A circadian rhythm of thermal preference in the ant Camponotus mus: masking and entrainment by temperature cycles

Abstract. Along a stable temperature gradient and under a LD 12:12 h cycle, nurse workers of the ant Camponotus mus Roger 1863 (Hymenoptera: Formicidae) select for the brood two different temperatures daily: 30.8°C at the middle of the light period (circadian phase = 90°), and 27.5°C 8 h later, during the dark period (circadian phase = 210°), this rhythm being of endogenous nature.When a 24 h temperature cycle was superimposed along the thermal gradient, so that the immobile brood experienced a temperature transition as they receive when translocated by nurses (8 h at 30.8°C and 16 h at 27.5°C), no brood translocations occurred.The thermal cycle masked the rhythm of brood translocation when temperature fitted the daily pattern expected by nurses.When the same temperature cycle was presented with a phase-advance, nurses did not tolerate the early thermal increase and removed the brood as temperature rose.However, when workers experienced this new phase relationship between light and temperature cycles for more than 10 days, brood translocations were suppressed.Records under constant conditions of light and temperature indicated that the overt rhythm was locked-on to the expected early increase in temperature, so that the temperature cycle dominated over the LD cycle in resetting brood-carrying activity.     

Bumble-bees learn the value of social cues through experience

Natural selection should lead animals to use social cues (SC) when they are useful, and disregard them when they are not. Theoretical investigation predicts that individuals should thus employ social learning ‘strategies’, but how might such context specificity be achieved on a proximate level? Operant conditioning, whereby the use of SC is reinforced through rewarding results, provides a potential mechanism. We investigate the role of reinforcement in joining behaviour in bumble-bees, Bombus terrestris. When bees visit unfamiliar flower species, they prefer to probe inflorescences where others are also foraging, and here we show that such behaviour is promoted through experience when conspecific presence reliably predicts reward. Our findings highlight a straightforward, but rarely discussed, mechanism by which animals can be selective about when to use SC.     

Social Learning and Primate Reintroduction

Research on social learning may be of use in the conservation of primates, especially great apes, through (a) promoting their public image, (b) identifying specific adaptations, and (c) devising reintroduction training programs. We surveyed all the instigated social learning studies in primates published since 1950 in order to assess their usefulness to devise reintroduction training programs. We identified 99 publications containing 130 data sets from 27 species of primates. Great apes produced significantly more positive social learning effects than either cercopithecines or cebids. There was also an enhanced social learning effect when skilled demonstrators were used. Our survey indicates that the scientific understanding of many aspects of primate social learning relevant to conservation, including its function, learning spatial route plotting, food and sleeping site location, predator avoidance and detection, and the effect of model and tutee status, would benefit from greater research. Future instigated studies on primate social learning would be most informative for reintroduction if they included ecologically valid tasks presented to 2 similarly composed social groups, one of which functioned as a control, i.e., without being exposed to a model.     

Understanding Behavioral Traditions in Primates: Are Current Experimental Approaches Too Focused on Food?

Recently, several researchers have highlighted the neglect of social behaviors relative to food-related behaviors in experimental research on social learning in primates, despite the significant number of apparent social traditions reported in the field. Here we aim to highlight the discrepancy between the relative number of nonfood-related behavioral traditions reported in the wild and food-related ones, and the almost exclusive investigation of food-related behaviors in an experimental context. First we discuss aspects of social and communicative customs that make them especially interesting. Then we consider reasons why experimental approaches are crucial to developing a full understanding of behavioral traditions observed in the wild. We report the results of a systematic literature survey in which we assessed the perceived discrepancy quantitatively. We also argue that the existing experimental literature, with its typical reliance on food as a motivator, may not be sufficient to elucidate the mechanisms underlying nonfood traditions, such as social conventions. Finally, we suggest new directions for the experimental investigation of social learning in primates, hoping to stimulate experimental research investigating social and communicative behavioral traditions.     

Social learning of predators in the dark: understanding the role of visual,chemical and mechanical information

The ability of prey to observe and learn to recognize potential predators from the behaviour of nearby individuals can dramatically increase survival and, not surprisingly, is widespread across animal taxa. A range of sensory modalities are available for this learning, with visual and chemical cues being well-established modes of transmission in aquatic systems. The use of other sensory cues in mediating social learning in fishes, including mechano-sensory cues, remains unexplored. Here, we examine the role of different sensory cues in social learning of predator recognition, using juvenile damselfish (Amphiprion percula). Specifically, we show that a predator-naive observer can socially learn to recognize a novel predator when paired with a predator-experienced conspecific in total darkness. Furthermore, this study demonstrates that when threatened, individuals release chemical cues (known as disturbance cues) into the water. These cues induce an anti-predator response in nearby individuals; however, they do not facilitate learnt recognition of the predator. As such, another sensory modality, probably mechano-sensory in origin, is responsible for information transfer in the dark. This study highlights the diversity of sensory cues used by coral reef fishes in a social learning context.     

Female bonobos use copulation calls as social signals

During mating events, females of many primate species produce loud and distinct vocalizations known as 'copulation calls'. The adaptive significance of these signals is considered to be in promoting the caller's direct reproductive success. Here, we investigated copulation calling in bonobos (Pan paniscus), a species in which females produce these vocalizations during sexual interactions with partners of both sexes. Females were more likely to call when mating with males than with females. We also observed a positive relationship between the likelihood of calling and partner rank, regardless of partner sex. Sexual activity generally increased with swelling size (an indicator of reproductive state) and, during their peak swelling, females called more with male than with female partners. Female bonobos are unusual among the non-human primates in terms of their heightened socio-sexuality. Our results suggest that in this species, copulation calls have undergone an evolutionary transition from a purely reproductive to a more general social function, reflecting the intrinsic evolutionary links between vocal behaviour and social cognition.     

Activity patterns of rodents: the physiological ecology of biological rhythms

To date, most research in the field of biological rhythms has been performed on nocturnal rodents under laboratory conditions. This research has made much progress in recent years. It is now time to investigate the adaptive value of the studied molecular mechanisms under natural conditions. Here we review relevant studies of rodent activity patterns. We also review a case study of temporal partitioning between spiny mice. We conclude that the response to environmental stimuli, using a system composed of a rigid master circadian oscillator and more flexible mechanisms such as peripheral oscillators with weak coupling, masking responses, and downstream switching mechanisms, is adaptive since it enables an animal to reset its activity phase without the cost of shifting the phase of the entire circadian system. We suggest that these mechanisms play a significant role in determining activity patterns under natural conditions, and are important for understanding the ecology and evolution of activity rhythms.     

Timekeeping Through Social Contacts: Social Synchronization of Circadian Locomotor Activity Rhythm in the Carpenter Ant Camponotus paria

In ant colonies a large proportion of individuals remain inside nests for most of their lives and come out only when necessary. It is not clear how, in a nest of several thousand individuals, information about local time is communicated among members of the colony. Central to this seem to be circadian clocks, which have an intrinsic ability to keep track of local time by entraining to environmental light-dark, temperature, and social cycles. Here, the authors report the results of their study aimed at understanding the role of cyclic social interactions in circadian timekeeping of a day-active species of carpenter ant Camponotus paria. The authors found that daily social interactions with visitors (worker ants) was able to synchronize the circadian locomotor activity rhythm of host worker ants and queens, in one-on-one (pair-wise) and multi-individual (group-wise) interactions. Interestingly, the outcome of cyclic social interactions was context specific; when visitor workers socially interacted with host workers one-on-one, host workers considered the time of interaction as subjective day, but when visitor workers interacted with a group of workers and queens, the hosts considered the time of interaction as subjective night. These results can be taken to suggest that members of the ant species C. paria keep track of local time by socially interacting with workers (foragers) who shuttle in and out of the colony in search of food. (Author correspondence: vsharma@jncasr.ac.in)     

Socially Adjusted Synchrony in the Activity Profiles of Common Marmosets in Light-Dark Conditions

Synchronized state of activity and rest might be attained by mechanisms of entrainment and masking. Most zeitgebers not only act to entrain but also to mask circadian rhythms. Although the light-dark (LD) cycle is the main zeitgeber of circadian rhythms in marmosets, social cues can act as weaker zeitgebers. Evidence on the effects of social entrainment in marmosets has been collected in isolated animals or in pairs where activity is not individually recorded. To characterize the synchronization between the daily activity profiles of individuals in groups under LD conditions, the motor activity of animals from five groups was continuously monitored using actiwatches for 15 days during the 5th, 8th, and 11th months of life of juveniles. Families consisting of twins (4 ♂♀/1 ♂♂) and their parents were maintained under controlled lighting (LD 12:12?h), temperature, and humidity conditions. Synchronization was evaluated through the synchrony between the circadian activity profiles obtained from the Pearson correlation index between possible pairs of activity profiles in the light and dark phases. We also calculated the phase-angle differences between the activity onset of one animal in relation to the activity onset of each animal in the group (ψ_on). A similar procedure was performed for activity offset (ψ_off). By visual analysis, the correlation between the activity profiles of individuals within each family was stronger than that of individuals from different families. A mixed-model analysis showed that within the group, the correlation was stronger between twins than between twins and their parents in all families, except for the family in which both juveniles were males. Because a twin is an important social partner for juveniles, a sibling is likely to have a stronger influence on its twin’s activity rhythm than other family members. Considering only the light phase, the second strongest correlation was observed between the activity profiles of the individuals in the reproductive pair. Regarding the parameters ψ_on and ψ_off, the juvenile/juvenile dyad had lower values than the other dyads, but these differences did not reach statistical significance in relation to all dyads. Comparing the results of the ψ_on and ψ_off, and correlation indices, we suggest that the latter could detect differences between the animals that were not observed in the results of the phase-angle differences. These differences could be related to changes that occur during the active phase but not only in a particular phase, such as the temporal changes during the activity phase that characterize unimodal or bimodal patterns. Based on the differences in the correlations between individuals subjected to the same LD routine, we suggest that social cues modulate the circadian activity profiles of marmosets as a result of interactions between the animals within each group. Future studies are necessary to characterize the mechanisms of synchronization that are involved in this social modulation. (Author correspondence: carolina@cb.ufrn.br)     

Olfactory cues in discrimination among individuals in dominance hierarchies in the cockroach, Nauphoeta cinerea

ABSTRACT. The purpose of this study was to explore the olfactory recognition mechanisms used by individual subordinate male cockroaches, Nauphoeta cinerea (Olivier), in a dominance hierarchy. Results of two independent sets of experiments, one using an olfactometer and the other using an arena, suggest that olfactory cues are important to males. Subordinate males did not avoid dominant male odour in an olfactometer but could discriminate between the odours of familiar and unfamiliar individual dominant males, preferring the odour of the dominant male with which they had previous social contact. Since test subordinates did not avoid dominant male odours in the olfactometer, it is possible that the distance an individual remains from a dominant is important. To test this, individual dominant and subordinate males were tethered in the centre of an arena. Subordinate males were introduced into the arena and allowed to approach the tethered male. They approached tethered dominants and subordinates differently, and tended to keep away from the dominants. Tethered males unfamiliar to the test animals were avoided as well.     

Effects of housing conditions and season on the activity rhythm of spider monkeys (Ateles geoffroyi) kept under natural conditions within their distributional range in Central Mexico

The timing and pattern of mammalian behavioral activities are regulated by an evolutionary optimized interplay of the genetically based biological (circadian) clock located in the brain’s suprachiasmatic nuclei and direct responses to environmental factors that superimpose and thus mask the clock-mediated effects, the most important of which is the photically induced phase-setting (synchronization) of the circadian rhythmicity to the 24-hour solar day. In wild and captive animals living under the natural conditions prevailing in their habitat, to date, only a few attempts have been made to analyze the role of these two regulatory mechanisms in the species’ adaptation to the time structure prevailing in their habitat. We studied the impact of housing conditions and season on the daily timing and pattern of activity in Mexican spider monkeys (Ateles geoffroyi). To this end, we carried out long-term activity recordings with Actiwatch® AW4 accelerometer/data-logger devices in 11 adult Ateles living under identical natural lighting and climatic conditions in either a large wire netting cage or a 0.25?ha forest enclosure in the primatological field station of Veracruz State University near Catemaco, Mexico. In a gravid female in the forest enclosure, we obtained first-hand information on the effect of late pregnancy and parturition on the monkey’s activity rhythm. The Ateles behaved strictly diurnal and undertook about 90% of daily total activity during this activity time. Due to a higher second activity peak in late afternoon, the bimodal activity pattern was more pronounced in monkeys living in the forest enclosure. Although the spider monkeys kept there had an earlier activity onset and morning activity peak than their conspecifics in the cage, no consistent differences were found in the parameters characterizing the phase-setting of the circadian system to the environmental 24-h periodicity, either by comparison or correlation with the external time markers of sunrise (SR) and sunset (SS). The most obvious effect of late pregnancy, parturition and lactation was a distinct reduction of the activity level during the week of parturition and the next. Seasonal variations in the form of significant differences between the long-day summer half year and the short-day winter half year were established in the phase-angle differences of the morning activity peak to SR, in the evening activity peak and activity offset to SS, as well as in the activity time and the peak-to-peak interval, but not in the phase position of activity onset to SR or in the height of the morning and evening activity peak. These findings in combination with a high variability of the phase angle differences indicate that in A. geoffroyi, a relatively weak circadian component and strong masking direct effects of environmental factors are involved in the regulation of the daily activity rhythm.