Diet and habitat use by age-0 deepwater sculpins in northern Lake Huron, Michigan and the Detroit River

JGLR-00607; No. of pages: 8; 4C: Journal of Great Lakes Research xxx (2013) xxx–xxx

Contents lists available at ScienceDirect

Journal of Great Lakes Research journal homepage: www.elsevier.com/locate/jglr

Diet and habitat use by age-0 deepwater sculpins in northern Lake Huron, Michigan and the Detroit River Edward F. Roseman ⁎ USGS Great Lakes Science Center, 1451 Green Road, Ann Arbor, MI 48105, USA

a r t i c l e

i n f o

Article history: Received 26 February 2013 Accepted 2 July 2013 Available online xxxx Communicated by John Martin Farrell Index words: Myoxocephalus thompsonii Deepwater sculpin Lake Huron Detroit River Diet

a b s t r a c t Deepwater sculpins (Myoxocephalus thompsonii) are an important link in deepwater benthic foodwebs of the Great Lakes. Little information exists about deepwater sculpin spawning habits and early life history ecology due to difficulty in sampling deep offshore habitats. Larval and age-0 deepwater sculpins collected in northern Lake Huron and the Detroit River during 2007 were used to improve our understanding of their habitat use, diet, age, and growth. Peak larval density reached 8.4/1000 m3 in the Detroit River during April and was higher than that in Lake Huron. Offshore bottom trawls at DeTour and Hammond Bay first collected benthic age-0 deepwater sculpins in early September when fish were ≥25 mm TL. Otolith analysis revealed that hatch dates for pelagic larvae occurred during late March and larvae remained pelagic for 40 to 60 days. Diet of pelagic larvae (10–21 mm TL) was dominated by calanoid copepods at all sample locations. Diets of benthic age-0 fish varied by location and depth: Mysis and chironomids were prevalent in fish from Hammond Bay and the 91 m site at DeTour, but only chironomids were found in fish from the 37 m DeTour site. This work showed that nearshore epilimnetic sites were important for pelagic larvae and an ontogenetic shift from pelagic planktivore to benthivore occurred at about 25 mm TL in late summer. Age analysis showed that larvae remained pelagic long enough to be transported through the St. Clair–Detroit River system, Lake Erie, and the Niagara River, potentially contributing to populations in Lake Ontario. Published by Elsevier B.V. on behalf of International Association for Great Lakes Research.

Introduction Due to challenges associated with sampling fishes in deep offshore habitats of the Great Lakes, population dynamics and ecology of Great Lakes' deepwater sculpin (Myoxocephalus thompsonii) are not well studied except for insights provided by annual indices of abundance from agency trawl surveys (e.g. Gorman et al., 2012; Madenjian et al., 2012; Riley et al., 2012; Weidel et al., 2012) and, using samples from these surveys, occasional glimpses at adult feeding ecology (described below). Even less studied and understood are dynamics of deepwater sculpin early life history stages including the distribution and feeding ecology of larvae. Examples of the few deepwater sculpin early life history studies include examinations of abundance and distribution in Lake Michigan (Geffen and Nash, 1992; Mansfield et al., 1983) and inshore– offshore distribution in Lake Superior (Oyadomari and Auer, 2004). Geffen and Nash (1992) included estimates of larval growth and survival and speculated on sources of larval mortality that included predation. Using indices of annual abundance from bottom trawls and bioenergetics models, Madenjian et al. (2005) found that alewife (Alosa pseudoharengus) and burbot (Lota lota) predation were important in structuring Lake Michigan deepwater sculpin populations and concluded that control of the alewife population was a prerequisite ⁎ Tel.: +1 734 214 7237. E-mail address: [email protected].

for recovery of deepwater sculpin populations. Similarly, Brandt (1986) and Wells and McLain (1973) suggested that alewife were a major predator on deepwater sculpin larvae. In Lake Huron, abundance of alewives declined to low levels in 2004 and remained low through 2011 (Riley et al., 2012; Roseman and Riley, 2009). During this period, deepwater sculpin abundance continued to decline (O'Brien et al., 2009; Riley et al., 2008) possibly due to predation by an expanding lake trout (Salvelinus namaycush) population in Lake Huron (Riley et al., 2007) or other foodweb changes. While predation on larvae may be influential, competition for food resources may also limit deepwater sculpin abundance. For example, coincident with the decline of deepwater sculpins, benthic macroinvertebrate abundance declined (French et al., 2009; Nalepa et al., 2007; Pothoven et al., 2011), quagga mussel (Dreissena rostriformis bugensis) abundance and distribution increased (Nalepa et al., 2007), and round goby (Neogobius melanostomus) distributions expanded to deeper waters (Riley et al., 2008; Schaeffer et al., 2005). These factors in concert suggest that competition for limited food resources may have contributed to the decline of deepwater sculpins in addition to predation. Diets of large age-0 (≥40 mm TL) and adult deepwater sculpin have been documented in Lake Michigan (Hondorp et al., 2011; Kraft, 1977; Wells, 1980; Wojcik et al., 1986), Lake Superior (Selgeby, 1988), Lake Ontario (McAllister, 1961), and some interior lakes in Canada (Black and Lankester, 1981; Dymond, 1926; McPhail and Lindsey, 1970).

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.2013.07.004

Please cite this article as: Roseman, E.F., Diet and habitat use by age-0 deepwater sculpins in northern Lake Huron, Michigan and the Detroit River, J Great Lakes Res (2013), http://dx.doi.org/10.1016/j.jglr.2013.07.004

2

E.F. Roseman / Journal of Great Lakes Research xxx (2013) xxx–xxx

Recent studies of adult deepwater sculpin feeding have focused on Lake Michigan (Davis et al., 2005; Hondorp et al., 2005) and Lake Huron (O'Brien et al., 2009). Nearly all of these studies showed that deepwater sculpins relied heavily on Diporeia, Mysis diluviana (hereafter Mysis), chironomids, and to a lesser extent, other benthic invertebrates and fish eggs. Diet preferences of larval deepwater sculpin are understudied as no published reports on their feeding ecology were found. However, it is assumed that, like most pelagic larval fishes in the Great Lakes, deepwater sculpin larvae are zooplanktivorous. Zooplankton communities in offshore waters of Lake Huron have decreased in diversity and biomass, as recently noted by a 90% decrease in non-predatory cladoceran and cyclopoid copepod biomass since 2002 (Barbiero et al., 2009). This decline may be due to increased predation pressure by the invasive planktivore Bythotrephes (Bunnell et al., 2011) in conjunction with a decline in phytoplankton biomass following the introduction of dreissenid mussels (Barbiero et al., 2009; Nalepa et al., 2007). These changes in zooplankton community structure may have influenced the prey selectivity of Lake Huron larval fishes underscoring the importance of studies examining diet. Because deepwater sculpin are pelagic (Geffen and Nash, 1992), drift of larvae influences their distribution and overlaps with habitat. Geffen and Nash (1992) observed that larval deepwater sculpins in Lake Michigan hatched in deep water in March, rose to the surface, and were transported inshore. These larvae moved offshore and deeper in the water column after metamorphosis and were benthic by late fall. Densities of pelagic deepwater sculpin larvae were generally higher inshore than offshore near the Keweenaw Peninsula, Lake Superior (Oyadomari and Auer, 2004) and in northern Lake Huron (Roseman and O'Brien, in press). Pelagic deepwater sculpin larvae were collected from the St. Clair–Detroit river system (Hatcher and Nester, 1983; Jude, 1991) and western Lake Erie (Roseman et al., 1998) and these fish were thought to originate in Lake Huron. While adult deepwater sculpins have not been reported from Lake Erie, downstream drift of larvae from the upper Great Lakes remains as a possible source of introduction and may, in part, be responsible for the resurgence of deepwater sculpin in Lake Ontario (Lantry et al., 2007), although recovery of a

DeTour, MI

relict Lake Ontario population is thought to be more likely (M. Walsh, USGS Lake Ontario Biological Station, personal comm.). In this study, I integrate samples and data on pelagic larval and benthic age-0 deepwater sculpin collected during a 2007 study of the northern Lake Huron foodweb (Savino, 2009) and data on pelagic larval deepwater sculpin collected during an inventory of fish nursery areas in the St. Clair and Detroit rivers from 2007 to 2012 to assess their abundance, diet, and age. Using information gleaned from this study, I discuss the importance of Great Lakes coastal zones and connecting channels as habitat for deepwater sculpin, emphasizing the importance of connectivity between inshore and offshore habitats within Lake Huron and via the connecting channels between the upper and lower Great Lakes.

Methods Larval fish collections Samples of larval fish were collected from inshore sites (1–15 m depths) at DeTour and Hammond Bay in northern Lake Huron (Fig. 1) beginning in mid-April 2007 as soon as ice-out occurred and waters were safely navigable with a small vessel (7 m hull length). Daytime collections were made at inshore sites using a 2.0 m2 framed neuston net fitted with 500 μm mesh netting. The neuston net was towed in the upper 2.0 m of the water column for approximately 5 min at a speed of 7.0 km/h at each sample site. Nearshore (37 m) and offshore (91 m) bottom trawl collections were made at night from the R/V Sturgeon once per month during May, June, July, and September 2007 at two sites off the Hammond Bay and DeTour ports (Fig. 1). These sites are standard bottom trawl locations for the Lake Huron forage fish assessment program (Riley et al., 2012). A 3/4 Yankee Standard No. 35 bottom trawl (12-m headrope, 15.5-m footrope, with a 13-mm cod end mesh) towed at 3.5–4.0 km·hour−1 for 10 min was used to collect benthic juvenile deepwater sculpins (Savino, 2009). Fish captured with bottom trawls were sorted and identified on the research vessel then euthanized and preserved in 95% ethanol. Identifications of

Drummond Island

Ontario

Michigan

Lake Huron Hammond Bay

Fig. 1. Deepwater sculpin collection sites in northern Lake Huron showing inshore (● 1–12 m), nearshore (★ 37 m), and offshore (▲ 91 m) locations.

Please cite this article as: Roseman, E.F., Diet and habitat use by age-0 deepwater sculpins in northern Lake Huron, Michigan and the Detroit River, J Great Lakes Res (2013), http://dx.doi.org/10.1016/j.jglr.2013.07.004

E.F. Roseman / Journal of Great Lakes Research xxx (2013) xxx–xxx

age-0 fishes made in the field were confirmed at the laboratory with the aid of a microscope. Larval sampling occurred in the Detroit River from 2007 to 2012 and in the St. Clair River during 2010–2012. Larval sampling began in the Detroit River in mid-March and continued weekly through June. Ichthyoplankton samples were collected at sites in the river upstream of Belle Isle, upstream of the Ambassador Bridge, mid-river across Hennepin Point on the upstream end of Grosse Ile, the lower river crossing the southern tip of Grosse Ile, and in western Lake Erie near the mouth of the Detroit River (Fig. 2). For these weekly collections, I used a paired bongo sampler weighted with a 22.7 kg oceanographic depressor plate and fitted with two 60 cm diameter by 3.3 m long nets with mesh sizes of 333 and 500 μm. A flow meter was positioned in the mouth of each net to estimate the volume of water sampled. The bongo sampler was towed into the current at about 2.0 km/h for 6 min at each site. Samples were collected from the upper 2 m of the water column at all sites and at 6 m depths where water depth was sufficient. For all larval fish collection gear, volume of water sampled by the net was estimated using a flow meter mounted in the mouth of the net. Neuston nets typically sampled 500 m3 of water in a five-minute tow and each bongo net strained about 115 m3 in 5 min. All larval fish samples were euthanized with a lethal dose of tricaine methanesulfonate and preserved and stored in 95% ethanol. At the laboratory, preserved samples were sorted and identified to species according to Auer (1982). Catch data for individual species were converted into abundance estimates (#/1000 m3) to compare relative abundances. Zooplankton Seasonal numeric densities of zooplankton were estimated from 153 μm mesh zooplankton net samples collected at the 3 and 5 m inshore larval fish sites in northern Lake Huron and from the main channel sites in the Detroit River concurrently with larval fish collections. Crustacean zooplankton were sampled with vertical hauls using a 0.5-m-diameter zooplankton net retrieved at a speed of 0.5 m·s−1. A flow meter mounted

3

in the mouth of the net frame provided and estimate of volume sampled. The cod end (cup) of each sample was removed and placed in a bath of effervescent antacid for 2–5 min in order to narcotize the organisms before the contents were transferred to a sample jar and preserved in 5% formaldehyde until laboratory processing. Zooplankton processing followed protocols described by Barbiero and Tuchman (2004). Briefly, the samples were processed until at least 200 individuals were encountered in a known subsample volume. All species were identified following Balcer et al. (1984) and enumerated using a counting wheel and dissecting microscope. The only exception to species-level identification was immature calanoids and cyclopoids, which were identified to suborder or genus. Zooplankton species were grouped into one of five categories: small cladocerans (primarily Bosmina) large cladocerans (primarily Daphnia and Holopedium spp.), cyclopoid copepods (dominated by Diacyclops thomasi [Forbes] and Mesocyclops edax [Forbes]), calanoid copepods (primarily Limnocalanus macrurus [Sars], and Leptodiaptomus spp.), and nauplii. Fish diets For diet analysis, all prey items anterior to the pyloric caecum were identified to genera and enumerated. Stomach contents of individual fish were removed by dissection under a stereoscopic microscope. All zooplankton prey in the stomach were identified and measured as described above using a stereo-microscope and ocular micrometer. Benthic macroinvertebrates were identified to species following Balcer et al. (1984) and Pennak (2001). For partially digested prey items, I considered pairs of eye stalks for Mysis and head capsules of Chironomidae and Diporeia as evidence that one prey item was consumed. I calculated the mean number of organisms per stomach and percent frequency of occurrence (Bowen, 1996). For individual pelagic deepwater sculpin larvae collected at inshore sites in northern Lake Huron, prey electivity was estimated using the Manly–Chesson index, αi, calculated as m X ri =ni αi ¼ ðri =ni Þ= i¼1

where m is the number of prey sizes or species, ri is the proportion of prey i ingested, and ni is the proportion of prey i in the environment (Chesson, 1978; Lechowicz, 1982; Manly, 1974; Vanderploeg and Scavia, 1979). Average αi scores were then calculated for each site/date. For m prey species in a sample, α ≥ 1/m indicates positive selection of species i. Spearman's ranked correlation (Rs) was used to assess the relationships between length of deepwater sculpins and length and number of prey consumed.

Belle Isle

3 sites

Larval age

Fighting Island Lake St. Clair

Grosse Isle

Michigan

Ontario

Lake Erie

Ohio

Daily ages of deepwater sculpin were estimated using sagittal otoliths following protocols described in Secor et al. (1991) and Jones (1986). Otoliths were dissected from fish with the aid of a microscope using cross-polarized light filters and mounted to glass slides using adhesive epoxy. Whole and sanded structures were interpreted with the aid of a compound microscope with variable magnification. Hatch dates were back-calculated assuming daily ring deposition. Otoliths from fish N 18 mm TL and about 60 days of age were difficult to interpret due to close spacing of rings and data from these fish were deemed unreliable and not used in the analyses. Results Larval abundance

Fig. 2. Larval fish collection sites in the Detroit River.

In northern Lake Huron, pelagic deepwater sculpin larvae were found in daytime inshore samples collected at DeTour and Hammond Bay from mid-April through May when water temperatures ranged

Please cite this article as: Roseman, E.F., Diet and habitat use by age-0 deepwater sculpins in northern Lake Huron, Michigan and the Detroit River, J Great Lakes Res (2013), http://dx.doi.org/10.1016/j.jglr.2013.07.004

E.F. Roseman / Journal of Great Lakes Research xxx (2013) xxx–xxx

from 2.5° to 9.0° C. Abundance at inshore sites was higher at DeTour than at Hammond Bay where only one fish was collected. Larval abundance was highest at DeTour during mid-April through late May (0.4–0.6/1000 m3; Fig. 3). Nearshore and offshore bottom trawls at DeTour and Hammond Bay first collected age-0 benthic deepwater sculpins in early September when fish were about 25 mm TL although estimates of their density were not calculated. Bottom water temperatures at all trawl sites ranged from 4.2° to 4.7° C. Similar to observations in northern Lake Huron, pelagic larval deepwater sculpins were found in samples collected from the main channels of the Detroit River from late March through May 2007 when water temperatures ranged from 3.7° to 11.8° C. The highest density was observed during mid- and late-April. Densities of larvae were about an order of magnitude higher in the Detroit River than in northern Lake Huron (Fig. 3). Larval deepwater sculpins also appeared in samples collected from the Detroit River during the spring of 2006 (N = 2) and 2012 (N = 1) and from the St. Clair River in 2010 (N = 3).

35,000 Nauplii

30,000

Large Cladocerans Small Cladocerans

25,000

Density (No./M3)

4

Cyclopoid Calanoid

20,000 15,000 10,000 5,000 0 17-Apr

1-May

15-May

29-May

12-Jun

26-Jun

20-May

30-May

9-Jun

19-Jun

29-Jun

2,000 1,800

Zooplankton

Diet Diets were enumerated for 20 pelagic larvae and 48 demersal age-0 deepwater sculpins collected from northern Lake Huron and 18 pelagic larvae collected from the Detroit River in 2007. All pelagic larvae examined from northern Lake Huron had identifiable food in their stomachs while 14 of the 18 (78%) stomachs examined from the Detroit River had identifiable food. For demersal age-0 deepwater sculpins in northern Lake Huron, all fish collected in bottom trawls from Hammond Bay and the DeTour 37 m site had identifiable remains in their stomachs

Fig. 3. Densities (No./1000 m3) of pelagic deepwater sculpins larvae in the Detroit River (solid line, solid circle) and at DeTour, northern Lake Huron (dashed line, open square) during spring 2007.

1,600 1,400

Density (NO./M3)

Zooplankton abundance was over an order of magnitude higher in northern Lake Huron than in the Detroit River and increased over the course of the spring and summer at both locations (Fig. 4). Densities ranged from about 800/m3 in early May to about 1800/m3 in late June in the Detroit River and from about 2500/m3 in mid-April to about 30,000 m3 in late June in northern Lake Huron. Relative proportions of zooplankton types also varied over time and between sites. The Detroit River community was dominated by copepod nauplii and calanoid copepods throughout the spring and early summer with abundance of small cladocerans peaking during early June. Cyclopoid copepods were present in low abundances throughout the spring and summer and increased in abundance during late June (Fig. 4). In northern Lake Huron, nauplii were the dominant zooplankter throughout the spring and summer with increases in the abundance of small cladocerans, cyclopoid copepods, and calanoid copepods occurring during June (Fig. 4).

1,200 1,000 800 600 400 200 0 10-May

Fig. 4. Mean abundance (No./m3) of crustacean zooplankton collected from inshore sites near DeTour, MI in northern Lake Huron (top panel) and the Detroit River (bottom panel) during 2007.

and 14 of 18 (78%) fish from the DeTour 91 m site contained identifiable food remains. Calanoid copepods were the dominant prey item for pelagic deepwater sculpin larvae in April and early May at both study sites (Table 1). Nauplii were found in stomachs collected from the Detroit River in mid-April and northern Lake Huron during early and late-May. Large cladocerans and rotifers were also eaten by larvae in northern Lake Huron (Table 1). While the size (Fig. 5) and number (Fig. 6) of zooplankton found in pelagic larval deepwater sculpin stomachs tended to increase with larval length at both study sites, these relationships were not statistically significant (Rs b 0.35; p N 0.24). Pelagic larvae collected from northern Lake Huron showed significant positive selection for calanoid copepods during April (αi = 0.85) and May (αi = 0.99) and for cladocerans in April (αi = 0.15; Table 2). In September, the diet of demersal age-0 deepwater sculpins collected in bottom trawls had shifted to Mysis, Diporeia and chironomid larvae, although a few fish continued to feed on calanoid copepods and Bythotrephes (Table 3). Chironomids were the only prey item found in fish collected from the 37 m depth at DeTour, averaging 27.3 midges per stomach. An average of about one Mysis was found in stomachs of deepwater sculpins collected at the 37 and 91 m depths at Hammond Bay and the 91 m depth at DeTour while Diporeia were found in diets of fish from only the two 91 m sites (Table 3). For all fish at all sites, the mean size of Mysis consumed was 7.95 mm carapace length (1.12 standard deviation) and Diporeia averaged 4.17 mm (0.96 standard deviation).

Please cite this article as: Roseman, E.F., Diet and habitat use by age-0 deepwater sculpins in northern Lake Huron, Michigan and the Detroit River, J Great Lakes Res (2013), http://dx.doi.org/10.1016/j.jglr.2013.07.004

E.F. Roseman / Journal of Great Lakes Research xxx (2013) xxx–xxx

5

Table 1 Collection date, site, number collected (N), mean total length (TL), mean number of prey (standard deviation), and percent frequency of occurrence of prey items found in pelagic larval deepwater sculpin stomachs collected from the Detroit River (DR) and northern Lake Huron (LH) during spring 2007. Date

Site

N

TL

Mean number of prey (SD) Calanoid

10 Apr 13 Apr 27 Apr 9 May 17 May 23 May 17 Apr 1 May 15 May 26 May 30 May 27 Jun

DR DR DR DR DR DR LH LH LH LH LH LH

1 4 8 3 1 1 6 5 1 6 1 1

11.4 11.6 15.6 16.4 15.9 19.1 11.0 13.1 15.1 17.1 17.0 21.0

6.0 1.5 (1.7) 1.0 (1.1) 3.3 (2.9) 0.0 2.0 3.3 (1.4) 3.4 (1.9) 5.0 4.2 (1.9)

Cladoceran

% frequency of occurrence Nauplii

Rotifer

100 100 100 100 100

0.1 (0.4) 0.2 (0.5) 0.8 (0.8)

9.0

Cladoceran

100 75 63 66

0.8 (1.5)

1.0

Calanoid

4.0

Nauplii

Rotifer

25

17 20 67 100

100

100

My results demonstrate important ontogenetic diet and habitat shifts for deepwater sculpin in northern Lake Huron. Fish in this study were zooplanktivorous during the pelagic larval stage until they reached a size between 20 and 25 mm TL, occurring around the end of June and early July, when they became demersal and switched to feeding on benthic macroinvertebrates. Geffen and Nash (1992) observed a similar habitat shift for deepwater sculpin at about 25 mm TL, occurring in August– September in Lake Michigan, but did not report on diet. Growth rates for the Lake Michigan fish were lower than those observed in northern Lake Huron and the Detroit River, at only about 0.14 mm/day (Geffen and Nash, 1992). Mansfield et al. (1983) found pelagic deepwater sculpin up to 22 mm TL in samples collected as late as August in southern Lake Michigan. Selgeby (1988) reported the collection of several larval deepwater sculpins ranging in size from 10 to 22 mm TL in the Apostle Islands area of Lake Superior during May 1974. In that same report, he notes that demersal age-0 deepwater sculpin collected in bottom trawls from the

Stockton Island region of Lake Superior averaged 41 mm TL at the end of their first growing season whereas fish that were collected in bottom trawls from northern Lake Huron were somewhat smaller (about 33 mm TL) in the middle of September. Based on results from these studies of larval and age-0 deepwater sculpin in the upper Great Lakes, an ontogenetic shift from pelagic to demersal habitats likely occurs when larvae reach a size of about 25 mm TL. What remains unknown is if fish became demersal before migrating to deep offshore waters or if pelagic larvae drifted offshore, then became demersal. Pelagic larvae in both northern Lake Huron and the Detroit River were exclusively zooplanktivorous, showing a preference for calanoid copepods. While no other diet studies for pelagic deepwater sculpin were available to compare my results to, George et al. (in press) reported that larval burbot L. lota collected from northern Lake Huron during this study (Savino, 2009) ate mostly cyclopoid copepods, followed by copepod nauplii and calanoid copepods. These results concur with George et al. (in press) that recent declines in Lake Huron's cladocerans and cyclopoid copepods (Barbiero et al., 2009) may influence the prey availability and selectivity of larval fishes and represent a potential bottleneck for growth and recruitment. Further examination of larval deepwater sculpin feeding behavior is required to answer important questions related to diet feeding periodicity, prey selection, and larval growth in relation to changing Great Lakes' zooplankton communities and climate. Despite lower zooplankton abundances than observed in northern Lake Huron, larval deepwater sculpins collected from the Detroit River ate similar numbers of copepods as fish in northern Lake Huron. Successful feeding by larval fish in the Detroit River suggests that river habitats are capable of supporting larvae, including transients drifting

Fig. 5. Relationship between size of pelagic larval deepwater sculpins and size of zooplankton prey consumed for fish collected from the Detroit River (filled circles) and northern Lake Huron (open squares) during spring, 2007.

Fig. 6. Relationship between size of pelagic larval deepwater sculpins and total number of prey found in stomachs for fish collected from the Detroit River (filled circles) and northern Lake Huron (open squares) during spring, 2007.

Age and growth Hatch dates for fish from northern Lake Huron and the Detroit River were estimated to occur during the last weeks of March. While larvae from the Detroit River were typically larger than those collected from northern Lake Huron at any given age, no statistically significant differences were found in the relationships between length and age between study locations (Fig. 7; ANCOVA; p = 0.2832). Mean growth rates were 0.21 and 0.18 mm/d for larvae collected from northern Lake Huron and the Detroit River, respectively (Fig. 8). Discussion

Please cite this article as: Roseman, E.F., Diet and habitat use by age-0 deepwater sculpins in northern Lake Huron, Michigan and the Detroit River, J Great Lakes Res (2013), http://dx.doi.org/10.1016/j.jglr.2013.07.004

6

E.F. Roseman / Journal of Great Lakes Research xxx (2013) xxx–xxx

Table 2 Prey selectivity (Manly–Chesson αi) for prey types found in larval deepwater sculpin collected from inshore and offshore sites in northern Lake Huron, 2007. Positive selection (*) is indicated when αi N 1/n, neutral selection when αi = 1/n, and negative selection when αi b 1/n (Vanderploeg and Scavia, 1979). N = number of deepwater sculpin per sample, n = number of prey types. Location

Month

N

1/n

Calanoid

Nauplii

Cladoceran

Rotifer

Inshore

April May

6 6

0.14 0.14

0.85* 0.99*

0.00 0.01

0.15* 0.00

0.00 0.00

downstream from the upper Great Lakes. Poe (1983) examined diets of larval yellow perch (Perca flavescens) from the Detroit River during 1977–78 and found that fish ate primarily calanoid and cyclopoid copepods but larvae collected from the upper river had a higher incidence of feeding than larvae collected in the lower river. He attributed this to gradients in water quality, with lower water quality that occurred downstream affecting fish feeding. McDonald et al. (in press) conducted diet analyses on larval round goby, yellow perch, and bluegill (Lepomis macrochirus) collected from the main channel and embayments of the lower Detroit River during 2007. These fish had high feeding rates and consumed a variety of zooplankton suggesting improved water quality compared to Poe's (1983) results. Deepwater sculpin larvae have been found drifting through the St. Clair and Detroit rivers in a number of studies, which have suggested that deepwater sculpins originated from the Lake Huron population. Hatcher and Nester (1983) reported that deepwater sculpins collected from the St. Clair and Detroit rivers during 1977 were derived from the spawning population in Lake Huron. Similarly, Leslie and Timmins (1991) reported on the collection of deepwater sculpins from the Chematogan Channel (which splits from the South Channel in the St. Clair River and flows between Squirrel and Walpole Islands into Lake St. Clair) and considered these larvae “drifters” from Lake Huron based on the lack of spawning habitat available in the shallow channel. Roseman et al. (1998) and Lantry et al. (2007) concluded that deepwater sculpin found in the Western basin of Lake Erie resulted from downstream transport of the larval fish from the Lake Huron population through the St. Clair and Detroit rivers, and could have possibly made their way to Lake Ontario. While the exact spawning location is unknown, the distance from Lake Huron to Lake Erie through the St. Clair–Detroit River system is 250 km (Roseman et al., 1998). Hatcher et al. (1991) estimated that newly hatched fish from Lake Huron could be transported to Lake Erie within one week. Lantry et al. (2007) found that the larvae near the surface waters of Lake Erie could travel from the mouth of the Detroit River to the head of the Niagara River in a minimum of 35 days. Age data suggest that larval deepwater sculpins were still pelagic between 40 and 60 days of age, adding further evidence to the feasibility of the downstream transport hypothesis. While transport of deepwater sculpin larvae to the deep waters of central and eastern Lake Erie and Lake Ontario is certainly possible, no collections of this species have been reported from Lake Erie (Coldwater Task Group, 2012). In Lake Ontario, however, deepwater sculpins have increased in bottom trawl catches since 2005 after being absent or rare in trawl catches during the 1980s and much of the 1990s. The source of the recent resurgence of deepwater sculpin in Lake Ontario is

Fig. 7. Relationship between age and length for age-0 deepwater sculpins collected from the Detroit River (filled circles) and northern Lake Huron (open squares) during 2007.

speculative because little information exists on spawning habits or habitat requirements or transport of fishes through the Niagara River. Survival of larvae passing over Niagara Falls is currently not quantified, but some fish may survive (see Kapuscinski et al., 2013, for adult muskellunge (Esox masquinongy) example). Fish could also pass from Lake Erie through the Welland Canal into Lake Ontario. The recovery of the Lake Ontario population could be the result of natural reproduction by the remnant population in Lake Ontario, downstream drift of pelagic larvae from Lake Huron, or both (Lantry et al., 2007). Deepwater sculpin are recognized as important prey in Great Lakes foodwebs and vibrant populations are considered necessary for restoration of deepwater foodwebs across the Great Lakes (Zimmerman and Krueger, 2009). Because early life history stages are integral to a species' success, a complete understanding of the ontogenetic feeding ecology, growth, and movement of larval deepwater sculpin could provide insight to the factors that influence population dynamics. The positive selection for calanoid copepods by larval deepwater sculpin and the avoidance of other more abundant prey types observed in this study suggest that deepwater sculpin are relatively inflexible in their prey choices at the larval stage. Determining if this feeding behavior is based on optimal foraging, visual detection ability, or relative abundances of prey types remains speculative given the limited scope and sample sizes of this study. However, if the Lake Huron zooplankton community continues to shift in composition and decline due to Bythotrephes predation (Bunnell et al., 2011) and other food web disruptions caused by invasive species, a decline in abundance of preferred prey for larval deepwater sculpin could occur. A more comprehensive understanding of the effects of invasive species influences on foodwebs and how these interactions affect larval deepwater sculpin and other planktivorous ichthyoplankton is needed to fully evaluate how fish early life history is being affected by invasive species at multiple trophic levels. This study provides new information on the ecology of larval and age-0 deepwater sculpin including the first description of their diet in the Great Lakes. My results emphasize the importance of zooplankton as food for pelagic larvae and document the growth/age when an

Table 3 Collection date, site, number collected (N), mean total length (TL), mean number of prey (standard deviation), and percent frequency of occurrence for prey items found in demersal age-0 deepwater sculpin stomachs collected with bottom trawls from Hammond Bay (HB) and DeTour (DT) in northern Lake Huron during September 2007. Calan is calanoid copepods, Bytho is Bythotrephes, Dipo is Diporeia, and Chiro is chironomid larvae. Date

Site

Depth

N

TL

8 Sep 9 Sep 10 Sep 12 Sep

HB DT DT HB

37 37 91 91

3 13 13 19

27.3 30.1 32.4 33.0

Mean number (SD) Calan

Bytho

% frequency of occurrence Mysis

Dipo

1.0 (0.0) 0.3 (1.1) 0.1 (0.2)

0.1 (0.3) 0.1 (0.2)

1.0 (1.0) 1.1 (0.9)

Chiro

Calan

Bytho

0.3 (0.6) 27.3 (16.8) 0.2 (0.4) 0.7 (1.0)

Mysis

Dipo

100 8 5

8 5

62 68

Chiro 33 100

15 42

Please cite this article as: Roseman, E.F., Diet and habitat use by age-0 deepwater sculpins in northern Lake Huron, Michigan and the Detroit River, J Great Lakes Res (2013), http://dx.doi.org/10.1016/j.jglr.2013.07.004

E.F. Roseman / Journal of Great Lakes Research xxx (2013) xxx–xxx

Fig. 8. Mean length of age-0 deepwater sculpins (±one standard error) collected from the Detroit River (filled circles) and northern Lake Huron (open squares) during spring, 2007.

ontogenetic shift from pelagic zooplanktivore to demersal benthivore occurred. These data will serve as a valuable benchmark for foodweb modelers, researchers, and fisheries managers seeking to gain a better understanding of changing trophic interactions in Great Lakes deepwater foodwebs and for developing strategies to restore native fish populations. Acknowledgments Bryon Daley, Bruce Davis, Erick Larson, Erik McDonald, Timothy P. O'Brien, Phil “Phlipp” Pepper, and Edward O. Roseman assisted with field collections and laboratory processing. David Bennion, Robin DeBruyne, Ellen George, and Patricia Thompson assisted with editing and formatting of tables and figures. This project was funded by the EPA Project Number DW-14-94816701-0 and the USGS Great Lakes Science Center. This article is Contribution 1771 of the U.S. Geological Survey, Great Lakes Science Center. References Auer, N.A. (Ed.), 1982. Identification of larval fishes of the great lakes basin with emphasis on the Lake Michigan drainage. Great Lakes Fishery Commission, Spec. Pub. 82–3 (Ann Arbor, MI, USA). Balcer, M.D., Korda, N.L., Dodson, S.I., 1984. Zooplankton of the Great Lakes: A Guide to the Identification and Ecology of the Common Crustacean Species. The University of Wisconsin Press, Madison, Wisconsin. Barbiero, R.P., Tuchman, M.L., 2004. Long-term dreissenid impacts on water clarity in Lake Erie. J. Great Lakes Res. 30, 557–565. Barbiero, R.P., Bunnell, D.B., Rockwell, D.C., Tuchman, M.L., 2009. Recent increases in the large glacial-relict calanoid Limnocalanus macrurus in Lake Michigan. J. Great Lakes Res. 35, 285–292. Black, G.A., Lankester, M.W., 1981. The biology and parasites of deepwater sculpin, Myoxocephalus quadricornis thompsonii (Girard), in Burchell Lake, Ontario. Can. J. Zool. 59, 1454–1457. Bowen, S.H., 1996. Quantitative description of the diet, In: Murphy, B.R., Willis, D.W. (Eds.), Fisheries Techniques, 2nd ed. Am. Fish. Soc. , pp. 513–532 (Bethesda, MD). Brandt, S.B., 1986. Disappearance of the deepwater sculpin (Myoxocephalus thompsonii) from Lake Ontario: the keystone predator hypothesis. J. Great Lakes Res. 12 (1), 18–24. Bunnell, D.B., Davis, B.M., Warner, D.M., Chriscinske, M.A., Roseman, E.F., 2011. Planktivory in the changing Lake Huron zooplankton community: Bythotrephes consumption exceeds that of Mysis and fish. Freshw. Biol. 56, 1281–1296. Chesson, J., 1978. Measuring preference in selective predation. Ecology 9, 211–215. Coldwater Task Group, 2012. Report of the Lake Erie Coldwater Task Group, March 2012. Presented to the Standing Technical Committee. Lake Erie Committee of the Great Lakes Fishery Commission, Ann Arbor, Michigan, USA. Davis, B.M., Savino, J.F., Ogilvie, L.M., 2005. Diets of forage fish in Lake Michigan. U.S. Environmental Protection Agency Report EPA/IAG DW14947692-01-0. (Chicago, IL, USA). Dymond, J.R., 1926. The fishes of Lake Nipigon. University of Toronto Studies in Biology. Ser.27. , 27. Publications of the Ontario Fisheries Research Lab 1–108. French III, J.R.P., Schaeffer, J.S., Roseman, E.F., Adams, J.V., Kiley, C.S., Fouilleroux, A., 2009. Abundance and distribution of benthic macroinvertebrates in offshore waters of western Lake Huron, 2001–2006. J. Great Lakes Res. 35, 120–127. Geffen, A.J., Nash, R.D.M., 1992. The life history strategy of deepwater sculpin, Myoxocephalus thompsonii (Girard), in Lake Michigan: dispersal and settlement patterns during the first year of life. J. Fish Biol. 41 (Supplement B), 101–110.

7

George, E.M., Roseman, E.F., Davis, B.M., O'Brien, T.P., 2013. Feeding ecology of pelagic larval burbot Lota lota in northern Lake Huron, Michigan. Trans. Am. Fish. Soc. (in press). Gorman, O.T., Evrard, L.M., Cholwek, G.A., Yule, D.L., Vinson, M.R., 2012. Status and trends of the nearshore fish community of Lake Superior, 2011. Annual Report to the Great Lakes Fish. Comm., Ann Arbor, MI. Hatcher, C.0., Nester, R.T., 1983. Distribution and Abundance of Fish Larvae in the St. Clair and Detroit Rivers. U. S. FWS, Ann Arbor, MI (Admin. Rep. 83-5, USFWS-GLFL/AR-83-5). Hatcher, C.O., Nester, R.T., Muth, K.M., 1991. Using larval fish abundance in the St, Clair and Detroit Rivers to predict year-class strength of forage fish in lakes Huron and Erie. J. Great Lakes Res. 17 (1), 74–84. Hondorp, D.W., Pothoven, S.A., Brandt, S.B., 2005. Influence of Diporeia density on diet composition, relative abundance, and energy density of planktivorous fishes in southeast Lake Michigan. Trans. Am. Fish. Soc. 134, 588–601. Hondorp, D.W., Pothoven, S.A., Brandt, S.B., 2011. Feeding selectivity of slimy sculpin Cottus cognatus and deepwater sculpin Myoxocephalus thompsonii in southeast Lake Michigan: Implications for species coexistence. J. Great Lakes Res. 37, 165–172. Jones, C., 1986. Determining age of larval fish with the otolith increment technique. Fish. Bull. 84 (1), 91–104. Jude, D.J., 1991. Belle River Power Plant fish entrainment and Impingement Study, 1990–1991. Freshwater Physicians, Inc., Brighton, MI (Report No. 91–3 to Detroit Edison Company). Kapuscinski, K.L., Sloss, B.L., Farrell, J.M., 2013. Genetic population structure of muskellunge in the Great Lakes. Trans. Amer. Fish. Soc. 142, 1075–1089. Kraft, C.E., 1977. Comparative Trophic Ecology of Deepwater Sculpins and Slimy Sculpins in Lake Michigan. (M.Sc. Thesis) University of Wisconsin, Madison, WI, USA. Lantry, B.F., O'Gorman, R., Walsh, M.G., Casselman, J.M., Hoyle, J.A., Keir, M.J., Lantry, J.R., 2007. Reappearance of deepwater sculpin in Lake Ontario: resurgence or last gasp of a doomed population? J. Great Lakes Res. 33 (Supp1), 34–45. Lechowicz, M.J., 1982. The sampling characteristics of electivity indices. Oecologia 52, 22–30. Leslie, J.K., Timmins, C.A., 1991. Distribution and abundance of young fish in Chenal Ecarte and Chematogen Channel in the St. Clair River delta, Ontario. In: Munawar, M., Edsall, T. (Eds.), Environmental Assessment and Habitat Evaluation of the Upper Great Lakes Connecting Channels. Hydrobiologia, 219. Kluwer Academic Publishers, Belgium, pp. 135–142. Madenjian, C.P., Hondorp, D.W., Desorcie, T.J., Holuszko, J.D., 2005. Sculpin community dynamics in Lake Michigan. J. Great Lakes Res. 31, 267–276. Madenjian, C.P., Bunnell, D.B., Desorcie, T.J., Chriscinske, M.A., Kostich, M.J., Adams, J.V., 2012. Status and trends of prey fish populations in Lake Michigan, 2011. Annual Report to the Great Lakes Fish. Comm., Ann Arbor, MI. Manly, B.F.J., 1974. A model for certain types of selection experiments. Biometrics 30, 281–294. Mansfield, P.J., Jude, D.J., Michaud, D.T., Brazo, D.C., Gulvas, J., 1983. Distribution and abundance of larval burbot and deepwater sculpin in Lake Michigan. Trans. Am. Fish. Soc. 112, 162–172. McAllister, D.E., 1961. The origin and status of the deepwater sculpin, Myoxocephalus thompsonii, a nearctic glacial relict. Nat. Mus. Can. Bull. 172, 44–65. McDonald, E.A., McNaught, A.S., Roseman, E.F., 2013. Use of main channel and nursery embayment habitats by larval fishes in the Detroit River. J. Great Lakes Res. (in press, This volume). McPhail, J.D., Lindsey, C.C., 1970. Freshwater fishes of northwestern Canada and Alaska Fish. Res. Board Can. Bull. 173. Nalepa, T.F., Fanslow, D.L., Pothoven, S.A., Foley III, A.J., Lang, G., 2007. Long-term trends in benthic macroinvertebrate populations in Lake Huron over the past four decades. J. Great Lakes Res. 33 (2), 421–436. O'Brien, T.P., Roseman, E.F., Kiley, C.S., Schaeffer, J.S., 2009. Fall diet and bathymetric distribution of deepwater sculpins (Myoxocephalus thompsonii) in Lake Huron. J. Great Lakes Res. 35, 464–472. Oyadomari, J.K., Auer, N.A., 2004. Inshore–offshore distribution of larval fishes in Lake Superior off the western coast of the Keweenaw Peninsula, Michigan. J. Great Lakes Res. 30 (Supplement 1), 369–384. Pennak, R.W., 2001. Fresh-Water Invertebrates of the United States, 4th ed. John Wiley and Sons, New York. Poe, T.P., 1983. Food habits of larval yellow perch as a potential indicator of water and habitat quality. U.S. Fish and Wildlife Service, Great Lakes Fishery Laboratory, Administrative Report 83-2. (Ann Arbor, MI). Pothoven, S.A., Hondorp, D.W., Nalepa, T.F., 2011. Declines in deepwater sculpins Myoxocephalus thompsonii energy density associated with the disappearance of Diporeia spp. in lakes Huron and Michigan. Ecol. Freshw. Fish 20, 14–22. Riley, S.C., He, J., Johnson, J., O'Brien, T.P., Schaeffer, J., 2007. Evidence of widespread natural reproduction of lake trout Salvelinus namaycush in the Michigan waters of Lake Huron. J. Great Lakes Res. 33 (4), 917–921. Riley, S.C., Roseman, E.F., Nichols, S.J., O'Brien, T.P., Kiley, C.S., Schaeffer, J.S., 2008. Deepwater demersal fish community collapse in Lake Huron. Trans. Am. Fish. Soc. 137 (6), 1879–1890. Riley, S.C., Roseman, E.F., O'Brien, T.P., Fingerle, A.L., Londer, J.G., George, E.M., 2012. Status and trends of the Lake Huron offshore demersal fish community, 1976–2011. Annual Report to the Great Lakes Fish. Comm., Ann Arbor, MI. Roseman, E.F., O'Brien, T.P., 2013. Spatial distribution of pelagic fish larvae in northern main basin of Lake Huron. Aquat. Ecosyst. Health Manag. (in press, Accepted 4 Feb 2013). Roseman, E.F., Riley, S.C., 2009. Biomass of deepwater demersal forage fishes in Lake Huron, 1994–2007: implications for offshore predators. Aquat. Ecosyst. Heal. Manag. 12 (1), 29–36. Roseman, E.F., Jude, D.J., Raths, M.K., Coon, T.G., Taylor, W.T., 1998. Occurrence of the deepwater sculpin (Myoxocephalus thompsonii) in western Lake Erie. J. Great Lakes Res. 24 (2), 479–483.

Please cite this article as: Roseman, E.F., Diet and habitat use by age-0 deepwater sculpins in northern Lake Huron, Michigan and the Detroit River, J Great Lakes Res (2013), http://dx.doi.org/10.1016/j.jglr.2013.07.004

8

E.F. Roseman / Journal of Great Lakes Research xxx (2013) xxx–xxx

Savino, J., 2009. The role of Invasive Species in Lake Huron Food Web Disruptions. Research Completion Report Prepared for US EPA Great Lakes National Program Office, Chicago, Illinois. Schaeffer, J.S., Bowen, A., Thomas, M., French III, J.R.P., Curtis, G.L., 2005. Invasion history, proliferation, and offshore diet of the round goby Neogobius melanostomus in western Lake Huron, USA. J. Great Lakes Res. 31, 414–425. Secor, D.H., Dean, J.M., Laban, E.H., 1991. Otolith removal and preparation for microstructural examination. Chapter 3.In D. Stephenson and S. Campana (eds.), Otolith Microstructure Examination and Analysis. Spec. Publ. Can. J. Fish. Aquat. Sci. 117, 17–59. Selgeby, J.H., 1988. Comparative biology of the sculpins of Lake Superior. J. Great Lakes Res. 14, 44–51. Vanderploeg, H., Scavia, D., 1979. Calculation and use of selectivity coefficients of feeding: Zooplankton grazing. Ecol. Model. 7, 135–149.

Weidel, B.C., Walsh, M.G., Connerton, M.J., 2012. Sculpin and round goby assessment in the U.S. waters of Lake Ontario, 2011. Status of important prey fishes in the U.S. Waters of Lake Ontario, 2011. Annual Report, Bureau of Fisheries, Lake Ontario Unit and St. Lawrence River Unit to Great Lakes Fishery Commission's Lake Ontario Committee 12–20. Wells, L., 1980. Food of alewives, yellow perch, spottail shiners, trout perch, and slimy and fourhorn sculpins in southeastern Lake Michigan. Tech. papers USFWS, 98. Wells, L., McLain, A.L., 1973. Lake Michigan: man's effects on native fish stocks and other biota. Great Lakes Fish. Comm. Tech. Rep., 14. Wojcik, J.A., Evans, M.S., Jude, D.J., 1986. Food of the deepwater sculpin, Myoxocephalus thompsonii, from southeastern Lake Michigan. J. Great Lakes Res. 12, 225–231. Zimmerman, M.S., Krueger, C.C., 2009. An ecosystem perspective on re-establishing native deepwater fishes in the Laurentian Great Lakes. N. Am. J. Fish. Manag. 29, 1352–1371.

Please cite this article as: Roseman, E.F., Diet and habitat use by age-0 deepwater sculpins in northern Lake Huron, Michigan and the Detroit River, J Great Lakes Res (2013), http://dx.doi.org/10.1016/j.jglr.2013.07.004