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Transcoelomic expulsion of an ingested foreign object by a carcharhinid shark

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A wild lemon shark (Negaprion brevirostris) was observed to expel an ingested foreign object through its body wall, over a minimum period of 435 days. We observed this lemon shark at a recreational diving feeding site off the coast of Juno Beach (FL, USA) on 12 occasions between 6 December 2014 and 14 December 2016. At the final observation, following expulsion, we observed this lemon shark with scar tissue and in apparent healthy condition. At minimum, this lemon shark was able to survive for over 1 year under perforation of its stomach lining, coelom and body wall. This account provides further evidence for the resilience and recovery capabilities of elasmobranch fish.
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Transcoelomic expulsion of an ingested foreign object by a
carcharhinid shark
S. T. Kessel
A
,
H
,J. Fraser
B
,W. G. Van Bonn
C
,J. L. Brooks
D
,T. L. Guttridge
E
,
N. E. Hussey
F
and S. H. Gruber
G
A
Daniel P. Haerther Center for Conservation and Research, John G. Shedd Aquarium,
1200 South Lake Shore Drive, Chicago, IL 60605, USA.
B
Ocean Artworks LLC, Boynton Beach, FL 33435, USA.
C
A. Watson Armour III Center for Animal Health and Welfare, John G. Shedd Aquarium,
1200 S Lake Shore Drive, Chicago, IL, 60605, USA.
D
Fish Ecology and Conservation Physiology Laboratory, Department of Biology,
Carleton University, Ottawa, ON, K1S 5B6, Canada.
E
Bimini Biological Field Station Foundation, South Bimini, Bahamas.
F
Biological Sciences, University of Windsor, 401 Sunset Avenue, Windsor, ON,
N9B 3P4, Canada.
G
Rosenstiel School of Marine and Atmospheric Sciences, University of Miami, Miami,
FL 33149, USA.
H
Corresponding author. Email: skessel80@gmail.com
Abstract. A wild lemon shark (Negaprion brevirostris) was observed to expel an ingested foreign object through its
body wall, over a minimum period of 435 days. We observed this lemon shark at a recreational diving feeding site off the
coast of Juno Beach (FL, USA) on 12 occasions between 6 December 2014 and 14 December 2016. At the final
observation, following expulsion, we observed this lemon shark with scar tissue and in apparent healthy condition. At
minimum, this lemon shark was able to survive for over 1 year under perforation of its stomach lining, coelom and body
wall. This account provides further evidence for the resilience and recovery capabilities of elasmobranch fish.
Additional keywords: deep hook, diver observation, gut hook, lemon shark, stomach eversion, spiral valve eversion.
Received 27 January 2017, accepted 2 May 2017, published online 13 July 2017
Introduction
Ingestion of foreign objects by sharks has long been established in
both the literature and popular culture. This has largely been the
result of a long-standing human fascination with cutting open
shark stomachs to reveal strange contents, such as bibles, unex-
ploded bombs and ticking watches (Gapps 2011). As far back as
1949, oil cans, tin cans, rope and a large piece of tile were docu-
mented in the stomach contents of tiger sharks (Galeocerdo
cuvier) in the Florida Keys (Gudger 1949). Questions surroundthe
motivation and cause of ingestion events, but arguably the more
important issue is the implication of foreign objects in the sto-
machs of sharks relative to their health and post-ingestion survival.
Many shark species are capable of expelling objects through
the voluntary induction of stomach eversions, a known mecha-
nism to facilitate expulsion of indigestible matter from their
stomachs (Brunnschweiler et al. 2005). Famously, in 1935, a
tiger shark housed in the Coogee Aquarium Baths (Sydney,
NSW, Australia) ejected a human arm in this manner in front of
unsuspecting patrons (Castles 1995). Multiple elasmobranch
species in captivity and in the wild have been documented to
eject some small objects by the eversion and protrusion of their
spiral valve through their cloaca to rinse it of debris (Christie
2012;Wiersma et al. 2016). However, if the ingested object is
too big, or the shark is unable to disgorge it through these
mechanisms, what is the expected fate for that individual?
A necropsy of a washed up whale shark (Rhincodon typus)in
Thailand indicated the cause of death to be internal injuries as a
result of the ingestion of a rigid plastic straw (Haetrakul et al.
2009). A juvenile sand tiger shark (Carcharias taurus) held in
captivity at the Singapore Zoo ingested part of the exhibit
rockwork. After failing to expel the object after 3 weeks, it
was deemed necessary to surgically remove the item (Lloyd and
Lloyd 2011). Under such circumstances, where sharks are
unable to expel ingested foreign objects either through the
digestive system or by stomach eversion, are there other meth-
ods that the animal may adopt to rid themselves of the item?
Herein, we document observations of a wild adult lemon
shark (Negaprion brevirostris) that was able to expel an ingested
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Marine and Freshwater Research
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Short Communication
foreign object through its coelom and body wall over a mini-
mum period of 435 days. Over this period, the foreign object was
progressively expelled through the coelom and body wall until it
was completely ejected, and the body wall healed to the point
that the only lasting external evidence was scar tissue. To the
best of our knowledge, this is the first documented account of
transcoelomic expulsion of a foreign object by an elasmobranch.
Materials and methods
A mature male lemon shark (,250-cm estimated total length)
was observed on 12 occasions between 6 December 2014 and 14
December 2016 at a recreational diving shark feeding site
known as the ‘Lemon Drop’, located off the coast of Juno Beach,
Florida (208530N, 798590W). Occurrence at the feeding site was
exclusively during the winter months of December–February
each year, consistent with the seasonal presence of lemon sharks
in this region (Kessel et al. 2014).
Ethical considerations
All applicable international, national, and institutional guide-
lines for the care and use of animals were followed. The present
study was purely observational and, as such, no physical contact
with the animal was made.
Results
Observations from 6 to 27 December 2014
Between 6 and 27 December 2014, the lemon shark was sighted
five times at the feeding site with a foreign object protruding out
from its right side, ,10–15 cm anterior to the right pectoral fin
(Table 1,Fig. 1a,b, and Video S1, available as Supplementary
material to this paper). At this time it was not clear what the
object was, only that it was of metallic composition. On 27
December 2014, a slight bulge was noticed on the ventral left
side of the shark.
Observation on 2 January 2016
The affected lemon shark returned to the feeding ground and we
observed the metallic object protruding further out of its right
side (Video S1). At this time, we identified the object as a
stainless steel ‘fish stringer’, a piece of equipment spear fish-
ermen use to retain captured fish while continuing to hunt
(a)(b)
Fig. 1. Initial observations showing a metallic foreign object protruding from the right side of the lemon shark: (a) profile view of right side on
6 December 2014; (b) ventral view on 21 December 2014 shows no protrusion from the underside at this time. Inset, close-up image of the protrusion.
(Photographs taken by Joanne Fraser.)
Table 1. Dates on which the individual was observed and the status of foreign object across the entire period
Visual references refer to the images and video footage (available as Supplementary material) associated with each observation. N/A, not available
Date Status of object Visual reference
6 December 2014 Protruding from right side only Fig. 1a
13 December 2014 Protruding from right side only N/A
21 December 2014 Protruding from right side only Fig. 1b
22 December 2014 Protruding from right side only N/A
27 December 2014 Protruding from right side only, ventral left side bulge first noticed Video S1
10 January 2015 Protruding from right side only Video S1
25 January 2015 Protruding from right side only Video S1
2 January 2016 Protruding from both right and ventral side Video S1
6 February 2016 Protruding from both right and ventral side Fig. 2a,b
13 February 2016 Protruding from right and ventral side, ventral left side bulge prominent Fig. 2c,d
14 February 2016 Protruding from right and ventral side, ventral left side bulge prominent N/A
14 December 2016 Absent and wounds healed with visible scar tissue Fig. 3a,b, Video S1
BMarine and Freshwater Research S. T. Kessel et al.
(Fig. 2). By this point, the free end of the open stringer (see
Fig. 2b) had also breached the body wall and was protruding
from the ventral surface of the shark.
Observations from 6 to 14 February 2016
Between 6 and 14 February 2016, the affected lemon shark was
sighted three times at the feeding site (Table 1). The fish stringer
was protruding further from both the right and ventral sides. The
individual appeared progressively more emaciated over the
course of our observations to this point. The bulge on the ventral
left side of the shark become much more prominent, probably
caused by an item blocked by the stringer pushing against the
coelom wall (Fig. 3c,d). At this time, we saw that the complex
structure of the stringer was completely protruding from the
right side of the shark (Fig. 3b), leaving only the curved, but
otherwise smooth, shaft of the stringer inside the body cavity
(Fig. 2b).
Observation on 14 December 2016
On 14 December 2016, the shark returned to the feeding site with
the stringer fully ejected from its body cavity (Fig. 4a,b,and
Video S1). We identified the individual by the scar tissue that was
evident at both past protrusion sites, in addition to its size, sex and
specific pectoral fin notching. The wounds were both closed and
covered by scar tissue. At this time, based on our estimates of
girth, the individual looked robust and in improved condition.
~40 cm
Structure Free
end
(a)(b)
Fig. 2. Schematic of (a) a closed stringer and (b) an open stringer seen
protruding from a lemon shark (Negaprion brevirostris) at a dive site off
Juno Beach (FL, USA). Ellipses highlight the section of the structure that
was protruding from the right side of the shark, and the free end that was
protruding from the ventral surface.
(a)(b)
(c)(d)
Fig. 3. Subsequent observations on (a,b) 6 and (c,d) 13 February 2016 showing the secondary protrusion on the ventral side of the lemon shark.
(a,b) Orientation of the foreign object from the right (a) and from the ventral side (b); inset, the structure of the section protruding from the right side.
(c,d) The ventral bulge that became more prominent on the left hand side of the shark, near the ventral protrusion, (c) from the right side and (d) from
the left side. (Photographs taken by Joanne Fraser.)
Lemon shark transcoelomic expulsion Marine and Freshwater Research C
Discussion
We can only speculate on the events that resulted in the ingestion
of the fish stringer by the lemon shark. The most probable
scenario is that fish were being retained on the stringer and the
lemon shark consumed them, resulting in the inadvertent
ingestion of the stringer as well. We believe ingestion to be the
only reasonable pathway into the body cavity. Fish stringers are
merely a tool for the retention of captured fish, and are not a
projectile used in spear fishing. We do not believe it is feasible
that a diver would have been able to force such a large rigid
object through the body wall of a free-swimming shark by hand.
Such an unlikely scenario would have resulted in considerable
external marking, which was not present on this individual.
We can equally only speculate on the specific event that led to
the final removal of the object. Given the shape and structure of
the stringer, it most probably exited through the opening on the
right side of the shark. It is difficult to ascertain how the object
was finally expelled, but we postulate that the stringer was either
snagged on a bottom structure or removed by a diver. Whatever
the circumstances that led to the ingestion and expulsion of the
stringer, this individual was able to expel the large foreign object
over a minimum period of 435 days. This demonstrates a high
level resilience and recovery after major internal trauma.
Importantly, this lemon shark was able to survive for over 1 year
under perforation of its stomach lining, coelom and muscle wall.
Carcharhinid sharks are well documented to survive and
exhibit considerable tissue regeneration following extensive
external trauma (Bird 1978); however, we observed that they
are also resilient to considerable internal damage. Our observa-
tions have implications in relation to other internal injuries
experienced by sharks, suchas gut (or deep) hooking. Commonly,
estimates of fisheries-related mortality for sharks include
gut hooking as a factor in post-release survival estimates
(e.g. Campana et al. 2006). Our account suggests that sharks
may be particularly resilient to such internal injuries, including
perforation of the stomach wall. This may be expected because
the prey items of many shark species include porcupine fish,
spiny crustaceans and stingrays (Gudger 1949;Strong et al.
1990;Chapman and Gruber 2002). All such prey items have the
potential to cause internal damage after consumption. We
suggest that the ability to sustain and recover from such internal
trauma would confer a strong fitness factor, and would be
evolutionarily beneficial for sharks to survive and reproduce
in the face of such injury. Equally, our observations lend
credence to the practice of cutting leaders on gut-hooked sharks
rather than trying to remove the hook, as demonstrated for other
fish species to result in higher survival rates (Fobert et al. 2009;
Weltersbach et al. 2016). The present observations suggest that
lemon sharks, and most probably other shark species, are able to
expel large objects such that their ingestion is not necessarily
fatal.
Conflicts of interest
The authors declare that they have no conflicts of interest.
Supplementary material
The supplementary material for this paper is in the form of a
video file (see https://youtu.be/z6ZybPWn0sc).
Acknowledgements
The authors acknowledge Captain Luis A. Roman of Calypso Dive Charters
(Lake Park, FL, USA) for providing continued vessel support throughout
these observations. The authors also acknowledge the editor and two
anonymous reviewers for their constructive comments on the earlier draft of
this manuscript, which improved the current version.
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Lemon shark transcoelomic expulsion Marine and Freshwater Research E
... Las áreas de cría de N. brevirostris han sido estudiadas extensivamente en las Islas de Bimini, Bahamas, durante las últimas tres décadas (Gruber, 1982a;Gruber et al., 1988, Morrissey & Gruber, 1993a, 1993bGruber et al., 2001, Feldheim et al., 2002aEdrén et al., 2005;Jennings et al., 2008;Newman et al., 2010Newman et al., , 2012Finger et al., 2016;Keller et al., 2017;Hussey et al., 2017;Stump et al., 2017). La teoría ecológica sobre la utilización de las áreas de cría de tiburones indica que ciertas estrategias del uso de hábitat pueden incidir positivamente en la sobrevivencia y desarrollo de los individuos juveniles. ...
... Sin embargo, los mismos autores también encontraron que para los juveniles (0-3 años) que habitan dentro del área de cría, la selección natural favorece a los individuos de tamaños pequeños y tasas de crecimiento bajas. Este aspecto al parecer se relaciona con una diferencia en las zonas de alimentación en dicha área de estudio, donde los juveniles pequeños prefieren alimentarse en las áreas circundantes a los manglares y los juveniles de mayor tamaño tienen una preferencia por las zonas de fanerógamas marinas donde quedan más expuestos a ser depredados (Hussey et al., 2017). Estas diferencias en el comportamiento pueden tener su origen en la personalidad de los individuos, adquirida a su vez por la experiencia de acuerdo a la edad (Hussey et al., 2017). ...
... Este aspecto al parecer se relaciona con una diferencia en las zonas de alimentación en dicha área de estudio, donde los juveniles pequeños prefieren alimentarse en las áreas circundantes a los manglares y los juveniles de mayor tamaño tienen una preferencia por las zonas de fanerógamas marinas donde quedan más expuestos a ser depredados (Hussey et al., 2017). Estas diferencias en el comportamiento pueden tener su origen en la personalidad de los individuos, adquirida a su vez por la experiencia de acuerdo a la edad (Hussey et al., 2017). En todo caso, este tipo de comportamiento, que puede tener también su origen en cuestiones genéticas, puede variar según el tipo de hábitat y las zonas geográficas. ...
Thesis
Full-text available
A pesar de los esfuerzos que se han hecho en materia de conservación de los tiburones durante los últimos años, las poblaciones de este grupo de peces continúan estando amenazadas. Actualmente, los tiburones están considerados como uno de los grupos de vertebrados marinos más amenazados a nivel global. Una de las estrategias de conservación que ha incrementado su relevancia en los últimos años es la identificación y protección de las áreas de cría de tiburones. La importancia de las áreas de cría radica en que éstas están directamente relacionadas con el proceso de reclutamiento y mantenimiento de las poblaciones. En este sentido, la caracterización de éstos hábitats esenciales constituye un aspecto elemental para el diseño de los planes de manejo. El tiburón limón, Negaprion brevirostris, es una especie relativamente común en el Mar Caribe; sin embargo, en Venezuela esta especie no ha sido estudiada por lo que existe un vacío de información sobre su distribución, abundancia y estructura poblacional. La particular presencia de N. brevirostris en el Archipiélago Los Roques ofrece una oportunidad para investigar varios aspectos biológicos y ecológicos de la población juvenil de esta especie. Además, existe la sospecha que ciertas características bióticas y abióticas de las islas oceánicas tropicales ofrecen condiciones óptimas para el desarrollo de los tiburones juveniles, y por ende podrían contribuir a maximizar la eficiencia bilógica de los individuos. El presente trabajo estuvo enfocado en evaluar varios aspectos del tiburón limón en el Archipiélago Los Roques: la distribución espacial, área de cría y estructura de tallas; el crecimiento, edad y sobrevivencia; el patrón de actividad espacial y su relación con la distribución de las presas potenciales. Para ello se utilizó una combinación de métodos como por ejemplo, el seguimiento de la pesca comercial de tiburones en el Archipiélago Los Roques, la aplicación del método de marcaje y recaptura, el registro de avistamientos de juveniles durante los períodos de navegación y la utilización de la telemetría acústica. Entre los resultados más importantes se encontró que las lagunas de Sebastopol y de Los Bobos constituyen áreas de cría mono-específicas de la especie N. brevirostris, y además existe una partición de las zonas habitadas por los juveniles, descritas como áreas de cría primarias y secundarias. Esta estrategia de uso podría ser ventajosa, toda vez que contribuiría a reducir la competencia y depredación intra-específica. Por otra parte, el análisis del crecimiento indicó que los juveniles exhiben tasas de crecimiento elevadas, las cuales son comparables con las poblaciones de otras islas oceánicas tropicales. Sin embargo, se encontró que el crecimiento de los juveniles incrementa con la talla/edad, siendo contrario a lo que biológicamente se esperaría. Los juveniles pequeños aparentemente están sujetos a una mayor presión de depredación por parte de sus congéneres más grandes, y ello puede afectar negativamente la alimentación y el desarrollo. Por otra parte, los valores de las probabilidades de sobrevivencia obtenidas para los juveniles fueron bajos. A su vez, el análisis indicó que no existe diferencia entre las probabilidades de sobrevivencia entre grupos de edad, y por lo tanto el crecimiento y la sobrevivencia no se encuentran inversamente relacionados. Los niveles de sobrevivencia exhibidos por los juveniles más pequeños podrían tener un costo energético que se traduce en tasas de crecimiento bajas, con relación a los ejemplares de mayor tamaño. Así pues, los juveniles pequeños podrían estar invirtiendo más tiempo y energía en movilizarse y refugiarse constantemente para evitar ser depredados por sus congéneres de mayor edad, lo cual a su vez también conllevaría a una inadecuada ingesta de alimentos por parte de los tiburones. Con relación a los resultados de la actividad espacial de los juveniles del tiburón limón, el análisis arrojó que el movimiento de los individuos se encuentra restringido a la Laguna de Sebastopol, exhibiendo así un elevado nivel de fidelidad espacial. También se encontró que la relación entre la edad de los juveniles y el tamaño de las áreas de actividad (MPC y Kernel) están positivamente correlacionadas; es decir, los individuos incrementan progresivamente su área de actividad a medida que se desarrollan dentro del área de cría. Como en el caso de otros estudios, este comportamiento podría estar influenciado por varios factores, como por ejemplo la demanda de alimento y la protección contra los depredadores. A medida que los individuos incrementan sus áreas de actividad, es natural que éstos extiendan también sus hábitats, observándose cambios en variables como la profundidad y el tipo de fondo. El análisis para evaluar el solapamiento entre las áreas de abundancia de las presas potenciales y las áreas de actividad espacial de los individuos, arrojó que los resultados no fueron concluyentes. El conjunto de estrategias descritas con relación a la utilización del hábitat, así como de ciertas características bióticas y abióticas presentes en el Archipiélago Los Roques, tendría implicaciones positivas para el mantenimiento de las poblaciones, toda vez que favorecen el crecimiento, el desarrollo y la sobrevivencia de los tiburones durante las etapas tempranas de vida. Los resultados de éste estudio constituyen un nuevo aporte de información para la región; sin embrago, los trabajos dirigidos a estas especies y sus hábitats esenciales como las áreas de cría, deberían continuar en el tiempo con el propósito de detectar cambios en la dinámica de las poblaciones, y de este modo proponer las respectivas medidas de manejo y conservación.
... Healing of integumental wounds in fish can be influenced by numerous physiological, pathological, and environmental factors. These include stress, which in captive sharks has been linked to epidermal necrosis (Garner 2013), infection including opportunistic integumental or environmental bacteria and external parasites (Cheung et al. 1982;Bertone et al. 1996;Garner 2013), persistent foreign material (Heupel and Bennett 1997;Kessel et al. 2017), and environmental temperature (Bansemer and Bennett 2010). Because of the multitude of factors that can influence healing, more studies are needed to fully understand the tissue reactions to integumental injuries in sharks under different environmental and physiological conditions. ...
... The foreign material present in the large wound could complicate and thus delay healing, although it was most likely a spurious finding that resulted from a short-term contact with the invasive drifting algae found on the shark during the capture event. Former studies on responses to foreign bodies in sharks vary from minimal (Heupel and Benett 1997;Kessel et al. 2017) to severe (Borucinska et al. 2001(Borucinska et al. , 2002a, indicating that their presence can change healing characteristics. ...
Article
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Despite reports that sharks have an exceptional capacity to heal from traumatic injuries, no detailed microscopic observations of integumental wounds have been reported for sharks. This study details the histopathological features of such wounds in a free-ranging shark. An adult male blacktip shark Carcharhinus limbatus was collected in 2017 during fisheries-independent sampling efforts in the coastal southeastern U.S. Atlantic. The shark had numerous lesions on his head, torso, and left pectoral fin that were compatible with shark bites. Representative samples from two wounds on the head were examined by light microscopy. The epidermal changes included hyperplasia and hypertrophy, intracellular edema, and absence of goblet cells, denticles, and chromatophores. In the dermis, fibrinocellular exudation, granulation tissue, and marked skeletal muscle necrosis and regeneration were observed. The above features were comparable with wound healing in bony fish, albeit minor differences were found. Although this case documents exceptionally good regeneration of skeletal muscle in the shark, we found no evidence of unique morphological healing patterns. Further studies on wound healing are needed because recent molecular and genetic findings do suggest evolutionary adaptations enhancing healing in sharks.
... Shark pectoral fins are moveable about the insertion, with musculature that allows them to be elevated, depressed and rotated relative to the body, and are critical for both vertical (rising and sinking) and horizontal (turning) manoeuvrability (Hoffmann et al., 2019;Maia et al., 2012;Wilga & Lauder, 2000), therefore the constant elevation of the pectoral fins caused by the apparatus would likely have affected swimming performance. Sharks have a high capacity for wound healing and recovery following injury (Bird, 1978;Chin et al., 2015;Kessel et al., 2017;Riley et al., 2009). Survivorship after entanglement was confirmed in a shortfin mako shark that had similarly deep wounds (Wegner & Cartamil, 2012) and since bull sharks are relatively resistant to capture stress (Dapp et al., 2016;Gallagher et al., 2014;Hyatt et al., 2012), it is likely that the shark survived and ultimately healed from its injuries. ...
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A 193cm total length female bull shark Carcharhinus leucas was captured in Florida bearing intentionally attached materials which resembled a harness. Harness‐type live bait rigs are commonly used for small baitfish; some anglers use such devices with small sharks when targeting large sharks and bony fish. Biofouling on the apparatus and the extent of the injuries indicated the material had likely been on the shark for several years. This case highlights the dangers of using these types of devices on juveniles of long‐lived species that attain a large body size.
... However, ingestion of plastic debris is not a major problem for most elasmobranch since they are able to expel objects through voluntary induction of stomach eversions, a mechanism that facilitates the expulsion of indigestible matter from their stomachs (Brunnschweiler et al., 2005). Recent studies have similarly reported that many elasmobranch species eject small objects by eversion and protrusion of their spiral valve through their cloaca to rinse it of debris (Christie, 2012;Wiersma et al., 2016;Kessel et al., 2017). However, when the ingested materials are big enough, or the shark is unable to disgorge the materials through the usual mechanisms, it may lead to internal injuries and death. ...
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... Depending on the nature of the injury, a fish should either be released immediately to minimise additional handling stress, or euthanised (Fobert et al., 2009). Some species, however, are demonstrably resilient to injuries (Chin et al., 2015;Kessel et al., 2017). Physical injuries (e.g., scale loss or cuts) can also arise from entanglement and abrasion, crushing injuries from net fishing gears and barotrauma following rapid ascent; severe injuries can quickly lead to critical failure of vital tissues (Cook et al., 2019). ...
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... Chondrichthyans (sharks, batoids, and chimaeras) have been identified as having a remarkable ability to heal and regenerate from grave injuries such as gill destruction or body wall penetration [1] [2] [3]. In the early 1990s, this ability extended to claims that sharks do not, or rarely, get cancer [4] [5]. ...
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The European eel (Anguilla anguilla) is a commercially and recreationally important fishery target species. In the last decades, the eel has experienced dramatic stock declines and has been listed as critically endangered. To reduce fishing mortality, several European countries have closed the fishery or introduced stricter management measures which increase the likelihood of catch-and-release in the recreational fishery. This study investigated hook shedding mechanisms of deep-hooked, line-cut eels via radiography, and quantified hook shedding rates, post-release mortality and sub-lethal effects in captivity. Eels were caught with four different hook treatments, monitored in a tank for 23 weeks, and radiographed 0, 1, 3, 10, 24, 54, 115 and 163 days after capture. After 163 days, total hook shedding rate was significantly higher for smaller hooks (41.2%) compared to larger hooks (0.0%), and increased with fish length. Post-release mortality rates ranged between 27.3% and 50.0% after 23 weeks (not adjusted for handling and holding) and did not differ significantly between hook treatments.The majority of dead eels showed gastric perforations caused by the hooks leading to internal haemorrhaging and the intrusion of digestive fluids into the body cavity inducing lethal degradation and inflammation of vital organs. Anglers are encouraged to minimise bycatch of eel in countries where eel harvest is prohibited. Anglers targeting eel should use selective and appropriate fishing gears, baits and tactics (e.g. very large hooks, immediate hook setting after a bite) to reduce deep hooking and the catch of undersized eels, ultimately promoting the eel's conservation.
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Intestinal rinsing via eversion through the cloaca has been documented in a number of sharks that possess a scroll or conicospiral type of valvular intestine (Bspiral valve^). This valve was first described by Marcus Aurelius Severinis in 1645 and is the lower part of a shark's intestine that is twisted to allow a greater surface area for digestion and increased nutrient absorption. To date, intestinal eversion and rinsing of the spiral colon has been documented in eight species of carcharhiniform sharks, including five of the genus Carcharhinus, two of the ge-nus Negaprion, and Triaenodon obesus (Howe et al. 1990). Eversion has also been documented in the sawfish Pristis pectinata (Henningsen et al. 2005). All of these observations occurred with individuals held in captivity in aquaria. Only one example of eversion has been documented in the field, which was also notable because it occurred in a ray, Manta birostris (Clark et al. 2008). Here, we report the first field observation of intestinal eversion by a shark, the broadnose sevengill shark. In March 2013, a female broadnose sevengill shark (2.5 m in length) was photographed in shallow water (10 m depth) in a sheltered cove (S34°14.21′ E018°28.60′) at False Bay, South Africa. While swimming towards the photographer, the shark assumed a Bhunched^ posture and everted its intestine (Fig. 1). This eversion and re-traction was rapid, lasting only a few seconds. Why eversion occurred in this instance is not known, although observations of captive sharks support the hypothesis that at least one function of eversion is to free mucous and indigestible particles from the spiral colon. The broadnose sevengill shark was one of a group of several sharks of the same species that occur predictably in the cove during daylight hours. No feeding by these animals was observed in more than 20 dives at the site. Our observations show that the phenomenon of intestinal eversion in sharks is not simply a consequence of captivity and has relevance to the natural behaviours of these animals in the wild. It likely serves the same function as gastric eversion in clearing the intestinal tract of indigestible objects. Fig. 1 Intestinal rinsing in a broadnose sevengil shark
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Understanding how and why animals are distributed through time and space has always been a fundamental component of ecology and is an essential prerequisite for effective conservation and/or management. However, for highly mobile K-selected species, behavioural predictability is rarely considered over appropriate scales relative to life history. To address this point, a multidisciplinary approach combining telemetry, external tagging, physical assessment, environmental monitoring and genetic analysis was adopted to determine a spatial framework for the movements of adult lemon sharks Negaprion brevirostris at multiple spatial and temporal scales from 2007 to 2011. Lemon sharks (n = 83) were tracked with passive acoustic telemetry, revealing a winter residency in the southeast Florida region. Detections from individuals recorded within the core winter habitat for >20 d (n = 56) were incorporated into generalized linear mixed-effects models to investigate the influence of water temperature, photoperiod, moon phase, month and year on presence. The findings of this study suggest a temperature driven ‘migration-residency’ model for mature lemon shark distribution across the USA eastern seaboard. Lemon sharks are distributed across a wide geographical area in the summer months and migrate south concentrating off southeast Florida in the winter, with this pattern repeated each year. From comparative genetic analysis and the absence of any evidence of mating behaviour during the winter residency period, mating and parturition most probably occur in May/June between northern Florida and the Carolinas. This study highlights the importance of determining the specific dynamics and proximate causes of animal movement and distribution over appropriate spatial and temporal scales relative to life history.
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Video observation of oral gastric eversion in a free-living Caribbean reef shark (Carcharhinusperezi) shows voluntary gastric eversion followed by retraction not only occurs, but is extremely rapid (lasting [similar]0.3 s). Eversion may occur by stomach relaxationcleansing’ function for removing indigestible food particles, parasites or mucus from the stomach lining. Sharks, and possibly other animals with similar gut morphologies, may use this technique to help maintain a healthy alimentary tract.
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a b s t r a c t Research on a wide range of fish species has revealed that deep hooking is perhaps the single most important determinant of injury and post-release mortality in recreational fisheries. However, there is little information on the best option for dealing with deeply hooked fish that are to be released; should the line be cut or should the hook be removed? Using bluegill sunfish (Lepomis macrochirus) as a model we investigated sublethal (e.g., swimming performance, physiological condition, injury levels) and lethal consequences associated with removal of deeply ingested hooks versus cutting the line and leaving the hook embedded in the esophagus, relative to shallowly hooked controls. Neither hook retention nor deep hook-removal altered the swimming performance of the fish in this study relative to controls. However, there was evidence of short-term physiological disturbance. For example, hematocrit was reduced for fish that had hooks removed, consistent with visual observations of bleeding. In addition, blood glucose levels tended to be higher and plasma Na + levels tended to be lower in deeply hooked fish that had hooks removed indicating stress and ionic imbalance even 24 h after capture. During holding experiments we noted the highest mortality levels in fish for which the hook was removed (33% after 48 h and 44% after 10 days). Mortality rates were lowest for the controls (0% after 48 h and 4% after 10 days) and intermediate for the line-cut treatment (8% after 48 h and 12.5% after 10 days). After 48 h, 45.5% of the fish from the line-cut treatment group were able to expel the hook originally embedded in their esophagus, and at the end of the 10 day study, 71.4% had expelled the hook. Even with the hook left in the esophagus, fish were able to feed although at lower rates than controls during the first 48 h of holding. By 10 days post-capture, there were no differences in feeding rates as evidenced by growth patterns among the treatment groups, nor were there differences in the hepatosomatic index. Collectively, the findings from this study demonstrate that cutting the line is a more effective release method than removing the hook when fish are deeply hooked. As such, angler education efforts should focus on disseminating this message to anglers as well as encouraging the use of gear and techniques that minimize incidences of deep hooking (e.g., circle hooks, non-organic bait).