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Ecological theory predicts both negative and positive effects of increasing environmental variability on species persistence. Increasing variance in vital rates tends to decrease long-term average population growth rates (Lande 1988; Tuljapurkar 1990; Boyce 1992; Higgins et al. 2000; Menges 2000). Environmental variation can also threaten populations when extreme years are catastrophic. Alternatively, temporal environmental variation can benefit species persistence through the storage effect (Chesson 2000; Levine & Rees 2004; Adler et al. 2006). If species differ in the years in which they experience their maximal performance, climatic fluctuations enable rare species to avoid interspecific competition. Forecasting species persistence in a changing climate thus requires understanding of how populations respond to climate variability and the mechanisms underlying this response (Fieberg & Ellner 2001; Meyer et al. 2006).
The most intuitive mechanism, and the one commonly assumed to operate, is water limitation. In arid systems, where water is known to be a limiting factor, wet years may ease water limitation of vital rates such as survival and fecundity, whereas dry years may not even provide the water resources necessary for successful completion of the life cycle (Gutierrez & Meserve 2003; Adler & Levine 2007).
A second mechanism by which rainfall drives fluctuations in annual plant populations is between-year variation in germination cueing. Rainfall years differ greatly in the timing and conditions coincident with the germination-inducing storm, cues that regulate germination and the size of the emergent population (Went 1948; Beatley 1974; Baskin & Baskin 2001). This mechanism is related to the first in that selection should favour germination in response to environmental cues predictive of future moisture conditions (Pake & Venable 1996). Indeed, winter desert annuals germinate best when the temperature at the time of seed wetting is cool (Went 1948; Beatley 1974), presumably indicative of upcoming winter rains. In fact, if temperature conditions required for germination are not met by early storms, subsequent precipitation may have little effect on desert annual population dynamics (Beatley 1974). More general appreciation for the possibility that variation in germination cueing underlies plant population fluctuations is only beginning to develop.
While the first two mechanisms involve direct responses to rainfall conditions, a third mechanism poses that plant populations may fluctuate with climate due to indirect effects mediated by changes in the surrounding community (Levine & Rees 2004). If rainfall variability drives large between-year variation in the competitive environment of a focal species, its population may fluctuate because of temporal variation in competitive suppression. For example, Pitt & Heady (1978) argue that mid-winter drought years favour the deep rooted Erodium in California grasslands because such years are disproportionately stressful for their exotic grass competitors.
Varying rainfall can thus influence annual plant population dynamics through ‘water limitation’, ‘germination cueing’, and ‘competitive suppression’ mechanisms, or some combination of the three. Determining when each process dominates is critical to forecasting how populations will respond to the wetter or drier climates of the future, or the warmer temperatures that will presumably accompany the germination-inducing rains. Evaluating these mechanisms is also important for predicting beneficial effects of environmental variability on persistence. If population variability is controlled largely by germination cueing, and competitors differ in their cues, environmental variation can strongly buffer species from extinction via the storage effect (Chesson 1990, 2000; Pake & Venable 1996). Similar buffering arises from differential effects of water limitation on different species.
In this study we examine how the populations of three seed banking, rare annual plants endemic to the California Channel Islands respond to wide variation in precipitation and the mechanisms underlying their response. Island endemic plants such as these are particularly threatened by climate change because their current ranges are unlikely to overlap regions that are climatically favourable in the future (Walther et al. 2002; Thomas et al. 2004) and their often small populations make them particularly sensitive to climatic variability. Moreover, restricted dispersal prevents them from reaching more favourable habitats in the future, and thus their persistence depends on how they respond to climate change in their current locations.
To evaluate the different mechanisms underlying plant population response to climate, we monitored the emergent populations of three different annuals and their competitors over 5–12 years, a period including severe drought and wet El Niño years (Schonher & Nicholson 1989; McPhaden et al. 2006). We then correlated emergent population size with variables related to germination, water limitation and competition. To examine between-year variation in population growth rates, we combined the monitoring data with vital rates obtained in experimentally sown plots. We then used elasticity analyses and life table response experiments (Caswell 2001) to evaluate the mechanisms responsible for temporal variation in population growth rates. Lastly, we used the demographic data to assess the relative endangerment of our three focal species, and the type of climate years most critical to population persistence.
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Understanding the climate factors that drive temporal variation in plant populations is critical to forecasting their persistence under natural and anthropogenically altered climate regimes. The three rare and endangered annual plants of Santa Rosa Island studied here may be particularly threatened by climate change because their geographic ranges are narrow and therefore unlikely to include locations with comparable climates in the future. Indeed, the sensitivity of Gilia, Malacothrix and Phacelia to climate was borne out in the current study. Through years differing greatly in total annual rainfall, and conditions surrounding the first major rainfall event, all three species showed large between-year variation in above-ground springtime plant density (Figs 2–4). For Phacelia, this variation was roughly 100-fold and for Gilia and Malacothrix it was ninefold. Similarly large temporal variation in plant abundance has been noted in a wide range of annual systems, and particularly those of arid and semi-arid regions of the world (Talbot et al. 1939; Went 1948; Heady et al. 1958; Beatley 1974; Young et al. 1981; Bowers 1987; Gutierrez & Meserve 2003; Fox et al. 2006).
interactive effects of water limitation and germination cueing on springtime plant abundance
Temporal variation in rainfall can influence annual plant population dynamics by differentially provisioning water resources across years, differentially cueing germination, or by altering competitive environments. For all species in the current study, low plant abundance during the severe drought year of 2007 supported the water limitation mechanism. However, beyond the effects of severe drought, plant populations seemed remarkably insensitive to season-long rainfall. Species derived little benefit from above average rainfall, as evidenced by low abundance of Malacothrix and Phacelia plants in the wet 2005 El Niño year, and the only marginally above average Gilia plant density that year. In sum, results suggest that droughts force low plant abundance for the three focal species. But there remains considerable variation in plant density in non-drought years, variation that is largely unrelated to total annual rainfall.
Our results support the importance of temperature-based germination cues as a control over the dynamics of our focal annuals in non-drought years. Outside of the 2007 drought year, the nightly low temperature after the first major rain event explained over half the between-year variation in Gilia plant density (Fig. 2c), and over 90% of the variation in our significantly shorter time series for Malacothrix and Phacelia (Figs 3c, 4c). Temperature at the time of seed wetting is well-known to influence the germination of California annuals in general (Went 1949), and in laboratory trials, cold temperatures induce the germination of our three focal species (J.M. Levine, unpublished data). Indeed, the Gilia germination rate in the field (Fig. 5a) was highest in the year with the coldest of the germination-inducing storms. In general, these results suggest that variation in germination is likely to explain much of the between-year variation in plant density in non-drought years.
the role of competitor dynamics and the storage effect
Temporal variation in the springtime plant densities of Gilia and Phacelia was not correlated with the total vegetative cover of their respective surrounding communities. This suggests that between-year variation in competitive suppression is not the major driver of the observed population fluctuations of these two species. Moreover, that they and their competitors respond differently to the environment is a key requirement for positive effects of climate variation on persistence via the storage effect (Chesson 2000). The more differently the rare focal annuals and their competitors respond to different years, the more the competitor species collectively suppress themselves, favouring the persistence of the rare annuals. In contrast to Gilia and Phacelia, Malacothrix showed a non-significant, but negative correlation between its emergent density and cover in the surrounding community. This could reflect the impact of temporal variation in competitive suppression, or alternatively, strong differences in how Malacothrix and its competitors respond to different year types.
mechanisms underlying variation in population growth rate
Like springtime above-ground plant density, species per capita growth rate estimates from 2004 to 2006 showed a lack of dependence on season-long rainfall. Growth rates were lowest during the wet 2005 El Nino year for Gilia and Malacothrix, and negative for Phacelia (Fig. 5g–i). Even the seeds produced per germinant, F, the demographic variable which would seem most sensitive to water limitation, was unrelated to season-long precipitation (the high 2005 Phacelia value is based on only two germinants). Thus, while elasticity analyses show that F is as important as the germination rate, g, in determining population growth rate of the three focal species, F simply did not correlate with rainfall over the short time series of our study. Similarly, life table response experiments showed that observed variation in F was responsible for much of the observed variation in population growth rate for all three species. However, without a connection between rainfall and F, this result provides little support for the water limitation mechanism.
Elasticity analyses and life table response experiments indicate the variation in g has the same potential as F to drive variation in population growth rates. Indeed, the reduction in Gilia population growth rate from 2004 to 2005 could be explained by lower germination in 2005 (Fig. 6a). Importantly, the reduced 2005 germination (Fig. 5a) occurred in a year with warmer first rains (Fig. 1b), providing a link between population growth rate and germination cueing. More generally, based on the high elasticity of g, and its apparent sensitivity to the temperature and the time of the first major rains (Figs 2c, 3c and 4c), we hypothesize that germination cueing is a key driver of temporal variation in population growth rate.
relationship between population growth rate and trends in springtime plant density
A finding with broad implications is that fluctuations in population growth rates were only weakly related to variation in above-ground plant abundance. Most studies of temporal variation in annual plant systems focus on above-ground measures of population performance (Talbot et al. 1939; Heady 1958; Beatley 1974; Bowers 1987). Although this likely reflects the ease of obtaining plant density or abundance data, such measures can be misleading when predicting the effects of individual years on population viability. Over longer time scales, however, population growth rates and trends in the above-ground population dynamics should be concordant.
In our study, population growth rate estimates for our three species were generally consistent with decadal long trends in their spring-time population size. Phacelia had negative per capita growth rates projected in all 3 years of the study (Fig. 5i), matching long-term trends. In 1998, 1465 plants were noted in the swale and crest sites. Seven hundred and seventy-one plants were counted in these sites in 2001, 360 in 2003 and 21 in 2007. Although low population densities were also observed throughout this time series, peak population sizes over the last 10 years appear to be declining, consistent with the negative growth rates projected here. By contrast, Malacothrix and Gilia, with much higher projected population growth rates (Fig. 5g,h) have not suffered the decadal decline seen in the Phacelia population.
evolutionary and biogeographic implications
One of the most striking results of this study is that all three annuals had their greatest population sizes in years with cold first rains. Although we speculate, this consistency suggests an adaptive explanation may be involved. Indeed, a cold requirement for germination may allow these species to avoid germination with the rare late summer storms (August and September). In coastal California, with its Mediterranean climate, these late summer storms are unlikely to be followed by considerable rainfall for several warm months. This creates drought conditions even more severe than in 2007, when populations were uniformly low. Importantly, the early season storms are usually tropical in origin, and are thus associated with relatively warm weather systems. As a consequence, cold temperatures at the time of seed wetting may be indicative of winter or late fall, a time when subsequent rainfall is almost guaranteed.
Alternatively, cold temperature requirements for germination may be a relictual trait, having evolved in desert environments. Much of the annual plant species diversity in coastal California, including the Phacelia, Gilia and Malacothrix genera, is derived from taxa that historically moved into the region from Mexico via desert environments (Raven & Axelrod 1978). Classic work by Went (1949) has shown that California winter annuals in the desert require relatively cold temperatures at the time of seed wetting to induce germination (see also Baskin & Baskin 2001). As in the current study, research in desert systems has shown an overriding importance of germination cueing over water limitation in controlling temporal variation in annual plant populations (Went 1949; Beatley 1974; Bowers 1987). High rainfall years only drive large populations of Mojave desert winter annuals if the appropriate germination cues were presented in the fall or early winter (Beatley 1974).
population persistence under current and future climate regimes
Gilia, Malacothrix and Phacelia showed precipitous declines in springtime plant density over the five focal years of our study (2003–07). Based on our understanding of how rainfall variability affects these populations, their recent declines may not necessarily reflect long-term directional change in population health. Our results lead us to hypothesize that the species were relatively abundant in the early part of the time series (2003 and 2004) because cold first rains were coupled with reasonable subsequent rainfall. Populations were low in 2005 and 2006 because of warm first rains, and low in 2007 because of severe drought conditions. Given that all of these plants have modest to high annual survival of ungerminated seeds (0.57–0.75), a year with cold first rains and non-drought conditions may facilitate their return to higher plant abundance. More generally, these hypotheses emphasize the value of understanding the climatic controls over temporal variation in plant demography when forecasting population persistence and interpreting trends in population dynamics.
Temperature is forecast to increase over the next century in California and elsewhere, while future precipitation regimes are more uncertain (Bell et al. 2004; Salinger 2005). Our work suggests that barring severe droughts, changes in the timing and temperatures associated with the first major rains may have much stronger effects on population persistence than changes in total annual rainfall. Even if season-long precipitation remains unchanged, warmer first rains will likely mean lower germination, and lower population growth rates for all three Santa Rosa Island annuals. Our work adds to a growing body of work (Visser & Both 2005) suggesting that alteration of environmental cues may strongly determine how climate change affects plant communities.