Deep-sea predator niche segregation revealed by combined cetacean biologging and eDNA analysis of cephalopod prey.

Fundamental insight on predator-prey dynamics in the deep sea is hampered by a lack of combined data on hunting behavior and prey spectra. Deep-sea niche segregation may evolve when predators target specific prey communities, but this hypothesis remains untested. We combined environmental DNA (eDNA) metabarcoding with biologging to assess cephalopod community composition in the deep-sea foraging habitat of two top predator cetaceans. Risso's dolphin and Cuvier's beaked whale selectively targeted distinct epi/meso- and bathypelagic foraging zones, holding eDNA of 39 cephalopod taxa, including 22 known prey. Contrary to expectation, extensive taxonomic overlap in prey spectra between foraging zones indicated that predator niche segregation was not driven by prey community composition alone. Instead, intraspecific prey spectrum differences may drive differentiation for hunting fewer, more calorific, mature cephalopods in deeper waters. The novel combination of methods presented here holds great promise to disclose elusive deep-sea predator-prey systems, aiding in their protection.

In situ observations show vertical community structure of pelagic fauna in the eastern tropical North Atlantic off Cape Verde.

Distribution patterns of fragile gelatinous fauna in the open ocean remain scarcely documented. Using epi-and mesopelagic video transects in the eastern tropical North Atlantic, which features a mild but intensifying midwater oxygen minimum zone (OMZ), we established one of the first regional observations of diversity and abundance of large gelatinous zooplankton. We quantified the day and night vertical distribution of 46 taxa in relation to environmental conditions. While distribution may be driven by multiple factors, abundance peaks of individual taxa were observed in the OMZ core, both above and below the OMZ, only above, or only below the OMZ whereas some taxa did not have an obvious distribution pattern. In the eastern eropical North Atlantic, OMZ expansion in the course of global climate change may detrimentally impact taxa that avoid low oxygen concentrations (Beroe, doliolids), but favour taxa that occur in the OMZ (Lilyopsis, phaeodarians, Cydippida, Colobonema, Haliscera conica and Halitrephes) as their habitat volume might increase. While future efforts need to focus on physiology and taxonomy of pelagic fauna in the study region, our study presents biodiversity and distribution data for the regional epi- and mesopelagic zones of Cape Verde providing a regional baseline to monitor how climate change may impact the largest habitat on the planet, the deep pelagic realm.

Trace element analysis reveals bioaccumulation in the squid Gonatus fabricii from polar regions of the Atlantic Ocean.

The boreoatlantic gonate squid (Gonatus fabricii) represents important prey for top predators-such as marine mammals, seabirds and fish-and is also an efficient predator of crustaceans and fish. Gonatus fabricii is the most abundant cephalopod in the northern Atlantic and Arctic Ocean but the trace element accumulation of this ecologically important species is unknown. In this study, trace element concentrations (Ag, As, Cd, Co, Cr, Cu, Fe, Hg, Mn, Ni, Pb, Se, and Zn) were analysed from the mantle muscle and the digestive gland tissue of juveniles, adult females, and adult males that were captured south of Disko Island off West-Greenland. To assess the feeding habitat and trophic position of this species, stable isotopes of carbon (δ13C) and nitrogen (δ15N) were measured in their muscle tissue. Mercury concentrations were positively correlated with size (mantle length) and trophic position. The Hg/Se ratio was assessed because Se has been suggested to play a protective role against Hg toxicity and showed a molar surplus of Se relative to Hg. Cadmium concentrations in the digestive gland were negatively correlated with size and trophic position (δ15N), which suggested a dietary shift from Cd-rich crustaceans towards Cd-poor fish during ontogeny. This study provides trace element concentration data for G. fabricii from Greenlandic waters, which represents baseline data for a northern cephalopod species. Within West-Greenland waters, G. fabricii appears to be an important vector for the transfer of Cd in the Arctic pelagic food web.

High cadmium and mercury concentrations in the tissues of the orange-back flying squid, Sthenoteuthis pteropus, from the tropical Eastern Atlantic.

The orange-back flying squid, Sthenoteuthis pteropus, plays an important role in the eastern tropical Atlantic Ocean (ETA) pelagic food web, as both predator and prey. Specimens of S. pteropus were caught off the Cape Verde Islands and concentrations of Ag, As, Cd, Co, Cr, Cu, Fe, Hg, Mn, Ni, Pb, Se, V, and Zn were measured in the digestive gland. Among the analysed elements, Cd showed the highest average concentration with values among the highest ever recorded in cephalopods. In addition to the digestive gland, Hg concentrations were also analysed in the buccal mass and mantle tissue. Among the three tissues, buccal mass showed the highest Hg concentrations. In females, Hg concentrations in the buccal mass were positively correlated with stable isotope ratios (δ13C and δ15N) and mantle length, showing both bioaccumulation with age and bioamplification along the trophic levels. High Cd and Hg concentrations in the digestive gland and muscle respectively would lead to elevated exposure of squid-eating top predators such as yellowfin tuna, swordfish or dolphinfish, which are commercially harvested for human consumption. This study provides a deeper understanding of the trace element contamination in an abundant and ecologically important, but poorly studied pelagic squid in the ETA.

Bathyal feasting: post-spawning squid as a source of carbon for deep-sea benthic communities.

In many oceanic carbon budgets there is a discrepancy between the energetic requirements of deep-sea benthic communities and the supply of organic matter. This suggests that there are unidentified and unmeasured food sources reaching the seafloor. During 11 deep-sea remotely operated vehicle (ROV) surveys in the Gulf of California, the remains (squid carcasses and hatched-out egg sheets) of 64 post-brooding squid were encountered. As many as 36 remains were encountered during a single dive. To our knowledge this is one of the largest numbers of natural food falls of medium-size deep-sea nekton described to date. Various deep-sea scavengers (Ophiuroidea, Holothuroidea, Decapoda, Asteroidea, Enteropneusta) were associated with the remains. Although many of the 80 examined ROV dives did not encounter dead squids or egg sheets (n = 69), and the phenomenon may be geographically and temporally restricted, our results show that dead, sinking squid transport carbon from the water column to the seafloor in the Gulf of California. Based on food fall observations from individual dives, we estimate that annual squid carcass depositions may regionally contribute from 0.05 to 12.07 mg C m-2 d-1 to the seafloor in the areas where we observed the remains. The sinking of squid carcasses may constitute a significant but underestimated carbon vector between the water column and the seafloor worldwide, because squid populations are enormous and are regionally expanding as a result of climate change and pressure on fish stocks. In the future, standardized methods and surveys in geographical regions that have large squid populations will be important for investigating the overall contribution of squid falls to regional carbon budgets.

The giant deep-sea octopus Haliphron atlanticus forages on gelatinous fauna.

Feeding strategies and predator-prey interactions of many deep-sea pelagic organisms are still unknown. This is also true for pelagic cephalopods, some of which are very abundant in oceanic ecosystems and which are known for their elaborate behaviors and central role in many foodwebs. We report on the first observations of the giant deep-sea octopus Haliphron atlanticus with prey. Using remotely operated vehicles, we saw these giant octopods holding medusae in their arms. One of the medusae could be identified as Phacellophora camtschatica (the egg-yolk jelly). Stomach content analysis confirmed predation on cnidarians and gelatinous organisms. The relationship between medusae and H. atlanticus is discussed, also in comparison with other species of the Argonautoidea, all of which have close relationships with gelatinous zooplankton.

Mating behavior of a deep-sea squid revealed by in situ videography and the study of archived specimens.

The mating behavior of deep-sea squids is shrouded in mystery. The squids for which mating has been observed use a hectocotylus, a modified arm, for the transfer of sperm packets called spermatophores. However, many deep-sea squid species lack a hectocotylus. We present the first in situ observations of mating behavior in a deep-sea squid that has no hectocotylus but instead uses an elongated terminal organ for the transfer of spermatangia, which are released from the spermatophores and burrow deeply into the female tissue. With remotely operated vehicles (ROVs), we observed two mating pairs of the deep-sea squid Pholidoteuthis adami in the Gulf of Mexico. The male adopted a peculiar position during mating, with its ventral side up and its posterior mantle above the female's head. While the male held the female in what looked like a firm grip, we observed the long terminal organ extending through the funnel of the male, contacting the female dorsal mantle. Examinations of museum specimens show that spermatangia burrow from the outer dorsal mantle into the inner dorsal mantle. This combination of serendipitous in situ observations and archived specimens can be a powerful tool for understanding the behavior of deep-sea animals.