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Nicholas S. Johnson

Publications and source records attributed to Nicholas S. Johnson.

At least 91 records · Page 5Linked to original sources

Habituation of adult sea lamprey repeatedly exposed to damage-released alarm and predator cues

Predation is an unforgiving selective pressure affecting the life history, morphology and behaviour of prey organisms. Selection should favour organisms that have the ability to correctly assess the information content of alarm cues. This study investigated whether adult sea lamprey Petromyzon marinus habituate to conspecific damage-released alarm cues (fresh and decayed sea lamprey extract), a heterospecific damage-released alarm cue (white sucker Catostomus commersonii extract), predator cues (Northern water snake Nerodia sipedon washing, human saliva and 2-phenylethylamine hydrochloride (PEA HCl)) and a conspecific damage-released alarm cue and predator cue combination (fresh sea lamprey extract and human saliva) after they were pre-exposed 4 times or 8 times, respectively, to a given stimulus the previous night. Consistent with our prediction, adult sea lamprey maintained an avoidance response to conspecific damage-released alarm cues (fresh and decayed sea lamprey extract), a predator cue presented at high relative concentration (PEA HCl) and a conspecific damage-released alarm cue and predator cue combination (fresh sea lamprey extract plus human saliva), irrespective of previous exposure level. As expected, adult sea lamprey habituated to a sympatric heterospecific damage-released alarm cue (white sucker extract) and a predator cue presented at lower relative concentration (human saliva). Adult sea lamprey did not show any avoidance of the Northern water snake washing and the Amazon sailfin catfish extract (heterospecific control). This study suggests that conspecific damage-released alarm cues and PEA HCl present the best options as natural repellents in an integrated management program aimed at controlling the abundance of sea lamprey in the Laurentian Great Lakes.

Environmental Biology of Fishes

Theory and application of semiochemicals in nuisance fish control

Controlling unwanted, or nuisance, fishes is becoming an increasingly urgent issue with few obvious solutions. Because fish rely heavily on semiochemicals, or chemical compounds that convey information between and within species, to mediate aspects of their life histories, these compounds are increasingly being considered as an option to help control wild fish. Possible uses of semiochemicals include measuring their presence in water to estimate population size, adding them to traps to count or remove specific species of fish, adding them to waterways to manipulate large-scale movement patterns, and saturating the environment with synthesized semiochemicals to disrupt responses to the natural cue. These applications may be especially appropriate for pheromones, chemical signals that pass between members of same species and which also have extreme specificity and potency. Alarm cues, compounds released by injured fish, and cues released by potential predators also could function as repellents and be especially useful if paired with pheromonal attractants in “push-pull” configurations. Approximately half a dozen attractive pheromones now have been partially identified in fish, and those for the sea lamprey and the common carp have been tested in the field with modest success. Alarm and predator cues for sea lamprey also have been tested in the laboratory and field with some success. Success has been hampered by our incomplete understanding of chemical identity, a lack of synthesized compounds, the fact that laboratory bioassays do not always reflect natural environments, and the relative difficulty of conducting trials on wild fishes because of short field seasons and regulatory requirements. Nevertheless, workers continue efforts to identify pheromones because of the great potential elucidated by insect control and the fact that few tools are available to control nuisance fish. Approaches developed for nuisance fish also could be applied to valued fishes, which suffer from a lack of powerful management tools.

Journal of Chemical Ecology

A portable trap with electric lead catches up to 75% of an invasive fish species

A novel system combining a trap and pulsed direct current electricity was able to catch up to 75% of tagged invasive sea lamprey Petromyzon marinus in free-flowing streams. Non-target mortality was rare and impacts to non-target migration were minimal; likely because pulsed direct current only needed to be activated at night (7 hours of each day). The system was completely portable and the annual cost of the trapping system was low ($4,800 U.S. dollars). Use of the technology is poised to substantially advance integrated control of sea lamprey, which threaten a fishery valued at 7 billion U.S. dollars annually, and help restore sea lamprey populations in Europe where they are native, but imperiled. The system may be broadly applicable to controlling invasive fishes and restoring valued fishes worldwide, thus having far reaching effects on ecosystems and societies.

Scientific Reports

Glass-eel-stage American Eels respond to conspecific odor as a function of concentration

The American Eel Anguilla rostrata has experienced staggering population declines in recent decades and is now the focus of restoration efforts. Studies have demonstrated that olfaction is critical to anguillid behavior and that glass eels (the life stage which migrates inland from saltwater to freshwater) are attracted to conspecific washings. We evaluated conspecific cueing as a potential mechanism for American Eel inland migration coordination by assessing (1) the affinity of glass eels to conspecific washings, (2) the concentration–response relationships, and (3) changes in responsiveness to washings during the glass eel-to-elver transition. In two-choice maze assays, glass eels were attracted to glass eel washings over a wide range of concentrations (0.20–0.40 g of glass eels·L −1 ·h −1 ), and a logarithmic function provided the best fit to the concentration–response relationship. When given a choice between two conspecific washings of higher and lower concentrations, the glass eels generally preferred the higher concentration. Responses to undiluted glass eel washings did not significantly differ among stage-3–7 glass eels, although stage-7 eels were not attracted to the washings, whereas the other stages were. Washing affinity remained similar over the course of several weeks. These results support aspects of the conspecific cueing hypothesis at the glass eel life stage under laboratory conditions, suggesting that conspecific cueing is an important component of migration coordination among juvenile American Eels and warrants additional study.

Transactions of the American Fisheries Society

Management strategy evaluation of pheromone-baited trapping techniques to improve management of invasive sea lamprey

We applied a management strategy evaluation (MSE) model to examine the potential cost-effectiveness of using pheromone-baited trapping along with conventional lampricide treatment to manage invasive sea lamprey. Four pheromone-baited trapping strategies were modeled: (1) stream activation wherein pheromone was applied to existing traps to achieve 10 −12 mol/L in-stream concentration, (2) stream activation plus two additional traps downstream with pheromone applied at 2.5 mg/hr (reverse-intercept approach), (3) trap activation wherein pheromone was applied at 10 mg/hr to existing traps, and (4) trap activation and reverse-intercept approach. Each new strategy was applied, with remaining funds applied to conventional lampricide control. Simulating deployment of these hybrid strategies on fourteen Lake Michigan streams resulted in increases of 17 and 11% (strategies 1 and 2) and decreases of 4 and 7% (strategies 3 and 4) of the lakewide mean abundance of adult sea lamprey relative to status quo. MSE revealed performance targets for trap efficacy to guide additional research because results indicate that combining lampricides and high efficacy trapping technologies can reduce sea lamprey abundance on average without increasing control costs.

Natural Resource Modeling

Evidence for partial overlap of male olfactory cues in lampreys

Animals rely on a mosaic of complex information to find and evaluate mates. Pheromones, often comprised of multiple components, are considered to be particularly important for species-recognition in many species. While the evolution of species-specific pheromone blends is well-described in many insects, very few vertebrate pheromones have been studied in a macro-evolutionary context. Here, we report a phylogenetic comparison of multi-component male odours that guide reproduction in lampreys. Chemical profiling of sexually mature males from eleven species of lamprey, representing six of ten genera and two of three families, indicated the chemical profiles of sexually mature male odours are partially shared among species. Behavioural assays conducted with four species sympatric in the Laurentian Great Lakes indicated asymmetric female responses to heterospecific odours, where Petromyzon marinus were attracted to male odour collected from all species tested but other species generally preferred only the odour of conspecifics. Electro-olfactogram recordings from P. marinus indicated that although P. marinus exhibited behavioural responses to odours from males of all species, at least some of the compounds that elicited olfactory responses were different in conspecific male odours compared to heterospecific male odours. We conclude that some of the compounds released by sexually mature males are shared among species and elicit olfactory and behavioural responses in P. marinus , and suggest that our results provide evidence for partial overlap of male olfactory cues among lampreys. Further characterization of the chemical identities of odour components is needed to confirm shared pheromones among species.

Journal of Experimental Biology

A semelparous fish continues upstream migration when exposed to alarm cue, but adjusts movement speed and timing

Animals make trade-offs between predation risk and pursuit of opportunities such as foraging and reproduction. Trade-offs between antipredator behaviours and foraging are well suited to manipulation in laboratory and field settings and have generated a vast compendium of knowledge. However, much less is known about how animals manage trade-offs between predation risk and pursuit of reproductive opportunities in the absence of the confounding effects of foraging. In the present study, we investigated how the nonfeeding migratory life stage of sea lamprey, Petromyzon marinus , responds to odour from dead conspecifics (a cue that induces avoidance behaviours in laboratory and field studies). We released groups of PIT-tagged sea lamprey 65 m from the shore of Lake Michigan or 287 m upstream in Carp Lake River and used antennas to detect their movements in the river. As the breeding season progressed, sea lamprey initiated upstream movement earlier and were more likely to enter the river. Sea lamprey that began the night in Lake Michigan entered Carp Lake River at higher rates and accelerated upstream when exposed to high concentrations of alarm cue, consistent with animals attempting to minimize time spent in risky areas. Sea lampreys that began the night in the river delayed upstream movement when exposed to alarm cue, consistent with animals sheltering and gathering information about a source of risk. We attribute this context-specific reaction to alarm cue to differences in perceived vulnerability to predation in sheltered positions in the river versus exposed positions in the lake. Once in the river, the vast majority of sea lamprey moved upstream independent of alarm cue or Julian date. Although life-history-induced time and energy budgets place rigid constraints on the direction of migration, sea lamprey attend to predation risk by modifying movement timing and speed.

Animal Behaviour

Five-year evaluation of habitat remediation in Thunder Bay, Lake Huron: Comparison of constructed reef characteristics that attract spawning lake trout

Degradation of aquatic habitats has motivated construction and research on the use of artificial reefs to enhance production of fish populations. However, reefs are often poorly planned, reef design characteristics are not evaluated, and reef assessments are short-term. We constructed 29 reefs in Thunder Bay, Lake Huron, in 2010 and 2011 to mitigate for degradation of a putative lake trout spawning reef. Reefs were designed to evaluate lake trout preferences for height, orientation, and size, and were compared with two degraded natural reefs and a high-quality natural reef (East Reef). Eggs and fry were sampled on each reef for five years post-construction, and movements of 40 tagged lake trout were tracked during three spawning seasons using acoustic telemetry. Numbers of adults and spawning on the constructed reefs were initially low, but increased significantly over the five years, while remaining consistent on East Reef. Adult density, egg deposition, and fry catch were not related to reef height or orientation of the constructed reefs, but were related to reef size and adjacency to East Reef. Adult lake trout visited and spawned on all except the smallest constructed reefs. Of the metrics used to evaluate the reefs, acoustic telemetry produced the most valuable and consistent data, including fine-scale examination of lake trout movements relative to individual reefs. Telemetry data, supplemented with diver observations, identified several previously unknown natural spawning sites, including the high-use portions of East Reef. Reef construction has increased the capacity for fry production in Thunder Bay without apparently decreasing the use of the natural reef. Results of this project emphasize the importance of multi-year reef assessment, use of multiple assessment methods, and comparison of reef characteristics when developing artificial reef projects. Specific guidelines for construction of reefs focused on enhancing lake trout spawning are suggested.

Lake Huron, Thunder Bay

Evidence that sea lampreys ( Petromyzon marinus ) complete their life cycle within a tributary of the Laurentian Great Lakes by parasitizing fishes in inland lakes

The sea lamprey ( Petromyzon marinus ) invaded the upper Laurentian Great Lakes and feeds on valued fish. The Cheboygan River, Michigan, USA, is a large sea lamprey producing tributary to Lake Huron and despite having a renovated dam 2 km from the river mouth that presumably blocks sea lamprey spawning migrations, the watershed upstream of the dam remains infested with larval sea lamprey. A navigational lock near the dam has been hypothesized as the means of escapement of adult sea lampreys from Lake Huron and source of the upper river population (H1). However, an alternative hypothesis (H2) is that some sea lampreys complete their life cycle upstream of the dam, without entering Lake Huron. To evaluate the alternative hypothesis, we gathered angler reports of lamprey wounds on game fishes upstream of the dam, and captured adult sea lampreys downstream and upstream of the dam to contrast abundance, run timing, size, and statolith microchemistry. Results indicate that a small population of adult sea lampreys (n < 200) completed their life cycle upstream of the dam during 2013 and 2014. This is the most comprehensive evidence that sea lampreys complete their life history within a tributary of the upper Great Lakes, and indicates that similar landlocked populations could occur in other watersheds. Because the adult sea lamprey population upstream of the dam is small, complete elimination of the already low adult escapement from Lake Huron might allow multiple control tactics such as lampricides, trapping, and sterile male release to eradicate the population.

Michigan

White sucker Catostomus commersonii respond to conspecific and sea lamprey Petromyzon marinus alarm cues but not potential predator cues

Recent studies proposed the use of chemosensory alarm cues to control the distribution of invasive sea lamprey Petromyzon marinus populations in the Laurentian Great Lakes and necessitate the evaluation of sea lamprey chemosensory alarm cues on valuable sympatric species such as white sucker. In two laboratory experiments, 10 replicate groups (10 animals each) of migratory white suckers were exposed to deionized water (control), conspecific whole-body extract, heterospecific whole-body extract (sea lamprey) and two potential predator cues (2-phenylethylamine HCl (PEA HCl) and human saliva) during the day, and exposed to the first four of the above cues at night. White suckers avoided the conspecific and the sea lamprey whole-body extract both during the day and at night to the same extent. Human saliva did not induce avoidance during the day. PEA HCl did not induce avoidance at a higher concentration during the day, or at night at the minimum concentration that was previously shown to induce maximum avoidance by sea lamprey under laboratory conditions. Our findings suggest that human saliva and PEA HCl may be potential species-specific predator cues for sea lamprey.

Journal of Great Lakes Research

Evaluating potential artefacts of photo-reversal on behavioral studies with nocturnal invasive sea lamprey ( Petromyzon marinus )

Sea lampreys ( Petromyzon marinus L., 1758) are nocturnal, so experiments evaluating their behaviour to chemosensory cues have typically been conducted at night. However, given the brief timeframe each year that adult P. marinus are available for experimentation, we investigated whether P. marinus exposed to a 12 h shifted diurnal cycle (reversed photoperiod) could be tested in a darkened arena during the day and show the same response to chemosensory cues as natural photoperiod P. marinus that were tested during the night. Ten replicates of 10 P. marinus , from each photoperiod, were exposed to deionized water (negative control), 2-phenylethylamine hydrochloride (PEA HCl, putative predator cue), or P. marinus whole-body extract (conspecific alarm cue). All P. marinus demonstrated a significant avoidance response to both cues. No significant differences were found in avoidance to PEA HCl between photoperiods. Avoidance of P. marinus whole-body extract was significantly stronger in natural compared with reversed photoperiod P. marinus . The use of reversed photoperiod subjects is suitable for examining the presence or absence of avoidance in response to novel chemosensory alarm cues, or the change in the magnitude of antipredator response. Studies investigating the natural magnitude of antipredator response should use natural photoperiod experimental subjects.

Canadian Journal of Zoology

Female sea lamprey shift orientation toward a conspecific chemical cue to escape a sensory trap

The sensory trap model of signal evolution hypothesizes that signalers adapt to exploit a cue used by the receiver in another context. Although exploitation of receiver biases can result in conflict between the sexes, deceptive signaling systems that are mutually beneficial drive the evolution of stable communication systems. However, female responses in the nonsexual and sexual contexts may become uncoupled if costs are associated with exhibiting a similar response to a trait in both contexts. Male sea lamprey ( Petromyzon marinus ) signal with a mating pheromone, 3-keto petromyzonol sulfate (3kPZS), which may be a match to a juvenile cue used by females during migration. Upstream movement of migratory lampreys is partially guided by 3kPZS, but females only move toward 3kPZS with proximal accuracy during spawning. Here, we use in-stream behavioral assays paired with gonad histology to document the transition of female preference for juvenile- and male-released 3kPZS that coincides with the functional shift of 3kPZS as a migratory cue to a mating pheromone. Females became increasingly biased toward the source of synthesized 3kPZS as their maturation progressed into the reproductive phase, at which point, a preference for juvenile odor (also containing 3kPZS naturally) ceased to exist. Uncoupling of female responses during migration and spawning makes the 3kPZS communication system a reliable means of synchronizing mate search. The present study offers a rare example of a transition in female responses to a chemical cue between nonsexual and sexual contexts, provides insights into the origins of stable communication signaling systems.

Behavioral Ecology

Behavioural response of adult sea lamprey (Petromyzon marinus) to predator and conspecific alarm cues: evidence of additive effects

Sea lampreys Petromyzon marinus, an invasive pest in the Upper Great Lakes, avoid odours that represent danger in their habitat. These odours include conspecific alarm cues and predator cues, like 2-phenylethylamine hydrochloride (PEA HCl), which is found in the urine of mammalian predators. Whether conspecific alarm cues and predator cues function additively or synergistically when mixed together is unknown. The objectives of this experimental study were to determine if the avoidance response of sea lamprey to PEA HCl is proportional to the concentration delivered, and if the avoidance response to the combination of a predator cue (PEA HCl) and sea lamprey alarm cue is additive. To accomplish the first objective, groups of ten sea lampreys were placed in an artificial stream channel and presented with stepwise concentrations of PEA HCl ranging from 5 &times; 10&minus;8 to 5 &times; 10&minus;10 M and a deionized water control. Sea lampreys exhibited an increase in their avoidance behaviour in response to increasing concentrations of PEA HCl. To accomplish the second objective, sea lampreys were exposed to PEA HCl, conspecific alarm cue and a combination of the two. Sea lampreys responded to the combination of predator cue and conspecific alarm cue in an additive manner.

St.Mary's River

Factors influencing capture of invasive sea lamprey in traps baited with a synthesized sex pheromone component

The sea lamprey, Petromyzon marinus , is emerging as a model organism for understanding how pheromones can be used for manipulating vertebrate behavior in an integrated pest management program. In a previous study, a synthetic sex pheromone component 7&alpha;,12&alpha;, 24-trihydroxy-5&alpha;-cholan-3-one 24-sulfate (3kPZS) was applied to sea lamprey traps in eight streams at a final in-stream concentration of 10 &minus;12 M. Application of 3kPZS increased sea lamprey catch, but where and when 3kPZS had the greatest impact was not determined. Here, by applying 3kPZS to additional streams, we determined that overall increases in yearly exploitation rate (proportion of sea lampreys that were marked, released, and subsequently recaptured) were highest (20&ndash;40 %) in wide streams (~40 m) with low adult sea lamprey abundance (<1000). Wide streams with low adult abundance may be representative of low-attraction systems for adult sea lamprey and, in the absence of other attractants (larval odor, sex pheromone), sea lamprey may have been more responsive to a partial sex pheromone blend emitted from traps. Furthermore, we found that the largest and most consistent responses to 3kPZS were during nights early in the trapping season, when water temperatures were increasing. This may have occurred because, during periods of increasing water temperatures, sea lamprey become more active and males at large may not have begun to release sex pheromone. In general, our results are consistent with those for pheromones of invertebrates, which are most effective when pest density is low and when pheromone competition is low.

Journal of Chemical Ecology

A sea lamprey ( Petromyzon marinus ) sex pheromone mixture increases trap catch relative to a single synthesized component in specific environments

Spermiating male sea lamprey ( Petromyzon marinus ) release a sex pheromone, of which a component, 7α, 12α, 24-trihydoxy-3-one-5α-cholan-24-sulfate (3kPZS), has been identified and shown to induce long distance preference responses in ovulated females. However, other pheromone components exist, and when 3kPZS alone was used to control invasive sea lamprey populations in the Laurentian Great Lakes, trap catch increase was significant, but gains were generally marginal. We hypothesized that free-ranging sea lamprey populations discriminate between a partial and complete pheromone while migrating to spawning grounds and searching for mates at spawning grounds. As a means to test our hypothesis, and to test two possible uses of sex pheromones for sea lamprey control, we asked whether the full sex pheromone mixture released by males (spermiating male washings; SMW) is more effective than 3kPZS in capturing animals in traditional traps (1) en route to spawning grounds and (2) at spawning grounds. At locations where traps target sea lampreys en route to spawning grounds, SMW-baited traps captured significantly more sea lampreys than paired 3kPZS-baited traps (~10 % increase). At spawning grounds, no difference in trap catch was observed between 3kPZS and SMW-baited traps. The lack of an observed difference at spawning grounds may be attributed to increased pheromone competition and possible involvement of other sensory modalities to locate mates. Because fishes often rely on multiple and sometimes redundant sensory modalities for critical life history events, the addition of sex pheromones to traditionally used traps is not likely to work in all circumstances. In the case of the sea lamprey, sex pheromone application may increase catch when applied to specifically designed traps deployed in streams with low adult density and limited spawning habitat.

Journal of Chemical Ecology

Quantification of 15 bile acids in lake charr feces by ultra-high performance liquid chromatography–tandem mass spectrometry

Many fishes are hypothesized to use bile acids (BAs) as chemical cues, yet quantification of BAs in biological samples and the required methods remain limited. Here, we present an UHPLC&ndash;MS/MS method for simultaneous, sensitive, and rapid quantification of 15 BAs, including free, taurine, and glycine conjugated BAs, and application of the method to fecal samples from lake charr ( Salvelinus namaycush ). The analytes were separated on a C 18 column with acetonitrile&ndash;water (containing 7.5 mM ammonium acetate and 0.1% formic acid) as mobile phase at a flow rate of 0.25 mL/min for 12 min. BAs were monitored with a negative electrospray triple quadrupole mass spectrometer (Xevo TQ-S&trade;). Calibration curves of 15 BAs were linear over the concentration range of 1.00&ndash;5,000 ng/mL. Validation revealed that the method was specific, accurate, and precise. The method was applied to quantitative analysis of feces extract of fry lake charr and the food they were eating. The concentrations of analytes CA, TCDCA, TCA, and CDCA were 242.3, 81.2, 60.7, and 36.2 ng/mg, respectively. However, other taurine conjugated BAs, TUDCA, TDCA, and THDCA, were not detected in feces of lake charr. Interestingly, TCA and TCDCA were detected at high concentrations in food pellets, at 71.9 and 38.2 ng/mg, respectively. Application of the method to feces samples from lake charr supported a role of BAs as chemical cues, and will enhance further investigation of BAs as chemical cues in other fish species.

Journal of Chromatography B: Analytical Technologi

A pheromone outweighs temperature in influencing migration of sea lamprey

Organisms continuously acquire and process information from surrounding cues. While some cues complement one another in delivering more reliable information, others may provide conflicting information. How organisms extract and use reliable information from a multitude of cues is largely unknown. We examined movement decisions of sea lampreys ( Petromyzon marinus L.) exposed to a conspecific and an environmental cue during pre-spawning migration. Specifically, we predicted that the mature male-released sex pheromone 3-keto petromyzonol sulfate (3kPZS) will outweigh the locomotor inhibiting effects of cold stream temperature (less than 15&deg;C). Using large-scale stream bioassays, we found that 3kPZS elicits an increase (more than 40%) in upstream movement of pre-spawning lampreys when the water temperatures were below 15&deg;C. Both warming temperatures and conspecific cues increase upstream movement when the water temperature rose above 15&deg;C. These patterns define an interaction between abiotic and conspecific cues in modulating animal decision-making, providing an example of the hierarchy of contradictory information.

Royal Society Open Science

Application of a putative alarm cue hastens the arrival of invasive sea lamprey ( Petromyzon marinus ) at a trapping location

The sea lamprey Petromyzon marinus is an invasive pest in the Laurentian Great Lakes basin, threatening the persistence of important commercial and recreational fisheries. There is substantial interest in developing effective trapping practices via the application of behavior-modifying semiochemicals (odors). Here we report on the effectiveness of utilizing repellent and attractant odors in a push–pull configuration, commonly employed to tackle invertebrate pests, to improve trapping efficacy at permanent barriers to sea lamprey migration. When a half-stream channel was activated by a naturally derived repellent odor (a putative alarm cue), we found that sea lamprey located a trap entrance significantly faster than when no odor was present as a result of their redistribution within the stream. The presence of a partial sex pheromone, acting as an attractant within the trap, was not found to further decrease the time to when sea lamprey located a trap entrance relative to when the alarm cue alone was applied. Neither the application of alarm cue singly nor alarm cue and partial sex pheromone in combination was found to improve the numbers of sea lamprey captured in the trap versus when no odor was present — likely because nominal capture rate during control trials was unusually high during the study period. Behavioural guidance using these odors has the potential to both improve control of invasive non-native sea lamprey in the Great Lakes as well as improving the efficiency of fish passage devices used in the restoration of threatened lamprey species elsewhere.

Michigan