The capacity to transition from aquatic to terrestrial environments
is most easily recognized when accompanied by morphological
specializations associated with weight bearing in a gravity-
dominated environment; e.g. fins that adopt a limb-like structure.
However, such anatomical changes are not always required for
transient exploitation of the terrestrial habitat. The mangrove rivulus
Kryptolebias marmoratus [formerly Rivulus marmoratus (Poey
1880)] is an amphibious fish native to mangrove swamps ranging
from central Florida to northern Brazil (Davis et al., 1990). These
small, fusiform teleosts of the order Cyprinodontiformes are notable
for their ability to fully emerse from the water when conditions are
poor (Abel et al., 1987; Taylor, 2000). Tidal fluctuations, elevated
hydrogen sulfide levels and anoxic water conditions are common
in upland mangrove environments (Harrington, 1961). Mangrove
rivulus respond to high sulfide levels and low oxygen levels with
a threshold-mediated emersion behavior (Abel et al., 1987; Regan
et al., 2011). Taylor (Taylor, 2000) has also tied emersion events
to intraspecific competition. Kryptolebias marmoratus have the
ability to respire cutaneously, a trait well suited for their habitat and
emersion behaviors (Grizzle and Thiyagarajah, 1987). Abel et al.
(Abel et al., 1987) showed that K. marmoratus can survive out of
the water for more than 30days in moist leaf litter, and Taylor
(Taylor, 1990) witnessed terrestrial survivability of 66days in an
artificial muddy environment. Kryptolebias marmoratus have
recently been found concentrated inside of logs far removed from
the water, with anywhere from a dozen to 100 individuals in a single
log (Taylor et al., 2008). The discovery of K. marmoratus in this
surprising environment points to another adaptive trait: the ability
to locomote on land.
Cursory descriptions of terrestrial motion such as ‘burrowing’ in
leaf litter, ‘slithering’ on land and using an ‘S-shaped posture’ when
jumping were described by Huehner et al. (Huehner et al., 1985).
Taylor (Taylor, 1992) also employed adjectives with snake-like
connotations in his descriptions, using the term ‘serpentine’ to
characterize the motions of K. marmoratus. In a laboratory study,
Huehner et al. (Huehner et al., 1985) used the terms ‘slithering’ and
‘jumping’ to describe the capture of termites on land and the fish’s
subsequent return to the water. A natural history study (Taylor, 1992)
found terrestrial food items in the stomachs of fish that were sampled
out of the water, providing further evidence that K. marmoratus use
directed terrestrial locomotion to exploit various land resources in
How, then, are these fish able to move from water to land?
Amphibiousness is not a new evolutionary trait in modern fishes.
Proto-tetrapods such as Acanthostegamost likely moved terrestrially
by dragging their bodies across the substrate with modified pectoral
fins in the late Devonian period (Carroll and Holmes, 2008).
Anatomical modifications to facilitate terrestrial movement are
common in amphibious fish. Extant teleosts such as the mudskipper
(Periopthalmus koelreuteri), the clingfish (Sicyases sanguineus) and
the climbing perch (Anabas spp.) actively direct their terrestrial
movement, aided by morphological adaptations to their gill covers
or paired fins (Harris, 1960; Ebeling et al., 1970; Davenport and
Mangrove rivulus (Kryptolebias marmoratus) are small fusiform teleosts (Cyprinodontiformes) with the ability to locomote on
land, despite lacking apparent morphological adaptations for terrestrial movement. Rivulus will leave their aquatic habitat for
moist, terrestrial environments when water conditions are poor, or, as we show here, to capture terrestrial insects. Specimens
were conditioned to eat pinhead crickets on one side of their aquaria. After 2weeks of conditioning, a barrier with a slope of
15deg was partially submerged in the middle of the tank, forcing the fish to transition from water to land and back into water in
order to feed. Kinematics during the transition were recorded using Fastec high-speed video cameras (125–250framess–1). Videos
were analyzed using Didge and ImageJ software programs. Transition behaviors were characterized and analyzed according to
their specific type. Body oscillation amplitude and wave duration were quantified for movements along the substrate, along with
initial velocity for launching behaviors. Kryptolebias marmoratus used a diverse suite of behaviors to transition from water to
land. These behaviors can be categorized as launches, squiggles and pounces. Prey were captured terrestrially and brought
underwater for consumption. Kryptolebias marmoratus’s suite of behaviors represents a novel solution to non-tetrapodal
terrestrial transition, which suggests that fishes may have been able to exploit land habitats transiently, without leaving any
apparent evidence in the fossil record.
Supplementary material available online at http://jeb.biologists.org/cgi/content/full/216/21/3988/DC1
Key words: mangrove rivulus, transitional kinematics, amphibious fish, locomotion.
Received 19 April 2013; Accepted 15 July 2013
The Journal of Experimental Biology 216, 3988-3995
© 2013. Published by The Company of Biologists Ltd
Launches, squiggles and pounces, oh my! The water–land transition in mangrove
rivulus (Kryptolebias marmoratus)
Alexander J. Pronko, Benjamin M. Perlman* and Miriam A. Ashley-Ross
Department of Biology, Wake Forest University, Box 7325, Winston-Salem, NC 27109, USA
*Author for correspondence (email@example.com)
THE JOURNAL OF EXPERIMENTAL BIOLOGY
3989Water–land transition in K. marmoratus
Abdul Martin, 1990). In contrast, quasi-amphibious fish such as
leaping blennies (Hsieh, 2010) and K. marmoratus have no obvious
phenotypic modifications for locomotion on land. Here we describe
the kinematic and behavioral characteristics that allow K.
marmoratus to transition successfully from water to land in pursuit
of terrestrial prey.
MATERIALS AND METHODS
Animals and experimental setup
Twelve specimens of K. marmoratus were used, representing a mix
of wild-caught (Florida Keys, FL, USA, and Belize) and laboratory-
reared individuals. Selected K. marmoratus had a mean (±s.e.m.)
total length (TL; tip of the snout to end of the tail fin) of
4.144±0.438cm. Five of these specimens were housed separately
in 10liter tanks with brackish water (25ppt salinity), maintained at
24±1°C with a 12h:12h light:dark photoperiod, and fed ‘pinhead’
crickets once a day. These fish were conditioned to traverse a barrier
made of Permoplast modeling clay (AMACO, Indianapolis, IN,
USA), flush with the water surface, in the middle of the tank before
feeding on the opposite side of the tank. Conditioning lasted 3 to
4weeks, and involved gradually increasing the barrier length until
the fish had to cross a terrestrial environment before feeding. The
ultimate barrier was sloped at 15deg and plateaued above the water
line (Fig.1). The slope angle at the water–land interface of red
mangrove swamps in the Florida Keys, FL, USA, and Lighthouse
Reef Atoll, Belize, was measured to determine an ecologically
relevant slope (range: 8–16deg; B.M.P., unpublished); the slope used
experimentally was within the range of natural slopes.
Seven of the 12 specimens were used in trials to quantify the
squiggle behavior (defined below). Fish were housed in 1liter plastic
containers under the same conditions as above, and fed 1.5ml of
Artemia nauplii solution per day. Squiggle trials were captured on
a flat, rectangular surface (22.5×34.5cm) made of the same
Permoplast clay, slightly moistened with water to simulate a
transitional microenvironment from water to land. One specimen
was filmed on wetted bench-liner paper at a different facility. Similar
trends were observed for the squiggle behavior on both flat surfaces
and the sloped barrier. All procedures were approved by the Wake
Forest University IACUC (protocol no. A11-134).
All transitional behaviors observed on the sloped barrier were filmed
in the same tank in which the fish were housed. Room temperature
remained at 24±1°C. Data collection took place between 10:00 and
16:00h, during the fish’s daily feeding schedule. Two Fastec high-
speed video cameras (Fastec Imaging, San Diego, CA, USA) were
used to record all events; first at 250framess–1illuminated by two
CN-126 LED lights (CowboyStudio, Allen, TX, USA), and later at
125framess–1under ambient lighting. No differences in behavior
were noted between the two light conditions. One camera was
Dorsolateral high-speed camera 1
Lateral high-speed camera 2
10 liters, 25 ppt salinity, 25°C
Fig.1. Experimental tank setup. Dorsolateral camera 1 is
suspended in parallel with the slope for direct two-dimensional
analysis of recorded videos. Lateral camera 2 is perpendicular to
the tank, with the same view as the reader. System is calibrated
according to known total lengths of fish. Image of mangrove
rivulus courtesy of Tracey Saxby, Integration and Application
Network, University of Maryland Center for Environmental Science
80 ms120 ms136 ms
8 ms 64 ms
Fig.2. Frame-by-frame representative lateral
sequence of launch behavior. Frames are
labeled in milliseconds. Time starts at first
THE JOURNAL OF EXPERIMENTAL BIOLOGY
suspended above the tank at a 15deg angle from the horizontal to
capture the dorsal aspect of motion (this camera was parallel to the
slope of the clay barrier). The second camera was oriented laterally
to the tank (Fig.1). Immobilized crickets were placed in the water
on the right side of the tank for transitional trials and placed on the
barrier within 4cm of the water’s edge for feeding trials. Events
were considered successful if the fish emersed at least half of its
body from the water. After traversing the barrier, fish were returned
to the left side of the tank using a dip net. All recorded behaviors
Additional squiggle trials were recorded by taking fish out of
their 1liter containers and placing them on the wetted flat clay (or
wetted bench liner). A Fastec camera was suspended parallel to the
clay’s surface, and recorded motion from a dorsal view at
250framess–1. No extra artificial lighting was necessary. Only
squiggle behaviors of at least one wavelength were analyzed.
High-speed videos were split into sequential BMP images and
imported into the program Didge (A. Cullum, Creighton University,
Omaha, NE, USA). Images were calibrated for distance using an
object of known size placed in the video field. Two-dimensional
midline coordinates (x,y) of the squiggle transitional behavior were
digitized frame-by-frame using the ‘segment’ function of Didge
(Pace and Gibb, 2011) with 20 segments per total length of each
fish, starting at the tip of the snout and ending at the tip of the tail.
These coordinates were then imported into a spreadsheet program.
Trials that exhibited body contact along the wall of the tanks during
the transitional period were excluded from the analysis. Sigma Plot
(SYSTAT Software, Chicago, IL, USA) was used to create both a
midline trace and a body percentage trace of a representative
squiggle. Adobe Illustrator (Adobe Systems, San Jose, CA, USA)
The Journal of Experimental Biology 216 (21)
was used to create a full-body trace of the squiggle movement. Wave
duration and amplitude of the squiggle motion were analyzed from
the coordinates. Wave amplitude is defined as the distance that the
body of the fish is displaced from a direct line of motion, and is
analyzed by drawing a line between the start and end locations of
a body point in a single wave and then determining how far away
the body point deviates from that line in each frame. Microsoft Excel
(Microsoft Corporation, Redmond, WA, USA) was used to create
an aggregate illustration of the amplitude of each body point at any
given time percentage through a wave. All amplitude data were
standardized to body length. The distance ratio of the squiggle
behavior was also tabulated (Pace and Gibb, 2011). The distance
ratio is the linear distance a body point travels from the beginning
to the end of a wave divided by the total, non-linear distance that
body point actually travels from frame to frame through the same
wave. This ratio hints at the mechanical efficiency of a motion (Pace
and Gibb, 2011): larger ratios have less lateral movement per forward
distance traveled. Distance ratio and maximum amplitude were
evaluated for significant differences between body points in SPSS
(IBM Corporation, Armonk, NY, USA) using a one-way ANOVA
and Tukey’s post hoc test (α=0.05). Homogeneity of equal variances
was found in the distance ratio data (P=0.964) and maximum
amplitude data (P=0.295) using Levene’s test. Videos were analyzed
in ImageJ (NIH, http://rsb.info.nih.gov/ij) to determine the take-off
velocity, take-off angle and height of the launching mode of
locomotion, as well as the distance and velocity of the pounce mode
Kryptolebias marmoratus were observed leaving the water using
three distinct modes of locomotion. ‘Launching’ makes up 54% of
the transitional behaviors, ‘squiggling’ accounts for 26% and
–16 ms0 ms
16 ms24 ms48 ms
Fig.3. Frame-by-frame representative dorsolateral
sequence of launch behavior. Frames are labeled
in milliseconds. Time starts at first forward motion;
movement before time zero represents windup
THE JOURNAL OF EXPERIMENTAL BIOLOGY
3991 Water–land transition in K. marmoratus
‘pouncing’ accounts for the remaining 20%. The first mode,
launching, involved the fish leaping out of the water (N=5, 1–4 trials
per specimen; Fig.2, see supplementary material Movie1). Fish
oriented themselves immediately below the water’s surface, facing
their eventual direction of motion, and used their tail fin for rapid
propulsion, starting from rest. Prior to launch, the fish curled into
an S-bend and rapidly accelerated out of the water (Fig.3, see
supplementary material Movie2). Its tail continued to oscillate even
when completely airborne. Take-off velocity was calculated at
27.5±3.69 (mean ± s.e.m.) body lengths (BL) per second (N=5 fish;
16 total trials), ~1ms–1. Take-off angle from the water was
consistent, averaging 47.6±8.19deg (range: 32.6–64.8deg), allowing
the fish to reach a mean height of 3.2±0.60cm (~0.77 BL) above
the water. If the fish did not clear the barrier, other behavioral modes
were used to reach the water on the other side, such as the squiggle.
The second-most observed transitional behavior was the squiggle,
which is characterized by a bending of the head and tail toward one
another in an oscillatory motion (N=9, 1–2 trials per fish, 1–3 waves
per trial; Fig.4, see supplementary material Movie3). In a squiggle,
the fish curls into a C shape, splaying the pectoral fin located on
the outside of the body curvature over the substrate. The fish then
yaws slightly, using the pectoral fin as a pivot point to push and
lift its body while it sweeps its tail and head through an S-shaped
bend until it reaches the opposite curvature. In the process, the non-
splayed pectoral fin arches off the substrate, pivots around the
splayed pectoral fin, and plants in a splayed configuration in a near
mirror image of the original C shape. This motion, representing a
half wave, is then repeated. Multiple waves may occur throughout
a squiggle. The distinctive bends of the squiggle behavior are best
illustrated by tracing the midline of the fish (Fig.5). Each tracked
point along the body (20, 40, 60, 80 and 100%) behaved in a
repeated, traceable spatiotemporal pattern (Fig.6). The broad ‘figure
eight’ motion of the tail and the tight S trace of 20% TL were
consistent among specimens.
Maximum amplitude of the squiggle wave-form motion differed
significantly between some, but not all, points along the body
(F=29.393, P<0.001; Fig.7). The head and tail had the largest
maximum amplitudes during any single oscillation, while the mid-
body points had smaller amplitudes. The point at 20% of the total
length had the lowest maximum amplitude, which corresponded with
Fig.4. Full-body trace of a representative
squiggle. Percentages mark stage of
motion through a single wave.
–1.5 –1.0 –0.5 0 0.5 1.0 1.5
Fig.5. Midline trace of representative transitional squiggle. Image
represents one half of a wave. Each line represents the midline trace of a
single frame in the image sequence. Consecutive points on a line indicate
body region starting at the tip of the head with 20% total length intervals.
Coordinate (0,0) is located at the midpoint between vertical and horizontal
extremes for half wave.
–1.5 –1.0 –0.5 0 0.5 1.0 1.5
Fig.6. Body-percentage trace of representative transitional squiggle. Image
represents one half of a wave. Each line represents a percentage of the
total length of the fish. Points on a line represent sequential frames, with a
five-frame interval between each point. Open circle represents first frame
for each body percentage. Coordinate (0,0) is located at the midpoint
between vertical and horizontal extremes for half wave.
THE JOURNAL OF EXPERIMENTAL BIOLOGY
the location of pectoral fin insertion; the fish pivot at this point during
the squiggle motion. Fig.8 illustrates the average amplitude of each
point along the body at any given time percentage through a wave.
At approximately 45% through a wave, body points at 80 and 100%
TL had a small, sudden drop in amplitude, which differed from the
overall trends of the other body points. At this point in time, the
vertebral column bent at a point immediately anterior to 80% TL,
reversing the curvature of the segment between 80% TL and the
tail. The same overall path of motion was maintained as the tail
continued toward the head region. The head, 80% TL and tail body
points of the fish had the smallest distance ratio (linear displacement
divided by total distance travelled in a single wave) during the
squiggle, while the point at 20% TL had the highest distance ratio
(F=36.851, P<0.001; Fig.9). The squiggle movement was rapid,
with a wave duration of 0.34±0.17s.
The third transitional behavior was a prey-capture technique,
designated the pounce (N=2, 1–6 trials; Fig.10, see supplementary
material Movie4). Upon locating a cricket placed on the clay barrier,
the fish oriented its body with its head region flush with the
The Journal of Experimental Biology 216 (21)
water–land interface, resting on its ventral side, with both pectoral
fins splayed. The fish then curled its tail toward its body while
slightly moving its head in the opposite direction to make an S
configuration (Fig.10). This wind-up motion was followed by the
fish’s immediate acceleration toward the cricket, sliding across the
substrate in order to grasp the prey in its jaws. If successful, the
fish returned to the water, reversing its S-shaped behavior and
curling its head toward its tail to complete a 180deg turn. Once
immersed, the fish shook its head multiple times and then consumed
the prey item. If unsuccessful at capturing the prey item on land,
the fish either returned to the water with a similar behavior, reversing
the Sshape, or continued to the other side of the tank viathe squiggle
motion. Only a single attempt at prey capture was made while the
fish was on land, regardless of making a successful or unsuccessful
pounce. Pounce behaviors were only observed for crickets placed
no more than 2cm from the water’s edge, with a mean distance of
1.21±0.62cm. Pounce velocity was relatively slow when compared
with launching behavior, with a mean of 5.38±2.42BLs–1, or
Kryptolebias marmoratus were observed to use three very distinct,
consistent behaviors when transitioning from water to land: launches,
squiggles and pounces. Launches and squiggles were directed
locomotory behaviors onto land, while pounces were used
exclusively for terrestrial prey capture. All of these behaviors could
be independently elicited without a stimulus, although some were
generated with specific conditional variables such as the distance
of cricket placement from the water–land interface on the sloped
Ballistic launches from the water by aquatic vertebrates have been
described in numerous species [blacktip sharks (Brunnschweiler,
2005); flying fish (Davenport, 1990); silver arowana (Lowry et al.,
2005); sockeye salmon (Lauritzen et al., 2005); Trinidadian guppies
(Soares and Bierman, 2013)]. The larger species, including sharks
and cetaceans, typically launch into the air after a period of burst
swimming (Brunnschweiler, 2005; Davenport, 1990; Hester et al.,
1963; Hui, 1989; Lauritzen et al., 2005), while smaller fish accelerate
out of the water after at most a few tail strokes from an S-start
windup (present study; Lowry et al., 2005; Soares and Bierman,
2013). The launch behavior of K. marmoratus seems suited to
rapidly propel the fish across a maximal distance. The mean angle
of the launch, 47.6±8.19deg from the horizontal plane, is close to
Head 20 40 60 80 Tail
Mean maximum amplitude (% standard length)
Fig.7. Combined standardized maximum amplitude. Bars represent mean
maximum amplitude during a single squiggle wave in units of percent
standard body length for any given body point. Error bars represent
standard error between fish (N=9, 1–3 waves per fish). Bars with a shared
letter are not significantly different based on Tukey’s post hoc test (α=0.05).
0 10 20 30 40 50 60 70 80 90 100
Amplitude body percentage
Time percentage through wave
Fig.8. Averaged amplitude per given time
percentage through a wave. Points illustrate
averaged amplitude in percent total body
length. Line color differentiates points along the
body. Error bars removed for clarity (N=9, 1–3
waves per fish).
THE JOURNAL OF EXPERIMENTAL BIOLOGY
3993Water–land transition in K. marmoratus
the angle of optimum projection (45deg) in a ballistic motion
consisting of equal vertical and horizontal forces (Price and Romano,
1998). However, there is substantial deviation in this launch angle
both within and among specimens, likely because of slight
differences in the initial position of the fish. Drag from air resistance
should be minimal in this motion, as the fish is in the air for a very
short period of time. Fish sometimes landed in the water on the
other side of the tank, but often hit the barrier and slid across the
clay; the slope of the ramp might inhibit the ability of the fish to
visually predict where it will land before launch.
The squiggle of K. marmoratus is a novel mode of transitional
locomotion, yet employs muscle and bone structure common to all
teleosts. The movement, involving the splaying of the pectoral fin
and yawing motions of the body axis, does not fit into any of the
classic lateral undulation, sidewinding or concertina movements of
snakes, opposing any description of the squiggle as a ‘serpentine
movement’ (Jayne, 1986; Pace and Gibb, 2011; Huehner et al., 1985;
Taylor, 1992). During the squiggle, K. marmoratus relies largely
on its tail for propulsion while the planted pectoral fin acts as a
pivot. Therefore, traction against the substrate plays an important
role in movement efficiency. Slipping was periodically observed in
the area surrounding the water–land interface of the sloped clay
barrier, where the fish could not make enough purchase on the
partially submerged substrate to move forward. Many squiggle trials
were observed and recorded, but some included wall effects and
could only add to a qualitative description of the movement.
However, this suggests that the fish actively seeks complex, three-
dimensional surfaces to aid its terrestrial locomotion, a possible
adaptation to the dense prop roots of its mangrove environment.
Distance ratios for each body point support the tail-based propulsion
method described above (Fig.9). The pectoral fin insertion point at
20% TL has the least amount of lateral movement during the forward
motion, while ratios for the head, tail and 80% TL of the fish were
the lowest, and were not significantly different (Fig.6). However,
the head’s lateral displacement appears to be due to both the tail-
driven rotation at the pectoral fins and the active pushing of the
pectoral fins off the substrate. Comparison to distance ratios for
terrestrial movement in the limbless ropefish shows a higher ratio
than K. marmoratus in every region but 20%, where distance ratios
are similar. These differences indicate that ropefish need a smaller
amplitude of oscillation for forward motion. Ropefish lack clear,
significant differences in the distance ratios between each body
percentage point, which is most likely due to the equality of each
Head 0.2 0.4 0.6 0.8 Tail
0 ms72 ms108 ms288 ms
404 ms496 ms556 ms 652 ms
Fig.9. Distance ratios for each individual body point. Smaller ratios have
more lateral displacement for the same forward movement (N=9, 1–3
waves per fish). Bars with a shared letter are not significantly different
based on Tukey’s post hoc test (α=0.05). Error bars represent standard
Fig.10. Dorsolateral view of frame-by-frame sequence of pounce behavior, with cricket placed on the slope out of the water. Frames are labeled in
milliseconds. Time starts at frame before the windup motion. Dashed line indicates the water–land interface.
THE JOURNAL OF EXPERIMENTAL BIOLOGY
body point’s contribution to oscillatory motion (Pace and Gibb,
2011). This serves as a contrast to K. marmoratus, where a large
disparity is found in distance ratios between the extremes of the
fish and the pectoral fin insertion point at 20% TL. Distance ratio
is a proxy for the mechanical ‘efficiency’ of a movement, as a lower
distance ratio means that less time is spent moving forward (Pace
and Gibb, 2011), and more time spent moving laterally.
A single trial was recorded in which the fish squiggled through
three microenvironments – aquatic (0–24.9% emersion), transitional
(25–74.9% emersion) and terrestrial (75–100% emersion) – in three
uninterrupted, sequential waves. Each wave had a trend of increasing
oscillatory amplitude as the fish moved from water to land
(supplementary material Fig.S1). The squiggle motion of the fish
while still submerged (0–25% emersion), included the addition of
aquatic tail-based propulsion, and a smaller lateral displacement was
observed. Distance ratios were higher in the aquatic zone than the
terrestrial microenvironment; however, the transitional zone tended
to have the highest distance ratios for each body point
(supplementary material Fig.S2). Further kinematic analyses and a
larger sample size are needed for each zone to elucidate solid
The pounce behavior is also seemingly novel in its execution.
The splaying of pectoral fins for stability on the substrate and the
‘line-up’ behavior while still immersed are unique. Mudskippers
(Periopthalmus argentilineatus) are well known for their use of
pectoral fins during terrestrial locomotion, and the strategy of fin
splaying seems to be similar; fins are oriented to maximize contact
with the ground (Pace and Gibb, 2009). However, a kinematic mode
similar to the pounce has not been described in mudskippers (Pace
and Gibb, 2009). Kryptolebias marmoratus often swam to and from
the water–land edge for an indefinite amount of time, stopping to
line up with their prey and then swimming away multiple times
before attempting a pounce. Although the S-bend wind-up behavior
for the pounce is similar to the launch wind-up, the fish’s body
orientation is much more horizontal with respect to the water’s
surface and the velocity of the motion is much slower. This suggests
that the fish are able to modulate the force of their rapid
accelerations. Similar S-bend ambush mechanisms have been
recorded aquatically for elongate fishes (Porter and Motta, 2004).
The narrow range of predator–prey distances observed for the
pounce suggests that this mode of behavior is very opportunistic.
Kryptolebias marmoratus only attempted one pounce behavior per
line-up. If unsuccessful, the fish remained stationary, and eventually
either continued to locomote across the clay or returned to the water.
There was no second consecutive attempt at prey capture. Upon
successful prey capture, the fish always returned to the water,
shaking its prey vigorously before attempting to consume it. No
incidence of complete terrestrial food consumption was observed.
Thus, K. marmoratus may go through a period of starvation when
on land, which corresponds with Brockmann’s (Brockmann, 1975)
observation of emaciation in K. marmoratus found far from sources
The recorded data for the slope trials show that when given an
environment conducive to all three modes of locomotion, the launch
behavior represents 54% of the fish’s transition kinematics, while
the pounce and the squiggle made up 20 and 26% of the fish’s
movements, respectively. These numbers are not entirely accurate
descriptors of the observed frequency of the locomotory modes. The
frequency of the launching behavior when compared with the other
behaviors may be the product of the laboratory environment, and
may not necessarily reflect the incidence of behaviors in the natural
habitat of K. marmoratus. The squiggle behavior was used somewhat
The Journal of Experimental Biology 216 (21)
more frequently than the analyzed data reflect; many of these
instances involved wall-effects, non-transitioning behavior, or could
not be properly filmed and identified and were thus discarded.
Because the fish had to travel a set distance to reach their food and
encountered no predators during this experiment, it can be postulated
that the launch transitional behavior was the most energetically
efficient when compared with the squiggle because it covered a
longer distance with a single effort. The squiggle seems to be a
more cautious approach to locomotion: in their natural habitat, fish
would be able to alter the direction of movement in order to find
shelter or escape potential predators. The blind landing nature of
the launch and inability of the fish to alter its direction once in the
air suggests that the launch may be a more dangerous method of
transitioning from water to land in a mangrove swamp. We noted
that fish were more likely to squiggle on the wetted, flat clay surface
in places where water had pooled or beaded up. When on completely
dry clay, the fish implemented another, strictly terrestrial mode of
jumping, a ‘tail-flip’, in which the fish lifts and curls its head over
the center of mass and uses its tail to propel itself away from a
stimulus (Gibb et al., 2011; Gibb et al., 2013). As the tail-flip is not
a transitional behavior, we did not describe it in this study. It is
possible that the squiggle behavior is only used in a narrow range
of environments, where there is not enough water to execute an
aquatic launch and not enough traction to execute a tail-flip.
Squiggle transitional behaviors have been observed in the wild from
fish that were captured and returned to their habitat (B.M.P.,
Though this study is the first published description of the
transitional behavior of K. marmoratus, limited evidence suggests
that some other fishes may move terrestrially using a similar squiggle
method, such as three walking catfish species [Clarias batrachus,
Clarias gariepinus and Ictalurus punctatus (Pace et al., 2010)].
Furthermore, Cucherousset et al. (Cucherousset et al., 2012) have
reported instances of a pounce-like behavior in the wels catfish
(Silurus glanis) when ambushing birds found along the shore. The
kinematics of terrestrial motion in such organisms have not yet been
quantified; however, a comparative study between K. marmoratus
and similarly behaving teleosts would be a useful complement to
this study. We did not quantify fully terrestrial behavior in this study.
However, K. marmoratus jump using a directed, repeatable motion
on land that requires further, in-depth analysis. Huehner et al.
(Huehner et al., 1985) described K. marmoratus as active foragers,
citing personal observations of fish leaping out of the water to catch
moving prey. This was not observed in any of the feeding trials, as
almost all pounces were directed at stationary crickets. Further study
of prey-capture behavior is needed to determine whether K.
marmoratus will actively hunt terrestrial food or is strictly an
opportunistic terrestrial feeder.
The ability of K. marmoratus to have multiple directed modes
of transitional kinematics is evolutionarily significant. Although K.
marmoratus is not a basal teleost, having possibly diverged from
its South American congeners as recently as 2 million years ago
(Tatarenkov et al., 2009), its amphibious nature and ability to exploit
land resources with behavioral modification may serve as a model
for earlier fishes. Currently, an increasing pressure to exploit land
resources is considered one of the main ‘pushes’ for tetrapod
evolution in amphibious fish (Long and Gordon, 2004). Taxa such
as K. marmoratus suggest that pressure and eventual ability to
venture onto land does not necessarily correlate with limb
development. Kryptolebias marmoratus
morphological adaptations for transition to a terrestrial environment,
but is still able to successfully exploit land habitats. A
has no obvious
THE JOURNAL OF EXPERIMENTAL BIOLOGY
3995Water–land transition in K. marmoratus
morphologically similar ancient amphibious fish, though not
necessarily an evolutionarily close relative, could also have exploited
terrestrial resources with modified behavior, which would not be
readily apparent in the fossil record.
We thank Dr Ryan Earley for contributing a portion of the specimens used in this
study. We also thank Dr Susan Fahrbach, Dr Miles Silman, members of the
Ashley-Ross lab and two anonymous reviewers for their helpful feedback on the
This study was conceived by B.M.P. and M.A.A.-R., designed and executed by
B.M.P. and A.J.P., and all three authors contributed equal amounts to the
interpretations of the results. All three authors made equal contributions to the
No competing interests declared.
Financial support was provided by the Wake Forest University Department of
Biology and the Wake Forest Undergraduate Research and Creative Activities
Center (URECA) to A.J.P.
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