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The Role of Soil Chemistry in the Geographic Distribution of Ceanothus otayensis (Rhamnaceae)

Abstract Ceanothus otayensis McMinn (Rhamnaceae) was previously known only from metavolcanic-derived soils of the northern Peninsular Ranges—predominantly the San Ysidro Mountains—in San Diego County, California, and adjacent Baja California, Mexico. Recently, a new population of C. otayensis was discovered on sedimentary soils at Marine Corps Air Station Miramar, 25 km northwest of the next nearest known population. Sedimentary deposits at the new locality are thought to produce unusual soils. It is possible that the disjunct distribution of C. otayensis is a response to soil conditions, a phenomenon frequently seen in other members of Ceanothus, for instance on serpentine. The present study uses soil chemistry data for seven populations and subpopulations of C. otayensis (metavolcanic: n  =  5; sedimentary: n  =  2), as well as 22 populations of closely related Ceanothus, to determine whether soils of C. otayensis are chemically distinct from those of closely related Ceanothus, and answer the following question: are sedimentary-derived soils at the new locality chemically similar to metavolcanic-derived soils that support all other known populations of the species? Soils of C. otayensis proved to be chemically distinct from soils of closely related Ceanothus, with significantly lower levels of nitrate, sulfur, and conductivity. Sedimentary and metavolcanic soils of C. otayensis proved to be chemically indistinguishable from one another (P < 0.05), with low levels of all assayed nutrients other than Ca, suggesting a chemical similarity among the soils of C. otayensis that may help explain its disjunct distribution. Population size estimates indicate that the new disjunct locality at Marine Corps Air Station Miramar supports about 75 adult individuals.

Plant-soil interactions are a primary driver of plant distribution, as well as a potentially potent force in plant evolution (Stebbins 1942;Kruckeberg 2002;Kay et al. 2011). Unusual soils-such as serpentine-have long been known to support unusual plant communities, including many species that are endemic to such soils, and likely specialized via local adaptation (Gankin and Major 1964;Kruckeberg 1986;O'Dell and Rajakaruna 2011). Although several such ''edaphic endemic'' taxa have been examined using modern soil chemistry and experimental tools (Baldwin 2005;Sambatti and Rice 2006;Burge et al. 2013), little is presently known about how soil conditions influence adaptation and geographic distribution in such plants, particularly those that are specialized to soils other than serpentine. By examining specific cases of edaphic endemism using soil chemistry data, it may be possible to discern general trends in the evolution and maintenance of soil associations in edaphically specialized species or plant communities.
The present contribution focuses on Ceanothus otayensis McMinn, a member of Ceanothus subgenus Cerastes S. Wats. Ceanothus otayensis is a low-stature, ascending shrub that is morphologically similar to Ceanothus perplexans Trel. and Ceanothus crassifolius Torr. (Boyd and Keeley 2002), and was once thought to have arisen via hybridization between these two species (McMinn 1942). However, neither of the putative parent species is present within the geographic range of C. otayensis, and genetic evidence does not support a hybrid origin (Burge et al. 2011).
Ceanothus otayensis was previously thought to occur only on metavolcanic-derived soils of the Peninsular Ranges in southern San Diego County, California, and adjacent Baja California, Mexico (McMinn 1942;. Ceanothus otayensis, along with a small group of species endemic to the San Ysidro Mountains, has been treated as a specialist on metavolcanic-derived soils. Such soils are thin, extremely rocky, and very fast-draining (Bowman 1973). However, very little research has focused on the chemical and physical properties of these soils, or their potential influence on plant life.
During a visit to the San Diego Natural History Museum, the author came upon a specimen of C. otayensis collected at Marine Corps Air Station Miramar (hereafter MCAS Miramar; Roberts & Dossey 6209; Appendix 1), 25 km to the northwest of the next nearest known population (Figs. 1 and 2). In 2009, the author visited the locality and was able to locate a small population of these plants (estimated at the time MADROÑ O, Vol. 61, No. 3, pp. 276-289, 2014 FIG. 1. Global distribution of C. otayensis. Locality data for C. otayensis taken primarily from the Consortium of California Herbaria (http://ucjeps.berkeley.edu/consortium); additional data from Jon Rebman (personal communication); only unique localities mapped (Appendix 2). Inset map of topography is from Jarvis et al. (2008). The present study uses chemical analysis of soils to answer two outstanding questions on the soil chemistry associations and distribution of C. otayensis: 1) Are the soils occupied by C. otayensis chemically distinct from those occupied by other members of Ceanothus subgenus Cerastes in California? and 2) Are the sedimentaryderived soils at the new MCAS Miramar locality chemically similar to the metavolcanic-derived soils that support other known populations of C. otayensis? Population size estimates for C. otayensis at MCAS Miramar are also presented, and conservation implications for this rare species are discussed.

Determining Geological Formations and Soil Types
To determine the general soil and geology associations of C. otayensis, a GIS approach was applied to available georeferenced specimens of the species. Occurrence data for sites other than those reported by DOB (Appendix 1) were obtained from the Consortium of California Herbaria (CCH 2013). Records were selected only if they explicitly provided latitude and longitude data on the label. Duplicates were removed using location; records with the same location-based on latitude and longitude rounded to three decimal places-were removed, resulting in a list of high-quality localities (Appendix 2).
Geological formations and soil types at individual sites were determined using a GIS approach, combined with reference to the geological and soil literature. Latitude and longitude data were used in the program DIVA-GIS v 7.5 (Hijmans et al. 2001) to infer general geology from the digital version of the 1:750,000 Geologic Map of California (Jennings et al. 1977;Saucedo et al. 2000). Local geology was inferred by visual examination of higher resolution physical or digital maps, including the Geological Maps of the Otay Mesa, La Mesa, and Jamul 7.59 Quadrangles (Kennedy and Tan 1977). Local soils were inferred using data from the Soil Survey Geographic (SSURGO) database for San Diego County, California, obtained from the United States Department of Agriculture Natural Resource Conservation Service (USDA 2007).

Soil Sampling
To quantify the soil chemistry associations of C. otayensis and closely related members of Ceanothus subg. Cerastes, soils were collected from 29 plant populations in California (Table 2, Fig. 1). The aim of this sampling was to obtain soils from as many C. otayensis populations as possible, and from a representative diversity of soils occupied by other members of Ceanothus subg. Cerastes. For the species other than C. otayensis, an effort was made to maximize the diversity of substrates represented in the dataset, and to sample from as many purported edaphicendemic taxa as possible. . Seven of the resulting samples were from populations or subpopulations of C. otayensis (5 metavolcanic from the San Ysidro Mountains; 2 sedimentary, from MCAS Miramar), and 22 were from species other than C. otayensis, representing 13 of the 23 currently recognized members of Ceanothus subg. Cerastes ) and all but one of the approximately eight edaphic-endemic members of this group (Table 2, Figs. 1 and 2). Sampling of soil was carried out in April and May 2009, and again in April 2013. The soil sampling procedure follows that of Burge and Manos (2011).

Soil Chemistry Assays
Soil chemistry analyses were done by the Texas A&M University Soil, Water, and Forage Testing Laboratory. Methods were as described by Burge and Manos (2011). In all, 13 soil properties were assayed (Table 3), including pH, nitrate (NO 3 2 ), electrical conductivity, major nutrients (P, K, Ca, Mg, and S), micronutrients (Cu, Fe, Mn, and Zn), and sodium (Na).

Analysis of Soil Chemistry Data
Soil chemistry data were treated in a multivariate statistical framework. Differences between sedimentary (MCAS Miramar; n 5 2) and metavolcanic (San Ysidro Mountains; n 5 5) soils of C. otayensis, as well as differences between the soils of C. otayensis and other species of Ceanothus subg. Cerastes from California (n 5 22), were summarized and tested using principal component analysis (PCA) and generalized canonical discriminant analysis (Gittins 1985). Principal components analysis was done in R version 2.10.1 (R Development Core Team 2013), using the ''ecodist'' package of Goslee and Urban (2007). Soil chemistry variables were transformed into Z-scores before analysis. Following analysis, the first two principal components were visualized in bivariate space and the contribution of different soil chemistry variables to the components was assessed using vector loading. Generalized canonical discriminant analysis was done in R (R Development Core Team 2013), using the ''candisc'' package of Friendly and Fox (2009). Wilks' Lambda was used to test for significant differences between the two groups based on the 13 soil chemistry variables (Friendly 2007).

Estimation of Population Size at MCAS Miramar
A transect approach was used to estimate the size of the C. otayensis population at its disjunct locality on MCAS Miramar. With the exception of a few outlying shrubs, C. otayensis at MCAS Miramar is restricted to a patch of extremely dense chaparral at the head of a tributary of San Clemente Canyon (Fig. 3). Because this patch is surrounded by open scrub, it was possible to walk the perimeter of the patch and count individual adult plants. Two observers (DOB and K. Zhukovsky) walked the margin of the chaparral patch ( Fig. 3), pausing approximately every 5 m to tally the number of new individuals observable in a line across the canyon. In addition, the surrounding portions of Kearny Mesa and upper San Clemente Canyon were explored on foot (Fig. 3), and additional outlying individuals of C. otayensis were noted. The position of isolated individuals was recorded using a hand-held GPS and the WGS84 datum. All work for the population size estimate was carried out on 18 April 2013.

Geological Formations and Soil Types
Using the CCH database and collections obtained specifically for this project, 19 unique C. otayensis localities were identified (CCH 2013, Appendix 2). Fourteen of these are in the Peninsular Ranges of southern San Diego County, California and northern Baja California, Mexico (San Ysidro Mountains and San Miguel Mountain; Fig. 1), and two are at the recently discovered locality at MCAS Miramar in northern San Diego County. Inferred geological and soil formations for these sites (Appendix 2) indicate that three major groupings of sites are present (Table 1) Table 1). At the second set of localities, by contrast, the rocks are classified as volcanic or metavolcanic; soils are classified as San Miguel-Exchequer rocky silt loams and metamorphic rock land (Table 1). The final locality, from Baja California, Mexico, is apparently on soils derived from andesite, a volcanic rock type (Appendix 1; Table 1). However, this rock is likely metavolcanic, based on the geological setting and field observations by the author (2009).

Soil Chemistry
In comparison to the soils of other Ceanothus species assayed, the soils of C. otayensis have, on average, lower pH, lower electrical conductivity, lower concentrations of nitrate, and lower levels of every assayed nutrient other than potassium, sodium, zinc, and manganese (Table 3). These differences are significant in the case of conductivity, nitrate, sulfur, and sodium (Student's paired t-tests, P , 0.03). In comparison to C. otayensis from metavolcanic soils of the San Ysidro Mountains (n 5 5), the soils of C. otayensis from MCAS Miramar (n 5 2) have nearly identical levels for all of the assayed chemical properties (Table 3); there were no significant differences for any of these properties (Student's paired t-tests, P . 0.05).
Principal components analysis and canonical discriminant analysis provide a summary of the results for the 13 soil chemistry variables (Fig. 4). In the case of PCA, the first two principal components account for 50% of variance, with 30% on the first principal component and 20% on the second. The first principal component is strongly positively correlated with conductivity (vector loading 5 0.45) and iron (vector loading 5 0.44), and strongly negatively correlated with phosphorous (vector loading 5 20.13).
In canonical discriminant analysis, three groups (1, C. otayensis MCAS Miramar; 2, C. otayensis San Ysidro Mountains; and 3, other species; Table 2) were used to transform soil chemistry variables into canonical space (Fig. 5). A single coordinate axis accounted for 100% of the variance, and the Wilks' Lambda test (approximate F 5 4.06) allowed for rejection of the null hypothesis of no difference between the means for the three groups (P 5 0.005). Examination of the canonical discriminant plot (Fig. 5) indicates that this pattern is driven by the difference in chemistry between soils of C. otayensis and the other species. To test this, a two-tailed t-test was carried out using vector loadings from the first and second principal components of the PCA (Fig. 4), using the two C. otayensis localities (MCAS Miramar and San Ysidro Mountains) as groups. This test indicated that the two groups are not distinguishable on the basis of the first or second principal component axes (P 5 0.95 and P 5 0.39, respectively).

Population Size at MCAS Miramar
A total of 74 individual shrubs of C. otayensis were observed during the transect work (Fig. 3). All individuals were mature, many of them in heavy fruit at the time of observation. No seedlings were observed. Many of the C. otayensis individuals were senescent. A few isolated individuals of C. otayensis were observed in the vicinity of the core population at the head of San Clemente Canyon (Fig. 3; Burge 1378; Appendix 1; Table 2), but no other populations were located at MCAS Miramar.
DISCUSSION Soils of C. otayensis from the two disjunct population centers (Figs. 1 and 2; San Ysidro Mountains and MCAS Miramar) are chemically indistinguishable (Fig. 5), which is surprising given the very different geological origin of these materials (Table 2); those from the San Ysidro Mountains region have arisen from metavolcanic rocks, while those from MCAS Miramar are from sedimentary rocks, including Quaternary alluvium and more ancient conglomerate (Appendix 2). The chemical similarity of these soils may help to explain the disjunct occurrence of C. otayensis at MCAS Miramar, 25 km northwest of other known populations (Figs. 1 and 2).

Substrate Associations
Results presented here indicate that edaphic conditions experienced by C. otayensis represent a cohesive and distinctive subset of conditions

LOCALITIES.
Group refers to the three general groupings of localities mentioned in the body of the paper (Fig. 1). Region refers to geographic regions (Fig. 1). Collection number refers to the herbarium sheet upon which the record is based (Appendix 2). General geology is from the Geologic Map of California (Jennings et al. 1977); data for Burge 1063 is from Reconnaissance Geology of the State of Baja California (Gastil et al. 1971).
Local geology is from Geology of La Mesa, Jamul, and Otay Mesa 7.59 Quadrangles (Kennedy et al. 1977

Burge 1063
Volcanic (Tpa)* -from those supporting other Ceanothus species in California and adjacent Mexico (Fig. 4). Soils of C. otayensis contain notably small amounts of nitrate and P, low availability of which is known to result in disorders affecting the growth and reproduction of crop plants (Brady and Weil 2002). The soils also have low pH and conductivity, which is probably due to generally low levels of nutrient and other ions (Table 3).
Geospatial data on geological formations and soil types show that the geology and soils of C. otayensis from the San Ysidro Mountains and San Miguel Mountain are highly consistent (Table 2; Appendix 2), with metavolcanic geology giving rise to soils from two series, the San Miguel-Exchequer rocky silt loams and Metamorphic rock land. Metavolcanic rocks of the San Ysidro Mountains and San Miguel Mountain are part of  ; Code D. O. Burge collecting code; Locality country, state, and county for sampling (also see Appendix 1); all collections by DOB, all deposited at DUKE; Soil Type geological material from which soil is derived, with codes from Geological Map of California in parentheses (Jennings et al. 1977  Hesperocyparis forbesii (Jeps.) Bartel (Cupressaceae). Many of these species are also known from gabbro-derived soils of San Diego County, which often support a unique suite of rare species (Zedler 1995, Alexander 2011. The presence of these rare taxa on both metavolcanic and gabbro rock suggests that there may be some chemical similarity between soils derived from this material, as the present paper shows for the metavolcanic-derived and sedimentary soils of C. otayensis. Future work should compare the substrate associations of these species. Such work would likely aid in the management of these rare and poorly-known taxa. Sedimentary soils like those at the MCAS Miramar locality are also known to support a diverse and unusual flora, possibly due to the low pH that prevails on some soils (Crocker 1956). However, most of these species are vernal-pool endemics or associates. Ceanothus otayensis, a shrub normally associated with chaparral habitats, thus provides an unusual counterpoint to the typical pattern of endemic plant diversity at important to also consider populations from Baja California, Mexico. In the case of C. otayensis, a population of the species is known to occur near the summit of Cerro Jesú s María in Baja California, one of the southern peaks of the San Ysidro Mountains (Fig. 1). Here, it appears to occur on andesite-derived (volcanic) soils (Appendix 1). It would be helpful to obtain soil samples from this locality for future work involving the evolution and ecology of C. otayensis. It would also be helpful to analyze soil samples from the populations of plants that have been reported from San Miguel Mountain in San Diego County (Keeley 27100-27117, Rebman 24367; Appendix II).

Evolution of Soil Specificity
Although my work does not directly address the evolutionary history of the new, disjunct C. otayensis population on Kearney Mesa at MCAS Miramar, it is possible to speculate on the historical events that may have led to the present distribution of the species. One possibility is that the population at MCAS Miramar is the product of a recent dispersal event from the south, and has been able to persist in the new, unusual habitat due to the amenable chemistry of the soils. Alternatively, plants at MCAS Miramar may be relictual, isolated by the loss of plant populations in the region separating MCAS Miramar from the San Ysidro Mountains and San Miguel Mountain. It is intriguing to note that metavolcanic rocks, as well as sedimentary formations of the same type found at the MCAS Miramar locality, are broadly distributed in a continuous band from the San Ysidro Mountains region to north of MCAS Miramar (Fig. 2). It is possible that some of these areas support other small, undiscovered populations of C. otayensis.
The soils of C. otayensis are chemically similar to soils that support another narrowly-endemic Ceanothus species, Ceanothus roderickii Knight, which is known from gabbro-derived soils of the central Sierra Nevada (Fig. 4; Burge and Manos 2011). Recent research on C. roderickii indicates that the chemistry of its soils may provide a powerful agent of natural selection, possibly leading to reduced gene flow with closely related species, local adaptation, and speciation (Burge et al. 2013). If this hypothetical mode of divergence and speciation is common in Ceanothus, it may help explain the origin of C. otayensis, as well as several other narrowly-endemic Ceanothus species from southern California and nearby Baja California, including Ceanothus ophiochilus S. Boyd, T. S. Ross, & Arnseth on pyroxenite-rich gabbros of Riverside County (Boyd and Arnseth 1991), and Ceanothus bolensis S. Boyd & J. Keeley on metavolcanic rocks of Baja California's Cerro Bola (Boyd et al. 2002).
In general, it would be worthwhile to make a broader test of soil chemistry associations across the ten or so supposedly edaphic-endemic members of Ceanothus subg. Cerastes, to determine whether there is a consistent syndrome of edaphic adaptation across the group. Such work should ideally include common garden experiments, reciprocal transplant experiments, and more detailed analyses of other soil parameters that are potentially related to the chemical parameters, such as moisture availability. This would help to overcome the limitations of this and many similar studies, which often rely on purely observational data from a small suite of chemical soil properties.

Status of the New Population and of the Species
Ceanothus otayensis is on list 1B.2 of the California Native Plant Society Inventory of Rare and Endangered Plants (CNPS 2014), meaning that it is rare in California as well as in its other areas of distribution (in this case Baja California, Mexico). Ceanothus otayensis is facing a number of significant threats throughout its geographic range. The major threat to the persistence of the species is likely fire regime; C. otayensis is an obligate seeding species that requires fire for recruitment . However, too frequent fire has been shown to eliminate obligate seeding species from chaparral habitats in southern California (Zedler 1995 FIRE 2014). These were two of the largest fires in the recorded history of California (CAL FIRE 2014), and both burned substantial portions of C. otayensis habitat in the San Ysidro Mountains and nearby Peninsular Ranges, including portions in Baja California, Mexico. Short fire intervals of this kind will probably result in the extirpation of C. otayensis populations that are unable to reach sexual maturity between fires.
Though populations of C. otayensis in the San Ysidro Mountains are large and seem reasonably secure, the smaller populations at San Miguel Mountain and MCAS Miramar could suffer drastic losses in the event of future fires. For example, virtually the whole of San Miguel Mountain was burned in the 2007 Witch Creek Fire (CAL FIRE 2014), including the portion of the mountain where C. otayensis was most recently recorded (Keeley 27100-27117, Rebman 24367; Appendix 1).
As discussed above, the new record of the species from MCAS Miramar represents a significant expansion of the ecological and geographic range known for the species. The new locality at MCAS Miramar brings the total number of population centers for the species to three, one in the San Ysidro Mountains, a second on San Miguel Mountain, and a third, now, at MCAS Miramar (Fig. 1). Nevertheless, the population at MCAS Miramar is extremely small, seemingly consisting of no more than 74 mature plants. Although the size of the nearest C. otayensis population on San Miguel Mountain is also very small (probably no more than 100 individuals as of 2010, Jon Rebman personal communication), population sizes in the San Ysidro Mountains are generally significantly larger, consisting of thousands of plants, becoming a co-dominant member of the chaparral plant community at higher elevations. The very small size of the C. otayensis population at MCAS Miramar makes it especially vulnerable to loss. In such populations, chance events such as wildfire, flooding, or disease introduction can lead to drastic losses of individuals, and possibly local extinction. In addition, the population genetic status of this small population is unknown. If the population is derived via a recent dispersal event from the southern populations, it may suffer from a lack of genetic diversity due to a population bottleneck (Ellstrand and Elam 1993). On the other hand, if the plant at MCAS Miramar is a relictual population, isolated by the loss of plant populations in the region separating Kearny Mesa from the San Ysidro Mountains, it may harbor unique genetic variation not present in the southern populations. Future work should aim to quantify population genetic variation across the range of C. otayensis, especially in isolated population centers, such as those at MCAS Miramar and San Miguel Mountain.

ACKNOWLEDGMENTS
The author thanks Katherine Zhukovsky, Jon Rebman, and Dieter Wilken for providing constructive criticism of drafts. Assistance with field work and field logistics was provided by Katherine Zhukovsky, JoEllen Kassebaum, and Joyce Schlachter. Funding was provided by the American Society of Plant Taxonomists, The Hunt Institute for Botanical Documentation, Duke University, and a National Science Foundation grant to DOB and PSM (NSF 000457253).