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INTRODUCTION: Adult sea lamprey (Petromyzon marinus) cease feeding and migrate to spawning streams where males build nests, undergo final sexual maturation, and subsequently produce and release large quantities of bile acid pheromones that attract mature females. These animals are predicted to rearrange their metabolic pathways drastically to support their reproductive strategies, presenting advantageous opportunities to examine how sex and the maturation processes affect metabolism. OBJECTIVES: The objective is to investigate the metabolic differences between sexes and maturation states in sea lamprey that support changes in physiological functions. METHODS: We compared plasma metabolomes of spawning and prespawning sea lamprey in both sexes using both non-targeted and targeted metabolomics approaches using UPLC/MS-MS with electrospray ionization in both positive and negative modes. The data were processed using Progenesis QI, Compound Discoverer and XCMS softwares for alignment, peak picking, and deconvolution of the peaks. Principle component analyses (PCA) and partial least squares discriminant analyses (PLS-DA) were performed using SIMCA and Metaboanalyst softwares to identify discriminating features, followed by fragmentation matching with extensive database search and pathway mapping. RESULTS: The pheromonal bile acid biosynthesis was upregulated significantly in males compared to females. Spermiating males further upregulated bile acid biosynthesis by altering amino acid metabolisms, upregulating cofactors and nucleotide metabolisms, but downregulating carbohydrate and energy metabolisms. CONCLUSION: Plasma metabolomes are sex- and maturation-dependent and reflect the special metabolic demands at each life stage and reproductive strategy.

Sea lamprey (Petromyzon marinus) is a unique vertebrate model to examine how liver metabolomes support different reproductive functions. Juvenile sea lamprey prey on other fish species by attaching to their body and feeding on their blood and body fluids. Once reaching adulthood, they cease feeding, migrate to spawning streams and begin their final sexual maturation. During these processes, the male livers produce large quantities of bile acid pheromone precursors to be modified and released via gills, whereas the female livers synthesize vast amounts of vitellogenin (yolk lipophosphoprotein) to be transported to the ovary.

Predator encounters during early life can elicit behavioral and physiological responses that have fitness consequences during subsequent prey life stages. In threatened lake sturgeon (Acipenser fulvescens) and other lithophilic-spawning fishes, newly hatched larvae (free embryos) are exposed to abundant predators including aquatic insect larvae that co-occupy stream substrates. We investigated stress effects on lake sturgeon larvae after encounters with common aquatic insect predators by quantifying mortality, body size, cortisol levels, and swimming behavior. Free embryos were exposed to either Perlidae (stonefly obligate predators) or Isonychiidae (mayfly filterers and facultative predators) or to no predators (controls). Free embryos that encountered perlids experienced high mortality, elevated cortisol levels, and exhibited cortisol reactivity when subsequently exposed to an acute stressor. Free embryos that encountered isonychiids exhibited elevated mortality, and elevated cortisol and cortisol reactivity relative to controls. Findings indicate that lake sturgeon free embryos are stressed by exposure to members of benthic stream communities during early life stages (predation of nearby conspecifics), and that metrics of stress exhibited threat sensitivity. Data are consistent with predictions that individuals modulate antipredator behavior in response to the intensity of perceived predation threat in the environment. We determined that behavioral outcomes associated with encounters with aquatic insects altered future behavioral trajectories, potentially as an adaptive response that can affect predation rates in subsequent life stages. Results contribute to a broader understanding of how interspecies interactions among co-occurring predator and prey communities may impact individual fitness and fish population recruitment.

Migratory fishes are renowned for their ability to home to natal streams for spawning. Learned olfactory cues play a critical role in natal homing of Pacific salmon and other fishes, but the underlying chemical signature of streams remains poorly understood after decades of study. The molecules that convey a stream-specific odour must differ among sites but remain constant over time. Among leading odorant candidates are amino acids; however, little research has assessed the spatial and temporal variability of amino acid profiles in streams. We report a comprehensive chemical study of dissolved amino acids as potential olfactory cues for homing by migratory fish. Specifically, we profiled amino acids in water from 23 streams in the upper Laurentian Great Lakes basin over 2 years. We investigated variation in amino acid profiles (1) among regions and rivers within a year, (2) between years and (3) among sites and across the seasons of migration and early life history within a stream. Liquid-chromatography tandem mass spectrometry revealed nanomolar concentrations for most of the 20 L-amino acids measured, above the levels detectable by studied migratory fishes. Moreover, amino acid profiles were temporally stable between 2 years and across an annual season from adult spawning migration through offspring early-life development within a stream. However, spatial differences in amino acid profiles were evident primarily over large geographic distances (among regions) but not among tributaries within regions or among sites within a stream. Collectively, our results indicate dissolved amino acids may be consistent components of rivers' odorant profiles but suggest additional molecules are likely important for natal homing of migratory fishes to specific spawning sites. We suggest that future studies consider the combined importance of amino acids and molecules from other chemical classes. Understanding the chemical basis of olfactory-guided natal homing is especially important as human activities could alter the odorant profiles of streams and thereby disrupt fish migrations and negatively impact population recruitment.

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.