The disruption of birds' double mutualistic interactions in novel ecosystems.

Non-native trees disrupt ecological processes vital to native plant communities. We studied how forests dominated by Acacia dealbata and Eucalyptus globulus affect the role of birds as dual pollinators and seed dispersers in a region heavily impacted by these two non-native species. We compared bird-plant interactions in the native and in the two non-native forest types. We constructed a multilayer regional network for each forest type and evaluated differences in network dissimilarity between networks. We also calculated the bird's importance in connecting processes and variables associated with module diversity. To determine how the networks react to changes in species richness, we did a simulation of species richness gradient and link percentage for each forest type. The number of birds acting both as pollinators and seed dispersers was higher in native than in non-native forests. However, birds in non-native forests still play a crucial role in maintaining the ecological services provided to native plant communities. However, the eucalyptus network exhibited a concerning simplification, forcing bird species to fully exploit the few remaining resources, leaving little room for structural adjustments and limiting the ecosystem's ability to withstand further species loss. These findings highlight how non-native trees may trigger cascading effects across trophic levels.

Dietary metabarcoding reveals the simplification of bird-pest interaction networks across a gradient of agricultural cover.

Agriculture is vital for supporting human populations, but its intensification often leads to landscape homogenization and a decline in non-provisioning ecosystem services. Ecological intensification and multifunctional landscapes are suggested as nature-based alternatives to intensive agriculture, using ecological processes like natural pest regulation to maximize food production. Birds are recognized for their role in increasing crop yields by consuming invertebrate pests in several agroecosystems. However, the understanding of how bird species, their traits and agricultural land cover influence the structure of bird-pest interactions remains limited. We sampled bird-pest interactions monthly for 1 year, at four sites within a multifunctional landscape, following a gradient of increasing agricultural land cover. We analysed 2583 droppings of 55 bird species with DNA metabarcoding and detected 225 pest species in 1139 samples of 42 bird species. As expected, bird-pest interactions were highly variable across bird species. Dietary pest richness was lower in the fully agricultural site, while predation frequency remained consistent across the agricultural land cover gradient. Network analysis revealed a reduction in the complexity of bird-pest interactions as agricultural coverage increased. Bird species abundance affected the bird's contribution to the network structure more than any of the bird traits analysed (weight, phenology, invertebrate frequency in diet and foraging strata), with more common birds being more important to network structure. Overall, our results show that increasing agricultural land cover increases the homogenization of bird-pest interactions. This shows the importance of maintaining natural patches within agricultural landscapes for biodiversity conservation and enhanced biocontrol.

A agricultura é essencial para suportar a população humana, mas a sua intensificação geralmente leva à homogeneização da paisagem e à redução dos serviços do ecossistema que não sejam de provisão. A intensificação ecológica e paisagens multifuncionais são sugeridas como alternativas naturais à agricultura intensiva, utilizando processos ecológicos como a regulação natural de pragas para maximizar a produção de alimentos. As aves são conhecidas pelo seu papel no aumento da produtividade das culturas por consumirem pragas em diversos agroecossistemas. Contudo, o conhecimento de como as espécies de aves, as suas características e a cobertura agrícola influenciam as interações entre aves e pragas são limitados. Nós amostrámos estas interações mensalmente durante um ano, em quatro locais, numa paisagem multifuncional, ao longo um gradiente de aumento da cobertura agrícola. Analisamos 2583 dejetos de 55 espécies de aves com DNA metabarcoding e detetamos 225 espécies praga em 1139 amostras de 42 espécies de aves. Como esperado, as interações entre aves e pragas foram muito distintas entre as várias espécies de aves. A riqueza de pragas na dieta foi menor no local completamente dominado por área agrícola, enquanto a frequência de predação de pragas foi constante ao longo do gradiente de cobertura agrícola. A análise de redes demonstrou uma redução na complexidade das interações entre aves e pragas à medida que a cobertura agrícola aumenta. A abundância das espécies de aves influenciou mais a contribuição das aves para a estrutura da rede do que qualquer uma das características analisadas (peso, fenologia, frequência de invertebrados na dieta e estrato de alimentação), sendo as aves mais comuns as mais importantes na estrutura da rede. De forma geral, os nossos resultados indicam que o aumento da cobertura agrícola aumenta a homogeneização das interações entre aves e pragas. Isto demonstra a importância de preservar áreas naturais em paisagem agrícolas para a conservação de biodiversidade e melhor controlo biológico.

The impact of habitat loss on pollination services for a threatened dune endemic plant.

Habitat loss is currently a major threat to biodiversity, affecting species interactions, such as plant-pollinator interactions. This is particularly important in self-incompatible plants relying on pollinators to reproduce and sustain their populations. Here, we evaluated how habitat loss affects the pollination system, plant individual-pollinator species interaction network, and plant reproductive fitness of the self-incompatible Jasione maritima var. sabularia, a threatened taxon from dune systems. This plant is a pollinator generalist, visited by 108 species from distinct taxonomic groups. Results suggest that increasing habitat loss led to a significant decline in pollinator richness, increased pollen limitation, and a decrease in reproductive fitness of J. maritima var. sabularia. Visitation rate per individual did not significantly change with available area, indicating that the quality of pollen differed across populations. The topology of the network between J. maritima var. sabularia individuals and its pollinator species did not change, which may be attributed to the stability in the core of pollinator species. This suggests that the lower fitness of plants with increasing habitat degradation may be explained not only by the lower richness of peripheral pollinators but also by the genetic structure of the plant populations, as there is a possible higher transference of less quality pollen by pollinators, ultimately compromising the persistence of plant populations. Our study highlights the need of future studies to integrate the fine details provided by individual-level networks, which will increase our understanding of the pattern of species interactions and its consequences for the fitness of threatened plant populations.

Integrating plant species contribution to mycorrhizal and seed dispersal mutualistic networks.

Mutualistic interactions like those established between plants and mycorrhizal fungi or seed dispersers are key drivers of plant population dynamics and ecosystem functioning; however, these interactions have rarely been explored together. We assembled a tripartite fungi-plant-disperser network in the Gorongosa National Park-Mozambique, to test (1) if diversity and importance of plant mutualists above- and belowground are correlated, and (2) whether biotically and abiotically dispersed plants are associated with distinct arbuscular mycorrhizal fungi (AMF). We quantified seed dispersal by animals for 1 year and characterized the AMF of 26 common plant species. Sixteen plant species were dispersed by 15 animals and colonized by 48 AMF virtual taxa (VT), while the remaining 10 plant species were not dispersed by animals and associated with 34 AMF VT. We found no evidence for a correlation between the number of plant partners above- and belowground or on plant specialization on both types of partners. We also found no evidence for differentiation of AMF communities between biotically and abiotically dispersed plants. Our results suggest that the establishment of plant interactions with seed dispersers and mycorrhizal fungi is largely independent and that both biotically and abiotically dispersed plants seem to associate with similar communities of AMF.

Pollination networks from natural and anthropogenic-novel communities show high structural similarity.

The Anthropocene is marked by an unprecedented homogenisation of the world's biota, confronting species that never co-occurred during their evolutionary histories. Interactions established in these novel communities may affect ecosystem functioning; however, most research has focused on the impacts of a minority of aggressive invasive species, while changes inflicted by a less conspicuous majority of non-invasive alien species on community structure are still poorly understood. This information is critical to guide conservation strategies, and instrumental to advance ecological theory, particularly to understand how non-native species integrate in recipient communities and affect the interactions of native species. We evaluated how the structure of 50 published pollination networks changes with the proportion of alien plant species and found that network structure is largely unaffected. Although some communities were heavily invaded, the proportion of alien plant species was relatively low (mean = 10%; max. = 38%). We further characterized the pollination network in a botanic garden with a plant community dominated by non-invasive alien species (85%). We show that the structure of this novel community is also not markedly different from native-dominated communities. Plant-pollinator interactions revealed no obvious differences regarding plant origin (native vs. alien) or the native bioregion of the introduced plants. This overall similarity between native and alien plants is likely driven by the contrasting patterns of invasive plants (promoting generalism), and non-invasive aliens, suggested here to promote specialization.

Arbuscular mycorrhizal fungi communities from tropical Africa reveal strong ecological structure.

Understanding the distribution and diversity of arbuscular mycorrhizal fungi (AMF) and the rules that govern AMF assemblages has been hampered by a lack of data from natural ecosystems. In addition, the current knowledge on AMF diversity is biased towards temperate ecosystems, whereas little is known about other habitats such as dry tropical ecosystems. We explored the diversity and structure of AMF communities in grasslands, savannas, dry forests and miombo in a protected area under dry tropical climate (Gorongosa National Park, Mozambique) using 454 pyrosequencing. In total, 147 AMF virtual taxa (VT) were detected, including 22 VT new to science. We found a high turnover of AMF with ˂ 12% of VT present in all vegetation types. Forested areas supported more diverse AMF communities than savannas and grassland. Miombo woodlands had the highest AMF richness, number of novel VT, and number of exclusive and indicator taxa. Our data reveal a sharp differentiation of AMF communities between forested areas and periodically flooded savannas and grasslands. This marked ecological structure of AMF communities provides the first comprehensive landscape-scale evidence that, at the background of globally low endemism of AMF, local communities are shaped by regional processes including environmental filtering by edaphic properties and natural disturbance.

Refaunation and the reinstatement of the seed-dispersal function in Gorongosa National Park.

Large animals are important seed dispersers; however, they tend to be under a high extinction risk worldwide. There is compelling evidence that the global biodiversity crisis is leading to the deterioration of several ecosystem functions, but there is virtually no information on how large-scale refaunation efforts can reinstate seed dispersal. We evaluated the effectiveness of a 62-km2 wildlife sanctuary, which was established to recover populations of large mammals in Gorongosa National Park (Mozambique), in restoring seed dispersal. We collected animal scats during the dry season of 2014 (June-August) along 5 transects inside and 5 transects outside the sanctuary fence (50 km total) with the same type of plant community, identified animal and plant species in the transects, and quantified the number of seeds in each scat. Based on these data, we built bipartite networks and calculated network and species-level descriptor values, and we compared data collected inside and outside the sanctuary. There were more scats (268 vs. 207) and more scats containing seeds (132 vs. 94) inside than outside the sanctuary. The number of mammal dispersers was also higher inside (17) than outside the sanctuary (11). Similarly, more seeds (2413 vs. 2124) and plant species (33 vs. 26) were dispersed inside than outside the sanctuary. Overall, the seed-dispersal network was less specialized (0.38 vs. 0.44) and there was a greater overlap (0.16 vs. 0.07) inside than outside the sanctuary. Both networks were significantly modular and antinested. The high number and richness of seeds dispersed inside the sanctuary was explained mostly by a higher abundance of dispersers rather than by disperser identity. Our results suggest conservation efforts aimed at recovering populations of large mammals are helping to reestablish not only target mammal species but also their functional roles as seed dispersers in the ecosystem.

Evidence of a European seed dispersal crisis.

Seed dispersal is crucial for ecosystem persistence, especially in fragmented landscapes, such as those common in Europe. Ongoing defaunation might compromise effective seed dispersal, but the conservation status of pairwise interactions remains unknown. With a literature review, we reconstructed the first European-wide seed dispersal network and evaluated the conservation status of interactions by assessing each interacting partner's IUCN (International Union for Conservation of Nature) conservation status and population trends. We found that a third of the disperser species and interactions face potential extinction and that 30% of the plant species have most of their dispersers threatened or declining. Our study reveals a developing seed dispersal crisis in Europe and highlights large knowledge gaps regarding the dispersers and conservation status of zoochorous plants, urging further scrutiny and action to conserve the seed dispersal service.

O armário: Fruiting phenology data for 4,462 plant taxa in Portugal (1926-2013).

Species phenology - the timing of key life events - is being altered by ongoing climate changes with yet underappreciated consequences for ecosystem stability. While flowering is generally occurring earlier, we know much less about other key processes such as the time of fruit ripening, largely due to the lack of comprehensive long-term datasets. Here we provide information on the exact date and site where seeds of 4,462 taxa were collected for the Index Seminum (seed exchange catalogue) of the Botanic Garden of the University of Coimbra, between 1926 and 2013. Seeds were collected from spontaneous and cultivated individuals across Portugal, including both native and introduced taxa. The database consists of 127,747 curated records with information on the species, or infraspecific taxa (including authority), and the day and site where seeds were collected. All records are georeferenced and provided with a confidence interval for the collection site. Taxonomy was first curated manually by in-house botanists and then harmonized according to the GBIF backbone taxonomy.

Inventory of tiger- and ground-beetles (Coleoptera, Caraboidea, Cicindelidae and Carabidae) in two sampling seasons of the Gorongosa National Park, Mozambique.

Background: The Gorongosa National Park (Mozambique) is one of the most emblematic protected areas in Africa, well known for its vertebrate biodiversity and restoration ecology efforts following the Mozambican civil war in 1992. The invertebrate biodiversity of Gorongosa National Park is still poorly studied, although the scarce information available indicates the existence of a rich number of species, namely in the case of tiger- and ground-beetles (Coleoptera, Caraboidea). Moreover, the study of arthropod assemblages is key for designing conservation practices since they are potentially accurate biodiversity and ecological indicators. Hence, the diversity assessment of Caraboidea beetles using standardised methodologies is likely to provide a new insight for future conservation planning and help to quantify the effects of climate change in areas identified as vulnerable to anthropogenic pressures, such as the Gorongosa National Park. New information: We report the occurrence of five tiger beetles (Cicindelidae) and 93 ground-beetles (Carabidae) species/morphospecies in Gorongosa National Park from a field survey funded by the ECOASSESS project. Sampling was performed in the four main habitat types present in the Park (miombo tropical forest, mixed dry forest, transitional forest and grasslands) between 25 October and 25 November 2019. In this sampling window, the turnover of Caraboidea species from the dry season to the wet season was recorded for the first time. Twenty-eight species of ground-beetles are new records to Mozambique, including three new subgenera and three new genera. Additional information on species phenology and habitat preferences is also provided.

Global and regional ecological boundaries explain abrupt spatial discontinuities in avian frugivory interactions.

Species interactions can propagate disturbances across space via direct and indirect effects, potentially connecting species at a global scale. However, ecological and biogeographic boundaries may mitigate this spread by demarcating the limits of ecological networks. We tested whether large-scale ecological boundaries (ecoregions and biomes) and human disturbance gradients increase dissimilarity among plant-frugivore networks, while accounting for background spatial and elevational gradients and differences in network sampling. We assessed network dissimilarity patterns over a broad spatial scale, using 196 quantitative avian frugivory networks (encompassing 1496 plant and 1004 bird species) distributed across 67 ecoregions, 11 biomes, and 6 continents. We show that dissimilarities in species and interaction composition, but not network structure, are greater across ecoregion and biome boundaries and along different levels of human disturbance. Our findings indicate that biogeographic boundaries delineate the world's biodiversity of interactions and likely contribute to mitigating the propagation of disturbances at large spatial scales.

The role of soils on pollination and seed dispersal.

Ongoing environmental changes are affecting physical, chemical and biological soil components. Evidence of impacts of soil changes on pollinators' and seed dispersers' behaviour, fitness and density is scarce, but growing. Here, we reviewed information on such impacts and on a number of mechanisms that may explain its propagation, taking into account the full range of resources required by the large and diverse number of species of these two important functional groups. We show that while there is substantial evidence on the effects of soil nitrogen enrichment and changes in soil water content on the quality and quantity of floral and fruit resources, little is known on the effects of changes of other soil properties (e.g. soil pH, soil structure, other nutrients). Also, the few studies showing correlations between soil changes and pollinator and seed disperser foraging behaviour or fitness do not clearly identify the mechanisms that explain such correlation. Finally, most studies (including those with nitrogen and water) are local and limited to a small number of species, and it remains unclear how variable such effects are across time and geographical regions, and the strength of interactive effects between soil properties. Increasing research on this topic, taking into consideration how impacts propagate through species interaction networks, will provide essential information to predict impacts of ongoing environmental changes and help guide conservation plans that aim to minimize impacts on ecosystem functioning. This article is part of the theme issue 'The role of soils in delivering Nature's Contributions to People'.

Assessing the effects of temperature and salinity oscillations on a key mesopredator fish from European coastal systems.

A population dynamics model was developed to assess the short and long-term effects of temperature and salinity variations in the common goby Pomatoschistus microps in a Portuguese estuary (Minho estuary, NW Portugal). The population was divided into juveniles, females and males, which constituted the model's state variables. Linear regressions between the observed and the predicted density of juveniles, females and the total population were significant. Parameter's sensitivity and uncertainty analysis were estimated. The model was able to satisfactory describe the P. microps population dynamics, and thus was used to simulate the effects of climatic changes on the fish population. Simulations indicated that the common goby population is sensitive to both temperature and salinity changes. Overall, scenarios of more than 3 °C increase caused significant population decreases. Similarly, increased salinities led to a population shrinkage, whereas scenarios of salinity decrease generated an opposite variation on the population. According to the IPCC predictions for climatic tendencies, the population of the common goby will tend to decrease in the near future, experiencing marked oscillations (decrease or increase) during climatic extremes, namely droughts and floods, respectively. These results may be a useful for future planning and management of estuarine systems given that the common goby is an important species of estuarine food webs in many temperate ecosystems.

Author Correction: Multilayer networks reveal the spatial structure of seed-dispersal interactions across the Great Rift landscapes.

The original version of this Article contained Figshare links in the Code availability statement that were not functional. The correct Figshare links to MATLAB scripts and R code used in this study are https://doi.org/10.6084/m9.figshare.4955651 and https://doi.org/10.6084/m9.figshare.4836383, respectively. These errors have now been corrected in both the PDF and HTML versions of the Article.

Multilayer networks reveal the spatial structure of seed-dispersal interactions across the Great Rift landscapes.

Species interaction networks are traditionally explored as discrete entities with well-defined spatial borders, an oversimplification likely impairing their applicability. Using a multilayer network approach, explicitly accounting for inter-habitat connectivity, we investigate the spatial structure of seed-dispersal networks across the Gorongosa National Park, Mozambique. We show that the overall seed-dispersal network is composed by spatially explicit communities of dispersers spanning across habitats, functionally linking the landscape mosaic. Inter-habitat connectivity determines spatial structure, which cannot be accurately described with standard monolayer approaches either splitting or merging habitats. Multilayer modularity cannot be predicted by null models randomizing either interactions within each habitat or those linking habitats; however, as habitat connectivity increases, random processes become more important for overall structure. The importance of dispersers for the overall network structure is captured by multilayer versatility but not by standard metrics. Highly versatile species disperse many plant species across multiple habitats, being critical to landscape functional cohesion.

High Resilience of Seed Dispersal Webs Highlighted by the Experimental Removal of the Dominant Disperser.

The pressing need to conserve and restore habitats in the face of ongoing species loss [1, 2] requires a better understanding of what happens to communities when species are lost or reinstated [3, 4]. Theoretical models show that communities are relatively insensitive to species loss [5, 6]; however, they disagree with field manipulations showing a cascade of extinctions [7, 8] and have seldom been tested under field conditions (e.g., [9]). We experimentally removed the most abundant seed-dispersing ant species from seed dispersal networks in a Mediterranean landscape, replicating the experiment in three types of habitat, and then compared these communities to un-manipulated control communities. Removal did not result in large-scale changes in network structure. It revealed extensive structural plasticity of the remaining community, which rearranged itself through rewiring, while maintaining its functionality. The remaining ant species widened their diet breadth in a way that maintained seed dispersal, despite the identity of many interactions changing. The species interaction strength decreased; thus, the importance of each ant species for seed dispersal became more homogeneous, thereby reducing the dependence of seed species on one dominant ant species. Compared to the experimental results, a simulation model that included rewiring considerably overestimated the effect of species loss on network robustness. If community-level species loss models are to be of practical use in ecology or conservation, they need to include behavioral and population responses, and they need to be routinely tested under field conditions; doing this would be to the advantage of both empiricists and theoreticians.