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Climate change and phenology: long-term temporal dynamics of mutualistic ecological networks

Periodic Reporting for period 1 - TEMPNET (Climate change and phenology: long-term temporal dynamics of mutualistic ecological networks)

Reporting period: 2018-10-01 to 2020-09-30

The unprecedented environmental change produced by human activities is not only reducing biodiversity in terms of a number of species, but also by the extinction of interactions among them. These ecological interactions (such as herbivory, parasitism, plant pollination by insects, seed dispersal by frugivores, or competition) are the wireframe that sustains the Web of Life, providing functional links and allowing species co-existence. Unfortunately, ecological interactions are also being lost at a very fast pace, sometimes preceding species extinctions, and this disappearance of interactions might trigger the collapse of communities, yet most recent efforts for biodiversity conservation focus on species. Thus, unveiling the complexity of ecological interactions is fundamental for biodiversity conservation in an era of global threats imposed by human impacts.

The main aim of the TEMPNET action was to provide a deep understanding of how phenological changes in interacting plants and animals affect their dynamics over seasonal and long-term time spans. TEMPNET has combined two temporal scales (frequent intra-annual censuses and long-term replication with 37 yrs of time span) for comparing fruit-frugivore networks from the Doñana National Park (Spain). Using state-of-the-art mathematical advances in multilayer network analysis, sound ecological theory, and field observation, temporal changes in interactions between fruits and birds have been shown. The results of this action point out that frugivorous birds in Doñana are relatively in worse conditions nowadays than when compared with 1981-1983: they had less fat content, migrant species are scarcer and they migrate earlier, which can lead to a mismatch with fruiting plant species. We generated different models simulating phenological change and evaluated the prevalence of forbidden links, i.e. interactions that do not take place, irrespective of sampling effort. Results emphasize the role of phenological changes in the presence of forbidden links, with higher frequencies occurring when shifts were maintained over long temporal spans. Our results signal the vulnerability of mutualistic interactions to phenological shifts induced by global change and the need of including phenology in biodiversity assessments. Results of TEMPNET action have exploitable applications for biodiversity conservation in a context of global change. Moreover, tools of network analyses employed have also applications for a range variety of fields, including transportation, banking, computing, or the study of contagion dynamics of infectious diseases.
The research has been distributed in three work packages aimed at 1) an in-depth understanding of the temporal dynamics of ecological interactions; 2) predicting the prevalence of phenological disruptions and consequences for biodiversity conservation; and 3) producing informed forecasting of future impacts of climate change on the structure and function of biodiversity. For this, we have carried out a sampling of birds using mist nets from 2019 to 2021 in Doñana and linear 1-km brid transects for estimating bird diversity. Captured birds were ringed, assigned to a species, and measured. Birds’ feces were collected and the seed content was analyzed at the microscope. We have also marked plants and monitored their phenology for 2 years. This is a replication of the same protocol that was undertaken in 1981-1983 in the same area. The main interest of the TEMPNET action was to determine temporal changes in seed-dispersal networks and forecast future mismatches among interacting partners. The most important results show that there are important changes both in the avian and plant communities, affecting their interactions. For bird species, we have found a profound transformation of species composition, bird phenology, and body condition: in ~40 years, the avian community showed a 66% and 18.4% decrease of the wintering and seed-disperser species, respectively. Seasonal abundance peaks were advanced for at least one month in 9 of the 11 frugivorous bird species included in the analyses. Avian body condition during the migratory passage has worsened, with fewer individuals showing a high-fat percentage and good body condition now than in the past. There is also a reported decrease in fruit production of almost half in 2019-2021 compared to 1981-1983, probably linked to habitat encroachment by pine trees and replacement of fleshy-fruited shrubs. Vegetation encroachment and climate change are the most plausible explanations for the observed changes in the avian community, but the relative importance of these factors is yet unknown. Our results at a local scale mirror the dramatic consequences of global change affecting the diversity, phenology, and physical condition of frugivorous bird species reported in multiple studies across the globe.

Two journal articles related to the research activity in this project have been published so far (Ecosistemas, 29(2): 1995. DOI: 10.7818/ECOS.1995; Oikos 2022(2). doi:10.1101/2020.10.27.356709) plus a data repository (Dryad, DOI: 10.5061/dryad.p2ngf1vrt). Other two major additional publications are expected to be submitted in 2022, plus other secondary publications derived from undergoing collaborations. Results of this action have been presented at five communications at scientific conferences in 2018-2021. Dissemination activities of the action included two different participation in the Night of European Researchers (2019 and 2021), a workshop in the 7th Fair of Science in Jerez (2019), and several outreach talks related to the International Day of Woman in Science and Doñana to high school students. A promotional video, outreach publications, and press releases have also been delivered to disseminate the results of the action.
The COVID-19 pandemic crisis has highlighted more than ever the urgent need for a holistic approach to the ongoing environmental crisis. The underlying causes of biodiversity loss, climate change, food insecurity, and global health are all interlinked and related to human activities. Society needs to better understand how ecological interactions are going to be affected by climate change and the TEMPNET action has been a step forward in that direction. Results of this action have demonstrated that current communities have fewer links, are less biodiverse, and that phenological changes are affecting both the plants and the animals that interact.

Gaining more knowledge on the links that will be lost in the future due to more extreme climatic conditions is very helpful for trying to mitigate this by some compensatory actions or at least, trying to adapt our society to these new changes.

This action has implied a fundamental advance in network analyses by the inclusion of temporal dynamics in multilayer networks, a field that is still under strong development. Applications of networks in our everyday life are numerous, including the internet, banking, or transportation. Gaining insight into the theoretical basis of network models has a long-term benefit for society because it will help in the development of models that have a strong impact on our economy and welfare. Above all, the results of TEMPNET highlight the high vulnerability of current ecosystems to future scenarios in which very likely interaction mismatches will arrive.
Turdus philomelos bird captured for bird ringing and faecal analyses
bird ringing technique of Sylvia melanocephala
sampled feces
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