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Physiological and behavioural mechanisms underpinning the climate-driven range extension of snapper Chrysophrys auratus in southeast Tasmania

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posted on 2023-05-28, 00:11 authored by Barrett WolfeBarrett Wolfe
Geographical species redistributions are among the primary ecological responses to global climate change. In subtropical and temperate oceans, the predominant climate-driven distributional responses are range extensions, which outpace warm, trailing range-edge contractions by four times over on average. Climate-driven species range extensions have unpredictable consequences for recipient communities and the provision of associated ecosystem services, presenting a critical concern for management. However, the rates of species' responses to changing climate vary considerably, preventing accurate forecasts of range extensions based on climate data alone. Most of this variability appears to arise from the dynamic physiological and behavioural traits which underpin ectothermic species' responses to temperature and other habitat changes. Predictive capacity can be increased by understanding and incorporating these biological mechanisms from which range extensions emerge. Pursuit of key mechanisms spans a growing body of observational, experimental, and modelling efforts as well as theoretical frameworks. These domain-specific approaches have yielded considerable insights into aspects of range extensions and their mechanisms. However, limited integration across domains and inadequate ecological realism in general have hindered efforts to develop a mechanistic understanding of range extensions. At the typically 'cool', leading range edges pertinent to range extensions, both abiotic and biological conditions likely diverge from historical ranges. For example, water temperatures vary seasonally and over even small distances which virtually all mobile animals will select for non-randomly. Furthermore, range-extending individuals are likely to vary in behavioural and physiological responses to temperature due to plasticity and selection. Thus, research assuming average regional range-edge temperatures and population mean traits do not accurately reflect the conditions in which range extensions occur. However, contemporary range extension fronts provide a unique opportunity to investigate these conditions. Here, I integrated laboratory-based experimental and field-based observational approaches to examine the thermal physiological performance, movement behaviour, and field energetics of snapper Chrysophrys auratus (Forster 1801) at the extreme poleward front of the species' ongoing range extension into southeast Tasmania. Specifically, I i) identify the physiological performances, behaviours, and their interactions relevant to persistence at range edge conditions; ii) test hypotheses regarding the mechanisms underpinning range extensions at the range limit of snapper; iii) and address knowledge gaps for management of this important teleost predator and its emerging range-edge fishery. First, I experimentally compared swimming and aerobic metabolism performances of snapper after range-optimal (20 ¬∞C) and ambient range-edge winter temperature acclimation (10 ‚- 12 ¬∞C) with swim tunnel respirometry and establish baseline allometric scaling relationships for this key species. I tested and found little support for performance limitation arising from aerobic capacity insufficiency, a prominent hypothesis in the field. Moreover, I found that while range front acclimation curtails top end sustained swimming and metabolic performance, low speed swimming energetic efficiency increases, and maintenance costs declined. However, the degree to which these declines could pose a mechanism of ecological limitation depends on demands on these performances in the field. Next, I characterised the movements of 30 range front snapper with passive acoustic telemetry to determine the degree to which snapper are able to behaviourally thermoregulate and whether novel patterns of movement behaviour have emerged in this population. Range-front snapper are resident to small areas of key warm inshore habitat in summer which decline to unfavourably cold temperatures in winter. However, snapper exhibit a novel inshore-offshore seasonal migration strategy, selecting optimal temperatures across at least 45 km. I demonstrate aspects of snapper ecology of key management concern such as high seasonal site fidelity to predictable localised habitats, and I identify thermal limitation of nursery habitat as a potential mechanism of distributional limitation. I also present new methods to characterise daily patterns of telemetry data. Finally, I integrated lab and field approaches to characterise field acceleration and swimming energetics of ten snapper with accelerometer acoustic transmitters. Contrary to a commonly assumed monotonic relationship between field acceleration and temperature optimality, snapper acceleration peaked at moderate suboptimal temperatures during seasonal migration-related behaviour. Swim speeds and associated metabolic demands were predicted from transmitter acceleration with functions developed from experimental swim tunnel calibration of seven snapper implanted with transmitters. Swimming activity-related demands on aerobic metabolism in the field did not increase at the most sub-optimal temperatures, incongruent with the hypothesis that sub-optimal temperatures drive aerobic scope budgeting conflicts. Energetic efficiency did not appear to have a predominant effect in shaping volitional swim speeds. My work realises a long-proposed, integrated approach to range extensions reveals the complex, dynamic interplay of behaviour, performance, and environmental variability at root of climate-driven range extensions. I have demonstrated novel behaviour can cause extended range ecology to deviate from expected habitat relationships (i.e., those underpinning correlative distribution models), and by integrating experimental performance data, greatly increased the inference that can be drawn from field-based work on thermal limitation. For example, this approach has enabled the test of several hypotheses generated from theoretical frameworks of thermal limitation: aerobic scope does not appear to be a limiting factor at a species' distributional limit; In situ body acceleration did not serve as a suitable as a proxy for thermal performance because the relative use of performance wasn't greatest at the most physiologically favourable temperatures and instead varied with the demands of adaptive seasonal behaviours. These results provide the data needed for bioenergetic modelling that can provide the basis for forecasts of this range-extending species' demography and ecological interactions, critical for management of this global phenomenon. Finally, in situ investigations of range extensions are rare in large part due to logistical constraints. The success of this study illustrates the importance of engaging with stakeholders, in this case the Tasmanian recreational fishing community, enabling obtaining experimental animals, and facilitating the generation of hypotheses and effective design of field studies.

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