Visual behaviour in fish: the influence of metabolic stress and the choroid rete mirabile

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dc.contributor.advisor Wells, Rufus en Herbert, Neill A. en 2007-07-21T09:29:51Z en 2007-07-21T09:29:51Z en 2002 en
dc.identifier THESIS 02-177 en
dc.identifier.citation Thesis (PhD--Biological Sciences)--University of Auckland, 2002 en
dc.identifier.uri en
dc.description Full text is available to authenticated members of The University of Auckland only. en
dc.description.abstract This thesis addresses aspects of the physiology, behaviour and anatomy of fishes in order to test the hypotheses that (i) visual performance is influenced by metabolic stress and the development of an oxygen concentrating apparatus in the eye (i.e. the choroid rete mirabile) and that (ii) visually-mediated behaviour is important in offsetting the metabolic costs of hypoxic stress and predatory challenge in an air-breathing fish. It is hypothesised that the transport of oxygen to the retinal cells, and hence the visual performance, of fish with Root effect haemoglobins is impaired by strenuous exercise due to a proton load that drastically reduces arterial haemoglobin-oxygen affinity. Routinely active tropical reef fishes have enhanced oxygen transport and anaerobic (i.e. blood lactate loading) potentials relative to inactive species. Surprisingly, the development of the choroid rete mirabile is directly correlated with post-exercise lactate loads rather than with the magnitude of the Root effect, and suggests that increased retial development is adaptive for fish with high anaerobic potentials. The hypothesis that visual acuity (i.e. the ability to resolve fine detail) is reduced by strenuous exercise was tested in the tropical striped snapper, Lutjanus carponotatus, using the optomotor response. Moderate blood lactate loads (2 mmol l-1 blood lactate) and red cell swelling responses were induced by exercise, but visual acuity thresholds (180 min of arc) were maintained. A moderate metabolic disturbance does not therefore appear to be a liability for the visual performance of a tropical fish in possession of Root effect haemoglobins. It is further hypothesised that the visual acuity of rainbow trout, Oncorhynchus mykiss, will be impaired by strenuous exercise as a result of metabolic stress (blood lactacidosis) that activates the Root effect and limits the oxygen carrying capacity of blood flowing to the eye. Strenuous exercise induced a high metabolic acidosis (8.0 mmol l-1 blood lactate) and a significant red cell swelling response but no change in the visual acuity threshold (120 min of arc) was observed. Beta-adrenergic blockade (propranolol) abolished post-exercise red cell swelling but visual acuity thresholds were still maintained at 120 min of arc despite a significant blood lactate load. The choroid rete mirabile of the trout is extremely well developed (rete area: eye volume=6 mm-1) and may maintain acuity thresholds by ensuring a relatively direct supply of oxygen to the central regions of the avascular retina. Exercised β-blocked fish exhibited an enhanced optomotor response at 240 - 300 min of arc. Assuming that these responses were the result of "tunnel vision", adrenergic regulation of red cell function may preserve a high ocular PO2 gradient that satisfies the oxygen demand of remote retinal cells. The hypothesis that visual acuity is influenced by the presence of a choroid rete mirabile and by strenuous exercise was tested behaviourally using the optomotor response in two nototheniid species from Antarctica. Although both species possess Root effect haemoglobins, the rete is absent in Pagothenia borchgrevinki, an active cryopelagic zooplanktivore, and poorly developed in Trematomus bernaccii, a sluggish benthic nototheniid. The optomotor response of T. bernacchii was positively influenced by subtended angle but no effect of exercise was detected. In contrast, P. borchgrevinki did not respond to any subtended angle (0-600 min of arc) either pre- or post-exercise. The optomotor response of T. bernacchii may therefore have been facilitated by the presence of the choroid rete. The hypothesis that the development of the choroid rete in fish influences temporal resolution (i.e. the detection of movement or flicker) was tested by examining the optomotor response of representative species from Antarctic, temperate and tropical environments. Although interspecifically variable, temporal resolution was linked with water temperature but not with the physiological potential for activity of each species. The development of the choroid rete mirabile was indeed strongly correlated with temporal resolution in P. borchgrevinki and T. bernacchii, O. mykiss and L. carponotatus, and may be determined by the metabolic demand of diverse retinal topographies. Interestingly, the retinal topography of the Antarctic species is comparable and specifically indicates that an increase in ocular PO2 may have enhanced the visual performance of T. bernacchii, which possess a rete. Comparison of fish from the three environments showed a strong correlation between the development of the choroid rete and post-exercise blood lactate concentrations. An increasingly well-developed choroid rete appears to be associated with vision dependence in fish that possess high anaerobic potentials for burst activity. Air-breathing frequency in the blue gourami, Trichogaster trichopterus, is expected to increase when aquatic oxygen tensions decline. With the visual threat of predation, however, this behaviour must be modified at a potential cost to aerobic metabolism. We therefore tested the hypothesis that metabolic responses to predatory challenge and aquatic hypoxia are subject to behavioural modulation. Physiological characteristics of the blood oxygen transport system and muscle metabolism indicate a high dependence on aerobic pathways. Haemoglobin concentration and haematocrit were modest and the blood oxygen affinity (P50=17.4 mmHg at pH 7.4 and 28°C) and its sensitivity to pH (Bohr factor, Φ=-0.34) favour oxygen unloading at relatively high PO2. The intracellular buffering capacity (44.0 slykes) and LDH activity (154.3 i.u. g-1) do not support exceptional anaerobic capabilities. Computer generated visual stimuli consistently reduced air-breathing frequency at 150, 50 and 25 mmHg PO2. Bi-directional rates of spontaneous activity were similarly reduced. The metabolic cost of this behaviour was estimated and positively correlated with aquatic PO2 but not with visual stimulation, thus indicating down-regulation of spontaneous activity rather than breath-holding behaviour. Neither PO2 nor visual stimulation resulted in significant change to muscle lactate and ATP concentrations and confirm that aerobic breath-hold limits were maintained following behavioural modulation of metabolic demands. en
dc.language.iso en en
dc.publisher ResearchSpace@Auckland en
dc.relation.ispartof PhD Thesis - University of Auckland en
dc.relation.isreferencedby UoA99101773414002091 en
dc.rights Restricted Item. Available to authenticated members of The University of Auckland. en
dc.rights Items in ResearchSpace are protected by copyright, with all rights reserved, unless otherwise indicated. en
dc.rights.uri en
dc.title Visual behaviour in fish: the influence of metabolic stress and the choroid rete mirabile en
dc.type Thesis en Biological Sciences en The University of Auckland en Doctoral en PhD en
dc.subject.marsden Fields of Research::270000 Biological Sciences::270700 Ecology and Evolution::270702 Marine and estuarine ecology (incl. marine ichthyology) en
dc.rights.holder Copyright: The author en

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