WETLANDS, Vol. 29, No. 1, March 2009, pp. 196–203
’ 2009, The Society of Wetland Scientists
EFFECTS OF NITROGEN AND PHOSPHORUS ADDITIONS ON PRIMARY
PRODUCTION AND INVERTEBRATE DENSITIES IN A GEORGIA (USA) TIDAL
FRESHWATER MARSH
Joshua W. Frost*, Tymeri Schleicher, and Christopher Craft
School of Public and Environmental Affairs, Indiana University, Bloomington, Indiana, USA 47405
*Current address: Carolina Wetland Services, Inc., 550 E. Westinghouse Blvd., Charlotte, North Carolina, USA
28273. E-mail: [email protected]
Abstract: We added nitrogen (N), phosphorus (P), and N+P to a Zizaniopsis miliacea (Giant Cutgrass)
dominated tidal freshwater marsh in Georgia USA to investigate nutrient limitation of tidal freshwater
marsh primary production and invertebrate densities. After two years, aboveground biomass was
significantly greater in the plots receiving N (2130 g m22), and N+P (2066 g m22) than in the control
(886 g m22) and P (971 g m22) only treatments. We observed no enrichment of leaf N or P in response to
nutrient additions. Rather leaf N decreased and C:N increased in plots receiving N, suggesting that leaf N
was diluted by increased production of carbon laden structural components used to support increased
plant height. N:P ratios (mol:mol) of the plant tissue were consistently , 30 (14–27) in the treatment
plots, also suggesting N limitation of primary production. Total densities of benthic invertebrates and
oligochaete worms (primarily Tubificidae and Lumbriculidae) were significantly greater in the N+P plots
than in the other treatments after two years of nutrient additions. There were no clear differences in
diversity of benthic invertebrates among treatments. Our results suggest that tidal freshwater marsh
primary and secondary production is limited or co-limited by N, and thus, like estuaries and salt marshes,
are susceptible to N enrichment and eutrophication.
Key Words: biomass, eutrophication, nutrients, vegetation, Zizaniopsis miliacea
Kiehl et al. 1997), although phosphorus limitation
has been demonstrated in a few studies (Tyler 1967,
Teal 1986). Nitrogen and N+P limitation has also
been reported for brackish marshes (Burdick et al.
1989, Whigham 1990). Secondary production in salt
marshes is controlled by nitrogen availability as well
(Slansky and Feeny 1977, Vince et al 1981, Keats et
al 2004). Keats et al (2004) conducted an in situ
fertilization experiment where five different levels of
nitrogen (0–33.8 mmol DIN m2 2d) were added to
mesocosms containing Ruppia maritima. After one
growing season, numbers of r-selected, small opportunistic benthic invertebrate species increased, with
decreases in grazer specialists. In another study,
additions of N and NPK increased insect herbivore
biomass through its effect of increasing biomass and
leaf N-content of Spartina alterniflora (Vince et al
1981). Long-term (15 year) additions of NPK to a
salt marsh tidal creek of the Great Sippewissett
Marsh (MA, USA) increased macrofaunal density
and production (primarily oligochaete worms)
relative to control plots (Sarda et al.1996).
Much less is known about nutrient limitation of
tidal freshwater marshes. Studies suggest that tidal
freshwater marsh vegetation is limited by either
nitrogen (Morse et al. 2004) or phosphorous
INTRODUCTION
Tidal freshwater marshes exist at the headwaters
of river-dominated estuaries where diurnal astronomical tides penetrate, but still allow the marshes
to be inundated by freshwater river flow. Tidal
freshwater marshes are less common than salt
marshes and brackish marshes, and it is estimated
that there are 0.8 Mha of freshwater tidal marshes
compared to 1.9 Mha of salt marsh (Mitsch and
Gosselink 2000). Less is known about tidal freshwater marshes relative to other tidal wetlands,
although they are thought to be as or more
productive than highly productive salt marshes
(Doumlele 1981). Net primary production (NPP)
of these wetlands ranges from about 1000 to
3000 g m22 yr21 (Odum et al. 1984, Sasser and
Gosselink 1984, Visser 1989, White 1993, Sasser et
al. 1995).
Nutrient availability frequently governs primary
production of tidal marshes (Broome et al. 1975,
Odum 1988) and other wetlands (Onuf et al. 1977,
Craft et al. 1995). In salt marshes, nitrogen
limitation of vegetation has been shown in most
studies (Sullivan and Daiber 1974, Valiela and Teal
1974, Leendertse 1995, Jefferies and Perkins 1997,
196
Frost et al., NUTRIENT ENRICHMENT OF TIDAL FRESHWATER MARSHES
197
(Paludan and Morris 1999, Sundareshwar and
Morris 1999) as has been inferred from N:P ratios
of sediments, above ground biomass, and phosphorus uptake rates in plants. Morse et al. (2004) added
22.5 g N m22 as urea and/or 11.2 g P m22 as triple
super phosphate to four replicate treatment plots
(N, P, N+P, and control) to determine nutrient
limitation of tidal freshwater marsh primary production. However, they did not observe a growth
response to the fertilizer treatments over the oneyear study. Thus, studies to date offer no clear
indication of the source (N or P) of nutrient
limitation of tidal freshwater marsh primary or
secondary production.
We added nitrogen (N), phosphorus (P), and N+P
to plots in a tidal freshwater marsh in Georgia
(USA) for two years to identify which, if either,
nutrient limits primary and secondary productivity.
Aboveground plant biomass, leaf N, leaf P, benthic
invertebrate density, and invertebrate taxon richness
were measured to identify the source, N or P, of
nutrient limitation and its effect on primary and
secondary producers.
METHODS
Sixteen 2 m 3 2 m unenclosed plots were
established in a tidal freshwater marsh on Hammersmith Creek near the head of the Altamaha River
estuary (Figure 1). The area has a diurnal tidal
range of 2.3 m. Plots were separated by buffers of 2–
3 m to minimize fertilizer movement between plots.
The vegetation consists of a near-monoculture of
Zizaniopsis miliacea (Giant Cutgrass), with Pontedaria cordata (Pickerel weed) contributing to , 3%
of the total vegetation cover. Treatments consisted
of additions of N, P, N+P, and no additions
(control), replicated four times. Nitrogen and
phosphorus was broadcasted by hand, at low tide
when no water was present on the surface, twice a
year (March, May) at annual rates of 50 g N
m22 yr21 and 10 g P m22 yr21 beginning in 2004.
Triple superphosphate (45% P2O5) was used as the
phosphorus source. In year 1, N was added as water
soluble ammonium chloride (NH4Cl). In year 2, we
switched to a polymer coated urea CO(NH2)2
(Polyon, Pursell Technologies Inc., Sylacauga, AL,
USA), a 9-month timed-released fertilizer, to ensure
a constant, longer lasting supply of N in the
treatment plots.
Net primary production was estimated by nondestructive measurements of aboveground biomass
at the end-of-the growing season (October). Birch
and Cooley (1982) reported that monthly measurements of aboveground biomass of Zizaniopsis
Figure 1. Map of study area located on Hammersmith
Creek, Altamaha River Georgia, USA. Black dot
indicates the location of the study marsh.
milacea at the nearby Savannah River peaked in
October. Within each plot, a 0.25 m2 subplot
was established, and the number and height of
leaves in each subplot was measured. A polynomial allometric equation (mass 5 20.006(height) +
0.0002(height)2; r2 5 0.91) was used to convert leaf
heights to mass. The regression was developed by
harvesting 509 Z. miliacea leaves outside of, but in
close proximity, to the treatment plots, and measuring height and dry biomass of each leaf.
Five leaves of Z. miliacea of average height were
randomly selected from each plot for N and P
analysis. Leaves were oven-dried at 70uC and
ground using a Wiley Mill. Carbon and N were
determined on oven-dried (70uC) subsamples using
the Perkin-Elmer 2400 CHN analyzer. P was
determined colorimetrically following digestion in
HNO3 - HClO4 digests (Sommer and Nelson 1972).
Recovery of N and P in NIST standards (1515 apple
leaves (N), 1575a pine needles (P)) was 97.7% for N
and 85% P (P standard n 5 10, N standard n 5 24).
Benthic invertebrate densities were measured in
year 2 of the experiment. Two soil cores, 3.7 cm
diameter by 5 cm deep, were collected from each
plot in May and August 2006. Samples were preserved and stained with a mixture of Rose Bengal
198
WETLANDS, Volume 29, No. 1, 2009
dye in 5% solution of formalin in the field (Mason et
at. 1967, Findlay et al. 1989). In the laboratory the
cores were washed through a 250 mm mesh sieve,
and organisms remaining on the screen were sorted
and identified to order or family using keys in Pratt
(1948), Brinkhurst and Jamieson (1971), and Engemann and Hegner (1981), and a reference
collection created by David Lenat (North Carolina
Division of Environmental Management, Water
Quality Section).
Repeated measures analysis of variance (ANOVA) based on treatment and year was used to test
the effect of nutrient additions on leaf height,
number of leaves, and aboveground biomass.
ANOVA based on treatment and year was used to
test the effect of nutrient additions on leaf N and P
(SAS 2002). Two-way ANOVA was also used to test
for the effects on nutrient additions on benthic
invertebrate total density, diversity, and density of
specific taxa across treatments and sampling dates
(SAS 2002). Benthic invertebrate populations were
log10(X+1) transformed to improve normality and
homogeneity of variances. Means were separated
using the Ryan-Einot-Gabriel-Welsch multiple
range test (SAS 2002). All tests of significance were
made at a 5 0.05.
RESULTS
Emergent Vegetation
Aboveground biomass was significantly greater in
the N and N+P treatments relative to the control
and P treatments, but only after the second year of
nutrient additions (Figure 2a). Greater aboveground
biomass was attributed to both greater numbers of
leaves (N+P treatment only) (Figure 2b) and taller
leaves (N, N + P treatments) (Figure 2c). Although
aboveground biomass was not measured in the
treatment plots prior to nutrient additions, control
plot aboveground biomass averaged 992 g m22 and
886 g m22 in year 1 and 2 of the study. These values
are consistent with average aboveground biomass
destructively measured outside the plots (941 g m22,
n 5 9) to develop the allometric equation. Leaf N
and P also responded to nutrient additions, but not
in the same manner as aboveground biomass
(Figure 3a,b). After one year, leaves collected from
plots receiving P (P, N + P) contained less N than
the control treatment (Figure 3a). After two years,
leaves in the N treatment contained less N relative to
the P only treatment (Figure 3a). P content of green
leaves also differed among treatments as, after two
years, leaf P was significantly less in the N treatment
than in the other three treatments (Figure 3b).
Leaf C:N:P also varied in response to nutrient
additions. After one year, leaf N:P was significantly
less in plots receiving P additions (P, N + P
treatments) (Figure 4a) and it was attributed to
higher leaf P concentrations (Figure 3b). Following
the second year, N:P was lower in the leaves
collected from the P only treatment relative to the
other treatments. N:P ratios were significantly
greater in year 2, and this was attributed to lower
leaf P in the plots relative to year 1 (Figure 4a).
During year one, leaf C:N was significantly greater
in the P treatment, as compared to the control, N,
and N + P treatments. After the second year of
nutrient additions, plots receiving N had higher C:N
than control and P plots (Figure 4b).
After two years of nutrient additions, only 7% (N
treatment) to 11% (N + P treatment) of the N
applied and only 1% (P plot) and 6% (N + P plot) of
the P applied after two years of nutrient additions
could be accounted for in aboveground biomass.
Benthic Invertebrates
After two years, total density of benthic invertebrates was significantly greater in the N + P plots
than in the other three treatments during both May
and August sampling events (Figure 5a). Oligochaeta densities also were significantly greater in the
N + P treatments compared to the N, P, and control
treatments (Table 1). Within the order Oligochaeta,
densities of the families, Tubificidae and Lumbriculidae were greatest in the N + P treatment, although
not significantly so (Table 1). In contrast, there was
no difference among treatments in invertebrate
taxon richness (Figure 5b). Overall, infauna densities were significantly greater during May (73,135
individuals m22) than August (10,522 individuals
m22), and taxon richness also was greater in May
(4.5 taxa per 10.75 cm2 core) than August (3.7 taxa
per 10.75 cm2 core).
DISCUSSION
Our two year study suggests that N limits primary
production of tidal freshwater marshes of Georgia.
In tidal freshwater marshes in other portions of the
US Atlantic Coast, results are equivocal. In a Maine
tidal oligohaline high marsh dominated by Spartina
patens, Juncus gerardii, and Juncus balticus, Crain
(2007) found that the plant community was colimited by N + P after one year of N (NH4NO3) and
P (superphosphate) additions. Their findings were
based, like ours, on plant growth response and not
differences in N:P ratios. Morse et al. (2004)
fertilized a tidal freshwater marsh in Virginia, but
Frost et al., NUTRIENT ENRICHMENT OF TIDAL FRESHWATER MARSHES
199
Figure 3. A) Nitrogen and B) phosphorus of green
leaves of Zizaniopsis miliacea (Giant Cutgrass) in response
to N, P, and N+P additions. Means separated by the same
letter are not significantly different (p . 0.05) according to
the Ryan-Einot-Gabriel-Welsch Multiple Range test.
Figure 2. A) Mean aboveground biomass (g m22), B)
leaves m22), and C) leaf height (cm) in response to N, P,
and N+P during years 1 and 2 of nutrient additions.
Samples were collected non-destructively within 0.25 m2
subplots of treatment plots. Means indicated by the same
letter are not significantly different (p . 0.05; Ryan-EinotGabriel-Welsch Multiple Range test).
found no significant differences in either above
ground peak biomass or soil nutrient availability
after one year of N, P, or N + P nutrient additions.
Our findings are consistent with studies in salt
marshes where N additions typically stimulate
primary production (Sullivan and Daiber 1974,
Valiela and Teal 1974, Leendertse 1995, Jefferies
and Perkins 1997, Kiehl et al. 1997).
We observed a significant growth response to N
only after the second year of nutrient additions.
Other nutrient addition studies report increased
biomass production in the second year of the
fertilization but not the first (Craft et al. 1995,
Kiehl et al. 1997); perhaps a lag exists between initial
application and response. However, Crain (2007)
found that aboveground biomass increased by 50%
and 75% in the N and N + P treatments after only
one year of addition, with plant biomass increasing
200
Figure 4. A) N:P ratio and B) C:N ratio of Zizaniopsis
miliacea (Giant Cutgrass) in response to N, P, and N+P
additions. Means separated by the same letter are not
significantly different (p . 0.05) according to the RyanEinot-Gabriel-Welsch Multiple Range test.
even more in year 2 (100%) and year 3 (300%). We
cannot eliminate the possibility that the lack of
response in year 1 of our study was a design artifact.
In year 1, N was added as NH4Cl, and because this
formulation is water soluble, much of it dissolved
and probably was carried away by tidal and river
flushing. In year 2, we added N in a time release
formulation, which presumably remained in the
plots longer and perhaps, elicited a stronger
response. Our sample size (n 5 4 plots per
treatment) might have also been too small to detect
change in the first year; that year aboveground
biomass was greater, but not significantly, in the N
and N+P treatments relative to the control and P
treatments (Figure 2a).
After two years of nutrient additions, plots
receiving N only exhibited a large decrease in
percent leaf N (Figure 3a) and an increase in leaf
C:N (Figure 4b). The concentration of P in leaves
WETLANDS, Volume 29, No. 1, 2009
Figure 5. A) Benthic invertebrate density and B)
invertebrate taxa richness in May and August in response
to N, P, and N + P additions. Abundance data were
log10(X+1) transformed. Means separated by the same
letter are not significantly different (p . 0.05; Ryan-EinotGabriel-Welsch Multiple Range test).
also decreased in the N only plots (Figure 3b). The
reduction in both N and P concentrations in the
leaves was likely due to dilution caused by the large
increase in plant growth and aboveground biomass
(Broome et al 1983, Dai and Wiegert 1997).
Additions of N + P to a S. alterniflora marsh in
North Carolina, USA yielded results similar to our
study; aboveground biomass and leaf C:N increased
whereas leaf N decreased (Broome et al 1975).
Likewise, additions of N to short form S. alterniflora
resulted in dilution of leaf N as a result of leaf area
expansion (Dai and Wiegert 1997). These researchers concluded that expanding the leaf area provides
more efficient N use and also reduced insect
herbivory due to decreased palatability (Dai and
Wiegert 1997). However, other studies where S.
alterniflora is fertilized with N only have shown that
N concentrations of marsh emergent vegetation
increase (Valiela and Teal 1974, Broome et al
1975, and Gallagher 1975).
Re-translocation of N to roots and leaching from
leaves may have had some effect on N concentra-
Frost et al., NUTRIENT ENRICHMENT OF TIDAL FRESHWATER MARSHES
201
Table 1. Taxa identified, and mean densities (individuals m22) of invertebrates present in control (C), P, N, and N + P
treatment plots. Only Oligochaeta densities in May differed significantly among treatments, and means indicated by the
same letter are not significantly different (p . 0.05; Ryan-Einot-Gabriel-Welsch Multiple Range test).
May
Taxon
Turbellaria
Nematoda
Polychaeta
Oligochaeta
Lumbriculidae
Enchytraeidae
Tubificidae
Naididae
Gastropoda
Collembola
Amphipoda
Diptera
C
0
3140
120
15930 a
9070
120
6280
470
470
1160
230
1160
P
0
3020
120
28490 a,b
13950
120
14190
230
0
470
0
580
August
N
0
1980
230
25580 a,b
12330
580
11740
930
0
1050
0
580
tions in our Z. miliacea leaves. Hopkinson (1992)
estimated that in Altamaha River marshes 10.1 g N
m22 yr21 was retranslocated by Z. miliacea to
belowground stocks following senescence. Green
and senesced leaves were estimated to leach 6.5 and
7.4 g N m22 yr21, respectfully. Although we did not
sample senesced leaves, some retranslocation of N to
the roots and leaching probably occurred and was
not accounted for in our study.
Nitrogen:phosphorus ratios have been used to
infer N versus P limitation and Koerselman and
Meuleman (1996) suggested that when N:P ratios
are , 30 (mol:mol), N limits plant growth, between
30–35, N and P co-limit growth, and . 35 P limits
plant growth. During both years of nutrient
additions, N:P of leaves collected from all treatments was , 30 (14–27), suggesting N limitation of
plant productivity, which supports our observations
of a growth response to N additions. Morse et al.
(2004) measured N:P ratios , 30 (mol:mol) in
accumulating sediments (N:P 4–38), surface soils
(N:P 5–26), and above ground plant tissue (12–26)
of tidal freshwater marshes in Virginia, also
suggesting that their tidal freshwater marshes may
be N limited.
We measured greater total densities of benthic
invertebrates (Figure 5a) and oligochaetes (Table 1)
in N+P plots suggesting that both N and P limit
secondary production in tidal freshwater marshes. A
sludge-based fertilization study conducted in a tidal
salt marsh creek also found that oligochaetes
showed the greatest response to fertilizer additions
in plots treated with N+P, compared to plots
receiving C, N, and P (Sarda et al. 1992). In salt
marsh, Sundareshwar et al (2003) reported that
N+P
230
3840
120
66050 b
26740
120
38840
350
230
810
120
120
C
P
N
N+P
0
1163
233
4070
2326
116
1511
116
0
581
698
0
0
1512
698
6395
3953
116
2209
116
116
1163
465
349
0
1628
233
4419
1860
116
2326
116
0
349
233
116
0
1279
465
13023
5581
0
7209
116
0
1744
1047
116
microbial production is limited by P and plant
production is limited by N. Invertebrate response in
our study could result from larger populations of
microbes supported by P additions and greater
quantities of plant detritus produced by N additions.
CONCLUSION
Our study is the first to experimentally document
N limitation of tidal freshwater marsh vegetation. It
is also the first to examine benthic invertebrate
response to nutrient additions in a tidal freshwater
marsh. Changes in N sources after year 1, and
limited sampling events of both primary and
secondary producers limited some of the conclusions
that can be made. Our results indicate that primary
production of Zizaniopsis miliacea dominated
marshes in Georgia are limited by N based on
increases in leaf height, number of leaves, and
aboveground biomass in response to N and N + P
additions. Secondary production, as indicated by
benthic invertebrate densities, may be co-limited by
N + P in these marshes. Our findings suggest that,
like salt marshes and estuaries, tidal freshwater
marshes can be N limited and thus, may be
susceptible to N enrichment and eutrophication.
ACKNOWLEDGMENTS
Thanks to Mark Loomis, Jon Shelby, and Kristen
Wardlaw for preparation and processing of vegetative samples and invertebrate sieving. Also, thanks
to David Lenat for preparation of a reference
invertebrate collection and additional information
on invertebrates. This research was supported by
202
WETLANDS, Volume 29, No. 1, 2009
grant OCE-9982133 from the National Science
Foundation to the Georgia Coastal Ecosystem
LTER program and grant RD 83222001-0 from
the U.S. Environmental Protection Agency Science
to Achieve Results (STAR) program. This is
Contribution 966 of the University of Georgia
Marine Institute.
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Manuscript received 4 May 2007; accepted 1 September 2008.