Received: 2 June 2018 Revised: 21 September 2018 Accepted: 24 September 2018 DOI: 10.1002/rra.3369 SPECIAL ISSUE PAPER 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 Julian D. Olden1,2 | Stewart J. Fallon3 | David T. Roberts4 | Tom Espinoza5 | Mark J. Kennard2 1 School of Aquatic and Fishery Sciences, University of Washington, Seattle, Abstract Washington, United States Meeting the conservation challenges of long‐lived animal species necessitate long‐ 2 Australian Rivers Institute, Griffith term assessments of trophic ecology. The use of dietary proxies, such as ratios of University, Brisbane, Queensland, Australia naturally occurring stable isotopes in animal tissues demonstrating progressive 3 Research School of Earth Sciences, The Australian National University, Canberra, growth, has shown considerable promise to reconstruct trophic histories of long‐ Australian Capital Territory, Australia lived organisms experiencing environmental change. Here, we combine innovative 4 Queensland Bulk Water Supply Authority (Seqwater), Brisbane, Australia radiocarbon scale‐ageing techniques with stable isotope analysis of carbon and nitro- 5 Queensland Department of Natural gen from cross sections of scale to reconstruct the trophic ecology of Australian lung- Resources, Mines and Energy, Queensland fish (Neoceratodus forsteri) across its remaining global distribution. Over a 65‐year Government, Brisbane, Queensland, Australia δ13 δ15 Correspondence period, we found pronounced temporal shifts in the C and N isotopic ratios J. D. Olden, School of Aquatic and Fishery of lungfish that coincided with a period of hydrological modification by dams and Sciences, University of Washington, Seattle, ‐ WA, USA 98105. land use intensification associated with agriculture and livestock grazing. In the Email: [email protected] Brisbane and Burnett Rivers, whose hydrology is substantially regulated by large Funding information dams, lungfish showed consistent trends of δ13C depletion and δ15N enrichment over American Philosophical Society; Australian Research Council, Grant/Award Number: time. This may indicate anthropogenic changes in background isotopic levels of basal LP130100118; Mohamed bin Zayed Species energy sources and/or that additional seston exported downstream from impound- Conservation Fund; National Geographic Society ments represent a carbon source that was previously unavailable, thus shifting lungfish diet from benthic‐dominated primary production typical of unmodified river systems, to pelagic carbon sources. By contrast, δ13C ratios of lungfish in the unreg- ulated Mary River were more stable through time, whereas δ15N ratios increased during a period of dairy industry expansion and increased application of nitrogen fertilization and then subsequently decreased at the same time that rates of pasture development declined and nutrient inputs presumably decreased. In conclusion, we provide evidence for human‐caused alterations in background isotopic levels and potential changes in availability of benthic versus pelagic energy resources supporting Australian lungfish and demonstrate how detectable trophic signals in long‐lived fish scales can reveal long‐term anthropogenic changes in riverine ecosystems. KEYWORDS impoundment, long‐term studies, nutrients, river regulation, scale, stable isotope analysis River Res Applic. 2018;1–11. wileyonlinelibrary.com/journal/rra © 2018 John Wiley & Sons, Ltd. 1 2 OLDEN ET AL. 1 | INTRODUCTION microchemistry (Campana, 2005), investigations using fish scales have proved useful to document both age and life history patterns (Tzadik Large, long‐lived freshwater fishes face tremendous conservation chal- et al., 2017). Scales share several properties with otoliths such as lenges to ensure their future persistence (Hogan, Moyle, May, Vander incremental growth and the incorporation of chemical constituents Zanden, & Baird, 2004; Jensen et al., 2009; Olden, Hogan, & Vander from the surrounding environment within each increment. In addition, Zanden, 2007). Characterized by slow growth, late maturity, and thus scale growth in most fish species is coupled to somatic growth, low rates of population growth, long‐lived species are intrinsically more resulting in growth cycles being recorded as concentric circuli of calci- vulnerable to environmental change and, ultimately, extinction (Pimm, fied collagen corresponding to age (Hutchinson & Trueman, 2006; Jones, & Diamond, 1988). For example, the Australian lungfish, Trueman & Moore, 2007). Studies have shown that stable isotope Neoceratodus forsteri (Krefft, 1870), listed as “vulnerable” under federal values of slower turnover tissues such as fish scale collagen, correlate legislation, is one of only six surviving lungfish species in the world and well with other calcified and noncalcified tissues (Jardine et al., 2012; may be the oldest living vertebrate on the planet (Tokita, Okamoto, & Fincel, Vandehey, & Chipps, 2012), and have the distinct advantage of Hikida, 2005). Despite ongoing threats and repeated calls to fill critical being a nonlethal alternative to otolith removal. knowledge gaps, very little is known about the implications of long‐term Stable isotope analysis of carbon and nitrogen in fish scales can environmental change for the Australian lungfish (hereafter “lungfish”; provide a chronological repository of long‐term ecosystem changes. Arthington, 2009; Curtis, Dennis, McDonald, Kyne, & Debus, 2012). Previous studies have used isotopic changes to provide evidence for Riparian degradation and nutrient addition associated with agricul- catchment nitrogen loading (Roussel et al., 2014), ecosystem eutrophi- tural land use, and hydrologic alteration from impoundments, modify the cation and reoligotrophication (Grey, Graham, Britton, & Harrod, availability and quality of basal food resources in river ecosystems (e.g., 2009), climate cycles (Satterfield & Finney, 2002), hydrologic change Anderson & Cabana, 2006; Boëchat, Krüger, Giani, Figueredo, & Gücker, (Delong et al., 2011), changing prey availability (Pruell, Taplin, & 2011; Delong, Thorp, Thoms, & McIntosh, 2011; Kennedy et al., 2016). Cicchelli, 2003), interactions with invasive species (Mercado‐Silva, Agricultural land use subject to livestock grazing and cropping practices Helmus, & Vander Zanden, 2009), and fisheries overexploitation increase run‐off of sediments and nutrients leading to anthropogenic (Wainright, Fogarty, Greenfield, & Fry, 1993). Stable isotope analysis nutrient enrichment and altered delivery of allochthonous carbon (e.g., for trophic reconstruction is most often measured by homogenizing Buck, Niyogi, & Townsend, 2004; Hagen, McTammany, Webster, & entire scales or subsampling the scale's growing edge to provide either Benfield, 2010). By intercepting flooding events, dams often reduce a combined lifetime measure, or just the most recent diet proxy, lateral inundation of riparian and floodplain areas downstream, thus respectively (Tzadik et al., 2017). By contrast, cross‐sectional sampling limiting allochthonous inputs to riverine environments (Tockner & across a scale's longitudinal axis has rarely been examined (e.g., Seeley, Stanford, 2002). Similarly, the increased hydrologic stability below dams Miller, & Walther, 2015) but offers new opportunities to sample dis- can lead to excessive growth of autochthonous sources including mac- crete time periods over the life of a fish. The reason being is that rophytes, periphyton, and phytoplankton (Pingram, Collier, Hamilton, well‐calcified layers accrete radially towards the leading edge as new David, & Hicks, 2012). Large impoundments are also a significant layers overlay older layers (Hutchinson & Trueman, 2006). Provided source of planktonic production, which ultimately provides food subsi- scales are thick enough to allow targeted cross‐sectional sampling, dies to downstream aquatic consumers (Doi et al., 2008; Growns, assays of the elemental composition across growth increments can Chessman, Mitrovic, & Westhorpe, 2014). provide a lifetime profile of trophic ecology and previous water chem- Human‐induced environmental change has been shown to modify istry encountered by individual fish (Seeley et al., 2015; Tzadik et al., isotope ratios of actively cycled elements such as carbon and nitrogen 2017). This is the case for lungfish where the large elasmoid scales (Bowen, 2010) and alter the availability of benthic versus pelagic and (in excess of 50 mm from primordia to leading edge) are retained for allochthonous versus autochthonous basal energy resources life, laying down successive new layers of thick collagen material as supporting riverine food webs (Growns et al., 2014; Robertson, Bunn, they increase in body size (Kemp, 2012). Furthermore, by combining Boon, & Walker, 1999; Shannon et al., 2001; Sheldon & Thoms, 2006). isotopic profiles with bomb‐curve radiocarbon ageing (Uno et al., Such shifts in isotope signatures and dominant basal energy sources 2013), the chronological record of lungfish trophic ecology can be can translate to changes in the quantity and quality of resources avail- reconstructed over extended time periods (James, Fallon, McDougall, able to higher trophic level consumers (Delong et al., 2011; Delong & Espinoza, & Broadfoot, 2010; Fallon et al., 2015, n.d.). Thoms, 2016). However, anticipating species responses to long‐term In this study, we combine innovative radiocarbon scale‐ageing