Intra- and Interspecific Foraging and Feeding Interactions in Three Sea Stars and a Gastropod from the Deep Sea.

Competitive interactions come in a variety of forms and may be modulated by the size and number of individuals involved, and/or the resources available. Here, intra- and interspecific competitive behaviours for food (i.e., foraging/food search and feeding/food ingestion) were experimentally characterized and quantified in four co-existing deep-sea benthic species. Three sea stars (Ceramaster granularis, Hippasteria phrygiana, and Henricia lisa) and one gastropod (Buccinum scalariforme) from the bathyal Northwest Atlantic were investigated using video trials in darkened laboratory conditions. A range of competitive or cooperative behaviours occurred, depending on species (conspecific or heterospecific), comparative body size, and the number of individuals involved. Contrary to expectations, small individuals (or smaller species) were not always outcompeted by larger individuals (or larger species) when foraging and feeding. Moreover, faster species did not always outcompete slower ones while scavenging. Overall, this study sheds new light on scavenging strategies of co-existing deep-sea benthic species in food-limited bathyal environments, based on complex behavioural inter- and intraspecific relationships.

ROV-based monitoring of passive ecological recovery in a deep-sea no-take fishery reserve.

In the context of marine conservation, trawl fishing activity is the most important ecosystem stressor in demersal Mediterranean waters. Limited management measures in bottom trawling have caused deep-sea stocks of the iconic Norway lobster Nephrops norvegicus to decrease over the last decade. This crustacean acts as an umbrella species for co-existing megafauna. Here, we used non-invasive Remote Operated Vehicle (ROV) video-surveys to investigate the status of a pilot deep-sea no-take reserve implemented in the northwestern Mediterranean by quantifying demographic indicators of Norway lobsters and the co-existing benthic community, seafloor restoration, and the presence of marine litter. The results revealed that in the no-take reserve the Norway lobster stock showed higher abundance and biomass, and slightly larger body sizes than in the control area without fishing prohibition. Some taxa, such as the fishes Helicolenus dactylopterus and Trigla lyra and anemones of the family Cerianthidae, increased in abundance. We also observed that all trawling marks were smoothed and most of the seafloor was intact, clear indicators of the recovery of the muddy seafloor. The accumulation of marine debris and terrestrial vegetation was similar in the no-take reserve and the fished area. On the basis of the results of this study, we suggest that the use of no-take reserves might be an effective measure for recovering the Norway lobster stock, its co-existing megafauna community, and the surrounding demersal habitat. We also suggest that ROV video-survey might be a useful, and non-invasive method to monitor megafauna and seafloor status in protected deep-sea environments.

Established and Emerging Research Trends in Norway Lobster, Nephrops norvegicus.

The burrowing crustacean decapod Nephrops norvegicus is a significant species in European Atlantic and Mediterranean fisheries. Research over the decades has mainly focused on behavioral and physiological aspects related to the burrowing lifestyle, since animals can only be captured by trawls when engaged in emergence on the seabed. Here, we performed a global bibliographic survey of all the scientific literature retrieved in SCOPUS since 1965, and terminology maps were produced with the VOSviewer software to reveal established and emerging research areas. We produced three term-map plots: term clustering, term citation, and term year. The term clustering network showed three clusters: fishery performance, assessment, and management; biological cycles in growth, reproduction, and behavior; and finally, physiology and ecotoxicology, including food products. The term citation map showed that intense research is developed on ecotoxicology and fishery management. Finally, the term year map showed that the species was first studied in its morphological and physiological aspects and more recently in relation to fishery and as a food resource. Taken together, the results indicate scarce knowledge on how burrowing behavior and its environmental control can alter stock assessment, because of the poor use of current and advanced monitoring technologies.

Image dataset for benchmarking automated fish detection and classification algorithms.

Multiparametric video-cabled marine observatories are becoming strategic to monitor remotely and in real-time the marine ecosystem. Those platforms can achieve continuous, high-frequency and long-lasting image data sets that require automation in order to extract biological time series. The OBSEA, located at 4 km from Vilanova i la Geltrú at 20 m depth, was used to produce coastal fish time series continuously over the 24-h during 2013-2014. The image content of the photos was extracted via tagging, resulting in 69917 fish tags of 30 taxa identified. We also provided a meteorological and oceanographic dataset filtered by a quality control procedure to define real-world conditions affecting image quality. The tagged fish dataset can be of great importance to develop Artificial Intelligence routines for the automated identification and classification of fishes in extensive time-lapse image sets.

Different Traits, Different Evolutionary Pathways: Insights from Salamandrina (Amphibia, Caudata).

Species delimitation is often based on a single or very few genetic or phenetic traits, something which leads to misinterpretations and often does not provide information about evolutionary processes. Here, we investigated the diversity pattern of multiple phenetic traits of the two extant species of Salamandrina, a genus split only after molecular traits had been studied but the two species of which are phenetically very similar. The phenetic traits we studied are size, external body shape and head colour pattern, in a model comparison framework using non-linear mixed models and unsupervised and supervised clustering. Overall, we found high levels of intra-specific variability for body size and shape, depending on population belonging and habitat, while differences between species were generally lower. The habitat the salamanders dwell in also seems important for colour pattern. Basing on our findings, from the methodological point of view, we suggest (i) to take into account the variability at population level when testing for higher level variability, and (ii) a semi-supervised learning approach to high dimensional data. We also showed that different phenotypic traits of the same organism could result from different evolutionary routes. Local adaptation is likely responsible for body size and shape variability, with selective pressures more similar across species than within them. Head colour pattern also depends on habitat, differently from ventral colour pattern (not studied in this paper) which likely evolved under genetic drift.

Marine Robotics for Deep-Sea Specimen Collection: A Taxonomy of Underwater Manipulative Actions.

In order to develop a gripping system or control strategy that improves scientific sampling procedures, knowledge of the process and the consequent definition of requirements is fundamental. Nevertheless, factors influencing sampling procedures have not been extensively described, and selected strategies mostly depend on pilots' and researchers' experience. We interviewed 17 researchers and remotely operated vehicle (ROV) technical operators, through a formal questionnaire or in-person interviews, to collect evidence of sampling procedures based on their direct field experience. We methodologically analyzed sampling procedures to extract single basic actions (called atomic manipulations). Available equipment, environment and species-specific features strongly influenced the manipulative choices. We identified a list of functional and technical requirements for the development of novel end-effectors for marine sampling. Our results indicate that the unstructured and highly variable deep-sea environment requires a versatile system, capable of robust interactions with hard surfaces such as pushing or scraping, precise tuning of gripping force for tasks such as pulling delicate organisms away from hard and soft substrates, and rigid holding, as well as a mechanism for rapidly switching among external tools.

Marine Robotics for Deep-Sea Specimen Collection: A Systematic Review of Underwater Grippers.

The collection of delicate deep-sea specimens of biological interest with remotely operated vehicle (ROV) industrial grippers and tools is a long and expensive procedure. Industrial grippers were originally designed for heavy manipulation tasks, while sampling specimens requires dexterity and precision. We describe the grippers and tools commonly used in underwater sampling for scientific purposes, systematically review the state of the art of research in underwater gripping technologies, and identify design trends. We discuss the possibility of executing typical manipulations of sampling procedures with commonly used grippers and research prototypes. Our results indicate that commonly used grippers ensure that the basic actions either of gripping or caging are possible, and their functionality is extended by holding proper tools. Moreover, the approach of the research status seems to have changed its focus in recent years: from the demonstration of the validity of a specific technology (actuation, transmission, sensing) for marine applications, to the solution of specific needs of underwater manipulation. Finally, we summarize the environmental and operational requirements that should be considered in the design of an underwater gripper.

Correction: Lopez-Vazquez et al. Video Image Enhancement and Machine Learning Pipeline for Underwater Animal Detection and Classification at Cabled Observatories. Sensors 2020, 20, 726.

The authors wish to correct the following error in the original paper [...].

Seafloor litter at oceanic islands and seamounts of the southeastern Pacific.

Seafloor litter in oceanic islands of the southeastern Pacific Ocean have rarely been described and quantified, mainly due to the associated logistical challenges. In this study, we describe and quantify the different kinds of litter from 60 to 320 m depths in Rapa Nui (RN) and Desventuradas Islands (DI), and evaluated the relationship of this litter with the local population in terms of demographic density and fishing activity. The study compiled data from 84 stations surveyed with a ROV representing a total distance of 22 km. Litter was grouped into six categories. 96 observations of litter and debris were taken around RN, most of which associated with local artisanal fishing activity, especially fishing anchors (56%). No tourism-associated debris were reported. Any kind of seafloor litter was observed at DI. The present study provides baseline information for the local community to improve management by understanding the potential sources of seafloor litter.

Research Trends and Future Perspectives in Marine Biomimicking Robotics.

Mechatronic and soft robotics are taking inspiration from the animal kingdom to create new high-performance robots. Here, we focused on marine biomimetic research and used innovative bibliographic statistics tools, to highlight established and emerging knowledge domains. A total of 6980 scientific publications retrieved from the Scopus database (1950-2020), evidencing a sharp research increase in 2003-2004. Clustering analysis of countries collaborations showed two major Asian-North America and European clusters. Three significant areas appeared: (i) energy provision, whose advancement mainly relies on microbial fuel cells, (ii) biomaterials for not yet fully operational soft-robotic solutions; and finally (iii), design and control, chiefly oriented to locomotor designs. In this scenario, marine biomimicking robotics still lacks solutions for the long-lasting energy provision, which presently hinders operation autonomy. In the research environment, identifying natural processes by which living organisms obtain energy is thus urgent to sustain energy-demanding tasks while, at the same time, the natural designs must increasingly inform to optimize energy consumption.

Don't catch me if you can - Using cabled observatories as multidisciplinary platforms for marine fish community monitoring: An in situ case study combining Underwater Video and environmental DNA data.

Cabled observatories are marine infrastructures equipped with biogeochemical and oceanographic sensors as well as High-Definition video and audio equipment, hence providing unprecedented opportunities to study marine biotic and abiotic components. Additionally, non-invasive monitoring approaches such as environmental DNA (eDNA) metabarcoding have further enhanced the ability to characterize marine life. Although the use of non-invasive tools beholds great potential for the sustainable monitoring of biodiversity and declining natural resources, such techniques are rarely used in parallel and understanding their limitations is challenging. Thus, this study combined Underwater Video (UV) with eDNA metabarcoding data to produce marine fish community profiles over a 2 months period in situ at a cabled observatory in the northeast Atlantic (SmartBay Ireland). By combining both approaches, an increased number of fish could be identified to the species level (total of 22 species), including ecologically and economically important species such as Atlantic cod, whiting, mackerel and monkfish. The eDNA approach alone successfully identified a higher number of species (59%) compared to the UV approach (18%), whereby 23% of species were detected by both methods. The parallel implementation of point collection eDNA and time series UV data not only confirmed expectations of the corroborative effect of using multiple disciplines in fish community composition, but also enabled the assessment of limitations intrinsic to each technique including the identification of false-negative detections in one sampling technology relative to the other. This work showcased the usefulness of cabled observatories as key platforms for in situ empirical assessment of both challenges and prospects of novel technologies in aid to future monitoring of marine life.

Burrow emergence rhythms of Nephrops norvegicus by UWTV and surveying biases.

Underwater Television (UWTV) surveys provide fishery-independent stock size estimations of the Norway lobster (Nephrops norvegicus), based directly on burrow counting using the survey assumption of "one animal = one burrow". However, stock size may be uncertain depending on true rates of burrow occupation. For the first time, 3055 video transects carried out in several Functional Units (FUs) around Ireland were used to investigate this uncertainty. This paper deals with the discrimination of burrow emergence and door-keeping diel behaviour in Nephrops norvegicus, which is one of the most commercially important fisheries in Europe. Comparisons of burrow densities with densities of visible animals engaged in door-keeping (i.e. animals waiting at the tunnel entrance) behaviour and animals in full emergence, were analysed at time windows of expected maximum population emergence. Timing of maximum emergence was determined using wave-form analysis and GAM modelling. The results showed an average level of 1 visible Nephrops individual per 10 burrow systems, depending on sampling time and depth. This calls into question the current burrow occupancy assumption which may not hold true in all FUs. This is discussed in relation to limitations of sampling methodologies and new autonomous robotic technological solutions for monitoring.

An Automated Pipeline for Image Processing and Data Treatment to Track Activity Rhythms of Paragorgia arborea in Relation to Hydrographic Conditions.

Imaging technologies are being deployed on cabled observatory networks worldwide. They allow for the monitoring of the biological activity of deep-sea organisms on temporal scales that were never attained before. In this paper, we customized Convolutional Neural Network image processing to track behavioral activities in an iconic conservation deep-sea species-the bubblegum coral Paragorgia arborea-in response to ambient oceanographic conditions at the Lofoten-Vesterålen observatory. Images and concomitant oceanographic data were taken hourly from February to June 2018. We considered coral activity in terms of bloated, semi-bloated and non-bloated surfaces, as proxy for polyp filtering, retraction and transient activity, respectively. A test accuracy of 90.47% was obtained. Chronobiology-oriented statistics and advanced Artificial Neural Network (ANN) multivariate regression modeling proved that a daily coral filtering rhythm occurs within one major dusk phase, being independent from tides. Polyp activity, in particular extrusion, increased from March to June, and was able to cope with an increase in chlorophyll concentration, indicating the existence of seasonality. Our study shows that it is possible to establish a model for the development of automated pipelines that are able to extract biological information from times series of images. These are helpful to obtain multidisciplinary information from cabled observatory infrastructures.

Quality Control and Pre-Analysis Treatment of the Environmental Datasets Collected by an Internet Operated Deep-Sea Crawler during Its Entire 7-Year Long Deployment (2009-2016).

Deep-sea environmental datasets are ever-increasing in size and diversity, as technological advances lead monitoring studies towards long-term, high-frequency data acquisition protocols. This study presents examples of pre-analysis data treatment steps applied to the environmental time series collected by the Internet Operated Deep-sea Crawler "Wally" during a 7-year deployment (2009-2016) in the Barkley Canyon methane hydrates site, off Vancouver Island (BC, Canada). Pressure, temperature, electrical conductivity, flow, turbidity, and chlorophyll data were subjected to different standardizing, normalizing, and de-trending methods on a case-by-case basis, depending on the nature of the treated variable and the range and scale of the values provided by each of the different sensors. The final pressure, temperature, and electrical conductivity (transformed to practical salinity) datasets are ready for use. On the other hand, in the cases of flow, turbidity, and chlorophyll, further in-depth processing, in tandem with data describing the movement and position of the crawler, will be needed in order to filter out all possible effects of the latter. Our work evidences challenges and solutions in multiparametric data acquisition and quality control and ensures that a big step is taken so that the available environmental data meet high quality standards and facilitate the production of reliable scientific results.

Stepped Coastal Water Warming Revealed by Multiparametric Monitoring at NW Mediterranean Fixed Stations.

Since 2014, the global land and sea surface temperature has scaled 0.23 °C above the decadal average (2009-2018). Reports indicate that Mediterranean Sea temperatures have been rising at faster rates than in the global ocean. Oceanographic time series of physical and biogeochemical data collected from an onboard and a multisensor mooring array in the northwestern Mediterranean Sea (Blanes submarine canyon, Balearic Sea) during 2009-2018 revealed an abrupt temperature rising since 2014, in line with regional and global warming. Since 2014, the oligotrophic conditions of the water column have intensified, with temperature increasing 0.61 °C on the surface and 0.47 °C in the whole water column in continental shelf waters. Water transparency has increased due to a decrease in turbidity anomaly of -0.1 FTU. Since 2013, inshore chlorophyll a concentration remained below the average (-0.15 mg·l-1) and silicates showed a declining trend. The mixed layer depth showed deepening in winter and remained steady in summer. The net surface heat fluxes did not show any trend linked to the local warming, probably due to the influence of incoming offshore waters produced by the interaction between the Northern Current and the submarine canyon. Present regional and global water heating pattern is increasing the stress of highly diverse coastal ecosystems at unprecedented levels, as reported by the literature. The strengthening of the oligotrophic conditions in the study area may also apply as a cautionary warning to similar coastal ecosystems around the world following the global warming trend.

Towards Naples Ecological REsearch for Augmented Observatories (NEREA): The NEREA-Fix Module, a Stand-Alone Platform for Long-Term Deep-Sea Ecosystem Monitoring.

Deep-sea ecological monitoring is increasingly recognized as indispensable for the comprehension of the largest biome on Earth, but at the same time it is subjected to growing human impacts for the exploitation of biotic and abiotic resources. Here, we present the Naples Ecological REsearch (NEREA) stand-alone observatory concept (NEREA-fix), an integrated observatory with a modular, adaptive structure, characterized by a multiparametric video-platform to be deployed in the Dohrn canyon (Gulf of Naples, Tyrrhenian Sea) at ca. 650 m depth. The observatory integrates a seabed platform with optoacoustic and oceanographic/geochemical sensors connected to a surface transmission buoy, plus a mooring line (also equipped with depth-staged environmental sensors). This reinforced high-frequency and long-lasting ecological monitoring will integrate the historical data conducted over 40 years for the Long-Term Ecological Research (LTER) at the station "Mare Chiara", and ongoing vessel-assisted plankton (and future environmental DNA-eDNA) sampling. NEREA aims at expanding the observational capacity in a key area of the Mediterranean Sea, representing a first step towards the establishment of a bentho-pelagic network to enforce an end-to-end transdisciplinary approach for the monitoring of marine ecosystems across a wide range of animal sizes (from bacteria to megafauna).

The Hierarchic Treatment of Marine Ecological Information from Spatial Networks of Benthic Platforms.

Measuring biodiversity simultaneously in different locations, at different temporal scales, and over wide spatial scales is of strategic importance for the improvement of our understanding of the functioning of marine ecosystems and for the conservation of their biodiversity. Monitoring networks of cabled observatories, along with other docked autonomous systems (e.g., Remotely Operated Vehicles [ROVs], Autonomous Underwater Vehicles [AUVs], and crawlers), are being conceived and established at a spatial scale capable of tracking energy fluxes across benthic and pelagic compartments, as well as across geographic ecotones. At the same time, optoacoustic imaging is sustaining an unprecedented expansion in marine ecological monitoring, enabling the acquisition of new biological and environmental data at an appropriate spatiotemporal scale. At this stage, one of the main problems for an effective application of these technologies is the processing, storage, and treatment of the acquired complex ecological information. Here, we provide a conceptual overview on the technological developments in the multiparametric generation, storage, and automated hierarchic treatment of biological and environmental information required to capture the spatiotemporal complexity of a marine ecosystem. In doing so, we present a pipeline of ecological data acquisition and processing in different steps and prone to automation. We also give an example of population biomass, community richness and biodiversity data computation (as indicators for ecosystem functionality) with an Internet Operated Vehicle (a mobile crawler). Finally, we discuss the software requirements for that automated data processing at the level of cyber-infrastructures with sensor calibration and control, data banking, and ingestion into large data portals.

Behavioral rhythms of an opportunistic predator living in anthropogenic landscapes.

BACKGROUND: Human activities have profoundly altered the spatio-temporal availability of food resources. Yet, there is a clear lack of knowledge on how opportunistic species adapt to these new circumstances by scheduling their daily rhythms and adjust their foraging decisions to predicable patterns of anthropic food subsidies. Here, we used nearly continuous GPS tracking data to investigate the adaptability of daily foraging activity in an opportunistic predator, the yellow-legged gull (Larus michahellis), in response to human schedules. METHODS: By using waveform analysis, we compared timing and magnitude of peaks in daily activity of different GPS-tracked individuals in eleven different habitat types, in relation to type of day (i.e., weekday vs. weekend). RESULTS: Daily activity rhythms varied greatly depending on whether it was a weekday or weekend, thus suggesting that gulls' activity peaks matched the routines of human activity in each habitat type. We observed for the first time two types of activity as modelled by waveforms analysis: marine habitats showed unimodal patterns with prolonged activity and terrestrial habitats showed bimodal patterns with two shorter and variable activity peaks. CONCLUSIONS: Our results suggest that gulls are able to fine-tune their daily activity rhythms to habitat-specific human schedules, since these likely provide feeding opportunities. Behavioral plasticity may thus be an important driver of expansive population dynamics. Information on predictable relationships between daily activity patterns of gulls and human activities is therefore relevant to their population management.

A Flexible Autonomous Robotic Observatory Infrastructure for Bentho-Pelagic Monitoring.

This paper presents the technological developments and the policy contexts for the project "Autonomous Robotic Sea-Floor Infrastructure for Bentho-Pelagic Monitoring" (ARIM). The development is based on the national experience with robotic component technologies that are combined and merged into a new product for autonomous and integrated ecological deep-sea monitoring. Traditional monitoring is often vessel-based and thus resource demanding. It is economically unviable to fulfill the current policy for ecosystem monitoring with traditional approaches. Thus, this project developed platforms for bentho-pelagic monitoring using an arrangement of crawler and stationary platforms at the Lofoten-Vesterålen (LoVe) observatory network (Norway). Visual and acoustic imaging along with standard oceanographic sensors have been combined to support advanced and continuous spatial-temporal monitoring near cold water coral mounds. Just as important is the automatic processing techniques under development that have been implemented to allow species (or categories of species) quantification (i.e., tracking and classification). At the same time, real-time outboard processed three-dimensional (3D) laser scanning has been implemented to increase mission autonomy capability, delivering quantifiable information on habitat features (i.e., for seascape approaches). The first version of platform autonomy has already been tested under controlled conditions with a tethered crawler exploring the vicinity of a cabled stationary instrumented garage. Our vision is that elimination of the tether in combination with inductive battery recharge trough fuel cell technology will facilitate self-sustained long-term autonomous operations over large areas, serving not only the needs of science, but also sub-sea industries like subsea oil and gas, and mining.