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Concept: Cephalopod

272

Over thirty years ago anecdotal accounts of the undescribed Larger Pacific Striped Octopus suggested behaviors previously unknown for octopuses. Beak-to-beak mating, dens shared by mating pairs, inking during mating and extended spawning were mentioned in publications, and enticed generations of cephalopod biologists. In 2012-2014 we were able to obtain several live specimens of this species, which remains without a formal description. All of the unique behaviors listed above were observed for animals in aquaria and are discussed here. We describe the behavior, body color patterns, and postures of 24 adults maintained in captivity. Chromatophore patterns of hatchlings are also shown.

Concepts: Biology, Ocean, Mollusca, Cuttlefish, Chromatophore, Cephalopod, Octopus

173

Cephalopoda are a class of Mollusca species found in all the world’s oceans. They are an important model organism in neurobiology. Unfortunately, the lack of neuronal molecular sequences, such as ESTs, transcriptomic or genomic information, has limited the development of molecular neurobiology research in this unique model organism.

Concepts: Central nervous system, Nervous system, Brain, Biology, Caenorhabditis elegans, Model organism, Cephalopod, Octopus

168

Coleoid cephalopods have an elaborate camera eye whereas nautiloids have primitive pinhole eye without lens and cornea. The Nautilus pinhole eye provides a unique example to explore the module of lens formation and its evolutionary mechanism. Here, we conducted an RNA-seq study of developing eyes of Nautilus and pygmy squid. First, we found that evolutionary distances from the common ancestor to Nautilus or squid are almost the same. Although most upstream eye development controlling genes were expressed in both species, six3/6 that are required for lens formation in vertebrates was not expressed in Nautilus. Furthermore, many downstream target genes of six3/6 including crystallin genes and other lens protein related genes were not expressed in Nautilus. As six3/6 and its controlling pathways are widely conserved among molluscs other than Nautilus, the present data suggest that deregulation of the six3/6 pathway led to the pinhole eye evolution in Nautilus.

Concepts: Gene expression, Evolution, Eye, Lens, Mollusca, Crystallin, Cephalopod, Nautilus

161

Externally shelled cephalopods were important elements in open marine habitats throughout Earth history. Paleotemperatures calculated on the basis of the oxygen isotope composition of their shells can provide insights into ancient marine systems as well as the ecology of this important group of organisms. In some sedimentary deposits, however, the aragonitic shell of the ammonite or nautilid is poorly or not preserved at all, while the calcitic structures belonging to the jaws are present. This study tests for the first time if the calcitic jaw structures in fossil cephalopods can be used as a proxy for paleotemperature. We first analyzed the calcitic structures on the jaws of Recent Nautilus and compared the calculated temperatures of precipitation with those from the aragonitic shell in the same individuals. Our results indicate that the jaws of Recent Nautilus are secreted in isotopic equilibrium, and the calculated temperatures approximately match those of the shell. We then extended our study to ammonites from the Upper Cretaceous (Campanian) Pierre Shale of the U.S. Western Interior and the age-equivalent Mooreville Chalk of the Gulf Coastal Plain. In the Pierre Shale, jaws occur in situ inside the body chambers of well-preserved Baculites while in the Mooreville Chalk, the jaw elements appear as isolated occurrences in the sediment and the aragonitic shell material is not preserved. For the Pierre Shale specimens, the calculated temperatures of well-preserved jaw material match those of well-preserved shell material in the same individual. Analyses of the jaw elements in the Mooreville Chalk permit a comparison of the paleotemperatures between the two sites, and show that the Western Interior is warmer than the Gulf Coast at that time. In summary, our data indicate that the calcitic jaw elements of cephalopods can provide a reliable geochemical archive of the habitat of fossil forms.

Concepts: Sedimentary rock, Cretaceous, Mollusca, Fossil, Cephalopod, Nautilus, Ammonite, Siphuncle

150

New coleoid cephalopods are described from statolith remains from the Middle Eocene (Middle Lutetian) of the Paris Basin. Fifteen fossil statoliths are identified and assigned to the Sepiidae (Sepia boletzkyi sp. nov.,? Sepia pira sp. nov.), Loliginidae (Loligo clarkei sp. nov.), and Ommastrephidae (genus indet.) families. The sediments containing these fossils indicate permanent aquatic settings in the infralittoral domain. These sediments range in age from 46 Mya to 43 Mya. Analysis of the fossil record of statoliths (from findings described here, together with a review of previously published data) indicates marked biases in our knowledge. Fossil statoliths are known from as far back as the Early Jurassic (199.3 to 190.8 Mya) but surprisingly, to the best of our knowledge, no record occurs in the Cretaceous. This is a “knowledge bias” and clearly calls for further studies. Finally, we attempt to compare findings described here with fossils previously used to constrain divergence and/or diversification ages of some coleoid subclades in molecular phylogenies. This comparison clearly indicates that the new records detailed here will challenge some estimated divergence times of coleoid cephalopod subclades.

Concepts: Evolution, Phylogenetics, Fossil, Dinosaur, Cuttlefish, Cephalopod, Nautilus

150

Nautilus is often used as an analogue for the ecology and behavior of extinct externally shelled cephalopods. Nautilus shell grows quickly, has internal growth banding, and is widely believed to precipitate aragonite in oxygen isotope equilibrium with seawater. Pieces of shell from a wild-caught Nautilus macromphalus from New Caledonia and from a Nautilus belauensis reared in an aquarium were cast in epoxy, polished, and then imaged. Growth bands were visible in the outer prismatic layer of both shells. The thicknesses of the bands are consistent with previously reported daily growth rates measured in aquarium reared individuals. In situ analysis of oxygen isotope ratios using secondary ion mass spectrometry (SIMS) with 10 μm beam-spot size reveals inter- and intra-band δ18O variation. In the wild-caught sample, a traverse crosscutting 45 growth bands yielded δ18O values ranging 2.5‰, from +0.9 to -1.6 ‰ (VPDB), a range that is larger than that observed in many serial sampling of entire shells by conventional methods. The maximum range within a single band (~32 μm) was 1.5‰, and 27 out of 41 bands had a range larger than instrumental precision (±2 SD = 0.6‰). The results from the wild individual suggest depth migration is recorded by the shell, but are not consistent with a simple sinusoidal, diurnal depth change pattern. To create the observed range of δ18O, however, this Nautilus must have traversed a temperature gradient of at least ~12°C, corresponding to approximately 400 m depth change. Isotopic variation was also measured in the aquarium-reared sample, but the pattern within and between bands likely reflects evaporative enrichment arising from a weekly cycle of refill and replacement of the aquarium water. Overall, this work suggests that depth migration behavior in ancient nektonic mollusks could be elucidated by SIMS analysis across individual growth bands.

Concepts: Oxygen, Mass spectrometry, Isotope, Mollusca, Cephalopod, Oxygen isotope ratio cycle, Nautilus

95

We present a mechanism by which organisms with only a single photoreceptor, which have a monochromatic view of the world, can achieve color discrimination. An off-axis pupil and the principle of chromatic aberration (where different wavelengths come to focus at different distances behind a lens) can combine to provide “color-blind” animals with a way to distinguish colors. As a specific example, we constructed a computer model of the visual system of cephalopods (octopus, squid, and cuttlefish) that have a single unfiltered photoreceptor type. We compute a quantitative image quality budget for this visual system and show how chromatic blurring dominates the visual acuity in these animals in shallow water. We quantitatively show, through numerical simulations, how chromatic aberration can be exploited to obtain spectral information, especially through nonaxial pupils that are characteristic of coleoid cephalopods. We have also assessed the inherent ambiguity between range and color that is a consequence of the chromatic variation of best focus with wavelength. This proposed mechanism is consistent with the extensive suite of visual/behavioral and physiological data that has been obtained from cephalopod studies and offers a possible solution to the apparent paradox of vivid chromatic behaviors in color blind animals. Moreover, this proposed mechanism has potential applicability in organisms with limited photoreceptor complements, such as spiders and dolphins.

Concepts: Photoreceptor cell, Color, Mollusca, Color blindness, Cuttlefish, Cephalopod, Octopus

83

Human activities have substantially changed the world’s oceans in recent decades, altering marine food webs, habitats and biogeochemical processes [1]. Cephalopods (squid, cuttlefish and octopuses) have a unique set of biological traits, including rapid growth, short lifespans and strong life-history plasticity, allowing them to adapt quickly to changing environmental conditions [2-4]. There has been growing speculation that cephalopod populations are proliferating in response to a changing environment, a perception fuelled by increasing trends in cephalopod fisheries catch [4,5]. To investigate long-term trends in cephalopod abundance, we assembled global time-series of cephalopod catch rates (catch per unit of fishing or sampling effort). We show that cephalopod populations have increased over the last six decades, a result that was remarkably consistent across a highly diverse set of cephalopod taxa. Positive trends were also evident for both fisheries-dependent and fisheries-independent time-series, suggesting that trends are not solely due to factors associated with developing fisheries. Our results suggest that large-scale, directional processes, common to a range of coastal and oceanic environments, are responsible. This study presents the first evidence that cephalopod populations have increased globally, indicating that these ecologically and commercially important invertebrates may have benefited from a changing ocean environment.

Concepts: Natural environment, Ocean, Mollusca, Environmental science, Cuttlefish, Cephalopod, Octopus

43

Octopuses typically have a single reproductive period and then they die (semelparity). Once a clutch of fertilized eggs has been produced, the female protects and tends them until they hatch. In most shallow-water species this period of parental care can last from 1 to 3 months, but very little is known about the brooding of deep-living species. In the cold, dark waters of the deep ocean, metabolic processes are often slower than their counterparts at shallower depths. Extrapolations from data on shallow-water octopus species suggest that lower temperatures would prolong embryonic development periods. Likewise, laboratory studies have linked lower temperatures to longer brooding periods in cephalopods, but direct evidence has not been available. We found an opportunity to directly measure the brooding period of the deep-sea octopus Graneledone boreopacifica, in its natural habitat. At 53 months, it is by far the longest egg-brooding period ever reported for any animal species. These surprising results emphasize the selective value of prolonged embryonic development in order to produce competitive hatchlings. They also extend the known boundaries of physiological adaptations for life in the deep sea.

Concepts: Natural selection, Ocean, Mollusca, Charles Darwin, Deep sea, Cephalopod, Octopus, Octopodidae

36

Cephalopods show behavioral parallels to birds and mammals despite considerable evolutionary distance [1, 2]. Many cephalopods produce complex body patterns and visual signals, documented especially in cuttlefish and squid, where they are used both in camouflage and a range of interspecific interactions [1, 3-5]. Octopuses, in contrast, are usually seen as solitary and asocial [6, 7]; their body patterns and color changes have primarily been interpreted as camouflage and anti-predator tactics [8-12], though the familiar view of the solitary octopus faces a growing list of exceptions. Here, we show by field observation that in a shallow-water octopus, Octopus tetricus, a range of visible displays are produced during agonistic interactions, and these displays correlate with the outcome of those interactions. Interactions in which dark body color by an approaching octopus was matched by similar color in the reacting octopus were more likely to escalate to grappling. Darkness in an approaching octopus met by paler color in the reacting octopus accompanied retreat of the paler octopus. Octopuses also displayed on high ground and stood with spread web and elevated mantle, often producing these behaviors in combinations. This study is the first to document the systematic use of signals during agonistic interactions among octopuses. We show prima facie conformity of our results to an influential model of agonistic signaling [13]. These results suggest that interactions have a greater influence on octopus evolution than has been recognized and show the importance of convergent evolution in behavioral traits. VIDEO ABSTRACT.

Concepts: Signal, Mollusca, Cuttlefish, Chromatophore, Cephalopod, Octopus, Prima facie