Descriptions of spawning of the pouched lamprey (Geotria australis) in tanks and of morphological changes leading up to and following spawning
K. R. Paton A , M. H. Cake A B , D. J. Bird A and I. C. Potter AA Centre for Sustainable Aquatic Resources, Murdoch University, Murdoch, WA 6150, Australia.
B Corresponding author. Email: max.cake@murdoch.edu.au
Pacific Conservation Biology 26(3) 301-307 https://doi.org/10.1071/PC19025
Submitted: 25 June 2019 Accepted: 23 November 2019 Published: 12 December 2019
Abstract
The anadromous Geotria australis, one of only three lamprey species representing the early agnathan (jawless) stage of vertebrate evolution in Australia and New Zealand, is declining in abundance. Its adults were caught soon after they had entered rivers on their non-trophic upstream migration and maintained in laboratory tanks for 13–15 months through to spawning. As adult G. australis are susceptible to haemorrhagic septicaemia, they were treated prophylactically and maintained in 3-m3 aquaria supplied with a flow-through charcoal filtration system and UV steriliser. Air temperature and the light : dark regime were constantly adjusted to parallel those in the environment. Males developed the very large suctorial disc and gular pouch characteristic of maturity and both sexes matured at the same time as in the wild. While males frequently showed aggressive behaviour towards each other, the same male and female mated on several occasions. The male coiled around the female and, with his urogenital papilla close to the female’s cloaca, twisted and vibrated, leading to egg release. These eggs formed coagulated clusters as in the wild, with many progressing through to the eight-cell stage. Remarkably, numerous G. australis were still alive 95–392 days after the end of the short spawning period, and one male after a further 119 days. Postspawning survival would be facilitated inter alia by extensive proteolysis, reflected in a shortening of the body. The data in this paper emphasise that G. australis is a highly atypical lamprey and provides invaluable information for conserving this declining species.
Additional keywords: energy reserves, mating behaviour, non-trophic, post-spawning longevity, secondary sexual characters, spawning run.
References
Abou-Seedo, F. S., and Potter, I. C. (1979). The estuarine phase in the spawning run of the river lamprey Lampetra fluviatilis. Journal of Zoology 188, 5–25.| The estuarine phase in the spawning run of the river lamprey Lampetra fluviatilis.Crossref | GoogleScholarGoogle Scholar |
Allen, M. G., Beatty, S. J., and Morgan, D. L. (2017). Aquatic fauna refuges in Margaret River and Cape to Cape region of Australia’s Mediterranean-climatic Southwestern Province. Fishes in Mediterranean Environments 2017, 1–26.
| Aquatic fauna refuges in Margaret River and Cape to Cape region of Australia’s Mediterranean-climatic Southwestern Province.Crossref | GoogleScholarGoogle Scholar |
Baker, C. F., Jellyman, D. J., Reeve, K., Crow, S., Stewart, M., and Buchinger, T. (2017). First observations of spawning nests in the pouched lamprey (Geotria australis). Canadian Journal of Fisheries and Aquatic Sciences 74, 1603–1611.
| First observations of spawning nests in the pouched lamprey (Geotria australis).Crossref | GoogleScholarGoogle Scholar |
Bird, D. J., and Potter, I. C. (1983a). Proximate composition at various stages of adult life in the Southern Hemisphere lamprey Geotria australis Gray. Comparative Biochemistry and Physiology. Part A, Molecular & Integrative Physiology 74, 623–633.
| Proximate composition at various stages of adult life in the Southern Hemisphere lamprey Geotria australis Gray.Crossref | GoogleScholarGoogle Scholar |
Bird, D. J., and Potter, I. C. (1983b). Changes in the fatty acid composition of triacylglycerols and phospholipids during the life cycle of the lamprey Geotria australis Gray. Comparative Biochemistry and Physiology. Part B, Biochemistry & Molecular Biology 75, 31–41.
| Changes in the fatty acid composition of triacylglycerols and phospholipids during the life cycle of the lamprey Geotria australis Gray.Crossref | GoogleScholarGoogle Scholar |
Brosnahan, C. L., Pande, A., Keeling, S. E., van Andel, M., and Jones, J. B. (2019). Lamprey (Geotria australis; Agnatha) reddening syndrome in Southland rivers, New Zealand 2011–2013: laboratory findings and epidemiology, including the incidental detection of an atypical Aeromonas salmonicida. New Zealand Journal of Marine and Freshwater Research 53, 416–436.
| Lamprey (Geotria australis; Agnatha) reddening syndrome in Southland rivers, New Zealand 2011–2013: laboratory findings and epidemiology, including the incidental detection of an atypical Aeromonas salmonicida.Crossref | GoogleScholarGoogle Scholar |
Cochran, P. A., and Gripentrog, A. P. (1992). Aggregation and spawning by lampreys (genus Ichthyomyzon) beneath cover. Environmental Biology of Fishes 33, 381–387.
| Aggregation and spawning by lampreys (genus Ichthyomyzon) beneath cover.Crossref | GoogleScholarGoogle Scholar |
Cochran, P. A., Bloom, D. D., and Wagner, R. J. (2008). Alternative reproductive behaviors in lampreys and their significance. Journal of Freshwater Ecology 23, 437–444.
| Alternative reproductive behaviors in lampreys and their significance.Crossref | GoogleScholarGoogle Scholar |
Dawson, H. A., Quintella, B. R., Almeida, P. R., Treble, A. J., and Jolley, J. C. (2015). The ecology of larval and metamorphosing lampreys. In ‘Lampreys: Biology, Conservation and Control’. (Ed. M. F. Docker.) Volume 1, Chapter 3, pp. 75–137. (Springer: Dordrecht.)
Dunn, N. R., Allibone, R. M., Closs, G. P., Crow, S. K., David, B. O., Goodman, J. M., Griffiths, M., Jack, D. C., Ling, N., Waters, J. M., and Rolfe, J. R. (2018). ‘Conservation Status of New Zealand Freshwater Fishes, 2017.’ (Department of Conservation: Wellington.)
Glova, G. (1995). The secret life of the lamprey. NIWA Water & Atmosphere 3, 20–21.
Hagelin, L. O. (1959). Further aquarium observations on the spawning habits of the river lamprey (Petromyzon fluviatilis). Oikos 10, 50–64.
| Further aquarium observations on the spawning habits of the river lamprey (Petromyzon fluviatilis).Crossref | GoogleScholarGoogle Scholar |
Hardisty, M. W. (2006). ‘Lampreys: Life without Jaws.’ (Forrest Text: Cardigan, UK.)
Hardisty, M. W., and Potter, I. C. (1971). The behaviour, ecology and growth of larval lampreys. In ‘The Biology of Lampreys’. (Eds M. W. Hardisty, and I. C. Potter.) Volume 1, Chapter 3, pp. 85–125. (Academic Press: London.)
Hilliard, R. W., Pass, D. A., and Potter, I. C. (1979). Haemorrhagic septicaemia in the lamprey Geotria australis Gray. Acta Zoologica 60, 115–121.
| Haemorrhagic septicaemia in the lamprey Geotria australis Gray.Crossref | GoogleScholarGoogle Scholar |
Hubbs, C. L., and Potter, I. C. (1971). Distribution, phylogeny and taxonomy. In ‘The Biology of Lampreys’. (Eds M. W. Hardisty, and I. C. Potter.) Volume 1, Chapter 1, pp. 1–65. (Academic Press: London.)
Jellyman, D. J., Glova, G. J., and Sykes, J. R. E. (2002). Movements and habitats of adult lamprey (Geotria australis) in two New Zealand waterways. New Zealand Journal of Marine and Freshwater Research 36, 53–65.
| Movements and habitats of adult lamprey (Geotria australis) in two New Zealand waterways.Crossref | GoogleScholarGoogle Scholar |
Johnson, N. S., Buchinger, T. J., and Li, W. (2015). Reproductive ecology of lampreys. In ‘Lampreys: Biology, Conservation and Control’. (Ed. M. F. Docker.) Volume 1, Chapter 6, pp. 265–303. (Springer: Dordrecht.)
Kelso, J. R. M., and Todd, P. R. (1993). Instream size segregation and density of Geotria australis ammocoetes in two New Zealand streams. Ecology Freshwater Fish 2, 108–115.
| Instream size segregation and density of Geotria australis ammocoetes in two New Zealand streams.Crossref | GoogleScholarGoogle Scholar |
Lanzing, W. J. R. (1959). ‘Studies on the River lamprey Lampetra fluviatilis during its anadromous migration’. (Uitgeversmaatschappij Neerlandia: Utrecht.)
Moore, J. W., and Potter, I. C. (1976). Aspects of feeding and lipid deposition and utilization in the lampreys Lampetra fluviatilis (L.) and Lampetra planeri (Bloch). Journal of Animal Ecology 45, 699–712.
| Aspects of feeding and lipid deposition and utilization in the lampreys Lampetra fluviatilis (L.) and Lampetra planeri (Bloch).Crossref | GoogleScholarGoogle Scholar |
Morgan, D. J., Unmack, P. J., Beatty, S. J., Ebner, B. C., Allen, M. G., Keleher, J. J., Donaldson, J. A., and Murphy, J. (2014). An overview of the ‘freshwater fishes’ of Western Australia. Journal of the Royal Society of Western Australia 97, 263–278.
Moser, M. L., Almeida, P. R., Kemp, P. S., and Sorensen, P. W. (2015). Lamprey spawning migration. In ‘Lampreys: Biology, Conservation and Control’. (Ed. M. F. Docker.) Volume 1, Chapter 5, pp. 215–263. (Springer: Dordrecht.)
Moser, M. L., Hume, J. B., Aronsuu, K. K., Lampman, R. T., and Jackson, A. D. (2019). Lamprey reproduction and early life history: insights from artificial propagation. In ‘Lampreys: Biology, Conservation and Control’. (Ed. M. F. Docker.) Volume 2, Chapter 2, pp. 187–245. (Springer: Dordrecht.)
Paton, K. R., Cake, M. H., and Potter, I. C. (2011). Metabolic responses to exhaustive exercise change markedly during the protracted non-trophic spawning migration of the lamprey Geotria australis. Journal of Comparative Physiology. B, Biochemical, Systemic, and Environmental Physiology 181, 751–763.
| Metabolic responses to exhaustive exercise change markedly during the protracted non-trophic spawning migration of the lamprey Geotria australis.Crossref | GoogleScholarGoogle Scholar | 21442322PubMed |
Paton, K. R., Cake, M. H. and Potter, I. C. (in press). Lipid and protein catabolism contribute to aerobic metabolic responses to exhaustive exercise during the protracted spawning run of the lamprey Geotria australis. Journal of Comparative Physiology B, Biochemical, Systems, and Environmental Physiology.
Potter, I. C. (1980). Ecology of larval and metamorphosing lampreys. Canadian Journal of Fisheries and Aquatic Sciences 37, 1641–1657.
| Ecology of larval and metamorphosing lampreys.Crossref | GoogleScholarGoogle Scholar |
Potter, I. C., and Strahan, R. (1968). The taxonomy of the lampreys Geotria and Mordacia and their distribution in Australia. Proceedings of the Linnean Society of London 179, 229–240.
| The taxonomy of the lampreys Geotria and Mordacia and their distribution in Australia.Crossref | GoogleScholarGoogle Scholar |
Potter, I. C., and Beamish, F. W. H. (1977). The freshwater biology of anadromous sea lampreys Petromyzon marinus. Journal of Zoology 181, 113–130.
| The freshwater biology of anadromous sea lampreys Petromyzon marinus.Crossref | GoogleScholarGoogle Scholar |
Potter, I. C., and Hilliard, R. W. (1986). Growth and the average duration of larval life in the Southern Hemisphere lamprey Geotria australis Gray. Experientia 42, 1170–1173.
| Growth and the average duration of larval life in the Southern Hemisphere lamprey Geotria australis Gray.Crossref | GoogleScholarGoogle Scholar |
Potter, I. C., and Hilliard, R. W. (1987). A proposal for the functional and phylogenetic significance of differences in the dentition of lampreys (Agnatha: Petromyzontiformes). Journal of Zoology 212, 713–737.
| A proposal for the functional and phylogenetic significance of differences in the dentition of lampreys (Agnatha: Petromyzontiformes).Crossref | GoogleScholarGoogle Scholar |
Potter, I. C., and Robinson, E. S. (1991). Development of the testis during post-metamorphic life in the Southern Hemisphere lamprey Geotria australis Gray. Acta Zoologica 72, 113–119.
| Development of the testis during post-metamorphic life in the Southern Hemisphere lamprey Geotria australis Gray.Crossref | GoogleScholarGoogle Scholar |
Potter, I. C., and Welsch, U. (1997). The structure of the gular pouch of mature males of the lamprey Geotria australis. Acta Zoologica 78, 97–106.
| The structure of the gular pouch of mature males of the lamprey Geotria australis.Crossref | GoogleScholarGoogle Scholar |
Potter, I. C., Cannon, D., and Moore, J. W. (1975). The ecology of algae in the Moruya River, Australia. Hydrobiologia 47, 415–430.
| The ecology of algae in the Moruya River, Australia.Crossref | GoogleScholarGoogle Scholar |
Potter, I. C., Hilliard, R. W., and Bird, D. J. (1980). Metamorphosis in the Southern Hemisphere lamprey, Geotria australis. Journal of Zoology 190, 405–430.
| Metamorphosis in the Southern Hemisphere lamprey, Geotria australis.Crossref | GoogleScholarGoogle Scholar |
Potter, I. C., Hilliard, R. W., Bird, D. J., and Macey, D. J. (1983). Quantitative data on morphology and organ weights during the protracted spawning-run period of the Southern Hemisphere lamprey Geotria australis. Journal of Zoology 200, 1–20.
| Quantitative data on morphology and organ weights during the protracted spawning-run period of the Southern Hemisphere lamprey Geotria australis.Crossref | GoogleScholarGoogle Scholar |
Potter, I. C., Gill, H. S., Renaud, C. B., and Haoucher, D. (2015). The taxonomy, phylogeny, and distribution of lampreys. In ‘Lampreys: Biology, Conservation and Control’. (Ed. M. F. Docker.) Volume 1, Chapter 2, pp. 35–73. (Springer: Dordrecht.)
Renaud, C. B., Gill, H. S., and Potter, I. C. (2009). Relationships between the diets and characteristics of the dentition, buccal glands and velar tentacles of the adults of the parasitic species of lampreys. Journal of Zoology 278, 231–242.
| Relationships between the diets and characteristics of the dentition, buccal glands and velar tentacles of the adults of the parasitic species of lampreys.Crossref | GoogleScholarGoogle Scholar |