Adaptive niche-based sampling to improve ability to find rare and elusive species: Simulations and field tests

This is the peer reviewed version of the following article: Chiffard, Marciau, Yoccoz, Mouillot, Duchateau, Nadeau, Fontanilles, Besnard. Adaptive niche-based sampling to improve ability to find rare and elusive species: Simulations and field tests. Methods in Ecology and Evolution. 2020;11(8):899-909, which has been published in final form at https://doi.org/10.1111/2041-210X.13399. This article may be used for non-commercial purposes in accordance with Wiley Terms and Conditions for Use of Self-Archived Versions. Sampling efficiency is crucial to overcome the data crisis in biodiversity and to understand what drives the distribution of rare species.</li Adaptive niche‐based sampling (ANBS) is an iterative sampling strategy that relies on the predictions of species distribution models (SDMs). By predicting highly suitable areas to guide prospection, ANBS could improve the efficiency of sampling effort in terms of finding new locations for rare species. Its iterative quality could potentially mitigate the effect of small and initially biased samples on SDMs. In this study, we compared ANBS with random sampling by assessing the gain in terms of new locations found per unit of effort. The comparison was based on both simulations and two field surveys of mountain birds. We found an increasing probability of contacting the species through iterations if the focal species showed specialization in the environmental gradients used for modelling. We also identified a gain when using pseudo‐absences during first iterations, and a general tendency of ANBS to increase the omission rate in the spatial prediction of the species' niche or habitat. Overall, ANBS is an effective and flexible strategy that can contribute to a better understanding of distribution drivers in rare species. </ol

Song birds of mountain and alpine meadows as indicators of global changes

Du fait de la croissance démographique et économique de la population humaine, nos sociétés sont de plus en plus dépendantes de la nature, et plus précisément de certains processus biologiques regroupés sous le terme services écosystémiques. Comprendre les mécanismes de réponse des systèmes biologiques face aux changements globaux que nos activités induisent à plusieurs échelles est donc un enjeu scientifique et de société. Cette thèse a été pensée et réalisée en interaction avec plusieurs équipes de recherche et gestionnaires d’espaces naturels dans le cadre du développement d’un suivi temporel des oiseaux de montagne comme indicateurs des conséquences des changements globaux sur la biodiversité. Les massifs montagneux de France sont en effet exposés aux changements de climat et à l’évolution de l’élevage des grands herbivores, une activité exposée aux fluctuations des prix des matières premières et des aides publiques. Les forts gradients bioclimatiques « en facettes » (selon l’exposition) qui caractérisent des massifs montagneux font de ces espaces des modèles d’étude particulièrement intéressants pour étudier les effets des changements globaux sur la biodiversité, mais aussi fortement contingents. L’objet général de ma thèse est d’identifier et de quantifier le rôle respectif de la température, de la structure de la végétation, et des activités d’élevage, sur cette communauté d’oiseaux, afin de mieux comprendre quelles pourraient être les conséquences de changements majeurs de climat et d’usage des terres. Les gradients altitudinaux ont été historiquement étudiés de façon isolée et dans de grandes diversités d’habitats. Suivant les objectifs généraux de la thèse nous avons choisi d’adopter l’approche inverse dans le premier chapitre, en multipliant les sites d’études dans un habitat standardisé (1100 points d’écoute réalisés dans les Alpes et les Pyrénées). Nos résultats montrent que la ressource, la température et la structure de l’habitat influent fortement sur la communauté. De plus 5 des 8 espèces étudiées semblent favorisées par le pâturage. Dans le second chapitre, j’ai testé l’effet de la forte saisonnalité qui caractérise le climat des massifs montagneux tempérés, en testant son effet sur la survie individuelle dans une population de Chocards à bec jaune Pyrrhocorax graculus. Je me suis appuyé pour cela sur un suivi individuel (CMR) d’un millier d’individus mené pendant 30 ans par Anne Delestrade. Les Chocards présentent une survie forte et un patron saisonnier, en interaction avec le sexe des individus, avec une survie plus basse pour les femelles après les hivers et printemps chauds. J’ai ensuite présumé que les passereaux insectivores savent profiter des troupeaux en consommant des insectes coprophages. J’ai mesuré les ratios isotopiques stables de l’azote présents dans les fèces des oiseaux les plus communs pour estimer le niveau trophique de leurs proies, et ainsi tester cette hypothèse et quantifier le mécanisme. On observe dans les deux massifs un décalage très marqué vers le prélèvement d’insectes non-herbivores quand l’intensité de pâturage augmente. Le dernier chapitre évalue le potentiel d’échantillonnages itératifs basés sur des modèles de répartition d’espèces pour augmenter la probabilité de contacter une espèce rare dans de nouvelles localités. Cette étude comprend des simulations et un test de terrain dans les Pyrénées sur la Niverolle alpine Montifringilla nivalis et le Monticole de roche Monticolla saxatilis. Les résultats montrent le fort potentiel de la méthode en pratique, et ses limites, avec une augmentation de la spécificité au détriment d’une augmentation des omissions. En discussion générale, je propose des perspectives de recherche visant à généraliser le lien fort entre régime alimentaire des oiseaux de montagne et troupeaux de mammifères herbivores, et à mieux comprendre la phénologie des populations des pelouses d’altitude en fonction de l’enneigement.Growth of human populations and economy causes human societies to be more and more dependent on ecosystem services. Understand the mechanisms underlying the response of biological systems to global changes is thus a scientific and social issue. This research was thank and realized when developing a long term monitoring scheme for mountain birds with different research teams and conservation stakeholders. In this long term monitoring, birds are used as indicators of the effects of global changes on biodiversity. Mountain massifs of France are exposed to climate change, and land use evolution, as livestock grazing is dependent on raw material prices and public support. Mountains are interesting, but contingent, ecological contexts to study the effects of global changes on biodiversity, due to the sharp bioclimatic gradients and facet landscapes. My main objective was to characterize and quantify the respective effects of temperature, vegetation structure, and livestock grazing activities on this bird community, to better predict the consequences of major climate and land use changes. Elevation gradient have been mostly studied in isolated sites and large elevation gradients. Following our main objective, in the first chapter, we chose the opposite approach, by multiplying study sites in a standardized habitat (open grasslands, 1100 point counts in Alps and Pyrenees). Our results show that primary productivity, temperature and habitat structure all influence the bird community. Also 5 out of the 8 most common species seemed to be favorited by livestock grazing activities. In the second chapter, I tested the effect of the strong seasonality typical from temperate mountains’ climate, by testing it’s effect on the survival of individuals in a population of alpine Choughs Pyrrhocorax graculus. I relied on the CMR survey of more than 1000 individuals carried out by Anne Delestrade during 30 years. Choughs show the highest survival known in corvids, with a seasonal pattern, in interaction with individuals’ states like sex group. Adult females also showed lower spring survival after warm winters. In third chapter I speculated on the ability of insectivorous passerines to get benefit from the presence of large domestic herbivorous mammals, by eating coprophagous insects. I measured the stable nitrogen isotopic ratios in the feces of most common birds to provide an estimation of the trophic level of birds’ preys, and thus test my hypothesis and eventually quantify the mechanism. We observed, in both mountain massif, a shift from herbivorous from higher trophic level insects catched by birds, from locations with low grazing intensity to those with high grazing intensity. The last chapter present an evaluation of the potential of adaptive niche based sampling to increase the ability to find rare species in new localities. This study includes simulations and field test in the Pyrenees mountains on two alpine bird species, Snowfinch Montifringilla nivalis and rock Thrush Monticolla saxatilis. Results show the strong potential of the method in the field, and its limit, with an increase in specificity at the cost of omissions that also increase. As a general discussion, I develop research perspective to generalize the strong link found between birds’ diet and large mammalian herbivores, and to better understand the phenology of populations facing unpredictable snow cover during breeding period

Oiseaux chanteurs des milieux ouverts de montagne et changements globaux

Growth of human populations and economy causes human societies to be more and more dependent on ecosystem services. Understand the mechanisms underlying the response of biological systems to global changes is thus a scientific and social issue. This research was thank and realized when developing a long term monitoring scheme for mountain birds with different research teams and conservation stakeholders. In this long term monitoring, birds are used as indicators of the effects of global changes on biodiversity. Mountain massifs of France are exposed to climate change, and land use evolution, as livestock grazing is dependent on raw material prices and public support. Mountains are interesting, but contingent, ecological contexts to study the effects of global changes on biodiversity, due to the sharp bioclimatic gradients and facet landscapes. My main objective was to characterize and quantify the respective effects of temperature, vegetation structure, and livestock grazing activities on this bird community, to better predict the consequences of major climate and land use changes. Elevation gradient have been mostly studied in isolated sites and large elevation gradients. Following our main objective, in the first chapter, we chose the opposite approach, by multiplying study sites in a standardized habitat (open grasslands, 1100 point counts in Alps and Pyrenees). Our results show that primary productivity, temperature and habitat structure all influence the bird community. Also 5 out of the 8 most common species seemed to be favorited by livestock grazing activities. In the second chapter, I tested the effect of the strong seasonality typical from temperate mountains’ climate, by testing it’s effect on the survival of individuals in a population of alpine Choughs Pyrrhocorax graculus. I relied on the CMR survey of more than 1000 individuals carried out by Anne Delestrade during 30 years. Choughs show the highest survival known in corvids, with a seasonal pattern, in interaction with individuals’ states like sex group. Adult females also showed lower spring survival after warm winters. In third chapter I speculated on the ability of insectivorous passerines to get benefit from the presence of large domestic herbivorous mammals, by eating coprophagous insects. I measured the stable nitrogen isotopic ratios in the feces of most common birds to provide an estimation of the trophic level of birds’ preys, and thus test my hypothesis and eventually quantify the mechanism. We observed, in both mountain massif, a shift from herbivorous from higher trophic level insects catched by birds, from locations with low grazing intensity to those with high grazing intensity. The last chapter present an evaluation of the potential of adaptive niche based sampling to increase the ability to find rare species in new localities. This study includes simulations and field test in the Pyrenees mountains on two alpine bird species, Snowfinch Montifringilla nivalis and rock Thrush Monticolla saxatilis. Results show the strong potential of the method in the field, and its limit, with an increase in specificity at the cost of omissions that also increase. As a general discussion, I develop research perspective to generalize the strong link found between birds’ diet and large mammalian herbivores, and to better understand the phenology of populations facing unpredictable snow cover during breeding period.Du fait de la croissance démographique et économique de la population humaine, nos sociétés sont de plus en plus dépendantes de la nature, et plus précisément de certains processus biologiques regroupés sous le terme services écosystémiques. Comprendre les mécanismes de réponse des systèmes biologiques face aux changements globaux que nos activités induisent à plusieurs échelles est donc un enjeu scientifique et de société. Cette thèse a été pensée et réalisée en interaction avec plusieurs équipes de recherche et gestionnaires d’espaces naturels dans le cadre du développement d’un suivi temporel des oiseaux de montagne comme indicateurs des conséquences des changements globaux sur la biodiversité. Les massifs montagneux de France sont en effet exposés aux changements de climat et à l’évolution de l’élevage des grands herbivores, une activité exposée aux fluctuations des prix des matières premières et des aides publiques. Les forts gradients bioclimatiques « en facettes » (selon l’exposition) qui caractérisent des massifs montagneux font de ces espaces des modèles d’étude particulièrement intéressants pour étudier les effets des changements globaux sur la biodiversité, mais aussi fortement contingents. L’objet général de ma thèse est d’identifier et de quantifier le rôle respectif de la température, de la structure de la végétation, et des activités d’élevage, sur cette communauté d’oiseaux, afin de mieux comprendre quelles pourraient être les conséquences de changements majeurs de climat et d’usage des terres. Les gradients altitudinaux ont été historiquement étudiés de façon isolée et dans de grandes diversités d’habitats. Suivant les objectifs généraux de la thèse nous avons choisi d’adopter l’approche inverse dans le premier chapitre, en multipliant les sites d’études dans un habitat standardisé (1100 points d’écoute réalisés dans les Alpes et les Pyrénées). Nos résultats montrent que la ressource, la température et la structure de l’habitat influent fortement sur la communauté. De plus 5 des 8 espèces étudiées semblent favorisées par le pâturage. Dans le second chapitre, j’ai testé l’effet de la forte saisonnalité qui caractérise le climat des massifs montagneux tempérés, en testant son effet sur la survie individuelle dans une population de Chocards à bec jaune Pyrrhocorax graculus. Je me suis appuyé pour cela sur un suivi individuel (CMR) d’un millier d’individus mené pendant 30 ans par Anne Delestrade. Les Chocards présentent une survie forte et un patron saisonnier, en interaction avec le sexe des individus, avec une survie plus basse pour les femelles après les hivers et printemps chauds. J’ai ensuite présumé que les passereaux insectivores savent profiter des troupeaux en consommant des insectes coprophages. J’ai mesuré les ratios isotopiques stables de l’azote présents dans les fèces des oiseaux les plus communs pour estimer le niveau trophique de leurs proies, et ainsi tester cette hypothèse et quantifier le mécanisme. On observe dans les deux massifs un décalage très marqué vers le prélèvement d’insectes non-herbivores quand l’intensité de pâturage augmente. Le dernier chapitre évalue le potentiel d’échantillonnages itératifs basés sur des modèles de répartition d’espèces pour augmenter la probabilité de contacter une espèce rare dans de nouvelles localités. Cette étude comprend des simulations et un test de terrain dans les Pyrénées sur la Niverolle alpine Montifringilla nivalis et le Monticole de roche Monticolla saxatilis. Les résultats montrent le fort potentiel de la méthode en pratique, et ses limites, avec une augmentation de la spécificité au détriment d’une augmentation des omissions. En discussion générale, je propose des perspectives de recherche visant à généraliser le lien fort entre régime alimentaire des oiseaux de montagne et troupeaux de mammifères herbivores, et à mieux comprendre la phénologie des populations des pelouses d’altitude en fonction de l’enneigement

Grazing intensity drives a trophic shift in the diet of common alpine birds

Large mammalian herbivores (LMH) shape vertebrate communities and structure food webs in many terrestrial ecosystems. However, the mechanisms that underlie the effects of LMH on other vertebrates are poorly understood. In France, domestic LMH have grazed alpine and mountain grasslands for thousands of years, profoundly influencing landscapes and wildlife. As LMH modify habitat structure, favour coprophagous insects and compete with herbivorous insects, the diet of insectivorous alpine birds may be deeply influenced by LMH grazing intensity. To investigate this, we sampled common insectivorous birds faeces (water pipit Anthus spinoletta and wheatear Oenanthe oenanthe) in sites characterized by different levels of grazing intensity by domestic and wild herbivores, in the open landscapes of the southern French Alps and the western Pyrenees. We used isotopic discrimination based on nitrogen stable isotope ratios as an indicator of the trophic level of the arthropods found in bird faeces. From isotopic ratios, we found that bird diets shift from mainly herbivorous arthropods at sites of low grazing intensity, to one mainly composed of other groups, such as predatory, detritivorous or coprophagous arthropods, at sites of higher grazing intensity. This result highlights the strong trophic link between LMH and insectivorous birds in open landscapes, contributing to a better understanding of interactions between domestic grazing, an activity that has historically modelled European landscapes, and biodiversity, with particular relevance for landscape management and bird conservation

Exclusion in the field: wild brown skuas find hidden food in the absence of visual information

International audienceInferential reasoning by exclusion allows responding adaptively to various environmental stimuli when confronted with inconsistent or partial information. In the experimental context, this mechanism allows selecting correctly between an empty option and a potentially rewarded one. Recently, the increasing reports of this capacity in phylogenetically distant species have led to the assumption that reasoning by exclusion is the result of convergent evolution. Within one largely unstudied avian order, i.e. the Charadriiformes, brown skuas (Catharacta antarctica ssp lonnbergi) are highly flexible and opportunistic predators. Behavioural flexibility, along with specific aspects of skuas' feeding ecology, may act as influencing factors in their ability to show exclusion performance. Our study aims to test whether skuas are able to make choice by exclusion in a visual two-way object-choice task. Twenty-six wild birds were presented with two opaque cups, one covering a food reward. Three conditions were used: 'full information' (showing the content of both cups), 'exclusion' (showing the content of the empty cup), and 'control' (not showing any content). Skuas preferentially selected the rewarded cup in the full information and exclusion condition. The use of olfactory cues was excluded by results in the control condition. Our study highlights the cognitive potential of this predatory seabird and opens new investigations for testing further its cognition in the wild

Potential distribution of a climate sensitive species, the White-winged Snowfinch Montifringilla nivalis in Europe

The White-winged Snowfinch Montifringilla nivalis nivalis is assumed to be highly threatened by climate change, but this high elevation species has been little studied and the current breeding distribution is accurately known only for a minor portion of its range. Here, we provide a detailed and spatially explicit identification of the potentially suitable breeding areas for the Snowfinch.We modelled suitable areas in Europe and compared them with the currently known distribution.We built a distribution model using 14,574 records obtained during the breeding period that integrated climatic, topographic and land-cover variables, working at a 2-km spatial resolution with MaxEnt. The model performed well and was very robust; average annual temperature was the most important occurrence predictor (optimum between c.-3°C and 0°; unsuitable conditions below -10° and above 5°). The current European breeding range estimated by BirdLife International was almost three times greater than that classified as potentially suitable by our model. Discrepancies between our model and the distribution estimated by BirdLife International were particularly evident in eastern Europe, where the species is poorly monitored. Southern populations are likely more isolated and at major risk because of global warming. These differences have important implications for the supposed national responsibility for conservation of the species and highlight the need for new investigations on the species in the eastern part of its European range

Building spaces of interactions between researchers and managers: Case studies with wildlife monitoring and conservation in France

International audience1. To document and halt biodiversity loss, monitoring, quantifying trends and assessing management and conservation strategies on wildlife populations and communities are crucial steps. 2. With increasing technological innovations, more and more data are collected and new quantitative methods are constantly developed. These rapid developments come with an increasing need for analytical skills, which are hardly accessible to managers. On the other hand, researchers spend more and more time on research grant applications and administrative tasks, which leaves fewer opportunities for knowledge transfer. This situation tends to increase the gap between researchers and managers. Here, we illustrate how to fill this gap by presenting two long-term collaborations between a research unit—Centre for Functional and Evolutionary Ecology; CEFE—and a national agency—French Biodiversity Agency; OFB. 3. The first example is a collaboration providing statistical support to national parks for the design and implementation of scientific monitoring protocols. It relies on the recruitment of a research engineer funded by OFB and physically based at CEFE, who works closely with OFB and managers. The second example is a collaboration on the management of large carnivores. For more than 10 years, it has involved several PhD students and post-doctoral fellows co-supervised by CEFE and OFB, and has recently resulted in the recruitment of a permanent OFB researcher who works half-time at CEFE and half-time at OFB. These case studies illustrate the modalities of collaborative work between public institutions acting at different levels of biodiversity conservation for the co-construction of research agendas and the exchange of knowledge. 4. These collaborations also bring out some challenges. Inter-knowledge and mutual learning remain difficult at scales larger than that of the teams concerned. The staff working at this interface needs to possess good listening skills, respect all partners' needs and demonstrate flexibility. Knowledge exchanges require time, thus reducing productivity according to quantitative metrics such as scientific publications or institutional reports. These collaborations can therefore be difficult to assume socially, and remain tenuous because they rely on a good understanding of the differences in governance of the various partners. 5. Based on our experience, success is favoured by long-term and close relationships, and by co-construction of projects at early stage. Sharing a space (i.e. office or building) facilitates face-to- face interactions during planned work sessions and casual meetings that build up a shared scientific culture and mutual trust

The DeepFaune initiative: a collaborative effort towards the automatic identification of Europeanfauna in camera trap images

Camera traps have revolutionized how ecologists monitor wildlife, but their full potential is realized only when the hundreds of thousands of collected images can be readily classified with minimal human intervention. Deep-learning classification models have allowed extraordinary progress towards this end, but trained models remain rare and are only now emerging for European fauna. We report on the first milestone of the DeepFaune initiative (https://www.deepfaune.cnrs.fr), a large-scale collaboration between more than 50 partners involved in wildlife research, conservation and management in France. We developed aclassification model trained to recognize 26 species or higher-level taxa that are common in Europe, with an emphasis on mammals. The classification model achieved 0.97 validation accuracy and often >0.95 precision and recall for many classes. These performances were generally higher than 0.90 when tested on independent out-of-sample datasets for which we used image redundancy contained in sequences of images. We implemented our model in a software to classify images stored locally on a personal computer, so as to provide a free, user-friendly and high-performance tool for wildlife practitioners to automatically classify camera trap images. The DeepFaune initiative is an ongoing project, with new partners joining regularly,which allows us to continuously add new species to the classification model