ABSTRACT
Agricultural practices constitute both the greatest cause of biodiversity loss and the greatest opportunity for conservation1,2, given the shrinking scope of protected areas in many regions. Recent studies have documented the high levels of biodiversity-across many taxa and biomes-that agricultural landscapes can support over the short term1,3,4. However, little is known about the long-term effects of alternative agricultural practices on ecological communities4,5 Here we document changes in bird communities in intensive-agriculture, diversified-agriculture and natural-forest habitats in 4 regions of Costa Rica over a period of 18 years. Long-term directional shifts in bird communities were evident in intensive- and diversified-agricultural habitats, but were strongest in intensive-agricultural habitats, where the number of endemic and International Union for Conservation of Nature (IUCN) Red List species fell over time. All major guilds, including those involved in pest control, pollination and seed dispersal, were affected. Bird communities in intensive-agricultural habitats proved more susceptible to changes in climate, with hotter and drier periods associated with greater changes in community composition in these settings. These findings demonstrate that diversified agriculture can help to alleviate the long-term loss of biodiversity outside natural protected areas1.
Subject(s)
Agriculture/methods , Agriculture/statistics & numerical data , Biodiversity , Birds/classification , Forests , Animals , Cattle , Costa Rica , Crops, Agricultural/supply & distribution , Extinction, Biological , Forestry/statistics & numerical data , Global Warming/statistics & numerical data , Pest Control, Biological , Pollination , Seed Dispersal , Time FactorsABSTRACT
An amendment to this paper has been published and can be accessed via a link at the top of the paper.
ABSTRACT
While some agricultural landscapes can support wildlife in the short term, it is uncertain how well they can truly sustain wildlife populations. To compare population trends in different production systems, we sampled birds along 48 transects in mature forests, diversified farms, and intensive farms across Costa Rica from 2000 to 2017. To assess how land use influenced population trends in the 349 resident and 80 migratory species with sufficient data, we developed population models. We found, first, that 23% of species were stable in all three land use types, with the rest almost evenly split between increasing and decreasing populations. Second, in forest habitats, a slightly higher fraction was declining: 62% of the 164 species undergoing long-term population changes; nearly half of these declines occurred in forest-affiliated invertivores. Third, in diversified farms, 49% of the 230 species with population changes were declining, with 60% of these declines occurring in agriculture-affiliated species. In contrast, 51% of the species with population changes on diversified farms showed increases, primarily in forest-affiliated invertivores and frugivores. In intensive farms, 153 species showed population changes, also with similar proportions of species increasing (50%) and decreasing (50%). Declines were concentrated in agriculture-affiliated invertivores and forest-affiliated frugivores; increases occurred in many large, omnivorous species. Our findings paint a complex picture but clearly indicate that diversified farming helps sustain populations of diverse, forest-affiliated species. Despite not fully offsetting losses in forest habitats, diversified farming practices help sustain wildlife in a critical time, before possible transformation to nature-positive policies and practices.
Subject(s)
Agriculture , Forests , Animals , Farms , Animals, Wild , BirdsABSTRACT
Islands support unique plants, animals, and human societies found nowhere else on the Earth. Local and global stressors threaten the persistence of island ecosystems, with invasive species being among the most damaging, yet solvable, stressors. While the threat of invasive terrestrial mammals on island flora and fauna is well recognized, recent studies have begun to illustrate their extended and destructive impacts on adjacent marine environments. Eradication of invasive mammals and restoration of native biota are promising tools to address both island and ocean management goals. The magnitude of the marine benefits of island restoration, however, is unlikely to be consistent across the globe. We propose a list of six environmental characteristics most likely to affect the strength of land-sea linkages: precipitation, elevation, vegetation cover, soil hydrology, oceanographic productivity, and wave energy. Global databases allow for the calculation of comparable metrics describing each environmental character across islands. Such metrics can be used today to evaluate relative potential for coupled land-sea conservation efforts and, with sustained investment in monitoring on land and sea, can be used in the future to refine science-based planning tools for integrated land-sea management. As conservation practitioners work to address the effects of climate change, ocean stressors, and biodiversity crises, it is essential that we maximize returns from our management investments. Linking efforts on land, including eradication of island invasive mammals, with marine restoration and protection should offer multiplied benefits to achieve concurrent global conservation goals.
Subject(s)
Conservation of Natural Resources , Ecosystem , Animals , Humans , Biodiversity , Introduced Species , Climate Change , MammalsABSTRACT
The genus Rosenbergiella is one of the most frequent bacterial inhabitants of flowers and a usual member of the insect microbiota worldwide. To date, there is only one publicly available Rosenbergiella genome, corresponding to the type strain of Rosenbergiella nectarea (8N4T), which precludes a detailed analysis of intra-genus phylogenetic relationships. In this study, we obtained draft genomes of the type strains of the other Rosenbergiella species validly published to date (R. australiborealis, R. collisarenosi and R. epipactidis) and 23 additional isolates of flower and insect origin. Isolate S61T, retrieved from the nectar of an Antirrhinum sp. flower collected in southern Spain, displayed low average nucleotide identity (ANI) and in silico DNA-DNA hybridization (isDDH) values when compared with other Rosenbergiella members (≤86.5 and ≤29.8â%, respectively). Similarly, isolate JB07T, which was obtained from the floral nectar of Metrosideros polymorpha plants in Hawaii (USA) had ≤95.7â% ANI and ≤64.1â% isDDH with other Rosenbergiella isolates. Therefore, our results support the description of two new Rosenbergiella species for which we propose the names Rosenbergiella gaditana sp. nov. (type strain: S61T=NCCB 100789T=DSM 111181T) and Rosenbergiella metrosideri sp. nov. (JB07T=NCCB 100888T=LMG 32616T). Additionally, some R. epipactidis and R. nectarea isolates showed isDDH values<79â% with other conspecific isolates, which suggests that these species include subspecies for which we propose the names Rosenbergiella epipactidis subsp. epipactidis subsp. nov. (S256T=CECT 8502T=LMG 27956T), Rosenbergiella epipactidis subsp. californiensis subsp. nov. (FR72T=NCCB 100898T=LMG 32786T), Rosenbergiella epipactidis subsp. japonicus subsp. nov. (K24T=NCCB 100924T=LMG 32785T), Rosenbergiella nectarea subsp. nectarea subsp. nov. (8N4T = DSM 24150T = LMG 26121T) and Rosenbergiella nectarea subsp. apis subsp. nov. (B1AT=NCCB 100810T= DSM 111763T), respectively. Finally, we present the first phylogenomic analysis of the genus Rosenbergiella and update the formal description of the species R. australiborealis, R. collisarenosi, R. epipactidis and R. nectarea based on new genomic and phenotypic information.
Subject(s)
Fatty Acids , Plant Nectar , Bees , Animals , Phylogeny , Sequence Analysis, DNA , DNA, Bacterial/genetics , RNA, Ribosomal, 16S/genetics , Bacterial Typing Techniques , Base Composition , Fatty Acids/chemistry , Nucleic Acid Hybridization , InsectaABSTRACT
Along with bacteria, fungi can represent a significant component of animal- and plant-associated microbial communities. However, we have only begun to describe these fungi, much less examine their effects on most animals and plants. Bacteria associated with the honey bee, Apis mellifera, have been well characterized across different regions of the gut. The mid- and hindgut of foraging bees house a deterministic set of core species that affect host health, whereas the crop, or the honey stomach, harbors a more diverse set of bacteria that is highly variable in composition among individual bees. Whether this contrast between the two regions of the gut also applies to fungi remains unclear despite their potential influence on host health. In honey bees caught foraging at four sites across the San Francisco Peninsula of California, we found that fungi were less distinct in species composition between the crop and the mid- and hindgut than bacteria. Unlike bacteria, fungi varied substantially in species composition throughout the honey bee gut, and much of this variation could be predicted by the location where we collected the bees. These observations suggest that fungi may be transient passengers and unimportant as gut symbionts. However, our findings also indicate that honey bees could be vectors of infectious plant diseases as many of the fungi we found in the honey bee gut are recognized as plant pathogens.
Subject(s)
Gastrointestinal Tract , Microbiota , Bees , Animals , Gastrointestinal Tract/microbiology , Bacteria , Stomach , FungiABSTRACT
Lifelong infection of the gastric mucosa by Helicobacter pylori can lead to peptic ulcers and gastric cancer. However, how the bacteria maintain chronic colonization in the face of constant mucus and epithelial cell turnover in the stomach is unclear. Here, we present a new model of how H. pylori establish and persist in stomach, which involves the colonization of a specialized microenvironment, or microniche, deep in the gastric glands. Using quantitative three-dimensional (3D) confocal microscopy and passive CLARITY technique (PACT), which renders tissues optically transparent, we analyzed intact stomachs from mice infected with a mixture of isogenic, fluorescent H. pylori strains with unprecedented spatial resolution. We discovered that a small number of bacterial founders initially establish colonies deep in the gastric glands and then expand to colonize adjacent glands, forming clonal population islands that persist over time. Gland-associated populations do not intermix with free-swimming bacteria in the surface mucus, and they compete for space and prevent newcomers from establishing in the stomach. Furthermore, bacterial mutants deficient in gland colonization are outcompeted by wild-type (WT) bacteria. Finally, we found that host factors such as the age at infection and T-cell responses control bacterial density within the glands. Collectively, our results demonstrate that microniches in the gastric glands house a persistent H. pylori reservoir, which we propose replenishes the more transient bacterial populations in the superficial mucosa.
Subject(s)
Gastric Mucosa/microbiology , Helicobacter pylori/growth & development , Microscopy, Confocal/methods , Animals , Anti-Bacterial Agents/pharmacology , Cell Line, Tumor , Colony Count, Microbial , Female , Gastric Mucosa/drug effects , Helicobacter Infections/microbiology , Helicobacter pylori/drug effects , Helicobacter pylori/genetics , Host-Pathogen Interactions/drug effects , Humans , Mice, Inbred C57BL , Mice, Knockout , Mutation/genetics , Species Specificity , T-Lymphocytes/drug effectsABSTRACT
Modern coexistence theory is increasingly used to explain how differences between competing species lead to coexistence versus competitive exclusion. Although research testing this theory has focused on deterministic cases of competitive exclusion, in which the same species always wins, mounting evidence suggests that competitive exclusion is often historically contingent, such that whichever species happens to arrive first excludes the other. Coexistence theory predicts that historically contingent exclusion, known as priority effects, will occur when large destabilizing differences (positive frequency-dependent growth rates of competitors), combined with small fitness differences (differences in competitors' intrinsic growth rates and sensitivity to competition), create conditions under which neither species can invade an established population of its competitor. Here we extend the empirical application of modern coexistence theory to determine the conditions that promote priority effects. We conducted pairwise invasion tests with four strains of nectar-colonizing yeasts to determine how the destabilizing and fitness differences that drive priority effects are altered by two abiotic factors characterizing the nectar environment: sugar concentration and pH. We found that higher sugar concentrations increased the likelihood of priority effects by reducing fitness differences between competing species. In contrast, higher pH did not change the likelihood of priority effects, but instead made competition more neutral by bringing both fitness differences and destabilizing differences closer to zero. This study demonstrates how the empirical partitioning of priority effects into fitness and destabilizing components can elucidate the pathways through which environmental conditions shape competitive interactions.
Subject(s)
Ecosystem , Models, Biological , Hydrogen-Ion Concentration , Microbial Interactions/physiology , Plant Nectar , Species Specificity , Sugars/chemistry , Yeasts/growth & development , Yeasts/physiologyABSTRACT
Ecological communities typically contain more species when located within geologically older regions. This pattern is traditionally attributed to the long-term accumulation of species in the regional species pool, with local species interactions playing a minor role. We provide evidence suggesting a more important role of local species interactions than generally assumed. We assembled 320 communities of root-associated fungi under 80 species pools, varying species pool richness and the mean age of the sites from which the fungi were collected across a 4-myr soil chronosequence. We found that local diversity increased more with increasing species pool richness when species were from older sites. We also found that older species pools had lower functional and phylogenetic diversity, indicating greater competitive equivalence among species. Our results suggest that older regions have higher local richness not simply because older pools are more speciose but also because species have evolved traits that allow them to locally co-occur.
Subject(s)
Biodiversity , Soil , PhylogenyABSTRACT
The history of species immigration can dictate how species interact in local communities, thereby causing historical contingency in community assembly. Since immigration history is rarely known, these historical influences, or priority effects, pose a major challenge in predicting community assembly. Here, we provide a graph-based, non-parametric, theoretical framework for understanding the predictability of community assembly as affected by priority effects. To develop this framework, we first show that the diversity of possible priority effects increases super-exponentially with the number of species. We then point out that, despite this diversity, the consequences of priority effects for multispecies communities can be classified into four basic types, each of which reduces community predictability: alternative stable states, alternative transient paths, compositional cycles and the lack of escapes from compositional cycles to stable states. Using a neural network, we show that this classification of priority effects enables accurate explanation of community predictability, particularly when each species immigrates repeatedly. We also demonstrate the empirical utility of our theoretical framework by applying it to two experimentally derived assembly graphs of algal and ciliate communities. Based on these analyses, we discuss how the framework proposed here can help guide experimental investigation of the predictability of history-dependent community assembly.
Subject(s)
Ciliophora , Biodiversity , Neural Networks, Computer , PlantsABSTRACT
AbstractLife-history trade-offs among species are major drivers of community assembly. Most studies investigate how trade-offs promote deterministic coexistence of species. It remains unclear how trade-offs may instead promote historically contingent exclusion of species, where species dominance is affected by initial abundances, causing alternative community states via priority effects. Focusing on the establishment-longevity trade-off, in which high longevity is associated with low competitive ability during establishment, we study the transient dynamics and equilibrium outcomes of competitive interactions in a simulation model of plant community assembly. We show that in this model, the establishment-longevity trade-off is a necessary but not sufficient condition for alternative stable equilibria, which also require low fecundity for both species. An analytical approximation of our simulation model demonstrates that alternative stable equilibria are driven by demographic stochasticity in the number of seeds arriving at each establishment site. This site-scale stochasticity is affected only by fecundity and therefore occurs even in infinitely large communities. In many cases where the establishment-longevity trade-off does not cause alternative stable equilibria, the trade-off still decreases the rate of convergence toward the single equilibrium, resulting in decades of transient dynamics that can appear indistinguishable from alternative stable equilibria in empirical studies.
Subject(s)
Ecosystem , Fertility , Computer Simulation , Demography , Models, BiologicalABSTRACT
Plant-soil feedback (PSF) may change in strength over the life of plant individuals as plants continue to modify the soil microbial community. However, the temporal variation in PSF is rarely quantified and its impacts on plant communities remain unknown. Using a chronosequence reconstructed from annual aerial photographs of a coastal dune ecosystem, we characterized > 20-yr changes in soil microbial communities associated with individuals of the four dominant perennial species, one legume and three nonlegume. We also quantified the effects of soil biota on conspecific and heterospecific seedling performance in a glasshouse experiment that preserved soil properties of these individual plants. Additionally, we used a general individual-based model to explore the potential consequences of temporally varying PSF on plant community assembly. In all plant species, microbial communities changed with plant age. However, responses of plants to the turnover in microbial composition depended on the identity of the seedling species: only the soil biota effect experienced by the nonlegume species became increasingly negative with longer soil conditioning. Model simulation suggested that temporal changes in PSF could affect the transient dynamics of plant community assembly. These results suggest that temporal variation in PSF over the life of individual plants should be considered to understand how PSF structures plant communities.
Subject(s)
Ecosystem , Soil , Biota , Plants , Soil MicrobiologyABSTRACT
A detailed evaluation of eight bacterial isolates from floral nectar and animal visitors to flowers shows evidence that they represent three novel species in the genus Acinetobacter. Phylogenomic analysis shows the closest relatives of these new isolates are Acinetobacter apis, Acinetobacter boissieri and Acinetobacter nectaris, previously described species associated with floral nectar and bees, but high genome-wide sequence divergence defines these isolates as novel species. Pairwise comparisons of the average nucleotide identity of the new isolates compared to known species is extremely low (<83â%), thus confirming that these samples are representative of three novel Acinetobacter species, for which the names Acinetobacter pollinis sp. nov., Acinetobacter baretiae sp. nov. and Acinetobacter rathckeae sp. nov. are proposed. The respective type strains are SCC477T (=TSD-214T=LMG 31655T), B10AT (=TSD-213T=LMG 31702T) and EC24T (=TSD-215T=LMG 31703T=DSM 111781T).
Subject(s)
Acinetobacter/classification , Bees/microbiology , Phylogeny , Plant Nectar , Acinetobacter/isolation & purification , Animals , Bacterial Typing Techniques , Base Composition , California , DNA, Bacterial/genetics , Flowers , Nucleic Acid Hybridization , RNA, Ribosomal, 16S/genetics , Sequence Analysis, DNAABSTRACT
Floral nectar is commonly colonized by yeasts and bacteria, whose growth largely depends on their capacity to assimilate nutrient resources, withstand high osmotic pressures, and cope with unbalanced carbon-to-nitrogen ratios. Although the basis of the ecological success of these microbes in the harsh environment of nectar is still poorly understood, it is reasonable to assume that they are efficient nitrogen scavengers that can consume a wide range of nitrogen sources in nectar. Furthermore, it can be hypothesized that phylogenetically closely related strains have more similar phenotypic characteristics than distant relatives. We tested these hypotheses by investigating the growth performance on different nitrogen-rich substrates of a collection of 82 acinetobacters isolated from nectar and honeybees, representing members of five species (Acinetobacter nectaris, A. boissieri, A. apis, and the recently described taxa A. bareti and A. pollinis). We also analyzed possible links between growth performance and phylogenetic affiliation of the isolates, while taking into account their geographical origin. Results demonstrated that the studied isolates could utilize a wide variety of nitrogen sources, including common metabolic by-products of yeasts (e.g., ammonium and urea), and that phylogenetic relatedness was associated with the variation in nitrogen assimilation among the studied acinetobacters. Finally, nutrient source and the origin (sample type and country) of isolates also predicted the ability of the acinetobacters to assimilate nitrogen-rich compounds. Overall, these results demonstrate inter-clade variation in the potential of the acinetobacters as nitrogen scavengers and suggest that nutritional dependences might influence interactions between bacteria and yeasts in floral nectar.
Subject(s)
Nitrogen , Plant Nectar , Acinetobacter , Animals , Bees , Insecta , PhylogenyABSTRACT
Understanding the origins and maintenance of biodiversity remains one of biology's grand challenges. From theory and observational evidence, we know that variability in environmental conditions through time is likely critical to the coexistence of competing species. Nevertheless, experimental tests of fluctuation-driven coexistence are rare and have typically focused on just one of two potential mechanisms, the temporal storage effect, to the neglect of the theoretically equally plausible mechanism known as relative nonlinearity of competition. We combined experiments and simulations in a system of nectar yeasts to quantify the relative contribution of the two mechanisms to coexistence. Resource competition models parameterized from single-species assays predicted the outcomes of mixed-culture competition experiments with 83% accuracy. Model simulations revealed that both mechanisms have measurable effects on coexistence and that relative nonlinearity can be equal or greater in magnitude to the temporal storage effect. In addition, we show that their effect on coexistence can be both antagonistic and complementary. These results falsify the common assumption that relative nonlinearity is of negligible importance, and in doing so reveal the importance of testing coexistence mechanisms in combination.
Subject(s)
Biodiversity , Models, Biological , Mycobiome , Plant Nectar , Saccharomycetales/physiology , Adaptation, Biological , Amino Acids , Computer Simulation , Monte Carlo Method , Osmotic Pressure , Plant Nectar/chemistry , Species Specificity , SucroseABSTRACT
Global changes in climate, atmospheric composition, and pollutants are altering ecosystems and the goods and services they provide. Among approaches for predicting ecosystem responses, long-term observations and manipulative experiments can be powerful approaches for resolving single-factor and interactive effects of global changes on key metrics such as net primary production (NPP). Here we combine both approaches, developing multidimensional response surfaces for NPP based on the longest-running, best-replicated, most-multifactor global-change experiment at the ecosystem scale-a 17-y study of California grassland exposed to full-factorial warming, added precipitation, elevated CO2, and nitrogen deposition. Single-factor and interactive effects were not time-dependent, enabling us to analyze each year as a separate realization of the experiment and extract NPP as a continuous function of global-change factors. We found a ridge-shaped response surface in which NPP is humped (unimodal) in response to temperature and precipitation when CO2 and nitrogen are ambient, with peak NPP rising under elevated CO2 or nitrogen but also shifting to lower temperatures. Our results suggest that future climate change will push this ecosystem away from conditions that maximize NPP, but with large year-to-year variability.
Subject(s)
Climate Change , Ecosystem , Environmental Monitoring , Air Pollutants , California , Carbon Dioxide/metabolism , Grassland , Humans , Nitrogen/metabolismABSTRACT
Inhibitory priority effects, in which early-arriving species exclude competing species from local communities, are thought to enhance regional species diversity via community divergence. Theory suggests, however, that these same priority effects make it difficult for species to coexist in the region unless individuals are continuously supplied from an external species pool, often an unrealistic assumption. Here we develop an eco-evolutionary hypothesis to solve this conundrum. We build a metacommunity model in which local priority effects occur between two species via interspecific interference. Within each species there are two genotypes: one is more resistant to interspecific interference than the other but pays a fitness cost for its resistance. Because of this trade-off, species evolve to become less resistant as they become regionally more common. Rare species can then invade some local patches and consequently recover in regional frequency. This "eco-evolutionary buffering" enables the regional coexistence of species despite local priority effects, even in the absence of immigration from an external species pool. Our model predicts that eco-evolutionary buffering is particularly effective when local communities are small and connected by infrequent dispersal.
Subject(s)
Animal Distribution , Biodiversity , Biological Evolution , Models, Biological , Plant DispersalABSTRACT
Priority effects, or the effects of species arrival history on local species abundances, have been documented in a range of taxa. However, factors determining the extent to which priority effects affect community assembly remain unclear. Using laboratory populations of the bacterium Pseudomonas fluorescens, we examined whether shared evolutionary history affected the strength of priority effects. We hypothesized that sympatric evolution of populations belonging to the same guild would lead to niche differentiation, resulting in phenotypic complementarity that weakens priority effects. Consistent with this hypothesis, we found that priority effects tended to be weaker in sympatrically evolved pairs of immigrating populations than in allopatrically evolved pairs. Furthermore, priority effects were weaker under higher phenotypic complementarity. However, these patterns were observed only in populations with a relatively short history of sympatric evolution, and disappeared when populations had evolved together for a long time. Together, our results suggest that the evolutionary history of organismal traits may dictate the strength of priority effects and, consequently, the extent of historical contingency in the assembly of ecological communities.
Subject(s)
Biological Evolution , Pseudomonas fluorescens/physiology , Sympatry , Population DynamicsABSTRACT
Many species of yeast are integral to human society. They produce many of our foods, beverages and industrial chemicals, challenge us as pathogens, and provide models for the study of our own biology. However, few species are regularly studied and much of their ecology remains unclear, hindering the development of knowledge that is needed to improve the relationships between humans and yeasts. There is increasing evidence that insects are an essential component of ascomycetous yeast ecology. We propose a 'dispersal-encounter hypothesis' whereby yeasts are dispersed by insects between ephemeral, spatially disparate sugar resources, and insects, in turn, obtain the benefits of an honest signal from yeasts for the sugar resources. We review the relationship between yeasts and insects through three main examples: social wasps, social bees and beetles, with some additional examples from fruit flies. Ultimately, we suggest that over the next decades, consideration of these ecological and evolutionary relationships between insects and yeasts will allow prediction of where new yeast diversity is most likely to be discovered, particularly yeasts with traits of interest to human industry.
Subject(s)
Ascomycota/physiology , Food Industry , Insecta/microbiology , Animals , Biological Evolution , Ecosystem , Humans , Plant Nectar/metabolism , SymbiosisABSTRACT
The species of yeasts that colonize floral nectar can modify the mutualistic relationships between plants and pollinators by changing the chemical properties of nectar. Recent evidence supporting this possibility has led to increased interest among ecologists in studying these fungi as well as the bacteria that interact with them in nectar. Although not fully explored, nectar yeasts also constitute a promising natural microcosm that can be used to facilitate development of general ecological theory. We discuss the methodological and conceptual advantages of using nectar yeasts from this perspective, including simplicity of communities, tractability of dispersal, replicability of community assembly, and the ease with which the mechanisms of species interactions can be studied in complementary experiments conducted in the field and the laboratory. To illustrate the power of nectar yeasts as a study system, we discuss several topics in community ecology, including environmental filtering, priority effects, and metacommunity dynamics. An exciting new direction is to integrate metagenomics and comparative genomics into nectar yeast research to address these fundamental ecological topics.