All clear? Meerkats attend to contextual information in close calls to coordinate vigilance

Socio-demographic factors, such as group size and their effect on predation vulnerability, have, in addition to intrinsic factors, dominated as explanations when attempting to understand animal vigilance behaviour. It is generally assumed that animals evaluate these external factors visually; howeve...

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Published inBehavioral ecology and sociobiology Vol. 65; no. 10; pp. 1927 - 1934
Main Authors Townsend, Simon W., Zöttl, Markus, Manser, Marta B.
Format Journal Article
LanguageEnglish
Published Berlin/Heidelberg Springer 01.10.2011
Springer-Verlag
Springer Nature B.V
Subjects
Online AccessGet full text
ISSN0340-5443
1432-0762
DOI10.1007/s00265-011-1202-6

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Abstract Socio-demographic factors, such as group size and their effect on predation vulnerability, have, in addition to intrinsic factors, dominated as explanations when attempting to understand animal vigilance behaviour. It is generally assumed that animals evaluate these external factors visually; however, many socially foraging species adopt a foraging technique that directly compromises the visual system. In these instances, such species may instead rely more on the acoustical medium to assess their relative risk and guide their subsequent anti-predator behaviour. We addressed this question in the socially foraging meerkat (Suricata suricatta). Meerkats forage with their head down, but at the same time frequently produce close calls ('Foraging' close calls). Close calls are also produced just after an individual has briefly scanned the surrounding environment for predators ('Guarding' close calls). Here, we firstly show that these Guarding and Foraging close call variants are in fact acoustically distinct and secondly subjects are less vigilant (in terms of frequency and time) when exposed to Guarding close call playbacks than when they hear Foraging close calls. We argue that this is the first evidence for socially foraging animals using the information encoded within calls, the main adaptive function of which is unrelated to immediate predator encounters, to coordinate their vigilance behaviour. In addition, these results provide new insights into the potential cognitive mechanisms underlying anti-predator behaviour and suggest meerkats may be capable of signalling to group members the 'absence' of predatory threat. If we are to fully understand the complexities underlying the coordination of animal anti-predator behaviour, we encourage future studies to take these additional auditory and cognitive dimensions into account.
AbstractList Socio-demographic factors, such as group size and their effect on predation vulnerability, have, in addition to intrinsic factors, dominated as explanations when attempting to understand animal vigilance behaviour. It is generally assumed that animals evaluate these external factors visually; however, many socially foraging species adopt a foraging technique that directly compromises the visual system. In these instances, such species may instead rely more on the acoustical medium to assess their relative risk and guide their subsequent anti-predator behaviour. We addressed this question in the socially foraging meerkat (Suricata suricatta). Meerkats forage with their head down, but at the same time frequently produce close calls (‘Foraging’ close calls). Close calls are also produced just after an individual has briefly scanned the surrounding environment for predators (‘Guarding’ close calls). Here, we firstly show that these Guarding and Foraging close call variants are in fact acoustically distinct and secondly subjects are less vigilant (in terms of frequency and time) when exposed to Guarding close call playbacks than when they hear Foraging close calls. We argue that this is the first evidence for socially foraging animals using the information encoded within calls, the main adaptive function of which is unrelated to immediate predator encounters, to coordinate their vigilance behaviour. In addition, these results provide new insights into the potential cognitive mechanisms underlying anti-predator behaviour and suggest meerkats may be capable of signalling to group members the ‘absence’ of predatory threat. If we are to fully understand the complexities underlying the coordination of animal anti-predator behaviour, we encourage future studies to take these additional auditory and cognitive dimensions into account.
Socio-demographic factors, such as group size and their effect on predation vulnerability, have, in addition to intrinsic factors, dominated as explanations when attempting to understand animal vigilance behaviour. It is generally assumed that animals evaluate these external factors visually; however, many socially foraging species adopt a foraging technique that directly compromises the visual system. In these instances, such species may instead rely more on the acoustical medium to assess their relative risk and guide their subsequent anti-predator behaviour. We addressed this question in the socially foraging meerkat ( Suricata suricatta ). Meerkats forage with their head down, but at the same time frequently produce close calls (‘Foraging’ close calls). Close calls are also produced just after an individual has briefly scanned the surrounding environment for predators (‘Guarding’ close calls). Here, we firstly show that these Guarding and Foraging close call variants are in fact acoustically distinct and secondly subjects are less vigilant (in terms of frequency and time) when exposed to Guarding close call playbacks than when they hear Foraging close calls. We argue that this is the first evidence for socially foraging animals using the information encoded within calls, the main adaptive function of which is unrelated to immediate predator encounters, to coordinate their vigilance behaviour. In addition, these results provide new insights into the potential cognitive mechanisms underlying anti-predator behaviour and suggest meerkats may be capable of signalling to group members the ‘absence’ of predatory threat. If we are to fully understand the complexities underlying the coordination of animal anti-predator behaviour, we encourage future studies to take these additional auditory and cognitive dimensions into account.
Socio-demographic factors, such as group size and their effect on predation vulnerability, have, in addition to intrinsic factors, dominated as explanations when attempting to understand animal vigilance behaviour. It is generally assumed that animals evaluate these external factors visually; however, many socially foraging species adopt a foraging technique that directly compromises the visual system. In these instances, such species may instead rely more on the acoustical medium to assess their relative risk and guide their subsequent anti-predator behaviour. We addressed this question in the socially foraging meerkat (Suricata suricatta). Meerkats forage with their head down, but at the same time frequently produce close calls ('Foraging' close calls). Close calls are also produced just after an individual has briefly scanned the surrounding environment for predators ('Guarding' close calls). Here, we firstly show that these Guarding and Foraging close call variants are in fact acoustically distinct and secondly subjects are less vigilant (in terms of frequency and time) when exposed to Guarding close call playbacks than when they hear Foraging close calls. We argue that this is the first evidence for socially foraging animals using the information encoded within calls, the main adaptive function of which is unrelated to immediate predator encounters, to coordinate their vigilance behaviour. In addition, these results provide new insights into the potential cognitive mechanisms underlying anti-predator behaviour and suggest meerkats may be capable of signalling to group members the 'absence' of predatory threat. If we are to fully understand the complexities underlying the coordination of animal anti-predator behaviour, we encourage future studies to take these additional auditory and cognitive dimensions into account.[PUBLICATION ABSTRACT]
Author Townsend, Simon W.
Manser, Marta B.
Zöttl, Markus
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Keywords Acoustic information
Playbacks
Vigilance coordination
Meerkats
Close calls
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PublicationDate 2011-10-01
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PublicationDate_xml – month: 10
  year: 2011
  text: 2011-10-01
  day: 01
PublicationDecade 2010
PublicationPlace Berlin/Heidelberg
PublicationPlace_xml – name: Berlin/Heidelberg
– name: Heidelberg
PublicationTitle Behavioral ecology and sociobiology
PublicationTitleAbbrev Behav Ecol Sociobiol
PublicationYear 2011
Publisher Springer
Springer-Verlag
Springer Nature B.V
Publisher_xml – name: Springer
– name: Springer-Verlag
– name: Springer Nature B.V
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SchiblerFManserMBThe irrelevance of individual discrimination in meerkat alarm callsAnim Behav2007741259126810.1016/j.anbehav.2007.02.026
BellMBVRadfordANSmithRAThompsonAMRidleyARBargaining babblers: vocal negotiation of cooperative behaviour in a social birdProc R Soc B2010277322332282051922110.1098/rspb.2010.06431:STN:280:DC%2BC3cflsV2gsw%3D%3D
ManserMBResponse of foraging group members to sentinel calls in suricates, Suricata suricattaProc R Soc B19992661013101910.1098/rspb.1999.0737
ManserMBBellMBFletcherLBThe information that receivers extract from alarm calls in suricatesProc R Soc B2001268248524911174756810.1098/rspb.2001.17721:STN:280:DC%2BD3MjgtVeisw%3D%3D
ShannonCA mathematical theory of communicationBell Syst Tech J194827379–423623656
SchelAMCandiottiAZuberbühlerKPredator-deterring alarm call sequences in Guereza colobus monkeys are meaningful to conspecificsAnim Behav20108079980810.1016/j.anbehav.2010.07.012
JenningsTEvansSMInfluence of position in the flock and flock size on vigilance in the starling, Sturnus vulgarisAnim Behav19802863463510.1016/S0003-3472(80)80071-6
GouzoulesSGouzoulesHMarlerPRhesus monkey (Macaca mulatta) screams: representational signalling in the recruitment of agonistic aidAnim Behav19843218219310.1016/S0003-3472(84)80336-X
AllisonPDMultiple regression: a primer1999Thousand OaksPine Forge
SeyfarthRMCheneyDLBergmanTFischerJZuberbuhlerKHammerschmidtKThe central importance of information in studies of animal communicationAnim Behav20108013810.1016/j.anbehav.2010.04.012
CarterAJPaysOGoldizenAWIndividual variation in the relationship between vigilance and group size in eastern grey kangaroosBehav Ecol Sociobiol20096423724510.1007/s00265-009-0840-4
ZuberbuhlerKReferential labeling in Diana monkeysAnim Behav2000599179271086051910.1006/anbe.1999.1317
TownsendSWManserMBThe function of non-linear phenomena in meerkat alarm callsBiol Lett2011747492065992610.1098/rsbl.2010.0537
RadfordANVocal mediation of foraging competition in the cooperatively breeding green woodhoopoe, Phoeniculus purpureusBehav Ecol Sociobiol20045627928510.1007/s00265-004-0785-6
EvansCSEvansLRepresentational signaling in birdsBiol Lett20072007381110.1098/rsbl.2006.0561
CheneyDLSeyfarthRMHow monkeys see the world1990ChicagoUniversity of Chicago Press
WicklerWCoordination of vigilance in bird groups: the “watchman’s song” hypothesisZ Tierpsychol19856925025310.1111/j.1439-0310.1985.tb00150.x
Fernandez-JuricicEErichsenJTKacelnikAVisual perception and social foraging in birdsTrends Ecol Evol20041925311670122210.1016/j.tree.2003.10.003
HunterTBSkinnerJDVigilance behavior in African ungulates: the role of predation pressureBehaviour1998135195211
SullivanKAInformation exploitation by downy woodpeckers in mixed-species flocksBehaviour19849129431110.1163/156853984X00128
GallistelCRThe organization of learning1990CambridgeMIT Press
BellMBVRadfordANRoseRWadeHRidleyARThe value of constant surveillance in a risky environmentProc R Soc B2009276299730051949390010.1098/rspb.2009.02761:STN:280:DC%2BD1MvotVCqsA%3D%3D
TownsendSWHollenLIManserMBMeerkat close calls encode group-specific signatures but receivers fail to discriminateAnim Behav20108013313810.1016/j.anbehav.2010.04.010
Manser MB (1998) The evolution of auditory communication in suricates (Suricata suricatta). Ph.D. thesis, University of Cambridge
BlumsteinDTDanielJCMcLeanIGGroup size effects in quokkasAust J Zool20014964164910.1071/ZO01032
WeinerNCybernetics; or control and communication in the animal and the machine1961New YorkMIT Press10.1037/13140-000
CharltonBDZhangZSnyderRJGiant pandas perceive and attend to formant frequency variation in male bleatsAnim Behav2010791221122710.1016/j.anbehav.2010.02.018
UsterDZuberbuhlerKThe functional significance of Diana monkey ‘clear calls’Behaviour200113874175610.1163/156853901752233389
EvansCSEvansLMarlerPOn the meaning of alarm calls: functional reference in an avian vocal systemAnim Behav199346233810.1006/anbe.1993.1158
RasaOAECoordinated vigilance in dwarf mongoose family groups: the ‘watchman song’ hypothesis and the costs of guardingEthology19867134034410.1111/j.1439-0310.1986.tb00598.x
SeyfarthRMCheneyDLMarlerPVervet monkey alarm calls: semantic communication in a free-ranging primateAnim Behav1980281070109410.1016/S0003-3472(80)80097-2
RadfordANRidleyARIndividuals in foraging groups may use vocal cues when assessing their need for antipredator vigilanceBiol Lett200732492521742600610.1098/rsbl.2007.0110
RiceWRAnalyzing tables of statistical testsEvolution19894322322510.2307/2409177
BednekoffPABowmanRWoolfendenGEDo conversational gutturals help Florida scrub-jays coordinate their sentinel behavior?Ethology200811431331710.1111/j.1439-0310.2008.01467.x
ManserMBThe acoustic structure of suricates’ alarm calls varies with predator type and the level of response urgencyProc R Soc B2001268231523241170387110.1098/rspb.2001.17731:STN:280:DC%2BD3Mnlt1Onug%3D%3D
CrawleyMJStatistical computing: an introduction to data analysis using S-Plus2002ChichesterWiley
BugnyarTKijneMKotrschalKFood calling in ravens: are yells referential signals?Anim Behav20016194995810.1006/anbe.2000.1668
BurkartJMvan SchaikCPCognitive consequences of cooperative breeding in primates?Anim Cogn20101311191962955110.1007/s10071-009-0263-7
SlocombeKETownsendSWZuberbuhlerKWild chimpanzees distinguish between different scream types: evidence from a playback studyAnim Cogn20091234414491911258310.1007/s10071-008-0204-x
MundryRSommerCDiscriminant function analysis with nonindependent data: consequences and an alternativeAnim Behav20077496597610.1016/j.anbehav.2006.12.028
ValoneTJFrom eavesdropping on performance to copying the behaviour of others: a review of public information useBehav Ecol Sociobiol20076211410.1007/s00265-007-0439-6
MacedoniaJMEvansCSVariation among mammalian alarm call systems and the problem of meaning in animal signalsEthology19939317719710.1111/j.1439-0310.1993.tb00988.x
LimaSLBednekoffPABack to basics of antipredatory vigilance: can nonvigilant animals detect attack?Anim Behav1999585375431047936910.1006/anbe.1999.1182
HollenLIBellMBVRadfordANCooperative sentinel calling? Foragers gain increased biomass intakeCurr Biol2008185765791842414710.1016/j.cub.2008.02.0781:CAS:528:DC%2BD1cXkvFCgtLk%3D
RidleyARRaihaniNJTask partitioning increases reproductive output in cooperative birdBehav Ecol2008191136114210.1093/beheco/arn097
HauserMDThe evolution of communication1996CambridgeMIT Press
PulliamHROn the advantages of flockingJ Theor Biol197338419422473474510.1016/0022-5193(73)90184-71:STN:280:DyaE3s7jt1OjsA%3D%3D
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References_xml – reference: CharltonBDZhangZSnyderRJGiant pandas perceive and attend to formant frequency variation in male bleatsAnim Behav2010791221122710.1016/j.anbehav.2010.02.018
– reference: SchelAMCandiottiAZuberbühlerKPredator-deterring alarm call sequences in Guereza colobus monkeys are meaningful to conspecificsAnim Behav20108079980810.1016/j.anbehav.2010.07.012
– reference: RiceWRAnalyzing tables of statistical testsEvolution19894322322510.2307/2409177
– reference: GouzoulesSGouzoulesHMarlerPRhesus monkey (Macaca mulatta) screams: representational signalling in the recruitment of agonistic aidAnim Behav19843218219310.1016/S0003-3472(84)80336-X
– reference: PulliamHROn the advantages of flockingJ Theor Biol197338419422473474510.1016/0022-5193(73)90184-71:STN:280:DyaE3s7jt1OjsA%3D%3D
– reference: Fernandez-JuricicEErichsenJTKacelnikAVisual perception and social foraging in birdsTrends Ecol Evol20041925311670122210.1016/j.tree.2003.10.003
– reference: ZuberbuhlerKReferential labeling in Diana monkeysAnim Behav2000599179271086051910.1006/anbe.1999.1317
– reference: PalombitRACheneyDLSeyfarthRMMale grunts as mediators of social interaction with females in wild chacma baboons (Papio cynocephalus ursinus)Behaviour199913622124210.1163/156853999501298
– reference: RidleyARRaihaniNJTask partitioning increases reproductive output in cooperative birdBehav Ecol2008191136114210.1093/beheco/arn097
– reference: ManserMBBellMBFletcherLBThe information that receivers extract from alarm calls in suricatesProc R Soc B2001268248524911174756810.1098/rspb.2001.17721:STN:280:DC%2BD3MjgtVeisw%3D%3D
– reference: Clutton-BrockTHGaynorDKanskyRMacCollADCMcIlrathGChadwickPBrothertonPNMO’RiainJMManserMSkinnerJDCosts of cooperative behaviour in suricates (Suricata suricatta)Proc R Soc B1998265185190949340510.1098/rspb.1998.02811:STN:280:DyaK1c7lsVCmtA%3D%3D
– reference: MacedoniaJMEvansCSVariation among mammalian alarm call systems and the problem of meaning in animal signalsEthology19939317719710.1111/j.1439-0310.1993.tb00988.x
– reference: BellMBVRadfordANRoseRWadeHRidleyARThe value of constant surveillance in a risky environmentProc R Soc B2009276299730051949390010.1098/rspb.2009.02761:STN:280:DC%2BD1MvotVCqsA%3D%3D
– reference: WicklerWCoordination of vigilance in bird groups: the “watchman’s song” hypothesisZ Tierpsychol19856925025310.1111/j.1439-0310.1985.tb00150.x
– reference: HauserMDThe evolution of communication1996CambridgeMIT Press
– reference: BlumsteinDTDanielJCMcLeanIGGroup size effects in quokkasAust J Zool20014964164910.1071/ZO01032
– reference: RadfordANRidleyARIndividuals in foraging groups may use vocal cues when assessing their need for antipredator vigilanceBiol Lett200732492521742600610.1098/rsbl.2007.0110
– reference: TownsendSWManserMBThe function of non-linear phenomena in meerkat alarm callsBiol Lett2011747492065992610.1098/rsbl.2010.0537
– reference: SlocombeKETownsendSWZuberbuhlerKWild chimpanzees distinguish between different scream types: evidence from a playback studyAnim Cogn20091234414491911258310.1007/s10071-008-0204-x
– reference: EvansCSEvansLMarlerPOn the meaning of alarm calls: functional reference in an avian vocal systemAnim Behav199346233810.1006/anbe.1993.1158
– reference: CarterAJPaysOGoldizenAWIndividual variation in the relationship between vigilance and group size in eastern grey kangaroosBehav Ecol Sociobiol20096423724510.1007/s00265-009-0840-4
– reference: WeinerNCybernetics; or control and communication in the animal and the machine1961New YorkMIT Press10.1037/13140-000
– reference: HollenLIBellMBVRadfordANCooperative sentinel calling? Foragers gain increased biomass intakeCurr Biol2008185765791842414710.1016/j.cub.2008.02.0781:CAS:528:DC%2BD1cXkvFCgtLk%3D
– reference: SnowdonCTElowsonAM‘Babbling’ in pygmy marmosets: development after infancyBehaviour20011381235124810.1163/15685390152822193
– reference: UsterDZuberbuhlerKThe functional significance of Diana monkey ‘clear calls’Behaviour200113874175610.1163/156853901752233389
– reference: FarawayJJLinear models with R2006Boca RatonChapman & Hall/CRC
– reference: GallistelCRThe organization of learning1990CambridgeMIT Press
– reference: BednekoffPABowmanRWoolfendenGEDo conversational gutturals help Florida scrub-jays coordinate their sentinel behavior?Ethology200811431331710.1111/j.1439-0310.2008.01467.x
– reference: SeyfarthRMCheneyDLMarlerPVervet monkey alarm calls: semantic communication in a free-ranging primateAnim Behav1980281070109410.1016/S0003-3472(80)80097-2
– reference: BugnyarTKijneMKotrschalKFood calling in ravens: are yells referential signals?Anim Behav20016194995810.1006/anbe.2000.1668
– reference: MundryRSommerCDiscriminant function analysis with nonindependent data: consequences and an alternativeAnim Behav20077496597610.1016/j.anbehav.2006.12.028
– reference: CheneyDLSeyfarthRMHow monkeys see the world1990ChicagoUniversity of Chicago Press
– reference: ValoneTJFrom eavesdropping on performance to copying the behaviour of others: a review of public information useBehav Ecol Sociobiol20076211410.1007/s00265-007-0439-6
– reference: HunterTBSkinnerJDVigilance behavior in African ungulates: the role of predation pressureBehaviour1998135195211
– reference: ManserMBResponse of foraging group members to sentinel calls in suricates, Suricata suricattaProc R Soc B19992661013101910.1098/rspb.1999.0737
– reference: TownsendSWHollenLIManserMBMeerkat close calls encode group-specific signatures but receivers fail to discriminateAnim Behav20108013313810.1016/j.anbehav.2010.04.010
– reference: LimaSLBednekoffPABack to basics of antipredatory vigilance: can nonvigilant animals detect attack?Anim Behav1999585375431047936910.1006/anbe.1999.1182
– reference: ShannonCA mathematical theory of communicationBell Syst Tech J194827379–423623656
– reference: Manser MB (1998) The evolution of auditory communication in suricates (Suricata suricatta). Ph.D. thesis, University of Cambridge
– reference: BurkartJMvan SchaikCPCognitive consequences of cooperative breeding in primates?Anim Cogn20101311191962955110.1007/s10071-009-0263-7
– reference: SchiblerFManserMBThe irrelevance of individual discrimination in meerkat alarm callsAnim Behav2007741259126810.1016/j.anbehav.2007.02.026
– reference: BellMBVRadfordANSmithRAThompsonAMRidleyARBargaining babblers: vocal negotiation of cooperative behaviour in a social birdProc R Soc B2010277322332282051922110.1098/rspb.2010.06431:STN:280:DC%2BC3cflsV2gsw%3D%3D
– reference: AllisonPDMultiple regression: a primer1999Thousand OaksPine Forge
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– reference: SullivanKAInformation exploitation by downy woodpeckers in mixed-species flocksBehaviour19849129431110.1163/156853984X00128
– reference: CrawleyMJStatistical computing: an introduction to data analysis using S-Plus2002ChichesterWiley
– reference: RasaOAECoordinated vigilance in dwarf mongoose family groups: the ‘watchman song’ hypothesis and the costs of guardingEthology19867134034410.1111/j.1439-0310.1986.tb00598.x
– reference: SeyfarthRMCheneyDLBergmanTFischerJZuberbuhlerKHammerschmidtKThe central importance of information in studies of animal communicationAnim Behav20108013810.1016/j.anbehav.2010.04.012
– reference: EvansCSEvansLRepresentational signaling in birdsBiol Lett20072007381110.1098/rsbl.2006.0561
– reference: Clutton-BrockTHO’RiainMJBrothertonPNMGaynorDKanskyRGriffinASManserMSelfish sentinels in cooperative mammalsScience1999284164016441035638710.1126/science.284.5420.16401:CAS:528:DyaK1MXjs1Kitrc%3D
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– reference: RadfordANVocal mediation of foraging competition in the cooperatively breeding green woodhoopoe, Phoeniculus purpureusBehav Ecol Sociobiol20045627928510.1007/s00265-004-0785-6
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Snippet Socio-demographic factors, such as group size and their effect on predation vulnerability, have, in addition to intrinsic factors, dominated as explanations...
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StartPage 1927
SubjectTerms Acoustic data
Acoustics
Animal behavior
Animal communication
Animal Ecology
Animal vocalization
Animals
Audio frequencies
Behavioral Sciences
Biomedical and Life Sciences
Coordinate systems
forage
Foraging
Foraging behavior
group size
head
hearing
Life Sciences
Mating behavior
Original Paper
predation
Predators
relative risk
Small mammals
Suricata suricatta
Zoology
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Title All clear? Meerkats attend to contextual information in close calls to coordinate vigilance
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