Learning and Task Interference by Corpse-removal Specialists in Honey Bee Colonies

Undertakers are considered to be among the most specialized of pre-foraging honey bee (Apis mellifera L.) workers. In this study we examined a possible benefit and a cost of the corpse-rem oval specialty, the improvement in performance with experience, and interference by individuals attempting to perform the same task in the same location, respectively. Experienced bees removed corpses significantly faster than less experienced bees and also were less likely to drop corpses while exiting the hive (5.5% vs. 14.3% of attempts). Superior performance by experienced undertakers might occur as a consequence of learning, or by greater ability from the outset. Because active undertakers (≥ 3 corpse removals) did not improve with experience over their own careers, learning was not demonstrated. An extreme specialist, Yellow 54, removed a total of 114 corpses (33.8% of experimentally introduced dead bees) from the hive over a 13-day period. This is the longest recorded tenure of undertaking to date and demonstrates how a few individuals can dominate this task in a honey bee colony-Yellow 54 removed corpses significantly faster than other active bees, but she demonstrated no obvious improvement in performance over her undertaking career. This suggests the possibility that active undertakers were more talented than less active undertakers, irrespective of learning. When two undertakers worked together to remove a corpse from the hive, they took longer to complete the task than did single individuals. When multiple undertakers flew together from the hive, they were less likely to clear a nearby obstruction than single undertakers and were more likely to drop the corpse within 1 m of the hive. Thus, mutual interference exacted a measurable cost as a result of the undertaking specialization while learning provided few benefits.     

Spatial Aspects of Corpse Removal in the Western Harvester Ant, <Emphasis Type="Italic">Pogonomyrmex occidentalis</Emphasis>

Eusocial insects actively combat pathogen proliferation with a myriad of tactics, one of which is the removal of corpses from the nest, a behavior known as necrophoresis. Spatial patterns of corpse depositions by colonies of the western harvester ant, Pogonomyrmex occidentalis, were examined. Colonies were presented with nestmate and non-nestmate corpses to discern if each type of waste was handled differently. Specialized areas for corpse disposal were not observed. Non-nestmate corpses were carried farther from the nest than were nestmate corpses, perhaps reducing the chance of introduction of pathogens new to the colony that may be harbored by a non-nestmate. Factors external to the nest mound, such as slope and neighboring colonies, had no perceptible effect on these depositions and did not change the uniformity of dispersal of this particular waste. These findings add to our knowledge of the intricacies of corpse removal in eusocial insects and suggest that this is a more dynamic activity than previously thought.     

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.     

Behavioral response of a chimpanzee mother toward her dead infant

The mother-offspring bond is one of the strongest and most essential social bonds. Following is a detailed behavioral report of a female chimpanzee 2 days after her 16-month-old infant died, on the first day that the mother is observed to create distance between her and the corpse. A series of repeated approaches and retreats to and from the body are documented, along with detailed accounts of behaviors directed toward the dead infant by the mother and other group members. The behavior of the mother toward her dead infant not only highlights the maternal contribution to the mother-infant relationship but also elucidates the opportunities chimpanzees have to learn about the sensory cues associated with death, and the implications of death for the social environment.     

Aliens among us: nestmate recognition in the social huntsman spider, Delena cancerides

Unlike all other social spiders, the social huntsman spider, Delena cancerides, has been reported to rapidly respond to non-nestmates with lethal aggression, similar to the behavior of some eusocial insects. We tested for the presence of nestmate recognition in D. cancerides under laboratory conditions by introducing 105 unrelated alien conspecifics into foreign colonies and comparing their behavior to 60 control spiders removed and returned to their natal colony. Spiders demonstrated nestmate recognition by investigating alien spiders far more than nestmates and by resting closer to nestmates than to aliens. Serious attacks or deaths occurred in 23% of all trials; however, aggression was not directed significantly more toward aliens than to nestmates. Most notably, aggression was largely mediated by the adult females (resident or alien), who were most likely to attack or kill other subadult or mature individuals. Young individuals (resident or alien) were largely immune from serious aggression. Spiders recently collected from the field tended to be more aggressive than spiders born and raised in the laboratory, possibly due to blurring of recognition cues related to laboratory husbandry. Our findings support the prediction that nestmate recognition should evolve when there is a benefit to discriminating against non-kin, as in this social spider system where foraging individuals may enter a foreign colony and the colony retreat is a limited resource.     

Demand for Task Performance and Workforce Replacement: Undertakers in Honeybee, Apis mellifera, Colonies

Undertakers are a specialized task group of honey bees that remove dead bees from the colony. The mean adult age of undertakers is 12.5 days; this is similar to that of other specialized task groups, such as guards. The mean number of undertakers in colonies was 544. However, because the number of bees expressing this behavior is dependent on the demand for task performance, undertaker estimates vary depending on the experimental technique. Increasing the demand for undertaking resulted in more bees engaging in the task. Depleting the number of undertakers by removal of bees carrying corpses resulted in new bees assuming undertaking duties. These results support a response-threshold model for engagement of worker bees in task performance.     

秦岭川金丝猴的携带死婴行为

母婴纽带是灵长类社群中最为稳固和重要的社会关系之一,雌性对后代的照料行为是其繁殖投入的一种形式,但雌性对死亡后代的照料不但没有回报,甚至还可能影响其后续繁殖,然而在许多灵长类中却存在母亲对死亡后代的携带和照料行为。本研究于2013年10月至2014年06月采用焦点动物取样法和全事件记录法观察和记录了4例秦岭川金丝猴（Rhinopithecus roxellana）母亲携带和照料死婴行为,以期探讨影响秦岭川金丝猴死婴携带和照料行为的相关因素,为死婴携带和照料行为的相关假说提供数据支持。研究表明携带死婴的雌性均表现出紧张和悲伤的情绪,并存在针对死婴的理毛和嗅吻等行为;死婴的年龄、腐烂与否都不影响雌性携带和照料的时间;出现于交配末期的死婴,雌性对其携带和照料时间变短,这可能有利于雌性进入新的繁殖状态;结合栖息地食物物候和死婴的体重,发现雌性对死婴的携带和照料受到能量成本的限制。     

Near-infrared spectroscopy identifies the colony and nest of origin of weaver ants, <Emphasis Type="Italic">Oecophylla smaragdina</Emphasis>

The ability of social insects to differentiate between colony members and others is essential for the survival of the colony. It enables individuals to direct altruistic behavior towards colony mates, while protecting the colony from intruders. Colonies have a distinct chemical signature that facilitates colony-mate recognition. However, in large polydomous colonies, this signal is likely to be modified by factors unique to each nest. We demonstrate, using near-infrared spectroscopy (NIRS), that individual weaver ants, Oecophylla smaragdina, can be differentiated with respect to their colony and nest of origin. 76.5% of individuals from four colonies could be correctly assigned to their colony of origin; and 79.6% of individuals could be assigned to the correct nest (of two) within their colony. Despite the differences between nests within colonies, in most cases individuals from one nest were more similar to individuals from the other nest within the colony than they were to individuals from any nest outside the colony. Therefore, a distinctive colony identity is maintained despite differences between nests within colonies. We discuss the advantages of using NIRS as a faster and less expensive alternative to the analysis of cuticular hydrocarbons following extraction and identification with gas chromatography/mass spectroscopy. Received 26 November 2007; revised 22 January 2008; accepted 25 January 2008.     

Colony fusion in a termite: What makes the society "open"?

Summary. Sociobiological theories assume that insect societies are closed, i.e., members always act aggressively toward alien conspecific individuals. However, introduction of non-nestmate workers into a host colony of a lower termite, Reticulitermes speratus revealed various levels of agonism: from genocide to colony fusion. Members of the host colony attacked and killed the intruders having a higher nymph ratio (the number of nymphs/the number of workers) than the host colony had. In contrast, the intruders were accepted if they had a lower nymph ratio than the host colony. Acceptance of a lower-nymph-ratio colony could be beneficial for the host colony because it would gain additional labor force to feed its own nymphs. However, acceptance of a higher-nymph-ratio colony might be disadvantageous because the workers must rear non-relative nymphs additionally. Here we show that termites facultatively change their agonistic response toward non-nestmates according to the cost and benefit of colony fusion. Contrary to the existent concept, we report for the first time that colony fusion is an adaptive tactic in social insects.     

Behavioural response of Lucilia sericata to a decaying body infested by necrophagous insects

Numerous insect species are necrophagous, with Dipterans and Coleopterans being the most abundant on a corpse. Whether the presence of necrophageous species on a corpse affects the attraction of adult blowflies to the corpse is sparsely studied. We test the hypothesis that Lucilia sericata can discriminate the odour of a noncolonized cadaver from the odour of a cadaver on which conspecific and/or heterospecific necrophagous insects are feeding. The volatile organic compounds are collected from decomposing rats under four modalities: (i) in the absence of insects; (ii) in the presence of L. sericata adults; (iii) in the presence of Dermestes frischii adults; (iv) and in the presence of both D. frischii adults and L. sericata adults. During a multiple‐choice bioassay, blowflies are exposed to the four odour samples, and are shown to prefer the odour of a corpse where conspecific larvae are present. We also expect blowflies to avoid cadavers on which predators where present, although L. sericata are not repulsed by the odour of a cadaver colonized by hide beetles. We then compare the average quantities of all 61 volatile molecules identified, finding that the presence of necrophagous insects impacts some of them. However, none of the volatile organic compounds previously reported in the literature as being attractive for L. sericata adults are impacted by the presence of necrophagous insects. The results of the present study suggest that blowfly larvae modify the volatilome of a corpse, enabling adults to discriminate a colonized from a noncolonized corpse.     

Keep the nest clean: survival advantages of corpse removal in ants

Sociality increases exposure to pathogens. Therefore, social insects have developed a wide range of behavioural defences, known as ‘social immunity’. However, the benefits of these behaviours in terms of colony survival have been scarcely investigated. We tested the survival advantage of prophylaxis, i.e. corpse removal, in ants. Over 50 days, we compared the survival of ants in colonies that were free to remove corpses with those that were restricted in their corpse removal. From Day 8 onwards, the survival of adult workers was significantly higher in colonies that were allowed to remove corpses normally. Overall, larvae survived better than adults, but were slightly affected by the presence of corpses in the nest. When removal was restricted, ants removed as many corpses as they could and moved the remaining corpses away from brood, typically to the nest corners. These results show the importance of nest maintenance and prophylactic behaviour in social insects.     

Nestmate discrimination in ants: effect of bioassay on aggressive behavior

Summary: Aggression assays are commonly used to study nestmate recognition in social insects. Methods range from detailed behavioral observations on small numbers of insects to counts of individuals fighting in group interactions. These assays vary in the equipment used and the intensity and duration of observations. We used the Argentine ant, Linepithema humile, to compare four aggression bioassays for consistency between replicates, similarity between assays, and ability to predict whole colony interactions. The assays included were 1 live – 1 dead ant interactions, live 1-1 battles, live 5-5 battles, and 1 ant introduced to a foreign colony. We tested six ant colonies in all pairwise combinations using four different assays and two to three scoring methods per assay. We also conducted a colony merging experiment to see which assays were capable of predicting this ecologically important event. We found that scoring methods within assays yielded very similar results, giving us no reason to favor observationally intense procedures, such as continuous scanning, over less observationally intense systems, such as snapshot surveys. Assays differed greatly in their consistency between replicates. No two replicates of the 1 live – 1 dead assay were significantly correlated. The live 5-5 and the colony introduction assays were the most consistent across replicates. The mean scores of the live 1-1, live 5-5 and colony introduction assays were all significantly correlated with each other; only the live 5-5 assay was significantly correlated with the 1 live – 1 dead assay. Assays that utilized the greatest number of live ants were the most likely to reveal high levels of aggression. The aggression scores of all but the 1 live – 1 dead assay were positively correlated with the number of ants that died during whole colony encounters and negatively associated with colony merging. We conclude that all live ant assays tested are useful tools for analyzing aggressive interactions between colonies, but that the pairing of a live and dead ant produced inconsistent results and generally lower levels of aggression. We found relatively low consistency between trials using the live 1-1 assay, but found that with sufficient replication its results were highly correlated with the assays using more interacting ants. We suggest that isolated aggressive acts in assays do not necessarily predict whole colony interactions: some colonies that fought in bioassays merged when the entire colonies were allowed to interact.     

Prey size,prey perishability and group foraging in a social spider

Summary Selection might favor group foraging and social feeding when prey are distributed in patches that do not last long enough for a solitary individual to consume more than a small fraction of them (Pulliam and Millikan 1982; Pulliam and Caraco 1984). Here we considered the foraging behavior of a social spider, Anelosimus eximius, in light of this ephemeral resource hypothesis. This species builds large webs in which members cooperate to capture a wide variety of different sizes and types of prey, many of which are very large. The capture success of this species was very high across all prey sizes, presumably due to the fact that they foraged in groups. Group consumption times in natural colonies for all prey larger than five mm were less than the time that dead insects remained on the plastic sheets that we used as artificial webs. Solitary consumption estimates, calculated from the rate at which laboratory individuals extracted insect biomass while feeding, were the same as the residence times of insects on artificial webs in the field for insects between 6 and 15 mm in length and were significantly longer than the persistence of insects on plastic sheets for all larger insects. Large prey, that contribute substantially to colony energy supplies, appeared to be ephemeral resources for these spiders that could not be consumed by a single spider in the time they were available. These factors made the food intake of one spider in a group less sensitive to scavenging by others and could act to reinforce the social system of this species.     

Kin recognition in social bees

Kin recognition in social insects has become a central issue in sociobiology because studies of the recognition abilities of social insects provide a test of kin selection theory. W.D. Hamilton(1) formalized kin selection theory by showing how individuals can gain fitness by increasing the reproductive output of relatives (kin). The social interactions of individuals, or groups, should be influenced by the genetic structure of the population. The ability to recognize kin can increase the adaptive value of social behavior by modulating it according to genetic relationship. From this, the specific prediction emerges: if individuals can distinguish among others with which they interact on the basis of the degree to which they are related, then behavior should be biased preferentially toward more closely related reproductive individuals.     

Complex undertaking behavior in <Emphasis Type="Italic">Temnothorax lichtensteini</Emphasis> ant colonies: from corpse-burying behavior to necrophoric behavior

Removal of dead bodies is considered an essential act in social behavior. Here we show that in Temnothorax lichtensteini (formerly Leptothorax), the reaction to the presence of a corpse within the nest is more complex than previously hypothesized. Depending on the nature of the corpse, we observe not only necrophoric behavior but also corpse-burying behavior and the alternation of these two behaviors. Alien but newly dead-corpses were buried, while old sister-corpses were transported outside the nest. Numerous other situations studied produce mixed results and contradictory behaviors, indicating behavioral plasticity. Thus, T. lichtensteini workers discriminate alien corpses from nestmate corpses, and old corpses from new corpses. The individual and/or collective characteristics of the behavioral decisions are discussed in the light of our results.     

Pupal developmental temperature and behavioral specialization of honeybee workers (<Emphasis Type="Italic">Apis mellifera</Emphasis> L.)

Honeybees (Apis mellifera) are able to regulate the brood nest temperatures within a narrow range between 32 and 36°C. Yet this small variation in brood temperature is sufficient to cause significant differences in the behavior of adult bees. To study the consequences of variation in pupal developmental temperature we raised honeybee brood under controlled temperature conditions (32, 34.5, 36°C) and individually marked more than 4,400 bees, after emergence. We analyzed dancing, undertaking behavior, the age of first foraging flight, and forager task specialization of these workers. Animals raised under higher temperatures showed an increased probability to dance, foraged earlier in life, and were more often engaged in undertaking. Since the temperature profile in the brood nest may be an emergent property of the whole colony, we discuss how pupal developmental temperature can affect the overall organization of division of labor among the individuals in a self-organized process.     

Relatedness and Social Behaviors in <Emphasis Type="Italic">Cercopithecus solatus</Emphasis>

Inclusive fitness and kin selection theories predict that organisms will evolve biased behavior toward kin when the inclusive fitness benefits outweigh the costs of such behaviors. Researchers have long observed that primates bias their behavior toward relatives, particularly maternal kin. We examined the effect of kinship on social behaviors in a semifree-ranging colony of Cercopithecus solatus, a poorly studied forest guenon species. We used microsatellite loci and paternity analyses to determine the degree of relatedness between individuals, as well as kinship. Individuals biased some of their behavior according to relatedness. Specifically, related individuals are more spatially associated and less aggressive toward each other. When we replaced the relatedness coefficients with defined kin categories, Cercopithecus solatus seemed to behave preferentially toward maternal kin versus paternal kin. Even though the setting of the colony and the small sample size limit our conclusions, we discuss the potential implications of our finding for the study of the impact of kin selection in primate social relationships.     

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.     

Fitness in invasive social wasps: the role of variation in viral load,immune response and paternity in predicting nest size and reproductive output

Within any one habitat, the relative fitness of organisms in a population can vary substantially. Social insects like the common wasp are among the most successful invasive animals, but show enormous variation in nest size and other fitness‐related traits. Some of this variation may be caused by pathogens such as viruses that can have serious consequences in social insects, which range from reduced productivity to colony death. Both individual immune responses and colony‐level traits such as genetic diversity are likely to influence effects of pathogen infections on colony fitness. Here we investigate how infections with Kashmir Bee Virus (KBV), immune response and intracolony genetic diversity (due to queen polyandry) affect nest size in the invasive common wasp Vespula vulgaris. We show that KBV is highly prevalent in wasps and expression of antiviral immune genes is significantly increased with higher viral loads across individuals. Patriline membership within a nest did not influence KBV susceptibility or immune response. A permutational MANCOVA revealed that polyandry, viral load and expression of the immune gene Dicer were significant predictors of variation in nest size. High intracolony genetic diversity due to polyandry has previously been hypothesized to improve colony‐level resistance to parasites and pathogens. Consistent with this hypothesis, we observed genetically diverse colonies to be significantly larger and to produce more queens, although this effect was not driven by the pathogen we investigated. Invasive wasps clearly suffer from pathogens and expend resources, as indicated here by elevated immune gene expression, toward reducing pathogen‐impact on colony fitness.