Transcoelomic expulsion of an ingested foreign object by a
S. T. Kessel
,W. G. Van Bonn
,J. L. Brooks
,T. L. Guttridge
N. E. Hussey
and S. H. Gruber
Daniel P. Haerther Center for Conservation and Research, John G. Shedd Aquarium,
1200 South Lake Shore Drive, Chicago, IL 60605, USA.
Ocean Artworks LLC, Boynton Beach, FL 33435, USA.
A. Watson Armour III Center for Animal Health and Welfare, John G. Shedd Aquarium,
1200 S Lake Shore Drive, Chicago, IL, 60605, USA.
Fish Ecology and Conservation Physiology Laboratory, Department of Biology,
Carleton University, Ottawa, ON, K1S 5B6, Canada.
Bimini Biological Field Station Foundation, South Bimini, Bahamas.
Biological Sciences, University of Windsor, 401 Sunset Avenue, Windsor, ON,
N9B 3P4, Canada.
Rosenstiel School of Marine and Atmospheric Sciences, University of Miami, Miami,
FL 33149, USA.
Corresponding author. Email: firstname.lastname@example.org
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
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
Marine and Freshwater Research
Journal compilation CSIRO 2017 www.publish.csiro.au/journals/mfr
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).
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.
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
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
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.
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.
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
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
Conflicts of interest
The authors declare that they have no conflicts of interest.
The supplementary material for this paper is in the form of a
video file (see https://youtu.be/z6ZybPWn0sc).
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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Fig. 4. Final observations on 14 December 2016 showing the foreign body to be completely expelled from the lemon shark and the protrusion
wounds healed. (a) Profile view of the right hand side; (b) ventral view. Insets show close-up images of the scar tissue. (Photographs taken by Joanne
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