Hydrobiologia 443: 177–185, 2001. © 2001 Kluwer Academic Publishers. Printed in the Netherlands.
177
Assessing ecosystem integrity of restored prairie wetlands from species production–diversity relationships Paul M. Mayer1,2 & Susan M. Galatowitsch3 1 Graduate
Program in Conservation Biology, Department of Ecology, Evolution and Behavior, University of Minnesota-Twin Cities, St. Paul, MN 55108, U.S.A. 2 Current address: U.S. Environmental Protection Agency, National Risk Management Research Laboratory, 919 Kerr Research Drive, Ada, OK 74820, U.S.A. E-mail:
[email protected] 3 Departments of Horticulture and Landscape Architecture, University of Minnesota-Twin Cities, St. Paul, MN 55108, U.S.A. E-mail:
[email protected] Received 17 August 1999; in revised form 25 September 2000; accepted 18 October 2000
Key words: diatom, diversity, ecological assessment, ecosystem integrity, restored wetland
Abstract We assessed ecosystem integrity in restored prairie wetlands in eastern South Dakota, U.S.A., by examining the relationship between and diatom diversity and production. We asked three questions: (1) Is production related to species diversity? (2) Can production-diversity relationships be used to distinguish between restored and reference wetlands with the purpose of assessing ecological integrity? (3) Are production-diversity relationships influenced by species composition? Eight undisturbed, unrestored wetlands were chosen as references to compare to eight wetlands restored after drainage. Diatoms were collected from artificial substrates that allowed communities to be transplanted from restored to reference wetlands and visa versa. Production was measured as total cell biovolume and diversity as species richness. Neither diversity nor production alone differed between restored and reference wetlands. However, production was negatively related to diversity at restored wetlands, whereas production at reference wetlands was not. Communities transplanted from reference to restored wetlands exhibited a productiondiversity relationship like that observed among control samples in restored wetlands. Likewise, communities transplanted from restored to reference wetlands apparently lost any such relationship after they were relocated. Production was dependent on species composition. Furthermore, production of some species differed by restored and reference wetland type. The negative relationship observed between diversity and production was strongly influenced by Rhopalodia gibba and Epithemia species, suggesting that these species were superior competitors under the conditions found in some restored wetlands. We consider restored wetlands displaying the highest production:diversity ratio to be the most impaired sites, based on the extreme deviation from reference wetlands. We conclude that the relationships between diversity and production provided a rapid measure of restored wetland integrity with respect to baseline conditions observed in reference sites.
Introduction Assessing ecological integrity are goals of researchers and managers involved in restoration. Integrity can be gauged only in relation to reference ecosystems not impacted by anthropogenic disturbance (Rodriguez, 1994). Therefore, integrity is probably best defined
as a deviation from the baseline measure of an ecological characteristic of interest in reference ecosystems (Karr, 1991, 1994). Karr & Dudley (1981) suggested measuring characteristics that reflect an ecosystem’s “capability of supporting and maintaining a balanced, integrated, adaptive community of organisms having species composition, diversity, and functional organ-
178 ization comparable to that of natural habitats of the region”. Therefore, our approach in this study was to compare a community of organisms in impaired aquatic ecosystems and in undisturbed, natural systems nearby. The approach of using reference wetlands provides a set of reference standards for the ecological indicator of choice and establishes a ‘template’ for restoration goals (Brinson & Rheinhardt, 1996). Selection of an appropriate ecological indicator that fit the Karr & Dudley (1981) criteria, was based on current experimental evidence demonstrating that species diversity and ecosystem function are inextricably linked (Naeem et al., 1994; Tilman & Downing, 1994; Tilman et al., 1996, 1997; Hooper & Vitousek, 1997; McGrady-Steed et al., 1997). Though the relationship of diversity to function may vary (Schläpfer & Schmid, 1999; Waide et al., 1999), the pattern in reference ecosystems serves as a baseline from which to compare patterns in disturbed systems. Furthermore, because disturbance often affects species composition, diversity, and functional organization differently (Schindler, 1987, 1990; Cottingham & Carpenter, 1998), taken alone, an indicator of structure or function may fall short of characterizing true ecosystem integrity (Risser, 1995). Thus, the connection between diversity and ecosystem function may provide a useful gauge of ecosystem integrity and recovery of restored systems. Restored prairie wetlands in South Dakota, U.S.A. were chosen to test the utility of using a diversityecosystem function relationship as an indicator of integrity in aquatic systems. Many prairie wetlands in the northern Great Plains of the U.S. and Canada (Cowardin et al., 1979; Kantrud et al., 1989) have been drained and converted to agricultural uses (Dahl, 1990). However, some wetlands have recently been restored through the United States’ Food Security Act of 1985 and the associated Conservation Reserve Program (Galatowitsch & Van Der Valk, 1994). Recovery of restored wetlands in this region has been slow and incomplete as demonstrated by analyses of plant and bird communities (Delphey & Dinsmore, 1993; Galatowitsch & Van Der Valk, 1996). We chose to examine diatom communities as our ecological indicator. Diatoms have long been used as ecological indicators of aquatic systems (Patrick, 1949; Shubert, 1984; Stoermer & Smol, 1999) because they respond quickly to ambient biogeochemical levels such as pH, silica, phosphorous, nitrogen and salinity (Tilman et al., 1982; Stoermer, 1984; Schindler, 1987; Stoermer & Smol, 1999) and to disturbance
events such as drought (Dodds et al., 1996) and flooding (Steinman & McIntire, 1990). Therefore, diatom presence and abundance should reflect current environmental conditions, and by inference, effects of past drainage disturbance. We examined diversity among diatom communities in prairie wetlands and estimated primary production as a measure of ecosystem function. The relationship between diversity and production of diatoms was used as a gauge of integrity for restored aquatic ecosystems. The purpose of this study was to answer the following questions: (1) Is ecosystem function related to species diversity? (2) If so, can the relationship between function and diversity be used to distinguish between restored and reference wetlands? That is, can examining the relationship be a useful method to assess ecological integrity? (3) How is this relationship influenced by species composition? In keeping with the definition of Karr & Dudley (Karr, 1981; Karr & Dudley, 1981) and the approach of Brinson & Rheinhardt (1996), integrity here is defined as a measure of the deviation from the baseline conditions measured in reference wetlands. Therefore, if diversity-function relationships in restored wetlands differed from those in reference wetlands, then restored wetlands were assumed to have lost ecological integrity as a function of drainage.
Study area Suitable wetland sites were located in the Prairie Coteau region of northeastern South Dakota in Marshall and Roberts Counties (45.2◦–46.0◦ N lat., 96.5◦– 98.0◦ W long.), an area characterized by the presence of numerous wetlands and lakes of glacial origin among mixed-grass prairie (Kantrud et al., 1989). Climate in this area is characterized by great annual temperature extremes and cyclic wet-drought periods (Hubbard, 1988; Kantrud et al., 1989). Much of the land in this region had been converted to grain production (e.g. wheat (Triticum spp.), barley (Hordeum spp.) and oats (Avena spp.)) by the early 1900s (Leitch, 1989), but high soil erosion rates prompted conversion to pasture soon thereafter. National Wetlands Inventory photographs, Soil Conservation Service soils maps and Waubay National Wildlife Refuge (WNWR) files were used to identify wetland types and sizes. All but one wetland selected were classified as semi-permanent (Cowardin et
179 al., 1979). Wetlands were characterized by emergent vegetation species such as Typha spp., Scirpus acutus (Muhl) Bigel. and Sparganium eurycarpum Engelm. and by such submergents as Utricularia vulgaris L. and Ceratophyllum demersum L. Eight restored wetlands, located on private lands enrolled in the Conservation Reserve Program where cultivation was prohibited or on Waterfowl Production Areas (WPA) managed by WNWR, were chosen for study. Livestock watering dugouts and/or roads had been constructed in or around four restored wetlands. One restored wetland possessed a water control structure, but water levels were not manipulated during the study. Eight undisturbed control wetlands (reference wetlands) that had never been drained were compared to restored wetlands. No roads, ditches, culverts, livestock dugouts or wells had been constructed in the reference wetlands. Reference wetlands were located on WPA’s where cultivation was prohibited. Wetlands had been restored by plugging drainage ditches with earth. Restoration occurred 3–15 (mean = 6.6, SD = 3.9) years previous to this study. No additional restoration to the basin such as reseeding, soil addition or surface grading was attempted. Most wetlands were drained about 50 years ago, according to the few records that remain. Drainage apparently altered hydrology sufficiently so that, on average, wetlands dried earlier in the year and in dry years, some cropping may have occurred within the basin. The purpose of drainage efforts in this area was to optimize grass production for cattle. Consequently, drainage in this area changed the hydrology of semi-permanent wetlands to that of seasonal or temporary wetlands. Cattle grazing was a disturbance (e.g. nutrient inputs) that could not be excluded when selecting restored or control wetlands. Although records are incomplete, grazing occurred at various intensities concurrently with and/or 1–2 years previously to the study at all restored and reference wetlands. All wetlands were ≥ 200 m from potential chemical or sediment inputs from nearby cultivated land.
Methods
range finder. A two-sample t-test was used to compare restored and reference wetland size and depth. Sampling Diatoms were collected in 1995 from artificial substrates placed at the centers of each wetland and at four additional points within the emergent vegetation-free (pelagic) zone. These four points were located by randomly choosing a compass direction and a percentage distance (10–90%) from the center sampling point to the edge of the emergent vegetation zone. We placed substrates consisting of 10 × 12 cm clear rectangular plates of mylarTM plastic suspended by floats approximately 30 cm below the water surface. The plates fluctuated with water level changes and rotated freely so that the plate surface constantly changed with respect to the direct rays of the sun. Plates were unprotected from grazers. Initial placement of plates in wetlands occurred from 31 May 1995 to 8 June 1995. Three plates were placed at each sampling point in each wetland. One of the plates was collected from each sampling point after approximately 5 weeks on 11–15 July 1995 (early sample) and the second plate was collected after approximately 10 weeks on 24 August to 3 September 1995 (late sample). The third plate served as the ‘transplant’ sample. Transplants were performed concurrently with the early-season sample collection period. Plates were exchanged randomly in a non-reciprocal pattern among wetlands. Plates from each randomly selected restored wetland were transplanted to a randomly selected reference wetland and vice versa. Plates were transported in an insulated cooler in which the plates were freely suspended in water collected from their respective wetlands. Total travel time between wetlands was ≤2 h. Diatoms appeared to adhere well to the plates during transport. All transplanted plates were collected concurrently with the late season samples. Plates were placed on ice in the field and later frozen to arrest cell senescence. Early and late season samples represent controls to the transplants. Enumeration and identification
Wetland size and depth Wetland depths (m) were measured at five randomly selected points in each wetland. Wetland size (ha) was estimated by measuring the basin dimensions, including the emergent vegetation zone, with an optical
Diatoms and other algae were removed from a known area of the plates with a razor blade. Organic matter in the samples was digested following the protocol of Stoermer et al. (1995). Slides of cleaned diatom frustules were prepared using the method described by
180 Scherer (1994). Diatoms were permanently mounted in NaphraxTM and examined at 1000× under oil using a Leitz Ortholux microscope fitted with an objective lens with an aperture of 1.30. Diatoms were identified to species from slide preparations with obviously well-dispersed frustules, following the enumeration methods of Battarbee (1986). Diatoms were enumerated by counting valves (considered as 1/2 of a frustule) along known transects using the microscope micrometer as the transect width. Girdle views were identified where possible and were counted as two valves. Identifications were made based on standard references (Hustedt, 1930; Patrick & Reimer, 1966, 1975; Hustedt & Jensen, 1985; Kramer & Lange-Bertalot, 1986, 1988, 1991a, b). Some difficult specimens were verified against a reference collection at Iowa Lakeside Laboratory (C. Reimer & E. Stoermer, pers. comm.). Valve fragments were categorized as 3/4, 1/2 or 1/4 of a whole valve and then summed to yield whole valve values. At least 500 valves were counted for each sample. One plate for each wetland was analyzed for each sample type (early season, late season and transplants). Thus, a total of 48 substrate samples were enumerated. Only species occurring at ≥5% relative density at ≥1 site were included in the analyses. Diatom counts were standardized by relating transect counts to the substrate area from which diatoms were sampled. Therefore, valve densities were measured per mm2 of the original substrate area sampled. This standardization helps to avoid the biases introduced into the results of certain multivariate analyses when counts are represented as percentages or proportions (Jackson, 1997). Production Diatom production was estimated as standing crop biomass measured from biovolume and calculated as a function of frustule shape and species density. Cell volume is a significant predictor of carbon content in diatoms (Menden-Deuer & Lessard, 2000). For volume calculation purposes, all frustule shapes were considered to be cylindrical. Median lengths and widths for each species were obtained from standard references (Patrick and Reimer, 1966, 1975; Hustedt & Jensen, 1985; Kramer & Lange-Bertalot, 1986, 1988, 1991a,b). Units of production are in microns3/mm2 of substrate. Production estimates were normalized by a log10 (x + 1) transformation (Poole, 1974) prior to statistical analyses.
Table 1. Mean size and depth of restored and reference wetlands observed in Marshall and Roberts Counties, South Dakota. See text for t-test results of the comparison between restored and reference wetlands Wetland type
Sample size
Size (ha) mean SD
Depth (m) mean SD
Restored
8
6.39
5.97
1.13
0.40
Reference
8
5.77
3.71
1.13
0.40
Analysis One-way ANOVA was used to test for the influence of species type on variability in total production. The ANOVA model included production as the dependent variable and species type as a factor. Two-way ANOVA was used to test the effects of wetland type (restored, reference), and sample type (early, late, transplanted) on species diversity and on production. Models included species diversity and production, respectively, as dependent variables with wetland type and sample type as factors. MANOVA was used to test variability in mean production among species by wetland type. The MANOVA model included species as dependent variables and wetland type as the independent variable. Wilks’ Lambda test was chosen as the multivariate test, while univariate F -tests were performed to test for production differences among species by wetland type (Wilkinson, 1998). Simple linear regression models were constructed to test for relationships between diversity and production. Because early and late samples may be influenced by season effects and the transplanted samples by environmental changes, sample types were analyzed separately. Therefore, models were constructed for each of the six ‘treatment-sample’ types (early, late and transplanted samples for each the restored and reference treatments). Results Wetland basin characteristics, production and diversity Restored and reference wetlands did not differ in size (t = 0.25, df = 14, P = 0.81; Table 1) or depth (t = 0.00, df = 14, P = 1.0; Table 1). Total diatom richness among all wetlands was 33 species (Appendix 1).
181 Appendix 1. Cumulative list of diatom species with ≥5% relative density in restored and reference wetlands in Marshall and Roberts Counties, South Dakota. (1) Acnanthes hungarica Grunow (2) Acnanthes lanceolata Br´ebisson ex Kützing (3) Acnanthes minutissima Kützing (4) Cocconeis placentula Ehrenberg (5) Cymbella cistula (Ehrenberg) Kirchner (6) Cymbella microcephala Grunow (7) Cymbella minuta Hilse ex Rabenhorst (8) Epithemia adnata (Kützing) Br´ebisson (9) Epithemia argus (Ehrenberg) Kützing (10) Epithemia sorex Kützing (11) Epithemia turgida (Ehrenberg) Kützing (12) Eunotia curvata (Kützing) Lagerstedt (13) Eunotia valida Hustedt (14) Fragilaria capucina var. mesolepta Rabenhorst (15) Gomphonema accuminatum Ehrenberg (16) Gomphonema dichotomum Kützing (17) Gomphonema gracile Ehrenberg (18) Gomphonema parvulum Kützing (19) Gomphonema subclavatum Grunow (20) Gomphonema subtile Ehrenberg (21) Gomphonema tenellum Kützing (22) Gomphonema truncatum Ehrenberg (23) Mastogloia smithii Thwaites ex W. Smith (24) Navicula gottlandica Grunow (25) Navicula minima Grunow (26) Navicula radiosa var. tenella (Br´ebisson ex Kützing) Grunow (27) Navicula radiosa var. radiosa Kützing (28) Nitzschia amphibia Grunow (29) Nitzschia intermedia Hantzsch ex Cleve and Grunow (30) Rhopalodia gibba (Ehrenberg) O. Müller (31) Synedra acus var. radians Kützing (32) Synedra tenera W. Smith (33) Synedra ulna Nitzsch
Table 2. Linear regression results of diversity on diatom production in restored and reference wetlands observed in Marshall and Roberts Counties, South Dakota Sample type F
Restored R2
P
F
Early
4.109
0.406
0.089
0.036
0.006
0.856
Transplant
3.892
0.393
0.096
0.633
0.095
0.456
13.338
0.690
0.011
0.700
0.105
0.435
Late
Reference R2 P
Figure 1. Simple linear regression plot of the relationship of diatom production to diversity in restored wetlands for early, late and transplanted samples.
Species richness within a wetland ranged from 8 to 24 species (mean = 16.9, SD = 3.6). Only one species was not found in both wetland types; Mastogloia smithii was found only in restored wetlands. Two-way ANOVA results revealed no differences in species diversity by wetland type (i.e. restored, reference) (F = 0.03, df = 1, P = 0.88) or sample type (i.e. early, late, transplant) (F = 0.90, df = 2, P = 0.41). Production within a wetland ranged from 1.04×105 to 1.35×108 microns3/mm2 (mean = 1.04×107, SD = 2.57×107). Two-way ANOVA results revealed no differences in total production by wetland type (F = 0.42, df = 1, P = 0.52) or sample type (F = 2.15, df = 2, P = 0.13). Relationship of production to species diversity Production was negatively related to diversity at all restored wetland sample categories (Table 2 and Fig. 1), whereas production at reference wetlands was not
Figure 2. Simple linear regression plot of the relationship of diatom production to diversity in reference wetlands for early, late and transplanted samples.
182
Figure 3. Mean production (±1 SE) of species by wetland type (shaded bars represent restored wetlands, clear bars represent reference wetlands). Letters denoting species correspond to the list in Appendix 1. Pairs of bars with an asterisk (∗ ) have significantly different production means (P < 0.05). See text for further explanation.
(Table 2 and Fig. 2). The transplanted diatom communities took on the relationship of the treatment to which they were relocated. That is, the relationship between production and diversity among communities transplanted from reference to restored wetlands was like that observed among control communities in restored wetlands. Likewise, communities transplanted from restored to reference wetlands apparently lost any such relationship after they were relocated. Relationship of production to species composition One-way ANOVA results indicated that total production was dependent upon species types (F = 38.62, df = 32, P < 0.001). MANOVA results indicated that species differed in their contribution to production by wetland type (Wilks’ Lambda = 0.13, F = 2.74, df = 33, 14, P = 0.02). Acnanthes hungarica, Gomphonema accuminatum and Gomphonem parvulum had higher mean production in restored wetlands than in reference (univariate F-tests, P ≤ 0.05), whereas Cocconeis placentula had higher mean production in reference wetlands (univariate F-test, P = 0.01). The negative relationship between species diversity and diatom production in restored wetlands was strongly influenced by high production among the sites with greatest production by Rhopalodia gibba, Epithemia adnata, Epithemia turgida and Epithemia
sorex (Fig. 2). R. gibba, E. turgida and E. adnata exhibited the 1st, 2nd, and 3rd highest overall production, respectively, among diatoms (Fig. 3). Therefore, restored sites exhibiting the most extreme ratios of high production to low diversity were those sites with greatest contribution by R. gibba, E. adnata, and E. turgida. No reference wetlands possessed such high production from these three species despite the observation that mean production of R. gibba, E. adnata and E. turgida was the same in reference and restored wetlands (MANOVA, univariate F-tests, P > 0.05). The influence of Rhopalodia and Epithemia species is further demonstrated by analyzing the relationship between species diversity and the combined production of Rhopalodia and Epithemia species as compared with the production of all other species. Production of Rhopalodia and Epithemia species was negatively related to diversity at restored wetlands but not at reference wetlands (F = 21.93, R2 = 0.50, P < 0.001; Fig. 4). Furthermore, production of all other species was not related to species diversity in either reference or restored wetlands (P > 0.4; Fig. 4). These data suggest that Rhopalodia and Epithemia species are superior competitors under the conditions found in some restored wetlands, displacing species and reducing overall diatom diversity.
Discussion Our study demonstrates the difficulty of assessing the condition of disturbed ecosystems when using single measures of ecosystem structure or function. We found that overall production and species diversity did not differ in restored and reference wetlands. Additionally, few species could be identified as potential indicators of drainage disturbance because all but one species were found in both restored and reference wetlands and only four species differed in production by wetland type. Furthermore, previous analysis at our study site did not reveal distinct differences in species composition between restored and reference wetlands (Mayer & Galatowitsch, 1999). However, the approach taken here to link ecosystem structure (species diversity) and function (production) by simultaneously examining two inextricably linked ecosystem variates was more revealing. We found that production was negatively related to diversity at restored wetlands but not at reference wetlands. Communities transplanted from reference to restored wetlands exhibited a production-diversity relationship like that observed
183
Figure 4. Simple linear regression plot of the relationship of diatom production to diversity in reference and restored wetlands sorted by R. gibba and Epithemia species combined (Epithemiaceae) and all other species.
among control samples in restored wetlands. Likewise, communities transplanted from restored to reference wetlands apparently lost any such relationship after they were relocated. Therefore, the transplant experiments suggested that restored wetlands could not support a level of integrity equivalent to that in the undisturbed, reference wetlands. The deviation of the restored wetlands from the reference wetlands suggests that restored wetlands had impaired ecological integrity. Restored sites displaying the highest production:diversity ratio must be considered the most impaired sites based on deviation from the baseline represented by reference wetlands. Experimental work indicates that low diversity communities often exhibit reduced ecosystem function, often measured as biomass production (e.g. Naeem et al., 1994; Tilman et al., 1997). However, in this study, production was highest in low-diversity restored sites owing to disproportionate production by R. gibba, E. adnata and E. turgida. These results suggest that high production is not necessarily a positive attribute of ecosystem function and may be an indicator of impairment in some systems. Some Rhopalodia and Epithemia species are known to form endosymbiotic relationships with N-fixing cyanobacteria (Drum & Pankratz, 1965; Geitler, 1977; Floener & Bothe, 1980; Fairchild & Lowe, 1984; Round et al., 1990). Although we do not have information about N-fixation rates in our study, it seems prudent
to consider the possibility that R. gibba and Epithemia species may have functioned differently than other diatoms in our observed communities. Therefore, the high production:diversity ratios observed at some restored wetlands may reveal a nutrient-based mechanism of competition and subsequent production response where species with N-fixing capabilities are favoured. R. gibba and Epithemia species may have responded to high phosphorous and/or decreasing nitrogen availability that allowed overwhelming production (De Yoe et al., 1992). Such a scenario fits a theoretical framework of resource competition which predicts decreased species diversity and domination by a few superior competitors, corresponding with increased nutrient availability and subsequent reduction in resource heterogeneity (Tilman, 1982; but see Hall et al., 2000). With respect to our original questions, we conclude that: (1) production of diatoms is related to species diversity, (2) production-diversity relationships of diatoms can be used to distinguish between restored and reference wetlands, and (3) production-diversity relationships in wetlands are influenced by diatom species composition. We submit that examining productiondiversity relationships was a useful approach to environmental assessment in an experimental design based on comparisons with reference sites. The rapid shift (≤ 5 weeks) in production-diversity relationships observed among the transplanted samples sug-
184 gests strong environmental control of diatom growth and survival, an observation supported by previous analyses of species composition shifts (Mayer & Galatowitsch, 1999). These data also suggest that residual diatom frustules from displaced or dead diatoms did not influence the analysis. Such rapid response to environmental change supports the use of diatoms in wetland assessment given that adequate information is available on both the structure and the function of the diatom community (Schindler, 1987, 1990; Grime, 1997; Johnson, 1998).
Acknowledgements Research funding came from the U.S. Bureau of Reclamation, Carolyn M. Crosby Fellowships and the Dayton-Wilkie Fund for Natural History. The Minnesota Co-operative Fisheries and Wildlife Research Unit managed the transfer of grant monies. Housing and various equipment were generously provided by the U.S. Fish and Wildlife Service at Waubay National Wildlife Refuge. T. Wickstrom helped locate potential study sites. N. Bien, D. Fisher and P. Wold allowed access to their wetland sites. J. R. Tester provided research advice. S. Weisberg provided statistics advice. R. J. Mayer assisted with field work, data entry and editing. T. Canfield, D. Niyogi, C. Umbanhowar, and two anonymous reviewers made many useful comments on earlier drafts of this manuscript. We thank R. Nelson for his support in developing this research.
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