15Alpha-hydroxyprogesterone in male sea lampreys, Petromyzon marinus L

There is growing evidence that sea lampreys, Petromyzon marinus L., produce gonadal steroids differing from those of other vertebrates by possessing an additional hydroxyl group at the C15 position. Here we demonstrate that sea lamprey testes produce 15alpha-hydroxyprogesterone (15alpha-P) in vitro when incubated with tritiated progesterone, that 15alpha-P is present in the plasma of sea lampreys, and that plasma concentrations of immunoreactive (ir) 15alpha-P rise dramatically in response to injections of gonadotropin-releasing hormone (GnRH). The identity of the tritiated 15alpha-P produced in vitro was confirmed by co-elution with standard 15alpha-P on high performance liquid chromatography, co-elution with standard and acetylated 15alpha-P on thin layer chromatography, and specific binding to antibodies raised against standard 15alpha-P. The in vitro conversion was used to produce tritiated 15alpha-P label for a radioimmunoassay (RIA), which is able to detect 15alpha-P in amounts as low as 2 pg per tube. The RIA has been used to measure the plasma concentrations of 15alpha-P in males given two serial injections, 24 h apart, of either lamprey GnRH I or GnRH III (50, 100, or 200 microg/kg) or saline control, with plasma being sampled 8 and 24 h after the second injection. Plasma concentrations of ir-15alpha-P rose from < 1 to 36 ng/ml (mean of all treatments) 8 h after injection and declined within 24 h. This is the first time that an RIA has detected such high steroid concentrations in lampreys. This finding is suggestive of a role for 15alpha-P in control of reproduction in the sea lamprey.     

Distribution of ferric iron in larval lampreys, Petromyzon marinus L

The distribution and abundance of ferric iron in larval lampreys (Petromyzon marinus L.) were investigated using light microscopy and the Prussian blue stain. Animals from various watersheds contained different concentrations of iron, although the sites of deposition were the same for all animals. A major portion of iron is within adipose tissue, while the liver, and cartilage contain predominantly low to trace amounts of iron, respectively. Iron is associated with fibrous connective tissue in several places in the body, and this association may have particular significance in the inner ear. Iron is also located in cells of the meninges. The presence of iron in the epithelial cells of the posterior intestine may reflect elimination of the metal through the extrusion of iron-loaded cells into the intestinal lumen. Iron within mucous cells of the epidermis, suggest elimination of iron during mucous secretion. Iron-loaded cells of bipolar shape are also present in the epidermis, but are particularly prominent around the branchiopore. Low concentrations of iron are observed within in melanin-containing macrophages (melano-macrophages) in regions of iron absorption, erythrophagocytosis, and haemopoiesis. High levels of iron in the epithelia and lumina of pronephric tubules are concomitant with degeneration of this organ. These data are evidence of the wide spread distribution of iron in lamprey tissues and additional evidence for the potential value of lampreys for the study of iron metabolism in vertebrates.     

Glycoconjugate profiles of adrenocorticotropic and melanotropic cells in the pituitary of adult sea lampreys (Petromyzon marinus): a lectin histochemical study

In the lamprey, adrenocorticotropin (ACTH) and melanotropins (MSHs) are produced from two distinct precursors, proopiocortin (POC) and proopiomelanotropin (POM). Both POC and POM have been suggested to be glycoproteins. The present study aimed to demonstrate glycoconjugates in ACTH and MSH cells in the pituitary of adult sea lampreys (Petromyzon marinus) by means of a lectin histochemistry. A total of 19 kinds of lectins were tested. ACTH cells were distributed in both the rostral pars distalis and the proximal pars distalis, and were stained positively with N-acetylglucosamine binding lectins (i.e., succinylated wheat germ agglutinin), N-acetylgalactosamine binding lectins (i.e., soybean agglutinin), D-mannose binding lectins (i.e., Lens culinaris agglutinin), and D-galactose binding lectins (i.e., Erythrina cristagall lectin). MSH cells were distributed in the pars intermedia, and were stained with N-acetylgalactosamine binding lectins (i.e., Dolichos biflorus agglutinin), D-mannose binding lectin (Pisum sativum agglutinin) and D-galactose binding lectins (i.e., peanut agglutinin). These results suggested that ACTH and MSH cells produce different types of glycoconjugates which may be attributed to the difference in glycoconjugate moieties between the precursor proteins, POC and POM.     

Fine structure and immunocytochemistry of cells within the endocrine pancreas of larval and adult sea lampreys, Petromyzon marinus L

Immunocytochemistry with protein A-gold and routine electron microscopy were used to identify cell types within the endocrine pancreas of larvae, juvenile adults, and upstream-migrant adults of the sea lamprey, Petromyzon marinus. The larval pancreatic islets are composed only of insulin-immunoreactive B-cells, which are uniform in their fine structure. The cranial and caudal pancreatic tissue in both adult periods contains three cell types: B-cells, somatostatin-immunoreactive D-cells, and a third cell type of unknown content. No glucagon-immunoreactive cells are present in lampreys, but B- and D-cells exist in equal numbers in the pancreatic tissue of adults. The B-cells of adults have a fine structure similar to those in larvae. D-cells have secretory granules that are distinctly different from those both in B-cells and in the third cell type. Although B- and D-cells in lamprey pancreatic tissues have a basic morphological similarity to these cells in other vertebrates, their granules are generally of smaller dimensions. The inclusion of granules within large pleomorphic bodies in many D-cells indicates that granule turnover is common. Immunocytochemistry will be a useful tool for showing the relationship between the cells in the degenerating bile ducts and those of the developing adult pancreas.     

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.     

Differences in the fatty acid composition of larvae and metamorphosing sea lampreys, Petromyzon marinus

This study was designed to evaluate biochemical changes in the fatty acid (FA) compositions of selected lipid depot (kidney and liver) and absorption (intestine) organs in larvae and metamorphosing sea lamprey, Petromyzon marinus. Palmitic or stearic acids were generally the predominant saturated fatty acids (SFA) before and during metamorphosis, but the greatest proportion of myristic acid occurred in renal triacylglycerol (TG). Monoenes, dienes, and polyenes consist mainly of 16:1, 18:1, and 20:1, 18:2 and 20:2omega6, and 18:4omega3, respectively. Alterations in these predominant fatty acids occurred during lamprey metamorphosis, but depended on tissue, lipid class, and developmental status. During metamorphosis, kidney TG and phospholipid (PL) classes tended to mobilize SFA and enhance the fatty acid unsaturation, as indicated by increased unsaturated/saturated ratio, unsaturation index (USI), and total mean chain length (MCL). There was a tendency to increase saturation in the fatty acids of liver TG and PL classes and intestine TG, FA and monoacylglycerol (MG) classes, but to increase unsaturation in the fatty acids of liver cholesteryl ester (CE), FA and MG classes and intestine PL and CE classes from larva or stage 3 to stage 7. Increased polyunsaturated fatty acids in kidney TG and PL from larvae to stage 5 transformers and intestine PL and CE from stage 3 to stage 7 transformers may reflect an osmoregulatory pre-adaptation. The presence of branched-chain SFA (BCSFA) and the odd number of fatty acids (ONFA) indicated a significant role of detritivores in the benthic larvae. Decreased abundance of BCSFA, ONFA, and 18:2 dienes occurred in the transformed intestine TG as non-trophic metamorphosis proceeded. These data suggest that sea lamprey metamorphosis may proceed in a habitat, dietary, osmoregulatory, energetic, and developmental pre-adaptation of fatty acid composition from benthic filter-feeding larvae to pelagic parasitic juveniles.     

Distribution of55Fe in juvenile adult lampreys,Petromyzon marinus L., following oral intubation of the isotope

Summary The capacity of a sanguivorous lamprey,Petromyzon marinus L., to deal with ingested iron was studied over time using autoradiography and scintillation counting of solubilized tissue samples after intubation of the oesophagus with a single dose of⁵⁵ferrous citrate. A highly efficient mechanism for absorption in the anterior intestine was recognized with 17% of the intubated radioactivity absorbed into the body after only 5 min, 66% by 3 h, and almost 80% by 21 h. Iron concentration in the epithelial cells of the anterior intestine may be a factor in restricting iron absorption during spontaneous feeding. A decline in total body radioactivity over the 15 days following iron intubation probably results from transport of the metal in the blood and release of radioiron from the mucous cells of the posterior intestine. The kidneys appear to play a smaller but still significant role in iron loss. Gradual increases in radioiron concentration (cpm g^–1 wet weight) and percent of total body radioactivity occur in the liver (2 to 26%), carcass (14 to 37%), and integument (4 to 12%) during the course of the experiment, indicating that these are the chief sites of iron storage during times of metal excess. However, eventually integument may also be a site of iron excretion. Significant fluctuations in radioiron concentration (cpm ml^–1) in whole blood during the 15 day period can be correlated with transport of the metal to sites of storage and excretion, and maybe with incorporation into haemoglobin and with erythropoietic activity. Feeding adult lampreys represent a valuable system, with both general and unique characters, for studying iron metabolism in vertebrates.     

Relationship of density to growth and metamorphosis of caged larval sea lampreys, Petromyzon marinus Linnaeus, in Michigan streams

Larval sea lampreys, Petromyzon marinus , of the 1976 year class were studied between May 1977 and October 1981 in five Michigan streams to determine the relationship of density to growth and metamorphosis. Two cages were placed in each stream; one cage contained 25 larvae (low density group) and the other 75 larvae (high density group). Changes in body length, as an indicator of growth, were monitored in all streams from age I to V. Mean lengths ranged from 25 to 55 mm at the beginning of the study and from 102 to 158 mm at the end. Some ammocoetes attained lengths greater than 160 mm. Growth was related mainly to density; crowding affected growth from age I to metamorphosis. Mean increases of total length ranged from 90 to 128 mm among low-density groups and from 54 to 97 mm among high-density groups. Growth was typically greater in the cage with fewer lampreys in each stream. Most growth occurred from May to October when stream temperatures were highest. In two streams in which cages were not vandalized, 96% and 92% of the lampreys in the low-density groups and 68% and 52% in the high-density groups survived to age V. Metamorphosis occurred at age V in low-density groups. Five lampreys (2.4%; range, 133–145 mm long) metamorphosed among the 207 that survived until completion of the study.     

Male sea lampreys,Petromyzon marinus L., excrete a sex pheromone from gill epithelia

During the period when they are producing sperm, male sea lampreys (Petromyzon marinus L.) release a sex pheromone 7alpha, 12alpha, 24-trihydroxy-5alpha-cholan-3-one-24-sulfate (3 keto-petromyzonol sulfate, 3ketoPZS) that induces search and preference behaviors in ovulating females. In this study, we conducted a series of experiments to demonstrate that release of this pheromone into water takes place exclusively through the gills. In a behavioral maze, water conditioned with the anterior region of spermiating males induced an increase of search and preference behaviors in ovulating females. Similar behavior was not elicited by water conditioned by the posterior region. The anterior region washings and whole-body washings from spermiating males also elicited large and virtually identical electro-olfactogram responses from female sea lampreys, while the posterior washings produced negligible responses. Further, mass spectrometry and immunoassay confirmed that virtually all the 3ketoPZS released into water was through the gills. Immunocytochemistry revealed some gill epithelial cells and hepatocytes from spermiating males contained dense immunoreactive 3ketoPZS, but not those from prespermiating males. These results demonstrate that 3ketoPZS is released through the gill epithelia and suggest that this pheromone or its precursor may be produced in the liver.     

Anadromous sea lampreys (Petromyzon marinus) are ecosystem engineers in a spawning tributary

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Variable effects of goitrogens in inducing precocious metamorphosis in sea lampreys (Petromyzon marinus)

The ability of different goitrogens (anti-thyroid agents) to induce precocious metamorphosis in larval sea lampreys (Petromyzon marinus) was assessed in four separate experiments. Two of these goitrogens (propylthiouracil [PTU] and methimazole [MMI]) are inhibitors of thyroid peroxidase-catalyzed iodination, and three (potassium perchlorate [KClO(4)], potassium thiocyanate [KSCN], and sodium perchlorate [NaClO(4)]) are anionic competitors of iodide uptake. Because, theoretically, all of these goitrogens prevent thyroid hormone (TH) synthesis, we also measured their influence on serum concentrations of thyroxine and triiodothyronine. All goitrogens except PTU significantly lowered serum TH concentrations and induced metamorphosis in some larvae. The incidence of metamorphosis appeared to be correlated with these lowered TH concentrations in that KClO(4), NaClO(4), and MMI treatments resulted in the lowest serum TH concentrations and the highest incidence of metamorphosis in sea lampreys. Moreover, fewer larvae metamorphosed in the KSCN and low-KClO(4) treatment groups and their serum TH concentrations tended to be greater than the values in the aforementioned groups. MMI treatment at the concentrations used (0.087 and 0.87 mM) was toxic to 55% of the exposed sea lampreys within 6 weeks. The potassium ion administered as KCl did not alter serum TH concentrations or induce metamorphosis. On the basis of the results of these experiments, we have made the following conclusions: (i) In general, most goitrogens other than PTU can induce metamorphosis in larval sea lampreys, and this induction is coincident with a decline in serum TH concentrations. (ii) The method by which a goitrogen prevents TH synthesis is not directly relevant to the induction of metamorphosis. (iii) PTU has variable effects on TH synthesis and metamorphosis among lamprey species. (iv) Unlike in protochordates, potassium ions do not induce metamorphosis in sea lampreys and are not a factor in the stimulation of this event.     

Importance of the olfactory sense to migratory sea lampreys Petromyzon marinus seeking riverine spawning habitat

This study tested the hypothesis that the sea lamprey Petromyzon marinus, a diadromous species of fish, relies on innately discerned odours, including pheromones, to locate riverine spawning habitat. Migratory, sexually immature P. marinus were captured as they entered streams flowing into the Great Lakes, and their olfactory systems were occluded or not by injecting either innocuous dental impression material or a saline control into their nasopores. Animals were then released back into lakes or streams and their recapture rates in stream traps noted. When released into Lake Huron, P. marinus with intact (functional) olfactory systems were very successful in locating rivers (recapture rates ranged up to 65%), while animals with occluded nasopores were virtually unable to do so and had recapture rates five to 20 times lower than intact animals. With few exceptions, intact fish entered the stream closest to their release point within a few days, irrespective of where they had been originally captured; their ability to locate streams is apparently innate and well developed. In contrast, when released within streams, both intact and occluded P. marinus successfully swam upstream to traps for several days although the ability of the former exceeded that of the latter after this period. Migratory P. marinus rely heavily on olfactory cues, of which a larval pheromone is presumably one, to locate river mouths and to a lesser extent to promote upstream movement within rivers.     

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

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.     

Feeding of sea lampreys Petromyzon marinus on minke whales Balaenoptera acutorostrata in the St Lawrence Estuary, Canada

Sea lampreys Petromyzon marinus were observed on 109 occasions on 47 individual minke whales Balaenoptera acutorostrata. Bloody lesions could be identified as previous attachment sites, indicating P. marinus feeding on B. acutorostrata blood.     

Rapid metabolic recovery following vigorous exercise in burrow-dwelling larval sea lampreys (Petromyzon marinus)

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(-1) h(-1) and -1,800 nmol g(-1) h(-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.     

Iron loading in the livers of metamorphosing lampreys,Petromyzon marinus L.

Iron loading of hepatocytes was followed through the stages (1-7) of metamorphosis in lamprey (Petromyzon marinus L.) using light- and electron-microscopic histochemistry. Iron is present in ferric and ferrous forms in the hepatocytes of larval lampreys in levels that can only be detected in the electron microscope. During the initial stages (1-3) of metamorphosis iron begins to increase in the cytoplasmic matrix and in dense bodies but it is not apparent in the light microscope until stage 4. The increased accumulation of iron through the subsequent stages (5-7) of metamorphosis coincides with the advanced degeneration and ultimate disappearance of bile canaliculi and bile ducts. The absence of a bile canaliculus is concurrent with the beginning of staining of lateral cell borders for ferrous iron and with intense concentrations of ferric iron throughout the cytoplasmic matrix and within cytoplasmic dense bodies. By the end of metamorphosis the hepatocytes resemble iron-loaded hepatocytes in pathological and experimentally induced situations in other vertebrates. The iron loading of hepatocytes during metamorphosis is discussed with respect to both the concomitant atresia of the biliary tree and alteration of several aspects of blood morphology and chemistry. Since iron loading occurs synchronously in the hepatocytes of a given population of metamorphosing lampreys, this organism should prove to be a useful experimental system for investigation on cellular mechanisms of iron loading in vertebrates.     

Downstream migration and hematophagous feeding of newly metamorphosed sea lampreys (Petromyzon marinus Linnaeus, 1758)

The metamorphosis of sea lamprey (Petromyzon marinus Linnaeus, 1758) allows young postmetamorphic individuals to migrate to the sea and start the hematophagous feeding. However, the information about this phase is very limited, especially for European populations. Herein, we provide for the first time a comprehensive study on the phenology of downstream migration, the timing and location of first feeding and the prey species in the River Ulla and its estuary (NW Spain). Results show that downstream migration occurs between October and May with a peak in March. At least for a part of the postmetamorphic lampreys this migration stops for several months when they reach the estuary, where lampreys find shelter and abundant food, before moving to coastal waters. Hematophagous feeding in the estuary allows postmetamorphics to increase their total length and weight exponentially. Our results also suggest that part of the postmetamorphics (10–30%) start the hematophagous feeding in the river, with a special affinity for anadromous species, probably because of their larger size.     

The hemoglobin of the sea lamprey,Petromyzon marinus

The blood hemoglobin of the sea lamprey presents a curious mixture of primitive and highly specialized properties. Like muscle hemoglobin, it has a molecular weight of about 17,000, and apparently contains a single heme. Its isoelectric point is like that of a typical invertebrate hemoglobin. Its amino acid composition is partly characteristic of invertebrate) partly of vertebrate hemoglobins (Pedersen; Roche and Fontaine). In the present experiments, the oxygen equilibrium curve of this pigment was measured at several pH's. As expected, it is a rectangular hyperbola, the first such function to be observed in a vertebrate blood hemoglobin. Other hemoglobins known to possess this type of oxygen dissociation curve—those of vertebrate muscle, the worm Nippostrongylus, and the bot-fly larva—appear to serve primarily the function of oxygen storage rather than transport. Lamprey hemoglobin on the contrary is an efficient oxygen-transporting agent. It achieves this status by having, unlike muscle hemoglobin, a relatively low oxygen affinity, and a very large Bohr effect. In these properties it rivals the most effective vertebrate blood hemoglobins.