Número 23, enero, 2024: 77–85

ISSN versión impresa: 2071–9841        ISSN versión en línea: 2079–0139 https://doi.org/10.33800/nc.vi23.348

Nota científica

A NEW RECORD OF BONY FISH PREY FOR THE GENUS ISISTIUS

(CHONDRICHTHYES: DALATIIDAE) IN A COASTAL ZONE OF SOUTHEASTERN MEXICO

Nuevo registro de un pez óseo como presa del género Isistius 

(Chondrichthyes: Dalatiidae) en una zona costera del sureste de México

Armando T. Wakida-Kusunoki1*, Vicente Anislado-Tolentino2a, Jorge I. Rosales-Vásquez2b,

Rodolfo Castro-Barbosa3, and Luis Fernando Del Moral-Flores4

1 Centro Regional de Investigación Pesquera y Acuacultura, Instituto Mexicano de Investigación en Pesca y Acuacultura Sustentables, México, https://orcid.org/0000-0002-7917-2651. 2 Grupo de Investigadores Libres Sphyrna. Querétaro, México, a                            https://orcid.org/0000-0002-2184-0047, anislado@gmail.com; bhttps://orcid. org/0000-0001-5245-3376, carcharodon.rosales@gmail.com. 3 Investigador independiente, Ciudad del Carmen, Campeche, https://orcid.org/0000-0002-5108-3120, rodolfocatro14@gmail.com. 4 Facultad de Estudios Superiores Iztacala, Universidad Nacional Autónoma de México, Tlalnepantla, Edo de México, https://orcid. org/0000-0002-7804-2716, delmoralfer@gmail.com. *Corresponding author: armandowakida@yahoo.com.mx.

 [Recieved: September 04, 2023. Accepted: January 03, 2024]

ABSTRACT

The first report of bite wounds from cookiecutter shark in a specimen of cobia in the Southern Gulf of Mexico is described. The specimen was captured by artisanal fishery in the coastal zone of Tabasco, Mexico. It presented three bite wounds with 25 to 26 teeth marks per wound, major axis interval between 3.7 and 4.7 cm and all areas of less than 10 cm2. This is new record of a bony fish as prey of genus Isistius maybe of I. brasiliensis in coastal waters over the continental shelf, in the Southern Gulf of Mexico.

Keywords: bite wounds, Rachycentron canadum, Tabasco, opportunistic feeding, continental shelf.

RESUMEN

Se describe el primer reporte de heridas por mordidas del tiburón cigarro a un espécimen de cobia en la parte sur del golfo de México. El espécimen fue capturado por pesquería artesanal en la zona costera de Tabasco, México. Presentó tres heridas por mordidas con 25 a 26 marcas de dientes por herida, un intervalo del eje mayor entre 3.7 a 4.7 cm y todas las áreas menores a 10 cm2. Este es un nuevo registro de un pez óseo como presa del género Isistius, posiblemente I. brasiliensis, en aguas costeras sobre la plataforma continental, para el sur del golfo de México.

Palabras clave: heridas por mordidas, Rachycentron canadum, Tabasco, alimentación oportunista, plataforma continental.

The family Dalatiidae includes 10 species of sharks, all considered mesopelagic, with records of three species that predate on larger prey: Dalatias licha Bonnaterre, 1788, Isistius brasiliensis Quoy & Gaimard, 1824 and I. plutodus Garrick & Springer, 1964 (Ebert et al., 2021). The cookiecutter shark Isistius brasiliensis is a species that presents a maximum length of approximately 55 cm and is found in both coastal and oceanic habitats worldwide at depths ranging from 85 to 3700 m (Compagno, 1984; Ebert et al., 2021; Strasburg, 1963).

In the Gulf of Mexico, this species has been reported mainly in the northern zone with fewer records in the southern Gulf (Castro-Aguirre & García-Domínguez, 1988; Retzer, 1990; RuizAbierno et al., 2016). Recently, Grace et al. (2018) reported cookiecutter shark bite wounds on cetaceans, showing the presence of this phenomenon over an extensive area of the Gulf of Mexico.

Cookiecutter sharks are small mesopelagic sharks that present diel vertical migrations (Strasburg, 1963; Widder, 1998) best known for their feeding behavior, which has been determined by some authors as ectoparasitic, feeding on pieces of flesh from large marine animals (Honebrink et al., 2011; Menezes et al., 2022) in addition to active predation over small bony fishes, squid and crustaceans (Compagno, 1984; Ebert et al., 2021). These sharks have been implicated as responsible for round-shaped wounds in marine megafauna (Dwyer & Visser 2011) and even humans (Honebrink et al., 2011). Cookiecutter attack wounds have been found in tuna, swordfish and billfish (Muñoz-Chápuli et al., 1988; Niella et al., 2018; Papastamatiou et al., 2010), white shark (Hoyos-Padilla et al., 2013), cetaceans (Dwyer & Visser, 2011), pinnipeds (Gallo-Reynoso & Figueroa-Carranza, 1992; Souto et al., 2009) and sirenians (Reddacliff, 1988).

The cobia (Ranchycentrum canadum [Linnaeus, 1766]) is a large and pelagic-coastal bony fish that is distributed in tropical and subtropical waters, in depths up to 70 m, except in the eastern Pacific (Shaffer & Nakamura, 1989). In Mexico, this fish is one of the fishing and aquaculture resources with high commercial importance (DOF, 2012), the dried-salted presentation works as a substitute for cod. However, even when its commercial importance is evident, there are no studies on its predators, leaving only anecdotes about the dolphin fish (Shaffer & Nakamura, 1989) and the mako shark (fisherman observations), with which the ecological niche of cobia cannot be reliably established.

Forensic analysis of shark bite wounds allows to establish a good approximation of the attacking species and the position of either the victim or the attacker and is widely used for shark-human relationship studies (Ribéreau-Gayon et al., 2017; Ritter & Levine, 2004). However, these studies have not been conducted on marks left by cookiecutter sharks on fish and marine mammals, allowing predator identification only at the supra-species level, with possible identification based solely on the current knowledge of the geographic distribution of the two Isistius species (Best & Photopoulou, 2016), without considering that the less abundant species increase their distribution when they are adequately identified (Zidowitz et al., 2004). An assertive identification of the attacking species would not only determine which species prey on the affected animals, but could also provide data that increase the regional taxonomic listings and allows a better understanding of the ecology and ethology of prey and predator.

The objective of this work is to provide the record of a new species of bony fish as prey of the genus Isistius in shallow Mexican waters of the Gulf of Mexico from the description of bite wounds on a cobia.

Figure 1. Sampling zone of the Cobia (Rachycentron canadum) with three cookiecutter shark (Isistius sp.) bite wounds in the Southern Gulf of Mexico.

On October 12, 2020, during a sampling performed at a monitoring of artisanal fishery in Barra Carlos Rovirosa, Tabasco, Mexico (92° 41’ 05” W, 18° 35’ 10” N), a cobia with three fresh wounds was found. It was caught with a 3.5 inch, 1389 m long gillnet operating at a depth of 30 m (92° 34’ 36.162 W, 18° 55’ 45.58 N) (Fig. 1). The specimen presents three ovoid shaped wounds in its right flank (Fig. 2a), with evident dental marks characteristic of those made by cookiecutter sharks (Isistius spp). The total length (TL) of the cobia and of the three wounds were measured with a 1.5 m tape measure (±1 mm). The wounds were measured along two axes (length and width) to calculate perimeters and areas.

                                                                                 

The bite wounds were analyzed with Gimp 2.1 (Free Software Foundation), counting the entries or the grooves left by the cusps (Lowry et al., 2009) and delimiting them by the presence of shreds of skin or meat (Anislado-Tolentino et al., 2016). Since the bitemarks left on prey by Isistius leave a greater impression of the lower teeth (Ribéreau-Gayon et al., 2018), the counts obtained from the analysis were compared with the dental formulas of the lower jaw from the cookiecutter shark Isistius brasiliensis (12+1+13), the largetooth cookiecutter shark I. plutodus (9+1+9) (de Figueiredo Petean & De Carvalho, 2018) and the kitefin shark Dalatias licha (L 17–20) (Ebert et al., 2021).

The cobia had a TL of 82 cm, a standard length (SL) of 72 cm and weighed 8 kg. The three wounds were ovoid in shape with 25–26 lower teeth marks (Fig. 2b, c and d) and areas of less than 10 cm2. The measurements of the bite wounds are presented in the Table I. Wound number 1 showed clearer evidence of 26 teeth marks (Fig. 2b). According to the counts carried out and the calculated wound areas, it could be deduced that the predatory species that caused the bites was a shark of the genus Isistius, with high probability was Isistius brasiliensis.

Ribéreau-Gayon et al. (2018) indicates that the major axis interval for Isistius bites is between 1–10 cm and the area is less than 10 cm2. The measurements obtained in this study (Table I) show that the wounds are within the parameters established for the genus Isistius. Since D. licha (17–20) and I. plutodus (17–19) show fewer lower teeth than the dental marks (26) found in the bite wounds of the studied cobia (R. canadum), the species responsible for the feeding event was the cookiecutter shark I. brasiliensis.

Figure 2. a) Studied cobia (Rachycentron canadum) with three bite wounds (W) on its right flank; b) wound 1 (W1) lower teeth mark count; dots indicate the lower teeth marks, visible shreds of skin from marks 1 to 11; in marks 12 to 26 the trajectory of the dental cusps can be appreciated; c) wound 2 (W2) with 25 lower teeth marks and d) wound 3 (W3) with 25 lower teeth marks. Photographs by Rodolfo Castro-Barbosa.

Table I. Measurements of the wounds shown in the right flank of the cobia (Rachycentron canadum). Numbers only identify the wounds (see Figure 1).

Wound (W) number

Major axis (cm)

Minor axis (cm)

Number of

lower teeth marks

Perimeter (cm)

Area (cm2)

1

3.3

1.7

26

6.28

4.41

2

4.7

2.1

25

10.88

7.75

3

4.1

2.7

25

9.83

8.91

Following the criteria of Papastamatiou et al. (2010), the bite wounds were fresh, which indicates that they could have been made when the organism was caught in the fishing net. On the other hand, the authors mention that most pelagic fish, caught with longlines present more than two wounds. Likewise, according to Widder (1998), since I. brasiliensis is a slow swimmer, attacks on large free-swimming prey results in only one bite per organism, with the shark displaying a feeding behaviour in which it holds on to the prey using its modified suckerlike lips and pharynx to later penetrate the skin and tissue with its large, cutting-type lower teeth, using the momentum of the fast-swimming prey to generate the rotational energy necessary to detach the piece of tissue, securing the piece of flesh with its upper teeth while the sharks pulls free (Ribéreau-Gayon et al., 2018). The presence of three wounds in the studied cobia suggests that the bites were the result of opportunistic predation by I. brasiliensis, taking advantage of the fish’s inability to move when it was caught in the fishing net.

Some authors mention that cookiecutter sharks migrate at night from mesopelagic depths to shallower water (Compagno, 1984; Widder, 1998), and during the winter months (Papastamatiou et al., 2010), so the predatory events could be seasonal (Feunteun et al. 2018). This is also observed in the Mexican North Pacific of the Baja California peninsula, where during the winter and early spring months (February to March) that correspond to the fishing season of Pacific bluefin tuna Thunnus orientalis (Temminck & Schlegel, 1844), it is common for tuna caught using longlines to display bites of cookiecutter shark on their bodies.

According to Carlisle et al. (2021), I. brasiliensis preys upon epipelagic, mesopelagic, and vertically emigrant fishes (Table II) and presents a diel cycle, hunting during the day at the mesopelagic zone migrating, perhaps following prey, to the epipelagic zone at night. Fishing catches that normally show evidence of cookiecutter shark bites are tuna, billfish, and other large bycatch fishes at the offshore and open-ocean fisheries. For this work, the studied cobia was caught by artisanal fishery, at low depth (30 m) and at the littoral zone. The presence of the bite wounds by a cookiecutter shark on a prey in a low depth zone is evidence of their vertical migration diel behaviour. The cookiecutter shark, maybe I. brasiliensis, swim to the coastal zone in order to forage, and recently found a new prey, the cobia, on the continental shelf of southeastern Mexico. Because cobia along with other potential prey are important in the catches of small-scale coastal fisheries, it is necessary to establish a monitoring program to determine the diversity of prey of this type of shark in the coastal zone of the Gulf of Mexico.

Table II. List of cookiecutter shark Isistius brasiliensis identified fish prey species. Mesopelagic (MP), epipelagic (EP) and vertically emigrant fish species (VEF). The superscript letter in species column corresponding to: a, Carlisle et al. (2021); b, Hoyos-Padilla et al. (2013); c, Jones (1971); d, Nakano & Tabuchi (1990); e, Niella et al. (2018); f, Papastamatiou et al. (2010); g, this study.

Family

Species

Common name

Type

Lamnidae

Carcharadon carchariasb

White shark

VEF

Lampridae

Lampris guttatusf

Opah

MP

Ariommatidae

Ariomma sp.a

Driftfish

MP

Bramidae

Taractichthys steindachnerif

Sickle pomfret

MP

 

Brama japonicad

Pacific pomfret

MP

Gempylidae

Ruvettus pretiosusf

Oil fish

MP

Scombridae

Acanthocybium solandrif

Wahoo

VEF

 

Thunnus obesusf

Bigeye tuna 

VEF

 

Thunnus albacaresc

Yellow fin tuna

VEF

 

Katsuwonus pelamisf

Skipjack tuna

VEF

 

Euthynnus affinisc

Kawakawa

VEF

 

Euthynnus alletteratuse

Little tunny

VEF

 

Sarda sardae

Atlantic bonito

VEF

Carangidae

Caranx spp.c

Large jacks

VEF

 

Elagatis sp.c

Rainbow runners

VEF

Coryphaenidae

Coryphaena hippurusc

Dolphinfish

VEF

Istiophoridae

Makaira mazaraf

Pacific blue marlin

VEF

 

Tetrapturus audaxf

Striped marlin

VEF

 

Tetrapturus angustirostrisf

Shortbill sailfish

VEF

Rachycentridae

Rachycentron canadumg

Cobia

VEF

Xiphiidae

Xiphias gladiusf

Swordfish

VEF

Scomberesocidae          Cololabis sairaa                                           Pacific saury                    EP

ACKNOWLEDGEMENTS

This work was possible thanks to the support provided by the Instituto Mexicano de Investigación en Pesca y Acuacultura Sustentables (IMIPAS) through its Regional Center for Aquaculture and Fisheries Research in Ciudad del Carmen, Campeche by its artisanal fishing research program. To SNI-CONAHCyT for the support granted.

REFERENCES

Anislado-Tolentino, V., González-Medina, G. & Ramos-Carrillo, S. (2016). Los patrones de la mordida en víctimas de ataques de tiburón, como herramienta para la identificación de especies. Casos de estudio. Zihuatanejo, México. Mayo 2008. In L. F. Del Moral Flores, A. J. Ramírez Villalobos, J. A. Martínez Pérez, A. F. González Acosta & J. Franco López, Colecciones ictiológicas de Latinoamérica (pp. 558–576). Universidad Nacional Autónoma de México.

Best, P. B. & Photopoulou, T. (2016). Identifying the “demon whale-biter”: Patterns of scarring on large whales attributed to a cookie-cutter shark Isistius sp. PLOS ONE, 11(4), e0152643.

https://doi.org/10.1371/journal.pone.0152643

Carlisle, A. B., Allan, E. A., Kim, S. L., Meyer, L., Port, J., Scherrer, S. & O’Sullivan, J. (2021). Integrating multiple chemical tracers to elucidate the diet and habitat of Cookiecutter Sharks. Scientific Reports, 11. https://doi.org/10.1038/s41598-021-89903-z

Castro-Aguirre, J. L. & García-Domínguez, F. (1988). Sobre la presencia de Isistius brasiliensis (Quoy y Gaimard) (Squaliformes: Squalidae: Dalatiidae) en el Golfo de México. Con un elenco sistemático de las especies mexicanas pertenecientes al superorden Squalomorphii. Anales de la Escuela Nacional de Ciencias Biológicas, México, 32(1), 91–108. https:// biblat.unam.mx/hevila/AnalesdelaEscuelaNacionaldeCienciasBiologicas/1988/vol32/no14/5.pdf

Compagno, R. J. V. (1984). FAO species catalogue. Sharks of the world. An Annotated and Illustrated Catalogue of Shark Species Known to Date Part 2 – Carcharhiniformes. FAO Fisheries Synopsis, 4(125): Part 2. 655 p.

de Figueiredo Petean, F. & R. de Carvalho M. (2018). Comparative morphology and systematics of the cookiecutter sharks, genus Isistius Gill (1864) (Chondrichthyes: Squaliformes: Dalatiidae). PLoS ONE 13(8): e0201913. https://doi.org/10.1371/journal.pone.0201913

DOF, Diario Oficial de la Federación (2012). Acuerdo por el que se da a conocer la Actualización de la Carta Nacional Pesquera. June 06 2012 [On line]. Avalaible on: https://www.dof.gob. mx/nota_detalle.php?codigo=5249902&fecha=06/06/2012#gsc.tab=0

Dwyer, S. & Visser, I. N. (2011). Cookie cutter shark (Isistius sp.) Bites on cetaceans, with particular reference to killer whales (Orca) (Orcinus orca). Aquatic Mammal, 37(2), 111–138. https://doi.org/10.1578/am.37.2.2011.111

Ebert, D. A., Dando, M. & Fowler, S. (2021). Sharks of the World: A complete guide. Princeton University Press.

Feunteun, A., de Schrevel, C., Verhaegen, M., Chevallier, D., Duchemin, M., Ziani, N., & de Montgolfier, B. (2018). First evaluation of the cookie-cutter sharks (Isistius sp.) predation pattern on different cetacean species in Martinique. Environmental Biology of Fishes,

101(5), 749–759. https://doi.org/10.1007/s10641-018-0735-1

Gallo-Reynoso, J. P. & Figueroa-Carranza, A. L. (1992). A cookiecutter shark wound on a Guadalupe fur seal male. Marine Mammal Science, 8(4), 428–430. https://doi. org/10.1111/j.1748-7692.1992.tb00060.x

Grace, M. A., Dias, L. A., Maze-Foley, K., Sinclair, C., Mullin, K. D., Garrison, L. & Noble, L. (2018). Cookiecutter shark bite wounds on cetaceans of the Gulf of Mexico. Aquatic Mammals, 44(5), 491–499. https://doi.org/10.1578/AM.44.5.2018.491

Honebrink, R., Buch, R., Galpin, P. & Burgess, G. H. (2011). First documented attack on a live human by a cookiecutter shark (Squaliformes, Dalatiidae: Isistius sp.). Pacific Science, 65(3), 365–374. https://doi.org/10.2984/65.3.365

Hoyos-Padilla, M., Papastamatiou, Y. P., O’Sullivan, J. & Lowe, C. G. (2013). Observation of an attack by a Cookiecutter shark (Isistius brasiliensis) on a white shark (Carcharodon carcharias). Pacific Science, 67(1), 129–134.  https://doi.org/10.2984/67.1.10

Jones, E. C. (1971). Isistius brasiliensis, a squaloid shark, the probable cause of crater wounds on fishes and cetaceans. Fishery Bulletin, 69(40), 791–798.

Lowry, D., Fagundes de Castro, A. L., Mara, K., Whitenack, L. B., Delius, B., Burgess, G. H. & Motta, P. (2009). Determining shark size from forensic analysis of bite damage. Marine Biology, 156(12), 2483–2492. doi:10.1007/s00227-009-1273-3

Menezes, R., Marinho, J. P. D., de Mesquita, G. C. & da Silva, G. B. (2022). Cookiecutter shark (Isistius spp.) bite patterns on pelagic fishes in aggregated schools in the western equatorial Atlantic Ocean. Environmental Biology of Fishes, 105, 519–530. https://doi.org/10.1007/ s10641-022-01257-1

Muñoz-Chápuli, R., Salgado, J. C. R. & de la Serna, J. M. (1988). Biogeography of Isistius brasiliensis in the north-eastern Atlantic, inferred from crater wounds on swordfish (Xiphias gladius). Journal of the Marine Biological Association of the United Kingdom, 68(2), 315–321. https://doi.org/10.1017/s0025315400052218

Nakano, H. & Tabuchi, M. (1990). Occurrence of the cookiecutter shark Isistius brasiliensis in surface waters of the north Pacific Ocean. Japanese Journal of Ichthyology, 37(1):60–63.

Niella, Y. V., Duarte, L. A. G., Bandeira, V. R., Crespo, O., Beare, D. & Hazin, F. H. V. (2018). Cookie-cutter shark Isistius spp. predation upon different tuna species from the southwestern Atlantic Ocean. Journal of Fish Biology, 92(4), 1082–1089. https://doi.org/10.1111/ jfb.13569

Papastamatiou, Y. P., Wetherbee, B. M., O’Sullivan, J., Goodmanlowe, G. D. & Lowe, C. G. (2010). Foraging ecology of Cookiecutter Sharks (Isistius brasiliensis) on pelagic fishes in Hawaii, inferred from prey bite wounds. Environmental Biology of Fishes, 88(4), 361–368. https://doi.org/10.1007/s10641-010-9649-2

Reddacliff, G. (1988). Crater wounds in marine mammals. In M. L. Augee (Ed). Marine mammals of Australasia: Field biology and captive management (133–134). Royal Zoological Society.

Retzer, M. E. (1990). New records and range extensions of twelve species of fishes in the Gulf of Mexico. Northeast Gulf Sciences, 11(2), 137–142. https://doi.org/10.18785/negs.1102.06

Ribéreau-Gayon, A., Carter, D. O., & Regan, S. (2018). New evidence of predation on humans by cookiecutter sharks in Kauai, Hawaii. International Journal of Legal Medicine, 132, 1381–1387. https://doi.org/10.1007/s00414-018-1786-8

Ribéreau-Gayon, A., Rando, C., Schuliar, Y., Chapenoire, S., Crema, E. R., Claes, J., Seret, B., Maleret, V. & Morgan, M. (2017). 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. International Journal of Legal Medicine, 131, 423–432. https://doi.org/10.1007/s00414-016-1449-6.

Ritter, K. E. & Levine, M. (2004). Use of forensic analysis to better understand shark attack behavior. The Journal of forensic odonto-stomatology, 22(2), 40–46. https://ojs.iofos.eu/ index.php/Journal/article/view/1701/307

Ruiz-Abierno, A., Rojas-Corzo, A. & Angulo-Valdés, J. A. (2016). Primer reporte de tiburón cigarro (Isistius brasiliensis) para aguas cubanas. Revista de Investigaciones Marinas, 36(1), 158–161. https://biblat.unam.mx/hevila/Revistadeinvestigacionesmarinas/2016/ vol36/no1/10.pdf

Shaffer, R. V. & Nakamura, E. L. (1989). Synopsis of biological data on the cobia, Rachycentron canadum (Pisces: Rachycentridae) (NOAA Techical Report NMFS, 82). FAO. https:// repository.library.noaa.gov/view/noaa/5898

Souto, L. R. A., Abrão-Oliveira, J. G., Maia-Nogueira, R. & Dórea-Reis, L. W. (2009). Interactions between subantarctic fur seal (Arctocephalus tropicalis) and cookiecutter shark (Isistius plutodus) on the coast of Bahia, north-eastern Brazil. Marine Biodiversity, 2. https://doi.org/10.1017/S1755267209000992

Strasburg, D. W. (1963). The diet and dentition of Isistius brasiliensis, with remarks on tooth replacement in other sharks. Copeia, 1963(1), 33–40. https://doi.org/10.2307/1441272

Widder, E. A. (1998). A predatory use of counter illumination by the squaloid shark, Isistius brasiliensis. Environmental Biology of Fishes, 53(3), 267–273. https://doi. org/10.1023/A:1007498915860

Zidowitz, H., Fock, H. O., Pusch, C. & von Westernhagen, H. (2004). A first record of Isistius plutodus in the north-eastern Atlantic. Journal of Fish Biology, 64(5), 1430–1434. https://doi.org/10.1111/j.0022-1112.2004.00382.x

Citation: Wakida-Kusunoki, A. T., Anislado-Tolentino, V., Rosales-Vásquez, J. I., Castro-Barbosa, R., & Del Moral-Flores, L. F. (2024). A new record of bony fish prey for the genus Isistius (Chondrichthyes: Dalatiidae) in a coastal zone of southeastern Mexico. Novitates Caribaea, (23), 77–85. https://doi.

org/10.33800/nc.vi23.348