▪ Abstract The pollination of flowering plants by animals represents a critical ecosystem service of great value to humanity, both monetary and otherwise. However, the need for active conservation of pollination interactions is only now being appreciated. Pollination systems are under increasing threat from anthropogenic sources, including fragmentation of habitat, changes in land use, modern agricultural practices, use of chemicals such as pesticides and herbicides, and invasions of non-native plants and animals. Honeybees, which themselves are non-native pollinators on most continents, and which may harm native bees and other pollinators, are nonetheless critically important for crop pollination. Recent declines in honeybee numbers in the United States and Europe bring home the importance of healthy pollination systems, and the need to further develop native bees and other animals as crop pollinators. The “pollination crisis” that is evident in declines of honeybees and native bees, and in damage to webs of plant-pollinator interaction, may be ameliorated not only by cultivation of a diversity of crop pollinators, but also by changes in habitat use and agricultural practices, species reintroductions and removals, and other means. In addition, ecologists must redouble efforts to study basic aspects of plant-pollinator interactions if optimal management decisions are to be made for conservation of these interactions in natural and agricultural ecosystems.
The timing of life history traits is central to lifetime fitness and nowhere is this more evident or well studied as in the phenology of flowering in governing plant reproductive success. Recent changes in the timing of environmental events attributable to climate change, such as the date of snowmelt at high altitudes, which initiates the growing season, have had important repercussions for some common perennial herbaceous wildflower species. The phenology of flowering at the Rocky Mountain Biological Laboratory (Colorado, USA) is strongly influenced by date of snowmelt, which makes this site ideal for examining phenological responses to climate change. Flower buds of Delphinium barbeyi, Erigeron speciosus, and Helianthella quinquenervis are sensitive to frost, and the earlier beginning of the growing season in recent years has exposed them to more frequent mid-June frost kills. From 1992 to 1998, on average 36.1% of Helianthella buds were frosted, but for 1999-2006 the mean is 73.9%; in only one year since 1998 have plants escaped all frost damage. For all three of these perennial species, there is a significant relationship between the date of snowmelt and the abundance of flowering that summer. Greater snowpack results in later snowmelt, later beginning of the growing season, and less frost mortality of buds. Microhabitat differences in snow accumulation, snowmelt patterns, and cold air drainage during frost events can be significant; an elevation difference of only 12 m between two plots resulted in a temperature difference of almost 2 degrees C in 2006 and a difference of 37% in frost damage to buds. The loss of flowers and therefore seeds can reduce recruitment in these plant populations, and affect pollinators, herbivores, and seed predators that previously relied on them. Other plant species in this environment are similarly susceptible to frost damage so the negative effects for recruitment and for consumers dependent on flowers and seeds could be widespread. These findings point out the paradox of increased frost damage in the face of global warming, provide important insights into the adaptive significance of phenology, and have general implications for flowering plants throughout the region and anywhere climate change is having similar impacts.
Shifts in the timing of spring phenology are a central feature of global change research. Long-term observations of plant phenology have been used to track vegetation responses to climate variability but are often limited to particular species and locations and may not represent synoptic patterns. Satellite remote sensing is instead used for continental to global monitoring. Although numerous methods exist to extract phenological timing, in particular start-of-spring (SOS), from time series of reflectance data, a comprehensive intercomparison and interpretation of SOS methods has not been conducted. Here, we assess 10 SOS methods for North America between 1982 and 2006. The techniques include consistent inputs from the 8 km Global Inventory Modeling and Mapping Studies Advanced Very High Resolution Radiometer NDVIg dataset, independent data for snow cover, soil thaw, lake ice dynamics, spring streamflow timing, over 16 000 individual measurements of ground-based phenology, and two temperature-driven models of spring phenology. Compared with an ensemble of the 10 SOS methods, we found that individual methods differed in average day-of-year estimates by AE 60 days and in standard deviation by AE 20 days. The ability of the satellite methods to retrieve SOS estimates was highest in northern latitudes and lowest in arid, tropical, and Mediterranean ecoregions. The ordinal rank of SOS methods varied geographically, as did the relationships between SOS estimates and the cryospheric/hydrologic metrics. Compared with ground observations, SOS estimates were more related to the first leaf and first flowers expanding phenological stages. We found no evidence for time trends in spring arrival from ground-or model-based data; using an ensemble estimate from two methods that were more closely related to ground observations than other methods, SOS Correspondence: Michael A. White, tel. 1 1 435 797 3794, fax 1 1 435 797 187, trends could be detected for only 12% of North America and were divided between trends towards both earlier and later spring.
Phenology-the timing of biological events-is highly sensitive to climate change. However, our general understanding of how phenology responds to climate change is based almost solely on incomplete assessments of phenology (such as first date of flowering) rather than on entire phenological distributions. Using a uniquely comprehensive 39-y flowering phenology dataset from the Colorado Rocky Mountains that contains more than 2 million flower counts, we reveal a diversity of species-level phenological shifts that bring into question the accuracy of previous estimates of long-term phenological change. For 60 species, we show that first, peak, and last flowering rarely shift uniformly and instead usually shift independently of one another, resulting in a diversity of phenological changes through time. Shifts in the timing of first flowering on average overestimate the magnitude of shifts in the timing of peak flowering, fail to predict shifts in the timing of last flowering, and underrepresent the number of species changing phenology in this plant community. Ultimately, this diversity of species-level phenological shifts contributes to altered coflowering patterns within the community, a redistribution of floral abundance across the season, and an expansion of the flowering season by more than I mo during the course of our study period. These results demonstrate the substantial reshaping of ecological communities that can be attributed to shifts in phenology.growing season | no-analogue community | phenological mismatch | phenology curve | species interactions P henology, the timing of biological events, is intimately tied to the reproduction and survival of organisms (1). Phenological events generally are occurring earlier in temperate environments in accordance with climate change, although several recent studies have emphasized species-specificity in the direction and magnitude of change (2-5). The great majority of these longterm datasets contain a single measure of phenology for individual species, most often the first day on which a biological event is observed (i.e., "phenological firsts" such as first flowering) (Fig. 1A). In addition to phenological firsts, basic components of an entire phenological response include the timing of the ending of a biological event and details of intermediate stages, such as the timing and magnitude of peak abundance or activity (Fig. 1A). Given that phenological firsts represent the early tail of a population-level response, most assessments of phenological change to date may provide an incomplete view of the magnitude of change, the number of responsive species, and how species-level shifts contribute to change at higher levels of biological organization.We have amassed a unique long-term record of flowering phenology that allows us to investigate complete phenological responses for a plant community. Over a 39-y period , we have sampled a montane site (2,900 m elevation) in Colorado, USA, counting the total number of flowers of 121 plant species across a series of permanent...
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.
Climate change is altering the phenology of species across the world, but what are the consequences of these phenological changes for the demography and population dynamics of species? Time-sensitive relationships, such as migration, breeding and predation, may be disrupted or altered, which may in turn alter the rates of reproduction and survival, leading some populations to decline and others to increase in abundance. However, finding evidence for disrupted relationships, or lack thereof, and their demographic effects, is difficult because the necessary detailed observational data are rare. Moreover, we do not know how sensitive species will generally be to phenological mismatches when they occur. Existing long-term studies provide preliminary data for analysing the phenology and demography of species in several locations. In many instances, though, observational protocols may need to be optimized to characterize timing-based multi-trophic interactions. As a basis for future research, we outline some of the key questions and approaches to improving our understanding of the relationships among phenology, demography and climate in a multi-trophic context. There are many challenges associated with this line of research, not the least of which is the need for detailed, long-term data on many organisms in a single system. However, we identify key questions that can be addressed with data that already exist and propose approaches that could guide future research.
Calendar date of the beginning of the growing season at high altitude in the Colorado Rocky Mountains is variable but has not changed significantly over the past 25 years. This result differs from growing evidence from low altitudes that climate change is resulting in a longer growing season, earlier migrations, and earlier reproduction in a variety of taxa. At our study site, the beginning of the growing season is controlled by melting of the previous winter's snowpack. Despite a trend for warmer spring temperatures the average date of snowmelt has not changed, perhaps because of the trend for increased winter precipitation. This disjunction between phenology at low and high altitudes may create problems for species, such as many birds, that migrate over altitudinal gradients. We present data indicating that this already may be true for American robins, which are arriving 14 days earlier than they did in 1981; the interval between arrival date and the first date of bare ground has grown by 18 days. We also report evidence for an effect of climate change on hibernation behavior; yellow-bellied marmots are emerging 38 days earlier than 23 years ago, apparently in response to warmer spring air temperatures. Migrants and hibernators may experience problems as a consequence of these changes in phenology, which may be exacerbated if climate models are correct in their predictions of increased winter snowfall in our study area. The trends we report for earlier formation of permanent snowpack and for a longer period of snow cover also have implications for hibernating species. In high mountains, such as the Colorado Rocky Mountains, there is a short, but active, growing season during which resources are abundant and temperatures mild. In contrast, there is a very long winter when the ground is covered with deep snow and temperatures can reach Ϫ40°C. Animal species in this environment have evolved various responses to the onset of winter, during which snow may cover the ground for more than 7 months. One set of species has adopted hibernation as a way to conserve energy during the time when food is unavailable (e.g., marmots, ground squirrels, chipmunks), and another set migrates to more favorable climates at lower altitudes or lower latitudes (e.g., elk, deer, birds). Climate change may pose special challenges to some of these species if it results in changes in the length of the summer or winter seasons or if the cues used by migrants at different altitudes between their winter and summer grounds change their synchrony.A growing body of evidence suggests that climate change is affecting the phenology (seasonal timing) of animal and plant activity at low altitudes. For example, long-term studies in England have documented the earlier arrival of migratory birds (1), earlier reproduction by amphibians (2) and birds (3, 4), earlier breaking of leaf buds (5), and changes in moth phenology (6). There are fewer published studies to date about similar changes in North America, but one report documents earlier egg laying by tr...
JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact support@jstor.org.. Ecological Society of America is collaborating with JSTOR to digitize, preserve and extend access to Ecology.There is some confusion in the terminology of pollination ecology used to describe the way flower visitors collect nectar. Although the concepts involved are relatively distinct, and the distinction has been noted in the literature, there remains some overlap in the use of particular terms. The purpose of this paper is to propose a means of separating these concepts in the future.We can consider "flower visitor" to be the most general in a hierarchy of terms describing animals which visit flowers. A flower visitor may also be, but is not necessarily, a pollinator. The terms "legitimate" and "illegitimate" have also been used to distinguish flower visitors on flowers for which they appear to be adapted (legitimate visitors) or unadapted (illegitimate). The remainder of this discussion concerns flower visitors which generally are not pollinators. The next level of refinement was suggested by Faegri and Van der PijI (1966:78): "The distinction between simple theft and house-breaking exists in pollination ecology, too; thieves that cannot creep into the flower and steal nectar that way, may bite a hole through the perianth and get at it from the outside." Although they indicated the difference between simple theft and housebreaking, they did not suggest a corresponding dichotomy in terminology. The term nectar robbing is perhaps most appropriately used to describe the situation in which force is used, while nectar thieving or nectar theft, which do not imply the use of force, are best reserved for situations in which holes are not made in the flowers.Nectar robbing is generally accomplished by making a hole in a sympetalous corolla, allowing the flower visitor to obtain nectar more directly from the nectary than is possible for pollinators which visit the flower "legitimately," in the fashion for which it seems to have evolved. This hole can be made in a variety of ways, including piercing by the beaks of birds (Ingels 1976, Inouye 1981, McDade and Kinsman 1980), biting by the mandibles of bumblebees or ants (Rust 1979, Inouye 1981), and slicing by the proboscis of carpenter bees (Schremmer 1972). A further distinction can be made between primary and secondary
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