Global Change Biology (2012), doi: 10.1111/gcb.12019
Caribbean coral diseases: primary transmission or secondary infection? E R I N N M . M U L L E R * † and R O B E R T V A N W O E S I K † *Mote Marine Laboratory, 1600 Ken Thompson Parkway, Sarasota, FL 34236, USA, †Department of Biological Sciences, Florida Institute of Technology, 150 West University Blvd, Melbourne, FL 32901, USA
Abstract Over the last 40 years, disease outbreaks have significantly reduced coral populations throughout the Caribbean. Most coral-disease models assume that coral diseases are contagious and that pathogens are transmitted from infected to susceptible hosts. However, this assumption has not been rigorously tested. We used spatial epidemiology to examine disease clustering, at scales ranging from meters to tens of kilometers, to determine whether three of the most common Caribbean coral diseases, (i) yellow-band disease, (ii) dark-spot syndrome, and (iii) white-plague disease, were spatially clustered. For all three diseases, we found no consistent evidence of disease clustering and, therefore, these diseases did not follow a contagious-disease model. We suggest that the expression of some coral diseases is instead a two-step process. First, environmental thresholds are exceeded. Second, these environmental conditions either weaken the corals, which are then more susceptible to infection, or the conditions increase the virulence or abundance of pathogens. Exceeding such environmental thresholds will most likely become increasingly common in rapidly warming oceans, leading to more frequent coral-disease outbreaks. Keywords: coral diseases, coral reefs, infectious-disease dynamics, Montastraea annularis, Siderastrea siderea, spatial epidemiology Received 13 June 2012; revised version received 23 August 2012 and accepted 24 August 2012
Introduction The Caribbean is a hotspot for coral diseases. Over 66% of the world’s coral diseases occur within this region, although it only supports 8% of the world’s coral reefs (Green & Bruckner, 2000). Coral diseases are arguably the main cause of the recent decline in Caribbean corals. Although researchers have been studying coral diseases for several decades, most studies have focused on identifying the particular pathogens that cause disease. Laboratory experiments have shown that many coral diseases are infectious, but of the 18 diseases described in the Caribbean, only four studies have fulfilled Koch’s postulates (Smith et al., 1996; Patterson et al., 2002; Denner et al., 2003; Cervino et al., 2004; Table 1). There are limitations to the application of Koch’s postulates in the marine environment, primarily because of the requirement to grow potential pathogens in pure culture, which eliminates most marine viruses, protozoa, fungi and bacteria (Ritchie et al., 2001). In addition, it is difficult to determine the causative agent of a disease, such as black-band disease, which requires a consortium of bacteria (Richardson, 2004). However, identifying causative agents and understanding the mechanisms that drive coral-disease dynamics is essential for predicting,
Correspondence: Erinn M. Muller, tel. + 941 388 4441, fax + 941 388 4312, e-mail:
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© 2012 Blackwell Publishing Ltd
and thus possibly reducing, the occurrence of coraldisease outbreaks in the future. Currently, several coral-disease models are governed by transmission parameters that transfer individual corals from the susceptible population to the infected population (Sokolow et al., 2009; Yakob & Mumby, 2011; but see Jorda´n-Garza et al., 2011). The inclusion of transmission parameters within models follows the assumption that an infectious coral disease is also contagious. Infectious diseases result from the presence and activity of microbial agents, such as bacteria, protozoans, fungi, or viruses, whereas contagious diseases are infectious diseases that are also transmissible through indirect or direct contact (Stedman, 1976). Infectious diseases, however, are not always contagious. If coral diseases are contagious, transmission on contemporary reefs, with low coral-colony densities, most likely occurs through indirect contact via water-borne or vector transmission. Direct physical contact among individual colonies is limited on many present-day reefs, especially within the Caribbean where some reefs only support 2% coral cover (Gardner et al., 2003). Richardson et al. (1998) and Aeby & Santavy (2006) both tested the possibility of water-borne transmission of coral diseases, commonly found within the Caribbean, using laboratory manipulations. Indirect transmission of white-plague disease type II was documented on colonies of Dichocoenia stokesi, suggesting a water-borne pathogen (Richardson et al., 1998). By contrast, indirect 1
2 E. M. MULLER & R.
VAN
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Table 1 Commonly reported Caribbean hard-coral and octocoral diseases, highlighting whether Koch’s postulates have been fulfilled for the disease and the pathogen identified, where ’?’ indicates unknown pathogen
Disease
Fulfillment of Koch’s postulates (reference)
Aspergillosis
Yes (Smith et al., 1996)
Black band
No*
Caribbean ciliate infection Dark-spot syndrome Growth anomalies Pigmentation response Red band Sea fan purple spots Shutdown reaction Ulcerative white spots White band type I White band type II White plague type I White plague type II
No†
White plague type III White pox White syndromes Yellow band
Pathogen
No No No
Aspergillis sydowii A bacterial consortium Halofaliculina spp. ? ? ?
No No No No
? ? ? ?
No No‡ No Yes (Denner et al., 2003) No Yes (Patterson et al., 2002) No Yes (Cervino et al., 2004)
? Vibrio harveyi ? Aurantimonas coralicida ? Serratia marcescens ? Vibrio spp.
*Several bacteria are required for the formation of black-band disease and, therefore, will never complete Koch’s postulates. †This disease is identified by the presence of the ciliate Halofaliculina spp., but Koch’s postulates have not been fulfilled (Croquer et al., 2006). ‡Only three of the four Koch’s postulates have been fulfilled (Gil-Agudelo et al., 2006).
water-borne transmission of black-band disease did not occur unless susceptible individuals had open wounds (Aeby & Santavy, 2006). Laboratory manipulations have successfully transmitted yellow-band disease across coral colonies in direct contact with each other (Weil et al., 2009), but in situ manipulations did not transmit yellow-band disease across colonies (Jorda´nGarza & Jorda´n-Dahlgren, 2011). An alternative to laboratory and field manipulations is the use of spatial epidemiology. Spatial epidemiology examines whether diseased individuals consistently show a clustered pattern. A contagious mode of transmission is likely if diseased individuals are consistently more clustered than the null distribution of clustered individuals. If diseased individuals are not clustered,
then the disease is probably not contagious. Disease mapping has been used since the outbreak of cholera in London in 1854 (Snow, 1854). Although cholera is rarely spread from person to person, the clustered distribution of infected individuals identified the source of the pathogen – a contaminated water pump. However, spatial epidemiology has had limited applications within the marine environment and most of those studies have been spatially limited. For example, Jolles et al. (Jolles et al., 2002) examined the fungal disease aspergillosis on sea fans in 200 m2 quadrats on three reefs in the Florida Keys, and found the disease clustered in only one of those quadrats. Zvuloni et al. (Zvuloni et al., 2009) examined a 100 m2 site in Eilat, Israel, and showed that clustering of black-band disease only occurred during warm months. By contrast, Foley et al. (Foley et al., 2005) found no clustering of colonies with yellow-band disease on four, 360 m2 transects in Akumal, Mexico. Recently, Lentz et al. (Lentz et al., 2011) found that levels of clustering of white-band disease differed depending on whether transect or colony level data were used in their analysis. Most previous studies have only focused on relatively small spatial scales (i.e., tens of meters). The present Caribbean study was undertaken at three locations (St. Croix and St. John, United States Virgin Islands, and La Parguera, Puerto Rico), to examine the spatial patterns (from meters to tens of kilometers), of three Caribbean coral diseases. We examined a total reef area of 25 300 m2. Our objective was to determine whether yellow-band disease, dark-spot syndrome, and whiteplague disease clustered, and therefore followed a contagious-disease model.
Materials and methods A hierarchical sampling design was used to determine the clustering pattern of diseases over two spatial scales (m and km) at 253, 100 m2 sites in the US Virgin Islands (USVI) and Puerto Rico (PR). A geo-referenced habitat map of each of the three locations – St. Croix and St. John (USVI), and La Parguera (PR) – was used to stratify the sampling design by habitat type. Within each location, the domain of interest (hard-bottom habitat) was defined using ArcView 9.2® Global Information System software (Environmental Systems Resource Institute, 2009. ArcView 9.2. ESRI Redlands, CA, USA) and National Oceanic and Atmospheric Administration (NOAA) habitat maps (http://ccma.nos.noaa.gov/products/biogeography/ benthic/data/). Within the hard-bottom habitat, random waypoints were generated to provide the latitude and longitude of each site. A site consisted of a single 10 9 10 m quadrat located at each randomly generated waypoint. According to previously published studies, a 10 9 10 m quadrat was large enough to capture coral-disease clusters (Jolles et al., 2002; Zvuloni et al., 2009). Each location was surveyed twice, with a similar number of sites (n) surveyed each sampling period.
© 2012 Blackwell Publishing Ltd, Global Change Biology, doi: 10.1111/gcb.12019
CORAL DISEASES DO NOT CLUSTER 3 St. Croix (USVI) was surveyed both in March 2009 (n = 49) and October 2009 (n = 43), St. John (USVI) was surveyed both in July 2009 (n = 53) and July 2010 (n = 41), and La Parguera (PR) was surveyed both in August 2009 (n = 44) and August 2010 (n = 33). The majority of the surveys took place in midsummer, when coral disease was believed to be most prevalent, and to avoid potential seasonal variation. All data for each sampling period were recorded within a 2-week window. The surveys quantified the proportion of all sites with disease within each location, and prevalence of each disease was measured as the proportion of the susceptible coral population showing signs of disease. The three most common diseases found within each location were yellow-band disease, darkspot syndrome, and white-plague disease. Several other diseases were observed, but had such low prevalence that they were not included in this study. Still photographs of the benthic community were taken at each site using a Sony Cybershot camera (7 megapixels) held on a polyvinyl carbon frame fixed approximately 1.5 m from the substrate. Each photograph captured about 1 m2 of the substrate. There were approximately 120 photos taken per 100 m2 site, which incorporated some overlap. The still images were stitched together using Canon Photostich® (Tokyo, Japan), to create a mosaic of each site. Coral diseases were identified in situ. Yellow-band disease only affected colonies of the Montastraea annularis spp. complex, and darkspot syndrome only affected Siderastrea siderea colonies. Although white-plague disease is known to affect several species of corals, our study only focused on white-plague disease affecting S. siderea because it was most often observed on this coral species. Progression rates are needed to differentiate between the three different ‘types’ of whiteplague disease. However, our study did not follow individual colonies over time and the progression rates could not be determined. Therefore, colonies that suffered tissue loss similar to that described for white-plague disease were lumped into one ‘white-plague disease’ category. If disease was found within a site, every individual colony of Montastraea annularis spp. complex or Siderastrea siderea (>4 cm: the visual size limit from the photographs), depending on the type of disease present, was outlined using Coral Point Count (CPCe) software (Kohler & Gill 2006). Within each site, all colonies of M. annularis spp. complex were outlined if at least one colony of this species complex showed signs of yellow-band disease, whereas colonies of S. siderea were outlined if dark-spot syndrome or white-plague disease was observed. Colonies were not outlined if only healthy individuals were observed within a site. After completing the mosaic and outlining the necessary corals, a grid was placed over the photomosaic quadrat, and the location of each colony within the quadrat was identified. This procedure provided a map of every colony within each 100 m2 site. The presence or absence of disease was also recorded for each mapped colony. The spatial distribution of sites with coral disease was analyzed using the Ripley’s function, K(r), which was defined as the expected number of sites within a distance (r) from an arbitrary site (Ripley, 1981). All analyses were conducted using the Spatstat package (Baddeley & Turner, 2005) in the
program R (R Development Core Team, 2011, version 2.15). Ripley’s K was calculated as: n n X X Ir dij ^ ðrÞ ¼ A K ; n2 i¼1 j¼1;j6¼1 wij where A was the total area of the location, n was the number of sites, and dij was the distance between any two sites i and j. Ir(dij) indicated whether there was a site within distance r from site i. Therefore, Ir(dij) had a value of 1 if dij
