Download Advances of mixed forest litter decomposition researches

Review of mixed forest litter decomposition researches
Fan Xiaoxua, Song Ruiqingb, Song Fuqianga,*
a Key
Laboratory of Microbiology, Life Science College, Heilongjiang University, Harbin, 150080, China
b College
of Forest, Northeast Forestry University, Harbin, 150040, China
Song Fuqiang： [email protected]
Abstract: The litter plays an important role in forest ecosystems. Decomposition of mixed leaf
litters has recently become an active research area because it mimics the natural state of leaf litters
in most of forests. Many studies reported effects of mixing litters on their decomposition, ranging
from positive, negative to neutral. In this paper decomposition mechanisms of mixed litters
concluded by researchers were summarized. Firstly, plant litter quality had been recognized as an
important factor to affect decomposition rate. Some studies showed a positive significant
correlation between initial N, P concentration and non-additive effect in litter mixture
decomposition. Secondly, it has been suggested that litter mixture could increase abundance and
diversity of fauna and microbial decomposers, especially fungi. Thirdly, compared with single
litter decomposition, the nutrient exchange between different litter species is often considered as
one of main non-additive effects observed in litter mixture. Some results showed that the active
transport of nutrients by fungal hyphae drived positive effect on the decomposition of litter
mixture. The multiple factors such as, leaf litter species, investigation method and plot, were also
analyzed. In conclusion, it is necessary to enhance a further research on factors in mixed litter
decomposition and an interaction between various factors due to the complex relationship. We are
looking forward to using these theories of mixed litter decomposition to direct practical forest
management.
Keyword: Forest litter; litter mixtures; Single-species decomposition; Non-additive effect;
Mycelial transport
Forest litter is a part of photosynthesis production from green plant, as well as an essential
pathway to return nutrient in forest ecosystem. Generally every year the rich nutrients released
from litter decomposition could meet 69~87% forest growth required [1]. Meanwhile, CO2
released is closed related to carbon cycle of terrestrial ecosystem. Thus, the process of litter
decomposition plays an important role in tree growth especially in poor soil. Accordingly studies
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on litter decomposition have been receiving long-term extensive attention. Relevant researches in
China started after 1980s, which is relatively later than it abroad. Previously researches focused on
single-species litter decomposition that does not exist in nature. Because in forest ecosystem
majority is mixed forest and although in pure stands litter is also mixed with understory and
herbaceous plant litter. In other words, the decomposition of a single species of litter usually
occurs in association with that of other species of litter. Therefore, litter mixture decomposition
has gradually become hotspot that domestic and foreign scholars are interested in [2]. Many
emerging researches directly examine decomposition in leaf mixtures as well as in all component
species decaying alone. In these litter-mix experiments, Characteristics of decomposition in
litter-mixes that deviate from responses predicted from decomposition of single-species litters
alone are designated "non-additive". In other words, its rate differs from the expected values
calculated as the arithmetic means of individual litter types; "additive" responses in mixes are
predictable from component species decaying alone. It is clear that decomposition patterns are not
always predictable from single-species dynamics. Compared with single species, mass loss of
litter-mix treatment is often increased on the whole [3]. In this article, we review recent
developments and mechanism deduced of litter mixture decomposition researches at home and
abroad, then provide key research questions and future perspectives to well understand the
mechanism of litter mixture decomposition and promote the effective application of the choice of
tree species in mixed forest.
1. Review of litter mixture decomposition experiments
Generally, O2 absorption, CO2 release and mass loss of litter are regarded as commom
indicators to measure decomposition rate of forest litter [4]. Many published data showed that
under different conditions the effects of mixing on the decomposition of litter is controversial,
ranging from negative to neutral to positive. With respect of positive effect, Taylor [5] found that
total mass losses increased obviously when Alnus crispa litter was added to Populus tremuloides
leaf litter. Fyle and Fyle [6] incubated Pseudotsuga menziesii foliage litter with Alnus rubra in the
laboratory. Throughout this study the mixtures decomposed faster than predicted from pure litter.
Briones et al. [7] determined decomposition rate by CO2 release. In their experiment Eucalyptus
globulus litter was mixed with either oak (Quercus petraea), ash (Fraxinus excelsior) or birch
(Betula pendula) litter, total CO2 release of any combination of two litter types was enhanced.
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Above researches suggested that compared with the pure components, mixture decomposition was
faster and has positive impacts on litter decay.
However, the results of Prescott et al. [8] indicated that there was no detectable effect on
decomposition when litter of Picea glauca, Pseudotsuga menziesii, Pinus contorta, Populus
tremuloides and Alnus rubra were mixed.
Otherwise, positive and negative effects of litter mixing have been detected within the same
study of Chapman et al. [9]. When Picea abies and Pinus sylvestris were mixed, metabolic activity
in the decomposer community of the forest floor were enhanced compared with single species
stands. But mixtures of Picea abies with Alnus glutinosa or Quercus petraea were depressed.
From an overall perspective, there was a common limitation in previous litter-mixing studies. In
earlier studies only the total mass loss of mixture was calculated and the component species of the
mixture was not separated from one another after incubation. So there have little evidence to
determine the contribution of the individual species to the total mass loss. In particular, it was
impossible to analyze how the species present influenced each other in litter decomposition.
With further research, interaction, negative or positive effect, between litter species in mixture
was detected after sorting the mixed litter according to litter type [10]. Peng Zhang [11] conducted
a mixing experiment to investigate the interaction between Castanopsis eyrei leaves and Pinus
massoniana needles during decomposition. These results showed that the mass loss of mixture
was not different from the sum of it in single species decomposition respectively. But after
mixture components were seperated, the decomposition of C. eyrei leaves was accelerated when it
was mixed with P. massoniana needles. On the other hand the decomposition of P. massoniana
needles was retarded when it was mixed with C. eyrei leaves. Based on this report, we could
deduce that if positive effect is greater than negative effect in litter mixture, mass loss of the
mixture will be enhanced than that in single litter type decomposition. Contrarily it will be
depressed. Meanwhile it is possible that positive and negative effect were canceled out and total
mass loss will don’t differe significantly from the predicted by single species. Thus this may be
reason that leads to different conclusion on mixture decomposition. Taking Phoeba bournei litter
added to Chinese fir, which is considered as one of the most important species of timber sourced
at plantations around Southern China, as an example [12], the component species was separated
from mixture afer sampled, then oven-dried until its dry mass determined. Its results showed that
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the rate of Chinese fir litter decomposition was accelerated when the Phoeba bournei was added.
The more Phoeba bournei litter was added to mixture, the faster Chinese fir litter was decomposed.
And compared with pure Chinese fir litter decomposition, the time to breakdown 95% litter
mixture, which contains 75% Chinese fir and 25% Phoeba bournei, was reduced by 1.44a; the
time to decompose 50% mixture was reduced by 0.37a. This research provided evidence to solve
soil fertility that has declined considerably in this region, and choose tree species with Chinese fir
plantation.
2. Mechanisms of litter mixture decomposition
Litter decomposition, dominated by bioprocesses while assisted by physical and chemical
reactions, is an important ecosystem-level process. Biotic factor and abiotic factor are both
involved in it, and the interacted two factors are the two sides that are looked into by researchers.
Abiotic factor mainly includes temperature, humidity, and pH and so on. With global climate
changes, increasing atmospheric CO2 and UV were also considered in present research. At present
abiotic factors in single species decomposition have been well understood. But the reports about
mixture decomposition are limited. Some researches indicated that the characteristic of moisture
adsorption in litter mixture was improved than single type decomposition. Then the humidity of
mixture was promoted. Wardle et al. [14] found that when needle and broad-leaved litter was
mixed, slow decomposition needle litter increased water content of litter layer, and promoted
decomposition rate of broad-leaved litter.
The main biotic factors controlling decomposition rate are litter quality, litter decomposer and
interactive effect between different litter species. The following review is described from the three
above.
2.1 Litter quality in mixture decomposition
Litter quality has long been recognized as a critical inner driver of decomposition rate. It refers
to easy decomposition components including protein, pectin and starch, hard decomposition
organic components, such as lignin, cellulose, hemicelluloses and polyphenols, as well as their
composition proportion. In addition, nutrient content and tissue structure are also involved. The
concentration of N, P, lignin, as well as the ratio of C to N, P, lignin are common indicators of
litter quality, among above indicators the ratio of C/N and lignin /N could well reflect the
decomposition rate. N is well known to affect the decomposition rate of individual litter types [5,
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15]. Meanwhile P may be also important factor especially in P-deficient ecosystems [16, 17].
Taylor [5] found that in early phase the decomposition rate largely depended on initial litter N
concentrations, and in later stage the concentration of lignin or the ratio of lignin to N became
determinative factor. However, the relation between litter quality and non-additive effects of litter
mixtures is still a controversy. In Hoorens [18] reports, the decomposition of a wide array of
two-species litter mixtures with differences initial litter chemistry was tested. They found that the
non-additive effects existed in many of litter mixtures. Although initial litter C, P, and polyphenol
concentrations of litter were significantly correlated with decomposition rates, they were not
related to the non-additive effects of litter mixtures. However, the research of Liu Ping et al. [19]
showed that initial litter N and P concentrations were significantly correlated with the nonadditive
effects of litter mixtures. They considered that because of obvious demands of active heterotrophs
for N, litter with higher initial N concentration (lower C/N ratio) usually decomposed faster in the
early stage [20]. When various species litter were mixed together, high N and P concentrations
type might induce a priming effect on the litters of low N and P concentrations, facilitating faster
decomposition of the low quality litters without necessarily retarding the decomposition of the
high quality litters [21]. Other studies also found that higher nutrient concentrations litter types
could supply nutrient and promote low quality litter decomposition [22].
2.2 Litter decomposer in mixture decomposition
In natural habitats soil invertebrata, such as earthworms and millipedes, play an important role
in litter decomposition from full litter shape to fragments. They mainly contribute to degrade
vegetation residuum, increase fragments surface, as well as mix soil organics with mineral on
surface layer to improve soil structure. Anderson [23] found that crypyostigmatid mite diversity to
be positively correlated with microhabitat structural diversity. Others [24, 25] both found that
microarthropod diversity is greater in two- species and three-species litter mixtures than in single
litter. At this point David et al. [26] conducted litter mixing and monoculture experiments using
litterbags in a New Zealand rainforest. In this study litter mixing had few effects on densities of
mesofauna and macrofauna, but litter types promoted different subsets of the fauna, notably
microbe-feeding and predatory nematodes. Above researches showed that except for the effect of
litter type, litter mixing stimulates decomposer diversity, quantity and activity through promoting
habitats diversity.
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Litter mixture decomposition has significant impacts on habitat of fauna; meanwhile the fauna
also has feed-back effect on mixture decomposition. Ha¨ttenschwiler’s [27] results provided
evidence that, a well developed soil macrofauna community played a fundamental role for altering
decomposition in response to changing litter diversity. For example millipedes had a significant
effect on the mass loss of the more slowly decomposing litter species. In the presence of
millipedes, the recalcitrant Quercus litter disappeared remarkably faster with increasing litter
diversity, showing a 26% greater mass loss in the six-species mixture than monocultures. However,
mass loss of Quercus litter did not change in response to increasing litter diversity without
macrofauna or when earthworms alone were present. Whereas earthworms were more important in
determining mass loss of more rapidly decomposing litter species. Therefore, the feedback exits
between litter mixing effect and soil fauna. Soil fauna not only processes large amounts of dead
plant material and determine its fate to a great extent in many ecosystems [28], and is closely
related with nutrient availability in the forest floor or soil. Furthermore it may have effect on C
pathway in litter decomposition. However, this factor, soil fauna, is notoriously excluded in
present decomposition studies [29].
After crushing effect, the further docomposition is drived by enzyme system of microorganism.
This process causes large changes in chemical composition of the substrate and achieved a
complete litter decomposition and nutrient release. Bacteria, actinomycetes and fungi including
yeast all take part in litter decomposition. Fungi are eukaryotic microorganisms and constitute a
major component of soil biota in forest ecosystems. In 2004, Cla´udia Pascoal [30] examined the
contribution of fungi and bacteria to litter decomposition. Their results showed that the
contribution of fungi to overall leaf carbon loss (29.0 to 38.8%) greatly exceeded that of bacteria
(4.2 to 13.9%). In conclusion, fungi play an important role in leaf litter decomposition, because
they could decompose the lignocelluloses matrix in the litter that other organisms are only rarely
able to decompose. In particular, filamentous fungi in acid environment are important component
of soil microorganism. Litter mixture decomposition also affected microflora diversity and their
structure. Song Fuqiang et al. [31] investigated the cultivable filamentous fungal diversity in litter
layer of two main forest types, Pinus massoniana and Liguidambar formasana mixed forest and
Quercus variabilis forest, in Zijin Mountain. After isolation and identification, fungal diversity in
the mixed forest was not only higher than that in Q. variabilis forest, but also filamentous fungi
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quantity in the fermented layer of mixed forest is almost twice that Quercus variabilis forest.
Although tree species is different in this mixed and pure forest, it partly showed that litter mixed
decomposition provides a series of favorable and essential conditions for fungi growth, and
accelerates litter decay rate through enhancing fungi quantity and their integration.
Simultaneously, mutual effect also exits in microflora. For example Dinishi Jayasinghe et al.
[32] found that the frequently isolated actinomycetes could act as antagonists for some common
leaf litter and wood decomposer fungi. Fast growing fungi genera (e.g. Mucor, Penicillium and
Trichoderma) were more tolerant of actinomycete antagonism than slow and moderately slow
growing genera (e.g. Cladosporium, Mortierella). The colonization of organic substrates by some
actinomycetes did reduce the degree of subsequent colonization by susceptible decomposer fungi.
Meanwhile, Fungal- bacterial antagonistic interaction on decomposing leaves was also observed.
Jacob Mùller et al. [33] found that inoculation of beech leaves with Humicola sp. alone resulted in
the highest mineralization rate, but when bacteria were added the mineralization rate was reduced
by more than 50%, and the NAGase and CELase activities of Humicola sp. showed a clear
depressing effect. Antagonistic interaction between fungi and actinomycetes, bacteria are
significant because of competition for substrate. Therefore, litter mixture decomposition not only
promots decomposer diversity, but on the other hand their positive effect in some extent may be
partly canceled out by antagonistic interaction between decomposer.
In a word, the positive effect of litter mixed decomposition was confirmed through providing
advantageous factors for microbial community. But in some studies [34, 35] plant litter quality had
been recognized as a dominate factor in their decomposer diversity and microbial community
structure. In the other words, different litter quality corresponds to special decomposer community
with different ability to decompose. Thus, the correspondence decomposer community which may
have strong ability to decompose or not, and interaction between microorganisms, such as
antagonism, also should be included in consideration. Considering litter type and mixture
decomposition comprehensively, we could conclude that litter decay rate may not be accelerated
after mixed.
2.3 The nutrient exchange between different litter species
Although interaction among chemical component of litter hinder a clear understanding of the
relation between certain litter component and non-additive effect, the nutrient exchange between
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different litter species is often regarded as one of the most important mechanisms of non-additive
effects observed in litter mixtures. Overall, this exchange can be carried out by a passive diffusion
[36] and an active transport by fungal hyphae [37]. In relation to passive diffusion, this process
transports nutrients that stimulated microbial activity as well as inhibitory compounds [37], such
as phenolics, secondary metabolism, usually produced by needle-leave evergreen plant responding
to interspecies competition, excessive consumption by animals, and air pollution, especially when
soil nutrient in shortage. Seen from passive diffusion, litter decay rate may faster, slow or not
change by the presence of other litter species. At the same time active transport is achieved by
fungal hyphae. The micromycetes produce dense networks of hyphae that connect litter fragments,
and presumably translocate nutrients from high quality litter types to the low ones. The nutritional
status of low quality types was improved and their mass losses are accelerated. However, the
inhibitory compounds are not transported. Thus, the microbial activity and decomposition rates of
litter mixtures are more likely to increase. Then in litter mixed decomposition the relative
importance of passive and active nutrient exchange should depend on the physical state of the
litter. Alexei [37] reported a laboratory experiment in which the effect of the litter species
diversity on decomposition was compared in mixtures of differently fragmented litter. His results
showed that litter mixture decomposition effect is not significant in small litter fragments,
eventually did not affect the mass loss of mixture after 142 days. In contrast, the decomposition
rate of litter in large fragments got faster with species increased, and 93% of all mixtures
decomposed faster than that predicted from monocultures. Thus it is clear that the active transport
of nutrients by fungal hyphae, rather than passive diffusion, drives positive effect of the litter
species diversity on decomposition.
3. Recommendations and further direction
In general, the results of most litter mixed decomposition experiments are various, and even
contradictory. This is because due to different conditions used in each research such as litter type,
investigation method, temperature and humidity of plot, each influencing factor of mixture
decomposition accounts for different proportions. Then different dominant factor controlling
decomposition rates has lead to different results, and present studies in this field could not be
compared with each other horizontally. Taking investigation method for example, microcosms and
litterbag methods are common measures used in mixture decomposition experiment. In this
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respect Eric F. Salamanca [38] used field microcosms (FM), greenhouse microcosms (GM) and
litterbag (LB) methods. The results indicated that decay rate of Quercus was enhanced in field
microcosms (FM) compared to LBs. The decay rates of both litter types were significantly
suppressed in GM as compared to field set up (FM and LB) which were comparable. Above
phenomenon showed that mass loss of litter was not only related to mixed decomposition, but also
research method. In addition, litter decomposition has obvious time mode [39], observation time
in each research is different. This may be another reason that leads to different analytic result.
Accordingly, we complete this review with a list of recommendations below that would be
conducive to well understand the mechanisms of litter mixture decomposition in further study.
1. At present the factor affecting litter decomposition is well known. From global perspective,
litter decomposition is closely related with climatic zone. Photoperiod, temperature, humidity
and other abiotic environment index are all significant impact factors in litter decay rate. But
in local scale, litter quality become more important. However, the results of mixed litter
decomposition are still no rules to follow. Thus, it is essential to study what percentage of
each factor accounting for and their status in mixture decomposition all around.
2. In the further mixed litter decomposition study we should avoid the complexity of multiple
factors interaction. In relation to internal factors, researchers in this field should reach
agreement firstly, that is typical quality litter species were selected as model plant. After the
mechanism of model plant mixture decomposition was determined, and then other tree species
of actual plantations could learn from it. About external factor, except for temperature and
moisture, decomposer community is various markedly between different study plot. For
example, the average of monthly individual of soil meso and microfauna were usually
increased as the latitude increased [40]. Pure-culture tests can be used in order to avoid
external factor. Two or more model litter species mixture could be sterilized [41] and
incubated with known decomposers to process solid fermentation, finally their mass loss was
detected respectively. Results of above method could neglect the effect of study material and
the disturbance of microflora and soil fauna in study plots. In the end the acting factors in
pure-culture are investigated just from litter quality because other interferences are removed.
Once the interactions of all acting factors in mixed decomposition are thoroughly studied, the
mechanism of mixed decomposition will be well known.
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3. The theory, which is obtained in litter mixture decomposition simulation study, is needed to
verify in nature forest after long-term location. Although in some degree the plant litter in
litter bags mimics the state of their natural decomposition, interference with the natural
environment is less compared with litter layer naturally occurring. Moreover, because the time
of litter fall is different, natural litter layer is not ideal model, one litter type in each litter layer.
Thus, the state of mixed litter is a dynamic process. In a word, the long-term location study in
natural forest will be more convincing and value to direct practical afforestation.
4. Global environment change would obviously affect mixed litter decomposition [42]. The
effects of global warming, elevated CO2 and especially increased UV-B radiation have been
increasingly concerned. It is no double that UV-B radiation will be a new factor considered in
litter mixture decomposition.
In general, mixed litter decomposition could promote vegetation nutrient availability [9, 43], its
growth and net primary productivity [44]. In order to choose appropriate tree species for the
success of mixed afforestation, it is valuable to study further the mechanism of forest litter mixture
decomposition in ecosystem. Many reports have showed that compared with pure stand, timber
outputs in mixed forest increased with biological productivity, for example Michelia macclurei
var.sublanea mixed with Cunninghamia lanceolata [45], or with Pinus massoniana [46]. Thus it
can be seen that complementation and coordinated developments of nutrient space, shade
tolerance and biochemical interaction between main tree species and associated tree species
should be considered when mixed forest plantation. Meanwhile, the interaction between two or
more litter species during decomposition process also should be included [47]. We are looking
forward to deep understanding about litter mixture decomposition, and obtain theory in planting
mixed forest, which has high level of sustained productivity and forest soil fertility.
Acknowledgements
The project was financially supported by National Science Foundation of China (No. 30571493,
30710103), Harbin Science Foundation for Outstanding Scholarship (2007RFXXN047), Chinese
National Programs for Science and Technology Development (2006BAD08A11105) and Natural
Science Foundation of Heilongjiang University (No.200818).
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