Insights on long-term ecosystem changes from stable isotopes in historical squid beaks.

BACKGROUND: Assessing the historical dynamics of key food web components is crucial to understand how climate change impacts the structure of Arctic marine ecosystems. Most retrospective stable isotopic studies to date assessed potential ecosystem shifts in the Arctic using vertebrate top predators and filter-feeding invertebrates as proxies. However, due to long life histories and specific ecologies, ecosystem shifts are not always detectable when using these taxa. Moreover, there are currently no retrospective stable isotopic studies on various other ecological and taxonomic groups of Arctic biota. To test whether climate-driven shifts in marine ecosystems are reflected in the ecology of short-living mesopredators, ontogenetic changes in stable isotope signatures in chitinous hard body structures were analysed in two abundant squids (Gonatus fabricii and Todarodes sagittatus) from the low latitude Arctic and adjacent waters, collected between 1844 and 2023. RESULTS: We detected a temporal increase in diet and habitat-use generalism (= opportunistic choice rather than specialization), trophic position and niche width in G. fabricii from the low latitude Arctic waters. These shifts in trophic ecology matched with the Atlantification of the Arctic ecosystems, which includes increased generalization of food webs and higher primary production, and the influx of boreal species from the North Atlantic as a result of climate change. The Atlantification is especially marked since the late 1990s/early 2000s. The temporal patterns we found in G. fabricii's trophic ecology were largely unreported in previous Arctic retrospective isotopic ecology studies. Accordingly, T. sagittatus that occur nowadays in the high latitude North Atlantic have a more generalist diet than in the XIXth century. CONCLUSIONS: Our results suggest that abundant opportunistic mesopredators with short life cycles (such as squids) are good candidates for retrospective ecology studies in the marine ecosystems, and to identify ecosystem shifts driven by climate change. Enhanced generalization of Arctic food webs is reflected in increased diet generalism and niche width in squids, while increased abundance of boreal piscivorous fishes is reflected in squids' increased trophic position. These findings support opportunism and adaptability in squids, which renders them as potential winners of short-term shifts in Arctic ecosystems.

Experimental mining plumes and ocean warming trigger stress in a deep pelagic jellyfish.

The deep pelagic ocean is increasingly subjected to human-induced environmental change. While pelagic animals provide important ecosystem functions including climate regulation, species-specific responses to stressors remain poorly documented. Here, we investigate the effects of simulated ocean warming and sediment plumes on the cosmopolitan deep-sea jellyfish Periphylla periphylla, combining insights gained from physiology, gene expression and changes in associated microbiota. Metabolic demand was elevated following a 4 °C rise in temperature, promoting genes related to innate immunity but suppressing aerobic respiration. Suspended sediment plumes provoked the most acute and energetically costly response through the production of excess mucus (at ≥17 mg L-1), while inducing genes related to aerobic respiration and wound repair (at ≥167 mg L-1). Microbial symbionts appeared to be unaffected by both stressors, with mucus production maintaining microbial community composition. If these responses are representative for other gelatinous fauna, an abundant component of pelagic ecosystems, the effects of planned exploitation of seafloor resources may impair deep pelagic biodiversity and ecosystem functioning.

Miles down for lunch: deep-sea in situ observations of Arctic finned octopods Cirroteuthis muelleri suggest pelagic-benthic feeding migration.

Deep-sea cephalopods are diverse, abundant, and poorly understood. The Cirrata are gelatinous finned octopods and among the deepest-living cephalopods ever recorded. Their natural feeding behaviour remains undocumented. During deep-sea surveys in the Arctic, we observed Cirroteuthis muelleri. Octopods were encountered with their web spread wide, motionless and drifting in the water column 500-2600 m from the seafloor. Individuals of C. muelleri were also repeatedly observed on the seafloor where they exhibited a repeated, behavioural sequence interpreted as feeding. The sequence (11-21 s) consisted of arm web spreading, enveloping and retreating. Prey capture happened during the enveloping phase and lasted 5-49 s. Numerous traces of feeding activity were also observed on the seafloor. The utilization of the water column for drifting and the deep seafloor for feeding is a novel migration behaviour for cephalopods, but known from gelatinous fishes and holothurians. By benthic feeding, the octopods benefit from the enhanced nutrient availability on the seafloor. Drifting in the water column may be an energetically efficient way of transportation while simultaneously avoiding seafloor-associated predators. In situ observations are indispensable to discover the behaviour of abundant megafauna, and the energetic coupling between the pelagic and benthic deep sea.

Deep-sea impacts of climate interventions.

Ocean manipulation to mitigate climate change may harm deep-sea ecosystems.

Making marine image data FAIR.

Underwater images are used to explore and monitor ocean habitats, generating huge datasets with unusual data characteristics that preclude traditional data management strategies. Due to the lack of universally adopted data standards, image data collected from the marine environment are increasing in heterogeneity, preventing objective comparison. The extraction of actionable information thus remains challenging, particularly for researchers not directly involved with the image data collection. Standardized formats and procedures are needed to enable sustainable image analysis and processing tools, as are solutions for image publication in long-term repositories to ascertain reuse of data. The FAIR principles (Findable, Accessible, Interoperable, Reusable) provide a framework for such data management goals. We propose the use of image FAIR Digital Objects (iFDOs) and present an infrastructure environment to create and exploit such FAIR digital objects. We show how these iFDOs can be created, validated, managed and stored, and which data associated with imagery should be curated. The goal is to reduce image management overheads while simultaneously creating visibility for image acquisition and publication efforts.

Rapid Range Expansion of a Marine Ectotherm Reveals the Demographic and Ecological Consequences of Short-Term Variability in Seawater Temperature and Dissolved Oxygen.

AbstractThe distributions of marine ectotherms are governed by physiological sensitivities to long-term trends in seawater temperature and dissolved oxygen. Short-term variability in these parameters has the potential to facilitate rapid range expansions, and the resulting ecological and socioeconomic consequences may portend those of future marine communities. Here, we combine physiological experiments with ecological and demographic surveys to assess the causes and consequences of sudden but temporary poleward range expansions of a marine ectotherm with considerable life history plasticity (California market squid, Doryteuthis opalescens). We show that sequential factors related to resource accessibility in the core range-the buildup of large populations as a result of competitive release and climate-associated temperature increase and oxygen loss that constrain aerobic activity-may drive these expansions. We also reveal that poleward range expansion alters the body size-and therefore trophic role-of invading populations, with potential negative implications for socioeconomically valuable resident species. To help forecast rapid range expansions of marine ectotherms, we advocate that research efforts focus on factors impacting resource accessibility in core ranges. Determining how environmental conditions in receiving ecosystems affect body size and how body size is related to trophic role will help refine estimates of the impacts of future marine communities.

Pelagic observations of the midwater scorpionfish Ectreposebastes imus (Setarchidae) suggests a role in trophic coupling between deep-sea habitats.

During pelagic video transects off Santo Antão, Cabo Verde, we encountered the midwater scorpionfish Ectreposebastes imus in midwater between 300 and 800 m over a bottom depth of about 1000 m. The fish were typically positioned vertically with their heads pointing upwards. These first midwater observations of E. imus suggest migratory (potentially feeding) behaviour into the pelagic realm and hence a possible role of this species in the trophic coupling between the pelagic and benthic habitats in the deep seas of Cabo Verde and elsewhere in its global distribution.

A novel metabarcoding primer pair for environmental DNA analysis of Cephalopoda (Mollusca) targeting the nuclear 18S rRNA region.

Cephalopods are pivotal components of marine food webs, but biodiversity studies are hampered by challenges to sample these agile marine molluscs. Metabarcoding of environmental DNA (eDNA) is a potentially powerful technique to study oceanic cephalopod biodiversity and distribution but has not been applied thus far. We present a novel universal primer pair for metabarcoding cephalopods from eDNA, Ceph18S (Forward: 5'-CGC GGC GCT ACA TAT TAG AC-3', Reverse: 5'-GCA CTT AAC CGA CCG TCG AC-3'). The primer pair targets the hypervariable region V2 of the nuclear 18S rRNA gene and amplifies a relatively short target sequence of approximately 200 bp in order to allow the amplification of degraded DNA. In silico tests on a reference database and empirical tests on DNA extracts from cephalopod tissue estimate that 44-66% of cephalopod species, corresponding to about 310-460 species, can be amplified and identified with this primer pair. A multi-marker approach with the novel Ceph18S and two previously published cephalopod mitochondrial 16S rRNA primer sets targeting the same region (Jarman et al. 2006 Mol. Ecol. Notes. 6, 268-271; Peters et al. 2015 Mar. Ecol. 36, 1428-1439) is estimated to amplify and identify 89% of all cephalopod species, of which an estimated 19% can only be identified by Ceph18S. All sequences obtained with Ceph18S were submitted to GenBank, resulting in new 18S rRNA sequences for 13 cephalopod taxa.

Strange eyes, stranger brains: exceptional diversity of optic lobe organization in midwater crustaceans.

Nervous systems across Animalia not only share a common blueprint at the biophysical and molecular level, but even between diverse groups of animals the structure and neuronal organization of several brain regions are strikingly conserved. Despite variation in the morphology and complexity of eyes across malacostracan crustaceans, many studies have shown that the organization of malacostracan optic lobes is highly conserved. Here, we report results of divergent evolution to this 'neural ground pattern' discovered in hyperiid amphipods, a relatively small group of holopelagic malacostracan crustaceans that possess an unusually wide diversity of compound eyes. We show that the structure and organization of hyperiid optic lobes has not only diverged from the malacostracan ground pattern, but is also highly variable between closely related genera. Our findings demonstrate a variety of trade-offs between sensory systems of hyperiids and even within the visual system alone, thus providing evidence that selection has modified individual components of the central nervous system to generate distinct combinations of visual centres in the hyperiid optic lobes. Our results provide new insights into the patterns of brain evolution among animals that live under extreme conditions.

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.

A draft genome sequence of the elusive giant squid, Architeuthis dux.

BACKGROUND: The giant squid (Architeuthis dux; Steenstrup, 1857) is an enigmatic giant mollusc with a circumglobal distribution in the deep ocean, except in the high Arctic and Antarctic waters. The elusiveness of the species makes it difficult to study. Thus, having a genome assembled for this deep-sea-dwelling species will allow several pending evolutionary questions to be unlocked. FINDINGS: We present a draft genome assembly that includes 200 Gb of Illumina reads, 4 Gb of Moleculo synthetic long reads, and 108 Gb of Chicago libraries, with a final size matching the estimated genome size of 2.7 Gb, and a scaffold N50 of 4.8 Mb. We also present an alternative assembly including 27 Gb raw reads generated using the Pacific Biosciences platform. In addition, we sequenced the proteome of the same individual and RNA from 3 different tissue types from 3 other species of squid (Onychoteuthis banksii, Dosidicus gigas, and Sthenoteuthis oualaniensis) to assist genome annotation. We annotated 33,406 protein-coding genes supported by evidence, and the genome completeness estimated by BUSCO reached 92%. Repetitive regions cover 49.17% of the genome. CONCLUSIONS: This annotated draft genome of A. dux provides a critical resource to investigate the unique traits of this species, including its gigantism and key adaptations to deep-sea environments.

Life histories of Antarctic incirrate octopods (Cephalopoda: Octopoda).

As a general trend in the life history of marine organisms, species inhabiting cold waters have reduced growth rates and increased lifespans. Studies based on egg sizes and brooding times of deep-sea and polar octopods support this hypothesis, but empirical data on growth are still scarce. To test the hypothesis that octopods inhabiting cold waters (< 3°C) live longer than temperate and warm water species, this study investigated size-at-age, maturation and growth rates in incirrate Antarctic octopods. Octopod age was estimated via the interpretation and quantification of beak growth increments, which in shallow water octopods have been validated to be formed on a daily basis. Specimens from the families Megaleledonidae (Adelieledone spp., Pareledone spp. and Megaleledone setebos) and Enteroctopodidae (Muusoctopus rigbyae) were collected on the shelf and slope regions off the Antarctic Peninsula during a cruise in 2012. Examined specimens included early juveniles to animals in advanced maturity. The total number of growth increments ranged from 192-599 in Pareledone aequipapillae (body mass [BM] 2-109 g), 182-431 in Pareledone charcoti (BM 5-124 g), 98-906 in M. setebos (BM 10-6000 g) and 207-425 in M. rigbyae (BM 24-256 g). After the cruise, eleven specimens of P. charcoti were kept alive in captivity for more than 12 months and these animals had 219-364 growth increments, suggesting that increment formation in this species takes longer than one day. The complex population structure (size, age and maturity range) of the specimens that were captured during a relatively short time, the number of beak increments quantified, and the preliminary validation observations indicate that Antarctic octopods do not deposit increments daily, and may have lifespans exceeding 3 years. These findings corroborate the general trend that cold water molluscs have a longer lifespan than their warm water relatives.

TuLUMIS - a tunable LED-based underwater multispectral imaging system.

Multispectral imaging (MSI) is widely used in terrestrial applications to help increase the discriminability between objects of interest. While MSI has shown potential for underwater geological and biological surveys, it is thus far rarely applied underwater. This is primarily due to the fact light propagation in water is subject to wavelength dependent attenuation and tough working conditions in the deep ocean. In this paper, a novel underwater MSI system based on a tunable light source is presented which employs a monochrome still image camera with flashing, pressure neutral color LEDs. Laboratory experiments and field tests were performed. Results from the lab experiments show an improvement of 76.66% on discriminating colors on a checkerboard by using the proposed imaging system over the use of an RGB camera. The field tests provided in situ MSI observations of pelagic fauna, and showed the first evidence that the system is capable of acquiring useful imagery under real marine conditions.

In situ observations lead to the discovery of the large ctenophore Kiyohimea usagi (Lobata: Eurhamphaeidae) in the eastern tropical Atlantic.

We report on the first records of Kiyohimea usagi Matsumoto Robison 1992 (Ctenophora; Eurhamphaeidae) in the Atlantic Ocean. This large, fragile ctenophore cannot be captured by nets, and can only be studied in its natural habitat, the pelagic ocean. In the eastern Atlantic, in the Cape Verde region, in situ observations were obtained using the manned submersible JAGO and a towed pelagic observation system. Between 2015 and 2018 we documented 10 individuals which were encountered between 47-590 m depth. A description of the gastrovascular canal system is provided and potential feeding behavior is discussed. Our study confirms how in situ observations in the poorly explored pelagic realm will lead to the discovery of relatively large and previously undocumented fauna.

Diet and stable isotope analyses reveal the feeding ecology of the orangeback squid Sthenoteuthis pteropus (Steenstrup 1855) (Mollusca, Ommastrephidae) in the eastern tropical Atlantic.

In the eastern tropical Atlantic, the orangeback flying squid Sthenoteuthis pteropus (Steenstrup 1855) (Cephalopoda, Ommastrephidae) is a dominant species of the epipelagic nekton community. This carnivore squid has a short lifespan and is one of the fastest-growing squids. In this study, we characterise the role of S. pteropus in the pelagic food web of the eastern tropical Atlantic by investigating its diet and the dynamics of its feeding habits throughout its ontogeny and migration. During three expeditions in the eastern tropical Atlantic in 2015, 129 specimens were caught by hand jigging. Stomach content analyses (via visual identification and DNA barcoding) were combined with stable isotope data (∂15N and ∂13C) of muscle tissue to describe diet, feeding habits and trophic ecology of S. pteropus. Additionally, stable isotope analyses of incremental samples along the squid's gladius-the chitinous spiniform structure supporting the muscles and organs-were carried out to explore possible diet shifts through ontogeny and migration. Our results show that S. pteropus preys mainly on myctophid fishes (e.g. Myctophum asperum, Myctophum nitidulum, Vinciguerria spp.), but also on other teleost species, cephalopods (e.g. Enoploteuthidae, Bolitinidae, Ommastrephidae), crustaceans and possibly on gelatinous zooplankton as well. The squid shows a highly opportunistic feeding behaviour that includes cannibalism. Our study indicates that the trophic position of S. pteropus may increase by approximately one trophic level from a mantle length of 15 cm to 47 cm. The reconstructed isotope-based feeding chronologies of the gladii revealed high intra- and inter-individual variability in the squid's trophic position and foraging area. These findings are not revealed by diet or muscle tissue stable isotope analysis. This suggests a variable and complex life history involving individual variation and migration. The role of S. pteropus in transferring energy and nutrients from lower to higher trophic levels may be underestimated and important for understanding how a changing ocean impacts food webs in the eastern Atlantic.

Association of deep-sea incirrate octopods with manganese crusts and nodule fields in the Pacific Ocean.

Incirrate octopods (those without fins) are among the larger megafauna inhabiting the benthic environments of all oceans, commonly in water depths down to about 3,000 m. They are known to protect and brood their eggs until the juveniles hatch, but to date there is little published information on octopod deep-sea life cycles and distribution. For this study, three manganese-crust and nodule-abundant regions of the deep Pacific were examined by remote operated-vehicle and towed camera surveys carried out between 2011 and 2016. Here, we report that the depth range of incirrate octopods can now be extended to at least 4,290 m. Octopods (twenty-nine individuals from two distinct species) were observed on the deep Ka'ena and Necker Ridges of the Hawaiian Archipelago, and in a nodule-abundant region of the Peru Basin. Two octopods were observed to be brooding clutches of eggs that were laid on stalks of dead sponges attached to nodules at depths exceeding 4,000 m. This is the first time such a specific mineral-biota association has been observed for incirrate octopods. Both broods consisted of approximately 30 large (2.0-2.7 cm) eggs. Given the low annual water temperature of 1.5oC, it is likely that egg development, and hence brooding, takes years [1]. Stalked-sponge fauna in the Peru Basin require the presence of manganese nodules as a substrate, and near total collapse of such sponge populations was observed following the experimental removal of nodules within the DISCOL (DISturbance and COLonisation) area of the Peru Basin [2]. Stalked fauna are also abundant on the hard substrates of the Hawaiian archipelago. The brooding behavior of the octopods we observed suggests that, like the sponges, they may also be susceptible to habitat loss following the removal of nodule fields and crusts by commercial exploitation.

Lubricating the swordfish head.

The swordfish is reputedly the fastest swimmer on Earth. The concave head and iconic sword are unique characteristics, but how they contribute to its speed is still unknown. Recent computed tomography scans revealed a poorly mineralised area near the base of the rostrum. Here we report, using magnetic resonance imaging and electron microscopy scanning, the discovery of a complex organ consisting of an oil-producing gland connected to capillaries that communicate with oil-excreting pores in the skin of the head. The capillary vessels transport oil to abundant tiny circular pores that are surrounded by denticles. The oil is distributed from the pores over the front part of the head. The oil inside the gland is identical to that found on the skin and is a mixture of methyl esters. We hypothesize that the oil layer, in combination with the denticles, creates a super-hydrophobic layer that reduces streamwise friction drag and increases swimming efficiency.