Death among geladas (Theropithecus gelada): a broader perspective on mummified infants and primate thanatology

Despite intensive study in humans, responses to dying and death have been a neglected area of research in other social mammals, including nonhuman primates. Two recent reports [Anderson JR, Gillies A, Lock LC. 2010. Pan thanatology. Current Biology 20:R349–R351; Biro D, Humle T, Koops K, Souse C, Hayashi M, Matsuzawa T. 2010. Chimpanzee mothers at Bossou, Guinea carry the mummified remains of their dead infants. Current Biology 20:R351–R352] offered exciting new insights into behavior toward dying and dead conspecifics in our closest living relatives—chimpanzees. Here, we provide a comparative perspective on primate thanatology using observations from a more distant human relative—gelada monkeys (Theropithecus gelada)—and discuss how gelada reactions to dead and dying groupmates differ from those recently reported for chimpanzees. Over a 3.75‐year study period, we observed 14 female geladas at Guassa, Ethiopia carrying dead infants from 1 hr to ≥48 days after death. Dead infants were carried by their mothers, other females in their group, and even by females belonging to other groups. Like other primate populations in which extended (>10 days) infant carrying after death has been reported, geladas at Guassa experience an extreme climate for primates, creating conditions which may favor slower rates of decomposition of dead individuals. We also witnessed the events leading up to the deaths of two individuals and the responses by groupmates to these dying individuals. Our results suggest that while chimpanzee mothers are not unique among primates in carrying their dead infants for long periods, seemingly “compassionate” caretaking behavior toward dying groupmates may be unique to chimpanzees among nonhuman primates (though it remains unknown whether such “compassionate” behavior occurs outside captivity). Am. J. Primatol. 73:405–409, 2011. © 2010 Wiley‐Liss, Inc.     

alpha-Amylase and programmed cell death in aleurone of ripening wheat grains

Late maturity alpha-amylase (LMA) in wheat is a genetic defect that may result in the accumulation of unacceptable levels of high pI alpha-amylase in grain in the absence of germination or weather damage. During germination, gibberellin produced in the embryo triggers expression of alpha-Amy genes, the synthesis of alpha-amylase and, subsequently, cell death in the aleurone. LMA also involves the aleurone and whilst LMA appears to be independent of the embryo there is nevertheless some evidence that gibberellin is involved. The aim of this investigation was to determine whether the increase in alpha-amylase activity in LMA-prone genotypes, like alpha-amylase synthesis by aleurone cells in germinating or GA-challenged grains, is followed by aleurone cell death. Programmed cell death was seen in aleurone layers from developing, ripe and germinated grains using confocal microscopy and fluorescent probes specific for dead or living cells. Small pockets of dying cells were observed distributed at random throughout the aleurone of ripening LMA-affected grains and by harvest-ripeness these cells were clearly dead. The first appearance of dying cells, 35 d post-anthesis, coincided with the later part of the 'window of sensitivity' in grain development in LMA-prone wheat cultivars. No dead or dying cells were present in ripening or fully ripe grains of control cultivars. In germinating grains, dying cells were observed in the aleurone adjacent to the scutellum and, as germination progressed, the number of dead cells increased and the affected area extended further towards the distal end of the grain. Aside from the obvious differences in spatial distribution, dying cells in 20-24 h germinated grains were similar to dying cells in developing LMA-affected grains, consistent with previous measurements of alpha-amylase activity. The increase in high pI alpha-amylase activity in developing grains of LMA-prone cultivars, like alpha-amylase synthesis in germinating grains, is associated with cell death, providing further evidence for the involvement of gibberellin in the LMA response.     

Death among primates: a critical review of non‐human primate interactions towards their dead and dying

For the past two centuries, non‐human primates have been reported to inspect, protect, retrieve, carry or drag the dead bodies of their conspecifics and, for nearly the same amount of time, sparse scientific attention has been paid to such behaviours. Given that there exists a considerable gap in the fossil and archaeological record concerning how early hominins might have interacted with their dead, extant primates may provide valuable insight into how and in which contexts thanatological behaviours would have occurred. First, we outline a comprehensive history of comparative thanatology in non‐human primates, from the earliest accounts to the present, uncovering the interpretations of previous researchers and their contributions to the field of primate thanatology. Many of the typical behavioural patterns towards the dead seen in the past are consistent with those observed today. Second, we review recent evidence of thanatological responses and organise it into distinct terminologies: direct interactions (physical contact with the corpse) and secondary interactions (guarding the corpse, vigils and visitations). Third, we provide a critical evaluation regarding the form and function of the behavioural and emotional aspects of these responses towards infants and adults, also comparing them with non‐conspecifics. We suggest that thanatological interactions: promote a faster re‐categorisation from living to dead, decrease costly vigilant/caregiving behaviours, are crucial to the management of grieving responses, update position in the group's hierarchy, and accelerate the formation of new social bonds. Fourth, we propose an integrated model of Life‐Death Awareness, whereupon neural circuitry dedicated towards detecting life, i.e. the agency system (animate agency, intentional agency, mentalistic agency) works with a corresponding system that interacts with it on a decision‐making level (animate/inanimate distinction, living/dead discrimination, death awareness). Theoretically, both systems are governed by specific cognitive mechanisms (perceptual categories, associative concepts and high‐order reasoning, respectively). Fifth, we present an evolutionary timeline from rudimentary thanatological responses likely occurring in earlier non‐human primates during the Eocene to the more elaborate mortuary practices attributed to genus Homo throughout the Pleistocene. Finally, we discuss the importance of detailed reports on primate thanatology and propose several empirical avenues to shed further light on this topic. This review expands and builds upon previous attempts to evaluate the body of knowledge on this subject, providing an integrative perspective and bringing together different fields of research to detail the evolutionary, sensory/cognitive, developmental and historical/archaeological aspects of primate thanatology. Considering all these findings and given their cognitive abilities, we argue that non‐human primates are capable of an implicit awareness of death.     

The causes of perinatal death induced by prenatal exposure of rats to the pesticide, mirex. Part I: Pre-parturition observations of the cardiovascular system

Prenatal exposure to mirex, a chlorinated hydrocarbon insecticide, induces a high rate of perinatal death, but only a low incidence of visible abnormalities which could help to account for these deaths. This study is an attempt to determine the cause of these deaths. Pregnant rats were intubated with a moderate dose of mirex, in oil, 6 mg/kg/day, on days 8 1/2-15 1/2 of gestation. Observations, on 78 control and 136 treated fetuses, were made on the morning before parturition was expected. Fetuses were sequentially exposed and electrocardiograms obtained with the fetus attached to the placenta and uterus. ECGs were evaluated for rate of beat, regularity of beat, PR intervals, and other features. Fetuses were examined for edema level and vitality. None of the controls were dead and none had abnormal ECGs. Of the treated group, 14% were dead, 16% had a first-degree heart block, and 2% had a second-degree heart block. Some (6%) had slow, feeble atrial beats only, possibly a third-degree block, and appeared to be dying. The severity of the symptoms was proportional to the degree of visible edema. Most of the fetuses with little or no visible edema had normal ECGs, but the majority of the moderate to severely edematous fetuses (i.e., with a layer of subcutaneous edema across the back of 0.5 mm or more) had abnormal ECGs and/or were either dead or dying. These data show that the effects of mirex on the fetal cardiovascular system are a major factor in inducing prenatal death.     

From regulation of dying cell engulfment to development of anti-cancer therapy

Cell death and efficient engulfment of dying cells ensure tissue homeostasis and is involved in pathogenesis. Clearance of dying cells is a complex and dynamic process coordinated by interplay between ligands on dying cell, bridging molecules, and receptors on engulfing cells. In this review, we will discuss recent advances and significance of molecular changes on the surface of dying cells implicated in their recognition and clearance as well as factors released by dying cells that attract macrophages to the site of cell death. It is now becoming apparent that phagocytes use a specific set of mechanisms to discriminate between live and dead cells, and this phenomenon will be illustrated here. Next, we will discuss potential mechanisms by which removal of dying cells could modulate immune responses of phagocytes, in particular of macrophages. Finally, we will address possible strategies for manipulating the immunogenicity of dying cells in experimental cancer therapies.     

Maternal responses to dead and dying infants in wild troops of ring-tailed lemurs at the Berenty Reserve,Madagascar

We describe responses of seven mothers and other troop members to dead and dying infants in several troops of ring-tailed lemurs(Lemur catta) at the Berenty Reserve, Madagascar. In contrast to mothers in simian species, ring-tailed lemur mothers rarely carried their dying, immobile or dead infants. However, they sniffed, licked, and touched them even after they had died. While the dying infants were still peeping, their mothers remained near them, and 15 to 76 min after the infants ceased to peep, they were left by their mothers. Six of the seven mothers returned to their dead infants several times within the first few hours after they had left them. All seven mothers gave repeated calls, such as “mew” and “pyaa,” when they were separated from either their dead infants or other troop members or both. Thus, each mother exhibited some form of maternal behavior toward her dead infant for hours after its death. These results indicate that there may not be a great gap in terms of maternal affection between simian and prosimian mothers. We also discuss visuospatial memory ability in ring-tailed lemurs and the causes of the infants’ deaths.     

Enabling more dying people to remain at home.

When it comes to dying there is no place like home. Since earliest times most cultures have accepted that dying people should remain at home. But this was never possible for all. Some were destined to die in accidents, on battlefields, by execution, and from catastrophic illness, maybe many miles away. Nevertheless, with few exceptions people could expect to die in their own beds and in the bosom of their families. In Europe from the Middle Ages until a century ago there was a simplicity about dying. Aware that the end was approaching, people would take to their sickbeds and preside over the ritual. The family, including children, friends, and neighbours would congregate. The ceremony was public and doctors often complained about overcrowding. Death was not regarded as a frightening event and was accepted as an inevitable and integral part of life. Dramatic changes in attitudes to death have taken place since the mid-nineteenth century. The natural acceptance of a biological reality has been lost and people are now unable to come to terms with their own mortality. One consequence is that death has become institutionalised. This paper seeks to answer five questions. These refer to where people die, where they would choose to die, where they spend their last year of life, the reasons for admission for terminal care, and whether more dying people could remain at home. Discussion is restricted to adults in the United Kingdom. References are mostly from the past decade.     

Cyclosporin A potentiates the cytotoxic effects of methyl methanesulphonate in HL-60 and K562 cells

Methyl methanesulphonate (MMS) is a DNA damaging agent, which induces oxidative stress, ATP depletion, and consequently, cell death, in HL-60 and K562 cells. The cell death induced by MMS predominantly exhibited the morphological and biochemical hallmarks of necrosis. A minor population of dying cells exhibited apoptotic hallmarks, especially in K562 cell cultures. Cyclosporin A (CsA) was used to modulate the MMS-induced cell death. Our results indicated that CsA did not prevent cells from dying, but changed the mode of death from necrotic to apoptotic. Surprisingly, CsA enhanced oxidative stress and increased the overall number of dead cells. Based on these results, we conclude that the modulatory effect of CsA on MMS-induced cell death might arise from an interference by CsA with mitochondrial metabolism, rather than from inhibition of the MMS efflux mediated by P-glycoprotein.     

Hepatic cell division and tissue repair: a key to survival after liver injury

The survival of patients suffering from severe liver damage depends heavily on the ability of the remaining hepatocytes to regenerate and replace the dead or dying cells; death usually occurs when the regenerating ability of the liver is compromised owing to heavy damage to the liver. The current approach to therapy aims only to block additional liver injury from hepatotoxicants or hepatic disease. It hepatocellular regeneration and tissue repair could be stimulated after hepatic damage by a therapeutically compatible mechanism, then it might be possible to prevent death arising from serious liver injury.     

Cell death (apoptosis) in hair follicles and consequent changes in the width of hairs after irradiation of growing follicles

Irradiation of anagen (growing) hair follicles results in a dose-dependent increase in the number of histologically identifiable fragments of dead cells (apoptotic fragments). The incidence of apoptotic fragments is linearly related to dose, increasing at a rate of 2.92 fragments per follicle section per Gy. The effects of doses of 0.2 Gy can be easily detected. Subjective attempts to associate clusters of fragments with dead or dying cells suggests that the number of fragments per cell increases with dose (about 1.7 fragments per cell after 1 Gy to about 2.7 fragments per cell after 5 Gy). There is a natural incidence of cell death in controls (0.13 +/- 0.06 fragments per follicle section with about 1.4 fragments per dead or dying cell). Damage to the follicle cells is expressed in the differentiated product of the follicle, the hair, by a reduction in width. This is probably the cellular basis for the production of dysplastic hairs. The hair width has been measured and is reduced by about 7 per cent for every gray of radiation. The value of the hair and hair follicles as potential biological dosimeters is discussed.     

Cell death and the regulation of populations of cells in the periodontal ligament

Summary The contribution of cell death in regulating cellular populations of periodontal ligament was studied in young adult rats. Mandibular first molar periodontium was prepared for light-microscopic radioautography after a pulse of ³H-thymidine in 6 rats and for electron microscopy in 4 rats. The labeling index for ³H-thymidine and the density of fibroblast-like cells were computed from radioautographs. The percentages of dying or dead cells and macrophages were computed from electron micrographs. The labeling index of cells within 20 m of bone and cementum was significantly lower (p<0.01) than the labeling index within the body of the periodontal ligament. The patterns of cellular density and indices of death were the inverse of the labeling indices. Macrophages were plentiful (% macrophages = 3.68%±0.30) and were clustered around blood vessels (mean distance from blood vessel=2.3 m). However, only 10% of dying or dead cells were within 10 m of blood vessels. These data show that death of cells in the periodontal ligament may, in part, balance production of cells by mitosis. The relationships between labeling index, index of death, and cellular density suggest that cells born in the middle of the periodontal ligament may migrate to regions of high cellular density near bone and cementum, and that they may die there. Macrophages do not appear to be associated with dying cells of the periodontal ligament.     

Collared peccary (Pecari tajacu) behavioral reactions toward a dead member of the herd

Humans, elephants, chimpanzees, and cetaceans show concern with the death of other members of their species and respond to death in particular ways. Science considers that these species are exceptions and that other mammal species show little or no reaction to the dead bodies of individuals of their species. Collared peccaries (Pecari tajacu; Tayassuidae) are social animals that live in groups of 5–50 individuals maintaining close and complex social relationships. The collared peccary occupies many different environments and it is widely distributed from the south of North America to the north of Argentina. Their behavior is well studied, but we know little about their behavior toward the dead. We directly observed and filmed with a camera trap the reactions of a five‐member herd of collared peccaries to the death of a herd member. We worked on a suburban forested area in the mountains of central Arizona. We found that the herd visited and spent time with the dead body for 10 days after the peccary died. The frequency of the visits declined until the cadaver was consumed by coyotes. Most of the videos showed two individuals visited the dead animal (44%), solitary records were also frequent (39%) and only 4% of the videos recorded three peccaries. Visits were more frequent during the night (64%). Peccaries do react to the death of a herd member by behaving in particular ways. Reactions include pushing at the dead individual, staring at it, biting it, and trying to pick it up by putting their snout under the corpse and pushing it up, and defending it from coyotes, among others. These levels of behavioral complexity for peccaries are beyond those known so far. The behaviors of this herd of peccaries resemble those of humans, cetaceans, chimpanzees, and elephants and show that these groups are not the only ones that react to death.     

What do we owe the newly dead? An ethical analysis of findings from Japan's corpse hotels workers

While people are still alive, we owe them respect. Yet what, if anything, do we owe the newly dead? This question is an urgent practical concern for aged societies, because older people die at higher rates than any other age group. One novel way in which Japan, the frontrunner of aged societies, meets its need to accommodate high numbers of newly dead is itai hoteru or corpse hotels. Itai hoteru offer families a way to wait for space in over‐crowded crematoriums while affording an environment conducive to grieving. Drawing on conversations with itai hoteru employees, we delineate the values this contemporary death practice expresses and show how these values comprise part of the broader idea of a good death. A good death implies duties on both sides of death's divide: to both the dying and the newly dead.     

Pan thanatology

Chimpanzees' immediate responses to the death of a group-member have rarely been described. Exceptions include maternal care towards dead infants, and frenzied excitement and alarm following the sudden, traumatic deaths of older individuals [1-5]. Some wild chimpanzees die in their night nest [6], but the immediate effect this has on others is totally unknown. Here, with supporting video material, we describe the peaceful demise of an elderly female in the midst of her group. Group responses include pre-death care of the female, close inspection and testing for signs of life at the moment of death, male aggression towards the corpse, all-night attendance by the deceased's adult daughter, cleaning the corpse, and later avoidance of the place where death occurred. Without death-related symbols or rituals, chimpanzees show several behaviours that recall human responses to the death of a close relative.     

A blast from the past: clearance of apoptotic cells regulates immune responses

Apoptosis, which is a programmed and physiological form of cell death, is known to shape the immune system by regulating populations of effector lymphocytes. However, the binding and ingestion of dying cells by monocytes/macrophages and dendritic cells can also influence immune responses markedly by enhancing or suppressing inflammation. Therefore, dead cells, which are a reflection of an organism's immediate past, can control its immunological future.     

Frequency,Magnitude, and Possible Causes of Stranding and Mass-Mortality Events of the Beach Clam Tivela mactroides (Bivalvia: Veneridae)

Stranding combined with mass-mortality events of sandy-beach organisms is a frequent but little-understood phenomenon, which is generally studied based on discrete episodes. The frequency, magnitude, and possible causes of stranding and mass-mortality events of the trigonal clam Tivela mactroides were assessed based on censuses of stranded individuals, every four days from September 2007 through December 2008, in Caraguatatuba Bay, southeastern Brazil. Stranded clams were classified as dying (closed valves did not open when forced) or dead (closed valves were easily opened). Information on wave parameters and the living intertidal clam population was used to assess possible causes of stranding. This fine-scale monitoring showed that stranding occurred widely along the shore and year-round, with peaks interspersed with periods of low or no mortality. Dead clams showed higher mean density than dying individuals, but a lower mean shell length, attributed to a higher tolerance to desiccation of larger individuals. Wave height had a significant negative relationship to the density of dying individuals, presumed to be due to the accretive nature of low-energy waves: when digging out, clams would be more prone to be carried upward and unable to return; while larger waves, breaking farther from the beach and with a stronger backwash, would prevent stranding in the uppermost areas. This ecological finding highlights the need for refined temporal studies on mortality events, in order to understand them more clearly. Last, the similar size structure of stranded clams and the living population indicated that the stranded individuals are from the intertidal or shallow subtidal zone, and reinforces the ecological and behavioral components of this process, which have important ecological and socioeconomic implications for the management of this population.