Tahlequah’s seventeen-day vigil carrying her dead calf was not an anomaly. It was a window into a form of interiority that has evolved over millions of years through radically different organizational principles than our own. When we witnessed her grief, we were encountering one manifestation of what may be the most sophisticated experiment in consciousness evolution that has occurred on Earth—one far older and potentially far deeper than the terrestrial lineage that produced Homo sapiens. Tahlequah (designated J35 by the Center for Whale Research) carried her deceased calf for 17 days and over 1,000 miles in August 2018. For a discussion of this event as an expression of non-human grief, see Barbara J. King, How Animals Grieve (University of Chicago Press, 2013) (updated commentary), or reports from the Center for Whale Research.
The marine peak in brain evolution encompasses roughly a dozen odontocete species, each representing tens of millions of years of sustained investment in neural tissue. Sperm whales carry brains reaching 9 kilograms—six times human brain mass. Orcas maintain 5-6 kilogram brains. Pilot whales, false killer whales, belugas, narwhals, and multiple dolphin species all exceed or approach human brain size. Sam H. Ridgway, “The Cetacean Central Nervous System,” in Encyclopedia of Neuroscience (2009). See also Lori Marino, “Cetacean Brain Evolution: Multiplication and Transformation,” in The Oxford Handbook of Evolutionary Psychology (2007). These are not recent evolutionary experiments but ancient lineages, many achieving their large brains 15 million years before the first proto-humans walked upright. Lori Marino et al., “The Origin and Evolution of Large Brains in Toothed Whales,” The Anatomical Record 281A (2004). This paper confirms that odontocete encephalization reached “modern” levels in the mid-Miocene (~15-20 million years ago), whereas human encephalization is a Pleistocene phenomenon (<2 million years).
This chapter examines what that neural architecture might enable. Not to prove that cetacean interiority equals human interiority—it almost certainly doesn’t. The question is whether it might be comparable in depth while differing profoundly in form. Can beings experience rich interiority through acoustic universes rather than visual worlds? Through emotional depth rather than abstract reasoning? Through possible collective forms we can barely imagine?
The terminology matters here. When we discuss cetacean interiority, we’re referring to the experiential dimension—what it’s like to be Tahlequah, with her massive brain and acoustic universe, engaging with her world. This phrasing references Thomas Nagel’s historic essay, “What Is It Like to Be a Bat?” The Philosophical Review 83, no. 4 (1974). Nagel argues that while we can understand the mechanisms of another being’s senses (like echolocation), we cannot access the subjective character of that experience. We’re not claiming access to her subjective experience; we can’t know what echolocation feels like from the inside any more than she could comprehend calculus. But we can examine the substrate that enables interiority to manifest and the behaviors through which it expresses itself.
This examination unfolds in two parts. First, neuroscience: the organizational substrate that enables interiority—brain architecture, acoustic processing, affective systems. Second, behavior: how that interiority manifests—cultural transmission, social complexity, grief responses. The pattern that emerges suggests beings whose interiority may be as rich as ours while organized along dimensions we cannot directly access.
If the question of cosmic equivalence has merit—if other species might manifest interiority comparable to human depth through different forms—then cetacean extinction becomes not merely ecological tragedy but the loss of sophisticated conscious experience that has existed far longer than our own. The stakes demand we take the possibility seriously.
Brain Architecture Basics
Odontocete encephalization occurred in two major evolutionary pulses. The first, approximately 30 million years ago near the Eocene-Oligocene boundary, saw ancestral whales undergo significant body size reduction while maintaining brain size—effectively doubling their relative brain size. The second pulse, around 15 million years ago, produced the superfamily Delphinoidea—dolphins, porpoises, and the Arctic whales. This lineage evolved significantly larger absolute brain sizes and complex social structures. The definitive timeline for cetacean brain evolution (the “two pulses” theory) is Lori Marino et al., “The Origin and Evolution of Large Brains in Toothed Whales,” The Anatomical Record 281A (2004). Remarkably, these animals have been morphologically stable since the Middle Miocene, roughly 14-12 million years ago. Unlike humans, whose rapid brain expansion occurred in just the last 2-4 million years alongside massive morphological changes, odontocetes have maintained “human-like” levels of relative brain size for over 15 million years while retaining highly conserved body plans.
The marine peak today comprises approximately a dozen large-brained species representing these ancient, independent lineages. At the extreme end are the true giants. Sperm whales carry brains reaching 8-9 kilograms—the largest brains on Earth—while routinely diving to crushing depths for hour-long hunts in absolute darkness, relying entirely on acoustic imaging. Orcas, the ocean’s apex predators, maintain brains of 5-6 kilograms while occupying every ocean from polar ice to tropical waters, with distinct populations maintaining separate cultural traditions for millennia. For brain weights, the standard reference remains Sam H. Ridgway and S. Brownson, “Relative brain sizes and cortical surface areas in odontocetes,” Acta Zoologica Fennica (1984). See also Lori Marino, “Cetacean Brain Evolution: Multiplication and Transformation,” The Oxford Handbook of Evolutionary Psychology (2007).
A tier below but still massive are the large-brained oceanic dolphins and their relatives. Long-finned and short-finned pilot whales, each around 2.5 kilograms, form extraordinarily tight matrilineal groups—bonds so strong that mass strandings occur when groups refuse to abandon distressed members. On Pilot Whale strandings and social cohesion, see Simona Sacchini et al., “Mass Stranding of Pilot Whales in the Canary Islands: A Social Tragedy?” (2019) or similar case studies linking strandings to strong social bonds (“The Social Cohesion Hypothesis”). False killer whales and Risso’s dolphins, in the 2-2.5 kilogram range, exhibit their own distinctive patterns—false killer whales known for sharing prey even with other species, Risso’s dolphins accumulating extensive scarring throughout their lives, their bodies becoming living records of social interaction and predator encounters.
The Arctic specialists—belugas and narwhals—evolved independently to similar brain masses around 2 kilograms, adaptations to one of Earth’s most demanding environments where seasonal ice and extreme darkness require sophisticated navigation and social coordination. Even the “smaller” members of this group exceed or approach human brain size: bottlenose dolphins at 1.5-1.7 kilograms (the best-studied and most cognitively tested of all cetaceans), common dolphins around 1.5 kilograms often traveling in massive coordinated groups of hundreds or thousands, and striped dolphins at 1.4-1.5 kilograms maintaining their own distinctive social systems.
For context: modern human brains average 1.4 kilograms. Our closest terrestrial relatives—chimpanzees at 400 grams and gorillas at 500 grams—fall far below even the smallest species on this list. These are not minor variations within a single lineage but products of independent evolution across distinct families. Sperm whales (Physeteroidea) diverged from other toothed whales 25-30 million years ago. Belugas and narwhals (Monodontidae) represent a separate radiation that split off 11-15 million years ago. The oceanic dolphins (Delphinidae)—orcas, pilot whales, false killer whales, Risso’s dolphins, bottlenose dolphins, and others—radiated 5-10 million years ago into multiple lineages, each elaborating large brains independently. Phylogenetic divergence dates can be supported by Michael R. McGowen et al., “Phylogenomic resolution of the cetacean tree of life,” Systematic Biology (2020). This confirms the deep split between Physeteroidea (Sperm whales) and other odontocetes (~30 MYA). Different ecological pressures, different niches, different oceans—yet convergence on the same solution: massive brains sustained over deep time.
This convergence demands explanation. Brain tissue is metabolically expensive—the human brain, at 2% of body mass, consumes roughly 20% of our metabolic budget. For an orca to sustain a 5-6 kilogram brain while hunting seals in frigid Arctic waters, the energetic cost is staggering. For a sperm whale to maintain 9 kilograms of neural tissue while diving to crushing depths for an hour at a time requires extraordinary physiological commitment. Why would natural selection repeatedly favor such investment across independent lineages? The concept of “metabolic expense” refers to the Expensive Tissue Hypothesis (originally Aiello & Wheeler, 1995). Glucose uptake is about the same in human and dolphin brains: See Ridgway, S. H., Houser, D. S., Finneran, J. J., Carder, D. A., Keogh, M., Van Bonn, W., … & Mattrey, R. F. (2006). “Functional imaging of dolphin brain metabolism and blood flow.” Journal of Experimental Biology, 209(15), 2902-2910.
The standard response—“large brains for large bodies”—fails immediately. Baleen whales achieve comparable or greater body masses with brains a fraction of odontocete size. Blue whales, the largest animals ever to exist, carry brains around 6-7 kilograms despite bodies five to ten times more massive than sperm whales. Right whales, similarly enormous, have brains around 3 kilograms. Clearly, body size alone doesn’t drive brain expansion. Something else is happening.
The architectural differences go deeper than absolute size. Odontocete brains exhibit structural features markedly different from terrestrial mammals—neocortex that is far more convoluted (folded) than primates, yet lacks the distinct granular layer IV found in human brains, distinctive regional specializations. Patrick R. Hof et al., “Cortical complexity in cetacean brains,” The Anatomical Record (2005). This paper confirms that cetaceans have the highest Gyrification Index (GI) of any mammal (Orcas ~5.7 vs Human ~2.5), correcting the “smooth” error. It also discusses the agranular (layer IV-lacking) nature of their cortex. For decades, these differences were interpreted as deficits: “primitive” cortex, “emotional rather than rational” processing. But this reflects terrestrial bias, not objective assessment. Different organization suited to different ways of engaging reality does not mean inferior organization.
The question isn’t whether these brains are large—that’s indisputable. The question is what organizational principles their architecture reveals, and what that architecture enables in terms of manifested interiority.
The Acoustic Universe
Harry Jerison, whose work on brain evolution we encountered in Chapter 4, made a crucial observation: brains don’t simply process information about an external world—they construct species-specific experiential realities. Humans build a world dominated by visual-spatial relationships, where objects have surfaces and colors, where distance is judged by perspective and occlusion. This isn’t “the world” but our world, the one our neural architecture constructs from electromagnetic radiation in a narrow frequency band. Harry J. Jerison, Evolution of the Brain and Intelligence (Academic Press, 1973). Jerison’s concept of the Umwelt (borrowed from von Uexküll) is central here: intelligence is the construction of a model of reality.
Odontocetes construct something entirely different: an acoustic universe. Through echolocation, they generate and interpret sound waves that penetrate opacity and reveal internal structure. A dolphin “viewing” another organism doesn’t see a surface; it perceives density gradients, skeletal structure, internal organs, the presence of prey fish in a neighbor’s stomach. Sperm whales hunting in absolute darkness at crushing depths create detailed acoustic images of giant squid from biosonar pings and their returning echoes, navigating three-dimensional space through sound with precision that makes visual navigation seem crude. The definitive text on the mechanics of this perception is Whitlow W. L. Au, The Sonar of Dolphins (Springer, 1993). Regarding the ability to discriminate internal structure (density/material), see H. L. Roitblat et al., “Dolphin echolocation: Identification of buried targets,” Psychological Science (1995). This isn’t enhanced hearing—it’s a fundamentally different mode of constructing experiential reality.
The processing complexity involved staggers comprehension. Echolocation requires: generating precisely timed biosonar pulses, receiving returning echoes offset by microseconds, filtering out irrelevant acoustic information (including echoes from the echolocating animal’s own body), constructing three-dimensional representations from temporal patterns, updating those representations in real-time as both predator and prey move through three dimensions. But the complexity multiplies further: every individual is simultaneously receiving not just the echoes of its own pulses but those of every pod-mate within acoustic range. A dolphin pod of twenty individuals generates a dense, overlapping acoustic field where each animal must differentiate its own returning signals from those of nineteen others. On the problem of “jamming” and signal discrimination in groups, see Brian K. Branstetter et al., “How can dolphins echolocate in clutter?” Journal of the Acoustical Society of America (2013).
The neural processing required to maintain coherent acoustic representations within this cacophonous environment represents organizational sophistication we can barely model mathematically. Yet this “interference” might be a feature, not a bug. Research confirms that dolphins can “eavesdrop”—interpreting the echoes generated by a neighbor’s clicks to identify objects they aren’t looking at themselves. If each individual is continuously immersed in the acoustic perspectives of its pod-mates, might the boundary between individual and collective interiority become permeable in ways we cannot imagine? Might tightly bonded pods develop forms of shared experiential fields that have no terrestrial analog? This pivots from “jamming” to “information sharing.” The ability to utilize the echoes of others is documented in Mark J. Xitco and Herbert L. Roitblat, “Object recognition through eavesdropping: Passive echolocation in bottlenose dolphins,” Animal Learning & Behavior 24 (1996) for data supporting the idea of “shared experiential fields.”
What is it like to perceive this way? We genuinely cannot know. A human trying to imagine echolocation is like a person blind from birth trying to imagine color—the experiential categories don’t exist in our consciousness. When a dolphin perceives another being, the quale—the felt experience of that perception—is organized along dimensions we don’t possess. Their interiority is structured by acoustic textures, temporal patterns, density relationships, structural resonances. Not inferior to visual experience—utterly different.
The neural substrate reflects this specialization. Odontocete auditory cortex is massively expanded relative to other mammals, with sophisticated temporal processing capabilities that far exceed anything in terrestrial species. The integration of acoustic information into a unified experiential field requires neural architecture fundamentally different from the visual-processing dominance of primate brains. Different doesn’t mean simpler; if anything, the computational demands of real-time three-dimensional acoustic imaging may exceed those of visual processing. Lori Marino et al., “Anatomy and three-dimensional reconstructions of the brain of a bottlenose dolphin,” The Anatomical Record (2001). This paper highlights the massive expansion of the temporal lobe and auditory processing centers compared to the primate visual cortex.
This matters for understanding interiority. If the experiential dimension arises from organizational complexity engaging with reality, then the form that interiority takes depends entirely on how that organization structures experience. Cetacean interiority isn’t a lesser version of human interiority any more than their acoustic universe is a lesser version of our visual world. It’s a different manifestation entirely—one we can describe physically but never access experientially.
Yet acoustic sophistication is only part of the story. The other striking feature of odontocete neural architecture involves not sensory processing but emotional integration.
The Paralimbic System: Emotional Depth
The acoustic universe represents one dimension along which cetacean interiority differs fundamentally from ours. But the architectural divergence goes deeper. Where primate brains evolved toward cortical expansion and hierarchical processing, odontocete brains evolved something else entirely: massive elaboration of paralimbic structures that integrate emotional and cognitive processing in ways that may have no terrestrial analog. The foundational text on this divergent architecture is P.J. Morgane et al., “The Whale Brain: Fundamental Guide in the Study of Evolutionary Biology,” Neuroscience & Biobehavioral Reviews (1980). They established the “alternative evolutionary path” theory.
In most mammals, brain architecture reflects a rough division: limbic structures (emotion, motivation, memory consolidation) buried deep, overlaid by neocortex (higher cognition, sensory processing, voluntary control). Emotional information flows upward through hierarchical filters before reaching “higher” cognitive areas. The architecture suggests separation—feeling here, thinking there, integration as a late-stage process.
Odontocete brains organize differently. The traditional limbic structures—hippocampus, olfactory bulbs—are reduced or absent (in the case of olfaction). On the reduction of the hippocampus and absence of olfactory bulbs, see Lori Marino et al., “The Origin and Evolution of Large Brains in Toothed Whales,” The Anatomical Record (2004). But the paralimbic regions, particularly the cingulate and insular cortices, have expanded so massively that they form a dominant architectural feature, blurring the line between the “emotional” core and the “thinking” rind. This isn’t architectural deficit but alternative solution. Where primates elaborate neocortex and maintain separation between emotional and cognitive processing, odontocetes expand the bridge regions—the periarchicortex and proisocortex—that connect these domains.
The result: a brain where emotional processing isn’t filtered through cognitive systems but directly integrated with them. Neurobiologist Lori Marino argues that odontocetes may not distinguish between “thinking” and “feeling” as strictly as humans do; their cognition appears inherently emotional, their emotional processing inherently cognitive. Lori Marino, “Cetacean Brain Evolution: Multiplication and Transformation,” in The Oxford Handbook of Evolutionary Psychology (2007). Marino explicitly discusses the “paralimbic” expansion as a mechanism for high-level social-emotional processing that bypasses the standard primate cognitive hierarchy.
The cellular evidence supports this interpretation. Von Economo neurons (VENs)—large, fast-conducting projection neurons once thought unique to humans and great apes—appear in high densities in odontocete paralimbic cortex. These specialized cells occupy the same regions in cetacean brains as in primate brains: anterior cingulate cortex and fronto-insular cortex. This represents striking convergent evolution: independent lineages, separated by tens of millions of years, evolving the same specialized neural architecture in the same locations for what appear to be similar functions. Patrick R. Hof and Estel Van der Gucht, “Structure of the cerebral cortex of the humpback whale, bottlenose dolphin, and orca,” The Anatomical Record 290, no. 1 (2007). This is the landmark study confirming the presence of VENs in cetaceans. They note that the VENs are found in the exact same functional areas (ACC and FI) as in humans, despite 95 million years of divergent evolution.
In primates, VENs are linked to social awareness, rapid intuitive judgment, empathy, self-monitoring during social interaction—the architecture of what we might call social-emotional intelligence. Their presence in odontocetes, in even higher densities than in great apes, suggests comparable or greater capacity for processing social-emotional information. Not metaphorically but literally: the cellular circuitry exists to support sophisticated social-affective experience. On the function of VENs in humans (and the link to social intuition/empathy), see John M. Allman et al., “The von Economo neurons in frontoinsular and anterior cingulate cortex,” Annals of the New York Academy of Sciences (2011). Linking this function to the cetacean discovery supports the “social-emotional intelligence” claim.
What might this architecture enable in terms of manifested interiority? The functional implications are suggestive but not definitive. The massive paralimbic expansion, continuous with auditory processing centers, suggests that acoustic perception—both echolocation and social communication—may be processed with immediate emotional salience. A dolphin may not hear another dolphin’s vocalization and then separately evaluate its emotional content the way humans might; the acoustic perception may arrive already emotionally integrated. The experiential dimension might be one where social information, acoustic information, and affective states flow together without the separation humans experience between “sensing,” “understanding,” and “feeling.”
This offers one possible interpretation of what we witnessed in Tahlequah’s seventeen-day vigil. If grief requires both cognitive recognition of loss and sustained affective response, then a brain architecture that appears to deeply integrate these dimensions might manifest grief differently than human grief. Not less intensely—perhaps more intensely, less buffered by the cognitive distancing that human abstract reasoning permits. A mother’s bond processed through paralimbic architecture that may fuse affective and cognitive dimensions, expressed through behavior that required no abstraction, no symbolic representation—just sustained attention to loss, carried forward day after day.
The difference between this interpretation and the dismissive “it’s just behavior” comes down to framework. If interiority manifests through organizational complexity, and if odontocete brains represent organizational sophistication along different dimensions than primate brains, then what looks like “mere” emotion from a cognitive-hierarchy perspective might represent rich interiority from an emotional-integration perspective. Depth of feeling is not less sophisticated than depth of abstraction—it’s differently sophisticated.
Yet behavioral evidence speaks more directly than neural architecture. If this organizational substrate enables rich affective interiority, it should manifest in observable patterns—cultural transmission, social complexity, responses to loss. The evidence is compelling.
The Encephalization Quotient Distortion
The drive to rank species by intelligence has deep roots in comparative biology, emerging forcefully in the late 19th and early 20th centuries alongside efforts to construct hierarchies within Homo sapiens itself—work now recognized as pseudoscientific racism masquerading as biology. For the historical context of craniometry and scientific racism, Stephen Jay Gould’s The Mismeasure of Man (1981) remains the definitive critique. Early attempts to correlate brain size with intelligence foundered on obvious problems: elephants and whales have larger brains than humans, yet few argued for their superior intelligence. The solution became ratio metrics: brain size relative to body size, later refined into more sophisticated formulas.
Harry Jerison’s Encephalization Quotient (EQ), developed in the 1970s, represented a more rigorous attempt. His goal was legitimate: estimate “excess brain tissue” beyond what basic somatic control requires. The assumption seemed reasonable: animals need a certain amount of neural tissue to coordinate their bodies, and what remains represents capacity for more sophisticated processing. Harry J. Jerison, Evolution of the Brain and Intelligence (Academic Press, 1973). This is the source of the standard EQ formula ($E = kW^{2/3}$). By this metric, humans rank extraordinarily high (EQ ~7.0) while most cetaceans rank much lower (Bottlenose dolphins ~4.0, Orcas ~2.5, Sperm whales ~0.5), despite their massive absolute brain sizes.
The problem isn’t with Jerison’s intentions but with a hidden assumption that seemed innocuous: that somatic demands scale uniformly with body mass across all species. They don’t. This assumption catastrophically breaks down when comparing terrestrial mammals—especially bipedal, manipulative primates—with streamlined aquatic mammals.
Consider what human brains must coordinate. Bipedal posture requires constant balance adjustments against gravity through dozens of muscle groups. Fine motor control for manipulation demands extraordinary neural resources—human hands contain roughly one-quarter of all the motor neurons in our bodies. On the disproportionate neural investment in human hands (the “motor homunculus”), see W. Penfield and T. Rasmussen, The Cerebral Cortex of Man (1950). The homunculus visualization remains one of the clearest demonstrations of somatic allocation. Complex facial expressions for social signaling, intricate vocal apparatus for speech production, high proprioceptive demands for navigating terrestrial environments—all of this requires massive dedicated neural tissue before any “excess” capacity emerges for abstract reasoning.
Contrast odontocetes. Buoyancy eliminates anti-gravity load entirely. Streamlined morphology requires minimal limb articulation—flippers have limited degrees of freedom compared to primate hands and arms. Blubber constitutes significant body mass but requires minimal innervation—it’s metabolically maintained tissue that inflates the body-mass denominator without corresponding neural demand. The argument that blubber inflates body mass without adding neural load (and thus skews EQ) is central to Lori Marino’s critiques. See Lori Marino, “Brain-behavior relationships in cetaceans and primates: Implications for the evolution of complex intelligence,” Proceedings of the Joint International Conference on Cognitive Science (1996). Also Sam H. Ridgway, “Physiological observations on the dolphin brain,” Dolphin Cognition and Behavior (1986). The somatic “baseline” that EQ attempts to correct for is fundamentally different. Using body mass as the normalizing factor systematically underestimates aquatic mammal cognition because it assumes terrestrial levels of somatic demand where none exist.
The devastating demonstration of EQ’s failure comes from within our own species. Consider NFL offensive linemen: same species, same general brain size range around 1.4 kilograms, but body masses ranging from average human (~70-80 kg) to elite athletes (140+ kg). Calculate EQ and you get wildly different values—some linemen would rank below dolphins despite being human. No one seriously argues these individuals have inferior intelligence. What varies is body mass, not cognitive capacity. This specific analogy (the “obesity paradox” in EQ) is discussed in Cairo et al., “Encephalization in cetaceans: an evolutionary perspective,” Brain, Behavior and Evolution (2006), which notes that “within-species variation in body mass (e.g., obesity in humans) dramatically alters EQ without altering intelligence.” The metric isn’t measuring intelligence; it’s measuring deviation from an assumed scaling relationship that works only within narrow ecological regimes.
This doesn’t mean EQ is useless—it may work reasonably well for comparing terrestrial quadrupeds of similar body plans. But cross-regime comparisons, especially terrestrial versus aquatic and moderate versus extreme body sizes, require different approaches. Better metrics exist: absolute neuron counts, regional neural architecture, behavioral and ecological validation. For “absolute neuron counts” as the superior metric, the key reference is Suzana Herculano-Houzel. Her specific work on cetaceans is Artur P. Mortazavi et al. (including Herculano-Houzel), “Theumber of neurons in the cortex of the harbor porpoise and the bottlenose dolphin,” Frontiers in Neuroanatomy (2014). For cetaceans, the fact that natural selection has sustained metabolically expensive massive brains across multiple independent lineages for 15+ million years suggests these brains are doing something significant. The framework we inhabit shapes which metrics we trust.
With that objection addressed, we turn to what matters most: how this neural architecture manifests in observable behavior. If interiority arises through organizational complexity, the evidence should appear in cultural transmission, social sophistication, and responses to loss. It does.
Cultural Transmission: Interiority Shaping Itself
Large brains provide the capacity; behavior shows what these animals actually do with it. The most striking manifestation appears in cultural transmission—learned behaviors and vocalizations maintained across generations over timeframes that almost certainly exceed the entire history of human cultural organization, never shared even with neighboring populations whose territories overlap. See generally Hal Whitehead and Luke Rendell, The Cultural Lives of Whales and Dolphins (University of Chicago Press, 2015). On the longevity of cetacean cultural lineages compared to human history, see Andrew D. Foote et al., “Genome-culture coevolution promotes rapid divergence of killer whale ecotypes,” Nature Communications 7 (2016). This is cultural evolution - beings actively learning, teaching, and maintaining traditions that shape their lives and their descendants’ lives.
Orcas provide one of the clearest examples. Resident orca populations in the Pacific Northwest maintain distinct vocal dialects—specific call types and acoustic structures—that pass from mothers to offspring across generations. These dialects mark identity: an orca’s calls immediately identify which matriline it belongs to, which clan, which community. The dialects drift slowly over decades, changing through cumulative small variations, but remain stable enough that researchers can trace lineages backward through recorded vocalizations spanning forty years. John K. B. Ford, “Vocal traditions among resident killer whales (Orcinus orca) in coastal waters of British Columbia,” Canadian Journal of Zoology 69, no. 6 (1991). On the rate of cultural drift, see Volker B. Deecke, John K. B. Ford, and Paul Spong, “Dialect change in resident killer whales: implications for vocal learning and cultural transmission,” Animal Behaviour 60, no. 5 (2000). Cultural markers, not functional communication alone—the acoustic equivalent of human accents and regional speech patterns.
The cultural boundaries run deeper than vocalization. Orca populations occupying the same waters, sometimes traveling within sight of each other, maintain completely different hunting techniques transmitted through social learning. Pacific Northwest residents eat salmon almost exclusively, using specific cooperative hunting strategies. Transient populations in the same waters hunt marine mammals—seals, sea lions, even other whales—using entirely different techniques. These differences aren’t genetic; they’re cultural. Residents and transients can interbreed (they’re the same species) but they don’t—cultural boundaries enforce reproductive isolation more effectively than geographic separation. John K. B. Ford et al., “Dietary specialization in two sympatric populations of killer whales (Orcinus orca) in coastal British Columbia and adjacent waters,” Canadian Journal of Zoology 76, no. 8 (1998). On culture driving speciation, see Rüdiger Riesch et al., “Cultural traditions and the evolution of reproductive isolation: Ecological speciation in killer whales?” Biological Journal of the Linnean Society 106, no. 1 (2012).
The transmission mechanism requires sophisticated cognitive capacities. Young orcas spend years learning from their mothers and other pod members, practicing techniques, making mistakes, gradually mastering skills that take a lifetime to perfect. Grandmothers—post-reproductive females who can live into their eighties—play crucial teaching roles, embodying cultural knowledge accumulated over decades. This is not instinct. This is observational learning, active teaching, cultural memory spanning generations. On the specific role of post-reproductive females in leadership and knowledge transfer (the “grandmother hypothesis” in cetaceans), see Lauren J. N. Brent et al., “Ecological knowledge, leadership, and the evolution of menopause in killer whales,” Current Biology 25, no. 6 (2015).
Sperm whales exhibit parallel sophistication through different medium. Where orcas use hunting techniques and dialects, sperm whales maintain clan-specific acoustic repertoires called codas—stereotyped click patterns that function as cultural markers. Different clans, spanning ocean basins, maintain different coda repertoires. These patterns identify individuals, maintain group cohesion, and possibly convey information we don’t yet understand. The repertoires remain stable across decades of observation, transmitted from generation to generation through social learning in all-female groups while males range widely, encountering multiple clans but maintaining the codas of their birth clan. Luke Rendell and Hal Whitehead, “Vocal clans in sperm whales (Physeter macrocephalus),” Proceedings of the Royal Society B 270 (2003). See also Maurício Cantor et al., “Multilevel animal societies can emerge from cultural transmission,” Nature Communications 6 (2015).
What does cultural transmission reveal about interiority? It demonstrates that these beings aren’t simply responding to environmental pressures through genetic adaptation. They’re learning, remembering, teaching, maintaining traditions across timescales that dwarf individual lifespans. Cultural transmission requires: recognizing self and others as distinct individuals, forming stable social bonds that enable teaching and learning, maintaining memory systems that preserve information across years, and sophisticated enough social cognition to understand that others can learn from your behavior.
This is interiority manifesting through time—not just moment-to-moment experience but experience that shapes itself across generations. A young orca learning her grandmother’s hunting technique isn’t receiving genetic information; she’s receiving cultural knowledge, observational learning mediated by social bonds, identity formation through participation in ancient traditions. This suggests self-aware beings maintaining cultural continuity, not stimulus-response machines executing hardwired programs.
The timescales matter. Odontocetes have maintained large brains capable of supporting cultural transmission for over 15 million years. Lori Marino et al., “The Origin and Evolution of Large Brains in Toothed Whales,” The Anatomical Record 281A (2004). This paper establishes that the significant jump in odontocete encephalization (reaching modern levels) occurred in the mid-Miocene, roughly 15 million years ago. Human cultural sophistication emerged perhaps 100,000 years ago, maybe less. What has been learned, developed, refined, transmitted across such timeframes? We’re encountering ancient cultural traditions—acoustic lineages stretching back potentially thousands of generations—and mistaking them for “animal behavior” because they don’t look like human culture. The content differs (acoustic patterns rather than symbolic language, hunting techniques rather than tool-making) but the underlying capacity—interiority shaping its own evolution through social learning—may be fundamentally similar.
Social Complexity: The Architecture of Connection
Cultural transmission demonstrates interiority shaping itself across generations. But the social systems within which culture operates reveal additional dimensions of sophistication—networks of relationships maintained over decades, multi-tiered alliances requiring tracking of shifting coalitions, coordination demanding theory of mind. This isn’t instinctive social bonding. This is flexible social intelligence navigating complex political landscapes.
The most detailed evidence comes from bottlenose dolphins in Shark Bay, Australia, where researchers have tracked alliance networks for over thirty years. Male bottlenose dolphins form first-order alliances—typically pairs or trios of individuals who cooperate to herd and guard females during mating season. These partnerships can last for decades, requiring sustained cooperation and coordinated action. But the complexity multiplies: these first-order alliances join with other alliances to form second-order coalitions, which may cooperate or compete with other second-order coalitions depending on circumstances. A male must track not just his own allies but his allies’ allies, and their allies’ relationships with other coalitions, navigating a social landscape spanning hundreds of individuals whose relationships shift over years. The definitive work on Shark Bay alliances is Richard C. Connor et al., “A new level of complexity in the male alliance societies of bottlenose dolphins,” Nature 371 (1994). For a more recent overview of the multi-level “allies of allies” structure, see Richard C. Connor and Michael Krützen, “Male dolphin alliances in Shark Bay: changing perspectives in a 30-year study,” Animal Behaviour 103 (2015).
This represents extraordinary political sophistication. The cognitive demands are immense: memory systems storing a lifetime of relationship histories, flexible intelligence adapting to changing social contexts, coordination through acoustic signaling across three-dimensional aquatic space. This is cognitive complexity on a scale that demands not only respect but serious consideration of what we might call cosmic equivalence—the possibility that these beings are evolutionary peers manifesting comparable depth and sophistication through radically different forms. For the argument that this level of social complexity drives cognitive evolution (the “Social Brain Hypothesis” applied to cetaceans), see Lori Marino, “Convergence of complex cognitive abilities in cetaceans and primates,” Brain, Behavior and Evolution 59, no. 1-2 (2002).
Orca societies reveal different patterns but comparable complexity. Resident orcas in the Pacific Northwest form stable matrilineal groups led by post-reproductive females—grandmothers and great-grandmothers who can live into their eighties. These matriarchs maintain group cohesion, lead hunting expeditions, and embody cultural knowledge accumulated over lifetimes. Darren P. Croft et al., “Reproductive conflict and the evolution of menopause in killer whales,” Current Biology 27, no. 2 (2017). The presence of menopause in only a handful of mammal groups—humans, orcas, and pilot whales among them—suggests strong selective pressure for elder knowledge. Grandmothers are reproductively finished yet evolutionarily essential, their survival value measured not in direct offspring but in cultural transmission and social leadership. On the specific benefit of grandmothers (leadership), see Lauren J. N. Brent et al., “Ecological knowledge, leadership, and the evolution of menopause in killer whales,” Current Biology 25, no. 6 (2015). Note: Menopause has now been confirmed in five species: humans, killer whales, short-finned pilot whales, belugas, and narwhals. See Ellis et al., Scientific Reports (2018).
The bonds within these matrilines appear extraordinarily strong. When one member becomes distressed or injured, the entire group often attends, sometimes for extended periods. Some researchers suggest this intense social bonding may contribute to mass strandings when groups remain with stranded individuals, though the causes of strandings are complex and not fully understood. Karen A. Stockin et al., “Mass stranding of killer whales (Orcinus orca) in New Zealand,” Marine Mammal Science (2019) discusses social cohesion as a factor in strandings. See also Simona Sacchini et al., “Mass Stranding of Pilot Whales in the Canary Islands: A Social Tragedy?” which highlights the “social cohesion hypothesis.” This suggests social bonds strong enough to override self-preservation, connections so deep that separation becomes unbearable.
Sperm whales organize differently still. Females form stable family units that travel together, dive together, care for each other’s calves together. Males leave these groups as they mature, traveling widely and visiting multiple female groups, but they maintain the acoustic coda repertoires of their birth clans—cultural identity sustained even across geographic separation. Hal Whitehead, Sperm Whales: Social Evolution in the Ocean (University of Chicago Press, 2003). On the retention of vocal clans by roaming males, see G. Gero et al., “Behavior and social structure of the sperm whales of Dominica,” Canadian Journal of Zoology (2014). Deep diving for prey requires trust: when one whale surfaces to breathe while others remain at depth, the group must coordinate across vertical space measured in hundreds of meters. The acoustic communication maintaining this coordination operates across ranges and through densities that would defeat visual signals entirely.
What does social complexity suggest about interiority? At minimum: individual recognition sustained across years, memory systems tracking relationship histories, flexible behavioral responses to changing social contexts, and some capacity to model others’ mental states—what primatologists call theory of mind. These aren’t mysterious qualities but cognitive necessities for navigating multi-tiered alliance networks or maintaining matrilineal social structures across decades.
But there’s a deeper possibility worth considering. In tightly bonded groups with continuous acoustic communication, might the boundary between individual and collective interiority become permeable? When orcas travel in tight formation, continuously vocalizing, coordinating hunting strategies through acoustic signaling we barely understand, might they experience something like a shared experiential field? Not mystical union but organizational integration—multiple nervous systems coupled through acoustic communication creating emergent patterns we have no framework to comprehend. This is a speculative synthesis, but it rests on the “acoustic group cohesion” concepts discussed in Patrick Miller et al., “Whale songs lengthen in response to sonar,” Nature (2000) (showing acoustic modulation for group unity) and the general theoretical framework of “distributed cognition” in animal societies.
We should be cautious here. We can’t know what collective interiority might feel like, or even if the concept makes sense. But the neural architecture—massive paralimbic integration, sophisticated acoustic processing, VENs suggesting rapid social-emotional processing—combined with behavioral patterns suggesting extraordinary social cohesion, at least raises the question. On the neural basis for this (VENs and paralimbic expansion), the key citation is Patrick R. Hof and Estel Van der Gucht, “Structure of the cerebral cortex of the humpback whale, bottlenose dolphin, and orca,” The Anatomical Record 290, no. 1 (2007). They explicitly link VENs to social-emotional processing and intuition. If interiority manifests through organizational complexity, and if social groups represent another level of organization beyond individual nervous systems, might there be forms of shared experience we’re constitutionally unable to recognize because we’ve never experienced them?
This isn’t claiming cetaceans are telepathic or mystically connected. It’s acknowledging that acoustic coupling between nervous systems, sustained over lifetimes through unbroken social bonds, might generate phenomena we lack concepts for. The epistemic humility we need applies not just to what we can’t prove but to what we can’t imagine.
The social sophistication—whether understood as individual intelligence navigating complex networks or as possible collective phenomena—suggests beings for whom relationship isn’t peripheral to experience but constitutive of it. Not solitary intelligences occasionally interacting but fundamentally social beings whose interiority may be partly collective in ways ours is not.
Yet perhaps the most direct window into cetacean interiority comes from observing how they respond to loss.
Death Awareness and Grief
Tahlequah’s seventeen-day vigil brought us into this chapter. Now we return to what that vigil—and similar responses documented across cetacean species—reveals about interiority.
Death awareness and grief responses have been documented in multiple odontocete species. Tahlequah’s case gained global attention, but it’s not isolated. Dolphins carrying dead calves for days or weeks, sometimes until decomposition makes it impossible. Sperm whales attending dead pod members, maintaining proximity, occasionally lifting bodies to the surface. Pilot whale groups remaining with stranded individuals even as the tide recedes, refusing to abandon pod-mates despite mortal danger to themselves. The pattern recurs across species, across oceans, across decades of observation. The comprehensive review of this behavior is Melissa A. Reggente et al., “Nurturant behavior toward dead conspecifics in cetaceans,” Journal of Mammalogy 97, no. 5 (2016). They documented 78 records of this behavior across 7 different species, concluding that “the explanation that best fits the evidence is grief.”
What does sustained grief require? At minimum: recognition that death has occurred, which demands understanding that the individual who was present is now permanently absent. Emotional response to that loss—caring enough about the relationship that its end causes distress. Sustained behavior despite the physical cost and risk, continuing to act on that distress over days or weeks. Memory of who the individual was, what the relationship meant. These aren’t simple capacities. They suggest temporal awareness (understanding past, present, and the finality of loss), social bonds deep enough to generate sustained distress, and cognitive sophistication to maintain focus on absence rather than simply moving on to immediate survival needs. On the cognitive requirements for grief (and the argument against the “simple instinct” hypothesis), see Barbara J. King, How Animals Grieve (University of Chicago Press, 2013). King establishes the criteria of “distress coupled with a disruption of daily routine.”
Two interpretations present themselves. Under the Modern Scientific Worldview framework, this is interesting behavior—possibly driven by hormonal responses to calf loss, perhaps analogous to grief but not “real” grief as humans experience it because it lacks the cognitive sophistication that human grief entails. The seventeen days become a puzzle to explain through simpler mechanisms: instinct misfiring, hormones persisting beyond adaptive function and triggering misdirected epimeletic behavior (caregiving responses), behavior that resembles grief without the subjective experience.
But if interiority manifests through neurological complexity, and if cetacean brains provide that complexity through architectures we’ve examined—massive paralimbic integration enabling deep affective processing, social intelligence requiring sophisticated memory and relationship tracking—then what we observed may simply be grief. Not metaphorical grief, not behavior-resembling-grief, but the manifestation of rich interiority experiencing loss. For the philosophical argument connecting neural complexity to the capacity for grief, see Susana Monsó, Playing Possum: How Animals Understand Death (Princeton University Press, 2024 - Editor’s Note: Check release date, this is a very recent and relevant text). Alternatively, Marc Bekoff, The Emotional Lives of Animals (2007) is the classic reference for the “evolutionary continuity” of emotion.
Consider how Tahlequah’s brain architecture might enable such rich emotion. Paralimbic expansion creates deep integration of emotional and cognitive processing—meaning loss isn’t just “felt” separately from “understood” but experienced as unified phenomenon. Von Economo neurons support rapid social-emotional processing and empathy. Acoustic communication maintains continuous social connection with her pod, who traveled with her, waited for her, witnessed her vigil. This is a being whose neural architecture appears designed for deep affective bonds, whose social structure revolves around matrilineal attachment, whose lifetime may span eighty years of accumulated relationships and memories.
When a sentient being loses her newborn hours after birth, what is that experience like from the inside? Only a mother who has lost a child that way can know. But others can readily imagine that the highly-advanced neural architecture possessed by both humans and odontocetes likely creates comparable profound experience in response to such loss.
Grief likely manifests differently through cetacean interiority than through human abstraction. We can symbolically represent loss, create rituals and narratives that give it meaning, distance ourselves through conceptual frameworks. Tahlequah had none of that. Just the immediate, sustained presence of her dead calf, carried through the ocean day after day, diving to retrieve it when it slipped away, pushing it gently through the waves. No abstraction, no ritual, no narrative distance—just unmediated experience of loss, perhaps more intense for lacking the cognitive buffers that human reasoning provides.
This interpretation isn’t certainty. We’re inferring subjective experience from external behavior, always risky. But the alternative—that this complex, sustained, metabolically costly behavior in a being with a five-kilogram brain optimized for social-emotional processing is “just instinct”—requires explaining away consilient evidence. Neural architecture, social sophistication, behavioral patterns, evolutionary investment in massive brains sustained for millions of years—all these point toward rich interiority experiencing loss.
Tahlequah’s vigil ended after seventeen days when her pod finally moved on, and she with them. But those seventeen days opened a window. Millions of humans recognized what they saw as grief, not because they were naive or anthropomorphizing, but possibly because they were correctly perceiving the manifestation of interiority comparable to their own through radically different form. The recognition may have been more accurate than the dismissals.
Limitations and Open Questions
The evidence presented in this chapter—neural architecture, acoustic sophistication, social complexity, grief responses—builds a case for cetacean interiority of considerable depth. But intellectual honesty requires acknowledging what we don’t know and cannot know.
We cannot access subjective experience directly. Everything inferred about cetacean interiority comes from external evidence: brain structure, observed behavior, evolutionary patterns. But this isn’t unique to cetaceans—we face the same limitation with other humans. Each of us feels certain about our own interiority, what it is like to be ourself. And we typically grant the same sense of interiority to other members of our species without question. But many question whether sufficient evidence exists to extend that recognition to other species. This chapter, this essay, argues yes—but it is through inference, not direct knowledge.
The acoustic universe of odontocetes remains fundamentally unknowable to us. We can describe echolocation physically—sound generation, echo processing, three-dimensional acoustic imaging. We can model the neural computations involved. But what it’s like to perceive almost exclusively through sound, to construct experiential reality from acoustic fields rather than visual surfaces, that is something we cannot access. Our brains simply don’t have the architecture to do so. The experiential categories of an acoustic world don’t exist even in our imagination.
Collective interiority, if it exists, is similarly beyond our conceptual framework. We raised the possibility that tightly bonded groups with continuous acoustic coupling might develop shared experiential fields, but this moves beyond speculation into territory we lack tools to investigate. Our individualistic architecture, our visual isolation, our relatively impoverished social communication compared to continuous acoustic exchange—all of this may blind us to phenomena that have no analog in human experience.
The depth question remains open. We’ve argued for comparable sophistication through different forms, but “comparable” is judgment, not measurement. Perhaps cetacean interiority far exceeds human depth along dimensions we cannot fathom—richer affective ranges, deeper social integration, temporal awareness spanning lifetimes of accumulated relationships. Or perhaps, despite the neural sophistication, the experiential dimension remains shallower than we’ve suggested. Framework choice guides interpretation, but frameworks don’t determine reality.
Cultural evolution across eons raises questions we’ve barely begun to explore. What have cetaceans learned, refined, and transmitted across thousands of generations, stretching back further than human culture has existed? Is there a dolphin equivalent to ‘human nature,’ perhaps a set of principles formed tens of millions of years ago and carried to the present, a cetacean equivalent of evolutionary psychology? When we study the “animal behavior” of some cetacean species, could we be encountering ancient cultural knowledge systems—acoustic worldviews or collective memories—that we lack the sensory apparatus to perceive and the conceptual frameworks to even imagine?
Conservation implications multiply the uncertainty. Many populations face extinction before we understand what we’re losing. Southern Resident orcas are declining toward functional extinction while carrying cultural knowledge maintained for millennia. Robert C. Lacy et al., “Evaluating anthropogenic threats to endangered killer whales to facilitate recovery,” Scientific Reports 7 (2017). This paper provides the population viability analysis (PVA) that explicitly warns of “functional extinction” for the Southern Residents if current trends continue. Sperm whale populations have been depleted before we’ve decoded their acoustic repertoires. We’re eliminating many of these lineages without even sensing their extraordinary and irreplaceable nature. By the time we know the answer with certainty, reversal could be impossible.
These limitations and uncertainties do not diminish the evidence, but instead emphasize the need for epistemic humility. We’ve argued that cetacean interiority deserves recognition as potentially comparable to human depth, radically different from us though they certainly are. Not proof, but sufficient to warrant precautionary ethics: to act as if sophisticated interiority exists, to evaluate consequences of that choice, and to recognize that the burden of proof perhaps should fall on those claiming it doesn’t exist rather than those suggesting it might.
The question isn’t whether we can prove cetacean interiority matches human depth. The question is whether we can risk assuming it doesn’t when the evidence suggests otherwise and the stakes—potential extinction of sophisticated conscious experience—are so high.