Delivery of nutrients and seston from the Muskegon River Watershed to near shore Lake Michigan

Journal of Great Lakes Research 39 (2013) 672–681

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Delivery of nutrients and seston from the Muskegon River Watershed to near shore Lake Michigan Katharine M. Marko a,⁎, Edward S. Rutherford b,c, Brian J. Eadie c, Thomas H. Johengen d, Margaret B. Lansing c a

School of Natural Resources and the Environment, University of Michigan, Ann Arbor, MI 48109, USA Institute for Fisheries Research, School of Natural Resources and the Environment, University of Michigan, Ann Arbor, MI 48109, USA NOAA-Great Lakes Environmental Research Laboratory, Ann Arbor, MI 48109, USA d Cooperative Institute for Limnology and Ecosystem Research, University of Michigan, Ann Arbor, MI 48109, USA b c

a r t i c l e

i n f o

Article history: Received 15 October 2012 Accepted 13 July 2013 Available online 3 October 2013 Communicated by Lars Rudstam Keywords: Stable isotopes Muskegon River Lake Michigan Seston Near shore Nutrients

a b s t r a c t Drowned river mouth lakes are major features of coastal Great Lakes habitats and may influence nutrient and organic matter contributions from watersheds to near shore coastal zones. In May through October 2003, we measured loads of nutrients, surficial sediment, and seston to track the delivery of riverine-derived materials from the lower Muskegon River Watershed (MRW) into the near shore area of southeast Lake Michigan. Nutrient flux data indicated that seasonal loads of 1800 metric tons (MT) of particulate organic carbon, 3400 MT of dissolved organic carbon, and 24 MT of total phosphorus were discharged from the lower Muskegon River, with approximately 33% of TP load and 53% of the POC load intercepted within the drowned river mouth terminus, Muskegon Lake. Carbon: phosphorus molar ratios of seston in Muskegon River (C:P = 187) and Muskegon Lake (C:P = 176) were lower than in Lake Michigan (C:P = 334), indicating phosphorus limitation of phytoplankton in near shore Lake Michigan. Isotopic signatures of seston collected in Muskegon Lake were depleted in δ13C (−30.8 ± 1.6‰) relative to the isotope signatures of seston from Lake Michigan (−26.2 ± 1.3‰) or the mouth of the Muskegon River (−28.1 ± 0.5‰), likely due to the presence of biogenic methane in Muskegon Lake. Seston δ15N increased on a strong east-to-west gradient within Muskegon Lake, indicating significant microbial processing of nutrients. The extent of nutrient uptake in Muskegon Lake altered the chemical and isotopic characterization of seston flowing into Lake Michigan from Muskegon River. Published by Elsevier B.V. on behalf of International Association for Great Lakes Research.

Introduction Drowned river mouth lakes and wetlands are major coastal features of the Great Lakes coastal zone and receive nutrients and organic matter from upstream watersheds and the Great Lakes themselves (Larson et al., 2012). These types of wetlands are considered “freshwater estuaries” because they are characterized by high amounts of organic matter from deposition of watershed materials and due to protection from coastal processes including waves and currents (Albert et al., 2005) while still exchanging water with coastal waters of the Great Lakes. However, these unique coastal habitats and the processes that occur within them have received relatively little attention in the scientific literature (Bhagat and Reutz, 2011). In Lake Michigan and other Great lakes, dramatic changes have occurred in nutrient cycling and phytoplankton biomass as a result of the phosphorus abatement program and the establishment of the

⁎ Corresponding author at: US EPA-Western Ecology Division, Pacific Coastal Ecology Branch, Newport, OR 97365, USA. Tel.: +1 541 867 5083. E-mail addresses: [email protected] (K.M. Marko), [email protected] (E.S. Rutherford), [email protected] (B.J. Eadie), [email protected] (T.H. Johengen), [email protected] (M.B. Lansing).

invasive dreissenid mussels (quagga mussel Dreissena rostriformis bugensis; zebra mussel Dreissena polymorpha) (Fahnenstiel et al., 2010; Kerfoot et al., 2010; Mida et al., 2010). Phytoplankton community composition has changed and biomass has declined in Lake Huron and southern Lake Michigan since 2004, such that the primary productivity in these areas is now similar to the oligotrophic Lake Superior (Evans et al., 2011). A proposed mechanism for this reduction in phytoplankton biomass is a “nearshore shunt,” by which phosphorus is retained in nearshore environments as a result of dreissenid bioactivity and biomass, thereby blocking transport of this material to the offshore region (Hecky et al., 2004). Thus, there is an increased need to understand fate and retention of watershed-derived nutrients and organic matter in nearshore habitats and their eventual influence on offshore processes (Evans et al., 2011; Hiriart-Baer et al., 2008). Understanding the linkages between watersheds and the Great Lakes requires estimation of source, load and fate of organic materials and nutrients within these watersheds to adequately understand the impact of these systems on the near shore zones of the Great Lakes (Larson et al., 2012; Makarewicz et al., 2012). Coastal embayments and river-mouths are critical areas in the Great Lakes where the Lakes are connected to terrestrial habitats (Chen and Driscoll, 2009; Larson et al., 2012). The delivery of terrestrial materials from watersheds into

0380-1330/$ – see front matter. Published by Elsevier B.V. on behalf of International Association for Great Lakes Research. http://dx.doi.org/10.1016/j.jglr.2013.08.002

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shallow, wide connecting basins may be characteristic of Muskegon River and other drowned river-mouth tributaries feeding Lake Michigan, but is likely different in tributaries that feed directly into Lake Michigan or other Great Lakes basins. For example, the Grand River (MI) is characterized by a different geomorphology than the Muskegon River, and culminates in a river delta rather than a drowned river-mouth lake. One might expect to find higher terrestrial influences in Great Lakes areas such as Saginaw Bay, Green Bay or western Lake Erie where discharge from tributaries is high relative to the volume and depth of their receiving coastal waters. Arend (2008) found that morphology of Lake Ontario embayments and the degree of watershed inputs and connectivity to Lake Ontario influenced the extent to which terrestrial carbon subsidies were incorporated into the food web. One of the most commonly used tools for identifying sources of organic matter within aquatic systems and tracking the processing of such materials is stable isotope analysis (SIA) (McCusker et al., 1999; Peterson and Fry, 1987; Peterson et al., 2007). Aquatic systems can be supported by a mix of internally-derived (autochthonous) and externally-derived (allochthonous) materials (Wetzel, 2001). SIA has shown that food webs in freshwater lakes can be supported by allochthonous materials (eg., Cole et al., 2011; Vander Zanden et al., 2005). SIA also has been extremely useful in identifying alternative energy sources such as methane, which is highly depleted in δ13C and generated from both surficially hypoxic and anoxic environments in freshwater lakes (Bastviken et al., 2003, 2008; Kiyashko et al., 2004). Given these advancements in the state of the science, SIA has now become a critical tool for elucidating origin and transfer of energy within aquatic food webs (Fry, 1999; Hoffman et al., 2012). In this study, we sought to quantify the amount of terrestrial-derived materials from the Muskegon River Watershed (MRW) that was delivered to near shore Lake Michigan, and the fraction intercepted within the drowned river mouth Muskegon Lake during the spring, summer and fall of 2003. Our specific objectives were: (1) to quantify seasonal loads of total phosphorous (TP), particulate organic carbon (POC), and dissolved organic carbon (DOC) from the MRW into Muskegon Lake and near shore Lake Michigan; and (2) to use sediment grain size and stable isotope ratios to characterize the origin of the seston and surficial sediments within the lower MRW, Muskegon Lake, and the near shore zone of Lake Michigan. These calculations permitted estimation of amounts of nutrients and organic matter coming from the Muskegon River that were intercepted by the drowned river mouth Muskegon Lake. Materials and methods Site description The MRW (Fig. 1) has the second largest catchment in Michigan with an area of 7302 km2, and runs southwest from Higgins Lake in central Michigan for 370 km before terminating in Muskegon Lake, a drowned river-mouth lake on Lake Michigan's eastern shore. The mean annual discharge of the Muskegon River measured at a USGS stream gage placed at the Croton Dam was 56.5 m3/s from 2000 to 2006. The watershed predominately consists of forested (53.2%) and agricultural lands (23.0%), and urban land cover (4.2%). The MRW is predicted to become significantly more urbanized, with the proportion of urbanized land potentially increasing to 11.5% by the year 2040 (Tang et al., 2005). Our study focused on the 75 km of riverine habitat below Croton Dam, which is characterized by high velocity flows and hard bottom substrates in the immediate 19 km below Croton dam, and lower flows, soft-bottom substrates, and a large (32 km2) wetland complex in the rest of the lower river (Ivan et al., 2010; Torbick et al., 2010). The Muskegon River terminates at Muskegon Lake, a 16.8 km2 drowned river-mouth lake connected to Lake Michigan via a narrow shipping channel. Muskegon Lake serves as an important nursery habitat for some of the region's most important fisheries (Höök et al., 2008).

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Muskegon Lake has a mean depth of 7.1 m, a maximum depth of 21 m, and an estimated volume of 119 million m3 given a low water datum mark of 173.35 m above sea level for Lake Michigan (Evans, 1992). The mean hydraulic residence time in Muskegon Lake is 23 days (Carter et al., 2006). However, residence time can vary seasonally over a range of fourteen to seventy days, depending on discharge from Muskegon River. Muskegon Lake has been heavily impacted by industrial and human waste since settlement, prompting the U.S. Environmental Protection Agency to list it as an area of concern (AOC) in 1985 (EPA, 2009). Dissolved oxygen concentrations as low as 2 mg/L have been recorded in the bottom waters of Muskegon Lake during a monitoring period from 2002 through 2007 (Bopiah Biddanda, Annis Water Resources Institute, personal communication). Since 2003, a concerted effort has taken place involving the Michigan Department of Environmental Quality (MDEQ), regional scientists, and local stakeholders to establish targets and monitor remediation efforts in Muskegon Lake (Steinman et al., 2008). Lake Michigan is the third largest of the Laurentian Great Lakes, with a surface area of 57,800 km2, a total volume of 4920 km3, and a hydraulic residence time of 62 years (Eadie, 1997). The lake is divided into a northern and southern basin. Lake Michigan is oligotrophic, though productivity in the southern basin is higher than in the northern basin due to differences in geology and nutrient supply from the respective drainage basins (Mackin et al., 1980; Meyers and Eadie, 1993). Circulation in Lake Michigan is almost entirely wind-driven and consequently is extremely episodic (Kerfoot et al., 2004). Turbidity plumes have been documented along the southern coast of the lake during high wind events in late winter and spring, re-suspending sediments for up to six weeks at a time (Schwab et al., 2000). Our sampling area in near shore Lake Michigan encompassed the area from the shoreline to the 30 m depth contour, and 1 min of latitude north and south of the Muskegon channel opening (Fig. 1). Water chemistry Measurements of daily flow and temperature in Muskegon River were recorded by a USGS stream gage beneath Croton Dam. Whole water samples were collected monthly for analysis of nutrient concentrations and seston from March to October 2003 at five fixed stations (Fig. 1). Two stations were located in the Muskegon River at Pine Street boat launch near Croton Dam (Upper River) and in the North Channel at the Highway 120 Bridge (Lower River). One station was located in the middle of Muskegon Lake and another in the shipping channel connecting it to Lake Michigan. The final sampling station was in the near shore zone of Lake Michigan, 0.5 km directly west of the shipping channel. The Muskegon Lake, Lake Michigan, and Lower River stations were sampled using Niskin bottles to collect water samples from a depth of 3 m. Samples were then transferred to acid-washed 4 L polyethylene bottles. At the Upper River station, the sample was obtained by wading approximately 7 m into the river channel and collecting water directly in the polyethylene bottle. All samples were stored on ice until they could be processed within 24 h of collection. Sample processing involved filtering whole water samples to prepare the following components for measurement: dissolved organic carbon (DOC), seston, total suspended material (TSM), total dissolved phosphorus (TDP), and nitrate (NO3). Total phosphorous (TP) concentrations were obtained from un-filtered water samples. DOC samples were obtained by filtering 50 ml aliquots thru pre-combusted 25 mm diameter Whatman GF/F filters and collecting the filtrate into Kimble amber glass vials (Fisher Scientific, Chicago, IL). The vials were then frozen and sent to G.G. Hatch Isotope Laboratories (Ottawa, Ontario, Canada) for analysis of DOC concentration (mg/L) and δ13C signatures. Seston samples were obtained by filtering 300 ml of whole water through pre-combusted 25 mm diameter Whatman GF/F filters (Fisher Scientific, Chicago, IL). Seston filters were soaked with 2N HCl and dried in an oven overnight at 60 °C to acidify them. The filters were then

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Fig. 1. A map of the Muskegon River watershed, western lower peninsular Michigan, U.S.A. Water sampling stations noted with open triangles. The town of Newaygo, Michigan is represented by a black dot and Croton Dam is presented as a black line for location references.

placed in Vycor tubes which had been pre-combusted at 900 °C. Precombusted copper powder and copper oxide wire were added to these tubes which were then evacuated and flame sealed. The samples were combusted at 650 °C for 10 h. Gasses were purified by cryogenic vacuum distillation; H2O was frozen into a dry-ice 2-propanol trap (~80 °C), CO2 was frozen into a sample tube and then immersed in liquid nitrogen, and nitrogen frozen into a sample bulb containing silica gel at liquid nitrogen temperature (approximately −195 °C). Stable isotopes of carbon and nitrogen were analyzed using a VG PRISM mass spectrometer. TSM samples were obtained by filtering 500–1000 ml of water (depending on turbidity of the sample) onto pre-weighed 47 mm diameter Whatman GF/F filters (Fisher Scientific, Chicago, IL). Filters were then stored frozen until they could be dried in an 80 °C oven for 24 h and weighed to the nearest tenth of a milligram to determine the TSM concentration (mg/L). TP samples were obtained by pouring 50 ml of whole water into acid-rinsed Pyrex tubes and refrigerating the samples. TDP samples were collected by filtering a 20 ml aliquot of whole water through a 0.2 μm nylon syringe filter into an acid-rinsed Pyrex tube and refrigerating the sample. TP and TDP samples were digested in an autoclave after addition of potassium persulfate (5% final concentration) and then measured for soluble

phosphorus (Menzel and Corwin, 1965). Nitrate concentrations (NO3 + NO2) were determined by the cadmium reduction method based on an azo dye reaction. Nutrient concentrations were measured using standard automatic colorimetric procedures on an Auto Analyzer II (Davis and Simmons, 1979). We estimated seasonal loads of POC, DOC and TP from Muskegon River to Muskegon Lake, and from Muskegon Lake to Lake Michigan to determine the amount of material retained in Muskegon Lake. We estimated nutrient loads (MT) in each month from March to October at sites upstream and downstream of Muskegon Lake by multiplying cumulative monthly discharge estimates at those sites by the sitespecific nutrient concentration measured in that month. We assumed that the one-day measurement of nutrient concentrations in each month represented the average concentration for that month. We summed the monthly load estimates just upstream of Muskegon Lake, and assumed discharge into Muskegon Lake equaled discharge out of the lake and into Lake Michigan. We also compared our nutrient load estimates over the 235-day period from March to October to loads estimated by USGS from the Muskegon River watershed to near shore Lake Michigan during March–October in 1994 and 1995. In the USGS study, nutrient concentrations and loads were measured at the intersection

K.M. Marko et al. / Journal of Great Lakes Research 39 (2013) 672–681

of the Muskegon outflow site (Muskegon Channel) and Lake Michigan. As with our study, the nutrient loads were estimated by USGS by multiplying nutrient concentrations by cumulative monthly discharges.

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calculations were PeeDee limestone for carbon, or atmospheric nitrogen gas for nitrogen (Peterson and Fry, 1987). Statistics

Surficial sediments A ponar with a sampling area of 0.047 m2 was used to sample sediments from stations in Muskegon River, Muskegon Lake and Lake Michigan in spring and fall. In May 2003, sediments were sampled from five stations within Muskegon River and 25 stations in Muskegon Lake and Lake Michigan. Unfortunately due to a sample processing error, the samples collected in May from Muskegon Lake and Lake Michigan could not be used in this analysis. In September 2003, sediments were sampled from 38 stations in Muskegon Lake and the near shore zone of Lake Michigan. Ponar samples were carefully placed in a tub and emptied slowly to preserve the top layer of the sample. When possible, this top layer (encompassing several centimeters) was scraped from the ponar sample and placed in a plastic bag to isolate the most recently deposited materials. If the sample was too sandy to get a defined upper layer of several centimeters, than the entire sample was mixed such that a representative sample could be collected. The samples were transported to the lab on ice for further sieving and analysis of nutrients. Each sample was passed through a 500 μm screen to remove invertebrates and large debris; then transferred into pre-weighed, acetone-rinsed containers and allowed to settle in a refrigerator for 24 h, before the overlying water was siphoned off. The samples were freeze-dried and sieved once again to isolate three size fractions: fine material (b63 μm), a mid-size fraction (63–210 μm), and a large size fraction (N210 μm). All visible particles of shells were removed and the samples were ground into homogenized powder with a mortar and pestle and weighed. Carbonates were removed from sub-samples of approximately 0.2 g of sediment by adding several milliliters of 2N HCl and mixing on a shaker table overnight. The subsamples were then dried for 24 h at 60 °C and ground once again with a mortar and pestle before analysis for organic carbon and nitrogen content using a Carbo Erba elemental analyzer model 1110. Aliquots of acidified sediment were weighed into aluminum tins. Total phosphorus was determined following the combustion method of Anderson (1975). The sediments were weighed into acid-cleaned Pyrex test tubes and combusted for two hours at 450 °C. Then, 30 mL of 1N HCl were added to the samples and boiled in a water bath for 30 min. The samples were diluted up to 50 mL with deionized water and then analyzed on an Auto Analyzer II using standard colorimetric procedures. Plots of sediment grain size and isotope concentrations were created using the “geometrical interval” function in ArcMap 10 (ESRI Redlands, CA). This function splits continuous data by minimizing the sum of squares of the number of elements in each class such that the classes are proportionally filled with relatively consistent intervals between them.

All statistical analyses were run on SigmaStat Version 3.1. Differences in water chemistry concentrations (DOC, TSM, TP, TDP, POC, and NO3) and the δ13C and δ15N signatures of seston among sites were evaluated with a one-way ANOVA when the data were normally distributed and with a Kruskal–Wallis ANOVA on ranks when the data were not normally distributed (Zar, 2009). We checked if the data were normally distributed using the Kolmogorov–Smirnov test and for equal variance using Bartlett's test. Post-hoc pairwise comparisons were made with Tukey's or Dunn's tests. Differences in isotope concentration or size composition of sediments from Muskegon Lake and Lake Michigan were analyzed with t-tests or Mann–Whitney tests on ranks, depending on whether the equal variance assumption was met by the data. Results of statistical tests were tested for significance at the α = 0.05 level. Results Water chemistry The total annual discharge of the Muskegon River at Croton Dam in 2003 was compared to discharge averaged over a 6-year span of flow data from 2000 to 2002 and 2004 to 2006. In 2003, discharge was lower than the 6-year average from January to March, but higher than average in late October through November after sampling had been completed (Fig. 2). In 2003, discharge ranged from a low of 21.2 m3/s recorded on 11 September 2003 to a high of 115.2 m3/s on 5 November 2003 with a spring peak of 90.3 m3/s occurring on 21 April; the average daily mean water temperature measured at Croton Dam was 10.3 °C and ranged from 0.5 °C to 22.5 °C throughout the year. Spatial differences existed in water chemistry within the MRW, Muskegon Lake, and near shore Lake Michigan (Table 1). TSM concentrations (mg/L) varied significantly among sites (Kruskal–Wallis ANOVA; H = 26.65, df = 4, P b 0.001). TSM concentrations measured at the Lower River were significantly higher than concentrations at any of the other sites, except Muskegon Lake (Tukey test; P b 0.05). Total suspended materials (TSM) were significantly elevated by a factor of 3–5 times at the Lower River station compared to the Upper River station, showing the contribution from the lower portion of the watershed.

Stable isotope analysis Carbon and nitrogen stable isotope analyses of sediments were conducted by the Terrestrial Ecosystems Laboratory at the University of Michigan School of Natural Resources and Environment. The samples were converted to CO2 or N2 gas and analyzed for percentage of 15N and 13 C atoms on a Delta Plus isotope ratio mass spectrometer with a Conflo II interface (Thermo Finnigan, San Jose, CA). The coefficient of variation for all replicate isotope samples was approximately 0.2‰ for δ13C and 0.3‰ for δ15N. Stable isotope ratios were calculated using the following equation: δX ¼

h


 i 3 Rsample =Rstandard −1  10 ;

where X is 13C or 15N, and R is the ratio of heavy to light isotope 13C/12C or 15N/14N. The standard reference materials used to complete these

Fig. 2. Average daily discharge (m3/s) for the Muskegon River beneath Croton Dam as measured by a USGS stream gage in 2003. The solid line represents average daily flows measured in 2003; the dashed line represents daily mean water temperature. The dotted line represents average daily flows (vertical lines represent ±.2 s.e.) averaged over a period of six years from 2000 to 2002 and 2004 to 2006. The solid dots represent the dates sampled in 2003.

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throughout the sampling period at all the sample stations. Though the nitrate data for September were lost, the general declining temporal trend continued through October. However, differences in nitrate concentration were not significant among the sites (Kruskal–Wallis ANOVA; H = 3.19, df = 4, P = 0.53). Dissolved (DOC) and particulate (POC) organic carbon concentrations also exhibited explicit spatial patterns (Table 2). Differences in DOC concentrations (mg/L) were statistically significant among the sites (ANOVA; F = 6.55, df = 4, P b 0.001). DOC concentrations measured in Lake Michigan were consistently lower than at any other site; peaked in June and decreased in late summer and fall. However despite the differences in DOC concentration, the δ13C of DOC did not show significant variation among the sites (Kruskal–Wallis ANOVA; H = 6.670, df = 0.154). POC concentrations (mg/L) also varied significantly across the sites (Kruskal–Wallis ANOVA; H = 14.24, df = 4, P = 0.007) with significant differences between the Lower River and Lake Michigan (Dunn's test, P b 0.05). Seston δ13C signatures were statistically significant different across the sites (ANOVA; F = 14.079, df = 4, P b 0.001) (Fig. 3). The seston δ13C signature was significantly more enriched in Lake Michigan compared to all the other stations except the Muskegon Channel station (Tukey test, P b 0.05). Seston δ13C was more depleted at the Muskegon Lake station (−30.85 ± 1.56‰) than at the Upper River (−28.62 ± 1.1‰) and Lower River stations (−28.10 ± 0.5‰) and Lake Michigan (−26.20 ± 1.3‰) (Tukey test; P b 0.05); but not different between the Upper River and Lower River stations (Tukey test; P = 9.34). Seston δ15N values varied significantly between the sites (ANOVA; F = 7.928, df = 4, P b 0.001). Station comparisons indicated that seston δ15N from Lake Michigan (3.41 ± .0.98‰) was significantly lower than from Muskegon Lake (6.31 ± 1.21‰) (Tukey test; P b 0.050).

Table 1 Measured values for each water chemistry parameter sampled at five sites in the Muskegon River watershed and near shore Lake Michigan, sampled monthly from March to October 2003. “NDC” designations indicate that no data were collected. Sample date

Location

TSM (mg/L)

TP (μg/L)

TDP (μg/L)

NO3 (mg/L)

03/27/03

Upper River Lower River Muskegon Lake Muskegon Outflow Lake Michigan Upper River Lower River Muskegon Lake Muskegon Outflow Lake Michigan Upper River Lower River Muskegon Lake Muskegon Outflow Lake Michigan Upper River Lower River Muskegon Lake Muskegon Outflow Lake Michigan Upper River Lower River Muskegon Lake Muskegon Outflow Lake Michigan Upper River Lower River Muskegon Lake Muskegon Outflow Lake Michigan Upper River Lower River Muskegon Lake Muskegon Outflow Lake Michigan Upper River Lower River Muskegon Lake Muskegon Outflow Lake Michigan

3.4 9.7 2.9 2.0 1.2 2.9 18.5 2.1 1.7 1.7 1.5 7.3 2.4 2.0 1.5 1.4 7.8 2.2 2.1 2.4 1.4 13.1 2.5 2.3 0.9 1.1 6.1 4.6 2.6 0.9 1.8 3.2 3.1 4.2 1.3 0.8 7.5 2.6 1.4 1.3

19.3 29.5 26.3 21.7 5.8 20.3 48.0 18.3 16.8 7.0 14.0 24.8 23.0 19.6 8.3 11.1 21.8 19.8 20.4 10.9 7.5 16.0 14.1 10.0 2.6 19.9 23.6 36.0 23.2 4.9 42.9 24.4 28.5 29.6 9.4 30.3 32.2 29.7 28.0 10.5

11.6 14.8 9.7 6.2 2.0 4.6 10.7 4.8 4.8 6.4 5.3 7.6 6.5 7.6 2.0 6.1 7.3 6.8 6.0 3.1 8.4 10.4 7.2 5.8 2.1 14.5 9.7 6.0 8.5 2.0 23.3 8.7 7.3 6.4 2.7 26.3 15.9 11.0 18.1 3.2

0.8 0.9 0.8 0.7 0.4 0.7 0.7 0.7 0.7 0.5 0.6 0.6 0.5 0.5 0.4 0.5 0.6 0.4 0.4 0.4 0.3 0.4 0.2 0.2 0.3 0.2 0.4 0.1 0.1 0.3 NDC NDC NDC NDC NDC 0.2 0.3 0.2 0.2 0.2

04/21/03

05/19/03

06/11/03

07/07/03

08/26/03

09/11/03

10/11/03

Surficial sediments Size fractionation of surficial sediment samples collected in September showed that Muskegon Lake had a high proportion of fine (b 63 μm) sediment, with most of the samples consisting of more than 60% fine grain (Fig. 4A). In contrast, surface sediments in near shore Lake Michigan were primarily comprised of mid-size grains (63–210 μm), which were not prevalent in Muskegon Lake (Fig. 4B). Localized areas of coarse (N210 μm) sediment were present on shelf areas in both near shore Lake Michigan and Muskegon Lake (Fig. 4C). Stable isotope analysis of the fine-grained (b63 μm) sediment collected in September revealed extensive differences in δ13C of the surface sediments collected from Muskegon Lake and Lake Michigan. Fine sediment δ13C signatures in Muskegon Lake were significantly lighter (−29 to −30‰) than those found in near shore Lake Michigan (−23 to −26‰) (T = 174.0, n = 17, 21, P b 0.001) (Fig. 5A). Differences in δ15N signatures between fine-grained sediments from Muskegon Lake and Lake Michigan were not significantly different (t = 0.978, df = 36, P = 0.335) (Fig. 5B). However, fine-grained sediment δ15N values in Muskegon Lake clearly increased along a gradient from east to west within Muskegon Lake. The eastern end of Muskegon Lake was characterized by significantly lighter δ15N signatures (~4‰) than the western end of the lake (~6‰) (t = −6.856, df = 19, P b 0.001).

TSM concentrations in Lake Michigan averaged about half of those found in Muskegon Lake and only about 10% of those measured at the Lower River station. Total phosphorus (TP) concentrations were significantly different among the sites (Kruskal Wallis ANOVA; H = 19.31, df = 4, P b 0.001). Peak concentrations of TP occurred during summer at the Upper River, Muskegon Lake, and Muskegon Channel stations and ranged between 25 and 42 μg/L. TP concentrations in near shore Lake Michigan ranged from 17 to 53% of those in the Muskegon Lake outflow, but followed similar seasonal patterns. Total dissolved phosphorus (TDP) concentrations also varied significantly among the sites (Kruskal–Wallis ANOVA; H = 20.03, df = 4, P b 0.001). The proportion of TDP to TP averaged about 30% but varied substantially (20–90%) among sites and months. Nitrate concentrations declined

Table 2 Average station concentrations (mg/L) of dissolved organic carbon (DOC) and particulate organic carbon (POC), and stable isotope concentrations (‰) of DOC δ13C, seston δ13C, seston δ15N and total phosphorus (TP, μg/l) at sampling stations in the Muskegon River watershed and near shore Lake Michigan. The stations were: Upper River below Croton Dam (UR), Lower River at mouth of Muskegon River (LR), Muskegon Lake (ML), Muskegon Channel (MC), and near shore Lake Michigan (LM). Values were averaged (±1 s.e.) over the sampling period of March– October, 2003 at five sampling stations. Station

DOC

UR LR ML MC LM

4.33 4.10 4.14 3.83 1.94

DOC δ13C

POC ± ± ± ± ±

0.52 0.33 0.38 0.43 1.15

1.05 1.99 1.67 1.19 0.96

± ± ± ± ±

0.13 0.30 0.20 0.14 0.12

−28.9 −29.0 −28.4 −28.6 −31.7

± ± ± ± ±

0.8 0.8 0.8 0.9 1.1

Seston δ13C

Seston δ15N

TP

−28.7 −28.1 −30.9 −29.4 −26.2

5.3 4.9 6.3 6.4 3.7

20.9 27.5 24.5 21.2 7.4

± ± ± ± ±

0.4 0.2 0.6 0.5 0.5

± ± ± ± ±

0.6 0.1 0.6 0.4 0.2

± ± ± ± ±

4.0 3.4 2.5 2.5 1.1

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Fig. 3. Average C and N isotopic signatures of seston samples collected from the Muskegon River Watershed, Muskegon Lake, and Lake Michigan. Error bars represent one standard error around mean.

An analysis of organic carbon (OC), phosphorus, and C/N concentrations of surficial sediments also indicated the extent to which riverine material is deposited and processed within Muskegon Lake. Levels of organic carbon (OC) were significantly higher in the surficial sediments of Muskegon Lake (74.1 ± 2.9 mg C/g) than in Lake Michigan (20.2 ± 2.6 mg C/g) (t = −13.171, df = 35, P b 0.001). Total phosphorus concentrations of fine sediments also were significantly higher in Muskegon Lake (1.7 ± 0.1 mgP/g) than in Lake Michigan (1.4 ± 0.2 mgP/g) (Mann–Whitney T = 230.0, n = 16, 21, P = 0.024). On a mass basis, the average C/N ratio of the five bulk sediment samples collected from the Muskegon River was 21.4 ± 3.4. The C/N ratios of fine sediments were considerably higher (t = −6.325, df = 35, P b 0.001) in Muskegon Lake (C/N = 11.3 ± 2.1) than in Lake Michigan (C/N = 7.5 ± 1.3). A comparison of surficial sediment C/P molar ratios across the sites indicated that values decreased from C/P = 187 in lower Muskegon River, 176 in Muskegon Lake, to 137 in Muskegon Channel, but was highest (C/P = 334) in Lake Michigan. Molar ratios (C:N:P) of fine sediments were higher in Muskegon Lake (115:9:1) than in Lake Michigan (38:4:1).

Loads The data collected during this experiment permitted estimation of nutrient and organic matter loads delivered from March to September 2003 to Muskegon Lake and from Muskegon Lake to Lake Michigan, and hence the amount intercepted in Muskegon Lake. The amount of POC intercepted in Muskegon Lake was estimated at 950 metric tons (MT), as the difference between 1800 MT flowing into Muskegon Lake and 850 MT flowing out. The DOC load intercepted in Muskegon Lake was estimated at 100 MT, a difference between 3400 MT flowing in and 3300 MT flowing out. Finally, the amount of TP intercepted in Muskegon Lake was estimated at 8 sMT/yr, a difference between 24 MT flowing into Muskegon Lake and 16 MT flowing out. Therefore, Muskegon Lake intercepts 33% of the phosphorus and 53% of the particulate organic carbon coming from the Muskegon River (Table 3). Our estimate of seasonal POC loads to Lake Michigan were similar to those in 1994 and 1995, but phosphorus and DOC loads were much lower than in 1994 and 1995. By comparison, seasonal phosphorus loads for the Muskegon River in 1994 and 1995 were 45 and 31 MT, respectively. Seasonal DOC loads in 1994 and 1995 were 9862 and 8049 MT, respectively, and higher than in 2003. Seasonal POC loads in 1994 and 1995 were 868 and 932 MT, and similar to our estimated annual load in 2003.

Fig. 4. Maps showing percent grain size composition for samples collected in September 2003. X and Y axes represent longitude and latitude coordinates, respectively. The size of the sample points (i.e. dots) increase with increasing % composition in the respective grain size class for sampled locations in Muskegon Lake and the near shore zone of Lake Michigan adjacent to Muskegon Lake. Panel A) gives percent b 63 μm, panel B) gives 63–210 μm and panel C) percent N 210 μm.

Discussion Drowned river-mouths and coastal wetlands provide critical spawning and nursery habitat for Great Lakes fishes (Brazner et al., 2001; Hoffman et al., 2010; Höök et al., 2007), but the potential for these habitats to intercept and process terrestrial materials from feeding

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Fig. 5. Maps of the isotopic signatures of fine-grained (b63 μm) surficial sediments collected from Muskegon Lake and the near shore zone of Lake Michigan adjacent to Muskegon Lake sampled in September 2003. X and Y axes represent longitude and latitude coordinates, respectively. Panel A) δ13C signatures; panel B) δ15N signatures. The size of the sample points (i.e. dots) increases with increasing isotopic ratios.

tributaries is poorly known (Chen and Driscoll, 2009; Larson et al., 2012). The flow of nutrients and seston from watersheds through drowned river mouth lakes is critical to understanding the coastal ecology of near shore Great Lakes habitats. Our study quantified nutrient loadings, seston isotopes, and surficial sediment chemistry of one of Lake Michigan's largest watersheds, the Muskegon River, in order to determine the fate and delivery of terrestrial materials from the MRW to near shore Lake Michigan. Our results indicate that a significant portion of terrestrial material is intercepted and processed by Muskegon Lake before reaching near shore Lake Michigan. During the EPA-sponsored Lake Michigan mass balance program (1994–95), nutrients were measured near the Muskegon Channel

Table 3 Estimated loadings (metric tons ‘MT’) of particulate and dissolved organic carbon (POC, DOC) and total phosphorus (TP) into and out of Muskegon Lake, and amount intercepted over the 235 day period from 5 March to 26 October, 2003. Seasonal load estimates to Lake Michigan in 1994 and 1995 were from the US EPA Lake Michigan Mass Balance Project for the same 235-day time period.

2003 into ML 2003 into LM 2003 intercept by ML 1994 to LM 1995 to LM

POC (MT C/yr)

DOC (MT C/yr)

TP (MT P/yr)

1800 850 950 868 932

3400 3300 100 9862 8049

24 16 8 45 31

opening to Lake Michigan and annual nutrient fluxes to Lake Michigan were estimated. Comparison of our load estimates with estimates from the Lake Michigan mass balance program indicated that in 2003, loads of POC to Lake Michigan were similar to loads in 1994 and 1995, while DOC and TP loads in 2003 were lower than in 1994 and 1995 (Table 3). In 2003, C:P molar values in Lake Michigan were significantly higher than values measured by T. Johengen (unpublished data) in 1999–2000 for the same near shore area off Muskegon (1999 avg. C: P = 155, n = 19; 2000 avg. C:P = 127, n = 16). The lower C:P values in 1999–2000 likely were caused by the nearly 10% higher discharges in those years relative to 2003; C:P ratios in near shore lake environments are known to vary inversely with terrestrial inputs and resuspension events (Biddanda and Cotner, 2002). Our DOC estimates also varied seasonally and were lowest in spring and highest in summer, perhaps in response to spring and late summer phytoplankton bloom formation (Biddanda and Cotner, 2002). Nitrate and total phosphorus concentrations peaked in spring and fall in response to discharge events. Plumes of terrestrial materials originating from tributaries are a well-documented phenomenon in the Great Lakes. Previous research on southern Lake Michigan and its various tributaries has shown that riverine inputs into Lake Michigan are characterized by significantly elevated DOC (×5) and TDP (×10) concentrations relative to those measured in Lake Michigan (Biddanda and Cotner, 2002). Johengen et al. (2008) used field and laboratory experiments to demonstrate that seasonal inputs from the nearby St. Joseph River and episodic sediment resuspension events could enhance heterotrophic and autotrophic production in near shore Lake Michigan by three to five-fold. For the 1994–2008 period, both the St. Joseph River and Grand River contributed much higher loads of total phosphorus (374 and 555 MT/yr) to Lake Michigan when compared to average annual loads from the Muskegon River watershed (71 MT/yr, Dolan and Chapra, 2012). Possible explanations for this difference in loadings among watersheds are that the Grand and St. Joseph River watersheds have a greater percentage of agriculture in their watersheds, and terminate directly into Lake Michigan instead of terminating in a drowned river mouth lake. Recent studies in the Great Lakes region suggest that tributary geomorphology may influence the delivery and fate of nutrients from a given watershed (Arend, 2008; Chen and Driscoll, 2009). Great Lakes coastal embayments and wetlands that are “open” to the Lakes are regularly influenced by wind driven seiche events and changing lake levels (Hoffman et al., 2012; Wilson et al., 2005). However, Muskegon Lake is attached to Lake Michigan by a narrow shipping channel (approximately 90 m wide). Thus, in addition to restricting flow from Muskegon Lake, the potential for Lake Michigan waters to flow into Muskegon Lake is likely limited. Another possible explanation for the lack of a strong watershed signal in near shore Lake Michigan may be that materials originating in the MRW are being rapidly advected away from the near shore zone of Lake Michigan into deeper water. Surficial sediments in Muskegon Lake were mostly composed of greater than 60% of the fine grained (b63 μm) size fraction, while virtually none of the Lake Michigan samples comprised a large percentage of fine grain. In a study of samples collected from a series of sediment traps deployed off the mouth of the Grand River in Lake Michigan, Meyers et al. (1984) used C:N ratios, lipids, and various other biomarkers to demonstrate the presence of a plume of materials of terrestrial origin off the mouth of the Grand River (Meyers et al., 1984). Using the same series of sediment traps, Eadie et al. (1984) demonstrated that organic carbon concentrations of surficial sediments increased along with an increase in percentage of fine sediment with distance from shore (up to 35 km offshore), and proposed that terrestrial materials were transported from near-bottom downslope to offshore. Meyers and Eadie (1993) found that seston δ13C values increased at depth in sediment trap samples collected from a trap deployed at a depth of 145 m. They theorized that lateral transport of seston from coastal regions with higher levels of productivity was the source of the enriched δ13C (Meyers and Eadie, 1993). More intensive sampling

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around peak discharge or resuspension events, that includes shorter sampling intervals and sampling at deeper depths in Lake Michigan are likely needed to document and trace terrestrial organic matter and nutrients from drowned river mouth lakes in Great Lakes near shore zones at finer scales. In addition to understanding the transport of watershed-derived materials into and out of Muskegon Lake and near shore Lake Michigan, we also sought to understand the processes that may be acting on these materials when they reach those habitats. Isotopic signatures of suspended seston particles lend an understanding to the sources of energy and processes occurring within a given food web, as well as transfers among food webs in adjacent habitats (Hoffman et al., 2010, 2012; Keough et al., 1996; Larson et al., 2012; Peterson and Fry, 1987). Our study revealed significant differences in the stable isotope signatures of seston among Muskegon River, Muskegon Lake, and Lake Michigan, indicating that a number of different energy sources and processes may be occurring within these respective food webs. Previous studies in the Great Lakes have also used seston (or particulate organic matter) stable isotope signatures in an attempt to understand energy transfers among adjacent habitats. Keough et al. (1996) demonstrated differences in stable isotope signatures of organic matter between near shore and offshore food webs in Lake Superior, where the offshore food web was characterized by enriched δ13C of POM relative to the δ13C of POM from the wetland, though both food webs appeared to be based on phytoplankton. In the St. Louis River tributary of Lake Superior, Hoffman et al. (2010) identified a pattern of increased enrichment in δ13C signatures of primary producers, seston, zooplankton, and zoobenthos with distance downstream towards the open lake. We note that a similar trend was also apparent in the δ13C of Muskegon River and Lake Michigan seston, wherein δ13C of Lake Michigan seston was enriched by roughly 2‰ compared to the seston signature collected at both of the Muskegon River stations, and nearly 5‰ compared to the Muskegon Lake station. Seston δ13C and δ15N signatures at the Upper and Lower Muskegon River stations were not statistically different from one another even though these two stations were associated with very different riverine habitats. Both Muskegon River stations had δ13C values ~−28‰, and δ15N values of ~5‰. The Upper River station was in close proximity to Croton Dam and was characterized by clear, fast moving water with a hard rock/cobble substrate at the bottom. In contrast, the Lower River station was characterized by slower moving waters, a soft substrate bottom, and its close proximity to a large coastal wetland complex. Given the difference in these habitats, one might expect to find significant differences in the seston isotope signals from these stations. Nonetheless, riverine seston samples represent a mixture of terrestrial, detrital, and aquatic materials mixed together by the physical processes associated with downstream river flow (Gu et al., 2011). It is possible that more intensive sampling at finer scales would highlight differing energy sources that are supporting these habitats, but these differences were not picked up by our sampling. The enriched δ13C signal (−26.2 ± 0.5‰) in Lake Michigan relative to the other stations can be explained by preferential uptake by primary producers during photosynthesis. Seston from Lake Michigan was characterized by an enriched δ13C that fluctuated seasonally, and a depleted δ15N signature relative to seston at stations in the Muskegon River and Muskegon Lake. Previous isotopic studies of Great Lakes seston have demonstrated that algae and other primary producers preferentially use the lighter isotope (12C) during photosynthesis (Schelske and Hodell, 1991). During periods of increased primary productivity, the 12C in the dissolved inorganic carbon pool may be used up faster than can be replaced, leaving more of the 13CO2 to be used for photosynthesis (Leggett et al., 1999; Schelske and Hodell, 1991). As a result, δ13C signatures of phytoplankton become enriched during periods of high primary productivity as was seen in Lake Michigan seston samples collected for this study, which were enriched in δ13C during spring and summer.

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Larson et al. (2012) reported a trend of depleted-to-enriched δ13C, and enriched-to-depleted δ15N in seston and consumer signatures along a gradient from river to near shore habitats in a study of 11 tributaries of Lake Michigan. This trend in δ15N was often interrupted at tributary river mouths, likely resulting from the presence of low-flow depositional habitats that occur there. Additionally, spatial patterns in δ13C signatures at two rivers (the Pike River in Wisconsin and the Betsie River in Michigan) were significantly different relative to signatures measured at upriver or near shore stations. In particular, the Betsie River terminates in a drowned river mouth lake (Betsie Lake) and showed a pattern of depleted δ13C and enriched δ15N signatures in consumers at the river mouth compared to either tributary or near shore Lake Michigan habitats. Larson et al. (2012) concluded that there may have been alternative sources of carbon (other than “river” or “lake” carbon) in the river mouths influencing the δ13C signal in these two systems, and that river mouths generally represented a “disconnect” between rivers and lakes in terms of their isotopic signals. In our study, seston signatures measured at the drowned river mouth (Muskegon Lake) station were unique, being depleted in δ13C (−30.9 ± 0.6‰) and enriched in δ15N (6.3 ± 0.6‰) relative to both Muskegon River and Lake Michigan, similar to what Larson et al. (2012) measured in the Betsie River. TSM concentrations indicated that substantial amounts of material coming from Muskegon River settle within Muskegon Lake. In systems where high amounts of organic matter are present, microbial processing of this material can lead to a shortage of oxygen in sediments and overlying waters (Kiyashko et al., 2004). Low oxygen (hypoxic) waters are defined as having oxygen concentrations of less than 3 mg/L of dissolved oxygen (ESA, 2008). Dissolved oxygen concentrations as low as 2 mg/L were recorded in the bottom waters of Muskegon Lake from 2002 thru 2007 (Bopiah Biddanda, Annis Water Resources Institute, personal communication). In the absence of sufficient oxygen, methanogenic bacteria process organic material, producing methane that is isotopically light (−60 to −80‰ δ13C) (Kiyashko et al., 2004). This δ13C depleted methane is then oxidized to CO2 in the water column, and eventually makes its way into the food web via primary productivity (Wetzel, 2001). Biogenic methane has been shown to be a critical source of carbon as well as a link between benthic and pelagic food webs in aquatic systems (Bastviken et al., 2003; Jones and Grey, 2011). Kiyashko et al. (2004) reported depleted carbon isotope signatures in chironomids collected in Lake Biwa, Japan, where oxygen concentrations in the hypolimnion are ~3 mg/L during stratification. Through an analysis of the fatty acid compositions of the chironomids, Kiyashko et al. (2004) determined that a large part of their diets consisted of methanotrophic bacteria. DIC δ13C values would undoubtedly help explain the pattern of depleted seston δ13C in Muskegon Lake. Unfortunately, they were not directly measured in this study, though previous studies have noted lower background DIC δ13C values in Muskegon Lake than in Lake Michigan equivalent to 7‰ (Dufour et al., 2005, 2008). Future research should be directed to examine the stable isotope values of DIC in Muskegon Lake as well as the extent of methane production to quantify the impact of this potential source of depleted carbon on the food web. Muskegon Lake seston δ15N values were roughly 1‰ higher than those measured in Muskegon River, and 2.6‰ higher than those measured in Lake Michigan. Interestingly, surficial sediment δ15N values also increased within Muskegon Lake along an east-to-west gradient from the mouth of the Muskegon River to the start of the shipping channel. Increases in δ15N among seston and sediments can be attributed to a number of factors including: impacts of anthropogenic stressors such and urbanization and runoff, agriculture, as well as microbial processing of organic matter and denitrification (Hoffman et al., 2012). Given the fact that Muskegon Lake is surrounded by a relatively large population center and industrial facilities, and that the nutrient loading data indicate that a large amount of nutrients are retained within the lake, we assume that the increase in seston and sediment δ15N values reflect the effects of urbanization around, and the level of microbial activity

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occurring within the lake. The fact that Muskegon Lake seston is characterized by a different isotope signature than that of the seston in Lake Michigan, means that there is potential to use this unique isotope signal as a natural tracer for fishes that move between these habitats regularly, such as the walleye Sander vitreus. Spatial variation in nutrient concentrations and seston stoichiometry may play a significant role in ecological processes in aquatic systems, and may indicate relative deficiency of nutrients for phytoplankton growth (Hecky et al., 1993). DOC values were lowest in near shore Lake Michigan compared to the Muskegon River watershed, perhaps in response to demand by bacterial production (Biddanda and Cotner, 2002). The C:P molar ratios found for lower Muskegon River, Muskegon Lake, and Muskegon Channel in this study were relatively similar and within the range of median values reported for large lakes by Hecky et al. (1993) and Sterner et al. (2008). However, the mean C:P value (342) we found for Lake Michigan was much higher than values in the watershed and higher than most values reported for freshwater lakes (Sterner et al., 2008) because of lower phosphorus concentrations in Lake Michigan — high C:P values indicate phosphorus limitation to phytoplankton growth (Hecky et al., 1993). The seston C:P ratio also was higher than in surficial sediments sampled in either Muskegon Lake or Lake Michigan, possibly due to dissolution of phosphorus from seston to the water column (Hecky et al., 1993). With the phosphorous abatement program, significant improvements of water quality in Great Lakes offshore habitats have been realized (Makarewicz and Howell, 2012; Makarewicz et al., 2012). However, Great Lakes nearshore environments are stilled plagued by persistent outbreaks Microcystis and Cladophora as well as everchanging nutrient dynamics due to the population explosion of the invasive dreissenid mussels (Dolan and Chapra, 2012; Hecky et al., 2004; Makarewicz et al., 2012). This study demonstrates the unique ability of a drowned river mouth lake, Muskegon Lake, to intercept and process terrestrial materials flowing out of the Muskegon River. These results support recent calls in the Great Lakes research community for an increased focus of nearshore, coastal habitat, and river mouth nutrient dynamics.

Conclusion Although lateral transport of materials from near shore to offshore environments has been demonstrated in the Great Lakes, the narrow channel between Muskegon Lake and Lake Michigan may constrain the amount of material transported out of it. As a result of organic matter deposition and high nutrient retention within Muskegon Lake, methane produced from low oxygen portions of the lake may be a depleted carbon source being incorporated into the Muskegon Lake food web. The depleted δ13C signature and δ15N signature of Muskegon Lake seston relative to either Lake Michigan or the Muskegon River indicate a fundamental difference at the bases of the food webs in these respective habitats, and will likely be a useful natural tracer to determine fish utilization of Muskegon Lake in future research.

Acknowledgments We acknowledge support from the University of Michigan's (UM) Office of Vice President of Research, the Cooperative Institute for Limnology and Ecosystems Research, the UM School of Natural Resources and Environment; and the Great Lakes Fisheries Trust. The field assistance for this project was provided by Lori Ivan, Tomas Höök, David Swank, Jessica Blake, Becky Loftus, Joel Van Noord, and Rob McTear. Help in creating the site map was provided by Lacey Mason (University of Michigan), and the contour plots were created by Pat Clinton (US EPA). This is contribution number 2013-1676 from NOAA's Great Lakes Environmental Research Laboratory.

References Albert, D.A., Wilcox, D.A., Ingram, J.W., Thompson, T.A., 2005. Hydrogeomorphic classification for Great Lakes coastal wetlands. J. Great Lakes Res. 31 (S1), 129–146. Anderson, J.M., 1975. An ignition method for determination of total phosphorus in lake sediments. Water Res. 10, 329–331. Arend, K.K., 2008. The Role of Environmental Characteristics on Fish Community Structure and Food Web Interactions in Lake Ontario Embayments. Ph.D. dissertation Cornell University, Ithaca. Bastviken, D., Ejlertsson, J., Sundh, I., Tranvik, L., 2003. Methane as a source of carbon and energy for lake pelagic food webs. Ecology 84, 969–981. Bastviken, D.J., Cole, J.J., Pace, M.L., Van de Bogert, M.C., 2008. Fates of methane from different lake habitats: connecting whole-lake budgets and CH4 emissions. J. Geophys. Res. 113, G02024. http://dx.doi.org/10.1029/2007JG000608. Bhagat, Y., Reutz III, C.R., 2011. Temporal and fine-scale spatial variation in fish assemblage structure in a drowned river mouth system of Lake Michigan. Trans. Am. Fish. Soc. 140 (6), 1429–1440. Biddanda, B.A., Cotner, J.B., 2002. Love handles in aquatic ecosystems: the role of dissolved organic carbon drawdown, resuspended sediments, and terrigenous inputs in the carbon balance of Lake Michigan. Ecosystems 5, 431–445. Brazner, J.C., Tanner, D.K., Morrice, J.A., 2001. Fish mediated nutrient and energy exchange between a Lake Superior coastal wetland and its adjacent bay. J. Great Lakes Res. 27, 98–111. Carter, G.S., Nalepa, T.F., Rediske, R.R., 2006. Status and trends of benthic populations in a coastal drowned river mouth lake of Lake Michigan. J. Great Lakes Res. 32, 578–595. Chen, X., Driscoll, C.T., 2009. Watershed land use controls on chemicals inputs into Lake Ontario embayments. J. Environ. Qual. 38, 2084–2095. Cole, J.J., Carpenter, S.R., Kitchell, J., Pace, M.L., Solomon, C.T., Weidel, B., 2011. Strong evidence for terrestrial support of zooplankton in small lakes based on stable isotopes of carbon, nitrogen, and hydrogen. Proc. Natl. Acad. Sci. 108, 1975–1980. Davis, C.O., Simmons, M.S., 1979. Water Chemistry and Phytoplankton Field and Laboratory Procedures. Great Lakes Research Division, University of Michigan, Ann Arbor, MI. Dolan, D.M., Chapra, S.C., 2012. Great Lakes total phosphorus revisited: 1. Loading analysis and update (1994–2008). J. Great Lakes Res. 38, 730–740. Dufour, E., Patterson, W.P., Höök, T.O., Rutherford, E.S., 2005. Early life history of Lake Michigan alewives (Alosa pseudoharengus) inferred from intra-otolith stable isotope ratios. Can. J. Fish. Aquat. Sci. 62, 2362–2370. Dufour, E., Höök, T.O., Patterson, W.P., Rutherford, E.S., 2008. High-resolution isotope analysis of young alewife Alosa pseudoharengus otoliths: assessment of temporal resolution and reconstruction of habitat occupancy and thermal history. J. Fish Biol. 73, 2434–2451. Eadie, B.J., 1997. Probing particle processes in Lake Michigan using sediment traps. Water Air Soil Pollut. 99, 133–139. Eadie, B.J., Chambers, R.L., Gardner, W.S., Bell, G.L., 1984. Sediment trap studies in Lake Michigan: resuspension and chemical fluxes in the southern basin. J. Great Lakes Res. 10, 307–321. EPA, 2009. Muskegon Lake Area of Concern. http://www.epa.gov/glnpo/aoc/msklake. html. ESA (Ecological Society of America), 2008. http://www.esa.org/education/edupdfs/ hypoxia.pdf. Evans, E.D., 1992. Mona, White, and Muskegon Lakes in Muskegon County, Michigan: the 1950s to the 1980s. Michigan Department of Natural Resources. Evans, M.S., Fahnenstiel, G.L., Scavia, D., 2011. Incidental oligotrophication of North American Great Lakes. Environ. Sci. Technol. 45, 3297–3303. Fahnenstiel, G.L., Nalepa, T.F., Pothoven, S.A., Carrick, H.J., Scavia, D., 2010. Lake Michigan lower food web: long-term observations and Dreissena impact. J. Great Lakes Res. 36, 1–4. Fry, B., 1999. Using stable isotopes to monitor watershed influences on aquatic trophodynamics. Can. J. Fish. Aquat. Sci. 56, 2167–2171. Gu, B.H., Schelske, C.L., Waters, M.N., 2011. Patterns and controls of seasonal variability of carbon stable isotopes of particulate organic matter in lakes. Oecologia 165, 1083–1094. Hecky, R.E., Campbell, P., Hendzel, L.L., 1993. The stoichiometry of carbon, nitrogen, and phosphorus in particulate matter of lakes and oceans. Limnol. Oceanogr. 38, 709–724. Hecky, R.E., Smith, R.E.H., Barton, D.R., Guildford, S.J., Taylor, W.D., Charlton, M.N., Howell, T., 2004. The near shore phosphorus shunt: a consequence of ecosystem engineering by dreissenids in the Laurentian Great Lakes. Can. J. Fish. Aquat. Sci. 61, 1285–1293. Hiriart-Baer, V.P., Diep, N., Smith, R.E.H., 2008. Dissolved organic matter in the Great Lakes: role and nature of allochthonous material. J. Great Lakes Res. 34, 383–394. Hoffman, J.C., Peterson, G.S., Cotter, A.M., Kelly, J.R., 2010. Using stable isotope mixing in a Great Lakes coastal tributary to determine food web linkages in young fishes. Estuaries Coasts 33, 1391–1405. Hoffman, J.C., Kelly, J.R., Peterson, G.S., Cotter, A.M., Starry, M.A., Sierszen, M.E., 2012. Using δ15N in fish larvae as an indicator of watershed sources of anthropogenic nitrogen: response at multiple spatial scales. Estuaries Coasts 35, 1453–1467. Höök, T.O., Rutherford, E.S., Mason, D.M., Carter, G.S., 2007. Hatch dates, growth, survival, and overwinter mortality of age-0 alewives in Lake Michigan: implications for habitat-specific recruitment success. Trans. Am. Fish. Soc. 136, 1298–1312. Höök, T.O., Rutherford, E.S., Croley II, T.E., Mason, D.M., Madenjian, C.P., 2008. Annual variation in habitat-specific recruitment success: implications from an individual based model of Lake Michigan alewife (Alosa pseudoharengus). Can. J. Fish. Aquat. Sci. 65, 1402–1412. Ivan, L.N., Rutherford, E.S., Riseng, C., Tyler, J.A., 2010. Density, production, and survival of walleye (Sander vitreus) eggs in the Muskegon River, Michigan. J. Great Lakes Res. 36, 328–337.

K.M. Marko et al. / Journal of Great Lakes Research 39 (2013) 672–681 Johengen, T.H., Biddanda, B.A., Cotner, J.B., 2008. Stimulation of Lake Michigan plankton metabolism by sediment resuspension and river runoff. J. Great Lakes Res. 34, 213–227. Jones, R.I., Grey, J., 2011. Biogenic methane in freshwater food webs. Freshw. Biol. 56, 213–229. Keough, J.R., Sierszen, M.E., Hagley, C.A., 1996. Analysis of a Lake Superior coastal food web with stable isotope techniques. Limnol. Oceanogr. 41, 136–146. Kerfoot, W.C., Budd, J.W., Eadie, B.J., Vanderploeg, H.A., Agy, M., 2004. Winter storms: sequential sediment traps record Daphnia ephippial production, resuspension, and sediment interactions. Limnol. Oceanogr. 49, 1365–1381. Kerfoot, W.C., Yousef, F., Green, S.A., Budd, J.W., Schwab, D.J., Vanderploeg, H.A., 2010. Approaching storm: disappearing winter bloom in Lake Michigan. J. Great Lakes Res. 36, 30–41. Kiyashko, S.I., Imbs, A.B., Narita, T., Svetashev, V.I., Wada, E., 2004. Fatty acid composition of aquatic insect larvae Stictochironomus pictulus (Diptera: Chironomidae): evidence of feeding upon methanotrphic bacteria. Comp. Biochem. Physiol. B 139, 705–711. Larson, J.H., Richardson, W.B., Valazza, J.M., Nelson, J.C., 2012. An exploratory investigation of the landscape-lake interface: land cover controls over consumer N and C isotopic composition in Lake Michigan rivermouths. J. Great Lakes Res. 38, 610–619. Leggett, M.F., Servos, M.R., Hesslein, R.H., Johannsson, O.E., Millard, E.S., Dixon, D.G., 1999. Biogeochemical influences on the carbon isotope signatures of Lake Ontario biota. Can. J. Fish. Aquat. Sci. 56, 2211–2218. Mackin, J.E., Owen, R.M., Meyers, P.A., 1980. A factor analysis of elemental association in the surface microlayer of Lake Michigan and its fluvial inputs. J. Geophys. Res.-Oceans Atmos. 85, 1563–1569. Makarewicz, J.C., Howell, E.T., 2012. The Lake Ontario nearshore study: introduction and summary. J. Great Lakes Res. 38, 2–9. Makarewicz, J.C., Booty, W.G., Bowen, G.S., 2012. Tributary phosphorus loading into Lake Ontario. J. Great Lakes Res. 38, 14–20. McCusker, E.M., Ostrom, P.H., Ostrom, N.E., Jeremiason, J.D., Baker, J.E., 1999. Seasonal variation in the biogeochemical cycling of seston in Grand Traverse Bay, Lake Michigan. Org. Geochem. 30, 1543–1557. Menzel, D.W., Corwin, N., 1965. The measurement of total phosphorous liberated in seawater based on the liberation of organically bound fractions by persulfate oxidation. Limnol. Oceanogr. 10, 280–282. Meyers, P.A., Eadie, B.J., 1993. Sources, degradation and recycling of organic matter associated with sinking particles in Lake Michigan. Org. Geochem. 20, 47–56.

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Meyers, P.A., Leenheer, M.J., Eadie, B.J., Maule, S.J., 1984. Organic geochemistry of suspended and settling particulate matter in Lake Michigan. Geochim. Cosmochim. Acta 48, 443–452. Mida, J.L., Scavia, D., Fahnenstiel, G.L., Pothoven, S.A., Vanderploeg, H.A., Dolan, D.M., 2010. Long-term and recent changes in southern Lake Michigan water quality with implications for present trophic status. J. Great Lakes Res. 36, 42–49. Peterson, B.J., Fry, B., 1987. Stable isotopes in ecosystems studies. Annu. Rev. Ecol. Syst. 18, 293–320. Peterson, G.S., Sierzen, M.E., Yurista, P.M., Kelly, J.R., 2007. Stable nitrogen isotopes of plankton and benthos reflect a landscape-level influence on Great Lakes coastal ecosystems. J. Great Lakes Res. 33, 27–41. Schelske, C.L., Hodell, D.A., 1991. Recent changes in productivity and climate of Lake Ontario detected by isotopic analysis of sediments. Limnol. Oceanogr. 36, 961–975. Schwab, D.J., Beletsky, D., Lou, J., 2000. The 1998 coastal turbidity plume in Lake Michigan. Estuarine Coastal Shelf Sci. 50, 49–58. Steinman, A.D., Ogdahl, M., Rediske, R., Ruetz III, C.R., Biddanda, B.A., Nemeth, L., 2008. Current status and trends in Muskegon Lake, Michigan. J. Great Lakes Res. 34, 169–188. Sterner, R.W., Andersen, T., Elser, J.J., Hessen, D.O., Hood, J.M., McCauley, E., Urabe, J., 2008. Scale-dependent carbon:nitrogen:phosphorus seston stoichiometry in marine and freshwaters. Limnol. Oceanogr. 53, 1169–1180. Tang, Z., Engel, B.A., Pijanowski, B.C., Lim, K.J., 2005. Forecasting land use change and its environmental impact at a watershed scale. J. Environ. Manage. 76, 35–45. Torbick, N.M., Becker, B.L., Hession, S.L., Qi, J., Roloff, G.J., Stevenson, R.J., 2010. Assessing invasive plant infestation and disturbance gradients in a freshwater wetland using a GIScience approach. Wetl. Ecol. Manag. 18, 307–319. Vander Zanden, M.J., Vadeboncoeur, Y., Diebel, M.W., Jeppesen, E., 2005. Primary consumer stable nitrogen isotopes as indicators of nutrient source. Environ. Sci. Technol. 39, 7509–7515. Wetzel, R.G., 2001. Limnology: Lake and River Ecosystems, third edition. Academic Press, San Diego, CA. Wilson, C.G., Mastioff, G., Whiting, P.J., Klarer, D.M., 2005. Transport of fine sediment through a wetland using radionuclide tracers: Old Woman Creek, OH. J. Great Lakes Res. 31, 56–67. Zar, J.H., 2009. Biostatistical Analysis, 5th ed. PearsonHigherEd.com (Published by).