Plant and Soil

, Volume 429, Issue 1–2, pp 91–100 | Cite as

Effects of indigenous soil cyanobacteria on seed germination and seedling growth of arid species used in restoration

  • M. Muñoz-RojasEmail author
  • A. Chilton
  • G. S. Liyanage
  • T. E. Erickson
  • D. J. Merritt
  • B. A. Neilan
  • M. K. J. Ooi
Regular Article


Background and aims

Cyanobacteria from biocrusts can enhance soil function and structure, a critical objective when restoring degraded dryland ecosystems. Large-scale restoration of biodiversity requires direct seeding of native plant species, and bio-priming seeds with cyanobacteria is a potential method of initiating enhanced soil functioning. The utility of cyanobacteria for improving soil is therefore dependent on whether target plant species remain unaffected during its application.


Cyanobacteria from the genera Microcoleus and Nostoc were isolated from locally-sourced biocrust samples, and cultured under controlled conditions. A two-factor laboratory experiment was conducted including cyanobacteria and the culture growth medium (BG11) as factors. We bio-primed seeds of five species native to Western Australia, commonly used in dryland restoration, by soaking them in the cultures developed, and assessed germination and growth.


We found significant positive effects of seeds bio-primed with cyanobacteria on germination and seedling growth of two species, Senna notabilis and Acacia hilliana, respectively. Importantly, no significant negative effects of cyanobacteria were found for any of the species studied.


Few studies of cyanobacteria effects on regeneration of native species exist. We found that the potential benefits of applying indigenous bacteria via bio-priming seeds would not inhibit plant establishment, and indeed may be beneficial for some species used in dryland restoration.


Pilbara Drylands Biocrust Native plants Seedling recruitment Land rehabilitation Bio-priming 


Millions of hectares of drylands are being degraded each year, and restoring these areas is a global priority within the Sustainable Development Goals of the United Nations 2030 Agenda (Keesstra et al. 2018). A critical challenge for successful restoration in dryland ecosystems is ensuring that suitable soil substrates with viable seedbanks are available to support plant establishment (Muñoz-Rojas et al. 2016a). Given the large scale of disturbance from human activities such as mining, and the subsequent scale of restoration required, direct seeding is often the only viable means for restoring diverse and functional native vegetation communities (Erickson et al. 2017). This seeding effort can only be justifiable if seeds surpass the crucial life-history stages of seed germination and seedling emergence. These early phases of plant establishment involve many interlinked transitions (Erickson et al. 2017; Larson and Funk 2016) and seed regeneration is the foundation for the recovery of functional native plant communities and thus, the persistence and maintenance of terrestrial biodiverse ecosystems worldwide (Jiménez-Alfaro et al. 2016; Miller et al. 2017; Perring et al. 2015).

Biological crusts, or biocrusts, are communities of microscopic and macroscopic organisms that live in the upper surface of soils (Büdel et al. 2016; Chilton et al. 2017). Cyanobacteria are major components of biocrust and consist of, oxygenic, photosynthetic bacteria capable of surviving in extreme environmental conditions and tolerating high temperatures, desiccation, extreme pH and salinity (Singh et al. 2016; Williams et al. 2014). In recent years, studies have highlighted the key role of cyanobacteria as ‘ecological engineers’ in drylands by enhancing soil function and structure (Antoninka et al. 2016; Bowker 2007; Park et al. 2017). These organisms are one of the most promising microorganisms used as bio-fertilizer as they produce active compounds that enhance plant growth and improve overall soil conditions (Singh et al. 2016). Some cyanobacteria species are able to release exopolysaccharides (EPS) that work as a cement, increasing soil stability, crusting, and moisture-holding capacity (Rossi et al. 2017). But these substances have also shown a potential for increasing germination of desert plants (Song et al. 2017). Thus, the cyanobacteria culture medium, where EPS are excreted, has been proposed as a nutrient supplement to promote succession of artificial cyanobacterial biocrust (Xu et al. 2013), and could also be used as an inoculant to promote other early plant recruitment processes. However, the effects of cyanobacteria on the early plant life-history stages of germination and seedling growth still warrant further investigation. Most of the available studies addressing the use of cyanobacteria as bio-fertilizer have been conducted in plants used in agriculture, such as rice or wheat crops (Singh et al. 2016). The few studies conducted in natural ecosystems have shown contrasting results that include positive, negative, or uncorrelated interactions between vascular plants and cyanobacteria species (Song et al. 2017; Su et al. 2009; Zhang et al. 2016; Zaady et al. 1997). Thus, the utility of cyanobacteria as a way of enhancing soil function and structure for restoration is dependent on whether the associated plant species targeted for restoration remain unaffected during its application, or even benefit from it. To our knowledge, no studies investigating the effects of cyanobacteria on bio-primed seeds in a restoration context currently exist.

Here, we assessed the early-stage transitions of germination and seedling growth of seeds bio-primed with locally-sourced indigenous cyanobacteria for five native species used in arid land restoration (Acacia hilliana, Senna notabilis, Grevillea wickhamii, Triodia epactia and Triodia wiseana). These species cover a range of genera (Table 1), are native to the Pilbara region (an arid, biodiverse region of north-west Western Australia) and are targeted for use in restoration after intensive mining activities have ceased (Bateman et al. 2016; Kneller et al. 2018; Muñoz-Rojas et al. 2016b).
Table 1

List of five plant species native to the Pilbara region used in this study


Plant species

Life form (photosynethetic pathway)*


Acacia hilliana

Shrub (C3)


Senna notabilis

Shrub (C3)


Grevillea wickhamii

Shrub or small tree (C3)


Triodia epactia

Grass (C4)


Triodia wiseana

Grass (C4)

*Adapted from Bateman et al. (2016)

Materials and methods

Cyanobacteria culturing and selection

A polyphasic approach combining whole community 16S rDNA profiling as well as culturing was used to identify candidate cyanobacterial strains that were both representative of the native community and able to be up-scaled for scalable growth trials (Table 2). Soil biocrust samples were collected from two cyanobacteria-dominated biological soil crusts free of mosses, lichens and plant material near Gallery Hill in the Pilbara Region of Western Australia (21°37.416’S, 119°02.303′E) in May 2009. Samples were taken from the upper 10 mm and transported in air-tight zip lock bags to the University of New South Wales (UNSW, Sydney, Australia) and stored at 4 °C until processing in July 2009 (Fig. 1).
Table 2

Cyanobacteria isolates identified to genus and species level with viability for large-scale growth where ‘-‘ indicates isolates did not outgrow 3 ml of media, ‘+’ indicates isolates did not outgrow 20 ml of culture, ‘++’ indicates isolates were up-scaled to greater than 50 ml of media



Large scale growth


Limnothrix sp.


Microcoleus paludosus



Limnothrix sp.



Leptolyngbya foveolarum


Leptolyngbya sp.



Microcoleus paludosus



Leptolyngbya sp.



Calothrix sp.


Calothrix desertica



Nostoc microscopicum



Leptolyngbya sp.


Calothrix sp.


Scytonema sp.


Fig. 1

(a) Example of the top and bottom of cyanobacterial biocrusts sampled; Liquid cultures of (b) Nostoc microscopicum and (c) Microcoleus paludosus and; Microscopy of (d) Nostoc microscopicum and (e) Microcoleus paludosus

Bacterial profiling was performed upon whole-community DNA extracted using the FastDNA SPIN Kit for Soil (MP Biomedicals) as per the manufacturer’s instructions. Genomic DNA was submitted to RTL Genomics (Lubbock, Texas) where pyrosequencing of the 16S rDNA was conducted using the universal bacterial primers 28F/519R. Pyrosequencing data from each site was combined and analysed using standard approaches (Schloss et al. 2011) resulting in 16,093 high-quality reads across 2840 OTUs formed at 97% similarity (see Supplementary Material for further detail, Fig. S1). The majority of sequences (78%) were cyanobacterial according to GreenGenes (McDonald et al. 2012) taxonomic assignment and comprised of a diverse range of genera dominated by the families Oscillatoriophycideae and Nostocophycideae (42.4% and 41.8% of sequences, respectively) (Fig. 2). These families typify two distinct morphotypes: large, simple filamentous able to form tightly interwoven mats (Oscillatoriophycideae) and long, heterocystic types which produce scytonemin-containing gelatinous sheaths (Nostocophycideae).
Fig. 2

Relative abundance of cyanobacterial orders (inner ring) and genera (outer ring) as determined via genomic profiling

Cyanobacteria cultures were isolated as in Rippka (1988) and identified to species via microscopy, BLAST analysis and phylogeny (see Supplementary Material for further detail, Table S1). The species identified (Table 2) were distinct from those detected via community profiling using the GreenGenes database, however, this was not unexpected due to the problematic nature of cyanobacterial classification (Garcia-Pichel et al. 1996). For example, Microcoleus and Phormidium are phenotypically and ecologically similar and are poorly resolved phylogenetically (Garcia-Pichel et al. 2013). We sought to select candidate cyanobacteria species which were both representative of the dominant morphotypes detected via pyrosequencing and that exhibited sufficient growth of biomass for bio-priming. Based on these criteria and our findings we selected isolates corresponding to Microcoleus paludosus (Oscillatoriophycideae) and Nostoc microscopicum (Nostocophycideae) (Fig. 1). These taxa have a broad presence in Australian and arid lands worldwide (Büdel et al. 2016; Chilton et al. 2017; Williams et al. 2014). Optimal cyanobacterial growth was achieved using deep-pan petri dishes using BG11 media at 25 °C under constant 80 umol m−2 s−1 of light. For bio-priming, culture mass for Nostoc microscopicum and Microcoleus paludosus was mixed at a ratio of 50:50 to reflect the relative abundance of the two dominant morphotypes observed via pyrosequencing. The mixed culture was filtered and oven dried to obtain the dry biomass, and re-suspended in both distilled water (H2Od) and the culture growth BG11 to achieve a concentration of 1 g/L in both treatments.

Bio-priming of seeds with cyanobacteria

Seeds for each species were collected from wild plant populations in the Pilbara region of Western Australia in Nov-Dec 2013. Seeds were stored in a controlled environment room at 15 °C and 15% RH prior to experimentation. Prior to germination testing, seeds of A. hilliana and S. notabilis were first treated to overcome physical dormancy by placement for 1–2 min in hot water at 80–100 °C. Seeds of Triodia possess physiological dormancy and these seeds were first removed from their covering floret structures that restrict germination (following methods outlined in Erickson et al. (2016). Non-viable seeds for all species were removed via x-ray analysis to eliminate seed quality as a potential impediment to germination responses. Seeds from all species were then surface sterilized in a 1% (w/v) calcium hypochlorite [Ca(OCl)2] solution for 30 min and rinsed before cyanobacteria bio-priming.

For each of the five plant species, a two-factor fully orthogonal experiment was conducted in the laboratory in July 2017, with the application of cyanobacteria culture and the BG11 medium as the two factors. Seeds were bio-primed with cyanobacteria in either an H2O solution (CY + H2O), or in the culture growth medium BG11 solution (CY + BG11). H2Od as a control (Control-H2O) and culture growth media without cyanobacteria (Control-BG11) were also included. Seeds (n = 100) were plated in replicated 90 mm Petri dishes (n = 4 per treatment; 25 seeds per dish) and incubated at 28/20 °C (12/12 hr). Each dish was initially irrigated with 10 mL of either H2O or BG11 solution, depending on treatment, and subsequently topped up with 2 mL to prevent drying out.

Germination was scored as emergence of the radicle and checked daily for 7 d, and again at day 10. Measurements of root and shoot lengths were undertaken on 7 day old seedlings. Ungerminated seeds were assessed for viability after 17 d using a cut test (Ooi et al., 2004). Germination rate was calculated as the time required to reach 50% of the total germination (T50). Proportional data were analysed using Generalised Linear Models (GLMs) with a binomial distribution (germination, seedling survival). A linear model was used for analysing root/shoot lengths. The main factors tested for these data were BG11 medium (yes or no) and cyanobacteria (yes or no). Post-hoc multiple comparisons were made using the package lsmeans. All analyses were conducted using the R statistical platform Version 3.1.2 (R Core Team 2017). The values of P < 0.05 were considered as statistically significant. Germination rate was calculated using the R package drc (Ritz and Streibig 2005) with the time required to reach 50% of the total seeds germinated (T50). Comparisons between treatments were made using the compParm function.

Data availability

Sequences used in this study are available for download from the NCBI short read achieve (SRA) under Bioproject number PRJNA310158. Cyanobacteria isolate sequences are available from GenBank under accession numbers KU612238- KU612249. All other data generated or analysed during this study are included in this published article (and its supplementary information files).


The polyphasic characterisation of cyanobacteria revealed a diverse array of genera exhibiting traits critical for colonisation and survival within extreme arid conditions, including filamentous growth, heterocysts (for Nostocophycideae), and EPS production (Table 2, Fig. 2).

The best model for the germination of Acacia hilliana seeds included both factors, with a significant interaction between cyanobacteria and BG11 (df = 1, χ 2 = 7.4164 P = 0.006). Although Acacia hilliana seeds germinated to similar proportions across all treatments, there was a small but significant positive effect of the Control-BG11 treatment (Fig. 3a). However, a similar highly significant interaction found for Acacia hilliana seedling survival (df = 1, χ 2 = 14.652 P < 0.001) (Fig. 3b), and seedling shoot (df = 1224, F = 40.551 P < 0.001) and root growth (df = 1224, F = 32.852 P < 0.001) (Fig. 4a, b), was driven by a strong negative effect of the BG11 medium; seeds soaked in BG11 germinated but nearly all quickly died (mortality measured at Day 17 for all seeds germinating by Day 6). The negative effect of the culture medium appeared to be counteracted by the addition of cyanobacteria, as survival and seedling growth of Acacia hilliana was not affected in seeds bio-primed with cyanobacteria + BG11 (Fig. 3, Fig. 4).
Fig. 3

(a) Seeds germinated and (b) survived seeds bio-primed with cyanobacteria (vs control) in water and BG11 medium (Mean proportion ± SE; n = 100). Levels of significance: (*) P < 0.05; (**) P < 0.005; (***) P < 0.001

Fig. 4

(a) Seedling shoot length and (b) seedling root length of seeds bio-primed with cyanobacteria (vs control) in water and BG11 medium (Mean proportion ± SE; n = 100). Levels of significance: (*) P < 0.05; (**) P < 0.005; (***) P < 0.001

For Senna notabilis, the best fitting model for germination contained only the main effect of cyanobacteria (df = 1, χ 2 = 9.0091 P = 0.003). The addition of cyanobacteria had a significant positive effect on germination in the presence of H2O, and a positive but non-significant effect in the presence of BG11 solution (Fig. 3). There were no effects on shoot growth, but a significant main effect of cyanobacteria on root growth (df = 1226, F = 6.333, P = 0.0125). However, we did not find any significant differences between treatments (with or without cyanobacteria added) within each level of media (Fig. 4b).

For all remaining species (Grevillea and the two Triodia species), there were no significant effects found for germination, but several small effects on seedling survival or growth. There were significant main negative effects of the BG11 medium on Grevillea (df = 188, F = 2.107, P = 0.004) and Triodia epactia root growth (df = 1125, F = 31.944, P < 0.001). For Triodia wiseana, there was a significant main effect of the BG11 medium on shoot growth (df = 1129, F = 7.223, P = 0.008) and a significant interaction between the two factors for root growth (df = 1129, F = 4.189, P = 0.043), driven mainly by a slight suppression of growth with the BG11 medium (Fig. 3, Fig. 4).

There were no clear differences found between treatments on the rate of germination (T50) for any of the study species. The only significant effect showed that cyanobacteria slowed germination rate slightly for Grevillea wickhamii seeds in the BG11 solution (3.84 ± 0.15 versus 4.51 ± 0.22 days). Senna notabilis was the fastest species, with a T50 of 0.08 days (cyanobacteria + water) (0.08–0.32 days across all treatments), followed by Triodia epactia (1.74–1.86 days), Triodia wiseana (1.67–2.08 days), Acacia hilliana (2.62–3.35 days) and Grevillea wickhamii (3.84–4.51 days) (Fig. S2).


Effects of seed bio-priming with cyanobacteria on early developmental stages of native species

Cyanobacteria and the BG11 medium had no effect on the germination and growth of Grevillea wickhamii or the two Triodia species, meaning application of either as a nutrient supplement to promote artificial cyanobacterial biocrusts would have little impact on the early life-history stages of these species, at least within in the timeframe evaluated in this study. However, our results did show large significant effects on aspects of Acacia hilliana and Senna notabilis germination, seedling survival and growth over the timeline evaluated, suggesting that there may even be some beneficial effects of bio-priming seeds with indigenous cyanobacteria. While there are some species-specific differences in responses, in agreement with previous studies conducted in arid areas (Song et al., 2017; Zaady et al. 1997), overall cyanobacteria did not have an inhibitory effect on any of the species studied.

Seed germination and seedling growth are critical stages of plant development largely influenced by water potential, air and soil temperature (Arnold et al. 2014; Ooi 2007; Ooi et al. 2009). Since biocrust cyanobacteria can influence several soil characteristics such as soil structure, porosity, nutrient and water availability (Chamizo et al. 2012), there are several ways in which cyanobacteria may influence germination in the soil and therefore seed responses may be different in the field. Subsequently, the formed biocrust will have an effect on seedling emergence and plant establishment. Some studies have reported an inhibition of seedling emergence, survival, and establishment with the appearance of biocrust as a response to the species-specific interactions between vascular plants and forming biocrust (Escudero et al. 2007). Nevertheless, in most cases biocrusts have a positive effect on seedling growth caused by the increase in soil N contents and the release of beneficial substances such as exopolysaccharides (EPS) (Wang et al. 2009; Xu et al. 2013).

The biocrust community structure found here is comparable to early stage biocrusts in Australia (Chilton et al. 2017) and, globally, to Type 1 and 2 biocrusts from the Kalahari (Elliott et al. 2014), to biocrusts on dune slopes of the Gurbantünggüt Desert (Liu et al. 2014) and early-stage crusts from the Colorado Plateau (Nunes da Rocha et al. 2015). In our study, cyanobacteria composition was held constant and thus the differences found in germination and growth across plant species is likely attributable to seed traits (Zhang and Belnap 2015). For example, one explanation for the positive effect of cyanobacteria on seeds of Senna notabilis is that these seeds are known to germinate rapidly over a wide temperature regime when compared to other native species of northern deserts in Western Australia (Commander et al., 2017). Given this species appears to be programmed for rapid germination, a trait known to help some species in arid ecosystems (Parsons 2012), the added advantage of a bio-fertilizer may have been expressed in this early recruitment phase when compared to other species evaluated.

Some studies have shown that the exopolysaccharides (EPS) surrounding cyanobacterial cells have a major role in protecting these cells from stress in extreme environmental conditions such as desiccation (Pointing and Belnap 2012; Chittapun et al. 2017). These substances are capable of forming a microenvironment that prevent water loss by buffering osmotic potential (Rossi et al. 2017). Therefore, recent research has focused on the specific effect of EPS excreted by cyanobacteria on seed germination of arid plant species, obtaining higher rates of germination with addition of these substances (Xu et al. 2013). The positive effects of the locally-sourced cyanobacteria species used in this study (Nostoc microscopicum and Microcoleus paludosus) on particular species is likely related to their capacity to produce EPSs, which makes them potentially ideal candidates for bio-fertilization of native plant species.

Although seeds of Acacia hilliana germinated in similar proportions under all treatments, there was a notable effect on seeds soaked in the control BG11 solution (Control- BG11) (Fig. 2), and they did not develop further to produce healthy radicle and shoot growth (Fig. 3b, Fig. 4). The negative effect of the culture medium appeared to be counteracted by adding cyanobacteria, as seedling survival and growth of Acacia hilliana was not affected in seeds bio-primed with cyanobacteria + BG11 (Fig. 3b, Fig. 4). BG11 (Broth w/ Minerals) is a universal medium for the cultivation and maintenance of blue green algae (cyanobacteria) that has been extensively used in inoculation experiments (Rossi et al. 2017), and is mainly composed of salts in the form of sodium nitrate (NaNO3) (George et al., 2014).

Some studies have reported that the presence of soluble salts can suppress plant growth. This could be seen by small reductions in growth for several of our study species in the BG11 medium. However, in susceptible species, such as seen in the Acacia, interacting factors including the osmotic potential effect, ion toxicity and antagonism can have much larger negative effects on growth (Rehman et al. 2000; Abari et al. 2011). Inhibition of seedling growth by sodium elements has been attributed to insufficient water absorption for radicle emergence, or toxic effects on the embryo (Azza et al. 2007). Hosseini et al., (2002) suggested that differences in sensitivity between germination and subsequent seedling growth in the presence of high salt concentrations may be caused by several factors. One of the potential causes is that germination is less responsive to high tissue Na + concentrations than seedling growth (Debez et al. 2004; Kim et al. 2012). The role of cyanobacteria appears then to be critical for removing Na + at this early seedling stage in Acacia hilliana. Several studies have underpinned the ability of cyanobacteria not only to tolerate stresses that are predominant in salt-affected soils, such as nutrient deficiency, salinity, drought and temperature increases, but also to uptake Na + for their growth and nitrogen fixation function. Thus, these organisms adopt various mechanisms for salt tolerance and have been suggested to reclaim salt-affected soils (Rossi et al. 2017; Singh et al. 2016). Our results highlight the need for further assessment of the ability of cyanobacteria to alleviate the negative effects of saline conditions in native species.

Implications for direct-seeding practices in land restoration

In addition to the beneficial effects of cyanobacteria on soil C sequestration, N fixation and soil stability to restore dryland ecosystems (Büdel et al. 2018; Rossi et al. 2017), this study underpins the potential role for native seeds to be inoculated with beneficial cyanobacteria during early-stage seed applications and not be detrimental to the critical plant regeneration stages of germination and seedling growth phases known to be problematic for restoration success. The results of Acacia hilliana point towards a role for salt-tolerant cyanobacteria in alleviating salinity stress during seedling growth, which can be important for seedling recruitment and subsequent plant development in restoration. Salinity imposes serious environmental problems in arid and semi-arid regions by limiting plant growth and productivity during all developmental stages (Anaya-Romero et al. 2015; Azza et al. 2007).

A critical consideration in the application of indigenous cyanobacteria for landscape-scale restoration projects is the ability to grow substantial biomass (Velasco Ayuso et al. 2016). Moreover, how beneficial cyanobacteria can be integrated into restoration settings remains to be tested, but could be delivered in combination with rapidly developing seed enhancement technologies such as seed coating, pelleting, and priming approaches (O’Callaghan 2016; Erickson et al. 2017). Developing novel formulations that maintain the viability of both seeds and cyanobacteria inoculant during storage and application will be crucial for using these technologies in large-scale restoration. This line of work provides an exciting opportunity for scientists and on-ground practitioners to merge multiple research disciplines together to aid future land restoration opportunities.


We found significant positive effects of bio-primed seeds with locally-sourced indigenous cyanobacteria from the genera Microcoleus and Nostoc on seed germination and seedling growth of Senna notabilis and Acacia hilliana, respectively. No significant effects were observed on Grevillea wickhamii, Triodia epactia and Triodia wiseana. Our results showed that the influence of cyanobacteria on early seedling development is species-specific but overall, cyanobacteria did not have an inhibitory effect on any of the species studied. This study highlights the potential role for native seeds to be inoculated with beneficial cyanobacteria during early-stage seed applications and not be detrimental to critical germination and early seedling growth, phases known to be problematic for restoration success. Further considerations such as the ability to grow substantial biomass, and the most effective way to deliver seed and cyanobacteria inoculum will be critical to upscale these applications to landscape restoration.



This research project was supported by BHP Billiton Iron Ore Community Development Project (contract no. 8600048550) under the auspices of the Restoration Seedbank Initiative (2013-2018), a partnership between BHP Billiton Iron Ore, The University of Western Australia, and the Botanic Gardens and Parks Authority; and The University of Western Australia Research Collaboration Award 2018 Innovative nature-based strategies for drylands restoration: the potential of indigenous cyanobacteria. MMR acknowledges the support from the Australian Research Council Discovery Early Career Researcher Award (DE180100570).

Supplementary material

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11104_2018_3607_MOESM3_ESM.docx (729 kb)
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  1. Abari AK, Nasr MH, Bayat D (2011) Salt effects on seed germination and seedling emergence of two acacia species. African J Plant Sci 5:52–56Google Scholar
  2. Anaya-Romero M, Abd-Elmabod SK, Muñoz-Rojas M, Castellano G, Ceacero CJ, Alvarez S, Méndez M, De la Rosa D (2015) Evaluating soil threats under climate change scenarios in the Andalusia region, southern Spain. Land Degrad Dev 26:441–449CrossRefGoogle Scholar
  3. Antoninka A, Bowker MA, Reed SC, Doherty K (2016) Production of greenhouse-grown biocrust mosses and associated cyanobacteria to rehabilitate dryland soil function. Restor Ecol 24:324–335CrossRefGoogle Scholar
  4. Arnold S, Kailichova Y, Knauer J, Ruthsatz AD, Baumgartl T (2014) Effects of soil water potential on germination of co-dominant Brigalow species: implications for rehabilitation of water-limited ecosystems in the Brigalow Belt bioregion. Ecol Eng 70:35–42CrossRefGoogle Scholar
  5. Azza Mazher AM, EM FEL-Q, Farahat MM (2007) Responses of ornamental plants and woody trees to salinity. World J Agric Sci 3(3):386–395Google Scholar
  6. Bateman A, Lewandrowski W, Stevens J, Muñoz-Rojas M (2016) Ecophysiological indicators to assess drought responses of arid zone native seedlings in reconstructed soils. Land Degrad Dev.
  7. Bowker MA (2007) Biological soil crust rehabilitation in theory and practice: an underexploited opportunity. Restor Ecol 15:13–23CrossRefGoogle Scholar
  8. Büdel B, Dulic T, Darienko T, Rybalka N, Friedl T (2016) Cyanobacteria and algae of biological soil crusts. In: Weber B, Büdel B, Belnap J (eds) Biological soil crusts: an organizing principle in drylands. Springer international publishing, Cham, pp 55–80CrossRefGoogle Scholar
  9. Büdel B, Williams WJ, Reichenberger H (2018) Annual net primary productivity of a cyanobacteria-dominated biological soil crust in the Gulf Savannah, Queensland, Australia. Biogeosciences 15(2):491–505CrossRefGoogle Scholar
  10. Chamizo S, Cantón Y, Miralles I, Domingo F (2012) Biological soil crust development affects physicochemical characteristics of soil surface in semiarid ecosystems. Soil Biol Biochem 49:96–105CrossRefGoogle Scholar
  11. Chilton AM, Neilan BA, Eldridge DJ (2017) Biocrust morphology is linked to marked differences in microbial community composition. Plant Soil.
  12. Chittapun S, Limbipichai S, Amnuaysin N, Boonkerd R, Charoensook M (2017) Effects of using cyanobacteria and fertilizer on growth and yield of rice, Pathum Thani I: a pot experiment. J Appl Phycol.
  13. Commander LE, Golos PJ, Miller BP, Merritt DJ (2017) Seed germination traits of desert perennials. Plant Ecol 218:1077–1091CrossRefGoogle Scholar
  14. Debez A, Ben Hamed K, Grignon C et al (2004) Salinity effects on germination, growth, and seed production of the halophyte Cakile Maritima. Plant Soil 262:179–189CrossRefGoogle Scholar
  15. Elliott DR, Thomas AD, Hoon SR, Sen R (2014) Niche partitioning of bacterial communities in biological crusts and soils under grasses, shrubs and trees in the Kalahari. Biodivers Conserv 23:1709–1733CrossRefGoogle Scholar
  16. Erickson TE, Barrett RL, Symons DR, Turner SR, Merritt DJ (2016) An atlas to the plants and seeds of the Pilbara region. In: Erickson TE, Barrett RL, Merritt DJ, Dixon KW (eds) Pilbara seed atlas and field guide: plant restoration in Australia's arid northwest. CSIRO Publishing, Dickson, pp 43–256Google Scholar
  17. Erickson TE, Muñoz-Rojas M, Kildisheva OA, Stokes BA, White SA, Heyes JL, Dalziell EL, Lewandrowski W, James JJ, Madsen MD, Turner SR, Merritt DJ (2017) Benefits of adopting seed-based technologies for rehabilitation in the mining sector: a Pilbara perspective. Aust J Bot 65:646. CrossRefGoogle Scholar
  18. Escudero A, de la Martínez I, Cruz A, Otáora MAG, Maestre FT (2007) Soil lichens have species-specific effects on the seedling emergence of three gypsophile plant species. J Arid Environ 70:18–28CrossRefGoogle Scholar
  19. Garcia-Pichel F, Prufert-Bebout L, Muyzer G (1996) Phenotypic and phylogenetic analyses show Microcoleus Chthonoplastes to be a cosmopolitan cyanobacterium. Appl Environ Microbiol 62:3284–3291PubMedPubMedCentralGoogle Scholar
  20. Garcia-Pichel F, Loza V, Marusenko Y, Mateo P, Potrafka RM (2013) Temperature drives the continental-scale distribution of key microbes in topsoil communities. Science 340:1574–1577CrossRefPubMedGoogle Scholar
  21. George B, Pancha I, Desai C, Chokshi K, Paliwal C, Ghosh T, Mishra S (2014) Effects of different media composition, light intensity and photoperiod on morphology and physiology of freshwater microalgae Ankistrodesmus falcatus – a potential strain for bio-fuel production. Bioresour Technol 17:1367–1374Google Scholar
  22. Hosseini M, Powell A, Bingham I (2002) Comparison of the seed germination and early seedling growth of soybean in saline conditions. Seed Sci Res 12(3):165–172. CrossRefGoogle Scholar
  23. Jiménez-Alfaro B, Silveira FAO, Fidelis A, Poschlod P, Commander LE (2016) Seed germination traits can contribute better to plant community ecology. J Veg Sci 27:637–645. CrossRefGoogle Scholar
  24. Keesstra S, Nunes J, Novara A, Finger AD, Kalantari Z, Cerdà A (2018) The superior effect of nature based solutions in land management for enhancing ecosystem services. Sci Total Environ 610:997–1009. CrossRefPubMedGoogle Scholar
  25. Kim S, Rayburn AL, Voigt T, Parrish A, Lee DK (2012) Salinity effects on germination and plant growth of prairie cordgrass and switchgrass. Bioenerg Res 5:225–235. CrossRefGoogle Scholar
  26. Kneller T, Harris R, Bateman A, Muñoz-Rojas M (2018) Native-plant amendments and topsoil addition to enhance soil quality in post-mining arid grasslands. Sci Total Environ 621:744–752. CrossRefPubMedGoogle Scholar
  27. Larson JE, Funk JL (2016) Regeneration: an overlooked aspect of trait-based plant community assembly models. J Ecol 104:1284–1298CrossRefGoogle Scholar
  28. Liu R, Li K, Zhang H, Zhu J, Joshi D (2014) Spatial distribution of microbial communities associated with dune landform in the Gurbantunggut Desert, China. J. Microbiol 52(11):898–907CrossRefPubMedGoogle Scholar
  29. McDonald D, Price MN, Goodrich J, Nawrocki EP, DeSantis TZ, Probst A et al (2012) An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J 6:610–618CrossRefPubMedGoogle Scholar
  30. Miller BP, Sinclair EA, Menz MHM, Elliott CP, Bunn E, Commander LE, Dalziell E, David E, Davis B, Erickson TE, Golos PJ, Krauss SL, Lewandrowski W, Mayence CE, Merino-Martín L, Merritt DJ, Nevill PG, Phillips RD, Ritchie AL, Ruoss S, Stevens JC (2017) A framework for the practical science necessary to restore sustainable, resilient, and biodiverse ecosystems. Restor Ecol 25(4):605–617CrossRefGoogle Scholar
  31. Muñoz-Rojas M, Erickson TE, Martini DC, Dixon KW, Merritt DJ (2016a) Climate and soil factors influencing seedling recruitment of plant species used for dryland restoration. Soil 2:287–298. CrossRefGoogle Scholar
  32. Muñoz-Rojas M, Erickson TE, Dixon KW, Merritt DJ (2016b) Soil quality indicators to assess functionality of restored soils in degraded semiarid ecosystems. Restor Ecol 24:S43–S52CrossRefGoogle Scholar
  33. Nunes da Rocha U, Cadillo-Quiroz H, Karaoz U, Rajeev L, Klitgord N, Dunn S, Truong V, Buenrostro M, Bowen BP, Garcia-Pichel F, Mukhopadhyay A, Northen TR, Brodie EL (2015) Isolation of a significant fraction of non-phototroph diversity from a desert biological soil crust. Front Microbiol 6:277CrossRefPubMedPubMedCentralGoogle Scholar
  34. O’Callaghan M (2016) Microbial inoculation of seed for improved crop performance: issues and opportunities. Appl Microbiol Biotechnol 100:5729–5746CrossRefPubMedPubMedCentralGoogle Scholar
  35. Ooi MKJ (2007) Dormancy classification and potential dormancy-breaking cues for shrub species from fire-prone south-eastern Australia. In: Adkin S, Ashmore S, Navie SC (eds) Seeds: biology, development and ecology. CABI, Wallingford, pp 205–216Google Scholar
  36. Ooi MKJ, Auld TD, Whelan RJ (2004) Comparison of the cut and tetrazolium tests for assessing seed viability: a study using Australian native Leucopogon species. Ecol Manag Restor 5:141–143CrossRefGoogle Scholar
  37. Ooi MKJ, Auld TD, Denham AJ (2009) Climate change and bet-hedging: interactions between increased soil temperatures and seed bank persistence. Glob Chang Biol 15:2375–2386CrossRefGoogle Scholar
  38. Park C-H, Li XR, Zhao Y, Jia RL, Hur J-S (2017) Rapid development of cyanobacterial crust in the field for combating desertification. PLoS One 12(6):e0179903. CrossRefPubMedPubMedCentralGoogle Scholar
  39. Parsons RF (2012) Incidence and ecology of very fast germination. Seed Sci Res 22:161–167CrossRefGoogle Scholar
  40. Perring MP, Standish RJ, Price JN, Craig MD, Erickson TE, Ruthrof KX, Whiteley AS, Valentine LE, Hobbs RJ (2015) Advances in restoration ecology: rising to the challenges of the coming decades. Ecosphere 6(8):art131CrossRefGoogle Scholar
  41. Pointing SB, Belnap J (2012) Microbial colonization and controls in dryland systems. Nat Rev Microbiol 10(8):551–562CrossRefPubMedGoogle Scholar
  42. R Core Team 2017 R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. Accessed 25 Oct 2017
  43. Rehman S, Harris PJC, Bourne WF, Wilkin J (2000) The relationship between ions, vigour and salinity tolerance of acacia seeds. Plant Soil 220:229–233CrossRefGoogle Scholar
  44. Rippka R (1988) Isolation and purification of cyanobacteria. Methods Enzymol 167:3–27CrossRefPubMedGoogle Scholar
  45. Ritz C, Streibig JC (2005) Bioassay analysis using R. J Stat Softw 12:1–22CrossRefGoogle Scholar
  46. Rossi F, Li H, Liu Y, De Philippis R (2017) Cyanobacterial inoculation (cyanobacterisation): perspectives for the development of a standardized multifunctional technology for soil fertilization and desertification reversal. Earth Sci Rev 171:28–43CrossRefGoogle Scholar
  47. Schloss PD, Gevers D, Westcott SL (2011) Reducing the effects of PCR amplification and sequencing artifacts on 16S rRNA-based studies. PLoS One 6:e27310CrossRefPubMedPubMedCentralGoogle Scholar
  48. Singh JS, Kumar A, Rai AN, Singh DP (2016) Cyanobacteria: a precious bioresource in agriculture, ecosystem, and environmental sustainability. Front Microbiol 7:1–9Google Scholar
  49. Song G, Li X, Hui R (2017) Effect of biological soil crusts on seed germination and growth of an exotic and two native plant species in an arid ecosystem. PLoS One 12(10):e0185839CrossRefPubMedPubMedCentralGoogle Scholar
  50. Su YG, Li XR, Zheng JG, Huang G (2009) The effect of biological soil crusts of different successional stages and conditions on the germination of seeds of three desert plants. J Arid Environ 73:931–936CrossRefGoogle Scholar
  51. Velasco Ayuso S, Giraldo Silva A, Nelson CJ, Barger NN, Garcia-Pichel F (2016) Microbial nursery production of high-quality biological soil crust biomass for restoration of degraded dryland soils. Appl Environ Microbiol 83:e02179–e02116. CrossRefGoogle Scholar
  52. Wang W, Liu Y, Li D, Hu C, Rao B (2009) Feasibility of cyanobacterial inoculation for biological soil crusts formation in desert area. Soil Biol Biochem 41:926–929CrossRefGoogle Scholar
  53. Williams WJ, Büdel B, Reichenberger H, Rose N (2014) Cyanobacteria in the Australian northern savannah detect the difference between intermittent dry season and wet season rain. Biodivers Conserv 23:1827–1184CrossRefGoogle Scholar
  54. Xu Y, Rossi F, Colica G, Deng S, Philippis RD, Chen L (2013) Use of cyanobacterial polysaccharides to promote shrub performances in desert soils: a potential approach for the restoration of desertified areas. Biol Fertil Soils 49:143–152CrossRefGoogle Scholar
  55. Zaady E, Gutterman Y, Boeken B (1997) The germination of mucilaginous seeds of Plantago Coronopus, Reboudia pinnata, and Carrichtera Annua on cyanobacterial soil crust from the Negev Desert. Plant Soil 190:247–252CrossRefGoogle Scholar
  56. Zhang YM, Belnap J (2015) Growth responses of five desert plants as influenced by biological soil crusts from a temperate desert, China. Ecol Res 30:1037–1045CrossRefGoogle Scholar
  57. Zhang Y, Aradottir AL, Serpe M (2016) Interactions of biological soil crusts with vascular plants. Biological Soil Crusts: An Organizing Principle in Drylands. Springer International Publishing, Switzerland, pp 385–406CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • M. Muñoz-Rojas
    • 1
    • 2
    • 3
    Email author
  • A. Chilton
    • 4
  • G. S. Liyanage
    • 3
  • T. E. Erickson
    • 1
    • 2
  • D. J. Merritt
    • 1
    • 2
  • B. A. Neilan
    • 4
    • 5
  • M. K. J. Ooi
    • 3
  1. 1.School of Biological SciencesThe University of Western AustraliaCrawleyAustralia
  2. 2.Kings Park Science, Department of BiodiversityConservation and AttractionsKings ParkAustralia
  3. 3.Centre for Ecosystem Science, School of Biological, Earth & Environmental SciencesUniversity of New South WalesSydneyAustralia
  4. 4.Australian Centre for Astrobiology and School of Biotechnology and Biomolecular SciencesUniversity of New South WalesSydneyAustralia
  5. 5.School of Environmental and Life SciencesUniversity of NewcastleCallaghanAustralia

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