Greta S. Aeby

Comprehensive characterization of skeletal tissue growth anomalies of the finger coral Porites compressa

The scleractinian finger coral Porites compressa has been documented to develop raised growth anomalies of unknown origin, commonly referred to as “tumors”. These skeletal tissue anomalies (STAs) are circumscribed nodule-like areas of enlarged skeleton and tissue with fewer polyps and zooxanthellae than adjacent tissue. A field survey of the STA prevalence in Oahu, Kaneohe Bay, Hawaii, was complemented by laboratory analysis to reveal biochemical, histological and skeletal differences between anomalous and reference tissue. MutY, Hsp90a1, GRP75 and metallothionein, proteins known to be up-regulated in hyperplastic tissues, were over expressed in the STAs compared to adjacent normal-appearing and reference tissues. Histological analysis was further accompanied by elemental and micro-structural analyses of skeleton. Anomalous skeleton was of similar aragonite composition to adjacent skeleton but more porous as evidenced by an increased rate of vertical extension without thickening. Polyp structure was retained throughout the lesion, but abnormal polyps were hypertrophied, with increased mass of aboral tissue lining the skeleton, and thickened areas of skeletogenic calicoblastic epithelium along the basal floor. The latter were highly metabolically active and infiltrated with chromophore cells. These observations qualify the STAs as hyperplasia and are the first report in poritid corals of chromophore infiltration processes in active calicoblastic epithelium areas.

Predictive Modeling of Coral Disease Distribution within a Reef System

Diseases often display complex and distinct associations with their environment due to differences in etiology, modes of transmission between hosts, and the shifting balance between pathogen virulence and host resistance. Statistical modeling has been underutilized in coral disease research to explore the spatial patterns that result from this triad of interactions. We tested the hypotheses that: 1) coral diseases show distinct associations with multiple environmental factors, 2) incorporating interactions (synergistic collinearities) among environmental variables is important when predicting coral disease spatial patterns, and 3) modeling overall coral disease prevalence (the prevalence of multiple diseases as a single proportion value) will increase predictive error relative to modeling the same diseases independently. Four coral diseases: Porites growth anomalies (PorGA), Porites tissue loss (PorTL), Porites trematodiasis (PorTrem), and Montipora white syndrome (MWS), and their interactions with 17 predictor variables were modeled using boosted regression trees (BRT) within a reef system in Hawaii. Each disease showed distinct associations with the predictors. Environmental predictors showing the strongest overall associations with the coral diseases were both biotic and abiotic. PorGA was optimally predicted by a negative association with turbidity, PorTL and MWS by declines in butterflyfish and juvenile parrotfish abundance respectively, and PorTrem by a modal relationship with Porites host cover. Incorporating interactions among predictor variables contributed to the predictive power of our models, particularly for PorTrem. Combining diseases (using overall disease prevalence as the model response), led to an average six-fold increase in cross-validation predictive deviance over modeling the diseases individually. We therefore recommend coral diseases to be modeled separately, unless known to have etiologies that respond in a similar manner to particular environmental conditions. Predictive statistical modeling can help to increase our understanding of coral disease ecology worldwide.

Vibrio owensii induces the tissue loss disease Montipora white syndrome in the Hawaiian reef coral Montipora capitata.

Incidences of coral disease in the Indo-Pacific are increasing at an alarming rate. In particular, Montipora white syndrome, a tissue-loss disease found on corals throughout the Hawaiian archipelago, has the potential to degrade Hawaii’s reefs. To identify the etiologic agent of Montipora white syndrome, bacteria were isolated from a diseased fragment of Montipora capitata and used in a screen for virulent strains. A single isolate, designated strain OCN002, recreated disease signs in 53% of coral fragments in laboratory infection trials when added to a final concentration of 107 cells/ml of seawater. In addition to displaying similar signs of disease, diseased coral fragments from the field and those from infection trials both had a dramatic increase in the abundance of associated culturable bacteria, with those of the genus Vibiro well represented. Bacteria isolated from diseased fragments used in infection trails were shown to be descendants of the original OCN002 inocula based on both the presence of a plasmid introduced to genetically tag the strain and the sequence of a region of the OCN002 genome. In contrast, OCN002 was not re-isolated from fragments that were exposed to the strain but did not develop tissue loss. Sequencing of the rrsH gene, metabolic characterization, as well as multilocus sequence analysis indicated that OCN002 is a strain of the recently described species Vibrio owensii. This investigation of Montipora white syndrome recognizes V. owensii OCN002 as the first bacterial coral pathogen identified from Hawaii’s reefs and expands the range of bacteria known to cause disease in corals.

Growth Anomalies on the Coral Genera Acropora and Porites Are Strongly Associated with Host Density and Human Population Size across the Indo-Pacific

Growth anomalies (GAs) are common, tumor-like diseases that can cause significant morbidity and decreased fecundity in the major Indo-Pacific reef-building coral genera, Acropora and Porites. GAs are unusually tractable for testing hypotheses about drivers of coral disease because of their pan-Pacific distributions, relatively high occurrence, and unambiguous ease of identification. We modeled multiple disease-environment associations that may underlie the prevalence of Acropora growth anomalies (AGA) (n = 304 surveys) and Porites growth anomalies (PGA) (n = 602 surveys) from across the Indo-Pacific. Nine predictor variables were modeled, including coral host abundance, human population size, and sea surface temperature and ultra-violet radiation anomalies. Prevalence of both AGAs and PGAs were strongly host density-dependent. PGAs additionally showed strong positive associations with human population size. Although this association has been widely posited, this is one of the first broad-scale studies unambiguously linking a coral disease with human population size. These results emphasize that individual coral diseases can show relatively distinct patterns of association with environmental predictors, even in similar diseases (growth anomalies) found on different host genera (Acropora vs. Porites). As human densities and environmental degradation increase globally, the prevalence of coral diseases like PGAs could increase accordingly, halted only perhaps by declines in host density below thresholds required for disease establishment.

Phase shift from a coral to a corallimorph-dominated reef associated with a shipwreck on Palmyra atoll.

Coral reefs can undergo relatively rapid changes in the dominant biota, a phenomenon referred to as phase shift. Various reasons have been proposed to explain this phenomenon including increased human disturbance, pollution, or changes in coral reef biota that serve a major ecological function such as depletion of grazers. However, pinpointing the actual factors potentially responsible can be problematic. Here we show a phase shift from coral to the corallimorpharian Rhodactis howesii associated with a long line vessel that wrecked in 1991 on an isolated atoll (Palmyra) in the central Pacific Ocean. We documented high densities of R. howesii near the ship that progressively decreased with distance from the ship whereas R. howesii were rare to absent in other parts of the atoll. We also confirmed high densities of R. howesii around several buoys recently installed on the atoll in 2001. This is the first time that a phase shift on a coral reef has been unambiguously associated with man-made structures. This association was made, in part, because of the remoteness of Palmyra and its recent history of minimal human habitation or impact. Phase shifts can have long-term negative ramification for coral reefs, and eradication of organisms responsible for phase shifts in marine ecosystems can be difficult, particularly if such organisms cover a large area. The extensive R. howesii invasion and subsequent loss of coral reef habitat at Palmyra also highlights the importance of rapid removal of shipwrecks on corals reefs to mitigate the potential of reef overgrowth by invasives.

Patterns of Coral Disease across the Hawaiian Archipelago: Relating Disease to Environment

In Hawaii, coral reefs occur across a gradient of biological (host abundance), climatic (sea surface temperature anomalies) and anthropogenic conditions from the human-impacted reefs of the main Hawaiian Islands (MHI) to the pristine reefs of the northwestern Hawaiian Islands (NWHI). Coral disease surveys were conducted at 142 sites from across the Archipelago and disease patterns examined. Twelve diseases were recorded from three coral genera (Porites, Montipora, Acropora) with Porites having the highest prevalence. Porites growth anomalies (PorGAs) were significantly more prevalent within and indicative of reefs in the MHI and Porites trematodiasis (PorTrm) was significantly more prevalent within and indicative of reefs in the NWHI. Porites tissue loss syndrome (PorTLS) was also important in driving regional differences but that relationship was less clear. These results highlight the importance of understanding disease ecology when interpreting patterns of disease occurrence. PorTrm is caused by a parasitic flatworm that utilizes multiple hosts during its life cycle (fish, mollusk and coral). All three hosts must be present for the disease to occur and higher host abundance leads to higher disease prevalence. Thus, a high prevalence of PorTrm on Hawaiian reefs would be an indicator of a healthy coral reef ecosystem. In contrast, the high occurrence of PorGAs within the MHI suggests that PorGAs are related, directly or indirectly, to some environmental co-factor associated with increased human population sizes. Focusing on the three indicator diseases (PorGAs, PorTrm, PorTLS) we used statistical modeling to examine the underlying associations between disease prevalence and 14 different predictor variables (biotic and abiotic). All three diseases showed positive associations with host abundance and negative associations with thermal stress. The association with human population density differed among disease states with PorGAs showing a positive and PorTrm showing a negative association, but no significant explanatory power was offered for PorTLS.

2000-2002 Rapid Ecological Assessment of Corals (Anthozoa) on Shallow Reefs of the Northwestern Hawaiian Islands. Part 1: Species and Distribution

Rapid Ecological Assessment (REA) surveys at 465 sites on 11 reefs in the Northwestern Hawaiian Islands (NWHI) inventoried coral species, their relative abundances, and their distributions during 2000-2002. Surveys (462) around the 10 islands were in depths of a 20 m, and three surveys on the submerged Raita Bank were in depths of 30Ð35 m. Data from 401 REA sites met criteria for quantitative analysis. Results include 11 first records for stony coral species in the Hawaiian Archipelago and 29 range extensions to the NWHI. Several species may be new to science. There are now 57 stony coral species known in the shallow subtropical waters of the NWHI, similar to the 59 shallow and deep-water species known in the better-studied and more tropical main Hawaiian Islands. Coral endemism is high in the NWHI: 17 endemic species (30%) account for 37-53% of the abundance of stony corals on each reef of the NWHI. Three genera (Montipora, Porites, Pocillopora) contain 15 of the 17 endemic species and most of the endemic abundance. Seven Acropora species are now known from the central NWHI despite their near absence from the main Hawaiian Islands. Coral abundance and diversity are highest at the large, open atolls of the central NWHI (French Frigate, Maro, Lisianski) and decline gradually through the remaining atolls to the northwest (Pearl and Hermes, Midway, and Kure). Stony corals are also less abundant and less diverse off the exposed basalt islands to the southeast (Nihoa, Necker, La Perouse, Gardner), where soft corals (Sinularia, Palythoa) are more abundant. Exposure to severe wave action appears to limit coral development off these small islands and surrounding deep platforms. Temperature extremes and natural accumulation of lagoon sediments may contribute to decline of coral species and abundance at the northwestern end of the chain.

Disease dynamics of Montipora white syndrome within Kaneohe Bay, Oahu, Hawaii: distribution, seasonality, virulence, and transmissibility.

We report on an investigation of Montipora white syndrome (MWS), which is a coral disease reported from Hawaii, U.S.A., that results in tissue loss. Disease surveys of Montipora capitata within Kaneohe Bay (Oahu) found colonies that were affected by MWS on 9 reefs within 3 regions of Kaneohe Bay (south, central, north). Mean MWS prevalence ranged from 0.02 to 0.87% and average number of MWS cases per survey site ranged from 1 to 28 colonies. MWS prevalence and number of cases were significantly lower in the central region as compared to those in the north and south regions of Kaneohe Bay. There was a positive relationship between host abundance and MWS prevalence, and differences in host abundance between sites explained approximately 27% of the variation in MWS prevalence. Reefs in central Kaneohe Bay had lower M. capitata cover and lower MWS levels. MWS prevalence on reefs was neither significantly different between seasons (spring versus fall) nor among 57 tagged colonies that were monitored through time. MWS is a chronic and progressive disease causing M. capitata colonies to lose an average of 3.1% of live tissue mo(-1). Case fatality rate was 28% after 2 yr but recovery occurred in some colonies (32%). Manipulative experiments showed that the disease is acquired through direct contact. This is the first study to examine the dynamics of MWS within Hawaii, and our findings suggest that MWS has the potential to degrade Hawaiis reefs through time.

Pathology of tissue loss (white syndrome) in Acropora sp. corals from the Central Pacific

We performed histological examination of 69 samples of Acropora sp. manifesting different types of tissue loss (Acropora White Syndrome-AWS) from Hawaii, Johnston Atoll and American Samoa between 2002 and 2006. Gross lesions of tissue loss were observed and classified as diffuse acute, diffuse subacute, and focal to multifocal acute to subacute. Corals with acute tissue loss manifested microscopic evidence of necrosis sometimes associated with ciliates, helminths, fungi, algae, sponges, or cyanobacteria whereas those with subacute tissue loss manifested mainly wound repair. Gross lesions of AWS have multiple different changes at the microscopic level some of which involve various microorganisms and metazoa. Elucidating this disease will require, among other things, monitoring lesions over time to determine the pathogenesis of AWS and the potential role of tissue-associated microorganisms in the genesis of tissue loss. Attempts to experimentally induce AWS should include microscopic examination of tissues to ensure that potentially causative microorganisms associated with gross lesion are not overlooked.

Vibrio coralliilyticus Strain OCN008 Is an Etiological Agent of Acute Montipora White Syndrome

ABSTRACT Identification of a pathogen is a critical first step in the epidemiology and subsequent management of a disease. A limited number of pathogens have been identified for diseases contributing to the global decline of coral populations. Here we describe Vibrio coralliilyticus strain OCN008, which induces acute Montipora white syndrome (aMWS), a tissue loss disease responsible for substantial mortality of the coral Montipora capitata in Kāne‘ohe Bay, Hawai‘i. OCN008 was grown in pure culture, recreated signs of disease in experimentally infected corals, and could be recovered after infection. In addition, strains similar to OCN008 were isolated from diseased coral from the field but not from healthy M. capitata. OCN008 repeatedly induced the loss of healthy M. capitata tissue from fragments under laboratory conditions with a minimum infectious dose of between 107 and 108 CFU/ml of water. In contrast, Porites compressa was not infected by OCN008, indicating the host specificity of the pathogen. A decrease in water temperature from 27 to 23°C affected the time to disease onset, but the risk of infection was not significantly reduced. Temperature-dependent bleaching, which has been observed with the V. coralliilyticus type strain BAA-450, was not observed during infection with OCN008. A comparison of the OCN008 genome to the genomes of pathogenic V. coralliilyticus strains BAA-450 and P1 revealed similar virulence-associated genes and quorum-sensing systems. Despite this genetic similarity, infections of M. capitata by OCN008 do not follow the paradigm for V. coralliilyticus infections established by the type strain.