(A bit) Earlier or later is always better: Phenological shifts in consumer–resource interactions

Phenology is a crucial life history trait for species interactions and it can have great repercussions on the persistence of communities and ecosystems. Changes in phenology caused by climate change can disrupt species interactions causing decreases in consumer growth rates, as suggested by the match–mismatch hypothesis (MMH). However, it is still not clear what the long-term consequences of such phenological changes are. In this paper, we present models in which phenology and consumer–resource feedbacks determine long-term community dynamics. Our results show that consumer viability is constrained by limits in the amount of phenological mismatch with their resources, in accordance with the MMH, but the effects of phenological shifts are often nonmonotonic. Consumers generally have higher abundances when they recruit some time before or after their resources because this reduces the long-term effects of overexploitation that would otherwise occur under closer synchrony. Changes in the duration of recruitment phenologies also have important impacts on community stability, with shorter phenologies promoting oscillations and cycles. For small community modules, the effects of phenological shifts on populations can be explained, to a great extent, as superpositions of their effects on consumer–resource pairs. We highlight that consumer–resource feedbacks and overexploitation, which are not typically considered in phenological models, are important factors shaping the long-term responses to phenological changes caused by climate change.     

Diapause and bet-hedging strategies in insects: a meta-analysis of reaction norm shapes

Many organisms escape from lethal climatological conditions by entering a resistant resting stage called diapause, which needs to be optimally timed with seasonal change. As climate change exerts selection pressure on phenology, the evolution of mean diapause timing, but also of phenotypic plasticity and bet-hedging strategies is expected. The potential of the latter strategy as a means of coping with environmental unpredictability has received little attention in the climate change literature. Populations should be adapted to spatial variation in local conditions; contemporary patterns of phenological strategies across a geographic range may hence provide information about their evolvability. We thus extracted 458 diapause reaction norms from 60 studies. First, we correlated mean diapause timing with mean winter onset. Then we partitioned the reaction norm variance into a temporal component (phenotypic plasticity) and among-offspring variance (diversified bet-hedging) and correlated this variance composition with variability of winter onset. Mean diapause timing correlated reasonably well with mean winter onset, except for populations at high latitudes, which apparently failed to track early onsets. Variance among offspring was, however, limited and correlated only weakly with environmental variability, indicating little scope for bet-hedging. The apparent lack of phenological bet-hedging strategies may pose a risk in a less predictable climate, but we also highlight the need for more data on alternative strategies.     

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.     

Environmental controls on the phenology of moths: predicting plasticity and constraint under climate change

Ecological systems have naturally high interannual variance in phenology. Component species have presumably evolved to maintain appropriate phenologies under historical climates, but cases of inappropriate phenology can be expected with climate change. Understanding controls on phenology permits predictions of ecological responses to climate change. We studied phenological control systems in Lepidoptera by analyzing flight times recorded at a network of sites in Finland. We evaluated the strength and form of controls from temperature and photoperiod, and tested for geographic variation within species. Temperature controls on phenology were evident in 51% of 112 study species and for a third of those thermal controls appear to be modified by photoperiodic cues. For 24% of the total, photoperiod by itself emerged as the most likely control system. Species with thermal control alone should be most immediately responsive in phenology to climate warming, but variably so depending upon the minimum temperature at which appreciable development occurs and the thermal responsiveness of development rate. Photoperiodic modification of thermal controls constrains phenotypic responses in phenologies to climate change, but can evolve to permit local adaptation. Our results suggest that climate change will alter the phenological structure of the Finnish Lepidoptera community in ways that are predictable with knowledge of the proximate physiological controls. Understanding how phenological controls in Lepidoptera compare to that of their host plants and enemies could permit general inferences regarding climatic effects on mid- to high-latitude ecosystems.     

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.     

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     

Phenologically explicit models for studying plant–pollinator interactions under climate change

Climate change is significantly influencing phenology. One potential effect is that historically interacting partners will respond to climate change at different rates, creating the potential for a phenological mismatch among previously synchronized interacting species, or even sexes of the same species. Focusing on plant demographics in a plant–pollinator interaction, we develop a hybrid dynamical model that uses a “non-autonomous” differential equation system (Zonneveld model) for within-season dynamics and discrete equations for season-to-season dynamics. Our model outlines how and when changes in the relative phenologies of an interacting species pair will alter the demographic outcome of the interaction. For our plant–pollinator system, we find that plant population growth rates are particularly sensitive to phenology mismatch when flowers are short-lived, when pollinators are short-lived, or when flowers and pollinators exhibit high levels of within-population synchrony in emergence or arrival dates. More generally, our aim is to introduce the use of hybrid dynamical models as a framework through which researchers can directly explore the demographic consequences of climatically driven phenological change.     

Effects of microtopography and hydrology on phenology of an invasive herb

Phenological traits may influence invasion success via effects on invasiveness of the colonizing species and invasibility of the receiving ecosystems. Many species exhibit substantial fine-scaled spatial variation in phenology and interannual differences in phenological timing in response to environmental variation. Yet describing and understanding this variation is limited by the availability of appropriate spatial and temporal datasets. Remote sensing provides such datasets, but has primarily been used to monitor broad-scale phenological patterns at coarse resolutions, necessarily missing fine spatial detail and intraspecies variation. We used hyperspectral remote sensing to characterize the spatial and temporal phenological variation of the invasive species Lepidium latifolium (perennial pepperweed) at two sites in California's San Francisco Bay/Sacramento–San Joaquin River Delta. Considerable phenological variation was detected: L. latifolium was simultaneously present in vegetative, early flowering, peak flowering, fruiting, and senescent stages in late June; the relative dominance and distribution of these stages varied interannually. Environmental determinants of phenology were investigated with variables derived from the hyperspectral image data, from a high resolution LiDAR (light detection and ranging) digital elevation model (DEM), and from local precipitation and streamflow data. Lepidium latifolium phenology was found to track water availability, and may also be influenced by intraspecific competition and edaphic stress. Lepidium latifolium has a unique phenology (summer flowering) relative to the communities it invades, which may allow invasion of an empty niche. Furthermore, many habitats are invaded by L. latifolium, which occurs in locally appropriate phenologies under the different environmental conditions. The environmental responsiveness of L. latifolium phenology may mediate the wide breadth of invasible habitats.     

Genetic and phenotypic sources of life history variation along a cline in voltinism in the cricket Allonemobius socius

Clinal variation in life histories can be genetically based, resulting from selection imposed by different environments, or it may be due to the differential expression of phenotypically plastic traits. We examined the cline in voltinism in the egg-diapausing cricket Allonemobius socius, with populations spanning the switch from a univoltine to a bivoltine phenology. A common garden experiment was employed, using environments that mimicked photoperiod and temperature conditions found in the field. There were only small differences in development time among populations, and the difference in phenology observed in the field is likely due to clinal variation in the length of the growing season. We found large genetically-based differences in the reaction norm for egg diapause that were further magnified by environmental cues. The synergism of genetic and environmental effects was an example of cogradient selection. In the zone of transition between phenologies, voltinism appeared to be a conditional strategy, rather than a genetic polymorphism. First-generation females from this area can lay either direct-developing or diapause eggs depending on the likelihood that a second generation will have sufficient time to develop. For this species, the cline in voltinism is the result of a combination of environmental effects on development, and genetic and environmental influences on egg diapause propensity.     

Predicting phenology by integrating ecology,evolution and climate science

Forecasting how species and ecosystems will respond to climate change has been a major aim of ecology in recent years. Much of this research has focused on phenology – the timing of life‐history events. Phenology has well‐demonstrated links to climate, from genetic to landscape scales; yet our ability to explain and predict variation in phenology across species, habitats and time remains poor. Here, we outline how merging approaches from ecology, climate science and evolutionary biology can advance research on phenological responses to climate variability. Using insight into seasonal and interannual climate variability combined with niche theory and community phylogenetics, we develop a predictive approach for species’ reponses to changing climate. Our approach predicts that species occupying higher latitudes or the early growing season should be most sensitive to climate and have the most phylogenetically conserved phenologies. We further predict that temperate species will respond to climate change by shifting in time, while tropical species will respond by shifting space, or by evolving. Although we focus here on plant phenology, our approach is broadly applicable to ecological research of plant responses to climate variability.     

北京地区木本春季物候特征与生物学特性的关系

植物物候是植物生活史中的重要性状,也是指示气候与自然环境变化的重要指标,现已成为全球变化领域的研究热点之一。传统物候研究多假设物候由气候因素决定,如气温、降水、光照等,并主要从植物物候的年际变化角度探讨了气候因素对物候特征的影响。然而,不同物种的物候存在较大差异表明植物物候还与自身生物学特性（如系统发育和功能性状）有关,但植物生物学特性如何影响植物物候仍缺乏深入研究。基于北京地区44种木本植物1965-2018年的展叶始期和开花始期观测资料,以展叶始期和开花始期的3类物候特征（平均物候期、物候对温度的响应敏感度和物候期的积温需求）为例,探究植物物候特征与系统发育和功能性状的关系。首先,利用系统发育信号Blomberg’s K和进化模型检验植物物候特征是否具有系统发育保守性,并通过系统发育信号表征曲线直观表达植物物候特征的进化模式;之后,利用广义估计方程分析植物生活型、传粉型与物候特征的关系,以揭示不同植物的资源利用方式及生存策略的差异。研究发现：（1）除展叶始期的温度敏感度外,其余物候特征的进化均受随机遗传漂变和自然选择力的共同作用,可推断物候特征具有系统发育保守性,即亲缘关系越近的物种物候特征越相似。（2）开花始期的系统发育信号强度比展叶始期更大,表明繁殖物候的系统发育可能比生长物候更保守。（3）植物展叶始期及其积温需求与生活型密切相关。灌木比乔木的展叶时间早、积温需求少。植物开花始期与传粉型相关,风媒植物开花显著早于虫媒植物。研究成果有助于深入理解物候变化的生物学机制,对于丰富物候学的理论研究有重要意义,同时对植物保护也具有重要的指导价值。     

Inter and intraspecific variation on reproductive phenology of the Brazilian Atlantic forest Rubiaceae: ecology and phylogenetic constraints

The reproductive phenology of seven species of Rubiaceae from the Brazilian Atlantic rain forest was compared to evaluate the occurrence of phylogenetic constraints on flowering and fruiting phenologies. Since phenological patterns can be affected by phylogenetic constraints, we expected that reproductive phenology would be similar among plants within a family or genus, occurring during the same time (or season) of the year. Observations on flowering and fruiting phenology were carried out monthly, from December 1996 to January 1998, at Núcleo Picinguaba, Parque Estadual da Serra do Mar, Ubatuba, S?o Paulo State, Brazil. Nine phenological variables were calculated to characterize, quantify and compare the reproductive phenology of the Rubiaceae species. The flowering patterns were different among the seven species studied, and the Kruskal-Wallis test indicated significant differences in flowering duration first flowering, peak flowering and flowering synchrony. The peaks and patterns of fruiting intensity were different among the Rubiaceae species studied and they differed significantly from conspecifics in the phenological variables fruiting duration, fruiting peak date, and fruiting synchrony (Kruskal-Wallis test). Therefore, we found no evidence supporting the phylogenetic hypotheses, and climate does not seem to constrain flowering and fruiting patterns of the Rubiaceae species in the understory of the Atlantic forest.     

QUANTITATIVE GENETICS OF SIZE AND PHENOLOGY OF LIFE-HISTORY TRAITS IN CHAMAECRISTA FASCICULATA

Despite numerous adaptive scenarios concerning the evolution of plant life-history phenologies few studies have examined the heritable basis for and genetic correlations among these phenologies. Documentation of genetic variation for and covariation among reproductive phenologies is important because it is this variation/covariation that will determine the potential for response to evolutionary forces. To address this problem, I conducted a breeding experiment to determine narrow-sense heritabilities for and genetic correlations among the phenologies of life-history events and plant size in Chamaecristafasciculata, a temperate summer annual plant species. Paternal families showed no evidence of heritable variation for two estimates of plant size, six measures of reproductive phenology or two fitness components. Similarly, paternal estimates of genetic correlations among these traits were low or zero. In contrast, maternal estimates of heritability suggested the influence of maternal parent on one estimate of plant size and four phenological traits. Likewise, maternal effects influenced maternal estimates of genetic correlations. These maternal effects can arise from three sources: endosperm nuclear, cytoplasmic genetic and/or maternal phenotypic. The degree to which the phenology of one life-history trait acts as a constraint on the evolution of other phenological traits depends on the source of the maternal influence in this species.     

Cryptic phenology in plants: Case studies,implications, and recommendations

Plant phenology—the timing of cyclic or recurrent biological events in plants—offers insight into the ecology, evolution, and seasonality of plant‐mediated ecosystem processes. Traditionally studied phenologies are readily apparent, such as flowering events, germination timing, and season‐initiating budbreak. However, a broad range of phenologies that are fundamental to the ecology and evolution of plants, and to global biogeochemical cycles and climate change predictions, have been neglected because they are “cryptic”—that is, hidden from view (e.g., root production) or difficult to distinguish and interpret based on common measurements at typical scales of examination (e.g., leaf turnover in evergreen forests). We illustrate how capturing cryptic phenology can advance scientific understanding with two case studies: wood phenology in a deciduous forest of the northeastern USA and leaf phenology in tropical evergreen forests of Amazonia. Drawing on these case studies and other literature, we argue that conceptualizing and characterizing cryptic plant phenology is needed for understanding and accurate prediction at many scales from organisms to ecosystems. We recommend avenues of empirical and modeling research to accelerate discovery of cryptic phenological patterns, to understand their causes and consequences, and to represent these processes in terrestrial biosphere models.     

Confounding effects of spatial variation on shifts in phenology

Shifts in the timing of life history events have become an important source of information about how organisms are responding to climate change. Phenological data have generally been treated as purely temporal, with scant attention to the inherent spatial aspects of such data. However, phenological data are tied to a specific location, and considerations of sampling design, both over space and through time, can critically affect the patterns that emerge. Focusing on flowering phenology, we describe how purely spatial shifts, such as adding new study plots, or the colonization of a study plot by a new species, can masquerade as temporal shifts. Such shifts can look like responses to climate change but are not. Furthermore, the same aggregate phenological curves can be composed of individuals with either very different or very similar phenologies. We conclude with a set of recommendations to avoid ambiguities arising from the spatiotemporal duality of phenological data.     

Phenology research for natural resource management in the United States

Natural resource professionals in the United States recognize that climate-induced changes in phenology can substantially affect resource management. This is reflected in national climate change response plans recently released by major resource agencies. However, managers on-the-ground are often unclear about how to use phenological information to inform their management practices. Until recently, this was at least partially due to the lack of broad-based, standardized phenology data collection across taxa and geographic regions. Such efforts are now underway, albeit in very early stages. Nonetheless, a major hurdle still exists: phenology-linked climate change research has focused more on describing broad ecological changes rather than making direct connections to local to regional management concerns. To help researchers better design relevant research for use in conservation and management decision-making processes, we describe phenology-related research topics that facilitate “actionable” science. Examples include research on evolution and phenotypic plasticity related to vulnerability, the demographic consequences of trophic mismatch, the role of invasive species, and building robust ecological forecast models. Such efforts will increase phenology literacy among on-the-ground resource managers and provide information relevant for short- and long-term decision-making, particularly as related to climate response planning and implementing climate-informed monitoring in the context of adaptive management. In sum, we argue that phenological information is a crucial component of the resource management toolbox that facilitates identification and evaluation of strategies that will reduce the vulnerability of natural systems to climate change. Management-savvy researchers can play an important role in reaching this goal.     

Phenological patterns of <Emphasis Type="Italic">Ficus citrifolia</Emphasis> (Moraceae) in a seasonal humid-subtropical region in Southern Brazil

Year-round flowering is widely reported in fig trees and is necessary for the survival of their short-living, specialized Agaonid pollinators. However, seasonality in both fig and leaf production has been noted in almost all published phenological studies. We have addressed the following questions in the present study: (1) Are reproductive and vegetative phenologies seasonal and, consequently, related to climate? (2) Does Ficus citrifolia produce ripe figs year round? (3) Is the fig development related to climate? And, (4) Are reproductive and vegetative phenologies independent? By investigating these questions with a F. citrifolia population over a two-year period, at the southern edge of the tropical region in Brazil, we detected phenological seasonality that was significantly correlated with climate. Our findings can be summarized as follows: (1) Trees became deciduous during the cold and dry months; (2) The flowering onset was asynchronous among individuals, but with moderate concentration during the hot and rainy months; (3) There was a correlation between the onset of flowering and vegetative phenology, with significantly higher crop initiations in individuals with full-leaf canopy; (4) Fig developmental time was longer in cold months; and (5) Ripe fig production occurred year-round and was not correlated with climate. Our results suggest that there are strong selection pressures that maintain the year-round flowering phenology in figs, for we have observed little seasonality in the phenology of such species despite the strong seasonality in the environment.     

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.     

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.     

Variation in breeding phenology provides insights into drivers of long-term population change in harbour seals

Phenological trends provide important indicators of environmental change and population dynamics. However, the use of untested population-level measures can lead to incorrect conclusions about phenological trends, particularly when changes in population structure or density are ignored. We used individual-based estimates of birth date and lactation duration of harbour seals (Phoca vitulina) to investigate energetic consequences of changes in pupping phenology. Using generalized linear mixed models, we first demonstrate annual variation in pupping phenology. Second, we show a negative relationship between lactation duration and the timing of pupping, indicating that females who pup early nurse their pups longer, thereby highlighting lactation duration as a useful proxy of female condition and resource availability. Third, individual-based data were used to derive a population-level proxy that demonstrated an advance in pupping date over the last 25 years, co-incident with a reduction in population abundance that resulted from fisheries-related shootings. These findings demonstrate that phenological studies examining the impacts of climate change on mammal populations must carefully control for changes in population density and highlight how joint investigations of phenological and demographic change provide insights into the drivers of population declines.