Steven E. Travers

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.

The Establishment of Genetically Engineered Canola Populations in the U.S.

Concerns regarding the commercial release of genetically engineered (GE) crops include naturalization, introgression to sexually compatible relatives and the transfer of beneficial traits to native and weedy species through hybridization. To date there have been few documented reports of escape leading some researchers to question the environmental risks of biotech products. In this study we conducted a systematic roadside survey of canola (Brassica napus) populations growing outside of cultivation in North Dakota, USA, the dominant canola growing region in the U.S. We document the presence of two escaped, transgenic genotypes, as well as non-GE canola, and provide evidence of novel combinations of transgenic forms in the wild. Our results demonstrate that feral populations are large and widespread. Moreover, flowering times of escaped populations, as well as the fertile condition of the majority of collections suggest that these populations are established and persistent outside of cultivation.

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.

Shifts in the flowering phenology of the northern Great Plains: patterns over 100 years.

PREMISE OF THE STUDY Climate change is associated with phenological shifts in an increasing number of organisms worldwide. However, accurate estimates of these shifts are dependent on long-term data sets that include phenological observations from before annual average temperatures began to rise. METHODS We compared the first flowering times of native prairie plants between 2007 and 2010 with historical data recorded by O. A. Stevens from 1910 to 1961. By merging climate variable data from the same time period, it also was possible to correlate first flowering dates with associated climate variables. KEY RESULTS Over the past 100 years, spring temperatures in the Red River Valley near Fargo, North Dakota, USA, have increased, and growing seasons have lengthened significantly. Seventy-five percent of the 178 species observed by Stevens had flowering times that were sensitive to at least one variable related to temperature or precipitation. Over the past 4 yr, 5% to 17% of the species observed have significantly shifted their first flowering time either earlier or later relative to the previous century. CONCLUSIONS The results of this study indicate that as spring temperatures in the northern Great Plains have increased and the growing season has lengthened, some spring flowering species have advanced their first flowering time, some fall species have delayed their first flowering, and some species have not changed. Given the importance of flowering timing for reproductive success, the changing climate in the Great Plains is expected to have long-term ecological and evolutionary consequences for native plant species.

The Influence of Starvation and Predators on the Mating Behavior of a Semiaquatic Insect

Few experimental studies of mating behavior have examined mating behavior shifts in response to ecological factors (e.g., predators, starvation). We conducted experiments designed to: (1) examine multiple trade—doffs between predator avoidance, feeding behavior, and copulating duration in a semiaquatic insect (Microvelia austrina); and (2) address the influence of altered copulation duration on male reproductive success. To examine multiple trade—offs, we used a 2 x 2 factorial design where we measured the amount of time that mating microveliids remained in tandem, for starved and fed microvellids in the presence and absence of predaceous water striders (Gerris remigis). We also looked at the effects of presence vs. absence of green sunfish (Lepomis cyanellus) on microveliid tandem duration. To address the impact of premature pair separation on male mating success, we separated paired microvellids in field populations and measured the time required for each sex to find new mates. To examine the effects of local sex ratio on remating times of males and females, we quantified the sex ratio of field populations via periodic censuses and correlated local sex ratio with remating times. Finally, to address oviposition rates while pairs are in tandem, we measured female oviposition patterns relative to tandem duration for poorly fed and well—fed females. Both Starvation and gerrid presence significantly reduced tandem duration. As a result of male—biased sex ratios, males that prematurely separated from females often faced long search times before securing a new mate. Females oviposited at a constant rate while in tandem. A simple computer simulation incorporating the above observations suggests that reductions in tandem duration can decrease fertilization rates.

Flowering date of taxonomic families predicts phenological sensitivity to temperature: Implications for forecasting the effects of climate change on unstudied taxa

PREMISE OF THE STUDY Numerous long-term studies in seasonal habitats have tracked interannual variation in first flowering date (FFD) in relation to climate, documenting the effect of warming on the FFD of many species. Despite these efforts, long-term phenological observations are still lacking for many species. If we could forecast responses based on taxonomic affinity, however, then we could leverage existing data to predict the climate-related phenological shifts of many taxa not yet studied. METHODS We examined phenological time series of 1226 species occurrences (1031 unique species in 119 families) across seven sites in North America and England to determine whether family membership (or family mean FFD) predicts the sensitivity of FFD to standardized interannual changes in temperature and precipitation during seasonal periods before flowering and whether families differ significantly in the direction of their phenological shifts. KEY RESULTS Patterns observed among species within and across sites are mirrored among family means across sites; early-flowering families advance their FFD in response to warming more than late-flowering families. By contrast, we found no consistent relationships among taxa between mean FFD and sensitivity to precipitation as measured here. CONCLUSIONS Family membership can be used to identify taxa of high and low sensitivity to temperature within the seasonal, temperate zone plant communities analyzed here. The high sensitivity of early-flowering families (and the absence of early-flowering families not sensitive to temperature) may reflect plasticity in flowering time, which may be adaptive in environments where early-season conditions are highly variable among years.

Photosynthetic and growth responses of reciprocal hybrids to variation in water and nitrogen availability

UNLABELLED PREMISE OF THE STUDY Fitness of plant hybrids often depends upon the environment, but physiological mechanisms underlying the differential responses to habitat are poorly understood. We examined physiological responses of Ipomopsis species and hybrids, including reciprocal F(1)s and F(2)s, to variation in soil moisture and nitrogen. • METHODS To examine responses to moisture, we subjected plants to a dry-down experiment. Nitrogen was manipulated in three independent experiments, one in the field and two in common environments. • KEY RESULTS Plants with I. tenuituba cytoplasmic background had lower optimal soil moisture for photosynthesis, appearing better adapted to dry conditions, than plants with I. aggregata cytoplasm. This result supported a prediction from prior studies. The species and hybrids did not differ greatly in physiological responses to nitrogen. An increase in soil nitrogen increased leaf nitrogen, carbon assimilation, integrated water-use efficiency, and growth, but the increases in growth were not mediated primarily by an increase in photosynthesis. In neither the field, nor in common-garden studies, did physiological responses to soil nitrogen differ detectably across plant types, although only I. aggregata and hybrids increased seed production in the field. • CONCLUSIONS These results demonstrate differences in photosynthetic responses between reciprocal hybrids and suggest that water use is more important than nitrogen in explaining the relative photosynthetic performance of these hybrids compared to their parents.

Genetic Variation of Sclerotinia sclerotiorum from Multiple Crops in the North Central United States.

Sclerotinia sclerotiorum is an important pathogen of numerous crops in the North Central region of the United States. The objective of this study was to examine the genetic diversity of 145 isolates of the pathogen from multiple hosts in the region. Mycelial compatibility groups (MCG) and microsatellite haplotypes were determined and analyzed for standard estimates of population genetic diversity and the importance of host and distance for genetic variation was examined. MCG tests indicated there were 49 different MCGs in the population and 52 unique microsatellite haplotypes were identified. There was an association between MCG and haplotype such that isolates belonging to the same MCG either shared identical haplotypes or differed at no more than 2 of the 12 polymorphic loci. For the majority of isolates, there was a one-to-one correspondence between MCG and haplotype. Eleven MCGs shared haplotypes. A single haplotype was found to be prevalent throughout the region. The majority of genetic variation in the isolate collection was found within rather than among host crops, suggesting little genetic divergence of S. sclerotiorum among hosts. There was only weak evidence of isolation by distance. Pairwise population comparisons among isolates from canola, dry bean, soybean and sunflower suggested that gene flow between host-populations is more common for some crops than others. Analysis of linkage disequilibrium in the isolates from the four major crops indicated primarily clonal reproduction, but also evidence of genetic recombination for isolates from canola and sunflower. Accordingly, genetic diversity was highest for populations from canola and sunflower. Distribution of microsatellite haplotypes across the study region strongly suggest that specific haplotypes of S. sclerotiorum are often found on multiple crops, movement of individual haplotypes among crops is common and host identity is not a barrier to gene flow for S. sclerotiorum in the north central United States.

First‐flowering dates of plants in the Northern Great Plains

Phenological observations of plant flowering patterns provide useful information for studying the ecological impact of global climate change over long-term periods. However, the long-term data sets with which meaningful comparisons can be made are rare, especially in the less-populated Northern Great Plains region of North America. Here we present the observations of first-flowering time of native and nonnative plant species in North Dakota and Minnesota over the course of 51 years in the last century. Orin A. Stevens recorded the first-flowering time of 753 species in the vicinity of Fargo, North Dakota, USA, and throughout North Dakota from 1910 to 1961. These data offer baseline indications of both the timing of first flowering and the presence/absence for a wide variety of plants in a region of North America with a relatively short growing season. The complete data sets corresponding to abstracts published in the Data Papers section of the journal are published electronically in Ecological Archives at http://esapubs.org/archive. (The accession number for each Data Paper is givendirectly beneath the title.)