An Examination of the Effects of Dorsal Fin-Mounted SPOT on Carcharodon carcharias, the Great White Shark

Abstract

This opinion piece presents empirical evidence to examine possible negative consequences of the use of penetrative tagging as used on the great white shark (GWS). Tagging programs currently using this method attach SPOT (Spatial Positioning Only Tags) using corrodible bolts inserted through the dorsal fin while the shark is taken out of water. Such methods can cause harm to the tagged individual. Possible adverse effects include impacts on growth, tag biofouling, wounds, heightened stress, and hemorrhaging. This method may adversely impact dorsal fin structure and the shark’s hydrodynamics. As a result, data collected may not be reflective of natural behavior. Bolted SPOT are semi-permanently affixed to the shark but can have a battery life of approximately 3.5 years. Most of these tags (69%) ceased transmitting in less than 2 years. Alternative tagging technologies exist as more humane options.

1. Introduction

There are few studies that have directly investigated the effects of penetrative tagging methods on elasmobranchs, yet these tagging programs are common [1,2,3,4,5,6,7,8,9]. For example, Carcharodon carcharias (GWS, great white shark)-tagging activities have received extensive media attention, especially on “Shark week”. The primary goal for tagging GWS is to obtain shark migration data [10]. Migration data add essential information to the knowledge of GWS ecology.

This review focused on SPOT (Smart Position Only Tags), a commonly employed method [7,9]. SPOT are secured by bolting the tag into the first dorsal fin. The penetrative nature of attaching these tags damages the skin and internal structures. The paper by Jewell et al. [8] raised the concern of negative long-term consequences from these bolted tags. Penetrative tagging has caused wounds and an accumulation of biofouling on GWS dorsal fins and tags [7,8]. Additionally, this tagging method may affect fin growth in juvenile GWS [8]. These effects have the capacity to compromise the hydrodynamic role of the dorsal fin and alter natural behavior [11].

This paper also reports evidence indicating that hemorrhaging occurs when a GWS is removed from the water and placed on a flat platform for tagging. Typical practice in tagging programs involves removing GWS from the water so that the research team has complete access to the shark for collecting samples “https://www.ocearch.org/tracker/ (accessed on 7 May 2024)”. GWS, like other elasmobranchs, are cartilaginous and lack a solid, non-flexible rib cage to protect vital organs from damage [12]. Due to this skeletal flexibility, excessive pressure is placed on the internal organs when the weight of the shark is not properly supported when GWS is out of water. This phenomenon also has occurred in beached whales, which have a stronger, bony skeleton [13]. This trauma leads to dark hemorrhagic bands forming ventrally along the snout, jaw area, underbelly, below the gills, and caudal peduncle. Other studies have used less harmful methods, whereby the shark is in a harness or restrained via a tail rope in water while being handled [14]

Tag longevity was also examined in GWS equipped with a dorsal-fin-mounted SPOT. The purpose was to quantify tag longevity and evaluate whether tags were lasting for the total transmission duration as programmed by researchers.

2. Materials and Methods

SPOT longevity data were obtained from the Ocearch tagging program website “https://www.ocearch.org/tracker/ (accessed on 7 May 2024)”. These data are summarized in Table S1. Longevity was determined by the number of days the tag was displayed as transmitting. The data were then compiled into a histogram with bin lengths of one year. Tag longevity data for other shark species were obtained from the literature and are summarized in Table S1. Images of GWS with likely hemorrhaging are published on the Ocearch website “https://www.ocearch.org/tracker/ (accessed on 7 May 2024)”. These data are recorded in Table S2.

3. Results: SPOT Longevity

One commonly used tag model, SPOT-257, should transmit for approximately 3.5 years according to the manufacturer, Wildlife Computers. SPOT-257 was a commonly used tag by Ocearch (Wildlife Computers, pers comm October 2023). The majority of SPOT (69%) used by Ocearch ceased transmitting in less than 2 years (Figure 1). SPOT longevity data for Prionace glauca, Sphyrna mokarran, and Sphyrna lewini showed durations of less than a year (

Table 1. Longevity data from other shark species also tagged with a bolted dorsal fin SPOT.

Citation	Species	Tag Model	Programmed Tag Lifetime (Days)	Actual Tag Lifetime (Days)
Stevens et al. [15]	Prionace glauca	SPOT-4	159	52
Stevens et al. [15]	Prionace glauca	SPOT-4	159	0
Stevens et al. [15]	Prionace glauca	SPOT-4	159	129
Stevens et al. [15]	Prionace glauca	SPOT-4	159	137
Stevens et al. [15]	Prionace glauca	SPOT-4	159	6
Stevens et al. [15]	Prionace glauca	SPOT-5	159	159
Heim et al. [16]	Sphyrna mokarran	SPOT-364	130	114
Heim et al. [16]	Sphyrna mokarran	SPOT-364	130	78
Heim et al. [16]	Sphyrna mokarran	SPOT-364	130	51
Heim et al. [16]	Sphyrna lewini	SPOT-364	130	93
Heim et al. [16]	Sphyrna lewini	SPOT-364	130	178

) [15,16,17], although SPOT-257 was not used in these studies (Stevens et al. [15]: SPOT-4 and -5; Heim et al. [16]: SPOT-364; Drymon and Wells [17]: SPOT-6). All tags were manufactured by Wildlife Computers. Programmed tag battery lifetimes are listed in Table 1. The study on S. mokarran by [17] was short term and is not included in Table 1.

4. Discussion:

SPOT use the Argos satellite system to approximate a tagged individual’s position “https://wildlifecomputers.com/ (accessed on 7 May 2024)”. Depending on the make and model of the tag, accuracy and resolution vary (see “https://wildlifecomputers.com/ (accessed on 7 May 2024)” for specifics). SPOT rely on the tag’s antenna breaking the surface [7]. As a result, gaps in data have arisen when these tags are used on species that remain submerged for extended periods [18]. To apply the tag, some studies remove the shark from the water [18,19]. The tag is then secured with nuts and corrodible bolts through a hole drilled into the fin. This attachment method is meant to be permanent. Possible reasons for reduced longevity in satellite tags are: (1) technical failure, (2) the tag battery running out, and (3) mortality [15,17,20].

There are six possible adverse effects resulting from the use of bolted SPOT: (1) growth, (2) tag biofouling, (3) wounds, (4) stress, (5) hemorrhaging and (6) drag on swimming hydrodynamics.

4.1. Growth

Studies investigating the effects of penetrative tagging methods on growth have indicated that effects are species specific and depend on food availability, injuries sustained during the tagging process, and irritation caused by the tags [1]. A literature review [1] summarized that growth was affected in the following: Ginglymostoma cirratum, Squalus acanthias, Sphyrna tiburo, Negaprion brevirostris, Mustelus lenticulatus, Carcharhinus tilstoni, and Carcharhinus sorrah. The growth rate of Negaprion brevirostris was not greatly affected by tagging when food was not a limiting factor [21]. Tagging did not affect the growth rate of Galeocerdo cuvier [22]. Changes to body size caused by tagging were deemed non-detrimental in Hemiscyllium ocellatum [23]. Effects on growth due to various tagging methods may be associated with body size at the time of tagging. For example, juvenile N. brevirostris experienced a significantly decreased growth rate when tagged with dart tags [24]. Also, bolted SPOT have been implicated in affecting the growth of sub-adult GWS dorsal fins, resulting in deformation of a single shark’s fin, when the tag did not release within the 12–24-month window recommended for deployment by Jewell et al. [8]. The authors concluded that these tags should not be used on juvenile GWS for this reason [8].

4.2. Tag Biofouling

Antifouling paints have been used to prevent tag biofouling [7,8]. Biofouling involves the colonization of algae and other micro and macro-organisms when a biofilm forms on surfaces exposed to seawater [25]. The first published study to report biofouling on SPOT using photographic evidence was Jewell et al. [8]. Fouling occurred in one shark’s fin ~5 months after applying antifouling paint to the tag [8] (Figure 2). Hammerschlag et al. [7] noted that tagging may facilitate parasite recruitment. Wounds and infections surrounding the area of insertion were also identified as risks [7]. Tissue degradation and infection caused by SPOT biofouling has been documented in dolphins [26].

4.3. Wounds

Jewell et al. [8] found that bolted SPOT become biofouled and cause hyperpigmentation and structural damage to the dorsal fin (Figure 3). Of the images of 15 tagged GWS, 8 had signs of hyperpigmentation and 2 had fouling on their tags. One individual had both fouling and a dorsal fin that leaned to the left. The leaning of the dorsal fin was thought to be due to (1) the weight of the algal growth on the tag, (2) the weight of the tag, or (3) the combined weight of both the algae and the tag [8].

4.4. Stress

Stress is defined as “a physiological cascade of events that occurs when the organism is attempting to resist death or reestablish homeostatic norms in the face of insult” [27]. Factors that have led to changes in homeostatic state in elasmobranchs during tagging are: time out of the water, cortisol and lactate levels due to time fighting on hook and line, and muscular fatigue [28]. Stress responses have been observed and measured in field studies that deploy penetrative tags [28]. However, studies on physiological stress responses in GWS being tagged with dorsal fin-mounted SPOT have not yet been conducted. Additionally, stress responses in elasmobranchs have been found to be species specific [29].

Stress responses can also be triggered by pain. As described in Lacap [30], elasmobranchs possess nociceptors in the snout and on the top of the head. Nociceptors are a prerequisite for pain perception. Lacap [30] concluded that a shark’s capacity to feel pain should not be ruled out.

4.5. Hemorrhaging

Elasmobranchs appeared to hemorrhage in response to induced trauma due to handling while on tagging platforms. Crushing of internal organs is also a recognized issue and has been mitigated using supports such as harnesses [14]. Hemorrhagic bands have formed ventrally along the snout, abdomen, and caudal peduncle of GWS (Figure 4). Hemorrhaging has been characterized by red banding on tissues [31].

4.6. Impact on Fin Hydrodynamics

The dorsal fin of GWS is a dynamic stabilizer and penetrative tagging may inhibit its function in swimming. GWS are thunniform swimmers [11,32]. Thunniform swimmers rely on the caudal hydrofoil to maintain thrust when swimming at high speeds [32,33]. The thunniform mode of swimming is primarily driven by caudal fin oscillations [34,35]. A hydrodynamic consequence stemming from this swimming mode is the potential recoil brought about via lateral oscillations of the head. The dorsal fin of GWS acts as a dynamic stabilizer during swimming [11]. The dorsal fin acts as a center of mass point of the shark. Additionally, lamnid sharks lack a ventrally flattened head. A ventrally flattened head reduces roll [11]. To compensate, the lamnid dorsal fin acts as an additional dynamic stabilizer to reduce roll [11,36]. Thus, the location and mass of the dorsal fin act as a dynamic stabilizer while the shark is actively swimming.

Other than the location of the dorsal fin itself, the shark’s ability to transfer tensile strength between the perimysial connective tissues (PCTs) and inner-musculature tissues of the body to those located within the dorsal fin also contributes to the dorsal fin’s role as a dynamic stabilizer [11]. PCTs extend approximately one-quarter of the way into the dorsal fin and are attached to cartilaginous radials via dense cartilaginous tissue sheaths that wrap around the radials [11]. The PCTs also attach to the dermis and dorsal septum [11]. The radials themselves are attached via connective tissue to stiff pterygiophores located at the base of the dorsal fin and extend approximately halfway through the fin [11]. The next layer of tissues, the stratum compactum, is composed of scattered, unstacked bundles of ceratotrichia coupled with groups of fiber bundles [11]. The fiber bundles are stacked to promote tensile strength while not preventing fiber movement [11]. The ceratotrichia are filamentous dermal fibers that extend throughout the length of the dorsal fin and act as structural support [37]. The ceratotrichia are flexible and, when perimysial muscle fibers contract within the body cavity, the contraction places tension on the ceratotrichia [11]. This stiffens the dorsal fin in the direction contralateral to the contracting fibers and increases hydrostatic pressure within the body. The opposite occurs when the fibers are relaxed, and hydrostatic pressure is reduced [38]. Thus, changes in hydrostatic pressure initiate tension or relaxation of the dorsal fin. Lingham-Soliar [11] describe this mechanism as something akin to the rigging of a ship’s mast. Thus, the shark’s dorsal fin morphological function is being impacted by drilling holes in it. The shark’s dorsal fin is an integral part of the body and covered by skin and placoid denticles [12]. It is not like a teleost’s fin, which can be torn and will regrow. However, elasmobranchs have recovered from partial removal of the dorsal fin [39,40]. However, this may impair natural behaviors such as predation [39]. Also, securing a SPOT on the dorsal fin may also affect dorsal fin hydrodynamics due to added drag and an uneven weight distribution across the dorsal fin.

4.7. Alternative Tagging Methods and Future Directions

The great white shark (GWS) is listed as “vulnerable” by the International Union for Conservation of Nature (IUCN) [41]. Concern around using SPOT bolted to the fin stems from how researchers only obtaining a relatively short-term dataset from individual tags that (1) are meant to be semi-permanently affixed to the dorsal fin, which may have harmful effects on tagged individuals, and (2) that such harmful methods are imposed upon a vulnerable species. However, individual tag data can be compiled into a larger dataset [42,43].

Other tagging methods, such as dart and implanted tags, have also been used on elasmobranchs [1]. Dart tags are conventionally deployed using a harpoon-like device to stab the tag into the upper epaxial musculature while the shark is in the water or on a boat [44]. Dart tags eventually accumulate biofouling organisms that add drag to the tag. Acoustic tags have been surgically implanted into the abdominal cavity [1]. Surgical implantation has taken place both with the shark in the water and on the deck of a boat [1]. In addition to the invasiveness of the surgical procedure, changes in natural behavior have occurred post-implantation. For example, tagged sharks have been observed leaving their aggregation areas after the procedure [Lobel pers. obs]. Both of these tags have associated stress due to handling, as well as direct physical trauma with resulting wounds. Dart tags have been used with satellite transmitters but obviously these do not work with a surgically implanted tag.

There are two examples of alternative methods that either reduce or eliminate adverse effects of bolting tags: bracelet tagging and fin clamping. A bracelet tag is a non-penetrative method that is temporary [45,46]. It has been used with acoustic tags that are attached to a degradable bracelet that encircles the caudal peduncle. These are attached to a shark that is in water and has been rendered into tonic immobility as the shark is brought alongside a boat [45,46]. Bracelet tags have not yet been paired with SPOT, but alterations are possible that could allow an antenna to transmit, such as taping the satellite antenna to the upper caudal fin. Fin clamps are also non-penetrative and temporary [6,47]. Tags are slid onto a clamp attached to the end of a tagging pole and are secured to the dorsal fin after the trigger on the pole is activated [6,47]. The tag is applied to free-swimming sharks at the surface [6,47]. Detachment time can be pre-programmed [6,47]. Fin clamps have caused necrosis in the dorsal fin 5 weeks post-application [47]. This is one reason fin clamps are currently deployed for short time intervals. Fin clamp design needs to be further innovated to eventually be attached long term without harm.

5. Conclusions

Due to the structural damage to the dorsal fin, as well as possible health consequences and data concerns, it is recommended that alternatives to penetrative tagging methods be developed. No other species, especially “vulnerable” ones, are subject to such invasive tagging methods. Non-penetrative methods, such as bracelet tags and fin clamps, should be further engineered to improve elasmobranch welfare and obtain data that are reflective of natural behavior and not a shark’s response to invasive wounds.