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Photographic evidence from a recreational angler of the northernmost record of the bull shark Carcharhinus leucas (Elasmobranchii: Carcharhinidae) in the western Pacific Ocean

Published online by Cambridge University Press:  12 October 2023

Yukiya Ogata Open the ORCID record for Yukiya Ogata [Opens in a new window]  and
Atsunobu Murase Open the ORCID record for Atsunobu Murase [Opens in a new window]
Yukiya Ogata*
Affiliation:
Interdisciplinary Graduate School of Agriculture and Engineering, University of Miyazaki, 1-1 Gakuen-kibanadai-nishi, Miyazaki 889-2192, Japan Nobeoka Marine Science Station, Field Science Center, University of Miyazaki, 376-6 Akamizu, Nobeoka, Miyazaki 889-0517, Japan
Atsunobu Murase
Affiliation:
Nobeoka Marine Science Station, Field Science Center, University of Miyazaki, 376-6 Akamizu, Nobeoka, Miyazaki 889-0517, Japan Department of Marine Biology and Environmental Sciences, Faculty of Agriculture, University of Miyazaki, 1-1 Gakuen-kibanadai-nishi, Miyazaki 889-2192, Japan
*
Corresponding author: Yukiya Ogata; Email: [email protected]
Rights & Permissions [Opens in a new window]

Abstract

Photographs of a single shark specimen (1040 mm in total length) caught in the Oyodo River estuary, Miyazaki Prefecture, Kyushu, Japan, by a recreational angler and uploaded to the social networking service Facebook, were identified as a juvenile specimen of the bull shark Carcharhinus leucas. The photographic record, now deposited in the Kanagawa Prefectural Museum of Natural History collection, represents the northernmost record of this species in the western Pacific Ocean. Although C. leucas is known to utilize primarily tropical estuarine habitats as nursery grounds, a few reports exist regarding the utilization of subtropical and warm-temperate latitude estuaries, as in this case. From the perspectives of species conservation and shark-bite mitigation in warm-temperate latitudes, further information on C. leucas occurrence around its northern distribution limit is required.

Keywords

citizen scienceelasmobranchsestuarine-associated fishphotographic voucherrange extensionsocial networking service
Type
Marine Record
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 103 , 2023 , e80
Copyright
Copyright © The Author(s), 2023. Published by Cambridge University Press on behalf of Marine Biological Association of the United Kingdom

Introduction

The bull shark Carcharhinus leucas Valenciennes, 1839, is circumglobally distributed, occurring mainly in tropical, subtropical, and warm-temperate latitudes in shallow continental and shelf waters. This species has a high tolerance of low-salinity environments, such as estuaries and rivers, which are often utilized as essential habitats, especially during early C. leucas life stages (Ebert et al., Reference Ebert, Dando and Fowler2021; Gausmann, Reference Gausmann2021). However, such habitats have often been subjected to depletion, degradation, modification, and pollution due to human activities (Costanza et al., Reference Costanza, d'Arge, de Groot, Farber, Grasso, Hannon, Limburg, Naeem, O'Neill, Paruelo, Raskin, Sutton and van de Belt1997; Lotze et al., Reference Lotze, Lenihan, Bourque, Bradbury, Cooke, Kay, Kidwell, Kirby, Peterson and Jackson2006; Barbier et al., Reference Barbier, Hacker, Kennedy, Koch, Stier and Silliman2011). In addition, C. leucas has been overfished throughout its range for fins, flesh, skins, and liver oils (Last and Stevens, Reference Last and Stevens2009), despite a warning that a decline in population numbers would require a long recovery time due to slow maturation of individuals (15–20 years) and low birth rate (1–14 pups at one time after 10–11 months of gestation; Nevill et al., Reference Nevill, Bamboche and Philoe2013; Ebert et al., Reference Ebert, Dando and Fowler2021). Accordingly, the C. leucas population is considered to be declining on a global scale; it is assessed in the IUCN Red List as ‘Vulnerable’ (Rigby et al., Reference Rigby, Espinoza, Derrick, Pacoureau and Dicken2021). Any conservation strategy requires an understanding of distribution patterns and habitat utilization, especially in the case of threatened taxa (Lamoreux et al., Reference Lamoreux, Morrison, Ricketts, Olson, Dinerstein, McKnight and Shugart2006; Mota-Vargas and Rojas-Soto, Reference Mota-Vargas and Rojas-Soto2012; Moore, Reference Moore2018). In the western Pacific Ocean, C. leucas has been recorded primarily from tropical and subtropical latitudes, the only reliable record from a warm-temperate latitude in the region was of a juvenile male specimen (729 mm in total length) collected off the coast of Shanghai, China, at approximately 31°N (Catalogue No. BMNH 74.1.16.63; Garrick, Reference Garrick1982; Gausmann, Reference Gausmann2021). Clearly, information on the western Pacific warm-temperate latitude occurrence and habitat utilization of C. leucas is extremely limited.

The recent frequency of reported unprovoked shark-bite incidents has increased around the world (McPhee, Reference McPhee2014), presumably due to an increase in the number of ocean users. A number of species have been implicated, including (most commonly) the great white shark (Carcharodon carcharias), the tiger shark (Galeocerdo cuvier), and the bull shark (C. leucas; McPhee, Reference McPhee2014; Chapman and McPhee, Reference Chapman and McPhee2016). Although shark-bite incidents attract a great deal of public and media attention (Neff, Reference Neff2012), many large shark species, including those mentioned earlier, are legally protected or threatened (Ebert et al., Reference Ebert, Dando and Fowler2021). Therefore, public policies considering both public safety and the responsibility for protecting endangered predators, such as C. leucas, are needed (Neff, Reference Neff2012). In addition, the actual risks to humans from sharks need to be re-assessed, based on the most up-to-date scientific knowledge of shark abundance and distribution (Simpfendorfer et al., Reference Simpfendorfer, Heupel, White and Dulvy2011; Chapman and McPhee, Reference Chapman and McPhee2016).

In recent years, the general public has contributed to scientific knowledge in many ways, with so-called ‘citizen science’ becoming widespread in many fields (Devictor et al., Reference Devictor, Whittaker and Beltrame2010; Dickinson et al., Reference Dickinson, Zuckerberg and Bonter2010; Kobori et al., Reference Kobori, Dickinson, Washitani, Sakurai, Amano, Komatsu, Kitamura, Takagawa, Koyama, Ogawa and Miller-Rushing2016; Eitzel et al., Reference Eitzel, Cappadonna, Santo-Lang, Duerr, Virapongse, West, Kyba, Bowser, Cooper, Sforzi, Metcalfe, Harris, Thiel, Haklay, Ponciano, Roche, Ceccaroni, Shilling, Dörler, Heigl, Kiessling, Davis and Jiang2017). It is considered a useful tool for clarifying the distribution and population ranges of species in ichthyology, recording, for example, a new distribution location of a species (Miyazaki et al., Reference Miyazaki, Murase, Sahara, Angulo and Senou2017; Heard et al., Reference Heard, Chen and Wen2019), movement ranges of individuals (Armstrong et al., Reference Armstrong, Armstrong, Bennett, Richardson, Townsend and Dudgeon2019; Araujo et al., Reference Araujo, Ismail, McCann, McCann, Legaspi, Snow, Labaja, Manjaji-Mastumoto and Ponzo2020; Séguigne et al., Reference Séguigne, Mourier, Clua, Buray and Planes2023), and the presence of non-native species (Miyazaki et al., Reference Miyazaki, Teramura and Senou2016; Pentyliuk et al., Reference Pentyliuk, Schmidt, Poesch and Green2023). In fact, several citizen groups have been formed in some regions, with initiatives for shark conservation (Bargnesi et al., Reference Bargnesi, Lucrezi and Ferretti2020), there being a shift in perception from protecting humans from sharks to protecting sharks from humans (Simpfendorfer et al., Reference Simpfendorfer, Heupel, White and Dulvy2011). Although the number of cases of records deriving from citizen science by recreational anglers is increasing (Gibson et al., Reference Gibson, Streich, Topping and Stunz2019; Gausmann and Hasan, Reference Gausmann and Hasan2022), the amount of shark research involving citizen science remains still small, with most studies having been conducted by scuba divers (Bargnesi et al., Reference Bargnesi, Lucrezi and Ferretti2020). Here, we provide photographic evidence of an immature specimen of C. leucas that was caught by a recreational angler which represents the northernmost record of this species in the western Pacific Ocean.

Materials and methods

In September 2015, a live fish caught by a local recreational angler (M. Oshikawa) and kept in the water on a long string was predated at the mouth of the Oyodo River, Miyazaki Prefecture, Kyushu, Japan (Figure 1). In addition, the angler's friend caught a shark of about 700 mm total length (TL) at the same location later that month. Subsequently, the remains of a carp (Cyprinus carpio[caudal part missing]) were found at the same place on 6 October 2015. Assuming both cases of predation were due to a feeding shark and that the shark might still be in the locality, the angler returned to the same place several times hoping to catch it. On 27 May 2016, the angler finally caught a shark specimen by lure fishing. The specimen was photographed and its TL measured after landed and given to a friend of the angler. Although the shark was not preserved as a scientific specimen, the angler's posts, including photographs, were later found on a social networking service (SNS: Facebook) by the first author (Figures 2, 3). The authors identified the shark as C. leucas. Subsequently, permission was granted to the authors for use of the photographs and collection data for this report on C. leucas from an estuarine habitat in the warm-temperate latitude of Japan, thereby adding to knowledge of the distribution of the species. This new record represents the northernmost record of C. leucas in the western Pacific Ocean region.

Figure 1. Distribution map of Carcharhinus leucas in Japan. Black spot and grey mesh indicate present and previous records, respectively.

Figure 2. A post on Facebook posted by a recreational angler on 6 October 2015. Main points of comments translated and summarized in English as follows: ‘I found a recently predated carp at the mouth of the Oyodo River. My friend hooked a shark of about 700 mm total length at the same place a week ago, thus I believe the carp was predated by a shark.’

Figure 3. A post on Facebook posted by a recreational angler on 27 May 2016. Main points of comments translated and summarized in English as follows: ‘Finally, I caught a shark at the same place where I found the carp last year. Its length is 1040 mm total length. I don't know what species it is.’ Photographs cropped by author.

Results

Colour photographs of the shark individual produced by the recreational fishermen were deposited by the authors in the image database of fishes at the Kanagawa Prefectural Museum of Natural History (KPM-NR), with the accompanying data: Carcharhinus leucas, collected and photographed by M. Oshikawa on 27 May 2016; collection method: hook and line with lure; location: mouth of Oyodo River, Miyazaki City, Miyazaki Prefecture, Kyushu, southern Japan (31°53'24.0”N, 131°27'19.2”E); registration number: KPM-NR 213016A–C. Note: KPM registration numbers are expressed as seven digits, including leading zeros (e.g. KPM-NR0213016), on the museum database, but the latter are omitted here. TL of the specimen was measured as the distance between the distal tips of the snout and the caudal fin.

Photographs of the captured specimen (Figure 3: 1040 mm TL) were identified by the authors as Carcharhinus leucas, based on the following morphological characteristics according to Compagno (Reference Compagno1984), Last and Stevens (Reference Last and Stevens2009), and Ebert et al.'s (Reference Ebert, Dando and Fowler2021) observations were as follows: short, bluntly rounded snout; snout broader than long; internarial space less than preoral length; labial furrows inconspicuous; eyes small; large angular pectoral fin; first dorsal fin broad, height about three times the second dorsal fin height; margin of second dorsal fin concave; both dorsal fins with short rear tips; no interdorsal ridge; caudal keels inconspicuous; and fin tips dusky. Carcharhinus leucas is most similar to the pigeye shark, C. amboinensis; both species have a short, broad, and blunt snout, the upper anterolateral teeth broad, triangular, and serrated, and lacking an interdorsal ridge (Compagno, Reference Compagno1984; Last and Stevens, Reference Last and Stevens2009; Ebert et al., Reference Ebert, Dando and Fowler2021). However, the present specimen photographs differed from C. amboinensis in the following features: first dorsal fin height less than 3.1 times the second dorsal fin height (more than 3.1 times in C. amboinensis); second dorsal fin margin concave (nearly straight); fin tips, except for first dorsal fin, strikingly dusky [indistinct (Compagno, Reference Compagno1984; Last and Stevens, Reference Last and Stevens2009; Ebert et al., Reference Ebert, Dando and Fowler2021)]. The comparison of the morphometrical characteristics of both species with the photographic material obtained from the fishermen ruled out C. amboinensis and left C. leucas as the only possible species.

Discussion

Carcharhinus leucas is a circumglobal shark found in tropical to warm-temperate latitudes of both hemispheres (Ebert et al., Reference Ebert, Dando and Fowler2021; Gausmann, Reference Gausmann2021; Rigby et al., Reference Rigby, Espinoza, Derrick, Pacoureau and Dicken2021). In the western Pacific Ocean, however, the species has primarily been recorded from tropical and subtropical latitudes (Gausmann, Reference Gausmann2021), with only a single warm-temperate latitude record off the coast of Shanghai, China (Garrick, Reference Garrick1982; Gausmann, Reference Gausmann2021). In Japan, the species has been recorded previously only from the subtropical marine waters of Okinawa, Ishigaki, and Iriomote islands (Ryukyu Islands, Okinawa Prefecture) including freshwater habitats such as Iriomote's Urauchi River (Tachihara et al., Reference Tachihara, Nakao, Tokunaga, Tsuhako, Takada and Shimose2003; Matsumoto et al., Reference Matsumoto, Uchida, Toda and Nakaya2006; Masunaga et al., Reference Masunaga, Kosuge, Asai and Ota2008; Shimose and Taira, Reference Shimose and Taira2014; Aonuma et al., Reference Aonuma, Yamaguchi, Yagishita, Yoshino and Nakabo2013 [Figure 1]). Thus, the photographed specimen from the Oyodo River mouth, Kyushu, mainland Japan, currently represents the northernmost record of the species in the western Pacific Ocean (31°53'24.0”N).

The specimen (1040 mm TL) was considered to have been a juvenile because newly born C. leucas are reported as 560–810 mm TL, with males maturing at 1570–2260 mm and females at 1800–2300 mm (Compagno, Reference Compagno1984; Ebert et al., Reference Ebert, Dando and Fowler2021). Juvenile C. leucas prefer lower salinity zones, often spending considerable time in such habitats (Simpfendorfer et al., Reference Simpfendorfer, Freitas, Wiley and Heupel2005; Heupel and Simpfendorfer, Reference Heupel and Simpfendorfer2008; Werry et al., Reference Werry, Lee, Otway, Hu and Sumpton2011; Drymon et al., Reference Drymon, Ajemian and Powers2014). In the tropical and subtropical latitudes, juveniles utilize estuaries as their main nursery habitat (Simpfendorfer et al., Reference Simpfendorfer, Freitas, Wiley and Heupel2005; Heupel and Simpfendorfer, Reference Heupel and Simpfendorfer2008; Drymon et al., Reference Drymon, Ajemian and Powers2014), whereas in the warm-temperate latitude, the limit of the species distribution, such environments are rarely utilized for that purpose (Whitfield, Reference Whitfield1994; Gausmann, Reference Gausmann2021). However, in recent years, a northward shift of the species’ nursery habitat has been reported in the western North Atlantic Ocean which is the transitional zone between temperate and subtropical latitudes, associated with increased water temperature and salinity (Bangley et al., Reference Bangley, Paramore, Shiffman and Rulifson2018). Miyazaki Prefecture has a north–south open coast, defined as a warm-temperate latitude (Nishimura, Reference Nishimura and Nishimura1992; Kai and Motomura, Reference Kai, Motomura, Kai, Motomura and Matsuura2022), facing the Pacific Ocean, with the warm Kuroshio Current flowing offshore (Murase et al., Reference Murase, Miki and Motomura2017; Miki et al., Reference Miki, Murase and Wada2018). However, the distance of the coast from the Kuroshio Current increases northward (Murase, Reference Murase2020), resulting in a lower sea surface temperature off the northern coast of the prefecture (Akazaki et al., Reference Akazaki, Nakamura and Morishita2010; Murase et al., Reference Murase, Miki and Motomura2017). In addition, several tropical or subtropical fish species, represented by apparently adult specimens, have been reported along the southern coast of the prefecture (e.g. Miki et al., Reference Miki, Murase and Wada2018; Murase et al., Reference Murase, Miki, Wada, Itou, Motomura and Senou2018; Sakamoto et al., Reference Sakamoto, Miki and Murase2018; Shibuya et al., Reference Shibuya, Ogata, Miki, Wada and Motomura2020), suggesting a subtropical or similar environment. The Oyodo River mouth, where C. leucas was caught, is located on the southern coast of the prefecture. The water temperature data about once every three months at approximately 2 km upstream from the shark's landing site (31°54'02”N, 131°26'03”E) is available (Ministry of Land, Infrastructure, Transport and Tourism). According to this, the water temperatures are ranging from 26.1 °C in summer (22 August 2015) to 9.8 °C in winter (10 February 2016). These data indicate that water temperature of downstream of the river keeps around 20 °C or more except for winter season, being preferable condition for juveniles of C. leucas (Hueter and Tyminski, Reference Hueter and Tyminski2007; Gausmann, Reference Gausmann2021).

Furthermore, the bite-size of the predated carp was similar to the mouth size evident in the photo of C. leucas, the latter specimen having been caught using a lure (Figures 2, 3). The evidence suggests that young C. leucas utilize the estuarine zone of the Oyodo River as a nursery ground (at least temporarily). One-year-old juveniles of C. leucas utilize and stay in low-salinity zones as a nursery ground during the warmer months until water temperatures fall to about 21 °C (also found at 16.4 °C) and disappear during the colder months, and return to these areas next warm season (Hueter and Tyminski, Reference Hueter and Tyminski2007). It is assumed that juveniles of the species may undergo a similar seasonal migrating near the Miyazaki coastline, but any suggestion of seasonal occurrence, overwintering, or reproduction of bull sharks are presently unsupported. It is necessary to continue to monitor the occurrence of the bull shark not only in Miyazaki Prefecture but also near the boundaries of distributional ranges in order to elucidate the occurrence status (i.e. occasional visitor or resident) at known distribution limit for the avoidance of shark-bite incidents in temperate latitude under ongoing climate change. In addition, a recent molecular approach has also revealed that this species has a local population; the population of the Ryukyu Islands, including Iriomote Island, is genetically distinct (Devloo-Delva et al., Reference Devloo-Delva, Burridge, Kyne, Brunnschweiler, Chapman, Charvet, Chen, Cliff, Daly, Drymon, Espinoza, Fernando, Barcia, Glaus, González-Garza, Grant, Gunasekera, Hernandez, Hyodo, Jabado, Jaquemet, Johnson, Ketchum, Magalon, Marthick, Mollen, Mona, Naylor, Nevill, Phillips, Pillans, Postaire, Smoothey, Tachihara, Tillet, Valerio-Vargas and Feutry2023). Bull sharks occurring in the temperate latitudes of Japan need to be genetically examined to reveal population matching from the viewpoint of future conservation in the western Pacific regions.

Various research approaches are necessary for information supporting future conservation management strategies for sharks and rays (Simpfendorfer et al., Reference Simpfendorfer, Heupel, White and Dulvy2011). Citizen science can also be expected to contribute to the accumulation of biological information on endangered sharks, such as the whale shark (Rhincodon typus; Araujo et al., Reference Araujo, Ismail, McCann, McCann, Legaspi, Snow, Labaja, Manjaji-Mastumoto and Ponzo2020), as well as observations of human and marine wildlife interactions (Pirotta et al., Reference Pirotta, Hocking, Iggleden and Harcourt2022), being an information source not readily available to researchers or administrations (Miyazaki et al., Reference Miyazaki, Murase, Shiina, Naoe, Nakashiro, Honda, Yamaide and Senou2014; Eitzel et al., Reference Eitzel, Cappadonna, Santo-Lang, Duerr, Virapongse, West, Kyba, Bowser, Cooper, Sforzi, Metcalfe, Harris, Thiel, Haklay, Ponciano, Roche, Ceccaroni, Shilling, Dörler, Heigl, Kiessling, Davis and Jiang2017). As is the case with this study, the information or materials gained by recreational anglers could provide scientists with valuable evidence for fishery management and the critical habitat of sharks (Gibson et al., Reference Gibson, Streich, Topping and Stunz2019; Gausmann and Hasan, Reference Gausmann and Hasan2022). Especially in recent years, the magnitude of the contribution of those anglers for this topic in data-poor regions with some barriers to research such as financial limits and logistical difficulties has been emphasized (Gausmann and Hasan, Reference Gausmann and Hasan2022).

The ‘accidental crowdsourcing approach’ described here (i.e. a social network post, similar to Miyazaki et al. [Reference Miyazaki, Murase, Shiina, Naoe, Nakashiro, Honda, Yamaide and Senou2014]) is an example of the potential for scientists to work collaboratively with the general public, thereby filling gaps in shark distribution. In addition to changing human perception of sharks (Simpfendorfer et al., Reference Simpfendorfer, Heupel, White and Dulvy2011), it is likely that more data collected by members of the public will become available in the future with the development of camera technology and social networking services. Such data should be shared publicly in the discussion of future policies for more effective shark conservation management (Simpfendorfer et al., Reference Simpfendorfer, Heupel, White and Dulvy2011; Chapman and McPhee, Reference Chapman and McPhee2016).

Acknowledgements

We are grateful to Hiroshi Senou (Kanagawa Prefectural Museum of Natural History) and Hidetoshi Wada (The University Museum, The University of Tokyo), who registered the examined photographs, and Masahiro Oshikawa, who provided the examined photographs and information to us. We also thank Graham S. Hardy (New Zealand) for English revision of an early draft of the manuscript and appreciate the helpful comments from the editor and anonymous reviewers.

Data availability

All relevant data are within the manuscript.

Author contributions

YO was the major contributor to the manuscript. AM supervised the study and revised the manuscript. Both authors read and approved the final manuscript.

Competing interests

The authors declare none.

Ethical standards

Not applicable.

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Figure 0

Figure 1. Distribution map of Carcharhinus leucas in Japan. Black spot and grey mesh indicate present and previous records, respectively.

Figure 1

Figure 2. A post on Facebook posted by a recreational angler on 6 October 2015. Main points of comments translated and summarized in English as follows: ‘I found a recently predated carp at the mouth of the Oyodo River. My friend hooked a shark of about 700 mm total length at the same place a week ago, thus I believe the carp was predated by a shark.’

Figure 2

Figure 3. A post on Facebook posted by a recreational angler on 27 May 2016. Main points of comments translated and summarized in English as follows: ‘Finally, I caught a shark at the same place where I found the carp last year. Its length is 1040 mm total length. I don't know what species it is.’ Photographs cropped by author.