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.

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.

Natal-habitat experience mediates the relationship between insect and hostplant densities.

For some animals, the habitat which they first experience can influence the type of habitat which they select later in life and, thus, potentially their population distribution and dynamics. However, for many insect herbivores, whose natal habitat may consist of a single hostplant, the consequences of natal hostplant experience remain untested in landscapes relevant to the adult, which may select not only among plants, but among plant patches. As a first step towards understanding how natal hostplant experience shapes patterns of insect feeding damage in landscapes relevant to adults, we conducted partially caged field experiments with diamondback moths that were reared on either mustard or collard plants and then allowed to choose among and within patches of plants that varied in plant density and composition. We predicted that natal hostplant experience would interact with patch size and composition to influence the number of diamondback moth offspring and feeding damage per plant. As predicted, when moths were reared on collards, we found more offspring on and damage to collard plants in four-collard patches than in two-collard patches (i.e., resource concentration), but no difference when moths were reared on mustards. Contrary to predictions, we found no difference in the number of offspring on or damage to mixed plant patches compared with two- or four-collard plant patches regardless of natal hostplant type. Our research suggests that prior hostplant experience has complex consequences for how insects and their feeding damage are distributed in patchy environments and highlights the need for future research in this area.

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.

Increased consumer density reduces the strength of neighborhood effects in a model system.

An individual's susceptibility to attack can be influenced by conspecific and heterospecifics neighbors. Predicting how these neighborhood effects contribute to population-level processes such as competition and evolution requires an understanding of how the strength of neighborhood effects is modified by changes in the abundances of both consumers and neighboring resource species. We show for the first time that consumer density can interact with the density and frequency of neighboring organisms to determine the magnitude of neighborhood effects. We used the bean beetle, Callosobruchus maculatus, and two of its host beans, Vigna unguiculata and V. radiata, to perform a response-surface experiment with a range of resource densities and three consumer densities. At low beetle density, damage to beans was reduced with increasing conspecific density (i.e., resource dilution) and damage to the less preferred host, V. unguiculata, was reduced with increasing V. radiata frequency (i.e., frequency-dependent associational resistance). As beetle density increased, however, neighborhood effects were reduced; at the highest beetle densities neither focal nor neighboring resource density nor frequency influenced damage. These findings illustrate the importance of consumer density in mediating indirect effects among resources, and suggest that accounting for consumer density may improve our ability to predict population-level outcomes of neighborhood effects and our use of them in applications such as mixed-crop pest management.

Time since disturbance affects colonization dynamics in a metapopulation.

Disturbances are widespread in nature and can have substantial population-level consequences. Most empirical studies on the effects of disturbance track population recovery within habitat patches, but have an incomplete representation of the recolonization process. In addition, recent metapopulation models represent post-disturbance colonization with a recovery state or time-lag for disturbed ("focal") patches, thus assuming that recolonization rates are uniform. However, the availability of colonists in neighbouring "source" patches can vary, especially in frequently disturbed landscapes such as fire-managed forests that have a mosaic of patches that differ in successional state and undergo frequent local extinctions. To determine how time since disturbance in both focal and neighbouring source patches might affect metapopulations, we studied the effects of time since fire (TSF) on abundances of a specialist palmetto beetle within and between fire management units in Apalachicola National Forest, Florida. We measured beetle abundances at three distances from the shared edge of paired units, with units ranging from 0 to 64 months since fire and the difference in time since burning for a focal-source pair ranging from 3 to 58 months. Soon after fire, beetle abundances within management units were highest near the unit edge, but this pattern changed with increasing TSF. Between paired units, the more recently disturbed ("focal") unit's beetle abundance was positively related to source unit abundance, but the shape of this relationship differed based on focal unit TSF and the units' difference in time since burning. Results suggest that both focal and source habitat history can influence recolonization of recently disturbed patches and that these effects may persist over years. Thus, when predicting metapopulation dynamics, variation in habitat characteristics should be considered not only for patches receiving colonists but for patches supplying colonists as well.

Fractionation-dependent improvements in proteome resolution in the mouse hippocampus by IEF LC-MS/MS.

An assessment of fractionated mouse hippocampal peptides was conducted. Protein extract from a single mouse hippocampus was enzymatically digested and fractionated by IEF. Aliquots of fractions were pooled into fewer, more complex samples. The unfractionated lysate, fractions, and pooled fractions were subjected to LC-MS/MS analysis. Samples consisting of many individual fractions had more protein identifications, greater protein sequence coverage, and quantified proteins with more spectral counts than protein extract that was unfractionated or pooled into fewer LC-MS/MS samples. Additionally, prefractionation reduced the median CV for spectral counts as much as 33%. However, the relative gain in proteome resolution was found to saturate with increasing fractionation extent. This study demonstrates how prefractionation by offline IEF can improve the resolution of proteomic investigations of the mouse hippocampus, and that a data-driven pooling methodology can reduce excessive and cost-ineffective fractionation.

Bears benefit plants via a cascade with both antagonistic and mutualistic interactions.

Predators can influence primary producers by generating cascades of effects in ecological webs. These effects are often non-intuitive, going undetected because they involve many links and different types of species interactions. Particularly, little is understood about how antagonistic (negative) and mutualistic (positive) interactions combine to create cascades. Here, we show that black bears can benefit plants by consuming ants. The ants are mutualists of herbivores and protect herbivores from other arthropod predators. We found that plants near bear-damaged ant nests had greater reproduction than those near undamaged nests, due to weaker ant protection for herbivores, which allowed herbivore suppression by arthropod predators. Our results highlight the need to integrate mutualisms into trophic cascade theory, which is based primarily on antagonistic relationships. Predators are often conservation targets, and our results suggest that bears and other predators should be managed with the understanding that they can influence primary producers through many paths.

Nonrandom community assembly and high temporal turnover promote regional coexistence in tropics but not temperate zone.

A persistent challenge for ecologists is understanding the ecological mechanisms that maintain global patterns of biodiversity, particularly the latitudinal diversity gradient of peak species richness in the tropics. Spatial and temporal variation in community composition contribute to these patterns of biodiversity, but how this variation and its underlying processes change across latitude remains unresolved. Using a model system of sessile marine invertebrates across 25 degrees of latitude, from the temperate zone to the tropics, we tested the prediction that spatial and temporal patterns of taxonomic richness and composition, and the community assembly processes underlying these patterns, will differ across latitude. Specifically, we predicted that high beta diversity (spatial variation in composition) and high temporal turnover contribute to the high species richness of the tropics. Using a standardized experimental approach that controls for several confounding factors that hinder interpretation of prior studies, we present results that support our predictions. In the temperate zone, communities were more similar across spatial scales from centimeters to tens of kilometers and temporal scales up to one year than at lower latitudes. Since the patterns at northern latitudes were congruent with a null model, stochastic assembly processes are implicated. In contrast, the communities in the tropics were a dynamic spatial and temporal mosaic, with low similarity even across small spatial scales and high temporal turnover at both local and regional scales. Unlike the temperate zone, deterministic community assembly processes such as predation likely contributed to the high beta diversity in the tropics. Our results suggest that community assembly processes and temporal dynamics vary across latitude and help structure and maintain latitudinal patterns of diversity.

Can inducible resistance in plants cause herbivore aggregations? Spatial patterns in an inducible plant/herbivore model.

Many theories regarding the evolution of inducible resistance in plants have an implicit spatial component, but most relevant population dynamic studies ignore spatial dynamics. We examined a spatially explicit model of plant inducible resistance and herbivore population dynamics to explore how realistic features of resistance and herbivore responses influence spatial patterning. Both transient and persistent spatial patterns developed in all models examined, where patterns manifested as wave-like aggregations of herbivores and variation in induction levels. Patterns arose when herbivores moved away from highly induced plants, there was a lag between damage and deployment of induced resistance, and the relationship between herbivore density and strength of the induction response had a sigmoid shape. These mechanisms influenced pattern formation regardless of the assumed functional relationship between resistance and herbivore recruitment and mortality. However, in models where induction affected herbivore mortality, large-scale herbivore population cycles driven by the mortality response often co-occurred with smaller scale spatial patterns driven by herbivore movement. When the mortality effect dominated, however, spatial pattern formation was completely replaced by spatially synchronized herbivore population cycles. Our results present a new type of ecological pattern formation driven by induced trait variation, consumer behavior, and time delays that has broad implications for the community and evolutionary ecology of plant defenses.

Effects of plant neighborhoods on plant-herbivore interactions: resource dilution and associational effects.

Effects of neighboring plants on herbivore damage to a focal plant (associational effects) have been documented in many systems and can lead to either increased or decreased herbivore attack. Mechanistic models that explain the observed variety of herbivore responses to local plant community composition have, however, been lacking. We present a model of herbivore responses to patches that consist of two plant types, where herbivore densities on a focal plant are determined by a combination of patch-finding, within-patch redistribution, and patch-leaving. Our analyses show that the effect of plant neighborhood on herbivores depends both on how plant and herbivore traits combine to affect herbivore movement and on how experimental designs reveal the effects of plant density and plant relative frequency. Associational susceptibility should be the dominant pattern when herbivores have biased landing rates within patches. Other behavioral decision rules lead to mixed responses, but a common pattern is that in mixed patches, one plant type experiences associational resistance while the other plant experiences associational susceptibility. In some cases, the associational effect may shift sign along a gradient of plant frequency, suggesting that future empirical studies should include more than two plant frequencies to detect nonlinearities. Finally, we find that associational susceptibility should be commonly observed in experiments using replacement designs, whereas associational resistance will be the dominant pattern when using additive designs. Consequently, outcomes from one experimental design cannot be directly compared to studies with other designs. Our model can also be translated to other systems with foragers searching for multiple resource types.

Sex and stochasticity affect range expansion of experimental invasions.

Understanding and predicting range expansion are key objectives in many basic and applied contexts. Among dioecious organisms, there is strong evidence for sex differences in dispersal, which could alter the sex ratio at the expansion's leading edge. However, demographic stochasticity could also affect leading-edge sex ratios, perhaps overwhelming sex-biased dispersal. We used insects in laboratory mesocosms to test the effects of sex-biased dispersal on range expansion, and a simulation model to explore interactive effects of sex-biased dispersal and demographic stochasticity. Sex-biased dispersal created spatial clines in the sex ratio, which influenced offspring production at the front and altered invasion velocity. Increasing female dispersal relative to males accelerated spread, despite the prediction that demographic stochasticity would weaken a signal of sex-biased dispersal. Our results provide the first experimental evidence for an influence of sex-biased dispersal on invasion velocity, highlighting the value of accounting for sex structure in studies of range expansion.

Habitat loss alters the architecture of plant--pollinator interaction networks.

Habitat loss can have a negative effect on the number, abundance, and composition of species in plant-pollinator communities. Although we have a general understanding of the negative consequences of habitat loss for biodiversity, much less is known about the resulting effects on the pattern of interactions in mutualistic networks. Ecological networks formed by mutualistic interactions often exhibit a highly nested architecture with low modularity, especially in comparison with antagonistic networks. These patterns of interaction are thought to confer stability on mutualistic communities. With the growing threat of environmental change, it is important to expand our understanding of the factors that affect biodiversity and the stability of the communities that provide critical ecosystem functions and services. We studied the effects of habitat loss on plant--pollinator network architecture and found that regional habitat loss contributes directly to species loss and indirectly to the reorganization of interspecific interactions in a local community. Networks became more highly connected and more modular with habitat loss. Species richness and abundance were the primary drivers of variation in network architecture, though species compositi n affected modularity. Theory suggests that an increase in modularity with habitat loss will threaten community stability, which may contribute to an extinction debt in communities already affected by habitat loss.

Insect herbivores change the outcome of plant competition through both inter- and intraspecific processes.

Insect herbivores can affect plant abundance and community composition, and theory suggests that herbivores influence plant communities by altering interspecific interactions among plants. Because the outcome of interspecific interactions is influenced by the per capita competitive ability of plants, density dependence, and intrinsic rates of increase, measuring herbivore effects on all these processes is necessary to understand the mechanisms by which herbivores influence plant communities. We fit alternative competition models to data from a response surface experiment conducted over four years to examine how herbivores affected the outcome of competition between two perennial plants, Solidago altissima and Solanum carolinense. Within a growing season, herbivores reduced S. carolinense plant size but did not affect the size of S. altissima, which exhibited compensatory growth. Across seasons, herbivores did not affect S. carolinense density or biomass but reduced both the density and population growth of S. altissima. The best-fit models indicated that the effects of herbivores varied with year. In some years, herbivores increased the per capita competitive effect of S. altissima on S. carolinense; in other years, herbivores influenced the intrinsic rate of increase of S. altissima. We examined possible herbivore effects on the longer-term outcome of competition (over the time scale of a typical old-field habitat), using simulations based on the best-fit models. In the absence of herbivores, plant coexistence was observed. In the presence of herbivores, S. carolinense was excluded by S. altissima in 72.3% of the simulations. We demonstrate that herbivores can influence the outcome of competition through changes in both per capita competitive effects and intrinsic rates of increase. We discuss the implications of these results for ecological succession and biocontrol.

Climate data from the Rocky Mountain Biological Laboratory (1975-2022).

The Rocky Mountain Biological Laboratory (RMBL; Colorado, USA) is the site for many research projects spanning decades, taxa, and research fields from ecology to evolutionary biology to hydrology and beyond. Climate is the focus of much of this work and provides important context for the rest. There are five major sources of data on climate in the RMBL vicinity, each with unique variables, formats, and temporal coverage. These data sources include (1) RMBL resident billy barr, (2) the National Oceanic and Atmospheric Administration (NOAA), (3) the United States Geological Survey (USGS), (4) the United States Department of Agriculture (USDA), and (5) Oregon State University's PRISM Climate Group. Both the NOAA and the USGS have automated meteorological stations in Crested Butte, CO, ~10 km from the RMBL, while the USDA has an automated meteorological station on Snodgrass Mountain, ~2.5 km from the RMBL. Each of these data sets has unique spatial and temporal coverage and formats. Despite the wealth of work on climate-related questions using data from the RMBL, previous researchers have each had to access and format their own climate records, make decisions about handling missing data, and recreate data summaries. Here we provide a single curated climate data set of daily observations covering the years 1975-2022 that blends information from all five sources and includes annotated scripts documenting decisions for handling data. These synthesized climate data will facilitate future research, reduce duplication of effort, and increase our ability to compare results across studies. The data set includes information on precipitation (water and snow), snowmelt date, temperature, wind speed, soil moisture and temperature, and stream flows, all publicly available from a combination of sources. In addition to the formatted raw data, we provide several new variables that are commonly used in ecological analyses, including growing degree days, growing season length, a cold severity index, hard frost days, an index of El Niño-Southern Oscillation, and aridity (standardized precipitation evapotranspiration index). These new variables are calculated from the daily weather records. As appropriate, data are also presented as minima, maxima, means, residuals, and cumulative measures for various time scales including days, months, seasons, and years. The RMBL is a global research hub. Scientists on site at the RMBL come from many countries and produce about 50 peer-reviewed publications each year. Researchers from around the world also routinely use data from the RMBL for synthetic work, and educators around the United States use data from the RMBL for teaching modules. This curated and combined data set will be useful to a wide audience. Along with the synthesized combined data set we include the raw data and the R code for cleaning the raw data and creating the monthly and yearly data sets, which facilitate adding additional years or data using the same standardized protocols. No copyright or proprietary restrictions are associated with using this data set; please cite this data paper when the data are used in publications or scientific events.

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.

Disorder or a new order: How climate change affects phenological variability.

Advancing spring phenology is a well documented consequence of anthropogenic climate change, but it is not well understood how climate change will affect the variability of phenology year to year. Species' phenological timings reflect the adaptation to a broad suite of abiotic needs (e.g., thermal energy) and biotic interactions (e.g., predation and pollination), and changes in patterns of variability may disrupt those adaptations and interactions. Here, we present a geographically and taxonomically broad analysis of phenological shifts, temperature sensitivity, and changes in interannual variability encompassing nearly 10,000 long-term phenology time series representing more than 1000 species across much of the Northern Hemisphere. We show that the timings of leaf-out, flowering, insect first-occurrence, and bird arrival were the most sensitive to temperature variation and have advanced at the fastest pace for early-season species in colder and less seasonal regions. We did not find evidence for changing variability in warmer years in any phenophase groups, although leaf-out and flower phenology have become moderately but significantly less variable over time. Our findings suggest that climate change has not to this point fundamentally altered the patterns of interannual phenological variability.

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.

The indirect consequences of a mutualism: comparing positive and negative components of the net interaction between honeydew-tending ants and host plants.

1. In ecological webs, net indirect interactions between species are composed of interactions that vary in sign and magnitude. Most studies have focused on negative component interactions (e.g. predation, herbivory) without considering the relative importance of positive interactions (e.g. mutualism, facilitation) for determining net indirect effects. 2. In plant/arthropod communities, ants have multiple top-down effects via mutualisms with honeydew-producing herbivores and harassment of and predation on other herbivores; these ant effects provide opportunities for testing the relative importance of positive and negative interspecific interactions. We manipulated the presence of ants, honeydew-producing membracids and leaf-chewing beetles on perennial host plants in field experiments in Colorado to quantify the relative strength of these different types of interactions and their impact on the ant's net indirect effect on plants. 3. In 2007, we demonstrated that ants simultaneously had a positive effect on membracids and a negative effect on beetles, resulting in less beetle damage on plants hosting the mutualism. 4. In 2008, we used structural equation modelling to describe interaction strengths through the entire insect herbivore community on plants with and without ants. The ant's mutualism with membracids was the sole strong interaction contributing to the net indirect effect of ants on plants. Predation, herbivory and facilitation were weak, and the net effect of ants reduced plant reproduction. This net indirect effect was also partially because of behavioural changes of herbivores in the presence of ants. An additional membracid manipulation showed that the membracid's effect on ant activity was largely responsible for the ant's net effect on plants; ant workers were nearly ten times as abundant on plants with mutualists, and effects on other herbivores were similar to those in the ant manipulation experiment. 5. These results demonstrate that mutualisms can be strong relative to negative direct interspecific interactions and that positive interactions deserve attention as important components of ecological webs.

Trade-offs Among Resilience, Robustness, Stability, and Performance and How We Might Study Them.

Biological systems are likely to be constrained by trade-offs among robustness, resilience, and performance. A better understanding of these trade-offs is important for basic biology, as well as applications where biological systems can be designed for different goals. We focus on redundancy and plasticity as mechanisms governing some types of trade-offs, but mention others as well. Whether trade-offs are due to resource constraints or "design" constraints (i.e., structure of nodes and links within a network) will also affect the types of trade-offs that are important. Identifying common themes across scales of biological organization will require that researchers use similar approaches to quantifying robustness, resilience, and performance, using units that can be compared across systems.