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Open Access

Peer-reviewed

Research Article

Survival of the Stillest: Predator Avoidance in Shark Embryos

• Ryan Grand. Kempster,
• Nathan Southward. Hart,
• Shaun P. Collin

x

• Published: January 9, 2013
• https://doi.org/ten.1371/journal.pone.0052551

Figures

Abstract

Sharks use highly sensitive electroreceptors to detect the electric fields emitted by potential prey. All the same, it is not known whether prey animals are able to modulate their own bioelectrical signals to reduce predation chance. Here, we show that some shark (Chiloscyllium punctatum) embryos can detect predator-mimicking electric fields and respond past ceasing their respiratory gill movements. Despite being bars to the small space within the egg instance, where they are vulnerable to predators, embryonic sharks are able to recognise dangerous stimuli and react with an innate avoidance response. Knowledge of such behaviours, may inform the evolution of effective shark repellents.

Citation: Kempster RM, Hart NS, Collin SP (2013) Survival of the Stillest: Predator Avoidance in Shark Embryos. PLoS I 8(i): e52551. https://doi.org/x.1371/periodical.pone.0052551

Editor: Andrew Iwaniuk, Academy of Lethbridge, Canada

Received: September 17, 2012; Accepted: November 20, 2012; Published: Jan nine, 2013

Copyright: © 2013 Kempster et al. This is an open up-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original writer and source are credited.

Funding: This work was supported past funding from the WA Country Government and The University of Western Australia (to SPC). The funders had no role in study design, information collection and analysis, decision to publish, or training of the manuscript.

Competing interests: The authors have alleged that no competing interests exist.

Introduction

Electroreception is establish throughout the animal kingdom from invertebrates to mammals and has been shown to play an important function in detecting and locating prey [i], [2], mates [three], potential predators [4], [5] and is idea to exist important in orienting to the earth's magnetic field for navigation [6]–[8]. Electroreceptors of sharks, the ampullae of Lorenzini, find minute electric field gradients via an array of openings or 'pores' at the skin's surface [ii]. Spatial data on the location of a field source is assessed past the differential stimulation of ampullae equally the position of the source changes relative to the beast [1], [2], [half dozen], [nine]. The spatial separation and system of each pore in the array directly influences the detection of electrical stimuli and the resultant changes in the shark's behaviour [2], [10].

The electrosensory organisation of adult sharks is known to primarily mediate the passive detection of bioelectric stimuli produced past potential prey [ane], [two]. Nonetheless, it has been postulated that the electroreceptive organization can be used to notice, and thus avoid, potential predators [4]. Shark embryos that develop inside their female parent may accept little or no use for electroreception until nascency, given that they are protected within the uterus and are nourished either directly by their female parent (viviparity) or via an external yolk sac (ovoviviparity). However, oviposited embryos like those of the bamboo shark (Chiloscyllium punctatum) develop completely independently of their mother inside an egg case (oviparity) (Fig. 1A) [11]. These egg cases are typically deposited on or most the substrate, where they are vulnerable to predators including other sharks, teleost fishes, marine mammals and even large molluscan gastropods [12], [13].

Figure one. A–C.

Photographs depicting three major life stages of the bamboo shark (Chiloscyllium punctatum). A: Embryo encapsulated inside an egg case. B: Early on juvenile (mail hatching) showing its high contrast banding pattern. C. Sexually mature individual that has lost its banding leaving a more typical counter-shading pattern, which it uses to cover-up itself on the substrate. Scale bars = 10 mm.

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Chiloscyllium punctatum embryos volition spend up to five months encapsulated inside a leathery egg instance without the opportunity to escape or visually detect the arroyo of predators (Fig. 1A) [11]. After hatching, at simply x–12 cm in length [11], bamboo shark juveniles are extremely vulnerable to predation. Nevertheless, at this stage, their distinctive pattern of high dissimilarity banding (Fig. 1B) may assistance in avoiding predators since these conspicuous bands mimic the colouration of unpalatable or poisonous prey, i.e. ocean snakes, thereby avoiding predation (known equally Batesian mimicry). This potentially aposematic colouration is lost as the bamboo shark reaches maturity and the banded pattern fades. As it matures, this species adopts the more familiar counter-shading pigmentation exhibited by many other species of sharks, thereby enabling information technology to camouflage itself confronting a dark substrate (Fig. 1C).

During early embryonic development (stages 3–25) [11], [xiv], bamboo sharks are sealed within a pigmented egg example, where their presence would be masked to whatever visually-driven predators and there would exist no exchange of fluids [11] with the surrounding seawater, negating their detection via either mechanoreceptive (lateral line) or olfactory signals. Even so, every bit the embryo approaches the pre-hatching stage of development (stages 26–32), the lesser border of the egg case weakens and the marginal seals open up, thereby allowing the entry of seawater [xi] and the release of sensory cues that may be detectable by predators. As the embryo increases in size, it begins to undulate the tail to facilitate circulation of fresh seawater through the open seals of the egg case to assist in respiration. However, this is thought to increase the adventure of predation [13] owing to the greater likelihood that a passing predator could detect the presence of the embryo due to the release of olfactory cues and/or intermittent hydrodynamic disturbances. Following an increase in the frequency of tail undulations and respiratory gill movements, between stages 26 and 32, the electrosensory system differentiates and may become functional by stage 32 [xv], presumably to assist in predator detection prior to hatching [4].

Results and Give-and-take

When exposed to predator-simulating sinusoidal electrical fields, late stage bamboo shark embryos (phase 34) answer by the cessation of all respiratory gill movements, thereby minimising their ain electrosensory and mechanosensory output in social club to avoid detection (Fig. 2). The cessation of gill movements is immediately followed by a rapid coiling of the tail effectually the body, with little or no discernible body movement during exposure ('freeze' response). Vertebrates that exhibit a 'freeze' response to predators take too been shown to induce cardioventilatory responses, where they decrease their eye charge per unit (bradycardia) to reduce predation risk [xvi]–[21]. Every bit a result, the length of time that an animal is able to reply is finite, as the need to exhale and pump oxygen around the body volition eventually overcome the urge to remain still and undetected. Thus, the bamboo shark embryos tested eventually resume, admitting much reduced, gill movements whilst still being exposed to the predator-simulating stimuli.

Figure two. Average freeze response duration (±ii×Standard Fault) of bamboo shark embryos (stage 32–34) to a range of sinusoidal frequencies (0–20 Hz) and stimulus intensities (0.4–two.1 µV/cm).

Shaded bar corresponds to natural respiratory signals produced past potential predators (1.0–ii.0 Hz) [22] and depression frequency modulations of D.C. fields produced by approaching predators equally they motility relative to an object (0.1–i.0 Hz) [23]. Acme response frequency: 0.5 Hz; duration: mean 18.nine secs.

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Bamboo shark embryos (phase 32–34) prove the greatest abstention response to sinusoidal electrical field frequencies between 0.25 and 1.00 Hz (peaking at 0.v Hz; Fig. two), with response duration (measured from initial time of exposure) increasing every bit the electric field forcefulness increases (increasing electric field force may simulate closer and/or larger predators) (Fig. 3). Less developed embryos (stages 32–33) showroom a reduced response duration to predator-simulating stimuli (Fig. 3A–F). Embryos as young as stage 32 would only respond if the electric field was of sufficient strength, approximately ≥0.ix µV/cm (Fig. 3B). In contrast, stage 34 embryos would respond to electrical field strengths as depression as 0.4 µV/cm (Fig. 3I). Embryos prior to stage 32 failed to show any response to electric field strengths between 0.iv µV/cm and 2.i µV/cm.

Figure iii. A–I.

Freeze response elapsing (±2×Standard Error) of bamboo shark embryos (stages 32–34) to a range of sinusoidal frequencies (0–xx Hz) and stimulus intensities (0.4–2.i µV/cm). Embryos are categorised into nine groups according to their relative phase in development and intensity of the electric field strength exposure. A: Phase 32 embryos exposed to ane.9–2.one µV/cm (elevation response frequency: 0.5 Hz; elapsing: mean xvi.7 secs). B: Stage 32 embryos exposed to 0.ix–i.1 µV/cm (height response frequency: 0.five Hz; duration: mean fourteen.9 secs). C: Stage 32 embryos exposed to 0.4–0.6 µV/cm (elevation response frequency: 0.v Hz; duration: mean 0.3 secs). D: Phase 33 embryos exposed to i.nine–2.i µV/cm (pinnacle response frequency: 0.75 Hz; duration: mean 27.vii secs). E: Stage 33 embryos exposed to 0.ix–1.ane µV/cm (peak response frequency: 1.0 Hz; duration: mean 13.eight secs). F: Phase 33 embryos exposed to 0.4–0.6 µV/cm (peak response frequency: 0.v Hz; elapsing: mean 3.vii secs). G: Stage 34 embryos exposed to 1.9–2.1 µV/cm (height response frequency: 0.v Hz; duration: mean 59.4 secs). H: Stage 34 embryos exposed to 0.9–1.1 µV/cm (peak response frequency: 0.5 Hz; duration: mean 38.4 secs). I: Stage 34 embryos exposed to 0.4–0.six µV/cm (meridian response frequency: 0.5 Hz; elapsing: mean 15.8 secs).

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These results agree with the differentiation and development of the electrosensory organization, equally has been previously shown for the lesser spotted catshark (Scyliorhinus canicula) when the ampullary organs become innervated [v], [15]. Repeated exposure to the same stimulus as well resulted in a reduced response elapsing as embryos (stages 34) became desensitised; embryos appeared to recognise previously presented stimuli when repeatedly exposed within a 30–40 minute menstruum (Fig. four). In contrast, the lesser spotted catshark and the clearnose skate (Raja eglanteria) habituate to stimuli within simply v to 10 minutes of the initial exposure, respectively [4], [five], highlighting significant species-specific differences in the level of temporal sensitivity of the electrosensory organization in elasmobranchs.

Figure 4. Relative freeze response duration when embryos (stage 34) are repeatedly exposed to the same stimulus at set up time intervals after the get-go (initial) response.

Embryos were individually exposed to the same stimulus to get an average initial response time. Embryos were then exposed to the same stimulus 60 minutes after initial response, and re-exposed at decreasing fourth dimension intervals. Response duration is expressed every bit a pct of the initial response.

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The greatest avoidance response to sinusoidal electrical fields (0.25–1.00 Hz with a peak at 0.five Hz; Fig. two) exhibited by bamboo shark embryos in this report corresponds to the natural respiratory signals produced by their potential predators, i.eastward. teleosts and other elasmobranchs [3], [4], [thirteen], [22], and the low frequency modulations of D.C. fields produced past approaching predators [23]; thus indicating the important office of electroreception in the detection and avoidance of predators.

This study advances our understanding of how embryonic sharks respond to electric fields of specific frequency and intensity and how their survival instincts to feed and defend themselves may accept precedence over an electrical deterrent under some atmospheric condition [24]. The conditions under which this species habituates to electrical stimulation may likewise exist useful in the development of electrical shark repellent devices.

Materials and Methods

Ethics Statement

This report was carried out in strict accord with the guidelines of the Australian Code of Do for the Care and Use of Animals for Scientific Purposes (vii^thursday Edition 2004) 'The Code'. The protocol was approved by the Academy of Western Commonwealth of australia Brute Ethics Committee (Permit No. RA/3/100/917). Embryos were monitored daily to assess activity levels earlier, during and post stimulation to allow adequate rest fourth dimension betwixt experimental trials, and all efforts were made to minimise suffering.

Collection and staging of embryos

Bamboo shark embryos were collected every bit freshly oviposited egg cases from captive bred adults from Underwater Earth and Daydream Island Resort aquaria in Queensland, Australia. To enable video recording of embryo activity within the egg example, the opaque external fibrous layer of each egg example was scraped off upon collection. Developing embryos could then be seen conspicuously through the transparent inner layer when held in front end of a fibre optic calorie-free source. Eggs remained submerged in a shallow petri dish filled with seawater throughout this procedure. The embryos were monitored for developmental changes and compared to the stages described for Chiloscyllium punctatum [11] and the staging criteria outlined for Scyliorhinus canicula [fourteen]. All stages, ranging from when the embryo could first be observed with the unaided eye (stage 14), through to pre-hatching, fully developed embryos (stage 34), were tested. Developmental changes were only recorded in the most advanced embryos (stages 31–34).

Experimental design

Embryos encapsulated within the egg case were suspended in a 90 cm long, 45 cm broad, 50 cm deep glass aquarium and transferred individually to an identical tank for testing. A total of 11 embryos were stimulated with sinusoidal electric fields (0–20 Hz) at various stages in their evolution (stages ≤31–34). Electric stimuli were applied at three major intensities (0.4–0.vi µV/cm, 0.nine–1.1 µV/cm and 1.9–two.1 µV/cm) via a function generator and a custom built stimulus generator [25] with an applied electric current between 100 µA and 500 µA (Fig. 5). To ensure minimal variation in the electric field produced, water temperature of 24–25°C and water resistivity of 18–nineteen Ω cm were maintained.

Figure five. Experimental apparatus used to study the response of bamboo shark embryos to predator simulating dipole electrical fields.

A office generator and stimulus controller were used to deliver a dipole electric field of specific intensity and frequency to electrodes positioned along the same longitudinal axis as the embryo. Embryo responses were recorded with a video camera positioned direct in forepart of the experimental tank.

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To account for non-responses, embryos were each stimulated the aforementioned number of times (3 replicates of each stimulus forcefulness and frequency combination: 27 tests in full) and all test results (including zeros) were used to determine the average response duration. Therefore, each embryo was stimulated a total of 27 times (per developmental stage) to obtain a full data set up covering all frequency variations (0–xx Hz) and all stimulus forcefulness variations (0.4–2.1 µV/cm).

Electrical stimuli intensity (i.e. voltage gradient, Five/cm) at the position where the embryo responds to the stimulus was calculated using the equation, Five/cm = (ρ.I.d. cosα)/(2πr³) [26], based on the 'platonic dipole field' equation [27] and the 'charge distribution of an electric field' equation [28]. The variables are as follows: ρ is the resistivity of the seawater (Ω cm), I is the practical electric current (A), d is the altitude between the two electrodes of a dipole (cm), r is the radius (the distance from the eye of the dipole to the position in space where the potential is being calculated) and α is the angle from the position in space to the centre of the dipole with respect to the axis.

In pre-experimental trials, shark embryos appeared to show an increased response duration when the electrode separation distance was increased, indicating that the embryos may interpret this every bit an increase in the size of the simulated predator [28], [29]. To reduce these experimental variables, the electrode separation distance was set at five cm with the embryo held at a uniform radius of 12 cm from the dipole source. These measurements were based on tank size restrictions to minimise any backscatter effects. Further investigation is encouraged to ameliorate understand the issue of increasing electrode separation altitude on predator avoidance response (repellent effect).

The stimulus generator enabled the strength of the applied current to be varied and the function generator enabled a specific wave form to be selected and the output frequency controlled. An ammeter in serial allowed the corporeality of current existence practical through the circuit to be monitored in lodge to plant that the excursion was complete, thereby confirming that an electric field was being generated betwixt the electrodes in the tank. Current from the stimulus generator was delivered to the electrodes via submerged cables and seawater-filled polyethylene tube table salt bridges. A pair of shielded 18AWG coaxial underwater cables was plugged into the stimulus generator. Electric current was passed to seawater-filled polyethylene tubes via the exposed stainless steel pins of the cables [1]. The seawater-filled polyethylene tubing formed a table salt bridge betwixt the electrode arrays in club to eliminate boil currents due to inhomogeneities on the electrode surface [4]. The electrodes were positioned adjacent to the egg example along the longitudinal axis (Fig. 5). During the behavioural observations, stimulus frequencies were presented as continuous sinusoidal stimuli. Response to the stimulus was determined by cessation of all gill movements or a 'freeze' response [Movie S1]. Embryos were stimulated for a minimum of 10 seconds after they resumed initial gill movements, to ensure that the resumption of breathing had been accurately identified. In guild to avoid habituation to the electrical stimulus, an inter-trial interval of xl minutes was used after each freeze response was observed. The strength and frequency of the stimuli was as well varied pseudorandomly.

Video analysis

All behavioural trials were recorded in high definition using a Canon S95 digital video photographic camera. The photographic camera was positioned to view the embryo and at least one of the electrodes (Fig. v). Equally the electrodes were positioned along the same longitudinal axis every bit the embryo they could later be used as a calibration for measurements taken straight from the video clips (the electrodes were a known diameter) including embryo and yolk size and also to confirm embryo altitude from the electrode source. Sound from the video was used to decide the betoken at which the stimulus source was switched on and off. The video analysis software Kinovea™ was used to appraise behavioural clips and record response time.

Supporting Data

Acknowledgments

Nosotros wish to thank Blake and Clint Chapman from Underwater Globe and James Astley from Daydream Island Resort for providing shark embryos and to Channing Egeberg, Caroline Kerr and Carl Schmidt for their invaluable guidance and support throughout this work.

Writer Contributions

Conceived and designed the experiments: RMK. Performed the experiments: RMK. Analyzed the data: RMK. Contributed reagents/materials/analysis tools: RMK SPC. Wrote the newspaper: RMK NSH SPC.

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