Instituto Mixto de Investigación en Biodiversidad

Abstract Functional traits and associated trait‐based concepts have driven rapid innovation in ecology over recent years, with most progress based on insights from plants. However, plants are almost entirely restricted to a single trophic level, and an over‐reliance on plant traits therefore neglects the complexity and importance of biotic interactions across trophic levels. The need to expand the focus of trait‐based ecology to account for trophic complexity has led to an upsurge in attention on animal functional traits and the emergence of new concepts relevant to community ecology, macroecology and ecosystem science. Recent progress in the compilation of global trait datasets for some animal taxa has opened up new possibilities for testing ecological theory. In this Special Focus, we explore how trait‐based ecology can expand the scope of investigation from single to multiple trophic levels, how insights from these investigations can be used to upscale understanding from local communities to biogeographical patterns and how this can ultimately help to predict the impacts of global change on ecosystem functions. To address these key questions, we showcase studies on diverse animal taxa ranging in size from springtails to crocodiles and spanning multiple trophic levels from primary consumers to apex predators. This collection of studies shows how precise measurements of morphological or physiological traits can increase mechanistic understanding of community assembly across trophic levels, particularly of the mechanisms underpinning large‐scale biodiversity patterns. Furthermore, a clearer picture is emerging of systematic animal responses to environmental change that shape the trait composition of ecological communities and affect ecosystem functioning. The articles in this volume highlight the need to move trait‐based ecology beyond the limits of taxonomic boundaries. The integration of trait data and concepts across trophic levels opens up new possibilities for identifying general ecological mechanisms that shape patterns and processes operating at different scales. The identification of key functional traits and their interplay across trophic levels can underpin the development of a trait‐based ecology for whole ecosystems, which could eventually enable predictions of the ecosystem‐level consequences of biodiversity loss. Read the free Plain Language Summary for this article on the Journal blog.

Pollinators face multiple pressures and there is evidence of populations in decline. As demand for insect-pollinated crops increases, crop production is threatened by shortfalls in pollination services. Understanding the extent of current yield deficits due to pollination and identifying opportunities to protect or improve crop yield and quality through pollination management is therefore of international importance. To explore the extent of "pollination deficits," where maximum yield is not being achieved due to insufficient pollination, we used an extensive dataset on a globally important crop, apples. We quantified how these deficits vary between orchards and countries and we compared "pollinator dependence" across different apple varieties. We found evidence of pollination deficits and, in some cases, risks of overpollination were even apparent for which fruit quality could be reduced by too much pollination. In almost all regions studied we found some orchards performing significantly better than others in terms of avoiding a pollination deficit and crop yield shortfalls due to suboptimal pollination. This represents an opportunity to improve production through better pollinator and crop management. Our findings also demonstrated that pollinator dependence varies considerably between apple varieties in terms of fruit number and fruit quality. We propose that assessments of pollination service and deficits in crops can be used to quantify supply and demand for pollinators and help to target local management to address deficits although crop variety has a strong influence on the role of pollinators.

Abstract Ecological intensification in croplands aims to enhance biodiversity‐based ecosystem services, helping to increase yield while reducing agricultural environmental impacts. Identifying ecological intensification tools of wide applicability and easily implemented by farmers is, therefore, an imperative. Here, we verify the efficiency of provisioning artificial nest boxes for insectivorous birds to reinforce pest biological control in apple orchards. The study was conducted in 24 cider‐apple orchards in Asturias (NW Spain) over 3 years. We compared the effect of insectivorous birds between orchards with and without nest boxes occupied by different bird species, through insectivory estimates based on attack on a sentinel pest and measurements of arthropod abundance in apple trees. We also identified preys that birds of different species captured to feed nestlings. Bird occupancy of nest boxes was widespread, ranging 25.0%–33.3% each year. Great tit was the dominant species, followed by blue tit and, occasionally, common redstart. Predation pressure on apple pests increased in orchards with nest boxes, as judged by the increased proportion of sentinel models attacked by birds (34.9% increase in 2018 and 41.1% in 2019), decreased biomass of tree‐dwelling arthropods (−51.7%) and reduced probability of apple pest occurrence (from 57% to 40%), compared to orchards without nest boxes. Nesting species showed different predatory roles in apple orchards. Fewer attacks on sentinel pests but lower arthropod biomass was associated with blue tit rather than great tit. Besides, blue tit fed nestlings at a faster rate and included in their diet a higher proportion of apple pests than great tit, which preyed mostly on other herbivorous insects. Synthesis and applications . We demonstrated the usefulness of nest boxes for insectivorous birds in enhancing biological control of apple pests at a regional scale, identifying tit species as complementary predators of apple pests and herbivores. From the farmers' perspective, providing nest boxes in orchards may represent an efficient, easy to implement, cheap and attractive measure of ecological intensification, compatible with other actions fostering biodiversity in croplands.

Understanding the full diet of natural enemies is necessary for evaluating their role as biocontrol agents, because many enemy species do not only feed on pests but also on other natural enemies. Such intraguild predation can compromise pest control if the consumed enemies are actually better for pest control than their predators. In this study, we used gut metabarcoding to quantify diets of all common arachnid species in Swedish and Spanish apple orchards. For this purpose, we designed new primers that reduce amplification of arachnid predators while retaining high amplification of all prey groups. Results suggest that most arachnids consume a large range of putative pest species on apple but also a high proportion of other natural enemies, where the latter constitute almost a third of all prey sequences. Intraguild predation also varied between regions, with a larger content of heteropteran bugs in arachnid guts from Spanish orchards, but not between orchard types. There was also a tendency for cursorial spiders to have more intraguild prey in the gut than web spiders. Two groups that may be overlooked as important biocontrol agents in apple orchards seem to be theridiid web spiders and opilionids, where the latter had several small-bodied pest species in the gut. These results thus provide important guidance for what arachnid groups should be targets of management actions, even though additional information is needed to quantify all direct and indirect interactions occurring in the complex arthropod food webs in fruit orchards.

Abstract Functional traits mediate the response of communities to disturbances (response traits) and their contribution to ecosystem functions (effect traits). To predict how anthropogenic disturbances influence ecosystem services requires a dual approach including both trait concepts. Here, we used a response–effect trait conceptual framework to understand how local and landscape features affect pollinator functional diversity and pollination services in apple orchards. We worked in 110 apple orchards across four European regions. Orchards differed in management practices. Low‐intensity (LI) orchards were certified organic or followed close‐to‐organic practices. High‐intensity (HI) orchards followed integrated pest management practices. Within each management type, orchards encompassed a range of local (flower diversity, agri‐environmental structures) and landscape features (orchard and pollinator‐friendly habitat cover). We measured pollinator visitation rates and calculated trait composition metrics based on 10 pollinator traits. We used initial fruit set as a measure of pollination service. Some pollinator traits (body size and hairiness) were negatively related to orchard cover and positively affected by pollinator‐friendly habitat cover. Bee functional diversity was lower in HI orchards and decreased with increased landscape orchard cover. Pollination service was not associated with any particular trait but increased with pollinator trait diversity in LI orchards. As a result, LI orchards with high pollinator trait diversity reached levels of pollination service similar to those of HI orchards. Synthesis and applications . Pollinator functional diversity enables pollinator communities to respond to agricultural intensification and to increase pollination function. Our results show that efforts to promote biodiversity provide greater returns in low‐intensity than in high‐intensity orchards. The fact that low‐intensity orchards with high pollinator functional diversity reach levels of pollination services similar to those of high‐intensity orchards provides a compelling argument for the conversion of high‐intensity into low‐intensity farms.

Abstract The diversity of traits within animal assemblages has been shown to affect the magnitude of animal‐provided ecological functions. However, little is known about how consistent trait diversity effects are across ecological functions and ecosystems. More importantly, the importance of trait diversity in driving ecosystem functioning, relative to other components of biodiversity, has rarely been assessed. It also remains unclear how environmental gradients filter trait diversity and, ultimately, modulate ecological functions. Here, we test how different biodiversity components (i.e., trait diversity, phylogenetic diversity and abundance) affect the magnitude of avian seed dispersal and insect predation along large environmental gradients. We sampled frugivorous and insectivorous birds and their ecological functions across gradients of forest cover and fruit and insect abundances in woodland pastures and apple orchards in Northern Spain. We measured 6 morphological traits and compiled phylogenetic information on 43 bird species. We used Structural Equation Models to disentangle the effects of environmental gradients and biodiversity components on ecological functions. We found that different avian functions in the same agroecosystem were controlled by different biodiversity components. While seed dispersal was positively driven by bird abundance in woodland pastures, insect predation responded positively to trait and phylogenetic diversity. The positive effects of trait diversity on insect predation were, on the other hand, consistent across woodland pastures and apple orchards. Our results also pinpointed forest cover and resource availability as filters of the different components of avian diversity, suggesting that environmental gradients condition the effects of biodiversity on avian ecological functions. Our findings reveal variable effects of trait diversity on two different avian ecological functions, but consistent effects on the same function across agroecosystems. Consolidating the generalities of trait diversity effects will require further multi‐function studies, as well as a unifying framework for animal‐driven functions that integrates the causal links between environmental gradients, the different biodiversity components, and ecological functions. Read the free Plain Language Summary for this article on the Journal blog.

Global biodiversity is negatively affected by anthropogenic climate change. As species distributions shift due to increasing temperatures and precipitation fluctuations, many species face the risk of extinction. In this study, we explore the expected trend for plant species distributions in Central America and southern Mexico under two alternative Representative Concentration Pathways (RCPs) portraying moderate (RCP4.5) and severe (RCP8.5) increases in greenhouse gas emissions, combined with two species dispersal assumptions (limited and unlimited), for the 2061-2080 climate forecast. Using an ensemble approach employing three techniques to generate species distribution models, we classified 1924 plant species from the region's (sub)tropical forests according to IUCN Red List categories. To infer the spatial and taxonomic distribution of species' vulnerability under each scenario, we calculated the proportion of species in a threat category (Vulnerable, Endangered, Critically Endangered) at a pixel resolution of 30 arc seconds and by family. Our results show a high proportion (58-67%) of threatened species among the four experimental scenarios, with the highest proportion under RCP8.5 and limited dispersal. Threatened species were concentrated in montane areas and avoided lowland areas where conditions are likely to be increasingly inhospitable. Annual precipitation and diurnal temperature range were the main drivers of species' relative vulnerability. Our approach identifies strategic montane areas and taxa of conservation concern that merit urgent inclusion in management plans to improve climatic resilience in the Mesoamerican biodiversity hotspot. Such information is necessary to develop policies that prioritize vulnerable elements and mitigate threats to biodiversity under climate change.

Efficient and unbiased sampling of ecological interactions is essential to our understanding of the functions they mediate. Seed dispersal by frugivorous birds is a key mutualism for plant regeneration and community dynamics. Mist‐netting is one of the most widely used methods to sample avian seed dispersal through the identification of seeds in droppings of captured birds kept inside cloth bags. However, birds may drop seeds on the ground before being extracted from the net, leading to a fraction of missing information due to ineffective sampling. Worryingly, this fraction could be unevenly distributed across bird and plant species, leading to sampling biases. Here, we assess the effectiveness of using a 1‐m wide mesh below mist nets to sample seeds dropped by entangled birds. We used data from birds mist‐netted during one‐year‐round. We sampled nearly 50% of interaction events and 75% of dispersed seeds on the mesh band below the mist nets (i.e. lost information without this optimization). The proportion of seeds sampled on the mesh bands was not evenly distributed among bird species but strongly related to bird size, ranging from 57–63% in warblers to 84–94% in thrushes. Moreover, the proportion of seeds sampled on the mesh was negatively related to seed size, although this relationship was weaker. We also evaluated accumulation curves of species and pairwise interactions with increasing sampling effort, both with and without using the mesh bands. The number of seed species sampled increased by 21% when using the mesh bands and the number of pairwise interactions by 36%. Our findings provide strong evidence on how inefficient and biased traditional mist‐netting can be for sampling community‐wide seed–dispersal interactions. We thus urge the use of mesh bands in future studies to increase sampling effectiveness and avoid biases, which will ultimately improve our understanding of the seed dispersal function.

Areas used for livestock production and dominated by native grasses represent a unique opportunity to reconcile biodiversity conservation and livestock production. However, limited knowledge of individual species' responses to rangeland management restricts our capacity to design grazing practices that favor endangered species and other priority birds. In this work, we applied Hierarchical Modelling of Species Communities (HMSC) to study individual species responses, as well as the influence of traits on such responses, to variables related to rangeland management using birds of the Rio de la Plata Grasslands as a case study. Based on presence-absence data collected in 454 paddocks across 46 ranches we inferred the response of 69 species considering imperfect detection. This degree of detail fills a major gap in rangeland management, as species-level responses can be used to achieve targeted conservation goals other than maximizing richness or abundance. We found that artificial pastures had an overall negative impact on many bird species, whereas the presence of tussocks had a positive effect, including all threatened species. Grassland specialists were in general sensitive to grass height and tended to respond positively to tussocks but negatively to tree cover. Controlling grass height via adjustments in stocking rate can be a useful tool to favor grassland specialists. To favor a wide range of bird species in ranches, a mosaic of short and tall native grasslands with patches of tussocks and trees is desirable. We also found that species-specific responses were modulated by their traits: small-sized birds responded positively to tussocks and tree cover while large species responded negatively to increasing grass height. Ground foragers preferred short grass while birds that scarcely use this stratum were not affected by grass height. Results on the influence of traits on bird responses are an important novelty in relation to previous work in rangelands and potentially increase our predicting capacity and model transferability across grassland regions.

It is generally accepted that small birds cannot eat large fruits and that highly frugivorous species prefer lipid-poor ones (morphological and nutritional trait-matching). Yet, it is unclear if these rules operate globally and if their strength varies with latitude and on islands. This could have important functional implications for the degree of complementarity and irreplaceability of birds. We analyse avian frugivory in 59 communities across the globe and show that trait-matching is widespread. The strength of morphological trait-matching increased with latitude, and especially on islands, leading to high complementarity between large and small birds. However, whether this resulted in irreplaceability depended on the range of fruit sizes available in the community. Nutritional trait-matching was also common, but did not lead to complementarity or irreplaceability because birds with contrasting diets did not show opposite responses to lipid-poor fruits. We show that trait-matching is pervasive, but its functional consequences are complex.

Abstract Bats are acknowledged as suppliers of essential ecosystem services such as insect pest control in agroecosystems. Little is known, however, on how bat assemblages respond to the gradients imposed by anthropogenic landscapes and farming practices and how these environmental effects translate into changes in bat foraging. In this study, we use cider apple crop in northern Spain as a model to address the filtering effects of landscape composition and orchard management on, simultaneously, quantitative and qualitative characteristics of bat local assemblages and their foraging activity. For that, we carried out acoustic monitoring of bats and sampled pest moth abundance across a wider range of apple orchards covering different landscape contexts and local management conditions. We found that bat assemblages markedly varied across orchards, according mostly to landscape composition gradients but with contrasting landscape effects on different assemblage characteristics. Namely, higher levels of rural urbanization and lower cover of seminatural woody habitats around orchards promoted bat total activity and the number of bat species/species complexes. However, this also altered bat assemblage composition, increasing dominance by the most abundant species, and decreased bat functional diversity. Additionally, a greater cover of apple tree canopy within the orchards decreased bat total activity. Landscape gradients led into predictable variations of bat foraging activity, suggesting a potential persistence of pest control services even in landscapes with limited seminatural habitat cover. The present study highlights the differential responses of bat assemblages to apple crop landscape and orchard‐scale conditions, hindering the establishment of straightforward management guidelines. Further analysis on the relationship between bat assemblage characteristics and pest control is necessary to understand how ecosystem services can be promoted through management in the apple agroecosystem.

Understanding how the extinction of mutualistic partners affects species and their functional role in the community is a foundational question in ecology. Such changes impact the architecture of interaction networks, but it remains unclear how they affect interaction outcomes, such as the nutrient resource provisioning for animals. Here, we fitted a community-level frugivory model with a comprehensive dataset of plant-bird interactions in six communities from the Yungas Forest in Argentina. Then, we predicted bird fruit choices before and after plant loss allowing for rewiring and quantified changes in network architecture and interaction outcomes for frugivores (i.e. nutrient composition of diets). Using this modelling approach, we tested whether plants important for network cohesiveness also sustain the nutritional intake of birds. Also, we linked changes in networks and bird diets to the total consumption rates of plants and the nutrient content of their fruits. Finally, we evaluated how the ability of frugivores to exploit new resources after partner loss (i.e. rewire) protected them from nutritional changes in diets. Our results show that plant species that sustain network cohesiveness differ from those that determine the nutritional characteristics of bird diets. Most nutritious fruits and those offering distinctive nutrient combinations within communities were key for the nutrient intake of birds, but they were often overlooked by network metrics. In addition, we show that frugivores that more easily exploit new resources after partner loss can suffer important shifts in the average nutrient content of their diets. Our model suggests that key species for network architecture may not be the same as for bird diets. Thus, we should remain cautious when inferring the functional consequences of plant species loss based solely on their position within networks. In addition, we show that rewiring can affect birds' nutrition, which may carry some costs. Overall, our study reveals mechanistic links between extinctions, network architecture and interaction outcomes, which challenge some assumptions frequently made in frugivory studies.