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A group of eminent cetacean researchers respond to headlines charging that dolphins might be "flippin' idiots". They examine behavioural, anatomical and evolutionary data to conclude that the large brain of cetaceans evolved to support complex cognitive abilities.
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PLoS Biology | 0966
May 2007 | Volume 5 | Issue 5 | e139
he brain of a sperm whale is
about 60% larger in absolute
mass than that of an elephant.
Furthermore, the brains of toothed
whales and dolphins are signifi cantly
larger than those of any nonhuman
primates and are second only to human
brains when measured with respect to
body size [1]. How and why did such
large brains evolve in these modern
cetaceans? One current view of the
evolution of dolphin brains is that their
large size was primarily a response
to social forces—the requirements
for effective functioning within a
complex society characterized by
communication and collaboration
as well as competition among group
members [2–4]. In such a society,
individuals can benefi t from the
recognition of others and knowledge of
their relationships and from fl exibility
in adapting to or implementing new
behaviors as social or ecological
context shifts. Other views focus on the
cognitive demands associated with the
use of echolocation [5–7].
Recently, Manger [8] made the
controversial claim that cetacean
brains are large because they contain
an unusually large number of
thermogenic glial cells whose numbers
increased greatly to counteract
heat loss during a decrease in
ocean temperatures in the Eocene-
Oligocene transition. Therefore, he
argues, cetacean brain size could
have evolved independently of any
cognitive demands and, further, that
there is neither neuronal evidence
nor behavioral evidence of complex
cognition in cetaceans. These claims
have garnered considerable attention
in the popular press, because they
challenge prevailing knowledge and
understanding of cetacean brain
evolution, cognition, and behavior.
We believe that the time is ripe to
present an integrated view of cetacean
brains, behavior, and evolution based
on the wealth of accumulated and
recent data on these topics. Our
conclusions support the more generally
accepted view that the large brain of
cetaceans evolved to support complex
cognitive abilities.
The Origins and Evolution of Large
Brains in Odontocetes
The cetaceans arose from artiodactyls
(even-toed ungulates) early in the
Eocene approximately 55 million years
ago (Figure 1) [9,10]. The earliest
cetaceans, archaeocetes, were not
highly encephalized; rather there was
a signifi cant increase in relative brain
size in odontocetes (toothed whales,
including dolphins) during their initial
radiation in the late Eocene–early
Oligocene transition [11]. This
dramatic increase in relative brain size
involved a substantial decrease in body
size with a concurrent, more moderate,
increase in brain size.
As Manger correctly points out,
there is evidence for oceanic cooling
during late Eocene-Oligocene times
(Figure 1) [12]. Odontocete bodies
actually got smaller during that time,
whereas, generally, cooler climates
induce increases in body size [e.g., 13],
because larger animals lose relatively
less heat to the environment. Moreover,
cetaceans were already well above
the threshold for body size to deal
with oceanic cooling [14]. Therefore,
there was no need for odontocetes to
respond to these temperature decreases
with either change in body size or brain
size. Thus, such changes in brain size
(and body size) in odontocetes were
likely due to factors other than oceanic
temperature change.
Concurrent with changes in
relative size, the brain reorganized
into a form with relatively larger
cerebral hemispheres and overall
greater similarity to that of modern
cetaceans [11]. Tentative evidence
also suggests concomitant changes
in cranial architecture and ear
structure to support echolocation
[15]. Although the selection pressure
that drove the decrease in body size is
unknown, smaller animals would have
experienced changes in their ecology
(e.g., predation risk) that may have
driven further behavioral changes. This
Cetaceans Have Complex Brains
for Complex Cognition
Lori Marino
, Richard C. Connor, R. Ewan Fordyce, Louis M. Herman, Patrick R. Hof, Louis Lefebvre, David Lusseau,
Brenda McCowan, Esther A. Nimchinsky, Adam A. Pack, Luke Rendell, Joy S. Reidenberg, Diana Reiss, Mark D. Uhen,
Estel Van der Gucht, Hal Whitehead
Essays articulate a specifi c perspective on a topic of
broad interest to scientists.
Citation: Marino L, Connor RC, Fordyce RE, Herman
LM, Hof PR, et al. (2007) Cetaceans have complex
brains for complex cognition. PLoS Biol 5(6): e139.
Copyright: © 2007 Marino et al. 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.
Lori Marino is with the Neuroscience and Behavioral
Biology Program, Emory University, Atlanta, Georgia,
United States of America. Richard C. Connor is
with the Department of Biology, University of
Massachusetts Dartmouth, North Dartmouth,
Massachusetts, United States of America. R. Ewan
Fordyce is with the Department of Geology, University
of Otago, Dunedin, New Zealand. Louis M. Herman
is with the Department of Psychology, University of
Hawaii at Manoa, Hawaii, United States of America.
Patrick R. Hof is with the Department of Neuroscience,
Mount Sinai School of Medicine, New York, New York,
United States of America. Louis Lefebvre is with the
Department of Biology, McGill University, Quebec,
Canada. David Lusseau and Hal Whitehead are with
the Department of Biology, Dalhousie University,
Halifax, Nova Scotia, Canada. Brenda McCowan is
with the School of Veterinary Medicine, University
of California Davis, Davis, California, United States
of America. Esther A. Nimchinsky is with the Center
for Molecular and Behavioral Neuroscience, Rutgers
University, Newark, New Jersey, United States of
America. Adam A. Pack is with the The Dolphin
Institute, Honolulu, HI, United States of America.
Luke Rendell is with the Department of Biology,
St. Andrews University, Fife, United Kingdom. Joy
S. Reidenberg is with the Department of Anatomy
and Functional Morphology, Mount Sinai School
of Medicine, New York, New York, United States
of America. Diana Reiss is with the Department of
Psychology, Hunter College, CUNY, New York, New
York, United States of America and the New York
Aquarium of the Wildlife Conservation Society, Bronx,
New York, United States of America. Mark D. Uhen is
with the Department of Paleobiology, Smithsonian
Institution, Washington, DC, United States of America.
Estel Van der Gucht is with the Department of
Neuroscience, Mount Sinai School of Medicine, New
York, New York, United States of America.
* To whom correspondence should be addressed.
PLoS Biology | 0967
may indicate that the large brains of
early odontocetes were used, at least
partly, for processing this entirely
new sensory mode that evolved at the
same time as these anatomical changes
and perhaps for integrating this new
mode into an increasingly complex
behavioral ecological system.
Contemporary Cetacean
The common ancestor of cetaceans
and primates lived over 95 million years
ago [16], and cetacean brains have
been on an independent evolutionary
trajectory from other mammals for
close to 55 million years [17]. During
that time, cetacean brains evolved a
unique combination of features that
are different in many respects from
primate brains.
The cetacean neocortex was once
viewed as relatively homogeneous
in cellular architecture, regionally
unspecialized, and lacking
organizational complexity. It was
thought to have poorly differentiated
neuronal morphology, low numbers
of neurons and cortical areas, and
an indistinct prefrontal cortex. This
view of cetacean neocortex harks
back to an earlier era when a few
authors who considered dolphins
rather unintelligent saw little in the
neuroanatomy, not surprisingly,
to refute that view [18,19]. This
perspective infl uenced later thinking
about cetacean brains and led to the
“initial brain” hypothesis of cetacean
neocortical evolution [20] that asserted
cetacean neocortex was primitive.
However, modern neuroanatomical
techniques convincingly demonstrate
that the cetacean neocortex has
a degree of regional parcellation
comparable to that of many terrestrial
mammals (see Box 1) [21,22]. There
is certainly no evidence that the
“cetacean scheme” is incapable of
supporting complex processing similar
to that in primates and other mammals.
Likewise, there is no reason to
expect that cetacean and primate
prefrontal cortical analogs would be,
in fact, located in the same region of
the brain. However, the expansion of
the insular and cingulate cortices in
cetaceans is consistent with high-level
cognitive functions—such as attention,
judgment, intuition, and social
awareness—known to be associated
with these regions in primates [23].
This view is further supported by the
observation that the anterior insular
and anterior cingulate cortex in
cetacean species having the largest
brains exhibit a large number of large
layer V spindle neurons [22] (Figure
2), similar to those originally reported
to be unique to humans and great apes
[24.25]. These particular neurons are
considered to be responsible for neural
Figure 1. Relationships among Odontoceti and Mysticeti, between Neoceti and Archaeoceti, and higher level taxa of Whippomorpha (Cetacea
+ Hippopotamidae)
Note that within Cetacea, the only ghost lineage (any length of time missing fossils as inferred from the phylogeny) is a short gap at the origin of
Odontoceti. There is a large ghost lineage between Hippopotamidae and the base of Cetacea. The temperature curve shows a smoothed record for the
deep sea, in turn a proxy for global climate.
May 2007 | Volume 5 | Issue 5 | e139
PLoS Biology | 0968
networks subserving aspects of social
cognition [23].
The cetacean neocortex is also
characterized by a high ratio of glial cells
to neurons, consistent with the general
pattern found in other mammals, where
neuron density decreases with absolute
brain size, probably to maintain certain
properties of neural transmission. “Glia”
include several distinct cell populations,
including: (1) oligodendrocytes, which
provide myelin for axons or “white
matter;” (2) astrocytes, which have
several roles and predominate in the
gray matter; and (3) microglia, immune
cells which are not embryologically
related to other glia or neurons. Given
their vastly different roles, it is important
to know which is being counted to
interpret the functional signifi cance
of a high glial cell/neuron ratio in
cetaceans. If, for instance, a high glial
cell/neuron ratio is due to an increase
in oligodendrocytes, this would be
consistent with previous observations
that as brains get larger, the white
matter increases proportionally more
than the gray matter [26]. In fact, recent
imaging studies show that it is precisely
by a greater proportion of white matter
that humans can be distinguished from
apes and monkeys [27,28]. Moreover,
growing evidence demonstrates that
astrocytes contribute to the modulation
and coordination of neural activity in
the brain [29–31]. Therefore, despite
Manger’s argument, a high glia cell/
neuron ratio is consistent with the
increased needs of complex brains for
rapid communication and synaptic
effi ciency.
Cetacean Cognition and Behavior
in the Laboratory
The preceding description of
cetacean brains reveals not only
their large absolute and relative size
but also underscores a structural
complexity that could support complex
information processing, allowing for
intelligent, rational behavior. There is
considerable behavioral data to support
that assumption.
Laboratory studies of bottlenose
dolphins have documented
various dimensions of their
intellectual abilities. These include
an understanding of symbolic
representations of things and
events (declarative knowledge); an
understanding of how things work or
how to manipulate them (procedural
knowledge); an understanding of the
activities, identities, and behaviors
of others, (social knowledge); and
an understanding of one’s own
image, behavior, and body parts (self
knowledge) [reviewed in 32]. All these
capabilities rest on a strong foundation
of memory; investigations have
demonstrated that bottlenose dolphin
auditory, visual, and spatial memory are
accurate and robust [33–36].
Learning, remembering, and
innovation can be life-saving cognitive
tools in a challenging environment. The
exible and diverse learning capabilities
of dolphins are well documented,
including, for example, the learning of a
variety of types of abstract rules [37,38]
and the spontaneous understanding
and execution of instructions from
televised trainers [39]. Learning of
an imposed language is perhaps the
most challenging cognitive task that
dolphins have faced in the laboratory.
Dolphins learned to understand not
only the semantic features of artifi cial
gestural and acoustic languages, but also
the syntactic features [40]. Learning
of complex syntactic structures or
decoding of anomalous structures was
often achieved through inference,
rather than through explicit instruction
Dolphins spontaneously learn
associations between sounds and
temporally paired events [42] and
demonstrate extensive imitative abilities
for sounds and for behaviors (see Box
2) [42, 43–45]. Dolphins can develop
a concept of mimicry—copying an
observed behavior or sound if given a
symbolic instruction to do so. Dolphins
are the only mammal, other than
humans, shown capable of extensive
Figure 2. Spindle Cells in the Humpback Whale Anterior Cingulate Cortex
A large number of spindle cells (arrowheads) are found in the anterior cingulate and insular and
frontopolar cortices. They exhibit an elongate morphology with clearly visible apical and basal
dendrites, and frequent grouping in clusters. Scale bar = 100 µm.
Figure 3. One of Two Bottlenose
Dolphins That Passed the Mark Test, Thus
Demonstrating Mirror Self-Recognition
(Photo credit: Diana Reiss, Wildlife
Conservation Society)
May 2007 | Volume 5 | Issue 5 | e139
PLoS Biology | 0969
and rich vocal and behavioral mimicry.
Indeed the evidence that bottlenose
dolphins are capable of imitation, one
of the highest forms of social learning,
is so strong that a leading primatologist
has concluded that they “ape better
than apes” [46].
Social knowledge includes awareness
of the indications of another.
Dolphins readily learn to understand
the signifi cance of human pointing
gestures and head gaze [47–49]. They
attend not only to the direction in
which the human points or gazes,
but also to the object of regard [50].
Dolphins can also attend to a target
being echoically interrogated by
another dolphin by “eavesdropping”
on the returning echoes [51]. Dolphins
echolocate by orienting both their body
and their narrow-beam echolocation
signal in a particular direction, which
may be a rough analog to arm and
hand directional pointing by humans
[47]. Additionally, dolphins can use
their rostrums and body alignment to
point and direct a human swimmer to
an object or place of interest [52] and
monitor whether the human receiver is
attending to them [52,53].
Self-knowledge, including self-
awareness, enables one to develop a
self-image and monitor and evaluate
one’s own behaviors. Dolphins
recognize themselves in a mirror [54]
(Figure 3), a rare ability previously
demonstrated in the great apes and
humans ([54] for a review) and,
recently, in elephants [55]. Mirror self-
Box 1. Complexity in the Cetacean Neocortex
The cetacean neocortex surpasses in
gyrifi cation all other mammals, including
humans [61,62], as seen on panels A and
B showing parasagittal sections through
the brains of a bottlenose dolphin (A) and
a humpback whale (B, anterior is to the
left). The cetacean neocortex comprises
limbic, paralimbic, and supralimbic
regions [63]. The cetacean neocortex
is thin, and it has a prominent thick
layer I, which is far more cellular than in
terrestrial species. It also displays large
inverted neurons in the cell-dense layer
II, and very large pyramidal neurons
arranged in clusters of variable size
at the border between layers III and
V. Layers III and VI vary considerably
in thickness and cellular density
across regions [21,22]. The cetacean
neocortex appears agranular due to a
lack of layer IV. Studies of neocortical
cytoarchitecture in several cetacean
species reveal clearly identifi able cortical
domains and regional complexity
as seen in primates and carnivores
[21,22,64–66]. The photomontages in
(C) show examples of the region likely to
correspond to the primary visual cortex
in the humpback whale, the Cuvier’s
beaked whale, the beluga whale, the
dwarf sperm whale, and the striped
dolphin. Note the alternating neuronal
modules, characteristic of this region,
forming columns and patches of neuropil
in layers V and VI. The absence of layer
IV, the thickness of layers I and layer VI
patterns may mean that thalamocortical
projections of cetaceans rely on a
very different wiring scheme than in
terrestrial species. In fact, mysticetes
exhibit striking cortical modules in
layer II of vast expanses of the occipital
cortex ([D], arrowheads), that are not observed in odontocetes (or other mammals) in this location, but are reminiscent of those seen
in the entorhinal cortex of mammals and in the insula of toothed whales. These neuron clusters may represent a strategy to optimize
intrahemispheric connectivity in the very large brains of mysticetes [22]. In the box fi gure, cortical layers are indicated by Roman
numerals; wm, white matter (C, D). Scale bars: (D), 400 µm; (C), except for S. coeruleoalba, 250 µm; (A), 1.2 cm; (B), 3.5 cm.
May 2007 | Volume 5 | Issue 5 | e139
PLoS Biology | 0970
recognition not only indicates an ability
to correctly interpret information in a
mirror as oneself but also demonstrates
an individual’s motivation to use the
mirror as a tool to view one’s own body.
Dolphins are also aware of their own
behaviors, able to understand and
act on gestural instructions to repeat
or not repeat a previously performed
behavior, or to monitor self-produced
bubble rings [56–58], Dolphins
also reveal conscious awareness and
conscious control of their own body
parts, using them in specifi c and often
novel ways as directed by gestural
instructions [59]. Finally, dolphins
demonstrate awareness of their own
knowledge states, i.e., metacognition,
by indicating their certainty or
uncertainty about which of two sounds
is of higher pitch [60].
Cetacean Cognition and Behavior
in the Wild
Beyond knowing what cetaceans can
do with their large complex brains,
it’s equally important to ask what
they do naturally. Long-term fi eld
research has shown that dolphins live
in large complex groups with highly
differentiated relationships that
include long-term bonds, higher-order
alliances, and cooperative networks
[61–62] that rely on learning and
memory. Some of the complexities
typical of within-group primate
alliances, such as individuals switching
sides in different social contexts, are
also seen among bottlenose dolphins.
Moreover, “alliances of alliances,”
observed in bottlenose dolphins,
are rare outside of our own species,
even among old world monkeys and
apes [3]. There is also evidence that
individual role taking has emerged
in dolphin societies to facilitate
cooperative relationships [63] and
decision-making processes [64,65].
Field studies have documented
impressive cultural learning of dialects,
foraging sites, and foraging and
feeding strategies in cetaceans. Culture,
the transmission of learned behavior, is
one of the attributes of cetaceans that
most sets them apart from the majority
of other nonhuman species [66] and is
likely underpinned by advanced social
learning abilities. Cultural attributes
have been identifi ed in many species
of cetaceans but principally in those
best studied: the bottlenose dolphin,
the killer whale, the sperm whale, and
the humpback whale [66]. One of the
most distinctive elements of cetacean
culture is multiculturalism—groups
with different cultures using the
same habitat—which is known in
bottlenose dolphins, humpback whales,
killer whales, and sperm whales. For
example, killer whale populations of
the eastern North Pacifi c are structured
into several social tiers, which possess
distinctive cultural attributes in vocal,
social, feeding, and play behavior
Social complexity and culture in
cetaceans are arguably dependent on a
complex and fl exible communication
system, encompassing vocal, visual,
tactual, and possibly chemical
signals [69]. There are differences
across cetaceans in their sound
Box 2. Imitation in Dolphins
Imitation is an important type of
social learning that can readily lead
to stable cultures. While it is clear
that many cetaceans are natural
mimics, executing synchronous motor
behaviors, such as “porpoising” in
unison, and spontaneously imitating
sounds, including the whistles of others,
imitation is a complex multidimensional
ability that is most intimately studied
in the laboratory. Bottlenose dolphin
abilities for both arbitrary vocal and
motor imitation were demonstrated
at the Kewalo Basin Marine Mammal
Laboratory in Honolulu. Vocal imitation
was investigated by broadcasting
electronically generated “model” sounds
underwater into a dolphin’s habitat [43].
In response, the dolphin vocalized into a
hydrophone. Figure A in this box shows
spectrograms of each of nine model
sounds and the resulting imitation. The
arrow points to the beginning of the
dolphin’s imitation. A variety of different
waveforms were imitated accurately;
the imitations of sounds G and H show
spontaneous octave generalization, the
imitation occurring precisely an octave
above (G) or an octave below (H) the
model sound. Octave generalization is
a rare ability that, for example, has not
been elicited from songbirds.
Social motor imitation was
demonstrated fi rst by having two
dolphins side by side with a partition
between them that allowed the
dolphins to see each other but not their
respective trainers. The “demonstrator”
dolphin was instructed gesturally by
its trainer to perform one of many
possible behaviors, including its own
self-chosen behavior. Then, the “imitator” dolphin was instructed by its trainer to either
“mimic” the demonstrated behavior or to perform another behavior. Both dolphins
successfully imitated familiar and novel modeled behaviors. This ability generalized
easily to imitating human behaviors demonstrated either at poolside (Figure B) or on a
television monitor placed behind an underwater window. Motor mimicry also extended
to self-imitation, the imitation of one’s own previous behavior. No nonhuman animal
has shown the levels of diversity, fl exibility, and cognitive control of imitative skill
demonstrated in bottlenose dolphins [44].
Figure A. Spectrograms of each of nine
model sounds and the resulting imitation.
The arrow points to the beginning of the
dolphin’s imitation.
Figure B. Dolphin imitates the behavior of
a human by using its tail as an analogy for
a leg.
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production mechanisms. Odontocetes
(primarily high-frequency producers,
echolocating) and mysticetes
(primarily low-frequency producers,
non-echolocating) exhibit radically
divergent nasal, laryngeal, and hyoid
anatomy [70–74]. Cetaceans also
supplement their repertoire of vocal
signals with visual cues (e.g., changes
in body posture), tactile behaviors
(e.g., fl ipper touching, teeth raking),
and nonvocal auditory behaviors (e.g.,
breaching, lob tailing). The temporal
sequencing of these latter nonvocal
communicative events can be highly
structured, demonstrating a complex
and diverse nonvocal communication
system [64,75].
Dolphins produce several different
whistle types and sounds. Evidence
also shows that the sequential order
of whistle production is an important
feature of their communication system
[76,77]. Extensive fi eldwork has
shown that cetacean call types exhibit
enormous variation [78,79], evolve
over time [80], and are used differently
across social groups [81]. In some
cases, the variation is so pronounced
that other species have learned to use
it in judging predation risk [82]. In
bottlenose dolphins, there is evidence
that this variation is the basis for a
referential identity-labeling system
Cultural learning of behaviors may
proceed through motor imitation or
perhaps even through direct teaching
(pedagogy), as may be the case for
killer whale calves “instructed” in beach
capture of pinnipeds by their mothers
[66,84]. Vocal imitation also occurs,
such as the development of dialects
among killer whale family groups
[78–80, 85]. The close synchrony
seen among wild dolphins is a form
of imitative behavior that may serve
in part to express their affi liation
[86]. Tool use, which is a measure of
intelligence that correlates with relative
brain size in primates [87] and birds
[88], is also documented in dolphins,
who use sponges to probe into crevices
for prey and appear to transmit the
technique culturally [89].
Evidence from various domains of
research demonstrates that cetacean
brains underwent elaboration and
reorganization during their evolution
with resulting expansion of the
neocortex. Cortical evolution, however,
proceeded along very different lines
than in primates and other large
mammals. Despite this divergence,
many cetaceans evince some of the
most sophisticated cognitive abilities
among all mammals and exhibit
striking cognitive convergences with
primates, including humans. In many
ways, it is because of the evolution of
similar levels of cognitive complexity
via an alternative neuroanatomical
path that comparative studies of
cetacean brains and primate brains
are so interesting. They are examples
of convergent evolution of function
largely in response, it appears, to
similar societal demands.
Returning to Manger, his
controversial claim is reminiscent of
the conclusion reached about bees by
physicists and mathematicians in the
1930s—that the anatomical structure of
bees and the known principles of fl ight
indicate that bee fl ight is impossible
[90]. Rightfully oblivious to Manger’s
contentions, cetaceans continue to
provide an enormous body of empirical
evidence for complex behavior,
learning, sociality, and culture. 
Support for PRH and EVdG provided
by the James S. McDonnell Foundation
(220020078). Support for contributions
by LH and AP provided by members of
The Dolphin Institute, LeBurta Atherton,
Terrie and Larry Henry, the Arthur M.
Blank Family Foundation, and The Resort
Group at Ko Olina. Support for DL
provided by the Killam Trusts. Support
for LM and MU provided by the National
Science Foundation. LR was supported by
a NERC Postdoctoral Fellowship (NER/I/
S/2002/00632). Support for DR provided by
Brian and Darlene Heidtke and the Quadra
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... Honeyguides appear to store and process spatial and temporal information about bees' nests (Corfield et al., 2013;Isack & Reyer, 1989), and New Caledonian crows (for which cooperation with humans remains unconfirmed) demonstrate exceptional cognitive flexibility during foraging tasks (Weir et al., 2002). Dolphins and orcas exhibit some of the largest relative brain sizes and cognitive capacities of all non-human mammals (Marino et al., 2007;Whitehead & Rendell, 2014), and their cooperation with humans may arise from their ability to innovate (Patterson & Mann, 2011), communicate (Janik, 2013), socially learn new foraging techniques (including how to force prey into enclosed areas, Guinet & Bouvier, 1995) and cooperate (with each other and non-human species, Zaeschmar et al., 2013). Clarifying the cognitive processes required for human-wildlife cooperation should provide insights into why some animal species regularly cooperate with humans and others do not. ...
Full-text available
Human‐wildlife cooperation is a type of mutualism in which a human and a wild, free‐living animal actively coordinate their behaviour to achieve a common beneficial outcome. While other cooperative human‐animal interactions involving captive coercion or artificial selection (including domestication) have received extensive attention, we lack integrated insights into the ecology and evolution of human‐wildlife cooperative interactions. Here, we review and synthesise the function, mechanism, development, and evolution of human‐wildlife cooperation. Active cases involve people cooperating with greater honeyguide birds and with two dolphin species, while historical cases involve wolves and orcas. In all cases, a food source located by the animal is made available to both species by a tool‐using human, coordinated with cues or signals. The mechanisms mediating the animal behaviours involved are unclear, but they may resemble those underlying intraspecific cooperation and reduced neophobia. The skills required appear to develop at least partially by social learning in both humans and the animal partners. As a result, distinct behavioural variants have emerged in each type of human‐wildlife cooperative interaction in both species, and human‐wildlife cooperation is embedded within local human cultures. We propose multiple potential origins for these unique cooperative interactions, and highlight how shifts to other interaction types threaten their persistence. Finally, we identify key questions for future research. We advocate an approach that integrates ecological, evolutionary and anthropological perspectives to advance our understanding of human‐wildlife cooperation. In doing so, we will gain new insights into the diversity of our ancestral, current and future interactions with the natural world. Read the free Plain Language Summary for this article on the Journal blog. A cooperação entre humanos e animais selvagens é um tipo de mutualismo no qual um humano e um animal, de vida livre, coordenam ativamente seu comportamento para alcançar um benefício comum. Embora outras interações cooperativas entre humanos e animais envolvendo coerção em cativeiro ou seleção artificial (incluindo domesticação) tenham recebido muita atenção, um entendimento integrado sobre a ecologia e a evolução das interações cooperativas entre humanos e animais selvagens se faz necessário. Neste estudo revisamos e sintetizamos a função, os mecanismos, o desenvolvimento e a evolução da cooperação entre humanos e animais selvagens. Casos atualmente ativos envolvem humanos que cooperam com aves Guia‐de‐mel e com duas espécies de golfinhos, enquanto casos históricos envolvem humanos, lobos e orcas. Em todos os casos, uma fonte de alimento localizada pelo animal é disponibilizada para ambas as espécies por um humano que usa uma ferramenta e coordena seu comportamento seguindo pistas ou sinais do parceiro animal. Os mecanismos envolvidos na mediação dos comportamentos animais não são claros, mas podem se assemelhar aos mecanismos subjacentes à cooperação intraespecífica e à redução de neofobia. As habilidades necessárias parecem desenvolver‐se, pelo menos parcialmente, pelo aprendizado social, tanto nos humanos, quanto nos parceiros animais. Como resultado, surgiram variantes comportamentais distintas, em cada tipo de interação cooperativa entre humanos e animais selvagens, em ambas as espécies envolvidas, e essas interações foram incorporadas nas culturas humanas locais. Propomos múltiplas origens potenciais para essas interações cooperativas únicas e destacamos como as mudanças para outros tipos de interação ameaçam sua persistência. Por fim, identificamos questões‐chave para pesquisas futuras, como abordagens que integrem perspectivas ecológicas, evolutivas e antropológicas para avançar na compreensão dessas cooperações. Dessa forma, esperamos novos entendimentos sobre a diversidade de nossas interações ancestrais, atuais e futuras com o mundo natural. Ushirikiano kati ya binadamu na wanyamapori hutokea wakati binadamu na wanyamapori wanapounganisha kikamilifu tabia zao na kutekeleza manufaa kwa pande zote. Ingawa mifano mingine ya ushirikiano kati ya binadamu na wanyamapori inahusisha ukuzaji au uteuzi bandia, tunakosa maarifa jumuishi katika ikolojia na mageuzi kuhusu mwingiliano wa binadamu na wanyamapori. Hapa, tunapitia na kuunganisha tabia, utaratibu, maendeleo na mageuzi ya ushirikiano kati ya binadamu na wanyamapori. Kesi zinazoendelea zinahusisha watu wanaoshirikiana na ndege ndege anayeongoza warinaji kuelekea asali ilipo (‘kiongozi wa asali’) na aina mbili za pomboo, wakati kesi za kihistoria zinahusisha mbwa mwitu na nyangumi. Katika mifano yote, mnyama anatafuta sehemu yenye chakula iko, na baada yakuona anatumia ishara kumelekeza mtumia‐zana mwanadamu sehumu iliopo. Mbinu zinazowezesha tabia za wanyama zinazohusika haziko wazi, lakini zinaweza kufanana na zile za msingi za ushirikiano wa ndani na kupunguza hofu ya vitu vipya (‘neophobia’). Kunauwezekano ujuzi unaohitajika inaonekana inakuzwa kupitia mafunzo ya kijamii kwa wanadamu na wanyama. Kwa sababu hii, tofauti tofauti za kitabia zimeibuka katika kila aina ya ushirikiano kati ya binadamu na wanyamapori katika spishi zote mbili, na ushirikiano kati ya binadamu na wanyamapori umepachikwa ndani ya tamaduni za kibinadamu katika maeneo ambayo hupatikana. Tunapendekeza asili nyingi zinazowezea kutufafanulia mwanzo wa tabia hizi za kipekee, lakini pia tunangazia jinsi mabadiliko ya tabia inaweza kusababisha vikwazo mpaka tabia hizi zinapotea. Hatimaye, tunaorodhesha maswali muhimu kwa ajili ya utafiti mbeleni. Tunashauri mbinu inayojumuisha mtazamo wa kiikolojia, mageuzi na kianthropolojia ili kuendeleza uelewa wetu wa ushirikiano kati ya binadamu na wanyamapori. Katika kufanya hivyo tutapata maarifa mapya kuhusu utofauti wa mwingiliano wa mababu zetu, wa sasa na wa siku zijazo za ulimwengu wa asili. Read the free Plain Language Summary for this article on the Journal blog.
... [3,4]), cetaceans (e.g. [5]), canids (e.g. [6,7]), and elephants [8,9•], has suggested that, through convergent evolution, these animals may share similar cognitive traits with us as well. ...
While researchers interested in the evolution of human intelligence have traditionally focused on the psychology of other primates, a growing field aims to understand how similar cognitive abilities emerge in evolutionarily distant taxa. Here, we briefly review what we know, and why we do not know more, about the ‘mind’ of one such animal — the elephant — as well as its relevance to understanding convergent cognitive evolution across species. We also discuss the importance of studying animals such as elephants in the wild to better identify expressions of cognitive flexibility in human-impacted environments. Finally, as researchers invested in the study of an endangered species, we emphasize the need to contribute to the management of conservation-related problems from novel, cognitive perspectives.
... For example, for a physical aspect to be considered important for an animal's welfare, it must be likely that it is impacting upon the animal's mental state. Therefore, animal welfare applies only to those species that are sentient, including cetaceans [70][71][72][73][74], and that can experience both positive and negative mental states depending on their circumstances [1,69,70,[75][76][77]. ...
Full-text available
Wildlife management can influence animal welfare and survival, although both are often not explicitly integrated into decision making. This study explores fundamental concepts and key concerns relating to the welfare and survival of stranded cetaceans. Using the Delphi method, the opinions of an international, interdisciplinary expert panel were gathered, regarding the characterisation of stranded cetacean welfare and survival likelihood, knowledge gaps and key concerns. Experts suggest that stranded cetacean welfare should be characterised based on interrelated aspects of animals’ biological function, behaviour, and mental state and the impacts of human interventions. The characterisation of survival likelihood should reflect aspects of stranded animals’ biological functioning and behaviour as well as a 6-month post-re-floating survival marker. Post-release monitoring was the major knowledge gap for survival. Welfare knowledge gaps related to diagnosing internal injuries, interpreting behavioural and physiological parameters, and euthanasia decision making. Twelve concerns were highlighted for both welfare and survival likelihood, including difficulty breathing and organ compression, skin damage and physical traumas, separation from conspecifics, and suffering and stress due to stranding and human intervention. These findings indicate inextricable links between perceptions of welfare state and the likely survival of stranded cetaceans and demonstrate a need to integrate welfare science alongside conservation biology to achieve effective, ethical management at strandings.
... Cultural transmission, the social learning of information, is believed to occur in several groups of animals, including primates, cetaceans, and birds . Cultural attributes have been vertically (from parents to offspring), obliquely (from studied in many species of cetaceans, principally in the previous generation via a nonparent model to bottlenose dolphins (Tursiops sp.), Atlantic spotted younger individuals), or horizontally (between unre-dolphins (Stenella frontalis), killer whales (Orcinus lated individuals from similar age classes or within orca), sperm whales (Physeter macrocephalus), and generations) (Whitehead et al., 2004;Herzing, 2005; humpback whales (Whitehead et al., 2004;Krützen Garland et al., 2011;Whitehead & Rendell, 2014;Marino et al., 2007;Bender et al., 2009). In the present study, at least three individu-the BSA, but efforts are being made to biopsy sample als performed the natural barrier feeding behav-humpback whales in the area. ...
... Melba and David Caldwell (Caldwell & Caldwell, 1965) first identified and described for the first time these distinctive vocalizations in captive bottlenose dolphins. Their results were questioned (McCowan & Reiss, 1995a, 1995b, 2001, but further study has confirmed their interpretation of the data Marino et al., 2007;Sayigh et al., 2007). As a result of these evaluations, hundreds of captive and free-living bottlenose dolphins have had their SWs registered and successfully cataloged (Caldwell & Caldwell, 1965;Caldwell et al., 1990;Esch et al., 2009;Harley, 2008;Janik, 1999Janik, , 2009Janik et al., 1994;Janik & Slater, 1998;Janik et al., 2006;Kriesell et al., 2014;Luís et al., 2016;Sayigh et al., 1995Sayigh et al., , 2007Watwood et al., 2005). ...
Full-text available
This study is the first baseline acoustic description of common bottlenose dolphin populations (Tursiops truncatus) from Revillagigedo Archipelago and the first identification of signature whistles (SWs) in an oceanic population of T. truncatus. A total of 85% (199/233) of the recorded whistles were classified as stereotyped whistles and subsequently (bout analysis/SIGID) categorized into one of five SW types. External observers were in perfect agreement in classifying whistles into the adopted SW categorization. SWs represented 42% (98/233) of the repertoire. Overall, most whistle types were categorized as sine (80%; SW1, SW2, SW4, and SW5) with one downsweep (20%, SW3). Roca Partida Island had the highest number of SW types. Principal component analysis explained 77% of the total SWs variance, highlighting the importance of shape/contour variables to the SWs variance. The combined mean SWs acoustic parameters from Revillagigedo Archipelago were higher than that recorded in coastal regions, which may indicate there are differences between SWs of pelagic and coastal populations. However, further acoustic and ecological studies in the Archipelago are needed to clarify and expand our findings, to identify its members (Photo ID and SW Revillagigedo Catalog), and to investigate this topic at other oceanic islands.
... It should also be noted that despite frequent claims for intelligence in cetaceans and especially bottlenose porpoises (Falk 2022), not only is the evidence for mirror self-recognition weak and the methodology often questionable, but in spite of unusually large brains, their other accomplishments in the intellectual domain are not nearly as profound as some would like to believe (Marino et al. 2007;Marino et al. 2008). For a compelling and rigorous review of the faulty thinking, poor methodology and weak evidence for intelligence in cetaceans see Manger (2013). ...
Full-text available
We evaluate claims for extraterrestrial intelligence based on the logic behind assertions such as the absence of evidence is not evidence of absence. To assess intelligence elsewhere in the universe we outline two of the principle scientific claims for intelligence on Earth. One involves the idea that intelligence involves working out the reasons for our own existence. The other involves self-awareness and the capacity to make inferences about what others know, want, or intend to do. The famous quote from Rene Descartes "I think; therefore, I am" needs to be revised to read "I am; therefore, I think." Some of the conclusions we derive about intelligence include the idea that most species on planet Earth have clever brains but blank minds (no self-consciousness); humans are the only species where what you know could get you killed; if humans become extinct it is highly unlikely that human-like intelligence will re-emerge on this planet and the odds of human-like intelligence evolving on other worlds is infinitely small. However, if intelligence exists elsewhere in the universe it may not have revealed itself because humans are dangerous and are perceived as posing too great a risk.
... Thus, the low LSO neuron density in D delphis may be the result to the large size of LSO neurons. As it was previously proposed for the dolphin auditory cortex, the increase in functional significance of hearing may be associated with an enlargement of auditory structures in the brain, and not with higher neuron densities (Marino et al., 2007;Poth et al., 2005). This research was also supported by a Baden-Württemberg Student Scholarship to CN through the University of Freiburg, Germany, and a grant from to DLR R01 AG043640 from NIH. ...
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In all mammals, the superior olivary complex (SOC) comprises a group of auditory brainstem nuclei that are important for sound localization. Its principal nuclei, the lateral superior olive (LSO) and the medial superior olive (MSO) process interaural time and intensity differences, which are the main cues for sound localization in the horizontal plane. Toothed whales (odontocetes) rely heavily on hearing and echolocation for foraging, orientation, and communication and localize sound with great acuity. The investigation of the SOC in odontocetes provides insight into adaptations to underwater hearing and echolocation. However, quantitative anatomical data for odontocetes are currently lacking. We quantified the volume, total neuron number, and neuron density of the LSO of six common dolphins (Delphinus delphis) using the Cavalieri principle and the unbiased stereology optical fractionator. Our results show that the LSO in D. delphis has a volume of 150 + (SD = 27) mm3 , which is on average 69 (SEM = 19) times larger than the LSO in human, or 37 (SEM = 11) times larger than the human LSO and MSO combined. The LSO of D. delphis contains 20,876 ± (SD = 3300) neurons. In comparison, data reported for the human brainstem indicate the LSO has only about ¼ that number but about the same number for the LSO and MSO combined (21,100). LSO neurons range from 21 to 25 μm (minor axis) and from 44 to 61 μm (major axis) in transverse sections. The LSO neuron packing density is 1080 ± (SD = 204) neurons/mm3 , roughly half of the LSO neuron density in human. SMI-32-immunohistochemistry was used to visualize projection neurons in the LSO and revealed the presence of principal, marginal, and multipolar neurons in transverse sections. The distinct morphology of the LSO likely reflects the common dolphin's superb sensitivity to ultra-high frequencies and ability to detect and analyze sounds and their location as part of its underwater spatial localization and echolocation tasks.
This chapter explores those interactions between marine mammals and people in which the animals seem to choose to connect with us. Some well-documented examples are considered, and particular attention given to the phenomenon of “solitary-sociable dolphins,” of which more than three dozen have been recorded since 2008. The history of these “friendly” animals reveals that they are often exposed to harmful, and even lethal, interactions, underlining the need to manage their circumstances better, including trying to prevent them from becoming habituated to human company in the first place. The case studies explored include the histories of Springer and Luna, orcas (Orcinus orca) that became separated from their natal pods when very young, Hvaldimir, a beluga (Delphinapterus leucas), who had once been a captive, and Fungie, a common bottlenose dolphin (Tursiops truncatus), who lived alone for thirty-six years in a small bay in Ireland. The stories of Springer and Hvaldimir show that repatriation to the wild is at times possible for such animals. Some “friendly” pinnipeds seeking human company have also been recorded with examples including a monk seal (Monachus monachus) in Samos, Greece and numerous friendly gray seals (Halichoerus grypus) in the United Kingdom. Three other categories of interactions are also described: cooperative fishing (where dolphins and fishermen act in collaboration to the advantage of both), other solicitations of human assistance (instances where animals have approached swimmers or divers to assist them in removing something from their bodies), and food-sharing (where animals pass food to people). Some of the behaviors reported reflect the high-cognitive ability of the marine mammals concerned. Combined with the associated highly social nature of many small cetaceans, which can even extend to animals outside of their own species, this may help to explain why they sometimes form associations with people.
Von Economo neurons (VENs) are a recently evolved cell type which may be involved in the fast intuitive assessment of complex situations. As such, they could be part of the circuitry supporting human social networks. We propose that the VENs relay an output of fronto-insular and anterior cingulate cortex to the parts of frontal and temporal cortex associated with theory-of-mind, where fast intuitions are melded with slower, deliberative judgments. The VENs emerge mainly after birth and increase in number until age 4 yrs. We propose that in autism spectrum disorders the VENs fail to develop normally, and that this failure might be partially responsible for the associated social disabilities that result from faulty intuition.
Of all aquatic animals only odontocete cetaceans are known to have a well developed sonar system. While certain other marine vertebrates will be discussed briefly in the latter part of this review, we are primarily concerned with the toothed whales.
Humans respond adaptively to uncertainty by escaping or seeking additional information. To foster a comparative study of uncertainty processes, we asked whether humans and a bottlenosed dolphin (Tursiops truncatus) would use similarly a psychophysical uncertain response. Human observers and the dolphin were given 2 primary discrimination responses and a way to escape chosen trials into easier ones. Humans escaped sparingly from the most difficult trials near threshold that left them demonstrably uncertain of the stimulus. The dolphin performed nearly identically. The behavior of both species is considered from the perspectives of signal detection theory and optimality theory, and its appropriate interpretation is discussed. Human and dolphin uncertain responses seem to be interesting cognitive analogs and may depend on cognitive or controlled decisional mechanisms. The capacity to monitor ongoing cognition, and use uncertainty appropriately, would be a valuable adaptation for animal minds. This recommends uncertainty processes as an important but neglected area for future comparative research.
Cetaceans diverged from terrestrial mammals between 50 and 60 million years ago and acquired, during their adaptation to a fully aquatic milieu, many derived features, including echolocation (in odontocetes), remarkable auditory and communicative abilities, as well as a complex social organization. Whereas brain structure has been documented in detail in some odontocetes, few reports exist on its organization in mysticetes. We studied the cerebral cortex of the humpback whale (Megaptera novaeangliae) in comparison to another balaenopterid, the fin whale, and representative odontocetes. We observed several differences between Megaptera and odontocetes, such as a highly clustered organization of layer II over the occipital and inferotemporal neocortex, whereas such pattern is restricted to the ventral insula in odontocetes. A striking observation in Megaptera was the presence in layer V of the anterior cingulate, anterior insular, and frontopolar cortices of large spindle cells, similar in morphology and distribution to those described in hominids, suggesting a case of parallel evolution. They were also observed in the fin whale and the largest odontocetes, but not in species with smaller brains or body size. The hippocampal formation, unremarkable in odontocetes, is further diminutive in Megaptera, contrasting with terrestrial mammals. As in odontocetes, clear cytoarchitectural patterns exist in the neocortex of Megaptera, making it possible to define many cortical domains. These observations demonstrate that Megaptera differs from Odontoceti in certain aspects of cortical cytoarchitecture and may provide a neuromorphologic basis for functional and behavioral differences between the suborders as well as a reflection of their divergent evolution. Anat Rec Part A, 2006. (c) 2006 Wiley-Liss, Inc.
Cetaceans produce sounds at opposite ends of the frequency spectrum. The laryngeal role in odontocete sound production (echolocation, communication) remains unclear. Mysticete infrasonics are presumed to be laryngeal in origin, but production mechanisms are unknown. To address this, we examined postmortem larynges in 6 mysticete species (3 genera) and compared them to our odontocete collection (20 species/15 genera). Results indicate that the rostral portion of the odontocete larynx is elongated, narrow, rigid, and normally positioned intranarially. This portion of the mysticete larynx is comparatively shortened, open, pliable, and in Megaptera may be retracted from its intranarial position. Internally, mysticete vocal folds are thick, paired, and oriented horizontally, compared with the thin, usually unpaired, and vertically oriented odontocete fold. Mysticetes may generate low frequency sounds via pneumatically driven fold vibrations, which then pass to attached laryngeal sac walls, through overlying throat pleats, to water. Rorqual mysticetes may also vibrate paired corniculate flaps while regulating airflow into the nasal region. Infrasonic pulses may pass through adjacent soft palate, skull, or nasal cartilages to water. Laryngeal anatomy in mysticetes and odontocetes appears highly divergent. These morphological differences may correlate to adaptations for producing infrasonic (mysticete) or ultrasonic (odontocete) communication. [Work supported by ONR:N00014-96-1-0764, ONR:N00014-99-1-0815, and AMNHSOF.]