Gillanders Aquatic Ecology Lab
2019 publications (links to each paper available at Read More)
Source: Chris Davey / Flickr. License: CC by Attribution-NonCommercial
Dispersal of an exploited demersal fish species (Argyrosomus japonicus, Sciaenidae) inferred from satellite telemetry
Barnes, TC, PJ Rogers, Y Wolf, A Madonna, D Holman, GJ Ferguson, W Hutchinson, A Loisier, D Sortino, M Sumner, BM Gillanders. 2019. Marine Biology 166: 125.
Mulloway (Argyrosomus japonicus) are an iconic recreational, indigenous, and commercial fishery species with declining numbers across some parts of their range, with relatively little known about their movements. During the Austral summers and autumns from 2011 to 2014, we deployed 19 pop-up satellite archival tags (PSATs) on mature mulloway at an aggregation site within the Great Australian Bight Marine Park (GABMP), to examine their movement patterns. Twelve tags provided data from deployments ranging from 8 to 110 days including five tags that gathered data over autumn and seven over summer. Five of the seven mulloway tagged during summer likely remained in the vicinity of the tagging location and hence within or in close proximity to marine-protected areas (MPAs) over summer; however, relatively large horizontal movements were observed over autumn for most fish, including a maximum net displacement of ~ 550 km. The median pop-up distance from deployment was 51 and 212 km for summer-and autumn-tagged fish, respectively. Depths encountered by the tagged mulloway ranged from the surface to 56.5 m deep. Our study provides new information on the dispersal of a poorly understood fish species which could aid their conservation.
Image: Periodic table
Juvenile fish habitat across the inner Danish waters: Using otolith chemistry to discriminate between hybridising con-familials and contiguous, coastal habitat
Brown, EJ, P Reis-Santos, BM Gillanders, JG Stottrup. 2019. Estuarine Coastal and Shelf Science 220: 111-119.
Connectivity between juvenile habitats and adult stocks is important for determining the resilience of local fisheries and the relative contribution of different juvenile habitat areas to adult populations. Otolith chemistry is commonly employed to differentiate between individuals from different juvenile habitat areas; whereby different environmental exposures, mediated by intrinsic physiological processes, produce different trace element concentrations in the biologically inert otolith. This study aims to determine if otolith chemistry can differentiate between juveniles of hybridising con-familials where they are found in the same habitat and to establish if otolith chemistry can effectively re-assign individuals to contiguous coastal juvenile habitat areas of the inner Danish waters (IDW). Sympatric pairs of juvenile European plaice (Pleuronectes platessa) and flounder (Platichthys flesus) caught together in a juvenile beam trawl survey, in areas where the two species hybridise, were used to address the first aim. Juvenile plaice and common sole (Solea solea) caught during the same survey
were used to determine if otolith chemistry can correctly re-assign individuals back to contiguous coastal juvenile habitat areas. Laser ablation inductively coupled plasma mass spectroscopy (LA-ICPMS) was used to analyse the trace elements in edge spots of juvenile otoliths and Canonical Analysis of Principal Coordinates was employed to test the reassignment of individuals back to correct species or area. Using a suite of eight trace elements, ∼72% of individual plaice (∼70%) and flounder (∼73%) were correctly identified. Greater than twothirds (∼67%) of plaice were correctly re-allocated to four juvenile habitat areas and close to four out of five (∼79%) individual sole were correctly re-allocated to three juvenile habitat areas. These results indicate that the hybridising con-familial plaice and flounder of the IDW warrant further attention and could be a valuable model
system to assess how intrinsic and extrinsic factors influence elemental incorporation. Furthermore, this study shows otolith chemistry is a valuable tool for tracing marine fish back to juvenile habitat areas, even where they are found along contiguous coastal areas.
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Image: Part of cover of Marine and Freshwater Research special issue
Women in marine science in Australia - Editorial
Gillanders, BM, MR Heupel. 2019. Marine and Freshwater
Research 70: I-III
This special issue of Marine and Freshwater Research brings together 12 contributions led by women and involving other women (or men) as co-authors (Buddle et al. 2019; Coleman et al. 2019; Day et al. 2019; Deaker et al. 2019; Green et al. 2019; Heupel et al. 2019; Joyce et al. 2019; Lara-Lopez et al. 2019; Morgan et al. 2019; Schaefer et al. 2019; Wood et al. 2019; Woodings et al. 2019). These contributions span a diversity of fields within marine science and represent 40 women across all career stages from 20 institutions. Although this issue doesn’t represent the full complement of women in marine science in Australia, it aimed to include a broad spectrum of women in this community. In this special issue, we aimed to provide a series of contributions highlighting women as lead authors and representing the breadth of the research they lead.
The twelve contributions are all available as part of the special issue.
Image: Resting respirometers chambers; Kayla Gilmore
Prolonged exposure to low oxygen improves hypoxia tolerance in a freshwater fish
Gilmore, KL, ZA Doubleday, BM Gillanders. 2019.
Conservation Physiology 7, coz058
Persistent hypoxic or low-oxygen conditions in aquatic systems are becoming more frequent worldwide, causing large-scale mortalities to aquatic fauna. It is poorly understood, however, whether species can acclimate to long-term hypoxic conditions. In two experiments, we exposed juvenile freshwater fish (Murray cod, Maccullochella peelii) to low-oxygen conditions and investigated acclimation effects. Experiment 1 determined how responses could be modified by exposure to different temperatures (20, 24 and 28◦C) and oxygen conditions (control 6–8 mgO2 L−1 and low-oxygen 3–4 mgO2 L−1) over 30 days. Experiment 2 determined the acclimation ability of fish exposed to two temperatures (20 and 28◦C) and low-oxygen conditions (3–4 mgO2 L−1) for three different acclimation periods (7, 14 and 30 days). Responses were measured by determining critical
oxygen tension (Pcrit), loss of equilibrium and aerobic capacity using resting respirometry. In experiment 1, resting oxygen requirements were negatively affected by long-term low-oxygen exposure except at the highest temperature (28◦C).However, long-term acclimation in low-oxygen improved tolerance as measured by loss of equilibrium but not Pcrit. In experiment 2, fish could tolerate lower oxygen levels before reaching loss of equilibrium after 7 days acclimation, but this declined overtime. Murray codwere most tolerant to low-oxygen at the lowest temperature (20◦C) and shortest exposure time (7 days). Extended low-oxygen exposure resulted in reduced aerobic capacity of fish particularly at the lowest temperature.While prior exposure to low-oxygen may allow fish to cope with hypoxic conditions better in the long-term, acclimation time was inversely related to tolerance, suggesting that resistance to hypoxia might decrease as a function of exposure time. Our study fills a much-needed gap in our understanding of how freshwater species acclimate to hypoxia, and in particular, how exposure to prolonged periods of low-oxygen and elevated temperatures affect organisms physiologically.
Image: Andrew Fox; Rodney Fox Shark Expeditions, andrew@rodneyfox.com.au
Comparative population genomics confirms litte population structure in two commercially targeted carcharhinid sharks
Junge, C, SC Donnellan, C Huveneers, CJA Bradshaw, A Simon, M Drew, C Duffy, G Johnson, G Cliff, M Braccini, SC Cutmore, P Butcher, R McAuley, V Peddemors, P Rogers, BM Gillanders. 2019. Marine Biology 166, 16
Many shark species are at risk of overexploitation due to their high economic value, slow maturation, and low recruitment compared to most teleosts. However, there is insufficient knowledge about population structure at different spatial scales necessary to optimise fisheries models. We used single-nucleotide polymorphisms (SNPs) obtained through complexity reduction genome sequencing to quantify the population structure of two highly mobile and commercially fished shark species: bronze whalers (Carcharhinus brachyurus) and dusky sharks (C. obscurus). We applied a comprehensive approach to test several population-structure hypotheses and signal consistency across methods and marker type. We found that C. obscurus was panmictic across Australia and Indonesia and across the Indian Ocean to South Africa based on neutral loci, whereas for C. brachyurus, the westernmost Australian samples appeared to be separate from the rest. The southernmost east Australian samples indicated some difference from the rest of Australia and New Zealand based on candidate loci for C. brachyurus, and potentially also C. obscurus; however, the lack of a reference genome makes the interpretation difficult. Despite similar patterns in both species, subtle and potentially important structure differences emphasise the importance of studying each target species independently rather than assuming similar patterns from closely related species with similar dispersal abilities, as well as considering different marker types in future studies. We found evidence of connectivity across the regions sampled, suggesting that the cumulative effects of regional fisheries and the potential for cross-jurisdictional fishery assessments and management should be considered for Australian, Indonesian, and New Zealand populations.
Source: Illustration by Luisa Rivera/Yale E360;
One hundred pressing questions on the future of global fish migration science, conservation and policy
Lennox, RJ, CP Paukert, and 29 others including BM Gillanders. 2019. Frontiers in Ecology and Evolution 7
Migration is a widespread but highly diverse component of many animal life histories. Fish migrate throughout the world’s oceans, within lakes and rivers, and between the two realms, transporting matter, energy, and other species (e.g., microbes) across boundaries. Migration is therefore a process responsible for myriad ecosystem services. Many human populations depend on the presence of predictable migrations of fish for their subsistence and livelihoods. Although much research has focused on fish migration, many questions remain in our rapidly changing world. We assembled a diverse team of fundamental and applied scientists who study fish migrations in marine and freshwater environments to identify pressing unanswered questions. Our exercise revealed questions within themes related to understanding the migrating individual’s internal state, navigational mechanisms, locomotor capabilities, external drivers of migration, the threats confronting migratory fish including climate change, and the role of migration. In addition, we identified key requirements for aquatic animal management, restoration, policy, and governance. Lessons revealed included the difficulties in generalizing among species and populations, and in understanding the levels of connectivity facilitated by migrating fishes. We conclude by identifying priority research needed for assuring a sustainable future for migratory fishes.
Graphical abstract: Jasmin Martino
Full image and blog available here
Metabolic effects on carbon isotope biomarkers in fish
Martino, JC, ZA Doubleday, BM Gillanders. 2019a. Ecological Indicators 97: 10-16.
Carbon stable isotopes (δ13C) in animal tissues are a powerful tool for tracking biological and environmental change. However, carbon isotope signatures can be altered by both physiological and environmental factors which can cloud interpretation in their use as biomarkers. We investigated metabolic effects (by varying temperatures) on δ13C of three fish tissues (otolith, muscle and liver) and the proportional contributions of environmental water (dissolved inorganic carbon; DIC) and diet (metabolic sources). Juvenile Australasian snapper (Chrysophrys auratus) were laboratory-reared at four temperatures for up to two months and then δ13C in otolith, liver and muscle were measured using isotope-ratio mass spectrometry (IRMS). Temperature significantly altered δ13C signatures in all tissues. δ13C in otoliths reflected carbon signatures from diet and water DIC, with values and variation of proportional contributions influenced by temperature. In muscle and liver, we found
differences in δ13C between tissues and across temperature treatments with concurrent high diet-to-tissue fractionation. We conclude that metabolic effects influenced carbon incorporation for all tissues, with otolith carbon providing valuable insights into field metabolic rates. However, metabolic effects complicated the use of soft-tissue to track diet. This study deepens our understanding of internal and external drivers of carbon isotopic signatures in fish tissues and enhances their utility as a biomarker in the field. Improved insight into biomarkers facilitates more accurate predictions of ecological and environmental change for better understanding and management of wild populations.
Graphical abstract: Jasmin Martino
Larger image and blog available here
Using otolith chronologies to understand long-term trends and extrinsic drivers of growth in fisheries
Martino, JC, AJ Fowler, ZA Doubleday, GL Grammer, BM Gillanders. 2019b. Ecosphere 10, Article e02553.
Identifying trends and drivers of fish growth in commercial species is important for ongoing
sustainable management, but there is a critical shortage of long-term datasets in marine systems. Using otolith (ear bone) sclerochronology and mixed-effects modeling, we reconstructed nearly four decades (37 yr) of growth across four oceanographically diverse regions in an iconic fishery species, snapper (Chrysophrys auratus). Growth was then related to environmental factors (sea surface temperature, chlorophyll-a, and Southern Oscillation Index) and population performance indicators (recruitment and commercial catch). Across the decades, growth rates declined in the two most productive fishery regions. Chlorophyll a (a measure of primary productivity) was the best predictor of growth for all regions, but direction and magnitude of the relationships varied, indicating regional-specific differences in intra-specific competition. Sea surface temperature was positively correlated with fish growth, but negatively correlated after temperature reached optimum thermal maxima, which suggests individuals in warmer regions may be under thermal stress. Growth also decreased at the extremes of the Southern Oscillation Index, indicating fish growth is impeded in significant climatic events. Contrasting relationships between growth, catch, and recruitment indicated regional-specific density-dependent effects, with growth positively correlated with population size in one region but negatively correlated in another. Our results indicate that under future ocean warming and increased frequency of extreme climate events, fish growth and fisheries productivity are likely to be affected. Furthermore, the interactive effects of extrinsic factors also indicated that stressors on fisheries should be managed collectively. We show that otolith chronologies are an effective method to
assess longterm trends and drivers of growth in fishery species. Such informed ecological predictions will help shape the sustainable management of fisheries under future changing climates.
Graphical abstract: Matt McMillan
Larger image available here
Partial female migration and cool-water migration pathways in an overfished shark
McMillan, MN, C Huveneers, JM Semmens, BM Gillanders. 2019. Ices Journal of Marine Science 76: 1083-1093.
Knowledge about reproductive movements can be of important conservation value for over-exploited species that are vulnerable when moving between and within key reproductive habitats. Lack of knowledge persists around such movements in the overfished school shark Galeorhinus galeus in Australia. Management assumes all pregnant females migrate between adult aggregations in the Great Australian Bight, South Australia, and nursery areas around Bass Strait and Tasmania. We tracked 14 late-term pregnant females tagged in South Australia using satellite-linked pop-up archival tags to investigate extent, timing, and routes of migrations. We found partial migration, with some females (n.7) remaining near aggregating areas throughout the pupping season, some migrating to known nursery areas (n.3), and one migrating 3 000 km to New Zealand. We conclude female movements and pupping habitats are less spatially constrained than assumed and propose
females use cool-water routes along the shelf break to reduce energy costs of migration. Migrating females using these routes faced greater fishing pressure than sharks in inshore areas and were not protected by inshore shark fishing closures designed to protect them. This study demonstrates the complexity of reproductive movements that can occur in wide-ranging species and highlights the value of explicit movement data.
Image from paper
Introgressive hybridisation between two widespread sharks in the east Pacific region
Pazmino, DA, L van Herderden, CA Simpfendorfer, C Junge, SC Donnellan, EM Hoyos-Padilla, CAJ Duffy, C Huveneers, BM Gillanders, PA Butcher, GE Maes. 2019. Molecular Phylogenetics and Evolution 136: 119-127.
With just a handful of documented cases of hybridisation in cartilaginous fishes, shark hybridisation remains poorly investigated. Small amounts of admixture have been detected between Galapagos (Carcharhinus galapagensis) and dusky (Carcharhinus obscurus) sharks previously, generating a hypothesis of ongoing hybridisation. We sampled a large number of individuals from areas where the species co-occur (contact zones) across the Pacific Ocean and used both mitochondrial and nuclear-encoded SNPs to examine genetic admixture and introgression between the two species. Using empirical analytical approaches and simulations, we first developed a set of 1873 highly informative SNPs for these two species to evaluate the degree of admixture between them. Overall, results indicate a high discriminatory power of nuclear SNPs (FST=0.47, p < 0.05) between the two
species, unlike mitochondrial DNA (ΦST=0.00 p > 0.05), which failed to differentiate these species. We identified four hybrid individuals (∼1%) and detected bi-directional introgression between C. galapagensis and C. obscurus in the Gulf of California along the east Pacific coast of the Americas. We emphasize the importance of including a combination of mtDNA and diagnostic nuclear markers to properly assess species identification, detect patterns of hybridisation, and better inform management and conservation of these sharks, especially given the morphological similarities within the genus Carcharhinus.
Source: Mark Norman / Museum Victoria. License: CC by Attribution
Element composition of shark vertebrae shows promise as a natural tag
Pistevos, CA, P Reis-Santos, C Izzo, BM Gillanders. 2019. Marine and Freshwater Research 70: 1722-1733.
Reconstructing movements and environmental histories of sharks may be possible by using the element composition of vertebrae, but unlocking such possibilities requires an understanding of the effects of extrinsic and intrinsic factors on element composition. We assessed water temperature and pH effects (independently and in combination) on vertebral chemistry of Port Jackson sharks while accounting for intrinsic factors (condition and sex) using indoor aquaria and outdoor mesocosm environments, where the latter may better reflect natural field conditions. We analysed eight
element : Ca ratios (7Li, 8B, 24Mg, 55Mn, 65Cu, 88Sr, 138Ba and 238U) by laser ablation inductively coupled plasma mass spectrometry and found positive temperature-dependant responses for multiple elements, including B : Ca, Mn: Ca, Sr : Ca and Ba :Ca (r2 . 0.43, 0.22, 0.60 and 0.35 respectively), whereas pH had a minor effect on vertebral Mg:Ca and Li : Ca (r2 . 0.10 and 0.31 respectively). As shown for teleost otoliths, condition affected element composition (Mn : Ca),
suggesting potential physiological influences on element uptake. The suitability of vertebral chemistry as a natural tag appears to be element specific, and likely governed by a suite of potentially codependent extrinsic and intrinsic factors. Overall, variations in vertebrae chemistry show promise to reconstruct movements and habitat use of cartilaginous fishes. Yet, further research is required to understand the ubiquitous nature of the findings presented here.
Graphical abstract: Troy Rogers
Discriminating natal source populations of a temperate marine fish using larval otolith chemistry
Rogers, TA, AJ Fowler, MA Steer, BM Gillanders. 2019a. Frontiers in Marine Science 6, 711.
The life cycles of many marine species depend on a dispersive larval stage that connects spatially segregated populations. However, quantifying larval movement among populations remains one of the greatest challenges in marine ecology. Such movement determines whether a population is essentially a self-recruiting stock, or if it forms part of a larger meta-population where recruits originate from multiple sources. Previous research has struggled to differentiate between such stock structure models for King George whiting (Sillaginodes punctatus; Perciformes) in southern Australia, largely due to difficulties in identifying the source populations of dispersing larvae. In this study,
pelagic larvae were collected throughout the only recognized spawning area in South Australia in 2017 and 2018. First, we identified that the distribution of larvae was broadly divisible into two groups – those in southern Spencer Gulf and those in Investigator Strait. Then, the incremental structure and elemental composition of otoliths of larvae from the two regions were compared to determine if they had originated from a common source population. There were no spatial differences in the sizes (3.0–5.0 mm SL), ages (5–21 days), hatch dates (April 7–24) or average growth rates (0.09–0.21 mm d1) of larvae. However, multi-elemental (Li, Mg, Mn, Sr, and Ba) otolith signatures differed
significantly between the two regions, primarily driven by differences in concentrations of Li and Ba. Although otolith signatures were year-specific, larvae were assigned to their region of capture with 70–82% accuracy. Larvae in each region hatched at the same time yet had significantly different otolith chemistry, providing strong evidence that those in southern Spencer Gulf and Investigator Strait originated from spatially segregated water masses. This study has demonstrated the ability of otolith chemistry to discriminate source populations of pelagic larvae in a fully marine environment, which provides a basis to quantify larval movement between fish populations.
Resolving the early life history of King George whiting (Sillaginodes punctatus: Perciformes) using otolith microstructure and trace element chemistry
Rogers, TA, AJ Fowler, MA Steer, BM Gillanders. 2019b. Marine and Freshwater Research 70: 1659-1674.
Understanding the early life history processes of fish that lead to recruitment is critical for understanding population dynamics. This study explored the early life history of King George whiting (Sillaginodes punctatus) that recruited to an important nursery area in South Australia in 2016 and 2017. The early life history was reconstructed based on the retrospective analysis of otolith microstructure and chemistry for settlement-stage larvae collected fortnightly from July to November. These fish hatched between March and July, but a 3-week period in May led to 52–71% of recruitment. Recruits from successive sampling occasions differed in age, size and growth rate, potentially related to seasonal changes in water temperature and larval food availability. During both years, there were significant changes in otolith elemental chemistry among the groups of recruits that primarily related to changes in Sr : Ca. There are two hypotheses to account for
the differences in otolith chemistry: either (1) a single, primary spawning source and within-season environmental change; or (2) multiple spawning sources. Further investigation with oceanographic models of larval dispersal will help differentiate between these. The retrospective analysis of otoliths has improved the understanding of early life history for this important species, with implications for fishery management.
Source: Julian K. Finn / Museum Victoria. License: CC by Attribution
Spatial connectivity during the early life history of a temperate marine fish inferred from otolith microstructure and geochemistry
Rogers, TA, AJ Fowler, MA Steer, BM Gillanders. 2019c.
Estuarine Coastal and Shelf Science 227.
Connectivity during the ontogenetic development of fishes identifies the spatial scale over which populations function, which is the appropriate scale for conservation and management. For many marine species, spawning grounds and nursery areas are spatially segregated and larval dispersal is an obligate process that connects life history stages. This study investigated the spatial scale of early life history for one such species, the King George whiting (Sillaginodes punctatus; Perciformes), through the retrospective analysis of otolith microstructure and elemental chemistry of recently-settled larvae. The aim was to determine whether the South Australian population constitutes a single panmictic stock, or if it comprises multiple sub-populations. Sizes (15.1–25.1mm SL), ages (85–183 d) and hatch dates (24-Apr to 1-Aug) of larvae varied considerably between nursery areas at
different spatial scales. Regional differences in multi-elemental otolith signatures indicated that multiple spawning grounds contribute to recruitment, and larvae that settled in each region dispersed through different water masses. Within each region, there were differences in hatch dates and otolith chemistry indicative of finer scale relationships between particular spawning grounds and nursery areas, consistent with local oceanographic circulation patterns. Although multi-elemental signatures were year-specific, concentrations of Ba and Mn were largely responsible for spatial differences and assigned larvae to regional groups with 52–66% accuracy. The results suggest the State-wide stock is replenished by three putative source populations, and provide an example of how otolith chemistry can discriminate among geographically-close, yet-ecologically separated groups of fish in coastal marine ecosystems.
Graphical abstract: Troy Rogers
Introduction to the 6th International Otolith Symposium - Editorial
Wang, C.H., B.D. Walther, B.M. Gillanders. 2019. Marine and Freshwater Research 70: I-III.
Otoliths have served as natural recorders of fish life-history information for over a century. Many of the analytical methodologies developed for otoliths have been further applied to other calcified structures in aquatic organisms and those techniques have provided analogous biological, ecological and environmental information. This special issue includes a selection of papers that were presented in the 6th International Otolith Symposium in Taiwan and highlight the recent developments and advances of otolith research.
All papers in the special issue are open access - available here.
Image: Part of cover of Marine and Freshwater Research special issue
Goyder Blue Carbon Research projects: Synthesis report
Jones, AR, S Dittmann, L Mosley, M Clanahan, K Beaumont, M Walcott, BM Gillanders 2019. Goyder Institute for Water Research Technical Report Series No. 19/30
Blue carbon refers to the carbon that is captured and stored in coastal vegetated ecosystems. Over the last two years, two collaborative Goyder Institute for Water Research funded research projects have been undertaken in South Australia investigating blue carbon: the Coastal Carbon Opportunities project led through the University of Adelaide and the Salt-to-C project led through Flinders University. The Coastal Carbon Opportunities project estimated baseline carbon stocks and carbon storage dynamics at case study sites within South Australian coastal carbon ecosystems and assessed the impact of degradation and restoration on blue carbon sequestration and stocks. The Salt-to-C project investigated whether tidal re-connection and restoration of the Dry Creek salt fields could provide a pathway towards realising blue carbon opportunities for South Australia.
A wealth of technical knowledge has been produced in both blue carbon research projects, filling some critical knowledge gaps around the sequestration of carbon and its long-term storage in South Australian coastal ecosystems. Knowledge synthesis and transfer are critical to making the most of these outputs and so this report synthesises key outcomes from both projects. The report outlines the distribution of blue carbon ecosystems in the state and estimates of carbon sequestration and stocks and will support the South Australian Government’s strategic objectives related to blue carbon.
Besides this synthesis report there were 8 reports from the Coastal Carbon Opportunities project plus 2 reports from the Salt to C project, as well as a Research Agenda for Blue Carbon in South Australia produced - all reports are available at the link below.
Image: Rene Campbell Art
 Near Calperun Station, SA |  Giant Australian cuttlefish |  Flinders Chase |
|---|---|---|
 Tourville Bay |  Streaky Bay |  Kangaroo Island |
 Routeburn Track |  White Island |