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The study of coral diseases, coral pathogens, and the effects of diseases on tropical and subtropical coral reefs are all current, high-profile research areas. This interest has grown steadily since the first report of a coral disease in 1973. The author of this report was Arnfried Antonius and the publication was an abstract in the proceedings of a scientific meeting of the Association of Marine Laboratories of the Caribbean, or AMLC (then known as the Association of Island Marine Laboratories of the Caribbean). Since Antonius’ pioneering communication he continued ]]>
in situ experimental studies aimed at discerning ]]>
Key words: Caribbean coral diseases, black band disease, white band disease, Arnfried Antonius.
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Resumen
El estudio de las enfermedades de los corales, los patogenos de los corales y los efectos de estas enfermedades sobre los arrecifes tropicales y subtropicales son actualmente areas importantes de investigacion. El interés en este tema ha crecido continuamente desde el primer informe sobre una ]]>
observacion de una nueva enfermedad ]]>
in situ que tenian como objetivo el estudio de la etiologia de las enfermedades ]]>
Palabras clave: Enfermedades de corales, enfermedad de banda negra, enfermedad de banda blanca, Arnfried Antonius ]]>
In 1973, at the 10th meeting of the Association of Island Marine Laboratories of the Caribbean, Arnfried Antonius gave the first report of a coral disease. Abstracts from this meeting were published in 1976, and Antonius’ report, titled “New observations on coral destruction in reefs”, is now widely cited as the ]]>
Fig. 1. Although the publication was produced in 1976, this report has been consistently cited as Antonius (1973) by Antonius himself in his subsequent publications and by subsequent investigators in the field. The actual first publication of a coral disease was by Garrett and Ducklow in 1975.
In the four decades ]]>
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(Sutherland et al. 2004, Weil 2004).
Although widely recognized as the “father of coral disease” for his first reports in this research area, Antonius’ early work also is highly notable in that he was the first to combine field observations with experimental work in the laboratory using controlled conditions; the first to document the relationships ]]>
Recognition and Description of the ]]>
Black Band Disease: The subject of Antonius’ first coral disease report (Antonius 1976) was black band disease (BBD). Although not referred to as a disease in his report (Fig. 1), he conferred this name in the literature in a later publication (Antonius 1981a). In addition to describing the pattern of ]]>
he identified as Oscillatoria submembranacea (Fig. 1) based on a personal communication with Drouet (Antonius 1985a). At that time Drouet was a recognized expert in cyanobacterial taxonomy, using morphological characteristics as the defining criteria. Antonius described the BBD cyanobacterial pathogen ]]>
Phormidium corallyticum in three back-to-back papers (Rutzler & Santavy 1983, Rutzler et al. 1983, Taylor 1983) on which Antonius was co-author of one (Rutzler et al. 1983). In the 2000s the new application of molecular genetics (16SrRNA gene sequencing) to the study of BBD led to much controversy in the ]]>
scillatoria, Geitlerinema, and Leptolyngbya (Cooney et al. 2002, Frias-Lopez et al. 2003, Myers et al. 2007) in the Caribbean and Oscillatoria and Pseudoscillatoria in the Indo-Pacific and Red Sea (Sussman et al. 2006, Rasoulouniriana et ]]>
2009, Sato et al. 2009). Only very recently has this cyanobacterium been formally described under the International Code of Botanical Nomenclature as the new cyanobacterial genus and species Roseofilum reptotaenium (Casamata et al. 2012), which translates as “creeping band of red thread”. The formal characterization includes description of an identifying morphology, that of one tapering and one rounded end cell, as noted and reported by Antonius (1985a).
As seen in Antonius’ first report (Fig. 1), BBD was attributed to the “coral killing” cyanobacterium he described. This contention also became a subject of investigation and controversy, and for many years the BBD pathogen was proposed to be, in addition, to the cyanobacterium, a sulfide-oxidizing bacterium (Ducklow & Mitchell 1979), various heterotrophic bacteria (Cooney
et al. 2002, Frias-Lopez et al. 2004), and a marine fungus (Ramos-Flores 1983). BBD was also proposed as a polymicrobial disease, i.e. caused by a community of bacteria with no primary pathogen (Richardson et al. 1997). A recent meta-analysis of clone libraries constructed from 87 BBD samples collected between 2002 and 2010 (Miller & Richardson 2011) revealed that by far the most common 16S rRNA gene sequence was for R. reptotaenium, detected ]]>
Roseovarius crassostreae, known to be the pathogen of Juvenile Oyster Disease, an uncultured alphaproteobacterium associated with Juvenile Oyster Disease, and a Cytophaga sp. (Cooney et al. 2002, Frias-Lopez
et al. 2002, Sekar et al. 2008). Recently, a unialgal laboratory culture of R. reptotaenium was shown to infect coral in the laboratory and produce BBD (Casamata et al. 2012). While the culture has bacterial contaminants, none of these were found in the BBD-derived clone libraries (Miller & Richardson 2011). Since the culture cannot live without associated bacteria (a pure culture could not maintain viability) Koch’s ]]>
R. reptotaenium as the BBD primary pathogen is currently not feasible. For a discussion of this issue in general see Fredricks & Relman (1996). In 1981 (Antonius 1981a) Antonius modified his identification of a single (cyanobacterial) BBD pathogen to a cyanobacterial pathogen “in association with bacteria”. It appears that he has been right all along.
White Band Disease: White band disease (WBD), first described by Antonius in 1981 (Antonius 1981a, 1981b), was described as “a band of brilliant white skeleton always visible in the wake of a moving front of tissue destruction” (Antonius 1981b). As is the case with BBD, WBD has been, since Antonius’ first report, the subject of ongoing and controversial research and discussion. In particular, a bacterial pathogen of WBD has been elusive and confusing to the point that it has been suggested that various disease signs given names such white plague and white death, in addition to white band, should be referred to as “white syndrome” ]]>
et al. 2003). This same point was made by Antonius in his first report of the disease (1981a) in which he states that WBD is “variously called White Death, Plague, etc.” Antonius experimentally demonstrated that WBD could not be transmitted between coral hosts, either by direct contact or by injection with fresh disease material (Antonius 1981b), and could not be cured using antibiotics (Antonius 1985b). In contrast, in his 1985 study he successfully demonstrated that BBD could be easily transmitted and was curable with antibiotics. Antonius’ overall conclusions about WBD etiology, that it is a ]]>
Shut Down Reaction: In 1977 Antonius first described the coral disease he termed shut down reaction (SDR). He noted that this disease only occurred in corals maintained in aquaria (Antonius 1977), an observation that holds true today (Sutherland et al. 2004). The ]]>
Skeleton Eroding Band: The final coral disease that Antonius was the first to describe is skeleton ]]>
Halofolliculina corallasia, which appears as a dark band that moves across corals while lysing tissue. The fact that Antonius recognized this as separate from BBD attests to his exceptional observational skills, for it is only by close visual examination that one can tell the difference between the two. Antonius reported SEB on corals in the Indo-Pacific. A similar protozoan infection on Caribbean corals has only relatively recently been noted (Croquer et al. 2006)
Combining Field Observations and Experimental Work
While it is well-known that Antonius was the first to report and name several coral diseases, less well know is the fact that he was the first to conduct the combination ]]>
In Antonius’ ongoing work to determine the pathogens associated with BBD and WBD, summarized above, he made the observations that: i) BBD could be easily transmitted between corals, whereas WBD could not; ii) inoculation of a healthy coral with BBD would produce an infection on a healthy coral whereas ]]>
in situ to antibiotics would cure a BBD infected coral but not one infected with WBD; and iv) new BBD infections appeared to occur only on corals infected with WBD, specifically at the site of WBD infection.
The last observation (reported in Antonius 1981a, 1981b, and 1985b) was the basis for a remarkable seven ]]>
in situ on the reef for experimental use. Furthermore, indicative of Antonius’ detailed and exhaustive approach to research, the experiment included corals on reefs of both the Caribbean and the Indo-Pacific. In each region four species of WBD and BBD susceptible corals were studied, a total of eight coral species ]]>
Antonius’ experimental design (Antonius 1985a) consisted of field experiments in which a BBD-infected coral was placed near a WBDinfected coral, and laboratory experiments using aquaria in which he manipulated WBD and BBD-infected corals. ]]>
Antonius’ results were, in his word, “unequivocal” proof of the positive relationship between BBD and WBD. Analysis of the results of the 12 experiments showed that at 30˚C the appearance of a BBD infection on a WBD lesion ranged, for Caribbean corals, from 58-83% on the reef and from 69-92% in aquaria. For Indo-Pacific corals the values were 62-86% on the reef and 71-93% in ]]>
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As remarkable as these experiments is the fact that in the 27 years since this paper was published none of the many investigators in coral disease research has further investigated these fascinating and compelling findings.
Coral Disease Incidence and Environmental Factors ]]>
In the last few decades, as coral disease incidence and prevalence have increased on reefs world-wide, there has been a major focus on the relationship between coral disease and environmental factors, in particular those associated with human activity. Virtually all of the studies that found a positive relationship were preceded by similar work by Antonius.
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Antonius was the first to report a temperature threshold for coral disease, specifically BBD and WBD. His first mention of this (Antonius 1981a) was the observation that both BBD and WBD were seasonal on reefs of high latitude (Bermuda and Florida), with diseased colonies present in the summer but not the winter and with the BBD season longer than that for WBD on the same reefs. Based on extensive field surveys on reefs in the Red Sea combined with temperature data, he demonstrated that BBD activity was strongest at 30˚C but did not occur at or below 26˚C (Antonius 1985b). ]]>
Antonius was also the first to report a correlation of a disease (BBD) with nutrients and sewage outflow. His first observation occurred when he was conducting BBD infection experiments to determine coral host species susceptibility ]]>
et al. 2005).
Coral Diseases and Coral Reef Ecology
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Antonius’ body of work also illustrates his insight into the effect of coral diseases on coral biology and coral reef ecology. Three examples are summarized. The first, part of his ongoing study on BBD infection and transmission, involved experimentally testing the hypothesis that wounds on corals caused by lysing of tissue by mesenterial filaments of aggressive corals of other species could be infected by BBD (Antonius 1985a). He did document successful infection, which he recorded as lower than BBD infections on WBD lesions (40-50% on the reef, 30-40% in aquaria) a ]]>
The second example also arose from BBD infection studies. In this case Antonius noted that BBD often began at the site of a clump of green algae growing near or onto a coral colony. His interpretation was that the pathogenic BBD cyanobacterium resided in the green algal turf, which served as a reservoir, and that as the turf moved against the coral via wave action it abraded the ]]>
Finally, Antonius showed that susceptibility to coral disease could be used as a coral taxonomic tool. In Antonius (1988b) he noted that there was confusion as to whether Platygyra lamellina and ]]>
P. daedalea were one or two species. The controversy was resolved when he determined that P. daedalea could not be infected with BBD, whereas P. lamellina was susceptible. In addition to these three examples there are many more cases of extrapolation of his work to coral reef ecology in his papers.
Coral Diseases and ]]>
Since Antonius’ first report of a coral disease at the AMLC meeting in 1973 there has been a steady stream of papers presented at AMLC scientific meetings that focused on, or were related to, coral diseases (see proceedings on the AMLC website, http://www.amlc-carib.org/). And, beginning in 1997 and at every AMLC scientific meeting since, there were sessions dedicated to ]]>
Acknowledgments
Arnfried Antonius ]]>
th Scientific Meeting of the AMLC, held at the Universidad de Costa Rica, San Pedro, Costa Rica, was dedicated to his memory as is this paper, presented at the meeting. References
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*Correspondencia: Laurie L. Richardson: Department of Biological Sciences, Florida International University, Miami, Florida 33199 USA; richardl@fiu.edu
1 Department of Biological Sciences, Florida International University, Miami, Florida 33199 USA; richardl@fiu.edu
Received 22-VII-2011. Corrected 17-XI-2011. Accepted 20-XII-2011.