A dawn peak in the occurrence of ‘knifing behaviour’ in blue sharks
© Doyle et al. 2015
Received: 23 December 2014
Accepted: 11 September 2015
Published: 8 October 2015
Knifing is a behaviour whereby a shark swims directly at the surface with its dorsal fin out of the water. While this behaviour has been reported in a number of species, information on the frequency and timing of such behaviour could provide insights on how sharks use the ocean–atmosphere interface.
Our analysis of the timing of the reception of satellite (Argos) messages from SPOT-tagged blue sharks has revealed important insights on knifing behaviour in one of the ocean’s most abundant large predators. We found that knifing behaviour was common in all tagged sharks and occurred during 54–76 % of days tracked, with a mean (and SD) of 4.7 ± 0.4 knifing events per day when observed. The frequency of knifing behaviour increased during the dawn period in all sharks and was supported by analysis of high-resolution depth data from a recovered archival tag. One shark also had a pronounced peak in knifing activity at dusk.
We suggest that blue sharks may be using surface waters during twilight periods to maximise foraging opportunities. Light conditions at dawn are consistent with surface-dwelling prey being both more dispersed and silhouetted by ambient light conditions, making individual prey more visible. The application of this analysis to other species of sharks may provide further insights on knifing behaviour.
Background and aims
A review of the literature shows a large amount of work focusing on the depth preferences of oceanic sharks [1–4]. Despite limited examples in the literature where sharks are recorded spending considerable time in surface waters or are described as surface orientated [5–7], the behaviour whereby sharks ‘knife’ their dorsal fin through the water’s surface (hereafter termed knifing behaviour) is largely unreported outside of the planktivorous sharks . Tracking studies on blue sharks suggest that this species displays knifing behaviour regularly, as smart position only tags (SPOTs) successfully transmit multiple locations throughout the day [9, 10] and pop-up satellite archival tags (PSATs) have described distinct surface-orientated behaviours .
Here, we use an intrinsic feature of all shark satellite tracking studies that utilise the advanced research and global observation satellite (Argos) system and SPOT tags; namely, the timing and frequency of satellite locations received is dependent on the shark’s dorsal fin breaking the surface. Therefore, this present study aimed to quantify the timing and degree of knifing behaviour by blue sharks using a novel analysis of Argos data.
Shark summary data
Mean values (±SD)
Length of shark (fork length and total length in cm)
Sex of shark
Number of days tracked
Number of days knifing events were recorded
% of days knifing events were recorded
Number of knifing events recorded
Daily rate of knifing events (excl. of days when no knifing events were recorded)
Maximum number of knifing events recorded (per day)
Longest duration (days) no knifing events were detected
Argos messages (uplinks) occur when a SPOT tag breaks the water surface and successfully transmits to a satellite. SPOT tags were configured to transmit up to 250 transmissions a day with a 45-s delay between transmissions, resulting in a string of messages if the tag remained above the surface. Each string of messages (and associated location) was considered a ‘knifing event’.
Mixed effects models (using the lme4 package, with model checks using the LMERConvenienceFunctions package) in the R statistical framework were used to investigate the influence of time of day, proximity to dawn/dusk, and location on shark surfacing behaviour, with individual included as a random factor. A stepwise model selection process was undertaken using a combination of AIC values  and maximum likelihood ratio tests . Patterns in knifing behaviour were validated by ruling out potential bias due to satellite coverage using G tests. Knifing events (0 m depth, n = 271,503) recorded by the recovered PSAT tag (shark B) were binned by hour into a frequency distribution to visualise patterns in the timing of knifing behaviour for comparative purposes.
Sharks with SPOT tags were tracked for 74–314 days with a total of 1898 knifing events recorded (Table 1) (see Additional file 1: Figure S1). Surfacing events (knifing) of one message accounted for 32.2 % of the total number of events, 26.8 % of events had five messages or more (≥3.75 min duration) and 6.9 % of events had 10 messages or more suggesting a prolonged time spent at the surface (>7.5 min). Maximum knifing duration was ~12 min (based on 16 continuous messages detected by passing satellite and the tags programmed to transmit at the fast repetition rate of 45 s only and never to switch to the slow repetition rate of 90 s) (Additional file 1: Figure S2). For sharks C, D and E, knifing events were detected during 76.4, 60.8 and 54.1 % of tracked days. The mean number of knifing events per day (exclusive of days when no knifing events were recorded) was 4.7 ± 0.4 (Table 1), with the frequency of knifing events varying between individuals (Table 1) and location. It must be noted that the frequency of knifing events is likely much higher as the detection of such events depends on the coverage provided by the Argos system (a function of latitude and the angle of the satellite above the horizon) which is typically 20–25 %. Bad weather (i.e. large waves) may also prevent satellite tag transmissions from reaching a satellite.
Analysis of Argos messages demonstrated that blue sharks frequently swim at the surface with their dorsal fin out of the water (knifing), often for durations exceeding seven and a half minutes. A mixed effects model showed that ‘proximity to dawn’ explained 36 % of the variability in shark knifing behaviour between midnight and midday, with a post-dawn peak evident in knifing behaviour (Fig. 1). Despite a dusk peak in knifing behaviour being evident for shark C, the mixed effects model using ‘proximity to dusk’ found no corresponding peak in knifing behaviour across all sharks around dusk. We are confident that the pattern in knifing behaviour was not influenced unduly by bias in satellite coverage or tag setup and transmission frequency (Additional file 1: Figures S4, S5). The observed pattern of knifing behaviour was further supported by high-resolution time at depth data from a recovered PSAT (Fig. 3). While surface orientated behaviour has previously been documented for blue sharks [7, 9], for example, a study in the Northeast Atlantic found that blue sharks can spend large periods of their time ‘at or near the surface’ ; the authors do not specify knifing behaviour. Here we specifically highlight the frequency and timing of knifing behaviour that has not been reported in previous studies, likely due to a combination of coarse resolution of binned depth data in PSAT tags (Fig. 2), and/or a broader focus on other behaviours such as diel vertical migration  or spatial ecology .
Surface-oriented behaviour more generally (top 20 m of water) has been observed in many species of teleosts and elasmobranchs, and has been linked with various hypotheses including thermal recovery after deep diving , navigation/orientation [3, 15] and optimal foraging . For deep-diving fish species, surfacing periods are likely linked with thermoregulation [14, 16], with surfacing behaviour resulting in elevated body temperatures that enable animals to spend longer periods at depth or speed up physiological processes. All three sharks tagged with SPOT tags showed an increase in knifing activity at dawn, a time inconsistent with a thermal recovery. The recovered PSAT tag data revealed very little difference (<0.2 °C) in the mean temperature experienced during night versus day and that the warmest waters experienced were typically during midday to afternoon (Additional file 1: Figure S6). Navigation may also play a part in surface swimming in sharks, with use of celestial cues hypothesised as a reason for a white shark (Carcharodon carcharias) swimming just below the surface (0–0.5 m) for 61 % of its time in oceanic waters . Indeed, many animals use the sun as a primary compass in conjunction with a map sense , and therefore, the observed increased frequency of knifing near dawn (and dusk for shark C) may be a good way of defining direction.
Perhaps the most parsimonious explanation for increased knifing post-dawn is that blue sharks are feeding on increased prey densities at the surface around dawn, or are taking advantage of the changing light conditions to surprise attack prey silhouetted at the surface. For example, a 13-year study at Seal Island, South Africa, observed white sharks making 61 nonconsumptive strikes on seabirds . Remarkably, most of these strikes occurred within an hour of dawn, consistent with our post-dawn peak . In the same area, studies of white shark predatory interactions with Cape fur seals (Arctocephalus pusillus pusillus) found that predatory success was highest during low light levels occurring at dawn . For blue sharks, such surface orientated ‘curiosity’ could result in a meal. Several studies have reported blue sharks consuming birds [20, 21] and lumpsucker fish (Cyclopterus lumpus), a fish associated with rafting seaweed . Support also exists for blue sharks profiting from increased densities of surface-dwelling prey at dawn. A study on blue shark diet near Santa Catalina Island, California, found that northern anchovies (Engraulis mordax) were the most abundant prey item and that predation most likely occurred in predawn hours when anchovy schools dispersed into a thin surface scattering layer . Success rates of sharks feeding on schools may be lower than when targeting single prey (e.g. predator confusion effect, [24, 25]), so a combination of non-aggregated anchovy in surface waters and dawn light silhouetting them against the surface may provide increased foraging opportunities and explain the increased knifing behaviour at this time. The increase in knifing behaviour observed in one shark (shark C) at dusk is also likely to be related to similar processes occurring around dawn.
In conclusion, our novel analysis of the timing of Argos messages has provided important insights on the frequency and timing of knifing behaviour in blue sharks. Similarly, a new study evaluated predator–prey interactions between tiger sharks (Galeocerdo cuvier) and loggerhead turtles (Caretta caretta) by testing for differences in their surfacing behaviour (derived from the frequency of Argos messages received from satellite tags, as in our study) in and out of home range overlap areas . The wider implications of our study are that blue sharks may be more vulnerable to bycatch from surface longlines during the twilight periods. Furthermore, the application of this method to larger datasets and other species (i.e. fin-mounted SPOT tags have been successfully deployed on at least five other species ) is likely to increase our understanding of the ecology and behaviour of wide-ranging marine predators.
TKD, LAH and MJ conceived of the study. LAH, TKD and DH conducted the fieldwork. AB, MJ and TKD performed the data analyses. TKD, MJ and AB wrote the manuscript with contributions from LAH and DH. All authors read and approved the final manuscript.
Sharks were tagged under license AE191130/I007 AE19130/P002 and issued by the Irish Health Products Regulatory Authority (HPRA) and complied with the EU Directive 2010/63/EU for scientific research on animals. We wish to thank the skipper of the Osprey II, Pat Condon for his expertise, Pio Enright for his fishing expertise, and Nigel Motyer, Kieran McManamon and Aidan O’Donoghue for the field assistance. We would like to thank Damien Giraud for recovery of the PSAT tag. We would also like to thank Heather Baer of Wildlife Computers and Fernand Sid of CLS User Office (Argos) for their technical support. AB was supported by a Beaufort Marine Research Award funded under the Marine Research Sub-Programme of the National Development Plan 2007–2013, and MJ and DH were supported under Marine Renewable Energy Ireland (MaREI), The SFI Centre for Marine Renewable Energy Research (12/RC/2302). LH was supported by the School of Biological, Earth and Environmental Sciences (BEES), University College Cork (UCC), and the project was part funded by the UCC Strategic Research Fund 2013. TKD was supported by the Coastal and Marine Research Centre, University College Cork. Finally, we would like to acknowledge two anonymous reviewers for greatly improving the manuscript.
Compliance with ethical guidelines
Competing interests The authors declare that they have no competing interests.
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- Boustany AM, Davis SF, Pyle P, Anderson SD, Le Boeuf BJ, Block BA. Satellite tagging—expanded niche for white sharks. Nature. 2002;415:35–6.View ArticlePubMedGoogle Scholar
- Hammerschlag N, Gallagher AJ, Lazarre DM. A review of shark satellite tagging studies. J Exp Mar Biol Ecol. 2011;398:1–8.View ArticleGoogle Scholar
- Klimley AP, Beavers SC, Curtis TH, Jorgensen SJ. Movements and swimming behavior of three species of sharks in La Jolla Canyon, California. Environ Biol Fish. 2002;63:117–35.View ArticleGoogle Scholar
- Sims DW, Southall EJ, Richardson AJ, Reid PC, Metcalfe JD. Seasonal movements and behaviour of basking sharks from archival tagging: no evidence of winter hibernation. Mar Ecol Prog Ser. 2003;248:187–96.View ArticleGoogle Scholar
- Bonfil R, Meyer M, Scholl MC, Johnson R, O’Brien S, Oosthuizen H, et al. Transoceanic migration, spatial dynamics, and population linkages of white sharks. Science. 2005;310:100–3.View ArticlePubMedGoogle Scholar
- Vaudo JJ, Wetherbee BM, Harvey G, Nemeth RS, Aming C, Burnie N, et al. Intraspecific variation in vertical habitat use by tiger sharks (Galeocerdo cuvier) in the western North Atlantic. Ecol Evol. 2014;4:1768–86.PubMed CentralView ArticlePubMedGoogle Scholar
- Queiroz N, Humphries NE, Noble LR, Santos AM, Sims DW. Short-term movements and diving behaviour of satellite-tracked blue sharks Prionace glauca in the northeastern Atlantic Ocean. Mar Ecol Prog Ser. 2010;406:265–79.View ArticleGoogle Scholar
- Sims DW, Quayle VA. Selective foraging behaviour of basking sharks on zooplankton in a small-scale front. Nature. 1998;393:460–4.View ArticleGoogle Scholar
- Stevens JD, Bradford RW, West GJ. Satellite tagging of blue sharks (Prionace glauca) and other pelagic sharks off eastern Australia: depth behaviour, temperature experience and movements. Mar Biol. 2010;157:575–91.View ArticleGoogle Scholar
- Vandeperre F, Aires-da-Silva A, Fontes J, Santos M, Santos RS, Afonso P. Movements of blue sharks (Prionace glauca) across their life history. PLoS One. 2014;9(8):e103538.PubMed CentralView ArticlePubMedGoogle Scholar
- Wagenmakers EJ, Farrell S. AIC model selection using Akaike weights. Psychon Bull Rev. 2004;11:192–6.View ArticlePubMedGoogle Scholar
- Vuong QH. Likelihood ratio tests for model selection and non-nested hypotheses. Econometrica. 1989;57:307–33.View ArticleGoogle Scholar
- Queiroz N, Humphries NE, Noble LR, Santos AM, Sims DW. Spatial dynamics and expanded vertical niche of blue sharks in oceanographic fronts reveal habitat targets for conservation. PLoS One. 2012;7(2):e32374.PubMed CentralView ArticlePubMedGoogle Scholar
- Thums M, Meekan M, Stevens J, Wilson S, Polovina J. Evidence for behavioural thermoregulation by the world’s largest fish. J R Soc Interface. 2013;10(78):1–5.Google Scholar
- Papastamatiou YP, Cartamil DP, Lowe CG, Meyer CG, Wetherbee BM, Holland KN. Scales of orientation, directed walks and movement path structure in sharks. J Anim Ecol. 2011;80:864–74.View ArticlePubMedGoogle Scholar
- Thorrold SR, Afonso P, Fontes J, Braun CD, Santos RS, Skomal GB, et al. Extreme diving behaviour in devil rays links surface waters and the deep ocean. Nat Commun. 2014;5:4274.PubMed CentralView ArticlePubMedGoogle Scholar
- Gould JL, Grant Gould C. Nature’s compass: the mystery of animal navigation. Princeton and Oxford: Princeton University Press; 2012.Google Scholar
- Hammerschlag N, Martin RA, Fallows C, Collier RS, Lawrence R. Investigatory behavior toward surface objects and nonconsumptive strikes on seabirds by white sharks, Carcharodon carcharias, at Seal Island, South Africa (1997–2010). In: Domeier ML, editor. Global perspectives on the biology and life history of the great white shark. 1st ed. Boca Raton: CRC Press; 2012. p. 91–103.View ArticleGoogle Scholar
- Hammerschlag N, Martin RA, Fallows C. Effects of environmental conditions on predator–prey interactions between white sharks (Carcharodon carcharias) and Cape fur seals (Arctocephalus pusillus pusillus) at Seal Island, South Africa. Environ Biol Fish. 2006;76(2–4):341–50. doi:10.1007/s10641-006-9038-z.View ArticleGoogle Scholar
- Henderson AC, Flannery K, Dunne J. Observations on the biology and ecology of the blue shark in the North-east Atlantic. J Fish Biol. 2001;58:1347–58.View ArticleGoogle Scholar
- Vaske Junior T, Lessa RP, Gadig OBF. Feeding habits of the blue shark (Prionace glauca) off the coast of Brazil. Biota Neotropica. 2009;9:55–60.View ArticleGoogle Scholar
- Vandendriessche S, Messiaen M, O’Flynn S, Vincx M, Degraer S. Hiding and feeding in floating seaweed: floating seaweed clumps as possible refuges or feeding grounds for fishes. Estuar Coast Shelf Sci. 2007;71:691–703.View ArticleGoogle Scholar
- Tricas TC. Relationships of the blue shark, Prionace glauca, and its prey species near Santa Catalina Island, California. Fish Bull. 1979;77:175–82.Google Scholar
- Jeschke JM, Tollrian R. Prey swarming: which predators become confused and why? Anim Behav. 2007;74:387–93.View ArticleGoogle Scholar
- Neill SRS, Cullen JM. Experiments on whether schooling by their prey affects hunting behavior of cephalopods and fish predators. J Zool. 1974;172:549–69.View ArticleGoogle Scholar
- Hammerschlag N, Broderick AC, Coker JW, Coyne MS, Dodd M, Frick MG, et al. Evaluating the landscape of fear between apex predatory sharks and mobile sea turtles across a large dynamic seascape. Ecology. 2015;96(8):2117–26. doi:10.1890/14-2113.1.View ArticlePubMedGoogle Scholar