ORIGINAL RESEARCH
published: 17 December 2019
doi: 10.3389/fevo.2019.00482
Neglected but Potent Dry Forest
Players: Ecological Role and
Ecosystem Service Provision of
Biological Soil Crusts in the
Human-Modified Caatinga
Michelle Szyja 1*, Artur Gonçalves de Souza Menezes 2 , Flávia D. A. Oliveira 2 , Inara Leal 2 ,
Marcelo Tabarelli 2 , Burkhard Büdel 1 and Rainer Wirth 1
1
Plant Ecology & Systematics, University of Kaiserslautern, Kaiserslautern, Germany, 2 Departamento de Botânica,
Universidade Federal de Pernambuco, Recife, Brazil
Edited by:
Nicole Pietrasiak,
New Mexico State University,
United States
Reviewed by:
Scott Ferrenberg,
New Mexico State University,
United States
Gianalberto Losapio,
ETH Zürich, Switzerland
*Correspondence:
Michelle Szyja
michelle.szyja@web.de
Specialty section:
This article was submitted to
Biogeography and Macroecology,
a section of the journal
Frontiers in Ecology and Evolution
Received: 28 June 2019
Accepted: 25 November 2019
Published: 17 December 2019
Citation:
Szyja M, Menezes AGS, Oliveira FDA,
Leal I, Tabarelli M, Büdel B and Wirth
R (2019) Neglected but Potent Dry
Forest Players: Ecological Role and
Ecosystem Service Provision of
Biological Soil Crusts in the
Human-Modified Caatinga.
Front. Ecol. Evol. 7:482.
doi: 10.3389/fevo.2019.00482
Biological soil crusts (biocrusts) have been recognized as key ecological players in arid
and semiarid regions at both local and global scales. They are important biodiversity
components, provide critical ecosystem services, and strongly influence soil-plant
relationships, and successional trajectories via facilitative, competitive, and edaphic
engineering effects. Despite these important ecological roles, very little is known about
biocrusts in seasonally dry tropical forests. Here we present a first baseline study on
biocrust cover and ecosystem service provision in a human-modified landscape of
the Brazilian Caatinga, South America’s largest tropical dry forest. More specifically,
we explored (1) across a network of 34 0.1 ha permanent plots the impact of
disturbance, soil, precipitation, and vegetation-related parameters on biocrust cover
in different stages of forest regeneration, and (2) the effect of disturbance on species
composition, growth and soil organic carbon sequestration comparing early and late
successional communities in two case study sites at opposite ends of the disturbance
gradient. Our findings revealed that biocrusts are a conspicuous component of the
Caatinga ecosystem with at least 50 different taxa of cyanobacteria, algae, lichens
and bryophytes (cyanobacteria and bryophytes dominating) covering nearly 10% of the
total land surface and doubling soil organic carbon content relative to bare topsoil.
High litter cover, high disturbance by goats, and low soil compaction were the leading
drivers for reduced biocrust cover, while precipitation was not associated Second-growth
forests supported anequally spaced biocrust cover, while in old-growth-forests biocrust
cover was patchy. Disturbance reduced biocrust growth by two thirds and carbon
sequestration by half. In synthesis, biocrusts increase soil organic carbon (SOC) in dry
forests and as they double the SOC content in disturbed areas, may be capable of
counterbalancing disturbance-induced soil degradation in this ecosystem. As they fix and
fertilize depauperated soils, they may play a substantial role in vegetation regeneration
in the human-modified Caatinga, and may have an extended ecological role due to the
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Caatinga Biocrust Distribution and Services
ever-increasing human encroachment on natural landscapes. Even though biocrusts
benefit from human presence in dry forests, high levels of anthropogenic disturbance
could threaten biocrust-provided ecosystem services, and call for further, in-depth
studies to elucidate the underlying mechanisms.
Keywords: biological soil crusts, Caatinga, dry forest, exotic goats, human disturbances, soil organic carbon
INTRODUCTION
Overall, biocrusts are composed of mainly slow-growing
organisms highly sensitive to their close environment, including
soil attributes, microclimatic conditions, and vascular plant
communities. In addition to a potential competition for
water, nutrients and light, vascular plants provide shaded
habitats, and cause litter deposition on biocrusts, what has
been considered a negative effect on biocrust colonization,
performance and development toward late successional stages
(Boeken and Orenstein, 2001; Berkeley et al., 2005). Biocrusts
are also sensitive to human disturbances such as trampling by
livestock (Condon and Pyke, 2018), soil degradation (Belnap
and Gillette, 1998) and invasion by vascular plants (Belnap
et al., 2006). Disturbed biocrusts usually experience changes
in their physiological performance, taxonomic and ecological
composition (Concostrina-Zubiri et al., 2014; Mallen-Cooper
et al., 2018), which often represents a retrogressive succession
from late (abundant lichens and bryophytes) to early successional
stages (only cyanobacteria). As biocrust-mediated processes and
services depend on the successional stage, human impacts can
deplete them (Belnap, 1995, 2006). To provide an example,
trampling by livestock can deteriorate biocrusts, causing soil
degradation and a cascade of effects such as increased wind
erodibility (Belnap et al., 2007), loss of key ecosystem processes
like water infiltration (Chamizo et al., 2016), or favoring exotic
plant invasion (Eldridge et al., 2010). In synthesis a myriad
of interconnected variables drive biocrust spatial organization,
performance, diversity, successional dynamics, and related
services and impacts.
Research about the presence of biocrusts, their taxonomic
composition and functional role in different habitats as
well as their susceptibility to disturbance have initially been
concentrated in arid and semiarid regions (Belnap et al., 2001).
In most situations, there is a clear climatic limitation to vascular
plants, implying that the relationships between biocrust and
vascular plants can’t be properly assigned as well as the role
played by biocrusts on successional trajectories or vegetation
dynamics beyond biocrust succession itself (Duane Allen, 2010).
In fact, little attention has been devoted to tropical ecosystem
dominated by vascular plants, such as dry forests, where
according to theory and the state of research, biocrusts are not
expected to be either abundant or ecologically relevant (Belnap
et al., 2001; Maestre and Cortina, 2002; Seitz et al., 2017). To the
best of our knowledge, there are only two studies on biocrusts
in dry tropical forests (Maya and López-Cortés, 2002; Büdel
et al., 2009) and apparently South America has been entirely
overlooked in the context of biocrust research (Büdel et al.,
2016). This scientific negligence may be partly due to the relative
recency of global change phenomena. In fact, most of the tropical
Biological soil crusts (hereafter referred to as “biocrusts”)
are communities consisting of photosynthetic (i.e.,
cyanobacteria, eukaryotic algae, lichens, and bryophytes)
and non-photosynthetic organisms, such as heterotrophic
bacteria and microfungi (Chamizo et al., 2013), covering
around 12% of the Earth’s terrestrial surface (RodriguezCaballero et al., 2018). As light dependent associations,
they colonize the topsoil layer, where they aggregate soil
particles via organic exudates and filamentous structures
(Belnap and Büdel, 2016). While biocrusts cover a wide
range of latitudes, from tropical to temperate and polar
ecosystems (Belnap et al., 2001), they are particularly
abundant across arid and semiarid regions, where vascular
plants are not able to outcompete them (Belnap and
Lange, 2013). Across suitable habitats, they can cover
up to 100% of the terrestrial surface throughout the year
(Kleiner and Harper, 1972).
Biocrusts have been identified as a key ecological component
across many arid and semi-arid regions regarding biodiversity,
ecosystem functions.They promote both primary and secondary
succession and drive many ecological processes associated
to early communities, such as biogenic weathering, soil
development, nutrient uptake, and water balance (Belnap, 2001a;
Chamizo et al., 2016). In bare soil spots, biocrusts follow a
successional process initiated by cyanobacteria and algae, which
favor the subsequent establishment of lichens and bryophytes
(Belnap, 1995, 2001a). In this perspective biocrusts can facilitate,
inhibit or have neutral effects on succession in vascular plant
communities (Zhang et al., 2016), thus acting as ecosystem
engineers. Biocrusts have been proposed to affect nutrient
availability for vascular plants by fixing considerable amounts
of nitrogen and carbon, enhancing phosphorous availability and
reducing nutrient leaching through soil profiles (Elbert et al.,
2012; Barger et al., 2016; Sancho et al., 2016). Due to their
carbon and nitrogen fixing abilities, biocrusts have been found
to be major players of the global nitrogen cycle and also affect
the global carbon cycle (Elbert et al., 2012). Moreover, biocrusts
improve soil aggregation, stability and porosity (Belnap, 2006;
Castillo-Monroy et al., 2011) largely influencing soil attributes,
such as moisture, hydrology and susceptibility to erosion (Bu
et al., 2015; Belnap and Büdel, 2016). In addition to soil
conditions and nutrient budgets, these organisms can directly
affect seed germination of vascular plants, either positively
or negatively, indicating that biocrust-mediated processes have
relevance beyond simple soil development (Deines et al., 2007;
Song et al., 2017).
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forest landscape is moving toward human-modified landscapes,
usually represented by the establishment of land-use mosaics
including active and old crop fields, pasture lands and patches
of native forests (Tabarelli et al., 2010). This is particularly
true in the Caatinga dry forest of northeast Brazil, the largest
and one of the most species-rich seasonally dry tropical forests
worldwide (Silva et al., 2017). Slash-and-burn agriculture and
free-ranging goat/cattle has transformed the old-growth forest
into a temporally dynamic mosaic consisting of old fields (i.e.,
abandoned crop or pasture fields), regenerating forest patches
of varying ages and remaining old-growth forest patches at the
landscape spatial scale (Tabarelli et al., 2017). This dynamic
mosaic probably offers at least temporal windows of opportunity
for biocrusts (i.e., open or sun-exposed habitats) with their spatial
and ecological organization and potential impacts and services
largely mediated by livestock and land use dynamics.
The effects of biocrust diversity and structure on dry tropical
forests remains unstudied, especially with respect to ecosystem
service provision, as for example carbon sequestration and soil
fertilization. Soil organic carbon (SOC) accumulation can be
considered an especially important ecosystem service for the
naturally poor soils of the Caatinga (Tiessen et al., 1998). SOC
is connected to numerous ecosystem functions upon which
humans depend in the Caatinga, so that changes will have
immediate consequences for the local population (Thomas,
2012). As in other drylands, SOC in the Caatinga is concentrated
in the uppermost centimeters (Schulz et al., 2016) and therefore
very sensitive to disturbance (Althoff et al., 2018). As this
corresponds with the biocrust stratum, their presence might have
a great impact. In drylands and areas at the stage of primary
succession, such as in the Caatinga after land abandonment,
SOC sequestration is mediated mainly by biocrusts (Lange, 2001;
Thomas et al., 2011; Thomas, 2012). Possible positive effects of
soil fertilization by biocrusts could be lost in the future, as the
Caatinga is highly threatened by climate change and land use and
land-use-driven reductions in SOC stocks have been reported
for biocrusts (Thomas et al., 2011). The Caatinga is poorly
understood in terms of biogeochemical cycling in general (Moura
et al., 2016; Althoff et al., 2018) but more so for biocrust influence.
Nonetheless, because of its size it may play an important role
in global nutrient cycles and could act as a potential sink for
atmospheric CO2.
The climate of dry forests in general should offer a suitable
habitat for biocrusts (Rodriguez-Caballero et al., 2018), but have
never been investigated for their presence or ecosystem services
there. As has been known from studies worldwide, biocrusts
can provide essential ecosystem services and are responsible for
ecosystem integrity in many different habitats. Therefore, we
aimed to investigate if biocrusts are an abundant component
of dry forests and if they provide ecosystem services essential
to the survival of a dry forest under human pressure, using
the Caatinga as an exemplary forest biome. Here we present
a baseline study on the occurrence, diversity, and ecological
role of biocrusts inhabiting a human-modified landscape of the
Caatinga dry forest in northeast Brazil. Biocrusts and drivers
of biocrust organization at landscape scale were systematically
recorded across a network of 34 permanent plots covering a
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wide range of land use from regenerating forest stands following
slash-and-burn agriculture to old-growth forest patches. We
expected that (1) biocrust cover, (2) taxonomic composition
and (3) successional stage of biocrusts will be affected by forest
successional stage (regenerating vs. old growth), litter cover (as a
proxy of competition with vascular plants for light), precipitation
patterns, goat trails/feces, and soil compaction Additionally, we
investigate the impact of human disturbance and variable annual
rainfall patterns on the ecosystem service of carbon sequestration
and biocrust growth. We expected that human disturbance would
severely limit the ability of biocrusts to capture/ store carbon
by changing the species composition of the biocrust and their
growth- We also expected that the reduction of SOC in biocrusts,
induced by multiple low rain years could be canceled out by
a single strong precipitation year. We highlight the unexpected
diversity supported by biocrusts and the complex relationships
between biocrusts and human disturbances, particularly how
biocrusts can benefit from, but also potentially affect forest
resistance and resilience across human-modified landscapes.
MATERIALS AND METHODS
Study Area
This study was carried out in the Catimbau National Park,
a human-modified landscape of the Caatinga dry forest
in northeast Brazil, with a predominance of Cactacea,
Euphorbiaceae, and Fabaceae (Rito et al., 2017). The 607km² landscape consists of a vegetation mosaic, resulting from
the presence of small farmers devoted to slash-and-burn
agriculture and livestock grazing (Tabarelli et al., 2017). Active
and abandoned crop fields, second-growth forest patches of
varying ages, and old-growth forests prevail. All vegetation
types are exposed to chronic anthropogenic disturbance through
firewood and forage collection, timber exploitation and livestock
browsing (Arnan et al., 2018; Souza et al., 2019). Canopy cover
never achieves 80–90% (M. Tabarelli personal information and
Figure 1A). Soil is composed of sedimentary, deep lithosols
with quartz sands, with the presence of sandstone outcrops;
soils are naturally unfertile with pH around 4.5 (SNE, 2002).
The regional climate is semi-arid (<0.65 precipitation/ potential
evapotranspiration) with an annual temperature of 23◦ C
(Sampaio, 1995). In Catimbau, annual rainfall varies between
480 and 1,100 mm across the landscape, with rain concentrated
between March and July (water deficit between August and
February; SNE, 2002) and high spatial and temporal variations,
including droughts lasting more than a year (Sampaio, 1995;
Rito et al., 2017).
Human Disturbance and Biocrust Spatial
Organization
To investigate the spatial distribution and organization of
biocrusts at the landscape level we adopted a sampling design
based on 34 × 0.1 m²-permanent plots as follows: 19 oldgrowth forest plots and 15 secondary growth forest stands with
stands ranging from 5 to 70 years after land abandonment; i.e.,
regenerating stands of varying ages and vegetation structure from
almost bare-soil plots up to well-developed forest achieving over
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FIGURE 1 | Biocrusts of the Caatinga dry forest in the Catimbau National Park, northeastern Brazil. Overview of the canopy openness in old-growth forests with
agricultural farmlands in the background (photo courtesy of Jens Brauneck, University of Kaiserslautern) (A). Trampling paths of goats left in the otherwise closed
(Continued)
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FIGURE 1 | biocrust cover (B) as well as association of biocrusts with vascular plants (C); shrubs marked with a red arrow Croton argyrophylloides (B) and shrubs
marked with a white arrow Jatropha mutabilis (C). In both images the crusts are dominated by dark cyanobacteria (Nostoc spp., Scytonema sp. and Microcoleus
vaginatus) demarcated with black triangles. Light microscopic images of cyanobacteria and green algae isolates (F–J), as well as lichen species [in situ, (D,E); white
bar represents 500 µm], new to biocrusts of South America and found in Catimbau National Park. Heppia conchiloba (D), Bibbya cf. albomarginata (E),
Scenedesmus sp. (F), Follicularia sp. (G), Cylindrocystis brebissonii (H), Scotelliopsis cf. rubescens (I), Macrochaete lichenoides (J).
120 Mg ha−1 of aboveground biomass (Souza et al., 2019). Plots
also covered a gradient of precipitation (510–940 mm of annual
rainfall) and of chronic human disturbance, particularly firewood
collection and livestock browsing as detailed by Arnan et al.
(2018) and Rito et al. (2017). We thus considered to have included
a considerable habitat variation resulting from the old-growth
forest encroachment by small farmers; i.e., a typical Caatinga
human-modified landscape (Tabarelli et al., 2017). The 34 plots
were sampled three times during a 12-mo period (August 2017 to
July 2018), with plots being regularly sampled every 4 months.
Plots were sampled by adopting a square grid sizing 0.5
× 0.5 m (0.25 m²) made of PVC tubes, subdivided with
string into twenty-five cells of 0.1 × 0.1 m (0.1 m²). The
grid was disposed on the ground every 10 m, along two 50
m-transects, summing up 10 grids per plot. Each plot was
sampled three times during 1 year, with transects disposed at
different spots inside the plot every sampling period. It resulted
in a total of 1,020 grids; i.e., 34 plots sampled via 10 grids
each of the three sampling periods. As grid-based variables we
adopted: (1) biocrust cover, (2) cover by herbs and seedlings
up to 50 cm tall, (3) ground litter biomass (kg ha-1), (4) goat
dung pellets, (5) goat trail cover, and (6) soil penetrability.
Biocrust cover was quantified using the point intercept method
(Levy and Madden, 1933) adopting three succession-related
categories: (a) cyanobacterial biocrust, (b) lichen biocrust, and
(c) bryophyte biocrust. Biocrust cover divided into functional
groups has long been implemented as a basic variable in biocrust
ecology research (Eldridge and Rosentreter, 1999). The pointintercept method was also adopted to estimate plant and goat
trail cover. Soil compaction was measured by a penetrometer
produced with a sharp steel bar 1.5 m tall, which was thrown
into a 32 mm PVC tube (1.5 m long) against the ground
(Passos and Oliveira, 2004). Vascular plant cover, trampling by
livestock and soil texture/consistency have been identified as
key drivers of biocrust performance and occurrence (Belnap
and Gillette, 1998; Condon and Pyke, 2018). In this context,
forest successional stage (old-growth vs. regenerating stands),
cover by herbs, and the amount of ground litter were considered
as proxies of total vascular plant cover, while dung and trails
by goats as proxy of disturbance. Additionally, mean annual
precipitation amount per plot, calculated by WordClim data, was
investigated, because water availability is an important driver
for biocrust occurrence and succession (Belnap et al., 2006). To
investigate the effect of successional stage of the vegetation on
biocrust distribution further, for each plot frequency of biocrust
occurrence was calculated based on all 30 grids per plot. The
available environment for the occurrence of biocrusts presented
great physical and biological heterogeneity. Across the 34 plots,
ground litter ranged from 29.1 kg ha-1 to 524.7 kg ha−1 (195.4
± 120.3), the coverage by goat trails between 0 and 88.3%
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(39, 6 ± 21.5), soil compaction (penetrability) between 3.8 and
17.7 cm (10.7 ± 2.8), the amount of feces between 0.0 and 48
pellets/m²(16 ± 14.4), herb cover between 0.0 and 54.5% (8.7 ±
12.1), and precipitation ranging from 510 to 940 mm (748 ± 145).
Finally, biocrust cover was also estimated via point-intercept
grids into a network of long-standing goat trails crossing a
degraded pasture field established after clearing a large patch of
old-growth forest. This pasture field supported immense biocrust
patches of Nostoc spp., Scytonema sp. and Microcoleus vaginatus
(pers. obs. BB and MS), which were closely associated to small
shrubs such as Croton argyrophylloides and Jatropha mutabilis.
(Euphorbiaceae) (Figures 1B,C). We randomly selected 30
sampling points along a total of 100 m of goat trails (i.e., trail
grids), at least 10 m apart from each other. Paired control grids
were placed next to the trail grids (5 m at maximum) but clearly
apart from goat trail influences. Point intercept measurements
were carried out once in the beginning of the 2017-dry season.
Taxonomic Identification and Microscopy
In order to obtain a basic and rather qualitative understanding
of the natural species richness of biocrusts occurring in the
Catimbau landscape, including taxonomic and ecological groups,
two non-systematic surveys were carried out, outside the 34
0.1 ha plots. First, biocrusts were actively searched in 10 sites,
covering a wide range of habitat types representing different
successional stages and degrees of disturbance, from abandoned
crop and pastures to old-growth forest patches. The sites were
chosen as distinctly differing successional stages and under
different disturbance regimes, to represent the mosaic-like
structure of the Caatinga vegetation. A basic understanding
of biocrust presence in the Caatinga was gained and found
species were taxonomically assigned. Samples were collected
haphazardly by pressing inverted petri dishes (ø 10 cm) into the
biocrust and carefully detaching it from the soil matrix with the
aid of a spatula. At the field site, biocrusts were identified to
the lowest taxon possible using a 10 x magnifying glass, and a
light microscope (400 x). Second, biocrusts of two study sites
representing the extremes of the disturbance gradient (see soil
organic carbon measurements) were identified, using a culturing
approach following (Jung et al., 2018) for three samples at
both sites. For each sample, 250 mg of biocrust material was
randomly picked from a natural sample (one petri dish) and
incubated in 15 ml liquid Bold’s Basal Medium with soil extract
(BBM; Bischoff, 1963) overnight. The samples were being shaken
and allowed to settle for 30 s, to remove floating particles. The
supernatant was then added to 15 ml BBM. This was repeated
three times, resulting in 45 ml sample in BBM medium. After
centrifugation for 5 min at 1,000 rpm, the supernatant was
decanted and the pellet resuspended in 250 ml of double-distilled
water, from which the samples were transferred to solidified
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mixed with a scoop tip of CaCO3 , covered in DMSO, and heated
in a water bath at 65◦ C for 45 min twice. After centrifugation
at 2000 rcf for 10 min, the optical density (OD) of each sample
was measured with a spectrophotometer (UV/Vis Spectrometer
LAMBDA 35, Perking Elmer Inc. Waltham, MA, USA) at two
wavelengths: 700 and 665 nm. Chlorophyll content was then
calculated for each sample with the following equation (Arnon,
1949): Chlorophyll a (µg) = [(OD665 ∗ OD700 ) ∗ 12.19] ∗ mL
DMSO, where OD700 is the unspecific absorption and OD665 the
absorption peak for chlorophyll a.
SOC content was determined by the loss on ignition method
(LOI) described by Black (1965). Samples were prepared
following the protocol of Throop et al. (2012), by sieving them
through a 2 mm sieve to exclude stones, passing other aggregates
through the sieve, and discarding the skeletal fraction. About 10 g
were ground finely in an oscillating mill for subsequent ignition
at 550◦ C for 2 h. SOC stock was calculated according to Schulz
et al. (2016) to provide results comparable to those of other
surveys: SOC stock [g cm−2 ] = bulk density [g cm−3 ] ∗ SOC
content [g kg−1 ] ∗ depth [cm].
BBM with soil extract, with two replicates for each sample. The
cultures were kept in a culture cabinet at standard conditions
used in our lab (15–17◦ C, light-dark cycle of 16:8 h, light intensity
of ca. 20–50 µmol photons m−2 s−1 ). The cyanobacterial and
green algal colonies were examined with a light microscope
(Axioskop, Carl Zeiss, Jena, Germany, 630 x) operated with Zeiss
Axiovision software after 5, 12, and 17 weeks. The organisms
from the cultures and field samples (also including bryophytes
and lichens, were determined with taxonomic keys (e.g., Ettl
and Gärtner, 1996; Komárek and Anagnostidis, 1998, 2005), as
well as own (B. Büdel) and external expert knowledge (K.C.
Pôrto, UFPE).
Soil Organic Carbon Sequestration and
Biomass Increase
For this investigation, we chose two case study sites representing
contrasting successional stages of biocrust communities along the
disturbance gradient of the Catimbau National Park (referred
to henceforth as “Early site” and “Late site”). While the Early
site is an actively managed Cashew plantation (3.96 ha in
size), the Late site (2.64 ha) represents former agricultural
land, mainly pasture, on which a young secondary forest
with shrub vegetation developed following abandonment ca. 40
years ago (details see Table S1). Both sites were investigated
for biomass increase and carbon sequestration before the
rainy seasons of the years 2017 and 2018. Since the biomass
increment of biocrusts of a given year should primarily reflect
growth conditions of the previous years, the status of the
2017 biocrust represents 2016, which was a drought year,
while 2018 represents 2017, which was an unusually wet
year (see Table S2). Biocrust coverage was studied in March
2017 only.
To explore the impact of biocrusts on SOC and assess
their biomass contribution, bare soil (n = 16) and biocrust
(n = 45) samples were collected from random biocrust and
control patches of differing size (biocrusts: 0.0035–1.2462 m²;
control: 0.0067–0.5519 m²), in both study sites for both years.
Distance between the patches and between the controls was
always >5 m. For each patch a cylinder of 1 cm depth, which
is adequate for biocrusts (Maestre et al., 2013), and 2.5 cm
diameter was pushed into the biocrust 7 times and thereafter
mixed, to extract enough material for the analyses. The biocrust
samples were covered 100% by cyanobacterial biocrusts in
both sites; bryophyte and/or lichen presence was avoided to
ensure sample homogeneity. Cyanobacterial biocrusts are of
key interest, as they are the most dominant group at both
sites and throughout the whole national park (Figure 2B). In
the laboratory, the samples were separated into two fractions,
one for quantifying biomass and growth using the amount
of chlorophyll a as biomass proxy for autotrophic biocrusts
(e.g., Johnson et al., 2012), the other for soil organic carbon
(SOC) measurements.
To assess biocrust biomass and, hence, growth between 2017
and 2018 for both case study sites, chlorophyll a was extracted
with dimethyl sulfoxide (DMSO; Ronen and Galun, 1984) and
determined spectrophotometrically. For this, each sample was
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Data Analysis
For the assessment of biocrust cover in 34 plots across the
park landscape, the point-intercept data from three sampling
campaigns were collapsed into a single sample per plot (i.e.,
30 grids per plot). Accordingly, the number of recorded
cells containing biocrusts, goat trails or vascular plants was
transformed into a percentage of the total cells evaluated in
the plot (i.e., 30 grids vs. 25 cells per grid per plot). The
data were successfully tested for normal gaussian distribution
and homogeneity of variance prior to statistical analyses.
Pearson’s correlation coefficient was used to test potential
relationships among explanatory variables and because of that
we finally adopted: goat trail cover (%), fine litter biomass (kg
ha−1 ), soil compaction (penetrability in cm) and precipitation
gradient (mm). Generalized linear mixed models (GLMM) were
performed to examine potential effects of these variables plus
forest successional stage (old-growth vs. regenerating stands) on
cover of: (1) total biocrust, (2) cyanobacterial crust, (3) lichen-,
and (4) bryophyte-dominated biocrust, with plot as the random
factor and LME as the estimation method. All analyzes were
performed in the R 3.0.0 programming language environment
using the packages nlme, stats, mlmRev, lme4, gplots, psych
and Rcmdr. Additionally, the difference in biocrust frequency
between the two vegetation successional stages was investigated
with a global χ² test, followed by a pairwise post hoc test. The
p-value was adjusted by Bonferoni correction. The analysis was
performed using Statistica (Statistica, version 10, StatSoft, Inc.,
Palo Alto, CA, USA).
For the differences in biocrust-related biomass increase
and SOC sequestration at the two case study sites, a multifactorial ANOVA was used, with site (succession), study year
(precipitation) and bare soil vs. biocrust (biocrust effect) as
explanatory variables. The data were normally distributed and
homogenous in variance. The analysis was also performed
using Statistica.
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FIGURE 2 | Coverage and frequency of biocrust communities in the Catimbau National Park, northeastern Brazil. Map representing vegetation density (generated with
rapideye bands reflectance by Davi Jamelli, Federal University of Pernambuco) and average cover of biocrusts inside the 34 permanent plots (A). Difference in mean
biocrust coverage (± SD) between two successional stages of vegetation (old-growth forest n = 19; regeneration forest n = 15), separated into functional groups of
biocrusts (B). Proportion of plots with low (<10%), intermediate (10–30%) and high (>30%) frequency of biocrust occurrence in the two forest successional stages
(C). Frequencies generally differed between old-growth and regeneration forest (global χ² = 9.55, df = 2, p = 0.008); for pairwise test results see text. Significant
differences between old growth and second growth forest are denoted with different letters above the bars following a pair wise chi-square post hoc test (p < 0.05).
RESULTS
taxa), green algae (nine taxa), lichens (seven taxa) and bryophytes
(four taxa). The cyanobacteria Nostoc spp., Scytonema sp., the
liverworts Riccia sp. 1 and sp. 2, and the moss Bryum exile
were the most frequent taxa. While the number of cyanobacteria,
bryophytes and green algae species was similar under contrasting
rainfall and disturbance intensities, more lichen species occurred
in wetter areas (Table 1).
At the plot spatial scale (n = 34), biocrusts of all three
successional stages were recorded throughout the year, although
in six plots (17.6%), no biocrust was recorded during the three
sampling campaigns (Figure 2A). However, most of the plots
In total, our biocrust surveys including the active search across
10 sites, random sampling in all 34 permanent plots, and the
culturing approach using samples from the two case study sites,
resulted in 50 biocrust taxa throughout Catimbau National Park.
More precisely, 19 biocrust organisms were identified to the
species level, 33 to the genus, and one taxon to the family. A
total of 23 taxa have not been reported yet for South America,
and hence the Caatinga in the context of biocrust research
(Table 1 and Figures 2D–J). They include cyanobacteria (three
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TABLE 1 | Biocrust taxa found in the National Park Catimbau, northeastern Brazil, roughly assigned to their occurrence in high and low precipitation and disturbance
regimes.
Species
High rainfall
(>748 mm)
Low rainfall
(≤748 mm)
High
disturbance
Low
disturbance
Cyanobacteria
Aphanocapsa sp.
Calothrix sp.
Chroococcidiopsis sp.
Gloeocapsa sp.
Leptolyngbya sp.
Macrochaete lichenoides
Microcoleus vaginatus
Nostoc edaphicum
Nostoc ellipsoides
Nostoc sp. 1
Nostoc sp. 2
Oscillatoria sp.
Pseudophormidium sp.
Schizothrix sp.
Scytonema hyalinum
Scytonema sp. 1
Stigonema sp.
Tolypothrix sp.
Green algae
Chlorella sp.
Cylindrocystis brebissonii
Desmococcus sp.
Follicularia sp.
Heterococcus sp.
Klebsormidium sp.
Macrochloris multinucleata
Neochloris sp.
Scenedesmus sp.
Scotiellopsis rubescens
Spongiochloris sp.
Stichococcus sp.
Trebouxiophyceae
Green algae sp. 1
Green algae sp. 2
Green algae sp. 3
Green algae sp. 4
Mosses
Bryum argenteum
Bryum exile
Campylopus pilifer
Fissidens submarginata
Tortela humilis
Liverworts
Riccia sp. 1
Riccia sp. 2
Riccia vtialii
(Continued)
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TABLE 1 | Continued
Species
High rainfall
(>748 mm)
Low rainfall
(≤748 mm)
High
disturbance
Low
disturbance
Lichens
Buellia sp.
Cladonia foliacea
Cladonia verticillaris
Heppia conchiloba.
Lecidea sp.
Peltula michoacanensis
Bibbya cf. albomarginata
Precipitation is categorized as high if the plot a species has occurred in has a higher mean annual rainfall than the mean annual rainfall across all investigated plots (748 mm). Disturbance
is categorized according to Arnan et al. (2018), where plots with chronic anthropogenic disturbance values (GMDI) higher than 34 (mean of all plots) were considered highly disturbed,
and below or equal to 34 as low disturbed sites. Morphospecies were assigned as sp. 1 – 4 through comparison of the cell sizes of 50 cells and 20 heterocytes, if present in the
species. Species that have not yet been registered for biocrusts in South America are marked in red. Gray color indicates that the species has been found in the respective category of
disturbance or precipitation regime.
degraded pastures reached 23.0 ± 2.6% of the soil surface covered
by biocrusts [t (30) = 13.5, df = 39.50, p < 0.0001].
SOC content in bare soil (control) was equal for both
case study sites (Tukey posthoc: p2017 = 0.58; p2018 = 0.56).
Therefore, site differences between biocrusts are solely due to
the successional status of the biocrust communities themselves
[F succession(1, 236) = 71.1, p = 0.000]. SOC content roughly
doubled in biocrusted soils compared to bare ground (from
6.04 and 8.70 g kg−1 to 10.67 and 19.82 g kg−1 , respectively for
Early and Late site) [F biocrust effect(1, 236) = 145.55, p = 0.000],
independent of site and precipitation. Likewise, SOC doubled
in late as compared to early successional biocrusts (10.67 to
19.82 g kg−1 ) (Tukey posthoc: p2017 = 0.000; p2018 = 0.000;
Figure 4A). Precipitation did not show any effect on SOC,
neither in biocrusts nor in control soils [F precipitation(1, 236) =
0.037, p = 0.85, Figure 4A].
Likewise, the control soils of both case study sites had
similar Chlorophyll a concentration as a proxy of biomass of
autotrophic biocrusts (Tukey posthoc: p2017 = 1.000; p2018 =
0.999), so that differences are a result of biocrust successional
status [F succession(1, 236) = 11.3, p = 0.001]. In the wet year, the
presence of biocrusts increased the chlorophyll a content of top
soil layers by more than 1,500-fold (from 0.0036 to 5.85 mg m−2 )
in the early successional crusts and 12-fold (from 1.25 to 15.82 mg
m−2 ) in late successional biocrusts (Tukey posthoc: pearly = 0.04;
plate = 0.000; Figure 4B) compared to bare soil. Biocrust presence
in general showed a pronounced increase of chlorophyll a content
in the soil [F biocrust effect(1, 236) =37.4, p = 0.000]. Precipitation
had a strong effect on biocrust growth across the study years:
From the drought year 2017 to the wet year 2018, chlorophyll a
increased 7 times at the Early site (from 0.71 to 5.85 mg m−2 )
and 6.5 times (from 2.12 to 15.85 mg m−2 ) at the Late site
[F precipitation(1, 236) =27.9, p = 0.000].
(44.4% of 27 plots with biocrusts recorded) supported only
cyanobacteria biocrusts (i.e., initial biocrusts), particularly those
dominated by Scytonema sp. Only 7.4% of plots exhibited lichen
biocrusts, particularly Bibbya cf. albomarginata (intermediate
successional biocrusts), while 48.2% had bryophytes recorded;
i.e., late biocrusts with mosses and liverworts. Total plot cover of
biocrusts ranged from 0 to 54.4% (8.1 ± 13.6; mean ± standard
deviation) with no difference between successional stages of the
vegetation [t (34) = −0.146, p = 0.885] (Figure 2B). Frequency
of biocrust coverage however, did show a difference between
the two successional stages of the forest. Regenerating forest
supported more plots with moderate biocrust frequency between
10 and 30% (χ² (1; N = 11) = 9.38, p = 0.002]. On the
other hand, more patches of low biocrust frequency (<10%)
where found in old-growth forest [χ² (1; N = 17) = 5.85, p =
0.016] (Figure 2C). Plots with high crust frequency (>30%) were
seldomly and evenly encountered across forest successional types
[χ² (1; N = 6) = 0.34, p = 0.56]. Considering only the 27 plots
in which biocrusts occurred, cover by cyanobacterial biocrusts
(initial) ranged from 0.13 to 53.1% (7.5 ± 11.5), lichen biocrust
(intermediate) between 0.26 and 1.8% (1.24 ± 0.6) and bryophyte
biocrust (late) between 0.11 and 9.3% (3.8 ± 3.2).
Across plots, biocrust cover decreased with (1) greater
coverage of goat trails, (2) higher fine litter biomass, and (3)
higher soil penetrability (Table 2, Figures 3A–C), while other
factors such as precipitation, herb cover, or feces showed no
effects. The cyanobacteria biocrust responded negatively to
litter (Figures 3D–F, Table 2), while no significant relationship
was found between the coverage by lichen biocrusts and
the explanatory variables (Figures 3G–I, Table 2). Bryophyte
biocrusts negatively responded only to goat trails (Figures 3J–L,
Table 2), but positively to soil compaction. The successional
stage of the vegetation (regenerating vs. old-growth forest) did
not directly affect biocrust coverage, but its interaction with the
soil compaction affected both the total cover of biocrusts and
the cover of bryophytes, this interaction being stronger across
old-growth forests (Table 2). Finally, long-standing goat trails
supported only 6.3 ± 6.1% of biocrust cover, while spots of
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DISCUSSION
Our results suggest that human-modified landscapes of the
Caatinga dry forest can support biocrust communities at different
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0.90
successional stages, with high taxonomic and ecological diversity.
Biocrusts composed of at least 50 taxonomic groups occurred
across numerous habitats—from abandoned farmlands to oldgrowth forests, although there was a predominance of initial
biocrusts dominated by cyanobacteria. Bryophytes were the
second most abundant group, while lichens were almost absent,
although being the typically intermediate stage of succession in
hot arid/semi-arid areas. Biocrusts covered a significant fraction
of the soil surface (8.1 ± 13.64 %; mean ± standard deviation
of the biocrusts in the Catimbau National Park) throughout the
year, with more than 50% coverage of cyanobacterial biocrusts
in some areas. Biocrust communities benefited from reduced
ground litter and little goat pressure, while forest successional
stage and precipitation amount per se had no effect. They
were potent carbon sequestering agents of dry forests and
due to this fertilization effect could play a substantial role
in forest regeneration. However, high levels of anthropogenic
disturbance lead to a pronounced decrease in biocrust growth
and SOC sequestration.
1.30
VSS *SC
5.89
0.02
0.24
0.35
0.88
1.30
VSS
0.75
Significant effects are in bold (P < 0.05); DF, degree of freedom; F, effect value; R2m, squared R marginal; R2c , squared R conditional.
0.56
1.30
VSS*GT
0.33
0.76
0.09
1.30
VSS
0.35
0.01
6.11
0.87
1.30
1.30
VSS*GT
Goat trail
Bryophyte crust coverage (%)
0.88
0.02
1.30
VSS
Conventionally, biocrusts are known to predominate in
landscapes with little cover by vascular plants (i.e., arid and
semi-arid regions dominated by sparse shrubs) and reduced
human disturbances (Belnap et al., 2016; Ayuso et al., 2017).
Our findings suggest that even in forest biotas, biocrusts can be
ecologically/taxonomically diverse and abundant, particularly
in the case of rural populations creating vegetation mosaics.
Although comparisons across studies are difficult due to
differences in sampling effort and geographic scale, the presence
of 33 genera only in the Catimbau National Park suggests
that the Caatinga supports a relatively diverse community at
landscape scale. As an example, in Australia 86 genera were
recorded considering 83 sites (Thompson et al., 2006) and
more than 60 taxa were found across seven ecosystems in
Africa (Büdel et al., 2009). Most taxa found exhibit a broad
geographical distribution, occurring with high abundance
across deserts and semi-deserts, e.g. Bryum (moss; e.g., Kidron
et al., 2002), Riccia (liverwort; e.g., Eldridge and Tozer, 1996),
Heppia (lichen, e.g., McCune and Rosentreter, 1995), Scytonema,
Microcoleus and Nostoc (cyanobacteria; see Büdel et al., 2016),
and Chlorella (green algae; e.g., Rosentreter and Belnap, 2001).
The list of biocrust species was expanded by 23 taxa that
have not yet been registered as biocrust members for the
Caatinga, Brazil or South America and included cyanobacteria
(e.g., Macrochaete lichenoides; Figure 1J), green algae (e.g.,
Cylindrocystis brebissonii; Figure 1H), lichens (e.g., Heppia
conchiloba; Figure 1D) and mosses (e.g., Fissidens submarginata).
The dominant functional group of biocrusts in the study
landscape, independent of forest successional stage, was
cyanobacteria and, occasionally, green algae, making up 79.3 %
of the biocrust-covered area. Cyanobacteria belong to the first
colonizers of open soils and throughout the whole succession
of a biocrust, are an important component of it (Weber et al.,
2016). Both forest systems supporting mainly this biocrust type
suggests that the development of later successional stages might
be suppressed by irregular rainfall, vascular plant presence or
0.75
1.30
VSS*Litter
0.50
0.50
1.30
0.89
VSS
0.26
0.05
3.41
1.29
1.30
1.30
Soil comp.
0.88
0.53
0.92
0.01
0.40
1.30
1.30
VSS*Litter
Biocrust Composition and Diversity
0.19
0.02
0.35
0.58
0.31
0.88
1.30
1.30
VSS*GT
Goat trail
Lichen crust coverage (%)
0.76
0.09
1.30
VSS
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Litter
VSS
1.30
0.00
0.95
0.02
VSS *SC
0.12
0.97
0.00
1.30
VSS
0.78
2.43
1.30
1.30
Soil comp.
0.87
0.65
0.89
0.01
0.20
1.30
1.30
VSS*Litter
0.88
Litter
VSS
1.30
0.44
0.50
0.00
VSS *SC
0.38
0.05
0.88
0.89
0.22
0.58
0.46
0.54
1.30
VSS
1.55
0.29
1.30
1.30
VSS *SC
0.89
0.02
0.23
1.47
5.43
1.30
1.30
VSS*Litter
0.89
0.11
0.11
0.07
3.29
2.68
1.30
1.30
VSS*GT
Goat trail
Cyanobacteria crust coverage (%)
0.40
1.30
SSV
0.70
0.14
Litter
VSS
1.30
1.24
0.27
0.15
Soil comp.
0.007
0.15
2.09
1.30
VSS
8.26
10.3
1.30
VSS *SC
1.30
0.09
0.89
0.66
2.95
1.30
1.30
VSS*Litter
0.89
0.11
2.28
1.30
1.30
VSS*GT
Goat trail
Richness of biocrust morphotypes
0.74
0.14
0.11
0.84
0.04
4.27
0.04
1.30
1.30
Goat trail
VSS
Biocrust coverage (%)
Litter
0.41
0.14
Soil comp.
0.003
0.24
0.12
0.9
0.91
0.34
0.66
0.01
6.47
0.18
1.30
1.30
Soil comp.
0.02
0.89
0.04
5.84
1.30
1.30
VSS
0.89
Litter
0.84
0.16
VSS
R2m
P
F
DF
R2c
Effect
DF
F
P
R2m
R2c
Effect
DF
F
P
R2m
Effect
Caatinga Biocrust Distribution and Services
Variable
TABLE 2 | Effect of goat trail soil coverage (%, GT), fine litter biomass (kg ha−1 ), soil compaction (SC, soil penetrability in cm), vegetation succession stage (VSS) and its interaction with soil cover by biological soil
crusts (BSC) on richness of BSC morphotypes and cover by cyanobacteria crust, lichen crusts, and bryophyte crusts in the Catimbau National Park, Pernambuco, Northeast Brazil.
R2c
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FIGURE 3 | The relationships between biocrust communities of the Caatinga dry forest and goat trail cover (%), accumulated fine litter biomass (kg ha−1 ) and soil
(penetrability cm). Variables and functional groups depicted are: total biocrust cover (A–C), cover of cyanobacteria crusts (D–F), lichen (G–I), and bryophyte biocrust
(J–L) cover across regenerating (n = 15) and old-growth forest plots (n = 19).
et al., 2016), where lichens, especially of the genus Collema,
form intermediate biocrust successional stages. The relative
lack of lichens in the sedimentary Caatinga may be explained
by the facts that they are heavily susceptible to trampling (e.g.,
Concostrina-Zubiri et al., 2014), dense litter cover (Briggs and
Morgan, 2008) and don’t grow well on coarse sand (Bowker et al.,
sandy soils. Bryophytes were the second most abundant group
while still subdominant (18% of all biocrusts). The almost
complete absence of lichen-dominated biocrust communities in
every habitat independent of vascular succession in the study
landscape (2.7%) contrasts with our current understanding of
biocrust succession in drylands (Seppelt et al., 2016; Weber
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disturbances, such as treefall gaps, that disappear during forest
succession (Seitz et al., 2017). This was not the case in the
Caatinga, where biocrusts were present at every successional
stage and reached similar coverage scores in old-growth and
regenerating forests. Most plausibly, the Caatinga dry forest
serves as a suitable habitat to biocrusts because light is not as
limiting as in rainforests and other forest biomes. Even the oldgrowth forest permit the occurrence of biocrusts by providing
relatively well-illuminated habitats. This is due to its low stature,
low leaf area index, and high proportion of deciduousness
(Pennington et al., 2009; Oliveira et al., 2013), thus reducing
forest biomass and litter production; all attributes associated
to a highly seasonal rainfall regime and a semiarid climate;
i.e., reduced ecosystem productivity (Eamus, 1999). However,
biocrusts benefited from human disturbance as the distribution
of biocrusts in regeneration areas was less patchy than in oldgrowth-forests, where they may primarily occur because of the
pronounced discontinuity of the canopy (see Figure 1A). As oldgrowth forests are converted into agricultural-forest mosaics,
biocrusts spread over more illuminated habitats, such as old
fields (abandoned crops and pastures) and second-growth forest
stands of varying ages. Precipitation is usually advantageous for
biocrust presence (Bowker et al., 2016) though it comes with
the disadvantage of having to compete with vascular plants for
light and space (Harper and Belnap, 2001; Thompson et al.,
2006). Surprisingly and despite a strong rainfall gradient across
the study landscape, precipitation did not show a significant
impact on biocrust coverage. This may be explained by (1)
the pronounced spatio-temporal patchiness of rainfall in the
Caatinga region (Silva et al., 2017), (2) a high wet season rainfall
allowing biocrusts to water-saturate and grow (saturating water
content for biocrusts see e.g., Szyja et al., 2018), or (3) other
factors adding noise to the biocrust distribution pattern. To
provide an example, chronic anthropogenic disturbance, e.g.,
fuel wood collection, represents a continuous factor opening
canopies at all regeneration stages, independent of precipitation
amount, thus potentially altering biocrust cover and community
composition. Similar results have been found by a recent study
on the distribution of vascular plant biomass, which could be
explained by a multitude of factors, except rainfall (Souza et al.,
2019). Moreover, the values used for the analysis of rainfall effects
were long-term annual means, thereby ignoring the fact that
biocrusts show short-term responses to intensity and frequency
of rainfall in individual years. This is illustrated by the very
steep increase in biomass following a year of above-average
rainfall (Figure 4).
In contrast to rainfall, leaf litter is a factor that clearly
negatively affected the establishment and growth of total biocrust
and cyanobacteria biocrusts in the Caatinga, thus confirming
earlier studies (e.g., Boeken and Orenstein, 2001). However,
litter did not influence biocrust cover between old growth and
regeneration forests, despite differences in standing biomass
among stages of forest regeneration (Souza et al., 2019). This may
be partly accounted by abundance and density of woody parts of
the vegetation, but also be caused by the fact that leaf biomass is
known to rapidly reach a plateau as forest stands mature (Tadaki,
1977). To our knowledge, the reported estimate of biocrust cover
FIGURE 4 | Edaphic characteristics of topsoil layers in bare soils and
biocrusts at early and late successional case study sites in the Catimbau
National Park, northeastern Brazil. Depicted are means ± SD of soil organic
carbon content (A) and chlorophyll a concentration (B) in biocrusts (n = 45)
and bare soil (n = 16). Measurements were done in a year following a drought
period (2017) and after a very wet year (2018) (see material and methods for
details). Significant differences between means are denoted with different
letters above the bars following Tukey’s post hoc test (p < 0.05).
2006). In fact, burial by sand or litter is known to kill lichens,
green algae and smaller cyanobacteria (Campbell, 1979) but may
promote bryophytes, as some species are able to push through a
litter or recent dust layer (Marschall and Proctor, 2004). While
we qualitatively observed a tendency for lichen species to occur
in wetter areas with lower disturbance intensity, their low overall
cover in the study likely compromised statistical power to detect
drivers of lichen distribution.
Biocrust Distribution and Anthropogenic
Disturbance
Biocrusts in (sub-)tropical forests have either been neglected
entirely or described as a transient phenomenon associated to
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pulses and should increase the SOC content of the soil during
a very rainy season (Ferrenberg et al., 2015; Tucker et al.,
2019). This lack of feedback could be explained by the fact that
during years with little or no rainfall, both biocrust growth and
decomposition is restricted (e.g., Thomas et al., 2011), and net
loss in SOC is probably low. Additionally, SOC input might not
only be due to increased net primary productivity of the biocrust
itself but caused by the dust-trapping mechanism of the rough
surface of biocrusts (Belnap, 2003). This is not influenced by
the precipitation amount and collects nutrient rich dust, eroded
at other sites. This theory is supported by measuring biomass,
using chlorophyll a as a proxy for net primary productivity,
which showed a pronounced increase in biocrust biomass at
both sites after the wet year without an increase of SOC.
Disturbance had a negative impact on biocrust growth as biomass
increase was only one third of that in the undisturbed habitat.
The SOC stocks of topsoils with or without biocrusts fit well
within the range of reported values for the Caatinga, related
to other habitats it is very low (Table 3). Values resulting
from this study might underestimate the actual SOC input by
biocrusts in the Caatinga. Later successional stages including
bryophytes and lichens, which have been excluded in this
analysis, have higher carbon sequestration values (Lange, 2001)
and react different to moisture and temperature changes than
cyanobacterial dominated crusts (Tucker et al., 2019). The carbon
stored in biocrusts represents ca. 7% of the carbon sequestered
in aboveground biomass, estimated in a recent quantification of
standing biomass in the Caatinga (Souza et al., 2019). The loss
of such a considerable fraction of the overall carbon balance
due to climate change or increasing disturbance might seriously
threaten this fragile ecosystem and reduce its resilience to
mitigate human impacts. While our results suggest a considerable
influence of biocrusts on the Caatinga ecosystem, one should
be mindful that they reflect carbon sequestration and biocrust
growth of two sites at opposite ends of the disturbance gradient.
In view of the complexity and patchiness of the human-modified
Caatinga (Silva et al., 2017), a future research agenda should
therefore aim at exploring additional environmental conditions
and stages of forest regeneration. Nevertheless, the control
soils of both study sites were equal in SOC and chlorophyll
content, indicating that the observed differences were in fact
based on biocrust presence and biocrust age. These in turn are
shaped by the disturbance regime found at the sites. Filamentous
cyanobacteria such as those from the dominating genera in our
focal landscapes (i.e., Scytonema sp. and Microcoleus vaginatus)
have been indicated as aggregators of sandy soils (Ferrenberg
et al., 2015) thus reducing soil runoff and degradation (i.e.,
a key service in crop/pasturelands Pimentel et al., 1987). At
landscape and regional scale, the Caatinga can be approached
as a successional mosaic through which local farmers support
livelihood by forest products and services such as recovery
of nutrient stocks via forest regeneration. Unfortunately, the
Caatinga dry forest has been driven toward desertification over
large areas as soils become deeply depauperated due to superficial
erosion (i.e., runoff) and nutrient exportation via crops/livestock
(Leal et al., 2005; Vieira et al., 2015). Local depletion of forest
regeneration sources, such as seeds, seedlings and resprouts can
in the Catimbau National Park (ca. 8% of the total area), represent
the first quantitative assessment for tropical dry forests. Studies
in savannas in southern Africa, one of the few investigations
done in woodland ecosystems, found biocrust cover reaching
<1% (except for one site in Sonop province with up to 20%;
Jürgens et al., 2010). It should be emphasized that the Caatinga
human-modified landscapes provide suitable conditions for the
development of biocrust assemblages that have been traditionally
considered “typical” of relatively undisturbed arid habitats
(Belnap, 2001b). In the Caatinga, the best environment for
biocrust development, considering physiological performance,
successional development, ground cover and persistence, consists
of habitats free of vascular plants and lack of soil disturbance.
But vascular plants can also have a beneficial effect on biocrust
presence: Caatinga human-modified landscapes usually support
high stock rates; i.e., 4–6 goats per km², particularly across
regenerating forest stands and old fields (11 goats per km²; Melo,
2017). Although goats consume litter, intense trampling does not
allow biocrusts to settle and develop toward late successional
stages, as confirmed by consistent negative relationships between
goat trails and biocrusts in this study and previously published
studies (Guo et al., 2008; Bowker et al., 2013; Ferrenberg
et al., 2017). Goat-induced disturbance, which leads to a lower
abundance of biocrust presence, except underneath shrubs,
is therefore a plausible mechanism behind the unsuspected
positive association observed between biocrusts and smallstatured shrubs, when plant presence usually would reduce
biocrust distribution. Although more subject to deposition of
litter and competition for light, biocrusts beneath small shrubs
likely benefit from reduced trampling, particularly beneath less
palatable shrubs, such as latex-bearing Jatropha and Croton
species, and reduced evaporation through shading (Bowker et al.,
2005; Zhang et al., 2016), especially at sites with high disturbance
(Tabeni et al., 2014).
Biocrusts as Ecosystem Service Providers
and Their Role for Dry-Forest Resilience
Biocrusts have been reported to influence several ecosystem-level
processes, some of which can be considered as ecological services
of local and global relevance. Understanding of biogeochemical
cycles, including carbon cycling of biocrusts, is limited in
the Caatinga (Elbert et al., 2012; Moura et al., 2016; Althoff
et al., 2018). Cyanobacteria-dominated biocrusts double the soil
organic carbon (SOC) content in the first cm of soil when
compared to open soil, at both sites. The higher disturbance
at the early site reduced the natural SOC stock in the soil and
in the biocrust by half in comparison to the undisturbed site.
However, the loss of SOC in bare soil can be neutralized by the
presence of biocrusts which nonetheless double the SOC amount
in underlying soil. A higher SOC content in the late biocrust
is most likely attributed to a different species composition with
later successional cyanobacteria (e.g., Nostoc sp.) being able to
sequester more carbon (Lange, 2001). Interestingly, no difference
of SOC content could be detected between either the wet or
the dry year, even though one of the dominant organisms in
both crusts, Microcoleus vaginatus, is highly adapted to rain
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Szyja et al.
Caatinga Biocrust Distribution and Services
TABLE 3 | Overview of published and own (highlighted in gray) data on soil organic carbon (SOC) stocks in the Caatinga and other semi-arid ecosystems.
Area/Organism
SOC g kg−1
Depth
Publication
Early Site cyanobacterial biocrust
10.67 ± 4.50
1 cm
This study
Early Site soil
6.04 ± 2.30
1 cm
This study
Late Site cyanobacterial biocrust
19.82 ± 4.04
1 cm
This study
Late Site soil
8.70 ± 4.54
1 cm
This study
Caatinga slash and burn recovering soil
8.61
20 cm
Freitas et al., 2012
Caatinga preserved soil
11.62
20 cm
Freitas et al., 2012
Horqin Desert moss biocrust
6.53 ± 4.63
10 cm
Li et al., 2017
Western Loess Plateau moss biocrust
5.07 ± 0.16
10 cm
Li et al., 2017
Mu Us Desert Cyanobacterial and moss biocrust
10.59 ± 4.93
10 cm
Li et al., 2017
Tengger-Alxa Desert mixed lichen, moss, cyanobacterial biocrust
4.86 ± 0.77
10 cm
Li et al., 2017
Guerbantunggut Desert cyanobacterial and lichen biocrust
2.38 ± 0.62
10 cm
Li et al., 2017
Qaidam Desert cyanobacterial biocrust
0.41 ± 0.17
10 cm
Li et al., 2017
∼ 2.2–5
5 cm
Zhao et al., 2018
SOC Mg ha−1
Depth
Early site cyanobacterial biocrust
1.40 ± 0.60
1 cm
Early Site soil
0.77 ± 0.30
1 cm
This study
Late Site cyanobacterial biocrust
2.49 ± 0.54
1 cm
This study
Late Site soil
1.13 ± 0.60
1 cm
This study
Caatinga soil
20.00
10 cm
Tiessen et al., 1998
Caatinga soil
26.20
10 cm
Kauffman et al., 1993
Caatinga soil
4.14
5 cm
Schulz et al., 2016
Caatinga soil
17.00
5–60 cm
Schulz et al., 2016
Caatinga soil
35.13–46.46
40 cm
Barros et al., 2015
Caatinga slash and burn recovering soil
23.15
20 cm
Althoff et al., 2018
Caatinga preserved soil
31.85
20 cm
Althoff et al., 2018
Deserts and Semi Deserts soil
57.00
Across all horizons
Prentice et al., 2001
Tropical Savannas and Grasslands soil
90.00
Across all horizons
Prentice et al., 2001
Tropical Forest soil
122.00
Across all horizons
Prentice et al., 2001
Temperate Forest soil
147.00
Across all horizons
Prentice et al., 2001
Boreal Forest soil
274.00
Across all horizons
Prentice et al., 2001
Guerbantunggut desert, moss biocrust (Bryum argenteum)
Area/Organism
which they proliferate, reaching considerable coverage, although
they are exposed to the controlling effects imposed by goats,
litter cover and soil attributes. Such a positive synergism
between human populations and biocrusts may result in a
more crucial ecological role played by biocrusts as humans
proceed with the encroachment of tropical landscapes, including
those covered by forest vegetation. Although the presence
of woody vegetation may impose some negative impacts on
biocrusts (i.e., competition and litter cover) it also appears
to provide protection against intense goat trampling. In this
perspective, there must be an optimum combination for biocrusts
considering vascular plant cover and goat pressure. Biocrusts act
as carbon sequestering fertilizers of the Caatinga soils and their
cover benefits from human presence. However, anthropogenic
disturbance will lead to a considerable decrease in this ecosystem
service provided by biocrusts, even if their coverage is not
affected. Considering the intense dynamics of land use provoked
by shifting cultivation and livestock breeding in the Caatinga,
future studies need to investigate functions and services provided
by biocrusts, particularly as drivers for forest regeneration and
also be important (Tabarelli et al., 2017). Increased aridity (as
predicted by climate change models; Torres et al., 2017) can
magnify this human-induced degradation. In this scenario, it
is reasonable to propose an unlimited number of connections
between biocrusts, soil attributes/amelioration, forest recovery
and human well-being/sustainability. As a working hypothesis,
soil engineering by biocrusts, for example, enhances crop
production, retard soil degradation on crops fields, favor
forest recovery after land abandonment and old-growth forest
productivity (i.e., higher forest resilience). Facilitation/nucleation
promoted by sparse shrub-biocrust association may represent
the best opportunity for forest regeneration across degraded
habitats covering naturally poor soils, such as those in our
focal landscape. In other words, biocrusts are connected to
ecosystem resistance/resilience.
In summary, biocrusts seem to be a conspicuous and highly
diverse component of Caatinga human-modified landscapes,
extending the ecological role played by these associations to
a prior overlooked ecosystem type. Furthermore, biocrusts
benefit from the establishment of second-growth forests, in
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Publication
This study
14
December 2019 | Volume 7 | Article 482
Szyja et al.
Caatinga Biocrust Distribution and Services
Desenvolvimento Científico e Tecnológico (CNPq-PELD
project ID: 403770/2012-2). The preparation of the manuscript
was supported by the German-Brazilian PROBRAL program
(CAPES process 88881.030482/2013-01; DAAD project ID:
57413496) to RW, IL, and MT.
as a prevention of further desertification, as they are crucial for
sustainable use of the Caatinga.
DATA AVAILABILITY STATEMENT
The raw data supporting the conclusions of this manuscript will
be made available by the authors, without undue reservation, to
any qualified researcher.
ACKNOWLEDGMENTS
RW, MT, IL, BB, MS, and AM conceived and planned the
experiment. AM, MS, and FO carried out the experiments with
help from BB. MS and AM analyzed the data. BB, RW, and MT
contributed to the interpretation of the results. MS took the lead
in writing the manuscript. MT, RW, BB, and IL supervised the
project. All authors provided critical feedback and helped shape
the research, analysis and manuscript.
IL and MT acknowledge CNPq for productivity grants and MT
also acknowledges the Alexander von Humboldt Foundation
(Germany) for a research grant. Finally, the authors would
like to thank Einar Timdal for the help of identifying the
Bybbia cf. albomarginata lichen species and Kátia Pôrto and
Bruno Silva for the identification of the bryophyte species. The
authors would also like to thank Davi Jamelli for providing and
creating the vegetation classes of the map in Figure 2, and Jens
Brauneck for providing the overview picture of the Caatinga
in Figure 1.
FUNDING
SUPPLEMENTARY MATERIAL
This study was funded by the Coordenação de Aperfeiçoamento
de Pessoal de Nível Superior (CAPES project ID:
88881.030482/2013-01) and the Conselho Nacional de
The Supplementary Material for this article can be found
online at: https://www.frontiersin.org/articles/10.3389/fevo.
2019.00482/full#supplementary-material
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Conflict of Interest: The authors declare that the research was conducted in the
absence of any commercial or financial relationships that could be construed as a
potential conflict of interest.
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