Endemic fish calling: Acoustics and reproductive behaviour of the Neretva dwarf goby Orsinigobius croaticus
Abstract
The Neretva dwarf goby Orsinigobius croaticus (Gobiiformes, Gobionellidae) is an en -demic fish native to the freshwaters of the Adriatic Basin in Croatia and Bosnia and Herzegovina, a Mediterranean Biodiversity Hotspot. Due to its limited distribution range, specific karst habitat and endangered status, laboratory studies on reproduc-tive biology are scarce but crucial. Herein, we investigated the sound production and acoustic behaviour of the endangered O. croaticus during reproductive intersexual laboratory encounters, utilising an interdisciplinary approach. We also performed dis -sections and micro-computed tomography (μCT) scanning of the pectoral girdle to explore its potential involvement in sound production. Finally, comparative acousticanalysis was conducted on sounds produced by previously recorded soniferous sand gobies to investigate whether acoustic features are species-specific. The endemic O. croaticus is a soniferous species. Males of this species emit pulsatile sounds com -posed of a variable number of short (~15 ms) consecutive pulses when interacting with females, usually during the pre-spawning phase in the nest, but also during courtshipoutside the nest. Pulsatile sounds were low-frequency and short pulse trains (~140 Hz, <1000 ms). Male visual behaviour rate was higher when co-occurring with sounds and females entered the male's nest significantly more frequently when sounds were present. Characteristic body movements accompanied male sound production, such as head thrust and fin spreading. Furthermore, μCT scans and dissections suggest that O. croaticus shares certain anatomical similarities of the pectoral girdle (i.e. osseous elements and arrangement of levator pectoralis muscles) to previously studied sand gobies that could be involved in sound production. Multivariate comparisons, using sounds produced by eight soniferous European sand gobies, effectively distinguished soniferous (and sympatric) species based on their acoustic properties. However, the discrimination success decreased when temperature-dependent features (sound duration and pulse repetition rate) were excluded from the analysis. Therefore, we suggest both spectral and temporal features are important for the acoustic differen-tiation of sand gobies.
Full text
Ecology and E olu ion. 2023;13:e10673.
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1 o 18
h ps://doi.o g/10.1002/ece3.10673
www.ecole ol.o g
Recei ed:15May2023
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Re ised:27Sep embe 2023
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Accep ed:16Oc obe 2023
DOI:10.1002/ece3.10673
RESEARCH ARTICLE
Endemic ish calling: Acous ics and ep oduc i e beha iou o
he Ne e a dwa goby O sinigobius c oa icus
S enHo a ić1 | E ic Pa men ie 2 | S e ano Mala asi3 | Ma ia P. Cla a Amo im4 |
Paulo J. Fonseca5 | Da o Zanella1
Thisisanopenaccessa icleunde he e mso heC ea i eCommonsA ibu ionLicense,whichpe mi suse,dis ibu ionand ep oduc ioninanymedium,
p o ided he o iginal wo k is p ope ly ci ed.
©2023TheAu ho s.Ecology and E olu ionpublishedbyJohnWiley&SonsL d.
1Depa men o Zoology,Facul yo
Science,Uni e si yo Zag eb,Zag eb,
C oa ia
2Labo a o yo Func ionaland
E olu iona yMo phology,FOCUS,
Uni e si yo Liège,Liège,Belgium
3Depa men o En i onmen alSciences,
In o ma icsandS a is ics,CàFosca i,
Uni e si yo Venice,VeneziaMes e,I aly
4Depa amen odeBiologiaAnimaland
MARE–Ma ineandEn i onmen al
SciencesCen e/ARNET-Aqua ic
Resea chNe wo k,FaculdadedeCiências,
Uni e sidadedeLisboa,Lisbon,Po ugal
5Depa amen odeBiologiaAnimaland
cE3c-Cen e o Ecology,E olu ionand
En i onmen alChanges,Faculdadede
Ciências,Uni e sidadedeLisboa,Lisbon,
Po ugal
Co espondence
Da o Zanella,Depa men o Zoology,
Facul yo Science,Uni e si yo Zag eb,
Zag eb,C oa ia.
Email:da o [email p o ec ed].h
Funding in o ma ion
Minis yo Ag icul u e,Republico
C oa ia
Abs ac
TheNe e adwa gobyO sinigobius c oa icus(Gobii o mes,Gobionellidae)isanen-
demic ishna i e o he eshwa e so heAd ia icBasininC oa iaandBosniaand
He zego ina,aMedi e aneanBiodi e si yHo spo .Due oi slimi eddis ibu ion
ange,speci icka s habi a andendange eds a us,labo a o ys udieson ep oduc-
i ebiologya esca cebu c ucial.He ein,wein es iga ed hesoundp oduc ionand
acous icbeha iou o heendange edO. c oa icus du ing ep oduc i e in e sexual
labo a o yencoun e s,u ilisinganin e disciplina yapp oach.Wealsope o meddis-
sec ionsandmic o-compu ed omog aphy(μCT)scanningo hepec o algi dle o
explo ei spo en ialin ol emen insoundp oduc ion.Finally,compa a i eacous ic
analysiswasconduc edonsoundsp oducedbyp e iously eco dedsoni e oussand
gobies o in es iga e whe he acous ic ea u es a e species-speci ic. The endemic
O. c oa icusisasoni e ousspecies.Maleso hisspeciesemi pulsa ilesoundscom-
posedo a a iablenumbe o sho (~15 ms)consecu i epulseswhenin e ac ingwi h
emales,usuallydu ing hep e-spawningphasein henes ,bu alsodu ingcou ship
ou side henes .Pulsa ilesoundswe elow- equencyandsho pulse ains(~140 Hz,
<1000 ms).Male isualbeha iou a ewashighe whenco-occu ing wi hsounds
and emalesen e ed hemale'snes signi ican lymo e equen lywhensoundswe e
p esen .Cha ac e is icbodymo emen saccompaniedmalesoundp oduc ion,such
ashead h us and insp eading.Fu he mo e,μCT scans and dissec ions sugges ha
O. c oa icussha esce ainana omicalsimila i ieso hepec o algi dle(i.e.osseous
elemen sanda angemen o le a o pec o alismuscles) op e iouslys udiedsand
gobies ha couldbein ol edinsoundp oduc ion.Mul i a ia ecompa isons,using
soundsp oducedbyeigh soni e ousEu opeansandgobies,e ec i elydis inguished
soni e ous(andsympa ic)speciesbasedon hei acous icp ope ies.Howe e , he
disc imina ion success dec eased when empe a u e-dependen ea u es (sound
du a ionandpulse epe i ion a e)we eexcluded om heanalysis.The e o e,we
sugges bo hspec aland empo al ea u esa eimpo an o heacous icdi e en-
ia iono sandgobies.
2o 18
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HORVATIĆ e al.
1 | INTRODUCTION
The Medi e anean Biodi e si y Ho spo (MBH) is a widely e-
nowned egion o i ssigni ican en i onmen aldi e si yandendan-
ge edwildli e(Da walle al.,2014; Mye s e al., 2000).The i e so
heAd ia icSeaBasininC oa iaa epa o heMBHandDalma ian
eshwa e eco egions (Abell e al., 2008), and a e especially ich
in eshwa e endemic ish,wi h40specieso almos 30%o he
o alC oa ianich hyo auna,endemic o hisa ea(Ćale ae al.,2015,
2019;Ko ela &F eyho ,2007; Mye s e al., 2000).Thisendemism
isa ea u eo hehabi a so heDina icka s ha co e s oughly
54% o C oa ian e i o y, wi h he p esence o nume ous ca es,
sinkholes, cold seasonal wells, and unde g ound i e s (Ku le, 1999;
M ako čiće al.,2006).
Among hese endemic ish species, O sinigobius c oa icus
(M ako čiće al.,1996), o me lydesc ibedasKnipowi schia c o-
a ica, is a small ben hic and sho -li ed (less han 2 yea s) sand
gobycon ined o heDina icka s o heDalma ianeco egion.I
canbe oundexclusi elyin he eshwa e so C oa iaandBosnia
andHe zego ina(Abelle al.,2008;Ćale ae al.,2019;Ho a ić
e al., 2017;Tu mane al.,2020;Zanellae al.,2011).InC oa ia,
hisspeciesinhabi s heEas e npa o heAd ia icBasinandhas
ana u ally agmen eddis ibu ion ange ha includes heNe e a
Ri e ,Ma icaRi e , heV go ačkoPoljeandRas očkoPolje ields
andBaćinaLakes,someo whicha eNATURA2000si es(Ćale a
e al., 2015; M ako čić e al., 1996; Zanella e al., 2011, 2017;
seeHo a iće al.,2017 o hemapwi hi sdis ibu iona ea).
In i s na u al habi a , O. c oa icus occupiessandybo oms wi h
occasional s ones/pebbles in ka s i e s, slow- lowing s eams
andoligo ophiclakes(Ho a iće al.,2017;Zanellae al.,2011).
Du ing win e and ea ly sp ing, O. c oa icus h i esinsmall i e s
ands eamswhe easdu ing hesumme pe iod, hisgobysu i es
insmallka s unde g oundpondsand e uges,when hewa e -
cou sescomple elyd you (Mille ,2004;M ako čiće al.,2006).
On heIUCNRedLis ,O. c oa icusisassessedgloballyas ulne a-
ble(VU,B2ab(iii);D2, e .3.1.),bu egionallyasendange ed(EN)
due oi shighlylimi ed/ agmen edhabi a anddeclininghabi a
quali y(C i elli,2018;Ho a iće al.,2017;M ako čiće al.,2006).
Howe e , hisendange eds a usisalsodue oalacko knowledge
ega dingi sbiological ai s.The eisli lepublishedda aon he
ecologyo biologyo O. c oa icus(Ho a iće al.,2017;M ako čić
e al., 2006;Zanella e al.,2011, 2017). Likeo he sandgobies,
O. c oa icusisapolygamousmul iplespawne species ha achie es
sexual ma u i y qui e ea ly (i.e. wi hin i s i s yea ), and ep o-
duces omMa ch oNo embe ,al houghmos spawningoccu s
om Ap il o Sep embe (Ko ela & F eyho , 2007; Mazzoldi &
Rasso o, 2001;Zanellae al.,2011, 2017).
The sand gobies a e a monophyle ic gobii o m g oup
(Gobionellidae, Gobii o mes) o abou 30 species in he gen-
e a Knipowi schia, Poma oschis us, Economidich hys, Ninnigobius
and O sinigobius (Be ancu -R e al., 2017; Nelson e al., 2016;
Thacke , 2009; Thacke e al., 2019; Touga d e al., 2021).They
inhabi in e idalma ineandcoas al eshwa e ecosys emswi h
muddy- o-pebblebo omac ossEu ope,including hewa e so
heMedi e anean,Pon o-CaspianandNo heas A lan ic egions
(F eyho , 2011;Ko ačić&Pa zne ,2011; Mille , 2004;Šanda&
Ko ačić,2009).Recen phylogene ics udies ounde idence ha
sound p oduc ion is widesp ead among ac inop e ygian ishes,
sugges ing ha acous icbeha iou e ol edindependen lymul-
iple imes inun ela ed cladesand ha he eis a s ong selec-
ion o heuseo soundp oduc ionasabeha iou al ai ac oss
e eb a ee olu ion(Fine&Pa men ie ,2015; Rice e al., 2020,
2022).Communica i esoundemissionin ishisusuallylinked o
cou shipandspawningo agg essi ebeha iou (Amo im,2006;
Mann e al., 2008;My be gJ .&Lugli,2006).In ishbioacous ics,
acous ic signals associa ed wi h ep oduc i e in e sexual in e -
ac ionsha ebeen hemos commonlys udied ypeso sounds
(Amo im,2006),sincei isbelie ed ha hesesoundsse e oa -
ac po en ialma es(Long iee al.,2013;Pa men ie e al.,2010),
osynch onisespawningac i i iesa agg ega ionsi es(E isman&
Rowell, 2017;Jublie e al.,2019;Lobel,1992; Rowell e al., 2015)
o o synch onise game e elease by conspeci ics (Hawkins &
Amo im,2000;Lobel,2002).Sandgobiesa eacommonmodel
g oup among soni e ous ac inop e ygian ishes o sound p o-
duc ionandha elongbeenu ilisedine hologicalandcompa -
a i e bioacous ics s udies. The acous ic abili ies o sand gobies
ha e been in ensi ely in es iga ed in he las 30 yea s, espe-
ciallyin hespecieso hegene aPoma oschis us, Knipowi schia
and O sinigobius(Amo im&Ne es,2007;Blome al.,2016; Lugli
e al., 1997; Mala asi e al., 2008, 2009;Pa men ie e al.,2017;
To icelli e al., 1990;Zeyle al.,2016).Ineigh sandgobyspecies,
ei he pulsa ileo humpsounds(andsome imesbo h)ha ebeen
eco ded oda e(Amo im&Ne es,2007;Blome al.,2016; de
Jonge al.,2016;Zeyle al.,2016),whileinEconomidich hys pyg-
maeus(Holly,1929)soundswe eno de ec eddu ingbeha iou al
expe imen s (Gkenas e al., 2010). Mos o ou unde s anding
ega ding he acous ic abili ies o Medi e anean sand gobies
s ems om hecommon,widelydis ibu edandnon- h ea ened
speciesassigned o heleas conce n(LC;IUCNRedLis )ca e-
go y(Amo ime al.,2013;Blome al.,2016;deJonge al.,2016;
KEYWORDS
ana omicalanalysis,mic o-compu ed omog aphy, ep oduc i ee hology,soundanalysis
TAXONOMYCLASSIFICATION
Biodi e si yecology,Ecosys emecology,E olu iona yecology,Li ehis o yecology,
Popula ionecology,Socioecology
20457758, 2023, 11, Downloaded om h ps://onlinelib a y.wiley.com/doi/10.1002/ece3.10673 by Coch ane Po ugal, Wiley Online Lib a y on [24/11/2023]. See he Te ms and Condi ions (h ps://onlinelib a y.wiley.com/ e ms-and-condi ions) on Wiley Online Lib a y o ules o use; OA a icles a e go e ned by he applicable C ea i e Commons License
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3o 18
HORVATIĆ e al.
Zeyl e al., 2016). Howe e , since O. c oa icus was egionally
classi ied as a ulne able species wi h a e y es ic ed dis i-
bu ion(C i elli,2006,2018;Ho a iće al.,2017), his esea ch
is he i s s udy o he acous ic communica ionin endange ed
Medi e aneansandgoby.
The main goal o his s udy was o in es iga e he acous ic
communica iono O. c oa icus using an in e disciplina y app oach.
Speci ically,ou aimswe e o:(i)in es iga e hesoundp oduc iono
cap i e O. c oa icusmalesandquan i yacous icpa ame e so he
sounds;(ii)examine he ep oduc i ebeha iou o soni e ousmales
andi sassocia ion osoundp oduc ion;(iii)p o ideinsigh in o he
pu a i esound-p oducingmechanismbyexplo ing heana omyo
he pec o al gi dle and (i ) explo e he acous ic di e si ica ion o
soni e oussandgobiesbyquan i a i elycompa ingacous icsignals
be ween hes udyspeciesandp e iously eco dedMedi e anean
sandgobies(gene aNinnigobius, Poma oschis us, Knipowi schia and
O sinigobius).
2 | MATERIALSANDMETHODS
2.1 | Fishsampling,labo a o yhousingand
expe imen al design
O sinigobius c oa icuswascaugh usingelec o ishing(HansG assl,
model:EL65IIGI,powe :13 kW) omaboa du ing hesp ing2019.
Samplingwaspe o medon heMa icaRi e inC oa ia(nea he
illage Vina 43°10′30.33″ N, 17°23′12.36″ E). Di ec cu en was
useddu ingsamplingp ocedu essincei causesgal ano axiso an
a ac ionzonewhe e ishac i elyswim owa d heanode,andis
ypically less ha m ul. All ish displaying elec o- ac ic mo emen
owa ds he anode o pa alysis we e sampled using dip ne s. In
o al,wecollec ed25indi iduals(15malesand10 emales) om
hemain i e channela adep ho 0.5–2 m.Fishwe e ans e ed
ali e ola geplas icwa e con aine sequippedwi hae a o sand
anspo ed o helabo a o ya heFacul yo Science,Uni e si y
o Zag eb.A helabo a o y, ishwe esexedbasedonu ogeni al
papillaandbodycolou a ion(Mille ,1986)andhousedin ou sin-
gle-sexcommuni y ec angula anks(120 L; i e emalespe ank;
eigh malespe ank;Figu e S1).Eachcommuni y ankwasequipped
wi h 2–4 nes s. A e an acclima isa ion pe iod o 5–8 days, p o-
spec i esoni e ousmaleswe echosen o subsequen labo a o y
acous ic- isual eco dingsbasedoncolou a ion (comple eo pa -
iallyda kenbody, insandhead;Zanellae al.,2011)and e i o-
iali y. Eigh males (
x
± SD = 49.21 ± 0.8 mm o al leng h, LT; ange:
48.07–50.06 mm;
x
± SD = 41.07 ± 1.01 mm s anda d leng h, LS;
ange: 38.96–42.29 mm;
x
± SD = 1.24 ± 0.11 g weigh , W; ange:
1.10–1.40 g) exhibi ing ypical ep oduc i e beha iou we e cho-
sen o heexpe imen s.Females(N = 5;36.75 ± 5.10 mmLS; ange:
28.75–41.27 mm)we echosen o he eco dingsessionsacco ding
oyellowbellycolou a ion,luminescen g eenspo on he i s do -
sal inandda keyes,allindica o so emale eadiness o spawning
(Blome al.,2016;Zanellae al.,2011).
We ollowed heacous ic- isual eco dingp o ocoles ablished
byp e iousau ho s(Amo ime al.,2013;Amo im&Ne es,2007;
Ped osoe al.,2013),whe eexpe imen al anks,placedon opo
3 cm hick ubbe oamshockabso be s o educesubs a e-bo n
noise,we edi idedin o h eecompa men ssepa a edby emo -
ablepa i ions(Figu e S1). Each la e al compa men housed one
e i o ial male wi h a nes (a i icial unnel-shaped plas ic co e ,
dimensions:leng h = 100 mm,wid h = 60 mm,heigh = 50 mm),while
hemiddlesec ion(‘a ena’)wasoccupiedbya ipe emale.The e-
malecompa men wasno p o idedwi hanes .Theeigh males
we e di idedin o sepa a ela e al compa men s,whe e hey e-
mained h oughou heexpe imen s.Expe imen al ishwe ekep
a na u alpho ope iodand eddailyadlibi umwi hDaphnia.Wa e
empe a u e,moni o edwi ha he mome e (Aqua e a)andman-
ually egula edwi hahea e (Myli ell),wasmain ainedbe ween18
and22°C(na u al ange).The ankshada5 cm hicklaye o ine
sando g a elandeachmaleineachsec ionwasp o idedwi ha
wa e pumpsys emandae a ion.
Theexpe imen swe epe o med ommid-Ap il oOc obe ,a
andom imes.The ep oduc i ebeha iou o esiden maleswas
elici edbyin oducingone ipe emalein o he‘a ena’.Be o e i-
als,each emalewasle 12–24 hin heexpe imen al ank o ac-
clima isa ion.P io o eco dings(app ox.15 min),elec ici y,wa e
pumpsandae a ionwe eswi chedo ominimiseambien noise.
To u he educeunwan ednoise om he oomligh sys em, he
ceilingligh wasswi chedo and heexpe imen al ankwasillumi-
na edbyLEDligh om hesideo heaqua ium.Thisp ocedu e
hadnono iceablee ec son ishbeha iou .Themale– emale ials
las edapp oxima ely30 minandbeganby emo ingoneo hela -
e alpa i ions,allowingin e sexualin e ac ion.No e ha he wo
la e alpa i ionswe ene e emo eda hesame ime,and he e-
malealwaysin e ac edwi honlyonemale om hesame ank(i.e.
womales om hesame ankwe eusedinsepa a e ials).Be ween
consecu i e eco ding sessions 15–30 min pauses we e included,
wi hall hede ices u nedo .Theeigh e i o ialmaleswe ekep
in heexpe imen al anksun ilOc obe ,a e which heywe e e-
u ned omalecommuni y anks.A e eachdaily eco dingsession,
emaleswe e e u ned o hei communi y ank(Figu e S1).A he
endo each eco dingsession,malesand emaleswe emeasu ed
o leng handweigh .Measu emen swe emadeusingdigi alcalli-
pe sCD-15APXwi hap ecisiono 0.01 mm(Mi u oyo,Japan)anda
digi alscale(0.1 gp ecision).Asame ico malebodycondi ion,we
calcula ed hecondi ion ac o Ful on'sK [whe e K = (W/LS
3)*105]
ollowingAmo ime al.(2013).
2.2 | Acous ic eco dingsandsoundanalysis
Du ingacous ic eco dingsessions,ahyd ophone(H2A-XLRhy-
d ophone,Aqua ianAudio&Scien i ic;sensi i i y:−180 dB e.1 V
μPa−1; equency ange±4 dB om0.01 o100 kHz),wasplaced
abo e he shel e ( unnel-shaped plas ic co e ) and connec ed
oaIRIGPREp eampli ie (Aqua ianAudio&Scien i ic).Sounds
20457758, 2023, 11, Downloaded om h ps://onlinelib a y.wiley.com/doi/10.1002/ece3.10673 by Coch ane Po ugal, Wiley Online Lib a y on [24/11/2023]. See he Te ms and Condi ions (h ps://onlinelib a y.wiley.com/ e ms-and-condi ions) on Wiley Online Lib a y o ules o use; OA a icles a e go e ned by he applicable C ea i e Commons License
4o 18
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HORVATIĆ e al.
we e eco dedusingaZOOMH4npo abledigi alaudio eco de
(16bi /44.1 kHzsample a e;ZOOM).Thehyd ophonewasplaced
wi hin hea enua iondis ance om heemi e (less han5 cm),
andweobeyed helabo a o yp o ocol o minimum esonan e-
quency o smallglass anks(e.g.2.7 kHz o 170 L anks,acco ding
oAkama sue al.,2002).Reco dingswe ela e band-pass il e ed
(0.05–3 kHz) oimp o eS/N a ioandsubsampleda 4 kHz,and
u he ampli ied (10 dB) o be e audi o y and isual inspec-
iono heaudio acks.Digi alisedsoundswe eanalysedusing
A iso —SASLabP o5.2So wa e(1024-poin FFT,Fla Topwin-
dow;100% ame;A iso Bioacous ics).Tenaudio eco dings(2.5
pe male, eachlas ing app ox. 30 min)we e au allyand isually
inspec ed.No allsoundsp esen edagoodsignal- o-noise a io
(S/N) o acous icanalysis.F om10 eco dingsp esen ing hebes
S/N a io,weanalysed20 andomlyselec ed sounds.Tempo al
ea u eswe emeasu ed omoscillog ams,while equency- e-
la ed a iableswe eob ained om heloga i hmicpowe spec-
a(Fla Topwindow,512-poin sFFT,96.87%o e lap; esolu ion
8 Hz). Fo sounds, we measu ed he ollowing acous ic p ope -
ies ollowing Mala asi e al. (2008) and Amo im e al. (2013):
(1)sound a e(SR,numbe o soundsemi edin1 min om he
s a o soundp oduc ion);(2)sounddu a ion(DUR, o aldu a-
iono hecall,s);(3)numbe o pulses(NP);(4)pulse epe i ion
a e (PRR; NP di ided by DUR and mul iplied by 1000, Hz); (5)
pulsedu a ion(PD;measu ed om he i s o helas cyclein he
pulse,ms);(6)pulsepe iod(PP;a e agepeak- o-peakin e alo
consecu i epulses,ms);(7) equencymodula ion(FM,a e he
soundhasbeendi idedin o h ee empo allyiden icalsec ions,
FMi—ini ial,FMm—middleandFM — inal, equencymodula ion
wascalcula edas hedi e encebe ween he inalandini ialpulse
epe i ion a eandexp essedinHz;FMi,pulse epe i ion a eo
heini ialsec iono asoundandFM ,pulse epe i ion a eo he
inalsec iono a sound);(8)peak equency(PF, hepeakwi h
hehighes ene gy om heloga i hmicpowe spec um unc ion,
Hz).Ino de o ollow hep e ious eco dingp o ocolsasclosely
aspossible(Amo ime al.,2013;Amo im&Ne es,2007),wealso
calcula ed he ocalac i i ypa ame e spe male:(i)sound a e
(numbe o sounds p oduced pe min), (ii) maximum sound a e
(maximumnumbe o soundsemi edin1 min)and(iii)callinge -
o (pe cen ageo imespen calling,i.e.soundp oduc ioninsec-
ondsdi idedby hedu a iono he eco dinginseconds).Despi e
he ac ha he a iablesPPandPRRindica e hepulse epe i ion
pa e n, heywe edelibe a elyindica edsepa a elyhe e o a-
cili a ecompa isonswi h hegobyli e a u eonsoundp oduc ion.
2.3 | Video eco dingsandanalysiso
beha iou al ca ego ies
Du ingacous ic- isual eco dings,asecondhyd ophone(HTI-96-
Min,HighTechInc.,sensi i i y:−201 dB e.1 VμPa−1, equency
esponse2 Hz o30 kHz),placedless han3 cm om henes open-
ing,wasconnec eddi ec ly oa ideocamco de (CanonLeg ia
FS200, 41x digi al zoom, 25 ames/s) o di ec ly synch onise
acous icand isualsignalsin oauni o mda ase o subsequen
analysis.Thecamco de wasmoun edonas andandposi ioned
app ox. 40 cm om he on o he expe imen al glass anks.
Cou shipbeha iou beganwhen he emalesen e ed hemale
e i o ya adis anceo <5 cm om hemale'snes ,while hep e-
spawningphasewasobse edwhen he ipe emaleen e ed he
male'snes .Thespawningphasebeganwi h he emale u ning
upside-downin henes nume ous imesinsho successionand
s a ed ci cling he ceiling. Male beha iou s and he associa ed
soundemissionswe eobse edin ou soni e ousmalesdu ing
se en eco dingsessionsandanalysedusingSolomonCode ( e .
be a19.08.02).The ipe emaleswe echosen o he eco ding
sessionsacco ding o woindica o so hei eadiness o spawn-
ing(bellyandeyecolou a ion).
Beha iou alca ego iesexp essedby hemaleswe eclassi ied
ollowing heli e a u e(Amo ime al.,2013;Amo im&Ne es,2007,
2008; Mala asi e al., 2009).Weiden i iedninemalebeha iou al
ca ego ies wi hin h ee dis inc ep oduc i e phases in O. c oa icus
(Table S1):
• Cou shipphase,pe o medby hemaleou side henes :Chase,
Lead,App oachandCi cling;
• P e-spawningphase,pe o medby hemalewi hin henes :Nes
display,F on aldisplay,Nes ubbing,P e-ma ing;
• Spawningphase,pe o medwi hin henes :Spawning.
Spawning was conside ed when he emale epea edly pe -
o med he upside-down o belly-up posi ion, associa ed wi h
o iposi ion.Insomecases,Nes displayandF on aldisplaywe e
pe o medby hemaleoccupying henes wi ho wi hou a e-
male inside. Howe e , Nes ubbing, P e-ma ing and Spawning
we ealwayspe o medby hemalewhen he emalewasinside
he nes . In Solomon Code , wo da ase s we e analysed sepa-
a ely and hen compa ed. Fi s , beha iou ( equency (nmin−1)
anddu a ion(ins))wassco edin he ideo eco dingswi hsound
p oduc ion. We no ed he o al numbe o sounds emi ed pe
beha iou alca ego y o eachsoni e ousmale.Secondly,wean-
alysedeigh ideo eco dings( wope male)con aining hebe-
ha iou so hesame ou es edmales,bu when heydidno
p oduce sounds (i.e. males we e silen o he en i e eco ding
pe iod).Byha ing hese woda ase s,wein es iga ed hedi e -
encesin equencieso beha iou alca ego iesinmaleswhen hey
engagedinsoundp oduc ionandwhen heydidno .In o al,we
usedeigh malesinou expe imen s,bu ou we eun esponsi e
(i.e.didno pe o mcou shipbeha iou o sounds), esul ingin
insu icien da a o u he analyses.Weanalysed ideos o he
ollowingbeha iou alpa ame e s:malebeha iou a e( he o al
numbe o beha iou alca ego iespe min)(1)co-occu ingwi h
soundso (2)no co-occu ingwi hsounds;numbe o imesa e-
maleen e ed hemale'snes (3)accompaniedwi hsoundso (4)
wi hou sounds;(5) o albeha iou s(numbe o beha iou alca e-
go iespe ideo eco ding).
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5o 18
HORVATIĆ e al.
2.4 | Ana omicalanalysis
Fo ana omicaldissec ions,addi ionalO. c oa icus indi iduals we e
collec edinOc obe 2020 om hesamewa e cou senea he il-
lageB ečići(43°7′11.30″ N,17°29′4.03″ E)usingelec o ishing.Fi e
indi idualswe ecollec ed,o which h eemales(40–50 mmLT)we e
immedia elyeu hanisedwi hano e doseo MS-222( icaineme h-
anesulphona e;Pha maq),ands o ed o 1 weekin7% o maldehyde
ixa i esolu ionand hen ans e ed o70%e hanol.Specimens
we edissec edandexaminedwi haWildM10binocula mic oscope
(LeicaCame a,Leica)equippedwi hacame alucida os udy he
ana omyo hepu a i esound-p oducingmechanism.Sinceea lie
esea chongobieshighligh ed he oleo hepec o algi dleand
(pec o al) insinsoundp oduc ion,dissec ionsp ima ilyadd essed
he muscles ela ed o his body pa . The nomencla u e used o
designa emuscula pa swasbasedonea lie esea ch(Ad iaens
e al., 1993; Pa men ie e al., 2013, 2017; Win e bo om, 1974).
Addi ionally, one specimen was subjec ed o mic o-compu ed o-
mog aphy(μCT)scanning o isualise he ishskele ona hele el
o heneu oc aniumandpec o algi dle.Scanningwascomple ed
usingaRXEasyTom(RXSolu ions;h p : // w w w . x s o l u i o n s . ),wi h
analuminium il e .Imageswe egene a eda 75 kVand133 μA,wi h
a ame a eo 12.5,5a e age amespe image.Thisp ocedu e
gene a ed2897imagesa a oxelsizeo 10 μm.Recons uc ionwas
pe o medusingX-Ac so wa e omRXSolu ions.Segmen a ion,
isualisa ion and analysis we e pe o med using D agon ly so -
wa e (Objec Resea ch Sys ems (ORS) Inc, 2019; so wa e a ail-
able a h p : / / w w w . h e o b j e c s . c o m / d a g o n l y ). Th ee-dimensional
(3D)16-bi imageswe ep oducedandsubsequen lycon e edin o
8-bi oxelsusingImageJ(Ab amo e al.,2004).Th ee-dimensional
p ocessingand ende ingwe eob aineda e semi-au oma icseg-
men a iono hebodyusinga‘gene a edsu ace’,acco ding o he
p o ocolsdesc ibedbyZane ee al.(2013).Di ec olume ende -
ings(iso-su ace econs uc ions)we eused o isualiseasubse o
selec ed oxelso hean e io skele oninAMIRA2019.2.
2.5 | Acous iccompa isonamongsoni e ous
sand gobies
Thesoundso se ensoni e oussandgobies,Knipowi schia paniz-
zae Ve ga, 1841, Ninnigobius canes inii (Ninni 1883), O sinigobius
punc a issimus(Canes ini1864),Poma oschis us ma mo a us (Risso
1810),P. pic us(Malm,1865),P. mic ops(K øye ,1838)andP. minu us
(Pallas1770),we e eco dedandcha ac e isedbyp e iouss udies
(Amo ime al.,2013, 2018;Bolgane al.,2013; Lugli e al., 1995;
Lugli&To icelli,1999; Mala asi e al., 2008;Ped osoe al.,2013).
Howe e , hese acous ic da a we e ne e combined in o a single
phylogene icda ase andanalysedin e speci ically.The e o e,we
s udiedin e speci icacous ic a iabili yo soni e oussandgobies
(P. ma mo a us was sepa a ed geog aphically in o wo popula ions,
I alian and Po uguese). B ie ly, he species we e caugh in he
pas by au ho s o p e ious s udies ei he omb ackish habi a s
inno hAd ia icSea(K. panizzae, P. ma mo a us and N. canes inii),
om eshwa e so no h-wes pa o ReggioEmiliaRomagna,I aly
(O. punc a issimus;Linds öm&Lugli,2000; Lugli e al., 1995, 1997;
Lugli & To icelli, 1999), om Po uguesema ine/b ackish wa e s
(Amo ime al.,2013, 2018;Bolgane al.,2013)o hewes coas
o Sweden(Ped osoe al.,2013).Sound eco dingsga he ed om
hep e iouslyconduc edlabo a o yexpe imen swe e e-analysed
oallow o in e speci iccompa isonwi haminimalmeasu emen
expe imen ale o .Allin es iga edsandgobiesp oducedpulsa ile
sounds, husenablingacous icin e speci iccompa isons.Theda a-
se wascomposedo 36indi idualso eigh soni e oussandgobies
including O. c oa icus(min–max:3–5indi iduals,excep o asingle
indi idualo P. mic ops),wi ha leas h eesounds eco dedpe in-
di idual.In o alwecalcula ed hemeans o i eacous ic a iables
( empo al:DURinms,NP,PRRinHz;spec al:PFandFM,bo hin
Hz) o eachindi idual.Sincegobiesincludedin hecu en s udy
we e eco deda di e en wa e empe a u es( ange:15.8–22.6°C)
andi iswellknown ha heambien wa e empe a u ea ec s ish
acous ic signals (Ladich, 2018;Vicen ee al.,2015),weconduc ed
wosepa a emul i a ia eanalyses: he i s in ol ing hecomple e
da ase (all i eacous ic ea u es o eachspecies),and hesecond
excluding he empo al ea u es(DURandPRR)known obein lu-
encedbywa e empe a u e(Luglie al.,1996;Vicen ee al.,2015).
2.6 | S a is icalanalysis
The s a is ical analyses we e pe o med by combining he sounds
ommul ipleindi idualsin oasingleda ase .Ou lie sandex emes
we ede ec ed isually om heboxplo andwe eelimina ed om
heda ase i necessa y.Since heda awe eno no mallydis ibu ed
o some a iables om he awin aspeci icda ase (Shapi o-Wilk
es , p < .05), we used non-pa ame ic es s. Fo pai wise com-
pa isons be weensoni e ous O. c oa icusmales,weemployed he
K uskal-Wallis anksum es H ollowedbypai wiseDunn'smul i-
ple compa ison es wi h Bon e oni co ec ion o he p- alues.
Addi ionally, heChi-squa e(χ2)wasused o es o independenceo
beha iou omsoundp oduc ion.In his es , he esiduals om he
χ2we eused ode e minewhichbeha iou swe eposi i ely ela ed
osoundp oduc ion.K uskal-WallisH es wasused ocompa e he
meanbeha iou al a iables(calling a e,beha iou a e,n.o emale
nes en ances) be ween soni e ous males. Wilcoxon signed- ank
es waspe o med ocompa e he wodependen samples, ha is,
meanbeha iou al a iables(beha iou a eand emalenes en ance)
o maleswhen heyp oduced soundsandwhen heywe esilen .
Addi ionally,Wilcoxon es wasused ocompa e he equencyand
du a iono cou shipandp e-spawningphasesbe weenmales.
Fo hein e speci iccompa isons, hemeanso indi idualacous-
icp ope ies o soni e oussand gobies we ecompa ed wi h he
K uskal-WallisH- es ,since heda awe eno no mallydis ibu ed
(Shapi o-Wilk es ,p < .05).Toquan i yin e speci icacous ic a i-
abili yamong hesoni e oussandgobies omou s udy,weused
amul i a ia eapp oach.PCA,basedon heco ela ionma ix,was
pe o med on ans o med and s anda dised indi idual means o
i esound a iables( empo al:DUR,NP,PRR;spec al:PFandFM)
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6o 18
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HORVATIĆ e al.
oassesso e allacous ic a iabili ybe weensandgobies,andad-
di ionally o ecognise acous ic a iables explaining he obse ed
a iance.Toassess hepe cen ageo success ulclassi ica iono he
soundsassigned o heco ec gobyspecies,and omaximise he
sepa abili yamong axa,weusedlinea disc iminan analysis(LDA).
Twodi e en LDAswe epe o med, i s wi h hecomple eda ase
( i eacous ic a iables o eachspecies)and hen emo ing he em-
pe a u e-dependen ea u es(DURandPRR).Due o heFM'snega-
i e aw alues,weaddedaposi i e ac o o his ea u eso ha we
couldusei in hecompa a i eanalyses.Ou esul swe ep esen ed
asmeans(x ) ± s anda dde ia ion(SD),while hele elo signi icance
o in e -andin aspeci iccompa isonswas5%(α = 0.05).S a is ical
analyseswe epe o medinSTATISTICA®( .13.6.0.,TIBCO,USA),
Pas ( .4.11)andRS udio(2022.07.0)so wa e.
2.7 | Pe mi s
O sinigobius c oa icusislegallyp o ec edbylawasanendange ed
axoninC oa ia(O icialGaze eo heRepublico C oa ia,2016).
Inaddi ion,i isanendemicspecieswi h e ylimi eddis ibu ion.As
a esul , henumbe o indi idualsemployedin helabo a o yex-
pe imen swaskep oaminimum(less han15) op e en possible
e ec son hena u alpopula iono hisspecies.Thesamplingbyelec-
o ishing o scien i icpu posesin hena u alhabi a wasapp o ed
by heMinis yo Ag icul u e(pe mi numbe 525-13/0545-19-2),
whilealllabo a o y expe imen alp o ocols we e app o ed by he
Bioe hicsandAnimalWel a eCommi eeo heFacul yo Science,
Uni e si yo Zag eb(pe mi numbe 251-58-10617-21-147).
3 | RESULTS
3.1 | Soundp oduc ionandin aspeci icsound
signal s uc u e
Maleso O. c oa icusp oducedasingle ypeo acous icsignal,pulsa-
ilesound,du ingin e sexual(male– emale)in e ac ionsconduc ed
wi hin he ep oduc i eseason(Ap il–Oc obe ).Fou esiden males
(
x
± SD = 49.1 ± 0.8; ange:48.0–50.0 mmLT;40.9 ± 1.8; ange:38.9–
42.2 mm LS; 1.2 ± 0.1; ange: 1.1–1.4 g W; 1.7 ± 0.1; ange: 1.5–1.9
Ful on's K) p oduced sounds when in e ac ing wi h emales, while
heo he ou males emainedsilen anddidno cou .We eco ded
372soundsp oducedby he ou males(93soundspe male).Sounds
we ep oducedinani egula pa e n(7.7 ± 1.4; ange:6–10sound
min−1; Figu e 1; Table 1).Thesoundsa esho -du a ionsignals,las -
ing450 ms(442.0 ± 132.6 ms),andcomposedo a a iablenumbe o
sho pulses(14.2 ± 4.0)o a ound15 ms(14.5 ± 1.9 ms;Figu e 2a–d;
Table 1).Pulses uc u edi e edbe weensounds,exhibi ingone o
h eepeakswi h a iableampli ude.Gene ally, heampli udeo a
FIGURE1 (a)Maleand emaleo Ne e adwa goby,O sinigobius c oa icus.Pho oso indi iduals omHo a iće al.(2017),(b)Sound
p oduc iono O. c oa icusmales.The17-second eco dingclipdepic s heoscillog am( op)andspec og am(bo om)o ou pulsa ile
soundsp oducedbyamalegoby(g eydasheda ea).In hespec og am,wa me colou sindica ehighe acous icene gy(o angeishighes
andblueislowes ).Theho izon albanda low equency(app ox.100 Hz)co esponds oambien noises emming om heambien
labo a o ycondi ions.Spec og ampa ame e s:Fla Topwindow,1024leng hFFT;25% amesize;93.75%o e lap; esolu ion:4 Hz.RA,
ela i eampli ude.
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7o 18
HORVATIĆ e al.
soundchangedg adually, i s inc easingand hens eadilydec eas-
ing h oughou hesound,wi h he i s woo h eepulsesbeing he
highes inampli ude(Figu e 2a–d).Thepulse epe i ion a e a ied
om26.0 o38.0 Hz(32.5 ± 1.6 Hz),while hepulsepe iod(PP)a e -
aged32 ms(31.9 ± 1.4; angems).PPchangedwi hwa e empe a u e,
wi hhighe aluesoccu inga lowe empe a u es.In hepulsa ile
sounds,las PPwasalwayslonge han he emainingPPs.Peak e-
quency a ied om89 o340 Hz(137.4 ± 38.3 Hz),al houghse e al
highe equency componen s we e also p esen , especially in he
ange0.5–1.5 kHz.Ene gyex ended om0.05 o2 kHz(Figu e 2a,d;
Table 1),wi hmos o hesoundene gyconcen a edwi hin0.05–
0.6 kHz. F equency modula ion o he sounds anged om 0.7 o
1.1 Hz.Addi ionally, hecallinge o a iedbe weenmales om0.37
o0.60o soundp oduc ion/so eco ding(0.49 ± 0.09),indica ing
ha someindi idualsemi edsoundsmo e equen ly hano he s
(Table 1).In e es ingly,soundswe ene e o ganisedinbu s s,which
a eusuallycomposedo se e alconsecu i esoundsp oducedwi h
egula in e -soundin e als,asobse edinsomesandgobies.Du ing
ou in e sexualacous icexpe imen s,no emalesp oducedasound.
In aspeci ically, soni e ous O. c oa icus males di e ed in all
acous ic ea u es(K uskal-WallisH- es ,SRχ2 = 8.59,DURχ2 = 22.87,
NP χ2 = 24.53, PRR χ2 = 8.5936.87, PD χ2 = 8.07, PP χ2 = 23.73, PF
χ2 = 34.68, FMi χ2 = 38.05, FM χ2 = 29.92, FM χ2 = 12.81; d = 3;
N = 80; p < .05 o all ea u es) excep o calling e o (K uskal-
WallisH- es ,χ2 = 5.67;d = 3;N = 7;p > .05;Table 1).
3.2 | Rep oduc i ee hologyandassocia ion
wi h sounds
The equency,du a ionando e allpe cen ageo malebeha iou al
ca ego ieswe esco ed o ou soni e ousmalesindi e en ses-
sions:wi hsoundp oduc ionandsilen .The i s da ase included
se en ideo eco dings(210 min)whe ea leas onesoundoccu ed
pe eco dingbyeachmale.O e all,weobse ed410beha iou al
ca ego ies (102.5 pe male). The beha iou al ca ego ies Nes dis-
play(29.3%),P e-ma ing(22.7%)andApp oach(19.1%)we emos
equen ly obse ed while Ci cling (1.2%), Chase (1.0%) and Lead
(0.7%)we e a ely eco ded(Figu e 3).O he410beha iou alca -
ego ies( om ou males),99ca ego ies(24.1%)we eaccompanied
by sound p oduc ion. Sound p oduc ion was documen ed du ing
ials o he p e-spawning phase: P e-ma ing (303 sounds), Nes
display (27 sounds),F on al display(20 sounds), Nes ubbing(16
sounds)and o hespawningphase:Spawning( i esounds).Sounds
didno co-occu wi h hecou shipphases:App oach,Ci clingand
Lead (Figu e 3).Du ing ou Chase,onlyonesoundwas eco ded.
Onlyonespawningac (Spawning)wasobse edin hiss udy,du ing
which i esoundswe ep oduced.Un o una ely,spawningsounds
we eno usedin hecompa a i epu posesdue o hei limi edoc-
cu ence.Thechi-squa e(χ2) es o independenceindica ed ha
beha iou al ca ego ies Nes display and P e-ma ing we e signi i-
can ly associa ed wi h sound p oduc ion (χ2 = 138.3;d = 5;N = 99;
p < .05; esidualsco e:1.5and41.5, espec i ely),whileo he ca -
ego ies ailed osuppo hishypo hesis(Figu e 3).
To compa e male beha iou when soni e ous o silen , a sec-
ondda ase o eigh ideo eco dingswasconside ed(190.5 min)o
hesame ou malesbu inwhichnosound p oduc ionwas docu-
men ed.In hese eco dings,weobse ed324malebeha iou alca -
ego ies(a e aging81.0pe male),o whichApp oach(38.3%),Lead
(31.8%)andNes display(20.1%)we e hemos equen ca ego ies
(Figu e 3).Con a y,Chase,Ci cling,P e-ma ingo Spawningwe eno
documen edwi hin hese eco dingsessions.Ingene al, he eisan
ob iousdissimila i ybe ween he equencyo hebeha iou alca -
ego ies ha we eo we eno accompaniedbysounds.Speci ically,
P e-ma ing,oneo he wobeha iou ssigni ican lyassocia edwi h
soundp oduc ion,dec eased omana e ageo 22.7%in he ials
Acous ic pa ame e s
x
SD Range H p- alue
DUR(ms) 442.1 158.7 156.8–952.9 22.9 <.05
NP 14.3 5.1 5.0–32.0 24.5 <.05
PD(ms) 14.6 2.1 9.8–23.0 8.1 <.05
PRR(Hz) 32.5 2.6 26.0–38.1 36.9 <.05
PP(ms) 32.0 2.8 27.7–37.6 23.7 <.05
PF(Hz) 137.4 55.5 89.0–340.8 34.7 <.05
FMi 39.0 4.1 31.4–60.0 38.1 <.05
FM 34.1 3.7 26.1–45.4 29.9 <.05
FM(Hz) 0.9 0.1 0.7–1.1 12.8 <.05
SR(no.o sounds/min) 4.7 2.1 1.3–7.8 8.6 <.05
Callinge o 0.5 0.1 0.3–0.6 5.7 >.05
No e:Fo eachpa ame e ,mean(
x
),s anda dde ia ion(SD)and angewe e epo ed,wi h he
co esponding esul s om hein aspeci icK uskal-Wallis anksum es andp- alue.
Desc ip i es a is icsa ebasedon20soundspe malep esen ing hebes S/N a io(N = 4,n = 80).
H- aluesa e he esul so K uskal–Wallis es scompa ingsoundpa ame e samongmales.Bolded
p- aluesindica e he ea u e ha di e edbe weenmalesacco ding o hesigni icancele elo .05.
Fo heabb e ia ionso acous icp ope ies,seeSec ion2.
TABLE 1 Desc ip i es a is icso
soundacous icpa ame e sp oducedby
maleO sinigobius c oa icus.
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8o 18
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HORVATIĆ e al.
wi hsounds o0%in he ialswi hou sound.Inaddi ion,Nes dis-
play, Nes ubbing and F on al display ca ego ies p oduced du ing
soundemissiondec easedin equencyinexpe imen swi hou he
sounds(Nes display: om29.3% o20.1%;Nes ubbing: om13.9%
o 3.7%; F on al display: om 12% o 6.2%). On he o he hand,
App oach and Leadwe e mo e equen du ing hesilen sessions
(31%and38%, espec i ely) handu ingsoundp oduc ion(19%and
0.7%, espec i ely;Figu e 3).O e all, hebeha iou al a edec eased
om 55.8% o44.1%whenmalesp oducedsoundsin compa ison
owhen heywe esilen (soni e ous s.silen males:means2.79 s.
1.55), hough hedi e enceswe eno signi ican (Wilcoxonsigned-
ank es , N = 14;p > .05).Impo an ly, henumbe o imes he e-
malesen e ed hemalenes di e edsigni ican lybe ween he wo
da ase s(3.71 s.0.71),as emalenes en ancewasmo e equen
whenmalesp oducedsound hanwhen heywe esilen (Wilcoxon
signed- ank es ,N = 16,p < .05).Finally, he womales ecei ing he
mos emaleen ieswe e hela ges insize(41.7and42.2 mmSL).
These womalesp oduced hesoundswi hhighes alueso NP(>13
pulses),FMi(>38.5 Hz)andPRR(>33.5 Hz).
Conside ing he sessions in which sound occu ed, he e-
quency o occu ence o beha iou s be ween he cou ship
(Chase,Lead,App oachandCi cling)andp e-spawning(Nes dis-
play,F on aldisplay,Nes ubbing,P e-ma ing)phaseso ep o-
duc iondidno di e (Wilcoxonsigned- ank es ,N = 8;p > .05),
hough hei du a ion did (Wilcoxon signed- ank es , N = 8;
p < .05).Gene ally,malesexhibi edcou ship- ela edbeha iou s
FIGURE2 S uc u eo apulsa ilesoundp oducedbyO sinigobius c oa icus.Diag amillus a ing heacous ic a iablesmeasu ed om
hepulsa ilesounds.(a)Spec og amand(b)oscillog amo hepulsa ilesound;(c)oscillog amo isola edpulses(6–8)ing ey;(d)powe
spec umo hepulsa ilesound om(a).DUR,sounddu a ion( o alleng ho hecall,measu edinmilliseconds);NP,numbe o pulses;
PRR,pulse epe i ion a e(NPdi idedbyDURandmul ipliedby1000 Hz);PD,pulsedu a ion(ms);PP,pulsepe iod(a e agepeak- o-
peakin e alo consecu i epulses,ms);FM, equencymodula ion(a e hesoundhasbeendi idedin o wosec ions,FMiandFM ,
equencymodula ionwascalcula edas hedi e encebe ween he inalandini ialpulse epe i ion a eandexp essedinHz);FMi,
equencymodula ion—ini ial(pulse epe i ion a eo heini ialsec iono ad um);FMm, equencymodula ion-middle,FM , equency
modula ion— inal(pulse epe i ion a eo he inalsec iono ad um);PF,peak equency(ob ainedasapeakwi h hehighes ene gy om
heloga i hmicpowe spec um unc ion,Hz;whi ea owinspec og am), 0alsoco espond o he undamen al equency.Spec og am
pa ame e s:Fla Topwindow,256leng hFFT;25% amesize;93.75%o e lap; esolu ion:4 Hz.RA, ela i eampli ude.
20457758, 2023, 11, Downloaded om h ps://onlinelib a y.wiley.com/doi/10.1002/ece3.10673 by Coch ane Po ugal, Wiley Online Lib a y on [24/11/2023]. See he Te ms and Condi ions (h ps://onlinelib a y.wiley.com/ e ms-and-condi ions) on Wiley Online Lib a y o ules o use; OA a icles a e go e ned by he applicable C ea i e Commons License
|
9o 18
HORVATIĆ e al.
less equen lyand o asho e pe iodcompa ed op e-spawning
beha iou s.
3.3 | Ana omical indingsandmo emen sdu ing
sound p oduc ion
The pec o al gi dle o O. c oa icus was subjec ed o μCT scan-
ninganddissec ion oiden i y he a iousosseouss uc u esand
muscles ha maybein ol edinsoundgene a ion.F omμCT scans,
h ee unc ionaluni swe edis inguishedin heskele alpa o he
pec o algi dleo O. c oa icus: heshoulde gi dle(composedo he
pos - empo al, hesup aclei h umand heclei h umbones)do sally
a ached o heneu oc anium, heshoulde pla e(i.e. ou la ge adi-
als)and he inpla e,madeupo in aysa icula edwi h heshoul-
de pla e (Figu e 4).On hedo sal ipo heclei h um,an e io and
pos e io p ocessesa ep esen .Thesup aclei h uma icula eswi h
hepos - empo aland heclei h um,connec ingwi h heclei h um
FIGURE3 Acous icbeha iou o O sinigobius c oa icusmalesdu ingsexualin e ac ionsexp essed h oughninebeha iou alca ego ies.
In(a),soundp oduc ionwasobse edince ainca ego ies(Chase,Nes display,F on aldisplay,Nes ubbing,P e-ma ingandSpawning),
whichwe eaccompaniedbysoundemission(i.e. heda kg eyba a he opo hecolumn).In(b),nosoundp oduc ionwasobse ed.In
(a)and(b), heligh g eycolou o hecolumnindica es henumbe o documen edcou shipbeha iou alac s.As e isk(*)indica es he
signi ican associa iono beha iou alca ego ieswi hsoundp oduc ion.Numbe sabo ecolumnsindica e he o alnumbe o eco ded
soundspe eachbeha iou alca ego y.Theg eena eaencompasses hecou shipphasepe o medou sideo henes , hedashedblue
a eahighligh s hep e-spawningphasewhile hedashedo angea eaindica es hespawningphaseo ep oduc ion,displayedin henes .
20457758, 2023, 11, Downloaded om h ps://onlinelib a y.wiley.com/doi/10.1002/ece3.10673 by Coch ane Po ugal, Wiley Online Lib a y on [24/11/2023]. See he Te ms and Condi ions (h ps://onlinelib a y.wiley.com/ e ms-and-condi ions) on Wiley Online Lib a y o ules o use; OA a icles a e go e ned by he applicable C ea i e Commons License
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