Salt Marsh Litter and Detritivores: a Closer Look at Redundancy

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-Universita¨t, 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.

Introduction of biodiversity, it is likely that functional redundan- Although the potential significance of species di- cy increases ecosystem stability (resistance to and versity in ecosystem maintenance has been the top- resilience from disturbance; e.g., Griffiths et al. ic of many ecological studies, this aspect of biodi- 2000). With respect to ecosystem functioning in versity has been addressed relatively rarely in stud- terms of particular processes, functional redundan- ies of decomposition processes. Studies of decom- cy may have little effect, owing to competitive in- position that do consider the significance of teractions between functionally redundant organ- detritivore diversity mostly conclude that species isms. Coexisting detritivores are usually found to diversity promotes ecosystem decomposition pro- differ in terms of feeding strategies, nutritional re- cesses (Sulkava and Huhta 1998; Zimmer and quirements, and digestive capabilities in both Topp 1999; Jonsson and Malmqvist 2000; Jonsson aquatic (Arsuffi and Suberkropp 1989; Graça et al. et al. 2001; Crowl et al. 2001). In addition to this 1993; Ray and Strasˇkraba 2001) and terrestrial top-down effect of diversity on decomposition pro- (Bardgett and Chan 1999; Zimmer and Topp 2000; cesses, there may also be a bottom-up effect in that Zimmer et al. 2002) ecosystems. It is these differ- plant litter diversity seems to affect both the rate ences that reduce competition and make coexis- of litter decomposition (Kautz and Topp 1998; Ka- tence possible (competitive exclusion principle: neko and Salamanca 1999; Conn and Dighton Hardin 1960; Armstrong and McGehee 1980; Rich- 2000; Zimmer 2002) and the rate of colonization ards et al. 2000), but the differences are also sig- by litter microbes (Sulkava et al. 2001), as well as nificant with respect to the species’ effects on eco- the relative significance of detritivores in the ecosystem processes (Zimmer and Topp 1999; Rich- system (Sulkava and Huhta 1998). A pressing as- ards et al. 2000; Cragg and Bardgett 2001; Zimmer pect of our current interest in biodiversity is un- et al. 2002). By definition members of the same derstanding the extent to which different species guild that differ in the way they use available food in the same guild are functionally redundant or sources cannot be considered redundant and may diverse (Chalcraft and Resetarits 2003a,b). even have additive or synergistic effects on ecosys- From what we know about the ecosystem effects tem functioning (Lawton et al. 1998; Jonsson and Malmqvist 2000; Duffy et al. 2001; Zimmer et al. * Corresponding author; tele: ϩ49/431/880-4153; fax: ϩ49/ 2002). High within-guild biodiversity may promote 431/880-4368; e-mail: [email protected] ecosystem processes, such as decomposition, if † Current address: Department of Biology and Biochemistry, functional redundancy in terms of detritivores’ University of Houston, Houston, Texas 77204-5001. ‡ Current address: North Inlet-Winyah Bay NERR, Baruch contributions to decomposition processes is low. Marine Laboratory, P.O. Box 1630, Georgetown, South Carolina In contrast to other intertidal habitats where de- 29442. tritus is either accumulated above the uppermost

ᮊ 2004 Estuarine Research Federation 753 754 M. Zimmer et al. tidal level or washed away through wave action, de- functionally redundant in terms of contributions tritus from angiosperms in salt marshes accumu- to decomposition processes or in serving as food lates in the dense vegetation. Energy flux from pri- for detritivores, respectively. We tested three hy- mary producers in these systems is thought to be potheses: syntopic detritivores in salt marshes dif- largely detritus-based (Smalley 1960; Teal 1962; fer with respect to their nutritional requirements Nixon and Oviatt 1973; Valiela and Teal 1979; Sil- and digestive capabilities, syntopic plants differ liman and Zieman 2001). Because salt marshes are with respect to litter quality as food for detritivores, dominated by plants of terrestrial origin (angio- and syntopic detritivores in salt marshes exhibit sperms), but contain animals of primarily marine differential effects on decomposition processes of origin (e.g., snails and crabs) many of which act as different plants, so neither detritivores nor plants detritivores (Ba¨rlocher et al. 1989; Kemp et al. are functionally redundant. While many studies on 1990; Ba¨rlocher and Newell 1994; Kneib et al. functional redundancy of consumers have created 1997; Graça et al. 2000) or omnivores (Buck et al. different diversity levels by excluding or including 2003), they provide an evolutionary and ecological different combinations of animals ( Jonsson and link between marine and terrestrial systems. Onis- Malmqvist 2000; Duffy et al. 2001), we took an al- cidean isopods are among the few terrestrial inver- ternate approach of examining each species’ ef- tebrates that invade salt marshes as detritivores that fects on decomposition processes in single-species feed on both littoral and supralittoral plant debris mesocosm experiments, since we were interested (Rietsma et al. 1982; Valiela and Rietsma 1984; in single-species effects and capabilities rather than Zimmer et al. 2002), increasing within-guild diver- the effects of different consumer combinations. sity of detritivores. Some consumer combinations in mesocosms were Decomposition of plant litter can be described impossible due to both species-specific environ- in terms of litter mass-loss that is due to feeding mental requirements and predator-prey interac- and digestion by detritivorous animals (detriti- tions (Buck et al. 2003). We stocked different me- vores) and microbiota, resulting in the mechanical socosms with different litter types to elucidate dif- breakdown and fragmentation of litter particles ferential effects of litter type on the detritivores. (comminution) and the egestion of surface-increased feces by shredders, and in changes in the Material and Methods chemical composition of the litter (degradation) Experiments were conducted at the Marine In- and the egestion of partially digested litter material stitute of the University of Georgia, at Sapelo Is- in feces. In both terrestrial systems (e.g., Wood land, Georgia, United States (31Њ27ЈN, 81Њ15ЈW), 1974; Facelli and Picket 1991; Zimmer 2002) and during March and April 2000. For our experi- intertidal salt marshes (Ba¨rlocher et al. 1989; ments, we used four detritivores and four angio- Kemp et al. 1990; Newell and Ba¨rlocher 1993; New- sperms common in high intertidal salt marshes ell 1996; Graça et al. 2000), decomposition pro- around the island. The detritivores were the peri- cesses of plant litter are controlled by comminu- winkle Littoraria irrorata (Gastropoda: Prosobran- tion through detritivore shredding and feeding, di- chia), the coffee-bean snail Melampus bidentatus gestive processes of detritivores, and detritivore- (Gastropoda: Pulmonata), the wharf crab Armases mediated activity of litter-processing microbiota. cinereum (Crustacea: Decapoda), and the coastal Intuitively implying that both detritivores and de- pillbug Venezillo parvus (V. evergladensis cf., Taiti and tritus are likely redundant (cf., Wardle 1999), and Ferrara 1991; Crustacea: Isopoda). The plants used despite the variety of plants that occur in salt as food for the detritivores were the smooth cord- marshes and the variety of potential detritivores, grass Spartina alterniflora, the black needlerush Jun- most studies of detritivoral processes in eastern cus roemerianus, the sea daisy Borrichia frutescens, North American coastal salt marshes have focused and the live oak Quercus virginiana. S. alterniflora is on the most abundant detritivore in southern the most common salt marsh plant along the At- marshes, the gastropod Littoraria irrorata, and its lantic coast of the U.S., dominating large areas of most important source of litter, the grass Spartina the low and middle marsh elevations (Bertness alterniflora; less is known about other detritivores 1999; Pennings and Bertness 2001). J. roemerianus and litter sources (Rietsma et al. 1982; Valiela and is the second most common salt marsh plant at Rietsma 1984; Kneib et al. 1997; Graça et al. 2000). southeastern sites, dominating the high marsh Most studies on salt marsh decomposition have fo- (Wiegert and Freeman 1990). Both S. alterniflora cused only on feeding and growth of detritivores, and J. roemerianus produce large amounts of litter or mass loss of litter. that accumulates in patches in the high marsh We have chosen to study four invertebrate detri- (Bertness and Ellison 1987; authors’ personal ob- tivores and the litter of four angiosperms, with the servations). B. frutescens is common in the high goal of determining whether these species are marsh, forming zones several meters wide at many Redundancy of Detritivores? 755

Fig. 1. Relative consumption rates (RCR) of detritivores Fig. 2. Relative growth rates (RGR) of detritivores feeding feeding on four different litter types or a mixture of these litter on four different litter types or a mixture of these litter types. types. Littoraria irrorata, Melampus bidentatus, Armases cinereum, Littoraria irrorata, Melampus bidentatus, Armases cinereum, and Ve- ϫ and Venezillo parvus. RCR is defined as dry g eaten [dry g nezillo parvus. RGR is defined as dry g mass gain ϫ (dry g initial ϫ Ϫ1 Ϯ body mass (including shells) d] . Data are means 1 SD; mass ϫ d)Ϫ1. Data are means Ϯ 1 SD; n ϭ 10 per litter type per ϭ n 10 per litter type per detritivore species; p values for one- detritivore species; p values for one-way ANOVAs are indicated way ANOVAs are indicated above bars; shared letters indicate above bars; shared letters indicate no significant differences ␣ϭ no significant differences among litter types (Tukey test at among litter types (Tukey test ␣ϭ0.05). 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 (Ϯ 95% CI) for fractional survival at any particular time. Armases cinereum and Venezillo parvus. Shared letters indicate no signiﬁcant differences among litter types (pair- wise Mantel-Haenszel tests at ␣ϭ0.05).

sites, and drops its leaves into the high marsh (Pen- Fig. 4. Crawling activity of Littoraria irrorata and respiration nings and Moore 2001). Q. virginiana is one of the of Melampus bidentatus and Armases cinereum after having fed on most common marsh-side trees in the southeastern four different litter types or a mixture of these litter types for U.S., and drops large amounts of litter directly into 30 d. Data are means Ϯ 1 SD; n ϭ 10 per litter type per detritivore species; p values for one-way ANOVAs are indicated above high marsh habitats (authors’ personal observa- bars; shared letters indicate no significant differences among tions). All species will be referred to by genus litter types (Tukey test ␣ϭ0.05). names. In mesocosm experiments, detritivores were housed individually in 1,000 ml (Armases) or 500 calculated using the Kaplan-Meier method. Surviv- ml (Littoraria) glass jars, or in groups of 4 (Melam- al curves plot percentage survival as a function of pus)or6(Venezillo) in 100 ml plastic jars, at am- time and 95% confidence interval for fractional bient temperature (20 Ϯ 2ЊC) and light conditions survival at any particular time. Pair-wise compari- (13 h light:11 h dark). By pooling individuals of son of survival curves were performed with Mantel- the smaller detritivore species, we standardized at Haenszel tests (log-rank test for two samples: Mo- least partially for size without risking measurement tulsky 1995). Detritivore biomass at the start of the error by offering very small amounts of food. One experiment was measured on a fresh mass basis potential problem with this design, intraspecific and later converted to dry mass through fresh competition, was circumvented by providing food mass:dry mass ratios (after drying to constant mass in excess. Mesocosms were opened every 2 d to at 60ЊC; n ϭ 10 for each species). allow air exchange and to add deionized water as We collected plant litter as follows: Spartina and needed according to weight loss of litter as deter- Juncus as fallen dead stems and leaves, respectively, mined in pre-experiments. Detritivore mortality that had accumulated in clumps (wrack) in the was recorded every 2 d, and survival curves were high intertidal zone, and Borrichia and Quercus as Redundancy of Detritivores? 757

Fig. 5. C:N ratios of detritivores, Littoraria irrorata (soft bod- Fig. 6. Comminution rate of four different litter types ies, without shells) Melampus bidentatus (whole bodies, including alone and in mixture by detritivores in relation to their bio- shells); Armases cinereum (whole bodies) and Venezillo parvus mass. Littoraria irrorata, Melampus bidentatus, Armases cinereum, (whole bodies) after having fed on four different litter types or and Venezillo parvus. Data are means Ϯ 1 SD; n ϭ 10 per litter a mixture of these litter types for 30 d. Data are means Ϯ 1 SD; type per detritivore species; p values for one-way ANOVAs are overall significance (one-way ANOVA) is indicated above bars; indicated above bars; shared letters indicate no significant shared letters indicate no significant differences among litter differences among litter types (Tukey test at ␣ϭ0.05). types (Tukey test at ␣ϭ0.05). 758 M. Zimmer et al.

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 (ϭ 100%). For the calculation of percent values, controls and treatments were random-paired. Littoraria Fig. 7. Fraction-size distribution of four different litter types irrorata, Melampus bidentatus, Armases cinereum, and Venezillo par- after comminution by detritivores. Littoraria irrorata, Melampus vus. Values for control mesocosms are indicated by dashed lines bidentatus, Armases cinereum, and Venezillo parvus. Data are means at 100%. Data are means Ϯ 1 SD; n ϭ 9 per litter type per of percent values; n ϭ 10 per litter type per detritivore species. detritivore species. Means that differ significantly from controls (ANOVA, ␣ϭ0.05) 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 ␣ϭ0.05). Redundancy of Detritivores? 759

TABLE 1. Inﬂuence of the litter type and the detritivore species (two-way ANOVA) on microbial respiration.

df SS F p Litter 4 14 3.1 0.019 Consumer 3 142 39.5 Ͻ0.001 Interaction 12 65 4.5 Ͻ0.001 Error 180 216 Total 199 437

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: Lit- toraria 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 ϭ 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 ϭ 10 per detritivore) to study the effect of litter diversity on detritivore- mediated 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 ϭ 10 for each detritivore-litter combination). Litter dry mass was determined based on fresh mass:dry mass ratios (n ϭ 20 per plant species). With four species of detritivores, five litter treatments (four species ϩ 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 re- vealed information on litter-mass loss (litter input Ϫ litter output); for mixed-litter assays, we sorted Fig. 9. Change in content of carbon and nitrogen in four litter types (Juncus, Spartina, Borrichia, and Quercus) after 30 d litter remnants by species before drying them. incubation in mesocosms as compared with initial values of the From these values and from measurements of de- litter (ϭ 100%). C ϭ control, L ϭ Littoraria irrorata, M ϭ Me- tritivore dry mass, we calculated consumption rates lampus bidentatus, A ϭ Armases cinereum, V ϭ Venezillo parvus. [(mg food ingested) ϫ (d ϫ mg average detriti- Initial values for litter are indicated by dashed lines at 100%. Ϫ1 Data are means Ϯ 1 SD; n ϭ 9 per litter type per detritivore vore mass) ] and relative growth rates [(mg dry species; shared letters indicate no significant differences among mass change) ϫ (d ϫ mg average detritivore treatments for each element within each litter type (ANOVA mass)Ϫ1] of detritivores for the 30-d duration of the followed by Tukey test at ␣ϭ0.05). Detritivore-free control experiment. Respiration rates of individual Armases means that differ from initial values are indicated with an asterisk above bars. and Melampus (expressed as CO2 production: ADC 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.

Carbon Nitrogen df SS F p SS F p Litter 3 516000 4580.8 Ͻ0.001 356800 1000.7 Ͻ0.001 Consumer 4 5289 35.2 Ͻ0.001 28500 59.9 Ͻ0.001 Interaction 12 47290 104.9 Ͻ0.001 15980 11.2 Ͻ0.001 Error 180 6759 21390 Total 199 575400 422700

LCA-4 CO2 Analyzer) were determined at the ter- information on the extent to which detritivores mination of the experiment. For Littoraria respi- mediated changes in litter quality. These effects ration rates could not be measured in the same could have occurred either through selective con- manner, because our measurement technique was sumption of litter or through direct inﬂuences of not sensitive enough for use with this species. detritivores (e.g., fecal amount and composition, Some Littoraria pulled back into their shells where- mucus, urine, molt deposition, and so on) on type as others crawled vigorously, and so it was impos- and abundance of microbiota. C and N were ana- sible to standardize activity level. We used a behav- lyzed in a Carlo Erba NA-1500 NCS Analyzer. Phe- ioral index, crawling activity (cm ϫ minϪ1 in moist nolics were determined as ferulic acid equivalents Petri dishes) at the completion of the experiment, (simple phenolics), tannic acid equivalents (hydro- as an alternative to the physiological measure- lyzable tannins), and quebracho equivalents (con- ments done on other species. After 30 d of feeding densed tannins) as described in Zimmer (2002). on different food sources, crawling is indicative of To estimate the digestive capabilities of detriti- diet quality: well-fed animals will be vigorous, poor- vores feeding on the different litter types, we com- ly-fed animals will be indolent. For every detriti- pared the phenolic, C, and N contents of detritivore the body carbon:nitrogen (C:N) ratio (Carlo vore feces with those of the initial litter. To deter- Erba NA-1500 NCS Analyzer) was determined after mine the impacts of microbiota on litter chemistry, the experiment. Performance of Armases and Ve- we compared litter chemistry at the start and end nezillo was further estimated in terms of mortality of the experiment in the detritivore-free meso- during the course of the experiment (snails expe- cosms. To determine impacts of detritivores, we rienced no mortality). compared litter chemistry at the end of the exper- Microbial respiration rate (expressed as CO2 iment (largest size fraction) among control meso- production: ADC LCA-4 CO2 Analyzer) was mea- cosms and mesocosms containing the different de- sured to gauge the effect of detritivore presence tritivores. on microbial activity of the litter. After removing detritivores from the mesocosms, we compared mi- Results crobial respiration [␮mol CO ϫ (mg litter ϫ h)Ϫ1] 2 DETRITIVORE PERFORMANCE in these mesocosms with values obtained from detritivore-free control mesocosms. We divided the The four detritivores ate the four litter types in values of detritivore assays by those of control as- a similar rank order: Borrichia Ն Juncus Ն Spartina says (random pairings) to calculate a promotion Ն Quercus (Fig. 1). They differed in that the mixed factor for microbial activity (expressed as a percent diet was consumed in large amounts by Littoraria of control value). and Armases, but in small amounts by Melampus. We determined litter-fraction size after the de- Venezillo ingested intermediate amounts of the tritivores were removed to obtain information on mixed diet. Armases was the only detritivore to gain the extent of grazing versus shredding by each de- mass on every diet (Fig. 2). The other three detri- tritivore species. We did this by measuring dry mas- tivores either maintained approximately their ini- ses (dried at 60ЊC to constant mass, invariably tial mass or lost mass on most diets. Both con- reached in Ͻ24 h) of litter size-fractions that had sumption and growth clearly depended on the type been separated into categories of Ͼ10 mm, Ͼ5 of litter available for every detritivore. Differences mm, Ͼ1 mm, Ͼ500 ␮m, Ͼ100 ␮m, Ͼ50 ␮m, and in consumption of different litter types were es- Ͻ50 ␮m by gentle sieving. The smallest fraction, pecially evident from mixed-litter diets. Armases Ͻ50 ␮m, was conﬁrmed by microscopic examina- consumed about the same amount of Juncus, Spar- tion to be detritivore feces. tina, and Quercus (each c. 20% of the total amount Differences in chemical composition (contents consumed), but twice as much of Borrichia. Almost of phenolics, C, and N) of freshly collected and half (45%) of the litter consumed by the snails was remnant litter of the largest size fraction, provided 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 Lit- toraria and Melampus; 11% of the litter consumed by Venezillo was Quercus, and only little more of Jun- cus was consumed (13%), while Spartina and Bor- richia 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 (Ͼ75% 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 com- parably 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.

DECOMPOSITION PROCESSES In control mesocosms, litter was essentially not comminuted, and more than 99% of the litter re- mained 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 ϫ (detritivore ϫ d)Ϫ1; Fig. 6). The isopods were most effective in shredding components of the mixed litter, but shredded relatively little Juncus and Quercus. Com- minution 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 comminu- Fig. 10. Change in content of three classes of phenolics in four litter types (Juncus, Spartina, Borrichia, and Quercus) after tion of the other types; shredding of mixed litter 30 d incubation in mesocosms as compared with initial values by Armases was intermediate. The gastropods were of the litter (ϭ 100%). Note that no quebracho or quebracho the least effective shredders. Shredding activity by equivalents were detected in the litter of Juncus and Spartina. C Littoraria was highest on mixed litter and inter- ϭ control, L ϭ Littoraria irrorata, M ϭ Melampus bidentatus, A ϭ mediate on Spartina and Quercus. Shredding by Me- Armases cinereum, V ϭ Venezillo parvus. Initial values for litter are indicated by dashed lines at 100%; control means that differ lampus did not differ among litter types, so, overall from initial values are indicated with an asterisk above bars. Data comminution of mixed litter represented an aver- are means Ϯ 1 SD; n ϭ 9 per litter type per detritivore species; age for all litter types. shared letters indicate no signiﬁcant differences among treat- Detritivores differed remarkably in how thor- ments for each element within each litter type (ANOVA followed by Tukey test at ␣ϭ0.05). Some analyses were not per- oughly they shredded the litter, that is, the frac- formed owing to too little material. 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.

Carbon Nitrogen df SS F p SS F p Litter 3 5041 56.7 Ͻ0.001 18500 109.8 Ͻ0.001 Consumer 4 123300 346.6 Ͻ0.001 84210 125.1 Ͻ0.001 Interaction 12 72880 204.9 Ͻ0.001 11730 17.4 Ͻ0.001 Error 180 8001 15160 Total 199 209200 129600 tion-size distribution of comminuted litter differed socosms, but Littoraria did not significantly affect among detritivores, and, for each detritivore, this the N content of any litter type. Melampus and Ve- pattern depended on the litter type (Fig. 7). Me- nezillo increased the N content of some litters but lampus was the only detritivore that fragmented not others. Armases also had strong effects on litter Quercus litter mostly into particles of Ͻ1 mm; the C content, increasing it relative to controls in one other detritivores produced Quercus fragments that case (Borrichia) and decreasing it in two others mostly were Ͼ5 mm. Fragment size of Spartina and (Juncus, Spartina). The other three detritivores had Juncus litter was homogeneously distributed in Lit- no significant effects on C content of any litter toraria and Armases mesocosms, but was mostly Ͻ1 type. The effects of detritivores on litter C and N mm in Melampus mesocosms and Ͼ0.5 mm in Ve- content strongly depended on both the detritivore nezillo mesocosms. The isopods, as well as Littoraria, and the litter type. fragmented Borrichia litter to Ͻ1 mm, but size-class Effects of microbial decomposition on litter phe- distribution of Borrichia fragments was almost ho- nolics in detritivore-free control mesocosms de- mogeneous in Armases and Melampus mesocosms. pended upon both phenolic class and litter type The ability to shred litter was in the order Melam- (Fig. 10, considering only the C bars). Clear pat- pus Ͼ Armases Ͼ Littoraria Ͼ Venezillo. The most terns were obvious in Quercus, with every measured thorough shredder was Melampus on Borrichia, phenolic being significantly reduced, and in Jun- where almost 90% of the initial litter material was cus, where no significant changes occurred. Simple comminuted. The least thorough shredder was Ve- phenolics were reduced in Spartina, but were not nezillo on Juncus, where only about 1% was com- changed in Borrichia. Hydrolyzable tannins were re- minuted. duced in Borrichia, but were not changed in Spar- Among detritivores, promotion of microbial res- tina. Condensed tannins in Borrichia were not piration correlated negatively with shredding activ- changed by microbial decomposition. Changes in ity. One of the least effective shredder in terms of phenolics due to detritivore-mediated effects of mi- the amount of comminuted litter, Melampus, in- crobial activity showed a diverse pattern. Detriti- creased microbial respiration over that occurring vore effects depended upon the phenolic com- in detritivore-free control mesocosms up to 5-fold, pounds as well as on both the detritivore and the whereas the other detritivores increased microbial detritus (Table 3: ANOVA). respiration by at most 2-fold (Fig. 8, Table 1). With respect to the digestion of C and N com- Among litter types, promotion of microbial respiration did not correlate well with comminution pounds and subsequent microbially mediated deg- (for example, respiration was not increased the radation of detritivore feces, we observed the same most on Borrichia litter nor the least on Quercus general pattern in every detritivore feeding on a litter), and effects were variable as indicated by a particular litter type (Fig. 11). With the exception statistical interaction of the factors litter and con- of a diet of Borrichia, detritivores mostly increased sumer in analysis of variance (ANOVA), suggesting the N content and decreased the C content relative consumer effects that depend upon the handled to changes in animal-free control mesocosms, pro- litter type. ducing a statistically significant interaction of de- Microbial decomposition in detritivore-free con- tritivore and litter type (Table 4: ANOVA). Even trol mesocosms resulted in significantly reduced N so, interpretation of the results is difficult; for ex- content and significantly increased C content in ample, while the N content of feces derived from every litter type but Borrichia (Fig. 9). Effects of Juncus and Spartina increased in comparison with detritivores on changes in the chemical composi- that of the litter in detritivore-free controls, and tion of litter remnants depended upon both the the C content decreased, both the N and C content detritivore species and the litter type (Fig. 9, Table of Borrichia decreased during gut passage. Data for 2: ANOVA). Armases increased the N content of Quercus treatments are incomplete (in many cases, every litter relative to detritivore-free control me- 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 Bor- richia and Quercus were highly variable depending on detritivore, plant, and phenolic class. Overall, no clear patterns in phenolic processing are obvious from our data. 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 un- known 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 (Zim- mer et al. 2002). According to recent studies of decomposition Fig. 11. Change in content of carbon and nitrogen due to processes, different functional groups within the digestive processes by detritivores feeding on four litter types (Juncus, Spartina, Borrichia, and Quercus) as compared with initial guild of detritivores would be expected to exhibit values of the litter (ϭ 100%). C ϭ leaf litter in control meso- differential effects on overall decomposition cosms, L ϭ Littoraria irrorata feces, M ϭ Melampus bidentatus fe- (Bardgett and Chan 1999; Richards et al. 2000; ces, A ϭ Armases cinereum feces, and V ϭ Venezillo parvus feces. Crowl et al. 2001), and even members of the same Initial values for litter are indicated by dashed lines at 100%; control means that differ from initial values are indicated with functional group may not necessarily be redundant an asterisk above bars. Data are means Ϯ 1 SD; n ϭ 9 per litter (Zimmer et al. 2002). Jonsson and Malmqvist type per isopod species; shared letters indicate no significant (2000) and Duffy et al. (2001) have independently differences among treatments for each element within each lit- shown that ecosystem processes may benefit from ter type (ANOVA followed by Tukey test). Some analyses were species richness even if all species belong to the not performed owing to too little material. 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 Juncus df SS F p df SS F p Phenolics 1 8281 5.3 0.024 1 16640 14.4 0.001 Consumer 4 224100 35.7 Ͻ0.001 4 127500 27.6 Ͻ0.001 Interaction 4 69330 11.1 Ͻ0.001 4 25450 5.5 0.001 Error 90 141400 90 103900 Total 99 443100 99 273500 Borrichia Quercus df SS F p df SS F p Phenolics 2 246000 104.8 Ͻ0.001 2 23240 17.9 Ͻ0.001 Consumer 3 275800 78.3 Ͻ0.001 4 22850 8.8 Ͻ0.001 Interaction 6 179000 25.4 Ͻ0.001 8 72420 14.1 Ͻ0.001 Error 108 126800 135 87310 Total 119 827500 149 205800 B Ferulic Acid Tannic Acid Quebracho df SS F p df SS F p df SS F p Litter 3 166300 45.4 Ͻ0.001 3 331900 104.0 Ͻ0.001 1 122500 216.4 Ͻ0.001 Consumer 4 139400 28.6 Ͻ0.001 4 187200 44.0 Ͻ0.001 4 124100 54.8 Ͻ0.001 Interaction 12 266500 18.2 Ͻ0.001 12 161200 12.6 Ͻ0.001 4 171300 75.6 Ͻ0.001 Error 180 219600 180 191500 90 50950 Total 199 791900 199 871800 99 468800 same functional group. In their study on the im- dundant; their intraguild diversity may actually pact of changing the diversity and species compo- benefit ecosystem processes, and the fate of salt sition of detritivores on decomposition processes marsh detritus in part depends upon its site of de- such as litter mass loss, microbial respiration, and composition. nutrient fluxes, Cragg and Bardgett (2001) sug- The detritivores in our study responded in a spe- gested that the composition of a detritivore com- cies-specific manner to the offered food sources. munity, rather than its diversity, is of greatest im- Although there were similar patterns across detri- portance for ecosystem functioning. Bardgett and tivore species (e.g., consumption rates had similar Chan (1999) stressed the significance of different rank order across the plant species), both their di- feeding strategies of belowground detritivores in gestive processes and overall performances dif- nutrient cycling and increasing plant productivity. fered markedly. The most striking difference was These differences reduce competition and make that Armases gained mass on every litter diet, while coexistence possible (Hardin 1960; Armstrong and the other detritivores either did not appreciably McGehee 1980; Richards et al. 2000). change in mass or lost mass on most diets. This is Besides species-specific differences in feeding likely explained by the fact that, in nature, these preferences and feeding rates (Rietsma et al. 1982; organisms eat a variety of food types, including Zimmer et al. 2002), it is likely that members of both detritus and microalgae, and that the more the diverse community of salt marsh detritivores limited diets presented in the mesocosms were nu- co-exist on a large scale (see above) in part by oc- tritionally inadequate. Some of the species may cupying different habitats (Littoraria favors regular- feed preferentially on litter from particular parts ly-flooded low and mid marsh habitats, Melampus of the plants that were not present in the jars— high marsh habitats, and Armases and Venezillo the Littoraria preferentially feeds on leaf blades, not terrestrial border of the marsh). Although we did stems, and prefers leaves that are heavily colonized not directly test for competition among the detri- with fungi (Newell and Ba¨rlocher 1993; Graça et tivores in our study, our data indicate that their al. 2000). Its consumption can have a strong neg- different feeding strategies and digestive efficacies ative impact on living Spartina when it occurs at lead to their processing of litter in many different high densities (Silliman and Zieman 2001; Silliman ways. In combination with different habitat pref- and Bertness 2002; Silliman and Newell 2003). Al- erences, these different feeding strategies will re- though we commonly observe Littoraria feeding on duce interspecies competition to a minimum. With stems in the field, this diet may not, by itself, be respect to contribution to decomposition process- sufficient to sustain growth. es, salt marsh detritivores are not functionally re- It is surprising that Littoraria and Venezillo lost Redundancy of Detritivores? 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 Quer- cus 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 con- tained enough Borrichia for the compounds to be lethal, but the compounds could have affected growth of some consumers. Such effects of Borri- chia 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 lar- vae (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. Me- Fig. 12. Change in content of three classes of phenolics due lampus gained from feeding on a mixed diet in that to digestive processes by detritivores feeding on four litter types (Juncus, Spartina, Borrichia, and Quercus) as compared with initial the C:N body ratios were higher on single-litter di- values of the litter (ϭ 100%). Note that no quebracho or que- ets. This was not true for Littoraria and Armases, but bracho equivalents were detected in the litter of Juncus and Spar- even here, our results clearly indicate that the abil- tina or in feces derived from these litter types. C ϭ leaf litter in control mesocosms, L ϭ Littoraria irrorata feces, M ϭ Melampus bidentatus feces, A ϭ Armases cinereum feces, and V ϭ Venezillo ← parvus feces. Initial values for litter are indicated by dashed lines at 100%; control means that differ from initial values are indi- no significant differences among treatments for each element cated with an asterisk above bars. Data are means Ϯ 1 SD; n ϭ within each litter type (ANOVA followed by Tukey test). Some 9 per litter type per isopod species; shared letters indicate 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 Juncus df SS F p df SS F p Phenolics 1 2209 0.7 0.408 1 220900 50.7 Ͻ0.001 Consumer 4 1693000 132.6 Ͻ0.001 4 528200 30.3 Ͻ0.001 Interaction 4 128300 10.1 Ͻ0.001 4 89220 5.1 0.001 Error 90 287400 90 392000 Total 99 2111000 99 1230000 Borrichia Quercus df SS F p df SS F p Phenolics 2 619300 156.6 Ͻ0.001 2 504900 88.1 Ͻ0.001 Consumer 3 618500 104.2 Ͻ0.001 4 798500 69.6 Ͻ0.001 Interaction 6 1024000 86.3 Ͻ0.001 8 1174000 51.2 Ͻ0.001 Error 108 213600 135 387000 Total 119 2476000 149 2865000 B Ferulic Acid Tannic Acid Quebracho df SS F p df SS F p df SS F p Phenolics 3 1284000 119.9 Ͻ0.001 3 160600 21.1 Ͻ0.001 1 370900 182.9 Ͻ0.001 Consumer 4 1436000 100.6 Ͻ0.001 4 646700 63.6 Ͻ0.001 4 609200 75.1 Ͻ0.001 Interaction 12 1225000 28.6 Ͻ0.001 12 1856000 60.8 Ͻ0.001 4 576200 71.1 Ͻ0.001 Error 180 642300 180 457900 90 182500 Total 199 4588000 199 3122000 99 1739000 ity to incorporate N, being limiting for animals Based on density ranges given in the literature feeding on plant material (White 1993), into their (Teal 1962; Fell et al. 1991; Ba¨rlocher and Newell biomass depended on the available litter type. 1994b; Zimmer et al. 2002) and on our own ob- Nutritional requirements of salt marsh detriti- servations on consumption of different litter types, vores are species-specific, a reflection in the short we have estimated the potential contribution of the term of specific enzymatic and other adaptations, four detritivores used in the present study to over- and in the long term of intraguild resource parti- all mass loss of salt marsh litter (Table 6). Due to tioning. We expect their food sources, i.e., the de- its high density in the field (up to 600 mϪ2:Ba¨r- tritus of different salt marsh plants, not to be equiv- locher and Newell 1994b), Littoraria would be ex- alent. In a comparison of different marshes, Fell et pected to contribute most strongly to disappear- al. (1998) did not find any effect of the invading ance of litter of all types. According to values of reed grass, Phragmites australis, on the abundance Spartina biomass production presented by Kemp et of semiterrestrial invertebrate salt marsh detriti- al. (1990), our estimated consumption of 550 g vores (including snails and isopods); they did not Spartina litter per square meter per year [(m2 ϫ study feeding by these detritivores. Angradi et al. a)Ϫ1] by the four detritivore species we tested (2001) found fewer macroinvertebrates in Phrag- would equal about 20% of the annual biomass pro- mites litter than in Spartina litter, and suggested dif- duction. Because our data are based on consump- ferences in the quality of the litter as a possible tion of Spartina stems, which are much less palat- explanations. Rietsma et al. (1982) found that able than the softer, thinner leaves (Newell and feeding preferences of different salt marsh detri- Ba¨rlocher 1993; Graça et al. 2000), consumption tivores was not related to the abundance of food. of Spartina litter even by Littoraria alone would like- These detritivores, including Melampus, a Littoraria ly greatly exceed our estimates [notwithstanding and an isopod, differed in their feeding preferenc- Kemp et al.’s (1990) Littoraria-consumption data of es, but clearly responded to similar feeding cues 360–720 g ϫ (m2 a)Ϫ1 in the field that are similar represented by N content (Ba¨rlocher and Newell to the results of the present study]. Based on daily 1993; White 1993), content of phenolic com- consumption rates in the laboratory presented by pounds (Valiela and Rietsma 1984; Ba¨rlocher and Graça et al. (2000) and field densities presented in Newell 1993), and biomass of microbial litter col- Table 6, Littoraria theoretically has the potential to onizers (Ba¨rlocher et al. 1989; Newell and Ba¨rloch- consume more than 3 kg ϫ (m2 ϫ a)Ϫ1 of Spartina er 1993; Graça et al. 2000). We conclude that the leaf litter. We also observed potential consumption litter of different plant species cannot be regarded rates of more than 1.3 kg Borrichia litter ϫ (m2 ϫ as redundant as food for salt marsh detritivores. a)Ϫ1 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 ϫ (m2 a)Ϫ1]as estimated from the present results and average density data from the literature (300 Littoraria mϪ2, 100 Melampus mϪ2;10Armases mϪ2;60Venezillo mϪ2; for references, see text).

Consumption, g(m2 a)Ϫ1 Juncus Spartina Borrichia Quercus Littoraria irrorata 800 500 1500 100 Melampus bidentatus 50 25 50 20 Armases cinereum 40 20 30 20 Venezillo parvus 5 5 60 2 Comminution, g(m2 a)Ϫ1 Juncus Spartina Borrichia Quercus Littoraria irrorata 100 150 100 150 Melampus bidentatus 20 30 30 20 Armases cinereum 30 10 15 10 Venezillo parvus 1 2 2 1

Littoraria is unlikely to gain access to these large motion of microbial activity on a range of litter amounts of Borrichia litter because it mostly occurs types, through its interchanging of nutrients and at lower levels in the intertidal zone than does Bor- energy between coast-forest and salt marsh habi- richia. Although Littoraria would theoretically be tats, and through its capabilities of digesting di- able to ingest about 125 g (dry mass) ϫ (m2 ϫ a)Ϫ1 verse phenolic litter compounds (present study; of Quercus litter, the probability of encountering Zimmer et al. 2002). Venezillo is also a potential this type of litter, too, is relatively low in the field. prey species of Armases (Buck et al. 2003), further For these high-intertidal region and marsh-fring- increasing its potential role in energy and nutrient ing litter types, crustacean detritivores may be fluxes between terrestrial and salt marsh habitats. more important with respect to litter consumption Direct contribution by the snail Melampus to litter and comminution. Our mesocosm data suggest disappearance through feeding, as based on aver- that Armases would consume much smaller age densities of about 100 mϪ2 (Table 6), is similar amounts of the four litter types in the field than to that by Armases. Although at some sites in north- Littoraria [about 40 g ϫ (m2 ϫ a)Ϫ1]. While litter ern salt marshes densities of more than 1,200 ind processing is monopolized by the sesarmid crab, mϪ2 have been observed (Fell et al. 1982), the eco- Gecarcoidea natalis, removing 39–87% of the annual system significance of this detritivore at Sapelo Is- leaf fall in the tropical rain forest of the Christmas land appears to be in its high contribution to litter Islands (Green et al. 1999), and sesarmid crabs in comminution and promotion of microbial activity mangroves in Peninsula Malaysia contribute signif- (see Figs. 6 and 7) rather than in its overall con- icantly to leaf litter removal (Ashton 2002), man- sumption of litter. grove leaf litter (Avicennia marina) seems to be of Considering only one litter type or one detriti- insufficient quality to fulfill the N requirements of vore species by studying only some of the param- other sesarmids, Neosarmatium meinerti and Sesarma eters of decomposition processes we studied would guttatum, and their natural diets consists by less not have enabled us to paint as clear a picture of than 10% of leaf litter (Skov and Hartnoll 2002). different functions of different detritivores feeding Since the omnivorous Armases is also known to prey on different litter types as we did here. Under- upon snails and small crustaceans (Buck et al. standing decomposition processes in the high 2003), its importance in the salt marsh ecosystem marsh zones where Littoraria is least abundant may be mainly in its intertrophic mediating influ- (Pennings unpublished data), and understanding ence on decomposition. It has the potential to how materials in the detritivore food web move more broadly influence decomposition processes, back and forth from marine to terrestrial habitats, and energy and nutrient fluxes, than any of the may require examining a variety of detritivores and other detritivores. Because Armases is far more mo- a variety of detrital food sources. Both Littoraria tile than the other detritivores, it probably has and Armases are absent in northern U.S. salt marsh- quicker access to new or isolated patches of litter es, while Melampus and Venezillo are abundant in that would be colonized more slowly, if at all, by northern and, to a lesser degree, in southern salt other detritivores. According to our estimates (Ta- marshes (Pennings unpublished data). Studies on ble 6), the isopod Venezillo provides little contri- solely Littoraria will not provide information of de- bution to decomposition in terms of litter con- composition in northeastern U.S. salt marshes. sumption. This small but abundant species (Zim- Our conclusions presented here, however, are mer et al. 2002) may be important through its pro- based on the result of mesocosm studies, and con- 768 M. Zimmer et al. sequently have a variety of attendant potential ar- Gastropoda). Journal of Experimental Marine Biology and Ecology tifacts; the high mortality of consumers feeding on 130:45–53. BERTNESS, M. D. 1999. The Ecology of Atlantic Shorelines. Sin- Borrichia litter was an artifact that would likely not auer Associates, Inc., Sunderland, Massachusetts. have happened in the field. It is also hard to de- BERTNESS,M.D.AND A. M. ELLISON. 1987. Determinants of pat- duce specific effects of these species on ecosystem tern in a New England salt marsh plant community. Ecological processes in the field from laboratory experiments Monographs 57:129–147. using single-species assays. Redundancy in terms of BUCK, T. L., G. A. BREED,S.C.PENNINGS,M.E.CHASE,M.ZIM- MER, AND T. H. CAREFOOT. 2003. Diet choice in an omnivorous such effects can experimentally be tested best by salt marsh crab: Different food types, crab allometry, and hab- successively adding or removing species to or from itat complexity. Journal of Experimental Marine Biology and Ecol- a given system. The present results provide insight ogy 292:103–116. into what the species tested here are able to con- CHALCRAFT,D.R.AND W. J. RESETARITS. 2003a. Mapping func- tribute to decomposition processes in salt marshes, tional similarity of predators on the basis of trait similarity. but these contributions might change as soon as The American Naturalist 162:390–402. CHALCRAFT,D.R.AND W. J. RESETARITS. 2003b. Predator identity other species are present, too. Due to character and ecological impacts: Functional redundancy or functional displacement, it is unlikely that species that differ diversity? Ecology 84:2407–2418. in what they do, and how they respond, to different CONN,C.AND J. DIGHTON. 2000. Litter quality influences on food sources become more alike when they co-oc- decomposition, ectomycorrhizal community structure and mycorrhizal root surface acid phosphatase activity. Soil Biology cur than when they act alone. Species-specificity as and Biochemistry 32:489–496. presented here can be taken as a hint on function- COVI,M.P.AND R. T. KNEIB. 1995. Intertidal distribution, pop- al diversity of the tested detritivores under natural ulation dynamics and production of the amphipod Uhlorches- conditions. Our results need to be confirmed and tia spartinophila in a Georgia, USA, salt marsh. Marine Biology extended by in situ studies of the various detriti- 121:447–455. CRAGG,R.G.AND R. D. BARDGETT. 2001. How changes in soil vore-litter combinations in their natural habitats. faunal diversity and composition within a trophic group influence decomposition processes. Soil Biology and Biochemistry 33: ACKNOWLEDGMENTS 2073–2081. We are grateful for financial support provided by the Univer- CROWL, T. A., W. H. MCDOWELL,A.P.COVICH, AND S. L. JOHNSON. sity of Georgia Marine Institute Visiting Scientist Program (M. 2001. 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