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Aspects of feeding and digestion in the southern hemisphere lamprey Geotria Australis Gray: A comprehensive study

Hilliard, Robert William (1987) Aspects of feeding and digestion in the southern hemisphere lamprey Geotria Australis Gray: A comprehensive study. PhD thesis, Murdoch University.

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The dentition, adult feeding mechanism, pancreatic tissue and intestine have been studied in the anadromous parasitic lamprey, Geotria australis (Geotriidae; Petrorryzoniformes). For coirparative purposes, the feeding structures of parasitic adults representing the two other families of extant lampreys (Petromyzontidae and Mordaciidae) have been examined, as have the pancreas of nordacia mordax and intestine of Lampetra spp. Wherever possible, the results of these studies on the feeding biology of lampreys are compared with those reported elsewhere. Conclusions drawn from these conparisons are used to elucidate phylogenetic relationships among the contenporary petromyzontiforms.

The unique oral disc teeth of G.australis appear well adapted to allow the oral disc to slide forwards over the surface of prey, yet restrict any tendency for the disc to slip backwards. The main cutting action results 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 results of this study have elucidated the feeding mechanism of G.australis, and support the view that this species removes considerable amounts of flesh rather than only blood from its prey.

The dentition of parasitic lanpreys representing the six genera of holarctic lanpreys (Petromyzontidae) and the other monogeneric Southern Hemisphere family (Mordaciidae) has also been studied. Attention was paid to coirparing the divergent dentitional characters, the locations of attack and the size of the oral disc and buccal glands of the blood-feeding Petromyzon marinus and those of the flesh-feeding Lampetra fluviatilis and Lanpetra ayresii. Conclusions drawn from these comparisons have been used to make suggestions regarding the feeding biology of those species for which less comprehensive data are available. It is also concluded that (a) blood-feeding preceded flesh-feeding in the modern lampreys, (b) endemic freshwater parasitic species typically ingest blood, (c) the ability to feed on flesh developed in populations which had access to estuarine and marine hosts. and (d) pre-Tertiary forms resembling contemporary Ichthyomyzon unicuspsis could have independently given rise to both genera of Southern Hemisphere lampreys.

The morphology of the pancreatic tissue has been examined in larval, metamorphosing and adult representatives of G.australis and in large larvae and recently metamorphosed adults of another Australian parasitic lamprey, M.mordax. The location of both the larval and adult pancreatic endocrine (islet) cells in both of these species differs markedly from that in comparable stages of holarctic lampreys. In larval G.australis, the main zone of islet cell proliferation is located laterally between the oesophagus and the inner edge of two large intestinal diverticula unique to this species, rather than dorsal and ventral to the oesophagus. The adult islet follicles of G.australis are packed into a single, discrete capsule adjacent to the oesophageal/intestinal junction, rather than separated into cranial, intermediate and caudal cords as in adult holarctic lampreys. In M.mordax, the larval islet cells are derived from the intestinal epithelium at the point where the anterior intestine is confluent with the oesophagous, but opposite the single intestinal diverticulum of this species. While adult islet follicles are also found en masse alongside the oesophageal/intestinal junction of M.mordax, they are not packed into a discrete capsule. The lack of separate intermediate and caudal cords in adults of the Southern Hemisphere lampreys is due to the lack of involvement of the bile duct in islet formation during metamorphosis. B cells are present in both larval and adult islet follicles of G.australis and M.mordax, and presumptive D cells were found in in all postlarval stages of G.australis after metamorphosing Stage 3, as well as in the young adults of M.mordax. While a further but less common u\ adult cell type was identified each Southern Hemisphere species, the shape and staining properties differed.

The exocrine pancreactic (zymogen) cells of larval G.australis are essentially restricted to the epithelium lining the two intestinal diverticula. The number of zymogen cells and digestive enzyme activity decline rapidly at the start of metamorphosis. While the diverticula are lost by metamorphosing Stage 4, zymogen cells reappear near the end of transformation in the mucosa lining the anterior intestine and de novo adult intestinal caecum. The latter structure, which is similar to that of adult holarctic lanpreys, develops alongside the new oesophageal/intestinal junction between Stages 4 and 6. In both larval and adult G.australis, tryptic, amylolytic and lipolytic activity were highest in those portions of the alimentary canal containing zymogen Differences cells. in the activity of the principal pancreatic enzymes within the gut of the larvae and adults have been related to the marked differences in the diet of the two divergent life cycle stages. While the exocrine pancreatic tissue of larval M.mordax is unique among lanpreys by being located within a single, large diverticulum containing an extensive network of mucosal folds, that of the adult is found in the same location as in those of other lanpreys. It is concluded that the different larval intestinal diverticula of Geotria and Mordacia represent independent specializations to increase and focus digestive enzyme activity at the front end of the intestine, possibly as a response to poor quality detritus in tenperate Australian streams. Such an explanation implies that the widely-dispersed populations of G.australis and the conteirporary fJordacia spp. radiated from stocks which evolved in Australia during the Tertiary.

Measurements have been made of those changes which lead to increases in the surface area of the intestine during the metamorphosis of G.australis, Lampetra fluviatilis and the nonparasitic brook lairprey. Lanpetra planeri. An account is also given of the pattern of intestinal fold formation, the fate of the typhlosolar pathway and the development of the typhlosolar vein in transforming G.australis. Although the intestine of G.australis increases in length by 12.5% and in diameter by 1.12 times during metamorphosis, the min cause of 5.71 times increase in surface area is the development of longitudinal folds. Except during Stages 3 and 4 of metamorphosis, the contribution of the typhlosole to the internal perimeter of the intestine is less in all life cycle stages of G.australis than in Lampetra spp. Metamorphic changes in the various intestinal measurements of the nonparasitic L.planeri parallel those of its presumed ancestral species, L.fluviatilis, between Stages 1 and 6. Subsequently, however, the longitudinal folds (but not the typhlosole) start regressing in the brook lairprey, just after the time when gonadal development is accelerated.

During the marine phase of G.australis, the external diameter of the intestine and the number and height of the longitudinal folds increase markedly, although the proportional contribution of the typhlosole to the internal perimeter of the anterior intestine falls from 12.2 to 7.5%. The intestine of fully grown adults of G.australis undergoes rapid atrophy when the animals leave the sea at the start of their upstream spawning migration, even though the gonads do not show any sign of accelerated development at this time.

Item Type: Thesis (PhD)
Murdoch Affiliation: School of Biological and Environmental Sciences
Notes: Note to the author: If you would like to make your thesis openly available on Murdoch University Library's Research Repository, please contact: Thank you.
Supervisor(s): Lethbridge, Roger
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