Geology topics

Weiming Li

Publications and source records attributed to Weiming Li.

At least 19 recordsLinked to original sources

USGS2026

DNA retention in sea lamprey digestive tracts: Insights from controlled feeding experiments

The sea lamprey ( Petromyzon marinus ), a non-native species in the Laurentian Great Lakes, has significantly impacted native fish communities and commercial fisheries, requiring population suppression efforts. While traditional control methods such as lampricides and barriers have reduced sea lamprey population abundance, questions remain regarding sea lamprey dietary composition given the focus of current damage assessments on economically and ecologically important host species. Recent advances in molecular technology offer promising methods of sea lamprey dietary assessment. Specifically, DNA metabarcoding enables species-specific identification of taxonomically diverse prey items from gut and fecal samples, and has proven effective in many taxa, including hematophagous species such as Arctic lamprey ( Lethenteron camtschaticum ) and sea lamprey. However, studies on DNA retention within digestive tracts are limited, particularly given the potential effects of environmental and dietary factors among hematophagous species. We used controlled feeding experiments to understand the effects these factors may have on DNA retention and host detectability within sea lamprey digestive tracts. Additionally, we evaluated the utility of metabarcoding for identifying multiple host species from consecutive feedings. Results indicate that host DNA can be detected up to 30 days post-feeding, with detection probability decreasing with increasing time following feeding. Temperature effects were dependent upon fasting periods, and host-switching trials indicated multiple previous host species could be detected from a single lamprey. Findings provide valuable insights for refining dietary analysis protocols for wild-caught sea lamprey within native and introduced ranges.

Environmental DNA↗

USGS2025

Ten lessons for controlling invasive species: Wisdom from the long-standing sea lamprey control program on the Laurentian Great Lakes

Sea lamprey ( Petromyzon marinus ) control in the Laurentian Great Lakes of North America is among the largest and most successful control programs of an invasive species anywhere on the planet. The effort began more than 75 years ago; it unites multiple nations, states, and provinces with the common goal of controlling this invasive species and protecting a valuable fishery. The science-based control program is administered by the Great Lakes Fishery Commission (GLFC), a body arising from a treaty signed by the United States and Canada. In the present article, we share 10 lessons learned from decades of successful sea lamprey control with the hopes of informing ongoing and future control programs targeting biological invasions. The 10 lessons we identified are to act boldly in times of crisis, to maintain the social license, to invest in capacity building, to break down the silos, to support fundamental science, to diversify your portfolio of control measures, to strive for continuous improvement, to confront the trade-off between information and action, to keep your foot on the gas, and to keep your eyes on the prize. The GLFC has long fostered a framework that uses some military strategy and verbiage that extends across the lessons (e.g., know your enemy). Other lessons are more nascent as the GLFC reenvisions its relationship with Indigenous peoples and governments in a path to reconciliation where two-eyed seeing is being embraced. Through adaptive management, horizon scanning methods, and embracing implementation science, the lessons learned about sea lamprey control will continue to evolve, which is itself a lesson. We submit that the lessons shared in the present article will help guide invasive species control programs spanning taxa, ecosystems, and regions.

Laurentian Great Lakes↗

USGS2025

Development of PCR blocking primers enabling DNA metabarcoding analysis of dietary composition in hematophagous sea lamprey

Conventional dietary assessments are challenging in hematophagous species, particularly in sea lamprey ( Petromyzon marinus ). However, recent technological developments and molecular approaches have provided an attractive alternative through the use of DNA metabarcoding. While DNA metabarcoding has been used for dietary analyses in numerous species, including lampreys, applications of universal primers that detect a diverse set of prey items can be limited by the amplification of predator DNA. In this study, we designed and tested eight blocking primers designed to suppress the amplification of sea lamprey DNA with vertebrate-universal primers targeting the mitochondrial 12S rRNA gene. This approach allowed for the use of a single marker to amplify a taxonomically diverse suite of host species, in contrast to previous studies that used multiple taxon-specific primer pairs (e.g., Salmonidae, Cyprinidae, and Catostomidae). Candidate blocking primers evaluated in this study differed in base pair length, end sequence modification, and purification method. Samples with different sea lamprey-to-host DNA ratios were subjected to multiple detection methods including gel electrophoresis, quantitative PCR, and DNA metabarcoding to assess the ability of each blocking primer to selectively suppress amplification of the sea lamprey 12S gene region. All blocking primers tested performed well and demonstrated high effectiveness, suppressing sea lamprey reads by > 99.9% in mock communities and improving host DNA sequence recovery across various sample types, including wild-caught lamprey. Results show that the blocking primers evaluated can facilitate molecular diet analysis in sea lamprey, allowing the amplification of a taxonomically diverse range of host fish species with universal primers.

Great Lakes↗

USGS2024

Male lake char release taurocholic acid as part of a mating pheromone

The evolutionary origins of sexual preferences for chemical signals remain poorly understood, due, in part, to scant information on the molecules involved. In the current study, we identified a male pheromone in lake char ( Salvelinus namaycush ) to evaluate the hypothesis that it exploits a non-sexual preference for juvenile odour. In anadromous char species, the odour of stream-resident juveniles guides migratory adults into spawning streams. Lake char are also attracted to juvenile odour but have lost the anadromous phenotype and spawn on nearshore reefs, where juvenile odour does not persist long enough to act as a cue for spawning site selection by adults. Previous behavioural data raised the possibility that males release a pheromone that includes components of juvenile odour. Using metabolomics, we found that the most abundant molecule released by males was also released by juveniles but not females. Tandem mass spectrometry and nuclear magnetic resonance were used to identify the molecule as taurocholic acid (TCA), which was previously implicated as a component of juvenile odour. Additional chemical analyses revealed that males release TCA at high rates via their urine during the spawning season. Finally, picomolar concentrations of TCA attracted pre-spawning and spawning females but not males. Taken together, our results indicate that male lake char release TCA as a mating pheromone and support the hypothesis that the pheromone is a partial match of juvenile odour.

Journal of Experimental Biology↗

USGS2024

Protocol for monitoring and analyzing pheromone-mediated behavioral response of sea lamprey in a natural system

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.

STAR Protocols↗

USGS2024

Evaluating behavioral responses of spawning-phase Walleyes to odors of rivers and other Walleyes

Many fish species show a remarkable ability to home to streams for spawning and fishery managers have applied that knowledge to restore or rehabilitate populations of some species. Walleye Sander vitreus show strong homing tendencies and the ability to select their natal river from other streams. The role of olfactory cues has been hypothesized but never tested in Walleye and many aspects of Walleye migratory behavior associated with spawning are poorly understood. The objectives of our study were: 1) to determine if spawning-phase Walleye from the Ford River in Michigan favored the odor of water from their home stream over that of a nearby river, and 2) to examine effects of male and female Walleye (conspecific) odors on water choice preferences of spawning-phase male Walleyes to learn whether such odors may attract adult Walleyes into rivers. Flow-through flume assays with two side-by-side channels were used to evaluate behavioral preferences of spawning-phase Walleye to river and conspecific odors. Odors of Ford River in 2021 trials and conspecific males in 2019 trials (when analyzed by individuals but not groups) influenced the behavior of male Walleye. However, follow up work during 2022 did not detect any responses to Ford River water or male-conditioned water. Additional work is needed to determine the possible role of olfactory cues in the homing behavior of spawning-phase Walleye.

Michigan↗

USGS2023

Synergistic behavioral antagonists of a sex pheromone reduce reproduction of invasive sea lamprey

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.

iScience↗

USGS2022

Comparative toxicity of aquatic per- and polyfluoroalkyl substance exposure in three species of amphibians

Per- and polyfluoroalkyl substances (PFAS) are contaminants of concern due to their widespread occurrence in the environment, persistence, and potential to elicit a range of negative health effects. Per- and polyfluoroalkyl substances are regularly detected in surface waters, but their effects on many aquatic organisms are still poorly understood. Species with thyroid-dependent development, like amphibians, can be especially susceptible to PFAS effects on thyroid hormone regulation. We examined sublethal effects of aquatic exposure to four commonly detected PFAS on larval northern leopard frogs ( Rana [Lithobates] pipiens ), American toads ( Anaxyrus americanus ), and eastern tiger salamanders ( Ambystoma tigrinum ). Animals were exposed for 30 days (frogs and salamanders) or until metamorphosis (toads) to 10, 100, or 1000 μg/L of perfluorooctane sulfonate (PFOS), perfluorooctanoic acid (PFOA), perfluorohexane sulfonate (PFHxS), or 6:2 fluorotelomer sulfonate (6:2 FTS). We determined that chronic exposure to common PFAS can negatively affect amphibian body condition and development at concentrations as low as 10 µg/L. These effects were highly species dependent, with species having prolonged larval development (frogs and salamanders) being more sensitive to PFAS than more rapidly developing species (toads). Our results demonstrate that some species could experience sublethal effects at sites with surface waters highly affected by PFAS. Our results also indicate that evaluating PFAS toxicity using a single species may not be sufficient for accurate amphibian risk assessment. Future studies are needed to determine whether these differences in susceptibility can be predicted from species' life histories and whether more commonly occurring environmental levels of PFAS could affect amphibians.

Environmental Toxicology and Chemistry↗

USGS2021

Diel patterns of pheromone release by male sea lamprey

Costs to producing sexual signals can create selective pressures on males to invest signaling effort in particular contexts. When the benefits of signaling vary consistently across time, males can optimize signal investment to specific temporal contexts using biological rhythms. Sea lamprey, Petromyzon marinus , have a semelparous life history, are primarily nocturnal, and rely on pheromone communication for reproduction; however, whether male investment in pheromone transport and release matches increases in spawning activity remains unknown. By measuring (1) 3keto-petromyzonol sulfate (3kPZS, a main pheromone component) and its biosynthetic precursor PZS in holding water and tissue samples at six points over the course of 24 hours and (2) 3kPZS release over the course of several days, we demonstrate that 3kPZS release exhibits a consistent diel pattern across several days with elevated pheromone release just prior to sunset and at night. Trends in hepatic concentrations and circulatory transport of PZS and 3kPZS were relatively consistent with patterns of 3kPZS release and suggest the possibility of direct upregulation in pheromone transport and release rather than observed release patterns being solely a byproduct of increased behavioral activity. Our results suggest males evolved a signaling strategy that synchronizes elevated pheromone release with nocturnal increases in sea lamprey behavior. This may be imperative to ensure that male signaling effort is not wasted in a species having a single, reproductive event.

Integrative and Comparative Biology↗

USGS2021

Progress towards integrating an understanding of chemical ecology into sea lamprey control

The sea lamprey, Petromyzon marinus , is a destructive invader in the Laurentian Great Lakes that relies on several complex chemical cues to complete their life cycle. The central roles of chemical cues in sea lamprey reproduction provide opportunities to leverage knowledge of sea lamprey chemical ecology when developing alternative or supplemental strategies for sea lamprey control. A solid foundation has been laid regarding sea lamprey chemical ecology, with recent advances in our understanding of the migratory pheromone, male sex pheromone, and alarm cues broadening our fundamental understanding of the diversity, complexity, and evolution of chemical cues used by sea lamprey. Additionally, research applying semiochemicals in differing management scenarios has provided useful insights into the challenges of incorporating chemical cues into the sea lamprey control program. Here, we synthesize new findings related to fundamental research of chemosensory cues along with knowledge learned from management-based tests and explore options for integrating an understanding of chemical ecology into sea lamprey control in light of new knowledge. We also highlight current unknowns and future research needs that should be addressed prior to implementation of sea lamprey chemical ecology into the sea lamprey control program.

Great Lakes↗

USGS2020

Pheromone pollution from invasive sea lamprey misguides a native confamilial

Animals living in the Anthropocene search for mates facing a barrage of pollutants. Few studies consider pheromones from invasive species as pollution, but their central role in the lives of many animals indicates cross-reaction among historically allopatric relatives has potentially damaging impacts. We hypothesized the sex pheromone of sea lamprey (Petromyzon marinus), an invasive fish in the Laurentian Great Lakes, misguides mate search in native chestnut lamprey (Ichthyomyzon castaneus). In a field test, 100 % of female I. castaneus chose male odourants from P. marinus over conspecifics. Chemical analysis of water in which males were held confirmed both species signal with 3-keto petromyzonol sulfate but revealed higher release rates in P. marinus. Our results indicate sex pheromones from invasive species can be an influential type of pollution and underscore the conservation implications of studies on pheromone evolution.

Current Zoology↗

USGS2020

Behavioural responses of female lake trout Salvelinus namaycush to male chemical stimuli and prostaglandin F2α

Male olfactory cues may guide aggregation on spawning reefs, mate evaluation, and synchronized gamete release in lake trout Salvelinus namaycush, but a lack of information on the source and identity of the cues precludes direct tests of their function. Using a two-channel flume assay, we found female lake trout increased time spent in the channel treated with male-conditioned water, urine, and bile but not synthesized prostaglandin F2α. We suggest future efforts to characterize male olfactory cues focus on urine and postulate that bile acids contribute to its behavioural activity.

Journal of Fish Biology↗

USGS2020

A pheromone antagonist liberates female sea lamprey from a sensory trap to enable reliable communication

The evolution of male signals and female preferences remains a central question in the study of animal communication. The sensory trap model suggests males evolve signals that mimic cues used in nonsexual contexts and thus manipulate female behavior to generate mating opportunities. Much evidence supports the sensory trap model, but how females glean reliable information from both mimetic signals and their model cues remains unknown. We discovered a mechanism whereby a manipulative male signal guides reliable communication in sea lamprey ( Petromyzon marinus ). Migratory sea lamprey follow a larval cue into spawning streams; once sexually mature, males release a pheromone that mimics the larval cue and attracts females. Females conceivably benefit from the mimetic pheromone during mate search but must discriminate against the model cue to avoid orienting toward larvae in nearby nursery habitats. We tested the hypothesis that spawning females respond to petromyzonol sulfate (PZS) as a behavioral antagonist to avoid attraction to the larval cue while tracking the male pheromone despite each containing attractive 3-keto petromyzonol sulfate (3kPZS). We found 1) PZS inhibited electrophysiological responses to 3kPZS and abated preferences for 3kPZS when mixed at the same or greater concentrations, 2) larvae released more PZS than 3kPZS whereas males released more 3kPZS than PZS, and 3) mixtures of 3kPZS and PZS applied at ratios measured in larval and male odorants resulted in the discrimination observed between the natural odors. Our study elucidates how communication systems that arise via deception can facilitate reliable communication.

Proceedings of the National Academy of Sciences of↗

USGS2020

American eels produce and release bile acids that vary across life stage

The American eel ( Anguilla rostrata ) is an imperilled fish hypothesized to use conspecific cues, in part, to coordinate long‐distance migration during their multistage life history. Here, holding water and tissue from multiple American eel life stages was collected and analysed for the presence, profile and concentration of bile acids. Distinct bile acid profiles were identified in glass, elver, yellow eel and silver eel holding waters using ultraperformance liquid chromatography high‐resolution mass spectrometry and principal component analysis. Taurochenodeoxycholic acid, taurodeoxycholic acid, cholic acid, deoxycholic acid, taurolithocholic acid and taurocholic acid were detected in whole tissue of American glass eels and elvers, and in liver, intestine and gallbladder samples of late‐stage yellow eels. Bile acids were not a major component of silver eel washings or tissue. This study is novel because little was previously known about bile acids produced and emitted into the environment by American eels. Future behavioural studies could evaluate whether any bile acids produced by American eels influence conspecific migratory behaviour.

Journal of Fish Biology↗

USGS2020

Behavioral responses of sea lamprey to varying application rates of a synthesized pheromone in diverse trapping scenarios

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.

Journal of Chemical Ecology↗

USGS2019

Intra- and interspecific variation in production of bile acids that act as sex pheromones in lampreys

Pheromones are important sexual signals in most animals, but research into their evolution is largely biased toward insects. Lampreys are a jawless fish with a relatively well-understood pheromone communication system and offer a useful opportunity to study pheromone evolution in a vertebrate. Once sexually mature, male sea lamprey (Petromyzon marinus), and likely other lampreys, produce and release bile acids that act as sex pheromones. Spawning males do not feed and therefore produce bile acids primarily for sexual communication whereas larvae produce the same bile acids but for digestion, offering an opportunity to compare the evolution of bile acids produced for sexual versus nonsexual functions. We profiled eight pheromone-related bile acids in livers from larvae and males and determined the effect of life stage on intra- and interspecific variation in bile acid production. Our results indicate less variation among males than larvae within P. marinus but more variation among species for males than larvae. We postulate that bile acid production in males is shaped by directional or stabilizing selection that reduces variance within P. marinus and directional or disruptive selection that promotes diversification across species. Although our results offer support for a role of sexual selection in the evolution of a lamprey pheromones, they do not eliminate possible roles of other aspects of lamprey ecology.

Physiological and Biochemical Zoology↗

USGS2018

Rapid evolution meets invasive species control: The potential for pesticide resistance in sea lamprey

Rapid evolution of pest, pathogen and wildlife populations can have undesirable effects; for example, when insects evolve resistance to pesticides or fishes evolve smaller body size in response to harvest. A destructive invasive species in the Laurentian Great Lakes, the sea lamprey (Petromyzon marinus) has been controlled with the pesticide 3-trifluoromethyl-4-nitrophenol (TFM) since the 1950s. We evaluated the likelihood of sea lamprey evolving resistance to TFM by (1) reviewing sea lamprey life history and control; (2) identifying physiological and behavioural resistance strategies; (3) estimating the strength of selection from TFM; (4) assessing the timeline for evolution; and (5) analyzing historical toxicity data for evidence of resistance. The number of sea lamprey generations exposed to TFM was within the range observed for fish populations where rapid evolution has occurred. Mortality from TFM was estimated as 82-90%, suggesting significant selective pressure. However, 57 years of toxicity data revealed no increase in lethal concentrations of TFM. Vigilance and the development of alternative controls are required to prevent this aquatic invasive species from evolving strategies to evade control.

Canadian Journal of Fisheries and Aquatic Sciences↗

USGS2017

Phylogenetic distribution of a male pheromone that may exploit a nonsexual preference in lampreys

Pheromones are among the most important sexual signals used by organisms throughout the animal kingdom. However, few are identified in vertebrates, leaving the evolutionary mechanisms underlying vertebrate pheromones poorly understood. Pre-existing biases in receivers’ perceptual systems shape visual and auditory signaling systems, but studies on how receiver biases influence the evolution of pheromone communication remain sparse. The lamprey Petromyzon marinus uses a relatively well-understood suite of pheromones and offers a unique opportunity to study the evolution of vertebrate pheromone communication. Previous studies indicate that male signaling with the mating pheromone 3-keto petromyzonol sulfate (3kPZS) may exploit a nonsexual attraction to juvenile-released 3kPZS that guides migration into productive rearing habitat. Here, we infer the distribution of male signaling with 3kPZS using a phylogenetic comparison comprising six of ten genera and two of three families. Our results indicate that only P. marinus and Ichthyomyzon castaneus release 3kPZS at high rates. Olfactory and behavioral assays with P. marinus, I. castaneus and a subset of three other species that do not use 3kPZS as a sexual signal indicate that male signaling might drive the evolution of female adaptations to detect 3kPZS with specific olfactory mechanisms and respond to 3kPZS with targeted attraction relevant during mate search. We postulate that 3kPZS communication evolved independently in I. castaneus and P. marinus , but cannot eliminate the alternative that other species lost 3kPZS communication. Regardless, our results represent a rare macroevolutionary investigation of a vertebrate pheromone and insight into the evolutionary mechanisms underlying pheromone communication.

Journal of Evolutionary Biology↗