Mass mortality of marine invertebrates in the NW Mediterranean (Summer 1999)

Paramuricea clavata was one the most affected species. Here injuries are important, the necrosis rate is higher than 70%. Photo: J.G. Harmelin.

Eunicella singularis has been severely affected. Several weeks after the break-up, the bare axial skeleton is colonised by macroscopic pioneer taxa such as hydroids, bryozoans, serpulid polychaetes and algae. Photo: J.G. Harmelin.

The commercial species Spongia officinalis. The first sign of mortality observed was a white bacterial veil on the epidermis. Soon after, the areas under the bacterial layer appeared rotten and death occurred within two days. Skeletons of dead specimens remained attached to the rocks and were eventually detached by storms. Photo: J.G. Harmelin.

Numerous cases of bleaching of the scleractinian coral Cladocora caespitosa, resulting in the total or partial death of colonies, were also observed. Photo: J.G. Harmelin.

Temperature stress has been recognised as a main factor in the development of marine diseases that seem to be increasing around the world (Peters, 1993, Harvell et al., 1999). Among the most severe events recorded, a mass mortality occurred in the NW Mediterranean in summer 1999 (Perez et al., 2000; Cerrano et al., 2000). The area affected stretches from Elba Island in Italy to the Bay of Marseilles in France. All other NW Mediterranean regions appeared to have been spared by this event. However, cases of mortality, apparently similar to those described here, have been reported to us in August and September 1999 in Tunisia, Greece, Morocco, Cyprus and Turkey. A possible link between these observations and the event recorded in France and Italy has not yet been established.

The incidence and the virulence of this mortality event were surveyed by SCUBA diving between September 1999 and March 2000, both by scientists and by recreational divers under the supervision of scientists. In general, each survey was carried out from the surface to a maximum depth of 60 m. The species affected were noted as well as their degree of necrosis and some environmental parameters: depth range, type of substratum and orientation to the main currents. Surveys were conducted with the help of amateur divers previously trained, their observations being submitted to quality control whenever considered necessary. Interviews with diving club officers also allowed gathering information on the date of first appearance of mortality signs for different species and localities.

The species affected

All species affected dwell in rocky habitats and several of them are prominent components of the infralittoral and circalittoral communities (photophylic algae assemblages, coralligenous and semi-obscure caves). This event appears to be the largest mass mortality event ever recorded in the Mediterranean with respect to (i) the large geographic area concerned, (ii) the great diversity of taxa affected: sponges, cnidarians, bivalves, ascidians and bryozoans, and (iii) the high mortality rates observed. Twenty eight species of marine invertebrates have been observed to be involved in the 1999 mass mortality event. The most affected taxa were sponges and cnidarians. Among sponges, the keratose species (with spongin fibre skeletons) were the most damaged. Commercial sponges from the genera Spongia and Hippospongia were dramatically affected in most of the area concerned with mortality rates reaching 75% in some places (Perez, 2001)

Among cnidarians, the gorgonians suffered spectacular and extensive damages. In the most affected species, the gorgonians Paramuricea clavata and Eunicella singularis, the mortality rate reaching 90% in some sites (Sartoretto et al., in prep). Extensive injuries of the red coral Corallium rubrum and numerous cases of bleaching of the scleractinian Cladocora caespitosa, resulting in the total or partial death of colonies, were also observed in shallow waters (above 30m) (Perez et al., 2000; Garrabou et al., 2001). Abnormal recent death among bivalve molluscs (Lima lima and Neopycnodonte cochlear) and solitary tunicates (Microcosmus spp., Pyura dura and Halocynthia papillosa) was indicated by empty valves and tunics still attached to the substrate or accumulated on the bottom. Finally, it was noted that fouling rate showed a significant increase on three branched bryozoan species (e.g. Adeonella calveti, Myriapora truncata, Pentapora fascialis, Turbicellepora avicularis).

Causes of mortality

There is to date no clear explanation about the cause(s) of this mortality event. However, there is clear evidence that this mass mortality took place under an unusual environmental context characterised by high and stable water column temperatures (Romano et al. 2000; Perez et al. 2000; Cerrano et al., 2000). Indeed, the thermal structure of the water column was remarkable, displaying a general warming of 2-3°C in the surface (above thermocline) water layers, while the thermocline went down to 40m (Romano et al, 2000; Cerrano et al., 2000). In such conditions, the impacted invertebrates have probably been exposed to temperatures near to or beyond their thermal tolerance, the exposure time having lethal consequences either directly, leading to physiological stress, and/or indirectly by triggering the virulence of pathogens (Perez et al., 2000; Perez, 2001). The hypothesis that temperature played a key role in this event is supported by the remarkable decrease in the rate of injuries with depth (no signs of mortality having been recorded below 45 m), and by changes in the levels of expression of heat shock proteins in sponges (Garrabou et al., 2001; Perez, 2001, Sartoretto et al., in prep.).

Recovery not certain

The recovery of impacted populations may be uncertain since most of the affected species are characterised by slow dynamics: low growth, recruitment and death rates. For instance, it will take decades for gorgonian or sponge populations to fully recover, and worse this might fail in case of new outbreaks occurring in the area. This catastrophic scenario is not unlikely since many biological indicators point to a global warming of the NW Mediterranean (species migration and distribution, life-history shifts and increases of disturbance rates) (see for example Francour et al., 1994). Moreover, climatic models foresee a significant increment of temperature and significant changes in extreme climatic events frequency for the next decades in the NW Mediterranean area (Parry et al. 2000). Since the Mediterranean harbours 4 to 18 % of total marine biodiversity over only 0.82% of oceanic surface (Bianchi & Morri 2000), potential effects of global change in that particular area could have dramatic consequences for the conservation of marine diversity as a whole. These threats warrant a concerted effort to help understand past and future effects of global change on marine Mediterranean biodiversity.

Some references

Bianchi, N & Morri, C (2000): Marine biodiversity of the Mediterranean Sea: situation, problems and prospects for future research. Mar. Pollut. Bull. 40, 367-376.

Cerrano, C., Bavestrello, G., Bianchi, C.N., Cattaneo-Vietti, R., Bava, S., Morganti, C., Morri, C., Picco, P., Sara, G., Schiaparelli, S., Siccardi, A., & Sponga, F. (2000): A Catastrophic Mass-mortality Episode of Gorgonians and Other Organisms in the Ligurian Sea (North-western Mediterranean), Summer 1999. Ecology Letters 3, 284-293.

Garrabou, J., Perez, T., Sartoretto, S., & Harmelin, J.G. (2001): Mass mortality event in red coral (Corallium rubrum, Cnidaria, Anthozoa, Octocorallia) population in the Provence region (France, NW Mediterranean). Mar. Ecol. Prog. Ser. 217, 263-272.

Francour, P., Boudouresque, CF., Harmelin, JG., Harmelin-Vivien, ML., & Quignard, JP., (1994). Are the Mediterranean waters becoming warmer? Information from biological indicators. Mar. Pollut. Bull., 28(9): 523-526.

Harvell, C.D., Kim, K., Burkholder, J.M., Colwell, R.R., Epstein, P.R., Grimes, D.J., Hofmann, E.E., Lipp, E.K., Osterhaus, A.D.M.E., Overstreet, R.M., Porter, J.W., Smith, G.W., & Vasta, G.R. (1999): Emerging marine diseases - Climate links and anthropogenic factors. Science 285, 1505-1510.

Parry, M.L (Ed.) (2000): Assessment of potential effects and adaptations for climate change in Europe: the Europe ACACIA project. Jackson Environment Institute, University of East Anglia, Norwich. 320 pages.

Perez, T. (2001): Qualité de l'environnement marin littoral: étude des spongiaires pour la bioévaluation des peuplements de substrats durs. Doctorat Thesis, Université de la Méditerranée, Centre d'Océanologie de Marseille. 229 p.

Perez, T., Garrabou, J., Sartoretto, S., Harmelin, J.G., Francour, P., & Vacelet, J (2000): Mortalité massive d'invertébrés marins: un événement sans précédent en Méditerranée nord-occidentale - Mass mortality of marine invertebrates: an unprecedented event in the NW Mediterranean. C. R. Acad. Sci. Paris, III 323, 853-865.

Peters, E.C. (1993): Disease of other invertebrate phyla: Porifera, Cnidaria, Ctenophora, Annelida, Echinodermata. In: Pathobiology of Marine and Estuarine Organisms. (Eds: Couch, John A. & Fournie, John W) CRC Press, Boca Raton, 393-449.

Romano, J.C., Bensoussan, N., Younes, W.A.N., & Arlhac, D (2000): Anomalies thermiques dans les eaux du golfe de Marseille durant l'été 1999. Une explication partielle de la mortalité d'invertébrés fixés. C. R. Acad. Sci. Paris, III 323, 415-427.