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Nicholas S. Johnson

Publications and source records attributed to Nicholas S. Johnson.

At least 55 records · Page 3Linked to original sources

Behavioural response of sea lamprey (Petromyzon marinus) to acoustic stimuli in a small stream

Sea lamprey ( Petromyzon marinus ) are invasive in the Laurentian Great Lakes and parasitically feed on valued fishes. Migration barriers and selective pesticides are used to control sea lamprey, but there is a desire to develop additional control tools such as traps with nonphysical deterrents. Sound has been used as a deterrent for other invasive species, but its potential for manipulating sea lamprey behavior in natural stream conditions remains untested. Here, behavioral responses of upstream-migrating adult sea lamprey in response to low frequency sounds of 70 or 90 Hz was tracked in a small stream (8 m wide) using passive integrated transponder (PIT) telemetry. The low frequency sounds shifted sea lamprey distribution, with up to 30% more sea lamprey detected on PIT antennas without sound compared with PIT antennas with sound playing. Future studies could continue testing low frequency sounds in larger rivers with larger speakers for use as a natural deterrent at sea lamprey barriers to push sea lamprey toward traps.

Canadian Journal of Fisheries and Aquatic Sciences

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

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

Evaluation of visible light as a cue for guiding downstream migrant juvenile Sea Lamprey

Light can modify orientation and locomotory behaviors in fish and has been applied to attract or repel migrant fish by inducing positive or negative phototaxis. Here, recently metamorphosed downstream‐migrating Sea Lamprey Petromyzon marinus were exposed to light cues in several orientations and intensities at night under controlled flowing‐water conditions in a laboratory flume. Behaviors and rates of downstream movement were monitored with overhead cameras and nets. When exposed to low‐intensity white light, 16–23% more Sea Lamprey were captured in a net closest to the light cue array compared to a dark control condition, suggesting some degree of positive phototaxis at low light levels (100 lx at a distance of 1 m from the light source). An interaction with the side of the flume (possibly due to varying flow conditions) and light treatment was also observed. At higher light intensities (1,000 lx at 1 m from the source), Sea Lamprey progressed downstream at a lower rate than was observed during dark conditions. After high‐intensity light treatments, fewer Sea Lamprey were observed in the nets at the downstream end of the flume and more Sea Lamprey were observed in the flume or in the release channel compared to dark control trials. Therefore, some photonegative behavior may be expressed at light levels of 1,000 lx or greater, perhaps as an attempt to avoid detection by predators by remaining stationary or seeking shelter. Light may have utility as a cue used for guidance devices to control Sea Lamprey, but further research is needed to define how light intensity and the environment (turbidity, depth, water velocity, and natural habitat features) influence locomotion, changes in swimming depth, and other behavioral responses of downstream‐migrating juvenile Sea Lamprey.

Transactions of the American Fisheries Society

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

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

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

Push and pull of downstream moving juvenile sea lamprey (Petromyzon marinus) exposed to chemosensory and light cues

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.

Massachusetts

Is there convergence of gut microbes in blood-feeding vertebrates?

Animal microbiomes play an important role in dietary adaptation, yet the extent to which microbiome changes exhibit parallel evolution is unclear. Of particular interest is an adaptation to extreme diets, such as blood, which poses special challenges in its content of proteins and lack of essential nutrients. In this study, we assessed taxonomic signatures (by 16S rRNA amplicon profiling) and potential functional signatures (inferred by Phylogenetic Investigation of Communities by Reconstruction of Unobserved States (PICRUSt)) of haematophagy in birds and bats. Our goal was to test three alternative hypotheses: no convergence of microbiomes, convergence in taxonomy and convergence in function. We find a statistically significant effect of haematophagy in terms of microbial taxonomic convergence across the blood-feeding bats and birds, although this effect is small compared to the differences found between haematophagous and non-haematophagous species within the two host clades. We also find some evidence of convergence at the predicted functional level, although it is possible that the lack of metagenomic data and the poor representation of microbial lineages adapted to haematophagy in genome databases limit the power of this approach. The results provide a paradigm for exploring convergent microbiome evolution replicated with independent contrasts in different host lineages.

Philosophical Transactions of the Royal Society B:

Bloom forming cyanobacteria can adversely affect zebra and quagga mussel veligers

Quagga ( Dreissena rostriformis bugensis ) and zebra ( D. polymorpha ) mussels are broadcast spawners that produce planktonic, free swimming veligers, a life history strategy dissimilar to native North American freshwater bivalves. Dreissenid veligers require highly nutritious food to grow and survive, and thus may be susceptible to increased mortality rates during harsh environmental conditions like cyanobacteria blooms. However, the impact of cyanobacteria and one of the toxins they can produce (microcystin) has not been evaluated in dreissenid veligers. Therefore, we exposed dreissenid veligers to eleven distinct cultures (isolates) of cyanobacteria representing Anabaena, Aphanizomenon, Dolichospermum, Microcystis, and Planktothrix species and the cyanotoxin microcystin to determine the lethality of cyanobacteria on dreissenid veligers. Six-day laboratory bioassays were performed in microplates using dreissenid veligers collected from the Detroit River, Michigan, USA. Veligers were exposed to increasing concentrations of cyanobacteria and microcystin using the green algae Chlorella minutissima as a control. Based on dose response curves formulated from a Probit model, the LC 50 values for cyanobacteria used in this study range between 15.06 and 135.06 μg/L chlorophyll- a , with the LC 50 for microcystin-LR at 13.03 μg/L. Because LC 50 values were within ranges observed in natural waterbodies, it is possible that dreissenid recruitment may be suppressed when veliger abundances overlap with seasonal cyanobacteria blooms. Thus, the toxicity of cyanobacteria to dreissenid veligers may be useful to include in models forecasting dreissenid mussel abundance and spread.

Ecotoxicology and Environmental Safety

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

Cyanobacteria reduce motility of quagga mussel (Driessena rostriformis bugensis) sperm

The temporal expansion of harmful algal blooms, primarily associated with cyanobacteria, may impact aquatic organisms at vulnerable life history stages. Broadcast spawning species release gametes into the water column for external fertilization, directly exposing sperm to potential aquatic stressors. To determine if cyanobacteria can disrupt reproduction in freshwater broadcast spawners, we evaluated sub‐lethal effects of cyanobacteria exposure on quagga mussel ( Dreissena rostriformis bugensis ) sperm. In laboratory studies, sperm were collected after inducing mussels to spawn using serotonin and exposed to 11 cultures of cyanobacteria including Anabaena flos‐aquae , Aphanizomenon flos‐aquae , Dolichospermum lemmermanii , Gloeotrichia echinulata , five cultures of Microcystis aeruginosa, M. wesenbergii , and Planktothrix suspensa . Sperm motility, using endpoints of cumulative distance traveled and mean velocity was calculated for a minimum of 10 individual sperm using a novel optical biotracking assay method. The distance and velocity at which sperm travelled decreased when exposed to Aphanizomenon flos‐aquae and two M. aeruginosa cultures. Our findings indicate that cyanobacteria impede the motility of quagga mussel sperm, which can potentially result in reproductive impairments to mussels, and potentially other broadcast spawning species.

Environmental Toxicology and Chemistry

An underwater observation dataset for fish classification and fishery assessment

Using Dual-Frequency Identification Sonar (DIDSON), fishery acoustic observation data was collected from the Ocqueoc River, a tributary of Lake Huron in northern Michigan, USA. Data were collected March through July 2013 and 2016 and included the identification, via technology or expert analysis, of eight fish species as they passed through the DIDSON’s field of view. A set of short DIDSON clips containing identified fish was curated. Additionally, two other datasets were created that include visualizations of the acoustic data and longer DIDSON clips. These datasets could complement future research characterizing the abundance and behavior of valued fishes such as walleye ( Sander vitreus ) or white sucker ( Catostomus commersonii ) or invasive fishes such as sea lamprey ( Petromyzon marinus ) or European carp ( Cyprinus carpio ). Given the abundance of DIDSON data and the fact that a portion of it is labeled, these data could aid in the creation of machine learning tools from DIDSON data, particularly for invasive sea lamprey which are amply represented and a destructive invader of the Laurentian Great Lakes.

Scientific Data

Protection from UV light is an evolutionarily conserved feature of the haematopoietic niche

Haematopoietic stem and progenitor cells (HSPCs) require a specific microenvironment, the haematopoietic niche, which regulates HSPC behaviour . The location of this niche varies across species, but the evolutionary pressures that drive HSPCs to different microenvironments remain unknown. The niche is located in the bone marrow in adult mammals, whereas it is found in other locations in non-mammalian vertebrates, for example, in the kidney marrow in teleost fish. Here we show that a melanocyte umbrella above the kidney marrow protects HSPCs against ultraviolet light in zebrafish. Because mutants that lack melanocytes have normal steady-state haematopoiesis under standard laboratory conditions, we hypothesized that melanocytes above the stem cell niche protect HSPCs against ultraviolet-light-induced DNA damage. Indeed, after ultraviolet-light irradiation, unpigmented larvae show higher levels of DNA damage in HSPCs, as indicated by staining of cyclobutane pyrimidine dimers and have reduced numbers of HSPCs, as shown by cmyb (also known as myb ) expression. The umbrella of melanocytes associated with the haematopoietic niche is highly evolutionarily conserved in aquatic animals, including the sea lamprey, a basal vertebrate. During the transition from an aquatic to a terrestrial environment, HSPCs relocated into the bone marrow, which is protected from ultraviolet light by the cortical bone around the marrow. Our studies reveal that melanocytes above the haematopoietic niche protect HSPCs from ultraviolet-light-induced DNA damage in aquatic vertebrates and suggest that during the transition to terrestrial life, ultraviolet light was an evolutionary pressure affecting the location of the haematopoietic niche.

Nature

A simple, cost-effective emitter for controlled release of fish pheromones: development, testing, and application to management of the invasive sea lamprey

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.

PLoS ONE

Characterization of Sea Lamprey stream entry using dual‐frequency identification sonar

Effective methods to control invasive Sea Lampreys Petromyzon marinus in the Laurentian Great Lakes often rely on knowledge of the timing of the Sea Lamprey spawning migration, which has previously been characterized using data gathered from traps. Most assessment traps are located many kilometers upstream from the river mouth, so less is known about when Sea Lampreys enter spawning streams and which environmental cues trigger their transition from lakes to rivers. To decide how to develop barriers and traps that target Sea Lampreys when they enter a stream, the stream entry of Sea Lampreys into a Lake Huron tributary during 2 years was assessed using dual‐frequency identification sonar (DIDSON). Sea Lampreys entered the stream in low densities when temperatures first reached 4°C, which was up to 6 weeks and a mean of 4 weeks earlier than when they were first captured in traps located upstream. The probability of stream entry was significantly affected by stream temperature and discharge, and stream entry timing peaked when stream temperatures rose to 12°C and discharge was high. Examination of the entry at a finer temporal resolution (i.e., minutes) indicated that Sea Lampreys did not exhibit social behavior (e.g., shoaling) during stream entry. Our findings indicate that Sea Lampreys may be vulnerable to alternative trap types near river mouths and hydraulic challenges associated with traditional traps. Also, seasonal migration barriers near stream mouths may need to be installed soon after ice‐out to effectively block the entire adult Sea Lamprey cohort from upstream spawning habitat.

Michigan

Cyanobacteria reduce quagga mussel (Dreissena rostriformis bugensis) spawning and fertilization success

Quagga mussels ( Dreissena rostriformis bugensis ) are highly fecund broadcast spawners invasive to freshwaters of North America and western Europe. We hypothesized that environmental cues from phytoplankton can trigger gamete release in quagga mussels. Nutritious algae may stimulate dreissenid spawning, but less palatable food, such as bloom-forming cyanobacteria, could be a hindrance. The objective of our study was to test whether exposure to cyanobacteria can inhibit quagga mussel spawning and fertilization. We assessed spawning in the presence of serotonin, a known spawning inducer, where adult quagga mussels placed in individual vials were exposed to 13 cyanobacteria cultures and purified algal toxin (microcystin-LR) with artificial lake water as the control. Fertilization success was evaluated by combining eggs with sperm in conjunction with cyanobacteria, and enumerating zygote formation marked by cellular cleavage. Several cyanobacterial strains reduced spawning and fertilization success, but microcystin-LR had no effect. Fertilization was more sensitive to cyanobacteria than gamete release. Only 1 culture, Aphanizomenon flos-aquae , inhibited spawning, whereas 6 cultures consisting of Anabaena flos-aquae , Dolichospermum lemmermanii , Gloeotrichia echinulata , Lyngbya wollei , and 2 Microcystis aeruginosa isolates reduced fertilization rates by up to 44%. The effects of cyanobacteria on reproduction in invasive freshwater mussels in the wild have not yet been identified. However, our laboratory studies show that concentrations of cyanobacteria that are possible during bloom conditions probably limit reproduction. Reproductive consequences on wild populations may become more prevalent as cyanobacteria blooms occur earlier in the year, making overlap between blooms and mussel spawning more common. Describing the mechanism by which cyanobacteria inhibit spawning and fertilization could reveal novel control methods to limit reproduction of this invasive species.

Freshwater Science

A distributed pipeline for DIDSON data processing

Technological advances in the field of ecology allow data on ecological systems to be collected at high resolution, both temporally and spatially. Devices such as Dual-frequency Identification Sonar (DIDSON) can be deployed in aquatic environments for extended periods and easily generate several terabytes of underwater surveillance data which may need to be processed multiple times. Due to the large amount of data generated and need for flexibility in processing, a distributed pipeline was constructed for DIDSON data making use of the Hadoop ecosystem. The pipeline is capable of ingesting raw DIDSON data, transforming the acoustic data to images, filtering the images, detecting and extracting motion, and generating feature data for machine learning and classification. All of the tasks in the pipeline can be run in parallel and the framework allows for custom processing. Applications of the pipeline include monitoring migration times, determining the presence of a particular species, estimating population size and other fishery management tasks.

Conference Paper