Lethal temperatures of ammocoetes of the Southern Hemisphere lamprey,Geotria australis Gray

Synopsis The resistance time of ammocoetes ofGeotria australis was related to the time of emergence from the substrate. The incipient lethal temperatures of animals acclimated at 5, 15 and 25° C were 27.3, 27.5 and 28.2° C respectively, the ultimate incipient lethal being 28.3° C. This value, which is similar to that of Northern Hemisphere lampreys such asLampetra planeri, almost certainly accounts for the restriction of this species to the southernmost rivers in Western Australia.     

Quantitative data on morphology and organ weights during the protracted spawning-run period of the Southern Hemisphere lamprey Geotria australis

Data are presented for a wide variety of different measurements and observations made on representatives of the lamprey Geotria australis caught during the first four months after they had left the sea in seven successive years. Comparisons have been made with the trends shown by similar data obtained from animals subsequently held in the laboratory for a number of months to provide information on the subsequent pattern of changes and the duration of the spawning run. In comparison with anadromous holarctic species, the gonads at the beginning of the upstream migration in July were very small. The eggs, which did not yet contain yolk platelets, measured only 190 μm in diameter and took until October of the following year to reach 1120 μm, which is comparable to the size of the mature eggs of other lampreys. This indicates that the spawning run of G. australis lasts for the exceptionally long period of 16 months, which is consistent with the time of appearance of young larvae. At the commencement of the spawning run, the mean lengths and weights of G. australis were approximately 655 mm and 250 g. Hepatosomic (c. 0·8%) and heart ratios (c. 0·18%) were significantly lower than those of other species. The relatively long length of the trunk, which was associated with a very high mean myomere number (78·8), helped to compensate for a small body depth and permitted the production of a large number of eggs (mean fecundity 57,943). The intestine underwent rapid atrophy immediately after the animal entered fresh water, even though the gonads were not developing rapidly at this time. Migratory movements in the river were most marked on nights when water levels were rising, the temperature lay between 12 and 14.5°C, rain was falling and extensive cloud cover or the dark phase of the moon was present.     

Basal oxygen consumption,ventilatory frequency,and heart rate during the protracted spawning run of the Southern Hemisphere lamprey Geotria australis

Summary Basal oxygen consumption, ventilatory frequency, and heart rate were recorded at four different times during the unusually protracted 15–16-month spawning run of the Southern Hemisphere lamprey Geotria australis. At 15°C, the mean basal oxygen consumption of G. australis caught immediately after they had left the sea and embarked on the spawning run (45 l · g^-1 · h^-1) was less than in young adults about to commence their marine feeding phase (64 l · g^-1 · h^-1), but greater than in large ammocoetes (26.5 l · g^-1 · h^-1). Basal oxygen consumption fell progressively during the spawning-run of to 33 l · g^-1 · h^-1 after 5 months and 25 l · g^-1 · h^-1 after 10 months, before rising to 35 l · g^-1 · h^-1 after 15 months when the animals were approaching sexual maturity. The downwards trend in basal oxygen consumption contrasts with that recorded during the spawning run of Lampetra fluviatilis. Furthermore, these values for spawning-run of G. australis are far lower than those measured at any time during the upstream migration of L. fluviatilis or during the parasitic phase of landlocked Petromyzon marinus. A low and declining metabolic rate during much of the spawning run of G. australis would facilitate the conservation of energy reserves during this very long non-feeding period. Trends shown by ventilatory frequency and heart rate essentially parallel those of basal oxygen consumption. The Q₁₀s for basal oxygen consumption, ventilatory frequency and heart rate over the temperature range 5–25°C were 1.6, 1.6, and 1.7, respectively. The trends shown by basal oxygen consumption during metamorphosis and the upstream migration did not parallel those exhibited by circulating thyroid hormones.     

Proximate body composition of the larval,metamorphosing and downstream migrant stages in the life cycle of the Southern Hemisphere lamprey,Geotria australis

Synopsis The water, total lipid, protein and ash content have been measured in larval, metamorphosing (stages 1–7) and downstream migrantGeotria australis caught in Western Australia between October 1977 and August 1979. The total lipid content of ammocoetes changed markedly with season and increased with body size. Although, unlike other species, the ammocoetes ofG. australis continue to increase in length during the latter part of larval life, the relative amount of total lipid still rose during this period, eventually reaching levels equivalent to approximately 14% of the wet body weight at the commencement of metamorphosis. During the six months between the onset of metamorphosis and the downstream migration, total lipid declined to approximately 8%. Assays for phospholipid of larval and metamorphosingG. australis indicated that changes in total lipid were almost entirely due to variations in neutral lipid. Changes in the percentage amount of total lipid were accompanied by an inverse but slightly greater amount of change in percentage water. During metamorphosis, the absolute amount of total lipid in a standard animal declined from 122 mg at stage 1 to 53 mg at stage 7, whereas water rose initially from 597 mg at stage 1 to 638 mg at stage 3, before declining to 442 mg by stage 7. Although the percentage amount of protein and ash tended to increase slightly during larval life, neither showed conspicuous seasonal changes. In both relative and absolute terms, protein declined during metamorphosis. A comparison of the data on the proximate body composition inG. australis and holarctic lampreys shows that different strategies have been employed to accumulate large amounts of fat by the end of larval life and to utilize protein during metamorphosis.     

The oral fimbriae of the lamprey Geotria australis

The frond-like fimbriae surrounding the oral disc of the lamprey, Geotria australis , have been examined in living specimens, and by using histological, histochemical and ultra-structural techniques. Approximately 57 fimbriae are present in this species, with those at the posterior end of the disc being significantly larger than those in the anterior and lateral regions. The terminal finger-like projections of the fimbriae possess a stratified epithelium composed solely of a series of rows of mucous-producing cells. Tests have shown that the mucus of the epithelial cells contains large amounts of N-acetyl neuraminic acid. Since the adjacent fimbriae are closely apposed when the lamprey is using its oral disc for suction, it is suggested that their flexible shape, mucous secretions and production of an increased surface area for attachment, help to provide a more efficient seal. Since fimbriae are present in all lampreys except those species belonging to the Mordaciidae, it is postulated that their absence in this latter family can be related to known differences in the behaviour of their adult stages.     

The Dentition and Feeding Mechanism in Adults of the Southern Hemisphere Lamprey Geotria australis Gray

Scanning electron micrographs of the teeth and sections and dissections of the head have been used to describe the functional interrelationships between the dentition and associated cartilages, muscles and ligaments in adults of the southern hemisphere lamprey Geotria australis. These studies, together with manipulation of the piston and oral disc in living specimens, elucidated the probable feeding mechanism in this species. The main cutting action appears to result from a scissoring movement brought about by the rapid interlocking of the three sharp and stout cusps of the transverse lingual lamina with large grooves on the rear face of the supraoral lamina. The movement of excised flesh back through the oral passage to the pharynx would be facilitated by the action of the pair of strongly cuspid longitudinal lingual laminae. The unique oral disc teeth of G. australis are apparently adapted to allow the disc to slide forward over the host and yet restrict any tendency to slip backwards.     

Development of the Testis During Post-metamorphic Life in the Southern Hemisphere Lamprey Geotria australis Gray

Spermatogenesis during post-metamorphic life in the anadromous parasitic lamprey Geotria australis was examined in histological sections of testes of animals collected in the field or maintained in the laboratory. The fully metamorphosed downstream migrants of G. australis possessed a very small testis in which the germ cells consisted of irregularly arranged prospermatogonia. By the end of the subsequent protracted marine trophic phase, the testis had increased in cross-sectional area by about 20 times and become organised into well-defined cysts. Since approximately 40% of these cysts possessed spermatocytes and 12% contained spermatids or early sperm, meiosis is initiated prior to the non-feeding upstream migration, which in G. australis lasts for the unusually long period of 15–16 months. The incidence of cysts with meiotic and post-meiotic stages decreased during the first 3 months of the spawning run before starting to rise during subsequent months. Spermiogenesis was never completed in any animals caught in the field during the first 9 months of the upstream migration or in those subsequently held in the laboratory up to and beyond November, the month when spawning naturally takes place. The phasing and asynchrony of spermatogenesis during post-metamorphic life in G. australis differs markedly from the situation in Northern Hemisphere lampreys.     

Distribution of Iron-Containing Granules in Lampreys,with Particular Reference to the Southern Hemisphere Species Geotria australis Gray

Perl's Prussian blue and bathophenanthroline have been used to investigate the sites where iron-containing granules are found within representatives of each of the three extant families of lampreys. Amongst the larvae, granules were present in the columnar cells of the posterior intestine in small amounts in some but not all northern hemisphere species (Petromyzonidae), and in moderate and very large amounts in the southern hemisphere families Geotriidae and Mordaciidae respectively. Granules were only found in large numbers elsewhere in the body of larvae of the Geotriidae, in which they were predominant in the adipose tissue of the nephric fold and fat column. It is suggested that these large iron deposits reflect the intake of an unusually large amount of iron, a feature which in turn could be related to the relatively high plasma iron levels and haemotocrit found in larvae of the Geotriidae. During metamorphosis, iron deposits accumulate in the liver of all species as haemoglobin is broken down.     

Oral papillae of adults of the southern hemisphere lamprey Geotria australis

The morphology, cell types, and innervation of the several small papillae (x? = 17) and two larger papillae, which together form a ring just outside the fimbriae surrounding the suctorial disc of adult Geotria australis, have been studied using various histological stains, including silver impregnation, and scanning and transmission electron microscopy. The epithelium of all papillae consists almost entirely of mucigenic cells. The multivillous and oligovillous cells, which are found elsewhere in the lamprey epidermis, were not observed, and Merkel and polyvillous cells are rare. Free nerve endings are common, however, in the basal layers of the epidermis. Unlike the small papillae, the two large papillae contain a core of skeletal muscle and a prominent layer of dermal collagen. In the submucosa of these large papillae, the nerves form a dense, compact layer that contains many large and probably sensory axons. It is suggested that the oral disc papillae of adult G. australis are encapsulated mechanosensory structures that play a role in enabling the animal to locate and attach to a suitable point on host fishes or other surfaces.     

The cardiovascular chromaffin cell system of the southern hemisphere lamprey,Geotria australis gray

This study demonstrates that the silver technique of Grimelius (Acta Soc. Med. Ups. 73:243–270, 68) is ideally suited for the study of cardiovascular chromaffin cells in lampreys. This method showed that in the Southern Hemisphere lamprey, Geotria australis, the distribution of chromaffin cells differs from that described for holarctic species. In G. australis, the chromaffin cells are found mainly in the sinus venosus, atrium, and nearby regions of the cardinal and jugular veins, and they are absent from the ventricle and conus arteriosus. The location and discreteness of the large accumulation of chromaffin cells in the lateral wall of the right posterior cardinal vein of adults resemble those of the precardiac axillary bodies of elasmobranchs. Chromaffin cells become more abundant during metamorphosis. The possible phylogenetic and functional significance of lamprey chromaffin cells is briefly discussed.     

The morphology and histology of the endocrine pancreas of the southern hemisphere lamprey, Geotria australis gray

The location and arrangement of the pancreatic endocrine tissue in larval and adult Geotria australis (Geotriidae) differ markedly from those exhibited by the comparable stages of Northern Hemisphere lampreys (Petromyzontidae). In larval Geotria australis, the main zones of islet proliferation are located laterally between the oesophagus and the inner edge of the two large intestinal diverticula unique to this species rather than dorsal and ventral to the oesophagus. In adult Geotria australis, the islet follicles are closely packed into a single discrete capsule which could be easily removed surgically, rather than into cranial, intermediate, and caudal cords. The differences in the adult can be related to a lack of involvement of the bile duct in islet formation during metamorphosis. While B cells were found in both larval and adult islet follicles, the PI acidophilic cells and argyrophilic cells, which appeared respectively at stages 3 and 4 in metamorphosis, were present in all adult stages.     

The relationship between total non-haem,ferritin and haemosiderin iron in larvae of Southern Hemisphere lampreys (Geotria australis andMordacia mordax)

Summary The major iron binding protein (IBP) of larvalM. mordax has an estimated molecular weight (354,000), subunit molecular weight (18,000) and pI (5.1) identical to those recorded previously for larvalG. australis. The IBP in larvalG. australis has also been shown to be relatively heat stable and to react immunologically with antihorse spleen ferritin. The weight of total non-haem iron in the whole body, and both the ferritin and haemosiderin iron components, increased with increasing body weight in larvalG. australis. While the concentration of ferritin iron remained similar throughout larval life, the concentration of total non-haem iron and haemosiderin iron increased rapidly in animals up to a body weight of 0.1–0.2 g, but thereafter rose only slowly throughout the rest of larval life. This implies that any iron in excess of the amount required for the maintenance of a constant ferritin concentration is converted into haemosiderin iron, and that once non-haem iron has reached a particular concentration (c. 500–600 g g^–1), the rate of iron accumulation is greatly reduced. While the larvae of bothG. australis andM. mordax had very high plasma iron levels (>19,000 g 100 ml^–1), the former had significantly greater concentrations of iron in the whole body (702vs. 267 g g^–1) and more particularly in the nephric fold (7382vs. 224 g g^–1). A greater reservoir of non-haem iron could facilitate the maintenance of the large amounts of haem and erythrocytic ferritin present in this species as a result of an exceptionally high haemoglobin concentration and red blood cell number. The greater concentration of non-haem iron in the intestine ofM. mordax than ofG. australis (1338vs. 824 g g^–1), when considered in conjunction with histological studies, indicates thatMordacia mordax eliminates a larger amount of iron during the extrusion of its intestinal columnar cells.Abbreviation IBP iron binding protein     

Retinal Amino Acid Neurochemistry of the Southern Hemisphere Lamprey,Geotria australis

Lampreys are one of the two surviving groups of the agnathan (jawless) stages in vertebrate evolution and are thus ideal candidates for elucidating the evolution of visual systems. This study investigated the retinal amino acid neurochemistry of the southern hemisphere lamprey Geotria australis during the downstream migration of the young, recently-metamorphosed juveniles to the sea and during the upstream migration of the fully-grown and sexually-maturing adults to their spawning areas. Glutamate and taurine were distributed throughout the retina, whilst GABA and glycine were confined to neurons of the inner retina matching patterns seen in most other vertebrates. Glutamine and aspartate immunoreactivity was closely matched to Müller cell morphology. Between the migratory phases, few differences were observed in the distribution of major neurotransmitters i.e. glutamate, GABA and glycine, but changes in amino acids associated with retinal metabolism i.e. glutamine and aspartate, were evident. Taurine immunoreactivity was mostly conserved between migrant stages, consistent with its role in primary cell functions such as osmoregulation. Further investigation of glutamate signalling using the probe agmatine (AGB) to map cation channel permeability revealed entry of AGB into photoreceptors and horizontal cells followed by accumulation in inner retinal neurons. Similarities in AGB profiles between upstream and downstream migrant of G. australis confirmed the conservation of glutamate neurotransmission. Finally, calcium binding proteins, calbindin and calretinin were localized to the inner retina whilst recoverin was localized to photoreceptors. Overall, conservation of major amino acid neurotransmitters and calcium-associated proteins in the lamprey retina confirms these elements as essential features of the vertebrate visual system. On the other hand, metabolic elements of the retina such as neurotransmitter precursor amino acids and Müller cells are more sensitive to environmental changes associated with migration.     

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.     

Reissner's fiber,massa caudalis and ampulla caudalis in the spinal cord of lamprey larvae (Geotria australis)

Summary The subcommissural organ (SCO), Reissner's fiber (RF) and its massa caudalis of lamprey larvae (Geotria australis) were investigated immunocytochemically by use of an antiserum raised against bovine RF as primary antibody. The affinities of RF and massa caudalis for Ricinus communis agglutinin I (RCA) with and without previous acid hydrolysis, concanavalin A (Con A), wheat-germ agglutinin (WGA), aldehyde fuchsin, and PAS reaction were also studied.SCO and massa caudalis were strongly immunoreactive, whereas RF proper was distinctly negative. RF did not react with Con A and RCA. Only the periphery of RF was WGA-positive. RCA showed affinity for RF only after acid hydrolysis. RF was homogeneously stained by the aldehyde-fuchsin and PAS-methods. At variance with RF proper, the periphery of the massa caudalis reacted with RCA without previous acid hydrolysis, but its core was WGA-positive and reacted with RCA only after hydrolysis. It is suggested that (i) RF has a coat of glycoproteins containing sialic acid as terminal residue, whereas the massa caudalis possesses a coat with galactose as terminal residue; (ii) in RF proper and the massa caudalis the spatial arrangement of glycoproteins might be different.Routine transmission electron-microscopic observations indicate that in larvae of Geotria australis an open communication exists between the ampulla caudalis and blood capillaries via large cavities or lacunae.Supported by Grant I 38259 from the Stiftung Volkswagenwerk, Federal Republic of Germany, Grant S-85-39 from the Dirección de Investigaciones, Universidad Austral de Chile, and Grant 6027 from Fondo Nacional de Desarrollo Científico y Tecnológico, Chile     

Data on the adult marine and migratory phases in the life cycle of the southern hemisphere lamprey,Geotria australis Gray

Synopsis Large numbers of the Southern Hemisphere lamprey, Geotria australis, have been found in the regurgitated food of albatrosses breeding on South Georgia. This finding suggests that this lamprey is found in large groups at sea, presumably associated with its host, and can travel very large distances from its natal streams. The length and morphology of the individuals from South Georgia, which almost certainly represent a South American stock, were compared with those of representatives of the immediately pre- and post-marine trophic stages of G. australis caught in Western Australia. No significant differences could be detected either in the number of trunk myomeres or in the number and arrangement of the teeth. The mean length of the animals (± 95% confidence limits) from South Georgia was 45.9 ± 0.90 cm compared with 10.0 ± 0.23 cm and 62.5 ± 0.85 cm in G. australis collected from Western Australia just before they had entered and returned from the sea respectively.     

Intercellular junctions in the water-blood barrier of the gill lamella in the adult lamprey (Geotria australis,Lampetra fluviatilis)

Thin sections and freeze-fracture replicas of the water-blood barrier in the gill lamellae of adult lampreys (Geotria australis, Lampetra fluviatilis) demonstrate that the occluding junctions between epithelial pavement cells differ markedly from those between endothelial pillar cells in the structure and arrangement of their strands. The zonulae occludentes between pavement cells typically consist of complex networks of 4–6 strands, the mean number of which undergoes a small but significant decline when the animal is acclimated to seawater. In comparison, the occluding junctions between pillar cells are less elaborate and may represent maculae or fasciae, rather than zonulae occludentes. They do not apparently undergo a change when the animal enters saltwater. The results indicate that the main part of the paracellular diffusion barrier to proteins and ions is located in the epithelium rather than the endothelium. Communicating (gap) junctions are present between adjacent pavement cells, between pavement and basal cells and between pillar cells. These findings suggest that the epithelial cells and the pillar cells in the water-blood barrier of lampreys both form functional syncytia. The results are discussed in the context of ion-transporting epithelia in other aquatic vertebrates.This paper is dedicated to Professor H. Leonhardt on the occasion of his 75^th birthday     

Changes in the amount of nonhaem iron in the plasma, whole body, and selected organs during the postlarval life of the lamprey Geotria australis

The concentration of plasma nonhaem iron and the concentration and weight of all nonhaem iron in the whole body and selected organs, together with its partitioning into ferritin and haemosiderin iron, have been measured during the metamorphosis and upstream spawning migration of the Southern Hemisphere lamprey Geotria australis. Some nonhaem iron was lost from the animal during metamorphosis. However, the concentration and weight of nonhaem iron in the liver rose sharply at this time, following its release from important storage sites in adipose tissue and the degradation of larval haemoglobins. The nephric fold of larval and metamorphosing stages contained over 40% of all nonhaem iron in the body at the commencement of metamorphosis. This was predominantly in the form of haemosiderin. While the rise in liver iron during the transition from larva to adult primarily reflected an increase in the weight of ferritin iron, the amount of iron stored as haemosiderin rose conspicuously towards the end of metamorphosis. The rise in ferritin iron in the liver was accompanied by a decrease in ferritin iron in the plasma, which implies that changes in the liver during metamorphosis result in a greater filtering of circulating ferritin. Such a process would account for the very much lower plasma nonhaem iron concentrations which characterise later adult stages. The weight of nonhaem iron increased markedly in the liver and adult opisthonephros and in the whole animal during the nontrophic upstream spawning migration. This was primarily due to a marked rise in ferritin which in turn could be related to the degradation of adult haemoglobins.(ABSTRACT TRUNCATED AT 250 WORDS)     

The Development of Teeth and Associated Feeding Structures During the Metamorphosis of the Lamprey,Geotria australis

The pattern of development of the teeth, laminae, piston, muscles, cartilages and fimbriae associated with the suctorial disc of lampreys has been investigated histologically during the seven stages of metamorphosis in the Southern Hemisphere species, Geotria australis. The cirrhi-bearing hood of ammocoetes and the earliest stage of metamorphosis (S1) were indistinguishable. In stages S2, S3, S4, these cirrhi regressed and the supraoral lamina, piston and infraoral lamina primordial regions began to differentiate. The fifth stage (S5) was characterised by an elaboration of the annular cartilage and disc musculature, deposition of the tectal cartilage, initiation of tooth development, formation of oral fimbriae, and eruption of the keratin cone of the transverse lingual lamina. Subsequently (S6), the keratin cusps of the supraoral and infraoral laminae became exposed at the surface, and distinct retractor and protractor muscles formed around the lingual cartilage. In the latter part of the terminal stage in metamorphosis (S7), just prior to the time when the animal migrates downstream, the primary tooth cones and the keratin cusp of the longitudinal lingual laminae began breaking through the epithelial surface of the disc.