The demographic causes of population change vary across four decades in a long-lived shorebird.

Understanding which factors cause populations to decline begins with identifying which parts of the life cycle, and which vital rates, have changed over time. However, in a world where humans are altering the environment both rapidly and in different ways, the demographic causes of decline likely vary over time. Identifying temporal variation in demographic causes of decline is crucial to assure that conservation actions target current and not past threats. However, this has rarely been studied as it requires long time series. Here we investigate how the demography of a long-lived shorebird (the Eurasian Oystercatcher Haematopus ostralegus) has changed in the past four decades, resulting in a shift from stable dynamics to strong declines (-9% per year), and recently back to a modest decline. Since individuals of this species are likely to respond differently to environmental change, we captured individual heterogeneity through three state variables: age, breeding status, and lay date (using integral projection models). Timing of egg-laying explained significant levels of variation in reproduction, with a parabolic relationship of maximal productivity near the average lay date. Reproduction explained most variation in population growth rates, largely due to poor nest success and hatchling survival. However, the demographic causes of decline have also been in flux over the last three decades: hatchling survival was low in the 2000s but improved in the 2010s, while adult survival declined in the 2000s and remains low today. Overall, the joint action of several key demographic variables explain the decline of the oystercatcher, and improvements in a single vital rate cannot halt the decline. Conservations actions will thus need to address threats occurring at different stages of the oystercatcher's life cycle. The dynamic nature of the threat landscape is further supported by the finding that the average individual no longer has the highest performance in the population, and emphasizes how individual heterogeneity in vital rates can play an important role in modulating population growth rates. Our results indicate that understanding population decline in the current era requires disentangling demographic mechanisms, individual variability, and their changes over time.

GPS tracking data of Eurasian oystercatchers (Haematopusostralegus) from the Netherlands and Belgium.

We describe six datasets that contain GPS and accelerometer data of 202 Eurasian oystercatchers (Haematopusostralegus) spanning the period 2008-2021. Birds were equipped with GPS trackers in breeding and wintering areas in the Netherlands and Belgium. We used GPS trackers from the University of Amsterdam Bird Tracking System (UvA-BiTS) for several study purposes, including the study of space use during the breeding season, habitat use and foraging behaviour in the winter season, and impacts of human disturbance. To enable broader usage, all data have now been made open access. Combined, the datasets contain 6.0 million GPS positions, 164 million acceleration measurements and 7.0 million classified behaviour events (i.e., flying, walking, foraging, preening, and inactive). The datasets are deposited on the research repository Zenodo, but are also accessible on Movebank and as down-sampled occurrence datasets on the Global Biodiversity Information Facility (GBIF) and Ocean Biodiversity Information System (OBIS).

Conceptualizing and quantifying body condition using structural equation modelling: A user guide.

Body condition is an important concept in behaviour, evolution and conservation, commonly used as a proxy of an individual's performance, for example in the assessment of environmental impacts. Although body condition potentially encompasses a wide range of health state dimensions (nutritional, immune or hormonal status), in practice most studies operationalize body condition using a single (univariate) measure, such as fat storage. One reason for excluding additional axes of variation may be that multivariate descriptors of body condition impose statistical and analytical challenges. Structural equation modelling (SEM) is used in many fields to study questions relating multidimensional concepts, and we here explain how SEM is a useful analytical tool to describe the multivariate nature of body condition. In this 'Research Methods Guide' paper, we show how SEM can be used to resolve different challenges in analysing the multivariate nature of body condition, such as (a) variable reduction and conceptualization, (b) specifying the relationship of condition to performance metrics, (c) comparing competing causal hypothesis and (d) including many pathways in a single model to avoid stepwise modelling approaches. We illustrated the use of SEM on a real-world case study and provided R-code of worked examples as a learning tool. We compared the predictive power of SEM with conventional statistical approaches that integrate multiple variables into one condition variable: multiple regression and principal component analyses. We show that model performance on our dataset is higher when using SEM and led to more accurate and precise estimates compared to conventional approaches. We encourage researchers to consider SEM as a flexible framework to describe the multivariate nature of body condition and thus understand how it affects biological processes, thereby improving the value of body condition proxies for predicting organismal performance. Finally, we highlight that it can be useful for other multidimensional ecological concepts as well, such as immunocompetence, oxidative stress and environmental conditions.

Insect biomass decline scaled to species diversity: General patterns derived from a hoverfly community.

Reports of declines in biomass of flying insects have alarmed the world in recent years. However, how biomass declines reflect biodiversity loss is still an open question. Here, we analyze the abundance (19,604 individuals) of 162 hoverfly species (Diptera: Syrphidae), at six locations in German nature reserves in 1989 and 2014, and generalize the results with a model varying decline rates of common vs. rare species. We show isometric decline rates between total insect biomass and total hoverfly abundance and a scale-dependent decline in hoverfly species richness, ranging between -23% over the season to -82% at the daily level. We constructed a theoretical null model to explore how strong declines in total abundance translate to changing rank-abundance curves, species persistence, and diversity measures. Observed persistence rates were disproportionately lower than expected for species of intermediate abundance, while the rarest species showed decline and appearance rates consistent with random expectation. Our results suggest that large insect biomass declines are predictive of insect diversity declines. Under current threats, even the more common species are in peril, calling for a reevaluation of hazards and conservation strategies that traditionally target already rare and endangered species only.

msGBS: A new high-throughput approach to quantify the relative species abundance in root samples of multispecies plant communities.

Plant interactions are as important belowground as aboveground. Belowground plant interactions are however inherently difficult to quantify, as roots of different species are difficult to disentangle. Although for a couple of decades molecular techniques have been successfully applied to quantify root abundance, root identification and quantification in multispecies plant communities remains particularly challenging. Here we present a novel methodology, multispecies genotyping by sequencing (msGBS), as a next step to tackle this challenge. First, a multispecies meta-reference database containing thousands of gDNA clusters per species is created from GBS derived High Throughput Sequencing (HTS) reads. Second, GBS derived HTS reads from multispecies root samples are mapped to this meta-reference which, after a filter procedure to increase the taxonomic resolution, allows the parallel quantification of multiple species. The msGBS signal of 111 mock-mixture root samples, with up to 8 plant species per sample, was used to calculate the within-species abundance. Optional subsequent calibration yielded the across-species abundance. The within- and across-species abundances highly correlated (R2 range 0.72-0.94 and 0.85-0.98, respectively) to the biomass-based species abundance. Compared to a qPCR based method which was previously used to analyse the same set of samples, msGBS provided similar results. Additional data on 11 congener species groups within 105 natural field root samples showed high taxonomic resolution of the method. msGBS is highly scalable in terms of sensitivity and species numbers within samples, which is a major advantage compared to the qPCR method and advances our tools to reveal hidden belowground interactions.

Plant traits alone are poor predictors of ecosystem properties and long-term ecosystem functioning.

Earth is home to over 350,000 vascular plant species that differ in their traits in innumerable ways. A key challenge is to predict how natural or anthropogenically driven changes in the identity, abundance and diversity of co-occurring plant species drive important ecosystem-level properties such as biomass production or carbon storage. Here, we analyse the extent to which 42 different ecosystem properties can be predicted by 41 plant traits in 78 experimentally manipulated grassland plots over 10 years. Despite the unprecedented number of traits analysed, the average percentage of variation in ecosystem properties jointly explained was only moderate (32.6%) within individual years, and even much lower (12.7%) across years. Most other studies linking ecosystem properties to plant traits analysed no more than six traits and, when including only six traits in our analysis, the average percentage of variation explained in across-year levels of ecosystem properties dropped to 4.8%. Furthermore, we found on average only 12.2% overlap in significant predictors among ecosystem properties, indicating that a small set of key traits able to explain multiple ecosystem properties does not exist. Our results therefore suggest that there are specific limits to the extent to which traits per se can predict the long-term functional consequences of biodiversity change, so that data on additional drivers, such as interacting abiotic factors, may be required to improve predictions of ecosystem property levels.

Biodiversity increases multitrophic energy use efficiency, flow and storage in grasslands.

The continuing loss of global biodiversity has raised questions about the risk that species extinctions pose for the functioning of natural ecosystems and the services that they provide for human wellbeing. There is consensus that, on single trophic levels, biodiversity sustains functions; however, to understand the full range of biodiversity effects, a holistic and multitrophic perspective is needed. Here, we apply methods from ecosystem ecology that quantify the structure and dynamics of the trophic network using ecosystem energetics to data from a large grassland biodiversity experiment. We show that higher plant diversity leads to more energy stored, greater energy flow and higher community-energy-use efficiency across the entire trophic network. These effects of biodiversity on energy dynamics were not restricted to only plants but were also expressed by other trophic groups and, to a similar degree, in aboveground and belowground parts of the ecosystem, even though plants are by far the dominating group in the system. The positive effects of biodiversity on one trophic level were not counteracted by the negative effects on adjacent levels. Trophic levels jointly increased the performance of the community, indicating ecosystem-wide multitrophic complementarity, which is potentially an important prerequisite for the provisioning of ecosystem services.

Limited evidence for spatial resource partitioning across temperate grassland biodiversity experiments.

Locally, plant species richness supports many ecosystem functions. Yet, the mechanisms driving these often-positive biodiversity-ecosystem functioning relationships are not well understood. Spatial resource partitioning across vertical resource gradients is one of the main hypothesized causes for enhanced ecosystem functioning in more biodiverse grasslands. Spatial resource partitioning occurs if species differ in where they acquire resources and can happen both above- and belowground. However, studies investigating spatial resource partitioning in grasslands provide inconsistent evidence. We present the results of a meta-analysis of 21 data sets from experimental species-richness gradients in grasslands. We test the hypothesis that increasing spatial resource partitioning along vertical resource gradients enhances ecosystem functioning in diverse grassland plant communities above- and belowground. To test this hypothesis, we asked three questions. (1) Does species richness enhance biomass production or community resource uptake across sites? (2) Is there evidence of spatial resource partitioning as indicated by resource tracer uptake and biomass allocation above- and belowground? (3) Is evidence of spatial resource partitioning correlated with increased biomass production or community resource uptake? Although plant species richness enhanced community nitrogen and potassium uptake and biomass production above- and belowground, we found that plant communities did not meet our criteria for spatial resource partitioning, though they did invest in significantly more aboveground biomass in higher canopy layers in mixture relative to monoculture. Furthermore, the extent of spatial resource partitioning across studies was not positively correlated with either biomass production or community resource uptake. Our results suggest that spatial resource partitioning across vertical resource gradients alone does not offer a general explanation for enhanced ecosystem functioning in more diverse temperate grasslands.

Effects of extreme rainfall events are independent of plant species richness in an experimental grassland community.

Global climate models predict more frequent periods of drought stress alternated by heavier, but fewer rainfall events in the future. Biodiversity studies have shown that such changed drought stress may be mitigated by plant species richness. Here, we investigate if grassland communities, differing in species richness, respond differently to climatic extremes within the growing season. In a 3-year outdoor mesocosm experiment, four grassland species in both monoculture and mixture were subjected to a rainfall distribution regime with two levels: periods of severe drought in the summer intermitted by extreme rainfall events versus regular rainfall over time. Both treatments received the same amount of water over the season. Extreme rainfall combined with drought periods resulted in a 15% decrease in aboveground biomass in the second and third year, compared to the regular rainfall regime. Root biomass was also reduced in the extreme rainfall treatment, particularly in the top soil layer (- 40%). All species developed higher water use efficiencies (less negative leaf δ13C) in extreme rainfall than in regular rainfall. These responses to the rainfall/drought treatment were independent of species richness, although the mixtures were on an average more productive in terms of biomass than the monocultures. Our experimental results suggest that mixtures are similarly able to buffer these within-season rainfall extremes than monocultures, which contrasts with findings in the studies on natural droughts. Our work demonstrates the importance of investigating the interactions between rainfall distribution and drought periods for understanding effects of climate change on plant community performance.

Signs of stabilisation and stable coexistence.

Many empirical studies motivated by an interest in stable coexistence have quantified negative density dependence, negative frequency dependence, or negative plant-soil feedback, but the links between these empirical results and ecological theory are not straightforward. Here, we relate these analyses to theoretical conditions for stabilisation and stable coexistence in classical competition models. By stabilisation, we mean an excess of intraspecific competition relative to interspecific competition that inherently slows or even prevents competitive exclusion. We show that most, though not all, tests demonstrating negative density dependence, negative frequency dependence, and negative plant-soil feedback constitute sufficient conditions for stabilisation of two-species interactions if applied to data for per capita population growth rates of pairs of species, but none are necessary or sufficient conditions for stable coexistence of two species. Potential inferences are even more limited when communities involve more than two species, and when performance is measured at a single life stage or vital rate. We then discuss two approaches that enable stronger tests for stable coexistence-invasibility experiments and model parameterisation. The model parameterisation approach can be applied to typical density-dependence, frequency-dependence, and plant-soil feedback data sets, and generally enables better links with mechanisms and greater insights, as demonstrated by recent studies.

Hatching failure and accumulation of organic pollutants through the terrestrial food web of a declining songbird in Western Europe.

Population growth in passerine birds is largely driven by fecundity. If fecundity is affected, for instance by hatching failure, populations may decline. We noted high hatching failure of up to 27% per year in relict populations of the Northern wheatear (Oenanthe oenanthe) in The Netherlands, a strongly declining, migratory passerine in Europe. This hatching failure itself can cause population decline, irrespective of other adverse factors. Additionally, we investigated the cause of hatching failure. Unhatched eggs showed egg yolk infections or embryonic malformations, part of which is associated with the actions of dioxin-like compounds (DLCs). Indeed, DLCs appear to bioaccumulate in the local foodweb, where the soil contained only background concentrations, similar to those found at many other locations. DLC concentrations in Dutch eggs were six-fold higher than those in a reference population in Sweden, where egg failure was only 6%. However, Northern wheatears appear to be only moderately sensitive to the actions of DLCs, because of their specific Ah-receptor type which may moderate the receptor mediated effects of DLCs. This indicates that the concentrations of DLCs, although elevated, may not have caused the embryo malformations or the low hatching rates. We discuss whether other toxins may be important or imbalances in the nutrition and if inbreeding may play a larger role than expected.

The Future of Complementarity: Disentangling Causes from Consequences.

Evidence suggests that biodiversity supports ecosystem functioning. Yet, the mechanisms driving this relationship remain unclear. Complementarity is one common explanation for these positive biodiversity-ecosystem functioning relationships. Yet, complementarity is often indirectly quantified as overperformance in mixture relative to monoculture (e.g., 'complementarity effect'). This overperformance is then attributed to the intuitive idea of complementarity or, more specifically, to species resource partitioning. Locally, however, several unassociated causes may drive this overperformance. Here, we differentiate complementarity into three types of species differences that may cause enhanced ecosystem functioning in more diverse ecosystems: (i) resource partitioning, (ii) abiotic facilitation, and (iii) biotic feedbacks. We argue that disentangling these three causes is crucial for predicting the response of ecosystems to future biodiversity loss.

A multitrophic perspective on biodiversity-ecosystem functioning research.

Concern about the functional consequences of unprecedented loss in biodiversity has prompted biodiversity-ecosystem functioning (BEF) research to become one of the most active fields of ecological research in the past 25 years. Hundreds of experiments have manipulated biodiversity as an independent variable and found compelling support that the functioning of ecosystems increases with the diversity of their ecological communities. This research has also identified some of the mechanisms underlying BEF relationships, some context-dependencies of the strength of relationships, as well as implications for various ecosystem services that mankind depends upon. In this paper, we argue that a multitrophic perspective of biotic interactions in random and non-random biodiversity change scenarios is key to advance future BEF research and to address some of its most important remaining challenges. We discuss that the study and the quantification of multitrophic interactions in space and time facilitates scaling up from small-scale biodiversity manipulations and ecosystem function assessments to management-relevant spatial scales across ecosystem boundaries. We specifically consider multitrophic conceptual frameworks to understand and predict the context-dependency of BEF relationships. Moreover, we highlight the importance of the eco-evolutionary underpinnings of multitrophic BEF relationships. We outline that FAIR data (meeting the standards of findability, accessibility, interoperability, and reusability) and reproducible processing will be key to advance this field of research by making it more integrative. Finally, we show how these BEF insights may be implemented for ecosystem management, society, and policy. Given that human well-being critically depends on the multiple services provided by diverse, multitrophic communities, integrating the approaches of evolutionary ecology, community ecology, and ecosystem ecology in future BEF research will be key to refine conservation targets and develop sustainable management strategies.

Lost in diversity: the interactions between soil-borne fungi, biodiversity and plant productivity.

There is consensus that plant species richness enhances plant productivity within natural grasslands, but the underlying drivers remain debated. Recently, differential accumulation of soil-borne fungal pathogens across the plant diversity gradient has been proposed as a cause of this pattern. However, the below-ground environment has generally been treated as a 'black box' in biodiversity experiments, leaving these fungi unidentified. Using next generation sequencing and pathogenicity assays, we analysed the community composition of root-associated fungi from a biodiversity experiment to examine if evidence exists for host specificity and negative density dependence in the interplay between soil-borne fungi, plant diversity and productivity. Plant species were colonised by distinct (pathogenic) fungal communities and isolated fungal species showed negative, species-specific effects on plant growth. Moreover, 57% of the pathogenic fungal operational taxonomic units (OTUs) recorded in plant monocultures were not detected in eight plant species plots, suggesting a loss of pathogenic OTUs with plant diversity. Our work provides strong evidence for host specificity and negative density-dependent effects of root-associated fungi on plant species in grasslands. Our work substantiates the hypothesis that fungal root pathogens are an important driver of biodiversity-ecosystem functioning relationships.

More than 75 percent decline over 27 years in total flying insect biomass in protected areas.

Global declines in insects have sparked wide interest among scientists, politicians, and the general public. Loss of insect diversity and abundance is expected to provoke cascading effects on food webs and to jeopardize ecosystem services. Our understanding of the extent and underlying causes of this decline is based on the abundance of single species or taxonomic groups only, rather than changes in insect biomass which is more relevant for ecological functioning. Here, we used a standardized protocol to measure total insect biomass using Malaise traps, deployed over 27 years in 63 nature protection areas in Germany (96 unique location-year combinations) to infer on the status and trend of local entomofauna. Our analysis estimates a seasonal decline of 76%, and mid-summer decline of 82% in flying insect biomass over the 27 years of study. We show that this decline is apparent regardless of habitat type, while changes in weather, land use, and habitat characteristics cannot explain this overall decline. This yet unrecognized loss of insect biomass must be taken into account in evaluating declines in abundance of species depending on insects as a food source, and ecosystem functioning in the European landscape.

Root chemistry and soil fauna, but not soil abiotic conditions explain the effects of plant diversity on root decomposition.

Plant diversity influences many ecosystem functions including root decomposition. However, due to the presence of multiple pathways via which plant diversity may affect root decomposition, our mechanistic understanding of their relationships is limited. In a grassland biodiversity experiment, we simultaneously assessed the effects of three pathways-root litter quality, soil biota, and soil abiotic conditions-on the relationships between plant diversity (in terms of species richness and the presence/absence of grasses and legumes) and root decomposition using structural equation modeling. Our final structural equation model explained 70% of the variation in root mass loss. However, different measures of plant diversity included in our model operated via different pathways to alter root mass loss. Plant species richness had a negative effect on root mass loss. This was partially due to increased Oribatida abundance, but was weakened by enhanced root potassium (K) concentration in more diverse mixtures. Equally, grass presence negatively affected root mass loss. This effect of grasses was mostly mediated via increased root lignin concentration and supported via increased Oribatida abundance and decreased root K concentration. In contrast, legume presence showed a net positive effect on root mass loss via decreased root lignin concentration and increased root magnesium concentration, both of which led to enhanced root mass loss. Overall, the different measures of plant diversity had contrasting effects on root decomposition. Furthermore, we found that root chemistry and soil biota but not root morphology or soil abiotic conditions mediated these effects of plant diversity on root decomposition.

Benefits of flooding-induced aquatic adventitious roots depend on the duration of submergence: linking plant performance to root functioning.

Background and Aims: Temporal flooding is a common environmental stress for terrestrial plants. Aquatic adventitious roots (aquatic roots) are commonly formed in flooding-tolerant plant species and are generally assumed to be beneficial for plant growth by supporting water and nutrient uptake during partial flooding. However, the actual contribution of these roots to plant performance under flooding has hardly been quantified. As the investment into aquatic root development in terms of carbohydrates may be costly, these costs may - depending on the specific environmental conditions - offset the beneficial effects of aquatic roots. This study tested the hypothesis that the balance between potential costs and benefits depends on the duration of flooding, as the benefits are expected to outweigh the costs in long-term but not in short-term flooding. Methods: The contribution of aquatic roots to plant performance was tested in Solanum dulcamara during 1-4 weeks of partial submergence and by experimentally manipulating root production. Nutrient uptake by aquatic roots, transpiration and photosynthesis were measured in plants differing in aquatic root development to assess the specific function of these roots. Key Results: As predicted, flooded plants benefited from the presence of aquatic roots. The results showed that this was probably due to the contribution of roots to resource uptake. However, these beneficial effects were only present in long-term but not in short-term flooding. This relationship could be explained by the correlation between nutrient uptake and the flooding duration-dependent size of the aquatic root system. Conclusions: The results indicate that aquatic root formation is likely to be selected for in habitats characterized by long-term flooding. This study also revealed only limited costs associated with adventitious root formation, which may explain the maintenance of the ability to produce aquatic roots in habitats characterized by very rare or short flooding events.

Surviving in a Cosexual World: A Cost-Benefit Analysis of Dioecy in Tropical Trees.

Dioecy has a demographic disadvantage compared with hermaphroditism: only about half of reproductive adults produce seeds. Dioecious species must therefore have fitness advantages to compensate for this cost through increased survival, growth, and/or reproduction. We used a full life cycle approach to quantify the demographic costs and benefits associated with dioecy while controlling for demographic differences between dioecious and hermaphroditic species related to other functional traits. The advantage of this novel approach is that we can focus on the effect of breeding system across a diverse tree community. We built a composite integral projection model for hermaphroditic and dioecious tree populations from Barro Colorado Island, Panama, using long-term demographic and newly collected reproductive data. Integration of all costs and benefits showed that compensation was realized through increased seed production, resulting in no net costs of dioecy. Compensation was also facilitated by the low contribution of reproduction to population growth. Estimated positive effects of dioecy on tree growth and survival were small and insignificant for population growth rates. Our model revealed that, for long-lived organisms, the cost of having males is smaller than generally expected. Hence, little compensation is required for dioecious species to maintain population growth rates similar to those of hermaphroditic species.