Phylogeny of selected Sepiidae (Mollusca, Cephalopoda) based on 12S, 16S, and COI sequences, with comments on the taxonomic reliability of several morphological characters

Phylogenetic relationships among 11 species of sepiids from Japanese waters and Sepia officinalis from Mediterranean were studied using partial sequences of the mitochondrial 12S rRNA, 16S rRNA, and cytochrome c oxidase subunit I genes. These three genes had been analyzed in an Atlantic species S. elagans and was obtained from database. In the two-gene set analysis (16S+COI), sequence data of another 4 species were added from database. We also studied morphological characters of radulae, tentacular clubs, and cuttlebones. The molecular phylogeny was not congruent with relationships detected by the number of rows in radulae and the arrangement of suckers on the tentacular club. As to the cuttlebone shape, the molecular phylogeny suggests the separation of two groups, Doratosepion species with a lanceolate cuttlebone and the others with a broad cuttlebone. Our molecular phylogenetic study revealed these sepiids are separated into four clades. The first clade includes Sepia officinalis, S. hierrendda, S. bertheloti, S. pharaonis and Sepiella japonica. The second clade consists of S. latimanus and Metasepia tullbergi from sub-tropical waters. The third clade includes Sepia esculenta, S. madokai, S. aculeata and S. lycidas, which have a cuttlebone with a prominent spine. The fourth clade consists of Doratosepion species complex, S. kobiensis, S. lorigera, S. pardex, S. peterseni, and S. sp., which are characterized by a narrow cuttlebone with a distinct outer cone at the posterior end. The lack of membranous structures in the cuttlebone is a synapomorphy for this clade. S. elegans did not clearly belong to any of these clades and might represent the fifth clade.     

Dimorphic growth in male and female cuttlefish<Emphasis Type="Italic"> Sepia orbignyana</Emphasis> (Cephalopoda: Sepiidae) from the Adriatic Sea

The relationships between mantle length and number of cuttlebone chambers (or septa), and between weight and number of cuttlebone chambers were studied in Sepia orbignyana collected in the south-western Adriatic Sea. Weight-at-chamber count and mantle length-at-chamber count were statistically higher in females than in males. As the available literature suggests that the rate of cuttlebone septum formation is the same in both sexes of Sepia species, it follows that in S. orbignyana females have higher growth rates than males. Received in revised form: 6 February 2001 Electronic Publication     

Morphological character evolution and molecular trees in sepiids (Mollusca: Cephalopoda): is the cuttlebone a robust phylogenetic marker?

The sepiids are characterized by their cuttlebone or sepion, an internal shell resulting from secondary mineralization of a chitinous 'gladius'. The various species are identified using a combination of shell criteria and 'soft-part' characters. Using mitochondrial genes, we established phylogenetic relationships of sepiids including the three accepted genera ( Sepia , Sepiella , Metasepia ) and a species complex of uncertain status ( Doratosepion ). We showed the Sepia genus to be paraphyletic and found no direct correlation between geographical distribution and systematics. We mapped, on the molecular tree, shell characteristics commonly used as reliable diagnostic criteria for taxonomy. Due to the plasticity of the shell, these characters did not appear phylogenetically informative. In an attempt to define systematic categories related to phylogenetic relationships, new clear synapomorphies need to be established for each genus, necessitating a revision of the genus Sepia .  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 89 , 139–150.     

Cuttlebone: Characterisation, Application and Development of Biomimetic Materials

Cuttlebone signifies a special class of ultra-lightweight cellular natural material possessing unique chemical,mechanical and structural properties,which have drawn considerable attention in the literature.The aim of this paper is to better understand the mechanical and biological roles of cuttlebone.First,the existing literature concerning the characterisation and potential applications inspired by this remarkable biomaterial is critiqued.Second,the finite element-based homogenisation method is used to verify that morphological variations within individual cuttlebone samples have minimal impact on the effective mechanical properties.This finding agrees with existing literature,which suggests that cuttlebone strength is dictated by the cuttlefish habitation depth.Subsequently,this homogenisation approach is further developed to characterise the effective mechanical bulk modulus and biofluidic permeability that cuttlebone provides,thereby quantifying its mechanical and transporting functionalities to inspire bionic design of structures and materials for more extensive applications.Finally,a brief rationale for the need to design a biomimetic material inspired by the cuttlebone microstructure is provided,based on the preceding investigation.     

Swimming behavior in relation to buoyancy in an open swimbladder fish, the Chinese sturgeon

The swimbladder of fishes is readily compressed by hydrostatic pressure with depth, causing changes in buoyancy. While modern fishes can regulate buoyancy by secreting gases from the blood into the swimbladder, primitive fishes, such as sturgeons, lack this secretion mechanism and rely entirely on air gulped at the surface to inflate the swimbladder. Therefore, sturgeons may experience changes in buoyancy that will affect their behavior at different depths. To test this prediction, we attached data loggers to seven free-ranging Chinese sturgeons Acipenser sinensis in the Yangtze River, China, to monitor their depth utilization, tail-beating activity, swim speed and body inclination. Two distinct, individual-specific, behavioral patterns were observed. Four fish swam at shallow depths (7–31 m), at speeds of 0.5–0.6 m s⁻¹, with ascending and descending movements of 1.0–2.4 m in amplitude. They beat their tails continuously, indicating that their buoyancy was close to neutral with their inflated swimbladders. In addition, their occasional visits to the surface suggest that they gulped air to inflate their swimbladders. The other three fish spent most of their time (88–94%) on the river bottom at a depth of 106–122 m with minimum activity. They occasionally swam upwards at speeds of 0.6–0.8 m s⁻¹ with intense tailbeats before gliding back passively to the bottom, in a manner similar to fishes that lack a swimbladder. Their bladders were probably collapsed by hydrostatic pressure, resulting in negative buoyancy. We conclude that Chinese sturgeons behave according to their buoyancy, which varies with depth due to hydrostatic compression of the swimbladder.     

Seasonal variation in septal spacing of Sepia officinalis and some Ordovician actinocerid nautiloids

Studies of cuttlebone of Sepia officinalis L. from the English Channel show a direct and linear correlation between ambient water temperature and septal spacing. The application of this observation to fossil shallow-water nautiloids and ammonoids is complicated by the equatorial habitat of many of these shells, their declining rate of chamber production through ontogeny and a paucity of large and complete specimens. But annual temperature variations are the most likely cause of variations in septal spacing a priori , temperature apparently being the prime determinant of feeding and growth rates of individuals at a particular ontogenetic stage. ▭ Nautiloids, annual growth, Ordovician , Sepia, English Channel.     

Buoyancy Range, Gas Bladder Volume, and Lipid Content of Adult Bloater, Coregonus hoyi Gill, in the Laurentian Great Lakes

We analyzed buoyancy characteristics (buoyancy range, gas bladder volume, and lipid content) of adult bloater, Coregonus hoyi Gill, in the Laurentian Great Lakes. Buoyancy was measured directly in individual bloater and compared with the hydrostatic pressures at the depths of capture. The results of the buoyancy comparisons suggest that C. hoyi has a buoyancy range comparable to the 'free vertical range' of movement that has been described for other fishes. The buoyancy range of bloater does not support the argument that they undergo diel vertical migrations, as suggested in earlier studies. Rather, the buoyancy range for bloater reflects the depths of neutral buoyancy and the distance above these depths at which they can maintain vertical position in the water column. The available data suggest that adult bloater are neutrally buoyant near the lake bottom, and C. hoyi with 50% positive buoyancy are at the top of their depth range. Large bloater have relatively small gas bladder volumes and a high lipid content. Based on the observed vertical distribution of large and small C. hoyi and our results, we deduced that large fish are more adept than small fish at regulating their buoyancy for prolonged stays at higher hydrostatic pressures. Lipid content for bloater was not significantly different with respect to sex or origin (wild vs. captive-raised).     

Behavioral laterality and morphological asymmetry in the cuttlefish, Sepia lycidas

Behavioral laterality is widely found among vertebrates, but has been little studied in aquatic invertebrates. We examined behavioral laterality in attacks on prey shrimp by the cuttlefish, Sepia lycidas, and correlated this to their morphological asymmetry. Behavioral tests in the laboratory revealed significant individual bias for turning either clockwise or counterclockwise toward prey, suggesting behavioral dimorphism in foraging behavior. Morphological bias was examined by measuring the curvature of the cuttlebone; in some the cuttlebone was convex to the right (righty), while in others, the cuttlebone was convex to the left (lefty). The frequency distributions of an index of cuttlebone asymmetry were bimodal, indicating that populations were composed of two types of individuals: "righty" and "lefty." Moreover, an individual's laterality in foraging behavior corresponded with the asymmetry of its cuttlebone, with righty individuals tending to turn counterclockwise and lefty ones in the opposite direction. These results indicate that cuttlefish exhibit behavioral dimorphism and morphological antisymmetry in natural populations. The presence of two types of lateral morph in cuttlefish provides new information on the relationship between antisymmetric morphologies and the evolution of individual laterality in behavioral responses in cephalopods. The implications of these findings for the interpretation of ecological meaning and maintenance mechanisms of laterality in cuttlefish are also discussed.     

Comparative character of the deep-water and inshore cottoid fishes endemic to Lake Baikal

Lake Baikal's 29 endemic species of cottoid fishes form three groups: shallow-water species in depths to 350 m; eurybathic species from 50 to 1300 m; and abyssal species from 400 to 1600 m. These groups differ in their abilities to withstand high hydrostatic pressure. As in marine deep-water fishes, abyssal cottoids in Baikal have few or no cones in the retina, and some have tubular eyes. Their seismosensory systems predominate, based chiefly on free neuromasts. The proportion of species with canal systems decreases with depth. Diversity of the predominantly gammarid foods also decreases from 45 species in shallow water to five species in deep water, and the lateral line system plays the dominant role in food detection at all depths. Two abyssal cottoids have become secondary pelagic, achieving close to neutral buoyancy through high lipid levels and reduced skeletal mineralization. These forms take advantage of the abundant pelagic planktonic amphipod populations. The adaptations of abyssal forms parallel those seen in deep-water marine fishes.     

Intra- and inter-specific variation in buoyancy of some estuarine fishes

Synopsis Buoyancy was measured on eight species of estuarine fishes that were caught in 1 m depth or less. Mean buoyancies of the physoclists Fundulus heteroclitus, F. majalis, Cyprinodon variegatus and Leiostomus xanthurus were similar and ranged from –6.5 to –18.0 kiloPascals below atmospheric pressure at sea level. Menidia menidia and Pomatomus saltatrix measured –36.6 and –46.1 kPa, respectively. Two physostomes, Brevoortia tyrannus and Anchoa mitchilli, measured + 2.9 and –23.5 kPa, respectively, but the latter probably releases air when handled.The four most buoyant physoclist species live near the bottom in areas that receive daily tide induced currents. Negative buoyancy probably functions in them as in stream dwelling minnows and salmonids, which respond to currents by decreasing their buoyancy. The pronounced negative buoyancy of M. menidia may be a response to a preference for habitat where the currents are stronger, P. saltatrix, which can secrete gas into the swim bladder at the fastest rate known for any fish, combines high secretion (and resorption) rates with marked negative buoyancy. This enables it to quickly change depths over a wide vertical range, without overexpanding the swim bladder to cause positive buoyancy.     

The foraging benefits of being fat in a highly migratory marine mammal

Foraging theory predicts that breath-hold divers adjust the time spent foraging at depth relative to the energetic cost of swimming, which varies with buoyancy (body density). However, the buoyancy of diving animals varies as a function of their body condition, and the effects of these changes on swimming costs and foraging behaviour have been poorly examined. A novel animal-borne accelerometer was developed that recorded the number of flipper strokes, which allowed us to monitor the number of strokes per metre swam (hereafter, referred to as strokes-per-metre) by female northern elephant seals over their months-long, oceanic foraging migrations. As negatively buoyant seals increased their fat stores and buoyancy, the strokes-per-metre increased slightly in the buoyancy-aided direction (descending), but decreased significantly in the buoyancy-hindered direction (ascending), with associated changes in swim speed and gliding duration. Overall, the round-trip strokes-per-metre decreased and reached a minimum value when seals achieved neutral buoyancy. Consistent with foraging theory, seals stayed longer at foraging depths when their round-trip strokes-per-metre was less. Therefore, neutrally buoyant divers gained an energetic advantage via reduced swimming costs, which resulted in an increase in time spent foraging at depth, suggesting a foraging benefit of being fat.     

The development and vertical distribution of populations of gas-vacuolate bacteria in a eutrophic,monomictic lake

The role of gas vacuoles in the vertical stratification of planktonic bacteria is analysed. Measurements made with certain gas-vacuolate bacteria in laboratory culture suggest that only colonial forms could sink or float fast enough to form population maxima in lakes by vertical migration from other depths. It is suggested that in the case of individual cells the importance of the buoyancy provided by gas vacuoles is to minimise sinking rates and thereby to increase residence times of the organisms at depths where conditions support their growth.Changes in the vertical distribution of a number of gas-vacuolate bacteria were followed throughout the year in a monomictic, eutrophic lake (Crose Mere, Shropshire). All were restricted to the anaerobic hypolimnion which developed in summer. The various species formed maxima at different depths and times. With some of them (e.g. species of Thiopedia, Pelonema and Brachyarcus) growth was necessary to explain their development. In others (e. g. species of Pelodictyon and two colourless bacteria) vertical migrations might also have contributed to their development.     

Depth distributions of coral reef fishes: the influence of microhabitat structure,settlement, and post-settlement processes

Many coral reef fishes have restricted depth ranges that are established at settlement or soon after, but the factors limiting these distributions are largely unknown. This study examines whether the availability of microhabitats (reef substrata) explains depth limits, and evaluates whether juvenile growth and survival are lower beyond these limits. Depth-stratified surveys of reef fishes at Kimbe Bay (Papua New Guinea) showed that the abundance of new settlers and the cover of coral substrata differed significantly among depths. A field experiment investigated whether settling coral reef fishes preferred particular depths, and whether these depth preferences were dependent on microhabitat. Small patch reefs composed of identical coral substrata were set up at five depths (3, 6, 10, 15 and 20 m), and settlement patterns were compared to those on unmanipulated reef habitat at the same five depths. For all species, settlement on patch reefs differed significantly among depths despite uniform substratum composition. For four of the six species tested, depth-related settlement patterns on unmanipulated habitat and on patch reefs did not differ, while for the other two, depth ranges were greater on the patch reefs than on unmanipulated habitat. A second experiment examined whether depth preferences reflected variation in growth and survival when microhabitat was similar. Newly settled individuals of Chrysiptera parasema and Dascyllus melanurus were placed, separately, on patch reefs at five depths (as above) and their survival and growth monitored. D. melanurus, which is restricted to shallow depths, had highest survival and growth at the shallowest depth. Depth did not affect either survival or growth of C. parasema, which has a broader depth range than D. melanurus (between 6 and 15 m). This suggests that the fitness costs potentially incurred by settling outside a preferred depth range may depend on the strength of the depth preference.     

The argonaut shell: gas-mediated buoyancy control in a pelagic octopus

Argonauts (Cephalopoda: Argonautidae) are a group of rarely encountered open-ocean pelagic octopuses with benthic ancestry. Female argonauts inhabit a brittle ‘paper nautilus’ shell, the role of which has puzzled naturalists for millennia. The primary role attributed to the shell has been as a receptacle for egg deposition and brooding. Our observations of wild argonauts have revealed that the thin calcareous shell also functions as a hydrostatic structure, employed by the female argonaut to precisely control buoyancy at varying depths. Female argonauts use the shell to ‘gulp’ a measured volume of air at the sea surface, seal off the captured gas using flanged arms and forcefully dive to a depth where the compressed gas buoyancy counteracts body weight. This process allows the female argonaut to attain neutral buoyancy at depth and potentially adjust buoyancy to counter the increased (and significant) weight of eggs during reproductive periods. Evolution of this air-capture strategy enables this negatively buoyant octopus to survive free of the sea floor. This major shift in life mode from benthic to pelagic shows strong evolutionary parallels with the origins of all cephalopods, which attained gas-mediated buoyancy via the closed-chambered shells of the true nautiluses and their relatives.     

The Burgundy-blood phenomenon: a model of buoyancy change explains autumnal waterblooms by Planktothrix rubescens in Lake Zürich

Buoyancy changes of the cyanobacterium Planktothrix rubescens- the Burgundy-blood alga - were modelled from its buoyancy response to light and irradiance changes in Lake Zürich during autumnal mixing. The daily insolation received by filaments at fixed depths and circulating to different depths was calculated from the measured light attenuation and surface irradiance. The active mixing depth, za5, was determined from the vertical turbulent diffusion coefficient, Kz, calculated from the wind speed, heat flux and temperature gradients. The fixed depth resulting in filament buoyancy, zn, decreased from 13 to 2 m between August and December 1998; the critical depth for buoyancy, zq, to which filaments must be circulated to become buoyant, decreased from >60 m in the summer to <10 m in winter. When za5 first exceeded zn, in September, P. rubescens was mixed into the epilimnion. In October, zq > za5: circulating filaments would have lost buoyancy in the high insolation. Often in November and December, after deeper mixing and lower insolation, za5 > zq: filaments would have become buoyant but would have floated to the lake surface (the Burgundy-blood phenomenon) only under subsequent calm conditions, when Kz was low. The model explains the Burgundy-blood phenomenon in deeper lakes; waterblooms near shallow leeward shores arise from populations floating up in deeper regions of the lake.     

Emergence of temperate pasture grases from different sowing depths: importance of seed weight, coleoptiele plus mesocotyl length and shoot strength

Inter-specific relationships between mean seed weight, coleoptile + mesocotyl (sub-coleoptile internode) length and width, shoot strength and emergence from different sowing depths were examined for timothy (Phleum pratense L., mean seed weight 0.33-0.48 mg depending on seed line), cocksfoot (Dactylis glomerata L., 0.65-0.78 mg), perennial ryegrass (Lolium perenne L., 1.71-2.19 mg), tall fescue (Festuca arundinucea Schreb., 1.73–2.60 mg), annual ryegrass (Lolium multiflorum Lam., 5.10-5.20 mg) and prairie grass (Bromus willdenowü Kunth., 10.5–12.2 mg). Across species at 10,30 and 60 mm sowing depths in the field and 10, 15 and 30 mm sowing depths under controlled environment conditions, there was a significant (P < 0.05) positive correlation between emergence % and mean seed weight. Across species at 10–30 mm sowing depth under controlled environment conditions, emergence % was not significantly correlated with coleoptile + mesocotyl length but there were significant positive correlations between emergence % and coleoptile and mesocotyl width: shoot strength increased with increased coleoptile width across species. For seed lines of timothy of different mean seed weight (0.21-0.81 mg), emergence %, coleoptile + mesocotyl length and coleoptile and mesocotyl width increased with increased seed weight at 10 and 15 mm sowing depth. Shoot strength increased with increased coleoptile width for timothy. For emerged and non-emerged cocksfoot and timothy seedlings regardless of seed weight, mean coleoptile + mesocotyl length was > 10 mm at 10 mm sowing depth. It is concluded that at 10–30 mm sowing depth, increased emergence % with increased seed weight across species is not due to increased coleoptile + mesocotyl length. It is proposed that increased emergence % with increased seed weight across species at 10–30 mm sowing depths and across seed lines of timothy at 10 mm sowing depth is primarily due to increased coleoptile and mesocotyl width resulting in increased shoot strength and hence an increased ability to penetrate the substrate.     

Buoyancy under Control: Underwater Locomotor Performance in a Deep Diving Seabird Suggests Respiratory Strategies for Reducing Foraging Effort

Background

Because they have air stored in many body compartments, diving seabirds are expected to exhibit efficient behavioural strategies for reducing costs related to buoyancy control. We study the underwater locomotor activity of a deep-diving species from the Cormorant family (Kerguelen shag) and report locomotor adjustments to the change of buoyancy with depth.

Methodology/Principal Findings

Using accelerometers, we show that during both the descent and ascent phases of dives, shags modelled their acceleration and stroking activity on the natural variation of buoyancy with depth. For example, during the descent phase, birds increased swim speed with depth. But in parallel, and with a decay constant similar to the one in the equation explaining the decrease of buoyancy with depth, they decreased foot-stroke frequency exponentially, a behaviour that enables birds to reduce oxygen consumption. During ascent, birds also reduced locomotor cost by ascending passively. We considered the depth at which they started gliding as a proxy to their depth of neutral buoyancy. This depth increased with maximum dive depth. As an explanation for this, we propose that shags adjust their buoyancy to depth by varying the amount of respiratory air they dive with.

Conclusions/Significance

Calculations based on known values of stored body oxygen volumes and on deep-diving metabolic rates in avian divers suggest that the variations of volume of respiratory oxygen associated with a respiration mediated buoyancy control only influence aerobic dive duration moderately. Therefore, we propose that an advantage in cormorants - as in other families of diving seabirds - of respiratory air volume adjustment upon diving could be related less to increasing time of submergence, through an increased volume of body oxygen stores, than to reducing the locomotor costs of buoyancy control.     

Buoyancy and its constraints on the underwater foraging behaviour of Reed Cormorants Phalacrocorax africanus and Darters Anhinga melanogaster

The effects of changing buoyancy on the diving and feeding behaviour of Reed Cormorants Phalacrocorax africanus and Darters Anhinga melanogaster was investigated at Lake Kariba, Zimbabwe. A qualitative model of the energetic constraints caused by buoyancy changes on the diving behaviour of these two birds is presented and the predictions from the model are tested. The buoyancy of both species declined exponentially at different rates with water depth. Reed Cormorants were neutrally buoyant at 5–6 m while Darters were neutrally buoyant at 2–4 m depth. Buoyancy changes affect underwater swimming speed, which for Reed Cormorants is twice as fast on the bottom than when commuting, and for the Darter is significantly slower when diving than at any other time. Cormorants feeding in water deeper then 6 m spent less time on the bottom and fed less successfully than those birds feeding in shallower water. This is because their bottom times were significantly reduced as a result of the energetic constraints caused by changes in their buoyancy.     

Stratification by cyanobacteria in lakes: a dynamic buoyancy model indicates size limitations met by Planktothrix rubescens filaments

The ability of the Planktothrix rubescens to stratify in Lake Zürich is related to the size and shape of the cyanobacterial filaments. Detailed measurements made in the lake are used in a dynamic computer model of buoyancy regulation to investigate the vertical movements of filaments tracking the depth at which the irradiance would support neutral buoyancy. The movement of the filament lags behind the constantly changing target depth owing to (a) the time taken for the filament to respond to the irradiance by changing its density and (b) the time it takes to move by sinking down or floating up through the water column. The model simulates the stratification depth over a 5-month period of the summer from the continuous measurements of irradiance and weekly measurements of light attenuation and temperature, without any further adjustment over the period. Models using filaments of the size observed in Lake Zürich explain several details of the observed depth changes: smaller planktonic cyanobacteria (e.g. Limnothrix sp.) are unable to migrate fast enough and larger ones (e.g. Anabaena spp.) will overshoot and become entrained in the epilimnion. The model can be used to simulate recruitment of Planktothrix filaments from different depths after vernal stratification. Recruitment of filaments from depths down to 45 m will contribute to the metalimnetic population increase in early July.     

The absence of sharks from abyssal regions of the world's oceans

The oceanic abyss (depths greater than 3000 m), one of the largest environments on the planet, is characterized by absence of solar light, high pressures and remoteness from surface food supply necessitating special molecular, physiological, behavioural and ecological adaptations of organisms that live there. Sampling by trawl, baited hooks and cameras we show that the Chondrichthyes (sharks, rays and chimaeras) are absent from, or very rare in this region. Analysis of a global data set shows a trend of rapid disappearance of chondrichthyan species with depth when compared with bony fishes. Sharks, apparently well adapted to life at high pressures are conspicuous on slopes down to 2000 m including scavenging at food falls such as dead whales. We propose that they are excluded from the abyss by high-energy demand, including an oil-rich liver for buoyancy, which cannot be sustained in extreme oligotrophic conditions. Sharks are apparently confined to ca 30% of the total ocean and distribution of many species is fragmented around sea mounts, ocean ridges and ocean margins. All populations are therefore within reach of human fisheries, and there is no hidden reserve of chondrichthyan biomass or biodiversity in the deep sea. Sharks may be more vulnerable to over-exploitation than previously thought.