A propagation technique for native tundra bryophytes for Arctic ecosystem restoration
Abstract
Extreme environmental conditions and limited understanding of ecosystem processes and community dynamics pose significant challenges for Arctic ecosystem restoration activities. As pioneer species, bryophytes are critical to the function and structure of northern ecosystems and play an important role in facilitating soil and microhabitat development. A total of 11 bryophytes species were collected from a mixed community near Lac de Gras in the Northwest Territories, Canada, and a 12 week laboratory study was conducted. Three propagule types (large = 2.1–40 mm, medium = 1.0–2 mm, and small = <1 mm phyllids) and three slurries (distilled water, beer, and buttermilk) were used to determine effective bryophyte propagation techniques and slurries for species introduction in Arctic restoration sites. Medium-size fragments were more effective than large or small for propagating bryophytes as they led to greater bryophyte plant count and cover. Water and beer were more effective than buttermilk, although their effects decreased after 12 weeks. Bryum pseudotriquetrum Hedw. was the most abundant species propagated, followed by Aulacomnium turgidum (Wahlenb.) Schwägr. and Ceratodon purpureus (Hedw.) Brid. This study suggests that propagation with medium-size fragments and distilled water would be most efficient for field application in Arctic ecosystem restoration if bryophyte revegetation is a focus.
Introduction
Arctic ecosystems are characterized by extreme conditions with low air and soil temperatures, low soil water content, shallow depth to thaw, nutrient deficiencies, and short growing seasons (Lewis et al. 2017; Lett et al. 2022) which are further exacerbated by mining activities (Miller et al. 2021; Dhar et al. 2022). Extreme environmental conditions and a limited understanding of northern ecosystem processes and community dynamics impede restoration (Forbes and McKendrick 2002; Hnatowich et al. 2022). In many tundra ecosystems, bryophytes contribute a greater portion (>50%) of primary production and standing biomass (Huemmrich et al. 2010) and play important roles in soil hydrology, biogeochemical cycling, surface energy balance, and species diversity (e.g., Lindo and Gonzalez 2010; Turetsky et al. 2012), thus effectively promoting their growth is critical for restoration. Despite their major role in ecosystem function and structure, there is a lack of research on how to establish bryophytes in tundra ecosystems after disturbances.
Bryophytes are capable of both sexual and asexual reproduction where cutting of fragments is a common method of vegetative propagation (Hugonnot and Celle 2012; Ónody et al. 2016; Maciel-Silva 2017). A high rate of regeneration from fragments allows for easy and fast vegetative propagation (La Farge et al. 2013; Ónody et al. 2016). Fragment size varies with method, as it does naturally with species and environmental conditions. Propagules can be reduced to small (<1 mm), dust-sized particles, by pulverizing or blending (Schenk 1997; McDonough 2006). Grating material through a mesh sieve can produce medium (1–2 mm), phyllid fragments (Schenk 1997; Jones and Rosentreter 2006) which approximates multicellular fragments, can be easily transported by wind and known to propagate, such as detached (Giordano et al. 1996; Hugonnot and Celle 2012) or wounded leaves (Gemmell 1953). Larger fragments (2–40 mm) approximate whole or partial plants translocated by soil or water movement or transportation on another living organism. Large fragments can be produced by manually breaking dried material (Aradóttir 2012; Lamarre et al. 2023) or clipping to a standard length (Graf and Rochefort 2010). Although propagation with phyllid fragments and sizes promoted bryophyte growth in other regions (Wilmot-Dear 1980; Giordano et al. 1996; Hugonnot and Celle 2012; Ónody et al. 2016), little research comparing the effectiveness of fragment size has been conducted for tundra bryophytes.
Slurries can promote regeneration and/or fastening of fragmented bryophyte material to substrates. Numerous slurry preparation methods have been suggested, including mixes of bryophyte material with soil, distilled water, fertilizer, epoxy resin, tackifiers, and/or household materials such as beer, buttermilk, compost, and manure (Schenk 1997; Buxton et al. 2005; Ónody et al. 2016; Glime 2017; Blankenship et al. 2020). Although most common slurries include a combination of water, beer, and buttermilk or yogurt, no rigorous testing of slurries for tundra bryophytes propagation has been conducted.
The science of reintroduction of bryophyte species to disturbed lands is relatively novel (Antoninka et al. 2020). A deeper understanding of growth of specific individual species is necessary for restoration of disturbed tundra ecosystems (Cargill and Chapin 1987; Lamarre et al. 2023). Therefore, a 12 week laboratory-based study using three bryophyte slurries (water, beer, and buttermilk) was conducted to determine effectiveness of three fragment sizes (small, medium, and large) to facilitate revegetation of selected bryophyte species in Arctic reclamation sites. The outcome of this study will help to select fragment sizes and slurries for field application.
Materials and methods
Collection and identification
Native tundra bryophyte samples were collected in fall from natural areas near Diavik Diamond Mine (64°49′N and 110°27′W), approximately 320 km northeast of Yellowknife in the Northwest Territories, Canada, and approximately 100 km north of the treeline. Collection microsites were randomly selected to cover a variety of hydrologic regimes, soils, and plant communities as sample homogeneity and species composition varied with microhabitat properties. However, these microsite properties were not considered or evaluated for experimental design or interpretation of results. These microsite descriptions were incorporated for information only. Fist-sized bunches of bryophytes were separated and pulled by hand from substrates or surrounding vegetation and deposited into paper bags labeled with microsite type and description. Samples were transported to the University of Alberta for identification.
During identification and sorting, samples were rehydrated with a distilled water dilution of the surfactant Aerosol OT (sodium bis(2-ethylhexyl) sulfosuccinate) (Prof. Dr. René Belland, University of Alberta, Edmonton, Alberta (personal communication, 2014)). Bryophytes were identified according to Crum (2004) and Atherton et al. (2010), with assistance from Dr. René Belland. Species were sorted and air dried in open trays on a laboratory bench for 3 days, until a constant weight was achieved, prior to experimental applications. The final dry weight of each species was determined for a general estimate of initial abundance. The most common 11 bryophytes species from the collected sample were identified and selected for this study—Aulacomnium turgidum (Wahlenb.) Schwägr., Cephalozia sp., Ceratodon purpureus (Hedw.) Brid., Cynodontium alpestre (Wahlenb.) Milde, Funaria hygrometrica Hedw., Pohlia sp., Polytrichum juniperinum Hedw., Polytrichum strictum Bridel, J. Bot. (Schrader), Ptilidium ciliare (L.) Hampe, Racomitrium lanuginosum (Hedw.) Brid., and Tetralophozia setiformis (Ehrh.) Schljak. (Table 1).
Table 1.
Treatments, experimental design, and laboratory procedures
A 12 week laboratory experiment using three fragment sizes (small, medium, and large) of bryophyte material and three liquids (distilled water, beer, and buttermilk) to create bryophyte slurries in a randomized block design was conducted to evaluate growth potential of selected bryophyte species. Large bryophyte fragments (2.1–40.0 mm) were separated by hand from entire individual plants, medium fragments (1.1–2.0 mm) were created by sifting plant material through a 1.0 mm soil sieve, while small fragments (<1 mm) were produced by grinding dried samples in a standard handheld electric coffee grinder. The three liquids were selected based on previous bryophyte propagation studies (Schenk 1997; Smith 2012; Ónody et al. 2016; Glime 2017). The beer was unpasteurized, contained no preservatives, and was made from organic malts with pH 4 and 5% alcohol content. Buttermilk sourced from a local grocery store contained 3.3% fat with pH 4.3. Distilled water with pH 6.3 was sourced from the University of Alberta laboratory. They were inexpensive, easy to purchase, and if purchased, were abundant in markets.
Before creating the slurry, an equal amount of dried biomass of each of the 11 bryophytes was mixed together based on fragment-size categories. Slurries were made by hand mixing 2.0 g of bryophytes with 50.0 mL distilled water and 50.0 mL of either beer, buttermilk, or more distilled water, using glass beakers and stir sticks. Slurries were allowed to stand for a minimum of 5 min to rehydrate the desiccated bryophytes and slurries were applied to plastic sponges (11 × 9 cm) overlaid with a double layer of natural, white, 100% cotton, 1.0 mm2 mesh cheesecloth (20 threads per inch). Erosion control is likely to be essential for retaining bryophyte fragments in the windswept tundra. Commonly employed straw and coconut mats are too thick for bryophytes to emerge through, therefore cheesecloth can provide an alternative (faster decomposition, weed-free, and cost-effective) for northern reclamation. Several other studies used cheesecloth for bryophyte revegetation (McDowell 1972; Schenk 1997; Glime 2017) or as erosion control in Arctic tundra, as cheesecloth is lightweight, low bulk, costs less than comparable reclamation materials, and degrades quickly. McDowell (1972) suggested revegetation using cheesecloth as it can easily be rolled and transferred to the field during reclamation activities. The cheesecloth was fastened to the sponge at each of its four corners using plastic toothpicks. The damp sponges and cheesecloth stood in open trays of distilled water, at an ambient temperature of approximately 23.0 °C. Bryophyte slurries were poured onto the cheesecloth in a circular 7.5 cm diameter metal frame to concentrate their location. Each of the sponges received a single slurry. There were 45 experimental units consisting of 3 slurry materials × 3 fragment sizes × 5 replicates. Replicates and fragment sizes were randomized in trays of designated slurry composition to avoid contamination, for a total of nine trays, three per slurry treatment. It is always difficult to mimic the Arctic conditions in a laboratory setting, therefore, constant 24 h light (fluorescent) and 23 °C temperature over 12 weeks may not fully represent the Arctic conditions.
To minimize the potential limiting factors, sponges were misted with distilled water twice weekly and were injected with distilled water, using a 500.0 mL squirt bottle, when dry. Trays were covered with clear plastic lids for 2 days. Replicates with mold were treated with a distilled water dilution (50%) fungicide of 0.3% potassium salts and 0.2% sulfur on day 4 of the experiment. Fuzzy white growth immediately receded in some replicates but persisted in all buttermilk and some beer replicates for the duration of the experiment. Fungicide application was halted after 1 month when most of the mold growth had receded, as it had a desiccating effect on sponges and to limit its potentially harmful effects on bryophyte growth. The duration of the experiment was 12 weeks.
Vegetation assessments
Percent cover and count of live bryophytes (green and/or regenerating gametophyte fragments) were visually estimated separately within and outside the circular frame weekly. Cover estimates to the closest percent were calibrated to a visual guide. The individuals that were counted in weeks 2–10 were not identified to species, however, at week 12 individuals were identified to species. Weekly counts of individuals per sponge was determined separately inside and outside the circular frame using a magnifying lamp and click counter. After 12 weeks, species that regenerated inside and outside the circular frame were identified (Crum 2004; Atherton et al. 2010) and counted. Species counts were approximate, as plants were often small and growing in compact mats. Although weight of individual species would have been desirable, it was not taken at the end of the experiment due to difficulty in removing plants from the degrading cheesecloth.
Statistical analyses
A permutational two-way analysis of variance (permANOVA) was performed in R (R Core Team 2021) to examine the influence of independent variables (size and slurry and their interaction) on dependent variables (cover and count). To raise confidence in the significance of permutational output, tests that were not strongly significant were run 10 times, and the most common output was selected. Significance was accepted at p < 0.05. One PermANOVA was conducted for all weeks combined and separate analyses were repeated for every week to determine if statistical significance increased or decreased with time. Boxplots and Shapiro–Wilk’s tests were used to assess normality. Data transformations, including square root, log, and inversion, were performed, but failed to achieve normality; therefore permutational analyses were conducted. Results from week 12, the end of the experiment, were different from all weeks combined, therefore both are discussed. A Tukey’s multiple comparison was conducted to evaluate significance of differences between sizes and slurries at week 12.
Results
Treatment effects on cover and plant count
Fragment size and slurry types significantly affected overall plant live cover (p < 0.001) and count (individual number) (p < 0.001). Medium fragments had a higher live cover and count than small or large fragments; buttermilk had a lower cover and count than beer or water (Fig. 1). All sizes and slurries were statistically distinct and no interaction effects occurred for live cover and bryophyte count. However, after 12 weeks only size (p = 0.007) on live cover and both size (p = 0.006) and slurry (p = 0.004) showed a significant effect on count. Medium-size fragments had a significantly (p = 0.005) greater live cover than large fragments whereas no differences were found with small fragments (Fig. 2a). Beer had the highest plant count, followed by water and buttermilk (Fig. 2b). Overall, beer and water were statistically distinct from buttermilk, but did not differ from each other. Buttermilk was the only slurry that differed significantly (p < 0.001) from beer and water at the end of the experiment ( Fig. 2b).
Fig. 1.
Fig. 2.
Treatment effects on species
After 12 weeks, a new species Bryum pseudotriquetrum Hedw., tiny unidentifiable bryophytes or phytomere and protonemal growth dominated the vegetation regardless of treatment. Abundance of most species was low and approximately half of the planted species propagated by week 12. Total plant count in all fragment size and slurry treatments were highest for Bryum pseudotriquetrum (1328) and Aulacomnium turgidum(245), followed by Ceratodon purpureus(199), Ptilidium ciliare(19), Polytrichum strictum(18), Tetralophozia setformis(4), and Funaria hygrometrica(1). Four planted species, Cephalozia sp., Cynodontium alpestre, Pohlia sp., and Racomitrium lanuginosum, were not found at the end of experiment. Approximately 1345 (∼30% of total) unknown individuals were too small to identify. Protonemal growth dominated the bare cloth outside the circular frame, on sponge edges, and was found in all treatments. Edge protonemal growth was highest in buttermilk with medium (41.0% mean live cover) and large fragments (17.8%), and in beer with medium fragments (6.4%). Protonemal growth in the planted area was also highest on buttermilk (medium 67.4%, small 20.0%, large 8.0%). Bryum pseudotriquetrum and protonemal showed extended growth to the edges of the sponges. This occurred mainly on buttermilk, where 749 individuals were counted. No individuals were counted outside the main planted area of sponges with only distilled water, and only 35 were found on beer sponges. Unidentifiable protonema were found on almost all outer sponge edges and inside planted areas, in all treatments.
Discussion
This study revealed that slurries may be more important for initial propagation even though their effect is neutralized after 12 weeks. The pH of the slurry types did not influence the propagation, as beer was the most acidic, followed by buttermilk, and distilled water. Slower propagation of bryophytes on buttermilk slurries may be related to the fungal growth that affected buttermilk, the fungicide used to treat it, and/or chemical composition of buttermilk. The increase in bryophyte counts with buttermilk around week 10 could be due to dilution and leaching of buttermilk and fungicide and/or a delayed growth after mold was reduced. Mixed results were reported by some studies when buttermilk was used as a slurry for moss revegetation (Ónody et al. 2016; Glime 2017) and suggested a 1:7 buttermilk and water solution could provide better performance during spring.
Greater count and live cover with medium size fragments relative to small or large are likely due their (medium size fragments) most closely resemblance to the size of plant parts that naturally occur with bryophytes, many of which propagated from phyllid or stem pieces (Ónody et al. 2016; Glime 2017). The biological potential for growth of detached leaves and stem apices is well known, with many species relying primarily on this method for regeneration (Longton and Greene 1979; Robinson and Miller 2013). Small pieces may not have had enough stored energy for propagation, with stress of desiccation and fragmentation intolerable. The large fragments had slow rates of regeneration, possibly due to elevated desiccation stress or energy requirement in supporting the entire plant. However, the hydrologic and atmospheric conditions in the laboratory were different from natural tundra. Higher temperatures, no water deficits, and lack of wind likely had a beneficial effect on bryophyte regeneration and thus results may be more optimistic than the field.
When considering treatment effect on species level, Bryum pseudotriquetrum and protonemal growth extended to the edges of the sponges, likely due to the effect of water runoff from the main sponge area, which pooled around the plastic toothpicks in the corners. Growth on outer edges of sponges around toothpicks often surpassed growth on the planted area. Species that propagated were likely adapted to the hydrologic, light, and temperature conditions in the laboratory and propagated from fragments or regenerated from entire stems. Aulacomnium turgidum (245 count) likely propagates preferentially through fragmentation or branching, as it is rarely seen with capsules (Atherton et al. 2010). Ceratodon purpureus(199 count) is a common colonizer, known to be tolerant of sterile or disturbed substrates (Crum 2004). Bryum pseudotriquetrum (1328 count or 29% of total) was not found in the initial assessment of vegetation prior to slurry mixing. It may have been present in a limited number of stems or a form that was too small to be detected as it is very small—plants, fragments, or spores. Bryum pseudotriquetrum is a common marsh species and can be found in most wide-ranging disturbance sites (Crum 2004), therefore, it was likely well adapted to the hydrologic condition of the sponges.
Spread of protonemal material to depressions is of significant importance in field reclamation. Fragments that are carried by runoff have potential to be more productive than directly deposited material, which may die or be blown away, particularly in northern environments with high speed and frequent wind (Forbes and McKendrick 2002; Hnatowich et al. 2022). Promoting and accounting for mobility of planted bryophyte material could be an important consideration for field application. Since materials will likely be transported by precipitation or wind to microdepressions, creating a substrate surface that is heterogeneous would likely be beneficial for formation of small bryophyte islands. On a long-term scale, applying any of the three fragmentation methods would likely be beneficial for bryophyte propagation; however, medium size could provide better outcome. When considering field application, rapid establishment and growth are critical factors in preventing water runoff and wind erosion of bare substrates. Hydrologic and atmospheric conditions in the laboratory were ideal relative to a field setting, thus 12 weeks in the laboratory may be equivalent to many months or years in the field, and the short-term benefits provided by fragmentation in the laboratory could have important consequences on first few growing seasons of revegetation.
Implications in Arctic restoration
The outcomes of this laboratory experiment have significant potential implications on reintroduction of bryophytes into disturbed Arctic sites. Application of the fragmentation methods assessed in this study are supported by their simplicity and effectiveness for short-term bryophyte establishment in a field as rapid establishment of vegetative cover is of primary importance for erosion-prone Arctic conditions. This study suggests rough hand pulverization may be useful for stimulating bryophyte propagation and can be applied during Arctic restoration. Our results support those of others in that laboratory growth is a plausible method of revegetating bryophytes; however, the use of food products in a field setting is impractical due to transportation cost and potential attraction to wildlife, potentially disturbing the fragile site, and endangering workers. Since water and beer did not differ significantly in this experiment, water is recommended for large-scale field application. Instead of distilled water, rain water or other water sources can be used in Arctic ecosystem restoration following disturbances. Cheesecloth has great potential for use as an erosion control material in northern ecosystems which can minimize fluctuations in soil water content and temperature and promote the most bryophyte colonization.
Conclusion
In this study, medium-size fragments (1.0–2.0 mm) were more effective than large or small fragments for propagating bryophytes over 12 weeks. Distilled water and beer were both effective at short-term propagation of bryophytes, although water could be more efficient for field application. After 12 weeks, the effects of slurries were decreasing. In this condition, Bryum pseudotriquetrum was the most abundant species propagated, followed by Aulacomnium turgidum and Ceratodon purpureus. We conclude that water is the best liquid for bryophyte slurries, as it is easy to use, low cost, and readily available; medium-sized fragments performed the best. These techniques are ready to be tested in the field to enhance water capture for reintroduction of bryophytes into disturbed Arctic sites.
Acknowledgements
We thank the Environment Department of Diavik Diamond Mine, for logistical support and site information.
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Information & Authors
Information
Published In
Arctic Science
Volume 9 • Number 3 • September 2023
Pages: 743 - 749
History
Received: 8 November 2022
Accepted: 12 April 2023
Accepted manuscript online: 19 May 2023
Version of record online: 19 June 2023
Copyright
© 2023 The Author(s). This work is licensed under a Creative Commons Attribution 4.0 International License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author(s) and source are credited.
Data Availability Statement
The data presented in this study may be available on request from the corresponding author. The data are not publicly available due to copyright issues.
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Authors
Author Contributions
Conceptualization: MAN
Data curation: JJML
Formal analysis: JJML, AD
Funding acquisition: MAN
Writing – original draft: AD
Writing – review & editing: AD, MAN
Competing Interests
The authors declare there are no competing interests.
Funding Information
This work was supported by the Diavik Diamond Mine under grant number RES0018011.
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Jasmine J.M. Lamarre, Amalesh Dhar, and M. Anne Naeth. 2023. A propagation technique for native tundra bryophytes for Arctic ecosystem restoration. Arctic Science.
9(3): 743-749. https://doi.org/10.1139/as-2022-0046
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