1 Department of Mathematics & Statistics, University of West Florida, 11000 University Parkway, Bldg. 4, Pensacola, Florida 32514, USA
2 Shark Research Institute, Global Shark Attack File, P.O. Box 40 Princeton, NJ 08540, USA
3 Shark School Associate, 5970 Osprey Place, Pensacola, FL 32504, USA
Close-up videos of sharks foraging on other live sharks are rare, especially when it comes to footage of the entire duration of an event.
Our goal was to present an in-depth analysis involving a Galapagos shark, Carcharhinus galapagensis, foraging on a whitetip reef shark, Triaenodon obesus.
A frame by frame video examination was used to highlight the different aspects of this bout.
Several behavioral characteristics, including the somewhat cryptic approach, the extensive shaking once the Galapagos shark had the whitetip reef shark between its jaws, and devouring tail-first, stand out in this event.
The entire act appeared very smooth, indicating that this bout, or at least parts thereof, may represent a common hunting strategy for Galapagos sharks.
open-access license: This is an open access article distributed under the terms of the Creative Commons Attribution 4.0 International Public License (CC-BY 4.0), a copy of which is available at: (https://creativecommons.org/licenses/by/4.0/legalcode). This license permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
* Address correspondence to this author at the Department of Mathematics & Statistics, University of West Florida 11000 University Parkway, Bldg. 4 Pensacola, Florida 32514, USA; E-mail: email@example.com
It is commonly accepted that sharks occasionally forage on other live sharks [1Myers RA, Baum JK, Shepherd TD, Powers SP, Peterson CH. Cascading effects of the loss of apex predatory sharks from a coastal ocean. Sci 2007; 315: 1846-50.[http://dx.doi.org/10.1126/science.1138657] -3Heupel MR, Knip DM, Simpfendorfer CA, Dulvy NK. Sizing up the ecological role of sharks as predators. Mar Ecol Prog Ser 2014; 495: 291-8.[http://dx.doi.org/10.3354/meps10597] ]. Although video-sharing websites and TV channels have occasionally offered insights into potential selachivorous bouts in the past [4National Geographic, July 30, 2016 Tiger shark vs hammerhead shark [video file] 2016. Retrieved from: https://www.youtube.com/watch ?v=PHCG0IT1SM-6International Fishing Videos. Huge tiger shark eats smaller shark [video file] 2013. Retrieved from: https://www.youtube.com/watch ?v=ToNmPb9j-ZU], the videos were either taken from too far away, were incomplete, reflected kleptoparasitism during shark fishing, or did not show the actual kill but merely a clash between two sharks without any observable consequences for either of them [7Barcroft TV. Shark vs shark: giant white shark attacks another great white shark [video file] 2016. Retrieved from: https://www.youtube.com/ watch?v=MkWTVwJEQ7c]. Thus, none of those videos are particularly useful for reaching an understanding of the potential behavioral characteristics underlying a bout between two sharks. As a consequence, existing data primarily stems from stomach content analyses [8White WT, Platell ME, Potter IC. Comparisons between the diets of four abundant species of elasmobranchs in a subtropical embayment: Implications for resource partitioning. Mar Biol 2004; 144: 439-48.[http://dx.doi.org/10.1007/s00227-003-1218-1] -10Navarro J, López L, Coll M, Barría C, Sáez-Liante R. Short-and long-term importance of small sharks in the diet of the rare deep-sea shark Dalatias licha. Mar Biol 2016; 161: 1697-707.[http://dx.doi.org/10.1007/s00227-014-2454-2] ] without any indications of how the shark pursued, killed and devoured the other shark.
Here, we describe a close-up video sequence of the first documented predatory bout of a Galapagos shark, Carcharhinus galapagensis, a fairly common species [11Wetherbee BM, Crow GL, Lowe CG. Biology of the galapagos shark Carcharhinus galapagensis in Hawai’i. Environ Biol Fishes 1996; 45: 299-310.[http://dx.doi.org/10.1007/BF00003099] -13Dale JJ, Meyer CG, Clark CE. The ecology of coral reef top predators in the Papahānaumokuākea Marine National Monument. J Mar Biol 2011.[http://dx.doi.org/10.1155/2011/725602] ], killing and swallowing a whitetip reef shark, Triaenodon obesus. We discuss the different parts of the bout regarding the potential influence of the external circumstances where the kill took place. The incident was observed during a night dive; thus the kill was probably affected to some extent by the proximity of the divers as well as the lights they used. Still, the bout appeared rather fluid and effective, suggesting that at least some sections of it reflect general characteristics of a Galapagos shark’s potential hunting strategy.
2. METHODS AND RESULTS
On the evening of April 29, 2015, a group of divers did a night dive at the “Manuelita Coral Garden” site within the Archipelago of Cocos Island, Costa Rica. An area of about 100 m2 was illuminated during the dive. While observing whitetip reef sharks, a Galapagos shark moved into the illuminated area, milled around for a few seconds, then killed and consumed one of the whitetip reef sharks. The entire bout lasted around 15 seconds from the initial contact to the last gulp and was filmed in 720p HD at 30 frames/second. The size of the two sharks could not be measured accurately, but the Galapagos shark was estimated by one of the authors (AM) to be close to 2.5m in length, not uncommon around Cocos Island [14White ER, Myers MC, Flemming JM, Baum JK. Shifting elasmobranch community assemblage at Cocos Island–an isolated marine protected area. Conserv Biol 2015; 29: 1186-97.[http://dx.doi.org/10.1111/cobi.12478] ], whereas the whitetip reef shark, based on comparison to the Galapagos shark, seemed to be about a quarter of that length.
To better describe the bout, the event was divided into four phases: prowl, contact, manipulation, and devouring.
Prowl–During the moments before the kill, the Galapagos shark lowered its head twice towards a whitetip reef shark swimming in front and one swimming beneath its position (see supplemental video). However, it didn’t pursue either of them any further. How long the Galapagos shark was on the prowl prior to the recorded bout remains unknown (Fig. 1a).
Galapagos shark forages on a whitetip reef shark. (a) Galapagos shark prowls prior to the attack. (b) Frontal body area torques towards prey, begin of the actual contact with the prey. (c) Vertical position to enhance pressure onto the whitetip. (d) Shaking prey and moving grip posteriorly. (e) Aligning with whitetip shark to swallow tail-first. (f) Devouring whitetip shark. Numbers reflect duration in fraction of seconds from the beginning of first contact (Fig. 1b).
Immediately before the hit, the Galapagos shark appeared to turn in accordance with the swim pattern of the chosen whitetip reef shark, directly below. The predator then torqued its frontal body area towards the seafloor (Fig. 1b) and pinned down its prey. This motion was immediately followed by shifting its entire body into a vertical position, pushing the prey into the reef (Fig. 1c). The initial bite was aimed at the gill area of the whitetip reef shark. The duration of this phase was less than three seconds.
Once the whitetip reef shark was caught square between the jaws of the Galapagos shark, the predator shook it for about six seconds (Fig. 1d). During this phase, the Galapagos shark changed its hold from mid-body to the tail of the whitetip reef shark. Despite the continued shaking, neither gouging nor ripping of the prey apart occurred.
The onset of this phase transpired seamlessly after the final head shake (Fig. 1e). Although the Galapagos shark gulped six times to swallow the entire whitetip shark, after the first three gulps that took around two seconds, only parts of the whitetip’s head remained visible. It could not be determined if the whitetip reef shark was already dead when being swallowed or just immobilized (Fig. 1f). The entire act of devouring took around six seconds.
The hunting strategies of most shark species are poorly understood since direct observations are rare, except for white sharks, Carcharodon carcharias [15Klimley AP, Le Boeuf BJ, Cantara KM, et al. The hunting strategy of white sharks (Carcharodon carcharias) near a seal colony. Mar Biol 2001; 138: 617-36.[http://dx.doi.org/10.1007/s002270000489] -17Towner AV, Leos-Barajas V, Langrock R, et al. Sex-specific and individual preferences for hunting strategies in white sharks. Funct Ecol 2016; 30: 1397-407.[http://dx.doi.org/10.1111/1365-2435.12613] ], tiger sharks [18Heithaus M, Dill L, Marshall G, Buhleier B. Habitat use and foraging behavior of tiger sharks (Galeocerdo cuvier) in a seagrass ecosystem. Mar Biol 2002; 140: 237-48.[http://dx.doi.org/10.1007/s00227-001-0711-7] ] and a few other species [19Ebert DA. Observations on the predatory behaviour of the sevengill shark Notorynchus cepedianus. S Afr J Mar Sci 1991; 11: 455-65.[http://dx.doi.org/10.2989/025776191784287637] -21Sims DW, Quayle VA. Selective foraging behaviour of basking sharks on zooplankton in a small-scale front. Nature 1998; 393: 460-4.[http://dx.doi.org/10.1038/30959] ]. But even among those species, selachivorous bouts are poorly described or not documented at all, and any potential hints primarily stem from stomach content analyses [22Simpfendorfer CA, Goodreid A, McAuley RB. Diet of three commercially important shark species from Western Australian waters. Mar Freshw Res 2001; 52: 975-85.[http://dx.doi.org/10.1071/MF01017] -24Torres-Rojas YE, Hernández-Herrera A, Galván-Magana F, Alatorre-Ramírez VG. Stomach content analysis of juvenile scalloped hammerhead shark Sphyrna lewini captured off the coast of Mazatlán Mexico. Aquat Ecol 2010; 44: 301-8.[http://dx.doi.org/10.1007/s10452-009-9245-8] ].
Although the video presented is a single event and should be interpreted with caution, especially since it happened within the range of divers holding flashlights, the fluid execution and the smooth transitions between the individual phases suggest that this is potentially a general strategy for Galapagos sharks around Cocos Island.
It is likely that the dive lights increased the numbers of fish gathering which could then have attracted more whitetips [25Martins RS, Perez JAA. Cephalopods and fish attracted by night lights in coastal shallow-waters off southern Brazil with the description of squid and fish behavior. Rev Etol 2006; 8: 27-34.-27Cooke SJ, Lennox RJ, Bower SD, et al. Fishing in the dark: The science and management of recreational fisheries at night. Bull Mar Sci 2018; 93: 519-38.[http://dx.doi.org/10.5343/bms.2015.1103] ]. Although an advantage for the Galapagos shark is possible and the lights may have facilitated the shark’s foraging behavior, the opposite could also be true, and the predator was blinded by the lights and thus moved away from them. This potential drawback, however, would then raise the question of why the Galapagos shark swam into the lights in the first place. Since the potential effect of the divers and their lights can’t be determined, it can also not be established which parts of the bout transpired by chance due to those influences and which ones reflected genuine characteristics of this predator’s hunting strategy. Some of the better-known shark species show an array of strategies when going after prey, ranging from laying in wait to stalking and actively chasing prey down [28Fouts WR, Nelson DR. Prey capture by the Pacific angel shark Squatina californica: Visually mediated strikes and ambush-site characteristics. Copeia 1999; 1999: 304-12.[http://dx.doi.org/10.2307/1447476] -30Papastamatiou YP, Iosilevskii G, Leos-Barajas V, et al. Optimal swimming strategies and behavioral plasticity of oceanic whitetip sharks. Sci Rep 2018; 8: 551.[http://dx.doi.org/10.1038/s41598-017-18608-z] ]. The recorded strategy could be interpreted as stalking or stealth and indeed appeared cryptic to the milling whitetips. Outwardly, the Galapagos shark seemed just to cruise along but was indeed searching for a suitable whitetip reef shark to attack, highlighted by its head motions while on the prowl. It is most plausible that the targeted whitetip was unaware of the imminent attack since the Galapagos shark was directly above the whitetip when striking. The Galapagos shark only had to torque its body downward to capture its prey without an actual forward motion, indicating that the attempt was intentional. Intent to strike is further supported by the observation that the Galapagos shark aimed for the gills, the most unprotected and exposed part of a shark’s body regarding the location of the heart.
The subsequent shaking by the Galapagos shark seemed excessive bearing in mind the rather small size of the whitetip reef shark. The much larger size of the Galapagos shark would suggest a single, well-placed bite could immobilize the prey and thus be sufficient to begin the devouring process; hence the extended shaking may have been a deliberate strategy. Neither of the two most apparent potential strategies, either gouging or severing the prey’s body into two parts, occurred. A third possibility is that the actual shaking was part of the intended strategy to either immobilize or kill the prey. This last option has some merit considering the fluid transition from shaking to the actual devouring phase. Assuming the shift between shaking and the start of devouring was deliberate, then it would be easy to understand why a tail-first swallowing of the whitetip reef shark occurred.
Examination of the manipulation phase shows that the way the Galapagos shark swallowed the prey appeared to be methodical; thus it is a likely possibility that this form of devouring is a common strategy for Galapagos sharks. This does not exclude head-first swallowing. However, such swallowing would require facing potential prey before an attack, or then manipulating prey while holding on to it. Head-first swallowing is often preferred, especially among teleosts, where such orientation prevents a prey’s body parts like opercula, fin rays, or spines from flaring outward during swallowing [31L’Abée-Lund JH, Aass P, Saegrov H. Prey orientation in piscivorous brown trout. J Fish Biol 1996; 48: 871-7.[http://dx.doi.org/10.1111/j.1095-8649.1996.tb01482.x] -33Albins MA, Lyons PJ. Invasive red lionfish Pterois volitans blow directed jets of water at prey fish. Mar Ecol Prog Ser 2012; 448: 1-5.[http://dx.doi.org/10.3354/meps09580] ]. Since a large portion of a Galapagos shark’s diet includes teleosts [12Papastamatiou YP, Wetherbee BM, Lowe CG, Crow GL. Distribution and diet of four species of carcharhinid shark in the Hawaiian Islands: Evidence for resource partitioning and competitive exclusion. Mar Ecol Prog Ser 2006; 320: 239-51.[http://dx.doi.org/10.3354/meps320239] ], head-first swallowing therefore seems most likely. Interestingly, when great hammerheads, Sphyrna mokarran, swallow stingrays, Dasyatis americana, they do it in a head-first fashion as well, although their initial attack occurs from behind [34Strong WR, Snelson FF, Gruber SH. Hammerhead shark predation on stingrays: An observation of prey handling by Sphyrna mokarran. Copeia 1990; 1990: 836-40.[http://dx.doi.org/10.2307/1446449] ]. For hammerheads, the most likely reason for this strategy is that the ray’s tail barb could flare in a tail-first swallowing scenario.
In addition to teleosts, mollusks, crustaceans, and even certain mammals belong to the Galapagos shark’s diet, suggesting this species to be an opportunistic hunter [11Wetherbee BM, Crow GL, Lowe CG. Biology of the galapagos shark Carcharhinus galapagensis in Hawai’i. Environ Biol Fishes 1996; 45: 299-310.[http://dx.doi.org/10.1007/BF00003099] , 12Papastamatiou YP, Wetherbee BM, Lowe CG, Crow GL. Distribution and diet of four species of carcharhinid shark in the Hawaiian Islands: Evidence for resource partitioning and competitive exclusion. Mar Ecol Prog Ser 2006; 320: 239-51.[http://dx.doi.org/10.3354/meps320239] , 35Compagno LJV. Sharks of the world: An annotated and illustrated catalogue of shark species known to date 1984.]. A more stationary population along Cocos Island, where food availability remains less diverse, could have a more specialized diet than more broadly ranging populations of this species. In this case, it is likely that whitetip reef sharks belong to the regular diet for the Cocos population. However, without detailed stomach content analyses for members of the population from Cocos Island, the content of their usual diet cannot be accurately known. Bearing in mind how frequently Galapagos and whitetip reef sharks are observed around Cocos Island (personal observation, EKR), it is likely that whitetips are common prey which is also consistent with the bite volume of the larger Galapagos shark. The bite volume reflects the maximum dimension of a single bite a shark can gouge from a larger animal [36Ritter EK, Levine M. Bite motivation of sharks reflected by the wound structure on humans. Am J Forensic Med Pathol 2005; 26: 136-40.] and is comparable to gape size [3Heupel MR, Knip DM, Simpfendorfer CA, Dulvy NK. Sizing up the ecological role of sharks as predators. Mar Ecol Prog Ser 2014; 495: 291-8.[http://dx.doi.org/10.3354/meps10597] , 37Matott MP, Motta PJ, Hueter RE. Modulation in feeding kinematics and motor pattern of the nurse shark Ginglymostoma cirratum. Environ Biol Fishes 2005; 74: 163-74.[http://dx.doi.org/10.1007/s10641-005-7435-3] , 38Long DJ, Jones RE. White shark predation and scavenging on cetaceans in the eastern North Pacific Ocean. In: Klimley AP, Jones E, Eds. Great white sharks: The biology of Carcharodon carcharias 1996; 293-307.[http://dx.doi.org/10.1016/B978-012415031-7/50028-8] ]. Bite volume for average-sized Galapagos sharks thus may be an indicator of the maximum size of prey that could be consumed whole. Using the size and width of the whitetip reef shark and the estimated bite volume of the Galapagos shark seen in this video suggests that prey selection and devouring it whole did likely not happen by chance. Assuming that the particular prey size was aimed for by the Galapagos shark, the location for the attack could also have been deliberately chosen. The fewer obstructions that an environment has, the less restricted the pursuit of prey will be. The reef structure in this bout offered whitetip reef sharks some protection, which likely contributed to the early abortion of the two prior possible attempts to go after whitetip reef sharks before the actual bout. The selection of this particular whitetip reef shark could indicate primarily that the Galapagos shark saw an appropriately sized whitetip move into a favorable position and took the chance.
The two initial attempts prior to the real bout could indicate that a fitting prey may indeed have to be in a specific location where it could be pinned down, but also in a favorable body orientation, such as perpendicular to the predator’s main body axis and by extension its jaws, and not exceeding a certain size. This would suggest some form of foraging plasticity to take into account the environment and body form [39Helfman GS. Mode selection and mode switching in foraging animals. Adv Stud Behav 1990; 19: 249-98.[http://dx.doi.org/10.1016/S0065-3454(08)60205-3] -41Scharf FS, Buckel JA, Juanes F, Conover DO. Estimating piscine prey size from partial remains: Testing for shifts in foraging mode by juvenile bluefish. Environ Biol Fishes 1997; 49: 377-88.[http://dx.doi.org/10.1023/A:1007318918434] ]. However, such a choice may simply reflect a situational artifact when being presented with several prey species rather than being an indicator of natural steps taken during a bout when going after a single prey.
Whitetip reef sharks are a typical reef dwelling species. Should Galapagos sharks indeed hunt for them occasionally, they would likely have adapted their strategy to the point where structural reliefs matter. Therefore the hunting success recorded in this video would likely reflect such an adaptation.
ETHICS APPROVAL AND CONSENT TO PARTICIPATE
HUMAN AND ANIMAL RIGHTS
CONSENT FOR PUBLICATION
CONFLICT OF INTEREST
The authors declare no conflict of interest, financial or otherwise.
Lucifora LO, García VB, Menni RC, Escalante AH, Hozbor NM. Effects of body size age and maturity stage on diet in a large shark: Ecological and applied implications. Ecol Res 2009; 24: 109-18.[http://dx.doi.org/10.1007/s11284-008-0487-z]
White WT, Platell ME, Potter IC. Comparisons between the diets of four abundant species of elasmobranchs in a subtropical embayment: Implications for resource partitioning. Mar Biol 2004; 144: 439-48.[http://dx.doi.org/10.1007/s00227-003-1218-1]
Cabrera-Chávez-Costa AA, Galván-Magaña F, Escobar-Sánchez O. Food habits of the silky shark Carcharhinus falciformis (Müller & Henle 1839) off the western coast of Baja California Sur Mexico. J Appl Ichthyology 2010; 26: 499-503.[http://dx.doi.org/10.1111/j.1439-0426.2010.01482.x]
Navarro J, López L, Coll M, Barría C, Sáez-Liante R. Short-and long-term importance of small sharks in the diet of the rare deep-sea shark Dalatias licha. Mar Biol 2016; 161: 1697-707.[http://dx.doi.org/10.1007/s00227-014-2454-2]
Papastamatiou YP, Wetherbee BM, Lowe CG, Crow GL. Distribution and diet of four species of carcharhinid shark in the Hawaiian Islands: Evidence for resource partitioning and competitive exclusion. Mar Ecol Prog Ser 2006; 320: 239-51.[http://dx.doi.org/10.3354/meps320239]
Martin RA, Hammerschlag N, Collier RS, Fallows C. Predatory behaviour of white sharks (Carcharodon carcharias) at Seal Island South Africa. J Mar Biol Assoc U K 2005; 85: 1121-36.[http://dx.doi.org/10.1017/S002531540501218X]
Sims DW, Quayle VA. Selective foraging behaviour of basking sharks on zooplankton in a small-scale front. Nature 1998; 393: 460-4.[http://dx.doi.org/10.1038/30959]
Simpfendorfer CA, Goodreid A, McAuley RB. Diet of three commercially important shark species from Western Australian waters. Mar Freshw Res 2001; 52: 975-85.[http://dx.doi.org/10.1071/MF01017]
Joyce WN, Campana SE, Natanson LJ, Kohler NE, Pratt HL, Jensen CF. Analysis of stomach contents of the porbeagle shark (Lamna nasus Bonnaterre) in the northwest Atlantic. ICES J Mar Sci 2002; 59: 1263-9.[http://dx.doi.org/10.1006/jmsc.2002.1286]
Torres-Rojas YE, Hernández-Herrera A, Galván-Magana F, Alatorre-Ramírez VG. Stomach content analysis of juvenile scalloped hammerhead shark Sphyrna lewini captured off the coast of Mazatlán Mexico. Aquat Ecol 2010; 44: 301-8.[http://dx.doi.org/10.1007/s10452-009-9245-8]
Martins RS, Perez JAA. Cephalopods and fish attracted by night lights in coastal shallow-waters off southern Brazil with the description of squid and fish behavior. Rev Etol 2006; 8: 27-34.
Nightingale B, Longcore T, Simenstad CA. Artificial night lighting and fishes. In: Rich C, Longcore T, Eds. Ecological consequences of artificial night lighting 2006; 257-76.
Fouts WR, Nelson DR. Prey capture by the Pacific angel shark Squatina californica: Visually mediated strikes and ambush-site characteristics. Copeia 1999; 1999: 304-12.[http://dx.doi.org/10.2307/1447476]
Meyer CG, Clark TB, Papastamatiou YP, Whitney NM, Holland KN. Long-term movement patterns of tiger sharks Galeocerdo cuvier in Hawaii. Mar Ecol Prog Ser 2009; 381: 223-35.[http://dx.doi.org/10.3354/meps07951]
Long DJ, Jones RE. White shark predation and scavenging on cetaceans in the eastern North Pacific Ocean. In: Klimley AP, Jones E, Eds. Great white sharks: The biology of Carcharodon carcharias 1996; 293-307.[http://dx.doi.org/10.1016/B978-012415031-7/50028-8]