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.     

Predicting the sensitivity of butterfly phenology to temperature over the past century

Studies to date have documented substantial variation among species in the degree to which phenology responds to temperature and shifts over time, but we have a limited understanding of the causes of such variation. Here, we use a spatially and temporally extensive data set (ca. 48 000 observations from across Canada) to evaluate the utility of museum collection records in detecting broad‐scale phenology‐temperature relationships and to test for systematic differences in the sensitivity of phenology to temperature (days °C^?1) of Canadian butterfly species according to relevant ecological traits. We showed that the timing of flight season predictably responded to temperature both across space (variation in average temperature from site to site in Canada) and across time (variation from year to year within each individual site). This reveals that collection records, a vastly underexploited resource, can be applied to the quantification of broad‐scale relationships between species' phenology and temperature. The timing of the flight season of earlier fliers and less mobile species was more sensitive to temperature than later fliers and more mobile species, demonstrating that ecological traits can account for some of the interspecific variation in species' phenological sensitivity to temperature. Finally, we found that phenological sensitivity to temperature differed across time and space implying that both dimensions of temperature will be needed to translate species' phenological sensitivity to temperature into accurate predictions of species' future phenological shifts. Given the widespread temperature sensitivity of flight season timing, we can expect long‐term temporal shifts with increased warming [ca. 2.4 days °C^?1 (0.18 SE)] for many if not most butterfly species.     

Plant phenology networks of citizen scientists: recommendations from two decades of experience in Canada

Plant phenology networks of citizen scientists have a long history and have recently contributed to our understanding of climate change effects on ecosystems. This paper describes the development of the Alberta and Canada PlantWatch programs, which coordinate networks of citizen scientists who track spring development timing for common plants. Tracking spring phenology is highly suited to volunteers and, with effective volunteer management, observers will stay loyal to a phenology program for many years. Over two decades beginning in 1987, Alberta PlantWatch volunteers reported 47,000 records, the majority contributed by observers who participated for more than 9 years. We present a quantitative analysis of factors that determine the quality of this phenological data and explore sources of variation. Our goal is to help those who wish to initiate new observer networks with an analysis of the effectiveness of program protocols including selected plant species and bloom stages.     

Macrophenology: insights into the broad-scale patterns,drivers, and consequences of phenology

Plant phenology research has surged in recent decades, in part due to interest in phenological sensitivity to climate change and the vital role phenology plays in ecology. Many local-scale studies have generated important findings regarding the physiology, responses, and risks associated with shifts in plant phenology. By comparison, our understanding of regional- and global-scale phenology has been largely limited to remote sensing of green-up without the ability to differentiate among plant species. However, a new generation of analytical tools and data sources—including enhanced remote sensing products, digitized herbarium specimen data, and public participation in science—now permits investigating patterns and drivers of phenology across extensive taxonomic, temporal, and spatial scales, in an emerging field that we call macrophenology. Recent studies have highlighted how phenology affects dynamics at broad scales, including species interactions and ranges, carbon fluxes, and climate. At the cusp of this developing field of study, we review the theoretical and practical advances in four primary areas of plant macrophenology: (1) global patterns and shifts in plant phenology, (2) within-species changes in phenology as they mediate species' range limits and invasions at the regional scale, (3) broad-scale variation in phenology among species leading to ecological mismatches, and (4) interactions between phenology and global ecosystem processes. To stimulate future research, we describe opportunities for macrophenology to address grand challenges in each of these research areas, as well as recently available data sources that enhance and enable macrophenology research.     

Phenological Changes in the Southern Hemisphere

Current evidence of phenological responses to recent climate change is substantially biased towards northern hemisphere temperate regions. Given regional differences in climate change, shifts in phenology will not be uniform across the globe, and conclusions drawn from temperate systems in the northern hemisphere might not be applicable to other regions on the planet. We conduct the largest meta-analysis to date of phenological drivers and trends among southern hemisphere species, assessing 1208 long-term datasets from 89 studies on 347 species. Data were mostly from Australasia (Australia and New Zealand), South America and the Antarctic/subantarctic, and focused primarily on plants and birds. This meta-analysis shows an advance in the timing of spring events (with a strong Australian data bias), although substantial differences in trends were apparent among taxonomic groups and regions. When only statistically significant trends were considered, 82% of terrestrial datasets and 42% of marine datasets demonstrated an advance in phenology. Temperature was most frequently identified as the primary driver of phenological changes; however, in many studies it was the only climate variable considered. When precipitation was examined, it often played a key role but, in contrast with temperature, the direction of phenological shifts in response to precipitation variation was difficult to predict a priori. We discuss how phenological information can inform the adaptive capacity of species, their resilience, and constraints on autonomous adaptation. We also highlight serious weaknesses in past and current data collection and analyses at large regional scales (with very few studies in the tropics or from Africa) and dramatic taxonomic biases. If accurate predictions regarding the general effects of climate change on the biology of organisms are to be made, data collection policies focussing on targeting data-deficient regions and taxa need to be financially and logistically supported.     

Phenological indices of avian reproduction: cryptic shifts and prediction across large spatial and temporal scales

Climate change‐induced shifts in phenology have important demographic consequences, and are frequently used to assess species' sensitivity to climate change. Therefore, developing accurate phenological predictions is an important step in modeling species' responses to climate change. The ability of such phenological models to predict effects at larger spatial and temporal scales has rarely been assessed. It is also not clear whether the most frequently used phenological index, namely the average date of a phenological event across a population, adequately captures phenological shifts in the distribution of events across the season. We use the long‐tailed tit Aegithalos caudatus (Fig. 1) as a case study to explore these issues. We use an intensive 17‐year local study to model mean breeding date and test the capacity of this local model to predict phenology at larger spatial and temporal scales. We assess whether local models of breeding initiation, termination, and renesting reveal phenological shifts and responses to climate not detected by a standard phenological index, that is, population average lay date. These models take predation timing/intensity into account. The locally‐derived model performs well at predicting phenology at the national scale over several decades, at both high and low temperatures. In the local model, a trend toward warmer Aprils is associated with a significant advance in termination dates, probably in response to phenological shifts in food supply. This results in a 33% reduction in breeding season length over 17 years – a substantial loss of reproductive opportunity that is not detected by the index of population average lay date. We show that standard phenological indices can fail to detect patterns indicative of negative climatic effects, potentially biasing assessments of species' vulnerability to climate change. More positively, we demonstrate the potential of detailed local studies for developing broader‐scale predictive models of future phenological shifts.     

Phenology of two interdependent traits in migratory birds in response to climate change

In migratory birds, arrival date and hatching date are two key phenological markers that have responded to global warming. A body of knowledge exists relating these traits to evolutionary pressures. In this study, we formalize this knowledge into general mathematical assumptions, and use them in an ecoevolutionary model. In contrast to previous models, this study novelty accounts for both traits—arrival date and hatching date—and the interdependence between them, revealing when one, the other or both will respond to climate. For all models sharing the assumptions, the following phenological responses will occur. First, if the nestling-prey peak is late enough, hatching is synchronous with, and arrival date evolves independently of, prey phenology. Second, when resource availability constrains the length of the pre-laying period, hatching is adaptively asynchronous with prey phenology. Predictions for both traits compare well with empirical observations. In response to advancing prey phenology, arrival date may advance, remain unchanged, or even become delayed; the latter occurring when egg-laying resources are only available relatively late in the season. The model shows that asynchronous hatching and unresponsive arrival date are not sufficient evidence that phenological adaptation is constrained. The work provides a framework for exploring microevolution of interdependent phenological traits.     

Tell me what you eat and I'll tell you when you fly: diet can predict phenological changes in response to climate change

Changes in phenology are correlated with climate change. However, we still struggle to understand the traits making species susceptible to climate change, and the implications of species' reactions for communities and food webs. Butterflies and moths are an ecologically important group that have shown pronounced phenological changes over the last decades. Tests using a > 150-year dataset from 566 European butterfly and moth species demonstrated that variation in phenological change was strongly related to traits describing plant-herbivore interactions (larval diet breadth, diet composition), and the life cycle. The results indicate that climate change related shifts in phenology are correlated with the seasonal availability and palatability of food plants. Lepidopterans feeding on herbaceous plants showed smaller shifts in flight periods but larger increases in voltinism than lepidopterans feeding on woody plants. Consequently, the effect of herbivorous lepidopterans may increase in herb-rich grassland ecosystems under warmer conditions, and not in forest ecosystems.     

A phenological shift in the time of recruitment of the shipworm,Teredo navalis L., mirrors marine climate change

For many species, seasonal changes in key environmental variables such as food availability, light, and temperature drive the timing (“phenology”) of major life‐history events. Extensive evidence from terrestrial, freshwater, and marine habitats shows that global warming is changing the timings of many biological events; however, few of these studies have investigated the effects of climate change on the phenology of larval recruitment in marine invertebrates. Here, we studied temperature‐related phenological shifts in the breeding season of the shipworm Teredo navalis (Mollusca, Bivalvia). We compared data for the recruitment period of T. navalis along the Swedish west coast during 2004–2006 with similar data from 1971–1973, and related differences in recruitment timing to changes in sea surface temperature over the same period. We found no significant shift in the timing of onset of recruitment over this ~30‐year time span, but the end of recruitment was an average of 26 days later in recent years, leading to significantly longer recruitment periods. These changes correlated strongly with increased sea surface temperatures and coincided with published thermal tolerances for reproduction in T. navalis. Our findings are broadly comparable with other reports of phenological shifts in marine species, and suggest that warmer sea surface temperatures are increasing the likelihood of successful subannual reproduction and intensifying recruitment of T. navalis in this region.     

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。     

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.     

Interannual phenological variability in two North-East Atlantic populations of Calanus finmarchicus

Phenological variations of the marine copepod Calanus finmarchicus were studied in Svalbard and northern Iceland, where samples were collected in summer and spring, respectively, over two decades. Four phenological indices, developed for copepodite stage-structured data, were used: the proportion of CV to total abundance (CVT), the population development index (PDI), the average weighted stage (AWS), and the average age in days (AAD). The variation of these indices was compared within and between locations to evaluate their suitability for the analysis of phenological effects. For both populations, phenology was related to local temperature and spring bloom dynamics, influenced by Atlantic water inflow. Large-scale climate was related to phenological variation only in the Svalbard population. C. finmarchicus phenology advanced under warmer conditions in both locations. We conclude that vertical phenological indices, i.e. based on interannual changes in copepodite stage structure, are useful to investigate zooplankton phenology, especially when data series covering the whole life cycle are unavailable. We suggest that AWS and AAD can be applied irrespective of sampling time, while PDI and CVT should be applied for early and late sampling seasons, respectively. When multiple phenological indices are needed, AAD in combination with either CVT or PDI should be preferred.     

A reversal of the shift towards earlier spring phenology in several Mediterranean reptiles and amphibians during the 1998–2013 warming slowdown

Herps, especially amphibians, are particularly susceptible to climate change, as temperature tightly controls many parameters of their biological cycle—above all, their phenology. The timing of herps’ activity or migration period—in particular the dates of their first appearance in spring and first breeding—and the shift to earlier dates in response to warming since the last quarter of the 20^th century has often been described up to now as a nearly monotonic trend towards earlier phenological events. In this study, we used citizen science data opportunistically collected on reptiles and amphibians in the northern Mediterranean basin over a period of 32 years to explore temporal variations in herp phenology. For 17 common species, we measured shifts in the date of the species’ first spring appearance—which may be the result of current changes in climate—and regressed the first appearance date against temperatures and precipitations. Our results confirmed the expected overall trend towards earlier first spring appearances from 1983 to 1997, and show that the first appearance date of both reptiles and amphibians fits well with the temperature in late winter. However, the trend towards earlier dates was stopped or even reversed in most species between 1998 and 2013. We interpret this reversal as a response to cooling related to the North Atlantic Oscillation (NAO) in the late winter and early spring. During the positive NAO episodes, for certain species only (mainly amphibians), the effect of a warm weather, which tends to advance the phenology, seems to be counterbalanced by the adverse effects of the relative dryness.     

A systematic review of vegetation phenology in Africa

The study of vegetation phenology is important because it is a sensitive indicator of climate changes and it regulates carbon, energy and water fluxes between the land and atmosphere. Africa, which has 17% of the global forest cover, contributes significantly to the global carbon budget and has been identified as potentially highly vulnerable to climate change impacts. In spite of this, very little is known about vegetation phenology across Africa and the factors regulating vegetation growth and dynamics. Hence, this review aimed to provide a synthesis of studies of related Africa's vegetation phenology and classify them based on the methods and techniques used in order to identify major research gaps. Significant increases in the number of phenological studies in the last decade were observed, with over 70% of studies adopting a satellite-based remote sensing approach to monitor vegetation phenology. Whereas ground based studies that provide detailed characterisation of vegetation phenological development, occurred rarely in the continent. Similarly, less than 14% of satellite-based remote sensing studies evaluated vegetation phenology at the continental scale using coarse spatial resolution datasets. Even more evident was the lack of research focusing on the impacts of climate change on vegetation phenology. Consequently, given the importance and the uniqueness of both methods of phenological assessment, there is need for more ground-based studies to enable greater understanding of phenology at the species level. Likewise, finer spatial resolution satellite sensor data for regional phenological assessment is required, with a greater focus on the relationship between climate change and vegetation phenological changes. This would contribute greatly to debates over climate change impacts and, most importantly, climate change mitigation strategies.     

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.     

Who flies first? – habitat‐specific phenological shifts of butterflies and orthopterans in the light of climate change: a case study from the south‐east Mediterranean

1. Insects undergo phenological change at different rates, showing no consistent trend between habitats, time periods, species or groups. Understanding how and why this variability occurs is crucial. 2. Phenological patterns of butterflies and Orthoptera were analysed using a novel approach of standardised major axis (SMA) analysis. It was investigated whether: (i) phenology (the mean date and duration of flight) of butterflies and Orthoptera changed from one survey (1998 and 1999 respectively) to another (2011), (ii) the rate at which phenology changed differed between taxa and (iii) phenological change was significantly different across habitat types (agriculture fields, grasslands, and forests). Using the 2011 dataset, we investigated relationships between habitat‐specific variables and species phenology. 3. For both groups, late‐emerging species had an advanced onset on the second survey while the duration showed no consistent trend for butterflies and did not change for Orthoptera. Although the rate at which phenology changed was consistent between the two groups, at the habitat level, a longer duration of flight period emerged for butterflies in agriculture fields while Orthoptera showed no differentiation in flight duration between habitats. We found an earlier emergence of butterflies in grasslands compared to forests, attributed to habitat‐specific temperature, whereas spatial variation in humidity had a significantly lower effect on butterflies' phenology in grasslands compared to forests. A gradual delay of butterfly appearances as the canopy cover increased was also found. 4. The utility of SMA analysis was demonstrated in phenological studies and evidence was detected that both habitat type and habitat‐specific variables refine species' phenological responses.     

Forecasting phenology under global warming

As a consequence of warming temperatures around the world, spring and autumn phenologies have been shifting, with corresponding changes in the length of the growing season. Our understanding of the spatial and interspecific variation of these changes, however, is limited. Not all species are responding similarly, and there is significant spatial variation in responses even within species. This spatial and interspecific variation complicates efforts to predict phenological responses to ongoing climate change, but must be incorporated in order to build reliable forecasts. Here, we use a long-term dataset (1953–2005) of plant phenological events in spring (flowering and leaf out) and autumn (leaf colouring and leaf fall) throughout Japan and South Korea to build forecasts that account for these sources of variability. Specifically, we used hierarchical models to incorporate the spatial variability in phenological responses to temperature to then forecast species'' overall and site-specific responses to global warming. We found that for most species, spring phenology is advancing and autumn phenology is getting later, with the timing of events changing more quickly in autumn compared with the spring. Temporal trends and phenological responses to temperature in East Asia contrasted with results from comparable studies in Europe, where spring events are changing more rapidly than are autumn events. Our results emphasize the need to study multiple species at many sites to understand and forecast regional changes in phenology.     

Mismatch managed? Phenological phase extension as a strategy to manage phenological asynchrony in plant–animal mutualisms

Species‐specific shifts in phenology (timing of periodic life cycle events) are occurring with climate change and are already disrupting interactions within and among trophic levels. Phenological phase duration (e.g. beginning to end of flowering) and complementarity (patterns of nonoverlap), and their responses to changing conditions, will be important determinants of species' adaptive capacity to these shifts. Evidence indicates that extension of phenological duration of mutualistic partners could buffer negative impacts that occur with phenological shifts. Therefore, we suggest that techniques to extend the length of phenological duration will contribute to management of systems experiencing phenological asynchrony. Techniques of phenological phase extension discussed include the role of abiotic heterogeneity, genetic and species diversity, and alteration of population timing. We explore these approaches with the goal of creating a framework to build adaptive capacity and address phenological asynchrony in plant–animal mutualisms under climate change.     

Land Surface Phenology in the Tropics: The Role of Climate and Topography in a Snow-Free Mountain

Leaf phenology represents a major temporal component of ecosystem functioning, and understanding the drivers of seasonal variation in phenology is essential to understand plant responses to climate change. We assessed the patterns and drivers of land surface phenology, a proxy for leafing phenology, for the meridional Espinhaço Range, a South American tropical mountain comprising a mosaic of savannas, dry woodlands, montane vegetation and moist forests. We used a 14-year time series of MODIS/NDVI satellite images, acquired between 2001 and 2015, and extracted phenological indicators using the TIMESAT algorithm. We obtained precipitation data from the Tropical Rainfall Measuring Mission, land surface temperature from the MODIS MOD11A2 product, and cloud cover frequency from the MODIS MOD09GA product. We also calculated the topographic wetness index and simulated clear-sky radiation budgets based on the SRTM elevation model. The relationship between phenology and environmental drivers was assessed using general linear models. Temporal displacement in the start date of the annual growth season was more evident than variations in season length among vegetation types, indicating a possible temporal separation in the use of resources. Season length was inversely proportional to elevation, decreasing 1.58 days per 100 m. Green-up and senescence rates were faster where annual temperature amplitude was higher. We found that water and light availability, modulated by topography, are the most likely drivers of land surface phenology in the region, determining the start, end and length of the growing season. Temperature had an important role in determining the rates of leaf development and the strength of vegetation seasonality, suggesting that tropical vegetation is also sensitive to latitudinal temperature changes, regardless of the elevational gradient. Our work improves the current understanding of phenological strategies in the seasonal tropics and emphasizes the importance of topography in shaping light and water availability for leaf development in snow-free mountains.     

植物物候学研究进展

植物物候变化在研究陆地生态系统对气候变化的响应时被誉为"矿井中的金丝雀",全球气候变化愈演愈烈,重新引起了人们对植物物候研究的广泛关注。随着观测技术的发展,在各种空间和生态尺度上收集到的物候观测数据迅速累积,尽管已经在多个尺度上（物种、群落和景观尺度）观察到物候变化,但物候变化的机理仍然没有得到很好的理解。回顾了国内外植物物候研究的发展历程;总结了物候数据收集技术进展和全球物候变化的主要趋势;归纳了植物物候变化的机理与驱动因素;探讨了物候模型研究及物候对气候变化响应研究的主要方向。随着物候观测技术在不同尺度上应用的增加,物候研究进入了一个新的阶段。未来物候研究需要制定跨区域标准化观测指南,融合所有相关学科,改进物候模型,拓展研究区域;同时融合有效的历史物候资料,采用新技术和长期收集的物候数据为大数据时代植物物候学研究提供基础。