ABSTRACT
A diversity of aquatic organisms manage predation risk by avoiding waters activated with conspecific alarm cues, a chemical mixture released from injuries. The sea lamprey (Petromyzon marinus) is a nocturnal migratory species that relies on its alarm cue to navigate around areas of predation risk when moving through river channels. Identification of the cue's chemistry would allow managers to harness this innate behavioral response to guide migrating sea lamprey to traps (invasive population in the Laurentian Great Lakes) or to fish passage devices where dams block migrations in their native range. We pursued isolation of the sea lamprey alarm cue through behaviorally guided fractionation, fractionating the alarm cue into water-soluble and chloroform-soluble fractions, each of which elicited a substantial avoidance response. Recombining the two fractions restored full reactivity, suggesting the alarm cue mixture contains components that exhibit high solubility in water (e.g., nitrogenous compounds), chloroform (e.g., lipids), or perhaps materials that dissolve readily in either solvent. We further screened 13 individual compounds or pure isolates and 6 sub-fractions from the water-soluble fraction and found one of the pure isolates, isoleucine, evoked an avoidance response on its own, but not consistently when found in other mixtures. In a third experiment, we observed no behavioral response after recombining 32 compounds isolated and identified from the water-soluble fraction. These results confirm other suggestions that the process of elucidating alarm cue constituents is challenging. However, we suggest the pursuit is worthwhile given the strong evidence for the utility of alarm cues for use in the conservation and management of fishes and other aquatic organisms.
Subject(s)
Petromyzon , Animals , Petromyzon/physiology , Cues , Chloroform , Water , FishesABSTRACT
Use of the first fish pheromone biopesticide, 3-keto petromyzonol sulfate (3kPZS) in sea lamprey (Petromyzon marinus) control requires an understanding of both how the amount 3kPZS applied to a trap relates to catch, and how that relationship varies among stream types. By conducting 3kPZS dose-response experiments over two years and across six varied trapping contexts, we conclude (1) that 3kPZS application is best standardized by how much is emitted from the trap instead of the fully mixed concentration achieved downstream, and (2) that 3kPZS is more effective in wide streams (>30 m). In wide streams, emission of 3kPZS at 50 mg hr.-1 from the trap increased capture rate by 10-15% as sea lamprey were 25-50% more likely to enter the trap after encounter. However, in narrow streams (< 15 m), 50 mg hr.-1 3kPZS generally reduced probabilities of upstream movement, trap encounter, and entrance. While 3kPZS significantly influenced upstream movement, encounter, and capture probabilities, these behaviors were also highly influenced by water temperature, stream width, sea lamprey length, and sex. This study highlights that a pheromone component in a stream environment does not ubiquitously increase trap catch in all contexts, but that where, how, and when the pheromone is applied has major impacts on whether it benefits or hinders trapping efforts.
Subject(s)
Biological Control Agents/pharmacology , Cholic Acids/pharmacology , Pest Control, Biological/methods , Petromyzon/physiology , Pheromones/pharmacology , Animals , Dose-Response Relationship, Drug , Female , MaleABSTRACT
Movement data provide a window - often our only window - into the cognitive, social and biological processes that underlie the behavioural ecology of animals in the wild. Robust methods for identifying and interpreting distinct modes of movement behaviour are of great importance, but complicated by the fact that movement data are complex, multivariate and dependent. Many different approaches to exploratory analysis of movement have been developed to answer similar questions, and practitioners are often at a loss for how to choose an appropriate tool for a specific question. We apply and compare four methodological approaches: first passage time (FPT), Bayesian partitioning of Markov models (BPMM), behavioural change point analysis (BCPA) and a fitted multistate random walk (MRW) to three simulated tracks and two animal trajectories - a sea lamprey (Petromyzon marinus) tracked for 12 h and a wolf (Canis lupus) tracked for 1 year. The simulations - in which, respectively, velocity, tortuosity and spatial bias change - highlight the sensitivity of all methods to model misspecification. Methods that do not account for autocorrelation in the movement variables lead to spurious change points, while methods that do not account for spatial bias completely miss changes in orientation. When applied to the animal data, the methods broadly agree on the structure of the movement behaviours. Important discrepancies, however, reflect differences in the assumptions and nature of the outputs. Important trade-offs are between the strength of the a priori assumptions (low in BCPA, high in MRW), complexity of output (high in the BCPA, low in the BPMM and MRW) and explanatory potential (highest in the MRW). The animal track analysis suggests some general principles for the exploratory analysis of movement data, including ways to exploit the strengths of the various methods. We argue for close and detailed exploratory analysis of movement before fitting complex movement models.
Subject(s)
Animal Distribution , Ecology/methods , Ethology/methods , Homing Behavior , Petromyzon/physiology , Wolves/physiology , Animals , Models, Biological , MovementABSTRACT
The sea lamprey, Petromyzon marinus, is emerging as a model organism for understanding how pheromones can be used for manipulating vertebrate behavior in an integrated pest management program. In a previous study, a synthetic sex pheromone component 7α,12α, 24-trihydroxy-5α-cholan-3-one 24-sulfate (3kPZS) was applied to sea lamprey traps in eight streams at a final in-stream concentration of 10(-12) M. Application of 3kPZS increased sea lamprey catch, but where and when 3kPZS had the greatest impact was not determined. Here, by applying 3kPZS to additional streams, we determined that overall increases in yearly exploitation rate (proportion of sea lampreys that were marked, released, and subsequently recaptured) were highest (20-40%) in wide streams (~40 m) with low adult sea lamprey abundance (<1000). Wide streams with low adult abundance may be representative of low-attraction systems for adult sea lamprey and, in the absence of other attractants (larval odor, sex pheromone), sea lamprey may have been more responsive to a partial sex pheromone blend emitted from traps. Furthermore, we found that the largest and most consistent responses to 3kPZS were during nights early in the trapping season, when water temperatures were increasing. This may have occurred because, during periods of increasing water temperatures, sea lamprey become more active and males at large may not have begun to release sex pheromone. In general, our results are consistent with those for pheromones of invertebrates, which are most effective when pest density is low and when pheromone competition is low.
Subject(s)
Introduced Species , Pest Control/instrumentation , Petromyzon/physiology , Sex Attractants , Animals , Behavior, Animal/drug effects , Female , Male , Michigan , Ontario , Sex Attractants/pharmacologyABSTRACT
Spermiating male sea lamprey (Petromyzon marinus) release a sex pheromone, of which a component, 7α, 12α, 24-trihydoxy-3-one-5α-cholan-24-sulfate (3kPZS), has been identified and shown to induce long distance preference responses in ovulated females. However, other pheromone components exist, and when 3kPZS alone was used to control invasive sea lamprey populations in the Laurentian Great Lakes, trap catch increase was significant, but gains were generally marginal. We hypothesized that free-ranging sea lamprey populations discriminate between a partial and complete pheromone while migrating to spawning grounds and searching for mates at spawning grounds. As a means to test our hypothesis, and to test two possible uses of sex pheromones for sea lamprey control, we asked whether the full sex pheromone mixture released by males (spermiating male washings; SMW) is more effective than 3kPZS in capturing animals in traditional traps (1) en route to spawning grounds and (2) at spawning grounds. At locations where traps target sea lampreys en route to spawning grounds, SMW-baited traps captured significantly more sea lampreys than paired 3kPZS-baited traps (~10% increase). At spawning grounds, no difference in trap catch was observed between 3kPZS and SMW-baited traps. The lack of an observed difference at spawning grounds may be attributed to increased pheromone competition and possible involvement of other sensory modalities to locate mates. Because fishes often rely on multiple and sometimes redundant sensory modalities for critical life history events, the addition of sex pheromones to traditionally used traps is not likely to work in all circumstances. In the case of the sea lamprey, sex pheromone application may increase catch when applied to specifically designed traps deployed in streams with low adult density and limited spawning habitat.
Subject(s)
Environment , Petromyzon/physiology , Sex Attractants/chemical synthesis , Sex Attractants/pharmacology , Animals , Ecosystem , Female , Male , Ovulation/drug effectsABSTRACT
Background: Little is known about the transformer stage of the parasitic lampreys, a brief but critical period that encompasses juvenile out-migration from rivers to lakes or oceans to begin parasitic feeding. Information about this life stage could have significant conservation implications for both imperiled and invasive lampreys. We investigated tag retention, survival, wound healing, and swim performance of newly transformed sea lamprey (Petromyzon marinus) implanted with a new micro-acoustic transmitter, the eel-lamprey acoustic transmitter (ELAT), in a controlled laboratory environment. Results: The 61-day survival of our tagged subjects was 71%, within the range reported in similar studies of juvenile lampreys. However, survival was significantly lower in the tagged animals (vs control), with no effect statistically attributable to measures of animal length, mass, condition, or population of origin (Great Lakes vs. Atlantic drainage). Mortality in tagged fish was concentrated in the first four days post-surgery, suggesting injury from the surgical process. An unusually long recovery time from anesthesia may have contributed to the increased mortality. In a simple burst swim assay, tagged animals swam significantly slower (- 22.5%) than untagged animals, but were not significantly different in endurance swim tests. A composite wound healing score at day four was a significant predictor of maximum burst swim speed at day 20, and wound condition was related to animal mass, but not length, at the time of tagging. Conclusions: Impairments to survival and swim performance of juvenile sea lamprey implanted with the ELAT transmitter were within currently reported ranges for telemetry studies with small, difficult to observe fishes. Our results could be improved with more refined anesthesia and surgical techniques. The ability to track migratory movements of imperiled and pest populations of parasitic lampreys will improve our ability to estimate vital rates that underlie recruitment to the adult population (growth, survival) and to investigate the environmental factors that regulate the timing and rates of movement, in wild populations.
ABSTRACT
The sea lamprey, Petromyzon marinus, is a harmful invader of the Laurentian Great Lakes. The odor emitted by larval lampreys resident to streams attracts migrating adults to high quality spawning habitats. Three components of the larval pheromone have been identified and tested in laboratory settings: petromyzonol sulfate, petromyzosterol disulfate, and petromyzonamine disulfate. Here, we report the first field test of six mixtures of synthetic versions of these pheromone components, and we compare lamprey responses to these with those elicited by the complete larval odor in a natural stream. Exposure to larval odor both increased upstream movement and attracted migrants into the portion of a channel containing the odor. No tested combination of synthetic pheromone components proved similarly attractive. These findings suggest the existence of unknown additional components of the pheromone that await discovery and are likely necessary if the pheromone is to be useful in management of this pest. Further, we hypothesize that the complete pheromone mixture is necessary to attract migrants into spawning habitat at the conclusion of the migration, whereas a partial pheromone may be effective at the transition from lake to stream when natural factors both dilute and alter the ratio of components from that actually emitted by sea lamprey larvae.
Subject(s)
Petromyzon/physiology , Pheromones/pharmacology , Animals , Behavior, Animal/drug effects , Cholestanes/chemistry , Cholestanes/pharmacology , Cholic Acids/chemistry , Cholic Acids/pharmacology , Larva/metabolism , Odorants , Petromyzon/growth & development , Pyrrolidinones/chemistry , Pyrrolidinones/pharmacology , RiversABSTRACT
The detection of predation risk without direct engagement with a predator is an important driver of prey movement strategies. Consequently, the application of alarm cues may prove an effective tool in guiding the movements of fishes targeted for control or conservation. However, failure to contemplate the sensory, physiological and cognitive outcomes of repeated or persistent exposure to the cue will likely lead to poor performance of management practices. Using a series of behavioural tests and physiological recordings from the olfactory organ, we examined the timing of onset and recovery of the alarm response in sea lamprey (Petromyzon marinus L.) when exposed continuously or sporadically to its alarm cue. In the laboratory, sea lamprey exhibited short-term, reversible attenuation of the alarm response over 2-4 h with continuous exposure. The alarm response spontaneously recovered after 30-60 min of removal from the cue. In long-duration free-swimming tests, where the animals were allowed to move into and out of the odour plume volitionally, repeated but sporadic encounter with the alarm cue over 5 h did not alter the alarm response. Electro-olfactogram recordings from the main olfactory epithelium indicated that olfactory sensory neurons quickly adapt to alarm cue and recovered within 15 min. Our findings strongly implicate habituation as the mechanism that induces reduction in the alarm response and provide insight into the design of effective management practices that seek to use fish alarm cues as repellents.
ABSTRACT
Fish use odor to avoid exposure to predation and disease. Harnessing these odors as repellents is proving useful for management initiatives that conserve native species or control invasive populations. Here, we evaluated the behavioral response of invasive sea lamprey to putrescine, a decay molecule that many prey organisms avoid. Putrescine is found in tissue extracts that contain sea lamprey alarm cue, and human saliva, two mixtures known to elicit flight and avoidance responses in migratory sea lamprey. We used two behavioral assays to evaluate metrics of repellency: behavioral preference (space use) and change in activity rates and found context-dependent results. In smaller assays with individual fish, we found that putrescine had no effect on sea lamprey activity but did induce avoidance. In larger assays with multiple animals, sea lamprey did not avoid putrescine. Our results also showed consistent changes in activity and avoidance behavior in sea lamprey exposed to alarm cue in the smaller assay, concluding that this design could prove useful as a high-throughput screening tool. We also investigated a novel odor identified in sea lamprey skin, petromyzonacil, and found no behavioral effects to this odor on its own or in synergy with putrescine. Our results show limited evidence that putrescine acts as robust repellent for sea lamprey and highlight the importance of environmental context when interpreting avoidance behavior in laboratory settings.
Subject(s)
Petromyzon , Animals , Humans , Odorants , Petromyzon/physiology , Predatory Behavior , Putrescine/pharmacology , Tissue ExtractsABSTRACT
Sea lamprey (Petromyzon marinus), a parasitic fish which survives on blood of other fishes, is consumed as a delicacy in many countries. Our earlier studies on sea lamprey compounds that showed potential to deter adult sea lampreys yielded several sterols, glycerides, free fatty acids, amino acids, organic acids and nitrogenous compounds. Therefore, this study was to assess the health-benefits of these compounds including additional isolates from HPLC fractions that kept aside due to lack of activity in sea lamprey deterrent assays. In vitro cyclooxygenase enzymes (COX-1 and -2) and lipid peroxidation (LPO) inhibitory assays, respectively, were used to determine antiinflammatory and antioxidant activities. Among the tested sterols, cholesteryl eicosapentaenoate and cholesteryl arachidonate exhibited IC50 values of 14.6 and 17.7 µg/mL for COX-1 and 17.3 and 20.8 µg/mL for COX-2, respectively. Cholesteryl palmitate and cholesteryl oleate showed moderate COX-1 and COX-2 enzyme inhibition at 25 µg/mL. Amino acids arginine, tyrosine, glutamic acid, tryptophan and asparagine also showed moderate COX-1 and COX-2 inhibition at the same concentration. Among the twelve new isolates from fractions that we did not investigate earlier, a novel uracil derivative petromyzonacil showed COX-1 and COX-2 inhibition at 25 µg/mL by 35 and 15%, respectively. Cholesterol esters tested at 25 µg/mL exhibited LPO inhibition between 38 and 82 percent. Amino acids cysteine, methionine, aspartic acid, threonine, tryptophan, histidine, glutamic acid, phenylalanine and tyrosine at 25 µg/mL showed LPO inhibition between 37 and 58% and petromyzonacil by 32%. These assay results indicate that consumption of sea lamprey offer health-benefits in addition to nutritional benefits.
Subject(s)
Petromyzon/metabolism , Animals , Anti-Inflammatory Agents/pharmacology , Antioxidants/metabolism , Biological Assay , Cyclooxygenase 1/metabolism , Cyclooxygenase 2/metabolism , Lipid Peroxidation/drug effectsABSTRACT
Migratory prey experience spatially variable predation across their life cycle. They face unique challenges in navigating this predation landscape, which affects their perception of risk, antipredator responses, and resulting mortality. Variable and unfamiliar predator cues during migration can limit accurate perception of risk and migrants often rely on social information and learning to compensate. The energetic demands of migration constrain antipredator responses, often through context-dependent patterns. While migration can increase mortality, migrants employ diverse strategies to balance risks and rewards, including life history and antipredator responses. Humans interact frequently with migratory prey across space and alter both mortality risk and antipredator responses, which can scale up to affect migratory populations and should be considered in conservation and management.
Subject(s)
Ecology , Predatory Behavior , Animals , Cues , Humans , LearningABSTRACT
The sea lamprey (Petromzons marinus) is a devastating invasive species that represents a significant impediment to restoration of the Laurentian Great Lakes. There is substantial interest in developing environmentally benign control strategies for sea lamprey, and many other aquatic invasive species, that employ the manipulation of semiochemical information (pheromones and chemical cues) to guide the movements of invaders into control opportunities (e.g. traps, locations for safe pesticide application, etc.). A necessary precursor to the use of semiochemicals in conservation activities is the identification of the chemical constituents that compose the odors. Here, we characterize the major nitrogenous substances from the water-soluble fraction of a skin extract that contains the sea lamprey alarm cue, a powerful repellent that has proven effective in guiding the movements of migrating sea lamprey in rivers. Nitrogenous compounds are suspected components of fish alarm cues as the olfactory sensory neurons that mediate alarm responses transduce amino acids and related compounds. A laboratory assay confirmed the behavioral activity contained in the alarm cue resides in the water-soluble fraction of the skin extract. This water-soluble fraction consisted primarily of creatine (70%), heterocyclic nitrogenous compounds (4.3%) and free amino acids (18.4%), respectively. Among the free amino acids characterized in our study, essential amino acids constituted 13% of the water-soluble fraction. Free amino acids isolated from the water-soluble fraction composed of arginine, phenylalanine, threonine, and asparagine 3.9, 2.7, 2.6 and 2.4% of the water-soluble fraction, respectively. We discuss the implications of these findings for understanding the nature and use of the sea lamprey alarm cue in conservation activities.
Subject(s)
Nitrogen Compounds/analysis , Petromyzon/physiology , Animal Migration , Animals , Female , Great Lakes Region , Introduced Species , Male , Nitrogen Compounds/metabolism , Skin/chemistry , Skin/metabolismABSTRACT
Visual and olfactory stimuli induce behavioural responses in fishes when applied independently, but little is known about how simultaneous exposure influences behaviour, especially in downstream migrating fishes. Here, downstream moving juvenile sea lamprey (Petromyzon marinus) were exposed to light and a conspecific chemosensory alarm cue in a flume and movement were monitored with overhead cameras and nets. When exposed to light, sea lamprey were more likely to be captured in a net closest to the light array. When exposed to the alarm cue, sea lamprey transit rate through the flume increased, but sea lamprey did not avoid the alarm cue plume by moving perpendicular to flow. When the alarm cue and light were applied simultaneously in a push and pull configuration, the alarm cue still triggered enhanced downstream movement (push downstream) and more sea lamprey was still captured in the net nearest the light (pull to the side), resulting in twice as many sea lamprey being captured in the lighted net relative to controls. To our knowledge, this is the first study using multiple sensory cues in a push-pull configuration to modulate fish outmigration. Push and pull of juvenile sea lamprey with sensory cues could be useful to reduce turbine entrainment where native and enhance trap catch where invasive.
ABSTRACT
Semiochemicals that elicit species-specific attraction or repulsion have proven useful in the management of terrestrial pests and hold considerable promise for control of nuisance aquatic species, particularly invasive fishes. Because aquatic ecosystems are typically large and open, use of a semiochemical to control a spatially dispersed invader will require the development of a cost-effective emitter that is easy to produce, environmentally benign, inexpensive, and controls the release of the semiochemical without altering its structure. We examined the release properties of five polymers, and chose polyethylene glycol (PEG) as the best alternative. In a series of laboratory and field experiments, we examined the response of the invasive sea lamprey to PEG, and to a partial sex pheromone emitted from PEG that has proven effective as a trap bait to capture migrating sea lamprey prior to spawning. Our findings confirm that the sea lamprey does not behaviorally respond to PEG, and that the attractant response to the pheromone component was conserved when emitted from PEG. Further, we deployed the pheromone-PEG emitters as trap bait during typical control operations in three Great Lakes tributaries, observing similar improvements in trap performance when compared to a previous study using mechanically pumped liquid pheromone. Finally, the polymer emitters tended to dissolve unevenly in high flow conditions. We demonstrate that housing the emitter stabilizes the dissolution rate at high water velocity. We conclude the performance characteristics of PEG emitters to achieve controlled-release of a semiochemical are sufficient to recommend its use in conservation and management activities related to native and invasive aquatic organisms.
Subject(s)
Ecosystem , Fishes/physiology , Introduced Species , Petromyzon/physiology , Sex Attractants/metabolism , Animal Migration/physiology , Animals , Delayed-Action Preparations , LakesABSTRACT
The sea lamprey (Petromzons marinus) is an invasive ectoparasite of large-bodied fishes that adversely affects the fishing industry and ecology of the Laurentian Great Lakes. Lipid content in the whole sea lamprey and muscles, liver and kidney of metamorphosing larval stages has been reported. Similarly, the fatty acid profile of the rope tissues of sexually-mature male sea lampreys has also been reported. The average body weight of a sub-adult migratory sea lamprey is 250 g, which includes 14.4% skin (36 g). Our preliminary extraction data of an adult sea lamprey skin revealed that it contained approximately 8.5% of lipophilic compounds. Lamprey skin is home to a naturally aversive compound (an alarm cue) that is being developed into a repellent for use in pest management. As part of an ongoing investigation to identify the chemical structure of the sea lamprey alarm cue, we extracted the skin with water and methanol, respectively. The methanolic extract (1.55%) contained exclusively lipophilic compounds and did not include the alarm cue. We chemically characterized all compounds present in the methanolic extract as cholesterol esters (CE), tri- and di-glycerides (TG and DG), cholesterol, free fatty acids (FFA) and minor amounts of plasticizers. The free fatty acids fraction was composed of saturated (41.8%), monounsaturated (40.7%) and polyunsaturated (17.4%) fatty acids, respectively. The plasticizers characterized were phthalate and benzoate and found to be 0.95 mg and 2.54 mg, respectively, per adult sea lamprey skin. This is the first report of the chemical characterization of all the lipophilic constituents in the skin of sub-adult migratory sea lamprey. The CEs isolated and characterized from sea lamprey skin are also for the first time.