Floral trait variation across individual plants within a population enhances defense capability to nectar robbing.

Floral trait variation may help pollinators and nectar robbers identify their target plants and, thus, lead to differential selection pressure for defense capability against floral antagonists. However, the effect of floral trait variation among individuals within a population on multi-dimensional plant-animal interactions has been little explored. We investigated floral trait variation, pollination, and nectar robbing among individual plants in a population of the bumble bee-pollinated plant, Caryopteris divaricata, from which flowers are also robbed by bumble bees with varying intensity across individuals. We measured the variation in corolla tube length, nectar volume and sugar concentration among individual plants, and evaluated whether the variation were recognized by pollinators and robbers. We investigated the influence of nectar robbing on legitimate visitation and seed production per fruit. We found that the primary nectar robber (Bombus nobilis) preferred to forage on plants with long-tubed flowers, which produced less nectar and had lower sugar concentration compared to those with shorter corolla tubes. Individuals with shorter corolla tubes had comparatively lower nectar robbing intensity but higher visitation by legitimate visitors (mainly B. picipes) and higher seed production. Nectar robbing significantly reduced seed production because it decreased pollinator visits. However, neither pollination nor seed production differed between plants with long and short corolla tubes when nectar robbers were excluded. This finding suggests that floral trait variation might not be driven by pollinators. Such variation among individual plants thus allows legitimate visitors and nectar robbers to segregate niches and enhances population defense against nectar robbing in unpredictable conditions.

Extensive regional variation in the phenology of insects and their response to temperature across North America.

Climate change models often assume similar responses to temperatures across the range of a species, but local adaptation or phenotypic plasticity can lead plants and animals to respond differently to temperature in different parts of their range. To date, there have been few tests of this assumption at the scale of continents, so it is unclear if this is a large-scale problem. Here, we examined the assumption that insect taxa show similar responses to temperature at 96 sites in grassy habitats across North America. We sampled insects with Malaise traps during 2019-2021 (N = 1041 samples) and examined the biomass of insects in relation to temperature and time of season. Our samples mostly contained Diptera (33%), Lepidoptera (19%), Hymenoptera (18%), and Coleoptera (10%). We found strong regional differences in the phenology of insects and their response to temperature, even within the same taxonomic group, habitat type, and time of season. For example, the biomass of nematoceran flies increased across the season in the central part of the continent, but it only showed a small increase in the Northeast and a seasonal decline in the Southeast and West. At a smaller scale, insect biomass at different traps operating on the same days was correlated up to ~75 km apart. Large-scale geographic and phenological variation in insect biomass and abundance has not been studied well, and it is a major source of controversy in previous analyses of insect declines that have aggregated studies from different locations and time periods. Our study illustrates that large-scale predictions about changes in insect populations, and their causes, will need to incorporate regional and taxonomic differences in the response to temperature.

Current and lagged climate affects phenology across diverse taxonomic groups.

The timing of life events (phenology) can be influenced by climate. Studies from around the world tell us that climate cues and species' responses can vary greatly. If variation in climate effects on phenology is strong within a single ecosystem, climate change could lead to ecological disruption, but detailed data from diverse taxa within a single ecosystem are rare. We collated first sighting and median activity within a high-elevation environment for plants, insects, birds, mammals and an amphibian across 45 years (1975-2020). We related 10 812 phenological events to climate data to determine the relative importance of climate effects on species' phenologies. We demonstrate significant variation in climate-phenology linkage across taxa in a single ecosystem. Both current and prior climate predicted changes in phenology. Taxa responded to some cues similarly, such as snowmelt date and spring temperatures; other cues affected phenology differently. For example, prior summer precipitation had no effect on most plants, delayed first activity of some insects, but advanced activity of the amphibian, some mammals, and birds. Comparing phenological responses of taxa at a single location, we find that important cues often differ among taxa, suggesting that changes to climate may disrupt synchrony of timing among taxa.

Skewness in bee and flower phenological distributions.

Phenological distributions are characterized by their central tendency, breadth, and shape, and all three determine the extent to which interacting species overlap in time. Pollination mutualisms rely on temporal co-occurrence of pollinators and their floral resources, and although much work has been done to characterize the shapes of flower phenological distributions, similar studies that include pollinators are lacking. Here, we provide the first broad assessment of skewness, a component of distribution shape, for a bee community. We compare skewness in bees to that in flowers, relate bee and flower skewness to other properties of their phenology, and quantify the potential consequences of differences in skewness between bees and flowers. Both bee and flower phenologies tend to be right-skewed, with a more exaggerated asymmetry in bees. Early-season species tend to be the most skewed, and this relationship is also stronger in bees than in flowers. Based on a simulation experiment, differences in bee and flower skewness could account for up to 14% of pairwise overlap differences. Given the potential for interaction loss, we argue that difference in skewness of interacting species is an underappreciated property of phenological change.

Life-history traits predict responses of wild bees to climate variation.

Life-history traits, which are physical traits or behaviours that affect growth, survivorship and reproduction, could play an important role in how well organisms respond to environmental change. By looking for trait-based responses within groups, we can gain a mechanistic understanding of why environmental change might favour or penalize certain species over others. We monitored the abundance of at least 154 bee species for 8 consecutive years in a subalpine region of the Rocky Mountains to ask whether bees respond differently to changes in abiotic conditions based on their life-history traits. We found that comb-building cavity nesters and larger bodied bees declined in relative abundance with increasing temperatures, while smaller, soil-nesting bees increased. Further, bees with narrower diet breadths increased in relative abundance with decreased rainfall. Finally, reduced snowpack was associated with reduced relative abundance of bees that overwintered as prepupae whereas bees that overwintered as adults increased in relative abundance, suggesting that overwintering conditions might affect body size, lipid content and overwintering survival. Taken together, our results show how climate change may reshape bee pollinator communities, with bees with certain traits increasing in abundance and others declining, potentially leading to novel plant-pollinator interactions and changes in plant reproduction.

Lagged and dormant season climate better predict plant vital rates than climate during the growing season.

Understanding the effects of climate on the vital rates (e.g., survival, development, reproduction) and dynamics of natural populations is a long-standing quest in ecology, with ever-increasing relevance in the face of climate change. However, linking climate drivers to demographic processes requires identifying the appropriate time windows during which climate influences vital rates. Researchers often do not have access to the long-term data required to test a large number of windows, and are thus forced to make a priori choices. In this study, we first synthesize the literature to assess current a priori choices employed in studies performed on 104 plant species that link climate drivers with demographic responses. Second, we use a sliding-window approach to investigate which combination of climate drivers and temporal window have the best predictive ability for vital rates of four perennial plant species that each have over a decade of demographic data (Helianthella quinquenervis, Frasera speciosa, Cylindriopuntia imbricata, and Cryptantha flava). Our literature review shows that most studies consider time windows in only the year preceding the measurement of the vital rate(s) of interest, and focus on annual or growing season temporal scales. In contrast, our sliding-window analysis shows that in only four out of 13 vital rates the selected climate drivers have time windows that align with, or are similar to, the growing season. For many vital rates, the best window lagged more than 1 year and up to 4 years before the measurement of the vital rate. Our results demonstrate that for the vital rates of these four species, climate drivers that are lagged or outside of the growing season are the norm. Our study suggests that considering climatic predictors that fall outside of the most recent growing season will improve our understanding of how climate affects population dynamics.

Bee phenology is predicted by climatic variation and functional traits.

Climate change is shifting the environmental cues that determine the phenology of interacting species. Plant-pollinator systems may be susceptible to temporal mismatch if bees and flowering plants differ in their phenological responses to warming temperatures. While the cues that trigger flowering are well-understood, little is known about what determines bee phenology. Using generalised additive models, we analyzed time-series data representing 67 bee species collected over 9 years in the Colorado Rocky Mountains to perform the first community-wide quantification of the drivers of bee phenology. Bee emergence was sensitive to climatic variation, advancing with earlier snowmelt timing, whereas later phenophases were best explained by functional traits including overwintering stage and nest location. Comparison of these findings to a long-term flower study showed that bee phenology is less sensitive than flower phenology to climatic variation, indicating potential for reduced synchrony of flowers and pollinators under climate change.

Wild hummingbirds discriminate nonspectral colors.

Many animals have the potential to discriminate nonspectral colors. For humans, purple is the clearest example of a nonspectral color. It is perceived when two color cone types in the retina (blue and red) with nonadjacent spectral sensitivity curves are predominantly stimulated. Purple is considered nonspectral because no monochromatic light (such as from a rainbow) can evoke this simultaneous stimulation. Except in primates and bees, few behavioral experiments have directly examined nonspectral color discrimination, and little is known about nonspectral color perception in animals with more than three types of color photoreceptors. Birds have four color cone types (compared to three in humans) and might perceive additional nonspectral colors such as UV+red and UV+green. Can birds discriminate nonspectral colors, and are these colors behaviorally and ecologically relevant? Here, using comprehensive behavioral experiments, we show that wild hummingbirds can discriminate a variety of nonspectral colors. We also show that hummingbirds, relative to humans, likely perceive a greater proportion of natural colors as nonspectral. Our analysis of plumage and plant spectra reveals many colors that would be perceived as nonspectral by birds but not by humans: Birds' extra cone type allows them not just to see UV light but also to discriminate additional nonspectral colors. Our results support the idea that birds can distinguish colors throughout tetrachromatic color space and indicate that nonspectral color perception is vital for signaling and foraging. Since tetrachromacy appears to have evolved early in vertebrates, this capacity for rich nonspectral color perception is likely widespread.

Effects of climate change on alpine plants and their pollinators.

Alpine environments are among the habitats most strongly affected by climate change, and consequently their unique plants and pollinators are faced with the challenge of adapting or going extinct. Changes in temperature and precipitation affect snowpack and snowmelt, resulting in changes in the growing season in this environment where plant growth and pollinator activity are constrained to the snow-free season, which can vary significantly across the landscape if there is significant topographic complexity. As in other ecosystems, the resulting changes in phenology are not uniform among species, creating the potential for altered and new interspecific interactions. New plant and animal species are arriving as lower altitude species move up with warming temperatures, introducing new competitors and generating changes in plant-pollinator interactions. Repeating historical surveys, taking advantage of museum collections, and using new technology will facilitate our understanding of how plants and pollinators are responding to the changing alpine environment.

Global agricultural productivity is threatened by increasing pollinator dependence without a parallel increase in crop diversification.

The global increase in the proportion of land cultivated with pollinator-dependent crops implies increased reliance on pollination services. Yet agricultural practices themselves can profoundly affect pollinator supply and pollination. Extensive monocultures are associated with a limited pollinator supply and reduced pollination, whereas agricultural diversification can enhance both. Therefore, areas where agricultural diversity has increased, or at least been maintained, may better sustain high and more stable productivity of pollinator-dependent crops. Given that >80% of all crops depend, to varying extents, on insect pollination, a global increase in agricultural pollinator dependence over recent decades might have led to a concomitant increase in agricultural diversification. We evaluated whether an increase in the area of pollinator-dependent crops has indeed been associated with an increase in agricultural diversity, measured here as crop diversity, at the global, regional, and country scales for the period 1961-2016. Globally, results show a relatively weak and decelerating rise in agricultural diversity over time that was largely decoupled from the strong and continually increasing trend in agricultural dependency on pollinators. At regional and country levels, there was no consistent relationship between temporal changes in pollinator dependence and crop diversification. Instead, our results show heterogeneous responses in which increasing pollinator dependence for some countries and regions has been associated with either an increase or a decrease in agricultural diversity. Particularly worrisome is a rapid expansion of pollinator-dependent oilseed crops in several countries of the Americas and Asia that has resulted in a decrease in agricultural diversity. In these regions, reliance on pollinators is increasing, yet agricultural practices that undermine pollination services are expanding. Our analysis has thereby identified world regions of particular concern where environmentally damaging practices associated with large-scale, industrial agriculture threaten key ecosystem services that underlie productivity, in addition to other benefits provided by biodiversity.

Author Correction: A statistical estimator for determining the limits of contemporary and historic phenology.

In the version of this Article originally published, the rate of change plotted in Figure 2 was incorrect because of a coding error. The corrected figure is shown below. In the original Figure 2 legend, the onset of flowering slope was given as '0.99, 95% CI: 0.90-1.08', the cessation of flowering slope was given as '1.02, 95% CI: 0.91-1.13', and the r2adjusted for each model was given as greater than 74%'. The correct values are '1.04, 95% CI: 0.97-1.12', '1.25, 95% CI: 0.87-1.62', and '60%', respectively. The main text and the conclusion that the slopes of these relationships are statistically indistinguishable from 1.00 are unchanged. These errors have now been corrected in the PDF and HTML versions of the article. The authors are grateful to A. Iler, who drew attention to this issue.

Phenological responses to multiple environmental drivers under climate change: insights from a long-term observational study and a manipulative field experiment.

Climate change has induced pronounced shifts in the reproductive phenology of plants, yet we know little about which environmental factors contribute to interspecific variation in responses and their effects on fitness. We integrate data from a 43 yr record of first flowering for six species in subalpine Colorado meadows with a 3 yr snow manipulation experiment on the perennial forb Boechera stricta (Brassicaceae) from the same site. We analyze shifts in the onset of flowering in relation to environmental drivers known to influence phenology: the timing of snowmelt, the accumulation of growing degree days, and photoperiod. Variation in responses to climate change depended on the sequence in which species flowered, with early-flowering species reproducing faster, at a lower heat sum, and under increasingly disparate photoperiods relative to later-flowering species. Early snow-removal treatments confirm that the timing of snowmelt governs observed trends in flowering phenology of B. stricta and that climate change can reduce the probability of flowering, thereby depressing fitness. Our findings suggest that climate change is decoupling historical combinations of photoperiod and temperature and outpacing phenological changes for our focal species. Accurate predictions of biological responses to climate change require a thorough understanding of the factors driving shifts in phenology.

Direct and indirect effects of episodic frost on plant growth and reproduction in subalpine wildflowers.

Frost is an important episodic event that damages plant tissues through the formation of ice crystals at or below freezing temperatures. In montane regions, where climate change is expected to cause earlier snow melt but may not change the last frost-free day of the year, plants that bud earlier might be directly impacted by frost through damage to flower buds and reproductive structures. However, the indirect effects of frost mediated through changes in plant-pollinator interactions have rarely been explored. We examined the direct and pollinator-mediated indirect effects of frost on three wildflower species in southwestern Colorado, USA, Delphinium barbeyi (Ranunculaceae), Erigeron speciosus (Asteraceae), and Polemonium foliosissimum (Polemoniaceae), by simulating moderate (-1 to -5°C) frost events in early spring in plants in situ. Subsequently, we measured plant growth, and upon flowering measured flower morphology and phenology. Throughout the flowering season, we monitored pollinator visitation and collected seeds to measure plant reproduction. We found that frost had species-specific direct and indirect effects. Frost had direct effects on two of the three species. Frost significantly reduced flower size, total flowers produced, and seed production of Erigeron. Furthermore, frost reduced aboveground plant survival and seed production for Polemonium. However, we found no direct effects of frost on Delphinium. When we considered the indirect impacts of frost mediated through changes in pollinator visitation, one species, Erigeron, incurred indirect, negative effects of frost on plant reproduction through changes in floral traits and pollinator visitation, along with direct effects. Overall, we found that flowering plants exhibited species-specific direct and pollinator-mediated indirect responses to frost, thus suggesting that frost may play an important role in affecting plant communities under climate change.

Interannual bumble bee abundance is driven by indirect climate effects on floral resource phenology.

Climate change can influence consumer populations both directly, by affecting survival and reproduction, and indirectly, by altering resources. However, little is known about the relative importance of direct and indirect effects, particularly for species important to ecosystem functioning, like pollinators. We used structural equation modelling to test the importance of direct and indirect (via floral resources) climate effects on the interannual abundance of three subalpine bumble bee species. In addition, we used long-term data to examine how climate and floral resources have changed over time. Over 8 years, bee abundances were driven primarily by the indirect effects of climate on the temporal distribution of floral resources. Over 43 years, aspects of floral phenology changed in ways that indicate species-specific effects on bees. Our study suggests that climate-driven alterations in floral resource phenology can play a critical role in governing bee population responses to global change.

A statistical estimator for determining the limits of contemporary and historic phenology.

Climate change affects not just where species are found, but also when species' key life-history events occur-their phenology. Measuring such changes in timing is often hampered by a reliance on biased survey data: surveys identify that an event has taken place (for example, the flower is in bloom), but not when that event happened (for example, the flower bloomed yesterday). Here, we show that this problem can be circumvented using statistical estimators, which can provide accurate and unbiased estimates from sparsely sampled observations. We demonstrate that such methods can resolve an ongoing debate about the relative timings of the onset and cessation of flowering, and allow us to place modern observations reliably within the context of the vast wealth of historical data that reside in herbaria, museum collections, and written records. We also analyse large-scale citizen science data from the United States National Phenology Network and reveal not just earlier but also potentially more variable flowering in recent years. Evidence for greater variability through time is important because increases in variation are characteristic of systems approaching a state change.

Multitrophic interactions mediate the effects of climate change on herbivore abundance.

Climate change can influence the abundance of insect herbivores through direct and indirect mechanisms. In this study, we evaluated multitrophic drivers of herbivore abundance for an aphid species (Aphis helianthi) in a subalpine food web consisting of a host plant (Ligusticum porteri), mutualist ants and predatory lygus bugs (Lygus spp.). We used a model-selection approach to determine which climate and host plant cues best predict year-to-year variation in insect phenology and abundance observed over 6 years. We complemented this observational study with experiments that determined how elevated temperature interacts with (1) host plant phenology and (2) the ant-aphid mutualism to determine aphid abundance. We found date of snowmelt to be the best predictor of yearly abundance of aphid and lygus bug abundance but the direction of this effect differed. Aphids achieved lower abundances in early snowmelt years likely due to increased abundance of lygus bug predators in these years. Elevating temperature of L. porteri flowering stalks reduced their quality as hosts for aphid populations. However, warming aphid colonies on host plants of similar quality increased population growth rates. Importantly, this effect was apparent even in the absence of ants. While we observed fewer ants tending colonies at elevated temperatures, these colonies also had reduced numbers of lygus bug predators. This suggests that mutualism with ants becomes less significant as temperature increases, which contrasts other ant-hemipteran systems. Our observational and experimental results show the importance of multitrophic species interactions for predicting the effect of climate change on the abundances of herbivores.

Nectar replenishment maintains the neutral effects of nectar robbing on female reproductive success of Salvia przewalskii (Lamiaceae), a plant pollinated and robbed by bumble bees.

Background and Aims: It has been suggested that the dynamics of nectar replenishment could differ for flowers after being nectar robbed or visited legitimately, but further experimental work is needed to investigate this hypothesis. This study aimed to assess the role of nectar replenishment in mediating the effects of nectar robbing on pollinator behaviour and plant reproduction. Methods: Plant-robber-pollinator interactions in an alpine plant, Salvia przewalskii , were studied. It is pollinated by long-tongued Bombus religiosus and short-tongued B. friseanus , but robbed by B. friseanus . Nectar production rates for flowers after they were either robbed or legitimately visited were compared, and three levels of nectar robbing were created to detect the effects of nectar robbing on pollinator behaviour and plant reproduction. Key Results: Nectar replenishment did not differ between flowers that had been robbed or legitimately visited. Neither fruit set nor seed set was significantly affected by nectar robbing. In addition, nectar robbing did not significantly affect visitation rate, flowers visited within a plant per foraging bout, or flower handling time of the legitimate pollinators. However, a tendency for a decrease in relative abundance of the pollinator B. religiosus with an increase of nectar robbing was found. Conclusions: Nectar robbing did not affect female reproductive success because nectar replenishment ensures that pollinators maintain their visiting activity to nectar-robbed flowers. Nectar replenishment might be a defence mechanism against nectar robbing to enhance reproductive fitness by maintaining attractiveness to pollinators. Further studies are needed to reveal the potential for interference competition among bumble bees foraging as robbers and legitimate visitors, and to investigate variation of nectar robbing in communities with different bumble bee species composition.

Detrending phenological time series improves climate-phenology analyses and reveals evidence of plasticity.

Time series have played a critical role in documenting how phenology responds to climate change. However, regressing phenological responses against climatic predictors involves the risk of finding potentially spurious climate-phenology relationships simply because both variables also change across years. Detrending by year is a way to address this issue. Additionally, detrending isolates interannual variation in phenology and climate, so that detrended climate-phenology relationships can represent statistical evidence of phenotypic plasticity. Using two flowering phenology time series from Colorado, USA and Greenland, we detrend flowering date and two climate predictors known to be important in these ecosystems: temperature and snowmelt date. In Colorado, all climate-phenology relationships persist after detrending. In Greenland, 75% of the temperature-phenology relationships disappear after detrending (three of four species). At both sites, the relationships that persist after detrending suggest that plasticity is a major component of sensitivity of flowering phenology to climate. Finally, simulations that created different strengths of correlations among year, climate, and phenology provide broader support for our two empirical case studies. This study highlights the utility of detrending to determine whether phenology is related to a climate variable in observational data sets. Applying this as a best practice will increase our understanding of phenological responses to climatic variation and change.