Arthur E. Linkins

Carbon and nitrogen dynamics along the decay continuum: Plant litter to soil organic matter

Decay processes in an ecosystem can be thought of as a continuum beginning with the input of plant litter and leading to the formation of soil organic matter. As an example of this continuum, we review a 77-month study of the decay of red pine (Pinus resinosa Ait.) needle litter. We tracked the changes in C chemistry and the N pool in red pine (Pinus resinosa Ait.) needle litter during the 77-month period using standard chemical techniques and stable isotope, analyses of C and N.Mass loss is best described by a two-phase model: an initial phase of constant mass loss and a phase of very slow loss dominated by degradation of ‘lignocellulose’ (acid soluble sugars plus acid insoluble C compounds). As the decaying litter enters the second phase, the ratio of lignin to lignin and cellulose (the lignocellulose index, LCI) approaches 0.7. Thereafter, the LCI increases only slightly throughout the decay continuum indicating that acid insoluble materials (‘lignin’) dominate decay in the latter part of the continuum.Nitrogen dynamics are also best described by a two-phase model: a phase of N net immobilization followed by a phase of N net mineralization. Small changes in C and N isotopic composition were observed during litter decay. Larger changes were observed with depth in the soil profile.An understanding of factors that control ‘lignin’ degradation is key to predicting the patterns of mass loss and N dynamics late in decay. The hypothesis that labile C is needed for ‘lignin’ degradation must be evaluated and the sources of this C must be identified. Also, the hypothesis that the availability of inorganic N slows ‘lignin’ decay must be evaluated in soil systems.

Wood decomposition: Nitrogen and phosphorus dynamics in relation to extracellular enzyme activity

Because plant litter decomposition is directly mediated by extracellular enzymes (ectoenzymes), analyses of the dynamics of their activity may clarify the mechanisms that link decomposition rates to substrate quality and nutrient availability. We investigated this possibility by placing arrays of white birch sticks at eight upland, riparian, and lotic sites on a forested watershed in northern New York. For 3 yr, samples were analyzed for mass loss, protein, total Kjeldahl nitrogen (TKN), and total phosphorus (TP) accumulation, and the activity of 11 classes of extracellular enzymes involved in C, N, and P cycling. The relationship between lignocellulase activity and mass loss did not differ among sites. TKN and TP immobilization exhibited some spatial variation; rates of accumulation per 1% loss of initial mass, estimated from linear regressions, ranged from 2.2 to 4.4 mg/g OM for TP and from 43 to 139 mg/g OM for TKN, with maximum concentrations reached at °80% mass loss. The relationship between the activities of acid phosphatase (AcPase) and N—acetylglucosaminidase (NAGase), enzymes involved in the acquisition of P and N from organic sources, and mass loss displayed even greater variation among sites; the slopes of linear regressions relating mass loss and temporally integrated activity ranged from 0.019 to 0.135 activity—months per mass loss point and 0.107 to 0.775 activity—months per mass loss point, respectively, suggesting that edaphic rather than substrate quality factors were regulating activity. The extent of N limitation at each site was inferred by plotting TKN accumulation, defined as the slope of the linear regression TKN concentration vs. mass loss, in relation to NAGase activity accumulation, defined as the slope of the linear regression cumulative NAGase activity—months vs. mass loss. P limitation at each site was similarly assessed from an analogous plot of TP accumulation in relation to AcPase activity accumulation. Low N or P accumulation in conjunction with high acquisition activity was taken as an indication of nutrient limitation while the converse indicated surfeit. The diagrams suggested that decomposition at the upland hemlock and lotic sites, which displayed intermediate rates of OM loss (zero order k = 0.29 g/mo and 0.23 g/mo, respectively), was primarily N limited, while the riparian sites, which had the lowest rates of OM loss (k = 0.14 g/mo), appeared to be P limited. Relative to the others, OM loss at the upland deciduous sites (k = 0.38 g/mo) was not limited by either N or P. The concordance of field observations with predictions based on ectoenzyme regulation mechanisms suggest that enzyme activity assays in conjunction with nutrient concentration measurements may be a useful indicator of nutrient limitation. An economic model is proposed that directly links N and P availability to litter decomposition rates on the basis of microbial allocation of resources of extracellular enzyme production.

An enzymic approach to the analysis of microbial activity during plant litter decomposition

Abstract The microbial degradation of plant litter is mediated by extracellular enzymes. Their specificity makes enzyme assays useful for comparing microbial communities, monitoring community succession, evaluating the effects of disturbance or ecosystem variables on microbial processes and for studying microbial processes at the molecular level. Thus far, the application of enzymic techniques to ecological studies of plant litter decomposition has been limited. Applied in combination with general indices of microbial biomass and activity, taxonomic analyses and process rate measurements, enzyme assays offer a mechanistic approach to decomposition studies. This potential is illustrated by discussing the role of cellulase in leaf litter degradation and by proposing a conceptual model of plant litter degradation from an enzymic perspective.

Wood decomposition over a first-order watershed: Mass loss as a function of lignocellulase activity

Abstract Because plant litter decomposition is directly mediated by extracellular enzymes, analyses of the dynamics of their activity may clarify the mechanisms that link decomposition rates to substrate quality and to temperature, moisture and nutrient availability patterns. We investigated this possibility by placing arrays of white birch ice-cream sticks at eight upland, riparian and lotie sites on a forested watershed in northern New York. For 3 yr, samples were analyzed for mass loss, protein, nitrogen and phosphorus accumulation and the activity of 11 classes of extracellular enzymes involved in lignocellulose degradation and nutrient cycling. Despite considerable heterogeneity both within and between sites, decomposition rates were closely related to the activity of lignocellulose-degrading enzymes. A statistical model was developed that accounted for 94% of the variance in mass loss rates as a function of the temporally-integrated activity of these enzymes. Models of this type contribute to our understanding of scale integration and may facilitate the estimation of decomposition rates among landscape units.

Production of phenol oxidases and peroxidases by wood-rotting fungi

Quantitative studies of extracellular phenol oxidase and peroxidase production by eight species of wood-rotting fungi were performed. Coriolus versicolor, Phellinus igniarius and Lycoperdon sp. exhibited high laccase activities. Phanerochaete chrysosporium and Piptoporus betulinus produced Mn-dependent peroxidase, while Chaetomium piluliferum and C. cellulolyticum expressed low peroxidase activities. In Lenzites trabea, we did not find any extracellular oxidase or peroxidase activity. For P. igniarius and C. versicolor (one isolate) maximum specific activity of laccase was observed in trophophase, and in P. chrysosporium, maximum specific Mn-dependent peroxidase activity was observed in idiophase. We noticed marked differences in phenol oxidase activities between two strains of C. versicolor, one of them recently isolated and the other from ATCC. This result suggests that fungi can lose their abilities for enzyme production when cultured for long periods of time. Under our experimental conditions ligninase activity was not found in any of the species studied.

Temperature responses of enzymes in two forest soils.

The temperature response curves (Arrhenius plots) for endocellulase, exocellulase, exochitinase, laccase and peroxidase found in the upper horizons of a mixed hardwood and a Pinus resinosa stand in central Massachusetts were linear over the range of ambient temperatures (2–30°C). Energies of activation, determined from Arrhenius functions, are higher in mineral soil than in forest floor for endoand exocellulases and are higher for bound than for extractable endocellulases. The results are comparable with results from Arctic tundra and indicate that the potential for soil enzyme activity remains high at freezing temperatures.

The enzymic basis of plant litter decomposition: emergence of an ecological process

Abstract Plant litter decomposition is an integral process in the macronutrient cycles of ecosystems. The absence of fine-scale models for this process hampers attempts to simulate ecosystem responses to disturbance. Two recent studies have suggested that mass loss from decomposing plant litter can be directly related to the temporally-integrated activity of extracellular lignocellulose-degrading enzymes. To evaluate the generality and potential application of such relationships, we surveyed the literature and found eight studies that included mass loss data and some enzymic measure of lignocellulose degradation potential. Although the number of suitable studies was small, they encompassed a broad range of ecosystem and litter types. For all studies, there were strong linear relationships between temporally integrated enzyme activity, expressed as cumulative activity-days, and mass loss. No single enzyme gave the best fit in all cases; multiple linear regressions that included all enzymes measured within a particular study generally yielded better goodness of fit statistics than single enzyme models. Where methodological compatibility permitted, direct comparisons of apparent enzymatic efficiency (relative mass loss/activity-day) were made between studies; values for particular enzymes varied by a factor of ten and were strongly correlated with mean exposure temperature ( r 2 = 0.88). Activation energy for enzymatic decomposition was estimated at 58 kJ mol −1 . Principal components analysis (PCA) was used to generate a composite lignocellulase variable from each study, providing a common format for comparison. The results suggested that the three microcosm studies differed from the field investigations: enzymatic efficiency was approximately half that estimated for field studies and the data were more stochastic. We attributed these differences to disruptions in microbial succession caused by the lack of exogenous sources of colonists, nutrients and grazers. PCA also permitted the calculation of a global regression model for mass loss as a function of cumulative lignocellulase activity. For the five field studies, this model had an r 2 value of 0.73 in linear form and 0.76 in logarithmic form. Our analyses suggest that enzymatic decomposition models retain predictive value even when viewed from the ecosystem perspective. This hierarchal penetrance suggests useful applications: as a monitoring tool for the estimation of litter turnover in the field and as a basis for the simulation of decomposition processes at the microbial community level.

Decomposition processes: modelling approaches and applications

Abstract Decomposition is a fundamental ecosystem process, strongly influencing ecosystem dynamics through the release of organically bound nutrients. Decomposition is also a complex phenomenon that can be modified by changes in the characteristics of the decaying materials or prevailing environmental conditions. For these reasons, the impacts of local, regional or global environmental changes on the quality and turnover of dead organic matter are of considerable interests. However, realistic limits to the complexity, as well as temporal and spatial scales, or experimental studies restrict their usefulness in extrapolating long-term or large-scale results of simultaneous environmental changes. Alternatively, many simulation models have been constructed to gain insight to potential impacts of anthropogenic activities. Because structure and approach determine the strengths and limitations of a model, they must be considered when applying one to a problem or otherwise interpreting model behaviour. There are two basically different types of models: (1) empirical models generally ignore underlying processes when describing system behaviour, while (2) mechanistic models reproduce system behaviour by simulating underlying processes. The former models are usually accurate within the range of conditions for which they are constructed but tend to be unreliable when extended beyond these limits. In contrast, application of a mechanistic model to novel conditions assumes only that the underlying mechanisms behave in a consistent manner. In this paper, we examine models developed at different levels of resolution to simulate various aspects of decomposition and nutrient cycling and how they have been used to assess potential impacts of environmental changes on terrestrial ecosystems.

Cellulase activity on decomposing leaf litter in microcosms.

In this paper, we describe cellulase and cellobiose dehydrogenase (CBDH) dynamics in relation to incubation time, mass loss and chemical composition of decomposing deciduous leaf litter. Cellulose disappearance from litter coincided with periods of maximum cellulase activity. CBDH activity peaked later in decomposition after cellulase activity had declined. Enzyme activity patterns differed among litter types when expressed on the basis of decomposition time or cumulative mass loss. The patterns converged when expressed on the basis of chemical composition as indexed by the fraction of cellulose in the lignocellulose complex. We present a three-stage model of decomposition based on temporal changes in cellulase activities and coincident changes in litter chemical composition.

The root surface phosphatases ofEriophorum vaginatum: Effects of temperature, pH, substrate concentration and inorganic phosphorus

Eriophorum vaginatum L. subsp.spissum (Fern.) Hult., a dominant plant in arctic tundra ecosystems, has acid phosphatase activity evenly distributed along its root surface from the root tip to a distance at least 16 cm from the tip. These root surface phosphatases have optimal activity from pH 3.5 to 4.0; mean soil pH for soil samples collected with roots was 3.69. Apparent energy of activation and Q10 values (14.0 kcal mol−1 and 2.2, respectively) do not provide evidence for temperature acclimation, but substantial phosphatase activity was measured at 1°C. Kinetic parameters determined for this root surface phosphatase were as follows: Km=9.23 mM, Vmax=1.61×10−3 μmoles mm−2h−1. The presence of inorganic phosphorus in the assay medium did not inhibit root surface phosphatase activity except at very high concentrations (100 mM); even then, only slight inhibition was detected (7 to 19%). A comparison of hydrolysis rates with inorganic phosphate assimilation rates measured forE. vaginatum indicates that organic phosphate hydrolysis may occur at approximately one third the rate of inorganic phosphate absorption. Calculations show that inorganic phosphate produced by root surface phosphatase activity may satisfy 65% of the annual phosphate demand ofE. vaginatum. Since arctic tundra soils are typically higher in dissolved organic phosphorus compounds than in inorganic phosphate, root surface phosphatase activity may make a considerable contribution to the phosphate nutrition of this widespread and abundant arctic plant.