ALBERT

Description: Highlights: • We investigated growth and longevity of three deep-sea squids from the Monterey Bay. • We found daily growth increments in the statoliths of two deep-sea squids. • The estimated longevities are higher than those of shallow water relatives. • The estimated growth rates suggest a reduced pace of life in deep-sea squids. Abstract Coastal and epipelagic cephalopods are among the fastest growing invertebrates, with life cycles of typically 1 year or less. Evidence is accumulating that deep-sea taxa often live longer and grow slower than their shallow water relatives. We test the hypothesis that deep-sea squid show increased longevity and reduced growth rates compared to coastal and epipelagic species, by validation experiments and quantification of statolith increments of three deep-sea squids from the Monterey Submarine Canyon. The periodicity of statolith increment formation in coastal species is daily, but is unknown for deep-sea squid. Between 2010 and 2013, specimens of Chiroteuthis calyx, Galiteuthis phyllura and Octopoteuthis deletron were captured by remotely operated vehicles and trawl nets off California. ROV-captured living squid were immersed in tetracycline and kept alive in the lab for between 3 and 14 days. Correlating the number of elapsed days with the number of newly deposited statolith increments, and statolith growth after the fluorescent tetracycline mark, provided evidence of regular and daily increment deposition, in C. calyx and O. deletron. This relationship was less strong in G. phyllura and the one-increment-per-day hypothesis was not accepted for this species. Reconstructing growth rates based on statolith counts and wet weights from animals of a wide size range suggest that O. deletron is a slower growing squid (0.59% BW/day) than C. calyx (1.3% BW/day) and G. phyllura (1.2% BW/day). Octopoteuthis deletron matures at around two years, the oldest C. calyx was a mature male of 1.5 years and the eldest G. phyllura was 10 months and still immature. Maximum reported sizes for G. phyllura and C. calyx exceed those of our examined specimens, and therefore their longevity likely exceeds 2 years, in particular if the females brood their eggs. Our study supports the hypothesis that deeper living squid exhibit reduced growth rates and an increased longevity compared to shallow living species. We discuss these traits in the context of a life in the deep pelagic ocean.

Description: 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.

Description: Coleoid cephalopods are thought to go through only one reproductive cycle in their life. We here report that vampire squid (Vampyroteuthis infernalis) show evidence of multiple reproductive cycles. Female vampire squid spawn their eggs, then return to a resting reproductive state, which is followed by the development of a new batch of eggs. This reproductive cycle is likely to be repeated more than twenty times. This combination of reproductive traits is different from that of any other extant coleoid cephalopod.

Description: Highlights: • In situ observations can provide valuable information on feeding behavior in deep-sea organisms. • Gonatus spp. in Monterey Bay consume mesopelagic fishes, congeners and their own species. • Sympatric species of the Gonatidae show differences in prey choice. • Cannibalism is a significant component of the diet of Gonatus spp. in Monterey Bay. Abstract: In situ observations are rarely applied in food web studies of deep-sea organisms. Using deep-sea observations obtained by remotely operated vehicles in the Monterey Submarine Canyon, we examined the prey choices of more than 100 individual squids of the genus Gonatus. Off the California coast, these squids are abundant, semelparous (one reproductive cycle) oceanic predators but their diet has remained virtually unknown. Gonatus onyx and Gonatus berryi were observed to feed on mesopelagic fishes (in particular the myctophid Stenobrachius leucopsarus) as often as on squids but inter-specific differences in feeding were apparent. Gonatids were the most common squid prey and while cannibalism occurred in both species it was particularly high in Gonatus onyx (42% of all prey items). Typically, the size of prey was similar to the size of the predator but the squids were also seen to take much larger prey. Postjuvenile gonatids are opportunistic predators that consume nektonic members of the meso-and bathypelagic communities, including their own species. Such voracious feeding is likely necessary to support the high energetic demands associated with the single reproductive event; and for females the long brooding period during which they must depend on stored resources.

Description: "Deep-sea" cephalopods are here defined as cephalopods that spend a significant part of their life cycles outside the euphotic zone. In this chapter, the state of knowledge in several aspects of deep-sea cephalopod research are summarized, including information sources for these animals, diversity and general biogeography and life cycles, including reproduction. Recommendations are made for addressing some of the remaining knowledge deficiencies using a variety of traditional and more recently developed methods. The types of oceanic gear that are suitable for collecting cephalopod specimens and images are reviewed. Many groups of deep-sea cephalopods require taxonomic reviews, ideally based on both morphological and molecular characters. Museum collections play a vital role in these revisions, and novel (molecular) techniques may facilitate new use of old museum specimens. Fundamental life-cycle parameters remain unknown for many species; techniques developed for neritic species that could potentially be applied to deep-sea cephalopods are discussed. Reproductive tactics and strategies in deep-sea cephalopods are very diverse and call for comparative evolutionary and experimental studies, but even in the twenty-first century, mature individuals are still unknown for many species. New insights into diet and trophic position have begun to reveal a more diverse range of feeding strategies than the typically voracious predatory lifestyle known for many cephalopods. Regular standardized deep-sea cephalopod surveys are necessary to provide insight into temporal changes in oceanic cephalopod populations and to forecast, verify and monitor the impacts of global marine changes and human impacts on these populations.

Description: 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.

Description: 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.

Description: Highlights: • Micronekton ecology differed between equatorial (EQ) and low-oxygen waters (LO). • The δ15N enrichment per trophic level was lower in the productive LO than in the EQ. • Migrating fauna in the LO encounter increased competition for food resources. • The δ15N values of non-migrators increased with depth in the EQ, but not in the LO. • The δ15N values of mesopelagic micronektonivores were lower in the productive LO. Abstract: The ecology of vertically migrating mesopelagic micronekton is affected by physical properties of their environment. Increased light attenuation in particle-rich productive waters, as well as low oxygen conditions decrease the migration amplitude. This likely has implications on the trophic organisation of micronekton communities, which are predominantly governed by niche partitioning in the vertical dimension. We investigated trophic structures of pelagic communities in the eastern tropical North Atlantic by comparing micronekton species assemblages from the low-oxygen region influenced by Mauritanian upwelling between 8° and 11° N (LO) and the less productive and more oxygenated equatorial area between 0 and 4°N (EQ). We analysed stable isotopes of carbon (δ13C) and nitrogen (δ15N) in body tissues of 35 species of mesopelagic fishes, four species of cephalopods, two species of cnidarians, and two species of decapods and used these values as a proxy for their trophic niche and correlated them with the traits feeding guild, migration pattern, mean depth of occurrence and body size. Our results demonstrate significant regional differences in the food web structure and vertical trophic interactions of the investigated micronekton assemblages. Diurnally migrating fishes that predominantly feed on copepods exhibited higher δ15N values in the LO (9.6‰) than in the EQ (8.9‰), reflecting changes in baseline values of pelagic tunicates. Contrary, all other Feeding – Migrator guilds show lower or similar δ15N values in the LO compared to the EQ, indicating reduced isotopic enrichment between trophic levels (TL) in the LO compared to the EQ. Further, a generally lower δ15N enrichment between TL3 – TL4 compared to TL2 – TL3 was observed (LO: TL2 – TL3: ~2.2‰, TL3 – TL4: ~1.2‰; EQ: TL2 – TL3: ~3.5‰, TL3 – TL4: ~2.2‰). Quantitative isotopic niche metrics suggest enhanced competition in trophic niche space, whereas relative isotopic niche positions indicate an increased importance of food from lower trophic levels (non-crustacean and/or gelatinous prey resources) for fishes from the LO compared to the EQ. The absence of a depth-related increase in δ15N values of partial- and nonmigrators of the LO is contrary to results from the EQ and previously published data. Low δ15N values in partially and nonmigrating micronektonivores of the LO in comparison with those of the EQ could be due to feeding on lower trophic prey components in the LO, as is indicated by an overlap in isotopic niche with that of partially and nonmigrating mixed crustacean feeders in the LO. Alternatively, driving mechanisms could be the consumption of prey from shallower waters, regional differences in δ15N enrichment, species-specific ecological differences or a combination of these processes. Each of these explanations is likely tightly correlated to a vertical biogeochemical structuring effect of low oxygen midwater layers fuelled by high nitrate inputs from the Mauritanian upwelling region. Our study provides crucial ecological insights for a better understanding of large-scale gradients in micronekton migration patterns.

Description: Highlights: • The pace of life of life of vampire squid and Japetella were examined. • Japetella diaphana and Vampyroteuthis infernalis have contrasting reproductive strategies. • Brooding in Japetella is estimated to last for two years in water temperature ~4 °C. • Feeding ecology and metabolic rates suggest non-daily deposition of beak growth increments. • Both species’ life-history traits suggest a slow pace of life and longer lifespans.The pelagic cephalopods Japetella diaphana and Vampyroteuthis infernalis are charismatic and widely distributed members of deep pelagic ecosystems. Their habitat temperatures, metabolic rates, feeding and reproductive strategies all together suggest that the pace of life in these species is reduced when compared to neritic octopod species, but information on longevity, growth rates and age estimations are absent to date. To estimate the pace of life in pelagic octopods, this study investigated size at maturity, reproductive strategy, and the number of growth-increments in the upper beak lateral walls (LWS) of J. diaphana (an octopod) and V. infernalis (a vampyromorph). Daily deposition of growth increments in hard body structures (e.g., beaks and stylets) has been validated experimentally in some temperate and tropical octopods, but remains unquantified and not yet validated for most deep-sea and high-latitude cephalopods. We used a diverse assemblage of specimens ranging from early juveniles to adults for both species. Mature J. diaphana had a mantle length (ML) of 53–144 mm and a body mass (BM) of 18–235 g. A brooding female of J. diaphana captured at 1352 m in the Gulf of California was carrying 1419 eggs in pre-organogenetic stage that measured ~2.5 mm in diameter. The size range of mature V. infernalis was ML 66–122 mm and BM 34–286 g. The number of growth increments in the beaks ranged from 21 to 207 in J. diaphana and from 89 to 375 in V. infernalis. If the growth increments are formed daily, like in tropical octopod species, age estimates are incongruent with the low metabolic rates and reproductive strategies of the two species. These observations suggest that growth increments may require more than one day to be formed. To better understand the life histories of invertebrates in the largest but least studied habitat on the planet, age and growth validation studies are critical.