Cetacean Behavior Toward the Dead and Dying
- 109 Downloads
KeywordsCetacean Behavior Dead Calf Dead Infant Globicephala Terrestrial Mammals
Evolutionary Origin of Grieving Among Mammals
Behavioral patterns and psychological dispositions toward the dead – including grieving, mourning, and bereavement – have been studied thoroughly among humans, but similar behaviors are poorly understood when performed by nonhuman mammals. The shared roots of grieving among humans and other animals were recognized early by Charles Darwin (1872) and the evolutionary meaning and significance of grieving were later elaborated in the work of authors such as John Archer, John Bowlby, and Colin M. Parkes. Their insightful writings explain that grief is ultimately a reaction to a deficit, arising as a by-product of the broadly similar reaction to separation. In other words, grieving is the cost of commitment (Parkes 1972), the downside of attachment and love (Archer 1999), and its emotional responses have evolved from the basic need of maintaining proximity with a partner or offspring. The maladaptive aspects of grieving have been seen as a trade-off with other adaptive features, needed to maintain a stable relationship. Grieving results from the breaking of attachment bonds and its intensity generally parallels the strength of attachment: as Archer states, “if there is no attachment, there will be no grief.” When a dear one dies, the longing remains largely intact and the experience of loss often produces responses including distress, depression, and compulsive behaviors that may ultimately threaten the survivor, as documented by studies of humans and by a limited number of studies on other mammals (particularly primates).
While understanding death is generally regarded as a human attribute, such understanding per se does not necessarily help us overcome behavioral patterns and emotional responses that are deeply rooted in our evolutionary history. Observations of cetaceans (the taxonomic group that includes whales, dolphins and porpoises) suggest that at least in some cases – most notably upon the death of an offspring – behavioral patterns and emotional responses can parallel those found among humans and other terrestrial mammals. Whether or not they are explicitly referred to as grieving, cetacean reactions to a loss can be behaviorally extreme, strikingly maladaptive, and long-lasting. Such reactions possibly reflect aspects of bereavement, generated by terminal breaking of the strong social bonds known to exist among some cetacean species.
Cases of Epimeletic Behavior
Possibly more than one hundred cases related to epimeletic behavior have been documented in captive or free-ranging cetaceans (Norris and Prescott 1961; Caldwell and Caldwell 1966; Reggente et al. 2016), but reports tend to be opportunistic with an anecdotal, descriptive, and nonexperimental character. Early reports tend to be particularly blurry and most pre-1970 cases refer to either animals killed by whalers, observations resulting from the deliberate harming and killing of animals “for science,” or cetaceans held in captivity, not ideal settings for unbiased observations of natural behavior. The discussion in this entry refers to post-1970 published literature of cetacean behavior in the wild.
Cetaceans include 89 extant species, but the published reports of epimeletic behavior are restricted to a much smaller subset of relatively well-studied species. Of 45 published reports of cetacean behavior toward dead or dying conspecifics, 24 (53%) refer to only two genera: Tursiops (17 cases) and Globicephala (7). The remaining reports are scattered across 12 other genera, all within the family Delphinidae except for two cases involving the beluga Delphinapterus leucas, one involving the sperm whale Physeter macrocephalus and one involving the humpback whale Megaptera novaeangliae. The number of reports per species depends in part on opportunities of observing a relatively rare behavior, which vary depending on species abundance, distribution (e.g., increased accessibility due to proximity to shore), and other factors. Even considering these factors, cases of caregiving behavior appear rare among mysticetes (most cases are dated whaling episodes where individuals reacted to harpooned calves or group members; Caldwell and Caldwell 1966). Cases also appear to be uncommon among some intensively studied odontocetes. For instance, only one published record of epimeletic behavior exists for the highly social and cognitively advanced killer whale Orcinus orca (the observation of a female carrying a dead neonate in her mouth; Reggente et al. 2016).
Apart from the differences among species (cetaceans differ greatly in body size, cephalization, ecology, behavior, and social organization), differences are likely to exist within species. Attitudes towards the dead are known to have remarkable individual and cultural variability among human and nonhuman animals alike (Archer 1999; King 2013). Variability within the same cetacean species, or even within populations or groups of conspecifics may occur, due to differences related to age, sex, relationship with the deceased, ecological context, predation risk, and a number of other nontaxonomic factors. Because of the small sample size and other sampling constraints, the known cases of cetacean behavior toward the dead or dying may not represent the “typical” repertory of a particular species.
Caregivers and Receivers
Among humans, grief parallels the strength of attachment between caregiver and receiver, and the loss of a child is regarded as the most difficult to bear. Mothers generally show higher levels of attachment than fathers, because females make the greatest parental investment and paternity among males is uncertain (Archer 1999). Consistent with studies of wild terrestrial mammals, the caregiver among cetaceans is invariably an adult and the receiver is mostly a dead calf or juvenile (89% of 45 events directed toward conspecifics). When cases involve dead calves and the sex of the caregiver is known (n=12), it is typically a female (92%). Published observations of known male caregivers are limited to the single case of an adult short-finned pilot whale G. macrorhynchus carrying a dead calf in his mouth while swimming among other group members (Baird 2016). While this behavior was interpreted as grieving by the author, it may have alternative explanations. For instance, cases of infanticide and violent aggression directed toward conspecifics (and nonconspecifics) are not uncommon among common bottlenose dolphins T. truncatus and have been reported to occur in several other cetacean species. Considering these cases, it cannot be ruled out that a male may be carrying a dead calf – that he might have killed himself – to ensure the calf’s mother stays with him (possibly resulting in reproductive benefits when the time comes), as a “trophy,” or for other unknown reasons (Shane 1994).
Female caregivers are often inferred to be the mothers of the dead or dying calf, but parenthood is rarely confirmed. In one well-documented case, an unrelated female was observed providing most of the care to another female’s dead calf (Quintana-Rizzo and Wells 2016). A related observation involved a bottlenose dolphin mother who spent considerably more time with her grandson following the death of her own calf (Mann and Barnett 1999), possibly as a form of “compensation.”
In approximately 10% of the published observations from the wild, the main caregiver is assisted by other individuals, sometimes called “escorts,” which actively help support a dead or dying calf at the surface by pushing or nudging the carcass. Compared to these observations involving dead calves, records of multiple individuals targeting a dead adult or subadult conspecific (five observations, 11% of the total) appear to belong to a different category of behavior. All of the five observations include instances of arousal such as belly-to-belly contact, erected penises, and mating attempts targeting the deceased. Conversely, no cases of arousal have ever been observed among escorting group members when the receiver is a dead calf. Cases of necrophilia with dead conspecifics, and nonconspecifics alike, have been observed among wild marine mammal males (Harris et al. 2010), but these behaviors are rare in most mammalian species. Among cetaceans, cases of arousal in the presence of a dead adult or subadult conspecific seem to be common when several group members are present. In one of the five observations, the dead target was a subadult male bottlenose dolphin (Dudzinski et al. 2003); in another, an adult male humpback whale that was killed during a competitive interaction with conspecifics (Pack et al. 1998). Sexual arousal may be triggered by physiological responses related to stress or be expressions of dominance, devoid of a reproductive purpose.
Learning to Mother
The hypothesis known as “learning to mother” has been proposed to explain the carrying of dead offspring by nonhuman primates (e.g., Warren and Williamson 2004). This hypothesis contends that benefits can be gained by carrying a corpse, for instance, to learn useful motor skills while traveling and foraging. Because even brief exposure to infants can improve maternal skills among primates, it has been conjectured that carrying a dead infant may make a mother more capable of dealing with subsequent offspring that need to be carried. Practicing of parental skills also has been proposed to explain epimeletic behavior and carrying of dead calves by cetaceans, though none of the extant cetacean species would “carry” their living calves, and the benefits of practicing such behavior are dubious.
Grieving can reduce the survival of the caregiver due to energy expenditure, stress, increased exposure to predation risk, lower foraging opportunities, and other factors. The reactions of caregivers, however, can potentially have an adaptive component. While no inference can be made as to whether the caregiver knows that the receiver is alive or dead, observations of terrestrial mammals suggest that an inanimate receiver can return to life following forceful manipulation, hits, and strokes by a caregiver. Protracted manipulation of an inanimate body may be the animal equivalent of cardiopulmonary resuscitation. The typically energy-expensive initial phases of grieving, involving a “denial of reality” (Archer 1999), and active or even aggressive behavior may therefore have the occasional benefit of rescuing an apparently dead individual.
Cetacean mothers are known to respond to nonbreathing newborns by lifting them to the surface and stimulating the first breath, arguably an evolutionarily important behavior which general pattern might be related to similar attempts following perinatal death (Krasnova et al. 2014). Whether or not persistent manipulation actually results in occasional resuscitation among inanimate cetaceans is not known, but this possibility cannot be ruled out. Among cetaceans, however, such behavior is not limited to the time immediately following death, as one would expect if handling was exclusively related to resuscitation attempts having any chance of success. For instance, forceful handling involving tossing and vigorous strikes has included calves and juvenile cetaceans in moderate decomposition.
Length of Carry and Phases of Grief
Whether or not the caregivers can discriminate between life and death, or have an understanding thereof, proximity with the deceased facilitates acceptance of death, or at least can contribute to the necessary behavioral and emotional transitions. Among humans, there is a consensus that it is helpful for parents to see or hold their baby following a stillbirth. Human mothers need a period of time to come to terms with the loss, and maintaining proximity with a dead baby may help mitigate the trauma of separation. In such a context, grieving may have therapeutic benefits (Archer 1999). A cetacean corollary is that the well-intentioned decision of taking dead calves away from caregiving dolphins – often reported in the published literature (29% of the sample) – may not be in the best interest of the surviving animal(s), particularly in the early phases of grieving and following perinatal death.
In later phases, attachment and social bonds represent powerful psychological mechanisms delaying abandonment and the caregiver may become incapable of letting go. Unwillingness to leave the dead may prompt behaviors to become compulsive and stereotypic, with an increase in apparently maladaptive and aberrant components. Several odontocete species have been observed carrying calves in advanced decomposition, sometimes flaccid remains beyond recognition or even body parts (e.g., a truncated head). Only a few mammal species, all of which are primates, are known to carry the dead as long as cetaceans. Primate mothers of several species can carry their dead infants for days or weeks before abandoning them, sometimes until they are mummified – a behavior that has been related to extreme climatic conditions slowing down decomposition and extending the periods over which dead infants can be carried (Fashing et al. 2011).
Cetaceans can carry a dead calf over long distances while swimming and diving. Facilitated by reduced gravity, these aquatic mammals can afford carrying dead bodies for long periods of time, and some foraging obviously must occur when the carrying is protracted for weeks. Odontocete species with a dorsal fin may find it easier to carry a dead calf on their dorsum, draped over the anterior edge of their fin, while continuing to move and forage. Carrying may be comparatively more costly for deep-diving cetaceans or fast-moving gregarious species. For most terrestrial mammals, transporting a dead body can be challenging, or even virtually impossible. For example, giraffe mothers Giraffa sp. can remain vigilant in proximity to their dead calf for periods up to several days (Bercovitch 2013), but would not be able to actually carry it. Ring-tailed lemurs Lemur catta can hardly carry infants that do not hold themselves to their fur, and have been documented moving between a dead infant and their troop (Nakamichi et al. 1996). A comparatively lower energetic cost of carrying, for at least some cetacean species, may contribute to delayed abandonment as compared to other taxa. An additional factor that might delay abandonment of a decomposing carcass is the apparent lack of olfaction and taste in most cetaceans (Cozzi et al. 2017), which could potentially result in weak avoidance mechanisms. In terrestrial mammals with a pronounced olfaction, decomposition processes and the smell of death likely deter proximity to decaying bodies, implying a risk of disease transmission that triggers avoidance as decomposition progresses.
What causes a female to eventually stop carrying a dead calf? Among primates, physiological changes in the mother associated with infant death have been suggested to play a role in the abandonment. For instance, postpartum amenorrhea is shortened after an infant’s death, and the hormonal changes preparing the mother for the arrival of a new infant may contribute to a gradual release of the attachment to the dead infant and its remains (Biro et al. 2010). Among human mothers, the absence or cessation of breastfeeding may increase the desire to hold their baby, but such a desire will tend to fade over time. Similar physiological and psychological changes mediated by hormonal shifts are likely to occur among cetaceans as well, creating the conditions for abandonment. Other factors that may contribute to promoting detachment from the dead include the risk of losing contact with other group members when the rest of the group moves away, fear or uneasiness resulting from isolation and increased predation risk, and hunger.
Surrogates and Other Species
While caring for a living conspecific is clearly adaptive (Clutton-Brock 2009), the evolutionary meaning of caring becomes blurred when targets are living individuals or carcasses of other species, or even objects. In some of these cases, nonconspecifics and objects may become surrogates that help mitigate separation distress and address an overwhelming need to maintain attachment, if merely an illusion thereof. Even in these cases, the caregiver may respond in a protective manner when observers attempt to approach or remove their burden – whether unrelated animals or objects.
A vivid example – though not necessarily representative of natural behavior – is given by a captive beluga whose dead calf was removed from the pool postpartum. The female first started carrying her own placenta, and after the placenta was removed she resorted to a buoy, which she continued carrying for several months (Kilborn 1994). Possibly related observations (for a total of seven occurrences) were made in the wild, where belugas of undetermined sex were reported carrying a newborn, a placenta and amniotic sac, a piece of seine net, planks up to 2–2.5 m long (four cases), and the entire skeleton of a dead caribou Rangifer tarandus (Smith and Sleno 1986). These short-lasting and nonsystematic observations could document a need for surrogates following the death of previous calves, similar to the case observed in captivity, though some cases may have different meanings, such as playful behavior.
A particularly puzzling series of observations involved several short-finned pilot whales persistently carrying dead California sea lions Zalophus californianus in various stages of decomposition (“from freshly dead to furless blubbery corpses with bones extruding”; Shane 1994). This behavior was performed consistently by several pilot whales in 19 separate events observed over 12 days, with only two cases attributed to adult males. Considering the lack of social bonds between pilot whales and sea lions and several other aspects inconsistent with the hypothesis of epimeletic behavior or grieving, these events were tentatively explained as a way of conferring a particular status to the carrier (Shane 1994). However, the interpretation of these and other cases involving the carrying of dead nonconspecifics remains largely conjectural.
Cases of nonoffspring “adoption” and care toward living nonconspecifics are not uncommon among cetaceans and other mammals and may represent practice to deal skillfully with one’s own offspring. Caregiving behaviors directed toward living and dead nonconspecifics may also express (and potentially reinforce) “compassionate” behaviors that – beyond being apparently misdirected byproducts of generally adaptive models – can yield long-term net benefits. Such behaviors may include unexpected targets, adding striking aspects to the vast cetacean repertory. For instance, “interspecific altruism” was postulated to explain the repeatedly observed mobbing of mammal-eating killer whales by humpback whales, apparently intended to protect other cetacean species, but also pinnipeds and even a fish (the ocean sunfish Mola mola; Pitman et al. 2017).
Neural Basis of Grieving
What is the neural basis behind the complex behavior shown by some cetacean species towards the dead and dying, and is such a neural basis shared by all mammals displaying similar behaviors? “Higher” emotional behavior in humans and other primates has been at least partially localized in the orbitofrontal cortex, and instinctive behavior may be organized and activated by sensory areas, by the cingulate cortex and the amygdala (Rolls 2011). These parts, and their connections, may be identified and compared in different species by certain anatomical boundaries, but especially by their structure (i.e., the way the neurons that constitute them are placed, connected, and communicate chemically).
The functional anatomy of the cetacean brain has been particularly well studied in the common bottlenose dolphin (Cozzi et al. 2017). The structure and functional organization of the neocortex of this species disclose a thinner cortex and a different, apparently less complex, circuitry. The human neocortex (but also that of rodents and terrestrial carnivores), including the orbitofrontal, is a six-layered structure in which the fourth layer from the top plays a pivotal role and appears prominent in the brain’s sensory and associative areas. Among cetaceans, the fourth layer is absent or extremely reduced (Hof et al. 1999), and the projections of the cortex from and to the rest of the brain must follow a different pathway, with a circuitry similar to that of hoofed mammals (Cozzi et al. 2017).
An analysis of cetaceans’ limbic lobe leads to similar conclusions: a large part of the components of the limbic lobe in terrestrial mammals are phylogenetically and physiologically linked to the olfactory lobes and the perception of smell. Odontocetes have no olfactory nerve and lack all of the connected structures (Cozzi et al. 2017). Mysticetes have remnants of the olfactory structures, but their functionality remains to be validated. All that is left of the limbic lobe in cetaceans is an extremely reduced hippocampus (Morgane et al. 1982), so small that it may be difficult to identify even in very large brains (as a comparison, the same structure may amount to 1/5 or 1/6 of the entire telencephalon in some hoofed mammals).
The neuroanatomical aspects summarized above suggest that the structures of the dolphin brain potentially (by comparison) involved in emotional and instinctive behavior follow a strikingly different organization compared to humans and other terrestrial mammals: they have fewer neural layers, alternative neurochemical communication, and relatively simpler circuitry. Therefore, the grieving behavior of dolphins and that of humans and other well-studied terrestrial mammals cannot be based on comparable neuroanatomical and neurophysiological patterns. Observations of caregiving dolphins reviewed in this entry may lead to psychological analogies that remain unexplained by our current understanding of the structures physiologically involved in the neural basis of such behavior.
Beyond the remarkable differences in neuroanatomy, we concur with Darwin that if related species show similar responses under similar circumstances, the underlying proximate processes are probably homologous (i.e., derived from a common ancestor) rather than analogous (i.e., independently evolved) – a view consistent with recent research on mammalian empathy (de Waal and Preston 2017). A wide variety of vertebrates showing social attachment and parental care have a motivation to help distressed and vulnerable targets (de Waal and Preston 2017), and reactions equivalent to human grief can be expected among social animals separated by a companion with whom they have an evolutionarily important prolonged relationship (Archer 1999). Field observations of odontocetes suggest neural perception-action mechanisms similar to those observed among social terrestrial mammals such as primates – particularly when an adult female and a dead calf are involved. Nevertheless, several other aspects of cetacean behavior toward the dead and dying remain obscure, particularly when the target is a dead adult conspecific, or a dead nonconspecific. Clearly, much remains to be done to achieve a satisfactory understanding of the cognitive and behavioral aspects surrounding death among cetaceans.
Occurrence of caregiving behavior among different cetacean species deserves to be better investigated and framed in the larger context of research on behavioral patterns that may be expressions of empathy in nonhuman vertebrates.
- Baird, R. W. (2016). The lives of Hawai‘i’s dolphins and whales: Natural history and conservation. Honolulu: University of Hawai‘i Press.Google Scholar
- Bearzi, G., & Reggente, M. A. L. (2017). Epimeletic behavior. In B. Würsig, J. G. M. Thewissen & K. Kovacs (Eds.), Encyclopedia of marine mammals (3rd ed., pp. 369–370). Amsterdam and San Diego: Elsevier/Academic Press.Google Scholar
- Caldwell, M. C., & Caldwell, D. K. (1966). Epimeletic (care-giving) behavior in Cetacea. In K. S. Norris (Ed.), Whales, porpoises and dolphins (pp. 755–789). Berkeley: University of California Press.Google Scholar
- Cozzi, B., Huggenberger, S., & Oelschläger, H. A. (2017). Anatomy of dolphins: Insights into body structure and function. Amsterdam: Elsevier.Google Scholar
- Fashing, P. J., Nguyen, N., Barry, T. S., Barret Goodale, C., Burke, R. J., Jones, S. C. Z., Kerby, J. T., Lee, L. M., Nurmi, N. O., & Venkataraman, V. V. (2011). Death among geladas (Theropithecus gelada): A broader perspective on mummified infants and primate thanatology. American Journal of Primatology, 73, 405–409.CrossRefPubMedGoogle Scholar
- Harris, H. S., Oates, S. C., Staedler, M. M., Tinker, M. T., Jessup, D. A., Harvey, J. T., & Miller, M. A. (2010). Lesions and behavior associated with forced copulation of juvenile Pacific harbor seals (Phoca vitulina richardsi) by southern sea otters (Enhydra lutris nereis). Aquatic Mammals, 36, 331–341.CrossRefGoogle Scholar
- Hof, P. R., Glezer, I. I., Condé, F., Flagg, R. A., Rubin, M. B., Nimchinsky, E. A., & Vogt Weisenhorn, D. M. (1999). Cellular distribution of the calcium-binding proteins parvalbumin, calbindin, and calretinin in the neocortex of mammals: Phylogenetic and developmental patterns. Journal of Chemical Neuroanatomy, 16, 77–116.CrossRefPubMedGoogle Scholar
- Norris, K. S., & Prescott, J. H. (1961). Observations of Pacific cetaceans of California and Mexican waters. University of California Publications in Zoology, 63, 291–402.Google Scholar
- Parkes, C. M. (1972). Bereavement: Studies of grief in adult life. London: Tavistock.Google Scholar
- Pitman, R. L., Deecke, V. B., Gabriele, C. M., Srinivasan, M., Black, N., Denkinger, J., Durban, J. W., Mathews, E. A., Matkin, D. R., Neilson, J. L., Schulman-Janiger, A., Shearwater, D., Stap, P., & Ternullo, R. (2017). Humpback whales interfering when mammal-eating killer whales attack other species: Mobbing behavior and interspecific altruism? Marine Mammal Science, 33, 7–58.CrossRefGoogle Scholar
- Rolls, E. T. (2011). The emotional systems. In J. K. Mai & G. Paxinos (Eds.), The human nervous system (3rd ed., pp. 1328–1350). Amsterdam: Elsevier.Google Scholar
- Shane, S. H. (1994). Pilot whales carrying dead sea lions. Mammalia, 58, 494–498.Google Scholar
- de Waal, F. B. M., & Preston, S. D. (2017). Mammalian empathy: Behavioural manifestations and neural basis. Nature Reviews Neuroscience, 18, 498–509.Google Scholar