Challenging claims in the study of migratory birds and climate change

Recent shifts in phenology in response to climate change are well established but often poorly understood. Many animals integrate climate change across a spatially and temporally dispersed annual life cycle, and effects are modulated by ecological interactions, evolutionary change and endogenous control mechanisms. Here we assess and discuss key statements emerging from the rapidly developing study of changing spring phenology in migratory birds. These well‐studied organisms have been instrumental for understanding climate‐change effects, but research is developing rapidly and there is a need to attack the big issues rather than risking affirmative science. Although we agree poorly on the support for most claims, agreement regarding the knowledge basis enables consensus regarding broad patterns and likely causes. Empirical data needed for disentangling mechanisms are still scarce, and consequences at a population level and on community composition remain unclear. With increasing knowledge, the overall support (‘consensus view’) for a claim increased and between‐researcher variability in support (‘expert opinions') decreased, indicating the importance of assessing and communicating the knowledge basis. A proper integration across biological disciplines seems essential for the field's transition from affirming patterns to understanding mechanisms and making robust predictions regarding future consequences of shifting phenologies.     

The impacts of climate change on the annual cycles of birds

Organisms living today are descended from ancestors that experienced considerable climate change in the past. However, they are currently presented with many new, man-made challenges, including rapid climate change. Migration and reproduction of many avian species are controlled by endogenous mechanisms that have been under intense selection over time to ensure that arrival to and departure from breeding grounds is synchronized with moderate temperatures, peak food availability and availability of nesting sites. The timing of egg laying is determined, usually by both endogenous clocks and local factors, so that food availability is near optimal for raising young. Climate change is causing mismatches in food supplies, snow cover and other factors that could severely impact successful migration and reproduction of avian populations unless they are able to adjust to new conditions. Resident (non-migratory) birds also face challenges if precipitation and/or temperature patterns vary in ways that result in mismatches of food and breeding. Predictions that many existing climates will disappear and novel climates will appear in the future suggest that communities will be dramatically restructured by extinctions and changes in range distributions. Species that persist into future climates may be able to do so in part owing to the genetic heritage passed down from ancestors who survived climate changes in the past.     

Phenology of British butterflies and climate change

Data from a national butterfly monitoring scheme were analysed to test for relationships between temperature and three phenological measures, duration of flight period and timing of both first and peak appearance. First appearances of most British butterflies has advanced in the last two decades and is strongly related to earlier peak appearance and, for multibrooded species, longer flight period. Mean dates of first and peak appearance are examined in relation to Manley's central England temperatures, using regression techniques. We predict that, in the absence of confounding factors, such as interactions with other organisms and land‐use change, climate warming of the order of 1 °C could advance first and peak appearance of most butterflies by 2–10 days.     

Impact of climate change on migratory birds: community reassembly versus adaptation

Aim Species can respond to global climate change by range shifts or by phenotypic adaptation. At the community level, range shifts lead to a turnover of species, i.e. community reassembly. In contrast, phenotypic adaptation allows species to persist in situ, conserving community composition. So far, community reassembly and adaptation have mostly been studied separately. In nature, however, both processes take place simultaneously. In migratory birds, climate change has been shown to result in both exchange of species and adaptation of migratory behaviour. The aim of our study is to predict the impact of global climate change on migratory bird communities and to assess the extent to which reassembly and adaptation may contribute to alterations. Location Europe. Methods We analysed the relationship between current climate and the proportion of migratory species across bird assemblages in Europe. The magnitude of community reassembly was measured using spatial variation in the proportion of potentially migratory species. Adaptation was inferred from spatial variation in the proportion of potentially migratory species that actually migrate at a specific site. These spatial relationships were used to make temporal predictions of changes in migratory species under global climate change. Results According to our models, increasing winter temperature is expected to lead to declines in the proportion of migratory species, whereas increasing spring temperature and decreasing spring precipitation may lead to increases. Changes in winter and spring temperature are expected to cause mainly adaptation in migratory activity, while changes in spring precipitation may result in both changes in the proportion of potentially migratory species and adaptation of migratory activity. Main conclusions Under current climate change forecasts, changes in the proportion of migratory species will be modest and the communities of migratory birds in Europe are projected to be altered through adaptation of migratory activity rather than through exchange of species.     

Phenotypic plasticity and adaptive evolution contribute to advancing flowering phenology in response to climate change

Anthropogenic climate change has already altered the timing of major life-history transitions, such as the initiation of reproduction. Both phenotypic plasticity and adaptive evolution can underlie rapid phenological shifts in response to climate change, but their relative contributions are poorly understood. Here, we combine a continuous 38 year field survey with quantitative genetic field experiments to assess adaptation in the context of climate change. We focused on Boechera stricta (Brassicaeae), a mustard native to the US Rocky Mountains. Flowering phenology advanced significantly from 1973 to 2011, and was strongly associated with warmer temperatures and earlier snowmelt dates. Strong directional selection favoured earlier flowering in contemporary environments (2010-2011). Climate change could drive this directional selection, and promote even earlier flowering as temperatures continue to increase. Our quantitative genetic analyses predict a response to selection of 0.2 to 0.5 days acceleration in flowering per generation, which could account for more than 20 per cent of the phenological change observed in the long-term dataset. However, the strength of directional selection and the predicted evolutionary response are likely much greater now than even 30 years ago because of rapidly changing climatic conditions. We predict that adaptation will likely be necessary for long-term in situ persistence in the context of climate change.     

Keeping up with a warming world; assessing the rate of adaptation to climate change

The pivotal question in the debate on the ecological effects of climate change is whether species will be able to adapt fast enough to keep up with their changing environment. If we establish the maximal rate of adaptation, this will set an upper limit to the rate at which temperatures can increase without loss of biodiversity.The rate of adaptation will primarily be set by the rate of microevolution since (i) phenotypic plasticity alone is not sufficient as reaction norms will no longer be adaptive and hence microevolution on the reaction norm is needed, (ii) learning will be favourable to the individual but cannot be passed on to the next generations, (iii) maternal effects may play a role but, as with other forms of phenotypic plasticity, the response of offspring to the maternal cues will no longer be adaptive in a changing environment, and (iv) adaptation via immigration of individuals with genotypes adapted to warmer environments also involves microevolution as these genotypes are better adapted in terms of temperature, but not in terms of, for instance, photoperiod.Long-term studies on wild populations with individually known animals play an essential role in detecting and understanding the temporal trends in life-history traits, and to estimate the heritability of, and selection pressures on, life-history traits. However, additional measurements on other trophic levels and on the mechanisms underlying phenotypic plasticity are needed to predict the rate of microevolution, especially under changing conditions.Using this knowledge on heritability of, and selection on, life-history traits, in combination with climate scenarios, we will be able to predict the rate of adaptation for different climate scenarios. The final step is to use ecoevolutionary dynamical models to make the link to population viability and from there to biodiversity loss for those scenarios where the rate of adaptation is insufficient.     

Impact of climate change on risk of incursion of Crimean-Congo haemorrhagic fever virus in livestock in Europe through migratory birds

Aims: To predict the risk of incursion of Crimean‐Congo haemorrhagic fever virus (CCHFV) in livestock in Europe introduced through immature Hyalomma marginatum ticks on migratory birds under current conditions and in the decade 2075–2084 under a climate‐change scenario. Methods and Results: A spatial risk map of Europe comprising 14 282 grid cells (25 × 25 km) was constructed using three data sources: (i) ranges and abundances of four species of bird which migrate from sub‐Saharan Africa to Europe each spring, namely Willow warbler (Phylloscopus trochilus), Northern wheatear (Oenanthe oenanthe), Tree pipit (Anthus trivialis) and Common quail (Coturnix coturnix); (ii) UK Met Office HadRM3 spring temperatures for prediction of moulting success of immature H. marginatum ticks and (iii) livestock densities. On average, the number of grid cells in Europe predicted to have at least one CCHFV incursion in livestock in spring was 1·04 per year for the decade 2005–2014 and 1·03 per year for the decade 2075–2084. In general with the assumed climate‐change scenario, the risk increased in northern Europe but decreased in central and southern Europe, although there is considerable local variation in the trends. Conclusions: The absolute risk of incursion of CCHFV in livestock through ticks introduced by four abundant species of migratory bird (totalling 120 million individual birds) is very low. Climate change has opposing effects, increasing the success of the moult of the nymphal ticks into adults but decreasing the projected abundance of birds by 34% in this model. Significance and Impact of the Study: For Europe, climate change is not predicted to increase the overall risk of incursion of CCHFV in livestock through infected ticks introduced by these four migratory bird species.     

气候变化对鸟类影响的研究进展

气候变化对生物多样性的影响已成为热点问题.本文以鸟类为研究对象,根据鸟类受气候变化影响的最新研究成果,综述了气候变化对鸟类的分布、物候和种群等方面的影响.结果表明,在气候变化影响下,鸟类分布向高纬度或高海拔区移动,速度比以往加快,繁殖地和非繁殖地的分布移动变化并不相同,并且多数分布范围缩小,物候期发生复杂变化,种群数量下降明显.文章还讨论了该领域主要的预测和评估方法,以及进化适应等生物因素对气候变化预测结果的影响,除了以往单一的相关性模型外,目前应用最多的是集成模型,而未来最具发展潜力的是机理模型.进化适应方面的研究近来取得新进展,证实了生物个体积极应对气候变化影响的事实,从而对人为模型预测的准确性带来挑战.文章最后进行了总结和展望,结合国外研究经验和我国实际情况,提出一些建议:由于气候变化的影响及其研究是长期性的,从而对鸟类的历史监测数据提出很高的要求,当前我国急需建立一套长期、全面和可靠的鸟类数据监测系统;此外,人们需要综合评估现有各种预测模型的可靠性,在此基础上探索新的研究方法.     

Identification of a gene associated with avian migratory behaviour

Bird migration is one of the most spectacular and best-studied phenomena in behavioural biology. Yet, while the patterns of variation in migratory behaviour and its ecological causes have been intensively studied, its genetic, physiological and neurological control remains poorly understood. The lack of knowledge of the molecular basis of migration is currently not only limiting our insight into the proximate control of migration, but also into its evolution. We investigated polymorphisms in the exons of six candidate genes for key behavioural traits potentially linked to migration, which had previously been identified in several bird species, and eight control loci in 14 populations of blackcaps (Sylvia atricapilla), representing the whole range of geographical variation in migration patterns found in this species, with the aim of identifying genes controlling variation in migration. We found a consistent association between a microsatellite polymorphism and migratory behaviour only at one candidate locus: the ADCYAP1 gene. This polymorphism explained about 2.6 per cent of the variation in migratory tendency among populations, and 2.7-3.5% of variation in migratory restlessness among individuals within two independent populations. In all tests, longer alleles were associated with higher migratory activity. The consistency of results among different populations and levels of analysis suggests that ADCYAP1 is one of the genes controlling the expression of migratory behaviour. Moreover, the multiple described functions of the gene product indicate that this gene might act at multiple levels modifying the shift between migratory and non-migratory states.     

Rainfall-induced changes in food availability modify the spring departure programme of a migratory bird

Climatic warming has intensified selection for earlier reproduction in many organisms, but potential constraints imposed by climate change outside the breeding period have received little attention. Migratory birds provide an ideal model for exploring such constraints because they face warming temperatures on temperate breeding grounds and declining rainfall on many tropical non-breeding areas. Here, we use longitudinal data on spring departure dates of American redstarts (Setophaga ruticilla) to show that annual variation in tropical rainfall and food resources are associated with marked change in the timing of spring departure of the same individuals among years. This finding challenges the idea that photoperiod alone regulates the onset of migration, providing evidence that intensifying drought in the tropical winter could hinder adaptive responses to climatic warming in the temperate zone.     

Leaf morphology shift linked to climate change

Climate change is driving adaptive shifts within species, but research on plants has been focused on phenology. Leaf morphology has demonstrated links with climate and varies within species along climate gradients. We predicted that, given within-species variation along a climate gradient, a morphological shift should have occurred over time due to climate change. We tested this prediction, taking advantage of latitudinal and altitudinal variations within the Adelaide Geosyncline region, South Australia, historical herbarium specimens (n = 255) and field sampling (n = 274). Leaf width in the study taxon, Dodonaea viscosa subsp. angustissima, was negatively correlated with latitude regionally, and leaf area was negatively correlated with altitude locally. Analysis of herbarium specimens revealed a 2 mm decrease in leaf width (total range 1-9 mm) over 127 years across the region. The results are consistent with a morphological response to contemporary climate change. We conclude that leaf width is linked to maximum temperature regionally (latitude gradient) and leaf area to minimum temperature locally (altitude gradient). These data indicate a morphological shift consistent with a direct response to climate change and could inform provenance selection for restoration with further investigation of the genetic basis and adaptive significance of observed variation.     

Circadian flight schedules in night-migrating birds caught on migration

Many species of migratory birds migrate in a series of solitary nocturnal flights. Between flights, they stop to rest and refuel for the next segment of their journey. The mechanism controlling this behaviour has long remained elusive. Here, we show that wild-caught migratory redstarts (Phoenicurus phoenicurus) are consistent in their flight scheduling. An advanced videographic system enabled us to determine the precise timing of flight activity in redstarts caught at a northern European stopover site during their return trip from Africa. Birds were held captive for three days in the absence of photoperiodic cues (constant dim light) and under permanent food availability. Despite the absence of external temporal cues, birds showed clear bimodal activity patterns: intense nocturnal activity alternating with diurnal foraging and resting periods. The onset of their migratory activity coincided with the time of local sunset and was individually consistent on consecutive nights. The data demonstrate that night-migrating birds are driven by autonomous circadian clocks entrained by sunset cues. This timekeeping system is probably the key factor in the overall control of nocturnal songbird migration.     

Modeling nonbreeding distributions of shorebirds and waterfowl in response to climate change

To identify areas on the landscape that may contribute to a robust network of conservation areas, we modeled the probabilities of occurrence of several en route migratory shorebirds and wintering waterfowl in the southern Great Plains of North America, including responses to changing climate. We predominantly used data from the eB ird citizen‐science project to model probabilities of occurrence relative to land‐use patterns, spatial distribution of wetlands, and climate. We projected models to potential future climate conditions using five representative general circulation models of the Coupled Model Intercomparison Project 5 (CMIP 5). We used Random Forests to model probabilities of occurrence and compared the time periods 1981–2010 (hindcast) and 2041–2070 (forecast) in “model space.” Projected changes in shorebird probabilities of occurrence varied with species‐specific general distribution pattern, migration distance, and spatial extent. Species using the western and northern portion of the study area exhibited the greatest likelihoods of decline, whereas species with more easterly occurrences, mostly long‐distance migrants, had the greatest projected increases in probability of occurrence. At an ecoregional extent, differences in probabilities of shorebird occurrence ranged from ?0.015 to 0.045 when averaged across climate models, with the largest increases occurring early in migration. Spatial shifts are predicted for several shorebird species. Probabilities of occurrence of wintering Mallards and Northern Pintail are predicted to increase by 0.046 and 0.061, respectively, with northward shifts projected for both species. When incorporated into partner land management decision tools, results at ecoregional extents can be used to identify wetland complexes with the greatest potential to support birds in the nonbreeding season under a wide range of future climate scenarios.     

Climate variability slows evolutionary responses of Colias butterflies to recent climate change

How does recent climate warming and climate variability alter fitness, phenotypic selection and evolution in natural populations? We combine biophysical, demographic and evolutionary models with recent climate data to address this question for the subalpine and alpine butterfly, Colias meadii, in the southern Rocky Mountains. We focus on predicting patterns of selection and evolution for a key thermoregulatory trait, melanin (solar absorptivity) on the posterior ventral hindwings, which affects patterns of body temperature, flight activity, adult and egg survival, and reproductive success in Colias. Both mean annual summer temperatures and thermal variability within summers have increased during the past 60 years at subalpine and alpine sites. At the subalpine site, predicted directional selection on wing absorptivity has shifted from generally positive (favouring increased wing melanin) to generally negative during the past 60 years, but there is substantial variation among years in the predicted magnitude and direction of selection and the optimal absorptivity. The predicted magnitude of directional selection at the alpine site declined during the past 60 years and varies substantially among years, but selection has generally been positive at this site. Predicted evolutionary responses to mean climate warming at the subalpine site since 1980 is small, because of the variability in selection and asymmetry of the fitness function. At both sites, the predicted effects of adaptive evolution on mean population fitness are much smaller than the fluctuations in mean fitness due to climate variability among years. Our analyses suggest that variation in climate within and among years may strongly limit evolutionary responses of ectotherms to mean climate warming in these habitats.     

The impact of climate change on the geographical distribution of two vectors of Chagas disease: implications for the force of infection

Chagas disease, caused by the parasite Trypanosoma cruzi, is the most important vector-borne disease in Latin America. The vectors are insects belonging to the Triatominae (Hemiptera, Reduviidae), and are widely distributed in the Americas. Here, we assess the implications of climatic projections for 2050 on the geographical footprint of two of the main Chagas disease vectors: Rhodnius prolixus (tropical species) and Triatoma infestans (temperate species). We estimated the epidemiological implications of current to future transitions in the climatic niche in terms of changes in the force of infection (FOI) on the rural population of two countries: Venezuela (tropical) and Argentina (temperate). The climatic projections for 2050 showed heterogeneous impact on the climatic niches of both vector species, with a decreasing trend of suitability of areas that are currently at high-to-moderate transmission risk. Consequently, climatic projections affected differently the FOI for Chagas disease in Venezuela and Argentina. Despite the heterogeneous results, our main conclusions point out a decreasing trend in the number of new cases of Tr. cruzi human infections per year between current and future conditions using a climatic niche approach.     

A demographic approach to study effects of climate change in desert plants

Desert species respond strongly to infrequent, intense pulses of precipitation. Consequently, indigenous flora has developed a rich repertoire of life-history strategies to deal with fluctuations in resource availability. Examinations of how future climate change will affect the biota often forecast negative impacts, but these—usually correlative—approaches overlook precipitation variation because they are based on averages. Here, we provide an overview of how variable precipitation affects perennial and annual desert plants, and then implement an innovative, mechanistic approach to examine the effects of precipitation on populations of two desert plant species. This approach couples robust climatic projections, including variable precipitation, with stochastic, stage-structured models constructed from long-term demographic datasets of the short-lived Cryptantha flava in the Colorado Plateau Desert (USA) and the annual Carrichtera annua in the Negev Desert (Israel). Our results highlight these populations'' potential to buffer future stochastic precipitation. Population growth rates in both species increased under future conditions: wetter, longer growing seasons for Cryptantha and drier years for Carrichtera. We determined that such changes are primarily due to survival and size changes for Cryptantha and the role of seed bank for Carrichtera. Our work suggests that desert plants, and thus the resources they provide, might be more resilient to climate change than previously thought.     

Phenological response to climate change in China: a meta‐analysis

The change in the phenology of plants or animals reflects the response of living systems to climate change. Numerous studies have reported a consistent earlier spring phenophases in many parts of middle and high latitudes reflecting increasing temperatures with the exception of China. A systematic analysis of Chinese phenological response could complement the assessment of climate change impact for the whole Northern Hemisphere. Here, we analyze 1263 phenological time series (1960–2011, with 20+ years data) of 112 species extracted from 48 studies across 145 sites in China. Taxonomic groups include trees, shrubs, herbs, birds, amphibians and insects. Results demonstrate that 90.8% of the spring/summer phenophases time series show earlier trends and 69.0% of the autumn phenophases records show later trends. For spring/summer phenophases, the mean advance across all the taxonomic groups was 2.75 days decade^?1 ranging between 2.11 and 6.11 days decade^?1 for insects and amphibians, respectively. Herbs and amphibians show significantly stronger advancement than trees, shrubs and insect. The response of phenophases of different taxonomic groups in autumn is more complex: trees, shrubs, herbs and insects show a delay between 1.93 and 4.84 days decade^?1, while other groups reveal an advancement ranging from 1.10 to 2.11 days decade^?1. For woody plants (including trees and shrubs), the stronger shifts toward earlier spring/summer were detected from the data series starting from more recent decades (1980s–2000s). The geographic factors (latitude, longitude and altitude) could only explain 9% and 3% of the overall variance in spring/summer and autumn phenological trends, respectively. The rate of change in spring/summer phenophase of woody plants (1960s–2000s) generally matches measured local warming across 49 sites in China (R = ?0.33, P < 0.05).     

黄河流域2001-2020年植被物候及其对气候变化的响应

植被周期性的物候更替被公认为是全球气候变化的综合指示器,深入研究区域植被物候的变化趋势和时空特征,可以提高对该区生态系统稳定性及动态变化程度的认识。基于2001-2020年16天、250m分辨率的中分辨率成像光谱仪归一化植被指数（MODIS NDVI）数据,利用Savitzky-Golay滤波法（S-G）和相对阈值法提取黄河流域植被物候参数,结合谷歌地球引擎（GEE）平台提供的欧洲中期天气预报中心第五代陆地再分析数据集（ERA5-LAND）小时气候再分析数据集和气候危害组红外降水站数据（CHIRPS）日降水数据集数据,运用趋势分析和偏相关分析等方法,探究全球气候变化下黄河流域不同植被分区物候参数空间分布特征、变化趋势,及其对气候因子的响应。结果表明：（1）2001-2020年黄河流域气候整体呈暖湿化的发展趋势,年均温上升幅度为0.15℃/10a（P>0.05）,年降水增加幅度为24mm/10a（P<0.05）。（2）黄河流域暖温带落叶阔叶林区域的生长季始期和中期最早,温带南部典型草原亚地带和温带南部荒漠草原亚地带最晚,温带灌木、禾草半荒漠亚地带的生长季结束期最晚,青藏高原高寒植被区域的生长季长度最短。（3）全流域内生长季始期和中期分别有69.3%和66.4%的面积呈提前趋势（P<0.05）,生长季末期50.9%的面积结束期呈推迟趋势（P<0.05）,66.1%的面积整个生长季长度呈延长趋势（P<0.05）。（4）不同植被地带气候对物候参数影响存在差异,温度因子对带北部典型草原亚地带、高寒草原地带和高寒草甸地带的物候参数影响较大,降水和太阳辐射因子对温带南部典型草原亚地带、温带灌木、禾草半荒漠地带、温带南部荒漠草原亚地带和中亚热带常绿阔叶林地带的物候参数影响较大。     

The importance of phylogeny to the study of phenological response to global climate change

Climate change has resulted in major changes in the phenology—i.e. the timing of seasonal activities, such as flowering and bird migration—of some species but not others. These differential responses have been shown to result in ecological mismatches that can have negative fitness consequences. However, the ways in which climate change has shaped changes in biodiversity within and across communities are not well understood. Here, we build on our previous results that established a link between plant species'' phenological response to climate change and a phylogenetic bias in species'' decline in the eastern United States. We extend a similar approach to plant and bird communities in the United States and the UK that further demonstrates that climate change has differentially impacted species based on their phylogenetic relatedness and shared phenological responses. In plants, phenological responses to climate change are often shared among closely related species (i.e. clades), even between geographically disjunct communities. And in some cases, this has resulted in a phylogenetically biased pattern of non-native species success. In birds, the pattern of decline is phylogenetically biased but is not solely explained by phenological response, which suggests that other traits may better explain this pattern. These results illustrate the ways in which phylogenetic thinking can aid in making generalizations of practical importance and enhance efforts to predict species'' responses to future climate change.