macroinvertebrate community response to ...

WETLANDS, Vol. 28, No. 3, September 2008, pp. 686–694 ’ 2008, The Society of Wetland Scientists

MACROINVERTEBRATE COMMUNITY RESPONSE TO EUTROPHICATION IN AN OLIGOTROPHIC WETLAND: AN IN SITU MESOCOSM EXPERIMENT Shawn E. Liston1,3, Susan Newman2, and Joel C. Trexler1 Department of Biological Sciences, Florida International University Miami, Florida, USA 33199

1

2

Everglades Division, South Florida Water Management District 3301 Gun Club Road West Palm Beach, Florida, USA 33046 3

Present address: Audubon of Florida, Corkscrew Swamp Sanctuary 375 Sanctuary Road West Naples, Florida, USA 34120 E-mail: [email protected] Abstract: Eutrophication from anthropogenic nutrient enrichment is a primary threat to the oligotrophic freshwater marshes of southern Florida. Macrophyte and periphyton response to increased phosphorus (P) has been well documented in both correlative and experimental studies, but the response of consumer communities remains poorly understood, especially in southern marl prairies. We conducted a P-loading experiment in in situ mesocosms in Taylor Slough, Everglades National Park, and examined the response of macroinvertebrate communities. Mesocosms at two sites were loaded weekly with P at four levels: control (0 g P/m2/yr), low (0.2 g P/m2/yr), intermediate (0.8 g P/m2/yr), and high (3.2 g P/m2/ yr). After ,2 yrs of P-loading, macroinvertebrates were sampled using periphyton mat and benthic floc cores. Densities of macroinvertebrate taxa (no./g AFDM) were two to 16 times higher in periphyton mats than benthic floc. Periphyton biomass decreased with enrichment at one site, and periphyton was absent from many intermediate and all high P treatments at both sites. Total macroinvertebrate density in periphyton mats increased with intermediate P loads, driven primarily by chironomids and nematodes. Conversely, total macroinvertebrate density in benthic floc decreased with enrichment, driven primarily by loss of chironomids and ceratopogonids (Dasyhelea). This study suggests that macroinvertebrate density increases with enrichment until periphyton mats are lost, after which it decreases, and mat infauna fail to move into benthic substrates in response to mat loss. These results were noted at nutrient levels too low to yield anoxia, and we believe that the decrease of macroinvertebrate density resulted from a loss of habitat. This work illustrates the importance of periphyton mats as habitat for macroinvertebrates in the Everglades. This study also indicates that in this system, macroinvertebrate sampling should be designed to target periphyton mats or conducted with special attention to inclusion of substrates relative to their coverage. Key Words: benthic, Chironomidae, Everglades, Hyalella, periphyton, phosphorus

INTRODUCTION

ous studies have described macroinvertebrate response to enrichment in stream and lake ecosystems (e.g., Chambers et al. 2006, Langdon et al. 2006, Brauns et al. 2007), wetland macroinvertebrate community dynamics have been less thoroughly described. Furthermore, results from previous studies describing wetland invertebrate response to nutrient enrichment have been inconsistent, noting both increases (Gabor et al. 1994, King 2001) and species-specific responses (Hann and Goldsborough 1997, Jahnke et al. 2001, Duinen et al. 2006) to enrichment.

Macroinvertebrate communities provide considerable information about ecosystem impairment and are often used as early indicators of environmental quality (e.g., Feio et al. 2007). Macroinvertebrate communities can respond to a combination of nutrient-related factors, including oxygen availability (Saloom and Duncan 2005), food quality and quantity (Cross et al. 2006), habitat structure (Steinman et al. 2003), and dynamics of other trophic levels (Carpenter et al. 2001). While numer686

Liston et al., EUTROPHICATION IMPACTS WETLAND INVERTEBRATES The Florida Everglades is a highly oligotrophic system comprised of over 365,000 ha of freshwater wetlands (Davis et al. 1994). Eutrophication following phosphorus (P) additions is a primary threat to the environmental integrity of the Everglades (Everglades Forever Act, Florida Statutes 373.4592), especially in northern portions of the system. In recent years, numerous experimental and correlative studies have sought to describe system response to eutrophication. Nutrient loading studies have shown that periphyton rapidly accumulates P in proportion to the loading rate and that as P concentrations increase, physiological changes occur in periphyton mats (McCormick et al. 2002, Gaiser et al. 2005, 2006). Periphyton biomass increases with P-enrichment, but at high P levels calcareous floating periphyton mats are lost and replaced by an assemblage of filamentous cyanobacteria, filamentous green algae, and diatoms (McCormick and O’Dell 1996, McCormick et al. 2002, Gaiser et al. 2005, 2006). Fewer studies have documented the response of Everglades’ aquatic fauna to eutrophication, leaving the implications for higher trophic levels poorly understood. For example, studies conducted in northern areas of the Everglades (Water Conservation Area 2A) reported higher density of macroinvertebrates in open sloughs at enriched sites than unenriched sites (Rader and Richardson 1994), while more recent studies conducted in the same area found an increase in invertebrate density with enrichment using sweep nets, and a decrease using Hester-Dendy samplers (McCormick et al. 2004). Other studies have found the highest invertebrate density at intermediate levels of enrichment (King 2001). Macroinvertebrate abundance and biomass also showed a positive log-linear response to enrichment in an experimental mesocosm study (King 2001). Turner et al. (1999) found no difference in invertebrate standing crop at enriched and unenriched sites, attributing this pattern to topdown regulation by fishes. No previous studies, however, have focused on eutrophication effects in less disturbed marshes of the southern portion of the system. This study documents macroinvertebrate response to experimental P-loading in in situ mesocosms in Taylor Slough, Everglades National Park (ENP). Taylor Slough is characterized by extensive floating mats of calcareous periphyton and benthic mats. These floating mats provide both food and habitat for an abundant macroinvertebrate community that may be underrepresented by traditional sampling methods (Liston and Trexler 2005). Here, we target two key macroinvertebrate microhabitats, floating

687

periphyton mats and loose, flocculent benthic matter (hereafter called ‘‘floc’’), and describe variation in community structure and macroinvertebrate abundance with increased levels of P-loading. This work provides insight into the impact of eutrophication on consumer communities in the southern Everglades. METHODS Mesocosm Design Two mesocosm sites were constructed in Taylor Slough, ENP in Fall 1999 (TSN: 25u199240 N, 80u389200 W; TSS: 25u139510 N, 80u429160 W; Figure 1). Twelve circular mesocosm enclosures (1.2 m high 3 1.85 m diameter) were constructed from Lexan Sunlite, a polycarbonate UV-resistant material that allows for high PAR transmission. Each enclosure was perforated with numerous 10cm diameter holes to allow for water exchange and the movement of invertebrates and small fish between enclosures and the marsh. A sliding collar, made of the same material as the mesocosm and perforated with holes in the same pattern as the enclosure, was fitted around each mesocosm to allow the enclosure to be ‘‘opened’’ and ‘‘closed’’ to the surrounding marsh. No enclosures were placed at three locations in each site to serve as ‘‘open controls’’ to detect enclosure effects. Mesocosms were accessed by means of a fixed elevated walkway to minimize disturbance (see McCormick and O’Dell 1996, McCormick et al. 2001). P Loading Mesocosms were loaded weekly with orthophosphate (NaH2PO4) from November 3, 1999 to January 30, 2002 to achieve specific phosphorus (P) loading rates; P loading was not performed from December 6, 2000 to August 22, 2001 and for several weeks when low water levels or other logistical factors prevented access. Four loading rates were randomly assigned to each of the 12 mesocosms: control (0 g P/m2/yr), low (0.2 g P/m2/yr), intermediate (0.8 g P/m2/yr), and high (3.2 g P/m2/yr). Phosphorus was added manually as weekly pulses mixed with slough water using a gravity-feed system. Mesocosm collars were closed immediately prior to P loading and remained closed for approximately 24 h to allow removal (abiotic and biotic) of the added P from the water column (Jones 2001, McCormick et al. 2001, Noe et al. 2003). Mesocosms were left open between weekly P loading events in order to maintain background water quality condi-

688

Figure 1.

WETLANDS, Volume 28, No. 3, 2008

Location of two mesocosm sites (TSN and TSS) in Taylor Slough, Everglades National Park (ENP).

tions in the enclosures and to minimize changes caused by lack of flow. Average daily water depths at each site were estimated based on regressions with nearby hydrologic gauging stations (TSN: R2 5 0.985, TSS: R2 5 0.910; Figure 2). Soil (0–3 cm depth) and floc were collected in August 2001 and periphyton was collected in January 2002 to obtain

estimates of total phosphorus (TP) in mesocosms. Floc and soil TP were determined on acid-digested samples (USEPA 1983, 1986). Macroinvertebrate Sampling Macroinvertebrate densities were quantified February 13–14, 2002 by taking five 6-cm diameter floating periphyton mat cores and five 6-cm diameter benthic floc cores from each mesocosm (Liston 2006). All remaining periphyton was collected from each mesocosm to determine total periphyton biomass. Due to decreased mat coverage typical of P enrichment (McCormick and O’Dell 1996), floating mat samples could be obtained from only 27% of intermediate P treatments, and no periphyton samples could be obtained from high P treatments. Sample Processing

Figure 2. Estimated average daily water depths at two sites (TSN and TSS) throughout the study. The duration of weekly P-loading is indicated. Horizontal dashed line represents the approximate ground level.

Periphyton and floc cores were stained with Rose Bengal and refrigerated for $ 12 h. Each sample was rinsed in a 250-mm sieve and transferred to a petri dish for processing. Under a dissecting

Liston et al., EUTROPHICATION IMPACTS WETLAND INVERTEBRATES

689

Figure 3. Total phosphorus (mg/g) in A) periphyton, B) floc, and C) soil (0–3 cm) in mesocosms at two sites (TSN and TSS) across P-loading levels (OC 5 open control, C 5 control (0 g P/m2/yr), LO 5 0.2 g P/m2/yr, INT 5 0.8 g P/m2/yr, HI 5 3.2 g P/m2/yr). Periphyton was absent in high P treatments. Error bars indicate 6 1 SE.

microscope, all animals . ,1 mm in length were removed, identified to the lowest feasible taxonomic level, and preserved in 70% ethanol. Once all animals were removed, the substrate was dried to constant mass at 70uC for at least 48 h and incinerated at 500uC for 3 h to permit calculation of ash-free dry mass (AFDM) and a standardization of densities (no. invertebrates/g substrate AFDM). Data Analyses Analyses of macroinvertebrate data focused on common taxa (incidence $ 10%). Floating periphyton mat and benthic floc communities (relative abundance of macroinvertebrates) were compared using one-way analysis of similarities (ANOSIM; Clarke 1993, Clarke and Warwick 1994) based on standardized Bray-Curtis dissimilarity matrices. Comparisons of taxon densities among microhabitats (floating periphyton mat and benthic floc) were made using one-way analysis of variance (ANOVA). Community structure was analyzed for each microhabitat using ANOSIM (site, P-loading level) followed by similarity percentage breakdowns (SIMPER) to determine which taxa contributed to observed patterns. TP, periphyton biomass, and density of common taxa were analyzed using factorial ANOVA to describe variation between sites and across P-loading levels. Periphyton biomass (g AFDM) and taxon densities (no./g AFDM) were ln(y+1) transformed prior to all analyses to fulfill assumptions of normality. We report results based on type three sums-of-squares (Shaw and Mitchell-Olds 1993).

RESULTS Nutrient Analyses Periphyton TP was significantly higher at TSN than TSS in control and intermediate treatments (F1,13 5 16.09, P 5 0.001; pairwise: control P 5 0.03, intermediate P 5 0.01). Periphyton TP was significantly higher at intermediate P dosing levels than at control and low levels (F3,13 5 27.16, P , 0.001; Figure 3A). Floc TP was not different between sites (P . 0.05), but was significantly higher in mesocosms with high P loads than those with no added P (control) or low P loads (F3,13 5 11.26, P , 0.001; Figure 3B). Soil TP did not vary across sites or across P-loading levels (P . 0.05; Figure 3C). Variation in Microhabitat Communities We observed differences in community structure and abundance of macroinvertebrates in periphyton mat and benthic microhabitats. Multivariate analysis revealed significant differences in the structure of floating mat and floc communities (Global R 5 0.281, P 5 0.001). ANOVA indicated densities of all six common taxa and total density were higher in floating periphyton mats (Table 1). The magnitude of difference between densities in these microhabitats ranged from 2.3 to 15.8 times for individual taxa and was 3.7 times for total invertebrate density. Inter-Site Variation Total periphyton biomass (g AFDM) was 4.9 times higher at TSS than TSN (F1,20 5 20.2, P , 0.001; Table 2A). Community structure and abun-

690


Table 1. ANOVA of macroinvertebrate density (no./g AFDM) among periphyton mat and benthic floc microhabitats. Densities of all common taxa (and total invertebrates) were greater in periphyton mats. F1,22

P

R2

Magnitude higher in mat

5.49 14.97 22.99 8.17 19.98 8.54 29.65

0.029 0.001 , 0.001 0.009 , 0.001 0.008 , 0.001

0.200 0.405 0.511 0.271 0.476 0.280 0.574

2.33 6.23 13.43 3.03 15.83 4.43 3.73

Taxa Nematoda Hyalella azteca (Saussure) Bezzia Dasyhelea Diptera (pupa) Chironomidae Total invertebrates

dance of both periphyton mat and benthic floc macroinvertebrates were different between TSN and TSS. Periphyton-mat macroinvertebrate community structure varied among sites (Global R 5 0.652, P 5 0.001), driven by Chironomidae, Dasyhelea (Ceratopogonidae), and Nematoda (cumulative dissimilarity 5 80.1%). Densities of mat-dwelling Chironomidae, Nematoda, and total invertebrates were 8.7, 5.5, and 2.8 times higher, respectively, at TSN than TSS (Table 2B). Benthic floc community structure also differed between sites (Global R 5 0.837, P 5 0.001), driven by Chironomidae, Dasyhelea, and Nematoda (cumulative dissimilarity 5 82.5%). Density of floc-dwelling Chironomidae and total invertebrates were 10.7 and 1.4 times higher, respectively, at TSN and densities of Dasyhelea and Hyalella azteca (Saussure) were 3.6 and 2.1 times higher, respectively, at TSS (Table 2C).

Nutrient Effects Phosphorus loading in mesocosms significantly altered both floating periphyton mat and benthic floc macroinvertebrate communities. Total periphyton biomass decreased with P enrichment at both sites (Table 2A, Figure 4). In floating periphyton mats, relative abundances (community structure) of invertebrate taxa showed no variation with enrichment (Global R 5 20.009, P 5 0.508), although total invertebrate density increased with intermediate P loads at TSS (no samples were collected from high P treatments due to the absence of a periphyton mat; Table 2B, Figure 5). Benthic floc community structure at both sites varied across P-loading levels (Global R 5 0.410, P 5 0.001). Densities of Chironomidae, Dasyhelea, and total invertebrates decreased with increased Ploading level (Table 2C, Figure 5). Density of H.

Table 2. ANOVA of total periphyton biomass (g AFDM) (A) and macroinvertebrate density (no./g AFDM) in floating periphyton mat (B) and benthic floc (C) samples between sites (TSN: Taylor Slough North, TSS: Taylor Slough South) and among P-loading levels (open control, control, low, intermediate, high). No periphyton samples were collected in high P mesocosms due to absence of the floating mat. The only common taxa shown are those with significant models (P # 0.05, indicated in bold). Site A. Periphyton Biomass

F1,20

P-loading level Site 3 P-loading level P

F4,20

P

20.18 , 0.001 15.48 , 0.001 B. Floating Periphyton Mat Nematoda Chironomidae Total invertebrates C. Benthic Floc Hyalella azteca Dasyhelea Chironomidae Total invertebrates

F1,14

P

46.39 , 0.001 75.05 , 0.001 34.98 , 0.001 F1,20

P

F3,13 1.31 2.76 5.66 F4,20

F4,20 2.11

P 0.118

R2

Magnitude higher at site

0.819

4.93 at TSS

2

P

F3,13

P

R

0.311 0.082 0.009

0.82 0.78 1.39

0.503 0.523 0.288

0.804 0.868 0.814

P

F4,20

P

R2

1.53 0.72 1.38 1.06

0.231 0.585 0.276 0.401

0.772 0.700 0.850 0.597

5.24 0.033 14.10 , 0.001 17.75 , 0.001 6.53 0.002 94.28 , 0.001 3.37 0.029 3.69 0.069 5.42 0.004

5.53 at TSN 8.73 at TSN 2.83 at TSN

2.13 at TSS 3.63 at TSS 10.73 at TSN 1.43 at TSN

Liston et al., EUTROPHICATION IMPACTS WETLAND INVERTEBRATES

Figure 4. Total periphyton biomass (AFDM) in mesocosms at two sites (TSN and TSS) across P-loading levels (OC 5 open control, C 5 control (0 g P/m2/yr), LO 5 0.2 g P/m2/yr, INT 5 0.8 g P/m2/yr, HI 5 3.2 g P/m2/yr). Error bars indicate 6 1 SE.

azteca increased at intermediate and high P levels at TSS, but remained unchanged at TSN. DISCUSSION Variation in macroinvertebrate community structure between microhabitats observed in this study was similar to what has previously been described (Liston and Trexler 2005, Liston 2006). Densities of all common taxa were higher in periphyton mats than benthic floc, but differences were most marked in H. azteca, Bezzia (Ceratopogonidae), and Diptera pupae, whose densities were more than five times higher in floating mats. Chironomidae and Dasyhelea densities were more than three times higher in periphyton mats, and Nematoda density was more than two times higher. Ceratopogonidae and Diptera pupae were usually encased within the periphyton matrix, which may be an indication of the importance of (or preference for) this substrate for these taxa. It should be noted, however, that comparisons of floating periphyton and benthic communities could only be made at control, low P, and a few intermediate P treatments because of the disappearance of the periphyton mat with enrichment. There was a relatively large (four-fold) difference in the applied P load between low and intermediate P levels, and between intermediate and high P levels, and it is unclear how mat-dwelling communities respond as they approach the threshold where the periphyton mat disappears. It is unlikely that the 8-month pause in P-loading affected the outcome of this experiment as much of the lapse corresponded with marshes being dry

691

(Figure 2). Additionally, Everglades’ soils have been shown to accumulate and retain phosphorus extremely well despite periodic drying events (Newman et al. 2002, Noe et al. 2003, White et al. 2004). In this study, we observed the break-up and disappearance of the periphyton mat with P enrichment that has been noted in P-enriched regions of the Everglades (McCormick et al. 2002; Gaiser et al. 2005, 2006). Periphyton biomass decreased with enrichment, and periphyton was absent from many intermediate and all high P treatments. As periphyton biomass decreased, macroinvertebrate density within the mat increased, reaching a maximum in intermediate P treatments that was 2.6 times higher than control treatments. While it is difficult to determine the mechanism for these observations, one hypothesis is a concentration of mat infauna as their habitat disappears. Liston (2006), however, reported higher densities of mat infauna at enriched sites even when corrections were made for reduced mat coverage. Contrary to the trend observed in periphyton mats, we saw a gradual decrease in benthic floc macroinvertebrate density with increased P levels. A similar pattern was reported by McCormick et al. (2004) using HesterDendy samplers (placed directly above the substrate) along a nutrient gradient in northern portions of the system. They attributed the pattern to a deterioration of conditions near the sediment-water interface. Increased phosphorus loading in this system has been shown to be associated with a marked decline in dissolved oxygen and damped diel fluctuations, but these effects were only seen at higher P-loading levels than those used in this study and were not evident until the third year of loading (McCormick and Laing 2003). In our experiment, macroinvertebrates may indicate a deterioration of conditions before they are detectable by our measuring devices. Comparisons of data collected in this study to those collected in the open marsh in other parts of the Everglades using the same sampling method (Liston 2006, Liston and Trexler unpublished data) suggest the discrepancy between benthic H. azteca density in mesocosms versus the density in open controls is likely a deleterious enclosure effect. While the nature of this variation is uncertain (e.g., consumption by predators, response to reduced flow), we did not observe this effect with any other taxa. Differences observed between the two mesocosm sites are consistent with our interpretation of enrichment effects at each local site. TSS was ,12 km SSW of TSN (in an area that is naturally lower in TP availability) and had slightly lower periphyton TP, but considerably higher periphyton biomass. This suggests that long-term exposure to P

692


Figure 5. Density (no./g AFDM) of common macroinvertebrates in floating periphyton mats and benthic floc in mesocosms at two sites (TSN and TSS) across P-loading levels (OC 5 open control, C 5 control (0 g P/m2/yr), LO 5 0.2 g P/m2/yr, INT 5 0.8 g P/m2/yr, HI 5 3.2 g P/m2/yr). No periphyton samples were collected in high P treatments. Error bars indicate 6 1 SE.

Liston et al., EUTROPHICATION IMPACTS WETLAND INVERTEBRATES levels that are only slightly higher than ambient may have noticeable effects on periphyton mats (Gaiser et al. 2005). Macroinvertebrate density was generally higher at TSN than TSS, especially in periphyton mats. TSS was more sensitive to the applied P loads than TSN; we noted a dramatic reduction in periphyton biomass and abrupt increase in mat invertebrate densities between low and intermediate treatments at that site. It is unclear why densities of benthic Dasyhelea and H. azteca were considerably higher at TSS than TSN. Since both taxa are often found within (or attached to the surface of) periphyton mats, it is possible that TSS had a greater amount of benthic periphyton than TSN. TSS typically has a lower density of small fishes than does TSN (Trexler et al. 2002), and these may decrease local macroinvertebrate abundance by predation (Liston 2006). Results from this study have important implications for understanding the effects of eutrophication on the Everglades food web. Collections of fish in these mesocosms in 2000 indicated total fish abundance was higher in high-P treatments, but patterns were driven by herbivorous flagfish (Jordanella floridae Goode & Bean) (Trexler et al. 2002). Gaiser et al. (2005) reported that fish biomass in experimental P-dosed flumes in Shark River Slough, ENP, showed complex fluctuations in response to nutrient level and the duration of dosing. Periphyton mats provide valuable refuge for macroinvertebrates from fish predators (Browder et al. 1994). Loss of periphyton habitat with eutrophication may make infauna more available to predators (Smith 2004). The highly calcified periphyton mats found in Taylor Slough probably serve as a better refuge for macroinvertebrates than mats that are more edible and have less habitat structure. Our data suggest that loss of periphyton mats due to eutrophication results in a decrease in macroinvertebrate standing stock in Taylor Slough because mat infauna fail to move into benthic substrates in response to mat loss. The transfer of secondary productivity from invertebrates to fish is consistent with data in Turner et al. (1999) indicating an increase in small fish with P enrichment below levels leading to oxygen depletion, but little or no change in macroinvertebrate density. Microhabitat differences in the response of macroinvertebrate communities caused by nutrient enrichment may help explain the contradictory trends observed in previous studies (Rader and Richardson 1994, Turner et al. 1999, King 2001, McCormick et al. 2004). Each sampling method (e.g., sweep nets, benthic cores, Hester-Dendy samplers), targets different microhabitat communities or, most often, combines several different microhabitat communi-

693

ties. Combining communities with different responses to P enrichment may obscure results, making interpretations of whole community response quite difficult. In this study, failing to separate microhabitat communities would have indicated an increase in macroinvertebrate density with low to intermediate levels of enrichment and a dramatic decrease in density at high P levels, with no insight as to the mechanism behind this ‘hump-shaped’ response. Differentiating these microhabitat community dynamics is especially important in southern marl prairies where calcareous periphyton mats are a prominent feature, are extremely sensitive to eutrophication, and serve as critical macroinvertebrate habitat. ACKNOWLEDGMENTS This study was conducted in cooperation with the South Florida Water Management District (Paul McCormick, project leader), without whose financial and logistical support it would not have been possible (EPA Agreement #CR827565-01-0). We are grateful for field assistance provided by Amanda Hewitt, Walter DeLoach, J. Shawna Baker, R. Brooke Shamblin, Lawrence Wolski, and Raul Urgelles and the laboratory assistance of Erika Grumbach. Additional financial support was provided by STAR-GRO Fellowship No. U–915916 from the US Environmental Protection Agency and National Science Foundation Grant No. 9910514 (Florida Coastal Everglades LTER). This is contribution no. 146 of the FIU Tropical Biology Program and no. 378 from the Southeast Environmental Research Center at FIU.

LITERATURE CITED Brauns, M., X.-F. Garcia, M. T. Push, and N. Walz. 2007. Eulittoral macroinvertebrate communities of lowland lakes: discrimination among trophic states. Freshwater Biology 52:1022–32. Browder, J. A., P. J. Gleason, and D. R. Swift. 1994. Periphyton in the Everglades: spatial variation, environmental correlates, and ecological implications. p. 379–416. In S. M. Davis and J. C. Ogden (eds.) Everglades: The Ecosystem and Its Restoration. St. Lucie Press, Delray Beach, FL, USA. Carpenter, S. R., J. J. Cole, J. R. Hodgson, J. F. Kitchell, M. L. Pace, D. Bade, K. L. Cottingham, T. E. Essington, J. N. Houser, and D. E. Schindler. 2001. Trophic cascades, nutrients, and lake productivity: whole-lake experiments. Ecological Monographs 71:163–86. Chambers, P. A., R. Meissner, F. J. Wrona, H. Rupp, H. Guhr, J. Seeger, J. M. Culp, and R. B. Brua. 2006. Changes in nutrient loading in an agricultural watershed and its effects on water quality and stream biota. Hydrobiologia 556:399–415. Clarke, K. R. 1993. Non-parametric multivariate analyses of change in community structure. Australian Journal of Ecology 18:117–43.

694 Clarke, K. R. and R. M. Warwick. 1994. Change in Marine Communities: An Approach to Statistical Analyses and Interpretation. Natural Environmental Research Council, Plymouth Marine Laboratory, Plymouth, UK. Cross, W. F., J. B. Wallace, A. D. Rosemond, and S. L. Eggert. 2006. Whole-system nutrient enrichment increases secondary productivity in a detritus-based ecosystem. Ecology 87: 1556–65. Davis, S. M., L. H. Gunderson, W. A. Park, J. Richardson, and J. Mattson. 1994. Landscape dimension, composition, and function in a changing Everglades ecosystem. p. 419–44. In S. M. Davis and J. C. Ogden (eds.) Everglades: The Ecosystem and Its Restoration. St. Lucie Press, Delray Beach, FL, USA. Duinen, G. A., T. Timm, A. J. P. Smolders, A. M. T. Brock, W. C. E. P. Verberk, and H. Esselink. 2006. Differential response of aquatic oligochaetes to increased nutrient availability – a comparative study between Estonian and Dutch raised bogs. Hydrobiologia 564:143–55. Feio, M. J., S. F. P. Almeida, S. C. Craveiro, and A. J. Calado. 2007. Diatoms and macroinvertebrates provide consistent and complimentary information on environmental quality. Fundamental and Applied Limnology/Archiv fu ¨ r Hydrobiologie 169:247–58. Gabor, T. S., H. R. Murkin, M. P. Stainton, J. A. Boughen, and R. D. Titman. 1994. Nutrient additions to wetlands in the Interlake region of Manitoba, Canada: effects of a single pulse addition in spring. Hydrobiologia 279/280:497–510. Gaiser, E. E., D. L. Childers, R. D. Jones, J. H. Richards, L. J. Scinto, and J. C. Trexler. 2006. Periphyton responses to eutrophication in the Florida Everglades: cross-system patterns of structural and compositional change. Limnology and Oceanography 51:617–30. Gaiser, E. E., J. C. Trexler, J. H. Richards, D. L. Childers, D. Lee, A. L. Edwards, L. J. Scinto, K. Jayachandaran, G. B. Noe, and R. D. Jones. 2005. Cascading ecological effects of low-level phosphorus enrichment in the Florida Everglades. Journal of Environmental Quality 34:717–23. Hann, B. J. and L. G. Goldsborough. 1997. Responses of a prairie wetland to press and pulse additions of inorganic nitrogen and phosphorus: invertebrate community structure and interactions. Archiv fu ¨ r Hydrobiologie 140:169–94. Jahnke, B. J., D. H. Rickerl, T. Kirschenmann, D. E. Hubbard, and D. Kringen. 2001. Wetland invertebrate abundances and correlations with wetland water nutrients. Proceedings of the South Dakota Academy of Science 80:321–34. Jones, R. D. 2001. Phosphorus cycling. p. 450–55. In C. J. Hurst, R. L. Crawford, G. R. Knudsen, M. J. McInerney, and L. D. Stetzenbach (eds.) Manual of Environmental Microbiology, second edition. ASM Press, Washington, DC, USA. King, R. S. 2001. Dimensions of invertebrate assemblage organization across a phosphorus-limited Everglades landscape. Ph.D. Dissertation. Duke University, Durham, NC, USA. Langdon, P. G., Z. Ruiz, K. P. Brodersen, and I. D. L. Foster. 2006. Assessing lake eutrophication using chironomids: understanding the nature of community response in different lake types. Freshwater Biology 51:562–77. Liston, S. E. 2006. Interactions between nutrient availability and hydroperiod shape macroinvertebrate communities in Florida Everglades marshes. Hydrobiologia 569:343–57. Liston, S. E. and J. C. Trexler. 2005. Spatiotemporal patterns in community structure of macroinvertebrates inhabiting calcareous periphyton mats. Journal of the North American Benthological Society 24:832–44. McCormick, P. V. and J. A. Laing. 2003. Effects of increased phosphorus loading on dissolved oxygen in a subtropical wetland, the Florida Everglades. Wetlands Ecology and Management 11:199–216.

WETLANDS, Volume 28, No. 3, 2008 McCormick, P. V., S. Newman, S. Miao, D. E. Gawlik, D. Marley, K. R. Reddy, and T. D. Fontaine. 2002. Effects of anthropogenic phosphorus inputs on the Everglades. p. 83–126. In J. W. Porter and K. G. Porter (eds.) The Everglades, Florida Bay, and Coral Reefs of the Florida Keys: An Ecosystem Sourcebook. CRC Press, Boca Raton, FL, USA. McCormick, P. V. and M. B. O’Dell. 1996. Quantifying periphyton responses to phosphorus enrichment in the Florida Everglades: a synoptic-experimental approach. Journal of the North American Benthological Society 15:450–68. McCormick, P. V., M. B. O’Dell, R. B. E. Shuford, III, J. G. Backus, and W. C. Kennedy. 2001. Periphyton responses to experimental phosphorus enrichment in a subtropical wetland. Aquatic Botany 71:119–39. McCormick, P. V., R. B. E. Shuford, III, and P. S. Rawlik. 2004. Changes in macroinvertebrate community structure and function along a phosphorus gradient in the Florida Everglades. Hydrobiologia 529:113–32. Newman, S., S. Miao, A. L. Wright, and K. R. Reddy. 2002. Biogeochemical and macrophyte responses. In S. Newman, P. V. McCormick, S. L. Miao, J. Trexler, K. R. Reddy, R. B. E. Shuford, III, A. L. Wright, S. Baker, and X. Pagan (eds.) Effects of changes in phosphorus levels on the central and southern Everglades. EPA Agreement #CR827565-01-0. Report submitted to EPA Gulf Breeze, FL. Noe, G. B., L. J. Scinto, J. Taylor, D. L. Childers, and R. D. Jones. 2003. Phosphorus cycling and partitioning in an oligotrophic Everglades wetland ecosystem: a radioisotope tracing study. Freshwater Biology 48:1993–2008. Rader, R. B. and C. J. Richardson. 1994. Response of macroinvertebrates and small fish to nutrient enrichment in the northern Everglades. Wetlands 14:134–46. Saloom, M. E. and R. S. Duncan. 2005. Low dissolved oxygen levels reduce anti-predator behaviours of the freshwater clam Corbicula fluminea. Freshwater Biology 50:1233–38. Shaw, R. G. and T. Mitchell-Olds. 1993. Anova for unbalanced data: an overview. Ecology 74:1638–45. Smith, S. E. L. 2004. Defining the role of floating periphyton mats in shaping food-web dynamics in the Florida Everglades. Ph.D. Dissertation. Florida International University, Miami, FL, USA. Steinman, A. D., J. Conklin, P. J. Bohlen, and D. G. Uzarski. 2003. Influence of cattle grazing and pasture land use on macroinvertebrate communities in freshwater wetlands. Wetlands 23:877–89. Trexler, J. C., S. Baker, and X. Pagan. 2002. Response of invertebrates and fish to changes in phosphorus levels in the central and southern Everglades. In S. Newman, P. V. McCormick, S. L. Miao, J. Trexler, K. R. Reddy, R. B. E. Shuford, III, A. L. Wright, S. Baker, and X. Pagan (eds.) 2002. Effects of changes in phosphorus levels on the central and southern Everglades. EPA Agreement # CR827565-01-0. Report submitted to EPA Gulf Breeze, FL. Turner, A. M., J. C. Trexler, C. F. Jordan, S. J. Slack, P. Geddes, J. H. Chick, and W. F. Loftus. 1999. Targeting ecosystem features for conservation: standing crops in the Florida Everglades. Conservation Biology 13:898–911. U.S. Environmental Protection Agency. 1983. Methods for chemical analyses of water and wastes. Environmental Monitoring and Support Laboratory, Cincinnati, OH, USA. U.S. Environmental Protection Agency. 1986. Test methods for evaluating solid waste, physical and chemical methods. US EPA, Cincinnati, OH, USA. White, J. R., K. R. Reddy, and M. Z. Moustafa. 2004. Influence of hydrologic regime and vegetation on phosphorus retention in Everglades stormwater treatment area wetlands. Hydrological Processes 18:343–55. Manuscript received 3 December 2007; accepted 26 March 2008.