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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). 755 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). 756 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). 758 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. 760 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- 762 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. LITERATURE CITED ANGRADI, T. R., S. M. HAGAN, AND K. W. ABLE. 2001. Vegetation type and the intertidal macroinvertebrate fauna of a brackish marsh: Phragmites vs. Spartina. Wetlands 21:75–92. ARMSTRONG, R. A. AND R. MCGEHEE. 1980. Competitive exclusion. The American Naturalist 115:151–170. ARSUFFI, T. L. AND K. SUBERKROPP. 1989. Selective feeding by shredders on leaf-colonizing stream fungi: Comparison of macroinvertebrate taxa. Oecologia 79:30–37. ASHTON, E. C. 2002. Mangrove sesarmid crab feeding experiments in Peninsular Malaysia. Journal of Experimental Marine Biology and Ecology 273:97–119. BARDGETT, R. D. AND K. F. CHAN. 1999. Experimental evidence that soil fauna enhance nutrient mineralization and plant nutrient uptake in montane grassland ecosystems. Soil Biology and Biochemistry 31:1007–1014. BÄRLOCHER, F. AND S. Y. NEWELL. 1993. Removal of fungal and total organic matter from decaying cordgrass leaves by shredder snails. Journal of Experimental Marine Biology and Ecology 171:39–49. BÄRLOCHER, F. AND S. Y. NEWELL. 1994a. Growth of the saltmarsh periwinkle Littoraria irrorata on fungal and cordgrass diets. Marine Biology 118:109–114. BÄRLOCHER, F. AND S. Y. NEWELL. 1994b. Phenolics and proteins affecting palatability of Spartina leaves to the gastropod Littoraria irrorata. Marine Ecology 15:65–75. BÄRLOCHER, F., S. Y. NEWELL, AND T. L. ARSUFFI. 1989. Digestion of Spartina alterniflora Loisel material with and without fungal constituents by the periwinkle Littoraria irrorata Say (Mollusca: Gastropoda). Journal of Experimental Marine Biology and Ecology 130:45–53. BERTNESS, M. D. 1999. The Ecology of Atlantic Shorelines. Sinauer Associates, Inc., Sunderland, Massachusetts. BERTNESS, M. D. AND A. M. ELLISON. 1987. Determinants of pattern in a New England salt marsh plant community. Ecological Monographs 57:129–147. BUCK, T. L., G. A. BREED, S. C. PENNINGS, M. E. CHASE, M. ZIMMER, AND T. H. CAREFOOT. 2003. Diet choice in an omnivorous salt marsh crab: Different food types, crab allometry, and habitat complexity. Journal of Experimental Marine Biology and Ecology 292:103–116. CHALCRAFT, D. R. AND W. J. RESETARITS. 2003a. Mapping functional similarity of predators on the basis of trait similarity. The American Naturalist 162:390–402. CHALCRAFT, D. R. AND W. J. RESETARITS. 2003b. Predator identity and ecological impacts: Functional redundancy or functional diversity? Ecology 84:2407–2418. CONN, C. AND J. DIGHTON. 2000. Litter quality influences on decomposition, ectomycorrhizal community structure and mycorrhizal root surface acid phosphatase activity. Soil Biology and Biochemistry 32:489–496. COVI, M. P. AND R. T. KNEIB. 1995. Intertidal distribution, population dynamics and production of the amphipod Uhlorchestia spartinophila in a Georgia, USA, salt marsh. Marine Biology 121:447–455. CRAGG, R. G. AND R. D. BARDGETT. 2001. How changes in soil faunal diversity and composition within a trophic group influence decomposition processes. Soil Biology and Biochemistry 33: 2073–2081. CROWL, T. A., W. H. MCDOWELL, A. P. COVICH, AND S. L. JOHNSON. 2001. Freshwater shrimp effects on detrital processing and nutrients in a tropical headwater stream. Ecology 82:775–783. DUFFY, J. E., K. S. MACDONALD, J. M. RHODE, AND J. D. PARKER. 2001. Grazer diversity, functional redundancy, and productivity in seagrass beds: An experimental test. Ecology 82:2417–2434. FACELLI, J. M. AND S. T. A. PICKETT. 1991. Plant litter: Its dynamics and effects on plant community structure. Botanical Reviews 57:1–32. FELL, E. P., K. A. MURPHY, M. A. PECK, AND M. L. RECCHIA. 1991. Re-establishment of Melampus bidentatus and other macroinvertebrates on a restored impounded tidal marsh: Comparison of population above and below the impoundment dike. Journal of Experimental Marine Biology and Ecology 15:33–48. FELL, E. P., N. C. OLMSTEAD, E. CARLSON, W. JACOB, D. HITCHCOCK, AND G. SILBER. 1982. Distribution and abundance of macroinvertebrates on certain Connecticut tidal marshes, with emphasis on dominant molluscs. Estuaries 5:235–239. FELL, E. P., S. P. WEISSBACH, D. A. JONES, M. A. FALLON, J. A. ZEPPIERI, E. K. FAISON, K. A. LENNON, K. J. NEWBERRY, AND L. K. REDDINGTON. 1998. Does invasion of oligohaline marshes by reed grass, Phragmites australis (Cav.) Trin. ex Steud., affect availability of prey resources for the mummichog, Fundulus heteroclitus L.? Journal of Experimental Marine Biology and Ecology 222:59–77. GRAÇA, M. A. S., L. MALTBY, AND P. CALOW. 1993. Importance of fungi in the diet of Gammarus pulex and Asellus aquaticus I. feeding strategies. Oecologia 93:139–144. GRAÇA, M. A. S., S. Y. NEWELL, AND R. T. KNEIB. 2000. Grazing rates of organic matter and living fungal biomass of decaying Spartina alterniflora by three species of salt marsh invertebrates. Marine Biology 136:281–289. GREEN, P. T., P. S. LAKE, AND D. J. O’DOWD. 1999. Monopolization of litter processing by a dominant land crab on a tropical oceanic island. Oecologia 119:435–444. GRIFFITHS, B. S., K. RITZ, R. D. BARDGETT, R. COOK, S. CHRISTENSEN, F. EKELUND, S. J. SøRENSEN, E. BÅÅTH, J. BLOEM, P. C. DE RUITER, J. DOLFING, AND B. NICOLARDOT. 2000. Ecosystem response of pasture soil communities to fumigation-induced Redundancy of Detritivores? microbial diversity reductions: An examination of the biodiversity-ecosystem function relationship. Oikos 90:279–294. HARDIN, G. 1960. The competitive exclusion principle. Science 131:1292–1298. JONSSON, M. AND B. MALMQVIST. 2000. Ecosystem process rate increases with animal species richness: Evidence from leafeating, aquatic insects. Oikos 89:519–523. JONSSON, M., B. MALMQVIST, AND P.-O. HOFFSTEIN. 2001. Leaf litter breakdown rates in boreal streams: Does shredder species richness matter? Freshwater Biology 46:161–171. KANEKO, N. AND E. SALAMANCA. 1999. Mixed leaf litter effects on decomposition rates and soil microarthropod communities in an oak-pine stand in Japan. Ecological Research 14:131–138. KAUTZ, G. AND W. TOPP. 1998. Nachhaltige waldbauliche Maßnahmen zur Verbesserung der Bodenqualität. -Forstwissenschaftliches Centralblatt 117:23–43. KEMP, P. F., S. Y. NEWELL, AND C. S. HOPKINSON. 1990. Importance of grazing on the salt marsh grass Spartina alterniflora to nitrogen turnover in a macrofaunal detritivore, Littorina irrorata, and to decomposition of standing-dead Spartina. Marine Biology 104:311–319. KNEIB, R. T., S. Y. NEWELL, AND E. T. HERMENO. 1997. Survival, growth and reproduction of the saltmarsh amphipod Uhlorchestia spartinophila reared on natural diets of senescent and dead Spartina alterniflora leaves. Marine Biology 128:423–431. LAWTON, J. H., S. NAEEM, L. J. THOMPSON, A. HECTOR, AND M. J. CRAWLEY. 1998. Biodiversity and ecosystem function: Getting the Ecotron experiment in its correct context. Functional Ecology 12:848–852. MOTULSKY, H. 1995. Intuitive Biostatistics. Oxford University Press, New York. NEWELL, S. Y. 1993. Decomposition of shoots of a salt marsh grass. Advances in Microbial Ecology 13:301–326. NEWELL, S. Y. 1996. Established and potential impacts of eukaryotic mycelial decomposers in marine/terrestrial ecotones. Journal of Experimental Marine Biology and Ecology 200:187–206. NEWELL, S. Y. AND F. BÄRLOCHER. 1993. Removal of fungal and total organic material from decaying cordgrass leaves by shredder snails. Journal of Experimental Marine Biology and Ecology 171:39–49. NEWELL, S. Y., R. D. FALLON, R. M. CAL RODRIGUEZ, AND L. C. GROENE. 1985. Influence of rain, tidal wetting and relative humidity on release of carbon dioxide by standing-dead salt marsh plants. Oecologia 68:73–79. NIXON, S. W. AND C. A. OVIATT. 1973. Ecology of a New England salt marsh. Ecological Monographs 43:463–498. PENNINGS, S. C. AND M. D. BERTNESS. 2001. Salt marsh communities, p. 289–316. In M. D. Bertness, S. D. Gaines, and M. E. Hay (eds.), Marine Community Ecology. Sinauer Associates, Sunderland, Massachusetts. PENNINGS, S. C., T. H. CAREFOOT, E. L. SISKA, M. E. CHASE, AND T. A. PAGE. 1998. Feeding preferences of a generalist saltmarsh crab: Relative importance of multiple plant traits. Ecology 79:1968–1979. PENNINGS, S. C. AND D. J. MOORE. 2001. Zonation of shrubs in western Atlantic salt marshes. Oecologia 126:587–594. PENNINGS, S. C., M. T. NADEAU, AND V. J. PAUL. 1993. Selectivity and growth of the generalist herbivore Dolabella auricularia feeding upon complementary resources. Ecology 74:879–890. RAY, S. AND M. STRAŠKRABA. 2001. The impact of detritivorous fishes on a mangrove estuarine system. Ecological Modelling 140:207–218. RICHARDS, S. A., R. M. NISBET, W. G. WILSON, AND H. P. POSSINGHAM. 2000. Grazers and diggers: Exploitation competition and coexistence among foragers with different feeding strategies on a single resource. The American Naturalist 155:266–279. RIETSMA, C. S., I. VALIELA, AND R. BUCHSBAUM. 1988. Detrital chemistry, growth, and food choice in the salt-marsh snail (Melampus bidentatus). Ecology 69:261–266. 769 RIETSMA, C. S., I. VALIELA, AND A. SYLVESTER-SERIANNI. 1982. Food preferences of dominant salt marsh herbivores and detritivores. Marine Ecology 3:179–189. SILLIMAN, B. R. AND M. D. BERTNESS. 2002. A trophic cascade regulates salt marsh primary production. Proceedings of the National Academy of Sciences 99:10500–10505. SILLIMAN, B. R. AND S. Y. NEWELL. 2003. Fungal farming in a snail. Proceedings of the National Academy of Sciences 100:15643–15648. SILLIMAN, B. R. AND J. C. ZIEMAN. 2001. Top-down control of Spartina alterniflora production by periwinkle grazing in a Virginia salt marsh. Ecology 82:2830–2845. SKOV, M. W. AND R. G. HARTNOLL. 2002. Paradoxical selective feeding on a low-nutrient diet: Why do mangrove crabs eat leaves? Oecologia 131:1–7. SMALLEY, A. E. 1960. Energy flow of a salt marsh grasshopper population. Ecology 41:785–790. SULKAVA, P. AND V. HUHTA. 1998. Habitat patchiness affects decomposition and faunal diversity: A microcosm experiment on forest floor. Oecologia 116:390–396. SULKAVA, P., V. HUHTA, J. LAAKSO, AND E.-R. GYLÉN. 2001. Influence of soil fauna and habitat patchiness on plant (Betula pendula) growth and carbon dynamics in a microcosm experiment. Oecologia 129:133–138. TAITI, S. AND F. FERRARA. 1991. Terrestrial isopods (Crustacea) from the Hawaiian Islands. Bishop Museum Occasional Papers 31:202–227. TEAL, J. M. 1962. Energy flow in the saltmarsh ecosystem of Georgia. Ecology 43:614–624. VALIELA, I. AND C. S. RIETSMA. 1984. Nitrogen, phenolic acids, and other feeding cues for salt marsh detritivores. Oecologia 63:350–356. VALIELA, I. AND J. M. TEAL. 1979. Inputs, outputs and interconversions of nitrogen in a salt marsh ecosystem, p. 399–414. In R. L. Jefferies and A. J. Davy (eds.), Ecological Processes in Coastal Environments. Blackwell Scientific Publications, Oxford. U.K. VALIELA, I., J. WILSON, R. BUCHSBAUM, C. RIETSMA, D. BRYANT, K. FOREMAN, AND J. TEAL. 1984. Importance of chemical composition of salt marsh litter on decay rates and feeding by detritivores. Bulletin of Marine Science 35:261–269. WALDBAUER, G. P. AND S. FRIEDMAN. 1991. Self-selection of optimal diets by insects. Annual Review of Entomology 36:43–63. WARDLE, D. A. 1999. How soil food webs make plants grow. Trends in Ecology and Evolution 14:418–420. WHITE, T. C. R. 1993. The inadequate environment: Nitrogen and the abundance of animals. Springer, Berlin. WIEGERT, R. G. AND B. J. FREEMAN. 1990. Tidal salt marshes of the southeast Atlantic coast: A community profile. U.S. Department of the Interior, Fish and Wildlife Service, Biological Report 85(7.29). Washington, D.C. WOOD, T. G. 1974. Field investigations on the decomposition of leaves of Eucalyptus delegatensis in relation to environmental factors. Pedobiologia 14:343–371. ZIMMER, M. 2002. Is decomposition of woodland leaf litter influenced by its species richness? Soil Biology and Biochemistry 34: 277–284. ZIMMER, M., S. C. PENNINGS, T. L. BUCK, AND T. H. CAREFOOT. 2002. Species-specific patterns of litter processing by terrestrial isopods (Isopoda: Oniscidea) in high intertidal salt marshes and coastal forests. Functional Ecology 16:596–607. ZIMMER, M. AND W. TOPP. 1999. Relations between woodlice (Isopoda: Oniscidea), and microbial density and activity in the field. Biology and Fertility of Soils 30:117–123. ZIMMER, M. AND W. TOPP. 2000. Species-specific utilization of food sources by sympatric woodlice (Isopoda: Oniscidea). Journal of Animal Ecology 69:1071–1082. Received, January 27, 2004 Revised, April 23, 2004 Accepted, April 30, 2004