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The release of sterilized insects to control pest populations has been used successfully during the past 6 decades, but application of the method in vertebrates has largely been overlooked or met with failure. Here, we demonstrate for the first time in fish, that a small population of sea lamprey (Petromyzon marinus; Class Agnatha), arguably one of the most impactful invasive fish in the world, can be controlled by the release of sterilized males. Specifically, the release of high numbers of sterile males (~ 1000's) into a geographically isolated population of adult sea lamprey resulted in the first multiyear delay in pesticide treatment since treatments began during 1966. Estimates of percent reduction in recruitment of age-1 sea lamprey due to sterile male release ranged from 7 to 99.9% with the precision of the estimate being low because of substantial year-to-year variability in larval density and distribution. Additional monitoring that accounts for recruitment variability in time and space would reduce uncertainty in the degree to which sterile male release reduces recruitment rates. The results are relevant to vertebrate pest control programs worldwide, especially as technical opportunities to sterilize vertebrates and manipulate sex ratios expand., (© 2024. United States Geological Survey.)

Olfactory-mediated behaviors in fish are often examined in artificial microcosms that enable well-controlled treatments but fail to replicate environmental and social contexts. However, observing these behaviors in nature poses challenges. Here, we describe a protocol for recording sea lamprey (Petromyzon marinus) behaviors in a natural system. We describe steps for administering and verifying accurate odorant concentrations, surveying sea lamprey abundance, and tracking sea lamprey movements. We also detail procedures to analyze treatment effects on pheromone-mediated spawning in a high-density population. For complete details on the use and execution of this protocol, please refer to Scott et al. 1 ., Competing Interests: Declaration of interests The authors declare no competing interests., (Copyright © 2024 The Author(s). Published by Elsevier Inc. All rights reserved.)

Sex pheromones impart maximal attraction when their components are present at optimal ratios that confer balanced olfactory inputs in potential mates. Altering ratios or adding pheromone analogs to optimal mixtures may disrupt balanced olfactory antagonism and result in reduced attraction, however, tests in natural populations are lacking. We tested this hypothesis in sea lamprey ( Petromyzon marinus ), a fish whose male sex pheromone attracts females when two critical components, 3-keto petromyzonol sulfate (3kPZS) and petromyzonol sulfate (PZS), are present at certain ratios. Here, we report a pheromone analog, petromyzonol tetrasulfate (3sPZS), reduced female attraction to 3kPZS but not to PZS. 3sPZS mixed with additional PZS synergistically disrupted female attraction to the male pheromone and reduced spawning by 97% in a high-density population. Our results provide evidence of balanced olfactory antagonism in a vertebrate and establish a tactic to disrupt spawning of sea lamprey, a destructive invader of the Laurentian Great Lakes., Competing Interests: The authors declare no competing interest., (© 2023.)

Natural resource governance is inherently complex owing to the socio-ecological systems in which it is embedded. Working arrangements have been fundamentally transformed throughout the COVID-19 pandemic with potential negative impacts on trust-based social networks foundational to resource management and transboundary governance. To inform development of a post-pandemic new-normal in resource management, we examined trust relationships using the Laurentian Great Lakes of North America as a case study. 82.9% (n = 97/117) of Great Lakes fishery managers and scientists surveyed indicated that virtual engagement was effective for maintaining well-established relationships during the pandemic; however, 76.7% (n = 89/116) of respondents indicated in-person engagement to be more effective than virtual engagement for building and maintaining trust. Despite some shortcomings, virtual or remote engagement presents opportunities, such as: (1) care and nurturing of well-established long-term relationships; (2) short-term (1-3 years) trust maintenance; (3) peer-peer or mentor-mentee coordination; (4) supplemental communications; (5) producer-push knowledge dissemination; and, if done thoughtfully, (6) enhancing diversity, equity, and inclusion. Without change, pre-pandemic trust-based relationships foundational to cooperative, multinational, resource management are under threat., Competing Interests: Declaration of competing interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper., (Copyright © 2022 The Authors. Published by Elsevier Ltd.. All rights reserved.)

Sea lamprey ( Petromyzon marinus ) control in the Laurentian Great Lakes of North America is an example of using physiological knowledge to successfully control an invasive species and rehabilitate an ecosystem and valuable fishery. The parasitic sea lamprey contributed to the devastating collapse of native fish communities after invading the Great Lakes during the 1800s and early 1900s. Economic tragedy ensued with the loss of the fishery and severe impacts to property values and tourism resulting from sea lamprey-induced ecological changes. To control the sea lamprey and rehabilitate the once vibrant Great Lakes ecosystem and economy, the Great Lakes Fishery Commission (Commission) was formed by treaty between Canada and the United States in 1955. The Commission has developed a sea lamprey control programme based on their physiological vulnerabilities, which includes (i) the application of selective pesticides (lampricides), which successfully kill sedentary sea lamprey larvae in their natal streams; (ii) barriers to spawning migrations and associated traps to prevent infestations of upstream habitats and remove adult sea lamprey before they reproduce; and (iii) the release of sterilized males to reduce the reproductive potential of spawning populations in select streams. Since 1958, the application of the sea lamprey control programme has suppressed sea lamprey populations by ~90% from peak abundance. Great Lakes fish populations have rebounded and the economy is now thriving. In hopes of further enhancing the efficacy and selectivity of the sea lamprey control programme, the Commission is exploring the use of (i) sea lamprey chemosensory cues (pheromones and alarm cues) to manipulate behaviours and physiologies, and (ii) genetics to identify and manipulate genes associated with key physiological functions, for control purposes. Overall, the Commission capitalizes on the unique physiology of the sea lamprey and strives to develop a diverse integrated programme to successfully control a once devastating invasive species.

Chemical cues and pheromones guide decisions in organisms throughout the animal kingdom. The neurobiology, function, and evolution of olfaction are particularly well described in insects, and resulting concepts have driven novel approaches to pest control. However, aside from several exceptions, the olfactory biology of vertebrates remains poorly understood. One exception is the sea lamprey (Petromyzon marinus), which relies heavily upon olfaction during reproduction. Here, we provide a broad review of the chemical cues and pheromones used by the sea lamprey during reproduction, including overviews of the sea lamprey olfactory system, chemical cues and pheromones, and potential applications to population management. The critical role of olfaction in mediating the sea lamprey life cycle is evident by a well-developed olfactory system. Sea lamprey use chemical cues and pheromones to identify productive spawning habitat, coordinate spawning behaviors, and avoid risk. Manipulation of olfactory biology offers opportunities for management of populations in the Laurentian Great Lakes, where the sea lamprey is a destructive invader. We suggest that the sea lamprey is a broadly useful organism with which to study vertebrate olfaction because of its simple but well-developed olfactory organ, the dominant role of olfaction in guiding behaviors during reproduction, and the direct implications for vertebrate pest management.

A sulphate-conjugated bile alcohol, 3,12-diketo-4,6-petromyzonene-24-sulfate (DKPES), was identified using bioassay-guided fractionation from water conditioned with sexually mature male sea lamprey (Petromyzon marinus). The structure and relative stereochemistry of DKPES was established using spectroscopic data. The electro-olfactogram (EOG) response threshold of DKPES was 10(-7) Molar (M) and that of 3-keto petromyzonol sulfate (3 KPZS; a known component of the male sea lamprey sex pheromone) was 10(-10) M. Behavioural studies indicated that DKPES can be detected at low concentrations by attracting sexually mature females to nests when combined with 3 KPZS. Nests baited with a mixture of DKPES and 3 KPZS (ratio 1∶29.8) attracted equal numbers of sexually mature females compared to an adjacent nest baited with 3 KPZS alone. When DKPES and 3 KPZS mixtures were applied at ratios of 2∶29.8 and 10∶29.8, the proportion of sexually mature females that entered baited nests increased to 73% and 70%, respectively. None of the sexually mature females released were attracted to nests baited with DKPES alone. These results indicated that DKPES is a component of the sex pheromone released by sexually mature male sea lamprey, and is the second biologically active compound identified from this pheromone. DKPES represents the first example that a minor component of a vertebrate pheromone can be combined with a major component to elicit critical sexual behaviors. DKPES holds considerable promise for increasing the effectiveness of pheromone-baited trapping as a means of sea lamprey control in the Laurentian Great Lakes.

Background: Vertebrate pheromones are known to prime the endocrine system, especially the hypothalamic-pituitary-gonadal (HPG) axis. However, no known pheromone molecule has been shown to modulate directly the synthesis or release of gonadotropin releasing hormone (GnRH), the main regulator of the HPG axis. We selected sea lamprey (Petromyzon marinus) as a model system to determine whether a single pheromone component alters the output of GnRH.Sea lamprey male sex pheromones contain a main component, 7α, 12α, 24-trihydroxy-5α-cholan-3-one 24-sulfate (3 keto-petromyzonol sulfate or 3kPZS), which has been shown to modulate behaviors of mature females. Through a series of experiments, we tested the hypothesis that 3kPZS modulates both synthesis and release of GnRH, and subsequently, HPG output in immature sea lamprey., Results: The results showed that natural male pheromone mixtures induced differential steroid responses but facilitated sexual maturation in both sexes of immature animals (χ(2) = 5.042, dF = 1, p < 0.05). Exposure to 3kPZS increased plasma 15α-hydroxyprogesterone (15α-P) concentrations (one-way ANOVA, p < 0.05) and brain gene expressions (genes examined: three lamprey (l) GnRH-I transcripts, lGnRH-III, Jun and Jun N-terminal kinase (JNK); one-way ANOVA, p < 0.05), but did not alter the number of GnRH neurons in the hypothalamus in immature animals. In addition, 3kPZS treatments increased lGnRH peptide concentrations in the forebrain and modulated their levels in plasma. Overall, 3kPZS modulation of HPG axis is more pronounced in immature males than in females., Conclusions: We conclude that a single male pheromone component primes the HPG axis in immature sea lamprey in a sexually dimorphic manner.

During the period when they are producing sperm, male sea lampreys (Petromyzon marinus L.) release a sex pheromone 7alpha, 12alpha, 24-trihydroxy-5alpha-cholan-3-one-24-sulfate (3 keto-petromyzonol sulfate, 3ketoPZS) that induces search and preference behaviors in ovulating females. In this study, we conducted a series of experiments to demonstrate that release of this pheromone into water takes place exclusively through the gills. In a behavioral maze, water conditioned with the anterior region of spermiating males induced an increase of search and preference behaviors in ovulating females. Similar behavior was not elicited by water conditioned by the posterior region. The anterior region washings and whole-body washings from spermiating males also elicited large and virtually identical electro-olfactogram responses from female sea lampreys, while the posterior washings produced negligible responses. Further, mass spectrometry and immunoassay confirmed that virtually all the 3ketoPZS released into water was through the gills. Immunocytochemistry revealed some gill epithelial cells and hepatocytes from spermiating males contained dense immunoreactive 3ketoPZS, but not those from prespermiating males. These results demonstrate that 3ketoPZS is released through the gill epithelia and suggest that this pheromone or its precursor may be produced in the liver.

We show that reproductively mature male sea lampreys release a bile acid that acts as a potent sex pheromone, inducing preference and searching behavior in ovulated female lampreys. The secreted bile acid 7alpha,12alpha,24-trihydroxy-5alpha-cholan-3-one 24-sulfate was released in much higher amounts relative to known vertebrate steroid pheromones and may be secreted through the gills. Hence, the male of this fish species signals both its reproductive status and location to females by secreting a pheromone that can act over long distances.