Planktonic Duration of the Bryozoan Cyphonautes Larva and Limits on Growth Rate Imposed by Its Form-Limited Maximum Clearance Rate.

AbstractThe form of the cyphonautes larva of bryozoans changes little during development. The ciliated band that generates the feeding current increases nearly in proportion to body length, so that the maximum rate of clearing planktonic food from a volume of water becomes increasingly low relative to body protein. This development is unlike the other larvae that produce a feeding current with bands of simple cilia. The cyphonautes' growth rate has therefore been predicted to be unusually low when food is scarce. As predicted, cyphonautes larvae of a species of Membranipora starved at concentrations of food that supported growth of pluteus larvae. Comparisons between the cyphonautes and plutei of a sand dollar were for growth from first feeding to metamorphosis, with a mix of two algal species. Another comparison was for growth of cyphonautes at an advanced stage and plutei of a regular sea urchin at an early stage, with food in seawater at a reduced concentration. The low maximum clearance rate did not prevent rapid growth and development of some cyphonautes from egg through metamorphosis when food was abundant. Twenty-nine days for development to metamorphosis in the laboratory with abundant food was close to Yoshioka's estimate of larval duration from the time lag between adult zooid density and larval abundance in a population in the Southern California Bight. Despite individual variation in growth rates and other physiological and environmental influences, simple measures of larval form predicted the differences in larval performance: scarce food extended larval duration for the cyphonautes more than for plutei.

Scope for Developmental Plasticity of Feeding Larvae of a Holothuroid, Contrasted with Other Echinoderm Larvae.

AbstractFeeding larvae of echinoderms appear to differ in scope for adaptive developmental plasticity in response to food. Extension of the ciliary band on narrow arms supported by skeletal rods, as in echinoid and ophiuroid larvae, may enable a greater increase in maximum clearance rate per cell added, conferring greater advantages from developing longer ciliary bands when food is scarce. Formation of the juvenile mouth and water vascular system at a new site, as in echinoid and asteroid larvae, permits extensive growth of the juvenile rudiment during larval feeding, with advantages from earlier or more growth of the rudiment when food is abundant. In contrast, plasticity in storage of nutrients is unrelated to the form of the ciliary band or the site of formation of the juvenile's mouth. Feeding larvae (auriculariae) of holothuroids lack arms supported by skeletal rods and formation of the mouth at a new site but as a unique feature store nutrients in hyaline spheres. In this study, more food for auriculariae of Apostichopus californicus resulted in juveniles (pentactulae) with longer and wider bodies and larger hyaline spheres, but effects of food supply on the size of most body parts of auriculariae were small. Auriculariae with more food developed relatively larger stomachs and larger posterior hyaline spheres, indications of greater nutrient storage. Auriculariae with less food developed relatively wider mouths and differed in some exterior dimensions, which might enhance the capture of food. Plasticity is limited in rudiment development and perhaps in structures for feeding, but plasticity in nutrient storage can provide advantageous compromises between duration of growth as a feeding larva and the condition of juveniles formed at metamorphosis.

The association of coloniality with parental care of embryos.

Many colonial marine animals care for embryos by brooding them on or in their bodies. For brooding to occur, features of the animals must allow it, and brooding must be at least as advantageous as releasing gametes or zygotes. Shared features of diverse colonial brooders are suspension feeding and a body composed of small modules that are indefinitely repeated and can function semi-autonomously, such as polyps or zooids. Suspension feeding permits capture of sperm for fertilization of ova that are retained by the parent. Distribution of broods among numerous small polyps, zooids, or other small modules facilitates supply of oxygen to embryos that are retained and protected by the parent. Brooding increases survival of offspring, controls dispersal, and can provide other developmental advantages. Colonial ascidians, pterobranch hemichordates, and entoprocts brood; most bryozoans and many colonial cnidarians brood. An unanswered question is why so many colonial anthozoans do not brood. Sponges share with colonies capacities for capturing sperm and separating numerous retained embryos yet many do not brood. Hypotheses for nonbrooding by colonies and sponges necessarily must apply to particular taxa. Few have been tested.

Initiation of Posterior Coeloms of an Ophiuroid (Brittle Star) and Plasticity in Their Development.

AbstractIn the ophioplutei of brittle stars, the posterior coeloms are commonly assumed to be produced by a transverse fission of the initially formed coeloms; but in ophioplutei of Ophiopholis aculeata, the posterior coeloms first appear separately as aggregations of mesenchyme-like cells near the base of the posterolateral arms. Initiation of posterior coeloms was similar in ophioplutei of another family and may be similar in diverse ophiuroids. Initiation is easily missed without frequent observations. Early interpretations that diagrammed a fission of the first-formed coeloms appear to have influenced later authors for more than a century. Growth of posterior coeloms from a small initial size facilitated observations of developmental plasticity in growth of coeloms relative to that of larval arms. This plasticity, as observed in echinoplutei of echinoids, is relatively greater growth of a ciliary band for food capture when food is scarce and relatively greater growth of juvenile structures that will function after metamorphosis when food is abundant; however, juvenile structures develop extensively as a rudiment within the echinopluteus prior to settlement and metamorphosis, whereas in ophioplutei there is little development of juvenile structures until metamorphosis. In ophioplutei there is, therefore, less scope for shifting growth to structures that gain function after metamorphosis. Nevertheless, we found that when ophioplutei were at higher concentrations of food, the growth of the posterior coeloms was greater relative to the growth of the larval arms. Developmental plasticity in allocation of growth to larval and postlarval equipment can occur despite disparate patterns of development.

Contrasting Metatrochal Behavior of Mollusc and Annelid Larvae and the Regulation of Feeding While Swimming.

Molluscan veliger larvae and some annelid larvae capture particulate food between a preoral prototrochal band of long cilia that create a current for both swimming and feeding and a postoral metatrochal band of shorter cilia that beat toward the prototroch. Larvae encountering satiating or noxious particles must somehow swim without capturing particles or else reject large numbers of captured particles. Because high rates of particle capture are inferred to depend on the beat of both ciliary bands, arrest of the metatroch could be one way to swim while reducing captures. Larvae in eight families of annelids arrest metatrochal cilia frequently during prototrochal beat, often over a large part of the metatrochal band and with the arrested cilia aligned near the beginning of the effective stroke. In contrast, metatrochs of veligers of gastropods and bivalves rarely arrested while the prototroch beat, and those arrests were more localized and variable in position. This difference in metatrochal arrest was unexpected under hypotheses of either a single origin of this feeding mechanism or multiple origins within each phylum. Although different in metatrochal arrests, larvae of both phyla can separate swimming from feeding while both prototroch and metatroch beat. One hypothesis explaining low rates of capture per encounter, without metatrochal arrest, is a change in adhesion of prototrochal cilia with algae. In a few observations, part of the velar edge was retained within the veliger's shell so that exposed prototrochal cilia contributed to swimming while the adjacent metatroch and food groove were sequestered.

Arms of larval seastars of Pisaster ochraceus provide versatility in muscular and ciliary swimming.

Larval swimming with cilia, unaided by muscles, is the presumed ancestral condition for echinoderms, but use of muscles in swimming has evolved several times. Ciliation and musculature of the arms of brachiolaria-stage larvae in the family Asteriidae provide unusual versatility in the use of muscles in swimming. The muscles affect swimming in two different ways. (1) Contraction of muscles moves the arms, propelling the larva. (2) Contraction of muscles changes orientation of the arms, thereby changing direction of ciliary currents and direction of swimming. New observations of the brachiolaria of the asteriid seastar Pisaster ochraceus demonstrate more versatility in both of these uses of muscles than had been previously described: the posterolateral arms stroke in more ways to propel the larva forward and to change the direction of swimming, and more pairs of the arms point ciliary currents in more directions for changes in direction of swimming. Morphology of brachiolariae suggests that these uses of muscles in swimming evolved before divergence of the families Stichasteridae and Asteriidae within forcipulate asteroids. This versatile use of muscles for swimming, both alone and in combination with ciliary currents, further distinguishes the swimming of these brachiolariae from swimming by larvae of other echinoderms and larvae of acorn worms in the sister phylum Hemichordata.

Brood Reduction, Not Poecilogony, in a Vermetid Gastropod with Two Developmental Outcomes within Egg Capsules.

A small vermetid gastropod broods capsules containing nurse eggs and embryos that develop into small veligers. A few of these veligers continue development and growth while nurse eggs and developmentally arrested sibling veligers disappear. Survivors hatch as crawling pediveligers and juveniles. None of the veligers, if removed from capsules, swim in a directed way or withdraw into their shells, indicating that even the developing veligers are unsuited for extracapsular life until they can crawl. The shells of arrested veligers decalcify while their siblings grow. Few of the developmentally arrested veligers that were isolated from siblings and fed algal cells resumed detectable growth. Nurse eggs rather than cannibalism provide most of the food, but full growth of developing veligers depends on limited sharing; arrest of some siblings is a necessary adjunct of the nurse-egg feeding. Here, two developmental outcomes for larvae produced by developmental arrest of some (often termed poecilogony) serves instead as a means of brood reduction. Brood reduction is often attributed to family conflicts resulting from genetic differences. Another hypothesis is that a mother who cannot accurately sort numbers of nurse eggs and developing eggs into capsules could rely on brood reduction to adjust food for her offspring. At the extreme, an entirely random packaging would produce a binomial distribution of embryos in capsules, a very uneven distribution of food per embryo, and some capsules with no embryos. Males have yet to be found in this species, but even if reproduction is asexual, selection could still favor brood reduction.

When is dispersal for dispersal? Unifying marine and terrestrial perspectives.

Recent syntheses on the evolutionary causes of dispersal have focused on dispersal as a direct adaptation, but many traits that influence dispersal have other functions, raising the question: when is dispersal 'for' dispersal? We review and critically evaluate the ecological causes of selection on traits that give rise to dispersal in marine and terrestrial organisms. In the sea, passive dispersal is relatively easy and specific morphological, behavioural, and physiological adaptations for dispersal are rare. Instead, there may often be selection to limit dispersal. On land, dispersal is relatively difficult without specific adaptations, which are relatively common. Although selection for dispersal is expected in both systems and traits leading to dispersal are often linked to fitness, systems may differ in the extent to which dispersal in nature arises from direct selection for dispersal or as a by-product of selection on traits with other functions. Our analysis highlights incompleteness of theories that assume a simple and direct relationship between dispersal and fitness, not just insofar as they ignore a vast array of taxa in the marine realm, but also because they may be missing critically important effects of traits influencing dispersal in all realms.

Culturing larvae of marine invertebrates.

Larvae of marine invertebrates cultured in the laboratory experience conditions that they do not encounter in nature, but development and survival to metamorphic competence can be obtained in such cultures. This protocol emphasizes simple methods suitable for a wide variety of larvae. Culturing larvae requires seawater of adequate quality and temperature within the tolerated range. Beyond that, feeding larvae require appropriate food, but a few kinds of algae and animals are sufficient as food for diverse larvae. Nontoxic materials include glass, many plastics, hot-melt glue, and some solvents, once evaporated. Cleaners that do not leave toxic residues after rinsing include dilute hydrochloric or acetic acid, sodium hypochlorite (commercial bleach), and ethanol. Materials that can leave toxic residues, such as formaldehyde, glutaraldehyde, detergents, and hand lotions, should be avoided, especially with batch cultures that lack continuously renewed water. Reverse filtration can be used to change water gently at varying frequencies, depending on temperature and the kinds of food that are provided. Bacterial growth can be limited by antibiotics, but antibiotics are often unnecessary. Survival and growth are increased by low concentrations of larvae and stirring of large or dense cultures. One method of stirring large numbers of containers is a rack of motor-driven paddles. Most of the methods and materials are inexpensive and portable. If necessary, a room within a few hours of the sea could be temporarily equipped for larval culture.

Opposed ciliary bands in the feeding larvae of sabellariid annelids.

The larvae of marine annelids capture food using an unusual diversity of suspension-feeding mechanisms. Many of the feeding mechanisms of larval annelids are poorly known despite the abundance and ecological significance of both larvae and adults of some annelid taxa. Here we show that larvae of two species of sabellariid annelids, Sabellaria cementarium and Phragmatopoma californica, bear prototrochal and metatrochal cilia that beat in opposition to each other. For larvae of S. cementarium, we provide evidence that these opposed bands of cilia are used to capture suspended particles. In video recordings, captured particles were overtaken by a prototrochal cilium and then moved with the cilium to the food groove, a band of cilia between the prototroch and metatroch. They were then transported by cilia of the food groove to the mouth. Lengths of the prototrochal cilia, lengths of the prototrochal ciliary band, size range of the particles captured, and estimated rates of clearance increased with larval age and body size. Confirmation of the presence of opposed bands in larvae of sabellariids extends their known occurrence in the annelids to members of 10 families. Opposed bands in these different taxa differ in the arrangements and spacing of prototrochal and metatrochal cilia, and in whether they are used in combination with other feeding mechanisms. Opposed bands appear to be particularly widespread among the larvae of sabellidan annelids (a clade that includes sabellariids, sabellids, and serpulids), even in some species whose larvae do not feed. A parsimony analysis suggests that opposed bands are ancestral in this clade of annelids.

Plasticity of hatching and the duration of planktonic development in marine invertebrates.

Plasticity in hatching potentially adjusts risks of benthic and planktonic development for benthic marine invertebrates. The proportionate effect of hatching plasticity on duration of larval swimming is greatest for animals that can potentially brood or encapsulate offspring until hatching near metamorphic competence. As an example, early hatching of the nudibranch mollusk Phestilla sibogae is stimulated by scattering of encapsulated offspring, as by a predator feeding on the gelatinous egg ribbon. When egg ribbons are undisturbed, hatching is at or near metamorphic competence. Disturbance of an unguarded benthic egg mass can insert 4 or more days of obligate larval dispersal into the life history. As another example, the spionid annelid Boccardia proboscidea broods capsules, each with both cannibalistic and developmentally arrested planktivorous siblings plus nurse eggs. Early hatching produces mainly planktivorous larvae with a planktonic duration of 15 days. Late hatching produces mainly adelphophages who have eaten their planktivorous siblings and metamorphose with little or no period of swimming. Mothers actively hatch their offspring by tearing the capsules, and appeared to time hatching in response to their environment and not to the stage of development of their offspring. Higher temperature increased the variance of brooding time. Females appeared to hatch capsules at an earlier developmental stage at lower temperatures. Species that release gametes or zygotes directly into the plankton have less scope for plasticity in stage at hatching. Their embryos develop singly with little protection and hatch at early stages, often as blastulae or gastrulae. Time of hatching cannot be greatly advanced, and sensory capabilities of blastulae may be limited.

Capture of particles by direct interception by cilia during feeding of a gastropod veliger.

Ciliary feeders vary in the arrangement of ciliary bands and mechanisms of capture of food. Some larvae use opposed parallel bands of preoral (prototroch) and postoral (metatroch) cilia. Hypotheses for the mechanism of particle capture include filtration by adhesion to a cilium that overtakes a particle (direct interception), but until now unequivocal evidence for this mechanism has been lacking. Here, high-speed video recordings of veliger larvae of the gastropod Lacuna vincta demonstrated direct interception of particles by prototrochal cilia. Adhesion between cilium and particle was seen when a prototrochal cilium tugged a diatom chain into the food groove while in contact with one part of the chain. In several recorded events, a prototochal cilium overtook a particle during its effective stroke and subsequently pulled the particle inward with its recovery stroke; thereupon, the particle was deposited onto the food groove and transported to the mouth. Captures varied, however. In some cases the particle was intercepted multiple times in one capture event; in others, several cilia passed a particle without interception. Particles occasionally remained in the area of recovery strokes, indicating retention without continuing adhesion to a cilium. In three events, a particle lost from prototrochal cilia was intercepted and moved into the food groove by metatrochal cilia. Particles as wide as or wider than the food groove were also captured and transported but were not ingested.

Evolutionary and experimental change in egg volume, heterochrony of larval body and juvenile rudiment, and evolutionary reversibility in pluteus form.

Heterochronic developmental plasticity of the juvenile rudiment and larval body of sea urchin larvae occurs in response to supply of food. Evolutionary increase in egg size can also be associated with earlier development of the juvenile rudiment. We examined effects of egg volume of feeding larvae on this heterochrony and other changes in larval form. (1) Evolutionary and experimental enlargements of egg volume did not accelerate formation of the rudiment relative to the larval body. Development of the larval body and juvenile rudiment was compared for the echinoids Strongylocentrotus purpuratus (with an egg of 78-82 microm) and Strongylocentrotus droebachiensis (with an egg of 150-160 microm diameter). Development of both larval body and rudiment were accelerated in S. droebachiensis relative to S. purpuratus but with greater acceleration of the larval body, so that the rudiment of S. droebachiensis was initiated at a later larval stage even though at an earlier age. Also, experimentally doubling the egg volume of S. purpuratus did not accelerate development of the juvenile rudiment relative to the larval body. (2) Both species exhibited similar plasticity in timing of rudiment development in response to food supplies. (3) Doubling egg volume of S. purpuratus produced a larval form more similar to that of S. droebachiensis. This result mirrors previous experiments in which larvae from half embryos of S. droebachiensis were more similar to larvae of S. purpuratus. Many of the effects of egg volume on larval form are similar against either species' genetic background and are thus evolutionarily reversible effects on larval form.

Loss and gain of the juvenile rudiment and metamorphic competence during starvation and feeding of bryozoan larvae.

In many animals, larval structures and juvenile rudiments develop independently. One advantage of this independence is that juvenile rudiments can be expended as a nutrient reserve or for energy conservation. When bryozoan cyphonautes larvae were starved, structures required for settlement and metamorphosis shrank. When the larvae were again fed, these structures grew back. Starvation reduced the size of both the internal sac, a rudiment of postlarval juvenile structures, and the pyriform organ, which functions in sensing and crawling on the substratum at settlement. In contrast, starvation affected neither the size of the larval shell nor the lengths of the ciliary bands used in swimming and feeding. Starved larvae that had reduced the pyriform organ and internal sac did not metamorphose in response to stimuli from a laminarian alga. The laminarian alga did stimulate metamorphosis of the same larvae after renewed feeding, when the larvae had regrown these structures. Thus starved larvae expended body parts needed for settlement and metamorphosis when food was scarce while retaining structures for feeding, swimming, and defense. Starved larvae thereby retained the capacity to regrow structures needed for settlement and metamorphosis when they again encountered food. Advantages from expendable juvenile rudiments may enhance selection for their being developmentally distinct from structures for larval swimming and feeding.

Predators induce cloning in echinoderm larvae.

Asexual propagation (cloning) is a widespread reproductive strategy of plants and animals. Although larval cloning is well documented in echinoderms, identified stimuli for cloning are limited to those associated with conditions favorable for growth and reproduction. Our research shows that larvae of the sand dollar Dendraster excentricus also clone in response to cues from predators. Predator-induced clones were smaller than uncloned larvae, suggesting an advantage against visual predators. Our results offer another ecological context for asexual reproduction: rapid size reduction as a defense.

An extraordinarily long larval duration of 4.5 years from hatching to metamorphosis for teleplanic veligers of Fusitriton oregonensis.

Veliger larvae of the NE Pacific snail Fusitriton oregonensis were reared in culture for 4.5 to 4.6 years from hatching to metamorphosis and through postlarval growth to reproduction. Larval shells grew in length from 0.20 to 3.9 mm. Late veligers grew slowly, but shell sizes increased even in the 4th and 5th years. Widths of larval shells at late stages equaled or exceeded those of the protoconchs of two juveniles from the field. Cultured larvae did not metamorphose until presented with subtidal rocks and associated biota. There was no indication of larval senescence: the first 2 years of postmetamorphic shell growth were slightly faster, and time from metamorphosis to first reproduction (3.3 years) was slightly less than for an individual that had developed to metamorphic competence in the plankton. A 4.5-year larval phase exceeds previous estimates for teleplanic larval durations and greatly exceeds estimates of the time for transport across oceans. This extraordinarily long larval period may exceed the usual duration in nature but shows that larval periods can be much longer than previously suspected without complete stasis in growth and with little if any loss of viability.

Time and extent of ciliary response to particles in a non-filtering feeding mechanism.

Mechanisms of suspension feeding are usually described by the physics of inanimate filters. High-speed videorecordings in this study demonstrated that sea urchin larvae concentrate particles without filtration. They actively captured individual particles. At most times and places, the effective strokes of the swimming/feeding ciliary band were away from the circumoral field. Cilia of this band responded to particles by a reversal of beat that redirected the particle toward the circumoral field. A change of beat occurred along approximately 80 micro m of ciliary band during particle capture. Cilia responded 0.02 to 0.06 s after the particle was within reach of effective strokes and reversed beat, usually for about 0.1 to 0.2 s. The whole event (disruption of forward beat) generally lasted between 0.13 and 0.5 s. These observations imply reversed movement of a parcel of water much larger than the included captured particle, but particles are nevertheless greatly concentrated because water is directed toward the circumoral field only when and where a particle is sensed. Thus most of the concentration of particles occurs by a temporarily and locally redirected current, without filtration, and size and quality of particles captured depends on sensory capabilities, not the mechanics of filtration.

Good eaters, poor swimmers: compromises in larval form.

Compromises between swimming and feeding affect larval form and behavior. Two hypotheses, with supporting examples, illustrate these feeding-swimming trade-offs. (1) Extension of ciliated bands into long loops increases maximum clearance rates in feeding but can decrease stability of swimming in shear flows. A hydromechanical model of swimming by ciliated bands on arms indicates that morphologies with high performance in swimming speed and weight-carrying ability in still water differ from morphologies conferring high stability to external disturbances such as shear flows. Instability includes movement across flow lines from upwelling to downwelling water in vertical shear. Thus a hypothesis for the high arm elevation angles of sea urchin larvae, which reduce speed in still water, is that they reduce a downward bias imposed by the vertical shear in turbulence. Observations of sea urchin larvae in vertical shear and comparisons among brittle star larvae are consistent with the performance trade-offs predicted by the model. (2) Structures and behaviors that reduce swimming speed can enhance filtering for feeding. In the opposed-band feeding mechanisms of veligers and many trochophores, cilia push water to swim but movement of cilia relative to the water occurs when cilia overtake and capture particles. Features that may increase clearance rates at the expense of speed and weight capacity include structures that increase drag or body weight and a ciliary band that beats in opposition to the feeding-swimming current. Larval feeding mechanisms inherited from distant ancestors result in different swimming-feeding trade-offs. The different trade-offs further diversify larval form and behavior.

Evolution of fast development of planktonic embryos to early swimming.

Planktonic embryos of marine animals swim at an early stage and age. Although natural selection has apparently favored rapid development of structures for swimming, taxa have not converged on the same, minimal time from first cell division to first swimming. Comparisons of 34 species with planktonic embryos in 10 phyla revealed factors that account for variation in time to swimming. Time to first swimming correlated significantly with time from first to second cleavage (first cell cycle) in analyses of all embryos sampled and separately within the Spiralia and Echinodermata. Time to first swimming also correlated significantly with egg diameter in some clades, but not in all. Correlations between egg diameter and cell cycle duration were low except for the three species of Urochordata. Development to a feeding or nonfeeding larva did not affect time to first swimming beyond effects attributable to egg size. Time to first swimming did not correlate with type of locomotion developed (uniciliated cells, multiciliated cells, or muscle). Nonetheless, differences in locomotion are associated with changes in cell cycle durations prior to swimming. The ratios of time to first swimming and time for first cell cycle suggests that allocation of time to multiplication of cells versus differentiation of cells is resolved differently in species with different types of locomotion.

Risk and the evolution of cell-cycle durations of embryos.

Embryos at low risk evolve slower development rates. In seven independent evolutionary contrasts for marine invertebrates (two in asteroids, three in gastropods, one each in phoronids and brachiopods) the more protected embryos had longer cell cycles from first to second cleavage than less protected planktonic embryos. Protected embryos had longer cell cycles even when protected eggs were smaller than planktonic eggs. In an eighth contrast, among tunicates, the embryonic cell cycle was unrelated to brooding and nearly proportional to egg size, but the literature provides examples of especially slow development in some brooding tunicates. The faster development of planktonic embryos is consistent with published estimates of greater mortality rates for planktonic larvae than for embryos in broods or egg masses. Examples from the literature for annelids, arthropods, holothuroids, and chordates also demonstrated longer embryonic cell cycles for more protected embryos with no consistent effect of egg size on cell-cycle duration. Longer cell cycles presumably reduce the benefits of protecting offspring because of longer exposure to whatever hazards remain, but slow development may permit compensating benefits. Hypothesized benefits of longer cell cycles include less maternal investment in rate-limiting materials, more or different transcription, and correction of errors. Such trade-offs are independent of feeding and growth and are influenced by parental protection.