Wagner Lab Group » Research

The Ecology of Social Information Use in the Sea Lamprey (Petromyzon marinus)

Dr. Wagner sets up PIT-tag antennas in the Ocqueoc River.

The sea lamprey, Petromyzon marinus, is a rapacious parasite of large-bodied fishes; multiple attacks from its rasping suctorial mouth typically result in the death of the host. Invasion of the Laurentian Great Lakes by the sea lamprey resulted in near extinction of the dominant piscivore (lake trout, Salvelinus namaycush), contributed to the extinction of three endemic fishes – the deepwater cisco (Coregonus johannae), the shortnose cisco (C. reighardi), and the blackfin cisco (C. senithicus) – and set the stage for a population explosion by two invasive prey fishes (alewife, Alosa psuedoharengus, and rainbow smelt, Osmerus mordax). The US and Canadian governments now undertake an integrated pest management program to suppress sea lamprey populations by reducing recruitment to the parasitic stage (pesticide application) and suppressing reproduction (barriers to spawning migrations, sterile male introduction) (Christie and Goddard 2003).

Like humans, lamprey decision-making is strongly influenced by observing the behavior of others, both directly and indirectly. By observing others as they interact with the environment an individual can acquire useful cues (social information) to maximize foraging and mating success via informed habitat selection. This is a form of Public Information, where individuals inadvertently advertise their success and thereby reveal the quality of the local resources upon which other similar organisms also rely. Over time, an animal may evolve innate recognition of the most reliable cues. When those cues are emitted by conspecifics, they move into the realm of direct communication (i.e., a signal).

Mike Twohey of the U.S. Fish and Wildlife Service assists graduate student Mark Luehring with a dye test to map pheromone plumes at the field site.

Olfactory communication plays a critical role in the life of a sea lamprey. Its lifetime fitness is wholly invested in a single reproductive episode that takes place at the end of a long migration from offshore feeding grounds into rivers where it dies soon after spawning. These movements are guided by a symphony of odors. A pheromone emitted by larvae living in stream sediments attracts migrating adults into high quality larval rearing habitats (Sorensen et al. 2005, Wagner et al. 2006, 2009). Another, emitted by mature males, attracts females onto defended nests where spawning commences (Li et al. 2002, Johnson et al. 2009). Our recent work has been heavily focused on: 1) understanding the role of chemical signals used by the sea lamprey to mediate its foraging, migration, and reproduction; and, 2) identifying novel ways to exploit this communication system to achieve sea lamprey control in the Great Lakes. Recent projects are briefly described below. Please contact us for more detailed information.

Migration: The Role of Larval Pheromones

Trevor and Eric prepare the EcoMapper for launch.

Although the role of larval odorants in the riverine migration has received much attention of late (e.g., Wagner et al. 2006, 2009), little is known about the critical interaction between odor, environment, and a migratory lamprey’s tendency to approach and enter a potential spawning stream. In fact, how fishes generally use olfactory information to locate odor sources over large distances (>10 km) in open water remains poorly understood despite considerable research effort (DeBose and Nevitt 2008). Migrating sea lampreys appear to locate potential spawning streams using mechanisms consistent with localization of a large, diffuse odor source (Moore and Crimaldi 2004) and similar to homing behaviors reported for salmon (Doving et al. 1985). Using acoustic telemetry and sophisticated measurement of river plume dynamics (the EcoMapper autonomous underwater vehicle), we are examining the role of larval odorants in each phase of habitat assessment during the transition from lacustrine to riverine migration.

Reproduction: Mate search and female mate preferences

Few reproductive events have as great an impact on individual fitness as finding a proper mate. This biologically profound process requires direct information as to the identity, sexual readiness, and location of potential mates that is typically acquired through multiple sensory channels. The use of odorants to convey reproductive information is likely the most ancient and omnipresent form of reproductive communication (Wyatt 2003). Despite this observation, whether and how vertebrates use pheromones to localize and assess potential mates in natural circumstances remains largely uninvestigated. Thus, recent and growing evidence that mate-prospecting animals (i.e., the choosing sex) make choices in response to variation in both the quantity and quality of chemical advertisements produced by the calling sex is both exciting and expected (Johansson and Jones 2007).

Kris records the behavior of female sea lampreys as they approach cages containing mature males.

John Teeter (1980) and his associates were the first to demonstrate that the odor emitted by a nesting male sea lamprey functions as an attractant to ovulating females; a fact exploited by European fishermen for some time (Fontaine 1938). We now believe that mate-finding by female sea lamprey is a directed process mediated by a pheromone composed of novel bile acids released through the gills of nesting males (Li et al. 2002; Siefkes et al. 2003b, 2005). To date, two putative constituents of the pheromone have been identified: 3-keto-petromyzonol sulfate (3kPZS) and 3-keto-allocholic acid (3kACA) (Li et al. 2002; Yun et al. 2003). Although it’s ultimate role in the sea lamprey mating system may comprise several functions (e.g., mate choice), at a minimum this pheromonal cue operates as an instinctual indicator of male readiness to spawn and likely facilitated the establishment of sea lamprey in the Great Lakes.

We are currently investigating whether and how females discriminate among the odors emitted by individual and grouped male lampreys on the spawning grounds. For example, Mark Luehring (M.S. student) recently discovered that females likely seek the most intense odors in part to ensure contact with groups of males in spawning condition. Identifying odors that indicate a group of ready mates may facilitate reproductive success in female fishes by relaxing the need to remember the quality of recently encountered males for long periods, and thereby reducing the costs of performing mate assessment.

A Sea Lamprey Necromone?

Anne is collecting the odor emitted by putrefying lamprey using Soxhlet extractors.

We've recently confirmed a long-standing anecdotal observation: sea lamprey are chemically aware of, and actively avoid, the odor emitted by dead conspecifics (a so-called necromone). Such avoidance is typically thought to be an indirect response to the threat of predation, revealed through the odor emitting from ruptured or decaying conspecifics (reviewed by Chivers and Smith 1998, Yao et al. 2009). Because predation is one of the most pervasive and powerful selection pressures on individual fitness (Lima and Dill 1990, Wisenden 2000, Brown 2003), there is considerable evidence that indirect predator cues, conveyed through olfactory channels, are used by many species to assess risk associated with space and resource use (e.g., Turner 1997, Dicke and Grostal 2001, Brown 2003). We are currently investigating whether and how the sea lamprey utilizes innate responses to conspecific mortality at least twice in its life-history (stream-resident larvae and migrating immature adults). In both cases, we believe the cue regulates spatial habitat use.

We will be recruiting a new graduate student to work on this project in Fall 2010.

Developing Useful Solutions from Science: Novel Control Strategies for the Great Lakes

Because lamprey attacks threaten a significant fishery (valued at $1.55 billion per year; Ferreri and Taylor 1999), the Great Lakes Fishery Commission (GLFC) undertakes an integrated pest management program to suppress sea lamprey populations (Christie and Goddard 2003). Control is principally achieved through the application of lampricides to exterminate larvae prior to metamorphosis into the destructive parasitic life stage. Although effective, growing concern over the economic and environmental challenges associated with maintaining a large pesticide application program has motivated the GLFC to pursue the use of non-toxic alternatives (GLFC 1992, 2001). We are working to translate our behavioral research findings into new means to control the sea lamprey through the application of pheromones. Here’s an example.

3kPZS: Reverse-Intercept Trapping with a Partial Sex Pheromone

Traditional sea lamprey trapping occurs when upstream migrating lampreys encounter barriers (dams) in early spring. By placing unbaited traps along the dam face lampreys are captured when they encounter the trap while seeking a path around the barrier. These traps enjoy a wide range of efficiency, typically removing 30-40% of the run prior to spawning by intercepting the migration. The residual population will typically spawn in appropriate habitat some distance below the dam.

Johnson et al. (2009) demonstrate clearly the primary function of 3kPZS is to serve as a long-distance beacon to lure females onto nests, and in simple odor landscapes absent additional cues from the male (including his presence), it works effectively to attract females into traps. However, a few investigations aimed at understanding the behavioral responses of female lampreys to 3kPZS in real-life management scenarios have revealed a challenge to using the compound as a trap attractant: 3kPZS is not as fully attractive as the whole sex pheromone. Consequently, simply baiting traps with this partial pheromone during the spawning period will likely have little impact when the females may choose to associate with free-living males.

An array of traps baited with 3kPZS is poised to catch spawning lampreys as night approaches.

We observed that 3kPZS-baited traps tend to do better the closer they are placed to the dam. It appeared the migrants pooled at or near the dam face until maturation and the time of spawning approaches. Lampreys then reversed course and headed downstream to locate spawning habitat and mates. We hypothesized 3kPZS-baited traps will be best positioned to capture the spawners when placed between the dam and the spawning grounds. Here, as lampreys move downstream, they will pass through the odor plumes emitted by the traps before encountering any natural male pheromone and thereby should be more vulnerable to capture. We term this approach a “reverse-intercept” due to the reversal in the direction of movement as opposed to the dam-face traps which simply “intercept” an upstream movement. Adam Thomas recently validated this approach in a full-scale management experiment.