Abstract

The sublethal effects of retained fishing hooks on sharks remain largely unknown, with limited research assessing their long-term impact on individual health and survival. In a previous study, we reported a high prevalence of retained hooks in free-ranging blue sharks observed in the NW Mediterranean Sea. These findings ranked among the highest values reported within the literature. To further investigate this issue, we conducted a study during 2023 and 2024, carrying out 111 pelagic shark surveys (898.7 hours), during which we observed 135 non-YOY blue sharks. We could assess the prevalence of retained fishing hooks (RH) and trailing lines in 121 of these free-ranging blue sharks. A 20% of sharks showed RH or scars derived from hooks. Eight of these specimens exhibited severe lesions (SL) (6.6% of the whole sample): lower jaw dislocation, nictitating membrane protrusion, presence of fibronecrotic tissue and neurological signs, consistent with ataxia, uncoordinated swimming movements and loss of buoyancy. The 33.3% of sharks affected by RH presented SL. SL were found significantly more frequently in specimens affected by RH than those that had not been previously captured. None of the blue sharks without RH or signs of having had them showed evidence of a SL. Such injuries are more frequent than previously suspected and may severely impact the sharks’ ability to feed and survive. Our results reinforce concerns that Western Mediterranean blue shark populations may be seriously exposed to by-catch events and their consequences, classified as a “Critically Endangered” species.

Keywords:Blue shark; Prionace glauca; Hooks; Lesion; Conservation; By-catch; Longline fishery

Keywords:CCC: Cap de Creus Submarine Canyon; dF: Degrees of freedom; IRHP: prevalence of internally retained hooks within the aerodigestive tract; IRHRHP: prevalence of IRH within sharks affected by retained hooks; IUCN: International Union for the Conservation of Nature; NAP: prevalence of active necrotic areas; NARHP: prevalence of NA within sharks affected by retained hooks; NSDMP: SL related to neurologic signs and dysfunctional movements; NSDMRHP: prevalence of NSDM within sharks affected by retained hooks; PVC: Polyvinyl chloride; RH: Retained hook; RHP: Retained hook prevalence; SL: severe lesion; SLEP: prevalence of SL affecting eyes; SLERHP: prevalence of SL affecting eyes within sharks affected by retained hooks.; SLJP: prevalence of SL affecting jaws and their functionality; SLJRHP: prevalence of SL affecting jaws within sharks affected by retained hooks; SLP: prevalence of SL in all sharks observed; SLRHP: prevalence of SL in all sharks affected by retained hooks; TL: Total length; YOY: Young of the Year

Introduction

The pervasive threat of bycatch in pelagic longline fisheries has long been recognized as a primary driver of shark populations decline globally [1,2]. In the Mediterranean Sea, the blue shark (Prionace glauca) has been particularly affected by unintentional fisheries interactions, leading to its designation as Critically Endangered in the region by the IUCN [3]. Historically, bycatch analyses on sharks have predominantly concentrated on immediate and delayed mortality [4,5]; in contrast, sublethal injuries -particularly those resulting from retained fishing hooks- remain a largely unexplored yet critical aspect of these interactions.

Retained hooks, both externally and internally lodged, can induce a variety of lesions ranging from localized fibrosis and tissue necrosis to more complex systemic pathologies [6,7]. These injuries may not be immediately fatal but can compromise vital functions such as feeding, locomotion, and sensory input, potentially leading to starvation, impaired growth, secondary infections, or chronic inflammation [8,9]. Notably, cases of mandibular dislocation, nictitating membrane paralysis, and internal hook retention with associated behavioral dysfunctions suggest the occurrence of severe anatomical and neurological impairments in blue sharks exposed to long line gear [6,10-12]. Despite the critical relevance of these conditions, very little attention has been paid to systematically evaluate the prevalence and pathophysiological consequences of retained hooks in elasmobranchs under natural conditions. In previous works [12,13], a surprisingly high Retained Hook Prevalence (RHP) of over 20% was documented in free-ranging P. glauca from the NW Mediterranean. Moreover, several of these individuals exhibited permanent lesions related to the by-catch capture by means of hooks.

The present study aims to expand on those findings by focusing specifically on severe and functionally significant injuries. Specifically, our objectives were:

a) to identify and classify the range of severe injuries associated with retained hooks and lines

b) to establish whether these cases of severe injuries are found in the entire population of blue sharks or mainly linked to specimens that have presented RH

c) to quantify their prevalence both in the general population and among affected blue sharks over a two-year period (2023-2024) in the Cap de Creus Submarine Canyon (CCC), a main breeding and nursery aggregation area for this species [14-16]

By combining underwater visual assessments with injury classification grounded in comparative pathology, results from this study will provide a more comprehensive understanding of the potential implications of bycatch on sharks’ individual fitness and population sustainability.

Methods

Study area and data collection

This study was located on a section of 25 × 19 km from the upper part of the CCC, in the NE of the Iberian Peninsula. This area is characterized by a permanent marine circulation system, which contributes to its status as a significant biodiversity hotspot in the NW Mediterranean Sea -including for sharks- as demonstrated in previous works [12,14].

We collected data over two consecutive years (2023 and 2024) using a standardized, non-invasive technique. Sharks were studied following the method described by Riera-Renter and col. [12], which involved the attraction of pelagic sharks by means of chumming and perforated Polyvinyl chloride (PVC) tubes containing sardines.

Underwater footage and photographs were initially taken from the boat to document sharks before they potentially left the area. Once sharks were habituated to human presence, researchers entered the water cautiously using snorkelling and freediving to obtain additional close-range images. All images and videos were obtained using a Canon G7X still camera with a Nauticam NA-G7XMKII waterproof case, an Olympus Tg6 camera and two GoPro Hero 10 cameras. Whereas in a part of 2023 sharks were measured by direct comparison between boat equipment and structures, in 2024, the Olympus Tg6 camera was equipped with a device with two parallel lasers (Glowdive, model Acho II) separated by 20 cm, that allowed us to measure the shark’s length with precision [16,17]. These methods enabled the collection of the following information:

a) total length estimation (TL)

b) sex determination

c) presence and characteristics of RH and/or their scars and trailing lines

d) presence of injuries and their classification.

Additionally, underwater footage and photographs were analyzed to identify injuries and abnormal behaviours potentially - but not directly- linked to the impact of hooks, whether currently present or from past exposure. All these parameters aided with the individual recognition of sharks [12].

Age class assessment and classification of hook-related injuries in observed sharks

Sharks were classified into age classes according to their TL estimation [12,16], being defined as follows: young-of-the-year (YOY), juveniles (individuals of ages 1+, 2+ and 3+ years), subadults (4+ years) and adults (5+ o more years).

Scars, stains, spots, abrasions, lacerations, fibronecrotic injuries and other specific but less common symptoms, potentially associated to hook-injuries, were identified as lesions. Among these, severe lesions (SL) were also identified and classified according to their anatomical position (jaw or eyes, for example) when possible. Severe lesions were defined as physical injuries or infections caused by an external cause that produced a permanent physical damage or abnormal behaviour, negatively impacting on their normal life, their fitness or thriving. Each SL was then classified into the following categories: SL affecting jaws and their functionality (SLJ); SL affecting eyes and/or their functional structures, such as the nictitating membrane (SLE); active necrotic areas (NA); SL related to neurologic signs and dysfunctional movements (NSDM); and internally retained hooks within the aerodigestive tract, revealed by lines merging from the mouth (IRH).

Statistical analysis

All observed YOY were excluded from the analysis due to lower catchability with standard hook-fishing methods. First, we calculated the “retained hook prevalence” (RHP), defined as the probability (ranging from 0 to 1) that a shark of a specific age, sex or period exhibited a retained hook and/or derived lesion caused by hooks at the time of observation. We also calculated the probability (prevalence, ranging from 0 to 1) of finding sharks with specific SL, defined as follows:

a) SLJP: prevalence of SL affecting jaws and their functionality

b) SLEP: prevalence of SL affecting eyes and/or their functional structures, such as the nictitating membrane

c) NAP: prevalence of active necrotic areas

d) NSDMP: SL related to neurologic signs and dysfunctional movements

e) IRHP: prevalence of internally retained hooks within the aerodigestive tract

f) SLP: prevalence of SL as a whole (SLP = SLJP + SLEP + NAP + NSDMP). IRHP was not included in this formula because the only affected shark exhibited both an IRH and NSDM.

We also calculated the probability (prevalence, ranging from 0 to 1) of finding sharks with specific SL within only sharks affected by hooks, as follows:

g) SLJRHP: prevalence of SL affecting jaws within sharks affected by retained hooks.

h) SLERHP: prevalence of SL affecting eyes within sharks affected by retained hooks.

i) NARHP: prevalence of NA within sharks affected by retained hooks.

j) NSDMRHP: prevalence of NSDM within sharks affected by retained hooks.

k) IRHRHP: prevalence of IRH within sharks affected by retained hooks.

l) SLRHP: prevalence of SL as a whole within sharks affected by retained hooks (SLRHP = SLJRHP + SLERHP + NARHP + NSDMRHP). Also not including IRHRHP for the same reason.

The Chi-Square test was used to compare the absolute frequencies observed across the different analyses.

Results

Residual hooks, trailing lines and derived lesions

From April 2023 to October 2024, we carried out 111 pelagic shark surveys (898.7 hours), during which we observed 135 non- YOY blue sharks, and only one was seen twice. Among all observed sharks, 121 (87 in 2023, and 34 in 2024) could be studied in detail. Among the two years, 24 sharks showed either retained hooks or scars derived from rejected hooks (RHP=0.20). No significant differences were found between the 2023 prevalence (RHP=0.20) and the 2024 prevalence (RHP=0.20) (χ² = 0.0113; 1 dF; p=0.916). Among the 24 affected sharks, 54.2% of the specimens also presented trailing lines (8 in 2023 and 5 in 2024).

SL derived from residual hooks

Among the 121 sharks studied in detail, 8 specimens presented SL (SLP = 0.066), differences being not significant between 2023 (SLP = 0.046) and 2024 (SLP = 0.118) (χ² = 2.034; 1 dF; p=0.154) (Table 1).

In general, the prevalence of the different types of SL ranged from 0.008 to 0.017. Especially important was the fact that some of these lesions previously considered as rare or infrequent, were observed in different specimens and/or in both years. In both 2023 and 2024 we found sharks with lesions in the jaw compatible with mandible dislocation (Figure 1), and in the eyes (Figure 2). Particularly, one of the last affected sharks exhibited a persistent protrusion of the nictitating membrane, consistent with trauma-induced dysfunction (Figure 2); and the other one showed scleral discoloration, corneal hyperpigmentation, euriblepharon and exophtalmos. In 2023 we found two sharks with fibronecrotic injuries (Figure 3), and in 2024 we detected sharks with no visible external hook but presenting nylon lines merging from the buccal cavity (Figure 4), suggesting an internal hook retention. One of the last specimens also exhibited neurological signs, consistent with ataxia, uncoordinated swimming movements, and loss of buoyancy.

When considering only the sharks affected by retained hooks (n=24), prevalence raised considerably. Nearly one out of three affected-by-hooks sharks presented a severe lesion (SLAHP = 0.333). The prevalence of sharks exhibiting severe lesions was higher in 2024 (SLAHP = 0.571) compared to 2023 (SLAHP =0.235), but differences between both years were not statistically significant (χ2 = 1.2353, with Yates correction factor; 1 dF; p > 0.05) (Table 2). No significant differences in the presence of SL were observed between males and females (χ² = 2.524; 1 dF; p = 0.112), nor between juveniles and non-juveniles (including preadults 4+ and adults 5+) (χ2 = 0.010; 1 dF; p = 0.920).

Furthermore, SL were found significantly more frequently in specimens presenting retained hooks or evidence of having had them, than those that had not been previously captured using hooks (χ2 = 34.662, with Yates correction factor; 1 dF; p < 0.0001). In fact, all specimens presenting a SL had or had evidence of having a hook previously, while none of the blue sharks without retained hooks or signs of having had them showed evidence of a SL.

Discussion

Our study confirmed that the high prevalence of RH previously reported [12] persists over time and revealed that approximately a quarter of the total blue sharks (Prionacea glauca) surveyed in the NW Mediterranean population exhibit signs of RH or associated lesions. Among the affected individuals by RH, around 33.3% presented visible severe lesions. Notably, all individuals exhibiting severe lesions also showed clear evidence of prior interaction with fishing gear (bycatch events). These findings indicate that fishing gear-related trauma may be more common and detrimental to sharks than previously recognized.

We reported two individuals with mandible dislocation, most likely related to a retained hook due to the presence of a circular perforation in the same oral commissure. In sharks, proper feeding mechanics are dependent on complex jaw kinematics. For instance, in carcharhiniforms such as P. glauca, feeding involves a kinetic suspension system in which the hyomandibulae are posteriorly oriented and the palatoquadrate articulates with the neurocranium via flexible ethmopalatine ligaments [18,19]. During prey capture, the hyomandibulae swing laterally, rotating the upper jaw ventrally and outward to enable a gouging bite, often accompanied by vigorous lateral head movements [20,21]. This mechanism allows these predators to excise tissue from prey too large to be fully engulfed, a strategy that is ecologically essential given their pelagic lifestyle and prey types. Therefore, any type of injury that compromises the functional integrity of the jaw apparatus impairs the shark’s ability to capture and process prey. Given the dependence of pelagic sharks on active predation for survival, such lesions may lead to chronic undernourishment and potentially fatal declines in body condition, particularly in juveniles or subadults, which have high energetic demands [4,6].

Periocular injuries are frequently observed in wild sharks and may result from intraspecific aggression, predator-prey interactions, or anthropogenic sources such as propellers [22]. In our study, we observed two blue sharks with eye lesions. Notably, one individual exhibited a persistent protrusion of the third eyelid (nictitating membrane), along with a nylon line emerging from the same side of the buccal cavity, suggesting a potential link between the ocular trauma and an internal retained hook. In P. glauca, the third eyelid is highly developed and composed of dense connective tissue covered by placoid scales [23]. This nictitating membrane plays a critical role in protecting the eye, particularly during feeding events [22]. Its movement is closely coordinated with jaw opening and relies on proper function of the levator palpebrae nictitans muscle, which is innervated by the oculomotor nerve (cranial nerve III). Traumatic injuries, such as those caused by internal hooks, can damage this nerve, leading to dysfunction of the third eyelid mechanism and for example, lead to prolonged corneal exposure [24]. This may directly affect the shark’s ability to detect and capture prey. In fact, experimental studies have shown that vision loss in sharks can lead to significant behavioral changes and reduced foraging efficiency [25]. As vision plays a critical role in prey detection, any damage to the visual system may have substantial ecological and fitness consequences [26,27]. Although we also observed other ocular lesions, such as permanent exophthalmos and corneal discoloration, their impact on visual functionality remains even less understood. More research is needed to understand the structure and function of the third eyelid and vision in sharks, and the role of these in their ecological and behavioral patterns.

We described two cases of skin lesions in the sharks’ cheeck associated with retained fishing hooks, characterized by granulation tissue, fibrosis and necrosis. In both individuals, either the hooks themselves or residual perforations suggestive of previous hook presence were surrounded by extensive fibronecrotic tissue. Open wounds located near the mouth or other anatomically mobile regions may impair normal function and hinder tissue regeneration due to persistent mechanical stress. This, in turn, can facilitate secondary infections and perpetuate chronic inflammation [9]. What initially presents as a localized infection may subsequently progress to a systemic condition, ultimately compromising the animal’s health and survival [27].

Fishing hooks can also cause significant harm, even when there is no direct visual evidence of their presence. For instance, the emergence of nylon fishing lines from the oral cavity is indicative of hook ingestion, with the hook likely lodged in internal tissues or anatomical structures, potentially resulting in severe internal injuries [7,9]. In our study, we identified two sharks exhibiting external nylon lines protruding from the mouth. One of these individuals also showed signs compatible with neurological impairment, including loss of buoyancy control and erratic swimming behavior. Given the high prevalence of visible hook-associated injuries observed in our sharks, it is likely that the actual incidence is underestimated. This may be due to the presence of hooks without external indicators (e.g., detached from visible lines) that remain undetected, as well as the fact that severe internal injuries may compromise survival, leading to mortality before the affected individuals can be observed or recorded [28]. However, these factors have barely been explored in shark species.

Our findings suggest that the impact of RH on blue sharks and potentially other shark species in the Mediterranean may be greater than previously assumed [13], underscoring the urgency of implementing affective bycatch mitigation strategies. These impacts remain poorly documented and are therefore likely underestimated. A variety of bycatch mitigation strategies have been proposed, including modifications to bait type and gear configuration (e.g., use of nylon leaders, large circle hooks, deeper longline settings), as well as improved handling and release practices such as in-water release and reduced manipulation times [29,30]. While some of these methods have shown promising results in reducing shark bycatch and improving post-release survival, their effectiveness varies by species and fishery [31]. Further investigation, including capture–mark–recapture and telemetry studies, is needed to assess the long-term impacts and true efficacy of these strategies. An additional complementary approach involves the establishment of spatial management measures, such as marine protected areas or temporal fishing closures in known shark aggregation or reproductive zones, such as the CCC for blue sharks in the NW Mediterranean Sea [13]. Evidence suggests that despite the wide-ranging movements of many shark species, spatial protection can be effective for certain species such as the grey nurse shark (Carcharias taurus) [28]. Nonetheless, a deeper understanding of the practical and socio-economic barriers that limit the adoption of these technically validated mitigation strategies is required. Therefore, research (both scientific and economic) is crucial to evaluate the cost–benefit trade-offs of adopting alternative fishing gears and practices. This must include assessing potential changes in target and non-target species captures, initial and ongoing costs of this alternative fishing gear, fisherman extra work requirements, and operational safety concerns associated with gear modifications and shark handling protocols.

Conclusion

Although sharks may initially survive capture and release events during fisheries, the long-term consequences of these interactions remain a significant concern for the conservation and management of these species. Consequences of bycatch may lead to shark starvation, impaired growth, and decreased fitness, ultimately affecting individual survival and reproductive success. In species already under severe demographic pressure, such as P. glauca, classified as Critically Endangered in the Mediterranean by the IUCN [3], these sublethal but debilitating injuries represent a serious conservation concern. However, gaps remain in understanding post-release survival and the long-term impact of retained fishing gear on sharks. Addressing these issues will require targeted capture-mark-recapture and tagging studies, alongside the development and testing of bycatch mitigation strategies.

Acknowledgement

We appreciate the help and collaboration of Elisenda Giró Para, Mireia Riera Giró, Francisco Fernández Rivera, Francesc Carbonell, Elisabeth Salvador, Marc Ruiz-Sagalés, Ana Maria Abril Duro, and all participants of the Cap de Creus Experience programme.

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