Biological Bulletin (BIOL BULL-US)

Publications in this journal

• Source

  Available from: biolbull.org

  Article: Serotonin and dopamine have opposite effects on phototaxis in larvae of the bryozoan Bugula neritina

  A. Pires, R. M. Woollacott
  Biological Bulletin 02/2013; 192:399-409.
• Article: Oxidative breakdown products of catecholamines and hydrogen peroxide induce partial metamorphosis in the nudibranch Phestilla sibogae Bergh (Gastropoda: Opisthobranchia)

  Pires A, Hadfield MG
  Biological Bulletin 02/2013; 180:310-317.
• Article: Microtransplantation of Cellular Membranes From Squid Stellate Ganglion Reveals Ionotropic GABA Receptors

  Conti L, Limon A, Palma E, Miledi R
  [show abstract] [hide abstract]
  ABSTRACT: The squid has been the most studied cephalopod, and it has served as a very useful model for investigating the events associated with nerve impulse generation and synaptic transmission. While the physiology of squid giant axons has been extensively studied, very little is known about the distribution and function of the neurotransmitters and receptors that mediate inhibitory transmission at the synapses. In this study we investigated whether γ-aminobutyric acid (GABA) activates neurotransmitter receptors in stellate ganglia membranes. To overcome the low abundance of GABA-like mRNAs in invertebrates and the low expression of GABA in cephalopods, we used a two-electrode voltage clamp technique to determine if Xenopus laevis oocytes injected with cell membranes from squid stellate ganglia responded to GABA. Using this method, membrane patches containing proteins and ion channels from the squid's stellate ganglion were incorporated into the surface of oocytes. We demonstrated that GABA activates membrane receptors in cellular membranes isolated from squid stellate ganglia. Using the same approach, we were able to record native glutamate-evoked currents. The squid's GABA receptors showed an EC50 of 98 μmol l–1 to GABA and were inhibited by zinc (IC50 = 356 μmol l–1). Interestingly, GABA receptors from the squid were only partially blocked by bicuculline. These results indicate that the microtransplantation of native cell membranes is useful to identify and characterize scarce membrane proteins. Moreover, our data also support the role of GABA as an ionotropic neurotransmitter in cephalopods, acting through chloride-permeable membrane receptors
  Biological Bulletin 02/2013; 224(1):47-52.
• Article: Characterization of Novel Cytoplasmic PARP in the Brain of Octopus vulgaris Author(s): De Lisa, Emilia; De Maio, Anna; Moroz, Leonid L.; et al. Source: BIOLOGICAL BULLETIN Volume: 222 Issue: 3 Pages: 176-181 Published: JUN 2012

  Emilia De Lisa, Anna De Maio, Leonid L. Moroz, Maria rosaria Faraone mennella, anna di cosmo
  Biological Bulletin 06/2012; 222(3):176-181.
• Article: Molluscan larvae: Pelagic juveniles or slowly metamorphosing larvae?

  Louise R Page
  [show abstract] [hide abstract]
  ABSTRACT: Asking the right questions about evolution of development, larval morphology, and life history requires knowledge of ancestral state. Two hypotheses dominate current opinion about the ancestral life cycle of bilaterians: the "larva-first" and the "intercalation" hypotheses. Until recently, the larva-first hypothesis was preeminent. This proposes that the original indirect life cycle of bilaterians included a planktotrophic larva followed by a benthic adult. Phylogenetic evidence suggests that a planktotrophic larva is plesiomorphic for echinoderms. A preponderance of developmental studies on echinoderms may have fostered a tendency to extrapolate conclusions about echinoderm development to other clades, particularly the concept that larval and juvenile/adult bodies are mostly separate entities. However, some of the recent reconstructions of bilaterian phylogeny suggest that nonfeeding larvae may have been ancestral for bilaterians, and these may have been intercalated into a life cycle that was originally direct. I review comparative data on molluscan development that suggests the trochophore-like stage is little more than a gastrula with transient structures (prototroch and apical sensory organ) to allow a temporary planktonic phase during development. Most lineage founder cells of molluscan embryos generate progeny that develop through the veliger stage into structures of the juvenile, which becomes benthic when the prototroch and apical sensory organ are lost. In light of this, the model of separate larval and juvenile bodies with the latter developing from nests of multipotent cells within the larva is inappropriate for molluscs. The intercalation hypothesis may be a better model for interpreting development of molluscs and other lophotrochozoans.
  Biological Bulletin 07/2009; 216(3):216-25.
• Article: Shaping the things to come: ontogeny of lophotrochozoan neuromuscular systems and the tetraneuralia concept.

  Andreas Wanninger
  [show abstract] [hide abstract]
  ABSTRACT: Despite the large variation in adult bodyplan phenotypes, a worm-shaped morphology is considered plesiomorphic for both Lophotrochozoa and Bilateria. Although almost all larval and adult lophotrochozoan worms have serially arranged ring muscles in their body wall, a comparison of their ontogeny reveals no less than six different developmental pathways that lead to this homogenous arrangement of ring muscles. However, in all taxa, with the exception of chaetodermomorph molluscs and the segmented annelids, ring muscle development starts with synchronous formation of certain pioneer myocytes, which is thus considered basal for Lophotrochozoa. Recent studies on spiralian neurogenesis revealed remnants of ancestral segmentation in echiurans and sipunculans, thus confirming molecular phylogenetic studies that propose a close relationship of these three taxa. Larval entoprocts exhibit a mosaic of larval and adult molluscan characters and, among other apomorphies, share with polyplacophoran Mollusca a complex larval apical organ and a tetraneurous nervous system, strongly suggesting a monophyletic assemblage of Entoprocta and Mollusca. The term Tetraneuralia is proposed herein for this lophotrochozoan clade. Overall, formation of the lophotrochozoan neuromuscular bodyplan appears as a highly dynamic process on both the ontogenetic and the evolutionary timescales, highlighting the importance of insights into these processes for reconstructing ancestral bodyplan features and phylogenetic relationships.
  Biological Bulletin 07/2009; 216(3):293-306.
• Article: Not my "type": larval dispersal dimorphisms and bet-hedging in opisthobranch life histories.

  Patrick J Krug
  [show abstract] [hide abstract]
  ABSTRACT: When conditions fluctuate unpredictably, selection may favor bet-hedging strategies that vary offspring characteristics to avoid reproductive wipe-outs in bad seasons. For many marine gastropods, the dispersal potential of offspring reflects both maternal effects (egg size, egg mass properties) and larval traits (development rate, habitat choice). I present data for eight sea slugs in the genus Elysia (Opisthobranchia: Sacoglossa), highlighting potentially adaptive variation in traits like offspring size, timing of metamorphosis, hatching behavior, and settlement response. Elysia zuleicae produced both planktotrophic and lecithotrophic larvae, a true case of poecilogony. Both intracapsular and post-hatching metamorphosis occurred among clutches of "Boselia" marcusi, E. cornigera, and E. crispata, a dispersal dimorphism often misinterpreted as poecilogony. Egg masses of E. tuca hatched for up to 16 days but larvae settled only on the adult host alga Halimeda, whereas most larvae of E. papillosa spontaneously metamorphosed 5-7 days after hatching. Investment in extra-capsular yolk may allow mothers to increase larval size relative to egg size and vary offspring size within and among clutches. Flexible strategies of larval dispersal and offspring provisioning in Elysia spp. may represent adaptations to the patchy habitat of these specialized herbivores, highlighting the evolutionary importance of variation in a range of life-history traits.
  Biological Bulletin 07/2009; 216(3):355-72.
• Article: Quantifying the "bio-" components in biophysical models of larval transport in marine benthic invertebrates: advances and pitfalls.

  Anna Metaxas, Megan Saunders
  [show abstract] [hide abstract]
  ABSTRACT: Biophysical models are being used increasingly, both as predictive tools of larval dispersal for a particular system and for general evaluation of the role of different factors in larval transport. In the results of such models, larval duration, mortality, and behavior in the water column have exhibited pronounced effects on larval dispersal of marine benthic invertebrates. The parameterization of these processes has broadly reflected values from laboratory experiments, but the accuracy of these values is unknown. The pelagic larval duration used in models should be determined by laboratory, or preferably field, studies and should incorporate environmentally dependent variability. For mortality, in situ estimates are now feasible and, likely, more accurate than the currently used values. Larval behavior can be measured in the field, by high-frequency sampling of distributional changes relative to features in the water column or by controlled larval releases in tractable systems. To successfully validate the outcomes of these models, we must either improve our techniques for measuring larval abundance at the end of larval transport immediately before settlement, or incorporate components for settlement into the models. We must also address the mismatch in sampling resolution between biological and physical processes. If used with caution, this powerful approach can significantly advance our understanding of larval transport.
  Biological Bulletin 07/2009; 216(3):257-72.
• Article: Larval development with transitory epidermis in Paranemertes peregrina and other hoplonemerteans.

  Svetlana A Maslakova, Jörn von Döhren
  [show abstract] [hide abstract]
  ABSTRACT: We describe development of the hoplonemertean Paranemertes peregrina from fertilization to juvenile, using light, confocal, and electron microscopy. We discovered that the uniformly ciliated lecithotrophic larva of this species has a transitory epidermis, which is gradually replaced by the definitive epidermis during the course of planktonic development. The approximately 90 large multiciliated cleavage-arrested cells of the transitory larval epidermis become separated from each other by intercalating cells of the definitive epidermis, then gradually diminish in size and disappear more or less simultaneously. Rudiments of all major adult structures-the gut, proboscis, cerebral ganglia, lateral nerve cords, and cerebral organs-are already present in 4-day-old larvae. Replacement of the epidermis is the only overt metamorphic transformation of larval tissue; larval structures otherwise prefigure the juvenile body, which is complete in about 10 days at 7-10 degrees C. Our findings on development of digestive system, nervous system, and proboscis differ in several ways from previous descriptions of hoplonemertean development. We report development with transitory epidermis in two other species, review evidence from the literature, and suggest that this developmental type is the rule for hoplonemerteans. The hoplonemertean planuliform larva is fundamentally different both from the pilidium larva of the sister group to the Hoplonemertea, the Pilidiophora, and from the hidden trochophore of palaeonemerteans. We discuss the possible function and homology of the larval epidermis in development of other nemerteans and spiralians in general.
  Biological Bulletin 07/2009; 216(3):273-92.
• Article: Larval biology of the crab Rhithropanopeus harrisii (Gould): a synthesis.

  Richard B Forward
  [show abstract] [hide abstract]
  ABSTRACT: This synthesis reviews the physiological ecology and behavior of larvae of the benthic crab Rhithropanopeus harrisii, which occurs in low-salinity areas of estuaries. Larvae are released rhythmically around the time of high tide in tidal estuaries and in the 2-h interval after sunset in nontidal estuaries. As in most subtidal crustaceans, the timing of larval release is controlled by the developing embryos, which release peptide pheromones that stimulate larval release behavior by the female to synchronize the time of egg hatching. Larvae pass through four zoeal stages and a postlarval or megalopal stage that are planktonic before metamorphosis. They are retained near the adult population by means of an endogenous tidal rhythm in vertical migration. Larvae have several safeguards against predation: they undergo nocturnal diel vertical migration (DVM) and have a shadow response to avoid encountering predators, and they bear long spines as a deterrent. Photoresponses during DVM and the shadow response are enhanced by exposure to chemical cues from the mucus of predator fishes and ctenophores. The primary visual pigment has a spectral sensitivity maximum at about 500 nm, which is typical for zooplankton and matches the ambient spectrum at twilight. Larvae can detect vertical gradients in temperature, salinity, and hydrostatic pressure, which are used for depth regulation and avoidance of adverse environmental conditions. Characteristics that are related to the larval habitat and are common to other crab larval species are considered.
  Biological Bulletin 07/2009; 216(3):243-56.
• Article: Nervous system development in feeding and nonfeeding asteroid larvae and the early juvenile.

  Laura Elia, Paulina Selvakumaraswamy, Maria Byrne
  [show abstract] [hide abstract]
  ABSTRACT: Larval and juvenile nervous systems (NS) of three asterinid sea stars with contrasting feeding and nonfeeding modes of development were characterized using the echinoderm-specific synaptotagmin antibody. In the feeding bipinnaria and brachiolaria larvae of Patiriella regularis, the species with ancestral-type development, an extensive NS was associated with the ciliary bands (CBs) and attachment complex. Lecithotrophic planktonic (Meridastra calcar) and benthic (Parvulastra exigua) brachiolariae lacked CBs and the associated NS, but had an extensive NS in the attachment complex. The similarity in the distribution and morphology of synaptotagmin immunoreactive neurons and the anatomy of the NS in the attachment complex of these closely related sea stars suggests conservation of neurogenesis in settlement-stage larvae regardless of larval feeding mode. Nerve cells were prominent on the brachia of all three species. In advanced brachiolariae the larval nervous system was localized to the adhesive disc as the larval body resorbed during metamorphosis. The structures and tissues that contained larval neurons degenerated during metamorphosis. There was no evidence that the larval NS persists through metamorphosis. In juvenile development, synaptotagmin IR was first evident in the NS of the tube feet. As the central nervous system developed, synaptotagmin IR reflected the histological organization of the adult NS. The juvenile NS formed de novo with a temporal lapse between histogenesis and synaptotagmin IR. We evaluated the ontogeny of NS organization in the change in body plan from the bilateral larva to the radial juvenile.
  Biological Bulletin 07/2009; 216(3):322-34.
• Article: Sniffing out new data and hypotheses on the form, function, and evolution of the echinopluteus post-oral vibratile lobe.

  Cory D Bishop, Brian K Hall
  [show abstract] [hide abstract]
  ABSTRACT: The performance requirements of ciliary band feeding explain the convoluted forms of many marine invertebrate larvae. Convolutions increase surface area and therefore feeding rates per unit body volume. We review recent advances in morphology, neural development, and behavior at settlement of the echinoid Lytechinus pictus and provide new ultrastructural and expression data on larvae of its congener, L. variegatus. Larvae of the echinometrid Colobocentrotus atratus contain neurons identified by their expression of nitric oxide synthase (NOS), indicating that this character is not unique to Lytechinus. We hypothesize that in some echinoids the convoluted shape of the post-oral vibratile lobe (POVL) covaries with the distribution of identified sensory neurons to enable olfaction during settlement. An analysis of variation in structural elaboration of the post-oral transverse ciliary band (PTB) within Echinoida and in feeding larvae of other echinoderm classes indicates that only echinoids, but not all echinoids, possess this novel character; larvae that do are distributed heterogeneously within the class. In recognition of this specialized function for the POVL and surrounding ectoderm, and because it is lobate and grows toward the mouth, we propose naming this structure the adoral lobe.
  Biological Bulletin 07/2009; 216(3):307-21.
• Article: Pre-settlement behavior in larval bryozoans: the roles of larval age and size.

  Scott C Burgess, Simon P Hart, Dustin J Marshall
  [show abstract] [hide abstract]
  ABSTRACT: Larval behaviors prior to settlement are important for both dispersal and the likelihood that larvae will encounter settlement habitat. The role of endogenous factors such as larval age and size are likely to be important in determining pre-settlement behavior but are less well understood than exogenous factors. In a simple experiment we explored the role of larval age and size on pre-settlement behavior in two species of bryozoan. We then used the results of this experiment to develop a theoretical model, which explored potential fitness benefits associated with phenotype-dependent changes in larval behavior (i.e., behaviors that changed depending on larval age or larval size) in a heterogeneous environment. In the experiment we delayed the metamorphosis of larvae of Bugula neritina andWatersipora arcuata and assessed the changes in the behavior of individual larvae (exploring the substratum vs. swimming away from it) as a function of larval age and size. In B. neritina, larval size had no effect on larval swimming behavior, but the youngest and oldest larvae spent more time exploring the substrate than did larvae of intermediate age. In W. arcuata, larval size and age had interactive effects on larval behavior. Our theoretical model predicted that phenotype-dependent behaviors carried a fitness benefit relative to phenotype-independent behaviors, but this depended strongly on the availability and quality of habitat elsewhere. We suggest that, taken together, larval age and size are important endogenous factors that act to affect pre-settlement larval behavior and that changes in behavior may act to increase fitness.
  Biological Bulletin 07/2009; 216(3):344-54.
• Article: Egg size as a life history character of marine invertebrates: Is it all it's cracked up to be?

  Amy L Moran, Justin S McAlister
  [show abstract] [hide abstract]
  ABSTRACT: Egg size is one of the most important aspects of the life history of free-spawning marine organisms, and it is correlated with larval developmental mode and many other life-history characters. Egg size is simple to measure and data are available for a wide range of taxa, but we have a limited understanding of how large and small eggs differ in composition; size is not always the best measure of the characters under selection. Large eggs are generally considered to reflect increased maternal investment, but egg size alone can be a poor predictor of energetic content within and among taxa. We review techniques that have been used to measure the energetic content and biochemical makeup of invertebrate eggs and point out the strengths and difficulties associated with each. We also suggest a number of comparative and descriptive approaches to biochemical constituent analysis that would strengthen our understanding of how natural selection shapes oogenic strategies. Finally, we highlight recent empirical research on the intrinsic factors that drive intraspecific variation in egg size. We also highlight the relative paucity of these data in the literature and provide some suggestions for future research directions.
  Biological Bulletin 07/2009; 216(3):226-42.
• Article: How did indirect development with planktotrophic larvae evolve?

  Claus Nielsen
  [show abstract] [hide abstract]
  ABSTRACT: The two main types of theories for the evolution of the biphasic life cycles in marine invertebrates are discussed. The "intercalation" theories propose that the larval stages (planktotrophic or lecithotrophic) have evolved as specializations from the ancestral, direct life cycle. The opposing "terminal addition" theories propose that the ancestor was holopelagic and that the adult stage was added to the life cycle with the pelagic stage retained as a planktotrophic larva. It is emphasized that theories based on hypothetical ancestors that were unable to feed must be rejected. This applies to planula theories based on a compact planula. Various arguments against the theories that consider the feeding larvae as ancestral in the major eumetazoan lineages and in particular against the trochaea theory are discussed and found untenable. It is suggested that the "Cambrian explosion" was actually a rapid Ediacaran radiation of the eubilaterians that was made possible by the evolution of a tubular gut with all the resulting possibilities for new body plans.
  Biological Bulletin 07/2009; 216(3):203-15.
• Article: Biological bulletin virtual symposium: biology of marine invertebrate larvae.

  Richard B Emlet, Svetlana A Maslakova, Alan L Shanks, Craig M Young
  Biological Bulletin 07/2009; 216(3):201-2.
• Article: Pelagic larval duration and dispersal distance revisited.

  Alan L Shanks
  [show abstract] [hide abstract]
  ABSTRACT: I present dispersal distances for 44 species with data on propagule duration (PD) for 40 of these. Data were combined with those in Shanks et al. (2003; Ecol. Appl. 13: S159-S169), providing information on 67 species. PD and dispersal distance are correlated, but with many exceptions. The distribution of dispersal distances was bimodal. Many species with PDs longer than 1 day dispersed less than 1 km, while others dispersed tens to hundreds of kilometers. Organisms with short dispersal distances were pelagic briefly or remained close to the bottom while pelagic. Null models of passively dispersing propagules adequately predict dispersal distance for organisms with short PDs (<1 day), but overestimate dispersal distances for those with longer PDs. These models predict that propagules are transported tens of kilometers offshore; however, many types remain within the coastal boundary layer where currents are slower and more variable, leading to lower than predicted dispersal. At short PDs, dispersal distances estimated from genetic data are similar to observed. At long PDs, genetic data generally overestimate dispersal distance. This discrepancy is probably due to the effect of rare individuals that disperse long distances, thus smoothing genetic differences between populations. Larval behavior and species' life-history traits can play a critical role in determining dispersal distance.
  Biological Bulletin 06/2009; 216(3):373-85.