RESEARCH ARTICLE
Risso’s dolphins plan o aging di es
Pa icia A anz
1,2,
*, Kelly J. Benoi -Bi d
3
, B andon L. Sou hall
4,5
, John Calambokidis
6
, A i S. F iedlaende
4,7
and
Pe e L. Tyack
1
ABSTRACT
Humans emembe he pas and use ha in o ma ion o plan u u e
ac ions. Lab expe imen s ha es memo y o he loca ion o ood show
ha animals ha e a simila capabili y o ac in an icipa ion o u u e
needs, bu less wo k has been done on animals o aging in he wild. We
hypo hesized ha planning abili ies a e c i ical and common in b ea h-
hold di e s who adjus each di e o o age on p ey a ying in quali y,
loca ion and p edic abili y wi hin cons ain s o limi ed oxygen
a ailabili y. We equipped Risso’s dolphins wi h sound-and-mo ion
eco ding ags o e eal whe e hey ocus hei a en ion h ough hei
ex e nally obse able echoloca ion and how hey ine une sea ch
s a egies in esponse o expec ed and obse ed p ey dis ibu ion. The
in o ma ion om he dolphins was in eg a ed wi h synop ic p ey da a
ob ained om echosounde s on an unde wa e ehicle. A he s a o
he di es, whales adjus ed hei echoloca ion inspec ion anges in ways
ha sugges planning o o age a a pa icula dep h. Once en e ing a
p oduc i e p ey laye , dolphins educed hei sea ch ange compa able
o he scale o pa ches wi hin he laye , sugges ing ha hey we e using
echoloca ion o selec p ey wi hin he pa ch. On ascen , hei sea ch
ange inc eased, indica ing ha hey decided o s op o aging wi hin ha
laye and s a ed sea ching o p ey in shallowe laye s. In o ma ion
abou p ey, lea ned h oughou he di e, was used o plan o aging in he
nex di e. Ou esul s demons a e ha planning o u u e di es is
modula ed by spa ial memo y de i ed om mul i-modal p ey sampling
(echoic, isual and cap u e) du ing ea lie di es.
KEY WORDS: P eda o –p ey dynamics, Pe cep ual ange,
G ampus g iseus, Animal decision making, Episodic-like memo y,
Fo aging beha iou
INTRODUCTION
Animals use pas expe iences o make decisions abou u u e e en s
(Os a h and Ma in-O das, 2014; P ei e and Fos e , 2013). The
abili y o emembe in o ma ion abou esou ce dis ibu ion and use
his o plan o aging allows hem o educe hei sea ch ime and
inc ease o aging e iciency, ep esen ing a po en ial a ge o
na u al selec ion (Benhamou, 1994; Saye s and Menzel, 2012). This
abili y o an indi idual o ecall empo ally da ed e en s and
empo al–spa ial ela ionships among hese e en s is called
‘episodic memo y’in humans (Tul ing and Donaldson, 1972).
The abili y o go back in ime (episodic memo y) and o p ojec in o
he u u e is e med ‘men al ime a el’(Suddendo and Co ballis,
1997; Cheke and Clay on, 2010) and was ega ded, un il ecen ly, as
an exclusi ely human abili y. This emains a con en ious subjec in
compa a i e cogni ion (She lewo h, 2007; Vonk and Shackel o d,
2012; Robe s e al., 2012). While challenging o demons a e in
non-linguis ic animals, h ee beha iou al c i e ia, namely con en ,
s uc u e and lexibili y, ha e been p oposed o es ing episodic-
like memo y and u u e planning in animals (Clay on e al., 2003).
Resea ch in he las decade has sough o explo e he capaci y o
in o med o esigh in non-humans, pa icula ly whe he an animal’s
beha iou can be d i en by he an icipa ion o a u u e need ha is
di e en om i s cu en mo i a ional s a e (Suddendo and
Co ballis, 1997).
A se ies o inno a i e s udies ha e shown ha cap i e bi ds lea n
o p o ide o upcoming needs, ca ching ood whe e hey ha e
lea ned ha i will no be a ailable when hey a e hung y in he
u u e (Raby e al., 2007). Ra s modi y consump ion o one ood
ype in an icipa ion o access o ano he (C ys al, 2012). Apes
ained in he lab o selec an objec du ing a sho ime window can
o ego selec ing an objec ha would sa is y an immedia e
mo i a ion and ins ead selec a ool ha hey plan o use o
ob aining some hing be e hou s la e (Mulcahy and Call, 2006;
Os a h and Os a h, 2008).
Ai -b ea hing ma ine p eda o s ha o age a dep h mus al e na e
be ween wo spa ially seg ega ed esou ces: ood a dep h and
oxygen a he su ace. Thus, we hypo hesized ha hey ha e he
abili y o plan hei ac i i ies acco ding o pas expe iences and hei
needs o bo h esou ces. E idence o his is ound in penguins and
pinnipeds, which inc ease hei oxygen s o e when hey expec o
o age deepe (Wilson, 2003; Sa o e al., 2011; Gallon e al., 2007).
Simila ly, male spe m whales in high-la i ude habi a s adjus hei
echoloca ing sampling beha iou a he s a o di es ela i e o he
expec ed ange o p ey (Fais e al., 2015). While hese examples
sugges planning in di e en species, hey lack da a abou bo h p io
explo a o y sensing beha iou and he en i onmen al con ex o
animal decisions –speci ically, he ine-scale dis ibu ion o
epheme al p ey –da a ha a e impo an o expe imen al
demons a ions o u u e planning.
Echoloca ing p eda o s acqui e senso y in o ma ion by scanning
he en i onmen using di ec ional sona pulses and e alua ing he
ime delay om pulse o echo o es ima e ange (Su lykke e al.,
2009; Seibe e al., 2013). We call he ange associa ed wi h he
ound- ip a el ime o he in e -click in e al he ‘inspec ion
ange’. To a oid pulse–echo o e lap, which may esul in
ambiguous ange es ima ions, echoloca ing species gene ally
adjus hei click a e o allow echoes o a i e be o e he nex
pulse is emi ed (Simmons, 1973; Kadane and Penne , 1983). This
means ha h ough ac i e acous ic sensing, hey e eal whe e hey
a e ocusing hei a en ion o na iga e and ind p ey. Mo eo e , hey
Recei ed 21 June 2017; Accep ed 18 Decembe 2017
1
Sea Mammal Resea ch Uni , School o Biology, Uni e si y o S And ews, Eas
Sands, S And ews KY16 8LB, UK.
2
Depa men o Animal Biology, Uni e si y o La
Laguna, A da. As o isico Fco Sanchez s/n, La Laguna 36200, Tene i e, Spain.
3
Mon e ey Bay Aqua ium Resea ch Ins i u e, 7700 Sandhold Road, Moss Landing,
CA 95039, USA.
4
Sou hall En i onmen al Associa es, 9099 Soquel D i e, Sui e 8,
Ap os, CA 95003, USA.
5
Long Ma ine Labo a o y, Ins i u e o Ma ine Sciences,
Uni e si y o Cali o nia San a C uz, 1156 High S , San a C uz, CA 95064, USA.
6
Cascadia Resea ch Collec i e, 218 1/2 4 h A e W, Olympia, WA 98501, USA.
7
Depa men o Fishe ies and Wildli e, Ma ine Mammal Ins i u e, 2030 Ma ine
Science D i e, Newpo , OR 97365, USA.
*Au ho o co espondence ([email p o ec ed])
P.A., 0000-0001-8998-5149
1
© 2018. Published by The Company o Biologis s L d
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Jou nal o Expe imen al Biology (2018) 221, jeb165209. doi:10.1242/jeb.165209
Jou nal o Expe imen al Biology
p oduce as click se ies e med ‘buzzes’when hey a emp o
cap u e p ey (Mille e al., 2004; Johnson e al., 2004; A anz e al.,
2016), p o iding an indica o o o aging choices. This makes
biosona an e ec i e senso y sys em o explo ing he manne in
which animals ac i ely seek in o ma ion h ough hei senses and
how hey p ocess, e ain and decide o ac on i , when combined
wi h he esul ing o aging beha iou and da a on p ey dis ibu ion.
The ma ine en i onmen is cha ac e ized by a high le el o
pa chiness and ood esou ces in shallow wa e s can be epheme al
and occu a e y di e en densi ies (S eele, 1976). In con as ,
small midwa e animals ha se e as impo an p ey o many
species o en o m ‘deep sca e ing laye s’ ha ex end ho izon ally
o ens o kilome es o mo e wi hin a ela i ely cons an dep h
ange. While p edic able, hese laye s may ep esen a less-
accessible esou ce o an animal ha mus hold i s b ea h o
o age a dep h. The p esence o unp edic able shallow esou ces
wi h mo e p edic able deep p ey in oduces he p oblem o decision
making o ai -b ea hing ma ine p eda o s. One solu ion o hese
p eda o s would be o sample p ey oppo unis ically (She lewo h,
1998), hen plan hei o aging di es acco dingly (Dunlap and
S ephens, 2012) wi hin he cons ain s imposed by limi ed oxygen
a ailabili y. Echoloca ing di e s may be able o assess cu en
esou ces using hei long- ange biosona (Au, 1993; A anz e al.,
2016), which could be a c i ical capabili y needed o decide ea ly in
di es whe e o o age (Au e al., 2000). The maximum sona ange
o delphinids is hough o be <100 m o indi idual p ey i ems
(Madsen e al., 2007), bu i dense p ey laye s p o ide s onge sona
a ge s, his could allow hem o be de ec ed a g ea e anges
(Au and Lamme s, 2016). While sea ch ime migh be educed by
echoloca ion on descen , o aging e iciency may be u he
inc eased by emembe ing in o ma ion abou p ey loca ion, ype
and alue om he las di e and using i o plan he nex o age
be o e s a ing he nex di e (Benhamou, 1994; Saye s and Menzel,
2012; Ba aquand e al., 2009). I so, echoloca ing ma ine p eda o s
ep esen a p omising model o s udying whe he animals can ecall
pas e en s o s a egize o he u u e.
We in es iga ed whe he he echoloca ing ma ine p eda o Risso’s
dolphin, G ampus g iseus (Cu ie 1812), uses p io in o ma ion
abou p ey dis ibu ion o plan o aging. Mo e speci ically, we
explo ed whe he hese dolphins use in o ma ion abou p ey ea u es
om p e ious di es o plan he nex o aging di e and how hese
plans a e a ec ed by p ey encoun e a es du ing he o aging di e. As
analysis o he ela ionship be ween en i onmen al inpu and
beha iou al ou pu is equi ed o unde s and he p ocesses ha
media e be ween hem (She lewo h, 2001), he e we used ine-scale
p eda o beha iou al da a eco ded wi h suc ion-cup-a ached sound-
and-mo ion eco ding ags (Johnson and Tyack, 2003) coupled wi h
independen and concu en p ey measu emen s ob ained om
shipboa d and unde wa e ehicle-based echosounde sys ems. We
p esen an in eg a i e s udy linking pe cep ion, memo y and
senso imo o con ol in o ma ion om a ee- anging p eda o o in
si u p ey ields, p o iding he con ex in which animal decisions a e
execu ed unde na u al condi ions. We used hese da a o in es iga e
he unde lying cogni i e mechanisms p eda o s use o ind p ey and
o age e ec i ely in dynamic en i onmen s.
MATERIALS AND METHODS
Da a collec ion
P eda o s
G ampus g iseus, o San Clemen e Island, CA, USA, we e
equipped wi h high- esolu ion, sound-and-mo emen eco ding
ags (DTags; Johnson and Tyack, 2003) be ween 2011 and 2016.
The agging p ocedu e is desc ibed in de ail in A anz e al. (2016).
Focal ollows o agged animals we e conduc ed om he ag boa
using VHF adio acking equipmen wi hin a minimum ange o
25 m. The acks o agged dolphins we e geo- e e enced when
possible om isual obse a ions using GPS (Fig. 1). Acous ic
da a we e sampled in s e eo wi h a 16-bi esolu ion a 240 kHz.
P essu e senso , i-axial accele ome e and magne ome e da a
we e sampled a 200 Hz pe channel and decima ed o 25 Hz o
analysis. Pi ch and dep h o he agged dolphins we e de i ed om
o ien a ion and p essu e senso s on he ags (Johnson and Tyack,
2003). Tag da a p ocessing and analysis we e ca ied ou using
MATLAB (h p://www.ma hwo ks.es/), DTag oolbox and cus om
unc ions.
O he 33 agged dolphins, 18 we e exposed o playbacks o
acous ic s imuli as pa o he Sou he n Cali o nia Beha io al
Response S udy (SOCAL-BRS; Sou hall e al., 2012), bu only
beha iou al da a eco ded be o e he onse o he playbacks we e
analysed o exposed dolphins. Di es we e de ined as e ical
excu sions >20 m dep h. Di e bou s we e de ined as a g oup o
di es ending wi hin 10 min o he s a o he nex one. These dep h
–118.326 –118.281 –118.237 –118.192 –118.147
–118.326 –118.281 –118.237 –118.192 –118.147
33.304
33.335
33.367
33.304
33.335
33.367
Fig. 1. Map o hyd oacous ic su ey and
dolphin agging expe imen s o Ca alina
Island. Lines ep esen acous ic ansec s,
whi e and g ey o he ship and yellow o he
obo ; do ed lines ep esen he acks o he
agged dolphins, in e ed om su ace
obse a ions.
2
RESEARCH ARTICLE Jou nal o Expe imen al Biology (2018) 221, jeb165209. doi:10.1242/jeb.165209
Jou nal o Expe imen al Biology
and ime c i e ia we e selec ed based on he change o slope o he
log-su i o ship plo o maximum di e dep hs and in e -di e
in e als, espec i ely (Sla e and Les e , 1982). Di es ha s a ed
wi hin 15 min o a achmen o he ag we e excluded o emo e da a
po en ially a ec ed by he agging p ocedu e. Incomple e di es a
he s a o end o he eco d we e also excluded. Fi e ag eco dings
did no ha e su icien da a o mee ou c i e ia and we e no u he
analysed.
P ey
Synch onous da a on he dis ibu ion o p ey we e ob ained o
wo agged G. g iseus (gg13_266b and gg13_267) om ship-
and au onomous unde wa e ehicle (AUV)-based hyd oacous ic
su eys (spli -beam Sim ad EK60s a 38 and 120 kHz). An
echosounde in eg a ed in o a REMUS 600 AUV (Moline e al.,
2015) sampled a dep hs whe e di ing p eda o s we e eeding,
allowing indi idual p ey animals ( a ge s) o be esol ed. Ins umen
speci ica ions and calib a ion me hods we e acco ding o hose in
Moline e al. (2015). Vessel-based echosounde ansec s we e
conduc ed du ing he day ime a an a e age speed o 2 m s
−1
,
co e ing he sides o a squa e o ∼12 km
2
o e lapping in space and
ime wi h agged dolphin acks (Fig. 1). The AUV sampled a a
speed o ∼1.5 m s
−1
a he dep hs o iden i ied sca e ing ea u es.
Hyd oacous ic da a we e p ocessed using Eco iew (h p://we labs.
com/so wa e/eco iew-0). The maximum acous ic in ensi y a ei he
38 o 120 kHz was in eg a ed in o 50 cm dep h by 1 min ime bins
be o e he de ec ion o laye s. Fo each bin, a unning 25 m median
cen ed on he bin was calcula ed e ically o de ine he backg ound
sca e ing. The emo al o he backg ound om he maximum
acous ic in ensi y o each bin e ealed he dep h dis ibu ion o
sca e ing laye s. The edges o laye s we e de ined as he i s and
las loca ions in a con iguous ea u e ha exceeded he backg ound.
The uppe and lowe bounda ies o each dep h laye o e he
sampling a ea we e de ined as he hi d qua ile o each edge’s dep h
ac oss he samples. Ta ge s eng h o indi idual p ey wi hin
sca e ing ea u es measu ed wi h he AUV was es ima ed om
echoes o single a ge s (a single e u n ecei ed pe acous ic
e e be a ion olume o each pulse; Sawada e al., 1993), a 38 and
120 kHz, which acili a ed coa se axonomic classi ica ion (by
equency esponse) and size es ima ion. In addi ion, hese da a we e
used o examine in e -indi idual and in e -g oup spacing o p ey in
laye s.
Tag da a analysis
Da a om he wo dolphins o which p ey da a we e a ailable we e
used o de ine di e classes by looking a he maximum di e dep h
and he dis ibu ion o he sca e ing ea u es. Mos di es had a
maximum dep h ha ell wi hin one o he laye s. Di es wi h a
maximum dep h ha did no all in o one o he laye s (15%) we e
classi ied as pe aining o he nea es shallowe laye . In shallow
di es, he descen and ascen phases we e no de ined because he
shallow bounda y o he p ey laye (25 m) was jus 5 m below he
20 m de ini ion o he s a o he di e. Fo buzz a e analysis
in ol ing he la ge da a se (N=174 di es om 28 dolphins),
including he 26 dolphins whe e he p ey laye s we e no measu ed,
he bo om phase was de ined as deepe han 70% o he maximum
dep h (A anz e al., 2016). Echoloca ion clicks and buzzes we e
isola ed on he eco dings om he agged dolphins ollowing he
me hods desc ibed in A anz e al. (2016). Fo aging di es we e
de ined as di es ha con ained one o mo e buzzes eco ded om
he agged dolphin, because buzzes indica ed p ey sea ch and
cap u e (A anz e al., 2016). The in e -click in e al o he dolphins
a a ce ain pi ch angle was used o es ima e hei inspec ion slan
ange. The e ical componen o his inspec ion ange equalled he
slan ange imes he sin (pi ch). The inspec ion dep h was
calcula ed by adding he dep h o he dolphin plus he e ical
componen o he inspec ion ange. When aken om he i s clicks
in he di e, he in e -click in e al can be used as an indica o o he
expec ed ange o p ey o an echoloca ing p eda o based on
in o ma ion ga he ed on he p e ious di e, be o e new in o ma ion
is gained ia echoloca ion (Fais e al., 2015). The ini ial inspec ion
ange was compu ed om he maximum in e -click in e al o he
i s h ee clicks emi ed in he di e by he agged dolphin. We used
Spea man’s ank ρ o check o mono onic co ela ions be ween
dolphin and p ey a iables, as he assump ion o linea i y ailed a e
compa ing hem wi h a i ed e sus esidual plo . S a is ical
signi icance was judged a a c i ical P- alue o 5%.
To compa e ela i e mo emen s o he animals a he bo om
phase o di es associa ed wi h o aging in di e en p ey laye s, we
econs uc ed he dead- eckoned ack o he dolphins (sensu
Johnson and Tyack, 2003). Swim speed was app oxima ed om
he e ical eloci y ( a e o change o dep h) and pi ch angle o he
dolphins using a Kalman il e . The ack was gene a ed by
combining swim speed du ing he bo om phase o he di e wi h he
pi ch and heading o he dolphin a a 1 Hz sampling a e. The
a e age pi ch angle a he bo om phase o di es was small (7±5 deg,
mean±s.d.). We acknowledge ha he eliabili y o his speed
es ima e dec eases a such low pi ch angles and ha we a e igno ing
wa e cu en s ha may a ec he speed o he animal o e he
g ound. Howe e , as we we e compa ing ela i e mo emen s ac oss
sca e ing ea u es, he e ec o cu en s may be negligible and
a ia ions in he absolu e alues may ha e li le impac on he
o e all conclusions.
Pe mi de ails
Expe imen s we e pe o med unde he US Na ional Ma ine
Fishe ies Se ice (NMFS; pe mi no. 14534-2), Channel Islands
Na ional Ma ine Sanc ua y (pe mi no. 2010-003) (B.L.S.,
p incipal in es iga o o bo h) and IACUC pe mi s issued o he
p ojec in es iga o s.
RESULTS
A o al o 9 h o synch onous p eda o and p ey da a, comp ising
sound and mo emen DTag eco dings om 37 di es pe o med by
wo dolphins and hyd oacous ic mapping o p ey wi hin hei
o aging a ea, we e analysed. Addi ional DTag da a om 26
G. g iseus agged in he same gene al a ea, amoun ing o 83.2 h o
da a and 174 di es, we e used o in es iga e p eda o sea ch
beha iou in ela ion o o aging a es. A di e was conside ed as
s a ing he i s ime he dolphins exceeded 20 m dep h a e a
su acing and ending a he nex su acing. Di es wi h one o mo e
buzzes, i.e. p ey cap u e a emp s (A anz e al., 2016), om he
agged dolphins, hence o h e e ed o as o aging di es, las ed o
1–10 min and con ained on a e age 5 ( ange: 1–11) buzzes.
Di e and p ey da a in eg a ion
Hyd oacous ic su eys concu en wi h ag da a e ealed a s ong
seg ega ion o biomass e ically in sca e ed pa ches 50–150 m
ac oss be ween 100 and 200 m dep h, and in h ee sound-sca e ing
laye s, each o which was ho izon ally con inuous (Fig. 2).
The h ee sca e ing laye s we e iden i ied as ollows: ‘shallow’
(30–90 m minimum and maximum dep hs o he laye bounda ies
a e aged o he wo da ase s, ounded o he nea es 10); ‘midwa e ’
(200–300 m, mig a ing e ically in 24 h cycles) and ‘deep’
3
RESEARCH ARTICLE Jou nal o Expe imen al Biology (2018) 221, jeb165209. doi:10.1242/jeb.165209
Jou nal o Expe imen al Biology
(350–450 m, no diu nal mig a ion). Al hough he e ical
dis ibu ion o hese laye s emained ela i ely cons an o e he
du a ion o he wo ag deploymen s, when moni o ed o e longe
ime scales, he p esence o he shallow laye a ied in an
unp edic able ashion when compa ed wi h he mo e eliable
midwa e and deep sca e ing laye s. In he ho izon al domain,
midwa e and deep laye s had a ubiqui ous dis ibu ion o e a scale
o ens o kilome es wi h a complex he e ogeneous inne s uc u e
composed o small-scale, disc e e agg ega ions o animals o simila
sizes and axonomic g oups app oxima ely 100 indi iduals ac oss,
and adjacen o agg ega ions o animals o a di e en size and/o
g oup (Benoi -Bi d e al., 2017). The sca e ed pa ches ound
be ween 100 and 200 m dep h ( axonomy and size o animal wi hin
unknown) ep esen ed only 5% o he wa e olume wi hin hese
dep hs and had a less p edic able occu ence han he pa ches ha
o med disc e e laye s a g ea e dep hs.
Di e ypes
Dolphins o aged in bou s o 7–11 di es co e ing a wide dep h
ange, wi h only 1–3 min spen a he su ace be ween di es wi hin
he same bou . The maximum dep h o di es a ied by 260 m ac oss
bou s and 120 m wi hin bou s (median o 3 di e bou s pe ag). The
maximum dep h o mos di es ell wi hin he bounda y o one o he
ou obse ed p ey ea u es (co esponding o ei he laye s o
sca e ed pa ches; Fig. 3). Di es we e classi ied in o ou di e ypes
based on he deepes sca e ing ea u e isi ed. O e all, dolphins
pe o med 57% o di es o no deepe han he shallow laye , 30% o
he sca e ed pa ches, 17% o he midwa e laye and 12% o he
deep laye (Fig. 3). Each di e was di ided in o h ee phases based on
he bounda y o p ey ea u es: (i) descen – he pe iod be ween when
he dolphin le he su ace and en e ed he deepes p ey laye isi ed
du ing he di e; (ii) ascen – he pe iod om when he dolphin le
he deepes p ey laye isi ed o when i eached he su ace; and (iii)
bo om – he pe iod be ween he end o he descen and s a o he
ascen , excep o shallow di es whe e he e was no descen o
ascen and he whole di e was conside ed a bo om phase. Mos
buzzes (112/181) occu ed du ing he bo om phase o di es;
o e all, 31% occu ed in he shallow laye , 21% in he sca e ed
pa ches, and 33% and 15% in he midwa e and deep laye s. These
p opo ions di e ed om he pe cen age o di es o each o hese
p ey ea u es. Di es ha eached he midwa e and deep laye s
egula ly ea u ed buzzes on he ascen , accoun ing o 30% o he
o al numbe o buzzes, mos o hem (66%) wi hin sca e ed
pa ches, wi h 26% and 7% in shallow and midwa e laye s,
espec i ely. The emaining 7% o buzzes (13/181) we e pe o med
on di e descen s, p ima ily in he shallow laye (N=6) and sca e ed
pa ches (N=6).
Ad anced selec ion o o aging laye
To explo e whe he dolphins planned o aging wi hin a speci ic
dep h ange be o e gaining new in o ma ion by sensing he
en i onmen in he cu en di e, we i s in es iga ed whe he
planning would cause animals o wai o s a clicking un il hey
swam close o he planned laye a he han nea he su ace.
500 11.5 12 12.5 13 13.5
12 13 15
Time local (h)
Dep h (m)
14 16 18
17
450
400
350
300
250
200
150
100
50
A
B
0
500
450
400
350
300
250
200
150
100
50
0
Shallow
Sca e ed pa ches
Midwa e
Deep
Shallow
Sca e ed pa ches
Midwa e
Deep
Fig. 3. Fo aging ac i i y o he dolphins and synch onous ime–dep h
dis ibu ion o p ey agg ega ions. The colou ed laye s ep esen , om
da ke o ligh e blue, he mean dep h, hi d qua ile and 95% con idence
in e al o each edge’s dep h laye in eg a ed ac oss he sampling a ea. The
di e p o ile (black) is shown wi h buzzes ( ed ci cles) ha indica e a emp s o
cap u e p ey o dolphin one (A) and wo (B).
500
–35
–45
–55
–65
–75
012
Dis ance (km)
Dep h
3
400
300
200
100
0
s (dB e. 1 m−1)
Fig. 2. Longi udinal sec ion o he acous ic backsca e olume o
Ca alina Island, CA, USA, showing ela i e dis ibu ion and composi ion
o p ey agg ega ions. The colou map o acous ic backsca e uses g ey o
ep esen low alues, blue o in e media e, and g een and ed o high alues.
F om shallow o deep wa e s, based on a ge s eng h measu emen s, he e
was a ai ly dilu e shallow laye o small nek on, a zone o sca e ed pa ches o
unknown composi ion, and midwa e and deep sound-sca e ing laye s
composed o o ganisms o la ge sizes.
4
RESEARCH ARTICLE Jou nal o Expe imen al Biology (2018) 221, jeb165209. doi:10.1242/jeb.165209
Jou nal o Expe imen al Biology
Pooling da a om wo dolphins, he mean dep h o he i s click in
di es was 23±13 m, indica ing ha he dolphins always s a ed
echoloca ing ea ly in di es, ega dless o how deep hey s a ed
o aging. Mo eo e , he dep h a which he i s click occu ed was
only weakly co ela ed o he mean dep h o he sca e ing ea u e in
which he i s o aging a emp o he di e was eco ded
(Spea man’sρ=0.27, P=0.11, N=33 di es). This sugges ed ha
e en when dolphins planned o o age a dep h, hey s ill s a ed
sampling in shallowe laye s.
Second, we in es iga ed whe he he inspec ion ange o he i s
clicks on descen co ela ed wi h he dep h o he i s o aging
a emp . The ini ial inspec ion ange occu ed o e a wide b ead h
(50–460 m) and showed a signi ican ly posi i e co ela ion wi h he
dep h o he u hes edge o he i s p ey laye whe e buzzes we e
eco ded (Spea man’sρ=0.64, P=0.0001, N=33 di es), consis en
wi h ou planning hypo hesis.
Sampling adjus ed o p ey ea u es
Based on he dis ibu ion o po en ial p ey, we p edic ed h ee ypes
o sea ch pa e ns each cha ac e ized by how he inspec ion ange
a ied o e he cou se o descen s. I a dolphin planned o o age in
a shallow laye o shallow sca e ed pa ches and ound he expec ed
p ey he e, hen we p edic ed a sho inspec ion ange ha would no
change as a unc ion o dep h. I dolphins planned o o age in a
shallow p ey ea u e bu encoun e ed ewe p ey o lowe quali y
p ey han expec ed, we p edic ed hey may swi ch hei a en ion o a
new, deepe p ey laye , esul ing om emembe ing he dep h o
o he p ey ea u es. A sudden inc ease in he inspec ion ange was
expec ed i such a decision was made, compa able o he ange o
he new expec ed p ey laye . Al e na i ely, i a dolphin was planning
a he beginning o a di e o o age on a medium o deep laye , we
p edic ed ha he inspec ion ange would s a a long anges and
educe g adually as he dolphin descended o ack he sca e ing
ea u e on which i planned o o age. To es his hypo hesis, we
i s ook he descen phase o indi idual di es as he uni o analysis
and, o each di e ype, assessed he co ela ion be ween he
maximum dep h sea ched by he dolphin and he dep h o he
deepes p ey laye isi ed. In shallow di es (N=12), dolphins
exhibi ed a ela i ely sho and cons an inspec ion ange o e he
di e (mean inspec ion ange be o e he i s buzz, 97±52 m). In 11
o he 12 shallow di es, he inspec ion ange in he pe iod om he
emission o he i s echoloca ion click and he i s buzz was no
associa ed wi h he dis ance o he u hes edge o he shallow
sca e ing laye (mean Spea man’sρ=0.1, P>0.05, N=12 di es).
Simila ly, in 7 o 8 di es a ge ing sca e ed pa ches, he dolphins
employed a ela i ely sho inspec ion ange (112±60 m) and he e
was no co ela ion wi h he dis ance o he u he edge o he dep h
ange o sca e ed pa ches (mean Spea man’sρ=0.03, P>0.05, N=8
di es; Fig. 4A). A e iew o midwa e and deep di es e ealed
wo dis inc i e pa e ns: one pa e n (Fig. 4B) sugges ed he
in en ion o di e o deepe dep hs om he ou se , while he o he
(Fig. 4C) was consis en wi h he dolphin ini ially planning a
shallow di e bu la e swi ching i s a en ion o a deepe laye .
Midwa e and deep di es wi h Spea man’sρ<0.5 (N=6) had an
ini ially sho inspec ion ange (140±90 m) and o en ea u ed
buzzes du ing he descen (1±1 buzz eco ded in 5 o 8 di es). In he
descen phase o hese di es, dolphins main ained a ela i ely
cons an and sho inspec ion ange, oughly equi alen o ha
obse ed in di es a ge ing he shallow laye and sca e ed pa ches,
un il he i s p ey cap u e a emp occu ed, usually be ween 100
and 200 m dep h (85% o he buzzes). Sho ly a e he buzz, he
dolphins inc eased hei inspec ion ange. This dis ance was
compa able o he ange o he laye ul ima ely a ge ed du ing he
di e and he inspec ion ange employed wi hin he same dep h ange
in di es in which laye acking was appa en (i.e. di es wi h s ong
co ela ions o ini ial inspec ion ange and dis ance o he u he
edge o he chosen p ey laye ) (Fig. 4C). In hese cases, he dolphins
ended up o aging a he bo om phase o he di e in a deepe laye .
This swi ch om sho o long sea ches du ing he descen and
subsequen deepe o aging was obse ed in 40% o he midwa e
and deep di es. In con as , in midwa e and deep di es wi h
Spea man’sρ>0.5 (N=8), he ini ial inspec ion ange was long
0
ABC
100
Sca e ed pa ches
Midwa e
Deep
200
Dep h (m)Inspec ion ange (m)
300
400
500
400
300
200
100
00123
Di e ime (min)
0246802468
0
100
200
300
400
500
400
300
200
100
0
0
100
200
300
400
500
400
300
200
100
0
Fig. 4. Examples o he sampling s a egies o he dolphins in ela ion o p ey laye s in h ee di e ypes. Uppe panel: di e p o ile wi h clicks (whi e) and
buzzes ( ed), and mean dep h o he bounda ies o he p ey laye a ge ed, (A) sca e ed pa ches, (B) midwa e and (C) deep laye s. Lowe panel:
dolphin inspec ion ange (black do s) aken om he in e -click in e al mul iplied by one/hal he speed o sound as a unc ion o di e ime. The g eya ea
ep esen s he bo om phase o he di e and he ed lines indica e buzzes. The co ela ion be ween inspec ion ange and ange o he deepe bounda y o he i s
p ey laye wi h o aging buzzes was assessed isually o exempli y di es wi h none (A), weak (C) and s ong (B) co ela ions. No e he buzz du ing he descen o
he deep di e (C) and associa ed changes in he inspec ion ange a e wa ds.
5
RESEARCH ARTICLE Jou nal o Expe imen al Biology (2018) 221, jeb165209. doi:10.1242/jeb.165209
Jou nal o Expe imen al Biology

(400±100 m) and g adually dec eased as hey app oached he o age
laye in a pa e n consis en wi h ini ially planning o o age in he
deep laye s. Dolphins did no p oduce buzzes du ing he descen o
hese di es.
Fo midwa e and deep di es in which dolphins swi ched hei
a en ion o a new p ey laye o e he cou se o he descen (i.e. di es
wi h buzzes du ing descen , N=5), we measu ed whe he dolphins
could ha e de ec ed he new expec ed laye based upon clicking
while a shallow dep hs o in sca e ed pa ches. The a e age
di e ence be ween he ange o he shallowes edge o he new
o aging laye and he maximum inspec ion dep h be o e he i s
buzz eco ded o e he descen was −348±108 m. This sugges ed
ha he dolphins we e sampling he new o aging laye be o e he
las buzz in shallowe laye s a he han simply elying on
in o ma ion om p e ious deep di es.
Sampling adjus ed o p ey pa ch
Once en e ing he o aging laye , dolphins adop ed a mean
inspec ion ange ha was simila o sca e ed pa ches (127±
15 m), midwa e (127±22 m) and deep di es (127±7 m) and ended
o dec ease in shallow di es (105±7 m). On a e age, his ange was
oughly simila o he ho izon al dis ance co e ed by he dolphins
while o aging in he laye (99±47 m). Bo h we e compa able o
he mean size, in he ho izon al dimension, o mono-speci ic
agg ega ions (Scalab in e al., 1996) con aining he la ges a ailable
p ey in each laye (113±34 m), sugges ing ha dolphins use
echoloca ion o selec p ey wi hin hese agg ega ions. As epo ed in
Benoi -Bi d e al. (2017), he a ge s eng h o indi idual p ey in
he shallow laye was signi ican ly lowe han ha in deepe
agg ega ions and shallow p ey we e gene ally in smalle
agg ega ions, which co ela es wi h he use o sho e inspec ion
anges by he dolphins.
Ascen sampling based on p ey expec a ions
Op imal o aging heo y p edic s ha b ea h-hold di e s would
maximize he ime spen o aging a dep h and minimize he ime
spen in ansi (Mo i, 1998). This led us o p esume ha dolphins
will o age o as long as possible in hei chosen o aging laye
and cease sea ching o p ey on he di e ascen once hey ha e le
he laye . Al e na i ely, dolphins may echoloca e all he way up o
o ien a ion, o because hey expec o gain om cap u ing
shallowe p ey du ing he ascen , o o gain new in o ma ion
abou p ey o planning he nex di e. To es hese hypo heses, we
examined he dep h o he las click in di es and he sampling
s a egy used by he dolphins on di e ascen s in ela ion o p ey
ea u es and buzz occu ences. Pooling da a om he wo dolphins
o which p ey da a we e a ailable, he mean dep h o he las click
in a di e was 37±36 m, indica ing hey echoloca ed almos all he
way up o he su ace, i espec i e o he ype o di e. Fu he mo e,
he buzz a es, i.e. numbe o buzzes pe minu e, du ing di e
ascen s we e up o six imes highe han hose du ing descen s
(signed- ank P=0.005, N=14 pai ed compa isons o buzz a e
du ing descen e sus ascen phases). Dolphins emi ed buzzes
du ing he ascen in 40% o di es. In hose di es, clicking con inued
a e he las buzz eco ded on he ascen . All midwa e and deep di es
wi h no buzz on ascen and one wi h buzz on ascen had buzzes on
descen (4 o 14 di es). A e age ascen du a ion was 58±31 and 76
±42 s o di es wi hou and wi h buzzes on he ascen , espec i ely,
whe eas bo om ime was educed om 158±61 o 110±50 s du ing
he same di es. To es whe he , on ascen , dolphins we e seeking
mo e e icien o aging in uppe laye s, we explo ed whe he he buzz
a e du ing he bo om phase was highe han ha du ing he ascen .
Buzz a es a he bo om phase we e wo imes highe han hose
du ing ascen (signed- ank P=3.2e−9, N=130 pai ed compa isons o
buzz a e du ing bo om e sus ascen phases), sugges ing ha
dolphins we e o aging mo e e icien ly a he bo om o he di e
compa ed wi h o aging on ascen .
Du ing ascen s o mos di es, an inspec ion ange consis en wi h
acking he nex p ey ea u e was obse ed, sugges ing he dolphins
ocused hei sea ch on expec ed shallowe sca e ing ea u es.
The e was only one deep di e (ou o 4) du ing which he dolphin
did no p oduce buzzes on he ascen and his was he only di e o
which he ini ial ascen inspec ion ange was adjus ed o a ange
consis en wi h acking he su ace. The i e buzzes eco ded a he
bo om phase o his di e we e compa able o he a e age numbe o
buzzes eco ded a he bo om phase o deep di es in which buzzes
on ascen we e also eco ded (3.5±1.5 buzzes). Fo midwa e di es,
we es ed whe he he dolphins we e mo e likely o swi ch o a
longe sea ch ange a he s a o ascen han while hey we e
sea ching o p ey wi hin he laye . Fo his es , we compa ed he
mean maximum inspec ion ange o he las h ee clicks eco ded a
he bo om phase (177±86 m) wi h he i s h ee clicks o he ascen
phase (366±160 m). The same a iables measu ed in deep di es
we e 198±44 and 370±244 m, espec i ely. Bo h in midwa e and in
deep di es, he e was a s ong co ela ion be ween he e ical
inspec ion ange measu ed om he i s h ee clicks o he dolphins
emi ed on he ascen and he dep h di e ence be ween he dolphin
and he shallowe edge o he nex shallowe laye whe e buzzes
we e eco ded (Spea man’sρ=0.66, P=0.01, N=14 di es). The
absolu e di e ence be ween hese wo a iables was small (16±14
and 17±11 m in midwa e and deep di es, espec i ely), suppo ing
he hypo hesis ha dolphins we e sampling p ey a a pa icula
dep h, on hei way up o he su ace.
To explo e whe he dolphins sensed p ey loca ed abo e hem
du ing he bo om phase o he di e o emembe ed hei loca ion
om be o e ha phase, we es ed whe he he e ical inspec ion
ange o long- ange clicks (i.e. es ima ed inspec ion ange >200 m)
eco ded o e he bo om phase o he di e ma ched he dep h
di e ence be ween he dolphin, when emi ing he click, and he
shallowe edge o he nex shallowe laye whe e buzzes we e
eco ded on ascen . The a e age absolu e di e ence be ween he
wo a iables was 5±78 m in midwa e di es and 40±85 m in deep
di es, sugges ing ha dolphins could sense shallowe p ey ea u es
loca ed abo e hem while a he bo om o he di es.
P ey-dependen planning
To es whe he dolphins plan he laye in which o o age based on
pe cei ed p ey p o i abili y in he p e ious di e, we looked a he
ela ionship be ween he buzz a e a he bo om phase o he
p e ious di e and he ini ial inspec ion ange in he nex di e,
pooling da a o 28 dolphins. I a p e ious di e sugges ed he bes
pa ches we e shallow, and he animal used his in o ma ion o plan
he nex di e, hen we expec ed ha i would s a sampling a a sho
ange. In con as , i pas expe iences indica ed ha shallow pa ches
we e o low p o i , we expec ed he animal would s a sea ching a a
longe ange. The esul s suppo ed his hypo hesis; a e shallow
di es when buzz a es we e mode a e o high (>3 buzzes min
−1
),
dolphins s a ed sampling a a sho ange (169±158 m) du ing he
nex di e (Fig. 5). A e shallow di es wi h low buzz a es
(<3 buzzes min
−1
), dolphins, on a e age, chose o sample a longe
anges du ing he nex di e (249±204 m). A e e se pa e n was
obse ed a e deep di es: when buzz a es we e mode a e o high
(>3 buzzes min
−1
), dolphins s a ed sampling a a long ange
(414±157 m) du ing he nex di e (Fig. 5); when buzz a es we e
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Jou nal o Expe imen al Biology
low (<3 buzzes min
−1
), dolphins sampled a sho e anges (181
±110 m) in he nex di e, consis en wi h dolphins using
in o ma ion on p ey om a p e ious di e o plan he o aging
dep h in he nex one.
DISCUSSION
Each ime an ai -b ea hing aqua ic animal di es o o age, i mus
make decisions o adjus i s physiology o di e en leng hs and
dep hs o di es. In en i onmen s wi h epheme al pa ches o p ey a
close shallow anges and p edic able esou ces a mo e cos ly deepe
anges, he animal may bene i om using in o ma ion om
p e ious di es o plan he nex o aging di e. Ye , we a ely can
ob ain e idence o how an indi idual’s decisions a e a ec ed by
p io knowledge and modula ed by compa isons o eal- ime
in o ma ion and balancing a ailable al e na i es, and his has
na owed p og ess in s udies o animal planning and decision
making unde na u al se ings.
Echoloca ing di e s a e a good axon o use o add ess hese
ques ions because hey p o ide us wi h in o ma ion on hei sea ch
anges (i.e. wha in o ma ion is a ailable in o de o make a
decision) and when and whe e p ey cap u e a emp s occu
(i.e. ac ual choices). In eg a ion o his in o ma ion wi h
con empo aneous ine-scale da a om he p ey ields, sampled a
he same dep hs and imes whe e he p eda o s occu , p o ides a
unique pe spec i e on he choices a ailable o a p eda o in a h ee-
dimensional ma ine sys em. He e, we shed ligh on how p eda o s
adjus hei sea ch based upon sensing he cu en dis ibu ion o
p ey o using in o ma ion ga he ed in p e ious di es o om ea lie
phases o he same di e. These p ocesses we e iewed om sub-
mesoscales (i.e. how hey plan and choose o o age on di e en
p ey agg ega ions) o mic oscales (i.e. how hey adjus hei acous ic
gaze o sea ch wi hin a pa ch).
The dolphins explo ed hei en i onmen based on pas
expe iences o in o m upcoming o aging decisions o di e- ime
alloca ion and p ey choice. They used a long inspec ion ange o
di es when hey we e planning o o age in he s able deep pa ches,
and swi ched o a sho inspec ion ange once hey loca ed a pa ch in
which o o age. Once his decision was made, he inspec ion ange
emained oughly cons an and compa able o he scale o p ey
pa ches con aining he la ges p ey, sugges ing ha inspec ion ange
was adjus ed o selec p ey wi hin he expec ed size o p ey pa ches.
When dolphins pe o med well in one pa ch, as judged by high buzz
a es, hey planned o a ge he same laye in he nex di e. Obse ed
di e ences in maximum di e dep h o di es wi hin bou s we e
p obably d i en by a ia ions in p ey selec ion by he dolphins on a
di e-by-di e basis. The e was an appa en misma ch be ween he
p opo ion o di es and buzzes pe o med wi hin each p ey laye , as
judged by he g adual dec ease in he pe cen age o di es pe o med
pe p ey ea u e agains he mo e Gaussian dis ibu ion o buzz
coun s. This may be because he la e is ela ed o he ela i e cap u e
a e in each laye , whe eas he o me may be d i en by ene ge ic
cos s o di ing o di e en dep hs. La ge deep-di ing odon oce es,
such as spe m o beaked whales, emi be ween 3 and 5 imes mo e
buzzes han G. g iseus a he bo om phase o di es (A anz e al.,
2011; Wa wood e al., 2006; his s udy). This appa en , highe
o aging e iciency o la ge species p obably e lec s di e ences in
o aging equi emen s as well as hei g ea e di ing capaci y and
lowe cos o anspo (Williams e al., 1999). G ampus g iseus a e
small- o medium-sized delphinids o which ex ending he ime
o aging a dep h o compensa e o long ansi imes (Thompson and
Fedak, 2001) may be limi ed by he a ailable oxygen s o es.
Animals conside ing po en ial p ey al e na i es wi h a iable
bene i s as well as a iable cos s o locomo ion o a el o hese
pa ches may need o ack he en i onmen ela i ely closely o
0
0
250
500
246 02
Buzz a e (p e ious di e) (buzzes min–1)
Ini ial inspec ion ange
(cu en di e) (m)
46 024602 46
Sca e ed pa ches Midwa e Deep
Shallow
Fig. 5. Ini ial inspec ion ange adap ed o he bes o aging dep h encoun e ed on he p e ious di e, om 174 di es by 28 dolphins. (A) Illus a ion o an
indi idual’s o aging scena io showing buzzes ( ed s a s) emi ed in he p e ious di e in a gi en p ey ea u e and he inspec ion ange a he s a o cu en di e.
(B) Ini ial inspec ion ange o he cu en di e (y-axis) as a unc ion o buzz a e in he las di e (x-axis). No e he endency o he dolphin o a ge he dep h laye
whe e i had he highes buzz a e on he p e ious di e. Di e ypes a e classi ied using he dep h dis ibu ion o p ey ea u es desc ibed in Fig. 1.
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Jou nal o Expe imen al Biology
upda e exis ing in o ma ion in o de o espond quickly o sho -
e m changes in cos and bene i (Dunlap and S ephens, 2012; Mo i,
1998). He e, in con as o o he deep-di ing odon oce es
(A anz e al., 2011; Wa wood e al., 2006), he dolphins s a ed
echoloca ing ea ly and h oughou he di es, p obably o gain
in o ma ion on he dep h dis ibu ion and a ailabili y o p ey and o
espond swi ly o apid changes in habi a s uc u e a di e en
dep hs. We ound e idence ha dolphins upda ed hei o aging
plans based on in o ma ion abou p ey ga he ed du ing he di e,
sugges ing ha animals we e e isi ing plans egula ly, compa ing
al e na i es based on memo y wi h hose based on cu en
assessmen o esou ce dis ibu ion ia senso y in o ma ion
acqui ed om sampling h oughou he di e. Be o e ascen ,
dolphins planned when o o age on he way up and when no o,
as e idenced by hei inspec ion ange a he s a o he ascen .
Sampling du ing descen s o o aging dep hs may guide ini ial
decisions abou which p ey ea u es o sample on ascen , as
demons a ed by he jump in he inspec ion ange when dolphins
decided o lea e he bo om o aging laye . S ikingly, when
dolphins a emp ed o ca ch p ey (demons a ed by he p oduc ion o
buzzes) on descen , hey did no p oduce buzzes on ascen , pe haps
because he inc eased ime on descen in e e ed wi h oppo uni ies
o o age on ascen , gi en he ime cons ain s imposed by b ea h-
hold di ing. Dolphins a imes slowed down hei ascen , aking
20% longe in o de o sea ch o and cap u e p ey in shallowe
laye s. These esul s sugges ha while dolphins may sample p ey on
descen , hey make a decision abou whe he o sho en o aging a
he bo om o o age on ascen based upon in o ma ion abou p ey
and oxygen a ailabili y. The endency o dolphins o o age on
ascen e sus descen may esul om he s abili y o p ey pa ches
and he abili y o an indi idual o aging in he bo om laye o weigh
he bene i s los by b eaking o om o aging a he bo om o
o age on ascen .
Fo aging on ascen con adic s mos o aging heo ies, which
emphasize minimizing he ime in di e ansi s o and om o aging
dep hs o ex end bo om ime and he e o e he p obabili y o inding
p ey (Mo i, 1998; Thompson and Fedak, 2001). Mos di ing
mammals s udied o da e, including spe m, beaked, blue and
humpback whales, do no show o aging ac i i y on he di e ascen
(A anz e al., 2011; Wa wood e al., 2006; Hazen e al., 2015;
Doniol-Valc oze e al., 2011). Mo eo e , mos deep-di ing
echoloca ing species s op clicking ea ly in he ascen . Howe e ,
he e is conside able selec ion p essu e o sea ch s a egies ha
inc ease he encoun e a e wi h ood and he e o e hei o aging
e iciency (Cowie, 1977; F iedlaende e al., 2016; Ydenbe g and
Hu d, 1998). Spe m whales o aging in high-la i ude habi a s ha e
been obse ed sea ching o and cap u ing p ey on di e ascen s
(Fais e al., 2015), as he Risso’s dolphins did in his s udy. This
sugges s ha such a s a egy migh ep esen an adap i e beha iou
o ai -b ea hing p eda o s in mul i-laye ed habi a s con aining bo h
shallow- and deep-wa e p ey o a iable p edic abili y.
In his pape , we ha e shown ha a he s a o a o aging di e,
dolphins selec ed an echoloca ion ange ha a ge ed he bes
o aging dep h encoun e ed on he las di e. This can be in e p e ed
as dolphins ecalling in o ma ion om he p e ious di e o plan he
nex o aging di e (i.e. episodic-like memo y). Al e na i ely, one
can a gue ha ha ing spa ial memo y abili ies is su icien o allow
such beha iou (i.e. seman ic knowledge). Howe e , u he
con incing e idence o planning comes om si ua ions in which
an animal beha es in a way ha igno es i s cu en mo i a ional s a e
in o de o mee a need o an expec ed u u e mo i a ional s a e
(Naqshbandi and Robe s, 2006). He e, we ound ha dolphins emi
clicks h oughou hei ascen o he su ace a e eeding a he
bo om laye , when he dolphins ha e lowe mo i a ion o eed and
highe mo i a ion o b ea he. The unc ion o his beha iou appea s
o be o sample p ey a di e en laye s in an icipa ion o hei u u e
di e in o de o upda e hei knowledge on p ey dis ibu ion,
suppo ing he lexible deploymen o in o ma ion in no el
si ua ions (Clay on e al., 2003). In his si ua ion, he dolphins
appea ed o igno e hei mo e u gen mo i a ion o b ea he in o de
o imp o e hei o aging on he nex di e, by po en ially modi ying
hei sea ch s a egy; howe e , a e b ea hing, hei p ima y
mo i a ion again became o o age.
The da a p esen ed he e on he spa ial dis ibu ion o p ey and
du a ions o e which dis ibu ion was s able, coupled wi h ou da a
on how b ea h-hold di e s make use o senso y in o ma ion o make
o aging decisions, p o ide unique insigh in o how hese animals
plan dynamically, wi h a balance o s a egy and lexibili y, o cope
wi h a ying p edic abili y in he dis ibu ion o hei ood.
Acknowledgemen s
The au ho s hank he SOCAL-BRS pa icipan s, pa icula ly ag ope a o s Alison
S impe and Ann Allen, o hei assis ance in he ield. We also g a e ully
acknowledge ChloeYzoa d o dolphin illus a ions and one anonymous e iewe o
cons uc i e c i icism on he manusc ip .
Compe ing in e es s
The au ho s decla e no compe ing o inancial in e es s.
Au ho con ibu ions
Concep ualiza ion: P.A., K.J.B., B.L.S., P.L.T.; Me hodology: K.J.B., B.L.S.;
So wa e: K.J.B.; Valida ion: P.L.T.; Fo mal analysis: P.A., K.J.B.; In es iga ion: P.A.,
K.J.B., J.C., A.S.F.; Resou ces: J.C., A.S.F.; Da a cu a ion: P.A., K.J.B.; W i ing -
o iginal d a : P.A.; W i ing - e iew & edi ing: P.A., K.J.B., B.L.S., J.C., A.S.F., P.L.T.;
Supe ision: P.L.T.; P ojec adminis a ion: B.L.S., J.C., P.L.T.; Funding acquisi ion:
K.J.B., B.L.S., J.C., P.L.T.
Funding
Funding o he SOCAL-BRS p ojec was p o ided by he Chie o Na al Ope a ions
En i onmen al Readiness Di ision, he U.S. Na y’s Li ing Ma ine Resou ces
P og am, and he O ice o Na al Resea ch Ma ine Mammal P og am. The S a egic
En i onmen al Resea ch and De elopmen P og am ia a U.S. A my Co ps o
Enginee s Con ac (K.J.B. and B.L.S.) p o ided unding o da a collec ion and p ey
analysis. This s udy was suppo ed by he MASTS pooling ini ia i e (Ma ine Alliance
o Science and Technology o Sco land). MASTS is unded by he Sco ish Funding
Council (g an e e ence HR09011) and con ibu ing ins i u ions.
Da a a ailabili y
Da a a e a ailable om he D yad Digi al Reposi o y (A anz e al., 2017): h p://
doi:10.5061/d yad.48 q4
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