Jenica M. Allen

Warming experiments underpredict plant phenological responses to climate change

Warming experiments are increasingly relied on to estimate plant responses to global climate change. For experiments to provide meaningful predictions of future responses, they should reflect the empirical record of responses to temperature variability and recent warming, including advances in the timing of flowering and leafing. We compared phenology (the timing of recurring life history events) in observational studies and warming experiments spanning four continents and 1,634 plant species using a common measure of temperature sensitivity (change in days per degree Celsius). We show that warming experiments underpredict advances in the timing of flowering and leafing by 8.5-fold and 4.0-fold, respectively, compared with long-term observations. For species that were common to both study types, the experimental results did not match the observational data in sign or magnitude. The observational data also showed that species that flower earliest in the spring have the highest temperature sensitivities, but this trend was not reflected in the experimental data. These significant mismatches seem to be unrelated to the study length or to the degree of manipulated warming in experiments. The discrepancy between experiments and observations, however, could arise from complex interactions among multiple drivers in the observational data, or it could arise from remediable artefacts in the experiments that result in lower irradiance and drier soils, thus dampening the phenological responses to manipulated warming. Our results introduce uncertainty into ecosystem models that are informed solely by experiments and suggest that responses to climate change that are predicted using such models should be re-evaluated.

Phylogenetic conservatism in plant phenology

Summary 1. Phenological events – defined points in the life cycle of a plant or animal – have been regarded as highly plastic traits, reflecting flexible responses to various environmental cues. 2. The ability of a species to track, via shifts in phenological events, the abiotic environment through time might dictate its vulnerability to future climate change. Understanding the predictors and drivers of phenological change is therefore critical. 3. Here, we evaluated evidence for phylogenetic conservatism – the tendency for closely related species to share similar ecological and biological attributes – in phenological traits across flowering plants. We aggregated published and unpublished data on timing of first flower and first leaf, encompassing ~4000 species at 23 sites across the Northern Hemisphere. We reconstructed the phylogeny for the set of included species, first, using the software program Phylomatic, and second, from DNA data. We then quantified phylogenetic conservatism in plant phenology within and across sites. 4. We show that more closely related species tend to flower and leaf at similar times. By contrasting mean flowering times within and across sites, however, we illustrate that it is not the time of year that is conserved, but rather the phenological responses to a common set of abiotic cues. 5. Our findings suggest that species cannot be treated as statistically independent when modelling phenological responses. 6. Synthesis. Closely related species tend to resemble each other in the timing of their life-history events, a likely product of evolutionarily conserved responses to environmental cues. The search for the underlying drivers of phenology must therefore account for species’ shared evolutionary histories.

Sensitivity of Spring Phenology to Warming Across Temporal and Spatial Climate Gradients in Two Independent Databases

Disparate ecological datasets are often organized into databases post hoc and then analyzed and interpreted in ways that may diverge from the purposes of the original data collections. Few studies, however, have attempted to quantify how biases inherent in these data (for example, species richness, replication, climate) affect their suitability for addressing broad scientific questions, especially in under-represented systems (for example, deserts, tropical forests) and wild communities. Here, we quantitatively compare the sensitivity of species first flowering and leafing dates to spring warmth in two phenological databases from the Northern Hemisphere. One—PEP725—has high replication within and across sites, but has low species diversity and spans a limited climate gradient. The other—NECTAR—includes many more species and a wider range of climates, but has fewer sites and low replication of species across sites. PEP725, despite low species diversity and relatively low seasonality, accurately captures the magnitude and seasonality of warming responses at climatically similar NECTAR sites, with most species showing earlier phenological events in response to warming. In NECTAR, the prevalence of temperature responders significantly declines with increasing mean annual temperature, a pattern that cannot be detected across the limited climate gradient spanned by the PEP725 flowering and leafing data. Our results showcase broad areas of agreement between the two databases, despite significant differences in species richness and geographic coverage, while also noting areas where including data across broader climate gradients may provide added value. Such comparisons help to identify gaps in our observations and knowledge base that can be addressed by ongoing monitoring and research efforts. Resolving these issues will be critical for improving predictions in understudied and under-sampled systems outside of the temperature seasonal mid-latitudes.

Socioeconomics drive woody invasive plant richness in New England, USA through forest fragmentation

Woody invasive plants are an increasing component of the New England flora. Their success and geographic spread are mediated in part by landscape characteristics. We tested whether woody invasive plant richness was higher in landscapes with many forest edges relative to other forest types and explained land use/land cover and forest fragmentation patterns using socioeconomic and physical variables. Our models demonstrated that woody invasive plant richness was higher in landscapes with more edge forest relative to patch, perforated, and especially core forest types. Using spatially-explicit, hierarchical Bayesian, compositional data models we showed that infrastructure and physical factors, including road length and elevation range, and time-lagged socioeconomic factors, primarily population, help to explain development and forest fragmentation patterns. Our social–ecological approach identified landscape patterns driven by human development and linked them to increased woody plant invasions. Identifying these landscape patterns will aid ongoing efforts to use current distribution patterns to better predict where invasive species may occur in unsampled regions under current and future conditions.

Global shifts in the phenological synchrony of species interactions over recent decades

Significance Shifts in the timing of species interactions are often cited as a consequence of climate change and, if present, are expected to have wide-reaching implications for ecological communities. Our knowledge about these shifts mostly comes from single systems, which have provided no clear picture, thus limiting our understanding of how species interactions may be responding overall. Using a new global database based on long-term data on the seasonal timing of biological events for pairwise species interactions, we find that the relative timing of interacting species has changed substantially in recent decades. The observed shifts are greater in magnitude than before recent climate change began, suggesting that there will be widespread warming-related shifts in the synchrony of species in the future. Phenological responses to climate change (e.g., earlier leaf-out or egg hatch date) are now well documented and clearly linked to rising temperatures in recent decades. Such shifts in the phenologies of interacting species may lead to shifts in their synchrony, with cascading community and ecosystem consequences. To date, single-system studies have provided no clear picture, either finding synchrony shifts may be extremely prevalent [Mayor SJ, et al. (2017) Sci Rep 7:1902] or relatively uncommon [Iler AM, et al. (2013) Glob Chang Biol 19:2348–2359], suggesting that shifts toward asynchrony may be infrequent. A meta-analytic approach would provide insights into global trends and how they are linked to climate change. We compared phenological shifts among pairwise species interactions (e.g., predator–prey) using published long-term time-series data of phenological events from aquatic and terrestrial ecosystems across four continents since 1951 to determine whether recent climate change has led to overall shifts in synchrony. We show that the relative timing of key life cycle events of interacting species has changed significantly over the past 35 years. Further, by comparing the period before major climate change (pre-1980s) and after, we show that estimated changes in phenology and synchrony are greater in recent decades. However, there has been no consistent trend in the direction of these changes. Our findings show that there have been shifts in the timing of interacting species in recent decades; the next challenges are to improve our ability to predict the direction of change and understand the full consequences for communities and ecosystems.

Climate change both facilitates and inhibits invasive plant ranges in New England

Significance Invasive species are often expected to benefit from novel conditions encountered with global change. Our range models based on demography show that invasive Alliaria petiolata (garlic mustard) may have much lower establishment in New England under future climate, despite prolific success under current climate, whereas other invasive and native plants may expand their ranges. Forecasts suggest that management should focus on inhibiting northward spread of A. petiolata into unoccupied areas and understanding source–sink population dynamics and how community dynamics might respond to loss of A. petiolata (it modifies soil properties). Our methods illustrate inadequacy of current approaches to forecasting invasions in progress, which are based on correlations between species’ occurrence and environment and illustrate critical need for mechanistic studies. Forecasting ecological responses to climate change, invasion, and their interaction must rely on understanding underlying mechanisms. However, such forecasts require extrapolation into new locations and environments. We linked demography and environment using experimental biogeography to forecast invasive and native species’ potential ranges under present and future climate in New England, United States to overcome issues of extrapolation in novel environments. We studied two potentially nonequilibrium invasive plants’ distributions, Alliaria petiolata (garlic mustard) and Berberis thunbergii (Japanese barberry), each paired with their native ecological analogs to better understand demographic drivers of invasions. Our models predict that climate change will considerably reduce establishment of a currently prolific invader (A. petiolata) throughout New England driven by poor demographic performance in warmer climates. In contrast, invasion of B. thunbergii will be facilitated because of higher growth and germination in warmer climates, with higher likelihood to establish farther north and in closed canopy habitats in the south. Invasion success is in high fecundity for both invasive species and demographic compensation for A. petiolata relative to native analogs. For A. petiolata, simulations suggest that eradication efforts would require unrealistic efficiency; hence, management should focus on inhibiting spread into colder, currently unoccupied areas, understanding source–sink dynamics, and understanding community dynamics should A. petiolata (which is allelopathic) decline. Our results—based on considerable differences with correlative occurrence models typically used for such biogeographic forecasts—suggest the urgency of incorporating mechanism into range forecasting and invasion management to understand how climate change may alter current invasion patterns.

Development and characterization of microsatellite markers for Berberis thunbergii (Berberidaceae).

PREMISE OF THE STUDY Microsatellite markers were isolated and characterized in Berberis thunbergii, an invasive and ornamental shrub in the eastern United States, to assess genetic diversity among populations and potentially identify horticultural cultivars. METHODS AND RESULTS A total of 12 loci were identified for the species. Eight of the loci were polymorphic and were screened in 24 individuals from two native (Tochigi and Ibaraki prefectures, Japan) and one invasive (Connecticut, USA) population and 21 horticultural cultivars. The number of alleles per locus ranged from three to seven, and observed heterozygosity ranged from 0.048 to 0.636. CONCLUSIONS These new markers will provide tools for examining genetic relatedness of B. thunbergii plants in the native and invasive range, including phylogeographic studies and assessment of rapid evolution in the invasive range. These markers may also provide tools for examining hybridization with other related species in the invasive range.

Predicting land use/cover change in Long Island Sound Watersheds and its effect on invasive species: a case study for glossy buckthorn

ABSTRACT Land use/cover change (LUCC) is a major threat to ecosystems. It may affect the abundance and distribution of species. Despite the importance of LUCC to ecological patterns and processes, few quantitative projections are available for use in ecological modelling. To fill in this literature gap, we constructed a LUCC model for Long Island Sound Watersheds (LISW) and explored the potential effect of the future LUCC on the range size of an invasive species (glossy buckthorn, Frangula alnus). We first applied the multi-layer perceptron–Markov chain model to predict the future LUCC in the LISW area within New England, USA, and then used the predicted land use/cover data as input into a species distribution model to simulate the future range size of glossy buckthorn. Our results indicate that under the current LUCC trend, there is a continued loss of forest and an increase of developed land in the near future, and this LUCC affects the relative suitability for glossy buckthorn.

Species distribution model for the ‘Northern’ Oak hairstreak (Satyrium favonius ontario) with comments on its conservation status in the northeastern United States

Satyrium favonius ontario: (W. H. Edwards) (Lepidoptera: Lycaenidae) is considered to be a rare butterfly in the northeastern United States. It receives legal protection in the state of Massachusetts as a Species of Special Concern. We studied the ecology and natural history of a colony of S. f. ontario at Great Blue Hills Reservation in Canton, Massachusetts. In addition, we assembled a database of confirmed S. f. ontario occurrences (n = 362) and used this along with climate and oak abundance data to build a species distribution model for the northeastern portion of the butterfly’s range in the United States. The model predicts that essentially the entirety of southern New England is suitable for the species, and thus its modeled distribution extends well north of all documented colonies/localities. Just two climate variables, precipitation seasonality and minimum temperature of the coldest month, explained 95% of the model and largely determined relative suitability predictions. We make the case that the hairstreak is a canopy-dwelling insect that sporadically makes ground-level visits, and that its assumed regional rarity is due to detection difficulties rather than demographic rarity. While the butterfly may be imperiled and worthy of legal protection in portions of its range, we question the validity of population estimates and necessity of conservation efforts based on ground-level adult sightings, and recommend larval sampling using burlap bands as a more reliable method to census this butterfly. We also discuss the possibility that other Satyrium and more distantly related hairstreaks (e.g., Callophrys hesseli and Parrhasius m-album) may be additional examples of temperate, canopy-based butterflies.