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Relation between deep bioluminescence and oceanographic variables: A statistical analysis using time-frequency decompositions

Authors:
séverine Martini at Institut Méditerranéen d’océanologie
séverine Martini
David Nerini at Aix-Marseille University
David Nerini
Christian Tamburini at French National Centre for Scientific Research
Christian Tamburini
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d(t)
m(t)
d(t)
C(t)
X(t)C(t)X(t)
(i)
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Upper envelope
Data
Mean envelope
Lower envelope
Extremum (minimum)
Amplitude
Time
X(t)
C(t)
Z(t) = C(t) + iY (t),
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4.8×10−7Hz
3.8×10−6Hz
1.9×10−6Hz
2.0×10−5Hz
4.8×10−7Hz WX(a, b)
2.0×10−5Hz
WX(a, b)
9.5×10−74.8×10−7
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4.8×10−71.0×10−5Hz
1.9×10−62.0×10−5
4.8×10−7
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Salinity, 1.92, R2 = 0.99
Bioluminescence, 1.96, R2 = 0.99
Temperature, 1.87, R2 = 0.98
Current speed, 1.93, R2 = 0.99
2.0×10−5Hz
9.5×10−73.8×10−6
2.0×10−5Hz
4.8×10−7Hz
2.4
9.5×10−7Hz
4.8×10−7Hz
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4.8×10−7Hz
4.8×10−7Hz
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6.1×10−6
5.7×10−6
1.9×10−6
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A)
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5.7×10−6
1.1×10−5
1.9×10−6
4.8×10−7Hz
A)
B)
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Bioluminescence (kHz) WX (a,b)
Current speed (cm s-1)WX (a,b)
WX (a,b)
Salinity
WX(a, b)
... The trait of bioluminescence is distributed over a diverse range of marine species, from bacteria to fish [2]. Over the last years the distribution and quantification of bioluminescence in the deep sea and individual luminescent organisms have been studied using a variety of observational techniques [1,[3][4][5][6]. Most in-situ observation techniques rely on actively triggering the light production by disturbing the environment and stimulating the organisms, since spontaneous emission does not occur at statistically sufficient rates for observation times in the order of hours [7][8][9]. ...
... These telescopes aim to detect Cherenkov radiation caused by charged secondary particles, which are induced by high-energy cosmic neutrino interactions with constituents of water molecules. The records of these telescopes were used to analyze the dynamics of deep sea bioluminescence [4,[32][33][34]. The majority of the recorded bioluminescence is assumed to be triggered by sea currents and turbulence around the detectors [4,33]. ...
... The records of these telescopes were used to analyze the dynamics of deep sea bioluminescence [4,[32][33][34]. The majority of the recorded bioluminescence is assumed to be triggered by sea currents and turbulence around the detectors [4,33]. Therefore, the challenge to observe spontaneous bioluminescence remains. ...
Studying Bioluminescence Flashes with the ANTARES Deep Sea Neutrino Telescope
Preprint
Full-text available
  • Jul 2021
We develop a novel technique to exploit the extensive data sets provided by underwater neutrino telescopes to gain information on bioluminescence in the deep sea. The passive nature of the telescopes gives us the unique opportunity to infer information on bioluminescent organisms without actively interfering with them. We propose a statistical method that allows us to reconstruct the light emission of individual organisms, as well as their location and movement. A mathematical model is built to describe the measurement process of underwater neutrino telescopes and the signal generation of the biological organisms. The Metric Gaussian Variational Inference algorithm is used to reconstruct the model parameters using photon counts recorded by the neutrino detectors. We apply this method to synthetic data sets and data collected by the ANTARES neutrino telescope. The telescope is located 40 km off the French coast and fixed to the sea floor at a depth of 2475 m. The runs with synthetic data reveal that we can reliably model the emitted bioluminescent flashes of the organisms. Furthermore, we find that the spatial resolution of the localization of light sources highly depends on the configuration of the telescope. Precise measurements of the efficiencies of the detectors and the attenuation length of the water are crucial to reconstruct the light emission. Finally, the application to ANTARES data reveals the first precise localizations of bioluminescent organisms using neutrino telescope data.
View
... More recently, sediment resuspension events (Durrieu de Madron et al., 2017) were correlated with newly formed deep-water events and deep-sea bioluminescent events recorded in the NW Mediterranean Sea (Martini et al., 2014;Tamburini et al., 2013a). Since the presence of active luminous bacteria has been demonstrated on the site , it has been hypothesized that resuspended luminescent bacteria present in sediment can be part of these luminescence events (Durrieu de Madron et al., 2017). ...
... Other approaches have been developed unexpectedly from astrophysics telescopes ( Fig. 1, item h) using photomultipliers with a very high sensitivity to photons embedded into optical modules. These instruments have been proven to be efficient to detect bioluminescence in deep-sea environments and over long-time surveys (Aguzzi et al., 2017;Martini et al., 2014;Tamburini et al., 2013a). Another example of quantitative records of photon counts is the equipment of bio-samplers, such as elephant seals, with a small, autonomous tag recording environmental light and bioluminescence (Fig. 1g). ...
Reviews and syntheses: Bacterial bioluminescence – ecology and impact in the biological carbon pump
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  • Jul 2020
  • BG
Around 30 species of marine bacteria can emit light, a critical characteristic in the oceanic environment is mostly deprived of sunlight. In this article, we first review current knowledge on bioluminescent bacteria symbiosis in light organs. Then, focusing on gut-associated bacteria, we highlight that recent works, based on omics methods, confirm previous claims about the prominence of bioluminescent bacterial species in fish guts. Such host–symbiont relationships are relatively well-established and represent important knowledge in the bioluminescence field. However, the consequences of bioluminescent bacteria continuously released from light organs and through the digestive tracts to the seawater have been barely taken into account at the ecological and biogeochemical level. For too long neglected, we propose considering the role of bioluminescent bacteria and reconsidering the biological carbon pump, taking into account the bioluminescence effect (“bioluminescence shunt hypothesis”). Indeed, it has been shown that marine snow and fecal pellets are often luminous due to microbial colonization, which makes them a visual target. These luminous particles seem preferentially consumed by organisms of higher trophic levels in comparison to nonluminous ones. As a consequence, the sinking rate of consumed particles could be either increased (due to repackaging) or reduced (due to sloppy feeding or coprophagy/coprorhexy), which can imply a major impact on global biological carbon fluxes. Finally, we propose a strategy, at a worldwide scale, relying on recently developed instrumentation and methodological tools to quantify the impact of bioluminescent bacteria in the biological carbon pump.
View
... Other approaches have been developed unexpectedly from astrophysics telescopes using photomultipliers with a very high sensitivity to photons embedded into optical modules. These instruments have been proven to be efficient to detect bioluminescence in deep-sea environments and over long-time surveys (Martini et al., 2014;Tamburini et al., 2013a). Another example of quantitative records of photon counts is the equipment of bio-samplers, such as elephant seals, with a small, autonomous tag recording environmental light and bioluminescence. ...
Molecular Biology Plant Physiology
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... For example, data on the ocean interior are used to calibrate and validate satellite readings, a connection enabled by various degrees of continuity in combined data collection via vessel-assisted autonomous underwater vehicles (AUVs), multiparameter coastal cabled observatories, and moored buoys and Argo floats (Riser et al., 2016; National Aeronautics and Space Administration [NASA], 2018). Moreover, underwater neutrino telescopes initially conceptualized and deployed to detect astroparticles, have been integrated into water-column research (e.g., Martini et al., 2014), detecting life in the form of bioluminescence. ...
Developing technological synergies between deep-sea and space research
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Full-text available
  • Feb 2022
Recent advances in robotic design, autonomy and sensor integration create solutions for the exploration of deep-sea environments, transferable to the oceans of icy moons. Marine platforms do not yet have the mission autonomy capacity of their space counterparts (e.g., the state of the art Mars Perseverance rover mission), although different levels of autonomous navigation and mapping, as well as sampling, are an extant capability. In this setting their increasingly biomimicked designs may allow access to complex environmental scenarios, with novel, highly-integrated life-detecting, oceanographic and geochemical sensor packages. Here, we lay an outlook for the upcoming advances in deep-sea robotics through synergies with space technologies within three major research areas: biomimetic structure and propulsion (including power storage and generation), artificial intelligence and cooperative networks, and life-detecting instrument design. New morphological and material designs, with miniaturized and more diffuse sensor packages, will advance robotic sensing systems. Artificial intelligence algorithms controlling navigation and communications will allow the further development of the behavioral biomimicking by cooperating networks. Solutions will have to be tested within infrastructural networks of cabled observatories, neutrino telescopes, and offshore industry sites with agendas and modalities that are beyond the scope of our work, but could draw inspiration on the proposed examples for the operational combination of fixed and mobile platforms.
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... A recent addition to cabled observatories allows the study of subatomic particles such as neutrinos (Agostini et al., 2020). Using a suite of photomultipliers and other lightsensitive sensors, these neutrino telescopes are also capable of continuously monitoring bioluminescence from migrating deepscattering layers and bacterioplankton (Martini et al., 2013(Martini et al., , 2014Tamburini et al., 2013;Bailly et al., 2021). These crossdisciplinary infrastructures will provide key complementary data for long-term monitoring of bentho-pelagic coupling in a rapidly changing ocean (Chatzievangelou et al., 2021). ...
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Deep-sea ecosystems are reservoirs of biodiversity that are largely unexplored, but their exploration and biodiscovery are becoming a reality thanks to biotechnological advances (e.g., omics technologies) and their integration in an expanding network of marine infrastructures for the exploration of the seas, such as cabled observatories. While still in its infancy, the application of environmental DNA (eDNA) metabarcoding approaches is revolutionizing marine biodiversity monitoring capability. Indeed, the analysis of eDNA in conjunction with the collection of multidisciplinary optoacoustic and environmental data, can provide a more comprehensive monitoring of deep-sea biodiversity. Here, we describe the potential for acquiring eDNA as a core component for the expanding ecological monitoring capabilities through cabled observatories and their docked Internet Operated Vehicles (IOVs), such as crawlers. Furthermore, we provide a critical overview of four areas of development: (i) Integrating eDNA with optoacoustic imaging; (ii) Development of eDNA repositories and cross-linking with other biodiversity databases; (iii) Artificial Intelligence for eDNA analyses and integration with imaging data; and (iv) Benefits of eDNA augmented observatories for the conservation and sustainable management of deep-sea biodiversity. Finally, we discuss the technical limitations and recommendations for future eDNA monitoring of the deep-sea. It is hoped that this review will frame the future direction of an exciting journey of biodiscovery in remote and yet vulnerable areas of our planet, with the overall aim to understand deep-sea biodiversity and hence manage and protect vital marine resources.
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... Thus, when mass migrating into deeper layers of the ocean, these species can potentially affect the background intensity of ambient light. Indeed, variability of light intensities has already been recorded over multiannual time-series in the deep ocean using sensors, originally installed with the purpose to study neutrino emissions in the ocean's interior (Tamburini et al., 2013;Martini et al., 2014;Aguzzi et al., 2017). In general, the presence of bioluminescent organisms at aphotic depths, where there are minimal-if any at all-detectable traces of sunlight, can modify the local ambient light regime by being the strongest (or sole) light source (Cronin et al., 2016), consequently shaping local communities and important functions of the respective ecosystems. ...
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The deep sea (i.e., >200 m depth) is a highly dynamic environment where benthic ecosystems are functionally and ecologically connected with the overlying water column and the surface. In the aphotic deep sea, organisms rely on external signals to synchronize their biological clocks. Apart from responding to cyclic hydrodynamic patterns and periodic fluctuations of variables such as temperature, salinity, phytopigments, and oxygen concentration, the arrival of migrators at depth on a 24-h basis (described as Diel Vertical Migrations; DVMs), and from well-lit surface and shallower waters, could represent a major response to a solar-based synchronization between the photic and aphotic realms. In addition to triggering the rhythmic behavioral responses of benthic species, DVMs supply food to deep seafloor communities through the active downward transport of carbon and nutrients. Bioluminescent species of the migrating deep scattering layers play a not yet quantified (but likely important) role in the benthopelagic coupling, raising the need to integrate the efficient detection and quantification of bioluminescence into large-scale monitoring programs. Here, we provide evidence in support of the benefits for quantifying and continuously monitoring bioluminescence in the deep sea. In particular, we recommend the integration of bioluminescence studies into long-term monitoring programs facilitated by deep-sea neutrino telescopes, which offer photon counting capability. Their Photo-Multiplier Tubes and other advanced optical sensors installed in neutrino telescope infrastructures can boost the study of bioluminescent DVMs in concert with acoustic backscatter and video imagery from ultra-low-light cameras. Such integration will enhance our ability to monitor proxies for the mass and energy transfer from the upper ocean into the deep-sea Benthic Boundary Layer (BBL), a key feature of the ocean biological pump and crucial for monitoring the effects of climate-change. In addition, it will allow for investigating the role of deep scattering DVMs in the behavioral responses, abundance and structure of deep-sea benthic communities. The proposed approach may represent a new frontier for the study and discovery of new, taxon-specific bioluminescence capabilities. It will thus help to expand our knowledge of poorly described deep-sea biodiversity inventories and further elucidate the connectivity between pelagic and benthic compartments in the deep-sea.
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... Despite the known functions of bioluminescence such as defense and offense, mate attraction, and intra-and inter-specific interactions (Haddock et al. 2010), some of the ecological applications of bioluminescence phenomenon are explored. Deep-sea bioluminescence is used as real-time biomarker to study biological activities in the deep ocean (Craig et al. 2011a;Gillibrand et al. 2007a;Martini et al. 2014;Tamburini et al. 2013). This ecological trait also utilized to study the spatial, seasonal, or diurnal biomass patterns and community composition changes of dominant pelagic organisms found at different depths (Craig et al. 2011a, b;Cronin et al. 2016;Martini et al. 2019;Martini and Haddock 2017;Messié et al. 2019). ...
Terrestrial and marine bioluminescent organisms from the Indian subcontinent: a review
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Full-text available
The inception of bioluminescence by Harvey (1952) has led to a Nobel Prize to Osamu Shimomura (Chemistry, 2008) in biological research. Consequently, in recent years, bioluminescence-based assays to monitor toxic pollutants as a real-time marker, to study various diseases and their propagation in plants and animals, are developed in many countries. The emission ability of bioluminescence is improved by gene modification, and also, search for novel bioluminescent systems is underway. Over 100 species of organisms belonging to different taxa are known to be luminous in India. However, the diversity and distribution of luminous organisms and their applications are studied scarcely in the Indian scenario. In this context, the present review provides an overview of the current understanding of various bioluminescent organisms, functions, and applications. A detailed checklist of known bioluminescent organisms from India's marine, terrestrial, and freshwater ecosystems is detailed. This review infers that Indian scientists are needed to extend their research on various aspects of luminescent organisms such as biodiversity, genomics, and chemical mechanisms for conservation, ecological, and biomedical applications.
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... The increase of the OC flux with relatively undegraded OM during the violent mixing and the sinking and spreading phases contributed to the "fertilization" of the deep pelagic and benthic ecosystems. Fertilization of the basin by previous deep dense water formation events was suggested by , Company et al. (2008), Tamburini et al. (2013), Severin et al. (2014) and Martini et al. (2014), although the exact timing and the evolution of the OM composition could not be elucidated until now. ...
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Studying bioluminescence flashes with the ANTARES deep‐sea neutrino telescope
Article
We develop a novel technique to exploit the extensive data sets provided by underwater neutrino telescopes to gain information on bioluminescence in the deep sea. The passive nature of the telescopes gives us the unique opportunity to infer information on bioluminescent organisms without actively interfering with them. We propose a statistical method that allows us to reconstruct the light emission of individual organisms, as well as their location and movement. A mathematical model is built to describe the measurement process of underwater neutrino telescopes and the signal generation of the biological organisms. The Metric Gaussian Variational Inference algorithm is used to reconstruct the model parameters using photon counts recorded by photomultiplier tubes. We apply this method to synthetic data sets and data collected by the ANTARES neutrino telescope. The telescope is located 40 km off the French coast and fixed to the sea floor at a depth of 2475 m. The runs with synthetic data reveal that we can model the emitted bioluminescent flashes of the organisms. Furthermore, we find that the spatial resolution of the localization of light sources highly depends on the configuration of the telescope. Precise measurements of the efficiencies of the detectors and the attenuation length of the water are crucial to reconstruct the light emission. Finally, the application to ANTARES data reveals the first localizations of bioluminescent organisms using neutrino telescope data.
View
Rapid response of benthic deep-sea microbes (viruses and prokaryotes) to an intense dense shelf water cascading event in a submarine canyon of the NW Mediterranean Sea
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A major dense shelf water cascading (DSWC) event occurred in 2005 downward the Cap de Creus Canyon (Gulf of Lion, NW Mediterranean Sea), which caused a significant change in environmental parameters and biological components. Here we describe the effects of this DSWC event on benthic microbes and on virus-prokaryote interactions, and we explore their implications on the functioning of the canyon's ecosystem. We collected sediment samples at increasing depths inside the canyon and in the adjacent deep continental margin over a period of five years, i.e. during and after the DSWC event, which led to the deposition of high amounts of fresh and labile organic matter that stimulated C production by benthic prokaryotes and increased their abundance and biomass. The enhanced prokaryotic metabolism, still evident 6 months after the DSWC event, was associated with high viral replication rates and prokaryotic mortality, which released 3.4–6.3 gC m⁻² over such a 6 months period. Such values are up to 3-times higher than the yearly C-flux to the seafloor reported in this area in years without DSWC. We conclude that DSWC can significantly enhance benthic prokaryotic metabolism and C cycling through viral-induced prokaryotic mortality.
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On the trophic regimes of the Mediterranean Sea: a satellite analysis
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Full-text available
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  • BGD
The ten years of the SeaWiFS satellite surface chlorophyll concentration observations, presently available, were used to characterize the biogeography of the Mediterranean Sea and the seasonal cycle of the surface biomass in different areas of the basin. The K-means cluster analysis was applied on the satellite time-series of chlorophyll concentration. The resulting coherent patterns were then explained on the basis of the present knowledge of the basin functioning. Winter biomass enhancements were shown to occur in most of the basin and last for 2–3 months depending on the region. Classical spring bloom regimes were also observed, regularly in the North Western Mediterranean, and intermittently in four others specific areas. The analysis confirmed that the Mediterranean Sea is an ideal area to evaluate the impacts of the external physical forcing on the marine ecosystem functioning.
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Impact of open-ocean convection on particle fluxes and sediment dynamics in the deep margin of the Gulf of Lions
Article
Full-text available
  • Sep 2012
  • BGD
The deep outer margin of the Gulf of Lions and the adjacent basin, in the Western Mediterranean Sea, are regularly impacted by open-ocean convection, a major hydrodynamic event responsible for the ventilation of the deep water in the Western Mediterranean Basin. However, the impact of open-ocean convection on the flux and transport of particulate matter remains poorly understood. The variability of water mass properties (i.e. temperature and salinity), currents, and particle fluxes was monitored between September 2007 and April 2009 at five instrumented mooring lines deployed between 2050 and 2350 m-depth in the deepest continental margin and adjacent basin. Four of the lines followed a NW–SE transect, while the fifth one was located on a sediment wave field to the west. The results of the main, central line SC2350 ("LION"), located at 42° 02.5′ N and 4° 41′ E, at 2350 m-depth, show that open-ocean convection reached mid-water depth (≈ 1000 m-depth) during winter 2007–2008, and reached the seabed (≈ 2350 m-depth) during winter 2008–2009. Horizontal currents were unusually strong with speeds up to 39 cm s−1 during winter 2008–2009. The measurements at all 5 different locations indicate that mid-depth and near-bottom currents and particle fluxes gave relatively consistent values of similar magnitude across the study area except during winter 2008–2009, when near-bottom fluxes abruptly increased by one to two orders of magnitude. Particulate organic carbon contents, which generally vary between 3 and 5%, were abnormally low (≤ 1%) during winter 2008–2009 and approached those observed in surface sediments (≈ 0.6%). Turbidity profiles made in the region demonstrated the existence of a bottom nepheloid layer, several hundred meters thick, and related to the resuspension of bottom sediments. These observations support the view that open-ocean deep convection events in the Gulf of Lions can cause significant remobilization of sediments in the deep outer margin and the basin, with a subsequent alteration of the seabed likely impacting the functioning of the deep-sea ecosystem.
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The global component of the US Ocean Observatories Initiative and the global OceanSITES project
Conference Paper
  • Sep 2011
The NSF-funded Ocean Observatories Initiative (OOI) will establish four comprehensive and interactive open-ocean observatories for sustained timeseries observations, two of which are located in the Pacific Basin. At each site they will include four moorings and three gliders, with a wide range of multidisciplinary sensors. These installations will represent infrastructure for the ocean research community and enable both process experiments and climate-timescale investigations. In addition to free data access and mechanisms to manipulate the assets and sensors of the observatories, there will be expansion capacity for user-provided instruments. This presentation will explain the plans and capabilities for these open-ocean observatories. The OOI sites are embedded in the global and international timeseries project OceanSITES, which is an established component of the global ocean observing system. Many countries are contributing to this network. OceanSITES provides coordination, integration into a global system, and a data management framework which enables the accessibility and dissemination of the data to the community. There are presently about 100 sites with 200 platforms globally in OceanSITES. The status and benefits of the project will be explained. New sites are continually being added and both the research and operational community are encouraged to add their open-ocean sustained timeseries sites to OceanSITES.
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Principal warps: Thin-plate splines and the decomposition of deformations
Article
  • Jan 1992
The decomposition of deformations by principal warps is demonstrated. The method is extended to deal with curving edges between landmarks. This formulation is related to other applications of splines current in computer vision. How they might aid in the extraction of features for analysis, comparison, and diagnosis of biological and medical images is indicated.
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Open-ocean convection: Observations, theory, and models
Article
  • Feb 1999
We review what is known about the convec-tive process in the open ocean, in which the properties of large volumes of water are changed by intermittent, deep-reaching convection, triggered by winter storms. Observational, laboratory, and modeling studies reveal a fascinating and complex interplay of convective and geostrophic scales, the large-scale circulation of the ocean, and the prevailing meteorology. Two aspects make ocean convection interesting from a theoretical point of view. First, the timescales of the convective process in the ocean are sufficiently long that it may be modified by the Earth's rotation; second, the convective process is localized in space so that vertical buoyancy transfer by upright convection can give way to slantwise transfer by baroclinic instability. Moreover, the convec-tive and geostrophic scales are not very disparate from one another. Detailed observations of the process in the Labrador, Greenland, and Mediterranean Seas are de-scribed, which were made possible by new observing technology. When interpreted in terms of underlying dynamics and theory and the context provided by labo-ratory and numerical experiments of rotating convec-tion, great progress in our description and understand-ing of the processes at work is being made.
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A Practical Guide to Wavelet Analysis
Article
  • Jan 1998
  • B AM METEOROL SOC
A practical step-by-step guide to wavelet analysis is given, with examples taken from time series of the El NiñoSouthem Oscillation (ENSO). The guide includes a comparison to the windowed Fourier transform, the choice of an appropriate wavelet basis function, edge effects due to finite-length time series, and the relationship between wavelet scale and Fourier frequency. New statistical significance tests for wavelet power spectra are developed by deriving theoretical wavelet spectra for white and red noise processes and using these to establish significance levels and confidence intervals. It is shown that smoothing in time or scale can be used to increase the confidence of the wavelet spectrum. Empirical formulas are given for the effect of smoothing on significance levels and confidence intervals. Extensions to wavelet analysis such as filtering, the power Hovmöller, cross-wavelet spectra, and coherence are described. The statistical significance tests are used to give a quantitative measure of changes in ENSO variance on interdecadal timescales. Using new datasets that extend back to 1871, the Niño3 sea surface temperature and the Southern Oscillation index show significantly higher power during 1880-1920 and 1960-90, and lower power during 1920-60, as well as a possible 15-yr modulation of variance. The power Hovmöller of sea level pressure shows significant variations in 2-8-yr wavelet power in both longitude and time.
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