Visual Biology of Hawaiian Coral Reef Fishes. III. Environmental Light and an Integrated Approach to the Ecology of Reef Fish Vision

In the previous two papers in this three-part series, we have examined visual pigments, ocular media transmission, and colors of the coral reef fish of Hawaii. This paper first details aspects of the light field and background colors at the microhabitat level on Hawaiian reefs and does so from the perspective and scale of fish living on the reef. Second, information from all three papers is combined in an attempt to examine trends in the visual ecology of reef inhabitants. Our goal is to begin to see fish the way they appear to other fish. Observations resulting from the combination of results in all three papers include the following. Yellow and blue colors on their own are strikingly well matched to backgrounds on the reef such as coral and bodies of horizontally viewed water. These colors, therefore, depending on context, may be important in camouflage as well as conspicuousness. The spectral characteristics of fish colors are correlated to the known spectral sensitivities in reef fish single cones and are tuned for maximum signal reliability when viewed against known backgrounds. The optimal positions of spectral sensitivity in a modeled dichromatic visual system are generally close to the sensitivities known for reef fish. Models also predict that both UV-sensitive and red-sensitive cone types are advantageous for a variety of tasks. UV-sensitive cones are known in some reef fish, red-sensitive cones have yet to be found. Labroid colors, which appear green or blue to us, may he matched to the far-red component of chlorophyll reflectance for camouflage. Red cave/hole dwelling reef fish are relatively poorly matched to the background they are often viewed against but this may be visually irrelevant. The model predicts that the task of distinguishing green algae from coral is optimized with a relatively long wavelength visual pigment pair. Herbivorous grazers whose visual pigments are known possess the longest sensitivities so far found. Labroid complex colors are highly contrasting complementary colors close up but combine, because of the spatial addition, which results from low visual resolution, at distance, to match background water colors remarkably well. Therefore, they are effective for simultaneous communication and camouflage.

Global trajectories of the long-term decline of coral reef ecosystems

Degradation of coral reef ecosystems began centuries ago, but there is no global summary of the magnitude of change. We compiled records, extending back thousands of years, of the status and trends of seven major guilds of carnivores, herbivores, and architectural species from 14 regions. Large animals declined before small animals and architectural species, and Atlantic reefs declined before reefs in the Red Sea and Australia, but the trajectories of decline were markedly similar worldwide. All reefs were substantially degraded long before outbreaks of coral disease and bleaching. Regardless of these new threats, reefs will not survive without immediate protection from human exploitation over large spatial scales.

Closely related Symbiodinium spp. differ in relative dominance in coral reef host communities across environmental, latitudinal and biogeographic gradients

The diversity and community structures of symbiotic dinoflagellates are described from reef invertebrates in southern and central provinces of the Great Barrier Reef (GBR), Australia, and Zamami Island, Okinawa, Japan. The symbiont assemblages from region to region were dominated by Clade C Symbiodinium spp. and consisted of numerous host-specific and/or rare types (specialists), and several types common to many hosts (generalists). Prevalence in the host community among certain host-generalist symbionts differed between inshore and offshore environments, across latitudinal (central versus southern GBR) gradients, and over wide geographic ranges (GBR versus Okinawa). One particular symbiont (C3h) from the GBR had a dramatic shift in dominance. Its prevalence ranged from being extremely rare, or absent on high-latitude reefs to dominating the scleractinian diversity on a mid-latitude inshore reef. These changes occurred among coral fauna whose larvae must acquire symbionts from environmental sources (horizontal symbiont acquisition). Such differences did not occur among 'vertical transmitters' such as Porites spp., Montipora spp. and pocilloporids (corals that directly transmit symbionts to their offspring) or among those hosts displaying 'horizontal acquisition', but that associate with specific symbionts. Most host-specialized types were found to be characteristic of a particular geographic region (i.e. Okinawa versus Central GBR versus Southern GBR). The mode of symbiont acquisition may play an important role in how symbiont composition may shift in west Pacific host communities in response to climate change. There is no indication that recent episodes of mass bleaching have provoked changes in host-symbiont combinations from the central GBR.

A Century of Change in Coral Reef Status in Southeast and Central Pacific: Polynesia Mana Node, Cook Islands, French Polynesia, Kiribati, Niue, Tokelau, Tonga, Wallis and Futuna

The Polynesia Mana Node of the southeast and central Pacific contains 7 independent or autonomous countries or territories with only 6,000 km2 of land on 347 islands, but surrounded by 12 million km2 of EEZ. These seas contain 13,000 km2 of coral reefs as the main natural ecosystem providing food resources and opportunities for development, especially for tourism and pearl culture for 500,000 inhabitants. During the 19th and first half of the 20th centuries, there was major exploitation by the colonial powers of mother-of-pearl oysters for the button industry, as well as guano, sandalwood and trepang. The Polynesian people were largely involved in a subsistence economy and all coral reefs and lagoons were healthy. During the last two decades of the 20th, all countries experienced rapid development and urbanization, rising populations, and some increased agriculture. These developments were limited to a few islands of each country (i.e. 15 islands amongst the 347) with resulting degradation of the coral reefs around these sites. The other islands remained mostly uninhabited and pristine, and continued with a subsistence economy. Generally, there was more damage to the coral reefs through natural events such as cyclones and coral bleaching, than by human activities. There is however, an urgent need to combat the threats on some islands from increased sedimentation, over-fishing, dredging and nutrient pollution.

The effects of copper on the microbial community of a coral reef sponge

Marine sponges often harbour communities of symbiotic microorganisms that fulfil necessary functions for the well-being of their hosts. Microbial communities associated with the sponge Rhopaloeides odorabile were used as bioindicators far sublethal cupric ion (Cu2+) stress. A combined strategy incorporating molecular, cultivation and electron microscopy techniques was adopted to monitor changes in microbial diversity. The total density of sponge-associated bacteria and counts of the predominant cultivated symbiont (alpha -proteobacterium strain NW001) were significantly reduced in response to Cu2+ concentrations of 1.7 mug l(-1) and above after 14 days of exposure. The number of operational taxonomic units (OTUs) detected by restriction fragment length polymorphism (RFLP) decreased by 64% in sponges exposed to 223 mug l(-1) Cu2+ for 48 h and by 46% in sponges exposed to 19.4 mug l(-1) Cu2+ for 14 days. Electron microscopy was used to identify 17 predominant bacterial morphotypes, composing 47% of the total observed cells in control sponges. A reduction In the proportion of these morphotypes to 25% of observed cells was evident in sponges exposed to a Cu2+ concentration of 19.4 mug l(-1). Although the abundance of most morphotypes decreased under Cu2+ stress, three morphotypes were not reduced in numbers and a single morphotype actually increased in abundance. Bacterial numbers, as detected using fluorescence in situ hybridization (FISH), decreased significantly after 48 h exposure to 19.4 mug l(-1) Cu2+. Archaea, which are normally prolific in R. odorabile, were not detected after exposure to a Cu2+ concentration of 19.4 mug l(-1) for 14 days, indicating that many of the microorganisms associated with R. odorabile are sensitive to free copper. Sponges exposed to a Cu2+ concentration of 223 mug l(-1) became highly necrosed after 48 h and accumulated 142 +/- 18 mg kg(-1) copper, whereas sponges exposed to 19.4 mug l(-1) Cu2+ accumulated 306 +/- 15 mg kg(-1) copper after 14 days without apoptosis or mortality. Not only do sponges have potential for monitoring elevated concentrations of heavy metals but also examining changes in their microbial symbionts is a novel and sensitive bioindicator for the assessment of pollution on important microbial communities.

Cleaner fish Labroides dimidiatus reduce 'temporary" parasitic corallanid isopods on the coral reef fish Hemigymnus melapterus

To determine if cleaners affect 'temporary' parasitic corallanid isopods (Argathona macronema) on fish, we used caged fish Hemigymnus meldpterus (Labridae) on 5 patch reefs on Lizard Island, Great Barrier Reef, and removed all cleaner fish Labroides dimidiatus (Labridae) from 3 of the reefs, In a short-term experiment, fish were sampled after 12 or 24 h, at dawn and sunset respectively, and in a long-term experiment they were sampled after 12 d at sunset. Isopod prevalence, abundance and size were measured. In the short-term experiment, on reefs without cleaners the prevalence of A. macronema was higher after 24 h than after 12 h while on reefs with cleaners, prevalence was low at all times, Although the abundance of A, macronema did not vary after 12 and 24 h, when combined over the 24 h, the effect of cleaners was significant with only 2 % of all the A. macronema found on reefs with cleaners. Cleaners had no effect on the size frequency distribution of A. macronema in the short-term experiment, most likely because fish had so few isopods on reef with cleaners. In the longer-term experiment, the effects of cleaners on isopod prevalence and abundance were less clear. Their effect on isopod size was, however, significant with smaller parasites on reefs without cleaners. The reduction of isopod prevalence and abundance by cleaner fish over a period of hours may explain why these A, macronema are rare on wild fish. Our findings support the idea that cleaning is beneficial to clients and has important implications for the control of parasites of fish farmed in cages,

Visual Biology of Hawaiian Coral Reef Fishes. I. Ocular Transmission and Visual Pigments

The visual biology of Hawaiian reef fishes was explored by examining their eyes for spectral sensitivity of their visual pigments and for transmission of light through the ocular media to the retina. The spectral absorption curves for the visual pigments of 38 species of Hawaiian fish were recorded using microspectrophotometry. The peak absorption wavelength (lambda(max)) of the rods varied from 477-502 nm and the lambda(max) of individual species conformed closely to values for the same species previously reported using a whole retina extraction procedure. The visual pigments of single cone photoreceptors were categorized, dependent on their lambda(max)-values, as ultraviolet (347-376 nm), violet (398-431 nm) or blue (439-498 nm) sensitive cones. Eight species possessed ultraviolet-sensitive cones and 14 species violet-sensitive cones. Thus, 47% of the species examined displayed photosensitivity to the short-wavelength region of the spectrum. Both identical and nonidentical paired and double cones were found with blue sensitivity or green absorption peaks (> 500 nm). Spectrophotometry of the lens, cornea, and humors for 195 species from 49 families found that the spectral composition of the light transmitted to the retina was most often limited by the lens (73% of species examined). Except for two unusual species with humor-limited eyes, Acanthocybium solandri (Scombridae) and the priacanthid fish, Heteropriacanthus cruentatus, the remainder had corneal-limited eyes. The wavelength at which 50% of the light was blocked (T50) was classified according to a system modified from Douglas and McGuigan (1989) as Type I, T50 < = 355 nm, (32 species); Type IIa, 355 < T50 < = 380 nm (30 species); Type IIb, 380 < T50 405 nm (84 species). Possession of UV-transmitting ocular media follows both taxonomic and functional lines and, if the ecology of the species is considered, is correlated with the short-wavelength visual pigments found in the species. Three types of short-wavelength vision in fishes are hypothesized: UV-sensitive, UV-specialized, and violet-specialized. UV-sensitive eyes lack UV blockers (Type I and IIa) and can sense UV light with the secondary absorption peak or beta peak of their longer wavelength visual pigments but do not possess specialized UV receptor cells and, therefore, probably lack UV hue discrimination. UV-specialized eyes allow transmission of UV light to the retina (Type I and IIa) and also possess UV-sensitive cone receptors with peak absorption between 300 and 400 nm. Given the appropriate perceptual mechanisms, these species could possess true UV-color vision and hue discrimination. Violet-specialized eyes extend into Type IIb eyes and possess violet-sensitive cone cells. UV-sensitive eyes are found throughout the fishes from at least two species of sharks to modern bony fishes. Eyes with specialized short-wavelength sensitivity are common in tropical reef fishes and must be taken into consideration when performing research involving the visual perception systems of these fishes. Because most glass and plastics are UV-opaque, great care must be taken to ensure that aquarium dividers, specimen holding containers, etc., are UV-transparent or at least to report the types of materials in use.

Volunteer-based coral reef monitoring: reliability of data, environmental education and implications for conservation

Coral reefs are the most biodiverse ecosystems of the ocean and they provide notable ecosystem services. Nowadays, they are facing a number of local anthropogenic threats and environmental change is threatening their survivorship on a global scale. Large-scale monitoring is necessary to understand environmental changes and to perform useful conservation measurements. Governmental agencies are often underfunded and are not able of sustain the necessary spatial and temporal large-scale monitoring. To overcome the economic constrains, in some cases scientists can engage volunteers in environmental monitoring. Citizen Science enables the collection and analysis of scientific data at larger spatial and temporal scales than otherwise possible, addressing issues that are otherwise logistically or financially unfeasible. “STE: Scuba Tourism for the Environment” was a volunteer-based Red Sea coral reef biodiversity monitoring program. SCUBA divers and snorkelers were involved in the collection of data for 72 taxa, by completing survey questionnaires after their dives. In my thesis, I evaluated the reliability of the data collected by volunteers, comparing their questionnaires with those completed by professional scientists. Validation trials showed a sufficient level of reliability, indicating that non-specialists performed similarly to conservation volunteer divers on accurate transects. Using the data collected by volunteers, I developed a biodiversity index that revealed spatial trends across surveyed areas. The project results provided important feedbacks to the local authorities on the current health status of Red Sea coral reefs and on the effectiveness of the environmental management. I also analysed the spatial and temporal distribution of each surveyed taxa, identifying abundance trends related with anthropogenic impacts. Finally, I evaluated the effectiveness of the project to increase the environmental education of volunteers and showed that the participation in STEproject significantly increased both the knowledge on coral reef biology and ecology and the awareness of human behavioural impacts on the environment.

Classification of coral reef types in Torres Strait (GIS files in zip-archive 319 kB)

Coral reefs represent major accumulations of calcium carbonate (CaCO3). The particularly labyrinthine network of reefs in Torres Strait, north of the Great Barrier Reef (GBR), has been examined in order to estimate their gross CaCO3 productivity. The approach involved a two-step procedure, first characterising and classifying the morphology of reefs based on a classification scheme widely employed on the GBR and then estimating gross CaCO3 productivity rates across the region using a regional census-based approach. This was undertaken by independently verifying published rates of coral reef community gross production for use in Torres Strait, based on site-specific ecological and morphological data. A total of 606 reef platforms were mapped and classified using classification trees. Despite the complexity of the maze of reefs in Torres Strait, there are broad morphological similarities with reefs in the GBR. The spatial distribution and dimensions of reef types across both regions are underpinned by similar geological processes, sea-level history in the Holocene and exposure to the same wind/wave energetic regime, resulting in comparable geomorphic zonation. However, the presence of strong tidal currents flowing through Torres Strait and the relatively shallow and narrow dimensions of the shelf exert a control on local morphology and spatial distribution of the reef platforms. A total amount of 8.7 million tonnes of CaCO3 per year, at an average rate of 3.7 kg CaCO3 m-2 yr-1 (G), were estimated for the studied area. Extrapolated production rates based on detailed and regional census-based approaches for geomorphic zones across Torres Strait were comparable to those reported elsewhere, particularly values for the GBR based on alkalinity-reduction methods. However, differences in mapping methodologies and the impact of reduced calcification due to global trends in coral reef ecological decline and changing oceanic physical conditions warrant further research. The novel method proposed in this study to characterise the geomorphology of reef types based on classification trees provides an objective and repeatable data-driven approach that combined with regional census-based approaches has the potential to be adapted and transferred to different coral reef regions, depicting a more accurate picture of interactions between reef ecology and geomorphology.