Possible Applications of Pheromones in an Integrated Sea Lamprey Management Program

J. Great Lakes Res. 29 (Supplement 1):794–800 Internat. Assoc. Great Lakes Res., 2003

Possible Applications of Pheromones in an Integrated Sea Lamprey Management Program Michael B. Twohey1,*, Peter W. Sorensen2, and Weiming Li3 1U.S.

Fish and Wildlife Service Marquette Biological Station 1924 Industrial Pkwy. Marquette, Michigan 49855 2University

of Minnesota Department of Fisheries, Wildlife, and Conservation Biology 200 Hodson Hall 1980 Folwell Ave. St. Paul, Minnesota 55108 3Michigan

State University Department of Fish and Wildlife Natural Resources Bldg., Room 13 East Lansing, Michigan 48824-1222 ABSTRACT. A group of research scientists and fishery managers met during the Sea Lamprey International Symposium II to discuss how recent progress understanding sea lamprey (Petromyzon marinus) pheromone systems might contribute to an integrated management program. Summarized here are those discussions about how pheromone cues might be used and what steps should be taken to develop them as new tools in Great Lakes sea lamprey management. It is now evident that larval sea lampreys release a migratory pheromone that guides maturing adults into streams, and that mature sea lampreys use sex pheromones to affect locomotion and distribution of conspecific individuals on spawning grounds. Synthetic and purified pheromones have potential to enhance trap efficiencies, divert spawning migrations to streams with favorable management characteristics, and disrupt spawning behavior. Populations of native lamprey species might be established in strategic locations to provide migratory pheromone attraction. Pheromone production in spawning-phase males could be enhanced to bait traps and lure females, or to provide sterilized males with a competitive advantage in mating. Assays for analysis of the migratory pheromone could estimate the size of spawning runs and detect larval populations in streams. Pheromone strategies that integrate and enhance existing management techniques are likely to be the most beneficial. For example, the low density of adult sea lampreys in the St. Marys River makes it a good candidate for use of pheromones to enhance the current strategy of sterile-male release and trapping. Variation in recruitment and changes in growth and mortality could affect success of pheromone strategies that reduce reproduction. Continued support for basic research into developing and understanding pheromones and the new technologies associated with them is recommended. INDEX WORDS:

Sea lamprey, migratory pheromone, sex pheromone, integrated pest management.

INTRODUCTION Pheromones are chemical signals that pass between organisms of the same species to communicate (Ben-Ari 1998, Sorensen and Wyatt 2000). Sea *Corresponding

lampreys (Petromyzon marinus) rely heavily upon these cues to find spawning rivers and mates. Since the first Sea Lamprey International Symposium (Teeter 1980), understanding of these systems has progressed to the point where it is now realistic to consider developing management techniques that exploit these natural cues.

author. E-mail: [email protected]

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Pheromones in Sea Lamprey Management Information presented since the first Sea Lamprey International Symposium demonstrates that larval sea lampreys release a potent pheromone which attracts migratory adult sea lampreys into streams (Teeter 1980, Li et al. 1995, Bjerselius et al. 2000, Polkinghorne et al. 2001, Vrieze and Sorensen 2001, Sorensen and Vrieze 2003). A unique bile acid, petromyzonol sulfate, is now known to be a primary component of the migratory pheromone (Sorensen and Vrieze 2003). Convincing evidence was also presented during the first Sea Lamprey International Symposium (Teeter 1980) and during the most recent Sea Lamprey International Symposium II (Li et al. 2003), that sea lampreys use sex pheromones to affect locomotion and distribution of conspecific individuals on spawning grounds. The principal component of the pheromone released by spermiating males has been identified and was demonstrated to attract ovulated females (Li et al. 2003). Similarly, there is clear evidence that post-ovulatory females release a sex pheromone that attracts spermiating males (Teeter 1980, Li et al. 2003). The structure of this pheromone has yet to be characterized. The migratory and sex pheromones function independently of each other. Maturing sea lampreys of both sexes respond to the migratory pheromone and not the sex pheromones (Teeter 1980, Bjerselius et al. 2000), while only sexually mature adults respond to the sex pheromones (Teeter 1980, Li et al. this volume). Pheromones clearly present new opportunities for the integrated management of sea lampreys in the Great Lakes. Pheromones have long been used in insect pest management to detect and monitor pest populations, to attract and remove pests, and to disrupt reproduction (Birch and Haynes 1982). These management strategies are advantageous for insects because pheromones are: 1) active in minute quantities, 2) often specific at the species level, 3) naturally occurring nontoxic products, and 4) potentially economical to develop and apply (Tette 1974). Although pheromones have not yet been approved by the U.S. Environmental Protection Agency for use with vertebrate species, it is likely they will be environmentally friendlier and easier to license as agents for pest control than traditional pesticides. Clearly, strategies based on exploitation of pheromone communication have the potential to further integrate sea lamprey management, offer new capabilities, and improve efficacy of existing techniques. In this manuscript a variety of strategies are pro-

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posed by which pheromones could be used in sea lamprey management, their potential utilities in the program are discussed, and recommendations are made for research and management. These strategies were generated from a discussion during the Sea Lamprey International Symposium II, convened at Lake Superior State University, Sault Ste. Marie, Michigan (U.S.A.), 13 to 18 August 2000. Because pheromones have never before been used in the management of an exotic species of fish and understanding of sea lamprey pheromone systems is far from comprehensive, caution must be used when extrapolating from these ideas. STRATEGIES WHICH EMPLOY PHEROMONES Lure Lampreys into Traps The most obvious use for pheromones is to use them as attractants to enhance capture rates in traps. Both the migratory pheromone and male sex pheromone attract conspecifics. These pheromones likely can be used to attract spawning-phase sea lampreys to sites where traps are installed, and possibly, directly lure the target animals into traps. This is important because trapping efficiencies are presently low and variable at many locations. Conventional sea lamprey traps (Schuldt and Heinrich 1982) are located at barriers to upstream migrations and are most effective with a single attractant water source to lure lampreys into them. Trapping is difficult or ineffective at sites without these characteristics, but could be improved with pheromones. Notably, even small increases in trap capture efficiencies could be extremely beneficial to an integrated lamprey control program that reduces spawning success through trapping and sterile-male (or female) releases (Twohey et al. 2003). Increased trapping efficiency could also benefit the barrier program because barrier efficacy is diminished by the fact that many blocked lampreys will spawn in the lower reaches of rivers, or swim to other rivers to spawn (Applegate and Smith 1950, Kelso and Gardner 2000). Perhaps the greatest promise associated with the migratory pheromone is that it opens the door to entirely new trapping technologies. At present, lamprey traps are designed to catch upstream migrants; thus, they are restricted to those few rivers that can be easily trapped at accessible sites some distance upstream from the river mouth. Traps are only operated for a few weeks of the year during the upstream migration. However, recent tagging studies

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(P.W. Sorensen, University of Minnesota, St. Paul, MN, pers. comm.), and various anecdotal accounts suggest that sea lampreys start searching for rivers many months prior to commencing movement upstream and probably stage in river mouths (Applegate 1950, McLain et al. 1965). Further, Vrieze and Sorensen (2001) find compelling evidence that spawning-phase sea lampreys searching for a suitable stream are strongly influenced by the migratory pheromone. This scenario suggests that it may be possible to design and build pheromone-baited lamprey traps at stream mouths (or perhaps the lake) and place them early in the season to attract animals. By so doing, the geographic extent and duration of trapping activity would be increased. After removal of the females, the males could be sterilized and released back into target streams early in the spawning season, which would allow more time for the animals to integrate into the resident population. Although the ability of the migratory pheromone to lure adult lampreys from distances is presently poorly understood, anecdotal data are promising. Vrieze and Sorensen (2001) note that adult sea lamprey distribution in a laboratory maze was influenced by larval holding water (migratory pheromone) added to lake water at 5°C, a temperature well below that associated with riverine migration. The migratory pheromone was attractive when introduced in the lower stretches of flowing streams and tested on early-run animals (Bjerselius et al. 2000). Attraction to the migratory pheromone was greatly enhanced by small increases in stream velocity, a variable that is easily manipulated. Finally, Vrieze and Sorensen (2001) note that other extractable stream odors strongly synergize the action of the pheromone. These data suggest that a strong long-distance lure could be designed for use early in the spawning season, perhaps even in the lower stretches of some rivers with low velocities. Potential sources of the pheromone include crude larval extracts (a technology being developed at present), synthesized pheromone, or even aggregations of native lamprey species located upstream of barriers to the sea lamprey spawning migration. The migratory pheromone appears to have great promise for use in many ways that would greatly expand the duration, geographic range, and efficacy of current trapping technologies. As with the migratory pheromone, sex pheromones have potential to extend both the time and geographic areas where trapping of spawningphase sea lampreys could be effective. Laboratory

tests suggest that male and female sea lampreys, once mature, release sex pheromones that communicate their gender and attract the opposite sex (Teeter 1980). Current trapping techniques are most effective in capturing spawning-phase sea lampreys at barriers to upstream migration before they are sexually mature. Once mature, animals that have eluded capture in traditional traps might be vulnerable to capture near the spawning grounds in traps baited with sex pheromones. For sea lampreys, the male sex pheromone is better understood than the female sex pheromone and shows the most potential for luring females into traps. It has been shown to lure ovulated female sea lampreys to scented sites on a spawning ground (Li et al. 2003). Removal of female reproductive potential would particularly enhance strategies of sterile-male release and trapping as employed in the St. Marys River, or other sites where reproductive disruption has been contemplated (Twohey et al. 2003). Synthetic pheromones and concentrated washings from mature animals are potential sources of suitable sex pheromone. Techniques are being developed to increase sex pheromone production in male lampreys that could allow males to be used as a potent bait source. Disrupt Key Mating Behaviors Just as pheromones provide cues to assist sea lampreys in locating suitable spawning streams and successful reproduction, these cues could be used to confuse and confound mating signals. Potential strategies for using pheromones to disrupt insect mating have been proposed, tested, and implemented with at least some success (Carde 1990, Carde and Minks 1995). These strategies are based on generating sensory adaptation or habituation, promoting competition between the natural pheromone and synthetic disruptor, camouflaging the pheromone plumes generated, creating imbalance in sensory inputs, or releasing antagonists. All these strategies have the potential to be applied in sea lamprey management and would have high value for reducing reproduction in targeted rivers if coupled with other strategies. Increase Sex Pheromone Production in Sterile-male Sea Lampreys Since 1991, sea lamprey management agencies have implemented a sterile-male-release program in which male lampreys are sterilized and stocked into

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spawning grounds to compete with fertile males for mates (Twohey et al. 2003). Sterilized male sea lampreys are known to compete effectively with fertile males in mating (Hanson and Manion 1978, 1980). Recently, male sea lampreys sterilized with bisazir have also been found to release the sex pheromone at a level similar to that of non-sterile males (Li et al. 2003), suggesting that production of the male sex pheromone is not affected by the sterilant. It is postulated that if production of the male sex pheromone were increased in sterile-male sea lampreys, they would have a competitive advantage over untreated males in obtaining mates. If this hypothesis is correct, and if a technique can be developed to induce sterile males to produce and release the sex pheromone at a higher level and/or for a longer period of time (up-regulated), the efficacy of the current sterile-male-release technique could be substantially improved. Introduction of up-regulated sterile males would have the same effect as releasing additional sterile males into the resident population. This benefit may prove to be far-reaching because the current application of the sterile-male-release technique is limited by the supply of males suitable for sterilization (Twohey et al. 2003). In particular, this method has potential to further suppress sea lamprey reproduction in the St. Marys River, the stream in which the sterile-malerelease technique has been most intensively implemented. This method may also enable extension of the sterile-male-release technique into additional tributaries of the Great Lakes or Lake Champlain with the current supply of males. Potential constraints on this strategy are twofold. First, it has yet to be experimentally proven that sterile males with up-regulated sex pheromone production have a distinct advantage in competing for mates. Second, the development of techniques to potentiate pheromone production may prove to be challenging and time consuming. The main limitation is that the regulation of this pheromone is not fully understood. Nonetheless, its release has been clearly linked to spermiation (Li et al. 2003), which often results from surges of plasma reproductive hormones. It may be possible to use hormones to potentiate pheromone synthesis in sterile males.

management objectives. Lampricide treatments, which temporarily remove the larval source of the migratory pheromone from a river, cause some migrating sea lampreys that would normally be attracted to that river to choose other streams with the pheromone (Moore and Schleen 1980). Sorensen and Vrieze (2003) suggest that the migratory pheromone might be used to draw migratory adults away from rivers that are difficult to treat with lampricide, or where the treatment cycle could be extended if the number of spawning-phase sea lampreys could be reduced. Application of synthetic pheromone, manipulation of native larval populations, and coordination of lampricide treatments may have the combined potential to divert sea lampreys from some streams and draw them into others that are scheduled for lampricide treatment, have effective trapping facilities, or where reproductive success is low. Increased migration into streams with effective traps could be very useful to augment the supply of males for use in the sterilemale-release technique. The sex pheromones have potential to attract sexually mature male and female lampreys into distinct areas of rivers where spawning habitat and larval survival are poor. Male and female lampreys might be lured to separate areas of a river system to prevent mate-finding. The sex and migratory pheromones might be useful in a combined strategy to draw migrating sea lampreys into unproductive areas of rivers and hold them there until they spawned. One concern about these strategies is that it is unclear whether sufficient attraction to a specific stream could be created to reduce reproduction in an adjacent river to levels that would affect the lampricide treatment schedule. Migratory cues that lampreys use to find and enter spawning rivers are likely to be complex and involve many factors (Teeter 1980, Sorensen and Vrieze 2003). The complexity of these cues, interference from migratory pheromones released by untreated native lamprey species, and potential effects of density-dependent compensation and density-independent variation (Jones et al. 2003) are potential constraints on the feasibility of these approaches.

Divert or Draw Adult Sea Lampreys into Selected Rivers or Tributaries Migratory and sex pheromones could be employed to direct spawning migrations to selected locations and away from others to achieve specific

Assess Riverine Levels of Pheromones Relatively easy to use and highly sensitive immunoassays are currently being developed for assessing the concentration of the migratory pheromone and the male sex pheromone in water.

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Assays are needed to assess ambient levels of pheromone which are indicative of the concentration necessary for effective management. These assays may also have potential for use in population assessment, but their usefulness will be limited as specific levels of pheromone are likely influenced by natural degradation. Pheromone production and release are probably correlated with sea lamprey biomass of certain life stages (Moore and Schleen 1980, Teeter 1980, Sorensen and Vrieze 2003), and could predict larval and adult population size. An assay that measures the concentration of migratory pheromone might conceivably be used to assess larval biomass and predict relative strength of spawning runs. The potential use of pheromone concentration for assessing larval populations may be limited to determining presence or absence of lampreys, but not lamprey species. Nevertheless, the ability to quickly determine the presence or a change in the biomass of larval lampreys, followed by direct assessment by electrofishing, may be valuable because of the tremendous expense of assessing sea lamprey populations in streams. Additionally, migratory pheromone concentration might be useful to improve estimates of adult sea lampreys in the Great Lakes and to predict the size of spawning runs. The number of adult sea lampreys entering tributaries to spawn is presently estimated from a regression model that accounts for the distribution of spawning-phase sea lampreys into tributaries using trap catch data on a subset of streams (Mullett et al. 2003). The number of years since a stream was last treated is a variable in the model and provides a relative indication of the size of the larval population and its attraction for spawning-phase sea lampreys (Moore and Schleen 1980, Teeter 1980, Sorensen and Vrieze 2003). The model might be improved by using direct measurements of migratory pheromone concentration in streams in lieu of the number of years since treatment. The relative size of the spawning run in individual streams might also be predicted and would be useful for planning trapping operations. It seems likely that this information could help in understanding factors that control lamprey distribution. Assays for the sex pheromones could be useful to assess the general size of the spawning population, determine presence or absence of mature lampreys in tributaries, and to assist in timing releases of sterile males. Accuracy of this tool might be poor if the compound rapidly degrades or if its release is uneven during the spawning migration. Since the

assay would not likely produce a highly accurate estimate of spawner numbers, such use might be limited to rivers where sea lamprey traps are not effective. DENSITY DEPENDENT AND INDEPENDENT EFFECTS AND INTEGRATED MANAGMENT STRATEGIES Because all pheromone strategies discussed herein are aimed at reducing sea lamprey reproductive success, their possible effects on reducing parasitic sea lamprey populations may be limited by density-dependent changes in hatching, growth, and mortality (compensation), and by density-independent recruitment variation. Jones et al. (2003) found evidence of such compensation in experimental sea lamprey populations, but not at low sea lamprey densities that currently are typical in the Great Lakes. Compensation at low densities may have been masked by substantial density-independent variation in recruitment. The investigators observed a wide range of recruitment for any given stock size. Further simulation modeling suggested that variation in recruitment could reduce the effectiveness of techniques that reduce reproduction. However, they noted that density-independent variation in recruitment was reduced when spawner densities were low. To be successful, strategies for reproductive suppression will need to reduce reproduction below a threshold where density-dependent and density-independent effects could limit their success. Perhaps the most useful pheromone strategies will be those that integrate and enhance existing management actions to further lower reproduction. The St. Marys River is a good example of a site where pheromone applications have potential for integration with existing management strategies to increase the effectiveness of control. This river is the largest source of sea lampreys in the Great Lakes and is too large to treat with conventional lampricides, yet it attracts a relatively low density of spawning-phase sea lampreys (Schleen et al. 2003). The combination of sterile-male releases and trapping during 1997 to 2000 reduced reproduction in the St. Marys River by an estimated average of 87% (Klar and Schleen 2001). Although the ability of pheromones to increase trap efficiency is presently unknown, it can be calculated that an improvement in trap efficiency in the St. Marys River, from the current 45% to 65%, and including the sterilization and release of the additional 2,700 male captures, would improve the average overall

Pheromones in Sea Lamprey Management suppression in the river to 95%. By way of comparison, an equivalent level of improvement in control based on adding more sterile males alone would require an additional 49,000 males, a number of animals which is simply not available. Increasing (or controlling) the release of sex pheromone in sterilized males to make them more attractive might also yield significant benefits at low cost. These combined techniques could compliment each other. Key to an effective management program will be the integration of a variety of highly effective tools based on different aspects of the lamprey life history, and pheromones help achieve this. RESEARCH AND MANAGEMENT RECOMMENDATIONS Recent support for pheromone research has resulted in new understanding and the potential to develop new management strategies. It appears that integration of pheromone applications with trapping and sterile-male releases has the greatest potential for improving suppression of sea lamprey populations. These strategies seem feasible and would enhance existing methods. Some of the other strategies discussed above, such as disruption of mating behaviors and diversion of the spawning migration, may eventually play an important role in sea lamprey management, but would take a longer time to develop. To implement any of the strategies discussed above, a comprehensive understanding of pheromone communication in sea lampreys will be needed. The migratory and male sex pheromones need to be fully characterized, and the female sex pheromone still needs to be identified. Sea lamprey control managers and researchers should investigate the dynamics of pheromone distribution and the physiological and behavioral mechanisms of lamprey response to the pheromones. These investigations would include the processes by which sea lampreys find rivers for spawning, how pheromone plumes enter lakes, how sea lampreys follow these plumes, if pheromones can lead lampreys into traps, the effective ranges of pheromone concentration, persistence of pheromones in water, and the effects of ambient concentrations in rivers. Other studies should include methods to enhance native lamprey populations above barriers and the potential effect of the pheromones released by those populations on the size of spawning runs. Historic records of lampricide treatments and sea lamprey assessments could be analyzed to ascertain effects of location

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and larval population sizes (native and sea lamprey species) on sea lamprey spawning migrations. The regulation of male pheromone production needs further study in order to develop a technique to enhance its release. Other approaches to mating disruption may have potential, but more study is needed to clarify the functions and regulation of pheromone communication. Perhaps most importantly, economical means to synthesize these pheromones need to be developed. Understanding how pheromones work will prove useful in developing new and powerful strategies for integrated management of sea lampreys. As knowledge of pheromone communication and sea lamprey behavior is increased, and approaches to using these technologies become clear, management objectives must be established. A task force structure has been useful to the Great Lakes Fishery Commission in guiding new technologies into new management initiatives (Schleen et al. 2003, Twohey et al. 2003) and again should be useful in the development of pheromone technology. ACKNOWLEDGMENTS Participants in the discussion group at the Sea Lamprey International Symposium II that initiated this paper included Marc Bacigalupi, Michael Boogaard, Phil Cochran, Jared Fine, Cheryl Kaye, Dave Nettles, Mike Siefkes, Bill Swink, Lance Vrieze, and the authors. REFERENCES Applegate, V.C. 1950. Natural history of the sea lamprey (Petromyzon marinus) in Michigan. U.S. Fish Wildl. Serv. Spec. Sci. Rep. Fish. 55. ———, and Smith, B.R. 1950. Sea lamprey spawning runs in the Great Lakes, 1950. U.S. Fish Wildl. Serv. Spec. Sci. Rep. Fish. 61. Ben-Ari, E.T. 1998. Pheromones: What’s in a Name? BioScience 48: 505–511. Birch, M.C., and Haynes, K.F. 1982. Insect pheromones. Stud. Biol. 147. Bjerselius, R., Li, W., Teeter, J.H., Seelye, J.G., Johnsen, P.R., Maniak, P.J., Grant G.C., Polkinghorne, C.N., and Sorensen, P.W. 2000. Direct behavioral evidence that unique bile acids released by larval sea lamprey function as a migratory pheromone. Can. J. Fish. Aquat. Sci. 57:557–569. Carde, R.T. 1990. Principles of mating disruption. In Behavior-Modifying Chemicals for Pest Management: Applications of Pheromones and Other Attractants, eds. R.L. Ridgway, R.M. Silverstein, and M.N. Inscoe, pp. 47–71. New York: Marcel Dekker.

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Polkinghorne, C.A., Olson, J.M., Gallaher, D.G., and Sorensen, P.W. 2001. Larval sea lamprey release two unique bile acids to the water at a rate which is sufficient to produce a detectable pheromonal plume. Fish Physiol. Biochem. 25:15–30. Schleen, L.P., Christie, G.C., Heinrich, J.W., Bergstedt, R.A., Young, R.J., Morse, T.J, Lavis, D.S., Bills, T.D., Johnson, J.E., and Ebener, M.P. 2003. Development and implementation of an integrated program for control of sea lampreys in the St. Marys River. J. Great Lakes Res. 29 (Suppl. 1):677–693. Schuldt, R.J., and Heinrich, J.W. 1982. Portable trap for collecting adult sea lampreys. Prog. Fish-Cult. 44:220–221. Sorensen, P.W., and Vrieze, L.A. 2003. The chemical ecology and potential application of the sea lamprey migratory pheromone. J. Great Lakes Res. 29 (Suppl. 1):66–84. ——— , and Wyatt, T.D. 2000. Pheromones. In The Corsini Encyclopedia of Psychology and Behavioral Science, 3 rd Ed., eds. W.E. Craighead and C.B. Nemeroff, pp. 1193–1195. New York: John Wiley and Sons. Teeter, J. 1980. Pheromone communication in sea lampreys (Petromyzon marinus): implications for population management. Can. J. Fish. Aquat. Sci. 37:2123–2132. Tette, J.P. 1974. Pheromones in insect population management. In Pheromones, ed. M. Birch, pp. 399–410. Amsterdam: North-Holland. Twohey, M.B., Heinrich, J.W., Seelye, J.G., Fredricks, K.T., Bergstedt, R.A., Kaye, C.A., Scholefield, R.J., McDonald, R.B., and Christie, G.C. 2003. The sterilemale-release technique in Great Lakes sea lamprey management. J. Great Lakes Res. 29 (Suppl. 1): 410–423. Vrieze, L.A.,and Sorensen, P.W. 2001. Laboratory assessment of the role of a larval pheromone and natural stream odor in spawning stream localization by migratory sea lamprey (Petromyzon marinus). Can. J. Fish. Aquat. Sci. 58:2374–2385. Submitted: 7 June 2001 Accepted: 5 June 2002 Editorial handling: Michael L. Jones