Wetlands (2013) 33:1151–1163
DOI 10.1007/s13157-013-0470-5
ARTICLE
Litter Decomposition, and Associated Invertebrate
Communities, in Wetland Ponds of the Copper River
Delta, Alaska (USA)
Scott D. Tiegs & Sally A. Entrekin & Gordon H. Reeves &
Deyna Kuntzsch & Richard W. Merritt
Received: 26 November 2012 / Accepted: 30 July 2013 / Published online: 21 August 2013
# Society of Wetland Scientists 2013
Abstract High-latitude wetlands provide vital ecological
functions, many of which rely on the decomposition of plant
litter, but little understanding exists of how decomposition
rates vary across space, and among common plant species.
We investigated the litter decomposition of seven plant species
in six wetland ponds on the Copper River Delta (Alaska,
USA), and the litter-associated invertebrates. The ponds exist
on common geomorphic surfaces of the delta: surfaces created
by glacial retreat and outwash, and those resulting from
uplifted intertidal area following a powerful 1964 earthquake.
An eight-fold range in decomposition rates existed across litter
species and correlated with phosphorus (r=0.63), but not
nitrogen and carbon content of the litter. Macroinvertebrate
abundance also differed among leaf species. Litter-decay rates
did not differ between pond types when expressed on a
percent-mass-loss per-day basis; however, on a per-degreeday basis, decomposition in outwash ponds was more rapid.
Electronic supplementary material The online version of this article
(doi:10.1007/s13157-013-0470-5) contains supplementary material,
which is available to authorized users.
S. D. Tiegs (*)
Department of Biological Sciences, Oakland University, Rochester,
MI 48309, USA
e-mail: tiegs@oakland.edu
S. A. Entrekin
Department of Biology, University of Central Arkansas, Conway,
AR 72035, USA
G. H. Reeves
USDA Forest Service, Pacific Northwest Research Station, Corvallis,
OR 97331, USA
D. Kuntzsch
USDA Forest Service, Cordova Ranger District, Cordova, AK
99574, USA
R. W. Merritt
Department of Entomology, Michigan State University, East
Lansing,, MI 48824, USA
Litter in outwash ponds also had greater invertebrate abundance than uplift ponds, a pattern driven by collector-gatherer
chironomids. Invertebrate activity was deemed a minor source
of litter-mass loss relative to microbial decomposition. Results
suggest that litter-associated invertebrate communities differ
between pond types, but that differences in plant-litter decomposition are subtle.
Keywords High-latitude wetlands . Plant litter . Leaf-litter
breakdown . Macroinvertebrates . Wetland functioning
Introduction
High-latitude wetlands serve vital ecological functions including climate regulation, nitrogen cycling, and habitat availability, and many of these hinge on the decomposition of organic
matter. For example, given that about a third of global soil
carbon is stored in northern peatlands (Gorham 1991),
organic-matter decomposition in high-latitude wetlands is
believed to be a significant regulator of atmospheric greenhouse gases. At more-local scales, organic-matter decomposition plays a role in the successional rates of wetlands, and by
extension the long-term viability of habitats such as areas of
open water.
Plant litter is a dominant source of carbon in most wetlands,
and its decomposition is a fundamental ecosystem-level process that is governed by: 1) intrinsic factors related to litter
quality, and 2) extrinsic factors related to the wetland environment. For example, litter species (Webster and Benfield 1986),
the presence of secondary compounds (Gessner and Chauvet
1994; Kraus et al. 2003), and nutrient content of the litter
(Enríquez et al. 1993) are intrinsic factors that influence litter
decomposition in aquatic and terrestrial ecosystems. Examples
of extrinsic factors include invertebrate consumption, temperature, and in aquatic habitats, dissolved-nutrient concentrations
(Graca 2001; Davidson and Janssens 2006; Fennessy et al.
1152
2008; Woodward et al. 2012). Ultimately these factors influence the fate of plant-derived carbon, such as whether the litter
is consumed by invertebrates, and if wetlands become net
sources or sinks for carbon (Updegraff et al. 1995).
Increasingly, high-latitude wetlands are influenced by environmental changes stemming from both natural and anthropogenic origins, and understanding how such changes influence
organic-matter decomposition is necessary if the carbon budgets and the overall ecology of these wetlands are to be well
understood.
The Copper River Delta parallels 75 km of the southcentral coast of Alaska (USA) where it supports about
1,000 km2 of wetlands, making this the largest area of coastal
wetlands on the Pacific Coast of North America (Fig. 1a). The
wetlands here have been broadly classed into physiographic
zones including tidal flats, marshlands, and glacial outwash
plains (Thilenius 1995). In aggregate, these diverse wetlands
constitute significant habitat that supports migratory waterfowl, a productive commercial salmon fishery, and species of
conservation concern (Alaska Department of Fish and Game
2012).
The ecology of the Copper River Delta changed abruptly
after the ‘Good Friday’ earthquake of 1964 (Richter magnitude 9.2), one of the most powerful ever recorded. The earthquake uplifted much of the Copper River Delta by 2–3 m,
converting subtidal areas to intertidal, and intertidal areas to
supertidal, and subsequently, the formation of large areas of
‘uplifted’ freshwater marshland (hereafter termed ‘uplifted
marsh’) where previously there had been none (Thilenius
1990, 1995). Loss of tidal influence on uplifted marsh
areas following the earthquake isolated uplifted marshes
from marine deltaic sediment inputs (Boggs 2000),
suggesting that post-earthquake accretion stems from the
accumulation of undecomposed organic matter, rather than
marine sediments. Decomposition rates may therefore be
particularly important in regulating the future ecology of
these wetlands.
Here we present a study that was designed to provide
information on: 1) how the litter of seven common plant
species on the Copper River Delta decomposes, and 2) how
decomposition varies among wetland ponds located on the
two most common geomorphic surfaces of the delta: uplifted
marsh that originated after the 1964 earthquake, and glacial
outwash plains. While some information exists on the ecological succession of uplifted wetlands on the Copper River Delta
(e.g.,Thilenius 1990, 1995), research has yet to target fundamental ecosystem-level processes such as primary production
or organic-matter decomposition, and how they may vary
between the younger uplifted marsh and other habitats. An
additional important knowledge gap relates to the relative
contribution of high-latitude wetland invertebrates to the process of decomposition, the communities of which have
remained largely unexplored (as identified in Thilenius
Wetlands (2013) 33:1151–1163
1995; but see Van Duzor 2011) relative to other wetlands
(Poi de Neiff et al. 2009). Our study was designed to evaluate
intrinsic (e.g., litter quality) and extrinsic drivers (environmental conditions, decomposer abundance) of decomposition, and
the litter-associated invertebrates on the Copper River
Delta. Such information is needed and fundamental to
understanding nutrient cycling, successional trajectories,
ecosystem functioning, invertebrate communities, and the
overall ecology of these vast but little-studied high-latitude
wetland ecosystems.
Methods
Site Description
The Copper River Delta (60° 25′ N, 145° 03′ W) forms where
the Copper River deposits sediment into the Gulf of Alaska
(Fig. 1). The delta supports about 1,000 km 2 of wetlands that
have been broadly classed into physiographic zones including
tidal flats, floodplains, marshlands, and glacial outwash plains
(Thilenius 1995). These marshlands and plains are interspersed by the reticulated channels of the Copper River, smaller rivers and streams that originate from nearby glaciers, and
sloughs that drain tidewater and the wetlands. Groundwater
inputs, tidal fluctuations, and beaver activity further complicate the hydrology of the Copper River Delta. Together these
diverse wetland types are significant habitat that supports the
largest gathering of shorebirds in the western hemisphere, a
productive commercial salmon fishery, and several species of
conservation concern (Alaska Department of Fish and Game
2012).
Climate
The climate of the Copper River Delta is cool maritime, but
becomes increasingly continental with distance from coast
and proximity to the Copper River (Thilenius 1990). The
growing season spans approximately 110 days from midMay to mid-September (Boggs 2000). Mean monthly temperatures range from −3 °C in January to 12 °C in July (at the
Cordova airport; Boggs 2000). Precipitation is abundant with
an average monthly precipitation of 20 cm (Boggs 2000).
Outwash Plains and Uplifted Marsh
Outwash plains and uplifted marshes are the dominant landscapes on the Copper River Delta (Boggs 2000), and ponds on
each of these surfaces are abundant (Fig. 1b). Outwash plains
consist of glacial deposits that are interwoven by the active and
abandoned channels of small streams. Groundwater inputs into
these systems are common. Uplifted marsh was previously an
intertidal area that was uplifted and made super-tidal by the
Wetlands (2013) 33:1151–1163
1153
Fig. 1 a Map with inset showing the location of the Copper River delta and approximate locations of the study ponds and b low-elevation aerial
photograph showing the abundance of ponds on the delta with the Chugach Mountains in the background
1964 Good Friday earthquake. The increased elevation
coupled with high precipitation that characterizes the delta
converted this intertidal area to freshwater marsh. Loss of tidal
influence on uplifted marsh areas following the earthquake
isolated these ponds from marine deltaic sediment inputs
(Boggs 2000), suggesting that accretion and plant succession
stems from the accumulation of undecomposed autochthonous
organic matter.
Plant community succession on the Copper River Delta,
following the earthquake, was characterized by Thilenius
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Wetlands (2013) 33:1151–1163
(1990). Successional trajectories in uplifted ponds appear to
be moving communities towards being similar to those of
outwash ponds. In general, shallow-water areas, such as those
around pond margins, are dominated by sedge (Carex
lyngbyei [Hornem.]), horsetail (Equisetum spp.), and marestail
(Hippuris vulgaris [L.]), with buckbean (Menyanthes
trifoliata [L.]) being found in slightly deeper water, and pond
lily (Nuphar polysepalum [Engelm.]) being common in
deeper, otherwise-open-water areas. Woody vegetation that
typically occupies less-frequently inundated sites such as
pond margins includes alder (Alnus crispa [Aiton]), and sweet
gale (Myrica gale [L.]). The decomposition of the litter of
each of these seven species was examined.
Experimental Design
Two experiments were conducted to better understand
organic-matter dynamics, and litter-associated invertebrate
communities in the ponds of the Copper River Delta.
Experiment 1 was designed to assess the decomposition of
eight litter types from the seven common plant species listed
above, and how invertebrate assemblages might colonize and
influence the decomposition of these different litter types.
Experiment 2 was designed to assess the variability in litter
decomposition and associated invertebrate communities that
may exist between ponds located in outwash plains, and
uplifted marsh (Table 1).
Field Methods
Litter decomposition was evaluated in each experiment with a
litter-bag approach (Boulton and Boon 1991; Tiegs et al.
2009). In September, a month when plants in the region are
naturally senescing and leaves are entering detrital pools,
leaves from seven terrestrial and aquatic plants common to
the Copper River Delta were gathered in the field. For one
species, lily, the stems were also gathered, for a total of eight
litter types. After being transported to the laboratory, replicate
subsets of each litter type were weighed, dried, and weighed
again to estimate the initial moisture content of each litter type.
Table 1 Pond types, and coordinates for each of the 6 ponds examined.
Coordinates are UTMs based on NAD83 datum
Pond Name
Pond Type
UTM Longitude
UTM Latitude
Lily
Square pond
Sheridan N
Rusty 2
Sheridan 1
Sheridan 2
Outwash
Outwash
Outwash
Uplifted
Uplifted
Uplifted
576707.2474
588327.8196
588860.7886
592471.4868
588136.2432
588592.1639
6710083.888
6705095.958
6705734.536
6694100.689
6705106.169
6705422.076
The moisture content was later used to ensure that a comparable dry mass was used across litter types. A mass of fresh
litter equivalent to approximately 6 g dry mass of each litter
type was then placed into coarse- and fine-mesh litter bags
(pore size approximately 10 mm and 2 mm). Using coarseand fine-mesh litter bags respectively allows and discourages
access by detritivorous macroinvertebrates, and enables estimation of the separate roles of microbes and invertebrate
activity on the decomposition process (Merritt et al. 1979;
Tiegs et al. 2009), although other mechanisms for differences
between the two bag types are also possible (water movement,
diffusion rates, etc.) (Boulton and Boon 1991).
Litter bags were transported to the six ponds in midSeptember (2009) and dispersed across five locations in each
pond. The bags were fixed in place by tying them to a nylon
rope that was attached to 2-m-long bamboo rod, approximately half the length of which was inserted vertically into the
pond sediments. Water depth at each location was approximately 40 cm, and litter bags were placed near the sedimentwater interface. At each location in each pond, a single coarsemesh bag and a single fine-mesh bag was deployed that
contained each litter type. For Experiment 1 this meant that
16 litter bags were included at each location (one pond, eight
litter types, two mesh sizes, five replicates, 80 litter bags total),
and for Experiment 2, eight litter bags were included at each
location (six ponds, four litter types, two mesh sizes, five
replicates, 240 litter bags total). In Experiment 1, litter bags
containing eight litter types were incubated in a single pond
(Lily pond – Table 1) for 56 days. This pond was selected
because 1) it was believed to be representative of many ponds
on the Copper River Delta and 2) it was readily accessible for
field workers. In Experiment 2, litter from four species was
allowed to overwinter and decompose for 227 days.
Temperature was recorded six times daily at each pond
with temperature loggers (Ibuttons, Maxim, San Jose, CA,
USA) to calculate the number of degree days to which the
litter was exposed during Experiment 2. Multiple loggers were
initially placed in each pond, however, many of the loggers
failed, and in some instances only a single logger was
downloaded from each pond. In instances when data from
multiple loggers were available, a mean was calculated for
each pond.
Laboratory Methods
After being incubated in the field, the litter bags were placed
individually into polyethylene bags, transported to the laboratory, and stored frozen. The litter was then thawed with a
small amount of water in a shallow white pan, and the contents
of the bag were rinsed over a 500 μm sieve. The litter was
gently cleaned with a paintbrush to remove biofilm and adhering debris and then dried in a tin at 40 ○C, cooled in a
desiccator, and weighed. All visible invertebrates were picked
Wetlands (2013) 33:1151–1163
by hand and stored in 70 % ethanol for later identification and
enumeration. All invertebrates were identified to lowest practical level, usually genus, using a dissecting microscope and a
functional group was assigned (Thorp and Covich 2001;
Merritt et al. 2008).
A subsample of the litter materials of each litter type was
ground to a fine powder, and the quantity of carbon and
nitrogen determined with a Costech Elemental Analyzer
(Costech Analytical Industries Inc., Valencia, CA, USA).
Phosphorus concentration was determined spectrophotometrically using the molybdate-ascorbic acid method (after
Kuehn et al. 2011).
Statistical Analysis
In Experiment 1, two-way analysis of variance (ANOVA) was
used to test for differences in decomposition rates across litter
types (fixed effect), the effect of invertebrate feeding (as
evidenced by significant differences between mesh types;
fixed effect), and interaction between these two factors.
Nested ANOVA was used in Experiment 2 to test for differences in decomposition rates between the two pond types
(fixed effect; outwash and uplifted), the six ponds (random
effect, pond nested within pond type), the effect of invertebrate activity (fixed effect; as differences between mesh
types), and litter type (fixed effect). In Experiment 2, when
higher-order interaction terms involving the main effects were
not significant, they were removed, and the ANOVA iteratively performed again.
Decomposition data were expressed as percent litter-mass
loss per day in Experiments 1 and 2 using the equation (Wi Wf)/Wi/time where Wf is the final mass of litter remaining in
the litter bags and Wi was the initial mass prior to incubation in
the field. In Experiment 2 the decomposition data were also
expressed on a per-degree-day basis to remove the effect of
temperature differences among ponds and pond types (after
Hanson et al. 1984). This was done by substituting degree
days for time in the equation shown above. KomolgorovSmirnov’s test was used to examine data for normality, and
Levene’s test was used to evaluate homoscedasticity. Some
slight departures from normality and homoscedasticity were
present and the mass-loss data were arcsine square-root
transformed. Pearson’s correlation coefficients were used to
explore hypothesized relationships between initial litter carbon, nitrogen and phosphorus content of each litter type used
in Experiment 1, and decomposition rates.
Similar statistical approaches were used to evaluate the
invertebrates associated with litter in the coarse-mesh bags.
In Experiment 1, one-way ANOVA was used to test for the
effect of litter type, followed by Tukey’s post-hoc test when
litter type was a significant factor. In Experiment 2, nested
ANOVA was used to evaluate differences in invertebrate
abundance across pond types, litter species, and ponds.
1155
When statistical significance was present, ANOVAs were
followed by Tukey’s post-hoc tests in each experiment.
Invertebrate data were expressed as the number of individuals
per gram of litter remaining in each litter bag, and log
transformed when data were not normally distributed.
Differences in macroinvertebrate community assemblage between the two wetland types and different leaf species were
also analyzed with non-metric multidimensional scaling
(NMS). All macroinvertebrate densities were log10 (x + 1)
transformed and taxa absent in more than 18 samples were
removed from the analysis. Sorenson’s distance measures
were used to calculate sample distances relative to each other
(McCune and Grace 2002). Taxa correlation coefficients
greater than 0.5 were considered important in NMS groupings
and are presented and discussed. Two multi-response permutation procedures (MRPP) using Sorenson distances tested for
community-level differences between wetland type (outwash
or uplifted) and leaf species (alder, sedge, lily, sweet gale)
where A is chance-corrected within-group agreement and p is
probability of grouping due to chance (McCune and Grace
2002). Two indicator species analyses were used to identify
taxa that are found most often and in greatest abundance in a
particular wetland type (outwash or uplifted) or associated
with a particular leaf species. All analyses described above
were run in PC-ORD version 6.
Results
Experiment 1
Litter-decomposition rates in coarse-mesh bags ranged by a
factor of approximately eight across litter the types examined
in Experiment 1 (Table 2; Fig. 2), varying from 0.0016–
0.0137% mass loss per day, with litter from sedge being the
slowest-decaying litter types examined, and lily stems being
the most rapid. These decay rates resulted in mass loss in
coarse-mesh bags of 9.7 – 76.6 % by the end of the 56-daylong incubation period. Other species filled the gradient of
decay rates across this range (Fig. 2). Despite appreciable
mass loss in many of the litter types during the experiment,
the effect of invertebrate activity, evidenced as differences
between coarse- and fine-mesh litter bags, was not significant,
and the decay rates in the two litter-bag types were comparable across all species (Table 2; Fig. 2).
The wide variation in decay rates across litter types in
Experiment 1 reflected more subtle variation in the initial
nutrient content of the litter (Fig. 3). Phosphorus content of
the litter types examined was within the range reported for
other litter species (Ostrofsky 1997), as was carbon and nitrogen content. Phosphorus content varied by more than 4 fold
across litter types, nitrogen and carbon less so, varying by
about three fold and 1.4 fold respectively. Variation in decay
1156
Wetlands (2013) 33:1151–1163
Table 2 ANOVA results of percent litter-mass loss per across the two
experiments. Higher order interaction terms were iteratively removed
when not significant. All data were arcsine square-root transformed. Bold
indicates statistical significance
Experiment 1
Experiment 2
Experiment 2 temp
corrected
Source
df SS
Species
Mesh
Species*Mesh
Type
Pond[Type]
Species
Mesh
Species*Type
TYPE*Mesh
Species*Mesh
TYPE
Pond[Type]
Species
Mesh
7
1
7
1
4
3
1
3
1
3
1
4
3
1
Species*Type 3
Mesh*Type
1
Species*Mesh 3
F
prob>f
0.05 110.8
<0.01
0.24
<0.01
0.43
<0.01
1.61
<0.01
9.58
0.03 283.06
<0.01
7.46
<0.01
0.48
<0.01
0.04
<0.01
1.48
<0.01
8.84
<0.01 36.29
0.01 237.95
0.00
6.56
<0.01
<0.01
<0.01
<.0001
0.63
0.88
0.21
<.0001
<.0001
0.007
0.69
0.84
0.22
0.003
<.0001
<.0001
0.011
0.69 0.56
0.08 0.77
2.18 0.091
rates was correlated with phosphorus content (r = 0.63,
p=0.047), but not nitrogen or carbon (Fig. 3).
Experiment 2
Differences in decomposition rates were not observed between outwash and uplifted ponds, and all interaction terms
were not significant (Table 2). Statistically significant different
decomposition rates (as percent mass loss/d) were observed,
however, among the 6 ponds examined, among the four litter
species, and between mesh types (Table 2; Fig. 4). The overall
difference in mass loss across all species and mesh types
between the pond with the most rapid decay (Sheridan
North) and the pond with the slowest decay (Sheridan 2)
was about 10 %, and differences among ponds were a modest
0.016
0.014
0.012
% Mass Loss/Day
Fig. 2 Mean decomposition rates
(as percent mass loss per day)
(+/− 1 SD) varied among the 8
litter types examined in
Experiment 1, in coarse-mesh (C)
and fine-mesh (F) litter bags.
Differences between mesh types
were not significant, suggesting
minimal litter feeding by
invertebrates. The dashed line
indicates the overall mean
decomposition rate
Macroinvertebrates responded to the different litter types used
in Experiment 1. Total invertebrate abundance ranged by a factor
of approximately 11 across litter species (Table 3; Appendix 1),
with buckbean harboring the greatest number of invertebrates per
gram of litter remaining (19.9 individuals/g), and alder litter
supporting the fewest (1.8 individuals/g). In general, the abundance of individuals belonging to different functional feeding
groups, including shredders, did not vary among litter types. A
notable exception was collector-gatherers (Table 3), which closely mirrored, and strongly influenced, total invertebrate abundance. Collector-gatherer abundance ranged by approximately
12 fold, with the greatest abundance being found in buckbean
(12.8 individuals/g) and lily litter (11.6 individuals/g), and the
least abundance observed in alder litter (1.0 individuals/g).
0.010
mean=0.0075
SD=0.0042
0.008
0.006
0.004
0.002
0.000
C F
Sedge
C F
Alder
C F
Sweetgale
C F
C F
Horse- Marestail
tail
C F
Lily
Leaf
C F
Buckbean
C F
Lily
Stem
Wetlands (2013) 33:1151–1163
1157
Fig. 3 Scatter plots of initial litter chemistry vs. decomposition rate of the
8 litter types examined in Experiment 1. Phosphorus was positively
correlated with decomposition, while carbon and nitrogen were not.
Decomposition data shown are from coarse-mesh bags, which integrates
microbial activity and feeding by macroinvertebrates
source of variation in the data set (Table 2). In contrast, litter
type was a major source of variation in the dataset (Table 2),
and as with Experiment 1, differences among litter types were
sometimes-pronounced, with lily leaves decomposing about
4.5 times more rapidly than sedge. Unlike the results of
Experiment 1, statistically significant differences between
coarse- and fine-mesh bags were observed in Experiment 2
(Table 2), evidence interpreted as macroinvertebrate activity.
However, the magnitude of the differences between mesh
types was modest (Fig. 4), suggesting that microbes were the
dominant decomposer in each of the two experiments. None
of the interaction terms were significant in Experiment 2.
When the mass-loss data were expressed on a per-degreeday basis (to account for temperature differences among
ponds), results were obtained that were similar to data
expressed on a per-day basis: significant differences existed
among ponds, among litter species, and between mesh types,
and none of the interaction terms were significant (Table 2).
Interestingly, however, pond type also became a significant
factor when decomposition was expressed on a per-degreeday basis, and mass loss per-degree-day was more rapid in
outwash ponds than that of uplifted marshes. The magnitude
of these differences was fairly modest, with decomposition in
outwash ponds being about 9 % faster across all species and
mesh types.
Invertebrate abundance differed among the 4 litter species
used in Experiment 2, with the number of invertebrates found
in leaf packs with lily leaves (17 individuals/g) being consistently greater than the litter of the other three species (Fig. 5;
Appendix 2). While less than the invertebrate abundance
observed in lily leaves, abundance was greater in sweet gale
litter (3 individuals/g) than in alder and sedge litter (which did
not differ [~1 individual/g]) (Table 4). The overall abundance
of invertebrates did not differ between pond types, or ponds
(Fig. 5) (Table 4).
In contrast to overall invertebrate abundance, the abundance of invertebrates from several functional feeding groups
differed between the two pond types (Table 4). Shredding
Table 3 Experiment 1 results for macroinvertebrates collected from leaf-litter bags with different leaf species in Lily Pond. All metrics are expressed per
gram of leaf litter remaining. All abundances were log10 transformed
Community Metric
df
ss
f ratio
prob>f
Tukey’s post-hoc
Total abundance
7
1421.2
5.09
0.001
Taxa Richness
Shannon diversity
Collector-gatherers
Predators
Scrapers
Filterers
Shredders
7
7
7
7
7
7
7
0.78
0.42
6.87
1.45
0.91
0.76
0.86
0.61
0.88
<.0001
0.22
0.51
0.62
0.55
buckbean > sedge and alder
buckbean = lily = horsetail = marestail = sweet gale
lily > alder
12.1
0.61
662.0
50.77
0.38
1.03
110.4
[[buckbean = lily] > [sedge = alder]] = [horsetail = marestail = sweet gale]
1158
Wetlands (2013) 33:1151–1163
Sheridan North
Square
Lily
Outwash
% mass loss/d
0.004
0.003
mean=0.0018
mean=0.0015
mean=0.0015
SD=0.0011
SD=0.0012
0.002
SD=0.009
0.001
0.000
Sheridan 2
Rusty 2
Sheridan 1
0.003
0.002
mean=0.0017
mean=0.0017
mean=0.0014
Uplift
% mass loss/d
0.004
SD=0.0010
SD=0.0012
SD=0.0010
0.001
0.000
C F
C F
C F
C F
C F
C F
C F
C F
C F
C F
C F
C F
Alder
Sedge
Lily
Leaf
Sweetgale
Alder
Sedge
Lily
Leaf
Sweetgale
Alder
Sedge
Lily
Leaf
Sweetgale
pond types when data were expressed on a percent-mass-loss basis,
however, differences were detected when data were expressed on a
percent-mass-loss per-degree-day basis
100
40
Lily
Sheridan
North
Square
20
Outwash
80
mean=10.11
mean=6.69
SD=27.69
SD=10.58
mean=2.25
SD=1.02
0
100
80
40
Sheridan 1
Rusty 2
Sheridan 2
Uplift
invertebrate abundance (#/g litter remaining)
Fig. 4 Mean decomposition rates (as percent mass loss per day) (+/− 1
SD) across the two pond types, litter species, in coarse (C)- and fine (F)mesh litter bags. The dashed line indicates a mean for each pond across all
species and mesh sizes. Differences were not observed between the two
20
mean=7.54
mean=4.65
mean=3.68
SD=7.52
SD=5.41
0
Alder Sedge Lily SweetLeaf gale
SD=0.65
Alder Sedge Lily SweetLeaf gale
Fig. 5 Bar graphs showing invertebrate abundance (means +/− 1 SD) in
coarse-mesh litter bags across the 6 ponds (standardized by litter mass
remaining), and the 2 pond types examined in Experiment 2. Pie charts in
each panel show the relative abundance of functional feeding groups.
Alder Sedge Lily SweetLeaf gale
Scrapers, shredders, and collector-gatherer abundance was significantly
greater in outwash ponds than in uplift ponds. Invertebrates tended to be
more abundant in lily litter than other litter species
Wetlands (2013) 33:1151–1163
1159
Table 4 Results for macroinvertebrates collected from leaf-litter bags in each pond used in Experiment 2. All metrics are expressed per gram of leaf litter
remaining. All abundances were log10 transformed
Source
df
Taxa richness
Type
Pond[Type]
Species
Type*Species
1
4
3
3
0.034
5.67
7.11
0.67
0.01
0.59
1.00
0.09
Shannon Diversity
Type
Pond[Type]
Species
Type*Species
Type
Pond[Type]
Species
Type*Species
Type
Pond[Type]
Species
Type*Species
Type
Pond[Type]
Species
Type*Species
Type
Pond[Type]
1
4
3
3
1
4
3
3
1
4
3
3
1
4
3
3
1
4
0.32
0.59
0.12
0.38
0.048
1.059
15.89
0.54
0.05
0.34
2.02
0.03
0.09
0.13
0.15
0.16
0.12
0.22
1.48
0.68
0.18
0.59
0.30
1.69
33.99
1.15
1.03
1.63
13.06
0.17
4.18
1.37
2.07
2.24
3.04
1.40
0.23
0.60
0.91
0.62
0.58
0.16
<.0001
0.34
0.31
0.17
<.0001
0.91
0.044
0.25
0.11
0.089
0.085
0.24
Species
Type*Species
Type
Pond[Type]
Species
Type*Species
Type
Pond[Type]
3
3
1
4
3
3
1
4
0.58
0.18
0.59
0.22
1.15
0.22
0.29
0.61
4.97
1.57
13.18
1.25
8.57
1.66
5.05
2.60
0.003
0.20
0.001
0.29
<.0001
0.18
0.027
0.041
Species
Type*Species
3
3
5.96
0.32
33.89
1.82
<.0001
0.15
Total abundance
Predator abundance
Scraper abundance
Filterer abundance
Shredder abundance
Collector-Gatherer
abundance
SS
invertebrates were 3.5 time more abundant in outwash ponds
than uplifted ponds. Interestingly, scraping invertebrates were
rare in uplifted ponds, and 29 times more abundant in outwash
ponds. Collector-gatherers were slightly (0.42 times) more
abundant in uplifted ponds. Other functional feeding groups
(predators, filterers) did not differ between pond types
(Table 4).
NMS analysis separated distinct macroinvertebrate communities in two-dimensional space (final stress 11.62) with
Axis 1 explaining 40 % and Axis 2 explaining 42 % of
variation in communities across wetland types and leaf species
F
prob > f
Tukey’s post-hoc
0.91
0.67
0.39
0.96
lily leaf > sweet gale > sedge = alder
lily leaf > sweet gale = sedge = alder
outwash > uplift
lily leaf = sweet gale > sedge = alder
outwash > uplift
lily leaf > sweet gale = sedge = alder
uplift > outwash
[up.]sherid. 1 = [out.]square > [up.]rusty
2 = [up.]sherid. 2 = [outwash]sherid N >
[outwash]lily
lily leaf > sweet gale = sedge = alder
(Fig. 6). Macroinvertebrates separated along Axis 1 by the
abundance and occurrence of collector-gatherer chironomid
midges (r=−0.94) (individuals belonging to Dicrotendipes
and Polypedilum were the most abundant), predaceous
midges (Tanypodinae) (r= −0.79), amphipods (Hyalella)
(r=−0.65), snails (Planorbidae) (r=−0.51), and fingernail
clams (Sphaeriidae) (r=−0.50) associated with lily leaves.
Macroinvertebrates separated along Axis 2 by the abundance
and occurrence of the amphipod, Crangonyx. Differences in
macroinvertebrate communities between pond types were
confirmed with an MRPP (p=0.05; A=0.03). Filter feeding
1160
1.5
Lily
1.0
Lily
Axis 2 (42%)
Fig. 6 Non-metric
multidimensional scaling
representing log10 abundance of
all dominant taxa (represented in
more than 20 % of the samples) in
outwash (open symbols) and
uplift ponds (filled symbols) for
each litter type: alder (circle),
sedge (square), lily leaf
(diamond), sweet gale (hexagon)
Wetlands (2013) 33:1151–1163
Lily
0.5
Rusty 2
Square
Sheridan N
Square
Sheridan N
0.0
Sheridan 2
Sheridan N
Rusty 2
Rusty 2
Square
Square
Sheridan 1
Sheridan 2
-0.5
Sheridan 2Sheridan 2
Sheridan N
Sheridan 1
Sheridan 1
Rusty 2
-1.0
-1.5
-1.0
-0.5
0.0
Sheridan 1
0.5
1.0
1.5
2.0
Axis 1 (40%)
Polycentropus (ISA=66, p=0.014) and predaceous Hirudinea
(63, 0.013) were indicators of uplifted wetlands. Shredding
Crangonyx (ISA=75, p=0.0006) and scraping Planorbidae
(55, 0.013) were indicators of outwash ponds.
Macroinvertebrate communities also differed across leaf
species. Macroinvertebrate communities in lily litter differed
(p<0.05) from those on alder, sedge, and sweet gum. Sedge
communities also differed from sweet gum. Macroinvertebrate
indicator species were only identified in lily litter and they
included predaceous chironomid midges (ISA=59, p=0.02),
collector-gatherer chironomid midges (ISA=55, p=0.0004),
shredding Hyalella (ISA=48, p=0.05), and filter feeding fingernail clams (ISA=55, 0.05).
Discussion
We evaluated select aspects of ecosystem structure and functioning of uplifted and outwash ponds on the Copper River
Delta. The structure of litter-associated-invertebrate communities differed between uplifted and outwash ponds, with
uplifted ponds having significantly more collector-gatherers
(chironomids), and outwash ponds having a greater abundance of scrapers (snails) and shredders (amphipods).
Despite these and other differences in invertebrate community
structure, the two pond types were similar with regards to their
organic matter decomposition. Conspicuous differences in
decomposition were observed, however, among the different
litter types, and a wide-range in decay rates was observed
across litter species. While invertebrate activity was not
deemed a significant source of litter-mass loss, invertebrates
were significantly more abundant in some litter types than
others. Decomposition rates were very slow relative to most
published values (e.g., review by Webster and Benfield 1986),
and probably temperature related, and suggested organicmatter accumulation and storage on an annual basis. Overall
these results illustrate the value of evaluating both ecosystem
structure and function to provide a complete picture of ecosystems, such as the high-latitude ponds of the Copper River
Delta.
A large body of literature has developed around using
plant-litter quality to predict litter-decomposition rates, and
while the results from individual studies have sometimes been
contrasting, nutrient content of the litter often emerges as
having a significant influence. Numerous studies have shown
positive correlation between rates of litter-mass loss and ratios
of carbon-to-nitrogen in the litter (e.g., Ostrofsky 1997;
Enríquez et al. 1993); however, our study did not. Rather,
the 8-fold range in decomposition observed across the 8 litter
types was positively correlated with litter phosphorus content,
a finding consistent with others (e.g., Rejmánková and
Houdková 2006). Additional evidence that litter nitrogen content was not significant in influencing decomposition is that
while the leaves and stems of lily had the greatest and least
nitrogen content across all litter types, and they had very
similar decomposition rates. These results, coupled with evidence that most of the mass loss that was observed was
attributed to microbes, suggests that the microbial communities of these ponds are phosphorus-limited, but future experiments are needed.
Our experimental design did not allow us to isolate the
mechanisms responsible for the differences in invertebrate
abundance that were observed across litter types, but several
are possible. Differences in invertebrate production across litter
types, for example, would explain the patterns in invertebrate
abundance that were observed. The greatest abundance of
Wetlands (2013) 33:1151–1163
invertebrates was found in litter types with a high P content, an
observation that is consistent with litter-quality-driven differences in invertebrate production (e.g., Leroy and Marks 2006;
Greenwood et al. 2007; Tank et al. 2010). Differential production could also have been driven by variation in habitat quality
that was provided by the different litter types, which could
result, for example, in variable refuge quality and differential
predation rates within the litter packs. An additional, and not
mutually exclusive mechanism for the patterns in invertebrate
abundance that were observed, could be aggregation/
avoidance of litter packs with desirable/undesirable attributes
(e.g., as a food resource, or habitats). This idea is distinct from
those suggested above in that it is a behavioral response
involving net movement of invertebrates into the litter bags,
and not directly related to production in the litter bags themselves (Abos et al. 2006; Entrekin et al. 2008; Tiegs et al.
2008).
The invertebrate results from Experiment 1 were largely
mirrored in Experiment 2, where greater invertebrate abundance was found in lily leaves. While the greater abundance of
shredders in Experiment 2 leaf packs containing lily leaves
makes intuitive sense given their high nitrogen and phosphorus content, it is less clear why other functional feeding groups
were so abundant on lily leaves. For example, filterers were
more abundant on the leaves of lily than the other litter types
examined in Experiment 2, as were collector-gatherers. In the
case of collector-gatherers, which made up the majority of
invertebrates in our study, and were more abundant on lily
leaves in both Experiments 1 and 2, individuals may have
preferred the biofilm present on the surface of this rapidly
decomposing litter type. Microbial communities differ across
litter types, and the different abundances of collector-gatherers
may reflect differences in microbial communities (Ward and
Cummins 1979).
Macroinvertebrate taxa richness across both experiments
was low, with a total of only 16 taxa identified, which may
be reflective of the geography, geologic history, and environmental conditions of the ponds. Most functional feeding groups
were represented by only 2–3 taxa. For example, in Experiment
1, the only shredding taxa were a trichopteran represented by a
single species of Nemotaulius (Limnephilidae), and the amphipods Crangonyx, and Hyalella. In geologic terms the ponds we
examined are young, existing only since the last glacial retreat,
and therefore might be expected to harbor relatively few species (Pianka 1966). Furthermore, the freshwater habitats of the
delta are surrounded by the Gulf of Alaska to the south,
and the Chugach Mountains to the north, both of which
may function as barriers to dispersal for some freshwater macroinvertebrates. In the case of the uplift ponds,
where all freshwater taxa have colonized in the years
subsequent to the 1964 earthquake, it is not surprising
to find so few taxa. Given that our study was not
conducted during the summer, additional taxa would
1161
likely have been encountered had our study been
conducted during the summer months, with possible
consequences for litter decomposition. Lastly, harsh environmental conditions in the ponds likely exclude certain taxa (Battle and Golladay 2001). Colonization by a
few key taxa in the future, such as large-bodied shredders, could have consequences for the functioning of
ponds on the Copper River Delta.
The differences in functional feeding groups that we observed between pond types may reflect differences in ecosystem conditions, such as degree of heterotrophy and storage of
organic matter. For example, the number of shredders/
collectors - an indicator of coarse particulate organic matter
(CPOM) storage in wetlands relative to that of fine particulate
organic matter (FPOM) (Merritt et al. 1999) - was approximately five times greater in outwash ponds relative to uplifted
ponds. This finding suggest that CPOM has greater influence
on structuring foodwebs in outwash ponds. A related indicator
is the abundance of scrapers relative to the abundance of
shredders + collectors, with greater values translating to more
autotrophy. Based on this indicator the degree of autotrophy
was less in outwash ponds (a value of 0.14) relative to uplift
ponds (a value of less than 0.01), although both pond types
were strongly heterotrophic. Perhaps the most obvious reason
for these ostensible differences in ecosystem condition is pond
age, with the relatively young age of the uplift ponds limiting
the amount of CPOM accrual. Inferences about the ecosystem
condition of these ponds based on our invertebrate data should
be tempered, however, given that the invertebrates were gathered via litter bags, and not more conventional means of
sampling.
Differences in litter decomposition between pond types
became apparent only when decomposition rates were
expressed on a per-degree-day basis, perhaps due to differences in temperature among ponds. Decomposition rates were
very similar (approximately a 1 % difference) between the two
pond types on a per-day basis (0.00157 and 0.00156 % mass
loss per day in uplifted and outwash ponds respectively when
data across mesh and litter types were combined).
Temperature-corrected decomposition rates were significantly
more rapid (by approximately 9 %), however, in outwash
ponds compared to uplift ponds (.00066 and .00061 across
mesh and litter types). Perhaps the most parsimonious interpretation of these results is that statistically significant differences in litter decomposition between pond types became
detectable only in the absence of noise that resulted from
temperature differences among ponds. While ANOVA revealed that there was no significant difference in the number
of degree days between the two pond types (F=0.37, p=0.58),
the magnitude of the non-significant difference in the mean
number of degree days between the two pond types was 58
more than in outwash ponds (554 vs. 612° days). This finding
can be explained by the greater proximity of uplifted ponds to
1162
the relatively moderate winter temperatures of the localized
marine environment in Southcentral Alaska. This lack of
significant difference between degree days might be due to
low levels of statistical power, rather than a true ecological
difference between the pond types. Regardless, by accounting
for temperature variation among ponds through the use of
temperature-corrected decay rates, the sensitivity of our
ANOVA model was improved, and subtle differences in decomposition between uplifted and outwash ponds were
revealed.
An additional and complementary explanation for the more
rapid temperature-corrected decomposition in outwash ponds
is litter-feeding invertebrates. Overall, shredders were a relatively minor component of invertebrate communities, but they
were more abundant in the litter bags from outwash ponds.
Evidence of differential invertebrate activity between pond
types should have been indicated by significant interaction
of mesh and pond type in our ANOVA models. No interactions were present, however, indicating that while structural
differences were present in the invertebrate communities between pond types, they did not translate to differences in
decomposition rates.
Decomposition attributed to microbial activity was a
more substantial source of mass loss than litter consumption by invertebrates. Invertebrate feeding activity,
evidenced as statistically significant differences between
coarse- and fine-mesh bags, was not apparent in
Experiment 1, but was apparent in Experiment 2. This
discrepancy can probably be attributed to the fact that
Experiment 1 was 56 days in duration compared to
Experiment 2 that lasted 227 days. Experiment 1 was
perhaps of insufficient duration to allow microbial conditioning and subsequent consumption by invertebrates.
Although differences in mass loss between mesh types
were present in Experiment 2, they were modest compared
to the amount of overall mass loss that occurred in most
species (Fig. 4). In aggregate this information indicates
that the appreciable mass loss that was present across
most litter species was driven by microbial activity, and
with invertebrate feeding activity being secondary. This
finding bears relevance for the future functioning of the
wetlands of the Copper River Delta given that warming:
1) is projected for coastal Alaska (Haufler et al. 2010),
and 2) is predicted to increase microbial-decomposition
rates (and to a greater degree than invertebrate-mediated
decomposition) (Boyero et al. 2011). Additionally, given
that Carex is a dominant plant genus with poor nutritional
quality (as evidenced by carbon, nitrogen and phosphorus
content), and given that the decomposition of nutrient-poor
litter is believed to increase more in response to warming
than the decomposition of nutrient-rich litter (Ferreira and
Chauvet 2011), warming trends on the Copper River Delta
would seem to have particular ecological relevance.
Wetlands (2013) 33:1151–1163
Conclusions
The Copper River Delta harbors significant social and ecological value, but surprisingly little research has been
conducted in terms of the delta’s ecology, especially the
functioning of the delta as an ecosystem. Our results suggest
some functional similarities between outwash and uplifted
ponds, and structural differences between invertebrate communities. Decomposition in both pond types was very slow,
suggesting potential for accumulation and storage of organic
matter on an annual basis. Given that the successional trajectories of the uplifted ponds will include increased abundance
of slow-decomposing species such as sedge, alder, and sweet
gale, the carbon-storage-related services provided by uplifted
ponds can be expected to increase. While our study offers
some insights into the contemporary ecology of the Copper
River Delta, given that area is largely unmanaged (Haufler
et al. 2010), the data presented also have value as a baseline
against which future work can be compared to understand
environmental change in this vast and unique ecosystem.
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