Basin-scale Patterns in the Drift of Embryonic and Larval Fishes and Lamprey Ammocoetes in two Coastal Rivers

We studied the distribution and abundance of drifting embryonic and larval fishes and lampreys in the Smith and Van Duzen rivers of northern California, U.S.A. We collected seven fish species in four families and at least one lamprey species in the drift. All taxa drifted almost exclusively at night. Sculpins, Cottus aleuticus and C. asper, outnumbered all other taxa, comprising 63% of the catch in the Van Duzen River and 90% of the catch in the Smith River. We estimated that sculpin drift reached 3×10⁷ individualsh^–1 during the relatively high flow period from late winter through early summer. Most sculpin in these two rivers appeared to drift to the estuaries; we estimated 2.5×10⁹ sculpin embryos and larvae reached the Smith River estuary in 1995. In contrast to the sculpins, the patterns in the drift of other taxa suggest limited transport to the estuaries. Suckers, Catostomus occidentalis in the Van Duzen River, C. rimiculus in the Smith River, threespine stickleback, Gasterosteus aculeatus, and lamprey, Lampetra tridentata and possibly L. richardsoni, drifted at much lower rates and later in the year than sculpins. In the Van Duzen River, drift appeared to serve as a dispersal mechanism for only one of three introduced cyprinids. California roach, Lavinia symmetricus, drifted at low rates throughout the summer while we captured only seven Sacramento pikeminnow, Ptychocheilus grandis, and no speckled dace, Rhynichthys osculus. The information gathered on the drift of early life history phases is germane to both the conservation of native fishes and management of non-indigenous species in coastal rivers.     

Metamorphosis of the mountain brook lamprey Ichthyomyzon greeleyi

Synopsis Metamorphosis of the nonparasitic mountain brook lamprey, I. greeleyi, is described within 7 phases based on external morphological changes. The commencement of metamorphosis in early August is consistent with the pattern for northern hemisphere lampreys which display an inverse relationship with latitude. The sequence of external changes including the development of eyes, oral disc, teeth, tongue, oral fimbriae and lateral line its consistent among individuals of I. greeleyi and lampreys in general. Some of the changes realized during metamorphosis of I. greeleyi are important to the adult period while others reflect their presumed parasitic ancestry. Energy reserves by nonfeeding I. greeleyi during the 104–140 days required to complete metamorphosis are replaced by water so that total length and body weight do not change significantly during this time.     

Neuroendocrine and behavioral responses to weak electric fields in adult sea lampreys (Petromyzon marinus)

We characterized the behavioral and neuroendocrine responses of adult sea lampreys (Petromyzon marinus) to weak electric fields. Adult sea lampreys, captured during upstream spawning migration, exhibited limited active behaviors during exposure to weak electric fields and spent the most time attached to the wall of the testing arena near the cathode (−). For adult male sea lampreys, exposure to weak electric fields resulted in increased lamprey (l) GnRH-I mRNA expression but decreased lGnRH-I immunoreactivities in the forebrain, and decreased Jun (a neuronal activation marker) mRNA levels in the brain stem. Similar effects were not observed in the brains of female sea lampreys after weak electric field stimulation. The influence of electroreception on forebrain lGnRH suggests that electroreception may modulate the reproductive systems in adult male sea lampreys. The changes in Jun expression may be associated with swimming inhibition during weak electric field stimulation. The results for adult sea lampreys are the opposite of those obtained using parasitic-stage sea lampreys, which displayed increased activity during and after cathodal stimulation. Our results demonstrate that adult sea lampreys are sensitive to weak electric fields, which may play a role in reproduction. They also suggest that electrical stimuli mediate different behaviors in feeding-stage and spawning-stage sea lampreys.     

Incidence of lamprey marks on Lake Sturgeon (Acipenser fulvescens Rafinesque, 1817) in the St. Clair – Detroit River System: Implications for Sea Lamprey (Petromyzon marinus Linnaeus, 1758) effects

Laurentian Great Lakes Lake Sturgeon (Acipenser fulvescens) are hosts to lamprey species, including native Silver Lamprey (Ichthyomyzon unicuspis) and invasive Sea Lamprey (Petromyzon marinus). Silver Lamprey coevolved with Lake Sturgeon and cause negligible mortality, but Sea Lamprey can negatively affect Lake Sturgeon populations. Sea Lamprey abundance in Lake Erie has been above targets set by resource managers, with the St. Clair – Detroit River System (SCDRS) suspected as a source of Sea Lamprey production into Lake Erie. This study summarizes lamprey marking on Lake Sturgeon captured during agency assessment surveys in the SCDRS since 1996 and provides insight on the potential for Sea Lamprey to negatively affect Lake Sturgeon in the SCDRS. Lamprey marks (any lamprey species) were noted on 48.2% of Lake Sturgeon (2.5 marks/fish) and 3.3% of Lake Sturgeon assumed to be susceptible to mortality by Sea Lamprey (<760 mm TL; 0.06 marks/fish). Silver Lamprey were the only lamprey species found attached to Lake Sturgeon and there was no difference between oral disc diameters of Silver Lamprey and marks measured on Lake Sturgeon in Lake St. Clair and the lower St. Clair River (p = .45). Based on logistic regression, probability of at least one lamprey mark increased with Lake Sturgeon total length and was highest in Lake St. Clair. The probability of observing at least one lamprey mark on a 760 mm Lake Sturgeon was 8.1% or less for each sampling location in the SCDRS aside from Lake St. Clair (28.1%). Results suggest that parasitism of Lake Sturgeon by Sea Lamprey in the SCDRS is rare, particularly for Lake Sturgeon <760 mm TL. Low incidence of lamprey marks on Lake Sturgeon assumed to be susceptible to mortality from Sea Lamprey parasitism and zero occurrence of Sea Lamprey being observed attached to a Lake Sturgeon suggest Sea Lamprey at their current abundance likely have little effect on the Lake Sturgeon population in the SCDRS. Caution should be taken when using mark size to assign marks to lamprey species as there is substantial overlap among species oral disc diameters, potentially inflating the perceived impact of Sea Lamprey on Lake Sturgeon in areas with native lampreys.     

Using visible implant elastomer to study ammocoete populations with Cormack–Jolly–Seber models

This study examined the efficacy of marking wild populations of lampreys with visible implant elastomer (VIE) for 6–18 months to examine ammocoete movements using Cormack–Jolly–Seber (CJS) open‐population models. These methods were tested on two lamprey populations in different river systems. American brook lamprey Lethenteron appendix at Dyke Creek apparent survival (φ) was high in the summer and winter (c. 0·7), but declined after flow events in the spring and autumn. Sea lamprey Petromyzon marinus at Oquaga Creek φ in the top‐ranked models varied with stream location and time. Estimates of φ were similar to Dyke Creek during the summer (c. 0·7), but declined after flow events and remained low (c. 0·1) in winter. Open‐population models support current understanding of ammocoete movement, i.e. dispersal is driven by high‐flow events at certain times of the year. The present study provides a framework to study ammocoetes with VIE.     

Locomotor activity of river lamprey Lampetra fluviatilis (L.) during the spawning season

At high latitudes (62–64°N) the river lamprey Lampetra fluviatilis (L.) is shown to have a 24-hr locomotor activity during its spawning period just before midsummer. By keeping lampreys in cold water, the spawning was delayed about one month. Analysis of event recorder graphs indicate that the 24-hr activity is caused by addition of diurnal spawning activity to the basic nocturnal activity and is not caused by weak Zeitgeber conditions during midsummer.Water temperature might indirectly determine time of spawning of the river lamprey.     

Communicating (gap) junctions between chloride cells in the gill epithelium of the lamprey,Geotria australis

Summary Freeze-fracture replicas show that communicating (gap) junctions are present between chloride cells in the gill epithelium of young adults of the Southern Hemisphere lamprey, Geotria australis, acclimated to full-strength sea water. The junctions, which were already present when these lampreys were migrating downstream, may help coordinate the secretory activities of the chloride cells during the marine phase of the lamprey life cycle.     

Variability in migration timing of adult Pacific lamprey (<Emphasis Type="Italic">Lampetra tridentata</Emphasis>) in the Columbia River,U.S.A.

We examined the effects of river environment on the timing of spawning migrations by anadromous Pacific lamprey, Lampetra tridentata, in the Columbia River (U.S.A.). In a 41-year time series of adult lamprey counts, migration timing was earliest in warm, low-discharge years and latest in cold, high-flow years. Threshold temperatures associated with run timing were similar throughout the dataset despite significant impoundment-related warming, suggesting that temperature-dependent migration cues have been temporally stable. Within each year, migration rates of PIT-tagged lampreys were positively correlated with temperature and negatively correlated with discharge through multiple river reaches, offering additional evidence for environmental control of upstream movement. Both visual count and PIT-tag data indicated that there may be population-based differences in migration timing within the aggregate Columbia River lamprey run. These life history and behavioral results have potentially far-reaching implications for management of lamprey species.     

Do sturgeon limit burrowing shrimp populations in Pacific Northwest Estuaries?

Green sturgeon, Acipenser medirostris, and white sturgeon, Acipenser transmontanus, are frequent inhabitants of coastal estuaries from northern California, USA to British Columbia, Canada. An analysis of stomach contents from 95 green sturgeon and six white sturgeon commercially landed in Willapa Bay, Grays Harbor, and the Columbia River estuary during 2000–2005 revealed that 17–97% had empty stomachs, but those fish with items in their guts fed predominantly on benthic prey items and fish. Burrowing thalassinid shrimp (mostly Neotrypaea californiensis) were important food items for both white and especially for green sturgeon taken in Willapa Bay, Washington during summer 2003, where they represented 51% of the biomass ingested (84.9% IRI). Small pits observed in intertidal areas dominated by these shrimp, are likely made by these sturgeon and we present evidence from exclusion studies and field observation that the predator making the pits can have a significant cumulative negative effect on burrowing shrimp density. These burrowing shrimp present a threat to the aquaculture industry in Washington State due to their ability to de-stabilize the substrate on which shellfish are grown. Despite an active burrowing shrimp control program in these estuaries, it seems unlikely that current burrowing shrimp abundance and availability as food is a limiting factor for threatened green sturgeon stocks. However, these large predators may have performed an important top down control function on shrimp populations in the past when they were more abundant.     

Occurrence of the parasitic sea lamprey<Emphasis Type="Italic">Petromyzon marinus</Emphasis> on western North Atlantic right whales <Emphasis Type="Italic">Eubalaena glacialis</Emphasis>

Few data exist on the marine distribution and host organisms of the parasitic sea lamprey, Petromyzon marinus. Some observers have speculated that cetaceans serve as hosts for these fish based on scars, but few lamprey – cetacean interactions have been described in detail in the literature. Here we discuss 35 previously unreported records of sea lampreys that were observed while attached to western North Atlantic right whales, Eubalaena glacialis, during the period 1984 – 2002. Of these observations, 11 were photographically documented with images of sufficient quality to identify the lamprey as P. marinus based on morphological characteristics. The majority of the attachments were recorded in the Bay of Fundy during the summer months when P. marinus are preparing to spawn. It is unknown how lampreys might benefit from this association or what cost may be incurred by their right whale hosts. Feeding and transport are two possible reasons for the attachments.     

Aggregation and spawning by lampreys (genus Ichthyomyzon) beneath cover

Synopsis Lampreys are generally reported to spawn in shallow water on open, gravel bottoms. During surveys in Wisconsin and Minnesota, we regularly observed aggregations of adult Ichthyomyzon c.f. gagei, I. castaneus, and I. fossor beneath such cover objects as boulders, woody debris, and, at one site, vegetation. In some cases, observations of eggs or rapid quivering by individual lampreys indicated that spawning was occurring. The literature includes scattered anecdotal reports of similar behavior in other populations of Ichthyomyzon. Our data for I. c.f. gagei suggest that aggregations beneath cover objects occur at a greater range of depths than those in the open, but that aggregations in the open can contain greater numbers of individuals. Facultative spawning beneath cover objects may permit lampreys to spawn in deep waters with swift current where spawning could not otherwise occur. Moreover, this behavior may reduce the vulnerability of spawning lampreys to some types of predators.     

Central projections of the pineal complex in the silver lamprey Ichthyomyzon unicuspis

Summary The central projections of the pineal complex of the silver lamprey Ichthyomyzon unicuspis were studied by injection of horseradish peroxidase. The pineal tract courses caudally along the left side of the habenular commissure, and a few fibers penetrate the brain through the caudalmost portion of this commissure. Most of the fibers, however, continue caudally and enter the brain through the posterior commissure. The pineal tract projects bilaterally to the subcomissural organ, the superficial and periventricular pretectum, the posterior tubercular nucleus, the dorsal and ventral thalamus, the dorsal hypothalamus, the optic tectum, the torus semicircularis, the midbrain tegmentum, and the oculomotor nucleus. A few fibers decussate in the tubercular commissure, but the course of these decussate fibers could not be followed owing to the bilateral nature of the projections. No retrogradely labeled cells were found in the brain. With the exception of the projections to the optic tectum and torus semicircularis, the pineal projections in the silver lamprey are similar to those reported in other anamniote vertebrates.     

Characterization of vitellogenin from white sturgeon,Acipenser transmontanus

Sturgeon are an ancient family (Acipenseridae) of fishes that lie close to the divergence of fish that eventually evolved into terrestrial animals and those that evolved into modern teleost species. Therefore, white sturgeon vitellogenin sequences fill a gap in the current understanding of the functional domains of this protein family. Vitellogenin cDNA was sequenced and used to investigate gene expression in white sturgeon, Acipenser transmontanus. Estrogen-induced vitellogenin mRNA was detected in the livers of both males and females and was also detected in undifferentiated gonads of estrogen-treated fish. Low levels of vitellogenin mRNA were also detected in the testis of both control and estrogen-treated males. The cDNA encoded a 186-kDa protein that was missing only six to seven of the amino-terminal amino acids. Comparisons to silver lamprey, Xenopus, and chicken vitellogenin sequences indicate that the overall structure of the yolk protein domains were highly conserved. There was considerable homology in three regions of the lipovitellin I domain. These conserved sequences are likely to be involved in vitellogenin receptor binding. The phosvitin domain of white sturgeon vitellogenin contained fewer and shorter serine repeats as predicted from yolk protein phosphate content of fish compared to Xenopus and chicken. However, the vitellogenin of white sturgeon had a lower serine content as compared with silver lamprey, indicating that an increased serine content is not strictly a function of evolutionary age. Correspondence to: C. A. Bidwell     

A Noninvasive Technique for Determining Sex of Live Adult North American Sturgeons

We have developed a noninvasive technique to determine the sex of adult North American sturgeon by examination of the external morphology of live individuals. We analyzed four sturgeon species taken by commercial and scientific harvest: white Acipenser transmontanus, green A. medirostris, Atlantic A. oxyrinchus and shortnose A. brevirostrum. Males have a urogenital opening in the shape of a letter Y, while the opening of females is in the shape of the letter O. We accurately sexed 26 of 36 sturgeon using this criterion. Accuracy was highest in live fish (82%), and significantly lower in dead fish (29%). Dead sturgeon usually have the rectum prolapsed so that the urogenital opening is protruded, and thus making the sexes indistinguishable.     

Allozyme Polymorphisms and Biochemical-Genetic Taxon Markers in Lampreys (Lampetra, Eudontomyzon, Petromyzon)

Variation at 23 putative enzyme-coding loci was scored in 424 lampreys, including 321 European brook lampreys (Lampetra planeri), 83 European river lampreys (L. fluviatilis), 11 Ukrainian brook lampreys (Eudontomyzon mariae), and nine sea lampreys (Petromyzon marinus). Twelve polymorphisms are described for Lampetra species (LDH*, SOD-2*, PNP*, AAT-1*, AK-1*, ES-2*, LGL*, MPI*, GPI-1*, GPI-2*, PGM*, IDHP-2*), and two each for E. mariae (GPI-1*, ME-2*) and P. marinus (MDH-1*, ME-2*). Diagnostic allozymes are presented for the discrimination of lamprey taxa, some of which are difficult to recognize from the morphology of ammocoetes larvae, the life stage usually encountered when collecting cyclostomes. The allelic markers described permit the clear allocation to a genus, except for the species L. fluviatilis and L. planeri, which are not differentiated by qualitative allozyme analysis.     

River lamprey present an unusual predation threat to Atlantic salmon smolts in Lough Neagh,Northern Ireland

A new monitoring programme on the Lough Neagh catchment has documented a high incidence of river lamprey, Lampetra fluviatilis L., predation on Atlantic salmon smolts, Salmo salar L. In total 470 smolts were examined during the 2020 emigration period with 168 fish (36%) exhibiting lamprey scars of which 57 were lightly scarred and 111 were classed as heavily scarred. Lamprey predation was not size selective on Lough Neagh S. salar smolts.     

Thermal maxima for juvenile shortnose sturgeon acclimated to different temperatures

Many populations of shortnose sturgeon, Acipenser brevirostrum, in the southeastern United States continue to suffer from poor juvenile recruitment. High summer water temperatures, which may be exacerbated by anthropogenic activities, are thought to affect recruitment by limiting available summer habitat. However, information regarding temperature thresholds of shortnose sturgeon is limited. In this study, the thermal maximum method and a heating rate of 0.1°C min⁻¹ was used to determine critical and lethal thermal maxima for young-of-the-year (YOY) shortnose sturgeon acclimated to temperatures of 19.5 and 24.1°C. Fish used in the experiment were 0.6 to 35.0 g in weight and 64 to 140 days post hatch (dph) in age. Critical thermal maxima were 33.7°C (±0.3) and 35.1°C (±0.2) for fish acclimated to 19.5 and 24.1°C, respectively. Critical thermal maxima significantly increased with an increase in acclimation temperature (p < 0.0001). Lethal thermal maxima were 34.8°C (±0.1) and 36.1°C (±0.1) for fish acclimated to 19.5 and 24.1°C, respectively. Lethal thermal maxima were significantly affected by acclimation temperature, the log₁₀ (fish weight), and the interaction between log₁₀(fish weight) and acclimation temperature (p < 0.0001). Thermal maxima were used to estimate upper limits of safe temperature, thermal preferences, and optimal growth temperatures of YOY shortnose sturgeon. Upper limits of safe temperature were similar to previous temperature tolerance information and indicate that summer temperatures in southeastern rivers may be lethal to YOY shortnose sturgeon if suitable thermal refuge cannot be found.     

Carbohydrate reserves,radial growth,and mechanisms of resistance of oak trees to phloem-boring insects

Summary The twolined chestnut borer, Agrilus bilineatus (Weber) (Coleoptera: Buprestidae), attacks oaks (Quercus spp.) that have been weakened by prior environmental or biotic stress. Our earlier work showed that trees with relatively low winter starch reserves are more likely to be attacked by A. bilineatus the following summer. We hypothesized that such trees may have less energy available for defense (Callus formation and allelo-chemical synthesis) in tissues wounded by borer larvae. However, wounding experiments showed little or no relationship between winter or summer carbohydrate reserves, callus formation, radial growth, or concentrations of tannins and phenolics in wounded or nonwounded phloem tissues. Trees with relatively low winter carbohydrate reserves were again found to be attractive to adult A. bilineatus, although not all low starch trees were attacked or successfully colonized by borers. There was a trend for carpenterworm larvae, Prinoxystus robiniae (Lepidoptera: Cossidae), a generalist bark and wood borer, to be more successful in establishing galleries on low starch trees. Carpenterworms gained significantly more weight when fed phloem from trees attractive to A. bilineatus. Oaks that attracted large numbers of A. bilineatus or that were successfully colonized by the borer produced significantly less callus than did non-attacked trees when experimentally wounded at about the time of Agrilus egg hatch. Callus formation may limit the establishment of small larvae that feed slowly in the cambial region. These results indicate that current theory regarding relationships between increased tree stress and decreased allocation of energy reserves to radial growth and defense against phloem borers may be an oversimplification. We suggest that tree growth and the defensive response of phloem tissues may be limited more by the rate of carbohydrate utilization or by changes in source-sink relationships than by storage levels. Callus formation and synthesis of allelochemicals in wounded phloem may be under the same control as cambial activation, which is mediated by plant growth regulators and can be influenced by environmental conditions.     

Contemporary gene flow between “paired” silver (<Emphasis Type="Italic">Ichthyomyzon unicuspis</Emphasis>) and northern brook (<Emphasis Type="Italic">I. fossor</Emphasis>) lampreys: implications for conservation

In most lamprey genera, “paired” species exist in which the larvae are morphologically similar or indistinguishable but, following metamorphosis, one species becomes parasitic while the other bypasses the adult feeding phase and rapidly becomes sexually mature. Since DNA barcoding and similar studies using short segments of the mitochondrial genome do not provide sufficient resolution to distinguish between recent divergence and a lack thereof, the current study examined the relationship between the parasitic silver lamprey (Ichthyomyzon unicuspis) and nonparasitic northern brook lamprey (I. fossor) using up to 10,230 bp from the mitochondrial genome to make phylogenetic inferences and mitochondrial restriction fragment length polymorphism (RFLP) and microsatellite markers to test for significant differences in allele frequencies. We found that silver and northern brook lampreys are not reciprocally monophyletic; two lineages were observed but each occurred within both species. There also were no significant range-wide differences in RFLP haplotype or microsatellite allele frequencies between the species, nor were there significant differences where they occurred sympatrically within the Lake Huron basin. Significant genetic differentiation was found only within the Lake Michigan basin where the results were potentially confounded by geographic separation. Our results thus support suggestions that silver and northern brook lampreys represent ecotypes of a single species since, where they are sympatric, they appear to be experiencing ongoing gene flow. However, alternative life history strategies can be important for a species’ long-term persistence, and critical data are needed to decide whether these two feeding types should be managed as a single unit.     

Disturbance of the indigenous gene pool of the threatened brook lamprey Lethenteron sp. S by intraspecific introgression and habitat fragmentation

Artificial introduction and habitat fragmentation affect the indigenous gene pools of fluvial animals. To investigate the effect of human activities on the genetic population structure of vulnerable brook lamprey Lethenteron sp. S in a single river system, samples from 12 tributaries of the Jinzu River, Japan, were analyzed using mitochondrial and microsatellite DNA markers. Exogenous Lake Biwa (Japan) haplotypes and alleles were detected in lampreys from several Jinzu River tributaries. Since Lake Biwa is the source of the commercial ayu fish Plecoglossus altivelis that is introduced in the Jinzu River, the exogenous Lake Biwa lamprey genotypes in the Jinzu River probably originated from the Lake Biwa lampreys that were unintentionally introduced along with the ayu fish. Bayesian admixture and mitochondrial DNA analyses revealed various genetic disturbance phases of the exogenous genotypes in the Jinzu River, such as the six indigenous populations, four admixed populations with low frequencies (average admixture proportion = 0.02–0.04; exogenous haplotype proportion <0.01), one introgressed population (0.71 and 0.57) and one population almost displaced by exogenous genotypes (0.93 and 0.96). Samples from three tributaries with weirs were genetically differentiated from the others by using pairwise F _ST and Bayesian analyses; the results suggested isolation by the weirs. Reduced mitochondrial DNA diversity was observed in 1 of the 3 samples probably due to reduced population size. These findings indicate that the indigenous lamprey populations in the Jinzu River are seriously affected by introgression with exogenous genotypes via unintentional introduction and habitat fragmentation by weirs.