Effects of consumer identity and disturbance on stream mesocosm ...

Fundam. Appl. Limnol. Stuttgart, June 2010

Vol. 177/2, 143–149

Article

Effects of consumer identity and disturbance on stream mesocosm structure and function John P. Ludlam 1 and Daniel D. Magoulick* USGS, Arkansas Cooperative Fish and Wildlife Research Unit, Department of Biological Sciences, University of Arkansas, Fayetteville, AR, U.S.A. With 2 figures and 2 tables Abstract: Consumers can alter the structure and function of aquatic ecosystems, but the interactions that regulate

ecosystem functioning are context dependent. In many streams, environmental disturbance and consumer identity may interact to influence benthic ecosystem structure and function. We predicted that effects of two common consumers (central stonerollers (Campostoma anomalum), and Meek’s crayfish (Orconectes meeki meeki)) in Ozark Mountain streams (Arkansas, USA) would be altered by disturbance. In stream mesocosms we crossed disturbance (simulated spate) and consumer identity (crayfish, central stonerollers, or no consumers). Stream ecosystem function was quantified as leafpack decomposition and net primary productivity (NPP). Ecosystem structure was measured as algal chlorophyll-a, ash-free dry mass (AFDM), and chironomid density. Disturbance and interactions between disturbance and consumer identity did not significantly affect any response variable. Chlorophyll-a, AFDM, and chironomid density were influenced by consumer identity, and effects differed between stonerollers and crayfish and with time. Crayfish and stonerollers reduced day 15 chironomid density compared with no consumer treatments. Stonerollers reduced day 30 chironomid density and day 15 periphyton abundance compared with crayfish and no consumer treatments. Crayfish increased leafpack breakdown rates above stoneroller and no consumer treatments, but NPP did not differ among consumer treatments. In this experiment, consumers had stronger effects on benthic structure and function than the disturbance treatment. Future studies should investigate a wider range of disturbance frequency and intensity. Key words: aquatic ecosystem, environmental disturbance, crayfish, central stonerollers.

Introduction Consumers can alter the structure and function of aquatic ecosystems (e.g. Power 1990, Gelwick & Matthews 1992), but the ecological interactions that regulate ecosystem functioning are context dependent (Power et al. 1988b, Cardinale et al. 2000). In many streams, benthic-feeding fish and crayfish play an important role in mediating stream processes by graz-

ing periphyton, processing leaf litter, and disturbing sediments (Power et al. 1988a, Creed 1994, Ludlam & Magoulick 2009). Through these effects, they alter ecosystem processes like primary production, decomposition, energy transport, and nutrient cycling (e.g. Gelwick & Matthews 1992, Schofield 2001). However, the importance of consumers can depend on biotic and abiotic factors like the presence of avian and fish predators (Power & Matthews 1983, Power et al.

Authors’ address: 1

USGS, Arkansas Cooperative Fish and Wildlife Research Unit, Department of Biological Sciences, University of Arkansas, Fayetteville, AR, U.S.A. 72701 * Corresponding author; e-mail: [email protected] © 2010 E. Schweizerbart’sche Verlagsbuchhandlung, Stuttgart, Germany DOI: 10.1127/1863-9135/2010/0177-0143

www.schweizerbart.de 1863-9135/10/0177-0143 $ 1.75

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John P. Ludlam and Daniel D. Magoulick

1989), consumer identity (Gelwick 2000, Vaughn et al. 2007, Bengtson et al. 2008), flow (Hart 1992, Wootton et al. 1996), and season (Fortino 2006). Scouring spates may be a particularly important influence on ecological interactions in streams (Feminella & Hawkins 1995, Power et al. 2008). Spates scour the bottom of accumulated matter, shift substrates, and displace or kill organisms (Dodds et al. 1996). Severe seasonal scouring can promote summer algal blooms by reducing the abundance of important grazer taxa (Wootton et al. 1996, Power et al. 2008). High flows scour periphyton communities and alter algal succession (Power & Stewart 1987, Lohman et al. 1992, Allan 1995, Dodds et al. 1996), and disturbance often disproportionately affects filamentous algae while favoring closely attached grazer-resistant taxa. Consumer effects will likely differ following disturbance if high flows alter the abundance or composition of benthic communities. For example, Wellnitz & Rader (2003) found that effects of the mayfly Rhithrogena robusta and light on periphyton differed on tiles subjected to extended high flows compared with protected tiles. In this case, scouring apparently shifted the periphyton community towards scour and grazingresistant taxa. In many streams in the central United States crayfish (e.g. Orconectes spp.) and central stoneroller minnows are abundant and important benthic consumers. Previous research has demonstrated differences in the functional ecology of stonerollers and crayfish. Gut contents and stable isotope analysis of stonerollers and two related crayfish taxa (Orconectes nais and Orconectes neglectus) in a prairie stream indicated that both stonerollers and crayfish consumed algae, amorphous detritus, animal matter, and leaves (EvansWhite et al. 2001, Evans-White et al. 2003). However, crayfish and stonerollers depended on different components of the benthic environment; algae and amorphous detritus dominated stoneroller production, but leaves and animal matter contributed most to crayfish production (Evans-White et al. 2003). Morphology accounts for some of these differences. Crayfish use their chelae to rapidly process leaf litter and filamentous algae, and the inferior mouth and cartilaginous lower lip of stonerollers are well suited for grazing diatoms and other attached algae (Robison & Buchanan 1988, Evans-White et al. 2003). Since stonerollers and crayfish have unique effects on benthic resources, the effects of stonerollers and crayfish on benthic communities may respond differently to disturbance. However, little is known about interactions between consumer identity and distur-

bance. Hence, we investigated how benthic consumer identity (stoneroller minnows or Meek’s crayfish) and disturbance (simulated scouring prior to adding consumers) affected ecosystem structure and function in experimental stream mesocosms. A single disturbance was used to simulate a large spate prior to summer drying. We predicted that consumer effects on primary production and leafpack decomposition rates and algal and invertebrate abundance would be stronger in the absence of disturbance. We expected stonerollers would have strong negative effects on periphyton and primary production, while O. meeki would increase the rate of detrital decomposition and decrease invertebrate abundance. Disturbance effects should be greatest on periphyton and invertebrate abundance, thus altering stoneroller effects on periphyton and crayfish effects on invertebrates. Global climate change is altering the frequency and intensity of precipitation events and affecting the hydrological regime of streams and rivers (Allan & Soden 2008). Though flow-related disturbance in streams is increasing, we have a limited understanding of how these changes will affect stream ecosystems (Lake et al. 2000). Streams perform critical roles in nutrient cycling, biodiversity, and organic matter transport (Peterson et al. 2001), so it is important to understand the interactive effects of disturbance and consumers on stream functioning.

Methods Experiments were conducted in thirty re-circulating 100-liter (0.67 m2) tanks housed in a temperature-controlled greenhouse bay. Tanks were filled with dechlorinated city water and filtered with an external canister filter (Fluval 2051, Rolf C. Hagen Inc., Montreal, Canada). Gravel substrate was added to tanks along with two 11 × 11 cm unglazed ceramic tiles and two 3-g leafpacks. Leafpacks were assembled from fresh Acer saccharum leaves that were dried to constant mass at room temperature and clipped together with plastic fasteners. Tanks were inoculated with algae from a local river 30 days prior to the experiment. The disturbance treatment was designed to simulate benthic scouring from an early summer spate, including substrate movement and removal of accumulated periphyton. Tank substrate was thoroughly raked and overturned with a garden rake and tiles were scrubbed with a bristle brush immediately prior to stocking consumers. Disturbance (disturbed or undisturbed) and consumer treatments (crayfish, stonerollers, or no consumers) were systematically assigned with a randomized starting point in a fully factorial design. Then, consumer treatments 1

The use of trade, product, industry or firm names or products is for informative purposes only and does not constitute an endorsement by the U.S. Government or the U.S. Geological Survey.

Stream mesocosm structure and function

were stocked with either 8 male crayfish (17–26 mm carapace length, 12.9 g ± 0.2 (mean ± SE) wet weight biomass per tank) or 8 stonerollers (50–66 mm total length, 10.8 g ± 0.2 wet weight biomass per tank). These densities span the range of average stoneroller and crayfish densities for Ozark streams (Magoulick 2000, Flinders & Magoulick 2003, Rabalais & Magoulick 2006, Magoulick & DiStefano 2007, D. D. Magoulick, unpublished data). Observed mortalities were replaced with individuals of similar size. The experiment ran from 26 August to 26 September, 2008. Tanks were covered with 6 mm plastic mesh to contain occupants. Because tanks did not receive substantial resource inputs (e.g. nutrients, terrestrial insects), all tanks were supplemented with commercially available fish food on approximately 2–3 day intervals. Temperature/light loggers (Hobo Pendant UA-002-64, Onset Computer Corporation, Pocasset, Massachusetts, USA) were placed in 7 tanks. Water turbidity was measured with a portable nephelometric turbidity meter (T-100, Oakton Instruments, Vernon Hills, Illinois, USA). Dissolved oxygen and conductivity were measured with a YSI 85 meter, and a YSI 60 meter recorded pH (YSI, Yellow Springs, Ohio, USA). Net primary productivity was estimated for tanks on day 30 by measuring tank dissolved oxygen with an YSI 550 meter every 2 hours from dawn until peak afternoon levels (Bengtson et al. 2008). Mean production was calculated by averaging oxygen production for each interval (n = 5–6). Re-aeration was assumed to be similar among tanks since tanks were comparable in size and current velocity. Tiles were collected on day 15 and 30 and frozen before analysis. Each tile was scraped with a razor blade and brushed with a nylon toothbrush, and periphyton was rinsed into a beaker. Each periphyton sample was diluted to 500 mL with water and mixed on a magnetic stir-plate. Two 10 to 20-mL subsamples were removed and filtered onto pre-weighed Whatman GF/F filters. One filter was dried for 24 h at 100 °C, weighed, then combusted at 550 °C for 1 h, rewetted, and dried to obtain sediment organic matter content as ash-free dry mass (AFDM). The 2nd filter was placed in 10 mL of 96 % ethanol for spectrophotometric analysis of chlorophyll-a concentration (Stich & Brinker 2005, Wasmund et al. 2006). Invertebrates (mainly chironomid larvae) in the remaining sample were filtered onto a 300 μm screen, preserved in 70 % ethanol, and measured using an ocular micrometer and a dissecting scope. Leafpacks were collected on day 30 and frozen. Leafpacks were rinsed onto a 3 mm screen, dried at 50 °C, weighed, ground with a coffee grinder, and a 250 mg subsample was ashed and reweighed. Initial leafpack mass was determined from 7 day 0 leafpacks. At the end of the experiment, crayfish and stonerollers were removed from tanks, weighed (wet mass), and measured. Mass for one stoneroller was not recorded and was estimated using a length-weight regression using length and wet mass data from the other stonerollers (R2 = 0.84). Tank pH, turbidity, temperature, and conductivity were similar among treatments. Mean tank water temperature was 24.6 °C (17.8–32.0 (range)), tank pH was 8.76 (8.22–9.80). Mean specific conductivity was 392.21 (mS cm–1, 235.40– 483.80), and turbidity was 0.56 (NTU, 0.06–1.72).

Data analysis Statistical analyses were done with SYSTAT (Version 11; Systat Software, Inc., San Jose, California). Two-way repeated measures analysis of variance (ANOVA) was done to test for differ-

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ences in chlorophyll-a, AFDM, and chironomid density among sampling periods (repeated) and consumer identity and disturbance treatments. Chlorophyll-a and AFDM were log(x+0.1)transformed and chironomid density was log(x+1)-transformed to reduce heteroschedasticity. Sampling period and consumer identity had significant interactive effects on chlorophyll-a, AFDM, and chironomid density, which precluded the interpretation of lower-level interactions (Underwood 1997). Therefore, separate 2-way ANOVAs with consumer identity and disturbance as the main effects were done for each sampling period. If consumer identity had a significant effect, multiple comparisons were conducted using t-tests to compare chlorophyll-a, AFDM, and chironomid density for consumer treatments (crayfish vs. stonerollers, crayfish vs. no consumers, and stonerollers vs. no consumers) separately for day 15 and 30 pooling over disturbance treatments. A false discovery rate (FDR) control was applied to control Type 1 error (α = 0.05) (Verhoeven et al. 2005). One chlorophyll sample and five AFDM samples were lost and not included in the analysis. Two-way analysis of variance with consumer identity and disturbance as main effects was used to test for differences in % leafpack AFDM remaining and wholetank net primary production (NPP).

Results Ecosystem structure

Day 30 crayfish abundance was lower (final including replacements/initial abundance = 51 %) than stoneroller abundance (93 %) but final biomass was similar (11.3 g ± 0.3 vs. 12.5 g ± 1.9, respectively). Sampling period (day) and consumer identity (consumers) had a significant interactive effect on chlorophyll-a, AFDM, and chironomid density (day × consumer, Table 1). Consumers had a significant effect on chlorophyll-a and AFDM on day 15 but not day 30 (Fig. 1A-B), and chironomid density differed among consumer treatments on day 15 and day 30 (Fig. 1C, Table 2). Stonerollers reduced day 15 chlorophyll-a compared with crayfish and no consumer treatments (p-values significant following FDR correction, p ≤ 0.008). Crayfish and stonerollers reduced day 15 chironomid density compared with the no consumer treatment (p ≤ 0.002), and stonerollers reduced day 30 chironomid density compared with crayfish and no consumer treatments (p ≤ 0.032). Disturbance did not significantly affect response variables (disturbance, Table 1, Fig. 1A-C). There were no significant consumer × disturbance, day × disturbance, or day × consumer × disturbance interactions (Table 1). Ecosystem function

Percent leafpack remaining was lower in crayfish than stoneroller and no grazer treatments (F2,24 = 27.657, p < 0.001) but did not differ among disturbance treat-

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Table 1. Repeated measures analysis of variance table for mesocosm experiment with consumer identity (consumer) and distur-

bance as main effects, sampling period (day) as the repeated variable, and chlorophyll-a, ash-free dry mass (AFDM), and chironomid abundance as the response variables. AFDM

Chlorophyll-a Source

df

Between Consumer 2 Disturbance 1 2 Consumer × disturbance Error 23 Within Day 1 2 Day × consumer 1 Day × disturbance Day × consumer × disturbance 2 Error 23

F

p

df

F

3.55 0.72 0.07

0.045 0.404 0.937

2 1 2 19

3.68 0.28 0.01

8.22 3.55 3.66 2.32

0.009 0.045 0.068 0.121

1 2 1 2 19

83.51 3.58 0.04 1.33

Chironomids p

df

F

p

0.045 0.602 0.985

2 1 2 24

17.87 0.91 1.02

< 0.001 0.350 0.375

< 0.001 0.048 0.852 0.289

1 2 1 2 24

9.78 3.48 0.46 0.56

0.005 0.047 0.506 0.576

Table 2. Analysis of variance tables for day 15 and day 30 with consumer identity (consumer) and disturbance as main effects and chlorophyll-a, ash-free dry mass (AFDM), and chironomid abundance as the response variables.

AFDM

Chlorophyll-a Source Day 15 Consumer Disturbance Consumer × disturbance Error Day 30 Consumer Disturbance Consumer × disturbance Error

Chironomids

df

F

p

df

F

p

df

F

p

2 1 2 23

6.18 0.00 0.46

0.007 0.966 0.640

2 1 2 21

3.92 0.06 1.26

0.036 0.802 0.304

2 1 2 24

15.47 0.20 0.57

< 0.001 0.658 0.572

2 1 2 24

2.10 2.02 0.61

0.145 0.168 0.550

2 1 2 22

2.09 0.39 0.30

0.147 0.537 0.743

2 1 2 24

12.45 1.58 1.35

< 0.001 0.221 0.279

ments (F1,24 = 0.338, p = 0.566, Fig. 2A). There was no evidence that consumers and disturbance had an interactive effect on % leafpack remaining (F2,24 = 0.100, p = 0.905). Net primary production did not differ significantly among consumer or disturbance treatments (F2,24 = 0.580, p = 0.569 and F1,24 = 1.79, p = 0.194 respectively), and there was no evidence for an interaction (F2,24 = 0.730, p = 0.490, Fig. 2B).

Discussion Disturbance is often an important factor structuring stream communities (Resh et al. 1988), and highflows can alter ecological interactions (e.g. Power et al. 2008). However, contrary to the initial hypothesis, a disturbance simulating a spate prior to summer drying did not significantly alter benthic function or consumer effects 15 or 30 days post-disturbance. Dis-

turbance frequency and intensity, in addition to mere disturbance presence, can be important regulators of disturbance effects (Connell 1978). The benthic community in this study (periphyton and chironomids) apparently recovered quickly in response to the initial disturbance. More frequent disturbance or the inclusion of longer-lived herbivore taxa (e.g. Ephemeroptera or Gastropoda) in our mesocosms may have resulted in more pronounced effects on interactions between consumers and stream structure and function. As predicted, O. meeki and stonerollers had both distinctive and overlapping effects on mesocosm structure and function. O. meeki increased detrital decomposition, stonerollers reduced periphyton, and both O. meeki (day 15) and stonerollers (day 15 and 30) reduced chironomid density. Counter to expectations, stonerollers had stronger and more consistent effects on chironomid density than crayfish. Chironomids in this study were small (~2 mm) and stonerollers likely

15

Crayfish Day 15

Stonerollers

None Day 30

0

5

10

A

147

0.5

1.0

1.5

B

1.000

C

0.050

ods) chlorophyll-a (A), ash-free dry mass (AFDM, (B)), and chironomid density (C) on tiles on day 15 and 30. Chironomid abundance is shown on a log scale.

0.001

Fig. 1. Mean (±1 SE; n ≤ 5, see Meth-

Chironomids (no. cm−2)

0.0

AFDM (mg cm−2)

2.0

Chlorophyll a (μg cm−2)


Disturbed

dislodged or consumed them while foraging. Contrary to the initial hypotheses, stonerollers did not influence whole-tank primary production despite effects on tile periphyton abundance. Other studies that have demonstrated effects of stonerollers on primary production (Stewart 1987, Gelwick & Matthews 1992) placed substrates in enclosed chambers to measure production. Whole-tank measurements integrate metabolism over a greater range of habitats (water-column, periphyton, and interstitial) than chamber measurements, and may better represent the effects of consumers on benthic systems. However, because whole-tank methods include habitats not directly used by fish and crayfish, these methods may be less likely to detect consumer effects on benthic primary production than chamber experiments with single tiles (e.g. Bertrand & Gido 2007, Bengtson et al. 2008). Other studies have demonstrated that the effects of crayfish and grazing fish can be similar or quite different depending on environmental context. Stonerollers and crayfish (O. neglectus) in artificial stream channels had similar effects on periphyton, as both consumers significantly reduced algal biomass on clay tiles relative to ungrazed tiles (Evans-White et al. 2001). However, in experimental mesocosms with and without

Undisturbed

Disturbed

Undisturbed

predatory bass (Micropterus salmoides), the effects of stonerollers and crayfish (Orconectes virilis) on filamentous algal abundance and distribution varied in response to differences in stoneroller and crayfish behavior and predation risk (Gelwick 2000). Abiotic factors can also influence the roles of consumers; Bengtson et al. (2008) found that O. neglectus and O. nais did not affect ecosystem properties in experimental streams in the fall (mean water temperature 12.9 °C), but southern redbelly dace (Phoxinus erythrogaster) reduced algal filament length and chironomid abundance. However, in the spring (mean water temperature 21.4 °C) crayfish reduced algal filament length and invertebrate abundance compared with dace. Together, these studies suggest that stonerollers and Orconectes spp. may have similar or different effects on stream communities depending on species-specific responses to biotic and abiotic factors. In our experiment, consumers affected chironomid abundance more consistently (day 15 and 30) than algal abundance (day 15 only). However, reductions in chironomid herbivores did not result in increased algal abundance. This is in agreement with other research done in these mesocosms (J. L., unpublished data) where O. meeki had strong effects on intermedi-


Crayfish Stonerollers None

A

60 40 0

20

% AFDM

80

100

148

80 100

Acknowledgements

40

60

This research was supported by a Sigma Xi Grant-in-Aid of Research to J. Ludlam and by the Arkansas Game and Fish Commission. Field and laboratory assistance was provided by Brandon Banks and Molly Ludlam. Suggestions from Gary Huxel, Art Brown, Susan Ziegler, Eric Larson, and Matt Dekar substantially enhanced the quality of this research.

20

NPP (mg m−2h−1)

B

the effects of both the experimental disturbance (since other disturbances were absent), and consumers (since resources may have been more limiting in the mesocosms). Understanding how disturbance influences the effects of fish and crayfish on stream functioning is important given the critical roles of streams in nutrient cycling, biodiversity, and organic matter transport (Peterson et al. 2001). In this experiment a simulated flood disturbance did not have strong effects on stream mesocosm properties or consumer effects as benthic communities recovered quickly, but consumer identity influenced ecosystem responses to benthic consumers. These results demonstrate that consumers can have stronger effects on benthic structure and function than disturbance under some disturbance regimes, and that more research is needed to investigate a wider range of disturbance frequency and intensity.

0

References

Disturbed

Undisturbed

Fig. 2. Mean (±1 SE; n = 5) % ash-free dry mass (AFDM) leaf-

pack remaining (A) and whole-tank net primary production (mg O2 m-2 h-1) on day 30 (B)

ate trophic levels but also consumed basal resources. Similar results have been reported in other systems where omnivory apparently prevents potential trophic cascades from developing (e.g. Nystrom et al. 1996, Dorn & Wojdak 2004). Consumer effects on periphyton may have also become more difficult to detect as algal abundance became increasingly variable among tanks by day 30. The experimental mesocosms differed in 2 important ways from natural stream pools. First, except for the experimental disturbance, environmental conditions (temperature, flow) were relatively uniform. Second, natural streams receive considerable inputs (e.g. water, terrestrial insects, detritus) from upstream and terrestrial habitats (Polis & Strong 1996, Nakano et al. 1999), but mesocosms were disconnected from these subsidies. These differences should have intensified

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Submitted: 16 July 2009; accepted: 28 May 2010.

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