Cryptic Diversity in Bryophyte Soil-Banks Along a Desert Elevational Gradient

Home , Ditrichaceae, Pottiaceae, Pterygoneurum ovatum

Lindbergia 36: 1–8, 2013 ISSN 0105-0761 Accepted 26 February 2013

Cryptic diversity in bryophyte soil-banks along a desert elevational gradient

Robert J. Smith

Robert J. Smith ([email protected]), School of Life Sciences, Univ. of Nevada Las Vegas, 4505 Maryland Parkway, Las Vegas, NV 89154-4004, USA.

Propagule soil-banks are important for colonization and for the maintenance of regional diversity among bryophytes of temperate regions, yet they have not previously been reported from hot desert ecosystems, and little is known about the relationship between soil-bank diversity and elevation. I used emergence germination methods to explore patterns of species composition and richness in bryophyte soil-banks along a 1400 m elevational gradient spanning three major vegetation zones in the Mojave Desert (southwestern USA). A total of 17 bryophyte taxa were present in soils collected at twelve sites. Community compositions shifted with increasing elevation, suggesting that soil-banks along the gradient are an important ‘cryptic’ component of the regional species pool. Bayesian linear regressions revealed that three measures of community diversity were positively associated with elevation: species richness (SR), Shannon entropy (H’), and phylogenetically-controlled species richness (PSR). Positive diversity–elevation trends in soil-banks of the Mojave Desert are the likely product of increasing moisture availability and frequent propagule production at higher elevations in dry mountain ranges.

In hot deserts of North America, bryophyte diversity re- bilization in arid ecosystems (Belnap and Lange 2001, flects the ability of individuals to reproduce, disperse, and Hardman and McCune 2010), we know little of how establish in the face of challenging abiotic conditions. Suc- soil-banks contribute to their diversity, either locally or cessful colonization results from at least one of three proc- across arid landscapes. Elsewhere, bryophyte soil-banks esses: 1) dispersal over distance; 2) soil-bank dormancy; have been described in a variety of habitats ranging from and 3) vegetative expansion of existing plants (During temperate grasslands, temperate wetlands and polar re- 1979). Soil-banks are of particular importance, not only gions (During 1986, Lewis-Smith 1987, Eckstein 2006), because they function as reservoirs of taxonomic and ge- where they are critical sources of colonization following netic diversity for bryophytes (Hock et al. 2008), but also disturbances of natural origin (Furness and Hall 1981, because they allow plants to avoid risks associated with Miles and Longton 1992a) and human origin (Bisang temporal fluctuations in stress and resource availability 1996, Hassel and Söderström 1998). Soil-banks are also (During 1997). Dormant propagules can remain viable important for colonization of bryophytes in tropical, bo- for nearly 50 years in dry soils (Whitehouse 1984), sug- real and temperate forests (Jonsson 1993, Rydgren and gesting that soil-banks are likely to exist in deserts, even in Hestmark 1997, Bisang et al. 2003, Ross-Davis and Frego locations where surface plants are absent. Assuming the 2004). Despite this range of studied habitats, soil-banks in persistence of propagules in soils of arid localities, soil- arid and semi-arid landscapes remain under-investigated. banks would be a key mechanism of ‘dispersal in time’, In one of the few available studies representing a semi- which permits desert bryophytes to avoid harsh abiotic arid region, soils from an African savanna exhibited sur- conditions and conditionally establish during favorable prisingly high diversity compared to surface communities periods. (During and Moyo 1999, During 2007), and featured one Despite the significant role of soil crust bryophytes moss genus that was new to science (Zander and During for nutrient dynamics, hydrological cycling, and soil sta- 1999). These findings suggest that bryophyte soil-banks

© 2013 The Author. This is an Open Access article. 1 in desert shrublands might similarly harbor ‘cryptic’ taxo- elevation soil-banks. While many low elevations (<1000 nomic richness. m) are typified by low species richness of surface bryo- The association of species richness with elevation is one phyte communities (Nash et al. 1977), the mechanisms of the fundamental questions in plant ecology (Whittaker maintaining diversity in sub-surface soil-banks may oper- 1960) and biogeography (Lomolino 2008). In bryophyte ate differently than in surface communities, and it remains communities surveyed along elevational gradients, spe- to be seen if elevation–richness patterns are consistent be- cies richness of surface communities can vary in a positive tween each profile. (Austrheim 2002), negative (Geissler and Velluti 1996), The purposes of this study were to characterize the or unimodal fashion (Wolf 1993), often depending on the diversity of bryophyte soil-bank communities in the length of the elevational gradient surveyed (Nogués-Bravo Mojave Desert, and to quantify changes in sub-surface et al. 2008). Elevation–richness patterns of bryophytes are diversity along a 1400 m elevational gradient. Because typically associated with moisture gradients that covary bryophyte reproduction in the region increases with el- with elevation (Lee and La Roi 1979), reflecting the fact evation and increasing moisture availability, I hypoth- that bryophytes are strongly dependent on external water esized that three separate measures of soil-bank diversity for growth and reproduction. In deserts of the southwest- would be positively related to elevation. Although simi- ern United States, persistent desiccation and water limita- lar approaches have been applied to other plant com- tion restrict reproductive frequency of surface bryophytes, munities, to my knowledge this study represents the first particularly at low elevations (Stark and Castetter 1987, to investigate a soil-bank community of bryophytes in a Benassi et al. 2011). In the absence of successful propagule temperate arid region, and the first to explicitly test the production and dispersal, meager deposition rates are also elevation–richness relationship for any bryophyte soil- expected to be reflected by minimal species richness in low bank.

Figure 1. Example of a mid-elevation soil collection site (1700 m a.s.l.) at Kyle Canyon on the eastern slopes of the Spring Mountain range in southern Nevada. Widely spaced Coleogyne ramossissima (blackbrush) shrubs are the dominant vegetation. Soils for germination were collected from vegetation-free areas in the open interspaces.

2 Methods per elevations (> 2000 m) were dominated by tall conifer- ous trees, mainly Pinus ponderosa Lawson & C. Lawson. In late September and early October of 2011, I sur- Study area and field collections veyed twelve sites along two parallel elevational gradients ascending the eastern slopes of the Spring Mountains (Ta- The Spring Mountains are a dry mountain range in the ble 1). The first transect (Kyle Canyon) included five sites Mojave Desert, approximately 40 km northwest of the spanning 1664–2235 m, while the second transect (Lee city of Las Vegas in southern Nevada, USA (36°00’6’’N, Canyon) included seven sites between 1019–2442 m. The 115°45’2’’W). On the eastern slopes of the Spring Moun- presence of mature vegetation and intact substrates at all tains (Fig. 1), limestone outcrops and wooded foothills sites indicated the absence of any recent fires or mechanical descend to sloping alluvial fans composed of shallow, disturbances. I collected four soil cores (10 cm diameter × well-drained, loamy-skeletal soils (USDA 2006). Much 3 cm depth) at each site from subjectively chosen patches of the terrain is dissected by dry washes created during (1 m2) that were free of any large rocks, litter, or surface episodic rainfall events. Annual precipitation in the area plants (including existing patches of bryophyte shoots). is sparse and highly variable (mean = 283 mm; SD ± 127 The 48 soil cores were sealed and immediately transported mm), following a bimodal seasonal pattern of late winter to the lab at room temperature in dry darkness before ger- showers and sporadic late-summer monsoons (National mination. Some cores were breached during transport and Climatic Data Center records for Spring Mountain State were discarded, yielding a total of 40 cores. Park, 1152 m a.s.l., period 1977–2011). At lower eleva- For germination, I air-dried and sieved each soil sample tions near 1000 m, local vegetation was dominated by the (355 µm fine wire mesh) to remove small rocks, coarse perennial evergreen shrub Larrea tridentata (DC.) Coville. organic matter, and any remnant plant parts, then placed Middle elevations (1200–1800 m) were characterized by a 4 cm3 subsample into 35 mm sterile polystyrene lidded the shrub Coleogyne ramosissima Torr., which intergraded culture dishes. Cultures were moistened, loosely covered at its upper limits with the small trees Pinus monophylla and maintained in a humid environment within a growth Torr. & Frém. and Juniperus osteosperma (Torr.) Little. Up- chamber, under a cycle of 12 h light (20°C) and 12 h dark

Table 1. Site descriptions, three community measures, and results of Bayesian linear regressions from soil-banks at twelve sites in the Spring Mountains of southern Nevada. Posterior means and credible intervals are in units of diversity per 1000 m change in elevation, all other values are in original units. See text for abbreviations.

Transect Elevation (m) Latitude N Longitude W Soil samples SR H’ PSR (canyon) Lee 2442 36°35’8’’ 115°66’4’’ 1 7 1.94 4.69 Lee 2346 36°35’3’’ 115°64’3’’ 1 5 1.6 3.16 Kyle 2235 36°25’9’’ 115°63’8’’ 4 7 1.94 4.69 Lee 2135 36°37’ 115°62’7’’ 2 5 1.6 2.99 Kyle 2002 36°27’2’’ 115°58’2’’ 4 4 1.38 3.24 Lee 1802 36°39’4’’ 115°58’5’’ 4 2 0.69 0.77 Kyle 1785 36°27’1’’ 115°54’4’’ 4 6 1.79 3.45 Kyle 1702 36°26’7’’ 115°51’1’’ 4 4 1.38 2.71 Kyle 1664 36°25’7’’ 115°52’1’’ 4 5 1.6 2.82 Lee 1524 36°41’8’’ 115°54’6’’ 4 5 1.6 2.47 Lee 1220 36°45’ 115°50’3’’ 4 4 1.38 2.24 Lee 1019 36°47’6’’ 115°47’ 4 2 0.69 1.47

Observed mean ± SD 4.64 ± 1.69 1.46 ± 0.43 2.89 ± 1.19 Observed range 2–7 0.69–1.95 0.77–4.69 Posterior mean of slope (β) parameter 2.47 0.60 1.82 95% Bayesian credible interval 0.48–4.56 0.01–1.11 0.35–3.15

3 (8°C). I also randomized two sterile soil samples among plied by the phylogenetic distance (‘branch length’ in a the culture dishes to detect unwanted aerial contamina- phylogenetic tree) between those species (Helmus et al. tion. Soil cultures were monitored twice weekly for mois- 2007). Therefore, related species give lower values for a ture and germination, and any vascular plant germinants site, and distantly related species give higher values. The were immediately removed. Preliminary observations tree upon which calculations were performed was manu- suggested that growth of microorganisms (e.g. fungi, cy- ally constructed using taxonomic distinctions defined by anobacteria, algae) in non-sterile soil had only a nominal the Bryophyte Names Authority List () of the Missouri Soil cultures were grown for five months to allow all prop- Botanical Garden. agules to germinate and reach identifiable stages, and at To detect elevation–diversity trends, I conducted monthly intervals I recorded the presence and identity of separate Bayesian linear regressions for each of the three bryophyte species in each sample. Bryophyte nomencla- diversity response variables using the package MHadap- ture follows Norris and Shevock (2004), with the excep- tive (Chivers 2012). Bayesian methods are flexible in that tion of the family Bryaceae which follows the recent revi- they provide a density distribution of possible hypotheses sions of Spence (2011). (the ‘posterior’) instead of simply assessing a rigid null hypothesis at a pre-defined confidence level (Gelman et al. 2004). Each regression began with flat, uninformative Statistical analyses priors and a linear log-likelihood function, and employed Metropolis–Hastings sampling of the Markov Chain over All analyses were performed in the R computing envi- 10 000 iterations; the first 2000 iterations (burn-in) were ronment (ver. 2.15.0; R Core Development Team) using discarded (Chivers 2012). supplemental packages as noted. To determine how climatic variables were associated with elevation, I obtained interpolated values for mean annual precipitation, tem- Results perature, relative humidity, and soil moisture for each of the twelve field sites from the FetchClimate web service Among twelve sites on the eastern slope of the Spring (), and then calcu- Mountains, elevation was positively correlated with mean lated pairwise Spearman correlation coefficients using the annual precipitation (Spearman correlation coefficient = packages Hmisc and corrplot. The FetchClimate web serv- 0.60), mean annual soil moisture (0.85), and mean an- ice generates interpolated values based solely on climate nual relative air humidity (0.85). Elevation was negatively data observations (National Oceanic and Atmospheric correlated with mean annual air temperature (–0.74). Administration records from 1948–2012, ) without regard to elevation information. the soil samples (Table 2). Of all bryophyte species, 58% For the species data, I assessed compositions by cal- represented the taxonomic family Pottiaceae, Bryaceae culating ordination site scores with non-metric mul- 17%, Funariaceae 11%, Ditrichaceae 5% and Encalyp- tidimensional scaling (NMS; Kruskal 1964) based on taceae 5%. There were few common species, and most Bray–Curtis distances and implemented in the package species were present in only a few sites (Table 2). External vegan. A two-dimensional solution was sought a priori contamination in the growth chamber was not detected from a maximum of 999 random starting configurations. by the sterile controls. The NMS ordination yielded two Composition–elevation trends were assessed visually by convergent solutions after ten random starts, with a final plotting site scores in the ordination space according to stress of 11.0%. The topology of NMS site scores plotted elevation. To assess the relationship between diversity and in species space suggested an association between species elevation, I first calculated three distinct measures of di- composition and elevation (Fig. 2). For example, commu- versity for each of the 12 sites. The first diversity measure, nities at lower elevation sites were associated with xeric species richness (SR), was the number of species in the species including Syntrichia caninervis Mitt. and Cross- pooled collection of soil cores at each site. The second idium aberrans Holz. & E.B. Bartram, while mesic species measure was Shannon entropy (H’), calculated for each such as Ceratodon purpureus (Hedw.) Brid. predominated site according to Oksanen et al. (2011). This measure in- at higher elevations (Fig. 2). Observations of the diversity tegrates the number of species at each site with the even- measures suggested a positive association with elevation, ness in the abundances among species; abundances were which was confirmed by the Bayesian regressions for all considered as the frequency of each species among each three measures (Table 1). Ninety-five percent Bayesian of the soil cores per site. The third measure, phylogenetic credible intervals for the regression slope parameter (β) species richness (PSR) was essentially an estimate of the did not include zero, consistent with a positive diversity– effective species richness of a site after accounting for elevation hypothesis (Fig. 3). Posterior means for each taxonomic relatedness. PSR was calculated in the picante slope parameter were: SR = 2.47 species; H’ = 0.597; and package as the number of species at a given site multi- PSR = 1.82 species per change in 1000 m.

4 Table 2. Species relative frequencies, expressed as the frequency of occurrence in 40 soil samples collected at the Spring Mountains, southern Nevada (n.d. = not determined).

Abbreviation Species Family Relative frequency (%) Bryarg Bryum argenteum Bryaceae 33.3 Bryrec Bryoerythrophyllum recurvirostre Pottiaceae 8.3 Cerpur Ceratodon purpureus Ditrichaceae 16.7 Croabe Crossidium aberrans Pottiaceae 25.0 Didvin Didymodon vinealis Pottiaceae 16.7 Encint Encalypta intermedia Encalyptaceae 8.3 Entmuh Entosthodon muhlenbergii Funariaceae 8.3 Fern Fern prothallus, n.d. n.d. 8.3 Funhyg Funaria hygrometrica Funariaceae 58.3 Gemcae Gemmabryum caespiticium Bryaceae 41.7 Gymspp Gymnostomum sp. Pottiaceae 25.0 Phacus Phascum cuspidatum Pottiaceae 8.3 Pteova Pterygoneurum ovatum Pottiaceae 75.0 Ptytur Ptychostomum turbinatum Bryaceae 8.3 Syncan Syntrichia caninervis Pottiaceae 41.7 Synrur Syntrichia ruralis Pottiaceae 25.0 Torbre Tortula brevipes Pottiaceae 8.3 Torine Tortula inermis Pottiaceae 8.3

Discussion bank diversity to elevation. The most noteworthy finding was that soil-bank diversity in the Mojave Desert was This study is the first to characterize species composition positively associated with elevation. Elevation was itself and diversity in bryophyte soil-banks of the driest desert significantly correlated with climatic variables including of the American Southwest, and to connect trends in soil- available moisture and temperature, indicating that eleva-

Figure 2. Results of NMS (non-metric multidimensional scaling) ordination (two-dimensional solution, stress = 10.9%) of bryophyte soil-bank communities. Site scores in species space are sized by elevation (left diagram), and species scores in species space are sized by relative frequency (right diagram). Lower elevation sites (lower left-hand corners) correspond with xeric species including Syntrichia caninervis, Crossidium aberrans, and Pterygoneurum ovatum. Abbreviations follow Table 2.

5 Figure 3. Three measures of diversity observed along the elevational gradient (top row), and posterior densities (bottom row) for the slope parameter (β) from Bayesian regressions of each diversity measure independently regressed on elevation. Values of β indicate the estimated change of the response variable for every 1000 meters of change in elevation, where values above zero (dotted lines) correspond to a positive relationship between each response and elevation. Note the difference in scales. tion can be a useful indicator of the stresses which bryo- sites. For example, Thompson et al. (2005) encountered phytes experience. Moisture and elevation are strongly 11 taxa (four shared in common with the current study) in linked in desert mountain ranges of the southwestern surface communities at other Spring Mountain locations United States, providing strong gradients which influence between 1030–1440 m, Bowker et al. (2000) reported six plant growth and reproduction (Smith et al. 1997). Stud- taxa (five shared) at 1494 m, and Nash et al. (1977) re- ies of surface vegetation in the region have shown fidelity ported just three species (three shared) at 1000 m, perhaps between elevation and bryophyte species compositions, indicative of moisture limitations at lower elevations. The which change along gradients corresponding to vegeta- moisture limitation concept was supported by my finding tion and climate. For example, Clark (2012) documented strong positive correlations between elevation and indica- compositional changes across 1000 m of vertical relief tors of moisture availability which included annual pre- spanning three vegetation zones at Grand Canyon Na- cipitation, soil moisture and relative humidity. tional Park in northern Arizona, revealing that acrocarpic, The generally positive elevation–diversity trend ob- xeric mosses of the Pottiaceae and Grimmiaceae families served in this study appears to parallel the positive trends predominated at lower elevations, and were superseded by observed at moderate elevations both in the Mojave mesic mosses (plus several liverworts) at higher elevations. Desert and elsewhere in the world. For example, Bisang I observed very similar patterns in soil-banks of the Spring et al. (2003) suggested that soil-bank richness in a tropi- Mountains, where Pottiaceae family members were well cal rainforest may increase with elevation. However, be- represented, although the saxicolous family Grimmiaceae yond approximately 2000 m, bryophyte species richness was conspicuously absent from soil profiles, perhaps be- in surface communities apparently declines, probably as cause its members require lithic substrates for germina- a result of increasing stresses (e.g. moisture and tempera- tion (Keever 1957). Outside of the southwestern United ture stresses) in some alpine zones (Geissler and Velluti States, Stehn et al. (2010) and Slack (1977) have observed 1996). Studies of very broad elevational gradients in excess similarly changing species compositions in montane sur- of 3000 m (Wolf 1993, Grau et al. 2007) often reveal a face communities of the eastern United States, supporting hump-shaped, unimodal relationship for bryophyte spe- the generality of the concept of compositional turnover cies richness in surface vegetation, with low-elevation in- along montane elevational gradients. creases eventually peaking and tapering in high montane Like species compositions, species richness in bryo- and alpine areas. Had the current study been extended phyte soil-banks of the Spring Mountains (17 taxa) cor- through the conifer forest and above upper treeline into responded well with the generally low species numbers the alpine zone, a similar unimodal peak and decline might found in the surface vegetation of other Mojave Desert have been expected for soil-bank species. Despite covering

6 three major vegetation–climate zones, the areas surveyed and John Brinda for confirming several species determinations. herein covered only the lower portion of a mountain range Partial funding was provided by the UNLV Graduate and Pro- that extends upward to 3633 m. Observing only a por- fessional Students’ Association, and by a UNLV Graduate As- tion of a larger elevation gradient could influence the ap- sistantship award. parent shape of the elevation–richness pattern (McCain and Grytnes 2010), which may explain the monotonic positive relationship which I observed in soil-banks of the References Spring Mountains. Bryophyte diversity at landscape scales is perhaps best Austrheim, G. 2002. Plant diversity patterns in semi-natural viewed in a context where local communities are sustained grasslands along an elevational gradient in southern Nor- way. – Plant Ecol. 161: 193–205. by dispersal from the regional species pool (During and Belnap, J. and Lange, O. L. 2001. Structure and functioning Lloret 2001, Leibold et al. 2004). In this regard, local of biological soil crusts: a synthesis. – In: Belnap, J. and richness and compositions are the product of stochastic Lange, O. L. (eds), Biological soil crusts: structure, func- immigration events which are then filtered by the capacity tion and management. Ecological Studies. Springer, pp. of bryophytes to tolerate local conditions. Like the ‘seed 471–479. rain’ of many vascular plants, the deposition of bryophyte Benassi, M., Stark, L. R., Brinda, J. C. et al. 2011. Plant size, sex spores (Miles and Longton 1992b) and asexual propagules expression and sexual reproduction along an elevation gradi- (Pohjamo et al. 2006) is greatest immediately around ent in a desert moss. – Bryologist 114: 277–288. source plants, and declines rapidly with distance. This is Bisang, I. 1996. Quantitative analysis of the diaspore banks of true from scales of several dozens of meters (Lönnell et al. bryophytes and ferns in cultivated fields in Switzerland. – Lindbergia 21: 9–20. 2012) to several hundreds of kilometers (Sundberg 2012), Bisang, I., Piipo, S. and Hedenäs, L. 2003. Bryophyte diaspore suggesting that proximity to reproductive plants may be bank in three Malaysian mountain rainforests. – J. Bryol. a strong determinant of the density and composition of 25: 68–70. propagules that comprise soil-banks (but see Hylander Bowker, M. A., Stark, L. R., McLetchie, D. N. et al. 2000. Sex 2009). Reproductive success increases with moisture expression, skewed sex ratios, and microhabitat distribution and elevation in southwestern USA deserts (Stark and in the dioecious desert moss Syntrichia caninervis (Pottiace- Castetter 1987), which suggests that soil-banks should be ae). – Am. J. Bot. 87: 517–526. richest at higher elevations where productive propagule- Chivers, C. 2012. General Markov chain Monte Carlo for Baye- producing plants occur more frequently. Conversely, low- sian inference using adaptive Metropolis–Hastings sam- elevation sites far from reproductive plants are expected pling. – to yield fewer soil-bank species, not necessarily because Clark, T. A. 2012. Bryophyte floristics and ecology in Grand propagules cannot survive there, but because their arrival Canyon National Park. Nat. Resour. Tech. Rep. NPS/ would require infrequent long-distance dispersal events SCPN/NRTR—2012/602. – National Park Service. originating from distant montane sources. During, H. J. 1979. Life strategies of bryophytes: a preliminary To summarize, this study documented 17 species of review. – Lindbergia 5: 2–18. bryophytes in sub-surface soil-banks along an elevational During, H. J. 1986. Longevity of spores of Funaria hygrometrica gradient covering 1400 m in a temperate arid mountain in chalk grassland soil. – Lindbergia 12: 132–134. range. 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Murithienne 114: 171– sites, and Katie Kleinick (BLM) and Donna Morell (UNLV) 178. in particular for helping secure survey permits. I am grateful to Gelman, A., Carlin, J. B., Stern, H. S. et al. 2004. Bayesian data Mandy Slate for assisting with field sampling, and to Lloyd Stark analysis. – Chapman and Hall/CRC Press.

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