Temporal dynamics influenced by global change: bee community phenology in urban,agricultural, and natural landscapes

Urbanization and agricultural intensification of landscapes are important drivers of global change, which in turn have direct impacts on local ecological communities leading to shifts in species distributions and interactions. Here, we illustrate how human‐altered landscapes, with novel ornamental and crop plant communities, result not only in changes to local community diversity of floral‐dependent species, but also in shifts in seasonal abundance of bee pollinators. Three years of data on the spatio‐temporal distributions of 91 bee species show that seasonal patterns of abundance and species richness in human‐altered landscapes varied significantly less compared to natural habitats in which floral resources are relatively scarce in the dry summer months. These findings demonstrate that anthropogenic environmental changes in urban and agricultural systems, here mediated through changes in plant resources and water inputs, can alter the temporal dynamics of pollinators that depend on them. Changes in phenology of interactions can be an important, though frequently overlooked, mechanism of global change.     

A perspective on match/mismatch of phenology in community contexts

Climate change has significant impacts on phenology of various organisms in a species‐specific manner. Facing this problem, the match/mismatch hypothesis that phenological (a)synchrony with resource availability strongly influences recruitment success of a consumer population has recently received much attention. In this article, we discuss extending the conventional pairwise concept and demonstrate a community module‐based approach as an initial step for exploring community consequences of species‐specific phenological shifts caused by climate change. Our multispecies match/mismatch perspective leads to the prediction that phenological (a)synchrony among interacting species critically affects not only population recruitment of species but also key dynamical features of ecological communities such as trophic cascades, competitive hierarchies, and species coexistence. Explicit identification and consideration of species relationships is therefore desirable for a better understanding of seasonal community dynamics and thus community consequences of climate change‐induced phenological shifts.     

Aggregative structure is the rule in communities of fleas: null model analysis

We used null models to examine patterns of species co‐occurrences in 59 communities of fleas parasitic on small mammals from 4 biogeographic realms (Afrotropics, Nearctic, Neotropics, and Palaearctic). We compared frequencies of co‐occurrences of flea species across host species with those expected by chance, using a null model approach. We used 4 tests for non‐randomness to identify pairs of species (within a community) that demonstrate significant positive or negative co‐occurrence. The majority of flea communities were non‐randomly assembled. Patterns of flea co‐occurrences on the same host species indicated aggregation but not segregation of flea species (except for the flea community of Madagascar). Although only a small fraction of species pairs were associated significantly (264 of 10, 943 species pairs according to the most liberal criterion), most of these associations were positive (except for 2 negatively associated species pairs). Significantly associated pairs were represented mainly by non‐congeneric species. The degree of non‐randomness of the entire flea community was similar among biogeographic regions, but the strength of pair‐wise association varied geographically, being the highest in the Afrotropics and the lowest in the European region of the Palaearctic.     

The role of seasonal timing and phenological shifts for species coexistence

Shifts in the phenologies of coexistence species are altering the temporal structure of natural communities worldwide. However, predicting how these changes affect the structure and long‐term dynamics of natural communities is challenging because phenology and coexistence theory have largely proceeded independently. Here, I propose a conceptual framework that incorporates seasonal timing of species interactions into a well‐studied competition model to examine how changes in phenologies influence long‐term dynamics of natural communities. Using this framework I demonstrate that persistence and coexistence conditions strongly depend on the difference in species’ mean phenologies and how this difference varies across years. Consequently, shifts in mean and interannual variation in relative phenologies of species can fundamentally alter the outcome of interactions and the potential for persistence and coexistence of competing species. These effects can be predicted by how per‐capita effects scale with differences in species’ phenologies. I outline how this approach can be parameterized with empirical systems and discuss how it fits within the context of current coexistence theory. Overall, this synthesis reveals that phenology of species interactions can play a crucial yet currently understudied role in driving coexistence and biodiversity patterns in natural systems and determine how species will respond to future climate change.     

The roles of shifting and filtering in generating community‐level flowering phenology

Plant phenologies are key components of community assembly and ecosystem function, yet we know little about how phenological patterns differ among ecosystems. Community‐level phenological patterns may be driven by the filtering of species into communities based on their phenology or by intraspecific responses to local conditions that shift when species flower. To understand the relative roles of filtering and shifting on community‐level phenological patterns we compared patterns of first flowering dates (FFD) for herbaceous species at Konza Prairie, KS, USA with those from the colder Fargo, ND, USA area and from Chinnor, England, which has a less continental climate. Comparing patterns of FFD supports that Konza's flowering patterns are potentially influenced both by filtering species that flower early in the growing season and by phenological shifting. Konza species flowering dates were earlier in the spring and later in the fall compared to Fargo, but were not shifted compared to Chinnor, which had a unique suite of early‐flowering species. In all, comparing flowering phenology among three sites reveals that intraspecific responses to climate can generate phenological shifts that compress or stretch community‐level phenological patterns, while novel niches in phenological space can also alter community‐level patterns. Community flowering patterns related to climate suggest that climatic warming has the potential to further distribute flowering of the Konza flora over a longer period, but also could further open it to introductions of non‐native species that have evolved to flower early in the season.     

A framework for understanding human‐driven vegetation change

Despite a major research focus on human‐mediated reshuffling of plant communities, no coherent framework unites the numerous types of changes in abundances and distributions of native and non‐native species that are driven by human activities. Human driven vegetation change can occur through: non‐native species introductions; population outbreaks or collapses; range expansions or contractions; and range shifts of both native and non‐native species. Boundaries among these different types of floristic changes are not always distinct because of an overlap in the ecological, climatic, and anthropogenic processes that underpin them. We propose a new framework that connects various human‐mediated causes of vegetation change, highlights the spatial scales at which drivers act and the temporal scale at which plant assemblages respond, and provides critical insights for identifying and appropriately managing these changes.     

Quantifying full phenological event distributions reveals simultaneous advances,temporal stability and delays in spring and autumn migration timing in long‐distance migratory birds

Phenological changes in key seasonally expressed life‐history traits occurring across periods of climatic and environmental change can cause temporal mismatches between interacting species, and thereby impact population and community dynamics. However, studies quantifying long‐term phenological changes have commonly only measured variation occurring in spring, measured as the first or mean dates on which focal traits or events were observed. Few studies have considered seasonally paired events spanning spring and autumn or tested the key assumption that single convenient metrics accurately capture entire event distributions. We used 60 years (1955–2014) of daily bird migration census data from Fair Isle, Scotland, to comprehensively quantify the degree to which the full distributions of spring and autumn migration timing of 13 species of long‐distance migratory bird changed across a period of substantial climatic and environmental change. In most species, mean spring and autumn migration dates changed little. However, the early migration phase (≤10th percentile date) commonly got earlier, while the late migration phase (≥90th percentile date) commonly got later. Consequently, species' total migration durations typically lengthened across years. Spring and autumn migration phenologies were not consistently correlated within or between years within species and hence were not tightly coupled. Furthermore, different metrics quantifying different aspects of migration phenology within seasons were not strongly cross‐correlated, meaning that no single metric adequately described the full pattern of phenological change. These analyses therefore reveal complex patterns of simultaneous advancement, temporal stability and delay in spring and autumn migration phenologies, altering species' life‐history structures. Additionally, they demonstrate that this complexity is only revealed if multiple metrics encompassing entire seasonal event distributions, rather than single metrics, are used to quantify phenological change. Existing evidence of long‐term phenological changes detected using only one or two metrics should consequently be interpreted cautiously because divergent changes occurring simultaneously could potentially have remained undetected.     

Community assembly along a successional gradient in sub‐alpine meadows of the Qinghai‐Tibetan Plateau,China

Community assembly is a dynamic progression that reflects the interaction of several processes functioning at multiple scales. Understanding how these processes work in communities at different successional stages is important for identifying when regional or local processes are more important for community assembly, and for developing effective preservation and restoration strategies. We examined community assembly using a chronosequence of sub‐alpine meadows in Qinghai‐Tibetan Plateau that range from ‘natural’ (never farmed), to those that have been protected from agricultural exploitation for 1 to 10 years. We tested for shifts in species and traits among meadows and also for changes in environmental and spatial correlates of species distributions within meadows. We found that species richness increased and species composition returned to natural conditions within ten years of protection. These changes coincided with shifts in species traits; abundant species had high seed mass and specific leaf area in late‐successional meadows, whereas the opposite occurred in early‐successional meadows. Despite these shifts among meadows of different ages, spatial distributions of species within meadows did not change – when associated with abiotic variables, these spatial patterns reflected changes in soil pH and nitrogen. There was also no consistent change in the relative importance of environmental and spatial correlates of species distributions within meadows. These trends indicate that local processes of community assembly are similar within meadows even when species in those meadows differ. We conclude that successional change is a large‐scale process that alters the species pool and resulting suite of traits that are present within meadows. As a result, regional planning that incorporates successional age should be the focus for the conservation of diversity in this area. In contrast, local processes work within the constraints of the species pool set by successional age, producing consistent patterns within meadows of different ages.     

Patterns of bird migration phenology in South Africa suggest northern hemisphere climate as the most consistent driver of change

Current knowledge of phenological shifts in Palearctic bird migration is largely based on data collected on migrants at their breeding grounds; little is known about the phenology of these birds at their nonbreeding grounds, and even less about that of intra‐African migrants. Because climate change patterns are not uniform across the globe, we can expect regional disparities in bird phenological responses. It is also likely that they vary across species, as species show differences in the strength of affinities they have with particular habitats and environments. Here, we examine the arrival and departure of nine Palearctic and seven intra‐African migratory species in the central Highveld of South Africa, where the former spend their nonbreeding season and the latter their breeding season. Using novel analytical methods based on bird atlas data, we show phenological shifts in migration of five species – red‐backed shrike, spotted flycatcher, common sandpiper, white‐winged tern (Palearctic migrants), and diederik cuckoo (intra‐African migrant) – between two atlas periods: 1987–1991 and 2007–2012. During this time period, Palearctic migrants advanced their departure from their South African nonbreeding grounds. This trend was mainly driven by waterbirds. No consistent changes were observed for intra‐African migrants. Our results suggest that the most consistent drivers of migration phenological shifts act in the northern hemisphere, probably at the breeding grounds.     

Robustness of mutualistic networks under phenological change and habitat destruction

Climate change can alter species phenologies and therefore disrupt species interactions. Habitat destruction can damage biodiversity and population viability. However, we still know very little about the potential effects of these two factors on the diversity and structure of interaction networks when both act simultaneously. Here we developed a mutualistic metacommunity model to explore the effects of habitat destruction and phenological changes on the diversity and structure of plant–pollinator networks. Using an empirical data set of plant and pollinator interactions and their duration in days, we simulated increasing levels of habitat destruction, under projected scenarios of phenological shifts as well for historically recorded changes in phenologies. On one hand, we found that habitat destruction causes catastrophic collapse in global diversity, as well as inducing alternative states. On the other hand, phenological shifts tend to make interactions weaker, increasing local extinction rates. Together, habitat destruction and phenological changes act synergistically, making metacommunities even more vulnerable to global collapse. Metacommunities are also more vulnerable to collapses under scenarios of historical change, in which phenologies are shortened, not just shifted. Furthermore, connectance and nestedness tends to decrease gradually with habitat destruction before the global collapse. Small phenological shifts can raise connectance slightly, due novel interactions appearing in a few generalist species, but larger shifts always reduce connectance. We conclude that the robustness of mutualistic metacommunities against habitat destruction can be greatly impaired by the weakening of positive interactions that results from the loss of phenological overlap.     

A centroid model of species distribution with applications to the Carolina wren Thryothorus ludovicianus and house finch Haemorhous mexicanus in the United States

Drastic shifts in species distributions are a cause of concern for ecologists. Such shifts pose great threat to biodiversity especially under unprecedented anthropogenic and natural disturbances. Many studies have documented recent shifts in species distributions. However, most of these studies are limited to regional scales, and do not consider the abundance structure within species ranges. Developing methods to detect systematic changes in species distributions over their full ranges is critical for understanding the impact of changing environments and for successful conservation planning. Here, we demonstrate a centroid model for range‐wide analysis of distribution shifts using the North American Breeding Bird Survey. The centroid model is based on a hierarchical Bayesian framework which models population change within physiographic strata while accounting for several factors affecting species detectability. Yearly abundance‐weighted range centroids are estimated. As case studies, we derive annual centroids for the Carolina wren and house finch in their ranges in the U.S. We further evaluate the first‐difference correlation between species’ centroid movement and changes in winter severity, total population abundance. We also examined associations of change in centroids from sub‐ranges. Change in full‐range centroid movements of Carolina wren significantly correlate with snow cover days (r = ?0.58). For both species, the full‐range centroid shifts also have strong correlation with total abundance (r = 0.65, and 0.51 respectively). The movements of the full‐range centroids of the two species are correlated strongly (up to r = 0.76) with that of the sub‐ranges with more drastic population changes. Our study demonstrates the usefulness of centroids for analyzing distribution changes in a two‐dimensional spatial context. Particularly it highlights applications that associate the centroid with factors such as environmental stressors, population characteristics, and progression of invasive species. Routine monitoring of changes in centroid will provide useful insights into long‐term avian responses to environmental changes.     

Phenology, ontogeny and the effects of climate change on the timing of species interactions

Climate change is altering the phenology of many species and the timing of their interactions with other species, but the impacts of these phenological shifts on species interactions remain unclear. Classical approaches to the study of phenology have typically documented changes in the timing of single life-history events, while phenological shifts affect many interactions over entire life histories. In this study, we suggest an approach that integrates the phenology and ontogeny of species interactions with a fitness landscape to provide a common mechanistic framework for investigating phenological shifts. We suggest that this ontogeny–phenology landscape provides a flexible method to document changes in the relative phenologies of interacting species, examine the causes of these phenological shifts, and estimate their consequences for interacting species.
Ecology Letters (2010) 13: 1–10     

Community‐wide changes in intertaxonomic temporal co‐occurrence resulting from phenological shifts

Global climate change is known to affect the assembly of ecological communities by altering species' spatial distribution patterns, but little is known about how climate change may affect community assembly by changing species' temporal co‐occurrence patterns, which is highly likely given the widely observed phenological shifts associated with climate change. Here, we analyzed a 29‐year phenological data set comprising community‐level information on the timing and span of temporal occurrence in 11 seasonally occurring animal taxon groups from 329 local meteorological observatories across China. We show that widespread shifts in phenology have resulted in community‐wide changes in the temporal overlap between taxa that are dominated by extensions, and that these changes are largely due to taxa's altered span of temporal occurrence rather than the degree of synchrony in phenological shifts. Importantly, our findings also suggest that climate change may have led to less phenological mismatch than generally presumed, and that the context under which to discuss the ecological consequences of phenological shifts should be expanded beyond asynchronous shifts.     

Trait matching and phenological overlap increase the spatio‐temporal stability and functionality of plant–pollinator interactions

Morphology and phenology influence plant–pollinator network structure, but whether they generate more stable pairwise interactions with higher pollination success remains unknown. Here we evaluate the importance of morphological trait matching, phenological overlap and specialisation for the spatio‐temporal stability (measured as variability) of plant–pollinator interactions and for pollination success, while controlling for species' abundance. To this end, we combined a 6‐year plant–pollinator interaction dataset, with information on species traits, phenologies, specialisation, abundance and pollination success, into structural equation models. Interactions among abundant plants and pollinators with well‐matched traits and phenologies formed the stable and functional backbone of the pollination network, whereas poorly matched interactions were variable in time and had lower pollination success. We conclude that phenological overlap could be more useful for predicting changes in species interactions than species abundances, and that non‐random extinction of species with well‐matched traits could decrease the stability of interactions within communities and reduce their functioning.     

Rapid climate driven shifts in wintering distributions of three common waterbird species

Climate change is predicted to cause changes in species distributions and several studies report margin range shifts in some species. However, the reported changes rarely concern a species' entire distribution and are not always linked to climate change. Here, we demonstrate strong north‐eastwards shifts in the centres of gravity of the entire wintering range of three common waterbird species along the North‐West Europe flyway during the past three decades. These shifts correlate with an increase of 3.8 °C in early winter temperature in the north‐eastern part of the wintering areas, where bird abundance increased exponentially, corresponding with decreases in abundance at the south‐western margin of the wintering ranges. This confirms the need to re‐evaluate conservation site safeguard networks and associated biodiversity monitoring along the flyway, as new important wintering areas are established further north and east, and highlights the general urgency of conservation planning in a changing world. Range shifts in wintering waterbirds may also affect hunting pressure, which may alter bag sizes and lead to population‐level consequences.     

Fear in the dark? Community‐level effects of non‐lethal predators change with light regime

The total effect of predators on prey is a combination of direct consumption, and non‐consumptive effects (NCEs), such as predator‐induced changes to prey morphology, behaviour and life history. Past research into NCEs has tended to focus on pair‐wise interactions between predators and prey, while in natural ecosystems, species exist in complex communities with several trophic levels made up of multiple autotrophic and heterotropic species. To address how predator NCEs alter the photosynthetic and heterotrophic components of communities, we exposed microbial microcosms to one of three predator treatments: live predators (full predator effect), freeze‐killed predators (NCEs only) or no predators (control), and incubated them under either 12 h:12 h light:dark conditions or continual darkness. Under 12 h:12 h light:dark conditions, NCEs‐only communities never differed from predator‐free communities, but differed from live predator communities. Under conditions of continual darkness, the structure of NCEs‐only communities differed from predator‐free controls, but not from live predator communities, suggesting NCEs can be strong enough to structure communities. Predation threat may cause certain prey to induce defences, such as reductions in movement, which make them less competitive in a community setting. This reduction in competitive ability could lead to these species being driven to extinction through interspecific competition, resulting in similar communities to those in which live predators are present. Heterotrophic species whose rates of resource acquisition depend on movement rates may be affected to a greater extent than autotrophs by predator‐induced reductions in movement, accounting for our observed differences in predator NCEs in ‘dark’ and ‘light’ communities. Our results suggest that the community‐level consequences of fear are greater in the dark. Synthesis Predators affect prey through consumptive and non‐consumptive effects (NCEs) such as alterations to prey behaviour, morphology, and life history. However, predators and prey do not exist in isolated pairs, but in complex communities where they interact with many other species. Using a long term study (>10 predator generations), we show that predator NCEs alone can alter community structure under conditions of darkness, but not in a 12h:12h light:dark cycle. Our results demonstrate for the first time that although the community‐level consequences of predator NCEs may be dramatic, they depend upon the abiotic conditions of the ecosystem.     

Plant–pollinator interactions and phenological change: what can we learn about climate impacts from experiments and observations?

Climate change can affect plant–pollinator interactions in a variety of ways, but much of the research attention has focused on whether independent shifts in phenology will alter temporal overlap between plants and pollinators. Here I review the research on plant–pollinator mismatch, assessing the potential for observational and experimental approaches to address particular aspects of the problem. Recent, primarily observational studies suggest that phenologies of co‐occurring plants and pollinators tend to respond similarly to environmental cues, but that nevertheless, certain pairs of interacting species are showing independent shifts in phenology. Only in a few cases, however, have these independent shifts been shown to affect population vital rates (specifically, seed production by plants) but this largely reflects a lack of research. Compared to the few long‐term studies of pollination in natural plant populations, experimental manipulations of phenology have yielded relatively optimistic conclusions about effects of phenological shifts on plant reproduction, and I discuss how issues of scale and frequency‐dependence in pollinator behaviour affect the interpretation of these ‘temporal transplant’ experiments. Comparable research on the impacts of mismatch on pollinator populations is so far lacking, but both observational studies and focused experiments have the potential to improve our forecasts of pollinator responses to changing phenologies. Finally, while there is now evidence that plant–pollinator mismatch can affect seed production by plants, it is still unclear whether this phenological impact will be the primary way in which climate change affects plant–pollinator interactions. It would be useful to test the direct effects of changing climate on pollinator population persistence, and to compare the importance of phenological mismatch with other threats to pollination.     

COEVOLUTION AND THE ARCHITECTURE OF MUTUALISTIC NETWORKS

Although coevolution is widely recognized as an important evolutionary process for pairs of reciprocally specialized species, its importance within species‐rich communities of generalized species has been questioned. Here we develop and analyze mathematical models of mutualistic communities, such as those between plants and pollinators or plants and seed‐dispersers to evaluate the importance of coevolutionary selection within complex communities. Our analyses reveal that coevolutionary selection can drive significant changes in trait distributions with important consequences for the network structure of mutualistic communities. One such consequence is greater connectance caused by an almost invariable increase in the rate of mutualistic interaction within the community. Another important consequence is altered patterns of nestedness. Specifically, interactions mediated by a mechanism of phenotype matching tend to be antinested when coevolutionary selection is weak and even more strongly antinested as increasing coevolutionary selection favors the emergence of reciprocal specialization. In contrast, interactions mediated by a mechanism of phenotype differences tend to be nested when coevolutionary selection is weak, but less nested as increasing coevolutionary selection favors greater levels of generalization in both plants and animals. Taken together, our results show that coevolutionary selection can be an important force within mutualistic communities, driving changes in trait distributions, interaction rates, and even network structure.     

Disentangling climate change effects on species interactions: effects of temperature, phenological shifts, and body size

Climate-mediated shifts in species’ phenologies are expected to alter species interactions, but predicting the consequences of this is difficult because phenological shifts may be driven by different climate factors that may or may not be correlated. Temperature could be an important factor determining effects of phenological shifts by altering species’ growth rates and thereby the relative size ratios of interacting species. We tested this hypothesis by independently manipulating temperature and the relative hatching phenologies of two competing amphibian species. Relative shifts in hatching time generally altered the strength of competition, but the presence and magnitude of this effect was temperature dependent and joint effects of temperature and hatching phenology were non-additive. Species that hatched relatively early or late performed significantly better or worse, respectively, but only at higher temperatures and not at lower temperatures. As a consequence, climate-mediated shifts in hatching phenology or temperature resulted in stronger or weaker effects than expected when both factors acted in concert. Furthermore, consequences of phenological shifts were asymmetric; arriving relatively early had disproportional stronger (or weaker) effects than arriving relatively late, and this varied with species identity. However, consistent with recent theory, these seemingly idiosyncratic effects of phenological shifts could be explained by species-specific differences in growth rates across temperatures and concordant shifts in relative body size of interacting species. Our results emphasize the need to account for environmental conditions when predicting the effects of phenological shifts, and suggest that shifts in size-structured interactions can mediate the impact of climate change on natural communities.     

Phenology in a warming world: differences between native and non‐native plant species

Phenology is a harbinger of climate change, with many species advancing flowering in response to rising temperatures. However, there is tremendous variation among species in phenological response to warming, and any phenological differences between native and non‐native species may influence invasion outcomes under global warming. We simulated global warming in the field and found that non‐native species flowered earlier and were more phenologically plastic to temperature than natives, which did not accelerate flowering in response to warming. Non‐native species' flowering also became more synchronous with other community members under warming. Earlier flowering was associated with greater geographic spread of non‐native species, implicating phenology as a potential trait associated with the successful establishment of non‐native species across large geographic regions. Such phenological differences in both timing and plasticity between native and non‐natives are hypothesised to promote invasion success and population persistence, potentially benefiting non‐native over native species under climate change.