Oikos 119: 1785–1795, 2010 doi: 10.1111/j.1600-0706.2010.18537.x

© 2010 Th e Authors. Oikos © 2010 Nordic Society Oikos Subject Editor: Beatrix Beisner. Accepted 10 March 2010

Direct and indirect food web regulation of microbial decomposers in headwater streams

Chad W. Hargrave , Samuel Hamontree and Kaitlen P. Gary

C. W. Hargrave (cwhargrave@shsu.edu), S. Hamontree and K. P. Gary, Center for Biological Field Studies and Dept of Biological Sciences, Sam Houston State Univ., PO Box 2116, Huntsville, TX 77341-2116, USA.

Th e direct and indirect regulation of primary productivity has been well established in autotrophic-based ecosystems; however, less is known about the processes aff ecting decomposers in detrital-based ecosystems. Because, small headwater, woodland streams are a dominate feature in most ecosystems and are tightly linked to terrestrial detritus, understanding decomposer-mediated functions in these systems is critical for understanding carbon processes across the landscape. In this light, we conducted a microcosm and mesocosm experiment to test the direct and indirect food web eff ects on decomposers in small stream ecosystems. Th e results from the microcosm experiment supported an existing literature, demonstrating that nutrients directly stimulate decomposers and that microbivores directly reduce decomposers. Based on well-founded food web theory in autotrophic systems, we predicted that fi shes from diff erent trophic-functional guilds would indi-rectly stimulate decomposers by enhancing dissolved nutrients and by reducing microbivore densities. Our mesocosm experiment partially supported these predictions. Specifi cally, we found that fi shes that consumed mostly terrestrial foods increased decomposers from the bottom – up by enhancing allochthonous nutrient loading into the stream ecosystems. Contrary to our predictions, however, predatory fi shes that consume microbivores did not increase decomposers from the top – down. Rather, in streams with the predatory fi sh species, microbivores increased (rather than decreased) on leaf litter. Th is may have resulted from an experimental artifact associated with refuge provided by leaf packs. In conclusion, our data demonstrate that decomposers are regulated by similar direct and indirect processes important in autotrophic-based ecosystems. Th is provides further evidence that food web processes can regulate leaf decomposition and fl ux of detrital carbon through ecosystems.

In many ecosystems the majority of primary production goes uneaten and, as a result, supports a diverse web of consumer trophic levels linked to these detrital energy resources (Duggins et al. 1989, Polis et al. 1997, Moore et al. 2004). In this ‘ brown food web ’ , the bacteria and fungi (microbes) provide a criti-cal link between detrital carbon (C) and consumer trophic levels (Swift et al. 1979). Th ese microbial decomposer taxa can be viewed much like the autotrophs in ‘ green food webs ’ which link atmospheric CO 2 to grazing and predatory con-sumers (Chen and Wise1999). It is not surprising then that similar bottom – up and top – down processes that regulate autotrophic productivity in many ecosystems also regulate microbial decomposer productivity in detritus-based sys-tems. For example, in forests, where detritus is an abundant energy source, bottom – up nutrient enrichment increases biomass of microbial decomposers, leaf litter invertebrates and accelerates leaf decomposition (Hobbie and Vitouseck 2000, Kaspari et al. 2008). Alternatively, top predators such as spiders, mites and ants can control the abundance of consum-ers that directly eat microbes (i.e. microbivores)(Miyashita and Niwa 2006, Milton and Kaspari 2007). Th is predatory control of the microbivore feeding guild can enhance microbial

decomposer production from the top – down (Lawrence and Wise 2000). Th ese direct and indirect eff ects on decompos-ers are important processes governing the fl ux of detrital C into consumers and back into the atmosphere – an important ecosystem function (Schlesinger 1997).

Small woodland streams are a dominant feature in most terrestrial ecosystems, comprising nearly 70% of most drain-age networks across the earth (Wetzel 2001). Th ese streams are tightly coupled to the terrestrial landscape with resource subsi-dies from the land driving much of the secondary production within these small systems (Baxter et al. 2005). Leaf litter is a principal terrestrial input and is an important energy source for most of the consumers inhabiting woodland streams (Fisher and Likens 1973, Vannote et al. 1980, Wallace et al. 1999). As in terrestrial systems, microbial decompos-ers that colonize leaf litter in these stream systems play an important ecosystem role by linking detrital C to consumers (Findlay and Arsuffi 1989, Suberkropp and Chauvet 1995). Th us, similar bottom – up and top – down processes that aff ect microbial decomposers in terrestrial ecosystems also are likely to regulate these taxa and associated ecosystem functions in headwater streams (Rosemond et al. 2001, Cross et al. 2005).

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Our general knowledge of the processes driving C fl ux across the landscape will be further enhanced by understanding the regulatory processes driving microbial decomposer productivity in these ubiquitous aquatic ecosystems.

Dissolved nutrients and aquatic invertebrate larvae play an important role in the direct regulation of C fl ux from stream detritus into the atmospheric CO 2 pool. For exam-ple, nutrient enrichment of small stream ecosystems stimu-lates microbial decomposers, enhancing stream respiration, leaf litter decomposition and density of invertebrates that feed on decomposers and leaf litter (Elwood et al. 1981, Gulis and Suberkropp 2003, Cross et al. 2006, Greenwood et al. 2007). Because microbial decomposers are directly con-sumed by many aquatic invertebrates (Wallace et al. 1982), predatory control of microbivore invertebrates may enhance rates of decomposer-mediated C fl ux from this detritus into the stream ecosystems. Based on these examples, we posit that, as in the ‘ green food web ’ , higher-order consumers that mediate dissolved nutrient loads and densities of microbi-vore invertebrates in small woodland streams also are likely to indirectly enhance ecosystem functions linked to the ‘ brown food web ’ .

Fishes are prominent large-bodied consumers in many stream ecosystems (Matthews 1998) that directly increase nutrient loads via excretion (Vanni 2002) and reduce inver-tebrate densities via predation (Dahl and Greenberg 1996, Englund et al. 1999). Indirect eff ects of fi shes on primary pro-duction via their direct eff ects on nutrients and grazing inver-tebrates has been well studied in autotrophic-based stream ecosystems (Power 1990, Gido and Matthews 2001, Hargrave 2006). However, the indirect eff ects of fi shes on microbial decomposer productivity in detritus-based stream ecosystems remains relatively novel (but see Konishi et al. 2001, Ruetz et al. 2002). Herein, we conducted two experiments designed to further our general understanding of the direct and indi-rect processes that could drive microbial decomposer produc-tivity on leaf litter detritus in small headwater streams.

We designed a microcosm experiment to test the hypoth-esis that availability of dissolved nutrients and presence of microbivore insects would directly aff ect microbial decom-poser productivity (measured as leaf litter respiration rate). We made two specifi c predictions related to this hypothesis: (1) that nutrient addition would directly enhance decom-poser respiration on leaf litter, and (2) that aquatic insect lar-vae would directly reduce decomposer respiration via direct consumption.

We designed a mesocosm experiment to test the hypoth-esis that three fi sh species from diff erent trophic-functional guilds can aff ect microbial decomposer productivity in small headwater streams through indirect bottom – up and top – down processes. We made three specifi c predictions related to this hypothesis: (1) that a surface feeding fi sh would enhance decomposer respiration from the bottom – up by increasing local nutrients through the consumption of ter-restrial insects and excretion of allochthonous nutrients into the stream ecosystem, (2) that a benthic feeding fi sh would increase decomposer respiration from the top – down by reducing aquatic invertebrate larvae that consume microbial decomposers, and (3) that a watercolumn feeding fi sh would increase decomposer respiration from both the bottom – up and top – down as described above.

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Material and methods

Microcosm experiment – direct effects on microbial decomposer respiration

Experimental setup We tested the direct eff ects of elevated dissolved nutrients and leaf litter insects on microbial decomposer respiration from leaf litter using 24 microcosms. We used 18-l plastic buckets as microcosms, which were maintained in a shaded, greenhouse structure at the Sam Houston State Univ. Center for Biological Field Studies (CBFS, Walker Co., TX, USA). Th is structure was designed to simulate the dense canopy of a small head water stream by blocking 92 � 2% (mean � 1 SD) of the photosynthetic active radiation (PAR) measured outside of the structure at about 12:00 h. On 2 June 2008, all 24 microcosms were fi lled with ∼ 10 l of phosphorus-poor well water ( ∼ 50:1, molar N:P), and inoculated with a 100 ml natural biofi lm slurry taken from the sediments from a stream on CBFS property (Harmon Creek). Each microcosm was then randomly assigned to one of four treatments: (1) low nutrients – low aquatic insects, (2) low nutrients – high aquatic insects, (3) high nutrients – low aquatic insects, and (4) high nutrients – high aquatic insects. Each treatment was replicated six times. Th e low nutrient treatment remained at ambient nutrient levels (28.3 � 7.7 μ mol l �1 N and 0.56 � 0.21 μ mol l �1 P). Dissolved nitrogen and phosphorus was quadrupled in the high nutrient treatment (12 microcosms) by adding ∼ 85 mg of KNO 3 and ∼ 2.3 mg of KH 2 PO 4 to each microcosm within this treatment. Aquatic insect coloniza-tion by ovipositing adults was controlled using insect screen-ing that covered the opening of the 12 microcosms assigned to the low insect treatment. Th e insect screen was standard, fi berglass, window screening, grey in color, with a 1.0 mm mesh. High insect treatments had a control screen that was elevated above the opening of the microcosm with PVC pipe. Th e control screens allowed access to the surface of the water in the microcosms by ovipositing insects while controlling for potential eff ects of the screen barriers. Following the experi-mental set up, the microcosms remained undisturbed for 10 days before adding leaf packs. Th is allowed establishment of biofi lms in all microcosms, and allowed for colonization by terrestrial insect larvae into microcosms assigned to the high insect treatment. Temperature was monitored in three randomly selected microcosms with insect screening and three randomly selected microcosms without insect screen-ing (n � 6) throughout the experiment using temperature loggers.

Microbial decomposers and invertebrates On 12 June 2008, three leaf packs containing 0.6 g (dry weight of about one whole leaf ) of abscised sycamore Platanus occidentalis leaf material was added to each micro-cosm. Leaf packs were made with black polyethylene netting (20 � 10 cm; 0.6 cm mesh) and were weighted to the micro-cosm bottom with a 20 cm steel nail. Th e day leaf packs were added to the microcosms was day 0 of the experiment. On day 35 (17 July 2008), all leaf packs were removed from the microcosms and returned to the laboratory. In the labora-tory, the leaf packs were opened and the decomposing leaf material from each bag was carefully removed.

We fi rst measured respiration rates of the microbial biofi lm on the leaf material (surrogate for microbial decomposer pro-ductivity). To do this, the leaf material was placed in a plas-tic ziploc storage bag with 500 ml of nutrient free, artifi cial stream water, which was made by adding 4.2 g CaCl 2 , 4.2 g MgSO 4 , and 1.5 g NaHCO 3 to about 40 l of reverse osmosis fi ltered water. Th is water was similar in pH (7.5) and con-ductivity (400 μ S) to water used in both the microcosm and mesocosm experiments. When each leaf was added to the bag, the dissolved oxygen concentration of the water was mea-sured using an oxygen meter. All air was then removed from each bag; the bags were sealed, covered with foil and allowed to incubate for about 1 h in the dark. After the incubation, dissolved oxygen of the water was measured, and we used this change in oxygen as an estimate of microbial decom-poser respiration (Bott 1996). To minimize disturbance to the leaf litter biofi lms, we elected not to remove insects from the leaf litter prior to estimating microbial decomposer res-piration. Th erefore, microbial decomposer respiration esti-mates also included any respiration of insects on the leaf litter. Th e additional respiration by invertebrates included with the microbial decomposer respiration estimates had little eff ect on our interpretations of data presented in this report. We elaborate on this argument in the fi nal paragraph of the results section. Temperature in the laboratory where respiration rates were measured was maintained at 25 ° C.

After estimating microbial decomposer respiration rates on each leaf, we removed the biofi lm and any benthic inver-tebrates from the leaf litter by gently scrubbing the leaf and rinsing with distilled water. Th e benthic invertebrates from this slurry were counted and identifi ed to family and in some cases to genus. Th e biofi lm-free leaf material was dried at 60 ° C to a constant mass and weighed to the nearest mg to estimate dry weight for each leaf pack at the end of the experiment. Microbial decomposer respiration rates and leaf litter invertebrates were standardized by fi nal leaf size by dividing each measurement by this fi nal leaf mass. We averaged all replicate leaf pack samples from each microcosm and tested for main treatment and interaction eff ects using proc GLM. Post hoc within treatment means were compared using a Tukey multiple comparisons procedure (SAS 2003).

Mesocosm experiment – indirect effects on microbial decomposers

Experimental setup Using 24 large, outdoor stream mesocosms located at the CBFS, we tested the eff ects of three fi sh species from dif-ferent trophic-functional groups on microbial decomposer respiration, density of leaf litter and sediment-dwelling (hereafter referred to as benthic) invertebrates, and water column nitrogen (N) and phosphorus (P) in a 35 day experi-ment (5 June to 10 July 2007). Th ese fi shes included a sur-face feeding insectivore (blackstripe topminnow, Fundulus notatus ), a benthic omnivore (bullhead minnow, Pimephales vigilax ) and a watercolumn omnivore (blacktail shiner, Cyprinella vensuta ). Th e mesocosms were designed to mimic small, shallow, sand-bottom headwater streams throughout the Gulf coastal slope of North America. Specifi cally, each mesocosm was 4 m long by 1 m wide, had a ∼ 10 cm thick sand substrate, an average water depth of ∼ 0.3 m, and similar

water chemistry to streams in the region (see Hargrave et al. 2009 for a comparison in abiotic and biotic characteristics between a second order Gulf coastal stream (Harmon Creek) and experimental mesocosms). Mesocosms were housed under a shade structure to simulate a dense canopy cover common to small headwater streams. Temperature in each mesocosm was measured throughout the experiment using 24 temperature loggers.

On 21 May 2007, each mesocosm was fi lled with phos-phorus-poor well water from the same source used in the microcosm experiment, and inoculated with a 1 l natural periphyton and biofi lm slurry taken from the sediments from Harmon Creek. Flow (0.12 � 0.2 m s �1 ) was main-tained in each unit using a 3500 l h �1 submersible pump. Streams remained unaltered until 3 June 2007 (13 days) to allow establishment of a biofi lm assemblage and to allow colonization of aquatic insect larvae by ovipositing adults prior to implementing the fi sh treatments. Invertebrates that colonized the stream mesocosms were primarily early succes-sion species, such as chironomid and dragonfl y larvae, and resembled density and biomass of the invertebrate assem-blages found in sand-bottom habitats common to Harmon Creek (Hargrave et al. 2009).

On 3 to 4 June 2007, we collected 100 individuals of all three fi sh species of similar size from creeks near the CBFS. Fishes were transported to the CBFS in insulated boxes for stocking into the mesocosms. At this time, we randomly assigned each mesocosm to one of the three fi sh treatments or to the control treatment (no fi sh). Fish were added to each mesocosm according to treatment designation at a rate of 4 fi sh m �2 (i.e. 16 fi sh per mesocosm). Th is density is at the upper end of natural densities for these fi shes in Harmon Creek during summer and autumn. For example, based on seasonal population estimates over four years (beginning autumn 2006 through 2009) blackstripe topminnow, black-tail shiner and bullhead minnow densities ranged from 0.5 to 5.6 fi sh m �2 (average 2.5 fi sh m �2 ), 1.9 to 7.5 fi sh m �2 (average 4.2 fi sh m� 2 ), and 0 to 4.5 fi sh m �2 (average 1.3 fi sh m �2 ), respectively (Hargrave unpubl.). Each treatment (blackstripe topminnow, bullhead minnow, blacktail shiner, and no fi sh) was replicated six times.

Microbial decomposers and invertebrates On 5 June (day 0), we added four leaf packs containing 0.6 g of abscised sycamore leaf material to each mesocosm. Leaf packs were identical to those described previously. On days 15 and 35 (20 June and 10 July 2007), we randomly removed two leaf packs from each mesocosm. In the labora-tory, the leaf packs were opened and the decomposing leaf material from each bag was carefully removed. For these samples, we measured microbial decomposer respiration, insect density, and fi nal mass of the leaf material, using the same methods described above. Temperature in the labora-tory was maintained at 25 ° C during the leaf litter incubation procedure used to estimate microbial respiration.

We also took two core samples (400 cm 2 ) from each mesocosm on days 0 and 35 to estimate total benthic inver-tebrate density among treatments. To separate invertebrates from sediments, the core samples were placed into a 3-l tub. Th e tub was placed over a 250- μ m sieve and tap water was run into the tub while stirring/disturbing the sediments by

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hand for about 1 minute or until the water was clear of sus-peded insects and particulates. Th e suspended invertebrates and other particulates were captured in the sieve, transferred to a jar and preserved with 5% formalin. Th e invertebrates from each core were counted and identifi ed to family or genus under a dissecting microscope.

Water column nutrients and terrestrial inputs On days 0, 15 and 35, we took water samples from each meso-cosm. Samples were placed on ice returned to the laboratory where we measured total water column phosphorus (P) and total nitrogen (N) using persulfate digestion followed by the ascorbic acid method for P and cadmium reduction method for N (APHA 1998). We estimated rates of insect input for each mesocosm on days 0, 15 and 35 using pan traps (730 cm 2 ) fi lled with a solution of soap and water (South-wood 1978). Pan traps were placed on the stream surface for 48 h, and, after which, retrieved and the contents fi ltered through glass fi ber fi lters. Th is fi ltrand was dried to a con-stant mass and combusted to determine ash free dry mass (AFDM) of terrestrial input on each sample date.

Fish excretion and feeding On day 35, we estimated excretion rates for 20 black-stripe topminnows, 20 blacktail shiners and 19 bull-head minnows. To do this, we removed 3 to 4 fi sh from each mesocosm with a seine and placed each fi sh in a separate container (18 � 11 � 6.5 cm) containing 1 l of nutrient free, artifi cial stream water (described above). Th e fi sh were held in the container undisturbed for about 1 h, after which, a water sample was taken from each con-tainer and stored on ice. Th e fi sh were weighed wet to the nearest mg and preserved in 10% formalin for gut content analysis. Within 12 h, each water sample was analyzed for ammonia and soluble reactive phosphorus using the phen-ate and ascorbic acid method, respectively (APHA 1998). Following excretion estimates, we removed and all remain-ing fi sh from each mesocosm, and preserved all individuals in separate jars per mesocosm with 10% formalin. In the laboratory, we examined the gut contents of four individ-uals per mesocosm. We removed the anterior third of the alimentary tract and placed gut contents on a gridded petri dish. We calculated the proportion of items in the gut by dividing the number of grids occupied by each food type by the total number of grids the contents covered. From these data, we calculated the average proportion of diff erent items consumed for each species.

Statistical analyses To avoid pseudoreplication, all replicate samples per meso-cosm (i.e. leaf packs, core samples, etc.) were averaged within each mesocosm and sample day prior to statistical analyses. We calculated a separate repeated measures analysis of vari-ance (rmANOVA) for each response variable with sample day as the repeated measure to test for an eff ect of time, fi sh treatment, and time by fi sh treatment interaction on micro-bial decomposer respiration, invertebrate density on leaf lit-ter and in sediments, water column N and P, and terrestrial inputs. We used a separate one-way ANOVA and a Tukey multiple comparison procedure to test for diff erences among treatments within each time period for each response variable.

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We also used one-way ANOVAs to test for diff erences in average number of individuals recovered from each treat-ment as well as the total fi sh biomass from each treatment at the end of the experiment. We used analysis of covari-ance (ANCOVA) to compare mass-specifi c excretion rates among fi sh species. Percent similarity index (PSI) was used to calculate similarity in gut contents among species. Th e rmANOVAs, one-way ANOVAs, and ANCOVAs were calculated with SAS (2003), and the PSI was calculated with NtSYS pc 2.1 (Applied Biostatistics Inc. 2000).

Field study

On 10 June 2008, we placed 20 leaf packs containing 0.6 g (dry weight) of abscised sycamore leaf material in Har-mon Creek. Th e leaf packs were identical to those described in the previous experiments, and were distributed across a 1 km reach of stream. We placed the leaf packs in all major habitat types (e.g. pools, backwaters and sand runs) that are common within this stream reach. Temperature of Harmon Creek was monitored in one, shaded locality throughout this experiment using a temperature logger. On 15 July 2008, we removed all leaf packs from the stream and 14 additional samples of leaf material occurring naturally in this system (hereafter called natural leaf material). We made a concerted eff ort to select natural leaf material of similar size and that appeared to be in the same stage of decomposition as the leaf material in the leaf packs. Leaf packs and natural leaf material was returned to the laboratory where we measured microbial decomposer respiration and leaf-litter invertebrates on leaf material using the same methodologies described in the pre-vious experiments. We maintained temperature of the labo-ratory where we estimated microbial decomposer respiration at 25 ° C. We compared the microbial decomposer respira-tion and invertebrates from this leaf material to that from the microcosm and mesocosms experiments using a one-way ANOVA and Tukey multiple comparison procedure (SAS 2003).

Results

Microcosm experiment – direct effects on microbial decomposers

In general, the controlled microcosm experiment supported the predictions that nutrients can enhance microbial decom-poser respiration and chironomid density can reduce decom-poser respiration (Fig. 1). Th ere was a signifi cant insect barrier eff ect and a signifi cant nutrient eff ect on decomposer respiration (two-way ANOVA: screen eff ect F 1,23 � 54.47, p � 0.001; nutrient eff ect F 1,23 � 30.38, p � 0.001; interac-tion eff ect F 1,23 � 1.83, p � 0.191). Microbial decomposer respiration rates were about 1.9 times greater in micro-cosms with elevated nutrients than in microcosms with low nutrients, and about 2.4 times greater in microcosms with insect barriers than those without barriers (Fig. 1). More-over, there was a signifi cant interaction between insect barrier and nutrient enrichment on insect density from leaf litter (two-way ANOVA: screen eff ect F 1,23 � 46.80, p � 0.001; nutrient eff ect F 1,23 � 4.51, p � 0.046; interaction

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Figure 1. Mean ( � 1 SE; n � 6) microbial decomposer respiration (panel A) and aquatic insect density (panel B) measured from leaf litter in 18 l microcosms on day 35 in response to low (fi lled bar) and high (open bar) nutrient concentration and access by ovipositing insects.

eff ect F 1,23 � 5.76, p � 0.026). In most cases, leaf litter in microcosms with barriers had no invertebrate coloniza-tion, whereas, leaf litter in microcosms without barriers had insect densities that ranged from about 2 to 7 individuals g �1 (Fig. 1). However, the density of insects collected from leaf material in treatments without insect barriers was dependent on nutrient treatment, with insect density greatest in the high nutrient treatment (Fig.1).

Mesocosm experiment – indirect effects on microbial decomposers

Microbial decomposer respiration Fish eff ects on microbial decomposer respiration were time and species dependent, developing only on the fi nal sam-ple day (day 35) and in some fi sh treatments (Table 1). For example, in support of our predictions, mesocosms with blackstripe topminnow and blacktail shiner had microbial decomposer respiration rates that were about 2.7 times greater than control treatments (Fig. 2). However, contrary to our predictions, bullhead minnow had no eff ect on micro-bial decomposer respiration relative to controls (Fig. 2). Below, we present results that address potential mechanisms for the observed patterns in microbial decomposer respiration across treatments.

Water column nutrients One potential mechanism responsible for a signifi cant increase in microbial decomposer respiration was bottom – up, fi sh-mediated nutrient enrichment of watercolumn nutrients (i.e. N and P). Fish N and P excretion varied as a function of individual fi sh mass, but did not diff er among fi shes on a mass-specifi c basis (ANCOVA for nitrogen – mass: F 1,58 � 7.73, p � 0.008; species: F 2,58 � 2.01, p � 0.144; mass � species: F 2,58 � 0.66, p � 0.519; ANCOVA for phosphorus – mass: F 1,58 � 11.42, p � 0.001; species: F 2,58 � 1.21, p � 0.307; mass � species: F 2,58 � 0.08, p � 0.926;). For example, blackstripe topminnow excreted 0.977 � 0.409 μ mol-N g �1 h �1 and 0.093 � 0.053 μ mol-P g �1 h �1 (mean � 1 SD), blacktail shiner excreted 1.010 � 0.804 μ mol-N g� 1 h �1 and 0.111 � 0.058 μ mol-P g �1 h �1 , and bullhead minnow excreted 1.826 � 0.649 μ mol-N g �1 h �1 and 0.118 � 0.053 μ mol-P g �1 h �1 . In support of this general mechanism, N and P were signifi cantly greater in the meso-cosms with fi sh, but this eff ect also was dependent on time and species (Table 1). For example, blackstripe topminnow and blacktail shiner both caused about a two-fold increase in total N in the water column relative to mesocosms with no fi sh (Fig. 3). However, this increase occurred only on day 35 and did not diff er from bullhead minnow eff ects on water column N. Blackstripe topminnow doubled total P in the water column relative to control treatments, but this eff ect on total P also occurred only on day 35 and was not greater than eff ects of the other two fi sh species (Fig. 3).

Th e species with the greatest eff ect on water column nutri-ents were those that consumed mostly terrestrial foods. For example, gut contents of blackstripe topminnow matched its proposed trophic role, with terrestrial insects comprising about 80 � 39% (mean � 1 SD) of the diet. Other items, such as seeds, comprised nearly 20 � 40% of the diet in blackstripe topminnow. Th e trophic role of blacktail shiner was more similar to blackstripe topminnow than predicted, with 81% similarity in gut contents between these two spe-cies. Terrestrial insects and benthic aquatic invertebrates comprised 75 � 38% and 19 � 33% of the gut contents in blacktail shiner, respectively. Bullhead minnow matched its proposed trophic role, consuming primarily benthic inver-tebrates (88 � 26%). Th e diet of bullhead minnow was 9% similar to blackstripe topminnow and 25% similar to blacktail shiner.

Aquatic insects Th e insect assemblages that colonized the stream mesocosms were primarily chironomid ( Chironomus spp. 85%, Tanypo-dinae 10%) and odonate larvae (5%). We hypothesized that benthic feeding fi shes would enhance microbial decomposer respiration by reducing density of microbivore insects, such as chironomids, on leaf litter. Th us, we predicted that insect density in the benthos and on leaf litter would be reduced in blacktail shiner and bullhead minnow treatments. In gen-eral, fi shes with surface and benthic feeding strategies had diff erential eff ects on insect density in the mesocosm sedi-ments. Specifi cally, benthic insects increased by 76% in the blackstripe topminnow treatment where benthic foraging was minimal, and decreased by about 47% in the bullhead minnow treatment where benthic foraging was high (Fig. 2). However, the fi sh eff ects on benthic insects did not match

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Table 1. Six repeated-measure analysis of variance (using multivariate method and Wilks ’ Lambda) outputs showing degrees of freedom (DF), F - value, and associated level of signifi cance (p-value) for effects of time, fi sh treatment, and their interaction on microbial respiration rates on leaf litter, water column phosphorus and nitrogen, invertebrate density on leaf litter and in sediments, and terrestrial inputs in the 35 day mesocosm experiment. Signifi cant F-values and p-values (i.e. p � 0.05) are in bold.

DF F p DF Fe p

Decomposer respiration Water column phosphorusTime (T) 1,20 86.65 � 0.001 2,19 42.25 � 0.001 Fish (F) 3,20 6.43 0.003 3,20 3.57 0.032 T � F 3,20 42.45 � 0.001 6,38 2.79 0.024

Water column nitrogen Sediment insectsTime (T) 2,19 31.49 � 0.001 1,20 6.06 0.023 Fish (F) 3,20 3.86 0.025 3,20 25.80 � 0.001 T � F 6,38 2.96 0.018 3,20 20.17 � 0.001

Leaf litter insects Terrestrial inputsTime (T) 1,20 10.73 0.004 2,19 0.19 0.832Fish (F) 3,20 13.91 � 0.001 3,20 0.09 0.963T � F 3,20 0.27 0.848 6,38 0.27 0.946

eff ects on leaf litter insects as predicted. Rather, the signifi -cant fi sh eff ect on leaf litter insects (Table 1) resulted from a 9- and 3.5-fold increase (rather than decrease) in inver-tebrate density on leaf litter in treatments with bullhead minnow compared to control treatments on days 15 and 35, respectively (Fig. 2).

Uncontrolled effects Although eff orts were taken at the onset of the experiment to reduce size/biomass variation among the diff erent fi sh treat-ments and to replace individuals that were found dead in the mesocosms throughout the experiment, diff erences among treatments could have arisen and infl uenced some of the results presented above. To test whether our eff orts to maintain simi-lar fi sh density and biomass among treatments were eff ective, we analyzed the number of fi sh recovered from mesocosms at the end of the experiment and found no signifi cant diff erence among treatments (ANOVA: F 2,17 � 0.142, p � 0.869). In general, these fi sh recovery rates were high across all mesocosms (ca 94%), averaging 14.9 � 1.0 (mean � 1 SD) blackstripe topminnows, 15.0 � 1.1 bullhead minnows, and 15.2 � 1.2 blacktail shiners recovered from each treatment. Furthermore, we analyzed total fi sh biomass recovered from the mesocosms at the end of the experiment and also found no signifi cant diff er-ence among treatments (ANOVA: F 2,17 � 1.346, p � 0.290). Specifi cally, total fi sh biomass per mesocosm averaged 40.3 � 2.8, 42.5 � 2.9 and 40.3 � 2.2 g for blackstripe topminnow, bullhead minnow and blacktail shiner, respectively. Diff erential rates of insect inputs into the mesocosms could have aff ected water column nutrient loads (Hargrave et al. 2009), infl uenc-ing our results above. Th us, we examined variation in terrestrial input across treatments and found no signifi cant eff ect of time or treatment on terrestrial input in this experiment (Table 1), which averaged 144 � 27 mg m �2 d �1 (mean � 1 SD), 165 � 37 mg m �2 d �1 , and 160 � 14 mg m �2 d �1 on days 0, 15 and 30, respectively.

Field study

To evaluate the similarity of decomposer respiration from the controlled microcosm and mesocosm experiments to that from a natural stream, we measured microbial decomposer

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respiration rates of leaf litter from leaf packs that were placed in Harmon Creek after 35 days and from natural leaf litter col-lected from the creek. Microbial decomposer respiration rates of leaf litter from packs placed in Harmon Creek and from natu-ral leaf litter collected from the creek were diff erent, averaging 0.35 � 0.04 mg O 2 h �1 g �1 and 0.64 � 0.0 5 mg O 2 h �1 g �1 , respectively. Microbial decomposer respiration on leaf litter from packs that were placed in Harmon Creek were similar to respiration rates from the no fi sh (control) and bullhead min-now treatments in the large mesocosm experiment, and were similar to respiration rates of leaf litter from microcosms open to insect colonization (Table 2). Th e microbial decomposer res-piration of natural leaf litter collected from the creek was similar to that in the blackstripe topminnow and blacktail shiner treat-ments of the mesocosm experiment, and matched respiration in the high nutrient, low insect (with insect barrier) treatment in the microcosm experiment. Invertebrate densities on leaf lit-ter were similar among most treatments across all experiments except in the microcosm study where terrestrial insect access was restricted by barriers. In this treatment, invertebrates were about 13 times less dense than all other treatments.

Temperature of the microcosms with and without insect barriers averaged 26.3 � 3.8 ° C ( � 1 SD) and 26.4 � 4.0 ° C, respectively, temperature averaged 25.8 � 3.2 ° C in mesocosms, and averaged 26.8 � 1.0 ° C ( � 1 SD) in Harmon Creek. Th us, because temperatures were similar across experiments, this vari-able probably had little eff ect on the diff erences in microbial respiration rates reported above. We also argue that insect respi-ration on leaf litter probably had negligible eff ects on our over-all estimates of microbial decomposer respiration. For example, insect densities were greatest on leaf material with the lowest res-piration rates. Any additional respiration contributed by inver-tebrates would have made trends more conservative. Th erefore, our interpretations regarding direct negative eff ects of microbi-vores on microbial decomposer respiration rates are valid and likely conservative.

Discussion

In this study, we used two experiments to test the direct eff ects of nutrients and aquatic insects and the indirect eff ects

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Figure 2. Mean ( � 1 SE; n � 6) microbial decomposer respiration (panel A), and aquatic insect density in sediments (panel B) and on leaf litter (panel C) on days 0 (open bars), 15 (hatched bars) and 35 (fi lled bars) in mesocosms with no fi sh, a surface feeding fi sh (blackstripe topminnow), a water column feeding fi sh (blacktail shiner), and a benthic feeding fi sh (bullhead minnow). Bars within a time period that have the same letter were not statistically diff er-ent based on a Tukey multiple comparison procedure. A Tukey test was only performed if the one-way ANOVA within a time period was signifi cant (i.e. p � 0.05).

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Figure 3. Mean ( � 1 SE; n � 6) water column total nitrogen (A) and total phosphorus (B) on days 0 (open bars), 15 (hatched bars) and 35 (fi lled bars) in mesocosms with no fi sh, a surface feeding fi sh (blackstripe topminnow), a water column feeding fi sh (blacktail shiner), and a benthic feeding fi sh (bullhead minnow). Bars within a time period that have the same letter were not statistically diff er-ent based on a Tukey multiple comparison procedure. A Tukey test was only performed if the one-way ANOVA within a time period was signifi cant (i.e. p � 0.05).

of three fi sh species on respiration of leaf litter microbial decomposers. Our predictions that nutrients would directly enhance microbial decomposers and that leaf litter insects would directly reduce these decomposers were supported in the controlled microcosm experiment. However, our predic-tions were only partially supported for the larger mesocosm experiment. For example, our data supported the prediction that surface-feeding fi shes (e.g. blackstripe topminnow and blacktail shiner) enhance microbial decomposers from the

bottom – up by increasing local nutrient pools from terres-trial sources (terrestrial nutrient translocation; Schaus et al. 1997, Hargrave 2006), but this eff ect did not translate into increased microbivore density. Moreover, we found no sup-port for our prediction that a benthic omnivore (bullhead minnow) would increase microbial decomposers from the top – down by controlling invertebrate microbivores on leaf litter (trophic cascade; Power 1990). Below, we discuss the specifi cs of our fi ndings and demonstrate that trophic inter-actions of fi shes in stream food webs are likely to indirectly mediate microbial decomposers on detritus by altering the direct eff ects of nutrients and aquatic insects on these taxa.

In headwater stream ecosystems, increased water column nutrients can stimulate microbial decomposer respiration (Rosemond et al. 2002, Gulis and Suberkropp 2003, Cross et al. 2006). Our nutrient enrichment treatment in the controlled microcosm experiment supported this literature. Specifi cally, elevated nutrient treatment in this experiment increased decomposer respiration by several fold. Th ese data justify our hypothesis that higher-order consumers which enhance local nutrient pools also may positively aff ect

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Table 2. Mean ( � 1 SE) respiration rates of microbial decomposers and density of insects on leaf litter from treatments in the microcosm and mesocosm experiments, from leaf litter placed in leaf packs in Harmon Creek, and from natural leaf litter collected in Harmon Creek. Based on a Tukey multiple comparison procedure, means with the same letter were not statistically different.

Experimental treatment nMicrobial respiration

(mg O 2 h �1 g �1 ) TukeyLeaf litter invertebrates

(individuals g �1 ) Tukey

Microcosm experimentlow nutrients, with insects 6 0.16 � 0.02 a 2.17 � 1.48 alow nutrients, no insects 6 0.43 � 0.05 a,b 0.51 � 0.34 bhigh nutrients, with insects 6 0.34 � 0.04 a 7.67 � 1.42 c,dhigh nutrients, no insects 6 0.73 � 0.05 c 0.17 � 0.17 bMesocosm experimentno fi sh 6 0.20 � 0.03 a 2.67 � 0.78 ablackstripe topminnow 6 0.79 � 0.04 c 2.25 � 0.31 ablacktail shiner 6 0.89 � 0.11 c 3.08 � 0.81 abullhead minnow 6 0.41 � 0.05 a,b 9.42 � 1.19 dHarmon Creeklitter from leaf packs 20 0.35 � 0.04 a 5.95 � 1.39 a,clitter collected in the creek 14 0.64 � 0.05 a,b,c 3.28 � 1.64 a

decomposers and their contribution to detrital C fl ux in aquatic ecosystems. Because fi shes can enhance local nutri-ent pools in streams by consuming terrestrial foods and excretion of nutrients into the aquatic ecosystem (Schaus et al. 1997, Vanni 2002), we predicted that taxa fi tting this trophic-functional role in streams would stimulate micro-bial decomposer respiration. Our data supported this pre-diction. For example, blackstripe topminnow and blacktail shiner foraged primarily on terrestrial insects, excreted phos-phorus and nitrogen, and increased water column nutrients relative to mesocosms with no fi sh. Although elemental tracers were not used to identify nutrient source, we sug-gest, based on gut contents, that the nutrients excreted by these fi shes likely were derived from allochthonous sources (Vanni 2002). Th is enhanced the local nutrient pool and stimulated decomposer respiration on the leaf litter in a manner similar to the direct nutrient enrichment in the microcosm experiment.

Bottom – up enrichment of bacteria and fungi can move through the food web and aff ect consumers that eat these decomposer taxa (Wallace et al. 1999, Cross et al. 2003). Th us, we predicted that fi sh-mediated nutrient subsidies in aquatic ecosystems would enhance invertebrates that con-sume microbial taxa (Cross et al. 2006). In our experiment, chironomids comprised the majority of aquatic insect taxa, because our streams were designed to mimic the early stages of succession that are characteristic of many sand-bottom Gulf coastal streams. Moreover, because chironomids read-ily colonize leaf material and consume microbial decompos-ers, we expected these taxa to respond positively to nutrient enrichment (Rosemond et al. 2001). Our microcosm experi-ment supported this bottom – up eff ect on chironomids because chironomid density on leaf litter was greatest in the high nutrient treatment. However, in the larger, mesocosm experiment chironomid densities were no greater on leaf litter in treatments with elevated decomposer productivity (i.e. blackstripe topminnow and blacktail shiner treatments) than control treatments. Th is suggests that in more realistic experimental units (mesocosms with fi sh) bottom – up eff ects on leaf litter insects may be infl uenced by more complex processes.

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Th ree possibilities may explain the lack of a bottom – up eff ect on leaf litter chironomids in the blackstripe topminnow and blacktail shiner treatments. First, a diff erence in the tem-poral dynamics of N and P enrichment between the micro-cosm and mesocosm experiments could have contributed to this lack of congruence between experiments. For example, in the microcosm experiment, we experimentally enriched N and P by four-fold at the onset of the experiment. In the mesocosm study, blackstripe topminnow and blacktail shiner also enhanced N and P by about three- to four-fold. However, this fi sh-mediated nutrient enrichment took time to develop, becoming signifi cant only by the end of the study (day 35). Th e temporal delay in N and P enrichment in the mesocosms may not have provided suffi cient time for bottom – up eff ects to move through the food web and stimulate the microbivore trophic guild. Second, chironomids could have preferentially colonized sediments over leaf material in the absence of benthic foraging by fi shes. In support of this possibility, chironomid densities were greater in mesocosm sediments with blackstripe topminnow than in control streams. Blackstripe topminnow had little direct interactions with benthos, foraging primarily on insects from the stream surface. Th us, habitat selection by chironomids could have restricted the bottom – up eff ects of blackstripe topminnow to sediments and not leaf litter. Th ird, moderate benthic predation on chironomids could have pre-vented a positive bottom – up response in chironomid density on leaf litter and in the sediments. Blacktail shiner foraged to some degree on chironomids, but their predatory eff ects were not as intense as eff ects of bullhead minnow. For example, there was no visual evidence (i.e. pockmarks, disturbed sand) of benthic foraging activity by this species and benthic inver-tebrate densities did not decrease in blacktail shiner treatment. It is possible that any bottom – up eff ects on sediment dwelling and leaf litter chironomid densities could have been negated by moderate predation of this water column fi sh. Although direct bottom – up eff ects on chironomids occurred in the more controlled microcosm experiment, it appears that more complex nutrient dynamics, chironomid behavioral plasticity, and moderate predation could have explained why we found no bottom – up eff ect on chironomid densities on leaf litter in the larger mesocosm experiment.

Aquatic insects directly consume leaf material, reducing particle size and enhancing the rate of detrial C fl ux back into the atmosphere. In addition to this process, microbial taxa that colonize leaf material and fi ne particulates also have a vital role in C mineralization to the atmosphere (Gulis and Suberkroppp 2003). Th us, in the absence of larger inver-tebrate detritivores that shred leaf material, small aquatic invertebrates that consume microbial taxa may actually slow rates of leaf decomposition in stream ecosystems (Oberndor-fer et al. 1984). Our microcosm experiment supported this hypothesis. For example, the microcosm treatments with ele-vated chironomid densities (i.e. control insect barriers) had lower decomposer respiration rates than mesocosms with intact insect barriers. Th us, the increase in decomposer res-piration that we documented in the blackstripe topminnow and blacktail shiner treatments in the mesocosm study likely was maximized because chironomid density did not increase on leaf litter in these treatments. Because chironomids are abundant microbivores in many leaf litter communities, their abundance is likely to reduce microbial respiration and associated decomposition-related ecosystem services (Pace and Funke 1991, Meyer 1994, Mikola and Set ä l ä 1998). Th erefore, one would predict that predatory control of chi-ronomid densities would enhance decomposer-mediated C fl ux into the atmosphere.

Benthic fi shes consume sediment dwelling invertebrates and can indirectly regulate basal trophic levels through trophic cascades (Power 1990). Th us, we predicted that the benthic feeding bullhead minnow would reduce chirono-mid densities and stimulate microbial decomposers from the top – down. Benthic invertebrates (namely chironomids) comprised a large proportion of the bullhead minnow diet, supporting our proposed trophic-functional guild for this fi sh. Moreover, we observed pockmarks on the sediments of the stream mesocosms with this species, providing further evidence that this species was a benthic forager. However, the negative eff ect of bullhead minnow on invertebrates in mesocosm sediments was not observed on leaf litter. Rather, chironomids on the leaf litter were enhanced in the bullhead minnow treatment. We hypothesize that the increase in chi-ronomids on leaf litter resulted because of a behviorial shift in substrate choice by these taxa. Leaf packs were designed to exclude fi sh while allowing for invertebrates to freely colonize the leaf material. It is possible that chironomids selected leaf packs because they provided a refuge from bullhead minnow predation (Holomuzki and Hoyle 1990). Predator-mediated behavioral shifts in prey have been demonstrated in a vari-ety of ecosystems, including streams (Short and Holomuzki 1992, Werner and Peacor 2003). Th ese behavioral shifts in prey can result in trophic cascades and other indirect food web interactions, which sometimes produce data that are opposite of predictions based on traditional density-mediated mechanisms (Schmitz 1998, Schmitz et al. 2004). Th erefore, it is likely the eff ects of bullhead minnow did not match our predictions because of an interaction between benthic forag-ing behavior of this species and the shelter provided by leaf packs. Although these results likely were infl uenced by a leaf-pack eff ect, these data may translate into real ecosystems if natural leaf accumulations provide a refuge for invertebrates from benthic foragers (Rueda-Delgado et al. 2006).

Above, we discussed several mechanisms for the direct and indirect regulation of decomposer productivity in stream food webs. However, broad generalizations based on our experimental results likely are constrained by limitations associated with scaled-down nature of the microcosm and mesocosm units. First, the experimental units were closed systems with no fl ow (microcosm) or with recirculating fl ow (mesocosms). Th is likely enhanced nutrient-mediated eff ects in both experiments. Th us, extrapolations of these results likely apply under specifi c environmental contexts that favor positive eff ects of nutrient subsidies. Th ese include streams with high fi sh density and low background nutrients (olig-otrophic). Second, the leaf packs prevented direct interac-tions between fi shes and the decomposing leaf material. As discussed previously, this likely provided a refuge for ben-thic insects from fi sh predation. Th us, the direct eff ects of leaf litter invertebrates were likely exacerbated by this arti-fact. Th erefore, in natural streams, these eff ects are likely only to occur in shallow backwaters where access by fi shes is restricted. Finally, the invertebrate assemblages coloniz-ing leaf litter were simplistic compared to natural leaf lit-ter assemblages. Th e most notable absence was the shredder guild. Th erefore, the direct eff ects of leaf processing by larger invertebrates were lacking from our results. To address this concern, we focused on microbial decomposer respiration as the response rather than leaf decomposition. Microbial respiration is an important determinant of detritus qual-ity, which infl uences production rates in many consumers linked to detrital C (Suberkropp and Chauvet 1995). More-over, microbes can drive up to 50% of detrital decomposi-tion rates in streams (Weyers and Suberkropp 1996, Baldy et al. 2002, Gulis and Suberkropp 2003). Th us, estimates of decomposer productivity and biomass are indicative of the decomposition-related processes and ecosystem services in aquatic ecosystems.

Despite these limitations, the respiration rates mea-sured in some of our microcosms and mesocosm treatments matched respiration rates measured directly from natural leaf litter in Harmon Creek. In general, decomposer respiration rates were greatest for natural leaf material and in microcosms with elevated nutrients and low insects and for mesocosm treatments with surface-feeding fi shes. Th e combination of low microbivore density and enhanced nutrients in the water column of these ecosystems likely contributed to similar decomposer respiration across these experiments. Th us, the direct and indirect food web eff ects on microbial decompos-ers are likely to apply to natural ecosystems with background nutrient levels similar to those used in our experiments and with reduced leaf litter insect abundance.

Th e varying eff ects of top consumers on basal resources from diff ering trophic-functional guilds have been well established in the ‘ green food web ’ . However, relatively fewer studies have tested similar predictions in detritus-based ecosystems. Herein, we have demonstrated how nutrients and aquatic insects can directly regulate decomposers, and we have shown that top-consumers (i.e. fi shes) can indirectly regulate decomposers by directly altering nutrients and insect densities. Our data suggest that, much like autotrophic systems, community structure of top consumers in small headwater streams is likely to infl uence rates of C fl ux

1793

through detritus-based ecosystems. Th erefore, because of the great importance of detrital energy for many ecosystems, changes to community structure that aff ect decomposer productivity could have profound eff ects on energy and nutrient dynamics in many types of ecosystems (Polis and Strong 1996). Our results in combination with a variety of fi eld experiments from other researchers (Rosemond et al. 2001, Ruetz et al. 2002, Greenwood et al. 2007) provide a sound foundation that consumer-mediated food web inter-actions can regulate important ecosystem functions within the ‘ brown food web ’ .

Acknowledgements – We greatly appreciate the assistance of L. Shoe-maker and H. Turner in the fi eld and laboratory. We thank members of the R. Deaton and T. Primm labs for thoughtful and critical dis-cussion about this study. Partial funding for this project was pro-vided by the College of Arts and Sciences and Offi ce of Research and Sponsored Programs at Sam Houston State Univ. to CH. Collecting permits were issued by Texas Parks and Wildlife Dept, and use of fi shes was approved by SHSU IACUC (no. 07-01-15-1011-3-01).

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