Temperature Related Mass Mortalities of Cyanobacteria-Harbouring Sponges: Could Symbiosis Breakdown be Responsible?

 

During recent decades, numerous mass mortality events involving sessile, epibenthic invertebrates of the temperate, Western Mediterranean Sea have been reported.  The geographical coverage and number of taxa involved in such events has varied, but a general, temperature related trend has been observed. Anomalously high temperatures have been reported as occurring simultaneously to (or on occasion previous to) mass mortality events.  Unfortunately, such observations have been difficult to examine thoroughly in the past, as mass mortality events are often difficult to quantify due to a lack of baseline, pre-event data.  However, proceeding extensive die-offs of shallow water sponge populations in two Marine Protected Areas (MPAs) of the Western Mediterranean Sea (Cabrera National Park (Cabrera NP) and Scandola Marine Reserve (Scandola MR)), quantitative assessments of sponge population status were already underway.  This circumstance provides the basis of an investigation reported by Cebrian et al. (2011).

Cebrian et al. (2011) conducted a comparative evaluation of the impact of two mortality events which occurred in consecutive summers (2008; 2009), focusing on two, phylogentically close species of keratose bacteriosponges, Ircinia fasciculata and Sarcotragus spinosulum.  I. fasciculata is known to harbour both heterotrophic bacteria and cyanobacteria, whereas S. spinosulum hosts the former, but not the latter.  The percentage of injured sponges (i.e. sponges displaying white pustules or areas of necrosis indicative to these mass mortality events), and sponge density, were recorded via randomised sampling conducted once at the beginning, and once at the end of summer (in July and October, respectively), from July 2007 to October 2010 in Cabrera NP, and from October 2008 to October 2010 in Scandola MR.  In situ Water-temperature was recorded hourly throughout these periods via autonomous sensors, facilitating calculation of the percentage of time sponges spent in temperatures above defined threshold values. 

In both MPAs, the percentage of injured I. fasciculata individuals was reported as having peaked in the Octobers of both 2008 and 2009, at 80-100% (of surveyed individuals).  Injured individuals did not exceed 30% during the other periods sampled.  This contrasted to the percentage of injured S. spinosulum individuals, which varied between 10-30% in both MPAs over the entire 2007-2010 period, with differences over time not being found as significant.  The authors also reported a dramatic decrease in I. fasciculata density in both MPAs, from a mean 7 (Cabrera NP) or 10 (Scandola RN) specimens per m² before the summer 2008 mortality event, to less than 1 specimen per m² at the end of autumn 2010.  Over the same time period, mean S. spinosulum densities in Cabrera NP decreased from 7 to 3 specimens per m², but density decreases in Scandola MR were not found to be significant.  Regression analyses between the percentages of time above maximum temperature thresholds (Cabrera NP: 26^oC; Scandola RN: 25^oC) during the summer period, and the percentage of injured I. fasciculata specimens, were positively correlated for each site (i.e. the greater percentage of summer time above a maximum threshold, the higher the impact on sponge populations).

The ultrastructure of healthy and injured tissue from a single I. fasciculata specimen was examined via Electron Transmission Microscopy.  Healthy tissue was observed as containing healthy cyanobacteria and heterotrophic ‘symbiotic’ bacteria.  In injured tissue, cyanobacteria were always degraded, and an unidentified, microorganism was frequently observed in cellular vacuoles of ‘disorganised’ choanocytes.  From these observations, the authors formed a working hypothesis: high temperatures may induce a breakdown of the cyanobacteria-sponge symbiosis present in I. fasciculata (potentially related to sponge mortality as cyanobacteria are thought to contribute to sponge carbon requirements).  The biological mechanism which might be involved in such a breakdown was then investigated via laboratory based experimentation.  The effect of temperature on the photosynthetic efficiency of Cyanobacteria harboured by I. fasciculate was estimated via measurement of chlorophyll florescence parameters (effective quantum yield and photosynthetic electron transfer).  I. fasciculata individuals were maintained in seawater at 16 ^oC (control), 23 ^oC (‘normal summer), and 26 ^oC (‘extreme summer’); Only I.  fasciculata individuals maintained at 26 ^oC showed significantly lower photosynthetic efficiencies (i.e. photosynthetic inhibition) than those in control conditions.

This paper particularly interested me due to both the subject matter (being previously unaware of a potential link between photosynthetic inhibition and symbiosis breakdown in sponges), and the logical progression of the investigation (from observation of correlated factors in the environment, through to experimental investigation of a potential mechanism for this correlation).  Cebrian et al. (2011) provide some convincing evidence for a relationship between the I. fasciculata mass mortalities observed in the summers of 2008 and 2009, and elevated temperatures.  However, much remains to be investigated regarding the mechanisms of such mass mortality events.  Although the authors provide some interesting ideas regarding a possible relationship between sponge mortality and the photoinhibition of symbiotic cyanobacteria, certain limitations regarding the experimental method indicate that further investigation into this theory is required. 

Unfortunately, the experiment undertaken appeared to suffer from pseudoreplicaiton (each temperature treatment was represented by a number of individuals in a single tank), and although Cebrian et al. (2011) discuss the probability of photoinhibition driven damage via the formation of reactive oxygen species (ROS), no investigations into such damage (e.g. antioxidant assays) were performed.  Similarly, although the TEM observations of heterotrophic bacteria particular to injured I. fasciculata tissues were attributed to an opportunistic spongin consumer, and the possibility of pathogen virulence/density increase with elevated temperatures speculated upon, no surveys of microbial diversity (e.g. DGGE analysis) were reported at any point.  Considering the importance of opportunistic pathogens and shifts in microbial populations in mass mortality events of other sessile invertebrates (e.g. corals; bivalves), this omission appears particularly problematic.  Nevertheless, Cebrian et al. (2011) have reported some interesting ideas on the potential role of temperature related I. fasciculata-Cyanobacteria symbiosis breakdown.  Further investigations including quantitative TEM studies of cyanobacteria density/condition in injured and recovered I. fasciculata tissues, antioxidant assays, and microbiota diversity surveys may assist the exploration of this theory.

 

Cebrian, E., Uriz, M. J., Garrabou, J. & Ballesteros, E. (2011).  Sponge mass mortalities in a warming Mediterranean Sea: are cyanobacteria-harboring species worse off? PloS one 6, e20211.

http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3105983&tool=pmcentrez&rendertype=abstract