Northeastern Naturalist 380 J. Livermore, M. Trainor, and M.S.. Bednarski 22001177 NORTHEASTERN NATURALIST 2V4(o3l). :2348,0 N–3o9. 03 Successful Spawning of Anadromous Petromyzon marinus L. (Sea Lamprey) in a Restored Stream Channel Following Dam Removal Julia Livermore1,2, Michael Trainor1,*, and Michael S. Bednarski1,3 Abstract - Petromyzon marinus (Sea Lamprey) is a large, anadromous, ectoparasitic fish native to the Northeast Atlantic Coast. Sea Lamprey nest-building activities increase stream habitat heterogeneity, benthic invertebrate diversity, and fish density. The Sea Lamprey has undergone severe declines throughout most of its native range in part due to dams that limit access to spawning habitat. Here, we documented the spawning of Sea Lamprey in the Mill River in Taunton, MA, following stream channel reconstruction. Sea Lamprey nest-construction activities altered 129 m2 and 32 m2 of total streambed area within the reconstructed channel during 2014 and 2015, respectively. The association of Sea Lamprey spawning with stream restoration has important implications to the ecology of the Mill River and demonstrates that similar projects may facilitate the recovery of Sea Lamprey populations in the Northeast. Introduction Petromyzon marinus L. (Sea Lamprey) is a large (up to 1.2 m total length; Flescher and Martini 2002) semelparous, anadromous, and ectoparasitic fish native to coastal North Atlantic and northern Mediterranean watersheds (Maitland 2003). Sea Lamprey migrate into rivers during the spring to spawn. During this migration, individuals seek areas with gravel and sand substrate and may utilize habitats up to 500 km from the sea (Applegate 1950, Sabatié 1998). Upon reaching their nesting grounds, male Sea Lamprey use their oral disks to suction and move rocks to build large, oval-shaped nests consisting of depressions or pits in the substrate with larger stones on the periphery and a mound of coarse gravel and cobble downstream. Females then release eggs that adhere to sand particles within the nests (Applegate 1950). Sub-adult Sea Lamprey feed by parasitizing various fish species (Sabatié 1998). Sea Lamprey are obligate parasites of other fish during their marine life-history stage, but they do not parasitize any species in freshwater in their native range, except for the land-locked population of the Laurentian Great Lakes, where their effects have devastated some native fish populations (Smith and Tibbles 1980). While some managers view Sea Lamprey as detrimental to certain aquatic environments due to their parasitic marine life-history stage (Kircheis 2004), the species serves 1Massachusetts Division of Marine Fisheries, 1213 Purchase St., New Bedford, MA 02740. 2Current address – Rhode Island Department of Environmental Management, Division of Marine Fisheries, 3 Fort Wetherill Rd., Jamestown, RI, 02835. 3Current address - Virginia Department of Game and Inland Fisheries, PO Box 90778, Henrico, VA 23228. *Corresponding author - mike.trainor@state.ma.us. Manuscript Editor: James McKenna Northeastern Naturalist Vol. 24, No. 3 J. Livermore, M. Trainor, and M.S.. Bednarski 2017 381 an important ecological role in riverine systems. Sea Lamprey nest construction increases habitat heterogeneity by creating shallow, rapid, rocky habitat patches amongst areas of deep, slow, sandy substrate, resulting in varied microhabitats that persist for months after spawning ceases (Hogg et al. 2014). Sea Lamprey mounds in Maine caused habitat changes that led to a 77% rise in benthic invertebrate density as well as significant increases in the biomass and diversity of such organisms, chiefly insects (Hogg et al. 2014). Additionally, the Sea Lamprey’s semelparous life history makes it an important source of nutrients for oligotrophic river systems (Guyette 2012, Stockner et al. 2000). The Sea Lamprey has undergone precipitous declines through much of its range (OSPAR 2009). Although studies of Sea Lamprey abundance in the coastal systems of North America are limited, several European nations have noted severe declines and fragmentation of the distribution area because of habitat degradation (OSPAR 2008, 2009). While little is known of the natural variability of Sea Lamprey population size, activities such as dam construction, pollution, and eutrophication have been demonstrated to affect adult Sea Lamprey migrations and the success of ammocoetes in settling into river beds; thus, the decline is at least in part due to human activity (OSPAR 2005, 2009). Other lamprey species native to the Northern Hemisphere have also suffered from habitat degradation through pollution and stream alteration. Of the 34 species native to the Northern Hemisphere, 9 are vulnerable in part of their range, 10 are endangered, and 1 is already extinct (Renaud 1997). Mitigation measures are necessary to ensure that the North American Sea Lamprey population does not suffer similar consequences. The removal of dams is becoming a common tool for restoring diadromous fish species, but little is known of how Sea Lamprey utilize the restored stream channel following dam removal. The removal of the Hopewell Mills Dam on the Mill River in Taunton, MA, in 2012 presented an opportunity to answer this question. The dam was removed as part of a larger effort to restore unimpeded fish passage throughout the Mill River. As part of the removal, the channel upstream of the dam was reconstructed to mimic a natural stream. The objective of this study was to quantify the response of Sea Lamprey to the removal of the Hopewell Mills Dam by determining the extent of spawning activity occurring within the newly reconstructed channel. Study Site The Mill River is a moderate-sized tributary of the Taunton River, the watershed of which has a total drainage area of 3771 km² and ultimately empties into Narragansett Bay. The Taunton River is free flowing (i.e., there are no obstructions from Narragansett Bay up to the Mill River) and arises from the confluence of the Town and Matfield rivers in the town of Bridgewater. The Taunton River then flows through the towns of Halifax, Middleborough, and Raynham before entering Taunton, where the Mill River empties into it. The Mill River flows 6.2 km through the center of Taunton from its headwater, Lake Sabbatia. The total Mill River drainage area is ~113 km². Four dams were historically present in the Mill River system. The lowermost structure, the Hopewell Mills Dam, was removed in 2012. This dam Northeastern Naturalist 382 J. Livermore, M. Trainor, and M.S.. Bednarski 2017 Vol. 24, No. 3 consisted of a 106-m-long earthen berm with a 2.4-m hydraulic head. Flow passed over an 11.6-m-wide concrete ogee spillway and down a 30-m long channel with 2 vertical 1.2-m drops. Either side of the dam was bordered at the downstream end by vertical concrete abutment walls exceeding 30 m in length (Inter-Fluve, Inc. 2010a). Due to the height of the drops at the spillway, the Hopewell Mills Dam undoubtedly prevented access to upstream habitats prior to its removal (Inter-Fluve, Inc. 2010b). Due to this assessment of the dam and the fact that there was no documentation, scientific or anecdotal, of Sea Lamprey in the upstream impoundment, no formal survey of Sea Lamprey spawning upstream of the dam was conducted prior to removal. The former 2.1-ha impoundment reached up to 2.4 m in depth and contained an alluvium substrate, a mixture of stream-deposited gravel, silt, sand, and clay, in this case primarily sand (Inter-Fluve, Inc. 2010a), which is not suitable for Sea Lamprey spawning. Additionally, studies indicate that acceptable Sea Lamprey habitat requires a steady, unidirectional stream flow between 1.1 and 1.3 m/s, coupled with a medium gravel substrate (Applegate 1950, Morman et al. 1980), conditions that did not exist in the channel prior to dam removal. Project engineers classified the impoundment as degraded lentic habitat, benefiting non-native warmwater emigrants from Lake Sabbatia. Water temperatures regularly became high in the summer due to solar exposure, which resulted in intense algal and vegetative growth and consequent impaired dissolved oxygen concentrations (Inter-Fluve, Inc. 2010b). Channel reconstruction was designed to mimic a stream environment specifically to provide habitat for endemic aquatic species, and therefore incorporates native vegetation and substrate consistent with natural river habitat. The restored channel has 5 meander bends with banks constructed of coconut-fiber soil lifts and stabilized by native shrubs and trees. Each bend features a gravel deposit and pool, while the channel bed is composed of native and imported gravel and cobble 0.5–17.8 cm in median diameter (by weight: 5% 0.2–0.5 mm, 11% 2.0–2.3 cm, 34% 10.2–11.7 cm, 34% 12.2–14.2 cm, and 16% 15.2–17.8 cm). In addition, large wood pieces and root wads from trees cut down during the dam removal were placed into the stream bank to limit erosion and provide structured habitat (Inter-Fluve, Inc. 2010a, b). The final reconstructed channel was designed to create an overall average slope of 0.0051 through the impoundment, with a 15.2-mwide channel top and 0.75–0.90-m-high banks. Two sections of transition riffles (0.0092 and 0.0089 in slope) were included at the upstream and downstream ends of the channel to control the grade of the new channel. Riffle section substrate was constructed with a mixture of imported and salvaged substrate with a broad gradation ranging in size from 30.5 cm down to 0.5 cm sand (by weight: 5% 0.5–0.8 mm, 11% 3.6–4.1 mm, 34% 17.8–20.3 cm, 34% 20.3–25.4 cm, and 16% 29.9–30.5 cm; Inter-Fluve, Inc. 2010b). The restoration project created ~5472 m2 of lotic habitat in the ~360-m-long channel of the lower Mill River, between the Hopewell Mills Dam and the last remaining barrier, the West Britannia Dam (Fig. 1). The new channel (Section Northeastern Naturalist Vol. 24, No. 3 J. Livermore, M. Trainor, and M.S.. Bednarski 2017 383 A in Fig. 2) occupies 27% of the former lentic habitat by area and extends the full length of the former pond impoundment. The 370-m section upstream from Figure 1. Map of the Mill and Taunton Rivers (Taunton, MA) including locations of barriers (existing and removed) to fish passage along the Mill River . Northeastern Naturalist 384 J. Livermore, M. Trainor, and M.S.. Bednarski 2017 Vol. 24, No. 3 the impoundment but downstream from the West Britannia Dam, remains native, unreconstructed stream (Section B in Fig. 2). Our monitoring effort focused on Figure 2. Study site map including Sea Lamprey nest locations from 2014. No nest locations were recorded during the 2015 survey due to GPS unit technical issues. Northeastern Naturalist Vol. 24, No. 3 J. Livermore, M. Trainor, and M.S.. Bednarski 2017 385 quantifying the influence Sea Lamprey spawning activities have on river habitat following the restoration of full passage beyond the original barrier dam. Methods On 12 June 2014 and 1 June 2015, we performed a census of nests in the full length of the reconstructed stream channel (Section A in Fig. 2) between the West Britannia Dam and the former Hopewell Mills Dam site by visually observing the streambed while wading in the stream; we did not survey for Sea Lamprey nests upstream of the reconstructed channel (Section B in Fig. 2) or in 2013 immediately following dam removal. The surveys were timed to occur after Sea Lamprey spawning activity was complete but before periphyton growth had obscured the nests. Two biologists waded through the reconstructed streambed and identified nests visually, which was possible because of the dramatic color contrast between recently overturned substrate and the surrounding area. A transect tape measure was then used to measure the nests. To determine the amount of streambed area modified by spawning Sea Lamprey, we calculated individual nest area, making the assumption that all nests were generally oval in shape. We measured nest width (the total width of the nest pit plus any coarse gravel/cobble width beyond the pit perimeter; Fig. 3) and nest length (the combined nest pit and tailspill length). Oval areas were calculated using the equation A = π × (L/2) * (W/2) × 0.0001, where A is the area in m2, L is the nest length (cm), and W is the nest width (cm). Individual nest areas were summed by year to determine the total annual area of habitat used for nests within the reconstructed stream channel. Results The number of individual nests constructed by Sea Lamprey differed between the 2 years. We observed 33 nests in 2014 and 13 nests in 2015. The furthest downstream nest was located ~40 m upstream from the remnants of the former Hopewell Mills Dam (Fig. 3). All nests were located where water depth was 0.5–1 m. While nest locations were not recorded in 2015 due to technological issues with our GPS unit, the nests both years were distributed over the same section of the restored stream channel. The size of the cobble surrounding and downstream of each nest was 8–16 cm in diameter. Pebbles and gravel less than 5 cm in diameter littered the streambed and lined the pit section (center) of the nests. Finer sand and silt made up the rest of the substrate within and around each nest. Substrate composition and availability did not change between years. Nest dimensions averaged over 1.00 m for both length and width for both years sampled (Fig. 4). The maximum nest length recorded was 7.40 m and maximum width was 3.40 m; both maximum dimensions were observed in 2014. Over the 2-year sampling period, 73.9% of nest areas were greater than 1.5 m2, with a mean area of 3.52 m2 (± 0.50 SE; Fig. 4). The total area of reconstructed stream channel altered by the Sea Lamprey was 129 m2 in 2014 and 32 m2 in 2015. Northeastern Naturalist 386 J. Livermore, M. Trainor, and M.S.. Bednarski 2017 Vol. 24, No. 3 Figure 3. Nest size measurements used in calculating nest areas. Figure 4. Boxplots of summed nest lengths (m), widths (m), and areas (m2) for 2014, 2015, and the entire study period combined. Dots represent outliers. Dark horizontal lines indicate the median. Tops and bottoms of boxes are the 1st and 3rd quartile. Whiskers represent the maximum and minimum values, excluding outliers. Northeastern Naturalist Vol. 24, No. 3 J. Livermore, M. Trainor, and M.S.. Bednarski 2017 387 Discussion Adult Sea Lamprey spawned within the reconstructed stream channel of the Mill River the second year after the removal of the Hopewell Mills Dam. We conclude that the observance of ≥13 nests in each year of the study provides compelling evidence that the removal of the Hopewell Mills Dam provided new habitat for Sea Lamprey in the Mill River. We surveyed the restored habitat available to Sea Lamprey and found many nests in the section of river that was created by the removal of the Hopewell Mills Dam and subsequent channel restoration. Sea Lamprey spawning activity impacted 2.4% and 0.6% of the available restored stream channel habitat in 2014 and 2015, respectively. Therefore, the reconstructed Mill River channel represents new and usable habitat for Sea Lamprey, which may support run size increases in the future as has occurred after restoration projects in the Westfield, Farmington, Salmon, and Connecticut rivers (McMenemy 2004). This is the first generation of Sea Lamprey to utilize this habitat and as their numbers increase, the percentage of affected habitat can be expected to increase as well. It is also crucial to note that the substrate on which the Sea Lamprey spawned was imported by engineers as part of the dam removal project, demonstrating that artificially constructed stream channels can support spawning Sea Lamprey. Most of the restored stream channel supported spawning activity except for the section immediately upstream of where the new channel and native river were joined (the uppermost portion of Section A in Fig. 2). This river section is dynamic and contains larger boulders and tree stumps that create rapid channels and uneven riverbed terrain. No Sea Lamprey nests were observed in this section in 2014 or 2015; the absence of nests was likely due to its steep and rugose substrate, in addition to its lack of gravel/cobble, which is essential to support Sea Lamprey spawning (Applegate 1950). The distribution of adults among rivers and tributaries can fluctuate among years (Morman et al. 1980), as was the case in the reconstructed Mill River stream channel, where we identified 33 nests in 2014 and 13 nests in 2015. The difference in nest numbers, and consequently the area utilized by Sea Lamprey, in 2014 and 2015 may have been due to environmental conditions and possible changes in oceanic population size. Fluctuations in spawning Sea Lamprey populations are common in New England Rivers; annual lamprey counts between 1975 and 2016 at the Holyoke Dam Fishlift have ranged between 14,000 and 99,000 (HG&E 2017, McMenemy 2004), while those at the Vernon Dam fishway in Vermont have varied between several hundred and 16,000 (McMenemy 2004). It is unlikely that limited habitat caused the decline in nests in 2015 since there was no change in habitat availability in the Mill River between 2014 and 2015. The successful response of Sea Lamprey to stream restoration has important implications to the ecology of the Mill River. Habitats created by spawning Sea Lamprey likely provide young-of-the-year drift-feeding fish with energetically profitable foraging habitats. Sea Lamprey alterations may still be detectable in Northeastern Naturalist 388 J. Livermore, M. Trainor, and M.S.. Bednarski 2017 Vol. 24, No. 3 the early fall of each year, potentially increasing the density and diversity of benthic insects in affected substrate (Hogg et al. 2014, Kircheis 2004, Saunders et al. 2006). In addition to their role as ecosystem engineers, Sea Lamprey are obligately semelparous, and all adults die soon after spawning occurs (Beamish 1980). Carcass decomposition produces a pulse of increased nutrient availability (primarily phosphorus) during a time in which North Atlantic streams are most vulnerable to nutrient depletion (Guyette 2012, Nislow and Kynard 2009, Stockner et al. 2000) due to decreased nutrient inputs (from decreased surface runoff) and/or increases in biological uptake (Lee et al. 2012). This increased biological nutrient uptake results partially from fish species growing rapidly; Sea Lamprey carcass decomposition therefore occurs at a time during which other species require abundant prey for optimal growth conditions. Our study on the restoration of the Mill River indicates that river reconstruction projects can be designed to promote the spawning of Sea Lamprey in the Northeast. Most restoration projects in the region have focused on the recovery of Alosa aestivalis (Mitchill) (Blueback Herring), Alosa pseudoharengus (Wilson) (Alewife), Alosa sapidissima (Wilson) (American Shad), and Anguilla rostrata (Lesueur) (American Eel), while considering Sea Lamprey recovery a secondary benefit. Further restoration efforts in the north Atlantic region should not only continue to include goals for Sea Lamprey recovery, but also prioritize Sea Lamprey habitat restoration because of the importance of the species as an ecosystem engineer and contributor of important limiting nutrients in potentially oligotrophic waters. Acknowledgments The removal of dams along the Mill River and its subsequent restoration was carried out as a partnership between Massachusetts Division of Ecological Restoration (MA DER), Massachusetts Department of Health, Massachusetts Division of Marine Fisheries (MA DMF), Southeastern Regional Planning and Economic Development District, City of Taunton, USDA Natural Resources Conservation Service, National Oceanic and Atmospheric Administration (NOAA), US Fish and Wildlife Service (USFWS), American Rivers, The Nature Conservancy (TNC), Save The Bay/Restore America’s Estuaries, Taunton River Watershed Alliance, Massachusetts Audubon Society, Massachusetts Environmental Trust, and dam owners Horsley-Witten Group and Bridgewater State University. Funding for the restoration was provided by NOAA, USFWS, MA DER, TNC, American Rivers, and the Massachusetts Environmental Trust. Nick Nelson (Inter-Fluve) provided detailed information on stream channel reconstruction design and specifications. Alison Bowden (TNC) and Beth Lambert (MA DER) provided insight on restoration project development. Brad Chase (MA DMF), Sara Turner (MA DMF), Cathy Bozek (USFWS), Beth Lambert, Alison Bowden, and Kristen Ferry (MA DER) provided comments and feedback. Two anonymous reviewers greatly improved this manuscript. We are thankful for the contributions of the agencies, staff, and reviewers who provided assistance with this project. Literature Cited Applegate, V.C. 1950. Natural history of the Sea Lamprey, Petromyzon marinus, in Michigan. US Fish and Wildlife Service Special Scientific Report 55. Washington, DC. Northeastern Naturalist Vol. 24, No. 3 J. Livermore, M. Trainor, and M.S.. Bednarski 2017 389 Beamish, F.W. 1980. Biology of the North American anadromous Sea Lamprey, Petromyzon marinus. Canadian Journal of Fisheries and Aquatic Sciences 37:1924–1943. 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