Hypoxia and thermal tolerance in New Zealand triplefin fishes

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dc.contributor.advisor Herbert, N en
dc.contributor.advisor Hickey, A en
dc.contributor.author McArley, Tristan en
dc.date.accessioned 2019-11-05T00:18:39Z en
dc.date.issued 2019 en
dc.identifier.uri http://hdl.handle.net/2292/48835 en
dc.description.abstract Temperature and the availability of oxygen (O₂) each have a profound influence on the metabolism of fish and play a key role in shaping the distribution and abundance of species. All fishes are exposed to at least some fluctuation in each of these environmental parameters, but few species are subjected to the extreme acute changes in O₂ availability and temperature faced by fishes inhabiting intertidal rock pools. This thesis, with a focus on intertidal species, explores the physiological responses of New Zealand triplefin fishes to variability in O₂ availability (hypoxia and hyperoxia) and increased temperature (acute and chronic exposure). Decreased O₂ availability (hypoxia) is common in rock pools and challenges the aerobic metabolism of fishes living in these habitats. In Chapter 2, the critical O₂ tension (Pcrit) - a measure of hypoxia tolerance - was compared between two intertidal and two subtidal triplefin fishes endemic to New Zealand. The intertidal species had a lower Pcrit than the subtidal species indicating adaptations to meet O₂ demands of maintenance metabolism at lower O₂ tensions. While maintenance metabolism (measured as standard metabolic rate; SMR) did not show a major functional difference between species, the intertidal species had higher maximal rates of O₂ consumption (ṀO₂,max) and higher aerobic metabolic scope (MS). The high O₂ extractive capacity of the intertidal species was associated with increased blood O₂ carrying capacity (i.e. higher Hb concentration); additionally, intertidal species had higher mass-specific gill surface area and thinner gill secondary lamellae that collectively conveyed a higher capacity for O₂ flux across the gills. The specialist intertidal species also had higher glycogen stores in both white muscle and brain tissues, suggesting greater potential to generate ATP anaerobically and survive in rock pools with O₂ tensions less than Pcrit. Overall, Chapter 2 shows that the superior hypoxia tolerance of intertidal New Zealand triplefin species is not linked to a minimisation of basal metabolic demand (SMR), but is instead associated with a maximisation in the O₂ extractive capacity of the cardiorespiratory system (i.e. ṀO₂,max, MS, Hb concentration and gill O₂ flux) and glycolytic tissue stores. Environmental stressors often occur simultaneously or in quick succession, but how animals respond to multiple stressors is not well studied or understood. Acute heat shock has previously been shown to improve subsequent low O₂ (hypoxia) tolerance in an intertidal fish species, a process known as cross-tolerance, but it is not known whether this is a widespread phenomenon. As acute heat and hypoxic stress tend to occur out of phase in intertidal rock pools, Chapter 3 specifically examined whether a New Zealand rock pool specialist, the triplefin fish Bellapiscis medius, exhibits hypoxic cross-tolerance (i.e. longer time to loss of equilibrium (LOE) and lower critical O₂ saturation (Scrit) under hypoxia) after recovering from an ecologically relevant heat shock. Non-heat shock controls had a median time to loss of equilibrium (LOE50) of 54.4 min under severe hypoxia (7% of air saturation) and a Scrit of 15.8% air saturation. However, contrary to expectations, treatments that received an initial 8 or 10°C heat shock showed a significantly shorter LOE50 in hypoxia (+8°C = 41.5 min; +10°C = 28.7 min) combined with no significant change in Scrit (+8°C =17.0% air saturation; +10°C =18.3% of air saturation). No evidence of heat shock induced cross-tolerance in B. medius was, therefore, found because acute exposure to peak temperatures resulted in an impaired tolerance to hypoxia. This is cause-for-concern because climate change will increase the frequency and intensity of heat shock events in rock pools rendering B. medius less able to cope with multiple stressors across successive low tides. Daytime low tides that lead to high temperature events in stranded rock pools often co-occur with algal mediated hyperoxia as a result of strong solar radiation. Recent evidence shows MS can be expanded under hyperoxia in fish but so far this possibility has not been examined in intertidal species despite being an ecologically relevant scenario. Furthermore, it is unknown whether hyperoxia increases the upper thermal tolerance limits of intertidal fish and their ability to withstand extreme high temperature events. Therefore, Chapter 4 measured the metabolic response (mass-specific rate of oxygen consumption [ṀO₂]) to thermal ramping (21-29°C) and the upper thermal tolerance limit (CTmax) of two intertidal triplefin fishes (B. medius and Forsterygion lapillum) under hyperoxia and normoxia. Hyperoxia increased ṀO₂,max and MS of each species at ambient temperature (21°C) and also after thermal ramping to elevated temperatures such as those observed in rock pools (29°C). While hyperoxia did not provide a biologically meaningful increase in upper thermal tolerance of either species (>31°C under all conditions), the observed expansion of MS at 29°C under hyperoxia could potentially benefit the aerobic performance, hence the growth and feeding potential etc., of intertidal fish at non-critical temperatures. That hyperoxia does not increase upper thermal tolerance in a meaningful way is cause for concern, as climate change is expected to drive more extreme rock pool temperatures in the future; this could present a major challenge for these species. Intertidal fish species face gradual chronic changes in temperature and greater extremes of acute thermal exposure through climate induced warming. As sea temperatures rise, it has been proposed that whole animal performance will be impaired through oxygen and capacity limited thermal tolerance (OCLTT, reduced aerobic metabolic scope-MS) and, on acute exposure to high temperatures, thermal safety margins may be reduced due to constrained acclimation capacity of upper thermal limits. Using the New Zealand triplefin fish (F. lapillum), Chapter 5 addressed how performance in terms of growth and metabolism (MS) and upper thermal tolerance limits would be affected by chronic exposure to elevated temperature. Growth was measured in fish acclimated (12 weeks) to present and predicted future temperatures, and metabolic rates were then determined in fish at acclimation temperatures and with acute thermal ramping. In agreement with the OCLTT hypothesis chronic exposure to elevated temperature significantly reduced growth performance and MS. However, despite the prospect of impaired growth performance under warmer future summertime conditions, an annual growth model revealed that elevated temperatures may only shift the timing of high growth potential and not the overall annual growth rate. While the upper thermal tolerance (i.e. critical thermal maxima) increased with exposure to warmer temperatures and was associated with depressed metabolic rates during acute thermal ramping, upper thermal tolerance did not differ between present and predicted future summertime temperatures. This suggests that warming may progressively decrease thermal safety margins for hardy generalist species and limit the available habitat range of intertidal populations. en
dc.publisher ResearchSpace@Auckland en
dc.relation.ispartof PhD Thesis - University of Auckland en
dc.relation.isreferencedby UoA99265185914102091 en
dc.rights Items in ResearchSpace are protected by copyright, with all rights reserved, unless otherwise indicated. Previously published items are made available in accordance with the copyright policy of the publisher. en
dc.rights.uri https://researchspace.auckland.ac.nz/docs/uoa-docs/rights.htm en
dc.rights.uri http://creativecommons.org/licenses/by-nc-sa/3.0/nz/ en
dc.title Hypoxia and thermal tolerance in New Zealand triplefin fishes en
dc.type Thesis en
thesis.degree.discipline Marine Science en
thesis.degree.grantor The University of Auckland en
thesis.degree.level Doctoral en
thesis.degree.name PhD en
dc.rights.holder Copyright: The author en
dc.rights.accessrights http://purl.org/eprint/accessRights/OpenAccess en
pubs.elements-id 785157 en
pubs.org-id Science en
pubs.org-id Marine Science en
pubs.record-created-at-source-date 2019-11-05 en

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