Honeybee queen exposure to a widely used fungicide disrupts reproduction and colony dynamic.

Pollinators have to cope with a wide range of stressful, not necessarily lethal factors limiting their performance and the ecological services they provide. Among these stressors are pesticides, chemicals that are originally designed to target crop-harming organisms but that also disrupt various functions in pollinators, including flight, communication, orientation and memory. Although all these functions are crucial for reproductive individuals when searching for mates or nesting places, it remains poorly understood how pesticides affect reproduction in pollinators. In this study, we investigated how a widely used fungicide, boscalid, affects reproduction in honey bees (Apis mellifera), an eusocial insect in which a single individual, the queen, fulfills the reproductive functions of the whole colony. Boscalid is a succinate dehydrogenase inhibitor (SDHI) fungicide mainly used on rapeseed flowers to target mitochondrial respiration in fungi but it is also suspected to disrupt foraging-linked functions in bees. We found that immature queen exposure to sublethal, field relevant doses of boscalid disrupted reproduction, as indicated by a dramatic increase in queen mortality during and shortly after the nuptial flights period and a decreased number of spermatozoa stored in the spermatheca of surviving queens. However, we did not observe a decreased paternity frequency in exposed queens that successfully established a colony. Queen exposure to boscalid had detrimental consequences on the colonies they later established regarding brood production, Varroa destructor infection and pollen storage but not nectar storage and population size. These perturbations at the colony-level correspond to nutritional stress conditions, and may have resulted from queen reduced energy provisioning to the eggs. Accordingly, we found that exposed queens had decreased gene expression levels of vitellogenin, a protein involved in egg-yolk formation. Overall, our results indicate that boscalid decreases honey bee queen reproductive quality, thus supporting the need to include reproduction in the traits measured during pesticide risk assessment procedures.

Microbiota composition and diversity of multiple body sites vary according to reproductive performance in a seabird.

The microbiota is suggested to be a fundamental contributor to host reproduction and survival, but associations between microbiota and fitness are rare, especially for wild animals. Here, we tested the association between microbiota and two proxies of breeding performance in multiple body sites of the black-legged kittiwake, a seabird species. First we found that, in females, nonbreeders (i.e., birds that did not lay eggs) hosted different microbiota composition to that of breeders in neck and flank feathers, in the choanae, in the outer-bill and in the cloacae, but not in preen feathers and tracheae. These differences in microbiota might reflect variations in age or individual quality between breeders and nonbreeders. Second, we found that better female breeders (i.e., with higher body condition, earlier laying date, heavier eggs, larger clutch, and higher hatching success) had lower abundance of several Corynebacteriaceae in cloaca than poorer female breeders, suggesting that these bacteria might be pathogenic. Third, in females, better breeders had different microbiota composition and lower microbiota diversity in feathers, especially in preen feathers. They had also reduced dispersion in microbiota composition across body sites. These results might suggest that good breeding females are able to control their feather microbiota-potentially through preen secretions-more tightly than poor breeding females. We did not find strong evidence for an association between reproductive outcome and microbiota in males. Our results are consistent with the hypothesis that natural variation in the microbiota is associated with differences in host fitness in wild animals, but the causal relationships remain to be investigated.

Sex and hatching order modulate the association between MHC-II diversity and fitness in early-life stages of a wild seabird.

Genes of the major histocompatibility complex (MHC) play a pivotal role in parasite resistance, and their allelic diversity has been associated with fitness variations in several taxa. However, studies report inconsistencies in the direction of this association, with either positive, quadratic or no association being described. These discrepancies may arise because the fitness costs and benefits of MHC diversity differ among individuals depending on their exposure and immune responses to parasites. Here, we investigated in black-legged kittiwake (Rissa tridactyla) chicks whether associations between MHC class-II diversity and fitness vary with sex and hatching order. MHC-II diversity was positively associated with growth and tick clearance in female chicks, but not in male chicks. Our data also revealed a positive association between MHC-II diversity and survival in second-hatched female chicks (two eggs being the typical clutch size). These findings may result from condition-dependent parasite infections differentially impacting sexes in relation to hatching order. We thus suggest that it may be important to account for individual heterogeneities in traits that potentially exert selective pressures on MHC diversity in order to properly predict MHC-fitness associations.

Red coloration varies with dietary carotenoid access and nutritional condition in kittiwakes.

Carotenoid-based ornaments are common signaling features in animals. Although the mechanisms that link color-based signals to individual condition is key to understanding the evolution and function of these ornaments, they are most often poorly known. Several hypotheses have been posited. They include: (i) the role of foraging abilities on carotenoid acquisition and thereby carotenoid-based ornaments, and (ii) the role of internal processes linked to individual quality on the allocation and conversion of carotenoids in integuments. Here, we tested the influence of dietary carotenoid access versus internal process on gape coloration in black-legged kittiwakes (Rissa tridactyla). This seabird displays a vibrant red gape, whose coloration varies with individual quality in males and is due to the deposition of red ketocarotenoids, such as astaxanthin. We decreased hydroxycarotenoid and ketocarotenoid levels in plasma, but increased efficiency in internal processes linked to nutritional condition, by supplementing breeding males with capelin, a natural energy-rich fish prey. We found that, despite having lower carotenoid levels in plasma, supplemented birds developed redder coloration than control birds, but only in the year when dietary levels of astaxanthin in the natural diet were low. In contrast, in the astaxanthin-rich year, supplemented males had a less-red gape than unsupplemented birds. These results suggest that inter-individual differences in internal processes may be sufficient to maintain the honesty of gape coloration under conditions of low dietary astaxanthin levels. Nonetheless, when inter-individual variations in dietary astaxanthin levels are elevated (such as in the crustacean-rich year), carotenoid access seems a more limiting factor to the expression of gape coloration than internal processes. Therefore, our study revealed a complex mechanism of gape color production in kittiwakes, and suggests that the main factor maintaining the condition dependency of this ornaments may vary with environmental conditions and diet composition.

Emotional responses to conspecific distress calls are modulated by affiliation in cockatiels (Nymphicus hollandicus).

Vocal communication is used across the animal kingdom to transfer information from emitters to receivers, such as size, sex, age, dominance status or even emotional states. The transmission of an emotional state from one individual to another is called "emotional contagion" and is classified as the first level of empathy. Emotional contagion is thought to be stronger between familiar individuals. While affiliation represents a stronger relation between individuals than mere familiarity, it remains understudied whether affiliation modulates emotional reactions as well. Using cockatiels (Nymphicus hollandicus), we played back three types of audio stimuli to individual birds: a partner's distress call (emitted when birds are caught or forcibly restrained), a non-partner's distress call, and a control sound (white noise). The calls were recorded from familiar birds with either low (non-partners) or high levels of affiliation (partners). The subjects' response was scored using four behavioural parameters: the time spent near the loudspeaker, the amount of movements, the number of calls emitted, and the position of the crest. Across all variables, birds were more attentive and active when confronted to distress calls compared to control sounds, particularly when the distress call was emitted from a partner rather than a non-partner. These results raise the possibility that distress calls do not only function as a stimulus-triggering automatic reaction in cockatiels but also transmit emotions. Moreover, affiliation enhanced emotional reactions to conspecific distress calls. Our data provides first insights into the mechanisms of emotional contagion in parrots.