Abundance of some invertebrate species at Conero Promontory (NW Adriatic Sea) before, during and after the disease.

<p>Abundance of some invertebrate species at Conero Promontory (NW Adriatic Sea) before, during and after the disease.</p

Underwater pictures of different areas occupied by <i>Chondrosia reniformis</i> before, during and after the disease.

<p>A) Picture of a healthy individual of <i>C</i>. <i>reniformis</i> taken before the disease. B) During the disease, almost the total surface of <i>C</i>. <i>reniformis</i> showed necrotic areas characterized by white and putrefied tissues. C-D) Large areas visible in November 2013 after the detachment of dead <i>C</i>. <i>reniformis</i>; the rocky wall is covered with calcareous tubes of serpulids (C) and cirripeds (D). E-F) Recovery of the area after almost two years; the areas where <i>C</i>. <i>reniformis</i> was the dominant species (CrAs) were colonized by pioneer species such as the tubeworm <i>Spirobranchus triqueter</i> and the bryozoan <i>Schizobrachiella sanguinea</i> (E); the areas where <i>C</i>. <i>reniformis</i> was not the dominant species (OAs) were mainly occupied by cnidarians (cn), encrusting sponges (es) and the encrusting alga <i>Titanoderma</i> sp. (ea). Scale bars A-F 5 cm.</p

Mass Mortality Events in the NW Adriatic Sea: Phase Shift from Slow- to Fast-Growing Organisms

<div><p>Massive outbreaks are increasing all over the world, which are likely related to climate change. The North Adriatic Sea, a sub-basin of the Mediterranean Sea, is a shallow semi-closed sea receiving high nutrients inputs from important rivers. These inputs sustain the highest productive basin of the Mediterranean Sea. Moreover, this area shows a high number of endemisms probably due to the high diversity of environmental conditions and the conspicuous food availability. Here, we documented two massive mortalities (2009 and 2011) and the pattern of recovery of the affected biocoenoses in the next two years. Results show an impressive and fast shift of the benthic assemblage from a biocoenosis mainly composed of slow-growing and long-lived species to a biocoenosis dominated by fast-growing and short-lived species. The sponge <i>Chondrosia reniformis</i>, one of the key species of this assemblage, which had never been involved in previous massive mortality events in the Mediterranean Sea, reduced its coverage by 70%, and only few small specimens survived. All the damaged sponges, together with many associated organisms, were detached by rough-sea conditions, leaving large bare areas on the rocky wall. Almost three years after the disease, the survived specimens of <i>C</i>. <i>reniformis</i> did not increase significantly in size, while the bare areas were colonized by fast-growing species such as stoloniferans, hydrozoans, mussels, algae, serpulids and bryozoans. Cnidarians were more resilient than massive sponges since they quickly recovered in less than one month. In the study area, the last two outbreaks caused a reduction in the filtration efficiency of the local benthic assemblage by over 60%. The analysis of the times series of wave heights and temperature revealed that the conditions in summer 2011 were not so extreme as to justify severe mass mortality, suggesting the occurrence of other factors which triggered the disease. The long-term observations of a benthic assemblage in the NW Adriatic Sea allowed us to monitor its dynamics before, during and after the mortality event. The N Adriatic Sea responds quickly to climatic anomalies and other environmental stresses because of the reduced dimension of the basin. The long-term consequences of frequent mass mortality episodes in this area could promote the shift from biocoenoses dominated by slow-growing and long-lived species to assemblages dominated by plastic and short life cycle species.</p></div

Reduction of <i>Chondrosia reniformis</i> and Irciniidae/Spongiidae communities after the two disease events.

<p>Scheme illustrating a 0.5 x 0.5 m marked area subdivided in 9 sub-quadrats of 16.7 cm side in four different moments: before (June 2009) (A) and after (B) (October 2009) the first outbreak and after the second outbreak (November 2011 (C) and June 2013 (D)). The surfaces covered with <i>Chondrosia reniformis</i> and Irciniidae/Spongiidae were indicated in red and brown, respectively; numbers indicate the total cover of each species. Pictures E-F shows the central area of the quadrat (16.7 cm side) colonized by different assemblages in June 2009 (D) and June 2013 (D). Cr: <i>Chondrosia reniformis</i>, En: <i>Eupolymnia nebulosa</i>, Es: Encrusting sponges, Ms: <i>Microcosmus</i> sp., Pn: <i>Phallusia nigra</i>, IS: Irciniidae/Spongiidae, St: <i>Spirobranchus triqueter</i>, Sv: <i>Serpula vermicularis</i>. Figure F by F. Betti.</p

Duration of periods of calm sea and high temperature from 2000 to 2013.

<p>The years characterized by disease were showed in bold.</p><p>Duration of periods of calm sea and high temperature from 2000 to 2013.</p

Recovery of the study area.

<p>The bar charts show the comparison of the abundance of the most representative species before (June 2009) and after the disease (June 2013 and 2014) both in the areas where <i>C</i>. <i>reniformis</i> was the dominant species (CrAs) (A) and in the other areas (OAs) (B). C) Abundance of fauna associated to <i>C</i>. <i>reniformis</i> before (June 2009), immediately after (November 2011) and almost two years after the disease (June 2013).</p

Filtration rates of some species from the study area before and after the disease of 2009 and almost two years after the disease of 2011.

<p>*The sponge volume is calculated multiplying the average sponge surface (cm²) obtained by photo surveys by a thickness of 5 cm.</p><p>**Considered only big specimens of <i>C</i>. <i>reniformis</i></p><p>Filtration rates of some species from the study area before and after the disease of 2009 and almost two years after the disease of 2011.</p

Trend of weekly average values of wave height (m) and superficial temperature (°C) of 2011.

<p>The blue area indicates the prolonged period of calm sea conditions and high temperature (from June to the first week of October).</p

Average daily temperature from July to September of the years 2010–2012.

<p>The trend relative to the year with episodes of disease (2011) were showed by a continuous red line. Temperature kept high (≥23°C) throughout September.</p

Effects of the disease on some benthic species.

<p>A-B) Appearance of <i>Aplysina aerophoba</i> before (A) and during (B) the disease. C) The anemone <i>Aiptasia</i> sp. was contracted during the disease (C) but it appeared in healthy conditions about one month later (D). E-F) Colonies of <i>Eudendrium racemosum</i> lacking of polyps (E) and of <i>Cornularia cornucopiae</i> with contracted anthocodia (F). G) Hydroids completely recovered within a month from the disease (picture G by F. Betti). Scale bars A-F 5 cm, G 10 cm.</p