https://orcid.org/0009-0003-6341-8703
Figures
Abstract
The nocturnal feeding behavior and zoogeographical habitat of cookiecutter sharks Isistius brasiliensis and Isistius plutodus (Isistius spp.) greatly reduces interaction of this species with live humans. Attacks on live humans are exceedingly rare with 7 cases reported worldwide, 6 of them in Hawaiʻi, and 5 of these occuring among channel swimmers. Published research suggests that periods of bright moonlight may increase Isistius spp. contact with live humans and does not otherwise identify significant trends or risk factors. Yet 5 of the 6 Isistius spp. bites on live humans in Hawaiʻian waters occurred with the moon set and after nautical twilight end and before nautical twilight start. From 1961–2023 in Hawaiʻi, 129 successful solo channel crosses and 5 Isistius spp. related injuries in the habitat of cookiecutter sharks were analyzed across two groups: one where both the moon and sun were set (dark group) and one where the moon and/or sun was in the sky (light group). There was a significant difference for swimmers bitten by Isistius spp. in the dark 4 (12%) versus light groups 1 (1%), p = 0.012, RR 12.6 (95% confidence interval: 1.5–108.9). Swim start time and year was also significant (Pearson correlation 0.566, p <0.001). Swimmer gender and use of shark deterrent devices and artificial illumination were not significant. The growing popularity of channel swimming in Hawaiʻi and swim start times have contributed to an increasing likelihood of live human and Isistius spp. contact and a moonless night sky is a significant risk factor for this interaction.
Citation: Minaglia S, Liegl M (2024) Moonless night sky increases Isistius species (cookiecutter shark) and live human contact. PLoS ONE 19(2): e0291852. https://doi.org/10.1371/journal.pone.0291852
Editor: Daniel M. Coffey, Texas A&M University Corpus Christi, UNITED STATES
Received: September 6, 2023; Accepted: January 18, 2024; Published: February 21, 2024
Copyright: © 2024 Minaglia, Liegl. 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.
Data Availability: All relevant data are within the manuscript and its Supporting Information files.
Funding: The author(s) received no specific funding for this work.
Competing interests: The authors have declared that no competing interests exist.
Introduction
The two species of cookiecutter sharks, Isistius brasiliensis and Isistius plutodus (Isistius spp.) are best known for the characteristic wound they leave on their prey items and for their “hit and run” feeding behavior recently witnessed by live humans [1, 2]. These pelagic sharks remove circular plugs of flesh by sucking onto their prey using specialized pharyngeal muscles and fleshy lips, inserting their upper jaw teeth, and sweeping their proportionately larger lower jaw teeth through the flesh often twisting in a circular motion to remove and ingest their feed [3]. The resultant circular, concave wound is a characteristic sign of an Isistius spp. bite. Cookiecutter sharks are thought to undertake diel vertical migrations with a daytime depth range between 1,000–3,500 meters in primarily warm, coastal waters near islands [4]. They typically rise near the surface at night to feed on squid, small fish, and a variety of large pelagic species and then return to the bathyal zone when daylight resumes [5–7]. They possess a well-developed lateral line system, bioluminescence, and large eyes that give them a competitive advantage over their prey especially in low-light settings.
Contact between Isistius spp. and deceased humans afloat in the sea has been documented [8–11] yet contact with live humans is exceedingly rare. Out of 7 ever-documented and confirmed attacks on live humans, 6 occurred in Hawaiʻian waters between the years 2009 and 2023 and 5 of these occurred among channel-swimmers [1, 2, 12, 13]. Channels are bodies of water that separate land forms. Channel swimming is the sport of swimming across these large bodies of water from one land form to another. Hawaiʻi is home to 9 channels with varying distances and depths. Five of these channels match the zoogeographical habitat of Isistius spp. and have been traversed by channel swimmers (Table 1). All 6 Isistius spp. bites in Hawaiʻi have occurred in two of these channels, the ʻAlenuihāhā Channel being the 2nd deepest and the Kaiwi Channel being the 4th deepest in Hawaiʻi (Table 2). The minimum surface over water depth where one of the 6 bites in Hawaiʻi occurred was estimated at 366 meters [13].
Published research suggests that periods of bright moonlight may increase Isistius spp. contact with live humans [1, 14]. A 2022 National Geographic documentary film focused on a spike in attacks in 2019 but did not otherwise identify significant trends or risk factors [15]. Yet 5 out of 6 documented Isistius spp. bites on live humans in Hawaiʻian waters occurred with the moon set and after nautical twilight end and before nautical twilight start. The research question therefore generated from this observation is whether absence of the sun and moon from the night sky while a human swimmer transits through the zoogeographical zone of Isistius spp. is an independent risk factor for contact with the species and potential injury.
Materials and methods
A retrospective review of the State of Hawaiʻi Department of Land and Natural Resources (DLNR) Division of Aquatic Resources (DAR) Shark Incidents List [13] identified 6 live victims of Isistius spp. one of whom was not swimming a channel. A comprehensive Web of Science and Pubmed search of the literature written in English using the terms: “Isistius species”, “Isistius sp.”, “Isistius spp.”, “cookiecutter shark”, “cookiecutter shark bite”, “shark bite”, and “Hawaiʻi” on July 1, 2023 was also performed and confirmed the above 6 victims to be the only documented and confirmed cases of Isistius spp. attacks on live humans in Hawaiʻi. The International Shark Attack File identified these victims as well as another live victim in North Queensland, Australia in 2017 [12].
This retrospective cohort study included all channel swimmers that were either injured by Isistius spp. and/or successfully completed a solo crossing of any of the 5 Hawaiʻian channels that match the zoogeographical natural habitat of Isistius spp. With the exception of one swimmer, data for all swimmers including victims of attacks was obtained from publicly available, previously published sources [1, 2, 12, 13, 15, 16]. Specifically, the date of swim, duration of swim, gender, start and end times, and use of artificial lights and/or electronic shark deterrents were known for successful swimmers and are part of an established database used to certify and celebrate the accomplishment of the swimmers [16]. Additionally, data for 4 of the victims was complete and obtained from the case report and case series that described their attacks [1, 2]. Written informed consent was obtained from the sole successful yet injured swimmer described in this report (Fig 3., Table 2: Victim 6) whom provided additional data that was not publicly available at the time this study was performed. The Institutional Review Board policy of the Queen’s Medical Center does not require approval for use of the information pertaining to the one swimmer. All successful solo crossings were included in the analysis even if they were tandem solo crossings. One successful relay swim across the Kaʻieʻiewaho Channel and 5 successful relay swims across the Kaiwi channel were excluded from analysis due to multiple swimmers swimming in series with varying speeds, varying use of artificial illumination, and varying use of shark deterrent devices. Swims across the ʻAlenuihāhā, Kaulakahi, Kaiwi, and Kealaikahiki channels were thus included in the analysis.
The minimum surface over water depth where one of the 6 recorded Isistius spp. bites on live humans had occurred in Hawaiʻi was used as the benchmark to determine where the zoogeographical zone of Isistius spp. existed over the swimming course for each of Hawaiʻi’s 4 deepest and crossed-by-solo-swimmer channels [13]. Water depth was estimated from National Oceanic and Atmospheric Administration (NOAA) Office of Coast Survey charts 19010 and 19380 [17, 18]. Additionally, the exact location of each of the 5 channel-swimming victims at which time their injury occurred is known and lies within this calculated zoogeographical zone [1, 2, 12, 13]. The line distance of each swim course for each channel and the total swim time was known for all 129 completed swims occurring in the 4 channels from September 1961- July 1, 2023. Speed in statute miles per hour was calculated for the entirety of each completed swim and the estimated time each swimmer entered and exited the calculated zoogeographical zone of Isistius spp. was recorded.
Additional data included nautical twilight start and end times and moon rise and set times [19–21]. Swimmers transiting for any length of time through the above determined zoogeographical zone of Isistius spp. after nautical twilight end and with the moon set and before nautical twilight start were grouped as the ‘dark group’. The remaining swimmers comprised the ‘light group’ because they transited through this zone with the moon up and/or after nautical twilight start or before nautical twilight end.
Non-parametric Fisher’s exact test was performed for categorical variables (reported as N (%)). Pearson correlation coefficient was calculated to examine the relationships between start time of swim and year of channel swim. A p-value <0.05 was considered significant. SPSS version 28 (Chicago, Illinois, USA) was used for analyses.
Results
Review of the State of Hawaii Department of Land and Natural Resources (DLNR)- Division of Aquatic Resources (DAR) Shark Incidents List identified 6 live victims of Isistius brasiliensis and Isistius plutodus (Isistius spp.) one of whom was not swimming a channel. The individual not swimming a channel was attacked in the ʻAlenuihāhā Channel at an estimated surface over water depth of 366 meters and similar to 4 out of 5 of the channel-swimming victims was attacked with the moon set and after nautical twilight end and before nautical twilight start. Given the individual has remained confidential and was not participating in a channel-swim he/she has been excluded from analysis. Overall, the date of swim, duration of swim, start and end times, gender, use of artificial lights and/or electronic shark deterrents, nautical twilight start and end times and moon rise and set times were obtained for all 133 swimmers either successful and/or injured.
Of the 133 swimmers the majority were male (65%). The most common channel swim was Kaiwi (78%), followed by Kaulakahi (14%), Kealaikahiki (4%) and ʻAlenuihāhā (4%). All but 2 swimmers swam from Molokaʻi to Oʻahu to complete the Kaiwi Channel, all but 3 swimmers swam from Kauaʻi to Niʻihau to complete the Kaulakahi Channel, all swimmers swam from Hawaiʻi to Maui to complete the ʻAlenuihāhā channel and all swimmers swam from Kahoʻolawe to Lānaʻi to complete the Kealakahiki channel. 123 swimmers and/or crew (92%) were successfully contacted to obtain the additional data pertaining to use of artificial illumination and/or electronic shark deterrent devices. Overall, 111 (83%) of swimmers and/or crew were able to recall the use of artificial illumination and/or the use of electronic shark deterrent devices during their swims. 73% of the swimmers used artificial illumination. Electronic shark deterrent devices were used for over half the swimmers (53%). The sun was up for 56% of the swimmers and the sky was lit by moon or sun for the majority (76%).
A total of 5 swimmers (4%) encountered 7 Isistius spp. bites (Figs 1 and 2). 3 of the bitten swimmers used electronic shark deterrent devices. 3 of the bitten swimmers used glow sticks while the other 2 did not use any form of artificial illumination. Of note, boat lights went on shortly before the latter 2 swimmers were attacked. One swimmer was injured by two distinct Isistius spp. bites and was still able to complete the Kaiwi Channel (Fig 3). There was a significant difference for the swimmers bitten by Isistius spp. in the dark group 4 (12%) versus the light group 1 (1%), p = 0.012 (Table 3). The relative risk was 12.6 (95% confidence interval) 1.5–108.9). There were no significant differences when comparing dark and light sky with gender, use of shark deterrent devices and the presence of artificial illumination (sundown only). There were no significant differences when comparing those receiving no bite versus bite with gender, electronic shark deterrent devices, artificial illumination (sundown only). All 5 (100%) bites occurred with sun down versus the 70 (55%) swimmers in the no bite group. This was marginally significant at p = 0.068 (Table 4).
Provided by National Oceanic and Atmospheric Administration (NOAA) Office of Coast Survey, nauticalcharts.noaa.gov.
Provided by National Oceanic and Atmospheric Administration (NOAA) Office of Coast Survey, nauticalcharts.noaa.gov.
Consent to publication was obtained from the subject.
The two channels, Kaulakahi and Kealaikahiki are both 17 miles and on average took swimmers 11 hours 17 minutes (range 9:25–14:28) and 11 hours 22 minutes (range 10:24–11:53) to cross, respectively. The ʻAlenuihāhā and Kaiwi Channels are 30 and 26 miles in length and have average crossing times of 17 hours 26 minutes (range 14:51–20:08) and 16 hours 40 minutes (12:02–27:33), respectively. Swim start time and year of channel swim was significant when looking at the ‘Alenuihāhā and Kaiwi channels only. During the earlier years, the start time was just after midnight versus later years (post 2010) starting closer to 6 PM. Pearson correlation was 0.566, p <0.001 (Fig 2). There was no significant correlation between moon phase in days and year of swim for ‘Alenuihāhā channel (p = 0.723) and Kaiwi channel (p = 0.140) and both combined (p = 0.225)(Fig 5). In contrast, all swim start times were between 6:00 AM and 7:33 AM for the Kealaikahiki Channel and between 4:21 AM and 6:27 AM for the Kaulakahi Channel. This effectively placed all swimmers of these two channels in the zoogeographical habitat of Isistius spp. during daytime.
Discussion
The width of each channel determines the average time it takes for a channel swimmer to cross. The Kaiʻeiʻewaho Channel is 72 miles and has only been crossed once by a relay team of 6 swimmers with a total time of 47 hours 55 minutes. This channel is the deepest and given its length it is unlikely to be attempted by a serious solo swimmer. In 2008, the inclusion of the Kaiwi Channel to Oceans 7, a list of 7 long-distance open-water swims through some of the worlds’ most dangerous sea channels has led to a significant increase in swims across this particular channel. It is highly unlikely for any swimmer to complete either the ‘Alenuihāhā or Kaiwi channels exclusively during daylight hours given average crossing times.
Isistius spp. migrates to surface waters at night and during the day to depths up to 3500 meters. It feeds on large pelagic fishes with its unique “hit and run” feeding behavior and also consumes smaller prey including squid [4–7]. It is possible that this species attacks in groups as Fig 3 and numerous other reports show different diameter bites in live and deceased victims [1, 7–9]. The purple back squid, Sthenoteuthis oualaniensis often aggregates at night near boats where the water is illuminated and feeds on other cephalopods and myctophids [22]. S. oualaniensis is commonly caught at night in Hawaiʻian waters by shining lights into the water and jigging. Through the process of positive phototaxis the use of artificial lights at night likely contribute to feeding opportunities for Isistius spp. by attracting prey items. Anecdotally, deepwater fisherman that fish in Hawaiʻian waters at night often indicate that the darker the night sky the greater the ability of artificial lights to aggregate fish. In contrast, surface organisms are more scattered during periods of natural illumination and artificial lights do not possess the same aggregative ability. A hypothesis generated from this information is that on the darkest nights, the artificially lit human activity more effectively lures prey items of Isistius spp. to the surface thus creating an opportunity for the species to come in contact with live humans swimming at the surface. It is common for swimmers to wear artificial illumination on their suits, goggle straps, and caps and for accompanying kayakers to display artificial illumination for safety purposes and to avoid being lost at sea. It is possible that the addition of artificial illumination may contribute to aggregation of Isistius spp. prey items in otherwise dark conditions.
Fig 4 shows that around 2010 it became common for swimmers to start in the late afternoon or early evening. It is highly likely that this change in decision making intended to reduce sun exposure, the likelihood of a nighttime finish, and the impact of strong coastal winds that arise after sunrise while unintentionally increasing the likelihood that swimmers transit the zoogeographical habitat of Isistius spp. in the dark. It is clear from this analysis that swims started occurring more frequently with the sun down after 2010. An analysis of moon phase showed that there is no correlation between moon phase in days and year of swim (Fig 5). While tidal data was not collected it is unlikely to have had a significant impact on this analysis. Hawaiʻi like most of the Pacific has tides with strong and variable inequality meaning there is a difference in height between the two daily high tides and the two daily low tides. In addition, the timing of these tides changes every day. Therefore, if departing on a high or low tide was a primary objective then start times would not likely vary by year as they did and in fact be more evenly distributed across year as well as time of day.
Our data suggests that swimmers crossing the deepest portions of the Kaiwi and ʻAlenuihāhā Channels at night and during periods of no moon are at increased risk of contact with Isistius spp. This probability risk would marginally increase if the individual not swimming a channel while attacked in the ʻAlenuihāhā Channel with the moon set and after nautical twilight end and before nautical twilight start was included in the analysis. Indeed, there have never been any documented Isistius spp. bites on any other swimmers including the other 691 channel swimmers that successfully completed any of the ʻAuʻau, Pailolo, Kalohi, and Alalakeiki Channels in Hawaiʻi with a maximum surface over water depth of 251 meters [16–18]. Of note, several single, double, and triple cross swims in these shorter channels have included night swimming [16, 23, 24].
Strengths of this study include the definition of the zoogeographical habitat of Isistius spp. determined by local sources and current knowledge of species behavior. The definition of this habitat could be significantly improved in the future through electronic tagging of cookiecutter sharks instead of relying on the reported surface over water depth from 6 attacks. Additional strengths include the strict criteria used to determine the “light” versus “dark” groups of swimmers transiting this area. Swimmers were placed in the “dark” group if they transited the habitat in the dark with the moon down for any length of time. This decision was made to reflect exposure to the risk variable. Limitations include a very small sample size in the ‘bite group’ rendering these data preliminary and missing data from 22 swimmers and/or crew only pertaining to the use of artificial illumination and/or shark deterrent devices. Another limitation includes the methodology used to determine when swimmers entered and exited the zoogeographical habitat of Isistius spp. Times were calculated based on the average speed of each swimmer although it is possible that speed varied due to current and tidal factors. It is unlikely that this methodology affected any particular group disproportionately. More accurate data can be made available through the use of global positioning devices to better pinpoint a swimmer’s location in the channel at each time point, however use of these devices was not consistent among crews even in recent years. Prospective collection of this data is underway.
Conclusion
Periods of no natural light when both the moon and sun are set are associated with increased frequency of live human and Isistius spp. contact compared to moonlit nights and daytime. This is in stark contrast to prior reports suggesting moonlit nights confer greater risk. These data further support Isistius spp. zoogeographical data indicating that the species lives in marine environments with depths of at least 366 meters and are nocturnal hunters. It is possible that the presence of artificial sources of illumination in the darkest conditions may lead to increased Isistius spp. and live human interaction although this retrospective cohort study did not support this assumption. In addition to considering sea and weather conditions and sun exposure duration, a strong recommendation supporting human safety can be made to structure channel swimming so that a swimmer transits through the zoogeographical habitat Isistius spp. during moonlit nights or daytime.
Acknowledgments
The authors thank Carl Kawauchi, Michael Twigg-Smith, Bill Goding, Ivan Shigaki, Mike Spalding, Adherbal de Oliveira, Eric Schall, Isaiah Mojica, Andy Walberer, Steven Munatones, Dr. Harry Huffaker, Dr. Patrick Pedro, Dr. Darryl Takebayashi, and the swimmers of the Hawaiʻian channels for providing valuable information necessary to complete this research.
References
- 1. Honebrink R, Buch R, Galpin P, Burgess G. First documented attack on a live human by a cookiecutter shark (Squaliformes, Dalatiidae: Isistius sp.). Pacific Sci 2011; 65(3):365–374.
- 2. Scala VA, Ng K, Kaneshige J, Furuta S, Hayashi MS. Cookiecutter Shark-Related Injuries: A New Threat to Swimming Across the Ka’iwi Channel. Hawaii J Health Soc Welf 2021; 80(11 Suppl 3):31–37 (2021). pmid:34820633
- 3. deFigueiredo Petean F, R. de Carvalho M. Comparative morphology and systematics of the cookiecutter sharks, genus Isistius Gill(1864) (Chondrichthyes:Squaliformes:Dalatiidae). PLOSONE 2018; https://doi.org/10.1371/journal.pone.0201913.
- 4.
Last P, Stevens J. Sharks and rays of Australia. Fisheries Research and Development Corporation. CSIRO, Australia. Published 1994.
- 5. Compagno L. FAO species cata- log. Vol. 4. Sharks of the world: Annotated and illustrated catalogue of shark species known to date. Part 1. Hexanchi- formes to Lamniformes. FAO Fish. Synop 1984; 125:93–95.
- 6. Carlisle A, Allan EA, Kim SL, Meyer L, Port J, Scherrer S, O’Sullivan . Integrating multiple chemical tracers to elucidate the diet and habitat of Cookiecutter Sharks. J Sci Rep 2021; 11(1):11809. pmid:34083578
- 7. Papastamatiou YP, Wetherbee BM, O’Sullivan J, Goodmanlowe GD, Lowe CG. Foraging ecology of cookiecutter sharks (Isistius brasiliensis) on pelagic fishes in Hawaiʻi, inferred from prey bite wounds. Environ Bio Fishes 2010; 88:361–368.
- 8. Makino Y, Tachihara K, Ageda S, Arao T, Fuke C, Miyazaki T. Peculiar circular and C-shaped injuries on a body from the sea. Am J Forensic Med Pathol 2004; 25(2):169–71. pmid:15166773
- 9. Hayashi T, Higo E, Orito H, Ago K, Ogata M. Postmortem wounds caused by cookie-cutter sharks (Isistius species): an autopsy case of a drowning victim. Forensic Sci Med Pathol 2015; 11(1):119–21. pmid:25115672
- 10. Ribéreau-Gayon A, Rando C, Schuliar Y, Chapenoire S, Crema ER, Claes J, et al. Extensive unusual lesions on a large number of immersed human victims found to be from cookiecutter sharks (Isistius spp.): an examination of the Yemenia plane crash. Int J Legal Med 2017; 131(2):423–432. pmid:27623973
- 11. Ribéreau-Gayon A, Carter DO, Regan S. New evidence of predation on humans by cookiecutter sharks in Kauai, Hawaii. Int J Legal Med 2018;132(5):1381–1387. pmid:29445874
- 12.
International Shark Attack File (ISAF). https://www.floridamuseum.ufl.edu/shark-attacks//. Accessed July 1, 2023.
- 13.
State of Hawaiʻi Department of Land and Natural Resources (DLNR) Division of Aquatic Resources (DAR) Shark Incidents List. https://dlnr.hawaii.gov/sharks/shark-incidents/incidents-list/. Accessed July 1, 2023.
- 14. Keartes S. A plane crash, a boy with a bite & a cryptic deep-sea shark. https://www.earthtouchnews.com/oceans/sharks/a-plane-crash-a-boy-with-a-bite-a-cryptic-deep-sea-shark/. Published 2017. Accessed July 1, 2023.
- 15.
Lask K, director. When Sharks Attack Season 8 Episode 1 Hawaiʻian Fright Night [Film]; 2022. Washington, D.C.: National Geographic.
- 16. Kawauchi C, Arakaki K. Hawaiiswim.org. http://www.hawaiiswim.org/hawaiianChannel/DblPailoloChannel.html. Published 2013. Accessed July 1, 2023.
- 17. Oceanic National and Administration Atmospheric (NOAA) Office of Coast Survey. Chart 19010. https://www.charts.noaa.gov/OnLineViewer/19010.shtml. Accessed 1 July 2023.
- 18. National Oceanic and Atmospheric Administration (NOAA) Office of Coast Survey. Chart 19380. https://www.charts.noaa.gov/OnLineViewer/19010.shtml. Accessed 1 July 2023.
- 19.
Nautical twilight times, Honolulu, Hawaiʻi, United States. https://www.timeanddate.com/sun/usa/honolulu. Accessed 1 July 2023.
- 20.
Moon phases (1961–2023) https://www.moongiant.com. Accessed 1 July 2023.
- 21.
Moon phases (1990–2023) https://www.timeanddate.com/moon/usa/honolulu. Accessed 1 July 2023.
- 22. Parry M. Feeding behavior of two ommastrephid squids Ommastrephes bartramii and Sthenoteuthis oualaniensis off Hawaii. Mar Ecol Prog Ser 2006; 318:229–235.
- 23. Munatones S. 3 For 3, The ʻAu I Nā Mokupuni ʻEkolu Swim Challenge. https://www.openwaterswimming.com/3-for-3-au-i-na-mokupuni-ekolu-swi/. Published 2018. Accessed July 1, 2023.
- 24. Munatones S. Becca Mann Describes The Maui Nui On WOWSA Live. https://www.openwaterswimming.com/becca-mann-describes-the-maui-nui-on-wowsa-live/. Published 2020. Accessed July 1, 2023.