Register      Login
Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences
RESEARCH ARTICLE

Using an acoustic telemetry array to assess fish volumetric space use: a case study on impoundments, hypoxia and an air-breathing species (Neoceratodus forsteri)

D. T. Roberts A E , V. Udyawer B , C. Franklin C , R. G. Dwyer C and H. A. Campbell D
+ Author Affiliations
- Author Affiliations

A Seqwater, PO Box 16146, City East, Qld 4002, Australia.

B Australian Institute of Marine Science, Arafura Timor Research Facility, PO Box 41775, Casuarina MC, Casuarina, NT 0811, Australia.

C The School of Biological Sciences, The University of Queensland, Goddard Building, St Lucia, Brisbane, Qld 3052, Australia.

D Research Institute for the Environment and Livelihoods, Charles Darwin University, Ellengowan Drive, Casuarina, NT 0909, Australia.

E Corresponding author. Email: david.t.roberts@seqwater.com.au

Marine and Freshwater Research 68(8) 1532-1543 https://doi.org/10.1071/MF16124
Submitted: 8 April 2016  Accepted: 5 December 2016   Published: 9 February 2017

Abstract

Facultative air-breathing fish can persist in hypoxic waters due to their capacity to acquire atmospheric oxygen. Most studies examining responses of air-breathing fish to aquatic hypoxia have occurred under experimental conditions. How air-breathing fish respond to hypoxic conditions in the field has received less attention. Using depth sensor transmitters and an array of acoustic receivers to monitor the facultative air-breathing Australian lungfish (Neoceratodus forsteri), we investigated habitat preferences and behavioural responses to seasonal hypoxic zones in a riverine impoundment. Three-dimensional (3-D) kernel utilisation distribution (KUD) models revealed that during stratified conditions, lungfish remained above the oxycline, rarely venturing into hypoxic waters, whereas during holomixis lungfish used a wider range of depths. Total volumetric space utilisation did not change significantly during stratified periods, but the distribution of space used changed, constrained by the oxycline. Despite N. forsteri having lungs to supplement oxygen requirements, the presence of a hypoxic zone constrained the core (50% 3-D-KUD) volumetric space used by lungfish to <1.6% of the total available space of the study area. With increasing demand for new impoundments in many tropical and subtropical regions, the present study provides insights to how air-breathing fish species may respond to altered riverine conditions from impoundments.

Additional keywords: habitat preference, kernel utilisation distribution, lungfish, stratification, Vemco positioning system.


References

Adler, D., and Murdoch, D. (2016). rgl: 3-D visualization using OpenGL. R package, ver. 0.96.o. Available at https://CRAN.R-projecct.org/package=rgl [Verified 20 March 2016].

Altenritter, M. E. L., Wieten, A. C., Ruetz, C. R., and Smith, K. M. (2013). Seasonal spatial distribution of juvenile lake sturgeon in Muskegon Lake, Michigan, USA. Ecology Freshwater Fish 22, 467–478.
Seasonal spatial distribution of juvenile lake sturgeon in Muskegon Lake, Michigan, USA.Crossref | GoogleScholarGoogle Scholar |

Amarasinghe, U. A., and Smakhtin, V. (2014). Global water demand projections: past, present and future. (International Water Management Institute: Colombo, Sri Lanka.) Available at http://www.iwmi.cgiar.org/Publications/IWMI_Research_Reports/PDF/pub156/rr156.pdf [Verified 2 January 2017].

Antenucci, J. P., Ghadouani, A., Burford, M. A., and Romero, J. R. (2005). The long-term effect of artificial destratification on phytoplankton species composition in a sub-tropical reservoir. Freshwater Biology 50, 1081–1093.
The long-term effect of artificial destratification on phytoplankton species composition in a sub-tropical reservoir.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXlslWnur8%3D&md5=27a7cb3b8cadb877acc02c177fd7aafeCAS |

Arthington, A. H. (2009). Australian lungfish, Neoceratodus forsteri, threatened by a new dam. Environmental Biology of Fishes 84, 211–221.
Australian lungfish, Neoceratodus forsteri, threatened by a new dam.Crossref | GoogleScholarGoogle Scholar |

Bates, D., Maechler, M., Bolker, B., and Walker, S. (2015). Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67, 1–48.
Fitting linear mixed-effects models using lme4.Crossref | GoogleScholarGoogle Scholar |

Beckett, D. C., Aartila, T. P., and Miller, A. C. (1992). Contrasts in density of benthic invertebrates between macrophyte beds and open littoral patches in Eau-Galle Lake, Wisconsin. American Midland Naturalist 127, 77–90.
Contrasts in density of benthic invertebrates between macrophyte beds and open littoral patches in Eau-Galle Lake, Wisconsin.Crossref | GoogleScholarGoogle Scholar |

Boschilia, S. M., de Oliveira, E. F., and Schwarzbold, A. (2012). The immediate and long-term effects of water drawdown on macrophyte assemblages in a large subtropical reservoir. Freshwater Biology 57, 2641–2651.
The immediate and long-term effects of water drawdown on macrophyte assemblages in a large subtropical reservoir.Crossref | GoogleScholarGoogle Scholar |

Burford, M. A., McNeale, K., and McKenzie-Smith, F. J. (2006). The role of nitrogen in promoting the toxic cyanophyte Cylindrospermopsis raciborskii in a subtropical water reservoir. Freshwater Biology 51, 2143–2153.
The role of nitrogen in promoting the toxic cyanophyte Cylindrospermopsis raciborskii in a subtropical water reservoir.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1OisrbP&md5=2e2cbb04556463201a945748a5422ebdCAS |

Burt, K., Hamoutene, D., Perez-Casanova, J., Kurt Gamperl, A., and Volkoff, H. (2013). The effect of intermittent hypoxia on growth, appetite and some aspects of the immune response of Atlantic salmon (Salmo salar). Aquaculture Research 45, 124–137.
The effect of intermittent hypoxia on growth, appetite and some aspects of the immune response of Atlantic salmon (Salmo salar).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvV2lt77N&md5=61d3acddbf051d942dba8c27b8af1badCAS |

Cooke, S. J., Niezgoda, G. H., Hanson, K., Suski, C. D., Phelan, F. J. S., Tinline, R., and Philipp, D. P. (2005). Use of CDMA acoustic telemetry to document 3-D positions of fish: relevance to the design and monitoring of aquatic protected areas. Marine Technology Society Bulletin 39, 17–27.

Cooper, N. W., Sherry, T. W., and Marra, P. P. (2014). Modeling three-dimensional space use and overlap in birds. Auk 131, 681–693.
Modeling three-dimensional space use and overlap in birds.Crossref | GoogleScholarGoogle Scholar |

Cornelissen, I. J. M., van Zwieten, P. A. M., Peter, H. K., and Nagelkerke, L. A. J. (2015). Nile perch distribution in south-east Lake Victoria is more strongly driven by abiotic factors, than by prey densities. Hydrobiologia 755, 239–255.
Nile perch distribution in south-east Lake Victoria is more strongly driven by abiotic factors, than by prey densities.Crossref | GoogleScholarGoogle Scholar |

Davidsen, J. G., Plantalech Manel-la, N., Økland, F., Diserud, O. H., Thorstad, E. B., Finstad, B., Sivertsgård, R., McKinley, R. S., and Rikardsen, A. H. (2008). Changes in swimming depths of Atlantic salmon Salmo salar post-smolts relative to light intensity. Journal of Fish Biology 73, 1065–1074.
Changes in swimming depths of Atlantic salmon Salmo salar post-smolts relative to light intensity.Crossref | GoogleScholarGoogle Scholar |

de Lima Filho, J. A., Martins, J., Arruda, R., and Carvalho, L. N. (2012). Air-breathing behavior of the jeju fish Hoplerythrinus unitaeniatus in Amazonian streams. Biotropica 44, 512–520.
Air-breathing behavior of the jeju fish Hoplerythrinus unitaeniatus in Amazonian streams.Crossref | GoogleScholarGoogle Scholar |

del Carmen Hernandez, M., Alcocer, J., Oseguera, L. A., and Escobar, E. (2014). Profundal benthic invertebrates in an oligotrophic tropical lake: different strategies for coping with anoxia. Journal of Limnology 73, 387–399.

Domenici, P., Norin, T., Bushnell, P. G., Johansen, J. L., Skov, P. V., Svendsen, M. B. S., Steffensen, J. F., and Abe, A. S. (2015). Fast-starting after a breath: air-breathing motions are kinematically similar to escape responses in the catfish Hoplosternum littorale. Biology Open 4, 79–85.
Fast-starting after a breath: air-breathing motions are kinematically similar to escape responses in the catfish Hoplosternum littorale.Crossref | GoogleScholarGoogle Scholar |

Donaldson, M. R., Hinch, S. G., Suski, C. D., Fisk, A. T., Heupel, M. R., and Cooke, S. J. (2014). Making connections in aquatic ecosystems with acoustic telemetry monitoring. Frontiers in Ecology and the Environment 12, 565–573.
Making connections in aquatic ecosystems with acoustic telemetry monitoring.Crossref | GoogleScholarGoogle Scholar |

Duong, T. (2007). ks: kernel density estimation and kernel discriminant analysis for multivariate data in R. Journal of Statistical Software 21, 1–16.
ks: kernel density estimation and kernel discriminant analysis for multivariate data in R.Crossref | GoogleScholarGoogle Scholar |

Ekau, W., Auel, H., Poertner, H. O., and Gilbert, D. (2010). Impacts of hypoxia on the structure and processes in pelagic communities (zooplankton, macro-invertebrates and fish). Biogeosciences 7, 1669–1699.
Impacts of hypoxia on the structure and processes in pelagic communities (zooplankton, macro-invertebrates and fish).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtV2rtLjO&md5=efd92b5f2d35e7a664b85ccd92909292CAS |

Espinoza, M., Farrugia, T. J., Webber, D. M., Smith, F., and Lowe, C. G. (2011). Testing a new acoustic telemetry technique to quantify long-term, fine-scale movements of aquatic animals. Fisheries Research 108, 364–371.
Testing a new acoustic telemetry technique to quantify long-term, fine-scale movements of aquatic animals.Crossref | GoogleScholarGoogle Scholar |

Feng, D., and Tierney, L. (2008). Computing and displaying isosurfaces in R. Journal of Statistical Software 28, 1–24.
Computing and displaying isosurfaces in R.Crossref | GoogleScholarGoogle Scholar |

Fernandes-Castilho, M., and Eliane, G.-F., Cardoso Giaquinto, P., Feitosa de Oliveura, C. P., de Almeida-Val, V. M., and Val, A. L. (2007). Behavior and adaptation of air-breathing fishes. In ‘Fish Respiration and Environment’. (Eds M. Fernandes, F. Rantin, M. Glass, and B. Kapoor.) pp. 121–145. (Science Publishers: Enfield, NH, USA.)

Flint, N., Crossland, M. R., and Pearson, R. G. (2015). Sublethal effects of fluctuating hypoxia on juvenile tropical Australian freshwater fish. Marine and Freshwater Research 66, 293–304.
Sublethal effects of fluctuating hypoxia on juvenile tropical Australian freshwater fish.Crossref | GoogleScholarGoogle Scholar |

Fritsche, R., Axelsson, M., Franklin, C. E., Grigg, G. G., Holmgren, S., and Nilsson, S. (1993). Respiratory and cardiovascular responses to hypoxia in the Australian lungfish. Respiration Physiology 94, 173–187.
Respiratory and cardiovascular responses to hypoxia in the Australian lungfish.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2c%2Fpsl2lsw%3D%3D&md5=73891353885334be30c041dc729ecd48CAS |

Fujimoto, Y., and Iwata, M. (2005). Effect of natural light conditions on the use of cover in concrete block structures by Japanese dace Tribolodon hakonensis. Fisheries Science 71, 1019–1028.
Effect of natural light conditions on the use of cover in concrete block structures by Japanese dace Tribolodon hakonensis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFOrtLjP&md5=41eb2692093ec7f467b30a2b2c8c1bedCAS |

Graham, J. B. (1994). An evolutionary perspective for bimodal respiration: a biological synthesis of fish air breathing. American Zoologist 34, 229–237.
An evolutionary perspective for bimodal respiration: a biological synthesis of fish air breathing.Crossref | GoogleScholarGoogle Scholar |

Grigg, G. C. (1965). Studies on the Queensland lungfish, Neoceratodus forsteri (Krefft). 3. Aerial respiration in relation to habits. Australian Journal of Zoology 13, 413–422.
Studies on the Queensland lungfish, Neoceratodus forsteri (Krefft). 3. Aerial respiration in relation to habits.Crossref | GoogleScholarGoogle Scholar |

Harris, G. P., and Baxter, G. (1996). Interannual variability in phytoplankton biomass and species composition in a subtropical reservoir. Freshwater Biology 35, 545–560.
Interannual variability in phytoplankton biomass and species composition in a subtropical reservoir.Crossref | GoogleScholarGoogle Scholar |

Hasler, C. T., Midway, S. R., Jeffrey, J. D., Tix, J. A., Sullivan, C., and Suski, C. D. (2016). Exposure to elevated pCO2 alters post-treatment diel movement patterns of largemouth bass over short time scales. Freshwater Biology 61, 1590–1600.
Exposure to elevated pCO2 alters post-treatment diel movement patterns of largemouth bass over short time scales.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28Xht1yhtbzP&md5=e4d3f2eb8864ef74ed0b4fec73d791b8CAS |

Johannsson, O. E., Bergman, H. L., Wood, C. M., Laurent, P., Kavembe, D. G., Bianchini, A., Maina, J. N., Chevalier, C., Bianchini, L. F., Papah, M. B., and Ojoo, R. O. (2014). Air breathing in Magadi tilapia Alcolapia grahami, under normoxic and hyperoxic conditions, and the association with sunlight and reactive oxygen species. Journal of Fish Biology 84, 844–863.
Air breathing in Magadi tilapia Alcolapia grahami, under normoxic and hyperoxic conditions, and the association with sunlight and reactive oxygen species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXjvVOkurY%3D&md5=ebc3a7ea23420b883e01cbf23406135fCAS |

Kind, P. K. (2002). Movement patterns and habitat use in the Queensland lungfish Neoceratodus forsteri (Krefft 1870). Ph.D. Thesis, University of Queensland, Brisbane, Qld, Australia.

Kind, P. K. (2011). The natural history of the Australian Lungfish Neoceratodus forsteri (Krefft, 1870). In ‘Biology of Lungfishes’. (Eds J. M. Jorgensen and J. Joss.) pp. 61–96. (CRC Press: Enfield, NH, USA.)

Kind, P. K., Grigg, G. C., and Booth, D. T. (2002). Physiological responses to prolonged aquatic hypoxia in the Queensland lungfish Neoceratodus forsteri. Respiratory Physiology & Neurobiology 132, 179–190.
Physiological responses to prolonged aquatic hypoxia in the Queensland lungfish Neoceratodus forsteri.Crossref | GoogleScholarGoogle Scholar |

Knight, S. (2012). Movement and behaviour of Australian lungfish (Neoceratodus forsteri) in a modified system. B.Sc.(Hons) Thesis. Griffith University, Brisbane, Qld, Australia.

Kramer, D. L. (1987). Dissolved oxygen and fish behavior. Environmental Biology of Fishes 18, 81–92.
Dissolved oxygen and fish behavior.Crossref | GoogleScholarGoogle Scholar |

Lefevre, S., Huong, D. T. T., Ha, N. T. K., Wang, T., Phuong, N. T., and Bayley, M. (2011). A telemetry study of swimming depth and oxygen level in a Pangasius pond in the Mekong Delta. Aquaculture 315, 410–413.
A telemetry study of swimming depth and oxygen level in a Pangasius pond in the Mekong Delta.Crossref | GoogleScholarGoogle Scholar |

Lefevre, S., Huong, D. T. T., Phuong, N. T., Wang, T., and Bayley, M. (2012). Effects of hypoxia on the partitioning of oxygen uptake and the rise in metabolism during digestion in the air-breathing fish Channa striata. Aquaculture 364–365, 137–142.
Effects of hypoxia on the partitioning of oxygen uptake and the rise in metabolism during digestion in the air-breathing fish Channa striata.Crossref | GoogleScholarGoogle Scholar |

Lefevre, S., Wang, T., Huong, D. T. T., Phuong, N. T., and Bayley, M. (2013). Partitioning of oxygen uptake and cost of surfacing during swimming in the air-breathing catfish Pangasianodon hypophthalmus. Journal of Comparative Physiology ­– B. Biochemical, Systemic, and Environmental Physiology 183, 215–221.
Partitioning of oxygen uptake and cost of surfacing during swimming in the air-breathing catfish Pangasianodon hypophthalmus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvFOkt7w%3D&md5=f505128d37f2d3a45aa78bff4734367aCAS |

Lehner, B., Liermann, C. R., Revenga, C., Vorosmarty, C., Fekete, B., Crouzet, P., Doll, P., Endejan, M., Frenken, K., Magome, J., Nilsson, C., Robertson, J. C., Rodel, R., Sindorf, N., and Wisser, D. (2011). High-resolution mapping of the world’s reservoirs and dams for sustainable river-flow management. Frontiers in Ecology and the Environment 9, 494–502.
High-resolution mapping of the world’s reservoirs and dams for sustainable river-flow management.Crossref | GoogleScholarGoogle Scholar |

Liermann, C. R., Nilsson, C., Robertson, J., and Ng, R. Y. (2012). Implications of dam obstruction for global freshwater fish diversity. Bioscience 62, 539–548.
Implications of dam obstruction for global freshwater fish diversity.Crossref | GoogleScholarGoogle Scholar |

Littlejohn, C. L. (2004). Influence of artificial destratification on limnological processes in Lake Samsonvale (North Pine Dam), Queensland, Australia. M.Phil. Thesis, Griffith University, Brisbane, Qld, Australia.

Matley, J. K., Heupel, M. R., and Simpfendorfer, C. A. (2015). Depth and space use of leopard coral grouper Plectropomus leopardus using passive acoustic tracking. Marine Ecology Progress Series 521, 201–216.
Depth and space use of leopard coral grouper Plectropomus leopardus using passive acoustic tracking.Crossref | GoogleScholarGoogle Scholar |

Muller, R., and Stadelmann, P. (2004). Fish habitat requirements as the basis for rehabilitation of eutrophic lakes by oxygenation. Fisheries Management and Ecology 11, 251–260.
Fish habitat requirements as the basis for rehabilitation of eutrophic lakes by oxygenation.Crossref | GoogleScholarGoogle Scholar |

Müller, B., Bryant, L. D., Matzinger, A., and Wüest, A. (2012). Hypolimnetic oxygen depletion in eutrophic lakes. Environmental Science & Technology 46, 9964–9971.

Niezgoda, G., Benfield, M., Sisak, M., and Anson, P. (2002). Tracking acoustic transmitters by code division multiple access (CDMA)-based telemetry. Hydrobiologia 483, 275–286.
Tracking acoustic transmitters by code division multiple access (CDMA)-based telemetry.Crossref | GoogleScholarGoogle Scholar |

Nilsson, C., Reidy, C. A., Dynesius, M., and Revenga, C. (2005). Fragmentation and flow regulation of the world’s large river systems. Science 308, 405–408.
Fragmentation and flow regulation of the world’s large river systems.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjtFOnt7g%3D&md5=5976155184fd1f367c9e07ab7587e05fCAS |

Pinheiro, J., Bates, D., Debroy, S., Sarkar, D., and R Core Team (2016). nlme: linear and nonlinear mixed effects models. R package, ver. 3.1-128. Available at http://CRAN.R-project.org/package=nlme [Verified 20 March 2016].

Rahman, A. K. M., Al Bakri, D., Ford, P., and Church, T. (2005). Limnological characteristics, eutrophication and cyanobacterial blooms in an inland reservoir, Australia. Lakes and Reservoirs: Research and Management 10, 211–220.
Limnological characteristics, eutrophication and cyanobacterial blooms in an inland reservoir, Australia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtlWisbY%3D&md5=67a769558af963ddd8719212ef7abfbaCAS |

Raines, C. D., and Miranda, L. E. (2016). Role of riparian shade on the fish assemblage of a reservoir littoral. Environmental Biology of Fishes 99, 753–760.
Role of riparian shade on the fish assemblage of a reservoir littoral.Crossref | GoogleScholarGoogle Scholar |

Rankin, P. S., Hannah, R. W., and Blume, M. T. O. (2013). Effect of hypoxia on rockfish movements: implications for understanding the roles of temperature, toxins and site fidelity. Marine Ecology Progress Series 492, 223–234.
Effect of hypoxia on rockfish movements: implications for understanding the roles of temperature, toxins and site fidelity.Crossref | GoogleScholarGoogle Scholar |

Rechencq, M., Vigliano, P. H., Macchi, P. J., and Lippolt, G. E. (2014). Fish distribution patterns and habitat availability in lakes Moreno Este and Moreno Oeste, Patagonia, Argentina. Limnologica 49, 73–83.
Fish distribution patterns and habitat availability in lakes Moreno Este and Moreno Oeste, Patagonia, Argentina.Crossref | GoogleScholarGoogle Scholar |

Simpfendorfer, C. A., Olsen, E. M., Heupel, M. R., and Moland, E. (2012). Three-dimensional kernel utilization distributions improve estimates of space use in aquatic animals. Canadian Journal of Fisheries and Aquatic Sciences 69, 565–572.
Three-dimensional kernel utilization distributions improve estimates of space use in aquatic animals.Crossref | GoogleScholarGoogle Scholar |

Smith, J. A., Baumgartner, L. J., Suthers, I. M., and Taylor, M. D. (2011). Distribution and movement of a stocked freshwater fish: implications of a variable habitat volume for stocking programs. Marine and Freshwater Research 62, 1342–1353.
Distribution and movement of a stocked freshwater fish: implications of a variable habitat volume for stocking programs.Crossref | GoogleScholarGoogle Scholar |

Taabu-Munyaho, A., Kayanda, R. J., Everson, I., Grabowski, T. B., and Marteinsdottir, G. (2013). Distribution and exploitation of Nile perch Lates niloticus in relation to stratification in Lake Victoria, East Africa. Journal of Great Lakes Research 39, 466–475.
Distribution and exploitation of Nile perch Lates niloticus in relation to stratification in Lake Victoria, East Africa.Crossref | GoogleScholarGoogle Scholar |

Udyawer, V., Read, M., Hamann, M., Simpfendorfer, C. A., and Heupel, M. R. (2015). Effects of environmental variables on the movement and space use of coastal sea snakes over multiple temporal scales. Journal of Experimental Marine Biology and Ecology 473, 26–34.
Effects of environmental variables on the movement and space use of coastal sea snakes over multiple temporal scales.Crossref | GoogleScholarGoogle Scholar |

Veilleux, M. A. N., Lapointe, N. W. R., Webber, D. M., Binder, T. R., Blanchfield, P. J., Cruz-Font, L., Wells, M. G., Larsen, M. H., Doka, S. E., and Cooke, S. J. (2016). Pressure sensor calibrations of acoustic telemetry transmitters. Animal Biotelemetry 4, 3.
Pressure sensor calibrations of acoustic telemetry transmitters.Crossref | GoogleScholarGoogle Scholar |

Wantzen, K. M., Junk, W. J., and Rothhaupt, K.-O. (2008). An extension of the floodpulse concept (FPC) for lakes. Hydrobiologia 613, 151–170.
An extension of the floodpulse concept (FPC) for lakes.Crossref | GoogleScholarGoogle Scholar |

Zarfl, C., Lumsdon, A. E., Berlekamp, J., Tydecks, L., and Tockner, K. (2015). A global boom in hydropower dam construction. Aquatic Sciences 77, 161–170.
A global boom in hydropower dam construction.Crossref | GoogleScholarGoogle Scholar |