Phenology as a tool to link ecology and sustainable decision making in a dynamic environment
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Symposium 14, 94th Ecological Society of America Meeting, Albuquerque, New Mexico, USA, August 2009
Adaptation to climate change (i.e. actions that reduce negative and enhance positive climate impacts) is one of the most pressing issues of our time, from both human and ecological perspectives. Recent rapid changes have already affected the availability of water, the frequency and extent of wildfire, the persistence and distribution of species, the availability of nutrients, and many other ecological and physical processes (IPCC, 2007). At the 2009 annual meeting of the Ecological Society of America, a symposium entitled ‘Phenology, the Interdisciplinary Canary: Linkages between Ecology and Sustainable Decision Making in a Dynamic Environment’http://eco.confex.com/eco/2009/techprogram/S4149.HTM highlighted the ubiquitous role that phenology plays in many of these responses to climate change and described how phenology data can improve our ability to make management decisions in the face of climate change.
‘…the strength of a species’ phenological response to variations in climate might in fact indicate its vulnerability to climate change…’
The utility and ubiquity of phenology
Phenology is the study of seasonal recurring plant and animal life cycle stages, or phenophases, such as leafing and flowering of plants, maturation of agricultural crops, emergence of insects and migration of birds. The role of phenology in the structure and function of ecological systems is often underappreciated, but its importance is magnified by climate change. Shifts in phenology are among the most sensitive biological responses to climate change (Parmesan, 2007). They occur across trophic levels and are observable at local to global scales. Moreover, changes in the timing of phenological events have widespread impacts on ecological and biophysical processes. Nearly every ecological relationship and process depends on timing to some degree, often to a very large degree – viz., pollination, predation, competition, niche differentiation and primary productivity (Stenseth & Mysterud, 2002). In addition, the phenology of many organisms is plastic and integrates many climate variables, including temperature, precipitation, wind, day-length and even atmospheric concentrations of carbon dioxide. Thus, phenological data contain not just information about organismal timing, but also information about environmental variables.
Taken together, the ability of phenology to integrate climate variables, its ubiquitous role in ecological and physical responses to climate change, and the ease with which it can be observed, make phenological data a critical tool for improving our understanding of ecological processes and for managing resources in the face of climate change. The many applications for phenology data and models include agriculture, drought monitoring, wildfire risk assessment and the management of wildlife, invasive species, agricultural pests and other risks to human health and welfare, including allergies, asthma and vector-borne diseases. More broadly, phenology data can be used to inform the public about climate change science, and its impacts on the environment, through education and outreach programs. In this symposium, an interdisciplinary set of speakers highlighted new insights into how phenology mediates ecological responses to global change, new applications of phenology data and models in management contexts, and key unanswered questions. Speakers in this symposium also described the role of phenology in many ecological relationships and processes, including flower production, plant–pollinator relationships, invasive species, species distributions, agricultural pest management, ecosystem-level fluxes of carbon and water, and wildfires.
The role of phenology in some of these relationships and processes has been discussed extensively in the literature: the concept of climate-driven, temporal mismatches between an organism and key resources, such as food or pollinators (Visser & Both, 2005), has probably received the most attention. However, it is not clear that those mismatches will often occur or will necessarily lead to rapid declines in population sizes when they do occur, particularly for species with generalist interactions. Examples of climate-driven, temporal mismatches causing populations to decline are rare, possibly because the mismatches themselves are rare, or because the evidence required to describe them is difficult to collect.
The speakers described many other effects of phenological changes that are discussed less often and deserve further attention. For example, as phenology and climatic conditions shift simultaneously, albeit differentially, abiotic conditions at key life-history stages will also change. If leaf-out and flowering dates of early flowering plants shift too quickly relative to temperatures, they could be exposed to an increased incidence of frost, with consequences of reduced survival or reduced reproductive output (Inouye, 2008). If they change too slowly, they risk being out-competed by non-native species that open their leaves or flowers earlier, thereby exploiting the extended growing season (Xu et al., 2007).
At the ecosystem scale, changes in the length of the growing season could alter carbon and water cycling. Warmer temperatures and longer growing seasons that affect leaf and canopy structure or activity (e.g. the carbon-uptake period) are expected to increase both gross primary productivity and respiration, a potential feedback mechanism to the global carbon cycle and climate mitigation. However, the effect on net primary productivity is unclear, and may differ depending on the scale of observation and the type of ecosystem (Piao et al., 2008; Richardson et al., 2009). Much new research on this topic is needed.
Shifting phenologies: impact or plasticity?
Key to understanding and managing plant and animal species within and across changing environments is interspecific variability in the rates and directions of phenological change (Parmesan, 2007). For example, as described above, differential shifts in phenology can disrupt time-sensitive interactions (e.g. plant–herbivore relationships or exposure to environmental stresses such as frost and drought) in ways not necessarily predictable by simple enumeration of species-specific responses. From this variability arises an intriguing question: Is it generally beneficial for a species to track changes in climate by shifting its phenology?
In much research to date, shifts in phenology are used to indicate the effect of an external perturbation on the activity or behavior of plants and animals across space and time. However, investigators are beginning to explore the ecological significance of these changes beyond temporal mismatches. New research suggests that the strength of a species’ phenological response to variations in climate might in fact indicate its vulnerability to climate change: populations with phenologies that track climate tend to perform well, whereas those that do not track climate tend to decline (Møller et al., 2008; Willis et al., 2008). The mechanism underlying this pattern is not clear, and analyses to date are restricted to terrestrial systems. However, phenotypic plasticity has been invoked as a conceptual model – shifts in phenology may be a generally beneficial plastic response to rapid climate change, or phenological plasticity may be correlated to plasticity in other key traits. Assessments of species-specific changes in phenology, particularly when considered in light of changes in resources and abiotic conditions, may emerge as a valuable tool to facilitate the rapid assessment of species vulnerability to climate change. For example, managers and conservation biologists could target efforts to preserve species with phenologies that are not shifting in concert with climatic conditions. Species with generally nonplastic phenologies include most long-distance migratory birds and many plants species. Such a conceptual model could help conservation practitioners to take concrete actions to protect the species most vulnerable to climate change.
Coordinating collection of phenology data
The major limitation to our understanding of phenological responses to climate change, their consequences and their use in management decisions, is the lack of abundant, easily accessible data. Several recent studies, however, have shown the utility of nontraditional sources of phenology data, such as herbarium specimens, photographs and personal journals (Lavoie & Lachance, 2006; Miller-Rushing et al., 2006). In addition, new citizen-science programs are being developed to collect phenology data in the USA and other countries. One such program described in the symposium is the USA National Phenology Network (USA-NPN; http://www.usanpn.org), a new partnership among federal agencies, the academic community and the general public to establish a national science and monitoring initiative focused on using phenology as a tool to facilitate human adaptation to climate change. The USA-NPN is developing a National Phenology Information Management System that will collect new and historical phenology data and will make it freely available to scientists, managers, educators and the general public. Similar efforts are also underway in Europe and elsewhere (Sparks et al., 2009). Global collaboration on standards, data sharing and joint research could be greatly facilitated through the development of an international effort towards a Global Phenology Network.