Phenotypic drivers of hypoxia tolerance in a tropical diadromous fish (Lates calcarifer)

Collins, Geoffrey M. (2016) Phenotypic drivers of hypoxia tolerance in a tropical diadromous fish (Lates calcarifer). PhD thesis, James Cook University.

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Increasing coastal eutrophication and rising global temperatures are placing substantial pressure on wild fish populations. In the tropics, routinely high temperatures close to the equator have the combined effects of reducing the solubility of O₂ in water, increasing metabolic rates and enhancing thermal stratification. Such conditions may be particularly pronounced in lentic freshwater environments, and have led to a suite of adaptations by tropical fish species. Inter-specific diversity in hypoxia tolerance is widely acknowledged, however, many species exist not as a single, continuous population, but rather as multiple populations that may be distributed over broad latitudinal gradients, potentially spanning thousands of kilometres. In the absence of horizontal migration and genetic mixing between populations, and with differences in prevailing environmental conditions (such as temperature and dissolved O₂), such populations may become phenotypically and even genotypically divergent over time.

Performance of fish populations have been extensively investigated in the context of temperature, particularly with regard to projected temperature increases from climate change models. Despite the intrinsic relationship between temperature, O₂ and metabolism in fish, population differences in hypoxia tolerance have received little research attention to date. To address this knowledge gap, the hypoxia tolerance of geographically and genetically divergent populations of juvenile barramundi from across the distribution in northern Australia was assessed (Chapter 2). Juvenile barramundi were collected from five hatcheries across northern Australia, and were assessed for their resting O₂ consumption rate (ṀO₂) and critical O₂ level (O₂CRIT) using intermittent-flow respirometry. Measurements for all five populations were made at temperatures considered benign for this species across its distribution in Australia (26°C) and at temperatures that may be encountered during the pre-wet season (36°C). A posteriori comparisons revealed significant temperature effects for both resting ṀO₂ and O₂CRIT, but no conclusive evidence for population differences in either measure. The results from this study indicate a similar capacity for barramundi populations to regulate metabolism in response to hypoxia at typical and warm temperatures. The magnitude of temperature effects on O₂CRIT for barramundi was lower than for many other tropical and temperate fish species, indicating that barramundi retain a high capacity to regulate metabolism in hypoxic environments at high temperatures.

Over long time scales (tens to hundreds of thousands of years), populations that are genetically divergent may become either locally adapted to a specified range of conditions (if conditions are constrained within a narrow range), or they may retain a large degree of physiological plasticity (if the environments they inhabit are highly variable). Further, dissolved O₂ may display high spatial and temporal variability in coastal freshwater and estuarine systems that is often overlooked in empirical studies. To assess the contribution of population-of-origin or physiological plasticity to hypoxia tolerance, juvenile barramundi (one tropical and one sub-tropical population) were exposed to daily fluctuations in dissolved O₂ (>85% to <10% saturation) for 0 (control), 8 or 16 d (Chapter 3). Fish (separate cohorts) were then assessed for either resting ṀO₂ and O₂CRIT, or haematological parameters. No changes in any parameters were detected after 8 d, however after 16 d a reduction in O₂CRIT, and increases in both haematocrit and haemoglobin were observed. No population differences were detected for any measured parameter. This study demonstrates that barramundi populations are capable of acclimating to diel-cycling hypoxic conditions following repeated exposure, and that such changes are accompanied by improvements to blood-O₂ carrying capacity.

Inter-specific diversity in hypoxia tolerance of teleost fish is widely acknowledged, however the extent of intra-specific diversity in hypoxia tolerance is less well understood, due in part to the logistical and temporal constraints of measuring performance across a large number of individuals. Further, the temporal repeatability and hence the reliability of hypoxia tolerance measures have received virtually no attention in the broader scientific literature. To address these knowledge gaps, ~800 juvenile barramundi were first separated into hypoxia tolerance categories (Chapter 4) based on time to loss of equilibrium (LOE) tests: sensitive, intermediate and tolerant. Following a recovery period, fish were then assessed for growth performance, metabolic regulation under hypoxia (O₂CRIT) and repeatability of time to LOE. Further, the relationship between ṀO₂ and DO during O₂CRIT tests was assessed using non-linear regression and broken-stick regression techniques, which represents a novel approach to handling such a large empirical data set. Fish were reliably separated into different hypoxia tolerance categories, yet there were no significant category effects for any of the subsequently measured variables: growth rate, feed conversion ratio, standard metabolic rate or O₂CRIT. Non-linear regression was more robust in describing the relationship between ṀO₂ and DO than the more commonly used broken-stick regression method. Surprisingly, there was no significant relationship between two independent measures of hypoxia tolerance: time to LOE and O₂CRIT. The time to LOE test was broadly repeatable after ~100 d. This study highlights the extent of intra-specific diversity in hypoxia tolerance that can exist within fish populations.

All previous assessments of hypoxia tolerance were necessarily conducted on unfed individuals to eliminate the influence of specific dynamic action (SDA) on metabolic responses. In the wild, and on commercial fish farms, metabolism of fish may be elevated above resting levels due to feeding behaviour. Digestive responses are potentially influenced by dissolved O₂ conditions, however, few studies have assessed this possibility in tropical fish. Further, no studies have assessed the effect of hypoxia tolerance phenotype on digestive metabolic responses. Therefore, barramundi were separated into hypoxia tolerance phenotypes (sensitive or tolerant) based on time to LOE tests (Chapter 5). Fish were then fed a restricted ration (2.5% of their body-mass), before being assessed for ṀO₂ under normoxic (>85% saturation) and chronic hypoxic (~35% saturation) conditions. There was no effect of hypoxia tolerance phenotype for any measured parameter, and negligible differences in a range of digestive responses (SDA magnitude, SDA duration, SDA coefficient) under normoxic or hypoxic conditions. The results from this study suggest that barramundi are capable of maintaining maximal digestive capacity even when O₂ drops to 35% saturation.

The results from this thesis demonstrate that barramundi are extremely resilient to bouts of environmental hypoxia, and retain a strong tolerance to hypoxic conditions at extremely warm temperatures. The lack of population differences in hypoxia tolerance may be explained by the retention of a high degree of physiological plasticity as a strategy for responding to environmental hypoxia. The extent of phenotypic diversity in hypoxia tolerance is impressive, and the influence of this diversity on performance is still poorly understood. The homogeneity of performance between hypoxia tolerance phenotypes across two experiments and a number of measured parameters suggests that hypoxia tolerance is unrelated to several other performance metrics under either normoxic or hypoxic conditions. Future research should be directed at further exploring the relationship between phenotypic diversity in hypoxia tolerance and fitness, with an objective to more clearly elucidate the ecological consequences of trait variability.

Item ID: 48866
Item Type: Thesis (PhD)
Keywords: barramundi, climate change, critical oxygen saturation hypoxia, giant perch, hypoxia, hypoxia tolerance, Lates calcarifer, local adaptation, oxygen, tropical
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Publications arising from this thesis are available from the Related URLs field. The publications are:

Chapter 2: Collins, Geoffrey M., Clark, Timothy D., Rummer, Jodie L., and Carton, Alexander G. (2013) Hypoxia tolerance is conserved across genetically distinct sub-populations of an iconic, tropical Australian teleost (Lates calcarifer). Conservation Physiology, 1 (1). pp. 1-9.

Chapter 3: Collins, Geoffrey Mark, Clark, Timothy Darren, and Carton, Alexander Guy (2016) Physiological plasticity v. inter-population variability: understanding drivers of hypoxia tolerance in a tropical estuarine fish. Marine and Freshwater Research, 67 (10). pp. 1575-1582.

Date Deposited: 09 May 2017 05:00
FoR Codes: 06 BIOLOGICAL SCIENCES > 0602 Ecology > 060203 Ecological Physiology @ 80%
07 AGRICULTURAL AND VETERINARY SCIENCES > 0704 Fisheries Sciences > 070405 Fish Physiology and Genetics @ 20%
SEO Codes: 97 EXPANDING KNOWLEDGE > 970106 Expanding Knowledge in the Biological Sciences @ 70%
83 ANIMAL PRODUCTION AND ANIMAL PRIMARY PRODUCTS > 8301 Fisheries - Aquaculture > 830102 Aquaculture Fin Fish (excl. Tuna) @ 20%
96 ENVIRONMENT > 9603 Climate and Climate Change > 960305 Ecosystem Adaptation to Climate Change @ 10%
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