Energetics of habitat use in planktivorous coral reef fishes: does specialization confer sensitivity to changing environmental conditions?

Johansen, Jacob L. (2012) Energetics of habitat use in planktivorous coral reef fishes: does specialization confer sensitivity to changing environmental conditions? PhD thesis, James Cook University.

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Abstract

Tropical coral reefs are one of the most species rich ecosystems on earth. Highly diverse reef-associated fish assemblages are characterised by a high level of specialization in relation to environmental gradients, including temperature, water flow and turbidity. Species that are specialized on particular environments or resources can have an advantage over generalists in their ability to acquire and utilize resources. However, increasing human impacts on critical environmental parameters may be pushing specialized fish species beyond the levels to which they have evolved and can survive. Although coral reef ecosystems are regarded as thermally stable, ocean temperatures are expected to rise by about 3ºC within the next century due to global warming. In addition, flow conditions are expected to change due to shifting ocean currents and increasing storm intensities, and sedimentation and turbidity are expected to increase on many reefs due to rising coastal development, dredging and re-suspension during storms.

The overall goal of this thesis was to examine the performance of tropical coral reef fishes under present and future conditions of temperature, water flow and turbidity. It assesses how specialized reef fishes are for particular environmental conditions and how ability to access habitat and food resources is affected by environmental changes. The effects of temperature, flow and turbidity on the metabolism, swimming ability and foraging ability were assessed for 10 species of planktivorous coral reef damselfishes (Pomacentridae). Four objectives were examined using combinations of field and experimental protocols around Lizard Island, Northern Great Barrier Reef, Australia: 1) To determine the degree to which planktivorous coral reef fishes are physically and metabolically specialized for occupying particular habitat flow conditions and temperature regimes. 2) To measure how swimming performance, metabolic performance and optimum flow regime is influenced by the elevated temperature expected under climate change. 3) To determine the degree to which planktivorous coral reef fishes are specialized for foraging under particular habitat flow conditions, and their sensitivity to changes in flow. 4) To measure how foraging efficiency at different flow speeds is influenced by changes in visual range associated with changes in turbidity.

For each objective, water flow speeds were determined in-situ using automated flow meters purposely designed for this study, whilst field temperatures and cross-shelf turbidity levels were acquired from local weather stations and published water quality studies. Species distribution patterns, habitat use and foraging behaviours were determined in-situ by SCUBA divers. Metabolism and swimming performance was measured using flow tunnel respirometry at normal seasonal temperatures as well as 3ºC above present day maximum, and foraging performance on mobile and immobile planktonic prey was recorded experimentally in a flow chamber under different conditions of flow speeds and turbidity.

All study species were associated with different flow regimes and varied significantly in flow regime occupied. High flow species were found in reef habitats with flow speeds to ≤ 36 cms⁻¹, medium flow species to ≤ 21 cms⁻¹ and low flow species were confined to just ≤ 13 cms⁻¹. Flow conditions occupied were closely linked with temperature: All species showed strong thermal sensitivity and significant changes in metabolic performance and swimming ability between normal seasonal temperatures of 23ºC and 29ºC, and no species occupied habitats with flow speeds higher than their lowest recorded swimming speeds (at 23ºC or 29ºC). Standard metabolic rates were reduced by 41.4% overall when exposed to winter temperatures, reducing energetic needs for survival, while energy available for activity (aerobic factorial scope) increased by an average 38.4%, thereby increasing energetic resistance to adverse conditions. At the same time maximum swimming speeds using pectoral fins (i.e. the mode used for foraging) was reduced by an average 18.2%, limiting the ability to conduct ecological activities, gain energy and occupy habitats under winter conditions.

At elevated temperatures to 3ºC above present day maximum (32ºC), thermal impacts on performance increased even further: Standard metabolic rates increased by 20% on average, increasing energetic needs for survival. Aerobic scopes declined by up to ~65%, limiting energy available for overcoming challenges. Swimming speeds declined by up to ~50%, limiting the ability to gain the extra energy needed for survival, and some species lost so much swimming capacity that they were no longer able to overcome the flow speeds of the habitats they currently occupy.

Flow conditions occupied were also closely linked with foraging performance. All species were specialized for foraging on plankton under particular flow speeds, and foraging efficiency (i.e. proportion of successful attacks) rapidly declined above and below optima. Faster swimming species were up to 2.5-fold more efficient at foraging in high flow and could maintain above average foraging efficiency over a 2.8-fold wider range of flow speeds. Compared, slow swimming species showed below average foraging efficiency at flow speeds > 14cms⁻¹ and had low abundance in these habitats. However, several slow swimming species outperformed in currents < 10 cms⁻¹, foraging up to 1.3-fold more efficiently than faster swimming competitors. Accordingly, individual foraging efficiency was optimized for the same particular flow conditions as swimming performance and metabolic performance, and strongly correlated with field abundance.

Foraging efficiency was highly dependent on water clarity with turbidity levels as low as 4 and 8 NTU (nephelometric turbidity units) causing major reductions in efficiency. At 4 NTU there was up to ~58% loss of foraging efficiency in several species, with the greatest loss of efficiency seen at the higher flow speeds (i.e. > 15 cms⁻¹). At 8 NTU all species lost foraging efficiency. However, the loss grew up to ~70% for some species, and foraging efficiency rapidly reduced at flow speeds > 10 cms⁻¹. Mid- and outer-reef species showed significantly greater sensitivity to changes in turbidity than inner-reef species: In particular, there appeared to be a threshold limit of < 4 NTU for mid- to outer-reef species and < 8 NTU for inner-reef species above which foraging efficiency was significantly compromised. With turbidity in areas of frequent human activity often reaching levels well above 10 NTU, results provide a reasonable explanation for the lack of many planktivores fishes at inshore reefs and highlight sensitivity to turbidity similar to that seen in many corals.

In conclusion, it appears planktivorous coral reef damselfishes are specialized in relation to metabolic, swimming and foraging performance. The optimum environmental conditions for each species established in the laboratory closely matched the distribution patterns in the field. While physical and physiological specialization is often a superior evolutionary strategy for ecological performance in environmentally stable ecosystems, this study emphasises the compounding problems of such a strategy in an environment de-stabilized by anthropogenic disturbance. Given the level of specialization, performance is quickly lost following even minor changes in environmental conditions. The close links between performance and habitat use in these species mean that even minor changes in environmental condition may significantly impact on patterns of distribution and abundance. Consequently, planktivorous coral reef fishes may be more sensitive to environmental change than initially thought and unless adaptation is possible, significant problems may be expected for many of these tropical reef fishes in the years to come.

Item ID: 29099
Item Type: Thesis (PhD)
Keywords: global warming, elevated temperature, sedimentation, turbidity, coral reef fish, metabolism, energy, habitat use, swimming ability, feeding, water flow; environmental change, damselfishes, Pomacentridae, Lizard Island, Northern Great Barrier Reef, GBR, resilience
Additional Information:

Wenger, Amelia S., Johansen, Jacob L., and Jones, Geoffrey P. (2012) Increasing suspended sediment reduces foraging, growth and condition of a planktivorous damselfish. Journal of Experimental Marine Biology and Ecology, 428 . pp. 43-48.

Wenger, Amelia S., Johansen, J.L., and Jones, G.P. (2011) Suspended sediment impairs habitat choice and chemosensory discrimination in two coral reef fishes. Coral Reefs, 30 (4). pp. 879-887.

Chapter 3: Johansen, J.L., and Jones, G.P. (2011) Increasing ocean temperature reduces the metabolic performance and swimming ability of coral reef damselfishes. Global Change Biology, 17 (9). pp. 2971-2979.

Johansen, J.L., Vaknin, R., Steffensen, J.F., and Domenici, P. (2010) Kinematics and energetic benefits of schooling in the labriform fish, striped surfperch Embiotoca lateralis. Marine Ecology Progress Series, 420 . pp. 221-229.

Johansen, J.L., Bellwood, D.R., and Fulton, C.J. (2008) Do coral reef fishes exploit flow refuges in high-flow habitats. Marine Ecology Progress Series, 360 . pp. 219-226.

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Date Deposited: 05 Sep 2013 22:25
FoR Codes: 05 ENVIRONMENTAL SCIENCES > 0501 Ecological Applications > 050101 Ecological Impacts of Climate Change @ 33%
06 BIOLOGICAL SCIENCES > 0602 Ecology > 060203 Ecological Physiology @ 34%
06 BIOLOGICAL SCIENCES > 0602 Ecology > 060205 Marine and Estuarine Ecology (incl Marine Ichthyology) @ 33%
SEO Codes: 96 ENVIRONMENT > 9603 Climate and Climate Change > 960305 Ecosystem Adaptation to Climate Change @ 34%
96 ENVIRONMENT > 9605 Ecosystem Assessment and Management > 960507 Ecosystem Assessment and Management of Marine Environments @ 33%
96 ENVIRONMENT > 9608 Flora, Fauna and Biodiversity > 960808 Marine Flora, Fauna and Biodiversity @ 33%
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