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2 Department of Biological Sciences, University of Nevada, 4505 Maryland Parkway, Box 454004, Las Vegas, Nevada 89154-4004 USA; 3 Center for Evolution, Ecology and Behavior, T. H. Morgan School of Biological Sciences, 101 Morgan Building, University of Kentucky, Lexington, Kentucky 40506-0225 USA; and 4 University Herbarium, Jepson Herbarium, and Department of Integrative Biology, 1001 Valley Life Sciences Building, #2465, University of California, Berkeley, California 94720-2465 USA
Received for publication December 7, 1998. Accepted for publication July 20, 1999.
ABSTRACT
The moss Syntrichia caninervis is the dominant soil bryophyte in a blackbrush (Coleogyne ramosissima) community in the southern Nevada Mojave Desert, with a mean cover of 6.3%. A survey of the 10-ha study site revealed an expressed ramet sex ratio of 14
: 1
(N = 890), with 85% of ramets not expressing sex over their life span, and an expressed population sex ratio of 40 : 2 : 1 (female : male : mixed-sex, N = 89), with 52% of populations not expressing sex. A greater incidence of sex expression was associated with shaded microsites, higher soil moisture content, and taller ramets. Shaded microsites had higher surface soil moisture levels than exposed microsites. In the exposed microhabitat, surface soil moisture was positively correlated with ramet height but not with sex expression. Male ramets and populations were restricted to shaded microhabitats, whereas female ramets and populations were found in both shaded and exposed microhabitats, suggesting gender specialization. The rarity of mature sporophytes, found in 0% of the ramets sampled and in only 3% of the populations, is probably due to the rarity of mixed-sex populations. We hypothesize that mixed-sex populations are rare because of factors relating to male rarity and that the differential cost of sex expression reduces the clonal growth capacity of male individuals.
Key Words: bryophyte • cryptogamic crust • desert • haploid dioecy • ramet • sex expression • sex ratio • sporophyte
Mosses are characterized by free-living haploid gametophytes. In dioecious species (note that "dioicy" is preferred by some researchers when referring to haploid dioecy, because dioicy and dioecy are not homologous and the genetic consequences are dissimilar; for discussion see Zander, 1984
; Wyatt, 1985
; Allen and Magill, 1987
), male and female individuals must be nearly juxtaposed to achieve fertilization, due to sperm dispersal distances on the order of a few centimetres (Anderson and Lemmon, 1974
; Wyatt, 1977
). Mosses retain the ancestral reproductive system of the first land plants, which requires fertilization via swimming sperm, a very limited system for a dryland plant. This constraint in the life cycle has profound effects on the biology of mosses and has resulted in an unusual reliance on various modes of asexual reproduction (Mishler, 1988
). Fertilization produces a diploid sporophyte that is dependent on the gametophyte, undergoes meiosis, and produces haploid spores. Despite the theoretical expectation of 1 : 1 ratio of male and female gametophytic individuals based upon chromosomal sex determination and segregation of sex chromosomes at meiosis (Ramsay and Berrie, 1982
), the pattern of female-biased adult sex ratios in bryophytes is clear (Longton, 1990
; Wyatt, 1994
; reviewed in discussion herein). Moreover, most studies report many stems that fail to express sex over their life spans (e.g., Shaw, Niguidula, and Wilson, 1992
). Thus, it is not surprising that the frequency of sexual reproduction in many dioecious mosses, as judged by sporophytic production, is low (Rohrer, 1982
; Stark and Castetter, 1987
; a notable exception to this pattern is exhibited by Pleurozium schreberi (Brid.) Mitt. in Canada: Longton, 1985
).
Possible reasons that sporophyte production is rare in many dioecious mosses include: (1) skewed sex ratios coupled with proliferation of unisexual populations through clonal growth (Longton and Greene, 1969
); (2) short sperm dispersal distances (Wyatt, 1977
); (3) differential mortality of the sexes (a largely untested hypothesis); (4) inhibition of gametangial formation in one sex, perhaps involving sex-differential induction factors (Longton and Greene, 1979
; Mishler and Oliver, 1991
); and (5) variation in fecundity levels between males and females (McLetchie, 1996
).
In the Mojave Desert, the general patterns of low sex expression, male rarity, and sporophytic rarity appear to be further skewed to the point where populations can be composed entirely of female and sterile ramets and devoid of sporophytes. In a low-elevation (750 m) site dominated by creosote bush [Larrea tridentata (Sessé & Moc.] Cov. and white bursage [Ambrosia dumosa (Gray) Payne], Syntrichia caninervis Mitt. populations (the dominant moss) were found to be devoid of males and sporophytes, with sex expression and degree of sex expression correlated positively to ramet height, and an overall ramet sex ratio of 1; : 0 : 2.3 nonexpressing (Stark, Mishler, and McLetchie, 1998
). In the present study, we focus on populations of the desert moss S. caninervis growing in a Coleogyne ramosissima Torr. (blackbrush) community at a considerably higher elevation, near the ecological limit for the species. We determine the frequency of sexual reproduction and correlate environmental factors that are associated with sex expression and sexual reproduction. Specifically, we pose the following questions: (1) What is the cover and species composition? (2) What level of sex expression occurs at the ramet (a potentially independent part of a genetic individual: an upright stem in acrocarpous mosses irrespective of underground connections) and population levels? (3) Is sex expression related to microhabitat and soil moisture? (4) How does the sex ratio vary at the ramet and population levels? and (5) What is the frequency of sexual reproduction as inferred from the presence of sporophytes?
MATERIALS AND METHODS
Study site
A 10-ha area was selected near White Rock Spring in the Spring Mountains of southern Nevada (Fig. 1): elevation 1494 m, T 20S, R 58E, Section 33 (Clark County, Red Rock National Conservation Area, south of White Rock Spring, Nevada, USA). Average annual precipitation (1990–1996) is 25.23 ± 9.80 cm/yr (mean ± 1 SD), range 16.13 (1994)-41.91 (1992: National Climatic Data Center, state report). The site was selected because of (1) its homogeneity with respect to vascular vegetation, with the general area dominated by Coleogyne ramosissima; (2) the federally protected status given the area, which minimized potential disturbance; and (3) its location close to the high-elevation limit for S. caninervis. The study site was bordered by major washes on three directions and by an unpaved parking lot separated by a buffer zone of 100 m to the north.
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; Fig. 2). The species is closely related to S. ruralis (Hedw.) Web. & Mohr, which replaces S. caninervis at higher elevations (Flowers, 1973
; Oliver, Mishler, and Quisenberry, 1993
). Unlike S. ruralis, S. caninervis has bistratose leaves and can be distinguished in the field by its darker color and more appressed stem leaves. No gemmae or specialized asexual propagules are known; thus, the capacity for asexual reproduction is best termed clonality through fragmentation of ramets. Voucher specimens of S. caninervis were deposited at UNLV (Stark NV-3001, NV-3002).
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Soil moisture
At each of 32 randomly selected Coleogyne ramosissima shrubs, paired surface soil samples were taken on 10 April 1998. As of this date, three rainless days had passed after measurable precipitation had been recorded on four consecutive days (3.8, 1.8, 4.6, and 0.5 mm, respectively). Soil samples were taken (1) beneath the shrub canopy on the north side of the shrub midway between the rootstock and the canopy edge, and (2) in an exposed soil site 1 m due north of the first sample point (or farther outward along the transect until a site was encountered that was not beneath a shrub canopy). The surface 2 cm of soil was cored using a 4.54 cm3 PVC (polyvinyl chloride) corer. If the soil to be sampled had cryptogamic cover, cryptogams were removed and the soil beneath the plants was collected. Gravimetric soil moisture was determined using a microbalance following oven drying at 110°C for 72 h.
Plant sampling paired with soil moisture sampling
Coincident with the soil sampling described above, populations of S. caninervis were sampled at the shaded and exposed microhabitats adjacent to areas from which soil was sampled. If present, a 22-mm diameter core of S. caninervis was taken (1) beneath the shrub canopy midway between the rootstock and the canopy (drip) line, adjacent to the soil moisture collection site due north of the rootstock; and (2) adjacent to the exposed soil collection site along the 1 m transect extending from the shrub into a shrubless (exposed) area. If plants of S. caninervis were not present at (1) above, the nearest plants were collected to the east of this point under the shrub; if no plants of S. caninervis were present under the shrub, no sample was collected. If plants of S. caninervis were not present at (2) above, the 1-m transect was extended until a population was encountered.
Laboratory determinations
Each core sample of S. caninervis was randomly subsampled for ten ramets, some of which had lost integrity as a core of intact plants + soil after transport. Ramets were selected without regard to potential organic connections below the ground surface. Each ramet was hydrated and severed at the ground surface, leaving the aboveground portion of the stem (the ramet) for study. The stem was then denuded of leaves by removing leaves singly from the base to the apex of the stem, in order to avoid damaging inflorescences. The following measurements were carried out for each plant using a dissecting microscope and millimetre ruler and/or a compound microscope with ocular micrometer: (1) aboveground ramet height (length), after hydration, exclusive of leaf awn, to the nearest 0.1 mm; (2) number and type of inflorescences (perigonia: clusters of antheridia; perichaetia: clusters of archegonia); and (3) the relative maturity of each inflorescence (immature: gametangia not dehisced; mature: gametangia dehisced). If the stem did not have inflorescences, it was scored as "nonexpressing." Because "sterile" implies incapable of sex expression and "juvenile" implies youthfulness, neither of which necessarily describes the state of stems in this species, we prefer "nonexpressing" (or "indeterminate") for those stems that have not yet expressed sex over the course of their life span.
Statistical analyses
For community-wide analyses, a contingency table was produced with sex, ramet height, and exposure as categorical variables. Ramets were classified as "tall" if their height was above the mean ramet height of all ramets, and ramets were classified as "short" if their height was below the mean height of all ramets. The resulting contingency table of sex state (expressing, nonexpressing), ramet height (short, tall), and exposure class (under shrub, intermediate, exposed) was statistically analyzed using categorical data analysis of SAS (CATMOD procedure; SAS, 1994
). Ramet height and exposure class were considered as explanatory variables for the sexual state of ramets (expressing or not expressing sex). This procedure was also used to determine whether ramet height and exposure class were associated with the sex (male, female) of the ramets expressing sex; that is, to test if male and female frequencies differ among the six combinations of size and exposure classes. The mean height of ramets with one inflorescence was compared with the mean height of ramets with more than one inflorescence using a T test. Ramet height was log transformed.
For the paired microhabitat samples, the original 32 paired microsite samples were reduced to 25 pairs due to an absence of S. caninervis plants at one of the paired microsites (microsite here refers to the actual site of sampling within a microhabitat, whereas microhabitat refers to the collective shaded or exposed localities). Differences in soil moisture content between shaded and exposed microhabitats were tested using a paired T test. Pearson product-moment correlations were obtained between moisture levels for the paired microhabitats, as well as between mean ramet height and moisture within each microhabitat type (shaded, exposed). Soil moisture, estimated as the percentage mass of water in the soil, was arcsine transformed. Ramet height was log transformed.
Within each microhabitat type, moisture level was categorized as "high" or "low" based on whether the moisture content at that microsite was above (high level) or below (low level) the mean moisture content for that microhabitat. Microsites were classified into two microsite ramet size classes: (1) "short-stemmed" if the mean height of ramets within a microsite was below the mean height across all ramets for that microhabitat, and (2) "tall-stemmed" if the mean height of ramets within a microsite was above the mean ramet height across all ramets for that microhabitat. The resulting contingency tables of sex expression, microsite ramet size class by site, and microsite moisture level were analyzed as described above, using categorical data analysis of SAS (CATMOD procedure; SAS, 1994
). Both microsite moisture level and microsite ramet size class were used as explanatory variables for sex expression within each microhabitat.
RESULTS
Species cover and frequency
The total living vegetation cover (61%) was composed of 15 species of seed plants (44% cover), six species of mosses (11% cover), and an undetermined number of lichens (3–4, 7% cover). Blackbrush (Coleogyne ramosissima) was clearly the dominant plant species, occupying 31% of the total ground cover and occurring in 89% of the quadrats (Table 1). All other seed plant species were present at <5% cover, although the grass Bromus rubens occurred in 81% of the quadrats. The cover for this annual grass is expected to increase through the winter and spring; percent cover of dead standing stems of B. rubens exceeded Coleogyne. Cryptogamic (mosses and lichens) cover was dominated by lichens (Collema was abundant) and two species of mosses, Syntrichia caninervis (6.3% cover, present in 53% of the quadrats) and Bryum algovicum Sendtn. (3% cover, present in 15% of the quadrats).
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: 1. Of the 89 populations of S. caninervis sampled, all contained some nonexpressing ramets, with approximately half of these populations (46) containing only nonexpressing ramets. Of the remaining 43 populations with ramets that expressed sex, 40 contained female ramets, two contained male ramets, and one population contained ramets of both sexes (mixed-sex; Table 2).
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1.9 mm were classified as "short." Both ramet height and microhabitat effects were significantly associated with sex expression of the sampled ramets (Table 3A). Tall plants were more likely to express sex than short plants. There were no statistical differences in sex expression (expressing, nonexpressing) between ramets collected under shrubs and ramets collected under the intermediate exposure category, but ramets collected under these two shaded conditions were more likely to express sex than plants collected in exposed microhabitats (Table 3B, F).
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Current sex expression and sex ratio
Since the ramets were harvested just prior to the interval of fertilization, during which time gametangia mature, the current level of sex expression was taken to be the fraction of ramets bearing terminal immature inflorescences. This yields the proportion of ramets that will express sex during the upcoming winter: 22% of expressing ramets (Table 2). Thus, about one-fifth of those ramets that had (or currently) expressed sex in their aboveground lifetimes will likely produce mature gametangia (express sex) in the upcoming interval of fertilization. This percentage (0.22) was equivalent for both sexes. The current sex ratio (14 : 1) reflected the community-wide sex ratio (14 : 1).
Ramet height and number of inflorescences
Of those ramets expressing sex (N = 137), only 15% (21 of 137) produced more than a single inflorescence over the course of their aboveground life span, and all of these ramets were female (Table 2). For these females, ramets with two or more inflorescences were significantly taller than ramets with one inflorescence: 2.9 (±0.16) mm vs. 2.4 mm (±0.06), respectively (mean ±1 SE, T = -2.9579, df = 124.0, P < 0.005).
Microhabitat differences in soil moisture, ramet height, and sex expression
Three days after a series of rains at the study site, surface soil moisture (upper 2 cm) as percentage water by mass was significantly higher under Coleogyne than in exposed adjacent regions at least 1 m away from Coleogyne canopy (Table 4): 9.03 (±0.77) vs. 6.11 (±0.58), respectively, paired T test (N = 25, T = 6.806, P < 0.0001). Moisture content between paired shaded and exposed microhabitats was significantly correlated r = 0.833, P < 0.0001, N = 25). There was also a significant correlation between soil moisture and mean height of ramets from the exposed sites (r = 0.51, P < 0.05, N = 25). A similar association between soil moisture and height was not found in shaded sites r = -0.0272, P > 0.05, N = 25).
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: 0) and shaded microhabitats (24 : 1). Shaded and exposed sites were analyzed separately. Mean ramet height for shaded habitats was 2.54 mm, and microsites with a mean ramet height >2.54 mm were classified as "tall-stemmed," whereas microsites with a mean ramet height <2.54 mm were classified as "short-stemmed." For the shaded microhabitat, soil moisture was associated with sex expression when ramet height was controlled. Similarly, sex expression was associated with ramet height when soil moisture was controlled. Specifically, within tall-stemmed microsites, sites with high soil moisture content were 1.8 times more likely to contain ramets expressing sex than microsites with low soil moisture content (0.350 ± 0.06 vs. 0.197 ± 0.05, respectively). For short-stemmed microsites, sites with high soil moisture content were two times more likely to contain ramets expressing sex than sites with low moisture content (0.205 ± 0.04 vs. 0.107 ± 0.04, respectively; Table 3D). For exposed microhabitats, mean ramet height was 1.78 mm, and microsites with a mean ramet height >1.78 mm were classified as "tall-stemmed," whereas microsites with a mean ramet height <1.78 mm were classified as "short-stemmed." Tall-stemmed microsites were three times more likely to have ramets that expressed sex compared to short-stemmed microsites (0.149 ± 0.034 vs. 0.0476 ± 0.018, tall-stemmed vs. short-stemmed microsites across both moisture levels). However, moisture was not significantly associated with frequency of sex expression in exposed sites (Table 3E). Analyses to detect differences between the frequency of males and females were not done because only two males were recovered in the shaded sites and zero males in the exposed sites.
Sex ratios and sporophyte production
Male ramets and sporophytes were entirely absent from exposed microhabitats, occurring in very small numbers only in the shaded microhabitats. Female ramets, however, occurred in both shaded and exposed microhabitats. Only five abortive sporophytes were recovered in this study, with no mature sporophytes, from previous or current cycles. Abortive sporophytes were arrested in the late embryonic stage. Mature sporophytes were observed, however, in two of 89 populations; these mature sporophytes did not fall within the core samples. Thus, of the 128 female ramets sampled, none had recently produced a mature sporophyte.
DISCUSSION
Desert cryptobiotic crust communities in western North America are composed of lichens, mosses, free-living cyanobacteria, and algae (Belnap, 1993
). Studies of these crusts demonstrate their roles in reducing erosion, enhancing permeability and water retention, nitrogen-fixation, nutrient cycling and availability of nutrients to seed plants, and promoting establishment of seedlings (Meyer, 1986
; Lesica and Shelly, 1992
; Evans and Ehleringer, 1993
; Belnap and Harper, 1995
; Smith, Monson, and Anderson, 1997
). Soil binding is attributed to trichome sheaths of the algal species, to moss rhizoids, and to fungal mycelia (Anderson, Harper, and Holmgren, 1982
; Brotherson, Rushforth, and Johansen, 1983
). Enhancement of water permeability is attributed to the algal component of the crust because of the uneven, irregular surface and increased porosity (Brotherson, Rushforth, and Johansen, 1983
; but see Eldridge, 1993
, for opposing view). Water retention in the soil beneath the crust is attributed to all of the biotic components and can amount to an 18-fold difference in loss of soil moisture to air (Isichei, 1990
). The cyanobacteria and lichens with cyanobacterial symbionts fix nitrogen. Additionally, phosphorous and carbon are more available in soils with crustal cover (Dunne, 1989
). Because of the increased water retention and the irregular surface of the crust, some vascular plant seedlings may experience increased viability (St. Clair et al., 1984
). Despite this body of research documenting the ecological role of cryptobiotic crusts in arid lands, relatively little attention has been paid to aspects of reproduction in the component species.
Cryptogamic cover was found to constitute a significant component of the total vegetative cover in a community dominated by the flowering plant Coleogyne ramosissima. In southern Nevada, Coleogyne shrublands represent a widespread community that establishes on well-drained colluvial slopes between 1300 and 2100 m (Lei and Walker, 1997a
). The 18% total cryptogam cover reported here would have been higher had we estimated the cover as a percentage of the available ground surface, because the quadrats frequently intersected rootstocks of Coleogyne. Despite the rare occurrence of sexual reproduction, Syntrichia caninervis is the dominant cryptogam in the blackbrush community.
The poikilohydric nature of mosses translates into growth only when colonies are hydrated (Alpert, 1979
; Rundel and Lange, 1980
). In a region of low and unpredictable rainfall like the Mojave Desert, temporal aspects of water availability are critical for growth and sexual reproduction. The microhabitats in the community that desiccate less rapidly are found on the north-facing sides of the largest elements in the landscape (i.e., plants, boulders, or slopes). Moss populations with a south-facing aspect desiccated more rapidly than moss populations with a north-facing aspect in San Diego County (California): from 92 to 93% saturation of populations to 45% (north) and 25% (south) in a single morning of exposure in March (Alpert and Oechel, 1985
). In the community studied, the most prominent element of the landscape was the evergreen shrub Coleogyne ramosissima. These shrubs cast sizable shadows, and mosses grow on the soil at their bases (Fig. 2). Should the period of colony hydration be extended on soil under shrubs due to reduced surface evaporation compared to open sites, then the surface soil should contain more water in the days following a rainstorm. This shaded soil should remain in a hydrated state longer than adjacent exposed sites. We found this to be true for soils on the north-facing sides of blackbrush shrubs. The roots of Coleogyne were not found to be superficially located in the present study and are unlikely to exploit superficial soil moisture, consistent with earlier findings that the majority of Coleogyne roots are found at depths of 10–30 cm (Bowns, 1973
). Higher soil moisture levels under Coleogyne are consistent with the significantly cooler soil temperatures under shrubs than in open microhabitats in Coleogyne populations, with open soils exhibiting greater fluctuations in temperature (Lei and Walker, 1997b
). However, the annual invasive Bromus rubens, which reaches full cover in the spring and occupies similar microsites as S. caninervis, may compete for surface water and therefore represent a threat to the long-term survival of crustal species (Belnap, 1993
). The "islands of fertility" associated with Larrea shrubs, where N, P, Cl, S, and K were more concentrated under shrubs than in open microhabitats (Schlesinger et al., 1996
), probably apply to Coleogyne communities as well.
The higher soil moisture content of shaded soils is correlated with increased rates of sex expression, greater ramet height, and occurrence of sexual reproduction as inferred from the presence of sporophytes. Despite a similarity in patterns, paired microhabitats exhibited greater divergence in plant height, sex expression, current sex expression, and sex ratio than the community-wide analyses (Table 4). This divergence is likely because paired microhabitat populations were consistently sampled from (or very near to) due north of the shrub rootstock, whereas the "shaded" category (under shrub) in the community-wide analysis included partially shaded microhabitats, and microhabitats from all directional points relative to blackbrush rootstocks. Thus, the shaded category of the community-wide analysis was likely to be drier, on average, compared to the paired shaded microhabitat. Male plants and sporophytes of S. caninervis, which were absent at a lower elevation site in the Mojave Desert (Stark, Mishler, and McLetchie, 1998
), were recovered in the present study. Nevertheless, males and sporophytes were exceedingly rare, and sporophytes appear to be limited in part by the occurrence of mixed-sex populations. Only five fertilized female ramets were encountered from a total of 1453 sampled ramets (0.3%), and all five sporophytic females bore only abortive sporophytes. The 3% of S. caninervis populations recently productive of sporophytes in the present study is similar to the 1% reported across all dioecious bryophyte species in the Chihuahuan Desert (Stark and Castetter, 1987
). These desert sporophyte frequencies are much lower than the 15–27% reported for more mesic Michigan (USA) sites (Rohrer, 1982
) and far lower than sites in Canada of Pleurozium schreberi surveyed without prior knowledge of sporophyte presence (Longton, 1985
). We hypothesize that male rarity limits the frequency of mixed-sex populations, which, in turn, limits the production of sporophytes.
Finding a positive correlation between soil moisture and ramet height in exposed, but not shaded, paired microhabitats may be a result of the constraints of a one-time moisture measurement. At the time soil moisture was assessed (three rainless days after a total of 10.7 mm of precipitation over the four preceding days), the moisture level in shaded microhabitats may not reflect the moisture level that causes variation in stem height (assuming a cause/effect relationship). Alternatively, (1) the greater sex expression observed in shaded microsites may obscure any real correlation between stem height and soil moisture content, and/or (2) current soil moisture levels may be less important than the total duration of population hydration (since plants may be desiccated despite moist underlying soils).
Sex ratios among bryophytes have been quantitatively documented in 24 species, using either herbarium material, field study of single or a few populations, or culture studies. A female-biased sex ratio was present in 17 species (Bedford, 1938, 1940
; Lewis and Benson-Evans, 1960
; Pettet, 1967
; Longton and Greene, 1969
; Newton, 1971
; Riemann, 1972
; Collins and Oechel, 1977
; Stoneburner, 1979
; Glime, 1984
; Reese, 1984
; Longton, 1985
; Stark, 1987
; Mishler and Oliver, 1991
; Shaw, Jules, and Beer, 1991
; McLetchie, 1992
; Moyá, 1992
; Shaw and Gaughan, 1993
; Miller and Mogensen, 1997
; Stark, Mishler, and McLetchie, 1998
), a male-biased sex ratio in three (McQueen, 1985
; Cameron and Wyatt, 1990
; Shaw, Niguidula, and Wilson, 1992
), and tendencies were unclear in four species (Newton, 1972
; Wyatt, 1977
; Cameron and Wyatt, 1990
; Shaw, 1993
). We exclude from the above listing species known to have dwarf males; however, of those six dwarf male species discussed by Ramsay and Berrie (1982), a female-biased sex ratio is reported in five (since the number of dwarf males was counted per female branch, rather than on an individual per individual basis, the sex ratio is in terms of female branches per male individual). It is presently unknown why male rarity is the common pattern among bryophytes, given that sex determination is likely to be chromosomal, resulting in an expectation at meiosis of 1 : 1 (Allen, 1919
; Vaarama, 1954
; Ono, 1970
; Tatuno and Kise, 1970
; Ramsay and Berrie, 1982
), and indirect evidence also suggests that sex determination is chromosomal in most species (Anderson, 1980
; Shaw, Jules, and Beer, 1991
; McLetchie, 1992
). Thus, male rarity may result from differential survival of spores and/or individuals, differential sex expression [as shown in Plagiomnium undulatum (Hedw.) Schimp.; Newton, 1972
], or differential clonal growth, all of which favor females.
The low number of ramets expressing sex may suggest a significant cost to perichaetial and (especially) perigonial production. Similarly, plants that had expressed sex in their life span rarely expressed sex on more than one occasion (the mean number of inflorescences per ramet was close to 1.0). This finding is consistent with the correlation of ramet height and sex expression that was observed here and reported for a lower elevation site (Stark, Mishler, and McLetchie, 1998
). In clonal organisms with indeterminate growth, body size is an important determinant of sexual reproduction, with most species attaining a threshold size prior to the onset of sexual reproduction (sex expression). After attaining this minimum body size, reproductive output increases as a function of body size (Ebenman and Persson, 1988
; but see conflicting model in Wiener, 1988
). Syntrichia caninervis plants are both perennial and clonal, and thus likely to exhibit life-history trade-offs among sexual reproduction, vegetative (including clonal) growth, and maintenance (Silvertown and Lovett Doust, 1993
). Future explorations of the proximate and ultimate causes of male rarity in S. caninervis should include the differential cost of sex prior to fertilization: should the cost of producing male gametes be greater than the cost of producing female gametes, then the female plant could be at an advantage with respect to growth and maintenance (i.e., exhibit compensation). Evidence for sex-specific life-history patterns presented herein includes: (1) female ramets were far more common; (2) female ramets produced more inflorescences per ramet than male ramets; and (3) all five of the sporophytes encountered were abortive, suggesting a high relative cost of sporophyte production.
In some dioecious seed plants, sexes are separated spatially along gradients of moisture, nutrients, light, temperature, and salinity (Freeman, Klikoff, and Harper, 1976
; Cox, 1981
; Bierzychudek and Eckhart, 1988
; Lovett Doust and Lovett Doust, 1988
; Ramadan et al., 1994
), with females often more common under the less stressful conditions. Spatial segregation of the sexes was reported in the dioecious moss Splachnum sphaericum Hedw. within a single sporophytic population (i.e., on a much finer scale than reported here) by Cameron and Wyatt (1990). The aforementioned study indicated labile sex expression, and an abiotic factor has not yet been linked to the clumped distribution of male and female plants. Moreover, females of Splachnum were found to occupy more favorable sites, whereas we found expressing male ramets of S. caninervis to be restricted to shaded microhabitats and expressing female ramets to occur in both shaded and exposed microhabitats. This suggests a pattern of gender specialization that is opposite to the pattern found in seed plants (and to that reported by Cameron and Wyatt, 1990
). Whether the explanations for the absence of expressing males from exposed microhabitats represents a lack of males (a compensatory success of females), or in the inability of males to express sex under exposed conditions, remain as untested hypotheses. We caution, however, that the pattern of males being restricted to shaded microhabitats is weakened by the low levels of male sex expression observed. It is desirable to pinpoint the distribution of males, for males possibly occupy the moister microsites within the shaded microhabitat.
The overall rate of sex expression of 0.15 in S. caninervis falls within the reported range of other dioecious species in which nonexpressing individuals or stems were scored from mostly nonsporophytic populations or from community-wide sampling (0.08–0.32; Longton, 1985
; Shaw, Niguidula, and Wilson, 1992
; Shaw, 1993
; Shaw and Gaughan, 1993
; Stark, Mishler, and McLetchie, 1998
). Such data are usually interpreted as evidence that a failure to express sex plays a role in the absence of sexual reproduction, especially because higher rates of sex expression are reported in sporophytic populations (e.g., Collins and Oechel, 1977
). During the present study, our unpublished observations indicate that sex expression is significantly higher in sporophytic populations and will be investigated further.
Our finding of a virtual absence of mature sporophytes means that the great majority of populations showed no evidence of successful sexual reproduction over several years. In dioecious desert mosses, it is possible that sexual reproduction is vestigial, at best representing a minor contribution to reproductive fitness (Mishler, 1988
). Our data (here and Stark, Mishler, and McLetchie, 1998
) suggest that clonal growth is the primary component of fitness for desert populations of S. caninervis. The low level or lack of sexual reproduction in this species suggests that clonal growth is important for population maintenance, expansion, and even colonization of new sites. Since S. caninervis does not produce asexual propagules, regeneration of leaf and stem fragments may play major roles in clonality. Studies of possible adaptive trade-offs involving sexual reproduction would be improved by comparisons between desert species and their closest relatives from more mesic habitats.
To test the hypothesis that the period of colony hydration determines the rate of sex expression in S. caninervis, reciprocal transplants between exposed and shaded populations should be carried out. Direct observation of the period of colony hydration following summer and winter rain events would also be desirable, and a watering experiment comparing sex expression in populations that are watered vs. nonwatered would be helpful. Such experimental research is currently underway. In addition, an analysis of populations along an elevational gradient controlling for slope and aspect predicts that sex expression should increase with increasing elevation. Finally, the sex ratios of the sexual propagules (spores) need to be confirmed.
FOOTNOTES
1 The authors thank the National Geographic Society (grant number 5429-95) for providing partial travel costs; the Bureau of Land Management, Las Vegas (Gayle Marrs-Smith), for granting a collecting permit; the Red Rock National Recreation Area for permission to set up the study site; Dale Devitt for use of his laboratory microbalance; Daniel Norris for identification of Bryum algovicum; UNLV librarian Amy Quinn; Farnoush Athari, Don Bowker, Scott Graham, Karl Jessen, Kate Kupish, Jennifer Sholdra, Sergio Salgado, Robin Stark, and Steve Timinskas for field and laboratory assistance; and Royce Longton and Robert Wyatt for reviewing the manuscript. This paper is derived from the senior author's undergraduate research thesis in Environmental Studies, UNLV. 
5 Author for correspondence (702-895-3119, FAX 702-895-3956, e-mail: LRS{at}nevada.edu
).
6 Current address: National Park Service, Canyonlands National Park, 2282 South West Resource Boulevard, Moab, Utah 84532 USA.
LITERATURE CITED
Allen, B. H., and R. E. Magill. 1987 In support of a distinct terminology for bryophyte sexuality. Taxon 36: 57–58. [CrossRef][ISI]
Allen, C. E. 1919 The basis of sex inheritance in Sphaerocarpos. Proceedings of the American Philosophical Society 58: 289–316.
Alpert, P. 1979 Desiccation of desert mosses following a summer rainstorm. Bryologist 82: 65–71. [CrossRef][ISI]
———, and W. C. Oechel. 1985 Carbon balance limits the microdistribution of Grimmia laevigata, a desiccation-tolerant plant. Ecology 66: 660–669. [CrossRef][ISI]
Anderson, D. C., K. T. Harper, and R. C. Holmgren. 1982 Factors influencing development of cryptogamic soil crusts in Utah deserts. Journal of Range Management 35: 180–185. [CrossRef][ISI]
Anderson, L. E. 1980 Cytology and reproductive biology of mosses. In R. J. Taylor and A. E. Leviton [eds.], The mosses of North America, 37–76. Pacific Division, American Association for the Advancement of Science, San Francisco, California, USA.
———, and B. E. Lemmon. 1974 Gene flow distances in the moss, Weissia controversa Hedw. Journal of the Hattori Botanical Laboratory 38: 67–90.
Bedford, T. H. B. 1938 Sex distribution in colonies of Climacium dendroides W. and M., and its relation to fruit bearing. North Western Naturalist 13: 213–221.
———. 1940 The fruiting of Breutelia arcuata Schp. Naturalist 1940: 113–115.
Belnap, J. 1993 Recovery rates of cryptobiotic crusts: inoculant use and assessment methods. Great Basin Naturalist 53: 89–95.
———, and K. T. Harper. 1995 Influence of cryptobiotic soil crusts on elemental content of tissue of two desert seed plants. Arid Soil Research and Rehabilitation 9: 107–115.
Bierzychudek, P., and V. Eckhart. 1988 Spatial segregation of the sexes of dioecious plants. American Naturalist 132: 34–43. [CrossRef][ISI]
Bowns, J. 1973 An autecological study of blackbrush (Coleogyne ramosissima Torr.) in southern Utah. Ph.D. dissertation, Utah State University, Logan, Utah, USA.
Brotherson, J. D., S. R. Rushforth, and J. R. Johansen. 1983 Effects of long-term grazing on cryptogam crust cover in Navajo National Monument, Arizona. Journal of Range Management 36: 579–581. [CrossRef][ISI]
Cameron, R. G., and R. Wyatt. 1990 Spatial patterns and sex ratios in dioecious and monoecious mosses of the genus Splachnum. Bryologist 93: 161–166.
Collins, N. J., and W. C. Oechel. 1977 The pattern of growth and translocation of photosynthate in a tundra moss, Polytrichum alpinum. Canadian Journal of Botany 52: 355–363.
Cox, P. A. 1981 Niche partitioning between sexes of dioecious plants. American Naturalist 117: 295–307. [CrossRef][ISI]
Daubenmire, R. F. 1970 Steppe vegetation of Washington. Washington Agricultural Experiment Station Technical Bulletin 62.
Dunne, J. 1989 Cryptogamic crusts in arid ecosystems. Rangelands 11: 180–182.
Ebenman, B., and L. Persson [eds]. 1988 Size-structured populations. Springer-Verlag, Berlin.
Eldridge, D. J. 1993 Cryptogams, vascular plants, and soil hydrological relations: some preliminary results from the semiarid woodlands of eastern Australia. Great Basin Naturalist 53: 48–58.
Evans, R. D., and J. R. Ehleringer. 1993 A break in the nitrogen cycle in aridlands? Evidence from 
15N of soils. Oecologia 94: 314–317.
[CrossRef][ISI]
Flowers, S. 1973 Mosses: Utah and the West. Brigham Young University Press, Provo, Utah.
Freeman, D. C., L. C. Klikoff, and K. T. Harper. 1976 Differential resource utilization by the sexes of dioecious plants. Science 193: 597–599.
Glime, J. M. 1984 Physio-ecological factors relating to reproduction and phenology in Fontinalis dalecarlica. Bryologist 87: 17–23.
Isichei, A. O. 1990 The role of algae and cyanobacteria in arid lands: a review. Arid Soil Research and Rehabilitation 4: 1–17.
Lei, S. A., and L. R. Walker. 1997a Biotic and abiotic factors influencing the distribution of Coleogyne communities in southern Nevada. Great Basin Naturalist 57: 163–171.
———, and ———. 1997b Classification and ordination of Coleogyne communities in southern Nevada. Great Basin Naturalist 57: 155–162.
Lesica, P., and J. S. Shelly. 1992 Effects of cryptogamic soil crust on the population dynamics of Arabis fecunda (Brassicaceae). American Midland Naturalist 128: 53–60.
Lewis, K. R., and K. Benson-Evans. 1960 The chromosomes of Cryptothallus mirabilis (Hepaticae: Riccardiaceae). Phyton 14: 21–35.
Longton, R. E. 1985 Reproductive biology and susceptibility to air pollution in Pleurozium schreberi (Brid.) Mitt. (Musci) with particular reference to Manitoba, Canada. Monographs in Systematic Botany of the Missouri Botanical Garden 11: 51–69.
———. 1990 Sexual reproduction in bryophytes in relation to physical factors of the environment. In R. N. Chopra and S. C. Bhatla [eds.], Bryophyte development: physiology and biochemistry, 139–166. CRC Press, Boca Raton, Florida, USA.
———, and S. W. Greene. 1969 The growth and reproductive cycle of Pleurozium schreberi (Brid.) Mitt. Annals of Botany 33: 83–105.
———, and ———. 1979 Experimental studies of growth and reproduction in the moss Pleurozium schreberi (Brid.) Mitt. Journal of Bryology 10: 321–338. [ISI]
Lovett Doust, J., and L. Lovett Doust. 1988 Modules of production and reproduction in a dioecious clonal shrub, Rhus typhina. Ecology 69: 741–750.
McLetchie, D. N. 1992 Sex ratio from germination through maturity and its reproductive consequences in the liverwort Sphaerocarpos texanus. Oecologia 92: 273–278.
———. 1996 Sperm limitation and genetic effects on fecundity in the dioecious liverwort Sphaerocarpos texanus. Sexual Plant Reproduction 9: 87–92.
McQueen, C. B. 1985 Spatial pattern and gene flow distances in Sphagnum subtile. Bryologist 88: 333–336.
Meyer, S. E. 1986 The ecology of gypsophile endemism in the eastern Mojave Desert. Ecology 67: 1303–1313. [CrossRef][ISI]
Miller, N. G., and G. S. Mogensen. 1997 Cyrtomnium hymenophylloides (Bryophyta, Mniaceae) in North America and Greenland: male plants, sex-differential geographical distribution, and reproductive characteristics. Bryologist 100: 499–506. [ISI]
Mishler, B. D. 1988 Reproductive ecology of bryophytes. In J. Lovett Doust and L. Lovett Doust [eds.], Plant reproductive ecology: patterns and strategies, 285–306. Oxford University Press, New York, New York, USA.
———, and M. J. Oliver. 1991 Gametophytic phenology of Tortula ruralis, a desiccation-tolerant moss, in the Organ Mountains of southern New Mexico. Bryologist 94: 143–153. [CrossRef][ISI]
Moyá, M. T. 1992 Phenological observations and sex ratios in Marchantia chenopoda L. (Hepaticae: Marchantiaceae). Tropical Bryology 6: 161–168.
Newton, M. E. 1971 A cytological distinction between male and female Mnium undulatum Hedw. Transactions of the British Bryological Society 6: 230–243. [ISI]
———. 1972 Sex ratio differences in Mnium hornum Hedw. and M. undulatum Sw. in relation to spore germination and vegetative regeneration. Annals of Botany 36: 163–178.
Oliver, M. J., B. D. Mishler, and J. E. Quisenberry. 1993 Comparative measures of desiccation-tolerance in the Tortula ruralis complex. I. Variation in damage control and repair. American Journal of Botany 80: 127–136. [CrossRef][ISI]
Ono, K. 1970 Karyological studies on Mniaceae and Polytrichaceae, with special reference to the structural sex-chromosomes III. Journal of Science of Hiroshima University: Series B, Division 2 (botany) 13: 167–221.
Pettet, A. 1967 Sex ratios of Riccia frostii in Khartoum Province, Sudan. Transactions of the British Bryological Society 5: 332–337.
Ramadan, A. A., A. El-Keblawy, K. W. Shaltout, and J. Lovett-Doust. 1994 Sexual polymorphism, growth and reproductive effort in Egyptian Thymelaea hirsuta (Thymelaeaceae). American Journal of Botany 81: 847–857. [CrossRef][ISI]
Ramsay, H. P., and G. K. Berrie. 1982 Sex determination in bryophytes. Journal of the Hattori Botanical Laboratory 52: 255–274.
Reese, W. D. 1984 Reproductivity, fertility, and range of Syrrhopodon texanus Sull. (Musci: Calymperaceae), a North American endemic. Bryologist 87: 217–222. [CrossRef][ISI]
Riemann, B. 1972 On the sex distribution and the occurrence of sporophytes in Rhytidiadelphus triquetrus (Hedw.) Warnst. in Scandinavia. Lindbergia 1: 219–224.
Rohrer, J. 1982 Sporophyte production and sexuality of mosses in two northern Michigan habitats. Bryologist 85: 394–400. [CrossRef][ISI]
Rundel, P. W., and O. L. Lange. 1980 Water relations and photosynthetic response of a desert moss. Flora 169: 329–335. [ISI]
SAS. 1994 SAS/STAT user's guide, version 6, 4th ed., vol. I. SAS Institute, Cary, North Carolina, USA.
Schlesinger, W. H., J. A. Raikes, A. E. Hartley, and A. F. Cross. 1996 On the spatial pattern of soil nutrients in desert ecosystems. Ecology 77: 364–374. [CrossRef][ISI]
Shaw, A. J. 1993 Population biology of the rare copper moss, Scopelophila cataractae. American Journal of Botany 80: 1034–1041.
———, and J. F. Gaughan. 1993 Control of sex ratios in haploid populations of the moss, Ceratodon purpureus. American Journal of Botany 80: 584–591.
———, E. S. Jules, and S. C. Beer. 1991 Effects of metals on growth, morphology, and reproduction of Ceratodon purpureus. Bryologist 94: 270–277.
———, N. J. Niguidula, and T. M. Wilson. 1992 Reproductive biology of the rare "copper moss" Mielichhoferia mielichhoferiana. Contributions from the University of Michigan Herbarium 18: 131–140.
Silvertown, J. W., and J. Lovett-Doust. 1993 Introduction to plant population biology. Blackwell Scientific Publications, London, UK.
Smith, S. D., R. K. Monson, and J. E. Anderson. 1997 Physiological ecology of North American desert plants. Springer-Verlag, Berlin, Germany.
Stark, L. R. 1987 A taxonomic monograph of Forsstroemia Lindb. (Bryopsida: Leptodontaceae). Journal of the Hattori Botanical Laboratory 63: 133–218.
———, and R. C. Castetter. 1987 A gradient analysis of bryophyte populations in a desert mountain range. Memoirs of the New York Botanical Garden 45: 186–197.
———, B. D. Mishler, and D. N. McLetchie. 1998 Sex expression and growth rates in natural populations of the desert soil crustal moss Syntrichia caninervis. Journal of Arid Environments 40: 401–416.
St. Clair, L. L., B. L. Webb, J. R. Johansen, and G. T. Nebeker. 1984 Cryptogamic soil crusts: enhancement of seedling establishment in disturbed and undisturbed areas. Reclamation and Revegetation Research 3: 129–136.
Stoneburner, A. 1979 Fruiting in relation to sex ratios in colonies of Pleurozium schreberi in northern Michigan. Michigan Botanist 18: 73–81.
Tatuno, S., and Y. Kise. 1970 Cytological studies on Atrichum, with special reference to structural sex chromosomes and sexuality. Botanical Magazine, Tokyo 83: 163–172. [ISI]
Vaarama, A. 1954 Cytological observations on Pleurozium schreberi, with special reference to centromere evolution. Annales Botanici Societatis Zoologicae-Botanicae Fennicae "Vanamo" 28: 1–59.
Wiener, J. 1988 The influence of competition on plant reproduction. In J. Lovett-Doust and L. Lovett-Doust [eds.], Plant reproductive ecology: patterns and strategies, 228–245. Oxford University Press, New York, New York, USA.
Wyatt, R. 1977 Spatial pattern and gamete dispersal distances in Atrichum angustatum, a dioicous moss. Bryologist 80: 284–291. [CrossRef][ISI]
———. 1985 Terminology for bryophyte sexuality: toward a unified system. Taxon 34: 420–425. [CrossRef][ISI]
———. 1994 Population genetics of bryophytes in relation to their reproductive biology. Journal of the Hattori Botanical Laboratory 76: 147–157.
Zander, R. H. 1984 Bryophyte sexual systems: -oicous versus -oecious. Bryologische Beiträge 3: 46–51.
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