- A simple classifcation of biological soil crust habitat on the Colorado Plateau - 831

Journal of Vegetation Science 19: 831-840, 2008

doi: 10.3170/2008-8-18454, published online 15 April 2008
IAVS; Opulus Press Uppsala.
A simple classifcation of soil types as habitats
of biological soil crusts on the Colorado Plateau, USA
Bowker, Matthew A.
1,2*
& Belnap, Jayne
3
1
Department of Biological Sciences, Northern Arizona University, Box 5640, Flagstaff, AZ 86011,USA;
Current Address: rea de Biodiversidad y Conservacin, Universidad Rey Juan Carlos, c/ Tulipn s/n., E-28933 Mstoles
(Madrid), Spain;
3
Southwest Biological Science Center, U.S. Geological Survey, 2290 S.W. Resource Boulevard, Moab, UT
84532, USA; E-mail: Jayne_Belnap@usgs.gov;
*
Corresponding author; E-mail Matthew.Bowker@urjc.es
Abstract
Question: Can a simple soil classifcation method, accessible
to non-experts, be used to infer properties of the biological soil
crust (BSC) communities such as species richness, evenness,
and structure?
Location: Grand Staircase-Escalante National Monument, an
arid region of the Colorado Plateau, USA.
Methods: Biological soil crusts are highly functional soil
surface communities of mosses, lichens and cyanobacteria that
are vulnerable to soil surface disturbances such as grazing. We
sampled BSC communities at 114 relatively undisturbed sites.
We developed an eight-tier BSC habitat classifcation based
upon soil properties including texture, carbonate and gypsum
content, and presence of shrinking-swelling clays. We used
simple structural equation models to determine how well this
classifcation system predicted the evenness, richness, and
community structure of BSC relative to elevation and annual
precipitation.
Results: We found that our habitat classifcation system
explained at least 3.5 more variance in BSC richness (R
2

= 0.57), evenness (R
2
= 0.59), and community structure (R
2

= 0.34) than annual precipitation and elevation combined.
Gypsiferous soils, non-calcareous sandy soils, and limestone-
derived soils were all very high in both species richness and
evenness. Additionally, we found that gypsiferous soils were
the most biologically unique group, harboring eight strong to
excellent indicator species.
Conclusions: Community properties of BSCs are overwhelm-
ingly infuenced by edaphic factors. These factors can be
summarized effciently by land managers and laypeople using
a simple soil habitat classifcation, which will facilitate incor-
poration of BSCs into assessment and monitoring protocols
and help prioritize conservation or restoration efforts.
Keywords: Biodiversity conservation; Cryptogam; Ecological
indicator; Ecosystem engineer; Land management; Microbiotic
crust; Soil chemistry.
Nomenclature: Zander 2008 (Bryophytes); Esslinger 2008
(Lichen).
Abbreviation: BSC = Biological soil crust.
Introduction
Biological soil crusts (BSCs) are a type of thin (< 1
cm), desiccation tolerant microbial mat of cyanobacteria,
subsequently colonized by mosses and lichens, living at
the soil surface in drylands. These BSCs act as ecosystem
engineers (Jones et al. 1997) and contribute strongly to
dryland ecosystem function (Belnap 2002; Beymer &
Klopatek 1991). For example, the flamentous cyanobac-
teria of BSCs chemically and physically aggregate the
soil surface into a thin horizontal layer, increasing erosion
resistance and infuencing water redistribution (Mazor
et al. 1996). In arid lands, vascular plants are known
to create fertility islands, but BSCs are a dominant
infuence in the creation and maintenance of soil fertil-
ity in interspaces between vascular plants. Mechanisms
through which BSCs increase fertility include carbon
(C)-fxation (Beymer & Klopatek 1991), nitrogen (N)-
fxation (Belnap 2002), and dust trapping (Reynolds et
al. 2000), among others. Biological soil crusts also have
potential to be highly valuable as ecological indicators
of ecosystem health (Tongway & Hindley 1996). For
these reasons and others, scientists should enable the
inclusion of these information-rich ecological indicators
in the management of public lands and other commons,
in addition to private lands.
Many previous studies have related environmental
factors to the community composition and structure
of BSCs at both small (< 1 m; Bowker et al. 2006a;
Rosentreter 1986; Martinez et al. 2006) and large scales
(100s of km
2
; Ponzetti & McCune 2001; Bowker et al.
2005; Thompson et al. 2006). Often, a confusing array
of inter-correlated factors also correlate with specifc
components of the BSC community (Eldridge & Tozer
1997). Not surprisingly, BSC abundance, composition,
and distribution are infuenced by climate variables
such as annual precipitation, maximal temperature, and
proximity to maritime air (Rogers 1972a; Nash & Mo-
ser 1982). Another strong infuence is the physical and
chemical environment of the soil (Downing & Selkirk
1993; Ponzetti & McCune 2001; Bowker et al. 2005).
832 Bowker, M.A. & Belnap, J
Soil chemical and physical properties are especially
diffcult to consider independently, for example pH,
CaCO
3
, electrical conductivity, and available fractions
of immobile nutrients (P, Mn, Zn, Cu, Fe) are usually
strongly autocorrelated. Surface disturbances, such as
livestock grazing, are also highly infuential in reducing
BSC abundance (Brotherson et al. 1983). Potentially, a
much simpler means of describing the soil habitat would
be a desirable step in both descriptive and predictive
modeling of BSC distribution and foristic patterns.
Biological soil crusts are easily damaged or destroyed
by compressional forces associated with several distur-
bance types, including off road vehicles, foot traffc of
humans and other animals, and mining and associated
exploration activities (reviewed in Belnap & Eldridge
2003). Of these, livestock grazing is not the most severe
(Belnap & Eldridge 2003), but is the most widespread
of disturbance factors affecting the large majority of
the western USA, and most arid rangelands of the
world (Dregne & Chou 1992). Because BSCs are also
notoriously slow to recover from disturbance, usually
requiring decades (Belnap & Eldridge 2003), BSCs are
rarely observed at their potential abundance, diversity,
and functional state. Land managers increasingly require
methods for inferring information about potential BSC
communities to incorporate into assessment and moni-
toring protocols, and also to prioritize conservation or
restoration efforts after overgrazing and other soil surface
disturbances. An easy to use scheme for inferring com-
munity properties of BSCs is also potentially useful in
traditional conservation applications (Goldstein 1999),
such as identifying regions of high biological uniqueness
or diversity (Myers et al. 2000).
Thus, we developed a simple scheme of classifying
soils with similar chemistry, texture, and sometimes
appearance that was informative in predicting overall
abundance of broad functional groups of BSCs (Table 1,
Bowker et al. 2006b). The ability of this soil classifcation
scheme to characterize BSC community composition and
structure has not been studied previously. Our classifca-
tion system does not require special expertise in either
BSC taxonomy or ecology, or in soil science, but it does
allow the user to infer consider information about the form
and function of the BSC community. This classifcation
is based solely on soil surface characteristics and can be
derived from widely available information such as geo-
logic maps or soil surveys, and characteristics that can
be measured in the feld (Schoeneberger et al. 1998). Our
classifcation system included eight soil types that include
the majority of the soil types found on the Colorado Plateau
(Table 1). This soil classifcation explained 17-73% of the
variance in 19 specifc physico-chemical soil descriptors.
We hypothesized that our soil classifcation system would
also perform well in predicting BSC community charac-
teristics, and outperform elevation and annual precipita-
tion as predictors. The former was expected because: (1)
soil chemistry and texture (calcium carbonate, gypsum,
and clay and silt content) infuence inherent soil stability
and nutrient availability, (2) shrinking and swelling clays
create unstable substrates for slow growing soil surface
organisms, and (3) increased pore space (determined
by texture) provides an easier substrate for flamentous
growth forms (e.g. cyanobacterial flaments). In contrast,
precipitation ultimately determines activity time of these
desiccation tolerant organisms, and elevation is a surrogate
for temperature which strongly infuences photosynthetic
rates of BSC organisms (Lange et al. 1998).
Material and Methods
Sampling design and survey methods
We conducted sampling over three years in the ca.
800 000-ha Grand Staircase-Escalante National Monu-
ment (Utah, USA). Our sampling design and survey meth-
ods were designed to capture a broad array of ecological
gradients in our sampling strategy and are described in
detail in Bowker et al. (2006b). We divided the study area
into three precipitation brackets ( 20 cm.a
1
, 20 - 30
cm.a
1
, 30 cm.a
1
). All sites were classifed as one of
eight mutually exclusive soil types (Table 1): bentonitic
clay soils, calcareous sandy soils, non-calcareous sandy
soils, gypsiferous soils, siliceous sandy soils (these are
also non-calcareous, but are distinguished by large grain
size, and siliceous cementing in parent materials), non-
bentonitic fne soils, Kaiparowits-derived soils (a sandy
textured parent material that is unique because it forms
highly erodible badlands), and limestone-derived soils.
Soils were assigned to these soil types using information in
the GSENM Soil Survey (US Department of Agriculture-
Natural Resource Conservation Service [USDA-NRCS]
2005). All possible combinations (some did not exist in
GSENM) of soil type precipitation bracket were sampled
and replicated (average n = 6, range 2 - 18) for a total of
114 sites. Only sites with relatively minor soil surface
disturbance impacts were chosen for sampling, thus we did
not have the luxury of a balanced random design. Rarity on
the landscape accounted for low replication in a few soil
type precipitation combinations, but common combina-
tions were well replicated. At the completion of sampling,
we had 6 - 37 replicate sites of each soil type, and 19 - 49
replicate samples for each precipitation bracket.
To measure crust cover and composition, we used
a step point-intercept transect (modifed from Evans &
Love 1957) consisting of 300 points (spaced ca. 2 m
apart) at each of the 114 sampling sites. At each point,
ground cover measures were recorded, including mosses
- A simple classifcation of biological soil crust habitat on the Colorado Plateau - 833
Table 1. A dichotomous key and descriptions of soil types.
1a. Soils primarily consist of clay- and silt-sized particles. Clay content is almost always greater than 30%. Surfaces generally exhibit a roughened popcorn-
like texture due moderate to high shrink-swell capacity ( 4.5%).Bentonitic fne soils
1b. Soils are either more sand-dominated, or in some cases roughly equal proportions of sand, and clay size fractions. Clay content is almost always less than
30%. Soil surfaces may be roughened due to frost-heaving of biological soil crusts, but shrink-swell capacity is generally low2
2a. Soils contain at least 10% gypsum. Soil texture generally not sand-dominated, more often loamy. Soils often have visible exposures of white-gray
gypsum beds.Gypsiferous soils.
2b. Soils contain less than 10% gypsum. Soil texture may be loamy, but is more often sand-dominated. Exposures of gypsum are lack-
ing..3
3a. Soils are non-calcareous. There is little or no effervescence of HCL, [0, 0-3, or occasionally 1-5% calcium carbonate (CaCO
3
) equivalent
in USDA soil survey]. Textures are clearly sand-dominated4
4a. Soils are highly sand-dominated (> 75% sand sized particles). May be weathered in place from siliceously-cemented bedrock
(e.g. Navajo Sandstone) or eolian deposits of similar material Siliceous sandy soils
4b. Soils are sand-dominated but contain < 75% sand-sized particles. May be weathered in place (not from Navajo Sandstone), or
on well-weathered alluvial or fuvial terraces, or derived from parent material poor in CaCO
3
Non-calcareous soils
3b. Soils are calcareous. There is at least moderate effervescence of HCL at soil surface, usually > 5 maximum CaCO
3
equivalent. Textures
are variable5
5a. Soils effervesce strongly, generally containing maximal CaCO
3
equivalent > 15%. Derived from either Kaiparowits Formation
(Fm.), Timpoweap Member (Mbr.) of Moenkopi Fm., Kaibab Fm., or non-gypsiferous, non-limestone members of the Carmel
and Moenkopi Fms. ..6
6a. Soils are derived from the Kaiparowits Fm. and commonly occur in highly
eroded, gray-colored badlands, soil has sandy salt-and-pepper appearance Kaiparowits-derived soils
6b. Soils are often light colored (e.g. gray, yellowish-gray, pale orange), and are derived
from limestone (Timpoweap Mbr. of Moenkopi Fm. or Kaibab Fm. in
GSENM)..Limestone-derived soils
6c. Soils are deep orange or red grading into vermillion, and are derived from non-
gypsiferous, non-limestone members of the Moenkopi Fm. and Carmel Fm., often channery at surface Non-bentonitic
fne soils
5b. Soils are usually less effervescent, and less calcareous, but defnitely effervescent. Soils are not derived from above listed
formations, and do not generally occur in badlands. Most of these soils are sand-dominated, but include some loamy textured
soils as well.Calcareous sandy soils
Bentonitic fne soils (B): Weathered in place from Tropic Fm., Blue Gate & Tununk Mbrs. of Mancos Fm., Brushy Basin Mbr. of Morrison Fm.,
and various shale members of the Chinle Fm.; Colors variable but often impressive, may include grays, reds, mauve, and green; Forming badland landscapes
supporting very sparse vegetation, including the dwarf Atriplex corrugata; highly effervescent due to CaCO
3
and other carbonates; may be somewhat gypsif-
erous, but not containing whitish gypsum beds; clay sized particles predominate and smectitic clay minerals generate high shrink-swell capacity; Generally
lacking in BSC cover.
Gypsiferous soils (G): Weathered in place from Shnabkaib Mbr. of Moenkopi Fm., Crystal Creek and Paria River Mbrs. of Carmel Fm., and Paradox
Fm.; Gypsum-rich patches generally whitish or grayish, surrounding soil surface is reddish in many cases; Vegetation variable (Artemisia, Atriplex, Ephedra
and Pinus-Juniperus); Containing CaCO
3
, but gypsum always more abundant; Contain beds or pockets of gypsum, including alabaster cliffs in some cases;
Gypsum-rich microsites dominated by silt and clay sized particles, surrounding matrix may be more sandy; Potentially supporting high cover of moss and
lichen rich BSCs.
Siliceous sandy soils (S): Weathered in place or wind transported from non-calcareous siliceously-cemented sandstones (e.g. Navajo Sandstone and
Coconino Sandstone); Color may be nearly white to pink to deep orange; Vegetation variable, depth-dependent (includes desert grasslands and Artemisia
communities); CaCO
3
and gypsum lacking; Texture strongly skewed toward coarse sand; Potentially supporting high cover of cyanobacterial soil crusts.
Non-calcareous sandy soils (NC ): Derived from various parent materials (usually weakly calcareous, including Judd Hollow Mbr. of Straight Cliffs
Fm., or Shinarump Mbr. of Chinle Fm. but exclusive of siliceous sandstones), but surface weathering has been strong enough to leach out CaCO
3
; Colors vary,
dependent on parent material; Vegetation various, commonly Artemisia; Most abundant in relatively high precipitation areas due to greater leaching; Contain-
ing little or no CaCO
3
or gypsum; Dominated by sand sized particles (often poorly sorted), but generally less coarse than Siliceous sandy soils; Potentially
supporting moderate to high cover of cyanobacterially dominated BSCs, with a rich moss and lichen component.
Kaiparowits-derived soils (K): Weathered in place from the Kaiparowits Fm. Occur in gray colored badlands, with variable climate-dependent
vegetation; Violently effervescent due to carbonates, lacking gypsum; Texture is sand-dominated, with distinctive salt-and-pepper appearance. Generally
lacking BSC cover.
Limestone-derived soils (L): Weathered in place from any limestone (e.g. Kaibab Fm. or the Timpoweap Mbr. of Moenkopi Fm.; Colors range from
grays to pale yellow or orange coloration (dependent on parent material); Vegetation climate-dependent, usually Artemisia or Pinus-Juniperus dominated;
Moderately effervescent due to presence of CaCO
3
, gypsum not abundant; Texture generally loamy, but dependent on parent material; Potentially supporting
high cover of moss and lichen rich BSCs.
Non-bentonitic fne soils (NB): Weathered in place from non-limestone, non-gypsiferous, and non-bentonitic fuvial shale red beds (e.g. Mbrs. of
Moenkopi Fm., Carmel Fm., Halgaito Fm., Organ Rock Fm., Hermit Fm.); Notably deep orange, red or purple colored; Vegetation often sparse, including
Coleogyne, Artemisia, and Pinus-Juniperus; Moderately effervescent due to presence of CaCO
3
, gypsum not abundant; Texture usually loamy, but sand fraction
is fne; conspicuous fat channers often on surface, exposed soil forms a vesicular physical crust; Potentially supporting very low to moderate cover of moss
and lichen BSCs, dependent on moisture. Calcareous sandy soils (C): Derived at least partially from any calcareous sandstone, exclusive of the Kaiparowits
Fm. (e.g. Kayenta Fm., Entrada Sandstone, Dakota Fm. among several others), weathering has not been suffcient to remove all CaCO
3
from soil surface;
Colors variable, dependent on specifc parent material; Vegetation highly variable, climate dependent; Usually moderately effervescent, gypsum content
minor; Texture generally skewed toward more sandy size classes, although some soils are loamy; Potentially supporting low to moderate cyanobacterial BSC
cover, with some mosses and lichens.
834 Bowker, M.A. & Belnap, J
and lichens to species, light cyanobacterial BSCs (early
successional BSCs, almost exclusively Microcoleus
spp.), and dark cyanobacterial BSCs (later succesional
BSCs dominated by Microcoleus spp., Nostoc spp. and
Scytonema spp.).
Statistical analysis
To determine the relative contribution of three
environmental predictors linked to soil stability and
fertility, and physiological activity of BSC organisms
(soil type, annual mean precipitation [modeled within
a 5.08 cm resolution], elevation [values obtained us-
ing GPS]) to BSC richness, evenness (Pielous J), and
community structure, we used three simple structural
equation models (SEM) in Amos 5.0 (SPSS Inc., Anon.
2003). These models were essentially equivalent to
multiple regression models except that they allowed
the inclusion of the categorical predictor soil type as a
composite variable (Grace 2006), allowed the inclusion
of correlated predictors by specifying their relationship
to one another (e.g. our models specifcally state that
annual precipitation is infuenced by elevation), and used
a maximum likelihood technique to estimate regression
weights simultaneously. Often, researchers using SEM
advance a causal hypothesis and test the goodness of ft
of their model structure. In this case, the causal order-
ing of the variables in the models is known with high
confdence; thus, a test of ft was not of interest. Instead,
because we were interested only in maximum likelihood
estimates of regression weights and R
2
, we allowed all
of the predictors to freely covary, creating a saturated
model. Saturation precludes an overall goodness of
ft test, which is not of consequence here. Community
structure was a synthetic response variable derived from
a non-metric multidimensional scaling (NMDS) ordina-
tion. We used the slow and thorough autopilot setting
in PC-ORD 4.0 (MJM Software Design 1999), which
selects optimal dimensionality of the ordination using a
Monte Carlo test. In this and subsequent NMDS ordina-
tions, we used the Bray-Curtis distance measure because
it is compatible with the distribution problems common
to community data. Data were relativized to species
maximum (i.e. data for each species was rescaled from
0-1). This transformation suppresses the effect of a few
dominant taxa upon the analysis, and gives equal weight
to all community members; this is valuable in broadening
inference from the species to the community level. The
ordination was one-dimensional, thus the axis scores
were used as a univariate variable in our SEM.
To determine how specifc soil types differed in
species richness and evenness, we used two ANOVA
models in JMP IN 5.0 (SAS Inst. 2005). To determine
specifcally how community structure changed among
soil types, we used indicator species analysis (Dufrene
& Legendre 1997) in PC-ORD (MJM Software Design
1999). Indicator species analysis uses abundance and
frequency data to yield a percent of perfect indication
value for each variable-group combination and uses a
Monte Carlo test to determine the probability of obtain-
ing a given indicator value (IV) due to chance alone. We
defned a strong indicator of a particular soil type as
one with an IV of 0.25-0.50, a very strong indicator as
one with an IV of 0.51-0.75, and an excellent indicator
as one with an IV 0.76.
Fig. 1. Three structural equation models of identical structure
using three predictors (soil type, elevation, and annual pre-
cipitation) as determinants of three responses: BSC species
richness, evenness, and community structure. Rectangles
represent measured variables. The composite variable (Grace
2006) soil type is represented by a diamond. Unidirectional
arrows represent a directed causal infuence of one variable upon
another. Bidirectional arrows represent undefned covariance
between a pair of variables. Path coeffcients, appearing above
unidirectional arrows, are equivalent to regression weights or
partial correlation coeffcients (width of arrows is proportional
to path coeffcients). R
2
appears above every endogenous vari-
able and is interpreted as for any linear model. In all three cases,
soil type is the best predictor of BSC parameters.
a
correlations
of elevation with soil types: B = 0.10, G = 0.26, L = 0.35, NB
= 0.06, NC = 0.17, K = 0.04, S = 0.02.
b
correlations of pre-
cipitation with soil types: B = 0.24, G = 0.11, L = 0.23, NB
= 0.12, NC = 0.22, K = 0.04, S = 0.03. **** P < 0.0001
- A simple classifcation of biological soil crust habitat on the Colorado Plateau - 835
Results
BSC community properties as a function of environ-
mental predictors
Using simple structural equation models with
soil type, elevation, and precipitation as predictors, we
were able to explain more than half of the variance in
BSC species richness (R
2
= 0.57), about a third of the
variance in community structure (R
2
= 0.34), and over
half in BSC evenness (R
2
= 0.59) (Fig. 1).
In the case of richness and community structure, soil
type was much more informative than the other variables,
although they did make contributions. We found that in
the case of evenness, soil type (r = 0.77) accounted for
virtually all of the variance explained (Fig. 1).
BSC community properties as a function of soil type
Both species richness (F = 17.7429, P < 0.0001)
and evenness (F = 68.1449, P < 0.0001) were strongly
infuenced by soil type (Fig. 2). Richness was about six
times higher in gypsiferous soils compared to bentonitic
fne soils and Kaiparowits-derived soils; the other soil
types were intermediate. Evenness exhibited a similar
pattern except that limestone-derived soils were the
most even and were similar to gypsiferous soils; again
bentonitic fne soils and Kaiparowits-derived soils were
much lower (about fve-fold) and other soil types were
intermediate.
Because BSC community structure was also largely
a function of soil type, we conducted an indicator spe-
cies analysis. A total of 19 out of 59 species and other
taxonomic groups were strong to excellent indicators
(defned as IV > 25) of individual soil types (Table 1).
Bentonitic fne soils, calcareous sandy soils, Kaiparowits-
derived soils and non-bentonitic fne soils had no strong
indicator species. Gypsiferous soils had eight strong to
excellent indicators; seven of these were very strong,
(Lecanora gypsicola, Psora decipiens, Didymodon
nevadensis, Diploschistes diacapsis, Squamarina len-
tigera, Acarospora nodulosa ssp. nodulosa), and two
were excellent indicators (Catapyrenium spec., Ful-
gensia bracteata) primarily due to their fdelity to this
soil type. Limestone-derived soils were characterized
by fve strong indicators, of which Aspicilia aspera and
Psora cerebriformis were very strong. Siliceous sandy
soils and non-calcareous sandy soils each had two strong
indicators. However they were not as strong as those
for the gypsiferous soils or limestone-derived soils due
to lack of fdelity in the case of siliceous sandy soils,
and a lack of consistency in the case of non-calcareous
sandy soils.
Discussion
These data suggest that soil characters are by far
the most infuential natural abiotic predictor of the
richness, evenness, and community structure of BSCs
of the Colorado Plateau. A simple system of eight soil
types provides a relatively non-technical means of sum-
marizing BSC community properties. This information
is potentially applicable in inferring reference states in
range management (Bowker et al. 2006b) and ecological
restoration (Bowker 2007), conservation of BSC function
(Bowker et al. in press), and reserve design for conserv-
ing biodiversity of BSCs.
A useful framework for classifcation of BSC habitat
on the Colorado Plateau
The majority of soils of the Colorado Plateau are
characterized primarily by residuum weathered in place
from sedimentary rocks. Of the fve factors of soil for-
mation (Jenny 1941), parent material (i.e. geology) has
Fig. 2. Species richness and evenness as a function of soil
type. Error bars represent one standard error. B = bentonitic
fne soils, K = Kaiparowits-derived soils, C = calcareous sandy
soils, S = siliceous sandy soils, NB = non-bentontitic fne soils,
NC = non calcareous sandy soils, G = gypsiferous soils, L =
limestone-derived soils. Shared letters indicate Tukey-Kramer
test, P > 0.05.
836 Bowker, M.A. & Belnap, J
Table 2. Results of indicator species analysis, by community member or community type. Soil type refers to the soil type for which
a community member has the highest indicator value IV. B = bentonitic fne soils, C = calcareous sandy soils, G = gypsiferous soils,
K = Kaiparowits-derived soils, NB = non-bentontitic fne soils, NC = non calcareous sandy soils, S = siliceous sandy soils. Bold
I.V. and associated P-values indicate species that are strong to excellent indicators.
Species Taxonomic Group Soil type I.V. P
light cyanobacterial crust Cyanobacterial community C 15.9 0.11
dark cyanobacterial crust Cyanobacterial community S 33.8 0.0002
Aloina bifrons Moss G 20.3 0.03
Aspicilia hispida Lichen L 73.7 0.0002
Aspicilia aspera Lichen L 14.5 0.09
Aspicilia desertorum Lichen NC 34.7 0.0028
Aspicilia or Lecanora spec. Lichen S 12.7 0.19
Acarospora nodulosa Lichen G 58 0.0002
Acarospora schleicheri Lichen NC 25 0.010
Bryum argenteum and lanatum Moss S 32.3 0.003
Bryum kunzei Moss G 7.4 0.57
Bryum caespiticium Moss L 16.2 0.09
Crossideum spec. Moss G 18 0.03
Collema coccophorum Lichen L 41.1 0.0004
Catapyrenium spec. Lichen G 90 0.0002
Placidium spp. Lichen G 22.6 0.04
Ceratodon purpureus Moss NC 24.6 0.03
Cladonia pyxidata Lichen S 19.2 0.05
Collema tenax Lichen G 20.9 0.14
Candellariella terrigena Lichen NC 26.9 0.05
Calopolaca tominii Lichen G 23.6 0.03
Caloplaca jungermanii Lichen L 18.6 0.02
Caloplaca lactea Lichen L 20 0.01
Diploschistes muscorum Lichen NC 19 0.03
Diploschistes diacapsis Lichen G 64.3 0.0002
Didymodon nevadensis Moss G 66.7 0.0002
Desmatodon spec. Moss C 2.7 -
Didymodon vinealis Moss C 2.7 -
Endocarpon pusillum Lichen NB 20.1 0.06
Encalypta spp. Moss S 10.8 0.13
Fulgensia desertorum Lichen G 6.5 0.91
Fulgensia bracteata Lichen G 87.8 0.0002
Gypsoplaca macrophylla Lichen G 23.4 0.01
Grimmia orbicularis Moss G 33.3 0.0006
Grimmia anodon Moss L 10 0.23
Brachythecium collinum Moss C 2.7 -
Heppia spec. Lichen NC 6.2 0.68
Lecanora gypsicola Lichen G 74.6 0.0002
Leptogium lichenoides Lichen B 3.4 0.81
Lecanora muralis Lichen NC 21.3 0.02
Lecanora cf. zosterae Lichen B 3.5 0.93
Nostoc cf. fagelliforme Cyanobacterium L 23.5 0.02
Rinodina spec. Lichen NC 6.2 0.67
Psora cerebriformis Lichen L 57.7 0.0002
Psora globifera Lichen L 6.6 0.48
Psora pruinosa Lichen NC 19.8 0.04
Psora decipiens Lichen G 67.8 0.0002
Pterygoneurum ovatum Moss L 24.4 0.01
Peltigera rufescens Lichen NC 12.5 0.11
Pterygoneurum subsessile Moss L 8.2 0.24
Psora tuckermanii Lichen L 26.9 0.0128
Peltula patellata Lichen G 14.3 0.24
Unknown pyrenolichen Lichen C 2.7 -
Squamarina lentigera Lichen G 58.3 0.0002
Syntrichia caninervis Moss L 29.4 0.004
Syntrichia ruralis Moss S 24.1 0.06
Tortula brevipes Moss G 10.1 0.19
Tortula mucronifolia Moss K 16.7 0.05
Toninia sedifolia Lichen L 45.9 0.002
- A simple classifcation of biological soil crust habitat on the Colorado Plateau - 837
the dominant infuence because of the very different
textures and chemistries of the various rock formations
and due to the relative young age of many of the soils.
This differs considerably from the Great Basin, Mojave,
and Sonoran Deserts where older soils are composed
primarily of transported material of various origins,
and where climate, age of alluvial parent materials, and
slope may play more important roles in soil development
(Scull et al. 2004). In contrast, the complex and diverse
mosaic of geological formations in the Colorado Plateau
results in more stark differences and heterogeneity
among soils, but also more predictable soil properties.
Thus, considerable information can be inferred about
BSCs and other biota from geological surveys.
The system of eight soil functional types used here is
based upon observations and formal surveys of hundreds
of sites across the Colorado Plateau. Classifcation rules
(Table 1) are based upon available information in soil
surveys (e.g. soil physico-chemical properties and often
parent material; USDA-NRCS, Anon. 2005), geological
surveys (e.g. descriptions of parent materials; Doelling
& Davis 1989), and feld-observable characteristics
(Schoeneberger et al.1998). Bowker et al. (2006b) found
that this system explained variance in 19 different soil
properties, reducing the coeffcient of variation by 35%
on average. It is broad enough that it can be applied to
most soils of the Colorado Plateau and potentially to
other regions. To truly broaden our system to cover the
entire Colorado Plateau, additional soil types may need
to be invoked. Basalt-derived soils, and granite-derived
soils, are two potential additional groups that could be
added to this classifcation system in the future.
As with many groups of biota, BSCs appear to
contain species that are generalists and specialists. At
one extreme, some of the most common taxa occur
in virtually all deserts of the world, e.g. Microcoleus
vaginatus, Collema tenax or coccophorum, and Anomo-
bryum argenteum (Belnap & Lange 2003). Other taxa
have a high fdelity for particular soil chemical or
textural characters, e.g. Aspicilia hispida or A. aspera
and CaCO
3
, and Lecanora gypsicola and gypsum. Both
calcium carbonate and gypsum, can reduce the avail-
ability of immobile nutrients such as P, and free Ca+
ions can also displace exchangeable cations such as K+
and Mg+ in cells (Lajtha & Schlesinger 1988; Bates
& Farmer 1990). Habitat specialization based upon
calcium compounds in the soil may refect a disparity
in mechanisms for nutrient uptake. Furthermore, in
the case of gypsum specialization, sulfur may play an
important role as three of our very strong gypsum indica-
tors (Table 1; Diploschistes diacapsis, Psora decipiens,
and Squamarina lentigera) are also known to inhabit
the edges of sulfur-rich thermal springs (Rosentreter
& Belnap 2003). Soil texture can potentially have
many effects. High silt and clay content is likely to
increase water holding capacity of the soil which could
favor less drought-resistant BSC taxa (Anderson et al.
1982). Sandy soils also tend to be less aggregated and
therefore less stable, so perhaps the fastest-growing
BSC organisms (the cyanobacteria) are favored on
the sandier substrates (Dougill & Thomas 2004). In
addition, the greater pore spaces may present fewer
physical barriers to flamentous cyanobacteria. Poten-
tially, some combination of the latter two mechanisms
may have led to establishment of well-developed dark
cyanobacterial crusts on siliceous sandy soils (Table
1), the sandiest soils in our study region. No species
favored bentonitic clay soils, in fact these substrates
were nearly devoid of BSCs (also observed in Bowker
et al. 2005). Although we cannot rule out a chemical
mechanism to explain this, the simplest explanation is
that shrinking and swelling clays and high susceptibil-
ity to water erosion make these substrates very diffcult
for BSCs to colonize. In total, over half of the species
encountered exhibited at least some degree of habitat
specialization, and over one third of these were quite
strong (Table 1). Although the mechanisms behind these
physico-chemical soil preferences of specialist species
are not well understood, the phenomenon is highly
predictable using the soil types outlined here.
The specifc classifcation rules listed in Table 1
are designed for use across the 337 000-km
2
Colorado
Plateau region of the USA, but could be modifed for
use in other arid regions of the world. The key in accom-
plishing this is identifcation of the important abiotic
gradients which predict BSC community properties,
and classifcation of soils based upon possible combina-
tions of these properties. Examples of the same abiotic
gradients having predictive power for BSC community
properties in other regions include: soil texture Aus-
tralia (Eldridge & Tozer 1997; Thompson et al. 2006),
shrink-swell clays Italy (Loppi et al. 2004), gypsum
content Tunisia and Australia (Ullman & Bdel 2003),
Spain (Guerra et al. 1995), Namibia (Lalley & Viles
2005), and calcium carbonate content Tunisia and
Australia (Ullman & Bdel 2003); Columbia Basin,
USA (Ponzetti & McCune 2001). Fortunately many of
these characteristics are measured in or can be inferred
from geological surveys and soil surveys, and in many
cases maps already exist which can be used in GIS
applications.
838 Bowker, M.A. & Belnap, J
An application: reserve design for conserving biodi-
versity of BSCs
We previously developed an approach to conserva-
tion and restoration prioritization based upon BSC
functional signifcance which uses the same predic-
tors to determine where on the landscape BSCs may
play disproportionate roles in ecosystem function, and
overlays the information upon additional information
describing probability of surface disturbance (Bowker et
al. in press). Thus, we can identify the areas where BSCs
have the greatest signifcance and are simultaneously
most likely to be disturbed in the present or future; the
former might be considered restoration priority areas,
and the latter may be considered conservation priority
areas. Additionally, our soil classifcation system has
been used to model potential cover of key BSC types for
use as a reference condition parameter in either range
management or restoration-rehabilitation applications
(Bowker et al. 2006). In contrast to these applications,
when BSC biodiversity is the object of conservation, a
reserve design incorporating key gradients and regional
hotspots could be more useful. Of course, by acting to
conserve both organisms and function we could most
comprehensively protect these systems.
Traditional approaches to conservation of various
groups of taxa have often sought to determine which
spatial locations or habitat types support the greatest
biodiversity or biological uniqueness (Myers et al. 2000,
Stohlgren et al. 2005). Based upon the present work,
we can clearly say that conservation of BSC taxa would
be most effective via reserves on three soil types: non-
calcareous sandy soils, gypsiferous soils, and limestone-
derived soils. These three soil types were the richest and
also most even communities. Among the three groups,
there were a total of 15 indicator species, indicating
that these soil types contain many habitat specialists.
Non-specialist species are also well represented in this
soil type, indeed only a handful were never represented
in either gypsiferous soils, non-calcareous sandy soils,
and limestone derived soils. It appears that to a large
degree, the BSC fora of other soil types are a subsets
of the fora found on these three soil types.
For at least three decades, gypsiferous soils have
been known to harbor both a diverse and unique
community of soil crusts in both North America and
Europe (Anderson & Rushforth 1976; Guerra et al.
1995; Martinez et al. 2006). While fairly common
in the Mediterranean regions of Europe (Martinez et
al. 2006), gypsiferous soils are rare on the Colorado
Plateau. Examples of this unique and poorly studied
fora of Colorado Plateau gypsiferous soils include
three globally rare species frst described in the 1990s
(Didymodon nevadensis, Lecanora gypsicola), one
more broadly distributed species that was undetected
in North America until the 1980s (Acarospora nodulosa
ssp. nodulosa), and one globally rare genus and species
(Gypsoplaca macrophylla; St. Clair & Warrick 1987;
Zander et al.1995; Rajvanshi et al. 1998).
In contrast, most of the species of non-calcareous
and limestone-derived soils are widespread, however
the species turnover between these two habitat types
is large.
In addition to representing these regional-scale
hotspots that are rich in habitat specialists and are
biologically unique, it is important to capture important
ecological gradients in reserve design in heterogenous
areas (Diamond 1975). Climatic gradients are impor-
tant, but as we have shown here, edaphic gradients are
more important to the structure of BSC communities.
Thus, reserve design could primarily be based upon
edaphic gradients. Aside from gypsum content, perhaps
the most important gradient to capture is CaCO
3
content.
Calcareousness of substrates, either rock or soil, have
long been known to infuence the potential lichen and
moss communities (Downing & Selkirk 1993; Ponzetti
& McCune 2000). Additionally, soil texture has long
been recognized as an important determinant of BSC
development (Anderson et al. 1982).
Thompson et al. (2006) suggest that for BSCs, small
reserves would be adequate because species-area curves
saturate quickly. Although we did not study species-area
relationships specifcally, our observations agree with
this statement as long as the system of small reserves
(each of perhaps several hectares) capture variance
in the key gradients mentioned above. However, it is
important to explicitly state that this assertion applies
only to biodiversity conservation of BSC, and that small
reserves cannot appreciably conserve BSC function in
the larger ecosystem. Reserves are merely islands in a
matrix of landscape being used for livestock production,
a major negative infuence upon BSC development.
Incorporation of BSCs into land management ap-
plications such as reserve design and resource manage-
ment plans (Bowker et al. 2006b; Bowker et al. 2007)
requires the delivery of accessible tools to managers,
who cannot be expected to also be BSC experts. With
the application of the BSC habitat classifcation system
described here, non-specialists can make informed deci-
sions about where BSC biodiversity or function might
be conserved, and where BSCs might be most useful
as ecological indicators.
- A simple classifcation of biological soil crust habitat on the Colorado Plateau - 839
Acknowledgements. We thank GSENM (US Bureau of Land
Management) for funding this research. Dr. N. Johnson, S.
Reed, N. DeCrappeo, B. Chaudhary, A. Antoninka and M. Lau
provided useful comments on early drafts. Dr. Jan Bakker and
two anonymous reviewers helped us improve an early draft. We
thank Drs. K. Sutcliffe and M. Miller for providing valuable
consultation concerning the planning of this research. Dr. T.
ODell, S. Stewart, H. Barber, P. Chapman, and members of the
GSENM staff assisted with logistical support. Drs. J. Spence
and T. Graham provided helicopter access to remote sites. L.
Pfenninger, S. Bartlett, J. Brundage, K. Kurtz, C. Nelms, E.
Kneller, W. Fertig, and L. Fertig provided indispensable feld
assistance. Drs. R. Rosentreter, L. Stark, and J. Spence provided
consultation on diffcult lichen and moss identifcations. The
use of trade, product, or frm names in this publication is for
descriptive purposes only and does not imply endorsement by
the U.S. Government.
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Received 6 September 2007;
Accepted 18 December 2007;
Co-ordinating Editor: J.P. Bakker.