The effects of suspended sediments on the physiology and performance of coral reef fishes

Hess, Sybille (2019) The effects of suspended sediments on the physiology and performance of coral reef fishes. PhD thesis, James Cook University.

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Declining water quality, in particular increasing suspended sediment concentrations, is a major factor causing the degradation of marine ecosystems. Anthropogenic activities such as coastal development, agriculture, cattle grazing, mining, dredging, and shipping have led to an increase in suspended sediments in coastal waters over the past decades. On coral reefs, suspended sediments have been linked to declines in species diversity and abundance of both benthic and reef fish communities. Changes in physiological performance have been hypothesized to represent a mechanism driving the observed declines in fish populations, but evidence for this is currently lacking. Moreover, the cumulative effects of suspended sediments and co-occurring environmental factors, such as elevated ocean temperatures caused by anthropogenic climate change and different water flow regimes, on coral reef fishes are unknown. This information is essential to understand responses of reef fish populations to current and future environmental conditions. The overall aim of this thesis was to examine the effects of suspended sediments, both in isolation and in combination with elevated water temperature and elevated water flow, on the physiology and performance of coral reef fishes.

Suspended sediments commonly induce changes in fish gill morphology that have been hypothesized to compromise gill function. In chapter two, the effects of suspended sediments on the gill morphology and aerobic performance of three damselfish species (Amphiprion melanopus, Amphiprion percula, and Acanthochromis polyacanthus) were examined. Following suspended sediment exposure (0, 45, 90, 135 or 180 mgL⁻¹), all three species exhibited reductions in the length of gill lamellae (a proxy for gill surface area) and/or reductions in gas diffusion distances. Yet, only A. melanopus exhibited changes in oxygen uptake rates, i.e., a decrease in maximum oxygen uptake rates (ṀO₂max) and an increase in resting oxygen uptake rates (ṀO₂rest). This resulted in a decreased aerobic scope in A. melanopus, indicative of a reduced capacity for aerobic activities, such as growth and locomotion. Results from this chapter indicate that A. melanopus and other species that exhibit a reduction in aerobic performance induced by suspended sediments may decline as reefs become more turbid. In contrast, species that are able to maintain aerobic performance despite changes in gill morphology, such as A. polyacanthus and A. percula, may be able to persist or even gain a competitive advantage on turbid reefs.

The ability to avoid and escape predators is key to the survival for juvenile coral reef fishes. If fish undergo changes in gill morphology that result in decreased aerobic scope, as observed in chapter two, suspended sediments may potentially compromise predator escape performance and influence anti-predator behaviours (i.e., behaviours that reduce the likelihood of encountering a predator, such as vigilance, changes in activity levels and sheltering). In chapter three, juvenile A. melanopus were exposed to suspended sediments (0 or 180 mgL⁻¹) for 7 days (prolonged exposure), and their predator escape performance and anti-predator behaviours were assessed in both clear water and turbid water (acute exposure). Prolonged exposure to suspended sediments led to an enhanced predator-escape performance, i.e., fish responded faster to a mechanical stimulus, had faster turning rates, and escaped at higher speeds and from further away than control fish. This was regardless of whether juvenile A. melanopus were being tested in clear or turbid water. In addition, acute exposure to suspended sediments led to an enhanced anti-predator behaviour, with fish moving less and staying closer to the wall of the experimental arena, regardless of prolonged exposure to suspended sediments. The observed increases in predator-escape performance and antipredator behaviours were likely strategies to compensate for an increased perceived predation risk in turbid water due to a reduced ability to detect approaching predators. While the observed changes are expected to increase juvenile survival, they are likely associated with costly non-consumptive effects that may compromise growth rates of juveniles living on turbid reefs.

Ocean temperatures in the tropics have already increased by 0.25 – 0.75°C since pre-industrial times and are predicted to continue increasing in the future. Coral reef fishes on inshore reefs are thus increasingly exposed to the combination of suspended sediments and elevated temperatures. In chapter four, A. polyacanthus, was reared under current day (29°C) or projected future temperature (32°C) for 4.5 weeks. During the final week of exposure, suspended sediments (0, 90, or 135 mgL⁻¹) were added to aquaria in a full factorial design to simulate a turbidity event. Following treatment exposure, gill morphology, aerobic performance, and predator escape performance of fish were examined. While exposure to 90 mgL⁻¹ suspended sediments had no effects on gill morphology, 135 mgL⁻¹ suspended sediments led to a reduction in gas diffusion distance relative to control fish (i.e., fish exposed to 29°C and 0 mgL⁻¹ suspended sediments). Elevated temperature led to reductions in both gas diffusion distance and filament thickness relative to control fish, which would generally be expected to enhance gas exchange efficiency at the gills. Suspended sediments and elevated temperature combined did not have any interactive effects on gill morphology. The changes in gill morphology were not reflected by the observed changes in oxygen uptake rates; elevated temperature in isolation led to reductions in ṀO₂max and ṀO₂rest, while suspended sediments had no effects on oxygen uptake rates in isolation. In fish exposed to both stressors combined, ṀO₂max were not different from control fish, resulting in an enhanced aerobic scope compared to control fish regardless of suspended sediment concentration. Predator escape performance was solely influenced by suspended sediments, with fish exhibiting enhanced fast starts following suspended sediment exposure (i.e., increased average and maximum escape speeds and greater escape distances at 90mgL⁻¹ and shorter response latency at 135mgL⁻¹ suspended sediments, respectively) compared to control fish. This response was likely driven by an increased perceived predation risk in turbid waters due to a compromised ability to detect predators. These surprising findings show that suspended sediments did not compound, but rather masked some of the negative effects of elevated temperature on juvenile A. polyacanthus. While this interaction between the two stressors may help A. polyacanthus to acclimate to future environmental conditions on inshore coral reefs, future studies will need to examine potential trade-offs with other important performance traits or functions.

Inshore reefs are often characterized by high tidal and current flows. Elevated water flow and an associated increase in swimming activity leads to an increased oxygen demand, which may potentially reduce the capacity of coral reef fishes to tolerate gill changes induced by suspended sediment exposure. In chapter five, juvenile five-lined cardinalfish, Cheilodipterus quinquelineatus, were exposed to three suspended sediments (0, 90, and 180 mgL⁻¹) and two water flow conditions (20.0 ± 5.0 cm s⁻¹ flow speed during 6 hours day⁻¹ or continuous < 2 cm s⁻¹ flow speed) in a full factorial design. Elevated water flow led to an increase in ṀO₂max and aerobic scope compared to control fish (i.e., fish exposed to < 2 cm s- 1 flow speed and 0 mgL⁻¹ suspended sediments), likely driven by increased swimming activity. However, ṀO₂max and aerobic scope in fish exposed to both stressors combined were not different from control fish. This absence of any increases in ṀO₂max in fish exposed to both stressors was not linked to changes in gill morphology, which were trait-specific and did not show a consistent pattern across treatments. Regardless of the underlying mechanism, however, an inability to enhance aerobic performance suggests that these fish likely also lack the capacity to enhance their swimming performance in response to elevated water flow conditions. As such, fish exposed to both stressors may have a reduced capacity to sustain elevated water flow velocities compared to fish exposed to elevated water flow in isolation. This may result in fish exposed to both stressors spending more time sheltering and less time foraging, which may negatively affect their growth and survival. A reduced capacity to enhance aerobic performance induced by suspended sediments may thus ultimately lead to a decline in abundance of C. quinquelineatus on turbid inshore reefs exposed to currents or high tidal flows or may limit the distribution of this species to more sheltered reefs.

This thesis has provided the most extensive evidence to date that suspended sediments affect the physiology and performance of coral reef fishes. While generally there was no close link between gill morphology and fish performance, one of four examined species in this thesis appeared to be sensitive to changes in gill morphology induced by suspended sediments, as evident by a reduction in aerobic performance. The effects of suspended sediments on predator escape performance was more consistent, with both examined species in this thesis enhancing their fast start performance in response to suspended sediment exposure. However, the impact of suspended sediments on fish performance was influenced by other environmental factors, with suspended sediments masking some of the negative effects of elevated temperature on aerobic performance, while elevated water flow conditions compounded the effects of suspended sediments on aerobic performance. Aerobic performance and predator escape performance are both linked to fitness and survival of juvenile coral reef fishes. As any factor influencing survival of coral reef fishes during this early life history stage can have important effects on adult populations, it is likely that the changes in fish performance reported in the present thesis represent an underlying mechanism contributing to changes in the distribution and abundance of species sensitive to suspended sediments on turbid inshore reefs.

Item ID: 60836
Item Type: Thesis (PhD)
Keywords: clownfish, coastal development, dredging, fish health, predator-prey interactions, sub-lethal effects, suspended solids, turbidity
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Copyright Information: Copyright © 2019 Sybille Hess.
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Two publications arising from this thesis are stored in ResearchOnline@JCU, at the time of processing. Please see the Related URLs field. The publications are:

Chapter 2: Hess, Sybille, Prescott, Leteisha J., Hoey, Andrew S., McMahon, Shannon A., Wenger, Amelia S., and Rummer, Jodie L. (2017) Species-specific impacts of suspended sediments on gill structure and function in coral reef fishes. Proceedings of the Royal Society of London Series B, Biological Sciences, 284 (1866). 20171279.

Chapter 3: Hess, Sybille, Allan, Bridie J.M., Hoey, Andrew S., Jarrold, Michael D., Wenger, Amelia S., and Rummer, Jodie L. (2019) Enhanced fast-start performance and anti-predator behaviour in a coral reef fish in response to suspended sediment exposure. Coral Reefs, 38. pp. 103-108.

Date Deposited: 05 Nov 2019 01:43
FoR Codes: 06 BIOLOGICAL SCIENCES > 0602 Ecology > 060203 Ecological Physiology @ 34%
06 BIOLOGICAL SCIENCES > 0602 Ecology > 060205 Marine and Estuarine Ecology (incl Marine Ichthyology) @ 33%
06 BIOLOGICAL SCIENCES > 0608 Zoology > 060801 Animal Behaviour @ 33%
SEO Codes: 97 EXPANDING KNOWLEDGE > 970106 Expanding Knowledge in the Biological Sciences @ 100%
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