Convergent maternal provisioning and life-history evolution in echinoderms

In marine invertebrates, the frequent evolution of lecithotrophic nonfeeding development from a planktotrophic feeding ancestral developmental mode has involved the repeated, independent acquisition of a large, lipid-rich, usually buoyant egg. To investigate the mechanistic basis of egg-size evolution and the role of maternally provisioned lipids in lecithotrophic development, we identified and quantified the egg lipids in six sea urchin species and five sea star species encompassing four independent evolutionary transformations to lecithotrophy. The small eggs of species with planktotrophic development were dominated by triglycerides with low levels of wax esters, whereas the larger eggs of lecithotrophs contain measurable triglycerides but were dominated by wax ester lipids, a relatively minor egg component of planktotrophs. Comparative analysis by independent contrasts confirmed that after removing the influence of phylogeny, the evolution of a large egg by lecithotrophs was correlated with the conspicuous deposition of wax esters. Increases in wax ester abundance exceeded expectations based solely on changes in egg volume. Wax esters may have roles in providing buoyancy to the egg and for postmetamorphic provisioning. Experimentally reducing the amount of wax esters in blastula stage embryos of the lecithotroph Heliocidaris erythrogramma resulted in a viable but nonbuoyant larvae. During normal development for H. erythrogramma, wax ester biomass remained constant during development to metamorphosis (five days postfertilization), but decreased during juvenile development before complete mouth formation (12 days postfertilization) and was further reduced at 18 days postfertilization. The function of wax esters may be specific to the lecithotrophic developmental mode because there were negligible wax esters present in competent pluteus larvae of Strongylocentrotus drobachiensis, a planktotrophic species. These data suggest that this seminal evolutionary modification, the production of a large egg, has been accomplished in part by the elaboration of a preexisting oogenic component, wax esters. The modification of preexisting oogenic processes may facilitate the observed high frequency of transformations in larval mode in marine invertebrates.     

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.     

Neutral lipid components of eleven species of Caribbean sharks

1. Eleven species of sharks collected in the Caribbean Sea contained, on a dry weight basis, 21–95% lipid in their livers and 0.4–11% lipid on their muscle tissues.2. Based upon theoretical calculations, two species of shark (Centrophorus granulosa andDalatias licha) contained sufficient lipids to allow neutral buoyancy in seawater.3. In both of the above species, wax esters comprised the major lipid class. Triacylglycerols and hydrocarbons were present in lower concentrations.4. Deep water sharks generally possessed larger livers containing higher percentages of total lipids and unsaturated hydrocarbons than more shallow dwelling species.     

Pressure Effects on Cholesterol and Lipid Synthesis by the Swimbladder of an Abyssal Coryphaenoides Species

SYNOPSIS. The swimbladder gas gland is recognized as a cholesterolsynthesis site in abyssal rattail fishes, Coryphaenoides sp.(from 2000 m depth), and Galápagos Islands surface fish,Orthopristis forbesi, Seriola mazatlana, and Sphoeroides annulatus.This relates to high levels of cholesterol in the gas gland(up to 21% of lipid) and high cholesterol levels in the fattyswimbladder interior (up to 49% of lipid). The gas gland hasmore protein (45.4%) than the internal fatty mass (18%). Lipidssynthesized include phospholipids and triglycerides in 2:1 ratioin the gas gland and 1:2 ratio in the liver. Deep fish havefatty livers (66%) compared to shallow fish (28%). Shallow fishincorporated five times as much acetate-l-¹⁴C into lipids asdid deep fish, and seven to eight times as much acetate-l-¹⁴Cinto cholesterol. Pressure facilitation of cholesterol synthesiswas observed in gas gland and liver of O. forbesi and Coryphaenoides,whereas total lipid synthesis was inhibited by higher pressures.Optimal acetate-l-¹⁴C incorporation into lipids occurred at5000 psi and 2°C in Coryphaenoides; it occurred at 14.7psi and 15° in O. forbesi. These conditions closely approximatethe environment of the fish.     

Functional dorsoventral symmetry in relation to lift-based swimming in the ocean sunfish Mola mola

The largest (up to 2 tons) and a globally distributed teleost--the ocean sunfish Mola mola--is commonly regarded as a planktonic fish because of its unusual shape including absence of caudal fin. This common view was recently questioned because the horizontal movements of the ocean sunfish tracked by acoustic telemetry were independent of ocean currents. However, direct information regarding their locomotor performance under natural conditions is still lacking. By using multi-sensor tags, we show that sunfish indeed swam continuously with frequent vertical movements at speeds of 0.4-0.7 m s(-1), which is similar to the records of other large fishes such as salmons, marlins, and pelagic sharks. The acceleration data revealed that they stroked their dorsal and anal fins synchronously (dominant frequency, 0.3-0.6 Hz) to generate a lift-based thrust, as penguins do using two symmetrical flippers. Morphological studies of sunfish (mass, 2-959 kg) showed that the dorsal and anal fins had similar external (symmetrical shape and identical area) and internal (identical locomotory muscle mass) features; however, the muscle shape differed markedly. We conclude that ocean sunfish have functional dorsoventral symmetry with regards to the non-homologous dorsal and anal fins that act as a pair of vertical hydrofoils. Although sunfish lack a swimbladder, we found that they are neutrally buoyant independent of depth because of their subcutaneous gelatinous tissue that has low density and is incompressible. Efficient lift-based swimming in conjunction with neutral buoyancy enables sunfish to travel long distances both horizontally and vertically.     

Lipid composition of the liver oil of deep-sea sharks from the Chatham Rise, New Zealand

Deep-sea sharks approach neutral buoyancy by means of a large liver that contains large amounts of low-density lipids, primarily squalene and diacyl glyceryl ether (DAGE). As an animal increases in size and matures sexually, many biochemical changes take place within the animal. It was hypothesized that maintenance of neutral buoyancy in deep-sea sharks involves fine-scale changes in the chemical composition of the liver oil as individual sharks grow and develop. To test this hypothesis, the lipid composition of liver oil for individuals of different size and sex of deep-sea sharks from the Chatham Rise, New Zealand was compared. The composition of liver oil varied within and among species. Several species contained large amounts of squalene and DAGE, whereas only traces of these lipids were present in other species. The amounts of squalene and DAGE in liver oil were inversely related, and squalene content tended to decrease as sharks increased in size. Species with high squalene levels (>80%) in liver oil were not abundant on the Chatham Rise, although levels of DAGE (a lipid of increasing commercial interest) were elevated in many species. Maintenance of neutral buoyancy in deep-sea sharks appears to involve changes in the composition of low-density liver lipids as the sharks increase in size and mature.     

The lipid biochemistry of calanoid copepods

Calanus species, particularly those in high latitudes, can accumulate large oil reserves consisting predominantly of wax esters. These wax esters consist predominantly of 16:0, 20:1 (n–9) and 22:1 (n–11) fatty alcohols, mainly formed de novo by the animals from non-lipid dietary precursors, esterified with various fatty acids that are often polyunsaturated fatty acids and largely of dietary, phytoplanktonic origin. Wax ester formation is maximal in copepodite stages IV and V. The lipids are elaborated not primarily for buoyancy regulation but as a source of metabolic energy during overwintering, particularly for reproduction. Large quantities of wax esters are utilised for gonadal development when stage V copepodites mature to females. Development of stage V copepodites to males is not accompanied by wax ester utilisation but males consume large amounts of these lipids in physical activity during reproduction. The role of wax esters in the life history of calanoids is illustrated with particular reference to a comparison of Calanus finmarchicus and Metridia longa in Balsfjord, northern Norway.     

Proliferation of elongate fishes in the deep sea

It was hypothesized that energetically efficient anguilliform swimming and axial elongation in fishes is favoured in the deep sea and predicted that the degree of elongation of the body form of fishes would increase with depth. An index of fish shape was derived from the relationship between length and mass. This was combined with data on abundance of c. 266 fish species from 389 research trawl tows made at depths of between 300 and 2030 m in the north‐east Atlantic Ocean. The degree of elongation of the fish increased with depth to c. 1250 m before levelling off. The strength of this phenomenon varied between higher level taxa, being most apparent in the Gadiformes and Osmeriformes, and weak or absent in the Perciformes and Selachimorpha. The advantage of efficient elongate body forms may explain why certain taxa such as the grenadiers (Macrouridae) have dominated the deep sea, some have restricted depth ranges, e.g. the sharks, skates and rays, and others are almost entirely absent, e.g. the flatfishes (Pleuronectiformes).     

Different on the inside: extreme swimbladder sexual dimorphism in the South Asian torrent minnows

The swimbladder plays an important role in buoyancy regulation but is typically reduced or even absent in benthic freshwater fishes that inhabit fast flowing water. Here, we document, for the first time, a remarkable example of swimbladder sexual dimorphism in the highly rheophilic South Asian torrent minnows (Psilorhynchus). The male swimbladder is not only much larger than that of the female (up to five times the diameter and up to 98 times the volume in some cases), but is also structurally more complex, with multiple internal septa dividing it into smaller chambers. Males also exhibit a strange organ of unknown function or homology in association with the swimbladder that is absent in females. Extreme sexual dimorphism of non-gonadal internal organs is rare among vertebrates and the swimbladder sexual dimorphisms that we describe for Psilorhynchus are unique among fishes.     

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.     

Swimbladder volume and body density in an armoured benthic fish, the streaked gurnard

Body density of streaked gurnards Trigloporus lastoviza is anomalously low (mean 1·043 g ml⁻¹) for a benthic fish and overlaps with that of pelagic fish such as cod and lumpfish. It is clear that the heavy armour of gurnards is offset by buoyancy provided by the swimbladder. Swimbladder volume is a mean 3·88% of gurnard volume. Evidence is given to indicate that this is quite large for a marine teleost: data are also presented to show that the '5% of fish volume for marine fish, 7% for freshwater fish' rule for swimbladder volumes is unreliable.     

The contribution of the swimbladder to buoyancy in the adult zebrafish (Danio rerio): a morphometric analysis

Many teleost fishes use a swimbladder, a gas-filled organ in the coelomic cavity, to reduce body density toward neutral buoyancy, thus minimizing the locomotory cost of maintaining a constant depth in the water column. However, for most swimbladder-bearing teleosts, the contribution of this organ to the attainment of neutral buoyancy has not been quantified. Here, we examined the quantitative contribution of the swimbladder to buoyancy and three-dimensional stability in a small cyprinid, the zebrafish (Danio rerio). In aquaria during daylight hours, adult animals were observed at mean depths from 10.1 +/- 6.0 to 14.2 +/- 5.6 cm below the surface. Fish mass and whole-body volume were linearly correlated (r(2) = 0.96) over a wide range of body size (0.16-0.73 g); mean whole-body density was 1.01 +/- 0.09 g cm(-3). Stereological estimations of swimbladder volume from linear dimensions of lateral X-ray images and direct measurements of gas volumes recovered by puncture from the same swimbladders showed that results from these two methods were highly correlated (r(2) = 0.85). The geometric regularity of the swimbladder thus permitted its volume to be accurately estimated from a single lateral image. Mean body density in the absence of the swimbladder was 1.05 +/- 0.04 g cm(-3). The swimbladder occupied 5.1 +/- 1.4% of total body volume, thus reducing whole-body density significantly. The location of the centers of mass and buoyancy along rostro-caudal and dorso-ventral axes overlapped near the ductus communicans, a constriction between the anterior and posterior swimbladder chambers. Our work demonstrates that the swimbladder of the adult zebrafish contributes significantly to buoyancy and attitude stability. Furthermore, we describe and verify a stereological method for estimating swimbladder volume that will aid future studies of the functions of this organ.     

Structure and volume of the hoki, Macruronus novaezelandiae (Merlucciidae), swimbladder

The structure of the hoki, Macruronus novaezelandiae , swimbladder is similar to well-developed swimbladders in other deep water fish that undergo extensive diel vertical migrations. The preponderance of a globular mass of submucosal tissue in the posterio-ventral floor of the swimbladder in large individuals is an unusual feature of unknown function, but has characteristics similar to regressed swimbladders that occur in some species of the Myctophidae. Two out of three different estimates of swimbladder volume were significantly lower than 'neutral buoyancy volume' estimates, probably because the swimbladders were inflated artificially without accounting for their natural compliancy and internal pressure. Volume estimates from such swimbladders may reduce substantially the accuracy of target strength estimates from morphometry-based models of the swimbladder. However, this may be a trivial consideration in acoustic surveys compared to the probable occurrence of diel and seasonal variation in swimbladder shape and volume.     

Macrotidal estuaries: a region of collision between migratory marine animals and tidal power development

Macrotidal estuaries of the inner Bay of Fundy are utilized by large numbers of migratory fishes, particularly dogfish, sturgeon, herring, shad, Atlantic salmon and striped bass as well as by other migratory marine animals, many of which have large body sizes (squid, Lamnid sharks, seals and whales). Tagging experiments indicate the fishes originate from stocks derived over the entire North American Atlantic coast from Florida to Labrador. Population estimates suggest up to 2.0 times 10⁶adult American shad (Alosa sapidissima) migrate through an individual embayment each year. These migrations are an integral part of the life history of the respective species and appear to be controlled in part by the near shore movements of ocean currents. In other regions of the world similar macrotidal estuaries exist (Cook Inlet, Alaska; Severn Estuary, U.K.) and they, like the Bay of Fundy, are linked in continuum to the local ocean currents. We propose that marine animals utilize all these regions in a manner similar to the Bay of Fundy estuaries and properly designed surveys will reveal their presence. Fish passage studies utilizing the Annapolis estuary low-head, tidal turbine on the Bay of Fundy have shown that turbine related mortality of 20–80% per passage occurs depending on fish species, fish size and the efficiency of turbine operation. We suggest that introduction of tidal turbines into open ocean current systems will cause widespread impact on marine populations resulting in significant declines in abundance.     

Effects of simulated microgravity on the development of the swimbladder and buoyancy control in larval zebrafish (Danio rerio)

The gas-filled swimbladder of teleost fishes provides hydrodynamic lift which counteracts the high density of other body tissues, and thereby allows the fish to achieve neutral buoyancy with minimal energy expenditure. In this study, we examined whether the absence of a constant direction gravitational vector affects the ontogeny of the swimbladder and buoyancy control in zebrafish (Danio rerio). We exposed fertilized eggs to simulated microgravity (SMG) in a closed rotating wall vessel with control eggs placed in a similar but nonrotating container. All eggs hatched in both groups. At 96 hr of postfertilization (hpf), all larvae were removed from the experimental and control vessels. At this point, 62% of the control larvae, but only 14% of SMG-exposed larvae, were observed to have inflated their swimbladder. In addition, the mean volume of the inflated swimbladders was significantly greater in the control larvae compared with larvae raised in SMG. After transfer to open stationary observation tanks, larvae with uninflated swimbladders in both groups swam to the surface to complete inflation, but this process was significantly delayed in larvae exposed to SMG. Initial differences in swimbladder inflation and volume between groups disappeared by 144 hpf. Furthermore, there were no apparent changes in patterns of development and maturation of swimbladder musculature, vasculature, or innervation resulting from SMG exposure at later stages of ontogeny. These data indicate that, despite a transient delay in swimbladder inflation in zebrafish larvae exposed to SMG, subsequent swimbladder development in these animals proceeded similarly to that in normal larvae.     

The origin of stomach oil in marine birds: Analyses of the stomach oil from six species of subantarctic procellariiform birds

The stomach oil produced by many marine birds of the order Procellariiformes is an important aspect of their breeding ecology. Fifty-seven samples of stomach oil from six species of subantarctic sea birds were examined by thin-layer and gas chromatography to determine the degree of variation in stomach oil composition between individuals of the same species. The wide variability detected, the typically marine composition of the component fatty acids and alcohols of the wax esters and triacyglycerols examined and the presence of pristane, squalene, and astaxanthin in the stomach oils all indicate that the bulk of the oil is derived directly from the food. This is in contrast to the nutritive fluids produced by secretion in several other groups of birds. Many of the stomach oils contain large amounts of wax ester and marine birds represent a significant link in the marine food web for the reconversion of zooplankton wax ester to triacylglycerol. No substantial offshore pollution by petroleum hydrocarbons was indicated by the samples; stomach oil samples from pelagic birds may be valuable in monitoring offshore pollution.     

The endemic faunae of Lake Baikal: their general biochemistry and detailed lipid composition

The biochemical composition of the important endemic faunal groups in Lake Baikal, Siberia, have been examined. The major biochemical components were determined and detailed analyses of the lipid fractions are presented. The lipids are characterized by high levels of long-chain omega 3 polyunsaturated fatty acids in the glyceride-esters, the presence of large amounts of triglyceride in pelagic and bathy-pelagic species with a complete absence of wax esters, and a very simple sterol composition dominated almost exclusively by cholesterol. The results are discussed in relation to present knowledge concerning both marine and freshwater lipids and the possible origin and evolution of the Baikalian fauna. Present theories concerning the likely role of long-chain polyunsaturates and wax esters in lipids are considered in the light of these present results and a link is suggested between sterol diversity and type of evolution.     

Activity and inhibition of carbonic anhydrase in Amia calva, a bimodal-breathing holostean fish

Carbonic anhydrase (CA) activity was measured in the respiratory swimbladder, gill filaments and red blood cells of the primitive air-breathing holostean fish, the bowfin, Amia calva . The activity of swimbladder CA, relative to gill and red cell CA activities, was within the range reported previously for unimodally-breathing fishes and was comparable to the CA activities reported for the air-breathing organs of teleosts. It is unlikely that carbon dioxide excretion across the bowfin swimbladder is limited to the uncatalyzed rate of HCO₃-dehydration. Bowfin blood plasma lacked any endogenous inhibitor(s) of CA, in contrast with information on teleostean fishes. This absence may have interesting phylogenetic implications and may offer some potential for investigating the nature and physiological role of plasma CA inhibitors.     

Unexpected Positive Buoyancy in Deep Sea Sharks,Hexanchus griseus,and a Echinorhinus cookei

We do not expect non air-breathing aquatic animals to exhibit positive buoyancy. Sharks, for example, rely on oil-filled livers instead of gas-filled swim bladders to increase their buoyancy, but are nonetheless ubiquitously regarded as either negatively or neutrally buoyant. Deep-sea sharks have particularly large, oil-filled livers, and are believed to be neutrally buoyant in their natural habitat, but this has never been confirmed. To empirically determine the buoyancy status of two species of deep-sea sharks (bluntnose sixgill sharks, Hexanchus griseus, and a prickly shark, Echinorhinus cookei) in their natural habitat, we used accelerometer-magnetometer data loggers to measure their swimming performance. Both species of deep-sea sharks showed similar diel vertical migrations: they swam at depths of 200–300 m at night and deeper than 500 m during the day. Ambient water temperature was around 15°C at 200–300 m but below 7°C at depths greater than 500 m. During vertical movements, all deep-sea sharks showed higher swimming efforts during descent than ascent to maintain a given swimming speed, and were able to glide uphill for extended periods (several minutes), indicating that these deep-sea sharks are in fact positively buoyant in their natural habitats. This positive buoyancy may adaptive for stealthy hunting (i.e. upward gliding to surprise prey from underneath) or may facilitate evening upward migrations when muscle temperatures are coolest, and swimming most sluggish, after spending the day in deep, cold water. Positive buoyancy could potentially be widespread in fish conducting daily vertical migration in deep-sea habitats.