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Aggressive interactions between juvenile swordfishes and blue sharks in the Western Mediterranean: a widespread phenomenon?

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There are numerous reports of billfishes spearing objects, marine organisms, and even humans. Whether or not this behaviour is intentional and, if so, what is its functional meaning, are open questions. In 2016, an adult blue shark (Prionace glauca) was found to be killed by a juvenile swordfish (Xiphias gladius) in the western Mediterranean. Here we report on three more recent cases involving both species in the same area. In February 2017, an adult male blue shark was found stranded in Garrucha (Spain) with a fragment of a juvenile swordfish’s rostrum (18cm long x 2cm wide at proximal end) inserted in its cranium. In March 2017, an adult pregnant female blue shark was stranded alive on the coast of Ostia (Italy) but died shortly afterwards; a fragment of a juvenile swordfish’s rostrum (25x3cm) was found allocated between the eye and the cranium. Finally, in February 2018, an adult female blue shark appeared stranded in the coast of Vera (Spain), with a putative impalement injury anterior to the right eye but without an associated bill fragment. Surprisingly, X-ray and computed tomography revealed an older injury in the right nostril, with a small piece of a juvenile swordfish’s rostrum (5.3x1.2cm). These cases suggest that juvenile swordfish would drive their rostrum into blue sharks as a defensive strategy that is likely to be far from anecdotal. We suggest that no regular cases of these interactions are reported because they occur at high sea and evidence of them, when available, can easily be overlooked.
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314 Medit. Mar. Sci., 20/2, 2019, 314-319
Mediterranean Marine Science
Indexed in WoS (Web of Science, ISI Thomson) and SCOPUS
The journal is available on line at http://www.medit-mar-sc.net
DOI: http://dx.doi.org/10.12681/mms.18102
Research Article
Aggressive interactions between juvenile swordsh and blue sharks in the western Mediter-
ranean: a widespread phenomenon?
Jaime PENADÉS-SUAY1,2, Pablo GARCÍA-SALINAS2,3, Jesús TOMÁS1 and Francisco Javier AZNAR1
1 Marine Zoology Unit, Cavanilles Institute of Biodiversity and Evolutionary Biology, Universitat de València, València, Spain
2Associació LAMNA per a l’estudi dels elasmobranquis a la Comunitat Valenciana
3 Fundación Oceanogràfic
Corresponding author: jaime.penades@uv.es
Handling Editor: Fabrizio SERENA
Received: 23 June 2018; Accepted: 4 April 2019; Published on line: 4 June 2019
Abstract
There are numerous reports of billfishes spearing objects, marine organisms, and even humans. Whether or not this behaviour
is intentional and, if so, what is its functional meaning, are open questions. In 2016, an adult blue shark (Prionace glauca) was
found to be killed by a juvenile swordfish (Xiphias gladius) in the western Mediterranean. Here we report on four more recent
cases involving both species in the same area. In February 2017, an adult male blue shark was found stranded in Garrucha (Spain)
with a fragment of a juvenile swordfish’s rostrum (18cm long x 2cm wide at proximal end) inserted in its cranium. In March 2017,
an adult pregnant female blue shark was stranded alive on the coast of Ostia (Italy) but died shortly afterwards; a fragment of a
juvenile swordfish’s rostrum (25x3cm) was found allocated between the eye and the cranium. In February 2018, an adult female
blue shark appeared stranded in the coast of Vera (Spain), with a putative impalement injury anterior to the right eye but without
an associated bill fragment. Surprisingly, X-ray and computed tomography revealed an older injury in the right nostril, with a
small piece of a juvenile swordfish’s rostrum (5.3x1.2cm). Finally, in August 2018, an adult male blue shark appeared stranded
alive in the coast of Manacor (Spain) with a fragment of swordfish bill (6.8x1.5cm) embedded in the snout. These cases suggest
that juvenile swordfish would drive their rostrum into blue sharks as a defensive or territorial strategy that is likely to be far from
anecdotal. We suggest that no regular cases of these interactions are reported because they occur at high sea and evidence of them,
when available, can easily be overlooked.
Keywords: Xiphias gladius; Prionace glauca; lethal interaction; impalement; stranding; western Mediterranean.
Introduction
Over the last decades, impalement of inanimate ob-
jects and marine organisms by swordfish (Xiphias glad-
ius L.) has been reported in a number of scientific pub-
lications and media news. There are reports of swordfish
driving its rostrum into inanimate objects, such as vessels
(Gudger 1940, Fierstine & Crimmen 1996), bales of rub-
ber (Smith 1956) and submarines (Zarudski & Haedrich
1974). There are also reports of impalement on animals,
such as large fishes (Starck 1960, Smith 1961), whales
(Jonsgard 1962), marine turtles (Frazier et al. 1994 and
references therein) and even people (e.g., Haddad & De
Figuereido, 2009; Georgiadou et al., 2010). Usually,
these interactions are detected by the presence of the dis-
tal segment of the bill embedded in the substratum, which
results from a transverse fracture of the bill due to the
stress of the impact.
The functional meaning of this spearing behaviour is
still under discussion. Carey & Robinson (1981) reported
evidence of intraspecific spearing events. In other bill-
fishes similar cases have been accounted for accidental
collisions. For instance, Fierstine et al. (1997) linked
the injuries in other billfish species to the hypothetical
collisions produced while feeding on the same bait ball.
Likewise, impalement of marine turtles would occur
when swordfish try to prey on the fishes that use shad-
ow beneath turtles as cover (Frazier et al. 1994). In other
cases, however, impalement has been interpreted as in-
tentional (Smith 1956, Ellis 2013, for a detailed historical
account). The clearest evidence of aggressive behaviour
comes from cases involving humans, particularly when
swordfish are provoked or disturbed (Georgiadou et al.
2010, and references therein; Romeo et al. 2017, and ref-
erences therein), which has sometimes resulted in fatal
spearing (Gooi et al. 2006). Descriptions of some of the
events indicate that swordfish usually try to pierce its ‘en-
emy’ with the bill (Romeo et al. 2017).
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Medit. Mar. Sci., 20/2, 2019, 314-319
Penadés-Suay et al. (2017) recently reported the case
of a blue shark (Prionace glauca L.) apparently killed by
a swordfish. An adult female blue shark stranded alive
but died shortly afterwards, and the necropsy revealed a
fragment of the tip of a young swordfish’s rostrum that
caused significant lesions in the brain. Penadés-Suay et
al. (2017) raised the question whether or not impalements
by swordfish are anecdotal, and to what extent swordfish
uses spearing as defence behaviour. The answer to both
questions deemed difficult because the literature contains
mostly case studies, or reviews of ‘fait-acommpli’ re-
cords scattered over long periods.
In the present paper we report evidence of four addi-
tional cases of impalement of blue sharks by swordfish
that occurred between February 2017 and August 2018
in the western Mediterranean. Based on the new evidenc-
es, we suggest that impalement of blue sharks could be
far from anecdotal and might represent an overlooked
behaviour within the defensive or territorial strategy of
juvenile swordfish.
Materials and Methods
The four shark specimens included in the present study
were found dead on the beach at the moment of stranding
or shortly afterwards. The sharks were measured in situ to
the nearest cm and visually examined for external lesions.
In two cases, a standard necropsy was carried out on the
stranding beach (Figs. 1, 2). A detailed description of the
injuries provoked by the swordfish rostrum was performed,
and the rostrum fragment was collected, photographed and
measured to the nearest mm. In the third case (Fig. 3), the
intact head of the shark was carried out to the laboratory
for X-ray and computed tomography (CT). Diagnostic im-
aging studies included the following:
(1) Plain radiographic evaluation with a Philips Prac-
tix 400 unit (Philips Medical Systems) and a Kodak Di-
rect View Classic CR System (Carestream Health) with
35 × 43 cm Kodak cassettes (Kodak PQ Storage Phosphor
Screen Regular and 100 Microns, Carestream Health) in
dorsal-ventral (DV) and lateral-lateral (LL) projections.
Focal distance was 1 m, using exposure values 75 kV
and 7.2 mAs based on animal size. Digital images were
processed afterwards with Kodak Acquisition Software
(Onyx-RAD Diagnostic Viewer) for better visualization
and image interpretation.
(2) A CT was done using a Somatom Volume Access
(Siemens). Acquisition parameters through head explora-
tion of the blue shark were 5 mm slice thickness and 5 mm
slice interval, with 0.5 mm retro-recon acquisition under
lung and mediastinal algorithms. Images were post-pro-
cessed with Osirix software version 3.3.1 (Pixmeo).
Rostrum fragments were identified as belonging to a
swordfish (X. gladius) based on the following combina-
tion of features (Fierstine & Voigt 1996, Penadés-Suay et
al. 2017): (1) flattened appearance in cross-section (i.e.,
depth less than half of width); (2) absence of denticles
on the surface, and (3) presence of central chambers in
cross-section. To estimate swordfish total body length
(TL), the ratio of maximum width to length of the frag-
ment (R) was calculated. Then, the rostrum of two sword-
fish specimens conserved at the Osteological Collection
of the Department of Zoology, University of Valencia,
were used to obtain the points in which the value of R
was equal to the value obtained in each case (Penadés-
Suay et al. 2017). Assuming an isometric relationship
in the growth of the snout, total snout length (TSL) was
Fig. 1: ‘A’: Blue shark (Prionace glauca L.) stranded in the coast of Garrucha (East Spain, western Mediterranean) with a sword-
fish (Xiphias gladius L.) rostrum in its skull. Scale indicates 50 cm. ‘B’: details of the bill stuck close to the left eye. Scale bar
indicates 5 cm. ‘C’: details of the fractured swordfish rostrum. Scale bar indicates 2 cm.
316 Medit. Mar. Sci., 20/2, 2019, 314-319
calculated for each case in relation to the distance from
the tip to the breaking point. To add further correction,
we observed the arrangement of the paired nutrient ca-
nals at the breaking point, as shown in cross sections, to
compare it with a swordfish analysed by Habegger et al.
(2015). The allometric regression between TSL and body
length (BL), from post operculum to tail fork, was ob-
tained following McGowan (1988).
Results
Case 1: Garrucha (Spain)
On the 17th of February, 2017, a dead adult male
blue shark (TL: 236 cm) was found washed ashore on
the coast of Garrucha (Almería), Spain, 37.18833333º
N 1.81555556º W (Fig. 1A). The animal had an inci-
Fig. 2: ‘A’: blue shark (Prionace glauca L.) stranded in the coast of Ostia province (West Italy, western Mediterranean) with a
swordfish (Xiphias gladius L.) rostrum rostrum piercing its skull. its skull. Scale bar indicates 50 cm. ‘B’: details of the bill’s
incision close to the right eye. Scale bar indicates 5 cm. ‘C’: details of the fractured swordfish rostrum. Scale bar indicates 2 cm.
Fig. 3: ‘A’: blue shark (Prionace glauca L.) stranded in the coast of Vera (East Spain, western Mediterranean) with a swordfish
(Xiphias gladius L.) rostrum rostrum piercing its skull. its skull. Scale indicates 50 cm. ‘B’: details of the bill’s incision close to
the right eye. Scale bar indicates 5 cm. ‘C’: details of the fractured swordfish rostrum. Scale bar indicates 2 cm.
317
Medit. Mar. Sci., 20/2, 2019, 314-319
sive injury between the left eye and the snout. During
the necropsy, the broken tip of a swordfish bill, measur-
ing 180 mm long and 20 mm wide at the breaking point,
was found inside the cranium (Fig. 1B). The bill entered
the skull at 30º angle from the anteroposterior axis. The
lesion was assumed to be the cause of death due to the
associated brain damage. The broken tip found (Fig. 1C)
could be part of a snout ca. 404 mm long, corresponding
to a juvenile swordfish.
Case 2: Ostia (Italy)
On the 8th of March, 2017, an adult female blue shark
(TL: 260 cm) was found stranded on the coast of Ostia,
Italy, 41.70861111º N 12.32638889º E (Fig. 2A). The an-
imal was alive when found, but died shortly afterwards.
The shark showed an advanced state of pregnancy, with
five developed embryos inside her uterus, and no sign of
starvation or disease. An incision was visible between the
first gill slit and the right eye. The necropsy revealed the
presence of a swordfish bill penetrating the flesh between
the optic capsule and the post-orbital process (Fig. 2B).
Apparently, the incision did not damage any sensory or-
gan. The swordfish fragment (Fig. 2C) was 250 mm long
and 30 mm wide at its proximal end, corresponding also
to a juvenile swordfish (snout ca. 505 mm long).
Case 3: Vera (Spain)
On the 28th of February, 2018, an adult female blue
shark (TL: 260 cm) was found dead stranded in the coast
of Vera (Almería), Spain, 37.19388889º N 1.81361111º
W (Fig. 3A, 3B). An incision close to the right eye was
found, entering the head at 20º angle from the antero-
posterior axis. No fragment of bill was found by visual
inspection. Both X-ray (Fig. 4A) and CT (Fig. 4B) also
failed to find fragments of bill inside the incision but,
surprisingly, revealed the presence of a distal fragment
of swordfish bill inside the right nostril, anterior to the
firstly detected injury. No external sign of injury was ap-
parent in this case. The cavity of the nostril was surround-
ed by scarred tissue (Fig. 5). The broken tip of the bill
(Fig. 3C) measured 53 mm long and 12 mm wide at its
proximal end, corresponding also to a juvenile swordfish
(snout ca. 242 mm long).
Case 4: Manacor (Spain)
On the 2nd of August, 2018, an adult male blue shark
(TL: 293 cm) was found stranded and returned to the
water by bystanders several times within an hour in the
coast of Manacor (Balearic Islands), Spain, 39.457296º N
3.277984º W (Fig. 5A). By the time the rescue team ar-
rived, the shark was motionless in lateral decubitus close
to the shore, half meter deep in the water, without reacting
to any stimulus. After euthanasia, the necropsy revealed
signs of starvation and the presence of a distal fragment of
a swordfish bill embedded in the snout (Fig. 5B). The frag-
ment (Fig. 5C), measuring 68 mm long and 15 mm wide at
its proximal end, had entered the centre of the snout from
the right posterior side in a close angle to the anteroposte-
rior axis of the shark and was identified as belonging to a
juvenile swordfish (snout ca. 303 mm long).
Discussion
This survey reports four cases of impalement of blue
sharks by juvenile swordfish in the western Mediterra-
nean in less than two years. The question that arises is
the extent to which such events are instances of acciden-
tal collision between both species or of purposeful be-
haviour. Although we cannot rule out the first possibility,
there are some lines of evidence that conform to the hy-
pothesis that swordfish could actually have intentionally
hit sharks. Firstly, all cases here examined involved only
small swordfish and adult blue sharks. There is the pos-
sibility that juvenile swordfish perceive large blue sharks
as a threat, given that blue sharks are opportunistic preda-
tors that feed on a wide variety of cephalopods and fishes
(Vaske-Júnior et al. 2009; Markaida & Sosa-Nishizaki
2010), and some studies of their diet included swordfish,
although the size of swordfish consumed (ca. 1 kg, see
Vaske-Júnior et al. 2009) seems to be smaller than that
estimated for individuals in the present study. As noted
Fig. 4: Pictures showing the injury inflicted by a swordfish’s
bill to a blue shark stranded in Vera (Spain): ‘A’ ventral view
of the injury with X-rays, showing the fractured bill allocated
inside the nostril. ‘B’ lateral view of the wound using Comput-
ed Tomography, showing the bill perforating the nostril. Red
arrows indicate the location of the swordfish’ fractured bill in
both pictures.
318 Medit. Mar. Sci., 20/2, 2019, 314-319
above, swordfish frequently displays pugnacious be-
haviour, even towards prima facie non-threatening spe-
cies, including humans (Smith 1956, Georgiadou et al.
2010, Ellis 2013). Secondly, in all cases of impalement
on blue sharks reported so far (Penadés-Suay et al. 2017;
present study), the angle of piercing indicates a nearly
horizontal strike with respect to the sharks’ anteroposteri-
or axis. Although there is no reason to exclude the possi-
bility of an accidental collision during an act of predation
to the same prey, a voluntary offense to the blue shark
by juvenile swordfish is to be considered, given that the
type of impalement described could hardly result from
random collisions. Finally, at least the shark stranded in
the coast of Vera showed signs of two diverse interactions
with swordfish happened at different times, which would
refer to two swordfish interactions.
In this context, one may wonder if swordfish use
spearing as a typical defence strategy/territoriality ag-
gression or only as a last resort behaviour against blue
sharks. This is difficult to ascertain. On one hand, sever-
al studies suggest that the swordfish’ bill has important
hydrodynamic and feeding-related functions (Habegger
et al. 2015, Videler et al. 2016) thus bill breakage could
be seriously disadvantageous for swordfish. On the oth-
er hand, at least in billfishes, there are several reports of
apparently healthy individuals with damaged, malformed
or even missing rostra (Frazier et al. 1994). This raises
the possibility that juvenile swordfish may experience a
trade-off between the benefits of repelling a perceived
serious threat and the potential impairment of swimming
performance if the bill eventually breaks.
A third important question concerns the frequency of
such intentional impalements. The present study, and that
by Penadés-Suay et al. (2017), report on stabbings that
were inflicted on the head and, in some cases, resulted
in the death of the victim. However, blue sharks are oce-
anic predators that only exceptionally are washed ashore
when moribund or dead (hence the lack of studies report-
ing these events, see Neto et al. 2013). In general, most
carcasses of large marine vertebrates disappear at sea
(Carretta et al. 2016 and references therein). Hence, there
is the possibility that many cases of fatal impalement
of blue sharks have gone undetected because carcasses
were consumed by scavengers or sank before they could
be discovered. On the other hand, non-fatal impalement
lesions could easily be overlooked. Blue sharks are target
species of long-line fishery and, therefore, many individ-
uals are visually exposed in fish markets. Also, the fact
that only fragments from juvenile swordfish were found
leaves the question on whether they are more prone to
breakage than those of adults, giving then an added diffi-
culty to finding evidence of the collisions in those cases.
However, our study shows that not all impalements result
in a breakage of the swordfish’ bills, thus leaving only a
small external incision that is difficult to draw attention
or even to be noticed unless it is a specific target for ex-
amination. Moreover, old lesions are not visible external-
ly, even when bill fragments remain in the scarred tissue,
unless sophisticated technologies (X-rays, CT) are used,
and only a deep, thorough necropsy could reveal the evi-
dence of such past interactions. In fact, the finding of an
old impalement in shark 3 in our study was serendipitous.
In conclusion, our study reports four cases within less
than two years and only in the Western Mediterranean ba-
Fig. 5: ‘A’: blue shark (P. glauca L.) stranded on the coast of Manacor (Balearic islands, western Mediterranean) with a swordfish
(Xiphias gladius L.) rostrum piercing its snout. Scale indicates 1 m. ‘B’: details of the bill’s incision close to the centre of the snout.
Scale bar indicates 5 cm. ‘C’: details of the fractured swordfish rostrum. Scale bar indicates 1 cm.
319
Medit. Mar. Sci., 20/2, 2019, 314-319
sin, suggesting the relevance of this phenomenon. As an
additional example,, there is one short report describing
putative wounds in a bigeye thresher Alopias supercil-
iosus (Vacchi et al. 2000), similar to the case of a blue
shark reported in the same region by Penadés-Suay et al.
(2017). More attention on this matter is needed, looking
for evidences in all necropsy protocols and investigating
this kind of interactions in other shark species.
Acknowledgements
We would like to thank Equinac for all their field
work and assistance with the investigation in the first two
cases from Spain, MedSharks (especially Aldo Marinel-
li, Simona Clò and Eleonora de Sabata) for their report
and information from the case in Italy and Guillem Félix
along with the team from Palma Aquarium and the Bale-
aric Islands Government (Direcció General de Pesca de
la Conselleria de Medi Ambient, Agricultura i Pesca de
les Illes Balears) for their report on the last case. Special
acknowledgement goes to the staff of the Veterinary De-
partment of the Oceanogràfic Aquarium in Valencia for
letting us use their equipments to take some of the im-
ages shown in this paper and, by doing so, allowing us
to add further insight into the discussion. FJA and JT are
supported by project PROMETEO III of the Generalitat
Valenciana.
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... Impalements caused by billfishes on different taxonomic groups such as whales (Jonsgard 1962;Machida 1970;Oshumi 1973;Major 1979), sharks (Fierstine et al. 1997Penadés-Suay et al. 2017, 2019Jambura et al. 2020;Romeo et al. 2020), even humans (Carvajal et al. 2002Gooi et al. 2007;Mendonça-Caridad et al. 2008;Haddad Jr and Figueiredo 2009;Georgiadou et al. 2010;Galarza et al. 2016), and diverse inanimate objects, such as submarines (Zarudzki and Haedrich 1974) and ships (Gudger 1940;Romeo et al. 2017) have been recorded around the world. In contrast, records of turtles impaled by billfishes are rare (Frazier et al. 1994), even today, when images can be quickly captured using mobile phones. ...
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... sharks) and the potential impairment of high-speed locomotion. The shark species involved in these incidents are usually either the blue shark Prionace glauca (Penadés-Suay et al. 2017, 2019 or the mako shark Isurus oxyrinchus (Cliff et al. 1990;Fierstine et al. 1997), both of which are known to opportunistically prey on fish, including swordfish (e.g. Stillwell and Kohler 1982;Maia et al. 2006;Vaske Júnior et al. 2009). ...
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