Energetic Optimisation of Foraging Honeybees: Flexible Change of Strategies in Response to Environmental Challenges

Heterothermic insects like honeybees, foraging in a variable environment, face the challenge of keeping their body temperature high to enable immediate flight and to promote fast exploitation of resources. Because of their small size they have to cope with an enormous heat loss and, therefore, high costs of thermoregulation. This calls for energetic optimisation which may be achieved by different strategies. An ‘economizing’ strategy would be to reduce energetic investment whenever possible, for example by using external heat from the sun for thermoregulation. An ‘investment-guided’ strategy, by contrast, would be to invest additional heat production or external heat gain to optimize physiological parameters like body temperature which promise increased energetic returns. Here we show how honeybees balance these strategies in response to changes of their local microclimate. In a novel approach of simultaneous measurement of respiration and body temperature foragers displayed a flexible strategy of thermoregulatory and energetic management. While foraging in shade on an artificial flower they did not save energy with increasing ambient temperature as expected but acted according to an ‘investment-guided’ strategy, keeping the energy turnover at a high level (∼56–69 mW). This increased thorax temperature and speeded up foraging as ambient temperature increased. Solar heat was invested to increase thorax temperature at low ambient temperature (‘investment-guided’ strategy) but to save energy at high temperature (‘economizing’ strategy), leading to energy savings per stay of ∼18–76% in sunshine. This flexible economic strategy minimized costs of foraging, and optimized energetic efficiency in response to broad variation of environmental conditions.     

Population-Scale Foraging Segregation in an Apex Predator of the North Atlantic

In this work we investigated the between-colony spatial, behavioural and trophic segregation of two sub-populations of the elusive Macaronesian shearwaters Puffinus baroli breeding only ~340 km apart in Cima Islet (Porto Santo Island) and Selvagem Grande Island. Global location sensing (gls) loggers were used in combination with the trophic ecology of tracked individuals, inferred from the isotopic signatures of wing feathers. Results suggest that these two Macaronesian shearwater sub-populations do segregate during the non-breeding period in some ‘sub-population-specific’ regions, by responding to different oceanographic characteristics (habitat modelling). Within these disparate areas, both sub-populations behave differently (at-sea activity) and prey on disparate trophic niches (stable isotope analysis). One hypothesis would be that each sub-population have evolved and adapted to feed on particular and ‘sub-population-specific’ resources, and the segregation observed at the three different levels (spatial, behavioural and trophic) might be in fact a result of such adaptation, from the emergence of ‘cultural foraging patterns’. Finally, when comparing to the results of former studies reporting on the spatial, behavioural and trophic choices of Macaronesian shearwater populations breeding on Azores and Canary Islands, we realized the high ecological plasticity of this species inhabiting and foraging over the North-East Atlantic Ocean.     

Cooperative sentinel calling? Foragers gain increased biomass intake

Many foraging animals face a fundamental tradeoff between predation and starvation. In a range of social species, this tradeoff has probably driven the evolution of sentinel behavior, where individuals adopt prominent positions to watch for predators while groupmates forage. Although there has been much debate about whether acting as a sentinel is a selfish or cooperative behavior, far less attention has focused on why sentinels often produce quiet vocalizations (hereafter known as "sentinel calls") to announce their presence. We use observational and experimental data to provide the first evidence that group members gain an increase in foraging success by responding to these vocal cues given by sentinels. Foraging pied babblers (Turdoides bicolor) spread out more, use more exposed patches, look up less often, and spend less time vigilant in response to sentinel calling. Crucially, we demonstrate that these behavioral alterations lead to an increase in biomass intake by foragers, which is likely to enhance survival. We argue that this benefit may be the reason for sentinel calling, making it a truly cooperative behavior.     

Mutualism among safe, selfish sentinels: a dynamic game

Sentinels are group members that watch from prominent positions. Sentinel interchanges often appear orderly, and groups with sentinels rarely have zero or many sentinels. A dynamic game was constructed to examine if these observations about sentinels could be based on selfish actions by individual group members. In this game, each group member chose to forage or be a sentinel based on its own energetic state and the actions of others. Sentinels received a selfish antipredator benefit if their ability to detect approaching predators more than compensated for their increased exposure to undetected predators. Provided sentinels were relatively safe and that detection information spread to other group members when sentinels detected predators, sentinels appeared highly coordinated for all combinations of parameters. This apparent coordination was based on mutualism because each individual gained by being a sentinel when other group members were not (and foraging when other group members were being sentinels). The model was very robust, but exact level of sentinel behavior varied somewhat with changes in foraging and predation parameters. This model could best be tested by testing its assumptions about sentinel safety, foraging-predation trade-offs, and information transfer in groups.     

Eavesdropping foragers use level of collective commotion as public information to target high quality patches

Public information offers a valuable means for social foragers to determine the relative quality of foraging patches. Despite much evidence that foragers use public information based on others’ feeding behavior, no experiments have examined whether foragers might use public information based on others’ competitive behavior, particularly the collective commotion that can be generated by aggregations. Such commotion could potentially provide a rich source of public information: as foragers compete in a patch with an especially high value resource, their heightened competition intensity could enable eavesdropping foragers to target this superior patch, based simply on its higher level of collective commotion. To test the hypothesis that the level of collective commotion is used as public information by eavesdropping foragers I conducted field experiments on terrestrial hermit crabs Coenobita compressus. These animals engage in collective competitive interactions in foraging patches for food and shells, generating variable levels of commotion across different quality patches. By experimentally manipulating the level of collective commotion in sham aggregations in the wild I show that a higher level of commotion is exploited by eavesdropping foragers to differentially target more valuable patches. Broadly, these results highlight an underappreciated significance of competitive by‐products and higher‐ order collective pheno mena as forms of public information for foragers.     

The value of constant surveillance in a risky environment

In risky environments, where threats are unpredictable and the quality of information about threats is variable, all individuals face two fundamental challenges: balancing vigilance against other activities, and determining when to respond to warning signals. The solution to both is to obtain continuous estimates of background risk, enabling vigilance to be concentrated during the riskiest periods and informing about the likely cost of ignoring warnings. Human surveillance organizations routinely produce such estimates, frequently derived from indirect cues. Here we show that vigilant individuals in an animal society (the pied babbler, Turdoides bicolor) perform a similar role. We ask (i) whether, in the absence of direct predator threats, pied babbler sentinels react to indirect information associated with increased risk and whether they communicate this information to group mates; (ii) whether group mates use this information to adjust their own vigilance, and whether this influences foraging success; and (iii) whether information provided by sentinels reduces the likelihood of inappropriate responses to alarm calls. Using playback experiments, we show that: (i) sentinels reacted to indirect predator cues (in the form of heterospecific alarm calls) by giving graded surveillance calls; (ii) foragers adjusted their vigilance in reaction to changes in surveillance calls, with substantial effects on foraging success; and (iii) foragers reduced their probability of responding to alarm calls when surveillance calls indicated lowered risk. These results demonstrate that identifying attacks as they occur is only part of vigilance: equally important is continuous surveillance providing information necessary for individuals to make decisions about their own vigilance and evasive action. Moreover, they suggest that a major benefit of group living is not only the increased likelihood of detecting threats, but a marked improvement in the quality of information available to each individual.     

Do Conversational Gutturals Help Florida Scrub‐Jays Coordinate Their Sentinel Behavior?

Florida scrub‐jays, Aphelocoma coerulescens, perform sentinel behavior in which individuals alternate bouts of watchfulness with little overlap. We examined how calls might facilitate sentinel coordination. Small soft calls labeled conversational gutturals were heard more often from sentinels than from foraging birds. Calls occurred infrequently throughout sentinel bouts but were more common later in bouts. The pattern of calling does not match predictions for a ‘watchman’s song’ at regular intervals nor for a signal at the end of a sentinel bout. Thus, our quantitative assessment of calling by sentinels did not find support for either standard hypothesis. Although Florida scrub‐jays clearly have information on each other’s sentinel behavior, our results suggest that calls provide perhaps a fraction of this information.     

Florida Scrub-Jays (Aphelocoma coerulescens) are Sentinels More When Well-Fed (Even with no Kin Nearby)

Sentinels occupy high, exposed positions while other group members forage nearby. If sentinel behavior involves a foraging–predation risk trade‐off, animals should be sentinels more when fed supplemental food. When individual Florida scrub‐jays (Aphelocoma coerulescens) were fed fragments of peanuts, during the following 30 min they shifted 30% of their time from foraging to sentinel behavior. In a follow‐up experiment, we fed either one or two members in each group. As before, the jays reduced their foraging and spent much more time as sentinels when given supplemental food. In each treatment, pairs were sentinels simultaneously considerably less often than expected by chance. The dramatic shift from foraging to sentinel behavior suggests that for Florida scrub‐jays sentinel behavior brings substantial benefits for no greater cost than that of lost opportunities to forage. Because the results held for simple mated pairs of scrub‐jays, we argue that kin selection and social prestige are not necessary to explain sentinel behavior.     

Interspecific signalling between mutualists: food-thieving drongos use a cooperative sentinel call to manipulate foraging partners

Interspecific communication is common in nature, particularly between mutualists. However, whether signals evolved for communication with other species, or are in fact conspecific signals eavesdropped upon by partners, is often unclear. Fork-tailed drongos (Dicrurus adsimilis) associate with mixed-species groups and often produce true alarms at predators, whereupon associating species flee to cover, but also false alarms to steal associating species'' food (kleptoparasitism). Despite such deception, associating species respond to drongo non-alarm calls by increasing their foraging and decreasing vigilance. Yet, whether these calls represent interspecific sentinel signals remains unknown. We show that drongos produced a specific sentinel call when foraging with a common associate, the sociable weaver (Philetairus socius), but not when alone. Weavers increased their foraging and decreased vigilance when naturally associating with drongos, and in response to sentinel call playback. Further, drongos sentinel-called more often when weavers were moving, and weavers approached sentinel calls, suggesting a recruitment function. Finally, drongos sentinel-called when weavers fled following false alarms, thereby reducing disruption to weaver foraging time. Results therefore provide evidence of an ‘all clear’ signal that mitigates the cost of inaccurate communication. Our results suggest that drongos enhance exploitation of a foraging mutualist through coevolution of interspecific sentinel signals.     

Risk-Based Learning Games Improve Long-Term Retention of Information among School Pupils

Risk heightens motivation and, if used appropriately, may have the potential to improve engagement in the classroom. We have developed a risk-based learning game for school pupils in order to test whether such learning games can improve later recall of information. The study was performed during a series of public engagement workshops delivered by undergraduate students. Undergraduate neuroscience students delivered 90-minute science workshops to 9–10 year old school pupils (n = 448) that were divided into ‘Risk’, ‘No risk’ and ‘Control’ classes. ‘Risk’ classes received periodic multiple-choice questions (MCQs) during the workshops which required small teams of pupils to assign tokens to the answer(s) they believed to be correct. Tokens assigned to the correct answer were returned to the group and an equal number given back as a prize; tokens assigned to incorrect answers were lost. Participation was incentivised by the promise of a brain-related prize to the team with the most tokens at the end of the workshop. ‘No risk’ classes received MCQs without the risk component whilst the ‘Control’ classes received no MCQs. When presented with a neuroscience quiz based on workshop content at the end of the workshop, pupils in the ‘Risk’ classes exhibited significantly greater recall of information one week later. Quiz scores were higher than scores from the day of the workshop which suggested pupils may have discussed the workshop content outside of the classroom, thereby increasing knowledge over and above what was learned during the workshop. This is supported by feedback from pupils in ‘Risk’ classes which indicated that ‘Risk’ workshops were more interesting than ‘No risk’ and ‘Control’ workshops. These data suggest that there is a role for risk in the classroom but further investigations are required to elucidate the causal mechanisms of improved retention of information.     

Nine-spined sticklebacks exploit the most reliable source when public and private information conflict

Social foragers can potentially use private information gained from personal experience and public information gained from observing the foraging success of others to determine the profitability of a foraging patch. We investigated how nine-spined sticklebacks use conflicting public and private information of variable reliability to make foraging decisions. In a first experiment, when private information was reliable, sticklebacks ignored public information and based their foraging decision on private information. However, when private information was less reliable, sticklebacks tended to use public rather than private information. A second experiment investigated how the time since experiencing private information affected sticklebacks' use of this information when it conflicted with recent public information. Fish based their foraging decisions on recently acquired private information, but reliance on private information diminished as the period since experiencing it increased. Fish used public information if 7 days had elapsed since updating their private information. Our findings suggest that nine-spined sticklebacks flexibly adjust their decision making to exploit the most reliable information available, be it public or private, and that animals will weight private and public information appropriately depending on circumstances.     

Scaling laws of ambush predator ‘waiting’ behaviour are tuned to a common ecology

The decisions animals make about how long to wait between activities can determine the success of diverse behaviours such as foraging, group formation or risk avoidance. Remarkably, for diverse animal species, including humans, spontaneous patterns of waiting times show random ‘burstiness’ that appears scale-invariant across a broad set of scales. However, a general theory linking this phenomenon across the animal kingdom currently lacks an ecological basis. Here, we demonstrate from tracking the activities of 15 sympatric predator species (cephalopods, sharks, skates and teleosts) under natural and controlled conditions that bursty waiting times are an intrinsic spontaneous behaviour well approximated by heavy-tailed (power-law) models over data ranges up to four orders of magnitude. Scaling exponents quantifying ratios of frequent short to rare very long waits are species-specific, being determined by traits such as foraging mode (active versus ambush predation), body size and prey preference. A stochastic–deterministic decision model reproduced the empirical waiting time scaling and species-specific exponents, indicating that apparently complex scaling can emerge from simple decisions. Results indicate temporal power-law scaling is a behavioural ‘rule of thumb’ that is tuned to species’ ecological traits, implying a common pattern may have naturally evolved that optimizes move–wait decisions in less predictable natural environments.     

A dynamic over games drives selfish agents to win–win outcomes

Understanding human institutions, animal cultures and other social systems requires flexible formalisms that describe how their members change them from within. We introduce a framework for modelling how agents change the games they participate in. We contrast this between-game ‘institutional evolution’ with the more familiar within-game ‘behavioural evolution’. We model institutional change by following small numbers of persistent agents as they select and play a changing series of games. Starting from an initial game, a group of agents trace trajectories through game space by navigating to increasingly preferable games until they converge on ‘attractor’ games. Agents use their ‘institutional preferences'' for game features (such as stability, fairness and efficiency) to choose between neighbouring games. We use this framework to pose a pressing question: what kinds of games does institutional evolution select for; what is in the attractors? After computing institutional change trajectories over the two-player space, we find that attractors have disproportionately fair outcomes, even though the agents who produce them are strictly self-interested and indifferent to fairness. This seems to occur because game fairness co-occurs with the self-serving features these agents do actually prefer. We thus present institutional evolution as a mechanism for encouraging the spontaneous emergence of cooperation among small groups of inherently selfish agents, without space, reputation, repetition, or other more familiar mechanisms. Game space trajectories provide a flexible, testable formalism for modelling the interdependencies of behavioural and institutional evolutionary processes, as well as a mechanism for the evolution of cooperation.     

Rich Pickings Near Large Communal Roosts Favor ‘Gang’ Foraging by Juvenile Common Ravens,Corvus corax

Ravens (Corvus corax) feed primarily on rich but ephemeral carcasses of large animals, which are usually defended by territorial pairs of adults. Non-breeding juveniles forage socially and aggregate in communal winter roosts, and these appear to function as ‘information centers’ regarding the location of the rare food bonanzas: individuals search independently of one another and pool their effort by recruiting each other at roosts. However, at a large raven roost in Newborough on Anglesey, North Wales, some juveniles have been observed recently to forage in ‘gangs’ and to roost separately from other birds. Here we adapt a general model of juvenile common raven foraging behavior where, in addition to the typical co-operative foraging strategy, such gang foraging behavior could be evolutionarily stable near winter raven roosts. We refocus the model on the conditions under which this newly documented, yet theoretically anticipated, gang-based foraging has been observed. In the process, we show formally how the trade off between search efficiency and social opportunity can account for the existence of the alternative social foraging tactics that have been observed in this species. This work serves to highlight a number of fruitful avenues for future research, both from a theoretical and empirical perspective.     

Response of foraging group members to sentinel calls in suricates,Suricata suricatta

In the suricate (Suricata suricatta), a cooperatively breeding mongoose, one individual typically watches out for predators while the rest of the group is foraging. Most of the time these sentinels announce their guarding duty with special vocalizations. The response of foraging group members to these calls was investigated by analysing observational data, and by performing playback experiments. The use of special calls by sentinels, and the responses of the foraging group members to them, suggest that the coordination of vigilance is strongly influenced by vocal communication. Sentinel calls decreased the time spent alert by the foraging group members. Other group members were less likely to go on guard when a sentinel was vocalizing. Both the proportion of time during which guards overlapped, and the proportion of time the group was unprotected without a guard, decreased when sentinels announced their duty, due to better coordination of the rotation of sentinels. Suricates, however, do not appear to use sentinel calls to mediate a strict rotation of guarding duty.     

Colony and Individual Forager Responses to Food Quality in the New World Bumble Bee, Bombus occidentalis

The ability of a successful forager to activate colony foraging allows colonies to rapidly exploit ephemeral resources and is an important innovation in the evolution of sociality. We tested the ability of the species, Bombus occidentalis, to stimulate colony foraging for food varying in quality. We then analyzed the behavior of successful foragers inside the nest to learn more about potential foraging activation movements. The number of bees entering a foraging arena was positively correlated with food sucrose concentration (0.5, 1.0, and 2.5 M sucrose, equal to 16–65% w/w). Foragers spent significantly more time imbibing higher concentration solutions. Foragers then returned to the nest where they moved in elaborate paths at variable speeds. There was no significant effect of sucrose concentration on average forager velocity or time spent inside the nest. However, the length of a forager’s path inside the nest (total of all distances moved each 0.1 s) significantly increased with sucrose concentration. On average, individuals foraging on 2.5 M and 1.0 M solution walked paths respectively 1.6 fold and 1.4 longer than the paths of individuals foraging on 0.5 M solution. These longer paths could result in a greater number of nestmate contacts, a factor shown to be important in the activation of B. impatiens foragers and also reported in B. terrestris foragers.     

Complex and Conflicting Social Norms: Implications for Implementation of Future HIV Pre-Exposure Prophylaxis (PrEP) Interventions in Vancouver,Canada

Background

HIV Pre-Exposure Prophylaxis (PrEP) has been found to be efficacious in preventing HIV acquisition among seronegative individuals in a variety of risk groups, including men who have sex with men and people who inject drugs. To date, however, it remains unclear how socio-cultural norms (e.g., attitudes towards HIV; social understandings regarding HIV risk practices) may influence the scalability of future PrEP interventions. The objective of this study is to assess how socio-cultural norms may influence the implementation and scalability of future HIV PrEP interventions in Vancouver, Canada.

Methods

We conducted 50 interviews with young men (ages 18–24) with a variety of HIV risk behavioural profiles (e.g., young men who inject drugs; MSM). Interviews focused on participants’ experiences and perceptions with various HIV interventions and policies, including PrEP.

Results

While awareness of PrEP was generally low, perceptions about the potential personal and public health gains associated with PrEP were interconnected with expressions of complex and sometimes conflicting social norms. Some accounts characterized PrEP as a convenient form of reliable protection against HIV, likening it to the female birth control pill. Other accounts cast PrEP as a means to facilitate ‘socially unacceptable’ behaviour (e.g., promiscuity). Stigmatizing rhetoric was used to position PrEP as a tool that could promote some groups’ proclivities to take ‘risks’.

Conclusion

Stigma regarding ‘risky’ behaviour and PrEP should not be underestimated as a serious implementation challenge. Pre-implementation strategies that concomitantly aim to improve knowledge about PrEP, while addressing associated social prejudices, may be key to effective implementation and scale-up.     

Tolerance of understory plants subject to herbivory by roe deer

Classical foraging theory states that animals feeding in a patchy environment can maximise their long term prey capture rates by quitting food patches when they have depleted prey to a certain threshold level. Theory suggests that social foragers may be better able to do this if all individuals in a group have access to the prey capture information of all other group members. This will allow all foragers to make a more accurate estimation of the patch quality over time and hence enable them to quit patches closer to the optimal prey threshold level. We develop a model to examine the foraging efficiency of three strategies that could be used by a cohesive foraging group to initiate quitting a patch, where foragers do not use such information, and compare these with a fourth strategy in which foragers use public information of all prey capture events made by the group. We carried out simulations in six different prey environments, in which we varied the mean number of prey per patch and the variance of prey number between patches. Groups sharing public information were able to consistently quit patches close to the optimal prey threshold level, and obtained constant prey capture rates, in groups of all sizes. In contrast all groups not sharing public information quit patches progressively earlier than the optimal prey threshold value, and experienced decreasing prey capture rates, as group size increased. This is more apparent as the variance in prey number between patches increases. Thus in a patchy environment, where uncertainty is high, although public information use does not increase the foraging efficiency of groups over that of a lone forager, it certainly offers benefits over groups which do not, and particularly where group size is large.     

First satellite tracks of neonate sea turtles redefine the ‘lost years’ oceanic niche

Few at-sea behavioural data exist for oceanic-stage neonate sea turtles, a life-stage commonly referred to as the sea turtle ‘lost years’. Historically, the long-term tracking of small, fast-growing organisms in the open ocean was logistically or technologically impossible. Here, we provide the first long-term satellite tracks of neonate sea turtles. Loggerheads (Caretta caretta) were remotely tracked in the Atlantic Ocean using small solar-powered satellite transmitters. We show that oceanic-stage turtles (i) rarely travel in Continental Shelf waters, (ii) frequently depart the currents associated with the North Atlantic Subtropical Gyre, (iii) travel quickly when in Gyre currents, and (iv) select sea surface habitats that are likely to provide a thermal benefit or refuge to young sea turtles, supporting growth, foraging and survival. Our satellite tracks help define Atlantic loggerhead nursery grounds and early loggerhead habitat use, allowing us to re-examine sea turtle ‘lost years’ paradigms.