Deep-sea bioluminescence blooms after dense water formation at the ocean surface

Abstract

The deep ocean is the largest and least known ecosystem on Earth. It hosts numerous pelagic organisms, most of which are able to emit light. Here we present a unique data set consisting of a 2.5-year long record of light emission by deep-sea pelagic organisms, measured from December 2007 to June 2010 at the ANTARES underwater neutrino telescope in the deep NW Mediterranean Sea, jointly with synchronous hydrological records. This is the longest continuous time-series of deep-sea bioluminescence ever recorded. Our record reveals several weeks long, seasonal bioluminescence blooms with light intensity up to two orders of magnitude higher than background values, which correlate to changes in the properties of deep waters. Such changes are triggered by the winter cooling and evaporation experienced by the upper ocean layer in the Gulf of Lion that leads to the formation and subsequent sinking of dense water through a process known as "open-sea convection". It episodically renews the deep water of the study area and conveys fresh organic matter that fuels the deep ecosystems. Luminous bacteria most likely are the main contributors to the observed deep-sea bioluminescence blooms. Our observations demonstrate a consistent and rapid connection between deep open-sea convection and bathypelagic biological activity, as expressed by bioluminescence. In a setting where dense water formation events are likely to decline under global warming scenarios enhancing ocean stratification, in situ observatories become essential as environmental sentinels for the monitoring and understanding of deep-sea ecosystem shifts.

Figure 1. Map of the NW Mediterranean Sea showing the location of the ANTARES, LION and Lacaze-Duthiers Canyon (LDC) sites (a) as well as the extension of open-sea convection area in the Gulf of Lion and beyond from 2008 to 2010 (b–d).

The boundaries of the convection area in winter 2008 (red in b), 2009 (blue in c) and 2010 (green in d) are derived from MODIS-Aqua satellite-based surface Chlorophyll-a concentration images. The limits of the convection area for each of the three successive winters correspond to their maximum extents during periods of deep water formation measured at the LION site (see Text S1 and Fig. S5). Black arrows indicate the direction of the two main continental winds leading to the cooling and subsequent sinking of surface waters: Mistral (M) and Tramontane (T). The grey arrow indicates the path of the cyclonic surface mesoscale Northern Current bordering the open-sea convection region.

Figure 2. Time series measured at the ANTARES IL07 mooring line.

(a) Median PMT counting rates (log scale), salinity, potential temperature and current speed from December 2007 to June 2010. Shading indicates periods (b) from January to June 2009 and (c) from January to June 2010, in which bioluminescence blooms were recorded. The lack of data from June 24 to September 6, 2008 is due to a cable technical failure.

Figure 3. Links between bioluminescence, current speed and the modification of the properties of the Western Mediterranean Deep Water (WMDW).

Box-and-whisker plot of median PMT counting rates (log scale) versus current speed classes for salinities higher (red) or lower (grey) than 38.479 for data recorded in (a) 2008, (b) 2009 and (c) between January and June 2010. The salinity threshold of 38.479 is used as a marker of the intrusion of newly formed deep water at the ANTARES site. While bioluminescence increases with current speed, it is also enhanced by the modification of WMDW (red box-plots). The top and bottom of each box-plot represent 75% (upper quartile) and 25% (lower quartile) of all values, respectively. The horizontal line is the median. The ends of the whiskers represent the 10^th and 90^th percentiles. Outliers are not represented. The statistical comparison between the two box-plots (red and grey) in each current class is given by the Kruskal-Wallis test: the observed difference between the two samples is significant beyond the 0.05 (*), the 0.01 (**) and the 0.001 (***) levels. The absence of an asterisk in some current classes indicates that the difference between the two box-plots is not significant. The number of measurements for salinity lower or higher than 38.479 is given in black or in red, respectively. Note the different scales of figures a, b and c.

Figure 4. Time series of oceanographic parameters measured at the Lacaze-Duthiers Canyon (LDC) and the open-sea convection region in the Gulf of Lion (LION) from January 2008 to June 2010.

(a) Potential temperature at 500 and 1,000 m depth at the LDC mooring site and (b) from various water depths at the LION site, jointly with (c) salinity at 2,300 m depth, (d) horizontal current speed and (e) vertical current speed from various water depths at the LION site. The four levels of temperature measurements at LION presented here are a sub-set of measurement depths (see Fig. S1). Essentially stable temperatures in the deepest layers in 2008 show that open-sea convection reached only 700 m and did not modify the deep water in the study area. In contrast, strong convection events, reaching 2,300 m depth, occurred during February-March 2009 and 2010 with an abrupt cooling of the upper water column and an increase in temperature and salinity in the deep layers. A concurrent increase in current speed was also noticed in winter 2009 and 2010. The 5-month long data gap in 2009 is due to a damaging of the mooring line during the April 2009 recovery, which induced a postponement of its redeployment to September 2009.