Expression of three GnRH receptors in specific tissues in male and female sea lampreys Petromyzon marinus at three distinct life stages

Two recently cloned gonadotropin-releasing hormone (GnRH) receptors (lamprey GnRH-R-2 and lamprey GnRH-R-3) along with lamprey (l) GnRH-R-1 were shown to share similar structural features and amino acid motifs common to other vertebrate receptors. Here we report on our findings of RNA expression of these three GnRH receptors in the three major life stages (larval, parasitic, and adult phases) of the sea lamprey, Petromyzon marinus, a basal vertebrate. For each stage, we examined the expression of messenger RNA encoding the receptors in the brain, pituitary, gonad, heart, muscle, liver, eye, intestine, kidney, skin, thyroid, gill, and endostyle by RT-PCR. In adult lampreys, the spatial expression of the three receptors in the brain and pituitary was investigated by in situ hybridization. In general, the receptors were more widely expressed in adult tissues as compared to parasitic-phase tissues and least widely expressed in the larval tissues. There were noted differences in male and female lampreys in the adult and parasitic phases for all three receptors. The data showed the presence of all three receptor transcripts in brain tissues for adult and parasitic phases and all three receptor transcripts were expressed in the adult pituitaries, but not in the parasitic pituitaries. However, in the larval phase, only lGnRH-R-1 was expressed in the larval brain and pituitary. In situ hybridization revealed that lGnRH-R-2 and -3 were expressed in the pineal tissue of adult female lampreys while lGnRH-R-1 was expressed in the pineal in adult male lampreys, all restricted to the pineal pellucida. In summary, these data provide an initial comparative analysis of expression of three lamprey GnRH receptors suggesting differential regulation within males and females at three different life/reproductive stages

Demography of sea lamprey (Petromyzon marinus) ammocoete populations in relation to potential spawning-migration obstructions

Copyright © 2017 John Wiley & Sons, Ltd. Recent advances in the understanding of lamprey migrations have led to concerns over the impacts of obstructions on the demography of many species. This study investigated sea lamprey (Petromyzon marinus) larvae (ammocoetes) in two adjacent but contrasting rivers, both designated Special Areas of Conservation under the EC Habitats Directive (92/43/EEC), one (the River Wye) with a small number of potential migration obstructions in its upper reaches and one (the River Usk) with obstacles along its course. The geographical distributions, densities and age structures of the ammocoete populations were examined in relation to the locations of potential obstructions to the spawning migrations of anadromous adults. A minimum of three age classes was recorded as far as 200 km upstream of the mouth of the River Wye (93% of the length of the mainstem), demonstrating that adults regularly migrate to the upper reaches of the catchment (downstream of a natural waterfall). By contrast, sea lamprey ammocoetes appeared to be absent (in suitable habitat) from 20 km (17%) of the River Usk, and there was a reduction in density, prevalence and the number of age classes upstream of two putative spawning-migration obstructions. This study highlights some of the potential impacts of habitat fragmentation by obstructions on the spawning migrations of anadromous species, as inferred from ammocoete demography. When used in combination to compare contiguous reaches, ammocoete densities, prevalence and age structure may be a useful indicator of which structures are likely to be important migration obstructions, and where further studies or mitigation efforts should be focused. It is likely that passage past some obstructions is enhanced if high river levels occur during the spawning migration, but there is a need to facilitate passage during all conditions, to improve access to under-exploited spawning and nursery areas

Rapid Metabolic Recovery Following Vigorous Exercise in Burrow-Dwelling Larval Sea Lampreys (\u3cem\u3ePetromyzon marinus\u3c/em\u3e)

Although the majority of the sea lamprey’s (Petromyzon marinus) life cycle is spent as a burrow-dwelling larva, or ammocoete, surprisingly little is known about intermediary metabolism in this stage of the lamprey’s life history. In this study, larval sea lampreys (ammocoetes) were vigorously exercised for 5 min, and their patterns of metabolic fuel depletion and replenishment and oxygen consumption, along with measurements of net whole-body acid and ion movements, were followed during a 4–24-h postexercise recovery period. Exercise led to initial five- to sixfold increases in postexercise oxygen consumption, which remained significantly elevated by 1.5–2.0 times for the next 3 h. Exercise also led to initial 55% drops in whole-body phosphocreatine, which was restored by 0.5 h, but no significant changes in whole-body adenosine triphosphate were observed. Whole-body glycogen concentrations dropped by 70% immediately following exercise and were accompanied by a simultaneous ninefold increase in lactate. Glycogen and lactate were quickly restored to resting levels after 0.5 and 2.0 h, respectively. The presence of an associated metabolic acidosis was supported by very high rates of metabolic acid excretion, which approached 1,000 nmol g-1 during the first 2 h of postexercise recovery. Exercise-induced ion imbalances were also rapidly alleviated, as initially high rates of net Na+ and Cl- loss (—1,200 nmol g-1h-1 and —1,800 nmol g-1h-1 respectively) were corrected within 1–2 h. Although larval sea lampreys spend most of their time burrowed, they are adept at performing and recovering from vigorous anaerobic exercise. Such attributes could be important when these animals are vigorously swimming or burrowing as they evade predators or forage

Shifting Patterns of Nitrogen Excretion and Amino Acid Catabolism Capacity during the Life Cycle of the Sea Lamprey (\u3cem\u3ePetromyzon mariunus\u3c/em\u3e)

The jawless fish, the sea lamprey (Petromyzon marinus), spends part of its life as a burrow-dwelling, suspension-feeding larva (ammocoete) before undergoing a metamorphosis into a free swimming, parasitic juvenile that feeds on the blood of fishes. We predicted that animals in this juvenile, parasitic stage have a great capacity for catabolizing amino acids when large quantities of protein-rich blood are ingested. The sixfold to 20-fold greater ammonia excretion rates (JAmm) in postmetamorphic (nonfeeding) and parasitic lampreys compared with ammocoetes suggested that basal rates of amino acid catabolism increased following metamorphosis. This was likely due to a greater basal amino acid catabolizing capacity in which there was a sixfold higher hepatic glutamate dehydrogenase (GDH) activity in parasitic lampreys compared with ammocoetes. Immunoblotting also revealed that GDH quantity was 10-fold and threefold greater in parasitic lampreys than in ammocoetes and upstream migrant lampreys, respectively. Higher hepatic alanine and aspartate aminotransferase activities in the parasitic lampreys also suggested an enhanced amino acid catabolizing capacity in this life stage. In contrast to parasitic lampreys, the twofold larger free amino acid pool in the muscle of upstream migrant lampreys confirmed that this period of natural starvation is accompanied by a prominent proteolysis. Carbamoyl phosphate synthetase III was detected at low levels in the liver of parasitic and upstream migrant lampreys, but there was no evidence of extrahepatic (muscle, intestine) urea production via the ornithine urea cycle. However, detection of arginase activity and high concentrations of arginine in the liver at all life stages examined infers that arginine hydrolysis is an important source of urea. We conclude that metamorphosis is accompanied by a metabolic reorganization that increases the capacity of parasitic sea lampreys to catabolize intermittently large amino acid loads arising from the ingestion of protein rich blood from their prey/hosts. The subsequent generation of energy-rich carbon skeletons can then be oxidized or retained for glycogen and fatty acid synthesis, which are essential fuels for the upstream migratory and spawning phases of the sea lamprey’s life cycle

Population ecology of the sea lamprey (Petromyzon marinus) as an invasive species in the Laurentian Great Lakes and an imperiled species in Europe

The sea lamprey Petromyzon marinus (Linnaeus) is both an invasive non-native species in the Laurentian Great Lakes of North America and an imperiled species in much of its native range in North America and Europe. To compare and contrast how understanding of population ecology is useful for control programs in the Great Lakes and restoration programs in Europe, we review current understanding of the population ecology of the sea lamprey in its native and introduced range. Some attributes of sea lamprey population ecology are particularly useful for both control programs in the Great Lakes and restoration programs in the native range. First, traps within fish ladders are beneficial for removing sea lampreys in Great Lakes streams and passing sea lampreys in the native range. Second, attractants and repellants are suitable for luring sea lampreys into traps for control in the Great Lakes and guiding sea lamprey passage for conservation in the native range. Third, assessment methods used for targeting sea lamprey control in the Great Lakes are useful for targeting habitat protection in the native range. Last, assessment methods used to quantify numbers of all life stages of sea lampreys would be appropriate for measuring success of control in the Great Lakes and success of conservation in the native range

The Functional, Ecological, and Evolutionary Morphology of Sea Lampreys (Petromyzon marinus)

Lampreys (Petromyzontiformes) are jawless vertebrates with an evolutionary history lasting at least 360 million years and are often used in comparisons with jawed vertebrates because some of their morphological aspects, such as the segmented trunk musculature with curved myosepta and a non-mineralized skeleton fibrous skeleton, are thought to resemble the condition of early vertebrates before the evolution of jaws. Although earlier authors studied the morphology of the skeleto-muscular system of the trunk of lampreys, their studies are not detailed and complete enough to allow a functional and biomechanical analysis that is needed as a basis for modeling the mechanics of lamprey locomotion and for understanding the causal roles played by the anatomical structures within the trunk. Questions remain, such as what is the architecture of the trunk fibroskeleton, and how does it function with the musculature to bend the trunk? This dissertation studied the functional, ecological and evolutionary morphology of the trunk of Sea Lampreys (Petromyzon marinus) as well as its relevance in understanding the environmental history of landlocked lamprey populations. Functional morphology revealed that the fibroskeleton of the trunk is a self-supporting concatenated system of fibers, which creates a scaffold for the musculature and transmits forces to bend the trunk during swimming. Ecological morphology demonstrated the adaptive advantage of the fibroskeleton’s architecture, which enables the movements that are performed during migration and spawning and gives lampreys the capacity to colonize upstream realms. These results help explain the evolutionary morphology of lampreys, which likely originated in freshwater as algal feeders and evolved into parasites after going through an intermediary scavenging stage. When these insights are applied to the evolution of landlocked Sea Lampreys, it becomes evident that their entry into freshwater lakes occurred as soon as they were able to reach them and that populations likely became established in Lake Ontario, Lake Champlain, and the Finger Lakes thousands of years ago. This insight undermines the current status of landlocked Sea Lampreys as invasive species in these lakes and the case for their eradication. Hence, this dissertation provides a comprehensive and integrative analysis of lamprey biology from their anatomy to environmental policy

Sea Lamprey Petromyzon marinus Biology and Management Across Their Native and Invasive Ranges: Promoting Conservation by Knowledge Transfer

The anadromous sea lamprey Petromyzon marinus native range extends across the Northern Atlantic and includes much of Europe. Their complex lifecycle, involving freshwater spawning, juveniles (ammocoetes) that remain in freshwater for up to eight years, and adults migrating to sea before returning to reproduce, means native populations in Europe are threatened by multiple stressors, especially migration blockages and habitat loss. This has resulted in population declines across their European range, despite their ecological, evolutionary, and economic significance. Information on their population demography and long-term patterns are also scarce, with focus primarily on their ammocoete freshwater phase. This is inhibiting the development of biological reference points for utilization in population monitoring programs. In the Great Lakes of North America, however, P. marinus is invasive and the high damage caused to commercial fisheries resulted in their populations being controlled through a long-term, multi-method and integrated research and management approach over the last 40 years, with the development and application of a range of novel methods. Successful knowledge transfer to Europe could therefore facilitate the monitoring of threatened populations and develop new conservation actions, including modifying migration blockages to facilitate passage, implementing adult trapping programs, and applying pheromone treatments to manipulate adult movements and behaviors. This reveals the potential utility of using invasive fish populations to inform conservation practices in native ranges, and how pheromone research could further enhance fish conservation and monitoring

Synergizing basic and applied scientific approaches to help understand lamprey biology and support management actions

Lampreys (Petromyzontiformes) are a key component of freshwater ecosystems throughout temperate parts of the world. Of the 44 described species of lamprey, the sea lamprey (Petromyzon marinus) is certainly the most commonly recognized. This species has expanded its range from the Atlantic Ocean basin where it is of conservation concern in North America and Europe into the Laurentian Great Lakes where it is subject to a large-scale international control program. Many other species of lamprey are imperiled and require management intervention to ensure their persistence. These management efforts range from routine assessment and monitoring to active or proposed restoration plans where they have been extirpated. Regardless of whether the goal is to control or conserve a given lamprey population, an understanding of their basic biology is paramount when generating and executing management plans. Here, we take a broad look across core aspects of biology (survival, foraging, and reproduction) that encompass challenges and opportunities in regard to future science-based management of lampreys. We attempt to synergize basic and applied research to highlight where these findings are most applicable to solving management problems and reveal knowledge gaps. We conclude by suggesting future research avenues and questions aimed to stimulate progress in both basic and applied lamprey research