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Selection of top publications (links to each paper available at read more)

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Towards better identification, conservation and management of estuarine and marine nurseries

Beck, MW, KL Heck, KW Able, DL Childers, DB Eggleston, BM Gillanders, B Halpern, CG Hays, K Hoshino, TJ Minello, RJ Orth, PF Sheridan and MW Weinstein. 2001. Bioscience 51: 633-641.

Nearshore estuarine and marine ecosystems—e.g., seagrass meadows, marshes, and mangrove forests— serve many important functions in coastal waters. Most notably, they have extremely high primary and secondary productivity and support a great abundance and diversity of fish and invertebrates. Because of their effects on the diversity and productivity of macrofauna, these estuarine and marine ecosystems are often referred to as nurseries in numerous papers, textbooks, and government-sponsored reports. Indeed, the role of these nearshore ecosystems as nurseries is an established ecological concept accepted by scientists, conservation groups, managers, and the public and cited as justification for the protection and conservation of these areas. Nonetheless, the nursery-role concept has rarely been stated clearly, even in papers that purport to test it. This ambiguity hinders the effectiveness of the nursery-role concept as a tool for conservation and management. We seek to redress that ambiguity by briefly tracing the history of the concept, developing a clear hypothesis with testable predictions, and discussing how this work can focus efforts in research, conservation, restoration, and management.

Graphic: Nina Wootton

Output from an NCEAS working group investigating evidence for the nursery hypothesis.

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Graphic: Nina Wootton

Otolith chemistry to describe movements and life history parameters of fishes: hypotheses, assumptions, limitations, and inferences

Elsdon, TS, BK Wells, SE Campana, BM Gillanders, CM Jones, KE Limburg, DH Secor, SR Thorrold, BD Walther. 2008. Oceanography and Marine Biology: an Annual Review 46: 297-330.

In ever-increasing numbers, researchers wish to extract information based on chemical analyses from otoliths to determine movements and life-history patterns of fish. Such analyses make assumptions about chemical incorporation and interpretation that are beyond those that are important for stock discrimination studies, another common application. The authors aim to clarify the methods of determining fish movement based on natural and artificial otolith chemical tags and review current trends in determining movement using otolith chemistry, otolith sampling methods, and what influences otolith chemistry. Both spatial and temporal variability in water and otolith chemistries, which underpin the assumptions of several methods, are discussed. Five methods for determining movement and migration of fish are outlined: (1) estimates of movement and life-history traits of a single fish group, (2) assessing connectivity among groups using natural chemical tags in otoliths, (3) transgenerational marks to determine parentage and natal origins, (4) profile analysis to define life-history variation within a population and (5) profile analysis to describe movements through different environments. Within each of these methods, background information, specific hypotheses being tested and assumptions and limitations of each technique are provided. Finally, research directions required to fill current knowledge gaps and enhance the usefulness of otolith chemistry to determine fish movement are identified.

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Image: Classic concept of species with nursery habitats showing connectivity between juvenile and adult populations. Graphic: Nina Wootton.

Output from an NCEAS working group investigating evidence for the nursery hypothesis.

Evidence for connectivity between juvenile and adult habitats for mobile marine fauna: an important component of nurseries

Gillanders, BM, KW Able, JA Brown, DB Eggleston and PF Sheridan. 2003. Marine Ecology Progress Series 247: 281-295.

A critical link missing from our understanding of the nursery role of specific marine habitats is the evidence of connectivity between juvenile and adult habitats. This paper reviews and evaluates evidence of, and spatial scales for, movements from juvenile to adult habitats and it summarises the methods used to study movements. Examples include many fish families but few invertebrate taxa, and most are species of economic importance for USA and Australia. The types of juvenile habitat range from the entire estuary or shallow open coastal waters to specific habitats within estuaries or coastal waters; in some cases juvenile habitats include habitats not traditionally regarded as nursery areas (e.g. the surf zone). The duration of time spent in juvenile habitats averages 13 mo (range 8 d to 5 yr). The majority of organisms move distances of kilometres to hundreds of kilometres from juvenile to adult habitats, although the scale of movements ranged from metres to thousands of kilometres. Changes in abundance among separate habitats and the progression of size classes among separate habitats are the main methods used to infer movement and habitat connectivity. Spatial partitioning of stages of maturity, natural parasites, and a variety of artificial tagging methods have also been used. The latter will become more useful with continued developments in the miniaturisation of artificial tags. More recent studies have used natural tags (e.g. trace elements and stable isotopes) and these methods show great promise for determining movements from juvenile to adult habitats. Few studies provide good evidence for movement from specific juvenile habitats to adult habitats. Future studies need to focus on this movement to supplement data on density, growth and survival of organisms in putative nursery habitats. Such information will allow management and conservation efforts to focus on those habitats that make the greatest contribution to adult populations.

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Image: Seagrass meadow. CC-BY-CA-4.0; Milorad Mikota

Marine nurseries and effective juvenile habitats: concepts and application

Dahlgren, CP, T Kellison, AJ Adams, BM Gillanders, MS Kendall, C Layman, JA Ley, I Nagelkerken and JE Serafy. 2006. Marine Ecology Progress Series 312: 291-295.

Much recent attention has been focused on juvenile fish and invertebrate habitat use, particularly defining and identifying marine nurseries. The most significant advancement in this area has been the development of a standardized framework for assessing the relative importance of juvenile habitats and classifying the most productive as nurseries. Within this framework, a marine nursery is defined as a juvenile habitat for a particular species that contributes a greater than average number of individuals to the adult population on a per-unit-area basis, as compared to other habitats used by juveniles. While the nursery definition and framework provides a powerful approach to identifying habitats for conservation and restoration efforts, it can omit habitats that have a small per-unit-area contribution to adult populations, but may be essential for sustaining adult populations. Here we build on the nursery concept by developing a framework for evaluating juvenile habitats based on their overall contribution to adult populations, and introduce the concept of Effective Juvenile Habitat (EJH) to refer to habitats that make a greater than average overall contribution to adult populations.

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Graphic: Charlotte Gauthier, visiting PhD student

Output from Travis Elsdon's fourth year Honours research project.

Interactive effects of temperature and salinity on otolith chemistry: challenges for determining environmental histories of fish

Elsdon, TS and BM Gillanders. 2002. Canadian Journal of Fisheries and Aquatic Sciences 59: 1796-1808.

The concentrations of elements and isotopes in fish otoliths may provide a method of reconstructing movements of fish by differentiating between water bodies of different temperatures and salinities. However, before otoliths can be used to reconstruct environmental histories of fish, it is necessary to assess the effects of seawater temperature and salinity on otolith microchemistry. Using controlled laboratory experiments, juvenile black bream, Acanthopagrus butcheri (family Sparidae), were reared for 50 days in aquaria of varying temperatures and salinities using three experimental designs: temperature × salinity, temperature only, and salinity only. Temperature and salinity interacted to significantly affect the elemental concentration ratios of Sr:Ca and Ba:Ca and the concentrations of isotopes δ13C and δ18O in otoliths. The single-factor experiments showed that temperature significantly affected the concentration ratios of Sr:Ca and Ba:Ca and the concentrations of δ13C and δ18O in otoliths, whereas salinity alone did not affect the concentration ratios of any elements but did affect both isotopes. The concentration ratios of Mg:Ca and Mn:Ca varied considerably among fish within the same treatment level and showed little or no effects due to temperature and (or) salinity. The significant interactive effects of temperature and salinity on otolith microchemistry highlight the need for a multifactorial approach to testing hypotheses regarding the environmental histories of fish.

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Image: Zambezi River delta pouring water and sediment into the Indian Ocean through a vast delta in Mozambique. From: https://earthobservatory.nasa.gov/images/82361/zambezi-river-delta

Impact of changes in flow of freshwater on estuarine and open coastal habitats and the associated organisms

Gillanders, BM and MJ Kingsford. 2002. Oceanography and Marine Biology: an Annual Review 40: 233-309.

Freshwater is scarce in many regions of the world. In some areas, water entitlements currently exceed the available water supply yet few proposals for regulating quantities extracted are scrutinised in terms of possible impacts or undergo any form of rigorous impact assessment. In addition, there is little understanding of the potential impacts. There is a growing need to understand better the impact of altered flows of fresh water on estuarine and open coastal marine systems. There is a perception that fresh water is lost when it enters the marine environment. We argue that freshwater—saltwater dynamics have profound influences on coastal ecosystems. The purpose of this paper is to review the nature of freshwater discharges and the effects of fresh water on the physical aspects of estuaries as well as estuarine and marine flora, fauna and habitats. Although the review focuses on decreased flows to marine systems, major increases in flow can also have a major impact on estuarine and coastal systems. Freshwater runoff is a function of numerous environmental variables, depending primarily on climate (precipitation and evaporation) and the physical characteristics of the drainage

basin. Anthropogenic activities in catchments may result in diversions and reductions in freshwater flow, alterations of timing and rates of flow to estuarine and coastal systems, and/or adverse water quality conditions with major changes in nutrient loading. Sediment loads, pH, temperature, salinity, clarity, oceanography and nutrients are affected. Perturbations in coastal systems can be freshwater pulses (i.e. storms or opening of floodgates) or press scenarios (i.e. persistent flow of low variation from rivers or industry). Impacts on organisms can also be categorised as pulse events (where there is a rapid but not sustained change), or press events (where changes are sustained over long periods of time). Changes to freshwater input affect habitats and organisms within estuaries. The effects include mortality, changes in growth and development, and in some cases movement of organisms. Major mortalities are most likely during pulse events of freshwater input. There is considerable descriptive and small-scale experimental evidence to suggest that a variety of organisms may be affected by changes to freshwater input. Much of the experimental evidence focuses on single factor experiments and rarely have there been multifactorial experiments (an exception is seagrasses). In addition, there have been no large-scale experiments (e.g. size of sample unit 10’s to 100’s of metres), although it is acknowledged that such experiments will be difficult. We suggest that any changes in water management (e.g. removal of water for irrigation) should be treated as manipulative experiments and that estuarine and marine systems are monitored together with reference or control locations (where there has been no change) to determine the impact of such changes. At the large scale, finding suitable control locations could be difficult. Data should be collected multiple times prior to and after the change has occurred. In the first instance, objective scientific evidence should be used for decision-making and when that is not available, we suggest that the principle of precautionary action should be adhered to. In conclusion, freshwater flows have a great impact on physical and biological aspects of coastal environments. The impacts of fresh water on marine environments, as well as terrestrial environments, should therefore, be considered by managers.

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Graphic: Charlotte Gauthier, visiting PhD student

Reconstructing migratory patterns of fish based on environmental influences on otolith chemistry

Elsdon, TS and BM Gillanders. 2003. Reviews in Fish Biology and Fisheries 13: 219-235.

The analysis of elements in calcified structures of fish (e.g., otoliths) to discriminate among fish stocks and determine connectivity between populations is becoming widespread in fisheries research. Recently, the concentrations of elements in otoliths are being analysed on finer scales that allow the determination of a continuous record of otolith chemistry over a fish's entire life history. These elemental concentrations can potentially be used to reconstruct migration patterns, based upon the influence that water chemistry, temperature, and salinity have on otolith chemistry. In doing so, assumptions are made about how environmental and biological factors influence the concentration of elements in fish otoliths. However, there have been few experiments that have tested crucial assumptions regarding what influences elemental uptake and incorporation into fish otoliths. Specifically, knowledge regarding interactions among environmental variables, such as the ambient concentration of elements in water, temperature, and salinity, and how they may affect otolith chemistry, is limited. Similarly, our understanding of the rate at which elements are incorporated into otoliths and the implications this may have for interpretations is lacking. This review discusses methods of determining movement offish, the development of otolith research, and some physiological aspects of otoliths (e.g., pathways of elemental uptake). The types of analysis techniques that will lead to reliable and accurate migratory reconstructions are outlined. The effects that have on otolith chemistry are reviewed with the specific aim of highlighting areas lacking environmental variables in experimental data. The influences of the rate of elemental incorporation and ontogeny on otolith chemistry are also addressed. Finally, future research directions are suggested that will fill the gaps in our current knowledge of otolith chemistry. Hypotheses that need to be tested in order to reconstruct the migratory histories of fish are outlined, in a bid to clarify the direction that research should take before complex reconstructions are attempted.

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Graphic: Nina Wootton

Elements in otoliths may elucidate the contribution of estuarine recruitment to sustaining coastal reef populations of a temperate reef fish

Gillanders, BM and MJ Kingsford. 1996. Marine Ecology Progress Series 141: 13-20.

Estuaries and associated seagrass habitats are thought to be important nursery areas for many fishes. There is, however, no direct evidence for movement of fish from estuaries to reefs. The aim of this study was to determine if populations of Achoerodus viridis (Labridae) on rocky reefs were sustained by (1) recruitment to estuarine seagrass habitat followed by movement to rocky reefs, (2) direct recruitment to rocky reefs, or (3) a combination of the two. Recruits were collected from estuarine seagrass and rocky reef habitats and elements in their otoliths analysed by inductively coupled plasma-mass spectrometry (ICP-MS) to determine if different 'elemental fingerprints' could be found. Higher concentrations of Zn, Al, Pb, Mn, Ba and Co were found in otoliths of recruits from estuarine seagrass habitat than in otoliths of recruits from coastal reefs, the latter 3 elements showing significant differences. Strontium occurred in significantly higher concentrations in otoliths of recruits from coastal reefs. Differences in concentrations of some elements in the otoliths of recruits allowed fish from the 2 environments to be distinguished with a high degree of accuracy, enabling the contribution of estuarine recruitment to sustaining reef populations to be determined. Elemental composition of the juvenile core of otoliths from adults on reefs was related to the composition of otoliths of recruits from each environment to identify historical recruitment environments. Discriminant function analysis showed that 41% of adults had recruited to estuaries and 59% had recruited to reefs, but these figures may be overestimated because adults must be assigned to 1 of the 2 groups. There was evidence to suggest that some adults may form a third intermediate group. Further validation (e.g. comparison with laser or probe based methods and tagging techniques) of our approach is warranted. Elemental techniques may have great potential for resolving fisheries problems and identifying broader scale effects of environmental degradation.

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Image: Graphic associated with paper.

Global proliferation of cephalopods

Doubleday ZA, TAA Prowse, A Arkhipkin, GJ Pierce, J Semmens, M Steer, SC Leporati, S Lourenço, A Quetglas, W Sauer, BM Gillanders. 2016. Current Biology 26: R387-R407.

Human activities have substantially changed the world’s oceans in recent decades, altering marine food webs, habitats and biogeochemical processes. Cephalopods (squid, cuttlefish and octopuses) have a unique set of biological traits, including rapid growth, short lifespans and strong life-history plasticity, allowing them to adapt quickly to changing environmental conditions. There has been growing speculation that cephalopod populations are proliferating in response to a changing environment, a perception fuelled by increasing trends in cephalopod fisheries catch. To investigate long-term trends in cephalopod abundance, we assembled global time-series of cephalopod catch rates (catch per unit of fishing or sampling effort). We show that cephalopod populations have increased over the last six decades, a result that was remarkably consistent across a highly diverse set of cephalopod taxa. Positive trends were also evident for both fisheries-dependent and fisheries-independent time-series, suggesting that trends are not solely due to factors associated with developing fisheries. Our results suggest that large-scale, directional processes, common to a range of coastal and oceanic environments, are responsible. This study presents the first evidence that cephalopod populations have increased globally, indicating that these ecologically and commercially important invertebrates may have benefited from a changing ocean environment.

Potential effects of climate change on Australian estuaries and fish utilising estuaries: a review

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Image: Potential links between climate variability and anthropogenic influences on estuarine environments.

Gillanders, BM, TS Elsdon, IA Halliday, GP Jenkins, JB Robins, FJ Valesini. 2011. Marine and Freshwater Research 62: 1115-1131.

Estuaries are especially vulnerable to the impacts of climate change because changes in climatic and hydrologic variables that influence freshwater and marine systems will also affect estuaries. We review potential impacts of climate change on Australian estuaries and their fish. Geographic differences are likely because southern Australian climates are predicted to become warmer and drier, whereas northern regions may see increased precipitation. Environmental factors, including salinity gradients, suspended sediment, dissolved oxygen and nutrient concentrations, will be influenced by changing freshwater input and other climate variables. Potential impacts will vary depending on the geomorphology of the estuary and the level of build-up of sand bars across estuarine entrances. Changes to estuarine fish assemblages will depend on associated changes to salinity and estuarine-mouth morphology. Marine migrants may be severely affected by closure of estuarine mouths, depending on whether species ‘must’ use estuarine habitat and the level of migratory v. resident individuals. Depending on how fish in coastal waters locate estuaries, there may be reduced cues associated with estuarine mouths, particularly in southern Australia, potentially influencing abundance. In summary, climate change is expected to have major consequences for Australian estuaries and associated fish, although the nature of impacts will show significant regional variation.

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Graphic: Nina Wootton

Output from Melita deVries fourth year Honours research project.

Facilitation of barium uptake into fish otoliths: Influence of strontium concentration and salinity

de Vries, MC, BM Gillanders and TS Elsdon. 2005. Geochimica et Cosmochimica Acta 69: 4061-4072.

To reconstruct patterns of fish migration using otolith chemistry, it is essential to validate the relationship between elements in otoliths and the surrounding water, and in particular, how processes such as competition and facilitation among multiple elements influence otolith chemistry. Using a controlled laboratory experiment, juvenile black bream (Acanthopagrus butcheri) were reared in both brackish and seawater spiked with different concentrations of Sr and Ba. The addition of Sr to the solution facilitated the uptake of Ba into otoliths of fish reared in brackish water, but not in seawater. Conversely, Ba did not facilitate nor compete with the uptake of Sr in either brackish or seawater. In brackish water, Sr incorporation into otoliths may create crystal defects within the CaCO3 matrix, enabling greater incorporation of Ba. Ba:Ca partition coefficients (DBa) for brackish and seawater were 0.058 and 0.136, respectively, whereas Sr:Ca partition coefficients (DSr) for brackish and seawater were 0.463 and 0.287, respectively. The influence of Sr on Ba incorporation in fish otoliths is important to consider when reconstructing migration histories of fish, especially in brackish water environments.

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Image: Statolith of a recently hatched juvenile cuttlefish showing position of laser ablation through the lateral dome.

Output from Leanne Wilkinson's fourth year Honours research project.

Statolith chemistry of two life history stages of cuttlefish: Effects of temperature and seawater trace element concentration

Gillanders, BM, LM Wilkinson, AR Munro and MC de Vries. 2013. Geochimica et Cosmochimica Acta 101: 12-23.

The influence of seawater trace element concentration and temperature on statolith chemistry of the giant Australian cuttlefish, Sepia apama, was compared between encapsulated embryos and recently hatched juveniles under controlled laboratory conditions. Seawater Sr/Ca and Ba/Ca were positively related to statolith Sr/Ca and Ba/Ca in embryos and hatchlings for all temperatures. For statoliths of embryos the effect of spiking increased at 14 °C compared to 20 °C but for hatchlings increased Sr/Ca and Ba/Ca ratios in statoliths were found at 20 °C compared to 14 °C. The results imply that the influence of seawater trace element concentration and temperature on statolith chemistry was driven by elemental discrimination as described by partition coefficients but was reversed between life history stages. Differences in respiration and haemocyanin between the two life history stages may influence elemental uptake and discrimination. Thus, the results of the present study indicate that differences in element uptake in statoliths can occur among life history stages of S. apama and must be considered when reconstructing environmental histories of S. apama and other statolith bearing organisms.

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Image: Graphic from paper.

Strontium randomly substituting for calcium in fish otolith aragonite

Doubleday, ZA, HH Harris, C Izzo and BM Gillanders. 2014. Analytical Chemistry 86: 865-869.

The chemistry of fish ear bones (otoliths) is used to address fundamental questions in fish ecology and fisheries science. It is assumed that strontium (Sr), the most important element used in otolith chemistry research, is bound within the aragonitic calcium carbonate lattice of otoliths via random chemical replacement of calcium; however, this has never been tested and three other alternatives exist with regard to how Sr may be incorporated. If any variation in the mode of incorporation occurs, otolith chemistry data may be misinterpreted, impacting how fish and fisheries are understood and managed. Using X-ray absorption spectroscopy (specifically, analysis of extended X-ray absorption fine structure or EXAFS), we investigated how Sr is incorporated within fish otoliths from seven species collected from a range of aquatic environments. For comparison, aragonitic structures from other aquatic taxa (cephalopods and coral) were also analyzed. The results consistently indicated for all samples that Sr randomly replaces Ca within the aragonite lattice. This research explicitly shows how Sr is bound within otoliths and validates a fundamental and long-held assumption in aquatic research.

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Partial migration: Growth varies between resident and migratory fish

Gillanders, BM, C Izzo, ZA Doubleday and Q Ye. 2015. Biology Letters 11: 20140850.

Partial migration occurs in many taxa and ecosystems and may confer survival benefits. Here, we use otolith chemistry data to determine whether fish from a large estuarine system were resident or migratory, and then examine whether contingents display differences in modelled growth based on changes in width of otolith growth increments. Sixty-three per cent of fish were resident based on Ba : Ca of otoliths, with the remainder categorized as migratory, with both contingents distributed across most age/size classes and both sexes, suggesting population-level bet hedging. Migrant fish were in slightly better condition than resident fish based on Fulton's K condition index. Migration type (resident versus migratory) was 56 times more likely to explain variation in growth than a model just incorporating year- and age-related growth trends. While average growth only varied slightly between resident and migratory fish, year-to-year variation was significant. Such dynamism in growth rates likely drives persistence of both life-history types. The complex relationships in growth between contingents suggest that management of species exhibiting partial migration is challenging, especially in a world subject to a changing climate.

Graphic: Charlotte Gauthier, visiting PhD student

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Image: Graphical abstract made by Animate Your Science.

Otolith chemistry does not just reflect environmental conditions: A meta-analytic evaluation

Izzo, C, P Reis-Santos and BM Gillanders. 2018. Fish and Fisheries 19: 441-454.

Fish otoliths are widely used to answer biological and ecological questions related to movements and habitat use based on their chemical composition. Two fundamental assumptions underlie otoliths as environmental tracers and proxies for reconstructing exposure histories: (i) otolith chemistry reflects water chemistry, and (ii) ambient environmental conditions affect otolith element incorporation. Here, we test these assumptions for Sr and Ba through meta-analyses. Our first meta-analysis confirmed a correlation between concentrations of Sr:Ca and Ba:Ca in otoliths and the surrounding water, both elements displaying positive otolith–water correlations. The second meta-analysis examined the relative influences of salinity and temperature on otolith Sr and Ba partition coefficients (an index of otolith element regulation). Our environmental effects meta-analysis confirmed that otolith Sr and Ba are affected by temperature and salinity; however, study-level covariates (e.g., water chemical concentrations and species ecological niche) influenced otolith element incorporation, and this varied by element. These findings confirm that even though otolith chemistry and elemental incorporation are differentially affected by environmental conditions, other factors play a decisive role. While we focused on studies that directly linked water and otolith chemistry, systematic reviews are key to further demonstrate the link between otolith chemistry and extrinsic and intrinsic factors. Ultimately, disentangling the relative effects of multiple factors on otolith chemistry and a detailed understanding of biomineralization is critical to the continued use of otoliths as natural tags for tracing fish movements and habitat use.

Near Calperun Station, SA

Near Calperun Station, SA

Giant Australian cuttlefish

Giant Australian cuttlefish

Flinders Chase

Flinders Chase

Tourville Bay

Tourville Bay

Streaky Bay

Streaky Bay

Kangaroo Island

Kangaroo Island

Routeburn Track

Routeburn Track

White Island

White Island

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