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Protonibea Diacanthus Received: 21 October 2016 | Accepted: 30 May 2017 DOI: 10.1111/eva.12499 ORIGINAL ARTICLE Strong population structure deduced from genetics, otolith chemistry and parasite abundances explains vulnerability to localized fishery collapse in a large Sciaenid fish, Protonibea diacanthus Laura Taillebois1,2 | Diane P. Barton1,3 | David A. Crook1 | Thor Saunders3 | Jonathan Taylor3 | Mark Hearnden3 | Richard J. Saunders4,5 | Stephen J. Newman6 | Michael J. Travers6 | David J. Welch7 | Alan Greig8 | Christine Dudgeon9 | Safia Maher9 | Jennifer R. Ovenden9 1Research Institute for the Environment and Livelihoods, Charles Darwin University, Darwin, NT, Australia 2North Australia Marine Research Alliance, Arafura Timor Research Facility, Brinkin, NT, Australia 3Department of Primary Industry and Resources, Northern Territory Government, Berrimah, NT, Australia 4Centre for Sustainable Tropical Fisheries and Aquaculture, James Cook University, Douglas, QLD, Australia 5Animal Science, Queensland Department of Agriculture and Fisheries, Brisbane, QLD, Australia 6Western Australian Fisheries and Marine Research Laboratories, Department of Fisheries, Government of Western Australia, North Beach, WA, Australia 7 C2O Fisheries, Cairns, QLD, Australia 8School of Earth Sciences, The University of Melbourne, Melbourne, VIC, Australia 9Molecular Fisheries Laboratory, School of Biomedical Sciences, The University of Queensland, St. Lucia, QLD, Australia Correspondence Laura Taillebois, Research Institute for the Abstract Environment and Livelihoods, Charles Darwin As pressure on coastal marine resources is increasing globally, the need to quantita- University, Darwin, NT, Australia. Email: [email protected] tively assess vulnerable fish stocks is crucial in order to avoid the ecological conse- quences of stock depletions. Species of Sciaenidae (croakers, drums) are important Funding information Fisheries Research and Development components of tropical and temperate fisheries and are especially vulnerable to ex- Corporation, Grant/Award Number: Project ploitation. The black- spotted croaker, Protonibea diacanthus, is the only large sciaenid 2013/017; North Australia Marine Research Alliance in coastal waters of northern Australia where it is targeted by commercial, recreational and indigenous fishers due to its food value and predictable aggregating behaviour. Localized declines in the abundance of this species have been observed, highlighting the urgent requirement by managers for information on fine-­ and broad- scale popula- tion connectivity. This study examined the population structure of P. diacanthus across north- western Australia using three complementary methods: genetic variation in mi- crosatellite markers, otolith elemental composition and parasite assemblage composi- tion. The genetic analyses demonstrated that there were at least five genetically distinct populations across the study region, with gene flow most likely restricted by inshore biogeographic barriers such as the Dampier Peninsula. The otolith chemistry and parasite analyses also revealed strong spatial variation among locations within This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. © 2017 The Authors. Evolutionary Applications published by John Wiley & Sons Ltd Evolutionary Applications. 2017;1–16. wileyonlinelibrary.com/journal/eva | 1 2 | TAILLEBOIS ET AL. broad- scale regions, suggesting fine- scale location fidelity within the lifetimes of indi- vidual fish. The complementarity of the three techniques elucidated patterns of con- nectivity over a range of spatial and temporal scales. We conclude that fisheries stock assessments and management are required at fine scales (100 s of km) to account for the restricted exchange among populations (stocks) and to prevent localized extirpa- tions of this species. Realistic management arrangements may involve the successive closure and opening of fishing areas to reduce fishing pressure. KEYWORDS croaker, fisheries management, otolith chemistry, parasites, population genetics, stock discrimination 1 | INTRODUCTION Fishes of the family Sciaenidae, commonly known as croakers, are important components of commercial, recreational and indige- Nearshore coastal ecosystems provide an important source of food nous fisheries in tropical and temperate regions worldwide (Lenanton for human populations, supporting 90% of the global wild fish har- & Potter, 1987). They are targeted for their flesh and, increasingly, vest whilst accounting for only 7% of the ocean worldwide (Pauly for their swim bladders, which are sold fresh or dried in South- East et al., 2002). As global demand for seafood increases, many exploited Asia (Ghosh et al., 2009; Sadovy & Cheung, 2003; Tuuli, 2010). Many species in these regions have declined and large numbers of fisher- species of Sciaenidae have declined in recent decades due to over- ies are currently fished at unsustainable levels (Jackson et al., 2001; exploitation, and several are now considered threatened. The black- Smith et al., 2010). Sustainable management of exploited fish popu- spotted croaker Protonibea diacanthus (Lacapede, 1802) is a large lations requires detailed knowledge of population structure, natural species (>1.5 m max. total length; up to 42 kg mass) that is widely abundance and the degree of ecologically relevant exchange among distributed throughout coastal waters and estuaries of the tropical harvested stocks (Pauly et al., 2002). The concept of “stocks” as pop- Indo- West Pacific (Sasaki, 2001). In Australia, it is distributed along ulation units has long been anchored in fisheries science and can be the northern coast from Shark Bay, Western Australia to Hervey defined as groups of fish within a species that are self- recruiting; share Bay, Queensland (Bray, 2011). The species grows rapidly and has a similar growth rates and rates of natural and non- natural mortality; maximum recorded age of 13 years (Phelan, 2008). Spawning of and may react more or less independently to harvesting (Cadrin, Kerr, P. ­diacanthus in Australia occurs from August to December, and they & Mariani, 2013). appear to produce pelagic eggs and have a pelagic larval phase (Froese Methods for delineating stocks have advanced considerably in & Pauly, 2016; Leis & Carson- Ewart, 2000). Whilst inshore seasonal recent years and include genetic techniques, acoustic telemetry, breeding aggregations of P. diacanthus are thought to occur (Welch tagging, otolith chemistry, demographic analysis, otolith shape and et al., 2014), direct evidence of the behaviour of the species is limited meristic data (Hawkins et al., 2016). Genetic approaches speak to (Phelan, 2008) and little is known about the size and locations of the both inter-­ and intragenerational timescales as they track the life- aggregations. Commercial and recreational sectors both contribute to history stages of the fish (i.e., from fertilized eggs to adults) that total landings (667 tonnes in 2005), but catches have increased re- are interchanged between locations and which subsequently par- cently due primarily to growth in the commercial sector (from 43 to ticipate in successful spawning. Otolith multi- elemental signatures 250 tons per annum between 1995 and 2005; Coleman, 2004; Phelan and parasite assemblages are ecological markers recording the en- & Elphick, 2006). Intensive recreational fishing on the east coast of vironment the juvenile and adult fish inhabit and reflect processes Queensland (Bowtell, 1995, 1998) has also been attributed with re- occurring within the individuals’ lifetime. The integration of multiple ducing fish abundance and size to the point where the catches are techniques that operate over different temporal and spatial scales almost exclusively limited to immature fish. There is also evidence of makes it possible to overcome many of the limitations of single over- exploitation of P. diacanthus outside of Australian waters: over- technique approaches and greatly strengthens the inference avail- fishing in India in the 1980s led to local extirpation (James, 1994) and able from stock structure studies (Abaunza et al., 2008; Begg & a fishery that once thrived in Hong Kong no longer exists (Sadovy & Waldman, 1999; Lleonart & Maynou, 2003; Waldman, 1999; Welch Cheung, 2003). et al., 2009, 2015). As an example, Izzo et al. (2017) used an inte- Management practices to support the sustainable harvest of P. di- grated approach to reveal four stocks of the sardine Sardinops sagax acanthus in Western Australia, Queensland and the Northern Territory in Australian waters when it was previously considered a semi- are currently hindered by a lack of knowledge of the species’ popu- continuous meta- population. lation structure. In this study, we examined the population structure TAILLEBOIS ET AL. | 3 of the species across north- western Australia with the expectation of commercial fishers. The total length (TL), standard length (SL) and sex spatially distinct stocks, which would be consistent with the obser- of each specimen were recorded. For genetic analyses, muscle tissue vation of localized depletion. Moreover, we aimed to test the expec- or fin clips were sampled and immediately placed into vials contain- tation that genetics provides information on a broader spatial scale ing molecular grade 95% ethanol or 20% dimethyl sulfoxide (DMSO) than otolith chemistry and parasite data
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