Coastal upwelling drives ecosystem temporal variability from the surface to the abyssal seafloor.

Long-term biological time series that monitor ecosystems across the ocean's full water column are extremely rare. As a result, classic paradigms are yet to be tested. One such paradigm is that variations in coastal upwelling drive changes in marine ecosystems throughout the water column. We examine this hypothesis by using data from three multidecadal time series spanning surface (0 m), midwater (200 to 1,000 m), and benthic (~4,000 m) habitats in the central California Current Upwelling System. Data include microscopic counts of surface plankton, video quantification of midwater animals, and imaging of benthic seafloor invertebrates. Taxon-specific plankton biomass and midwater and benthic animal densities were separately analyzed with principal component analysis. Within each community, the first mode of variability corresponds to most taxa increasing and decreasing over time, capturing seasonal surface blooms and lower-frequency midwater and benthic variability. When compared to local wind-driven upwelling variability, each community correlates to changes in upwelling damped over distinct timescales. This suggests that periods of high upwelling favor increase in organism biomass or density from the surface ocean through the midwater down to the abyssal seafloor. These connections most likely occur directly via changes in primary production and vertical carbon flux, and to a lesser extent indirectly via other oceanic changes. The timescales over which species respond to upwelling are taxon-specific and are likely linked to the longevity of phytoplankton blooms (surface) and of animal life (midwater and benthos), which dictate how long upwelling-driven changes persist within each community.

ROV observations reveal infection dynamics of gill parasites in midwater cephalopods.

Gill parasites of coleoid cephalopods are frequently observed during remotely operated vehicle (ROV) dives in the Monterey Submarine Canyon. However, little knowledge exists on the identity of the parasite species or their effects on the cephalopod community. With the help of ROV-collected specimens and in situ footage from the past 27 years, we report on their identity, prevalence and potential infection strategy. Gill parasites were genetically and morphologically identified from collected specimens of Chiroteuthis calyx, Vampyroteuthis infernalis and Gonatus spp. In situ prevalence was estimated from video footage for C. calyx, Galiteuthis spp., Taonius spp. and Japetella diaphana, enabled by their transparent mantle tissue. The most common parasite was identified as Hochbergia cf. moroteuthensis, a protist of unresolved taxonomic ranking. We provide the first molecular data for this parasite and show a sister group relationship to the dinoflagellate genus Oodinium. Hochbergia cf. moroteuthensis was most commonly observed in adult individuals of all species and was sighted year round over the analyzed time period. In situ prevalence was highest in C. calyx (75%), followed by Galiteuthis spp. (29%), Taonius spp. (27%) and J. diaphana (7%). A second parasite, not seen on the in situ footage, but occurring within the gills of Gonatus berryi and Vampyroteuthis infernalis, could not be found in the literature or be identified through DNA barcoding. The need for further investigation is highlighted, making this study a starting point for unravelling ecological implications of the cephalopod-gill-parasite system in deep pelagic waters.

Atolla reynoldsi sp. nov. (Cnidaria, Scyphozoa, Coronatae, Atollidae): A New Species of Coronate Scyphozoan Found in the Eastern North Pacific Ocean.

We have observed and collected unusual specimens of what we recognize as undescribed types of the genus Atolla over the past 15 years. Of these, there appear to be three potentially different types. One of these has now been genetically sequenced and compared both morphologically and molecularly with five other Atolla species that have been found in the eastern Pacific. This new variant is so morphologically distinct from other previously described Atolla species that we believe it can be described as a new species, Atolla reynoldsi sp. nov. This species along with two additional types may comprise a new genus. It is also clear that a more accurate and diagnostic morphological key for the genus Atolla needs to be developed. This paper will also provide some potential starting points for a new key to the genus.

A hybrid underwater robot for multidisciplinary investigation of the ocean twilight zone.

Mesobot, an autonomous underwater vehicle, addresses specific unmet needs for observing and sampling a variety of phenomena in the ocean's midwaters. The midwater hosts a vast biomass, has a role in regulating climate, and may soon be exploited commercially, yet our scientific understanding of it is incomplete. Mesobot has the ability to survey and track slow-moving animals and to correlate the animals' movements with critical environmental measurements. Mesobot will complement existing oceanographic assets such as towed, remotely operated, and autonomous vehicles; shipboard acoustic sensors; and net tows. Its potential to perform behavioral studies unobtrusively over long periods with substantial autonomy provides a capability that is not presently available to midwater researchers. The 250-kilogram marine robot can be teleoperated through a lightweight fiber optic tether and can also operate untethered with full autonomy while minimizing environmental disturbance. We present recent results illustrating the vehicle's ability to automatically track free-swimming hydromedusae (Solmissus sp.) and larvaceans (Bathochordaeus stygius) at depths of 200 meters in Monterey Bay, USA. In addition to these tracking missions, the vehicle can execute preprogrammed missions collecting image and sensor data while also carrying substantial auxiliary payloads such as cameras, sonars, and samplers.

Distribution, associations and role in the biological carbon pump of Pyrosoma atlanticum (Tunicata, Thaliacea) off Cabo Verde, NE Atlantic.

Gelatinous zooplankton are increasingly acknowledged to contribute significantly to the carbon cycle worldwide, yet many taxa within this diverse group remain poorly studied. Here, we investigate the pelagic tunicate Pyrosoma atlanticum in the waters surrounding the Cabo Verde Archipelago. By using a combination of pelagic and benthic in situ observations, sampling, and molecular genetic analyses (barcoding, eDNA), we reveal that: P. atlanticum abundance is most likely driven by local island-induced productivity, that it substantially contributes to the organic carbon export flux and is part of a diverse range of biological interactions. Downward migrating pyrosomes actively transported an estimated 13% of their fecal pellets below the mixed layer, equaling a carbon flux of 1.96-64.55 mg C m-2 day-1. We show that analysis of eDNA can detect pyrosome material beyond their migration range, suggesting that pyrosomes have ecological impacts below the upper water column. Moribund P. atlanticum colonies contributed an average of 15.09 ± 17.89 (s.d.) mg C m-2 to the carbon flux reaching the island benthic slopes. Our pelagic in situ observations further show that P. atlanticum formed an abundant substrate in the water column (reaching up to 0.28 m2 substrate area per m2), with animals using pyrosomes for settlement, as a shelter and/or a food source. In total, twelve taxa from four phyla were observed to interact with pyrosomes in the midwater and on the benthos.

Ultra-black Camouflage in Deep-Sea Fishes.

At oceanic depths >200 m, there is little ambient sunlight, but bioluminescent organisms provide another light source that can reveal animals to visual predators and prey [1-4]. Transparency and mirrored surfaces-common camouflage strategies under the diffuse solar illumination of shallower waters-are conspicuous when illuminated by directed bioluminescent sources due to reflection from the body surface [5, 6]. Pigmentation allows animals to absorb light from bioluminescent sources, rendering them visually undetectable against the dark background of the deep sea [5]. We present evidence suggesting pressure to reduce reflected bioluminescence led to the evolution of ultra-black skin (reflectance <0.5%) in 16 species of deep-sea fishes across seven distantly related orders. Histological data suggest this low reflectance is mediated by a continuous layer of densely packed melanosomes in the exterior-most layer of the dermis [7, 8] and that this layer lacks the unpigmented gaps between pigment cells found in other darkly colored fishes [9-13]. Using finite-difference, time-domain modeling and comparisons with melanosomes found in other ectothermic vertebrates [11, 13-21], we find the melanosomes making up the layer in these ultra-black species are optimized in size and shape to minimize reflectance. Low reflectance results from melanosomes scattering light within the layer, increasing the optical path length and therefore light absorption by the melanin. By reducing reflectance, ultra-black fish can reduce the sighting distance of visual predators more than 6-fold compared to fish with 2% reflectance. This biological example of efficient light absorption via a simple architecture of strongly absorbing and highly scattering particles may inspire new ultra-black materials.

Revealing enigmatic mucus structures in the deep sea using DeepPIV.

Many animals build complex structures to aid in their survival, but very few are built exclusively from materials that animals create 1,2. In the midwaters of the ocean, mucoid structures are readily secreted by numerous animals, and serve many vital functions3,4. However, little is known about these mucoid structures owing to the challenges of observing them in the deep sea. Among these mucoid forms, the 'houses' of larvaceans are marvels of nature5, and in the ocean twilight zone giant larvaceans secrete and build mucus filtering structures that can reach diameters of more than 1 m6. Here we describe in situ laser-imaging technology7 that reconstructs three-dimensional models of mucus forms. The models provide high-resolution views of giant larvacean houses and elucidate the role that house structure has in food capture and predator avoidance. Now that tools exist to study mucus structures found throughout the ocean, we can shed light on some of nature's most complex forms.

Bioluminescent backlighting illuminates the complex visual signals of a social squid in the deep sea.

Visual signals rapidly relay information, facilitating behaviors and ecological interactions that shape ecosystems. However, most known signaling systems can be restricted by low light levels-a pervasive condition in the deep ocean, the largest inhabitable space on the planet. Resident visually cued animals have therefore been hypothesized to have simple signals with limited information-carrying capacity. We used cameras mounted on remotely operated vehicles to study the behavior of the Humboldt squid, Dosidicus gigas, in its natural deep-sea habitat. We show that specific pigmentation patterns from its diverse repertoire are selectively displayed during foraging and in social scenarios, and we investigate how these behaviors may be used syntactically for communication. We additionally identify the probable mechanism by which D. gigas, and related squids, illuminate these patterns to create visual signals that can be readily perceived in the deep, dark ocean. Numerous small subcutaneous (s.c.) photophores (bioluminescent organs) embedded throughout the muscle tissue make the entire body glow, thereby backlighting the pigmentation patterns. Equipped with a mechanism by which complex information can be rapidly relayed through a visual pathway under low-light conditions, our data suggest that the visual signals displayed by D. gigas could share design features with advanced forms of animal communication. Visual signaling by deep-living cephalopods will likely be critical in understanding how, and how much, information can be shared in one of the planet's most challenging environments for visual communication.

Author Correction: The vertical distribution and biological transport of marine microplastics across the epipelagic and mesopelagic water column.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

The vertical distribution and biological transport of marine microplastics across the epipelagic and mesopelagic water column.

Plastic waste has been documented in nearly all types of marine environments and has been found in species spanning all levels of marine food webs. Within these marine environments, deep pelagic waters encompass the largest ecosystems on Earth. We lack a comprehensive understanding of the concentrations, cycling, and fate of plastic waste in sub-surface waters, constraining our ability to implement effective, large-scale policy and conservation strategies. We used remotely operated vehicles and engineered purpose-built samplers to collect and examine the distribution of microplastics in the Monterey Bay pelagic ecosystem at water column depths ranging from 5 to 1000 m. Laser Raman spectroscopy was used to identify microplastic particles collected from throughout the deep pelagic water column, with the highest concentrations present at depths between 200 and 600 m. Examination of two abundant particle feeders in this ecosystem, pelagic red crabs (Pleuroncodes planipes) and giant larvaceans (Bathochordaeus stygius), showed that microplastic particles readily flow from the environment into coupled water column and seafloor food webs. Our findings suggest that one of the largest and currently underappreciated reservoirs of marine microplastics may be contained within the water column and animal communities of the deep sea.

Pelagic shrimp play dead in deep oxygen minima.

Pelagic crustaceans are arguably the most abundant group of metazoans on Earth, yet little is known about their natural behavior. The deep pelagic shrimp Hymenopenaeus doris is a common decapod that thrives in low oxygen layers of the eastern Pacific Ocean. When first observed in situ using a remotely operated vehicle, most specimens of H. doris appeared dead due to inactivity and inverted orientation. Closer inspection revealed that these animals were utilizing small, subtle shifts in appendage position to control their orientation and sink rate. In this mode, they resembled molted shrimp exoskeletons. We hypothesize that these shrimp may avoid capture by visually-cued predators with this characteristic behavior. The low metabolic rates of H. doris (0.55-0.81 mg O2 kg-1 min-1) are similar to other deep-living shrimp, and also align with their high hypoxia tolerance and reduced activity. We observed similar behavior in another deep pelagic decapod, Petalidium suspiriosum, which transiently inhabited Monterey Canyon, California, during a period of anomalously warm ocean conditions.

Deep pelagic food web structure as revealed by in situ feeding observations.

Food web linkages, or the feeding relationships between species inhabiting a shared ecosystem, are an ecological lens through which ecosystem structure and function can be assessed, and thus are fundamental to informing sustainable resource management. Empirical feeding datasets have traditionally been painstakingly generated from stomach content analysis, direct observations and from biochemical trophic markers (stable isotopes, fatty acids, molecular tools). Each approach carries inherent biases and limitations, as well as advantages. Here, using 27 years (1991-2016) of in situ feeding observations collected by remotely operated vehicles (ROVs), we quantitatively characterize the deep pelagic food web of central California within the California Current, complementing existing studies of diet and trophic interactions with a unique perspective. Seven hundred and forty-three independent feeding events were observed with ROVs from near-surface waters down to depths approaching 4000 m, involving an assemblage of 84 different predators and 82 different prey types, for a total of 242 unique feeding relationships. The greatest diversity of prey was consumed by narcomedusae, followed by physonect siphonophores, ctenophores and cephalopods. We highlight key interactions within the poorly understood 'jelly web', showing the importance of medusae, ctenophores and siphonophores as key predators, whose ecological significance is comparable to large fish and squid species within the central California deep pelagic food web. Gelatinous predators are often thought to comprise relatively inefficient trophic pathways within marine communities, but we build upon previous findings to document their substantial and integral roles in deep pelagic food webs.

From the surface to the seafloor: How giant larvaceans transport microplastics into the deep sea.

Plastic waste is a pervasive feature of marine environments, yet little is empirically known about the biological and physical processes that transport plastics through marine ecosystems. To address this need, we conducted in situ feeding studies of microplastic particles (10 to 600 µm in diameter) with the giant larvacean Bathochordaeus stygius. Larvaceans are abundant components of global zooplankton assemblages, regularly build mucus "houses" to filter particulate matter from the surrounding water, and later abandon these structures when clogged. By conducting in situ feeding experiments with remotely operated vehicles, we show that giant larvaceans are able to filter a range of microplastic particles from the water column, ingest, and then package microplastics into their fecal pellets. Microplastics also readily affix to their houses, which have been shown to sink quickly to the seafloor and deliver pulses of carbon to benthic ecosystems. Thus, giant larvaceans can contribute to the vertical flux of microplastics through the rapid sinking of fecal pellets and discarded houses. Larvaceans, and potentially other abundant pelagic filter feeders, may thus comprise a novel biological transport mechanism delivering microplastics from surface waters, through the water column, and to the seafloor. Our findings necessitate the development of tools and sampling methodologies to quantify concentrations and identify environmental microplastics throughout the water column.

New technology reveals the role of giant larvaceans in oceanic carbon cycling.

To accurately assess the impacts of climate change on our planet, modeling of oceanic systems and understanding how atmospheric carbon is transported from surface waters to the deep benthos are required. The biological pump drives the transport of carbon through the ocean's depths, and the rates at which carbon is removed and sequestered are often dependent on the grazing abilities of surface and midwater organisms. Some of the most effective and abundant midwater grazers are filter-feeding invertebrates. Although the impact of smaller, near-surface filter feeders is generally known, efforts to quantify the impact of deeper filter feeders, such as giant larvaceans, have been unsuccessful. Giant larvaceans occupy the upper 400 m of the water column, where they build complex mucus filtering structures that reach diameters greater than 1 m. Because of the fragility of these structures, direct measurements of filtration rates require in situ methods. Hence, we developed DeepPIV, an instrument deployed from a remotely operated vehicle that enables the direct measurement of in situ filtration rates. The rates measured for giant larvaceans exceed those of any other zooplankton filter feeder. Given these filtration rates and abundance data from a 22-year time series, the grazing impact of giant larvaceans far exceeds previous estimates, with the potential for processing their 200-m principal depth range in Monterey Bay in as little as 13 days. Technologies such as DeepPIV will enable more accurate assessments of the long-term removal of atmospheric carbon by deep-water biota.

Two eyes for two purposes: in situ evidence for asymmetric vision in the cockeyed squids Histioteuthis heteropsis and Stigmatoteuthis dofleini.

The light environment of the mesopelagic realm of the ocean changes with both depth and viewer orientation, and this has probably driven the high diversity of visual adaptations found among its inhabitants. The mesopelagic 'cockeyed' squids of family Histioteuthidae have unusual eyes, as the left and right eyes are dimorphic in size, shape and sometimes lens pigmentation. This dimorphism may be an adaptation to the two different sources of light in the mesopelagic realm, with the large eye oriented upward to view objects silhouetted against the dim, downwelling sunlight and the small eye oriented slightly downward to view bioluminescent point sources. We used in situ video footage from remotely operated vehicles in the Monterey Submarine Canyon to observe the orientation behaviour of 152 Histioteuthis heteropsis and nine Stigmatoteuthis dofleini We found evidence for upward orientation in the large eye and slightly downward orientation in the small eye, which was facilitated by a tail-up oblique body orientation. We also found that 65% of adult H. heteropsis (n = 69) had yellow pigmentation in the lens of the larger left eye, which may be used to break the counterillumination camouflage of their prey. Finally, we used visual modelling to show that the visual returns provided by increasing eye size are much higher for an upward-oriented eye than for a downward-oriented eye, which may explain the development of this unique visual strategy.This article is part of the themed issue 'Vision in dim light'.

Combined climate- and prey-mediated range expansion of Humboldt squid (Dosidicus gigas), a large marine predator in the California Current System.

Climate-driven range shifts are ongoing in pelagic marine environments, and ecosystems must respond to combined effects of altered species distributions and environmental drivers. Hypoxic oxygen minimum zones (OMZs) in midwater environments are shoaling globally; this can affect distributions of species both geographically and vertically along with predator-prey dynamics. Humboldt (jumbo) squid (Dosidicus gigas) are highly migratory predators adapted to hypoxic conditions that may be deleterious to their competitors and predators. Consequently, OMZ shoaling may preferentially facilitate foraging opportunities for Humboldt squid. With two separate modeling approaches using unique, long-term data based on in situ observations of predator, prey, and environmental variables, our analyses suggest that Humboldt squid are indirectly affected by OMZ shoaling through effects on a primary food source, myctophid fishes. Our results suggest that this indirect linkage between hypoxia and foraging is an important driver of the ongoing range expansion of Humboldt squid in the northeastern Pacific Ocean.

First in situ observations of the deep-sea squid Grimalditeuthis bonplandi reveal unique use of tentacles.

The deep-sea squid Grimalditeuthis bonplandi has tentacles unique among known squids. The elastic stalk is extremely thin and fragile, whereas the clubs bear no suckers, hooks or photophores. It is unknown whether and how these tentacles are used in prey capture and handling. We present, to our knowledge, the first in situ observations of this species obtained by remotely operated vehicles (ROVs) in the Atlantic and North Pacific. Unexpectedly, G. bonplandi is unable to rapidly extend and retract the tentacle stalk as do other squids, but instead manoeuvres the tentacles by undulation and flapping of the clubs' trabecular protective membranes. These tentacle club movements superficially resemble the movements of small marine organisms and suggest the possibility that G. bonplandi uses aggressive mimicry by the tentacle clubs to lure prey, which we find to consist of crustaceans and cephalopods. In the darkness of the meso- and bathypelagic zones the flapping and undulatory movements of the tentacle may: (i) stimulate bioluminescence in the surrounding water, (ii) create low-frequency vibrations and/or (iii) produce a hydrodynamic wake. Potential prey of G. bonplandi may be attracted to one or more of these as signals. This singular use of the tentacle adds to the diverse foraging and feeding strategies known in deep-sea cephalopods.

Oceanographic and biological effects of shoaling of the oxygen minimum zone.

Long-term declines in oxygen concentrations are evident throughout much of the ocean interior and are particularly acute in midwater oxygen minimum zones (OMZs). These regions are defined by extremely low oxygen concentrations (<20-45 µmol kg(-1)), cover wide expanses of the ocean, and are associated with productive oceanic and coastal regions. OMZs have expanded over the past 50 years, and this expansion is predicted to continue as the climate warms worldwide. Shoaling of the upper boundaries of the OMZs accompanies OMZ expansion, and decreased oxygen at shallower depths can affect all marine organisms through multiple direct and indirect mechanisms. Effects include altered microbial processes that produce and consume key nutrients and gases, changes in predator-prey dynamics, and shifts in the abundance and accessibility of commercially fished species. Although many species will be negatively affected by these effects, others may expand their range or exploit new niches. OMZ shoaling is thus likely to have major and far-reaching consequences.