Oecologia (1993) 94:457M71 Oecologia �9 Springer-Verlag 1993
Review article
Patterns in decomposition rates among photosynthetic organisms: the importance of detritus C :N :P content
S. Enriquez ~, C.M. Duarte ~, K. Sand-Jensen 2
t Centro de Estudios Avanzados de Blanes, (CSIC), Cami de Santa BArbara, 17300 Blanes, Girona, Spain 2 Freshwater Biological Laboratory, University of Copenhagen, 51 Helsingorsgade, 3400 Hillerod, Denmark
Received: 30 January 1993 / Accepted: 4 April 1993
Abstract. The strength and generality of the relationship between decomposition rates and detritus carbon, nitro- gen, and phosphorus concentrations was assessed by comparing published reports of decomposition rates of detritus of photosynthetic organisms, from unicellular algae to trees. The results obtained demonstrated the existence of a general positive, linear relationship be- tween plant decomposition rates and nitrogen and phos- phorus concentrations. Differences in the carbon, nitro- gen, and phosphorus concentrations of plant detritus accounted for 89% of the variance in plant decom- position rates of detritus originating from photosynthetic organisms ranging from unicellular microalgae to trees. The results also demonstrate that moist plant material decomposes substantially faster than dry material with similar nutrient concentrations. Consideration of lignin, instead of carbon, concentrations did not improve the relationships obtained. These results reflect the coupling of phosphorus and nitrogen in the basic biochemical processes of both plants and their microbial decom- posers, and stress the importance of this coupling for carbon and nutrient flow in ecosystems.
Key words: Decomposition - Plant kingdom - Nutrients
Carbon fixed by photosynthetic organisms is made avail- able to other ecosystem components via herbivores or detritivores. The detrital path is a major determinant of the flow of carbon fixed by plants in ecosystems were herbivores consume a modest fraction of primary production, as is often the case (Swift et al. 1979). De- composition of plant detritus is largely conducted by bacteria and fungi (e.g. Persson et al. 1980), and the rate of this process depends, therefore, on all factors influenc- ing their activity. These may be separated, following Swift et al. (1979), into abiotic factors, the physico-
This work was funded through a grant of CICYT (MAR91~503) to C.M.D.
Correspondence to: S. Enriquez
chemical conditions under which the decomposition oc- curs, and substrate quality (e.g. biochemical composition of plant litter), which constrains its suitability for micro- bial growth. Photosynthetic organisms can directly in- fluence decomposition rates through their biochemical composition. For instance, plants may accumulate de- fence chemicals in their tissues which, besides decreasing their palatability to grazers (e.g. Coley et al. 1985), also reduce their quality as a substrate for decomposer mi- croorganisms (Swift et al. 1979). Similarly, nutrient reab- sorption before abscission of plant tissues may, in addi- tion to improving the internal nutrient economy of the plant (Chapin 1980), affect their suitability as substrate for microbial decomposers.
Decomposer organisms tend to have very high nitro- gen and phosphorus contents (Findlay 1934; Thayer 1974; Swift et al. 1979; Goldman et al. 1987; Vadstein and Olsen 1989) indicative of high requirements for these nutrients. For instance balanced bacterial growth re- quires substrates with carbon, nitrogen, and phosphorus in an (atomic) ratio of 106:12:1 (Goldman et al. 1987), although bacteria have some capacity to vary these re- quirements (e.g. Tezuka 1990). These high nutrient con- tents are only encountered in fast-growing phytoplank- ton cells (Goldman et al. 1979; Duarte 1992), and micro- bial decomposers are often supplied with plant detritus depleted in nitrogen and phosphorus relative to their requirements. Recent research has demonstrated that bacterial growth efficiency (i.e. the fraction of the carbon used allocated to growth) decreases about 100-fold with increasing C/N and C/P ratios in their substrate (Gold- man et al. 1987). Thus, detritus with high nitrogen and phosphorus content should decompose fast because of the associated fast growth of the microbial populations, whereas excess carbon in the plant litter should lead to nutrient-controlled carbon remineralization (cf. Gold- man et al. 1987; Vadstein and Olsen 1989).
These arguments provide an explanation for the in- crease in decomposition rate with increasing nutrient concentration, or decreasing carbon/nutrient ratios, demonstrated six decades ago (Tenny and Waksman 1929), and confirmed since for different aquatic (e.g.
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Valiela et al. 1984; Twilley et al. 1986; Harrison 1989; Reddy and DeBusk 1991) and terrestrial (e.g. Gosz et al. 1973; Swift et al. 1979; Berg et al. 1982; Taylor et al. 1989; Upadhyay et al. 1989) systems. In addition to reflecting direct nutrient effects, these relationships also appear to have an indirect component, derived from a tendency towards reduced carbon quality and increasing amounts of secondary metabolites in plant litter as nu- trient availability decreases (Coley et al. 1985, Chapin et al. 1987). Hence, some ratios incorporating a descriptor of carbon quality (e.g. lignin/N ratios) have also been shown to be related to decay rates of plant litter (e.g. Melillo et al. 1982; Aber et al. 1990). However, lignin/N ratios appear to outperform C/nutrient ratios as a predic- tor of decay rates only when comparing plant litters of similar lignin contents (Taylor et al. 1989).
Whether the widespread finding of strong relation- ships between litter nutrient content and decomposition rates reflects the existence of a general relationship, ap- plicable to detritus originating from different photosyn- thetic organism, is not known as yet. The existence of such a general relationship is expected because all micro- bial decomposers have high nitrogen and phosphorus, in addition to carbon, needs in both aquatic (Goldman et al. 1987; Vadstein and Olsen 1989) and terrestrial (Find- lay 1934; Thayer 1974; Swift et al. 1979) environments. Conversely, these relationships might differ between dif- ferent sorts of plant detritus if they were indirect, result- ing from covariation between carbon quality (e.g. con- tents of lignin, polyphenols, etc.) and nutrient content within plant types (e.g. Melillo et al. 1982; Abet et al. 1990; Upadhyay et al. 1989).
Here we examine the strength and generality of the relationship between decomposition rates and plant nu- trient concentrations by comparing published reports of decomposition rates and litter nutrient contents across a broad spectrum of plant detritus, from unicellular algae to trees. We first examine the variability in decom- position rates of litter from different sources, and then assess the power of differences in their nutrient concen- tration to statistically account for the observed variabil- ity. A subset of these data, for which lignin contents were available in addition to nitrogen and phosphorus con- tents, was used to compare the strength of the relation- ship between lignin and nutrient contents and litter de- composition rates. Because plant nutrient concentrations are often strongly intercorrelated (Garten 1976; Duarte 1992), we used path analysis (Williams et al. 1990) to statistically resolve the direct contribution of carbon, nitrogen, phosphorus, and, where available, lignin, to the observed relationship between nutrient content and de- tritus decomposition rate.
Methods
We searched the literature for published reports of plant litter decomposition rates and chemical composition (carbon, lignin, nitrogen, and phosphorus concentrations) at initiation of decom- position. Decomposition rates (k, natural log units day-1) were described from the changes in plant dry weight (W) with time (t,
days) since the initiation of the experiments using the equation,
wt = Wo e-kt
which is the model most often used in the literature (Olson 1963) and simpler than the double-exponential model (e.g. O'Connell 1987). Because these decomposition rates have logarithmic units, we also described decomposition rates as the half-life of plant detritus (Ta/2, days), which, although a function of exponential decom- position rates (T1/2 = k - 1 . In 2), provides a more intuitive des- cription of detritus turnover times. Decomposition rates were often reported in the studies, and were otherwise calculated from tab- ulated data or digitized graphs of weight remaining with time elapsed. We included in the data set (Appendix) all studies encoun- tered during our search that included estimates of decomposition rates of plant litter (e.g. photosynthetic tissues, roots, rhizomes, stems), and any of the descriptor of tissue chemical composition needed to test our hypotheses (i.e. C, N, P, and lignin concentra- tions).
Additional detail in the general description of the data set was obtained by grouping the data according to detritus origin (phyto- plankton, macroalgae, seagrasses, freshwater angiosperms, am- phibious plants, sedges, mangroves, grasses, shrubs, conifers, and broad-leaved deciduous and evergreen trees). The relationships be- tween decomposition rates and nutrient concentrations were des- cribed using least-squares regression analyses of log-transformed data. Logarithmic transformation was found to be necessary to avoid heteroscedasticity in these analyses (Draper and Smith 1965). Differences in the relationship between plant litter decomposition rate and nutrient content depending on detritus origin (as defined above) were tested for using analysis of covariance (Draper and Smith 1966). The simultaneous influence of carbon (or lingin), nitrogen, and phosphorus on litter decomposition rates was tested for using multiple least squares regression analyses, instead of carbon/nutrient ratios, for the use of these ratios is conducive to statistical artifacts (cf. Chayes 1971; Atchley and Anderson 1978). The (statistical) influence of nitrogen, phosphorus, carbon (or lig- nin) contents on decomposition rates was partitioned into direct and indirect effects using path analysis (e.g. Williams et al. 1990). Separate path analyses were used to test the effects of C, N, and P, on the one hand, and those oflignin, N, and P, on the other, because lignin contents were only reported in a small subset of the studies, which did not include any study on phytoplankton or macroalgae.
Results and discussion
The data set comprised 256 reports of decomposition rates of plant litters originating from different photosyn- thetic organisms, from land an aquatic environments (Appendix). These data were gathered under a broad variety of conditions, from controlled laboratory experi- ments to field studies, and included decomposition of plant litter originating from photosynthetic tissues, roots, rhizomes, stems and branches, and mixtures of these (Appendix). Unfortunately, detailed descriptions of the experimental conditions (e.g. temperature, pH, oxygen tension) were only reported in a few studies and could not be included in the analysis.
Decomposition rates ranged between 0.00019 day -1 for non-photosynthetic tissues of an Australian shrub (Leucospermun parile), and 0.098 day- i for the cells of a cyanobacterium (Anabaena sp.) and the leaves of a submerged freshwater angiosperm (Vallisneria spiralis), and differed significantly according to their origin (ANO- VA, F=41.3, P < 0.0001; Fig. 1). Decomposition rates were faster for detritus derived from phytoplankton and
459
M i c r o a l g a e Freshwater plants
A m p h i b i o u s p lants Macroa lgae S e a g r a s s e s
Grasses S e d g e s
M a n g r o v e s Broad decid.tree leave:
S h r u b s , - C o n i f e r s
Broad perennial tree leaves
0 . 0 0 0 1
t
i
I I m ~
r-l----q f - y - -
P
0 . 0 0 1
i
** I'---f]
I I t'---
I I I '
7--3---1 , F ~
I I
]
O P
I
0.01
�9
0 . 1 0 5 0 0 1 0 0 0 1 5 0 0 2 0 0 0
b
. O �9
.
[
D e c o m p o s i t i o n r a t e s ( d a y -1 )
Fig. 1. Box plots showing the distribution of detritus decomposition rates and half-lives for detritus of different sources. Boxes encom- pass the 25 and 75% quartiles of all the data for each plant type, the central line represents the median, bars extend to the 95%
H a l f - l i f e o f d e t r i t u s ( d a y s )
confidence limits, asterisks-represent observations extending be- yond the 95% confidence limits, and circles represent observations beyond the 99% confidence limits
Table 1. Regression equations between detritus decomposition rate (K, In units day x) and carbon (C), phosphorus (P), nitrogen (N), and lignin concentrations (as % DW) in the plant litter
Variable Intercept Slope N Slope P Slope C Slope n r z F P dependent lignin
k -2.45 1.19+0.095 231 0.40 155 <0.001 k - 1.42 0.93 • 0.066 143 0.58 198 < 0.001 k 1.17 -2.1• 78 0.12 11.6 <0.001 k - 1.38 - 1.04• 0.20 54 0.32 25 .8 <0.001 k - 1 . 8 9 0.80• 0.50• 141 0.64 123 <0.001 k -0.22 0.71 • 0.220 0.66+0.154 - 1.0• 50 0.85 92 < 0.001 k - 1.87 0.31 ~ 0.240 0.39• -0.22• 43 0.37 9.14 < 0.001
Submersed detritus: k -2.30 1.33• 136 0.50 134 <0.001 k - 1.22 1.01 • 80 0.66 153 <0.001
Terrestrial detritus: k -2.77 0.48• 98 0.14 17 <0.001 k - 2.20 0.46 • 0.09 66 0.26 24 < 0.001
All variables were tog-transformed prior to regression analyses. Also shown are the SE of the regression coefficients, the number of observations involved (n), the coefficient of determination (r2), the
F-statistic (F), and the associated probability level (P) for the regres- sion analysis
amphib ious and submerged freshwater plants (Fig. 1), which had average half-lives between 17 and 58 days, and were slowest for litter derived f rom shrubs and perennial- leaf trees, which had average half-lives ranging between 2 and 3 years (Fig. 1). Lit ter nutr ient concent ra t ions also differed significantly accord ing to the detritus source ( A N O V A , F = 17.9 and 16.8 for N and P, respectively, P < 0.001), such that plants whose detritus decomposed fast also tended to p roduce detritus with high ni t rogen and phosphorus concentra t ions .
Decompos i t i on rates were s t rongly positively cor- related with the initial ni t rogen and phosphorus concen- t rat ion o f the detritus ( r = 0 . 6 4 and 0.76, respectively, P < 0.0001 ; Table 1, Fig. 2), and were weakly, negatively correlated to its c a rbon concent ra t ion ( r = - 0 . 3 7 ;
P < 0 . 0 0 5 ; Table 1). Regression analysis indicated that decomposi t ion rates ( k ) increased linearly (Ho: slope= 1, t-test, P > 0.05) with increasing litter ni t rogen and phosphorus concentra t ions (Table 1). This implies that half-lives (half life = k -1 In 2), and, therefore, de- tritus turnover times are inversely scaled to litter nutr ient concentrat ion. Detr i tus lignin content was negatively correlated with its n i t rogen and phosphorus contents (r = - 0.36 and - 0.57, respectively, P < 0.05), and was significantly, negatively related to litter decompos i t ion rates (Table 1), suppor t ing the impor tance o f ca rbon quali ty on decompos i t ion rates (e.g. Melillo et al. 1982; Aber et al. 1990; U p a d h y a y et al. 1989).
The relationships between decompos i t ion rates and ni trogen and phosphorus concent ra t ions differed signifi-
460
0.1
0.01
0.001
0 . 0 0 0 1
0 . 0 1
o ~ o
eo o
I I
0.10
, , - . /t ,
o ~/y'o_ wO~O e ~0
I I I
1 1 0 0 . 0 0 1 0 . 0 1 0 . 1 1
Nitrogen (% DW) Phosphorus (% DW)
10
Fig. 2. The relationships between de- composition rate and the initial nitro- gen and phosphorus concentrations in the detritus. S o l i d l ines represent the fitted regression lines (Table 1), and o p e n a n d s o l i d c i rc l e s represent detritus decomposing on land and submersed, respectively
' O . 1
0 . 0 1 e~ 0
0 . 0 O l E 0
j 9 6
O . O 0 0 l
0 . 0 1 0 . 1 0 1 0
N i t r o g e n c o n t e n t (% D W ) Fig. 3. Regression lines describing the relationships between decom- position rates and nitrogen and phosphorus concentrations for detritus of different sources. L i n e s extend the range of nutrient con- centrations for detritus source in the data set. 1 - microalgae;
i
t_
e~ 0
E 0
0 . 1
0 . 0 1 --
0 . 0 0 1 --
0 . 0 0 0 1
0 . 0 0 1
2 1
3 5
8 6
4
9
I I I
0 . 0 1 0 . 1 0 1 0
P h o s p h o r u s c o n t e n t ( % D W )
2 - freshwater plants; 3 amphibious plants; 4 macroalgae; 5 - seagrasses; 6 - grasses; 7 - sedges; 8 - mangroves; 9 - broad deciduous tree leaves; 10 - shrubs; 11 - conifers; 12 - broad perennial tree leaves
cantly depending on detritus origin (ANCOVA, F= 11.2 and 5.0, P < 0.001, for nitrogen and phosphorus concen- trations, respectively), which accounted for 32 % and 24 % of the unexplained variance in the relationship between decomposition rate and litter nitrogen and phosphorus concentrations, respectively. Decomposition rate of am- phibious plant litter increased fastest with increasing nitrogen and phosphorus concentration (Fig. 3, Table 2), and no relationship between litter nitrogen or phospho- rus content and decomposition rate was observed within some litter sources (e.g. phytoplankton, freshwater angiosperms; Fig. 3, Table 2). These differences were partially attributable to the different habitats where the detritus decomposed, for litter decomposed faster, for a given nutrient concentration, in water than on land (AN- COVA, F=12.4 and 4.9, P<0.001, for nitrogen and phosphorus, respectively), consistent with the stimulato- ry effect of moisture on decomposition rates (Swift et al. 1979). Moreover, decomposition rates of submerged plant detritus were strongly, linearly scaled to nutrient concentrations (Table 1), whereas those of plant material
decomposing on land were much weaker and scaled as the 1/2 power of nutrient concentration (Table 1).
The large variance in detritus decomposition rates unexplained by nitrogen or phosphorus concentration, as well as the lack of relationship within some sources of detritus, may be partially attributable to the need to consider the effects of carbon, nitrogen and phosphorus contents on plant decomposition in concert. This has been achieved in the past using the carbon/nitrogen and carbon/phosphorus ratios of the detritus, which reflect the relative limitation of decomposers by carbon - and energy - versus nutrients (e.g. Twilley et al. 1986; Taylor et al. 1989; Reddy and DeBusk 1991; and others). We also found strong negative correlations between decom- position rates and C/N and C/P ratios (Fig. 4), and simultaneous consideration of detritus nitrogen, phos- phorus, and carbon concentrations accounted for most (89%, SE of regression estimates = 1.7-fold) of the vari- ance in decomposition rates (Table 1), independently of detritus origin (ANCOVA, F-test, P>0.05). A similar relationship based on lignin, nitrogen, and phosphorus
461
Table 2. Regression equations between detritus decomposition rate (K, in units d 1) and nitrogen (N), and phosphorus (P) concentrations (as % DW), for the different detritus sources in the data set
Plant type Intercept Slope N Intercept Slope P Range n r 2 F P
Phytoplankton N - 1.51 0.314- 0.274 (8.94-2.30) 15 0.02 1.24 0.286 P - 1.26 0.23 • 0.204 (1.70-0.26) 13 0.02 1.25 0.287
Macroalgae N - 1.46 - 1.30 • 0.662 (3.92-1.00) 8 0.29 3.85 0.098 P - 1.54 1.11 • 1.401 (0.36-O.19) 6 0.000 0.63 0.473
Seagrasses N -2.19 0.16• (4.36-0.53) 24 0.000 0.15 0.702 P - 1.64 0.41 • 0.068 (2.50-0.04) 7 0.85 35.33 0.002
Freshwater N - 1 . 5 5 0.40:t:0.516 (3.66-1.15) 17 0.000 0.59 0.454 angiosperms P - 1 . 2 9 0.134-0.230 (0.85-0.10) 14 0.000 0.35 0.580
Amphibious plants N - 2.35 1.98 4- 0.384 (3.25-0.59) 12 0.701 26.75 0.000 P - 0.42 2.22 • 0.343 (0.47-0.08) 9 0.836 41.75 0.000
Sedges N - 1.78 0.744- 0.188 (2.77-0.18) 50 0.505 50.92 0.000 P - 1.78 0.744- 0.188 (0.29-0.01) 24 0.388 15.56 0.001
Mangroves N -2.17 1.62:6 1.046 (1.24-0.36) 8 0.165 2.38 0.174 P -3.71 1.564-0.739 (0.13-0.06) 4 0.537 4.47 0.169
Grasses N -2.48 0.6012.62 (3.52-0.18) 9 0.341 5.14 0.058 P - 1 . 8 5 0.684-0.165 (0.58-0.02) 8 0.699 17.22 0.006
Shrubs N - 2.62 1.19 4- 0.464 (2.15-0.44) 18 0.247 6.57 0.040 P - 1.96 0.574- 0.208 (0.56-0.005) 14 0.329 7.38 0.019
Conifers N - 2.91 0.71 4- 0.227 (4.96-0.35) 25 0.271 9.93 0.040 P -2.02 0.764-0.265 (0.55-0.02) 15 0.340 8.22 0.013
Broad deciduous tree N - 2.70 0.08 ~: 0.209 (3.07-0.07) 43 0.000 0.15 0.704 leaves P - 2.31 0.25 4- 0.291 (0,28-0,02) 26 0.000 0.76 0.391
Broad perennial tree N -2.14 1.53i363 (0.70-0.13) 6 0.770 17.76 0.014 leaves P - 1.57 0.76 • 0.329 (0.06-0.004) 6 0.465 5.34 0.082
All variables were log-transformed prior to regression analyses. Also shown are the SE of the regression coefficients, the range of nitrogen and phosphorus concentrations for the different sources of
detritus, the number of observations involved (n), the coefficient of determination (r2), the F-statistic (F), and the associated probability level (P) for the regression analysis
"7
0 .1
0 .01
0 .001
0 .0001
1 1000 10
6 6 z \ 0 I �9 o d ~t. o . ~ . $" 4 i t . . �9 �9 0 0 o �9
I r
10 100
C / N
I I
100 1000 10000
C/P
Fig. 4. The relationship between detritus decomposition rate and initial C/N and C/P atomic ratios. Solid lines represent the fitted re- gression lines
concen t ra t ions , was m u c h w e a k e r (37% o f the var iance expla ined , SE o f regress ion es t imates = 2.2-fold), pe rhaps because o f the n a r r o w e r r ange o f de t r i tus sources for which es t imates o f l ignin concen t r a t i on were avai lable .
N i t r o g e n a n d p h o s p h o r u s concen t r a t i ons in the p l a n t de t r i tus were h ighly co r r e l a t ed ( r = 0.83, P < 0.0001), as d e m o n s t r a t e d for te r res t r ia l ( G a r t e n 1976) and aqua t i c (Dua r t e 1990, 1992) p lants . The s t rong co l inear i ty be- tween p h o s p h o r u s a n d n i t rogen concen t r a t ions implies tha t the coefficients o f d e t e r m i n a t i o n o b t a i n e d in the mul t ip le regress ion analys is (Tab le 1) m a y be inflated, and the regress ion coefficients b iased ( D r a p e r and Smi th
1966). The s ta t is t ica l influence o f l i t ter n i t rogen, phos- phorus , and c a r b o n (or l ignin) concen t r a t ions on de- c o m p o s i t i o n ra tes is bes t depic ted , therefore , as a mix tu re o f d i rec t (i.e. d e p e n d e n t on the concen t r a t i on o f a par - t icu lar e lement) and indi rec t effects, ac t ing t h r o u g h the re la t ionsh ip to o the r nu t r ien ts (Fig. 5). W e used p a t h analys is (Wi l l iams et al. 1990) to e luc ida te these di f ferent effects. This showed tha t ind i rec t effects were indeed i m p o r t a n t , and accoun ted for 52% and 44% o f the effect o f n i t rogen and p h o s p h o r u s , respect ively, on l i t ter de- c o m p o s i t i o n rates (Fig. 5), whereas no signif icant d i rec t effect cou ld be a t t r i bu t ed to differences in c a r b o n concen-
462
~ 0 N, 0.41 P, 0.03 C)
�9 86 0 . 8 7 ~ -0 17 Phosphorus " �9 �9 i ' k (0.48 P, 0.34 N, 0 . 0 4 y Decompos i t ion
\ ~ Ca~rbon ~ -0.37 (-0"18 c, -0.07 N, -0.12 p)
rate
N i t rogen �9 ~ / ~ 0 . 4 9 ( 0 . 1 9 N, 0.26 P, 0.04 Lignin) 1 3 / / 0 . 6 1
0!36 Phosnl~orus 0.61 ~ . . " " P - - (0.43 P, 0.12 N, 0.06 lignin~,,~" Decompos i t ion rate
\ \ 0 . .... ~ / - 0 . 4 3 (-0.11 Lignin, -0.07 N, -0.25 P)
Lignin
Fig. 5a, b. Path diagrams describing the structure of the relationship be- tween decomposition rates and a ni- trogen, phosphorus and carbon, or b lignin concentrations. Numbers in bold type show the Pearson correla- tion coefficients among the variables, and numbers in parentheses partition the Pearson correlations between de- composition rates and nutrient con- centration into direct and indirect (i.e. attributable to indirect relation- ships to other variables) effects (cf. Williams et al. 1990)
tration. Similarly, path analysis on the smaller data set for which lignin concentration was available also re- vealed no significant direct effect of lignin concentration on detritus decomposition rates (Fig. 5).
These results provide evidence of the importance of the nitrogen and phosphorus concentration in the plant litter in regulating decomposition rates, consistent with current knowledge of microbial nutrient requirements. That detritus carbon concentrations were not particular- ly important in accounting for differences in decom- position rates is expected from the high C/N and C/P ratios characteristic of plant detritus (Fig. 4), relative to those of bacteria (Thayer 1974; Swift et al. 1979) and saprophytic fungi (Findlay 1934; Swift et al. 1979). The lack of strong relationships between detritus carbon or lignin concentrations and decomposition rates does not conflict with the important role of carbon quality in regulating decomposition rates. Instead, it probably re- flects the fact that carbon quality is a compound variable, involving a broad array of compounds besides lignin in the diverse set of detritus sources compared here. These results are, therefore, consistent with previous reports that differences in decomposition rates were best related to nutrient content when comparing litters from a broad range of plant sources, but to carbon quality when com- paring litter derived from similar plants (Taylor et al. 1989). The relationship between plant decomposition rates and detritus carbon, nitrogen and phosphorus con- centration found here accounted for most (89%) of the differences in the decomposition rates of detritus derived from photosynthetic organisms ranging from unicellular microalgae to trees. These results highlight, therefore, the importance of the nutritional balance (C :N :P) of plant detritus in regulating decomposition rates.
The nutritional balance of plant detritus plays, therefore, an important role in the control of material
flow in ecosystems. Nutrient constraints on carbon flow through detrital food webs may be, at least qualitatively, similar to the demonstrated importance of plant nutrient status for herbivory (e.g. Mattson 1980). Microbial de- composers also play a major role in the digestion of the plant material ingested by herbivores, so that the diges- tion process in herbivore guts involves, in fact, decom- position. Thus, there are close relationships between plant nutrient status and herbivory (Mattson 1980), and between plant nutrient concentration and the efficiency of conversion of ingested food (Mattson 1980). The par- allel between detritivory and herbivory extends beyond nutrient control of their rates. For instance, increasing temperature accelerates decomposition rates (Godshalk and Wetzel 1978; Swift et al. 1979; Best et al. 1990; Aizaki and Takamura 1991). Likewise, the digestive tracts of homeotherm herbivores provide, compared with those of poikilotherms, a suitable "digestion reactor" with high temperatures enabling efficient microbial activ- ity (Swift et al. 1979). Thus, herbivory and detritivory are, to some extent, constrained by similar factors, through similar causes. The recent awareness of the im- portance of microbial heterotrophs as links between pri- mary produceres and herbivores in planktonic ecosys- tems (i.e. the microbial loop, Azam et al. 1983), may well reflect the general structure of ecosystems, where primary producers and herbivores are linked by such microbial loop (whether internally, i.e. intestinal flora, or external- ly, i.e. decomposers).
The important role of nutrients in controlling plant decomposition rates has also the indirect effect of cou- pling growth and decomposition rates, for fast-growing plants tend to have high nutrient concentrations (Chapin et al. 1987), and also decompose fast because of the adequacy of their litter as substrate for microbial growth. Exceptions to this rule are systems where climatic con-
463
ditions reduce decompos i t ion rates, such as water- logged soils, lakes, and the sea floor, where plant decompos i t ion is reduced by low p H and /o r anoxia (Godsha lk and Wetzel 1978; Swift et al. 1979; Best et al. 1990), leading to an inordinate accumula t ion o f organic matter . H o w - ever, the general associat ion o f fast g rowth rates with fast decompos i t ion rates, resulting f rom the control l ing role o f nutrients in bo th processes, acts to prevent the accu- mula t ion o f ca rbon and associated nutrients as plant detritus. Conversely, the associat ion between slow plant g rowth rates and slow litter decompos i t ion rates ensures the release o f nutrients f rom plant detritus at rates slow enough to allow for efficient recycling. These pat terns are conducive, therefore, to an overall balance between the magni tude o f living and detrital p lant material, which is p robab ly a fundamenta l aspect o f ecosystem funct ioning and plant succession.
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son
1989
) W
ater
1.
90
0.00
13
(Har
riso
n 19
89)
Wat
er
3.00
0.
0040
(H
arri
son
1989
) W
ater
2.
64
0.55
0 55
.00
24.3
1 25
8.33
0.
0124
(H
emm
inga
& N
ieuw
enhu
ize
1991
) W
ater
2.
76
0.50
0 37
.00
15.6
4 19
1.17
0.
0230
(H
emm
inga
& N
ieuw
enhu
ize
1991
) W
ater
1.
12
34.4
0 35
.42
0.00
07
(Ken
wor
thy
& T
haye
r 19
84)
Wat
er
1.00
32
.00
37.3
3 0.
0183
(K
enw
orth
y &
Tha
yer
1984
)
Pla
nt t
ype
Spec
ies
Fra
ctio
n C
ondi
tion
s %
N
%P
%C
C
N
CP
K
(d
1)
Aut
hor
Fre
shw
ater
an
gios
perm
s
Am
phib
ious
P
lant
s
Zos
tera
mar
ina
Roo
ts
Wat
er
0.73
32
.00
51.1
4 0.
0048
Z
oste
ra m
arin
a R
hizo
mes
W
ater
0.
53
34.4
0 74
.84
0.00
35
Thal
assi
a te
stud
inum
L
eave
s (a
vera
ge)
Wat
er
2.10
36
.30
20.1
7 0.
0048
Th
alas
sia
test
udin
um
Lea
ves
(ave
rage
) W
ater
1.
80
33.9
0 21
.97
0.02
79
Cym
odoc
ea
nodo
sa
Lea
ves
Wat
er
4.36
50
.60
13.5
4 0.
0039
Z
oste
ra m
arin
a L
eave
s W
ater
1.
61
0.55
0 28
.98
21.0
0 14
0.91
0.
0136
Z
oste
ra m
arin
a L
eave
s W
ater
2.
41
2.50
0 33
.80
16.3
6 34
.93
0.03
57
Zos
tera
mar
ina
Mix
ed l
itte
r W
ater
1.
27
2.10
0 24
.10
22.1
4 29
.65
0.03
57
Pos
idon
ia o
cean
ica
Mix
ed l
itte
r (+
woo
d)
Wat
er (
20 m
.) 1
.40
0.07
8 31
.20
26.0
0 10
40
0.00
87
Pos
idon
ia o
eean
ica
Mix
ed l
itte
r (+
woo
d)
Wat
er (
5 m
.)
0.58
0.
038
23.7
0 47
.67
1633
0.
0066
Th
alas
sia
test
udin
um
Lea
ves
Wat
er
1.86
28
.18
17.6
8 0.
0149
H
alop
hila
stip
ulac
ea
Lea
ves
Wat
er
0.00
32
Pot
amog
eton
per
foli
atus
L
eave
s W
ater
1.
15
0.04
46
Pot
amog
eton
luc
ens
Lea
ves
Wat
er
2.40
0.
160
0.05
17
Pot
amog
eton
luc
ens
Lea
ves
Wat
er
1.20
0.
100
0.04
58
Elo
dea
cana
dens
is
Lea
ves
Wat
er
1.26
0.
200
0.04
75
Elo
dea
cana
dens
is
Lea
ves
Wat
er
3.66
0.
820
0.08
59
Cer
atop
hyllu
m
Lea
ves
(ave
rage
) W
ater
3.
44
0.84
8 55
.38
18.7
8 16
8.69
0.
0247
V
allis
neri
a sp
iral
is
Lea
ves
Wat
er
2.61
0.
370
0.09
87
Naj
asfl
exil
is
Lea
ves
Wat
er
1.80
31
.2
20.2
2 0.
0070
M
yrio
phyl
lum
het
erop
hyll
um
Lea
ves
Wat
er
2 24
.7
14.4
1 0.
0090
M
yrio
phyl
lum
het
erop
hyll
um
Lea
ves
Wat
er
2 24
.7
14.4
1 0.
0340
N
ajas
flex
ilis
L
eave
s W
ater
1.
80
31.2
20
.22
0.02
80
Pot
amog
eton
nod
osus
L
eave
s (a
vera
ge)
Wat
er
2.40
0.
430
41.6
0 20
.22
249.
2 0.
0483
P
otam
oget
on c
risp
us
Lea
ves
Wat
er
2.15
0.
290
0.06
48
Pot
amog
eton
cri
spus
L
eave
s W
ater
1.
90
0.29
0 0.
0640
Ju
stic
ia a
mer
ican
a L
eave
s, p
etio
les,
ste
ms
Wat
er
0.13
7 0.
0138
Ju
stic
ia a
mer
ican
a R
oots
and
Rhi
zom
es
Wat
er
0.29
8 0.
0398
P
otam
oget
on
Lea
ves
Wat
er
1.77
0.
360
31.9
21
.03
228.
912
0.03
10
Rap
pia
Lea
ves
Wat
er
1.37
0.
510
32.6
27
.76
165.
130
0.02
80
Myr
ioph
yllu
m
Lea
ves
Wat
er
2.79
0.
560
30.4
1
2.7
1
140.
238
0.04
50
Sagi
ttar
ia l
anc~
folia
L
eave
s W
ater
2.
40
0.15
0 0.
0058
Sa
gitt
aria
lan
cifo
lia
Ste
ms
Wat
er
1.40
0.
130
0.00
76
Nym
phoi
des
pelt
ata
Pet
iole
s W
ater
77
0.
0420
N
ymph
oide
s pe
ltat
a L
ong
Sho
ots
Wat
er
178
0.04
40
Nym
phoi
des
pelt
ata
Lea
ves
Wat
er
3.24
8 0.
465
50.0
4 22
0.
0560
N
ymph
oide
s pe
ltat
a L
eave
s W
ater
3.
248
0.46
5 50
.04
16
0.09
10
Nym
phoi
des
pelt
ata
Pet
iole
s W
ater
48
0.
0450
N
ymph
oide
s pe
ltat
a R
oots
W
ater
17
9 0.
0790
N
ymph
oide
s pe
ltat
a R
oots
W
ater
13
7 0.
0490
N
ymph
oide
s pe
ltat
a S
hort
Sho
ots
Wat
er
143
0.03
50
Nym
phoi
des
pelt
ata
Lon
g S
hoot
s W
ater
15
1 0.
0370
N
ymph
oide
s pe
ltat
a S
hort
Sho
ots
Wat
er
152
0.05
50
Nup
har
vari
egat
um
Lea
ves
Wat
er
2.4
39.3
19
.14
0.06
00
Nup
har
vari
egat
um
Lea
ves
Wat
er
2.4
39.3
19
.10
0.02
00
Spar
gani
um
eury
carp
um
Mix
ed l
itte
r W
ater
1.
41
38.6
7 32
0.
0076
Sp
arga
nium
eu
ryca
rpum
M
ixed
lit
ter
Wat
er
0.59
0.
079
38.4
3 76
57
0.00
0.
0021
Sp
arga
nium
eu
ryca
rpum
M
ixed
lit
ter
Wat
er
0.59
0.
130
38.4
3 76
57
0.00
0.
0017
E
ichh
orni
a cr
assi
pes
Mix
ed l
itte
r (a
vera
ge)
Wat
er
2.53
0.
270
88.9
1 41
71
0.00
0.
0095
(Ken
wor
thy
& T
haye
r 19
84)
(Ken
wor
thy
& T
haye
r 19
84)
(New
ell
et a
l. 19
86)
(New
ell
et a
l. 19
86)
(Ped
uzzi
& H
ernd
l 19
91)
(Pel
lika
an 1
982)
(P
elli
kaan
198
4)
(Pel
lika
an 1
984)
(R
omer
o et
al.
1992
) (R
omer
o et
al.
1992
) (R
uble
e &
Rom
an
1982
) (W
ahbe
h &
Mah
asne
h 19
85)
(Bas
tard
o 19
79)
(Bas
tard
o 19
79)
(Bas
tard
o 19
79)
(Bas
tard
o 19
79)
(Bas
tard
o 19
79)
(Bes
t et
al.
1990
) (B
rigg
s et
al.
1985
) (G
odsh
alk
& W
etze
l 19
78a)
(G
odsh
alk
& W
etze
l 19
78a)
(G
odsh
alk
& W
etze
l 19
78a)
(G
odsh
alk
& W
etze
l 19
78a)
(H
ill
1979
) (R
oger
s &
Bre
en 1
982)
(R
oger
s &
Bre
en 1
982)
(T
wil
ley
et a
l. 19
85)
(Tw
ille
y et
al.
1985
) (T
wil
ley
et a
l. 19
86)
(Tw
ille
y et
al.
1986
) (T
wil
ley
et a
l. 19
86)
(Bay
ley
et a
l. 19
85)
(Bay
ley
et a
l. 19
85)
(Bro
ck /
984)
(B
rock
198
4)
(Bro
ck 1
984)
(B
rock
198
4)
(Bro
ck 1
984)
(B
rock
198
4)
(Bro
ck 1
984)
(B
rock
198
4)
(Bro
ck 1
984)
(B
rock
198
4)
(God
shal
k &
Wet
zel
1978
a)
(God
shal
k &
Wet
zel
1978
a)
(Nee
ley
& D
avis
198
5)
(Nee
ley
& D
avis
198
5)
(Nee
ley
& D
avis
198
5)
(Red
dy &
DeB
usk
1991
)
4~
P
lant
typ
e Sp
ecie
s F
ract
ion
Con
diti
ons
%N
%
P %
C
CN
C
P
K (
d-l
) A
utho
r
Nup
har
lute
um
Lea
ves,
pet
iole
s, s
tem
s W
ater
2.
92
0.38
3 0.
0988
N
upha
r lu
teum
R
oots
and
rhi
zom
es
Wat
er
1.67
0.
245
0.01
42
Ter
rest
rial
pla
nts
:
Sedg
es
Ph
rag
mit
es
com
mun
is
Mix
ed l
itte
r W
ater
1.
04
0.00
1.8
Phr
agm
ites
com
mun
is
Mix
ed l
itte
r W
ater
0.
60
0.00
14
Pan
icum
sp.
Mix
ed l
itte
r W
ater
1.
60
0.07
0 0.
0071
Sp
artin
a al
tern
iflor
a R
oots
B
elow
grou
nd
0.39
38
.24
114.
39
0.00
67
Spar
tina
alte
rnifo
lia (s
hort
for
m)
Mix
ed l
itte
r S
oil/
Fer
tili
zed
2.54
41
.90
19.2
5 0.
0052
Sp
artin
a al
tern
ifolia
(tal
l fo
rm)
Mix
ed l
itte
r S
oil/
Fer
tili
zed
1.20
41
.70
40.5
4 0.
0081
Sp
artin
a al
tern
ifolia
(sho
rt f
orm
) M
ixed
lit
ter
Soi
l/C
ontr
ol
0.77
43
.10
65.3
0 0.
0033
Sp
artin
a al
tern
ifolia
(tal
l fo
rm)
Mix
ed l
itte
r S
oil/
Con
trol
0.
53
41.9
0 92
.23
0.00
63
Typh
a do
min
gens
is
Mix
ed l
itte
r W
ater
0.
50
0.01
4 0.
0010
Ty
pha
dom
inge
nsis
M
ixed
lit
ter
Wat
er
0.35
0.
012
0.00
099
Cla
dium
jam
aice
nse
Mix
ed l
itte
r W
ater
0.
40
0.02
0 0.
0013
C
ladi
um ja
mai
cens
e M
ixed
lit
ter
Wat
er
0.50
0.
022
0.00
07
Cla
dium
jam
aice
nse
Mix
ed l
itte
r W
ater
0.
30
0.00
6 0.
0007
Ty
pha
dom
inge
nsis
M
ixed
lit
ter
Wat
er
0.50
0.
028
0.00
21
Typh
a m
arsh
M
ixed
lit
ter
Wat
er
0.48
0.
001
Scir
pus
subt
erm
inal
is
Mix
ed l
itte
r W
ater
1.
2 30
.4
29.5
6 0.
0090
Sc
irpu
s ac
utus
M
ixed
lit
ter
Wat
er
1.5
43.6
33
.91
0.00
20
Scir
pus
acut
us
Mix
ed l
itte
r W
ater
1.
5 43
.6
33.9
1 0.
0050
Sc
irpu
s su
bter
min
alis
M
ixed
lit
ter
Wat
er
1.2
30.4
29
.56
0.00
20
Spar
tina
alte
rnifl
ora
Mix
ed l
itte
r W
ater
1.
33
0.01
11
Junc
us r
oem
eria
nus
Mix
ed l
itte
r W
ater
0.
79
0.00
91
Spar
tina
angl
ica
Mix
ed l
itte
r W
ater
1.
12
0.00
79
Spar
tina
angl
ica
Mix
ed l
itte
r W
ater
0.
71
0.00
22
Trig
loeh
in m
ariti
ma
Lea
ves
Wat
er
2.54
0.
0256
Sp
artin
a an
glie
a M
ixed
lit
ter
Wat
er
0.90
0.
0033
Sp
artin
a an
gIic
a M
ixed
lit
ter
Wat
er
1.29
0.
0093
Tr
iglo
chin
mar
itim
a M
ixed
lit
ter
Wat
er
2.09
0.
0025
Sp
artin
a an
glic
a L
eave
s W
ater
1.
67
0.00
61
Typh
a 9l
auca
M
ixed
lit
ter
Wat
er
0.48
0.
050
38.6
7 94
18
00.0
0 0.
0011
Ty
pha
glau
ca
Mix
ed l
itte
r W
ater
0.
55
38.6
6 82
0.
0016
Ty
pha
glau
ca
Mix
ed l
itte
r W
ater
0.
48
0.02
5 38
.67
94
1800
.00
0.00
11
Typh
a gl
auca
L
eave
s (s
enes
ced)
W
ater
0.
63
0.05
0 0.
0104
Ty
pha
glau
ca
Lea
ves
(gre
en)
Wat
er
2.77
0.
290
0.02
35
Junc
us r
oem
eria
nus
Mix
ed l
itte
r W
ater
0.
70
45.6
2 76
.03
0.00
17
Phr
agm
ites
eom
mun
is
Lea
ves
Wat
er
0.71
40
.00
65.7
3 0.
0045
Sp
artin
a M
ixed
lit
ter
Wat
er
1.07
0.
150
42.3
46
.12
728.
5 0.
0098
Sp
artin
a al
tern
ifolia
M
ixed
lit
ter
Wat
er
0.71
0.
0043
Sp
artin
a al
tern
ifolia
M
ixed
lit
ter
Wat
er
1.64
0.
0071
Ty
pha
glau
ca
Mix
ed l
itte
r W
ater
0.
82
0.10
8 47
.10
67.0
1 11
31.8
6 0.
0012
Sc
oloc
hloa
fest
ucac
ea
Mix
ed l
itte
r W
ater
0.
77
0.05
3 43
.10
65.3
0 21
00.7
9 0.
0016
Sc
irpu
s la
eust
ris
Mix
ed l
itte
r W
ater
0.
40
0.03
4 45
.40
132.
42
3449
.51
0.00
1 P
hrag
mite
s au
stra
lis
Mix
ed l
itte
r W
ater
0.
30
0.02
9 47
.50
187.
85
4305
.56
0.00
07
Scol
ochl
oafe
stuc
acea
M
ixed
lit
ter
Wat
er
0.87
0.
060
43.3
5 58
.13
1866
.46
0.00
22
Typh
a x
g!au
ca
Mix
ed l
itte
r W
ater
0.
75
0.09
2 46
.00
71.5
6 12
91.6
7 0.
0012
P
hrag
mite
s aus
tral
is
Mix
ed l
itte
r W
ater
0.
18
0.01
6 48
.60
315
7846
.88
0.00
03
(Tw
ille
y et
al.
198
5)
(Tw
ille
y et
al.
198
5)
(And
erse
n 19
78)
(And
erse
n 19
78)
(Bay
ley
et a
l. 19
85)
(Ben
ner
et a
l. 19
91)
(Bre
tele
r &
Tea
l 19
81)
(Bre
tele
r &
Tea
l 19
81)
(Bre
tele
r &
Tea
l 19
81)
(Bre
tele
r &
Tea
l 19
81)
(Dav
is 1
991)
(D
avis
199
1)
(Dav
is 1
991)
(D
avis
199
1)
(Dav
is 1
991)
(D
avis
199
1)
(Fin
dley
et
al.
1990
) (G
odsh
alk
& W
etze
l 19
78a)
(G
odsh
alk
& W
etze
l 19
78a)
(G
odsh
alk
& W
etze
l 19
78a)
(G
odsh
alk
& W
etze
l 19
78a)
(H
aine
s &
Han
son
1979
) (H
aine
s &
Han
son
1979
) (H
emm
inga
& B
uth
1991
) (H
emm
inga
& B
uth
1991
) (H
emm
inga
& B
uth
1991
) (H
emm
inga
& B
uth
1991
) (H
emm
inga
& B
uth
1991
) (H
emm
inga
& B
uth
1991
) (H
emm
inga
& B
uth
1991
) (N
eele
y &
Dav
is 1
985)
(N
eele
y &
Dav
is 1
985)
(N
eele
y &
Dav
is 1
985)
(N
elso
n et
al.
1990
) (N
elso
n et
al.
1990
) (N
ewel
l et
al.
198
4)
(Tan
aka
1991
) (T
wil
ley
et a
l. 19
86)
(Val
iela
et
al.
1984
) (V
alie
la e
t al
. 19
84)
(Van
der
Val
k et
al.
1991
) (V
an d
er V
alk
et a
l. 19
91)
(Van
der
Val
k et
al.
1991
) (V
an d
er V
alk
et a
l. 19
91)
(Van
der
Val
k et
al.
1991
) (V
an d
er V
alk
et a
l. 19
91)
(Van
der
Val
k et
al.
1991
)
Pla
nt t
ype
Spec
ies
Fra
ctio
n C
ondi
tion
s %
N
%P
%C
C
N
CP
K
(d-
1)
Aut
hor
Man
grov
es
Gra
sses
Bro
ad
deci
duou
s tr
ee l
eave
s
Scir
pus
lacu
stri
s M
ixed
lit
ter
Wat
er
0.63
0.
051
45.3
5 83
.98
2319
.88
0.00
15
Typ
haxg
lauc
a M
ixed
lit
ter
Wat
er
0.89
0.
123
48.2
0 63
.18
1012
.33
0.00
10
Seol
oehl
oafe
stuc
aeea
M
ixed
lit
ter
Wat
er
0.97
0.
067
43.6
0 52
.44
1681
.09
0.00
23
Phr
agm
ites
aus
tral
is
Mix
ed l
itte
r W
ater
0.
41
0.04
1 46
.40
132.
03
2923
.58
0.00
08
Scir
pus
lacu
stri
s M
ixed
lit
ter
Wat
er
0.86
0.
067
45.3
0 61
.45
1746
.64
0.00
11
Kan
delia
can
del,
Mix
ed l
itte
r (+
wo
od
) W
ater
0.
75
31.5
0 49
0.
0018
A
vice
nnia
mar
ina
Rhi
zoph
ora
man
gle
Mix
ed l
itte
r (+
wo
od
) W
ater
0.
40
43.3
5 12
6.44
0.
0095
R
hizo
phor
a sp
p.
Mix
ed l
itte
r (+
wo
od
) S
oil
0.37
37
.19
117.
27
0.00
08
Rhi
zoph
ora
spp.
M
ixed
lit
ter
(+w
oo
d)
Soi
l 0.
36
34.4
8 11
1.74
0.
0002
A
vice
nnia
mar
ina
Mix
ed l
itte
r (+
wo
od
) W
ater
/Bag
ged
0.74
0.
065
0.01
14
Avi
cenn
ia m
arin
a M
ixed
lit
ter
(+w
oo
d)
Wat
er/
0.76
0.
061
0.01
89
Unb
agge
d A
vice
nnia
mar
ina
Roo
ts
Wat
er
1.18
0.
106
0.00
38
Avi
cenn
ia m
arin
a L
eave
s W
ater
1.
24
0.12
7 0.
0071
Mol
inia
cae
rule
a M
ixed
lit
ter
Soi
l 1.
95
0,58
0 0.
0153
E
lym
us p
ycna
nthu
s M
ixed
lit
ter
Wat
er
0.90
0.
0079
E
ryth
rina
sp.
M
ixed
lit
ter
Soil
3.
52
0.21
0 0.
0095
C
ajan
us c
ajan
M
ixed
lit
ter
Soi
l 3.
48
0.18
0 0.
0047
In
ga e
dulis
M
ixed
lit
ter
Soi
l 3.
18
0.22
0 0.
0025
T
allg
rass
pra
irie
M
ixed
lit
ter
(ave
rage
) S
oil
0.18
0.
015
0.00
09
Whi
te p
ine
Nee
dles
S
oil
0.35
0.
0012
H
emlo
ck
Nee
dles
S
oil
0.66
0.
0009
6 W
hite
spr
uce
Nee
dles
S
oil
0.52
0.
060
0.00
14
Dou
glas
fir
N
eedl
es
Soi
l 0.
61
0.11
0 0.
0017
P
inus
rox
burg
hii
Nee
dles
S
oil
0.67
0.
050
0.00
21
Red
map
le
Lea
ves
Soi
l 1.
59
0.00
20
Red
oak
L
eave
s S
oil
1.90
0.
0011
A
spen
L
eave
s S
oil
2.14
0.
0014
R
ed o
ak
Lea
ves
Soi
l 1.
94
0,00
11
Sug
ar m
aple
L
eave
s S
oil
2.05
0.
0023
P
aper
bir
ch
Lea
ves
Soi
l 2.
22
0.00
17
Red
map
le
Lea
ves
Soi
l 1.
80
0.00
19
Red
oak
L
eave
s S
oil
2.26
0.
0009
W
hite
oak
L
eave
s S
oil
1.67
0.
0012
S
ugar
map
le
Roo
ts
Soi
l 2.
62
0.00
06
Aln
us i
nean
a L
eave
s S
oil
3.07
0.
137
0.00
09
Bet
ulap
ubes
cens
L
eave
s S
oil
0.77
0.
105
0,00
09
Bet
ula
pube
scen
s L
eave
s S
oil
1.74
0.
180
0.00
09
Pop
ulus
tre
mul
oide
s L
eave
s S
oil
0.84
0,
120
0.00
12
Que
rcus
elli
psoi
dalis
L
eave
s S
oil
1.40
0.
120
0.00
09
Bet
ula
papy
rife
ra
Lea
ves
Soi
l 0.
92
0.11
0 0.
0012
F
rang
ula
alnu
s L
eave
s S
oil
0.88
0.
030
0.00
54
Que
rcus
pyr
enai
ca
Lea
ves
Soi
l 0.
6 0,
042
0.00
30
Bet
ula
pube
seen
s L
eave
s S
oil
0.61
0,
029
0.00
33
Sali
x fr
agil
is
Lea
ves
Wat
er
1.20
0.
100
0.02
46
Aln
us g
luti
nosa
L
eave
s W
ater
2.
60
0,11
8 0.
0252
F
agus
syl
vati
ca
Lea
ves
Soi
l 0.
71
0.03
0 0.
0007
S
ugar
map
le
Lea
ves
Soil
0.
57
0.02
0 0.
0014
(Van
der
Val
k et
al.
1991
) (V
an d
er V
alk
et a
l. 19
91)
(Van
der
Val
k et
al.
1991
) (V
an d
er V
alk
et a
l. 19
91)
(Van
der
Val
k et
al.
1991
)
(Lee
198
9)
(New
ell
et a
l. 19
84)
(Rob
erts
on &
Dan
iel
1989
) (R
ober
tson
& D
anie
l 19
89)
(Van
der
Val
k &
Att
iwil
l 19
84)
(Van
der
Val
k &
Att
iwil
l 19
84)
(Van
der
Val
k &
Att
iwil
l 19
84)
(Van
der
Val
k &
Att
iwil
l 19
84)
(Aer
ts 1
989)
(H
emm
inga
& B
uth
1991
) (P
alm
& S
anch
ez 1
990)
(P
alm
& S
anch
ez 1
990)
(P
alm
& S
anch
ez 1
990)
(S
east
edt
1988
) (M
cCla
ughe
rty
et a
l. 19
85)
(McC
laug
hert
y et
al.
1985
) (T
aylo
r et
al.
1989
) (T
aylo
r et
al.
1989
) (U
padh
yay
et a
l. 19
89)
(Abe
r et
al.
1990
) (A
bet
et a
l. 19
90)
(Abe
r et
al.
1990
) (A
ber
et a
l. 19
90)
(Abe
r et
al.
1990
) (A
bet
et a
l. 19
90)
(Abe
r et
al.
1990
) (A
bet
et a
l. 19
90)
(Abe
r et
al.
1990
) (A
ber
et a
l. 19
90)
(Ber
g &
Ekb
ohm
19
91)
(Ber
g &
Ekb
ohm
199
1)
(Ber
g &
Ekb
ohm
199
1)
(Boc
khei
m e
t al
. 19
91)
(Boc
khei
m e
t al
. 19
91)
(Boc
khei
m e
t al
. 19
91)
(Esc
uder
o et
al.
1991
) (E
scud
ero
et a
l. 19
91)
(Esc
uder
o et
al.
1991
) (G
essn
er e
t al
. 19
91)
(Ges
sner
et
al.
1991
) (G
osz
et a
l. 19
73)
(Gos
z et
al.
1973
)
4~
Pla
nt t
ype
Spec
ies
Fra
ctio
n C
ondi
tion
s %
N
%P
%C
C
N
CP
K
(d
1)
Aut
hor
Shr
ubs
Con
ifer
s
Sug
ar m
aple
L
eave
s S
oil
0.62
0.
020
0.00
09
Yel
low
bir
ch
Lea
ves
Soi
l 1.
09
0.08
0 0.
0017
Y
ello
w b
irch
L
eave
s S
oil
0.85
0.
060
0.00
23
Fag
us s
ylva
tica
L
eave
s S
oil
0.82
0.
090
0.00
10
Fag
us s
ylva
tica
L
eave
s W
ater
0.
67
0.00
35
Fag
us s
ylva
tica
L
eave
s (a
vera
ge)
Soi
l 1.
12
0.00
21
Fag
us s
ylva
tica
L
eave
s S
oil
1.12
0.
0013
A
spen
L
eave
s S
oil
0.66
0.
0016
W
hite
oak
L
eave
s S
oil
0.67
0.
0015
R
ed m
aple
W
ood
chip
s S
oil
0.07
0.
0008
S
ugar
map
le
Lea
ves
Soi
l 0.
66
0.00
22
Aln
us n
epal
ensi
s W
ood
part
S
oil
2.56
0.
072
0.00
29
Asp
en
Lea
ves
Soi
l 0.
64
0.12
0 0.
0018
B
alsa
m p
opla
r L
eave
s S
oil
0.58
0.
130
0.00
16
Cow
-par
snip
M
ixed
lit
ter
Soi
l 1.
31
0.29
0 0.
0036
G
rass
M
ixed
lit
ter
Soi
l 0.
81
0.06
0 0.
0022
D
ogw
ood
leaf
lit
ter
Lea
ves
Soi
l 0.
78
0.08
0 0.
0021
Salic
orni
a vi
rgin
iea
Mix
ed l
itte
r (+
wo
od
) W
ater
1.
56
0.56
0 0.
0413
H
alim
ione
por
tula
coid
es
Mix
ed l
itte
r (+
wo
od
) W
ater
o
2.09
0.
0090
Li
rnon
ium
vul
gare
M
ixed
lit
ter
(+w
oo
d)
Wat
er
2.06
0.
0025
Li
mon
ium
vul
gare
L
eave
s W
ater
2.
15
0.00
48
Hal
imio
ne p
ortu
laeo
ides
M
ixed
lit
ter
(+w
oo
d)
Wat
er
1.70
0.
0090
Le
ucos
perr
num
pari
le
Mix
ed l
itte
r (+
wo
od
) S
oil
0.53
0.
023
51.0
666
11
2.4
1
5653
.81
0.00
02
Aca
cia
urop
hylla
M
ixed
lit
ter
(+w
oo
d)
Soi
l 0.
71
0.01
0 0.
0010
Tr
ymal
ium
spa
thul
atum
L
eave
s S
oil
0.6
0.01
9 0.
0031
B
ossi
aea
laid
law
aian
a L
eave
s S
oil
1.78
0.
019
0.00
16
Cas
uari
na d
ecus
sata
L
eave
s S
oil
0.44
0.
005
0.00
12
Aca
cia
urop
hylla
L
eave
s S
oil
1.27
0.
015
0.00
15
B.
laid
law
aian
a po
ds
Pod
s S
oil
0.61
0.
006
0.00
08
Cea
noth
us m
egac
arpu
s L
eave
s S
oil
0.63
0.
028
0.00
10
Salv
ia m
elif
era
Lea
ves
Soi
l 0.
58
0.10
5 0.
0011
Sa
lvia
mel
ifer
a L
eave
s S
oil
0.65
0.
133
0.00
09
Cea
noth
us m
egac
arpu
s L
eave
s S
oil
0.67
0.
046
0.00
1 R
ose
sp.
Lea
ves
Soi
l 1.
15
0.19
0 0.
0032
M
allo
tusp
hili
ppen
sis
Lea
ves
Soi
l 0.
50
0.13
0 0.
0110
Pin
us c
onto
rta
Nee
dles
So
il
0.45
0.
0004
W
hite
pin
e R
oots
S
oil
1.83
0.
0008
H
emlo
ck
Nee
dles
So
il
1.50
0.
001
Whi
te p
ine
Nee
dles
S
oil
0.97
0.
001
Red
pin
e N
eedl
es
Soi
l 1.
26
0.00
09
Sco
ts p
ine
Nee
dles
S
oil
1.89
0.
0008
S
cots
pin
e N
eedl
es
Soi
l 0.
37
0.00
07
Sco
ts p
ine
Nee
dles
S
oil
1.22
0.
0009
P
inus
syl
vest
ris
Nee
dles
S
oil
0.48
0.
033
0.00
08
Pin
us s
ylve
stri
s N
eedl
es
Soi
l 1.
51
0.13
1 0.
0010
L
odge
pole
pin
e N
eedl
es
Soi
l 0.
48
0.03
3 0.
0008
L
odge
pole
pin
e N
eedl
es
Soi
l 1.
05
0.08
2 0.
0008
B
row
n sp
ruce
N
eedl
es
Soi
l/
0.42
0.
041
0.00
06
Fer
tili
zeed
(Gos
z et
al.
1973
) (G
osz
et a
l. 19
73)
(Gos
z et
al.
1973
) (G
osz
et a
l. 19
73)
(Ive
rsen
197
3)
(Joe
rgen
sen
& M
eyer
199
0)
(Joe
rgen
sen
1991
) (M
cCla
ughe
rty
et a
l. 19
85)
(McC
laug
hert
y et
al.
1985
) (M
cCla
ughe
rty
et a
l. 19
85)
(McC
laug
hert
y et
al.
1985
) (S
harm
a &
Am
bash
t 19
87)
(Tay
lor
et a
l. 19
89)
(Tay
lor
et a
l. 19
89)
(Tay
lor
et a
l. 19
89)
(Tay
lor
et a
l. 19
89)
(Tay
lor
et a
l. 19
89)
(Hai
nes
& H
anso
n 19
79)
(Hem
min
ga &
But
h 19
91a)
(H
emm
inga
& B
uth
1991
a)
(Hem
min
ga &
But
h 19
91a)
(H
emm
inga
& B
uth
1991
a)
(Mit
chel
l et
al.
1986
) (O
'Con
nell
198
7)
(O'C
onne
ll 1
987)
(O
'Con
nell
198
7)
(O'C
onne
ll 1
987)
(O
'Con
nell
198
7)
(O'C
onne
ll 1
987)
(S
chle
sing
er 1
985)
(S
chle
sing
er 1
985)
(S
chle
sing
er 1
985)
(S
chle
sing
er 1
985)
(T
aylo
r et
al.
1988
) (U
padh
yay
et a
l. 19
89)
(Yav
itt
& F
ahey
198
6)
(Abe
r et
al.
1990
) (A
ber
et a
l. 19
90)
(Abe
r et
al.
1990
) (A
ber
et a
l. 19
90)
(Ber
g et
al.
1982
) (B
erg
et a
l. 19
82)
(Ber
g et
al.
1982
) (B
erg
& E
kboh
m
1991
) (B
erg
& E
kboh
m 1
991)
(B
erg
& E
kboh
m 1
991)
(B
erg
& E
kboh
m 1
991)
(B
erg
& T
amm
199
1)
Pla
nt t
ype
Spec
ies
Fra
ctio
n C
ondi
tion
s %
N
%P
%C
C
N
CP
K
(d-
1)
Aut
hor
Bro
ad p
eren
nial
tr
ee l
eave
s
Bro
wn
spru
ce
Nee
dles
S
oil
0.43
0.
041
0.00
05
Gre
en s
pruc
e N
eedl
es
Soi
l/
0.85
0.
132
0.00
08
Fer
tili
zeed
G
reen
spr
uce
Nee
dles
S
oil
0.85
0.
132
0.00
1 P
inus
ban
ksia
na
Nee
dles
S
oil
0.88
0.
080
0.00
05
Pin
us p
inas
ter
Nee
dles
S
oil
0.4
0.01
7 0.
0010
P
inus
syl
vest
ris
Nee
dles
S
oil
0.69
0.
037
0.00
20
Sit
ka s
pruc
e B
ranc
hes
Soi
l 4.
96
0.55
0 0.
0355
Q
uerc
us l
anug
inos
a L
eave
s So
il
1.32
0.
120
0.00
49
Lyon
ia o
valif
olia
L
eave
s S
oil
0.80
0.
080
0.00
73
Que
reus
gla
uca
Lea
ves
Soi
l 0.
94
0.07
0 0.
0073
Sh
orea
rob
usta
L
eave
s S
oil
0.99
0.
280
0.00
76
Que
rcus
flori
bund
a L
eave
s S
oil
0.97
0.
120
0.00
51
Que
rcus
leu
cotr
icho
phor
a L
eave
s S
oil
1.15
0.
220
0.00
52
Euc
alyp
tus
dive
rsic
olor
F
ruit
S
oil
0.21
0.
027
0.00
05
Euc
alyp
tus
dive
rsic
olor
L
eave
s S
oil
0.41
0.
010
0.00
15
Euc
alyp
tus
dive
rsic
olor
T
wig
s S
oil
0.21
0.
008
0.00
03
Euc
alyp
tus
dive
rsic
olor
B
ark
Soi
l 0.
13
0.00
4 0.
0006
M
yric
a es
cule
nta
Lea
ves
Soi
l 0.
58
0.05
7 0.
0043
R
hodo
dend
ron
arbo
reum
L
eave
s S
oil
0.70
0.
060
0.00
48
(Ber
g &
Tam
m 1
991)
(B
erg
& T
amm
199
1)
(Ber
g &
Tam
m 1
991)
(B
ockh
eim
et
al.
1991
) (E
scud
ero
et a
l. 1
991)
(E
scud
ero
et a
l. 19
91)
(Fah
ey e
t al
. 19
91)
(Upa
dhya
y et
al.
1989
) (U
padh
yay
et a
l. 19
89)
(Upa
dhya
y et
al.
1989
) (U
padh
yay
et a
l. 19
89)
(Upa
dhya
y et
al.
1989
) (U
padh
yay
et a
l. 19
89)
(O'C
onne
ll 1
988)
(O
'Con
nell
198
8)
(O'C
onne
ll 1
988)
(O
'Con
nell
198
8)
(Upa
dhya
y et
al.
1989
) (U
padh
yay
et a
l. 19
89)
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