An evaluation of statistical methods for estimating abundances of migrating adult sea lamprey

We evaluated statistical methods for estimating abundances of adult sea lamprey (Petromyzon marinus) migrating in Great Lakes tributaries. The sea lamprey is the target of a basin-wide, bi-national control program. Abundance estimates from mark-recapture data are used to evaluate program success and the efficiency of sea lamprey trapping. Recent tracking studies suggested the mark-recapture estimates of abundance could be biased. We compared four estimators of abundance using stratified (weekly) mark-recapture data for 19?years of trapping in the St. Marys River. Abundances from the pooled Petersen estimator were similar to abundances from the stratified Schaefer and stratified Petersen estimators, but substantially lower than abundances from a stratified Bayesian P-spline estimator. In simulations of virtual populations, pooled Petersen and Bayesian P-spline estimates were similar across a range of conditions where catchability differed between marked and unmarked lamprey and changed over the trapping season, with one exception. Abundances from the Bayesian P-spline estimator were strongly positively biased when catchability of marked lamprey increased over the season, while catchability of unmarked lamprey did not. Estimates from both estimators were negatively biased when lamprey displayed consistent individual differences in catchability and positively biased when a proportion of marked lamprey fell back. Discrepancies between mark-recapture and tracking studies cannot be reconciled by the choice of abundance estimator, but could be an outcome of bias due to individual differences in catchability. Sea lamprey managers could also switch from the stratified Schaefer to the pooled Petersen estimator to simplify field operations without losing accuracy and precision.     

Use of chemosensory cues as repellents for sea lamprey: Potential directions for population management

Sea lamprey invaded the Great Lakes in the early 20th century and caused an abrupt decline in the population densities of several native fish species. The integrated management of this invasive species is composed of chemical (lampricide) applications, low-head barrier dams, adult trapping and sterile male release. Recently, there has been an increased emphasis on the development of control methods alternative to lampricide applications. We propose as an alternative-control method the use of chemosensory cues as repellents for sea lamprey population management. Based on the available evidence at this time, we suggest that injury-released chemical alarm cues show promise as repellents for sea lamprey and further research should be directed at determining whether sea lamprey show an avoidance response to these types of chemosensory cues. From a management perspective, these chemosensory cues could be used to restrict sea lamprey access to spawning grounds. Repellents could also be used together with attractants like sex pheromones to manipulate sea lamprey behavior, similar to the “push–pull” strategies utilized with insect pests.     

Consistent individual differences in sea lamprey (Petromyzon marinus) behaviour: Implications for control via trapping

We tested if consistent individual differences (CIDs) in the behaviour of sea lamprey (Petromyzon marinus) from the Laurentian Great Lakes could influence their vulnerability to trapping. The sea lamprey is invasive in the Upper Laurentian Great Lakes and the target of a binational control program. Trapping could be used for control if trapping efficiency is unbiased and effective. Our test involved comparing the behaviour of sea lamprey collected in the field from a trap (n = 42) at a barrier and electrofished (n = 9) downstream of the barrier. We quantified each individual's latency to exit an enclosure (a measure of exploration), proportion of time spent moving (a measure of general activity), and change in activity in response to a putative predator cue (a measure of boldness). CIDs were detected for each behaviour measured (intraclass correlations: 0.3–0.5). CIDs in behaviour also differed between trapped individuals and those collected downstream using electrofishing, irrespective of size, sex, and maturity status. Trapped individuals decreased their activity in response to a putative predator cue, while individuals collected using electrofishing increased their activity in response to the cue. Trapped individuals also tended to spend a greater proportion of time moving than individuals sampled downstream of the trap. However, the two samples of lamprey did not differ significantly in time taken to exit an enclosure. The behavioural differences between sea lamprey sampled from a trap and those sampled downstream of the trap suggest that CIDs in behaviour can influence an individual's vulnerability to trapping.     

Implications of tagging effects for interpreting the performance of sea lamprey traps in a large river

Abundance estimates can be crucial for managing species of economic concern. The accuracy of these estimates can depend on the methods used to track animals and to estimate abundance from tracking data. We tested experimentally if disparate estimates of trapping efficiency calculated for sea lamprey (Petromyzon marinus) in the St. Marys River near Sault Ste. Marie, Canada could be explained by effects related to the invasiveness and handling involved in tagging or the tag size used in the marking procedures. Trapping is used to gauge adult abundance, trapping efficiency, and success of a binational sea lamprey control program in the Laurentian Great Lakes, North America. Our experiment compared nightly catches of sea lamprey marked with external fin clips, surgically-implanted passive integrated transponder tags (PIT-only), and surgically-implanted PIT and acoustic tags (PIT+acoustic). We found no evidence that the probability of being trapped was affected by the added invasiveness and handling of internal tagging. Nightly recaptures of PIT-only tagged sea lamprey, relative to fin-clipped sea lamprey, were not different from expectations based on the numbers of individuals released from each treatment group. Conversely, there was evidence of effects related to tag size. Nightly recaptures of PIT+acoustic tagged sea lamprey, relative to PIT-only tagged sea lamprey, were lower than expected based on numbers of individuals released from each treatment group. Effects related to tag size partially explain the disparate estimates in trapping efficiency observed for sea lamprey.     

A life cycle approach to modeling sea lamprey population dynamics in the Lake Champlain basin to evaluate alternative control strategies

Sea lamprey (Petromyzon marinus) is a nuisance species in the Laurentian Great Lakes and Lake Champlain that has devastated native fish populations and hampered sport fisheries development. We developed a modified stage-based life history matrix for sea lamprey to analyze the effects of various management efforts to suppress sea lamprey population growth in Lake Champlain. These efforts targeted different life stages of the sea lamprey life cycle. A beta distribution was used to distribute stochastic larval populations among twenty sea lamprey-bearing tributaries and five deltas to Lake Champlain, from which sea lamprey that survive through larval metamorphosis were then pooled into a lake-wide parasitic-phase population. Parasitic-phase survival to the spawning stage was evaluated based on proximity to the natal tributary and on the size of the resident larval population in each tributary. Potential control strategies were modeled at egg to emergence, larval, and spawning stages to reduce vital rates at each stage, with the goal of suppressing parasitic-phase production. Simulations indicate that control of the larval stage was essential to achieving this goal, and with supplemental effort to reduce the vital rates at early life stages and at the spawning stage, the parasitic-phase population can be further suppressed. Sensitivity simulations indicate that the life history model was sensitive to egg deposition rate, abundance of parasitic-phase sea lamprey from unknown, uncontrolled sources, and the method in which parasitic-phase sea lamprey select tributaries for spawning. Results from this model can guide management agencies to optimize future management programs.     

100 years of sea lampreys above Niagara Falls: A reflection on what happened and what we learned

In the one hundred years since sea lampreys (Petromyzon marinus) were discovered in Lake Erie, the species completed its invasion throughout the Great Lakes basin, contributed to the downfall of the commercial fishing industry, and served as a catalyst for the development of the collaborative fishery management regime that exists today. The sea lamprey invasion simultaneously caused wide-spread devastation while giving rise to a collective realization that the health of the Great Lakes would require ongoing cooperation among governments, scientists, and users of the resource. Since its inception, the effort to control sea lampreys in the Great Lakes has been defined by a “shoot for the moon” mentality. The desperation of communities directly harmed by the sea lamprey invasion, coupled with the determination and unyielding commitment to science by those tasked with addressing the problem, led to the formation of the only reported successful aquatic vertebrate invasive species control program at an ecosystem scale.     

The behavioural response of migratory sea lamprey (Petromyzon marinus) to potential damage-released larval and migratory chemical alarm cues

We investigated the presence of damage-released alarm cues and the reactions they may cause in landlocked migratory sea lamprey (Petromyzon marinus) using semi-natural laboratory conditions during the day. In two separate experiments, migratory sea lampreys were exposed to stimuli prepared from the skinless carcasses and skin tissue of larval sea lamprey and from the skin tissue and muscle tissue of migratory sea lamprey. Migratory female sea lamprey swam significantly longer after being exposed to the stimulus prepared from the skinless carcass of larval sea lamprey. No significant changes were seen in the behaviour of the migratory female lamprey in response to larval skin extract or in the behaviour of male sea lamprey to any experimental extract in the larval extract experiment. In the second experiment that utilised migratory lamprey stimuli, neither male and nor female migratory sea lamprey showed a significant difference in their behavioural response among different treatments and controls. Our findings indicate that adult female sea lamprey respond strongly to damage-released alarm cues from larval sea lamprey; hence, the latter holds promise for sea lamprey behavioural manipulations for control purposes during the day. Further research is needed to examine responses to damage-released alarm cues at night, when migratory sea lampreys are more active.     

Evaluating the growth potential of sea lampreys (Petromyzon marinus) feeding on siscowet lake trout (Salvelinus namaycush) in Lake Superior

Differences in the preferred thermal habitat of Lake Superior lake trout morphotypes create alternative growth scenarios for parasitic sea lamprey (Petromyzon marinus) attached to lake trout hosts. Siscowet lake trout (Salvelinus namaycush) inhabit deep, consistently cold water (4-6 °C) and are more abundant than lean lake trout (Salvelinus namaycush) which occupy temperatures between 8 and 12 °C during summer thermal stratification. Using bioenergetics models we contrasted the growth potential of sea lampreys attached to siscowet and lean lake trout to determine how host temperature influences the growth and ultimate size of adult sea lamprey. Sea lampreys simulated under the thermal regime of siscowets are capable of reaching sizes within the range of adult sea lamprey sizes observed in Lake Superior tributaries. High lamprey wounding rates on siscowets suggest siscowets are important lamprey hosts. In addition, siscowets have higher survival rates from lamprey attacks than those observed for lean lake trout which raises the prospect that siscowets serve as a buffer to predation on more commercially desirable hosts such as lean lake trout, and could serve to subsidize lamprey growth.     

A Practical Method for Obtaining Useful Quantities of Pheromones from Sea Lamprey and Other Fishes for Identification and Control

Pheromonally-mediated trapping is currently being developed for use in sea lamprey control in the Laurentian Great Lakes. To identify and test lamprey pheromones a practical procedure was needed to isolate relatively large quantities of pheromone from lamprey holding water. The present study developed such a technique. It employs Amberlite XAD7HP, an adsorbent resin which we found can extract over 80% of the sea lamprey migratory pheromone from larval holding water at low cost and with relative ease. This technique allowed us to collect tens of milligrams of all three components of the sea lamprey migratory pheromone, eventually permitting both identification and successful field testing. This technique might also be used to collect pheromones released by other species of fish.     

Warmer waters increase the larval sea lamprey's (Petromyzon marinus) tolerance to the lampricide 3-trifluoromethyl-4-nitrophenol (TFM)

Invasive sea lampreys (Petromyzon marinus) in the Great Lakes are controlled by applying the pesticide (lampricide) 3-trifluoromethyl-4-nitrophenol (TFM) to waters infested with larval lamprey. However, treatment effectiveness can be undermined by “residual” larval sea lamprey that survive TFM exposure, and subsequently complete metamorphosis into parasitic juvenile sea lamprey that prey on culturally and economically important fishes. We investigated how season and temperature influenced the TFM tolerance of larval sea lamprey. Acute toxicity tests on lamprey collected from the Au Sable River, Michigan, revealed that the 12-h LC₅₀ and LC_99.9 were 2.0- to 2.5-fold greater in late spring and summer, than in early spring and fall. Subsequent toxicity tests indicated that greater TFM tolerance in summer was due to warmer temperatures, based on an almost 2-fold greater 12-h LC₅₀ and LC_99.9 in warm (24 °C) compared to cool (6 °C) water. Variations in energy stores (glycogen, lipid, protein) or condition did not appear to affect TFM sensitivity. We conclude that higher water temperature is the primary factor driving the larval sea lamprey's greater tolerance to TFM during the summer, possibly due to an increase in their capacity to detoxify TFM. Considering seasonal variations in temperature may be prudent when selecting and treating sea lamprey infested streams with TFM to minimize treatment residuals. In the longer term, increases in average and peak water temperatures due to climate change could result in greater TFM requirements and costs due to the greater tolerance of larval sea lamprey to TFM at warmer temperatures.     

The Sea Lamprey in Lake Erie: a Case History

Sea lampreys (Petromyzon marinus), first reported in Lake Erie in 1921, emigrated from Lake Ontario via the Welland Canal. It was not until the advent of pollution abatement, stream rehabilitation, and salmonid enhancement programs that sea lampreys proliferated. The Great Lakes Fishery Commission (GLFC), in co-operation with state, provincial, and federal fisheries agencies, implemented an integrated sea lamprey management (IMSL) plan for Lake Erie in 1986. Suppression of sea lampreys was nearly immediate, as indicated by declining larval-, parasitic-, and spawning-phase abundance, while survival of lake trout (Salvelinus namaycush) was markedly improved. Consistent with their vision statement, the GLFC began reducing lampricide use by the mid-1990s, while increasing reliance on alternative control methodologies. Reduction of treatment effort coincided with the development of new lampricide application techniques and treatment selection criteria, in addition to heightened regional concern for the impact of lampricide on non-target species. Subsequently, Lake Erie's sea lamprey numbers have rebounded, and marking rates on lake trout have approached pre-control levels. It is hypothesized that Lake Erie's rising abundance is primarily fuelled by untreated and residual larval populations, although some migration of parasitic-phase sea lampreys from Lake Huron is suspected. Model simulations infer that treatment effort on Lake Erie was sub-optimal from 1995 to 1998. Beginning in 1999, the GLFC enhanced measures to identify and control sources of sea lampreys. Based on historical abundance patterns and model results, it is anticipated that intensified management in Lake Erie will reduce sea lamprey numbers and provide an opportunity for lake trout restoration.     

Assessing Assessment: Can the Expected Effects of the St. Marys River Sea Lamprey Control Strategy Be Detected?

In 1997 the Great Lakes Fishery Commission approved a 5-year (1998 to 2002) control strategy to reduce sea lamprey (Petromyzon marinus) production in the St. Marys River, the primary source of parasitic sea lampreys in northern Lake Huron. An assessment plan was developed to measure the success of the control strategy and decide on subsequent control efforts. The expected effects of the St. Marys River control strategy are described, the assessments in place to measure these effects are outlined, and the ability of these assessments to detect the expected effects are quantified. Several expected changes were predicted to be detectable: abundance of parasitic-phase sea lampreys and annual mortality of lake trout (Salvelinus namaycush) by 2001, abundance of spawning-phase sea lampreys by 2002, and relative return rates of lake trout and sea lamprey wounding rates on lake trout by 2005. Designing an effective assessment program to quantify the consequences of fishery management actions is a critical, but often overlooked ingredient of sound fisheries management.     

Movement of Sea Lamprey in the Lake Champlain Basin

Sea lamprey (Petromyzon marinus) are a nuisance aquatic species in the Great Lakes and Lake Champlain that have devastated native fish populations and hampered the restoration of sport fisheries. This study examined inter-basin movement of sea lamprey in Lake Champlain to identify tributaries that contribute parasitic-phase sea lamprey and provide information for prioritizing those tributaries for sea lamprey control. A total of 4,125 recently metamorphosed sea lamprey was captured in tributaries to Lake Champlain and marked using coded wire tags between the fall of 2001 and winter 2003. These sea lamprey migrated to the lake to prey on salmonids and other fishes and returned to tributaries to spawn about 12–18 months after migration. We recaptured 6 tagged sea lamprey from the lake from spring 2002 through winter 2004, and 35 from tributaries in spring 2003 and 2004. We noted no apparent trends in movement among basins. Sea lamprey were collected at distances up to 64 km from their natal tributaries. Tributary contributions of parasites were significantly different from expectations in the 2002 parasitic-phase cohort (χ² = 9.668, p < 0.011, 3 df), suggesting differential survival rates among out-migrating transformers from different tributaries. Estimates of the lake-wide out-migrating transformer population for the 2002 and 2003 parasitic-phase cohorts were 269,139 ± 55,610 (SD) and 111,807 ± 23,511 (SD). Results from this study suggest that sea lamprey movement is not inhibited by causeways dividing sub-basins, but movement among sub-basins is somewhat constrained. This indicates that management efforts to control sea lamprey should continue to treat the lake as a single system.     

Variability in sea lamprey fatty acid profiles indicates a range of host species utilization in Lake Michigan

Despite being a “top predator”/parasite in the Great Lakes, knowledge of sea lamprey feeding ecology remains hindered by methodological constraints. Particularly, our knowledge of sea lamprey dietary habits is likely biased as it relies primarily on wounding rates of commercially and recreationally caught fish. Biochemical methods provide a means to extract diet information from sea lamprey themselves, and therefore provide a more objective assessment of sea lamprey feeding ecology. Of particular interest is the use of fatty acid profiles to qualitatively describe foraging patterns of sea lamprey. Adult sea lamprey were captured throughout the Lake Michigan basin during spring spawning migrations into rivers, and muscle tissues were analyzed for fatty acid profiles. Exploratory multivariate analyses were used to investigate variation in fatty acid profiles among captured individuals and to compare these to profiles of potential host species. In general, we noted a large variability in fatty acid profiles suggesting a broad spectrum of host species targeted by sea lamprey. Comparing sea lamprey fatty acid profiles with published data on host species, we concluded that sea lamprey feed on a wide variety of host species.     

Lateral and vertical distribution of downstream migrating juvenile sea lamprey

Sea lamprey is considered an invasive and nuisance species in the Laurentian Great Lakes, Lake Champlain, and the Finger Lakes of New York and is a major focus of control efforts. Currently, management practices focus on limiting the area of infestation using barriers to block migratory adults, and lampricides to kill ammocoetes in infested tributaries. No control efforts currently target the downstream-migrating post-metamorphic life stage which could provide another management opportunity. In order to apply control methods to this life stage, a better understanding of their downstream movement patterns is needed. To quantify spatial distribution of downstream migrants, we deployed fyke and drift nets laterally and vertically across the stream channel in two tributaries of Lake Champlain. Sea lamprey was not randomly distributed across the stream width and lateral distribution showed a significant association with discharge. Results indicated that juvenile sea lamprey is most likely to be present in the thalweg and at midwater depths of the stream channel. Further, a majority of the catch occurred during high flow events, suggesting an increase in downstream movement activity when water levels are higher than base flow. Discharge and flow are strong predictors of the distribution of out-migrating sea lamprey, thus managers will need to either target capture efforts in high discharge areas of streams or develop means to guide sea lamprey away from these areas.     

Development of a pH/Alkalinity Treatment Model for Applications of the Lampricide TFM to Streams Tributary to the Great Lakes

It has long been known that the toxicity of the lampricide 3-trifluoromethyl-4-nitrophenol (TFM) is influenced by chemical and physical properties of water. As the pH, conductivity, and alkalinity of water increase, greater concentrations of TFM are required to kill sea lamprey (Petromyzon marinus) larvae. Consequently, the concentration of TFM required for effective treatment varies among streams. Brown trout (Salmo trutta) and sea lamprey larvae were exposed to a series of TFM concentrations in a continuous-flow diluter for 12 h. Twenty five exposures were conducted at various water alkalinities and pHs that treatment personnel encounter during lampricide treatments. Survival/mortality data were analyzed for lampricide concentrations that produced 50 and 99.9% mortality (LC₅₀ and LC_99.9) for sea lamprey larvae and 25 and 50% mortality (LC₂₅ and LC₅₀) for brown trout. Linear regression analyses were performed for each set of tests for each selected alkalinity by comparing the 12-h post exposure LC_99.9 sea lamprey data and LC₂₅ brown trout data at each pH. Mortality data from on-site toxicity tests conducted by lampricide control personnel were compared to predicted values from the pH/alkalinity prediction model. Of the 31 tests examined, 27 resulted in the LC₁₀₀s (lowest TFM concentration where 100% mortality of sea lamprey was observed after 12 h of exposure) falling within 0.2 mg/L of the predicted sea lamprey minimum lethal (LC_99.9) range. The pH/alkalinity prediction model provides managers with an operational tool that reduces the amount of TFM required for effective treatment while minimizing the impact on non-target organisms.     

In situ assessment of lampricide toxicity to age-0 lake sturgeon

The lampricides 3-trifluoromethyl-4-nitrophenol (TFM) and 2′, 5-dichloro-4′-nitrosalicylanilide (niclosamide) are used to control sea lamprey (Petromyzon marinus), an invasive species in the Great Lakes. Age-0 lake sturgeon (Acipenser fulvescens), a species of conservation concern, share similar stream habitats with larval sea lampreys and these streams can be targeted for lampricide applications on a 3- to 5-year cycle. Previous laboratory research found that lake sturgeon smaller than 100 mm could be susceptible to lampricide treatments. We conducted stream-side toxicity (bioassay) and in situ studies in conjunction with 10 lampricide applications in nine Great Lakes tributaries to determine whether sea lamprey treatments could result in in situ age-0 lake sturgeon mortality, and developed a logistic model to help predict lake sturgeon survival during future treatments. In the bioassays the observed concentrations where no lake sturgeon mortality occurred (no observable effect concentration, NOEC) were at or greater than the observed sea lamprey minimum lethal concentration (MLC or LC99) in 7 of 10 tests. We found that the mean in situ survival of age-0 lake sturgeon during 10 lampricide applications was 80%, with a range of 45–100% survival within streams. Modeling indicated that in age-0 lake sturgeon survival was negatively correlated with absolute TFM concentration and stream alkalinity, and positively correlated with stream pH and temperature. Overall survival was higher than expected based on previous research, and we expect that these data will help managers with decisions on the trade-offs between sea lamprey control and the effect on stream-specific populations of age-0 lake sturgeon.     

Effectiveness of Using Backpack Electrofishing Gear for Collecting Sea Lamprey (Petromyzon marinus) Larvae in Great Lakes Tributaries

The effects of water depth, larval density, stream conductance, temperature, lamprey length, and larval escapement were examined to determine the efficiency of sampling sea lamprey (Petromyzon marinus) larvae using direct current (DC) backpack electrofishing gear. A higher proportion of larvae of all sizes were collected per unit sampling effort when sample sites were shallower, contained fewer larvae, or were in streams of lower specific conductance (P < 0.001). Temperature did not affect the efficiency of sampling lamprey larvae in this study. The investigation of the effect of larval escapement on observed catch was inconclusive. Similar length distributions were found between lamprey larvae collected using electrofishing gear and those collected using either a suction dredge or collected during a lampricide treatment. These results have implications for the development of a sampling protocol that uses a single-pass electrofishing technique to estimate the overall abundance of sea lamprey larvae in a stream. This estimate is critical to determining the number of larvae with the potential to metamorphose as parasitic lamprey the following year, and consequently, the prioritization of streams for lampricide treatment.     

Future Sea Lamprey Control Through Regulation of Metamorphosis and Reproduction: a Report from the SLIS II New Science and Control Workgroup

Use of the selective lampricide 3-trifluoromethyl-4-nitrophenol (TFM) and other alternative control methods (such as barriers which prevent sea lampreys, Petromyzon marinus, from reaching their spawning grounds) have succeeded in reducing sea lamprey abundance in the Great Lakes to a level that permits the survival of economically-valuable fish species. The New Science and Control workgroup at the second Sea Lamprey International Symposium (SLIS II) addressed how new knowledge of lamprey biology might contribute to additional alternatives to the use of lampricides, and where future research efforts should be directed. This paper focuses on the discussions of one of three subgroups of the New Science and Control workgroup into two aspects of the sea lamprey life cycle (metamorphosis and reproduction) that might be targets of future control methods. Methods were suggested that might disrupt the pre-metamorphic accumulation of lipid reserves or the successful commencement of feeding, and areas identified that might improve regulation of lamprey reproduction. Although all aspects of the reproductive endocrinology of lampreys should be studied, there should be particular focus on those factors that determine the sex ratio, mating systems, and reproductive success of sea lampreys and those that trigger the onset of sexual maturation.     

Modeling the Suppression of Sea Lamprey Populations by Use of the Male Sex Pheromone

The suppression of sea lamprey populations, Petromyzon marinus (Linnaeus), was modeled using four different applications of the male sex pheromone: (1) pheromone-baited traps that remove females from the spawning population, (2) pheromone-baited decoys that exhaust females before they are able to spawn, (3) pheromone-enhanced sterile males that increase the proportion of non-fertile matings, and (4) camouflaging of the pheromone emitted by calling males to make it difficult for females to find a mate. The models indicated that thousands of traps or hundreds of thousands of decoys would be required to suppress a population of 100,000 animals. The potential efficacy of pheromone camouflages is largely unknown, and additional research is required to estimate how much pheromone is needed to camouflage the pheromone plumes of calling males. Pheromone-enhanced sterile males appear to be a promising application in the Great Lakes. Using this technique for three generations each of ca. 7 years duration could reduce sea lamprey populations by 90% for Lakes Huron and Ontario and by 98% for Lake Michigan, based on current trapping operations that capture 20 to 30% of the population each year.