Complex eco-evolutionary responses of a foundational coastal marsh plant to global change.

Predicting the fate of coastal marshes requires understanding how plants respond to rapid environmental change. Environmental change can elicit shifts in trait variation attributable to phenotypic plasticity and act as selective agents to shift trait means, resulting in rapid evolution. Comparably, less is known about the potential for responses to reflect the evolution of trait plasticity. Here, we assessed the relative magnitude of eco-evolutionary responses to interacting global change factors using a multifactorial experiment. We exposed replicates of 32 Schoenoplectus americanus genotypes 'resurrected' from century-long, soil-stored seed banks to ambient or elevated CO2 , varying levels of inundation, and the presence of a competing marsh grass, across two sites with different salinities. Comparisons of responses to global change factors among age cohorts and across provenances indicated that plasticity has evolved in five of the seven traits measured. Accounting for evolutionary factors (i.e. evolution and sources of heritable variation) in statistical models explained an additional 9-31% of trait variation. Our findings indicate that evolutionary factors mediate ecological responses to environmental change. The magnitude of evolutionary change in plant traits over the last century suggests that evolution could play a role in pacing future ecosystem response to environmental change.

Assessing opportunities and inequities in undergraduate ecological forecasting education.

Conducting ecological research in a way that addresses complex, real-world problems requires a diverse, interdisciplinary and quantitatively trained ecology and environmental science workforce. This begins with equitably training students in ecology, interdisciplinary science, and quantitative skills at the undergraduate level. Understanding the current undergraduate curriculum landscape in ecology and environmental sciences allows for targeted interventions to improve equitable educational opportunities. Ecological forecasting is a sub-discipline of ecology with roots in interdisciplinary and quantitative science. We use ecological forecasting to show how ecology and environmental science undergraduate curriculum could be evaluated and ultimately restructured to address the needs of the 21st century workforce. To characterize the current state of ecological forecasting education, we compiled existing resources for teaching and learning ecological forecasting at three curriculum levels: online resources; US university courses on ecological forecasting; and US university courses on topics related to ecological forecasting. We found persistent patterns (1) in what topics are taught to US undergraduate students at each of the curriculum levels; and (2) in the accessibility of resources, in terms of course availability at higher education institutions in the United States. We developed and implemented programs to increase the accessibility and comprehensiveness of ecological forecasting undergraduate education, including initiatives to engage specifically with Native American undergraduates and online resources for learning quantitative concepts at the undergraduate level. Such steps enhance the capacity of ecological forecasting to be more inclusive to undergraduate students from diverse backgrounds and expose more students to quantitative training.

Accounting for variability when resurrecting dormant propagules substantiates their use in eco-evolutionary studies.

There has been a steady rise in the use of dormant propagules to study biotic responses to environmental change over time. This is particularly important for organisms that strongly mediate ecosystem processes, as changes in their traits over time can provide a unique snapshot into the structure and function of ecosystems from decades to millennia in the past. Understanding sources of bias and variation is a challenge in the field of resurrection ecology, including those that arise because often-used measurements like seed germination success are imperfect indicators of propagule viability. Using a Bayesian statistical framework, we evaluated sources of variability and tested for zero-inflation and overdispersion in data from 13 germination trials of soil-stored seeds of Schoenoplectus americanus, an ecosystem engineer in coastal salt marshes in the Chesapeake Bay. We hypothesized that these two model structures align with an ecological understanding of dormancy and revival: zero-inflation could arise due to failed germinations resulting from inviability or failed attempts to break dormancy, and overdispersion could arise by failing to measure important seed traits. A model that accounted for overdispersion, but not zero-inflation, was the best fit to our data. Tetrazolium viability tests corroborated this result: most seeds that failed to germinate did so because they were inviable, not because experimental methods failed to break their dormancy. Seed viability declined exponentially with seed age and was mediated by seed provenance and experimental conditions. Our results provide a framework for accounting for and explaining variability when estimating propagule viability from soil-stored natural archives which is a key aspect of using dormant propagules in eco-evolutionary studies.

A century-long record of plant evolution reconstructed from a coastal marsh seed bank.

Evidence is mounting that climate-driven shifts in environmental conditions can elicit organismal evolution, yet there are sparingly few long-term records that document the tempo and progression of responses, particularly for plants capable of transforming ecosystems. In this study, we "resurrected" cohorts of a foundational coastal marsh sedge (Schoenoplectus americanus) from a time-stratified seed bank to reconstruct a century-long record of heritable variation in response to salinity exposure. Common-garden experiments revealed that S. americanus exhibits heritable variation in phenotypic traits and biomass-based measures of salinity tolerance. We found that responses to salinity exposure differed among the revived cohorts, with plants from the early 20th century exhibiting greater salinity tolerance than those from the mid to late 20th century. Fluctuations in salinity tolerance could reflect stochastic variation but a congruent record of genotypic variation points to the alternative possibility that the loss and gain in functionality are driven by selection, with comparisons to historical rainfall and paleosalinity records suggesting that selective pressures vary according to shifting estuarine conditions. Because salinity tolerance in S. americanus is tightly coupled to primary productivity and other vital ecosystem attributes, these findings indicate that organismal evolution merits further consideration as a factor shaping coastal marsh responses to climate change.

Increased water use efficiency leads to decreased precipitation sensitivity of tree growth, but is offset by high temperatures.

Both increases in temperature and changes in precipitation may limit future tree growth, but rising atmospheric CO2 could offset some of these stressors through increased plant Water Use Efficiency (WUE). The net balance between the negative impacts of climate change and positive effects of CO2 on tree growth is crucial for ecotones, where increased climate stress could drive mortality and shifts in range. Here, we quantify the effects of climate, stand structure, and rising CO2 on both annual tree-ring growth increment and intrinsic WUE (iWUE) at a savanna-forest boundary in the Upper Midwest United States. Taking a Bayesian hierarchical modelling approach, we find that plant iWUE increased by ~ 16-23% over the course of the twentieth century, but on average, tree-ring growth increments do not significantly increase. Consistent with higher iWUE under increased CO2 and recent wetting, we observe a decrease in sensitivity of tree growth to annual precipitation, leading to ~ 35-41% higher growth under dry conditions compared to trees of similar size in the past. However, an emerging interaction between summer maximum temperatures and annual precipitation diminishes the water-savings benefit under hot and dry conditions. This decrease in precipitation sensitivity, and the interaction between temperature and precipitation are strongest in open canopy microclimates, suggesting that stand structure may modulate response to future changes. Overall, while higher iWUE may provide some water savings benefits to growth under normal drought conditions, near-term future temperature increases combined with drought events could drive growth declines of about 50%.

The forests of the midwestern United States at Euro-American settlement: Spatial and physical structure based on contemporaneous survey data.

We present gridded 8 km-resolution data products of the estimated stem density, basal area, and biomass of tree taxa at Euro-American settlement of the midwestern United States during the middle to late 19th century for the states of Minnesota, Wisconsin, Michigan, Illinois, and Indiana. The data come from settlement-era Public Land Survey (PLS) data (ca. 0.8-km resolution) of trees recorded by land surveyors. The surveyor notes have been transcribed, cleaned, and processed to estimate stem density, basal area, and biomass at individual points. The point-level data are aggregated within 8 km grid cells and smoothed using a generalized additive statistical model that accounts for zero-inflated continuous data and provides approximate Bayesian uncertainty estimates. The statistical modeling smooths out sharp spatial features (likely arising from statistical noise) within areas smaller than about 200 km2. Based on this modeling, presettlement Midwestern landscapes supported multiple dominant species, vegetation types, forest types, and ecological formations. The prairies, oak savannas, and forests each had distinctive structures and spatial distributions across the domain. Forest structure varied from savanna (averaging 27 Mg/ha biomass) to northern hardwood (104 Mg/ha) and mesic southern forests (211 Mg/ha). The presettlement forests were neither unbroken and massively-statured nor dominated by young forests constantly structured by broad-scale disturbances such as fire, drought, insect outbreaks, or hurricanes. Most forests were structurally between modern second growth and old growth. We expect the data product to be useful as a baseline for investigating how forest ecosystems have changed in response to the last several centuries of climate change and intensive Euro-American land use and as a calibration dataset for paleoecological proxy-based reconstructions of forest composition and structure for earlier time periods. The data products (including raw and smoothed estimates at the 8-km scale) are available at the LTER Network Data Portal as version 1.0.

Quantifying trends and uncertainty in prehistoric forest composition in the upper Midwestern United States.

Forest ecosystems in eastern North America have been in flux for the last several thousand years, well before Euro-American land clearance and the 20th-century onset of anthropogenic climate change. However, the magnitude and uncertainty of prehistoric vegetation change have been difficult to quantify because of the multiple ecological, dispersal, and sedimentary processes that govern the relationship between forest composition and fossil pollen assemblages. Here we extend STEPPS, a Bayesian hierarchical spatiotemporal pollen-vegetation model, to estimate changes in forest composition in the upper Midwestern United States from about 2,100 to 300 yr ago. Using this approach, we find evidence for large changes in the relative abundance of some species, and significant changes in community composition. However, these changes took place against a regional background of changes that were small in magnitude or not statistically significant, suggesting complexity in the spatiotemporal patterns of forest dynamics. The single largest change is the infilling of Tsuga canadensis in northern Wisconsin over the past 2,000 yr. Despite range infilling, the range limit of T. canadensis was largely stable, with modest expansion westward. The regional ecotone between temperate hardwood forests and northern mixed hardwood/conifer forests shifted southwestward by 15-20 km in Minnesota and northwestern Wisconsin. Fraxinus, Ulmus, and other mesic hardwoods expanded in the Big Woods region of southern Minnesota. The increasing density of paleoecological data networks and advances in statistical modeling approaches now enables the confident detection of subtle but significant changes in forest composition over the last 2,000 yr.

A century of genetic variation inferred from a persistent soil-stored seed bank.

Stratigraphic accretion of dormant propagules in soil can result in natural archives useful for studying ecological and evolutionary responses to environmental change. Few attempts have been made, however, to use soil-stored seed banks as natural archives, in part because of concerns over nonrandom attrition and mixed stratification. Here, we examine the persistent seed bank of Schoenoplectus americanus, a foundational brackish marsh sedge, to determine whether it can serve as a resource for reconstructing historical records of demographic and population genetic variation. After assembling profiles of the seed bank from radionuclide-dated soil cores, we germinated seeds to "resurrect" cohorts spanning the 20th century. Using microsatellite markers, we assessed genetic diversity and differentiation among depth cohorts, drawing comparisons to extant plants at the study site and in nearby and more distant marshes. We found that seed density peaked at intermediate soil depths. We also detected genotypic differences among cohorts as well as between cohorts and extant plants. Genetic diversity did not decline with depth, indicating that the observed pattern of differentiation is not due to attrition. Patterns of differentiation within and among extant marshes also suggest that local populations persist as aggregates of small clones, likely reflecting repeated seedling recruitment and low immigration from admixed regional gene pools. These findings indicate that persistent and stratified soil-stored seed banks merit further consideration as resources for reconstructing decadal- to century-long records that can lend insight into the tempo and nature of ecological and evolutionary processes that shape populations over time.

Correction: Statistically-Estimated Tree Composition for the Northeastern United States at Euro-American Settlement.

[This corrects the article DOI: 10.1371/journal.pone.0150087.].

Novel and Lost Forests in the Upper Midwestern United States, from New Estimates of Settlement-Era Composition, Stem Density, and Biomass.

BACKGROUND: EuroAmerican land-use and its legacies have transformed forest structure and composition across the United States (US). More accurate reconstructions of historical states are critical to understanding the processes governing past, current, and future forest dynamics. Here we present new gridded (8x8km) reconstructions of pre-settlement (1800s) forest composition and structure from the upper Midwestern US (Minnesota, Wisconsin, and most of Michigan), using 19th Century Public Land Survey System (PLSS), with estimates of relative composition, above-ground biomass, stem density, and basal area for 28 tree types. This mapping is more robust than past efforts, using spatially varying correction factors to accommodate sampling design, azimuthal censoring, and biases in tree selection. CHANGES IN FOREST STRUCTURE: We compare pre-settlement to modern forests using US Forest Service Forest Inventory and Analysis (FIA) data to show the prevalence of lost forests (pre-settlement forests with no current analog), and novel forests (modern forests with no past analogs). Differences between pre-settlement and modern forests are spatially structured owing to differences in land-use impacts and accompanying ecological responses. Modern forests are more homogeneous, and ecotonal gradients are more diffuse today than in the past. Novel forest assemblages represent 28% of all FIA cells, and 28% of pre-settlement forests no longer exist in a modern context. Lost forests include tamarack forests in northeastern Minnesota, hemlock and cedar dominated forests in north-central Wisconsin and along the Upper Peninsula of Michigan, and elm, oak, basswood and ironwood forests along the forest-prairie boundary in south central Minnesota and eastern Wisconsin. Novel FIA forest assemblages are distributed evenly across the region, but novelty shows a strong relationship to spatial distance from remnant forests in the upper Midwest, with novelty predicted at between 20 to 60km from remnants, depending on historical forest type. The spatial relationships between remnant and novel forests, shifts in ecotone structure and the loss of historic forest types point to significant challenges for land managers if landscape restoration is a priority. The spatial signals of novelty and ecological change also point to potential challenges in using modern spatial distributions of species and communities and their relationship to underlying geophysical and climatic attributes in understanding potential responses to changing climate. The signal of human settlement on modern forests is broad, spatially varying and acts to homogenize modern forests relative to their historic counterparts, with significant implications for future management.

Statistically-Estimated Tree Composition for the Northeastern United States at Euro-American Settlement.

We present a gridded 8 km-resolution data product of the estimated composition of tree taxa at the time of Euro-American settlement of the northeastern United States and the statistical methodology used to produce the product from trees recorded by land surveyors. Composition is defined as the proportion of stems larger than approximately 20 cm diameter at breast height for 22 tree taxa, generally at the genus level. The data come from settlement-era public survey records that are transcribed and then aggregated spatially, giving count data. The domain is divided into two regions, eastern (Maine to Ohio) and midwestern (Indiana to Minnesota). Public Land Survey point data in the midwestern region (ca. 0.8-km resolution) are aggregated to a regular 8 km grid, while data in the eastern region, from Town Proprietor Surveys, are aggregated at the township level in irregularly-shaped local administrative units. The product is based on a Bayesian statistical model fit to the count data that estimates composition on the 8 km grid across the entire domain. The statistical model is designed to handle data from both the regular grid and the irregularly-shaped townships and allows us to estimate composition at locations with no data and to smooth over noise caused by limited counts in locations with data. Critically, the model also allows us to quantify uncertainty in our composition estimates, making the product suitable for applications employing data assimilation. We expect this data product to be useful for understanding the state of vegetation in the northeastern United States prior to large-scale Euro-American settlement. In addition to specific regional questions, the data product can also serve as a baseline against which to investigate how forests and ecosystems change after intensive settlement. The data product is being made available at the NIS data portal as version 1.0.

Habitat differences influence genetic impacts of human land use on the American beech (Fagus grandifolia).

Natural reforestation after regional forest clearance is a globally common land-use sequence. The genetic recovery of tree populations in these recolonized forests may depend on the biogeographic setting of the landscape, for instance whether they are in the core or in the marginal part of the species' range. Using data from 501 individuals genotyped across 7 microsatellites, we investigated whether regional differences in habitat quality affected the recovery of genetic variation in a wind-pollinated tree species, American beech (Fagus grandifolia) in Massachusetts. We compared populations in forests that were recolonized following agricultural abandonment to those in remnant forests that have only been logged in both central inland and marginal coastal regions. Across all populations in our entire study region, recolonized forests showed limited reduction of genetic diversity as only observed heterozygosity was significantly reduced in these forests (H(O) = 0.520 and 0.590, respectively). Within inland region, this pattern was observed, whereas in the coast, recolonized populations exhibited no reduction in all genetic diversity estimates. However, genetic differentiation among recolonized populations in marginal coastal habitat increased (F(st) logged = 0.072; F(st) secondary = 0.249), with populations showing strong genetic structure, in contrast to inland region. These results indicate that the magnitude of recovery of genetic variation in recolonized populations can vary at different habitats.

Ancient DNA from lake sediments: bridging the gap between paleoecology and genetics.

BACKGROUND: Quaternary plant ecology in much of the world has historically relied on morphological identification of macro- and microfossils from sediments of small freshwater lakes. Here, we report new protocols that reliably yield DNA sequence data from Holocene plant macrofossils and bulk lake sediment used to infer ecological change. This will allow changes in census populations, estimated from fossils and associated sediment, to be directly associated with population genetic changes. RESULTS: We successfully sequenced DNA from 64 samples (out of 126) comprised of bulk sediment and seeds, leaf fragments, budscales, and samaras extracted from Holocene lake sediments in the western Great Lakes region of North America. Overall, DNA yields were low. However, we were able to reliably amplify samples with as few as 10 copies of a short cpDNA fragment with little detectable PCR inhibition. Our success rate was highest for sediments < 2000 years old, but we were able to successfully amplify DNA from samples up to 4600 years old. DNA sequences matched the taxonomic identity of the macrofossil from which they were extracted 79% of the time. Exceptions suggest that DNA molecules from surrounding nearby sediments may permeate or adhere to macrofossils in sediments. CONCLUSIONS: An ability to extract ancient DNA from Holocene sediments potentially allows exciting new insights into the genetic consequences of long-term environmental change. The low DNA copy numbers we found in fossil material and the discovery of multiple sequence variants from single macrofossil extractions highlight the need for careful experimental and laboratory protocols. Further application of these protocols should lead to better understanding of the ecological and evolutionary consequences of environmental change.

Range-wide distribution of genetic diversity in the North American tree Juglans cinerea: a product of range shifts, not ecological marginality or recent population decline.

The spatial distribution of genetic diversity is a product of recent and historical ecological processes, as well as anthropogenic activities. A current challenge in population and conservation genetics is to disentangle the relative effects of these processes, as a first step in predicting population response to future environmental change. In this investigation, we compare the influence of contemporary population decline, contemporary ecological marginality and postglacial range shifts. Using classical model comparison procedures and Bayesian methods, we have identified postglacial range shift as the clear determinant of genetic diversity, differentiation and bottlenecks in 29 populations of butternut, Juglans cinerea L., a North American outcrossing forest tree. Although butternut has experienced dramatic 20th century decline because of an introduced fungal pathogen, our analysis indicates that recent population decline has had less genetic impact than postglacial recolonization history. Location within the range edge vs. the range core also failed to account for the observed patterns of diversity and differentiation. Our results suggest that the genetic impact of large-scale recent population losses in forest trees should be considered in the light of Pleistocene-era large-scale range shifts that may have had long-term genetic consequences. The data also suggest that the population dynamics and life history of wind-pollinated forest trees may provide a buffer against steep population declines of short duration, a result having important implications for habitat management efforts, ex situ conservation sampling and population viability analysis.

Mapping Ancient Forests: Bayesian Inference for Spatio-temporal Trends in Forest Composition Using the Fossil Pollen Proxy Record.

Ecologists use the relative abundance of fossil pollen in sediments to estimate how tree species abundances change over space and time. To predict historical forest composition and quantify the available information, we build a Bayesian hierarchical model of forest composition in central New England, USA, based on pollen in a network of ponds. The critical relationships between abundances of taxa in the pollen record and abundances as actual vegetation are estimated for the modern and colonial periods, for which both pollen and direct vegetation data are available, based on a latent multivariate spatial process representing forest composition. For time periods in the past with only pollen data, we use the estimated model parameters to constrain predictions about the latent spatio-temporal process conditional on the pollen data. We develop an innovative graphical assessment of feature significance to help to infer which spatial patterns are reliably estimated. The model allows us to estimate the spatial distribution and relative abundances of tree species over the last 2500 years, with an assessment of uncertainty, and to draw inference about how these patterns have changed over time. Cross-validation suggests that our feature significance approach can reliably indicate certain large-scale spatial features for many taxa, but that features on scales smaller than 50 km are difficult to distinguish, as are large-scale features for some taxa. We also use the model to quantitatively investigate ecological hypotheses, including covariate effects on taxa abundances and questions about pollen dispersal characteristics. The critical advantages of our modeling approach over current ecological analyses are the explicit spatio-temporal representation, quantification of abundance on the scale of trees rather than pollen, and uncertainty characterization.

Multidimensional evaluation of managed relocation.

Managed relocation (MR) has rapidly emerged as a potential intervention strategy in the toolbox of biodiversity management under climate change. Previous authors have suggested that MR (also referred to as assisted colonization, assisted migration, or assisted translocation) could be a last-alternative option after interrogating a linear decision tree. We argue that numerous interacting and value-laden considerations demand a more inclusive strategy for evaluating MR. The pace of modern climate change demands decision making with imperfect information, and tools that elucidate this uncertainty and integrate scientific information and social values are urgently needed. We present a heuristic tool that incorporates both ecological and social criteria in a multidimensional decision-making framework. For visualization purposes, we collapse these criteria into 4 classes that can be depicted in graphical 2-D space. This framework offers a pragmatic approach for summarizing key dimensions of MR: capturing uncertainty in the evaluation criteria, creating transparency in the evaluation process, and recognizing the inherent tradeoffs that different stakeholders bring to evaluation of MR and its alternatives.

Comparative phylogeography of unglaciated eastern North America.

Regional phylogeographical studies involving co-distributed animal and plant species have been conducted for several areas, most notably for Europe and the Pacific Northwest of North America. Until recently, phylogeographical studies in unglaciated eastern North America have been largely limited to animals. As more studies emerge for diverse lineages (including plants), it seems timely to assess the phylogeography across this region: (i) comparing and contrasting the patterns seen in plants and animals; (ii) assessing the extent of pseudocongruence; and (iii) discussing the potential applications of regional phylogeography to issues in ecology, such as response to climatic change. Unglaciated eastern North America is a large, geologically and topographically complex area with the species examined having diverse distributions. Nonetheless, some recurrent patterns emerge: (i) maritime - Atlantic vs. Gulf Coast; (ii) Apalachicola River discontinuity; (iii) Tombigbee River discontinuity; (iv) the Appalachian Mountain discontinuity; (v) the Mississippi River discontinuity; and (vi) the Apalachicola River and Mississippi River discontinuities. Although initially documented in animals, most of these patterns are also apparent in plants, providing support for phylogeographical generalizations. These patterns may generally be attributable to isolation and differentiation during Pleistocene glaciation, but in some cases may be older (Pliocene). Molecular studies sometimes agree with longstanding hypotheses of glacial refugia, but also suggest additional possible refugia, such as the southern Appalachian Mountains and areas close to the Laurentide Ice Sheet. Many species exhibit distinct patterns that reflect the unique, rather than the shared, aspects of species' phylogeographical histories. Furthermore, similar modern phylogeographical patterns can result from different underlying causal factors operating at different times (i.e. pseudocongruence). One underemphasized component of pseudocongruence may result from the efforts of researchers to categorize patterns visually - similar patterns may, in fact, not fully coincide, and inferring agreement may obscure the actual patterns and lead to erroneous conclusions. Our modelling analyses indicate no clear spatial patterning and support the hypothesis that phylogeographical structure in diverse temperate taxa is complex and was not shaped by just a few barriers.

Stability of forest biodiversity.

Two hypotheses to explain potentially high forest biodiversity have different implications for the number and kinds of species that can coexist and the potential loss of biodiversity in the absence of speciation. The first hypothesis involves stabilizing mechanisms, which include tradeoffs between species in terms of their capacities to disperse to sites where competition is weak, to exploit abundant resources effectively and to compete for scarce resources. Stabilization results because competitors thrive at different times and places. An alternative, 'neutral model' suggests that stabilizing mechanisms may be superfluous. This explanation emphasizes 'equalizing' mechanisms, because competitive exclusion of similar species is slow. Lack of ecologically relevant differences means that abundances experience random 'neutral drift', with slow extinction. The relative importance of these two mechanisms is unknown, because assumptions and predictions involve broad temporal and spatial scales. Here we demonstrate that predictions of neutral drift are testable using palaeodata. The results demonstrate strong stabilizing forces. By contrast with the neutral prediction of increasing variance among sites over time, we show that variances in post-Glacial tree abundances among sites stabilize rapidly, and abundances remain coherent over broad geographical scales.