Zoë A. Doubleday

Rapid assessment of fisheries species sensitivity to climate change

Climate change driven alterations in the distribution and abundance of marine species, and the timing of their life history events (phenology), are being reported around the globe. However, we have limited capacity to detect and predict these responses, even for comparatively well studied commercial fishery species. Fisheries provide significant socio-economic benefits for many coastal communities, and early warning of potential changes to fish stocks will provide managers and other stakeholders with the best opportunity to adapt to these impacts. Rapid assessment methods that can estimate the sensitivity of species to climate change in a wide range of contexts are needed. This study establishes an objective, flexible and cost effective framework for prioritising future ecological research and subsequent investment in adaptation responses in the face of resource constraints. We build on an ecological risk assessment framework to assess relative sensitivities of commercial species to climate change drivers, specifically in relation to their distribution, abundance and phenology, and demonstrate our approach using key species within the fast warming region of south-eastern Australia. Our approach has enabled fisheries managers to understand likely changes to fisheries under a range of climate change scenarios, highlighted critical research gaps and priorities, and assisted marine industries to identify adaptation strategies that maximise positive outcomes.

Global proliferation of cephalopods

Human activities have substantially changed the worlds oceans in recent decades, altering marine food webs, habitats and biogeochemical processes [1]. 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 [2-4]. 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 [4,5]. 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.

Strontium randomly substituting for calcium in fish otolith aragonite

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.

Partial migration: growth varies between resident and migratory fish

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 Fultons 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.

How ocean acidification can benefit calcifiers

Reduction in seawater pH due to rising levels of anthropogenic carbon dioxide (CO2) in the worlds oceans is a major force set to shape the future of marine ecosystems and the ecological services they provide [1,2]. In particular, ocean acidification is predicted to have a detrimental effect on the physiology of calcifying organisms [3]. Yet, the indirect effects of ocean acidification on calcifying organisms, which may counter or exacerbate direct effects, is uncertain. Using volcanic CO2 vents, we tested the indirect effects of ocean acidification on a calcifying herbivore (gastropod) within the natural complexity of an ecological system. Contrary to predictions, the abundance of this calcifier was greater at vent sites (with near-future CO2 levels). Furthermore, translocation experiments demonstrated that ocean acidification did not drive increases in gastropod abundance directly, but indirectly as a function of increased habitat and food (algal biomass). We conclude that the effect of ocean acidification on algae (primary producers) can have a strong, indirect positive influence on the abundance of some calcifying herbivores, which can overwhelm any direct negative effects. This finding points to the need to understand ecological processes that buffer the negative effects of environmental change.

A multilevel approach to examining cephalopod growth using Octopus pallidus as a model

SUMMARY Many aspects of octopus growth dynamics are poorly understood, particularly in relation to sub-adult or adult growth, muscle fibre dynamics and repro-somatic investment. The growth of 5 month old Octopus pallidus cultured in the laboratory was investigated under three temperature regimes over a 12 week period: seasonally increasing temperatures (14–18°C); seasonally decreasing temperatures (18–14°C); and a constant temperature mid-way between seasonal peaks (16°C). Differences in somatic growth at the whole-animal level, muscle tissue structure and rate of gonad development were investigated. Continuous exponential growth was observed, both at a group and at an individual level, and there was no detectable effect of temperature on whole-animal growth rate. Juvenile growth rate (from 1 to 156 days) was also monitored prior to the controlled experiment; exponential growth was observed, but at a significantly faster rate than in the older experimental animals, suggesting that O. pallidus exhibit a double-exponential two-phase growth pattern. There was considerable variability in size-at-age even between individuals growing under identical thermal regimes. Animals exposed to seasonally decreasing temperatures exhibited a higher rate of gonad development compared with animals exposed to increasing temperatures; however, this did not coincide with a detectable decline in somatic growth rate or mantle condition. The ongoing production of new mitochondria-poor and mitochondria-rich muscle fibres (hyperplasia) was observed, indicated by a decreased or stable mean muscle fibre diameter concurrent with an increase in whole-body size. Animals from both seasonal temperature regimes demonstrated higher rates of new mitochondria-rich fibre generation relative to those from the constant temperature regime, but this difference was not reflected in a difference in growth rate at the whole-body level. This is the first study to record ongoing hyperplasia in the muscle tissue of an octopus species, and provides further insight into the complex growth dynamics of octopus.

Long-term patterns in estuarine fish growth across two climatically divergent regions

Long-term ecological datasets are vital for investigating how species respond to changes in their environment, yet there is a critical lack of such datasets from aquatic systems. We developed otolith growth ‘chronologies’ to reconstruct the growth history of a temperate estuarine fish species, black bream (Acanthopagrus butcheri). Chronologies represented two regions in south-east Australia: South Australia, characterised by a relatively warm, dry climate, and Tasmania, characterised by a relatively cool, wet climate. Using a mixed modelling approach, we related inter-annual growth variation to air temperature, rainfall, freshwater inflow (South Australia only), and El Niño–Southern Oscillation events. Otolith chronologies provided a continuous record of growth over a 13- and 21-year period for fish from South Australia and Tasmania, respectively. Even though fish from Tasmania were sourced across multiple estuaries, they showed higher levels of growth synchronicity across years, and greater year-to-year growth variation, than fish from South Australia, which were sourced from a single, large estuary. Growth in Tasmanian fish declined markedly over the time period studied and was negatively correlated to temperature. In contrast, growth in South Australian fish was positively correlated to both temperature and rainfall. The stark contrast between the two regions suggests that Tasmanian black bream populations are more responsive to regional scale environmental variation and may be more vulnerable to global warming. This study highlights the importance of examining species response to climate change at the intra-specific level and further validates the emerging use of growth chronologies for generating long-term ecological data in aquatic systems.

Contribution of water chemistry and fish condition to otolith chemistry: comparisons across salinity environments

This study quantified the per cent contribution of water chemistry to otolith chemistry using enriched stable isotopes of strontium ((86) Sr) and barium ((137) Ba). Euryhaline barramundi Lates calcarifer, were reared in marine (salinity 40), estuarine (salinity 20) and freshwater (salinity 0) under different temperature treatments. To calculate the contribution of water to Sr and Ba in otoliths, enriched isotopes in the tank water and otoliths were quantified and fitted to isotope mixing models. Fultons K and RNA:DNA were also measured to explore the influence of fish condition on sources of element uptake. Water was the predominant source of otolith Sr (between 65 and 99%) and Ba (between 64 and 89%) in all treatments, but contributions varied with temperature (for Ba), or interactively with temperature and salinity (for Sr). Fish condition indices were affected independently by the experimental rearing conditions, as RNA:DNA differed significantly among salinity treatments and Fultons K was significantly different between temperature treatments. Regression analyses did not detect relations between fish condition and per cent contribution values. General linear models indicated that contributions from water chemistry to otolith chemistry were primarily influenced by temperature and secondly by fish condition, with a relatively minor influence of salinity. These results further the understanding of factors that affect otolith element uptake, highlighting the necessity to consider the influence of environment and fish condition when interpreting otolith element data to reconstruct the environmental histories of fish.

Fish as proxies of ecological and environmental change

Anthropogenic impacts have shifted aquatic ecosystems far from prehistoric baseline states; yet, understanding these impacts is impeded by a lack of available long-term data that realistically reflects the organisms and their habitats prior to human disturbance. Fish are excellent, and largely underused, proxies for elucidating the degree, direction and scale of shifts in aquatic ecosystems. This paper highlights potential sources of qualitative and quantitative data derived from contemporary, archived and ancient fish samples, and then, using key examples, discusses the types of long-term temporal information that can be obtained. This paper identifies future research needs with a focus on the Southern Hemisphere, as baseline shifts are poorly described relative to the Northern Hemisphere. Temporal data sourced from fish can improve our understanding of how aquatic ecosystems have changed, particularly when multiple sources of data are used, enhancing our ability to interpret the current state of aquatic ecosystems and establish effective measures to safeguard against further adverse shifts. The range of biological, ecological and environmental data obtained from fish can be integrated to better define ecosystem baseline states on which to establish policy goals for future conservation and exploitation practices.

Where do elements bind within the otoliths of fish

Otolith element analyses are used extensively to reconstruct environmental histories of fish based on the assumption that elements substitute for calcium within the CaCO3 otolith structure. However, elements may also be incorporated within the protein component of the otolith in addition to the direct substitution for calcium in the mineral component, and this could introduce errors in environmental reconstructions. The aim of the present study was to determine whether elements were incorporated into the protein or mineral components of otoliths and the relative proportion of each element in each component. Element concentrations from whole ground otoliths and the isolated protein component were quantified using solution inductively coupled plasma mass spectrometry (ICP-MS). Of the 12 elements investigated, most were found in both the proteinaceous and mineral components, but always in greater concentrations in the latter. Elements considered ‘non-essential’ to fish physiology with Ca-like properties (i.e. alkaline metals) were present in the mineral component in relatively high concentrations. Elements essential to fish physiology with smaller atomic radii than Ca (i.e. transition metals) were distributed throughout the protein and mineral components of the otolith. These findings enhance our understanding of element incorporation in the otolith and, ultimately, improve interpretations of otolith-based environmental reconstructions.