Behaviour of juvenile mud crabs Scylla serrata in aquaculture: Response to odours of moulting or injured crabs

Applied Animal Behaviour Science 121 (2009) 63–73

Behaviour of juvenile mud crabs Scylla serrata in aquaculture: Responseto odours of moulting or injured crabs

David Wall a, Brian Paterson b,*, Ram Mohan a

a The School of Integrative Biology, The University of Queensland, Queensland 4072, Australiab Bribie Island Aquaculture Research Centre, Queensland Department of Employment, Economic Development and Innovation, PO Box 2066 Bribie Island,

Queensland 4507, Australia

A R T I C L E I N F O

Article history:

Accepted 22 August 2009

Available online 9 September 2009

Keywords:

Aquaculture

Cannibalism

Crustacean

Moulting

Olfactory system

Sex influence

Body size

A B S T R A C T

Behaviour of juvenile mud crabs, Scylla serrata (70–90 mm carapace width, CW) were

observed in response to odours of moulting and injured conspecifics and food (pilchard)

under controlled flow conditions using bioassay technique. This study was undertaken to

better understand the role that chemical cues have in mediating the attraction of cannibal

crabs to moulting crabs in an aquaculture growout facility and thus aid in more successful

production. In response to moult odour juvenile S. serrata spent 5.6� 1.9% of the time in

locomotion but this did not differ significantly (P> 0.05) from that of control odours

(seawater, 2.6� 1.2%), however a tactile response was observed for moult odour not seen in

controls. Juveniles exposed to the odour of injured conspecifics (12.2� 2.3% of time in

locomotion) and to food (22.7� 3.1%) differed significantly from the seawater control

(P< 0.05). The possibility that the active agent in moult water is relatively dilute was

considered, however varying concentrations of food and crushed conspecific odour failed to

demonstrate concentration dependant behavioural results. Variation in the form of size

(carapace width) and sex was revealed, so too was preliminary evidence of behavioural

differences between crab hatchings. For example, larger crabs (around 80 mm CW) increased

tactile investigation of the odour inlet pipe in response to the crab-based odours of moulting

(3.5� 1.7% of the time) and injured conspecifics (2.6� 1.0%), though response to food

remained constant over all sizes (�10.0% of the time). In another experiment, larger female

crabs maintained a high frequency of tactile response to the odour of injured conspecifics. In

males, the response was attenuated in larger individuals. Despite no differences being found

between moult odour and controls some evidence exists to suggest that a small proportion of

crabs were responding to the moult odour and that this still has the potential to cause a

dramatic cumulative reduction in growout survival. Variation in size and subsequent

behaviour of individuals poses the question of whether behaviour contributes to growth rate

and might be a focus of genetic selection for more uniform growth.

Crown Copyright � 2009 Published by Elsevier B.V. All rights reserved.

Contents lists available at ScienceDirect

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1. Introduction

In the wild the mud crab, Scylla serrata, is widelydistributed throughout the Indo-Pacific region and withinAustralia its marketability as a high value seafood productmakes it a very appealing candidate as a profitable primaryindustry (Hill, 1982).

* Corresponding author.

E-mail address: [email protected] (B. Paterson).

0168-1591/$ – see front matter . Crown Copyright � 2009 Published by Elsevie

doi:10.1016/j.applanim.2009.08.005

Over the last 50 years the culture of Portunid crabs hasundergone an estimated seven-fold increase in production(Keenan, 2003). In order to aid in development of Portunidculture many aspects of production and biology have beeninvestigated. The greatest constraint to large scale commu-nal production is cannibalism in juvenile mud crabs (Mannand Paterson, 2003) as it is believed that cannibalism of softpost moult crabs has a strong chemically mediatedcomponent though no formal studies of chemoreceptionin S. serrata have yet been undertaken (Keenan, 1999).

r B.V. All rights reserved.

mailto:[email protected]

http://www.sciencedirect.com/science/journal/01681591

http://dx.doi.org/10.1016/j.applanim.2009.08.005

D. Wall et al. / Applied Animal Behaviour Science 121 (2009) 63–7364

Chemical stimuli are often considered to be some of themost primitive, ancient and yet essential sources ofinformation for crustaceans (Weissburg and Dusenbery,2002). As such the ability of crustaceans to detectchemicals in the environment is important for survival(Kozlowski et al., 2003) and may be the primary factor inmediating an appropriate response (Adams and Moore,2003). Crustaceans use chemical cues to identify andlocalise food and prey (Moore et al., 1991; Weissburg andZimmer-faust, 1994; Leonard et al., 1999), mates (Seifert,1982; Dunham and Oh, 1992) and shelter (Tamburri et al.,1996); and recognise the odour of injured conspecifics(Gherardi et al., 2002; Diaz et al., 2003; Hazlett, 2004).

Crabs and other crustaceans posses a number ofattributes that allow for the successful study of theirbehaviour. The generally large and robust nature of decapodcrustaceans, plus their simple yet distinct behaviours,allows accurate quantification of data (Huntingford et al.,1995). Investigations of the attraction to a moultingcrustacean or moult odour have in the past had strongecological context, focusing primarily on the role of moultodour in mating and courtship in mature animals (Seifert,1982; Hardege et al., 2002). As a result, the behaviour ofimmature crustaceans to moult odour has not been studied.

A second odour relevant to aquaculture, the odour of aninjured conspecific is often used to simulate a predationevent in chemosensory studies (Diaz et al., 2003; Mirza andChivers, 2003). Though often considered an ‘alarm’ or‘alert’ odour (Gherardi et al., 2002) different species ofcrabs have been observed to both retreat (Diaz et al., 2003)and enhance feeding type behaviours when exposed tocrushed conspecific odour (Zhou and Shirley, 1997).

A behavioural bio-assay of a crab’s responses to odoursmust not only involve a rigorous experimental approach(Dunham and Oh, 1992), it must also consider the impactof relevant additional factors. The role that size plays inaggressive interactions between individuals has often beenlinked to studies of cannibalism. In general, larger crabs areobserved to be more successful in aggressive encounters(Huntingford et al., 1995).

Studies observing actual cannibalistic acts have alsorecognised that size is an important factor (Dutil et al.,1997; Marshall et al., 2005). Initial examination of theliterature also suggests that the behavioural responseobserved from food and conspecific odour may be in partattributed to the potency of the odours themselves (Zhouand Shirley, 1997). As such, the effect of flux orconcentration is an important consideration when avariety of odours are compared. For most odours thathave been examined however, the effect of concentrationis often a simple relationship (but not linear), withincreases in concentration subsequently increasing beha-vioural intensity (Keller and Weissburg, 2004; Steulletet al., 2001).

Here, we report on the response of juvenile mud crab, S.

serrata, using a behavioural bioassay technique. The aimsof the study were to investigate the responses displayed bycrabs when exposed to odours representing food, injuredand moulting conspecifics. The effect of concentration wasalso considered as a factor after initial results demon-strated far higher responses to odours of food and injured

conspecific and these odours were subsequently diluted.Finally to examine the potential for variability of individualresponse, repeat tests were carried after a 7-day interval.

2. Materials and methods

2.1. Experimental site

This series of experiments were conducted at theQueensland Department of Employment, Economic Devel-opment and Innovation, Bribie Island AquacultureResearch Centre (BIARC), approximately 70 km north ofBrisbane, Australia.

2.2. Experimental animals

Juvenile mud crabs, S. serrata, were sourced fromexperimental cohorts produced at the BIARC crab hatchery.Experiments 1 and 2 used 64 animals each from the samecohort and Experiment 3 used 32 animals from a differentsibling cohort. Similar sizes and numbers of males (n = 31)and females (n = 33) were used in Experiment 1 and 2. Forexperiment 3, crabs were used at the sex ratio current forthe cohort at harvest (11 females and 22 males). Thejuvenile crabs were housed in a cellular system similar tothat used by commercial aquaculture facilities (Patersonet al., 2007). While in this system crabs were fed twicedaily, once in the morning and once in the afternoon, on acommercial kuruma prawn diet (Ebistar, Higashimaru,Japan). A profile for each crab was created prior to anysingle experiment similar to that of Marshall et al. (2005),recording parameters such as moult stage, carapace width(CW), weight, injuries and sex and it was expected thatthese parameters would remain consistent until the nextmoult (Heasman, 1980).

The CW of experimental crabs for Experiment 1 was53–88 mm (72� 7.3 mm) (mean� S.D), instar range 11–13;for Experiment 2 was 67–94 mm (80� 6.5 mm), instars 12–13; and Experiment 3 was 65–86 mm (74� 7 mm), instars12–13. For the instar 12 and 13 juveniles used in Experiment2, female CW (82.4� 6.3 mm, n = 33) was already signifi-cantly different (t = 2.22, P< 0.05, d.f. = 62) from male CW(78.9� 6.3 mm, n = 31). For Experiments 1 and 3, males andfemales still had the same CW (t = 0.56, d.f. = 62 and t = 0.33,d.f. = 31 respectively, P> 0.05). All animals were sexuallyimmature, but the dimorphism in carapace growth seen inExperiment 2 continues in later instars as the males investincreasing weight into their claws (Heasman, 1980).

In an attempt to standardise experimental animals onlythose in intermoult phase and with no visible injury (e.g.limb loss) were used. Crabs that were selected forcollection of moult water were visually, mechanicallyand chemically isolated from the cellular system andhoused in 4 L buckets for 1–2 days. Seawater wasexchanged in the morning if the crab failed to moult theprevious night.

2.3. Experimental environment

Testing was conducted in a room within BIARC inraceways containing four, isolated lanes and having a total

Table 1

Mud crab behaviours recorded in this study.

Behaviour Definition and/or explanation of behaviour

Resting Normal stance, not interacting or displaying any

other observable behaviour.

Locomotion Walking (forward and lateral) and swimming

(lateral, backwards and forwards) and

combination of both.

Chela display Reaching upwards and spreading the chelae

greater than parallel while in a stationary position.

Employed to maximise chemo- and tactile sensory

appendages and increase apparent size.

Tactile

investigation

Use of chelipeds to inspect source of stimulus

(i.e. grabbing at the inlet pipe).

Feeding One or both chelae and/or maxillipeds move

toward mouth (‘‘Triturition’’) as if bringing food to

the mouth.

Modified from Eales (1972), Zhou and Shirley (1997), Clark et al. (1999),

Ristvey and Rebach (1999), Hazlett (2004).

D. Wall et al. / Applied Animal Behaviour Science 121 (2009) 63–73 65

dimension of 800 mm� 610 mm (single lane 200 mm� 610 mm). Each lane was fitted with 4 mm inlet pipesat a depth of 40 mm and an overflow pipe at a depth of80 mm to regulate water depth. Overflow water flowed outof the system to waste. Each lane was set up to deliverwater through a gravity flow system sourced from a 4 Lcontainer using 4 mm plastic piping at a flow rate of 60 mL/min (Keller and Weissburg, 2004) regulated using 4 mmvalves. No substrate was provided in the raceways to avoidthe introduction of chemical cues other than those beingtested (Salierno et al., 2003). Each raceway was enclosed ina black plastic tent to minimise disturbance to crabs oncethey had been placed into the raceways (Marshall et al.,2005). Experiments were carried out in darkness under redlight illumination to improve quality of video recordings, atechnique that has been reported to cause no disturbancein other decapod crustaceans (Gribble, 1988; Smith andSumpton, 1989; Marshall et al., 2005).

2.4. Odour preparation

2.4.1. Controls

Seawater was used from BIARC reservoirs which hadpreviously been sourced from inshore oceanic waters andwas then further passed through a 1 mm activated carbonfilter to remove other possible odours already present inthe seawater (Chiussi and Diaz, 2002). The header watertank was provided with air stones, maintaining oxygen at84� 5.9% saturation (mean� S.D.). Temperature was main-tained in the header tank using a thermostat regulatedimmersion heater and averaged 24� 0.65 8C. Salinity and pHwere recorded at 35� 0.66% and 8.21� 0.14 respectively.This water then served as the control and was mixed withstimuli to achieve treatment odour solutions.

2.4.2. Food odour

One frozen pilchard (54.2� 4.9 g, mean� S.D., N = 8) wasplaced in 1 L of seawater, left to defrost and then crushed in astandardised manner using the base of a large beaker. Thecrushing action involved pressing the base of the beaker hardonto the pilchard and rotating the beaker. This food solutionwas filtered to remove solids and then diluted in the headertanks at a concentration of 50 mL/L for Experiment 1; and 50,17.5, 6 mL/L for Experiment 2. Food odour was prepared fresheach day.

2.4.3. Conspecific odour

Conspecific odour was prepared by firstly anaesthetis-ing one medium sized experimental crab (52.1� 9.5 g,mean� S.D., N = 12) at 4 8C for 20 min in 1 L of seawater andthen crushing, filtering and preparing solutions in the samemanner and concentrations as that used for the food odour.Conspecific odour was prepared fresh each day.

2.4.4. Moult odour

S. serrata predicted to moult within days were isolatedin containers containing 1 L of fresh seawater and leftovernight to moult. Water in which crabs had undergoneecdysis within the last 24 h was then filtered to removesolids and immediately frozen at �20 8C for storage. Moultwater was defrosted to room temperature prior to use and

was diluted to a concentration of 250 mL/L in header tanks.This concentration was chosen as the maximum that couldbe practically used and was somewhat based upon thedifficulties associated with collecting moult water.

2.5. Treatment procedure and data collection

Both experimental animals and timing experimentaltreatments were assigned randomly using a randomnumber table (Zar, 1974) and crabs for experiments 1and 2 were only used once throughout the investigation(Hughes and Seed, 1995). Crabs were removed from theholding system and mechanically, chemically and visuallyisolated for 1 h in the experimental raceways. Flow wasinitiated and crabs were allowed to acclimate to normalseawater for a further 15 min at which time recordingstarted. Pilot observations showed that the crabs rapidlyadopted ‘‘resting’’ behaviour in the raceway (Table 1). Afteracclimation, odours were added to header tanks at theappropriate concentrations and mixed thoroughly andrecordings were continued for a further 20 min. Uponcompletion of any single trial, crabs were returned to thecellular system and the experimental raceways werewiped over with a dilute chlorine solution before beingrinsed with copious amounts of fresh water. The odoursassigned to each lane were changed between recordingperiods to avoid positional effects and to enable blindscoring of the videos.

A total of three experiments were conducted in thisinvestigation and these were done in a sequential manner.Experiment 1 was conducted to test the differences inattractiveness between food, crushed conspecific andmoult odours. Next, to see whether diluting odours wouldreduce response (and explain the results of moult water inExperiment 1), the effects of concentration were examinedusing food and crushed conspecific odours. Finally in orderto examine the role of individual variation as well as theeffect repeat exposure has on behaviour, crabs were testingusing crushed conspecific odour with a 1-week intervalbetween exposures.

Recordings were be made in real-time using WV-BP130and WV-BP330 video surveillance cameras (PanasonicCorporation, Osaka, Japan) mounted over the raceways


(Weissburg and Zimmer-faust, 1994; Moody, 2003;Marshall et al., 2005) and recorded on VHS using TEACMV-6000 (TEAC Corporation, Tokyo, Japan) and LGAC450W (LG Electronics, Seoul, Korea) video recorders.Videos were viewed and data were collected by identifyingthe different behaviours of the crabs using three differentmethods: (1) latency of response of behaviour, (2) totalcount of a behaviour, and (3) by classifying behaviour at10 s intervals over the 20 min observational period. Thebehaviours recorded were those documented by similarstudies on decapod crustaceans, modified slightly tocompensate for the lack of actual food particles. Beha-viours included resting and locomotion (Eales, 1972);chela displays (Eales, 1972; Clark et al., 1999; Ristvey andRebach, 1999); tactile investigations (Hazlett, 2004) andfeeding (Eales, 1972; Zhou and Shirley, 1997) (Table 1).

2.6. Data analysis

A number of different approaches were used to analysedata collected in this investigation. Firstly, the data forlatency of response was fitted to a normal GeneralisedLinear Model (GLM, McCullagh and Nelder, 1989) becauseneither log normal nor negative binomial were superior tothis model when the distribution of residuals wasexamined. The analysis was ‘‘conditional’’ in that if theevent did not occur then no data could be analysed for thatindividual. Secondly, count data for the total number oftimes a behaviour occurred used a GLM with a Poissonerror distribution and log link transformation. Finally abinomial GLM using logit link function was employed toanalyse the proportional data where behaviour was scoredat 10-s intervals. LSD comparisons between means wereconducted for all analysis methods on those factors thatwere shown to be significant after initial accumulatedanalysis of variance (latency data) or deviance (total countsand proportional data) tests. Data are plotted or tabulatedas means� S.E. Interaction tables were used to furtherexplore significant interactions. All analyses were performedusing Genstat release 8.1 (Lawes Agricultural Trust,Rothamsted Experimental Station).

The concentration experiments (Experiment 2) wereanalysed by individual treatments (the different dilutionsof food and crushed conspecific odours as well as controlodours) rather than by a block design as the treatmentswere dilution of different raw extracts rather than knownconcentrations. There was no significant difference foundbetween controls for each odour treatment and they weresubsequently pooled in analysis. The paucity of beha-vioural response overall in Experiment 3 made analysisof data by all methods employed in both Experiments

Table 2

Interaction table (Carapace width (=CW)�Odour) showing means (�S.E.) of th

response to different odours in Experiment 1.

CW (mm) Treatment

Control Crushed consp

60 0.010� 0.009 0.001� 0.001

70 0.002� 0.003 0.006� 0.004

80 0.0001� 0.001 0.026� 0.011

1 and 2 not generally possible. Proportion of time spent inlocomotion was the only suitable analysis.

3. Results

3.1. Experiment 1—effects of food, crushed conspecific and

moult odours on S. serrata behaviour

3.1.1. Proportional data

Proportional data revealed a very highly significanteffect of treatment in the time spent at rest, locomotion,chela displays, tactile investigation and feeding (Table 2,Fig. 1). LSD testing revealed that for the proportions of allbehaviours moult odour was never significantly differentfrom seawater controls (Fig. 1). Responses to odours ofcrushed conspecific and food were often significantlydifferent from that of moult and control odours; as wellas being different from each other (Fig. 1). The proportionof time crabs spent feeding did not differ significantlybetween odours. In general the pattern of time spentdisplaying any given behaviour showed food> crushedconspecific>moult> control and not unexpectedly theresting response was the reverse of the locomotionresponse.

For locomotion and chela displays, a significantodour� CW interaction was found (Table 3). The timedevoted to these behaviours in response to crab-basedodours increased at larger CW, while food displayed thesame proportion of behaviours for all crab sizes (e.g. forchela display, Table 3). CW had a significant effect duringinvestigative and feeding behaviours (Table 3). The largercrabs increased their proportion of tactile behaviours andreduced their time spent feeding (Fig. 2).

3.1.2. Event count

Treatment was shown to be significant for the countsfor all behaviours recorded (Table 3) and, because itmirrored the outcome of the proportional data above, willnot be examined in detail. LSD testing demonstratedsimilar results to that of proportional data and again nodifferences between moult odour and control wereobserved (Table 4). Frequency of chela display and tactileinvestigation differed significantly between food andconspecific and between food and moult odours respec-tively (Table 4).

3.1.3. Latency of response

Response latency of all behaviours were significantlyaffected by the odours tested (Table 3). The latency ofresponse to moult odour was not significantly faster thanthat of the controls (Fig. 3). Despite this result, a tactile

e proportion of time that juvenile mud crabs engaged in chela displays in

ecific Food Moult

0.103� 0.038 0.002� 0.003

0.103� 0.019 0.009� 0.006

0.103� 0.024 0.035� 0.017

Fig. 1. Means� S.E of proportion of time juvenile S. serrata engaged in different behaviours in response to different odours. Different letters represent significant

differences by LSD testing (P< 0.05), N = 8.


response was observed using moult odours whereascrabs exposed to control seawater never demonstratedtactile or feeding responses (Fig. 3). Overall food odourelicited the fastest response latency and this was signi-ficantly quicker than crushed conspecific for all threebehaviours (Fig. 3)

3.2. Experiment 2—effect of dilution of food and crushed

conspecific odour on S. serrata behaviour

3.2.1. Proportional data

A significant effect of treatment was found in theproportion of time crabs spent displaying the behaviours

Table 3

Summaries of accumulated analysis of variances from the Generalised

Linear Models showing effect of different odours (treatment) and in some

cases carapace width (CW) on juvenile mud crab behaviours in

Experiment 1.

Data type and behaviour d.f. Statistic:

Deviance ratio

P

Proportion of time

Chela displays

Treatment 3,63 17.23 <0.001

CW 1,63 1.49 0.227

CW� Treatment 3,63 3.19 0.030

Feeding

Treatment 3,63 16.23 <0.001

CW 1,63 6.18 0.016

Locomotion

Treatment 3,63 13.96 <0.001

CW 1,63 0.22 0.641

CW� Treatment 3,63 3.93 0.013

Resting

Treatment 3,63 22.69 <0.001

Tactile investigation

Treatment 3,63 29.39 <0.001

CW 1,63 4.64 0.035


Deviance ratio

P

Number of events

Chela displays

Treatment 3,63 29.15 <0.001

Feeding

Treatment 3,63 24.49 <0.001


Treatment 3,63 26.22 <0.001

CW 1,63 3.70 0.059

Data type and behaviour d.f. Statistic: F P

Average latency

Chela displays

Treatment 3,26 10.12 <0.001

CW 1,26 4.02 0.059

CW� Treatment 3,26 3.16 0.048

Feeding

Treatment 1,18 5.61 0.030


Treatment 2,27 4.79 0.017

Crabs that did not show the particular behaviour where excluded from

the latency analysis (note the change in treatment d.f., e.g. seawater and

moult-water treatments did not elicit feeding responses).

Fig. 3. Means � S.E. of latency of response of juvenile S. serrata exposed to

different odours. Different letters represent significant differences by LSD

testing (P< 0.05). *Behaviour not recorded within observation period.

N = 0–8.

Fig. 2. Means� S.E. of proportion of time that juvenile S. serrata of different

carapace widths (CW) engaged in tactile and feeding behaviour.


recorded (Table 5). LSD testing showed that apart fromchela displays and feeding, significant differences wereoften found between control and food or crushedconspecific odours (Table 6) and, as this result is similarto the result of Experiment 1, will not be examined indetail. Dilution of food or conspecific extract did notsystematically decrease or increase the proportion of timespent displaying any particular behaviour.

Some behaviour variation was explained by CW and sex(Table 5). Females were found to spend a significantlygreater proportion of time displaying investigative beha-viours (0.087� 0.01) (mean� S.E.) when compared to males(0.043� 0.01). CW was also shown to significantly affect theproportion of time spent feeding and was included in acomplex interaction with treatment from which it is difficultto drawn generalisations (Table 5).

3.2.2. Event count

The total score of behaviours demonstrated a signifi-cant effect of treatment for chela display, tactile investiga-tion and feeding (Table 5). LSD testing revealed significantdifferences in frequency of chela display and tactileinvestigation behaviour between controls and varioustreatments (Table 6), with tactile investigation in dilutedcrushed conspecific extract indicating a possible concen-tration dependent effect. However, again, sex and sizevariation significantly influenced the responses of indivi-duals (Table 5). Females (3.15� 0.48 events) again dis-played significantly more tactile investigations than males(1.57� 0.31 events). This was coupled with significantinteractions between treatment and sex as well as betweensex and CW (Table 5). The response of larger males decreasedto 1.1� 0.5 tactile events, while larger females sustained arate of 4.2� 2.3 events during observations. The role of sex intactile investigations was not seen in all treatments; therewas an attenuated response of males to the crushedconspecific odour (Fig. 4). Females and males displayed avery similar number of tactile events to food odour at allconcentrations (Fig. 4).

3.2.3. Latency of response

Latency to display a behaviour showed no significanteffect of treatment for chela display, tactile investigation or

Table 4

The number of times (means� S.E.) juvenile mud crabs displayed each behaviour in response to odour treatments in Experiment 1.

Behaviour Treatment

Control Crushed conspecific Food Moult

Chela displays 0.19� 0.15a 1.00� 0.35a 6.19� 0.88b 0.38� 0.22a

Feeding 0.00� 0.00ab 1.06� 0.26ab 2.06� 0.36b 0.00� 0.00a

Tact. Invest. 0.00� 0.00abc 2.01� 0.49b 5.48� 0.84c 0.75� 0.31a

In each row, means with the same postscript are not significantly different at 5%.

Table 5

Summaries of accumulated analysis of variances from the Generalised

Linear Models showing effect of dilutions of pilchard and crushed

conspecific odours (treatment) and in some cases carapace width (CW)

and sex on juvenile mud crab behaviours in Experiment 2.


Deviance ratio

P

Proportion of time

Chela Display

Treatment 6,63 2.58 0.028

Feeding

Treatment 6,63 6.79 <0.001

CW 1,63 9.44 0.003

Treatment� CW 6,63 3.89 0.003

Locomotion

Treatment 6,63 7.91 <0.001

Resting

Treatment 6,63 4.92 <0.001


Treatment 6,63 5.65 <0.001

Sex 1,63 6.21 0.016


Deviance ratio

P

Number of events

Chela Display

Treatment 6,63 3.93 0.002

Feeding

Treatment 6,63 6.99 <0.001


Treatment 6,63 9.08 <0.001

CW 1,63 2.26 0.140

Sex 1,63 4.93 0.032

Treatment� CW 6,63 0.70 0.652

Treatment� Sex 6,63 2.90 0.018

Data type and behaviour d.f. Statistic: F P

Average latency

Chela Display

Treatment 5,32 1.60 0.188

Feeding

Treatment 5,32 0.33 0.888


Treatment 6,36 0.54 0.774

CW 1,36 6.10 0.020

Crabs that did not respond to the odour where excluded from the latency

analysis.


feeding behaviours (Table 5). CW significantly influencedthe tactile response. Larger (90 mm CW) crabs respondedfaster (65.6� 73.7 s) than smaller (70 mm CW) crabs(405.5� 85.9 s).

3.3. Experiment 3—Repeatability of individual response of

S. serrata

A large amount of variation was discovered withsignificantly more time devoted to locomotion in thesecond week of testing (Table 7). A weak correlation wasfound between weeks 1 and 2 (r = 0.35) and Fig. 5illustrates this variation in comparison to the line ofequilibrium that would denote an equal response eachweek. A significant effect of carapace width was observed(Table 7) with larger crabs spending proportionately lesstime moving around. In general this result is the oppositeof that seen in Experiments 1 and 2. Although treatmentalone was not significant, there was a significant interac-tion of treatment and carapace width (Table 7). Bothcrushed conspecific and seawater treatments displayingreduced locomotion in larger crabs though to differentdegrees.

4. Discussion

We have demonstrated that the odour of a moultingmud crab did not have a statistically significant effect onbehaviour of conspecifics. Still, the fact that crabs persistedwith tactile response to moult odour but not to theseawater control (Fig. 3) suggests that their behaviour isnot entirely random and so the concentration effect wasconsidered; perhaps particular behaviours in these crabsare harder to quantify at lower concentrations. However,reducing the concentration of other odours, representingfood and injured conspecifics, had no measurable effect onthe response of crabs to those odours though of coursemore extreme dilutions might have eliminated theresponse. If these results can be extended to the farmsituation it seems safer to conclude that there is noevidence for a widespread role for moult odour inbehaviour of juvenile S. serrata. Video studies can onlyreturn results within the resolution of the equipment used;no significant response in gross behaviour does notnecessarily mean no micro-behaviours occurred inresponse to moult odour.

Caution is also required when using this data tointerpret the significant difference in ‘‘attractiveness’’ ofthe food and crushed-conspecific odours. The odoursproduced here are relatively realistic in a farmingcontext. The powerful claws of Scylla spp. are designedto crush the shells of crustaceans and molluscs whenfeeding and their diet is also supplemented with so-called ‘‘trash fish’’ in aquaculture (Hill, 1976; Christen-sen et al., 2004). However, even with the standardisedodour production method used here, any innatedifferences in attractiveness of components or their

Table 6

Proportions of time (means� S.E.) juvenile mud crabs spent displaying particular behaviours following exposure to different dilutions of the crushed conspecific

and food odours in Experiment 2.

Statistic and behaviour Control Crushed conspecific Food

6 mL/L 17.5 mL/L 50 mL/L 6 mL/L 17.5 mL/L 50 mL/L

Proportion of time

Chela displ. 0.028� 0.010ax 0.014� 0.010a 0.001� 0.003a 0.018� 0.011a 0.049� 0.018x 0.038� 0.017x 0.060� 0.020x

Feeding 0.000� 0.000ax 0.023� 0.015a 0.016� 0.012a 0.030� 0.017a 0.071� 0.022x 0.066� 0.019x 0.038� 0.017x

Locomotion 0.052� 0.013ax 0.065� 0.020a 0.087� 0.023b 0.069� 0.020a 0.165� 0.030y 0.241� 0.035y 0.150� 0.029y

Resting 0.909� 0.033ax 0.852� 0.058a 0.731� 0.072a 0.777� 0.068a 0.560� 0.081y 0.555� 0.081y 0.666� 0.077y

Tact.invest. 0.008� 0.001ax 0.027� 0.016a 0.108� 0.030b 0.065� 0.024b 0.139� 0.033y 0.080� 0.026y 0.091� 0.032y

Number of events

Chela displ. 1.19� 0.43ax 0.75� 0.48a 0.13� 0.19a 1.375� 0.65a 3.13� 0.99y 4.00� 1.12y 2.88� 0.95x

Feeding 0.00� 0.00ax 1.63� 0.61a 1.88� 0.66a 1.75� 0.64a 3.50� 0.90x 3.38� 0.88x 2.25� 0.72x

Tact.invest. 0.19� 0.16ax 1.88� 0.68b 2.49� 0.86a 2.76� 0.82a 2.87� 0.88y 4.31� 0.98y 4.42� 1.21y

Average latency (s)

Chela displ. 452� 112 80� 185 86� 265 340� 194 221� 101 100� 99 270� 93

Feeding – 153� 188 359� 163 316� 163 345� 115 325� 115 186� 133

Tact.invest. 174� 174 130� 141 363� 123 109� 124 287� 87 180� 87 215� 87

Crabs that did not respond to the odour where excluded from the latency analysis. Responses to different odours are not compared. In each row, means with

the same postscript are not significantly different at 5%.


concentration are complicated by the stark visceraldifferences between fish and crabs.

The food/pilchard treatment was used here primarily asa positive control, to demonstrate that the experimentalconditions were not hindering the animal’s responses toodours. Still, this experiment was conducted in alaboratory under controlled conditions, so while we havedemonstrated responses to odours, obviously the parti-cular rates or levels of responses may alter undercircumstances that are the subject of further research.As discussed below, the roles of size and sex effects need tobe explored further, as does the possibility that aqua-cultured crabs ‘‘learn’’ that conspecifics are food.

Larger crabs of the first cohort used demonstratedhigher levels of behaviour (especially tactile investigation)and in one experiment females in particular respondedactively to the odour of an injured conspecific, which mayhave important practical implications. The possible geneticcause of the size effect needs to investigated in more depth,particularly in light of conflicting results showing a largeamount of individual variation as well as differences whenoffspring from the second cohort were used.

Fig. 4. Means� S.E of the number of times juvenile female and male S.

serrata display tactile investigation behaviours in response to food and

crushed conspecific odour. N = 8.

The use of moult odour in chemosensory investigation,has, in the past been restricted to investigations of sexuallymature crabs examining courtship and mating behaviours(Seifert, 1982) in response to sex pheromones (Bamber andNaylor, 1995). Our investigation is unique in the fact itmeasures the behaviour of juvenile crabs in response tomoult odour and as such direct comparison between otherspecies is not possible. In a non-crab species, the juvenilemale crayfish, Orconectes rusticus, is able to distinguish theodour of conspecific moulting male, spending significantmore time in the presence of these signals than control orintermoult male water (Adams and Moore, 2003).

In comparison to moult odours, the effect of cannibal-ism (anecdotally claimed to be mediated by moult odours)in juvenile crabs is well investigated and this phenomenonhas been documented in a number of species. A study ofthe blue swimmer crab, Portunus pelagicus, showedsignificantly more mortality immediately preceding(34%) and proceeding (54%) the moult. The ecdysis stageis expected to be associated with the greatest amount ofmoult odour (Marshall et al., 2005). It has been proposedthat changes in behaviour pre-ecdysis and the presence ofsoft vulnerable bodies after moulting are responsible forthis increase in cannibalism (Marshall et al., 2005), though

Table 7

Summary of the accumulated analysis of variance from the Generalised

Linear Model for proportional data showing effect of control and crushed

conspecific odour (treatment), week of observation and carapace width

(CW) on juvenile mud crab behaviours in Experiment 3.

d.f. Deviance ratio P

Treatment 1 1.29 0.262

Week 1 4.07 0.048

CW 1 5.12 0.028

Treatment�Week 1 0.44 0.509

Treatment� CW 1 4.29 0.043

Week� CW 1 0.19 0.662

Total 62

Fig. 5. Variation in the proportion of time individual juvenile S. serrata

from the second cohort spent in locomotion in response to crushed

conspecific odour on two occasions timed a week apart. The plotted line

describes the case where individual response is the same on both

occasions.


in environments that are visually depleted, chemicaldetection remains a potential option. Similarly studies ofthe blue crab, Callinectes sapidus, have shown cannibalismin relation to moulting even when fed to satiation(Moksnes et al., 1997). Survival rates as low as 5.7%(average 10.4%) over a range of stocking densities formegalopae grown to instar 6 have also been recorded(Zmora et al., 2005). In direct contrast to the resultsobtained for P. pelagicus and C. sapidus, Sainte-Marie andLafrance (2002) found that moulting crabs were notparticularly vulnerable to cannibalism in the snow crabChionoecetes opilio.

The odour of a crushed conspecific demonstratedstrong locomotion, tactile and feeding responses frommud crabs in this investigation and has in the literaturebeen classified as an ‘alarm’ or ‘alert’ odour (Gherardiet al., 2002), possibly warning nearby conspecifics of apredation event and allowing them to modify theirbehaviours appropriately (Mirza and Chivers, 2003). Thisis illustrated in a study of C. sapidus (Diaz et al., 2003)showing avoidance responses when exposed to crushedconspecific. Investigation of Western Australian marron,Cherax tenuimanus, and the yabby, Cherax albidus, on theother hand found that crushed conspecific did elicit aninterested response but that this response was signifi-cantly weaker than that of food (Gherardi et al., 2002) (likeour study found). Despite being classified as an ‘alerting’odour, the odour of an injured conspecific has beendemonstrated to show stronger feeding responses thanfood odours in the red king crab, Paralithodes camtscha-

ticus (Zhou and Shirley, 1997).Even when the ‘‘feeding/alarm’’ odour is diluted,

individual differences (in sex and body size) rather thanodour concentration seem to be the major source ofvariation. Perhaps individual variation is also responsiblefor the marginal response to moult odour. It must also be

recognized that the difficulties associated with collectingsufficient quantities of moult odour in S. serrata, will makefurther investigation into the response of crabs to thisodour problematic at best. Our methods of collectingmoult odour and subsequent freezing for storage couldhave affected the stability of the odour, though similarmethods have been used successfully in a number of otherstudies (Finelli et al., 2000; Adams and Moore, 2003).Recent studies of the shelf-life of the ‘‘alarm’’ odour of afreshwater crayfish show that it degrades quickly anddoes not survive freezing (Acquistapace et al., 2005).Despite the problematic nature of collecting and usingmoult odour, future studies should attempt to test crabs inresponse to freshly collected samples. This could alsoserve as a positive control to distinguish the differencebetween non-responding crabs and the potential for apoor moult odour sample.

As observed in a number of other studies linked tocannibalism the effects of variation in crab size has provento be important. This investigation generally revealed thatlarger crabs demonstrated an increase in behaviours suchas locomotion and tactile investigations, particularly whenexposed to crab-sourced odours. Differences in behaviouras a result of size are rarely, if at all, examined in odour-based investigations. Size related effects have been shownhowever in a study of cannibalism in P. pelagicus (Marshallet al., 2005; Møller et al., 2008) and in the snow crab C.

opilio (Dutil et al., 1997). Predation studies have alsoshown that larger crabs consume more prey items thansmaller conspecifics (Buck et al., 2003) while some cases,as observed in juvenile blue crabs, the size of the crab is notsignificantly important in the size of shrimp prey chosen(Mascaro and Seed, 2000).

While size effects are important in their own right,notice must be taken in the fact that the juvenile crabs usedin this investigation are all approximately the same agewhen tested (Experiments 1 and 2 using same spawning,while Experiment 3 animals were sourced from differentspawning) and yet are greatly variable in size. Theobserved variability between individuals with respect tosize poses an important question of whether crabs becomemore active (e.g. more locomotion and feeding) as theygrow larger or rather the reverse holds true, that beingpredisposed to higher activity levels allows some crabs torespond more quickly and thus get larger as a consequence(leaving less active crabs to stay small). In either case it isclear that this aspect needs to be further examined in thefuture especially in aquaculture contexts where sizedisparities are shown to have a large effect on cannibalismand survival rates.

Unlike other studies examining the behaviour ofjuvenile crabs a significant effect of sex was demonstratedin this investigation. Females displayed an elevatedbehavioural response to the odour of an injured con-specific. Another interpretation might be that males aredesensitised to the odour. A recent study of the juvenilestages of another crab, P. pelagicus, reported that althoughno sexual bias was found with respect to cannibalistic actsthat males were observed to be more aggressive and thatfemales more tolerant of other females (Marshall et al.,2005). A review of cannibalism (Polis, 1981) did in fact


somewhat support our result, reporting that females weremore cannibalistic in 86% of the 50 investigations in whichsexual differences in the predator were noted, but thatthese acts were also associated with courtship or mating. Arecent study of foraging by mature portunid shore crabs,Carcinus maenas, also found that females showed strongerfeeding responses than males, and the depression of malefeeding responses during the reproductive period suits themale’s mate guarding behaviour toward soft post-moultfemales (Hayden et al., 2007). Recent studies have shownthat the transition to physiological maturity in mud crabsprobably occurs at >100 mm CW (Heasman et al., 1985;Knuckey, 1996). As all crabs used in this experiment weresmaller, it is likely that sexual maturity had not yet beenreached. Further experiments need to be conducted tobetter explore this aspect of S. serrata biology as it mayhave important implications to the potential for ‘‘mono-sex’’ or female-only culture in this species.

5. Conclusions

This study has demonstrated, against anecdotalevidence suggesting a strong chemically mediated com-ponent in the attraction to post moult crabs, that moultodour does not elicit a global tactile or feeding response injuvenile mud crabs, S. serrata. Despite being statisticallyinsignificant, the biological importance of this phenom-enon must be considered, as even low percentages ofcannibalistic animals are still capable of dramaticallyreducing the population of crabs that survive to harvest.A large amount of size- and sex-related variability inresponse to crushed conspecific was found, particularlyduring repeat testing of a different cohort of juveniles.Future investigation is recommended to more com-prehensively study the cues mediating cannibalism inS. serrata, as is research to the possibility of geneticselection of particular traits more suited to high densityculture.

Acknowledgements

The statistical assistance of David Mayer (QDEEDI) isgratefully acknowledged.

At BIARC, David Mann aided in the design and cons-truction of the experimental raceways and Tom Asakawaand Beverley Kelly helped in rearing and maintenance ofthe experimental crabs used.

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Behaviour of juvenile mud crabs Scylla serrata in aquaculture: Response to odours of moulting or injured crabs