Gut content and stable isotope analysis of tadpoles in floodplain wetlands
J. F. Ocock
A B C D , K. J. Brandis C , B. J. Wolfenden A , K. M. Jenkins A C and S. Wassens A
+ Author Affiliations
- Author Affiliations
A Institute of Land, Water and Society, Charles Sturt University, Albury, NSW 2640, Australia.
B Water, Wetlands and Coast Science Branch, NSW Office of Environment and Heritage, 59–61 Goulburn Street, Sydney, NSW 2000, Australia.
C Centre for Ecosystem Science, School of Biological, Earth and Environmental Sciences, University of New South Wales, Randwick, NSW 2052, Australia.
D Corresponding author. Email: joanne.ocock@environment.nsw.gov.au
Australian Journal of Zoology 66(4) 261-271 https://doi.org/10.1071/ZO18043
Submitted: 20 June 2018 Accepted: 8 March 2019 Published: 23 April 2019
Abstract
Larval amphibians (tadpoles) are an important link in aquatic food webs, as they can be highly abundant consumers and prey for a wide variety of predators. Most tadpoles are considered omnivores, predominately grazing on algae, detritus and macrophytes, though recent work has identified greater plasticity and breadth in diet than previously considered. We used gut content and stable isotope analysis (SIA) in a baseline study to determine the important dietary items (ingested material) and food sources (assimilated material) for tadpoles of two abundant generalist frog species in regulated floodplain wetlands of the Murrumbidgee River, south-east Australia. We identified a wide variety of dietary items in the gut contents, including whole microcrustaceans, filamentous algae and macrophytes. The composition of several ingested food items was correlated with their availability in each wetland. However, SIA identified biofilm as the food source most consistently assimilated across several wetlands, though microcrustaceans and algae contributed when abundant. Biofilm is likely the most important basal food item for tadpoles in floodplain wetlands because it is ubiquitous and has a high nutritional quality. Identifying important food sources is a crucial step towards developing management strategies for promoting tadpole recruitment in regulated wetlands.
Additional keywords: amphibian, Australia, diet, Limnodynastes, river regulation.
References
Alford, R. A., and Richards, S. J. (1999). Global amphibian declines: a problem in applied ecology. Annual Review of Ecology and Systematics 30, 133–165.| Global amphibian declines: a problem in applied ecology.Crossref | GoogleScholarGoogle Scholar |
Altig, R., Whiles, M. R., and Taylor, C. L. (2007). What do tadpoles really eat? Assessing the trophic status of an understudied and imperiled group of consumers in freshwater habitats. Freshwater Biology 52, 386–395.
| What do tadpoles really eat? Assessing the trophic status of an understudied and imperiled group of consumers in freshwater habitats.Crossref | GoogleScholarGoogle Scholar |
Anstis, M. (2013). ‘Tadpoles and Frogs of Australia.’ (New Holland: London.)
Barnum, T. R., Drake, J. M., Colón-Gaud, C., Rugenski, A. T., Frauendorf, T. C., Connelly, S., Kilham, S. S., Whiles, M. R., Lips, K. R., and Pringle, C. M. (2015). Evidence for the persistence of food web structure after amphibian extirpation in a Neotropical stream. Ecology 96, 2106–2116.
| Evidence for the persistence of food web structure after amphibian extirpation in a Neotropical stream.Crossref | GoogleScholarGoogle Scholar | 26405736PubMed |
Bates, D., Maechler, M., Bolker, B., and Walker, S. (2014). Package lme4: linear mixed-effects models using Eigen and S4. R package version 1.1–7. 1. 1–9.
Bergamino, L., Lercari, D., and Defeo, O. (2011). Food web structure of sandy beaches: temporal and spatial variation using stable isotope analysis. Estuarine, Coastal and Shelf Science 91, 536–543.
| Food web structure of sandy beaches: temporal and spatial variation using stable isotope analysis.Crossref | GoogleScholarGoogle Scholar |
Bino, G., Kingsford, R. T., and Porter, J. (2015). Prioritizing wetlands for waterbirds in a boom and bust system: waterbird refugia and breeding in the Murray–Darling Basin. PLoS One 10, e0132682.
| Prioritizing wetlands for waterbirds in a boom and bust system: waterbird refugia and breeding in the Murray–Darling Basin.Crossref | GoogleScholarGoogle Scholar | 26161652PubMed |
Bino, G., Wassens, S., Kingsford, R. T., Thomas, R. F., and Spencer, J. (2018). Floodplain ecosystem dynamics under extreme dry and wet phases in semi‐arid Australia. Freshwater Biology 63, 224–241.
| Floodplain ecosystem dynamics under extreme dry and wet phases in semi‐arid Australia.Crossref | GoogleScholarGoogle Scholar |
Blaustein, A. R., Han, B. A., Relyea, R. A., Johnson, P. T. J., Buck, J. C., Gervasi, S. S., and Kats, L. B. (2011). The complexity of amphibian population declines: understanding the role of cofactors in driving amphibian losses. Annals of the New York Academy of Sciences 1223, 108–119.
| The complexity of amphibian population declines: understanding the role of cofactors in driving amphibian losses.Crossref | GoogleScholarGoogle Scholar | 21449968PubMed |
Bunn, S. E., and Arthington, A. H. (2002). Basic principles and ecological consequences of altered flow regimes for aquatic biodiversity. Environmental Management 30, 492–507.
| Basic principles and ecological consequences of altered flow regimes for aquatic biodiversity.Crossref | GoogleScholarGoogle Scholar | 12481916PubMed |
Bunn, S. E., Davies, P. M., and Winning, M. (2003). Sources of organic carbon supporting the food web of an arid zone floodplain river. Freshwater Biology 48, 619–635.
| Sources of organic carbon supporting the food web of an arid zone floodplain river.Crossref | GoogleScholarGoogle Scholar |
Burns, A., and Ryder, D. S. (2001). Potential for biofilms as biological indicators in Australian riverine systems. Ecological Management & Restoration 2, 53–64.
| Potential for biofilms as biological indicators in Australian riverine systems.Crossref | GoogleScholarGoogle Scholar |
Caut, S., Angulo, E., Díaz-Paniagua, C., and Gomez-Mestre, I. (2013). Plastic changes in tadpole trophic ecology revealed by stable isotope analysis. Oecologia 173, 95–105.
| Plastic changes in tadpole trophic ecology revealed by stable isotope analysis.Crossref | GoogleScholarGoogle Scholar | 22915331PubMed |
Connelly, S., Pringle, C. M., Whiles, M. R., Lips, K. R., Kilham, S., and Brenes, R. (2011). Do tadpoles affect leaf decomposition in neotropical streams? Freshwater Biology 56, 1863–1875.
| Do tadpoles affect leaf decomposition in neotropical streams?Crossref | GoogleScholarGoogle Scholar |
Cross, W. F., Benstead, J. P., Frost, P. C., and Thomas, S. A. (2005). Ecological stoichiometry in freshwater benthic systems: recent progress and perspectives. Freshwater Biology 50, 1895–1912.
| Ecological stoichiometry in freshwater benthic systems: recent progress and perspectives.Crossref | GoogleScholarGoogle Scholar |
Dauta, A., Devaux, J., Piquemal, F., and Boumnich, L. (1990). Growth rate of four freshwater algae in relation to light and temperature. Hydrobiologia 207, 221–226.
| Growth rate of four freshwater algae in relation to light and temperature.Crossref | GoogleScholarGoogle Scholar |
Dodds, W. K., Collins, S., Hamilton, S., Tank, J., Johnson, S., Webster, J., Simon, K., Whiles, M., Rantala, H., and McDowell, W. (2014). You are not always what we think you eat: selective assimilation across multiple whole‐stream isotopic tracer studies. Ecology 95, 2757–2767.
| You are not always what we think you eat: selective assimilation across multiple whole‐stream isotopic tracer studies.Crossref | GoogleScholarGoogle Scholar |
Douglas, M. M., Bunn, S. E., and Davies, P. M. (2005). River and wetland food webs in Australia’s wet–dry tropics: general principles and implications for management. Marine and Freshwater Research 56, 329–342.
| River and wetland food webs in Australia’s wet–dry tropics: general principles and implications for management.Crossref | GoogleScholarGoogle Scholar |
Ficetola, G. F., Rondinini, C., Bonardi, A., Baisero, D., and Padoa‐Schioppa, E. (2015). Habitat availability for amphibians and extinction threat: a global analysis. Diversity & Distributions 21, 302–311.
| Habitat availability for amphibians and extinction threat: a global analysis.Crossref | GoogleScholarGoogle Scholar |
Frazier, P., and Page, K. (2006). The effect of river regulation on floodplain wetland inundation, Murrumbidgee River, Australia. Marine and Freshwater Research 57, 133–141.
| The effect of river regulation on floodplain wetland inundation, Murrumbidgee River, Australia.Crossref | GoogleScholarGoogle Scholar |
Freeman, C., and Lock, M. A. (1995). The biofilm polysaccharide matrix: a buffer against changing organic substrate supply? Limnology and Oceanography 40, 273–278.
| The biofilm polysaccharide matrix: a buffer against changing organic substrate supply?Crossref | GoogleScholarGoogle Scholar |
Fry, B. (2006). ‘Stable Isotope Ecology.’ (Springer: New York.)
Hamilton, P. T., Richardson, J. M. L., and Anholt, B. R. (2012). Daphnia in tadpole mesocosms: trophic links and interactions with Batrachochytrium dendrobatidis. Freshwater Biology 57, 676–683.
| Daphnia in tadpole mesocosms: trophic links and interactions with Batrachochytrium dendrobatidis.Crossref | GoogleScholarGoogle Scholar |
Hof, C., Araujo, M. B., Jetz, W., and Rahbek, C. (2011). Additive threats from pathogens, climate and land-use change for global amphibian diversity. Nature 480, 516–519.
| Additive threats from pathogens, climate and land-use change for global amphibian diversity.Crossref | GoogleScholarGoogle Scholar | 22089134PubMed |
IUCN (2017). The IUCN Red List of Threatened Species. Version 2017-3. Available at: http://www.iucnredlist.org [accessed 5 December 2017].
Iwai, N., and Kagaya, T. (2007). Positive indirect effect of tadpoles on a detritivore through nutrient regeneration. Oecologia 152, 685–694.
| Positive indirect effect of tadpoles on a detritivore through nutrient regeneration.Crossref | GoogleScholarGoogle Scholar | 17351795PubMed |
Jenkins, K. M., and Boulton, A. J. (2003). Connectivity in a dryland river: short-term aquatic microinvertebrate recruitment following floodplain inundation. Ecology 84, 2708–2723.
| Connectivity in a dryland river: short-term aquatic microinvertebrate recruitment following floodplain inundation.Crossref | GoogleScholarGoogle Scholar |
Jenssen, T. A. (1967). Food habits of the green frog, Rana clamitans, before and during metamorphosis. Copeia 1967, 214–218.
| Food habits of the green frog, Rana clamitans, before and during metamorphosis.Crossref | GoogleScholarGoogle Scholar |
Kelleway, J., Mazumder, D., Wilson, G. G., Saintilan, N., Knowles, L., Iles, J., and Kobayashi, T. (2010). Trophic structure of benthic resources and consumers varies across a regulated floodplain wetland. Marine and Freshwater Research 61, 430–440.
| Trophic structure of benthic resources and consumers varies across a regulated floodplain wetland.Crossref | GoogleScholarGoogle Scholar |
Kingsford, R. T. (2000). Ecological impacts of dams, water diversions and river management on floodplain wetlands in Australia. Austral Ecology 25, 109–127.
| Ecological impacts of dams, water diversions and river management on floodplain wetlands in Australia.Crossref | GoogleScholarGoogle Scholar |
Kingsford, R. T., and Thomas, R. F. (2004). Destruction of wetlands and waterbird populations by dams and irrigation on the Murrumbidgee River in arid Australia. Environmental Management 34, 383–396.
| Destruction of wetlands and waterbird populations by dams and irrigation on the Murrumbidgee River in arid Australia.Crossref | GoogleScholarGoogle Scholar | 15520895PubMed |
Maerz, J. C., Cohen, J. S., and Blossey, B. (2010). Does detritus quality predict the effect of native and non‐native plants on the performance of larval amphibians? Freshwater Biology 55, 1694–1704.
McDiarmid, R. W., and Altig, R. (1999). ‘Tadpoles: the Biology of Anuran Larvae.’ (University of Chicago Press: Chicago.)
New South Wales Government (2008). RiverBank Water Use Plan for the Murrumbidgee water management area. Available at: http://www.environment.nsw.gov.au/research-and-publications/publications-search/riverbank-water-use-plan-for-the-murrumbidgee-water-management-area [accessed 3 March 2018].
Ocock, J. F., and Wassens, S. (2018). Status of decline and conservation of frogs in arid and semi-arid Australia. In ‘Status of Conservation and Decline of Amphibians in Australia, New Zealand and the Pacific Islands’. (Eds H. Heatwole and J. J. L. Rowley.) pp. 408–425. (CSIRO: Canberra.)
Ocock, J. F., Kingsford, R. T., Penman, T. D., and Rowley, J. J. (2016). Amphibian abundance and detection trends during a large flood in a semi-arid floodplain wetland. Herpetological Conservation and Biology 11, 408–425.
Oksanen, J., Blanchet, F. G., Kindt, R., Legendre, P., O’Hara, R. B., Simpson, G. L., Solymos, P., Stevens, M. H. H., and Wagner, H. (2011). Vegan: community ecology package. Available at: http://CRAN.R-project.org/package=vegan [accessed 4 November 2017].
Parnell, A. (2016). simmr: a stable isotope mixing model. R package version 0.3. Available at: https://CRAN.R-project.org/package=simmr [accessed 24 August 2017].
Parnell, A. C., Inger, R., Bearhop, S., and Jackson, A. L. (2010). Source partitioning using stable isotopes: coping with too much variation. PLoS One 5, e9672.
| Source partitioning using stable isotopes: coping with too much variation.Crossref | GoogleScholarGoogle Scholar | 20300637PubMed |
Peterson, C. G., and Boulton, A. J. (1999). Stream permanence influences microalgal food availability to grazing tadpoles in arid-zone springs. Oecologia 118, 340–352.
| Stream permanence influences microalgal food availability to grazing tadpoles in arid-zone springs.Crossref | GoogleScholarGoogle Scholar | 28307278PubMed |
Petranka, J. W., and Kennedy, C. A. (1999). Pond tadpoles with generalized morphology: is it time to reconsider their functional roles in aquatic communities? Oecologia 120, 621–631.
| Pond tadpoles with generalized morphology: is it time to reconsider their functional roles in aquatic communities?Crossref | GoogleScholarGoogle Scholar | 28308314PubMed |
R Core Team (2015). R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available at: https://www.R-project.org/ [accessed 7 May 2017].
Rantala, H. M., Nelson, A. M., Fulgoni, J. N., Whiles, M. R., Hall, R. O., Dodds, W. K., Verburg, P., Huryn, A. D., Pringle, C. M., and Kilham, S. S. (2015). Long‐term changes in structure and function of a tropical headwater stream following a disease‐driven amphibian decline. Freshwater Biology 60, 575–589.
| Long‐term changes in structure and function of a tropical headwater stream following a disease‐driven amphibian decline.Crossref | GoogleScholarGoogle Scholar |
Ranvestel, A. W., Lips, K. R., Pringle, C. M., Whiles, M. R., and Bixby, R. J. (2004). Neotropical tadpoles influence stream benthos: evidence for the ecological consequences of decline in amphibian populations. Freshwater Biology 49, 274–285.
| Neotropical tadpoles influence stream benthos: evidence for the ecological consequences of decline in amphibian populations.Crossref | GoogleScholarGoogle Scholar |
Reid, M., Delong, M., and Thoms, M. (2012). The influence of hydrological connectivity on food web structure in floodplain lakes. River Research and Applications 28, 827–844.
| The influence of hydrological connectivity on food web structure in floodplain lakes.Crossref | GoogleScholarGoogle Scholar |
Santos, F. J., Protázio, A. S., Moura, C. W., and Juncá, F. A. (2016). Diet and food resource partition among benthic tadpoles of three anuran species in Atlantic Forest tropical streams. Journal of Freshwater Ecology 31, 53–60.
| Diet and food resource partition among benthic tadpoles of three anuran species in Atlantic Forest tropical streams.Crossref | GoogleScholarGoogle Scholar |
Schalk, C. M., Montaña, C. G., Winemiller, K. O., and Fitzgerald, L. A. (2017). Trophic plasticity, environmental gradients and food‐web structure of tropical pond communities. Freshwater Biology 62, 519–529.
| Trophic plasticity, environmental gradients and food‐web structure of tropical pond communities.Crossref | GoogleScholarGoogle Scholar |
Schiesari, L. (2006). Pond canopy cover: a resource gradient for anuran larvae. Freshwater Biology 51, 412–423.
| Pond canopy cover: a resource gradient for anuran larvae.Crossref | GoogleScholarGoogle Scholar |
Schiesari, L., Werner, E. E., and Kling, G. W. (2009). Carnivory and resource-based niche differentiation in anuran larvae: implications for food web and experimental ecology. Freshwater Biology 54, 572–586.
| Carnivory and resource-based niche differentiation in anuran larvae: implications for food web and experimental ecology.Crossref | GoogleScholarGoogle Scholar |
Schmidt, K., Blanchette, M. L., Pearson, R. G., Alford, R. A., and Davis, A. M. (2017). Trophic roles of tadpoles in tropical Australian streams. Freshwater Biology 62, 1929–1941.
Schriever, T. A., and Williams, D. D. (2013). Ontogenetic and individual diet variation in amphibian larvae across an environmental gradient. Freshwater Biology 58, 223–236.
| Ontogenetic and individual diet variation in amphibian larvae across an environmental gradient.Crossref | GoogleScholarGoogle Scholar |
Smith, J. A., Mazumder, D., Suthers, I. M., and Taylor, M. D. (2013). To fit or not to fit: evaluating stable isotope mixing models using simulated mixing polygons. Methods in Ecology and Evolution 4, 612–618.
| To fit or not to fit: evaluating stable isotope mixing models using simulated mixing polygons.Crossref | GoogleScholarGoogle Scholar |
Souter, N., Walter, M., and Wen, L. (2012). Weir pool surcharge and a corresponding increase in algal biofilm community diversity in the lower River Murray, South Australia. River Research and Applications 28, 1853–1857.
| Weir pool surcharge and a corresponding increase in algal biofilm community diversity in the lower River Murray, South Australia.Crossref | GoogleScholarGoogle Scholar |
Tockner, K., and Stanford, J. A. (2002). Riverine flood plains: present state and future trends. Environmental Conservation 29, 308–330.
| Riverine flood plains: present state and future trends.Crossref | GoogleScholarGoogle Scholar |
Tockner, K., Klaus, I., Baumgartner, C., and Ward, J. V. (2006). Amphibian diversity and nestedness in a dynamic floodplain river (Tagliamento, NE-Italy). Hydrobiologia 565, 121–133.
| Amphibian diversity and nestedness in a dynamic floodplain river (Tagliamento, NE-Italy).Crossref | GoogleScholarGoogle Scholar |
Trakimas, G., Jardine, T. D., Barisevičiūtɹ, R., Garbaras, A., Skipitytɹ, R., and Remeikis, V. (2011). Ontogenetic dietary shifts in European common frog (Rana temporaria) revealed by stable isotopes. Hydrobiologia 675, 87.
| Ontogenetic dietary shifts in European common frog (Rana temporaria) revealed by stable isotopes.Crossref | GoogleScholarGoogle Scholar |
Venesky, M. D., Wilcoxen, T. E., Rensel, M. A., Rollins-Smith, L., Kerby, J. L., and Parris, M. J. (2012). Dietary protein restriction impairs growth, immunity, and disease resistance in southern leopard frog tadpoles. Oecologia 169, 23–31.
| Dietary protein restriction impairs growth, immunity, and disease resistance in southern leopard frog tadpoles.Crossref | GoogleScholarGoogle Scholar | 22038058PubMed |
Wada, E., Mizutani, H., and Minagawa, M. (1991). The use of stable isotopes for food web analysis. Critical Reviews in Food Science and Nutrition 30, 361–371.
| The use of stable isotopes for food web analysis.Crossref | GoogleScholarGoogle Scholar | 1910519PubMed |
Walker, K. F., Sheldon, F., and Puckridge, J. T. (1995). A perspective on dryland river ecosystems. Regulated Rivers: Research and Management 11, 85–104.
| A perspective on dryland river ecosystems.Crossref | GoogleScholarGoogle Scholar |
Wassens, S., Hall, A., Osborne, W., and Watts, J. (2010). Habitat characteristics predict occupancy patterns of the endangered amphibian Litoria raniformis in flow-regulated flood plain wetlands. Austral Ecology 35, 944–955.
| Habitat characteristics predict occupancy patterns of the endangered amphibian Litoria raniformis in flow-regulated flood plain wetlands.Crossref | GoogleScholarGoogle Scholar |
Wassens, S., Jenkins, K. M., Spencer, J., Thiem, J. D., Kobayashi, T., Bino, G., Lenon, E., Thomas, R., Baumgartner, L., Brandis, K., and Wolfenden, B. (2014). Murrumbidgee monitoring and evaluation plan. Report to the Commonwealth Environmental Water Holders Office. Available at: https://www.environment.gov.au/water/cewo/publications/murrumbidgee-me-plan [accessed 24 August 2018].
Wassens, S., Spencer, J., Thiem, J. D., Wolfenden, B., Jenkins, K. M., Hall, A., Ocock, J. F., Kobayashi, T., Thomas, R., Bino, G., Heath, J., and Lenon, E. (2016). Commonwealth Environmental Water Office long-term intervention monitoring program Murrumbidgee River system Selected Area evaluation report, 2014–16. Report prepared for the Commonwealth Environmental Water Office, Commonwealth of Australia. Available at: http://www.environment.gov.au/system/files/resources/9a75d0c3-4121-4687-932d-bb0c8bc9a0a7/files/murrumbidgee-ltim-report-2015-16.pdf [accessed 24 August 2018].
Whiles, M. R., Gladyshev, M. I., Sushchik, N. N., Makhutova, O. N., Kalachova, G. S., Peterson, S. D., and Regester, K. J. (2010). Fatty acid analyses reveal high degrees of omnivory and dietary plasticity in pond‐dwelling tadpoles. Freshwater Biology 55, 1533–1547.
| Fatty acid analyses reveal high degrees of omnivory and dietary plasticity in pond‐dwelling tadpoles.Crossref | GoogleScholarGoogle Scholar |
Whiles, M. R., Hall, R. O., Dodds, W. K., Verburg, P., Huryn, A. D., Pringle, C. M., Lips, K. R., Kilham, S. S., Colon-Gaud, C., Rugenski, A. T., Peterson, S., and Connelly, S. (2013). Disease-driven amphibian declines alter ecosystem processes in a tropical stream. Ecosystems 16, 146–157.
| Disease-driven amphibian declines alter ecosystem processes in a tropical stream.Crossref | GoogleScholarGoogle Scholar |
