vemco Mobile Transceiver VMT) and GPS technology can be used to deter-mine the spatial and temporal pattern of interactions between grey seals Halichoerus grypus andfish species in 2 large marine ecosystems the Eastern Scotian Shelf and the southern Gulf of StLawrence Canada During 4 yr of study the VMT on 9 of 64 adult grey seals recorded detectionsfrom 3 species of fish namely 17 adult Atlantic cod Gadus morhua 7 Atlantic salmon Salmo salarand 1 American eel Anguilla rostrata implanted with coded acoustic tags An examination of thetemporal and spatial pattern of these sealminusfish interactions suggested that 1 salmon and 2 codmight have been predated on However to have confidence in the occurrence of a predationevent more conclusive evidence is required which may be gathered through validation experi-ments These preliminary results provide proof-of-concept that large upper trophic level marinepredators fitted with VMT and GPS tags can provide information on species locations in areaswhere fixed receiver arrays are not present and allow new insights into the nature of interspeciesinteractions in otherwise inaccessible environments

KEY WORDS Interspecies interactions middot Grey seal middot Halichoerus grypus middot Predatorminusprey interac-tion middot Southern Gulf of St Lawrence middot Eastern Scotian Shelf

Resale or republication not permitted without written consent of the publisher

Mar Ecol Prog Ser 501 157ndash168 2014

(Estes et al 2011 Ritchie et al 2012) Technologicaladvances in telemetry have contributed towards agreater understanding of movement foraging be -haviour and habitat use of marine upper trophic levelpredators such as pinnipeds (eg Le Boeuf et al2000 Matthiopoulos et al 2004 Aarts et al 2008Breed et al 2009) Nevertheless little remainsknown about how marine mammals interact withtheir prey (Holland et al 2009 Hayes et al 2013)This limits our ability to address questions concern-ing the impact marine mammal predation may haveon fish populations of conservation or commercialinterest and the roles played by these predators inecosystem structure and functioning (Bowen 1997Matthiopoulos et al 2008)

Since the late 1980s and early 1990s Atlantic codGadus morhua stocks in eastern Canada havedeclined dramatically (Hutchings amp Myers 1994DFO 2003a) Similar trends have been observed forother fish species eg winter skate (Swain et al2013) Despite greatly reduced or halted fisheriesAtlantic cod stocks have not recovered or arerecovering at a pace slower than expected (Bundyamp Fanning 2005) Several theories have been pro-posed (eg Swain amp Mohn 2012) but none canaccount for the failure of the stocks to recoveralthough causes are likely multi faceted (Neubaueret al 2013) In contrast to the poor state of fishstocks the eastern Canadian grey seal Halichoerusgrypus population has increased from 13 000 in1960 to 410 000 in 2010 (Thomas et al 2011) Sev-eral studies have attempted to evaluate the impactof the grey seal on the recovery of depleted fishstocks with a focus on the Atlantic cod (Mohn ampBowen 1996 Fu et al 2001 Trzcinski et al 20062011 Bundy et al 2009) Among other things thesestudies have shown that model out comes are highlysensitive to estimates of the proportion of cod in thegrey sealsrsquo diet

The northwest Atlantic salmon Salmo salar in Can-ada has also been in decline and suffers fromunknown sources of high at-sea mortality (Gibson etal 2006 ICES 2008) Many Atlantic salmon popu -lations are listed as endangered by the Committeeon the Status of Endangered Wildlife in Canada(COSEWIC wwwcosewicgcca) and commercialfisheries for Atlantic salmon have been closed sinceat least the early 2000s (DFO 2008) Like Atlantic codsalmon are known to be consumed by grey seals(Beck et al 2007 Bowen et al 2011) thus under-standing the level of grey seal predation will con-tribute towards better evaluation of the sources ofsalmon mortality

Recent advances in acoustic telemetry may helpto reduce uncertainty surrounding the interactionswith and impact of marine mammals on commercialor vulnerable fish species (Holland et al 2009Stokesbury et al 2009 Lidgard et al 2012 Hayeset al 2013) Traditionally miniature acoustic trans-mitters and stationary receivers (Voegeli et al1998) were used to study interspecific interactionsA significant limitation with this design is therestricted geographical area within which infor -mation can be collected eg rivers or intertidal systems where species movements are relativelylimited and easily monitored A more recent ad -vancement is the animal-borne video camera thatprovides detailed observations of prey (Davis et al1999 Bowen et al 2002 Hooker et al 2002Heaslip et al 2012) However due to memory andbattery-life limitations the deployment period isshort and variation in video quality can lead to dif-ficulties in identifying prey The Vemco MobileTransceiver (VMT wwwvemcocom) overcomesthese problems The VMT is a 69 kHz coded trans-ceiver that alternates between transmitting a codedacoustic signal and listening for transmissions fromother Vemco 69 kHz coded acoustic transmittersAcoustic codes are unique due to the time intervalbetween pings and the length of time it takes totransmit the full code By attaching the VMT and aFastloctrade GPS satellite transmitter to a marinepredator such as a seal and tagging fish specieswith Vemco transmitters time-stamped georefer-enced records of interactions between seals andfish can be collected over extended periods of timeThus in principle one could examine species inter-actions including predation in the open ocean andseek to better understand the role of upper trophicpredators in marine ecosystems

In this study we sought to determine whether theVMT combined with Fastloctrade GPS telemetry couldbe used to examine interactions between grey sealsand several of their potential prey in 2 marine ecosys-tems off Eastern Canada

MATERIALS AND METHODS

The study was conducted between 15 October2009 and 21 January 2013 on the Eastern ScotianShelf and the southern Gulf of St Lawrence Canada(see Fig 1A) Both regions are important foragingareas for the grey seal (Breed et al 2006) The East-ern Scotian Shelf is a continental shelf (108 000 km2)composed of a series of offshore shallow banks and

158

Mar Ecol Prog Ser 501 157ndash168 2014

(Estes et al 2011 Ritchie et al 2012) Technologicaladvances in telemetry have contributed towards agreater understanding of movement foraging be -haviour and habitat use of marine upper trophic levelpredators such as pinnipeds (eg Le Boeuf et al2000 Matthiopoulos et al 2004 Aarts et al 2008Breed et al 2009) Nevertheless little remainsknown about how marine mammals interact withtheir prey (Holland et al 2009 Hayes et al 2013)This limits our ability to address questions concern-ing the impact marine mammal predation may haveon fish populations of conservation or commercialinterest and the roles played by these predators inecosystem structure and functioning (Bowen 1997Matthiopoulos et al 2008)

Since the late 1980s and early 1990s Atlantic codGadus morhua stocks in eastern Canada havedeclined dramatically (Hutchings amp Myers 1994DFO 2003a) Similar trends have been observed forother fish species eg winter skate (Swain et al2013) Despite greatly reduced or halted fisheriesAtlantic cod stocks have not recovered or arerecovering at a pace slower than expected (Bundyamp Fanning 2005) Several theories have been pro-posed (eg Swain amp Mohn 2012) but none canaccount for the failure of the stocks to recoveralthough causes are likely multi faceted (Neubaueret al 2013) In contrast to the poor state of fishstocks the eastern Canadian grey seal Halichoerusgrypus population has increased from 13 000 in1960 to 410 000 in 2010 (Thomas et al 2011) Sev-eral studies have attempted to evaluate the impactof the grey seal on the recovery of depleted fishstocks with a focus on the Atlantic cod (Mohn ampBowen 1996 Fu et al 2001 Trzcinski et al 20062011 Bundy et al 2009) Among other things thesestudies have shown that model out comes are highlysensitive to estimates of the proportion of cod in thegrey sealsrsquo diet

The northwest Atlantic salmon Salmo salar in Can-ada has also been in decline and suffers fromunknown sources of high at-sea mortality (Gibson etal 2006 ICES 2008) Many Atlantic salmon popu -lations are listed as endangered by the Committeeon the Status of Endangered Wildlife in Canada(COSEWIC wwwcosewicgcca) and commercialfisheries for Atlantic salmon have been closed sinceat least the early 2000s (DFO 2008) Like Atlantic codsalmon are known to be consumed by grey seals(Beck et al 2007 Bowen et al 2011) thus under-standing the level of grey seal predation will con-tribute towards better evaluation of the sources ofsalmon mortality

Recent advances in acoustic telemetry may helpto reduce uncertainty surrounding the interactionswith and impact of marine mammals on commercialor vulnerable fish species (Holland et al 2009Stokesbury et al 2009 Lidgard et al 2012 Hayeset al 2013) Traditionally miniature acoustic trans-mitters and stationary receivers (Voegeli et al1998) were used to study interspecific interactionsA significant limitation with this design is therestricted geographical area within which infor -mation can be collected eg rivers or intertidal systems where species movements are relativelylimited and easily monitored A more recent ad -vancement is the animal-borne video camera thatprovides detailed observations of prey (Davis et al1999 Bowen et al 2002 Hooker et al 2002Heaslip et al 2012) However due to memory andbattery-life limitations the deployment period isshort and variation in video quality can lead to dif-ficulties in identifying prey The Vemco MobileTransceiver (VMT wwwvemcocom) overcomesthese problems The VMT is a 69 kHz coded trans-ceiver that alternates between transmitting a codedacoustic signal and listening for transmissions fromother Vemco 69 kHz coded acoustic transmittersAcoustic codes are unique due to the time intervalbetween pings and the length of time it takes totransmit the full code By attaching the VMT and aFastloctrade GPS satellite transmitter to a marinepredator such as a seal and tagging fish specieswith Vemco transmitters time-stamped georefer-enced records of interactions between seals andfish can be collected over extended periods of timeThus in principle one could examine species inter-actions including predation in the open ocean andseek to better understand the role of upper trophicpredators in marine ecosystems

In this study we sought to determine whether theVMT combined with Fastloctrade GPS telemetry couldbe used to examine interactions between grey sealsand several of their potential prey in 2 marine ecosys-tems off Eastern Canada

MATERIALS AND METHODS

The study was conducted between 15 October2009 and 21 January 2013 on the Eastern ScotianShelf and the southern Gulf of St Lawrence Canada(see Fig 1A) Both regions are important foragingareas for the grey seal (Breed et al 2006) The East-ern Scotian Shelf is a continental shelf (108 000 km2)composed of a series of offshore shallow banks and

158

Lidgard et al Seal and fish encounters

inshore basins separated by deep gullies andcanyons (DFO 2003b) The southern Gulf of StLawrence (80 000 km2) is a semi-enclosed sea con-necting the St Lawrence estuary with the AtlanticOcean through 2 outlets Strait of Belle Isle andCabot Strait

Sable Island (43deg 55rsquo N 60deg 00rsquo W) is situated onthe Eastern Scotian Shelf ~300 km ESE of Halifaxand is the location of the worldrsquos largest breedingcolony of grey seals (Thomas et al 2011) Between1969 and 2002 groups of male and female greyseals at this colony were branded at weaning pro-viding a pool of individually identifiable known-age adults From this pool 44 female and 19 maleadults in addition to 9 non-branded female adultswere captured over a 4 yr period October 2009 (n= 15) September 2010 (n = 20) June 2011 (n = 20)and June 2012 (n = 17) Seals were weighed usinga 300 kg (plusmn1 kg) Salter spring balance and thenimmobilised using the chemical anaesthetic Telazol(males 045 mg kgminus1 females 090 mg kgminus1 Bowenet al 1999) to equip each seal with telemetryand data-logging devices These comprised a VHFtransmitter (164 to 165 MHz wwwatstrackcom)MK10-AF Fastloctrade GPS tag (wwwwildlifecomput-erscom) and a VMT tag The VHF tag was used tolocate animals returning to Sable Island to breed inthe following December and January The MK10-AF tag was programmed to transmit ARGOS andGPS positional data and to archive GPS data thatwere downloaded on recovery of the tag Theseunits were programmed to record a GPS locationevery 15 min GPS attempts were suspended whenthe unit was dry for gt20 min and a location hadbeen attained The VMT was programmed to trans-mit on an irregular schedule every 60 to 180 s (toavoid VMTs transmitting at the same time andcausing code collisions and false detections) toblank the receiver for the complete code transmis-sion ~36 s (to prevent the tag from receiving itsown transmission) and to remain in listening modefor the remainder of the time Peak sensitivities forhearing in phocids is between about 10 and 50 kHzwith a high frequency limit of ~100 kHz (Kasteleinet al 2009) Given the power output of the trans-mitters (146 to 149 dB re 1microPa source pressurelevel measured 1 m from the source) seals couldlikely hear the 69 kHz transmission pings (Bowleset al 2010) However if motivated it is not clearwhether a seal could localise other VMT-taggedseals or prey due to ambient background noisereflection and refraction of the signal and declinein sensitivity with the duration and frequency of

the ping (Bowles et al 2010) Seals in this studyexhibited similar foraging and breeding patterns toseals previously tagged with satellite transmittersbut with no acoustic tag (Mellish et al 1999Lidgard et al 2005 Breed et al 2006)

The VHF transmitter was attached to the MK10-AFunit using a stainless steel hose clamp and the wholeunit was attached to the hair on the top of the headusing a 5 min epoxy (Bonessl et al 1994) The VMTwas attached in the same manner as for the MK10-AF but was located on the lower back of the animalto maximise the likelihood that the tag remainedunderwater when the animal was at the surface andto minimise electromagnetic interference with theMK10-AF unit The tag mass burden (total mass oftags average body mass) was 030 for males and039 for females Individuals were recaptured during the subsequent breeding season (DecndashJan2009ndash2010 2010ndash2011 2011ndash2012 2012ndash2013) todetermine returning body mass and recover instru-ments

A total of 623 Atlantic cod were tagged with aVemco V13 acoustic transmitter in the southern Gulfof St Lawrence (249 between May 2009 and May2011) and the Eastern Scotian Shelf (374 between No-vember 2010 and November 2012) (see Fig 2) TheV13 tag is 13 mm in diameter 35 mm in length andweighs 6 g Cod ge40 cm in length were used in thisstudy since they are at a size that can accommodate aV13 tag (tag burden ~13) and are both sexuallymature and of commercial size (DFO 2009) In 2009 to2011 the V13 tags were programmed to transmit aunique acoustic code on an irregular schedule every60 to 180 s while in 2012 the transmission intervalwas reduced to every 40 to 80 s to increase the likeli-hood of detection V13 tags were placed in a sealedplastic bag and gas-sterilised using ethylene oxideBetween surgeries all instruments were kept in a panof 95 ethanol Cod were captured using longlinesset in waters lt40 m deep baited with mackerel on 14circle hooks Cod that were ge40 cm in length wereplaced in a 1000 l holding tank with seawater circula-tion until they had acclimated to the new conditionsAfter 90 min fish that were not swimming strongly orhaving trouble maintaining their position near thebottom of the tank were released Individuals werethen transferred to a 40 l tank with MS 222 (tricainemethanesulfonate 40 to 50 mg lminus1) until anaesthesiastage III2 (ie analgesia and muscle relaxation suffi-cient for most surgical procedures) was reached(~15 min) The tag was implanted in the peritonealcavity of the fish as follows Fish were removed fromthe anaesthesia bath and their length measured using

159

Mar Ecol Prog Ser 501 157ndash168 2014

an offset measuring board A small incision (2 cm) wasmade in the ventral wall of the peritoneal cavity mid-line and posterior to the pelvic fins After inserting thetransmitter the incision was closed using two 3 mmnylon sutures and a 19 mm reverse cutting needle andsealed using Vetbondtrade (www3mcom) and then covered with Polysporinreg (www polysporin ca) Theprocedure took ~1 min to complete Fish were thenplaced in a 1000 l circulating recovery tank for be-tween 45 and 90 min and released when they wereswimming strongly Fish were released close to theirsite of capture To avoid attracting predators and min-imise predation risk releases were staggered Allfield procedures were conducted in accordance withguidelines for the use of animals in research (ASAB2006) and with those of the Canadian Council on Animal Care The research protocol for the study wasapproved by the University Committee on LaboratoryAnimals Dalhousie Universityrsquos animal ethics com-mittee (animal care protocol 08-088 10-065 11-02012-64) and Fisheries and Oceans Canada (animal carepermits and licences 08-16 09-40 11-09 11-10 12-13 12-14)

During the same period of years Atlantic salmon mdashn = 298 in collaboration with the Ocean TrackingNetwork (OTN www oceantrackingnetwork org) andthe Atlantic Salmon Federation (ASF www asf ca)see Cooke et al (2011) Halfyard et al (2013) mdash andAmerican eel Anguilla rostrata mdash n = 17 in collabor -ation with the OTN University of Laval (www bio ulaval ca) Fisheries and Oceans Canada (DFOwww dfo-mpo gc ca) and Quebec Ministegravere desRessources Naturelles et de la Faune (wwwmrngouvqcca) see Cooke et al (2011) mdash weretagged with V9 or V13 Vemco acoustic transmittersto describe their distribution and movement patternsthus providing other fish species that could poten-tially be detected by instrumented grey seals (seeFig 2)

Data analysis

Archival GPS data provided more locations and ofhigher accuracy compared with the data transmittedto Service Argos thus we report only those datahere Propriety software from the manufacturer (WC-DAP www wildlife computerscom) and ar chivalephe meris data (www cddis gsfc nasa gov) wereused to determine GPS locations Locations acquiredfrom lt5 satellites andor with a residual error gt30were removed from the data set due to their loweraccuracy (Byrant 2007 Hazel 2009) VMT detectionscomprised a dateminustime stamp and the identities of

the Vemco transmitters de tected these were down-loaded and visualised using the dedicated softwareVUE (www vemcocom) False detections eg theproduction of legal codes from the collision of multi-ple codes from other active transmitters were identi-fied using proprietary software (Vemco) and deleted(16 of the total number of detections) Using thedateminustime data from each VMT and the sealrsquos GPSrecord the location of each sealminusfish encounter wasestimated using linear interpolation between GPSlocations Multiple detections were expected when aseal en countered a fish therefore it was necessary tooperationally define a sealminusfish encounter Inspec-tion of times between detections showed that 936of the data were lt10 min thus a period gt10 minbetween detections was considered to constitute theend of an encounter For encounters that involvedonly a single detection (n = 12) the duration of theassociation was set at 2 min since after this timebased on the least frequent transmission rate of theVemco transmitters another detection would haveoccurred if the 2 individuals were still together

Bottom depth and travel rate were assigned to eachseal location (Lidgard et al 2012) Bathymetric valueswere obtained from the Canadian HydrographicService (wwwdfo-mpogcca) with a 025 min resolu-tion We used the same approach as in Lidgard et al(2012) for modelling the travel rate data To discrimi-nate between 2 behavioural states (travel vs forag-ing) along each seal track and determine the activityof the seal during interactions with fish a hiddenMarkov model (HMM Patterson et al 2009 Zucchiniamp MacDonald 2009) was used We assumed that sealtravel rate is conditional on 2 discrete unobservedmovement states fast and slow movement whereslow movement (probability of area-restrictedsearch p(ARS) gt05) is assumed to be associatedwith foraging or resting behaviours (Barraquand ampBenhamou 2008)

Analyses were conducted using R statistical soft-ware v2141 (R Development Core Team 2011)Maps were generated using the Generic MappingTool (Wessel amp Smith 1995) Standard error isreported as the measure of variability

RESULTS

A total of 72 seals were studied during 4 field sea-sons (Table 1) Of these 64 (89) returned to SableIsland during the following breeding season andtheir GPS transmitter and VMT recovered Sealswere studied for an average of 79 d in 2009 to 203 d

160

Lidgard et al Seal and fish encounters

in 2011 (Table 1) In all 4 yr the movement of sealswas confined to the Eastern Scotian Shelf and thesouthern Gulf of St Lawrence with most seals usingthe former during repeated trips to and from SableIsland As estimated by the HMM seals exhibitedfast movement when moving between Sable Islandand shallow offshore areas and slower area-restricted movements over these shallow areas sug-gesting seals might be foraging (Fig 1) These move-ment patterns are typical of grey seals from SableIsland (Austin et al 2004 Breed et al 2006)

Nine of the 64 seals from which VMTs were recov-ered recorded 125 detections during 32 encounterswith Atlantic cod Atlantic salmon and American eel(Table 1 Fig 2) One Atlantic salmon smolt wasbelieved to be dead (J Carr pers comm) since it wasdetected in September when all smolts are expectedto have departed the Gulf and was excluded fromfurther analyses There were no encounters with fishin 2009 likely due to the low number of fish tagged(n = 100) and the spatial distribution of the taggedseals that did not overlap with the general areawhere the fish were tagged Sealminusfish encountersoccurred in both the southern Gulf of St Lawrence (n= 16) and on the Eastern Scotian Shelf (n = 16)(Fig 2) The location of 3 additional sealminuscodencounters was unknown due to battery failure inone of the satellite and GPS transmitters

The temporal nature of encounters between sealsand fish varied considerably (Fig 3AminusD) During themajority of encounters with Atlantic cod Atlanticsalmon (smolt or kelt) and American eel seals exhib-ited low p(ARS) values suggesting that they weremoving relatively quickly and encounters werebrief involving a single or relatively few detections(Fig 3AB) Presuming that if a fish is ingested so isits acoustic tag fish encounters that involved seal

predation are expected to show a continuous series ofdetections occurring over several hours or more asthe acoustic tag passes through the digestive tract ofthe seal None of the encounters described above hadthis expected pattern and it is more likely that theyinvolved a seal moving through an area used by atagged fish

A single encounter with an Atlantic salmon kelt(Gulf of St Lawrence) and 3 encounters with 2Atlantic cod (Canso Bank Eastern Scotian Shelf)shared a similar pattern which was different to thosedescribed above In these cases the encounters werelonger (253 176 206 and 385 min respectively)involved frequent detections (21 6 7 and 21 respec-tively) and the seals exhibited high p(ARS) values(078 10 10 and 097 respectively) suggestingarea-restricted search behaviour The characteristicsof these encounters suggest either the seal predatedon the tagged fish but did not consume the transmit-ter which may have fallen to the sea floor butremained within detection range of the VMT orthe seals were foraging in the same area as thetagged fish

In another case a seal engaged in multiple inter-rupted encounters with the same fish over anextended period of time In 2011 a single femalegrey seal detected the same Atlantic salmon kelt 3times over a 33 d period The distance between thefirst and second encounter was 7 km whereas thedistance between the second and third encounterwas 1 km The last encounter was the potential pre-dation event described above

All sealminusfish encounters occurred when the sealwas diving at depths from 4 to 74 m (Fig 3C)Encounters with cod occurred when the seal was offthe sea floor (Fig 3CD) The mean depth of all divesfor all 16 seals was 320 plusmn 80 m

161

Year No of seals Mean (plusmnSE) No of seals Fish No of No of No oftagged (recaptured) deployment with species fish detections encounters

Female Male (d) detections detected detected

2009 8(8) 7(5) 79 (plusmn06) 0 ndash ndash ndash ndash

2010 14(14) 6(6) 109 (plusmn17) 2 Atlantic salmon smolt 2 13 2

2011 20(16) ndash 203 (plusmn20) 3 Atlantic salmon kelt 2 34 4Atlantic cod 11 51 15

2012 11(11) 6(5) 196 (plusmn16) 11 Atlantic salmon smolt 1 2 1Atlantic salmon kelt 2 9 2

Atlantic cod 6 14 7American eel 1 2 1

Table 1 Number of grey seals equipped with telemetry instruments and recovered on Sable Island Nova Scotia from 2009to 2012 and details of sealminusfish encounters

Mar Ecol Prog Ser 501 157ndash168 2014162

Fig 1 (AminusD) Study area and GPS movement tracks for grey seals deployed from Sable Island in (A) 2009 (B) 2010 (C) 2011and (D) 2012 The light blue lines show the tracks of all seals The dark blue to dark red lines (coloured according to p(ARS) be -haviour mdash a continuous measure of the probability [p 0 dark blue to 1 dark red] of exhibiting area-restricted search behaviouraccording to the hidden Markov model) show the movement tracks of those seals that detected fish The white arrow indicates

the location of Sable Island

Lidgard et al Seal and fish encounters

DISCUSSION

We have shown that mobile acoustic transceiversand GPS technology deployed on an upper trophiclevel predator can be used to collect spatial and tem-poral distribution data on tagged fish over anextended period of time in a large marine ecosystemThe spatial and temporal pattern of these greysealminusfish encounters provides new opportunities forinferring the nature of interspecies interactions inlarge inaccessible environments

Our findings complement and extend previousstudies using Vemco acoustic telemetry In a pilotstudy Holland et al (2009) deployed 4 VMTs on free-roaming Galapagos sharks Carcharhinus galapagen-sis Although only 2 VMTs were recovered bothunits collected records of absence and presence fromseveral species of shark some of which occurred out-side of a monitoring acoustic arena demonstratingthe effectiveness of using mobile receivers Twenty-one VMTs recovered from northern elephant seals

Mirounga angustriostris after theirannual migration across the northeastPacific Ocean collected 9 detectionsfrom 2 species of sharks and 3 speciesof fish (Hayes et al 2013) In additionto inferences of between-species inter-actions VMT-equipped seals haverevealed an unexpectedly high num-ber of conspecific associations duringforaging trips on the Eastern ScotianShelf which may provide new insightsinto grey seal foraging behaviour(Lidgard et al 2012)

Grey seals are abundant and wide-ranging predators that are known toeat Atlantic cod (Breed et al 2006Beck et al 2007 Hammill 2010 Sten-son et al 2010 Bowen et al 2011Thomas et al 2011) Thus it is cer-tainly possible that grey seals may bepartly responsible for the lack of orslow recovery of cod stocks in thesouthern Gulf of St Lawrence and onthe Scotian Shelf However a keyuncertainty in tests of this hypothesis isthe proportion of total cod mortalityaccounted for by grey seal consump-tion (eg Mohn amp Bowen 1996) Thisquestion has been difficult to answer(eg Trzcinski et al 2006 2011)because of the limitations of the meth-ods used to estimate the diets of grey

seals and other pinnipeds and the difficulty in obtain-ing a representative sample of the diet from which todraw firm conclusions (Bowen amp Iverson 2013) Thishas led to the search for other approaches such asthe extent of spatial and temporal overlap betweenthe distribution of prey and the foraging effort of thepredator (Matthiopoulos et al 2008 Harvey amp Ham-mill 2010 Harvey et al 2012) Although such overlapis necessary it is not a sufficient basis to concludethat predation has occurred or to estimate the extentof predation

Given the absence of direct observation a degreeof speculation will be required to assess the likeli-hood of a predation event using acoustic telemetryTo determine the most likely predator of 6 silverAmerican eels tagged in the Gulf of St Lawrencewith miniature satellite pop-up tags Beacuteguer-Pon etal (2012) used temperature and depth profiles gener-ated post-predation to determine the most likelypredator In our case we expect that predationshould be evident in the continual pattern of acoustic

163

Fig 2 Distribution of fish deployments (n) grey sealminusfish encounters (s) andmovement tracks (light blue) for 16 grey seals on the Eastern Scotian Shelfand in the southern Gulf of St Lawrence from 2010 to 2012 Atlantic cod arerepresented by orange symbols Atlantic salmon smolts by red Atlanticsalmon kelts by pale yellow and American eel by blue The white arrows

indicate the location of a possible predation event

Mar Ecol Prog Ser 501 157ndash168 2014162

Fig 1 (AminusD) Study area and GPS movement tracks for grey seals deployed from Sable Island in (A) 2009 (B) 2010 (C) 2011and (D) 2012 The light blue lines show the tracks of all seals The dark blue to dark red lines (coloured according to p(ARS) be -haviour mdash a continuous measure of the probability [p 0 dark blue to 1 dark red] of exhibiting area-restricted search behaviouraccording to the hidden Markov model) show the movement tracks of those seals that detected fish The white arrow indicates

the location of Sable Island

Lidgard et al Seal and fish encounters

DISCUSSION

We have shown that mobile acoustic transceiversand GPS technology deployed on an upper trophiclevel predator can be used to collect spatial and tem-poral distribution data on tagged fish over anextended period of time in a large marine ecosystemThe spatial and temporal pattern of these greysealminusfish encounters provides new opportunities forinferring the nature of interspecies interactions inlarge inaccessible environments

Our findings complement and extend previousstudies using Vemco acoustic telemetry In a pilotstudy Holland et al (2009) deployed 4 VMTs on free-roaming Galapagos sharks Carcharhinus galapagen-sis Although only 2 VMTs were recovered bothunits collected records of absence and presence fromseveral species of shark some of which occurred out-side of a monitoring acoustic arena demonstratingthe effectiveness of using mobile receivers Twenty-one VMTs recovered from northern elephant seals

Mirounga angustriostris after theirannual migration across the northeastPacific Ocean collected 9 detectionsfrom 2 species of sharks and 3 speciesof fish (Hayes et al 2013) In additionto inferences of between-species inter-actions VMT-equipped seals haverevealed an unexpectedly high num-ber of conspecific associations duringforaging trips on the Eastern ScotianShelf which may provide new insightsinto grey seal foraging behaviour(Lidgard et al 2012)

Grey seals are abundant and wide-ranging predators that are known toeat Atlantic cod (Breed et al 2006Beck et al 2007 Hammill 2010 Sten-son et al 2010 Bowen et al 2011Thomas et al 2011) Thus it is cer-tainly possible that grey seals may bepartly responsible for the lack of orslow recovery of cod stocks in thesouthern Gulf of St Lawrence and onthe Scotian Shelf However a keyuncertainty in tests of this hypothesis isthe proportion of total cod mortalityaccounted for by grey seal consump-tion (eg Mohn amp Bowen 1996) Thisquestion has been difficult to answer(eg Trzcinski et al 2006 2011)because of the limitations of the meth-ods used to estimate the diets of grey

seals and other pinnipeds and the difficulty in obtain-ing a representative sample of the diet from which todraw firm conclusions (Bowen amp Iverson 2013) Thishas led to the search for other approaches such asthe extent of spatial and temporal overlap betweenthe distribution of prey and the foraging effort of thepredator (Matthiopoulos et al 2008 Harvey amp Ham-mill 2010 Harvey et al 2012) Although such overlapis necessary it is not a sufficient basis to concludethat predation has occurred or to estimate the extentof predation

Given the absence of direct observation a degreeof speculation will be required to assess the likeli-hood of a predation event using acoustic telemetryTo determine the most likely predator of 6 silverAmerican eels tagged in the Gulf of St Lawrencewith miniature satellite pop-up tags Beacuteguer-Pon etal (2012) used temperature and depth profiles gener-ated post-predation to determine the most likelypredator In our case we expect that predationshould be evident in the continual pattern of acoustic

163

Fig 2 Distribution of fish deployments (n) grey sealminusfish encounters (s) andmovement tracks (light blue) for 16 grey seals on the Eastern Scotian Shelfand in the southern Gulf of St Lawrence from 2010 to 2012 Atlantic cod arerepresented by orange symbols Atlantic salmon smolts by red Atlanticsalmon kelts by pale yellow and American eel by blue The white arrows

indicate the location of a possible predation event

Lidgard et al Seal and fish encounters

DISCUSSION

We have shown that mobile acoustic transceiversand GPS technology deployed on an upper trophiclevel predator can be used to collect spatial and tem-poral distribution data on tagged fish over anextended period of time in a large marine ecosystemThe spatial and temporal pattern of these greysealminusfish encounters provides new opportunities forinferring the nature of interspecies interactions inlarge inaccessible environments

Our findings complement and extend previousstudies using Vemco acoustic telemetry In a pilotstudy Holland et al (2009) deployed 4 VMTs on free-roaming Galapagos sharks Carcharhinus galapagen-sis Although only 2 VMTs were recovered bothunits collected records of absence and presence fromseveral species of shark some of which occurred out-side of a monitoring acoustic arena demonstratingthe effectiveness of using mobile receivers Twenty-one VMTs recovered from northern elephant seals

Mirounga angustriostris after theirannual migration across the northeastPacific Ocean collected 9 detectionsfrom 2 species of sharks and 3 speciesof fish (Hayes et al 2013) In additionto inferences of between-species inter-actions VMT-equipped seals haverevealed an unexpectedly high num-ber of conspecific associations duringforaging trips on the Eastern ScotianShelf which may provide new insightsinto grey seal foraging behaviour(Lidgard et al 2012)

Grey seals are abundant and wide-ranging predators that are known toeat Atlantic cod (Breed et al 2006Beck et al 2007 Hammill 2010 Sten-son et al 2010 Bowen et al 2011Thomas et al 2011) Thus it is cer-tainly possible that grey seals may bepartly responsible for the lack of orslow recovery of cod stocks in thesouthern Gulf of St Lawrence and onthe Scotian Shelf However a keyuncertainty in tests of this hypothesis isthe proportion of total cod mortalityaccounted for by grey seal consump-tion (eg Mohn amp Bowen 1996) Thisquestion has been difficult to answer(eg Trzcinski et al 2006 2011)because of the limitations of the meth-ods used to estimate the diets of grey

seals and other pinnipeds and the difficulty in obtain-ing a representative sample of the diet from which todraw firm conclusions (Bowen amp Iverson 2013) Thishas led to the search for other approaches such asthe extent of spatial and temporal overlap betweenthe distribution of prey and the foraging effort of thepredator (Matthiopoulos et al 2008 Harvey amp Ham-mill 2010 Harvey et al 2012) Although such overlapis necessary it is not a sufficient basis to concludethat predation has occurred or to estimate the extentof predation

Given the absence of direct observation a degreeof speculation will be required to assess the likeli-hood of a predation event using acoustic telemetryTo determine the most likely predator of 6 silverAmerican eels tagged in the Gulf of St Lawrencewith miniature satellite pop-up tags Beacuteguer-Pon etal (2012) used temperature and depth profiles gener-ated post-predation to determine the most likelypredator In our case we expect that predationshould be evident in the continual pattern of acoustic

163

Fig 2 Distribution of fish deployments (n) grey sealminusfish encounters (s) andmovement tracks (light blue) for 16 grey seals on the Eastern Scotian Shelfand in the southern Gulf of St Lawrence from 2010 to 2012 Atlantic cod arerepresented by orange symbols Atlantic salmon smolts by red Atlanticsalmon kelts by pale yellow and American eel by blue The white arrows

indicate the location of a possible predation event

Mar Ecol Prog Ser 501 157ndash168 2014

detections of individual prey during the pursuit andtime taken for the prey and the ingested acoustictag to pass through the predatorrsquos digestive tract andbe expelled in faeces In the case of grey seals cap-tive feeding experiments using herring Clupeaharengus cod whiting Merlangius merlangus orhaddock Gadus aeglefinus (Prime amp Hammond 1987Marcus et al 1998) found that the passage time forthe majority of prey remains was between 24 and48 h Thus during this time we would expect a reg-ular and frequent pattern of detections However it ispossible during the handling of large fish such assalmon kelts and adult cod that the transmitter maydislodge from the peritoneal cavity and fall to the seafloor or that the seal may not consume all parts of thefish (Rae 1968) In these cases and given that themean bathymetry of the areas where seals encoun-tered tagged fish was 49 plusmn 35 m we would still

expect to see a continual pattern of detections but fora much shorter duration while the tagged sealremained within proximity of the tag Although therewere no extended periods of time that would indicateingestion of the fish and tag there were 3 instanceswhen the seal spent between 250 and 485 minwithin proximity of a tagged Atlantic salmon and 2Atlantic cod and recorded frequent detections indi-cating possible predation

The speed of movement of the seal may also helpdetermine the likelihood that predation occurredWhen foraging grey seals most likely engage inarea-restricted search behaviour typical of manyanimals during foraging (Kareiva amp Odell 1987Wallin 1991 Bergman et al 2000) whereby the sealmoves slowly and turns frequently such that itremains in the prey patch In this study during themajority of encounters between grey seals and

164

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08

06

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02

00

40

30

20

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40

60

80

100

0

20

40

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3 17 1A

Dur

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in)

4 3 17 1B

Fish species

Dep

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)

1 2 3 4

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Bat

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4 3 17 1D

Fig 3 Plots describing sealminusfish encounters for grey seals on the Eastern Scotian Shelf and southern Gulf of St Lawrence from2010 to 2012 (A) Probability of seal exhibiting lsquoslow movementrsquo during an encounter (B) duration (min) of encounter (C)depth (m) of seal during encounter (dotted line signifies the mean dive depth of all 16 seals) and (D) bathymetry at encounterFish species 1 Atlantic salmon kelt 2 Atlantic salmon smolt 3 Atlantic cod 4 American eel The upper horizontal axis givesthe number of unique sealminusfish encounters note the number of dots may not correspond with the number of unique sealndashfish

encounters due to overlapping data points and unique sealndashfish events comprising of multiple encounters

Lidgard et al Seal and fish encounters

Atlantic cod Atlantic salmon or American eel theseal was moving relatively quickly in a directed man-ner suggesting travelling rather than foraging Fur-thermore although encounters occurred in relativelyshallow waters they were often not associated withthe shallow offshore banks where Sable Island greyseals are thought to forage However in those en -counters with salmon and cod that were longer induration with frequent and regular detections theseals were moving slowly suggesting area-restrictedsearch behaviour and the encounters with codoccurred at Canso Bank an area favoured by greyseals for foraging These observations therefore sup-port the possibility of a predation event Howeverwithout a strong predation signature that involvesthe seal consuming the tag the occurrence of a pre-dation event would need more conclusive evidencesuch as that gathered through validation experi-ments conducted under controlled conditions

We believe our findings demonstrate that there isadded value to the combined use of GPS or othertracking technologies and mobile acoustic receiversto contribute towards our understanding of the ex -tent that top predators associate with potential preyand support of conclusions from dietary analyses Forspecies such as Atlantic cod Atlantic salmon andAmerican eel this information is critical for identify-ing the sources of at-sea mortality Animal-bornevideo cameras have also provided insight into the for-aging ecology of marine mammals and their diet(Davis et al 1999 Bowen et al 2002 Hooker et al2002 Heaslip et al 2012) However although theycan provide detailed observations of interactionswith prey deployments are often one or a few forag-ing trips in length due to memory or battery limita-tions Variation in video quality may also make it dif-ficult to identify prey (Hooker et al 2002) The VMThas a longer life span (~8 mo) providing greater spatial and temporal coverage but compared withvideo at the cost of less detail

In the same spirit of using marine mammals to col-lect oceanographic data (Biuw et al 2007 Simmonset al 2007) VMTs deployed on top predators couldbe used to collect data on the spatial and temporaldistribution of acoustically tagged prey Although wehave some understanding of the gross movements ofAtlantic cod in the southern Gulf of St Lawrence(Campana et al 1999 Comeau et al 2002) fine-scalemovements and the movement of cod on the EasternScotian Shelf are poorly understood A better under-standing of cod seasonal distribution relative to thatof grey seals will be valuable in evaluating the oppor-tunity for grey seal predation Many populations of

the northwest Atlantic salmon in Canada have beenin decline for the last few decades with high at-seamortality for reasons largely unknown (Gibson et al2006 ICES 2008) and are listed as endangered byCOSEWIC (wwwcosewicgcca) There is also con-cern that rising sea temperatures may accentuate thedecline (Todd et al 2008) The oceanic lifestyle of codand salmon makes it difficult to assess the spatial andtemporal movement of individuals foraging areasand sources of mortality The size of satellite trans-mitters limits their use on adults and their cost limitsthe number that can be deployed (Thorstad et al2011) Acoustic transmitters however are muchcheaper and of a sufficient size to be deployed onyoung as well as older life stages In contrast to thetraditional use of stationary acoustic receivers greyseals range widely and thus can provide valuabledata on spatial and temporal patterns of fish move-ment as well as survival Furthermore a recentadvancement is the development of a Bluetooth linkbetween the satellite transmitter and the VMT thusallowing for data logged by the VMT to be transmit-ted to the satellite tag for eventual retrieval throughsystem ARGOS (authorsrsquo unpubl data) This removesthe necessity to recapture animals for instrumentrecovery and allows deployments to occur on a widerrange of species eg other pinnipeds cetaceans andturtles and in more inaccessible environments

Given the integrative nature of this work the effortrequired for this study and its success need to beevaluated within the context of the network withinwhich it operates (Cooke et al 2011) For exampleVMT-tagged grey seals collect not only records offish detections but also detections from other VMT-tagged seals to provide a better understanding ofgrey seal foraging tactics (Lidgard et al 2012) andoceanographic data to help identify the variables thatinfluence habitat choice by grey seals and fish spe-cies Strategically positioned fixed acoustic receiverarrays have collected a large volume of detectiondata from passing tagged fish and contribute towardsunderstanding seasonal changes in movement anddistribution patterns Similar to the grey sealautonomous gliders collect detection data and thusexpand the sampling effort for detecting acousticallytagged fish and collecting oceanographic data

Acknowledgements We are grateful to D Austin G BreedS Budge B Farmer N den Heyer S Heaslip W Joyce SLang E Leadon C McEwan J McMillan R Ronconi HSmith S Smith J Tremblay M Wilson and S Wong forassistance in the field We are also grateful for infrastructuresupport provided on Sable Island by Environment Canada

165

Mar Ecol Prog Ser 501 157ndash168 2014

We thank Eacute Aubry L Comeau and S Smith (Fisheries andOceans Canada (DFO)) for tagging Atlantic cod E Halfyard(Dalhousie University) J Carr and S Tinker (AtlanticSalmon Federation (ASF)) for tagging Atlantic salmon and JDussureault and M Tremblay (Ministegravere du Deacuteveloppe-ment durable de lrsquoEnvironnement de la Faune et Parcs) fortagging American eel S Hayes and 2 anonymous reviewersprovided valuable feedback on the manuscript andimproved its quality The study was supported through aResearch Network Grant (NETGP 375118-08) from the Nat-ural Sciences and Engineering Research Council (NSERC)of Canada and funds from the Canadian Foundation forInnovation (30200) and DFO NSERC Nova Scotia SalmonAssociation and ASF funded the tagging of Atlantic salmonand the Ontario Power Generation funded the tagging ofAmerican eel

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168

Editorial responsibility Peter Corkeron Woods HoleMassachusetts USA

Submitted September 10 2013 Accepted November 25 2013Proofs received from author(s) March 3 2014