Retro-observatories of animal biodiversity during the Anthropocene: how have global changes affected populations and communities? – REPAST

The REPAST project adopts an innovative approach by using guano accumulations as natural archives to reconstruct the impact of anthropogenic pressures on bats over time. These sedimentary deposits provide a chronology of environmental and biological conditions, exploited through methods derived from paleoecology, molecular biology, and analytical chemistry.

Dating and environmental reconstruction

The guano cores collected from several sites in Bourgogne-Franche-Comté are dated using radiometric methods (carbon-14, lead and cesium isotopes). The analysis of pollen contained in these sediments allows for the reconstruction of past landscapes and the identification of changes in hunting areas. In parallel, chemical analyses assess the exposure of bats to various contaminants (heavy metals, pesticides, persistent organic pollutants) over several decades.

Genetic diversity and diet

DNA extracted from guano reveals the evolution of genetic diversity in bats. The analysis of genetic markers allows for the detection of losses in diversity, indicative of critical demographic events. The DNA of insects contained in guano is also studied to reconstruct the evolution of bats' diet and understand the impact of environmental changes on their trophic resources.

Modeling interactions

The collected data are integrated into statistical models to identify the links between environmental pressures and biological responses. These models allow for the assessment of the cumulative effect of pollution, habitat changes, and climate on bat populations, by identifying critical periods of decline.

Overcoming technical challenges

One of the main challenges is the analysis of ancient and fragmented DNA, resulting from mixtures of multiple individuals. To limit biases, rigorous sequencing and authentication protocols are implemented. Similarly, chemical analyses are carefully calibrated to ensure reliable results.

Thanks to this interdisciplinary approach, REPAST offers a unique perspective on the impacts of human activities on biodiversity and serves as a valuable tool for better anticipating future threats and adapting conservation strategies.

The REPAST project made it possible to trace the impact of human activities on European bats through the analysis of guano cores accumulated in their colonies. These natural archives have revealed major transformations in their habitats, dietary patterns, and genetic diversity, highlighting the cumulative effects of anthropogenic pressures and pollution over the decades.

The results confirm a drastic decline in bat populations between 1950 and 1970, a period marked by agricultural intensification, the massive use of pesticides, and the destruction of natural habitats. If some species have shown stabilization since the 1990s, their numbers remain significantly lower than those before the war, reflecting the lasting impact of these disturbances.

The analysis of pollutants contained in guano revealed high concentrations of toxic substances such as DDT, lindane, neonicotinoids, and various heavy metals. The accumulation of these pollutants coincides with periods of population decline, suggesting a direct link with the decrease in survival and reproduction of bats. These contaminants, although some have been banned for decades, remain present in the environment and continue to affect wildlife.

Palynological studies have highlighted significant changes in the landscape during the 20th century, with a decrease in meadows in favor of intensive crops and planted forests. At the same time, the DNA of insects found in the guano shows a decline in beetles and orthopterans, the main prey of bats, replaced by less nutritious dipterans. This modification of food resources has probably contributed to weakening the populations by reducing the availability of prey suited to their energy needs.

The genetic analysis of guano revealed a gradual loss of genetic diversity in certain populations. Several genetic variants present before 1950 have disappeared, which could limit the bats' ability to adapt to new threats, such as climate change and the emergence of new diseases. This genetic erosion underscores the importance of preserving viable populations to ensure their long-term resilience.

The results of REPAST provide essential data to guide conservation policies. They highlight the need to preserve habitats favorable to bats, particularly grasslands and wetlands, to better regulate the use of pesticides, and to protect breeding and hibernation sites. These studies also illustrate the value of natural archives, such as guano, for reconstructing past environmental impacts and better anticipating future challenges.

The REPAST project opens numerous perspectives, both in fundamental and applied research. The innovative approach developed during the project, which relies on the exploitation of natural guano deposits as ecological and genetic archives, paves the way for new investigations on other taxa and environments. By extending this methodology to other bat species, as well as to colonial birds or mammals with fixed roosts, it would be possible to reconstruct population dynamics on a large scale and over long periods, far beyond conventional monitoring.

From a scientific perspective, REPAST provides a detailed temporal framework on the evolution of bat populations in Europe, documenting their decline, the environmental factors involved, and their impacts on genetic diversity. This framework can be used to test more refined hypotheses on the influence of environmental changes on biodiversity and to refine models for predicting future declines. Furthermore, the generated databases will be valuable for the scientific community, enabling comparative analyses on an international scale and facilitating the cross-referencing with other environmental indicators.

One of the major axes for extending the project is the improvement of dating and quantification methods for pollutants in organic deposits, in order to further refine the temporal resolution and clarify the causal links between pollution and population decline. Future research could also explore in more detail the physiological response of bats to the accumulation of contaminants, particularly through molecular biology approaches to study the epigenetic signatures left by these exposures.

On the conservation front, the project's results will provide robust arguments to strengthen the protection of bats and their habitats. By highlighting the impact of pesticides, landscape modifications, and climate on these species, REPAST fuels the debate on the need to more strictly regulate the use of chemicals and to create spaces favorable to wildlife. This data will be made available to natural space managers and biodiversity stakeholders to support protection actions.

Finally, REPAST has demonstrated the value of biological archives for documenting recent ecological history and raising public awareness about the challenges of biodiversity preservation. The continuation of collaborations with site managers and naturalist associations will allow for the integration of this data into participatory frameworks and encourage the collection and conservation of biological samples with a long-term research perspective.

Pressures on ecosystems have reached such an unprecedented rate that many ecosystems have been irreversibly damaged and that many animal populations have declined since the 1950s. Although human pressures on ecosystems have been identified, the mechanisms of biodiversity decline (i.e. relative importance of each pressure in the decline, temporality of events…) are poorly known. One reason is the lack of long-term data on population monitoring to study the impact of human pressures from past to present on animal populations and communities. REPAST proposes to use a retrospective multidisciplinary approach to study the impact of environmental pressures on the decline of bats through the study of guano cores collected in bat roosts. In caves or buildings, bat droppings (guano) fall to the ground and accumulate chronologically until reaching substantial thickness over time, and constitute historical archives containing temporally situated information about bat populations, environmental context, and human pressures. REPAST will test the general hypothesis that one or several stressors (habitat and climate changes, exposure to pollutants) will be associated to temporal variations of biological responses (pathogen prevalence, shift in diet, genetic diversity, bat richness). On 10 cores already sampled in bat colonies located in Burgundy Franche-Comté region, a robust chronology based on proxies used for paleoecological studies (14C, 137Cs, 210Pb concentrations) will be performed. The feasibility study done within the last 2 years shows that the cores date back from at least the 1950s, one being much older. Temporal variations of some anthropogenic pressures will also be reconstructed. Pollens will be studied on the cores to reconstruct the foraging areas (habitat) characteristics. The concentrations of some pollutants (~20 metals, 17 persistent organic pollutants including DDT and PCBs, and neonicotinoids) will be measured along the cores. Climate changes will be studied using meteorological data from 76 stations active since the 1940s across the region. Guano cores will also provide biological descriptors of bat colonies, which will be related to human pressures indices. The richness and composition of bat colonies, their diet using a metabarcoding approach, their exposure to eukaryotic pathogens, and their genetic diversity (using guano and Museum specimens already collected) will be reconstructed over time. Finally, historical archives and current counts from NGOs working in bat conservation will allow reconstructing the pattern of demographic trends and extinction risk of bat species since the 1940s. As the various anthropogenic pressures may act directly or indirectly on the biological responses, the complex set of variables measured in REPAST will be analysed using the structural equation modelling (SEM) framework. SEM’s causal diagrams will be constructed, based on explicit causal assumptions/hypotheses related to the mechanisms supposed to be involved between one or several pressures to one or several biological responses. The nature and the pattern of associations (what stressor(s) is(are) linked to what response(s) and how (from long and continuous associations to sudden shifts)) will improve our understanding of the mechanism(s) of bat decline. NGOs and stakeholders of bat roosts will be fully involved in the project and have already took part in the sampling process and share their data (e.g. bat counts). Apart from the classical scientific exploitation of the results (international meetings and articles), the large public will also be informed and invited to participate (e.g. in indicating colonies with guano accumulation unknown from NGOs) through a specific website and conferences. REPAST will allow gaining insights in the understanding of the mechanisms underlying the decline and the temporality of bat decline (and resilience) and, as some of the stressors still occur, may allow to predict and prevent new declines.