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Using microbial and plant indicators in a preliminary analysis of the differences in successional
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trajectory within two recovering Vaccinium macrocarpon (cranberry) bogs in the New Jersey
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Pine Barrens.
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William D. Eaton, Pace University, One Pace Plaza, New York, NY 10038, weaton@pace.edu
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Daniela J. Shebitz, Kean University, 1000 Morris Ave, Fanwood, NJ 07083 dshebitz@kean.edu
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Corresponding Author: William D. Eaton, Pace University, One Pace Plaza, New York, NY 10038,
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weaton@pace.edu, 212-346-1110
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Abstract:
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The New Jersey Franklin Parker Preserve has wetlands habitat, cranberry (Vaccinium macrocarpon)
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bogs, and old growth swamps. Since 2004, once intensively managed V. macrocarpon bogs had the soil
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and peat replaced with compacted sand, recontouring of the river, and overturning soil to accelerate
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recruitment of Acer rubrum L (red maple). Other bogs were restored leaving the peat, and cleared of all
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trees. We hypothesized that the treed restored bogs will have enhanced below and above ground
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recovery ofecosystems compared to the peat-based bogs. Soil cores were collected from old A. rubrum
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swamps (M plots), young restored A. rubrum sites (RMS plots) and restored peat-based bogs (B plots)
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and analyzed for the contributions of organic C and biomass C, relative abundance of bacterial and
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fungal DNA, and the percent cover of plants plants as understory and overstory. The lower qCO2 values,
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the greater relative contribution of organic C, C biomass, and fungal to bacterial DNA ratio found in the
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M plots, followed by the RMS plots, suggest a much more efficient use of organic C is occurring in these
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soils than in the B plots, and, thus, an accelerated recovery. Consistent with this was the observed
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greater percent coverage of vegetation types in the M and RMS plots, also indicative of accelerated
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recovery. These restoration activities are enhancing the fungal and vegetation communities and
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increasing the conversion of organic C into biomass. This work documents the essential recovery that
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occurs in mid-succession swamps that was not present in this Reserve prior to restoration activity.
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Key Words:
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Wetlands restoration; organic carbon development; soil succession; Franklin Parker Preserve
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Introduction:
Increasing concern over global climate change has stimulated interest in identifying existing and
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prospective carbon (C) sinks (Euliss et al. 2006). However, limited research has been conducted to
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consider the role of wetlands in managing C sequestration (Mitsch and Gosselink 2007), even though
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both natural and constructed wetlands have great potential for C sequestration ( de Klein and van der
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Werf 2013). As wetlands occupy 7% of global land area and contribute 10% of net primary productivity
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(US Climate Tech Prog 2003), these ecosystems have a great potential for exchange of the greenhouse
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gases (Strom et al. 2005). The U.S. Climate Technology Program (2003) stated restoring lost, and
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protecting remaining wetlands, represents an immediate substantial opportunity for enhancing
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terrestrial C sequestration. In March, 2008, the US announced new standards to promote no net loss of
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wetlands (EPA 2008), while Mitsch and Gosselink (2007) argue that such efforts offer the best
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opportunity for C sequestration.
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New Jersey has lost an estimated 39% of its wetlands since the 1870s (Balzano et al. 2002). The
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US Fish and Wildlife (2005) noted that the states remaining 900,000 acres of wetlands were
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experiencing increasing stress, with approximately 150 acres of wetlands disturbed annually. The New
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Jersey Department of Environmental Protection (NJDEP) therefore established a strategic planning goal
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for wetlands to “improve quality and function and achieve a net increase by 2005”. Techniques to
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mitigate the loss of wetlands include wetland creation, enhancement, restoration, preservation and
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banking (Balanzo et al. 2002).
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To understand how such wetlands mitigation affects the sequestration of C, one must gain
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knowledge about the biota and how they are impacted by different wetlands management practices.
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Wardle (2006) and Kardol and Wardle (2010) recognized the need to identify the linkages between
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above and below-ground diversity to understand nutrient cycles and ecosystem condition, and suggest
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that the soil biota and vegetation communities associated with soils should be studied collaboratively.
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Plants have a profound influence on soil biotic communities due to unique biochemical inputs of
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different plant species (Miethling et al. 2004, Söderberg et al. 2004). The benefits of these inputs to the
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soil will change with vegetation and successional stage changes, resulting in subsequent changes to the
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soil biota and biomass, and (Doran 2002; Filip 2002; Wardle2006; Kardol and Wardle 2010; Ehrenfeld
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2012).
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Land management that decreases vegetation diversity and complexity, also decreases the soil
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ecosystem condition, and causes a shift in soil biotic diversity and complexity, affecting above- and
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below-ground C (Doran and Zeiss 2000; Shan et al. 2001; Wardle 2006; Kardol and Wardle 2010). Thus,
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changes in vegetation community structure and condition that affect plant litter, organic matter, C cycle
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dynamics, and the soil biotic community structure are of interest as potential indicators of shifts in soil
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ecosystem condition (Anderson 2003; Buckley and Schmidt 2003; He et al. 2003; Carney et al. 2004;
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Moscatelli et al. 2005; Wardle 2006; Pendall et al. 2008; Kardol and Wardle 2010).
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The Franklin Parker Preserve within the New Jersey Pine Barrens region contains 5,000 acres of
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wetlands habitat, and adjacent forests of old growth Chamaecyparis thyoides L. (Atlantic white-cedar)
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and Acer rubrum L.(red maple) swamps. Since the New Jersey Conservation Foundation (NJCF) acquired
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the Preserve in 2004, it has been restoring areas which were once intensively managed as Vaccinium
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macrocarpon Aiton (cranberry) bogs with the goal of returning them to A. rubrum and C. thyoides
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swamps, historically present in the site. In “modernized bogs”, this restoration has included removing
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the peat and reintroducing hydric soil, recreating the original flow of rivers through the bogs, and
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recontouring the terrain by overturning the compact soil to create mounds. Since the mounds were
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created starting in 2004, accelerated succession appears to be occurring as Acer rubrum from the
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neighboring swamps has become established in these recovering areas. In the “peat-based” V.
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macrocarpon bogs, both peat and hydric soil are still intact, and restoration involves clearing of trees,
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redirecting the rivers and allowing natural succession to occur. This Preserve provides excellent
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experimental conditions with which to test the effects of the restoration of V. macrocarpon bogs
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resulting in an increase in the sequestration of C.
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Little is known about the impacts that wetland disturbances, such as V. macrocarpon bog
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agriculture and its restoration may have on the above and below-ground ecosystems. This project was
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conducted to compare the trajectory towards recovery of bogs using two different restoration methods,
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by studying part of the plant and soil microbial communities, and C dynamics within V. macrocarpon
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bogs and former V. macrocarpon bogs under restoration, in comparison to that occurring in old growth
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maple forests in the Franklin Parker Preserve. We hypothesized that: 1)the old growth A. rubrum
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swamps will have more complex soil ecosystems than other habitats in the area, and will be most
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efficient at C utililization; 2) the maple recruitment and accelerated succession in the restored
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modernized bogs will result in habitats with greater efficiency of C use compared to the peat-based
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bogs. Moreover, should these hypothese be accurate, we felt it would provide important evidence for
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further implementing the accelerated succesional restoration methods.
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Methods:
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Soil Sampling and Analysis: In the Franklin Parker Reserve, four 15 m x 15 m plots were established in old
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growth A. rubrum swamps (M samples), the “modernized bog” sites with young restored A. rubrum
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(RMS samples) undergoing accelerated succession, and “peat-based” bogs undergoing natural
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succession (B samples). At the time of sampling, twenty 2 cm x 15 cm soil cores were randomly
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collected in each of the four plots and composited by plot, sterilizing between plot collections. The pH
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and % water saturation was measured at each sample site using a Kelway HB-2 Soil and pH meter
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(Wyckoff, NJ, USA), and soil samples were refrigerated. The nutrient and microbial data presented were
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adjusted for soil moisture levels.
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The rate of soil respiration (as mg CO2/g dry soil/hr) was determined using the closed system
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methods of Alef and Nannapieri (1995). The soil microbial biomass C (Cmic) was determined by the
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standard fumigation-extraction methods as the difference between K2SO4 extracted dissolved organic
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carbon (DOC) levels in ethanol-free chloroform-fumigated and unfumigated 10 g soil subsamples. The
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DOC levels were determined by the Walkley-Black rapid dichromate procedure, modified by (Nelson and
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Sommers 1996). From these, the microbial metabolic quotients (qCO2) were determined to estimate the
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efficiency of utilization of organic C. The lower the qCO2, the more efficient the soil community is at
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using organic C, converting more C into biomass (Anderson 2003). The recent approach of Blagodatskya
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et al. (2011) and Kuzyakov (2011) was used to estimate the relative contributions of DOC, respiration,
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and Cmic in of the three habitats, and to compare the estimates of the relative amounts of C turnover in
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these soils.
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For the analysis of the abundance of bacterial and fungal DNA, soil microbial community DNA
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was extracted from three 0.3-g replicate samples of pooled soil using the Power Soil DNA Isolation Kit
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(MO BIO Laboratories, Inc., Carlsbad, CA, Catalog #: 12888), the DNA extracts from each replicate then
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pooled, and the concentration determined using a Nanodrop 2000 (Thermo Scientific, Wilmington,
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Delaware, USA). The percent relative abundance (%RA) of bacterial 16s rDNA and fungal ITS region DNA
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was estimated by qPCR analysis, using the PCR primers and reaction conditions of Martin-Laurent et al.
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(2001) and Gardes et al. (1993), respectively, and a MJ Research Opticon 1 Real Time Thermal Cycler.
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Each PCR product was assessed to confirm the presence of the correct size DNA bands. For the qPCR
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analyses, the fluorescence values were determined for sample DNA and for known concentrations of
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cloned control target DNA. These values were used to compare the threshold cycle (Ct) for sample DNA
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to the Ct of the positive control DNA and to calculate the abundance of the different target gene DNA
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concentrations in relation to the total abundance for all target genes to give the %RA calculations.
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Vegetation Assessment: Five 1m2 quadrats were randomly placed within each plot to sample vegetation.
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Within each quadrat, percent cover and density was calculated for all plant species as individuals and
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collectively as part of the understory and overstory. Plant data were analyzed with indicator species
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(such as A. rubrum and V. macrocarpon) as individual units and then were classified and analyzed by
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growth habit based on the United States Department of Agriculture, Natural Resources Conservation
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Service guidelines (https://plants.usda.gov/growth_habits_def.html).
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Data Analysis: Statistical analyses were performed using the software SPSS. ANOVA and Tukey’s
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methods for Ad hoc analysis were used to demonstrate differences in mean values, and Pearson’s
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correlation analyses were also conducted to determine the strength of the relationships between
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different soil and vegetation variables. A simple regression model was used to identify the best
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combination of predictors of indicators of C use in the soils, which we determined to be DOC and Cmic.
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Results:
There were important differences in the mean values of the indicators of C use, generally
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suggesting more efficient use of C in the older maple forest (M) followed by the RMS soils (Tables 1 and
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2). The DOC and Cmic levels were greater in the M soils than in the RMS (p = 0.011 and 0.008) and the B
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soils (p = 0.005 and 0.025), and the RMS soils also had greater levels of these than the B soils (p = 0.025).
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The levels of respiration were fairly similar at all three habitats (4.8-5.4 mg CO2/g dry soil/hr), but as the
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DOC was much greater in the two maple forest habitats, this made the qCO2 values much less in these
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soils than in the B samples (p < 0.001). As well, the qCO2 values were lower in the M than the RMS soils
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(p = 0.089). The relative abundance of bacterial DNA estimated to be in the soils was greater in the B
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soils than the M (p = 0.008) and RMS soils (p = 0.07). The relative abundance of fungal DNA was greater
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in both the M and RMS than the B soils (p = 0.002 and 0.011). Similarly, the ratio of fungal to bacterial
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DNA was greater in the M than either the RMS (p = 0.018) or the B soils (p = 0.002). The RMS soils had a
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greater fungal to bacterial DNA ratio in comparison to that of the B soils, but the difference between
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these was less important (p = 0.142). There were greater relative contributions (Table 3) of organic C,
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CO2 and Cmic comparing the M to the RMS and B soils, but greater relative contributions of organic C
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and Cmic in the RMS than the B soils. As well, the relative amount of C turnover was also greater
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comparing the M to RMS (2.26x greater) and B soils (2.96x greater), and comparing the RMS to the B
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soils (2.6x greater).
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Important differences were found in the vegetation characteristics between the three habitats
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(Table 4). The M sites had greater percent coverage overstory of trees (p = 0.001), A. rubrum specifically
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(p < 0.0001), and vines (p = 0.104) than found in the B sites. The B sites had greater percent coverage of
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understory vegetation, V. macrocarpon, and graminoid species (all p values <0.0001). The RMS plots had
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the least amount of graminoids, V. macrocarpon and understory, and the greatest amount of overstory
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and maple trees (all p values <0.0001 to 0.071), as they represent sites that were recently altered from
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former bogs, with A. rubrum growing in high densities on these restored modernized bog sites from the
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neighboring swamps by natural seeding. Thus, there is less understory at this point, and a greater
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percent of young trees providing the overstory. A good indicator of forest age is the percent of coverage
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of vines, which was greater in the M sites than the RMS sites (p = 0.099), and in the RMS compared to
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the B sites (p = 0.104).
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Strong correlations were found between critical indicators of C use efficiency (Table 5). The
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levels of DOC were correlated with levels of Cmic (r = 0.874, p <0.009), the qCO2 (r = -0.858, p <0.009),
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relative abundance of fungal DNA (r = 0.745, p = 0.005), relative abundance of bacterial DNA (r = -0.614,
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p = 0.034), and the ratio of fungal to bacterial DNA (r = 0.711, p = 0.01). The levels of Cmic were
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additionally correlated with the qCO2 (r = -0.914, p <0.009), relative abundance of fungal DNA (r = 0.739,
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p = 0.006), relative abundance of bacterial DNA (r = -0.662, p = 0.019), and the ratio of fungal to
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bacterial DNA (r = 0.731, p = 0.009). The levels of qCO2 were also correlated with the relative abundance
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of fungal DNA (r = -0.724, p = 0.007), relative abundance of bacterial DNA (r = 0.699, p = 0.011), and the
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ratio of fungal to bacterial DNA (r = -0.739, p = 0.006).
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Strong correlations were also found between some of the different indicators of more complex
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habitats (i.e., % Overstory, % A. rubrum, and % Vines), the indicators of less complex habitats (i.e.,
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%Understory and % V. macrocarpon) and the nutrient chemistry and microbial indicators (Table 6.). The
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water saturation levels were negatively correlated with the % overstory and red maple coverage (r = -
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0.963 to -0.931, p < 0.0001) and positive correlated with % understory, V. macrocarpon, and graminoid
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coverage (r = 0.707 to 0.941, p < 0.0001). The pH levels were positively correlated with the % overstory
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and A. rubrum coverage (r = 0.770 to 0.797, p = 0.002 to 0.003) and negatively correlated with %
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Understory and V. macrocarpon (r = -0.676 to -0.497, p = 0.016 to 0.100). The DOC and Cmic were
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negatively correlated with % Understory (r = -0.457, p = 0.135, and r = -0.738, p = 0.006) and V.
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macrocarpon (r = -0.473, p = 0.155, and r = -0.746, p = 0.006), and the Cmic positively correlated with %
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overstory (r = 0.427, p = 0.159) and A. rubrum coverage (r = 0.446, p = 0.141). The qCO2 (i.e., the
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metabolic quotient) was negatively correlated with the indicators of a more complex vegetation
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composition (% overstory coverage: r = -0.572, p = 0.052; and %A. rubrum coverage r = -0.528, p = 0.078)
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and positively correlated with indicators of a less complex vegetation composition (% understory
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coverage: r = 0.709, p = 0.010; % V. macrocarpon coverage: r = 0.893, p < 0.0001; % graminoid coverage:
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r = 0.635, p = 0.026). The %RA of the fungi and the fungal/bacterial ratio were positively correlated with
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the %overstory coverage (r = 0.494 to 0.794, p = 0.084 to 0.151) and % A. rubrum coverage (r = 0.528 to
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0.721, p = 0.030 to 0.147). These three metrics were also negatively correlated with indicators of less
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complex vegetation composition (% understory coverage: r = -0.557 to -0.411, p = 0.127 to 0.145; % V.
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macrocarpon coverage: r = -0.661 to -0.561, p = 0.019 to 0.058; % graminoid coverage: r = -0.551 to -
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0.451, p = 0.076 to 0. 155). The %RA of bacteria was negative correlated with the indicators of a more
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complex vegetation composition (% overstory coverage: r = -0.455, p = 0.158; and % A. rubrum coverage
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r = -0.426, p = 0.168) and positively correlated with indicators of a less complex vegetation composition
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(higher % V. macrocarpon) coverage: r = 0.725, p = 0.008; % graminoid coverage: r = 0.485, p = 0.110).
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The regression model we developed was based on the idea that the greater complexity of
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vegetation was strongly correlated (both positive and negative correlations) with a number of the
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nutrient and microbial parameters. Thus, we focused on the nutrient and microbial indicators that best
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predicted Cmic and DOC as indicators of below and above ground habitat condition. The resulting
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regression model showed that DOC, qCO2, relative abundance of fungal and bacterial DNA, and the ratio
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of fungal to bacterial DNA were good predictors of Cmic levels in soils with an adjusted R2 value = 0.76,
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R2 change value = 0.869, F of the change value = 7.98, and p of the change value = 0.013. Similarly, the
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regression model developed showed that Cmic, qCO2, relative abundance of fungal and bacterial DNA,
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and the ratio of fungal to bacterial DNA were good predictors of DOC levels in soils with an adjusted R2
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value = 0.651, R2 change value = 0.809, F of the change value = 5.10, and p of the change value = 0.036.
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Discussion
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Scientists around the world are developing and attempting to use indicator methods to
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characterize ecological differences between habitats, assess ecosystem condition within these habitats,
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and to identify the efficacy of restoration and other management strategies. For such assessments to be
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effective, it is critical to identify metrics that can demonstrate biologically important differences
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between habitats, and are also likely to provide early evidence of ecosystem damage and/or recovery.
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Wetlands are one habitat type that have been significantly disturbed around the world. Healthy wetland
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ecosystems exhibit high levels of productivity, accumulate large below ground stocks of C, and have a
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great potential for exchange of the GHG with the atmosphere, thus providing a significant potential
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source for C sequestration. However, little is known of the above and below ground ecology and C
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sequestration potential in these fragile systems (US Climate Technology Program 2003; Strom et al.
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2005; Mitsch and Gosselink 2007). This current project represents one of the few that have studied how
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restoration of a wetlands previously disturbed for commercial purposes can impact the above and
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below ground biota, and the C cycle dynamics. Trends found in this study provide support for the use of
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the metrics presented as indicators of success in wetlands management and restoration projects.
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The data from this project provide a very clear indication that the restoration activities
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implemented in the bogs within the Franklin Parker Reserve are having a positive effect of recuperating
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the abilities of the soils to turnover both CO2 and organic C into biomass. The data show that the
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amount of organic C and C biomass were greater in the A. rubrum swamps and recovering maple site as
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compared to the peat-based bog plots, which suggests an accelerated recovery in bogs that were
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actively restored to enhance succession. The much lower qCO2 values found in the existing swamp and
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the recovering maple site suggest a much more efficient use of organic C is occurring in these soils.
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Consistent with this analysis, the relative contribution of organic C and C biomass was about 25% to 90%
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greater in the old swamps and restored RMS plots as compared to the peat-based bog plots, and the
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estimate of the turnover of organic C and CO2 into biomass was about 2.5 to 3 times greater in the two
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different habitats with maple trees. It appears that the relative abundance of bacterial DNA was greater
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in the peat-based bog soils, and that of the fungal DNA was greater in the maple swamp and RMS soils.
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This resulted in a much greater fungal to bacterial ratio in both the young and older maple forest soil. An
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increase in this ratio often occurs as a result of an increasing fungal biomass in comparison to a
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relatively static bacterial biomass (Ohtonen et al. 1999; Van der Wal et al. 2006), and suggests there is
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an increase in the amount of organic C being made available for transfer up the food web (Anderson
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2003; Moscatelli et al. 2005). These data suggest a greater efficiency of C use in the old maple swamps
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and RMS sites consistent with the increased percent coverage of vegetation types more common in
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older forests observed in this study.
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Many studies have shown that comparisons of the fungal to bacterial ratios, the organic C, the
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respiration activity, the biomass, and qCO2 in soils can serve as good indicators of soil ecosystem
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condition (e.g., Anderson 2003; He et al. 2003; Moscatelli et al. 2005). More recently, Blagodatskya et
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al. (2011) and Kuzyakov (2011) showed that by using some of the same C-related measurements
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traditionally collected, one can provide estimates of the relative contribution of organic C and biomass C
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and the turnover estimates in soils, and that these are also good indicators of the condition of soil
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ecosystem functioning. The connection between these soil C and biotic metrics with differences
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observed in the vegetation community structure and condition is important. There is a complex
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relationship between changes in plant diversity, abundance, and litter quality and increases in plant-
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derived carbohydrates, lignin, celluloses and other more recalcitrant organic compounds, increased soil
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complexity and soil biomass development (e.g., Anderson 2003; He et al. 2003; Moscatelli et al. 2005;
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Bradford et al. 2008). Based on these accepted concepts, it appears clear that the differences in
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vegetation structure between the old maple swamp, the recovering maple swamp, and the peat-based
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bog are playing critical roles in the soil microbial community and the dynamics of the C cycle and
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biomass development within these habitats. The increase in vegetation diversity and biomass observed
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in the two maple forests are likely resulting in greater production of lignins and other more recalcitrant
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organic compounds which would select for fungi that degrade these materials (de Boer et al. 2005;
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Bradford et al. 2008; Sinsabaugh 2010), stimulating microbial-directed processes that enhance the soil
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organic matter complexity, decomposition, soil respiration, and mineralization of organic matter, and
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subsequent increases in organic compounds and soil biomass, a more efficient use of the soil organic
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matter, and more organic C available to the foodweb—thus enhancing the potential for C sequestration
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(Anderson 2003; He et al. 2003; de Boer et al. 2005; Moscatelli et al. 2005; Schwendenmann and
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Veldkamp 2006; Fierer et al. 2007; Bradford et al. 2008; Eaton et al. 2012).
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Few models are available that show trends in restoration of wetlands. In this study, it was
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shown using correlations and a simple linear regression model that organic C, soil C biomass, abundance
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of fungal and bacterial DNA, the ratio of fungal to bacterial DNA, and the qCO2 were well-correlated
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(both positive and negative correlations) with each other. As well, the qCO2 and amount of fungal DNA
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were well-correlated with a number of the vegetation-based indicators of later stages of succession. In
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particular, the % coverage of graminoids, V. macrocarpon, understory, overstory, A. rubrum , and the
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tree density were all tightly linked with the qCO2, the fungal DNA, and ratio of fungal to bacterial DNA.
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We suggest that the below ground metrics of the qCO2, fungal DNA, and the ratio of fungal to bacterial
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DNA, along with the above ground metrics % coverage of graminoids, V. macrocarpon, understory,
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overstory, and maple trees, be used in longer-term trials as good indicators of soil and overall ecosystem
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recovery following restoration processes in these swamps. From such an analysis we would expect to be
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able to develop a predictive model for soil recovery for these and other wetlands following restoration
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implementation.
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Clearly, then, the restoration activities used at the Franklin Parker Reserve are greatly affecting
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the microbial and vegetation communities and associated nutrient cycle dynamics. The increased
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abundance of woody vegetation in the recovering maple swamp is likely enhancing the microbial
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community, specifically the fungus. This acceleration of soil biotic recovery is likely increasing the
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amount of decomposition of plant material to be converted into more organic material for use in the
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greater development of soil C biomass in the forested areas as compared to the bogs. These findings are
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indicators of a greater efficiency of C use and a greater potential for increased C sequestration in the
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recovering maple swamp.
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In an intact Pine Barrens habitat, there is a natural mosaic of bogs and swamps in various stages
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of succession. By virtue of past land management practices in the area, there has been an absence of
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mid-succession swamps. The peat-based bogs and the later stage succession swamps in the Franklin
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Parker Preserve continue to provide vital ecosystem services. Our research has documented the benefit
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of the essential recovery that occurs in the mid-succession swamps that were not present prior to
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implementation of the accelerated succession restoration activity. This study provides evidence that
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others with regulatory control over other damaged wetlands should model the Franklin Parker Reserve
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restoration strategies.
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Acknowledgements
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The authors wish to thank Kean University for its support of this project through its Presidential Scholars
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Challenge grant program; Kathleen McGee, Kate Niemiera for their help in collecting soil and vegetation
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samples; and Emile DeVito for assistance and access to the Pine Barrens restoration sites.
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