Advertisement

Aquatic Sciences

, 82:8 | Cite as

Quality and contribution of food sources to Australian lungfish evaluated using fatty acids and stable isotopes

  • Juan TaoEmail author
  • Mark J. Kennard
  • David T. Roberts
  • Brian Fry
  • Martin J. Kainz
  • Yifeng Chen
  • Stuart E. Bunn
Research Article

Abstract

The Australian lungfish, Neoceratodus forsteri Krefft, 1870, is a threatened species whose long-term persistence is at risk due to land-use intensification, water resource development, and other human pressures. Changes to the hydrology of rivers has the potential to alter the availability of certain high-quality food resources for this species, that may impact recruitment success, and contribute to population declines. This study analysed the fatty acid (FA) composition of lungfish eggs and fin tissues from two locations upstream and downstream of a large dam in the Brisbane River. We tested the hypothesis that river impoundment and flow alteration associated with the dam have altered the dietary composition and the FA composition of important dietary items for N. forsteri which translates to the body tissues and eggs. The contribution of each food source was estimated with mixing models using carbon and nitrogen stable isotopes. The total FA content in lungfish fin and eggs was significantly higher in downstream sites compared to upstream. Few significant differences in FA contents of the nine potential lungfish food sources were found between sites upstream and downstream of the dam. Stable isotope analyses of lungfish fin tissues revealed the most likely food sources were gastropods, bivalves, and crustaceans, however their relative importance differed upstream and downstream of the dam. Collectively, these results indicate that the dam did not negatively affect food quality for lungfish downstream. The most likely mechanism for potential FA deficiency and subsequent impacts on recruitment success in N. forsteri would be due to changes to the availability of high-quality food sources. This study highlights the need for future research to determine whether the low FA contents we observed in lungfish, is a function of broader environmental changes, or if FA contents are naturally low for this sub-tropical species.

Keywords

Neoceratodus forsteri Human disturbance Reproduction Fatty acid Stable isotope Food quality 

Notes

Acknowledgements

The authors thank Thomas Espinoza, Andrew McDougall, Christopher Robinson, Stephen Faggotter, Sebastian Knight, Aaron Dunlop, and Jing Lu for their assistance with field sampling. We also thank Katharina Winter and Stefanie Danner for their help with laboratory analysis of FA samples. Lungfish sampling was conducted in accordance with the provisions of Queensland General Fisheries Permit 174232 and the Griffith University Animal Ethics committee (project reference ENV/12/14/AEC). This project was funded and supported by Seqwater, and JT was supported by a Chinese Academy of Sciences Stipend Scholarship and a Griffith University International Postgraduate Research Scholarship.

Supplementary material

27_2019_680_MOESM1_ESM.docx (81 kb)
Supplementary material 1 (DOCX 80 kb)

References

  1. Arthington AH (2009) Australian lungfish, Neoceratodus forsteri, threatened by a new dam. Environ Biol Fishes 84:211–221CrossRefGoogle Scholar
  2. Arthington A, Kennard MJ, Mackay SJ et al (2000) Environmental flow requirements of the Brisbane River downstream from Wivenhoe Dam. South East Queensland Water Corporation, and Centre for Catchment and In-Stream Research. Griffith University, BrisbaneGoogle Scholar
  3. Ashton HJ, Farkvam DO, March BE (1993) Fatty acid composition of lipids in the eggs and alevins from wild and cultured chinook salmon (Oncorhynchus tshawytscha). Can J Fish Aquat Sci 50:648–655CrossRefGoogle Scholar
  4. Asil SM, Kenari AA, Miyanji GR, Van Der Kraak G (2017) The influence of dietary arachidonic acid on growth, reproductive performance, and fatty acid composition of ovary, egg and larvae in an anabantid model fish, Blue gourami (Trichopodus trichopterus; Pallas, 1770). Aquaculture 476:8–18CrossRefGoogle Scholar
  5. Bell MV, Henderson RJ, Pirie B, Sargent JR (1985) Effects of dietary polyunsaturated fatty acid deficiencies on mortality, growth and gill structure in the turbot, Scophthalmus maximus. J Fish Biol 26:181–191CrossRefGoogle Scholar
  6. Bell MV, Henderson RJ, Sargent JR (1986) The role of polyunsaturated fatty acids in fish. Compar Biochem Physiol Part B Compar Biochem 83:711–719CrossRefGoogle Scholar
  7. Bell MV, Batty RS, Dick JR et al (1995) Dietary deficiency of docosahexaenoic acid impairs vision at low light intensities in juvenile herring (Clupea harengus L.). Lipids 30:443–449PubMedCrossRefGoogle Scholar
  8. Böhm M, Schultz S, Koussoroplis AM, Kainz MJ (2014) Tissue-specific fatty acids response to different diets in common carp (Cyprinus carpio L.). Plos One 9:e94759PubMedPubMedCentralCrossRefGoogle Scholar
  9. Bond AL, Diamond AW (2011) Recent Bayesian stable-isotope mixing models are highly sensitive to variation in discrimination factors. Ecol Appl 21:1017–1023PubMedCrossRefGoogle Scholar
  10. Brett MT (2014) Resource polygon geometry predicts Bayesian stable isotope mixing model bias. Mar Ecol Prog Ser 514:1–12CrossRefGoogle Scholar
  11. Brett M, Müller-Navarra D (1997) The role of highly unsaturated fatty acids in aquatic food web processes. Freshw Biol 38:483–499CrossRefGoogle Scholar
  12. Brett MT, Kainz MJ, Taipale SJ, Seshan H (2009) Phytoplankton, not allochthonous carbon, sustains herbivorous zooplankton production. Proc Natl Acad Sci USA 106:21197–21201PubMedCrossRefGoogle Scholar
  13. Bunn SE, Leigh C, Jardine TD (2013) Diet-tissue fractionation of δ15N by consumers from streams and rivers. Limnol Oceanogr 58:765–773CrossRefGoogle Scholar
  14. Castro LR, Claramunt G, Gonzalez HE et al (2010) Fatty acids in eggs of anchoveta Engraulis ringens during two contrasting winter spawning seasons. Mar Ecol Prog Ser 420:193–205CrossRefGoogle Scholar
  15. Clarke KR, Gorley RN (2006) PRIMER V6: user manual-tutorial. Plymouth Marine Laboratory, PlymouthGoogle Scholar
  16. Copeman LA, Parrish CC, Brown JA, Harel M (2002) Effects of docosahexaenoic, eicosapentaenoic, and arachidonic acids on the early growth, survival, lipid composition and pigmentation of yellowtail flounder (Limanda ferruginea): a live food enrichment experiment. Aquaculture 210:285–304CrossRefGoogle Scholar
  17. Duivenvoorden LJ (2008) Effects of water level fluctuations on Vallisneria nana in the Burnett River in southeast Queensland, Australia. River Res Appl 24:1362–1376CrossRefGoogle Scholar
  18. Espinoza T, Marshall SM, Mcdougall AJ (2013) Spawning of the endangered Australian Lungfish (Neoceratodus forsteri) in a heavily regulated river: a pulse for life. River Res Appl 29:1215–1225CrossRefGoogle Scholar
  19. Furuita H, Takeuchi T, Uematsu K (1998) Effects of eicosapentaenoic and docosahexaenoic acids on growth, survival and brain development of larval Japanese flounder (Paralichthys olivaceus). Aquaculture 161:269–279CrossRefGoogle Scholar
  20. Furuita H, Tanaka H, Yamamoto T et al (2000) Effects of n − 3 HUFA levels in broodstock diet on the reproductive performance and egg and larval quality of the Japanese flounder, Paralichthys olivaceus. Aquaculture 187:387–398CrossRefGoogle Scholar
  21. Furuita H, Ohta H, Unuma T et al (2003) Biochemical composition of eggsin relation to egg quality in the Japanese eel, Anguilla japonica. Fish Physiol Biochem 29:37–46CrossRefGoogle Scholar
  22. Guo F, Kainz MJ, Sheldon F, Bunn SE (2015) Spatial variation in periphyton fatty acid composition in subtropical streams. Freshw Biol 60:1411–1422CrossRefGoogle Scholar
  23. Guo F, Kainz MJ, Fran S, Bunn SE (2016a) The importance of high quality algal food sources in stream food webs—current status and future perspectives. Freshw Biol 61:815–831CrossRefGoogle Scholar
  24. Guo F, Kainz MJ, Sheldon F, Bunn SE (2016b) Effects of light and nutrients on periphyton and the fatty acid composition and somatic growth of invertebrate grazers in subtropical streams. Oecologia 181:449–462.  https://doi.org/10.1007/s00442-016-3573-x CrossRefPubMedGoogle Scholar
  25. Guo F, Kainz MJ, Valdez D et al (2016c) The effect of light and nutrients on algal food quality and their consequent effect on grazer growth in subtropical streams. Freshw Sci 35:1202–1212CrossRefGoogle Scholar
  26. Guo F, Bunn SE, Brett MT et al (2017) Polyunsaturated fatty acids in stream food webs—high dissimilarity among producers and consumers. Freshw Biol 62:1325–1334CrossRefGoogle Scholar
  27. Guschina IA, Harwood JL (2006) Lipids and lipid metabolism in eukaryotic algae. Prog Lipid Res 45:160–186PubMedCrossRefGoogle Scholar
  28. Heissenberger M, Watzke J, Kainz MJ (2010) Effect of nutrition on fatty acid profiles of riverine, lacustrine, and aquaculture-raised salmonids of pre-alpine habitats. Hydrobiologia 650:243–254.  https://doi.org/10.1007/s10750-010-0266-z CrossRefGoogle Scholar
  29. Ishizaki Y, Masuda R, Uematsu K et al (2001) The effect of dietary docosahexaenoic acid on schooling behaviour and brain development in larval yellowtail. J Fish Biol 58:1691–1703CrossRefGoogle Scholar
  30. Izquierdo MS, Fernandez-Palacios H, Tacon A (2001) Effect of broodstock nutrition on reproductive performance of fish. Aquaculture 197:25–42CrossRefGoogle Scholar
  31. Jardine TD, Gray MA, McWilliam SM, Cunjak RA (2005) Stable isotope variability in tissues of temperate stream fishes. Trans Am Fish Soc 134:1103–1110CrossRefGoogle Scholar
  32. Kainz MJ, Johannsson OE, Arts MT (2010) Diet effects on lipid composition, somatic growth potential, and survival of the benthic amphipod Diporeia spp. J Great Lakes Res 36:351–356CrossRefGoogle Scholar
  33. Kainz MJ, Hager HH, Rasconi S et al (2017) Polyunsaturated fatty acids in fishes increase with total lipids irrespective of feeding sources and trophic position. Ecosphere 8:e01753CrossRefGoogle Scholar
  34. Kemp A (1997) A revision of Australian Mesozoic and Cenozoic lungfish of the family Neoceratodontidae (Osteichthyes: Dipnoi), with a description of four new species. J Paleontol 71:713–733CrossRefGoogle Scholar
  35. Kemp A (2011) Comparison of embryological development in the threatened Australian lungfish Neoceratodus forsteri from two sites in a Queensland river system. Endanger Species Res 15:87–101CrossRefGoogle Scholar
  36. Kemp A (2014) Abnormal development in embryos and hatchlings of the Australian lungfish, Neoceratodus forsteri, from two reservoirs in south-east Queensland. Aust J Zool 62:63–79CrossRefGoogle Scholar
  37. Kemp A, Anderson T, Tomley A, et al (1981) The use of the Australian lungfish (Neoceratodus forsteri) for the control of submerged aquatic weeds. Queensland Weed Society, pp 155–158Google Scholar
  38. Kemp A, Heaslop M, Carr A (2015) Scale Structure in the Australian Lungfish, Neoceratodus forsteri (Osteichthyes: Dipnoi). J Morphol 276:1137–1145PubMedCrossRefGoogle Scholar
  39. Kind PK (2011) The natural history of the Australian lungfish Neoceratodus forsteri (Krefft, 1870). In: Jørgensen JM, Joss J (eds) The biology of lungfishes. Science Publidhers, Enfield, pp 61–99Google Scholar
  40. Larson JH, Richardson WB, Vallazza JM et al (2017) Using a gradient in food quality to infer drivers of fatty acid content in two filter-feeding aquatic consumers. Aquat Sci 79:855–865CrossRefGoogle Scholar
  41. Luo L, Ai L, Liang X et al (2017) n-3 Long-chain polyunsaturated fatty acids improve the sperm, egg, and offspring quality of Siberian sturgeon (Acipenser baerii). Aquaculture 473:266–271CrossRefGoogle Scholar
  42. Marshall SM, Espinoza T, Mcdougall AJ (2015) Effects of water level fluctuations on spawning habitat of an endangered species, the Australian Lungfish (Neoceratodus forsteri). River Res Appl 31:552–562CrossRefGoogle Scholar
  43. Montero D, Socorro J, Tort L et al (2004) Glomerulonephritis and immunosuppression associated with dietary essential fatty acid deficiency in gilthead sea bream, Sparus aurata L., juveniles. J Fish Dis 27:297–306PubMedCrossRefGoogle Scholar
  44. Mourente G, Rodriguez A, Tocher DR, Sargent JR (1993) Effects of dietary docosahexaenoic acid (DHA; 22:6n–3) on lipid and fatty acid compositions and growth in gilthead sea bream (Sparus aurata L.) larvae during first feeding. Aquaculture 112:79–98CrossRefGoogle Scholar
  45. Müller-Navarra DC, Brett MT, Liston AM, Goldman CR (2000) A highly unsaturated fatty acid predicts carbon transfer between primary producers and consumers. Nature 403:74–77PubMedCrossRefGoogle Scholar
  46. Murray DS, Hager HH, Tocher DR, Kainz MJ (2014) Effect of partial replacement of dietary fish meal and oil by pumpkin kernel cake and rapeseed oil on fatty acid composition and metabolism in Arctic charr (Salvelinus alpinus). Aquaculture 431:85–91CrossRefGoogle Scholar
  47. Olden JD, Fallon SJ, Roberts DT, Espinoza T, Kennard MJ (2018) Looking to the past to ensure the future of the world’s oldest living vertebrate: isotopic evidence for multi-decadal shifts in trophic ecology of the Australian lungfish. River Research and Applications.  https://doi.org/10.1002/rra.3369 CrossRefGoogle Scholar
  48. Olley J, Burton J, Hermoso V et al (2015) Remnant riparian vegetation, sediment and nutrient loads, and river rehabilitation in subtropical Australia. Hydrol Process 29:2290–2300CrossRefGoogle Scholar
  49. Olsen Y, Evjemo JO, Kjørsvik E et al (2014) DHA content in dietary phospholipids affects DHA content in phospholipids of cod larvae and larval performance. Aquaculture 428:203–214CrossRefGoogle Scholar
  50. Parnell AC, Inger R, Bearhop S, Jackson AL (2010) Source partitioning using stable isotopes: coping with too much variation. PLoS One 5:e9672PubMedPubMedCentralCrossRefGoogle Scholar
  51. Pethybridge HR, Parrish CC, Bruce BD et al (2014) Lipid, fatty acid and energy density profiles of white sharks: insights into the feeding ecology and ecophysiology of a complex top predator. PLoS One 9:e97877PubMedPubMedCentralCrossRefGoogle Scholar
  52. Phillips DL, Gregg JW (2001) Uncertainty in source partitioning using stable isotopes. Oecologia 127:171–179PubMedCrossRefGoogle Scholar
  53. Post DM (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83:703–718CrossRefGoogle Scholar
  54. Power M, Guiguer KR, Barton DR (2003) Effects of temperature on isotopic enrichment in Daphnia magna: implications for aquatic food-web studies. Rapid Commun Mass Spectrom 17:1619–1625PubMedCrossRefGoogle Scholar
  55. Pusey B, Kennard MJ, Arthington AH (2004) Freshwater fishes of north-eastern Australia. CSIRO Publishing, BrisbaneCrossRefGoogle Scholar
  56. Raghavan R, Philip S, Ali A et al (2016) Fishery, biology, aquaculture and conservation of the threatened Asian Sun catfish. Rev Fish Biol Fisheries 26:169–180CrossRefGoogle Scholar
  57. Renaud SM, Thinh L-V, Lambrinidis G, Parry DL (2002) Effect of temperature on growth, chemical composition and fatty acid composition of tropical Australian microalgae grown in batch cultures. Aquaculture 211:195–214CrossRefGoogle Scholar
  58. Roberts DT, Mallett S, Krück NC et al (2014) Spawning activity of the Australian lungfish Neoceratodus forsteri in an impoundment. J Fish Biol 84:163–177PubMedCrossRefGoogle Scholar
  59. Røjbek MC, Støttrup JG, Jacobsen C et al (2014) Effects of dietary fatty acids on the production and quality of eggs and larvae of Atlantic cod (Gadus morhua L.). Aquac Nutr 20:654–666CrossRefGoogle Scholar
  60. Rutherford JC, Marsh NA, Davies PM, Bunn SE (2004) Effects of patchy shade on stream water temperature: how quickly do small streams heat and cool? Mar Freshw Res 55:737–748CrossRefGoogle Scholar
  61. Saavedra M, Batista H, Pousão-Ferreira P (2016) Dietary fatty acid enrichment during the spawning season increases egg viability and quality in Hippocampus hippocampus. Aquac Nutr 22:343–351CrossRefGoogle Scholar
  62. Sargent JR (1993) Docosahexaenoic acid and the development of brain and retina in marine fish. In: Drevon CA, Baksaas I, Krokan HE (eds) Omega-3 fatty acids metabolism and biological effects. Omega-3 fatty acids; metabolism and biological effects, Basel, Switzerland, pp 139–149Google Scholar
  63. Sargent JR (1995) Origins and functions of egg lipids: nutritional implications. In: Bromage NR, Roberts RR (eds) Broodstock Management and Egg and Larval Quality. Broodstock Management and Egg and Larval Quality, Oxford, pp 353–372Google Scholar
  64. Sargent J, Bell G, McEvoy L et al (1999) Recent developments in the essential fatty acid nutrition of fish. Aquaculture 177:191–199CrossRefGoogle Scholar
  65. Seoka M, Kurata M, Kumai H (2007) Effect of docosahexaenoic acid enrichment in Artemiaon growth of Pacific bluefin tuna Thunnus orientalis larvae. Aquaculture 270:193–199CrossRefGoogle Scholar
  66. Tocher DR (2003) Metabolism and functions of lipids and fatty acids in teleost fish. Rev Fish Sci 11:107–184CrossRefGoogle Scholar
  67. Tocher DR (2010) Fatty acid requirements in ontogeny of marine and freshwater fish. Aquac Res 41:717–732CrossRefGoogle Scholar
  68. Tocher DR, Harvie DG (1988) Fatty acid compositions of the major phosphoglycerides from fish neural tissues;(n − 3) and (n − 6) polyunsaturated fatty acids in rainbow trout (Salmo gairdneri) and cod (Gadus morhua) brains and retinas. Fish Physiol Biochem 5:229–239PubMedCrossRefGoogle Scholar
  69. Torres-Ruiz M, Wehr JD, Perrone AA (2007) Trophic relations in a stream food web: importance of fatty acids for macroinvertebrate consumers. J N Am Benthol Soc 26:509–522.  https://doi.org/10.1899/06-070.1 CrossRefGoogle Scholar
  70. Tveiten H, Jobling M, Andreassen I (2004) Influence of egg lipids and fatty acids on egg viability, and their utilization during embryonic development of spotted wolf-fish, Anarhichas minor Olafsen. Aquac Res 35:152–161CrossRefGoogle Scholar
  71. Vander Zanden MJ, Rasmussen JB (2001) Variation in δ15N and δ13C trophic fractionation: implications for aquatic food web studies. Limnol Oceanogr 46:2061–2066CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Institute of International Rivers and Eco-securityYunnan UniversityKunmingChina
  2. 2.Australian Rivers InstituteGriffith UniversityBrisbaneAustralia
  3. 3.Institute of HydrobiologyChinese Academy of SciencesWuhanChina
  4. 4.SeqwaterBrisbaneAustralia
  5. 5.WasserCluster Lunz, Inter-University Centre for Aquatic Ecosystem ResearchLunz am SeeAustria

Personalised recommendations