Author
Results
Discussion
References
For further details log on website :
http://link.springer.com/article/10.1007/s11056-015-9491-7
We searched peer-reviewed literature published through Oct. 2014 to locate studies presenting growth responses of trees to biochar additions: we conducted searchers using Google Scholar (scholar.google.com) and Web of Science (thomasonreuters.com) databases using the search terms “biochar”, “char”, “charcoal”, and “black carbon”, and in addition consulted recent meta-analyses and reviews (in particular Spokas et al. 2012, Biederman and Harpole 2013; Liu et al. 2013; Stavi 2013). We included all studies based on woody plant species that presented mean responses for aboveground biomass, or for both height and stem diameter. We only considered studies specifically examining responses to chars, and not wood ash, except cases of high-carbon wood ash with organic matter >30 %. Where data were only available in graphical format, figures were scanned and digitized. We located a total of 17 studies examining responses of 36 woody plant species (Table 1).
Table 1
Studies included in meta-analysis of woody plant growth responses to biochar additions
Region
|
Country
|
Type
|
Duration (d)
|
Feedstock
|
Temp. (°C)
|
Dosage
|
Nspp
|
Ncomp
|
Reference
|
---|---|---|---|---|---|---|---|---|---|
Tropical
|
Indonesia
|
pot
|
84
|
NA
|
NA
|
5–15 %
|
1
|
12
|
Budi and Setyaningsih (2013)
|
Tropical
|
Zambia
|
pot
|
93
|
NA
|
NA
|
NA
|
7
|
7
|
Chidumayo (1994)
|
Temperate
|
Tasmania
|
field
|
821
|
Wood (Acacia)
|
550
|
47 t/ha
|
1
|
8
|
Eyles et al. (2013)
|
Tropical
|
Nigeria
|
pot
|
84
|
Wood
|
~350
|
5–20 t/ha
|
1
|
12
|
Fagbenro et al. (2013)
|
Tropical
|
Singapore
|
pot
|
180
|
NA
|
NA
|
25 %
|
2
|
6
|
Ghosh et al. (2015)
|
Temperate
|
USA
|
pot
|
49
|
Wood (Quercus)
|
500a
|
25 %
|
1
|
6
|
Headlee et al. (2014)
|
Boreal
|
Finland
|
pot
|
63
|
Wood (Picea/Pinus)
|
NAa
|
15–60 %
|
1
|
16
|
Heiskanen et al. (2013)
|
Temperate
|
Japan
|
pot
|
120
|
Mixed
|
NA
|
20 %
|
1
|
9
|
Makoto et al. (2010)
|
Temperate
|
USA
|
pot
|
56
|
Wood
|
NAa
|
25–50 t/ha
|
1
|
4
|
McElligott (2011)
|
Temperate
|
Spain
|
field
|
584
|
Wood
|
NAb
|
5–14 t/ha
|
1
|
30
|
Omil et al. (2013)
|
Boreal
|
Sweden
|
pot
|
70
|
Wood (various)
|
450
|
30 t/ha
|
4
|
216
|
Pluchon et al. (2014)
|
Boreal
|
Australia
|
pot
|
180
|
Wood (Eucalyptus)
|
700
|
37–74 t/ha
|
1
|
4
|
Reverchon et al. (2014)
|
Boreal
|
Canada
|
pot
|
102
|
Wood (Pinus)
|
410
|
4–7 t/ha
|
2
|
5
|
Robertson et al. (2012)
|
Temperate
|
USA
|
pot
|
548
|
Wood (Pinus)
|
550–600
|
25 t/ha
|
2
|
8
|
Scharenbroch et al. (2013)
|
Tropical
|
Indonesia
|
pot
|
167
|
NA
|
NA
|
10–20 %
|
2
|
41
|
Siregar (2007)
|
Tropical
|
Laos
|
field
|
1460
|
Rice hulls
|
NA
|
4 t/ha
|
8
|
24
|
Sovu et al. (2012)
|
Boreal
|
Sweden
|
pot
|
57
|
Wood (Empetrum)
|
450
|
20 t/ha
|
2
|
12
|
Wardle et al. (1998)
|
Growth responses were quantified as either aboveground or total biomass where these data were directly presented. In cases where stem diameter (d) and height (h) measures only were reported, we utilized d2h as a proxy measure for biomass. Following the precedent of recent meta-analyses of crop responses (Biederman and Harpole 2013; Liu et al. 2013), we utilized the log-transformed biomass response ratio as an effect size metric: RR = ln(B/C), where RR is the response ratio metric, B is mean biomass of biochar-treated trees, and C is mean biomass in control trees without biochar additions. In studies presenting data on responses to multiple biochar treatments (i.e., different dosages, biochar sources, or soil conditions) we treated each treatment type as a separate meta-analytic observation. We employed a paired non-parametric Wilcoxon test to detect positive responses, considering tests significant at P < 0.05. Non-paired Wilcoxon test were used to compare responses between groups. Analyses were conducted in the statistical software R version 3.1.0 (R Core Team 2012).
Results
Publications included in the meta-analysis indicate a consistent and strong overall pattern of positive growth responses to biochar additions among woody plants (Figs. 1, 2). The mean response ratio metric for the entire data set was 0.347 ± 0.046 (P < 0.001), corresponding to a 41 % increase in biomass in response to biochar additions. For all subgroups compared (Fig. 1), response ratio metrics likewise were significantly greater than zero (at P < 0.05). Responses of both tropical and boreal trees were larger than those observed for temperate tree species (P < 0.01 in both cases), but tropical and boreal responses were similar (Fig. 1a). Responses of hardwoods (angiosperms) were on average considerably greater than those of conifers (P < 0.001: Fig. 1b). In terms of study type, there were not detectable differences in response between pot trials (including greenhouse and growth chamber studies as well as shadehouse and similar studies with growth containers) and field trials with trees planted in native soils (P > 0.05: Fig. 1c). There were not detectable differences in responses relative to duration of study (P > 0.05: Fig. 1d); however, there was a trend toward shorter-term studies showing larger responses, and the pairwise comparison between medium-term studies (6–12 months) and long-term studies (>12 months) was marginally significant (P = 0.098).
Considering tree species with a relatively large number of trials represented in the data set (N ≥ 3), there was very high apparent variation in responses among species (Fig. 2). Response ratio metrics were positive in all cases, but varied from ~0.05 to 0.75. Species-specific responses were significant (by the conservative Wilcoxon test used) in 5 of 14 cases (Fig. 2).
Discussion
Prior meta-analyses for plant responses to char have essentially only examined data on agronomic crops (Jeffery et al. 2011; Biederman and Harpole 2013; Crane-Droesch et al. 2013; Liu et al. 2013). Our results strongly support the contention that trees in general show strong positive growth responses to biochar in a range of ecological systems and soil conditions. Indeed, the mean response ratio metric (response ratio metric of 0.347 ± 0.046, or a 41 % increase in biomass) is considerably higher than that found in prior meta-analyses of crop responses: response ratio metrics of ~0.27 for aboveground biomass and ~0.18 for yield as reported by Biederman and Harpole 2013, and mean increases of 11–14 % in yield reported by Jeffery et al. 2011 and Liu et al. 2013.
Although very encouraging, caution is required in interpreting and extrapolating these results. First, most results are from short-term pot experiments: 75 % of results included in analyses were for tree seedlings grown <6 months. Second, some of the very high growth responses observed, particularly for boreal tree species (e.g., Pluchon et al. 2014), may reflect unusual soil interactions in which strongly growth-inhibitory phenolics are sorbed by added chars (Wardle et al. 1998). Third, although we did not detect an obvious publication bias in graphical analyses of results, it is somewhat likely that there is under-reporting of neutral and negative results in the still-emerging literature on tree growth responses to biochar. Fourth, meta-analyses in general are best suited for cases in which treatments are highly standardized and repeatable (Gurevitch et al. 2001), and this cannot be said for biochar studies at present, due to the fact that biochars are inherently variable in properties. Many of the studies examined did not report the feedstock or pyrolysis temperature of char used (Table 1), posing serious problems for replicability of the particular studies, and comparability across studies. There is no real substitute for larger comparative studies conducted with well-characterized chars and soil conditions.
Both pot and field trials showed strong evidence of biomass growth responses, with no obvious difference in response, suggesting that pot trials may be broadly related to responses in the field, at least for early tree growth (Fig. 1c). The strongest responses appear to be found in short trials, with a weak pattern of declining response with increasing trial length. This could be due to physical changes in char through time, including uptake of soluble nutrients directly associated with fresh chars. However, another likely mechanism is that of inherent changes in growth responses arises from the leveling off of plant growth curves (e.g., Thomas et al. 1999): response ratios are likely to be maximized near the inflection point of plant growth curves, which in trees tend to fall very early in growth. The pattern of declining effects with time contrasts with that found for annual crops, where there is some evidence for increasing benefits of biochar over multiple cropping seasons (Major et al. 2010; Crane-Droesch et al. 2013).
The results also suggest important systematic differences in biochar response patterns in relation to tree phylogeny, among ecological systems, and among species. Among biomes there appears to be a general pattern of high response to boreal and tropical trees, with much lower responses in temperate trees. High responses to char additions observed in tropical species are consistent with a pervasive pattern of strong P limitation in tropical forests (Vitousek 1984), in conjunction with both high soluble P in chars and a capacity for chars to retain phosphate ions by sorption. P limitation effects seem much less likely to explain high responses in boreal tree species; however, Pluchon et al. (2014), found a relationship between P levels in char and seedling growth responses, suggesting P limitation in boreal forest. Along these lines, strong P limitation has been documented in some northern temperate forests where it is though to be related to high levels of anthropogenic N deposition (Gradowski and Thomas 2006, 2008). In addition, sorption of phenolics certainly contributes to high responses observed in some boreal studies (Wardle et al. 1998). We speculate that the low average response observed in temperate forests may thus result from N limitation in combination with low soil phenolics or other growth-inhibitory substances.
The analyses presented also suggest a pattern of higher biochar responses in hardwoods (angiosperms) than in conifers (Fig. 1b). In general evergreen conifers show relatively resource-conservative growth strategies relative to angiosperms, being generally adapted to environments with low productivity, in particular low temperatures and nutrient availability (Coomes et al. 2005; Lusk 2011). Associated traits include lower rates of nutrient uptake and adaptation to acid soils, which may explain the relatively low average biochar responses observed for conifers. However, the apparent systematic difference between conifers and angiosperms masks great interspecific differences, particularly apparent among angiosperms (Fig. 2). Such differences in plant response could potentially result in large effects of char additions on community composition and biodiversity of ecosystems. This is an important area for future research of particular relevance with respect to forest restoration.
Chars used in studies of tree responses have varied widely, and in many cases there is little information available in prior studies on char characteristics, feedstocks used, and properties (Table 1). It is widely recognized that pyrolysis conditions, in particular peak temperature and duration of pyrolysis, have profound effects on resulting chars (Enders et al. 2012), with, for example, pH, EC, and ash content increasing with pyrolysis temperature (Brewer et al. 2011; Kloss et al. 2012; Ronsse et al. 2013). Surface area generally increases with pyrolysis temperatures up to 500 °C, due to volatilization of compounds (Kloss et al. 2012); however surface area appears to commonly decrease at temperatures >600 °C (Ronsse et al. 2013). Wood biochars are generally the most aromatic and recalcitrant of biochars, and have the lowest ash content but also relatively low pH (Enders et al. 2012; Kloss et al. 2012). Wood is generally comprised of ~45 % cellulose, 25–30 % hemicellulose, and 20–25 % lignin (McKendry 2002; Yang et al. 2007); however, woods show remarkably high variation in these constituents, with distinct differences among groups. Notably, hemicellulose content is very low in most conifers, while lignin content is high (Pettersen 1984). Thus, different woods will result in chars with substantially different properties. It has even been suggested that the differences in properties of chars derived from different tree species may result in an ecological “afterlife” through differential effects of chars on seedling establishment and growth (Pluchon et al. 2014). Such ecological “afterlife effects” could contribute to positive feedbacks in post-disturbance regeneration: e.g., angiosperm biochar promoting angiosperm regeneration.
Biochar and natural disturbance emulation
An important general argument for the use of biochars in restoration is that natural disturbances often involve char deposition, and that colonizing species can be expected to be adapted to chars. Natural chars occur in many if not most soils in forests and other ecosystems (Krull et al. 2008; Jauss et al. 2015). In non-forest systems chars are increasingly recognized as playing a critical role in soil nutrient dynamics as well as constituting a long-term C stock (Spokas 2010). For example, recent results suggest that nearly all the cation exchange capacity of Mollisols, some of the world’s most productive agricultural soils, may be attributable to pyrogenic carbon (Mao et al. 2012). There is remarkably little information available on the distribution of natural chars, their properties, and their potential role in soil processes and forest productivity, particularly in forest ecosystems with relatively long natural fire return intervals. In many forested regions fire suppression has drastically reduced char inputs to forest soils in the last 100 years. Conversion of biomass into charcoal from wildfire occurs across a gradient of temperatures, pyrolysis time, and oxygen environments, and often from numerous feedstocks: the result is certain to be incredibly diverse chars, though data on natural char properties of forest soils are limited (Kuhlbusch et al. 1996; Czimczik et al. 2002).
Like industrially produced biochars, natural charcoals generally have high surface areas, ion exchange capacities, and liming capacity, properties that have the potential to enhance forest productivity. In temperate and boreal forests with little soil turnover charcoal is a fire legacy that is commonly recalcitrant at the organic-mineral soil interface (Hart and Luckai 2013). Mineral element solutes from freshly produced charcoal stimulate soil fauna and plant species classified as ecological pioneers following fire (DeLuca et al. 2006; Wardle et al. 1998). High surface areas and porosity allow for sorption of inhibiting soil compounds (e.g., phenolics) (Wardle et al. 1998), and have been hypothesized to provide habitat and refugia for soil fauna (Zackrisson et al. 1996). High porosity, combined with variable surface charge helps improve water retention on fine and coarsely textured soils (Busscher et al. 2003). Negative surface charges from oxidation increases cation exchange capacity, increasing nutrient retention and availability of important limiting elements like Ca and Mg (Laird et al. 2010; Brais et al. 2000). Perhaps the most important role of charcoal in systems with fire is its liming capacity: natural chars are deposited together with ash (primarily CaCO3) and the sorption of protons in the soil solution from negatively charged sites on charcoals can basify soils by several orders of magnitudes (Hart and Luckai 2013). Although chars are essential for sorption of nutrients, the “model” of natural wildfire points to the potential importance of combining biochar with ash in forest restoration, or of directly utilizing “high-ash” biochar.
Prospects for biochar in forest restoration
What might biochar specifically replace in forest restoration practice? First and foremost, biochar may replace other forms of organic matter, having the advantages of recalcitrance, high cation exchange capacity, capacity to reduce leaching of anions, and potential for sorption of toxic substances and salts. In an agricultural context, biochar is almost always added as an additional amendment to soils with appreciable organic matter, and it is common for biochar-compost mixtures to be used (Blackwell and Riethmuller 2009). One issue arising is that biochars generally have very low N content and through sorption of ammonium may so strongly sorb available N that it makes it less available, an effect expected to be offset by additions of fertilizers or composts with high N content. There are thus compelling reasons to expect that biochar use in forest restoration practice would be as a component of a mixture of soil amendments. There is also a strong case for biochar as a product substitute for lime. Dolomitic lime rapidly decomposes chemically and is a major source of agricultural CO2 emissions (West and McBride 2005). Thus substitution of char for lime would effectively have a two-fold effect on carbon emissions, by sequestering waste material C that would have been emitted, and by offsetting C emissions from lime. However, data suggest that the pH and liming capacity of wood-derived chars are generally lower than other chars (Ronsse et al. 2013), pointing to the importance of specifically designed chars or possibly use of high-ash biochars in cases where liming effects are of particular importance.
In agronomic systems, there is increasing recognition that biochar applications generally require biochars with specific properties to ameliorate specific soil conditions (e.g., Novak et al. 2009), and that large-scale differences in soil properties suggest a specific “niche” for biochar use in poorer soils with low CEC and soil C. These considerations are perhaps even more likely to be the case with biochars applied in the context of forest restoration. Wood biochars will likely be the most easily accessible in forest restoration projects, and to some extent engineered chars could potentially be ‘designed’ by choosing appropriate feedstocks; however, modification of pyrolysis temperature or system may also be important. Biochar use in practice is likely to be best targeted toward poor soils with low organic C, and perhaps specifically contaminated soils.
In conclusion, there is strong evidence for positive effects of biochar additions on growth of woody plants, with observed responses that appear to be generally larger than those observed in agricultural crops. However, there appears to be high heterogeneity in responses among tree species and ecological systems, and it is not possible to unambiguously distinguish this heterogeneity from differences in soils and chars used given existing data. Given the high heterogeneity in properties of chars and soils, it is critical that future studies provide more comprehensive details on properties of chars used, and the recent promulgation of characterization guidelines should assist in this regard (IBI 2014). Full realization of the potential for biochar use in forest restoration will necessitate a better understanding of heterogeneous responses to allow an informed matching of specific chars to specific restoration objectives.
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