Aquatic Invasions (2017) Volume 12, Issue 3: 287–297 DOI: https://doi.org/10.3391/ai.2017.12.3.03 Open Access © 2017 The Author(s). Journal compilation © 2017 REABIC Special Issue: Invasive Species in Inland Waters

Research Article

Rapid geographic expansion of spiny water flea (Bythotrephes longimanus) in Manitoba, Canada, 2009–2015

Wolfgang Jansen1,*, Ginger Gill1 and Brenda Hann2 1North/South Consultants Inc., 83 Scurfield Blvd., Winnipeg, Manitoba, Canada, R3Y 1G4 2Department of Biological Sciences, University of Manitoba, Winnipeg, Manitoba, Canada, R3T 2N2 Author e-mails: [email protected] (WJ), [email protected] (GG), [email protected] (BH) *Corresponding author Received: 1 October 2016 / Accepted: 12 May 2017 / Published online: 29 June 2017 Handling editor: Ashley Elgin

Editor’s note: This study was first presented at the 19th International Conference on Aquatic Invasive Species held in Winnipeg, Canada, April 10–14, 2016 (http://www.icais.org/html/previous19.html). This conference has provided a venue for the exchange of information on various aspects of aquatic invasive species since its inception in 1990. The conference continues to provide an opportunity for dialog between academia, industry and environmental regulators.

Abstract

The spiny water flea (Bythotrephes longimanus), an aquatic invasive zooplankton species native to Eurasia, was first recorded from Manitoba waters at the Pointe du Bois Generating Station on the Winnipeg River using a larval fish drift net with 950 µm mesh, on 18 July, 2009. Bythotrephes drift density upstream and downstream of the station was highly variable with maximum densities of 23.3 individuals/100 m3 (9 samples) in June 2010 and 9.4 individuals/100 m3 in June 2012 (60 samples). In August and October of 2011, Bythotrephes were identified from the stomachs of eight cisco (Coregonus artedi) collected from the South basin of Lake Winnipeg near the mouth of the Winnipeg River, indicating that the invader had become part of the local food web. Subsequent targeted sampling for Bythotrephes with ship-based vertical plankton net (76 µm mesh) tows at 65 offshore/pelagic sites in Lake Winnipeg during summer and fall of 2012 indicated that the invader had colonized the South basin by early August and had expanded its distribution into most of the North basin by early October. No individuals were captured at a site just past the lake outlet in the Nelson River. Densities of Bythotrephes in Lake Winnipeg ranged from 0 to 93.1 and 0 to 39.2 individuals/m3 among sites for the summer and fall sampling, respectively. The highest mean density (9.2 individuals/m3) was observed for the South basin in the summer of 2012. Non-targeted kick-net sampling at Playgreen Lake, located on the Nelson River approximately 27 km north of the Lake Winnipeg outlet in August of 2012, confirmed the rapid northward expansion of Bythotrephes through Lake Winnipeg. This represents the first evidence for further downstream dispersal. However, as of August 2015, multiple kick- net and Ekman/Ponar grab samples from Cross and Sipiwesk lakes further downstream on the Nelson River have not captured any Bythotrephes. Key words: aquatic invasive species, invasive crustacean, rivers, lakes, Lake Winnipeg, drift density

Introduction Bythotrephes habitat (MacIsaac et al. 2000). North- American lakes that support Bythotrephes popula- The spiny water flea Bythotrephes longimanus tions were significantly larger, and had higher mean (Leydig, 1860), hereafter referred to as Bythotrephes, and maximum depths than those that did not; though is native to large areas of Eurasia (Grigorovich et al. Secchi disk transparency, which was one of the main 1998; Strecker 2011), where it continues to expand variables separating lakes with (mean of 4.7 m) and its range (e.g., Ketelaars and Gille 1994), including without (1.7 m) Bythotrephes in Eurasia, did not into waterbodies not considered typical, high quality significantly differ between the respective groups of

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North American lakes (MacIsaac et al. 2000). The Material and methods presence of a low-light refuge from fish predation may also be important for the successful establish- Collections of Bythotrephes came from targeted and ment of Bythotrephes in a lake (Branstrator et al. 2006; non-targeted sampling for the species. All captures Young et al. 2009). of Bythotrephes from locations outside of Lake The dispersal mechanism(s) of Bythotrephes are Winnipeg originated from non-targeted sampling not fully understood, but transport of resting eggs that was primarily designed to capture fish early life within sediments and ballast water of large ships are stages with large drift traps, and/or benthic inver- likely important pathways. Ballast water transport tebrates with Ponar or Ekman samplers (henceforth has been postulated as the invasion vector for referred to as grab samples) and by kick-netting. Bythotrephes into North America (Sprules et al. 1990), Non-targeted sampling for Bythotrephes within Lake where it was first recorded in Lake Ontario in 1982 Winnipeg included open water sampling of live indi- (Johannsson et al. 1991). Over the next five years, viduals with kick-nets and grab samples. In addition, Bythotrephes spread throughout the remaining Lauren- Bythotrephes was documented from the diet analysis tian Great Lakes (Bur et al. 1986; Evans 1988; Cullis of two zooplanktivorous fish species in Lake Winnipeg and Johnson 1988). By 1989–1991, Bythotrephes had captured by trawling at several locations in the South invaded inland lakes in southern Ontario, Canada basin of the lake (Olynyk 2013). Once Bythotrephes (Yan et al. 1992) and in northern Minnesota, USA was documented from Lake Winnipeg in 2011, (Schuldt and Merrick, pers. comm. in Yan et al. systematic and targeted sampling of the species in 1992). As of 2015, Bythotrephes had been identified the lake was conducted with plankton nets starting in from 179 inland lakes in Ontario (Azan et al. 2015). the summer of 2012. Invasions of Bythotrephes have caused changes in Drift traps were deployed yearly between 2007 and 2012 with the exception of 2011. Traps consisted lake zooplankton communities, such as reduced 2 diversity, abundance, and biomass (Yan et al. 2002; of a stainless steel frame with a 43 × 85 cm (0.3655 m ) Boudreau and Yan 2003; Barbiero and Tuchman opening attached to a 3 m long, 0.95 mm mesh bag 2004; Kerfoot et al. 2016), and the displacement of and a 9 cm diameter cod end with 0.95 mm mesh native taxa (Weisz and Yan 2011). Bythotrephes also screen. Traps were deployed as pairs of surface has been deemed responsible for ecosystem effects (surface to 0.4 m depth) and bottom (4–13 m depth, such as lower epilimnetic zooplankton productivity depending on the depth of the water column) traps at (Strecker and Arnott 2008) and reduced fish growth several locations in the Winnipeg River upstream (Feiner et al. 2015). Some changes in ecosystem (maximum distance 2.8 km) and downstream (0.7 km) function associated with high Bythotrephes abun- of the Pointe du Bois Hydroelectric Generating Station dance have been linked to reduced ecosystem services, (GS). Traps were sampled after 24-hours. In situ and economic losses amounting to approximately 100 water velocity was measured at set and at pull of million US dollars for a single lake (Walsh et al. 2016). each trap and was averaged for the calculation of Bythotrephes was first documented in the Lake drift density (see below). Velocity at the mouth of Winnipeg watershed at Saganaga Lake, Ontario in surface traps was measured using a Swoffer Model 2100 current velocity meter, and an AA Price-Type September of 2003 (USGS 2016a), and thereafter in Model 6200 current meter was used for bottom several other northern Minnesota and northwestern traps. After the presence of Bythotrephes in the Ontario lakes (Branstrator et al. 2006; Kerfoot et al. Winnipeg River was confirmed from samples collec- 2016). In August 2007 the species was recorded ted in 2009, quantitative counts of Bythotrephes in approximately 350 km to the west of Saganaga Lake drift trap catches were obtained in 2010 and 2012. in Lake of the Woods (USGS 2016b), the source of Because early instars of Bythotrephes may evade a the Winnipeg River (Figure 1). No barriers exist for net with 0.95 mm mesh size, the counts (and resulting the natural dispersal of Bythotrephes from Lake of the drift densities) are not fully quantitative, and represent Woods down the Winnipeg River into Lake Winnipeg a conservative estimate. In 2010, drift was collected and further into the Nelson River. Thus, downstream at three sites downstream of the Pointe du Bois GS expansion of the invader from Lake of the Woods on 1 June, and at two sites upstream of the station on was to be expected. 9 June. In 2012, drift was collected at the same We report here on the first records of Bythotrephes locations as in 2010, with an increase in the number in Manitoba, its rapid expansion throughout Lake of traps and consecutive sets to three 24-hour Winnipeg, the 10th largest lake in the world by surface periods from 3–8 June. area, and further downstream into the upper reaches Grab samplers consisted of petite Ponar and Ekman of the Nelson River. samplers, both measuring 0.15 × 0.15 m (0.0225m2).

288 Geographic expansion of Bythotrephes longimanus in Manitoba

Figure 1. Invasion history of the spiny water flea Bythotrephes longimanus in Manitoba waterbodies from non-targeted sampling. Years indicate the first record at a location. Note that targeted sampling in 2012 documented B. longimanus in Lake Winnipeg just south of Mossy Bay (see Figure 2). The first record within the Lake Winnipeg watershed was in 2003 in Saganaga Lake, Ontario (350 km east of Lake of the Woods).

Samplers were deployed to collect benthic sediment was conducted at 65 sites, 26 in the South basin, 12 in water depths of 5–10 m; Ponar samplers over coarse in the Narrows, and 25 in the North basin, including substrates (e.g., gravel and cobble), and Ekman one site (NWL) where the lake outflow creates the samplers over soft substrates (e.g., sand and clay). Nelson River (Figure 2). At each sampling site, two The kick-net had a 0.5 m long bag (400 µm mesh) vertical zooplankton hauls were taken by pulling a with a cod end and was used to kick and sweep the conical zooplankton net with 25 cm diameter and substrate along perpendicular transects from the 76 µm mesh size through the water column, starting shoreline up to 1 m water depth. At each sampling approximately 2 m off the lake bottom, as determined location, 15 grabs and 15 kick-nets were executed, by an International Offshore model Datamarine depth three of which were combined to create a total of finder. The two vertical hauls at each site were five replicate grab or kick-net samples. Grab and combined into a composite sample. Density (indivi- kick-net sampling at Pointe du Bois was conducted duals/m3) of Bythotrephes at each station was in the forebay, approximately 11 and 8 km upstream determined from total volume of water filtered. of the station, respectively; grab sampling started in Plankton net samples were preserved in 70% ethanol. 2009, kick-net sampling in 2010. Grab, kick-net and drift trap samples were Targeted sampling of Bythotrephes in Lake preserved in 4% formaldehyde solution. Ekman and Winnipeg was conducted in 2012 during the summer Ponar samples were processed using sieves with (13 July–9 August) and fall (13 September–10 October) 500 µm mesh. Drift samples were divided into sub- cruises of the research vessel “Namao” operated by samples using a Folsom Plankton Splitter. Each the Lake Winnipeg Research Consortium. Sampling fraction was sorted until 300 organisms were counted.

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Figure 2. Distribution and density of Bythotrephes longimanus in Lake Winnipeg based on ship-based pelagic plankton tows at 65 sites in the summer (13 July–9 August) and fall (13 September–10 October) of 2012; three lake areas are separated by lines; n = number of individuals.

290 Geographic expansion of Bythotrephes longimanus in Manitoba

Table 1. Location and information for chronological sample collections in three waterbodies with indication of presence of Bythotrephes longimanus. Samples were collected from 2007 to 2015, however, Bythotrephes was not detected until 2009. Numbers in parentheses indicate sample size for each gear type. Bythotrephes Waterbody Location1 Sample Date Sampling Gear2 Presence Winnipeg River downstream of the PDB GS 18 July, 2009 BDT (18) yes Winnipeg River Lac du Bonnet 17 September, 2009 GRAB no Winnipeg River upstream of the PDB GS 18 September, 2009 GRAB no Winnipeg River upstream of the PDB GS 8 June, 2010 SDT (1,092) + BDT (14)) yes Winnipeg River downstream of the PDB GS 10-11 June, 2010 SDT (12,590) + BDT (185) yes Winnipeg River Lac du Bonnet 14 September, 2010 KN + GRAB no Winnipeg River upstream of the PDB GS 15 September, 2010 KN + GRAB no Winnipeg River upstream of the PDB GS 15 September, 2011 KN (5)+ GRAB (4) yes Winnipeg River Lac du Bonnet 17 September, 2011 KN (1) yes Winnipeg River downstream of the PDB GS 3-5 June, 2012 SDT (76) + BDT (108) yes Winnipeg River upstream of the PDB GS 5-8 June, 2012 SDT (2,021) + BDT (9) yes Winnipeg River upstream of the PDB GS 10 September, 2012 KN + GRAB no Winnipeg River Lac du Bonnet 11 September, 2012 KN + GRAB no Winnipeg River upstream of the PDB GS 17 September, 2013 KN no Winnipeg River Lac du Bonnet 18 September, 2013 KN + GRAB no Winnipeg River upstream of the PDB GS 6 September, 2014 KN + GRAB no Winnipeg River Lac du Bonnet 7 September, 2014 KN + GRAB no Winnipeg River Lac du Bonnet 1 September, 2015 KN + GRAB no Winnipeg River upstream of the PDB GS 2 September, 2015 KN + GRAB no Lake Winnipeg Mossy Bay 20, 22 August, 2013 KN + GRAB no Lake Winnipeg Mossy Bay 26 August, 2014 KN (1,139) yes Lake Winnipeg Mossy Bay 27 August, 2015 GRAB (1) yes Nelson River Playgreen Lake 27-28 August, 2009 GRAB no Nelson River Cross Lake 14 August, 2012 KN + GRAB no Nelson River Playgreen Lake 16 August, 2012 KN (230) yes Nelson River Cross Lake 27 August, 2013 KN + GRAB no Nelson River Cross Lake 27 August, 2014 KN + GRAB no Nelson River Sipiwesk Lake 21 August, 2014 KN + GRAB no Nelson River Playgreen Lake 26 August, 2015 KN (4) + GRAB (4) yes Nelson River Cross Lake 28 August, 2015 KN + GRAB no 1 PDB GS= Pointe du Bois Generating Station. 2 Surface drift traps (SDT); bottom drift traps (BDT); kick-net (KN); Ponar or Ekman benthic samplers (GRAB).

When the 300 organism count was achieved, the analysis. As data failed to meet normality and/or remaining organisms were counted so that a known homogeneity of variance assumptions, differences in fraction of the original sample was completely sorted. densities between upstream and downstream locations, Total abundance of Bythotrephes for the whole sample surface and bottom traps and between years were was estimated by multiplying the split factor by the ascertained by Kruskal-Wallis one-way analysis on number of individuals counted in the split portion(s). ranks. All analyses were conducted using the Drift densities (individuals/100 m3) were calculated SigmaPlot 11.0 statistics package. for each drift trap set based on the sampling area of the trap, the duration of the set, and the average water Results velocity (m/s) following the formula: Drift density = n × 100/(t × a × v), where: n = number of individuals; t Occurrence and geographical expansion = set duration in seconds, a = mouth area of sampler of Bythotrephes (0.3655 m2), and v = water velocity in meter per second. Mean drift densities did not differ statistically Bythotrephes was recorded for the first time in the for locations upstream and downstream of the Pointe province of Manitoba on 18 July, 2009 when 18 du Bois GS in 2010 (Kruskal-Wallis test, H = 0.54, individuals were recovered from a bottom drift trap df = 1, P = 0.56) and 2012 (Kruskal-Wallis test, H = set at the Pointe du Bois GS on the Winnipeg River 0.87, df = 1, P = 0.35) and were pooled for further (Table 1; Figure 1). This location is approximately

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260 km downstream of the south end of Lake of the approximately 27 km north of the outlet of Lake Woods, where Bythotrephes was reported in the summer Winnipeg (Figure 1), in each of five kick-net samples of 2007 (Figure 1). Grab samples taken upstream of collected on 16 August 2012. Per sample abundance the station on 18 September 2009 did not yield any was variable but generally high, ranging from 6 to 112 Bythotrephes (Table 1). In June of 2010, several individuals. Previous kick-net and grab sampling at thousand individuals of the invader were obtained Playgreen Lake in August 2009 had not resulted in from drift trap captures (Table 1). Again, no any captures of Bythotrephes (Table 1). Bythotrephes were found in the kick-net and grab Non-targeted sampling also confirmed expansion samples taken in the Pointe du Bois forebay on 15 of Bythotrephes into the north end of the North basin September, 2010. Drift trap sampling was not of Lake Winnipeg. On 26 August, 2014 relatively conducted in the Winnipeg River in 2011. However, large numbers of Bythotrephes (n = 133–286 indivi- small numbers of Bythotrephes were recorded from duals) were obtained in the five kick-net samples the kick-net (5 individuals) and grab (4 individuals) taken from Mossy Bay (Figure 1; Table 1). In 2015, samples taken in the Pointe du Bois reservoir on 15 small numbers (1 to 4 individuals) of Bythotrephes September (Table 1). On 17 September 2011, a were again collected in grab and kick-net samples at single Bythotrephes was found in a kick-net sample sites located in Lake Winnipeg (Mossy Bay) and from the Winnipeg River at Lac du Bonnet, Playgreen Lake (Table 1). No Bythotrephes were found approximately 70 km downstream of Pointe du Bois in kick-net and grab samples conducted further down- GS (Figure 1), where the species had not been stream on the Nelson River at Cross and Sipiwesk documented in kick-net or grab samples in the lakes between 2012 and 2015 (Table 1; Figure 1). previous two years (Table 1). Also in 2011, several Bythotrephes were retrieved from the stomach of Densities of Bythotrephes at Pointe du Bois GS eight cisco (Coregonus artedi La Sueur, 1818) and in Lake Winnipeg captured in the summer (1 August) and fall (27–28 September) from three locations (Stn 9, Stn W11, Stn The drift traps set in the Winnipeg River at Pointe du 6), in Lake Winnipeg close to the mouth of the Bois in 2010 and 2012 that were counted Winnipeg River, approximately 55–60 km downstream quantitatively for Bythotrephes provided some of Lac du Bonnet (Figures 1 and 2, Table S1). indication of the number of individuals present in the These findings represented the first confirmation of surface and bottom layers of the water column. Drift the presence of Bythotrephes in Lake Winnipeg and densities varied between 0 and 22.3 individuals/100 m3 show that the invader had become part of the local for the 69 samples taken from five sites located food web. On September 25 and 27, 2011, four upstream and downstream of the Pointe du Bois GS Bythotrephes were caught with plankton nets in the (Table 2), representing up to 10,800 Bythotrephes in open water of Lake Winnipeg, very close to where a 24 hour net set. The mean density of surface traps some of the cisco were captured (Manitoba Sustainable was significantly higher than that of bottom traps in Development, AIS Program, pers. comm., January 17, both years (Kruskal-Wallis test, H = 14.6, df = 1, P < 2017). 0.001), and the mean surface density in 2010 was The targeted sampling in the summer and fall of significantly higher than in 2012 (Kruskal-Wallis test, 2012 confirmed the incidental records of 2011 and H = 5.01, df = 1, P = 0.025; Table 2). The clearly demonstrated the rapid expansion of Bytho- relationship between drift density and water velocity trephes in Lake Winnipeg. In July and August, the was explored for surface traps. In 2012, when species was found most abundantly near the bay at velocities averaged 0.37 m/s (range: 0.06–0.75 m/s), the mouth of the Winnipeg River, but also occurred Bythotrephes was not found in traps set in areas where in most areas of the South basin (Figure 2; Table velocities exceeded 0.3 m/s (Figure 3). However, in S2). Bythotrephes was also captured at one site in 2010, when the only four available trap sets were the south end of the Narrows during summer, but not associated with higher velocities (mean: 0.95 m/s, at any sampling site further north. The fall sampling range: 0.27–1.32 m/s) compared to 2012, drift densities approximately two months later, showed that of 5.4 and 23.3 individuals/100 m3 were recorded at Bythotrephes had dispersed throughout the Narrows velocities of 1.0 and 1.3 m/s, respectively. and had colonized most of the North basin; no Densities of Bythotrephes based on vertical individuals were captured at the single sites in plankton tows from Lake Winnipeg in 2012 were Mossy Bay near the north shore and the lake outflow also highly variable, ranging from 0 to 93.1 and 0 to forming the Nelson River in 2012 (Figure 2). However, 39.2 individuals/m3 among sites for the summer and in the same year, Bythotrephes was found further fall sampling, respectively. Considering the three downstream in the Nelson River at Playgreen Lake different regions of the lake, the highest mean density

292 Geographic expansion of Bythotrephes longimanus in Manitoba

Figure 3. Relationship between drift density of Bythotrephes longimanus and water velocity for surface drift traps (see photo insert) deployed in the Winnipeg River at Point du Bois from 3–8 June, 2012; n = number of individuals.

3 (9.2 ± 3.7 individuals/m ; mean ± SE) was observed Table 2. Drift density (no. of individuals/100 m3) of Bythotrephes for the South basin in the summer, largely driven by longimanus in surface and bottom drift traps set in the Winnipeg five sites with densities of ≥ 25 individuals/m3 River at Pointe du Bois in 2010 and 2012; SE = standard error of (Figure 2). Mean densities in the fall were similar the mean, N = number of samples. 3 among regions, 3.4 ± 1.4 individuals/m in the South 2010 2012 basin, 2.2 ± 0.7 individuals/m3 in the Narrows, and Statistic Surface Bottom Surface Bottom 3.4 ± 1.8 individuals/m3 in the North basin. Only one site each in the North and South basin had a density Mean 8.1 0.17 1.5 0.03 exceeding 30 individuals/m3 (Figure 2). SE 5.2 0.12 0.4 0.01 Range 1.0–22.3 0.01–0.65 0–9.4 0–0.25 Discussion N 4 5 30 30 While drift net and benthic grab sampling at Pointe du Bois in the Winnipeg River started in 2007, Bythotrephes was not detected until 18 July, 2009. Considering an average current speed of the These results suggest that Bythotrephes had expanded Winnipeg River of 0.3 m/s, individuals that stay its distribution from Lake of the Woods (where first entrained in the main flow would reach Lake Winnipeg detected in August of 2007) into the Winnipeg River from Pointe du Bois within 5 days. Thus, the presence to Pointe du Bois as early as the spring of 2009. An of Bythotrephes in the diet of cisco captured in Lake earlier year for this expansion is unlikely based on Winnipeg near the mouth of the Winnipeg River the absence of Bythotrephes in the drift samples starting in early August of 2011, i.e. more than two from the previous two summers. Although Bytho- years after first detection approximately 140 km trephes are difficult to detect at low densities (Mills upstream in the Winnipeg River, is not surprising. It et al. 1992), it seems unlikely that they would have is likely that the earliest records of Bythotrephes been absent in drift traps filtering hundreds of thou- from Lake Winnipeg postdate the expansion of the sands of cubic meters of water and set at locations invader into the lake by some time. This conclusion suitable for capturing the species in large numbers in is indirectly supported by observations that selection 2010 and 2012. From Pointe du Bois, the invader of Bythotrephes by cisco increases once the species seems to have rapidly expanded its distribution down- becomes abundant (Young et al. 2009). Furthermore, stream via the Winnipeg River into Lake Winnipeg. results from ship-based zooplankton net tows at

293 W. Jansen et al. several sites indicate that Bythotrephes occurred in Mendota in Wisconsin (USA) using a combination the South basin of Lake Winnipeg at low abundance of standard 30-cm diameter and larger 50-cm (2 individuals in each of two samples) and very close diameter nets. Barbiero and Tuchman (2004) recorded to the mouth of the Winnipeg River by the end of an average summer density for years 1986–1999 of September 2011 (Manitoba Sustainable Develop- 41 individuals/m3 and 32 individuals/m3 in the ment, AIS Program, pers. comm., January 17, 2017). central and eastern basins of Lake Erie, and 13 and This post-dates our first record for the South basin 10 individuals/m3 in Lakes Huron and Michigan from cisco stomach content by approximately two respectively. These estimates are based on 50-cm months. In the summer (late July) of 2012, we found diameter and 64 μm mesh nets (1986–1996) and Bythotrephes in plankton tows at the southernmost since 1997 using 153 μm mesh nets. Lower densities of 12 locations in the Narrows between the north and of 1–13 individuals/m3 sampled using a 75-cm dia- the South basins of Lake Winnipeg, and by mid- meter net with 285 μm mesh were reported for 17 September of 2012, the invader was first detected in Canadian Shield lakes approximately 10 years after the North basin of the lake. their invasion by Bythotrephes (Boudreau and Yan Bythotrephes are reliably captured in standard 2003). The relatively low densities of Bythotrephes plankton tows except when their abundance is very in Lake Winnipeg may be indicative of its recent low (Boudreau and Yan 2004). However, plankton invasion and densities are expected to increase in the tows sample a much lower volume than drift traps future, at least in some parts of the lake. However, and, therefore, false negatives are more likely to we acknowledge that the low densities may, in part, occur with plankton tows. Hence, the invader may be a consequence of using the standard zooplankton have reached the lake almost two years prior to first net instead of a modified Bythotrephes-specific net detection in 2011, but abundance seems to have and of sampling only during the day (Yan and remained low with a distribution largely restricted to Pawson 1997; Armenio et al. 2017). the area close to the Winnipeg River mouth. Popula- Although the number of Bythotrephes collected tion densities would have increased as a consequence from kick-net sampling at Mossy Bay varied sub- of continuous seeding from the river and repro- stantially between 2014 and 2015, the more than duction within the lake during the summer and fall 1100 individuals obtained from the five samples in of 2010 and 2011 in a similar manner as described 2014 suggest a high abundance of the invader in the by Sprules et al. (1990) for the Laurentian Great Lakes. North basin of Lake Winnipeg. This conclusion is The available evidence suggest that Bythotrephes supported by recent presence-absence data from colonized Lake Winnipeg, which has a surface area zooplankton net tows from identical lake locations as of 24,514 km2 and distance north to south of 431 km, reported here for 2012; Bythotrephes is more probably within two years once population density regularly sampled from the North basin than the near the seeding location had increased over the South basin (Manitoba Sustainable Development, previous two years. This invader expanded its AIS Program, pers. comm., 6 April, 2016). Differen- distribution throughout the Laurentian Great Lakes ces in abundance of the invader between the two (approximately 244,106 km2) within five years of its basins may be expected based on some of their first detection in Lake Ontario, likely aided by secon- limnological characteristics. The South basin is dary intercontinental invasions (Sprules et al. 1990) shallower (mean depth of 9.0 m) and has a lower and dispersal by boats, bait buckets, and other Secchi disk depth (mean of 0.6 m) than the North anthropogenic factors (Weisz and Yan 2010). These basin (depth=13.3 m, Secchi=1.4 m; EC and MWS vectors may have also contributed to the rapid colo- 2011), conditions that are perhaps not conducive to nization by Bythotrephes of the Winnipeg River and high abundances of Bythotrephes. Similar differences parts of Lake Winnipeg. The river and the South in the abundance of Bythotrephes between lake basin of the lake have a relatively high shoreline basins have previously been observed for Lake Erie, coverage with cottages (compared with the North basin), where the invader failed to establish in the more shown to be the strongest predictor of Bythotrephes turbid western basin but thrived in the central and presence in a model that included physical, chemical, the eastern basins (Barbiero and Tuchman 2004). and human use variables (Weisz and Yan 2010). Lake Winnipeg is currently undergoing cultural The mean densities of 2.2–9.2 individuals/m3 for eutrophication (EC and MWS 2011), particularly in plankton net tows from different areas of Lake the South basin, which may further reduce water Winnipeg are similar, but at the lower end of ranges clarity. Bythotrephes declined in Lago Maggiore of densities reported from plankton net tows at other (Italy) as the lake experienced eutrophication and lakes in North America. Walsh et al. (2016) reported increased in abundance subsequent to lake re-oligo- fall densities of > 150 individuals/m3 from Lake trophication (Manca and Ruggiu 1998). Thus, unless

294 Geographic expansion of Bythotrephes longimanus in Manitoba nutrient loads (particularly phosphorus) into the lake The invasion of Bythotrephes has been associated (particularly the South basin) are reduced in the with alterations of the zooplankton community, such future, higher abundances of Bythotrephes may be as displacement of native taxa (Weisz and Yan 2011) limited to the North basin of Lake Winnipeg. and lower diversity, abundance, and biomass (Yan et Bythotrephes has invaded the upper reaches of the al. 2002; Boudreau and Yan 2003; Barbiero and Nelson River, and its further downstream dispersal Tuchman 2004). At the ecosystem level, Bythotrephes along the approximately 410 km of river to the has been associated with reduced fish growth (Feiner estuary into Hudson Bay seems inevitable. Over this et al. 2015) and lower epilimnetic zooplankton course the Nelson River widens into several riverine productivity (Strecker and Arnott 2008), resulting in lakes and is regulated by six hydroelectric generating a reduction in the availability of zooplankton biomass stations with associated reservoirs. However, kick- as prey for planktivorous fish (Foster and Sprules net and grab samples taken at two of the lakes (Cross 2009; Walsh et al. 2016). Lake Winnipeg has also and Sipiwesk, see Figure 1), approximately 31 and been recently (2013) invaded by the zebra mussel 95 km further downstream on the Nelson River from Dreissena polymorpha (Pallas, 1771). This mollusc Playgreen Lake, respectively, in 2014 and 2015 did is known to alter ecosystem function by, for example, not result in any captures of Bythotrephes. This does increasing water clarity (Geisler et al. 2016) and not necessarily indicate that Bythotrephes has not yet increasing benthic production at the cost of pelagic colonized these waterbodies; instead it may still be production (Johannsson et al. 2000; Rennie and below detection limits. The Nelson River and most Evans 2012; Higgins et al. 2014). With both these of its lake expansions and reservoirs may be a habitat keystone invaders expanding throughout the lake at less suited for abundant populations of Bythotrephes; the same time, the ecosystem of Lake Winnipeg (and the water is generally turbid with mean Secchi downstream habitats) will likely undergo some rapid depths of 0.3–0.8 m, only occasionally reaching and profound changes over the next decade. Because Secchi depths of 1.9–2.4 m in some waterbodies, as of the complexity of potential physical and measured during summer and fall of 2008–2010 biological interactions, the direction and magnitude (CAMP 2014). Bythotrephes mainly occurs in large, of these changes are difficult to predict. For example, deep, and clear lakes (MacIsaac et al. 2000; Branstrator Dreissena may actually increase water clarity in Lake et al. 2006), likely reflecting its strong reliance on Winnipeg, particularly in the South basin, despite visual feeding (Pangle and Peacor 2009; Jokela et al. opposing trends due to eutrophication, thus creating 2013). habitat conditions that would favor higher Bythotrephes The absence of Bythotrephes in several grab and abundance. Synergistic negative effects of Bythotrephes kick-net samples at locations in the Winnipeg River and Dreissena on zooplankton abundance and in years when drift trap sampling resulted in substan- production (Azan et al. 2015; Walsh et al. 2016) may tial catches of the invader indicated that the benthic make it difficult to predict consequences on the samplers and kick-nets used in our study may have a planktivorous fish community, including young-of- reduced probability of capturing Bythotrephes, the year fishes (Vanderploeg et al. 2012; Azan et al. particularly at low abundances. The latter two 2015), as well as other foodweb interactions. capture methods are not used for targeted sampling of Bythotrephes and we found no other published Acknowledgements studies with information on their capture success. The authors would like to acknowledge Manitoba Hydro and However, the first record of Bythotrephes in Manitoba Sustainable Development for financial support through the Manitoba, its first occurrence in Lake Winnipeg, and Pointe du Bois Generating Station Spillway Replacement Project and the further northward dispersal of the invader was the Coordinated Aquatic Monitoring Program. We thank Alicia Ali, Michael Alperyn, Jesse Bell, Julie Brunel, Duncan Burnett, Alix documented using methods that did not specifically Cameron, Don Cobb, Kathleen Dawson, Sarah Garner, Doug Gibson, target the species. While allowing only limited Mark Gillespie, Claire Hrenchuk, Susan Hertam, Mike Legge, Kim estimates on the abundance or density of Bythotrephes, Mandzy, Yhana Michaluk, Joe Mota, Lee Murray, Andrew Olynyk, these methods provided critical information on the Darcy Pisiak, Allan Schmidt, Natalia Waldner for their assistance during field and laboratory work, and Candace Parker for creating the geographical distribution of this ecologically and maps. Manitoba Sustainable Development (AIS Program) kindly economically important invasive species covering a provided data on Bythotrephes densities in Lake Winnipeg for 2012. distance along the invasion route of more than 600 The Lake Winnipeg Research Consortium generously provided space km. These findings emphasize the important contri- and time on the research vessel ‘Namao’. North/South Consultants Inc provided financial support for publishing this paper. Wolfgang bution of non-targeted sampling methods for the Jansen presented partial results of this paper at the 19th International early detection of aquatic invasive species, potentially Conference on Aquatic Invasive Species. We thank Mike Rennie, allowing for a timely implementation of management Ashley Elgin, and two anonymous reviewers for their constructive strategies. suggestions on an earlier draft of the manuscript.

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Supplementary material The following supplementary material is available for this article: Table S1. Geo-referenced (decimal degrees), chronological record data for Bythotrephes longimanus for Manitoba waterbodies from 2009–2015 (see Table 1); for locations within Lake Winnipeg also see Figure 2; PDB= Pointe du Bois; LdB= Lac Du Bonnet; Stn= Station. Table S2. Geo-referenced (decimal degrees) record data for Bythotrephes longimanus for plankton net sampling sites from three areas of Lake Winnipeg in summer and fall 2012 (see Figure 2). This material is available as part of online article from: http://www.aquaticinvasions.net/2017/Supplements/AI_2017_Jansen_etal_Supplement.xls

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