Sea Lamprey Control: Past, Present, and Future

Michael J. Siefkes, Todd B. Steeves, W. Paul Sullivan, Michael B. Twohey, and Weiming Li

Introduction

T e establishment of non-native species, whether intentional or accidental, combined with anthropogenic exploitation of fshes and their habitats have signifcantly and irreversibly altered the ecosystems of the Laurentian Great Lakes (Smith 1968; Loftus and Regier 1972; Eshenroder and Burnham-Curtis 1999; Leach et al. 1999). One invasive species that has had a marked impact upon Great Lakes fsh populations is the Sea Lamprey (Petromyzon marinus). T e history of Sea Lamprey invasion and control has been well-documented (Applegate 1950a, 1950b; Lawrie 1970; Smith et al. 1974), and the proceedings of two international symposia were published as supplementary issues of scientifc journals (Canadian Journal of Fisheries and Aquatic Sciences 1980 37[11]; Journal of Great Lakes Research 2003 29[Supplement 1]; SLIS I and SLIS II). T e Sea Lamprey Control Program in the Great Lakes is a case study in coordinated and integrated binational fshery management and is the only reported successful control program for a non-native, vertebrate pest species, as evidenced by the 90 percent reduction from peak levels of Sea Lamprey abundance and the resultant rehabilitation of fsheries across the Great Lakes basin.

Sea Lamprey Invasion and Fisheries Collapse

T e earliest record of Sea Lamprey in the Great Lakes occurred in 1835 in Lake Ontario (Lark 1973), where a naturalist described what is accepted to be a mature, spawning-phase Sea Lamprey in Duffns Creek, Ontario. T e timing of this observation is consistent with colonization after the opening of the Erie Canal during 1819 (Smith 1995). To the contrary, colonization of Lake Ontario via the Erie Canal is skeptically viewed (Daniels 2001), and genetic evidence supports the concept that Sea Lampreys from Lake Ontario are distinct from presumed Atlantic origins and are native (Waldman et al. 2004; Bryan et al. 2005). Nevertheless, the debate regarding the origin of Sea Lampreys in Lake Ontario continues (see Eshenroder 2009; Waldman et al. 2009). T e invasion of the remainder of the Great Lakes has been well-documented (Dymond 1922; Applegate 1950b; Lawrie 1970; Smith 1971; Pearce et al. 1980; Smith and Tibbles 1980), with frst observations of Sea

651 652 Michael J. Siefkes et al.

Lampreys in Lake Erie in 1921, Lake Huron in 1937, Lake Michigan in 1936, and Lake Superior in 1938. Examination of Sea Lamprey length data and location of the observation of these frst sightings indicate Sea Lampreys were likely present in the lakes above Niagara Falls for several years, without being observed either as parasites on fsh or in tributaries during their spawning phase (Smith 1971; Smith and Tibbles 1980; Eshenroder and Amatangelo 2005). T ere is widespread agreement among fshery biologists that changes in lake ecosystems during the period of Sea Lamprey invasion are due to a combination of overfshing, Sea Lamprey predation, and habitat alteration (Hile et al. 1951; Smith and Tibbles 1980; Coble et al. 1990; Eshenroder and Burnham- Curtis 1999; Hansen 1999; fg. 1). Debate remains about the proportional impacts of each of these factors in the decline of fsh species, particularly commercial species, such as the Lake Trout (Salvelinus namaycush), Lake Whitefsh (Coregonus clupeaformis), and deepwater Ciscoes (C. spp.; Hansen 1999; Coble et al. 1990; Eshenroder and Amatangelo 2005). Regardless of the cause of fshery decline, rehabilitation of the Lake Trout populations became the measure of fshery restoration for each lake. Stocking of hatchery-reared Lake Trout, improvement to Lake Trout habitat, and fshery regulation are part of the ef ort to restore Lake Trout to abundances observed during the early 1900s. It was evident by the 1950s that a program to control the Sea Lamprey would also be a vital part of Lake Trout restoration.

Chapter Goal and Outline

T is chapter’s goal is to describe the past, present, and future of Sea Lamprey control in the Great Lakes. T e remainder of this chapter begins with a history of Sea Lamprey control. T e development, implementation, and future of each component in Sea Lamprey control are then summarized. Given this background, the present status of Sea Lamprey control in each of the Great Lakes is examined. T e chapter concludes with a brief look into new developments in Sea Lamprey control, including two promising areas in which recent research has shown encouraging results for their use in Sea Lamprey control: pheromones and genomics.

Early Development of the Sea Lamprey Control Program

T e Sea Lamprey invasion in the Great Lakes was the primary catalyst for the governments of Canada and the United States to establish a binational entity to develop coordinated approaches to protect and rehabilitate shared fsh stocks (Fetterolf 1980; Gaden et al.2012). Previously, fshery management was not widely coordinated among the states and province bordering the Great Lakes (Dochoda and Koonce 1994). During 1946, the Great Lakes Sea Lamprey Committee was formed to develop coordinated, cooperative, and binational management focused on the life history and biological ef ects of the Sea Lamprey in the Great Lakes (Smith et al. 1974). T en, on September 10, 1954, the Convention on Great Lakes Fisheries (the Convention) was signed by Canada and the United States, establishing the Great Lakes Fishery Commission (GLFC; GLFC 1955). T e Convention mandated the GLFC “to formulate and implement a comprehensive program for the purpose of eradicating or minimizing Sea Lamprey populations” in the Great Lakes and to create and manage a fshery research program focusing on important fsh stocks (GLFC 1955). T e GLFC contracted with the Fisheries Research Board of Canada and the U.S. Fish and Wildlife Service (USFWS) to implement Sea Lamprey control in Canada and the United States, as recommended in Article VI of the Convention (Christie and Goddard 2003). During 1966, the Canadian Department FIG. 1. Commercial Lake Trout (Salvelinus namaycush) harvest for each Great Lake. Vertical dashed lines indicate frst observation of Sea Lamprey (Petromyzon marinus) in the lake (Lake Ontario is 1835) and the vertical black lines indicate the year of frst lampricide application.

Data from Baldwin et al. (2002). 654 Michael J. Siefkes et al. of Fisheries and Oceans (DFO) assumed the responsibility for Sea Lamprey control in Canada (Christie and Goddard 2003). Agency personnel contracted by the GLFC to implement the Sea Lamprey Control Program are termed control agents. Early Sea Lamprey control was guided by an advisory committee, consisting of members of the GLFC, control agents, and research biologists, that met annually to discuss recommendations for program funding and direction (Christie and Goddard 2003). A series of reviews during the 1980s led the GLFC to expand the advisory committee to include fshery management agencies to better link fsh community objectives with Sea Lamprey control (Koonce et al. 1982; Spangler and Jacobson 1985). Experts in integrated pest management were also invited to the newly structured advisory committee (Christie and Goddard 2003), which was named the Sea Lamprey Integration Committee (SLIC). Technical task forces were established under the SLIC to provide details and recommendations about control activities. T ese task forces included control agents, fshery managers, research biologists, and other relevant experts. T e SLIC and its task forces continue to support the GLFC’s decision-making process with input from a diverse group of experts as Sea Lamprey control continues to evolve. Another important guide for the Sea Lamprey Control Program was the development of the GLFC Vision (GLFC 1992, 2001). First established during 1992 and then revised during 2001, the GLFC Vision provided milestones for the Sea Lamprey Control Program and the restoration of the fshery for each Great Lake. Specifcally, targets for Sea Lamprey abundance in each lake were established and were to be achieved through the optimal implementation of control strategies, including appropriate assessment of Sea Lamprey recruitment, an integrated mix of lampricide and alternative controls, and control of Sea Lampreys in the St. Marys River. Overall, the GLFC Vision called for the successful control of Sea Lamprey populations to allow the rehabilitation of native and desirable fsh stocks in each lake. T e GLFC Vision continues to guide the Sea Lamprey Control Program. Two elements were crucial to the early Sea Lamprey control in the Great Lakes, before the establishment of the GLFC: the determination of the Sea Lamprey life cycle (fg. 2) and the cataloguing of the tributaries used for spawning (Applegate 1950a, 1950b). In the Laurentian Great Lakes, the Sea Lamprey has a potamodramous (migrating within fresh water only) life history comprehensively described in other publications (Applegate 1950a, 1950b; Scott and Crossman 1973). Sea Lampreys begin life in Great Lakes tributaries as non-parasitic larvae, where they flter-feed on microorganisms for three to six years. Larval Sea Lampreys then begin a dramatic metamorphosis, developing eyes, oral disks, and tongues covered with teeth and begin migrating downstream to the lakes; downstream-migrating Sea Lampreys are called transformers. Once larval Sea Lampreys have completely transformed and migrated to the lakes, they enter the parasitic-phase, feed on fsh, and grow for twelve to eighteen months. During the late winter or early spring, parasitic-phase Sea Lampreys stop feeding, enter the spawning-phase of their lifecycle, and begin to search for suitable spawning tributaries. On fnding and entering a tributary, spawning-phase Sea Lampreys begin the fnal stages of sexual maturation, reproduce during the spring and early summer, and die shortly after spawning. Review of the Sea Lamprey life history by early fshery managers indicated that impacts to populations would best be made during the stages spent in tributaries; larvae, transformers, and spawning-phase adults. Initial ef orts to control the Sea Lamprey began in the 1940s and focused on preventing migrating Sea Lampreys from reaching spawning areas through the use of mechanical and electrical weirs and low-head barriers (Lavis et al. 2003a). As problems with weirs and barriers were encountered, fshery SEA LAMPREY CONTROL 655

FIG. 2. T e Sea Lamprey (Petromyzon marinus) life cycle.

Great Lakes Fishery Commission.

managers quickly realized that fnding a pesticide (lampricide) that could be applied to tributaries to target larvae, limit the recruitment of Sea Lampreys to the Great Lakes prior to their parasitic-phase, and af ect as many as fve generations of larvae in the same tributary would likely be the most ef ective method of reducing Sea Lamprey populations.

Principal Techniques of Sea Lamprey Control—Lampricides

Development of Lampricides

Investigations to fnd a lampricide that could selectively kill larval Sea Lampreys, while having little or no ef ect on non-target organisms, were undertaken at Hammond Bay Biological Station in Millersburg, Michigan, during 1950. It was envisioned that the lampricide could be applied to tributaries throughout the Great Lakes, killing multiple generations of larval Sea Lampreys in the tributary prior to metamorphosis and the start of the parasitic phase. Ideally, a lampricide would kill larvae at a low concentration, work 656 Michael J. Siefkes et al. ef ectively over a short period, be metered into fowing water at precise rates, be soluble and mix thoroughly throughout the tributary, have no deleterious residual compounds once larvae were killed, and be inexpen- sive to produce. More than six thousand predominantly organic chemicals were examined for dif erential toxicity to larvae and twelve other fsh species in static bioassay and simulated stream experiments. A group of mono-nitrophenols containing bromine, chlorine, or fuorine was found to possess all of the desirable traits of an ef ective lampricide. Of these, the sodium salt form of 3-trifuoromethyl-4-nitrophenol (TFM) was found the most suitable compound for use as a liquid lampricide. The evaluation of compounds also led to the discovery of a second lampricide, 2,'5-dichloro-4'- nitrosalicylanilide, during 1963 (Howell et al. 1964). Initially registered as Bayer 73 and now registered as Bayluscide, 2,'5-dichloro-4'-nitrosalicylanilide is a water-soluble powder not as selectively toxic to Sea Lam- preys as TFM; one of Bayluscide’s additional uses is as a molluscicide, to control outbreaks of swimmer’s itch by reducing the population of snails that serve as vectors for the parasite that causes the disease. To date, three formulations of Bayluscide have been developed for application in the feld: a wettable powder and an emulsifable liquid are used as a synergistic additive during TFM treatments to reduce the amount of TFM required, resulting in a signifcant cost savings during the treatment of high-discharge tributaries; and a granular form, consisting of a grain of sand that is coated with Bayluscide and encapsulated within a water soluble coating containing a surfactant that enables application of the Bayluscide to waters greater than 1 m in tributaries and in lentic areas adjacent to tributary mouths. Bayluscide granules are used as an assessment tool to determine larval Sea Lamprey presence and abundance or as a method of control where the application of TFM is not practical. Experimental applications of TFM to tributaries was completed in Lake Huron during 1957; the success of these treatments resulted in the scheduling of treatments for twelve tributaries to Lake Superior during 1958 and an additional sixty from 1959 to 1960 (Smith and Tibbles 1980; Heinrich et al. 2003). T ese initial treatments had dramatic ef ects on the resident larval Sea Lampreys, subsequently reducing the lake-wide spawning-phase Sea Lamprey abundance estimate in Lake Superior from 1.35 million during 1960 to approximately 200,000 during 1962. Similar dramatic decreases in Sea Lamprey abundance estimates have been observed in each Great Lake, following the implementation of lampricide treatments.

Environmental Fate of Lampricides and Effects on Non-Target Organisms

Hubert (2003) and Dawson (2003) provide a comprehensive review of the fates of TFM and Bayluscide in the aquatic environment. T e persistence of TFM and Bayluscide after treatment application is relatively short, with the active ingredients in TFM and Bayluscide af ected by both abiotic and biotic processes in the stream environment. T e primary abiotic processes af ecting lampricides are sediment binding, particularly to sediments with high organic content, and photodecomposition, especially for Bayluscide. T e rate of removal by these processes is inversely af ected by pH. Hydrolysis and volatilization were not signifcant contributors to the breakdown of lampricides in the environment. Biotic processes appear less important to TFM, where water and sediment concentrations are below detectable limits before microbial breakdown can reduce TFM to non-detectable levels in the stream environment. Microbial activity, however, is important in the transformation of Bayluscide. T e non-target ef ects of TFM, as used in the Sea Lamprey Control Program, are limited to the aquatic environment. Birds and mammals that may drink from, swim in, or consume larval Sea Lampreys killed SEA LAMPREY CONTROL 657 by TFM treatment, are not af ected (Hubert 2003). In general, hard-bodied macroinvertebrates are less susceptible to TFM than soft-bodied macroinvertebrates, with aquatic annelids having the potential to be eliminated from a tributary after TFM treatment (Gilderhus et al. 1975). T e ef ects of TFM in concentrations suffcient to kill larval Sea Lampreys was estimated for stream invertebrates by Maki et al. (1975), based on the results of toxicity assays. Maki et al. (1975) found populations of annelids and black fy larvae would be reduced by 50 percent, three genera of mayfies would “suf er high mortalities” and the caddis fy Chimarra obscura would be virtually eliminated. Field observations support laboratory results, indicating signifcant mortality on the mayfy genus Hexagenia (Gilderhus and Johnson 1980). Torblaa (1968) and Maki (1980, cited in ACSCEQ 1985), however, found that abundance within pool and riffe stream assemblages before and after lampricide treatment were not signifcantly dif erent, despite the fact that the number of macroinvertebrates was reduced between 64 percent and 80 percent one day after treatment. One of the most notable ef ects was a ten-fold increase in the number of macroinvertebrates drifting downstream (drift rate) immediately after the start of TFM application, with a decline to a stable drift rate of twice the initial rate within three hours. Both authors noted a rapid recovery of macroinvertebrates within six weeks. Sampling one year post-treatment indicated a full recovery of the diversity and abundance of major taxonomic groups. As with macroinvertebrates, teleosts exhibit a range of sensitivity to TFM. T e ef ect of TFM on fsh varies with life stage, physiological condition, and species. In general, smaller fsh of any species are more susceptible than larger specimens of the same species, with the exception that eggs and sac fry are robust to the ef ects of TFM (Boogaard et al. 2003). Fish weakened from the rigors of spawning or through disease are also more susceptible to TFM. A number of studies have examined the ef ects of TFM on teleosts. Dahl and McDonald (1980) examined feld records from 1,300 lampricide treatments and found suckers (Catastomous spp.) were the most widely af ected by TFM, but the Stonecat (Noturus favus) was the most dramatically af ected, signifcantly reducing Stonecat abundance in fve of the nine tributaries in which it occurs in the western end of Lake Superior. Despite the toll that lampricide application has on Stonecats, in-stream refugia are found in some smaller tributaries not treated and their populations have not been completely extirpated. A similar situation exists for the Stonecat populations in northwestern Lake Ontario (Dahl and McDonald 1980). Other species that commonly experience some mortality during lampricide application include the Brown Bullhead (Ictalurus nebulosus), Brown (Salmo trutta) and Rainbow (Oncorhynchus mykiss) Trout, Northern Pike (Esox lucius), and Walleye (Sander vitreus), with smaller fsh, such as Logperch (Percina caprodes) and Trout Perch (Percopsis omiscomaycus), also suf ering higher rates of mortality during TFM treatment (Dahl and McDonald 1980; ACSCEQ 1985). Of particular concern is the Lake Sturgeon (Acipenser fulvescens), in which laboratory studies have shown that young-of-year Lake Sturgeon less than 100 mm total length are as susceptible to TFM as larval Sea Lampreys, although survival was improved by using a TFM/1 percent Bayluscide mixture (Boogaard et al. 2003). T ese observations on Lake Sturgeon resulted in changes to lampricide application protocols in the United States, by using lower lampricide concentrations applied later during the year to reduce the impacts on young-of-year Lake Sturgeon (Adair and Young 2004), although, during recent years, Michigan and Wisconsin have removed restrictions on concentration in response to concerns that lampricide treatment effcacy was being compromised. Canada has not adopted restrictions to concentration or timing of lampricide treatments, because feld observations of non-target impacts since the 1960s have not demonstrated 658 Michael J. Siefkes et al. that lampricides are inficting undue mortality on Lake Sturgeon, which is consistent with observations made during lampricide treatments in the United States over the same period. Recently, an in situ study has shown that survival of young-of-year Lake Sturgeon exposed to lampricides during treatment was identical to that in a control group (94 percent; Tom Pratt, personal communication). In addition, research has shown that Sea Lamprey mortality on Lake Sturgeon adults and sub-adults is signifcant (Patrick et al. 2009) and that protecting adults from mortality provides the most beneft to population maintenance and rehabilitation (Sutton 2004). T ese studies have led to a reevaluation of the benefts of using less lampricide and delaying treatment to later in the year, when more variable environmental conditions can hamper the delivery of ef ective lampricide treatments. Teleosts are not the only aquatic vertebrates af ected by TFM. T e Mudpuppy (Necturus maculosus), a native amphibian of the Great Lakes region, also experiences some mortality during lampricide application (Gilderhus and Johnson 1980). Lampricide toxicity tests, however, indicate that adult Mudpuppy populations would not be signifcantly af ected by lampricide treatments (Boogaard et al. 2003). Additional tests are needed to determine the toxicity of lampricides to juvenile Mudpuppies. By far, the greatest non-target ef ect of TFM has been on the native lamprey species: the non-parasitic American Brook (Lampetra appendix) and Northern Brook (Ichthyomyzon fossor) Lampreys, and the parasitic Silver (Ichthyomyzon unicuspis) and Chestnut (Ichthyomyzon castaneus) Lampreys. As all lamprey species in the Great Lakes have similar spawning requirements and virtually identical larval habitat requirements, the overlap among species in some tributaries is inevitable. Although laboratory studies have demonstrated that the Sea Lamprey is slightly more susceptible to TFM than the native lamprey species (Davis 1970), the dif erence is negligible and insuffcient to enable the selective removal of larval Sea Lampreys from tributaries inhabited by native lamprey species (Dawson et al. 1975). T e biology of the Silver Lamprey is most like the Sea Lamprey, and the Silver Lamprey has been the most af ected by TFM treatments. Schuldt and Goold (1980) reported a capture of 4,278 Silver Lampreys in Lake Superior electrical weirs during 1959, but only 91 were captured during the fve year span from 1973 to 1977, including the catch from the St. Marys River. T e decline in Silver Lampreys can be attributed to the ef ects of lampricide application to mutually shared natal tributaries and, to a lesser extent, the ef ects of the Sea Lamprey barrier program limiting the access of spawning-phase Silver Lampreys to suitable spawning habitats. Non-parasitic native lamprey species are less impacted by Sea Lamprey control activities. T e lack of a parasitic phase in the Brook Lampreys means they do not leave their natal tributary in search of a blood meal, and their presence in the head waters of tributaries above barriers provides a refuge from Sea Lamprey control activities and a source of Brook Lampreys to repopulate the tributary after TFM treatment. T e various forms of Bayluscide are less species-specifc than TFM and, as such, can have wider ef ects on non-target species. Powdered bayluscide is used in conjunction with TFM in a 98:2 or 99:1, TFM:Bayluscide ratio to reduce the amount of TFM required to treat high discharge tributaries. T ese mixtures follow the same toxicity patterns to fsh and invertebrates that a TFM-only treatment exhibits, but the LC50 for many species is lower in the TFM:Bayluscide powder mixture (ACSCEQ 1985; Boogaard et al. 2003). T e most acute non-target ef ect is observed when using Bayluscide granules. As Bayluscide granules are designed to sink to the substrate before the active ingredient is released, bottom-dwelling species are most often af ected, with species more commonly found in the water column able to swim out of the SEA LAMPREY CONTROL 659 application area. As expected, mollusks are particularly susceptible to Bayluscide, with both snails and clams experiencing signifcant, sometimes complete, mortality within the treated area (ACSCEQ 1985). Invertebrates, such as oligochaetes, turbellarians, and leeches also experience high rates of mortality (Dawson 2003). Bayluscide is more toxic to teleosts than TFM. As with TFM, free-swimming, exogenously feeding life stages are most susceptible, whereas eggs and sac fry are relatively resistant to Bayluscide (Dawson 2003). Because the granular formulation of Bayluscide is less selective than TFM for controlling Sea Lampreys, Bayluscide is not used as a lampricide for stream-wide application. Granular Bayluscide use is limited to evaluating and controlling populations in areas in which TFM is typically not ef ective, such as lentic or estuarine areas of tributaries. As the application of lampricides are generally limited to once every three to fve years, and the duration is no longer than sixteen hours in any single application, the long-term ef ects of lampricide control on most non-target species, with the exception of the native lamprey, are minimal.

Scheduling Lampricide Applications

Although there are approximately 5,400 tributaries to the Great Lakes, only 450 have produced Sea Lampreys (fg. 3; table 1). Funding is not suffcient to allow treatment of all tributaries that may produce Sea Lampreys within a year; consequently, a method of selecting tributaries for treatment is required. T e long history of Sea Lamprey Control Program enables the control agents to forecast when a tributary is expected to produce parasitic-phase Sea Lampreys. Consequently, approximately one-half of the tributaries currently selected for lampricide treatment during a given year are selected using this knowledge. T e other half are selected from a rank list of tributaries using cost per larval Sea Lamprey killed. T e scheduling of tributaries for treatment begins as much as eighteen months before the lampricide is actually applied. Larval Sea Lamprey population assessment is a critical component of Sea Lamprey control. T e presence, abundance, and size structure of larval Sea Lamprey populations in approximately two hundred tributaries and lentic areas throughout the Great Lakes basin are evaluated each year, one year prior to the expected recruitment of parasitic-phase Sea Lampreys to the lake (Christie et al. 2003). Larval Sea Lamprey populations are sampled using one of two methodologies: backpack electrofshing in waters

TABLE 1. Numbers of Tributaries to Each Great Lake, Including Historically Infested, Treated, and That Are Regularly Treated Due to Consistent Sea Lamprey (Petromyzon marinus) Recruitment and Growth

NUMBER OF TRIBUTARIES

LAKE TOTAL TRIBUTARIES INFESTED BY SEA LAMPREYS TREATED AT LEAST ONCE REGULARLY TREATED Superior 1,566 148 84 53 Huron 1,761 117 71 45 Michigan 511 121 72 34 Erie 842 22 9 5 Ontario 659 65 39 29

FIG. 3. Historic distribution of Sea Lamprey (Petromyzon marinus)-producing tributaries to the Great Lakes.

Great Lakes Fishery Commission. 662 Michael J. Siefkes et al. that are less than 0.8 m deep (Slade et al. 2003) and with granular Bayluscide in waters too deep or turbid to allow ef ective sampling using electrofshing gear (Weise and Rugen 1987). Initial methods to evaluate whether a tributary required lampricide treatment were based primarily on the subjective interpretation of sampling data by control agent biologists (Weise and Rugen 1987; Christie et al. 2003). T e basin-wide allocation of treatment resources among tributaries on both sides of the border necessitated the development of standardized sampling techniques to enable a more objective evaluation of the need to treat tributaries (Slade et al. 2003). Initial protocols focused on the development of index stations within each Sea Lamprey-producing tributary, accompanied by mark-recapture estimates of larval Sea Lamprey abundance at the time of treatment to determine the relative accuracy of abundance at the index stations, both within and among tributaries (Weise and Rugen 1987). More rigorous methods to estimate the abundance of larval Sea Lampreys, as well as the potential production of newly metamorphosed Sea Lampreys, began in 1995 (Slade et al. 2003). Standardized protocols were developed to estimate the density and size structure of the larval Sea Lamprey population, as well as evaluate the quantity and quality of larval habitat in Great Lakes tributaries (Christie et al. 2003). T ese measures of larval Sea Lamprey density and available larval habitat are inputs into the Empiric Stream Ranking Model (ESTR; Christie et al. 2003), in which they are combined with estimates of sampling effciency, growth, and metamorphosis to derive tributary-specifc estimates of the abundance of large Sea Lamprey larvae during the fall of the year of sampling and forecast the production of parasitic-phase Sea Lampreys the following year (Christie et al. 2003). Methods used to rank tributaries for lampricide application were reviewed, and several recommendations to improve the ability to estimate larval Sea Lamprey abundance within a tributary were made, including increased sampling of less-preferred larval habitats, reducing uncertainties associated with larval growth and metamorphosis parameters, and a better understanding of the factors that contribute to variation in larval density (Hansen et al. 2003). During the previous decade, several parameters of the ESTR model were refned, including electrofsher sampling effciency (Steeves et al. 2003), metamorphosis (Treble et al. 2008), and larval Sea Lamprey habitat use (Sullivan 2003), and the uncertainty in model parameters has been quantifed (Steeves 2002). To rank tributaries for treatment, the abundance of large larvae in each tributary is divided by the tributary-specifc cost of lampricide application to calculate a per-dollar cost to kill each transformer, and all tributaries sampled each year are ranked based on the cost per kill value (Christie et al. 2003; Slade et al. 2003). T e amount of control ef ort that can be expended annually is known, and as many tributaries as possible are treated with this control ef ort, starting with the lowest cost per kill tributary. Ranking of tributaries for lampricide treatment is done across the Great Lakes basin, regardless of lake. During 2008, the control agents changed the sampling protocol for wadable waters and the criteria used to rank tributaries for lampricide treatments (Hansen and Jones 2008). T e methods used between 1995 and 2008 were labor-intensive, such that a signifcant portion of the Sea Lamprey control budget was spent assessing tributaries for treatment, rather than actually applying lampricides. T e new methods build on the information collected since 1995, and the control agents now sample only the best quality habitat in each tributary. T e new method reduces the amount of time spent collecting data by 40 percent, and the time saved can be applied to lampricide treatments. T e ranking criterion in the ESTR model was also changed from the forecast of parasitic-phase production the year after assessment to the abundance of larvae greater than100 mm in the year of assessment. T e ranking criteria change reduces the overall uncertainty, by removing the uncertainty associated with the model of metamorphosis within ESTR SEA LAMPREY CONTROL 663

(Steeves 2002) and the tributary-specifc ef ects not captured in the ESTR program (Treble et al. 2008). Although the new method results in less precise estimates of larval Sea Lamprey abundance overall, the added uncertainty is compensated for by increased lampricide treatments and, thus, Sea Lamprey control each year (Hansen and Jones 2008). Methods of assessing larval Sea Lamprey populations in deep and turbid tributaries and lentic areas dif er from the usual methods required, as backpack electrofshing is not ef ective in these areas. As- sessment begins with an evaluation of the location and amount of suitable larval habitats. Prior to 2007, assessment was done using a labor-intensive method of collecting dredge samples of substrate along transects placed throughout the suspected infested area. Although the use of dredge sampling continues for evaluation of estuarine habitat in small and medium-sized streams, the control agents have adapted georeferenced RoxAnn sonar technology to enable a more rapid and comprehensive collection of substrate data to evaluate suitability to harbor larval Sea Lampreys in large estuaries and adjacent lentic areas. T e data collected using RoxAnn sonar and the resulting habitat areas are sampled using a dredge to verify substrate composition. Larval Sea Lamprey abundance, size structure, and distribution are determined by spreading granular Bayluscide over a number of plots throughout the surveyed area. A target treatment area is identifed and the same cost per kill criterion is calculated for larvae greater than 100 mm to rank these deep and turbid tributaries and lentic areas along with tributaries for lampricide treatment. One exception to the application of assessment methods just described is the St. Marys River. T e St. Marys River was discounted as a major contributor of Sea Lampreys to Lakes Huron and Michigan during the 1970s and 1980s (Schleen et al. 2003), but the ef ects of remediation led to an estimated larval Sea Lamprey population of 6.2 million during 1987 (Eshenroder et al. 1987). Flow modeling (Shen et al. 2003) indicated that a traditional TFM treatment would not be ef ective on the St. Marys River (Schleen et al. 2003). T ere was an obvious need to identify areas of high larval Sea Lamprey abundance to enable large-scale granular Bayluscide applications to control Sea Lampreys in the St. Marys River. As a solution, a backpack electrofsher was modifed to enable samples to be taken from deep water areas, coupled with a GPS system and mounted on a pontoon boat, to allow specifc densities of larval Sea Lampreys to be mapped. Between 1993 and 1996 a total of 11,809 points were sampled over 71 km2 of river (Fodale et al. 2003) and the areas of highest density demarcated.

Applying Lampricides

During the initial years of the lampricide control, static bioassays conducted prior to lampricide treatments were used to determine a safe, yet ef ective, concentration of TFM (Johnson and Stephens 2003). T e application of a fxed volume of TFM, however, did not always result in ef ective treatments. Initial measures of stream discharge could be inaccurate, resulting in too high or low a concentration of TFM in the river and either unacceptable non-target mortality or insuffcient toxicity to kill larval Sea Lampreys. In addition, application of lampricides for no more than the requisite nine hours of minimum lethal concentration could result in the lengthening of the lampricide block through areas of higher water velocity, whereas backwater areas, often containing the highest density of larval Sea Lampreys, took longer for TFM to accumulate to the proper concentration, and resulted in inef ective treatments. T e need to adapt TFM concentrations to changing stream conditions necessitated the ability to measure concentrations of TFM on the order of milligrams per liter (parts per million, ppm), while being 664 Michael J. Siefkes et al. applied to the tributary (Johnson 1961). During 1960, Smith et al. (1960) developed a colorimetric method to quantify TFM concentrations in the tributary, and application rates could be changed to compensate for changes in discharge. At the same time that the colorimetric method of measuring TFM concentration was being developed, initial testing of TFM demonstrated that the toxicity of the compound was af ected by chemical and physical parameters of the water (Howell et al. 1964). Lower temperatures have been shown to decrease toxicity of TFM to non-target species, but toxicity to larval Sea Lampreys is not similarly reduced. Alkalinity and pH have the largest ef ect on TFM toxicity, with an increase in these parameters requiring a higher concentration of TFM to kill larval Sea Lampreys (Kanayama 1963; Johnson and Stephens 2003). Tributaries that fow over the Canadian Shield have lower pH and alkalinities and require less TFM to achieve the same level of toxicity than do tributaries of Lakes Ontario, Erie, or Michigan. T e U.S. Geological Survey in La Crosse, Wisconsin, developed standardized charts to enable control agents to forecast the required concentration to kill larval Sea Lampreys through standard measurement of chemical and physical properties immediately prior to TFM application (Bills et al. 2003). Once the list of tributaries to be treated is fnalized, during the winter of a given year, the control agents begin extensive consultation and application for permits with provincial, state, and tribal fsheries and environmental management agencies. T e presence of threatened or endangered species within the proposed treatment area is taken into consideration, and treatment plans are adapted as needed. T e present protocol for the application of TFM combines elements of the current stream-specifc conditions with experience from previous treatments of the same or similar tributaries (Smith and Tibbles 1980). Discharge, pH, alkalinity, dissolved oxygen, and temperature are measured precisely over the course of the treatment, beginning one or two days prior to TFM application. Some treatments also require verifcation of the required TFM concentrations forecasted by the standardized charts through stream-side bioassays using larval Sea Lampreys collected from the target tributary (Johnson and Stephens 2003). Once the target lampricide concentration is determined, application points are mapped based on the distribution of larval Sea Lampreys and the requirement to augment lampricide concentration at specifc access points to accommodate additional water inputs, such as tributaries or groundwater infltration. Sample points to determine lampricide concentration are also identifed based on the fow timing of the lampricide moving through the system. In newly infested tributaries, or in tributaries in which current discharge is outside of previous treatment experience, a dye study may be conducted prior to lampricide treatment to gather information on fow timing and dilution and to identify problem areas. Although the majority of larval Sea Lampreys are found within the fowing portion of Great Lakes tributaries, some populations exist in lentic areas, including sheltered bays closely associated with Sea Lamprey-producing tributaries, as well as within the deep sections of channels and rivers that connect the Great Lakes, such as the St. Marys, St. Clair, and Niagara rivers. Contributions to Sea Lamprey populations from lentic areas were originally thought to be negligible, as these areas were presumably harsher conditions for larval Sea Lampreys, with fewer nutrients and degree days to accumulate the length required for metamorphosis (Smith and Tibbles 1980). T e use of aging techniques on Sea Lamprey statoliths (Beamish and Medland 1988), a structure analogous to otoliths in teleosts, for both larval and recently metamorphosed Sea Lampreys, demonstrated that larval Sea Lampreys in the St. Marys River transformed in four to seven years (Schleen et al. 2003) and that signifcant recruitment of Sea Lampreys to lakes Huron and Michigan from the St. Marys River was occurring. Investigation into the recruitment of Sea Lampreys from lentic areas is currently being conducted (B. Swink, Hammond Bay Biological Station, Millersburg, SEA LAMPREY CONTROL 665

Michigan, personal communication), but the observation of large larvae and transformers, during lentic surveys and treatments, indicates Sea Lampreys can complete the larval life stage in lentic environments. T e use of TFM is not an acceptable control method for lentic areas because of rapid dilution in lentic areas and the immense costs incurred by treatment of connecting channels by virtue of their large discharge and complexity (Schleen et al. 2003). Bayluscide granules are used to treat these areas and are applied from boats, using broadcast type spreaders, which can produce Bayluscide dust, requiring the use of safety equipment by control agents. Recently, a new type of spray boat that applies a dust-free Bayluscide granule/water slurry has been developed for faster, safer lentic area treatments

The Future of Lampricide Control

Lampricide application has been the cornerstone of the Sea Lamprey Control Program since 1958. Cur- rent strategies to target and apply lampricides, however, have resulted in an annual average of 430,000 spawning-phase Sea Lampreys in the Great Lakes basin. Innovative strategies to apply lampricides within and among tributaries are required to further reduce Sea Lamprey abundance. One such strategy involves the treatment of all nine Sea Lamprey-producing tributaries on Lake Erie, during two consecutive years, taking advantage of the signifcant and immediate reduction in Sea Lamprey abundance observed following the initial treatments during 1986. Although treating all Sea Lamprey-producing tributaries in consecutive years is applicable to Lake Erie, given the low number of Sea Lamprey-producing tributaries, other approaches are required for the remaining lakes. For example, models of Sea Lamprey control have consistently indicated that repeated treatment of large populations reduces larval Sea Lamprey abundance over time (Treble 2006; Jones et al. 2008). An application strategy that ensures these populations are successfully treated would increase the probability of success. T e mode of toxic action of TFM and Bayluscide to larval Sea Lampreys is not fully understood (Dawson 2003; Hubert 2003; McDonald and Kolar 2007) but is associated with the inability to detoxify TFM in the liver (Lech and Statham 1975). Recent research indicates TFM interferes with oxidative ATP production, which causes death through starvation (Wilkie et al. 2007). Research into the modes of uptake, location of toxic action, and the physiological detoxifcation of lampricides in larval Sea Lampreys and teleosts is also currently in progress. Research results may enable the development of dif erent formulations of lampricides that retain selective toxicity to larval Sea Lampreys, while reducing ef ects on non-target species.

Alternative Sea Lamprey Control Techniques

In addition to the application of selective lampricides, alternative control techniques have become increasingly important, as part of an integrated pest management (IPM) approach to Sea Lamprey control. T e GLFC originally endorsed an IPM approach during the 1970s (Policy Statement of the GLFC adopted December 1, 1975, and Guidelines for Barrier Dam Program for Sea Lamprey Control, June 16, 1977; for details see U.S. Department of the Interior 1978) and further embraced the concept of IPM, based on recommendations from the proceedings of SLIS I (see Sawyer 1980). During the 1980s, the GLFC commit- ted to the concept of IPM through development of policy on the integrated management of Sea Lampreys (IMSL; Sawyer 1980; Davis et al. 1982; Christie and Goddard 2003). T e IMSL policy allowed development of alternative controls (both old ideas and new ideas) for use in Sea Lamprey control. To date, three 666 Michael J. Siefkes et al. alternative control techniques have been used, including blocking spawning-phase Sea Lampreys from reaching spawning grounds using barriers, trapping and removing spawning-phase Sea Lampreys from the spawning population; and using sterilized spawning-phase male Sea Lampreys to reduce reproductive potential in isolated spawning populations.

Sea Lamprey Barriers

T e development and use of Sea Lamprey barriers to reduce recruitment, by limiting the number of tributaries and amount of spawning and larval habitat used by Sea Lampreys, is well documented in the SLIS I and SLIS II special issues (Hunn and Youngs 1980; Lavis et al. 2003a). During early Sea Lamprey control ef orts, mechanical and electrical barriers to spawning-phase Sea Lamprey migration and reproduction in Great Lakes tributaries were the main focus. After the development of lampricides and the recognition that barriers reduced species richness of native or desirable migratory fshes and their habitats (McLaughlin et al. 2006), the role of barriers in Sea Lamprey control was diminished. T e use of barriers, however, is an ef ective tool to control Sea Lampreys in certain situations, providing an alternative to lampricide control on tributaries in which physical, chemical, or other constraints made lampricide treatments diffcult, expensive, or inef ective. Barriers also reduce the number of tributaries needing regular lampricide treatments, saving time, ef ort, lampricide, and money. Because of these benefts, Sea Lamprey barriers will continue to be part of the Sea Lamprey Control Program.

Mechanical Weirs

T e frst attempts at Sea Lamprey control in the Great Lakes were made by installing mechanical weirs in tributaries, to block spawning-phase Sea Lampreys from reaching spawning areas. Early designs included permanent weirs with associated traps to block and capture Sea Lampreys in larger tributaries; screen weirs and associated traps that were portable to block and capture Sea Lampreys in small and medium-sized tributaries; barrier dams to block Sea Lampreys; and dams with inclined screen traps to block Sea Lampreys, but also capture downstream migrating Sea Lampreys that have transformed (Applegate 1950a; Applegate and Smith 1951a, 1951b; Applegate and Brynildson 1952; Applegate et al. 1952; Hunn and Youngs 1980). T e frst mechanical weir was constructed during 1944 on the Ocqueoc River, a Lake Huron tributary; however, the weir was not successful in blocking spawning-phase Sea Lampreys (Shetter 1949). T e frst successful weir was constructed during 1947 on the Black Mallard River, another tributary to Lake Huron. T e Black Mallard River weir was constructed out of steel grating and blocked nearly 100 percent of the Sea Lamprey run from 1947 to 1949 (Applegate 1950a). During 1948, a weir similar to the Black Mallard River weir was constructed on the Ocqueoc River and was operational well into the 1950s. In general, permanent or portable weirs constructed with steel grating and associated traps, such as the Black Mallard and Ocqueoc weirs, were the best design at the time, achieving some measure of Sea Lamprey control (Hunn and Youngs 1980), and were constructed in many tributaries to lakes Huron, Michigan, and Superior during 1950 (Applegate and Smith 1951a). Although steel-grating mechanical weirs did provide some Sea Lamprey control, they also presented problems. For instance, the relatively small mesh clogged easily with debris, especially during ice-out, foods, and other periods with high debris loads causing these weirs to frequently fail (Applegate 1950a). SEA LAMPREY CONTROL 667

To help prevent the weirs from failing, frequent checks were made to clear the mesh of debris and inspect the integrity of the weir (Applegate 1950a); however, these frequent checks made the weirs expensive to operate and maintain. Steel grating weirs also proved to be expensive to build (Hunn and Youngs 1980). T ese shortcomings inspired the search for better barrier designs and, eventually, steel-grating weirs were phased out. Today, very few steel-grating weirs are in operation and are not expected to block 100 percent of the Sea Lamprey run but are used, instead, to direct spawning-phase Sea Lampreys into traps.

Electromechanical Barriers

Experiments began in 1951 to develop barriers that could overcome the defciencies of the early mechanical weirs (Hunn and Youngs 1980). Several types of alternating current (AC) electrical barriers have been described (Applegate et al. 1952; Erkkila et al. 1956; Hunn and Youngs 1980) and were placed in tributaries to Lake Superior during 1953, to test their usefulness in blocking spawning-phase Sea Lampreys (McLain et al. 1965). Traps were often installed along with the electrical barriers, but the traps often interrupted the electrical feld, allowing Sea Lampreys to pass through the barrier (Hunn and Youngs 1980). Subsequently, the felds of electrical barriers that contained traps were modifed, and traps were moved downstream to establish uninterrupted electrical felds from bank to bank that would successfully block all Sea Lampreys. T e AC electrical barriers developed proved more cost-ef ective and effcient at blocking Sea Lampreys, when compared to mechanical weirs, and, by 1960, 162 electrical barriers had been installed in the United States and Canada (Smith and Tibbles 1980). Excessive mortality of non-target fshes was a continuous problem associated with early AC electrical barriers, and, therefore, the electrical felds were modifed (Erkkila et al. 1956; see McLain 1957 for a review of non-target mortality associated with early electrical barriers). Pulsed direct current (DC) was used to direct fsh away from the AC barriers (McLain and Nielsen 1953; McLain 1957; McLain et al. 1965) and was successful at reducing mortality, but mortality was not eliminated. Eventually, fueled by the development of selective lampricides (Smith and Tibbles 1980) and the non-target mortality and frequent breakdown issues associated with the AC electrical barriers, AC electrical barriers were phased-out of the Sea Lamprey Control Program (Lavis et al. 2003a). Although the early AC electrical barriers had the potential to block entire runs of Sea Lampreys (McLain et al. 1965), they probably did not have a signifcant impact on Sea Lamprey control (Smith and Tibbles 1980). T e ef ects of the electrical barriers on Sea Lamprey populations were impossible to measure (McLain et al. 1965), because most were operated for only a short period of time and a complete system of electrical barriers was never realized within a lake (Hunn and Youngs 1980). Today, electrical barriers have been all but eliminated from the Sea Lamprey Control Program. Electrical barriers evolved to use pulsed DC generators and bottom-mounted electrodes to produce an electrical feld perpendicular to the stream fow (Lavis et al. 2003a), and have only been constructed on the Jordan (Lake Michigan), Pere Marquette (Lake Michigan) and Ocqueoc (Lake Huron) rivers. T e Jordan River electrical barrier, built during 1988, only operated for eight years. Failure to block spawning-phase Sea Lampreys and eliminate the need for lampricide treatments made the Jordan River electrical barrier no longer cost-ef ective to operate. T e Pere Marquette River electrical barrier, built during 1988 and refurbished with a fsh passage device during 1999, is still in operation but will likely suf er the same fate as the Jordan River electrical barrier. T e Ocqueoc River electrical barrier is actually a hybrid low-head, 668 Michael J. Siefkes et al. fxed-crest, and electrical barrier (built during 1999). T e hybrid design allows for constructing a smaller- crested barrier, reducing environmental and economic costs, on systems prone to spring fooding. T e Ocqueoc River barrier has been successful at blocking Sea Lampreys, and the design is a model for tributaries with similar qualities that limit construction of conventional barriers.

Barrier Dams

Much like mechanical weirs and electrical barriers, the use of dams to block spawning-phase Sea Lampreys was investigated during the infancy of the Sea Lamprey Control Program. During 1951, a wooden low-head barrier with a steel overhanging “lip” was constructed in the Black River (Lake Michigan), to test its design in blocking Sea Lampreys; it was operated until 1957 (Applegate and Smith 1951b; Stauf er 1964; Hunn and Youngs 1980). During 1957, the frst low-head barrier to specifcally block Sea Lampreys was built in the Harris River (Lake Huron). Other low-head barrier projects were conducted on Cayuga Lake (Wigley 1959; Webster and Otis 1973). T ese early low-head barrier studies helped provide valuable information on the design of low-head barriers for use in Sea Lamprey control, such as minimum crest height during Sea Lamprey migration and the addition of an overhanging “lip” to the top of the dam (Hunn and Youngs 1980). Almost all purpose-built Sea Lamprey barriers constructed since the 1950s have been of the low- head, fxed-crest, with an overhanging “lip” design (Lavis et al. 2003a). Other Sea Lamprey barrier designs have emerged over the years largely to deal with fuctuating water levels and in response to concerns about the impacts of barriers on non-target fsh; however, they are not often used. T ese designs include low-head, adjustable-crest barriers, velocity barriers, and hybrid low- head/electrical barriers (Lavis et al. 2003a). Adjustable-crest barriers have been designed to be manually or automatically adjusted and to allow crest height to be lowered or the barrier to be removed entirely when Sea Lampreys are not migrating in the tributary, allowing the passage of non-target fsh. Adjustable designs, however, also increase the chance of spawning-phase Sea Lampreys escaping upstream, which would negate the benefts of the barrier and not reduce the need for lampricide treatment. A velocity barrier was constructed on the MacIntyre River (Lake Superior) and was subsequently removed because of its failure to block Sea Lampreys. T e water velocity needed to overcome the burst speed of a Sea Lamprey is likely impractical to achieve (Hunn and Youngs 1980). Low-head, electrical barriers like the one operating on the Ocqueoc River have shown promise. Other barriers not constructed primarily to block spawning-phase Sea Lampreys are also important to Sea Lamprey control. T ese barriers include the modifcation of natural waterfalls into permanent structures that block Sea Lampreys and, more importantly, existing dams originally built for other purposes (Smith and Tibbles 1980). T ese dams have been termed de facto Sea Lamprey barriers during recent years and have presented a unique set of issues for the Sea Lamprey Control Program. T ere are literally thousands of existing dams within the Great Lakes basin, and many of these add some value to Sea Lamprey control. T ere has not been a thorough inventory of these dams, so identifying and tracking the condition of those that are critical to Sea Lamprey control has been diffcult. A database that will identify all dams important to Sea Lamprey control within the Great Lakes basin is currently under construction. As important dams age and begin to fail and support for dam removals to create free-fowing lotic systems and promote access for fsh to upstream habitats grow (McLaughlin et al. 2007), the barrier database will be critical in identifying situations that would jeopardize Sea Lamprey control. SEA LAMPREY CONTROL 669

T e ef ects of Sea Lamprey barriers on stream habitats and non-target fsh species has always been an issue for the Sea Lamprey Control Program. Although few studies have been published on the impacts of low-head Sea Lamprey barriers to the biological integrity of river systems (Lavis et al. 2003a), the impacts are typically less than their larger counterparts, because crest heights are rarely high enough to signifcantly impound water behind them. Impacts can, however, be signifcant for non-jumping fsh species (Dodd 1999; Porto et al. 1999; Noakes et al. 2000). T e Sea Lamprey Control Program has adopted barrier designs to minimize the ef ects to non-target species. For example, the crest heights used in low-head barrier designs easily allow the passage of jumping fsh. Jumping pools are also often constructed with these structures to assist in jumping fsh passage. In addition, adjustable crest designs can be removed when spawning-phase Sea Lampreys are not migrating, allowing the passage of all fsh. Furthermore, experiments with other means of fsh passage, such as fsh ladders and vertical slot, trap-and-sort fshways, are being conducted.

Barrier Policy

T e use of barriers in Sea Lamprey control pre-dates the formation of the GLFC and was the main focus of the Sea Lamprey Control Program until selective lampricides were developed for wide-scale use. Even with the shift to lampricides, the GLFC endorsed the continued use of barriers in the Sea Lamprey Control Program as an alternative control method. T e GLFC, however, did not formalize a barrier program until the late 1970s. Prior to the formation of the GLFC barrier program, federal, state and provincial entities were largely responsible for the construction of Sea Lamprey barriers (Lavis et al. 2003a). During 1971, the GLFC recommended the formation of barrier task forces in the United States and Canada that would plan construction and integrate barriers into the Sea Lamprey Control Program (GLFC 1973). T ese task forces produced a rank list of Sea Lamprey-producing tributaries for the installation of barriers based on several criteria, including larval Sea Lamprey population size, lampricide treatment cost and ef ectiveness, and ef ects of lampricide application on non-target species (Lavis et al. 2003a). By 1975, the GLFC fully recognized the usefulness of barriers and adopted a policy statement that offcially established the GLFC barrier program and encouraged federal, state, and provincial governments and the GLFC to cooperate in the installation of barriers (Lavis et al. 2003a). Funds were frst allocated specifcally for the Sea Lamprey barrier program beginning in 1978, and three barriers were constructed by 1979. During the next three decades, the importance of the barrier program cycled. T e Sea Lamprey barrier program gained momentum during SLIS I, with the continued emphasis on an IPM approach to Sea Lamprey control (Sawyer 1980) and the indication that barrier construction costs could be decreased, because the crest height needed to block spawning-phase Sea Lampreys was shown to be lower than expected (Hunn and Youngs 1980). T e momentum gained during SLIS fueled the construction of thirty- one Sea Lamprey barriers between 1980 and 1989 (Lavis et al. 2003a). Barrier construction waned during the early 1990s, mostly because the escalating costs of lampricides required much of the Sea Lamprey control budget and only two Sea Lamprey barriers were built, both in Canadian tributaries, from 1990 to 1993 (Lavis et al. 2003a). T e barrier program experienced a renaissance during 1993, with the publication of the GLFC vision, which stated barriers would be used to help reduce lampricide use by 50 percent of 1980 levels by the year 2000 (GLFC 1992). T e new vision allowed the United States and Canada to hire full-time barrier coordinators to formulate a unifed, basin-wide barrier program (Lavis et al. 2003a). From 1994 to 1998, the GLFC investment in the barrier program increased more than three-fold, the U.S. Army 670 Michael J. Siefkes et al.

Corp of Engineers became a valuable partner in the construction of Sea Lamprey barriers, and sixteen barriers were constructed (eight in the United States and eight in Canada; Lavis et al. 2003a). T e revival of the barrier program continued during the late 1990s and early 2000s, with the development of standard operating procedures and recommendations on ways to expand and accelerate the barrier program (Millar et al. 2000) and with the GLFC’s intent to use alternatives to lampricide treatments for at least 50 percent of Sea Lamprey suppression by 2010 (Christie and Goddard 2003); however, barrier construction never returned to levels achieved during the 1980s and 1990s (from 1998 to 2008, only ten new or replacement barriers were constructed). Presently, the barrier program has still not regained momentum because of increasing concerns regarding the environmental impact of barriers and diffculties in gaining landowner cooperation and acquiring real estate for barrier projects. Instead, the focus of the barrier program has shifted to the inventory, maintenance, and replacement of the many de facto Sea Lamprey barriers important to the Sea Lamprey Control Program.

The Future of Sea Lamprey Barriers

T e GLFC is still focused on delivering an integrated Sea Lamprey Control Program, and barriers are still the only ef ective alternative to lampricide control (Lavis et al. 2003a; see fg. 4 for the location of Sea Lamprey barriers). Future policy on barriers needs to continue educating the public about the value of Sea Lamprey barriers and encourage landowner participation in barrier projects. Also, new or replacement barrier projects will likely only be constructed on lands owned by corporations or governments or on private lands that have full landowner cooperation. In addition, barriers will not be constructed where the biological integrity of a tributary would be damaged beyond the benefts provided by the barrier. Furthermore, the barrier program will continue to focus on inventory, maintenance, and replacement of de facto Sea Lamprey barriers and fsh passage research, both of which will be particularly important in the cases of aging dams on rivers with huge Sea Lamprey production capability, such as rivers like the Black Sturgeon (Lake Superior), Manistique (Lake Michigan), and Saugeen (Lake Huron). Fish passage and human safety are issues for the future use of barriers in the Sea Lamprey Control Program. Research is ongoing to develop the most ef ective Sea Lamprey barrier, while mitigating safety and fsh passage issues (McLaughlin et al. 2003). Current Sea Lamprey barriers employing trap-and-sort fshways have been shown to have an attraction rate of 80 percent for tagged fsh but a highly variable passage rate of the attracted fsh (Pratt et al. 2009). Fish passage success has been correlated with consistency of attractant fow from the trap, fsh retention once in the trap, timing of operation of the fshway, and crest height of the barrier (Lavis et al. 2003a; Klingler et al. 2003; McLaughlin et al. 2007; Pratt et al. 2009). McLaughlin et al. (2007) identifed thirteen topics by which additional information could improve the ef ectiveness of barriers, while reducing the non-target ef ects and safety issues surrounding barriers, including placement of barriers and traps within tributaries, retention of all fsh species once trapped, and alternate designs for barriers, traps, and fshways that can selectively remove migrating spawning-phase Sea Lampreys.

Sea Lamprey Traps

During the early years of the Sea Lamprey Control Program, several methods were used to capture spawning-phase Sea Lampreys in tributaries as they migrated upstream to spawn. Dip nets (Applegate SEA LAMPREY CONTROL 671 and Smith 1951b), gill and trap nets (Smith and Elliot 1953), wooden-framed traps and barrier nets (Wigley 1959), and traps associated with mechanical weirs and electrical barriers (McLain et al. 1965) were all used to capture Sea Lampreys, by exploiting their strong innate migratory drive. In all cases, capturing Sea Lampreys worked best when the trapping device was associated with a barrier; barriers concentrate Sea Lampreys in a relatively small area and increase the chance they will repeatedly interact with the trapping device, thus, increasing the probability of capture. T e incorporation of two technological advances helped make spawning-phase Sea Lamprey trapping more cost-ef ective. T e frst was the incorporation of an easy to operate and maintain portable trap placed below natural Sea Lamprey barriers or dams (Schuldt and Heinrich 1982). T e second was to strategi- cally integrate a permanent trap or traps into existing barriers or to design new barriers with permanent barrier-integrated traps. Barrier-integrated traps consist of a concrete vault with a trap insert that can be lifted for easy servicing. T ese two designs require less maintenance and can be operated by smaller crews.

Trapping for Sea Lamprey Population Assessment

Although signifcant numbers of spawning-phase Sea Lampreys could be captured using traps, control agents quickly learned trapping methods were expensive to operate (Schuldt and Heinrich 1982), ineffcient, and could not remove enough Sea Lampreys from the spawning population to reduce reproductive potential and, therefore, were not likely to become a viable control method using existing technologies. Trapping Sea Lampreys did, however, provide a means of assessing populations through calculations of relative abundance and, thus, success of the Sea Lamprey Control Program. Since the late 1970s and early 1980s, spawning-phase Sea Lamprey populations have been assessed using traps in all of the Great Lakes (Mullett et al. 2003 and reference therein; fg. 5). Population estimates on some tributaries with barriers are determined through mark-recapture methods, using a modifed Schaefer (1951) estimate. Mark-recapture studies cannot be conducted in all trapped tributaries because of funding constraints. T erefore, in trapped tributaries, but without mark and recapture data, trap catch can be an indicator of Sea Lamprey abundance, if trapping operations are held constant from year to year. In untrapped tributaries, a model was developed to generate Sea Lamprey abundance estimates. T e model uses fve independent variables: drainage area, geographic region, larval Sea Lamprey production potential, number of years since last lampricide treatment, and spawning year. For each lake, abundance estimates for each Sea Lamprey-producing tributary are summed to generate a lake-wide spawning-phase Sea Lamprey abundance estimate, which is used as the primary metric to assess Sea Lamprey Control Program success.

Trapping for Sea Lamprey Control

Trapping spawning-phase Sea Lampreys is currently only considered a control strategy in the St. Marys River. T e St. Marys River, which connects lakes Superior and Huron, has unique characteristics that make it impractical to treat with TFM (Schleen et al. 2003). As an alternative to TFM treatments, an IPM approach consisting of trapping sterile-male releases and selective Bayluscide treatments was developed. Trapping Sea Lampreys from Great Lakes tributaries provides male Sea Lampreys for sterilization and release into the St. Marys River. Trapping Sea Lampreys from the St. Marys River removes viable individuals

FIG. 4. Location of tributaries with Sea Lamprey (Petromyzon marinus) barriers.

Great Lakes Fishery Commission.

FIG. 5. Location of tributaries with Sea Lamprey (Petromyzon marinus) traps.

Great Lakes Fishery Commission. 676 Michael J. Siefkes et al. from the population and provides more male Sea Lampreys to be sterilized and released back to the river. T e combination of trapping sterile-male releases and selective Bayluscide treatment has reduced the reproductive potential of the river about 90 percent. Finally, trapping Sea Lampreys also provides research and educational specimens to individuals and institutions across Canada and the United States.

The Future of Sea Lamprey Trapping

McLaughlin et al. (2007) details further development of spawning-phase Sea Lamprey trapping. Current research relevant to trapping has focused on better understanding Sea Lamprey behavior, both in the context of the physical environments of tributaries and of reproductive pheromones, and will provide exploitable information to enhance trapping by taking advantage of Sea Lamprey behavior. In addition, alternative trapping methods are also being developed to capture Sea Lampreys in larger tributaries, where conventional trapping methods are diffcult to conduct, as well as methods that function independent of Sea Lamprey barriers and capture transforming Sea Lampreys as they migrated downstream to the lakes. Current research will provide better population assessment, turn trapping into a viable control strategy in tributaries outside of the St. Marys River, and better integrate trapping with other control techniques. Trapping spawning-phase Sea Lampreys to generate abundance estimates in tributaries, and, ultimately, lake-wide abundance estimates, evaluate the entire Sea Lamprey Control Program. T e trapping program was reviewed by an expert panel during 1998, and several recommendations for improving the accuracy, precision, and value were made. One recommendation was to improve trapping on large rivers. Trapping is easier on smaller tributaries, and, therefore, the Sea Lamprey abundance model (Mullett et al. 2003) is largely based on information from these small systems. T e model would be improved, if more data from larger tributaries and other data sources, such as parasitic-phase abundance, could be incorporated into the model (Jones 2007). T e precision of mark-recapture estimates could be improved, if trapping effciency were increased. Progress on the current behavior and alternative trapping research should provide means to increase trapping effciency. Not only will trapping research increase the precision of spawning-phase Sea Lamprey abundance estimates, and, ultimately, measures of program success, it should also improve the ef ectiveness of using trapping as a control strategy through physical removal of a greater number of Sea Lampreys from trapped tributaries. Recent technologies, such as radio and acoustic telemetry and passive integrated transponder systems, provide unique tools for current and future research.

Sterile-Male-Release Technique

T e sterile-male-release technique, as proposed during 1937 by Knipling (1968), is a method of reproductive suppression to control pest species. Sterilized males are released to “over-food” the wild population of males and to cause the wild population of females to waste their reproductive potential. Reproduction of the pest is reduced in proportion to the prevalence of sterile to untreated males in the population. Sterilized males must exhibit suffcient sexual vigor to compete for mates and engage in normal mating behaviors. T e technique was frst used to eradicate the Screwworm Fly (Cochliomyia hominivorax) from the West Indies island of Curacao during 1954 (Baumhover 1966). Since then, the technique has been used worldwide to manage or eradicate many pest insect species (Klassen and Curtis 2005). SEA LAMPREY CONTROL 677

Investigations to fnd an ef ective means of sterilizing spawning-phase Sea Lampreys began during the early 1970s at the Hammond Bay Biological Station, Millersburg, Michigan. Laboratory tests showed that P, P-bis (1-aziridinyl)-N-methylphosphinothioic amide (Bisazir; Chang et al. 1970) was the most promising of fourteen potential chemosterilants to test on Sea Lamprey in the feld (Hanson and Manion 1978). Field tests were conducted in the Big Garlic River near Marquette, Michigan (Hanson and Manion 1978, 1980; Hanson 1981). Sterile and untreated male Sea Lampreys were introduced in various combinations in barrier-divided sections of the river, and mating and egg survival were observed. T e tests confrmed that Bisazir-treated male Sea Lampreys were sterile and behaved normally; they made nests, competed for mates, and mated with female Sea Lampreys in a normal manner. Larval production in the study tributary was reduced to near the expected rate. T e investigations also suggested that Bisazir was an ef ective sterilant for female Sea Lampreys, but the result was not conclusive and sterilization of female Sea Lampreys was not pursued at that time. Other methods of sterilization were also investigated, in part, because of the human health concerns working with chemosterilants like Bisazir (Borkovec 1972; Rudrama and Reddy 1985; Hanson 1990), but few methods showed promise and none were as ef ective as Bisazir (Hanson 1990). A specialized facility for sterilizing spawning-phase male Sea Lampreys was constructed at the Ham- mond Bay Biological Station during 1990 (Twohey et al. 2003a) because of the station’s proximity to major sources of male Sea Lampreys, a good source of water, waste treatment facilities, electrical power needs, and technical and analytical support. T e new facility was designed to sterilize approximately 1,400 male Sea Lampreys per day and contain the toxic and mutagenic hazards of Bisazir. T e facility was designed to hold Sea Lampreys for forty-eight hours after treatment, after which Bisazir does not persist in tissues (Allen and Dawson 1987). Inside the facility, a unique computer controlled robotics device designed to administer Bisazir to male Sea Lampreys was installed (Twohey et al. 2003a). T e device minimized the risk of Bisazir exposure to personnel and assured accurate dosage administration. T e device calculated the proper amount of Bisazir based on weight (100 mg/kg), determined the injection position based on length (40 percent of body length from head), and administered the Bisazir by inter-peritoneal injection in an enclosed chamber to protect personnel.

Sources of Male Sea Lampreys

Spawning-phase male Sea Lampreys were captured for sterilization from a network of traps operated in spawning tributaries in the United States and Canada (Mullett et al. 2003; Twohey et al. 2003a). From 1991 to 1996, an average of twenty-six thousand (range nineteen thousand to thirty-six thousand) male Sea Lampreys were collected for sterilization from seven tributaries that had ongoing assessment trapping operations in northern lakes Huron and Michigan. T e network of traps supplying male Sea Lampreys for sterilization has expanded to include twenty-four tributaries across four Great Lakes (i.e., lakes Superior, Michigan, Huron, and Ontario). Male Sea Lampreys were transported to the sterilization facility from as far as 750 km (Duffns Creek, Ontario). Augmenting the supply of male Sea Lampreys for the technique using Lake Champlain, Finger Lakes, or Atlantic origin Sea Lampreys was considered, but concerns regarding T e discovery, during 2000, of heterosporis, a microsporidian parasite, in Lake Ontario prompted a recommendation by the Great Lakes Fish Health Committee to screen all spawning-phase Sea Lamprey transfers destined for the Upper Great Lakes. Transfers and screening began in 2003 and followed the American Fisheries Society blue book protocols (AFS-FHS 2004) and included all restricted pathogens, including viral 678 Michael J. Siefkes et al. hemorrhagic septicemia virus (VHSv). Neither heterosporis nor VHSv, nor any other pathogen that would preclude transfer from Lake Ontario has been found. Sea Lampreys can harbor a number of pathogens, including bacterial kidney disease, furunculosis, and enteric redmouth, but these pathogens found in Sea Lampreys from Lake Ontario have been of strains common in other fshes in the upper Great Lakes. Sea Lampreys were not screened prior to transfer among the upper three lakes, because these are open systems among which Sea Lampreys move freely.

Lake Superior Releases

Lake Superior was selected as an experimental site to implement the sterile-male-release technique from 1991 to 1996, because it met the basic criteria set forth by the sterile-male-release technique task force: low numbers of spawning-phase Sea Lampreys, isolation from other Sea Lamprey populations, and potential for evaluation of the ef ects of the technique on Sea Lamprey and fsh populations. An in-stream release strategy was implemented during 1991 (Kaye et al. 2003; Twohey et al. 2003a). From 1991 to 1996, an average of 16,100 sterilized male Sea Lampreys were release into thirty-three Lake Superior tributaries (Twohey et al. 2003a), achieving an average ratio of 1.5:1 sterile to untreated male Sea Lampreys. T e logistics of capturing, sterilizing, and releasing Sea Lampreys was a success. Behavioral observations indicated sterilized male Sea Lampreys appeared on nests at near the expected ratios, mated normally, and reduced production of larvae from nests (Bergstedt et al. 2003b). Other indices were not as encouraging. T e mean relative abundance of Sea Lampreys in the lake increased from the previous ten years (Heinrich et al. 2003). Changes in Sea Lamprey wounding rate estimates on Lake Trout did not decline as expected during 1998 or 1999. In retrospect, the number of sterilized male Sea Lampreys available for release in Lake Superior was not adequate for suffcient change to be observed against the backdrop of independent population variation and other management actions in the system (Twohey et al. 2003a).

St. Marys River Releases

T e St. Marys River was initially selected for the sterile-male release technique, because a growing larval population in the river defed lampricide control tactics, using TFM (Schleen et al. 2003), and the technique of ered a possible solution. Also, male spawning-phase Sea Lampreys collected from the extremely late run in the St. Marys River could not be used for sterile-male releases elsewhere. Sterile-male releases into the St. Marys River from 1991 to 1996 primarily relied on male Sea Lampreys captured from only the St. Marys River. An average of 4,600 sterile-males were released into the St Mary’s River, achieving an average ratio of 0.6:1 sterile to untreated male spawning-phase Sea Lampreys (Twohey et al. 2003a). T e ef ective number of spawning pairs in the river was reduced from an annual average of 11,100 to 5,000. Sterile-male releases into the St. Marys River were enhanced during 1997, as part of a two-pronged strategy to reduce Sea Lamprey recruitment from the river. Traps and sterile-males were used to reduce reproduction, and Bayluscide was used to spot treat high density concentrations of larvae (Schleen et al. 2003). From 1997 to 2009, traps removed an average of 40 percent of the spawning population in the river. T e average number of sterile-males released annually was 27,000. An average ratio of 3.7:1 sterile to untreated male spawning-phase Sea Lampreys was achieved. T e ef ective number of spawning pairs in the river was further reduced to 1,100. Key indices showed the integrated control strategy for the St. SEA LAMPREY CONTROL 679

Marys River was working, as measures of larval populations, transformers, spawning-phase populations, and Sea Lamprey wounding and mortality on Lake Trout were consistently lower since inception of the strategy (Bergstedt and Twohey 2007).

The Future of the Sterile-Male-Release Technique

Bergstedt and Twohey (2007) details further development of the sterile-male-release technique. Greater use of the sterile-male-release technique in Sea Lamprey control is limited by the supply of male spawning-phase Sea Lampreys. T e harvest of male Sea Lampreys is inherently limited, because the Sea Lamprey Control Program is actively treating the population from which male Sea Lampreys are obtained. Male Sea Lampreys captured outside the basin could supplement male Sea Lampreys from the Great Lakes and could increase the ef ectiveness of the sterile-male-release technique, particularly when Sea Lamprey population levels in the Great Lakes are greatly reduced. In addition, modest improvements in trapping would increase ef ectiveness of sterile-male release. Removal of more female Sea Lampreys from the treated population would further reduce reproductive potential, and removal of more male Sea Lampreys would further reduce male competitors and provide more male Sea Lampreys for sterilization. Better understanding of Sea Lamprey behavior and new trapping technologies are being pursued. Also, advances in pheromone technology (Twohey et al. 2003b; Li et al. 2007) may provide a boost to trapping ef ectiveness. Pheromones integrated with ef ective traps would be a powerful advancement of the sterile-male-release technique. Bisazir is a hazard to human health, during the injection and holding period prior to release of the sterilized male spawning-phase Sea Lampreys. Further development of the handling and release portion of the program depends on the development of a safer sterilant, and is particularly important if the ability to trap, inject, and release a greater number of male Sea Lampreys can be realized. T e release of additional sterilized male Sea Lampreys into the St. Marys River, however, carries another set of questions about the response of the Sea Lamprey population to an excess of male Sea Lampreys (Bergstedt and Twohey 2007). Would mate selection become more sensitive toward non-sterilized male Sea Lampreys? Could sterilized male Sea Lampreys be made more competitive or attractive, providing greater reduction in reproduction per sterilized male Sea Lamprey released? Answers to these questions will help determine the cost-ef ectiveness of increasing the number of sterilized male Sea Lampreys released into the St. Marys River. Research that may expand the use of Bisazir-sterilization in the Sea Lamprey Control Program is underway. Studies are being conducted to determine if female spawning-phase Sea Lampreys can be sterilized and ef ectively compete for mates and if their release will result in reduced larval recruitment. An abundance of female Sea Lampreys are available for sterilization, if that technique proves useful. Finally, recent work by Jones et al. (2003) indicates that density independent variation can mask benefts of reproductive suppression, except when spawning stocks are very low. Better understanding of Sea Lamprey population dynamics will allow the prediction of ef ects of techniques to reduce reproduction and to set suppression targets with greater confdence. T e sterile-male-release technique is an integral part of the control strategy for the St. Marys River, along with trapping and the treatment of larval populations with granular Bayluscide. T e ef ect of any individual component of the control program on the reduction of spawning-phase Sea Lampreys from the 680 Michael J. Siefkes et al. river cannot be determined from the available data, although modeling analysis indicates all three tactics play a role (Haeseker et al. 2003). A direct method of evaluating the ef ectiveness of the sterile-male-release technique is required.

Status of Sea Lamprey Control in Each Lake

Each of the Great Lakes dif ers in the number and size of Sea Lamprey-infested areas, as well as Sea Lamprey production and growth. Each infested area also varies in how ef ectively it can be treated with lampricides or alternative Sea Lamprey control techniques. T ese variables create unique situations in each lake and can sometimes af ect adjoining lakes. Sea Lamprey Control Program success is primarily measured by comparing annual estimates of lake-wide spawning-phase Sea Lamprey abundance with lake-specifc targets. For each of the Great Lakes, spawning-phase Sea Lamprey targets are prescribed in fsh community objectives or in Lake Trout rehabilitation plans developed by each lake committee. Sea Lamprey targets, approved by the fshery management agencies, vary by lake and equal the mean abundance during a fve-year period when Sea Lamprey wounding rates on Lake Trout were lowest in all the lakes, except Huron. In Lake Huron, the target is one-quarter of the mean abundance from 1992 to 1996 (the highest fve-year mean abundance of the time series). Progress toward Sea Lamprey targets is measured against the estimates of lake-wide abundance (Mullett et al. 2003). Sea Lamprey targets have been met on each of the Great Lakes; unfortu- nately, never on all the lakes at the same time. Measures of Sea Lamprey abundance are highly variable, so that a reduction (or increase) observed in a given lake during a given one- or two-year span may be feeting (e.g. Lake Huron 1987 and 2003). Low Sea Lamprey abundance observed over a longer duration, such as a fve-year span, would indicate successful Sea Lamprey control. A second metric of Sea Lamprey Control Program success is an annual measure of fresh Sea Lamprey wounds (King 1980; fg.6) per one hundred Lake Trout longer than 533 mm (age 5 Lake Trout in Lake Erie and Lake Trout longer than 433 mm in Lake Ontario) captured by the fshery management agencies during standardized gill-net surveys. Wounding rate estimates are refective of the number of Sea Lam- preys that escape Sea Lamprey control activities each year and are an indicator of Sea Lamprey-induced mortality on Lake Trout. Nevertheless, although there is a positive relationship between wounding rate and spawning-phase Sea Lamprey abundance among years, the relationship is quite variable, indicating there are other factors that infuence these measures of program success. In addition, the Sea Lamprey is not a species-specifc parasite, and, although it prefers large-bodied, cold water species, such as Lake Trout, it is opportunistic in its feeding habits (Farmer and Beamish 1973; Harvey et al. 2008), preying on warm water species and lower trophic level species in areas, such as Lake Superior’s Black Bay, where Lake Trout abundance is very low. Nevertheless, a target of fve wounds per one hundred Lake Trout, which was selected to ensure that suffcient numbers of mature fsh survive to enable natural reproduction, is applied in all the lakes, except Ontario, where a target of two Sea Lamprey wounds per one hundred Lake Trout was selected. T e dif erent wounding rate target used in Lake Ontario is thought to be a better estimate for that system (Schneider et al. 1996). Rutter and Bence (2003) have identifed limitations with this approach, specifcally the failure to recognize spatial and temporal patterns in wounding and the predictability between the number of wounds and host length. Interpretation of wounding rates may also be subject to bias resulting from seasonal dif erences in the timing of the gill-net surveys (Spangler et al.1980), which are SEA LAMPREY CONTROL 681

FIG. 6. A Sea Lamprey (Petromyzon marinus) wound on a Lake Trout (Salvelinus namaycush).

W. P. Sullivan.

conducted on lakes Superior and Michigan during spring, on lakes Huron and Ontario during fall, and on Lake Erie during late summer. Regardless of the method, wounding rate is only relevant when considered in the context of Lake Trout abundance, as one would expect an inverse relationship between Sea Lamprey wounding rate on Lake Trout and Lake Trout abundance, if the Sea Lamprey population is held static. Finally, program success can also be measured at the individual tributary level, through the post- treatment assessment of the relative abundance of Sea Lamprey larvae that survive lampricide treatment. Lampricide application is estimated to kill 95–99 percent of the Sea Lamprey larvae within a tributary (Heinrich et al. 2003). Treatment ef ectiveness can, however, vary both among tributaries and within tributaries over successive years of lampricide treatment because of fuctuations in water chemistry, infux of water from ground water exchange or from a rain event, or from reduced fows af ecting distribution of lampricide within the tributary. Although post-treatment assessment cannot detect minor dif erences in treatment ef ectiveness because of the uncertainty in larval relative abundance estimates, a large reduction in treatment ef ectiveness will likely be detected.

Lake Superior

Sea Lamprey production has been recorded in 148 of 1,566 tributaries to Lake Superior (Heinrich et al. 2003; Young and Adair 2008). Of these, 84 have been treated with lampricides at least once since 1998, and 53 require treatment on a regular cycle. Lampricide control in Lake Superior also includes the application 682 Michael J. Siefkes et al. of the Bayluscide granules to lentic areas associated with Sea Lamprey-producing tributaries. Although not unique to Lake Superior, this lake has the majority of these lentic Sea Lamprey populations, and only the St. Marys River has a higher abundance of Sea Lampreys treated with Bayluscide granules. In addition, Sea Lamprey barriers on 15 tributaries (Young and Adair 2008) complement the lampricide control program in Lake Superior. Spawning-phase Sea Lamprey are also trapped in 22 tributaries for population assessment purposes and to provide male Sea Lampreys for the sterile-male-release technique in the St. Marys River. Lake-wide spawning-phase Sea Lamprey abundance has remained at a level less than 10 percent of peak abundance (Heinrich et al. 2003; fg. 7a). Sea Lamprey abundance was near the target during the late 1980s and mid-1990s and reached the lowest recorded level during 1994. Sea Lamprey abundance trended upward between 1994 and 2001, but has been trending downward since then and was below the target during the most recent years (2008 and 2009). T e 2009 Sea Lamprey abundance estimate is twenty-seven thousand, which is under the target of thirty-six thousand, but only continued suppression for at least a fve-year period will indicate successful Sea Lamprey control. Sea Lamprey wounds per one hundred Lake Trout longer than 533 mm have not shown the same pattern of decrease, but recent wounding rate estimates have declined (fg. 7b). T e lake-wide wounding rate estimate, most recently at nine, is above the target of fve wounds per one hundred Lake Trout and has been increasing since 1994. Lake Trout abundance had been holding steady but appears to be increasing during recent years (fg. 7c), which could account for the recent decline in the wounding rate estimates. T e wounding rate estimate seems highest in the western portion of the lake but has recently declined in Minnesota waters. T e wounding rate estimate in Michigan waters indicates Sea Lamprey-induced mortality on Lake Trout exceeds fshery-induced mortality, but fshery induced-mortality is low in Michigan waters. Overall, fshery objectives for Lake Trout continue to be met, but Lake Trout populations are still threatened by high Sea Lamprey-induced mortality. In response to lake-wide spawning-phase Sea Lamprey abundance and wounding rate estimates above targets, increased lampricide control ef orts were initiated during 2001 and then further increased during 2006. T e recent decline of Sea Lamprey abundance to below the target is likely the result of the most recent increases in lampricide control ef ort initiated during 2006. Sea Lamprey abundance is expected to remain near the target during future years, and the upward trend in wounding rate estimates is expected to reverse as increased lampricide control ef orts are maintained.

Lake Michigan

Sea Lamprey production has been recorded in 121 of 511 tributaries to Lake Michigan (Young and Adair 2008). Of these, 72 have been treated with lampricides at least once since 1998 and 34 require treatment on a regular three- to fve-year cycle. Lampricide control in Lake Michigan also includes the application of Bayluscide granules to lentic areas associated with Sea Lamprey-producing tributaries. Lentic Sea Lamprey populations in Lake Michigan, however, are not as problematic as in Lakes Superior and Huron. In addition, Sea Lamprey barriers on 11 tributaries complement the lampricide control program. Spawning-phase Sea Lampreys are also trapped in 16 tributaries for population assessment purposes and to provide male Sea Lampreys for the sterile-male-release technique. Sea Lamprey control ef orts in Lake Huron also infuence Lake Michigan, as Sea Lampreys are known to move between lakes Michigan and Huron (Moore et al. 400 A. 350

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0 Spawning-Phase Sea Lamprey Abundance (thousands) 1975 1980 1985 1990 1995 2000 2005 2010

35 B. 30 FIG. 7. Status of Sea Lamprey (Petromyzon marinus) control 25 in Lake Superior: (A) lake-wide 20 spawning-phase Sea Lamprey abundance estimates (line with 15 diamonds) compared to the 10 target (black horizontal line); (B) lake-wide Sea Lamprey 5 wounding rate per one Sea Lamprey Wounding Rate per 100 Lake Trout 0 hundred Lake Trout (Salvelinus 1975 1980 1985 1990 1995 2000 2005 2010 namaycush; line with circles) longer than 533 mm compared to the fve-wound target (black 50 C. horizontal line); and (C) lake-wide Lake Trout relative 40 abundance (CPE = fsh/km/net night of lean Lake Trout longer

30 than 533 mm; line with cubes). Great Lakes Fishery Commission

10 Lake Trout Relative Abundance (CPE) Lake Trout

0 1975 1980 1985 1990 1995 2000 2005 2010 684 Michael J. Siefkes et al.

1974; Bergstedt et al. 2003a), and Sea Lampreys produced from northern Lake Huron, particularly from the St. Marys River, signifcantly contribute to the Lake Michigan population. Lake-wide spawning-phase Sea Lamprey abundance is at about 10 percent of peak levels, but has been trending upward since 1980 (Lavis et al. 2003b) and has fuctuated greatly since 2003, with sharp increases observed during 2004, 2006, and 2007 and sharp decreases during 2005, 2008, and 2009 (fg. 8a). Sea Lamprey abundance (sixty-thousand) was below the target (sixty-two thousand) during the most recent year (2009), but only continued suppression to target levels for at least a fve-year period will indicate successful Sea Lamprey control. Sea Lamprey wounds per one hundred Lake Trout longer than 533 mm has also shown an upward trend (fg. 8b), and the most recent wounding rate estimate (thirteen) is above the lake-wide target of fve wounds per one hundred Lake Trout. Lake Trout abundance appears to be holding steady (fg. 8c), but declining abundance of larger Lake Trout may be contributing to increasing wounding rate estimates. Increased Sea Lamprey-induced mortality on Lake Trout in the northern waters has set Lake Trout restoration ef orts back at least a decade. Furthermore, increased Sea Lamprey-induced mortality is af ecting the quota for the commercial fshery to the extent that components of the Lake Trout management regimen in the consent decree between the tribes, the state, and the federal government are currently suspended. Achievement of Lake Trout rehabilitation will continue to be hampered, if Sea Lamprey-induced mortality remains high. Increases in the spawning-phase Sea Lamprey abundance and wounding rate estimates during the 1990s can be partially attributed to Sea Lamprey production from the St. Marys River. In response, an integrated control strategy was initiated in the St. Marys River (Schleen et al. 2003). T e continued upward trend in Sea Lamprey abundance and wounding rate estimates during the late 1990s and early 2000s indicated there were other signifcant sources of Sea Lampreys. Increased lampricide control ef orts were initiated during 2001 and included the treatment of newly discovered larval Sea Lamprey populations in lentic areas and the Manistique River, a large system in which the deterioration of a dam near the river mouth allowed Sea Lampreys access to more than 400 km of river. Lampricide control ef orts were further increased during 2006. T e recent decline of Sea Lamprey abundance to the target is likely a result of increased lampricide control ef orts and lampricide treatments in the Manistique River during 2003, 2004, 2007, and 2009. Sea Lamprey abundance is expected to remain near the target during future years, and the upward trend in the wounding rate estimates is expected to reverse as increased lampricide control ef orts are maintained and the barrier on the Manistique River is replaced.

Lake Huron

Sea Lamprey production has been recorded in 117 of 1,761 tributaries to Lake Huron (Young and Adair 2008). Of these, 71 have been treated with lampricide at least once since 1998 and 45 require treatment on at a regular four- to six-year cycle. Lampricide control in Lake Huron also includes the application of Bayluscide granules to lentic areas associated with Sea Lamprey-producing tributaries and the St. Marys River, which has the highest abundance of larval Sea Lampreys treated with Bayluscide granules. In addition, Sea Lamprey barriers on 19 tributaries complement the lampricide control program, and the sterile-male-release technique is a component of the integrated Sea Lamprey control strategy in the St. Marys River. Spawning-phase Sea Lampreys are also trapped in 21 tributaries for population assessment 400 A. 350

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0 Spawning-Phase Sea Lamprey Abundance (thousands) 1975 1980 1985 1990 1995 2000 2005 2010

35 B. 30 FIG. 8. Status of Sea Lamprey 25 (Petromyzon marinus) control 20 in Lake Michigan: (A) lake-wide spawning-phase Sea Lamprey 15 abundance estimates (line with 10 diamonds) compared to the target (black horizontal line); 5 (B) lake-wide Sea Lamprey Sea Lamprey Wounding Rate per 100 Lake Trout 0

1975 1980 1985 1990 1995 2000 2005 2010 wounding rate per one hundred Lake Trout (Salvelinus namaycush; line with circles) longer than 533 mm compared 50 C. to the fve-wound target (black horizontal line); and (C) 40 lake-wide Lake Trout relative abundance (CPE = fsh/km/net 30 night of lean Lake Trout longer than 533 mm; line with cubes).

20 Great Lakes Fishery Commission

10 Lake Trout Relative Abundance (CPE) Lake Trout

0 1975 1980 1985 1990 1995 2000 2005 2010 686 Michael J. Siefkes et al. purposes and to provide male Sea Lampreys for the sterile-male-release technique, and trapping in the St. Marys River is a component of the integrated control strategy. Sea Lamprey control ef orts in Lake Michigan also infuence Lake Huron, as Sea Lampreys from northern Lake Michigan tributaries, such as the Manistique River, contribute to the Lake Huron population. Lake-wide spawning-phase Sea Lamprey abundance has remained at a level less than 10 percent of peak abundance (Morse et al. 2003; fg. 9a). During the early 1980s, Sea Lamprey abundance increased from the target, particularly in the northern portion of the lake, and peaked during 1993. Sea Lamprey abundance has not declined to target in Lake Huron for more than twenty-fve years. T e 2009 Sea Lamprey abundance estimate is 122,000, which is above the target of 73,000. Sea Lamprey wounds also have not decreased to the lake-wide target of fve wounds per one hundred Lake Trout longer than 533 mm, but signifcant declines occurred during the mid-1990s and wounding rate estimates have been at a relatively low level since 2002 (fg. 9b). T e wounding rate estimate was most recently estimated to be eight wounds per one hundred lake trout. Lake Trout abundance appears to be increasing (fg. 9c), which could account for the decline in wounding rate estimates. T rough the 1990s, there were more Sea Lampreys in Lake Huron than in all other lakes combined, and fshery objectives were not being achieved. Sea Lamprey-induced mortality was so severe that, during 1995, Lake Trout restoration ef orts were suspended in the northern portion of the lake. After signifcant decreases in wounding rate estimates, Lake Trout restoration ef orts were restored, and, although wounding rate estimates are still above the target, Lake Trout populations are increasing and showing signs of natural reproduction. Further reduction in Sea Lamprey-induced mortality on Lake Trout, however, is needed to further advance rehabilitation of the Lake Trout population. Above target lake-wide spawning-phase Sea Lamprey abundance and Lake Trout wounding rate estimates can be primarily attributed to Sea Lamprey production from the St. Marys River. In response, an integrated control strategy was initiated in the St. Marys River (Schleen et al. 2003), starting with an initial 880-hectare treatment of Sea Lamprey-infested areas of the river with Bayluscide granules (made possible by a $3 million grant from the state of Michigan), followed by the use of the sterile-male-release technique, trapping, and Bayluside granule spot treatments to maintain population suppression in subsequent years. Measures of success of the St. Marys River control strategy indicated Sea Lamprey recruitment had been dramatically reduced (Adams et al. 2003). As expected, Sea Lamprey abundance and Lake Trout wounding rate estimates in Lake Huron signifcantly declined following the implementation of the strategy. Ad- ditional lampricide control ef orts in the St. Marys River and other tributaries were initiated during 2001 and further enhanced during 2006. Nevertheless, Sea Lamprey abundance and Lake Trout wounding rate estimates have not continued to decline and are still above target, and larval Sea Lamprey populations in the St. Marys River are increasing. Sea Lamprey abundance and Lake Trout wounding rate estimates are expected to decrease during future years, as lampricide control ef orts are further enhanced, including another large-scale treatment of the St. Marys River.

Lake Erie

Sea Lamprey production has been recorded in 22 of 842 tributaries to Lake Erie (Young and Adair 2008). Of these, 10 have been treated with lampricides at least once since 1999 and 7 require treatment on a regular cycle. Lampricide control in Lake Erie using Bayluscide granules is minimal. In addition, Sea Lamprey 400 A. 350

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35 B. 30 FIG. 9. Status of Sea Lamprey

25 (Petromyzon marinus) control in Lake Huron: (A) lake-wide 20 spawning-phase Sea Lamprey

15 abundance estimates (line with diamonds) compared to the 10 target (black horizontal line);

5 (B) lake-wide Sea Lamprey

Sea Lamprey Wounding Rate per 100 Lake Trout wounding rate per one 0 1975 1980 1985 1990 1995 2000 2005 2010 hundred Lake Trout (Salvelinus namaycush; line with circles) longer than 533 mm compared to the fve-wound target (black 50 C. horizontal line); and (C) lake-wide Lake Trout relative 40 abundance (CPE = fsh/km/net night of lean Lake Trout longer 30 than 533 mm; line with cubes).

Great Lakes Fishery Commission 20

10 Lake Trout Relative Abundance (CPE) Lake Trout

0 1975 1980 1985 1990 1995 2000 2005 2010 688 Michael J. Siefkes et al. barriers on 7 tributaries complement the lampricide control program. Spawning-phase Sea Lampreys are also trapped in 4 tributaries for population assessment purposes. Lake-wide spawning-phase Sea Lamprey abundance has been widely variable in Lake Erie (Sullivan et al. 2003; fg. 10a), with periods of time within which abundance estimates were at pre-Sea Lamprey control levels (i.e., 1980–1987, 1998–2000, and 2005–2007) and periods of time within which abundance estimates were below or near the target (i.e., 1988–1997, 2001–2004, and 2008). Sea Lamprey abundance (thirty-six thousand) was nearly twice the pre-Sea Lamprey control abundance level and almost an order of magnitude above the target (four thousand) during the most recent year (2009). Sea Lamprey wounds per one hundred Lake Trout longer than 533 mm have also been widely variable in Lake Erie (fg. 10b). Except during 1989–1994, the achievement of the lake-wide wounding rate target of fve wounds per one hundred Lake Trout has been elusive. Wounding rate estimates have declined during recent years and fell to 6.7 wounds per one hundred fsh during 2008, providing optimism that the target would be achieved in the near future. T e wounding rate estimate for 2009, however, is projected to be over three times the target (J. Markham, personal communication). Lake Trout abundance has been variable but has also been increasing during recent years (fg. 10c), which could account for the recent decline in wounding rate estimates. Lake Trout survival increased to a suffcient level to meet rehabilitation objectives in the eastern basin of the lake during the late 1980s to mid-1990s. Above target wounding rate estimates since the mid-1990s, however, have set Lake Trout restoration ef orts back. Further reduction in Sea Lamprey-induced mortality on Lake Trout is needed to further advance rehabilitation of the Lake Trout population. T e initial lampricide treatments in Lake Erie, conducted during 1986 and 1987, reduced spawning- phase Sea Lamprey abundance and wounding rate estimates to the targets, which were maintained through treatment of reinfested tributaries in the late 1980s and early 1990s. T e high variation in the Sea Lamprey abundance estimates since then is likely due to an oscillating pattern of control: a period of high Sea Lamprey abundance, followed by intensive lampricide control ef ort and suppression, leading to relaxation of ef ort and a rebound in the population (Sullivan et al. 2003). Water quality and stream habitat improvements and changes in the fsh community in the eastern basin of Lake Erie have likely enhanced Sea Lamprey survival. A limitation in the Sea Lamprey abundance estimate due to the relatively few Sea Lamprey-producing tributaries also adds to the variation. A recent large-scale treatment strategy, conducted during 2008 and 2009, in which all Sea Lamprey-producing tributaries in Lake Erie were treated in back-to-back years is expected to break this oscillating pattern and reduce Sea Lamprey abundance to the target, possibly for an extended period of time delaying the need for further lampricide control.

Lake Ontario

Sea Lamprey production has been recorded in 65 of 659 tributaries to Lake Ontario (Young and Adair 2008). Of these, 39 have been treated with lampricide at least once since 1999 and 29 require treatment on a regular cycle. Lampricide control in Lake Ontario using Bayluscide granules is limited to a few lentic areas associated with Sea Lamprey-producing tributaries. In addition, Sea Lamprey barriers on 15 tributaries complement the lampricide control program. Spawning-phase Sea Lampreys are also trapped in 12 tributaries for population assessment purposes and to provide male Sea Lampreys for the sterile-male-release technique. 400 A. 350

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25 FIG. 10. Status of Sea Lamprey (Petromyzon marinus) control 20 in Lake Erie: (A) lake-wide 15 spawning-phase Sea Lamprey abundance estimates (line with 10 diamonds) compared to the 5 target (black horizontal line);

Sea Lamprey Wounding Rate per 100 Lake Trout (B) lake-wide Sea Lamprey 0 1975 1980 1985 1990 1995 2000 2005 2010 wounding rate per one hundred Lake Trout (Salvelinus namaycush; line with circles) longer than 533 mm compared 50 C. to the fve-wound target (black horizontal line); and (C) 40 lake-wide Lake Trout relative abundance (CPE = relative 30 abundance of age 5+ Lake Trout sampled from the eastern 20 basin; line with cubes).

Great Lakes Fishery Commission

10 Lake Trout Relative Abundance (CPE) Lake Trout

0 1975 1980 1985 1990 1995 2000 2005 2010 690 Michael J. Siefkes et al.

Lake-wide spawning-phase Sea Lamprey abundance estimates signifcantly declined during the 1980s (Larson et al. 2003), have been below or near the target since the late 1980s, and remain at a level less than 10 percent of peak abundance (fg. 11a). T e 2009 Sea Lamprey abundance estimate is thirty-eight thousand, which is slightly above the target of thirty-one thousand. Continued suppression of Sea Lamprey populations for nearly twenty-fve years indicates the successful control of Sea Lampreys in Lake Ontario. Sea Lamprey wounds per one hundred Lake Trout longer than 433 mm also signifcantly declined during the 1980s and have been near the lake-wide target of two wounds per one hundred Lake Trout since the mid-1980s (fg. 11b). T e most recent wounding rate estimate of 1.5 is below the target, but wounding rates of the mouth of the Niagara River have been high. Lake Trout abundance has steadily declined since the mid-1990s (fg. 11c), which may be af ecting wounding rate estimates. Achievement of Lake Trout rehabilitation objectives will continue to be hampered, if Lake Trout abundance further declines and Sea Lamprey-induced mortality increases. T e application of lampricides to important Sea Lamprey-producing tributaries during the 1980s, including the Black and Oswego systems, precipitated a signifcant decline in spawning-phase Sea Lamprey abundance and wounding rate estimates to below or near the targets. Subsequent lampricide control ef orts have maintained Sea Lamprey abundance and wounding rate estimates below or near the targets. Lampricide control ef orts will continue at the same level and Sea Lamprey abundance, and wounding rate estimates are expected to remain close to targets in the future.

Enhancing Measures of Program Success

Improving measures to determine program success is a priority of the Sea Lamprey Control Program. Confdence intervals around wounding rate estimates are currently being developed, and plans to measure spatial and temporal patterns in wounding rates have been made. Estimates of Lake Trout relative abundance are also currently being developed, and error estimation and analysis of spatial and temporal patterns are planned. Furthermore, plans to estimate wounding rates on other fsh species and how fsh abundance, size, habitat, etc. interact with wounding rate estimates are underway. T ese data will better link Sea Lamprey control to the fsh community as a whole, not just Lake Trout, and will allow a more thorough assessment of the impacts of the Sea Lamprey Control Program. In the ESTR model, the production of Sea Lampreys is valued equally among all tributaries to the Great Lakes, as evidenced in the cost per kill criteria used to rank tributaries for lampricide treatment. T e damage a Sea Lamprey causes, however, is not necessarily valued equally among lakes (Stewart et al. 2003). T e way Sea Lamprey production and damage are valued needs to be reconciled to better measure program success. Additionally, the survival of recently metamorphosed Sea Lamprey as they emerge from the tributary has been linked with the abundance of initial host species (Young et al. 1996; Harvey et al. 2008). T erefore, consideration of the entire fsh community should be part of the method to allocate Sea Lamprey control resources and, subsequently, be a measure of overall program success. To determine the holistic measure of program success, it is most appropriate to combine the evaluation of stream-specifc treatment ef ectiveness; the likelihood surviving larvae will fnd an initial host as newly metamorphosed parasitic-phase Sea Lampreys; the abundance of initial, intermediate, and terminal hosts; and the assessment of spawning-phase Sea Lamprey abundance. Many of these parameters are already quantifed; the next step is to combine predator-prey dynamics, bioenergetics, compensatory mechanisms, 400 A. 350

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15 FIG. 11. Status of Sea Lamprey (Petromyzon marinus) control 10 in Lake Ontario: (A) lake-wide 5 spawning-phase Sea Lamprey

Sea Lamprey Wounding Rate per 100 Lake Trout abundance estimates (line with 0 1975 1980 1985 1990 1995 2000 2005 2010 diamonds) compared to the target (black horizontal line); (B) lake-wide Sea Lamprey wounding rate per one 50 C. hundred Lake Trout (Salvelinus namaycush; line with circles) 40 longer than 433 mm compared to the two-wound target (black 30 horizontal line); and (C) lake-wide Lake Trout relative 20 abundance (CPE = fsh/km/net night of lean Lake Trout longer 10 than 433 mm; line with cubes). Lake Trout Relative Abundance (CPE) Lake Trout Great Lakes Fishery Commission

0 1975 1980 1985 1990 1995 2000 2005 2010 692 Michael J. Siefkes et al. and stock-recruitment relationships in a complex ecological model, to evaluate the places in the current program where changes in Sea Lamprey control practices can reduce Sea Lamprey abundance in the Great Lakes even further.

New Developments in Sea Lamprey Control

T e current Sea Lamprey Control Program takes an integrated approach to evaluating tributaries and lentic areas for Sea Lamprey production (i.e., larval assessment), evaluating and implementing options for control of Sea Lamprey (i.e., lampricide and alternative controls), and evaluating the ef ects of control activities (i.e., spawning-phase Sea Lamprey abundance and Lake Trout wounding rate estimates). Although the techniques used in the Sea Lamprey Control Program have been evolving for more than ffty years, method refnement and implementation of new technologies continue to change the application of Sea Lamprey control within the Great Lakes. What the future holds for each of the specifc techniques within the Sea Lamprey Control Program is outlined in the previous sections of this chapter. Five research theme papers that capture the state of knowledge and outline additional research needs for barriers and trapping, lampricide control, Sea Lamprey population dynamics, sterile-male release, and the implementation of pheromones in the Sea Lamprey Control Program are also available (McLaughlin et al. 2007; McDonald and Kolar 2007; Jones 2007; Bergstedt and Twohey 2007; Li et al. 2007). Above and beyond the principle Sea Lamprey Control Program elements, the future seems bright for two emerging areas: pheromones and genomics.

Pheromones

For decades, Sea Lamprey pheromones have been thought to hold potential for development of alternative Sea Lamprey control strategies (Teeter 1980). Pheromones are “substances that are excreted to the outside by an individual and received by a second individual of the same species in which they release a specifc reaction, for example a defnite behavior or developmental process” (Karlson and Luscher 1959). Initial laboratory studies indicated that spawning-phase Sea Lampreys detect and respond to odorants released by stream-dwelling larvae and by sexually mature individuals of the opposite sex (Teeter 1980). In principle, responses to pheromones are often innate, specifc, and robust, rendering target animals vulnerable to manipulation with minute amounts of pheromones (Li et al. 2003). Recognizing that pheromones may very well be developed into environmentally benign and ef ective alternative control strategies, the Sea Lamprey research community and control agents in the Great Lakes basin have collaborated in search of pheromonal chemicals. T is extensive research ef ort has come to fruition (Li et al. 2007). A series of studies has identifed a mating pheromone that could potentially be developed for incorporation into the Sea Lamprey Control Program. Spawning-phase male Sea Lampreys have long been suspected of releasing a pheromone that attracts female Sea Lampreys (Teeter 1980). Behavioral studies have demonstrated that ovulating female Sea Lampreys show search behavior, when exposed to water conditioned with spermiating male Sea Lampreys, also called washings (Li et al. 2002; Siefkes et al. 2005). In a spawning tributary, traps baited with spermiating male Sea Lampreys (Johnson et al. 2005) or washings from spermiating male Sea Lampreys (Johnson et al. 2006) capture a substantial proportion of ovulating female Sea Lampreys. Mature male Sea Lampreys rely on specialized cells in their gills to release SEA LAMPREY CONTROL 693 this pheromone (Siefkes et al. 2003), of which the main component is 3kPZS (3-keto Petromyzonol sulfate; 7α, 12α, 24-trihydroxy-5α-cholan-3-one 24 sulfate; Li et al. 2002). 3kPZS, and its synthesized copy, have been extensively studied in the Ocqueoc River, Michigan, for its potential use in Sea Lamprey control. T e synthesized copy of 3kPZS was highly ef ective in attracting ovulating female Sea Lampreys to artifcial nests upstream (Siefkes et al. 2005). When applied to the river, reaching concentrations between 10–14 and 10–10 molar (M), synthesized and natural 3kPZS were equally potent in inducing highly robust upstream movement in ovulating female Sea Lampreys and, eventually, luring them into baited traps (Johnson et al. 2008). Clearly, these fndings demonstrate the possible use of 3kPZS in the Sea Lamprey Control Program. Studies of chemicals released by larval Sea Lampreys have also resulted in identifcation of previously unknown compounds believed to function as migratory pheromones. Unlike salmon, migratory spawning- phase Sea Lampreys do not select their natal tributaries for reproduction (Bergstedt and Seelye 1995); rather, Sea Lampreys seem to prefer tributaries that contain a higher abundance of conspecifc larvae (Moore and Schleen 1980) and are attracted to the odor of larvae (Teeter 1980; Bjerselius et al. 2000; Vrieze and Sorensen 2001; Wagner et al. 2006). Larval Sea Lamprey compounds, petromyzonol sulfate (PZS), petromyzonamine disulfate (PADS), and petromyzosterol disulfate (PSDS), have been found to modify behaviors of migrating Sea Lampreys placed in laboratory mazes (Haslewood and Tokes 1969; Bjerselius et al. 2000; Sorensen et al. 2005). Based on these chemical and behavioral studies, Sorensen et al. (2005) further postulated that PADS is the major component of the migratory pheromone and that PS and PSDS are minor components. T is hypothesis, when further confrmed by empirical examination under natural conditions, may very well lead to the development of ef ective strategies for Sea Lamprey control. Application of pheromones in pest management has been studied more extensively for insects in which female pheromones are often deployed to trap males or disrupt reproductive behaviors (Beroza and Knipling 1972; Gaston et al. 1977). Field deployment of a vertebrate pheromone for control of vertebrate pests, however, has not been reported. Nevertheless, the most intensively studied Sea Lamprey pheromone compound, 3kPZS, appears to have several advantages for future deployment as an important strategy for the integrated control of the Sea Lamprey. Johnson et al. (2008) summarized an important feature of 3kPZS for potential use in Sea Lamprey control: 3kPZS alone modifes behaviors of ovulating female Sea Lampreys across a long distance. When 3kPZS is used to remove ovulating female Sea Lampreys from a spawning ground, it will result in a proportional reduction in viable eggs and, thus, is likely more ef ective than removal of male Sea Lampreys. An additional advantage of 3kPZS is that a single compound is less expensive to develop and register than multiple compounds. In addition to trapping, pheromones could potentially be used in other ways to control the Sea Lamprey, such as the development of antagonists to Sea Lamprey pheromones to disrupt mating or directing Sea Lampreys away from tributaries diffcult or expensive to treat with lampricides to tributaries easy or cheap to treat with lampricides (Li et al. 2007).

Genomics

T e advent and development of genomics have had a seismic ef ect on biological research. T e genome sequence endows a global view of the genetic landscape, potentially enabling identifcation of all the molecular components in cells and understanding of how these cells interact and function in various life stages. Wherever a genome is sequenced, the assembled sequence and other genomic resources have become a major impetus for discovery in that species. Fortunately, the Sea Lamprey genome has been 694 Michael J. Siefkes et al. sequenced by the National Institute of Health. T is genome is the blueprint that makes the Sea Lamprey a unique life form that has thrived in the Atlantic Ocean for more than fve hundred million years (Kumar and Hedges 1998; Shu et al. 1999) and that has recently become the most successful predator in the Great Lakes (Smith and Tibble 1980). Does this seemingly invincible species, however, have vulnerable parts? T e answer may be hidden in the same genome that makes the Sea Lamprey so successful. Eventually, knowing the Sea Lamprey genome may enable the identifcation of the Sea Lamprey’s Achilles’ heel. A direct beneft of sequencing the Sea Lamprey genome is new insights into biochemical, genetic, metabolic, and physiological pathways that could be exploited for Sea Lamprey control, with few ef ects on other organisms. It is known that many aspects of Sea Lamprey physiology are substantially dif erent from teleost fsh. T is is expected, because molecular studies of clusters of genes (Force et al. 2002; Irvine et al. 2002) and phylogenetic analysis of gene families (Escriva et al. 2002; Fried et al. 2003) indicate at least one of the two rounds of Sea Lamprey genome duplication happened after divergence between agnathans and gnathostomes. T is independence in genome duplication may be a key evolutionary event that resulted in the agnathan pedigree. T e Sea Lamprey genome sequence will provide a panoramic view of the Sea Lamprey genetic landscape, which, when compared to global views of gnathostome genomes, may unravel the molecular events that could be targeted for Sea Lamprey control. T e Sea Lamprey genome sequence will also facilitate and accelerate research of genetic control of the Sea Lamprey. Rapid development of biotechnology during recent years has generated new strategies for control and eradication of invasive species and pests (Gould 2008). Although autocidal technology has not been feld tested on species outside the insect taxa, this technology has been developed for invasive fsh species under laboratory conditions (T resher 2008). Similar approaches, based on the recombinant genetic technology, should be applicable for Sea Lamprey control. A major obstacle is that the ability to genetically engineer Sea Lampreys is not yet been fully developed. T is problem can be ameliorated, when the ever-increasing array of molecular genetic methods are tested in the Sea Lamprey. When this happens, genomic resources will implicate ample targets for development of a genetic control for the Sea Lamprey.

Summary

The Sea Lamprey Control Program in the Great Lakes is a case study in coordinated and integrated binational fshery management and is the only reported successful control program for a non-indigenous, vertebrate pest species. Since its inception in the mid-1900s, the program has evolved as knowledge and environmental momentum have shifted. Currently, lampricides serve as the backbone of the control program, but various alternative controls, such as barriers, trapping, and sterile-male releases, have also been implemented and are quite successful. Although Sea Lamprey populations in each lake are at about 10 percent of their peak levels prior to the Sea Lamprey Control Program, measures of program success indicate there is much work to be done, as spawning-phase Sea Lamprey abundance and Lake Trout wounding rate estimates are still above targets in most of the lakes. Enhancement of current Sea Lamprey control strategies and development of new strategies are needed to further improve Sea Lamprey control and bring their populations and the damage they infict to target levels. Exciting new prospects wait on the horizon, as more knowledge is gained about pheromone communication in Sea Lamprey and the benefts of having the Sea Lamprey genome sequenced are realized. Successful Sea Lamprey control is the cornerstone of fsh community restoration in the Great Lakes. SEA LAMPREY CONTROL 695

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