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

Cebrian E, Uriz MJ, Garrabou J, Ballesteros E - PLoS ONE (2011)

Bottom Line: 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.

View Article: PubMed Central - PubMed

Affiliation: Universitat de Girona, Facultat de Ciències, Departament de Ciències Ambientals, Girona, Spain. emma.cebrian@udg.edu

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.

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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).
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pone-0020211-g004: 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).

Mentions: The sponge tissue in close vicinity to the necrotic zones contained both choanocytes and archeocytes, plenty of phagocytosed cell debris, and empty vesicles. The cell nuclei were irregular in shape, with a poorly defined nuclear membrane. Cyanobacteria were always degraded, showing a cell volume that was twice to three times the volume of normal cyanobacteria (Fig. 4 a, b). Collagen fibrils were equally abundant in affected and healthy tissue although showed a poorer organization in the former (Fig. 4f). A non-identified microorganism, with a multilayered membrane was quite frequent in cellular vacuoles of disorganized choanocytes, where it divided (Fig. 4c). However, it could not be related unambiguously to the disease.


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

Cebrian E, Uriz MJ, Garrabou J, Ballesteros E - PLoS ONE (2011)

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).
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3105983&req=5

pone-0020211-g004: 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).
Mentions: The sponge tissue in close vicinity to the necrotic zones contained both choanocytes and archeocytes, plenty of phagocytosed cell debris, and empty vesicles. The cell nuclei were irregular in shape, with a poorly defined nuclear membrane. Cyanobacteria were always degraded, showing a cell volume that was twice to three times the volume of normal cyanobacteria (Fig. 4 a, b). Collagen fibrils were equally abundant in affected and healthy tissue although showed a poorer organization in the former (Fig. 4f). A non-identified microorganism, with a multilayered membrane was quite frequent in cellular vacuoles of disorganized choanocytes, where it divided (Fig. 4c). However, it could not be related unambiguously to the disease.

Bottom Line: 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.

View Article: PubMed Central - PubMed

Affiliation: Universitat de Girona, Facultat de Ciències, Departament de Ciències Ambientals, Girona, Spain. emma.cebrian@udg.edu

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.

Show MeSH
Related in: MedlinePlus