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Understanding how the structure of biological systems impacts their resilience (broadly defined) is a recurring question across multiple levels of biological organization. In ecology, considerable effort has been devoted to understanding how the structure of interactions between species in ecological networks is linked to different broad resilience outcomes, especially local stability. Still, nearly all of that work has focused on interaction structure in presence-absence terms, and has not investigated quantitative structure, i.e., the arrangement of interaction strengths in ecological networks. We investigated how the interplay between binary and quantitative structure impacts stability in mutualistic interaction networks (those in which species interactions are mutually beneficial), using community matrix approaches. We additionally examined the effects of network complexity and within-guild competition for context. In terms of structure, we focused on understanding the stability impacts of nestedness, a structure in which more-specialized species interact with smaller subsets of the same species that more-generalized species interact with. Most mutualistic networks in nature display binary nestedness, which is puzzling because both binary and quantitative nestedness are known to be destabilizing on their own. We found that quantitative network structure has important consequences for local stability. In more-complex networks, binary-nested structures were the most stable configurations, depending on the quantitative structures; but which quantitative structure was stabilizing depended on network complexity and competitive context. As complexity increases, and in the absence of within-guild competition, the most stable configurations have a nested binary structure with a complementary (i.e., anti-nested) quantitative structure. In the presence of within-guild competition, however, the most stable networks are those with a nested binary structure and a nested quantitative structure. In other words, the impact of interaction-overlap on community persistence is dependent on the competitive context. These results help to explain the prevalence of binary nested structures in nature and underscore the need for future empirical work on quantitative structure.
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Honey bee parasites remain a critical challenge to management and conservation. Because managed honey bees are maintained in colonies kept in apiaries across landscapes, the study of honey bee parasites allows the investigation of spatial principles in parasite ecology and evolution. We used a controlled field experiment to study the relationship between population growth rate and virulence (colony survival) of the parasite Varroa destructor (Anderson and Trueman). We used a nested design of 10 patches (apiaries) of 14 colonies to examine the spatial scale at which Varroa population growth matters for colony survival. We tracked Varroa population size and colony survival across a full year and found that Varroa populations that grow faster in their host colonies during the spring and summer led to larger Varroa populations across the whole apiary (patch) and higher rates of neighboring colony loss. Crucially, this increased colony loss risk manifested at the patch scale, with mortality risk being related to spatial adjacency to colonies with fast-growing Varroa strains rather than with Varroa growth rate in the colony itself. Thus, within-colony population growth predicts whole-apiary virulence, demonstrating the need to consider multiple scales when investigating parasite growth-virulence relationships.
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Interações Hospedeiro-Parasita , Dinâmica Populacional , Varroidae , Animais , Abelhas/parasitologia , Varroidae/fisiologia , Virulência , Criação de AbelhasRESUMO
PREMISE: Changes to flowering time caused by climate change could affects plant fecundity, but studies that compare the individual-level responses of phenologically distinct, co-occurring species are lacking. We assessed how variation in floral phenology affects the fecundity of individuals from three montane species with different seasonal flowering times, including in snowmelt acceleration treatments to increase variability in phenology. METHODS: We collected floral phenology and seed set data for individuals of three montane plant species (Mertensia fusiformis, Delphinium nuttallianum, Potentilla pulcherrima). To examine the drivers of seed set, we measured conspecific floral density and conducted pollen limitation experiments to isolate pollination function. We advanced the phenology of plant communities in a controlled large-scale snowmelt acceleration experiment. RESULTS: Differences in individual phenology relative to the rest of the population affected fecundity in our focal species, but effects were species-specific. For our early-season species, individuals that bloomed later than the population peak bloom had increased fecundity, while for our midseason species, simply blooming before or after the population peak increased individual fecundity. For our late-season species, blooming earlier than the population peak increased fecundity. The early and midseason species were pollen-limited, and conspecific density affected seed set only for our early-season species. CONCLUSIONS: Our study shows that variation in individual phenology affects fecundity in three phenologically distinct montane species, and that pollen limitation may be more influential than conspecific density. Our results suggest that individual-level changes in phenology are important to consider for understanding plant reproductive success.
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Flores , Polinização , Flores/fisiologia , Polinização/fisiologia , Reprodução/fisiologia , Pólen , Sementes/fisiologia , Estações do AnoRESUMO
Anthropogenic activities are triggering global changes in the environment, causing entire communities of plants, pollinators and their interactions to restructure, and ultimately leading to species declines. To understand the mechanisms behind community shifts and declines, as well as monitoring and managing impacts, a global effort must be made to characterize plant-pollinator communities in detail, across different habitat types, latitudes, elevations, and levels and types of disturbances. Generating data of this scale will only be feasible with rapid, high-throughput methods. Pollen DNA metabarcoding provides advantages in throughput, efficiency and taxonomic resolution over traditional methods, such as microscopic pollen identification and visual observation of plant-pollinator interactions. This makes it ideal for understanding complex ecological networks and their responses to change. Pollen DNA metabarcoding is currently being applied to assess plant-pollinator interactions, survey ecosystem change and model the spatiotemporal distribution of allergenic pollen. Where samples are available from past collections, pollen DNA metabarcoding has been used to compare contemporary and past ecosystems. New avenues of research are possible with the expansion of pollen DNA metabarcoding to intraspecific identification, analysis of DNA in ancient pollen samples, and increased use of museum and herbarium specimens. Ongoing developments in sequencing technologies can accelerate progress towards these goals. Global ecological change is happening rapidly, and we anticipate that high-throughput methods such as pollen DNA metabarcoding are critical for understanding the evolutionary and ecological processes that support biodiversity, and predicting and responding to the impacts of change.
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Código de Barras de DNA Taxonômico , Ecossistema , Código de Barras de DNA Taxonômico/métodos , Pólen/genética , Plantas/genética , DNA , Polinização/genéticaRESUMO
Many tropical seed-dispersing frugivores are facing extinction, but the consequences of the loss of endangered frugivores for seed dispersal is not well understood. We investigated the role of frugivore endangerment status via robustness-to-coextinction simulations (in this context, more accurately described as robustness-to-partner-loss simulations) using data from the Brazilian Atlantic Forest biodiversity hotspot. By simulating the extinction of endangered frugivores, we found a rapid and disproportionate loss of tree species with dispersal partners in the network, and this surprisingly surpassed any other frugivore extinction scenario, including the loss of the most generalist frugivores first. A key driver of this pattern is that many specialist plants rely on at-risk frugivores as seed-dispersal partners. Moreover, interaction compensation in the absence of endangered frugivores may be unlikely because frugivores with growing populations forage on fewer plant species than frugivores with declining populations. Therefore, protecting endangered frugivores could be critical for maintaining tropical forest seed dispersal, and their loss may have higher-than-expected functional consequences for tropical forests, their regeneration processes, and the maintenance of tropical plant diversity.
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Dispersão de Sementes , BrasilRESUMO
In the past decade, the broadcast-spray application of antibiotics in US crops has increased exponentially in response to bacterial crop pathogens, but little is known about the sublethal impacts on beneficial organisms in agroecosystems. This is concerning given the key roles that microbes play in modulating insect fitness. A growing body of evidence suggests that insect gut microbiomes may play a role in learning and behaviour, which are key for the survival of pollinators and for their pollination efficacy, and which in turn could be disrupted by dietary antibiotic exposure. In the laboratory, we tested the effects of an upper-limit dietary exposure to streptomycin (200 ppm)-an antibiotic widely used to treat bacterial pathogens in crops-on bumblebee (Bombus impatiens) associative learning, foraging and stimulus avoidance behaviour. We used two operant conditioning assays: a free movement proboscis extension reflex protocol focused on short-term memory formation, and an automated radio-frequency identification tracking system focused on foraging. We show that upper-limit dietary streptomycin exposure slowed training, decreased foraging choice accuracy, increased avoidance behaviour and was associated with reduced foraging on sucrose-rewarding artificial flowers flowers. This work underscores the need to further study the impacts of antibiotic use on beneficial insects in agricultural systems.
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Agricultura , Exposição Dietética , Estreptomicina , Animais , Antibacterianos/farmacologia , Aprendizagem da Esquiva , Abelhas , Produtos Agrícolas , Flores , Polinização/fisiologia , Estreptomicina/farmacologiaRESUMO
Pollination is a key ecological function of most terrestrial ecosystems. Decades of research on single-trophic-level communities, particularly plant communities, have helped to build the foundation of diversity-function theory. Yet as it stands, this theory appears to be less useful for intertrophic-level functions such as pollination, as evidenced by empirical findings that are often inconsistent with theoretical expectations. In this review, we evaluate how canonical diversity-function theory has been applied to pollination function, focusing on empirical studies of the mechanisms that drive pollinator diversity-function relationships. We first identified key features of pollination function that have hampered reconciliation with current theory. We then examined terminology for mechanisms used to discuss the findings from pollinator diversity-function studies that are sometimes inconsistent with established ecological concepts. We propose a revised diversity-function framework and describe two non-canonical diversity-function mechanisms that are particularly applicable to pollination. The first, "interactive functional complementarity," was identified previously but remains overlooked. The second, a new diversity-function mechanism, "functional enhancement," occurs when pollinator diversity increases within-niche activity. Finally, we discuss experimental approaches necessary to detect diversity-function effects in pollination.
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Ecossistema , Polinização , PlantasRESUMO
Biological systems are likely to be constrained by trade-offs among robustness, resilience, and performance. A better understanding of these trade-offs is important for basic biology, as well as applications where biological systems can be designed for different goals. We focus on redundancy and plasticity as mechanisms governing some types of trade-offs, but mention others as well. Whether trade-offs are due to resource constraints or "design" constraints (i.e., structure of nodes and links within a network) will also affect the types of trade-offs that are important. Identifying common themes across scales of biological organization will require that researchers use similar approaches to quantifying robustness, resilience, and performance, using units that can be compared across systems.
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Evolução Biológica , Aptidão Genética , AnimaisRESUMO
Molecular identification of mixed-species pollen samples has a range of applications in various fields of research. To date, such molecular identification has primarily been carried out via amplicon sequencing, but whole-genome shotgun (WGS) sequencing of pollen DNA has potential advantages, including (1) more genetic information per sample and (2) the potential for better quantitative matching. In this study, we tested the performance of WGS sequencing methodology and publicly available reference sequences in identifying species and quantifying their relative abundance in pollen mock communities. Using mock communities previously analyzed with DNA metabarcoding, we sequenced approximately 200Mbp for each sample using Illumina HiSeq and MiSeq. Taxonomic identifications were based on the Kraken k-mer identification method with reference libraries constructed from full-genome and short read archive data from the NCBI database. We found WGS to be a reliable method for taxonomic identification of pollen with near 100% identification of species in mixtures but generating higher rates of false positives (reads not identified to the correct taxon at the required taxonomic level) relative to rbcL and ITS2 amplicon sequencing. For quantification of relative species abundance, WGS data provided a stronger correlation between pollen grain proportion and sequence read proportion, but diverged more from a 1:1 relationship, likely due to the higher rate of false positives. Currently, a limitation of WGS-based pollen identification is the lack of representation of plant diversity in publicly available genome databases. As databases improve and costs drop, we expect that eventually genomics methods will become the methods of choice for species identification and quantification of mixed-species pollen samples.
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The composition of plant-pollinator interactions-i.e., who interacts with whom in diverse communities-is highly dynamic, and we have a very limited understanding of how interaction identities change in response to perturbations in nature. One prediction from niche and diet theory is that resource niches will broaden to compensate for resource reductions driven by perturbations, yet this has not been empirically tested in plant-pollinator systems in response to real-world perturbations in the field. Here, we use a long-term dataset of floral visitation to Ipomopsis aggregata, a montane perennial herb, to test whether the breadth of its floral visitation niche (i.e., flower visitor richness) changed in response to naturally occurring drought perturbations. Fewer floral resources are available in drought years, which could drive pollinators to expand their foraging niches, thereby expanding plants' floral visitation niches. We compared two drought years to three non-drought years to analyze changes in niche breadth and community composition of floral visitors to I. aggregata, predicting broadened niche breadth and distinct visitor community composition in drought years compared to non-drought years. We found statistically significant increases in niche breadth in drought years as compared to non-drought conditions, but no statistically distinguishable changes in community composition of flower visitors. Our findings suggest that plants' floral visitation niches may exhibit considerable plasticity in response to disturbance. This may have widespread consequences for community-level stability as well as functional consequences if increased niche overlap affects pollination services.
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Secas , Polinização , Flores , PlantasRESUMO
Animals often change their behaviour in the presence of other species and the environmental context they experience, and these changes can substantially modify the course their populations follow. In the case of animals involved in mutualistic interactions, it is still unclear how to incorporate the effects of these behavioural changes into population dynamics. We propose a framework for using pollinator functional responses to examine the roles of pollinator-pollinator interactions and abiotic conditions in altering the times between floral visits of a focal pollinator. We then apply this framework to a unique foraging experiment with different models that allow resource availability and sublethal exposure to a neonicotinoid pesticide to modify how pollinators forage alone and with co-foragers. We found that all co-foragers interfere with the focal pollinator under at least one set of abiotic conditions; for most species, interference was strongest at higher levels of resource availability and with pesticide exposure. Overall our results highlight that density-dependent responses are often context-dependent themselves.
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Flores , Polinização , AnimaisRESUMO
Infectious diseases are a major threat to both managed and wild pollinators. One key question is how the movement or transplantation of honeybee colonies under different management regimes affects honeybee disease epidemiology. We opportunistically examined any persistent effect of colony management history following relocation by characterising the virus abundances of honeybee colonies from three management histories, representing different management histories: feral, low-intensity management, and high-intensity "industrial" management. The colonies had been maintained for one year under the same approximate 'common garden' condition. Colonies in this observational study differed in their virus abundances according to management history, with the feral population history showing qualitatively different viral abundance patterns compared to colonies from the two managed population management histories; for example, higher abundance of sacbrood virus but lower abundances of various paralysis viruses. Colonies from the high-intensity management history exhibited higher viral abundances for all viruses than colonies from the low-intensity management history. Our results provide evidence that management history has persistent impacts on honeybee disease epidemiology, suggesting that apicultural intensification could be majorly impacting on pollinator health, justifying much more substantial investigation.
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Criação de Abelhas/estatística & dados numéricos , Abelhas/virologia , Vírus de Insetos/fisiologia , AnimaisRESUMO
The mite Varroa destructor is an important honey bee parasite that causes substantial losses of honey bee colonies worldwide. Evolutionary theory suggests that the high densities at which honey bees are managed in large-scale beekeeping settings will likely select for mites with greater growth and virulence, thereby potentially explaining the major damage done by these mites. We tested this hypothesis by collecting mites from feral bee colonies, "lightly" managed colonies (those from small-scale sedentary operations), and "heavily" managed colonies (those from large-scale operations that move thousands of colonies across the US on a yearly basis). We established 8 apiaries, each consisting of 11 colonies from a standardized lightly managed bee background that were cleared of mites, and artificially infested each apiary with controlled numbers of mites from feral, lightly managed, or heavily managed bees or left uninoculated as negative control. We monitored the colonies for more than 2 years for mite levels, colony strength (adult bee population, brood coverage, and honey storage), and survival. As predicted by evolutionary theory, we found that colonies inoculated with mites from managed backgrounds had increased V. destructor mite levels relative to those with mites from feral colonies or negative controls. However, we did not see a difference between heavily and lightly managed colonies, and these higher mite burdens did not translate into greater virulence, as measured by reductions in colony strength and survival. Our results suggest that human management of honey bee colonies may favor the increased population growth rate of V. destructor, but that a range of potential confounders (including viral infections and genotype-by-genotype interactions) likely contribute to the relationship between mite reproduction and virulence.
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Human demand for food, fiber, and space is accelerating the rate of change of land cover and land use. Much of the world now consists of a matrix of natural forests, managed forests, agricultural cropland, and urbanized plots. Expansion of domestic energy production efforts in the United States is one driver predicted to influence future land-use and land management practices across large spatial scales. Favorable growing conditions make the southeastern United States an ideal location for producing a large portion of the country's renewable bioenergy. We investigated patterns of bat occurrence in two bioenergy feedstocks commonly grown in this region (corn, Zea mays, and pine, Pinus taeda and P. elliottii). We also evaluated potential impacts of the three major pathways of woody biomass extraction (residue removal following clearcut harvest, short-rotation energy plantations, and mid-rotation forest thinning) to bat occurrence through a priori land-use contrasts. We acoustically sampled bat vocalizations at 84 sites in the Southeastern Plains and Southern Coastal Plains of the southeastern United States across three years. We found that mid-rotation thinning resulted in positive effects on bat occurrence, and potential conversion of unmanaged (reference) forest to managed forest for timber and/or bioenergy harvest resulted in negative effects on bat occurrence when effects were averaged across all species. The effects of short-rotation energy plantations, removal of logging residues from plantation clearcuts, and corn were equivocal for all bat species examined. Our results suggest that accelerated production of biomass for energy production through either corn or intensively managed pine forests is not likely to have an adverse effect on bat communities, so long as existing older unmanaged forests are not converted to managed bioenergy or timber plantations. Beyond bioenergy crop production, mid-rotation thinning of even-aged pine stands intended for timber production, increases to the duration of plantation rotations to promote older forest stands, arranging forest stands and crop fields to maximize edge habitat, and maintaining unmanaged forests could benefit bat communities by augmenting roosting and foraging opportunities.
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Quirópteros , Animais , Biomassa , Ecossistema , Florestas , Humanos , Sudeste dos Estados UnidosRESUMO
Within ecological communities, species engage in myriad interaction types, yet empirical examples of hybrid species interaction networks composed of multiple types of interactions are still scarce. A key knowledge gap is understanding how the structure and stability of such hybrid networks are affected by anthropogenic disturbance. Using 15,169 interaction observations, we constructed 16 hybrid herbivore-plant-pollinator networks along an agricultural intensification gradient to explore changes in network structure and robustness to local extinctions. We found that agricultural intensification led to declines in modularity but increases in nestedness and connectance. Notably, network connectance, a structural feature typically thought to increase robustness, caused declines in hybrid network robustness, but the directionality of changes in robustness along the gradient depended on the order of local species extinctions. Our results not only demonstrate the impacts of anthropogenic disturbance on hybrid network structure, but they also provide unexpected insights into the structure-stability relationship of hybrid networks.
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Agricultura , Polinização , Biota , Ecossistema , Herbivoria , PlantasRESUMO
It is generally thought that the intensification of farming will result in higher disease prevalences, although there is little specific modelling testing this idea. Focussing on honeybees, we build multi-colony models to inform how "apicultural intensification" is predicted to impact honeybee pathogen epidemiology at the apiary scale.We used both agent-based and analytical models to show that three linked aspects of apicultural intensification (increased population sizes, changes in population network structure and increased between-colony transmission) are unlikely to greatly increase disease prevalence in apiaries. Principally this is because even low-intensity apiculture exhibits high disease prevalence.The greatest impacts of apicultural intensification are found for diseases with relatively low R0 (basic reproduction number), however, such diseases cause little overall disease prevalence and, therefore, the impacts of intensification are minor. Furthermore, the smallest impacts of intensification are for diseases with high R0 values, which we argue are typical of important honeybee diseases. Policy Implications: Our findings contradict the idea that apicultural intensification by crowding honeybee colonies in large, dense apiaries leads to notably higher disease prevalences for established honeybee pathogens. More broadly, our work demonstrates the need for informative models of all agricultural systems and management practices in order to understand the implications of management changes on diseases.
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Habitat destruction is the single greatest anthropogenic threat to biodiversity. Decades of research on this issue have led to the accumulation of hundreds of data sets comparing species assemblages in larger, intact, habitats to smaller, more fragmented, habitats. Despite this, little synthesis or consensus has been achieved, primarily because of non-standardized sampling methodology and analyses of notoriously scale-dependent response variables (i.e., species richness). To be able to compare and contrast the results of habitat fragmentation on species' assemblages, it is necessary to have the underlying data on species abundances and sampling intensity, so that standardization can be achieved. To accomplish this, we systematically searched the literature for studies where abundances of species in assemblages (of any taxa) were sampled from many habitat patches that varied in size. From these, we extracted data from several studies, and contacted authors of studies where appropriate data were collected but not published, giving us 117 studies that compared species assemblages among habitat fragments that varied in area. Less than one-half (41) of studies came from tropical forests of Central and South America, but there were many studies from temperate forests and grasslands from all continents except Antarctica. Fifty-four of the studies were on invertebrates (mostly insects), but there were several studies on plants (15), birds (16), mammals (19), and reptiles and amphibians (13). We also collected qualitative information on the length of time since fragmentation. With data on total and relative abundances (and identities) of species, sampling effort, and affiliated meta-data about the study sites, these data can be used to more definitively test hypotheses about the role of habitat fragmentation in altering patterns of biodiversity. There are no copyright restrictions. Please cite this data paper and the associated Dryad data set if the data are used in publications.
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Managed honey bee (Apis mellifera) colonies are kept at much greater densities than naturally occurring feral or wild colonies, which may have detrimental effects on colony health and survival, disease spread, and drifting behavior (bee movement between natal and non-natal colonies). We assessed the effects of a straightforward apiary management intervention (altering the density and visual appearance of colonies) on colony health. Specifically, we established three "high density / high drift" ("HD") and three "low density / low drift" ("LD") apiary configurations, each consisting of eight bee colonies. Hives in the HD apiary configuration were of the same color and placed 1m apart in a single linear array, while hives in the LD apiary configuration were placed 10m apart at different heights, facing outwards in a circle, and made visually distinctive with colors and symbols to reduce accidental drift between colonies. We investigated disease transmission and dynamics between the apiary configurations by clearing all colonies of the parasitic mite Varroa destructor, and subsequently inoculating two randomly-chosen colonies per apiary with controlled mite doses. We monitored the colonies for two years and found that the LD apiary configuration had significantly greater honey production and reduced overwinter mortality. Inoculation and apiary management intervention interacted to affect brood mite levels, with the highest levels in the inoculated colonies in the HD configuration. Finally, foragers were more than three times more likely to drift in the HD apiary configurations. Our results suggest that a relatively straightforward management change-placing colonies in low-density visually complex circles rather than high-density visually similar linear arrays-can provide meaningful benefits to the health and productivity of managed honey bee colonies.
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Criação de Abelhas/métodos , Mel/análise , Carga Parasitária , Animais , Abelhas/parasitologia , Transmissão de Doença Infecciosa/prevenção & controle , Estações do Ano , Varroidae/patogenicidadeRESUMO
Numerous papers have shown that propolis contributes favorably to worker honey bee (Apis mellifera L.) immune response and colony social immunity. Moreover, resin-foraging specialists are more sensitive than pollen foragers to tactile information in the nest interior, and they respond to these stimuli by collecting more resin. In this study, we show that in-hive propolis deposition is increased, compared with nonmodified controls, with any one of the three methods for increasing textural complexity of hive wall interior surfaces: 1) plastic propolis trap material stapled to wall interior, 2) parallel saw kerfs cut into wall interior, or 3) roughening wall interior with a mechanized wire brush. Pairwise comparisons showed that propolis deposition was not significantly different among the three textural treatments; however, textural treatments interacted with time to show a more consistent benefit from plastic propolis trap material or roughened interior surface over saw kerfs. Although direct health benefits were not measured, this work shows that it is comparatively simple to increase propolis deposition above background levels by increasing textural stimuli in hive interiors.
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Ascomicetos , Colecionismo , Himenópteros , Própole , Animais , Abelhas , PólenRESUMO
Pollen DNA metabarcoding-marker-based genetic identification of potentially mixed-species pollen samples-has applications across a variety of fields. While basic species-level pollen identification using standard DNA barcode markers is established, the extent to which metabarcoding (a) correctly assigns species identities to mixes (qualitative matching) and (b) generates sequence reads proportionally to their relative abundance in a sample (quantitative matching) is unclear, as these have not been assessed relative to known standards. We tested the quantitative and qualitative robustness of metabarcoding in constructed pollen mixtures varying in species richness (1-9 species), taxonomic relatedness (within genera to across class) and rarity (5%-100% of grains), using Illumina MiSeq with the markers rbcL and ITS2. Qualitatively, species composition determinations were largely correct, but false positives and negatives occurred. False negatives were typically driven by lack of a barcode gap or rarity in a sample. Species richness and taxonomic relatedness, however, did not strongly impact correct determinations. False positives were likely driven by contamination, chimeric sequences and/or misidentification by the bioinformatics pipeline. Quantitatively, the proportion of reads for each species was only weakly correlated with its relative abundance, in contrast to suggestions from some other studies. Quantitative mismatches are not correctable by consistent scaling factors, but instead are context-dependent on the other species present in a sample. Together, our results show that metabarcoding is largely robust for determining pollen presence/absence but that sequence reads should not be used to infer relative abundance of pollen grains.