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Patterns in Decomposition Rates Among Photosynthetic Organisms: the Importance of Detritus C :N :P Content

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Patterns in Decomposition Rates Among Photosynthetic Organisms: the Importance of Detritus C :N :P Content Oecologia (1993) 94:457M71 Oecologia 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 chemical conditions under which the decomposition oc- between decomposition rates and detritus carbon, nitro- curs, and substrate quality (e.g. biochemical composition gen, and phosphorus concentrations was assessed by of plant litter), which constrains its suitability for micro- comparing published reports of decomposition rates of bial growth. Photosynthetic organisms can directly in- detritus of photosynthetic organisms, from unicellular fluence decomposition rates through their biochemical algae to trees. The results obtained demonstrated the composition. For instance, plants may accumulate de- existence of a general positive, linear relationship be- fence chemicals in their tissues which, besides decreasing tween plant decomposition rates and nitrogen and phos- their palatability to grazers (e.g. Coley et al. 1985), also phorus concentrations. Differences in the carbon, nitro- reduce their quality as a substrate for decomposer mi- gen, and phosphorus concentrations of plant detritus croorganisms (Swift et al. 1979). Similarly, nutrient reab- accounted for 89% of the variance in plant decom- sorption before abscission of plant tissues may, in addi- position rates of detritus originating from photosynthetic tion to improving the internal nutrient economy of the organisms ranging from unicellular microalgae to trees. plant (Chapin 1980), affect their suitability as substrate The results also demonstrate that moist plant material for microbial decomposers. decomposes substantially faster than dry material with Decomposer organisms tend to have very high nitro- similar nutrient concentrations. Consideration of lignin, gen and phosphorus contents (Findlay 1934; Thayer instead of carbon, concentrations did not improve the 1974; Swift et al. 1979; Goldman et al. 1987; Vadstein relationships obtained. These results reflect the coupling and Olsen 1989) indicative of high requirements for these of phosphorus and nitrogen in the basic biochemical nutrients. For instance balanced bacterial growth re- processes of both plants and their microbial decom- quires substrates with carbon, nitrogen, and phosphorus posers, and stress the importance of this coupling for in an (atomic) ratio of 106:12:1 (Goldman et al. 1987), carbon and nutrient flow in ecosystems. although bacteria have some capacity to vary these re- quirements (e.g. Tezuka 1990). These high nutrient con- Key words: Decomposition - Plant kingdom - Nutrients 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 Carbon fixed by photosynthetic organisms is made avail- requirements. Recent research has demonstrated that able to other ecosystem components via herbivores or bacterial growth efficiency (i.e. the fraction of the carbon detritivores. The detrital path is a major determinant of used allocated to growth) decreases about 100-fold with the flow of carbon fixed by plants in ecosystems were increasing C/N and C/P ratios in their substrate (Gold- herbivores consume a modest fraction of primary man et al. 1987). Thus, detritus with high nitrogen and production, as is often the case (Swift et al. 1979). De- phosphorus content should decompose fast because of composition of plant detritus is largely conducted by the associated fast growth of the microbial populations, bacteria and fungi (e.g. Persson et al. 1980), and the rate whereas excess carbon in the plant litter should lead to of this process depends, therefore, on all factors influenc- nutrient-controlled carbon remineralization (cf. Gold- ing their activity. These may be separated, following man et al. 1987; Vadstein and Olsen 1989). Swift et al. (1979), into abiotic factors, the physico- These arguments provide an explanation for the in- crease in decomposition rate with increasing nutrient This work was funded through a grant of CICYT (MAR91~503) concentration, or decreasing carbon/nutrient ratios, to C.M.D. demonstrated six decades ago (Tenny and Waksman Correspondence to: S. Enriquez 1929), and confirmed since for different aquatic (e.g. 458 Valiela et al. 1984; Twilley et al. 1986; Harrison 1989; days) since the initiation of the experiments using the equation, Reddy and DeBusk 1991) and terrestrial (e.g. Gosz et al. wt = Wo e-kt 1973; Swift et al. 1979; Berg et al. 1982; Taylor et al. 1989; Upadhyay et al. 1989) systems. In addition to which is the model most often used in the literature (Olson 1963) reflecting direct nutrient effects, these relationships also and simpler than the double-exponential model (e.g. O'Connell 1987). Because these decomposition rates have logarithmic units, we appear to have an indirect component, derived from a also described decomposition rates as the half-life of plant detritus tendency towards reduced carbon quality and increasing (Ta/2, days), which, although a function of exponential decom- amounts of secondary metabolites in plant litter as nu- position rates (T1/2 = k-1. In 2), provides a more intuitive des- trient availability decreases (Coley et al. 1985, Chapin et cription of detritus turnover times. Decomposition rates were often al. 1987). Hence, some ratios incorporating a descriptor reported in the studies, and were otherwise calculated from tab- of carbon quality (e.g. lignin/N ratios) have also been ulated data or digitized graphs of weight remaining with time shown to be related to decay rates of plant litter (e.g. elapsed. We included in the data set (Appendix) all studies encoun- tered during our search that included estimates of decomposition Melillo et al. 1982; Aber et al. 1990). However, lignin/N rates of plant litter (e.g. photosynthetic tissues, roots, rhizomes, ratios appear to outperform C/nutrient ratios as a predic- stems), and any of the descriptor of tissue chemical composition tor of decay rates only when comparing plant litters of needed to test our hypotheses (i.e. C, N, P, and lignin concentra- similar lignin contents (Taylor et al. 1989). tions). Whether the widespread finding of strong relation- Additional detail in the general description of the data set was obtained by grouping the data according to detritus origin (phyto- ships between litter nutrient content and decomposition plankton, macroalgae, seagrasses, freshwater angiosperms, am- rates reflects the existence of a general relationship, ap- phibious plants, sedges, mangroves, grasses, shrubs, conifers, and plicable to detritus originating from different photosyn- broad-leaved deciduous and evergreen trees). The relationships be- thetic organism, is not known as yet. The existence of tween decomposition rates and nutrient concentrations were des- such a general relationship is expected because all micro- cribed using least-squares regression analyses of log-transformed bial decomposers have high nitrogen and phosphorus, in data. Logarithmic transformation was found to be necessary to avoid heteroscedasticity in these analyses (Draper and Smith 1965). addition to carbon, needs in both aquatic (Goldman et Differences in the relationship between plant litter decomposition al. 1987; Vadstein and Olsen 1989) and terrestrial (Find- rate and nutrient content depending on detritus origin (as defined lay 1934; Thayer 1974; Swift et al. 1979) environments. above) were tested for using analysis of covariance (Draper and Conversely, these relationships might differ between dif- Smith 1966). The simultaneous influence of carbon (or lingin), ferent sorts of plant detritus if they were indirect, result- nitrogen, and phosphorus on litter decomposition rates was tested ing from covariation between carbon quality (e.g. con- for using multiple least squares regression analyses, instead of carbon/nutrient ratios, for the use of these ratios is conducive to tents of lignin, polyphenols, etc.) and nutrient content statistical artifacts (cf. Chayes 1971; Atchley and Anderson 1978). within plant types (e.g. Melillo et al. 1982; Abet et al. The (statistical) influence of nitrogen, phosphorus, carbon (or lig- 1990; Upadhyay et al. 1989). nin) contents on decomposition rates was partitioned into direct Here we examine the strength and generality of the and indirect effects using path analysis (e.g. Williams et al. 1990). relationship between decomposition rates and plant nu- Separate path analyses were used to test the effects of C, N, and P, trient concentrations by comparing published reports of 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, decomposition rates and litter nutrient contents across a which did not include any study on phytoplankton or macroalgae. 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- Results and discussion tration to statistically
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