Paul J. CaraDonna

Shifts in flowering phenology reshape a subalpine plant community

Significance Seasonal timing of biological events, phenology, is one of the strongest bioindicators of climate change. Our general understanding of phenological responses to climate change is based almost solely on the first day on which an event is observed, limiting our understanding of how ecological communities may be responding as a whole. Using a unique long-term record of flowering phenology from Colorado, we find that the number of species changing their flowering times likely has been underestimated and the magnitude of phenological change overestimated. In addition to earlier first flowering, we document a diverse assortment of other changes, such as delayed last flowering, as temperatures warm. This variety of species-level phenological shifts has ultimately reshaped various temporal components of the plant community. Phenology—the timing of biological events—is highly sensitive to climate change. However, our general understanding of how phenology responds to climate change is based almost solely on incomplete assessments of phenology (such as first date of flowering) rather than on entire phenological distributions. Using a uniquely comprehensive 39-y flowering phenology dataset from the Colorado Rocky Mountains that contains more than 2 million flower counts, we reveal a diversity of species-level phenological shifts that bring into question the accuracy of previous estimates of long-term phenological change. For 60 species, we show that first, peak, and last flowering rarely shift uniformly and instead usually shift independently of one another, resulting in a diversity of phenological changes through time. Shifts in the timing of first flowering on average overestimate the magnitude of shifts in the timing of peak flowering, fail to predict shifts in the timing of last flowering, and underrepresent the number of species changing phenology in this plant community. Ultimately, this diversity of species-level phenological shifts contributes to altered coflowering patterns within the community, a redistribution of floral abundance across the season, and an expansion of the flowering season by more than I mo during the course of our study period. These results demonstrate the substantial reshaping of ecological communities that can be attributed to shifts in phenology.

Asynchronous changes in phenology of migrating Broad‐tailed Hummingbirds and their early‐season nectar resources

Phenological advancements driven by climate change are especially pronounced at higher latitudes, so that migrants from lower latitudes may increasingly arrive at breeding grounds after the appearance of seasonal resources. To explore this possibility, we compared dates of first arrival of Broad-tailed Hummingbirds (Selasphorus platycercus) to dates of flowering of plants they visit for nectar. Near the southern limit of the breeding range, neither hummingbird arrival nor first flowering dates have changed significantly over the past few decades. At a nearby migration stopover site, first flowering of a major food plant has advanced, but peak flowering has not. Near the northern limit of the breeding range, first and peak flowering of early-season food plants have shifted to earlier dates, resulting in a shorter interval between appearance of first hummingbirds and first flowers. If phenological shifts continue at current rates, hummingbirds will eventually arrive at northern breeding grounds after flowering begins, which could reduce their nesting success. These results support the prediction that migratory species may experience the greatest phenological mismatches at the poleward limits of their migration. A novel hypothesis based on these results posits that the poleward limit for some species may contract toward lower latitudes under continued warming.

Phenological overlap of interacting species in a changing climate: an assessment of available approaches.

Concern regarding the biological effects of climate change has led to a recent surge in research to understand the consequences of phenological change for species interactions. This rapidly expanding research program is centered on three lines of inquiry: (1) how the phenological overlap of interacting species is changing, (2) why the phenological overlap of interacting species is changing, and (3) how the phenological overlap of interacting species will change under future climate scenarios. We synthesize the widely disparate approaches currently being used to investigate these questions: (1) interpretation of long-term phenological data, (2) field observations, (3) experimental manipulations, (4) simulations and nonmechanistic models, and (5) mechanistic models. We present a conceptual framework for selecting approaches that are best matched to the question of interest. We weigh the merits and limitations of each approach, survey the recent literature from diverse systems to quantify their use, and characterize the types of interactions being studied by each of them. We highlight the value of combining approaches and the importance of long-term data for establishing a baseline of phenological synchrony. Future work that scales up from pairwise species interactions to communities and ecosystems, emphasizing the use of predictive approaches, will be particularly valuable for reaching a broader understanding of the complex effects of climate change on the phenological overlap of interacting species. It will also be important to study a broader range of interactions: to date, most of the research on climate-induced phenological shifts has focused on terrestrial pairwise resource–consumer interactions, especially those between plants and insects.

Phenological responses to climate change do not exhibit phylogenetic signal in a subalpine plant community

Phylogenetic relationships may underlie species-specific phenological sensitivities to abiotic variation and may help to predict these responses to climate change. Although shared evolutionary history may mediate both phenology and phenological sensitivity to abiotic variation, few studies have explicitly investigated whether this is the case. We explore phylogenetic signal in flowering phenology and in phenological sensitivity to temperature and snowmelt using a 39-year record of flowering from the Colorado Rocky Mountains, USA that includes dates of first, peak, and last flowering, and flowering duration for 60 plant species in a subalpine plant community. Consistent with other studies, we found evidence in support of phylogenetic signal in first flowering date. However, the strength and significance of that signal were inconsistent across other measures of flowering in this plant community: peak flowering date exhibited the strongest phylogenetic signal, followed by first flowering date; last flowering date and duration of flowering exhibited patterns indistinguishable from random trait evolution. In contrast to first and peak flowering date, phenological sensitivities of all flowering measures to temperature and snowmelt did not exhibit a phylogenetic signal. These findings show that within ecological communities, phylogenetic signal in phenology does not necessarily imply phylogenetic signal in phenological sensitivities to abiotic variation.

Frost sensitivity of leaves and flowers of subalpine plants is related to tissue type and phenology

Summary Harsh abiotic conditions – such as low temperatures that lead to spring and summer frost events in high-elevation and high-latitude ecosystems – can have strong negative consequences for plant growth, survival and reproduction. Despite the predicted increase in episodic frost events under continued climate change in some ecosystems, our general understanding of the factors associated with frost sensitivity of reproductive and vegetative plant structures in natural plant communities is limited. The timing of growth and reproduction may be an important strategy by which plants can avoid frost. In this study, we experimentally investigated the frost sensitivity of eight long-lived perennial herbaceous plant species from a subalpine ecosystem in the Colorado Rocky Mountains, USA. The study taxa represent four congeneric pairs from four flowering plant families; within each pair, there is a species with early and late growth and reproductive phenology. Thus, we control for evolutionary history – and therefore additional traits shared through common ancestry – to some degree, while examining the influence of phenology on frost sensitivity. Specifically, we compared frost sensitivity of vegetative and reproductive structures for each species and asked whether frost sensitivity was similar between species within congeneric pairs or, instead, was related to phenology (i.e. differences in the timing of growth and reproduction). For most species (6 of 8), flowers were more sensitive to frost than leaves. Within most congeneric pairs (3 of 4), the leaves of species with later phenology were significantly more sensitive to frost than the leaves of species with earlier phenology. For flowers, the later flowering species were more sensitive in two of the four congeneric pairs. Synthesis. This study contributes to our general understanding of factors related to interspecific differences in plant sensitivity to episodic frost events of naturally occurring species. The increased frost sensitivity of reproductive structures compared to vegetative structures may be a widespread pattern for long-lived perennial plants. Furthermore, we find evidence for a trade-off between phenology and frost sensitivity, whereby species with later phenology exhibit higher frost sensitivity compared to species with earlier phenology. These results have implications for plant populations, species interactions and ecological communities.

Reproductive assurance for a rewardless epiphytic orchid in Puerto Rico: Pleurothallis ruscifolia (Orchidaceae, Pleurothallidinae)

Abstract Most angiosperms sustain pollinator visits by offering a reward, such as nectar or pollen, yet there are plants that do not offer rewards and instead depend on deception for successful pollen transfer. Unless rewardless plants have an extremely efficient means of deceit or are autogamous, they tend to experience less fruit set than those that offer pollinator rewards. In Puerto Rico, we studied the reproductive biology of a rewardless epiphytic orchid, Pleurothallis ruscifolia (Pleurothallidinae), a widespread Neotropical species. The Pleurothallidinae are primarily myophilous, self-incompatible, and pollinator dependent for fruit set and seed production. However, because our preliminary observations indicated that populations of P. ruscifolia on the island of Puerto Rico exhibited an unusually high fruit set, we hypothesized that our population is autogamous and that reproductive effort and fruiting success are resource limited. We monitored 168 plants in a single population during the 2009 reproductive season to determine the mating system of P. ruscifolia while looking for evidence of reproductive constraints. Fruit set in our population was high (66%) and no floral visitors were seen. Fruit set for our pollinator exclusion experiment was no different than fruit set for open pollinated plants. Most plants produced both chasmogamous and cleistogamous flowers, the majority of fruits produced by the latter. Furthermore, reproductive effort and fruiting success were limited by plant size, which is likely the result of resource constraints. We expect that autogamy is prevalent in P. ruscifolia of the West Indies, but outcrossing should be dominant in continental populations. Selection for reproductive assurance in the absence or rarity of an effective pollinator is the likely process leading to this autogamous system.

Atypical Flowers Can Be as Profitable as Typical Hummingbird Flowers

In western North America, hummingbirds can be observed systematically visiting flowers that lack the typical reddish color, tubular morphology, and dilute nectar of “hummingbird flowers.” Curious about this behavior, we asked whether these atypical flowers are energetically profitable for hummingbirds. Our field measurements of nectar content and hummingbird foraging speeds, taken over four decades at multiple localities, show that atypical flowers can be as profitable as typical ones and suggest that the profit can support 24-h metabolic requirements of the birds. Thus, atypical flowers may contribute to successful migration of hummingbirds, enhance their population densities, and allow them to occupy areas seemingly depauperate in suitable resources. These results illustrate what can be gained by attending to the unexpected.