Kjell Bolmgren

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.

CONTRASTING FLOWERING PHENOLOGY AND SPECIES RICHNESS IN ABIOTICALLY AND BIOTICALLY POLLINATED ANGIOSPERMS

Abstract Biotic pollination is thought to correlate with increased interspecific competition for pollination among plants and a higher speciation rate. In this study we compared patterns of flowering phenology and species richness between abiotically (wind) and biotically pollinated plants, using phylogenetically independent contrasts. We compiled phenological data from eight local seasonal floras, in which we found geographically overlapping sister clades. Of 65 documented origins of wind pollination, we were able to use up to 17 independent contrasts. In contrast to previous studies we found no difference in global species richness between wind‐ and biotically pollinated sister clades. Regarding phenology, we found wider phenological spread in biotically pollinated clades, earlier flowering onset in wind‐pollinated trees, but no difference in duration of flowering between pollination modes. These results corroborate previous views that niche space is more constrained for wind‐pollinated species, and that niche partitioning is less important between wind‐pollinated plants compared to plants pollinated by animals.

Herbarium Data Reveal an Association between Fleshy Fruit Type and Earlier Flowering Time

Herbarium phenology data were evaluated and then applied in a phylogenetically independent contrast study in which flowering times were compared between fleshy and nonfleshy‐fruited plants growing in the north‐temperate provinces of Uppland and Södermanland, southeastern Sweden (59°–60°N). To evaluate herbarium phenology data, flowering‐time information taken from herbarium specimens in the Swedish Natural History Museum (S) was compared with two independent field phenology data sets. Herbarium collections and the field studies were restricted to the province of Uppland. Flowering times derived from herbarium specimens correlated equally well with each of the two field‐phenology data sets as the field phenology data sets did to each other. Differences between flowering times derived from field and herbarium collections were not affected by the number of herbarium specimens used. However, these differences in flowering times were affected by flowering season such that herbarium‐derived flowering times were later for early spring‐flowering species and earlier for late summer‐flowering species when compared with flowering times derived from field data. In the phylogenetically independent contrast study of mean flowering times in fleshy‐ compared with nonfleshy‐fruited plants, herbarium data were compiled for 77 species in 17 phylogenetically independent contrasts. Flowering time was found to be earlier for fleshy‐fruited taxa, illustrating the evolutionary interdependence between flowering and fruiting phases and the constraining effects of a north‐temperate climate on phenology evolution. This study shows that herbaria are reliable and time‐saving data sources for comparative phenology studies and allow for studies at large phylogenetic and geographic scales that would otherwise be impossible.

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.

Specific leaf area as a superior predictor of changes in field layer abundance during forest succession

Question: How accurately can a suite of suggested functional traits predict plant species response to succession from semiopen woodland to closed deciduous canopy forest? Location: Southeastern Sweden. Methods: Abundance of 46 field-layer plant species in a temperate deciduous forest, measured as frequency of occupied plots, was estimated in 1961, 1970 and 2003. Abundance change over time across species was tested for correlations with functional traits and literature information on habitat preference. Results: Increase in abundance was positively correlated with specific leaf area (SLA), weakly negatively correlated with seed mass and not significantly correlated with plant height or start, peak and length of the flowering period. Change in abundance was correlated with the Ellenberg light indicator value, whereas no correlations were found with Ellenberg values for nitrogen, calcium and moisture, or forest preference according to the literature. Conclusions: SLA was a better predictor of how field layer plants responded to succession from semi-open woodland to closed canopy forest than empirically-derived measures of habitat preference. The same holds for SLA in relation to seed size, indicating that interactions in the established life-cycle phase are more important than the recruitment phase for species response to succession.

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.

Generic limits in Rhamnus L. s.l. (Rhamnaceae) inferred from nuclear and chloroplast DNA sequence phylogenies

This study tested the monophyly of the previously proposed genera Alaternus, Frangula, Oreoherzogia, and Rhamnus s.str., and the phylogenetic relations suggested by Grubov (1949), within the Rhamnu ...

The use of synchronization measures in studies of plant reproductive phenology

Phenological synchronization of plant reproduction has generated a lot of interest during the last decades. Being an important character in the interactions between plants and their pollinators, dispersers, predators or herbivores, several adaptive hypotheses have addressed variation in synchronization (Rathcke and Lacey 1985, Primack 1987, Gorchov 1990; but see Ollerton and Lack 1992). Synchronized flowering or fruiting could satiate predators (Augspurger 1981) as well as attract pollinators and dispersers through its mass display effect (Rathcke and Lacey 1985). The level of within-individual and between-individual synchronization could also be related to fruit quality through the level of outcrossing (Stephenson 1982, Bawa 1983, Primack 1987). Also lack of synchrony may be interpreted as adaptive. In accordance with Gillespies (1977) ideas on risk spreading, asynchronous reproductive phonology would be a way to hedge ones bets within the season. By opening flowers or ripening fruits asynchronously the plant could track the resources of pollinators, dispersers or any abiotic key-factor. Asynchronous flowering/fruiting has also been interpreted as a strategy to escape predators (Eriksson 1995). Willson and Thompson (1982) proposed bicoloured fruit displays as attractive to dispersers, thereby enhancing seed dispersal. For species with temporally bicoloured fruit ripening, asynchronous ripening would be a prerequisite to accomplish such an attractive display. Patterns of synchronization could be described both at the between-individual and within-individual levels. As adaptive advantages of between-individual synchronization could be confounded by within-individual patterns of synchronization we need to investigate the connection between these two levels. Earlier studies have almost always focused on between-individual synchronization and have thus become concerned with early, late and intermediate, or onand off-peak individuals (Augspurger 1981, Dieringer 1991; but see Marquis 1988, Gorchov 1990). That is, they were more interested in the mean timing of the phenophase than the distribution within the phenological phase. Some studies have used a quantification of betweenindividual synchronization based on flowering overlap (Augspurger 1983, Marquis 1988, G6mez 1993), but none of these quantitative measures has the ability to distinguish between different within-individual synchronization levels. As such patterns could be important for the reproductive success of plants we need to develop quantitative measures of within-individual synchronization. In their review of plant phenology, Rathcke and Lacey (1985) put synchronization on equal footing as variance. This straightforward approach was used by one of the three studies I have found that have quantified within-individual synchronization (Gorchov 1990). In his study of flowering and fruiting in 12 insect-pollinated and fleshy-fruited species, Gorchov (1990) used the standard deviation of onset of individual flowers/fruits (SDonset) as his synchronization measure. Any biological effect of such a dispersion could be confounded by variation in flower/fruit persistence. If flower/fruit persistence is extended, any effect of variation in the level of dispersion may be negligible. The two other studies using a quantified measure of synchronization do include flower/fruit persistence in their studies (Eriksson and Ehrlen 1991, Bolmgren 1997). Eriksson and Ehrlen (1991) compared the fruiting phenology of 34 fleshy-fruited species and they calculated the individuals level of synchronization as the quotient (fruit persistence/fruiting range). Obviously, such a measure does not differ between individuals with high and low SDonsetI Both of the parameters omitted by Gorchov (1990) and Eriksson and Ehrlen (1991), persistence and dispersion of onset, respectively, were included by Primack (1985a) in his general description of flowering phenol-

Climate change and the optimal flowering time of annual plants in seasonal environments

Long-term phenology monitoring has documented numerous examples of changing flowering dates during the last century. A pivotal question is whether these phenological responses are adaptive or not under directionally changing climatic conditions. We use a classic dynamic growth model for annual plants, based on optimal control theory, to find the fitness-maximizing flowering time, defined as the switching time from vegetative to reproductive growth. In a typical scenario of global warming, with advanced growing season and increased productivity, optimal flowering time advances less than the start of the growing season. Interestingly, increased temporal spread in production over the season may either advance or delay the optimal flowering time depending on overall productivity or season length. We identify situations where large phenological changes are necessary for flowering time to remain optimal. Such changes also indicate changed selection pressures. In other situations, the model predicts advanced phenology on a calendar scale, but no selection for early flowering in relation to the start of the season. We also show that the optimum is more sensitive to increased productivity when productivity is low than when productivity is high. All our results are derived using a general, graphical method to calculate the optimal flowering time applicable for a large range of shapes of the seasonal production curve. The model can thus explain apparent maladaptation in phenological responses in a multitude of scenarios of climate change. We conclude that taking energy allocation trade-offs and appropriate time scales into account is critical when interpreting phenological patterns.