Absence of shared mitochondrial DNA haplotypes between sea lamprey from North American and Spanish rivers

Sea lamprey Petromyzon marinus from the River Miño and Sella, Spain, showed an almost identical frequency for three observed haplotypes. None of these haplotypes were found among three North American populations. These results indicate an absence of exchange among sea lamprey populations spawning in the west and south‐east Atlantic coasts. The similarity between the collections from the two Spanish rivers suggests that homing does not occur in anadromous sea lamprey.     

Neither philopatric nor panmictic: microsatellite and mtDNA evidence suggests lack of natal homing but limits to dispersal in Pacific lamprey

Most species with lengthy migrations display some degree of natal homing; some (e.g. migratory birds and anadromous salmonids) show spectacular feats of homing. However, studies of the sea lamprey (Petromyzon marinus) indicate that this anadromous species locates spawning habitat based on pheromonal cues from larvae rather than through philopatry. Previous genetic studies in the anadromous Pacific lamprey (Entosphenus tridentatus) have both supported and rejected the hypothesis of natal homing. To resolve this, we used nine microsatellite loci to examine the population structure in 965 Pacific lamprey from 20 locations from central British Columbia to southern California and supplemented this analysis with mitochondrial DNA restriction fragment length polymorphism analysis on a subset of 530 lamprey. Microsatellite analysis revealed (i) relatively low but often statistically significant genetic differentiation among locations (97% pairwise F(ST) values were <0.04 but 73.7% were significant); and (ii) weak but significant isolation by distance (r(2) = 0.0565, P = 0.0450) but no geographic clustering of samples. The few moderate F(ST) values involved comparisons with sites that were geographically distant or far upstream. The mtDNA analysis--although providing less resolution among sites (only 4.7%F(ST) values were significant)--was broadly consistent with the microsatellite results: (i) the southernmost site and some sites tributary to the Salish Sea were genetically distinct; and (ii) southern sites showed higher haplotype and private haplotype richness. These results are inconsistent with philopatry, suggesting that anadromous lampreys are unusual among species with long migrations, but suggest that limited dispersal at sea precludes panmixia in this species.     

Aquatic food‐web dynamics following incorporation of nutrients derived from Atlantic anadromous fishes

Changes in the isotopic composition (δ¹³C and δ¹⁵N) in biofilm, macro‐invertebrates and resident salmonids were used to characterize temporal dynamics of marine derived nutrients (MDNs) incorporation between stream reaches with and without MDN inputs. Five Atlantic rivers were chosen to represent contrasting MDN subsidies: four rivers with considerable numbers of anadromous fishes; one river with little MDN input. Rainbow smelt Osmerus mordax, alewife Alosa pseudoharengus, sea lamprey Petromyzon marinus and Atlantic salmon Salmo salar, were the primary anadromous species for the sampled rivers. Regardless of the spatial resolution or the pathway of incorporation, annual nutrient pulses from spawning anadromous fishes had a positive effect on isotopic enrichment at all trophic levels (biofilm, 1·2–5·4‰; macro‐invertebrates, 0·0–6·8‰; fish, 1·2–2·6‰). Community‐wide niche space shifted toward the marine‐nutrient source, but the total ecological niche space did not always increase with MDN inputs. The time‐integrated marine‐nutrient resource contribution to the diet of S. salar parr and brook trout Salvelinus fontinalis ranged between 16·3 and 36·0% during anadromous fish‐spawning periods. The high degree of spatio‐temporal heterogeneity in marine‐nutrient subsidies from anadromous fishes lead to both direct and indirect pathways of MDN incorporation into stream food webs. This suggests that organisms at many trophic levels derive a substantial proportion of their energy from marine resources when present. The current trend of declining anadromous fish populations means fewer nutrient‐rich marine subsidies being delivered to rivers, diminishing the ability to sustain elevated riverine productivity.     

Fruit of the forest - larval sea lamprey Petromyzon marinus are fuelled by allochthonous resources

We used stable isotopes of carbon, hydrogen and nitrogen to quantify the trophic position and resource use of larval sea lamprey Petromyzon marinus, four benthic macroinvertebrate functional feeding guilds (scraper, shredder, collector and predator) and other fishes in three rivers in eastern Canada. Larval lamprey and most invertebrate guilds foraged as primary consumers in all rivers whereas all other fishes predominantly foraged as secondary consumers. Larval lamprey obtained 75–85% of their resources from allochthonous derived material. This level exceeded all invertebrate guilds, which assimilated approximately 50% allochthonous and 50% autochthonous materials and fishes, which predominantly assimilated between 25% and 60% allochthonous material. Larval lamprey occupied a unique position within the river food webs analysed and show remarkable fidelity to a trophic niche specialising on terrestrially derived detritus.     

Population dynamics and harvesting of semelparous species with phenotypic and genotypic variability in reproductive age

We study the evolution of polymorphic life histories in anadromous semelparous salmon and the effects of harvesting. We derive dynamic phenotypic and genetic ESS models for describing the evolutionary dynamics. We show in our deterministic analysis that polymorphisms are not possible in a panmictic random mating population. Instead, genetic or behavioral polymorphisms may be observed in populations with assortative mating systems. Positive assortative mating may be supported and generated by behavioral and phenotypic traits like male mate choice, spawning ground selection by phenotype, or within-river homing-migration-distance by size. In the case of an evolutionarily stable dimorphism, the ESS is characterized by a reproductive ideal free distribution such that at an equilibrium the individuals are indifferent from the fitness point of view between the two life histories of early and late reproduction. Different strategy models - that is, phenotypic and genetic ESS models - yield identical behavioral predictions and, consequently, genetics does not seem to play an important role in the present model. An evolutionary response to increased fishing mortality is obvious and may have resource management implications. High sea fishing mortalities drive the populations toward early spawning. Thus it is possible that unselective harvesting at sea may eliminate, depending on the biological system, behavioral polymorphisms or genetic heterozygozity and drive the population to a monomorphic one. If within-river homing migration distances depend on the size of fish, unselective harvesting at sea, or selective harvesting of spawning runs in rivers, may reduce local population sizes on spawning grounds high up rivers. Finally, harvesting in a population may cause a switch in a dominant life-history strategy in a population so that anticipated sustainable yields cannot be realized in practice.     

The haematophagous feeding stage of anadromous populations of sea lamprey Petromyzon marinus: low host selectivity and wide range of habitats

Limited information is available regarding habitat use and host species of the haematophagous feeding stage of the anadromous sea lamprey Petromyzon marinus Linnaeus, 1758, due to the difficulties in capturing feeding lampreys and wounded hosts. The aim of this study is to provide new records of P. marinus feeding on host species and to review the available information in this regard to better know the ecology and distribution of sea lamprey during this stage. Thus, new records of P. marinus individuals or wounds on 23 species of fishes and cetaceans are provided. Nineteen of these species were described for the first time as hosts of P. marinus. As a result, an updated list of 54 host species is provided. They belong to diverse taxonomic groups and exhibit different morphological, physiological and ecological patterns. The attacks were located from fresh and brackish waters to open sea. The results suggest that the marine distribution of P. marinus is mainly related to coastal areas with part of the population widely dispersed in offshore areas. This remarkable capacity of inhabiting a broad range of aquatic ecosystems and exploiting different host species could have favoured the dispersal ability and evolutionary success of sea lamprey.     

Occurrence of Ergasilus megaceros Wilson, 1916, in the sea lamprey and other fishes from North America

Ergasilus megaceros (Copepoda: Ergasilidae) was recovered from the nasal fossae (lamellae) of the olfactory sac in 1 (1.8%) of 56 sea lampreys, Petromyzon marinus Linne, 1758, collected in May 2002 from the Cheboygan River, Michigan. Although the sea lamprey is a new host record for E. megaceros, this fish species may not be a preferred host because of its low prevalence. Ergasilus megaceros is the second ergasilid species reported from the sea lamprey in North America. This is the third report of an ergasilid species infecting the nasal fossae of fishes in North America, with E. rhinos being the only other species reported from this site.     

THE VISUAL SYSTEM AND VITAMINS A OF THE SEA LAMPREY

The porphyropsin-vitamin A₂ cycle has been found heretofore only in the retinas of bony fishes capable of existence in fresh water. Cyclostomes, due to their primitive and isolated phylogenetic position, might be expected to possess the rhodopsin-vitamin A₁ cycle common to marine elasmobranchs, almost all marine teleosts, and all terrestrial vertebrates so far examined. Yet the anadromous sea lamprey, Petromyzon marinus, possesses primarily the porphyropsin system, like an anadromous teleost. This observation greatly extends the phylogenetic association of vitamin A₂ with the capacity for freshwater existence. Compared with freshwater and anadromous teleosts, the lamprey retina contains the porphyropsin system in extremely low concentration. The remaining eye tissues, like the retina, contain both vitamins A₁ and A₂, the latter greatly predominant. The livers of larval and adult lampreys, however, appear to contain vitamin A₁ alone. This situation also is not without teleost precedent, since the carp and certain anadromous salmonids display similar reversals of vitamin A pattern in the liver and eye tissues.     

Life history and genetic characterisation of sea trout Salmo trutta in the Adriatic Sea

1. The brown trout Salmo trutta is characterised by both anadromous (sea trout) and resident populations, naturally occurring in Atlantic and Ponto-Caspian rivers. Sea trout are currently considered absent from rivers of the Mediterranean area, probably because of the non-optimal chemical–physical characteristics of the Mediterranean Sea. However, the occasional bycatch of smoltified S. trutta in the Adriatic Sea is well known among fishermen and the biological explanation of this phenomenon is still controversial. The aim of this study was to compare the genetic diversity of freshwater and marine brown trout to try to understand the factors underlying the presence of putative anadromous brown trout in the Adriatic Sea.
2. In this study, we analysed the genetic diversity of: (1) wild brown trout collected from the Esino River (central Italy); (2) a domestic strain of brown trout used for stocking the study area; and (3) a sample of Adriatic sea trout collected near the outlet of the Esino River. Together with genetic analysis, we carried out scale analysis in order to track the freshwater/marine stages of the life cycle in the sea trout samples. The genetic characterisation was carried out by polymerase chain reaction–restriction fragment length polymorphism analysis of the mtDNA fragment ND-5/6 and the nuclear locus LDH-C1* and by genotyping 15 microsatellite loci. The genetic polymorphism obtained was used to investigate intra- and inter-population genetic diversity, rates of genetic introgression between wild and domestic samples and the origin of sea trout specimens by using assignment tests.
3. Our genetic analyses demonstrated that the sea trout analysed in this study are from the domestic strain of Atlantic origin used in central Italy for stocking activities. The level of genetic introgression between native and domestic samples is high in the Esino River. The populations more resilient to introgressive hybridisation appeared to be those living in the portion of the river network dominated by carbonate rocks. Assignment tests (GeneClass) suggest the existence of a link between stocking efforts and the freshwater origin of the sea trout. In addition, data obtained from the analysis of scales, size measurement, and sex determination showed a pattern of smolt age, size, and sex ratio very similar to those observed in other anadromous populations.
4. In conclusion, the present study highlighted that sea trout from the central Adriatic Sea originated from brown trout of Atlantic origin inhabiting the Esino River. Their seaward migratory behaviour could represent a consequence of an active migration instead of a passive displacement by water flow. Our results also showed that traditional stocking practices represent a negative activity for the conservation of the last Mediterranean native S. trutta populations.

     

Expression of olfactory receptors in different life stages and life histories of wild Atlantic salmon (Salmo salar)

It has been hypothesized that salmonids use olfactory cues to return to their natal rivers and streams. However, the key components of the molecular pathway involved in imprinting and homing are still unknown. If odorants are involved in salmon homing migration, then olfactory receptors should play a critical role in the dissipation of information from the environment to the fish. Therefore, we examined the expression profiles of a suite of genes encoding olfactory receptors and other olfactory-related genes in the olfactory rosettes of different life stages in two anadromous and one non-anadromous wild Atlantic salmon populations from Newfoundland, Canada. We identified seven differentially expressed OlfC genes in juvenile anadromous salmon compared to returning adults in both populations of anadromous Atlantic salmon. The salmon from the Campbellton River had an additional 10 genes that were differentially expressed in juveniles compared to returning adults. There was no statistically significant difference in gene expression of any of the genes in the non-anadromous population (P < 0.01). The function of the OlfC gene products is not clear, but they are predicted to be amino acid receptors. Other studies have suggested that salmon use amino acids for imprinting and homing. This study, the first to examine the expression of olfactory-related genes in wild North American Atlantic salmon, has identified seven OlfC genes that may be involved in the imprinting and homeward migration of anadromous Atlantic salmon.     

Movement of radio-tagged anadromous sea lamprey during the spawning migration in the River Mondego (Portugal)

The available spawning habitat for the anadromous sea lamprey, Petromyzon marinus L., population that enters the River Mondego has been drastically reduced in the last 20 years. The installation of a fish passage in the first impassable dam, the Açude-Ponte, would enable sea lamprey to recolonise the 34.6-km river stretch between the Açude-Ponte and Raiva dams. In order to assess the suitability of the upstream river stretches for this species, 10 radio-tagged sea lamprey were released upstream of the Açude-Ponte dam and tracked continuously throughout the entire migratory path. Lamprey were unable to pass over intact weirs that had been built for recreational purposes. Sea lamprey movements were more frequent during dusk and night than other periods. Increased river discharge at night, resulting from the operation of the Raiva power station, stimulated lamprey movements but reduced ground speeds recorded. After reaching a certain location, some of the animals maintained their position for several weeks, before undergoing a new movement. Two of the main tributaries of this river stretch were used by some sea lamprey, indicating that the animals were able to find these historical spawning grounds.     

Population structure and gene flow among anadromous arctic lamprey (Lethenteron camtschaticum) populations deduced from polymorphic microsatellite loci

Information on migration ecology is important for effective conservation and management of fishery resources, particularly diadromous animals. We investigated the genetic population structure and gene flow pattern of anadromous Arctic lamprey Lethenteron camtschaticum by analyzing polymorphic microsatellite loci. Bayesian population structure analysis was used to estimate the existence of two genetically divergent ancestral sources and latitudinal gradual changes of their frequencies among the present populations. When hypotheses of historical migration models were tested using coalescent-based methods, the best model was found to be an n-island model assuming equal population size and reciprocal migration among all populations. These results suggest that L. camtschaticum has considerable ability to migrate long distances in the sea and has lower homing abilities. For resource management of L. camtschaticum, unconstrained gene flow across all populations should be maintained. The present findings might be beneficial for conservation and contribute the sustainable use of L. camtschaticum resource.     

Patterns of invasion and colonization of the sea lamprey (Petromyzon marinus) in North America as revealed by microsatellite genotypes

Invasions by exotic organisms have had devastating affects on aquatic ecosystems, both ecologically and economically. One striking example of a successful invader that has dramatically affected fish community structure in freshwater lakes of North America is the sea lamprey (Petromyzon marinus). We used eight microsatellite loci and multiple analytical techniques to examine competing hypotheses concerning the origins and colonization history of sea lamprey (n = 741). Analyses were based on replicated invasive populations from Lakes Erie, Huron, Michigan, and Superior, populations of unknown origins from Lakes Ontario, Champlain, and Cayuga, and populations of anadromous putative progenitor populations in North America and Europe. Populations in recently colonized lakes were each established by few colonists through a series of genetic bottlenecks which resulted in lower allelic diversity in more recently established populations. The spatial genetic structure of invasive populations differed from that of native populations on the Atlantic coast, reflecting founder events and connectivity of invaded habitats. Anadromous populations were found to be panmictic (theta(P) = 0.002; 95% CI = -0.003-0.006; P > 0.05). In contrast, there was significant genetic differentiation between populations in the lower and upper Great Lakes (theta(P) = 0.007; P < 0.05; 95% CI = 0.003-0.009). Populations in Lakes Ontario, Champlain, and Cayuga are native. Alternative models that describe different routes and timing of colonization of freshwater habitats were examined using coalescent-based analyses, and demonstrated that populations likely originated from natural migrations via the St Lawrence River.     

Genetic signatures of historical bottlenecks in sympatric lake trout (Salvelinus namaycush) morphotypes in Lake Superior

Humans have played a significant role in reducing levels of genetic diversity and differentiation of many teleost fishes, leading to homogenization across biological entities. We compare patterns of historical and contemporary genetic structure for three sympatric Great Lake??s lake trout (Salvelinus namaycush) morphs (lean, siscowet, and humper) that differ in patterns of habitat occupancy, susceptibility to overfishing and predation by invasive sea lamprey (Petromyzon marinus). Differential susceptibilities to overfishing and predation were expected to result in different impacts to levels of genetic diversity loss for each morphotype. Genetic data was collected for samples at three points in time: 1948 (pre-collapse), 1959 (collapse) and 1990s (current), corresponding to periods of intensive fishing, mortality due to lamprey and recovery, respectively. The lean morph preferentially targeted by the fishery and recognized as highly preyed upon by sea lamprey was more highly impacted genetically than other morphs, as evidenced by greater loss of genetic diversity first during the period of overfishing, then during the period of high sea lamprey abundance once the fishery collapsed. The siscowet morph also experienced genetic bottlenecks during the period of overfishing (pre-collapse period). Results indicate significant levels of genetic differentiation among morphs historically prior to declines in abundance and also among contemporary populations, suggesting that periods of population decline and resurgence in abundance and distribution did not result in loss of genetic distinctiveness among morphs.     

Light and electron microscopic immunocytochemical localization of thyroglobulin in the thyroid gland of the anadromous sea lamprey,Petromyzon marinus L., during its upstream migration

Summary Antibodies made against thyroglobulin (TG) were used in an immunocytochemical study for the light and electron microscopic localization of TG in the thyroid gland of the anadromous sea lamprey, Petromyzon marinus, during its upstream migration. TG was found in the follicular lumen and in some colloid droplets within the follicular cells. Except for an immunoreactive product observed in a small portion of the interstitial connective tissue, the location of TG in the lamprey was similar to that in the thyroid of the rat.Supported by National Research Council of Canada Grant no. A5945 to J.H.Y. We thank Dr. F.W.W. Beamish and Mr. R. Robinson who helped in the capture of the lamprey     

A critical review of the discovery and application of a migratory pheromone in an invasive fish, the sea lamprey Petromyzon marinus L.

The sea lamprey Petromyzon marinus , an ancient and parasitic agnathan fish native to the North Atlantic, invaded the Laurentian Great Lakes approximately a century ago triggering its fisheries to collapse. Presently, this species is held in check through a toxicant-based control programme directed by a bi-national treaty organization that seeks to develop a more broadly based integrated pest management (IPM) strategy. After a long and difficult search, the most active components of a migratory pheromone for the sea lamprey were identified and synthesized. This pheromone has remarkable potency and considerable potential to enhance various control strategies that fall within an IPM scheme. The pheromone is comprised of a mixture of at least three sulphated steroids: petromyzonamine disulphate (PADS), petromyzosterol disulphate (PSDS) and petromyzonol sulphate (PS). A steroidal sex pheromone appears to have similar promise. These discoveries, which are prompting development of the first pheromonally guided pest management programme for an invasive fish, have revealed significant scientific and policy challenges. Among the former are the needs to acquire long-term and significant support for the science, to synthesize sufficient quantities of cues, and to deploy and measure pheromonal components in natural waters. Among the latter are the needs to regulate this new type of 'pesticide', protect these technologies from exploitation and promote future research on this and other invasive fish species. Lessons from these experiences may be applicable to the study of other invasive fishes.     

Lymphoid Components in the Branchial Cavernous Body of the Ammocoete of Petromyzon marinus

The cavernous body of the ammocoetes of the anadromous sea lamprey Petromyzon marinus was ultrastructurally analyzed with special emphasis on its lymphoid components. It is a vascular structure differentiated from the afferent artery of each gill filament and contains a specialized phagocytic endothelial cell, named the cavernous body (CB) cell. In the vascular spaces of the cavernous body there occur numerous lymphoid cells, including lymphocytes, lymphoblasts, mature and developing plasma cells and large macrophages, which make contact with the CB cells. The role of these cells is discussed as to the suggested functions of the cavernous body in the defence mechanisms of lampreys.     

Re-colonization of Atlantic and Pacific rivers by anadromous fishes: linkages between life history and the benefits of barrier removal

The last two decades have seen a rapid increase in barrier removals on rivers of the Northern Hemisphere, often for the explicit purpose of expanding the abundance, spatial distribution, and life history diversity of migratory fishes. However, differences in life history such as seasonal timing of migration and reproduction, iteroparity versus semelparity, and the extent of natal homing are likely to affect the capacity for expansion and re-colonization by taxa such as alosines, lamprey, and salmonids. We first review some basic life history traits that may affect re-colonization by migratory fishes, and then present selected examples from Atlantic and Pacific basins to illustrate these patterns and their implications for the success of barrier removal as a measure to advance the goal of fish conservation. We conclude that diadromous fishes have the capacity to rapidly re-colonize newly available habitats, though the life history patterns of each species, the proximity to source populations in the same or nearby river systems, and the diversity of habitats available may control the patterns and rates of re-colonization.     

Genetic diversity and differentiation in a wide ranging anadromous fish,American shad (Alosa sapidissima), is correlated with latitude

Studies that span entire species ranges can provide insight into the relative roles of historical contingency and contemporary factors that influence population structure and can reveal patterns of genetic variation that might otherwise go undetected. American shad is a wide ranging anadromous clupeid fish that exhibits variation in demographic histories and reproductive strategies (both semelparity and iteroparity) and provides a unique perspective on the evolutionary processes that govern the genetic architecture of anadromous fishes. Using 13 microsatellite loci, we examined the magnitude and spatial distribution of genetic variation among 33 populations across the species' range to (i) determine whether signals of historical demography persist among contemporary populations and (ii) assess the effect of different reproductive strategies on population structure. Patterns of genetic diversity and differentiation among populations varied widely and reflect the differential influences of historical demography, microevolutionary processes and anthropogenic factors across the species' range. Sequential reductions of diversity with latitude among formerly glaciated rivers are consistent with stepwise postglacial colonization and successive population founder events. Weak differentiation among U.S. iteroparous populations may be a consequence of human‐mediated gene flow, while weak differentiation among semelparous populations probably reflects natural gene flow. Evidence for an effect of reproductive strategy on population structure suggests an important role for environmental variation and suggests that the factors that are responsible for shaping American shad life history patterns may also influence population genetic structure.