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Home , Decomposition, Detritivore, Predation

Wetlands DOI 10.1007/s13157-012-0326-4

ARTICLE

Predator/-Interactions Promote of Low-Quality

Christine Ewers & Anika Beiersdorf & Kazimierz Więski & Steven C. Pennings & Martin Zimmer

Received: 29 February 2012 /Accepted: 10 July 2012 # Society of Scientists 2012

Abstract on is expected to decelerate were present, probably owing to predation on detritivorous -mediated decomposition processes. In field mes- . Thus, the effects of predator/prey-interactions on ocosms, we studied whether the decomposition of leaf and decomposition processes are context-dependent and are needle litter of live oak (Quercus virginiana) and loblolly controlled by quality. (Pinus taeda), respectively, was affected by saltmarsh detritivores (: Littoraria irrorata and Melampus Keywords Decomposition processes . Predator/prey- bidentatus) and predacious (Decapoda: Armases interaction . Omnivory . Saltmarsh . Spatial subsidy cinereum) and their interactions. Both and snails alone increased decomposition (mass loss) rates of oak litter, while a combination of both resulted in the same mass loss Introduction as in -free controls, probably due to crabs feeding on snails rather than litter. Neither crabs nor snails alone affect- of angiosperms is primarily con- ed mass loss of pine litter, but a combination of both signif- sumed by detritivores rather than (Teal icantly increased decomposition rates. Irrespective of the 1962;Cebrian1999). It has long been studied how litter type, crabs significantly increased mortality of the detritivores are affected by interactions with microbes snails but gained only on pine litter and only when (e.g., Newell and Bärlocher 1993; Newell 1996;Zimmer detritivorous snails were present. Our findings suggest that and Topp 1999; Kautz et al. 2000;Laaksoetal.2000; unidirectional facilitation of omnivorous semi-terrestrial Zimmer et al. 2003;Airaetal.2008), and with other crabs by their detritivorous prey (saltmarsh snails) promotes detritivores (e.g., Gonzalez and Seastedt 2001; Jonsson the decomposition of low-quality (pine) litter. On high-quality et al. 2001;Bradfordetal.2002;DeDeynetal.2003; (oak) litter, by contrast, negative effects of the predator pre- Jonsson and Malmqvist 2003; Wright and Covich 2005; vail, resulting in a drop of decomposition rates when crabs Zimmer et al. 2005; Bobeldyk and Ramirez 2007). Top-down effects of predators on detritivores, and thus on decomposition processes, have been studied as well (e.g., Lawrence and Wise Christine Ewers and Anika Beiersdorf contributed equally. : : 2000, 2004; Wu et al. 2011), but rarely have omnivorous C. Ewers A. Beiersdorf M. Zimmer detritivores, feeding on both detritus and other detritivores, Zoologisches Institut, Christian-Albrechts-Universität zu Kiel, been considered in this respect. Am Botanischen Garten 9, 24118 Kiel, Germany Some models predict that omnivory will desta- : bilize dynamics (Pimm and Lawton 1977, 1978; K. Więski S. C. Pennings Holt and Polis 1997), while others suggest that omnivory Department of and Biochemistry, University of Houston, can be stabilizing in some circumstances (Matsuda et al. Houston, TX 77204, USA 1986; Fagan 1997; McCann and Hastings 1997). The result- M. Zimmer (*) ing uncertainty underscores the need for detailed studies of FB Organismische Biologie, AG Ökologie, trophic interactions of omnivores and their prey and how Biodiversität & der Tiere, Paris-Lodron-Universität, they affect processes (Diehl 2003;Arimand Hellbrunner Str. 34, 5020 Salzburg, Austria Marquet 2004; van de Wolfshaar et al. 2006). To this end, e-mail: [email protected] effects of omnivores in detrital food webs may differ from those in food webs because herbivores usually compounds. To this end, these detritivores cannot be induce defences of , reducing quality regarded as functionally redundant with respect to decom- (Grime et al. 1996; Cornelissen et al. 2002), whereas detri- position processes. Owing to its wide range of activity along tivores may increase food quality of detritus by fragmenting the marine-terrestrial gradient and its omnivorous feeding litter or enhancing microbial activity (c.f. Zimmer et al. strategy, Armases cinereum may be of particular signifi- 2004). As has been shown for the interaction of endogean cance in this as an that transports matter and epigean woodlice (Zimmer et al. 2005), the and energy between intertidal and terrestrial mutual effects of different detritivores depend upon the (Zimmer et al. 2004). decomposability of the litter. To gain more insight into interactions between detritivores We examined the effects of an omnivorous detritivore on and omnivores during the decomposition of spatial subsidies, decomposition processes in saltmarshes on the Atlantic we studied the individual and joint effects of detritivores and of the United States. A limited number of macro- omnivores on mass loss of two types of terrestrially-derived are involved in decomposition process- litter in high-marsh . We hypothesized that (1) preda- es in saltmarshes (Rietsma et al. 1982; Valiela et al. 1984; tion by the omnivorous Armases impairs both (a) leaf litter Zimmer et al. 2004). Among these, the periwinkle Littoraria mass loss and (b) survival of detritivorous snails, while, in irrorata (Gastropoda: Prosobranchia), the coffeebean turn, (2) the omnivorous Armases benefits from the presence Melampus bidentatus (Gastropoda: Pulmonata), and the of snails because they provide an alternate food source; to this wharf Armases cinereum (Crustacea: Decapoda) are end, we expected Armases to reduce snail-mediated decom- particularly abundant along the North American Atlantic position rates and to gain more mass from feeding on snails coast (Lee and Silliman 2006; Buck et al. 2003; Zimmer et than on detritus. However, (3) the significance of predator/ al. 2004). Past studies have investigated competitive inter- prey-interactions will depend on the quality of the litter as actions between Littoraria and Melampus (Lee and Silliman food source for the omnivorous predator; thus, we expected 2006). Here, we consider how interactions between snails Armases to gain more from the presence of detritivorous snails (as a group) and Armases might mediate decomposition. when low-quality detritus (pine) was available. Armases is an omnivore that not only feeds on detritus and plants (Pennings et al. 1998; Zimmer et al. 2004) but also preys upon other (Buck et al. 2003; Ho and Pennings Material and Methods 2008). Thus, Armases may exert contrasting effects on salt- marsh decomposition processes: through feeding on leaf litter, Study Site and Species it may accelerate litter mass loss, but through intra- predation on detritivores, it may simultaneously decelerate All field work was done at Sapelo Island, Georgia, U.S.A. litter mass loss. (31°27′ N; 81°15′W). Saltmarshes around this island are In most studies of decomposition in saltmarshes, the typical of the southeastern U.S. Atlantic Coast (Pomeroy focus has been on autochthonous detritus derived from salt- and Wiegert 1981). There, terrestrial habitats immediately marsh angiosperms (Newell and Bärlocher 1993; Newell adjacent to the marsh are usually dominated by trees, espe- 2001a, b; Silliman and Zieman 2001; Silliman and Newell cially live oak (Quercus virginiana), loblolly pine (Pinus 2003). In the upper marsh, where semi-terrestrial and even taeda) and juniper (Juniperus virginiana). The branches of terrestrial detritivores are abundant and contribute to decom- these trees often hang several meters out over the high position processes (Rietsma et al. 1982; Valiela et al. 1984; marsh, and consequently drop large amounts of leaf litter Zimmer et al. 2002), significant amounts of leaf and needle as spatial subsidies into the high marsh system. The result- litter from trees that border the marsh spatially subsidizes ing ecotonal transition (marine-terrestrial) zone is common the high-intertidal region (Zimmer and Pennings, personal along the landward margin of many North Atlantic coastal observations). Only a few studies, however, have examined saltmarsh systems. the interactions between semi-terrestrial detritivores and The snails Littoraria irrorata and Melampus bidentatus terrestrial detritus in saltmarshes. In laboratory microcosms are the most abundant macro-gastropods in saltmarshes on with litter from different saltmarsh and woody plant species the Atlantic and Gulf of the United States. Littoraria that differ in their quality as food for detritivores (Zimmer et is most abundant at lower latitudes (Silliman and Zieman al. 2002, 2004), isopods, snails and crabs exhibited species- 2001). Melampus occurs along the entire U.S. East coast, specific effects on litter chemistry and on the activity of but its densities are suppressed at many low-latitude sites litter-colonizing microbiota: Melampus improved the quali- due to negative interactions with Littoraria (Lee and Silliman ty of litter as substrate for decomposition through promoting 2006). Both feed on microalgae and particulate microbial activity; by contrast, feeding by Armases resulted on the marsh surface (Daiber 1977;Thompson1984)andon in the accumulation of and several phenolic leaf litter of angiosperms that grow in the saltmarsh and Wetlands adjacent woods (Zimmer et al. 2004). At high densities, Field Mesocosm Experiments Littoraria will also graze and suppress live plants (Silliman and Zieman 2001; Silliman and Newell 2003). Although it We examined interactions between detritivores and detritus would have been interesting to explore species-specific inter- in the field using mesocosms. Work was done in the field in actions between Armases and snails, we chose to include both order to obtain the most natural abiotic conditions as possible. snail species together in the “snail” treatment as a more Litter and animals were enclosed in mesocosm cages in order logistically-tractable first step towards understanding these to prevent leaf litter from washing away with the tides, main- interactions. tain snails and crabs at fixed initial densities, and prevent other The wharf crab Armases (Sesarma) cinereum is a common detritivore or predator species from affecting the results. Mes- high-marsh omnivore (Teal 1958;Abele1992;Bucketal. ocosms were constructed of plastic tubs (33 cm long×27 2003). It is a semi-terrestrial crab that ranges throughout the wide×15 deep) with window screen covering the bottoms to >100 m inland (Seiple 1979;Penningsetal. and tops, and were buried 12 cm deep in the saltmarsh sedi- 1998), feeding on a wide variety of foods including live ment thus leaving solid wall of 3 cm above ground. The leaves, leaf litter, fungi, small and marsh sedi- window screen prevented large detritivores from entering or ments (Pennings et al. 1998;Zimmeretal.2004;Hoand leaving the tubs and new litter from falling in, but allowed Pennings 2008). Although it readily eats a variety of inverte- exchange of and air with the surrounding environment. brate prey, Armases has weak chelae compared with predatory The was replaced in the tubs after being sorted by hand to crabs, and has difficulty feeding on gastropods (Buck et al. remove both large pieces of detritus and macro-invertebrates. 2003). In the laboratory, Armases was better able to consume The mesocosms were placed in the upper zone of the salt- Melampus, which is relatively small and has a weak shell, than marsh at the South end of Sapelo Island, within 3 m of the Littoraria, which is larger, with a thicker shell, although some terrestrial border, under the canopy of oak trees. Littoraria were consumed (Buck et al. 2003). Mesocosms (N08 for each treatment) contained either 5.0± Detritivores were collected by hand 1 day before the 0.1 g of dried oak litter or 5.2±0.2 g of dried pine litter. Litter experiment started. Littoraria was collected from stems of was evenly spread over the mesocosm area and placed directly Spartina or Juncus in the high-intertidal marsh, Melampus on the soil. In addition to animal-free controls, we set up litter from dead oak leaves in the high-intertidal marsh, and mesocosms that harboured the naturally co-existing detritivores Armases from the surface of high-intertidal marsh sites. We in close-to-natural densities (c.f. Zimmer et al. 2004), thus, collected only male Armases with an average carapace width either 5 Littoraria and 15 Melampus (detritivores: D), or 1 of 18±4 mm (mean ± SD), in order to prevent any effect of Armases (omnivorous predator: A), or a combination of both reproductive activity on interspecific interactions. The shell (DA). Further, litter-free mesocosms served to control for the height of Littoraria averaged 14.5±0.8 mm and of Melampus effect of litter on the performance of detritivores (D) and 5.4±0.4 mm. These size classes are representative of average omnivorous predators (A) or both together (DA). adult sizes encountered in the field. Initial body mass of Mesocosms were stocked and the experiment ran for animals was determined before stocking the mesocosms. 22 days, representing a time interval during which both The leaf litter of oak and pine was collected over several mass gain of animals and mass loss of litter were big enough weeks in spring 2007 in mesh baskets placed below trees to to be detected but that prevented unnaturally high mortality prevent shed leaves from falling onto the ground, which owing to potentially unfavourable conditions in closed mes- limited decomposition prior to our study. Litter was returned ocosms. At the end of the experiment, we re-weighed crabs to the laboratory and air dried for several days at room and live snails (whole-body mass, assuming little shell . According to Zimmer et al. (2004), we consid- growth within 3 weeks), and dried (60 °C for 3 d) and ered oak litter high in quality to detritivores, since growth weighed any remaining litter. rates, mortality, activity and C/N ratios of different consum- We did not test for cage effects (c.f. Schmitz 2004)by ers (including Armases, Littoraria and Melampus) on oak including open cages, since our enclosure approach in a highly were similar to those on Juncus and Spartina, the latter dynamic intertidal system did not allow for the same control commonly being considered rather high quality. By contrast, through open cages as exclosure experiments do. In cage the C/N ratio of pine is by 30 % greater than of Juncus or controls, the tides would have washed litter away, all the oak (Zimmer et al. 2002). In terms of hydrolyzable , species would have migrated away, and other species oak and pine do not differ in content, both containing ca. (racoons, egrets, other crabs) would have affected the results. six-times more than Juncus; however, pine contains about twice as much condensed tannins, that are known to partic- Statistics ularly impair detritivores (e.g., Zimmer and Topp 1997), than oak (Zimmer et al. 2002). Thus, we considered pine We present untransformed data in box-plots, depicting the litter a low-quality food source. range (minimum and maximum) and the first, second Wetlands

(median) and third quartile of data. However, data were Table 1 Summary of ANOVA for effects of litter type, detritivores transformed to meet the prerequisites of homoscedasticity and predators on litter mass loss where necessary for three way-ANOVA with factors litter Source SS df F p (oak versus pine), detritivores (absent versus present) and predators (absent versus present) and subsequent Tukey Model 2,597 7 4,749 <0.001 pair-wise post hoc comparison. Constant 17,851 1 228,471 <0.001 Litter 0,292 1 3,732 0.058 Snails 0,419 1 5,366 0.024 Results Crabs 0,176 1 2,258 0.139 Litter × Snails 0,086 1 1,095 0.300 Irrespective of the litter type and the presence or absence of Litter × Crabs 0,378 1 4,841 0.032 snails or crabs, litter lost mass over 3 weeks in all meso- Snails × Crabs 0,117 1 1,501 0.226 cosms (Fig. 1). Overall, marginal effects of litter type and Litter × Snails × Crabs 1,129 1 14,449 <0.001 significant effects of detritivorous snails on litter mass loss (Table 1) depended on each other and on the presence of omnivorous crabs (litter x detritivore x predator interaction: rapid growth of Armases in this treatment (Fig. 2). Mass change Table 1) (Fig. 1a). To this end, neither snails (p00.58) nor of Armases wasaffectedbyboththelittertypeandthepresence crabs (p00.64) alone significantly affected mass loss of pine of detritvorous snails (litter × detritivore interaction: Table 2): litter (Fig. 1b). When both snails and crabs were present, Armases didnotsignificantlyincreaseinmassintheotherfive however, pine litter mass loss was almost twice as high as in treatments (test versus zero, p>0.4 in all cases), but grew well animal-free controls (p<0.01). Snails alone tended to eat on the pine litter diet when snails were present (p<0.01). slightly more oak than pine litter (Fig. 1a vs. 1b, p00.06). Accordingly, mortality of both Littoraria and Melampus was When snails and crabs were both present, mass loss of pine strongly affected by the presence of Armases (Fig. 3), suggest- was significantly greater than mass loss of oak (p<0.01). ing predatory interactions between crabs and snails (Table 3). The high rate of pine litter mass loss when both detritivorous Snail mortality was independent of litter type (p>0.4). snails and omnivorous crabs were present was accompanied by

Discussion 1.6 a: oak p<0.01 1.4 Our results indicate that detritivorous snails and omnivorous 1.2 b,c crabs through their interaction influence the decomposition b 1.0 of terrestrial leaf litter in the upper saltmarsh. In many North a,c 0.8 a Atlantic saltmarsh systems, this spatial subsidy significantly 0.6 mass loss (g) contributes to fluxes in this marine-terrestrial 0.4 . 0.2 0.0 no animals snails crabs snails & crabs 1.2 Armases b 1.0 1.6 b: pine p=0.01 0.8 1.4 ** a 0.6 1.2 0.4 ns 1.0 a 0.2 ns 0.8 a 0.0

0.6 (g) change mass mass loss (g)mass -0.2 0.4 -0.4 0.2 -0.6 0.0 no snails snails no snails snails no snails snails no animals snails crabs snails & crabs control oak pine

Fig. 1 Mass loss of oak (a) and pine (b) litter when either no animals, Fig. 2 Mass change of Armases in detritus-free controls, on oak litter detritivorous snails or omnivorous crabs, or both snails and crabs were or pine litter, either alone (“no snails”) or with potential prey (“snails”). present, with overall significance of means comparisons (ANOVA). Box plots indicate minimum and maximum, median, and first and third Box plots indicate minimum and maximum, median, and first and third quartile; asterisks and lower case letters designate statistical differences quartile; different lower case letters designate significant differences between “no snails” and “snails” treatment (ns not significant; **: between treatments (α00.05; post-ANOVA Tukey test) p<0.01; post-ANOVA Tukey test) Wetlands

Table 2 Summary of ANOVA for effects of litter type and detritivore Table 3 Summary of ANOVA for effects of litter type and predator presence on mass change of predators presence on mortality of (a) Littoraria and (b) Melampus

Source SS df F p Source SS df F p

Model 0,540 5 2,115 0.096 (a) Constant 0,229 1 4,485 0.044 Model 26,417 5 2,657 0.036 Litter 0,109 2 1,071 0.357 Constant 102,083 1 51,347 <0.001 Snails 0,097 1 1,891 0.181 Litter 3,792 2 0,954 0.394 Litter × Snails 0,347 2 3,393 0.049 Crabs 18,750 1 9,431 0.004 Litter × Crabs 3,875 2 0,975 0.386 (b) When alone, both crabs and snails increased decomposi- Model 442,417 5 7,530 <0.001 tion of oak litter, but the combination of crabs and snails had Constant 5852,083 1 498,050 <0.001 no effect on decomposition, probably because Armases fed Litter 15,792 2 0,672 0.516 less on oak when snails were available as prey (crab preda- Crabs 420,083 1 35,752 <0.001 tion on Littoraria was only significant on oak litter), and Litter × Crabs 6,542 2 0,278 0.758 because snail densities were thus suppressed. To this end, our hypotheses (1) that predation by the omnivorous Armases impairs both leaf litter mass loss and survival of and supported the highest growth rates of Armases, when detritivorous snails, and (2) that the omnivorous Armases both detritivores and omnivores were present. Our present benefits from the presence of snails were confirmed. By results do not allow for any rigorous explanation for this contrast, neither crabs nor snails alone increased decompo- effect, in particular not for the obvious difference in detri- sition of pine litter, but pine litter was decomposed rapidly, tivore/omnivore interactions among litter types, but it is tempting to speculate that snails increased the nutritional quality of pine litter (but not of oak litter) for Armases by 5 a: Littoraria promoting microbial conditioning of the litter. From our

4 hypothesis (3) that the significance of predator/prey-inter- ns actions depends on the quality of the litter as food source for 3 the omnivorous predator, we had predicted that Armases would gain more from the presence of detritivorous snails 2 ** when low-quality detritus is available. However, we consider mortality (N) ns it unlikely that increased predation when only low-quality 1 detritus was available accounted for this, since snail mortal-

0 ity was affected by the litter type only in that Littoraria no crabs crabs no crabs crabs no crabs crabs mortality increased through the presence of crabs on high- control oak pine quality oak litter (Fig. 3a), but litter type proved insignificant 18 (ANOVA: p>0.4; Table 3). Detailed mechanistic studies b: Melampus 16 would be required to unambiguously determine what the 14 mechanisms were that produced these results. 12 When omnivorous crabs were present, >90 % of Melampus 10 ** ** (*) but less than 50 % of Littoraria died during the course of the 8 experiment. Since mortality was significantly lower (on aver-

mortality (N) mortality 6 age (median) 30–60 % of Melampus and no Littoraria) when 4 predators were absent, we consider this observed mortality 2 either due to predation or to indirect effects of predator pres- 0 no crabs crabs no crabs crabs no crabs crabs ence (Preisser et al. 2005). The relatively small, weak-shelled control oak pine Melampus suffered more from encounters with Armases than Fig. 3 Mortality of Littoraria (a) and Melampus (b) in detritus-free the larger, strong-shelled Littoraria, as has been shown earlier controls, on oak litter or pine litter, either alone (“no crabs”) or with (Buck et al. 2003). We cannot, however, exclude the possibility their omnivorous predator (“crabs”). Box plots indicate minimum and that some mortality of Melampus, particularly in the absence of maximum, median, and first and third quartile; asterisks and lower crabs, was due to Littoraria exerting negative effects on its case letters designate statistical differences between “no crabs” and “crabs” treatment (ns not significant; (*): 0.05

Melampus, and experimental addition of the former resulted in Zucoloto 2001), in particular for detritivores that feed on a migration of the latter off the high marsh (Lee and Siliman low-quality food source (Rice 1982). Accordingly, we had 2006). Alternatively, some essential food sources may have expected Armases –an omnivore in saltmarshes and adjacent been missing from our treatments (c.f. Zimmer et al. 2004, coastal woods that feeds on a wide array of food sources, presenting low growth rates of Melampus on single-species including saltmarsh detritus and detritivorous snails and diets in lab microcosms). A more straightforward interpretation (Buck et al. 2003;Zimmeretal.2004)– to of our findings might have been possible, had we studied the perform better when both detritus and potential prey were interactions of omnivorous crabs and detritivorous snails available than when only detritus was offered. However, the separately for snail species. However, we did initially not present results clearly show that the better performance of aim in this direction but were rather interested in close-to- Armases in the presence of detritivorous snails was not natural systems consisting of the most common detritivores (solely) caused by predation, as mortality rates of snails in (i.e. Littoraria and Melampus) and their potential predator. the presence of Armases were independent of the litter type. From the present data, there is no straightforward expla- We did observe predation on snails by Armases; however, nation of how snails could have facilitated Armases when this was not the reason for better performance of the pred- 50–90 % of the initially present individuals died during the ator, because Armases did not grow better on a diet of oak experiment. One possibility is that the promoting effects of when snails were also available. Instead, the presence of Melampus on microbial activity (Zimmer et al. 2004) lasted snails on low-quality pine detritus must have enhanced the after many Melampus died. Alternatively, most of the facil- nutritional value of the detritus and made predator mass gain itation may have been brought about by Littoraria, which possible. Zimmer et al. (2004) observed increased microbial had fairly high survival rates (>50 % in all treatments). activity on leaf litter (including oak) when either Melampus We cannot unambiguously exclude the possibility that (on all tested litter types) or Littoraria (on three out of five increased mass loss of pine litter was due to compensatory litter types) were present; possibly snail mucus left on the feeding by Armases on this low-quality food source. How- litter surface promoted litter-colonizing microbes, or snail ever, we consider it unlikely that compensatory feeding on a feeding increased access by microbes to leaf material. Based food source of such low quality (c.f. Zimmer et al. 2002) on our present findings, we speculate that this effect of would result in two-times higher growth rates than non- snails can increase the nutritional value of low-quality compensatory feeding on a food source of distinctly higher detritus for other consumers. quality (Fig. 2, c.f. Zimmer et al. 2002, 2004), the more so Although oak litter, in contrast to pine, is palatable as crabs did not significantly increase mortality of Littoraria enough to be consumed and to allow for at least basal on pine and litter type did not significantly affect mortality performance of Armases, snail activity did not increase the of Melampus. Further, it is also unlikely that a low-quality nutritional value of oak litter to Armases, and the combination food source would be consumed at compensating rates when of snails and Armases did not result in a promotion of decom- a high-quality food source (snail prey) was also available, position processes. To the contrary, Armases sharply dimin- and according to our results, both crabs and snails ate more ished the effect of snail activity on oak decomposition (litter oak than pine when alone, although neither snails nor mass loss) to a level that did not differ from detritivore-free Armases grew significantly better on oak than on pine in controls. It is interesting to speculate whether this was owing to single- treatments. By contrast, when both snails reduced snail activity in the presence of crabs (A. Beiersdorf and crabs were present and presumably engaged in a com- and C. Ewers, pers. obs.; c.f. Preisser et al. 2005), but detailed bination of competitive and predator–prey interactions, studies will be needed to clarify this issue. Armases –but not the snails– gained the most mass on a In contrast to the present results, Zimmer et al. (2005) pine litter diet. Consistent with this result, crab/snail-inter- observed synergistic intra-guild interactions of detritivores actions promoted decomposition (litter mass loss) of pine (woodlice and earthworms) on a high-quality food source (but not oak) litter. Facilitation is generally considered to be (alder litter), while on oak litter (low to intermediate quality) of particular significance under unfavourable environmental these detritivores had additive effects on various decompo- conditions (Bertness and Callaway 1994), and our findings sition parameters. These authors suggested reciprocal facil- are consistent with this general theory. itation on high-quality but on low-quality food Since animals have a higher nitrogen content and a nar- sources. Our present results indicate unidirectional facilita- rower C:N ratio than plants (Mattson 1980; Matsumura et al. tion of a predacious omnivore (Armases) by its detritivorous 2004), consumers of vegetal biomass are usually nitrogen- prey (Littoraria and Melampus) on low-quality food that limited (White 1993; Awmack and 2002). Thus, resulted in synergistic effects on ecosystem processes. supplementing a plant diet with additional nitrogen from Taken together, the present results indicate a complex set higher trophic levels may offset the fundamental mismatch of interactions between detritivorous snails and their omniv- between nitrogen demand and supply (Barros-Bellanda and orous predator that range from predation with negative Wetlands effects on decomposition of high-quality detritus to Barros-Bellanda HCH, Zucoloto FS (2001) Influence of chorion ingestion (unidirectional) facilitation with positive effects on decom- on the performance of Ascia monuste and its association with – position of low-quality detritus. Such complex interactions . Ecological Entomology 26:557 561 Bertness MD, Callaway R (1994) Positive interactions in . of detritivores and omnivores may be of utmost significance Trends in Ecology & Evolution 9:191–193 for the processing of detritus and deserve detailed consider- Bless R (1977) Beitrag zur Ernährungsweise ausgewählter Nacktsch- ation in other studies of decomposition processes. Preda- neckenarten des Naturparks Kottenforst-Ville. Journal of Pest – cious detritivores are common in various systems. In Science 50:1612 4758 Bobeldyk AM, Ramirez A (2007) Leaf breakdown in a tropical headwater freshwaters, are known to feed on both detritus stream (Puerto rico): the role of freshwater and detritivorous and detritivores (Nisikawa 2000; Evans-White and Dodds . Journal of Freshwater Ecology 22:581–590 2003; Zhang et al. 2004). Caddisflies are frequently consid- Bradford MA, Jones TH, Bardgett RD, Black HIJ, Boag B, Bonkowski ered omnivores that directly (through consuming detritus) M, Cook R, Eggers T, Gange AC, Grayston SJ, Kandeler E, McCaig AE, Newington JE, Prosser JI, Setälä H, Staddon PL, and indirectly (through preying upon detritivores) mediate Tordoff GM, Tscherko D, Lawton JH (2002) Impacts of soil decomposition processes (Rosi-Marshall and Wallace faunal composition on model ecosystems. 2002). A similar role has been assigned to in the Science 298:615–618 terrestrial realm (Bless 1977), and have long Buck TL, Breed GA, Pennings SC, Chase ME, Zimmer M, Carefoot TH (2003) Diet choice in an omnivorous salt-marsh crab: different food been considered to be at least occasionally carnivorous in types, body size, and habitat complexity. Journal of Experimental addition to detritivorous (Hoffman and Payne 1969). Marine Biology and Ecology 292:103–116 Whether the conclusions we draw from the present results Cebrian J (1999) Patterns in the fate of production in plant communities. – from a saltmarsh also apply to other omnivorous detritivores American Naturalist 154:449 468 Cornelissen JHC, Pérez-Harguindeguy N, Díaz S, Grime JP, Marzano remains an open question that warrants detailed comparative B, Cabido M, Vendramini F, Cerabolini B (2002) Leaf structure studies of other detritivore-predator systems. However, the and defence control litter decomposition rate across species and results suggest that complicated food web interactions within forms in regional floras on two continents. New Phytologist – detrital food webs, that are dependent on litter quality, may 143:191 200 Daiber FC (1977) Salt-marsh animals: Distributions related to tidal mediate the impact of omnivores within these food webs. flooding, salinity and . In: Chapman VJ (ed) Wet coastal Although understanding context-dependent interactions is ecosystems. Elsevier, Amsterdam, pp 79–108 complicated, it may provide an important key to understanding De Deyn GB, Raaljmakers CE, Zoomer HR, Berg MP, de Rulter PC, variation in the rates of litter decomposition across space and Verhoef HA, Bezemer TM, van der Putten WH (2003) Soil invertebrate fauna enhances grassland succession and diversity. time. Nature 422:711–713 Diehl S (2003) The evolution and maintenance of omnivory: dynamic constraints and the role of food quality. Ecology 84:2557–2567 Acknowledgements Experiments described herein comply with the Evans-White MA, Dodds WK (2003) Ecosystem significance of cray- current of the U.S.A. and were conducted in conformity with the fishes and stonerollers in a prairie stream: functional differences “Guiding principles in the care and use of animals” approved by the between co-occurring omnivores. Journal of the North American Council of the American Physiological Society. AB and CE were Benthological Society 22:423–441 financially supported through grants from the Christian-Albrechts- Fagan WF (1997) Omnivory as a stabilizing feature of natural Universität zu Kiel. Franziska Seer, Gregor Putze and Yury Zablotski communities. American Naturalist 150:554–567 provided invaluable assistance at all stages of the field work. We thank Gonzalez G, Seastedt TR (2001) Soil fauna and decomposition the U.S. National Science Foundation (OCE06-20959) for financial in tropical and subalpine . Ecology 82:955–964 support. This is contribution number 1017 of the University of Georgia Grime JP, Cornelissen JHC, Thompson K, Hodgson JG (1996) Marine Institute. This work is a contribution of the Georgia Coastal Evidence of a causal connection between anti-herbivore defence Ecosystems LTER program. and the decomposition rate of leaves. Oikos 77:489–494 Ho CK, Pennings SC (2008) Consequences of omnivory for trophic interactions on a shrub. Ecology 89:1714–1722 Hoffman RL, Payne JA (1969) Diplopods as . Ecology References 50:1096–1098 Holt RD, Polis GA (1997) A theoretical framework for . American Naturalist 149:745–764 Abele LG (1992) A review of the grapsid crab genus Sesarma (Crus- Jonsson M, Malmqvist B (2003) Mechanisms behind positive diversity tacea: Decapoda: Grapsidae) in America, with the description of effects on ecosystem functioning: testing the facilitation and a new genus. Smithsonian Contributions to Zoology, Number interference hypotheses. Oecologia 134:554–559 527, Washington, DC Jonsson M, Malmqvist B, Hoffsten PO (2001) Leaf litter breakdown Aira M, Sampedro L, Monroy F, Domínguez J (2008) Detritivorous earth- rates in boreal streams: does shredder matter? directly modify the structure, thus altering the functioning of a Freshwater Biology 46:161–171 microdecomposer food web. and Biochemistry Kautz G, Zimmer M, Topp W (2000) Responses of the parthenogenetic 40:2511–2516 isopod, Trichoniscus pusillus, to changes in food quality. Arim M, Marquet PA (2004) Intraguild predation: a widespread interaction Pedobiologia 44:75–85 related to species biology. Ecology Letters 7:557–564 Laakso J, Setälä H, Palojärvi A (2000) Influence of food Awmack CS, Leather SR (2002) Host plant quality and fecundity in web structure and nitrogen availability on plant growth. Plant and herbivorous insects. Annual Review of Entomology 47:817–844 Soil 225:153–165 Wetlands

Lawrence KL, Wise DH (2000) predation on -floor ecosystems. In: Weisser WW, Siemann E (eds) Insects and Collembola and evidence for indirect effects on decomposition. Ecosystem Function, Springer Series in Ecological Studies. Pedobiologia 44:33–39 Springer-Verlag, Berlin, pp 277–302 Lawrence KL, Wise DH (2004) Unexpected indirect effect of Seiple W (1979) Distribution, habitat preferences and breeding on the rate of litter disappearance in a deciduous forest. Pedobiologia periods in the crustaceans Sesarma cinereum and S. reticula- 48:149–157 tum (Brachyura: Decapoda: Grapsidae). Marine Biology Lee SC, Silliman BR (2006) Competitive displacement of a detritivorous 52:77–86 salt marsh snail. Journal of Experimental Marine Biology and Silliman BR, Newell SY (2003) Fungal farming in a snail. Proceedings Ecology 339:75–85 of the National Academy of Sciences of the United States of Matsuda H, Kawasaki K, Shigesada N, Teramoto E, Ricciardi LM America 100:15643–15648 (1986) Switching effect on the stability of the prey-predator Silliman BR, Zieman JC (2001) Top-down control of Spartina alterniflora system with three trophic levels. Journal of Theoretical Biology production by periwinkle in a Virginia salt marsh. Ecology 122:251–262 82:2830–2845 Matsumura M, Trafelet-Smith GM, Gratton C, Finke DL, Fagan WF, Teal JM (1958) Distribution of fiddler crabs in Georgia salt marshes. Denno RF (2004) Does intraguild predation enhance predator Ecology 39:185–193 performance? A stoichiometric perspective. Ecology 85:2601– Teal JM (1962) Energy-flow in salt-marsh ecosystem of Georgia. 2615 Ecology 43:614 Mattson WJ (1980) Herbivory in relation to plant nitrogen-content. Thompson LS (1984) Comparison of the diets of the tidal marsh snail, Annual Review of Ecology and Systematics 11:119–161 Melampus bidentatus and the amphipod, Orchestia grillus. McCann K, Hastings A (1997) Re-evaluating the omnivory-stability 98:44–53 relationship in food webs. Proceedings of the Royal Society of Valiela I, Wilson J, Buchsbaum R, Rietsma C, Bryant D, Foreman K, London Series B-Biological Sciences 264:1249–1254 Teal J (1984) Importance of chemical composition of salt marsh Newell SY (1996) Established and potential impacts of eukaryotic litter on decay rates and feeding by detritivores. Bulletin of mycelial in marine/terrestrial . Journal of Marine Science 35:261–269 Experimental Marine Biology and Ecology 200:187–206 van de Wolfshaar KE, de Roos AM, Persson L (2006) Size-dependent Newell SY (2001a) Fungal biomass and in standing- interactions inhibit coexistence in intraguild predation systems decaying leaves of black needlerush (Juncus roemerianus). Marine with life-history omnivory. American Naturalist 168:62–75 and Freshwater Research 52:249–255 White TCR (1993) The inadequate environment. Springer, Berlin Newell SY (2001b) Multiyear patterns of fungal biomass dynamics and Wright MS, Covich AP (2005) Relative importance of and productivity within naturally decaying smooth cordgrass shoots. fungi in a tropical headwater stream: leaf decomposition and Limnology and Oceanography 46:573–583 invertebrate feeding preference. 49:536–546 Newell SY, Bärlocher F (1993) Removal of fungal and total organic- Wu X, Duffy EJ, Reich PB, Sun S (2011) A brown-world cascade in matter from decaying cordgrass leaves by shredder snails. Journal the dung decomposer food web of an alpine meadow: effects of of Experimental Marine Biology and Ecology 171:39–49 predator interactions and warming. Ecological Monographs 81: Nisikawa U (2000) Effects of crayfish on leaf processing and invertebrate 313–328 colonisation of leaves in a headwater stream: decoupling of a trophic ZhangY,RichardsonJ,NegishiJN(2004) Detritus processing, ecosystem cascade. Oecologia 124:608–614 engineering and benthic diversity: a test of predator-omnivore Pennings SC, Carefoot TH, Siska EL, Chase ME, Page TA (1998) interference. Journal of Animal Ecology 73:756–766 Feeding preferences of a generalist salt-marsh crab: relative Zimmer M, Topp W (1999) Relations between woodlice (: importance of multiple plant traits. Ecology 79:1968–1979 Oniscidea), and microbial density and activity in the field. Biology Pimm SL, Lawton JH (1977) Number of trophic levels in ecological and Fertility of 30:117–123 communities. Nature 268:329–331 Zimmer M, Pennings SC, Buck TL, Carefoot TH (2002) Species- Pimm SL, Lawton JH (1978) Feeding on more than one . specific patterns of litter processing by terrestrial isopods Nature 275:542–544 (Isopoda: Oniscidea) in high intertidal salt marshes and coastal Pomeroy LR, Wiegert RG (1981) The ecology of a salt marsh. Springer, forests. 16:596–607 New York Zimmer M, Kautz G, Topp W (2003) Leaf litter-colonizing microbiota: Preisser EL, Bolnick DI, Benard MF (2005) Scared to ? The supplementary food source or indicator of food quality for Porcellio effects of intimidation and consumption in predator-prey interactions. scaber (Isopoda: Oniscidea)? European Journal of Soil Biology Ecology 86:501–509 39:209–216 Rice DL (1982) The detritus nitrogen problem - new observations and Zimmer M, Pennings SC, Buck TL, Carefoot TH (2004) Salt marsh perspectives from organic geochemistry. Marine Ecology- litter and detritivores: a closer look at redundancy. Progress Series 9:153–162 27:753–769 Rietsma CS, Valiela I, Sylvester-Serianni A (1982) Food preferences of Zimmer M, Kautz G, Topp W (2005) Do woodlice and earthworms dominant salt marsh herbivores and detritivores. Marine Ecology interact synergistically in leaf litter decomposition? Functional 3:179–189 Ecology 19:7–16 Rosi-Marshall EJ, Wallace JB (2002) Invertebrate food webs along a Zimmer M, Topp W (1997) Does leaf litter quality influence popula- stream resource gradient. Freshwater Biology 46:129–141 tion parameters of the common , Porcellio scaber Latr., Schmitz OJ (2004) From mesocosms to the field: the role and value 1804 (Crustacea: Isopoda)? Biology and Fertility of Soils 24: of cage experiments in understanding top-down effects in 435–441