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Nicholas S. Johnson

Publications and source records attributed to Nicholas S. Johnson.

At least 109 records · Page 6Linked to original sources

Behavioral evidence for a role of chemoreception during reproduction in lake trout

Chemoreception is hypothesized to influence spawning site selection, mate search, and synchronization of gamete release in chars ( Salvelinus spp.), but behavioral evidence is generally lacking. Here, we provide a survey of the behavioral responses of reproductive male and female lake trout ( Salvelinus namaycush ) to natural conspecific chemosensory stimuli. A flow-through laboratory assay with side-by-side artificial spawning reefs was used to evaluate behavioral preferences of spawning-phase males and females for chemosensory stimuli from juveniles and from spawning-phase males and females. Males and females preferred male and juvenile stimuli over no stimuli, but only had weak preferences for female stimuli. Only females had a preference for male over juvenile stimuli when given a direct choice between the two. The unexpected observation of male attraction to male stimuli, even when offered female stimuli, indicates a fundamental difference from the existing models of chemical communication in fishes. We discuss our results from the perspectives of prespawning aggregation, mate evaluation, and spawning synchronization. Identification of specific components of the stimuli will allow confirmation of the function and may have management implications for native and invasive populations of lake trout that are ecologically and economically important.

Canadian Journal of Fisheries and Aquatic Sciences

Reproductive ecology of lampreys

Lampreys typically spawn in riffle habitats during the spring. Spawning activity and diel (i.e., during daylight and at night) behavioral patterns are initiated when spring water temperatures increase to levels that coincide with optimal embryologic development. Nests are constructed in gravel substrate using the oral disc to move stones and the tail to fan sediment out of the nest. Spawning habitat used by individual species is generally a function of adult size, where small-bodied species construct nests in shallower water with slower flow and smaller gravel than large-bodied species. The mating system of lampreys is primarily polygynandrous (i.e., where multiple males mate with multiple females). Lamprey species with adult total length less than 30 cm generally spawn communally, where a nest may contain 20 or more individuals of both sexes. Lamprey species with adult sizes greater than 35 cm generally spawn in groups of two to four. Operational sex ratios of lampreys are highly variable across species, populations, and time, but are generally male biased. The act of spawning typically starts with the male attaching with his oral disc to the back of the female’s head; the male and female then entwine and simultaneously release gametes. However, alternative mating behaviors (e.g., release of gametes without paired courtship and sneaker males) have been observed. Future research should determine how multiple modalities of communication among lampreys (including mating pheromones) are integrated to inform species recognition and mate choice. Such research could inform both sea lamprey control strategies and provide insight into possible evolution of reproductive isolation mechanisms between paired lamprey species in sympatry.

Book chapter

Investigations of novel unsaturated bile salts of male sea lamprey as potential chemical cues

Sulfated bile salts function as chemical cues that coordinate reproduction in sea lamprey, Petromyzon marinus . 7α, 12α, 24-trihydroxy-5α-cholan-3-one 24-sulfate (3kPZS) is the most abundant known bile salt released by sexually mature male sea lampreys and attracts ovulated females. However, previous studies showed that the male-produced pheromone consists of unidentified components in addition to 3kPZS. Here, analysis of water conditioned with mature male sea lampreys indicated the presence of 4 oxidized, unsaturated compounds with molecular weights of 466 Da, 468 Da, and 2 of 470 Da. These compounds were not detectable in water conditioned with immature male sea lampreys. By using mass spectrometry, 4 A-ring unsaturated sulfated bile salts were tentatively identified from male washings as 2 4-ene, a 1-ene, and a 1,4-diene analogs. These were synthesized to determine if they attracted ovulated female sea lampreys to spawning nests in natural streams. One of the novel synthetic bile salts, 3 keto-1-ene PZS, attracted ovulated females to the point of application at a concentration of 10 -12 M. This study reveals the structural diversity of bile salts in sea lamprey, some of which have been demonstrated to be pheromonal cues.

Journal of Chemical Ecology

Bile salts as semiochemicals in fish

Bile salts are potent olfactory stimuli in fishes; however the biological functions driving such sensitivity remain poorly understood. We provide an integrative review of bile salts as semiochemicals in fish. First, we present characteristics of bile salt structure, metabolism, and function that are particularly relevant to chemical communication. Bile salts display a systematic pattern of structural variation across taxa, are efficiently synthesized, and are stable in the environment. Bile salts are released into the water via the intestine, urinary tract, or gills, and are highly water soluble. Second, we consider the potential role of bile salts as semiochemicals in the contexts of detecting nearby fish, foraging, assessing risk, migrating, and spawning. Lastly, we suggest future studies on bile salts as semiochemicals further characterize release into the environment, behavioral responses by receivers, and directly test the biological contexts underlying olfactory sensitivity.

Chemical Senses

A new clarification method to visualize biliary degeneration during liver metamorphosis in sea lamprey ( Petromyzon marinus )

Biliary atresia is a rare disease of infancy, with an estimated 1 in 15,000 frequency in the southeast United States, but more common in East Asian countries, with a reported frequency of 1 in 5,000 in Taiwan. Although much is known about the management of biliary atresia, its pathogenesis is still elusive. The sea lamprey ( Petromyzon marinus ) provides a unique opportunity to examine the mechanism and progression of biliary degeneration. Sea lamprey develop through three distinct life stages: larval, parasitic, and adult. During the transition from larvae to parasitic juvenile, sea lamprey undergo metamorphosis with dramatic reorganization and remodeling in external morphology and internal organs. In the liver, the entire biliary system is lost, including the gall bladder and the biliary tree. A newly-developed method called “CLARITY” was modified to clarify the entire liver and the junction with the intestine in metamorphic sea lamprey. The process of biliary degeneration was visualized and discerned during sea lamprey metamorphosis by using laser scanning confocal microscopy. This method provides a powerful tool to study biliary atresia in a unique animal model.

Journal of Visualized Experiments

The behavioural response of adult Petromyzon marinus to damage-released alarm and predator cues

Using semi‐natural enclosures, this study investigated (1) whether adult sea lamprey Petromyzon marinus show avoidance of damage‐released conspecific cues, damage‐released heterospecific cues and predator cues and (2) whether this is a general response to injured heterospecific fishes or a specific response to injured P. marinus . Ten replicate groups of 10 adult P. marinus , separated by sex, were exposed to one of the following nine stimuli: deionized water (control), extracts prepared from adult P. marinus , decayed adult P. marinus (conspecific stimuli), sympatric white sucker Catostomus commersonii , Amazon sailfin catfish Pterygoplichthys pardalis (heterospecific stimuli), 2‐phenylethylamine (PEA HCl) solution, northern water snake Nerodia sipedon washing, human saliva (predator cues) and an adult P. marinus extract and human saliva combination (a damage‐released conspecific cue and a predator cue). Adult P. marinus showed a significant avoidance response to the adult P. marinus extract as well as to C. commersonii , human saliva, PEA and the adult P. marinus extract and human saliva combination. For mobile P. marinus , the N. sipedon washing induced behaviour consistent with predator inspection. Exposure to the P. pardalis extract did not induce a significant avoidance response during the stimulus release period. Mobile adult female P. marinus showed a stronger avoidance behaviour than mobile adult male P. marinus in response to the adult P. marinus extract and the adult P. marinus extract and human saliva combination. The findings support the continued investigation of natural damage‐released alarm cue and predator‐based repellents for the behavioural manipulation of P. marinus populations in the Laurentian Great Lakes.

Journal of Fish Biology

Growth and survival of sea lampreys from metamorphosis to spawning in Lake Huron

Larval Sea Lampreys Petromyzon marinus live burrowed in stream bottoms and then metamorphose into their parasitic stage. Among larvae that metamorphose in a given year (i.e., parasitic cohort), autumn out-migrants (October–December) to the Laurentian Great Lakes can feed on fish for up to 6 months longer than spring outmigrants (March–May), which overwinter in streams without feeding. We evaluated whether the season of outmigration affected growth or survival of newlymetamorphosed Sea Lampreys in LakeHuron. Newlymetamorphosed individuals (n=2,718) from three parasitic cohorts were netted during their out-migration from BlackMallard Creek, Michigan, to LakeHuron during autumn 1997 through spring 2000; each out-migrant was injected with a sequentially numbered coded wire tag and was released back into the creek. After up to 18 months of feeding in the Great Lakes, 224 (8.2%) Sea Lampreys were recaptured (in 1999–2001) as upstream-migrating adults in tributaries to Lakes Huron and Michigan. Recovery rates of autumn and spring out-migrants as adults were 9.4% and 7.8%, respectively, and these rates did not significantly differ. Overwinter feeding (i.e., as parasites) by autumn out-migrants did not produce adult mean sizes greater than those of spring out-migrants. Because we detected no growth or survival differences between autumn and spring out-migrants, the capture of newly metamorphosed Sea Lampreys at any point during their out-migration should provide equal reductions in damage to Great Lakes fisheries. The absence of a difference in growth or survival between autumn and spring out-migrants is an aspect of Sea Lamprey life history that yields resiliency to this invasive parasite and complicates efforts for its control in the Great Lakes.

Lake Huron

Anatomy of the lamprey ear: morphological evidence for occurrence of horizontal semicircular ducts in the labyrinth of Petromyzon marinus

In jawed (gnathostome) vertebrates, the inner ears have three semicircular canals arranged orthogonally in the three Cartesian planes: one horizontal (lateral) and two vertical canals. They function as detectors for angular acceleration in their respective planes. Living jawless craniates, cyclostomes (hagfish and lamprey) and their fossil records seemingly lack a lateral horizontal canal. The jawless vertebrate hagfish inner ear is described as a torus or doughnut, having one vertical canal, and the jawless vertebrate lamprey having two. These observations on the anatomy of the cyclostome (jawless vertebrate) inner ear have been unchallenged for over a century, and the question of how these jawless vertebrates perceive angular acceleration in the yaw (horizontal) planes has remained open. To provide an answer to this open question we reevaluated the anatomy of the inner ear in the lamprey, using stereoscopic dissection and scanning electron microscopy. The present study reveals a novel observation: the lamprey has two horizontal semicircular ducts in each labyrinth. Furthermore, the horizontal ducts in the lamprey, in contrast to those of jawed vertebrates, are located on the medial surface in the labyrinth rather than on the lateral surface. Our data on the lamprey horizontal duct suggest that the appearance of the horizontal canal characteristic of gnathostomes (lateral) and lampreys (medial) are mutually exclusive and indicate a parallel evolution of both systems, one in cyclostomes and one in gnathostome ancestors.

Journal of Anatomy

Blocking and guiding adult sea lamprey with pulsed direct current from vertical electrodes

Controlling the invasion front of aquatic nuisance species is of high importance to resource managers. We tested the hypothesis that adult sea lamprey ( Petromyzon marinus ), a destructive invasive species in the Laurentian Great Lakes, would exhibit behavioral avoidance to dual-frequency pulsed direct current generated by vertical electrodes and that the electric field would not injure or kill sea lamprey or non-target fish. Laboratory and in-stream experiments demonstrated that the electric field blocked sea lamprey migration and directed sea lamprey into traps. Rainbow trout ( Oncorhynchus mykiss ) and white sucker ( Catostomus commersoni ), species that migrate sympatrically with sea lamprey, avoided the electric field and had minimal injuries when subjected to it. Vertical electrodes are advantageous for fish guidance because (1) the electric field produced varies minimally with depth, (2) the electric field is not grounded, reducing power consumption to where portable and remote deployments powered by solar, wind, hydro, or a small generator are feasible, and (3) vertical electrodes can be quickly deployed without significant stream modification allowing rapid responses to new invasions. Similar dual-frequency pulsed direct current fields produced from vertical electrodes may be advantageous for blocking or trapping other invasive fish or for guiding valued fish around dams.

Michigan

Survival and metamorphosis of low-density populations of larval sea lampreys (Petromyzon marinus) in streams following lampricide treatment

Sea lamprey Petromyzon marinus control in the Great Lakes primarily involves application of lampricides to streams where larval production occurs to kill larvae prior to their metamorphosing and entering the lakes as parasites (juveniles). Because lampricides are not 100% effective, larvae that survive treatment maymetamorphose before streams are again treated. Larvae that survive treatment have not beenwidely studied, so their dynamics are notwell understood.Wetagged and released larvae in six Great Lake tributaries following lampricide treatment and estimated vital demographic rates using multistate tag-recovery models. Model-averaged larval survivals ranged from 56.8 to 57.6%. Model-averaged adult recovery rates, which were the product of juvenile survivals and adult capture probabilities, ranged from 6.8 to 9.3%. Using stochastic simulations, we estimated production of juvenile sea lampreys from a hypothetical population of treatment survivors under different growth conditions based on parameter estimates from this research. For fast-growing populations, juvenile production peaked 2 years after treatment. For slow-growing populations, juvenile production was approximately one-third that of fast-growing populations,with production not peaking until 4 years after treatment. Our results suggest that dynamics (i.e., survival, metamorphosis) of residual larval populations are very similar to those of untreated larval populations. Consequently, residual populations do not necessarily warrant special consideration for the purpose of sea lamprey control and can be ranked for treatment along with other populations. Consecutive lampricide treatments, which are under evaluation by the sea lamprey control program, would bemost effective for reducing juvenile production in large, fast-growing populations.

Michigan, Ontario, Wisconsin

Mercury accumulation in sea lamprey ( Petromyzon marinus ) from Lake Huron

We determined whole-fish total mercury (Hg) concentrations of 40 male and 40 female adult sea lampreys ( Petromyzon marinus ) captured in the Cheboygan River, a tributary to Lake Huron, during May 2011. In addition, bioenergetics modeling was used to explore the effects of sex-related differences in activity and resting (standard) metabolic rate (SMR) on mercury accumulation. The grand mean for Hg concentrations was 519 ng/g (standard error of the mean = 46 ng/g). On average, males were 16% higher in Hg concentration than females. Bioenergetics modeling results indicated that 14% higher activity and SMR in males would account for this observed sex difference in Hg concentrations. We concluded that the higher Hg concentration in males was most likely due to higher rate of energy expenditure in males, stemming from greater activity and SMR. Our findings have implications for estimating the effects of sea lamprey populations on mercury cycling within ecosystems, as well as for the proposed opening of sea lamprey fisheries. Eventually, our results may prove useful in improving control of sea lamprey, a pest responsible for substantial damage to fisheries in lakes where it is not native.

Michigan

Estimating reach-specific fish movement probabilities in rivers with a Bayesian state-space model: application to sea lamprey passage and capture at dams

Improved methods are needed to evaluate barriers and traps for control and assessment of invasive sea lamprey ( Petromyzon marinus ) in the Great Lakes. A Bayesian state-space model provided reach-specific probabilities of movement, including trap capture and dam passage, for 148 acoustic tagged invasive sea lamprey in the lower Cheboygan River, Michigan, a tributary to Lake Huron. Reach-specific movement probabilities were combined to obtain estimates of spatial distribution and abundance needed to evaluate a barrier and trap complex for sea lamprey control and assessment. Of an estimated 21 828 – 29 300 adult sea lampreys in the river, 0%–2%, or 0–514 untagged lampreys, could have passed upstream of the dam, and 46%–61% were caught in the trap. Although no tagged lampreys passed above the dam (0/148), our sample size was not sufficient to consider the lock and dam a complete barrier to sea lamprey. Results also showed that existing traps are in good locations because 83%–96% of the population was vulnerable to existing traps. However, only 52%–69% of lampreys vulnerable to traps were caught, suggesting that traps can be improved. The approach used in this study was a novel use of Bayesian state-space models that may have broader applications, including evaluation of barriers for other invasive species (e.g., Asian carp ( Hypophthalmichthys spp.)) and fish passage structures for other diadromous fishes.

Canadian Journal of Fisheries and Aquatic Sciences

Daytime avoidance of chemosensory alarm cues by adult sea lamprey ( Petromyzon marinus )

Sea lamprey ( Petromyzon marinus ) avoid damage-released and predator chemosensory cues at night, but their response to these cues during the day is unknown. Here, we explored (i) whether sea lamprey avoid these cues during the day and (ii) the effect of water temperature on the avoidance of chemosensory alarm cues in two diurnal laboratory experiments. We hypothesized that daytime activity would be temperature-dependent and that only sea lamprey vulnerable to predation (i.e., not hiding) would behaviourally respond to chemosensory alarm cues. Ten groups of ten sea lamprey were exposed to one of a variety of potential chemosensory cues. The experiments were conducted over a range of temperatures to quantify the effect of temperature on avoidance behaviour. Consistent with our hypothesis, a higher proportion of animals were active during daytime as water temperature increased. Moving sea lamprey showed an avoidance response to 2-phenylethylamine (a compound found in mammalian urine) and human saliva once water temperatures had risen to mean (±SD) = 13.7 (±1.4) °C. Resting and hiding sea lamprey did not show an avoidance response to any of the experimental stimuli.

Canadian Journal of Fisheries and Aquatic Sciences

Evidence for a receiver bias underlying female preference for a male mating pheromone in sea lamprey

Receiver bias models suggest that a male sexual signal became exaggerated to match a pre-existing sensory, perceptual or cognitive disposition of the female. Accordingly, these models predict that females of related taxa possessing the ancestral state of signalling evolved preference for the male trait in a non-sexual context. We postulated that female preference for the male-released bile alcohol mating pheromone, 3 keto petromyzonol sulfate (3kPZS), of the sea lamprey (Petromyzon marinus) evolved as a result of a receiver bias. In particular, we propose that migratory silver lamprey (Ichthyomyzon unicuspis), a basal member of the Petromyzontidae, evolved a preference for 3kPZS released by stream-resident larvae as a means of identifying productive habitat for offspring. Larval silver lamprey released 3kPZS at rates sufficient to be detected by migratory lampreys. Females responded to 3kPZS by exhibiting upstream movement behaviours relevant in a migratory context, but did not exhibit proximate behaviours important to mate search and spawning. Male silver lamprey did not release 3kPZS at rates sufficient to be detected by females in natural high-volume stream environments. We infer that female silver lamprey cue onto 3kPZS excreted by stream-resident larvae as a mechanism to locate habitat conducive to offspring survival and that males do not signal with 3kPZS. We suggest that this female preference for a male signal in a non-sexual context represents a bias leading to the sexual signalling observed in sea lamprey.

Michigan

Odor-conditioned rheotaxis of the sea lamprey: Modeling, analysis and validation

Mechanisms for orienting toward and locating an odor source are sought in both biology and engineering. Chemical ecology studies have demonstrated that adult female sea lamprey show rheotaxis in response to a male pheromone with dichotomous outcomes: sexually mature females locate the source of the pheromone whereas immature females swim by the source and continue moving upstream. Here we introduce a simple switching mechanism modeled after odor-conditioned rheotaxis for the sea lamprey as they search for the source of a pheromone in a one-dimensional riverine environment. In this strategy, the females move upstream only if they detect that the pheromone concentration is higher than a threshold value and drifts down (by turning off control action to save energy) otherwise. In addition, we propose various uncertainty models such as measurement noise, actuator disturbance, and a probabilistic model of a concentration field in turbulent flow. Based on the proposed model with uncertainties, a convergence analysis showed that with this simplistic switching mechanism, the lamprey converges to the source location on average in spite of all such uncertainties. Furthermore, a slightly modified model and its extensive simulation results explain the behaviors of immature female lamprey near the source location.

Bioinspiration and Biomimetics

Guiding out-migrating juvenile sea lamprey (Petromyzon marinus) with pulsed direct current

Non‐physical stimuli can deter or guide fish without affecting water flow or navigation and therefore have been investigated to improve fish passage at anthropogenic barriers and to control movement of invasive fish. Upstream fish migration can be blocked or guided without physical structure by electrifying the water, but directional downstream fish guidance with electricity has received little attention. We tested two non‐uniform pulsed direct current electric systems, each having different electrode orientations (vertical versus horizontal), to determine their ability to guide out‐migrating juvenile sea lamprey ( Petromyzon marinus ) and rainbow trout ( Oncorhynchus mykiss ). Both systems guided significantly more juvenile sea lamprey to a specific location in our experimental raceway when activated than when deactivated, but guidance efficiency decreased at the highest water velocities tested. At the electric field setting that effectively guided sea lamprey, rainbow trout were guided by the vertical electrode system, but most were blocked by the horizontal electrode system. Additional research should characterize the response of other species to non‐uniform fields of pulsed DC and develop electrode configurations that guide fish over a range of water velocity. Published 2013. This article is a U.S. Government work and is in the public domain in the USA.

River Research and Applications

PCB concentrations and activity of sea lamprey Petromyzon marinus vary by sex

We determined the polychlorinated biphenyl (PCB) concentrations of 40 male and 40 female adult sea lampreys Petromyzon marinus captured in the Cheboygan River, a tributary to Lake Huron, during May 2011. In addition, we performed a laboratory experiment using passive integrated transponder tags to determine whether male adult sea lampreys were more active than female adult sea lampreys. Sex had a significant effect on PCB concentration, and PCB concentration at a given level of sea lamprey condition was approximately 25 % greater in males than in females. Adjusting for the difference in condition between the sexes, males averaged a 17 % greater PCB concentration compared with females. Results from the laboratory experiment indicated that males were significantly more active than females. The observed sex difference in PCB concentrations was not due to female sea lampreys releasing eggs at spawning because the sea lamprey is semelparous, and we caught the sea lampreys before spawning. Rather, we attributed the sex difference in PCB concentrations to a greater rate of energy expenditure in males compared with females. We proposed that this greater rate of energy expenditure was likely due to greater activity. Our laboratory experiment results supported this hypothesis. A greater resting metabolic rate may also have contributed to a greater rate of energy expenditure. Our findings should eventually be applicable toward improving control of sea lamprey, a pest responsible for considerable damage to fisheries in lakes where it is not native.

Michigan