Download Decomposition of Leaf Litter in a U.S. Saltmarsh is Driven by

Decomposition of Leaf Litter in a U.S.
Saltmarsh is Driven by Dominant Species,
Not Species Complementarity
Malte Treplin, Steven C. Pennings &
Martin Zimmer
Wetlands
Official Scholarly Journal of the Society
of Wetland Scientists
ISSN 0277-5212
Volume 33
Number 1
Wetlands (2013) 33:83-89
DOI 10.1007/s13157-012-0353-1
1 23
Your article is protected by copyright and
all rights are held exclusively by Society
of Wetland Scientists. This e-offprint is for
personal use only and shall not be selfarchived in electronic repositories. If you
wish to self-archive your work, please use the
accepted author’s version for posting to your
own website or your institution’s repository.
You may further deposit the accepted author’s
version on a funder’s repository at a funder’s
request, provided it is not made publicly
available until 12 months after publication.
1 23
Author's personal copy
Wetlands (2013) 33:83–89
DOI 10.1007/s13157-012-0353-1
ARTICLE
Decomposition of Leaf Litter in a U.S. Saltmarsh
is Driven by Dominant Species, Not Species
Complementarity
Malte Treplin & Steven C. Pennings & Martin Zimmer
Received: 3 July 2012 / Accepted: 6 November 2012 / Published online: 14 November 2012
# Society of Wetland Scientists 2012
Abstract To add to our understanding of species richnesseffects on ecosystem processes, we studied the importance
of species complementarity in driving decomposition in a
saltmarsh in Georgia, USA. We studied pair-wise interactions of both detritivores and plant litter species and how
they affect decomposition rates in an experiment located on
the mid-marsh platform. Needle rush, Juncus roemerianus, had 2-3 times higher decomposition rates than
cordgrass, Spartina alterniflora, or live oak, Quercus
virginiana. Mixing litter types did not promote decomposition rates. Cordgrass decomposition was 1.5-times
higher when periwinkles, Littoraria irrorata, were present than in detritivore-free controls. In contrast, neither
coffee-bean snails, Melampus bidentatus, nor wharf
crabs, Armases cinereum, increased cordgrass decomposition rates. Mixing detritivore species did not increase
cordgrass mass loss beyond expected rates from an
additive model. We conclude that in this system, species
do not act complementarily with each other, but that
decomposition rates are controlled by the dominant species of angiosperms and invertebrate detritivores.
M. Treplin : M. Zimmer
Zoologisches Institut, Christian-Albrechts-Universität,
Am Botanischen Garten 9,
24118 Kiel, Germany
S. C. Pennings
Department of Biology and Biochemistry, University of Houston,
Houston, TX 77204-5001, USA
Present Address:
M. Zimmer (*)
Paris-Lodron-Universität Salzburg, FB Organismische Biologie,
AG Ökologie, Biodiversität & Evolution der Tiere,
Hellbrunner Str. 34,
5020 Salzburg, Austria
e-mail: [email protected]
Keywords Decomposition . Detritivores . Saltmarsh .
Species identity . Species richness . Species interaction
Introduction
Ecologists are increasingly interested in whether and how
species richness mediates ecological processes. Observed
positive effects of species richness have been related to (1)
"complementarity" (Naeem et al. 1994; Tilman et al. 1996;
Loreau 1998) or (2) "sampling" (Aarssen 1997; Huston
1997; Tilman et al. 1997; c.f. "selection/dominance effects"
in Loreau and Hector 2001; Fox 2005). Complementarity is
based on species-specific resource use or positive interspecific interactions (facilitation), resulting in higher performance (synergism) at the community level than expected
from performance of single species. Alternatively, according
to the sampling effect, the probability of including a particularly well-performing species will increase with species
richness. Hence, performance at the community level will
equal that of the best performing single species. The selection effect (Loreau and Hector 2001) or dominance effect
(Fox 2005) in addition takes into account the relative abundance of species in mixtures (Hector et al. 1999). In speciespoor systems, where there is little scope for the selection
effect to operate, the most likely mechanism that could
produce positive effects of species richness is complementary interactions between species.
Saltmarshes along the Atlantic US coast are relatively
poor in species richness of vascular plants and macroinvertebrates, being dominated by only few abundant species. In Georgia saltmarshes, for example, plant biomass is
dominated by the grass Spartina alterniflora (Wiegert and
Freeman 1990), and decomposition of S. alterniflora is
thought to be driven by interactions between fungi and a
single abundant snail species, Littoraria irrorata (Silliman
Author's personal copy
84
and Newell 2003). Although other plant and detritivore species
occur, their roles in ecosystem processes, and the potential
synergies between species, have been less studied. Although
nutrient cycles in intertidal saltmarshes are primarily detritusbased (Teal 1962; Nixon and Oviatt 1973; Valiela and Teal
1979), they are also naturally poor in species of the detritivorous macro-fauna. The decomposition of detrital matter, being
the result of complex interactions of detritivores and microbes,
serves in both (1) transferring energy to higher trophic levels
within the marsh, and (2) exporting energy to adjacent habitats.
Decomposition rates vary with the identity of both the detrital
source (Cornelissen 1996; Wardle et al. 1997) and the detritivores feeding on the litter, be it leaf litter of terrestrial origin
(Hättenschwiler and Gasser 2005; Zimmer et al. 2005; Treplin
and Zimmer 2012), seagrass (Moore and Fairweather 2006), or
macroalgal detritus (Godbold et al. 2009). Further, individual
species effects may be independent of other species (i.e.,
additivity), or emergent effects of species (i.e. non-additivity)
may occur in mixed-species combinations (c.f., Kominoski et
al. 2007; Ball et al. 2008), corroborating the complementarity
of species.
Saltmarsh detritivores are not redundant, but contribute
species-specifically to decomposition processes (Zimmer et
al. 2002, 2004). Because the different detritivores affect decomposition in different ways, it is reasonable to hypothesize
that mixtures of detritivores might out-perform any one species by functioning in a complementary manner. It remains,
however, unknown how co-existing saltmarsh detritivores
interact. Are their species-specific contributions complementary, resulting in non-additive (synergistic) enhancement of
decomposition? To answer this question, we studied how
single-species treatments differed from species mixtures in
terms of litter mass loss (as a proxy of decomposition processes) in field mesocosms. As a base line, we chose decomposition of the most common saltmarsh plant, the cordgrass
Spartina alterniflora (Pennings et al. 2001), through the action of the most common saltmarsh consumer, the periwinkle
Littoraria irrorata (Bärlocher and Newell 1994). By experimentally varying both species richness and identity of both
detritus and detritivores, we examined effects of both resources and consumers within the same system. More explicitly,
we tested for complementarity, hypothesizing that mixtures of
litter species would decompose faster than any single litter
through the combination of species-specific litter traits, and
that mixing detritivore species pair-wise would also increase
litter decomposition rates through the complementarity of
interacting functional traits.
Methods
The experiment was conducted in a saltmarsh habitat at
Sapelo Island (31.39° N, 81.29° W), GA, USA. The
Wetlands (2013) 33:83–89
experimental field site was located at Dean’s Creek, on the
south end of Sapelo Island (site GCE6 of the Georgia Coastal
Ecosystems Long-Term Experimental Research program:
http://gce-lter.marsci.uga.edu/public/app/studysites.asp). Experimental cages were constructed of a strip of plastic garden
edging, a 1.5 m PVC pipe, and fiberglass window screen
mesh. The plastic edging was formed into a ring of 35 cm
diameter and 10 cm height. The screen was sewed into a tube
that was looped around the plastic ring at the bottom to
prevent animals from entering or leaving the cage. The ring
was completely sunk into the soil, securing the bottom of the
mesh. In the center of the ring, the plastic pipe was inserted
into the soil 80 cm deep and the net was tied above the top of
the pipe with a cable tie to form a tent-like cage 70 cm in
height. Cages were placed on the marsh platform, at intermediate elevations within the saltmarsh.
We studied litter from three plants that commonly contribute to litter input at the field site (c.f., Zimmer et al.
2004), namely the cordgrass Spartina alterniflora Loisel,
the needle rush Juncus roemerianus Scheele, and live oak
Quercus virginiana Miller. Litter that showed little decay
upon visual inspection was handpicked from plant stands in
the adjacent area, air-dried and weighed. Litter was offered
as food to detritivores in single-species treatments (3 treatments) and all possible two-species combinations (3 treatments). We placed 20 g (dry weight) of litter in each cage
(either 20 g of one species, or 10 g each of two species).
Detritivores were collected from the local area, and kept
in the lab until used in the experiment. We studied the most
abundant detritivores (Buck et al. 2003; Zimmer et al. 2004)
at the field site (two snails and a decapod crab): the periwinkle Littoraria irrorata Say, the coffee bean snail Melampus bidentatus Say, and the omnivorous wharf crab
Armases cinereum Bosc. Another abundant detritivore, the
amphipod Orchestia grillus, was not included because of
high risk of mortality in captivity (authors' unpubl. obs.) and
because it is a preferred prey for the wharf crab (Buck et al.
2003). Detritivorous terrestrial isopods (Littorophiloscia vittata; Porcellionides virgatus; Venezillo parvus), occur at
higher tidal elevations than the intertidal elevation studied
here and were thus not included. We did not experimentally
manipulate the microbial decomposer community, which
consists of a mixture of fungi and bacteria (Osono and
Takeda 2002; Silliman and Newell 2003; Buchan et al.
2003), but instead allowed microbial communities to develop based on the litter and detritivore treatments. A ratio of
fresh weight to soft body water content was determined for
each detritivore species through weighing and oven-drying
(60 °C) to constant dry mass. Animal biomass was equalized according to these ratios based on the average density
of L. irrorata at Dean’s creek of ~90 snails per m2. Soft
body dry mass of 9 medium-sized L. irrorata equalled that
of 45 medium-sized M. bidentata, or 2 medium-sized A.
Author's personal copy
Wetlands (2013) 33:83–89
comparison to the weighted average of single-species effects
("expected" detritivore effects) that had also been corrected for
random-paired control values. Using the same approach, we
compared litter-mixture treatments ("observed") with the
weighted averages of single-litter treatments ("expected").
This process was done independently for detritivore-free controls, crab-, snail- and two-species treatments. Following
Wardle et al. (2006), the "expected" values were calculated by
weighting litter-specific mass loss with respect to the species
composition of the litter mixture at the end of the experiment.
Expected and observed values were compared using t tests
after ln- or square root-transformation as appropriate (c.f.
Zimmer et al. 2005; Treplin and Zimmer 2012).
Results
Decomposition rates of Juncus (needle rush) were 2-3 times
higher than those of Spartina (cordgrass) and Quercus (live
oak) (Fig. 1). Adding slowly-decomposing detritus (Spartina
or Quercus) to Juncus did not reduce its decomposition rate,
nor did adding Juncus detritus to Quercus or Spartina increase
decomposition rates of these species. Effects of mixing detrital
sources on total decomposition rates were exclusively additive
(Fig. 2), resulting in decomposition rates that were intermediate to single-detritus mass loss rates. Thus, we did not find any
effect of increasing litter species richness from one to two
species on litter mass loss, suggesting a lack of complementarity in litter decomposition.
100
total litter mass loss (%)
b
80
b
b
60
a
a
a
40
a
a
a
20
rti
na
(Q
)
ue
rc
us
)
Ju
nc
us
pa
s(
S
cu
cu
nc
Ju
Ju
n
un
us
(J
rc
us
s)
)
na
us
rti
rc
rc
Q
ue
Q
ue
us
(S
pa
cu
s)
Q
ue
us
)
rc
(J
un
na
rti
Q
ue
Sp
a
ar
tin
a(
Sp
ar
tin
a
0
Sp
cinereum. Total detritivore biomass was kept constant across
all treatments, resulting in experimental densities of detritivores (450 Melampus or 20 Armases per m2) that were
within the range of values observed in the field but higher
than the average (100 Melampus or 10 Armases per m2: c.f.,
Zimmer et al. 2004).
To study potential pair-wise complementary effects of increasing litter species richness, we compared decomposition of
the three litter types alone with all three possible 2-species
combinations of litter types in the presence of the most abundant detritivore, Littoraria irrorata (total of six litter treatments;
N07, each). To study potential pair-wise interactions of detritivore species, we compared decomposition of the dominant
saltmarsh plant, Spartina alterniflora, in the presence of no
detritivores (detritivore-free control), of all three detritivore
species in single-species treatments, and of all three possible
2-species combinations of detritivores (total of seven detritivore
treatments; N07, each). Hence, we installed a total of 13
(treatments) x 7 (replicates)0105 tents.
Experimental tents were placed on the marsh platform in a
stand of the perennial succulent, Batis maritima (Bataceae),
2.1±0.05 m above mean low water level (levelled with a
theodolite). All vegetation under the cages was removed by
clipping, and cages were haphazardly placed 50 cm apart in a
rectangular area. Cages were stocked with leaf litter and
detritivores in June 2006 and remained in the field for
3 months. During this time of high detritivore activity, daily
mean air temperature ranged from 23.5 °C to 30.5 °C. Except
for a heavy rain event on June 13, there was less than 10 mm
precipitation until August 12, with a total of ca 80 mm between August 12 and 30 (http://gce-lter.marsci.uga.edu; data
set ID marshlanding_daily_jan06-dec06). During the experiment, the site was inundated about 50 times, with a maximum
tide level of 45 cm above the soil level. Tides within the study
area are semi-diurnal with a tidal range that can vary from
1.5 m during neap tide to 3.0 m during spring tide. The tide
propagating into the saltmarshes becomes increasingly distorted because of frictional dissipation of energy in the shallow channels and intertidal marsh areas, leading to ebb tidal
currents that are stronger than flood tidal currents (Blanton et
al. 2002).
After 3 months, cages were sampled for litter mass: residual litter was sorted to species, cleaned of deposited sediments
and oven-dried to constant weight to obtain total dry weight.
Due to strong weather and the dynamic tidal regime, some
cages were destroyed or animals were missing. These cages
were not included in the analyses, and the number of replicates
was reduced to 5 in two treatments and 4 in one treatment.
Other than that, all detritivores survived the experiment.
For statistical analysis, we essentially followed Loreau
and Hector (2001). First, we tested effects of two-species
treatments, corrected for detritivore-free control values
through random-pairing ("observed" detritivore effects), in
85
Fig. 1 Percent litter mass loss of different detrital types in singlespecies treatments (Spartina, Quercus, Juncus) and in combination
with each other [(Quercus): in combination with Quercus, (Juncus):
in combination with Juncus, (Spartina): in combination with Spartina]
in the presence of Littoraria. Whisker-Box-Plots indicate minimum,
1st quartile, median, 3rd quartile, and maximum (N07); different
lower-case letters indicate significant differences (ANOVA; post hoc
pairwise comparison through Tukey’s multiple comparison; α00.05).
Author's personal copy
86
Wetlands (2013) 33:83–89
ns
total litter mass loss (%)
60
ns
50
free control, although their densities in the mesocosms were
higher than on average in the field. Joint effects of detritivores in mixtures were exclusively additive (Fig. 4). We
found no effects on litter mass loss of increasing detritivore
species richness from one to two species, indicating that
interactions among these species pairs showed no evidence
of complementarity.
40
ns
30
20
10
ex
pe
ct
ed
(S
ob
pa
se
rti
rv
na
ed
+Q
(S
pa
ue
ex
rti
rc
pe
na
us
ct
+Q
)
ed
ue
(S
ob
rc
pa
se
us
rti
rv
)
na
ed
+J
(S
ex
un
pa
pe
cu
rti
na
ct
s)
ed
+J
(Q
ob
un
ue
se
cu
rc
rv
s)
us
ed
+J
(Q
un
ue
cu
rc
us
s)
+J
un
cu
s)
0
Fig. 2 Effects of litter-mixing on decomposition (percent litter mass
lost). Observed decomposition rates were compared with expected
rates as described in the Methods. Whisker-Box-Plots indicate minimum, 1st quartile, median, 3rd quartile, and maximum (N07). (ns: not
significant; Wilcoxon matched-pairs signed rank tests; α00.05).
Decomposition of Spartina was 1.5-times higher when
Littoraria was present than in detritivore-free controls
(Fig. 3). In contrast, neither of the other two detritivores
increased Spartina decomposition relative to the detritivore-
b
a
a,b
40
a
a
According to Zimmer et al. (2004), the saltmarsh detritivores studied herein are not redundant, nor are the different
detrital sources used herein. The detritivores differ in feeding mode and impact on mass loss, and the litter types differ
in chemistry and structure. Nevertheless, neither different
litter sources nor different detritivore species interacted in a
complementary way to enhance detrital mass loss. Although
we cannot rule out the possibility that including other species would have led to different results, we found no evidence for complementarity in the interactions between the
species that we did study. Instead, results were purely additive, driven by the individual effects of the species studied.
Whether and how species richness affects decomposition
processes has been a topic of some controversy for a number
of years. In some cases, species identity rather than species
richness drives ecosystem processes (e.g., Vivanco and
Austin 2008; McLaren and Turkington 2010; but see Gessner
et al. 2010 for a recent, nuanced, review). The detritus types
60
total litter mass loss (%)
a,b
a
30
20
10
50
ns
ns
ns
40
30
20
10
s)
pu
el
+M
es
ob
se
ct
rv
ed
(A
rm
as
es
as
rm
(A
ed
am
pu
am
el
+M
+M
ia
ar
or
pe
s)
s)
pu
s)
el
am
am
pu
es
itt
(L
ed
rv
ob
se
ct
pe
ex
el
+M
ia
ar
or
itt
(L
ed
ed
rv
se
rm
as
ia
ar
or
itt
(L
itt
(L
ed
ct
ob
pe
ex
+A
rm
+A
ia
ar
or
+
as
es
Fig. 3 Percent mass loss of Spartina litter in detritivore-free controls and
in the presence of detritivores in single-species treatments (Littoraria,
Armases, Melampus) and in combinations. Whisker-Box-Plots indicate
minimum, 1st quartile, median, 3rd quartile, and maximum (N07);
detritivore treatments were pairwise compared to the control C to test
for detritivore effects on litter mass loss; combinations of detritivores
were compared to single-detritivore assays to test for diversity effects;
different lower-case letters indicate significant differences (α00.05).
as
es
s
pu
am
pu
el
M
el
am
as
ria
m
Ar
ra
Li
tto
Li
tto
ra
ria
+
+
M
Ar
m
am
el
M
s
es
s
pu
es
as
m
Ar
ra
tto
Li
co
n
tro
l
ria
)
)
0
0
ex
total litter mass loss (%)
50
Discussion
Fig. 4 Effects of detritivore-mixing on decomposition (percent
litter mass lost). Observed decomposition rates were compared
with expected rates as described in the Methods. Whisker-BoxPlots indicate minimum, 1st quartile, median, 3rd quartile, and
maximum (N 07). (ns: not significant; Wilcoxon matched-pairs
signed rank tests; α00.05)
Author's personal copy
Wetlands (2013) 33:83–89
we used herein differ significantly in terms of chemistry and
structure (c.f., Pennings et al. 1998; Zimmer et al. 2002,
2004), creating the potential for complementarity, since detritivores might improve their nutrition or minimize exposure to
particular defenses by feeding on mixtures of the two species.
Due to structural and chemical differences, detrital sources of
different origins differed in decomposition rate. In particular,
litter from Quercus and Spartina lost only 30 and 50 % as
much dry mass, respectively, as litter from Juncus lost during
the three-month experiment. Hence, in the upper saltmarsh,
where detritus of all three plants is common, Juncus will
contribute most rapidly to organic matter turnover and nutrient
cycling. Not surprisingly, it is common to see mats of Spartina
or Quercus litter in the marsh, but rare to see mats of Juncus
litter (authors' unpubl. obs.). Mixing live oak or cordgrass
detritus with needle rush detritus reduced the overall rate of
detrital mass loss, but not more so than would have been
expected from averaging mass loss rates (additive effects).
In sum, we found no evidence for complementarity of detrital
sources in this detritus-based system.
The detritivores we used herein differ significantly in
terms of feeding mode (c.f., Zimmer et al. 2004) and their
impact on litter mass loss, providing the potential for complementarity through interactions (c.f., Zimmer et al. 2005;
Treplin and Zimmer 2012), if one species processed litter in
ways that made it more palatable for the other species, as has
been suggested for Melampus, Littoraria and Armases by
Ewers et al. (2012). Whereas wharf crabs and coffee-bean
snails hardly affected mass loss of Spartina litter, the periwinkle Littoraria increased Spartina mass loss rates by
more than 50 %. Extrapolating this feeding rate results in
about 352 g Spartina detritus being consumed per m2 per
year (similar to the estimate of 500 gm2 a-1 in lab studies by
Zimmer et al. 2004). Mixing this efficient detritivore with
either Armases or Melampus slightly reduced the overall
rate of decomposition (but not significantly so: LA vs L:
p00.07; LM vs L: p00.29), thus reducing (c.f., Creed et al.
2009) an important ecosystem process, but to a rate no
slower than would be expected from averaging singlespecies mass loss rates (additive effects). In sum, we found
no evidence for complementary effects of detritivores in this
detritus-based system.
Based on these two negative results, we conclude that, in
Southeastern US saltmarshes, the overall rate of decomposition of dominant marsh plants is driven by the dominant
detritivore (in this case Littoraria). If additional species are
rare and/or ineffective, adding more species to the system
will only marginally add to the effectiveness of single ecosystem processes. Notwithstanding, these additional species
may significantly contribute in other ways to overall ecosystem functioning. For example, although Armases only
weakly contributed to detrital mass loss in this study, it plays
an important ecological role as a mediator of energy fluxes
87
between trophic levels and along the marine-terrestrial ecotone (Buck et al. 2003; Zimmer et al. 2004), a habitat where
Littoraria is essentially absent. Similarly, Melampus significantly promotes microbial activity on decaying saltmarsh
detritus, whereas the other detritivores do not (Zimmer et al.
2004; authors' unpubl. obs.). Melampus is negatively affected
by Littoraria (Lee and Silliman 2006), and Melampus is more
abundant at sites where Littoraria is rare (McFarlin et al.
2008). Hence, Melampus may play a larger role in decomposition processes in the absence of Littoraria than when this
superior competitor (c.f, Lee and Silliman 2006) is
present (as herein).
An important caveat to our results is that we cannot
exclude the possibility that we might have observed complementarity had we combined all three studied species.
Also, we did we not include Orchestia grillus in our study.
This amphipod is sometimes abundant (especially in the
upper marsh: Kneib 1984) and, together with another amphipod Uhlorchestia spartinophila (Graça et al. 2000), potentially contributes to the decomposition of saltmarsh litter.
Our experimental design, using closed cages, did not allow
for including these amphipods, because Armases readily
preys on amphipods (Buck et al. 2003), and would soon
have eliminated all individuals inside the cages. Similarly,
terrestrial isopods were not included because they are essentially lacking from the intertidal elevations studied, but
these may be important at high marsh elevations. Thus, it is
possible that we might have observed complementary
effects had we included other species combinations in the
study design.
According to Dangles and Malmqvist (2004), a species
with a strong ecosystem effect must occur at high densities
year-round, be highly motile, and be engaged in strong
interspecific interactions. Littoraria is highly abundant
throughout the saltmarsh except immediately adjacent to
creekbanks (Teal 1962; Fell et al. 1991; Bärlocher and
Newell 1994; Zimmer et al. 2004) and is present at all
seasons, although dormant in winter (Vaughn and Fisher
1992). Its seasonal range of activity, however, appears to
be no more than a circle of 2 m in diameter (Vaughn and
Fisher 1992). A strong regulating impact of Littoraria on
Spartina production has been shown (Silliman and Zieman
2001), and Littoraria is competitively superior to Melampus
and has the ability to displace the smaller snail (Lee and
Silliman 2006). Thus, despite its limited motility, Littoraria
appears to be a major player in Atlantic saltmarshes along
the U.S. East Coast that interacts with other detritivores
(Silliman and Newell 2003; Ewers et al. 2012) but, as we
have shown here, does not act complementarily with them.
Acknowledgements We are grateful to Sebastian Fraune, The Lord
of the Rings, for his invaluable help in setting-up this field study under
adverse conditions. This work is a contribution of the Georgia Coastal
Author's personal copy
88
Ecosystems Long-Term Ecological Research program (OCE99-82133,
OCE06-20959), and is contribution number ... of the University of
Georgia Marine Institute.
References
Aarssen LW (1997) High productivity in grassland ecosystems:
Effected by species diversity or productive species? Oikos
80:183–184
Bärlocher F, Newell SY (1994) Growth of the salt-marsh Periwinkle
Littoraria irrorata on fungal and cordgrass diets. Marine Biology
118:109–114
Ball BA, Hunter MD, Kominoski JS, Swan CM, Bradford MA (2008)
Consequences of non-random species loss on decomposition dynamics: Evidence for additive and non-additive effects. Journal of
Ecology 96:303–313
Blanton J, Lin G, Elston S (2002) Tidal current asymmetry in shallow
estuaries and tidal creeks. Continental Shelf Research 22:1731–
1743
Buchan A, Newell SY, Butler M, Biers EJ, Hollibaugh JT, Moran MA
(2003) Dynamics of bacterial and fungal communities on decaying salt marsh grass. Applied and Environmental Microbiology
69:6676–6687
Buck TL, Breed GA, Pennings SC, Chase ME, Zimmer M, Carefoot
TH (2003) Diet choice in an omnivorous salt-marsh crab: different food types, body size, and habitat complexity. Journal of
Experimental Marine Biology and Ecology 292:103–116
Cornelissen JHC (1996) An experimental comparison of leaf decomposition rates in a wide range of temperate plant species and
types. Journal of Ecology 84:573–582
Creed RP, Cherry RP, Pflaum JR, Wood CJ (2009) Dominant species
can produce a negative relationship between species diversity and
ecosystem function. Oikos 118:723–732
Dangles O, Malmqvist B (2004) Species richness-decomposition
relationships depend on species dominance. Ecology Letters
7:395–402
Ewers C, Beiersdorf A, Wieski K, Pennings SC, Zimmer M (2012)
Predator/prey-interactions promote decomposition of low-quality
detritus. Wetlands. doi:10.1007/s13157-012-0326-4
Fell PE et al (1991) Reestablishment of Melampus bidentatus (Say)
and other macroinvertebrates on a restored impounded tidal
marsh - Comparison of populations above and below the
impoundment dike. Journal of Experimental Marine Biology
and Ecology 152:33–48
Fox JW (2005) Interpreting the ‘selection effect’ of biodiversity on
ecosystem function. Ecology Letters 8:846–856
Gessner MO, Swan CM, Dang CK, McKie BG, Bardgett RD, Wall
DH, Hättenschwiler S (2010) Diversity meets decomposition.
Trends in Ecology & Evolution 25:372–380
Godbold JA, Killham K, Solan M (2009) Consumer and resource
diversity effects on macroalgal decomposition. Oikos 118:77–86
Graça MAS, Newell SY, Kneib RT (2000) Grazing rates of organic
matter and living fungal biomass of decaying Spartina alterniflora by three species of salt-marsh invertebrates. Marine Biology
136:281–289
Hättenschwiler S, Gasser P (2005) Soil animals alter plant litter diversity
effects on decomposition. Proceedings of the National Academy of
Sciences USA 102:1519–1524
Hector AB, Schmid C, Beierkuhnlein MC, Caldeira M, Diemer PG,
Dimitrakopoulos JA, Finn H, Freitas PS, Giller J, Good R, Harris
P, Högberg K, Huss-Danell J, Joshi A, Jumpponen C, Körner PW,
Leadley M, Loreau A, Minns CPH, Mulder G, O'Donovan SJ,
Otway JS, Pereira A, Prinz DJ, Read M, Scherer-Lorenzen E-D,
Wetlands (2013) 33:83–89
Schulze A-SD, Siamantziouras EM, Spehn AC, Terry AY, Troumbis
FI, Woodward S, Yachi JH, Lawton (1999) Plant diversity and
productivity experiments in European grasslands. Science
286:1123–1127
Huston MA (1997) Hidden treatments in ecological experiments:
re-evaluating the ecosystem function of biodiversity. Oecologia
110:449–460
Kneib RT (1984) Patterns of invertebrate distribution and abundance in
the intertidal salt marsh: causes and questions. Estuaries 7:392–
412
Kominoski JS, Pringle CM, Ball BA, Bradford MA, Coleman DC, Hall
DB, Hunter MD (2007) Nonadditive effects of leaf litter species
diversity on breakdown dynamics in a detritus-based stream.
Ecology 88:1167–1176
Lee SC, Silliman BR (2006) Competitive displacement of a detritivorous salt marsh snail. Journal of Experimental Marine Biology
and Ecology 339:75–85
Loreau M (1998) Separating sampling and other effects in biodiversity
experiments. Oikos 82:600–602
Loreau M, Hector A (2001) Partitioning selection and complementarity
in biodiversity experiments. Nature 412:72–76
McFarlin CR, Brewer JS, Buck TL, Pennings SC (2008) Impacts of
fertilization on a salt marsh food web in Georgia. Estuaries Coasts
31:313–325
McLaren JR, Turkington R (2010) Plant functional group identity
differentially affects leaf and root decomposition. Global Change
Biology 16:3075–3084
Moore TN, Fairweather PG (2006) Decay of multiple species of
seagrass detritus is dominated by species identity, with an important influence of mixing litters. Oikos 114:329–337
Naeem S, Thompson LJ, Lawler SP, Lawton JH, Woodfin RM (1994)
Declining biodiversity can alter the performance of ecosystems.
Nature 368:734–737
Nixon SW, Oviatt CA (1973) Ecology of a New England salt marsh.
Ecological Monographs 43:463–498
Osono T, Takeda H (2002) Comparison of litter decomposing ability
among diverse fungi in a cool temperate deciduous forest in
Japan. Mycologia 94:421–427
Pennings SC et al (1998) Feeding preferences of a generalist salt-marsh
crab: Relative importance of multiple plant traits. Ecology
79:1968–1979
Pennings SC, Siska E, Bertness MD (2001) Latitudinal variation in the
palatability of marsh plants. Ecology 82:1344–1359
Silliman BR, Newell SY (2003) Fungal farming in a snail. Proceedings of the National Academy of Sciences USA
100:15643–15648
Silliman BR, Zieman JC (2001) Top-down control of Spartina alterniflora
production by periwinkle grazing in a Virginia salt marsh. Ecology
82:2830–2845
Teal JM (1962) Energy flow in the saltmarsh system of Georgia.
Ecology 43:611–624
Tilman D, Wedin D, Knops J (1996) Productivity and sustainability
influenced by biodiversity in grassland ecosystems. Nature
379:718–720
Tilman D, Lehman CL, Thomson KT (1997) Plant diversity and
ecosystem productivity: theoretical considerations. Proceedings
of the National Academy of Sciences 94:1857–1861
Treplin M, Zimmer M (2012) Drowned or dry: a cross-habitat comparison of detrital breakdown processes. Ecosystems 15:477–491
Valiela I, Teal JM (1979) Inputs, outputs and interconversion of nitrogen in a salt marsh ecosystem. In: Jefferies RL, Davy AJ (eds)
Ecological processes in coastal environments. Blackwell Scientific
Publications, Oxford, pp 399–414
Vaughn CC, Fisher FM (1992) Dispersion of the salt-marsh Periwinkle
Littoraria irrorata - effects of water level, size, and season.
Estuaries 15:246–250
Author's personal copy
Wetlands (2013) 33:83–89
Vivanco L, Austin AT (2008) Tree species identity alters forest
litter decomposition through long‐term plant and soil interactions in Patagonia, Argentina. Journal of Ecology 96:727–
736
Wardle DA, Bonner KI, Nicholson KS (1997) Biodiversity and plant
litter: experimental evidence which does not support the view that
enhanced species richness improves ecosystem function. Oikos
79:247–258
Wardle DA, Yeates GW, Barker GM, Bonner KI (2006) The influence
of plant litter diversity on decomposer abundance and diversity.
Soil Biol Biochem 38:1052–1062
89
Wiegert RG, Freeman BJ (1990) Tidal salt marshes of the southeast
Atlantic coast: a community profile. U.S. Department of the
Interior, Fish and Wildlife Service, Washington, DC
Zimmer M, Pennings SC, Buck TL, Carefoot TH (2002) Speciesspecific patterns of litter processing by terrestrial isopods
(Isopoda: Oniscidea) in high intertidal salt marshes and
coastal forests. Functional Ecology 16:596–607
Zimmer M, Pennings SC, Buck TL, Carefoot TH (2004) Salt Marsh Litter
and Detritivores: A Closer Look at Redundancy. Estuaries 27:753–769
Zimmer M, Kautz G, Topp W (2005) Do woodlice and earthworms interact
synergistically in leaf litter decomposition? Functional Ecology 19:7–16