Evidence of Teaching in Atlantic Spotted Dolphins (Stenella Frontalis) by Mother Dolphins Foraging in The Presence of Their Calves

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ORI GI NAL PAPER

Evidence of teaching in atlantic spotted dolphins


(Stenella frontalis) by mother dolphins foraging in the presence
of their calves
Courtney E. Bender Denise L. Herzing
David F. Bjorklund
Received: 10 January 2008 / Revised: 18 March 2008 / Accepted: 5 June 2008 / Published online: 29 July 2008
Springer-Verlag 2008
Abstract Teaching is a powerful form of social learning,
but there is little systematic evidence that it occurs in
species other than humans. Using long-term video archives
the foraging behaviors by mother Atlantic spotted dolphins
(Stenella frontalis) were observed when their calves were
present and when their calves were not present, including
in the presence of non-calf conspecics. The nine mothers
we observed chased prey signicantly longer and made
signicantly more referential body-orienting movements in
the direction of the prey during foraging events when their
calves were present than when their calves were not pres-
ent, regardless of whether they were foraging alone or with
another non-calf dolphin. Although further research into
the potential consequences for the na ve calves is still
warranted, these data based on the maternal foraging
behavior are suggestive of teaching as a social-learning
mechanism in nonhuman animals.
Keywords Teaching Dolphins Social learning
Foraging
Introduction
Although one of the most potent forms of social learning in
humans, there has been little evidence to suggest that
teaching occurs in nonhuman animals. Some theorists have
suggested that this may be because teaching requires
advanced social-cognitive skills, including the ability to
take the perspective of another and theory of mind, the
ability to appreciate that an individuals behavior is based
on its knowledge and its desires (Boesch and Tomasello
1998; Tomasello 1996, 2000; Tomasello et al. 1993). For
example, previous examples of suggested teaching behav-
ior by meerkats, cheetahs, and domestic cats seem to
benet the prey-handling abilities of the young, but do not
require the use of higher cognitive mechanisms (Thornton
and McAuliffe 2006; Caro and Hauser 1992). However,
Caro and Hauser (1992) provided a denition of teaching
that may be more inclusive for nonhuman animals, dening
it as, An individual actor A can be said to teach if it
modies its behavior only in the presence of a naive
observer, B, at some cost or at least without obtaining an
immediate benet for itself. As behavior thereby encour-
ages or punishes Bs behavior, or provides B with
experience, or sets an example for B. As a result, B
acquires knowledge or learns a skill earlier in life or more
rapidly or efciently than it might otherwise do, or that it
would not learn at all (p. 153).
Previous studies that suggested teaching in primates and
cetaceans, although promising, lacked systematic mea-
surement of the behavior. Probably the best evidence of
teaching in nonhuman primates to date is Boeschs studies
of mother chimpanzees (Pan troglodytes) in the Tai
National Park of the Ivory Coast (Boesch 1991, 1993;
Greeneld et al. 2000). Boesch suggested that the
chimpanzee mothers facilitated the development of their
Electronic supplementary material The online version of this
article (doi:10.1007/s10071-008-0169-9) contains supplementary
material, which is available to authorized users.
C. E. Bender (&) D. F. Bjorklund
Department of Biological Sciences, Florida Atlantic University,
777 Glades Road, Boca Raton, FL 33431-0991, USA
e-mail: courtbender@yahoo.com; cgreen21@fau.edu
D. L. Herzing
Department of Biological Sciences, Wild Dolphin Project,
Florida Atlantic University, 777 Glades Road, Boca Raton,
FL 33431-0991, USA
1 3
Anim Cogn (2009) 12:4353
DOI 10.1007/s10071-008-0169-9
offsprings nut-cracking skills by means of stimulation,
facilitation, and active teaching. Nut cracking is observed
in only a few populations of chimpanzees, despite the
availability of nuts and appropriate tools (i.e., rocks
appropriate for use as anvils and hammers), qualifying, by
some denitions, as an example of culturally-transmitted
behavior (Whiten 2005; Whiten et al. 1999). The inter-
pretation of such episodes as teaching has been
questioned, however (Bering 2001; Bering and Povinelli
2003). Moreover, such episodes are rarely observed, sug-
gesting that direct teaching is not a common form of
cultural transmission in chimpanzees.
Although evidence of social learning is easier to docu-
ment in these terrestrial great apes than it is in marine
mammals, nongenetic transmission of behavior across
generations has also been observed for cetaceans (Kruetzen
et al. 2005; Rendell and Whitehead 2001), suggesting that,
like the great apes, these large-brained, slow-developing,
and socially complex species (Bjorklund and Bering 2003)
have evolved powerful social-learning mechanisms.
Similar to research with great apes, little is known about
the actual mechanism of transmission across generations in
cetaceans. Herzing (2005) described some potential sce-
narios and mechanisms observed for a group of free-ranging
Atlantic spotted dolphins (Stenella frontalis), including
implications of vertical, horizontal, and oblique directions
of transmission of information during various behavioral
contexts. Recently, Spininelli et al. (2006) described prey-
transfer between mother and calf in the marine tucuxi dol-
phin (Sotalia uvialis). Observations such as these suggest
that the mother-calf relationship may be one of the most
important sources of information in the young calfs life.
There is some evidence of presumed maternal teaching
behavior associated with stranding behavior as a foraging
specialization used by part of the population of killer whales
(Orcinus orca) in the Crozet Islands and off Punta Norte,
Argentina to capture seal pups onpinniped breeding beaches.
Adult females demonstrated a modication of their strand
foraging behavior in the presence of na ve juvenile observers
(presumably their calves), suggesting that teaching may be
involved in the development and the rate of success of calves
in mastering these behaviors (Guinet and Bouvier 1995).
This comparison between purported teaching in chimpan-
zees and killer whales is interesting because any
commonalities would have been derived through convergent
evolution, as the last common ancestor of primates with
cetaceans is estimated to have lived over 90 million years ago
(Marino et al. 2007). However, despite the multitude of
observations of chimpanzees and killer whales in the wild,
incidences of motherinfant teaching are scarce and
anecdotal in nature.
Foraging behavior is a likely candidate for social
learning among wild dolphins, particularly between mother
and calf. The mother/calf relationship is the strongest
association that Atlantic spotted dolphins have in their
lifetimes (Herzing and Brunnick 1997). The prolonged
developmental period provides both ample time and situ-
ational possibilities for a calf to learn foraging strategies
from its mother (Herzing 1996). The majority of daytime
feeding behavior of Atlantic spotted dolphins is benthic
foraging, in which dolphins use echolocation to locate sh
in the sandy bottom and then dig prey items out of the sand
in order to catch and eat them (Herzing 1996).
Much of what we know about marine mammal social
learning comes from research with captive animals due, in
part, to the difculty of studying such phenomena in the
wild. Attempts to assess teaching among captive animals
often involve contrived situations, which may affect the
animals success or failure (Kuczaj et al. 2005). Studies
that assess social learning in wild populations of marine
mammals are needed to validate and supplement the nd-
ings from captive animals and to better understand the
spontaneous occurrence of social learning in natural
settings.
In the present study, using video archives from a long-
term naturalistic study, we investigated social learning and
possible teaching behavior by the Atlantic spotted dolphin.
Unlike most previous research examining social learning in
nonhuman mammals in which the focus is on the observer/
learner (e.g., Bjorklund et al. 2002; Guinet and Bouvier
1995; Herman 2002; Tomasello et al. 1993), the present
study shifted the focus from the observer (in our case, the
calf observing the foraging behavior) to the model (the
mother performing the foraging behavior) to explore the
possibility of teaching behavior. We examined the foraging
behavior by mother dolphins when foraging in the presence
of their young (less than 3-year-old) calves in comparison
to when the calves were not present. Additionally, com-
parisons were then made between mothers foraging alone
and when they were foraging with non-calf conspecics.
Should the mothers alter their foraging behavior in the
presence of their young, it would be suggestive of teaching
and provide a possible mechanism for cultural transmission
within this dolphin species.
Methods and analysis
Natural history
This study was performed using underwater video record-
ings of the Atlantic spotted dolphin collected by the Wild
Dolphin Project (Herzing 1997) in the study area north of
Grand Bahama Island, Bahamas during summer eld sea-
sons between 1991 and 2004 (Fig. 1). Unlike many other
marine mammal habitats, this area is optimal for behavioral
44 Anim Cogn (2009) 12:4353
1 3
observation with clear, warm waters that allow for excel-
lent visibility up to 90 ft and long observational periods
(Herzing 1996). The dolphins in this study have been
observed since 1985, and include over 200 dolphins that
have been individually recognized and sexed. Atlantic
spotted dolphins can be categorized into four age classes,
based on the pigmentation of the individual (Herzing
1996). The number of spots on the individual is correlated
with age, with a newborn having no spots. Although most
individuals in the population are tracked from birth, this
allows for approximating the individuals age when it is not
known from previous sightings. Calves in the sampled
foraging events 3-years-old or younger were still observed
to be nursing during the encounter year. The year of the
calfs birth was determined from previous sightings of the
pregnant female followed by a sighting with a closely
associated calf or a sighting of the mother with a suckling
calf (Herzing 1997).
Apparatus and procedure
Video was recorded using various underwater cameras
(Sony CCDV9 8-mm, Yashica KXV Hi8-mm with attached
Labcore 76 hydrophone, Sony DCR-SC100 NTSC, or Sony
DCR-PC110 NTSC Digital Video). Underwater video
sequences were analyzed using focal follow (of the mother
with and without the calf) as a sampling rule and contin-
uous sampling as a recording rule. Video sequences from
the long-term video archives from the Wild Dolphin Pro-
ject

between 1991 and 2004 were assessed for the


presence of benthic foraging events by individual mothers,
either with or without their calves present, based on a
behavioral ethogram designed to measure the individual
benthic foraging behavior of the mother dolphins (see
Fig. 2). Each benthic sh catch was broken down into a
series of behaviors that made up a typical foraging event.
For the purpose of this study, a foraging event was
dened as the series of behaviors performed by the dolphin
in order to catch the prey animal. For benthic feeding, the
series of events was as follows:
scanning ! rooting ! chase ! ingestion
Scanning is observed when the dolphin moves its head
horizontally or vertically repeatedly while performing a
directional swim, and usually occurs near the sea oor and
can be followed by a dig or sh catch (Miles and Herzing
2003). Rooting or digging is observed when the dolphin
inserts the rostrum into the sea oor or sandy bottom to dig
the prey out of the substrate in the attempt to capture the
prey. Chasing is observed as swimming in the direction of
the prey object, as in pursuit of the prey. For our purposes,
ingestion was dened as the food going into mouth and
never being seen again. The categories of foraging
behaviors measured were chase latency and number of
body-orienting movements during pursuit. Chase latency,
the length of time the prey was pursued, was operationally
dened as the period of time when the sh appeared out of
the sand (was rooted out) until the time of ingestion by the
dolphin, or the dolphin no longer pursued prey (lost interest
in prey). Body-orienting movements were measured to
examine the dolphins attention to the prey object. A body-
orienting movement was measured in foraging events as a
movement of the body reorienting in direction of prey
object, often seen during pursuit of prey, from the time the
prey was rooted out of the sand. Body-orienting
movements were particularly interesting as they appeared
to be exaggerated movements in the direction of the prey,
which may be an attention-directed referential behavior
similar to the spontaneous pointing observed by dolphins
during experiments in captivity (Xitco et al. 2001).
Figure 2 is a visual ethogram describing the sequence of
the benthic foraging behavior (Miles and Herzing 2003).
Fig. 1 Map of study area for the wild dolphin project underwater
video recordings collected over sandbanks north of Grand Bahama
Island Study population of Atlantic spotted dolphins ranges over an
area of approximately 500 km
2
Anim Cogn (2009) 12:4353 45
1 3
The segments from the video archives in which mothers
were observed engaged in foraging behavior with or
without their calves were then viewed and then examined
for further criteria. Thirty-eight video segments were used
in the study based on the selection criteria: fourteen video
segments of mothers foraging with their calves present and
24 video segments of those mothers foraging without their
calves present. Videos were selected based on the presence
of a target female performing an individual foraging event,
as well as on the following designated video acceptance
criteria: (a) the individuals were identiable; (b) it was
possible to identify the beginning and end of the chase
sequence; (c) the prey was visible, or if the prey was not
completely visible, it was possible to identify the position
of the prey based on the behavior of the dolphin; (d) if the
calf was present, the calf was in a nearby position (within a
proximity of two body lengths) from which it was capable
of observing its mother; and (e) if the calf was present, it
was possible to identify the position of the calf relative to
the mother during the foraging event. The position of the
calf relative to the mother was recorded as Infant, Head-
under-head, Echelon, Observation, or Other, with com-
ments where necessary, as depicted in Fig. 2.
The mothers foraging behaviors were then individually
measured for the variables of chase latency and body-ori-
enting movements, both when foraging alone (or with other
juvenile or adult dolphins) and when foraging in the
presence of their calves. Other variables, such as types of
play involved in that foraging encounter, position of calf
relative to the mother, directionality of the calf, age of the
mothers and their calves, whether the mother eventually ate
the prey; the prey species, when identiable, were also
recorded for each foraging event.
Participants
The foraging behaviors of nine mother dolphins were
recorded both with (n = 14) and without (n = 22) their
calves present. Ten different calves were observed with the
nine mothers in the 14 foraging events, with one mother
observed during separate events with two different calves.
Calves ranged in age from neonate to 3 years old. All
calves were observed to be nursing within the same eld
season as the foraging event. Ages of the mothers were
known, or were estimated based on their age class. It is
important to note that some foraging events without calves
present (10 of the 22) occurred while the target female was
still a juvenile (prior to sexual maturity); however, during
those events, the mothers to be were already past the age
of weaning and were independently foraging. The mini-
mum age of any female during foraging events over the
12-year period was 10 years for mothers foraging with
their calves and 4 years for mothers-to-be foraging without
calves present. Of the observations without calves present,
four of the females were observed foraging as juveniles,
prior to becoming mothers. Of the nine mothers observed,
foraging events were observed for one female both when
she was a calf with her mother, and later as a mother
herself with her own calf.
The video segments of the foraging events were short-
ened to within 1 min of the beginning and end of the
foraging event and labeled with the foraging event number
and the individuals involved. Segments were then watched
by the rst author and two independent observers to mea-
sure the desired behaviors. Of the 38 total foraging events
measured, 32 were measured by the rst author and two
independent observers; the other six were measured by the
rst author and only one independent observer. For the
measurement of chase latencies of foraging events, there
was signicant correlation between the author and the rst
independent observer, r
36
= 1.0, P\0.001, between the
author and the second independent observer, r
30
= 0.999,
P\0.001, and between the rst and second observer,
r
30
= 0.998, P\0.001. For the measurement of number of
body-orienting movements, there was signicant correla-
tion between the author and the rst independent observer,
Positions of Calf Relative to Mother
Echelon Position
Observation Position
Infant Position Head-under-head
Position
Benthic Foraging Event
Sequence of Behaviors for
Individual Scanning Dig/Root Chase
Fig. 2 Visual ethogram of
select foraging behavioral
events (Miles and Herzing
2003). The visual ethogram
includes the possible positions
in which calves were observed
during foraging events in
relation to their mother and the
sequence of behaviors for a
benthic foraging event
46 Anim Cogn (2009) 12:4353
1 3
r
36
= 1.0, P\0.001, between the author and the second
independent observer, r
30
= 0.988, P\0.001, and
between the rst and second observer, r
30
= 0.988,
P\0.001.
The videos were watched and timed using Windows
Media Player version 10 on a Hewlett Packard laptop
computer and a projector in order to enlarge the viewing
area. Due to the restrictions of the media software used for
editing and playing the video, a second or less rule was
instituted for measurement of latencies in which the
latencies appearing to be less than 1 s were rounded up to
1 s in duration.
Results
Chase latencies
Mean chase latencies for each of the nine mothers, both
when foraging with and without their calves, is presented in
Table 1. The mothers chased the prey signicantly longer
when their calves were present (M = 22.24 s, SD = 9.36)
than when their calves were not present (M = 2.74 s,
SD = 1.47), t
8
= 6.57, P\0.001, d = 1.14. Mean chase
latencies were longer when foraging with their calves than
without their calves for each of the nine mothers (Fig. 3).
Body-orienting movements
Mean number of body-orienting movements for each of the
nine mothers, both when foraging with and without their
calves, is presented in Table 1. The mothers made signif-
icantly more body-orienting movements when their calves
were present (M = 1.26, SD = 1.04) than when their
calves were not present (M = 0.28, SD = 0.31), t
8
= 2.46,
P = 0.04, d = 2.31. Six of nine mothers made more body-
orienting movements when foraging in the presence of
their calves than when not foraging with their calves.
Cross-generational comparisons
Two consecutive generations of the mother/calf pairs in the
study showed the same altered foraging behavior. In the
rst generation, one mother, Nippy, and her calf, Nassau,
demonstrated the presumed teaching behavior. In the sec-
ond generation, Nassau, now a mother, showed the same
altered foraging behavior as her mother with her calf,
Neptune.
Foraging with non-calf individuals
Of the foraging events without calves, three mothers were
observed foraging both alone and with other individuals
that were not calves, at least juveniles or older. The chase
latencies and body-orienting movements for these mothers
were compared for the two conditions (alone and with non-
calf individuals). There were too few subjects (n = 3) to
perform a statistical test; however, the chase latencies of
these three mothers foraging alone (M = 1.33, SD = 0.58)
were comparable to the chase latencies of these same
mothers foraging with non-calf individuals (M = 3.44,
SD = 1.50), and both were much lower than the chase
Table 1 Mean chase latency of mothers with and without calf
Mother Little Gash Mugsy Nassau Nippy PR1 PR2 Rosemole Trimy Uno Mean SD
Mean chase latency
without calf (n)
5.6 (5) 2.25 (4) 2.00 (3) 2.00 (1) 2.17 (2) 4.00 (1) 1.67 (3) 4.00 (4) 1.00 (1) 2.74 1.47
Mean chase latency
with calf (n)
38.33 (1) 23.00 (2) 16.33 (2) 36.00 (1) 24.33 (3) 19.67 (1) 16.50 (2) 12.00 (1) 14.00 (1) 22.24 9.36
Mean number of BOM
without calf (n)
0.80 (5) 0.00 (4) 0.33 (3) 0.67 (1) 0.50 (2) 0.00 (1) 0.00 (3) 0.25 (4) 0.00 (1) 0.28 0.31
Mean number of BOM
with calf (n)
0.00 (1) 2.50 (2) 1.50 (2) 0.00 (1) 2.33 (3) 2.00 (1) 0.00 (2) 2.00 (1) 1.00 (1) 1.26 1.04
Bold indicates mothers who performed signicantly more body-orienting movements in the presence of their calves. Chase latencies were
signicantly longer for all nine mothers
38.33
23.00
16.33
36.00
24.33
19.67
16.50
12.00
14.00
5.60
2.25 2.00 2.00 2.17
4.00
1.67
4.00
1.00
0.00
5.00
10.00
15.00
20.00
25.00
30.00
35.00
40.00
45.00
Mother
Chase Latency of Mothers
Mothers Chasing
With Calves
Mothers Chasing
Without Calves
Fig. 3 Mean chase latencies of mothers foraging with and without
their calves present
Anim Cogn (2009) 12:4353 47
1 3
latencies of those mothers foraging with their calves
present (M = 17.56, SD = 6.26). Additionally, the number
of body-orienting movements of these three mothers for-
aging alone (M = 0.17, SD = 0.29) was comparable to the
number of body-orienting movements when they were
foraging with non-calf individuals (M = 0.33, SD = 0.58),
and both were less than the number of body-orienting
movements of those mothers foraging with their calves
present (M = 1.94, SD = 0.42).
Additional analyses
The differences observed for chase latencies and number of
body-orienting movements could not be attributed to prey
type, as there were no signicant differences in the foraging
behaviors between prey species. Prey species were identi-
ed for 14 observations. When foraging with calves present,
mothers were observed foraging for Snakesh (family
Synodontidae), n = 5, ounder (family Bothidae), n = 2,
and razorsh (family Clinidae), n = 1. The mean chase
latencies, M
Snakesh
= 19.0 (SD = 11.03), M
Flounder
= 20.5
(SD = 14.85), M
Razorsh
= 25.0 (SD = 0.0), and number
of body-orienting movements, M
Snakesh
= 0.6 (SD =
0.89), M
Flounder
= 25.0 (SD = 2.12), M
Razorsh
= 3.0
(SD = 0.0), were comparable for all three species of prey
when foraging with calves present. Both snakesh, n = 9,
and ounder, n = 4, were observed as prey types when the
females were observed foraging without calves present. The
mean chase latencies, M
Snakesh
= 2.22 (SD = 1.09),
M
Flounder
= 3.83 (SD = 3.57), and number of body-orient-
ing movements, M
Snakesh
= 0.5 (SD = 0.76), M
Flounder
=
0.5 (SD = 0.58), were comparable for both species when
foraging without calves present, and both were lower than
when foraging with calves present.
Additionally, individual foraging events of dolphins not
included in the study observed foraging for either snakesh
or ounder were collected and analyzed. Ten foraging
events each for catches of snakesh and ounder using
both dolphins in the present study and dolphins not used in
the study were randomly selected, and their corresponding
chase latencies and number of body-orienting movements
were compared between the two types of prey using an
independent samples Students t-test. There were no sig-
nicant differences found between the two types of prey for
either chase latencies, (M
ounder
= 4.60, SD
ounder
= 3.86,
M
snakesh
= 2.80, SD
snakesh
= 1.62) t
18
= -1.36,
P = 0.19, or number of body orienting movements for
dolphins foraging without calves present, (M
ounder
= 0.50,
SD
ounder
= 0.71, M
snakesh
= 0.37, SD
snakesh
= 0.48)
t
18
= -0.49, P = 0.63. This supports the conclusion that
the observed differences in this study for mothers foraging
with calves present would not likely be due to the type of
prey, as chase latencies and the number of body-orienting
movements do not normally vary signicantly between
snakesh and ounder, the two main types of prey observed
being caught by mother dolphins in this study.
To assess possible effects of age of calf and age of
mother on the dependent measures, correlations with each
dependent measure were computed separately with the age
of the calf and the age of the mother for the foraging events
when the calf was present. Correlations between age of the
calf and chase latency, r
13
= 0.37, P = 0.10, and number
of body-orienting movements, r
13
= -0.30, P = 0.15,
were both nonsignicant. Correlations between mothers
age and number of body-orienting movements were sig-
nicant, r
13
= -0.47, P = 0.046, with older mothers
making fewer body-orienting movements than younger
mothers. The correlation between mothers age and chase
latencies was not signicant, r
13
= 0.01, P = 0.48. When
comparing the foraging behaviors to the age of the mothers
when the calves were not present, correlations with both
chase latencies r
23
= -0.07, P = 0.73, and number of
body-orienting movements, r
23
= -0.12, P = 0.58, were
nonsignicant. The foraging behaviors of eight of the nine
mothers without calves were compared between those
females observed as juveniles and those observed as adults,
with three mothers being observed foraging as juveniles
and ve mothers observed foraging as adults.
1
There were
no signicant differences between chase latencies, t
(6)
= -
0.10, P = 0.92, or number of body-orienting movements,
t
(6)
= -0.12, P = 0.91, of females observed foraging
when juveniles or adults.
Additionally, of the nine mothers observed in this study,
three of the mothers, Little Gash, Mugsy, and PR2, were
observed foraging both with and without their calves
present during the same year, and each of those three
mothers being observed foraging both with and without
calves during the same eld encounter. The mean chase
latencies for these three mothers are compared in Table 2.
The chase latencies were much longer foraging with calves
than foraging alone for the mothers at the same age and
comparable to the mean chase latencies of foraging alone
for the mothers at an earlier age.
The position of the calf during the chase period was
indicated for each of the foraging events (N = 14) in which
the calf was present. Although some foraging events
involved multiple calf positions, the observation position
1
One mother, Little Gash, was observed foraging without her calf
present both as an adult and as a juvenile. When group means were
compared including Little Gash there were no signicant differences
between adults and juveniles for either chase latencies, t
(8)
= 0.05,
P = 0.96, or body-orienting movements, t
(8)
= 0.41, P = 0.69. Both
the mean chase latencies, M
A
= 3.67 and M
J
= 6.89, and mean
number of body-orienting movements, M
A
= 0.5 and M
J
= 1.0, for
Little Gash were comparable as an adult and as a juvenile.
48 Anim Cogn (2009) 12:4353
1 3
was found to be the most common, taking place in 11
(79%) of the foraging events. Head-under-head position
was present in one of the foraging events, Echelon was
present in two foraging events, and Infant position was
seen in one foraging event. Only Infant, Echelon, and
Observation positions were seen solely in an individual
foraging event, with one, one, and nine occurrences,
respectively.
For the foraging events collected in which the ingestion
by the mother was known (as seen by video or rst-hand
account), there were ve events, one event each for ve of
the nine mothers, in which the prey was not eaten. Each of
these foraging events occurred when the mothers calves
were present (36% of the total events with calves). In
addition, the calves were allowed to pursue the prey in each
of these events and were conrmed to have eaten the prey
in three of the foraging events, despite the fact that they
were still nursing and not dependent upon sh for food.
Four of the nine mothers were observed eating the prey in
seven of the fourteen events in which calves were present.
In two of the events in which calves were present it was not
known whether the prey was eaten.
Discussion
The nine mother dolphins observed in this study displayed
signicantly longer chase latencies and made signicantly
more body-orienting movements when foraging in the
presence of their calves than when foraging alone. The
chase latency data are particularly impressive. Mean chase
latencies were eight times longer for the female dolphins
when foraging with their calves (22.24 s) than without
them (2.74 s). As illustrated in Fig. 3, the distributions
were non-overlapping, with every mother having a longer
latency when foraging with her calf than when foraging
without her calf.
Although differences were not as robust for the body-
orienting movements, the overall number of body-orienting
movements was signicantly greater when the mothers
were foraging with their calves than when foraging alone,
with six of nine mothers displaying this pattern. Previous
research has shown that dolphins are capable of under-
standing the human gesture of pointing (Herman et al.
1999; Pack and Herman 2004), and of producing sponta-
neous referential gestures in articial experimental
contexts (Xitco et al. 2001). Although these body-orienting
movements were not demonstrated by all sampled mothers,
the present results may be evidence of referential gesturing
in a more ecologically valid context.
In addition to the elongated chase and presumed refer-
ential body-orienting movements in the direction of the
prey, the altered foraging behavior in the presence of the
calf appeared more exaggerated when compared to the
mothers foraging alone or with another non-calf dolphin.
Mothers seemed to toy with their prey, making it more like
play behavior and less like the typical foraging behavior of
mothers observed foraging without their calves present,
similar to descriptions of possible teaching of predatory
behavior from other species such as cats and killer whales
(Caro and Hauser 1992; Guinet and Bouvier 1995). Some
of the mothers were observed letting the prey swim away
and then digging them back out of the sand, sometimes
multiple times, after initially digging the sh out of the
sand, and also make jawing motions in the direction of the
prey. Mothers also allowed the seemingly attentive calves
to participate in the chase, and calves were observed eating
the prey in three of the events. Although 4 of the 9 mothers
were observed eating the prey in 7 of the 14 events, all of
the mothers were observed allowing the calves to partici-
pate and made little to no effort in these events to consume
the prey, only seemingly facilitating the calves experience
in chasing the prey. Despite the altered foraging behavior,
mothers were never observed losing the prey. In all events
in which ingestion of the prey was observed, either the
mother or the calf ate the prey, or the mother made no
further attempts to ingest the prey and left the prey to the
calf to chase. This altered foraging behavior can be
Table 2 Maternal age
comparison for mean chase
latency and number of body-
orienting movements
Encounter dates
by mother
Mean chase latency
with calf (n)
Mean chase latency
without calf (n)
Mean BOM
with calf
Mean BOM
without calf
Little Gash
30 May 2000 38.33 (1) 3.67 (2) 0.00 (1) 0.50 (2)
27 May 1991 4.00 (2) 1.50 (2)
Mugsy
29 August 1993 34.00 (1) 2.00 (1) 5.00 (1) 0.00
13 May 2000 4.00 (1) 0.00
11 August 2000 12.00 (1) 0.00
PR2
14 June 1994 19.67 (1) 4.00 (1) 2.00 0.00
Anim Cogn (2009) 12:4353 49
1 3
observed in the online supplemental movies S1 and S2
which exemplify the markedly different foraging behavior
of an adult female foraging alone (S1) with the foraging
behavior of a mother foraging in the presence of her calf
(S2).
There was a potential cost of the alteration of the
mothers foraging behavior in their calves presence. The
elongated chase time allowed more opportunity for prey to
escape, although this did not occur in any of the events
observed, as well as taking time away from catching
additional sh or other activities. Instead of the typical grab
and ingestion, these mothers toyed with their prey as their
calves watched, and, as mentioned above, sometimes even
avoided ingestion in these altered foraging events. Often in
teaching, the model will provide an exaggerated or elon-
gated version of the typical behavior in front of the na ve
observer, much as the mother chimpanzees observed in
Boeschs (1991) work. These exaggerated foraging
behaviors may provide a window of opportunity for the
calves to observe, and possibly learn from, the example
provided by their mothers, and thus be worthy of the extra
time and energy put forth by the mothers at a cost to
themselves in order to help ensure the success of their
offspring.
An alternative explanation for the altered foraging
behavior may be that the mothers were distracted by their
calves, resulting in longer chase latencies and exaggerated
movements to compensate for their divided attention.
However, we do not believe this to be the cause of the
altered foraging behavior for a few reasons. First, three of
the nine mothers observed in the present study demon-
strated the ability of dolphin mothers to forage without
distraction even when their calves were in the nearby
vicinity, but not directly observing the mothers. These
three mothers, Little Gash, Mugsy, and PR2, were
observed foraging both with and without their calves
present during the same eld encounter. These mothers
only altered their behavior when the calves were
observing the mother, but not during the sh catches in
which the calves were within the vicinity and not
observing. Table 2 compares the means for those events,
in which the mean chase latencies were much longer
foraging with calves than foraging alone during the same
eld encounter and comparable to the mean chase laten-
cies of foraging alone during separate eld encounters.
These data suggest that the calves being merely nearby is
not a distraction for the mothers, but instead the altered
foraging behavior only occurred when the calves were
directly observing the mothers behavior. If the calves
were a distraction for the mothers, the altered foraging
behavior should have occurred whenever the calves were
within the vicinity, regardless of whether the calves were
directly observing the mothers.
Second, Atlantic spotted dolphins participate in allo-
parenting, which permits mothers to frequently forage
separately from their calves (Herzing 1996). If the mothers
nutritional needs are being met in the absence of their calf
with the help of alloparenting, this would enable more time
and energy on the part of the mother for altered foraging
events for teaching when the calf is present. Additionally, it
would not be advantageous for the mother to forage with
the calf present solely for her nutritional purposes if there is
an alloparent available. In this study, there were potential
alloparents, juvenile or adult female dolphins, available in
all 14 of the calf-present events that would have permitted
the mothers to forage without distraction, which is often
observed in Atlantic spotted dolphins (Herzing 1996),
including the events for the previously mentioned three
mothers observed foraging with and without calves during
the same eld encounter.
Third, young dolphin calves are very precocious and the
calves in the observed foraging events appeared attentive
and interactive. Some of the evidence for the calves
attentiveness to the mothers foraging behavior was
observed through the calves positions relative to the
mothers, which was indicated during the chase period for
each of the foraging events in which the calf was present.
Although previous research (Mann and Smuts 1999) has
shown that dolphin calves in the wild, and in captivity
spend the majority of their time in infant or echelon posi-
tion until the time of weaning, calves were most commonly
found during the chase period in the observation position
relative to their mothers in which the calf was potentially
exposed to both visual and acoustic information and in
which calves appeared attentive to both the mother and the
prey
2
(Figure 2).
Additionally, the calves were allowed to pursue the prey
in ve of the foraging events and were conrmed to have
eaten the prey in three of the events, despite the fact that
they were still nursing and not dependent upon sh for
food. It is important to note that the only time when the sh
was not ingested was when the mothers were foraging with
their calves as part of their altered foraging behavior. The
prey was always consumed when foraging alone or in the
presence of a non-calf dolphin. This is potentially a costly
behavior for the mother as she is depriving herself of cal-
ories needed to nourish her still nursing calf by allowing
2
It is important to note that research in captivity (Pack and Herman
1995) has demonstrated the ability of dolphins to perceive and
recognize objects through either vision or echolocation. In addition,
their perceptions are readily shared or integrated across the senses,
regardless of which modality the dolphin originally perceived the
external stimuli. However, the sounds emitted from the dolphins were
not measured in the present study, but should be looked at in future
research in order to determine what sensory information the calf is
receiving.
50 Anim Cogn (2009) 12:4353
1 3
the prey to escape or allowing the calf to eat the prey, as
well as the energy to play with the prey rather than just
eating it quickly and efciently herself. It would be more
efcient and less costly for the mothers to have simply
caught and consumed the sh, or perhaps to have left the
calf in the care of an alloparent, as opposed to this altered
foraging behavior observed in these events.
Furthermore, the chase latencies and foraging behaviors
were drastically different with their calves present, not just
with the longer latencies but also with the presumed ref-
erential behaviors toward the prey objects and allowing the
still nursing calf to participate, which would be more
indicative of social learning. If the calves were merely a
distraction, the mothers could have either immediately
consumed the prey or disciplined the calf, as previously
observed by mothers in the population for undesirable
behaviors (Miles and Herzing 2003), rather than allowing
the calf to participate. Therefore, because the calves
appeared attentive, interacted with the prey and the mother,
and appeared to need little care during the event, they were
not likely a distraction to the mother.
Reciprocally, the mothers may have been altering their
foraging behavior because their calves were attentive, so
that a calfs attention may have stimulated the altered
maternal foraging behavior. Further analysis into the
calves behavior is warranted and may also elucidate the
exact learning mechanism at play on behalf of the calf.
For the majority of the mothers, there was a difference
in maternal age between the events observed foraging
without their calves compared to the events foraging with
their calves. It is not likely that the age differences, or
resulting level of experience would have resulted in the
observed differences in chase latencies and number of
body-orienting movements. Rather, an older or more
experienced dolphin should be expected to have quicker
chase latencies and fewer body-orienting movements due
to increased efciency, not the longer latencies and
increased number of body-orienting movements as
observed here. Additionally, of the nine mothers observed
in this study, three of the mothers, Little Gash, Mugsy, and
PR2, were observed foraging both with and without their
calves present during the same year, and each of these
three mothers were observed foraging both with and
without calves during the same eld encounter. For these
three mothers, mean chase latencies were much longer
foraging with calves than foraging alone at the same age
and comparable to the mean chase latencies of foraging
alone at an earlier age (Table 2). This suggests that there
was not a difference in foraging behavior due to difference
in age or experience, but rather due to the presence of their
calves.
There were also no signicant differences for chase
latencies or number of body-orienting movements for the
prey species observed in this study: thus the altered for-
aging behaviors were also not likely due to the difculty of
catching a specic type of prey.
The three episodes in which a target dolphin was
observed foraging with a non-calf individual, juvenile in
age or older, produced chase latencies and number of body-
orienting movements comparable to when these dolphins
foraged alone, and both substantially different from the
levels of behavior observed when these dolphins foraged
with their calves present. This suggests that the change in
behavior was not merely a social phenomenon seen in the
presence of other individuals, but instead reects teaching
behavior targeted at a na ve observer. However, the na ve
observers in this study were presumably the calves of the
observed mothers. Future research is needed to explore if
these same mothers or other alloparents also exhibit similar
altered foraging behavior when in the presence of other
na ve observers that are not their offspring.
This altered foraging behavior on behalf of the mothers
may be a valuable social learning mechanism for Atlantic
spotted dolphins. The mothers in the study clearly altered
their typical foraging behavior in the presence of their
calves at a potential cost to themselves due to the exag-
gerated behavior, as well as sometimes foregoing ingestion
of the prey. However, as per Caro and Hausers denition
of teaching, the observer must benet from the models
altered behavior, in this case through more rapid or skillful
acquisition of foraging behavior. In dolphin society this
skill would be essential, as mothers give birth approxi-
mately every 3 years, at which time the older calf would
become weaned and rely more on independently caught
sh. It is advantageous for the mother to ensure the success
of her offspring, presumably by investing her time and
energy into the calfs foraging capabilities before the calf
is weaned. Weaning is a gradual process in spotted dol-
phins, and although the calves were not dependent upon
sh for food, consuming the sh may have been an
important part of the development of the calves foraging
behavior, perhaps because it reinforced the social-learning
process.
Future research is warranted to explore the development
and skillfulness of the young calfs pre-weaning foraging
capabilities in order to examine the full effect of the
mothers presumed teaching efforts. If this is true teaching
behavior, the calf will derive some benet from observing
the mothers altered foraging behavior. Additionally, a
comparison is needed to compare the calves of teaching
and non-teaching or less attentive mothers. However,
because all of the mothers observed in this study demon-
strated the altered foraging behavior, it may be difcult to
assess the consequences of naturally occurring individual
differences in the mothers foraging behavior on the calves.
Although the full benet for the calf is unknown, it seems
Anim Cogn (2009) 12:4353 51
1 3
that the calf is indeed the target of this altered behavior,
which was observed only in the presence of the calf.
Additionally, further research is needed into the calfs
behavior and attention to the mother. Future research can
hopefully clarify if the calf is indeed attentive to the
mothers potential teaching behavior to gain something
from the experience, as well as clarify what mechanism
the calves may be using to learn from the mothers, such
as imitation, stimulus enhancement, or local enhance-
ment. Data from this study, such as the calves being
predominantly in the observation position relative to the
mother during the events, some of the calves chasing and
ingesting the sh, and the calves interactions with both
the mothers and prey objects, may be evidence that the
calves were attentive to the mothers altered foraging
behavior and support the argument for teaching. Future
data from the calf behavior will also hopefully
strengthen our argument that the altered maternal for-
aging behavior may be an example of teaching. The data
from the calf behavior are currently being collected and
analyzed as part of a separate ongoing project and will
be available for future publication. Despite this draw-
back, we believe that this study detailing the altered
foraging behavior of the mothers is a signicant nding
in the area of animal cognition, even without data on the
calf behavior.
Despite previous research that has shown that dolphins
pass mirror self-recognition tests (Reiss and Marino 2001),
understand referential pointing (Herman et al. 1999), and
spontaneously use referential gesturing in captive situa-
tions (Xitco et al. 2001), further evidence is needed before
attributing theory of mind to dolphins, which some
researchers argue is required for true teaching (Tomasello
et al. 1993). Regardless of the lack of conclusive evidence
supporting theory of mind in dolphins, the perspective-
taking abilities by dolphins supported by previous research
(Herman et al. 1999; Xitco et al. 2001) might be sufcient
for the presumed teaching behavior shown here. Although
the cognitive abilities behind the clear alteration of forag-
ing behavior of the mother dolphins in the presence of their
calves are yet to be determined, the observed teaching
behaviors in dolphins are nonetheless remarkable. Mother
dolphins provide opportunities for calves to observe for-
aging behaviors, and sometimes even provide opportunities
for calves to practice foraging. Teaching, then, may be an
important way in which aspects of cetacean social learning
and possibly culture are transmitted from one generation to
the next.
Acknowledgments We would like to thank Stan Kuczaj and Jesse
Bering for their helpful comments on earlier drafts of this manuscript,
and John Bender, Miley Fishero, Megan Rothrock, Melissa Ingui,
Wisline Shepherd, Sheryl Spencer, and the Wild Dolphin Project for
their assistance on the project.
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