Population Dynamics of Humboldt Bay Wallflower (Erysimum Menziesii) Over Three Decades on the North Spit of Humboldt Bay, California Andrea J

Population Dynamics of Humboldt Bay wallflower (Erysimum menziesii) over three decades on the North Spit of Humboldt Bay, California Andrea J. Pickart, Annie Eicher, and Laurel Goldsmith U.S. Fish and Wildlife Service October 2018 INTRODUCTION

Menzies’ wallflower (Erysimum menziesii) is a monocarpic perennial in the Brassicaceae restricted to early successional coastal dune habitats in Humboldt, Mendocino, and Monterey Counties, California. The current taxonomic treatment (Al-Shehbaz 2012) combines the different geographic populations as a single species, however, recent genetic work supports subspecies status for the Humboldt Bay population (Vorobik 2015), and it has been previously separated as Erysimum menziesii ssp. eurekense (Hickman 1993). Hereafter, we refer to the Humboldt Bay population as Humboldt Bay wallflower, by the genus name Erysimum or the common name “wallflower.” Humboldt Bay wallflower was listed by the U.S. Fish and Wildlife Service as an endangered species in 1992, with the recognized threats of invasive species displacement, recreational impacts, and lack of protected habitat (USFWS 1998). The wallflower is found only in the semi-stable foredune zone in the Abronia latifolia – Ambrosia chamissonis herbaceous alliance, also known as dune mat (Sawyer et al. 2005). This low-growing herbaceous community is characterized by relatively low cover (Pickart and Barbour 2007) in which wallflower assumes a patchy distribution. On the North Spit of Humboldt Bay, dune mat has been highly impacted by the spread of invasive species including: European beachgrass (Ammophila arenaria), ice plant (Carpobrotus edulis and C. edulis x C. chilensis), yellow bush lupine (Lupinus arboreus), and the annual grasses ripgut brome (Bromus diandrus) and rattlesnake grass (Briza maxima) (Pickart and Sawyer 1998). These species readily invade the sparse dune mat community, creating a dense canopy cover negatively correlated with wallflower presence (Duebendorfer 1992). Wallflower germinates in fall/winter following the onset of winter rains (Pickart et al. 2000) and then persists as a vegetative rosette for an average of three years before bolting (Pickart and Sawyer 1998) and flowering in late winter to early spring once it reaches a critical size threshold (Berg 1986). Fruits mature in summer, and the majority disperse close to the maternal plant in fall and winter. However, longer distance dispersal can also occur through a tumbleweed style of dispersal in which entire fruiting plants become dislodged and are transported by wind (Pickart and Sawyer 1998). There is no persistent seed bank, although some seeds remain viable in above-ground infructescence into a second year (Pickart 2004). Approximately 29% of dispersed seeds emerge and seedling mortality is very high, with only 05- 1.0% of seedlings reaching maturity (Pickart 2004). Mortality is highest during spring and summer months. Plants are subject to white rust disease caused by the biotrophic oomycete Albugo candida, which results in symptoms ranging from isolated white pustules to systemically infected plants in which reproduction is suppressed or prevented (Pickart 2004). A seasonal integral population model using demographic data from four cohorts of wallflower found that interannual variation in demographic rates was correlated with deviations from historical seasonal temperature averages (Schreiber 2015). Notably, fecundity of flowering individuals was lower during warmer winters, correlating with greater white rust disease severity. The model

1 predicted that warmer seasons contribute to lower population growth rates, with implications for a warming climate (Schreiber 2015). Management of Humboldt Bay dune habitats has been occurring for several decades, with the goal of restoration of invaded habitats to the early successional dune mat community through recovery of underlying processes (Pickart 2013), and in some cases with the stated goal of restoring habitat for Humboldt Bay wallflower (Pickart and Sawyer 1998). A survey of the wallflower over the entire North Spit was carried out in 1988 with the goal of establishing population levels, measuring geographic variation in population size, and to establish a baseline for measuring success of future management (Sawyer and André 1990). Since that time, population wide surveys have been carried out on approximately a decadal basis (Pickart et al. 2000). This paper documents results of the most recent (2015) survey and examines population trends over time.

METHODS

Methods in all surveys followed those established in the original 1988 baseline survey (Sawyer and André 1990). The North Spit was divided into 9 biopolitical strata representing geographically separate populations and/or those under separate management jurisdictions (Fig. 1). If a geographically continuous subpopulation was bisected by a management boundary, we created separate strata to allow us to detect differences due to management. Management entity and status for each strata is shown in Table 1. The 2015 survey occurred in the spring during the flowering season. Using a Trimble GPS, large, discrete clusters of wallflowers were mapped as polygons, and isolated occurrences or small clusters were mapped as points. As in previous surveys, plants less than 3 cm in diameter were excluded in order to reduce non-detection error and because plants this small in spring have a low likelihood of survival (Pickart and Sawyer 1998). In each stratum, selected polygons were sampled and others were censused, resulting in a stratified sampling design where the two strata consisted of sampled versus censused occurrences. Small polygons, and large polygons with relatively low plant density were censused, as were all points. We assigned numbers to polygons that were not censused and randomly selected enough polygons to yield a total sample size of 30 plots in each stratum. Circular plots of 1 m radius were then placed systematically within the polygon along east-west transects. Spacing between plots and between transects was consistent within a stratum but varied between strata in order to accommodate 30 plots per stratum. We measured reproductive status and disease incidence of every fifth censused plant (constituting a systematic sample) and of all plants in every other sample plot (constituting a cluster sample). To determine the amount of available habitat at the time of each survey, we used aerial imagery from within a year of each survey date, and heads-up digitized all dune mat. The most recent interval was field verified, which assisted with interpretation of older photographs as well. In order to explore the role of invasive species on available habitat, we heads-up digitized invasive species (Lupinus arboreus, Ammophila arenaria, Carpobrotus spp., and annual grasses) for the most recent time interval only.

Figure 1. Map of the North Spit Humboldt Bay showing location of strata.

Table 1. Ownership and management status of strata. Stratum Name Ownership Management Status BLM Wetland Protection Area BLM Protected, unmanaged BLM Endangered Plant Protection Area BLM Protected, managed Eureka Dunes Protected Area City of Eureka Protected, unmanaged Eureka Airport City of Eureka Unprotected, unmanaged Samoa Industrial Private Unprotected, unmanaged Samoa Dunes Pending and current Protected, unmanaged public ownership Humboldt Coastal Nature Center Friends of the Dunes Protected, managed Ma-le’l Dunes CMA BLM, USFWS Protected, managed Lanphere Dunes USFWS Protected, managed Bair addition USFWS Protected, managed

ANALYSIS

We used simple random sampling formulas (Arnab 2017) to estimate subpopulation totals and standard errors for sampled polygons by substrata (sampled portions of each stand). We then added the census totals to the sampling estimate to estimate the size of each subpopulation. Simple random sampling formulas for proportions were used to determine the proportions of reproductive and rust-infected plants for the subsample derived from censused strata. Cluster sampling formulas were used to estimate proportions for the subsample derived from sampled strata. Stratified random sampling formulas were used to combine the systematic and cluster estimates for each stratum, and to calculate an estimate for the entire population.

RESULTS Population Size The population-wide total has increased exponentially since sampling started in 1988, from approximately 20,000 to more than 133,000 individuals (Fig. 2). However, there was substantial intrapopulation variability, with the Lanphere Dunes and Bair addition subpopulations exhibiting a much higher rate of increase than all other subpopulations (Fig. 3). As of 2015, these two geographically continuous populations represented 64% of the total population but only 30% of the occupied habitat. Density of Erysimum individuals at Lanphere/Bair was 2.7 times greater than the average density elsewhere.

180000

160000 140000 120000 100000

80000

60000 PopulationSize 40000 20000

0 1988 1997 2006 2015

Year

Figure 2. Change in population size from 1988-2015 (error bars are standard error) The number of total individuals increased from 1988 to 2015 in all subpopulations other than the BLM Endangered Plant Area (BLM EPPA), the Samoa industrial site (“Mills”), and the Samoa Dunes.

Figure 3. Population size over time by stratum (subpopulation). Density The density of individuals has varied by site and over time (Fig. 4). In general, densities have declined over time, with the exception of the Lanphere Dunes and Bair subpopulations, which have increased. ANOVA followed by Duncan’s multiple comparison showed that density at the Lanphere/Bair site was significantly higher than all other sites (p<.05).

Figure 4. Density of Erysimum per m2 by stratum over time.

Reproductive Rate The proportion of reproductive plants in the population has varied by time interval, remaining between 0.4 and 0.5 for the first two intervals, then dropping to 0.3 in 2006 and jumping to 0.6 in 2015 (Fig. 5). While this trend was not constant among all subpopulations, it was true for the larger subpopulations (Fig. 6).

Figure 5. Proportion of reproductive plants in the population by time interval.

Figure 6. Reproductive rate over time by stratum (subpopulation).

Disease Incidence The proportion of plants exhibiting symptoms of white rust disease increased during the last two time intervals. The lowest incidence was in 1997, when only 6% of plants were symptomatic (Fig. 7). Infection rate increased to 74% in 2006 and 71% in 2015. Disease symptoms varied by subpopulation and over time. The Samoa subpopulations exhibited lower disease rates overall, but all subpopulations showed lower rates in 1997, with the southern subpopulations exhibiting no rust (Fig. 8).

Figure 7. Infection rate of the population over time.

Figure 8. Proportion of infected plants by stratum and year.

Available Habitat The amount of available habitat occupied by Erysimum for each stratum over time is shown in Fig. 9. The Lanphere Dunes and Bair sites were combined for this part of the analysis because of the continuity of the population, habitat, and management. Lanphere Dunes/Bair had the greatest available habitat during all time intervals. Available habitat declined at the southern sites over time. Examination of aerial photographs revealed that the reduction was primarily due to expansion of invasive species at these sites. In contrast, the Samoa Dunes, Ma-le’l Dunes, and Lanphere/Bair showed increases in available habitat over time. This corresponded to a combination of removal of invasives by restoration projects (Male’l and Lanphere/Bair) and/or the spread of dune mat onto previously mobile parabolic dunes (Samoa Dunes, Ma-le’l Dunes, and Lanphere/Bair).

Figure 9. Amount of available habitat (dune mat) by site over time.

Figure 9. Area (in ha) of available habitat by site and time interval.

Occupied Habitat All sites except for Lanphere/Bair showed increases in the proportion of occupied habitat over time, particularly in the last interval during the most pronounced population increases (Fig.

10). This result is consistent with the increase in densities measured at Lanphere/Bair compared with other sites.

Figure 10. Proportion of available habitat occupied by Erysimum by site and survey interval.

DISCUSSION

Schreiber (2015) found that temperature played a role in explaining demographic rates of the Erysimum population at the Lanphere Dunes in the late 1990s-early 2000s, and attributed this relationship to the effect of temperature on survival of vegetative rosettes and the incidence of white rust disease. Cooler temperatures were associated with higher rates of survivorship and fecundity. In our data set, we found a similar relationship, with the proportion of overall population increase highly negatively correlated with the mean monthly temperature for March- May (reproductive period) during the decade prior to the sample year (r2 = -.98). However, we did not find a direct relationship between rust incidence and spring temperatures, or between population increase and infection rate; i.e. warmer temperatures were not associated with increased disease. This suggests that the effect of cooler temperatures on survivorship of vegetative plants is more important than disease effect on reproductive plants. After experiencing high disease incidences in 2006, most subpopulations increased dramatically by 2015. The high disease rates in 2015 may be related to the high reproductive rate in that year, since disease is more prevalent in reproductive individuals (Pickart et al. 2000).

The disproportionate population increase at Lanphere Dunes may be related to other factors. There have been two instances of assisted dispersal at this site. In the 1970s seeds were brought from the south end of the North Spit and dispersed at the Lanphere site (Pickart 2004), and in the 1990s, seeds were moved from occupied habitat to unoccupied habitat to the south, resulting in a large and thriving new occurrence by 2015 (Fig. 11). The Bair addition was added to the Refuge in 2012, after which control of invasive species occurred. This subpopulation underwent a dramatic increase from 1997 to 2015 that could be partially explained by these management efforts. Similarly, the portion of the Ma-le’l Dunes owned by USFWS was acquired and restored in the late 2000s, and this site showed a corresponding large increase in Erysimum. The role of restoration and management is not clear, however, given that two unmanaged populations (Eureka Dunes Protected Area and Eureka airport) both showed significant increases over time. The Lanphere Dunes/Bair site receives the least recreational impact because it has the most restrictive access (permit required for visitors not attending a guided walk). Many of the occurrences at the Lanphere Dunes are on the trailing ridges of long-walled parabolic dunes, which are aligned with prevailing summer winds. This might enhance wind dispersal of seeds, including via tumbleweed style dispersal. The disproportionate population growth and high densities seen at this site could be due to a combination of intensive management (the site is treated annually to remove any new occurrences of Ammophila, Lupinus, and Carpobrotus, lack of recreational impacts, favorable topography, and history of assisted dispersal. The two subpopulations that are declining are the Samoa Dunes and Samoa Industrial (Mills) sites. These two sites differ markedly. The Samoa industrial site is highly invaded and plants are restricted to very small patches of native plants which are under increasing threat of displacement (Fig. 12). This subpopulation may be on its way to blinking out. The Samoa dunes site has a very patchy distribution over a larger area. Although invasive species cover much of the site, there are still substantial areas of unoccupied suitable habitat (Fig. 13). The southern portion of the site is not yet protected, and recreational impacts are high. The northern portion, owned by Manila Community Services District, is subject to high recreational use. Previously restored, that portion of the site has become reinfested with invasive species which are competing with Erysimum. The large increase in the BLM Wetland Protection Area is primarily due to a newly discovered occurrence that was undoubtedly present in previous years but had not been detected due to inaccessibility. The BLM EPPA has not experienced the increases seen at other managed sites, but rather has stayed similar in population size since 1988. The site had more Erysimum at the start of the study than the Eureka sites to the north, and over the western portion of the site Erysimum filled available habitat. Subsequent spread has likely been limited by lack of habitat (Fig. 11). In contrast, the Eureka Dunes and Airport sites began with lower densities of Erysimum, and plants have spread and now inhabit previously unoccupied habitat (Fig. 14). These three southern sites are characterized by higher proportions of occupied habitat compared with sites to the north (Fig 10). Although there remains available habitat at these sites, much of the unoccupied habitat consists of isolated fragments surrounded by dense invasive species which may inhibit dispersal. It appears that habitat at these southern sites may have become saturated given existing dispersal barriers.

Figure 11. Map showing the change in Erysimum occurrences at the Lanphere/Bair sites in relation to available habitat (2015). Populations grow along northwest-southeast trending trailing ridges. The oldest populations are overlain over newer populations to illustrate spread.

Figure 12. Map showing change in occurrences of Erysimum at the Samoa Industrial Site in relation to available habitat and invasive species (2015). The majority of the site is covered with invasive species and populations remain in small isolated patches of suitable habitat.

Figure 13. Map showing change in occurrence of Erysimum at the Samoa Dunes site in relation to available habitat and invasive species (2015). Although invasive species are abundant, Erysimum occupies only a small portion of available habitat, especially in the northern part of the site.

Figure 14. Map showing the changes in Erysimum occurrences at the BLM EPPA, Eureka Dunes Protected Area, and the Airport sites. The BLM site began with more occurrences had far less available habitat in which Erysimum could disperse after 1988 compared with the Eureka sites.

CONCLUSIONS Sampling of population attributes of a metapopulation of Erysimum menziesii on the North Spit of California over three decades revealed exponential growth, although intrapopulation variation was exhibited. The northermost subpopulation at the Lanphere/Bair sites showed disproportionately high increases in population size and greater density, attributed to several factors: past assisted dispersal, lack of recreational impacts, habitat restoration, and topography that facilitates dispersal. Subpopulations in decline included two southern sites, one of which (Samoa Industrial) is being overwhelmed by invasive species. The adjoining southern sites BLM EPPA, Eureka Dunes, and Eureka Airport show dissimilar trends. BLM EPPA began with larger populations in 1988 but may have saturated available habitat and has remained relatively static. The two Eureka sites continued to increase into unoccupied habitat but may be nearing saturation. Population growth overall was negatively correlated with mean spring temperatures for the decade prior to each survey, suggesting that cooler temperatures are beneficial to population growth. Population growth was not a function of rust incidence, and the two most recent decades showed both the highest rust incidence and the highest population increase rates. Despite the ability of white rust disease to suppress reproduction, Erysimum is able to achieve dramatic population size increases at favorable sites.

ACKNOWLEDGMENTS Researchers involved in past field work and analyses include Jim André, John Sawyer, Mignonne Bivin, Howard Stauffer, and Kimberly Hayler. Funding for the current survey was provided by U.S. Fish and Wildlife Service Region 8 Inventory and Monitoring Program. We thank private and public property owners who allowed access for field work, including U.S. Bureau of Land Management, the City of Eureka, Manila Community Services District, and Friends of the Dunes.

LITERATURE CITED

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