This article presents the development of an underwater gripper that utilizes soft robotics technology to delicately manipulate and sample fragile species on the deep reef. Existing solutions for deep sea robotic manipulation have historically been driven by the oil industry, resulting in destructive interactions with undersea life. Soft material robotics relies on compliant materials that are inherently impedance matched to natural environments and to soft or fragile organisms. We demonstrate design principles for soft robot end effectors, bench-top characterization of their grasping performance, and conclude by describing in situ testing at mesophotic depths. The result is the first use of soft robotics in the deep sea for the nondestructive sampling of benthic fauna.

The discovery of fluorescent proteins has revolutionized experimental biology. Whereas the majority of fluorescent proteins have been identified from cnidarians, recently several fluorescent proteins have been isolated across the animal tree of life. Here we show that biofluorescence is not only phylogenetically widespread, but is also phenotypically variable across both cartilaginous and bony fishes, highlighting its evolutionary history and the possibility for discovery of numerous novel fluorescent proteins. Fish biofluorescence is especially common and morphologically variable in cryptically patterned coral-reef lineages. We identified 16 orders, 50 families, 105 genera, and more than 180 species of biofluorescent fishes. We have also reconstructed our current understanding of the phylogenetic distribution of biofluorescence for ray-finned fishes. The presence of yellow long-pass intraocular filters in many biofluorescent fish lineages and the substantive color vision capabilities of coral-reef fishes suggest that they are capable of detecting fluoresced light. We present species-specific emission patterns among closely related species, indicating that biofluorescence potentially functions in intraspecific communication and evidence that fluorescence can be used for camouflage. This research provides insight into the distribution, evolution, and phenotypic variability of biofluorescence in marine lineages and examines the role this variation may play.

Transcriptome and genome data from twenty stony coral species and a selection of reference bilaterians were studied to elucidate coral evolutionary history. We identified genes that encode the proteins responsible for the precipitation and aggregation of the aragonite skeleton on which the organisms live, and revealed a network of environmental sensors that coordinate responses of the host animals to temperature, light, and pH. Furthermore, we describe a variety of stress-related pathways, including apoptotic pathways that allow the host animals to detoxify reactive oxygen and nitrogen species that are generated by their intracellular photosynthetic symbionts, and determine the fate of corals under environmental stress. Some of these genes arose through horizontal gene transfer and comprise at least 0.2% of the animal gene inventory. Our analysis elucidates the evolutionary strategies that have allowed symbiotic corals to adapt and thrive for hundreds of millions of years.DOI: http://dx.doi.org/10.7554/eLife.13288.001

Here, we present ultragentle soft robotic actuators capable of grasping delicate specimens of gelatinous marine life. Although state-of-the-art soft robotic manipulators have demonstrated gentle gripping of brittle animals (e.g., corals) and echinoderms (e.g., sea cucumbers) in the deep sea, they are unable to nondestructively grasp more fragile soft-bodied organisms, such as jellyfish. Through an exploration of design parameters and laboratory testing of individual actuators, we confirmed that our nanofiber-reinforced soft actuators apply sufficiently low contact pressure to ensure minimal harm to typical jellyfish species. We then built a gripping device using several actuators and evaluated its underwater grasping performance in the laboratory. By assessing the gripper’s region of acquisition and robustness to external forces, we gained insight into the necessary precision and speed with which grasping maneuvers must be performed to achieve successful collection of samples. Last, we demonstrated successful manipulation of three live jellyfish species in an aquarium setting using a hand-held prototype gripper. Overall, our ultragentle gripper demonstrates an improvement in gentle sample collection compared with existing deep-sea sampling devices. Extensions of this technology may improve a variety of in situ characterization techniques used to study the ecological and genetic features of deep-sea organisms.

We studied the effects of a bacterium (Pseudomonas chlororaphis) and a bactivorous protozoan (Uronema sp.) on transformations of labile dissolved organic carbon (DOC). In 36-day time series experiments, bacteria were grown on glucose both with and without protozoa. We measured bulk organic carbon pools and used electrospray ionization mass spectrometry to characterize dissolved organic matter on a molecular level. Bacteria rapidly utilized glucose, depleting it to nondetectable levels and producing new DOC compounds of higher molecular weight within 2 days. Some of these new compounds, representing 3 to 5% of the initial glucose-C, were refractory and persisted for over a month. Other new compounds were produced and subsequently used by bacteria during the lag and exponential growth phases, pointing to a dynamic cycling of organic compounds. Grazers caused a temporary spike in the DOC concentration consisting of labile compounds subsequently utilized by the bacteria. Grazing did not increase the complexity of the DOC pool already established by the bacteria but did continually decrease the particulate organic carbon pool and expedited the conversion of glucose-C to CO 2 . After 36 days, 29% of initial glucose-C remained in pure bacteria cultures, while only 6% remained in cultures where a grazer was present. In this study the bacteria were the primary shapers of the complex DOC continuum, suggesting higher trophic levels possibly have less of an impact on the qualitative composition of DOC than previously assumed.Dissolved organic matter (DOM) comprises the largest, yet least-characterized reservoir of reduced organic carbon in aquatic systems, estimated at 700 ϫ 10 15 g C (11). DOM is important in the carbon and nitrogen cycles, the scavenging and solubilization of trace contaminants, and biogeochemical cycles of other elements (3,14). Heterotrophic bacteria process and reprocess some of this DOM (2), channeling about one-half of oceanic primary production through the microbial loop (8).The role of bacteria in the rate and extent of DOM mineralization and their production of (semi)refractory DOM have received less attention. Some studies indicate that bacteria produce refractory DOM that is resistant to further utilization (5,12,37,39). Ogawa et al. (26) showed that a natural inoculum of marine bacteria (and undoubtedly nanoflagellates and viruses) growing on labile compounds (glucose and glutamate) produce new DOM compounds that appear to be refractory for at least a year. It was not known if a single strain of bacteria could produce similar refractory material. Bacterioplankton can also be a source of photoreactive C-DOM that is refractory to a natural bacteria assemblage following photochemical alteration (18). What kinds and how many different compounds make up the refractory DOM pool are largely unknown.In aquatic ecosystems, bacteria are consumed by protozoa and other zooplankton, which in turn release DOM as colloidal matter (17, 40) and macromolecular organic complexes (24). A substantial portion (Ͼ50%...

Photosynthetic coral reef structures extend from the shallow sundrenched waters to the dimly lit, "twilight" mesophotic depths. For their resident endosymbiotic dinoflagellates, primarily from the genus Symbiodinium spp., this represents a photic environment that varies ∼15-fold in intensity and also differs in spectral composition. We examined photosynthesis in the scleractinian coral Stylophora pistillata in shallow (3 m) and mesophotic settings (65 m) in the northern Red Sea. Symbiodinium spp. in corals originating from the mesophotic environment consistently performed below their photosynthetic compensation point and also exhibited distinct light harvesting antenna organization. In addition, the non-photochemical quenching activity of Symbiodinium spp. from mesophotic corals was shown to be considerably lower than those found in shallow corals, showing they have fewer defenses to high-light settings. Over a period of almost 4 years, we extensively utilized closed circuit Trimix rebreather diving to perform the study. Phylogenetic analysis showed that shallow corals (3 m) transplanted to a deep reef environment (65 m) maintained their initial Symbiodinium spp. community (clade A), rather than taking on deep low-light clades (clade C), demonstrating that shallow S. pistillata acclimate to low-light mesophotic environments while maintaining their shallow photosynthetic traits. Mesophotic corals exhibited static depth-related chlorophyll content per cell, a decrease in PSI activity and enhanced sigmoidal fluorescence rise kinetics. The sigmoidal fluorescence rise kinetics we observed in mesophotic corals is an indication of energy transfer between photosynthetic units. We postulate that at mesophotic depths, a community of adapted Symbiodinium spp. utilize a unique adaptation to lower light conditions by shifting their light harvesting to a PSII based system, where PSII is structured near PSI, with additional PCP soluble Einbinder et al.Novel Photosynthetic Characteristics of Mesophotic Photosymbionts antenna also trapping light that is funneled to the PSI reaction center. In this study, we provide evidence that mesophotic Symbiodinium spp. have developed novel adaptive low-light characteristics consisting of a cooperative system for excitation energy transfer between photosynthetic units that maximizes light utilization.

Modern marine biologists seeking to study or interact with deep-sea organisms are confronted with few options beyond industrial robotic arms, claws, and suction samplers. This limits biological interactions to a subset of “rugged” and mostly immotile fauna. As the deep sea is one of the most biologically diverse and least studied ecosystems on the planet, there is much room for innovation in facilitating delicate interactions with a multitude of organisms. The biodiversity and physiology of shallow marine systems, such as coral reefs, are common study targets due to the easier nature of access; SCUBA diving allows for in situ delicate human interactions. Beyond the range of technical SCUBA (~150 m), the ability to achieve the same level of human dexterity using robotic systems becomes critically important. The deep ocean is navigated primarily by manned submersibles or remotely operated vehicles, which currently offer few options for delicate manipulation. Here we present results in developing a soft robotic manipulator for deep-sea biological sampling. This low-power glove-controlled soft robot was designed with the future marine biologist in mind, where science can be conducted at a comparable or better means than via a human diver and at depths well beyond the limits of SCUBA. The technology relies on compliant materials that are matched with the soft and fragile nature of marine organisms, and uses seawater as the working fluid. Actuators are driven by a custom proportional-control hydraulic engine that requires less than 50 W of electrical power, making it suitable for battery-powered operation. A wearable glove master allows for intuitive control of the arm. The manipulator system has been successfully operated in depths exceeding 2300 m (3500 psi) and has been field-tested onboard a manned submersible and unmanned remotely operated vehicles. The design, development, testing, and field trials of the soft manipulator is placed in context with existing systems and we offer suggestions for future work based on these findings.

We implemented Machine Learning (ML) techniques to advance the study of sperm whale ( Physeter macrocephalus ) bioacoustics. This entailed employing Convolutional Neural Networks (CNNs) to construct an echolocation click detector designed to classify spectrograms generated from sperm whale acoustic data according to the presence or absence of a click. The click detector achieved 99.5% accuracy in classifying 650 spectrograms. The successful application of CNNs to clicks reveals the potential of future studies to train CNN-based architectures to extract finer-scale details from cetacean spectrograms. Long short-term memory and gated recurrent unit recurrent neural networks were trained to perform classification tasks, including (1) “coda type classification” where we obtained 97.5% accuracy in categorizing 23 coda types from a Dominica dataset containing 8,719 codas and 93.6% accuracy in categorizing 43 coda types from an Eastern Tropical Pacific (ETP) dataset with 16,995 codas; (2) “vocal clan classification” where we obtained 95.3% accuracy for two clan classes from Dominica and 93.1% for four ETP clan types; and (3) “individual whale identification” where we obtained 99.4% accuracy using two Dominica sperm whales. These results demonstrate the feasibility of applying ML to sperm whale bioacoustics and establish the validity of constructing neural networks to learn meaningful representations of whale vocalizations.