Honey Bee Inhibitory Signaling Is Tuned to Threat Severity and Can Act as a Colony Alarm Signal

Alarm communication is a key adaptation that helps social groups resist predation and rally defenses. In Asia, the world’s largest hornet, Vespa mandarinia, and the smaller hornet, Vespa velutina, prey upon foragers and nests of the Asian honey bee, Apis cerana. We attacked foragers and colony nest entrances with these predators and provide the first evidence, in social insects, of an alarm signal that encodes graded danger and attack context. We show that, like Apis mellifera, A. cerana possesses a vibrational “stop signal,” which can be triggered by predator attacks upon foragers and inhibits waggle dancing. Large hornet attacks were more dangerous and resulted in higher bee mortality. Per attack at the colony level, large hornets elicited more stop signals than small hornets. Unexpectedly, stop signals elicited by large hornets (SS _{large hornet}) had a significantly higher vibrational fundamental frequency than those elicited by small hornets (SS _{small hornet}) and were more effective at inhibiting waggle dancing. Stop signals resulting from attacks upon the nest entrance (SS _nest) were produced by foragers and guards and were significantly longer in pulse duration than stop signals elicited by attacks upon foragers (SS _forager). Unlike SS _forager, SS _nest were targeted at dancing and non-dancing foragers and had the common effect, tuned to hornet threat level, of inhibiting bee departures from the safe interior of the nest. Meanwhile, nest defenders were triggered by the bee alarm pheromone and live hornet presence to heat-ball the hornet. In A. cerana, sophisticated recruitment communication that encodes food location, the waggle dance, is therefore matched with an inhibitory/alarm signal that encodes information about the context of danger and its threat level.     

A Comparison of Social Organization in Asian Elephants and African Savannah Elephants

Asian and African elephant species have diverged by ca. 6 million years, but as large, generalist herbivores they occupy similar niches in their respective environments. Although the multilevel, hierarchical nature of African savannah elephant societies is well established, it has been unclear whether Asian elephants behave similarly. Here we quantitatively compare the structure of both species’ societies using association data collected using the same protocol over similar time periods. Sociality in both species demonstrates well-defined structure, but in contrast to the African elephants of Samburu the Uda Walawe Asian elephants are found in smaller groups, do not maintain coherent core groups, demonstrate markedly less social connectivity at the population level, and are socially less influenced by seasonal differences in ecological conditions. The Uda Walawe Asian elephants, however, do maintain a complex, well-networked society consisting of ≥2 differentiated types of associates we term ephemeral and long-term affiliates. These findings imply we must broaden our recognition of multilevel social organization to encompass societies that fall along a gradient of nestedness, and not merely those that exhibit hierarchical nesting. This in turn suggests that multilevel structures may be more diverse and widespread than generally thought, and that phylogenetic comparisons within species-rich clades, such as that of primates, using the methods presented can provide fresh insights into their socioecological basis.     

Response of African Elephants (Loxodonta africana) to Seasonal Changes in Rainfall

The factors that trigger sudden, seasonal movements of elephants are uncertain. We hypothesized that savannah elephant movements at the end of the dry season may be a response to their detection of distant thunderstorms. Nine elephants carrying Global Positioning System (GPS) receivers were tracked over seven years in the extremely dry and rugged region of northwestern Namibia. The transition date from dry to wet season conditions was determined annually from surface- and satellite-derived rainfall. The distance, location, and timing of rain events relative to the elephants were determined using the Tropical Rainfall Measurement Mission (TRMM) satellite precipitation observations. Behavioral Change Point Analysis (BCPA) was applied to four of these seven years demonstrating a response in movement of these elephants to intra- and inter-seasonal occurrences of rainfall. Statistically significant changes in movement were found prior to or near the time of onset of the wet season and before the occurrence of wet episodes within the dry season, although the characteristics of the movement changes are not consistent between elephants and years. Elephants in overlapping ranges, but following separate tracks, exhibited statistically valid non-random near-simultaneous changes in movements when rainfall was occurring more than 100 km from their location. While the environmental trigger that causes these excursions remains uncertain, rain-system generated infrasound, which can travel such distances and be detected by elephants, is a possible trigger for such changes in movement.     

Chimpanzee Alarm Call Production Meets Key Criteria for Intentionality

Determining the intentionality of primate communication is critical to understanding the evolution of human language. Although intentional signalling has been claimed for some great ape gestural signals, comparable evidence is currently lacking for their vocal signals. We presented wild chimpanzees with a python model and found that two of three alarm call types exhibited characteristics previously used to argue for intentionality in gestural communication. These alarm calls were: (i) socially directed and given to the arrival of friends, (ii) associated with visual monitoring of the audience and gaze alternations, and (iii) goal directed, as calling only stopped when recipients were safe from the predator. Our results demonstrate that certain vocalisations of our closest living relatives qualify as intentional signals, in a directly comparable way to many great ape gestures. We conclude that our results undermine a central argument of gestural theories of language evolution and instead support a multimodal origin of human language.     

Orchid Mimics Honey Bee Alarm Pheromone in Order to Attract Hornets for Pollination

Approximately one-third of the world's estimated 30,000 orchid species are deceptive and do not reward their pollinators with nectar or pollen [1]. Most of these deceptive orchids imitate the scent of rewarding flowers or potential mates [2] and [3]. In this study, we investigated the floral scent involved in pollinator attraction to the rewardless orchid Dendrobium sinense, a species endemic to the Chinese island Hainan that is pollinated by the hornet Vespa bicolor. Via chemical analyses and electrophysiological methods, we demonstrate that the flowers of D. sinense produce (Z)-11-eicosen-1-ol and that the pollinator can smell this compound. This is a major compound in the alarm pheromones of both Asian (Apis cerana) and European (Apis mellifera) honey bees [4] and [5] and is also exploited by the European beewolf (Philanthus triangulum) to locate its prey [6]. This is the first time that (Z)-11-eicosen-1-ol has been identified as a floral volatile. In behavioral experiments, we demonstrate that the floral scent of D. sinense and synthetic (Z)-11-eicosen-1-ol are both attractive to hornets. Because hornets frequently capture honey bees to feed to their larvae, we suggest that the flowers of D. sinense mimic the alarm pheromone of honey bees in order to attract prey-hunting hornets for pollination.     

African Elephants Adjust Speed in Response to Surface-Water Constraint on Foraging during the Dry-Season

Most organisms need to acquire various resources to survive and reproduce. Individuals should adjust their behavior to make optimal use of the landscape and limit the costs of trade-offs emerging from the use of these resources. Here we study how African elephants Loxodonta africana travel to foraging places between regular visits to waterholes. Elephant herds were tracked using GPS collars during two consecutive dry seasons in Hwange National Park, Zimbabwe. We segmented each individual movement track at each visit to water to define foraging trips, and then used trip-level statistics to build an understanding of movement strategies. Travel speed within these individually-consistent movement bouts was also analyzed to understand if speed was better linked to distance to water or progression in the trip over time. We found that elephants went further from water when drinking less often, which could result from a trade-off between drinking and foraging in less depleted, far from water, places. Speed increased towards the beginning and the end of the trips, and was also greater than observed during the wet season, suggesting that elephants were trying to save time. Numerous short trips traveled at greater speed, particularly when commuting to a different waterhole, was tentatively explained by the inability to drink at specific waterholes due to intra-specific interference. Unexpectedly elephants did not always minimize travel time by drinking at the closest waterhole, but the extra distance traveled remained never more than a few kilometers. Our results show how individuals may adjust movement behavior to deal with resource trade-offs at the landscape scale. We also highlight how behavioral context, here progression in the trip, may be more important than spatial context, here distance to water, in explaining animal movement patterns.     

Elephants in space and time

Autocorrelation in animal movements can be both a serious nuisance to analysis and a source of valuable information about the scale and patterns of animal behavior, depending on the question and the techniques employed. In this paper we present an approach to analyzing the patterns of autocorrelation in animal movements that provides a detailed picture of seasonal variability in the scale and patterns of movement. We used a combination of moving window Mantel correlograms, surface correlation and crosscorrelation analysis to investigate the scales and patterns of autocorrelation in the movements of three herds of elephants in northern Botswana. Patterns of autocorrelation of elephant movements were long‐range, temporally complicated, seasonally variable, and closely linked with the onset of rainfall events. Specifically, for the three elephant herds monitored there was often significant autocorrelation among locations up to lags of 30 days or more. During many seasonal periods there was no indication of decreasing autocorrelation with increasing time between locations. Over the course of the year, herds showed highly variable and complex patterns of autocorrelation, ranging from random use of temporary home ranges, periodic use of focal areas, and directional migration. Even though the patterns of autocorrelation were variable in time and quite complex, there were highly significant correlations among the autocorrelation patterns of the different herds, indicating that they exhibited similar patterns of movement through the year. These major patterns of autocorrelation seem to be related to patterns of rainfall. The strength of correlation in movement patterns of the different herds decreased markedly at the cessation of major rain events. Also, there was a strong crosscorrelation between strength of autocorrelation of movement and rainfall, peaking at time lags of between three and four weeks. Overall, these approaches provide a powerful way to explore the scales and patterns of autocorrelation of animal movements, and to explicitly link those patterns to temporally variable environmental attributes, such as rainfall or vegetation phenology.     

The Sound of Danger: Threat Sensitivity to Predator Vocalizations,Alarm Calls,and Novelty in Gulls

The threat sensitivity hypothesis predicts that organisms will evaluate the relative danger of and respond differentially to varying degrees of predation threat. Doing so allows potential prey to balance the costs and benefits of anti-predator behaviors. Threat sensitivity has undergone limited testing in the auditory modality, and the relative threat level of auditory cues from different sources is difficult to infer across populations when variables such as background risk and experience are not properly controlled. We experimentally exposed a single population of two sympatric gull species to auditory stimuli representing a range of potential threats in order to compare the relative threat of heterospecific alarm calls, conspecific alarms calls, predator vocalizations, and novel auditory cues. Gulls were able to discriminate among a diverse set of threat indicators and respond in a graded manner commensurate with the level of threat. Vocalizations of two potential predators, the human voice and bald eagle call, differed in their threat level compared to each other and to alarm calls. Conspecific alarm calls were more threatening than heterospecfic alarm calls to the larger great black-backed gull, but the smaller herring gull weighed both equally. A novel cue elicited a response intermediate between known threats and a known non-threat in herring gulls, but not great black-backed gulls. Our results show that the relative threat level of auditory cues from different sources is highly species-dependent, and that caution should be exercised when comparing graded and threshold threat sensitive responses.     

Elephants in Ancient Egypt and Nubia

ABSTRACT

This article examines the presence of elephants in civilizations of the ancient Nile valley, where they were hunted and distributed to Egypt and to the Classical Greco-Roman world for ivory, amusement, and military purposes. The full study of elephants requires diverse multidisciplinary research on their evolution, taxonomy, extinction, climate change, the history of human—elephant interactions, and modern issues relating to elephant and ivory policy. This regional view of the past illuminates some of the deep roots of these modern issues in human—elephant relations.     

Interspecific Semantic Alarm Call Recognition in the Solitary Sahamalaza Sportive Lemur,Lepilemur sahamalazensis

As alarm calls indicate the presence of predators, the correct interpretation of alarm calls, including those of other species, is essential for predator avoidance. Conversely, communication calls of other species might indicate the perceived absence of a predator and hence allow a reduction in vigilance. This “eavesdropping” was demonstrated in birds and mammals, including lemur species. Interspecific communication between taxonomic groups has so far been reported in some reptiles and mammals, including three primate species. So far, neither semantic nor interspecific communication has been tested in a solitary and nocturnal lemur species. The aim of this study was to investigate if the nocturnal and solitary Sahamalaza sportive lemur, Lepilemur sahamalazensis, is able to access semantic information of sympatric species. During the day, this species faces the risk of falling prey to aerial and terrestrial predators and therefore shows high levels of vigilance. We presented alarm calls of the crested coua, the Madagascar magpie-robin and aerial, terrestrial and agitation alarm calls of the blue-eyed black lemur to 19 individual Sahamalaza sportive lemurs resting in tree holes. Songs of both bird species’ and contact calls of the blue-eyed black lemur were used as a control. After alarm calls of crested coua, Madagascar magpie-robin and aerial alarm of the blue-eyed black lemur, the lemurs scanned up and their vigilance increased significantly. After presentation of terrestrial alarm and agitation calls of the blue-eyed black lemur, the animals did not show significant changes in scanning direction or in the duration of vigilance. Sportive lemur vigilance decreased after playbacks of songs of the bird species and contact calls of blue-eyed black lemurs. Our results indicate that the Sahamalaza sportive lemur is capable of using information on predator presence as well as predator type of different sympatric species, using their referential signals to detect predators early, and that the lemurs’ reactions are based on experience and learning.     

Ontogenetic and Sex Differences Influence Alarm Call Responses in Mammals: a Meta‐Analysis

Animals respond to alarm calls by increasing their antipredator behavior; however, responses may consistently differ by age or sex. Although several adaptive explanations have been proposed to account for age‐dependent antipredator behavior, similar explanations are rarely extended to sex‐specific responses. Furthermore, no attempts have been made to quantitatively estimate the direction or magnitude of these differences across studies. Here, we use meta‐analysis to discover overall trends in the literature, as well as differences owing to experimental or population parameters. Across our sample of available studies (unfortunately biased toward rodents and primates), males respond more than females, and young respond more than adults. Furthermore, young of quickly maturing species display more adult‐like antipredator behavior than young of slowly maturing species, suggesting that young must develop antipredator behavior at a pace consistent with the length of their ontogenetic period (a.k.a. juvenile/sub‐adult period, defined as the time between birth and attainment of sexual maturity). We review previously proposed explanations for such age differences, namely, that longer ontogenetic periods may provide juveniles with time to develop behavior through learning and experience, or, maturation rates may influence age‐specific selection pressures and the consequent evolution of age‐specific behavioral strategies. We evaluate our results in light of these hypotheses, although our conclusions are limited by the number and taxonomic bias of available studies. We therefore suggest ways in which future studies may tease apart the relative importance of learning and experience vs. age‐specific adaptive behavior, and draw attention to opportunities for research on age‐ and sex‐specific alarm call responses.     

Decrease in Alarm Call Response Among Tufted Capuchins in Competitive Feeding Contexts: Possible Evidence for Counterdeception

Animal signals function to elicit behaviors in receivers that ultimately benefit the signaler, while receivers should respond in a way that maximizes their own fitness. However, the best response may be difficult for receivers to determine when unreliable signaling is common. “Deceptive” alarm calling is common among tufted capuchins (Cebus apella nigritus) in competitive feeding contexts, and responding to these calls is costly. Receivers should thus vary their responses based on whether a call is likely to be reliable. If capuchins are indeed able to assess reliability, I predicted that receivers will be less likely to respond to alarms that are given during competitive feeding contexts than in noncompetitive contexts, and, within feeding contexts, that individuals inside or adjacent to a food patch will be less likely to respond to alarms than those further from the resource. I tested these predictions in a group of wild capuchins by observing the reactions of focal animals to alarm calls in both noncompetitive contexts and experimental feeding contexts. Antipredator escape reactions, but not vigilance reactions, occurred significantly less often in competitive feeding contexts than in noncompetitive contexts and individuals adjacent to food patches were more likely to respond to alarm calls than were those inside or further from food patches. Although not all predictions were fully supported, the findings demonstrate that receivers vary their behavior in a way that minimizes the costs associated with “deceptive” alarms, but further research is needed to determine whether or not this can be attributed to counterdeception.     

Development of a Body Condition Scoring Index for Female African Elephants Validated by Ultrasound Measurements of Subcutaneous Fat

Obesity-related health and reproductive problems may be contributing to non-sustainability of zoo African elephant (Loxodonta africana) populations. However, a major constraint in screening for obesity in elephants is lack of a practical method to accurately assess body fat. Body condition scoring (BCS) is the assessment of subcutaneous fat stores based on visual evaluation and provides an immediate appraisal of the degree of obesity of an individual. The objective of this study was to develop a visual BCS index for female African elephants and validate it using ultrasound measures of subcutaneous fat. To develop the index, standardized photographs were collected from zoo (n = 50) and free-ranging (n = 57) female African elephants for identifying key body regions and skeletal features, which were then used to visually determine body fat deposition patterns. This information was used to develop a visual BCS method consisting of a list of body regions and the physical criteria for assigning an overall score on a 5-point scale, with 1 representing the lowest and 5 representing the highest levels of body fat. Results showed that as BCS increased, ultrasound measures of subcutaneous fat thickness also increased (P<0.01), indicating the scores closely coincide with physical measures of fat reserves. The BCS index proved to be reliable and repeatable based on high intra- and inter-assessor agreement across three assessors. In comparing photographs of wild vs. captive African elephants, the median BCS in the free-ranging individuals (BCS = 3, range 1–5) was lower (P<0.001) than that of the zoo population (BCS = 4, range 2–5). In sum, we have developed the first validated BCS index for African elephants. This tool can be used to examine which factors impact body condition in zoo and free-ranging elephants, providing valuable information on how it affects health and reproductive potential of individual elephants.     

A Novel Objective Method of Estimating the Age of Mandibles from African Elephants (Loxodonta africana Africana)

The importance of assigning an accurate estimate of age and sex to elephant carcasses found in the wild has increased in recent years with the escalation in levels of poaching throughout Africa. Irregularities identified in current ageing techniques prompted the development of a new method to describe molar progression throughout life. Elephant mandibles (n = 323) were studied and a point near the distal dental alveolus was identified as being most useful in ranking each jaw according to molar progression. These ‘Age Reference Lines’ were then associated with an age scale based on previous studies and Zimbabwean mandibles of known age. The new ranking produced a single age scale that proved useful for both male and female mandibles up to the maximum lifespan age of 70–75 years. Methods to aid in molar identification and the sexing of found jaws were also identified.     

Responses of Redfronted Lemurs to Experimentally Modified Alarm Calls: Evidence for Urgency-Based Changes in Call Structure

Abstract The aim of this study was to investigate how information about the affective state is expressed in vocalizations. Alarm calls can serve as model systems with which to study this general question. Therefore, we examined the information content of terrestrial predator alarm calls of redfronted lemurs ( Eulemur fulvus rufus ), group-living Malagasy primates. Redfronted lemurs give specific alarm calls only towards raptors, whereas calls given in response to terrestrial predators (woofs) are also used in other situations characterized by high arousal. Woofs may therefore have the potential to express the perceived risk of a given threat. In order to examine whether different levels of arousal are expressed in call structure, we analysed woofs given during inter-group encounters or in response to playbacks of a barking dog, assuming that animals engaged in inter-group encounters experience higher arousal than during the playbacks of dog barks. A multivariate acoustic analysis revealed that calls given during group encounters were characterized by higher frequencies than calls given in response to playbacks of dog barks. In order to examine whether this change in call structure is salient to conspecifics, we conducted playback experiments with woofs, modified in either amplitude or frequencies. Playbacks of calls with increased frequency or amplitude elicited a longer orienting response, suggesting that different levels of arousal are expressed in call structure and provide meaningful information for listeners. In conclusion, the results of our study indicate that the information about the sender's affective state is expressed in the structure of vocalizations.     

The Social and Ecological Integration of Captive-Raised Adolescent Male African Elephants (Loxodonta africana) into a Wild Population

Background

A rapid rise in the number of captive African elephants (Loxodonta africana) used in the tourism industry in southern Africa and orphaned elephants in human care has led to concerns about their long-term management, particularly males. One solution is to release them into the wild at adolescence, when young males naturally leave their herd. However, this raises significant welfare concerns: little is known about how well released elephants integrate into wild populations and whether they pose a greater threat to humans than wild elephants. We document the release of three captive-raised adolescent male African elephants in the Okavango Delta, Botswana.

Methodology/Principal Findings

Despite having been part of a herd of working elephants for at least eight years, the three males progressively integrated into the complex fission-fusion society of wild bull elephants. In the three years following release, they showed no tendency to be closer to human habitation, and there were no significant differences between wild and captive-raised adolescent males in the total number of social interactions, size of ranges and habitat use. However, the captive-raised elephants sparred less and vocalised more, and spent more time alone and in smaller social groups. Thereafter the released elephants continued to expand their ranges and interact with both mixed-sex herds and males. One male was shot by farmers 94 months after release, along with ten wild elephants, on a ranch outside the protected area.

Conclusions/Significance

We show that captive-raised adolescent male elephants can integrate into a wild population. Long-term studies are required to determine the longevity, breeding success, and eventual fate of released male elephants, but we identified no significant short-term welfare problems for the released elephants or recipient population. Release of captive-raised mammals with complex social systems is a husbandry option that should be explored further.