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Integrating Diel Vertical Migrations Of Integrating Diel Vertical Migrations of Bioluminescent Deep Scattering Layers Into Monitoring Programs Damianos Chatzievangelou, Nixon Bahamon, Séverine Martini, Joaquin del Rio, Giorgio Riccobene, Michael Tangherlini, Roberto Danovaro, Fabio de Leo, Benoit Pirenne, Jacopo Aguzzi To cite this version: Damianos Chatzievangelou, Nixon Bahamon, Séverine Martini, Joaquin del Rio, Giorgio Ric- cobene, et al.. Integrating Diel Vertical Migrations of Bioluminescent Deep Scattering Layers Into Monitoring Programs. Frontiers in Marine Science, Frontiers Media, 2021, 8, pp.661809. 10.3389/fmars.2021.661809. hal-03256342 HAL Id: hal-03256342 https://hal.archives-ouvertes.fr/hal-03256342 Submitted on 10 Jun 2021 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. fmars-08-661809 May 24, 2021 Time: 15:50 # 1 REVIEW published: 28 May 2021 doi: 10.3389/fmars.2021.661809 Integrating Diel Vertical Migrations of Bioluminescent Deep Scattering Layers Into Monitoring Programs Damianos Chatzievangelou1*, Nixon Bahamon2, Séverine Martini3, Joaquin del Rio4, Giorgio Riccobene5, Michael Tangherlini6, Roberto Danovaro6,7, Fabio C. De Leo8,9, Benoit Pirenne8 and Jacopo Aguzzi2,6* 1 OceanLab, Department of Physics and Earth Sciences, Jacobs University, Bremen, Germany, 2 Functioning and Vulnerability of Marine Ecosystems Group, Department of Renewable Marine Resources, Instituto de Ciencias del Mar (ICM-CSIC), Barcelona, Spain, 3 Institut de Recherche pour le Développement (IRD), Centre National de la Recherche Scientifique (CNRS), Aix Marseille Université, Université de Toulon, Marseille, France, 4 SARTI, Universitat Politècnica de Catalunya (UPC), Barcelona, Spain, 5 Laboratori Nazionali del Sud LNS, Istituto Nazionale di Fisica Nucleare (INFN), Frascati, Italy, 6 Stazione Zoologica Anton Dohrn (SZN), Naples, Italy, 7 Dipartimento di Scienze della Vita e dell’Ambiente, Università Politecnica delle Marche (UNIVPM), Ancona, Italy, 8 Ocean Networks Canada (ONC), University of Victoria, Victoria, BC, Canada, 9 Department of Biology, University of Victoria, Victoria, BC, Canada The deep sea (i.e., >200 m depth) is a highly dynamic environment where benthic Edited by: ecosystems are functionally and ecologically connected with the overlying water Pedro A. Ribeiro, column and the surface. In the aphotic deep sea, organisms rely on external University of Bergen, Norway signals to synchronize their biological clocks. Apart from responding to cyclic Reviewed by: Ellen Pape, hydrodynamic patterns and periodic fluctuations of variables such as temperature, Ghent University, Belgium salinity, phytopigments, and oxygen concentration, the arrival of migrators at depth on Doug Bartlett, University of California, San Diego, a 24-h basis (described as Diel Vertical Migrations; DVMs), and from well-lit surface and United States shallower waters, could represent a major response to a solar-based synchronization *Correspondence: between the photic and aphotic realms. In addition to triggering the rhythmic behavioral Damianos Chatzievangelou responses of benthic species, DVMs supply food to deep seafloor communities through [email protected] Jacopo Aguzzi the active downward transport of carbon and nutrients. Bioluminescent species of [email protected] 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 Specialty section: This article was submitted to and quantification of bioluminescence into large-scale monitoring programs. Here, we Deep-Sea Environments and Ecology, provide evidence in support of the benefits for quantifying and continuously monitoring a section of the journal Frontiers in Marine Science bioluminescence in the deep sea. In particular, we recommend the integration of Received: 31 January 2021 bioluminescence studies into long-term monitoring programs facilitated by deep-sea Accepted: 03 May 2021 neutrino telescopes, which offer photon counting capability. Their Photo-Multiplier Tubes Published: 28 May 2021 and other advanced optical sensors installed in neutrino telescope infrastructures can Citation: boost the study of bioluminescent DVMs in concert with acoustic backscatter and video Chatzievangelou D, Bahamon N, Martini S, del Rio J, Riccobene G, imagery from ultra-low-light cameras. Such integration will enhance our ability to monitor Tangherlini M, Danovaro R, proxies for the mass and energy transfer from the upper ocean into the deep-sea De Leo FC, Pirenne B and Aguzzi J (2021) Integrating Diel Vertical Benthic Boundary Layer (BBL), a key feature of the ocean biological pump and crucial for Migrations of Bioluminescent Deep monitoring the effects of climate-change. In addition, it will allow for investigating the role Scattering Layers Into Monitoring of deep scattering DVMs in the behavioral responses, abundance and structure of deep- Programs. Front. Mar. Sci. 8:661809. doi: 10.3389/fmars.2021.661809 sea benthic communities. The proposed approach may represent a new frontier for the Frontiers in Marine Science| www.frontiersin.org 1 May 2021| Volume 8| Article 661809 fmars-08-661809 May 24, 2021 Time: 15:50 # 2 Chatzievangelou et al. Monitoring Bioluminescent Vertical Migrations 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. Keywords: bioluminescence, deep scattering layer, diel vertical migrations, activity rhythms, monitoring technologies, neutrino telescopes INTRODUCTION may generate a series of synchronized vertical movements of predators and preys within the adjacent depth strata (i.e., staged The deep sea (i.e., >200 m depth) is the largest biome of the migrations) or those movements could even occur in a single run planet. It represents the 65% of the whole planet’s surface and (Naylor, 2005; Aguzzi and Company, 2010; Brierley, 2014). Along contains more than 95% of the biosphere, with more than three continental margins on the middle and lower slopes, as well as at quarters of the ocean’s surface projecting to depths below 3,000 abyssal depths, animals could approach or even enter the ecotone m (Costello et al., 2010; Haddock et al., 2017; Sweetman et al., between the water column and the benthic ecosystems (i.e., the 2017). Unfortunately, only a minimal percentage of the deep benthic boundary layer; BBL) at a certain time of the day, acting sea has been explored in terms of its biological components, as predators or prey, hence being vectors of carbon and energy. and therefore most of marine biodiversity remains uncensused One important agent for the transfer of carbon and energy (Mora et al., 2011; Snelgrove, 2016). Species accumulation curves between benthic and pelagic ecosystems is the formation obtained from a range of deep-sea studies to date do not reach of deep scattering layers, i.e., aggregations of invertebrates an asymptotic plateau, indicating that the cataloged number and vertebrates driven by ecological needs, including food of species does not come close to the true species richness acquisition, reproduction or avoiding predators (Dietz, 1962). (Danovaro et al., 2010; Webb et al., 2010; Costello et al., Since physical and chemical gradients in the ocean are generally 2012). In fact, on Earth, of all classified species only 16% are stronger in the vertical rather than in the horizontal axis marine (Costello and Chaudhary, 2017). During the second over comparable spatial scales, they result in these horizontal half of the previous century, the prevalent perception of an large layers of organisms (Benoit-Bird et al., 2017; Sato and isolated benthic environment, with relative stability in terms Benoit-Bird, 2017). Through the exchange of energy across of hydrodynamism and associated oceanographic conditions, adjacent oceanic layers at rates faster than the ones dictated by was overturned (Hessler and Sanders, 1967; Levin et al., 2010; passive sinking and hydrodynamically-induced vertical mixing, Ramirez-Llodra et al., 2010; Levin and Sibuet, 2012; Smith the migrating animals enhance the efficiency of the biological et al., 2017). Additionally, it was considered oligotrophic and pump, sustain food webs, and provide temporal triggers for sustaining low biomass and biodiversity, which in turn was deep-sea communities, ultimately contributing to the vertical causing underestimations of global species abundance and connectivity in the marine environment (Bianchi et al., 2013; biomass (reviewed in Rex et al., 2006; Thurber et al., 2014). Davison et al., 2013; Ochoa et al., 2013; Irigoien et al., 2014; Nowadays this perception has changed drastically and, Kelly et al., 2019). As such, for the majority of benthic ecosystems although population densities are low and clustered, and while (i.e., apart from the occasional spots of chemosynthetic primary depth-related decreasing trends exist globally, this biome musters
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