Effects of climate change and land use intensification on regional biological soil crust cover and composition in southern Africa
Introduction
Earth’s drylands (mainly dominated by sensitive forests, steppes and deserts) occupy nearly half of the Earth́s terrestrial surface, and their coverage is expected to increase by the end of the century (Feng and Fu, 2013). Global climate models predict more frequent long-lasting droughts and increased warming within these ecosystems (Huang et al., 2016). This, as well as land use intensification has the potential to produce abrupt changes in multiple ecosystem attributes, thus affecting ecosystem functions, global Earth system functioning and human livelihood (Maestre et al., 2016, Berdugo et al., 2020).
One of the most representative biotic components of dryland regions around the world are biological soil crusts (abbreviated as biocrusts), which are complex communities of photosynthetic organisms, such as cyanobacteria, algae, lichens, and bryophytes, growing together with heterotrophic bacteria, fungi, and archaea within the uppermost millimeters of the soil (Weber et al., 2016). These diminutive communities are estimated to cover ∼12 % of the terrestrial soils (Rodríguez-Caballero et al., 2018a), influencing energy (Couradeau et al., 2016, Rutherford et al., 2017), water (Chamizo et al., 2016, Eldridge et al., 2020), C and N fluxes between the soil and atmosphere (Elbert et al., 2012, Porada et al., 2013, Porada et al., 2014, Porada et al., 2017, Weber et al., 2015, Lenhart et al., 2015). Moreover, they affect biogeochemical cycling within the soil (Delgado-Baquerizo et al., 2013, Maestre et al., 2013), with important effects on soil fertility (Chamizo et al., 2012a), local hydrology (Chamizo et al., 2016, Eldridge et al., 2020), and soil resistance to erosive forces (Belnap et al., 2014). Thus, they provide stable environments and additional resources for vascular vegetation (Luzuriaga et al., 2012, Rodríguez-Caballero et al., 2018b, Havrilla et al., 2019) and the soil fauna (Bamforth, 2008).
Although biocrusts are adapted to aridity, surviving extreme environmental conditions (Pointing and Belnap, 2012), biocrust forming organisms have been shown to be dramatically vulnerable to subtle changes of climatic parameters (Reed et al., 2012, Maestre et al., 2013, Darrouzet-Nardi et al., 2015). According to global change scenarios, their global coverage is expected to decrease dramatically by the end of this century (Rodríguez-Caballero et al., 2018a). Besides this overall reduction in biocrust coverage, climate manipulation experiments also showed that warming, and changes in precipitation patterns (i.e. an increase in the frequency of small water pulses during warm periods) will cause changes in cyanobacteria composition and a reduction of lichen or bryophyte coverage (Maphangwa et al., 2012, Reed et al., 2012, Escolar et al., 2012, García-Pichel et al., 2013, Maestre et al., 2013, Ladrón de Guevara et al., 2014, Ladrón de Guevara et al., 2018), with important implications for ecosystem functioning (Escolar et al., 2012, Maphangwa et al., 2012, Delgado-Baquerizo et al., 2013, Couradeau et al., 2016, Rutherford et al., 2017). Disturbance derived from land use intensification (e.g., trampling) has also been demonstrated to be a relevant threat for biocrusts. In fact, it has similar negative effects as climate change on their coverage and composition (Ferrenberg et al., 2015), causing an increase of soil erosion (Chamizo et al., 2012a, Chamizo et al., 2012b) and modifications of water (Chamizo et al., 2016) and nutrient (Belnap, 1996) cycling in the soil. Thus, both climate change and disturbance caused by land use intensification have major effects on the composition, survival, and distribution of biocrusts. However, especially field experiments on climate change have been limited to very few sites (e.g., Mojave Desert, Colorado Plateau, Iberian Peninsula), that only represent a small fraction of the whole range of ecosystems and climatic conditions under which biocrusts occur. These experimental studies are time-consuming, expensive, and often involve interfering side effects. Passive open-top chambers not only cause a warming inside the chambers, but also cut down the impact of dew and fog (Maphangwa et al., 2012), and warming lamps only heat the uppermost soil region with a downward gradient (Kimball, 2005). Such negative side-effects of field experiments can be avoided by combining experimental results with direct observations in the field or by applying remote sensing technologies (Palmer et al., 2002).
Space-for-time (SFT) substitutions, where spatial climatic and disturbance gradients are used to investigate the response of biocrusts to anticipated future conditions, form one of these options. This method has been frequently applied to analyse plant succession and to model climate change effects on biodiversity and species richness (Blois et al., 2013). In a recent study, it provided valuable data on the long-term effects of temperature and precipitation on the composition and coverage of biocrust communities (García-Pichel et al., 2013). Another methodology is the use of historical and open access high temporal resolution satellite images combined with coverage and composition data along climatic gradients. Such multi-temporal series of satellite images could provide crucial information on biocrust dynamics and response to environmental factors, such as temperature, precipitation, and disturbance (Karnieli et al., 1996, Karnieli, 2003, Burgheimer et al., 2006, Rodríguez-Caballero et al., 2015, Panigada et al., 2019).
The main objective of this paper is to investigate the long-term response of biocrusts to warming, livestock trampling, and changes in precipitation amount and frequency predicted for the Succulent Karoo. The study region is located within an arid winter rainfall biome of southern Africa (Mucina et al. 2006) that comprises a great diversity and unique flora of succulent plants (Mucina et al., 2006, Schmiedel and Jürgens, 1999). It also harbours a variety of different biocrust types that are considered as a critical component of the ecosystem (Büdel et al., 2009). To achieve the objective, we apply a multidisciplinary approach that combine information of the Normalized Difference Vegetation Index (NDVI) obtained form satellite images with field data and climate predictions.
We hypothesize that i) NDVI will reflect the rapid response of biocrusts to variations in climatic factors, and ii) as a consequence, the NDVIbiocrust will be reduced in the future due to a predicted increase in aridity according to the IPCC predictions for the region (Weber et al., 2018). We further suggest that iii) the reduced NDVIbiocrust will be the result of changes in both biocrust coverage and composition.
Section snippets
Material and methods
This study was conducted in a semi-arid ecosystem in the Succulent Karoo, South Africa, near the BIOTA biodiversity observatory Soebatsfontein S22 (Supplementary Fig. S1). More detailed information on the study site is provided in section 1 of the supplementary material and in Schmiedel et al., (2016). In order investigate the long-term response of biocrusts to climate change and livestock trampling we utilized climate data and satellite imagery, covering a time-span of 10 years. These data
Analysis of biocrust NDVI response to water pulses under different levels of disturbance
During the period from 2001 to 2010, biocrust-dominated areas within the Succulent Karoo had a mean daily NDVI value of 0.19, that varied strongly between seasons and years (Fig. 2). About 74 % of the variation in NDVIbiocrust could be explained by WD, SWC and incoming solar radiation (Supplementary Table S3). Water deficit, which is strongly influenced by temperature and precipitation, was the factor that exerted the largest effect on daily NDVI values, controlling its annual seasonality (Fig.
Discussion
This study shows that water deficit is the environmental factor most relevant for the occurrence and composition of biocrusts, which is reflected by both satellite (NDVIbiocrust) and field mapping data. Predicted increasing temperatures and decreasing rainfall amounts and numbers suggest a decrease in biocrust coverage and diversity during the next decades, which is aggravated by high livestock density.
Conclusions
Our results demonstrate that the combination of multi-temporal series of historical satellite images and Earth system models is well suited to identify climate change patterns and effects on biocrust cover and composition at regional scales. Doing this, we found that biocrust distribution within southwestern African drylands is governed by the interplay of climatic factors that determine whether biocrusts are active, the duration of activity periods and droughts, and by land use intensity. This
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
Research in South Africa was conducted with South African research permits (No. 048/2003) and the appendant export permits. ERC was supported by a Nobel Laureate Paul Crutzen fellowship; the REBIOARID (2018-101921-B-I00) project, funded by the FEDER/Science and Innovation Ministry-National Research Agency through the Spanish National Plan for Research and the European Union Funds for Regional Development; Consejería de Economía, Conocimiento, Empresas y Universidad from the Junta de Andalucía
References (70)
Protozoa of biological soil crusts of a cool desert in Utah
J. Arid Environ.
(2008)- et al.
Soil lichen and moss cover and species richness can be highly dynamic: The effects of invasion by the annual exotic grass Bromus tectorum, precipitation, and temperature on biological soil crusts in SE Utah
Appl. Soil Ecol.
(2006) - et al.
Controls on sediment production in two U.S. deserts
Aeolian Res.
(2014) - et al.
Ground and space spectral measurements for assessing the semi-arid ecosystem phenology related to CO2 fluxes of biological soil crusts
Remote Sens. Environ.
(2006) - et al.
Biological soil crust development affects physicochemical characteristics of soil surface in semiarid ecosystems
Soil Biol. Biochem.
(2012) - et al.
Rapid succession of biological soil crusts after experimental disturbance in the Succulent Karoo, South Africa
Appl. Soil Ecol.
(2011) - et al.
Small scale spatial heterogeneity of Normalized Difference Vegetation Indices (NDVIs) and hot spots of photosynthesis in biological soil crusts
Flora – Morphol., Distrib., Funct. Ecol. f Plants
(2012) - et al.
The effect of microphytes on the spectral reflectance of vegetation in semiarid regions
Remote Sens. Environ.
(1996) - et al.
Advanced image processing methods as a tool to map and quantify different types of biological soil crust
ISPRS J. Photogramm. Remote Sens.
(2014) - et al.
Importance of biocrusts in dryland monitoring using spectral indices
Remote Sens. Environ.
(2015)
Transferability of multi- and hyperspectral optical biocrust indices
ISPRS J. Photogramm. Remote Sens.
Effect of grazing on vegetation and soil of the heuweltjieveld in the Succulent Karoo, South Africa
Acta Oecol.
A new approach for mapping of Biological Soil Crusts in semidesert areas with hyperspectral imagery
Remote Sens. Environ.
Potential nitrogen fixation activity of different aged biological soil crusts from rehabilitated grasslands of the hilly Loess Plateau, China
J. Arid Environ.
Fitting linear mixed-effects models using lme4
J. Stat. Softw.
Soil surface disturbances in cold deserts: effects on nitrogenase activity in cyanobacterial-lichen soil crusts
Biol. Fertil. Soils
Response of desert biological soil crusts to alterations in precipitation frequency
Oecologia
Global ecosystem thresholds driven by aridity
Science
Space can substitute for time in predicting climate-change effects on biodiversity
Proc. Natl. Acad. Sci.
Southern African biological soil crusts are ubiquitous and highly diverse in drylands, being restricted by rainfall frequency
Microb. Ecol.
Discriminating soil crust type, development stage and degree of disturbance in semiarid environments from their spectral characteristics
Eur. J. Soil Sci.
Biocrusts positively affect the soil water balance in semiarid ecosystems
Ecohydrology
Bacteria increase arid-land soil surface temperature through the production of sunscreens
Nat. Commun.
Observations of net soil exchange of CO2 in a dryland show experimental warming increases carbon losses in biocrust soils
Biogeochemistry
Decoupling of soil nutrient cycles as a function of aridity in global drylands
Nature
Contribution of cryptogamic covers to the global cycles of carbon and nitrogen
Nat. Geosci.
The pervasive and multifaceted influence of biocrusts on water in the world's drylands
Glob. Change Biol.
Warming reduces the growth and diversity of biological soil crusts in a semi-arid environment: implications for ecosystem structure and functioning
Philos. Trans. R. Soc. London Ser. B, Biol. Sci.
Expansion of global drylands under a warming climate
Atmos. Chem. Phys.
Climate change and physical disturbance cause similar community shifts in biological soil crusts
Proc. Natl. Acad. Sci. U. S. A.
Temperature drives the continental-scale distribution of key microbes in topsoil communities
Science
The BIOTA observatories
Towards a predictive framework for biocrust mediation of plant performance: a meta-analysis
J. Ecol.
Diferentiating biological soil crusts in a sandy arid ecosystem based on multi- and hyperspectral remote sensing data
Cited by (14)
Utilization of deep learning tools to map and monitor biological soil crusts
2024, Ecological InformaticsChallenges and solutions to biodiversity conservation in arid lands
2023, Science of the Total EnvironmentCitation Excerpt :Consequently climate changes have caused floristic reorganization and from an increase in precipitation in Arizona, North America (Brown et al., 1997), as well as changes in floristic communities as a consequence of drought (Jürgens et al., 2018). Changes in climate (longer droughts and higher temperatures) can also impact on the biological soil crust (biocrust) (Reed et al., 2019; Rodríguez-Caballero et al., 2022) (especially in grazed areas), also undermining the capability of these systems to recover, and overlooking the unique biology of these regions. Furthermore, changes in climate have also been shown to change phenology and delay flowering in some regions, which may drive asynchronies and the potential loss of available pollinators (Daru et al., 2018).
The crucial interactions between climate and soil
2023, Science of the Total EnvironmentCitation Excerpt :Climate change induced shifts in plant community composition shape the composition and functioning of soil biota (Kardol et al., 2010), which, in turns, change soil respiration rates. This happens also in ecosystems without lush vegetation, such as drylands, where the complex microbial communities that occupy biological soil crusts (Xu et al., 2022a), despite their ability to adapt to extreme conditions, are sensitive to subtle changes of climatic parameters (Rodríguez-Caballero et al., 2022). On the other hand, any uncontrolled expansion of large animals in some regions may become a significant geomorphic forcing that causes soil compaction and structure deterioration, reduced water infiltration and increased runoff and erosion (Bayne et al., 2004; Mauri et al., 2019), with already mentioned implications for climate.