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International audience; Invasive species events related to globalization are increasing, resulting in parasitic outbreaks. Understanding of host defense mechanisms is needed to predict and mitigate against the consequences of parasite invasion. Using the honey bee Apis mellifera and the mite Varroa destructor, as a host–parasite model, we provide a comprehensive study of a mechanism of parasite detection that triggers a behavioral defense associated with social immunity. Six Varroa-parasitization-specific (VPS) compounds are identified that trigger Varroa-sensitive hygiene (VSH, bees’ key defense against Varroa sp.), enable the selective recognition of a parasitized brood and induce responses that mimic intrinsic VSH activity in bee colonies. We also show that individuals engaged in VSH exhibit a unique ability to discriminate VPS compounds from healthy brood signals. These findings enhance our understanding of a critical mechanism of host defense against parasites, and have the potential to apply the integration of pest management in the beekeeping sector.

Social interactions among conspecifics can have marked effects on individual physiology, especially through their modulation of the stress axis by affecting the production of adrenal glucocorticoids (GCs). Previous research has focused on how individual GC levels may be influenced by social status, but few studies have considered how the balance between positive (e.g. cooperation) and negative (e.g. competition) social interactions shape individual GC levels. A lack of association between individual GC levels and social factors may be confounded by opposite effects of social competition on the one hand and social cooperation on the other. We tested for these effects in the Columbian ground squirrel (Urocitellus columbianus), a colonial rodent. During the breeding season, females are exposed to territorial unrelated neighbors and to territorial, but more tolerant, close kin. On one hand, territoriality and competition for resources led us to predict a positive association between local colony density and female GC levels. On the other, higher tolerance of philopatric kin females and known fitness benefits led us to predict a negative association between kin numbers and female GC levels. We compared levels of fecal cortisol metabolites (FCMs) in females at two different spatial scales during lactation: local (a female’s core territory during lactation, 30-m radius about her nest burrow) and colony-wide. At the local scale, female FCM levels were neither related to colony density nor to the number of co-breeding female kin, but FCM levels increased with age. At the colony scale, female FCM levels varied in a quadratic fashion with female kin numbers. FCM levels decreased by 15% from 0 to 1 co-breeding kin present and increased with > 1 kin present. Among females that had only one co-breeding kin present, daughters (and littermate sisters and mothers, but not significantly) led to a 14% reduction in FCM levels compared with females that had no kin. Our results reject the idea that local colony density is associated with increased GC levels this species, but indicate subtle (positive and negative) effects of kin on individual GC secretion. They further call into question the importance of the nature of social relationships in modulating the stress experienced by individuals. Few studies have tested how the balance between positive (e.g. cooperation) and negative (e.g. competition) social interactions shapes individual stress and glucocorticoid (GC) levels in group-living animals. In colonial Columbian ground squirrels, breeding females are exposed to territorial neighbors and to more tolerant close kin. We show that kin numbers have subtle (positive and negative) effects on female GC levels. Compared with breeding females with no kin, female GC levels decrease by 15% with the presence of a single co-breeding close relative, but increase with the presence of more than one co-breeding related female. Among females that have only one co-breeding kin, the presence of daughters (and littermate sisters and mothers, but not significantly) leads to a 14% reduction in female GC levels. Our results highlight how GC levels may be influenced by the specific nature of social relationships in group-living animals.

Foraging in honeybees is energetically demanding. Here, we examined whether stressors, which generally increase metabolic demands, can impair foraging performance. A controlled non-pathogenic stressor (immune challenge) resulted in a change in the foraging preferences of bees. It reduced pollen foraging and increased the duration of trips in pollen foragers. Stress also reduced the amount of octopamine in the brain of pollen foragers (a biogenic amine involved in the regulation of foraging and flight behaviour in insects). According to the literature, flight metabolic rate is higher during pollen foraging than during nectar foraging, and nectar gives a higher energetic return relative to the foraging effort when compared with pollen. We thus propose that stress might be particularly detrimental to the performance of pollen foragers, and stressed bees prefer the energy-rich resource of nectar. In conclusion, stress, even at low levels, could have consequences for bee foraging behaviour and thereby the nutritional balance of the colony.

Since climate change is expected to bring more severe and frequent extreme weather events such as heat waves, assessing the physiological and behavioural sensitivity of organisms to temperature becomes a priority. We therefore investigated the responses of honeybees, an important insect pollinator, to simulated heat waves (SHW). Honeybees are known to maintain strict brood thermoregulation, but the consequences at the colony and individual levels remain poorly understood. For the first time, we quantified and modelled colony real-time activity and found a 70% increase in foraging activity with SHW, which was likely due to the recruitment of previously inactive bees. Pollen and nectar foraging was not impacted, but an increase in water foragers was observed at the expense of empty bees. Contrary to individual energetic resources, vitellogenin levels increased with SHW, probably to protect bees against oxidative stress. Finally, though immune functions were not altered, we observed a significant decrease in deformed wing virus loads with SHW. In conclusion, we demonstrated that honeybees could remarkably adapt to heat waves without a cost at the individual level and on resource flow. However, the recruitment of backup foraging forces might be costly by lowering the colony buffering capacity against additional environmental pressures.

In a rapidly changing environment, honeybee colonies are increasingly exposed to diverse sources of stress (e.g., new parasites, pesticides, climate warming), which represent a challenge to individual and social homeostasis. However, bee physiological responses to stress remain poorly understood. We therefore exposed bees specialised in different tasks (nurses, guards and foragers) to ancient (immune and heat stress) or historically more recent sources of stress (pesticides), and we determined changes in the expression of genes linked to behavioural maturation (vitellogenin – vg and juvenile hormone esterase – jhe) as well as in energetic metabolism (glycogen level, expression level of the receptor to the adipokinetic hormone – akhr, and endothermic performance). While acute exposure to sublethal doses of two pesticides did not affect vg and jhe expression, immune and heat challenges caused a decrease and increase in both genes, respectively, suggesting that bees had responded to ecologically relevant stressors. Since vg and jhe are expressed to a higher level in nurses than in foragers, it is reasonable to assume that an immune challenge stimulated behavioural maturation to decrease potential contamination risk and that a heat challenge promoted a nurse profile for brood thermoregulation. All behavioural castes responded in the same way. Though endothermic performances did not change upon stress exposure, the akhr level dropped in immune and heat-challenged individuals. Similarly, the abdomen glycogen level tended to decline in immune-challenged bees. Altogether, these results suggest that bee responses are stress specific and adaptive but that they tend to entail a reduction of energetic metabolism that needs to be studied on a longer timescale.

Nest drifting is often observed in honeybees (Apis mellifera) and can be detrimental to neighbouring colonies because it has the potential to increase disease transmission. However, the characteristics of drifting behaviour over a honeybee’s lifetime and the influence of parasitism on this phenomenon have been insufficiently investigated. Using optical bee counters, we tracked the drifting behaviour of workers that were either infected with the parasite Nosema ceranae or uninfected. Approximately 10 % of the tracked bees drifted into a foreign colony. The drifting prevalence was influenced by the colony’s location in space but not by N. ceranae parasitism. However, the number and duration of drifts changed over the lifetime of the bees and the season, and parasitism had an effect on drifters, with Nosema-infected bees performing more but shorter drifts. This phenomenon was more pronounced in old bees (+62 and −15 % for the number and duration of drifts, respectively) and could potentially be explained by the energetic stress induced by the parasite. In conclusion, combining a detailed analysis of drifting behaviour with the actual risk of newly established disease in colonies will benefit our knowledge of bee epidemiology.

National audience

International audience; As the number of breeding pairs depends on the adult sex ratio in a monogamousspecies with biparental care, investigating sex-ratio variability in natural populationsis essential to understand population dynamics. Using 10 years of data (2000–2009) in a seasonally monogamous seabird, the king penguin (Aptenodytespatagonicus), we investigated the annual sex ratio at fledging, and the potentialenvironmental causes for its variation. Over more than 4000 birds, the annual sexratio at fledging was highly variable (ranging from 44.4% to 58.3% of males), and onaverage slightly biased towards males (51.6%). Yearly variation in sex-ratio biaswas neither related to density within the colony, nor to global or local oceanographicconditions known to affect both the productivity and accessibility of penguinforaging areas. However, rising sea surface temperature coincided with an increasein fledging sex-ratio variability. Fledging sex ratio was also correlated withdifference in body condition between male and female fledglings. When moremales were produced in a given year, their body condition was higher (andreciprocally), suggesting that parents might adopt a sex-biased allocation strategydepending on yearly environmental conditions and/or that the effect ofenvironmental parameters on chick condition and survival may be sex-dependent.The initial bias in sex ratio observed at the juvenile stage tended to return to 1:1equilibrium upon first breeding attempts, as would be expected from Fisher’sclassic theory of offspring sex-ratio variation.

Providing cognitive challenges to zoo-housed animals may provide enriching effects and subsequently enhance their welfare. Primates may benefit most from such challenges as they often face complex problems in their natural environment and can be observed to seek problem solving opportunities in captivity. However, the extent to which welfare benefits can be achieved through programmes developed primarily for cognitive research is unknown. We tested the impact of voluntary participation cognitive testing on the welfare of a socially housed group of crested macaques (Macaca nigra) at the Macaque Study Centre (Marwell Zoo). First, we compared the rate of self-directed and social behaviours on testing and non-testing days, and between conditions within testing days. Minimal differences in behaviour were found when comparing testing and non-testing days, suggesting that there was no negative impact on welfare as a result of cognitive testing. Lipsmacking behaviours were found to increase and aggressive interaction was found to decrease in the group as a result of testing. Second, social network analysis was used to assess the effect of testing on associations and interactions between individuals. The social networks showed that testing subjects increased their association with others during testing days. One interpretation of this finding could be that providing socially housed primates with an opportunity for individuals to separate from the group for short periods could help mimic natural patterns of sub-group formation and reunion in captivity. The findings suggest, therefore, that the welfare of captive primates can be improved through the use of cognitive testing in zoo environments.

International audience