Effects of short-term sediment nutrient enrichment and grazer (Neritina reclivata) removal on sediment microalgae in a shallow eutrophic estuary (Alabama, USA)
Just Cebrian1*,2*, Adrienne L. Stutes1,2,5*, Scott Phipps3*, Jason P. Stutes1,2,5, Bart Christiaen1,2 & Jonathan R. Pennock4*
The olive snail (
Neritina reclivata) is ubiquitous in tropical and sub-tropical systems of the Gulf of Mexico, however its impacts on sediment microalgae have been little studied. Many coastal systems around the world are being eutrophied due to human activities, and seemingly they will continue to be eutrophied to a further extent in the future. Exploring the single and combined impacts of further nutrient enrichment and grazing by the olive snail on sediment microalgae in such eutrophic systems is an important question for our understanding and management of these ]]>
N. reclivata on sediment microalgal biomass and composition in a shallow eutrophic estuary (Weeks Bay, Alabama, USA) of the Northern Gulf of Mexico. For this, we performed a series of factorial experiments adding or not nutrients and removing or not the snail, for a total of four treatments in each experiment: ambient grazing, ambient nutrients; ambient grazing, increased nutrients; no grazing, ambient nutrients; and no grazing, increased nutrients. We did not find any significant impact of nutrient addition ]]>
N. reclivata is not a major control of sediment microalgal populations in the subtidal sedimentary areas studied. Our findings contrast with the results of past work in sediments with well-lit and nutrient poor conditions, or sediments with high densities of other snail grazers. In conjunction this and other investigations indicate that the response of sediment microalgae to nutrient enrichment and modified grazer abundance depends to a large extent on the initial levels of nutrient availability and grazing before the system is altered. ]]>
Key words: sediment microalgae, eutrophication, Meridian reclivata, chlorophylla, herbivory, bottom-up, top-down.
Resumen
El caracol Neritina reclivata está presente en los sistemas tropicales y subtropicales del Golfo de México, sin embargo, su impacto en los sedimentos de microalgas ha sido poco estudiado. Muchos de los sistemas costeros de todo el mundo están siendo eutrofizados debido a actividades humanas, y ]]>
N. reclivata no ejerce mayor control sobre las poblaciones de microalgas en las áreas submareales y sedimentarias estudiadas. Nuestros hallazgos contrastan con resultados de trabajos anteriores en sedimentos con buena iluminación y pobres condiciones nutritivas, o ]]>
Sediment microalgae have important roles in shallow coastal systems. They often account for a significant fraction of the system’s total primary productivity, reaching up to 25% of the productivity by phytoplankton and macrophytes (Moncreiff et al. 1992, Schreiber & Pennock 1995). They also represent food resources for many herbivorous and detritivorous organisms.
Consumers of sediment microalgae range from microbes to invertebrate to vertebrate organisms, ]]>
et al. 2000, Carman & Fry 2002). The mucilage that sediment microalgae excrete, besides being a food item for detritivores, helps stabilize the sediment and reduces coastal erosion (Miller et al. 1996, Cahoon 1999, Wolfstein & Stal 2002). Sediment microalgae are also key intermediaries in the cycling of organic and inorganic nutrients in shallow coastal systems, modulating nutrient fluxes between the bottom and overlying water-column (Sundbäck
et al. 1991, Rizzo et al. 1992).
Some gastropod species are ubiquitous consumers of sediment microalgae. They ingest sediment and obtain most of their nutritional requirements from inhabiting microalgae (Fenchel & Kofoed 1976, Levinton & Bianchi 1981). However, experiments with ]]>
et al. (2000) reported considerable consumption of sediment diatoms by Hydrobia ulvae, with individual consumption rates averaging 22ng chlorophyll-a (Chla) per snail per hour for a snail density of three individuals per square cm, in laboratory experiments with samples collected from Aiguillon Bay ]]>
Ilyanassa obsoleta could reduce by up to 50% the concentration of Chla in the sediment during field experiments done in estuaries of Waquoit Bay (Massachussets, USA). In contrast, Bennet et al. (1999) found almost no noticeable effect of Littoraria irrorata on sediment microalgal biomass in laboratory microcosm experiments done with sediments from Pass ]]>
Hydrobia sp. and Potamopyrgus jenkinsi, were predominant) had no significant impact on sediment Chla concentration.
Here we study the ]]>
Neritina reclivata) (Say), a species of gastropod that is ubiquitous in shallow coastal systems of the Gulf of Mexico such as marshes, lagoons and estuaries (Russell 1941). In particular we focused on the shallow estuary of Weeks Bay (Alabama). This gastropod is abundant in the oligohaline reaches of the estuary and the only potentially important epifaunal macroinvertebrate grazer on sediment ]]>
et al. 1996). Studies on the life history, habitat selectivity and feeding behavior of the gastropod are scarce. The few existing reports indicate that N. reclivata resides preferentially in subtidal and intertidal vegetated stands (i.e. seagrass beds and marshes), and hard substrates such as stumps and rocks (Lehman & Hamilton 1980, Sheridan & Livingston 1983). The reports also indicate that these gastropods feed effectively on epiphytic microalgae that grow attached ]]>
N. reclivata on the microalgae that live in the bare sediment adjacent to vegetated fringing habitats such as seagrass beds and marshes. Confirming this hypothesis is important to understand the ecological functions of this ubiquitous gastropod in shallow coastal systems of the Gulf of Mexico. ]]>
Along with grazing, nutrient availability may be an important factor for sediment microalgae. Under low ambient nutrient availability and favorable conditions of light, salinity and temperature, enhanced nutrient availability may lead to increased sediment microalgal biomass (e.g. Darley et al. 1981 Wulff et al. 2000, Cebrian et al. ]]>
et al. 2006, Orth et al. 2006). Increased nutrient delivery into coastal waters often results in higher biomass of phytoplankton in the water-column, which reduces the quantity of light that reaches sediment microalgae (Stutes
et al. 2007, Anton et al. 2011). Thus, due to high nutrient and low light ambient levels, the response of sediment microalgae to further nutrient enrichment in already-eutrophic coastal systems should be severely dampened in relation to pristine coastal systems.
That hypothesis has been confirmed ]]>
et al. 2009), and it also seems to be the case at the relatively deeper reaches (>0.5m) of the Weeks Bay estuary. Weeks Bay receives high nutrient loads from farms and crop fields through groundwater and discharge from the Fish and Magnolia Rivers (Pennock et al. 2001, Lehrter 2006). Indeed, Stutes et al. (2006) found almost no impact of fertilization on the productivity of sediment ]]>
et al. 2006). It remains to be seen if the response of sediment microalgae to further nutrient enrichment is also much reduced in the shallower reaches (<0.5m) of this eutrophic estuary, where higher light availability ]]>
In this paper, we examine whether there are any significant impacts by N. reclivata (i.e. top-down control) on the biomass of microalgae that grow in bare sediment ]]>
N. reclivata on the structure of the sediment diatom community. The results contribute to assessing how
N. reclivata and ephemeral nutrient pulses (i.e. short-term nutrient enrichment) affect sediment microalgae in eutrophic estuaries of the North Central Gulf of Mexico.
Materials and Methods
Study locations: The experiments were carried out at two locations in Weeks Bay, Alabama. The first location (hereafter referred to as Magnolia) is on the Southeastern shoreline near the mouth of Magnolia River (one of the two rivers discharging into Weeks Bay), and the second location (referred to as Reserve) is on the Northwestern shoreline within a little embayment near the mouth of Fish River. The locations are shallow, with water depth ranging 0.1-0.6m in both locations during our experiments. The mean tidal range in the Bay is 0.4m (Schroeder et al. 1990). Water flow ]]>
et al. 2001). The intertidal region is dominated by cordgrass (Spartina alterniflora Loisel) and black needlerush (Juncus roemerianus Scheele) in the two locations. There is no submerged aquatic vegetation present in the study locations. The subtidal sediment at Magnolia is mainly composed of sand, whereas at Reserve the sediment is dominated by highly-organic, unconsolidated mud. Sediment diatoms, such ]]>
Achnanthes sp., Amphora sp., Navicula sp. and Nitzschia sp., are abundant in both locations (Miller-Way et al. 1996). Further description and a map of the study area are available in Stutes et al. (2006).
]]>
Experimental design: Experiments were carried out seasonally from October 2002 to July 2003 at the two locations. In each season 20 plots were set up at each location. The plots were set up on subtidal sediment adjacent to the shoreline. Ten of the plots were rectangular (37x22x25cm) transparent acrylic cages. The cages had mesh-covered (500μm) windows on the sides (one window per side for a total of four windows per cage) to allow water exchange while preventing access by N. reclivata. ]]>
At each site, the area where the plots were set up appears homogeneous (i.e. area adjacent to fringing salt-marsh and completely covered with bare sediment, and similar ]]>
N. reclivata; (three) enhanced nutrient availability and grazing by N. reclivata and (four) enhanced nutrient availability and no grazing by N. reclivata, with each treatment having five replicates. Once during each of the experiments we counted N. ]]>
densities within a 25x25cm2 quadrat tossed ten times haphazardly around the experimental plots. The mean values of these counts should correspond well with the average density of snails found in the non-caged plots (grazing controls) during the experiments.
Sediment nutrient enrichment: Our ]]>
N. reclivata and nutrient enrichment on sediment microalgae. To do that, we directly fertilized the sediment one time at the beginning of the experiment and surveyed the plots for four days, in accordance with other studies of short-term impacts (Downing et al. 1999). We directly spiked the fertilizer into the sediment because we sought to maximize the chances for inhabiting microalgae to take up and respond to the added nutrients. Other studies ]]>
et al. 2006, Anton et al. 2011).
Prior to starting our experiments in fall 2002, we measured ambient ]]>
et al. 2000) and, based on human-induced ]]>
et al. 2011), it represents a realistic increase that could result in Weeks Bay from further human occupation. Then, based on the average ambient porewater P concentrations measured at the study locations, we calculated the level of P addition per plot needed to reach a 17:1 N:P molar ratio in fertilized plots, which corresponds to the internal ratio for sediment microalgae (Hillebrand & Sommer 1999). The calculated addition levels were 0.21g N and 0.03g P per plot in ]]>
Those nutrient quantities were applied on day zero of the Fall 2002 experiments as a quick-release form of solid commercial-grade ammonium-nitrate (17% ammoniacal nitrogen, 17% nitrate nitrogen, Royster-Clark Inc., Norfolk, VA) and super phosphate (46% P2O5, Agribusiness Inc., Covington, LA). Nutrients were weighed and placed in ]]>
Examination of the porewater nutrient concentrations for the Fall 2002 experiments revealed the concentrations tended to remain higher in fertilized than in non-fertilized plots through day one of the experiment, but those differences tended to fade somewhat on day three (Fig. 1,
Table 1). Therefore, in an effort to ensure elevated nutrient availability throughout the duration of the experiment in fertilized plots in relation to ambient conditions, we increased the levels of nutrient addition by three-fold in the other experiments. The new addition levels for the February 2003, May 2003 and July 2003 experiments were 0.63g N and 0.09g P per plot in Magnolia, and 0.9g N and 0.12g P per plot in Reserve. We measured porewater nutrient concentrations on days zero (before burying the packets) and three in all plots for each of these other experiments ]]>
Table 1). Indeed, whereas we only found significantly higher sediment pore water nutrient concentrations in fertilized than in non-fertilized plots on day three in two out of six possible instances (i.e. nitrate+nitrite, ammonium and phosphate at Magnolia and ]]>
Table 1).
These results indicate that overall we maintained elevated nutrient availability in fertilized in relation to non-fertilized plots throughout the four days the experiment lasted, at least for one of ]]>
Porewater nutrient analysis: Porewater nutrient samples were collected using a 60mL syringe attached to an eight cm-long piece of punctured rigid aquarium tubing (Stutes et al. 2006). In an effort to sample the porewater from the ]]>
]]>
Sediment microalgal biomass: We used chlorophyll a content as a proxy for microalgal biomass (de Jonge & Colijn 1994, Schreiber & Pennock 1995, Cebrian et al. 2008). We took sediment cores using a 2.5cm diameter coring tube. The top 1cm of sediment was transferred to a 50mL centrifuge tube and placed on ice for transportation to the laboratory. Samples were stored at -80oC ]]>
et al. (1984). In all experiments three chlorophyll a samples were taken per plot on days zero, one and three, and the three samples averaged as a single replicate. Sampled sediment areas were marked and avoided in subsequent visits.
Sediment diatom community structure: On days zero and three of the July 2003 experiments, we took one extra sediment core in each of three randomly-selected fertilized pairs of plots. The cores were extracted with the same type of tube used for the chlorophyll a samples and the top 0.5cm of sediment transferred to a 20mL glass vial. The samples were covered with Lugol’s solution, fixed with 4% buffered formalin, placed on ice, brought back to the laboratory and stored in the refrigerator. During processing, the samples were digested with ]]>
Samples were then ]]>
et al. 2003).
Potential side effects of the cages: Enclosure devices, such as the cages used here, may have a series of unwanted (i.e. spurious) impacts that may mask the effect of the factors researchers intend to test for. We examined three potential spurious impacts of the ]]>
We measured chlorine dissolution rates to estimate the reduction of ]]>
Additional sediment cores were ]]>
Hydrographic conditions: Water temperature, salinity and dissolved oxygen were measured with YSI Model 85 meter (Yellow Springs Instrument Co., Yellow Springs, OH, USA) on each sampling day just beneath the water surface and just above the sediment nearby the experimental plots. Water column nutrient (nitrate, nitrite, ammonium and phosphate) and chlorophyll-
a concentrations were measured at the beginning and end of each experiment. Samples were taken at mid watercolumn nearby the experimental area, stored on ice and brought back to the laboratory for analysis. Samples were filtered through 0.45μm glass fiber filters, the filtrate collected in duplicate Nalgene bottles, and filters and bottles stored at -80oC until processing.Chlorophyll-a concentration was measured according to the fluorometric method of Parsons et al. (1984). Water column nutrient concentrations were analyzed according to standard colorimetric methods ]]>
et al. 2006) and are reported in table 2 of that study.
With statistical analysis we found substantial variability in initial sediment chlorophyll-a content among ]]>
N. reclivata, we calculated the ratio of chlorophyll-a content on day one or three to chlorophyll-a ]]>
N. reclivata with a two-way ANOVA on the ratio values for each sampling time (day one or three) and experiment, for a total of 16 ANOVA’s (two days per experiment x eight experiments). We used t-tests to compare chlorine dissolution rates and the total abundance of major groups of infaunal macroinvertebrates ]]>
Changes in sediment diatom community structure over the course of the experiment were analyzed with the PRIMER statistical package (Clarke & Warwick 2001). We built the dissimilarity matrix using the Bray-Curtis index after ]]>
N. reclivata.
Results
Hydrographic conditions: Water-column temperature and salinity showed clear seasonal ]]>
Table 2, Stutes et al. 2006). Dissolved oxygen concentrations in the water column were elevated (generally >7mg/L), tending to be highest during the winter experiments. Water-column chlorophyll-a and nutrient concentrations featured values typical of estuaries in the Northern Gulf of Mexico (Bianchi et al. 1999).
Sediment chlorophyll-a content: In relation to the values found before applying our treatments, sediment chlorophyll-a content did not vary largely as the experiment progressed. Indeed, most of the ratios of contents on days one or three to the content on day zero were close to one (
Fig. 2). Interestingly, we found almost no significant impacts of nutrient enrichment and grazing by N. reclivata on that ratio. All the ANOVA’s displayed non-significant F values for the main effects and interaction of fertilization and grazing (p>0.05), except for a significant main effect of N. reclivata grazing on day three of the Fall 2002 experiment at Reserve where lower ratios were found in grazed plots in comparison with ungrazed plots (p<0.05).
Mean (±SE) values of sediment chlorophyll-a content were (in mg/m2): October 2002 experiment at Magnolia (all treatments and all days pooled together): 452.7±12.9; October 2002 experiment at Reserve: 36.98±1.14; February 2003 experiment at Magnolia: 295.17±6.56; February 2003 experiment at Reserve: ]]>
Sediment diatom community structure:Achnanthes, Amphora, Navicula and Nitzschia ]]>
Tables 2 and 3). Other common genera in both locations were Cocconeis, Cyclotella, Desikaneis, Fallacia, Fragilaria, Martyana, Opephora and Paralia.
As it can be inferred from tables 2 and 3, large differences in sediment diatom community structure were found among the three replicate plots, both for the grazed and ungrazed treatments, in the two study locations before starting the July 2003 experiment (i.e., samples taken on day zero; Fig. 3). The direction of ]]>
Fig. 3; ANOSIM, one-way comparison between grazed plots at day zero, ungrazed plots at day zero, grazed plots at day three, and ungrazed plots at day three, p=0.60 for ]]>
Chlorine dissolution rates: Chlorine dissolution rates varied substantially among experiments and, in general, the location at Magnolia displayed higher dissolution rates than the location at Reserve (Fig. 4). ]]>
Infaunal macroinvertebrate abundance: The total abundance of infaunal ]]>
Table 4). We only found significant differences between open and caged plots in the Fall 2002 experiment at Magnolia (t-test comparing mean abundance between open and caged plots, p<0.05) out of the seven experiments for which infaunal data were available (Table 4). ]]>
Discussion
With our fertilization procedure we made an effort to achieve realistic (i.e. within the range of fertilization values applied elsewhere and plausible in our study site following further human development of the watershed, Worm
et al. 2000, Anton et al. 2011) and stochiometrically-balanced (i.e. having a 17:1 N to P atomic ratio, which is the internal ratio of benthic microalgae at optimal growth, Hillebrand & Sommer 1999) nutrient enrichment. We also applied enough nutrients to ensure persistent high concentrations (at least for nitrate+nitrite) through the duration of the experiments (i.e. four days). Yet, we found no significant effects of nutrient enrichment on sediment chlorophyll-a content in any of the eight ]]>
Past experiments have shown that nutrient enrichment leads to higher benthic microalgal chlorophyll-a content in some instances ]]>
et al. 2009), but not in others (Hillebrand & Kahlert 2002, Stutes et al. 2006, Cebrian et al. 2009). Potential reasons as to why nutrient addition may not result in increased sediment chlorophyll-a content include severe light limitation of photosynthesis (Barranguet et al. 1998, Meyercordt & ]]>
et al. 2006), and loss due to horizontal advection and/or grazing (Blanchard et al. 2001, Cebrian 2004). Weeks Bay is a eutrophic estuary with poor light availability and high porewater nutrient concentrations in the deeper (>0.5m) reaches of the estuary (Schreiber & Pennock 1995, Pennock et al. ]]>
et al. (2006) carried out a number of fertilization experiments in areas nearby our study locations, but which were slightly deeper (>0.5m), and found no impact on the productivity of sediment microalgae. They attributed this to the limiting-light levels and saturating-nutrient levels for microalgal growth measured in the two areas. The locations studied here were adjacent to fringing marshes and shallower (most often <0.5m) than the areas examined by Stutes et al. (2006). We did not measure light ]]>
et al. (2006) bottom light irradiance in our study locations most likely exceeded 500µmol/m2.s photons during our experiments. These estimates appear to lie well over the range of published values of saturating light irradiance for benthic microalgal growth (i.e. 300 to ]]>
2.s photons; Pinckney & Zingmark 1991, 1993, Blanchard & Montagna 1992, Blanchard & Gall 1994, Wolfstein & Hartig 1998). This suggests bottom irradiance was not limiting for sediment microalgae in our study locations and probably not a reason why we did not find any fertilization impacts on their biomass.
The ambient sediment porewater ]]>
4+NO3+NO2) ranged 16.0-602.1μM (median=51.6μM) and concentrations of phos-phate ranged 0.1-8.3μM (median=1.1μM) in the sediment porewater of non-fertilized plots on day zero. In Reserve, those concentrations ranged 3.00-393.1μM (median=57.2μM) for dissolved inorganic nitrogen ]]>
et al. 2000). Perhaps more importantly, relationships between nutrient availability and growth of benthic microalgae developed in the laboratory (Smayda 1997) suggest that the ambient sediment porewater nutrient concentrations in our study locations, with perhaps the exception of phosphate concentrations at Reserve, are saturating, or near-saturating at a minimum, for sediment ]]>
et al. 1999, Wulff et al. 2000, Cebrian et al. 2009), but ]]>
et al. 2000, Hillebrand & Sommer 2000b, Cloern 2001).
Resuspension and ]]>
et al. 2001). The locations studied are shallow (<0.6m), and the sediment and inhabiting microalgae are often stirred up. Thus frequent resuspension and subsequent re-deposition could mask a significant effect of nutrient addition. Whatever the reason may be, here we report that short-term nutrient addition in shallow sediments adjacent to fringing marsh in Weeks Bay does not have a noticeable impact on the biomass of ]]>
We found little evidence for a significant role of grazing by N. reclivata on the biomass of ]]>
a content in open plots in comparison with caged plots on day three of the Fall 2002 experiment at Reserve. In addition, we did not find any significant impacts of exposure to the snail on the composition of the sediment diatom community in the two experiments where we tested for those effects (experiments at Reserve and Magnolia in July ]]>
N. reclivata. Other than preventing access by the snail, our exclosures did not appear to have any major undesired (i.e. spurious) direct or indirect effects over the four days that the experiments lasted. Light interception by the exclosure was minimal (i.e., five % of incident light), chlorine dissolution rates (a proxy for flow rates and potential sediment ]]>
Research done with other species of gastropod grazers has shown variable impacts that may range from negligible to large fractions of benthic microalgal biomass consumed (Pace et ]]>
1979, Branch & Branch 1980, Bennett et al. 1999, Blanchard et al. 2000). The low densities of N. reclivata recorded in our study locations (i.e. bare sediment adjacent to fringing marshes) in the fall, spring and summer experiments (mean±SE for the ten quadrats ranging from 0±0 to 8.0±3.6 snails/m among the six experiments) may explain the almost complete lack of significant impacts by the snail in these experiments. We recorded higher densities in the winter ]]>
N. reclivata on microalgae inhabiting bare sediment adjacent to vegetated stands due to low abundance of the snail in those habitats and inefficient grazing on the microalgae.
Overall our results ]]>
et al. 2006). Persistent nutrient delivery, however, could likely affect sediment microalgal standing stocks through mechanisms such as changes in the identity of dominant species (Hillebrand et al. 2000, Hillebrand & Sommer 2000b), and/or increased shading due to the buildup of phytoplankton and filamentous macroalgae (Cloern 2001, Hauxwell et al. 2001). Similarly, our results suggest the snail
N. reclivata is not a major control of sediment microalgal populations in the subtidal sedimentary areas studied. Perhaps longer experiments in winter would have revealed significant effects, but it seems that overall the impact by the snail is modest at best in those areas.
Clearly the impacts of short-term ]]>
Acknowledgments
We thank M.J. Sullivan for ]]>
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*Correspondencia: Just Cebrian: Dauphin Island Sea Lab, 101 Bienville Blvd., Dauphin Island, AL 36528; jcebrian@disl.org. Weeks Bay National Estuarine Research Reserve, 11300 U.S. Highway 98, Fairhope, AL 36532. Adrienne L. Stutes: Dauphin Island Sea Lab, 101 Bienville Blvd., Dauphin Island, AL 36528. Department of Marine Sciences, University of South Alabama, LSCB 25, Mobile, AL 36688. Present address: Pentec Environmental/Hart Crowser, Inc. 120 Third Ave, So. Edmonds, WA 98020; adrienne.stutes@hartcrowser.com Scott Phipps: Weeks Bay National Estuarine Research Reserve, 11300 U.S. Highway 98, Fairhope, AL 36532; scott.phipps@dcnr.alabama.gov Jason P. Stutes: Dauphin Island Sea Lab, 101 Bienville Blvd., Dauphin Island, AL 36528. Department of Marine Sciences, University of South Alabama, LSCB 25, Mobile, AL 36688. Present address: Pentec Environmental/Hart Crowser, Inc. 120 Third Ave, So. Edmonds, WA 98020; jason.stutes@hartcrowser.com Bart Christiaen: Dauphin Island Sea Lab, 101 Bienville Blvd., Dauphin Island, AL 36528; bchristiaen@disl.org. Department of Marine Sciences, University of South Alabama, LSCB 25, Mobile, AL 36688. Jonathan R. Pennock: University of New Hampshire, 24 Colovos Road, Durham, NH 03824-3505; jonathan.pennock@unh.edu 1. Dauphin Island Sea Lab, 101 Bienville Blvd., Dauphin Island, AL 36528; jcebrian@disl.org, bchristiaen@disl.org 2. Department of Marine Sciences, University of South Alabama, LSCB 25, Mobile, AL 36688. 3. Weeks Bay National Estuarine Research Reserve, 11300 U.S. Highway 98, Fairhope, AL 36532; scott.phipps@dcnr.alabama.gov 4. University of New Hampshire, 24 Colovos Road, Durham, NH 03824-3505; jonathan.pennock@unh.edu 5. Present address: Pentec Environmental/Hart Crowser, Inc. 120 Third Ave, So. Edmonds, WA 98020; adrienne.stutes@hartcrowser.com, jason.stutes@hartcrowser.com ]]>
Received 13-X-2011. Corrected 23-III-2012. Accepted 23-IV-2012. ]]>201121991-10091998173117-12619992421-2019991992287-1419941821-142000255247-260200126485-10019815125-128198046106-114200224085-9219993747-8620012004153-185200842391-40420093729-212001210223-253198117122-1281994104185-1961999.801157-1167197627367-3761968411-13.197615411-431200346562-5722001821007-10222006326145-156.199716035-46199944440-4462000426185-192200067221-236200020427-38200272143-1591980467-722006782356-23682005294117-129198139531-54520063121806-180919881999178179-1912000451224-1234199619202-2121996199287-171200656987-99619799121-13419961984200119917681-891993381373-138319928651-61194188347-40319836407-419199542335-3521990481-4931997421137-115319721671-310200631229-43200734855-70199174263-279199816663-71200223613-22200085359-3752000451144-1152