The deepwater amphipod Diporeia hoyi has disappeared from Lake Erie and much of Lake Ontario at depths < 80 m. This amphipod had supplied 20 percent of the fisheries energy budget in the Great Lakes. The exotic mussel Dreissena bugensis now forms most of the benthic biomass above 60 m depth, but Diporeia is absent over large areas where Dreissena are rare. The filamentous bacterium Thioploca ingrica is now common at many sites between 30 and 40 m where Diporeia has disappeared. Fisheries and Oceans, Canada, investigated the causes of the decline by examining the sediment chemistry, bacterial production and conducted sediment bioassays using Diporeia, Hyalella and Microtox® Microtox® showed no evidence of toxicity in sediments now devoid of Diporeia. Amphipod survival and growth was greatest in sediment that rapidly lost its Diporeia population in 1993. Presence of Thioploca had no effect on Diporeia survival. Hyalella was more sensitive than Diporeia to test sediments and to filtered water from mussel cultures. Sediment from sites with dense Dreissena populations had lower Diporeia survival. A diet of mussel pseudofaeces caused significantly lower survival in both Hyalella and Diporeia. The exact mechanism causing lower survival is currently unknown and may be related to a nutritional problem or associated waste metabolites.

Introduction

The deep-water amphipod Diporeia spp. was the dominant deposit feeding benthic invertebrate in the Great Lakes, and large boreal lakes of glaciated North America between the lower Mackenzie River eastward to Lake Champlain (Dadswell, 1974). The species burrows in mud at temperatures below 14°C, and is usually associated with the presence of lake trout (Salvelinus namaycus) and lake whitefish (Coregonus clupeaformis). The related species Monoporeia affinis and Pontoporeia femorata are common in nearshore areas of the Arctic Ocean, the Gulf of St. Lawrence, and are key elements of the Baltic benthos (Elmgren et al., 1990).

In the Great Lakes, Diporeia formed 60 to 80% of benthic biomass, except in shallow western Lake Erie. Before 1990, amphipod densities were typically > 3000 m−2, with maximum densities of 12,000 m−2 (Nalepa et al., 1998) and dry biomass of 3 g m−2 existing at depths between 30 and 60 m. Their high lipid levels (to 50% of their dry weight; Gauvin et al., 1989), and high assimilation of deposited diatoms (Fitzgerald and Gardner, 1993) made Diporeia an important pelagic—benthic link between the spring algal blooms and the commercial fisheries (lake whitefish and rainbow smelt (Osmerus mordax) and the forage fish: alewife (Alosa pseudoharengus), and sculpins (Cottus spp.) in the lakes (Flint, 1986; McDonald et al., 1990).

In the 1990s, zebra mussels (Dreissena polymorpha) invaded Lakes Erie and Ontario, with D. bugensis colonizing down to 60 m depth (Mills et al., 1993). Filtering by the mussels in nearshore areas increased water clarity and changed phytoplankton, benthic populations and food-webs (Nalepa and Fahnenstiel, 1995; Stewart et al., 1998). After the arrival of the mussels, Diporeia decreased in eastern Lake Erie beginning in 1992 (Dermott and Kerec, 1997) and eastern Lake Ontario in 1993 (Dermott, 2001). The amphipod has progressively disappeared from large areas at depths < 80 m in lakes Ontario, Erie, Michigan and Huron as shown in Figure 1 (Nalepa et al., 1998; Lozano et al., 2001; T. Nalepa, NOAA, personal communications). Declines in commercial catches and reproduction rate of lake whitefish and rainbow smelt have since occurred (Hoyle et al., 1999).

Figure 1.

Map of the Great Lakes showing areas where Diporeia populations have disappeared (shaded) and locations where sediments were collected (x) and sites where live Diporeia were collected for the assays (*).

Figure 1.

Map of the Great Lakes showing areas where Diporeia populations have disappeared (shaded) and locations where sediments were collected (x) and sites where live Diporeia were collected for the assays (*).

Hypothesized causes for the loss of Diporeia include, decreased food availability (i.e. diatoms) due to the intense filtering by nearshore dreissenid mussels populations, toxic sediments due to changing contaminant cycling, and toxic excretions or associated disease from the mussels. Between 1981 and 1995 there were significant reductions in phosphorus levels, algal biomass and chlorophyll in shallow eastern Lake Ontario but not in mid-lake (Johannsson et al., 1998). However, the 50% reduction of algae biomass is not sufficient to account for the complete disappearance of Diporeia from most of eastern Lake Ontario.

Altered food-webs may make sediment-bound contaminants more available, or toxicants may be associated with the large quantities of pseudofaeces that are deposited by the exotic mussels. During storms this material could be transported offshore to the Diporeia populations. Blooms of the Cyanobacteria Microcystis have increased as Dreissena selectively reject small-sized blue green algae (Vanderploeg et al., 2001). The toxicant microcystin present could be transferred offshore to Diporeia via deposited pseudofaeces. In addition, mats of the filamentous sulphur bacteria Thioploca ingrica (Beggiatoaceae) became common in parts of eastern Lake Ontario after Diporeia disappeared (Dermott and Legner, 2002). Thioploca form droplets of sulphur by reacting H2S in the sediment with NO3 from the water; thus, the presence of Thioploca could make the sediments a less favourable medium for Diporeia.

The objectives of this study were to examine the questions: 1) Are Great Lakes sediments that have lost their Diporeia populations now toxic to the amphipods Diporeia and Hyalella, or display toxicity in the Microtox®, pore water test? 2) Does the presence of the sediment bacterium Thioploca affect Diporeia survival? 3) Are dreissenid pseudofaeces or the excretions of Dreissena toxic to the amphipods?

Methods

Sediments were collected from sites where Diporeia have disappeared (Figure 1), sites where Diporeia are still present, and sediment containing bacterial mats of Thioploca (Bay of Quinte). Sediments were collected using an Ekman or PONAR grab. The top 4 cm of sediment was removed and stored in plastic bags at 5°C until used (within 3 months of collection). Sediment sub-samples were freeze dried for particle size and chemical analysis by the National Laboratory for Environmental Testing (Environment Canada, 1995) for major metals, loss on ignition, total organic carbon and neutral herbicides. Particle size was done by the sedigraph/sieve method. Bacterial production in the sediments was measured in the sediment-water interface layer from settled sediments by modification of the 3H Leucine uptake method (Hwang and Heath, 1997).

Microtox® porewater test

The bioluminescence or Microtox® test is used to quantify toxic effects of substances in aqueous solutions or pore waters. The Microtox® liquid phase acute toxicity assay was conducted using pore water extracted from sediment by centrifuging 240 ml of sediment at 6,000 rpm for 60 min at 4°C (Giesy et al., 1988; Munawar et al., 1999). The supernatant was filtered through glass microfibre filters (Whatman GF/C) under 10 psi vacuum. Pore water was maintained at 4°C until used. This assay was performed using a Beckman Microtox® model 500 toxicity analyzer following the standard 90% test protocol (Microtox Omni Software, Azur Environmental). Control standards of saline were prepared, as well as solutions of phenol and ZnSO4 used as a positive test of photo-inhibition of the photobacterium after 5-min and 15-min exposures.

Sediment assays with Hyalella

Sediment assays using Hyalella azteca were conducted for 28 d following the procedure by Borgmann and Norwood (1999) using Imhoff settling cones with 11 of water overlaying 15 ml of sediment. Hyalella were grown in laboratory cultures at room temperature with a 16 h light: 8 h dark photo period. Fifteen young Hyalella (0–10 day old) were added to each cone. The Hyalella were fed 2.5 mg of TetraMin® fish flakes added weekly to each cone. The Hyalella were exposed to the collected sediments, and to three treatments which used cotton gauze instead of sediment as a substrate. Control sediments used in the Hyalella assays were a composite from Lake Superior near the Keweenaw Peninsula, which combined sediments from two depths (104 and 164 m).

Two trial runs of four replicates were conducted for all treatments and in the case of the sediments there were two trials per sampling season (spring and fall). Prior to use, sediment was sieved through 1 mm mesh to remove macro-invertebrates, mussels, shell fragments and course particles. Temperature and pH were monitored throughout the incubation period, dissolved oxygen and ammonia concentrations were measured prior to the addition of the organisms and at the end of the 28 d period.

Sediment assays with Diporeia

Live Diporeia were collected during isothermal conditions from Colpoys Bay on Georgian Bay, or Charleston Lake near Kingston. The Diporeia were maintained in sediments from the collection location at 5°C in the dark. Half the water in the cultures was replaced every month, and they were fed freeze dried diatoms (0.8 g) every month. Assays were conducted for 90 d adapted from the methods of Gossiaux et al., 1993, Jackson et al., 1995 and Munawar et al., 1999. Five adult sized Diporeia (4–7 mm) were added to 40 ml of sediment in 250 ml jars (density about 1500 m−2). The amphipods were captured and transferred to the jars using 6 mm I.D. pipettes to reduce exposure to air. Each jar was covered with a 1 mm mesh held on by an elastic band. Six replicate jars were placed in a 12-litre aquarium containing 3 l of water leaving the jars 1 cm below the water surface. A bubbler was placed in each aquarium. Assays were done at 10°C, with a 12 h light/dark photo period. Once per week, 2 mg of freeze dried diatoms were added to each jar to exceed the feeding rate of Diporeia living in mid Lake Ontario (Dermott and Corning, 1988). At 30 and 60 days, the mud in the jars was screened through 1 mm mesh, the surviving amphipods counted, then replaced into the original mud in the same jars. At the end of 90 days, the mud was re-screened and the surviving amphipods removed, counted and examined before being preserved. Control sediments used in the Diporeia assays were a composite from Lake Superior near the Keweenaw Peninsula, or from Batchawana Bay on eastern Lake Superior.

Assays with bacteria or pseudofaeces

Assays of sediment from the Bay of Quinte exposed Hyalella and Diporeia to the sulphur bacterium Thioploca ingrica. In addition, survival of both Diporeia and the Thioploca was measured in one experiment. Thioploca filaments were collected from Bay of Quinte sediment by screening it through a 0.5 mm mesh. Approximately 0.12 g of bacteria was added to each of the jars containing pre-screened Bay of Quinte sediment. Five Diporeia were added to each of 5 jars, one jar had no Diporeia. At 30 and 60 days the jars were screened on a 0.5-mm sieve and the number of surviving Diporeia and the wet weight of surviving Thioploca filaments tallied.

Toxicity of the bacterium Bacillus thuringiensis (Bt) was tested on Hyalella and Diporeia by adding 5 μ l of a 4000 I.U. per mg solution (Thuricide) of the natural insecticide to the control sediments in each cone or jar. Sediments used for the added Bt assays were Batchawana Bay for Diporeia, and Colpoys Bay and the Bay of Quinte sediment for Hyalella.

Toxicity of pseudofaeces and Dreissena excretions was also tested. Laboratory cultures of mostly zebra mussels (Dreissena polymorpha) were fed frozen diatoms collected from Lake Ontario during the spring bloom (March–April). Pseudofaeces was collected from the aquaria by siphon onto a 28 μ mesh, placed in graduated tubes and allowed to settle for 24 h. After settling, the ratio of water was adjusted to 12 ml pseudofaeces: 8 ml water. One ml aliquots of this pseudofaeces slurry were dried and ashed to estimate average organic content. The organic content of the pseudofaeces used in the assays averaged 0.013 g ml−1 (S.E. 0.0014), or 14.62% (S.E. 1.28%) of its dry weight. The required volume of the 12:8 slurry that had double the organic content as compared to the diatom or TetraMin® diet was calculated, and this volume added to each jar once per week in place of the normal diet. The pseudofaeces were stored for a minimum of 2 wk at 5°C before use to represent a transport time from the nearshore to below the thermocline.

Filtered water from the aquarium containing Dreissena was prepared by filtering the water through a 0.45 μ filter to remove all but viral-sized particles and dissolved chemicals. The 3 l of water in each assay aquarium (Diporeia) or 11 in each Imhoff cone (Hyalella) was replaced every week with freshly filtered water cooled to the appropriate temperature. Control sediments for the Hyalella in the assays with added pseudofaeces or filtered water were from mid Lake Ontario, because of better survival than in the Lake Superior sediments. Assays with Hyalella were also done using cotton gauze as the substrate, exposure to filtered water, or mussel pseudofaeces added to the gauze.

Mean values and standard errors were determined for the amphipod assays. Significant differences (p < 0.05) between test samples and control sediment were determined by Analysis of Variance (ANOVA) of the number alive at the end of the assays, followed by Bonferroni comparisons.

Results and discussion

The sediments assayed, depth of collection, particle size and organic content are listed in Table 1. At all sites analyzed, levels of neutral herbicides were below detection limits (atrazine 18 ng g−1; simazine and D-simazine 10 ng g−1; benzoylpropethyl 2.7 ng g−1; butylate 10 ng g−1; diclofomethyl 6.2 ng g−1; metolachlor 17 ng g−1). This would be expected as only the Bay of Quinte site was close to tributary sources of agricultural chemicals. The concentrations of selected metals are listed in Table 2. Metal levels were greatest in sediments from mid Lake Ontario and western Lake Erie, but none of the sites had sediments that exceeded the Severe Effects Levels guidelines (SEL; Persaud et al., 1993). Both Batchawana Bay and Charleston Lake had elevated levels of Cr, Pb and Zn in spite of being in forested watersheds with relatively few inhabitants.

Depth (m), percent sand, mean particle size (μ m) and percent organics (loss on ignition) in the collected sediments.

Table 1.
Depth (m), percent sand, mean particle size (μ m) and percent organics (loss on ignition) in the collected sediments.
Station depth m % Dry % sand % clay Mean particle micron % Organic loss % of Dry Organic C % Organic N % Herbicides 
L.Superior-comp. 101 54.4 65.7 12.3 102.2 1.7 0.85 0.18 < d.l. 
Batchawana Bay 32 34.2 1.5 31.2 7.7 4.3 1.71 0.17 < d.l. 
Colpoy's Bay 38 — 22.8 27.8 5.2 2.4   < d.l. 
L. Erie-west 10 34.5 4.9 34.6 7.7 6.2 3.43 0.17 < d.l. 
L. Erie-east 38 43.4 0.3 60.7 2.7 3.4 2.45 0.11 < d.l. 
L. Ontario-west 45 41.8 22.1 17.9 17.8 3.2 2.60 0.22 < d.l. 
L. Ontario-mid 125 15.9 0.6 47.5 4.3 7.9 2.98 0.35 < d.l. 
L. Ontario-east 35 22.6 2.1 26.1 9.8 10.62 6.08 0.68 < d.l. 
Bay of Quinte 32 20.4 39.2 6.7 9.7 7.10 0.82 < d.l. 
Charleston Lake 40 9.8 1.2 37.6 7.3 25.29 12.1 1.36 < d.l. 

Detection limits (d.l. ng g−1): Atrazine 18.0; Simazine 10.0; Metolachlor 17.7; Benzoylpropethyl 2.7.

 
Station depth m % Dry % sand % clay Mean particle micron % Organic loss % of Dry Organic C % Organic N % Herbicides 
L.Superior-comp. 101 54.4 65.7 12.3 102.2 1.7 0.85 0.18 < d.l. 
Batchawana Bay 32 34.2 1.5 31.2 7.7 4.3 1.71 0.17 < d.l. 
Colpoy's Bay 38 — 22.8 27.8 5.2 2.4   < d.l. 
L. Erie-west 10 34.5 4.9 34.6 7.7 6.2 3.43 0.17 < d.l. 
L. Erie-east 38 43.4 0.3 60.7 2.7 3.4 2.45 0.11 < d.l. 
L. Ontario-west 45 41.8 22.1 17.9 17.8 3.2 2.60 0.22 < d.l. 
L. Ontario-mid 125 15.9 0.6 47.5 4.3 7.9 2.98 0.35 < d.l. 
L. Ontario-east 35 22.6 2.1 26.1 9.8 10.62 6.08 0.68 < d.l. 
Bay of Quinte 32 20.4 39.2 6.7 9.7 7.10 0.82 < d.l. 
Charleston Lake 40 9.8 1.2 37.6 7.3 25.29 12.1 1.36 < d.l. 

Detection limits (d.l. ng g−1): Atrazine 18.0; Simazine 10.0; Metolachlor 17.7; Benzoylpropethyl 2.7.

 

Metal values as mg kg−1 in tested sediments.

Table 2.
Metal values as mg kg−1 in tested sediments.
Sediment As Ca Cd Cr Cu Fe Ni Pb Zn 
Lake Superior          
   Composite 23800 0.3 25 25 16400 19.7 12.5 40 
   Batchawana Bay 7660 1.5 65 38 13713 31.7 30.5 111 
Lake Huron          
   Colpoys Bay 79456 1.9 48 25 25917 51.8 40.6 69 
Lake Erie          
   Western 35600 1.8 62 40 28900 46.9 48.8 159 
   Eastern 81300 0.4 49 26 32700 38.2 18.3 95 
Lake Ontario          
   Western 15600 0.4 38 27 27200 28.9 22.6 95 
   Mid-lake 20 16900 2.1 74 75 46200 61.9 88.1 293 
   Eastern 64100 1.2 42 47 20600 38.1 41.3 141 
Bay of Quinte 10 8440 1.0 63 42 43700 50.4 27.6 143 
Charleston lake 11400 2.2 64 41 43900 40.7 172 298 
SEL 33 — 10 110 110 — 75 250 820 

Also given are the Ontario Ministry of Environment's severe effect level (SEL) which is considered heavily polluted and affects the health of sediment-dwelling organisms (Persaud et al., 1993).

 
Sediment As Ca Cd Cr Cu Fe Ni Pb Zn 
Lake Superior          
   Composite 23800 0.3 25 25 16400 19.7 12.5 40 
   Batchawana Bay 7660 1.5 65 38 13713 31.7 30.5 111 
Lake Huron          
   Colpoys Bay 79456 1.9 48 25 25917 51.8 40.6 69 
Lake Erie          
   Western 35600 1.8 62 40 28900 46.9 48.8 159 
   Eastern 81300 0.4 49 26 32700 38.2 18.3 95 
Lake Ontario          
   Western 15600 0.4 38 27 27200 28.9 22.6 95 
   Mid-lake 20 16900 2.1 74 75 46200 61.9 88.1 293 
   Eastern 64100 1.2 42 47 20600 38.1 41.3 141 
Bay of Quinte 10 8440 1.0 63 42 43700 50.4 27.6 143 
Charleston lake 11400 2.2 64 41 43900 40.7 172 298 
SEL 33 — 10 110 110 — 75 250 820 

Also given are the Ontario Ministry of Environment's severe effect level (SEL) which is considered heavily polluted and affects the health of sediment-dwelling organisms (Persaud et al., 1993).

 

The west and east Lake Erie, and west Lake Ontario sites had the highest density of Dreissena in the sediments examined (500, 4590, 2320 m−2 respectively, Table 3). No mussels were collected at the mid or east Lake Ontario sites. Dreissena were present in Colpoys Bay at < 10 m−2 but not quantified. A negative association between Diporeia and Dreissena densities existed above densities of about 500 m−2 (Figure 2). This vivid negative relationship between the two species has also been shown in both Lake Erie and Ontario (Dermott and Kerec, 1997; Lozano and Nalepa, 2003), and suggests Dreissena densities of > 500 m−2 are detrimental to Diporeia.

Figure 2.

Relationship between Dreissena density and Diporeia density and survival in the sediments assayed.

Figure 2.

Relationship between Dreissena density and Diporeia density and survival in the sediments assayed.

Depth (m), density of Diporeia and dreissenid mussels (number m−2), and relative abundance of Thioploca at sites where sediments were collected.

Table 3.
Depth (m), density of Diporeia and dreissenid mussels (number m−2), and relative abundance of Thioploca at sites where sediments were collected.
Sediment Depth (m) Diporeia (no. m−2Dreissena (no. m−2Thioploca (g m−2 Wet) Bacterial production (mg C hr−1.) 
Lake Superior      
   Composite 101 96 —  
   Batchawana Bay 32 548 10 0.394 
Lake Huron      
   Colpoys Bay 33 2000 —  
Lake Erie      
   Western 10 500 — 0.400 
   Eastern 38 4590 12 0.999 
Lake Ontario      
   Western 45 2320 — 0.872 
   Mid-lake 125 987 — 0.397 
   Eastern 35 83 0.790 
Bay of Quinte 32 420 206 0.576 
Charleston Lake 40 3740 0.398 

Degree of abundance: − = not seen, + = low.

 
Sediment Depth (m) Diporeia (no. m−2Dreissena (no. m−2Thioploca (g m−2 Wet) Bacterial production (mg C hr−1.) 
Lake Superior      
   Composite 101 96 —  
   Batchawana Bay 32 548 10 0.394 
Lake Huron      
   Colpoys Bay 33 2000 —  
Lake Erie      
   Western 10 500 — 0.400 
   Eastern 38 4590 12 0.999 
Lake Ontario      
   Western 45 2320 — 0.872 
   Mid-lake 125 987 — 0.397 
   Eastern 35 83 0.790 
Bay of Quinte 32 420 206 0.576 
Charleston Lake 40 3740 0.398 

Degree of abundance: − = not seen, + = low.

 

Bacterial production at the sediment-water interface layer in the collected sediments was greatest in sediments from eastern Lake Erie, western and eastern Lake Ontario and lowest in Batchawana Bay (Table 3). Bacterial production reflected the increased organic content of the sediments from deposited material, and may be partly due to the pseudofaeces deposited by the mussels. In Charleston Lake much of the organic content was from refractory plant debris from the forest in the watershed (Table 1) and did not support high bacterial production.

Microtox® testing

Only the pore water from eastern Lake Ontario sediment caused a positive response in the Microtox® assay of less than 30% after 15 min exposure. Other sediments tested caused stimulation of photoactivity as compared to the saline controls (Table 4). The lack of significant difference in Microtox® activity before and after exposure to the sediment pore water indicated metal levels in the sediments (Table 2) were not sufficient to cause inhibition. Likewise, pore water from sediments with high Dreissena densities did not result in photo-inhibition. Thus, the absence of Diporeia in sediments from Lake Ontario or eastern Lake Erie does not appear to be due to toxic chemicals in the pore water.

Percent effect of various sediments in Microtox® assays, using a concentration of 90% pore water plus saline.

Table 4.
Percent effect of various sediments in Microtox® assays, using a concentration of 90% pore water plus saline.
Sediment 5 min. 15 min. 
Lake Superior   
   Composite 9.5 14.8 
   Batchawana Bay 8.5 4.8 
Lake Huron   
   Colpoy's Bay n.t. n.t. 
Lake Erie   
   Western −16.3 −24.9 
   Eastern −22.5 −30.8 
Lake Ontario   
   Western −26.1 −38.5 
   Mid lake −32.5 −25.9 
   Eastern 43.7 29.3 
   Bay of Quinte 0.3 −14.5 
Charleton Lake n.t. n.t. 
Saline Control 0.0 0.0 
Phenol (5 mg L−168.8 66.2 
ZnSO4 (5 mg L−132.0 70.0 

Two trials were done with measurements of photoactivity made at 5 and 15 minutes.

 

n.t = not tested.

 
Sediment 5 min. 15 min. 
Lake Superior   
   Composite 9.5 14.8 
   Batchawana Bay 8.5 4.8 
Lake Huron   
   Colpoy's Bay n.t. n.t. 
Lake Erie   
   Western −16.3 −24.9 
   Eastern −22.5 −30.8 
Lake Ontario   
   Western −26.1 −38.5 
   Mid lake −32.5 −25.9 
   Eastern 43.7 29.3 
   Bay of Quinte 0.3 −14.5 
Charleton Lake n.t. n.t. 
Saline Control 0.0 0.0 
Phenol (5 mg L−168.8 66.2 
ZnSO4 (5 mg L−132.0 70.0 

Two trials were done with measurements of photoactivity made at 5 and 15 minutes.

 

n.t = not tested.

 

Sediment assays

Diporeia survival was greatest in the pristine muds from Lake Superior and Charleston Lake (Table 5). Survival was lowest in sediment from the Niagara Bar, off the mouth of the Niagara River. Low amphipod populations in this area were considered a result of chemical inputs from the river (Nalepa and Thomas, 1976). Unfortunately, the Microtox® test was not done with the sediment from the Niagara Bar to determine if chemical contaminants are still present. There was lower Diporeia survival in sediments from Lake Erie and west Lake Ontario (64 to 68%), all of which have high Dreissena populations (> 2000 m−2). Survival was high in sediment from east Ontario and the Bay of Quinte which has been devoid of Diporeia since 1993 but still had only a few mussels present (Table 3; Dermott, 2001). Landrum et al. (2000) found that survival of Diporeia was not reduced in Lake Michigan sediments which had lost their amphipod populations, but suspected the low nutritional content caused the amphipods to avoid those sediments.

Percent survival, Standard Error (S.E.) of Hyalella and Diporeia in the assayed sediments (n = number of trials).

Table 5.
Percent survival, Standard Error (S.E.) of Hyalella and Diporeia in the assayed sediments (n = number of trials).
 Hyalella % Survival S.E. Diporeia % Survival S.E. 
L.Superior       
   Composite 81.7 7.4 98.4 1.8 12 
   Batchawana Bay 47.5* 9.1 16 95.0 3.6 12 
Lake Huron       
   Colpoys Bay 85.0 7.7 78.0* 7.2 
Lake Erie       
   Western 90.8 3.1 76.6 15.0 12 
   Eastern 71.0 5.7 20 64.4** 7.6 18 
Lake Ontario       
   Western 77.0 3.9 20 68.0** 7.8 18 
   Niagara Bar n.t.   60.0** 13.6 
   Mid-lake 84.1 3.9 16 95.0 4.2 12 
   Eastern 79.4 7.2 16 80.0 9.6 12 
   Bay of Quinte 79.1 3.8 20 96.6 2.6 12 
Charleston Lake 72.4 11.9 100 

Significant difference compared to control sediment

 

*= p < 0.05

 

**= p < 0.001.

 

n.t = not tested.

 
  
 Hyalella % Survival S.E. Diporeia % Survival S.E. 
L.Superior       
   Composite 81.7 7.4 98.4 1.8 12 
   Batchawana Bay 47.5* 9.1 16 95.0 3.6 12 
Lake Huron       
   Colpoys Bay 85.0 7.7 78.0* 7.2 
Lake Erie       
   Western 90.8 3.1 76.6 15.0 12 
   Eastern 71.0 5.7 20 64.4** 7.6 18 
Lake Ontario       
   Western 77.0 3.9 20 68.0** 7.8 18 
   Niagara Bar n.t.   60.0** 13.6 
   Mid-lake 84.1 3.9 16 95.0 4.2 12 
   Eastern 79.4 7.2 16 80.0 9.6 12 
   Bay of Quinte 79.1 3.8 20 96.6 2.6 12 
Charleston Lake 72.4 11.9 100 

Significant difference compared to control sediment

 

*= p < 0.05

 

**= p < 0.001.

 

n.t = not tested.

 
  

Hyalella was very sensitive to the mud from Batchawana Bay, in eastern Lake Superior (Table 5), an area with little human activity. The low concentrations of the chelators: calcium, iron and organic matter in the sediment from this site may make the metals in the igneous rocks around Batchawana Bay more bioavailable, especially the relatively higher levels of Cr and Zn (Table 2). Hyalella survival in sediment from eastern Lake Erie (71%) or Lake Ontario (77%) with high Dreissena densities was not statistically significantly lower than that in the Lake Superior composite sediment (81.7%; Table 5).

Bacterial assays

Neither Diporeia nor Hyalella had reduced survival in Bay of Quinte sediments that contained Thioploca (Table 6). The added Thioploca represented less than 1/4 of the amount that occurred naturally in these sediments (Table 3; Dermott and Legner, 2002). The amount of Thioploca decreased in jars with added Diporeia over 60 d (Figure 3), indicating the filamentous bacteria was consumed or destroyed by the amphipods. The recent increase of Thioploca in eastern Lake Ontario was likely a result of the bacteria taking advantage of increased sediment organic content following the decline of the Diporeia population. Survival of Hyalella was not reduced when exposed to the bacteria Bt on either Colpoys Bay or Bay of Quinte sediment (Table 6). Survival of Diporeia was over 93% when exposed to this natural insecticide, indicating Bt is not toxic to amphipods.

Figure 3.

Wet weight of Thioploca filaments surviving in sediment with (circle) or without (triangle) Diporeia. Bars are 1 standard error.

Figure 3.

Wet weight of Thioploca filaments surviving in sediment with (circle) or without (triangle) Diporeia. Bars are 1 standard error.

Assays of Diporeia and Hyalella survival using mussel pseudofaeces, filtered water, or added bacteria.

Table 6.
Assays of Diporeia and Hyalella survival using mussel pseudofaeces, filtered water, or added bacteria.
 Hyalella % Survival S.E. Diporeia % Survival S.E. 
L. Superior Composite 81.7 7.4 98.4 1.8 12 
Mid-Lake Ontario 84.1 3.9 16 95.0 4.2 12 
Pseudofaeces/control mud 17.5** 3.2 16 74.4** 5.2 24 
Filtered water/control mud 65.0* 10.3 89.6 3.4 24 
Thioploca/Bay of Quinte 79.1 3.8 20 100 
Bt/Batchawana n.t. —  93.4 9.4 
Bt/Colpoys Bay 88.7 3.3 n.t. —  
Bt/Bay of Quinte 81.3 4.7 n.t. —  
TetraMin®/gauze 55.0** 11.0 n.t. —  
Filtered water/gauze 52.5** 7.0 n.t. —  
Pseudofaeces/gauze 50.8* 10.1 n.t. —  

Control sediments for Diporeia were from Lake Superior or Batchawana Bay. Control substrates for Hyalella were mid-Lake Ontario sediment and gauze-only. Symbols are as in Table 5, n.t = not tested.

 
 Hyalella % Survival S.E. Diporeia % Survival S.E. 
L. Superior Composite 81.7 7.4 98.4 1.8 12 
Mid-Lake Ontario 84.1 3.9 16 95.0 4.2 12 
Pseudofaeces/control mud 17.5** 3.2 16 74.4** 5.2 24 
Filtered water/control mud 65.0* 10.3 89.6 3.4 24 
Thioploca/Bay of Quinte 79.1 3.8 20 100 
Bt/Batchawana n.t. —  93.4 9.4 
Bt/Colpoys Bay 88.7 3.3 n.t. —  
Bt/Bay of Quinte 81.3 4.7 n.t. —  
TetraMin®/gauze 55.0** 11.0 n.t. —  
Filtered water/gauze 52.5** 7.0 n.t. —  
Pseudofaeces/gauze 50.8* 10.1 n.t. —  

Control sediments for Diporeia were from Lake Superior or Batchawana Bay. Control substrates for Hyalella were mid-Lake Ontario sediment and gauze-only. Symbols are as in Table 5, n.t = not tested.

 

Pseudofaeces assays

Mussel pseudofaeces caused significantly less survival of Diporeia as compared to the control sediments (Table 6), in spite of the organic content of the added pseudofaeces being double that of the diatom diet in the controls. A diet of pseudofaeces would be less nutritional than a diet of diatoms, and would be expected to reduce growth rate but not short term survival. Mussel excretions, as filtered H20 from mussel cultures, reduced Diporeia survival only slightly (89%). This suggests that it is the consumption of the pseudofaeces and not the excretions of the mussels that is responsible for the reduced survival. Hyalella was very sensitive to mussel pseudofaeces on mud resulting in a survival of only 17.5%. Hyalella was less sensitive to pseudofaeces when it was added to assays using cotton gauze as the substrate. However, survival of Hyalella was similar in all the assays that used gauze as the substrate (Table 6). Hyalella was also more sensitive to the filtered water from the mussel cultures (65% survival) than was Diporeia. Biomagnification of contaminants in the mussel pseudofaeces would not be expected as the lab cultures of the Dreissena were fed the same diatoms as were the Diporeia living in the control sediments. This suggests either a waste product, a bacterium or a pathogen in the pseudofaeces may be responsible for the reduced survival of Diporeia.

Conclusions

  • There was no evidence of toxicity in the Microtox® test. This suggests the loss of Diporeia was not due to the presence of toxic chemicals in the sediment pore water.

  • Presence of Thioploca in the sediment (Bay of Quinte) did not reduce survival of either amphipod.

  • Exposure to Dreissena excretions or minute sized particles in the water inhabited by the mussels did not reduce survival of Diporeia.

  • Diporeia survival was reduced by 30% in sediments from sites with high mussel densities and their pseudofaeces also significantly reduced survival of both Hyalella and Diporeia.

  • The exact mechanisms explaining the loss of Diporeia is still unknown and may be related to nutritional problems, waste metabolites or diseases that effect fecundity.

Acknowledgments

We thank Bud Timmins (Fisheries and Oceans, Canada) for help in collecting sediments and Diporeia; Summer interns Bianca Radix, Sara Booth and Latha Logasundaram, as well exchange students Nadia Casillas Ituarte and Roxana Sierra Hernandez from the Instituto Politecnico Nacional, Mexico assisted with the amphipod assays and sediment analysis. Jack Colonnello and Tim Johnson of the Ontario Ministry of Natural Resources arranged the collection of the Lake Erie sediments. We are grateful to the 3 anonymous referees for their constructive comments of the manuscript. Sharon Lawrence and Jennifer Lorimer provided technical editing. This work was funded by Fisheries & Oceans ESSRF grant #2213.

References

Borgman, U. and Norwood, W. P.
1999
.
Sediment toxicity testing using large water-sediment ratios: an alternative to water renewal
.
Environm. Poll.
,
106
:
333
339
.
Dadswell, M. J.
1974
.
Distribution, ecology, and postglacial dispersal of certain crustaceans and fishes in eastern North America
,
National Museum of Natural Sciences Publications in Zoology, No 11. National Museums of Canada.
Dermott, R.
2001
.
Sudden disappearance of the amphipod Diporeia from eastern Lake Ontario: 1993–1995
.
J. Great Lakes Res.
,
27
:
423
433
.
Dermott, R. M. and Corning, K.
1988
.
Seasonal ingestion rates of Pontoporeia hoyi (Amphipoda) in Lake Ontario
.
Can. J. Fish. Aquat. Sci.
,
45
:
1886
1895
.
Dermott, R. and Kerec, D.
1997
.
Changes to the deep-water benthos of eastern Lake Erie since the invasion of Dreissena: 1979 to 1993
.
Can. J. Fish. Aquat. Sci.
,
54
:
922
930
.
Dermott, R. and Legner, M.
2002
.
Dense mat-forming bacterium Thioploca ingrica (Beggiatoaceae) in eastern Lake Ontario: implications to the benthic food web
.
J. Great Lakes Res.
,
28
:
688
697
.
Elmgren, R., Ankar, S. and Ejdung, G.
1990
.
Amphipods of the genus Pontoporeia as key elements in the Baltic benthos
.
Ann. Zool. Fennici.
,
27
:
303
304
.
Environment Canada
.
1995
.
Manual of analytical methods: major ions and nutrients, 1
,
p. 340
Ottawa, Ontario
:
N.W.R.I. Water Quality Branch
.
Fitzgerald, S. A. and Gardner, W. S.
1993
.
An algal carbon budget for pelagic-benthic coupling in Lake Michigan
.
Limnol. Oceanogr.
,
38
:
547
560
.
Flint, R. W.
1986
.
Hypothesized carbon flow through the deepwater Lake Ontario food web
.
J. Great Lakes Res.
,
12
:
344
354
.
Gauvin, J. M., Gardner, W. S. and Quigley, M. A.
1989
.
Effects of food removal on nutrient release rates and lipid content of Lake Michigan Pontoporeia hoyi
.
Can. J. Fish. Aquat. Sci.
,
46
:
1125
1130
.
Giesy, J. P., Graney, R. L., Newsted, J. L., Rosiu, C. J. and Benda, A.
1988
.
Comparison of three sediment bioassay methods using Detroit River sediments
.
Environm. Tox. Chem.
,
7
:
483
498
.
Gossiaux, D. C., Landrum, P. F. and Tsymbal, V. N.
1993
.
A survey of Saginaw River and Saginaw Bay, Lake Huron, sediments using two bioassays with the amphipod Diporeia spp
.
J. Great Lakes Res.
,
19
:
322
332
.
Hoyle, J. A., Shaner, T., Casselman, J. M. and Dermott, R.
1999
.
Changes in lake whitefish (Coregonus clupeaformis) stocks in eastern Lake Ontario following Dreissena mussel invasion
.
Great Lakes Res. Rev.
,
4
:
5
10
.
Hwang, S. -J. and Heath, R. T.
1997
.
Bacterial productivity and protistan bacterivory in coastal and offshore communities of Lake Erie
.
Can. J. Fish. Aquat. Sci.
,
54
:
788
799
.
Jackson, M., Milne, J., Johnston, H. and Dermott, R.
1995
.
Assays of Hamilton Harbour sediments using Diporeia hoyi (Amphipoda) and Chironomus plumosus (Diptera)
.
Can. Tech. Rep. Fish. Aquat. Sci.
,
2039
:
1
20
.
Johannsson, O. E., Millard, E. S., Ralph, K. M., Myles, D. D., Graham, D. M., Taylor, W. D., Giles, B. G. and Allen, R. E.
1998
.
The changing pelagia of Lake Ontario (1981 to 1995): a report of the DFO long-term Biological Monitoring Program
.
Can. Tech. Rep. Fish. Aquat. Sci.
,
2243
:
1
278
.
Landrum, P. F., Gossiaux, D. C., Nalepa, T. F. and Fanslow, D. L.
2000
.
Evaluation of Lake Michigan sediment for causes of the disappearance of Diporeia spp. in southern Lake Michigan
.
J. Great Lakes Res.
,
26
:
402
407
.
Lozano, S. J. and Nalepa, T F.
2003
. “
Disruption of the benthic community in Lake Ontario
”. In
State of Lake Ontario: Past, Present and Future
,
Ecovision World Monograph Series
Edited by: Munawar, M.
pp. 305
322
.
Aquatic Ecosystem Health and Management Society
.
Lozano, S. J., Sharold, J. V. and Nalepa, T. F.
2001
.
Recent declines in benthic macroinvertebrate densities in Lake Ontario
.
Can. J. Fish. Aquat. Sci.
,
58
:
518
529
.
McDonald, M. E., Crowder, L. B. and Brandt, S. B.
1990
.
. Changes in Mysis and Pontoporeia populations in southeastern Lake Michigan :a response to shifts in the fish community
.
Limnol. Oceanogr.
,
35
:
220
227
.
Mills, E. L., Dermott, R. M., Roseman, E. F., Dustin, D., Mellina, E., Conn, D. B. and Spidle, A.
1993
.
Colonization, ecology and population structure of the “quagga” mussel in the lower Great Lakes
.
Can. J. Fish. Aquat. Sci.
,
50
:
2305
2314
.
Munawar, M., Dermott, R., McCarthy, L. H., Munawar, S. F. and van Stam, H. A.
1999
.
A comparative bioassessment of sediment toxicity in lentic and lotic ecosystems of the North American Great Lakes
.
Aquat. Ecosystem Health and Manag
,
2
:
367
378
.
Nalepa, T. F. and Fahnenstiel, G. L.
1995
.
Dreissena polymorpha in the Saginaw Bay, Lake Huron Ecosystem: overview and perspective
.
J. Great Lakes Res.
,
21
:
411
416
.
Nalepa, T. F., Hartson, D. J., Fanslow, D. L., Lang, G. A. and Loranzo, S. J.
1998
.
Declines in benthic macroinvertebrate populations in southern Lake Michigan, 1980–1993
.
Can. J. Fish. Aquatic Sci.
,
55
:
2402
2413
.
Nalepa, T. F. and Thomas, N. A.
1976
.
Distribution of macrobenthic species in Lake Ontario in relation to sources of pollution and sediment parameters
.
J. Great Lakes Res.
,
2
:
150
163
.
Persaud, D., Jaagumagi, R. and Hayton, A.
1993
.
Guidelines for the Protection and Management of Aquatic Sediment Quality in Ontario
,
Ontario Ministry of Environment and Energy Report
Toronto, ON.
Stewart, T. W., Miner, J. M. and Lowe, R. L.
1998
.
Macroinvertebrate communities on hard substrates in western Lake Erie: structuring effects of Dreissena
.
J. Great Lakes Res.
,
24
:
868
879
.
Vanderploeg, H. A., Liebig, J. R., Carmichael, W. W., Agy, M. A., Johengen, T. H., Fahnenstiel, G. L. and Nalepa, T. F.
2001
.
Zebra mussel (Dreissena polymorph) selective filtration promoted toxic Microcystis blooms in Saginaw Bay (Lake Huron) and Lake Erie
.
Can. J. Fish. Aquat. Sci.
,
58
:
1208
1221
.