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Advances in the aquatic sciences
RESEARCH ARTICLE

Muddy waters: the influence of high suspended-sediment concentration on the diving behaviour of a bimodally respiring freshwater turtle from north-eastern Australia

Jason R. Schaffer A C , Mark Hamann B , Richard Rowe B and Damien W. Burrows A
+ Author Affiliations
- Author Affiliations

A TropWATER, James Cook University, Townsville, Queensland, Australia.

B College of Marine and Environmental Sciences, James Cook University, Australia.

C Corresponding author. Email: Jason.Schaffer1@jcu.edu.au

Marine and Freshwater Research 67(4) 505-512 https://doi.org/10.1071/MF14117
Submitted: 29 April 2014  Accepted: 23 February 2015   Published: 23 July 2015

Abstract

Increased suspended-sediment concentrations (SS) in rivers can affect aquatic respiration in riverine fauna by impairing respiratory function. Bimodally respiring freshwater turtles are likely to be sensitive to changes in SS because increased concentrations may affect their ability to aquatically respire. However, the impact of SS on the diving behaviour of bimodally respiring freshwater turtles has not been formally investigated. To test this, we examined the influence of dissolved oxygen (DO) saturation (25%, 100%) and temperature (17°C, 25°C) on the diving behaviour of Elseya irwini under clear (0 mg L–1) and turbid (79 mg L–1) conditions. We hypothesised that low temperature and high DO % saturation would increase dive duration and that high SS would negate the effect of DO, decreasing dive duration under highly oxygenated conditions. Our data demonstrated that increased SS significantly reduced mean dive duration by 73% (97.4 ± 10.1 min in 0 mg L–1 trials v. 26.4 ± 3.2 min in 79 mg L–1 trials) under conditions of low temperature (17°C) and high DO % saturation (100%) only. Increased SS directly affects the utilisation of DO by this species, so as to extend submergence times (aquatic respiration) under optimal conditions, raising concerns about the effect of SS on the persistence of populations of physiologically specialised freshwater turtles.

Additional keywords: aquatic respiration, dive duration, Elseya, turbidity.


References

Aldridge, D. W., Payne, B. S., and Miller, A. C. (1987). The effects of intermittent exposure to suspended solids and turbulence on three species of freshwater mussels’. Environmental Pollution 45, 17–28.
The effects of intermittent exposure to suspended solids and turbulence on three species of freshwater mussels’.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2c7psVOmtA%3D%3D&md5=addcf2ece941c6a55edfa6e3aee4bf56CAS | 15092759PubMed |

Allan, D. J. (2004). Landscapes and riverscapes: the influence of land use on stream ecosystems. Annual Review of Ecology Evolution and Systematics 35, 257–284.
Landscapes and riverscapes: the influence of land use on stream ecosystems.Crossref | GoogleScholarGoogle Scholar |

Au, D. W. T., Pollino, C. A., Wu, R. S. S., Shin, P. K. S., Lau, S. T. F., and Tang, J. Y. M. (2004). Chronic effects of suspended solids on gill structure, osmoregulation, growth, and triiodothyronine in juvenile green grouper Epinephelus coioides. Marine Ecology Progress Series 266, 255–264.
Chronic effects of suspended solids on gill structure, osmoregulation, growth, and triiodothyronine in juvenile green grouper Epinephelus coioides.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjs12ktL0%3D&md5=790b7a18df25c92786d336754ff698feCAS |

Baayen, H. R. (2009). ‘LanguageR. R Package.’ R available online at http://www.r-project.org/

Bagatto, B., Guyer, C., Hauge, B., and Henry, R. P. (1997). Bimodal respiration in two species of central American turtles. Copeia 1997, 834–839.
Bimodal respiration in two species of central American turtles.Crossref | GoogleScholarGoogle Scholar |

Bainbridge, Z., Lewis, S., and Brodie, J. (2007). Event-based community water quality monitoring in the Burdekin Dry Tropics Region: 2002–2007 (Vol. 2). ACTFR report number 07/22 for the Burdekin Dry Tropics NRM. Australian Centre for Tropical Freshwater Research, James Cook University, Townsville, Qld.

Bates, D., Maechler, M. (2009). ‘lme4: Linear Mixed-effects Models using S4 Classes. R Package Version 0.999375-31. [Software]. Available at http://cran.r-project.org/web/packages/lme4/index.html

Belkin, D. A. (1968). Aquatic respiration and underwater survival of two freshwater turtle species. Respiration Physiology 4, 1–14.
Aquatic respiration and underwater survival of two freshwater turtle species.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaF1c7lsV2lsA%3D%3D&md5=d89434278e0a6799c2a5f9e18a634280CAS | 5639522PubMed |

Berg, L., and Northcote, T. G. (1985). Changes in territorial, gill-flaring, and feeding behavior in juvenile coho salmon (Oncorhynchus kisutch) following short-term pulses of suspended sediment. Canadian Journal of Fisheries and Aquatic Sciences 42, 1410–1417.
Changes in territorial, gill-flaring, and feeding behavior in juvenile coho salmon (Oncorhynchus kisutch) following short-term pulses of suspended sediment.Crossref | GoogleScholarGoogle Scholar |

Bodie, J. R. (2001). Stream and riparian management for freshwater turtles. Journal of Environmental Management 62, 443–455.
Stream and riparian management for freshwater turtles.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MvmtFCitQ%3D%3D&md5=852e85ea7d87691b38c490d9b2a02be6CAS | 11505769PubMed |

Bruton, M. N. (1985). The effects of suspensoids on fish. Hydrobiologia 125, 221–241.
The effects of suspensoids on fish.Crossref | GoogleScholarGoogle Scholar |

Butler, P. J., and Jones, D. R. (1982). The comparative physiology of diving in vertebrates. In ‘Advances in Comparative Physiology and Biochemistry‘. (Ed. O. Lowenstein.) pp. 179–364. (Academic Press: New York.)

Cann, J. (1997). Irwin’s turtle. Elseya irwini sp. nov. Holotype Q.M. J59431 collected by J. Cann, October 1993. Monitor 9, 36–40.

Clark, N. J., Gordos, M. A., and Franklin, C. E. (2008a). Thermal plasticity of diving behaviour, aquatic respiration, and locomotor performance in the Mary River turtle Elusor macrurus. Physiological and Biochemical Zoology 81, 301–309.
Thermal plasticity of diving behaviour, aquatic respiration, and locomotor performance in the Mary River turtle Elusor macrurus.Crossref | GoogleScholarGoogle Scholar | 18419556PubMed |

Clark, N. J., Gordos, M. A., and Franklin, C. E. (2008b). Diving behaviour, aquatic respiration, and blood respiratory properties: a comparison of hatchling and juvenile Australian turtles. Journal of Zoology (London, England) 275, 399–406.
Diving behaviour, aquatic respiration, and blood respiratory properties: a comparison of hatchling and juvenile Australian turtles.Crossref | GoogleScholarGoogle Scholar |

Clark, N. J., Gordos, M. A., and Franklin, C. E. (2009). Implications of river damming: the influence of aquatic hypoxia on the diving physiology and behaviour of the endangered Mary River turtle. Animal Conservation 12, 147–154.
Implications of river damming: the influence of aquatic hypoxia on the diving physiology and behaviour of the endangered Mary River turtle.Crossref | GoogleScholarGoogle Scholar |

Dejours, P. (1994). Environmental factors as determinants in bimodal breathing – an introductory overview. American Zoologist 34, 178–183.

DERM (2014). Available at http://watermonitoring.dnrm.qld.gov.au/host.htm [Accessed 6 February 2015]

Dunlop, J., McGregor, G., and Horrigan, N. (2005). ‘Potential Impacts of Salinity and Turbidity in Riverine Ecosystems: Characterisation of Impacts and a Discussion of Regional Target Setting for Riverine Ecosystems in Queensland.’ (Queensland Department of Natural Resources and Mines, Brisbane, Australia.)

Ehrenfeld, D. W. (1970). ‘Biological Conservation.’ (Holt, Rinehart, & Winston: New York.)

Farley, S. M. (2004). Conservation genetics of the snapping turtle (Elseya sp.): an assessment of genetic diversity and population structure. B.Sc.(Hons) thesis, Applied Ecology Research Group, The University of Canberra, Canberra.

Fielder, D. P. (2012). Seasonal and diel dive performance and behavioral ecology of the bimodally respiring freshwater turtle Myuchelys bellii of eastern Australia. Journal of Comparative Physiology. A, Neuroethology, Sensory, Neural, and Behavioral Physiology 198, 129–143.
Seasonal and diel dive performance and behavioral ecology of the bimodally respiring freshwater turtle Myuchelys bellii of eastern Australia.Crossref | GoogleScholarGoogle Scholar | 22045114PubMed |

FitzGibbon, S. I., and Franklin, C. E. (2010). The importance of the cloacal bursae as the primary site of aquatic respiration in the freshwater turtle, Elseya albagula. Australian Journal of Zoology 35, 276–282.
The importance of the cloacal bursae as the primary site of aquatic respiration in the freshwater turtle, Elseya albagula.Crossref | GoogleScholarGoogle Scholar |

Goldes, S. A., Ferguson, H. W., Moccia, R. D., and Daoust, P. Y. (1988). Histological effects of the inert suspended clay kaolin on the gills of juvenile rainbow trout, Salmo gairdneri Richardson. Journal of Fish Diseases 11, 23–33.
Histological effects of the inert suspended clay kaolin on the gills of juvenile rainbow trout, Salmo gairdneri Richardson.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXitFOnsbo%3D&md5=a333dd36dbc27952ec664f8ef7d3bfc8CAS |

Gordos, M., and Franklin, C. E. (2002). Diving behaviour of two Australian bimodally respiring turtles, Rheodytes leukops and Emydura macquarii, in a natural setting. Journal of Zoology 258, 335–342.
Diving behaviour of two Australian bimodally respiring turtles, Rheodytes leukops and Emydura macquarii, in a natural setting.Crossref | GoogleScholarGoogle Scholar |

Gordos, M., Franklin, C. E., and Limpus, C. (2003). Seasonal changes in the diving performance of the bimodally respiring freshwater turtle Rheodytes leukops in a natural setting. Canadian Journal of Zoology 81, 617–625.
Seasonal changes in the diving performance of the bimodally respiring freshwater turtle Rheodytes leukops in a natural setting.Crossref | GoogleScholarGoogle Scholar |

Gordos, M. A., Limpus, C. J., and Franklin, C. E. (2006). Response of heart rate and cloacal ventilation in the bimodally respiring freshwater turtle, Rheodytes leukops, to experimental changes in aquatic PO2. Journal of Comparative Physiology 176, 65–73.
Response of heart rate and cloacal ventilation in the bimodally respiring freshwater turtle, Rheodytes leukops, to experimental changes in aquatic PO2.Crossref | GoogleScholarGoogle Scholar | 16235043PubMed |

Gordos, M. A., Hamann, M., Schauble, C. S., Franklin, C. E., and Limpus, C. J. (2007). Diving ecology of an undescribed freshwater turtle, Elseya sp. [Burnett River], from a pristine and hydrologically altered habitat. Journal of Zoology 272, 458–469.
Diving ecology of an undescribed freshwater turtle, Elseya sp. [Burnett River], from a pristine and hydrologically altered habitat.Crossref | GoogleScholarGoogle Scholar |

Grosse, A. M., Sterrett, S. C., and Maerz, J. C. (2010). Effects of turbidity on the foraging success of the eastern painted turtle. Copeia 3, 463–467.
Effects of turbidity on the foraging success of the eastern painted turtle.Crossref | GoogleScholarGoogle Scholar |

Hamann, M., Schauble, C., Emerick, S., Limpus, D., and Limpus, C. (2008). Freshwater turtle populations in the Burnett River. Memoirs of the Queensland Museum 52, 221.

Henley, W. F., Patterson, M. A., Neves, R. J., and Lemly, A. D. (2000). Effects of sedimentation and turbidity on lotic food webs: a concise review for natural resource managers. Reviews in Fisheries Science 8, 125.
Effects of sedimentation and turbidity on lotic food webs: a concise review for natural resource managers.Crossref | GoogleScholarGoogle Scholar |

Herbert, D. W., and Merkens, J. C. (1961). The effect of suspended mineral solids on the survival of trout. International Journal of Air and Water Pollution 5, 46–55.
| 1:STN:280:DyaF38%2FkvVSisg%3D%3D&md5=fc50914509edad4aa9eaeadf8556af57CAS | 13906627PubMed |

King, P., and Heatwole, H. (1994). Non-pulmonary respiratory surfaces of the chelid turtle Elseya latisternum. Herpetologica 50, 262.

Kleiber, M. (1965). Metabolic body size. In ‘Energy Metabolism’. (Ed. K. L Blaxter.) pp. 427–435. (Academic Press: London.)

Kramer, D. L. (1988). The behavioral ecology of air breathing by aquatic animals. Canadian Journal of Zoology 66, 89–94.
The behavioral ecology of air breathing by aquatic animals.Crossref | GoogleScholarGoogle Scholar |

Legler, J. M., and Georges, A. (1993). Family Chelidae. In ‘Fauna of Australia. Vol. 2A: Amphibians and Reptiles: 142’. (Eds C. Glasby, G. Ross, P. Beesley.) pp. 142–152. (Australian Government Printing Service: Canberra.)

Ligon, F. K., Dietrich, W. E., and Trush, W. J. (1995). Downstream ecological effects of dams. Bioscience 45, 183–192.
Downstream ecological effects of dams.Crossref | GoogleScholarGoogle Scholar |

Limpus, C., Limpus, D., and Hamann, M. (2002). Freshwater turtle populations in the area to be flooded by the Walla Weir, Burnett River, Queensland: baseline study. Memoirs of the Queensland Museum 48, 155.

Lin, H.-P., Charmantier, G., Thuet, P., and Trilles, J. P. (1992). Effects of turbidity on survival, osmoregulation and gill NA+-K+ ATPase in juvenile shrimp Penaeus japonicus. Marine Ecology Progress Series 90, 31–37.
Effects of turbidity on survival, osmoregulation and gill NA+-K+ ATPase in juvenile shrimp Penaeus japonicus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXktVGhtrc%3D&md5=c7a153db39fa210169b74378c301804dCAS |

Magoulick, D. D., and Kobza, R. M. (2003). The role of refugia for fishes during drought: a review and synthesis. Freshwater Biology 48, 1186–1198.
The role of refugia for fishes during drought: a review and synthesis.Crossref | GoogleScholarGoogle Scholar |

Mathie, N. J., and Franklin, C. E. (2006). The influence of body size on the diving behaviour and physiology of the bimodally respiring turtle, Elseya albagula. Journal of Comparative Physiology. B, Biochemical, Systemic, and Environmental Physiology 176, 739–747.
The influence of body size on the diving behaviour and physiology of the bimodally respiring turtle, Elseya albagula.Crossref | GoogleScholarGoogle Scholar | 16791587PubMed |

McKinney, M. L. (1997). Extinction vulnerability and selectivity: combining ecological and paleontological views. Annual Review of Ecology and Systematics 28, 495–516.
Extinction vulnerability and selectivity: combining ecological and paleontological views.Crossref | GoogleScholarGoogle Scholar |

McLeay, D. J., Birtwell, I. K., Hartman, G. F., and Ennis, G. L. (1987). Responses of Arctic grayling (Thymallus arcticus) to acute and prolonged exposure to Yukon placer mining sediment. Canadian Journal of Fisheries and Aquatic Sciences 44, 658–673.
Responses of Arctic grayling (Thymallus arcticus) to acute and prolonged exposure to Yukon placer mining sediment.Crossref | GoogleScholarGoogle Scholar |

Moll, D., and Moll, E. O. (2004). ‘The Ecology, Exploitation, and Conservation of River Turtles.’ (Oxford University Press: New York.)

Newcombe, C. P., and MacDonald, D. D. (1991). Effects of suspended sediments on aquatic ecosystems. North American Journal of Fisheries Management 11, 72–82.
Effects of suspended sediments on aquatic ecosystems.Crossref | GoogleScholarGoogle Scholar |

Packett, R. (2007). A mouthful of mud: the fate of contaminants from the Fitzroy River, Queensland, Australia and implications for reef water policy. In ‘Proceedings of the 5th Australian Stream Management Conference. Australian Rivers: Making a Difference’. (Eds A. L. Wilson, R. L. Dehaan, R. J. Watts, K. J. Page, K. H. Bowmer and A. Curtis.) pp. 294–299. (Charles Sturt University: Thurgoona, NSW.)

Prassack, S. L., Bagatto, B., and Henry, R. P. (2001). Effects of temperature and aquatic Po-2 on the physiology and behaviour of Apalone ferox and Chrysemys picta. The Journal of Experimental Biology 204, 2185.
| 1:STN:280:DC%2BD3Mzos12isg%3D%3D&md5=a7334a3e3138fc6a8a975ae99633e426CAS | 11441060PubMed |

Priest, T. (1997). Bimodal respiration and dive behaviour of the Fitzroy River turtle, Rheodytes leukops. B.Sc. (Hons) Thesis, Department of Zoology, The University of Queensland, Brisbane.

Priest, T., and Franklin, C. E. (2002). Effect of water temperature and oxygen levels on the diving behaviour of two freshwater turtles: Rheodytes leukops and Emydura maquarii. Journal of Herpetology 36, 555–561.
Effect of water temperature and oxygen levels on the diving behaviour of two freshwater turtles: Rheodytes leukops and Emydura maquarii.Crossref | GoogleScholarGoogle Scholar |

R Core Team (2014). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available at http://www.R-project.org/

Reese, D. A., and Welsh, H.H. Jr. (1998). Habitat use by western pond turtles in the Trinity River, California. The Journal of Wildlife Management 62, 842–853.
Habitat use by western pond turtles in the Trinity River, California.Crossref | GoogleScholarGoogle Scholar |

Schmidt-Nielsen, K. (1997). ‘Animal Physiology: Adaptation and Environment.’ (Cambridge University Press: Cambridge, UK.)

Schreer, J. F., and Kovacs, K. M. (1997). Allometry of diving capacity in air-breathing vertebrates. Canadian Journal of Zoology 75, 339–358.
Allometry of diving capacity in air-breathing vertebrates.Crossref | GoogleScholarGoogle Scholar |

Servizi, J. A., and Martens, D. W. (1992). Sublethal responses of coho salmon (Oncorhynchus kisutch) to suspended sediments. Canadian Journal of Fisheries and Aquatic Sciences 49, 1389–1395.
Sublethal responses of coho salmon (Oncorhynchus kisutch) to suspended sediments.Crossref | GoogleScholarGoogle Scholar |

Storey, E. M., Kayes, S. M., De Vries, I., and Franklin, C. E. (2008). Effect of water depth, velocity and temperature on the surfacing frequency of the bimodally respiring turtle Elseya albagula. Functional Ecology 22, 840–846.
Effect of water depth, velocity and temperature on the surfacing frequency of the bimodally respiring turtle Elseya albagula.Crossref | GoogleScholarGoogle Scholar |

Sutherland, A., and Meyer, J. (2007). Effects of increased suspended sediment on growth rate and gill condition of two southern Appalachian minnows. Environmental Biology of Fishes 80, 389–403.
Effects of increased suspended sediment on growth rate and gill condition of two southern Appalachian minnows.Crossref | GoogleScholarGoogle Scholar |

Tucker, A. D. (1999). ‘Cumulative Effects of Dams and Weirs on Freshwater Turtle Populations: Fitzroy, Kolan, Burnett and Mary River Catchments.’ (Queensland Parks and Wildlife Service, Queensland Department of Natural Resources: Brisbane.)

Ultsch, G. R. (1985). The viability of nearctic freshwater turtles submerged in anoxia and normoxia at 3 and 10°C. Comparative Biochemistry and Physiology. A. Comparative Physiology 81, 607–611.
The viability of nearctic freshwater turtles submerged in anoxia and normoxia at 3 and 10°C.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL2M3otlKrtA%3D%3D&md5=21fbc4b276f7352ef28a95ddd14dafe6CAS | 2863050PubMed |

Ward, J. V., and Stanford, J. A. (1989). Riverine ecosystems: the influence of man on catchment dynamics and fish ecology. Canadian Special Publication of Fisheries and Aquatic Sciences 106, 56–64.

Wikelski, M., and Cooke, S. J. (2006). Conservation physiology. Trends in Ecology & Evolution 21, 38–46.
Conservation physiology.Crossref | GoogleScholarGoogle Scholar |

Wood, P. J., and Armitage, P. D. (1997). Biological effects of fine sediment in the lotic environment. Environmental Management 21, 203–217.
Biological effects of fine sediment in the lotic environment.Crossref | GoogleScholarGoogle Scholar | 9008071PubMed |