Multimodalcommunication incourtingfiddlercrabs · 2017-05-02 · drumming with in situ performance (sprint speed) trials to test whether ﬁne-scale aspects of waving and/or drumming

rsosroyalsocietypublishingorg

ResearchCite this articleMowles SL Jennions MBackwell PRY 2017 Multimodalcommunication in courting fiddler crabsreveals male performance capacities R Socopen sci 4 161093httpdxdoiorg101098rsos161093

Received 27 December 2016Accepted 14 February 2017

Subject CategoryBiology (whole organism)

Subject Areasbehaviourecology

Keywordsbiotremology courtship fiddler crabmultimodal signal stamina vibrational signal

Author for correspondenceSophie L Mowlese-mail sophiemowlesangliaacuk

Electronic supplementary material is availableonline at httpsdxdoiorg106084m9figsharec3703657

Multimodal communicationin courting fiddler crabsreveals male performancecapacitiesSophie L Mowles12 Michael Jennions2 and Patricia

R Y Backwell21Animal and Environment Research Group Faculty of Science and TechnologyAnglia Ruskin University East Road Cambridge CB1 1PT UK2Evolution Ecology and Genetics Research School of Biology The Australian NationalUniversity Canberra Australian Capital Territory Australia

SLM 0000-0002-2323-0509

Courting males often perform different behavioural displaysthat demonstrate aspects of their quality Male fiddler crabsUca sp are well known for their repetitive claw-wavingdisplay during courtship However in some species malesproduce an additional signal by rapidly stridulating their clawcreating a lsquodrummingrsquo vibrational signal through the substrateas a female approaches and even continue to drum once insidetheir burrow Here we show that the switch from wavingto drumming might provide additional information to thefemale about the quality of a male and the properties of hisburrow (multiple message hypothesis) Across males there washowever a strong positive relationship between aspects of theirwaving and drumming displays suggesting that drummingadheres to some predictions of the redundant signal hypothesisfor multimodal signalling In field experiments we show thatrecent courtship is associated with a significant reduction inmale sprint speed which is commensurate with an oxygendebt Even so males that wave and drum more vigorouslythan their counterparts have a higher sprint speed Drummingappears to be an energetically costly multimodal display ofquality that females should attend to when making their matechoice decisions

1 IntroductionSexual selection due to female choice has led to the evolutionof elaborate male courtship displays that seem to communicatea malersquos quality as a mate [12] Males often court byproducing repetitive signals that range from sounds andphysical movements to electric pulses and vibrational signals

2017 The Authors Published by the Royal Society under the terms of the Creative CommonsAttribution License httpcreativecommonsorglicensesby40 which permits unrestricteduse provided the original author and source are credited

on March 29 2017httprsosroyalsocietypublishingorgDownloaded from

rsosroyalsocietypublishingorgRSocopensci4161093

(examples in [3]) In some species males produce displays that use a single channel of communicationsuch as stridulating in crickets (eg [45]) or head-nodding in land-dwelling fish [6] In other speciesmales produce lsquomultimodalrsquo displays which are defined as lsquocomposite signals received through morethan one sensory channelrsquo [7] For example male golden-collared manakins (Manacus vitellinus) use bothbody movements and sounds in their courtship displays [8] and male peacock spiders (Maratus volans)make both distinctive movements and produce vibratory signals to court females [910]

Does the use of multiple courtship signals simply serve to confirm the information beingcommunicated (the redundant signal hypothesis) (reviews [1112]) Or do different signals advertisedifferent aspects of a malersquos quality (the multiple message hypothesis) We might assume that sendingmultiple messages involves the use of different channels of communication (eg sound and vision) butthis need not be the case For example male Anolis lizards extend their dewlaps and perform lsquopush-uprsquodisplays in territorial displays These are both visual signals but dewlap size is thought to advertise amalersquos bite force [13] while the vigour of the lsquopush-uprsquo display is assumed to signal a malersquos stamina [14]Conversely it is possible that signals that use different channels of communication may provide the sameinformation For example courtship displays often seem to be indices of stamina and this informationcan be conveyed in several ways [315] For instance in some species males make vibrational signalsthat convey information about their stamina to females (eg wolf spiders that drum on leaves [1617])whereas in other species the rate of acoustic advertisement calling provides females with informationabout a malersquos energetic reserves (eg crickets [5]) To date few studies have looked at species thatcourt using several channels of communication to ask how different signal types are related to energyexpenditure or to ask about the relative investment that males put into each type of signal Here weaddress this oversight by studying courtship in the banana fiddler crab Uca mjoebergi

Fiddler crabs genus Uca are well known for their extreme sexual dimorphism Females havetwo small feeding claws while one of the claws in males is greatly enlarged (the major claw) [18]In many fiddler crab species males court by making a repetitive waving motion with their majorclaw [19] Females prefer males with larger claws (eg U perplexa [20]) that are waved at higher rates(eg U mjoebergi [21]) Claw waving is energetically costly lactic acid levels in malesrsquo haemolymphbecome elevated when they wave presumably because of anaerobic respiration [22] However no studyhas directly linked a malersquos wave rate to associated costs If there is a positive relationship between thevigour of waving and the accumulation of energetic costs it would confirm that courtship waving is asignal of stamina [3] Such energetically costly lsquosignals of staminarsquo are likely to be important to femalesas they would reflect the ability of the male to perform other demanding activities such as sprinting toavoid predators while also indicating that the male has accrued sufficient energy reserves to expendin display thus demonstrating that he is an effective forager These are attributes with which a choosyfemale should want to provision her offspring [23] Further the ability to perform a demanding displaywell may also indicate that the male is in good condition thus preventing females from mating withdiseased or parasitized males [24]

In some fiddler crab species males additionally produce vibrational signals via rapid movements oftheir major claw which are transmitted through the ground despite the stridulating major claw makinglittle if no contact with the substrate [25ndash27] Males perform this lsquodrummingrsquo [25] vibrational displayas a female approaches the malersquos burrow [26] and even continue to drum after she follows him intothe burrow There is evidence that females prefer males that emit rapid vibrations [28] but the specificfunction of drumming has yet to be investigated Drumming may contain information not providedby the waving display (ie the multiple message hypothesis) For example the vibratory nature of thedisplay might advertise structural properties of a malersquos burrow Burrow dimensions are important toa female because she stays inside the mated malersquos burrow to incubate her eggs (see [28]) Burrowproperties affect the speed at which eggs develop into larvae which is crucial to ensure the correct timingof larval release during a nocturnal spring tide (eg [2930]) Thus drumming might allow females tochoose a male with an appropriate burrow if the acoustic properties of the drumming display permitthe female to assess the physical characteristics of the burrow Alternatively drumming might advertiseother aspects of male quality such as size (multiple message hypothesis) Larger males are likely toproduce more powerful drums as occurs with shell-rapping by hermit crabs [31] If so drummingmight be an index of male size rather than an inherently costly handicap signal [32] although indicesand handicaps are often hard to distinguish [33] (eg drumming with a larger claw might consume moreenergy) Finally drumming might reinforce information already provided by waving (redundant signalhypothesis) Vibrational displays in other taxa are energetically costly (eg wolf spiders [16]) Drummingby a male fiddler crab might augment his claw-waving display by confirming his ability to perform ademanding activity consistent with a signal of stamina

In this study we examined signalling by male fiddler crabs in the final stage of courtship as a

female approaches a malersquos burrow We specifically tested the energetic consequences of waving anddrumming with in situ performance (sprint speed) trials to test whether fine-scale aspects of wavingandor drumming predict hence signal post-display performance We also tested whether the acousticproperties of the drumming display better agreed with the multiple messages or redundant signalhypotheses

2 Material and methods21 Study site and organismsWe carried out fieldwork on U mjoebergi from September to November 2014 at East Point ReserveDarwin Australia during the diurnal low tide period of neap tides In our experiments we presentedeach treatment male with a different stimulus female (see below) We always chose males (control andtreatment) that we had earlier seen waving as they were more likely to court a stimulus female if one waspresented (N = 89) Males were chosen haphazardly with respect to size to reflect the natural size range(carapace widths treatment males 1181 plusmn 010 mm control males 1185 plusmn 009 mm) (All summary dataare presented as mean plusmn se)

22 Stimulus femalesWe captured resident females at their burrows Each female was then carefully tethered to the end ofa thin wooden dowel (2 mm diameter) which was attached to a long dowel (1 cm diameter 120 cm inlength) The stimulus female was then moved towards a focal male to elicit natural courtship behaviourThese females were all similar in size (carapace width 915 plusmn 007 mm) to reduce any effect of variationin female body size on male courtship effort

23 Behavioural experimentsOnce we identified a focal male we placed a contact microphone (TWA-3S Japan frequency response100 Hzndash8 kHzplusmn3 dB) 15 cm from the burrow entrance We then drew a series of faint lines in thesand at 10 cm 5 cm and 25 cm from the burrow to provide set distances at which to temporarilyhalt the female as we moved her towards the male We used a Sony Handicam DCR-SR45E to filmboth the malersquos behaviour and the femalersquos progress along the graduated track To start a trial thestimulus female was held at the 10 cm mark for 1 min after which she was moved to the 5 cm markfor 1 min then to the 25 cm mark for 1 min and finally to the burrow entrance for one minuteThroughout her approach we video recorded the malersquos behaviour and recorded his drummingdisplay as 24 bit WAV files using a Tascam Linear PCM Recorder (DR-07 Mk II) receiving inputfrom the contact microphone Both the contact microphone and the recorder were calibrated at thestart of each trial to receive and record at 50 maximum on each occasion to prevent peaking of themicrophone

24 Sprint performance experimentsImmediately after the trial we captured the male and released him at the start of a 15 m long sprinttrack (made of two vertical plastic sheets that were 5 cm apart and embedded in the substrate (seeelectronic supplementary material S1) Males ran spontaneously when released and were pursuedalong the racetrack with a wooden probe The sprint speed over 50 cm was recorded from a lsquostartlinersquo to a lsquofinish linersquo in the first half of the track However the track was necessarily longer thanthis distance to ensure that the crab ran at full speed over the required distance instead of slowingtowards the end of the 50 cm Control males were tested identically except that they were not exposedto an approaching stimulus female We also ensured that as with treatment males we had earlierseen control males waving After the sprint trial the focal male was placed in an isolated cup (10 cmdiameter) filled to a depth of 1 cm with seawater and left in the shade for an hour before beingretested This process was repeated twice so that we eventually had three sprint speed measuresper male

25 Crab morphologyAfter the final sprint trial we measured the malersquos carapace width and major claw length to the nearest01 mm using a pair of dial callipers We also noted his handedness and if his claw was regenerated ororiginal Only five males per treatment group had a regenerated claw

26 Measuring burrow parametersAfter the burrow owner had been captured we surrounded the burrow entrance with a plastic collarto prevent other crabs from entering it We then filled the burrow with Polyfilla Expanding Foam Weallowed the cast to set for an hour before digging it out cleaning it and allowing it to dry (electronicsupplementary material S2) We measured the burrow volume by submerging the cast in a 1 l measuringcylinder to record how much water was displaced (to the nearest 25 cm3)

27 Behavioural analysesWe combined the video and audio files for each encounter using Windows Live Movie Maker The audiofrom the video files was muted to make any drumming recorded by the contact microphone more salientWe then watched the combined video and audio files and scored male behaviours using jWatcher eventrecording software We recorded each claw wave and each bout of drumming (and noted if it was on thesubstrate at the burrow entrance or underground)

28 Acoustic analysesThe frequencies recorded from the drumming crabs (3445ndash72882 Hz) were well within the frequencycharacteristics of the contact microphone (TWA-3S Japan frequency response 100 Hzndash8 kHzplusmn3 dB) andthat expected for a sand substrate [2834]

We analysed audio files using Raven Pro 14 The spectrograms were used to identify each individualsignal component making up each bout of drumming (see electronic supplementary material S3)from which the peak frequency (the frequency (hertz) at which the highest amplitude occurred) andpeak power (decibel) could be extracted We then tested whether drumming behaviour changed whenthe male was on the substrate (and with the distance of the female from the male) at the burrowentrance or within the burrow Any change in drumming allows us to identify whether drummingadvertises male or burrow characteristics For example changes in vigour would be indicative of adisplay of male stamina whereas a more consistent signal structure may indicate that the drummingsignal is used to advertise characteristics other than the performance capacity of the male such as thephysical structure of the burrow Further the precise point at which each individual beat was producedwas recorded enabling us to make fine-scale analyses of signal component production and escalationpatterns

29 Quantifying signal escalationWe measured the bivariate correlations between the vigour of signal production and the point duringthe trial at which the signal element was produced Thus the interval between bouts of drummingthe interval between individual lsquobeatsrsquo and the number of beatsbout were each correlated againstwhen they were produced during the trial For the interval measures the signal is escalated if thereis a negative correlation (ie intervals are shorter as the interaction progresses) For the beatsboutthe signal is escalated if there is a positive correlation (ie more beats are produced per bout asthe interaction progresses) Conversely signal reduction occurs if the correlations are in the oppositedirections Here we assign discrete categories to the type of signal change (escalation de-escalation orstatic) depending on whether the correlation is significantly greater than zero significantly less than zeroor non-significant [35]

210 Statistical methodsTo test for differences in the number of waves or drums produced when the female was at differentdistances from the male (10 5 25 or 0 cm from the burrow) we used Friedmanrsquos rank sum test becausethere were four repeated measurements per male

To assess whether courtship is energetically demanding we compared the performance (ie sprint

speed) of treatment males (that had just courted) and control males (that had not courted) Sprint speedwas log10 transformed to meet the requirements of the parametric tests We used a repeated measuresANOVA because we had three sprint estimates per male The between subject factor was male status(courtship treatment or control) and the repeated measure was the trial Trial 1 (immediately aftercapture) Trial 2 (1 h after capture) and Trial 3 (2 h after capture) Post hoc analyses were conducted usingone-way ANOVAs with male status as the factor

We calculated the relationships between male performance indices of drumming vigour (meanbout interval mean beat interval and beatsbout) morphology and drumming frequency (hertz) usingPearsonrsquos correlations We quantified the relationships between drumming amplitude morphologyand burrow volume using Spearmanrsquos correlations as amplitude and burrow volume could not benormalized by transformation All data were analysed using R v 310

3 Results31 Male courtship sequenceAs a female approached a male his waving decreased significantly (Friedman χ2

3 = 137445 p lt 0001)while the number of bouts of drumming increased significantly (Friedman χ2

3 = 139035 p lt 0001figure 1) Across males there was a significant positive relationship between the total number of wavesand the number of bouts of drumming performed (r = 0265 df = 87 p = 0012)

32 Courtship and sprint performanceControl males had significantly higher sprint speeds than males that had just courted (F1290 = 16567p lt 0001 figure 2) There was however a significant difference between the two types of males in howsprint speed changed over the three trials (F2290 = 4247 p = 0015) There was no difference in sprintspeed between control and recently courting males immediately after capture (Trial 1 F1145 = 2616p = 0108) However 1 or 2 h later recently courting males sprinted significantly more slowly than controlmales (Trial 2 F1145 = 1806 p lt 0001 Trial 3 F1145 = 1484 p lt 0001)

33 Sprint performance and courtship vigourIn the first performance trial males that produced more claw waves males that had a shorter intervalbetween drum beats and males that performed more beats per bout ran significantly faster (figure 3)There was however no relationship between the number of drumming bouts or the interval betweenthese bouts and how fast the male sprinted In the second and third performance trials none of the fivemeasures of courtship vigour were related to a malersquos sprint speed (table 1)

34 Sprint performance and male sizeFor males that had recently been induced to court larger individuals ran significantly faster in all threeperformance trials By contrast for control males there was no relationship between their size and sprintspeed in any of the three performance trials (table 2)

35 Male size and courtship vigourLarger males performed significantly more beats per bout of drumming There were however nosignificant relationships between male size and any of the other four measures of courtship vigour(table 3)

36 Courtship escalation and sprint performanceMales switch from waving to drumming as a female approaches (figure 1) Consequently waving alwaysdeclines while drumming escalates We therefore investigated net courtship escalation by combiningdata on the intervals between claw waves and bouts of drumming We then compared the performanceof three types of males those that showed an escalation (N = 16) de-escalation (N = 20) or a static rate ofcourtship display (N = 51) as the female approached To do this we carried out generalized linear models

waves drumming bouts

010 cmdistance between female and burrow entrance

5 cm 25 cm 0 cm

Figure 1 Themean number of waves and bouts of drumming produced by amale when the female is 10 cm 5 cm 25 cm and 0 cm fromhis burrow entrance Error bars represent standard errors

control courtship

00 h 1 h 2 h

time post-display

sndash1

Figure 2 The performance capacities (sprint speeds over 50 cm) of males that had courted and control males 2 h 1 h or immediatelyafter displaying Error bars represent standard errors

(GLMs) using a binomial error distribution and logit link function to test whether the category of overallsignal production exhibited by the male (escalation de-escalation or static rate of display) predicted theirsubsequent sprint speeds in the performance capacity trials Thus signal escalation was the factor in themodels while sprint speed in each trial was the dependent variable As crab size is related to sprintperformance we included it as a covariate in our models

In the initial performance trial there was no interaction between crab size and male performance sothe interaction was removed from this model There was no significant difference in sprint speed betweenthe three types of males (GLM z = 1442 df = 77 p = 0149) and no overall relationship between sprintspeed and male size (GLM z = 1129 df = 77 p = 0259)

For the second and third performance trials (1 and 2 h later) there were significant differences in sprintspeed between the three types of males (GLM Trial 2 z = 2199 p = 0028 Trial 3 z = 1990 p = 0047 bothdf = 76 figure 4) There was also a difference among male types in the relationship between body sizeand sprint speed (GLM Trial 2 z = minus2255 p = 0024 Trial 3 z = minus1992 p = 0046 both df = 76 figure 5)Among males that reduced their courtship display vigour larger males sprinted faster (Trial 2 r = 0664p = 0002 Trial 3 r = 0502 p = 0028 both df = 17) There was no such relationship for males that did

ndash1)

20181614121008060402

004 06 08 10 12 14 16 18

0020 0025 0030mean inter-beat interval

beats per drumming bout

0035 0040 0045

0 10 20 30 40 50 60 70 80 90no cheliped waves

Figure 3 The relationships between a malersquos performance capacity (sprint speed in cm sminus1) immediately after displaying and (a) thenumber of chelipedwaves (R2 = 0065) (b) themean interval between chelipedbeats (R2 = 0054) and (c) themeannumber of chelipedbeats per bout of drumming (R2 = 0055)

not change their courtship display vigour (r = 0173 p = 0235 r = 0177 p = 0223 both df = 47) or forthose that escalated their display vigour (Trial 2 r = minus0152 p = 0603 Trial 3 r = minus0156 p = 0592 bothdf = 12)

37 Escalation in the rate of drummingMost males maintained a static rate of drumming as courtship progressed (table 4) Other males escalatedtheir display by shortening the intervals between bouts or between beats within a bout Very few males(less than 3) increased the intervals between bouts or between beats within a bout Finally for mostmales the number of drums per bout remained constant as a female approached although 15 of males(N = 13) did reduce their rate of drumming

Table 1 The relationship between courtship display vigour and performance in subsequent sprint trials Performance was measured assprint speed in cm sminus1 Significant results are indicated in bold typeface

R df p-value

mean number of waves

performance immediately post-display 0255 80 0021

performance 1 h post-display 0028 80 0802

mean number of drumming bouts

performance 1 h post-display minus0047 80 0677

drumming characteristics

mean inter-drumming bout interval

performance immediately post-display minus0147 79 0190

mean inter-beat interval

mean beats per bout

Table 2 The relationship between male carapace width and performance in subsequent sprint trials Performance was measured assprint speed in cm sminus1

r df p-value

courtship trials

control trials

38 Acoustic properties of drumming and male sizeLarger males did not drum at a higher frequency (hertz) or amplitude (decibel) (table 5) Largermales constructed larger volume burrows (rs = 0452 N = 89 p lt 0001) The peak frequency (hertz)of drumming from within the burrow was higher for males with larger burrows (table 6 figure 6)and this remained the case even after controlling for male size (partial correlation r = 0352 N = 72

ndash1)

0de-escalation static escalation

Figure 4 The mean performance capacities 1 h post-display according to whether males escalated de-escalated or maintained a staticrate of signalling

ndash1)

095 105 115 125 135 145

male carapace width (mm)

de-escalation

static

escalationde-escalation

static

escalation

Figure 5 The interaction between male carapace width performance capacity and whether a male escalated de-escalated ormaintained a static rate of signalling

Table 3 The relationship between male carapace width and indices of display vigour Significant results are indicated in bold typeface

r df p-value

mean number of waves 0124 87 0246

mean number of drumming bouts minus0112 87 0297

mean inter-drumming bout interval 0040 85 0713

mean inter-beat interval minus0048 85 0656

mean beats per bout 0294 85 0006

p = 0003) There was however no relationship between burrow volume and the amplitude (decibel)of drumming Finally males with larger burrows produced more drums per bout (r = 0245 df = 85p = 0022) although this was driven by larger males producing more drums per bout (partial correlationr = 0219 N = 87 p = 0043) rather than burrow volume being directly linked to drumming vigour (partialcorrelation r = 0143 N = 87 p = 0189)

2000 50 100 150 200

burrow volume (cm3)

Figure 6 The relationship between burrow volume and the peak frequency of cheliped drumming

Table 4 The number of males producing drumming at constant escalating and de-escalating rates

static escalation de-escalation

bout interval 54 28 2

beat interval 45 39 3

drums per bout 69 5 13

Table 5 Correlations of male carapace width against the peak frequency and amplitude of drumming

frequency of drumming (Hz) range mean r df p-value

surface 3445ndash72882 53786 minus0142 35 0403

entrance 36723ndash70058 54065 minus0051 81 0645

underground 37060ndash71103 54961 0130 70 0277

amplitude of drumming (dB) rs N p-value

surface 6135ndash13186 8010 0033 37 0846

underground 7759ndash14094 9436 minus0035 72 0771

Table 6 The relationship between burrow volume and the peak frequency or amplitude of drumming Significant results are indicatedin bold typeface

rs N p-value

frequency of drumming

surface minus0190 37 0261

entrance 0112 83 0312

underground 0273 72 0020

amplitude of drumming

entrance minus0182 83 0099

underground minus0132 72 0268

4 DiscussionIn U mjoebergi males initially court a female by waving their brightly coloured major claw As sheapproaches they switch to stridulating their claw producing a lsquodrummingrsquo signal which althoughinvolving little to no contact between the major chela and the substrate is transmitted through thesubstrate as a series of rapid vibrations Wave rate influences female choice females prefer males thatwave at a higher rate [21] Females also prefer males with a larger claw [20] We do not yet know iffemale choice in U mjoebergi is influenced by drumming but females in another Uca species select malesbased on the vigour of their drumming display [28] Here we confirm that drumming in U mjoebergiconveys information about both a malersquos stamina and the size of his burrow suggesting that femaleswould benefit by choosing males using drumming signals

The simultaneous production of repetitive visual displays and vibrational courtship signals occursin several invertebrate taxa (eg Saliticid [910] and Lycosid [1617] spiders) In fiddler crabs howeverthe production of vibrational signals (drumming) can occur independently from visual displays (clawwaving) This occurs when a male is underground in his burrow but the female is still on the surface(eg [26]) Similarly in some spiders such as tarantulas (Eupalestrus weijenberghi and Acanthoscurriasuina) males on the surface drum to send vibrational signals to females that are underground [35]In U mjoebergi there is a gradual shift from waving to drumming as courtship progresses (electronicsupplementary material video) We showed that males that wave at a high rate also drum at a high rateThis suggests that the vibrational signal produced by drumming serves a similar function to that of thewaving display consistent with the redundant signal hypothesis [1112] The advantage of using twomodes of communication is however that males can still provide information from inside their burrowwhen they are no longer visible to a female

Repetitive courtship displays can advertise the quality of a male by (i) allowing the female repeatedopportunities to assess each individual signal and correct for productionreception errors (ie to increasethe accuracy of information acquisition see [315]) (ii) allowing the male to demonstrate his ability tobear signalling costs which might be extrinsic (eg enhanced predation risk see [3637]) or intrinsic(eg energetic costs of displaying [51622]) We found that male U mjoebergi suffer energetic costswhen courting Males experimentally induced to court had a significantly poorer performance in sprinttrials than non-courting control males However this difference was initially absent and it only becameapparent 1 or 2 h after courting This suggests that the build-up of lactic acid associated with signalling infiddler crabs [22] reduces future performance which is commensurate with an ongoing oxygen debt Theseemingly heavy investment required to drum and wave is likely to allow females to select physicallyfit mates

Female U mjoebergi can select physically fit males if they pay attention to both the absolute levelof courtship signal production and whether or not it increases as they approach a male In theinitial performance capacity trials immediately post-courtship before the effects of oxygen debt wereapparent males that had more vigorous displays (eg more waves shorter intervals between vibrationalsignals and more signals per drumming bout) had a higher performance capacity (ie sprint speed)Furthermore when retested 1 h later males that escalated their rate of courtship during a femalersquosapproach had a higher sprint speed than males whose display rate stayed the same or declined

The demanding courtship display of male fiddler crabs is informative as males seem to varyconsiderably in quality independently of body size A broad range of performance capacities is evidencedby the way in which sprint capacity in the later performance trials is affected by an interaction betweenmale size and the change in courtship rate Males that reduced their display rate exhibited a significantpositive correlation between speed and carapace width whereas this relationship was absent in malesthat either escalated or maintained a static display rate Once males have engaged in an energeticallydemanding display such that the anaerobic threshold is reached (most likely to have occurred for malesthat reduced their courtship an indication of exhaustion in signalling animals) body size is the bestpredictor of performance whereas initially stamina is highly variable amongst individuals and notpredicted by body size Indeed Matsumasa amp Murai [22] demonstrated great variation in baseline levelsof haemolymph glucose in fiddler crabs confirming that there can be significant variation in male qualityin this taxon Our results supports the general finding that courtship displays are energetically costly andthat females can profitably use them during mate choice to gauge male performance capacity

Aside from being linked to a malersquos performance capacity vibrational signals produced by drummingprovide information about a malersquos burrow Using this information could benefit females because itreduces their risk of being coerced into mating that arises when they enter a malersquos burrow to directlyassess its volume [38] In U mjoebergi the amplitude (decibel) of vibrational signals was unrelated to a

malersquos size or to that of his burrow however the peak frequency (hertz) was positively related to burrowvolume This is consistent with findings for substrate-borne signals in insects [39] and arachnids [40]their frequency is not dependent on the signallerrsquos body size (but see [28]) but instead is governed bythe properties of the substrate [41] In U mjoebergi larger volume burrows have proportionately wideropenings usually having been created by crabs of larger carapace widths Thus the higher frequenciesproduced from larger burrows are not due to narrower openings However larger volume burrows arelonger and deeper presenting a greater length of sand through which the low frequency componentsmay be filtered out during their transmission This is an area that requires further research to fullyresolve including an investigation of the physical properties of the substrate (eg compactness andsaturation) In U mjoebergi we also showed that larger males produce more signal components (beats)per bout of drumming and that this is correlated with burrow volume via male size Thus the frequencyof drumming is another signal that females can use to estimate burrow volume

Although females generally prefer bigger males [20] the value of a larger burrow depends on theambient temperature [42] and the stage of the lunar cycle at which mating occurs [43] Female U mjoebergiexhibit variation in their preference for male size hence burrow volume (as the two are correlated)over the 9-day semi-lunar mating period [30] It might therefore sometimes be detrimental for a maleto provide additional information about burrow volume by drumming Given that males performdrumming interspersed with waving on the substrate but continue to drum once inside their burrowwe suggest that drumming primarily reinforces a femalersquos perception of a malersquos stamina Drummingprovides an alternative means of assessment of stamina once a male has disappeared from view andwaving is no longer possible We therefore suggest that while the hypotheses are not mutually exclusivedrumming is more consistent with the redundant signal than the multiple message hypothesis Thisconclusion is further supported by the positive correlation between waving and drumming productionof both signals is seemingly governed by the same energetic mechanisms Parallel explanations for theuse of multiple signals might be common across many taxa including those that use single (eg [4445])or multiple channels of communication (eg [946]) That is multiple signals are implemented to reinforcea single aspect of sender quality

Ethics All work was undertaken with permission from the Darwin City Council (Permit No 2322876) and inaccordance with the Association for the Study of Animal BehaviourAnimal Behavior Society Guidelines for theUse of Animals in Research [47] All crabs were released after being tested and were provided with new burrowsData accessibility The dataset supporting this article has been uploaded as part of the electronic supplementary materialAuthorsrsquo contributions SLM carried out the data collection data analysis participated in the design of the study anddrafted the manuscript PRYB coordinated the study and helped draft the manuscript MJ participated in dataanalysis and helped draft the manuscript All authors gave final approval for publicationCompeting interests We have no competing interestsFunding The study was funded by an ARC Discovery Grant (DP120101427) to PRYBAcknowledgements We thank the staff at the North Australian Research Unit for their assistance Rob Magrath for helpwith acoustic analysis and Huon Clark Kecia Kerr Christina Painting and Daniella Perez for assistance in the fieldWe also thank Andrew Dunn and three anonymous reviewers for their helpful comments on the manuscript

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5 Mowles SL 2014 The physiological cost of courtshipfield cricket song results in anaerobic metabolismAnim Behav 89 39ndash43 (doi101016janbehav201312014)

6 Ord TJ Hsieh TH 2011 A highly social land-dwellingfish defends territories in a constantly fluctuating

environment Ethology 117 918ndash927 (doi101111j1439-0310201101949x)

7 Partan SR Marler P 2005 Issues in the classificationof multimodal communication signals Am Nat166 231ndash245 (doi101086431246)

8 Fusani L Day LB Canoine V Reinemann DHernandez E Schlinger BA 2007 Androgen and theelaborate courtship behavior of a tropical lekkingbird Horm Behav 51 62ndash68 (doi101016jyhbeh200608005)

9 Girard MB Kasumovic MM Elias DO 2011Multimodal courtship in the peacock spiderMaratus volans (OP-Cambridge 1874) PLoSONE 6 e25390 (doi101371journalpone0025390)

10 Girard MB Elias DO Kasumovic MM 2015 Femalepreference for multi-modal courtship multiplesignals are important for male mating success in

peacock spiders Proc R Soc B 282 20152222(doi101098rspb20152222)

11 Moslashller AP Pomiankowski A 1993 Why have birdsgot multiple sexual ornaments Behav Ecol 32167ndash176 (doi101007bf00173774)

12 Hebets EA Papaj DR 2005 Complex signal functiondeveloping a framework of testable hypothesesBehav Ecol Sociobiol 57 197ndash214 (doi101007s00265-004-0865-7)

13 Vanhooydonck B Herrel AY Van Damme R IrschickDJ 2005 Does dewlap size predict male biteperformance in Jamaican Anolis lizards FunctEcol 19 38ndash42 (doi101111j0269-8463200500940x)

14 Perry GK Levering K Girard I Garland TJr 2004Locomotor performance and social dominance inmale Anolis cristatellus Anim Behav 67 37ndash47(doi101016janbehav200302003)

15 Payne RJH Pagel M 1997 Why do animals repeat

displays Anim Behav 54 109ndash119 (doi101006anbe19960391)

16 Kotiaho JS Alatalo RV Mappes J Nielsen MGParri S Rivero A 1998 Energetic costs of size andsexual signalling in a wolf spider Proc R Soc LondB 265 2203ndash2209 (doi101098rspb19980560)

17 Parri S Alatalo RV Kotiaho JS Mappes J Rivero A2002 Sexual selection in the wolf spider Hygrolycosarubrofasciata female preference for drum durationand pulse rate Behav Ecol 13 615ndash621(doi101093beheco135615)

18 Rosenberg MS 2001 The systematics and taxonomyof fiddler crabs a phylogeny of the genus UcaJ Crust Biol 21 839ndash869 (doi10116320021975-99990176)

19 Perez DM Rosenberg MS Pie MR 2012 Theevolution of waving displays in fiddler crabs (Ucaspp Crustacea Ocypodidae) Biol J Linn Soc 106307ndash315 (doi101111j1095-8312201201860x)

20 Reaney LT 2009 Female preference for malephenotypic traits in a fiddler crab do females useabsolute or comparative evaluation Anim Behav77 139ndash143 (doi101016janbehav200809019)

21 Murai M Backwell PRY 2006 A conspicuouscourtship signal in the fiddler crab Uca perplexafemale choice based on display structure BehavEcol Sociobiol 60 736ndash741 (doi101007s00265-006-0217-x)

22 Matsumasa M Murai M 2005 Changes in bloodglucose and lactate levels of male fiddler crabseffects of aggression and claw waving Anim Behav69 569ndash577 (doi101016janbehav200406017)

23 Alatalo RV Kotiaho J Mappes J Parri S 1998 Matechoice for offspring performance major benefits orminor costs Proc R Soc Lond B 265 2297ndash2301(doi101098rspb19980574)

24 Tregenza T Simmons LW Wedell N Zuk M 2006Female preference for male courtship song and itsrole as a signal of immune function and conditionAnim Behav 72 809ndash818 (doi101016janbehav200601019)

25 Burkenroad MD 1947 Production of sound in thefiddler crab Uca pugilator Bosc with remarks on itsnocturnal and mating behavior Ecology 28458ndash462 (doi1023071931234)

26 Salmon M Atsaides SP 1968 Visual and acousticalsignaling during courtship by fiddler crabs (genusUca) Am Zool 8 623ndash639 (doi101093icb83623)

27 von Hagen HO 1984 Visual and acoustic display inUca mordax and U burgersi sibling species ofneotropical fiddler crabs II Vibration signalsBehaviour 91 204ndash228 (doi101163156853984X00281)

28 Takeshita F Murai M 2016 The vibrational signalsthat male fiddler crabs (Uca lactea) use to attractfemales into their burrows Sci Nat 103 49(doi101007s00114-016-1371-2)

29 Christy JH 1978 Adaptive significance ofreproductive cycles in the fiddler crab Uca pugilatora hypothesis Science 199 453ndash455 (doi101126science1994327453)

30 Clark HL Backwell PRY 2015 Temporal and spatialvariation in female mating preferences in a fiddlercrab Behav Ecol Sociobiol 69 1779ndash1784(doi101007s00265-015-1990-1)

31 Briffa M Elwood RW Russ JM 2003 Analysis ofmultiple aspects of a repeated signal power andrate of rapping during shell fights in hermit crabsBehav Ecol 14 74ndash79 (doi101093beheco14174)

32 Maynard Smith J Harper D 1988 The evolution ofaggression can selection generate variability PhilTrans R Soc Lond B 319 557ndash570 (doi101098rstb19880065)

33 Holman L 2012 Costs and constraints conspire toproduce honest signaling insights from an antqueen pheromone Evolution 66 2094ndash2105(doi101111j1558-5646201201603x)

34 Imafuku M Habu E Nakajima H 2001 Analysis ofwaving and sound-production display in the ghostcrab Ocypode stimpsoniMar Freshwater BehavPhysiol 34 197ndash211 (doi10108010236240109379074)

35 Quirici V Costa FG 2007 Seismic sexual signalsdesign of two sympatric burrowing tarantulaspiders frommeadows of Uruguay Eupalaestrusweijenberghi and Acanthoscurria suina (AraneaeTheraphosidae) J Arachnol 35 38ndash45(doi101636ST06-081)

36 Ryan MJ Tuttle MD Rand AS 1982 Bat predationand sexual advertisement in a Neotropical anuranAm Nat 119 136ndash139 (doi101086283899)

37 Zahavi A 1975 Mate selection a selection for ahandicap J Theor Biol 53 205ndash214 (doi1010160022-5193(75)90111-3)

38 Painting CJ Splinter W Callander S Maricic T PesoM Backwell PRY 2016 Ladies first coerced matingin a fiddler crab PLoS ONE 11 e0155707(doi101371journalpone0155707)

39 Cocroft RB De Luca P 2006 Size-frequencyrelationships in insect vibratory signals In Insectsound and communication physiology behaviorecology and evolution (eds S Drosopoulos MFClaridge) New York NY Taylor and Francis

40 Rivero A Alatalo RV Kotiaho JS Mappes J Parri S2000 Acoustic signalling in a wolf spider can signalcharacteristics predict male quality Anim Behav60 187ndash194 (doi101006anbe20001452)

41 Aicher B Tautz J 1990 Vibrational communicationin the fiddler crab Uca pugilator I Signaltransmission through the substratum J CompPhysiol A 166 345ndash353 (doi101007BF00204807)

42 Kerr KA Christy JH Joly-Lopez Z Luque J Collin RGuichard F 2014 Reproducing on time whentemperature varies shifts in the timing of courtshipby fiddler crabs PLoS ONE 9 e97593 (doi101371journalpone0097593)

43 Reaney LT Backwell PRY 2007 Temporal constraintsand female preference for burrow width in thefiddler crab Uca mjoebergi Behav Ecol Sociobiol61 1515ndash1521 (doi101007s00265-007-0383-5)

44 Lindquist ED Hetherington TE 1998 Semaphoringin an earless frog the origin of a novel visual signalAnim Cogn 1 83ndash87 (doi101007s100710050012)

45 Tokarz RR 2007 Changes in the intensity of malecourtship behavior following physical exposure ofmales to previously unfamiliar females in brownanoles (Anolis sagrei) J Herpetol 41 501ndash505(doi1016700022-1511(2007)41[501CITIOM]20CO2)

46 Takahashi M Arita H Hiraiwa-Hasegawa MHasegawa T 2008 Peahens do not prefer peacockswith more elaborate trains Anim Behav 751209ndash1219 (doi101016janbehav200710004)

47 Animal Behaviour 2012 Guidelines for thetreatment of animals in behavioural research andteaching Anim Behav 83 301ndash309 (doi101016janbehav201110031)

Introduction

Material and methods

Study site and organisms

Stimulus females

Behavioural experiments

Sprint performance experiments

Crab morphology

Measuring burrow parameters

Behavioural analyses

Acoustic analyses

Quantifying signal escalation

Statistical methods

Results

Male courtship sequence

Courtship and sprint performance

Sprint performance and courtship vigour

Sprint performance and male size

Male size and courtship vigour

Courtship escalation and sprint performance

Escalation in the rate of drumming

Acoustic properties of drumming and male size

Discussion

References

(examples in [3]) In some species males produce displays that use a single channel of communicationsuch as stridulating in crickets (eg [45]) or head-nodding in land-dwelling fish [6] In other speciesmales produce lsquomultimodalrsquo displays which are defined as lsquocomposite signals received through morethan one sensory channelrsquo [7] For example male golden-collared manakins (Manacus vitellinus) use bothbody movements and sounds in their courtship displays [8] and male peacock spiders (Maratus volans)make both distinctive movements and produce vibratory signals to court females [910]

Does the use of multiple courtship signals simply serve to confirm the information beingcommunicated (the redundant signal hypothesis) (reviews [1112]) Or do different signals advertisedifferent aspects of a malersquos quality (the multiple message hypothesis) We might assume that sendingmultiple messages involves the use of different channels of communication (eg sound and vision) butthis need not be the case For example male Anolis lizards extend their dewlaps and perform lsquopush-uprsquodisplays in territorial displays These are both visual signals but dewlap size is thought to advertise amalersquos bite force [13] while the vigour of the lsquopush-uprsquo display is assumed to signal a malersquos stamina [14]Conversely it is possible that signals that use different channels of communication may provide the sameinformation For example courtship displays often seem to be indices of stamina and this informationcan be conveyed in several ways [315] For instance in some species males make vibrational signalsthat convey information about their stamina to females (eg wolf spiders that drum on leaves [1617])whereas in other species the rate of acoustic advertisement calling provides females with informationabout a malersquos energetic reserves (eg crickets [5]) To date few studies have looked at species thatcourt using several channels of communication to ask how different signal types are related to energyexpenditure or to ask about the relative investment that males put into each type of signal Here weaddress this oversight by studying courtship in the banana fiddler crab Uca mjoebergi

Fiddler crabs genus Uca are well known for their extreme sexual dimorphism Females havetwo small feeding claws while one of the claws in males is greatly enlarged (the major claw) [18]In many fiddler crab species males court by making a repetitive waving motion with their majorclaw [19] Females prefer males with larger claws (eg U perplexa [20]) that are waved at higher rates(eg U mjoebergi [21]) Claw waving is energetically costly lactic acid levels in malesrsquo haemolymphbecome elevated when they wave presumably because of anaerobic respiration [22] However no studyhas directly linked a malersquos wave rate to associated costs If there is a positive relationship between thevigour of waving and the accumulation of energetic costs it would confirm that courtship waving is asignal of stamina [3] Such energetically costly lsquosignals of staminarsquo are likely to be important to femalesas they would reflect the ability of the male to perform other demanding activities such as sprinting toavoid predators while also indicating that the male has accrued sufficient energy reserves to expendin display thus demonstrating that he is an effective forager These are attributes with which a choosyfemale should want to provision her offspring [23] Further the ability to perform a demanding displaywell may also indicate that the male is in good condition thus preventing females from mating withdiseased or parasitized males [24]

In some fiddler crab species males additionally produce vibrational signals via rapid movements oftheir major claw which are transmitted through the ground despite the stridulating major claw makinglittle if no contact with the substrate [25ndash27] Males perform this lsquodrummingrsquo [25] vibrational displayas a female approaches the malersquos burrow [26] and even continue to drum after she follows him intothe burrow There is evidence that females prefer males that emit rapid vibrations [28] but the specificfunction of drumming has yet to be investigated Drumming may contain information not providedby the waving display (ie the multiple message hypothesis) For example the vibratory nature of thedisplay might advertise structural properties of a malersquos burrow Burrow dimensions are important toa female because she stays inside the mated malersquos burrow to incubate her eggs (see [28]) Burrowproperties affect the speed at which eggs develop into larvae which is crucial to ensure the correct timingof larval release during a nocturnal spring tide (eg [2930]) Thus drumming might allow females tochoose a male with an appropriate burrow if the acoustic properties of the drumming display permitthe female to assess the physical characteristics of the burrow Alternatively drumming might advertiseother aspects of male quality such as size (multiple message hypothesis) Larger males are likely toproduce more powerful drums as occurs with shell-rapping by hermit crabs [31] If so drummingmight be an index of male size rather than an inherently costly handicap signal [32] although indicesand handicaps are often hard to distinguish [33] (eg drumming with a larger claw might consume moreenergy) Finally drumming might reinforce information already provided by waving (redundant signalhypothesis) Vibrational displays in other taxa are energetically costly (eg wolf spiders [16]) Drummingby a male fiddler crab might augment his claw-waving display by confirming his ability to perform ademanding activity consistent with a signal of stamina

5 cm 25 cm 0 cm

control courtship

00 h 1 h 2 h

time post-display

sndash1

ndash1)

20181614121008060402

004 06 08 10 12 14 16 18

0035 0040 0045

R df p-value

mean beats per bout

r df p-value

courtship trials

control trials

ndash1)

095 105 115 125 135 145

de-escalation

static

escalation

r df p-value

2000 50 100 150 200

burrow volume (cm3)

surface 6135ndash13186 8010 0033 37 0846

rs N p-value

entrance 0112 83 0312

References

Introduction


Stimulus females



Crab morphology



Acoustic analyses


Statistical methods

Results









Discussion

References

5 cm 25 cm 0 cm

control courtship

00 h 1 h 2 h

time post-display

sndash1

ndash1)

20181614121008060402

004 06 08 10 12 14 16 18

0035 0040 0045

R df p-value

mean beats per bout

r df p-value

courtship trials

control trials

ndash1)

095 105 115 125 135 145

de-escalation

static

escalation

r df p-value

2000 50 100 150 200

burrow volume (cm3)

surface 6135ndash13186 8010 0033 37 0846

rs N p-value

entrance 0112 83 0312

References

Introduction


Stimulus females



Crab morphology



Acoustic analyses


Statistical methods

Results









Discussion

References

5 cm 25 cm 0 cm

control courtship

00 h 1 h 2 h

time post-display

sndash1

ndash1)

20181614121008060402

004 06 08 10 12 14 16 18

0035 0040 0045

R df p-value

mean beats per bout

r df p-value

courtship trials

control trials

ndash1)

095 105 115 125 135 145

de-escalation

static

escalation

r df p-value

2000 50 100 150 200

burrow volume (cm3)

surface 6135ndash13186 8010 0033 37 0846

rs N p-value

entrance 0112 83 0312

References

Introduction


Stimulus females



Crab morphology



Acoustic analyses


Statistical methods

Results









Discussion

References

5 cm 25 cm 0 cm

control courtship

00 h 1 h 2 h

time post-display

sndash1

ndash1)

20181614121008060402

004 06 08 10 12 14 16 18

0035 0040 0045

R df p-value

mean beats per bout

r df p-value

courtship trials

control trials

ndash1)

095 105 115 125 135 145

de-escalation

static

escalation

r df p-value

2000 50 100 150 200

burrow volume (cm3)

surface 6135ndash13186 8010 0033 37 0846

rs N p-value

entrance 0112 83 0312

References

Introduction


Stimulus females



Crab morphology



Acoustic analyses


Statistical methods

Results









Discussion

References

5 cm 25 cm 0 cm

control courtship

00 h 1 h 2 h

time post-display

sndash1

ndash1)

20181614121008060402

004 06 08 10 12 14 16 18

0035 0040 0045

R df p-value

mean beats per bout

r df p-value

courtship trials

control trials

ndash1)

095 105 115 125 135 145

de-escalation

static

escalation

r df p-value

2000 50 100 150 200

burrow volume (cm3)

surface 6135ndash13186 8010 0033 37 0846

rs N p-value

entrance 0112 83 0312

References

Introduction


Stimulus females



Crab morphology



Acoustic analyses


Statistical methods

Results









Discussion

References

ndash1)

20181614121008060402

004 06 08 10 12 14 16 18

0035 0040 0045

R df p-value

mean beats per bout

r df p-value

courtship trials

control trials

ndash1)

095 105 115 125 135 145

de-escalation

static

escalation

r df p-value

2000 50 100 150 200

burrow volume (cm3)

surface 6135ndash13186 8010 0033 37 0846

rs N p-value

entrance 0112 83 0312

References

Introduction


Stimulus females



Crab morphology



Acoustic analyses


Statistical methods

Results









Discussion

References

R df p-value

mean beats per bout

r df p-value

courtship trials

control trials

ndash1)

095 105 115 125 135 145

de-escalation

static

escalation

r df p-value

2000 50 100 150 200

burrow volume (cm3)

surface 6135ndash13186 8010 0033 37 0846

rs N p-value

entrance 0112 83 0312

References

Introduction


Stimulus females



Crab morphology



Acoustic analyses


Statistical methods

Results









Discussion

References

ndash1)

095 105 115 125 135 145

de-escalation

static

escalation

r df p-value

2000 50 100 150 200

burrow volume (cm3)

surface 6135ndash13186 8010 0033 37 0846

rs N p-value

entrance 0112 83 0312

References

Introduction


Stimulus females



Crab morphology



Acoustic analyses


Statistical methods

Results









Discussion

References

2000 50 100 150 200

burrow volume (cm3)

surface 6135ndash13186 8010 0033 37 0846

rs N p-value

entrance 0112 83 0312

References

Introduction


Stimulus females



Crab morphology



Acoustic analyses


Statistical methods

Results









Discussion

References

References

Introduction


Stimulus females



Crab morphology



Acoustic analyses


Statistical methods

Results









Discussion

References

References

Introduction


Stimulus females



Crab morphology



Acoustic analyses


Statistical methods

Results









Discussion

References

Introduction


Stimulus females



Crab morphology



Acoustic analyses


Statistical methods

Results









Discussion

References

Documents

Multimodalcommunication incourtingfiddlercrabs · 2017-05-02 · drumming with in situ performance (sprint speed) trials to test whether ﬁne-scale aspects of waving and/or drumming