Breeding during a Predation Regime Shift : Behavioural and physiological responses of female common eiders facing the recovery of their native predator

Predation is a key selective force driving prey trait evolution. Yet, the extent to which predator-consumptive and predation risk effects shape phenotypes is still poorly understood. Since predation risk increases the cost of current reproduction, long-lived prey are predicted to prioritize survival and future reproduction by reducing reproductive investment under high predation risk (e.g., through changes in life-history, behaviour, physiology or morphology). However, the relative roles played by adaptive plastic responses (i.e., withinindividual phenotypic variation) and selective processes (i.e., among-individual phenotypic variation) in allowing populations and individuals to persist under fluctuating predation threat in the wild have been overlooked. In my thesis, I shed light on these knowledge gaps by evaluating the responses of a sea duck species, the common eider Somateria mollissima, to fluctuating predation risk from their native predator, the white-tailed eagle Haliaeetus albicilla. I focused on adjustments of behavioural and physiological traits to the recovery of white-tailed eagles in southwestern Finland. As a longlived species characterised by energetically-costly fasting during incubation and frequent intermittent breeding, common eiders are ideal for studying the life-history trade-off between reproduction and survival. I relied on a longterm individual-based monitoring of breeding females (> 2500 breeding attempts from > 1000 individuals in 2008-2022) to explore variations in risktaking behaviour (measured by flight initiation distance) and physiological proxies of energy allocation (baseline corticosterone levels) and parental effort (baseline prolactin levels) in response to temporally and spatially variable predation risk. The longitudinal data collection was not restricted to the focal variables, but also integrated a monitoring of female characteristics (e.g., age, body condition and clutch size) and parameters such as nesting microhabitat and fine- and large-scale predation risk indices, allowing a good understanding of concurrent changes occurring in the population. First, in agreement with the prediction that long-lived prey should reduce parental investment under elevated predation threat, I found that increasing predation threat was associated with longer flight initiation distances (i.e., reduced risk-taking) over breeding attempts. Importantly, this response was explained by a plastic adjustment of flight initiation distance to the risk of predation on breeding females, but also by the selective disappearance of risktaking phenotypes from islands characterised by high nest predation risk. Supporting the latter notion, I showed that risk-taking strategies affected fitness (including survival, breeding propensity and hatching success), especially under elevated predation risk. My results thus provide among the first evidence that the target of predation (adults or offspring) determines the mechanisms driving adjustment of risk-taking propensity to perceived predation risk. In risky environments, females were also more likely to rely on prior experience with a threat to dampen their flight response when repeatedly confronted with a harmless stimulus (here, a human approach over consecutive days). Such short-term habituation to non-life-threatening stimuli is likely adaptive and could limit the reproductive costs of an overreaction to benign stimuli. Second, I found that baseline corticosterone levels were positively associated with reproductive investment. In addition, baseline corticosterone levels were downregulated when incubating under high predator activity, again reflecting decreased energetic reproductive investment under threat of predation. Additionally, this physiological adjustment was habitat-dependent, as females downregulated baseline corticosterone levels under higher predation risk on themselves on open islands (associated with lower adult survival) but not on forested islands where nests are visually concealed from predators. Last, while I predicted that incubating females would display lower baseline prolactin levels – mediating reduced parental effort – under high predation threat, this prediction was not directly supported by my results. However, elevated baseline prolactin levels were still found to be indirectly related to predation pressure. Indeed, elevated prolactin levels seemed to promote hatching success in years characterised by elevated predation pressure. Overall, high prolactin levels favoured hatching success under constraining extrinsic (e.g., poor climatic conditions) or intrinsic conditions (e.g., when incubating a large clutch). Thus, the results drawn from my thesis provide valuable insight into the short- and long-term responses of prey individuals and populations to a changing predation regime. Interestingly, most of the observed responses seemed to be driven by within-individual adjustments of behaviour or physiology to perceived predation threat, supporting the idea that predation risk effect may be more important in explaining prey trait evolution than predatorconsumptive effects. However, even though longitudinal studies carried out in the wild have the advantage of encompassing the complexity of natural processes by integrating concomitant changes in intrinsic or extrinsic factors, these studies remain correlational, and further experimental work is needed to assess the causal links between predation risk and prey responses. Nevertheless, my results have far-reaching implications for conservation, by improving the knowledge on seabird responses to fluctuating predation risk from a native avian predator.Predationen driver evolutionen av bytesdjurs egenskaper, men de direkta och indirekta predationseffekternas roll är omdebatterad. Eftersom predationsrisken ökar kostnaden för nuvarande reproduktion, förväntas långlivade bytesdjur prioritera överlevnad och framtida reproduktion genom minskad reproduktiv investering under hög predationsrisk (via förändringar i livshistoria, beteende, fysiologi eller morfologi). Dock är den relativa betydelsen av adaptiva plastiska reaktioner (inom-individuell fenotypisk variation) och selektion (fenotypisk variation mellan individer) föga kända vid anpassningen till varierande predationstryck. Jag fyller dessa kunskapsluckor genom att utvärdera hurdana beteendemässiga och fysiologiska responser ejdern Somateria mollissima uppvisar på fluktuerande predationsrisk från sin naturliga predator, havsörnen Haliaeetus albicilla, vars population snabbt återhämtat sig i sydvästra Finland. Eftersom ejdern är långlivad, genomgår en energimässigt påfrestande ruvning och regelbundet avstår från häckning, är den idealisk för att studera livshistorieavvägningen mellan reproduktion och överlevnad. Min avhandling bygger på en individuell långtidsuppföljning av häckande ådor (> 2500 häckningsförsök; > 1000 individer; t2008-2022) och m.h.a. dessa data undersökte jag hur risktagningsbenägenheten (flyktavstånd från boet), energiallokeringen (grundnivån av kortikosteron) och investeringen i omvårdnad av avkomman (grundnivån av prolaktin) beror på temporärt och rumsligt varierande predationsrisk. Data omfattade även andra individuella egenskaper (t.ex. ålder, kroppskondition och kullstorlek), häckningsmikrohabitat och fin- och storskaliga predationsriskindex, för att kunna följa upp andra förändringar som skett i populationen. Långlivade bytesdjur förväntas minska investeringen i reproduktion under förhöjt predationshot, och i enlighet med detta fann jag att ett ökat predationshot var förknippat med längre flyktavstånd från boet (minskat risktagande) mellan upprepade häckningsförsök. Detta förklarades av en plastisk justering av flyktavståndet till predationsrisk riktad mot häckaren själv, men också av ett selektivt bortfall av risktagande fenotyper på öar med hög bopredationsrisk. Sammantaget påverkade risktagningsstrategierna fitness (överlevnad, häckningsbenägenhet och häckningsutfall), i synnerhet då predationsrisken var hög. Dessa resultat utgör ett av de första bevisen på att målet för predation (vuxna individen eller avkomman) formar de mekanismer som driver anpassningen av risktagningsbenägenhet till predationsrisk. I farliga miljöer var ådorna också mer benägna att förlita sig på tidigare erfarenhet av predationshot, vilket dämpade flyktresponsen under upprepade konfrontationer med ett ofarligt stimulus (människa) under samma häckning. Kortvarig habituering till icke-livshotande stimuli är adaptivt ifall det minskar de reproduktiva kostnaderna för att överreagera på godartade stimuli. Grundnivån av kortikosteron var positivt associerad med reproduktiv investering. Kortikosteronnivåerna minskade då rovdjursaktiviteten var hög, vilket återspeglar minskad energetisk reproduktiv investering under predationshot. Denna fysiologiska justering berodde på livsmiljön – ådorna hade en lägre kortikosteronnivå då de utsattes för ett predationshot på öppna öar (lägre vuxenöverlevnad) – men inte på skogsklädda öar, som erbjuder ett bättre skydd från rovdjur. Jag förutspådde att ruvande ådor skulle uppvisa lägre grundnivåer av prolaktin under högt predationshot – eftersom detta kunde styra en minskad satsning på omvårdnad av avkomman – en prediktion som inte stöddes av mina resultat. Prolaktinnivåerna visade sig dock vara indirekt relaterad till predationstrycket, eftersom en hög nivå främjade kläckningsframgången då predationstrycket var högt. Sammantaget gynnade höga prolaktinnivåer kläckningsframgången under krävande yttre (dåliga klimatförhållanden) eller inre förhållanden (stor kull). Mina resultat belyser hur bytesindivider och -populationer på kort och lång sikt reagerar på en förändrad predationsregim. De flesta responser berodde på inom-individuella anpassningar av beteende eller fysiologi till predationshot; alltså kan predationsrisken vara viktigare för att förklara evolutionen av bytesdjurs egenskaper än den direkta dödligheten. Trots att longitudinella studier tar hänsyn till komplexiteten i naturliga processer genom att integrera förändringar i inre eller yttre faktorer, är de ofta korrelativa. Därför behövs experiment för att identifiera kausaliteten mellan predationsrisk och bytesdjurens responser. Det oaktat är mina resultat bevarandebiologiskt värdefulla, genom att de förbättrar kunskapen om sjöfåglars responser på fluktuerande predationsrisk från en naturligt förekommande fågelpredator.La prédation agit comme une force de sélection majeure faisant évoluer les phénotypes des proies. Cependant, la mesure dans laquelle la consommation directe de proies par les prédateurs et le risque de prédation façonnent ces traits est encore méconnue. Etant donné que le risque de prédation augmente le coût de la reproduction, les espèces longévives devraient prioriser leur survie et leur reproduction future en réduisant leur investissement reproducteur lorsque le risque de prédation est élevé (par exemple en modifiant leurs traits d’histoires de vie, comportement, physiologie ou morphologie). Cependant, le rôle de la plasticité et de la sélection dans la capacité des populations et des individus à faire face à un risque de prédation fluctuant a été peu étudiée dans un contexte naturel. Dans ma thèse, j’ai mis ces mécanismes en lumière en évaluant les réponses d’un oiseau marin, l’eider à duvet Somateria mollissima, face au retour de son prédateur, le pygargue à queue blanche Haliaeetus albicilla. Cette espèce est idéale pour étudier les compromis entre reproduction et survie, notamment en raison de sa longue durée de vie et de sa capacité à jeûner durant l’incubation et à se reproduire de manière intermittente. A travers un suivi à long terme (2008-2022) j’ai exploré les modifications de comportement de prise de risque (mesurée à travers la distance de fuite) et d’indicateurs physiologiques d’allocation énergétique (évaluée via les niveaux basaux de corticostérone) et d’effort parental (mesuré via les niveaux basaux de prolactine) en réponse à une variation spatio-temporelle de la prédation. Ce jeu de données n’est pas restreint au suivi des variables d’intérêt mais inclut également les caractéristiques des individus (par exemple leur âge, condition corporelle ou taille de ponte), de leur nid, ou le risque de prédation à fine et large échelles, permettant de comprendre les divers changements se produisant simultanément dans la population. Tout d’abord, en accord avec la prédiction selon laquelle les proies longévives devraient réduire leur investissement parental lorsque la prédation est forte, j’ai montré qu’une augmentation de la prédation était associée à un allongement de la distance de fuite, indiquant une réduction de la prise de risque. Cette réponse est liée à une modification plastique (intraindividuelle) de la distance de fuite au risque de prédation des adultes, à laquelle s’ajoute une disparition sélective (inter-individuelle) des phénotypes associés à une forte prise de risque sur les îles où la prédation des nids est forte. En accord avec cette idée, j’ai mis en évidence un lien entre stratégie de prises de risque traits démographiques (survie, probabilité de se reproduire et succès à l’éclosion), en particulier lorsque la prédation est élevée. Mes résultats sont parmi les premiers à montrer que les mécanismes (plasticité ou sélection) façonnant les ajustements de prise de risque des individus dépendent de la cible des prédateurs (parents ou progéniture). A l’échelle intra-annuelle, les femelles nichant sur des îles où la predation est forte étaient, au contraire, plus susceptibles de réduire leur distance de fuite lorsqu’elles étaient confrontées de manière répétée à une tentative de prédation (une approche humaine répétée pendant plusieurs jours consécutifs). Cette habituation à court terme pourrait limiter les coûts reproductifs associés à l’expression d’une surréaction face à des stimuli stressants mais bénins. De plus, j’ai montré que les niveaux basaux de corticostérone étaient reliés positivement à l’investissement reproducteur. Les femelles incubant sous fort risque de prédation présentaient des niveaux plus faibles, reflétant de nouveau une réduction de l’investissement énergétique dans la reproduction. Cet ajustement physiologique dépendait de l'habitat, les femelles réduisant leurs niveaux basaux de corticostérone en cas de risque élevé de prédation sur ellesmêmes sur les îles ouvertes (associées à une survie adulte plus faible), mais pas sur les îles boisées où les nids sont dissimulés sous la végétation. Enfin, alors que j'avais prédit que les femelles présenteraient des niveaux basaux de prolactine plus bas (médiant une réduction de l'effort parental) en cas de risque de prédation élevé, aucune relation directe entre la prolactine et la prédation n’a été mise en évidence par mes résultats. Néanmoins, j’ai montré l’existence d’une relation indirecte entre les niveaux basaux de prolactine et la prédation. En effet, maintenir des niveaux basaux élevées de prolactine pendant l’incubation semble favoriser le succès à l’éclosion lorsque les conditions extrinsèques ou intrinsèques sont contraignantes. Cela inclut un risque de prédation élevé, de mauvaises conditions nutritives avant la reproduction, ou encore le fait d’incuber un grand nombre d’oeufs. Les résultats de ma thèse permettent ainsi de mieux comprendre les réponses à court et long terme des proies face à un changement de régime de prédation. Ces réponses semblent principalement résulter d'ajustements intra-individuels, soutenant l’idée selon laquelle le risque de prédation pourrait mieux prédire les évolutions des phénotypes que la consommation directe des proies par les prédateurs. Cependant, même si les études basées sur des suivis long-terme en milieu naturel ont l'avantage de prendre en compte la complexité des processus naturels, elles restent corrélationnelles, et des travaux expérimentaux sont maintenant nécessaires afin d’identifier les liens de cause à effet entre le risque de prédation et les réponses des proies. Mes résultats ont néanmoins des implications pour la conservation, en approfondissant les connaissances sur les réponses des oiseaux marins à une prédation fluctuante de la part d'un prédateur indigène

Drivers of within- and among-individual variation in risk-taking behaviour during reproduction in a long-lived bird

International audiencePlastic and selective mechanisms govern parental investment adjustments to predation threat. We investigated the relative importance of plasticity and selection in risk-taking propensity of incubating female common eiders Somateria mollissima facing unprecedented predation in SW Finland, Baltic Sea. Using a 12-year individual-based dataset, we examined within- and among-individual variation in flight initiation distance (FID), in relation to predation risk, nest detectability, individual traits and reproductive investment ( N FID = 1009; N individual = 559). We expected females nesting in riskier environments (higher predation risk, lower nest concealment) to mitigate environmentally imposed risk by exhibiting longer FIDs, and females investing more in current reproduction (older, in better condition or laying larger clutches) to display shorter FIDs. The target of predation—adult or offspring—affected the mechanisms adapting risk-taking propensity; females plastically increased their FID under higher adult predation risk, while risk-avoiding breeders were predominant on islands with higher nest predation risk. Risk-taking females selected thicker nest cover, consistent with personality-matching habitat choice. Females plastically attenuated their anti-predator response (shorter FIDs) with advancing age, and females in better body condition were more risk-taking, a result explained by selection processes. Future research should consider predator type when investigating the fitness consequences of risk-taking strategies

Vineyards, but not cities, are associated with lower presence of a generalist bird, the Common Blackbird (Turdus merula), in Western France

Abstract Background Land-use change is one of the main drivers of the global erosion of biodiversity. In that context, it is crucial to understand how landscape characteristics drive the presence of rare endangered species. Nevertheless, it is also important to study common species in multiple habitats, because they represent a large proportion of biodiversity and are essential to maintain ecological functions. Interestingly, some habitats, as farmlands with permanent crops (e.g. vineyards), have been overlooked in the literature. Methods In this study, we investigated the distribution of a widespread and common bird species, the Common Blackbird (Turdus merula), within and between the three main habitats of our study area (rural Western France). We specifically focused on (1) woodlands, (2) farmlands with a high vineyard coverage, and (3) moderately urbanized areas. Specifically, we aimed to assess the beneficial and detrimental effects of these habitats and their fine-scale composition on the presence of a common bird species, relying on a survey by point counts (nearly 100 locations). We studied the effects of habitats and gradients of fine-scale habitat composition on blackbird presence using logistic regression analyses. Results Blackbirds were present in all studied habitats. However, their presence varied between habitats, being lower in vineyards than in woodlands and cities. In woodlands and cities, fine-scale analyses did not reveal any component driving the species’ presence. However, we found that shrub and tree vegetation cover had a significant positive effect on blackbird presence in vineyards. Conclusions Our results are in agreement with the definition of a generalist species. Interestingly, species distribution varied between habitats. The high presence of blackbirds in urban areas suggests that medium-sized cities, despite their artificialization, do not constrain the settlement of this former forest specialist and that green spaces may allow blackbirds to thrive in medium-sized cities. On the contrary, we found an impoverished presence of blackbirds in vineyards and a positive effect of vegetation on their presence in these landscapes. This suggests that permanent crops, and more generally farmlands, may impose important constraints to common species. Future studies should examine how to enhance biodiversity through agricultural management policies, especially in vineyards

Short-term dehydration influences baseline but not stress-induced corticosterone levels in the house sparrow ( Passer domesticus )

International audienc

Breeding under pressure : Corticosterone is associated with reproductive investment under fluctuating predation risk in a long-lived sea duck

1. Phenotypic plasticity may enable individuals to cope with predictable and unpredictable environments during their life-cycle. In that context, studying glucocorticoids-corticosterone (CORT) in birds-is relevant because of their primary role in allostasis. Higher baseline CORT levels are classically associated with environmental constraints and lower fitness (the CORT-fitness hypothesis). However, in some environments, higher baseline CORT levels can promote reproduction, therefore being associated with higher fitness (the CORT-adaptation hypothesis). These two hypotheses have been tested in multiple systems but rarely in a context of fluctuating predation threat.2. We used a long-term individual-based monitoring of baseline CORT levels in female common eiders Somateria mollissima ( n(CORT) = 1537; n(individual) = 790; 2009-2022) to disentangle the context-dependent links between environmental conditions, CORT and fitness. Importantly, the study population has been facing a drastic increase in predation pressure over the past decades, linked to the recovery of the white-tailed eagle Haliaeetus albicilla. Additionally, eiders breed on open or forested islands, further affecting adult and nest predation risk. This system allowed us to disentangle the relative contributions of within-and among-individual variation in baseline CORT levels under predation.3. Supporting the CORT-adaptation hypothesis, baseline CORT levels were positively associated with reproductive investment (clutch size), age and hatching success. By partitioning within-and among-individual effects, we showed that at the individual level, CORT flexibly increased with clutch size and age. Females displaying higher CORT levels were more successful, suggesting a link between CORT and individual quality.4. At both the population and individual levels, baseline CORT levels decreased over the study period. This decrease was correlated with an increase in predation risk. Females had reduced baseline CORT when nesting under high eagle abundance or adult predation risk (within-individual effect). Interestingly, apparent plasticity towards adult predation risk was only observed on open islands, likely reflecting habitat-dependent strategies.5. Consistent with the CORT-adaptation hypothesis, we show that changes in predation regime not only correlate with changes in reproductive investment, but also with rapid plastic adjustment of glucocorticoid levels and therefore individual strategies to cope with predation risk. Given the correlative nature of our study, we encourage further experimental studies testing for a causal relationship between predation and corticosterone levels.Peer reviewe

High contamination of a sentinel vertebrate species by azoles in vineyards: a study of common blackbirds (Turdus merula) in multiple habitats in western France

Azoles represent the most used family of organic fungicides worldwide and they are used in agriculture to circumvent the detrimental impact of fungi on yields. Although it is known that these triazoles can contaminate the air, the soil, and the water, field data are currently and dramatically lacking to assess if, and to what extent, the use of triazoles could contaminate non-target wild vertebrate species, notably in agroecosystems. In this study, we aimed to document for the first time the degree of blood contamination of a generalist wild bird species by multiple azoles which are used for plant protection and fungi pest control in various habitats. We deployed passive air samplers and captured 118 Common blackbirds (Turdus merula) in an agroecosystem (vineyard), a protected forest, and a city in western France. We collected blood and analyzed the plasma levels of 13 triazoles and 2 imidazoles. We found that a significant percentage of blackbirds living in vineyards have extremely high plasma levels of multiple azoles (means (pg.g−1); tebuconazole: 149.23, difenoconazole: 44.27, fenbuconazole: 239.38, tetraconazole: 1194.16), while contamination was very limited in the blackbirds from the protected forest and absent in urban blackbirds. Interestingly, we also report that the contamination of blackbirds living in vineyard was especially high at the end of Spring and the beginning of Summer and this matches perfectly with the results from the passive air samplers (i.e., high levels of azoles in the air of vineyards during June and July). However, we did not find any correlation between the levels of plasma contamination by azoles and two simple integrative biomarkers of health (feather density and body condition) in this sentinel species. Future experimental studies are now needed to assess the potential sub-lethal effects of such levels of contamination on the physiology of non-target vertebrate species