Bioluminescent Prey Research Articles

Spies of the deep: An animal-borne active sonar and bioluminescence tag to characterise mesopelagic prey size and behaviour in distinct oceanographic domains

Mesopelagic fishes, a central component of marine trophic networks, play a fundamental role in marine ecosystems. However, as they live in highly inaccessible environments, little information is currently available on their distribution and abundance. The emergence of biologging technologies has made it possible to use deep-diving predators as bio-samplers of their environment in under-sampled regions. In this work, we deployed an innovative miniaturised sonar tag that combines active acoustics with high-resolution GPS, pressure, movement and light sensors on Southern elephant seals, a deep-diving predator feeding on mesopelagic prey. Seals were also equipped with Conductivity-Temperature-Depth tags. Salinity and temperature depth profiles were used to define oceanographic domains, allowing us to explore distribution and ecology of mesopelagic prey targeted by seals and the seals’ foraging behaviour. We highlighted strong vertical differences in prey characteristics and behaviour, with larger, more evasive and less bioluminescent prey in deeper waters. Moreover, prey encountered in warmer waters were found deeper, were more evasive and displayed a more marked diel vertical migration behaviour compared to prey encountered in colder waters, suggesting that prey accessibility and characteristics differ according to oceanographic domains. This study highlights the usefulness of the sonar-bioluminescence tag to infer mesopelagic prey distribution and habitat when deployed on deep-diving predators such as elephant seals.

Flash and grab: deep-diving southern elephant seals trigger anti-predator flashes in bioluminescent prey.

ABSTRACTBioluminescence, which occurs in approximately 80% of the world's mesopelagic fauna, can take the form of a low-intensity continuous glow (e.g. for counter-illumination or signalling) or fast repetitions of brighter anti-predatory flashes. The southern elephant seal (SES) is a major consumer of mesopelagic organisms, in particular the abundant myctophid fish, yet the fine-scale relationship between this predator's foraging behaviour and bioluminescent prey remains poorly understood. We hypothesised that brief, intense light emissions should be closely connected with prey strikes when the seal is targeting bioluminescent prey that reacts by emitting anti-predator flashes. To test this, we developed a biologging device containing a fast-sampling light sensor together with location and movement sensors to measure simultaneously anti-predator bioluminescent emissions and the predator's attack motions with a 20 ms resolution. Tags were deployed on female SES breeding at Kerguelen Islands and Península Valdés, Argentina. In situ light levels in combination with duration of prey capture attempts indicated that seals were targeting a variety of prey types. For some individuals, bioluminescent flashes occurred in a large proportion of prey strikes, with the timing of flashes closely connected with the predator's attack motion, suggestive of anti-predator emissions. Marked differences across individuals and location indicate that SES do exploit bioluminescent organisms but the proportion of these in the diet varies widely with location. The combination of wideband light and acceleration data provides new insight into where and when different prey types are encountered and how effectively they might be captured.

Viscosity has dichotomous effects on Bdellovibrio bacteriovorus HD100 predation.

Bdellovibrio bacteriovorus HD100 is a highly motile predatory bacterium that consumes other Gram-negative bacteria for its sustenance. Here, we describe the impacts the media viscosity has both on the motility of predator and its attack rates. Experiments performed in polyethylene glycol (PEG) solutions, a linear polymer, found a viscosity of 10 mPa s (5% PEG) negatively impacted predation over a 24-h period. When the viscosity was increased to 27 mPa s (10% PEG), predation was nearly abolished. Tests with three other B. bacteriovorus strains, i.e., 109J and two natural isolates, found identical results. Short-term (2-h) experiments, however, found attack rates were improved in 1% PEG, which had a viscosity of 5.4 mPa s, using bioluminescent prey and their viabilities. In contrast, when experiments were performed in dextran, a branched polymer, no increase in predation was seen even though the viscosity was a comparable 5.1 mPa s. The enhanced attack rates in this solution coincided with a 31% increase in B. bacteriovorus HD100 swimming speeds (62 μm s-1 in 1% PEG vs. 47.5 μm s-1 in HEPES-salt).

A new halisaurine mosasaur (Squamata: Halisaurinae) from Japan: the first record in the western Pacific realm and the first documented insights into binocular vision in mosasaurs

A specimen of a halisaurine mosasaur is reported from Japan for the first time, closing the pre-existing biogeographical gap between the Middle East and the eastern Pacific. Phosphorosaurus ponpetelegans sp. nov., from the lowermost Maastrichtian of Hokkaido, has been assigned to the genus Phosphorosaurus for sharing the following suite of major cranial characters with P. ortliebi, the type species from Belgium: apex of posterodorsal triangular plateau on frontal reaching level of interorbital constriction; frontal lateral border forming a step-like junction between interorbital and preorbital segments of frontal; preorbital segment of frontal sloping anteroventrally; and stapedial meatus parallel-sided in latero-medial view. Potential autapomorphies that distinguish P. ponpetelegans from other members of Halisaurinae include: postorbitofrontal jugal process elongate and stalk-like, projecting laterally; this process distally bearing a ventrally facing depression for jugal articulation; and lateral surangular–articular suture angular rather than round. The long and laterally projecting jugal processes, when combined with a depressed as well as narrow snout, provide compelling evidence for well-developed binocular vision for the new mosasaur, with an estimated binocular field of view (BFoV) of 35°. This value is unusually high for non-ophidian squamates that typically exhibit a BFoV of 10—20°, and is higher than those of other measured mosasaur taxa by at least 5°. Among colubrid snakes, nocturnal species exhibit greater BFoV than diurnal ones in both arboreal and terrestrial taxa. Known also from the Maastrichtian of Hokkaido are fossils of lantern fish (myctophids) and 10-armed cephalopods (coleoids), both of which are typically bioluminescent today. It is hence proposed that the exceptionally large, forward-facing eyes of P. ponpetelegans may well have been a special adaptation for a nocturnal lifestyle, where they hunted small, bioluminescent prey at night while avoiding direct competition with larger, more piscine mosasaurine taxa such as Mosasaurus hobetsuensis that co-existed with P. ponpetelegans.http://zoobank.org/urn:lsid:zoobank.org:pub:3EF73BE7-B3FE-4441-BA5E-29C5D5FCCBC9

Visual acuity in pelagic fishes and mollusks

In the sea, visual scenes change dramatically with depth. At shallow and moderate depths (<1,000 m), there is enough light for animals to see the surfaces and shapes of prey, predators, and conspecifics. This changes below 1,000 m, where no downwelling daylight remains and the only source of light is bioluminescence. These different visual scenes require different visual adaptations and eye morphologies. In this study we investigate how the optical characteristics of animal lenses correlate with depth and ecology. We measured the radius, focal length, and optical quality of the lenses of pelagic fishes, cephalopods, and a gastropod using a custom-built apparatus. The hatchetfishes (Argyropelecus aculeatus and Sternoptyx diaphana) and the barrel-eye (Opisthoproctus soleatus) were found to have the best lenses, which may allow them to break the counterillumination camouflage of their prey. The heteropod lens had unidirectional aberrations that matched its ribbon-shaped retina. We also found that lens angular resolution increased with depth. Due to a similar trend in the angular separation between adjacent ganglion cells in the retinas of fishes, the perceived visual contrast at the retinal cutoff frequency was constant with depth. The increase in acuity with depth allows the predators to focus all the available light bioluminescent prey animals emit and detect their next meal.

Visual optics and ecomorphology of the growing shark eye: a comparison between deep and shallow water species

Elasmobranch fishes utilise their vision as an important source of sensory information, and a range of visual adaptations have been shown to reflect the ecological diversity of this vertebrate group. This study investigates the hypotheses that visual optics can predict differences in habitat and behaviour and that visual optics change with ontogenetic growth of the eye to maintain optical performance. The study examines eye structure, pupillary movement, transmission properties of the ocular media, focal properties of the lens, tapetum structure and variations in optical performance with ontogenetic growth in two elasmobranch species: the carcharhinid sandbar shark, Carcharhinus plumbeus, inhabiting nearshore coastal waters, and the squalid shortspine spurdog, Squalus mitsukurii, inhabiting deeper waters of the continental shelf and slope. The optical properties appear to be well tuned for the visual needs of each species. Eyes continue to grow throughout life, resulting in an ontogenetic shift in the focal ratio of the eye. The eyes of C. plumbeus are optimised for vision under variable light conditions, which change during development as the animal probes new light environments in its search for food and mates. By contrast, the eyes of S. mitsukurii are specifically adapted to enhance retinal illumination within a dim light environment, and the detection of bioluminescent prey may be optimised with the use of lenticular short-wavelength-absorbing filters. Our findings suggest that the light environment strongly influences optical features in this class of vertebrates and that optical properties of the eye may be useful predictors of habitat and behaviour for lesser-known species of this vertebrate group.

Melanism in the gastric mucosa of the scalloped ribbonfish from the Ligurian Sea

Internal stomach melanism was observed in two scalloped ribbonfish Zu cristatus from the Ligurian Sea. The phenomenon may help prevent advertizing the presence of this species after consumption of bioluminescent prey.

Retinal specialisations in the dogfish &lt;i&gt;Centroscymnus coelolepis&lt;/i&gt; from the Mediterranean deep-sea

The present work attempted to study the importance of vision in Centroscymnuscoelolepis , the most abundant shark in the Mediterranean beyond a depthof 1000 m, by using anatomical and histological data. C.coelolepis exhibited large lateral eyes with a large pupil, spherical lens and a tapetum lucidum that gave the eye a strong greenish-golden “eye shine”. In the outer retinal layer, a uniform population of rod-like photoreceptors was observed while in the vitreal retina a thick inner plexiform layer comprised up to 30% of the whole retinal thickness. The cell distribution of the ganglion cell layer formed a thin elongated visual streak in the central plane of the eye that provided a horizontal panoramic field of view. A specialised area of higher visual acuity was located caudally at 32-44o from the geometric centre of the retina and 5-10o above the horizontal plane of the eye. This position indicated that the visual axis pointed in a slightly outward-forward direction with respect to the fish body axis. A non-uniform distribution of large ganglion cells was also found in the horizontal plane of the retina that practically coincided with the distribution of the total cell population in the ganglion cell layer. This is the first time that this type of retinal specialisation has been observed in the elasmobranchs. These characteristics indicate that the retina of C.coelolepis is designed not only to increase sensitivity in the horizontal field of view, as was also observed in other sharks, but also to improve motion detection in the same plane. The visual capacities evolved by C.coelolepis make this species adapted for discriminating the horizontal gradation of light that exists in the mesopelagic environment. Similarly, the large ganglion cell distribution observed in its retina seems to be related to its predatory behaviour, since it allows this shark to perceive the movement of bioluminescent prey against a totally dark background.

Review of Data on Diets of Beaked Whales: Evidence of Niche Separation and Geographic Segregation

This study reviewed published data on dietary preferences of beaked whales (Ziphiidae) from stomach contents analysis. Detailed data were only available for three of the six beaked whale genera (Hyperoodon, Mesoplodon and Ziphius). Stomach samples of these three beaked whale genera primarily contained cephalopod and fish remains, although some also contained crustaceans. Mesoplodon spp. were found to contain the most fish, with some species containing nothing but fish remains, while the southern bottlenose whale (Hyperoodon planifrons) and Cuvier's beaked whale (Ziphius cavirostris) rarely, if ever, contained fish. Of cephalopods identified, Histioteuthid, Gonatid, Cranchiid and Onychoteuthid species usually contributed most to prey numbers and biomass for all beaked whale genera. There was a wide range of species and families of cephalopods recorded from stomach contents, with no obvious preference for bioluminescent prey species, vertical migrating prey species or prey species with specific body compositions. Whales of the genus Mesoplodon generally contained smaller prey, such as cephalopods under 500 g in weight, compared with other beaked whales. Hyperoodon and Ziphius frequently contained much larger cephalopods with many important prey species having a mean weight of over 1000 g. This suggests that Mesoplodon occupies a separate dietary niche from Hyperoodon and Ziphius, which may be an example of niche segregation. In contrast, Hyperoodon and Ziphius appear to occupy very similar dietary niches but have geographically segregated distributions, with Hyperoodon occupying cold-temperate to polar waters and Ziphius occupying warm-temperate to tropical waters.

Predation risk and moonlight avoidance in nocturnal seabirds

Unlike most seabird families, the vast majority of small petrel species are nocturnal on their breeding grounds. Further, they reduce markedly their activity when the light level increases. Moonlight avoidance might be a consequence of reduction in foraging profitability, as bioluminescent prey do not come to the sea surface on bright nights. Alternatively, petrels may avoid colonies during moonlit nights because of increased predation risk. We studied predation on petrels by Brown Skuas Catharacta antarctica lönnbergi at Kerguelen, and the influence of moonlight on behaviour of both skuas and petrels, to test the ‘predation risk’ hypothesis. On the study area, Brown Skuas hunt at night and prey heavily upon the Blue Petrel Halobaena caerulea and the Thin‐billed Prion Pachyptila belcheri. Predation risk was higher on moonlit nights, as skuas caught more prey, and particularly more Blue Petrels when the light level increased. Nightly intakes of Blue Petrel and Thin‐billed Prion by skuas was related to colony attendance of non‐breeders rather than that of breeders. Biometry of prey also suggested that skuas caught a higher proportion of non‐breeding birds than was present at the colonies. Predation risk was thus greater in non‐breeders and on moonlit nights. Colony attendance by non‐breeding Blue Petrels and Thin‐billed Prions was also reduced during moonlit nights. Vocal activity, which is mainly by non‐breeders, was also drastically reduced when the light level increased in the species suffering the highest predation rate. Our results supported the ‘predation risk’ hypothesis, although the ‘foraging efficiency’ and the ‘predation risk’ hypotheses are not mutually exclusive: the former might explain the moonlight avoidance behaviour of breeding, and the latter that of non‐breeding individuals.

Comparative Study of Temporal Resolution in the Visual Systems of Mesopelagic Crustaceans.

The temporal characteristics of the visual systems of eight species of mesopelagic crustaceans were studied using the electroretinogram (ERG). Experiments were conducted on shipboard, using dark-captured specimens collected off the south coast of Cuba. As one would expect based on the relative intensity differences in their light environments, the deepest living species, Systellaspis debilis and Sergia filictum, have low maximum critical flicker fusion frequencies (CFFs) of 21-25 Hz, whereas the shallower living species Oplophorus gracilirostris and Janicella spinacauda have higher maximum CFFs (31-32 Hz). One of the shallowest living species, Funchalia villosa, has an unusually low maximum CFF (24 Hz), which may be a function of working with a dark-adapted eye. Two of the bilobed euphausiid species, Nematobrachion flexipes and N. sexspinosus, have very high maximum CFFs (44-57 Hz), comparable to those of surface-dwelling crabs, even though they live between 400 and 600 m. The maximum CFF of Stylocheiron maximum, a shallower living bilobed euphausiid, is only 36 Hz, indicating that maximum CFF among the euphausiids cannot be correlated with depth of occurrence. The unusually high flicker fusion frequency of the deeper living euphausiids may be correlated to their preference for bioluminescent prey.

Black gut phenomenon in cardinal fishes (Apogonidae, Teleostei)

MEPS Marine Ecology Progress Series Contact the journal Facebook Twitter RSS Mailing List Subscribe to our mailing list via Mailchimp HomeLatest VolumeAbout the JournalEditorsTheme Sections MEPS 161:295-298 (1997) - doi:10.3354/meps161295 Black gut phenomenon in cardinal fishes (Apogonidae, Teleostei) L. Fishelson1,*, M. Goren1, O. Gon2 1Dept of Zoology, George S. Wise Faculty of Life Sciences, Tel-Aviv University, Ramat Aviv, 69978 Israel 2J.L.B. Smith Institute of Ichthyology, PB 1015, Grahamstown 6140, South Africa *E-mail: fishelv@ccsg.tau.ac.il A study of 78 species of cardinal fishes (Apogonidae) revealed that 22 of them had black guts, 5 species had partly black guts and, in 51 species, the digestive tube was unpigmented or had dispersed melanophores in the external tunic. The black pigmentation is caused by melanization of the submucosal connective tissue which is situated between the muscularis and the basal lamina of the internal epithelium. This phenomenon was previously observed in moray eels and some pelagic fish. In nocturnal predators, it appears to serve to conceal bioluminescent prey in the stomach cavity. Apogonids · Melanization of guts Full text in pdf format PreviousNextExport citation RSS - Facebook - Tweet - linkedIn Cited by Published in MEPS Vol. 161. Publication date: December 31, 1997 Print ISSN:0171-8630; Online ISSN:1616-1599 Copyright © 1997 Inter-Research.

Sexual Dimorphism and Niche Divergence in a Mid-Water Octopod (Cephalopoda: Bolitaenidae).

In the translucent mid-water octopod Eledonella pygmaea, the posterior salivary glands that release proteolytic enzymes into the esophageal crop grow five times faster in males than in females. I suggest that the sexes vertically partition the water column and that large glands have evolved in males as a result of their deepwater habitat. Members of the species undergo ontogenetic vertical descent and are suggested to mate at the lower end of the adult depth range where receptive females signal males with light organs. Selection for increased fitness is inferred to result in females increasing their fecundity by feeding at the upper limit of the adult range and in mature males increasing their encounters with mates by living at depths where mating occurs. To further increase their fitness, mature males--despite occurring in a prey-limited habitat--must expend energy to visually detect potential mates, to travel over wide areas, and to attempt to copulate. To increase the energy available to them, males at depth may exploit bioluminescent prey. The large glands protect the translucent males from increased predation by physically blocking light emitted by bioluminescent prey in their crops, and by speeding digestion.

Comparative internal morphology of deep‐sea eels, with particular emphasis on gonads and gut structure

Anatomic and cytological studies of some 110 species of deep‐sea eels of among others the families Congridae, Colocongridae, Heterenchelyidae, Synaphobranchidae, Nettastomatidae, Nemichthyidae, Serrivomeridae, revealed a very high diversity in the visceral organs, especially gonads, guts and kidneys and their relation to the anal opening.The ovaries of various species were either monocyclic, producing eggs periodically, or polycyclic with frequent egg production. Some testes showed synchronous and others asynchronous sperm production. In some of the families, such as Heterenchelyidae, all the gonads are situated post‐anally, in the tail, whereas in Congridae the extent of penetration varies in the different genera, indicating that this family is an artificial one. As some gonads of a few species were found to harbour gametes of the two sexes, the possible occurrence of hermaphroditism is discussed. Melanization of gut was observed in numerous species produced by the penetration of pigmented tissue between the muscle layers of the gut wall or between these and the gut epithelium, this differing between various taxa and in young and adult specimens. The melanization of gut or parts of gut prevent slight (emitted by the swallowed bioluminescent prey) from being seen outside, and in this way protects the eel from predation. Pigmentation also occurs in the kidneys and other explanations for melanization are therefore discussed. In numerous species the gut, kidney and gas chamber partially penetrate into the tail, and as with the gonads, these characters can also be used on eel taxonomy.

Bacterial Predator-Prey Interaction at Low Prey Density

A bacterial predator-prey interaction was studied using Bdellovibrio and bioluminescent prey bacteria. The attacking bdellovibrio causes decay of bioluminescence, which is correlated with bdellovibrio penetration into the prey. The behavior of the prey and predator populations over time was found to be well described by a Lotka-Volterra model. By using this model, the probability of bdellovibrio penetration after encountering a prey cell was found to be approximately 3.0%. The prey density required to give the bdellovibrios a 50% chance of survival was calculated to be at least 3.0 x 10 cells per ml, and the density required for population equilibria was calculated to be about 7 x 10 prey bacteria per ml. These values, not generally characteristic of natural habitats, suggest that the existence of Bdellovibrio in nature is limited to special ecological niches.