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Aerial Jumping in the Trinidadian Guppy (
Poecilia
reticulata
)
Daphne Soares*, Hilary S. Bierman
Department of Biology, University of Maryland, College Park, Maryland, United States of America
Abstract
Many fishes are able to jump out of the water and launch themselves into the air. Such behavior has been connected with
prey capture, migration and predator avoidance. We found that jumping behavior of the guppy Poecilia reticulata is not
associated with any of the above. The fish jump spontaneously, without being triggered by overt sensory cues, is not
migratory and does not attempt to capture aerial food items. Here, we use high speed video imaging to analyze the
kinematics of the jumping behavior P. reticulata. Fish jump from a still position by slowly backing up while using its pectoral
fins, followed by strong body trusts which lead to launching into the air several body lengths. The liftoff phase of the jump
is fast and fish will continue with whole body thrusts and tail beats, even when out of the water. This behavior occurs when
fish are in a group or in isolation. Geography has had substantial effects on guppy evolution, with waterfalls reducing gene
flow and constraining dispersal. We suggest that jumping has evolved in guppies as a behavioral phenotype for dispersal.
Citation: Soares D, Bierman HS (2013) Aerial Jumping in the Trinidadian Guppy (Poecilia reticulata). PLoS ONE 8(4): e61617. doi:10.1371/journal.pone.0061617
Editor: Melissa J. Coleman, Claremont Colleges, United States of America
Received March 1, 2012; Accepted March 14, 2013; Published April 16, 2013
Copyright: ß2013 Soares, Bierman. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: Work was supported by a 2011 summer fellowship to DS from the Marine Biological Laboratory, Woods Hole MA 02543, www.mbl.edu (no grant #).
The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing Interests: Daphne Soares is a PLOS ONE Editorial Board member. This does not alter the authors’ adherence to all the PLOS ONE policies on sharing
data and materials.
* E-mail: daph@umd.edu
Introduction
The kinematics of swimming has been a subject of interest for
biologists for many decades. Researchers have examined various
aspects of underwater locomotion of fishes from the physics of fin
propulsion, buoyancy and drag and thrust, to muscle physiology
and the adaptation of body morphology (for a review, see [1]). Less
is known about the jumping behavior of fishes. Fishes have been
reported to jump out of the water for three reasons: to catch non-
aquatic prey, to avoid predation from below and to negotiate
obstacles in migration routes. Here, we examine the jumping
kinematics of the Trinidadian guppy, Poecilia reticulata, and propose
that the jumping observed in this species may have evolved for
another reason.
I. Jumping in Fishes
Some fish species jump to consume non-aquatic food items.
This strategy allows fishes to exploit arboreal and terrestrial prey,
such as insects, spiders, and a variety of small vertebrates. One
such example comes from archer fishes. These fish are well known
for their ability to target prey with a bolus of water [2–4], but they
are also able to jump and catch prey in midair. This kinematics of
jumping has been described for the aerial prey-capture maneuvers
of the archer fish Toxotes microlepis [5]. That fish jumps vertically
out of the water from rest to capture prey, using a short thrust
production phase generated by the caudal fin followed by a drop
in acceleration to a motionless glide phase achieving greater
heights with greater numbers of tail strokes. Shih and Techet [5]
(2010) reported that T. microlepis jump up to 2.5 body lengths
(fishes measured 6.8 to 11.1 cm) with velocities of up to 1.4 m/sec.
The fish reaches its maximum velocity in 20 milliseconds and the
parabolic trajectory of the jump overshoots the prey before
descending into the water.
The osteoglossid Silver Arowana (Osteoglossum bicirrhosum) like
archer fishes, leaps from the water to ambush prey resting on low-
hanging branches. Lowry et al. [6] (2005) compared the kinemat-
ics of O. bicirrhosum feeding under water and in the air and reported
that aerial feeding events proceed more quickly (9.2 vs. 3.0 body
lengths/sec) than those in the water. These authors also reported
that in aerial feeding events, the fish increases its swimming speed
as it approaches the prey and, when it is within approximately one
body length of the prey, it bends its body into an S-shaped posture
prior to striking. Fish are out of water approximately 1 body
length. Other studies have mentioned aerial feeding in the four-
eyed fish, Anableps anableps [7], the rivulus, Rivulus hartii [8], the
Atlantic salmon, Salmo salar, and the sea trout, Salmo trutta [5,9], but
none has specifically examined the associated kinematics in detail.
Fishes also leap into the air to escape predators. The ability to
escape predators is critical for individual fitness and is presumed to
be under intense selective pressure [10–13]. At least three
unrelated families of fishes have evolved aerial excursions to avoid
predation. However, involvement of the brainstem startle circuit-
ry, including the Mauthner cells, has yet to be determined for each
family. Mauthner cells are a pair of large neurons that innervate
the axial musculature to produce the unilateral tail-flip or C-start
reflexes in teleost fish.
The marine flying fishes exhibit long glides in the air [14–
17]. Fish probably fly mainly to escape from predators,
particularly dolphins and squid, although these fish may also
jump as an energy-saving strategy for cruising long distances
[18]. Adult flying fish vary in size (15–50 cm body length) and
are broadly divided into two categories: ‘two-wingers’ in which
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the enlarged pectoral fins make up most of the lifting surfaces
(for example Fodiator, Exocoetus, Parexocoetus), and ‘four-wingers’ in
which both pectoral and pelvic fins are hypertrophied, such as
in Cypsilurus and Hirundichthys. Four wingers have been more
thoroughly studied and these fish swim toward the water surface
at high speed (,30 body lengths/sec) with the lateral fins
adducted, leap through the water surface at a shallow angle,
accelerate to take-off speed by taxiing with the lateral fins
abducted and the tail beating in the water (,50 beats/sec;
[17]0. Flying fish do not flap their pectoral of pelvic fins to gain
lift. Fish in the way can ascertain great distances. Cypsilurus
californicus for example, a four winger that measures ,45 cm in
length, produces aerial bouts that will reach heights of up to
eight meters (,20 body lengths), traveling great distances
(,30 m; ,60 body lengths; [17]).
The freshwater African butterfly fish, Pantodon buchholzi (family
Pantodontidae), and the hatchet fish, Carnegiella strigata (family
Gasteropelecidae), both also leave the water, moving along a
ballistic aerial path, in response to startle stimuli [19,20]. The
African butterfly fish (4–6 cm body length) inhabit the first few
centimeters below the water surface and will go into the air when
startled. It is still unclear if the fish are active or passive during the
aerial excursion, but jumps are a result of single pectoral fin
abduction and not by a tail flip. Jumps sometimes include body
rolls [20]. These fish posses a brainstem startle circuitry, including
a pair of Mauthner cells but lack the stereotypical lateral startle
response. Instead, they perform a vertical startle response that can
occur completely within water (2.5–8.4 cm in height) and into the
air (2.25–6.6 cm in height) [20]. The phylogenetically unrelated
hatchet fishes also have extended pectoral fins, hypertrophied
pectoral abductor muscles and jump out of the water when
startled, the mechanism produces this modified startle response is
achieved through the Mauthner mediated circuitry. [21]. Hatchet
fishes can jump either away or towards the stimulus to land behind
it in the latter case. Fish have either vertical (up to ,1.5 body
lengths in height and ,1 body length in distance) or horizontal
trajectories (up to ,1 body length in height and ,4 body lengths
in distance, [21]).
A third reason fishes leap into the air is to overcome
obstacles in their migration path. The Sockeye salmon,
Oncorhynchus nerka, and the brook trout, Salvelinus fontinalis,
negotiate objects that are blocking their path in the stream by
leaping over them [22,23]. Salmon in Alaska are able to jump
up to 2.7 body lengths (,170 cm) at takeoff speeds of
approximately 0.5 m/sec [22,23]. During migration in Colora-
do, the brook trout will jump as high as 4.7 body lengths
(,60 cm) when small in size (,15 cm in length), but only 3.0
body lengths when bigger (20 cm long or more) [23]. The
heights of these jumps are correlated to the depth of the pool
prior to the obstacle; shallower pools constrained the height of
the jumps in larger animals. The trout and salmon jumps are
both produced in water currents, creating a very specific type of
kinetic environment for the generation of leaps.
Lastly, some fish will take advantage of terrestrial habitats [24].
Some teleosts will voluntarily make use of land to evade predators
or escape poor conditions. This behavior has been observed for
killifishes (Cyprinodontiformes) and several different species have
been observed to move across land via a ‘‘tail flip’’ behavior that
generates a terrestrial jump. In Gambusia affinis (a killifish,
Cyprinodontiformes) and Danio rerio (a small carp, Cypriniformes;
both fishes are about 4 cm in body length) use tail flip-driven
terrestrial jumps as a escape, which are kinematically distinct from
aquatic escapes [24].
II. The Trinidadian Guppy
Guppies (Poecilia reticulata; Figure 1A) in Trinidad have rapidly
evolved in response to environmental pressures and are a well-
established animal model for the study of ecology and evolutionary
biology [25–28]. This live-bearing fish is common in the northern
mountains of Trinidad and is endemic to streams that vary in their
ecological characteristics [29]. Crispo et al. (2006) [30] argued that
geographical features have had substantial effects on the genetic
structure and evolution of this species, with waterfalls substantially
reducing gene flow [31]. Fishes from the lower parts of the streams
have more allelic diversity than those found upstream and are
believed to reflect an older, perhaps original population [32,33].
Downstream guppies have repeatedly and independently colo-
nized and adapted to upstream environments [34], resulting in
parallel, rapid changes in life-history traits, behavior and
morphology [26,28,35,36]. This dispersal has been partially
constrained by geological features [31], but is strongly driven by
high levels of predation in the lowlands [25,30,37].
Here, we describe the kinematics of spontaneous jumping
behavior of the male guppy from high predation stocks. We take
advantage of the well-described ecology and evolutionary history
of guppies and suggest possible roles that the jumping behavior
might play in their dispersal.
Methods
All experiments and animal-care activities were approved by the
institutional Animal Care and Use Committee of the Marine
Biological Laboratory (Woods Hole, MA). Fish were borrowed
from Dr. Kim Hoke at the Colorado State University (CSU) and
were shipped to the Marine Biological Laboratory to be used in a
parallel study.
Collection and Rearing in the Laboratory
Female guppies were collected from the Guanapo River, a high-
predation locality in the Northern Range Mountains of Trinidad
[38]. Second-generation family lines, from 20 to 30 wild-caught
gravid females, were established by Dr. Cameron Ghalambor in
2008 at CSU to reduce environmental and maternal influences
(see details in [39]). Male guppies from this colony were shipped to
the Marine Biological Laboratory in the summer of 2011, housed
in custom-made tanks with individual flow-through systems on a
12:12 hour light cycle that were kept in a temperature-controlled
chamber. The fish were fed a limited diet twice daily (Tetramin
tropical fish flake paste). All fish were mature at the time of the
experiment.
Video Recordings
Fish jumped spontaneously out of their home tank (so that tight
grid covers are necessary) and jumped in the experimental tank
after a few minutes of adaptation. No stimulation was necessary to
trigger jumping at any point. For this study, fish were individually
housed for 5 to 20 minutes in a custom-made Plexiglass
rectangular arena (10625625 cm). All of the sides of the tank
except for one were made opaque and we placed a mirror on the
clear side so as to be able to film the fish jumping dorsally and
laterally simultaneously. Most (7 out of 11) of the fish started
spontaneously jumping after a few minutes. Two (2 of 11) fish
spontaneously jumped after about an hour and the remaining two
(2 of 11) did not jump at all. Each jump was recorded using high-
speed videography (X-PRI camera; Del Imaging, Cheshire, CT) at
1000 frames per second and AOS imaging light software (Del
Imaging). Twenty jumps performed by five male fish were
recorded in this set-up. Recordings from another experiment
Poecilia reticulata Jumping
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performed in a different tank, in which all of the sides were opaque
(imaged from above) and in which no mirror was present were also
used. Twenty-two jumps of four different fish were recorded in this
second set-up, in which only the water component was digitized.
Three points were digitized in this study (Figure 1B): 1) head,
midpoint between the eyes, 2) midbody, at the widest part of the
body in the abdomen and 3) the base of tail before the fin rays.
These were used as references for analyses performed using
Proanalyst software (Xcitex, Boston, MA). Measurements of each
jump were taken between the frame prior to the start of the
jumping preparation period and the frame after the return to the
water. On three occasions, fish jumped out of frame or out of the
tank. In those cases, the last frame in view was the last to be
digitized, but we estimated the peak of the jump by examining the
deceleration and path. Fish were photographed, measured and
weighed after each session (Table 1). Presented values are means
Figure 1.
Poecilia reticulata
and body angle analysis. (A) Male Trinidadian guppy, Poecilia reticulata. Scale bar = 1 cm. (B) Schematic of digitized
points and method for measuring body angle. (C) Plot of body angle over time during a jump. * Indicates the fastest velocity of the fish, Lof body
length out of the water. (D) Plot of body angle over time during a startle response. Horizontal dashed lines in the centers of the angle diagrams
represent straight (180u) body positioning. The red box marks the first stroke of the jump and stage 1 of the C-start.
doi:10.1371/journal.pone.0061617.g001
Table 1. Descriptions of fish.
Fish standard length (cm) 1.8560.35
Fish weight (gm) 98610
Height of jump (cm, body length) 6.5461.92, 3.5260.96
Maximum velocity in air (cm/sec) 123.57630.0
Maximum velocity in water (cm/sec) 102.36 cm/sec 633.75
Angle of attack of jump 77.4u624.91
Depth prior to start of jump (cm,
body length)
1.8661.40, 1.0460.73
doi:10.1371/journal.pone.0061617.t001
Poecilia reticulata Jumping
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6s.d. unless stated otherwise. The statistical analysis was
performed using SigmaPlot software (Systat, San Jose, CA).
Results
Guppies spontaneously jumped out of the water without being
stimulated by a startle stimulus or being attracted by prey. This
behavior occurred among groups of fish in their home tanks (not
directly tested here, but observed anecdotally) and when fish were
isolated in individual tanks. All fishes were quiescent before
jumping and never jumped while exploring the tank or swimming.
From a still position, fish reversed using only their pectoral fins and
no body undulations were observed (Figure 1C ‘‘back-up’’ and
Figure 2A; Videos S1 and S2). Backward swimming was slow
(1064.0 cm/sec) for 3.0961.72 cm (0.8260.40 body lengths) and
distance was positively correlated with jump height (r
2
= 0.64,
p= 0.01). In contrast, there was a negative (20.19) correlation
(r
2
= 0.81, p,0.0001) between depth and jump height, so that, in
general, fish located at shallower depths jumped the highest, with
one exception (depth of 2.2 cm and a height of 8.2 cm).
Fish jumped, with adducted pectoral fins (Figure 2B,C,D), from
a depth of 1.8661.40 cm (,one body length) and reached a
height of 6.5461.92 cm (3.5260.96 body lengths; Figure 3A, B;
Videos S1 and S2). Thrust appeared to be generated by axial body
motion. In water, maximum velocities (102.36633.75 cm/sec)
were observed right before or at the moment the fishes’ head broke
the water/air interface. The peak velocities in the air were slightly
higher (123.57630.0 cm/sec), presumably because of decreased
drag, and were achieved immediately after breaking the interface,
at approximate Lto 1 body length out of the water. Higher peak
velocities yielded higher jumps (Figure 3A). Jump height was
positively correlated with the maximum velocity in the air (13.7,
r
2
= 0.64, p= 0.0002) and in the water (17.21, r
2
= 0.75, p,0.0001).
The average fish attack angle, measured as the angle between the
fish’s head and surface of the water, was 77.4u624.91uand fish
with attack angles close to 90ujumped the highest. Typical fast
body thrusts initiated the jump sequence, in which the first bend
from straight (180u) to maximum curvature (65u66.6u) took
7.860.5 msec and was followed by a faster second bend, with
8.061.0 msec from the maximum bend to the next maximum
bend.
The jumping cycle started with fast body thrusts, so that the
velocity, angle and performance of the first two body wall
contractions resembled escape responses. This suggests the
possible recruitment of the same neural circuitry responsible for
startle behaviors. Jumping behavior fits into a larger category of
fast-start behavior, including C-start and S-start escapes and
feeding [40–42]. Several kinematic similarities were observed
between jumping and fast C-start escapes. Similar to many other
species, guppies perform a typical C-start startle response with a
stage 1 C-bend and stage 2 reverse propulsive stroke (Figure 1D;
[43,44]). Jumping behavior started with a strong unilateral body
bend, similar to stage 1, which was followed by an oppositely
directed propulsive bend, similar to stage 2 (Figure 2C second and
third frames, top view). The timing between body bends was
comparable in the two behaviors (Figure 1C, D), but further
detailed kinematic studies are needed to compare the absolute and
relative durations of the different stages and the maximum
curvatures of guppy C-starts. Following the first two body wall
contractions, the jumping behavior continues with a series of high
frequency axial bends (Figure 1C). These movements are similar to
burst swimming, which follows a C-start (Figure 1D; [20,45]). In
jumping, propulsive movements may allow the animal to reach the
peak velocities observed as the fish break the water/air interface.
The burst speed, achieved with a C-start in animals of the same
species and length, is about 70 to 80 cm/sec (extrapolated from
[45] and this study). In comparison, the fastest speed we recorded
Table 2. Statistical data from guppy jumps.
Jumping height vs.:
R
2
Fp
Velocity in water 0.7499 41.9787 ,0.0001
Velocity in air 0.6447 25.4037 0.0002
Depth before jumping 0.8076 62.9712 ,0.0001
Back-up distance 0.6352 12.1901 0.0101
doi:10.1371/journal.pone.0061617.t002
Figure 2. Time-series of guppy jumping behavior. (A) Silhouette series of the preparation period of a jump showing backward swimming using
fins and without body undulations. Arrow shows the direction of movement and silhouettes are shown at 120-msec intervals. Scale bar = 0.5 cm. (B–
C) The jumping portion of the behavior viewed from the side (B) and from above (C). Images are shown at 10 msec intervals. * Indicates the moment
of highest speed in the water (128 cm/sec) and ** indicates the highest speed in the air (150 cm/sec). (D) Example of the out-of-the-water portion of
jump, shown in a different fish that reached height of 6.2 cm. Frames were overlaid at 12 msec intervals. Scale bar= 2 cm.
doi:10.1371/journal.pone.0061617.g002
Poecilia reticulata Jumping
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in water was 100.16633.9 cm/sec, and in the air, we recorded at
top speed of 123630.0 cm/sec.
Discussion
The Trinidadian Guppy, Poecilia reticulata is notable for its fast
evolution and habitat. Guppies are common in the northern
mountains of Trinidad and are endemic to streams that vary in
their ecological characteristics [29]. Fishes from the lower parts of
streams share habitats with predators and have repeatedly,
independently colonized and adapted to upstream environments
that contain no predators [34]. This has led to parallel, rapid
changes in life-history traits, behavior and morphology
Figure 3. Correlation of jump height with velocity and preparatory-period variables. (A) Jump height is positively correlated to greater
velocities in water and air. (B) Jump height is positively correlated with back-up distances observed during the preparatory period and negatively
correlated with depth prior to jumping.
doi:10.1371/journal.pone.0061617.g003
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[26,28,35,36]. We measured the characteristics of spontaneous
jumping in Guppies that were bred in the laboratory from high
predation sites. These fish will spontaneously jump out of the
water without being stimulated by a startle stimulus, or areal prey
items and are not under seasonal migration pressure. Here, we
quantified this behavior and demonstrated that it includes a
preparatory phase of slow backward swimming, followed by fast
forward swimming and an aerial phase. No descriptions of areal
jumping in fishes up until now show this preparatory backward
swimming phase. We also demonstrated that the first two body
bends of the jump share kinematic similarities with a C-start
behavior. The preparatory backward swimming prior to jumping
does not exclude the possibility that this behavior may be C-start
behavior, as ‘‘anti-predator posture’’ movements have been
observed and related to C-start responses in other species [46].
Further examination of startle kinematics and jumping physiology
is needed before any conclusions can be made about a shared
neural substrate. These similarities do not necessarily imply the
involvement of the Mauthner cells, but may suggest the
involvement of elements of the C-start response circuitry. Given
the high-speed nature of jumping kinematics, the sudden onset of
the jumping behavior and the high cost of developing and
maintaining the neural circuitry needed to drive such behavior, it
is reasonable to consider the possibility that some of the same
circuitry elements may be used in both of these jumping and C-
start.
It is possible that guppies also jump out of the water as a form of
startle response, but it is unlikely that jumping is involved in
seasonal migration [47], since guppies are not known to change
territories seasonally. There is also no evidence to date that
guppies feed on arboreal food items like the archer fish or the
Arowana. Previously, Wo¨hl and Schuster [42] (2007) argued that
the predictive start of a hunting archer fish is driven by a
modification of the C-start reticulospinal startle circuitry. One
report has suggested that, in the gulf sturgeon Acipenser oxyrinchus,
jumping may be involved in acoustic communication [48], but this
hypothesis is so far unique and has yet to be developed in guppy.
Because guppy jumping events start slowly with a preparatory
phase, and occur without external stimulation, we hypothesize that
a jumping behavior is deliberate and has been selected as a
strategy for dispersal. Dispersal is advantageous for avoiding
competition among kin [49–51] and for preventing inbreeding
[52–54] and also plays crucial roles in population dynamics,
species persistence, maintenance of genetic variability, preserva-
tion of biodiversity and speciation (see [55–57] for reviews). The
hypothesis that jumping is adaptive for dispersal could be further
tested through comparative studies of upstream and downstream
populations. If local habitat adaptation becomes dominant, then it
can be predicted that secondary populations (upstream with low
predation) are not under the same dispersal pressures as the
original (downstream, high predation) populations and that the
original high-performance jumper founder population will even-
tually lead to a decrease in jumping probability and performance.
Such changes in dispersal phenotype after colonization of a new
habitat have been noted in the literature. Charles Darwin [58] for
example, reported that many bird species endemic to islands have
lost their ability to fly after colonization. Similarly, insect species
that have colonized islands have become flightless [59–62]. Future
studies should include comparisons between populations from
locations with high and low levels of predation, as well as
comparisons of the kinematics of males and females. Male guppies
have been shown to move from their pool of origin more
frequently than females and the probability of emigration is
significantly biased toward upstream movement [63]. Therefore, it
is possible that jumping is more prominent among males from high
predation sites than among other groups.
Supporting Information
Video S1 High speed video of guppy jumping viewed
from the top. Notice the preparation phase.
(WMV)
Video High speed video of guppy jumping viewed on
a split screen.
(WMV)
Acknowledgments
We would like to thank our collaborator Kim Hoke for sharing the
animals, as well as comments on this manuscript; Adina Schwartz and Amy
Streets for animal care and help with the experiments and Melina Hale
and Gal Haspel for their helpful comments.
Author Contributions
DS HB. Conceived and designed the experiments: DS. Performed the
experiments: DS. Analyzed the data: DS. Contributed reagents/materials/
analysis tools: DS. Wrote the paper: DS HB.
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Poecilia reticulata Jumping
PLOS ONE | www.plosone.org 7 April 2013 | Volume 8 | Issue 4 | e61617