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Advances in the aquatic sciences
RESEARCH ARTICLE

Trophic relationships of the platypus: insights from stable isotope and cheek pouch dietary analyses

Melissa Klamt A E , Jenny A. Davis B , Ross M. Thompson B , Richard Marchant C and Tom R. Grant D
+ Author Affiliations
- Author Affiliations

A School of Biological Sciences, Monash University, Clayton, Vic. 3800, Australia.

B Institute for Applied Ecology, University of Canberra, ACT 2601, Australia.

C Sciences Department, Museum Victoria, Melbourne, Vic. 3001, Australia.

D Biological, Earth and Environmental Sciences, University of New South Wales, Sydney, NSW 2052, Australia.

E Corresponding author: melissa.klamt@monash.edu

Marine and Freshwater Research 67(8) 1196-1204 https://doi.org/10.1071/MF15004
Submitted: 11 November 2013  Accepted: 28 March 2015   Published: 4 September 2015

Abstract

The unique Australian monotreme, the platypus (Ornithorhynchus anatinus) potentially exerts a strong top-down influence on riverine food webs in eastern Australia. However, despite considerable interest in the evolutionary history and physiology of the platypus, little is known of its trophic relationships. To address this lack of knowledge we used stable isotope analysis, in combination with the analysis of food items stored in cheek pouches, to determine its position in a typical riverine food web. This was the essential first step in the process of designing a larger study to investigate the relative importance of top-down and bottom-up effects in rivers where the platypus occurs. We found that platypuses were feeding on a wide range of benthic invertebrates, particularly insect larvae. The similarity of δ13C and δ15N values recorded for the platypus, a native fish (Galaxias sp.) and the exotic mosquitofish (Gambusia holbrooki) indicated dietary overlap and potential competition for the same resources. Although cheek pouch studies identify most of the major groups of prey organisms, the potential for contribution of the soft-bodied organisms such as larval dipterans, is suggested by stable isotope analysis, indicating that the use of both techniques will be important in future ecological investigations.

Additional keywords: diet, δ13C, δ15N, macroinvertebrate, Ornithorhynchus anatinus.


References

Bethge, P., Munks, S., Otley, H., and Nicol, S. (2003). Diving behaviour, dive cycles and aerobic dive limit in the platypus Ornithorhynchus anatinus. Comparative Biochemistry and Physiology Part A 136, 799–809.
Diving behaviour, dive cycles and aerobic dive limit in the platypus Ornithorhynchus anatinus.Crossref | GoogleScholarGoogle Scholar |

Brodersen, K. P., and Lindegaard, C. (1999). Classification, assessment and trophic reconstruction of Danish lakes using chironomids. Freshwater Biology 42, 143–157.
Classification, assessment and trophic reconstruction of Danish lakes using chironomids.Crossref | GoogleScholarGoogle Scholar |

Bunn, S. E., and Boon, P. I. (1993). What sources of organic carbon drive food webs in billabongs? A study based on stable isotope analysis. Oecologia 96, 85–94.
What sources of organic carbon drive food webs in billabongs? A study based on stable isotope analysis.Crossref | GoogleScholarGoogle Scholar |

Caut, S., Angulo, E., and Courchamp, F. (2009). Variation in discrimination factors (Δ15N and Δ13C): the effect of diet isotopic values and applications for diet reconstruction. Journal of Applied Ecology 46, 443–453.
Variation in discrimination factors (Δ15N and Δ13C): the effect of diet isotopic values and applications for diet reconstruction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXkslGgu7k%3D&md5=4cca29ad67b7f90e0223111c5859becbCAS |

Churchfield, S., and Rychlik, L. (2006). Diets and coexistence in Neomys and Sorex shrews in Bialowieża forest, eastern Poland. Journal of Zoology 269, 381–390.
Diets and coexistence in Neomys and Sorex shrews in Bialowieża forest, eastern Poland.Crossref | GoogleScholarGoogle Scholar |

Churchfield, S., Rychlik, L., Yavrouyan, E., and Turlejski, K. (2006). First results on the feeding ecology of the Transcaucasian water shrew Neomys teres (Soricomorpha: Soricidae) from Armenia. Canadian Journal of Zoology 84, 1853–1858.
First results on the feeding ecology of the Transcaucasian water shrew Neomys teres (Soricomorpha: Soricidae) from Armenia.Crossref | GoogleScholarGoogle Scholar |

Diehl, S. (1992). Fish predation and benthic community structure: the role of omnivory and habitat complexity. Ecology 73, 1646–1661.
Fish predation and benthic community structure: the role of omnivory and habitat complexity.Crossref | GoogleScholarGoogle Scholar |

Faragher, R. A., Grant, T. R., and Carrick, F. N. (1979). Food of the platypus (Ornithorhynchus anatinus) with notes on the food of brown trout (Salmo trutta) in the Shoalhaven River, N.S.W. Australian Journal of Ecology 4, 171–179.
Food of the platypus (Ornithorhynchus anatinus) with notes on the food of brown trout (Salmo trutta) in the Shoalhaven River, N.S.W.Crossref | GoogleScholarGoogle Scholar |

Finlay, J. C. (2001). Stable-carbon-isotope ratios of river biota: implications for energy flow in lotic food webs. Ecology 82, 1052–1064.

Grant, T. R. (1982). Food of the platypus, Ornithorhynchus anatinus (Ornithorhynchidae: Monotremata) from various water bodies in New South Wales. Australian Mammalogy 5, 135–136.

Grant, T. R. (2007). ‘Platypus’, 4th edn. (CSIRO Publishing: Melbourne.)

Grant, T. R., and Carrick, F. N. (1974). Capture and marking of the platypus, Ornithorhynchus anatinus, in the wild. Australian Zoologist 18, 133–135.

Grant, T. R., and Carrick, F. N. (1978). Some aspects of the ecology of the platypus, Ornithorhynchus anatinus in the upper Shoalhaven River, New South Wales. Australian Zoologist 20, 181–199.

Grant, T. R., and Dawson, T. J. (1978). Temperature regulation in the platypus, Ornithorhynchus anatinus, production and loss of metabolic heat in air and water. Physiological Zoology 51, 315–332.

Grant, T. R., and Temple-Smith, P. D. (1998). Field biology of the platypus (Ornithorhynchus anatinus): historical and current perspectives. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 353, 1081–1091.
Field biology of the platypus (Ornithorhynchus anatinus): historical and current perspectives.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1czos1Gktw%3D%3D&md5=d5ba23b91363159b918be8a3ae03fe43CAS | 9720106PubMed |

Grant, T. R., Williams, R., and Carrick, F. N. (1977). Maintenance of the platypus, Ornithorhynchus anatinus in captivity under laboratory conditions. Australian Zoologist 19, 117–124.

Griffiths, M. (1978). ‘The Biology of the Monotremes.’ (Academic Press: New York.)

Hamilton, S. K., Lewis, W. M., and Sippel, S. J. (1992). Energy sources for the aquatic animals in the Orinoco River floodplain: evidence from stable isotopes. Oecologia 89, 324–330.
Energy sources for the aquatic animals in the Orinoco River floodplain: evidence from stable isotopes.Crossref | GoogleScholarGoogle Scholar |

Harvey, B. C., and Marti, C. D. (1993). The impact of dipper, Cinclus mexicanus, predation on stream benthos. Oikos 68, 431–436.
The impact of dipper, Cinclus mexicanus, predation on stream benthos.Crossref | GoogleScholarGoogle Scholar |

Hilderbrand, G. V., Schwartz, C. C., Robbins, C. T., Jacoby, M. E., Hanley, T. A., Arthur, S. M., and Servheen, C. (1999). The importance of meat, particularly salmon, to body size, population productivity, and conservation of North American brown bears. Canadian Journal of Zoology 77, 132–138.
The importance of meat, particularly salmon, to body size, population productivity, and conservation of North American brown bears.Crossref | GoogleScholarGoogle Scholar |

Ho, S. S. (2011). Comparative food web impacts of a native and an invasive fish in dynamic floodplain wetlands. Ph.D. thesis, Monash University, Melbourne.

Holland, N., and Jackson, S. M. (2002). Reproductive behaviour and food consumption associated with captive breeding of platypus (Ornithorhynchus anatinus). Journal of Zoology 256, 279–288.
Reproductive behaviour and food consumption associated with captive breeding of platypus (Ornithorhynchus anatinus).Crossref | GoogleScholarGoogle Scholar |

Hulbert, A. J., and Grant, T. R. (1983). A seasonal study of body condition and water turnover in a free-living population of platypuses, Ornithorhynchus anatinus (Monotremata). Australian Journal of Zoology 31, 109–116.
A seasonal study of body condition and water turnover in a free-living population of platypuses, Ornithorhynchus anatinus (Monotremata).Crossref | GoogleScholarGoogle Scholar |

Jefferies, R. L. (2000). Allochthonous inputs: integrating population changes and food-web dynamics. Trends in Ecology & Evolution 15, 19–22.
Allochthonous inputs: integrating population changes and food-web dynamics.Crossref | GoogleScholarGoogle Scholar |

Jones, F. W. (1923). ‘The Mammals of South Australia’. Reprint 1968. (Government Printer: Adelaide.)

Krueger, B., Hunter, S., and Serena, M. (1992). Husbandry, diet and behaviour of platypus Ornithorhynchus anatinus, at Healesville sanctuary. International Zoo Yearbook 31, 64–71.
Husbandry, diet and behaviour of platypus Ornithorhynchus anatinus, at Healesville sanctuary.Crossref | GoogleScholarGoogle Scholar |

Lewis, W. M., Hamilton, S. K., Lasi, M. A., Rodriguez, M., and Saunders, J. F. I. (2000). Ecological determinism on the Orinoco floodplain. Bioscience 50, 681–692.
Ecological determinism on the Orinoco floodplain.Crossref | GoogleScholarGoogle Scholar |

Lobinske, R. J., Chichra, C. E., and Ali, A. (2002). Predation by bluegill (Lepomis macrochirus) on larval Chironomidae (Diptera) in relation to midge standing crop in two central Florida Lakes. The Florida Entomologist 85, 372–375.
Predation by bluegill (Lepomis macrochirus) on larval Chironomidae (Diptera) in relation to midge standing crop in two central Florida Lakes.Crossref | GoogleScholarGoogle Scholar |

Marchant, R., and Grant, T. (2015). The productivity of the macroinvertebrate prey of the platypus in the upper Shoalhaven River, New South Wales. Marine and Freshwater Research , .
The productivity of the macroinvertebrate prey of the platypus in the upper Shoalhaven River, New South Wales.Crossref | GoogleScholarGoogle Scholar |

Mazumder, D., Johansen, M., Saintilan, N., Iles, J., Kobayashi, T., Knowles, L., and Wen, L. (2012). Trophic shifts involving native and exotic fish during hydrologic recession in floodplain wetlands. Wetlands 32, 267–275.
Trophic shifts involving native and exotic fish during hydrologic recession in floodplain wetlands.Crossref | GoogleScholarGoogle Scholar |

McCutchan, J. H., and Lewis, W. M. (2002). Relative importance of carbon sources for macroinvertebrates in a Rocky Mountain stream. Limnology and Oceanography 47, 742–752.
Relative importance of carbon sources for macroinvertebrates in a Rocky Mountain stream.Crossref | GoogleScholarGoogle Scholar |

McDowall, R. (1996). ‘Freshwater Fishes of South-Eastern Australia.’ (A. H. and A. W. Reed: Sydney.)

Mcilwee, A. P., and Johnson, C. N. (1998). The contribution of fungus to the diets of three mycophagous marsupials in Eucalyptus forests, revealed by stable isotope analysis. Functional Ecology 12, 223–231.
The contribution of fungus to the diets of three mycophagous marsupials in Eucalyptus forests, revealed by stable isotope analysis.Crossref | GoogleScholarGoogle Scholar |

McLachlan-Troup, T. (2007). The ecology and functional importance of the platypus (Ornithorhynchus anatinus) in Australian freshwater habitats. Ph.D. thesis, University of Sydney.

McLachlan-Troup, T. A., Dickman, C. R., and Grant, T. R. (2010). Diet and dietary selectivity of the platypus in relation to season, sex and macroinvertebrate assemblages. Journal of Zoology 280, 237–246.
Diet and dietary selectivity of the platypus in relation to season, sex and macroinvertebrate assemblages.Crossref | GoogleScholarGoogle Scholar |

Munks, S. A., Otley, H. M., Bethge, P., and Jackson, J. (2000). Reproduction, diet and daily energy expenditure of the platypus in a sub-alpine Tasmanian lake. Australian Mammalogy 21, 260–261.

Murphy, B. P., Bowman, D. M. J. S., and Gagan, M. K. (2007). The interactive effect of temperature and humidity on the oxygen isotope composition of kangaroos. Functional Ecology 21, 757–766.
The interactive effect of temperature and humidity on the oxygen isotope composition of kangaroos.Crossref | GoogleScholarGoogle Scholar |

Nyström, P., McIntosh, A. R., and Winterbourn, M. J. (2003). Top-down and bottom-up processes in grassland and forested streams. Oecologia 136, 596–608.
Top-down and bottom-up processes in grassland and forested streams.Crossref | GoogleScholarGoogle Scholar | 12802674PubMed |

Ormerod, S. J., and Tyler, S. J. (1991). Exploitation of prey by a river bird, the dipper Cinclus cinclus (L.), along acidic and circumneutral streams in upland Wales. Freshwater Biology 25, 105–116.
Exploitation of prey by a river bird, the dipper Cinclus cinclus (L.), along acidic and circumneutral streams in upland Wales.Crossref | GoogleScholarGoogle Scholar |

Ormerod, S. J., O’ Halloran, J., Gribbin, S. D., and Tyler, S. J. (1991). The ecology of dippers Cinclus cinclus in relation to stream acidity in upland Wales: breeding performance, calcium physiology and nestling growth. Journal of Applied Ecology 28, 419–433.
The ecology of dippers Cinclus cinclus in relation to stream acidity in upland Wales: breeding performance, calcium physiology and nestling growth.Crossref | GoogleScholarGoogle Scholar |

Pate, F. D., and Anson, T. J. (2008). Stable nitrogen isotope values in arid-land kangaroos correlated with mean annual rainfall: potential as a palaeoclimatic indicator. International Journal of Osteoarchaeology 18, 317–326.
Stable nitrogen isotope values in arid-land kangaroos correlated with mean annual rainfall: potential as a palaeoclimatic indicator.Crossref | GoogleScholarGoogle Scholar |

Peckarsky, B. L., and McIntosh, A. R. (1998). Fitness and community consequences of avoiding multiple predators. Oecologia 113, 565–576.
Fitness and community consequences of avoiding multiple predators.Crossref | GoogleScholarGoogle Scholar |

Peterson, B. J., and Fry, B. (1987). Stable isotopes in ecosystem studies. Annual Review of Ecology and Systematics 18, 293–320.
Stable isotopes in ecosystem studies.Crossref | GoogleScholarGoogle Scholar |

Phillips, D. L., Inger, R., Bearhop, S., Jackson, A. L., Moore, J. W., Parnell, A. C., Semmens, B. X., and Ward, E. J. (2014). Best practices for use of stable isotope mixing models in food-web studies. Canadian Journal of Zoology 92, 823–835.
Best practices for use of stable isotope mixing models in food-web studies.Crossref | GoogleScholarGoogle Scholar |

Post, D. M. (2002). Using stable isotopes to estimate trophic position: models, methods and assumptions. Ecology 83, 703–718.
Using stable isotopes to estimate trophic position: models, methods and assumptions.Crossref | GoogleScholarGoogle Scholar |

Power, M. E. (1992a). Habitat heterogeneity and the functional significance of fish in river food webs. Ecology 73, 1675–1688.
Habitat heterogeneity and the functional significance of fish in river food webs.Crossref | GoogleScholarGoogle Scholar |

Power, M. E. (1992b). Top-down and bottom-up forces in food webs: do plants have primacy? Ecology 73, 733–746.
Top-down and bottom-up forces in food webs: do plants have primacy?Crossref | GoogleScholarGoogle Scholar |

Power, M. E., Parker, M. S., and Dietrich, W. E. (2008). Seasonal reassembly of a river food web: floods, droughts, and impacts of fish. Ecological Monographs 78, 263–282.
Seasonal reassembly of a river food web: floods, droughts, and impacts of fish.Crossref | GoogleScholarGoogle Scholar |

Quinn, G. P., and Keough, M. J. (2002). ‘Experimental Design and Data Analysis for Biologists.’ (Cambridge University Press: New York.)

R Development Core Team (2008). R: a language and environment for statistical computing (R version 3.1.0). R Foundation for Statistical Computing, Vienna, Austria. Available at http://www.R-project.org [Verified June 2014].

Reid, D. J., Quinn, G., Lake, P. S., and Reich, P. (2008). Terrestrial detritus supports the food webs in lowland intermittent streams of south-eastern Australia: a stable isotope study. Freshwater Biology 53, 2036–2050.
Terrestrial detritus supports the food webs in lowland intermittent streams of south-eastern Australia: a stable isotope study.Crossref | GoogleScholarGoogle Scholar |

Sabo, J. L., and Power, M. E. (2002). River-watershed exchange: effects of riverine subsidies on riparian lizards and their terrestrial prey. Ecology 83, 1860–1869.

Sheppard, S. K., and Harwood, J. D. (2005). Advances in molecular ecology: tracking trophic links through predator–prey food-webs. Functional Ecology 19, 751–762.
Advances in molecular ecology: tracking trophic links through predator–prey food-webs.Crossref | GoogleScholarGoogle Scholar |

Sih, A., Englund, G., and Wooster, D. (1998). Emergent impacts of multiple predators on prey. Trends in Ecology & Evolution 13, 350–355.
Emergent impacts of multiple predators on prey.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3M7itF2lsQ%3D%3D&md5=e2f11aa725537742b1de818e88978feeCAS |

Steinmetz, J., Kohler, S. L., and Soluk, D. A. (2003). Birds are overlooked top predators in aquatic food webs. Ecology 84, 1324–1328.
Birds are overlooked top predators in aquatic food webs.Crossref | GoogleScholarGoogle Scholar |

Stenroth, P., Holmqvist, N., Nyström, P., Berglund, O., Larsson, P., and Granéli, W. (2006). Stable isotopes as an indicator of diet in omnivorous crayfish (Pacifastacus leniusculus): the influence of tissue, sample treatment, and season. Canadian Journal of Fisheries and Aquatic Sciences 63, 821–831.
Stable isotopes as an indicator of diet in omnivorous crayfish (Pacifastacus leniusculus): the influence of tissue, sample treatment, and season.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XksFKnu7k%3D&md5=47601fdb4c6323196581d026972b393aCAS |

Stock, B. C., and Semmens, B. X. (2013). MixSIAR GUI User Manual, version 1.0. Available at https://github.com/brianstock/MixSIAR [Verified 6 July 2015].

Syväranta, J., Hämäläinen, H., and Jones, R. I. (2006). Within-lake variability in carbon and nitrogen stable isotope signatures. Freshwater Biology 51, 1090–1102.
Within-lake variability in carbon and nitrogen stable isotope signatures.Crossref | GoogleScholarGoogle Scholar |

Thomson, J. R., Bond, N. R., Cunningham, S. C., Metzling, L., Reich, P., Thompson, R. T., and Mac Nally, R. (2012). The influences of climatic variation and vegetation on stream biota: lessons from the Big Dry in southeastern Australia. Global Change Biology 18, 1582–1596.
The influences of climatic variation and vegetation on stream biota: lessons from the Big Dry in southeastern Australia.Crossref | GoogleScholarGoogle Scholar |

Udy, J. W., and Bunn, S. E. (2001). Elevated δ15N values in aquatic plants from cleared catchments: why? Marine and Freshwater Research 52, 347–351.
Elevated δ15N values in aquatic plants from cleared catchments: why?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlt1Gmu7s%3D&md5=c7d3c63e092c48d934adfc305adea876CAS |

Watson, A., and Barmuta, L. A. (2011). Feeding-preference trials confirm stable isotope analysis results: freshwater macroinvertebrates do consume macrophytes. Marine and Freshwater Research 62, 1248–1257.
Feeding-preference trials confirm stable isotope analysis results: freshwater macroinvertebrates do consume macrophytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlagu7nK&md5=e5ba82d60dd4cdb670cb7b517924bd07CAS |

Zeug, S. C., and Winemiller, K. O. (2008). Evidence supporting the importance of terrestrial carbon in a large-river food web. Ecology 89, 1733–1743.
Evidence supporting the importance of terrestrial carbon in a large-river food web.Crossref | GoogleScholarGoogle Scholar | 18589537PubMed |