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Bacteria that affects coral health with an emphasis on the Gulf of Mexico and the Caribbean Sea.

INTRODUCTION

Coral reefs worldwide protect the high biodiversity of species that over time have been threatened by human activities and settlements in its vicinity (Zamudio-Aleman et al., 2014). The effect of climate change, by impacting with a gradual increase in water temperature, constitutes a threat to the existence of coral reefs. By the end of the century, in 2100, the average global temperature of water could rise from 1.4 [degrees] to 5.8 [degrees]C according to the International Panel on Climate Change (IPCC) (Rahman-Sunny, 2017; Abera-Hirpo, 2018). The trend in temperature increase for the present century is an observed value of 0.13 [degrees]C per decade from 1971 to 2000. For the current period from 2011 to 2040 a trend of an increase of 1.4 [degrees]C is expected, while for 2041 to 2070 that increment could rise to 2.4 [degrees]C (Magoni & Mesa-Munoz, 2018). The gradual increase in temperature shows a relationship with the presence of bacteria, which threatens coral communities causing damage to the polyp-symbiont-holobiont association (coral polyp, zooxanthellae and bacteria) (Maynard et al., 2015), the latter causes loss of coral cover (Jackson et al., 2014; Marulanda-Gomez et al., 2017).

Some pathogenic bacteria are difficult to identify, as are environmental parameters of the ocean that increase the infectious effect. There are not many phenotypic differences in disease in corals and may correspond to different types of infections (Page et al., 2016). Coral species present a difference in their bacterial composition, as well as in species found in the water column. However, there are still studies to be done, in order to know its origin and how pathogenic bacteria act on the coral (Sassi et al., 2015).

Microbiological studies in corals emerge because of the presence of different diseases (Table 1). Some authors have the purpose of identifying the pathogen, fulfilling the postulates of Koch (Puyana et al., 2015). For the identification of pathogens, the most commonly used techniques are microbiology and molecular biology like Polymerase Chain Reaction (PCR) because of their simplicity, low cost, and reliability of results (Sweet et al., 2017).

The study of the different diseases that are presented in corals is of international concern. Investigations that are being developed go from being descriptive to multidisciplinary. These investigations involve aspects of ecology, microbiology, and chemistry (Vogel et al., 2015; May & Woodley, 2016; Meyer et al., 2016). This review aims to present scientific information generated from the identification of different pathogenic bacteria that affect coral's health with an emphasis on the Gulf of Mexico and the Caribbean Sea.

Halofolliculina corallasia (Antonius & Lipscomb, 2001)

Halofolliculina corallasia is a sessile ciliary heterotrichea, although it is not a bacterium, it is the first reported protozoan that affects corals; it is distinguished by its type of reproduction (cell division and conjugation). The cell has two nuclei and at some stage in its life presents cilia (Antonius & Lipscomb, 2001). Coral species that are affected by this ciliary (Halofolliculina) have a dark band that surrounds the healthy tissue and on the opposite side a skeleton recently devoid of tissue. The particularity of this affectation is observed in an approach, where independent cilia can be observed, which is found in the dark band (Alder, 2014).

The genus Halofolliculina affects 25 species of scleractinian coral from six families in the Caribbean (Acroporidae, Agaricidae, Astrocoeniidae, Faviidae, Meandrinidae, and Poritidae) (Page et al., 2016). These observations include the coasts of Venezuela, Panama, Mexico, Curazao and Puerto Rico (Croquer et al., 2005). In the Indo-Pacific region, it was suspected that the species H. corallasia was the cause of diseases in its coral areas, but it was shown that this ciliate belongs to another species. The disease of the skeletal eroding band (SEB), which manifests as dense aggregations of the ciliate H. corallasia, is confused with diseases of the black band. Another disease caused by the bacterium is the Caribbean ciliate infection (CCI) a mottled appearance with black bands on the body of the coral; affecting ten coral species included Dichocoenia, Montastrea, Acropora spp. (Sheridan et al., 2013).

Damage caused by this species is undoubtedly a limiting factor for reef-forming coral species. The mechanisms that develop the disease are still unknown, so further research is needed on this subject (Croquer et al, 2005).

Oscillatoria sp.

The genus Oscillatoria belongs to the division of Cyanobacteria of the group of autotrophic prokaryotes, which inhabits fresh, brackish and marine shallow waters, is distributed throughout the world although some species are geographically more limited (Gardner, 1932). It is reported by (Myers et al., 2007), as the cause of affectations to scleractinian corals to Black Band Disease (BBD). The BBD is observed and described for presenting the skeleton of a naked coral followed by a dark band, where a consortium of bacteria, including the genus Oscillatoria, are the apparent cause of the disease. The band has a thickness of 5 to 20 mm, and after the band is the healthy tissue. The BBD affects more than 19 species of scleractinian corals, data obtained in the Caribbean Sea (Sutherland & Ritchie, 2004). Another disease caused by cyanobacteria Oscillatoria sp. is the Red Band Disease (RBD), affecting coral species such as Strigosa sp., Montastraea annularis, Montastrea cavernosa, Porites astreoides, and Siderastrea siderea, having a range of affectation per day of approximately 1 mm.

The movements of the Oscillatoria genus in the BBD and RBD bands appear to be in response to chemical factors and not to luminosity responses. Miller & Richardson (2012) tested Black Bands disease based on the production of toxins, microcystin, and sulfide, produced by the bacterial consortium including the genus Oscillatoria under controlled conditions, resulting in tissue lysis when adding the toxins to the coral and a time of the same reaction compared to sick corals by the BBD. In this way, the participation of cyanotoxins by cyanobacteria and sulfide by sulfur reducing bacteria is demonstrated.

Vibrio spp.

The species of Vibrio genus are Gram-negative bacteria, of a size of 2 to 3 [micro]m in length, have a polar flagellum that gives them great mobility, are positive oxidase and facultative anaerobes, which support alkaline media as well as high concentrations in a saline medium. Species of bacteria reported as pathogenic are implicated in many diseases in corals. The characteristics of the affections are in function of the species-environment-host, causing negative impacts on the composition of marine ecosystems (Castaneda-Chavez et al., 2015). Such is the case of V. coralliilyticus, V. shiloi that have been commonly detected in apparently healthy corals, which was studied by Kushmaro et al. (1997), revealing that V. shiloi affects the Oculina patagonica coral, this done in the Mediterranean Sea. Banin et al. (2001) further studied this etiology, finding that V. shiloi is attracted to the mucus generated by Patagonian coral. Oculina patagonica and adheres when temperatures range from 25-28 [degrees]C. V. shiloi produces extracellular toxins that hinder the production of photosynthesis of the zooxanthellae (Ross, 2014).

Dark spot syndrome (DSS) is another disease involving Vibrio spp. These organisms in the kingdom Fungi, also affect corals of the genus Montastraea, Siderastrea, Stephanocoenia and even to Agaricia agaricites. The disease can be appreciated in the annular part of the coral with purple margins (Sheridan et al, 2013).

Shut-down-reaction (SDR) is another condition in corals where Vibrio harveyi and V. alginolyticus bacteria are involved; these mainly affect the corals Stephanocoenia intersepta, Siderastrea siderea, and Montastraea annularis, the disease appears as rapid tissue degradation (Sheridan et al., 2013).

Ulcerative white spots (UWS) is caused by Vibrio spp. mainly affects species of the Porites genus. The appearance of the disease occurs with tissue whitening of 3-5 mm to 5 cm progressing in different patterns mainly in tissue loss (Raymundo et al., 2003).

Black band disease type II (BBD II) affects the coral Acropora cervicornis, and it is believed that Vibrio carchariae is the cause, as studies by Ritchie & Smith (1995) demonstrated the presence of bacteria in diseased corals and absence in healthy corals. Madigan et al. (2003), demonstrates the doubtful participation of bacteria V. charchariae in failing to fulfill Koch's fourth postulate (4o the presumed pathogen must reisolate itself from lesions produced in experimental organisms). There is no doubt that this disease has caused 99% of the death coral in the Caribbean Sea, an event discussed by Gladfelter in 1982 (Gil-Agudelo et al., 2009) and continues to wreak havoc along the Caribbean Sea (Gonzalez-Ontivero, 2006).

The genus Vibrio causes white Syndrome (WS), but the species is unknown. It mainly affects the coral genus Turbinaria, Acropora, Goniastrea, Pocillopora, Porites, Pavona, Stylophora, Montipora, and Faviidae. The disease characteristics are diffuse areas of tissue loss with an exposed skeleton (Sweet & Bythell, 2012). Yellow band disease (YBD) is caused by Vibrio spp. It affects mainly the Montastraea genus. The characteristic is spots where the skeleton is exposed, perimeter surrounded by a yellow to white margin (Croquer et al., 2013).

Some species of the Vibrio genus pose risks to corals health, which is undoubtedly demonstrated by the loss of coral cover and affects different coral species. There is a lack of identification of other agents of Vibrio spp., which are implicated in diseases of corals and the role of these bacteria in the infectious and etiological role of diseases (Arotsker & Kushmaro, 2016).

Phormidium sp. (Rutzler & Santavy, 1983)

The filamentous cyanobacteria Phormidium sp., presents a stratified macro and microscopic growth, is photoautotrophic, its phases (photoautotrophic and heterotrophic) are in the range of other species of cyanobacteria. Phormidium sp. causes damage to corals that facilitate the attack of other sulfoxide bacteria (Stal, 1995). Ravindran & Raghukumar (2002) report the cyanobacterium Phormidium valderianum (fulfilling the Koch postulates) as the cause of the Pink Line Syndrome (PLS) in the Indian Ocean, affecting the coral Porites lutea. The characteristic of this disease is a pink line, which separates dead tissue from living tissue. Ravindran & Raghukumar (2006), report that 20% of the Porites lutea colonies were affected by PLS in the Lakshadweep Islands, this in the Arabian Sea in 1996 and the percentage increased by 2000.

Studies were carried out to see the etiology of PLS caused by the cyanobacterium Phormidium valderianum, finding other pathogens of the Fungi kingdom (Aspergillus niger, Curvularia lunata), which together are involved in tissue degradation. In particular, the cyanobacteria attack and inhibit the photosynthesis originated by the zooxanthellae causing the expulsion of the same. In response to the PLS outbreak in coral, it was found that the abiotic factor is the increase of CO2 in the medium, this, without the presence of agents of the Fungi kingdom (Ravindran & Raghukumar, 2006).

Phormidium corallyticum was described by Rutzler & Santavy (1983) after a reclassification of a cyanobacteria, identified as Oscillatoria submembranacea by Antonius (1981). P. corallyticum was identified as the cause of BBD that attacks scleractinian corals. Frias-Lopez et al. (2003) identified three cyanobacteria that in a consortium originate BBD, thus discarding the participation of P. corallyticum. The discussion regarding the agents causing BBD is under investigation.

Aurantimonas coralicida (Antonius & Lipscomb, 2001)

Aurantimonas coralicida, an obligate aerobe, belongs to the order Rhizobiales. The family comprises only two species, they are recognized because they have a bacillus form with polar flagella, branched colonies, and obtain its nourishment chemo-heterotrophically. Denner et al. (2003) proposed A. coralicida, as the putative pathogen of White Plague Disease Type II (WPD II). This bacterium is reported to affect more than 40 different species of corals (Weil et al., 2006). Whereas the bacterial pathogen A. coralicida, isolated from Dichocoenia stokesi, is the only example for which Koch's postulates have been fulfilled (Denner et al., 2003).

Other studies such as Sunagawa et al. (2009) performed the identification of bacteria present in coral Montastraea faveolata, healthy and diseased tissue samples with signs of WPD II, not finding the putative pathogen A. coralicida. Sunagawa et al. (2009) refer that WPD II is probably attributed to a bacterial complex or to different bacteria that may be causing WPD II like signs in many different coral species in both the Pacific and Atlantic regions.

Helicostoma notatum (Kahl, 1931)

The ciliate Helicostoma notatum is the possible cause of the Brown band disease (BrBD) that affects corals of the Great Barrier Reef (GBR). The appearance of the disease is a brown colored band that divides healthy tissue from diseased tissue, there is no specific band size, and sometimes there is a white band between healthy tissue and the brown band. The coloration of the band originates from the density of the ciliary H. notatum, which in aquarium culture condition; the brown color has a jelly appearance (Borneman, 2001 apud Willis et al., 2004).

Serratia marcescens

Serratia marcescens is a Gram-negative Bacillus-like bacterium, growing in temperatures ranging from 540 [degrees]C. They grow in pH levels that range from 5 to 9 (Bennett & Bentley, 2000), it is common to find it in the intestines of animals. It is noted as causing diseases such as the White Pox (WP) that mainly affects corals of the genus Acropora. The disease was first observed and described, in the Florida Keys by Holden (1996). The pathological features are irregular white patches surrounded by a necrotic front in the body of the coral simulating smallpox. The disease is also called Patchy Necrosis (Bruckner & Bruckner, 1997).

Data from Sutherland & Ritchie (2004), Sutherland et al. (2011) show a loss of 87% Acropora palmata coral between 1996 and 2002 in the Florida Keys area. S. marcescens has been responsible for diseases in terrestrial animals, humans, and insects. The contribution of these bacteria to the marine environment is mainly by the discharge of wastewater that comes in direct contact with corals (Sutherland et al., 2011). The spread of the disease concerning other diseases in corals is slow and may take up to one year to infect another colony (Lesser et al., 2007).

Impact sources causing the presence of pathogenic bacteria in the marine environment

Coral reefs that are located near coastal areas, where there are human activities and settlements, are exposed to the excessive dumping of nutrients, sediments, and bacteria that threaten the growth, reproduction and interaction between important organisms (symbionts) for their subsistence (Fabricius, 2005; Bianchi et al., 2014).

Kaczmarsky et al. (2005) conducted a study to measure the relationship between coral diseases (BBD and WP II) and wastewater discharges at two sites, Frederiksted and Butler Bay, in U.S. Virginia Islands finding the highest rate of epizootics at site 1 with 3.7%, while at site 2 the rate was 2.5%. The colonies of corals, most susceptible to diseases were Diploria clivosa and Dichocoenia stokesi. These results contrast mainly because site 2 is the closest to the coast and has more influence on wastewater discharges, with more variety of colonies unlike site 1. Currents are a physical factor that helps both transport of nutrient sediments and bacteria that disperse all the material through the ocean. Zavala-Hidalgo et al. (2003) carried out a study on the behavior of currents in the Gulf of Mexico, finding differences in the pattern of circulation and temperatures during a whole year, which is regarded as a reference for the dispersion behavior of the wastewater discharges over the reef areas.

It has been verified through the study conducted by Gutierrez-Ruiz et al. (2011), that coral reefs are more susceptible both to disease and species diversity when they are close to the coast, in contrast to the more distant reefs. Temperature is another factor that promotes the emergence of diseases and limits the diversity of species. Factors in which, humans have intervened (global warming) causing stress and giving optimal conditions to opportunistic bacteria (Peters, 2015). Such is the case of Cervino et al. (2004), who carried out a study to measure the effects of Vibrio bacteria at four different temperatures, taking the survival index and disease signs leading to yellow blotch/band disease (YBD) in Caribbean corals Montastrea spp., in which, more significant signs of the disease were found at temperatures higher than 25 [degrees]C. Towards the end of the experiment, it was found that the mean diameter of the yellow lesion increased by 96 h from 0.74 cm at 20 [degrees]C to 2.2 cm at 33 [degrees]C. None of the controls developed YBD lesions.

Bruno et al. (2003) and Gutierrez-Ruiz et al. (2011), argue that human activities have altered the environmental conditions affecting coral ecosystems, reflected in the increase in the concentration of inorganic nitrogen and phosphorus in the ocean, because of the residual discharges and contributions from rivers. Nutrients increase benefits the increase of fungi population and bacteria and in turn their virulence as pathogens, leading to diseases such as aspergillosis and black band disease among others (Bruno et al., 2003, Pinzon et al., 2014). Fabricius (2005) evaluates the effects of terrestrial runoff on the growth and survival of hard coral colonies, coral reproduction, and recruitment, and organisms that interact on scleractinian coral populations, taking as parameters: increased dissolved inorganic nutrients, enrichment with the particulate organic matter, the light reduction from turbidity and increased sedimentation. Worldwide, the scale of reef pollution estimates that 22% of all coral reefs are classified as at high (12%) or medium (10%) threat from inland pollution and soil erosion. The models also classify 30% of reefs as threatened from coastal development (proximity to cities, mines, and resorts), and 12% at threat from marine pollution (distance to ports, oil tanks, oil wells, and shipping areas). Therefore, on a global scale, coral reefs are threatened by similar contaminations in risk and magnitude (Arellano-Mendez et al., 2016). Hernandez-Zulueta et al. (2017) emphasize the relationships of bacterial assemblages associated with coral reef species in the Mexican Central Pacific area.

Studies conducted in the Gulf of Mexico and the Mexican Caribbean

The following is a summary of some work done in important reef areas of the Gulf of Mexico and the Mexican Caribbean, regarding pollution, diseases and anthropogenic factors. In which, a significant environmental deterioration is reported; where the specific factors that degrade the environmental quality are directly related to the discharges of wastewater with high levels of nutrients, toxic substances and sedimentation of particles. Therefore, regional and global anthropic impacts are a probable cause of this deterioration (Daszak et al., 2001).

Bruno et al. (2003), conducted a study on nutrient uptake and severity in coral diseases in the Yucatan Peninsula (Akumal), based on environmental changes caused by human activities. It also shows evidence of increased nutrients in the environment and identifies two diseases, aspergillosis in the coral Gorgonia ventalina and the yellow band disease in Montastraea annularis and M. franksi. They propose water quality management to minimize nutrient enrichment, as well as identify other global aspects that may influence disease dynamics.

Jordan-Dahlgren et al. (2005) accomplished a study on the prevalence of clinical signs of disease and mortality in colonies of Montastraea annularis in the northeastern Caribbean and the Gulf of Mexico. It was proved that a higher prevalence of these parameters is constant when they are close to point sources of contamination.

Experiments were performed on three types of the reef, one isolated, another with urban influence and a third one influenced by industrial pollutants. The results show that concerning diseases in M.an nularis; no significant differences were found in relation to urban and industrial influence, so that the isolated reef presented prevalence in the diseases, thus rejecting their hypothesis. Jordan-Dahlgren et al. (2005), opens the possibility that other environmental and/or global factors may be playing another important role in the prevalence of coral diseases in the Caribbean and Gulf of Mexico. Pathogens in reefs show a high level of connectivity, such as circulation patterns, pollutants from inland, and warming of the sea surface that stresses corals.

Ward et al. (2006) analyzed the diversity of diseases in the Yucatan Peninsula. They quantified the prevalence of diseases and coral diversity, as well as the prevalence of these diseases and the relationship with octocorals and scleractinian corals. They also found species variability (71 species of corals) and documented six diseases for scleractinian corals that remained constant between 2002 and 2004, with a higher prevalence for octocorals. Therefore, no association was found between scleractinian corals and octocorals. These diseases, no doubt, become susceptible to coral's diversity. The present paper is the first study to measure the prevalence of diseases in the long term.

Aguirre-Macedo et al. (2008) studied the discharge of ballast water of the freighters that transit on the Cayo de Arcas Campeche Reef System (CACRS). The discharge of ballast water carries nutrients, phytoplankton, and pathogenic bacteria that may place the CACRS area at risk. Thirty oil tankers of PEMEX (Mexican Petroleum Company) and reference sites in the reef area were evaluated. The results indicate that ballast water discharges contain pathogenic bacteria, both for humans and for corals (70% of oil tanks). However, the evaluation of reference sites in the coral reef area did not show the presence of more pathogenic bacteria, beyond the presence of total coliforms, having with this good water quality. It is concluded that there is no detrimental effect regarding ballast water discharges to the Cayo de Arcas Campeche Reef.

Horta-Puga et al. (2008) analyzed the current state of Punta Gorda Reef in the Veracruz Reef System. The sampling of Punta Gorda reef included the geomorphological zones of the coral reef plain and windward slope. Thirty-three transects were positioned in the reef plain in which no coral was recorded, whereas in the windward area, 55 transects were positioned recording four species of scleractinian corals. Having through this, the data corresponding to the coral cover with a 0.39% for the slope of windward. Punta Gorda reef as shown in the study by Horta-Puga et al. (2008), is a profoundly impacted area that dates to colonial times (La Villa Rica de la Veracruz). To date, this reef no longer has the richness of species and the typical characteristics of one in function. It should be mentioned that this study was implemented to consider the possible expansion of the Port of Veracruz (API-Veracruz).

Gutierrez-Ruiz et al. (2011), carried out a study on anthropic disturbances on the diversity of stony corals in the Veracruz Reef System National Park (VRSNP), between reefs, located close (Sacrificio Reef) and far away (Santiaguillo Reef) of the port of Veracruz, Mexico. Taking as indicators, the diseases present in corals and the diversity of species in each area of study. Gutierrez-Ruiz et al. (2011) found that the predominance of diseases was higher at Sacrificios than at Santiaguillo; and the coral diversity was lower at Sacrificios than at Santiaguillo. Concluding that the northern area of the VRSNP is near the coast of Veracruz and the port traffic, consequently, they have been strongly impacted, while the Anton Lizardo area is better preserved, as it is further away from the city, and away from navigation routes to the port. However, the authors recommend the search for factors and diversity that originate diseases in the reef areas.

Hayasaka-Ramirez & Ortiz-Lozano, (2014), studied the generation of specific indicators linked to stranding events in the Veracruz Reef System National Park (VRSNP). In search of information on the subject, 126 events of this nature were described, as well as the causes and sites where they were performed, resulting in useful information given the demographic explosion in Veracruz Port.

Castaneda-Chavez et al. (2015), made a diagnosis of bacteria of the genus Vibrio spp. in corals of the VRSNP. With the support of the National Commission of Natural Protected Areas (NCNPA), they obtained samples of 12 fixed transects distributed within the polygon of the reef. A positive presence in a 42.3% of Vibrio complex, V. coralliilyticus and V. shilonii was observed in the coral tissue of Colpophyllia natans, Montastraea cavernosa, M. faveolata, Porites astreoides, and Siderastrea siderea. It was concluded that the presence of pathogenic bacteria comes from the contribution of organic matter from anthropogenic sources discharged directly into the area. Causing pathological affections in coral tissue, such as White Band, Black Band, Yellow Band, White Plague, and Bacterial Bleaching, are stimulating, in the short term, loss of coral cover and, in the long term, negative impacts on the faunal composition of the Veracruz Reef System (VRS).

Celis-Hernandez et al. (2017), conducted a study on sediment and pollution on the coast of Veracruz in four study sites, taking as reference the influence exerted by two rivers: Jamapa and La Antigua. The results present the potential to be taken as a baseline concerning future anthropic interventions in the specific treatment of heavy metals of greater toxicity and their possible effects on the biotic activities of goods and services as well as commercial activities carried out in that area.

CONCLUSIONS

The following pathogenic bacteria are identified as the main responsible for endangering the health of corals: Aurantimonas coralicide, Halofolliculina corallasia, Helicostoma nonatum, Oscillatoria sp., Phormidium corallycticum, Phormidium valderianum, Serratia marcescens, and Vibrio spp. It was concluded that the presence of pathogenic bacteria comes from the contributions of organic matter from anthropogenic sources that discharge directly into reef areas; generating pathological affectations in coral tissue, such as White Band, Black Band, Yellow Band, White Plague, and Bacterial Whitening. The preceding stimulates, in the short term, loss of coral reef cover and, in the long term, negative impacts on the faunal composition.

It is defined that other causes can cause the existence of affectations in corals, such as those related to climate change and global warming, being stressors, stimulators of growth and the activity of several pathogens in corals, which give rise to diseases known as: White Plague, Black Band, Yellow Band, and aspergillosis among others.

The design of conservation strategies with the support of public policies, as is being done in some countries that have this problem becomes a must. As well as managing which key areas for their high marine biodiversity, should be called protected natural areas and therefore receive support for their surveillance. It is necessary to strengthen efforts, with non-invasive techniques, for the restoration of reefs in the Caribbean and the Gulf of Mexico. The future will depend on the joint decisions made by humanity in the coming years to limit and stop the emission of greenhouse gases, which will reduce the increase in temperature and corals may have a better chance of survival.

DOI: 10.3856/vol46-issue5-fulltext-2

REFERENCES

Abera-Hirpo, L. 2018. The impact of climate change on fisheries in the tropics. Int. J. Fish. Aquat. Stud., 6(1): 122-127.

Aguirre-Macedo, L., V. Vidal-Martinez, J. HerreraSilveira, D. Valdes-Lozano, M. Herrera-Rodriguez & M. Olvera-Novoa. 2008. Ballast water as a vector of coral pathogens in the Gulf of Mexico: the case of the Cayo Arcas Coral Reef. Mar. Pollut. Bull., 56: 1570-1577.

Alder, V.A. 2014. Protistas marinos. Fundacion de Historia

Natural Felix de Azara, Buenos Aires, pp. 13-34. Antonius, A.A. 1981. Coral reef pathology: a review. In: E.D. Gomez, C.E. Birkeland, R.W. Buddemeier, R.E. Johannes, J.A. Marsh & R. Tsud Jr. (eds.). The Reef and Man. Proceedings of the Fourth International Coral Reef Symposium. Marine Sciences Center, University of the Philippines, Quezon City, 2: 3-6.

Antonius, A.A. 1981. The "band" diseases in coral reefs. In: E.D. Gomez, C.E. Birkeland, R.W. Buddemeier, R.E. Johannes, J.A. Marsh & R. Tsud Jr. (eds.). The Reef and Man. Proceedings of the Fourth International Coral Reef Symposium. Marine Sciences Center, University of the Philippines, Quezon City, 2: 7-14.

Antonius, A.A. & D. Lipscomb. 2001. En imprimacion protozoario coral-killer identificada en el Indo-Pacifico. Bol. Atoll Invest., Smithsonian Institution, 481(1-21): 8-15.

Arellano-Mendez, L.U., J. Bello-Pineda, J.A. Ake-Castillo, H. Perez-Espana & L. Martinez-Cardenas. 2016. Distribucion espacial y estructura morfometrica de las praderas de Thalassia testudinum (Hydrocharitaceae) en dos arrecifes del Parque Nacional Sistema Arrecifal Veracruzano, Mexico. Rev. Biol. Trop., 64(2): 427-448.

Arotsker, L. & A. Kushmaro. 2016. Vibriosis. In: C.M. Woodley, C.A. Downs, A.W. Bruckner, J.W. Porter & S.B. Galloway (eds.). Diseases of coral. John Wiley & Sons, Hoboken, pp. 206-220.

Banin, E., T. Israely, M. Fine, Y. Loya & E. Rosenberg. 2001. Role of endosymbiotic zooxanthellae and coral mucus in the adhesion of the coral-bleaching pathogen Vibrio shiloi to its host. FEMS Microbiol. Lett., 199: 33-37.

Bennett, J.W. & R. Bentley. 2000. Seeing red: the story of prodigiosin. Adv. Appl. Microbiol., 47: 1-32.

Bianchi, V., P. Varela, D. Flores & P. Durando. 2014. Evaluacion de Escherichia coli resistente a antibioticos como especie bioindicadora de contaminacion fecal en agua y peces en la cuenca inferior del Rio San Juan. Nat. Neotrop., 45(1): 45-69.

Borneman, E.H. 2001. Aquarium corals: selection, husbandry, and natural history. TFH Publishing, New Jersey, 464 pp.

Bruckner, A.W. 2016. White syndromes of western Atlantic reef-building corals. In: C.M. Woodley, C.A. Downs, A.W. Bruckner, J.W. Porter & S.B. Galloway (eds.). Diseases of coral. John Wiley & Sons, Hoboken, pp. 316-332.

Bruckner, A. & R.J. Bruckner. 1997. Outbreak of coral disease in Puerto Rico. Coral Reefs, 16(5): 260-260.

Bruno, F.J., E.L. Petes, D.C. Harvell & A. Hettinger. 2003. Nutrient enrichment can increase the severity of coral diseases. Ecol. Lett., 6: 1056-1061.

Castaneda-Chavez, M.R., F. Lango-Reynoso, I. Galaviz-Villa & J.L. Garcia-Fuentes. 2015. Vibrio spp. en corales del sistema arrecifal Veracruzano. In: A. Granados-Barba, L. Ortiz-Lozano, D. Salas-Monreal & Gonzalez-Gandara (eds.). Aportes al conocimiento del sistema arrecifal Veracruzano: hacia el Corredor Arrecifal del suroeste del Golfo de Mexico. Universidad Autonoma de Campeche, Campeche, pp. 267-280.

Celis-Hernandez, O., L. Rosales-Hoz, A.B. Cundy & A. Carranza-Edwards. 2017. Sedimentary heavy metal (loid) contamination in the Veracruz shelf, Gulf of Mexico: a baseline survey from a rapidly developing tropical coast. Mar. Pollut. Bull., 119: 204-213.

Cervino, J.M., R.L. Hayes, S.W. Polson, S.C. Polson, T.J. Goreau, R.J. Martinez & G.W. Smith. 2004. Relationship of Vibrio species infection and elevated temperatures to yellow blotch/band disease in Caribbean corals. Appl. Environ. Microbiol., 70: 6855-6864.

Croquer, A., E. Weil, A.I. Zubillaga & S.M. Pauls. 2005. Impact of a white plague-II outbreak on a coral reef in the Archipelago Los Roques National Park, Venezuela. Caribb. J. Sci., 41(4): 815-823.

Croquer, A., C. Bastidas, A. Elliott & M. Sweet. 2013. Bacterial assemblages shift from healthy to yellow band disease in the dominant reef coral Montastraea faveolata. Environ. Microbiol. Rep., 5: 90-96.

Daszak, P., A. Cunningham & D. Hyatt. 2001. Anthropogenic environmental change and the emergence of infectious diseases in wildlife. Acta Trop., 78: 103-116.

Denner, E.B.M., G.W. Smith, H.J. Busse, P. Schumann, T. Narzt & S.W. Polson. 2003. Aurantimonas coralicida gen. nov., sp nov., the causative agent of White Plague Type II on Caribbean scleractinian corals. Int. J. Syst. Evol. Microbiol., 53: 1115-1122.

Fabricius, K. 2005. Effects of terrestrial runoff on the ecology of corals and coral reefs: review and synthesis. Mar. Pollut. Bull., 50: 125-146.

Frias-Lopez, J., G.T. Bonheyo, Q. Jin & B.W. Fouke. 2003. Cyanobacteria associated with coral black band disease in Caribbean and Indo-Pacific reefs. Appl. Environ. Microbiol., 69(4): 2409-2413.

Gardner, N.L. 1932. The Myxophyceae of Porto Rico and the Virgin Islands. Scientific survey of Porto Rico and the Virgin Islands, 8: 249-311.

Gavio, B., M.A. Cifuentes-Ossa & M.J. Wynne. 2015. Notes on the marine algae of the International Biosphere Reserve Seaflower, Caribbean Colombia. V. First study of the algal flora of Quitasueno Bank. Bol. Invest. Mar. Cost., 44(1): 117-126.

Gil-Agudelo, D.L., G.W. Smith & E. Weil. 2006. The White band disease type II pathogen in Puerto Rico. Rev. Biol. Trop., 54(3): 59-67.

Gil-Agudelo, D.L., R. Navas-Camacho, A. Rodriguez-Ramirez, M.C. Reyes-Nivia, S. Bejarano, J. Garzon-Ferreira & G.W. Smith. 2009. Enfermedades coralinas y su investigacion en los arrecifes colombianos. Bol. Invest. Mar. Cost., 38(2): 189-224.

Gonzalez-Ontivero, O. 2006. Variaciones espaciales y temporales de las enfermedades en dos arrecifes de la region occidental de Cuba. Tesis de Maestria, Universidad de La Habana, La Habana, 66 pp.

Gutierrez-Ruiz, C., M. Roman-Vives, C. Vergara & E. Badano. 2011. Impact of anthropogenic disturbances on the diversity of shallow, stony corals in the Veracruz Reef System National Park. Rev. Mex. Biodivers., 82: 249-260.

Hayasaka-Ramirez, S. & L. Ortiz-Lozano. 2014. Anthropogenic pressure associated with vessel groundings on coral reefs in a marine protected area. Cienc. Mar., 40(4): 237-249.

Hernandez-Zulueta, J., L. Diaz-Perez, R. Araya, O. Vargas-Ponce, A.P. Rodriguez-Troncoso, E. Rios-Jara, M. Ortiz & F.A. Rodriguez-Zaragoza. 2017. Bacterial assemblages associated with coral species of the Mexican Central Pacific. Rev. Biol. Mar. Oceanogr., 52(2): 201-218.

Holden, C. 1996. Coral disease hot spot in the Florida Keys. Science, 274: 2017.

Horta-Puga, G., J. Tello, M. Avila & J. Nunez. 2008. Estado actual del arrecife Punta Gorda, Sistema Arrecifal Veracruzano. Universidad Autonoma de Mexico, Facultad de Estudios Superiores Iztacala, UBIPRO, 126 pp.

Iyer, G. 2016. Los corales que sobrevivieron: desentranando los secretos geneticos de la resistencia. Tropicos, 2(1): 16-18.

Jackson, J.B.C., M.K. Donovan, K.L. Cramer & V.V. Lam (eds.). 2014. Status and trends of Caribbean Coral Reefs: 1970-2012. Global Coral Reef Monitoring Network, UICN. Gland, 304 pp.

Jordan-Dahlgren, E., M.A. Maldonado & R.E. Rodriguez-Martinez. 2005. Diseases and partial mortality in Montastraea annularis species complex in reefs with differing environmental conditions (NW Caribbean and Gulf of Mexico). Dis. Aquat. Organ., 63: 3-12.

Kaczmarsky, L., M. Draud & E. Williams. 2005. Is there a relationship between proximity to sewage effluent and the prevalence of coral disease? Caribb. J. Sci., 41(1): 124-137.

Kahl, A. 1931. Urtiere oder Protozoa. I: Wimpertiere oder Ciliata (Infusoria). 2. Holotricha. Tierwelt Dtl., 21: 181-398.

Kemp, K.M., J.R. Westrich, M.S. Alabady, M.L. Edwards & E.K. Lipp. 2018. Abundance and multilocus sequence analysis of Vibrio bacteria associated with diseased elkhorn coral (Acropora palmata) of the Florida Keys. Appl. Environ. Microbiol., 84(2): e01035-17. doi: 10.1128/AEM.01035-17.

Kushmaro, A., E. Rosenberg, M. Fine & Y. Loya. 1997. Bleaching of the coral Oculina patagonica by Vibrio AK-1. Mar. Ecol. Prog. Ser., 147(1/3): 159-165.

Lesser, M.P., J.C. Bythell, R.D. Gates, R.W. Johnstone & O. Guldberg-Hoegh. 2007. Are infectious diseases really killing corals? Alternative interpretations of the experimental and ecological data. J. Exp. Mar. Biol. Ecol., 346: 36-44.

Madigan, M.T., J.M. Martinko & J. Parker. 2003. Brock biology of microorganisms. Pearson Education, Upper Saddle River, 1019 pp.

Magoni, M. & C. Mesa-Munoz. 2018. Cambio climatico y olas de calor en Colombia. Posibles efectos y estrategias de adaptacion. In: A. Petrillo & P. Bellaviti (eds.). Desarrollo urbano sostenible y globalizacion. Investigacion para el desarrollo. Springer, Cham. doi: https://doi.org/10.1007/978-3-319-61988-0_27.

Mantilla-Galindo, M.A. 2015. Descripcion de la etiologia de las enfermedades coralinas presentes en Siderastrea siderea en el arrecife de Punta Cebolleta en Isla Fuerte, Caribe Colombiano. Pontificia Universidad Javeriana, Bogota, 80 pp.

Marulanda-Gomez, A., M. Lopez-Victoria & S. Zea. 2017. Current status of coral takeover by an encrusting excavating sponge in a Caribbean reef. Mar. Ecol., 38: 1-8.

May, L.A. & C.M. Woodley. 2016. Chemiluminescent method for quantifying DNA abasic lesions in scleractinian coral tissues. In: C.M. Woodley, C.A. Downs, A.W. Bruckner, J.W. Porter & S.B. Galloway (eds.). Diseases of coral. Wiley-Blackwell, Hoboken, pp. 547-555.

Maynard, J., R. Van Hooidonk, C.M. Eakin, M. Puotinen, M. Garren, G. Williams, S.F. Heron, J. Lamb, E. Weil, B. Willis & C.D. Harvell. 2015. Projections of climate conditions that increase coral disease susceptibility and pathogen abundance and virulence. Nat. Clim. Change, 5: 688-694.

Meyer, F.W., N. Vogel, K. Diele, A. Kunzmann, S. Uthicke & C. Wild. 2016. Effects of high dissolved inorganic and organic carbon availability on the physiology of the hard coral Acropora millepora from the Great Barrier Reef. PLoS One, 11(3): 1-18.

Miller, A.W. & L.L. Richardson. 2012. Fine structure analysis of black band disease (BBD) infected coral and coral exposed to the BBD toxins microcystin and sulfide. Invertebr. Pathol., 109(1): 27-33.

Myers, J.L., R. Sekar & L.L. Richardson. 2007. Molecular detection and ecological significance of the cyano-bacterial Genera Geitlerinema and Leptolyngbya in black band disease of corals. Appl. Environ. Microbiol., 73(16): 5173-5182.

Page, C.A., A. Croquer, C. Bastidas, S. Rodriguez, S.J. Neale, E. Weil & B.L. Willis. 2016. Halofilliculina ciliate infections on corals (Skeletal Eroding Disease). In: C.M. Woodley, C.A. Downs, A.W. Bruckner, J.W. Porter & S.B. Galloway (eds.). Diseases of coral. Wiley-Blackwell, Hoboken, pp. 361-375.

Peters, E.C. 2015. Diseases of coral reef organisms. In: C. Birkeland (ed.). Coral reefs in the Anthropocene. Springer, Netherlands, pp. 147-148.

Pinzon, J.H., J. Beach-Letendre, E. Weil & L.D. Mydlarz. 2014. Relationship between Phylogeny and immunity suggests older Caribbean coral lineages are more resistant to disease. PLoS One, 9(8): 1-13.

Puyana, M., A. Acosta, K. Bernal-Sotelo, T. Velasquez-Rodriguez & F. Ramos. 2015. Spatial scale of cyanobacterial blooms in Old Providence Island, Colombian Caribbean. Univ. Sci., 20(1): 83-105.

Rahman-Sunny, A. 2017. A review on effect of global climate change on seaweed and seagrass. Int. Fish. Aquat. Stud., 5(6): 19-22.

Ravindran, J. & C. Raghukumar. 2002. Pink Line Syndrome (PLS) in the scleractinian coral Porites lutea. Coral Reefs, 21(3): 252.

Ravindran, J. & C. Raghukumar. 2006. Pink-Line Syndrome, a physiological crisis in the scleractinian coral Porites lutea. Mar. Biol., 149: 347-356.

Ravindran, J., C. Raghkumar & B. Manikandan. 2016. Pink-Lyne Syndrome. In: C.M. Woodley, C.A. Downs, A.W. Bruckner, J.W. Porter & S.B. Galloway (eds.). Diseases of coral. Wiley-Blackwell, Hoboken, pp. 391-395.

Raymundo, L.J., C.D. Harvell & T.L. Reynolds. 2003. Porites ulcerative white spot disease: description, prevalence, and host range of a new coral disease affecting Indo-Pacific reefs. Dis. Aquat. Organ., 56: 95-104.

Ritchie, K.B. & G.W. Smith 1995. Preferential carbon utilization by surface bacterial communities from water mass, normal, and white-band diseased Acropora cervicornis. Mol. Mar. Biol. Biotechnol., 4: 345-352.

Rodriguez-Villalobos, J.C., L.E. Calderon-Aguilera & A. Rocha-Olivares. 2013. ?De que se enferman los corales? Cienc. Des., 39(263): 6-11.

Rosenberg, E. & A. Kushmaro. 2011. Microbial diseases of corals: pathology and ecology. In: Z. Dubinsky & N. Stambler (eds.). Coral Reefs: an ecosystem in transition. Springer, Dordrecht, pp. 451-464.

Ross, A.M. 2014. Genet and reef position effects in out-planting pf nursery-grown Acropora cervicornus (Scleractinia: Acroporidae) in Montego Bay, Jamaica. Rev. Biol. Trop., 62(3): 95-106.

Rutzler, K. & D.L. Santavy. 1983. The black band disease of Atlantic Reef Corals. Mar. Ecol., 4(4): 301-319.

Sassi, R., C.F. Costa-Sassi, K. Gorlach-Lira & W.K. Fitt. 2015. Pigmentation changes in Siderastrea spp. during bleaching events in the coastal reefs of northeastern Brazil. Lat. Am. J. Aquat. Res., 43(1): 176-185.

Sheridan, C., E. Kramarsky-Winter, M. Sweet, A. Kushmaro & L.M. Costa. 2013. Diseases in coral aquaculture: causes, implications, and preventions. Aquaculture, 396-399: 124-135.

Stal, L.J. 1995. Physiological ecology of cyanobacteria in microbial mats and other communities. New Phytol., 131: 1-32.

Sunagawa, S., T.Z. DeSantis, Y.M. Piceno, E-L. Brodie, M.K. DeSalvo, C.R. Voolstra, E. Weil, G.L. Andersen & M. Medina. 2009. Bacterial diversity and white plague disease associated community changes in the Caribbean coral Montastrea faveolata. ISME J., 3: 512-521.

Sutherland, P. & K. Ritchie. 2004. White pox disease of the Caribbean elkhorn coral, Acropora palmata. In: E. Rosenberg & Y. Loya (eds.). Coral health and disease. Springer-Verlag, Berlin, pp. 289-300. doi: https://doi. org/10.1007/978-3-662-06414-6_16.

Sutherland, K.P., S. Shaban, J.L. Joyner, J.W. Porter & E.K. Lipp. 2011. Human pathogen shown to cause disease in the threatened eklhorn coral Acropora palmata. PLoS One, 6(8): e23468. doi: 10.1371/ journal.pone.0023468.

Sweet, M. & J. Bythell. 2012. Ciliate and bacterial communities associated with white syndrome and brown band disease in reef-building corals. Environ. Microbiol., 14: 2184-2199.

Sweet, M., A. Ramsey & M. Bulling. 2017. Designer reefs and coral probiotics: great concepts but are they good practice? Biodiversity, 18: 19-22.

Vogel, N., F.W. Meyer, C. Wild & S. Uthicke. 2015. Decreased light availability can amplify negative impacts of ocean acidification on calcifying coral reef organisms. Mar. Ecol. Prog. Ser., 521: 49-61.

Ward, J.R., K.L. Rypien, J.F. Bruno, C.D. Harvell, E. Jordan-Dahlgren, K.M. Mullen, R.E. Rodriguez-Martinez, J. Sanchez & G. Smith. 2006. Coral diversity and disease in Mexico. Dis. Aquat. Organ., 69: 23-31.

Weil, E., G. Smith & D.L Gil-Agudelo. 2006. Status and progress in coral reef disease research. Dis. Aquat. Organ., 69: 1-7.

Willis, B.L., C.A. Page & E.A. Dinsdale. 2004. Coral disease in the Great Barrier Reef. In: E. Rosenberg. & Y. Loya (eds.). Coral health and disease. Springer-Verlag, Berlin. pp. 69-104.

Work, T.M. & E. Weil. 2016. Dark-Spots Disease. In: C.M. Woodley, C.A. Downs, A.W. Bruckner, J.W. Porter & S.B. Galloway (eds.). Diseases of coral. Wiley-Bnackwell, Hoboken, pp. 354-360.

Zamudio-Aleman, R.E., M.R. Castaneda-Chavez, F. Lango-Reynoso, I. Galaviz-Villa, I.A. Amaro-Espejo & L. Romero-Gonzalez. 2014. Metales pesados en sedimento marino del Parque Nacional Sistema Arrecifal Veracruzano. Rev. Iberoam. Cienc., 1(4): 159-168.

Zavala-Hidalgo, J., S. Morey & J. O'Brien. 2003. Seasonal circulation on the western shelf of the Gulf of Mexico using a high-resolution numerical model. J. Geophys. Res., 108(C12): 3389. doi: 10.1029/2003 JC001879.

Received: 10 October 2017; Accepted: 5 July 2018

Maria del Refugio Castaneda-Chavez (1), Fabiola Lango-Reynoso (1) Jose Luis Garcia-Fuentes (1) & Angel Roberto Reyes-Aguilar (1)

(1) Tecnologico Nacional de Mexico, Instituto Tecnologico de Boca del Rio Division de Estudios de Postgrado e Investigacion, Boca del Rio, Veracruz, Mexico

Corresponding author: Maria del Refugio Castaneda-Chavez (castanedaitboca@yahoo.com.mx)

Corresponding editor: Mauricio Laterca
Table 1. Pathogenic bacteria in scleractinian corals.

Pathogen                 Distribution      Affected corals

Halofolliculina          Caribbean Sea,    Acroporidae,
corallasia               Mexican           Agaricidae,
                         Caribbean, Red    Astrocoeniidae,
                         Sea               Faviidae,
                                           Meandrinidae,
                                           Poritidae

Oscillatoria sp.         Caribbean Sea,    Scleractinian and
                         Mexican           octocoral corals
                         Caribbean

Vibrio spp.              Caribbean Sea     Scleractinian and
                         Pacific Ocean     octocoral corals
                         Indian Ocean

Phormidium               Caribbean Sea     Scleractinian and
corallycticum            Pacific Ocean     octocoral corals

Phormidium               Indian Ocean      Porites lutea
valderianum

Aurantimonas             Caribbean Sea     Dichocoenia stokesi
oralicida

Helicostoma nonatum      Caribbean Sea

Serratia marcescens      Caribbean Sea     Acrocporidae

Pathogen                 Disease

Halofolliculina          Eroded skeletal
corallasia               band

Oscillatoria sp.         Black band disease

Vibrio spp.              Multiple diseases

Phormidium               Black Band Disease
corallycticum

Phormidium               Pink Line Disease
valderianum

Aurantimonas             White Plague Disease
oralicida

Helicostoma nonatum      Brown Band

Serratia marcescens      White Pox

Pathogen                 Reference

Halofolliculina          Croquer et al.
corallasia               (2005); Iyer (2016)

Oscillatoria sp.         Frias-Lopez et al.
                         (2003); Miller &
                         Richardson (2012);
                         Gavio et al. (2015).

Vibrio spp.              Kushmaro et al.
                         (1997); Rosenberg &
                         Kushmaro (2011);
                         Mantilla-Galindo
                         (2015); Kemp et al.
                         (2018).

Phormidium               Frias-Lopez et al.
corallycticum            (2003); Work & Weil
                         (2016).

Phormidium               Ravindran &
valderianum              Raghukumar (2002);
                         Mantilla-Galindo
                         (2015); Ravindran et
                         al. (2016).

Aurantimonas             Denner et al.
oralicida                (2003);  Gil-
                         Agudelo et al.
                         (2006); Bruckner,
                         2016.

Helicostoma nonatum

Serratia marcescens      Sutherland & Ritchie
                         (2004); Rodriguez-
                         Villalobos et al.
                         (2013).
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Author:Castaneda-Chavez, Maria del Refugio; Lango-Reynoso, Fabiola; Garcia-Fuentes, Jose Luis; Reyes-Aguila
Publication:Latin American Journal of Aquatic Research
Date:Nov 1, 2018
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