Range-wide genetic analysis of an endangered bumble bee (Bombus affinis, Hymenoptera: Apidae) reveals population structure, isolation by distance, and low colony abundance.

Declines in bumble bee species range and abundances are documented across multiple continents and have prompted the need for research to aid species recovery and conservation. The rusty patched bumble bee (Bombus affinis) is the first federally listed bumble bee species in North America. We conducted a range-wide population genetics study of B. affinis from across all extant conservation units to inform conservation efforts. To understand the species' vulnerability and help establish recovery targets, we examined population structure, patterns of genetic diversity, and population differentiation. Additionally, we conducted a site-level analysis of colony abundance to inform prioritizing areas for conservation, translocation, and other recovery actions. We find substantial evidence of population structuring along an east-to-west gradient. Putative populations show evidence of isolation by distance, high inbreeding coefficients, and a range-wide male diploidy rate of ~15%. Our results suggest the Appalachians represent a genetically distinct cluster with high levels of private alleles and substantial differentiation from the rest of the extant range. Site-level analyses suggest low colony abundance estimates for B. affinis compared to similar datasets of stable, co-occurring species. These results lend genetic support to trends from observational studies, suggesting that B. affinis has undergone a recent decline and exhibit substantial spatial structure. The low colony abundances observed here suggest caution in overinterpreting the stability of populations even where B. affinis is reliably detected interannually. These results help delineate informed management units, provide context for the potential risks of translocation programs, and help set clear recovery targets for this and other threatened bumble bee species.

Plant species within Streptanthoid Complex associate with distinct microbial communities that shift to be more similar under drought.

Prolonged water stress can shift rhizoplane microbial communities, yet whether plant phylogenetic relatedness or drought tolerance predicts microbial responses is poorly understood. To explore this question, eight members of the Streptanthus clade with varying affinity to serpentine soil were subjected to three watering regimes. Rhizoplane bacterial communities were characterized using 16S rRNA gene amplicon sequencing and we compared the impact of watering treatment, soil affinity, and plant species identity on bacterial alpha and diversity. We determined which taxa were enriched among drought treatments using DESeq2 and identified features of soil affinity using random forest analysis. We show that water stress has a greater impact on microbial community structure than soil affinity or plant identity, even within a genus. Drought reduced alpha diversity overall, but plant species did not strongly differentiate alpha diversity. Watering altered the relative abundance of bacterial genera within Proteobacteria, Firmicutes, Bacteroidetes, Planctomycetes, and Acidobacteria, which responded similarly in the rhizoplane of most plant species. In addition, bacterial communities were more similar when plants received less water. Pseudarthrobacter was identified as a feature of affinity to serpentine soil while Bradyrhizobium, Chitinophaga, Rhodanobacter, and Paenibacillus were features associated with affinity to nonserpentine soils among Streptanthus. The homogenizing effect of drought on microbial communities and the increasing prevalence of Gram-negative bacteria across all plant species suggest that effects of water stress on root-associated microbiome structure may be predictable among closely related plant species that inhabit very different soil environments. The functional implications of observed changes in microbiome composition remain to be studied.

The evolution of glandularity as a defense against herbivores in the tarweed clade.

PREMISE: Glandular trichomes are implicated in direct and indirect defense of plants. However, the degree to which glandular and non-glandular trichomes have evolved as a consequence of herbivory remains unclear, because their heritability, their association with herbivore resistance, their trade-offs with one another, and their association with other functions are rarely quantified. METHODS: We conducted a phylogenetic comparison of trichomes and herbivore resistance against the generalist caterpillar, Heliothis virescens, among tarweed species (Asteraceae: Madiinae) and a genetic correlation study comparing those same traits among maternal half-sibs of three tarweed species. RESULTS: Within a tarweed species, we found no evidence that herbivore growth rate decreased on tarweed individuals or maternal sib groups with more glandularity or denser trichomes. However, tarweed species with more glandularity and fewer non-glandular trichomes resulted in slower-growing herbivores. Likewise, a trade-off between glandular and non-glandular trichomes was apparent among tarweed species, but not among individuals or sib groups within a species. CONCLUSIONS: Our results suggest that this key herbivore does not select for trichomes as a direct defense in tarweed species. However, trichomes differed substantially among species and likely affect herbivore pressure on those species. Our results demonstrate that trade-offs among plant traits, as well as inference on the function of those traits, can depend on scale.

Population genomic analysis of an emerging pathogen Lonsdalea quercina affecting various species of oaks in western North America.

Understanding processes leading to disease emergence is important for effective disease management and prevention of future epidemics. Utilizing whole genome sequencing, we studied the phylogenetic relationship and diversity of two populations of the bacterial oak pathogen Lonsdalea quercina from western North America (Colorado and California) and compared these populations to other Lonsdalea species found worldwide. Phylogenetic analysis separated Colorado and California populations into two Lonsdalea clades, with genetic divergence near species boundaries, suggesting long isolation and populations that differ in genetic structure and distribution and possibly their polyphyletic origin. Genotypes collected from different host species and habitats were randomly distributed within the California cluster. Most Colorado isolates from introduced planted trees, however, were distinct from three isolates collected from a natural stand of Colorado native Quercus gambelii, indicating cryptic population structure. The California identical core genotypes distribution varied, while Colorado identical core genotypes were always collected from neighboring trees. Despite its recent emergence, the Colorado population had higher nucleotide diversity, possibly due to its long presence in Colorado or due to migrants moving with nursery stock. Overall, results suggest independent pathogen emergence in two states likely driven by changes in host-microbe interactions due to ecosystems changes. Further studies are warranted to understand evolutionary relationships among L. quercina from different areas, including the red oak native habitat in northeastern USA.

Increased aridity is associated with stronger tradeoffs in ponderosa pine vital functions.

Trees must allocate resources to core functions like growth, defense, and reproduction. These allocation patterns have profound effects on forest health, yet little is known about how core functions trade off over time, and even less is known about how a changing climate will impact tradeoffs. We conducted a 21-year survey of growth, defense, and reproduction in 80 ponderosa pine individuals spanning eight populations across environmental gradients along the Colorado Front Range, USA. We used linear mixed models to describe tradeoffs among these functions and to characterize variability among and within individuals over time. Growth and defense were lower in years of high cone production, and local drought conditions amplified year-to-year tradeoffs between reproduction and growth, where trees located at sites with hotter and drier climates showed stronger tradeoffs between reproduction and growth. Our results support the environmental stress hypothesis of masting, which predicts that greater interannual variation in tree functions will be associated with more marginal environments, such as those that are prone to drought. With warming temperatures and increased exposure to drought stress, trees will be faced with stronger interannual tradeoffs, which could lead to further decreases in growth and defensive efforts, ultimately increasing risks of mortality.

Periodical Cicada Emergences Affect Masting Behavior of Oaks.

AbstractOaks (Quercus spp.) are masting species exhibiting highly variable and synchronized acorn production. We investigated the hypothesis that periodical cicadas (Magicada spp.), well known to have strong effects on the ecosystems in which they occur, affect acorn production of oaks through their xylem feeding habits as nymphs, the oviposition damage they inflict as adults during emergences, or the nutrient pulse resulting from the decomposition of their bodies following breeding. We found negative effects on acorn production during emergence years and the year following emergences and enhanced acorn production 2 years after emergence. We also found evidence indicating a significant effect of cicada emergences on spatial synchrony of acorn production by trees growing within the range of the same cicada brood compared with different broods. These results demonstrate that periodical cicadas act as a trophic environmental "veto" depressing acorn production during and immediately following emergences, after which the nutrient pulse associated with the cicada's demise enhances oak reproduction.

Combining local, landscape, and regional geographies to assess plant community vulnerability to invasion impact.

Invasive species science has focused heavily on the invasive agent. However, management to protect native species also requires a proactive approach focused on resident communities and the features affecting their vulnerability to invasion impacts. Vulnerability is likely the result of factors acting across spatial scales, from local to regional, and it is the combined effects of these factors that will determine the magnitude of vulnerability. Here, we introduce an analytical framework that quantifies the scale-dependent impact of biological invasions on native richness from the shape of the native species-area relationship (SAR). We leveraged newly available, biogeographically extensive vegetation data from the U.S. National Ecological Observatory Network to assess plant community vulnerability to invasion impact as a function of factors acting across scales. We analyzed more than 1000 SARs widely distributed across the USA along environmental gradients and under different levels of non-native plant cover. Decreases in native richness were consistently associated with non-native species cover, but native richness was compromised only at relatively high levels of non-native cover. After accounting for variation in baseline ecosystem diversity, net primary productivity, and human modification, ecoregions that were colder and wetter were most vulnerable to losses of native plant species at the local level, while warmer and wetter areas were most susceptible at the landscape level. We also document how the combined effects of cross-scale factors result in a heterogeneous spatial pattern of vulnerability. This pattern could not be predicted by analyses at any single scale, underscoring the importance of accounting for factors acting across scales. Simultaneously assessing differences in vulnerability between distinct plant communities at local, landscape, and regional scales provided outputs that can be used to inform policy and management aimed at reducing vulnerability to the impact of plant invasions.

SPCIS: Standardized Plant Community with Introduced Status database.

The movement of plant species across the globe exposes native communities to new species introductions. While introductions are pervasive, two aspects of variability underlie patterns and processes of biological invasions at macroecological scales. First, only a portion of introduced species become invaders capable of substantially impacting ecosystems. Second, species that do become invasive at one location may not be invasive in others; impacts depend on invader abundance and recipient species and conditions. Accounting for these phenomena is essential to accurately understand the patterns of plant invasion and explain the idiosyncratic results reflected in the literature on biological invasions. The lack of community-level richness and the abundance of data spanning broad scales and environmental conditions have until now hindered our understanding of invasions at a macroecological scale. To address this limitation, we leveraged quantitative surveys of plant communities in the USA and integrated and harmonized nine datasets into the Standardized Plant Community with Introduced Status (SPCIS) database. The database contains 14,056 unique taxa identified within 83,391 sampling units, of which 52.6% have at least one introduced species. The SPCIS database includes comparable information on plant species occurrence, abundance, and native status across the 50 U.S. States and Puerto Rico. SPCIS can be used to answer macro-scale questions about native plant communities and interactions with invasive plants. There are no copyright restrictions on the data, and we ask the users of this dataset to cite this paper, the respective paper(s) corresponding to the dataset sampling design (all references are provided in Data S1: Metadata S1: Class II-B-2), and the references described in Data S1: Metadata S1: Class III-B-4 as applicable to the dataset being utilized.

Fitness homeostasis across an experimental water gradient predicts species' geographic range and climatic breadth.

Species range sizes and realized niche breadths vary tremendously. Understanding the source of this variation has been a long-term aim in evolutionary ecology and is a major tool in efforts to ameliorate the impacts of changing climates on species distributions. Species ranges that span a large climatic envelope can be achieved by a collection of specialized genotypes locally adapted to a small range of conditions, by genotypes with stable fitness across variable environments, or a combination of these factors. We asked whether fitness expressed along a key niche axis, water availability, could explain a species' realized niche breadth, its geographic range and climate breadth, in 11 species from a clade of jewelflowers whose range sizes vary by two orders of magnitude. Specifically, we explored whether the range size of a species was related to the ability of genotypes (maternal families) to maintain fitness across a range of experimental water availabilities based on 30-year historical field precipitation regimes. We operationally characterized fitness homeostasis through the coefficient of variation in fitness of a genotype (family) across the experimental water gradient. We found that species with genotypes that had high fitness homeostasis, low variation in fitness over our treatments, had larger climatic niche breadth and geographic range in their field distributions. The result was robust to alternate measures of fitness homeostasis. Our results show that the fitness homeostasis of genotypes can be a major factor contributing to niche breadth and range size in this clade. Fitness homeostasis can buffer species from loss of genetic diversity and under changing climates, provides time for adaptation to future conditions.

MASTREE+: Time-series of plant reproductive effort from six continents.

Significant gaps remain in understanding the response of plant reproduction to environmental change. This is partly because measuring reproduction in long-lived plants requires direct observation over many years and such datasets have rarely been made publicly available. Here we introduce MASTREE+, a data set that collates reproductive time-series data from across the globe and makes these data freely available to the community. MASTREE+ includes 73,828 georeferenced observations of annual reproduction (e.g. seed and fruit counts) in perennial plant populations worldwide. These observations consist of 5971 population-level time-series from 974 species in 66 countries. The mean and median time-series length is 12.4 and 10 years respectively, and the data set includes 1122 series that extend over at least two decades (≥20 years of observations). For a subset of well-studied species, MASTREE+ includes extensive replication of time-series across geographical and climatic gradients. Here we describe the open-access data set, available as a.csv file, and we introduce an associated web-based app for data exploration. MASTREE+ will provide the basis for improved understanding of the response of long-lived plant reproduction to environmental change. Additionally, MASTREE+ will enable investigation of the ecology and evolution of reproductive strategies in perennial plants, and the role of plant reproduction as a driver of ecosystem dynamics.

Aún existen importantes vacíos en la comprensión de la respuesta reproductiva de las plantas al cambio medioambiental, en parte, porque su monitoreo en especies de plantas longevas requiere una observación directa durante muchos años, y estos conjuntos de datos rara vez han estado disponibles. Aquí presentamos a MASTREE +, una base de datos que recopila series de tiempo de la reproducción de las plantas de todo el planeta, poniendo a disposición estos datos de libre acceso para la comunidad científica. MASTREE + incluye 73.828 puntos de observación de la reproducción anual georreferenciados (ej. conteos de semillas y frutos) en poblaciones de plantas perennes en todo el mundo. Estas observaciones consisten en 5971 series temporales a nivel de población provenientes de 974 especies en 66 países. La mediana de la duración de las series de tiempo es de 10 años (media = 12.4 años) y el conjunto de datos incluye 1.122 series de al menos dos décadas (≥20 años de observaciones). Para un subconjunto de especies bien estudiadas, MASTREE +incluye un amplio conjunto de series temporales replicadas en gradientes geográficos y climáticos. Describimos el conjunto de datos de acceso abierto disponible como un archivo.csv y presentamos una aplicación web asociada para la exploración de datos. MASTREE+ proporcionará la base para mejorar la comprensión sobre la respuesta reproductiva de plantas longevas al cambio medioambiental. Además, MASTREE+ facilitará los avances en la investigación de la ecología y la evolución de las estrategias reproductivas en plantas perennes y el papel de la reproducción vegetal como determinante de la dinámica de ecosistemas.

INHABIT: A web-based decision support tool for invasive plant species habitat visualization and assessment across the contiguous United States.

Narrowing the communication and knowledge gap between producers and users of scientific data is a longstanding problem in ecological conservation and land management. Decision support tools (DSTs), including websites or interactive web applications, provide platforms that can help bridge this gap. DSTs can most effectively disseminate and translate research results when producers and users collaboratively and iteratively design content and features. One data resource seldom incorporated into DSTs are species distribution models (SDMs), which can produce spatial predictions of habitat suitability. Outputs from SDMs can inform management decisions, but their complexity and inaccessibility can limit their use by resource managers or policy makers. To overcome these limitations, we present the Invasive Species Habitat Tool (INHABIT), a novel, web-based DST built with R Shiny to display spatial predictions and tabular summaries of habitat suitability from SDMs for invasive plants across the contiguous United States. INHABIT provides actionable science to support the prevention and management of invasive species. Two case studies demonstrate the important role of end user feedback in confirming INHABIT's credibility, utility, and relevance.

North American tree migration paced by climate in the West, lagging in the East.

Tree fecundity and recruitment have not yet been quantified at scales needed to anticipate biogeographic shifts in response to climate change. By separating their responses, this study shows coherence across species and communities, offering the strongest support to date that migration is in progress with regional limitations on rates. The southeastern continent emerges as a fecundity hotspot, but it is situated south of population centers where high seed production could contribute to poleward population spread. By contrast, seedling success is highest in the West and North, serving to partially offset limited seed production near poleward frontiers. The evidence of fecundity and recruitment control on tree migration can inform conservation planning for the expected long-term disequilibrium between climate and forest distribution.

An intercontinental comparison of insect seed predation between introduced and native oaks.

Novel interactions between introduced oaks and their natural enemies across different continents provide an opportunity to test the enemy release hypothesis (ERH) at local and global scales. Based on the ERH, we assessed the impacts of native seed-feeding insects on introduced and native oaks within and among continents. We combined a common-garden experiment in China and biogeographic literature surveys to measure seed predation by insects and the proportion of acorn embryos surviving after insect infestation among 4 oak species with different geographical origins: Quercus mongolica origin from China, Q. robur and Q. petraea from Europe, and Q. rubra from North America. Mostly supporting the ERH, oaks in introduced continents escaped seed predation compared to those in native continents and compared to other native oaks in introduced continents. Common-garden comparisons showed that total acorn infestation rate of introduced Q. rubra (section Lobatae) was considerably lower than that of native oaks (section Quercus) in China and Europe, likely because of the differences in seed traits associated with different oak sections. Literature surveys showed that seed predation of introduced oaks was lower in the introduced continent than in the native continent. Embryo survival was higher in introduced Q. rubra than native oaks in China and Poland. However, insect seed predation of recently introduced Q. rubra in China was similar to that in Europe, which is not consistent with the ERH. Our results suggest that reduced acorn attack by native insects and higher embryo survival after acorn damage could increase the establishment success or invasion risk of introduced oaks in non-native continents.

Loss of branches due to winter storms could favor deciduousness in oaks.

PREMISE: Ecologists have an incomplete understanding of the factors that select for deciduous, evergreen, and marcescent leaf habits. Evergreens have more opportunities for photosynthesis but may experience costs when abiotic conditions are unfavorable such as during ice and windstorms. METHODS: We documented branch loss for species of oaks (Quercus spp.) in a common garden in California during an unusual windstorm. RESULTS: Branches of marcescent trees were more likely to break during the storm, and this pattern had a negligible phylogenetic signature. Branches of evergreen and marcescent species were mostly alive before breaking, which likely accrued a fitness cost, while those of deciduous species were mostly already dead. One explanation for the overrepresentation of broken branches from marcescent species is that their petioles are inflexible and have greater wind loading compared to the flexible petioles of evergreen leaves and the leafless condition of deciduous branches. CONCLUSIONS: These results suggest that branch loss during unusual winter storms may be an important cost of a marcescent leaf habit.

The effects of ENSO and the North American monsoon on mast seeding in two Rocky Mountain conifer species.

We aimed to disentangle the patterns of synchronous and variable cone production (i.e. masting) and its relationship to climate in two conifer species native to dry forests of western North America. We used cone abscission scars to reconstruct ca 15 years of recent cone production in Pinus edulis and Pinus ponderosa, and used redundancy analysis to relate time series of annual cone production to climate indices describing the North American monsoon and the El Niño Southern Oscillation (ENSO). We show that the sensitivity to climate and resulting synchrony in cone production varies substantially between species. Cone production among populations of P. edulis was much more spatially synchronous and more closely related to large-scale modes of climate variability than among populations of P. ponderosa. Large-scale synchrony in P. edulis cone production was associated with the North American monsoon and we identified a dipole pattern of regional cone production associated with ENSO phase. In P. ponderosa, these climate indices were not strongly associated with cone production, resulting in asynchronous masting patterns among populations. This study helps frame our understanding of mast seeding as a life-history strategy and has implications for our ability to forecast mast years in these species. This article is part of the theme issue 'The ecology and evolution of synchronized seed production in plants'.

The ecology and evolution of synchronized reproduction in long-lived plants.

Populations of many long-lived plants exhibit spatially synchronized seed production that varies extensively over time, so that seed production in some years is much higher than on average, while in others, it is much lower or absent. This phenomenon termed masting or mast seeding has important consequences for plant reproductive success, ecosystem dynamics and plant-human interactions. Inspired by recent advances in the field, this special issue presents a series of articles that advance the current understanding of the ecology and evolution of masting. To provide a broad overview, we reflect on the state-of-the-art of masting research in terms of underlying proximate mechanisms, ontogeny, adaptations, phylogeny and applications to conservation. While the mechanistic drivers and fitness consequences of masting have received most attention, the evolutionary history, ontogenetic trajectory and applications to plant-human interactions are poorly understood. With increased availability of long-term datasets across broader geographical and taxonomic scales, as well as advances in molecular approaches, we expect that many mysteries of masting will be solved soon. The increased understanding of this global phenomenon will provide the foundation for predictive modelling of seed crops, which will improve our ability to manage forests and agricultural fruit and nut crops in the Anthropocene. This article is part of the theme issue 'The ecology and evolution of synchronized seed production in plants'.

Modes of climate variability bridge proximate and evolutionary mechanisms of masting.

There is evidence that variable and synchronous reproduction in seed plants (masting) correlates to modes of climate variability, e.g. El Niño Southern Oscillation and North Atlantic Oscillation. In this perspective, we explore the breadth of knowledge on how climate modes control reproduction in major masting species throughout Earth's biomes. We posit that intrinsic properties of climate modes (periodicity, persistence and trends) drive interannual and decadal variability of plant reproduction, as well as the spatial extent of its synchrony, aligning multiple proximate causes of masting through space and time. Moreover, climate modes force lagged but in-phase ecological processes that interact synergistically with multiple stages of plant reproductive cycles. This sets up adaptive benefits by increasing offspring fitness through either economies of scale or environmental prediction. Community-wide links between climate modes and masting across plant taxa suggest an evolutionary role of climate variability. We argue that climate modes may 'bridge' proximate and ultimate causes of masting selecting for variable and synchronous reproduction. The future of such interaction is uncertain: processes that improve reproductive fitness may remain coupled with climate modes even under changing climates, but chances are that abrupt global warming will affect Earth's climate modes so rapidly as to alter ecological and evolutionary links. This article is part of the theme issue 'The ecology and evolution of synchronized seed production in plants'.

Understanding mast seeding for conservation and land management.

Masting, the intermittent and synchronous production of large seed crops, can have profound consequences for plant populations and the food webs that are built on their seeds. For centuries, people have recorded mast crops because of their importance in managing wildlife populations. In the past 30 years, we have begun to recognize the importance of masting in conserving and managing many other aspects of the environment: promoting the regeneration of forests following fire or other disturbance, conserving rare plants, conscientiously developing the use of edible seeds as non-timber forest products, coping with the consequences of extinctions on seed dispersal, reducing the impacts of plant invasions with biological control, suppressing zoonotic diseases and preventing depredation of endemic fauna. We summarize current instances and future possibilities of a broad set of applications of masting. By exploring in detail several case studies, we develop new perspectives on how solutions to pressing conservation and land management problems may benefit by better understanding the dynamics of seed production. A lesson common to these examples is that masting can be used to time management, and often, to do this effectively, we need models that explicitly forecast masting and the dynamics of seed-eating animals into the near-term future. This article is part of the theme issue 'The ecology and evolution of synchronized seed production in plants'.

Is there tree senescence? The fecundity evidence.

Despite its importance for forest regeneration, food webs, and human economies, changes in tree fecundity with tree size and age remain largely unknown. The allometric increase with tree diameter assumed in ecological models would substantially overestimate seed contributions from large trees if fecundity eventually declines with size. Current estimates are dominated by overrepresentation of small trees in regression models. We combined global fecundity data, including a substantial representation of large trees. We compared size-fecundity relationships against traditional allometric scaling with diameter and two models based on crown architecture. All allometric models fail to describe the declining rate of increase in fecundity with diameter found for 80% of 597 species in our analysis. The strong evidence of declining fecundity, beyond what can be explained by crown architectural change, is consistent with physiological decline. A downward revision of projected fecundity of large trees can improve the next generation of forest dynamic models.