1. Introduction: A Surfeit of Lampreys.- 2. The Taxonomy, Phylogeny, and Distribution of Lampreys.- 3. The Ecology of Larval and Metamorphosing Lampreys.- 4. Lamprey Metamorphosis.- 5. Lamprey Spawning Migration.- 6. Reproductive Ecology of Lamprey.- 7. The Reproductive Hypothalamic-Pituitary Axis in Lampreys.- 8. Conservation of Native Lampreys.

Lampreys : biology, conservation and control

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

/pdf/the-behavioural-response-of-adult-petromyzon-marinus-to-p0hr2tgp2m.pdf

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

Sea lamprey invaded the Laurentian Great Lakes above Lake Ontario in the 1900s, and were a factor in the collapse of several major fish stocks. Whether the species is native to Lake Ontario, Lake Champlain, and the Finger Lakes of New York is debated; nevertheless, it is considered to be a nuisance species in these waters. Early control of sea lamprey included use of barriers in streams to prevent upstream spawning, and use of lampricides to kill larvae; these methods are the mainstay of the current control program. Sterile males were used to reduce spawning success for several years in the St. Marys River, but this practice has been discontinued due to challenges with evaluating its success and the availability of improved lampricide options. Success of the control program is measured as reduction in number of spawning adults that ascend streams, and reduction in lake trout wounding. Both metrics have been substantially reduced and either meet or are close to targets for each of the Great Lakes; targets for the Finger Lakes and Lake Champlain are considerably higher than in the Great Lakes, and have not yet been met. Concerns about the effect of lampricides and barriers on non-target species and on ecosystem integrity have prompted a search for additional control methods. Research has focused on the use of pheromones and repellants, genetic strategies, and improving the specificity and efficacy of existing control methods. Prevention of the spread of sea lamprey into new bodies of water is also a priority. Over 60 years of sea lamprey control efforts have considerably advanced our understanding of sea lamprey behavior, physiology, genomics, and chemical communication.

Control of Invasive Sea Lamprey in the Great Lakes, Lake Champlain, and Finger Lakes of New York

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.

/pdf/the-haematophagous-feeding-stage-of-anadromous-populations-10i77ug8x6.pdf

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

Despite their highly conserved body plan and larval stage, adult life history type in lampreys diverges on two main axes related to migration and feeding. Of the 41–45 recognized lamprey species, 18 species feed parasitically after metamorphosis and their juvenile (sexually immature) feeding phase lasts from 3–4 months to 2–4 years. Nine of these species are exclusively freshwater resident; five are exclusively or almost exclusively anadromous, and four (sea lamprey, European river lamprey, Arctic lamprey, and, to a lesser extent, Pacific lamprey) are largely anadromous but with established freshwater populations. The other 23–27 described species are non-parasitic “brook” lampreys which remain within their natal streams. They initiate sexual maturation during metamorphosis, and, because the non-trophic periods of metamorphosis and sexual maturation are superimposed, the parasitic feeding phase is eliminated; this makes them the only vertebrates known to have non-trophic adults. Body size at maturity varies dramatically among life history types, ranging from ~110 to 150 mm total length (TL) in non-parasitic species to 800–900 mm TL in the anadromous sea lamprey. Freshwater forms are typically intermediate in size, although those that inhabit small systems may be no larger than non-parasitic lampreys and others (particularly the Great Lakes sea lamprey) are quite large. Some anadromous species (most notably European river lamprey, Pacific lamprey, and Arctic lamprey) show considerable intraspecific variation, consisting of typical large-bodied forms and dwarf or “praecox” forms that appear to feed at sea for a reduced period of time. Establishment in fresh water is more common in species that are consistently small-bodied or those with praecox forms. The only exceptions are the very small-bodied western river lamprey (mean TL at maturity ~200 mm), which does not produce freshwater parasitic forms (although it has given rise to innumerable non-parasitic freshwater populations), and the sea lamprey which, despite its very large size, has successfully colonized the Great Lakes. Abundant prey of a suitable size range is critical for establishment of freshwater parasitic populations. However, even with abundant prey, abandonment of anadromy is expected only under circumstances where decreases in mortality and the costs associated with migration make the reduction in size at maturity, and the accompanying reduction in fecundity, worthwhile. Pacific lamprey generally fail to establish when isolated above recently constructed barriers, likely because the reservoirs in which they have been isolated are relatively small and because they appear to osmoregulate poorly in fresh water. However, because colonization of fresh water appears to select for individuals “pre-adapted” to feed and grow to maturity in fresh water (i.e., relying on existing genetic variation within the source population), probability of establishment would likely increase with the number of founders. The existence of three closely related freshwater parasitic species suggests that Pacific lamprey successfully colonized fresh water in the past. Whether sea lamprey colonized Lake Ontario and Lake Champlain post-glacially or in historic times is debated. At present, the “invasion-by-canal” hypothesis appears to be the most convincing, but definitive resolution should be possible with genome-level analyses. Given the decimation of the Great Lakes ecosystem by sea lamprey, it is critical to be able to predict the potential for anadromous lampreys to become invasive in other freshwater systems. Migratory type is rarely considered a species-specific character unless it is accompanied by identifiable morphological differences. In contrast, variability in feeding type has long been considered a species-specific character because size-assortative mating was thought to result in reproductive isolation between parasitic and non-parasitic forms. However, not all parasitic and non-parasitic forms appear to be reproductively isolated, and different species show different degrees of divergence from their presumed parasitic ancestor. “Paired” non-parasitic species are defined as those that are morphologically similar to a particular parasitic species in all aspects other than body size, and “relict” brook lampreys are those that cannot be obviously paired with extant parasitic forms. However, molecular analyses have: (1) identified the closest extant parasitic relative to these relict species (although a few “orphan” species still remain, where identification of the closest living relative still sheds little light on the identity of the parasitic ancestor); (2) shown that the distinction between paired and relict species is sometimes unclear; and (3) demonstrated that there is also considerable variation among paired species in the degree to which they are morphologically and genetically differentiated from their parasitic ancestors. We review this “speciation continuum,” particularly in European river and brook lamprey populations where recent genetic and genomic studies show significant gene flow between these species where they co-occur (i.e., refuting assumptions of complete reproductive isolation resulting from size-assortative mating) while also showing that there are genome-level differences between the feeding types (i.e., refuting the hypothesis of phenotypic plasticity). In sympatry, European river and brook lampreys appear to be partially reproductively isolated ecotypes that nevertheless maintain distinct phenotypes, because regions of the genome involved in reproductive isolation and local adaptation resist the homogenizing effect of introgression. Interestingly, the results of analyses used to reconstruct the demographic history of divergence in this species pair are inconsistent with recent and rapid divergence in sympatry following the recent glacial retreat; rather, they support divergence in allopatry ~200,000–250,000 years ago and re-establishment of secondary contact ~90,000 years ago. Some loci have been identified that differ between the forms (e.g., the vasotocin and gonadotrophin-releasing hormone 2 precursor genes), but an understanding of the genetic basis of life history evolution in lampreys remains elusive. There appear to be strong parallels between factors that promote or constrain loss of anadromy in parasitic species (and reduction in duration of the feeding phase) and those that lead to or limit the evolution of non-parasitism (i.e., total elimination of the feeding phase). Smaller-bodied parasitic species have been far more prolific in producing non-parasitic derivatives than others; western river lamprey are already so small at maturity that “skipping” right to a non-parasitic form represents a more profitable trade-off between mortality and fecundity than freshwater parasitism. In contrast, there is a conspicuous absence of brook lamprey derivatives from the large-bodied sea, pouched, and Caspian lampreys. Our comparisons suggest that 300 mm TL (with a 10–12× reduction in fecundity) is the cut-off above which shifts to non-parasitism would not be beneficial. Therefore, we predict that Great Lakes sea lamprey is not an “intermediate” freshwater parasitic form that will give rise to a non-parasitic derivative, because complete elimination of the parasitic feeding phase would represent too large (~40×) a reduction in fecundity.

Life History Evolution in Lampreys: Alternative Migratory and Feeding Types

Approximately 6% of the freshwater living northern straight-mouth nase Pseudochondrostoma duriense in two Spanish rivers had attached post-metamorphic sea lamprey Petromyzon marinus. Minimum prey size was 16·1 cm fork length and 56·3 g mass. The condition factor of attacked P. duriense was 16% lower than that of unattacked conspecifics.

Haematophagous feeding of newly metamorphosed European sea lampreys Petromyzon marinus on strictly freshwater species.

/pdf/sexual-variation-in-biochemical-indicators-in-adults-of-sea-19t5usz34q.pdf

Sexual variation in biochemical indicators in adults of sea lamprey (Petromyzon marinus Linnaeus, 1758).

The non-native signal crayfish Pacifastacus leniusculus (Dana, 1852) has successfully been established in many catchments of Europe, causing detrimental impacts on both native flora and fauna. The aim of this paper was to report the anthropogenic introduction of P. leniusculus and its ectosymbionts (family Branchiobdellidae) in the River Tambre (NW Spain). Seventy one individuals of P. leniusculus were captured in the Barrie de la Maza reservoir in November 2016. The presence of several age classes, including young of the year individuals, and ovigerous females suggests that the population is already established and viable. Most individuals (96%) presented branchiobdellidans and 4% exhibited white spots probably caused by a virus. Melanised spots caused by the oomycete Aphanomyces astaci (Schikora, 1906) (crayfish plague) were not found in this sample. This population is expected to disperse through the River Tambre basin. The Tambre population may also be a source of individuals for new introductions in the region, where currently no P. leniusculus populations are known at a minimum radio of 150 km in straight line. Therefore, immediate management and preventive actions should be pursued to control the dispersion and growth of this population and to avoid new introductions (e.g. ban of crayfish fishing).

New data on the introduction of the invasive signal crayfish Pacifastacus leniusculus (Dana, 1852) (Crustacea, Decapoda) and ectosymbiont branchiobdellidans (Annelida, Clitellata) in NW Iberian Peninsula

/pdf/larval-habitat-of-sea-lamprey-petromyzon-marinus-linnaeus-460qjmq1lp.pdf

Larval habitat of sea lamprey Petromyzon marinus Linnaeus, 1758

/pdf/preliminary-data-on-feeding-behaviour-of-young-of-the-year-1k8kfmfajd.pdf

Preliminary data on feeding behaviour of young-of-the-year twaite shad, Alosa fallax (Lacepede, 1803), during their downstream migration in two rivers of the NW of the Iberian Peninsula

David José Nachón

Papers

Haematophagous feeding of newly metamorphosed European sea lampreys Petromyzon marinus on strictly freshwater species.

Sexual variation in biochemical indicators in adults of sea lamprey (Petromyzon marinus Linnaeus, 1758).

New data on the introduction of the invasive signal crayfish Pacifastacus leniusculus (Dana, 1852) (Crustacea, Decapoda) and ectosymbiont branchiobdellidans (Annelida, Clitellata) in NW Iberian Peninsula

Larval habitat of sea lamprey Petromyzon marinus Linnaeus, 1758

Preliminary data on feeding behaviour of young-of-the-year twaite shad, Alosa fallax (Lacepede, 1803), during their downstream migration in two rivers of the NW of the Iberian Peninsula