Research to Guide Use of Pheromones to Control Sea Lamprey

The Great Lakes Fishery Commission (GLFC) considers the application of sea lamprey pheromones a promising alternative-control method for its sea lamprey management program. Several components of two pheromones that regulate migration and reproduction, respectively, have been identified and synthesized. Potential utility of these pheromone compounds in lamprey management have been demonstrated in a series of field experiments. These discoveries have laid a solid foundation for development of pheromone-based management. In order to identify potential strategies that will be practical, effective, and economical, we propose a hypothesis driven approach that integrates concepts and experimental methods from several disciplines of biological science, such as neurobiology, biochemistry, and behavioral ecology to illustrate the exact function of identified compounds. In the interim, we identify the necessary steps, or issues critical to eventual implementation, to charter a pathway that leads from laboratory research to effective deployment of pheromones. Finally, we highlight a strategy that fosters collaboration among scientists across disciplines, as well as among research institutes and lamprey control agencies, to accomplish this research agenda. INDEX WORDS: Pheromone, sea lamprey, Petromyzon, reproduction, migration, control. *Corresponding author. E-mail: [email protected] INTRODUCTION Controlling the sea lamprey (Petromyzon marinus), an introduced parasitic predator of commercially and ecologically important fishes, is essential to maintaining a healthy and sustainable ecosystem in the Great Lakes. The Great Lakes Fishery Commission (GLFC), in partnership with Fisheries and Oceans Canada (DFO) and the U.S. Fish and Wildlife Service (USFWS), carries out an integrated pest management program to control sea lampreys in the Great Lakes. The main elements of this program are stock assessments, lampricide application to kill larvae, maintaining barriers to migration, trapping of adults, and controlled release of sterilized males. The future of sea lamprey management lies in the pursuit of new and effective control tactics, including alternatives to lampricide applications. The GLFC (2001) identified field deployment of one new alternative-control method by 2010 as an important milestone for its sea lamprey management program. They also identified the most promising method for future implementation: the application of recently identified pheromones that regulate migratory and reproductive behaviors of the sea lamprey. We prepared this review to construct a visible, transparent, and robust framework for research that supports and catalyzes the development and field deployment of pheromone-based applications. Our primary objective is to discuss the essential research issues through an analysis of current understanding of sea lamprey chemical communication and the information needs. We also seek to develop new research strategies that foster Sea Lamprey Pheromone Research 71 collaboration among scientists across disciplines, as well as among research institutes and lamprey control agencies, to accomplish these objectives. This review contains three primary sections. The first establishes a basic understanding of pheromone communication, much of which derived in the laboratory and from numerous disciplines, ranging from molecular biology to behavioral biology and ecology. It describes both our current understanding and remaining basic research needs. The next section of the paper identifies critical questions and research needs necessary to move pheromone research “from the laboratory to a tool for control”—that is, from basic knowledge to practical implementation as a management tool. Here, we consider some broad questions that relate to the ecological context for the use of pheromones in control, and we present a set of research questions organized around three broad pathways by which pheromones might be used to the greatest effect. The final section lays out the research strategy we envision for realizing all the promises held by lamprey pheromones into an integrated pest management strategy for the Great Lakes. FUNDAMENTAL UNDERSTANDING OF SEA LAMPREY PHEROMONES Sea Lamprey Olfactory Biology Biologically relevant odorants are critical for the sea lamprey to complete its complex life history. Each developmental stage—larvae, parasite, and spawning adult (Applegate 1950, Hardisty and Potter 1971)—is regulated to some extent by odors. Sedentary larval sea lampreys (ammocoetes) have sensitive and mature receptor neurons (VanDenBossche et al. 1995). A study on Pacific lampreys (Lampetra tridentate) implicated odorants in regulation of growth (Mallatt 1983). During the radical transformation from larvae to parasite, the olfactory system undergoes marked elaboration (VanDenBossche et al. 1997) where the sensory epithelium becomes enlarged and integrated into an olfactory apparatus that is highly sensitive to a unique repertoire of compounds (Kleerekoper 1972, Li et al. 1995, Li et al. 2002, Li and Sorensen 1997, Siefkes and Li 2004, Fine et al. 2004, Moore and Schleen 1980, Teeter 1980, Vrieze and Sorensen 2001). Among chordates, sea lamprey olfactory bulbs are exceptionally large relative to the brain (Stoddart 1990). Olfaction is believed to be the key modality that regulates and motivates basic behaviors in post-larval sea lampreys (Kleerekoper 1972), including migration (Bjerselius et al. 2000, Sorensen et al. 2005), mating behavior (Li et al. 2002, 2003a, b; Siefkes et al. 2003a, b; Teeter 1980), and sexual maturation (Li et al. unpublished data). Clearly, the sea lamprey’s complex life history and reliance on identifiable odorants offer ample targets for development of control strategies that exploit a multitude of odor-induced reactions. These strategies, once developed, are likely to be effective, efficient and environmentally benign. The natural odorants that hold the foremost promise for application in lamprey management are pheromones, or “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 specific reaction, for example a definite behavior or developmental process” (Karlson and Luscher 1959). According to their primary function, pheromones are either considered releasers, which elicit immediate behavioral changes, or primers, which induce changes in development and physiology (Wilson and Bossert 1963). Many pheromones have both releasing and priming functions, and the actions of primers often predispose those of releasers. In principle, both types of pheromones have several features favorable for exploitation in population management. Because responses to pheromones are often instinctual, they can be expected from all conspecific individuals at the proper developmental stage (Li et al. 2003b). Overall, we may expect these responses to be specific and robust, rendering target animals vulnerable to manipulation with minute amounts of pheromones (cf. Siefkes et al. 2005, Wagner et al. 2006). The driving force for research into lamprey olfaction is the development of new control methods. However, the research findings also reveal the sea lamprey’s utility as an animal model for the elucidation of fundamental principles of pheromone communication and olfactory transduction in vertebrates. Its male releasing pheromone (a mating pheromone) is the only one identified among fishes (Li et al. 2002, Yun et al. 2002), and the first found to have a large active space (Li et al. 2003b, Siefkes et al. 2005). Lamprey male pheromone function differs from the “chemical spying” of most previously identified fish pheromones (Sorensen and Stacey 1999). In addition, sea lamprey is the only species with a larval migratory pheromone identified (Bjerselius et al. 2000, Fine et al. 2004, Moore and Schleen 1980, Teeter 1980, Vrieze and Sorensen 2001, Sorensen et al. 2005). Sea lamprey and their close relatives typically have large sen-