Colonization of the deep sea by fishes.

Analysis of maximum depth of occurrence of 11 952 marine fish species shows a global decrease in species number (N) with depth (x; m): log10 N = -0·000422x + 3·610000 (r(2) = 0·948). The rate of decrease is close to global estimates for change in pelagic and benthic biomass with depth (-0·000430), indicating that species richness of fishes may be limited by food energy availability in the deep sea. The slopes for the Classes Myxini (-0·000488) and Actinopterygii (-0·000413) follow this trend but Chondrichthyes decrease more rapidly (-0·000731) implying deficiency in ability to colonize the deep sea. Maximum depths attained are 2743, 4156 and 8370 m for Myxini, Chondrichthyes and Actinopterygii, respectively. Endemic species occur in abundance at 7-7800 m depth in hadal trenches but appear to be absent from the deepest parts of the oceans, >9000 m deep. There have been six global oceanic anoxic events (OAE) since the origin of the major fish taxa in the Devonian c. 400 million years ago (mya). Colonization of the deep sea has taken place largely since the most recent OAE in the Cretaceous 94 mya when the Atlantic Ocean opened up. Patterns of global oceanic circulation oxygenating the deep ocean basins became established coinciding with a period of teleost diversification and appearance of the Acanthopterygii. Within the Actinopterygii, there is a trend for greater invasion of the deep sea by the lower taxa in accordance with the Andriashev paradigm. Here, 31 deep-sea families of Actinopterygii were identified with mean maximum depth >1000 m and with >10 species. Those with most of their constituent species living shallower than 1000 m are proposed as invasive, with extinctions in the deep being continuously balanced by export of species from shallow seas. Specialized families with most species deeper than 1000 m are termed deep-sea endemics in this study; these appear to persist in the deep by virtue of global distribution enabling recovery from regional extinctions. Deep-sea invasive families such as Ophidiidae and Liparidae make the greatest contribution to fish fauna at depths >6000 m.

Diet and feeding niches of juvenile Gadus morhua, Melanogrammus aeglefinus and Merlangius merlangus during the settlement transition in the northern North Sea.

A study on the feeding ecology of juvenile cod Gadus morhua, haddock Melanogrammus aeglefinus and whiting Merlangius merlangus during the pelagic to demersal transition was carried out on fishes sampled throughout their settlement season at a local nursery ground in the north-western North Sea, off the Scottish east coast. A comprehensive quantitative taxonomic analysis of the diets, as described in the paper, showed the emergence of distinctive feeding niches, minimizing the potential for competition between species and size categories. The diet of the juveniles changed with fish size, water depth, time of year and distance offshore. Small G. morhua were present in the study area earlier in the season, settled further inshore and ate a higher proportion of pelagic prey (copepods) and as size increased they moved into deeper waters and targeted larger, more benthic prey. As M. aeglefinus grew larger and moved into deeper waters, a diet of largely copepods, amphipods, pelagic Ammodytes spp., cyprids and pelagic gastropods evolved to one dominated predominantly by fishes and benthic invertebrates. In the case of M. merlangus, widespread ages and sizes throughout the sampling season, a consequence of their more protracted spawning season, resulted in dietary changes which were more likely to be influenced by seasonal changes in the prey field, in addition to developmental (size) changes, than the diets of the other two species.

Scavenging interactions between the arrow tooth eel Synaphobranchus kaupii and the Portuguese dogfish Centroscymnus coelolepis.

A scavenging interaction between the arrow tooth eel Synaphobranchus kaupii and the Portuguese dogfish Centroscymnus coelolepis, both ubiquitous components of fish assemblages at bathyal depths, was observed. Using a baited camera between 1297 and 2453 m in the eastern Atlantic Ocean continental slope, it was shown that despite consistently rapid arrival times of S. kaupii (<5 min), their feeding bouts (indicated by acute peak in numbers) did not take place until shortly after C. coelolepis arrived and removed the exterior surface of the bait (skipjack tuna Katsuwonus pelamis carcass). Change in the numbers of S. kaupii was hence dependent on the arrival of a more powerful scavenger throughout the study site, and at the deeper stations where the population of C. coelolepis declined, S. kaupii was observed to be present but waited for >2 h before feeding, thus contradicting conventional scavenging assumptions in the presence of a food fall.

Long-term changes in deep-water fish populations in the northeast Atlantic: a deeper reaching effect of fisheries?

A severe scarcity of life history and population data for deep-water fishes is a major impediment to successful fisheries management. Long-term data for non-target species and those living deeper than the fishing grounds are particularly rare. We analysed a unique dataset of scientific trawls made from 1977 to 1989 and from 1997 to 2002, at depths from 800 to 4800 m. Over this time, overall fish abundance fell significantly at all depths from 800 to 2500 m, considerably deeper than the maximum depth of commercial fishing (approx. 1600 m). Changes in abundance were significantly larger in species whose ranges fell at least partly within fished depths and did not appear to be consistent with any natural factors such as changes in fluxes from the surface or the abundance of potential prey. If the observed decreases in abundance are due to fishing, then its effects now extend into the lower bathyal zone, resulting in declines in areas that have been previously thought to be unaffected. A possible mechanism is impacts on the shallow parts of the ranges of fish species, resulting in declines in abundance in the lower parts of their ranges. This unexpected phenomenon has important consequences for fisheries and marine reserve management, as this would indicate that the impacts of fisheries can be transmitted into deep offshore areas that are neither routinely monitored nor considered as part of the managed fishery areas.

Liparid and macrourid fishes of the hadal zone: in situ observations of activity and feeding behaviour.

Using baited camera landers, the first images of living fishes were recorded in the hadal zone (6000-11000 m) in the Pacific Ocean. The widespread abyssal macrourid Coryphaenoides yaquinae was observed at a new depth record of approximately 7000 m in the Japan Trench. Two endemic species of liparid were observed at similar depths: Pseudoliparis amblystomopsis in the Japan Trench and Notoliparis kermadecensis in the Kermadec Trench. From these observations, we have documented swimming and feeding behaviour of these species and derived the first estimates of hadal fish abundance. The liparids intercepted bait within 100-200 min but were observed to preferentially feed on scavenging amphipods. Notoliparis kermadecensis act as top predators in the hadal food web, exhibiting up to nine suction-feeding events per minute. Both species showed distinctive swimming gaits: P. amblystomopsis (mean length 22.5 cm) displayed a mean tail-beat frequency of 0.47 Hz and mean caudal:pectoral frequency ratio of 0.76, whereas N. kermadecensis (mean length 31.5 cm) displayed respective values of 1.04 and 2.08 Hz. Despite living at extreme depths, these endemic liparids exhibit similar activity levels compared with shallow-water liparids.

Trends in body size across an environmental gradient: a differential response in scavenging and non-scavenging demersal deep-sea fish.

Body size trends across environmental gradients are widely reported but poorly understood. Here, we investigate contrasting relationships between size (body mass) and depth in the scavenging and predatory demersal ichthyofauna (800-4800 m) of the North-east Atlantic. The mean size of scavenging fish, identified as those regularly attracted to baited cameras, increased significantly with depth, while in non-scavengers there was a significant decline in size. The increase in scavenger size is a consequence of both intra and inter-specific effects. The observation of opposing relationships, in different functional groups, across the same environmental gradient indicates ecological rather than physiological causes. Simple energetic models indicate that the dissimilarity can be explained by different patterns of food distribution. While food availability declines with depth for both groups, the food is likely to be in large, randomly distributed packages for scavengers and as smaller but more evenly distributed items for predators. Larger size in scavengers permits higher swimming speeds, greater endurance as a consequence of larger energy reserves and lower mass specific metabolic rate, factors that are critical to survival on sporadic food items.

Sexually dimorphic expression of glutamate decarboxylase mRNA in the hypothalamus of the deep sea armed grenadier, Coryphaenoides (Nematonurus) armatus.

Glutamate decarboxylase (GAD), is a key enzyme in the central nervous system (CNS) that synthesizes the inhibitory neurotransmitter gamma-aminobutyric acid (GABA) from glutamate. Our previous phylogenetic studies on the evolution of this enzyme indicates that there are at least two distinct forms: GAD65 and GAD67. They are the products of separate genes and probably derive from a common ancestral GAD gene following gene duplication prior to the emergence of the teleosts more than 200 Myr ago. Furthermore, a third GAD-like molecule, GAD3, discovered in the armed grenadier, Coryphaenoides (Nematonurus) armatus, is equally divergent from both GAD65 and GAD67. Specimens of C. (N.) armatus were collected by trawl at a depth of 4,000 m in the Porcupine Seabight (Northeastern Atlantic), and brains dissected and frozen for RNA extraction. All three GAD forms are found in the cerebellum, telencephalon and hypothalamus. Semiquantitative PCR analysis showed that males and females have similar levels of expression of GAD67 and GAD3 in the tissues studied. Independent of the sex examined, the levels of expression of GAD65 and GAD67 in the cerebellum were approximately half that in the telencephalon. GAD3 levels were approximately 30% higher in the cerebellum than in either the telencephalon or hypothalamus. In contrast to GAD67 and GAD3, hypothalamic expression of GAD65 mRNA is 1.8 times higher (p < 0.05) in males than in females. These data indicate that the expression of GAD65, a key enzyme for the synthesis of GABA is sexually dimorphic in females and males of C. (N.) armatus.

Multiplicity of glutamic acid decarboxylases (GAD) in vertebrates: molecular phylogeny and evidence for a new GAD paralog.

The evolution of chordate glutamic acid decarboxylase (GAD; EC 4.1.1.15), a key enzyme in the central nervous system synthesizing the neurotransmitter gamma-amino-butyric acid (GABA) from glutamate, was studied. Prior to this study, molecular data of GAD had been restricted to mammals, which express two distinct forms, GAD65 and GAD67. These are the products of separate genes and probably are derived from a common ancestral GAD following gene duplication at some point during vertebrate evolution. To enable a comprehensive phylogenetic analysis, molecular information of GAD forms in other vertebrate classes was essential. By reverse transcriptase-polymerase chain reaction (RT-PCR), partial nucleotide sequences of GAD were cloned from brains of zebra finch (Taeniopygia guttata), turtle (Trachemys scripta), goldfish (Carassius auratus), zebrafish (Danio rerio), and armoured grenadier (Coryphaenoides (Nematonurus) armatus, a deep-sea fish), and from the cerebral ganglion plus neural gland of Ciona intestinalis, a protochordate. Whereas GAD65 and GAD67 homologs were expressed in birds, reptiles, and fish, only a single GAD cDNA with equal similarities to both vertebrate GAD forms was found in the protochordate. This indicates that the duplication of the vertebrate GAD gene occurred between 400 and 560 million years ago. For both GAD65 and GAD67, the generated phylogenetic tree followed the general tree topology for the major vertebrate classes. In turtle, an alternative spliced form of GAD65, putatively encoding a truncated, nonactive GAD, was found. Furthermore, a third GAD form, which is equally divergent from both GAD65 and GAD67, is expressed in C. (N.) armatus. This third form might have originated from an ancient genome duplication specific to modern ray-finned fishes.

Melatonin receptors are present in non-optic regions of the brain of a deep-sea fish living in the absence of solar light.

Pineal melatonin hormonally transduces photoperiod to influence daily and seasonal cycles in most vertebrates (1, 2). Evidence of melatonin receptors throughout the brain of several fish species (3-5), particularly in retinorecipient structures, also indicates a role in visual processing. Despite the absence of solar light many deepsea organisms show seasonality (6-8). The presence of central melatonin receptors was investigated by quantitative in vitro autoradiography in the deep-sea fish Coryphaenoides (Nematonurus) armatus. Specific, time-dependent, saturable, high affinity and guanine nucleotide sensitive, 2-[125I]iodomelatonin binding was found over the mid-brain tegmentum and hindbrain. Competing ligand potency was iodomelatonin > melatonin >> 5-HT. Although C.(N.) armatus has well developed eyes no 2-[125I]iodomelatonin binding occurred in optic tectum, cerebellum or hypothalamus. Thus melatonin involvement in processing of visual information and control of seasonal physiology via hypothalamic areas appears to be absent in this species. The presence of central G-protein coupled receptors indicates a function for melatonin unrelated to solar light.

Role of autoantibodies in the autoimmune response to testis in rainbow trout (Salmo gairdneri).

Rainbow trout, Salmo gairdneri, passively immunized with anti-sperm antibodies developed lesions in the testis characteristic of autoimmune attack. Only animals pre-treated with Freund's complete adjuvant developed these lesions. Investigations into the possible role of autoantibodies during autoimmune attack, carried out in vitro, showed that sperm antibodies were not cytotoxic but did have an opsonic effect on macrophage phagocytosis of sperm in the presence of complement.