Jillian Dunic
The predicted response of microbial communities and functions to salt marsh
restoration in the Neponset River Reservation
Current status of the Neponset River Reservation
The Neponset River Reservation (NRR) is a salt marsh ecosystem in the lower
Neponset River that has been severely perturbed over the last century. In the 1930’s,
the area was heavily ditched which likely lead to drainage of the marsh platform and a
relative increase in the marsh elevation. Then, in the 1960’s the lower Neponset was
used to store dredge spoils from construction of the route 93 embankment (Tom Palmer
pers. comm. 2014). These fill areas raised marsh elevations such that they are no
longer marsh habitats (Fig. 1). The area to be restored is the south side of the
reservation, which has two major creeks (Fig. 1). This marsh has been classified by the
US FWS as 82.12 acres of intertidal estuarine habitat, which is considered to be
emergent, meaning that this habitat is characterized by perennial, herbaceous
hydrophytes (Fig. 1). This marsh is subject to irregular flooding by tidal waters and is
heavily ditched. An additional 35.26 acres is considered estuarine, intertidal with
unconsolidated shores. Unconsolidated substrates have less that 75% cover of stones,
boulders, and bedrock, less than 30% vegetation cover, and is regularly flooded
(Federal Geographic Data Committee 2013). Currently, tidal flow and mixing is
restricted upstream of the Granite Avenue Bridge (Fig. 2), while upstream, freshwater
inputs are restricted by dams, namely the Baker Dam (Fig. 2). In particular, the
restriction of tidal flow caused by the Granite Avenue Bridge has reduced tidal mixing
in the NRR, leaving salinity less than 18 ppt even at high tide in the summer (Gardner
et al. 2005, Fig. 3). The changes that are most likely to affect microbial processes in
the marsh following restoration efforts in the NRR are increased salinity and changes to
the plant community (Blum et al. 2004). These factors are strong drivers of microbial
community structure and processes like nitrification (Giblin et al. 2010, Philippot et al.
2013) and carbon mineralization (Weston et al. 2010).
Biogeochemical cycling potential
Ammonia-oxidizing bacteria (AOB) are an important first step in nitrification,
because they convert ammonium to NO2, which is rapidly oxidized to NO3. Bernhard et
al. (2005) found that ammonia-oxidizing bacteria diversity, at sites in the Plum Island
Estuary, decreased as salinity increased over a range of 8.7, 24.7, to 31.7 psu.
However, AOB diversity was not correlated with with ammonium concentrations. In a
follow up study, Bernhard et al. (2007) quantified potential nitrification rates using
bacterial communities spanning a similar salinity gradient. Lab experiments to
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calculate potential nitrification rates showed that there were different community
responses to increasing salinity. Importantly, they found that communities taken from
marsh habitats where salinities were 10 psu or greater had similarly high potential
nitrification rates as salinity was increased from 5 psu to 30 psu. This may indicate that
given the current salinity of the NRR, as salinities increase, current microbial
communities found in the NRR are likely capable of at least maintain rates of
nitrification.
With the removal of P. australis it is unclear how nitrogen loading will change,
given that P. australis can immobilize high quantities of nitrogen. For example, P.
australis has been demonstrated to uptake 60% more nitrogen than S. patens, and 50%
more nitrogen than S. alterniflora. Microbial community composition and functioning
have shown resilience to moderate levels (70 µM) of nitrogen loading (Bowen et al.
2009, Bowen et al. 2011). Ammonia measurements in the NRR are similar to those
studied at the long-term nutrient enrichment experiment, while total nitrogen are
much greater than those used in the long-term enrichment experiment (Water Quality
Data NRWA 2014). Although there were no water quality measurements from within the
NRR, the Neponset River Watershed Association (NRWA) runs a Citizen Water Monitoring
Network (CWMN) that has measured water quality since 2002. In the 2014, in May,
June, July, August, and September, NH3 concentrations have ranged from 28 µM ± 30
µM, in September up to 0.104 µM ± 68 µM, (Fig. 4). Total dissolved nitrogen
measurements are even greater, where maximum values were measured in June (1440
µM ± 220 µM) and minimum values in August (850 µM ± 0.28 µM).
If microbial community and functioning is resilient at these higher levels of
nutrient enrichment found in the Neponset River, then nitrogen input at this moderate
level was not shown to increase rates of peat decomposition (Bowen et al. 2009),
which, suggests that if there is an apparent increase in nitrogen when P. australis is
removed either manually or by increased tidal inundation, nitrogen that has already
been sequestered in P. australis recalcitrant stem tissues remain buried in the
sediments. Although nitrogen enrichment may not alter decomposition rates, salinity
may alter these rates. Weston et al. 2011 examined the effect of salt water intrusion
on microbial respiration rates and organic carbon remineralization in tidal freshwater
marsh soils. They found that as salinity was increased to 5 ppt, rates of microbial
decomposition increased. This increase in decomposition rates corresponds to
increasing rates of sulphate reduction, while the rate of methanogenesis was
maintained. However, in an early study of methane emissions along a salinity gradient
in salt marshes by Bartlett et al. (1987), as salinities increased from 5 to 17 ppt,
methane production decreased. Methane emissions were greatest (± 3.4 g CH4 m-2 yr-1)
at salinities of 13 ppt and decreased to 5.6 ± 0.7 g CH4 m-2 yr-1 at salinities greater than
17 ppt. These results suggest that as salinities increase with restoration of tidal flow in
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the NRR, methane production should decrease on an annual basis as the NRR marsh will
likely have salinity values greater than 17 ppt for a large part of the year.
Biodiversity and ecosystem functioning
Given the suite of environmental factors that may change rapidly and which may
interact in unpredictable ways with respect to causing changes in microbial
functioning, it is unclear how microbial functions will respond to restoration. Recent
research suggests that increasing biodiversity will increase ecosystem functioning
(Philippot et al. 2013, Jones et al. 2014). For example, genetic diversity of the nosZ
community, a group of microbes that can reduce nitrous oxide, is related to the ability
of that community to reduce nitrous oxide to dinitrogen (Jones et al. 2014). What
controls the diversity and structure of a microbial community is still unclear. The
diversity of the nosZ community is related to the ratio of nirS and nirK abundances and
is related to the soil texture. However, the specific soil texture that promoted N 2O
reduction was not identified, and furthermore, this work was done in terrestrial
systems, therefore, it is unclear how well the soil characteristics that promote N2O
reduction or diversity of the microbial community would translate into a salt marsh.
But this does suggest that a better understanding of the microbial community structure
and identifying factors that could promote diversity in these communities in a salt
marsh could be used to improve microbial marsh functioning.
One benefit of restoration of a degraded marsh, rather than creation of a marsh
de novo is that the original microbial community may persist and be able to restore
functioning when environmental conditions are returned to a restored state. In a set of
transplant experiments between freshwater and brackish waters in an estuary in Maine,
Reed and Martiny (2013) found that even after two months in the new environments,
microbial community functioning, as measured by enzyme activity still exhibited an
origin effect, indicating that original community composition was an important aspect
of microbial functioning.
Current understanding of microbial communities and the relationship between
these communities and the functions that they provide is limited. Restoration will bring
a suite of changes to salinity, plant communities, and porewater chemistry, making it
difficult to predict the response of the microbial community and in particular, how
microbial functioning will respond to the combined effect of these changes.
Furthermore, future restoration events such as the removal of upstream dams are likely
to have downstream consequences on important factors affecting the marsh as a whole
and microbial functioning. However, even if we were to gather more data about
aspects of the Neponset River Reservation, such as porewater chemistry data, we are
limited in the predictions that we can make. More than anything, monitoring microbial
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functions prior to, during, and after the restoration, and comparing these functions to
predictions that have been made may be the most valuable way to consider microbes in
the NRR.
Literature Cited
Bartlett, K., D. Bartlett, R. Harriss, and D. Sebacher. 1987. Methane emissions along a salt marsh salinity gradient.
Biogeochemistry 4:183–202.
Bernhard, A. E., T. Donn, A. E. Giblin, and D. A Stahl. 2005. Loss of diversity of ammonia-oxidizing bacteria
correlates with increasing salinity in an estuary system. Environmental Microbiology 7:1289–97.
Bernhard, A. E., J. Tucker, A. E. Giblin, and D. Stahl. 2007. Functionally distinct communities of ammonia-oxidizing
bacteria along an estuarine salinity gradient. Environmental Microbiology 9:1439–47.
Blum, L. K., M. S. Roberts, J. L. Garland, and A. L. Mills. 2004. Distribution of microbial communities associated
with the dominant high marsh plants and sediments of the United States East Coast. Microbial Ecology
48:375–88.
Bowen, J. L., B. C. Crump, L. A. Deegan, and J. E. Hobbie. 2009. Increased supply of ambient nitrogen has minimal
effect on salt marsh bacterial production. Limnology and Oceanography 54:713–722.
Bowen, J. L., B. B. Ward, H. G. Morrison, J. E. Hobbie, I. Valiela, L. A Deegan, and M. L. Sogin. 2011. Microbial
community composition in sediments resists perturbation by nutrient enrichment. The ISME Journal 5:1540–
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Federal Geographic Data Committee. 2013. Classification of wetlands and deepwater habitats of the United States.
FGDC-STD-004-2013. Second Edition. Wetlands Subcommittee, Federal Geographic Data Committee and
U.S. Fish and Wildlife Service, Washington, DC.
Gardner, G. B., R. F. Chen, and A. Berry. 2005. High-resolution measurements of chromophoric dissolved organic
matter (CDOM) in the Neponset River Estuary, Boston Harbor, MA. Marine Chemistry 96:137–154.
Giblin, A. E., N. B. Weston, G. T. Banta, J. Tucker, and C. S. Hopkinson. 2010. The effects of salinity on nitrogen
losses from an oligohaline estuarine sediment. Estuaries and Coasts 33:1054–1068.
Jones, C. M., A. Spor, F. P. Brennan, M.-C. Breuil, D. Bru, P. Lemanceau, B. Griffiths, S. Hallin, and L. Philippot.
2014. Recently identified microbial guild mediates soil N2O sink capacity. Nature Climate Change 4:801–
805.
Philippot, L., A. Spor, C. Hénault, D. Bru, F. Bizouard, C. M. Jones, A. Sarr, and P.-A. Maron. 2013. Loss in
microbial diversity affects nitrogen cycling in soil. The ISME Journal 7:1609–19.
Reed, H. E., and J. B. H. Martiny. 2013. Microbial composition affects the functioning of estuarine sediments. The
ISME Journal 7:868–79.
Water Quality Data | Neponset River Watershed Association. (n.d.). Retrieved November 18, 2014, from
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http://www.neponset.org/projects/water-quality/water-quality-and-cwmn/cwmn-data/
Weston, N. B., M. A. Vile, S. C. Neubauer, and D. J. Velinsky. 2010. Accelerated microbial organic matter
mineralization following salt-water intrusion into tidal freshwater marsh soils. Biogeochemistry 102:135–151.
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Figure 1. United States Fish and Wildlife Services National Wetlands Inventory, shaded
polygons represent wetlands with classifications labelled. The two relevant
habitats are the E2EM1Pd (estuarine intertidal with persistent vegetation that is
irregularly flooded with salt water and has been ditched), and the E2USN
(estuarine intertidal with unconsolidated shore and less than 30% vegetation
cover, this habitat is regularly flooded). These wetland designations were based
off data collected by Cowardin et al. 1979, and show former marsh areas raised
by dredge spoils. This includes the dike found along the northwest edge of
Gulliver’s Creek.
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Figure 2. United States Geological Survey orthophoto topographical map from 1987.
Significant points are indicated: the Baker dam (restricting river flow and
sediment load), the Granite Avenue Bridge (restricting tidal input and mixing),
and Gulliver’s Creek (additional source of freshwater input).
Figure 3. Salinity ranges in the lower Neponset River as measured by Gardner et al.
(2005, Figure 12) at (a) high tide August 22, 2002, and (b) low tide, August 22,
2002. Data were collected from the first 0.3 m of the water column.
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1.6
Mean Concentration (mM)
1.4
1.2
1.0
0.8
0.6
0.4
0.2
0.0
May
June
July
August
September
Month
Figure 4. Nitrogen data from 2014 Neponset River Watershed Association Citizen Water
Monitoring Network within the Neponset watershed. Triangles indicate total
dissolved nitrogen measured, circles indicate dissolved NH3. Error bars are equal
to one standard deviation.
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