The hunting strategies of pelagic thresher sharks (Alopias pelagicus) were investigated at Pescador Island in the Philippines. It has long been suspected that thresher sharks hunt with their scythe-like tails but the kinematics associated with the behaviour in the wild are poorly understood. From 61 observations recorded by handheld underwater video camera between June and October 2010, 25 thresher shark shunting events were analysed. Thresher sharks employed tail-slaps to debilitate sardines at all times of day. Hunting events comprised preparation, strike, wind-down recovery and prey item collection phases, which occurred sequentially. Preparation phases were significantly longer than the others, presumably to enable a shark to windup a tail-slap. Tail-slaps were initiated by an adduction of the pectoral fins, a manoeuvre that changed a thresher shark's pitch promoting its posterior region to lift rapidly, and stall its approach. Tail-slaps occurred with such force that they may have caused dissolved gas to diffuse out of the water column forming bubbles. Thresher sharks were able to consume more than one sardine at a time, suggesting that tail-slapping is an effective foraging strategy for hunting schooling prey. Pelagic thresher sharks appear to pursue sardines opportunistically by day and night, which may make them vulnerable to fisheries. Alopiids possess specialist pectoral and caudal fins that are likely to have evolved, at least in part, for tail-slapping. The evidence is now clear; thresher sharks really do hunt with their tails.

Funding: This work was supported by a NERC PhD algorithm studentship awarded to SPO, [Blue Skies RES22709]. This study would not have been possible without financial support from the Thresher Shark Research and Conservation Project. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Copyright: © 2013 Oliver et al. This is an open-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 author and source are credited.

In this paper, evidence is provided to show that pelagic thresher sharks use their tails to prey upon sardines, and the kinematics associated with the behaviour are investigated. Hunting events were quantified from handheld video observations to address the following hypotheses: (1) thresher sharks execute a series of rapid body motions that drive tail-slaps during hunting events; (2) tail-slapping enables thresher sharks to stun several prey items at a time. Thresher shark hunting behaviour is discussed in relation to kinematics and hydrodynamics.

When investigating how killer whales forage on schooling herring in Norway, Domenici et al. (1999) showed that tail-slapping enabled the predator to stun up to 33 prey fish with one strike alone. Since sardines school in dense aggregations [4] it can be predicted that thresher sharks employing tail-slaps to hunt them will be able to consume more than one prey item at a time.

Tail-slapping has been observed in a range of marine predators. Humpback and sperm whales (Megaptera novaeanglia and Physeter catodon) communicate over great distances with ‘aerial’ tail-slaps [19] – [21] , and a similar surface behaviour was described as an agonistic threat to reduce resource competition among white sharks (Carcharodon carcharias) in close proximity to each other [22] – [24] , though the behaviour was less interpretable when conducted by bait-attracted individuals [25] . Dolphins (Delphinus delphis) control the shape and density of schooling prey fish using their tails [1] , and killer whales tail-slap bait balls with such ferocity that they produce sound and shockwaves powerful enough to stun fish [2] , [3] , [26] , [27] .

Predation strategies employed by sharks are diverse and vary among species and individuals [11] – [13] . Unique to their taxa, it has long been speculated that thresher sharks use their tails to corral and stun their prey [14] – [16] . Some empirical evidence for this unusual hunting strategy was recently quantified [17] though descriptions of the behaviour remain vague. Under controlled conditions Aalbers et al. (2010) showed that common thresher sharks, Alopias vulpinus were able to make contact with tethered bait using their caudal fins. Thresher sharks have also been frequently foul-hooked in the tails by fishermen longlining them [9] , [18] . While it has been suggested that bigeye (Alopias supersiliosus) and pelagic thresher sharks may employ similar methods of hunting to those described for A. vulpinus [7] , [17] , the kinematics that structure alopiid predatory behaviours in the wild have not been previously documented.

Reaching 365 cm in total length, approximately half of which comprises a scythe-like elongate tail fin, A. pelagicus are the smallest of the three recognised thresher shark (Alopiidae) species [7] . Described as cosmopolitan sharks that frequent warm and temperate offshore waters circumglobally [8] , [9] , pelagic thresher sharks mature late, have low fecundity and are classed as ‘vulnerable’ by the International Union for the Conservation of Nature and Natural Resources' (IUCN) Red List [10] . Since the summer of 2010, pelagic thresher sharks have been observed by SCUBA divers to visit Pescador Island in the central Visayas, where they prey upon Indian sardines, Sardonella longiceps. Sardines are believed to constitute an important component in the diet of thresher sharks [7] (Oliver unpublished data), and it is proposed that they visit this site to exploit its abundant food resources.

Dense aggregations of prey fishes, commonly termed ‘bait balls’, attract large marine predators to areas of high productivity across the globe [1] . Killer whales, Orcinus orca, visit fjords in Norway where they use specialist techniques to hunt schooling herring Clupea harengus [2] , [3] , and dolphins are known to migrate through the central Azores for similar purposes [1] . The seasonal run of the sardine Sardinops sagax in the nearshore waters of the South African coastline [4] has a strong influence over the abundance and distribution of carcharhinid and lamnid sharks that go there to satisfy part of their diets [5] , [6] . In this study it is shown that pelagic thresher sharks, Alopias pelagicus, employ specialist techniques to hunt schooling sardines in the waters surrounding a small coral island in the Philippines.

Methods

All of the research (including the handling of marine life, and the interruption of shark behaviour) was undertaken with the permission of the Governor of Cebu and adhered to the Philippine ‘Wildlife Resources Conservation and Protection Act’. The handling of marine life complied with Bangor University's Research Ethics' framework and ethical policy, and was approved by the College of Natural Sciences' Animal Ethics Committee.

Location Pescador is a small coral island situated in the Tañon Strait (N 09° 55′ 44.2′, E 123° 20′ 61.2′), approximately five kilometers due west from Moalboal, Cebu, in the Philippines (Figure 1). The island is fringed on all sides by a coral reef formed by a shallow plateau of low profile Acropora that crests and sheers down 60 m to the sea valley below. Although fishermen have exploited its resources for decades, Pescador's marine biomass is rich and recreational divers visit the island to observe its diverse wildlife on most days, generating important income for the region. A dense aggregation of sardines Sardonella longiceps, which can be observed year round along Pescador's northwestern reef crest, attracts a variety of marine predators including pelagic thresher sharks (Figure 1). PPT PowerPoint slide

PowerPoint slide PNG larger image

larger image TIFF original image Download: Figure 1. Map showing the location of Pescador Island off Moalboal, Cebu, in the Philippines. A dense aggregation of sardines Sardonella longiceps, can be observed year round along the northwestern crest of the fringing reef (A) where thresher sharks hunt them. https://doi.org/10.1371/journal.pone.0067380.g001

Sampling Fieldwork was undertaken over 70 days, spanning five months, from June to October 2010 (fieldwork was time restricted due to resource limitations). Handheld underwater video cameras were used by SCUBA divers to record thresher shark hunting behaviour during hour-long dives conducted between 09:00 and 16:00 hours. SCUBA divers used Sony Camcorders® FX-1 and HVR-Z1 housed in Gates Z1 underwater housings, fitted with dome ports, with their focal ranges locked to 0.4 m, and recorded their observations of thresher sharks onto MiniDVs in 1080i 50 (25 fps−1) and 1080i 60 (29.97 fps−1) HDV formats. Video records were captured opportunistically in the water column between 10 and 25 m depths with the camera recording when a thresher shark was present and observable in the viewfinder. Recordings were downloaded to a hard drive and screened for analysis. On some occasions, divers interrupted the feeding behaviour of the sharks to collect stunned and dead sardines by hand from the water column. These were brought to the surface where they were inspected for injury, photographed, total length measured, and then released if they were alive. Observable injuries sustained by collected individuals were assumed to be associated with a thresher shark's predatory behaviour. Since no stunned or dead sardines were observed prior to thresher shark attacks, their presence in the water column was used as a proxy for a successful hunting event.

Analysis of Video Recordings Video sequences documenting thresher sharks' hunting behaviour were classified into two main event types: those in which predation attempts were characterised by (1) an overhead tail-slap or (2) a sideways tail-slap. Overhead tail-slaps typically took place when the shark was positioned perpendicular to and facing the perimeter of the bait ball (Figure 2-A). Thresher sharks slapping at sardines from the side while they were aligned parallel to them characterised ‘sideways tail-slaps’ (Figure 2-B). PPT PowerPoint slide

PowerPoint slide PNG larger image

larger image TIFF original image Download: Figure 2. Diagram showing a thresher shark's position relative to the bait ball during (A) overhead; and (B) sideways tail-slaps. https://doi.org/10.1371/journal.pone.0067380.g002

Analysis of Thresher Shark Behaviour For analysis, hunting events were partitioned into ‘phases’ that were characterised by observable changes in a thresher shark's movement and behaviour during a tail-slap. Termed ‘preparation’, ‘strike’, ‘wind-down recovery’ and ‘prey item collection’, phases were analysed in 25 or 29.97 frames s−1 resolution using Final Cut Pro 7 (Apple Inc., CA) to document behaviours, and video still images were used to construct diagrams [28]. Examples of the video data are available in the supporting information (Movies S1–S4).

Defining Terms and Classifying Behaviours The terms ‘motion’, ‘mechanics’ and ‘kinematics’ were adapted from their standard uses in the literature [12]. Motion referred to a change in position of the anatomical structures involved in a thresher shark's hunting behaviour (mouth, caudal peduncle, tail) with respect to time and a fixed reference point. Mechanics referred to the functioning of the anatomical structures and considered the motions of the various parts, as well as the forces acting against them. Kinematics referred to the analysis of the motion alone without reference to any counter forces. Protocols developed by Slater for categorising behaviour [29] were used to differentiate the behavioural patterns observed in thresher sharks as they preyed upon sardines. A shark's relative orientation (parallel or perpendicular to the bait ball) and the kinematics of the mouth, caudal peduncle and tail were used to compare behaviours between the phases of the event types.

Shark Length To estimate a thresher shark's length measurements (total length (TL); precaudal length (PCL); and dorsal caudal fin margin (CDM)), a still image was taken from its video record when the shark was planar to, or in contact with, one of the sardines it was hunting, and both were perpendicular to the axis of observation. Assumed to be equal to the mean (± SE) of the total lengths (cm) of the sardines collected by SCUBA divers in situ (11.588±0.142, n = 56), the total length of a referenced sardine was measured in pixels using an image histogram in Photoshop CS4 (Adobe, San Jose, CA). Lengths were then measured in pixels for the thresher shark in the still image. The shark's actual lengths (cm) could then be expressed as where (f) was shark, (p) pixels and (s) the referenced sardine. Shark sex was determined by the presence or absence of claspers.

Kinematics Only sagittal and transverse plane video observations were selected for kinematic analysis, in which all four phases of the tail-slaps occurred within full view of the camera, and where the shark was close enough to identify the key anatomical parts used for hunting. Of the 22 recordings of overhead tail-slaps, only six sagittal and two transverse plane events were considered suitable for analysis. None of the video records of the sideways tail-slaps met selection standards and were therefore only used to describe the behaviour. For sagittal plane events, three key anatomical parts (i) the terminal caudal fin lobe (tip of the tail), (ii) the midpoint of the caudal peduncle, and (iii) the tip of the snout were tracked in two dimensions by analysing a sequence of video still images. Using the posterior base of the pectoral fin as a fixed reference point, the coordinates of the anatomical parts were plotted for each still frame (Figure 3). Coordinates were expressed as the actual distance (cm) each part was from the base of the pectoral fin (x/y intercept = 0) at the time it was plotted, and referenced in degrees, as well as by the speed it was travelling (ms−1). Anatomical parts were only plotted when they were clearly visible in the video still images. All video still images were oriented with left to right movement for analysis. PPT PowerPoint slide

PowerPoint slide PNG larger image

larger image TIFF original image Download: Figure 3. Diagram showing the method used for analysing the kinematics of a thresher shark's tail-slap from a sequence of video still images. For sagittal plane events, three key anatomical parts (a) the tip of the tail, (b) the midpoint of the caudal peduncle, and (c) the tip of the snout were tracked in two dimensions using the posterior base of the pectoral fin as a fixed reference point (x/y intercept = 0). The arc length of a thresher shark's tail-slap is shown in dashed line. https://doi.org/10.1371/journal.pone.0067380.g003 During the peak accelerations of the strike phase, the speed with which the tip of the tail travelled exceeded the frame rate of the underwater cameras used to record it. As a result, some images of the terminal caudal fin lobe were blurred, for all of the selected recordings. To plot the coordinates of the blurred images, a still image taken from a point in the video sequence when the terminal caudal fin lobe was clearly observable was layered on top of the original still image. The leading edge of the caudal fin, the caudal notch and the lower caudal lobe for the two layered still images were aligned. Since all of the leading edges of the caudal fins aligned precisely and only the tips of the caudal fins were blurred for all occurrences, it was assumed that the position of the terminal caudal fin lobe would not alter, relative to its orientation in the strike phase, and its coordinates were plotted from the image layered on top. For transverse plane events, the pectoral fins were the only anatomical features to be tracked. The ventral midpoint between the pectoral fins was used as a fixed reference point, and coordinates for both the tips of the pectoral fins and their posterior bases were plotted for each video still frame. The angles at which the pectoral fins protruded from a shark's body were measured and the angular velocity with which they adducted to initiate a tail-slap was calculated using trigonometry.