Download Salt Marsh Litter and Detritivores

Estuaries
Vol. 27, No. 5, p. 753–769
October 2004
Salt Marsh Litter and Detritivores: A Closer Look at Redundancy
MARTIN ZIMMER1,*, STEVEN C. PENNINGS2,†, TRACY L. BUCK2,‡, and THOMAS H. CAREFOOT3
1
Zoologisches Institut—Limnologie, Christian-Albrechts-Universität, Olshausentraße 40, 24098
Kiel, Germany
2 University of Georgia Marine Institute, Sapelo Island, Georgia 31327
3 Department of Zoology, University of British Columbia, Vancouver, BC V6T 1Z4, Canada
ABSTRACT: Most primary production of angiosperms in coastal salt marshes enters the detritivore food web; studies
of this link have predominantly focused on one plant species (Spartina alterniflora) and one detritivore species (Littoraria
irrorata). In mesocosm experiments, we studied the rates and pattern of decomposition of litter derived from four plant
species common in southeastern United States coastal salt marshes and marsh-fringing terrestrial habitats. Crustaceans
and gastropods were selected as detritivores feeding on, and affecting degradation of, the litter of two monocotyledons
and two dicotyledons. Despite interspecific similarities in consumption, detritivores exhibited species-specific effects on
litter chemistry and on the activity of litter-colonizing microbiota. The chemical composition of feces depended upon
both the litter type and the detritivores’ species-specific digestive capabilities. Growth rates and survival of detritivores
differed among litter species. Different salt marsh detritivores are likely to have different effects on decomposition
processes in the salt marsh and cannot be regarded as functionally redundant nor can the litter of different plant species
be regarded as redundant as food for marsh detritivores.
of biodiversity, it is likely that functional redundancy increases ecosystem stability (resistance to and
resilience from disturbance; e.g., Griffiths et al.
2000). With respect to ecosystem functioning in
terms of particular processes, functional redundancy may have little effect, owing to competitive interactions between functionally redundant organisms. Coexisting detritivores are usually found to
differ in terms of feeding strategies, nutritional requirements, and digestive capabilities in both
aquatic (Arsuffi and Suberkropp 1989; Graça et al.
1993; Ray and Straškraba 2001) and terrestrial
(Bardgett and Chan 1999; Zimmer and Topp 2000;
Zimmer et al. 2002) ecosystems. It is these differences that reduce competition and make coexistence possible (competitive exclusion principle:
Hardin 1960; Armstrong and McGehee 1980; Richards et al. 2000), but the differences are also significant with respect to the species’ effects on ecosystem processes (Zimmer and Topp 1999; Richards et al. 2000; Cragg and Bardgett 2001; Zimmer
et al. 2002). By definition members of the same
guild that differ in the way they use available food
sources cannot be considered redundant and may
even have additive or synergistic effects on ecosystem functioning (Lawton et al. 1998; Jonsson and
Malmqvist 2000; Duffy et al. 2001; Zimmer et al.
2002). High within-guild biodiversity may promote
ecosystem processes, such as decomposition, if
functional redundancy in terms of detritivores’
contributions to decomposition processes is low.
In contrast to other intertidal habitats where detritus is either accumulated above the uppermost
Introduction
Although the potential significance of species diversity in ecosystem maintenance has been the topic of many ecological studies, this aspect of biodiversity has been addressed relatively rarely in studies of decomposition processes. Studies of decomposition that do consider the significance of
detritivore diversity mostly conclude that species
diversity promotes ecosystem decomposition processes (Sulkava and Huhta 1998; Zimmer and
Topp 1999; Jonsson and Malmqvist 2000; Jonsson
et al. 2001; Crowl et al. 2001). In addition to this
top-down effect of diversity on decomposition processes, there may also be a bottom-up effect in that
plant litter diversity seems to affect both the rate
of litter decomposition (Kautz and Topp 1998; Kaneko and Salamanca 1999; Conn and Dighton
2000; Zimmer 2002) and the rate of colonization
by litter microbes (Sulkava et al. 2001), as well as
the relative significance of detritivores in the ecosystem (Sulkava and Huhta 1998). A pressing aspect of our current interest in biodiversity is understanding the extent to which different species
in the same guild are functionally redundant or
diverse (Chalcraft and Resetarits 2003a,b).
From what we know about the ecosystem effects
* Corresponding author; tele: 149/431/880-4153; fax: 149/
431/880-4368; e-mail: [email protected]
† Current address: Department of Biology and Biochemistry,
University of Houston, Houston, Texas 77204-5001.
‡ Current address: North Inlet-Winyah Bay NERR, Baruch
Marine Laboratory, P.O. Box 1630, Georgetown, South Carolina
29442.
Q 2004 Estuarine Research Federation
753
754
M. Zimmer et al.
tidal level or washed away through wave action, detritus from angiosperms in salt marshes accumulates in the dense vegetation. Energy flux from primary producers in these systems is thought to be
largely detritus-based (Smalley 1960; Teal 1962;
Nixon and Oviatt 1973; Valiela and Teal 1979; Silliman and Zieman 2001). Because salt marshes are
dominated by plants of terrestrial origin (angiosperms), but contain animals of primarily marine
origin (e.g., snails and crabs) many of which act as
detritivores (Bärlocher et al. 1989; Kemp et al.
1990; Bärlocher and Newell 1994; Kneib et al.
1997; Graça et al. 2000) or omnivores (Buck et al.
2003), they provide an evolutionary and ecological
link between marine and terrestrial systems. Oniscidean isopods are among the few terrestrial invertebrates that invade salt marshes as detritivores that
feed on both littoral and supralittoral plant debris
(Rietsma et al. 1982; Valiela and Rietsma 1984;
Zimmer et al. 2002), increasing within-guild diversity of detritivores.
Decomposition of plant litter can be described
in terms of litter mass-loss that is due to feeding
and digestion by detritivorous animals (detritivores) and microbiota, resulting in the mechanical
breakdown and fragmentation of litter particles
(comminution) and the egestion of surface-increased feces by shredders, and in changes in the
chemical composition of the litter (degradation)
and the egestion of partially digested litter material
in feces. In both terrestrial systems (e.g., Wood
1974; Facelli and Picket 1991; Zimmer 2002) and
intertidal salt marshes (Bärlocher et al. 1989;
Kemp et al. 1990; Newell and Bärlocher 1993; Newell 1996; Graça et al. 2000), decomposition processes of plant litter are controlled by comminution through detritivore shredding and feeding, digestive processes of detritivores, and detritivoremediated activity of litter-processing microbiota.
Intuitively implying that both detritivores and detritus are likely redundant (cf., Wardle 1999), and
despite the variety of plants that occur in salt
marshes and the variety of potential detritivores,
most studies of detritivoral processes in eastern
North American coastal salt marshes have focused
on the most abundant detritivore in southern
marshes, the gastropod Littoraria irrorata, and its
most important source of litter, the grass Spartina
alterniflora; less is known about other detritivores
and litter sources (Rietsma et al. 1982; Valiela and
Rietsma 1984; Kneib et al. 1997; Graça et al. 2000).
Most studies on salt marsh decomposition have focused only on feeding and growth of detritivores,
or mass loss of litter.
We have chosen to study four invertebrate detritivores and the litter of four angiosperms, with the
goal of determining whether these species are
functionally redundant in terms of contributions
to decomposition processes or in serving as food
for detritivores, respectively. We tested three hypotheses: syntopic detritivores in salt marshes differ with respect to their nutritional requirements
and digestive capabilities, syntopic plants differ
with respect to litter quality as food for detritivores,
and syntopic detritivores in salt marshes exhibit
differential effects on decomposition processes of
different plants, so neither detritivores nor plants
are functionally redundant. While many studies on
functional redundancy of consumers have created
different diversity levels by excluding or including
different combinations of animals ( Jonsson and
Malmqvist 2000; Duffy et al. 2001), we took an alternate approach of examining each species’ effects on decomposition processes in single-species
mesocosm experiments, since we were interested
in single-species effects and capabilities rather than
the effects of different consumer combinations.
Some consumer combinations in mesocosms were
impossible due to both species-specific environmental requirements and predator-prey interactions (Buck et al. 2003). We stocked different mesocosms with different litter types to elucidate differential effects of litter type on the detritivores.
Material and Methods
Experiments were conducted at the Marine Institute of the University of Georgia, at Sapelo Island, Georgia, United States (318279N, 818159W),
during March and April 2000. For our experiments, we used four detritivores and four angiosperms common in high intertidal salt marshes
around the island. The detritivores were the periwinkle Littoraria irrorata (Gastropoda: Prosobranchia), the coffee-bean snail Melampus bidentatus
(Gastropoda: Pulmonata), the wharf crab Armases
cinereum (Crustacea: Decapoda), and the coastal
pillbug Venezillo parvus (V. evergladensis cf., Taiti and
Ferrara 1991; Crustacea: Isopoda). The plants used
as food for the detritivores were the smooth cordgrass Spartina alterniflora, the black needlerush Juncus roemerianus, the sea daisy Borrichia frutescens,
and the live oak Quercus virginiana. S. alterniflora is
the most common salt marsh plant along the Atlantic coast of the U.S., dominating large areas of
the low and middle marsh elevations (Bertness
1999; Pennings and Bertness 2001). J. roemerianus
is the second most common salt marsh plant at
southeastern sites, dominating the high marsh
(Wiegert and Freeman 1990). Both S. alterniflora
and J. roemerianus produce large amounts of litter
that accumulates in patches in the high marsh
(Bertness and Ellison 1987; authors’ personal observations). B. frutescens is common in the high
marsh, forming zones several meters wide at many
Redundancy of Detritivores?
Fig. 1. Relative consumption rates (RCR) of detritivores
feeding on four different litter types or a mixture of these litter
types. Littoraria irrorata, Melampus bidentatus, Armases cinereum,
and Venezillo parvus. RCR is defined as dry g eaten 3 [dry g
body mass (including shells) 3 d]21. Data are means 6 1 SD;
n 5 10 per litter type per detritivore species; p values for oneway ANOVAs are indicated above bars; shared letters indicate
no significant differences among litter types (Tukey test at a 5
0.05).
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Fig. 2. Relative growth rates (RGR) of detritivores feeding
on four different litter types or a mixture of these litter types.
Littoraria irrorata, Melampus bidentatus, Armases cinereum, and Venezillo parvus. RGR is defined as dry g mass gain 3 (dry g initial
mass 3 d)21. Data are means 6 1 SD; n 5 10 per litter type per
detritivore species; p values for one-way ANOVAs are indicated
above bars; shared letters indicate no significant differences
among litter types (Tukey test a 5 0.05).
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M. Zimmer et al.
Fig. 3. Mortality (Kaplan-Meier survival analysis) of crustacean detritivores feeding on four different litter types or a mixture of these litter types. Survival curves display percent survival
as a function of time (6 95% CI) for fractional survival at any
particular time. Armases cinereum and Venezillo parvus. Shared letters indicate no significant differences among litter types (pairwise Mantel-Haenszel tests at a 5 0.05).
sites, and drops its leaves into the high marsh (Pennings and Moore 2001). Q. virginiana is one of the
most common marsh-side trees in the southeastern
U.S., and drops large amounts of litter directly into
high marsh habitats (authors’ personal observations). All species will be referred to by genus
names.
In mesocosm experiments, detritivores were
housed individually in 1,000 ml (Armases) or 500
ml (Littoraria) glass jars, or in groups of 4 (Melampus) or 6 (Venezillo) in 100 ml plastic jars, at ambient temperature (20 6 28C) and light conditions
(13 h light:11 h dark). By pooling individuals of
the smaller detritivore species, we standardized at
least partially for size without risking measurement
error by offering very small amounts of food. One
potential problem with this design, intraspecific
competition, was circumvented by providing food
in excess. Mesocosms were opened every 2 d to
allow air exchange and to add deionized water as
needed according to weight loss of litter as determined in pre-experiments. Detritivore mortality
was recorded every 2 d, and survival curves were
Fig. 4. Crawling activity of Littoraria irrorata and respiration
of Melampus bidentatus and Armases cinereum after having fed on
four different litter types or a mixture of these litter types for
30 d. Data are means 6 1 SD; n 5 10 per litter type per detritivore species; p values for one-way ANOVAs are indicated above
bars; shared letters indicate no significant differences among
litter types (Tukey test a 5 0.05).
calculated using the Kaplan-Meier method. Survival curves plot percentage survival as a function of
time and 95% confidence interval for fractional
survival at any particular time. Pair-wise comparison of survival curves were performed with MantelHaenszel tests (log-rank test for two samples: Motulsky 1995). Detritivore biomass at the start of the
experiment was measured on a fresh mass basis
and later converted to dry mass through fresh
mass:dry mass ratios (after drying to constant mass
at 608C; n 5 10 for each species).
We collected plant litter as follows: Spartina and
Juncus as fallen dead stems and leaves, respectively,
that had accumulated in clumps (wrack) in the
high intertidal zone, and Borrichia and Quercus as
Redundancy of Detritivores?
Fig. 5. C:N ratios of detritivores, Littoraria irrorata (soft bodies, without shells) Melampus bidentatus (whole bodies, including
shells); Armases cinereum (whole bodies) and Venezillo parvus
(whole bodies) after having fed on four different litter types or
a mixture of these litter types for 30 d. Data are means 6 1 SD;
overall significance (one-way ANOVA) is indicated above bars;
shared letters indicate no significant differences among litter
types (Tukey test at a 5 0.05).
757
Fig. 6. Comminution rate of four different litter types
alone and in mixture by detritivores in relation to their biomass. Littoraria irrorata, Melampus bidentatus, Armases cinereum,
and Venezillo parvus. Data are means 6 1 SD; n 5 10 per litter
type per detritivore species; p values for one-way ANOVAs are
indicated above bars; shared letters indicate no significant
differences among litter types (Tukey test at a 5 0.05).
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M. Zimmer et al.
Fig. 7. Fraction-size distribution of four different litter types
after comminution by detritivores. Littoraria irrorata, Melampus
bidentatus, Armases cinereum, and Venezillo parvus. Data are means
of percent values; n 5 10 per litter type per detritivore species.
Fig. 8. Change in microbial respiration through detritivores
feeding on four different litter types or a mixture of these litter
types in mesocosms after 30 d as compared with detritivore-free
control mesocosms (5 100%). For the calculation of percent
values, controls and treatments were random-paired. Littoraria
irrorata, Melampus bidentatus, Armases cinereum, and Venezillo parvus. Values for control mesocosms are indicated by dashed lines
at 100%. Data are means 6 1 SD; n 5 9 per litter type per
detritivore species. Means that differ significantly from controls
(ANOVA, a 5 0.05) are indicated with an asterisk above bars,
while those not differing significantly from controls are indicated with ns above bars. Shared letters indicate no significant differences among litter types for each detritivore species (Tukey
test at a 5 0.05).
Redundancy of Detritivores?
759
TABLE 1. Influence of the litter type and the detritivore species (two-way ANOVA) on microbial respiration.
Litter
Consumer
Interaction
Error
Total
df
SS
F
p
4
3
12
180
199
14
142
65
216
437
3.1
39.5
4.5
0.019
,0.001
,0.001
leaves from the salt marsh surface. For each plant
species, a single collection of litter was made. We
collected litter that was in an intermediate stage of
decomposition (neither freshly fallen nor heavily
decomposed); in every case this was the most
abundant stage available in the field. The collection was well mixed before it was offered to consumers.
We collected detritivores by hand as follows: Littoraria and Melampus from stems of Spartina and
Juncus at low tide, and Armases and Venezillo by
hand from high-intertidal marshes (Armases) or
marsh-fringing oak forests (Venezillo).
Each litter type was added to separate mesocosm
jars (n 5 10 for each detritivore-litter combination) in sufficient quantities (based on palatability
of the food and consumption rates of the particular detritivore involved as predicted according to
litter mass loss in pre-experiments) for a 30-d test
period. A mixture of all four litter types was used
in separate mesocosm jars (n 5 10 per detritivore)
to study the effect of litter diversity on detritivoremediated decomposition processes (cf., Sulkava
and Huhta 1998; Zimmer 2002). We used detritivore-free control mesocosms to monitor changes
due to leaching and microbial processing (n 5 10
for each detritivore-litter combination). Litter dry
mass was determined based on fresh mass:dry mass
ratios (n 5 20 per plant species). With four species
of detritivores, five litter treatments (four species
1 one combination), and 10 replicates of each, we
had 200 separate mesocosms with detritivores and
200 control mesocosms.
After 30 d, we removed detritivores from the mesocosms and monitored the following performance parameters. Dry mass of litter remnants revealed information on litter-mass loss (litter input
2 litter output); for mixed-litter assays, we sorted
litter remnants by species before drying them.
From these values and from measurements of detritivore dry mass, we calculated consumption rates
[(mg food ingested) 3 (d 3 mg average detritivore mass)21] and relative growth rates [(mg dry
mass change) 3 (d 3 mg average detritivore
mass)21] of detritivores for the 30-d duration of the
experiment. Respiration rates of individual Armases
and Melampus (expressed as CO2 production: ADC
Fig. 9. Change in content of carbon and nitrogen in four
litter types (Juncus, Spartina, Borrichia, and Quercus) after 30 d
incubation in mesocosms as compared with initial values of the
litter (5 100%). C 5 control, L 5 Littoraria irrorata, M 5 Melampus bidentatus, A 5 Armases cinereum, V 5 Venezillo parvus.
Initial values for litter are indicated by dashed lines at 100%.
Data are means 6 1 SD; n 5 9 per litter type per detritivore
species; shared letters indicate no significant differences among
treatments for each element within each litter type (ANOVA
followed by Tukey test at a 5 0.05). Detritivore-free control
means that differ from initial values are indicated with an asterisk above bars.
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M. Zimmer et al.
TABLE 2. Influence of the litter type and the detritivore species (two-way ANOVA) on changes in the carbon and nitrogen content
of litter remnants.
Litter
Consumer
Interaction
Error
Total
df
Carbon
SS
3
4
12
180
199
516000
5289
47290
6759
575400
F
p
4580.8
35.2
104.9
,0.001
,0.001
,0.001
LCA-4 CO2 Analyzer) were determined at the termination of the experiment. For Littoraria respiration rates could not be measured in the same
manner, because our measurement technique was
not sensitive enough for use with this species.
Some Littoraria pulled back into their shells whereas others crawled vigorously, and so it was impossible to standardize activity level. We used a behavioral index, crawling activity (cm 3 min21 in moist
Petri dishes) at the completion of the experiment,
as an alternative to the physiological measurements done on other species. After 30 d of feeding
on different food sources, crawling is indicative of
diet quality: well-fed animals will be vigorous, poorly-fed animals will be indolent. For every detritivore the body carbon:nitrogen (C:N) ratio (Carlo
Erba NA-1500 NCS Analyzer) was determined after
the experiment. Performance of Armases and Venezillo was further estimated in terms of mortality
during the course of the experiment (snails experienced no mortality).
Microbial respiration rate (expressed as CO2
production: ADC LCA-4 CO2 Analyzer) was measured to gauge the effect of detritivore presence
on microbial activity of the litter. After removing
detritivores from the mesocosms, we compared microbial respiration [mmol CO2 3 (mg litter 3 h)21]
in these mesocosms with values obtained from detritivore-free control mesocosms. We divided the
values of detritivore assays by those of control assays (random pairings) to calculate a promotion
factor for microbial activity (expressed as a percent
of control value).
We determined litter-fraction size after the detritivores were removed to obtain information on
the extent of grazing versus shredding by each detritivore species. We did this by measuring dry masses (dried at 608C to constant mass, invariably
reached in ,24 h) of litter size-fractions that had
been separated into categories of .10 mm, .5
mm, .1 mm, .500 mm, .100 mm, .50 mm, and
,50 mm by gentle sieving. The smallest fraction,
,50 mm, was confirmed by microscopic examination to be detritivore feces.
Differences in chemical composition (contents
of phenolics, C, and N) of freshly collected and
remnant litter of the largest size fraction, provided
Nitrogen
SS
356800
28500
15980
21390
422700
F
p
1000.7
59.9
11.2
,0.001
,0.001
,0.001
information on the extent to which detritivores
mediated changes in litter quality. These effects
could have occurred either through selective consumption of litter or through direct influences of
detritivores (e.g., fecal amount and composition,
mucus, urine, molt deposition, and so on) on type
and abundance of microbiota. C and N were analyzed in a Carlo Erba NA-1500 NCS Analyzer. Phenolics were determined as ferulic acid equivalents
(simple phenolics), tannic acid equivalents (hydrolyzable tannins), and quebracho equivalents (condensed tannins) as described in Zimmer (2002).
To estimate the digestive capabilities of detritivores feeding on the different litter types, we compared the phenolic, C, and N contents of detritivore feces with those of the initial litter. To determine the impacts of microbiota on litter chemistry,
we compared litter chemistry at the start and end
of the experiment in the detritivore-free mesocosms. To determine impacts of detritivores, we
compared litter chemistry at the end of the experiment (largest size fraction) among control mesocosms and mesocosms containing the different detritivores.
Results
DETRITIVORE PERFORMANCE
The four detritivores ate the four litter types in
a similar rank order: Borrichia $ Juncus $ Spartina
$ Quercus (Fig. 1). They differed in that the mixed
diet was consumed in large amounts by Littoraria
and Armases, but in small amounts by Melampus.
Venezillo ingested intermediate amounts of the
mixed diet. Armases was the only detritivore to gain
mass on every diet (Fig. 2). The other three detritivores either maintained approximately their initial mass or lost mass on most diets. Both consumption and growth clearly depended on the type
of litter available for every detritivore. Differences
in consumption of different litter types were especially evident from mixed-litter diets. Armases
consumed about the same amount of Juncus, Spartina, and Quercus (each c. 20% of the total amount
consumed), but twice as much of Borrichia. Almost
half (45%) of the litter consumed by the snails was
Borrichia, but the species differed in that Littoraria
Redundancy of Detritivores?
761
consumed more of Spartina (36%) than of Juncus
(15%), while Melampus consumed more of Juncus
(33%) than of Spartina (18%). Quercus made up
only 4% of the total food consumed by both Littoraria and Melampus; 11% of the litter consumed
by Venezillo was Quercus, and only little more of Juncus was consumed (13%), while Spartina and Borrichia made up 22% and 54%, respectively, of the
total.
All gastropods survived to the end of the experiment. The two crustacean species had high mortality rates (.75% after 30 d) in Borrichia mesocosms, but survived well on all other diets (Fig. 3).
At the end of the experiment, crawling activity of
Littoraria was significantly lower when snails had
fed on Quercus than on most of the other litter
types; Borrichia was intermediate in that Littoraria
activity on this litter neither differed from Quercus
nor from the other litter types (Fig. 4). Respiration
of Melampus after 30 d did not depend upon the
food source, while Armases respired significantly
more on mixed litter than on any single-species
litter. Feeding on mixed litter also resulted in comparably low C:N body ratios (i.e., high relative N
contents) in all detritivores but Littoraria (Fig. 5).
Besides this general pattern, detritivore species differed in that crustaceans had low C:N ratios when
feeding on Borrichia, while snails had low C:N ratios when feeding on Juncus and, surprisingly, on
Quercus.
Fig. 10. Change in content of three classes of phenolics in
four litter types (Juncus, Spartina, Borrichia, and Quercus) after
30 d incubation in mesocosms as compared with initial values
of the litter (5 100%). Note that no quebracho or quebracho
equivalents were detected in the litter of Juncus and Spartina. C
5 control, L 5 Littoraria irrorata, M 5 Melampus bidentatus, A 5
Armases cinereum, V 5 Venezillo parvus. Initial values for litter are
indicated by dashed lines at 100%; control means that differ
from initial values are indicated with an asterisk above bars. Data
are means 6 1 SD; n 5 9 per litter type per detritivore species;
shared letters indicate no significant differences among treatments for each element within each litter type (ANOVA followed by Tukey test at a 5 0.05). Some analyses were not performed owing to too little material.
DECOMPOSITION PROCESSES
In control mesocosms, litter was essentially not
comminuted, and more than 99% of the litter remained in the largest size fraction after 30 d. No
correction was necessary for nondetritivore-mediated comminution. In the test mesocosms, crustaceans were the most effective shredders relative to
their size, in that they broke down the most litter
material (mg litter produced (mg 3 (detritivore 3
d)21; Fig. 6). The isopods were most effective in
shredding components of the mixed litter, but
shredded relatively little Juncus and Quercus. Comminution of mixed litter by Venezillo was mostly due
to feeding activity on Spartina or Borrichia. Armases
was the next best shredder, causing moderate comminution of Juncus litter, but only little comminution of the other types; shredding of mixed litter
by Armases was intermediate. The gastropods were
the least effective shredders. Shredding activity by
Littoraria was highest on mixed litter and intermediate on Spartina and Quercus. Shredding by Melampus did not differ among litter types, so, overall
comminution of mixed litter represented an average for all litter types.
Detritivores differed remarkably in how thoroughly they shredded the litter, that is, the frac-
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M. Zimmer et al.
TABLE 3. Influence of the litter type and the detritivore species (two-way ANOVA) on the carbon and nitrogen content of feces
after feeding on different litter types.
Litter
Consumer
Interaction
Error
Total
df
Carbon
SS
3
4
12
180
199
5041
123300
72880
8001
209200
F
p
56.7
346.6
204.9
,0.001
,0.001
,0.001
tion-size distribution of comminuted litter differed
among detritivores, and, for each detritivore, this
pattern depended on the litter type (Fig. 7). Melampus was the only detritivore that fragmented
Quercus litter mostly into particles of ,1 mm; the
other detritivores produced Quercus fragments that
mostly were .5 mm. Fragment size of Spartina and
Juncus litter was homogeneously distributed in Littoraria and Armases mesocosms, but was mostly ,1
mm in Melampus mesocosms and .0.5 mm in Venezillo mesocosms. The isopods, as well as Littoraria,
fragmented Borrichia litter to ,1 mm, but size-class
distribution of Borrichia fragments was almost homogeneous in Armases and Melampus mesocosms.
The ability to shred litter was in the order Melampus . Armases . Littoraria . Venezillo. The most
thorough shredder was Melampus on Borrichia,
where almost 90% of the initial litter material was
comminuted. The least thorough shredder was Venezillo on Juncus, where only about 1% was comminuted.
Among detritivores, promotion of microbial respiration correlated negatively with shredding activity. One of the least effective shredder in terms of
the amount of comminuted litter, Melampus, increased microbial respiration over that occurring
in detritivore-free control mesocosms up to 5-fold,
whereas the other detritivores increased microbial
respiration by at most 2-fold (Fig. 8, Table 1).
Among litter types, promotion of microbial respiration did not correlate well with comminution
(for example, respiration was not increased the
most on Borrichia litter nor the least on Quercus
litter), and effects were variable as indicated by a
statistical interaction of the factors litter and consumer in analysis of variance (ANOVA), suggesting
consumer effects that depend upon the handled
litter type.
Microbial decomposition in detritivore-free control mesocosms resulted in significantly reduced N
content and significantly increased C content in
every litter type but Borrichia (Fig. 9). Effects of
detritivores on changes in the chemical composition of litter remnants depended upon both the
detritivore species and the litter type (Fig. 9, Table
2: ANOVA). Armases increased the N content of
every litter relative to detritivore-free control me-
Nitrogen
SS
18500
84210
11730
15160
129600
F
p
109.8
125.1
17.4
,0.001
,0.001
,0.001
socosms, but Littoraria did not significantly affect
the N content of any litter type. Melampus and Venezillo increased the N content of some litters but
not others. Armases also had strong effects on litter
C content, increasing it relative to controls in one
case (Borrichia) and decreasing it in two others
(Juncus, Spartina). The other three detritivores had
no significant effects on C content of any litter
type. The effects of detritivores on litter C and N
content strongly depended on both the detritivore
and the litter type.
Effects of microbial decomposition on litter phenolics in detritivore-free control mesocosms depended upon both phenolic class and litter type
(Fig. 10, considering only the C bars). Clear patterns were obvious in Quercus, with every measured
phenolic being significantly reduced, and in Juncus, where no significant changes occurred. Simple
phenolics were reduced in Spartina, but were not
changed in Borrichia. Hydrolyzable tannins were reduced in Borrichia, but were not changed in Spartina. Condensed tannins in Borrichia were not
changed by microbial decomposition. Changes in
phenolics due to detritivore-mediated effects of microbial activity showed a diverse pattern. Detritivore effects depended upon the phenolic compounds as well as on both the detritivore and the
detritus (Table 3: ANOVA).
With respect to the digestion of C and N compounds and subsequent microbially mediated degradation of detritivore feces, we observed the same
general pattern in every detritivore feeding on a
particular litter type (Fig. 11). With the exception
of a diet of Borrichia, detritivores mostly increased
the N content and decreased the C content relative
to changes in animal-free control mesocosms, producing a statistically significant interaction of detritivore and litter type (Table 4: ANOVA). Even
so, interpretation of the results is difficult; for example, while the N content of feces derived from
Juncus and Spartina increased in comparison with
that of the litter in detritivore-free controls, and
the C content decreased, both the N and C content
of Borrichia decreased during gut passage. Data for
Quercus treatments are incomplete (in many cases,
feces samples were lacking or too small for analyses
Redundancy of Detritivores?
763
of C or N content to be conducted) and do not
aid in our interpretation.
With respect to the digestion of litter phenolics,
we found species-specific differences in how detritivore digestion changed the phenol content from
litter to feces (Fig. 12, Table 5: ANOVA). The relative contents of different phenolics in Juncus increased during the gut passage in almost every detritivore, but did so in the case of Spartina only for
Littoraria and Venezillo. Results for phenolics in Borrichia and Quercus were highly variable depending
on detritivore, plant, and phenolic class. Overall,
no clear patterns in phenolic processing are obvious from our data.
Fig. 11. Change in content of carbon and nitrogen due to
digestive processes by detritivores feeding on four litter types
(Juncus, Spartina, Borrichia, and Quercus) as compared with initial
values of the litter (5 100%). C 5 leaf litter in control mesocosms, L 5 Littoraria irrorata feces, M 5 Melampus bidentatus feces, A 5 Armases cinereum feces, and V 5 Venezillo parvus feces.
Initial values for litter are indicated by dashed lines at 100%;
control means that differ from initial values are indicated with
an asterisk above bars. Data are means 6 1 SD; n 5 9 per litter
type per isopod species; shared letters indicate no significant
differences among treatments for each element within each litter type (ANOVA followed by Tukey test). Some analyses were
not performed owing to too little material.
Discussion
The role of detritivore diversity in decomposition processes has only recently begun to be addressed ( Jonsson and Malmqvist 2000; Cragg and
Bardgett 2001; Crowl et al. 2001; Jonsson et al.
2001; Zimmer et al. 2002), and it is largely unknown to what extent detritivores are functionally
redundant (Wardle 1999). While on a gross level,
detritivores appear to be all redundant, because
they apparently all use the same food source, a
closer look may reveal interspecific differences in
detail in how they use which component of this
food source, eventually resulting in additive or
even synergistic effects of different species of detritivores (e.g., Lawton et al. 1998; Jonsson and
Malmqvist 2000; Duffy et al. 2001; and Zimmer et
al. 2002). Our present results suggest that common
salt marsh detritivores are not completely redundant but contribute to decomposition processes in
terms of comminution, consumption and digestion
of litter material, and promotion of microbial activity in species-specific ways. Different litter types
are not redundant as food sources for marsh detritivores, indicating that detritivores differ in their
nutritive requirements and cannot substitute different food sources for another. Species-specificity
may in part reflect the fact that the detritivores
studied co-occur in southern salt marshes on a
large scale, but inhabit only partially overlapping
zones within a salt marsh on a smaller scale (Zimmer et al. 2002).
According to recent studies of decomposition
processes, different functional groups within the
guild of detritivores would be expected to exhibit
differential effects on overall decomposition
(Bardgett and Chan 1999; Richards et al. 2000;
Crowl et al. 2001), and even members of the same
functional group may not necessarily be redundant
(Zimmer et al. 2002). Jonsson and Malmqvist
(2000) and Duffy et al. (2001) have independently
shown that ecosystem processes may benefit from
species richness even if all species belong to the
764
M. Zimmer et al.
TABLE 4. (A) Influence of the phenolic class and the detritivore species (two-way ANOVA) on changes in phenolic content of
different litter types. (B) Influence of the litter type and the detritivore species (two-way ANOVA) on changes in different phenolics.
A
Spartina
SS
df
Phenolics
Consumer
Interaction
Error
Total
1
4
4
90
99
Phenolics
Consumer
Interaction
Error
Total
8281
224100
69330
141400
443100
df
Borrichia
SS
2
3
6
108
119
246000
275800
179000
126800
827500
p
F
5.3
35.7
11.1
Juncus
SS
df
0.024
,0.001
,0.001
1
4
4
90
99
16640
127500
25450
103900
273500
F
p
df
Quercus
SS
104.8
78.3
25.4
,0.001
,0.001
,0.001
2
4
8
135
149
23240
22850
72420
87310
205800
F
p
14.4
27.6
5.5
0.001
,0.001
0.001
F
p
17.9
8.8
14.1
,0.001
,0.001
,0.001
B
Ferulic Acid
Litter
Consumer
Interaction
Error
Total
Tannic Acid
Quebracho
df
SS
F
p
df
SS
F
p
df
SS
F
p
3
4
12
180
199
166300
139400
266500
219600
791900
45.4
28.6
18.2
,0.001
,0.001
,0.001
3
4
12
180
199
331900
187200
161200
191500
871800
104.0
44.0
12.6
,0.001
,0.001
,0.001
1
4
4
90
99
122500
124100
171300
50950
468800
216.4
54.8
75.6
,0.001
,0.001
,0.001
same functional group. In their study on the impact of changing the diversity and species composition of detritivores on decomposition processes
such as litter mass loss, microbial respiration, and
nutrient fluxes, Cragg and Bardgett (2001) suggested that the composition of a detritivore community, rather than its diversity, is of greatest importance for ecosystem functioning. Bardgett and
Chan (1999) stressed the significance of different
feeding strategies of belowground detritivores in
nutrient cycling and increasing plant productivity.
These differences reduce competition and make
coexistence possible (Hardin 1960; Armstrong and
McGehee 1980; Richards et al. 2000).
Besides species-specific differences in feeding
preferences and feeding rates (Rietsma et al. 1982;
Zimmer et al. 2002), it is likely that members of
the diverse community of salt marsh detritivores
co-exist on a large scale (see above) in part by occupying different habitats (Littoraria favors regularly-flooded low and mid marsh habitats, Melampus
high marsh habitats, and Armases and Venezillo the
terrestrial border of the marsh). Although we did
not directly test for competition among the detritivores in our study, our data indicate that their
different feeding strategies and digestive efficacies
lead to their processing of litter in many different
ways. In combination with different habitat preferences, these different feeding strategies will reduce interspecies competition to a minimum. With
respect to contribution to decomposition processes, salt marsh detritivores are not functionally re-
dundant; their intraguild diversity may actually
benefit ecosystem processes, and the fate of salt
marsh detritus in part depends upon its site of decomposition.
The detritivores in our study responded in a species-specific manner to the offered food sources.
Although there were similar patterns across detritivore species (e.g., consumption rates had similar
rank order across the plant species), both their digestive processes and overall performances differed markedly. The most striking difference was
that Armases gained mass on every litter diet, while
the other detritivores either did not appreciably
change in mass or lost mass on most diets. This is
likely explained by the fact that, in nature, these
organisms eat a variety of food types, including
both detritus and microalgae, and that the more
limited diets presented in the mesocosms were nutritionally inadequate. Some of the species may
feed preferentially on litter from particular parts
of the plants that were not present in the jars—
Littoraria preferentially feeds on leaf blades, not
stems, and prefers leaves that are heavily colonized
with fungi (Newell and Bärlocher 1993; Graça et
al. 2000). Its consumption can have a strong negative impact on living Spartina when it occurs at
high densities (Silliman and Zieman 2001; Silliman
and Bertness 2002; Silliman and Newell 2003). Although we commonly observe Littoraria feeding on
stems in the field, this diet may not, by itself, be
sufficient to sustain growth.
It is surprising that Littoraria and Venezillo lost
Redundancy of Detritivores?
Fig. 12. Change in content of three classes of phenolics due
to digestive processes by detritivores feeding on four litter types
(Juncus, Spartina, Borrichia, and Quercus) as compared with initial
values of the litter (5 100%). Note that no quebracho or quebracho equivalents were detected in the litter of Juncus and Spartina or in feces derived from these litter types. C 5 leaf litter in
control mesocosms, L 5 Littoraria irrorata feces, M 5 Melampus
bidentatus feces, A 5 Armases cinereum feces, and V 5 Venezillo
parvus feces. Initial values for litter are indicated by dashed lines
at 100%; control means that differ from initial values are indicated with an asterisk above bars. Data are means 6 1 SD; n 5
9 per litter type per isopod species; shared letters indicate
765
mass when feeding on the mixed-litter diet while
they gained mass on at least one of the single-litter
diets. The litter type they gained mass on was not
necessarily the one they consumed at highest rate.
Littoraria consumed Borrichia at a high rate but
grew only on Quercus, which it ingested little of.
According to findings by Waldbauer and Friedman
(1991) and Pennings et al. (1993) that suggest that
no single detrital food source may be nutritionally
sufficient if eaten alone and that self-selection of
optimal foods is the norm, we would have expected
the Littoraria to consume what was needed of Quercus from the mixed diet and grow as well on it as
on Quercus alone. Venezillo did not gain mass on the
mixed diet although there was plenty of Spartina
available, and did gain mass on the Spartina-only
diet. One possible explanation for these results is
that decomposition of Borrichia litter released toxic
compounds that negatively affected growth in the
mixed treatments. Pennings et al. (1998) found
that Borrichia leaves contain water-soluble materials
that reduced feeding by Armases. If these compounds were also toxic, this could explain the poor
survival of the crustaceans on the Borrichia diet. We
observed that crustaceans fed only Borrichia tended
to stand on top of the litter, as if they were trying
to avoid contact with the moist bottom of the mesocosm. Crustaceans in other diet treatments tended to hide within the litter at the bases of their
mesocosms. The mixed diet may not have contained enough Borrichia for the compounds to be
lethal, but the compounds could have affected
growth of some consumers. Such effects of Borrichia leachate would be unlikely to occur in the
field, where leached compounds would be rapidly
diluted. In contrast to the other consumers, although Armases had poor survival on the Borrichia
diet, the few crabs that did survive grew very well
(as they did on the mixed diet). Because Armases
is highly omnivorous, and includes in its diet a variety of plants, fungi, and chemically-rich insect larvae (Pennings et al. 1998) and other invertebrates
(Buck et al. 2003) it may be more tolerant of plant
secondary metabolites than Littoraria and Venezillo.
Venezillo had lower C:N ratios (i.e., higher relative N contents) after feeding on mixed diet or on
N-rich Borrichia than on the other litter types. Melampus gained from feeding on a mixed diet in that
the C:N body ratios were higher on single-litter diets. This was not true for Littoraria and Armases, but
even here, our results clearly indicate that the abil←
no significant differences among treatments for each element
within each litter type (ANOVA followed by Tukey test). Some
analyses were not performed owing to too little material.
766
M. Zimmer et al.
TABLE 5. (A) Influence of the phenolic class and the detritivore species (two-way ANOVA) on the phenolic content of feces after
feeding on different litter types. (B) Influence of the litter type and the detritivore species (two-way ANOVA) on different phenolics
in feces after feeding on different litter types.
A
Spartina
SS
df
Phenolics
Consumer
Interaction
Error
Total
1
4
4
90
99
Phenolics
Consumer
Interaction
Error
Total
2209
1693000
128300
287400
2111000
df
Borrichia
SS
2
3
6
108
119
619300
618500
1024000
213600
2476000
Juncus
SS
F
p
0.7
132.6
10.1
0.408
,0.001
,0.001
F
p
df
Quercus
SS
156.6
104.2
86.3
,0.001
,0.001
,0.001
2
4
8
135
149
504900
798500
1174000
387000
2865000
df
1
4
4
90
99
220900
528200
89220
392000
1230000
F
p
50.7
30.3
5.1
,0.001
,0.001
0.001
F
p
88.1
69.6
51.2
,0.001
,0.001
,0.001
B
Ferulic Acid
Phenolics
Consumer
Interaction
Error
Total
Tannic Acid
Quebracho
df
SS
F
p
df
SS
F
p
df
SS
F
p
3
4
12
180
199
1284000
1436000
1225000
642300
4588000
119.9
100.6
28.6
,0.001
,0.001
,0.001
3
4
12
180
199
160600
646700
1856000
457900
3122000
21.1
63.6
60.8
,0.001
,0.001
,0.001
1
4
4
90
99
370900
609200
576200
182500
1739000
182.9
75.1
71.1
,0.001
,0.001
,0.001
ity to incorporate N, being limiting for animals
feeding on plant material (White 1993), into their
biomass depended on the available litter type.
Nutritional requirements of salt marsh detritivores are species-specific, a reflection in the short
term of specific enzymatic and other adaptations,
and in the long term of intraguild resource partitioning. We expect their food sources, i.e., the detritus of different salt marsh plants, not to be equivalent. In a comparison of different marshes, Fell et
al. (1998) did not find any effect of the invading
reed grass, Phragmites australis, on the abundance
of semiterrestrial invertebrate salt marsh detritivores (including snails and isopods); they did not
study feeding by these detritivores. Angradi et al.
(2001) found fewer macroinvertebrates in Phragmites litter than in Spartina litter, and suggested differences in the quality of the litter as a possible
explanations. Rietsma et al. (1982) found that
feeding preferences of different salt marsh detritivores was not related to the abundance of food.
These detritivores, including Melampus, a Littoraria
and an isopod, differed in their feeding preferences, but clearly responded to similar feeding cues
represented by N content (Bärlocher and Newell
1993; White 1993), content of phenolic compounds (Valiela and Rietsma 1984; Bärlocher and
Newell 1993), and biomass of microbial litter colonizers (Bärlocher et al. 1989; Newell and Bärlocher 1993; Graça et al. 2000). We conclude that the
litter of different plant species cannot be regarded
as redundant as food for salt marsh detritivores.
Based on density ranges given in the literature
(Teal 1962; Fell et al. 1991; Bärlocher and Newell
1994b; Zimmer et al. 2002) and on our own observations on consumption of different litter types,
we have estimated the potential contribution of the
four detritivores used in the present study to overall mass loss of salt marsh litter (Table 6). Due to
its high density in the field (up to 600 m22: Bärlocher and Newell 1994b), Littoraria would be expected to contribute most strongly to disappearance of litter of all types. According to values of
Spartina biomass production presented by Kemp et
al. (1990), our estimated consumption of 550 g
Spartina litter per square meter per year [(m2 3
a)21] by the four detritivore species we tested
would equal about 20% of the annual biomass production. Because our data are based on consumption of Spartina stems, which are much less palatable than the softer, thinner leaves (Newell and
Bärlocher 1993; Graça et al. 2000), consumption
of Spartina litter even by Littoraria alone would likely greatly exceed our estimates [notwithstanding
Kemp et al.’s (1990) Littoraria-consumption data of
360–720 g 3 (m2 a)21 in the field that are similar
to the results of the present study]. Based on daily
consumption rates in the laboratory presented by
Graça et al. (2000) and field densities presented in
Table 6, Littoraria theoretically has the potential to
consume more than 3 kg 3 (m2 3 a)21 of Spartina
leaf litter. We also observed potential consumption
rates of more than 1.3 kg Borrichia litter 3 (m2 3
a)21 by Littoraria in their mesocosms. In the field,
Redundancy of Detritivores?
767
TABLE 6. Potential contributions of detritivores to consumption and comminution of plant litter in salt marshes [g 3 (m2 a)21] as
estimated from the present results and average density data from the literature (300 Littoraria m22, 100 Melampus m22; 10 Armases
m22; 60 Venezillo m22; for references, see text).
Consumption,
g (m2 a)21
Littoraria irrorata
Melampus bidentatus
Armases cinereum
Venezillo parvus
Comminution,
g (m2 a)21
Littoraria irrorata
Melampus bidentatus
Armases cinereum
Venezillo parvus
Juncus
800
50
40
5
Juncus
100
20
30
1
Littoraria is unlikely to gain access to these large
amounts of Borrichia litter because it mostly occurs
at lower levels in the intertidal zone than does Borrichia. Although Littoraria would theoretically be
able to ingest about 125 g (dry mass) 3 (m2 3 a)21
of Quercus litter, the probability of encountering
this type of litter, too, is relatively low in the field.
For these high-intertidal region and marsh-fringing litter types, crustacean detritivores may be
more important with respect to litter consumption
and comminution. Our mesocosm data suggest
that Armases would consume much smaller
amounts of the four litter types in the field than
Littoraria [about 40 g 3 (m2 3 a)21]. While litter
processing is monopolized by the sesarmid crab,
Gecarcoidea natalis, removing 39–87% of the annual
leaf fall in the tropical rain forest of the Christmas
Islands (Green et al. 1999), and sesarmid crabs in
mangroves in Peninsula Malaysia contribute significantly to leaf litter removal (Ashton 2002), mangrove leaf litter (Avicennia marina) seems to be of
insufficient quality to fulfill the N requirements of
other sesarmids, Neosarmatium meinerti and Sesarma
guttatum, and their natural diets consists by less
than 10% of leaf litter (Skov and Hartnoll 2002).
Since the omnivorous Armases is also known to prey
upon snails and small crustaceans (Buck et al.
2003), its importance in the salt marsh ecosystem
may be mainly in its intertrophic mediating influence on decomposition. It has the potential to
more broadly influence decomposition processes,
and energy and nutrient fluxes, than any of the
other detritivores. Because Armases is far more motile than the other detritivores, it probably has
quicker access to new or isolated patches of litter
that would be colonized more slowly, if at all, by
other detritivores. According to our estimates (Table 6), the isopod Venezillo provides little contribution to decomposition in terms of litter consumption. This small but abundant species (Zimmer et al. 2002) may be important through its pro-
Spartina
500
25
20
5
Spartina
150
30
10
2
Borrichia
Quercus
1500
50
30
60
100
20
20
2
Borrichia
Quercus
100
30
15
2
150
20
10
1
motion of microbial activity on a range of litter
types, through its interchanging of nutrients and
energy between coast-forest and salt marsh habitats, and through its capabilities of digesting diverse phenolic litter compounds (present study;
Zimmer et al. 2002). Venezillo is also a potential
prey species of Armases (Buck et al. 2003), further
increasing its potential role in energy and nutrient
fluxes between terrestrial and salt marsh habitats.
Direct contribution by the snail Melampus to litter
disappearance through feeding, as based on average densities of about 100 m22 (Table 6), is similar
to that by Armases. Although at some sites in northern salt marshes densities of more than 1,200 ind
m22 have been observed (Fell et al. 1982), the ecosystem significance of this detritivore at Sapelo Island appears to be in its high contribution to litter
comminution and promotion of microbial activity
(see Figs. 6 and 7) rather than in its overall consumption of litter.
Considering only one litter type or one detritivore species by studying only some of the parameters of decomposition processes we studied would
not have enabled us to paint as clear a picture of
different functions of different detritivores feeding
on different litter types as we did here. Understanding decomposition processes in the high
marsh zones where Littoraria is least abundant
(Pennings unpublished data), and understanding
how materials in the detritivore food web move
back and forth from marine to terrestrial habitats,
may require examining a variety of detritivores and
a variety of detrital food sources. Both Littoraria
and Armases are absent in northern U.S. salt marshes, while Melampus and Venezillo are abundant in
northern and, to a lesser degree, in southern salt
marshes (Pennings unpublished data). Studies on
solely Littoraria will not provide information of decomposition in northeastern U.S. salt marshes.
Our conclusions presented here, however, are
based on the result of mesocosm studies, and con-
768
M. Zimmer et al.
sequently have a variety of attendant potential artifacts; the high mortality of consumers feeding on
Borrichia litter was an artifact that would likely not
have happened in the field. It is also hard to deduce specific effects of these species on ecosystem
processes in the field from laboratory experiments
using single-species assays. Redundancy in terms of
such effects can experimentally be tested best by
successively adding or removing species to or from
a given system. The present results provide insight
into what the species tested here are able to contribute to decomposition processes in salt marshes,
but these contributions might change as soon as
other species are present, too. Due to character
displacement, it is unlikely that species that differ
in what they do, and how they respond, to different
food sources become more alike when they co-occur than when they act alone. Species-specificity as
presented here can be taken as a hint on functional diversity of the tested detritivores under natural
conditions. Our results need to be confirmed and
extended by in situ studies of the various detritivore-litter combinations in their natural habitats.
ACKNOWLEDGMENTS
We are grateful for financial support provided by the University of Georgia Marine Institute Visiting Scientist Program (M.
Zimmer), the U.S. National Science Foundation (DEB 0296160,
S. C. Pennings; OCE 99-82133, T. L. Buck, S. C. Pennings) and
the Natural Sciences and Engineering Research Council of Canada (T. H. Carefoot). This is contribution 2000-3 of the International Isopod Research Group (IIRG), and contribution # 934
of the University of Georgia Marine Institute.
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Received, January 27, 2004
Revised, April 23, 2004
Accepted, April 30, 2004