Exploring Individual- to Population-Level Impacts of Disease on Coral Reef Sponges: Using Spatial Analysis to Assess the Fate, Dynamics, and Transmission of Aplysina Red Band Syndrome (ARBS)

Abstract

BackgroundMarine diseases are of increasing concern for coral reef ecosystems, but often their causes, dynamics and impacts are unknown. The current study investigated the epidemiology of Aplysina Red Band Syndrome (ARBS), a disease affecting the Caribbean sponge Aplysina cauliformis, at both the individual and population levels. The fates of marked healthy and ARBS-infected sponges were examined over the course of a year. Population-level impacts and transmission mechanisms of ARBS were investigated by monitoring two populations of A. cauliformis over a three year period using digital photography and diver-collected data, and analyzing these data with GIS techniques of spatial analysis. In this study, three commonly used spatial statistics (Ripley’s K, Getis-Ord General G, and Moran’s Index) were compared to each other and with direct measurements of individual interactions using join-counts, to determine the ideal method for investigating disease dynamics and transmission mechanisms in this system. During the study period, Hurricane Irene directly impacted these populations, providing an opportunity to assess potential storm effects on A. cauliformis and ARBS.ResultsInfection with ARBS caused increased loss of healthy sponge tissue over time and a higher likelihood of individual mortality. Hurricane Irene had a dramatic effect on A. cauliformis populations by greatly reducing sponge biomass on the reef, especially among diseased individuals. Spatial analysis showed that direct contact between A. cauliformis individuals was the likely transmission mechanism for ARBS within a population, evidenced by a significantly higher number of contact-joins between diseased sponges compared to random. Of the spatial statistics compared, the Moran’s Index best represented true connections between diseased sponges in the survey area. This study showed that spatial analysis can be a powerful tool for investigating disease dynamics and transmission in a coral reef ecosystem.

Histological and ultrastructural features of Aplysina cauliformis affected by Aplysina red band syndrome

“…Increased disintegration of the thylakoid membranes of S. spongiarum, which would decrease the concentration of photosynthetic pigments, was observed in ARBS‐affected tissues, and this observation supports previous work that found reduced concentrations of chlorophyll a in ARBS‐affected individuals of A. cauliformis (Gochfeld, Easson, et al, ). This reduction in photopigments likely affects the sponge, which derives nutrients from this association, and may help to explain the slower growth and reduced biomass previously reported for ARBS‐affected sponges (Easson et al, ; Gochfeld, Easson, et al, ; Gochfeld, Kamel, et al, ).…”

“…To date, ARBS is the only Caribbean sponge disease shown to be readily transmissible (Olson et al, ). Long‐term monitoring of populations of A. cauliformis identified direct contact as the primary mode of disease transmission among these branching sponges (Easson et al, ), and this has been confirmed experimentally (Olson et al, ). Waterborne transmission occurs as well, although less rapidly (Easson et al, ; Olson et al, ).…”

“…Aplysina red band syndrome (ARBS) affects shallow–water branching sponges within the genus Aplysina (Verongida, Demospongiae) (Easson et al, ; Olson, Gochfeld, & Slattery, ). Aplysina cauliformis ( Carter 1882), which occurs widely across the Caribbean basin (Gochfeld, Schlöder, & Thacker, ; Loh & Pawlik, ; Thacker et al, ), is particularly susceptible.…”

“…ARBS has been found throughout the broader Caribbean basin, although its prevalence is highly variable among locations and even among sites within locations (Easson et al, ; Gochfeld et al, ; Olson et al, ). Reasons behind this variability are not yet understood.…”

“…Reasons behind this variability are not yet understood. Individuals of A. cauliformis affected by ARBS experience slower growth, reduced biomass and total protein content, changes in secondary metabolite profiles, and an increased probability of breakage during storms (Easson et al, ; Gochfeld, Easson, Freeman, Thacker, & Olson, ; Gochfeld, Kamel, Olson, & Thacker, ). However, in spite of extensive research on the impacts of ARBS at the individual and population levels, little is known about the pathogenesis of ARBS at the tissue or cellular level.…”