Mouth gaping in sharks has been considered
to be either a threat display or a response to
sharksucker irritation, but has never been
examined in greater detail. Another form of
gaping was observed frequently around feeding
scenarios, primarily when sharks swam away from
the food source.
This form of a yawn-like behavior of
Caribbean reef sharks, Carcharhinus perezi, was
videotaped during both standard feeding and
non-feeding scenarios, and examined for both
proximate causation and function. This type of
gaping reflects a simulated bite process,
including all bite phases, but differs from
actual bites in that the duration is as great as
10 times longer, with the expansion phase
disproportionally prolonged and a pause at the
gape's peak. Of all the possible functions
discussed, a maintenance
behavior.
Introduction
Varying forms of gaping have been observed
among all classes of vertebrates and can appear
as responses to physiological functions, such as
respiration (Greco et al. 1993; Baenninger 1997;
Walusinki 2006), expressions of comfort or
discomfort (Henry and Atchison 1979; Hadidian
1980; Mearns 1989), and communication (e.g.,
Smith 1999; Steinhart et al. 2005). For sharks,
it was suggested to be either a reaction to
sharksucker irritation and labeled as
''yawning'' (Ritter 2003) or part of a threat
display (Ritter and Godknecht 2000; Martin 2007)
and simply called ''gaping.'' Neither suggestion
has been thoroughly examined in sharks as
''yawning'' simply refers to an extended mouth
opening that is analogous to terrestrial
animals, and ''gaping'' refers to a threat
display without further clarification.
During feeding experiments with Caribbean
reef sharks, Carcharhinus perezi, gaping has
also been noted after feeding (Ritter 2001).
Such gaping behavior is executed slowly,
entailing all bite phases (Motta et al. 1997),
and most often includes upper jaw protrusion
(e.g., Wilga et al. 2001). The main objective of
this study was to further understand this type
of jaw opening with a special emphasis on both
proximate causation and function.
(...)
Discussion
All regular kinematic biting phases are
exhibited during the presented gaping behavior
with two major differences: (1) an approximate
10 times longer overall duration when compared
with regular bites of C. perezi and other
carcharhinid species (Motta 2004), and (2) a
motion freeze between 0.2 and 0.3 seconds at the
mouth opening's peak. While Motta (2004)
established that the average time of expansion
was 26% of an overall bite duration for
comparable carcharhinid species, the same phase
during these gapes for C. perezi was close to
twice that for protruding gapes, and even longer
for non-protruding gapes. This observation
indicates that slow opening appears to be of
importance during gape behavior. Probable causes
for this gaping behavior are likely feeding
related, indicated by (1) the immediate drop of
the gape rate by more than 72% after the food
was consumed, despite shark density being
reduced by only 18%, (2) the high occurrence of
gaping ( 98%) when the sharks swam away from the
food source, and (3) the lack of other
distinctive behaviors that could have triggered
this form of mouth opening. In order to tear off
a piece of the offered food source, a shark had
to first gouge it. Gouging is very complex
biomechanically where jaw elements are pulled
from their seats or resting positions when
biting into the food and are later repositioned
when the bite is completed (e.g., Motta et al.
1997; Wilga and Motta 1998).
During such motions, especially after
extended tearing, which is often observed at the
offered food source, it is likely that certain
jaw elements may not be repositioned properly
after the bite's execution, and gaping could
then function as a maintenance response.
Prolonged expansion could assist in slowly
pulling the jaw elements once more from their
resting positions before repositioning them into
their appropriate places. A possible
mis-repositioned element could be the
hyomandibula, with attachments to the
neurocranium and jaw, or the upper jaw itself,
with its orbital processes that fit into the
cranial seats when in a resting position
(Frazzetta and Prange 1987; Compagno 1988; Motta
and Wilga 2001). Although it could be argued
that the involved ligaments and muscles that
connect the upper jaw and the cranium ought to
prevent dislocation of the upper jaw (e.g.,
Wilga et al. 2001), protrusion per se is a form
of dislocation since the upper jaw elements are
pulled from their seats, and, hence, proper
retraction could fail occasionally. If indeed
this simulated, non-feeding biting behavior
functions as a maintenance behavior, then
non-protruding gapes would merely reflect a
stretching process, similar to the yawning
function in snakes (e.g., Graves and Duvall
1983).
Six sharks exhibited double-gaping behavior.
The most distinctive difference compared with
single gapes was that the second gapes were
executed significantly faster with a more than
twofold increase in speed. However, the first
gapes exhibited the same duration for all phases
as the single gapes. In addition, two sharks
yawned with their heads and rolled their bodies
during their second gape. It could be postulated
that a speed increase, together with an
additional head and body motion, also acts as a
stretching response for the mouth area and,
hence, further contributes to a proper
repositioning after an initial failed gape.
Although the low number of double-gapes is not
representative, it could imply that these
simulated, non-feeding biting behaviors per se
have a high rate of correct repositioning, and
double-gapes are more of an exception.
Gaping could also function as a cleaning
response. Food is moved through the buccal
cavity by the interactions between head, jaw,
and gill movements in an anterior to posterior
direction (e.g., Wilga et al. 2001), and food
particles could potentially become wedged in the
gill area. An increased volume of water, enabled
through gaping, would increase water pressure
through the buccal cavity and gill area when the
mouth is closing, thereby freeing these
particles. Although food particles were never
seen emerging from the gill slits after gaping
occurred, it is possible that they were
swallowed.
Throughout the vertebrates, gapings are
exhibited for a variety of reasons. In addition
to being a maintenance behavior (e.g., Hadidian
1980), gaping behavior can also reflect stress
or threat (e.g., Baenninger 1987), an arousal
response (e.g., Walusinski 2006), or the
well-known physiological response to a lack of
oxygen (e.g., Kita et al. 2000). Although
post-prandial effects in sharks after feeding
have occurred (Papastamatiou 2007; Papastamatiou
et al. 2007), increased oxygen demands did not
create such responses in these studies. However,
it was hypothesized (Baenninger 1987) that
teleosts may yawn prior to metabolically
demanding events such as feeding. Tricas' (1982)
anecdotal observation that sharks yawned prior
to consuming prey could support this hypothesis;
however, a single yawn to compensate for an
upcoming lack of oxygen seems unlikely for
sharks.
Among sharks, gaping has been linked to
threat display (e.g., Martin 2007) but that form
of gaping is always executed very quickly with
only a partial mouth opening and without upper
jaw protrusion. If the presented form of gaping
indeed were to reflect a threat display, it
would primarily occur when approaching a food
source to intimidate nearby sharks and not when
swimming away, as happened with 98% of the gapes
observed. This assumption would also be true for
a possible stress display. Similarly, during
non-feeding dives, no other sharks were commonly
present when gaping occurred, and the
observation area was unobstructed without the
possibility that a shark was cornered or
hindered in any other way that could have
triggered a stress response. Considering all the
parameters measured in this study, maintenance
behavior appears to be the most likely
explanation for the gaping behavior.
Nevertheless, further study should investigate
which of the upper jaw elements can be pulled
from their resting position to such an extent
that correct repositioning might
