Sponge mass mortalities in a warming Mediterranean Sea: are cyanobacteria-harboring species worse off?

Abstract

Mass mortality events are increasing dramatically in all coastal marine environments. Determining the underlying causes of mass mortality events has proven difficult in the past because of the lack of prior quantitative data on populations and environmental variables. Four-year surveys of two shallow-water sponge species, Ircinia fasciculata and Sarcotragus spinosulum, were carried out in the western Mediterranean Sea. These surveys provided evidence of two severe sponge die-offs (total mortality ranging from 80 to 95% of specimens) occurring in the summers of 2008 and 2009. These events primarily affected I. fasciculata, which hosts both phototrophic and heterotrophic microsymbionts, while they did not affect S. spinosulum, which harbors only heterotrophic bacteria. We observed a significant positive correlation between the percentage of injured I. fasciculata specimens and exposure time to elevated temperature conditions in all populations, suggesting a key role of temperature in triggering mortality events. A comparative ultrastructural study of injured and healthy I. fasciculata specimens showed that cyanobacteria disappeared from injured specimens, which suggests that cyanobacterial decay could be involved in I. fasciculata mortality. A laboratory experiment confirmed that the cyanobacteria harbored by I. fasciculata displayed a significant reduction in photosynthetic efficiency in the highest temperature treatment. The sponge disease reported here led to a severe decrease in the abundance of the surveyed populations. It represents one of the most dramatic mass mortality events to date in the Mediterranean Sea.

Figure 1. The western Mediterranean Sea, showing the surveyed localities of Ircinia fasciculata.

Figure 2. Aspects of Ircinia fasciculata mortality.

a) First stage of the affectation on I. fasciculata (arrow head) compared with healthy S. spinosulum (arrow), b) small whitish spots on the I. fasciculata surface, c) completely dead I. fasciculata with the skeleton (spongin network) free of cellular material, (d) white bacterial veil on unhealthy Sarcotragus spinosulum surface.

Figure 3. Several ultrastructural aspects of a healthy Ircinia fasciculata.

A) Archeocyte of a subectosomal zone, surrounded by numerous cyanobacteria (c) and some heterotrophic bacteria (h); B) Detail of a healthy cyanobacteria, close to an archeocyte plenty of glycogen rosettes (g); C) “symbiotic” bacterial community, typically found in the sponge; D) collagen layer (co) between endopinacocytes (pi) separating two choanocyte chambers (ch: choanocytes); E) collagen bundles, surrounded by endopinacocytes (pi); F) basal section of a choanocyte, full of heterogeneous phagosomes (ph), which is characteristic of the species (n: nucleus).

Figure 4. Several ultrastructural aspects of unhealthy specimens of Ircinia fasciculata.

A, B, C) Zone in the vicinity of a pustule (whitish spot): A) cyanobacteria under several degradation stages; B) section of a degenerating choanocyte chamber with multiple phagosomes (ph) and an unknown microorganism (mi); C) closer view of the “rare” microorganism, which divides within cell vacuoles (a) and shows a membrane complex (arrows) and an irregular, dark inner zone; D, E, F). Zone corresponding to a pustule (died whitish spot): D) completely degenerated cells with multiple released vesicles (v); E) Abundant foreign bacteria (fb), similar to the morphotype reported to consume on the skeleton of dead sponges (Vacelet et al. 1994), among completely degenerated sponge cells (sc); F) Close view of this particular bacterium, which is always associated to the collagen bundles (cb).

Figure 5. Mean percentages of injured Ircinia fasciculata (a) and Sarcotragus spinosulum (b) specimens recorded in Cabrera NP (circles) and Scandola RN (triangles) during the monitoring period.

Bars represent standard errors. Mean concentrations, which were not significantly different in a Tukey test, are joined by horizontal lines.

Figure 6. Mean densities of Ircinia fasciculata (a) and Sarcotragus spinosulum (b) recorded in Cabrera NP (circles, C) and Scandola RN (triangles, S) during the monitoring period.

Bars represent standard errors. Mean concentrations, which were not significantly different in a Tukey test, are joined by horizontal lines. N =  number of specimens sampled.

Figure 7. Percentage of the summer period with temperatures above 23°C, 24°C, 25°C and 26°C in Cabrera NP (a) and above 23°C, 24°C and 25°C in Scandola RN (b).

Data from SOMLIT (temperature sensors) data series.

Figure 8. Relationship between the percentage of time above a temperature threshold (26°C) from August 1 to September 30 and the percentage of affected I. fasciculata colonies in Cabrera NP.

Figure 9. The effective quantum yield (Φ_PSII) and photosynthetic electron transfer (ETR) during the experiment for the "control,” “medium” and “extreme” treatments.

Bars represent standard errors.