Factors Regulating Population Stand Structure in Blackbrush (Coleogyne ramosissima: Rosaceae), a Masting North American Desert Shrub

Abstract

Blackbrush (Coleogyne ramosissima Torr.) is the dominant shrub on three million hectares across the transition zone between the western North American warm and cold deserts. This paper presents a study of blackbrush population structure at the stand level at sixteen sites across the species range. New stand-level information is then integrated with what is already known about blackbrush population ecology to explore the stand-level consequences of several unusual features of blackbrush life history, including its masting reproductive strategy, its interactions with heteromyid rodents that are both seed predators and dispersers, and its ability to form ‘seedling banks’ of growth-suppressed individuals, often within the crowns of adult conspecifics. It complements earlier work showing that blackbrush stands are organized at both the inter-clump and intra-clump levels. Each clump represents an establishment nexus where younger individual genets replace older genets over an extended time period. Inter-clump structure is thus determined by the rate of establishment of new clumps rather than new individuals. This has resulted in contrasting stand structures in response to rodent community composition, disturbance regimes, and climatic variability at the leading and trailing edges of current blackbrush distribution in the eastern Mojave Desert and Colorado Plateau regions. Because blackbrush likely disperses too slowly to track anthropogenic climate change, assisted migration with wild-collected seeds may be necessary to promote its continued survival and dominance.

1. Introduction

Blackbrush (Coleogyne ramosissima Torr) occurs as a dominant xerophytic shrub species on shallow, infertile soils at middle elevations across much of the Mojave Desert and Colorado Plateau regions of western North America (Figure 1A–D). It is an important ecotonal species in the transition zone between warm and cold deserts, occurring as the dominant species on approximately three million hectares. Coleogyne is a monotypic outlier genus in the small tribe Kerrieae (Rosaceae) and is not closely related to any other desert shrub. It has often been described as a paleoendemic because of its taxonomic isolation and long history in the region [1], but recent studies by myself and my research partners have shown that it has high genetic diversity, with strong ecotypic differentiation across its large geographic range [2,3]. One objective of the present work is to examine how this ecotypic differentiation is expressed in terms of population dynamics at the stand level.

The older literature on blackbrush (Coleogyne ramosissima) population dynamics paints a picture of a slow-growing, long-lived shrub that forms essentially monospecific stands over large areas of suitable habitat and that maintains its dominance in this habitat over long periods of time in the absence of catastrophic disturbance [4,5,6,7]. It is considered very slow to recover following disturbance, particularly after large-scale disturbance such as fire [8,9] or debris flows [7,10]. This has commonly been attributed to infrequent seed production, limited dispersal potential, rare recruitment from seeds, and poor survival in the juvenile age classes. Similar population-dynamic models have been proposed for some other long-lived dominant warm desert shrubs, and these have been largely confirmed in subsequent studies [11,12]. In general, the recruitment of conspecifics into established stands is very rare in populations of late-seral warm desert shrubs [13,14]. Instead, they often have mechanisms, such as clonal growth in creosote bush (Larrea tridentata), that promote extraordinary longevity [15]. Our more recent studies on seed production, dispersal, recruitment, and juvenile survival have provided evidence that this model for desert shrub persistence may not apply to blackbrush [16,17,18,19,20]. These studies also show that blackbrush population dynamics can exhibit major spatial variability on regional and local scales as well as through time.

Table 1. Site information for 16 study sites included in the blackbrush stand characterization and community ecology studies. * Included in the within-clump demographic study [18]. ** Included in the post-2002-drought mortality study.

Site Code	Site Name	Latitude	Longitude	Elev (m)	Mean Soil Depth (cm)	Substrate	Mean Annual Precip. (mm)	Mean Jan Min Temp (°C)
	Spring Mtns. NV
BDI	Blue Diamond Turnoff	36°01′51.08″ N	115°23′08.23″ W	1041	26.1	limestone	178	0.79
RRO	Red Rocks Overlook	36°06′58.86″ N	115°26′40.49″ W	1174	16.8	limestone	224	0.15
LPT	Lower Potosi	35°59′48.92″ N	115°28′19.11″ W	1451	--	limestone	314	−1.38
PPS	Potosi Pass	36°00′52.77″ N	115°29′58.20″ W	1667	--	limestone	353	−2.11
	Beaver Dam Mtns. UT
CCL	Castle Cliff **	37°04′23.10″ N	113°52′21.26″ W	1213	39.0	limestone	305	2.21
WHL	* Winchester Hills **	37°13′25.30″ N	113°37′53.89″ W	1227	48.8	sandstone/basalt	312	−0.21
VYR	* Veyo Road **	37°16′24.30″ N	113°38′37.98″ W	1423	71.0	shale	352	−1.01
BDS	* Beaver Dam Summit **	37°06′01.14″ N	113°49′19.89″ W	1484	23.6	igneous intrusive	331	1.13
	St. George Basin UT
LGR	* LeGrande	37°10′33.30″ N	113°20′18.50″ W	985	74.4	sand/ basalt	280	−1.14
TOQ	* Toquerville Turnoff	37°16′47.82″ N	113°18′41.20″ W	1164	44.2	basalt	322	−1.70
BRW	Browse Turnoff **	37°21′43.47″ N	113°15′51.67″ W	1295	21.0	igneous intrusive	359	−3.17
	Colorado Plateau UT
HIT	Hite **	37°53′21.59″ N	110°24′50.96″ W	1232	12.5	shale	227	−4.67
DDT	* Dirty Devil Turnoff **	38°09′34.64″ N	110°37′14.66″ W	1500	30.6	sandstone	177	−8.49
NHK	* North Hanksville **	38°47′35.90″ N	110°26′12.28″ W	1343	74.4	sandstone	168	−9.40
LRK	* Little Rockies	37°45′35.54″ N	110°39′06.30″ W	1700	24.0	igneous intrusive	230	−5.96
SLV	Salt Valley (Arches NP)	38°45′40.65″ N	109°36′02.04″ W	1497	77.4	sandstone	242	−8.00

Table 1. Site information for 16 study sites included in the blackbrush stand characterization and community ecology studies. * Included in the within-clump demographic study [18]. ** Included in the post-2002-drought mortality study.

Site Code	Site Name	Latitude	Longitude	Elev (m)	Mean Soil Depth (cm)	Substrate	Mean Annual Precip. (mm)	Mean Jan Min Temp (°C)
	Spring Mtns. NV
BDI	Blue Diamond Turnoff	36°01′51.08″ N	115°23′08.23″ W	1041	26.1	limestone	178	0.79
RRO	Red Rocks Overlook	36°06′58.86″ N	115°26′40.49″ W	1174	16.8	limestone	224	0.15
LPT	Lower Potosi	35°59′48.92″ N	115°28′19.11″ W	1451	--	limestone	314	−1.38
PPS	Potosi Pass	36°00′52.77″ N	115°29′58.20″ W	1667	--	limestone	353	−2.11
	Beaver Dam Mtns. UT
CCL	Castle Cliff **	37°04′23.10″ N	113°52′21.26″ W	1213	39.0	limestone	305	2.21
WHL	* Winchester Hills **	37°13′25.30″ N	113°37′53.89″ W	1227	48.8	sandstone/basalt	312	−0.21
VYR	* Veyo Road **	37°16′24.30″ N	113°38′37.98″ W	1423	71.0	shale	352	−1.01
BDS	* Beaver Dam Summit **	37°06′01.14″ N	113°49′19.89″ W	1484	23.6	igneous intrusive	331	1.13
	St. George Basin UT
LGR	* LeGrande	37°10′33.30″ N	113°20′18.50″ W	985	74.4	sand/ basalt	280	−1.14
TOQ	* Toquerville Turnoff	37°16′47.82″ N	113°18′41.20″ W	1164	44.2	basalt	322	−1.70
BRW	Browse Turnoff **	37°21′43.47″ N	113°15′51.67″ W	1295	21.0	igneous intrusive	359	−3.17
	Colorado Plateau UT
HIT	Hite **	37°53′21.59″ N	110°24′50.96″ W	1232	12.5	shale	227	−4.67
DDT	* Dirty Devil Turnoff **	38°09′34.64″ N	110°37′14.66″ W	1500	30.6	sandstone	177	−8.49
NHK	* North Hanksville **	38°47′35.90″ N	110°26′12.28″ W	1343	74.4	sandstone	168	−9.40
LRK	* Little Rockies	37°45′35.54″ N	110°39′06.30″ W	1700	24.0	igneous intrusive	230	−5.96
SLV	Salt Valley (Arches NP)	38°45′40.65″ N	109°36′02.04″ W	1497	77.4	sandstone	242	−8.00

One of the most interesting discoveries to emerge from recently published studies on blackbrush is the realization that population structure is organized at two levels. Traditionally, a blackbrush ‘clump’ has been considered equivalent to a blackbrush plant, that is, the product of a single recruitment event [4]. At most, there has been recognition that the recruitment event, if it resulted from emergence from a rodent cache, might include multiple individuals, but the clump has been considered to represent members of a single age cohort [16]. Kitchen et al. [19] have shown based on rigorous and thorough clump excavation and dendrochronological analysis that many if not most blackbrush clumps of adult size are actually clusters comprising multiple individuals whose ages can span several decades. Thus, a blackbrush clump might better be called an ‘establishment nexus’, where multiple generations of plants grow together in a configuration that resembles a single multi-stemmed plant, and where younger recruits are likely to replace older plants as they senesce and die, leading to long-term clump persistence.

This study of blackbrush stand structure integrates new data on stand-level population structure for a set of representative populations from across the range with recently published information on seed production, dispersal, recruitment, and among- and within-clump plant age [16,17,18,19,20]. This provides support for an alternative model of blackbrush population dynamics and stand structure that is unique in the literature on desert shrubs, and that helps to explain how blackbrush stands can maintain their stable structure over long time periods. It also addresses the possible mechanisms by which blackbrush can colonize disturbances or expand its range, and how these processes might be limited by changed climate and disturbance regimes in the future.

2. Materials and Methods

Blackbrush stand characterization was carried out at 16 sites across the eastern two-thirds of the species range in Nevada and Utah, USA (Table 1, Figure 2). These 16 sites were also included in masting studies measuring temporal variability in reproductive output over a ten-year period [17]. Sites where intensive studies of seedling recruitment [16,18], within-clump age structure [19], and seed dispersal and predation [20] were carried are also included in this study, permitting direct comparisons among studies. We obtained GPS coordinates for each site and downloaded climatic data from the Prism Climate Group (https://prism.oregonstate.edu/explorer/ (accessed on 1 May 2023)) as is explained in more detail in [17]. Data were also collected on bedrock composition and approximate soil depth as measured by driving a steel rod into the ground until it met with definite resistance at ten points along a sample transect (Table 1).

For stand characterization at ten of the sites, a belt transect 5 m wide and 50 m long was divided into 2.5 m segments to make 20 12.5 m² plots totaling 250 m² in area. A larger plot size was employed at Hite because of very low densities (14 plots × 25 m²), while fewer plots (12 plots × 12.5 m²) were employed at the Little Rockies because of very high densities. At the four southern Nevada sites, variable numbers and sizes of plots result in sample areas of 300 m² at Blue Diamond Turnoff, 475 m² at Lower Potosi, 750 m² at Red Rocks Overlook, and 800 m² at Potosi Pass. These area differences were due to poor communication with field personnel; the differences had little or no effect on statistical error structure. Vegetation sampling took place at the different sites over a period of several years (1995–2003). This should not substantively affect comparisons, as blackbrush population structure is not expected to vary over short time periods [7,18,19].

Within each plot at each site, all blackbrush clumps were enumerated and measured (height and crown diameter). For clumps not close to circular in outline, the measurements were the maximum diameter and diameter perpendicular to the maximum diameter. All other woody species and succulents present in each plot were identified and enumerated (Supplemental Data Table S1). Herbaceous species frequency was also recorded, but because the data were collected at the different sites in different years and seasons, data for herbaceous species were considered not comparable and are not included.

At each site, the population sample contained at least 100 blackbrush clumps (Supplemental Data Table S2). To estimate blackbrush crown cover, crown diameter was converted to cover area using the formula for the area of a circle. In cases where two diameters were obtained, these were averaged prior to the calculation. Crown areas were summed across the sample area and divided by the total area to obtain blackbrush crown cover as a proportion of the area. To classify blackbrush clumps by size, the crown area was multiplied by the height to obtain an estimate of volume. Clumps were then classified into six size classes: <170 cm³ (post-seedling), <3220 cm³ (pre-reproductive), <50,300 cm³ (sub-adult), <488,000 cm³ (average adult), <1,045,400 cm³ (large adult), and >1,045,400 cm³ (very large adult). These volume classes were based on long-term field observations and corresponded to approximate height × crown diameter measurements of <6 cm × 6 cm (post-seedling), <16 cm × 16 cm (pre-reproductive), <40 cm × 40 cm (sub-adult), <85 cm × 85 cm (average adult), <110 cm × 110 cm (large adult), and >110 cm × 110 cm (very large adult), which are easier to visualize in the field.

Some of the eight sites where data were collected in 2003 showed considerable evidence of partial or even complete clump mortality, apparently as a consequence of severe drought conditions in 2002. For data taken in 2003, we included dead stems in blackbrush crown measurements to make the data comparable with sites sampled before the drought. We also estimated the proportion of each clump that had suffered mortality (Supplemental Data Table S2). Prior to the 2002 drought, we rarely noted evidence of even partial adult clump mortality, making it likely that the mortality observed in 2003 was a direct consequence of drought conditions the previous year. This gave us the opportunity to evaluate drought-related mortality as a function of site climate.

Differences in blackbrush stand attributes among sites were examined statistically using the analysis of variance for unequal sample sizes with plots as replicates (SAS Version 9.4, Proc GLM). Response variables included adult clump height and diameter, adult clump and total clump density, and total crown cover. Among-site differences in size class and drought mortality frequency distributions were evaluated using contingency table analysis with pairwise χ² tests using a Bonferroni-corrected significance level based on the number of pairwise comparisons (p < 0.0004 and p < 0.0014), respectively [21].

Contingency table analysis (p < 0.0004) was also used as a method for summarizing the community-level data set by evaluating among-site differences in adult blackbrush density relative to density of other woody and succulent species present. Categories in the plant community analysis included the dominants adult blackbrush, Ephedra spp., common succulents, and Gutierrezia sarothrae. Remaining species were grouped according to their regional distribution as characteristic of warm desert or foothill communities, or pooled in an ‘other species’ category. All χ² tests were carried out on count data underlying the proportions presented in the figures (Tables S1 and S2). This method was chosen over more complex multivariate techniques in order to place emphasis on the most important differences in community structure.

3. Results

3.1. Blackbrush Community Composition

Blackbrush was a dominant species in terms of woody plant density across all study sites (Figure 3). The absolute density of adult-sized blackbrush (height × crown > 40 × 40 cm) varied from 0.197 to 0.979 clumps-m⁻², while relative density varied from 50 to 94% of the total number of woody and succulent plants (Figure 3). The suite of regularly associated woody species in blackbrush stands was remarkably small, with only six species present in more than trace amounts (>1 plant-100 m⁻²) at three or more of the sixteen sites (Supplemental Table S1). Three of these were Ephedra species (E. viridis, E. nevadensis, and E. torreyana) and two were succulents (Opuntia erinacea and Yucca baccata). All are long-lived, stress-tolerant, late-seral species [10]. One early seral species, Gutierrezia sarothrae, occurred regularly at seven sites and was abundant at four sites, all of which had relative adult blackbrush densities <60% (Figure 3).

The commonly associated late seral species in blackbrush stands rarely occurred at high densities (Figure 3). However, both E. viridis and O. erinacea were common (>10 plant-100 m⁻²) at Salt Valley, while E. torreyana was common at the Little Rockies, and E. nevedensis was common at LeGrande and Winchester Hills. Other sites with lower relative densities of blackbrush were generally near either the upper or lower elevational limit for blackbrush, where it shared dominance with woody species characteristic of adjacent zones. For example, at Potosi Pass near the upper limit of its distribution, blackbrush was codominant with Artemisia tridentata, Juniperus osteosperma, and Pinus monophylla. Near the lower limit, at Red Rocks Overlook, associated species (e.g., Encelia frutescens, Hymenoclea salsola) were typically those associated with warm desert vegetation.

3.2. Blackbrush Stand Structure

The blackbrush total crown cover varied significantly among sites across the range, with an eightfold difference between the lowest value (8.5% at Hite) and the highest value (67.5% at Lower Potosi;

Table 2. One-way analyses of variance for a randomized design (Proc GLM, SAS 9.4) examining among-site differences in adult clump height, crown diameter, crown volume, and absolute density per m² for adult clumps, and absolute density per m² and absolute crown cover for all clump size classes combined (model d.f. = 15, error d.f. = 267 for all models).

Dependent Variable	F-Value	p-Value
Adult Clump Height	92.47	<0.0001
Adult Clump Crown Diameter	17.83	<0.0001
Adult Clump Crown Volume	22.25	<0.0001
Adult Clump Density	14.69	<0.0001
Total Clump Crown Cover	14.39	<0.0001
Total Clump Density	47.07	<0.0001

, Figure 4B). Sites heavily dominated by blackbrush in terms of relative density were often sites where blackbrush crown cover values were also high, for example, Lower Potosi and Veyo Road. An exception was North Hanksville, where the woody vegetation was dominated by blackbrush but crown cover was low (20%). Blackbrush crown cover averaged 40–50% at the Mojave Desert sites. On the Colorado Plateau, crown cover was lower (mean 24%).

There was a marked and significant difference in mean adult blackbrush height between the Mojave Desert and Colorado Plateau sites (Table 2, Figure 4C). The mean adult height at the Mojave Desert site ranged from 51 to 67 cm. The shorter mean heights were generally associated with more xeric sites (Table 1). On the Colorado Plateau, the mean clump height ranged from 38 to 45 cm, with no clear pattern by habitat. In contrast to the mean height, the mean crown diameter did not show consistent regional or habitat variation, possibly because it is more influenced by stand history and less by abiotic factors such as climate and soil depth (Figure 4D).

Absolute adult plant density also varied significantly among sites (Table 2, Figure 4A). Because of relatively minor differences among populations in the mean crown diameter values for adult clumps and the small contribution of smaller size classes to total crown cover, the adult absolute density and total crown cover were positively correlated (r = 0.806, n = 16, p < 0.001). Among the Mojave Desert sites, the highest absolute density values were found at the heavily blackbrush-dominated sites at middle elevation (e.g., Lower Potosi, Veyo Road) and the lowest values were usually at more xeric sites or sites with strong co-dominance by other species as discussed earlier. On the Colorado Plateau, adult blackbrush density at Hite was very low, while adult density at the Little Rockies was relatively high, and other sites had intermediate values.

3.3. Blackbrush Size Structure

Size class distributions varied significantly among sites (Figure 5). Most sites showed little evidence of recent recruitment (pre-reproductive or post-seedling size classes) into openings (Figure 3). Seven sites had post-seedling densities of zero, and another four sites had densities of <0.001 clumps-m⁻². Only three sites, the Salt Valley, Toquerville, and Little Rockies, had post-seedling densities >0.05 clumps-m⁻². Densities of clumps in the pre-reproductive size class were almost as low. The Dirty Devil Turnoff site along with the Salt Valley, Toquerville, and Little Rockies were the only sites with pre-reproductive densities of >0.05 clumps-m⁻², and seven sites had densities of <0.001 clumps-m⁻². Representation in the sub-adult size class was higher, with values >0.05 clumps-m⁻² at eleven sites and with values exceeding 0.02 clumps-m⁻² at all sites. Except at the Little Rockies, the average adult size class was the modal class, with densities ranging from 0.19 to 0.76 clumps-m⁻². The Colorado Plateau populations generally had low representation in the large and very large size classes because of their short stature, while many Mojave Desert sites showed high representation in the large size class, and a few of these, notably Lower Potosi, Veyo Road, Beaver Dam Summit, and Browse, included >0.07 clumps-m⁻² in the very large size class. These were all more upland sites, generally with high blackbrush cover (Table 1, Figure 4B).

Because size and age are loosely correlated for younger plants [19], the total absolute density of blackbrush clumps in the sub-adult and smaller size categories gives a rough estimate of recruitment frequency into openings between established clumps. The presence of clumps in smaller size classes represents the establishment of new clumps within existing blackbrush stands over time. It varied dramatically among sites, both in absolute value (0.03–2.51 clumps-m⁻²) and in terms of the percentage of total blackbrush clumps present (4–77%), indicating major differences in recruitment, and possibly in survival and growth, across sites (Figure 5). Most sites showed some evidence of past recruitment into openings in established stands, even the very dense and high-cover stand at Lower Potosi Pass (4% of clumps), although much of this recruitment was likely not recent, as clumps were in the subadult size class. Other sites with minimal evidence of recruitment into openings (4–7% of clumps) were Blue Diamond, Castle Cliff, and LeGrande, all of which are located just above the transition to creosote bush-dominated vegetation at the trailing edge of blackbrush distribution. All five Colorado Plateau populations had reasonably high percentages of sub-adult and smaller clumps (37–77%). Of the Mojave Desert sites, only Toquerville had a percentage of sub-adult and smaller clumps (39%) that fell in this range. The Little Rockies site had by far the highest total clump density (3.27 clumps-m⁻²) and the highest percentage of sub-adult and smaller clumps.

3.4. Blackbrush Drought Mortality

The idea that blackbrush clumps are generally long-lived especially in the adult size was supported by our field observations at the 16 study sites over a ten-year period from 1991 to 2001. During this period, we observed very few adult blackbrush clumps with complete or even noticeable partial mortality. However, when we measured size class distributions at eight of the sites in 2003, after the historically severe drought year of 2002, we observed considerable mortality at some sites (Figure 6). For five Mojave Desert sites, we found a strong and significant contrast in mortality levels between more xeric and more upland sites.

Two sites at the upper edge of blackbrush distribution (Browse and Beaver Dam Summit) exhibited no whole clump mortality and very little partial mortality. A similar pattern with slightly more mortality was observed at the upland Veyo Road site. At the more xeric Winchester Hills site and especially at the Castle Cliff site, a majority of clumps showed at least noticeable partial mortality, with complete or near-complete mortality in 27–41% of the clumps.

This analysis provides strong evidence that the mortality we observed at the Mojave Desert sites was drought related. Although we have no data to directly support this idea, we suggest that the observed patterns of within-clump mortality resulted from the death of some individuals in the clump rather than branch die-back throughout the entire clump.

We observed a slightly different pattern at three Colorado Plateau sites after the 2002 drought year (Figure 6). These sites did not show the high whole-clump mortality of the xeric Mojave Desert sites, but had higher percentages of clumps affected by the drought than the upland Mojave Desert sites. The Colorado Plateau sites were much more likely to show partial mortality, and only the Dirty Devil Turnoff site showed substantial whole-clump mortality. Lower drought-related mortality at the Colorado Plateau sites could be related to smaller stature and increased drought tolerance of adult plants (Figure 2). A related idea is that these sites are more xeric than the Mojave Desert sites on average, so that drought conditions did not represent as large a deviation from the norm (Table 1). Moreover, clumps on the Colorado Plateau contained more individuals on average than clumps in the Mojave Desert, making whole-clump mortality less probable [19]. Small clumps were also more likely to suffer complete mortality than clumps in the adult size classes, possibly for the same reason. Another explanation is that smaller plants are more vulnerable to drought stress.

4. Discussion

4.1. Inferring Stand History from Demographic Information

This study of blackbrush population structure at the stand level has demonstrated tremendous variation in blackbrush density, crown cover, and size class structure among contrasting sites across its range, but to truly understand the implications of this variation, it is helpful to look at these data in the context of studies that have quantified seed production, seedling emergence and establishment patterns, interactions with heteromyid rodents, and especially within- and among-clump age structure at many of these same sites [16,17,18,19,20]. This makes it possible to infer stand history from demographic information at contrasting sites, and thus to recognize how the larger patterns of blackbrush distribution on the landscape might be generated.

4.1.1. Veyo Road Study Site

The blackbrush population at the upland Veyo Road site in southwestern Utah is typical of many blackbrush stands throughout the range that could be considered ‘climax’ stands (Figure 1A, Figure 3 and Figure 4). This stand is characterized by low species diversity, a general absence of early seral species, strong dominance by blackbrush, and high density and crown cover. Many clumps are in the largest size classes, and rates of recruitment into openings appear to be regular but low. There is a pattern of regular recruitment into established clumps, with adult-sized clumps averaging 6.2 individuals per clump [19]. In addition, the estimated minimum age of the oldest measured clump in this stand was 121 years, indicating a long-term absence of disturbance. Even in the severe drought year, there was little or no whole-clump mortality, although some clumps apparently lost member plants (Figure 5).

The oldest measurable minimum age in such a climax stand is considered more a reflection of the average lifespan of individuals that reach maturity within a clump than of the date of clump establishment [19]. While we have no direct evidence to address this, it is possible that the process of senescence and death of older plants combined with their replacement by individuals of younger cohorts could have been ongoing for centuries. This is analogous to clonal growth in some other long-lived desert shrubs, but in this case, individual genets have finite lifespans, while clumps in the process of continuous individual self-replacement are potentially able to persist for a much longer period. Repeat photography has shown that the appearance of adult clumps at the Skidoo ghost town near Death Valley did not change appreciably over a 100-year period [7]. Given what we know about the likely maximum ages of individual plants in these clumps, it seems probable that the older clump members photographed originally have been gradually replaced over time.

4.1.2. LeGrande Study Site

The blackbrush population at the more xeric LeGrande site also probably represents a climax stand, as indicated by its relatively high blackbrush cover, density, adult crown diameter, and age of the oldest individual (95 years [19], Figure 1B, Figure 3 and Figure 4). The recruitment rate into established clumps at LeGrande was lower than that at Veyo Road (average 3.7 individuals per clump), and very few of these plants were recent recruits [19]. Even more telling was the complete lack of detectable recent recruitment into openings. We found no clumps in the two smallest size classes at LeGrande, in either the size class transect data set or when sampling for clump structure in the established stand. Moreover, we observed complete recruitment failure into the established stand at this site after the 1991 mast year, even though there was substantial emergence from rodent caches there in the following year [18]. There are several possible explanations for poor seedling survival and the apparent lack of self-replacement at this site. One explanation is that the site is ‘full’, that is, currently existing clumps have fully occupied the rooting space and this precludes the recruitment of new individuals. Evidence for this is that some successful recruitment onto an adjacent small-scale disturbance (power line right of way) was observed that year [18].

An alternative explanation is that the current climate at this site makes recruitment much less likely than in the past, even though adult plants can persist there. This would fit the ‘leading and trailing edge’ model of species distribution response to climate change, with the LeGrande site on the trailing edge, where long-term stand persistence is unlikely [3,16]. The same may be true of some of the other ‘trailing edge’ sites (Blue Diamond Turnoff, Castle Cliff).

A third explanation for regeneration failure at LeGrande is that seed and seedling predation by rodents is so extreme at this site that seedling establishment, especially into openings, is largely precluded even after mast years. This interpretation is supported by data from our establishment study at this site [18]. We found that 70% of the seedlings were clearly destroyed by predation in the first two months after emergence, and another 20% disappeared during this period, probably due to the same cause. In an earlier study there with artificial seed caches, there was seedling survival only in caches that were protected from rodent predation. Long-term recruitment failure at LeGrande is probably due to a combination of multiple factors. Regardless of the cause, however, the demographic structure at this site indicates probable future decline through eventual mortality of older plants that apparently cannot be not compensated by new recruitment. Unfortunately, we will not be able to examine this question further, as this privately owned site was developed for commercial and residential use three years after the study was initiated.

4.1.3. Toquerville Study Site

Just a few kilometers away from LeGrande, at the upland Toquerville site, we observed a contrasting demographic pattern (Figure 1C). Clumps at this site were well-distributed among the six size classes, suggesting regular recruitment through time (Figure 5). This conclusion is supported by data from the within-clump demographic study, in which recruitment events were detected in 21 of the years between 1970 and 2006 [19]. Adult plant density at this site is quite low (0.436 plants-m⁻²), but cover is relatively high (45%) because of high representation in the larger size classes (Figure 5). Most interestingly, these large clumps are not very old [19]. The oldest adult clump at Toquerville had a minimum age of 62 years, and the remaining 21 adult clumps sampled had minimum ages ranging from 20 to 45 years. This shows that blackbrush clumps can increase in size quite quickly under favorable conditions. These relatively young clumps had already accumulated an average of 6.6 individuals. These data taken collectively, along with the strong presence of early seral species like G. sarothrae (Figure 3), suggest that the blackbrush stand at this site may be in a process of active post-disturbance regeneration. Given the high frequency of fires in the adjacent vegetation, which is of the interior chaparral type, we surmise that the most likely explanation for the population structure at Toquerville is stand reestablishment after fires. Such stand reestablishment is reported to be rare [9]. However, at upland sites at the northern leading edge of blackbrush distribution in the Mojave Desert of Nevada, blackbrush stand reestablishment after fires has recently been documented [22]. This was aided by the patchy nature of these fires, which left intact blackbrush remnants that could provide a local source of seed, as was apparently also the case at the Toquerville site.

4.1.4. North Hanksville Study Site

The stand at the North Hanksville site represents another variation on this theme. As mentioned earlier, it combined high blackbrush dominance with low density and crown cover (Figure 3 and Figure 4). This site, which is on the northern-most edge of blackbrush distribution in central Utah, had an understory dominated by Indian ricegrass (Achnatherum hymenoides), sand dropseed (Sporobolus flexuousus), and galleta grass (Pleuraphis jamesii), with a high diversity of perennial forbs. As at Toquerville, the adult plants at North Hanksville are also relatively young, with minimum ages of 18 to 57 years. Recruitment into openings, as evidenced by the low frequency of small clumps, is not very frequent at this site (Figure 5), but regular recruitment into established adult clumps is evidenced by an average of 15.2 individuals per clump [19]. A possible interpretation of the stand structure at North Hanksville is that it represents a site where blackbrush is expanding, albeit fairly slowly, into another vegetation type, in this case grassland. We would expect to see such an expansion at the leading edge of blackbrush distribution, at the extreme northern edge of the current blackbrush range. The relatively low rate of recruitment into openings is probably explained by high rodent predation, as the sandy soil at this grassland site is ideal for kangaroo rats, and grass seeds would provide a source of food in non-mast years [20]. A kangaroo rat (Dipodomys ordii) burrow opening is evident at the lower right corner of Figure 1D.

4.1.5. Little Rockies Study Site

Lastly, the stand at the Little Rockies (Figure 7A,B) presents a demographic pattern that is completely different from any other site, with very high densities of clumps in the first three size classes, indicating essentially continuously high levels of clump recruitment into openings over a long time period (Figure 5). This suggests that some factor that limits recruitment at all the other sites is not operating at the Little Rockies. The character of the adult stand provides few clues to the identity of this factor, as adult plant density and cover values are higher than those at the Dirty Devil Turnoff, which does not have extraordinarily high clump recruitment (Figure 5). In our establishment study after the 1991 mast event at the Little Rockies study site, first year seedling survival was an astonishing 75% [18]. This high survival was due primarily to the near-absence of sprout predation in the weeks following emergence. Characterization of the rodent community at this site revealed a complete lack of kangaroo rats (Dipodomys spp.). The only heteromyid rodent present was the Great Basin pocket mouse (Perognathus parvus), which caches and consumes blackbrush seeds but apparently does not consume its sprouts. High densities of clumps in the post-seedling, pre-reproductive, and sub-adult size categories suggested that the high survival we saw after the 1992 recruitment event (27% after nine years) was not an anomaly but a regular occurrence at this site (Figure 7B).

The corollary of high recruitment success into an established stand of adult blackbrush plants is the slow growth rate of the juvenile size classes, which are strongly suppressed by the surrounding adults. After 9 years, most clumps that were recruited in 1992 at the Little Rockies were still in the post-seedling size class, and even after 21 years, most were still in the pre-reproductive size class (Figure 7C). This contrasts with North Hanksville, where plants <21 years of age were already in the adult size classes. This indicates that the growth rate in blackbrush can respond plastically to growing conditions, including the level of competition from adult conspecifics.

The presence of multiple cohorts of suppressed individuals in the understory of an established stand resembles the seedling bank phenomenon in masting forest trees [18]. This seedling bank phenomenon was most evident at the Little Rockies because of the high density of clumps in openings, but we also saw growth suppression of surviving juveniles in the open in established stands at Toquerville and Salt Valley as compared with juveniles on adjacent small-scale disturbances. One could also regard juvenile individuals that have been recruited into existing clumps as members of the seedling bank, with suppressed growth but sufficiently high survival until death of an older plant allows competitive release on a within-clump scale.

Adult clumps at the Little Rockies were up to 92 years old, indicating long-term stand stability, and there was ample evidence of recruitment into existing clumps, with 9.1 plants on average in adult clumps. This population appeared to be in a climax condition and capable of persisting indefinitely under the current climate regime.

4.2. The Role of Seed Dispersal

Similar to any other plant community, a blackbrush community will eventually be subjected to disturbance, and the remainder of the life history strategy for this species is related to the necessity for dispersal. Otherwise, it would not be selectively advantageous for blackbrush to produce seeds that are attractive to the rodent dispersers that are also major seed predators [20,23]. For perpetuation of an intact stand through within-clump recruitment, secondary rodent-assisted dispersal is probably not necessary, and any impact of the rodents therefore translates directly to predation. Seeds in non-mast years that fall directly into the crown of the maternal parent are likely never discovered and handled by rodents. That this pattern is the norm is supported by genetic data showing that plants of multiple ages within clumps, while not genetically identical, are usually closely related (B. Richardson, unpublished data).

Blackbrush seeds (one-seeded achenes) are quite heavy (15–21 mg; [24]), and do not disperse beyond any distance from the maternal plant without assistance. In order to colonize disturbances, or to migrate beyond the edge of current blackbrush distribution, they rely on heteromyid rodent dispersers [20]. Even though these dispersers consume a large majority of the seeds they move, some seeds are able to survive predation in the mast years and produce post-seedling juveniles that are no longer attractive as sprouts. The value of this trade-off for blackbrush is evident in its ability to escape post-caching seed predation in sufficient numbers to establish in new areas, especially small-scale disturbances near established stands. We regularly see recruitment onto road cuts, pipeline corridors, and abandoned roads in many locations across the Colorado Plateau (Figure 8A–C). We have also observed recruitment onto disturbances at the Mojave Desert sites [18]. Blackbrush individuals grow more quickly on disturbances, and can sometimes reach reproductive maturity in as few as ten years (Figure 8D).

4.3. Blackbrush Conservation Issues

Even though blackbrush is a dominant species over millions of hectares, it faces two serious potential threats to its survival over the long term. The first major threat is from invasive species and their association with increased wildfire. Historically, the blackbrush community type rarely experienced fire, but with the invasion of exotic annual grasses, primarily Bromus rubens, the frequency and size of wildfires in this community type has increased exponentially [25,26]. In high-precipitation years, these annual grasses form a continuous layer of highly flammable fine fuel in the interspaces. Blackbrush has no capacity to resprout after burning [19] and is killed outright by fire, resulting in stand loss sometimes over many thousands of hectares in a single burn [26]. The post-burn environment is not readily recolonized by blackbrush, and it is estimated that it could take centuries to return to the pre-burn condition through natural processes [27]. Burned areas can recover species richness and vegetative cover relatively quickly, but in most cases, there is little or no blackbrush recruitment post-burn [26]. Lack of a seed source, changes in soil attributes, and annual grass competition likely contribute to this low recruitment success. These areas may also have a high potential to re-burn due to increased annual grass dominance.

Experimental efforts to re-establish blackbrush after disturbances have met with mixed success even on a small scale, whether from direct seeding [18,28] or outplanting of container stock [3,29]. Its masting reproductive strategy creates the potential to make large seed collections in mast years for later use in restoration [17], and the seeds remain viable in storage for long periods [30]. The use of mycorrhizal inoculum has been shown to improve survival and growth as well as to confer increased competitive ability, at least in container culture, and could be useful in restoration [31].

The second major threat to the long-term survival of blackbrush is climate change. As an ecotonal species, it has experienced major range shifts in the past, migrating hundreds of kilometers from Pleistocene refugia in the Grand Canyon and the Lower Colorado Drainage to achieve its current distribution [2]. It is not known how this long-distance dispersal was achieved even over 10,000 years, let alone at a pace to keep up with the current rate of climate change. Bioclimate envelope modeling for the species suggests that, in at least one consensus future climate scenario, it will likely be extirpated within the next 40 years over much of its Mojave Desert range [3]. If the genetic diversity contained in these populations is to be preserved, long-term ex situ seed preservation followed by assisted migration and successful seeding into newly available habitat further north would likely be the best option over the distances involved.

5. Conclusions

Perhaps the biggest lesson from our studies of blackbrush population stand structure is that no two populations are the same. Each presents a unique combination of physical setting (climate and soil), biotic factors (including the community of granivorous rodents), and past stand history. Nonetheless, we can make some meaningful generalizations. First, individual blackbrush plants apparently have a finite potential lifespan, usually in the order of 100 years. In spite of this, at the clump level, it is possible for stand structure to persist essentially unchanged for much longer time intervals, through the process of self-replacement within clumps. This process of self-replacement seems to be pivotal in the ability of this shrub to completely dominate sites for such long periods of time. In the classic manner of climax forests of more mesic environments, young plants recruit into the suboptimal conditions under their elders and remain there in a suppressed condition, then seize the day when an adult dies and a gap finally occurs. Disturbance at the scale of individual plant death is usually thus hardly detectable. The prevalence of multi-individual and multi-cohort clumps across the wide range of population stand structures in this study is evidence that this modus operandi is standard for blackbrush, and permits long-term clump and stand persistence in the absence of major disturbances.

Dispersal, including rodent-assisted dispersal, has also been critical for the long-term success of blackbrush. A better-than-break-even point on the trade-off between dispersal and predation has probably been as essential to the perpetuation of blackbrush through geologic time as its ability to maintain itself in situ with little dispersal assistance. This is because, in the longer term, environmental changes shift the spatial pattern of habitats that blackbrush can successfully occupy, and in order to persist, it must be able to disperse into newly available habitats. Its unusual life history strategy has allowed this ancient species to persist for many thousands of years even in the face of long-term environmental change, but rapid anthropogenic change may present obstacles not previously encountered.