Coastal dune invasion and restoration at Point Reyes: the ecology of European sea rocket, Cakile maritima

Shay McGraw1, Jay Luce Nelson2, Yuxin Shen3, Aidé Villegas4

1 University of California, Davis; 2 University of California, Santa Cruz; 3 University of California, Irvine; 4 University of California, Merced

ABSTRACT

California coastal dune ecosystems are prime targets for conservation and restoration efforts due to their high native plant diversity and rates of endemism. Invasive dune species such as European sea rocket (Cakile maritima) may disrupt key ecosystem processes by altering dune physical processes and outcompeting native species, decreasing the success of the endangered species beach layia (Layia carnosa) and Tidestrom’s lupine (Lupinus tidestromii) at Point Reyes National Seashore in Marin County, California. We investigated potential abiotic and biotic stressors that may inhibit the success of C. maritima. We found that elevation did not affect C. maritima growth patterns, while topography played a larger role. The backdune community featured greater growth and less investment in belowground competition than the foredune and distal valley site. Competition with non-nitrogen-fixing plants was found to limit C. maritima growth and result in greater allocation of resources to root growth, though the number of native competitors did not affect performance. Conversely, native nitrogen-fixer presence (but not abundance) was associated with increased biomass and less investment in root growth, indicating that nitrogen may be one of multiple stressors limiting C. maritima success. Further understanding of these environmental stressors may aid in future prediction of susceptibility of coastal dune microhabitats to invasion and the prioritization of restoration project locations.

INTRODUCTION risk of extinction due to restricted geographic distribution and limited Maritime areas of California’s Central population sizes, and consequently are Coast represent some of the most prioritized in many conservation and species-rich regions in California, and restoration strategies (Myers et al. host particularly high rates of plant 2000). Coastal dune ecosystems are endemism (Raven & Axelrod 1978). particularly vulnerable to human use, Endemic species generally have higher pollution, and invasion by non-native

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plants. Coastal land is particularly of invasions in a relatively fragile targeted for residential development ecosystem make restoration efforts and recreational use because of its critical to the continued existence of aesthetic value and proximity to the many threatened and endangered ocean. A complex and difficult biotic native species, including many endemic threat to control, however, is the species. introduction of invasive species. Invasive species supplant natives, alter dune Restoration efforts in dune habitats physical processes and local topography, have been notoriously unsuccessful, and disrupt the foraging and nesting however, due to a lack of physiological behaviors of dune animals (Young 2017). understanding of the invading species, Consequently, California’s coastal dunes as demonstrated by the case of early have been an area of interest for many efforts to remove A. arenaria from conservation and restoration projects. California coastal dunes. Initial attempts at removal included burying patches of Alterations to dune topography and A. arenaria, but the grass reemerged vegetation composition caused by from where it was buried and spread invasive species degrade coastal dunes further throughout the surrounding as habitat for native species. Two of the area, instead amplifying the percent most extensive invasive species on the cover of the species (Young 2017). California coast, highway ice plant Additionally, restoration is difficult due (Carpobrotus edulis) and European to the ability of other invasive species to beach grass (Ammophila arenaria), were succeed the landscape when one purposefully introduced to stabilize dominant species is suddenly removed, dunes. By creating a higher and steeper decreasing competition for water and foredune via sand accumulation and nutrients while increasing open restricting sand from flowing to interior stretches of sand. In one case of A. dunes, these soil-stabilizing species arenaria removal, the grass was change the natural topography and manually removed when burial only successional conditions often required progressed the spread of the species. for native species. Many areas of While the grass population was severely California’s coast are carpeted with ice diminished, European sea rocket (Cakile plant, further limiting the space maritima) was readily able to colonize available for endemic and endangered the recently cleared landscape (Michael native plant species. The changes to Spaeth, personal communication). local topography and vegetation Going forward, physiological limits and composition in coastal dunes negatively responses to biological stressors of an impact the animals that rely on the invasive species should be studied habitat for foraging and nesting, like the extensively and utilized to establish endangered Western Snowy Plover effective and species-specific removal (Charadrius nivosus nivosus) (Pickart strategies to ensure cost-effective and 1997). The far-reaching consequences efficient restoration.

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Point Reyes National Seashore in included water table accessibility, salinity, California provides an excellent system and nutrient availability, which were with which to explore the abiotic and estimated using the proxies of elevation, biotic factors that affect a plant’s ability distance from the ocean, and site to invade. Point Reyes has seen topography, respectively. Biotic factors intensive efforts at coastal restoration were those associated with competition dating back decades. In 2009, Point from or facilitation by surrounding plants Reyes National Seashore reported that of three guilds: native nitrogen fixers, over 60% of the park’s coastal dunes native non-nitrogen-fixer competitors, had been invaded by European beach and invasive competitors. Biomass and grass and ice plant (Muldoon 2009). root:shoot ratio were used to evaluate Manual removal of A. arenaria has the growth performance and resource proven to be an effective restoration allocation by C. maritima. This study technique (Pickart 1997). Recent dune provides a basic insight on C. maritima restoration projects at Point Reyes have physiology in relation to resource implemented this technique with much allocation and growth and may be used to success, but a secondary invasive, prepare effective restoration strategies European sea rocket (Cakile maritima) both in terms of C. maritima control and has been noted as taking over restored assessment of the relative susceptibility of areas of the dune (Boyd 1988; Michael dunes to its colonization and spread. Spaeth, personal communication). Like A. arenaria, C. maritima stabilizes dunes METHODS and inhibits the progression of dune Natural History disturbance and succession cycles. This alteration of ecosystem function The study was conducted at Point Reyes decreases the abundance of the National Seashore in Marin County, CA, endangered endemic species Layia located northwest of San Francisco. carnosa (beach layia) and Lupinus Predominantly covered by Douglas fir tidestromii (Tidestrom’s lupine), which (Pseudotsuga menziesii) and Bishop pine thrive in early successional stages with (Pinus muricata) forests covering well unstabilized dunes; the same effect is over 34,000 acres, Point Reyes spans over associated with population declines of the 70,000 acres of coastal wilderness area endangered shorebird Charadrius nivosus (Sansing & Chapman 1978). In 1962, nivosus (western snowy plover) due to its United States President John F. Kennedy utilization of open sand for mating and established Point Reyes as a National reproduction (Pardini et al. 2015). Seashore protected by the National Forest Service, allowing the continued operation In this study, we examine both abiotic of the 26 ranches established in the area and biotic factors that may limit the beginning in the 1850s. It is also the most growth of C. maritima along a coastal recent site to be added to the University stretch of Point Reyes National Seashore of California Reserves in partnership with in Marin County, California. Abiotic factors the U.S. National Park as of August 2017.

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With the establishment of this site, mass were separated upon excavating an rangers have been able to adopt practices individual plant and measured separately. that help preserve both floral and faunal endangered species. Currently, Point The root:shoot ratio was calculated Reyes is focusing on preserving and using the following equation: improving the habitats of the threatened root mass (g) Root: shoot ratio = Western Snowy Plover on coastal beaches shoot mass (g) and the restoration of coastal dunes. Coastal dunes are prone to plant invasion Measurements were taken between due to the low richness of native species August 3rd and August 6th, 2017 at three adapted to harsh coastal conditions and distinct sites along Great Beach with an ar frequent disturbance by strong wind ea of 5.7 acres in the coastal dune habitat (Boyd 1992). European sea rocket (Cakile located south of Abbott’s Lagoon. maritima) is one such invasive plant that has disrupted the population of silver We assessed the effects on growth and lupine (Lupinus albifrons) as well as many resource allocation of three abiotic other native species. There is very little factors: elevation, site, and distance from accessible information regarding how C. the ocean. Elevation was used as an maritima interacts with other plant approximation of the distance from the species in North America, which makes water table, which serves as rough physiology-based restoration strategies estimate of groundwater availability. The for the species difficult to establish. value was recorded by GPS and calibrated with Google Earth due to equipment error Research Design related to thick cloud cover during the study period. Distance away from the This study aims to understand the ocean was used to describe the salinity, abiotic and biotic factors that may limit which is proportionally associated with the growth of C. maritima. We measured the travel distance of ocean spray. The total biomass and root:shoot ratio by coordinates of each plant were recorded mass to reflect the growth and by GPS and processed by Google Earth to belowground resource stress of C. calculate the distance from the ocean for maritima by uprooting individuals with each plant. Three sites were selected to roots intact. Total biomass acts as an represent topographical variation, sorted indicator of overall growth; root:shoot into ocean-facing foredunes, inland-facing ratio indicates the allocation of resources backdunes, and a flat, distal inland valley between belowground resource (Fig. 1); each site additionally featured a acquisition for survival and reproductive distinct distance from the ocean. Sunlight ability, as root:shoot ratios are more was not considered as a limiting factor due responsive to belowground pressures to high sun exposure in the dunes. In than those aboveground (Wilson 1988). addition, equipment limitations disallowed Total biomass was measured with spring for direct measurement of nutrients, which scales in grams. Root mass and shoot were estimated with a biotic proxy.

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Plants surrounding C. maritima Statistical Analysis individuals were sorted into three functional guilds: native nitrogen fixers, Statistical analyses were performed in non-nitrogen-fixing native competitors, the JMP Statistical Software package 13.0. and invasive competitors. Nitrogen fixers We used two-tailed T-tests and the Bivariate Fit Model to examine the can convert atmospheric nitrogen (N2) variation in the effects of biotic factors, into ammonium (NH4) or other molecules that can be utilized by a plant and benefit including both number of individuals and the surrounding plants by leaving presence or absence of surrounding plant remnants of usable nitrogen in the soil. species. Surrounding plants were defined as plants Variation caused by abiotic factors was located within a 1 m radius centered at analyzed using one-factor ANOVAs. Due each individual C. maritima root. Each to large sample size, distance from the surrounding plant was identified and ocean was approximated using three site classified into one of the three categories locations; the sites had distinctly different stated above. In addition, the abundance distances from the ocean. of each surrounding plant was recorded. RESULTS C. maritima individuals were selected randomly by generating a direction and Over the course of four days, 228 distance to travel before assessing the samples were collected to test total nearest plant. biomass and root:shoot ratios. Elevation showed no significant impact on growth performance (total biomass: F = 0.48, P > 0.20; root:shoot ratio: F=1.00, P > 0.20). The backdune site with a medium distance away from the ocean showed significantly higher biomass (F = 3.80, P < 0.05), and significantly lower root:shoot ratio (F = 13.57, P < 0.0001) compared to the other two sites.

For biotic factors, 15 different plant species were found within a 1-meter radius of C. maritima, including two nitrogen fixers, nine native competitors, and four invasive competitors. The presence of nitrogen fixers significantly increased biomass (F = 2.20, P < 0.05; Fig. Figure 1. The study system and its three 2a) and decreased root:shoot ratios (F = - sampling sites. The three sites were located along a stretch of coastal dune habitat and 3.39, P = 0.001; Fig. 2b). varied in topography and distance from the ocean.

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DISCUSSION

The results of our study suggest a correlation between biotic interactions and C. maritima performance. The presence of nitrogen fixers, i.e. native yellow bush lupine (Lupinus arboreus) and Tidestrom’s lupine (Lupinus tidestromii), significantly reduced belowground stress, allowing for higher biomass and a lower root:shoot ratio.

Nitrogen fixers increase the accessible nitrogen near C. maritima, thereby reducing the need to develop long, extensive roots and allowing the plant to allocate more resources to shoot growth. Shoot length is crucial to the reproductive success of C. maritima; a seed being dispersed more than 1 m away from the mother plant significantly increases survival (Barbour 1970). Nitrogen fixers may thereby facilitate the extension of C. maritima invasion by increasing their reproductive success. Figure 2. Effects of nitrogen fixer presence on (A) total biomass and (B) root:shoot Both native and invasive competitors mass ratio. The results shows significantly decreased the performance and increased higher biomass and lower root:shoot ratio with belowground stress of C. maritima. The the presence of nitrogen fixers. presence of native competitors may cause Inversely, the presence of native the plant to have a lower biomass and competitors significantly decreased allocate more resources to the root, but biomass (F = -4.74, P < 0.0001; Fig. 3a) and with an increase of the abundance of increased root:shoot ratio (F = 4.30, P < native competitors, the change in growth 0.0001; Fig. 3b). The abundance of performance is not significantly different. invasive competitors decreased biomass (F = 22.39, P < 0.0001; Fig. 4a) and increased root:shoot ratio (F = 18.77, P < 0.0001; Fig. 4b). An overview of the effects from surrounding species to C. maritima are summarized in Table 1.

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Figure 4. Effects of invasive competitor Figure 3. Effects of native competitor presence on (A) total biomass and (B) presence on (A) total biomass and (B) root:shoot mass ratio. Greater numbers of root:shoot mass ratio. Results showed invasive competitors surrounding C. significantly lower biomass and higher maritima were associated with reduced total belowground resource allocation (root:shoot biomass and greater relative prioritization of ratio) with the presence of native competitors. belowground resource allocation.

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Table 1. Summary of C. maritima biomass and belowground resource allocation (root:shoot) by nearby plant guilds. Belowground resource allocation indicating increased water or nutrient stress is indicated by ln[Root-to-shoot ratio]; total growth is represented by ln[Biomass]. Surrounding plants were classified into native nitrogen-fixers, native competitors, and non-native competitors. Both species presence/absence and species abundance were examined and listed with F/T ratio, P value, and R- square if applicable. Asterisks indicate significance. NA = Not Applicable.

Unlike native competitors, the presence native competition, the native roots are of invasive competitors significantly too short to pose an issue at any lowers the biomass but not the root:shoot abundance. More research into the root ratio, while the abundance of invasive system structure of the native and non- competitors significantly impact both native competitors is recommended to variables. Thus, native competitors better understand this relationship. negatively effect of C. maritima by their presence, and invasive competitors Abiotic components of coastal dune negatively affect C. maritima by both ecosystems measured by this study had a presence and abundance. This is likely the less reliable correlation with C. maritima result of a decrease in water availability in performance and belowground resource the soil causing the plant to either stress. The backdune site at an increase its resource investment in roots intermediate distance from the ocean or decrease overall size. Resource featured greater biomass and allocated investment in longer roots and decreased less resources to their roots, indicating investment in overall size takes away from the slightly sheltered dune area provided the plant’s ability to grow longer shoots less stress. This result is consistent with an and disperse its seeds farther. This earlier finding that the mortality of suggests that competitors decrease C. American sea rocket (C. edentula) was maritima reproductive success. higher closest to the ocean and farthest from the ocean compared to an One possible explanation for abundance intermediate distance. This was previously having little effect on resource allocation hypothesized to be due to high wave and or biomass in relation to natives may be wind stress near the ocean and lack of that competition from native competitors water or nutrients inland, where there is is limited by their maximum root length, little nutrient-providing detritus carried by and once C. maritima allocates enough waves (Payne & Maun 1984). Ocean salt resources to roots to grow beyond the spray and evaporation explain soil salinity

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gradients within varying distances from unknown where the species first invaded, the ocean, with the most inland areas but we speculate that the greater growth being the most saline. According to the and reproductive success found on the study of salinity effects on C. maritima by backdune may have aided in the dispersal Ahmed Debez et al. in 2004, C. maritima of C. maritima from the sea to the inland requires a moderate salt concentration valley. From this perspective, three (Debez et al. 2004). The backdune site, at primary steps to managing the species an intermediate distance from the ocean, become apparent: plant native species exhibited this by having higher biomass immediately following the removal of and lower root:shoot ratios relative to the non-native species, prioritize early other sites. Therefore, future restoration removal of invaders in backdune areas, efforts should focus on areas that have an and closely monitor areas with nitrogen- intermediate distance from the ocean. fixing species for signs of non-native colonization. When invasion of the species The results of this study could be used is noticed immediately, manual removal to pinpoint coastal dune sites that are at of fruits and seedlings may be sufficient high risk of C. maritima invasion. Sites for management of C. maritima. abundant with nitrogen fixers, low in competitors, and an intermediate Misunderstanding the life history of an distance from the ocean can be targeted invasive species when planning a for restoration and preventative measures restoration project is very costly in terms to halt invasion before it becomes of both money and time. It is imperative unmanageable and spreads to less to continue physiological research on vulnerable sites. invasive species to establish preventative measures and restoration guidelines for This study provides some insights on the early stages of invasion while a species is physiology of C. maritima that is needed still manageable and it is possible to to construct effective restoration extirpate the entire population. Not only strategies. Our findings are consistent will these efforts preserve California’s with the history of C. maritima in Point precious dune ecosystems through Reyes National Seashore: once the non- preserving their current states, native competitor A. arenaria was restoration will promote the resumption removed, the sand previously stabilized of traditional successional regimes and and dominated by the grass was open to assist in the renewal of the endemic and C. maritima invasion. The species was endangered populations that depend on largely free of competition in the newly- the coastal dune ecosystems. restored area; A. arenaria had dominated over the natives. C. maritima colonized ACKNOWLEDGEMENTS and was able to grow and disperse, likely establishing itself in areas with We would like to thank the UC Natural competitors but faring less well. It is likely Reserve System for the opportunity to that nitrogen fixers aiding reproduction learn from experienced reserve managers, promoted the spread of the species. It is course alumni, and a varied array of

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experienced ecologists over the course of Biodiversity and hotspots for conservation the California Ecology and Conservation priorities. Nature 403:853–858. field quarter. We are especially grateful Payne, A. M., & Maun, M. A. (1984). for the support given to us by our course Reproduction and survivorship of Cakile professors Kenwyn Blake Suttle and Krikor edentula var. lacustris along the Lake Huron Andonian. Special thanks go to course shoreline. American Midland Naturalist, 86– 95. alumnus and Point Reyes National Seashore restoration intern Michael Pardini, E. A., Vickstrom, K. E., & Knight, T. M. Spaeth for his knowledge of the local 2015. Early successional microhabitats natural history of C. maritima and allow the persistence of endangered plants assistance with locating suitable research in coastal sand dunes. PloS ONE, 10, e0119567. sites. Pickart, A. J. 1997. Control of European REFERENCES beachgrass (Ammophila arenaria) on the west coast of the United States. Barbour, M. G. 1970. Seedling ecology of Cakile Proceedings of the Symposium of the maritima along the California coast. Bulletin California Exotic Pest Plant Council. The of the Torrey Botanical Club, 280–289. Nature Conservacy Lanphere-Christensen Dunes Preserve, Arcata, California. Boyd, R. S. 1992. Influence of Ammophila arenaria on foredune plant Raven, P. H., and D.I. Axelrod. 1978. Origin and microdistributions at Point Reyes National relationships of the California flora (Vol. Seashore, California. Madroño 39:67–76. 72). University of California Press, Berkeley, California. Debez, A., Hamed, K. B., Grignon, C., & Abdelly, C. (2004). Salinity effects on germination, Sansing, J., H. Chapman. 1978. Statement for growth, and seed production of the Management: Point Reyes National halophyte Cakile maritima. Plant and soil, Seashore. 2–3. 262(1–2):179–189. Wilson, J.B. 1988. Shoot competition and root Muldoon, C. A. United States Department of the competition. Journal of Applied Ecology Interior. National Park Service: Point Reyes 25:279–296. National Seashore. 2009. Young, T. Coastal Communities. 2017, May 10. Myers, N., R.A. Mittermeier, C. G. Mittermeier, California Plant Communities. Lecture. G. A. B. de Fonseca, and J. Kent. 2000. Young Hall, Davis, California.

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