James W. Porter

Reef Corals: Mutualistic Symbioses Adapted to Nutrient-Poor Environments

Coral atoll communities are of special interest to marine biologists since they flourish in tropical waters characterized by low productivity (cf. Stoddart 1969). One of the aims of research in coral reef biology is to discern and describe quantitatively the adaptations that permit reef communities to exploit a marginally suitable habitat. Vital to this aim is an understanding of the nutrition of corals themselves since these lime-secreting cnidarians are the dominant life forms of many reefs and one of the principal reef builders. The general topic of coral nutrition has been reviewed recently (Muscatine 1973, Taylor 1973a) and serves as a convenient point of departure. The present discussion considers the potential nutritional capabilities of corals as mutualistic symbioses and the extent to which specific organismic and ecological manifestations of these capabilities have been described and quantified.

The etiology of white pox, a lethal disease of the Caribbean elkhorn coral, Acropora palmata

Populations of the shallow-water Caribbean elkhorn coral, Acropora palmata, are being decimated by white pox disease, with losses of living cover in the Florida Keys typically in excess of 70%. The rate of tissue loss is rapid, averaging 2.5 cm2⋅day−1, and is greatest during periods of seasonally elevated temperature. In Florida, the spread of white pox fits the contagion model, with nearest neighbors most susceptible to infection. In this report, we identify a common fecal enterobacterium, Serratia marcescens, as the causal agent of white pox. This is the first time, to our knowledge, that a bacterial species associated with the human gut has been shown to be a marine invertebrate pathogen.

Fate of Photosynthetic Fixed Carbon in Light- and Shade-Adapted Colonies of the Symbiotic Coral Stylophora pistillata

The total daily flux of photosynthetically fixed carbon in light- and shade-adapted phenotypes of the symbiotic coral, Stylophora pistillata, was quantified. Light adapted corals fixed four times as much carbon and respired twice as much as shade corals. Specific growth rates of zooxanthellae in situ were estimated from average daily mitotic indices and from ammonium uptake rates (nitrate uptake or nitrate reductase activity could not be demonstrated). Specific growth rates were very low, demonstrating that of the total net carbon fixed daily, only a small fraction (less than 5 %) goes into zooxanthellae cell growth. The balance of the net fixed carbon (more than 95 %) is translocated to the host. New and conventional methods of measuring total daily translocation were compared. The ‘growth rate’ method, which does not employ 14C, emerged as superior to the conventional in vitro and in vivo methods. The contribution of translocated carbon to animal maintenance respiration (czar) was 143 % in light corals and 58 % in shade corals. Thus, translocation in the former could supply not only the total daily carbon needed for respiration but also a fraction of the carbon needed for growth. Whereas light-adapted corals released only 6%, shade-adapted corals released almost half of their total fixed carbon as dissolved or particulate organic material. This much higher throughput of organic carbon may possibly benefit the heterotrophic microbial community in shade environments.

Light and the Bioenergetics of a Symbiotic Coral

Colonies of coral Stylophora pistillata growing at high light can obtain all the reduced carbon needed for animal respiration from photosynthesis by symbiotic zooxanthellae. In contrast, colonies in shaded reef areas must acquired 60% of their reduced carbon heterotrophically. More than 90% of the carbon fixed by zooxanthellae is translocated to the animal host in both light regimes, but very little is assimilated, apparently because the translocated products are deficient in nitrogen. Thus, the corals overall growth efficiency is similar to that of aquatic herbivores that forage actively. 29 references, 2 figures, 1 table.

The rising tide of ocean diseases: unsolved problems and research priorities

New studies have detected a rising number of reports of diseases in marine organisms such as corals, molluscs, turtles, mammals, and echinoderms over the past three decades. Despite the increasing disease load, microbiological, molecular, and theoretical tools for managing disease in the worlds oceans are under-developed. Review of the new developments in the study of these diseases identifies five major unsolved problems and priorities for future research: (1) detecting origins and reservoirs for marine diseases and tracing the flow of some new pathogens from land to sea; (2) documenting the longevity and host range of infectious stages; (3) evaluating the effect of greater taxonomic diversity of marine relative to terrestrial hosts and pathogens; (4) pinpointing the facilitating role of anthropogenic agents as incubators and conveyors of marine pathogens; (5) adapting epidemiological models to analysis of marine disease.

Autotrophy, Heterotrophy, and Resource Partitioning in Caribbean Reef-Building Corals

Competition can be shown to occur between two species when the removal or thinning of one causes an increase in numbers of the other. This is due to an increase in availability of resources formerly used by both. Over evolutionary time, competition can lead to the extinction of one of the species or to specialization onto different resources by either or both species involved, that is, niche separation, with a concomitant reduction in the degree of competition. Resource partitioning often occurs by character displacement in feeding structures or in feeding behavior in animals or in plants by adaptation to different physical regimes (Schoener 1974). How scleractinian reef corals compete for space (Lang 1973) and how these competitive strategies affect he community structure of New World coral reefs (Porter 1974a) has been worked out in detail. This paper will examine the consequences of competition for energy resources within the Caribbean fauna. Reef-building (hermatypic) corals differ considerably from most animals in functioning at every trophic level of their ecosystem (Porter 1974b). They contain symbiotic algae and can in shallow water produce more oxygen than they consume, placing them among the reefs primary producers. The importance of this symbiosis lies in the tight chemical cycling it allows between plant and animal in response to the nutrient deficiency, particularly of nitrogen, in tropical waters (Lewis 1973). The importance of this symbiosis is also clearly reflected in the morphology of many species, a number of which are plantlike in their growth forms, maximizing their surface area and orienting the major axis of their growth plane toward the light (Goreau 1959; Roos 1967). Although incontrovertible vidence demonstrates the movement of photosynthetic products (primarily glycerol, and to a lesser extent glucose, alanine, and glycolic acid [Muscatine 1973]) from the associated symbiotic algae to the coral, the absolute value of this organic material has not been established. One of the principal theses of this paper will be that, arguing from morphological evidence alone, one can estimate the potential energetic ontribution of the zooxanthellae relative to other means of energy procurement by each species. Equally incontrovertible evidence exists that corals eat zooplankton (Yonge

Resource partitioning by reef corals as determined from stable isotope composition

The pattern of resource partitioning vs depth by corals collected in February 1983 from Jamaica and the Red Sea was determined from their stable carbon isotope composition. Observations were made on isolated zooxanthellae and corresponding algae-free animal tissue from eight species at four depths over a 50 m bathymetric range. Zooxanthellae δ13C was high in shallow water and became lower as depth increased. This trend correlated significantly with the anual integrated photosynthetic rate. The trend is interpreted according to a “depletion-diffusion” hypothesis; in shallow water, at high rates of photosynthesis, metabolic CO2 is nearly depleted and the supply of CO2 from seawater bicarbonate is limited by diffusion. Since most of the available CO2 is fixed, isotope fractionation is minimal. In deeper water, at lower rates of photosynthesis, metabolic CO2 is ample, and isotope fractionation is greater. Animal tissue δ13C was slightly lower than corresponding zooxanthellae values in shallow water. As depth increased the difference between zooxanthellae and animal tissue δ13C increased and the latter approached the δ13C of oceanic particulate organic carbon. These data suggest that carbon is translocated at all depths and that deep-water corals draw significantly on allocthonous sources of carbon.

Patterns of spread of coral disease in the Florida Keys

Reefs in the Florida Keys are experiencing a dramatic increase in the number of localities and number of species with coral disease. In extensive surveys from Key Largo to Key West in 160 stations at 40 randomly chosen sites, there has been a dramatic increase in (1) the number of locations exhibiting disease (82% of all stations are now affected, a 404% increase over 1996 values), (2) the number of species affected (85% of all species are now affected, a 218% increase over 1996 values), and (3) the rate of coral mortality (the deep fore-reef at Carysfort experienced a 60% reduction of living coral cover during the survey). Two null hypotheses (1) that the incidence of disease has remained constant through time and (2) that the apparent increase in disease is due to a lack of comparable earlier data, are both falsified. Different diseases exhibit different patterns of spread: some diseases (e.g. black band) exhibit low incidence and jump rapidly between sites; other diseases (e.g. white pox) exhibit patchy distributions and increase in frequency at affected sites from one year to the next. The central question of why so many corals are becoming simultaneously susceptible to a host of marine pathogens remains unanswered.

Primary production and photoadaptation in light- and shade-adapted colonies of the symbiotic coral, stylophora pistillata

Photoadaptation by photosynthetic organisms to lowered light intensities occurs in part through changes in pigment concentrations and in characteristics of the photosynthetic response curve. We have characterized photoadaptive responses of light- and shade-adapted colonies of the reef coral Stylophora pistillata, which possesses symbiotic algae (zooxanthellae) and grows naturally under a variety of light intensities in the highly cavernous reefs of the Red Sea. Shade-adapted corals have significantly more chlorophyll per individual zooxanthella cell than light-adapted corals (2.98 compared to 12.97 pg chlorophyll a per cell), but not a significantly different number of cells per unit area (1.00 × 106 cells per square centimetre), with the result that the mass of chlorophyll per unit area is greater for shade-adapted corals than for light-adapted corals. Tissue nitrogen content per unit area is significantly lower (p < 0.05) in shade-adapted corals, correlating with a decrease in polyp density (0.10 > p > 0.05) in shade forms. These biomass characteristics are concomitant with a variety of functional responses to natural light intensities. Rate of photosynthesis at saturating light intensities is the same per unit area in both forms (20.2 µgO2cm-2 h-1 for shade specimens; 18.8 for light specimens); but it is significantly different when measured by amount of chlorophyll (1.6 µg O2 (chl a)-1 h-1 for shade specimens compared with 5.0 for light specimens). The initial slope of the P: I curve, α, is significantly higher for shade specimens by area (0.21 for shade corals compared with 0.12 for light corals), but significantly lower for shade specimens by amount of chlorophyll a (0.01 for specimens from shade compared to 0.04 for specimens growing in the light). Ik (the point at which maximum production begins) is significantly lower for shade specimens (138 µmol m-2 s-1 for shade compared to 273 for light), and likewise Ic (the compensation point at which net coral photosynthesis = 0) is also significantly less for shade specimens (30 µmol m-2 s-1 for shade compared to 141 for light). The average nocturnal respiration rate is significantly higher for specimens growing in the light (13.9 µg O2 cm-2 h-1 for light specimens compared to 7.6 for shade specimens). Corals in intense sunlight respire at almost twice the rate of shade corals, probably in response to their higher total gross production. Owing to higher production rates and lower respiration rates, integrated Pc (gross)/Rc (24 h) ratios are greater for shade-adapted specimens either in direct sunlight (1.76 P/R for shade specimens in the light compared to 1.10 for light specimens in the light), or in the shade (0.43 for shade specimens in the cave compared to 0.10 for light specimen in the cave). By using previously defined equations and biomass assumptions, it can be shown that light-adapted Stylophora pistillata can acquire all of their basal metabolic carbon through photosynthesis and translocation, but that shade-adapted Stylophora colonies growing in shade acquire slightly less than half. These results also show that if there were no photoadaptive response, shade-adapted specimens would acquire less than 4 % of their carbon from photosynthesis

Recovery of the coral Montastrea annularis in the Florida Keys after the 1987 Caribbean “bleaching event”

Many reef-building corals and other cnidarians lost photosynthetic pigments and symbiotic algae (zooxanthellae) during the coral bleaching event in the Caribbean in 1987. The Florida Reef Tract included some of the first documented cases, with widespread bleaching of the massive coral Montastrea annularis beginning in late August. Phototransects at Carysfort Reef showed discoloration of >90% of colonies of this species in March 1988 compared to 0% in July 1986; however no mortality was observed between 1986 and 1988. Samples of corals collected in February and June 1988 had zooxanthellae densities ranging from 0.1 in the most lightly colored corals, to 1.6x106 cells/cm2 in the darker corals. Minimum densities increased to 0.5x106 cells/cm2 by August 1989. Chlorophyll-a content of zooxanthellae and zooxanthellar mitotic indices were significantly higher in corals with lower densities of zooxanthellae, suggesting that zooxanthellar at low densities may be more nutrientsufficient than those in unbleached corals. Ash-free dry weight of coral tissue was positively correlated with zooxanthellae density at all sample times and was significantly lower in June 1988 compared to August 1989. Proteins and lipids per cm2 were significantly higher in August 1989 than in February or June, 1988. Although recovery of zooxanthellae density and coral pigmentation to normal levels may occur in less than one year, regrowth of tissue biomass and energy stores lost during the period of low symbiont densities may take significantly longer.