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.     

Evolutionary changes in the timing of gut morphogenesis in larvae of the marine annelid Streblospio benedicti

The planktonic larvae of marine invertebrates are diverse in their nutritional modes, suggesting that evolutionary transitions in larval nutritional mode have been frequent. One approach to identifying the developmental changes that play important roles in such transitions is to compare "intermediate" larval forms to closely related larvae representative of their common ancestor. Here we make such a comparison between obligately planktotrophic and facultatively feeding larvae of the poecilogonous polychaete annelid Streblospio benedicti. We used feeding experiments to show that the derived, facultatively feeding larvae of this species develop the ability to feed at a later developmental stage (five muscle bands) than planktotrophic larvae (two to three muscle bands). This delay in the onset of feeding ability does not appear to be caused by delay in the formation of particle capture structures, but instead by delay in the development of a continuous, functional gut. These observations are consistent with the hypothesis that evolutionary increases in egg size in annelids lead predictably to heterochronic delays in gut development, and hence to transitions in larval nutritional mode.     

The epitome of hand waving? Larval feeding and hypotheses of metazoan phylogeny

SUMMARY The homology of larval forms, and particularly their feeding methods, has been a major element in some recent discussions about animal phylogeny. "Downstream feeding" is one of two main larval-feeding modes and is usually equated to an opposed-band system with ciliary bands called the prototroch and metatroch. Feeding in larvae is reviewed here and the homology hypothesis of downstream larval feeding is expanded, encompassing any feeding involving the prototroch. It is often argued that the presence of planktotrophic larvae using downstream feeding is plesiomorphic among spiralian animals, and that there is a bias in transformations, such that feeding larvae tend to be lost rather than gained. These hypotheses are assessed using cladistic parsimony methodology, in relation to Spiralia, Trochozoa, and with particular reference to polychaete annelids. Methods adopted for the possibility of a bias in transformations toward loss of downstream larval feeding include: expanded primary homology arguments, character reconstructions favoring reversals, and polymorphic terminals coded as having downstream larval feeding. Nevertheless, all analyses show that downstream larval feeding appears to have evolved multiple times from a lecithotrophic condition. The results support a conclusion that the prototroch was primarily locomotory, and has become associated with feeding a number of times. Hypotheses of metazoan phylogeny predicated on the assumption that downstream-feeding larvae are plesiomorphic are re-assessed.     

Opposed bands of cilia in the nonfeeding larvae of the serpulid annelid Salmacina tribranchiata

The nonfeeding planktonic larvae of marine invertebrates typically lack larval feeding structures. One puzzling exception to this generalization is the annelid clade Sabellidae, in which nonfeeding larvae possess ciliary bands (specifically, food groove and metatroch) that, to the best of our knowledge, have no function other than in feeding. Nishi and Yamasu (1992b, Bulletin of the College of Sciences, University of the Ryukyus, 54 , 107–121) published a scanning electron micrograph showing that nonfeeding larvae of the serpulid annelid Salmacina dysteri also possess food groove and metatrochal cilia. Here I demonstrate that nonfeeding larvae of Salmacina tribranchiata also bear ciliary bands identifiable as food groove and metatroch by position. High‐speed video of ciliary beat patterns shows that, together with the prototrochal cilia, these bands function in an opposed band system. The presence of feeding structures in nonfeeding annelid larvae is thus more widely distributed than previously recognized. The presence of feeding structures may make evolutionary transitions to planktotrophy more likely, and may underlie an inferred origin of larval feeding in the common ancestor of one of the two major clades of serpulid annelids, Serpulinae.     

Versatile ciliary behaviour in capture of particles by the bryozoan cyphonautes larva

Cyphonautes larvae of a bryozoan, Membranipora membranacea, used several ciliary mechanisms to capture algal cells upstream from the lateral band of cilia that produces a feeding current. (1) Lateral cilia changed beat and a backcurrent occurred at the time and place that particles were retained. (2) Algal cells were sieved and held stationary at the upstream (frontal) side of a row of laterofrontal cilia that were not beating. (3) Localized extension of cilia toward the inhalant chamber, coincident with particle captures, indicated that laterofrontal cilia flick toward the inhalant chamber. These flicks may aid transport of captured particles toward the mouth. Thus my earlier report that larvae only sieve, in contrast to the adults (which have an active ciliary response) was in error. The similar ciliary bands in adult and larval bryozoans and in other lophophorates (brachiopods, and phoronids) suggest that these animals share a core repertoire of ciliary behaviours in the capture and concentration of suspended food particles.     

The nonfeeding auricularia of Holothuria mexicana (Echinodermata,Holothuroidea)

Among echinoderms, nonfeeding larvae usually are simplified in body shape, have uniform ciliation, and have lost the larval gut. A few species have nonfeeding larvae that express some remnant features of feeding larvae like ciliated bands and larval skeleton or larval arms, but typically their larval mouth never opens and their gut does not function. Still other species have retained the feeding larval form, a functional gut, and can feed, but they do not require food to metamorphose. The present note describes the development of a tropical holothurian, Holothuria mexicana, which hatches as a gastrula that is already generating coelomic structures. A translucent auricularia forms with a mouth that opens but becomes reduced soon thereafter. In form and ciliation this auricularia resembles a feeding larva, but it does not respond to food. A doliolaria forms on day 4 and the pentactula on day 6 post‐fertilization. Further study of this larva and that of its closely related congener, Holothuria floridana, is warranted.     

Ciliary sieving and active ciliary response in capture of particles by suspension-feeding brachiopod larvae

Larvae of a brachiopod, Glottidia pyramidata, used at least two ciliary mechanisms to capture algal cells upstream from the lateral band of cilia that produces a feeding/swimming current. (1) Filtration: the larvae retained algal cells on the upstream (frontal) side of a sieve composed of a row of stationary laterofrontal cilia. Movement of the laterofrontal cilia could not be observed during capture or rejection of particles, but the laterofrontal cilia can bend toward the beating lateral cilia, a possible mechanism for releasing rejected particles from the ciliary sieve. (2) Localized changes of ciliary beat: the larvae may also concentrate particles by a local change in beat of lateral cilia in response to particles. The evidence is that the beat of lateral cilia changed coincident with captures of algal cells and that captured particles moved on paths consistent with a current redirected toward the frontal side of the tentacle by an induced local reversal of the lateral cilia. The change of beat of lateral cilia could have been an arrest rather than a reversal of ciliary beat, however. The similar ciliary bands in adult and larval lophophorates (brachiopods, phoronids, and bryozoans) suggest that these animals share a range of ciliary behaviours. The divergent accounts of ciliary feeding of lophophorates could be mostly the result of different authors observing different aspects of ciliary feeding.     

Phototactic responses of unfed walleye pollock,Theragra chalcogramma larvae: comparisons with other measures of condition

Synopsis The capability of unfed walleye pollock, Theragra chalcogramma, larvae to swim horizontally towards light was used as a sensitive, sublethal measure of larval condition. At 9°C, positive phototaxis and swimming ability of larvae was fully developed by 4–6 d after hatching, then decreased steadily until death by 12 d after hatching. This measure of larval condition corresponded closely with previously established benchmarks of larval condition, including first feeding, yolksac absorption, point of no return and death by starvation. The presence and timing of behavioral deficits associated with starvation, such as decreased ability to swim, feed and avoid predators, may have significant effects on the ability of larvae to vertically migrate, avoid predators and find and capture food.     

Development of larval diets for milkfish (Chanos chanos)

This study aimed to develop nutritionally balanced and cost-effective processed diets for milkfish larvae ( Chanos chanos Forsskal). Two larval diets (feed A and feed B) were formulated and prepared to contain 45&percnt| protein and 10&percnt| lipid. Several larval diet preparations were tried such as microbound/ unpelleted (freeze-dried), microbound/pelleted (oven-dried) and microbound/flaked (drum-dried) and assessed in terms of feed particle size and buoyancy, water stability and feed acceptability. The preparation that gave the best particle size and buoyancy as well as good water stability was prepared as the microbound diet (using K -carrageenan as a binder) and flaked using a drum drier. A series of feeding experiments were conducted to determine the growth and survival of milkfish larvae reared on various feeding schemes using these processed larval diets which were fed either solely or in combination with live feed. Larvae in control treatments were reared on live foods such as Brachionus plicatilis and Artemia nauplii. Larvae were observed to ingest the diets, indicating that the feeds had suitable physical characteristics and were attractive to the larvae. The overall results of the feeding trials showed that the artificial diets could be fed to milkfish larvae in combination with Brachionus rotifers starting on day 2 or day 8, and could be fed alone starting from day 15. These promising results would reduce the dependence of milkfish larvae on live feed and would have significant economic benefits in the form of simplified milkfish hatchery procedures.     

The effect of age at metamorphosis on the transition from larval to adult suspension‐feeding of the slipper limpet Crepidula fornicata

Slipper limpets use different ciliary feeding mechanisms as larvae and adults. Veliger larvae of Crepidula fornicata developed part of the adult feeding apparatus, including ctenidial filaments, neck lobe, and radula, before metamorphosis, but ctenidial feeding did not begin until well after loss of the larval feeding apparatus (velum) at metamorphosis. Earlier initiation of ctenidial feeding by individuals that were older larvae when metamorphosis occurred suggests continued development toward ctenidial feeding during delay of metamorphosis. Early juveniles produced a ciliary current through the mantle cavity and moved the radula in a grasping action before they began to capture algal cells on mucous strands or form a food cord. Either early juveniles could not yet form mucous strands or they delayed their production until development of other necessary structures. The neck canal for transporting food from ctenidium to mouth cannot develop before velar loss. In their first feeding, juveniles fed much like the adults except that the neck canal was less developed and the path of the food cord toward the mouth sometimes varied. As suspension feeders, calyptraeids lack the elaborations of foregut that complicate transition to juvenile feeding for many caenogastropods, but a path for the food cord must develop after velar loss. Why individuals can initiate ctenidial feeding sooner when they are older at metamorphosis is not yet known. The juveniles became sedentary soon after metamorphosis and were not observed to feed by scraping the substratum with the radula, in contrast to the first feeding by juveniles of another calyptraeid species, observed by Montiel et al. ( 2005 ).     

Origin and evolution of animal life cycles

The ‘origin of larvae’ has been widely discussed over the years, almost invariably with the tacit understanding that larvae are secondary specializations of early stages in a holobenthic life cycle. Considerations of the origin and early radiation of the metazoan phyla have led to the conclusion that the ancestral animal (= metazoan) was a holopelagic organism, and that pelago-benthic life cycles evolved when adult stages of holopelagic ancestors became benthic, thereby changing their life style, including their feeding biology. The literature on the larval development and phylogeny of animal phyla is reviewed in an attempt to infer the ancestral life cycles of the major animal groups. The quite detailed understanding of larval evolution in some echinoderms indicates that ciliary filter-feeding was ancestral within the phylum, and that planktotrophy has been lost in many clades. Similarly, recent studies of the developmental biology of ascidians have demonstrated that a larval structure, such as the tail of the tadpole larva, can easily be lost, viz. through a change in only one gene. Conversely, the evolution of complex structures, such as the ciliary bands of trochophore larvae, must involve numerous genes and numerous adaptations. The following steps of early metazoan evolution have been inferred from the review. The holopelagic ancestor, blastaea, probably consisted mainly of choanocytes, which were the feeding organs of the organism. Sponges may have evolved when blastaea-like organisms settled and became reorganized with the choanocytes in collar chambers. The eumetazoan ancestor was probably the gastraea, as suggested previously by Haeckel. It was holopelagic and digestion of captured particles took place in the archenteron. Cnidarians and ctenophores are living representatives of this type of organization. The cnidarians have become pelago-benthic with the addition of a sessile, adult polyp stage; the pelagic gastraea-like planula larva is retained in almost all major groups, but only anthozoans have feeding larvae. Within the Bilateria, two major lines of evolution can be recognized: Protostomia and Deuterostomia. In protostomes, trochophores or similar types are found in most spiralian phyla; trochophore-like ciliary bands are found in some rotifers, whereas all other aschelminths lack ciliated larvae. It seems probable that the trochophore was the larval type of the ancestral, pelago-benthic spiralian and possible that it was ancestral in all protostomes. Most of the non-chordate deuterostome phyla have ciliary filter-feeding larvae of the dipleurula type, and this strongly indicates that the ancestral deuterostome had this type of larva.     

Trochophore concepts: ciliary bands and the evolution of larvae in spiralian Metazoa

‘Trochophore’ is a term used in a strict sense for larvae having an opposed-band method of feeding, involving a prototroch and metatroch. Other ciliary bands such as a telotroch and neurotroch may be present. The trochophore has been proposed to represent the ancestral larval form for a group of metazoan phyla (including all members of the Spiralia). The name trochophore is also often applied to larvae that do not conform to the above definition. A cladistic analysis of spiralian taxa (with special reference to polychaete annelids), based on a suite of adult and larval characters, is used to assess several hypotheses: (1) that the trochophore (in a strict sense) is a plesiomorphic form for the Spiralia; (2) that die stricdy defined trochophore is plesiomorphic for members of the Spiralia such as the Polychaeta. The homology of each of the various separate ciliary bands of spiralian larvae, and features such as the apical tuft and protonephridia is also assessed. The results favour the conclusion that the trochophore, if defined as a feeding larval form using opposed bands, should not be regarded as an ancestral (= plesiomorphic) type for the Spiralia, or any other large taxon such as the Polychaeta or Mollusca. The evidence suggests that the various ciliary bands have differing evolutionary histories, and only the Echiura (possibly an annelid group) has members with the classical trochophore. The trochophore is re-defined as a larval form with a prototroch. This broad definition covers a wide variety of larvae, and matches the current usage more accurately than the restricted term. Features such as the neurotroch, telotroch and opposed-band feeding show convergence and reversals. The nature of the metatroch requires further investigation. The presence of a prototroch (and hence trochophore larvae) is used to identify an apomorphy-based taxon, Trochozoa, that includes the first ancestor to have evolved a prototroch and all its descendants. This minimally includes the Annelida [sensu lato), Echiura, Entoprocta, Mollusca and Sipuncula and is a less inclusive taxon than the Spiralia.     

Interfacial feeding behavior and particle flow patterns ofAnopheles quadrimaculatus larvae (Diptera: Culicidae)

The interfacial feeding behavior, mouthpart movements, and particle flow patterns of Anopheles quadrimaculatuslarvae were investigated, using videotape recordings, high-speed microcinematography, SEM, and laboratory experiments. While positioned at the water surface, larvae demonstrated 12 behaviors associated with movements of the head. In one of these, a larva rotated its head 180° and directed its mouthparts against the air-water interface. The larva rapidly extended and retracted its lateral palatal brushes (LPBs) at a rate of 5 cycles/s (5 Hz), creating currents and allowing for the collection of particles. Particles moved toward the head at a velocity of 4.31 mm/s, in discrete stops and starts, as the LPBs beat. Our analyses determined that particle movement toward the mouth was governed by very low Reynolds numbers (0.002–0.009). This finding indicated that viscous forces predominated in Anophelesfeeding and no inertial movement of particles occurred. According to this model, the LPBs cannot intercept particles directly, but function as paddles for particle entrainment. We did not observe the pharynx to function in particle filtration but, rather, in food bolus formation. We propose that the maxillary pilose area and midpalatal brush function as interception structures. It appeared that the LPBs do not break the surface film to feed, but collect particles from the surface microlayers. A plume of uningested particles emerged from the sides of the cibarium and descended into the water column. The plume consisted of alternately clear and dark, lenticular laminae formed beneath the larval head during the collecting filtering feeding mode. A comparison of particle sizes from surface microlayers and gut contents of fourth instars showed that larvae ingested mainly small particles in the range of 1.5 to 4.5 pm in diameter. The potential significance of interfacial feeding by anopheline larvae in their aquatic environment is discussed.     

Metamorphosis and evolution of feeding behaviour in salamanders of the family Plethodontidae

Plethodontid salamanders capture prey with enhanced tongue protraction relative to other salamander taxa, yet metamorphosing plethodontids are hypothesized to be constrained relative to direct-developing plethodontids in their degree of tongue evolution (protraction length and velocity) by the presence of a larval stage in development. In this biphasic life history the hyobranchial apparatus serves the conflicting functions of larval suction feeding and adult tongue protraction. The deletion of the larval stage removes one of the conflicting functions and has thus permitted direct-developing plethodontids to circumvent this constraint and evolve extremely long tongues, which in some species can be projected to 80% of body length. To evaluate this constraint hypothesis and explore taxonomic diversity of feeding behaviours, we studied feeding in larvae, adults and metamorphosing individuals of seven species of metamorphosing plethodontids from the basal taxa Desmognathinae and Hemidactyliini using direct observations, high-speed videography and kinematic analysis. We found that larval plethodontids suction feed, but feeding is suspended entirely during metamorphosis, and aquatic adults do not suction feed. Adults have exapted the terrestrial modes of tongue and jaw prehension for aquatic prey capture. These findings substantiate the premise that suction feeding and tongue protraction are conflicting functions, and thus our results support the constraint hypothesis. Plethodontid adults have evolved their extreme tongue protraction ability at the expense of adult suction feeding. The rapid metamorphosis that characterizes plethodontids may be an adaptation that minimizes the non-feeding period imposed by the evolution of derived tongue protraction in adults. © 2002 The Linnean Society of London, Zoological Journal of the Linnean Society , 2002, 134 , 375–400.     

Why are there feeding and nonfeeding larvae in phytoseiid mites (Acari, Phytoseiidae)?

The larval feeding traits and oviposition behavior of ten phytoseiid mite species were investigated in the presence and absence of prey. Results showed a correlation between prey preferences, the manner of oviposition, and larval feeding behavior. Species with larvae that must feed to develop preferred prey species that were distributed sparsely and laid their eggs in a scattered fashion. Species with larvae that do not need to feed to develop preferred prey species with a high aggregation and laid their eggs in a clumped fashion. The results suggest that nonfeeding larval behavior may be an adaptation to avoid sib-cannibalism, which occurs when eggs are oviposited closer together. Received: October 13, 2000 / Accepted: December 15, 2000     

Bias? What bias? The evolution of downstream larval‐feeding in animals

The homology of larval-feeding modes has been a major element in recent discussions about animal phylogeny. 'Downstream-feeding' is one of the two main larval-feeding modes, and is usually equated to an opposed-band system involving ciliary bands called the prototroch and metatroch. Larval-feeding in Spiralia is reviewed here and the homology hypothesis of downstream larval-feeding is expanded, encompassing any feeding involving the prototroch. It is often argued that the presence of planktotrophic larvae using downstream-feeding is plesiomorphic among spiralian animals, and that there is a bias in transformations, such that feeding larvae tend to be lost rather than gained. These hypotheses are assessed in relation to the Spiralia, Trochozoa and particularly polychaete annelids. Cladistic parsimony analyses are performed based on datasets of Rouse & Fauchald (1997) and Rouse (1999) , with an additional character based on downstream larval-feeding. Methods adopted to assess the possibility of a bias in transformations towards loss of downstream larval-feeding include: expanded primary homology arguments, character transformations favouring reversals and polymorphic terminals coded as having downstream larval-feeding. These measures all tend to favour the possibility that downstream larval-feeding will be plesiomorphic, and tends to be lost rather than gained. Nevertheless, all analyses show that downstream larval-feeding is not plesiomorphic, and appears to have evolved multiple times. The results support a conclusion that the prototroch has become associated with feeding a number of times. Hypotheses of metazoan phylogeny that are predicated on the assumption that downstream-feeding larvae are plesiomorphic (e.g. Peterson et al . 1997 ) should be re-assessed.     

Evolution of direct-developing larvae: selection vs loss

Observations of a sea urchin larvae show that most species adopt one of two life history strategies. One strategy is to make numerous small eggs, which develop into a larva with a required feeding period in the water column before metamorphosis. In contrast, the second strategy is to make fewer large eggs with a larva that does not feed, which reduces the time to metamorphosis and thus the time spent in the water column. The larvae associated with each strategy have distinct morphologies and developmental processes that reflect their feeding requirements, so that those that feed exhibit indirect development with a complex larva, and those that do not feed form a morphologically simplified larva and exhibit direct development. Phylogenetic studies show that, in sea urchins, a feeding larva, the pluteus, is the ancestral form and the morphologically simplified direct-developing larva is derived. The current hypothesis for evolution of the direct-developing larval form in sea urchins suggests that major developmental changes occur by neutral loss of larval features after the crucial transition to a nonfeeding life history strategy. We present evidence from Clypeaster rosaceus, a sea urchin with a life history intermediate to the two strategies, which indicates that major developmental changes for accelerated development have been selected for in a larva that can still feed and maintains an outward, pluteus morphology. We suggest that transformation of larval form has resulted from strong selection on early initiation and acceleration of adult development.     

A spectrophotometric technique for measuring particle ingestion by black fly larvae

A spectrophotometric technique was developed to provide insight into the feeding behavior of Simulium vittatum Zetterstedt (Diptera: Simuliidae) larvae. Larvae were exposed to water insoluble Neon Red particles (NRP) (DayGlo^®) in a controlled current. The insoluble particles were available for capture by the cephalic fans of the larvae and subsequent ingestion. The length of gut occupied by the particles after a given exposure time was determined by visual inspection and measured with the aid of a dissecting microscope. Larvae were then homogenized in acetone to solubilize the particles. After filtration, the quantity of pigmented particles in the alimentary tract of the larvae was determined using spectrophotometric analysis. The quantity of particles per unit length of the alimentary tract was calculated. Experiments were conducted to determine the ideal concentration of NRP for obtaining an accurate measure of ingestion without interfering with normal larval feeding behavior. Larval mortality following ingestion of insecticidal proteins produced by Bacillus thuringiensis ssp. israelensis was used as an indirect measure of feeding behavior for these experiments. A concentration of 15 p.p.m. of NRP in the larval medium was the highest concentration used that did not interfere with larval mortality following exposure to the insecticidal proteins. Additional experiments demonstrated that components of the experimental matrix did not interfere with NRP absorbance. The final experiment revealed that the consumption of NRP and insecticidal proteins by larvae was influenced by clay and cellulose in the larval medium.