Magnitude and Trophic Fate of Black Needlerush (Juncus Roemerianus) Productivity: Does Nutrient Addition Matter?
Amy Hunter, Just Cebrian, Jason P. Stutes, David Patterson, Bart Christiaen, Celine Lafabrie & Josh Goff
Wetlands Official Scholarly Journal of the Society of Wetland Scientists
ISSN 0277-5212
Wetlands DOI 10.1007/s13157-014-0611-5
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Wetlands DOI 10.1007/s13157-014-0611-5
ORIGINAL RESEARCH
Magnitude and Trophic Fate of Black Needlerush (Juncus Roemerianus) Productivity: Does Nutrient Addition Matter?
Amy Hunter & Just Cebrian & Jason P. Stutes & David Patterson & Bart Christiaen & Celine Lafabrie & Josh Goff
Received: 7 July 2014 /Accepted: 10 December 2014 # Society of Wetland Scientists 2014
Abstract The black needlerush (Juncus roemerianus)isa nutrient dose rates at which significant impacts occur on plant common plant species in saltmarshes of the Gulf of Mexico. productivity and trophic fate in these and other marshes de- Our knowledge of the trophic fate of the plant’sproductivity, serves more research. which is important for an understanding of marsh functional- ity, is incomplete. Here we examine the productivity and Keywords Nutrient enrichment . Black needlerush . Primary trophic fate (herbivory, decomposition and biomass storage) productivity . Herbivory . Decomposition . Resiliency of two black needlerush-dominated marshes in the northern Gulf of Mexico. We also investigate the effects of low inten- sity, short duration (1.5 years) nutrient inputs. The marshes Introduction experienced low rates of leaf herbivory and decomposition, thereby leaving most leaf production available for storage in Coastal marshes provide a number of ecosystem services. the marsh or export to other systems. The marshes also fea- They constitute important habitat for many invertebrate and tured large pools of belowground biomass, which indicates an vertebrate organisms, including commercially valuable spe- important role as carbon reservoirs. Our nutrient inputs did not cies (Minello et al. 2003, Moody et al. 2013a), owing to their affect significantly the plant’s productivity and trophic fate. structural complexity. They also buffer wave energy and These results suggest black needlerush marshes may be resis- enhance sediment deposition and, in doing this, they help tant to low intensity, short-term nutrient inputs. However stabilize shorelines and protect coastal land against wave studies with other marsh plants have shown that longer, more scouring and storm surge (Morgan et al. 2009, Moody et al. intense nutrient inputs may lead to larger and diverse effects 2013b). Coastal marshes are also important carbon traps. They on plant productivity and trophic fate. Establishing the store large amounts of organic carbon in the soil and represent significant carbon sinks, thereby helping to palliate rising A. Hunter atmospheric CO2 levels (Chmura et al. 2003, Bridgham Department of Biological Sciences, University of Alabama, et al. 2006, Langley and Megonigal 2010). Tuscaloosa, AL 35487, USA The black needlerush (Juncus roemerianus) is a ubiquitous macrophyte in salt marshes of the northern Gulf of Mexico A. Hunter : J. Cebrian (*) : J. P. Stutes : D. Patterson : B. Christiaen : J. Goff (Eleuterius 1976). Research on the ecosystem services pro- Dauphin Island Sea Lab, 101 Bienville Blvd., Dauphin Island, vided by black needlerush-dominated marshes is meager in AL 36528, USA comparison with other marshes, such as smooth cordgrass e-mail: [email protected] (Spartina alterniflora)-dominated marshes. Documenting the J. Cebrian : B. Christiaen trophic fate of black needlerush primary productivity can Department of Marine Sciences, University of South Alabama, improve our understanding of the ecosystem good and ser- Mobile, AL 36688, USA vices provided by black needlerush-dominated marshes. This is because the trophic fate of primary productivity conditions a C. Lafabrie ECOSYM, Ecology of Coastal Marine Systems, 2 Place Eugène number of ecosystem services. Consumption by first-order Bataillon, 34095 Montpellier Cedex 5, France consumers corresponds to the flux of matter channeled from Author's personal copy
Wetlands plants to herbivores, detritivores and decomposers, which sets the ecosystem services provided by marshes. For instance, a minimum limit to the quantity of consumer productivity fertilization could increase the nutritional quality of marsh maintained in the system (i.e. an additional fraction of con- plants for first-order consumers (i.e. herbivores, detritivores sumer productivity could be fueled with allochthonous organ- and decomposers), thereby leading to higher rates of herbiv- ic import, Polis and Hurd 1996; Cebrian 2002). The excess of ory and decomposition, higher abundances of first-order con- productivity not consumed by first-order consumers can be sumers, and larger food availability for higher trophic-level exported out of the system or stored as organic matter within organisms (Sterner and Elser 2002; Cebrian and Lartigue the system. Organic matter storage denotes the capacity of the 2004). Conversely, increased decomposition rates could re- system to act as a carbon reservoir; systems with high primary duce the accumulation of refractory detritus and depress the productivity and low herbivory and decomposition rates store role of the marsh as a carbon reservoir. Accordingly, in a press large carbon pools (Mateo et al. 2006; Cebrian et al. 2009a). nutrient addition experiment that lasted 4 years, Murphy et al. A number of reports have addressed the trophic routes of (2012) found higher leaf nutrient contents, higher abundances black needlerush productivity separately. Parson and de la and plant consumption rates for a number of herbivorous Cruz (1980) recorded low levels of herbivory on black arthropods, and higher abundances of the detritivorous arthro- needlerush leaves and concluded that most leaf productivity pods Venezillo sp. in fertilized than non-fertilized plots of entered the detrital compartment in their study site. Most S. alterniflora. Increased herbivory and decomposition, and studies have focused on the plant’s detritus and have shown depressed refractory accumulation have been observed in low decomposition rates for leaf detritus (de la Cruz and response to fertilization in a number of aquatic and terrestrial Gabriel 1974, Stout and de la Cruz 1981, Christian et al. systems (Gruner et al. 2008). 1990) or rhizomes and roots detritus (Hackney and de la Cruz Past reports have examined the impacts of fertilization on 1980). This suggests that most black needlerush detritus is diverse characteristics of the black needlerush, such as growth available for export to other systems or storage as recalcitrant and biomass, intra- and inter-specific competition, and nutri- material in the system, which is in agreement with the large ent uptake and storage (Gallagher 1975; Pennings et al. 2002; pools of belowground detritus recorded for black needlerush Brewer 2003). However, our knowledge of how nutrient marshes (Gabriel and de la Cruz 1974,delaCruzandHackney enrichment affects the trophic routes of black needlerush 1977; Hackney et al. 1978). However, our characterization and primary productivity is scant. To date we only know of one understanding of the trophic fate of black needlerush produc- study that has partially addressed this question. Sparks and tivity is far from complete. In particular, no study exists that Cebrian (2014) carried out a fertilization experiment in a black addresses several routes simultaneously (e.g. herbivory, decom- needlerush marsh and found increased herbivory on fertilized position, and storage). than non-fertilized leaves. To help fill this gap, here we assess These various ecosystems services that black needlerush the impacts of fertilization on a number of trophic routes of and other marshes provide are lost following marsh decima- black needlerush productivity in two marshes of the northern tion by human activities. Marshes are being decimated at Gulf of Mexico, namely plant biomass and productivity, her- alarming rates worldwide (Mcleod et al. 2011; Pendleton bivory, decomposition and organic matter storage. We focus et al. 2012), and black needlerush marshes in the northern on low-intensity, short term nutrient enrichment, a form of Gulf of Mexico are no exception (Turner 1990;Sparksetal. nutrient loading that has been understudied (Table 1) but that 2013). Multiple stressors, which often operate in concert and may occur frequently through faulty septic tanks, fertilizer may include human land use, altered climate, eutrophication, leaching, and spills and runoff (Lehrter and Cebrian 2010; and sea level rise, cause marsh decline (Duarte et al. 2008, Sparks et al. 2014). Rabalais et al. 2009,Muddetal.2009; Pendleton et al. 2012). In particular, excessive nutrient inputs may lead to marsh loss. Deegan et al. (2012) reported that 9 years of continued fertil- Methods ization led to decreased belowground plant biomass and in- creased decomposition of sediment organic matter in marshes Study Site of the Plum Island estuary (Massachusetts, USA). This in turn led to reduced structural integrity and geomorphological sta- This research was conducted in two coastal marshes of Big bility of the marsh banks and caused extensive marsh loss. Lagoon (Perdido Bay, Florida, USA). The area studied was Other authors have also suggested that prolonged intense located at the marsh mid elevation range and dominated by eutrophication may cause marsh decline through reduced black needlerush. Both marshes circumscribe shallow embay- rhizome and root biomass and depressed belowground struc- ments that are subject to small tidal oscillations (<0.5 m). One tural integrity (Hartig et al. 2002; Turner 2011). of the marshes is bordered by maritime forest and surrounds However, moderate nutrient loading may not necessarily the embayment named East Cove (30°18′29″N, 87°24′11″W), be detrimental for marshes, but rather have varying impacts on which is situated in the Big Lagoon Florida State Park . The Author's personal copy
Wetlands
Table 1 Nutrient dosage used in marsh fertilization studies (N: dosage rates, we compiled values used in marsh fertilization nitrogen; P: phosphorus) studies (Table 1) and, in light of the values obtained, we Dosage rate (g m−2 yr−1) Reference applied 15 g nitrogen (N, applied as ammonium nitrate - −2 −1 NH4NO3-) m yr and 1.6 g phosphorus (P, applied as triple NP −2 −1 phosphate -P2O5-) m yr . In addition, we applied these dosage rates following two 372 8.8 Darby and Turner 2008a methods. First, in 2003 we used a point-input, subsurface 17.4–224.6 4.6–6.6 Darby and Turner 2008b method where the fertilizer was placed in nylon bags and 139.2 14.4 Emery et al. 2001 lowered to the bottom of 2.5 cm diameter PVC wells. The 365 402 Huang and Morris 2005 wells were inserted to a depth of 30 cm within the marsh soil, 318–400 223.2 Jefferies and Perkins 1977 which corresponds to the depth range of the rhizosphere. 208.8 21.6 Levine et al. 1998 Holes were drilled in the lower 20 cm of the well to enable 420 465 Morris and Bradley 1999 porewater flow and the release of fertilizer out of the well. The 61.2 81 Murphy et al. 2012 perforated portion of the well was covered with geo-textile 417.6 43.2 Pennings et al. 2002 cloth to prevent clogging, and the top of the well capped with 10.1–30.2 6.1–18.1 Valiela et al. 1975 removable lids. Six wells were evenly distributed within each 11.8–35.3 7.1–21.2 Valiela et al. 1976 fertilized plot (Fig. 1). Fertilizer was put in the wells on 360 Boyer and Zedler 1999 December 27, 2002; March 14, 2003; July 13, 2003; and 139.2 Brewer 2003 November 9, 2003. The second method consisted of hand- 48 Foster and Gross 1998 broadcasting the fertilizer over the plot. Specific application 20 Gallagher 1975 dates were January 20, April 16, and July 5 in 2004. 17 Gough and Grace 1997 17 Gough and Grace 1998 140 McFarlin et al. 2008 Variables Measured 200 Mendelssohn 1979 44 Newell et al. 1996 We did not sample the plots prior to starting fertilization. This, however, should not affect our conclusions because earlier 10 Van der Graaf et al. 2007 work done in the lagoons revealed the marsh areas studied 15 1.6 This work here have similar ambient characteristics (Hunter 2005). We
8 m other marsh is partially developed by residential housing and surrounds the embayment named Kee’s Bayou (30°18′47″N, 87°28′8″W). More information about these sites is provided in Wells for measurements of porewater nutrient concentraon Stutes et al. (2007) and Cebrian et al. (2009b).
Experimental Design Area for Locaons for measurements herbivory We fertilized four plots and left four unfertilized (control) of leaf producvity plots within the black needlerush monospecific zone in each measurements marsh. Plots were situated at a similar elevation (i.e. mid marsh). Control and fertilized plots were set up in blocks, with Area for each block having one fertilized and one control plot. Plots decomposion were placed randomly within each block. Plots were 8 m×8 m measurements and separated 4 m from each other within a block. Adjacent blocks were 5 m apart. We purposely chose to apply low nutrient dosage to our plots since our intent was to focus on the effects of low Wells for point-input ferlizer intensity, short-term nutrient enrichment that may occur from applicaon faulty septic tanks, fertilizer leaching, and/or spills and runoff. This form of nutrient enrichment has been little addressed in Fig. 1 Locations in the experimental field plots for measurements of leaf comparison with more intense, prolonged enrichment (Lehrter productivity, herbivory, decomposition and porewater nutrient and Cebrian 2010; Sparks and Cebrian 2014). To inform our concentrations; and point-input, subsurface application of fertilizer Author's personal copy
Wetlands started sampling response variables at different times due to of the samples in a Shimadzu UV-160 spectrophotometer logistic reasons (i.e. equipment and labor limitations). (Strickland and Parsons 1972; Solorzano and Sharp 1980; Fourqurean et al. 1992). To derive C:P ratios, phosphorus Porewater Nutrient Concentrations Sediment porewater was concentrations were combined with the C concentrations ob- sampled 15 times at approximately monthly intervals from tained with the ECS 4010 CHNS-O Analyzer. February 2003 to October 2004. Porewater was collected in three wells constructed as explained above for subsurface Productivity We used the method presented by Williams and fertilization. The three wells were located along the central Murdoch (1972) and Hopkinson et al. (1980) to measure leaf axis of the plot and were sided by two rows of point-input, productivity. In January 2003 we tagged all the leaves on five subsurface fertilization wells (Fig. 1). On each sampling date, shoots within each of three different locations in each of the the porewater within the well was pumped out with a syringe plots (Fig. 1) for a total of 15 tagged shoots per plot and 120 into acid-washed plastic vials and stored on ice until process- tagged shoots per site. The same shoots were visited season- ing. Upon return to the laboratory, all samples were filtered ally through July 2004. On each visit, we tagged the new through 25 mm Whatman GF/F filters and frozen until anal- leaves that had appeared during the interval (i.e. leaves bear- − − + ysis for nitrite (NO2 ), nitrate (NO3 ), ammonium (NH4 ), ing no tag), recorded the green and total (i.e. green plus + and phosphate (PO4 ) following standard wet chemical tech- brown) length of each leaf, noted whether the leaf was intact niques (Strickland and Parsons 1972) modified for the Skalar or broken, and recorded the number of shed leaves. New SAN+ Autoanalyzer (Pennock and Cowan 2001). To ensure shoots were tagged as needed to replace senescing shoots. that the samples obtained within the well reflected closely the Leaf growth for intact leaves was measured as the increase in conditions found in the sediment porewater around the well at total length over the interval. Leaf growth for broken leaves the time of sampling, on a few sampling dates early in the was measured as the increase in green length. Leaf growth experiment we pumped the wells dry after obtaining the measurements for broken leaves may be underestimates, how- samples, let them recharge overnight, and took another round ever the extent of underestimation should be small because of samples on the following day. In general porewater con- broken leaves are generally old and display little or no growth. centrations did not differ between the 2 days, indicating that Growth for all the leaves on the same shoot was pooled to our samples were generally representative of the conditions derive growth per shoot, and, for each season, growth on an around the wells at the time of sampling. areal basis (g DW per square meter of marsh per season) was calculated using the values of shoot density and leaf specific Biomass In January, April, July and October 2003 and Janu- weight (mg DW per cm of leaf) obtained from the biomass ary, April and July 2004 we measured black needlerush samples. aboveground and belowground biomass in each plot by hap- We used the maximum-minimum biomass method to esti- hazardly tossing a 25×25 cm2 quadrat in the plot once and mate belowground productivity (de la Cruz and Hackney harvesting all enclosed above- and belowground material. 1977). This method estimates annual belowground productiv- Samples were returned to the laboratory and the above- and ity as the difference between the maximum (normally found in belowground material rinsed off and separated. Shoots were winter/spring) and minimum (normally found in summer/fall) counted and the green and brown (i.e. senesced) length of each values observed in the annual cycle of belowground plant leaf measured. Roots, rhizomes and leaf green and brown mass (i.e. living and dead rhizomes and roots). We used the fractions were dried (90 °C for 2–4 days) and weighed full year July 2003 (6 months after the onset of fertilization) to separately. No effort was made to separate living from July 2004 (end of the experiment). Minimum biomass values dead tissue in the belowground parts (i.e. roots and rhi- of rhizomes and roots (living and dead) during that full year zomes) since that is extremely difficult and impractical occurred in October 03, and maximum values occurred in (de la Cruz and Hackney 1977). January 04. For each replicate plot we calculated belowground productivity for rhizomes and roots separately as the differ- Carbon:Nutrient Ratios We measured Carbon:Nitrogen ence between the maximum and minimum values. (C:N) and Carbon:Phosphorus (C:P) atomic ratios of plant aboveground and belowground parts three times during the Herbivory We measured the consumption of leaf biomass by course of the experiment: January, April and July 2004. We grasshoppers. Grasshoppers account for most of the herbivory haphazardly subsampled live and dead leaves, and root/ on black needlerush in the Gulf of Mexico (Wason and Pennings rhizome material from each biomass sample on each date. 2008). The grasshoppers have a marked annual cycle. The Tissues were ground using a Wiley Mill. A Costech Elemental nymphs hatch in spring, feed on black needlerush leaves and Combustion System (ECS 4010 CHNS-O Analyzer) was used grow through late summer, and the adults breed and die off in to determine C:N ratios. Phosphorus concentrations were early fall (Smalley 1960; Parsons and de la Cruz 1980). We used determined by measuring the phosphorus-specific absorbance the method presented by Sand-Jensen et al. (1994)andCebrian Author's personal copy
Wetlands et al. (1994) to quantify herbivory by grasshoppers in the number was less for the subsequent deployments. We did not summers of 2003 and 2004. This method calculates leaf con- deploy new bags when we switched from the point-input, sumption as the product between the number of leaves grazed subsurface to the hand-broadcasting fertilization method be- per square meter of marsh and the mean biomass removed per cause that new decomposition run starting in January 2004 grazed leaf. Grazed leaves were counted three times during each would have encompassed only some 7 months before the summer within a marked two m2 area at each plot (Fig. 1). To conclusion of the experiment, and this would have likely been calculate the mean biomass removed per grazed leaf, we har- too short of a time period to obtain accurate decomposition vested 25 grazed leaves within the plot but outside the two m2 measurements for black needlerush marshes. area on the same day where grazed leaves were counted. We Upon retrieval, bags were returned to the laboratory and the harvested grazed leaves outside the two m2 area to avoid affect- detritus remaining in the bag was carefully extracted, cleaned ing subsequent counts of grazed leaves (i.e. if we had harvested of attached sediment, and oven dried. Dried weights were grazed leaves within the two m2 area, those leaves would not recorded and decomposition rates estimated from the decrease have been counted on the next sampling visit). over time in the detritus mass remaining in the bags. For each The grazed leaves were brought to the lab. We calculated of the different runs (starting in February, April, July, and the volume (cm3) that the grazed portion of the leaf would November 2003) we derived the decomposition rate at each have if ungrazed following the volume equation for a cylinder of the eight plots in each site by fitting a log-transformed based on the diameter of the base and length of the grazed single exponential decay model to the data: portion. This volume was converted into weight using leaf tissue density (mg dry weight per cm3 of leaf). Finally, the ðÞ= ðÞ biomass consumed per grazed leaf was calculated as the ln Detritus mass retrieval Detritus mass beginning difference between the estimated weight of the grazed portion ¼ –ðÞΔ ðÞ had the portion been ungrazed and the actual weight of the C kx t 1 grazed portion. A mean value of biomass consumed per grazed leaf was calculated for each plot from the grazed leaves collected in the plot.
where (Detritus mass)beginning corresponds to the detritus mass Decomposition Leaf decomposition was measured using the enclosed in the bag at the beginning of the run, (Detritus litter-bag method (Stout and de la Cruz 1981; Christian et al. mass)retrieval corresponds to the detritus mass remaining in 1990). Mesh bags 80 cm tall×10 cm in diameter made of 1- the bag at retrieval, k is the decomposition rate, and Δt corre- mm mesh were used. Prior to deployment, standing senesced sponds to the time elapsed from the beginning of the run to leaves were harvested from the plots, air-dried for a few days retrieval. All fits were significant (P<0.05) and had coeffi- to a constant weight, and a known weight of leaf detritus cients of determination (R2) greater than 0.5, except in two enclosed in each bag. Air-dried weights were transformed into cases where 0.05 Wetlands seasonal and, in addition, we applied two fertilization repeated-measures ANOVA to analyze porewater nutrient methods). We used ANOVA to analyze all these factors in concentrations since we obtained the samples repeatedly concert. from the same wells. Time was the within-subject factor, The black needlerush is a clonal plant. Shoots pro- and treatment (control vs. fertilized) and site (State Park duced by the same rhizome correspond to a genetically vs. Kee’s Bayou) were the between-subject factors. Post- identical individual (i.e. genet). Because we sampled hoc comparisons were carried out as pertinent with plants over time within the same plot that most likely Tukey tests. Belowground productivity and leaf decom- corresponded to the same genetic individual (this was position were analyzed using regular two-factor ANOVA certainly the case for our measurements of aboveground (treatment and site as factors). For decomposition a dif- productivity), we used repeated-measures ANOVA to ferent ANOVA was done for each run, and for each run analyze plant biomass, carbon:nutrient ratios, above- the adjusted decomposition rates (one per plot) were ground productivity, and herbivory. We also use compared between treatments and sites. We did not find Fig. 2 Porewater nutrient concentrations in non-fertilized (C, open circles) and fertilized (F, closed circles)plots.Thedashed line represents the shift in the method of fertilizer application (see text). Values are means for 4 plot replicates and bars are SE Wetlands Table 2 Results of repeated-measures ANOVA Porewater N concentration Porewater P concentration Aboveground live biomass Aboveground dead biomass Source of Variation df F p df F p df F p df F p Between subjects Site 1 2.3 0.16 1 15.5 ≤0.05 1 0.9 0.36 1 1.6 0.23 Treatment 1 9.7 ≤0.05 1 8.3 ≤0.05 1 0.0 0.95 1 0.5 0.51 Site × treatment 1 0.3 0.60 1 0.0 0.95 1 0.3 0.60 1 0.4 0.53 Error 11 11 10 10 Within subjects Time 14 17.8 ≤0.05 14 10.6 ≤0.05 6 6.5 ≤0.05 6 2.7 ≤0.05 Time × site 14 1.5 0.10 14 1.5 0.11 6 2.7 ≤0.05 6 1.8 0.12 Time × treatment 14 4.3 ≤0.05 14 2.8 ≤0.05 6 0.8 0.57 6 0.8 0.57 Time × site × treatment 14 0.6 0.84 14 0.8 0.64 6 1.2 0.33 6 1.1 0.36 Author's Error 154 154 60 60 Source of Variation df F p df F p df F p df F p Between subjects Site 1 10.7 ≤0.05 1 4.0 0.07 1 4.0 0.07 1 9.9 ≤0.05 personal Treatment 1 3.9 0.07 1 0.3 0.62 1 3.2 0.10 1 8.1 ≤0.05 Site × treatment 1 0.1 0.73 1 0.2 0.68 1 0.3 0.60 1 0.7 0.41 Error 11 11 12 12 Within subjects Time 6 7.1 ≤0.05 6 28.8 ≤0.05 2 113.1 ≤0.05 2 58.2 ≤0.05 copy Time × site 6 1.6 0.16 6 2.0 0.08 2 5.6 ≤0.05 2 1.5 0.25 Time × treatment 6 0.7 0.64 6 1.2 0.32 2 1.3 0.28 2 2.7 0.09 Time × site × treatment 6 1.2 0.34 6 1.7 0.12 2 1.5 0.23 2 1.6 0.22 Carbon to Nitrogen ratio in rhizome biomass Carbon to Nitrogen ratio in root biomass Carbon to Phosphorus ratio in live leaf biomass Carbon to Phosphorus ratio in dead leaf biomass Source of Variation df F p df F p df F p df F p Between subjects Site 1 2.1 0.18 1 37.4 ≤0.05 1 13.8 ≤0.05 1 15.5 ≤0.05 Treatment 1 0.0 0.85 1 0.8 0.40 1 1.9 0.19 1 2.0 0.18 Site × treatment 1 1.5 0.24 1 8.2 ≤0.05 1 0.0 0.91 1 0.1 0.82 Error 10 11 12 12 Within subjects Time 2 13.5 ≤0.05 2 33.3 ≤0.05 2 14.4 ≤0.05 2 3.1 0.07 Time × site 2 1.7 0.21 2 9.7 ≤0.05 2 2.2 0.13 2 0.0 0.98 Time × treatment 2 0.9 0.43 2 1.2 0.32 2 0.5 0.64 2 0.1 0.93 Time × site × treatment 2 0.3 0.74 2 0.1 0.90 2 0.7 0.52 2 0.2 0.84 Author's personal copy Wetlands significant differences in the variables examined among blocks and, thus, this factor was not considered in the 0.05 0.05 ≤ p ≤ analyses. Normality was evaluated using normal probability plots and the Shapiro-Wilk statistic (Zar 1999). Homo- geneity of variance was determined using the Levene’s test. Data were log-transformed for a few variables to df F meet the above requirements. In addition, Mauchly’s criterion was used to determine whether the sphericity requirement of repeated-measures analysis was met (Crowder and Hand 1990). All but a few variables met 0.05 1 2.1 0.17 0.05 5 13.6 0.05 5 2.7 this requirement, and for those few variables not meeting ≤ ≤ p ≤ the requirement departures from sphericity were not se- vere. Therefore, we used univariate techniques to carry out the repeated-measures analyses (Moser et al. 1990). All statistical analyses were done with SYSTAT 11 and Sigma Plot 8.0. Results were considered significant at P≤0.05. df F Results Sediment Porewater Concentrations p Point-input subsurface fertilization did not increase N and P concentrations in the sediment porewater (Fig. 2). However, N and P concentrations became higher in fertilized than in un- phorus ratio in root biomass Leaf productivity Herbivory .7 0.43 1 1.1 0.32fertilized plots 1 in 1.6 the two 0.24 sites soon after starting to hand- broadcast the fertilizer. Such differences persisted throughout the end of the experiment (P≤0.05 for the interaction between nutrients and time, Table 2). df F Biomass Aboveground living biomass peaked in spring in State Park and in summer in Kee’s Bayou (Fig. 3a, P≤0.05 for the p interaction between time and site, Table 2). Peaks were not as clear for aboveground dead biomass, which nevertheless tended to be larger in 2004 than in 2003 (Fig. 3b, P≤0.05 for time main effect, P>0.05 for the interaction between time and site). Fertilization did not affect aboveground living or dead biomass at either site (P>0.05 for nutrients main effect and all interactions with nutrients). Total (i.e. living and dead) rhizome biomass showed large Carbon to Phosphorus ratio in rhizome biomass Carbon to Phos differences over time (Fig. 4a), peaking in winter/spring at the two sites (P≤0.05 for time main effect, P>0.05 for the inter- action between time and site, Table 2). Fertilization did not have any significant impact on rhizome biomass at any of the two sites (P>0.05 for nutrients main effect and all interactions (continued) with nutrients). These results were tantamount to those found for total root biomass (Fig. 4b),whichalsopeakedinwinter/ Error 20 22 24 24 Site 1 4.7 0.06 1 0.6 0.47 1 11.5 TreatmentSite × treatmentErrorTime 1 1 10 0.7 1.8 2 0.42 0.21 1.8 1 1 0.19 0 0.9 2 10 0.38 0.3 1 0.73 2.2 5 12 0.16 28.4 1 0.1 0.80 12 Time × site 2 0.3 0.75 2 0.3 0.74 5 7.8 Time × treatmentTime × site × treatmentError 2 2 1.1 0.3 20 0.36 0.73 2 2 0.4 0.6 0.68 20 0.57 5 5 2.0 0.9 0.10 0.49 60 5 5 1.7 1.0 0.15 0.42 60 Between subjects Within subjects Source of Variation df F P≤ P Table 2 spring at the two sites ( 0.05 for time main effect, >0.05 Author's personal copy Wetlands for the interaction between time and site) and was not affected Carbon:Nitrogen ratios in rhizomes decreased from Febru- by fertilization in either site (P>0.05 for nutrients main effect ary to April to July 2004, and that temporal decrease was and all interactions with nutrients). similar in the two sites (Fig. 5c, P≤0.05 for time main effect, P>0.05 for the interaction between time and site, Table 2). P Carbon:Nitrogen Ratios Fertilization did not affect these ratios ( >0.05 for nutrients main effect and all interactions with nutrients). Carbon:Nitrogen ratios in aboveground living biomass Carbon:Nitrogen ratios in roots also decreased from February showed higher values in April 2004 than in January and July toApriltoJuly2004(Fig.5d), although that temporal decline ’ P≤ 2004, and those temporal differences were more pronounced was more steady in State Park than in Kee sBayou( 0.05 in State Park than in Kee’s Bayou (Fig. 5a, P≤0.05 for the for the interaction between time and site). Fertilization de- ’ P≤ interaction between time and site, Table 2). Fertilization did creased these ratios in Kee s Bayou but not in State Park ( not affect these ratios (P>0.05 for nutrients main effect and all 0.05 for the interaction between nutrients and site). interactions with nutrients). Carbon:Nitrogen ratios in above- ground dead biomass were higher in April 2004 than in Carbon:Phosphorus Ratios January and July 2004 (Fig. 5b), and the overall extent of those temporal differences was similar in State Park and Kee’s Carbon:Phosphorus ratios in aboveground live biomass were Bayou (P≤0.05 for time main effect, P>0.05 for the interac- higher in April 2004 than in January and July 2004 (Fig. 6a, tion between time and site). Fertilization decreased these ratios Table 2), and the overall extent of those temporal differences at the two sites (P≤0.05 for nutrients main effect; P>0.05 for was similar in State Park and Kee’s Bayou (P≤0.05 for time all interactions with nutrients). main effect, P>0.05 for the interaction between time and site). Fig. 3 a Aboveground live biomass and (b) aboveground dead biomass. Bins represent mean values for 4 replicate plots in State Park (SP) or Kee’sBayou (KB) under non-fertilized (C) or fertilized (F) conditions. Bars represent SE Author's personal copy Wetlands Fig. 4 a Rhizome biomass and (b) root biomass in non-fertilized (C, open circles) and fertilized (F, closed circles) plots. Values are means for 4 plot replicates and bars are SE We did not find any significant temporal differences in 202.1 to 953.3 among control plots and from 563.2 to Carbon:Phosphorus ratios in aboveground dead biomass 3857.1 g DW m−2 yr−1 among fertilized plots in Kee’sBayou. among the three dates sampled (Fig. 6b; P>0.05 for time main Root productivity ranged from 1082.6 to 4724.6 among con- effect and all interactions with time). Fertilization did not trol plots and from 91.4 to 4287.5 g DW m−2 yr−1 among affect the Carbon:Phosphorus ratios in aboveground live or fertilized plots in State Park, and from 1330.4 to 3746.1 dead biomass (P>0.05 for nutrients main effect and all inter- among control plots and from 1084.3 to 6606.7 g DW actions with nutrients). m−2 yr−1 among fertilized plots in Kee’s Bayou. There were We did not find any temporal differences in no significant differences in rhizome or root productivity Carbon:Phosphorus ratios in rhizomes or roots among the between sites or treatments (Table 3;ANOVA:P>0.05 for three dates sampled (Fig. 6c and d, Table 2; P>0.05 for time site, treatment and their interaction for both rhizomes and main effect and all interactions with time). Fertilization did not roots). affect these ratios (P>0.05 for nutrients main effect and all interactions with nutrients). Leaf Herbivory Productivity Leaf herbivory decreased as the summer progressed in 2003, and in 2004 this continued to be the case in Kee’s Bayou but Leaf productivity varied over time (Fig. 7a) and peaked in late not in State Park where values remained low over that summer winter-spring in State Park and in mid-late spring in Kee’s (Fig. 7b; P≤0.05 for the interaction between time and site, Bayou (P≤0.05 for the interaction between time and site, Table 2). Fertilization did not affect leaf herbivory (P>0.05 Table 2). Fertilization did not affect leaf productivity for nutrients main effect and all interactions with nutrients). (P>0.05 for nutrients main effect and all interactions with nutrients). Decomposition Values of rhizome and root annual productivity varied widely among plots. Rhizome productivity ranged from 8.0 Decomposition rates varied among runs (Fig. 8). The runs to 3174.7 among control plots and from 501.0 to 1837.8 g started in February and April 2003 displayed higher rates than DW m−2 yr−1 among fertilized plots in State Park, and from those started in August and November 2003, probably Author's personal copy Wetlands because the former runs encompassed the entire summer it decomposes slowly. Our measured decomposition rates are season of 2003 when decomposition should proceed more similar (i.e. providing close estimates of quantity of leaf quickly due to high temperatures. Fertilization did not increase detritus decomposed over a given time interval) to rates mea- decomposition rates in any of the runs (P>0.05 for treatment sured for black needlerush in other studies (de la Cruz and and for the interaction between treatment and site for all four Gabriel 1974; Stout and de la Cruz 1981; Christian et al. 1990) ANOVAS). Decomposition rates were higher in Kee’s Bayou and, in concert all these reports indicate that black needlerush than in State Park for the April and August runs (P≤0.05 for decomposes slowly in comparison with other marsh plants site), but not for the February and November runs (P>0.05for (Enriquez et al. 1993; Cebrian 2002). site). We calculated the amount of black needlerush productivity that decomposed over the year, as well as the excess left over for accumulation or export (Fig. 9). To do that, we first calculated leaf detrital production from January 2003 through Discussion January 2004 ((Leaf detrital production)Jan03–Jan04)as: ðÞ Our results describe simultaneously a number of trophic Leaf detrital production Jan03− Jan04 routes of black needlerush productivity (i.e. herbivory, decom- ¼ ðÞLeaf productivity −ðÞHerbivory position, biomass storage) in two marshes. We found low Jan03− Jan04 Jan03− Jan04 −ðÞLeaf biomass accumulation herbivory by grasshoppers in both years of the study. The Jan03− Jan04 ð2Þ decrease observed in herbivory in late summer is probably due to the breakage of heavily grazed leaf tips (Sparks and Cebrian 2014), but the values remained low overall. Parsons and de la Cruz (1980) also found that grasshoppers removed only a where (Leaf productivity)Jan03–Jan04 was calculated by sum- small fraction (<5 %) of leaf production in their study site. ming all sampling intervals within January 2003–January Most leaf production in our study sites enters the detrital 2004; (Herbivory)Jan03–Jan04 corresponded to the value regis- compartment where, according to our litter-bag experiments, tered in June 2003, since the lower values measured in late Fig. 5 Carbon to Nitrogen ratios in live leaf (A), dead leaf (B), rhizome fertilized (F) conditions. Bars represent SE. Note the analyses for rhi- (C), and root (D) biomass. Bins represent mean values for 4 replicate plots zomes and roots were not done on samples taken for biomass measure- in State Park (SP) or Kee’s Bayou (KB) under non-fertilized (C) or ments (January 2004), but on samples taken in February 2004 Author's personal copy Wetlands Fig. 6 Carbon to Phosphorus ratios in live leaf (a), dead leaf (b), rhizome fertilized (F) conditions. Bars represent SE. Note the analyses for rhi- (c), and root (d)biomass.Bins represent mean values for 4 replicate plots zomes and roots were not done on samples taken for biomass measure- in State Park (SP) or Kee’s Bayou (KB) under non-fertilized (C) or ments (January 2004), but on samples taken in February 2004 summer likely reflected leaf senescence and ensuing break- have found slow belowground decomposition rates age; and (Leaf biomass accumulation) Jan03–Jan04 was calcu- (Hackney and de la Cruz 1980) and large pools of below- lated as the difference between leaf biomass in January 2004 ground mass (Gabriel and de la Cruz 1974; Hackney et al. and leaf biomass in January 2003 (leaf biomass accumulation 1978) in black needlerush marshes. was negative for Kee’sBayou,i.e.therewaslessstanding Our results also contribute other information that has been biomass in January 2004 than in January 2003, and thus that scarcely reported for the black needlerush, such as below- decrease in standing biomass was computed as a gain for leaf ground biomass and productivity and C:N and C:P ratios of detrital production, see Fig. 9). We then calculated the percent leaves, roots and rhizomes, thereby furthering our knowledge of leaf detrital production decomposed as (1−e−k×365)×100, and understanding of this common species. In particular, the wherekisthedecompositionrate(day−1)(Olson1963; higher leaf carbon:nutrient ratios found in April, and lower in Cebrian and Lartigue 2004). Finally leaf detritus available January and July, suggest possible nutrient dilution (i.e. tem- for accumulation or export was calculated as the difference porary reduction in internal nutrient concentration expressed between leaf detrital production and decomposition. Our mea- as %DW) in the spring coincident with fast leaf growth rates surements suggest that 36.6 % and 48.2 % of leaf detrital (Chapman and Craigie 1977; Bauer et al. 1997). production decomposes annually in State Park and Kee’s We did not find any clear effects of our low dosage, Bayou respectively. Hence, a substantial fraction of leaf detri- short-term (18 months) fertilizer application on the mag- tus can potentially be exported out of the system through nitude and trophic routing of black needlerush produc- waves and currents or be accumulated as refractory detritus tivity in the two marshes studied. We only found that within the system. hand broadcasting the fertilizer during the last 6 months We did not measure decomposition rates of rhizome and of the experiment increased sediment porewater nutrient root detritus. However the large pools of rhizome and root concentrations and, in a few cases, this method led to mass (including alive and dead organs) observed in our study higher internal nutrient contents in the plants. Specifi- sites suggest this detritus also decomposes slowly and, thus, a cally fertilization only increased nitrogen content in large fraction of belowground production is stored in the dead leaves in both sites and in roots in Kee’s Bayou system as recalcitrant organic matter. Indeed other studies out of eight possible instances (i.e. nitrogen and Author's personal copy Wetlands Fig. 7 a Leaf productivity and (b) herbivory. Bins represent mean values for 4 replicate plots in State Park (SP) or Kee’sBayou (KB) under non-fertilized (C) or fertilized (F) conditions. Bars represent SE phosphorus contents in live leaves, dead leaves, rhizome Darby and Turner 2008a). With the exception of one and roots). sampling time for DIN, our ambient concentrations were Ambient nutrient concentrations were probably not satu- comprised within those ranges (or even lower particu- rating for black needlerush in our study sites. To support this, larly for phosphate in State Park). we compiled values of ambient porewater nutrient concentra- Cross contamination between fertilized and control plots tions in studies where fertilization did have a positive effect on seems unlikely during the first year of the study when nutrients plant growth. Values for DIN concentrations ranged were applied through subsurface point inputs (wells) because from5to185μM, and values for phosphate from 1 with, the exception of the sampling date on October 2003, to 80 μM (Mendelssohn 1979; Mendelssohn and Kuhn porewater nutrient concentrations remained similar and low 2003; Morris and Bradley 1999; Emery et al. 2001; (i.e. within the low range of the ambient values compiled) in non-fertilized and fertilized plots. Nutrient cross-contamination Table 3 Rhizome and root productivity (g DW m-2 y-1). Values mayhaveoccurredtosomeextentinthelast6monthsofthe represent mean±SE for the four plot replicates study when the fertilizer was hand-broadcasted throughout the plots, as concentrations in controls plots seem a little higher Site Treatment Rhizome productivity Root productivity during that period in comparison to the previous year. However, Control 1478.4±663.7 2380.4±817.1 those concentrations were still seemingly non-saturating and, State Park most importantly, porewater nutrient concentrations were Fertilized 1284.8±322.5 1995.7±890 much higher in fertilized than control plots during the Control 540±154.9 2347.4±603.1 6 months of hand broadcasting. This suggests any po- Kee’sBayou tential nutrient cross-contamination that could have oc- Fertilized 1676.9±759.8 2872.7±1278 curred over the last 6 months of the study was not large and should not have masked strong fertilization effects. Author's personal copy Wetlands Leaf biomass State Park storage 0.7 Herbivory Leaf productivity Decomposition 2305 Accumulation or Export Kee’s Bayou 0.6 Herbivory Decomposition Leaf productivity 2150 Accumulation or Export Fig. 9 Trophic fate of black needlerush leaf productivity in the two marshes studied. All terms are expressed in g DW per m2 per year. Mean values for the eight plots were used, and non-fertilized and fertil- ized plots were pooled because we found no significant effects of fertil- ization on these variables. Values of k (see text) corresponded to the mean value of the eight plots for the February 2003 run, and non-fertilized and fertilized plots were pooled because we found no significant effect of fertilization on k be washed away from the marsh with ebbing tides (Whiting et al. 1987; Howes and Goehringer 1994; Osgood 2000), despite the fact that we hand broadcast nutrients at low tide. Overall these results suggest that black needlerush marshes Fig. 8 Decomposition rates for the runs started in February, April, are resistant to low intensity, short-term nutrient inputs, which August and November 2003 in State Park (SP) and Kee’s Bayou (KB). is in sharp contrast with the negative results reported for Bins represent mean values, and bars SE, for four non-fertilized (open prolonged, intense fertilization for other marshes (Hartig bins closed bins ) or fertilized ( ) plots et al. 2002; Turner 2011;Deeganetal.2012). Low intensity, short-term nutrient inputs may occur through faulty septic Therefore, the main reason for the weak fertilization effects systems, fertilizer leaching, and nutrient spills/runoff (Lehrter found in this study is probably the low dosage and short and Cebrian 2010; Sparks et al. 2014), and this study suggests duration of nutrient addition. In addition, uptake by sediment such nutrient inputs may not have a large bearing on black microflora and loss through advective losses (e.g. tidal forc- needlerush marshes. ing) could have also contributed to the lack of clear fertiliza- Nevertheless, it is possible that higher, longer fertilizer tion effects. Sediment microalgae and bacteria can quickly application could have larger and diverse effects on the mag- take a large fraction of incoming nutrients before plants do nitude and trophic fate of black needlerush productivity. The (Van Raalte et al. 1976; Tobias et al. 2001a;Lovell2005). comparison of some of the measured variables between the Furthermore, a significant fraction of the added nutrients may two sites suggests this could be the case. Sediment porewater Author's personal copy Wetlands phosphorus concentrations were higher in Kee’s Bayou than (e.g. wells), although experiments are needed to support this in State Park. Interestingly, the C:N ratio of live leaves was expectation. Previous research indicates that most nutrients lower in Kee’s Bayou than in State Park in one of the sampling that enter marshes through point sources can be taken up by dates in 2004, and the C:N ratio of dead leaves and the C:P surrounding plants within a few centimeters from the point ratios of live and dead leaves were lower in Kee’s Bayou than source, thereby leaving little nutrients for plants beyond that in State Park in all three sampling dates in 2004, which may be immediate vicinity (Tobias et al. 2001b; Fisher and Acreman partly due to the higher porewater phosphorus concentrations 2004 and references therein). in Kee’s Bayou (i.e. nutrient co-limitation, Harpole et al. 2011). In addition, herbivory was higher in Kee’s Bayou than in State Park in 2004, and leaf decomposition rates were Conclusion higher in Kee’s Bayou than in State Park for two (i.e. April and July) of the four runs done. In agreement with this, Sparks We describe for the first time several trophic routes of black and Cebrian (2014) fertilized black needlerush marsh plots for needlerush productivity simultaneously. This is a common 1yearat121gNm−2 yr−1 /7.5gPm−2 yr−1 and at species in marshes of the northern Gulf of Mexico, and the 242 g N m−2 yr−1 /15gPm−2 yr−1, and found increased results improve our understanding of the ecological roles of nitrogen contents and higher herbivory on the leaves of fertil- the species. Black needlerush in the studied marshes shows ized than non-fertilized plots. low rates of leaf herbivory and decomposition, and therefore Research with other marsh plants has shown that nutrient most leaf production is left over for storage in the marsh as addition dosages higher than the levels applied here can have refractory material or export to other coastal systems. Black large and diverse effects. For instance, McFarlin et al. (2008) needlerush also features large pools of belowground biomass, fertilized stands of S. alterniflora and J. roemerianus for 1 year which suggests an important role as reservoirs of organic (140 g N m−2 yr−1) and found higher nutrient contents in live matter. Our results also show that the productivity and trophic leaves of both plant species in fertilized than in non-fertilized fate of black needlerush seems resistant to low-intensity, plots. Higher herbivore abundances were found under fertil- short-term nutrient inputs. One year and a half of low nitrogen ized conditions, but those differences were attributed to par- and phosphorus dosage had no significant effects on the allel changes in plant structure (i.e. higher plant biomass, plant’s productivity and trophic routes measured in compari- cover and height) and not to increased herbivore feeding and son with non-fertilized conditions. Longer, more intense nu- growth rates on fertilized plants. However, fertilization did not trient inputs may have larger and diverse effects on the mag- significantly increase the nutrient content of dead leaves in nitude and trophic fate of black needlerush productivity, and relation to non-fertilized conditions, possibly due to nutrient determining the nutrient dosage thresholds at which these relocation to live leaves, leaching or not sufficiently long effects occur deserves more research. nutrient enrichment (1 year). Similarly, the consumption rates, growth rates and abundance levels of detritivore and decom- poser organisms did not differ between fertilized and non- Acknowledgments This paper is dedicated to the late Stanford (Chip) Bowman and her wife Melba. Their love for Kee’s Bayou and steward- fertilized conditions. Murphy et al. (2012) added nutrients for ship for a healthy environment is inspiring. We thank Laura Linn for help −2 −1 −2 −1 4 years at rates of 61.2 g N m yr and 81 g P m yr to with nutrient analysis, and Ron Kiene for use of his spectrophotometer. stands of S. alterniflora.Theyreportedhigherleafnutrient Laura Gough and Julie Olson provided valuable insights. The paper has contents, higher abundances and plant consumption rates for a also greatly benefited from several anonymous reviewers. This research was funded by the Alabama Center for Estuarine Studies (ACES) grant # number of herbivorous arthropods, and higher abundances of 5–21854. A. Hunter received support from a University of Alabama the detritivorous arthropods Venezillo sp. in fertilized than Alumni Association Fellowship in Aquatic Biology and a Mississippi- non-fertilized plots. Alabama Sea Grant student fellowship. The results further indicate that hand broadcasting appears to be a more effective method to spread fertilizer throughout the marsh than adding the fertilizer through a series of discrete References wells (i.e. subsurface point inputs). When we broadcast the fertilizer we found increased porewater nutrient concentra- tions and higher internal nitrogen contents for some plant Bauer G, Schulze ED, Mund M (1997) Nutrient contents and concentra- tions in relation to growth of Picea abies and Fagus sylvatica along a parts. None of this was found during the previous year of European transect. Tree Physiology 17:777–786 subsurface point nutrient delivery. This suggests that, even Boyer KE, Zedler JB (1999) Nitrogen addition could shift plant commu- when delivered at low dosage, widespread surface fertilizer nity composition in a restored California salt marsh. Restoration – application may have larger and faster effects on plant pro- Ecology 7:74 85 Brewer SJ (2003) Nitrogen addition does not reduce belowground com- ductivity and its trophic fate than when the same quantity of petition in a salt marsh clonal plant community in Mississippi fertilized is added through discrete subsurface point sources (USA). Plant Ecology 168:93–106 Author's personal copy Wetlands Bridgham SD, Megonigal JP, Keller JK, Bliss NB, Trettin C (2006) The Gallagher JL (1975) Effect of an ammonium nitrate pulse on the carbon balance of North American wetlands. Wetlands 26:889–916 growth and elemental composition of natural stands of Cebrian J (2002) Variability and control of carbon consumption, export, Spartina alterniflora and Juncus roemerianus.American and accumulation in marine communities. Limnology and Journal of Botany 62:644–648 Oceanography 47:11–22 Gough L, Grace JB (1997) The influence of vines on an oligohaline Cebrian J, Lartigue J (2004) Patterns of herbivory and decomposition in marsh community: results of a removal and fertilization study. aquatic and terrestrial ecosystems. Ecological Monographs 74:237–259 Oecologia 112:403–411 Cebrian J, Marba N, Duarte CM (1994) Estimating leaf age of the Gough L, Grace JB (1998) Herbivore effects on plant species density at seagrass Posidonia oceanica (L.) Delile using the plastochrone in- varying productivity levels. Ecology 79:1586–1594 terval index. Aquatic Botany 49:59–65 Gruner DS, Smith JE, Seabloom E, Sandlin S, Ngai JT, Hillebrand H, Cebrian J, Shurin JB, Borer ET, Cardinale BJ, Ngai JT, Smith MD, Fagan Harpole WS, Elser JJ, Cleland EE, Bracken ME, Borer ET, Bolker B WF (2009a) Producer nutritional quality controls ecosystem trophic (2008) A cross-system synthesis of consumer and nutrient resource structure. PloS One 4(3):e4929. doi:10.1371/journal.pone.0004929 control on producer biomass. Ecology Letters 11:740–755 Cebrian J, Corcoran AA, Stutes AL, Stutes JP, Pennock JR (2009b) Hackney CT, de la Cruz AA (1980) In situ decomposition of roots and Effects of ultraviolet-B radiation and nutrient enrichment on the rhizomes of two tidal marsh plants. Ecology 61:226–231 productivity of benthic microalgae in shallow coastal lagoons of Hackney CT, Stout JP, de la Cruz AA (1978) Standing crop and produc- the North Central Gulf of Mexico. Journal of Experimental Marine tivity of dominant marsh communities in the Alabama-Mississippi Biology and Ecology 372:9–21 Gulf Coast, p. I-1-29. In Evaluation of the Ecological Role and Chapman ARO, Craigie JS (1977) Seasonal growth in Laminaria Techniques for the Management of Tidal Marshes on the longicruris: relations with dissolved inorganic nutrients and internal Mississippi and Alabama Gulf Coast. Mississippi-Alabama Sea reserves of nitrogen. Marine Biology 40:197–205 Grant Publication. No. MASGP-78-044 Chmura GL, Anisfeld SC, Cahoon DR, Lynch JC (2003) Global carbon Harpole WS, Ngai JT, Cleland EE, Seabloom EW, Borer ET, Bracken sequestration in tidal, saline wetland soils. Global Biogeochemical MES, Elser JJ, Gruner DS, Hillebrand H, Shurin JB, Smith JE Cycles 17:1111. doi:10.1029/2002GB001917 (2011) Nutrient co-limitation of primary producer communities. Christian RR, Bryant WL Jr, Brinson MM (1990) Juncus roemerianus Ecology Letters 14:852–862 production and decomposition along gradients of salinity and hy- Hartig EK, Gornitz V, Kolker A, Mushacke F, Fallon D (2002) droperiod. Marine Ecology Progress Series 68:137–145 Anthropogenic and climate-change impacts on salt marshes of Crowder MJ, Hand DJ (1990) Analysis of repeated measures. Chapman Jamaica Bay, New York City. Wetlands 22:71–89 and Hall, London Hopkinson CS, Gosselink JG, Parrondo RT (1980) Production of coastal Darby FA, Turner RE (2008a) Effects of eutrophication on salt marsh root Louisiana marsh plants calculated from phenometric techniques. and rhizome biomass accumulation. Marine Ecology Progress Ecology 61:1091–1098 Series 363:63–70 Howes BL, Goehringer DD (1994) Porewater drainage and dissolved Darby FA, Turner RE (2008b) Below- and aboveground biomass of organic carbon and nutrient losses through the intertidal creekbanks Spartina alterniflora: response to nutrient addition in a Lousiana salt of a New England salt marsh. Marine Ecology Progress Series 114: marsh. Estuaries and Coasts 31:326–334 289–301 de la Cruz AA, Gabriel BC (1974) Caloric, elemental, and nutritive Huang XQ, Morris JT (2005) Distribution of phosphatase activity in changes in decomposing Juncus roemerianus leaves. Ecology 55: marsh sediments along an estuarine salinity gradient. Marine 882–886 Ecology Progress Series 292:75–83 de la Cruz AA, Hackney CT (1977) Energy value, elemental composition Hunter AE (2005) The Effects of Nutrient Enrichment on Coastal and productivity of belowground biomass of a Juncus tidal marsh. Wetlands of the northern Gulf of Mexico. Doctoral Dissertation. Ecology 58:1165–1170 The University of Alabama, Tuscaloosa, Alabama Deegan LA, Johnson DS, Warren RS, Peterson BJ, Fleeger JW, Jefferies RL, Perkins N (1977) The effects on the vegetation of the Fagherazzi S, Wollheim WM (2012) Coastal eutrophication as a additions of inorganic nutrients to salt marsh soils at Stiffkey, driver of salt marsh loss. Nature 490:388–392 Norfolk. Journal of Ecology 65:867–882 Duarte CM, Dennison WC, Orth RJW, Carruthers TJB (2008) The Langley JA, Megonigal JP (2010) Ecosystem response to elevated CO2 charisma of coastal ecosystems: addressing the imbalance. levels limited by nitrogen-induced plant species shift. Nature 466:96–99 Estuaries and Coasts 31:233–238 Lehrter JC, Cebrian JC (2010) Uncertainty propagation in an ecosystem Eleuterius LN (1976) The distribution of Juncus roemerianus in the salt nutrient budget. Ecological Applications 20:508–524 marshes of North America. Chesapeake Science 17:289–292 Levine JM, Brewer JS, Bertness MD (1998) Nutrients, competition and Emery NC, Ewanchuk PJ, Bertness MD (2001) Competition and salt- plant zonation in a New England salt marsh. Journal of Ecology 86: marsh plant zonation: stress tolerators may be dominant competi- 285–292 tors. Ecology 82:2471–2485 Lovell CR (2005) Belowground interactions among salt marsh plants and Enriquez S, Duarte CM, Sand-Jensen K (1993) Patterns in decomposition microorganisms. In: Kristensen E, Haese RR, Kostka JE (eds) rates among photosynthetic organisms: the importance of detritus C: Interactions between macro- and microorganisms in marine sedi- N:P content. Oecologia 94:457–471 ments (coastal and estuarine studies). American Geophysical Union, Fisher J, Acreman MC (2004) Wetland nutrient removal: a review of the Washington, D.C., pp 61–84 evidence. Hydrology and Earth System Sciences 8:673–685 Mateo MA, Cebrian J, Dunton K, Mutchler T (2006) Carbon flux in Foster BL, Gross KL (1998) Species richness in a successional grassland: seagrass ecosystems. In: Larkum AWD, Orth RJ, Duarte CM (eds) effects of nitrogen enrichment and plant litter. Ecology 79:2593– Seagrasses: biology. Ecology and Conservation. Springer, New 2602 York, pp 159–192 Fourqurean JW, Zieman JC, Powell GVN (1992) Phosphorus limitation McFarlin CR, Brewer JS, Buck TL, Pennings SC (2008) Impact of of primary production in Florida Bay: evidence from C:N:P ratios of fertilization on a salt marsh food web in Georgia. Estuaries and the dominant seagrass. Limnology and Oceanography 37:162–171 Coasts 31:313–325 Gabriel BC, de la Cruz AA (1974) Species composition, standing stock McLeod E, Chmura GL, Bouillon S, Salm R, Björk M, Duarte CM, and net primary production of a salt marsh community in Lovelock CE, Schlesinger WH, Silliman BR (2011) A blueprint for Mississippi. Chesapeake Science 15:72–77 blue carbon: toward an improved understanding of the role of Author's personal copy Wetlands vegetated coastal habitats in sequestering CO2. Frontiers in Ecology Sand-Jensen K, Jacobsen D, Duarte CM (1994) Herbivory and resulting and Environment 9:552–560 plant damage. Oikos 69:545–549 Mendelssohn IA (1979) Nitrogen metabolism in the height forms Smalley AE (1960) Energy flow of a salt marsh grasshopper population. of Spartina alterniflora in North Carolina. Ecology 60:574– Ecology 41:672–677 584 Solorzano L, Sharp JH (1980) Determination of total phosphorus and Mendelssohn IA, Kuhn NL (2003) Sediment subsidy: effects on soil- particulate phosphorus in natural water. Limnology and plant responses in a rapidly submerging coastal salt marsh. Oceanography 25:756–760 Ecological Engineering 21:115–128 Sparks EL, Cebrian J (2014) Effects of fertilization on grasshopper Minello TJ, Able KW, Weinstein MP, Hays CG (2003) Salt marshes as grazing of northern Gulf of Mexico salt marshes. Estuaries and nurseries for nekton: testing hypotheses on density, growth and Coasts. doi:10.1007/s12237-014-9858-6 survival through meta-analysis. Marine Ecology Progress Series Sparks EL, Cebrian J, Biber PD, Sheehan KL, Tobias CR (2013) Cost- 246:39–59 effectiveness of two small-scale salt marsh restoration designs. Moody RM, Cebrian J, Heck KL (2013a) Interannual recruitment dy- Ecological Engineering 53:250–256 namics for resident and transient marsh species: evidence for a lack Sparks EL, Cebrian J, Smith SM (2014) Removal of fast flowing nitrogen of impact by the Macondo oil spill. PloS One 8(3):e58376. doi:10. from marshes in sandy soils. PLoS ONE 9(10): e111456. doi:10. 1371/journal.pone.0058376 1371/journal.pone.0111456 Moody RM, Cebrian J, Kerner SM, Heck KL, Powers SP, Ferraro C Sterner RW, Elser JJ (2002) Ecological stoichiometry: the biology of elements (2013b) Effects of shoreline erosion on salt-marsh floral zonation. from molecules to the biosphere. Princeton University Press, Princeton Marine Ecology Progress Series 488:145–155 Stout JP, de la Cruz AA (1981) In situ decomposition of dead tissues of Morgan PA, Burdick DM, Short FT (2009) The functions and values of selected tidal marsh plants. Association of Southeastern Biologists fringing salt marshes in northern New England, USA. Estuaries and Bulletin 28:100 Coasts 32:483–495 Strickland JDH, Parsons TR (1972) A practical handbook of seawater Morris JT, Bradley PM (1999) Effects of nutrient loading on the carbon analysis, 2nd edn. Bulletin of the Fisheries Research Board of balance of coastal wetland sediments. Limnology and Canada 167:1–310 Oceanography 44:699–702 Stutes J, Cebrian J, Stutes AL, Hunter A, Corcoran AA (2007) Benthic Moser EB, Saxton AM, Pezeshki SR (1990) Repeated measures analysis metabolism across a gradient of anthropogenic impact in three of variance: application to tree research. Canadian Journal of Forest shallow coastal lagoons in NW Florida. Marine Ecology Progress Research 20:524–535 Series 348:55–70 Mudd SM, Howell S, Morris JT (2009) Impact of the dynamic feedback Tobias CR, Anderson IC, Canuel EA, Macko SA (2001a) Nitrogen between sedimentation, sea level rise, and biomass production on cycling through a fringing marsh-aquifer ecotone. Marine Ecology near surface marsh stratigraphy and carbon accumulation. Estuarine, Progress Series 201:25–39 Coastal and Shelf Science 82:377–389 Tobias CR, Macko SA, Anderson IC, Canuel EA, Harvey JW (2001b) Murphy SM, Wimp GM, Lewis D, Denno RF (2012) Nutrient presses Tracking the fate of a high concentration groundwater nitrate plume and pulses differentially impact plants, herbivores, detritivores and through a fringing marsh: a combined groundwater tracer and in situ their natural enemies. PloS One 7(8):e43929. doi:10.1371/journal. isotope enrichment study. Limnology and Oceanography 46:1977– pone.0043929 1989 Newell SY, Arsuffi TL, Palm LA (1996) Misting and nitrogen fertiliza- Turner RE (1990) Landscape development and coastal wetland losses in tion of shoots of a saltmarsh grass: effects upon fungal decay of leaf the northern Gulf of Mexico. Integrative and Comparative Biology blades. Oecologia 108:495–502 30:89–105 Olson JS (1963) Energy storage and the balance of producers and de- Turner RE (2011) Beneath the salt marsh canopy: loss of soil strength composers in ecological systems. Ecology 44:322–331 with increasing nutrient loads. Estuaries and Coasts 34:1084–1093 Osgood DT (2000) Subsurface hydrology and nutrient export from Valiela I, Teal JM, Sass WJ (1975) Production and dynamics of salt marsh barrier island marshes at different tidal ranges. Wetlands Ecology vegetation and the effects of experimental treatment with sewage and Management 8:133–146 sludge. Biomass, production and species composition. The Journal Parsons KA, de la Cruz AA (1980) Energy flow and grazing behavior of of Applied Ecology 12:973–981 conocephaline grasshoppers in a Juncus roemerianus marsh. Valiela I, Teal JM, Persson NY (1976) Production and dynamics of Ecology 61:1045–1050 experimentally enriched salt-marsh vegetation - Belowground bio- Pendleton L, Donato DC, Murray BC, Crooks S, Jenkins WA, Sifleet S, mass. Limnology and Oceanography 21:245–252 Craft C, Fourqurean JW, Kauffman JB, Marba N, Megonigal P, Van der Graaf AJ, Stahl J, Veen GF, Havinga RM, Drent RH Pidgeon E, Herr D, Gordon D, Barbera A (2012) Estimating global (2007) Patch choice of avian herbivores along a migration “blue carbon” emissions from conversion and degradation of vege- trajectory - From Temperate to Arctic. Basic and Applied tated coastal ecosystems. PloS One 7(9):e43542. doi:10.1371/ Ecology 8:354–363 journal.pone.0043542 Van Raalte CD, Valiela I, Teal JM (1976) Production of epibenthic salt Pennings SC, Stanton LE, Brewer JS (2002) Nutrient effects on the marsh algae: light and nutrient limitation. Limnology and composition of salt marsh plant communities along the Southern Oceanography 21(6):862–872 Atlantic and Gulf Coasts of the United States. Estuaries 25:1164–1173 Wason EL, Pennings SC (2008) Grasshopper (Orthoptera: Tettigoniidae) Pennock JR, Cowan JLW (2001) Analytical instrumentation methods composition and size across latitude in Atlantic coast salt marshes. manual. Marine environmental sciences consortium, Technical re- Estuaries and Coasts 31:335–343 port 98–003, 69 pp Whiting GJ, McKellar HN Jr, Kjerfve B, Spurrier JD (1987) Nitrogen Polis GA, Hurd SD (1996) Linking marine and terrestrial food webs: exchange between a southeastern USA salt marsh ecosystem and the Allochthonous input from the ocean supports high secondary pro- coastal ocean. Marine Biology 95:173–182 ductivity on small islands and coastal land communities. American Williams RB, Murdoch MB (1972) Compartmental analysis of the pro- Naturalist 147:396–423 duction of Juncus roemerianus in a North Carolina salt marsh. Rabalais NN, Turner RE, Justic D, Diaz RJ (2009) Global change and Chesapeake Science 13:69–79 eutrophication of coastal waters. ICES Journal of Marine Science Zar JH (1999) Biostatistical analysis, 4th edn. Prentice-Hall, Englewood 66:1528–1537 Cliffs Wetlands DOI 10.1007/s13157-015-0629-3 ERRATUM Erratum to: Magnitude and Trophic Fate of Black Needlerush (Juncus Roemerianus) Productivity: Does Nutrient Addition Matter? Amy Hunter & Just Cebrian & Jason P. Stutes & David Patterson & Bart Christiaen & Celine Lafabrie & Josh Goff # Society of Wetland Scientists 2015 Erratum to: Wetlands ing should be located following the “Within Subjects” DOI 10.1007/s13157-014-0611-5 “Error” row for the variables “Porewater N concentra- tion”, “Porewater P concentration”, “Aboveground live Table 2 in the paper Magnitude and Trophic Fate of biomass” and “Aboveground dead biomass”.The“With- Black Needlerush (Juncus Roemerianus) Productivity: in Subjects”“Error” row for the variables “Rhizome Bio- Does Nutrient Addition Matter? is missing the heading mass”, “Root Biomass”, “Carbon to Nitrogen ratio in for the variables “Rhizome Biomass”, “Root Biomass”, live leaf biomass” and “Carbon to Nitrogen ratio in dead “Carbon to Nitrogen ratio in live leaf biomass” and “Car- leaf biomass” is also missing. We now provide the cor- bon to Nitrogen ratio in dead leaf biomass”.Thishead- rect version of Table 2. The online version of the original article can be found at http://dx.doi.org/ 10.1007/s13157-014-0611-5. A. Hunter Department of Biological Sciences, University of Alabama, Tuscaloosa, AL 35487, USA A. Hunter : J. Cebrian (*) : J. P. Stutes : D. Patterson : B. Christiaen : J. Goff Dauphin Island Sea Lab, 101 Bienville Blvd., Dauphin Island, AL 36528, USA e-mail: [email protected] J. Cebrian : B. Christiaen Department of Marine Sciences, University of South Alabama, Mobile, AL 36688, USA C. Lafabrie ECOSYM, Ecology of Coastal Marine Systems, 2 Place Eugène Bataillon, 34095 Montpellier Cedex 5, France Wetlands Table 2 Results of repeated-measures ANOVA Porewater N concentration Porewater P concentration Aboveground live biomass Aboveground dead biomass Source of variation df F p df F p df F p df F p Between subjects Site 1 2.3 0.16 1 15.5 ≤0.05 1 0.9 0.36 1 1.6 0.23 Treatment 1 9.7 ≤0.05 1 8.3 ≤0.05 1 0.0 0.95 1 0.5 0.51 Site × treatment 1 0.3 0.60 1 0.0 0.95 1 0.3 0.60 1 0.4 0.53 Error 11 11 10 10 Within subjects Time 14 17.8 ≤0.05 14 10.6 ≤0.05 6 6.5 ≤0.05 6 2.7 ≤0.05 Time × site 14 1.5 0.10 14 1.5 0.11 6 2.7 ≤0.05 6 1.8 0.12 Time × treatment 14 4.3 ≤0.05 14 2.8 ≤0.05 6 0.8 0.57 6 0.8 0.57 Time × site × treatment 14 0.6 0.84 14 0.8 0.64 6 1.2 0.33 6 1.1 0.36 Error 154 154 60 60 Rhizome biomass Root biomass Carbon to Nitrogen ratio in Carbon to Nitrogen ratio in live leaf biomass dead leaf biomass Source of variation df F p df F p df F p df F p Between subjects Site 1 10.7 ≤0.05 1 4.0 0.07 1 4.0 0.07 1 9.9 ≤0.05 Treatment 1 3.9 0.07 1 0.3 0.62 1 3.2 0.10 1 8.1 ≤0.05 Site × treatment 1 0.1 0.73 1 0.2 0.68 1 0.3 0.60 1 0.7 0.41 Error 11 11 12 12 Within subjects Time 6 7.1 ≤0.05 6 28.8 ≤0.05 2 113.1 ≤0.05 2 58.2 ≤0.05 Time × site 6 1.6 0.16 6 2.0 0.08 2 5.6 ≤0.05 2 1.5 0.25 Time × treatment 6 0.7 0.64 6 1.2 0.32 2 1.3 0.28 2 2.7 0.09 Time × site × treatment 6 1.2 0.34 6 1.7 0.12 2 1.5 0.23 2 1.6 0.22 Error66662424 Carbon to Nitrogen ratio in Carbon to Nitrogen ratio in Carbon to Phosphorus ratio in Carbon to Phosphorus ratio rhizome biomass root biomass live leaf biomass in dead leaf biomass Source of variation df F p df F p df F p df F p Between subjects Site 1 2.1 0.18 1 37.4 ≤0.05 1 13.8 ≤0.05 1 15.5 ≤0.05 Treatment 1 0.0 0.85 1 0.8 0.40 1 1.9 0.19 1 2.0 0.18 Site × treatment 1 1.5 0.24 1 8.2 ≤0.05 1 0.0 0.91 1 0.1 0.82 Error10111212 Within subjects Time 2 13.5 ≤0.05 2 33.3 ≤0.05 2 14.4 ≤0.05 2 3.1 0.07 Time × site 2 1.7 0.21 2 9.7 ≤0.05 2 2.2 0.13 2 0.0 0.98 Time × treatment 2 0.9 0.43 2 1.2 0.32 2 0.5 0.64 2 0.1 0.93 Time × site × treatment 2 0.3 0.74 2 0.1 0.90 2 0.7 0.52 2 0.2 0.84 Error20222424 Carbon to Phosphorus ratio in Carbon to Phosphorus ratio Leaf productivity Herbivory rhizome biomass in root biomass Source of variation df F p df F p df F p df F p Between subjects Site 1 4.7 0.06 1 0.6 0.47 1 11.5 ≤0.05 1 2.1 0.17 Treatment 1 1.8 0.21 1 0.9 0.38 1 2.2 0.16 1 0.1 0.80 Site × treatment 1 0.7 0.42 1 0.7 0.43 1 1.1 0.32 1 1.6 0.24 Error10101212 Wetlands Table 2 (continued) Within subjects Time 2 1. 8 0.19 2 0.3 0.73 5 28.4 ≤0.05 5 13.6 ≤0.05 Time × site 2 0.3 0.75 2 0.3 0.74 5 7.8 ≤0.05 5 2.7 ≤0.05 Time × treatment 2 0.3 0.73 2 0.6 0.57 5 0.9 0.49 5 1.0 0.42 Time × site × treatment 2 1.1 0.36 2 0.4 0.68 5 2.0 0.10 5 1.7 0.15 Error20206060