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Article

What’s Going on Down There? Impacts of Long-Term Elevated CO2 and Community Composition on Components of Below-Ground Biomass in a Chesapeake Bay Saltmarsh

by
Rachel Collin
1,*,
Bert G. Drake
2 and
J. Patrick Megonigal
2,*
1
Smithsonian Tropical Research Institute, Ancon 0843-03092, Panama
2
Smithsonian Environmental Research Center, Edgewater, MD 21037, USA
*
Authors to whom correspondence should be addressed.
Hydrobiology 2025, 4(1), 8; https://doi.org/10.3390/hydrobiology4010008
Submission received: 30 November 2024 / Revised: 16 February 2025 / Accepted: 3 March 2025 / Published: 19 March 2025
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Abstract

:
Roots and rhizomes play diverse roles in the response of coastal wetland ecosystems to climate change through hydrobiogeomorphic and biogeochemical processes. The accumulation of living and dead belowground biomass contributes significantly to surface elevation gain, redox status through root oxygen loss and exudates, and plant transport of greenhouse gases to the atmosphere. Yet, responses of belowground biomass to global climate stressors are difficult to measure and remain poorly understood. Here, we report on the response of individual components of belowground biomass to 12 years of CO2 enrichment in a temperate tidal marsh. In both a community initially dominated by the C3 species Schoenoplectus americanus and another initially dominated by the C4 species Spartina patens, elevated CO2 increased total belowground biomass and subtly altered depth distributions of some components. In the Spartina community, this effect was the result of the direct effects of CO2 on plant biomass allocation, while any direct response in the Schoenoplectus community was difficult to detect because of changes in the relative abundance of C3 versus C4 species. In the Schoenoplectus community, belowground biomass was positively related to S. americanus stem density. Compared to the C4 community, the Schoenoplectus community had higher root and rhizome biomass and deeper rhizomes. These results highlight the importance of community composition and plant functional traits in understanding ecosystem- and community-scale responses to elevated CO2 and their potential impacts on marsh elevation.

1. Introduction

Coastal wetlands play an important role in global carbon and nitrogen cycles by sequestering carbon, emitting greenhouse gases, exporting dissolved organic and inorganic carbon to oceans, and protecting vulnerable aquatic ecosystems from land-derived eutrophication [1]. They are also important for the protection of coastal human infrastructure [2]. Yet, trapped between rising sea levels and anthropogenic land-use change, these ecosystems are vulnerable to being lost from the seascape by coastal squeeze [3]. Elucidating the responses of coastal wetlands to climate stressors and the mechanisms by which vegetation mediates these responses is of broad interest for managing and forecasting wetland responses to global change [4,5,6,7].
The plant species that dominate coastal wetlands are considered ecosystem engineers because they drive hydrogeomorphic feedbacks that help establish and stabilize the ecosystem. As such, coastal wetland responses to climate change are highly sensitive to wetland plant traits [8]. There is considerable research on responses to climate change factors for a wide variety of wetland plant functional types including grasses like Spartina, reeds like Phragmites, sedges like Schoenoplectus, rushes like Juncus, and mangroves like Rhizophora and Avicennia. However, most studies have focused on aboveground traits such as biomass, productivity, and phenology, with far less work on belowground responses. This is an important knowledge gap, as belowground biomass (e.g., roots and rhizomes) plays diverse roles in coastal wetland ecology and ultimately influences ecosystem-level phenomena. For example, belowground responses regulate the accumulation of living and dead belowground biomass that contribute significantly to marsh surface elevation change, soil carbon stocks, oxygen transport, soil redox status, and methane transport from the soil profile to the atmosphere [9,10,11,12,13,14,15,16,17].
Documenting drivers of variation in belowground biomass is important for understanding and modeling the biogeomorphic feedbacks that control surface accretion and elevation gain or loss relative to local sea level [18,19,20]. Organic matter derived primarily from belowground biomass contributes more volume per gram than sediment in wetland soils and can account for 79–92% of total vertical accretion in coastal marshes [20,21]. Experiments designed to determine how global change is impacting marsh elevation have shown in situ that elevated atmospheric CO2 can significantly increase aboveground productivity, fine root productivity, and soil carbon accumulation, resulting in elevation gain compared to ambient treatments in a Schoenoplectus-dominated tidal marsh [22]. A different in situ experiment in the same marsh showed that fine root growth is consistently stimulated by elevated CO2 in Schoenoplectus-dominated (C3) communities but not in Spartina-dominated (C4) communities, a difference explained by the sensitivity of the two photosynthetic pathways to CO2 concentration [23,24,25]. These responses can be modified by tidal flood duration and nitrogen availability [26,27]. These studies and others have documented the effects of elevated CO2 on belowground biomass productivity (a rate) using methods such as annual root ingrowth cores. However, they have not documented the long-term cumulative effects on belowground standing stock, a net quantity that integrates both production and mortality rates. In addition, few studies have evaluated the separate contribution of rhizomes, roots, or stem bases, nor changes in the depth distributions of these components. One exception is a mesocosm study that showed surface elevation gain in response to elevated CO2 in mixed-species tidal marsh communities was related to increased stem base volume mediated by changes in species composition [9].
Elevated CO2 can potentially alter soil carbon sequestration and elevation change via the chemical composition of the belowground biomass upon senescence (i.e., litter) [28]. We know very little about how elevated CO2 affects the chemistry of belowground structures, but it is likely that such differences influence decomposition rates [29,30,31,32,33]. To the extent that the chemical composition of belowground tissues varies across species, changes in species composition, a common global change response, can mediate changes in soil organic matter and nutrient cycling via belowground litter quality [32,34].
We investigated changes in the different components of belowground biomass over 13 years of in situ elevated CO2 exposure to gain insights into the mechanisms behind previously reported ecosystem-scale responses such as soil carbon sequestration, soil elevation gain, greenhouse gas fluxes, and redox conditions. We contrasted two tidal marsh plant communities, each of which was initially dominated by species with distinctly different traits: Schoenoplectus americanus (Pers.) Volkart ex Schinz & R. Keller (Chairmaker’s bulrush) and Spartina patens (Aiton) Muhl. (Saltmeadow cordgrass). Our objectives were to (1) document CO2 treatment effects on total belowground biomass and the depth distribution of belowground biomass functional components (roots, rhizomes, and culms) at the plant community level; (2) relate belowground biomass to differences in aboveground productivity (peak growing season biomass) and root productivity as assessed by ingrowth cores at the plant community level; and (3) determine how changes in plant community composition of the S. americanus-dominated community relate to differences in belowground biomass.

2. Methods

2.1. Experimental Treatments

This work was conducted at the Global Change Research Wetland, a facility operated by the Smithsonian Environmental Research Center located on the Chesapeake Bay in Maryland, USA (38.874214° N, −76.549571° W). The site supports several long-term global change experiments, the longest-running of which is a cross between elevated CO2 and plant community composition (a.k.a. the CO2 x Community experiment [25,28,35,36,37,38,39,40]). Since 1987, this experiment has manipulated three plant communities to one of three treatments: chambered with ambient CO2, chambered with elevated CO2, and unchambered control [41]. The three plant communities are designated by the genera that dominated them when the study began in 1987: Spartina, Schoenoplectus, or mixed (i.e., co-dominated by Spartina and Schoenoplectus). There are five replicates of each treatment per plant community, for a total of 45 plots. The ambient treatment open-top chambers are ventilated with ambient air, and the elevated treatment chambers receive ambient air with additional CO2 to raise the concentration by approximately 340 ppm CO2, roughly doubling the ambient concentration in 1999, and exceeding the current atmospheric concentration of ~420 ppm. Treatments are applied only during the growing season (May–Oct) after which the chambers are removed. The designations of the three plant communities can be misleading because they represent the initial conditions in 1987. The C4 grass-dominated community at that time was nearly completely dominated by Spartina patens (Aiton) Muhl and was still dominated by this species in 1999. The C3 sedge-dominated community was almost entirely Schoenoplectus americanus (Pers.) Volk. Ex Schinz & R. Keller (formerly known as Scirpus olneyi) in 1987, but from 1987 to 1999 (the date of this study) diversified to include significant biomass of the C4 grass Distichlis spicata (L.) Greene, and occasionally other species such as Atriplex patula L., Iva frutescens L., Kosteletskya virginica (L.) C. Presl ex. Gray, Lythrum lineare L., and Persicaria hydropiper (L.) Spach. We will continue to refer to the two communities by their designated names—Spartina community and Schoenoplectus community—but note that plant community composition at the time of the present study had changed, particularly in the C3 sedge community. When referring to a specific plant species (rather than a plant community), we use the species names S. patens and S. americanus.

2.2. Belowground Biomass and Litter

In August 1999, after 13 years of continuous growing season CO2 treatment, we collected soil cores from inside experimental chambers in the Spartina and Schoenoplectus communities; the mixed community and the unchambered controls were not sampled. Two soil cores, 5.1 cm in diameter and 100 cm in length, were extracted from each of the 20 chambers with a piston corer in three sections at intervals of 0–33 cm, 34–66 cm, and 67–100 cm. Each core was sectioned horizontally by depth. Sections from the top 15 cm were nominally 2.5 cm thick, and all belowground biomass was recovered from them. Between 15 and 100 cm, one 2.5-cm-thick sub-section was taken centered at 21.25 cm and 5-cm-thick sub-sections were taken at 32.5, 52.5, 72.5, and 92.5 cm depths. These soil sub-sections were used to estimate the components of belowground biomass and detritus. An additional frozen core was taken from 0 to 22 cm depth in each chamber for determination of carbon and nitrogen content and the δ13C of belowground biomass components (see below). This destructive sampling for belowground biomass was not repeated in subsequent years to limit soil disturbance on the world’s longest-running CO2 enrichment experiment.
For biomass estimation, samples were wet-sieved through a 1.0 mm sieve. Living belowground biomass was separated from necromass (i.e., dead roots and detritus; referred to here as litter) based on color, rigidity, and the condition of the epidermis using methods similar to Saunders et al. [28]. Consistency in sorting was aided by reference samples of each class of belowground biomass stored in refrigerated, water-filled bags. Live biomass was sorted into the morphological categories of roots, rhizomes, and culms. The smallest roots were subsampled by dispersing them in shallow DI water in a glass pan, randomly selecting 4 of 8 quadrants in the pan for biomass determination, then extrapolating to the full glass pan.
Living biomass was next categorized by color, which can be interpreted as coming from either grasses or sedges. Previous work in this system used tissue δ13C to establish that red roots, red rhizomes, and dark red roots in this system are from S. americanus; white rhizomes are from the grass S. patens; and that white roots are predominantly, but not exclusively, from S. patens [28]. The only exception is very young S. americanus roots, which can initially appear white before turning red. Distichlis spicata, another C4 grass species found in the marsh, was not present in the area sampled by Saunders et al. [28]. We confirmed the color-based classification by measuring the tissue δ13C of our morphological categories (Supplemental Table S2; Supplemental Figure S1). We estimated the proportion of white roots classified as S. patens (grass) that might have been young S. americanus (sedge) roots for our plots in 1999. A two-end-member mixing model was used to estimate the mass fraction of white sedge roots that were incorrectly categorized as white grass roots at 14–16%. End-members were different for the ambient and elevated CO2 treatments because the CO2 source used to raise CO2 concentrations inside the chambers is heavily depleted in 13C. The estimate used the white grass roots from the nearly monotypic Spartina community for the grass end-member (δ13C = −12.30 ambient, −20.62 elevated) and red roots from the Schoenoplectus community for the sedge end-member (δ13C = −25.66 ambient, −31.29 elevated). Using these values, we calculated the fraction of the white root category (nominally from Spartina) that were S. americanus roots in the Schoenoplectus community (δ13C = −14.16 ambient, −22.31 elevated). Given the relatively small mass fraction of misclassified roots, we assumed in our analysis that all white roots were from S. patens.
As reported in the dataset publication by Megonigal and Holmquist [42], roots were sorted into light-colored (LRT), red (RRT), or dark (DRT); rhizomes into red (RRH) or white (WRH); and culms into rhizomatous (RHC) or non-rhizomatous (NRHC) depending on the nature of the structure to which they were attached. Culms were treated as a single category in this analysis, and the light-colored root (LRT) category reported by Megonigal and Holmquist [42] is referred to here as white roots. After sorting, material was dried to a constant weight at 60 °C (for approximately two weeks) and weighed.

2.3. Organic Carbon, Nitrogen, and δ13C

Carbon isotope ratios were obtained by combusting 2–3 mg subsamples in an elemental analyzer (NA1500 Series 1, Carlo Erba Instrumentazione, Milan, Italy) and measuring δ13C on a SIRA Series II isotope ratio mass spectrometer. For nutrient analysis, freeze-dried samples were homogenized using a Wiley Mill, and the %C and %N of the samples were determined for each root and rhizome class using an elemental analyzer (NA1500 Series 1, Carlo Erba Instrumentazione). C:N ratios are expressed as mass ratios (i.e., %C of dry sample divided by %N of dry sample), and δ13C was calculated with respect to the Pee Dee Belemnite standard (the reference standard for δ13C analyses), expressed in parts per thousand (‰).

2.4. Aboveground Biomass, Shoot Density, and Root Growth

This subset of the data herein has been previously published in several studies and review papers [25,35,38,40,43,44] and is available at https://serc.si.edu/gcrew/CO2data (accessed on 30 March 2024). Briefly, all S. americanus stems in the entire 0.47-m2 plot area were counted, measured for height and width, and applied to a robust allometric equation [45] to calculate the aboveground biomass of each stem. Aboveground biomass of the plot was calculated as the product of plant density and mean individual plant biomass [37]. The biomass of all other species in the plots was determined by harvesting 5 replicate 25 cm2 subplots, sorting by species, and weighing their oven-dried mass. Belowground biomass productivity was assessed by placing 3 replicate ingrowth bags in each plot during autumn [23] and removing them the following autumn (i.e., a year later), recovering the biomass in each bag with a sieve, then oven drying and weighing. Thus, unlike the new belowground biomass data we report here, the belowground productivity data collected in 1999 did not distinguish between roots, rhizomes, or species.
In the 1-m-deep cores taken for belowground biomass, the biomass of the components in each core and the normalized cumulative mass were calculated using a previously published R script [42]. Statistical analyses were conducted independently on each community to compare differences between treatments in JMP 17. Linear mixed models were used to account for multiple measures (i.e., duplicate cores) within a single plot, using plot as a random effect nested within the community. For comparisons between aboveground and belowground variables, the replicate measures within a plot were averaged to generate a single value per plot, followed by analysis of variance (ANOVA) or covariance (ANCOVA), and linear regression in JMP 17. To compare normalized cumulative biomass with depth, we used JMP 17 to fit a logistic 2-parameter curve to the cumulative biomass by depth data and compared the growth rate (referred to subsequently as depth accumulation rate) and inflection point (referred to subsequently as peak depth) parameters across the four pairwise combinations of treatment and community. Due to the low number of plots (5 per treatment combination) and the resultant limits on the power to detect small effects, we consider p < 0.1 to be meaningful; however, we did not apply a strict p-value threshold to interpret the significance, following guidance from the statistics community [46,47,48].

3. Results

3.1. Community-Level Responses to Elevated CO2

After 13 years of exposure, elevated CO2 increased total belowground biomass by 26–29% in both communities (Table 1; Figure 1). Of the three functional components of belowground biomass examined in this study (roots, rhizomes, and culms), S. americanus culm and rhizome biomass were significantly higher, and S. patens root biomass was significantly higher in the elevated CO2 treatment compared to the ambient treatment. Averaging across CO2 treatments, the Schoenoplectus community had higher belowground biomass than the Spartina community (3907 vs. 2310 g/m2), and considerably more rhizome biomass (1699 vs. 622 g/m2) than the Spartina community. CO2 treatment had no effect on belowground litter biomass (Table 1).
We examined the depth distribution of belowground biomass visually and by comparing logistic two-parameter curve fits to their depth distribution (Figure 2 and Figure 3). The Schoenoplectus community had deeper rhizomes (the deepest occurring in the section centered on 15 cm) than the Spartina community. Compared to the Schoenoplectus community, rhizomes and roots in the Spartina community were significantly shallower, had faster depth accumulation rates, and more shallow peak depths (Supplemental Table S1; Figure 3). In the Schoenoplectus community, we found neither rhizomes nor culms below the 15 cm subsample in either treatment, while in the Spartina community few if any rhizomes were found below 10 cm. In both communities, live roots were found even in the deepest (92.5 cm) sections of the cores in both treatments, but their contribution to total root biomass was negligible.
The peak depth for rhizomes and culms differed between the CO2 treatments in the Schoenoplectus community; culms were significantly shallower and rhizomes significantly deeper in the elevated CO2 treatment (Supplemental Table S1; Figure 3). The 95% confidence intervals of the Spartina root accumulation rate and peak depth parameters also suggest that roots occurred shallower in the ambient CO2 treatment than in the elevated treatment. Living biomass was dwarfed by litter mass in all but the shallowest sections of the cores, and the Spartina community had higher litter mass than the Schoenoplectus community at all depths, resulting in an average of 48% more litter mass in the Spartina community under ambient conditions and 43% more in elevated treatments in the 1-m-deep cores (Table 1).
As part of these ongoing experiments at the GCReW experimental wetland, aboveground productivity and root productivity are evaluated annually using annual peak aboveground biomass and ingrowth cores, respectively [23,36,37]. We used these data to evaluate the relative allocation of growth to aboveground versus belowground structures in 1999, the same year we sampled the plots for belowground biomass by coring to 1 m. In the Spartina community, using ANOVA (N = 10), we found no differences between treatments in total aboveground biomass (p = 0.58), ingrowth core biomass (p = 0.21), or growth allocation. Growth allocation was assessed in three different ways: (i) ingrowth:shoot (p = 0.37), (ii) grass root:shoot (p = 0.61), and (iii) grass root + rhizome:shoot (p = 0.59). Similarly, in the Schoenoplectus community, we found no differences between treatments using one-way ANOVA (N = 10) with respect to total aboveground biomass (p = 0.51), ingrowth core biomass (p = 0.92), nor relative allocation to aboveground versus belowground structures as assessed three ways: (i) ingrowth:shoot (p = 0.85), (ii) total root:shoot (p = 0.57) (iii) root + rhizome:shoot biomass (p = 0.12).
There was a positive relationship between aboveground biomass and ingrowth core biomass in the Spartina community (linear regression R2 = 0.35; F-ratio = 4.43; p = 0.68), and a negative relationship between aboveground biomass and ingrowth cores biomass in the Schoenoplectus community (linear regression R2 = 0.24; F-ratio = 2.66; p = 0.14). Total belowground biomass did not relate across the plots with total aboveground biomass or with root productivity in either community (p > 0.20).

3.2. Belowground Biomass Separated by Plant Functional Group

In the 13th year of the experiment, the initially monotypic C3 sedge species Schoenoplectus community had significant aboveground grass biomass (see below). Belowground structures attributed to the S. americanus only occurred in appreciable amounts in the Schoenoplectus community where elevated CO2 increased the biomass of culms (described above), red rhizomes, and dark roots compared to the ambient treatment (Table 1 and Table 2; Figure 4). Culms and red roots had significantly higher C:N in the elevated CO2 treatment (Table 2). White roots and white rhizomes, which belong to grasses, occurred in both communities and displayed no effect of treatment on biomass or C:N (Table 1 and Table 2; Figure 4).
Comparing across the communities, we found significantly more white root biomass in the Spartina community compared to the Schoenoplectus community (mixed model N = 20; F-ratio = 37.07; DF = 1; p < 0.0001; Table 1), but no overall difference in white rhizomes between communities (F-ratio = 0.04; DF = 1; p = 0.84). For white roots, C:N was significantly higher in the Spartina community than the Schoenoplectus community (ANOVA F-ratio = 61.59, N = 20; p < 0.0001; Table 2), while the C:N of white rhizomes was higher in Schoenoplectus communities compared to Spartina communities (ANOVA F-ratio = 8.06; N = 20; p = 0.011; Table 2). Presumably, this reflects a difference in C:N between Spartina and Distichlis, the predominant grasses in the elevated and ambient Schoenoplectus community plots, respectively (see below and Figure 4 and Figure 5); however, it could also reflect differences in the small fraction of very young Schoenoplectus roots that are also initially white ([23,28] Curtis et al. 1990; Saunders et al. 2006).

3.3. Community Composition, Root:Shoot, and Plant Functional Type Responses to CO2 Treatment

In monospecific stands, the community response to an experimental treatment can reasonably be inferred to represent the average responses of a single species. This was the case with the Spartina community in this experiment in 1999, when belowground biomass was sampled. At that time, the Spartina community plots were monospecific stands in all but one of the chambers, where there was a small amount of D. spicata. S. patens was 100% of the average 470 g/m2 in aboveground biomass in the elevated plots and 98% of the average 413 g/m2 in the ambient plots. Therefore, treatment effects in this community directly reflect the responses of S. patens in the absence of competition with other species.
In contrast, the community composition of the Schoenoplectus plots in 1999 was a mix of C3 and C4 species (Figure 5), and their relative abundance differed between the experimental treatments. In the elevated CO2 treatment, 70% of the average 482 g/m2 of aboveground biomass was S. americanus, compared to only 40% of the 541 g/m2 in the ambient treatment (Figure 5). The remaining vegetation was mostly grasses, with overall shoot density co-dominated by S. patens (33% of total stems) and D. spicata (29% of total stems) in the elevated treatment, while D. spicata dominated (65% of total stems) compared to S. patens (21% of total stems) in the ambient treatment. A few stems of the woody shrub Iva frutescens contributed a large amount of biomass in one replicate plot (Chamber 12 in Figure 5), which was excluded from our analyses.
Since ambient and elevated CO2 chambers differed in species composition, it is possible that the effect of treatment on the Schoenoplectus community was mediated through shifts in species composition rather than a direct response by S. americanus to the CO2 treatment. We examined the relationship between S. americanus aboveground biomass and three different metrics of belowground biomass: (i) standing stock of S. americanus roots and rhizomes from the meter-deep cores, (ii) total belowground productivity from ingrowth cores (which were not separated by color into components), and (iii) culm biomass, which is the belowground portion of a stem. Treatment as a fixed factor and percent S. americanus aboveground biomass as a covariate explained 83% of the variation in root productivity from ingrowth cores (ANCOVA model R2 = 0.83; N = 10; F-ratio = 9.76; p = 0.01; Figure 6; Supplemental Table S3). In both elevated and ambient treatments, ingrowth belowground productivity was negatively correlated with the percentage of the aboveground biomass (AGB) that was S. americanus, though the slope was more negative in the elevated CO2 treatment. This relationship was weaker when the data were pooled across the treatments (Supplemental Figure S2). Neither culm biomass nor S. americanus belowground standing stock biomass was influenced by treatment, and there was no significant interaction. However, both were positively related to the fraction of aboveground S. americanus biomass (culms: R2 = 0.65; N = 10; F = 14.86; p = 0.0048. S. americanus belowground standing stock: R2 = 0.65; N = 10; F = 14.76; p = 0.0049; Figure 6; Supplemental Figure S2).
Aboveground productivity in each plot did not differ between CO2 treatments (ANOVA; N = 10; p = 0.51), despite the differences in plant species composition, because the aboveground productivity of grasses compensated for the lower productivity of S. americanus in the ambient treatment (which had very low S. americanus abundance). Total belowground productivity from ingrowth cores was also not significantly different between treatments (ANOVA; N = 10; p = 0.92), suggesting that root productivity from grasses compensated for lower S. americanus root productivity in the ambient CO2 treatment. However, this pattern of conservation of total community productivity (rates) through complementarity of grasses and sedges is not evident in belowground biomass standing stocks. Here, we see a difference between the CO2 treatments linked to the significant (R2 = 0.52; F-ratio = 8.58; p = 0.019) positive relationship between total belowground biomass and % ABG Schoenoplectus. Much of this difference in belowground standing stock biomass with community composition is driven by the greater biomass of rhizomes and culms of S. americanus compared to that of the grasses.
Taken together the relationships across treatments and different components of biomass or productivity (Supplemental Figures S3 and S4) lead us to the following understanding of how variation in plant species composition in the 10 Schoenoplectus community plots in 1999 influence our interpretation of the eCO2 response. The implications of variation in plant species composition across the 10 Schoenoplectus community plots in 1999 are fundamentally different for interpreting belowground productivity versus standing stock biomass data. Most previous observations of belowground responses to elevated CO2 at this site are based on annual growth rates measured by ingrowth bags, whereas we are reporting the standing stock biomass measured through soil coring. The two methods showed different responses, with no effect of elevated CO2 on total belowground productivity from ingrowth cores (ANOVA; N = 10; p = 0.92), a result that might be expected considering that sedges and grasses have roughly similar rates of productivity per area under ambient CO2 conditions [25], and the relatively high C4 grass biomass in both treatments muted the elevated CO2 response [49]. Thus, whereas the distinction between productivity and standing stock biomass is not particularly meaningful when considering aboveground dynamics in these species, where the shoots turn over annually, the distinction is important belowground, where these species are perennial and much of the production persists for several years.

4. Discussion

Our detailed examination of belowground biomass responses to 13 years of elevated CO2 enrichment highlights the importance of plant traits and community composition in regulating ecosystem responses to environmental change. Our results suggest that shifts in plant community composition dominate belowground responses to elevated CO2 and are more important than the direct responses of individual species. This is evident in the differences between the Spartina and Schoenoplectus communities at ambient CO2 concentrations, differences in their responses to the CO2 treatment, and differences in belowground biomass that reflect shifts in species composition within the Schoenoplectus community.

4.1. Effects of CO2 Treatment

Belowground biomass in the C4 Spartina community increased by 26% in response to elevated CO2, a response associated with higher root biomass and a slightly shallower root depth distribution. This result is surprising, considering that previous studies at this site have reported minimal effects of elevated CO2 treatments on Spartina communities with respect to aboveground biomass and belowground productivity [25,35,36,37,38], and C4 plants generally respond weakly to elevated CO2 [24,50]. However, elevated CO2 experiments with Spartina maritima and Spartina densiflora have reported positive responses, such as increased shoot growth, greater photosynthetic rates, and improved leaf water relations [51,52]. Spartina alterniflora has photosynthetic traits atypical of C4 plants [53], so perhaps other Spartina species, such as S. patens, do not respond to CO2 enrichment through the same photosynthetic mechanisms as strictly C4 plants.
Importantly, previous syntheses of belowground responses in this long-term study were based on annual root net primary productivity, measured by ingrowth cores [25]. The large Spartina (C4) community response in the present study, a novel result for this site, may reflect the fact that belowground standing stock biomass captured the net effects of our treatments on both net primary production and mortality over the 13 years preceding our coring campaign. Two explanations for different results from the two methods are: (i) elevated CO2 caused a small annual increase in grass belowground productivity that accumulated over 13 years to yield a large difference in standing stock, and (ii) elevated CO2 increased root and rhizome lifespan. These two mechanisms are not mutually exclusive. Support for hypothesis (i) is that previous syntheses reporting no effect of elevated CO2 on root productivity in the Spartina community were based on arbitrary p-value statistical thresholds even though average rates tended to be higher in the elevated than ambient treatments. For example, Erickson et al. [25] reported that there was no response to elevated CO2 based on a p-value of 0.12. We currently do not have data to evaluate hypothesis (ii) at our site, and lifespan responses to elevated CO2 in other ecosystems are inconclusive, with positive, negative, and null effects reported [54,55,56].
The Schoenoplectus community had 29% more belowground biomass (standing stock) in the elevated than in the ambient CO2 treatment, due primarily to higher rhizome biomass. Elevated CO2 also caused changes in tissue chemistry, with higher C:N ratios in red roots, red rhizomes, and culms. These data are consistent with our previous work showing that S. americanus responds directly to enriched CO2 with higher photosynthesis, quantum yield, net ecosystem CO2 exchange, shoot density, shoot production, root production, and root/shoot ratio [27,35,57]. However, our results indicate that in 1999 belowground standing stock treatment effects in the Schoenoplectus community were confounded by large differences in plant species composition between CO2 treatments. Whether the relatively high proportion of S. americanus aboveground biomass in the elevated CO2 plots was an indirect effect of the treatment is an open question. However, we note that elevated CO2 has not changed the co-dominance of the three major plant species in mixed-community plots over the nearly four decades of the experiment, even while the relative abundance of the species has changed slowly for other reasons (i.e., sea level rise). This suggests that plot-scale variation in species abundance in 1999 may not have been in response to elevated CO2 but caused by one or more external factors [57].

4.2. How Community Differences Impact Soil Carbon, Responses to SLR, and Methane Fluxes

Our study demonstrates that shifts in dominant plant species possessing distinct root traits can dramatically alter ecosystem-relevant belowground biomass characteristics. Our observation that the Spartina community had just 60% of the belowground biomass standing stock of the Schoenoplectus community (2310 versus 3907 g/m2) suggests that S. americanus has a stronger impact on soil surface elevation than S. patens through soil volume displacement. This supports Cherry et al. [9], who showed that soil elevation gain was positively related to aboveground biomass production of S. americanus in mesocosm experiments with mixed-species communities, and that this effect was mediated by the contribution of the volume of S. americanus shoot bases (i.e., culms). Although we lack data on how the biomass we measured relates quantitatively to the volume of live roots and rhizomes, their significant contribution to marsh elevation has been observed or inferred in this marsh [22] and in other tidal wetland ecosystems [58,59,60,61].
Because belowground biomass is advantageous for building marsh elevation, the relatively high belowground biomass of S. americanus communities presumably makes them less resilient when subjected to stress or plant mortality that reduces belowground biomass. Elevation loss occurs via compaction of the roots and rhizomes due to the loss of turgor and collapse of aerenchyma spaces [12]. As species differ in attributes related to living and dead tissues, such as aerenchyma volume, lignin content, and water content, data on how such traits vary in relation to the dry weights measured here are necessary to fully understand how the belowground biomass of these two species contributes to surface elevation, and how they may mediate community differences in elevation gain or loss with shifts in the plant species composition observed at this site [62].
The chemical constituents of plant materials and their stoichiometry influence rates of litter decomposition [63], influencing changes in soil volume through biomass turnover and decay. Previous work has demonstrated that S. americanus rhizomes contain more hot water-soluble compounds, less cellulose, less lignin, lower C:N, and lower lignin:N ratios than S. patens rhizomes [28]. All these features should favor relatively high decomposition rates in S. americanus, indicating that Schoenoplectus communities may be more susceptible to decomposition-driven elevation loss than S. patens communities. Indeed, Jones et al. [10] reported that S. patens aboveground biomass decomposes more slowly than S. americanus biomass. Interestingly, while elevated CO2 raises S. americanus C:N ratios, it does not necessarily alter decomposition rates [10], again demonstrating that trait differences between plant species may be more important than elevated CO2-induced changes in those traits.
These results lead to the hypothesis that the high belowground productivity and standing stock biomass of S. americanus are offset by rapid decomposition rates, while the low productivity and standing stock of S. patens are offset by relatively slow decomposition rates. The net effects of these offsetting traits may favor greater carbon storage in the Spartina community, which had 40–48% more belowground litter than the Schoenoplectus community. Differences in belowground litter accumulation may prove to be important for predicting soil carbon sequestration rates and ecosystem resilience to sea level rise, as mesohaline S. patens-dominated communities transition to S. americanus-dominated communities at our site and elsewhere in the Chesapeake Bay [64].
Finally, differences in belowground species traits can have important implications for greenhouse gas-relevant microbial processes such as decomposition and methane emissions. In this respect, S. patens and S. americanus have strikingly different belowground influences, with S. patens exhibiting higher root exudation, lower root oxygen loss, and consequently a more reduced rhizosphere per unit root surface area than S. americanus [16]. These functional traits appear to play a pivotal role in setting soil redox status, with increases in S. patens favoring more reduced soils and increases in S. americanus more oxidized soils [15,16]. The interplay of these factors was hypothesized to explain reductions in carbon accumulation [15] and methane emissions [65,66] in response to elevated CO2 in the Schoenoplectus community at our study site. The responses are ultimately mediated by the rhizosphere through a series of plant-microbe interactions that begin with CO2-stimulation of photosynthesis, leading to higher aboveground and belowground productivity (often with an increase in root/shoot ratio), increased soil redox potentials, and ultimately higher rates of decomposition and lower methane flux [15]. It is uncertain how elevated CO2-induced deepening of belowground biomass in the Schoenoplectus community affects elevation or biogeochemistry, but presumably it increases the depth of the soil profile exposed to root O2 loss. Collectively, our data illustrate how belowground plant traits and their variation within and among species drive important ecosystem functions.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/hydrobiology4010008/s1, Supplement Table S1: Details of curve fit and equation fitting the Logistic 2-parameter curve to the cumulative biomass by depth data; Supplemental Table S2: Summary of Carbon isotope ratios from the different components of belowground biomass in the different communities and treatments; Supplemental Table S3: The overall relationship between % Schoenoplectus in the above ground biomass and 3 response variables of interest; Supplemental Figure S1: Summary of Carbon isotope ratios from the different components of belowground biomass in the different communities and treatments; Supplemental Figure S2: The overall relationship between % Schoenoplectus in the above ground biomass and 3 response variables of interest; Supplemental Figure S3: Correlations between components of aboveground and belowground biomass (g/m2), in the Schoenoplectus plots; Supplemental Figure S4: Box plots summarizing the effects of CO2 treatment on different aspects of aboveground biomass in the Schoenoplectus community plots.

Author Contributions

Conceptualization, B.G.D. and J.P.M.; Methodology, J.P.M.; Formal Analysis, R.C.; Investigation, J.P.M.; Resources, B.G.D. and J.P.M.; Data Curation, R.C. and J.P.M.; Writing—Original Draft Preparation, R.C.; Writing—Review and Editing, R.C. and J.P.M.; Visualization, R.C.; Supervision, J.P.M.; Project Administration, J.P.M.; Funding Acquisition, R.C. and J.P.M. All authors have read and agreed to the published version of the manuscript.

Funding

Simons Foundation Pivot Fellowship; Department of Energy (DOE-98-59-MP-4; DOE-FG-97ER62458; DE-SC0008339), the National Science Foundation (DEB-0950080, DEB-1457100, DEB-1557009, DEB-2051343), and the Smithsonian Environmental Research Center.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

New data not previously published in Megonigal and Holmquist ([42] 2021) or Zhu et al. ([40] 2022) or available at https://serc.si.edu/gcrew/CO2data (accessed on 30 March 2024), are available in FigShare: https://doi.org/10.25573/data.27933732.v1.

Acknowledgments

We thank the Simons Foundation Pivot Fellowship program that supported RC during the preparation of this manuscript. We thank Colin Saunders for advice on soil coring and root sorting methods; Christine Fitzgerald for development and implementation of protocols, sample processing, data curation, and data analysis; Bill Kornicker for sample processing and data analysis; and Gary Peresta for field support.

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. The contribution of belowground biomass (positive values) and litter (negative values) in the top 1 m of the Spartina and Schoenoplectus communities under the two experimental CO2 treatments. Dead litter is presented as negative values for visual separation from living biomass. Values are averages of two cores in each of five replicate chambers in each community.
Figure 1. The contribution of belowground biomass (positive values) and litter (negative values) in the top 1 m of the Spartina and Schoenoplectus communities under the two experimental CO2 treatments. Dead litter is presented as negative values for visual separation from living biomass. Values are averages of two cores in each of five replicate chambers in each community.
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Figure 2. Depth distribution of belowground litter (detritus), rhizomes, roots, and culms. Data points are biomass (g/cm3) in the section of the core subsampled. The plotted depth is the center of each depth interval. Lines are a fitted spline, with shading representing the 95% confidence limits. Ambient treatments shown by the solid line and elevated CO2 by the dashed line. The Schoenoplectus community is blue and the Spartina community is red.
Figure 2. Depth distribution of belowground litter (detritus), rhizomes, roots, and culms. Data points are biomass (g/cm3) in the section of the core subsampled. The plotted depth is the center of each depth interval. Lines are a fitted spline, with shading representing the 95% confidence limits. Ambient treatments shown by the solid line and elevated CO2 by the dashed line. The Schoenoplectus community is blue and the Spartina community is red.
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Figure 3. Normalized cumulative mass with depth illustrating the differences between the two community types and treatments for roots, rhizomes, and culms, resulting from the statistically significant differences in the coefficients of the logistic two-parameter curve fits. Graphs to the left show curves fitted through the data points separated by CO2 treatment and plant community, while graphs to the right overlay the curves to highlight differences between the species and treatments. Data are plotted to half the full core depth (50 cm) to emphasize differences in the upper 20 cm of the soil profile.
Figure 3. Normalized cumulative mass with depth illustrating the differences between the two community types and treatments for roots, rhizomes, and culms, resulting from the statistically significant differences in the coefficients of the logistic two-parameter curve fits. Graphs to the left show curves fitted through the data points separated by CO2 treatment and plant community, while graphs to the right overlay the curves to highlight differences between the species and treatments. Data are plotted to half the full core depth (50 cm) to emphasize differences in the upper 20 cm of the soil profile.
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Figure 4. Mean biomass for aboveground biomass identified to species (positive values) and belowground components (negative values) attributed to either the sedge S. americanus (red structures) or the grasses S. patens and D. spicata (white structures). Negative values for the belowground components are for visual separation.
Figure 4. Mean biomass for aboveground biomass identified to species (positive values) and belowground components (negative values) attributed to either the sedge S. americanus (red structures) or the grasses S. patens and D. spicata (white structures). Negative values for the belowground components are for visual separation.
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Figure 5. Contribution of plant species to the aboveground biomass and total shoot density in the 10 Schoenoplectus community plots in 1999, after 13 years of elevated CO2 treatment. The large biomass of a single Iva plant in plot 12 was eliminated in this analysis. Numbers below each bar are the assigned plot numbers in the experiment.
Figure 5. Contribution of plant species to the aboveground biomass and total shoot density in the 10 Schoenoplectus community plots in 1999, after 13 years of elevated CO2 treatment. The large biomass of a single Iva plant in plot 12 was eliminated in this analysis. Numbers below each bar are the assigned plot numbers in the experiment.
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Figure 6. Relationships between S. americanus aboveground dominance (% of aboveground biomass) in the community and three measures of belowground dominance: (i) culm biomass, (ii) total root productivity in 1999, as assessed by ingrowth cores, and (iii) % of roots and rhizomes in the belowground biomass standing stock attributed to S. americanus (Table 1 and Table S2).
Figure 6. Relationships between S. americanus aboveground dominance (% of aboveground biomass) in the community and three measures of belowground dominance: (i) culm biomass, (ii) total root productivity in 1999, as assessed by ingrowth cores, and (iii) % of roots and rhizomes in the belowground biomass standing stock attributed to S. americanus (Table 1 and Table S2).
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Table 1. Comparisons of belowground components of biomass and litter between elevated and ambient treatments for each community, and between components within species and treatments. Statistical tests are mixed models with plot treated as a random effect nested within treatment (N = 10 cores/treatment). Hyphens indicate components that were absent in the particular community and treatment combination. Bold highlights values considered to be statistically significant. BGB: Belowground biomass.
Table 1. Comparisons of belowground components of biomass and litter between elevated and ambient treatments for each community, and between components within species and treatments. Statistical tests are mixed models with plot treated as a random effect nested within treatment (N = 10 cores/treatment). Hyphens indicate components that were absent in the particular community and treatment combination. Bold highlights values considered to be statistically significant. BGB: Belowground biomass.
CommunityVariableTreatmentMean Biomass (g/m2) (s.e.)F-Ratiop-Value
Community Totals
SchoenoplectusBGBAmbient3409 (369)8.010.022
Elevated4407 (450)
SpartinaBGBAmbient2042 (105)4.520.066
Elevated2579 (182)
SchoenoplectusLitterAmbient9514 (517)0.390.55
Elevated10,069 (551)
SpartinaLitterAmbient14,105 (542)0.0800.78
Elevated14,426 (676)
SchoenoplectusAll RootsAmbient1837 (156)0.570.47
Elevated2044 (179)
SpartinaAll RootsAmbient1515 (66)3.660.092
Elevated1862 (120)
SchoenoplectusAll RhizomesAmbient1397 (292)3.990.08
Elevated2002 (318)
SpartinaAll RhizomesAmbient527 (78)2.340.16
Elevated717 (91)
SchoenoplectusAll CulmsAmbient174 (48)13.330.0065
Elevated361 (66)
Roots and Rhizomes Divided by Category
SchoenoplectusWhite rhizomesAmbient676 (146)0.550.48
Elevated519 (154)
SpartinaWhite rhizomesAmbient527 (78)2.340.16
Elevated717 (91)
SchoenoplectusRed rhizomesAmbient760 (235)5.540.046
Elevated1482 (264)
SpartinaRed rhizomesAmbient---
Elevated---
SchoenoplectusWhite rootsAmbient957 (84)0.410.54
Elevated856 (104)
SpartinaWhite rootsAmbient1485 (69)2.970.12
Elevated1803 (122)
SchoenoplectusRed rootsAmbient581 (95)0.970.35
Elevated776 (117)
SpartinaRed rootsAmbient18 (5)1.130.32
Elevated28 (7)
SchoenoplectusDark rootsAmbient300 (33)4.060.078
Elevated412 (42)
SpartinaDark rootsAmbient12 (6)1.060.34
Elevated31 (12)
Table 2. Stoichiometry of carbon and nitrogen in components of belowground biomass in 1-m deep cores. Values are from material pooled from two replicate cores per plot and five replicate plots per treatment yielding N = 5 for each mean ± standard error (s.e.). Hyphens indicate components in a sample that were absent or yielded insufficient material for analysis in a particular community and treatment combination. Bold highlights values considered to be statistically significant.
Table 2. Stoichiometry of carbon and nitrogen in components of belowground biomass in 1-m deep cores. Values are from material pooled from two replicate cores per plot and five replicate plots per treatment yielding N = 5 for each mean ± standard error (s.e.). Hyphens indicate components in a sample that were absent or yielded insufficient material for analysis in a particular community and treatment combination. Bold highlights values considered to be statistically significant.
CommunityVariableTreatmentMean C:N (s.e.)F-Ratiop-Value
SchoenoplectusWhite rhizomesAmbient98.80 (5.63)0.700.43
Elevated107.15 (8.26)
SpartinaWhite rhizomesAmbient75.52 (5.41)1.640.24
Elevated88.91 (8.96)
SchoenoplectusRed rhizomesAmbient52.49 (8.04)1.940.20
Elevated70.39 (10.02)
SpartinaRed rhizomesAmbient---
Elevated---
SchoenoplectusWhite rootsAmbient71.48 (2.18)2.280.17
Elevated80.02 (5.22)
SpartinaWhite rootsAmbient105.71 (3.14)0.210.65
Elevated108.21 (4.40)
SchoenoplectusRed rootsAmbient84.73 (1.99)3.820.09
Elevated94.55 (4.61)
SpartinaRed rootsAmbient---
Elevated---
SchoenoplectusDark rootsAmbient79.08 (2.52)2.310.17
Elevated85.71 (3.56)
SpartinaDark rootsAmbient---
Elevated---
SchoenoplectusCulmsAmbient81.86 (4.04)6.620.02
Elevated99.51 (5.39)
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Collin, R.; Drake, B.G.; Megonigal, J.P. What’s Going on Down There? Impacts of Long-Term Elevated CO2 and Community Composition on Components of Below-Ground Biomass in a Chesapeake Bay Saltmarsh. Hydrobiology 2025, 4, 8. https://doi.org/10.3390/hydrobiology4010008

AMA Style

Collin R, Drake BG, Megonigal JP. What’s Going on Down There? Impacts of Long-Term Elevated CO2 and Community Composition on Components of Below-Ground Biomass in a Chesapeake Bay Saltmarsh. Hydrobiology. 2025; 4(1):8. https://doi.org/10.3390/hydrobiology4010008

Chicago/Turabian Style

Collin, Rachel, Bert G. Drake, and J. Patrick Megonigal. 2025. "What’s Going on Down There? Impacts of Long-Term Elevated CO2 and Community Composition on Components of Below-Ground Biomass in a Chesapeake Bay Saltmarsh" Hydrobiology 4, no. 1: 8. https://doi.org/10.3390/hydrobiology4010008

APA Style

Collin, R., Drake, B. G., & Megonigal, J. P. (2025). What’s Going on Down There? Impacts of Long-Term Elevated CO2 and Community Composition on Components of Below-Ground Biomass in a Chesapeake Bay Saltmarsh. Hydrobiology, 4(1), 8. https://doi.org/10.3390/hydrobiology4010008

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