MARINE ECOLOGY PROGRESS SERIES
Mar Ecol Prog Ser
Vol. 482: 255–263, 2013
doi: 10.3354/meps10286
Published May 22
Altered swimming gait and performance of
dolphin mothers: implications for interactions with
tuna purse-seine fisheries
S. R. Noren*
Institute of Marine Science, Center for Ocean Health, University of California Santa Cruz, 100 Shaffer Road, Santa Cruz,
California 95060, USA
ABSTRACT: Physical constraints while carrying an infant represent one of many reproductive
costs. For bottlenose dolphins Tursiops truncatus, near-term pregnancy and ‘carrying’ a calf in
echelon position (calf alongside mother’s mid-lateral flank) alter maternal swimming gait and performance. As calves mature an alternate form of ‘carrying’, infant position (calf underneath
mother’s tailstock) dominates. To complete our understanding of locomotion during motherhood
in dolphins, kinematics (peak-to-peak stroke amplitude, A, and tailbeat oscillation frequency, f )
and performance (swim speed, V ) while ‘carrying’ a calf in infant position were quantified. The
relationship (slope) for A and V differed between solitary swimming and swimming with a calf in
infant position (Z = −1.706, p = 0.088) as did the relationship (slope) for f and V (Z = −3.699, p <
0.001). Compared to solitary swimming (2.17 ± 0.02 m stroke−1; n = 166), mothers ‘carrying’ a calf
in infant position had diminished distance per stroke (1.82 ± 0.07 m stroke−1; n = 27, t = 5.209, df =
191, p < 0.001; means ± SE) concomitant with a significant reduction (54%) in average swim speed
(n = 27, 166, T = 629.00, p < 0.001). These results have implications for dolphins that interact with
tuna purse-seine fisheries in the Eastern Tropical Pacific (ETP). Dolphins ‘carrying’ a calf may be
unable to achieve speeds sustained by groups evading fishermen. To maintain proximity with the
group, mothers may become separated from their calf. Permanently separated dependent calves
represent unobserved mortality events, which may partially explain the non-recovery of depleted
ETP dolphin populations.
KEY WORDS:
Cetacean
Kinematics · Locomotion · Eastern Tropical Pacific · Maternal investment ·
Resale or republication not permitted without written consent of the publisher
Maternal investment in mammals includes gestation, lactation, and other forms of parental care. Carrying an infant is considered to be the most costly
form of parental care after lactation (Altmann &
Samuels 1992, Kramer 1998) and has been described
in 6 of 19 eutherian mammalian orders (for review
see Ross 2001). This behavior provides a solution for
mothers of diverse taxa that must maneuver within
their environment to forage and avoid predators
while accompanied by their young offspring (Ross
2001), which are handicapped by small body size,
physiological immaturity, and inexperience (Carrier
1996). Infant carrying behavior was only thought to
evolve in aerial and arboreal environments (Ross
2001), as for young primates which must accompany
their mothers yet are encumbered by underdeveloped locomotor performance (Altmann & Samuels
1992, Doran 1992, Wells & Turnquist 2001).
*Email: snoren@biology.ucsc.edu
© Inter-Research 2013 · www.int-res.com
INTRODUCTION
256
Mar Ecol Prog Ser 482: 255–263, 2013
Recent research has provided evidence of ‘carrying’ an infant in an aquatic environment. Although
cetaceans (whales and dolphins) cannot physically
carry their performance impaired calf (Noren et al.
2006), the mothers escort their calf in either echelon
position or infant position (Fig. 1). Early in life, echelon position is the dominant behavior displayed by
cetacean mother–calf dyads (McBride & Kritzler
1951, Norris & Prescott 1961, Au & Perryman 1982,
Taber & Thomas 1982, Krasnova et al. 2006); it
enables neonatal cetaceans to maintain close proximity to their mothers during travel (Norris & Prescott
1961, Lang 1966) by increasing the swimming efficiency of the infant (Kelly 1959, Weihs 2004, Noren et
al. 2008). As cetacean offspring increase in size, infant position becomes the dominant formation swimming strategy for mother–calf dyads (Taber &
Thomas 1982, Mann & Smuts 1999, Xian et al. 2012).
For example, bottlenose dolphin Tursiops truncatus
calves are observed in this position 38% of the time
Fig. 1. Tursiops truncatus. Bottlenose dolphin mother ‘carrying’ its calf. (a) Echelon position: calf in close proximity to its
mothers’ mid-lateral flank. (b) Infant position: calf in very
close positioning underneath its mother’s tailstock. Photo
credit: Dolphin Quest
by 1 yr postpartum (Gubbins et al. 1999), and this
behavior remains important for calves up to 4 yr old
(Gibson & Mann 2008). Indeed, dolphin calves tend
to assume infant position when they are startled or
tired (Gubbins et al. 1999) or traveling (Mann &
Smuts 1999).
Like echelon position (Weihs 2004, Noren et al.
2008), infant position improves the swimming capabilities of calves (Weihs 2004, Noren & Edwards
2011). However, empirical studies demonstrated that
the hydrodynamic benefits afforded by calves in
infant position are not as great as those gained by
calves in echelon position (Noren & Edwards 2011).
Noren & Edwards (2011) suggested that older,
stronger swimming calves are predominately in
infant position because by relinquishing some hydrodynamic benefits of echelon position they gain other
important benefits of infant position (Gubbins et al.
1999), including camouflage from predators. Nonetheless, there are maternal costs associated with
swimming with a calf in echelon position (Noren
2008), and it is likely that there are maternal costs
associated with swimming with a calf in infant position, although this remains to be quantified.
Current interactions between dolphins and tunapurse seine fisheries in the eastern tropical Pacific
Ocean (ETP) make the study of swimming abilities in
dolphin mothers especially timely. These fisheries
capture schools of yellowfin tuna Thunnus albacares
by locating, chasing and encircling herds of associated dolphins. As a result of this fishery, eastern
spinner Stenella longirostris oreintalis and northeastern offshore spotted Stenella attenuata attenuata
dolphins are only at 29% and 19%, respectively, of
their pre-1959 abundance levels when the yellowfin
tuna purse-seine fishery initiated setting on dolphin
schools (Wade et al. 2007). Despite a reduction in
observed dolphin mortality associated with this fishery, dolphin populations that were depleted are not
recovering, and the lack of recovery may be attributable to some unobserved mortality (Gerrodette &
Forcada 2005). Archer et al. (2004) observed a deficit
of dolphin calves in the historical bycatch, and suggested that separation of calves during fishery induced chase may represent unobserved mortality
events. They recommended that research efforts
should focus on how mother–calf pairs could become
separated during tuna purse-seine fishery interactions to elucidate the magnitude of unobserved
calf mortality and the effect that this may have on
dolphin populations.
In view of this, I examined the kinematics and performance of dolphin mothers swimming with their
Noren: Motherhood alters swimming gait and performance
calf in infant position (Fig. 1a) and compared this to
periods of solitary swimming by the mother (>1 m
from their calf and all other dolphins) to aid in completing our understanding of how ‘carrying’ an infant
affects maternal swimming in dolphins. The morphology and swimming kinematics of dolphins are
characteristic of the thunniform mode, which is typical of some of the fastest marine vertebrates, including scombrid fishes, laminid sharks, and cetaceans
(Lighthill 1969). Dolphins generate thrust exclusively
with a high aspect-ratio caudal hydrofoil (tailflukes;
Fish & Hui 1991). Thus, a qualitative assessment of
swim effort was obtained by considering both tail
movement amplitude and beat frequency; higher
amplitudes and frequencies are associated with
greater energy expenditure (Kooyman & Ponganis
1998). Performance was also examined quantitatively by comparing swim speeds. These data can
help elucidate how mother–calf pairs may become
separated during fishery induced chase. Understanding the effects of carrying an infant are important
because this type of maternal investment (infant carrying) has received little attention to date.
MATERIALS AND METHODS
257
Swimming trials
During each data collection interval, the swimming
motions of the dolphins were recorded daily throughout daylight hours. A submerged SCUBA diver, sitting stationary on a wide ledge on one side of the
enclosure, used a digital video camcorder (Sony Hi-8
in an underwater housing; Amphibico Dive Buddy,
Amphibico) to film the dolphins as they passed by.
The SCUBA diver kept the video camera stationary
such that the dolphins were only filmed when they
were in the field of view of the camcorder. The animals swam ~1 to 3 m below the surface of the water
and swam in a straight line path within 7 to 8 m parallel to the SCUBA diver. Experimental swim sessions included both opportunistic (no reward) and
directional between 2 trainers (reward based). For
opportunistic trials, the SCUBA diver was positioned
in an area of the lagoon where the dolphins passed in
a stereotypic straight-line path. For directional trials,
the trainers were positioned across the lagoon from
each other in a way that forced the dolphins to swim
a straight-line path. Rewards (tactile stimulation,
toys, and food) were based on the intensity of the
swimming provided. Standard operant conditioning
was used to train the directional swimming.
Experimental dolphins
Video analysis
Behavioral and physiological development of delphinid calves are generally similar across species
(Noren & Edwards 2007). The bottlenose dolphin
served as a model because its prevalence in human
care provided trained individuals for the experimental protocols. We studied 4 adult dolphin mothers in a
large, oblong semi-natural lagoon at Dolphin Quest
Hawaii (high tide dimensions: 43 × 53 × 7 m deep,
low tide dimensions: 37 × 46 × 5 m deep). The dolphin mothers had been held at the facility for a minimum of 4 yr, thus they were acclimated to their environment. Dolphins were fed a mixed diet of capelin,
herring, and squid supplemented with vitamins. Studies occurred from October 2003 to November 2005,
which corresponded to the time when the calves
were 1 wk to 2.5 yr of age. Data were collected during 1 wk intervals on a quarterly basis for the first
year, and during 1 wk intervals on a semi-annual
basis for the second year of the study. Infant position
swimming was represented by mothers swimming
with a calf ranging in age from 8 to 318 d (mean ± SE:
71 ± 17 d, median: 31 d). Water temperature during
the experimental period ranged from 24.0 to 26.7°C
(25.3 ± 0.4°C).
Short (2 to 6 s) video clips of the dolphins swimming were extracted from the videotapes using digital video editing software (Pinnacle Studio 8, Pinnacle Systems). Distinct morphological features including
the rostrum tip, cranial insertion of the dorsal fin, and
the fluke tip were digitized at a rate of 60 fields per
second of video using a motion-analysis system (Peak
Motus 6.1, Peak Performance Technologies) following methods similar to Skrovan et al. (1999) and
Noren et al. (2006). To correct for any slight deviations in the dolphins’ vertical angle in the water column, all coordinates were transformed so that the
starting position of the cranial insertion of the dorsal
fin (digitized point closest to the center of mass) represented the zero position on the y-axis. The measured body length (beak tip to fluke notch) of the dolphin mothers, which did not change during the study
interval because the females had already attained
mature body length, provided a scalar so that the
system could calculate instantaneous transformed
coordinates, velocity, and acceleration for each digitized point. Only video clips where dolphins swam
steadily, maintained a parallel path to the camera
Mar Ecol Prog Ser 482: 255–263, 2013
258
lens, and had no qualitatively apparent acceleration
were included in the analyses. In addition, a rock
within the field of view of the camcorder was also
digitized to ensure that the camera was held steady
throughout the entire pass of the individual. Digitized video clips that indicated that the reference
point moved were excluded from the analyses.
Swimming kinematics, Strouhal number,
and swim performance
The video clips were divided into 2 swimming
behavior categories: (1) infant position (calf underneath mother’s tailstock; Fig. 1b), and (2) solitary
swimming (mother >1 m away from calf and all other
dolphins). A quantitative assessment of gait was
obtained by calculating peak-to-peak fluke stroke
amplitude (A; in m) and tailbeat oscillation frequency
(f; in strokes s−1) from the data. Multiple sequential
strokes were used to calculate the mean stroke
amplitude and tailbeat oscillation frequency for each
video clip. Distance per stroke was also calculated so
that any differences in stroke frequency between
swimming behaviors could be detected without the
compounding effect of swim speed, since tailbeat frequency increases significantly with swim speed in
odontocetes (Fish 1993, 1998, Skrovan et al. 1999,
Fish et al. 2003, Noren et al. 2006). The principal
wake parameter, a dimensionless number called the
Strouhal number (St), was calculated according to
Triantafyllou et al. (1993):
St = f × A / V
(1)
where f = tailbeat oscillation frequency in strokes s−1,
A = peak-to-peak fluke stroke amplitude in m, and
V = the average of the instantaneous swim speed
(m s−1). A quantitative assessment of swim performance was possible by comparing swim speeds across
swimming behaviors.
Statistics
We examined 4 adult females with dependent
calves. Each performed numerous swim trials and
the swim speed for each trial varied. A mixed model
regression approach was used to determine the
effect of swimming behavior (B, categorical variable)
and peak-to-peak stroke amplitude (A, continuous
variable) on swimming speed (V, continuous variable). Likewise, a mixed model regression approach
was used to determine the effect of swimming behav-
ior (B, categorical variable) and tailbeat oscillation
frequency (f, continuous variable) on swimming
speed (V, continuous variable). An interaction term
was included to test the homogeneity of slopes
assumption; this was used to determine if the relationship (slope) between A (or f ) and V varied as a
function of B. In all cases, ‘individual’ was treated as
a random term. The full models were:
V=B+A+B×A
(2)
V=B+f+B×f
(3)
These standard statistical analyses were performed
using Sigma Stat version 2.03 and SYSTAT version
13.1 (Systat Software). All means are denoted with
±1 SE.
RESULTS
The random term ‘individual’ did not affect any of
the relationships noted in the statistical analyses section (mixed model p > 0.2). For both models, the interaction term was significant (we used p ≤ 0.10 as the
critical p-value based on low sample size). The relationship (slope) for A and V differed across swim
behaviors (Z = −1.706, p = 0.088) as did the relationship (slope) for f and V (Z = −3.699, p < 0.001; see
Fig. 2).
Given that ‘individual’ did not affect the parameters being tested, all dolphins were combined to
determine the relationships for A and V and f and V
for each swimming behavior. Least squares linear
regression analyses were used and the significance
of these regressions were determined using F-tests.
The results are shown in Table 1 and allow for comparisons to other studies on dolphin swimming kinematics that utilized least squares linear regressions to
report the influence of A and f on V (Fish 1993,
Skrovan et al. 1999, Fish et al. 2003, Noren et al.
2006, 2008, 2011, Noren 2008, Noren & Edwards
2011).
Comparisons of distance per stroke, Strouhal
number, and swim speed were also made across
swimming behaviors. Because individual did not
have an effect, data were pooled across individuals
and differences between the 2 swimming behaviors
were determined using student’s test or MannWhitney rank sum test when normality or equal
variance failed. Normality was determined using
the Kolmogorov-Smirnov test and equal variance
assumption testing with the Levene median test.
Distance per stroke was less for mothers with a calf
Noren: Motherhood alters swimming gait and performance
7
259
Table 1. Tursiops truncatus. Swimming kinematics of mothers during solitary swimming and when accompanied by
their calf in infant position. A = peak-to-peak stroke amplitude; f = tailbeat oscillation frequency; V = swim speed
a
6
5
4
3
Kinematic
Maternal solitary
swimming
Maternal infant
position swimming
A
V = 2.13 A + 2.36
r = 0.23, F = 9.49,
p = 0.002, n = 166
Not correlated
r = 0.24, p = 0.227,
n = 27
f
V = 2.05 f + 0.20
r = 0.88, F = 582.56,
p < 0.001, n = 166
V = 0.98 f + 0.81
r = 0.60, F = 13.93,
p < 0.001, n = 27
Swim speed (m s–1)
2
1
0
0.0
0.2
0.4
0.6
0.8
1.0
1.2
Peak-to-peak tailbeat amplitude (m)
7
achieved during solitary swimming (3.91 ± 0.09 m
s−1, n = 166, T = 629.00, p < 0.001). Similarly, the
maximum performance of dolphins accompanied by
a calf in infant position (2.98 m s−1) was approximately half of that achieved during solitary swimming (6.32 m s−1).
b
6
5
4
3
DISCUSSION
2
1
0
0.0
0.5
1.0
1.5
2.0
Tailbeat frequency (strokes
2.5
3.0
s–1)
Fig. 2. Tursiops truncatus. Kinematics in relation to swim
speed for 4 mothers during solitary swimming (d) and with
their calf in infant position (s). Individual did not affect
either relationship (mixed model p > 0.2). (a) The relationship for peak-to-peak stroke amplitude (A) and swim speed
(V ) differed across swim behaviors (Z = −1.706, p = 0.088).
Solid line: relationship for A and V for solitary swimming.
The relationship for A and V was not significant for infant
position swimming. (b) The relationship for tailbeat frequency (f ) and swim speed (V ) differed across swim behaviors (Z = −3.699, p < 0.001). Solid and dashed lines: relationship for A and V for solitary and infant position swimming,
respectively. See Table 1 for the statistics for the linear
regressions
in infant position (1.82 ± 0.07 m stroke−1; n = 27)
compared to periods of solitary swimming (2.17 ±
0.02 m stroke−1; n = 166, t = 5.209, df = 191, p <
0.001), yet Strouhal numbers were similar across the
2 swim behaviors (swimming with calf in infant
position: 0.316 ± 0.0161; solitary swimming: 0.341 ±
0.005; T = 2351, n = 27, 166, p = 0.320). Nonetheless,
the average speed of dolphin mothers swimming
with a calf in infant position (1.81 ± 0.10 m s−1, n =
27) was significantly lower than the average speed
Although carrying an infant is considered costly
(Altmann & Samuels 1992, Kramer 1998), and it is
evident across arboreal, aerial, terrestrial, and
aquatic environments, only a few studies have examined the energetic and locomotor consequences of
‘carrying’ for the carrier. These studies have predominately focused on terrestrial species, primarily primates (Altmann & Samuels 1992, Schradin & Anzenberger 2001) and marsupials (Baudinette & Biewener
1998). Nonetheless, Noren (2008) provided evidence
of locomotor consequences for dolphin mothers
swimming alongside a calf, but only investigated the
effect of ‘carrying’ when the dolphin mothers swam
with their calves in echelon position (Fig. 1a), because echelon position was considered to be the primary formation of mother–calf pairs. Yet observations of wild dolphins have shown that from 1 to 2 mo
post-parturition the frequency of echelon position
decreased from 69% to 11% while infant position increased from 8% to 18% of the time (Mann & Smuts
1999). Infant position appeared to remain important,
as calves up to 4 yr old were observed in this position
39% of the time (Gibson & Mann 2008). Captive dolphins have shown similar trends. During the first
year of life, the frequency of echelon position decreased from 67% to 23% while infant position
increased from 7% to 38% of the time (Gubbins et al.
1999). Given the predominance of infant position as
the calves mature, an examination of the locomotor
260
Mar Ecol Prog Ser 482: 255–263, 2013
consequences of maintaining a calf in infant position
(Fig. 1b) is needed to fully elucidate the maternal
costs of ‘carrying’ cetacean calves.
Dolphins ‘carrying’ a calf in infant position
Although formation locomotion is vital to the calf’s
survival by ensuring that mother–infant dyads remain intact during travel, it does not come without a
cost for the mother. The presence of the calf may disrupt the boundary flow around the mother causing it
to separate, which would increase turbulent flow
(Weihs 2004, Weihs et al. 2006). Meanwhile, the entrained calf could increase the surface area of the
mother. This would effectively increase the drag of
the swimmer and require more power to overcome
increased turbulent flow and drag (Webb 1975). As a
greater proportion of maternal power output is
needed to accommodate increased turbulent flow
and drag, there will be less energy available to propel the individual because total work is limited by its
metabolic scope (Weibel et al. 1987). Indeed, the
results suggest that dolphins swimming with a calf in
infant position must exert more effort compared to
solitary swimming, as evidenced by a reduction in
speed per a given tailbeat frequency (Fig. 2b).
In addition, the presence of the calf appears to alter
the swimming gait of the mother. Mothers with a calf
in infant position exhibited a size-specific stroke
amplitude of 0.23 ± 0.01 body lengths (mean ± SE,
n = 27) that was lower in magnitude than the mean
size-specific stroke amplitude (0.30 ± 0.00 body
lengths, n = 166) exhibited during periods of solitary
swimming. The reduced stroke amplitudes for mothers swimming with a calf in infant position may be
due to a mechanical constraint as the mothers
avoided bumping their calf with their tailflukes. Because power output per stroke is limited by mechanical constraints (Fish & Hui 1991) this undoubtedly
alters locomotor performance.
Indeed, the combination of increased drag and
altered gait in dolphins swimming with a calf in formation resulted in reduced performance. Mothers
swimming with a calf in infant position had a 16%
decrease in distance covered per stroke compared to
when the mothers swam alone. In addition, mean and
maximum swim performance was reduced by 54%
and 53%, respectively, when the mothers swam with
their calf in infant position compared to periods of
solitary swimming. These results are comparable to
the observation that dolphin mothers swimming with
a calf in echelon position had a 13% reduction in dis-
tance per stroke, 46% reduction in mean swim performance, and 24% reduction in maximum swim
performance compared to periods of solitary swimming (Noren 2008).
Interestingly, even though maternal gait and performance is altered by formation locomotion, the
principal wake parameter (termed the Strouhal number) seems to be unaltered by the mode of locomotion. The Strouhal number for mothers swimming
with a calf in infant position (means ± SD: 0.316 ±
0.0161; this study), mothers swimming with a calf in
echelon position (0.310 ± 0.00571; calculated using
unpubl. data from Noren 2008), and mothers swimming alone (0.341 ± 0.005; this study) all fell within
the range where efficiency is considered to be maximal (0.25 to 0.35; Triantafyllou et al. 1993). In addition, the Strouhal numbers calculated in this study
were in agreement with values determined previously for adult dolphins swimming alone (0.32 and
0.30; Triantafyllou et al. 1993). This implies that even
though dolphins swimming with a calf in formation
have an altered gait and reduced swim performance,
efficiency remains optimized.
Dolphins interacting with ETP tuna fishery
Diminished performance of dolphins swimming in
formation with their calf could have important consequences for dolphins that interact with the yellowfin
tuna fishery in the ETP. Yellowfin tuna are frequently
found swimming under schools of spotted or spinner
dolphins. For the past 5½ decades this fishery has
chased and encircled dolphins in purse-seines to
capture the associated tuna (see NRC 1992 for a
review of these fishing techniques). Fishery interactions are prolonged; chase and release may last for
several hours during which dolphins elevate routine
speeds to chase and burst speeds of 2 to 4 m s−1 and
5 to 8 m s−1, respectively (Au & Perryman 1982, Au et
al. 1988, Chivers & Scott 2002). Although the swim
performance of dolphin mothers that interact with
this fishery has yet to be quantified, the average
speed (2.1 m s−1) of adult spotted dolphins in the ETP
(Scott & Chivers 2009) is similar to the routine speed
(2.1 m s−1; Williams et al. 1993) of adult bottlenose
dolphins. This makes the bottlenose dolphin a viable
model for predicting outcomes for dolphins that interact with the tuna purse-seine fishery.
Our experimental approach likely captured the
swimming performance of wild dolphins. Average
swim speeds of satellite monitored bottlenose dolphins reached 2.4 m s−1 (rate of travel calculated from
Noren: Motherhood alters swimming gait and performance
straight-line distance between 2 sampled locations;
see Klatsky et al. 2007 for review), and falls within
the range of speeds measured for the dolphins in this
study (see Fig. 2) and other studies on dolphin
mother swimming kinematics and performance
(Noren 2008, Noren et al. 2011). Therefore, the data
compiled from dolphins in human care were utilized
to formulate predictions for wild dolphins. Maximum
swim performance of bottlenose dolphin mothers
trained for speed swimming was diminished when
accompanied by a calf in infant (2.98 m s−1; present
study) and echelon (4.39 m s−1; Noren 2008) position
compared to periods of solitary swimming (6.32 m s−1;
present study). The maximum swim speed (3.54 m
s−1) of 0−2 wk pre-parturition near-term pregnant
dolphins was also diminished (Noren et al. 2011). The
extra drag associated with formation locomotion
(Weihs 2004) and pregnancy (Noren et al. 2011)
reduces swim performance during motherhood.
Thus, dolphin mothers in the ETP may be unable to
achieve the burst speeds required to maintain proximity with their group during fishery interactions.
Dolphin mothers that are left behind during the
chase may attempt to reunite with their group after
the fishery interaction is terminated. However, unlike the stealthy, short duration chases associated
with natural predators like sharks, tuna purse-seine
chases are noisy and long in duration, including
20 min of chase and a 100 min escape response after
being released from the net (Myrick & Perkins 1995).
If wild dolphin mothers are only capable of achieving
the maximum swim speeds exhibited by the trained
dolphins in the kinematic studies, then mothers
with a calf in echelon position, mothers with a calf
261
in infant position, and near-term (0−2 wk preparturition) pregnant females, will be separated from
the group by 0.73, 2.42, and 1.75 km, respectively, at
the end of a 20 min 5 m s−1 chase (Fig. 3). These
groups will be separated by an additional 3.66, 12.12,
and 8.76 km, respectively, after 100 min of escape
behavior. The noise, prolonged duration, and expansive combined chase and escape distances of
4.39 to 14.54 km separating dolphin mothers from the
group may preclude a reunion.
Alternatively, females may become separated from
their drafting calf during fishery induced chase. The
presence of a calf does not appear to deter maternal
herd-conforming behavior during the flight response
as evident in photographs of an ETP dolphin school
evading a vessel (Weihs 2004). It was hypothesized
that chase may permanently separate mother–calf
dyads (Noren & Edwards 2007). Indeed, examination
of data collected from dolphins incidentally killed
during fishing operations revealed that 74% of lactating spinner and 82% of lactating spotted dolphins
were not associated with calves (Archer et al. 2001)
and 0−1 yr old eastern Stenella longirostris orientalis
and whitebelly S. longirostris spinner dolphins were
underrepresented in the nets (Larese & Chivers
2008). The relatively slow maximum swim speeds of
solitary calves <1 yr old (Noren et al. 2006) would
preclude them from staying with the group during
chase. Because this age group is not yet weaned
(Myrick et al. 1986, Archer & Robertson 2004), the
abandoned dependent calves are not likely to survive without their mothers for nourishment, protection, and social learning, and could represent an
unobserved mortality event (Noren & Edwards 2007).
Fig. 3. Distances that dolphin mothers would be separated from the group after a hypothetical 20 min fishery induced chase at
5 m s−1. The maximum swim performance of pregnant females 0−2 wk pre-parturition and mothers accompanied by a calf in
infant or echelon position precludes them from maintaining proximity with the pod. This figure was constructed using the
Stenella longirostris (spinner dolphin), powerboat, and purse seine images by Tracey Saxby, IAN Image Library (http://ian.
umces.edu/imagelibrary/)
Mar Ecol Prog Ser 482: 255–263, 2013
262
Overall, there has been a decrease in the propor- ➤ Archer F, Gerrodette T, Dizon A, Abella K, Southern S
(2001) Unobserved kill of nursing dolphin calves in a
tion of eastern spinner and northeastern pantropical
tuna purse-seine fishery. Mar Mamm Sci 17:540−554
spotted Stenella attenuata attenuata dolphin females
Archer F, Gerrodette T, Chivers S, Jackson A (2004) Annual
observed with calves, which was attributed to a
estimates of the unobserved incidental kill of pantropical
spotted dolphin (Stenella attenuata attenuata) calves in
decrease in birth rate or calf survival (Cramer et al.
the tuna purse-seine fishery in the eastern tropical
2008). If near-term pregnant dolphins are separated
Pacific. Fish Bull 102:233−244
from the group during fishery interactions and are
Au D, Perryman W (1982) Movement and speed of dolphin
unable to reunite with their group (or any other
schools responding to an approaching ship. Fish Bull 80:
groups in the vicinity), then the birth rate for these
371−379
Au DW, Scott MD, Perryman WL (1988) Leap-swim behavior
populations will be lowered. Meanwhile, if dependof ‘porpoising’ dolphins. Cetus 8:7−10
ent calves are separated during fishery induced
Baudinette RV, Biewener AA (1998) Young wallabies get a
➤
chase and subsequently die, then the calf survival
free ride. Nature 395:653−654
rate for these populations will be decreased. These
Carrier DR (1996) Ontogenetic limits on locomotor performance. Phys Z 69:467−488
events are likely to contribute to the non-recovery
Chivers
SJ, Scott MD (2002) Tagging and tracking of
observed for dolphin populations that interact with
Stenella spp. during the 2001 chase encirclement stress
the tuna purse-seine fishery in the ETP.
studies cruise. National Marine Fisheries Service Sci-
SUMMARY
➤
This study provides further empirical evidence of
consequences for dolphin mothers ‘carrying’ an ➤
infant. Regardless of a calf’s positioning alongside its
mother, the drafting calf alters the mother’s swimming performance. This may make dolphin mothers
vulnerable to separation from the group during interactions with tuna-purse seine fisheries in the ETP.
Even in the absence of fishery interactions, ‘carrying’
an infant in an aquatic environment is associated
with maternal costs, and this behavior could affect
maternal energy budgets, foraging efficiency, and ➤
predator evasion.
➤
Acknowledgements. I thank Dolphin Quest, especially
J. Sweeney and R. Stone, for providing dolphins and partial
funding for this study. This project was only possible with
additional financial support from the Protected Resources
Division at Southwest Fisheries Science Center. I also thank
the staff at Dolphin Quest Hawaii (particularly C. Buczyna)
for assistance during data collection, S. Chivers and E. Edwards for insightful discussions about tuna purse-seine fisheries and comments on previous versions of this manuscript,
P. Raimondi for invaluable assistance with statistical analyses, J. Redfern for assistance with data management, E. Ryan
for data entry, and T. Williams for use of her Peak Motus
system.
➤
➤
➤
➤
LITERATURE CITED
➤ Altmann J, Samuels A (1992) Costs of maternal care: infant- ➤
carrying baboons. Behav Ecol Sociobiol 29:391−398
➤ Archer F, Robertson KM (2004) Age and length at weaning
and development of prey preferences of pantropical
spotted dolphins, Stenella attenuata, from the eastern
tropical Pacific. Mar Mamm Sci 20:232−245
➤
ence Center Administrative Report LJ-02-33, SWFSC, La
Jolla, CA
Cramer KL, Perryman WL, Gerrodette T (2008) Declines in
reproductive output in two dolphin populations depleted
by the yellowfin tuna purse-seine fishery. Mar Ecol Prog
Ser 369:273−285
Doran DM (1992) The ontogeny of chimpanzee and pygmy
chimpanzee locomotor behavior: a case study of paedomorphism and its behavorial correlates. J Hum Evol 23:
139−158
Fish FE (1993) Power output and propulsive efficiency of
swimming bottlenose dolphins (Tursiops truncatus).
J Exp Biol 185:179−193
Fish FE (1998) Comparative kinematics and hydrodynamics
of odontocete cetaceans: morphological and ecological
correlates with swimming performance. J Exp Biol 201:
2867−2877
Fish FE, Hui CA (1991) Dolphin swimming — a review.
Mammal Rev 21:181−195
Fish FE, Peacock JE, Rohr JJ (2003) Stabilization mechanism
in swimming odontocete cetaceans by phased movements. Mar Mamm Sci 19:515−528
Gerrodette T, Forcada J (2005) Non-recovery of two spotted
and spinner dolphin populations in the eastern tropical
Pacific Ocean. Mar Ecol Prog Ser 291:1−21
Gibson QA, Mann J (2008) Early social development in
wild bottlenose dolphins: sex differences, individual
variation and maternal influence. Anim Behav 76:
375−387
Gubbins C, McCowan B, Lynn SK, Hooper S, Reiss D (1999)
mother–infant spatial relations in captive bottlenose dolphins, Tursiops truncatus. Mar Mamm Sci 15:751−765
Kelly HR (1959) A two body problem in the echelon swimming of porpoise. Naval Ordinance Test Station Technical Note 40606-1.
Klatsky LJ, Wells RS, Sweeney JC (2007) Offshore bottlenose dolphins (Tursiops truncatus): movement and dive
behavior near the Bermuda Pedestal. J Mammal 88:
59−66
Kooyman GL, Ponganis PJ (1998) The physiological basis for
diving at depth: birds and mammals. Annu Rev Physiol
60:19−32
Kramer PA (1998) The costs of human locomotion: maternal
investment in child transport. Am J Phys Anthropol 107:
71−85
Noren: Motherhood alters swimming gait and performance
263
➤ Krasnova VV, Bel’kovick VM, Chernetsky AD (2006)
tuna industry. National Academy Press, Washington, DC
mother–infant spatial relations in wild beluga (Delphinapterus leucas) during postnatal development under
natural conditions. Biol Bull 33:53−58
Lang TG (1966) Hydrodynamic analysis of cetacean performance. In: Norris KS (ed) Whales, dolphins, and porpoises. University of California Press, Berkeley, CA, p 410−432
Larese JP, Chivers SJ (2008) Age estimates for female eastern and whitebelly spinner dolphins (Stenella longirostris) incidentally killed in the eastern tropical Pacific
tuna purse-seine fishery from 1973–82. J Cetacean Res
Manag 10:169−177
Lighthill MJ (1969) Hydrodynamics of aquatic animal
propulsion. Annu Rev Fluid Mech 1:413−446
Mann J, Smuts B (1999) Behavioral development in wild
bottlenose dolphin newborns (Tursiops sp.). Behaviour
136:529−566
McBride AF, Kritzler H (1951) Observations on pregnancy,
parturition, and post-natal behavior in the bottlenose
dolphin. J Mammal 32:251−266
Myrick AC, Perkins PC (1995) Adrenocortical color darkness
and correlates as indicators of continuous acute premortem stress in chased and purse-seine captured male
dolphins. Pathophysiology 2:191−204
Myrick AC Jr, Hohn AA, Barlow J, Sloan PA (1986) Reproductive biology of female spotted dolphins, Stenella
attenuata, from the eastern tropical Pacific. Fish Bull 84:
247−259
Noren SR (2008) Infant carrying behavior in dolphins: costly
parental care in an aquatic environment. Funct Ecol 22:
284−288
Noren SR, Edwards EF (2007) Physiological and behavioral
development in dolphin calves: Implications for calf
separation and mortality due to tuna purse-seine sets.
Mar Mamm Sci 23:15−29
Noren SR, Edwards EF (2011) Infant position in mother–calf
dolphin pairs: a social interaction with hydrodynamic
benefits. Mar Ecol Prog Ser 424:229−236
Noren SR, Biedenbach G, Edwards EF (2006) The ontogeny
of swim performance and mechanics in bottlenose dolphins (Tursiops truncatus). J Exp Biol 209:4724−4731
Noren SR, Biedenbach G, Redfern JV, Edwards EF (2008)
Hitching a ride: the formation locomotion strategy of dolphin calves. Funct Ecol 22:278−283
Noren SR, Redfern JV, Edwards EF (2011) Pregnancy is a
drag: hydrodynamics, kinematics, and performance in
pre- and post-parturition bottlenose dolphins (Tursiops
truncatus). J Exp Biol 214:4151−4159
Norris KS, Prescott JH (1961) Observations on Pacific cetaceans of Californian and Mexican waters. University of
California Publications in Zoology, Vol 63, p 91−402
NRC (National Research Council) (1992) Dolphins and the
➤ Ross C (2001) Park or ride? Evolution of infant carrying in
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
Editorial responsibility: Peter Corkeron,
Woods Hole, Massachusetts, USA
primates. Int J Primatol 22:749−771
➤ Schradin C, Anzenberger G (2001) Costs of infant carrying
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
in common marmosets, Callithrix jacchus: an experimental analysis. Anim Behav 62:289−295
Scott MC, Chivers SJ (2009) Movements and diving behavior of pelagic spotted dolphins. Mar Mamm Sci 25:
137−160
Skrovan RC, Williams TM, Berry PS, Moore PW (1999) The
diving physiology of bottlenose dolphins (Tursiops truncatus) II. Biomechanics and changes in buoyancy at
depth. J Exp Biol 202:2749−2761
Taber S, Thomas P (1982) Calf development and mother–
calf spatial relationships in southern right whales. Anim
Behav 30:1072−1083
Tavolga MC, Essapian FS (1957) The behavior of the bottlenosed dolphin (Tursiops truncatus): mating, pregnancy,
parturition and mother–infant behavior. Zoologica 42:
11−31
Triantafyllou GS, Triantafyllou MS, Grosenbaugh MA
(1993) Optimal thrust development in oscillating foils
with application to fish propulsion. J Fluids Structures 7:
205−224
Wade PR, Watters GM, Gerrodette T, Reilly SB (2007)
Depletion of spotted and spinner dolphins in the eastern
tropical Pacific: modeling hypotheses for their lack of
recovery. Mar Ecol Prog Ser 343:1−14
Webb P (1975) Hydrodynamics and energetics of fish
propulsion. Bull Fish Res Board Can 190:1−158
Weibel ER, Taylor CR, Hoppeler H, Karas RH (1987) Adaptive variation in the mammalian respiratory system in
relation to energetic demand: I. Introduction to problem
and strategy. Resp Physiol 69:1−6
Weihs D (2004) The hydrodynamics of dolphin drafting.
J Biol 3(2):8, doi:10.1186/jbiol2
Weihs D, Ringel M, Victor M (2006) Aerodynamic interactions between adjacent slender bodies. AIAA J 44:
481−484
Wells JP, Turnquist JE (2001) Ontogeny of locomotion in
rhesus macaques (Macaca mulatta): II. Postural and locomotor behavior and habitat use in a free-ranging colony.
Am J Phys Anthropol 115:80−94
Williams TM, Friedl WA, Haun JE (1993) The physiology of
bottlenose dolphins (Tursiops truncatus): heart rate,
metabolic rate and plasma lactate concentration during
exercise. J Exp Biol 179:31−46
Xian Y, Wang K, Jiang W, Zheng B, Wang D (2012) The
development of spatial position between mother and calf
of Yangtze finless porpoises (Neophocaena asiaeorientalis asiaeorientalis) maintained in captive and seminatural environments. Aquat Mamm 38:127−135
Submitted: June 26, 2012; Accepted: January 24, 2013
Proofs received from author(s): April 23, 2013