An official website of the United States government
Abstract Larvae of many phyllodocidan annelids are planktotrophic, but the feeding mechanisms of larvae in this diverse clade are poorly known. Many larvae belonging to one large clade of phyllodocidans, Aphroditiformia, bear a bundle of long cilia attached to the left side of the prototroch, the oral brush, which they use in feeding. In 1936, D.P. Wilson observed that trochophore larvae ofNephtys hombergi, a member of the phyllodocidan family Nephtyidae, bore a strikingly similar bundle of long cilia on the left side of the body. Since Wilson's observation, numerous descriptions of nephtyid larvae have been published, but none remark on the presence of an oral brush. Here I show that metatrochophore I and II larvae ofMicronephtys cornutabear an oral brush, but that it is lost in the transition to the nectochaete stage, during which the larval mouth and foregut are also being remodeled to function in benthic feeding by juveniles. That an oral brush is clearly present in at least some larval stages of two genera suggests that oral brushes may be widespread in the feeding larvae of nephtyids, but have simply been overlooked for more than 80 years. Additional work is needed to make inferences on the evolutionary history of the oral brush in phyllodocidan annelids, and to distinguish among several hypotheses on the function of this peculiar group of cilia in larval feeding.
more »
« less
Opposed bands of cilia in the nonfeeding larvae of the serpulid annelid Salmacina tribranchiata
Abstract 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 annelidSalmacina dysterialso possess food groove and metatrochal cilia. Here I demonstrate that nonfeeding larvae ofSalmacina tribranchiataalso 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.
more »
« less
- Award ID(s):
- 1756531
- PAR ID:
- 10456961
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- Invertebrate Biology
- Volume:
- 139
- Issue:
- 2
- ISSN:
- 1077-8306
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract Spiralia is a large, ancient and diverse clade of animals, with a conserved early developmental program but diverse larval and adult morphologies. One trait shared by many spiralians is the presence of ciliary bands used for locomotion and feeding. To learn more about spiralian-specific traits we have examined the expression of 20 genes with protein motifs that are strongly conserved within the Spiralia, but not detectable outside of it. Here, we show that two of these are specifically expressed in the main ciliary band of the molluscTritia(also known asIlyanassa). Their expression patterns in representative species from five more spiralian phyla—the annelids, nemerteans, phoronids, brachiopods and rotifers—show that at least one of these,lophotrochin, has a conserved and specific role in particular ciliated structures, most consistently in ciliary bands. These results highlight the potential importance of lineage-specific genes or protein motifs for understanding traits shared across ancient lineages.more » « less
-
Abstract An animal's ability to regrow lost tissues or structures can vary greatly during its life cycle. The annelidCapitella teletaexhibits posterior, but not anterior, regeneration as juveniles and adults. In contrast, embryos display only limited replacement of specific tissues. To investigate when during development individuals ofC. teletabecome capable of regeneration, we assessed the extent to which larvae can regenerate. We hypothesized that larvae exhibit intermediate regeneration potential and demonstrate some features of juvenile regeneration, but do not successfully replace all lost structures. Both anterior and posterior regeneration potential of larvae were evaluated following amputation. We used several methods to analyze wound sites: EdU incorporation to assess cell proliferation; in situ hybridization to assess stem cell and differentiation marker expression; immunohistochemistry and phalloidin staining to determine presence of neurites and muscle fibers, respectively; and observation to assess re‐epithelialization and determine regrowth of structures. Wound healing occurred within 6 h of amputation for both anterior and posterior amputations. Cell proliferation at both wound sites was observed for up to 7 days following amputation. In addition, the stem cell markervasawas expressed at anterior and posterior wound sites. However, growth of new tissue was observed only in posterior amputations. Neurites from the ventral nerve cord were also observed at posterior wound sites. De novoashexpression in the ectoderm of anterior wound sites indicated neuronal cell specification, although the absence ofelavexpression indicated an inability to progress to neuronal differentiation. In rare instances, cilia and eyes re‐formed. Both amputations induced expanded expression of the myogenesis geneMyoDin preexisting tissues. Our results indicate that amputated larvae complete early, but not late, stages of regeneration, which indicates a gradual acquisition of regenerative ability inC. teleta. Furthermore, amputated larvae can metamorphose into burrowing juveniles, including those missing brain and anterior sensory structures. To our knowledge, this is the first study to assess regenerative potential of annelid larvae.more » « less
-
null (Ed.)ABSTRACT The swimming behavior of invertebrate larvae can affect their dispersal, survival and settlement in the ocean. Modeling this behavior accurately poses unique challenges as behavior is controlled by both physiology and environmental cues. Some larvae use cilia to both swim and create feeding currents, resulting in potential trade-offs between the two functions. Food availability is naturally patchy and often occurs in shallow horizontal layers in the ocean. Also, larval swimming motions generally differ in the horizontal and vertical directions. In order to investigate behavioral response to food by ciliated larvae, we measured their behavioral anisotropy by quantifying deviations from a model based on isotropic diffusion. We hypothesized that larvae would increase horizontal swimming and decrease vertical swimming after encountering food, which could lead to aggregation at food layers. We considered Crepidula fornicata larvae, which are specifically of interest as they exhibit unsteady and variable swimming behaviors that are difficult to categorize. We tracked the larvae in still water with and without food, with a portion of the larvae starved beforehand. On average, larvae in the presence of food were observed higher in the water column, with higher swimming speeds and higher horizontal swimming velocities when compared with larvae without food. Starved larvae also exhibited higher vertical velocities in food, suggesting no aggregation behavior. Although most treatments showed strong anisotropy in larval behavior, we found that starved larvae without food exhibited approximately isotropic kinematics, indicating that behavioral anisotropy can vary with environmental history and conditions to enhance foraging success or mitigate food-poor environments.more » « less
-
Abstract Feeding for most animals involves bouts of active ingestion alternating with bouts of no ingestion. In insects, the temporal patterning of bouts varies widely with resource quality and is known to affect growth, development time, and fitness. However, the precise impacts of resource quality and feeding behavior on insect life history traits are poorly understood. To explore and better understand the connections between feeding behavior, resource quality, and insect life history traits, we combined laboratory experiments with a recently proposed mechanistic model of insect growth and development for a larval herbivore,Manduca sexta. We ran feeding trials for 4th and 5th instar larvae across different diet types (two hostplants and artificial diet) and used these data to parameterize a joint model of age and mass at maturity that incorporates both insect feeding behavior and hormonal activity. We found that the estimated durations of both feeding and nonfeeding bouts were significantly shorter on low‐quality than on high‐quality diets. We then explored how well the fitted model predicted historical out‐of‐sample data on age and mass ofM. sexta. We found that the model accurately described qualitative outcomes for the out‐of‐sample data, notably that a low‐quality diet results in reduced mass and later age at maturity compared with high‐quality diets. Our results clearly demonstrate the importance of diet quality on multiple components of insect feeding behavior (feeding and nonfeeding) and partially validate a joint model of insect life history. We discuss the implications of these findings with respect to insect herbivory and discuss ways in which our model could be improved or extended to other systems.more » « less
