Calochortus plummerae Greene (Plummer's Mariposa Lily) is a geophyte of California chaparral that flowers abundantly after fire. It is endemic to five counties in southern California and has a California Rare Plant Rank of 4.2 (“plants of limited distribution; fairly threatened in California”; California Department of Fish and Wildlife 2021). It usually produces a single, basal strap leaf from an underground corm in the spring, which withers before the plant flowers. Flowering, if it occurs, takes place between May and July (Fiedler 2012). In years between fires, Calochortus species often remain in a vegetative state, putting up leaves in the spring (e.g., Christensen and Muller 1975; Keeley et al. 2006). Horton and Kraebel (1955), however, suggested that the corms of C. plummerae also become dormant as shrub cover increases in the years after fire, and that the plants produce leaves only in exceptionally wet years.

Fire-stimulated flowering is common among geophytes in Mediterranean climates, including that of C. plummerae's range, and flowering of some species is more tightly restricted to post-fire years than that of others (Stone 1951; Horton and Kraebel 1955; Christensen and Muller 1975; Keeley et al. 1981; Le Maitre and Brown 1992; Rundel 1996; Lamont and Downes 2011). Factors that may contribute to this post-fire bloom include reduced competition for resources (light, nutrients, and water), release of soil nutrients by fire, reduced herbivory, and, potentially, stimulatory effects of smoke on flowering (Christensen and Muller 1975; Keeley 1993; Light et al. 2007; Borchert and Tyler 2009). Furthermore, flowering itself may deplete energy reserves, contributing to low growth rates and low incidence of flowering after the post-fire bloom (Tyler and Borchert 2003; Borchert and Tyler 2009). In years between fires, geophytes may grow vegetatively or their underground organs may become dormant for some period (Keeley and Davis 2007).

In the fall of 2003, multiple wildfires burned a large fraction of C. plummerae's range, providing an opportunity to study plant fate and phenology in the years following fire. The largest of these were the Simi Fire, the Old Fire, the Grand Prix/Padua Fire, which together burned over 105,000 ha across Ventura, Los Angeles, and San Bernardino Counties (Clark et al. 2003). Prolific flowering of C. plummerae the following spring made it apparent that the species was not as rare as had previously been believed. Among the newly discovered populations of C. plummerae that year was one on the campus of California State University San Bernardino, a campus that partially burned in the Old Fire (Williams et al. 2006).

The primary goals of this study were to quantify changes in flowering of C. plummerae in the years following fire, describing the degree to which flowering was restricted to the post-fire environment, and to explore correlates of interannual variation in flowering (in particular, variation in rainfall). Three years into the study, however, we expanded the focus to measure plant survival, potential dormancy, interannual variation in leaf size, and herbivory. We did not measure seedling recruitment because we could not distinguish seedlings of C. plummerae from seedlings of Calochortus splendens Douglas ex Benth., which was also present on the site (Williams et al. 2006). Flowering was monitored for 10 years and vegetative characteristics (leaf emergence, leaf size, and leaf loss to herbivory) were monitored for six years. We explored the relationship between annual precipitation and flowering of C. plummerae plants, we documented year-to-year variation in the size of the strap leaf produced (specifically, leaf width), and we tested effects of reducing leaf area (experimental herbivory or leaf clipping) on current-year flowering.

Methods

Results

Flowering, Survival and Dormancy

As expected, the number of C. plummerae plants flowering was highest in the first year after fire (Fig. 1A). Year to year variability was high. Flowering completely failed in the driest year (the 2006–2007 season) but reached a level equivalent to 27% of the post-fire bloom eight years after fire (in 2011; Fig. 1A). Plants that bloomed in 2004, right after the fire, constituted a smaller and smaller fraction of the blooming population as the years passed, but one survivor still bloomed in 2013 (Fig. 1A).

Fig. 1.

Year-to-year variation in plant performance (flowering and leaf width) and potential controlling factors (rainfall and herbivory). A. Total number of C. plummerae plants flowering in plots. Stacked bars show flowering plants that were originally marked in 2004, separating the set of 25 plants included in the leaf-width analysis (black bars) from others (hatched bars), and flowering plants that were new, or not encountered in 2004 (white bars). B. Rainfall from July of the previous year through June at Redlands, CA. C. Leaf width (mean ± SE) of 25 individuals for which measurements were available from every census. Bars labeled with the same letter were not significantly different from each other according to multiple pair-wise t-tests with a Bonferroni correction. D. Number of plants of Calochortus spp. that experienced severe herbivory (leaving < 3 cm of leaf length; solid bars) and those that experienced less severe or no herbivory each year.

Thirty percent of the originally marked plants were observed in 2013, having survived at least 10 years. The fraction of the originally marked population that produced a leaf during the six years with early-season surveys (i.e., were neither dead nor dormant) ranged from 25% to 30% (25% in 2007, 28% in 2008, 32% in 2010, 31% in 2011, and 30% in both 2012 and 2013). Approximately 60% of the originally marked plants were not observed at all during the last seven years of the study and were, therefore, presumed dead. The remaining 10% were not observed during the last year of the study, but we could not determine whether they were dead or merely dormant.

Of those plants that were found in the last year of the study, only 58% were observed above ground every year during the six years with early-season surveys. The rest were not observed during some years, reappearing after a one year “absence” (28%) or an “absence” of two or more years (14%). These “absent” survivors were either dormant, or their leaves were eaten so early and so thoroughly that they could not be detected.

Flowering and Rainfall

The statistical effect of rainfall on flowering only became significant when a second factor was included in the model to account for the stimulatory effect of fire. Annual rainfall varied widely over the course of the study, ranging from 100 mm in the 2006–2007 season to 643 mm in 2004–2005 (Fig. 1B). The number of plants that flowered in a year was not well predicted by annual rainfall alone (R² = 0.22, P = 0.17). However, examination of the trajectory of flowering over the years suggested that flowering did increase with rainfall, but that the effect decreased over time (Fig. 2). A multiple-regression model that incorporated both rainfall and an asymptotically decreasing effect of time since fire yielded a good estimation of the number of C. plummerae plants flowering in our plots over the 10 years of this study (R² = 0.98, adjusted R² = 0.97, P < 0.001). It also predicted increased flowering in a subsequent wet year (28 plants in 2019) fairly closely (Fig. 3). The equation obtained was

where F was the number of C. plummerae plants flowering in plots, R was the annual rainfall the preceding year (mm), and T was time since fire in years, with year one being the spring following fire. Both rainfall (t-test, t = 6.97, P < 0.001) and the inverse of time since fire (t-test, t = 15.37, P < 0.001) contributed significantly to the predictive capacity of the model.

Fig. 2.

Relationship between annual rainfall (July–June) and number of C. plummerae plants flowering in plots at the end of the season (late May to early June). Arrows indicate the trajectory over time, from the number of plants flowering in 2004 (top) to the number flowering in 2013 (bottom).

Fig. 3.

Number of plants flowering vs. model estimate based on precipitation and time since fire. Closed circles represent data used to form the model, and the dotted lines represent the 95% prediction interval for those data. Triangles represent data taken later, in 2014, 2016, and 2019. Unrealistic predictions of negative numbers of plants flowering in dry years was the result of the model being a simple regression model with a negative intercept, rather than a biological or mechanistic model.

Discussion

Flowering of Calochortus plummerae was not completely restricted to the first year or two immediately after fire, but flowering declined substantially after the initial post-fire bloom. After the second year post-fire, the density of flowering plants did not exceed 27% of that observed immediately after fire. The mechanisms responsible for both the post-fire bloom and the decrease in flowering over subsequent years were not addressed in this study but most likely include changes in plant competition. Competition was very low the first year after fire, with plots supporting only sparse growth of annual plants and very small resprouts of chaparral shrubs (primarily Adenostoma fasciculatum Hook. & Arn.). Although chaparral recovery was not formally measured, it followed a typical trajectory. Acmispon glaber (Vogel) Brouillet, a rapidly growing subshrub, dominated some areas with cover peaking the third year after fire (2006). The crowns of Adenostoma fasciculatum continued to increase in size throughout the study, and their heights surpassed those of the faster-growing Salvia species (Salvia mellifera Greene and Salvia apiana Jeps.) by the fifth or sixth year of the study. Although changing competition from shrubs and subshrubs may have played a major role in the asymptotically decreasing trajectory of flowering in C. plummerae over the years, we cannot rule out other factors. “Time since fire” subsumed all changing factors related to post-fire recovery, allowing us to test effects of factors unrelated to fire cycles, such as variation in rainfall.

Flowering of C. plummerae was well predicted by annual rainfall once the overall effect of “time since fire” was factored out. This was true both at a population level and when individual plants were followed (Fig. 1A). The set of 25 plants that consistently had measurable leaves during early-season surveys produced narrower leaves and were less likely to flower during dry years than during wetter years. Increased plant dormancy may have contributed to low flowering during dry years, but data supporting increased dormancy during dry years was weak. The fraction of the originally marked population that was active (produced a leaf) in years with early-season censuses only ranged from 25% to 32%. Even during the driest year of the study (2007), a quarter of the originally marked plants produced leaves. Plant dormancy, therefore, could not account for the complete lack of flowering that year.

Over the 10 yr of the study, there was substantial turnover in the population that flowered. A large fraction of the originally marked population (60%) was not observed at all during the last 7 yr of the study. These plants were either very deeply dormant or dead. We assumed, however, that they were dead. Studies of bulb dormancy in other Calochortus species have found either little evidence of dormancy (e.g., Fiedler 1987; Fredricks 1992) or a pattern similar to the pattern we found for C. plummerae, with the largest fraction of apparently dormant plants producing leaves after a dormant period of only one year, a smaller fraction producing leaves after a dormant period of 2 yr, and an extremely small fraction producing leaves after a dormant period of three or more years (Miller et al. 2004). The fact that more than a quarter of our originally marked plants put up leaves every year or skipped periods of only one year make it unlikely (although possible) that other individuals experienced such deep dormancy that they failed to produce leaves for 7 yr in a row. As years went by, new individuals began to flower. After 7 yr, the originally marked plants accounted for less than half of the flowering population.

The fact that leaf area removal (simulated herbivory) eliminated flowering later the same year suggests that flowering in this species is largely dependent on current-year carbon gain. There is good evidence that carbon gain in prior years and the size of the underground storage organ influence flowering of various other geophytes (e.g., Dafni et al. 1981; Tyler and Borchert 2003; Schlising and Chamberlain 2006; Borchert and Tyler 2009). Moreover, the flowering of some geophytes appears to exhaust their reserves to the extent that they grow more slowly, remain dormant, or fail to flower the following year (Eggert 1992, Tyler and Borchert 2003; Lesica and Crone 2007). Tyler and Borchert (2003) suggested that a decline in flowering of some geophytes in the years following the first post-fire year may be due, in part, to the depletion of storage reserves caused by the post-fire flowering, itself. We did not see patterns in our flowering data to suggest that the act of flowering exhausted reserves of C. plummerae plants to such an extent that they failed to flower the next year. In fact, a few individuals flowered 3 yr in a row between the fifth and tenth years after fire. The dynamics of carbon gain and depletion in prior years may play a role in the flowering of C. plummerae, but our data suggest that current-year carbon gain is a critical determinant of flowering in this species. The pattern of increased flowering in wet years and in the period after fire (with consequently higher levels of soil nutrients and lower competition for light and water) is consistent with effects of increased resources on carbon gain and with the observation that flowering is dependent on current-year carbon gain.

Although resources released by fire may largely account for prolific flowering after fire, large fires can also reduce herbivory (Christensen and Muller 1975; Barro and Conard 1991). Patterns of herbivore damage on C. plummerae at our site suggested that mammalian herbivores were responsible for most instances of severe herbivory. This observation is consistent with those of Fiedler (1987) who noted that the most damaging herbivory on four Calochortus species that she studied along the central California coast was caused by small mammals (several rabbit species and pocket gophers) and by mule deer. While burrowing animals may survive fires, large fires have been reported to cause heavy mortality among herbivores such as brush rabbits (replaced by desert cottontails at our site) and California ground squirrels (Chew et al. 1959; Quinn 1990; van Mantgem et al. 2015). Mule deer may die in fires (Chew et al. 1959) but often flee fire and recolonize the area in the years after fire (Quinn 1990; van Mantgem et al. 2015). Therefore, herbivore damage to C. plummerae plants at our site may have lowest in the years immediately following fire, before we began monitoring it.

One apparent paradox in our findings was that herbivory had a strong effect on flowering, and severe herbivory varied among years, but we did not need to include herbivory in the model to obtain a good prediction of flowering. Since herbivore populations have been shown to respond to both fire and rainfall, usually in complex and species-specific ways (e.g., Christensen and Muller 1975; Barro and Conard 1991; Holmgren et al. 2001; van Mantgem et al. 2015) it is possible that impacts of herbivory on flowering were subsumed under either the “time since fire” effect or the “rainfall” effect.

Regardless of the causal mechanisms, we found interannual patterns of flowering in Calochortus plummerae that were consistent both with fire-promotion of flowering and with flowering that was controlled increasingly by direct or indirect effects of precipitation during the fire-free interval. Flowering was eliminated during severe drought, and this flowering failure occurred despite the continued presence of non-dormant plants on the site. Although high rainfall during the fire-free interval appeared to stimulated flowering of C. plummerae, the density of flowering plants in this recovering shrubland vegetation was rarely more than a quarter of that found during the initial post-fire bloom.