Decomposition of Leaf Litter in a U.S. Saltmarsh is Driven by Dominant Species, Not Species Complementarity Malte Treplin, Steven C. Pennings & Martin Zimmer
Wetlands Official Scholarly Journal of the Society of Wetland Scientists ISSN 0277-5212 Volume 33 Number 1 Wetlands (2013) 33:83-89 DOI 10.1007/s13157-012-0353-1
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Author's personal copy Wetlands (2013) 33:83–89 DOI 10.1007/s13157-012-0353-1
ARTICLE
Decomposition of Leaf Litter in a U.S. Saltmarsh is Driven by Dominant Species, Not Species Complementarity Malte Treplin & Steven C. Pennings & Martin Zimmer
Received: 3 July 2012 / Accepted: 6 November 2012 / Published online: 14 November 2012 # Society of Wetland Scientists 2012
Abstract To add to our understanding of species richnesseffects on ecosystem processes, we studied the importance of species complementarity in driving decomposition in a saltmarsh in Georgia, USA. We studied pair-wise interactions of both detritivores and plant litter species and how they affect decomposition rates in an experiment located on the mid-marsh platform. Needle rush, Juncus roemerianus, had 2-3 times higher decomposition rates than cordgrass, Spartina alterniflora, or live oak, Quercus virginiana. Mixing litter types did not promote decomposition rates. Cordgrass decomposition was 1.5-times higher when periwinkles, Littoraria irrorata, were present than in detritivore-free controls. In contrast, neither coffee-bean snails, Melampus bidentatus, nor wharf crabs, Armases cinereum, increased cordgrass decomposition rates. Mixing detritivore species did not increase cordgrass mass loss beyond expected rates from an additive model. We conclude that in this system, species do not act complementarily with each other, but that decomposition rates are controlled by the dominant species of angiosperms and invertebrate detritivores.
M. Treplin : M. Zimmer Zoologisches Institut, Christian-Albrechts-Universität, Am Botanischen Garten 9, 24118 Kiel, Germany S. C. Pennings Department of Biology and Biochemistry, University of Houston, Houston, TX 77204-5001, USA Present Address: M. Zimmer (*) Paris-Lodron-Universität Salzburg, FB Organismische Biologie, AG Ökologie, Biodiversität & Evolution der Tiere, Hellbrunner Str. 34, 5020 Salzburg, Austria e-mail:
[email protected]
Keywords Decomposition . Detritivores . Saltmarsh . Species identity . Species richness . Species interaction
Introduction Ecologists are increasingly interested in whether and how species richness mediates ecological processes. Observed positive effects of species richness have been related to (1) "complementarity" (Naeem et al. 1994; Tilman et al. 1996; Loreau 1998) or (2) "sampling" (Aarssen 1997; Huston 1997; Tilman et al. 1997; c.f. "selection/dominance effects" in Loreau and Hector 2001; Fox 2005). Complementarity is based on species-specific resource use or positive interspecific interactions (facilitation), resulting in higher performance (synergism) at the community level than expected from performance of single species. Alternatively, according to the sampling effect, the probability of including a particularly well-performing species will increase with species richness. Hence, performance at the community level will equal that of the best performing single species. The selection effect (Loreau and Hector 2001) or dominance effect (Fox 2005) in addition takes into account the relative abundance of species in mixtures (Hector et al. 1999). In speciespoor systems, where there is little scope for the selection effect to operate, the most likely mechanism that could produce positive effects of species richness is complementary interactions between species. Saltmarshes along the Atlantic US coast are relatively poor in species richness of vascular plants and macroinvertebrates, being dominated by only few abundant species. In Georgia saltmarshes, for example, plant biomass is dominated by the grass Spartina alterniflora (Wiegert and Freeman 1990), and decomposition of S. alterniflora is thought to be driven by interactions between fungi and a single abundant snail species, Littoraria irrorata (Silliman
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and Newell 2003). Although other plant and detritivore species occur, their roles in ecosystem processes, and the potential synergies between species, have been less studied. Although nutrient cycles in intertidal saltmarshes are primarily detritusbased (Teal 1962; Nixon and Oviatt 1973; Valiela and Teal 1979), they are also naturally poor in species of the detritivorous macro-fauna. The decomposition of detrital matter, being the result of complex interactions of detritivores and microbes, serves in both (1) transferring energy to higher trophic levels within the marsh, and (2) exporting energy to adjacent habitats. Decomposition rates vary with the identity of both the detrital source (Cornelissen 1996; Wardle et al. 1997) and the detritivores feeding on the litter, be it leaf litter of terrestrial origin (Hättenschwiler and Gasser 2005; Zimmer et al. 2005; Treplin and Zimmer 2012), seagrass (Moore and Fairweather 2006), or macroalgal detritus (Godbold et al. 2009). Further, individual species effects may be independent of other species (i.e., additivity), or emergent effects of species (i.e. non-additivity) may occur in mixed-species combinations (c.f., Kominoski et al. 2007; Ball et al. 2008), corroborating the complementarity of species. Saltmarsh detritivores are not redundant, but contribute species-specifically to decomposition processes (Zimmer et al. 2002, 2004). Because the different detritivores affect decomposition in different ways, it is reasonable to hypothesize that mixtures of detritivores might out-perform any one species by functioning in a complementary manner. It remains, however, unknown how co-existing saltmarsh detritivores interact. Are their species-specific contributions complementary, resulting in non-additive (synergistic) enhancement of decomposition? To answer this question, we studied how single-species treatments differed from species mixtures in terms of litter mass loss (as a proxy of decomposition processes) in field mesocosms. As a base line, we chose decomposition of the most common saltmarsh plant, the cordgrass Spartina alterniflora (Pennings et al. 2001), through the action of the most common saltmarsh consumer, the periwinkle Littoraria irrorata (Bärlocher and Newell 1994). By experimentally varying both species richness and identity of both detritus and detritivores, we examined effects of both resources and consumers within the same system. More explicitly, we tested for complementarity, hypothesizing that mixtures of litter species would decompose faster than any single litter through the combination of species-specific litter traits, and that mixing detritivore species pair-wise would also increase litter decomposition rates through the complementarity of interacting functional traits.
Methods The experiment was conducted in a saltmarsh habitat at Sapelo Island (31.39° N, 81.29° W), GA, USA. The
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experimental field site was located at Dean’s Creek, on the south end of Sapelo Island (site GCE6 of the Georgia Coastal Ecosystems Long-Term Experimental Research program: http://gce-lter.marsci.uga.edu/public/app/studysites.asp). Experimental cages were constructed of a strip of plastic garden edging, a 1.5 m PVC pipe, and fiberglass window screen mesh. The plastic edging was formed into a ring of 35 cm diameter and 10 cm height. The screen was sewed into a tube that was looped around the plastic ring at the bottom to prevent animals from entering or leaving the cage. The ring was completely sunk into the soil, securing the bottom of the mesh. In the center of the ring, the plastic pipe was inserted into the soil 80 cm deep and the net was tied above the top of the pipe with a cable tie to form a tent-like cage 70 cm in height. Cages were placed on the marsh platform, at intermediate elevations within the saltmarsh. We studied litter from three plants that commonly contribute to litter input at the field site (c.f., Zimmer et al. 2004), namely the cordgrass Spartina alterniflora Loisel, the needle rush Juncus roemerianus Scheele, and live oak Quercus virginiana Miller. Litter that showed little decay upon visual inspection was handpicked from plant stands in the adjacent area, air-dried and weighed. Litter was offered as food to detritivores in single-species treatments (3 treatments) and all possible two-species combinations (3 treatments). We placed 20 g (dry weight) of litter in each cage (either 20 g of one species, or 10 g each of two species). Detritivores were collected from the local area, and kept in the lab until used in the experiment. We studied the most abundant detritivores (Buck et al. 2003; Zimmer et al. 2004) at the field site (two snails and a decapod crab): the periwinkle Littoraria irrorata Say, the coffee bean snail Melampus bidentatus Say, and the omnivorous wharf crab Armases cinereum Bosc. Another abundant detritivore, the amphipod Orchestia grillus, was not included because of high risk of mortality in captivity (authors' unpubl. obs.) and because it is a preferred prey for the wharf crab (Buck et al. 2003). Detritivorous terrestrial isopods (Littorophiloscia vittata; Porcellionides virgatus; Venezillo parvus), occur at higher tidal elevations than the intertidal elevation studied here and were thus not included. We did not experimentally manipulate the microbial decomposer community, which consists of a mixture of fungi and bacteria (Osono and Takeda 2002; Silliman and Newell 2003; Buchan et al. 2003), but instead allowed microbial communities to develop based on the litter and detritivore treatments. A ratio of fresh weight to soft body water content was determined for each detritivore species through weighing and oven-drying (60 °C) to constant dry mass. Animal biomass was equalized according to these ratios based on the average density of L. irrorata at Dean’s creek of ~90 snails per m2. Soft body dry mass of 9 medium-sized L. irrorata equalled that of 45 medium-sized M. bidentata, or 2 medium-sized A.
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comparison to the weighted average of single-species effects ("expected" detritivore effects) that had also been corrected for random-paired control values. Using the same approach, we compared litter-mixture treatments ("observed") with the weighted averages of single-litter treatments ("expected"). This process was done independently for detritivore-free controls, crab-, snail- and two-species treatments. Following Wardle et al. (2006), the "expected" values were calculated by weighting litter-specific mass loss with respect to the species composition of the litter mixture at the end of the experiment. Expected and observed values were compared using t tests after ln- or square root-transformation as appropriate (c.f. Zimmer et al. 2005; Treplin and Zimmer 2012).
Results Decomposition rates of Juncus (needle rush) were 2-3 times higher than those of Spartina (cordgrass) and Quercus (live oak) (Fig. 1). Adding slowly-decomposing detritus (Spartina or Quercus) to Juncus did not reduce its decomposition rate, nor did adding Juncus detritus to Quercus or Spartina increase decomposition rates of these species. Effects of mixing detrital sources on total decomposition rates were exclusively additive (Fig. 2), resulting in decomposition rates that were intermediate to single-detritus mass loss rates. Thus, we did not find any effect of increasing litter species richness from one to two species on litter mass loss, suggesting a lack of complementarity in litter decomposition. 100
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cinereum. Total detritivore biomass was kept constant across all treatments, resulting in experimental densities of detritivores (450 Melampus or 20 Armases per m2) that were within the range of values observed in the field but higher than the average (100 Melampus or 10 Armases per m2: c.f., Zimmer et al. 2004). To study potential pair-wise complementary effects of increasing litter species richness, we compared decomposition of the three litter types alone with all three possible 2-species combinations of litter types in the presence of the most abundant detritivore, Littoraria irrorata (total of six litter treatments; N07, each). To study potential pair-wise interactions of detritivore species, we compared decomposition of the dominant saltmarsh plant, Spartina alterniflora, in the presence of no detritivores (detritivore-free control), of all three detritivore species in single-species treatments, and of all three possible 2-species combinations of detritivores (total of seven detritivore treatments; N07, each). Hence, we installed a total of 13 (treatments) x 7 (replicates)0105 tents. Experimental tents were placed on the marsh platform in a stand of the perennial succulent, Batis maritima (Bataceae), 2.1±0.05 m above mean low water level (levelled with a theodolite). All vegetation under the cages was removed by clipping, and cages were haphazardly placed 50 cm apart in a rectangular area. Cages were stocked with leaf litter and detritivores in June 2006 and remained in the field for 3 months. During this time of high detritivore activity, daily mean air temperature ranged from 23.5 °C to 30.5 °C. Except for a heavy rain event on June 13, there was less than 10 mm precipitation until August 12, with a total of ca 80 mm between August 12 and 30 (http://gce-lter.marsci.uga.edu; data set ID marshlanding_daily_jan06-dec06). During the experiment, the site was inundated about 50 times, with a maximum tide level of 45 cm above the soil level. Tides within the study area are semi-diurnal with a tidal range that can vary from 1.5 m during neap tide to 3.0 m during spring tide. The tide propagating into the saltmarshes becomes increasingly distorted because of frictional dissipation of energy in the shallow channels and intertidal marsh areas, leading to ebb tidal currents that are stronger than flood tidal currents (Blanton et al. 2002). After 3 months, cages were sampled for litter mass: residual litter was sorted to species, cleaned of deposited sediments and oven-dried to constant weight to obtain total dry weight. Due to strong weather and the dynamic tidal regime, some cages were destroyed or animals were missing. These cages were not included in the analyses, and the number of replicates was reduced to 5 in two treatments and 4 in one treatment. Other than that, all detritivores survived the experiment. For statistical analysis, we essentially followed Loreau and Hector (2001). First, we tested effects of two-species treatments, corrected for detritivore-free control values through random-pairing ("observed" detritivore effects), in
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Fig. 1 Percent litter mass loss of different detrital types in singlespecies treatments (Spartina, Quercus, Juncus) and in combination with each other [(Quercus): in combination with Quercus, (Juncus): in combination with Juncus, (Spartina): in combination with Spartina] in the presence of Littoraria. Whisker-Box-Plots indicate minimum, 1st quartile, median, 3rd quartile, and maximum (N07); different lower-case letters indicate significant differences (ANOVA; post hoc pairwise comparison through Tukey’s multiple comparison; α00.05).
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ns
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free control, although their densities in the mesocosms were higher than on average in the field. Joint effects of detritivores in mixtures were exclusively additive (Fig. 4). We found no effects on litter mass loss of increasing detritivore species richness from one to two species, indicating that interactions among these species pairs showed no evidence of complementarity.
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Fig. 2 Effects of litter-mixing on decomposition (percent litter mass lost). Observed decomposition rates were compared with expected rates as described in the Methods. Whisker-Box-Plots indicate minimum, 1st quartile, median, 3rd quartile, and maximum (N07). (ns: not significant; Wilcoxon matched-pairs signed rank tests; α00.05).
Decomposition of Spartina was 1.5-times higher when Littoraria was present than in detritivore-free controls (Fig. 3). In contrast, neither of the other two detritivores increased Spartina decomposition relative to the detritivore-
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According to Zimmer et al. (2004), the saltmarsh detritivores studied herein are not redundant, nor are the different detrital sources used herein. The detritivores differ in feeding mode and impact on mass loss, and the litter types differ in chemistry and structure. Nevertheless, neither different litter sources nor different detritivore species interacted in a complementary way to enhance detrital mass loss. Although we cannot rule out the possibility that including other species would have led to different results, we found no evidence for complementarity in the interactions between the species that we did study. Instead, results were purely additive, driven by the individual effects of the species studied. Whether and how species richness affects decomposition processes has been a topic of some controversy for a number of years. In some cases, species identity rather than species richness drives ecosystem processes (e.g., Vivanco and Austin 2008; McLaren and Turkington 2010; but see Gessner et al. 2010 for a recent, nuanced, review). The detritus types 60
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Fig. 3 Percent mass loss of Spartina litter in detritivore-free controls and in the presence of detritivores in single-species treatments (Littoraria, Armases, Melampus) and in combinations. Whisker-Box-Plots indicate minimum, 1st quartile, median, 3rd quartile, and maximum (N07); detritivore treatments were pairwise compared to the control C to test for detritivore effects on litter mass loss; combinations of detritivores were compared to single-detritivore assays to test for diversity effects; different lower-case letters indicate significant differences (α00.05).
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Discussion
Fig. 4 Effects of detritivore-mixing on decomposition (percent litter mass lost). Observed decomposition rates were compared with expected rates as described in the Methods. Whisker-BoxPlots indicate minimum, 1st quartile, median, 3rd quartile, and maximum (N 07). (ns: not significant; Wilcoxon matched-pairs signed rank tests; α00.05)
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we used herein differ significantly in terms of chemistry and structure (c.f., Pennings et al. 1998; Zimmer et al. 2002, 2004), creating the potential for complementarity, since detritivores might improve their nutrition or minimize exposure to particular defenses by feeding on mixtures of the two species. Due to structural and chemical differences, detrital sources of different origins differed in decomposition rate. In particular, litter from Quercus and Spartina lost only 30 and 50 % as much dry mass, respectively, as litter from Juncus lost during the three-month experiment. Hence, in the upper saltmarsh, where detritus of all three plants is common, Juncus will contribute most rapidly to organic matter turnover and nutrient cycling. Not surprisingly, it is common to see mats of Spartina or Quercus litter in the marsh, but rare to see mats of Juncus litter (authors' unpubl. obs.). Mixing live oak or cordgrass detritus with needle rush detritus reduced the overall rate of detrital mass loss, but not more so than would have been expected from averaging mass loss rates (additive effects). In sum, we found no evidence for complementarity of detrital sources in this detritus-based system. The detritivores we used herein differ significantly in terms of feeding mode (c.f., Zimmer et al. 2004) and their impact on litter mass loss, providing the potential for complementarity through interactions (c.f., Zimmer et al. 2005; Treplin and Zimmer 2012), if one species processed litter in ways that made it more palatable for the other species, as has been suggested for Melampus, Littoraria and Armases by Ewers et al. (2012). Whereas wharf crabs and coffee-bean snails hardly affected mass loss of Spartina litter, the periwinkle Littoraria increased Spartina mass loss rates by more than 50 %. Extrapolating this feeding rate results in about 352 g Spartina detritus being consumed per m2 per year (similar to the estimate of 500 gm2 a-1 in lab studies by Zimmer et al. 2004). Mixing this efficient detritivore with either Armases or Melampus slightly reduced the overall rate of decomposition (but not significantly so: LA vs L: p00.07; LM vs L: p00.29), thus reducing (c.f., Creed et al. 2009) an important ecosystem process, but to a rate no slower than would be expected from averaging singlespecies mass loss rates (additive effects). In sum, we found no evidence for complementary effects of detritivores in this detritus-based system. Based on these two negative results, we conclude that, in Southeastern US saltmarshes, the overall rate of decomposition of dominant marsh plants is driven by the dominant detritivore (in this case Littoraria). If additional species are rare and/or ineffective, adding more species to the system will only marginally add to the effectiveness of single ecosystem processes. Notwithstanding, these additional species may significantly contribute in other ways to overall ecosystem functioning. For example, although Armases only weakly contributed to detrital mass loss in this study, it plays an important ecological role as a mediator of energy fluxes
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between trophic levels and along the marine-terrestrial ecotone (Buck et al. 2003; Zimmer et al. 2004), a habitat where Littoraria is essentially absent. Similarly, Melampus significantly promotes microbial activity on decaying saltmarsh detritus, whereas the other detritivores do not (Zimmer et al. 2004; authors' unpubl. obs.). Melampus is negatively affected by Littoraria (Lee and Silliman 2006), and Melampus is more abundant at sites where Littoraria is rare (McFarlin et al. 2008). Hence, Melampus may play a larger role in decomposition processes in the absence of Littoraria than when this superior competitor (c.f, Lee and Silliman 2006) is present (as herein). An important caveat to our results is that we cannot exclude the possibility that we might have observed complementarity had we combined all three studied species. Also, we did we not include Orchestia grillus in our study. This amphipod is sometimes abundant (especially in the upper marsh: Kneib 1984) and, together with another amphipod Uhlorchestia spartinophila (Graça et al. 2000), potentially contributes to the decomposition of saltmarsh litter. Our experimental design, using closed cages, did not allow for including these amphipods, because Armases readily preys on amphipods (Buck et al. 2003), and would soon have eliminated all individuals inside the cages. Similarly, terrestrial isopods were not included because they are essentially lacking from the intertidal elevations studied, but these may be important at high marsh elevations. Thus, it is possible that we might have observed complementary effects had we included other species combinations in the study design. According to Dangles and Malmqvist (2004), a species with a strong ecosystem effect must occur at high densities year-round, be highly motile, and be engaged in strong interspecific interactions. Littoraria is highly abundant throughout the saltmarsh except immediately adjacent to creekbanks (Teal 1962; Fell et al. 1991; Bärlocher and Newell 1994; Zimmer et al. 2004) and is present at all seasons, although dormant in winter (Vaughn and Fisher 1992). Its seasonal range of activity, however, appears to be no more than a circle of 2 m in diameter (Vaughn and Fisher 1992). A strong regulating impact of Littoraria on Spartina production has been shown (Silliman and Zieman 2001), and Littoraria is competitively superior to Melampus and has the ability to displace the smaller snail (Lee and Silliman 2006). Thus, despite its limited motility, Littoraria appears to be a major player in Atlantic saltmarshes along the U.S. East Coast that interacts with other detritivores (Silliman and Newell 2003; Ewers et al. 2012) but, as we have shown here, does not act complementarily with them. Acknowledgements We are grateful to Sebastian Fraune, The Lord of the Rings, for his invaluable help in setting-up this field study under adverse conditions. This work is a contribution of the Georgia Coastal
Author's personal copy 88 Ecosystems Long-Term Ecological Research program (OCE99-82133, OCE06-20959), and is contribution number ... of the University of Georgia Marine Institute.
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