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Showing papers in "The Biological Bulletin in 2014"


Journal ArticleDOI
TL;DR: This study significantly expands previous reports on microbial abundances in sponge tissues and contributes to a better understanding of the HMA-LMA dichotomy in sponge-microbe symbioses.
Abstract: The dichotomy between high microbial abundance (HMA) and low microbial abundance (LMA) sponges has been long recognized. In the present study, 56 sponge species from three geographic regions (greater Caribbean, Mediterranean, Red Sea) were investigated by transmission electron microscopy for the presence of microorganisms in the mesohyl matrix. Additionally, bacterial enumeration by DAPI-counting was performed on a subset of samples. Of the 56 species investigated, 28 were identified as belonging to the HMA and 28 to the LMA category. The sponge orders Agelasida and Verongida consisted exclusively of HMA species, and the Poecilosclerida were composed only of LMA sponges. Other taxa contained both types of microbial associations (e.g., marine Haplosclerida, Homoscleromorpha, Dictyoceratida), and a clear phylogenetic pattern could not be identified. For a few sponge species, an intermediate microbial load was determined, and the microscopy data did not suffice to reliably determine HMA or LMA status. To experimentally determine the HMA or LMA status of a sponge species, we therefore recommend a combination of transmission electron microscopy and 16S rRNA gene sequence data. This study significantly expands previous reports on microbial abundances in sponge tissues and contributes to a better understanding of the HMA-LMA dichotomy in sponge-microbe symbioses.

182 citations


Journal ArticleDOI
TL;DR: In this article, the effects of ocean acidification on coastal molluscs were examined to provide hypotheses of the potential impacts of high-CO2 on predator-prey interactions.
Abstract: The influence of environmental change on species interactions will affect population dynamics and community structure in the future, but our current understanding of the outcomes of species interactions in a high-CO2 world is limited. Here, we draw upon emerging experimental research examining the effects of ocean acidification on coastal molluscs to provide hypotheses of the potential impacts of high-CO2 on predator-prey interactions. Coastal molluscs, such as oysters, mussels, and snails, allocate energy among defenses, growth, and reproduction. Ocean acidification increases the energetic costs of physiological processes such as acid-base regulation and calcification. Impacted molluscs can display complex and divergent patterns of energy allocation to defenses and growth that may influence predator-prey interactions; these include changes in shell properties, body size, tissue mass, immune function, or reproductive output. Ocean acidification has also been shown to induce complex changes in chemoreception, behavior, and inducible defenses, including altered cue detection and predator avoidance behaviors. Each of these responses may ultimately alter the susceptibility of coastal molluscs to predation through effects on predator handling time, satiation, and search time. While many of these effects may manifest as increases in per capita predation rates on coastal molluscs, the ultimate outcome of predator-prey interactions will also depend on how ocean acidification affects the specified predators, which also exhibit complex responses to ocean acidification. Changes in predator-prey interactions could have profound and unexplored consequences for the population dynamics of coastal molluscs in a high-CO2 ocean.

119 citations


Journal ArticleDOI
TL;DR: A simple and straightforward approach to detecting PCR duplicates from ddRAD libraries by introducing a degenerate base region (DBR) in the sequencing adapter and suggesting that DBR regions should generally be included in PCR-based RAD studies.
Abstract: Restriction-site associated DNA sequencing (RAD) has emerged as a powerful marker system for study- ing genome-wide DNA polymorphisms using next-genera- tion sequencing. A recent technical facilitation of RAD is double-digest RAD (ddRAD), which utilizes two restriction enzymes for library preparation. The more flexible and balanced ddRAD allows analysis of genomic loci in hun- dreds of individuals. However, in contrast to paired-end sequencing of traditional RAD libraries, PCR duplicates cannot be detected with ddRAD. This is a concern because duplicates can contribute substantially to read coverage data and erroneously inflate the proportion of homozygous loci (allele dropout). Allele dropout can bias population genetic parameter inference and complicate the detection of outlier loci under selection. Here we outline a simple and straight- forward approach to detecting PCR duplicates from ddRAD libraries. Our approach introduces a degenerate base region (DBR, 12,288 unique combinations) in the sequencing adapter. We demonstrate the high efficiency and low rate of false positives in simulations. In addition, a pilot study was performed to test this approach on six aquatic invertebrates, sequenced on a HiSeq 2500 sequencer. The reads of the ddRAD libraries consisted of 33.48% PCR duplicates dis- tributed on 19.40% of the loci. A disproportionate number of PCR duplicates were detected in only 4.66% of the loci. While this should not be a concern for general parameter inference, outlier loci detection in particular would be im- proved by the DBR technique. Given the easy and straight- forward application of the technique in other RAD protocols as well, we suggest that DBR regions should generally be included in PCR-based RAD studies.

76 citations


Journal ArticleDOI
TL;DR: Comparison of recent trends in annual calcification with century-scale baseline calcification rates reveals that the frequency of growth anomalies has increased since the late 1990s throughout most of the world’s coral reef ecosystems.
Abstract: The tropical ocean environment is changing at an unprecedented rate, with warming and severe tropical cyclones creating obvious impacts to coral reefs within the last few decades and projections of acidification raising concerns for the future of these iconic and economically important ecosystems. Documenting variability and detecting change in global and regional climate relies upon high-quality observational records of climate variables supplemented, prior to the mid-19th century, with reconstructions from various sources of proxy climate information. Here we review how annual density banding patterns that are recorded in the skeletons of massive reef-building corals have been used to document environmental change and impacts within coral reefs. Massive corals provide a historical perspective of continuous calcification processes that pre-date most ecological observations of coral reefs. High-density stress bands, abrupt declines in annual linear extension, and evidence of partial mortality within the s...

74 citations


Journal ArticleDOI
TL;DR: The lessons learned from previous HTS surveys are documented and the current advances and applications focusing on foraminiferal eDNA are presented to discuss the problems associated with HTS approaches and predict the future trends and avenues that hold promises for surveying foraminIFeral diversity accurately and efficiently.
Abstract: Foraminifera are commonly defined as marine testate protists, and their diversity is mainly assessed on the basis of the morphology of their agglutinated or mineralized tests. Diversity surveys bas...

67 citations


Journal ArticleDOI
TL;DR: The next generation of studies is likely to truly facilitate the transition from population genetics to population genomics in marine fishes, which will advance the understanding of basic evolutionary processes and will offer new possibilities for conservation and management of valuable marine resources.
Abstract: Over the past few years, technological advances have facilitated giant leaps forward in our ability to generate genome-wide molecular data, offering exciting opportunities for gaining new insights into the ecology and evolution of species where genomic information is still limited. Marine fishes are valuable organisms for advancing our understanding of evolution on historical and contemporary time scales, and here we highlight areas in which research on these species is likely to be particularly important in the near future. These include possibilities for gaining insights into processes on ecological time scales, identifying genomic signatures associated with population divergence under gene flow, and determining the genetic basis of phenotypic traits. We also consider future challenges pertaining to the implementation of genome-wide coverage through next-generation sequencing and genotyping methods in marine fishes. Complications associated with fast decay of linkage disequilibrium, as expected for spec...

67 citations


Journal ArticleDOI
TL;DR: A general negative trend on holobiont growth was observed across most species of LBFs in response to both stressors, and major gaps in knowledge are outlined in addressing the potential for LBF species persistence in a changing ocean.
Abstract: Concerns regarding the response of calcifiers in future warmer and more acidic oceans have been raised in many studies. Tropical large benthic foraminifera (LBF) are important carbonate producers that reside in coral reefs worldwide. Similar to corals, these organisms live in sym- bioses with microalgae, which promote high calcification rates. The contribution of LBFs to reef sediments is under threat due to climate change. In this review, we synthesize research conducted on the effects of increased temperature and acidification on these organisms, and assess the poten- tial impacts on reef carbonate production. A meta-analysis of all available experimental data (18 publications, 84 indi- vidual experiments) on the effects of ocean warming and acidification on LBF holobiont health was performed using log-transformed response ratios (LnRR) comparing present- day ambient and projected future scenarios. For the latter, we used Representative Concentration Pathway 8.5 from the Intergovernmental Panel on Climate Change, which projects changes of 4° C and0.3 pH units by the year 2100. Overall, a general negative trend on holobiont growth was observed across most species of LBFs in response to both stressors. The only exception was the hyaline species (porous CaCO3 test composed of interlocking microcrys- tals) that have diatom symbionts. Species in this group appear resilient to future ocean acidification scenarios. Dif- ferences in the response of LBF species to warming and acidifying oceans may be due to (1) differences in the carbonate species' use in formation of the CaCO3 skeleton (CO2 vs. CO3 2- ), (2) varied responses of the symbiont types (diatom, dinoflagellate, rhodophyte) to stressors, or (3) the degree of nutritional dependence of the host to its symbiont. We also summarize current estimates of carbonate produc- tion by LBFs to provide a context of their contribution to reefs. Finally, we outline major gaps in knowledge in ad- dressing the potential for LBF species persistence in a changing ocean.

54 citations


Journal ArticleDOI
TL;DR: Although the impact of ocean acidification on the skeleton of echinoderms has been considered as a major threat from the first studies, a better understanding of the induced changes, in particular the functional consequences of growth modifications and dissolution related to mechanical properties is suggested.
Abstract: Available evidence on the impact of acidification and its interaction with warming on the skeleton of postmetamorphic (juvenile and adult) echinoderms is reviewed. Data are available on sea urchins, starfish, and brittle stars in 33 studies. Skeleton growth of juveniles of all sea urchin species studied so far is affected from pH 7.8 to 7.6 in seawater, values that are expected to be reached during the 21st century. Growth in adult sea urchins (six species studied) is apparently only marginally affected at seawater pH relevant to this century. The interacting effect of temperature differed according to studies. Juvenile starfish as well as adults seem to be either not impacted or even boosted by acidification. Brittle stars show moderate effects at pH below or equal to 7.4. Dissolution of the body wall skeleton is unlikely to be a major threat to sea urchins. Spines, however, due to their exposed position, are more prone to this threat, but their regeneration abilities can probably ensure their maintenance, although this could have an energetic cost and induce changes in resource allocation. No information is available on skeleton dissolution in starfish, and the situation in brittle stars needs further assessment. Very preliminary evidence indicates that mechanical properties in sea urchins could be affected. So, although the impact of ocean acidification on the skeleton of echinoderms has been considered as a major threat from the first studies, we need a better understanding of the induced changes, in particular the functional consequences of growth modifications and dissolution related to mechanical properties. It is suggested to focus studies on these aspects.

46 citations


Journal ArticleDOI
TL;DR: Meta-analyses across eight studies and four urchin species largely support prevailing hypotheses about the impact of ocean acidification on marine calcifiers and validates the accuracy of gene expression in predicting the consequences of ocean change and justifies its continued use in future studies.
Abstract: Sea urchins are ecologically and economically important calcifying organisms threatened by acidification of the global ocean caused by anthropogenic CO2 emissions. Propelled by the sequencing of the purple sea urchin (Strongylocentrotus purpuratus) genome, profiling changes in gene expression during exposure to high pCO2 seawater has emerged as a powerful and increasingly common method to infer the response of urchins to ocean change. However, analyses of gene expression are sensitive to experimental methodology, and comparisons between studies of genes regulated by ocean acidification are most often made in the context of major caveats. Here we perform meta-analyses as a means of minimizing experimental discrepancies and resolving broader-scale trends regarding the effects of ocean acidification on gene expression in urchins. Analyses across eight studies and four urchin species largely support prevailing hypotheses about the impact of ocean acidification on marine calcifiers. The predominant expression ...

41 citations


Journal ArticleDOI
TL;DR: In this article, a natural pH gradient caused by marine CO2 seeps off Vulcano Island (Italy) was used to assess the effects of ocean acidification on coccolithophores, which are abundant planktonic unicellular calcifiers.
Abstract: A natural pH gradient caused by marine CO2 seeps off Vulcano Island (Italy) was used to assess the effects of ocean acidification on coccolithophores, which are abundant planktonic unicellular calcifiers. Such seeps are used as natural laboratories to study the effects of ocean acidification on marine ecosystems, since they cause long- term changes in seawater carbonate chemistry and pH, exposing the organisms to elevated CO2 concentrations and therefore mimicking future scenarios. Previous work at CO2 seeps has focused exclusively on benthic organisms. Here we show progressive depletion of 27 coccolithophore spe- cies, in terms of cell concentrations and diversity, along a calcite saturation gradient from calcite 6.4 to 1. Water collected close to the main CO2 seeps had the highest concentrations of malformed Emiliania huxleyi. These ob- servations add to a growing body of evidence that ocean acidification may benefit some algae but will likely cause marine biodiversity loss, especially by impacting calcifying species, which are affected as carbonate saturation falls.

35 citations


Journal ArticleDOI
TL;DR: The results demonstrate that the impacts of OA on key coral reef builders go beyond declines in calcification and growth, and suggest important changes to aspects of population dynamics and community ecology.
Abstract: Calcification and growth of crustose coralline algae (CCA) are affected by elevated seawater pCO2 and associated changes in carbonate chemistry. However, the effects of ocean acidification (OA) on population and community-level responses of CCA have barely been investigated. We explored changes in community structure and population dynamics (size structure and reproduction) of CCA in response to OA. Recruited from an experimental flow-through system, CCA settled onto the walls of plastic aquaria and developed under exposure to one of three pCO2 treatments (control [present day, 389 ± 6 ppm CO2], medium [753 ± 11 ppm], and high [1267 ± 19 ppm]). Elevated pCO2 reduced total CCA abundance and affected community structure, in particular the density of the dominant species Pneophyllum sp. and Porolithon onkodes. Meanwhile, the relative abundance of P. onkodes declined from 24% under control CO2 to 8.3% in high CO2 (65% change), while the relative abundance of Pneophyllum sp. remained constant. Population size ...

Journal ArticleDOI
TL;DR: This review of bryozoan growth and calcification allows a general perspective, but also reveals gaps in knowledge which need to be addressed.
Abstract: Bryozoans are colonial benthic marine inver- tebrate calcifiers, important and especially abundant and diverse in southern hemisphere shelf environments. Large heavily calcified colonies can be up to 50 years old, but most longer-lived bryozoans are limited to 10-20 y. Many smaller species are annual. Radial extension in flat encrust- ing bryozoans is generally on the order of 1-5 mm/y. Erect calcified species generally grow vertically 2-15 mm/y, though articulated species such as Cellaria may reach rates of 40 mm/y. Corresponding calcification rates are generally 10 1 -10 2 mg/y, but there can be an order of magnitude variation in rate among years in high-latitude bryozoans. Multi-branched bryozoans produce up to 24 g of CaCO3/y. The carbonate produced by bryozoans varies from calcite to aragonite and mixtures of both. Skeletal carbonate mineral- ogy of bryozoans is complex and appears to be strongly genetically controlled. Global climate change, leading to increasing water temperatures, will generally increase ma- rine bryozoan metabolic rates, and may increase Mg in calcite. On the other hand, decreasing pH (ocean acidifica- tion) causes corrosion, changes in mineralogy, and de- creased survival. This review of bryozoan growth and cal- cification allows a general perspective, but also reveals gaps in our knowledge which need to be addressed.

Journal ArticleDOI
TL;DR: Against expectations, this study found an increase in predation after exposure of the predator to predicted near-future levels of estuarine pCO2.
Abstract: Ocean acidification is anticipated to decrease calcification and increase dissolution of shelled molluscs. Molluscs with thinner and weaker shells may be more susceptible to predation, but not all studies have measured negative responses of molluscs to elevated pCO2. Recent studies measuring the response of molluscs have found greater variability at the population level than first expected. Here we investigate the impact of acidification on the predatory whelk Morula marginalba and genetically distinct subpopulations of the Pacific oyster Crassostrea gigas. Whelks and eight family lines of C. gigas were separately exposed to ambient (385 ppm) and elevated (1000 ppm) pCO2 for 6 weeks. Following this period, individuals of M. marginalba were transferred into tanks with oysters at ambient and elevated pCO2 for 17 days. The increase in shell height of the oysters was on average 63% less at elevated compared to ambient pCO2. There were differences in shell compression strength, thickness, and mass among family...

Journal ArticleDOI
TL;DR: Taxonomic variation within and between sampled locations throughout the study was observed, suggesting potential yearly variation in communities and continued sampling over a longer timeframe will provide a more complete understanding of seasonality and variation within these communities.
Abstract: Meiofauna are important components of food webs and for nutrient exchange between the benthos and water column. Recent studies have focused on these com- munities in the Gulf of Mexico due to potential impacts of the Deepwater Horizon Oil Spill (DWHOS). In particular, intertidal meiofaunal communities from Mobile Bay and Dauphin Island, Alabama, were previously shown to shift from predominately metazoan taxa prior to DWHOS to a fungal-dominated community after the spill. However, knowledge of variability within these communities remains unknown. Herein, we used Illumina high-throughput ampli- con sequencing to examine variation throughout a year for the same locations for which the organismal shift was noted. Sediment samples were collected bi-monthly for a year (July 2011-July 2012) from which the meiofaunal commu- nity was examined by sequencing the eukaryotic hypervari- able V9 region of the 18S rRNA gene. Results showed that the presence of fungal taxa was limited within these com- munities, suggesting that previously reported acute impacts of the DWHOS on meiofauna were apparently short term. However, these meiofaunal communities show shifts in proportions of metazoan taxa compared to pre-spill sam- ples. Whether this change is due to prolonged impacts of the spill or variation in community composition is unclear. Taxonomic variation within and between sampled locations throughout the study was observed, suggesting potential yearly variation in communities. Continued sampling over a longer timeframe will provide a more complete understand- ing of seasonality and variation within these communities.

Journal ArticleDOI
TL;DR: Fluorescent in situ hybridization is used to localize an algal nuclear gene, prk, found in both larval and adult slug DNA by PCR and in adult RNA by transcriptome sequencing and RT-PCR, confirming gene transfer between alga and slug.
Abstract: The horizontal transfer of functional nuclear genes, coding for both chloroplast proteins and chlorophyll synthesis, from the food alga Vaucheria litorea to the sea slug Elysia chlorotica has been demonstrated by pharmacological, polymerase chain reaction (PCR), real time PCR (qRT-PCR), and transcriptome sequencing experiments. However, partial genomic sequencing of E. chlorotica larvae failed to find evidence for gene transfer. Here, we have used fluorescent in situ hybridization to localize an algal nuclear gene, prk, found in both larval and adult slug DNA by PCR and in adult RNA by transcriptome sequencing and RT-PCR. The prk probe hybridized with a metaphase chromosome in slug larvae, confirming gene transfer between alga and slug.

Journal ArticleDOI
TL;DR: In this paper, the authors used transcriptomes collected for phylogenomic studies to search for toll-like receptor (TLR) genes in poorly sampled lophotrochozoan clades (Annelida, Mollusca, Brachiopoda, Phoronida, and Entoprocta).
Abstract: The growing volume of genomic data from across life represents opportunities for deriving valuable biological information from data that were initially collected for another purpose. Here, we use transcriptomes collected for phylogenomic studies to search for toll-like receptor (TLR) genes in poorly sampled lophotrochozoan clades (Annelida, Mollusca, Brachiopoda, Phoronida, and Entoprocta) and one ecdysozoan clade (Priapulida). TLR genes are involved in innate immunity across animals by recognizing potential microbial infection. They have an extracellular leucine-rich repeat (LRR) domain connected to a transmembrane domain and an intracellular toll/interleukin-1 receptor (TIR) domain. Consequently, these genes are important in initiating a signaling pathway to trigger defense. We found at least one TLR ortholog in all but two taxa examined, suggesting that a broad array of lophotrochozoans may have innate immune systems similar to those observed in vertebrates and arthropods. Comparison to the SMART database confirmed the presence of both the LRR and the TIR protein motifs characteristic of TLR genes. Because we looked at only one transcriptome per species, discovery of TLR genes was limited for most taxa. However, several TRL-like genes that vary in the number and placement of LRR domains were found in phoronids. Additionally, several contigs contained LRR domains but lacked TIR domains, suggesting they were not TLRs. Many of these LRR-containing contigs had other domains (e.g., immunoglobin) and are likely involved in innate immunity.

Journal ArticleDOI
TL;DR: The aboral sensory organ (apical organ) of ctenophores contains a statocyst with a single large statolith which comprises living cells (lithocytes), each containing a large membrane-bound concretion.
Abstract: The aboral sensory organ (apical organ) of ctenophores contains a statocyst with a single large statolith. The statolith comprises living cells (lithocytes), each containing a large membrane-bound concretion. The statolith is supported on the distal ends of four compound motile mechanoresponsive cilia (balancers) which control the beat frequencies of the eight locomotory comb rows, and thereby the orientation of animals to gravity. In Mnemiopsis leidyi and Pleurobrachia pileus, lithocytes arise in the thickened epithelial floor of the apical organ on opposite sides along the tentacular plane. Lithocytes progressively differentiate and migrate toward the apical surface where they bud off next to the bases of the balancers. New lithocytes are transported up the balancers by ciliary surface motility to form the statolith (Noda, 2013). The statolith has a superellipsoidal shape due to the rectangular arrangement of the four balancers and the addition of new lithocytes to its ends via the balancers. The size of the statolith increases with animal size, starting at the highest rate of growth in younger stages and gradually decreasing in larger animals. The total number of developing lithocytes in the epithelial floor increases rapidly in smaller animals and reaches a plateau range in larger animals. Lithocytes are therefore produced continually throughout life for enlargement of the statolith and possibly for turnover and replacement of existing lithocytes. The dome cilia enclosing the statocyst were observed to propagate slow, low-ampitude waves distally. The dome cilia may act as an undulating screen to prevent foreign objects in the seawater from being transported non-specifically up the balancers to make a defective statolith.

Journal ArticleDOI
TL;DR: The results highlight the importance of including density and crowding effects when macroscale patterns are explored, particularly in gregarious species, since these patterns could also be modulated by density-dependent processes, which might then override latitudinal trends of shell thickness when they are not included in the analyses.
Abstract: At broad geographical scales, the variation in bivalve shell thickness can be modulated by environmental factors that vary with latitude, such as sea surface temper- ature (SST), seawater pH, or calcium carbonate availability. Mussels usually form multilayered beds, and shell thickness is also expected to be affected by density and layering due to intraspecific competition. In this work, we explored the geographical variation of shell thickness in the intertidal mussel Perumytilus purpuratus between 18° and 42°S along the southeastern Pacific coast. We tested the hypothesis that there was a positive relationship between shell thickness and SST, and then we explored other variables that could have an effect on thickness, such as density, number of layers, and others environmental variables (pH and calcite concentration). The expected positive linear relationship between shell thickness and sea surface temperature was not found, but when the other population variables were in- cluded in the analysis, an unexpected inverse SST-thickness relationships appeared as significant, probably because this species could be adapted to colder and more acid seawater as are those of the tips of South America. Thickness was also negatively affected by density, which was expected for a gregarious species showing high intraspecific competition. Finally, our results highlight the importance of including density and crowding effects when macroscale patterns are explored, particularly in gregarious species, since these pat- terns could also be modulated by density-dependent pro- cesses, which might then override latitudinal trends of shell thickness when they are not included in the analyses.

Journal ArticleDOI
TL;DR: Antibodies to α- or β-tubulin and to the bioactive peptide FMRFamide were used to investigate the organization of the ectodermal nervous structures in five species of scyphomedusae as mentioned in this paper.
Abstract: Antibodies to α- or β-tubulin and to the bioactive peptide FMRFamide were used to investigate the organization of the ectodermal nervous structures in five species of scyphomedusae. Within the swim system, morphological evidence, including a developmental sequence, suggests that the tubulin-immunoreactive nerve net in the subumbrella is the Giant Fiber Nerve Net (Motor Nerve Net) that directly activates the swim musculature, and the FMRFamide-immunoreactive nerve net is the Diffuse Nerve Net that serves a sensory function and also enhances swim muscle activity. Similar dual labeling was found in other structures, including those involved in feeding and protective reactions (pedalia and tentacles, radial strips of smooth muscle), and in the exumbrella, where the networks were associated with batteries of nematocysts. In addition, FMRFamide immuno-staining in the rhopalia and rhopalial niches suggests that sensory components of these networks may aid in the gravitational sense of scyphomedusae.

Journal ArticleDOI
TL;DR: In this species dissolution of the sperm plug was synchronized with ovarian development and occurred simultaneously with spermatophore dehiscence, showing the evolutionary relationship of the seminal receptacle and the female reproductive system to the storage of sperMatophores and spermatozoa.
Abstract: To understand sperm plug dissolution and spermatophore dehiscence in Portunidae, histological and ultrastructural changes in the seminal receptacle (SR) of Arenaeus cribrarius were investigated during ovarian development. In juvenile females the SR was filled with acid polysaccharides and the dorsal epithelium was stratified. Mated females with rudimentary ovaries showed a large SR filled by a glycoprotein sperm plug. This plug was present until the developing-ovary stage, when spermatophore dehiscence and intense holocrine secretions in the dorsal dense layer occurred. The plug was absent after the intermediate stage, and the SR became flaccid. The secretion produced moved the spermatophores into the ventral region. The modified dorsal epithelium in the transition between the dorsal and ventral regions released acid polysaccharides, which were found among the sperm, by exocytosis. The morphological changes of the SR in A. cribrarius, including the presence of the sperm plug, followed the macroscopic pattern observed in other members of Portunidae, such as blue crabs. However, in this species dissolution of the sperm plug was synchronized with ovarian development and occurred simultaneously with spermatophore dehiscence, showing the evolutionary relationship of the seminal receptacle and the female reproductive system to the storage of spermatophores and spermatozoa.

Journal ArticleDOI
TL;DR: It is shown that burrowing worms control their velocity by increasing or decreasing their burrowing frequency rather than by altering cycle distance as shown previously for crawling earthworms.
Abstract: Muddy and sandy sediments have different physical properties. Muds are cohesive elastic solids, whereas granular beach sands are non-cohesive porous me- dia. Infaunal organisms such as worms that burrow through sediments therefore face different mechanical challenges that potentially lead to a variety of burrowing strategies and morphologies. In this study we compared three morpholog- ically distinct polychaete species representing different clades in the family Orbiniidae and related differences in their burrowing behaviors and morphologies to their natural environments (mud or sand). Worms burrowed in transpar- ent analogs for muds and sands, and kinematic analysis showed differences both among species and between mate- rials. Leitoscoloplos pugettensis lives in mud and burrows by fracture, using its pointed head to concentrate stress at the tip of the burrow. Naineris dendritica lives in sand and uses its broader head that fluctuates in width over a bur- rowing cycle to decrease backward slipping in sand, poten- tially preventing burrow collapse. Orbinia johnsoni lives in sand and uses internal body expansions to pack sand grains, another mechanism to prevent burrow collapse. By combin- ing data from species and materials to obtain a broad range of burrowing velocities, we show that burrowing worms control their velocity by increasing or decreasing their bur- rowing frequency rather than by altering cycle distance as shown previously for crawling earthworms. This study demonstrates how fairly small evolutionary divergences in morphologies and behaviors facilitate locomotion in envi- ronments with different physical constraints.

Journal ArticleDOI
TL;DR: Data show that the bacterial symbionts not only induce apoptosis of the field, but also change the form, function, and biochemistry of the cells as part of the morphogenic program.
Abstract: The symbiotic association between the Hawaiian bobtail squid Euprymna scolopes and the luminous marine bacterium Vibrio fischeri provides a unique opportunity to study epithelial morphogenesis. Shortly after hatching, the squid host harvests bacteria from the seawater using currents created by two elaborate fields of ciliated epithelia on the surface of the juvenile light organ. After light organ colonization, the symbiont population signals the gradual loss of the ciliated epithelia through apoptosis of the cells, which culminates in the complete regression of these tissues. Whereas aspects of this process have been studied at the morphological, biochemical, and molecular levels, no in-depth analysis of the cellular events has been reported. Here we describe the cellular structure of the epithelial field and present evidence that the symbiosis-induced regression occurs in two steps. Using confocal microscopic analyses, we observed an initial epithelial remodeling, which serves to disable the function of the harvesting apparatus, followed by a protracted regression involving actin rearrangements and epithelial cell extrusion. We identified a metal-dependent gelatinolytic activity in the symbiont-induced morphogenic epithelial fields, suggesting the involvement of Zn-dependent matrix metalloproteinase(s) (MMP) in light organ morphogenesis. These data show that the bacterial symbionts not only induce apoptosis of the field, but also change the form, function, and biochemistry of the cells as part of the morphogenic program.

Journal ArticleDOI
TL;DR: Fertilization of Strongylocentrotus purpuratus was robust to a broad range of pH, encompassing both present-day and future ocean acidification scenarios, even though the two congeners have similar habitats.
Abstract: Ocean acidification impacts fertilization in some species of sea urchin, but whether sensitivity is great enough to be influenced by present-day pH variability has not been documented. In this study, fertilization in two congeneric sea urchins, Strongylocentrotus purpuratus and S. franciscanus, was found to be sensitive to reduced pH, 7.50, but only within a range of sperm-egg ratios that was species-specific. By further testing fertilization across a broad range of pH, pH-fertilization curves were generated and revealed that S. purpuratus was largely robust to pH, while fertilization in S. franciscanus was sensitive to even modest reductions in pH. Combining the pH-fertilization response curves with pH data collected from these species' habitat demonstrated that relative fertilization success re- mained high for S. purpuratus but could be as low as 79% for S. franciscanus during periods of naturally low pH. In order for S. franciscanus to maintain high fertilization suc- cess in the present and future, adequate adult densities, and thus sufficient sperm-egg ratios, will be required to negate the effects of low pH. In contrast, fertilization of S. purpu- ratus was robust to a broad range of pH, encompassing both present-day and future ocean acidification scenarios, even though the two congeners have similar habitats.

Journal ArticleDOI
TL;DR: Growth rates did not decrease as fronds approached their maximum observed size, suggesting that maximum frond size might be determined not by intrinsic factors but by external factors such as wave-induced drag forces.
Abstract: Ocean acidification caused by rising atmospheric CO2 is predicted to negatively impact growth and calcification rates of coralline algae. Decreases in coralline abundance may have cascading effects on marine ecosystems and on carbon sequestration worldwide. In this study, we measured growth and calcification rates of three common species of articulated coralline algae (Bossiella plumosa, Calliarthron tuberculosum, and Corallina vancouveriensis) at an intertidal field site in British Columbia. Linear growth rates measured in the field were slow, although Bossiella grew significantly faster (0.22 cm mon−1) than Calliarthron and Corallina (0.17 and 0.15 cm mon−1, respectively). Growth rates in the field were generally slower than growth rates in the laboratory, suggesting that data generated in the laboratory may not be representative of natural field conditions. Growth rates did not decrease as fronds approached their maximum observed size, suggesting that maximum frond size might be determined not by intri...

Journal ArticleDOI
TL;DR: The results indicate that gamete production in M. capitata is a resilient process; no differences in gamete development or fecundity were observed among sites with very different sedimentation regimes.
Abstract: Environmental conditions can influence the physiology of marine organisms and have important impli- cations for their reproductive performance and capacity to supply new recruits. This study examined the seasonal re- productive patterns of the coral Montipora capitata in hab- itats exposed to different sedimentation regimes. Although M. capitata is a main reef-building coral in the Hawaiian Archipelago, little is known about the gametogenic cycle and reproductive ecology of this important species. Our results indicate that gamete production in M. capitata is a resilient process; no differences in gamete development or fecundity were observed among sites with very different sedimentation regimes. The gametogenic cycle of M. capi- tata lasts between 10 and 11 months, with spawning occur- ring over 3-5 months during warmer months (May-Sep- tember). Oocytes were found throughout the year, but spermatocysts were only found April-August. The largest increases in oocyte size occurred during February to May, the months when solar radiation increased rapidly. The largest variation in oocyte sizes was found during July and August; during this period individual colonies contained mature oocytes for immediate spawning and new oocytes being formed for spawning the next year. The capacity of M. capitata to reproduce in areas with high sedimentation is an interesting finding highlighting the potential of the spe- cies for acclimatization, adaptation, or both. Despite this optimistic finding, the management of terrestrial runoff and the restoration of habitat quality for corals remains a top

Journal ArticleDOI
TL;DR: The results offer insight into how the peripheral nerve nets of box jellyfish are organized to produce the complex swimming, feeding, and defensive behaviors observed in cubomedusae.
Abstract: At least two conducting systems are well documented in cubomedusae. A variably diffuse network of large neurons innervates the swim musculature and can be visualized immunohistochemically using antibodies against α- or β-tubulin. Despite the non-specificity of these antibodies, multiple lines of evidence suggest that staining highlights the primary motor networks. These networks exhibit unique neurite distributions among the muscle sheets in that network density is greatest in the perradial frenula, where neurites are oriented in parallel with radial muscle fibers. This highly innervated, buttress-like muscle sheet may serve a critical role in the cubomedusan mechanism of turning. In scyphomedusae, a second subumbrellar network immunoreactive to antibodies against the neuropeptide FMRFamide innervates the swim musculature, but it is absent in cubomedusae. Immunoreactivity to FMRFamide in cubomedusae is mostly limited to a small network of neurons in the pacemaker region of the rhopalia, the pedalial apex at the nerve ring junction, and a few neuron tracts in the nerve ring. However, FMRFamide-immunoreactive networks, as well as tubulin-immunoreactive networks, are nearly ubiquitous outside of the swim muscle sheets in the perradial smooth muscle bands, manubrium, pedalia, and tentacles. Here we describe in detail the peripheral nerve nets of box jellyfish on the basis of immunoreactivity to the antibodies above. Our results offer insight into how the peripheral nerve nets are organized to produce the complex swimming, feeding, and defensive behaviors observed in cubomedusae.

Journal ArticleDOI
TL;DR: It is demonstrated that E. brasiliensis produces endogenous melatonin, in the gonads, under a circadian pattern with a nocturnal peak of production, and it is shown that the enzymes arylalkylamine N-acetyltransferase and tryptophan hydroxylase are present and are probably regulating the melatonin production.
Abstract: The primary hormone of the vertebrate pineal gland, melatonin, has been identified broadly throughout the tree of life, in animals, plants, and fungi, supporting a deep evolutionary origin for this signaling molecule. However, some key groups have not been studied. Echinoderms, deu- terostome animals, are one of these groups. Herein we study the presence of melatonin and enzymes of its pathway in the sea star Echinaster brasiliensis. We demonstrate that E. brasiliensis produces endogenous melatonin, in the go- nads, under a circadian pattern with a nocturnal peak of production. We also show that the enzymes arylalkylamine N-acetyltransferase (AANAT) and tryptophan hydroxylase (TPH) are present and are probably regulating the melatonin production.

Journal ArticleDOI
TL;DR: Early life stages of the coral Seriatopora caliendrum were used to test the hypothesis that the depression of dark respiration in coral recruits by high pCO2 is caused by perturbed protein metabolism, and findings suggest that protein anabolism accounted for a large proportion of metabolic costs in Coral recruits and was affected by highpCO2.
Abstract: Early life stages of the coral Seriatopora caliendrum were used to test the hypothesis that the depression of dark respiration in coral recruits by high pCO2 is caused by perturbed protein metabolism. First, the contribution of protein anabolism to respiratory costs under high pCO2 was evaluated by measuring the aerobic respiration of S. caliendrum recruits with and without the protein synthesis inhibitor emetine following 1 to 4 days at 45 Pa versus 77 Pa pCO2. Second, protein catabolism under high pCO2 was evaluated by measuring the flux of ammonium (NH4 (+)) from juvenile colonies of S. caliendrum incubated in darkness at 47 Pa and 90 Pa pCO2. Two days after settlement, respiration of recruits was affected by an interaction between emetine and pCO2, with emetine reducing respiration 63% at 45 Pa pCO2 and 27% at 77 Pa pCO2. The interaction disappeared 5 days after settlement, when respiration was reduced 27% by emetine under both pCO2 conditions. These findings suggest that protein anabolism accounted for a large proportion of metabolic costs in coral recruits and was affected by high pCO2, with consequences detected in aerobic respiration. Juvenile S. caliendrum showed net uptake of NH4 (+) at 45 Pa pCO2 but net release of NH4 (+) at 90 Pa pCO2, indicating that protein catabolism, NH4 (+) recycling, or both were affected by high pCO2. Together, these results are consistent with the hypothesis that high pCO2 affects protein metabolism in corals.

Journal ArticleDOI
TL;DR: It is hypothesized that the host B. neritina may regulate the distribution of the symbiont within the colony via mechanisms of biofilm degradation and actin rearrangement, and consequently, influences bryostatin localization to bestow symbionT-associated protection to larvae developing in the reproductive zooids.
Abstract: Mutualism, a beneficial relationship between two species, often requires intimate interaction between the host and symbiont to establish and maintain the partnership. The colonial marine bryozoan Bugula neritina harbors an as yet uncultured endosymbiont, “Candidatus Endobugula sertula,” throughout its life stages. The bacterial symbiont is the putative source of bioactive complex polyketide metabolites, the bryostatins, which chemically defend B. neritina larvae from predation. Despite the presence of “Ca. Endobugula sertula” in all life stages of the host, deterrent bryostatins appear to be concentrated in reproductive portions of the host colony, suggesting an interaction between the two partners to coordinate production and distribution of the metabolites within the colony. In this study, we identified host genes that were differentially expressed in control colonies and in colonies cured of the symbiont. Genes that code for products similar to glycosyl hydrolase family 9 and family 20 proteins, actin,...

Journal ArticleDOI
TL;DR: An in-depth survey of next-generation DNA sequencing of ciliate diversity and community structure in two permanently ice-covered McMurdo Dry Valley lakes during the austral summer and autumn suggests that the vertical trends in dissolved oxygen concentration and salinity may play a critical role in structuring ciliate communities.
Abstract: We report an in-depth survey of next-generation DNA sequencing of ciliate diversity and community structure in two permanently ice-covered McMurdo Dry Valley lakes during the austral summer and autumn (November 2007 and March 2008). We tested hypotheses on the relationship between species richness and environmental conditions including environmental extremes, nutrient status, and day length. On the basis of the unique environment that exists in these high-latitude lakes, we expected that novel taxa would be present. Alpha diversity analyses showed that extreme conditions-that is, high salinity, low oxygen, and extreme changes in day length-did not impact ciliate richness; however, ciliate richness was 30% higher in samples with higher dissolved organic matter. Beta diversity analyses revealed that ciliate communities clustered by dissolved oxygen, depth, and salinity, but not by season (i.e., day length). The permutational analysis of variance test indicated that depth, dissolved oxygen, and salinity had significant influences on the ciliate community for the abundance matrices of resampled data, while lake and season were not significant. This result suggests that the vertical trends in dissolved oxygen concentration and salinity may play a critical role in structuring ciliate communities. A PCR-based strategy capitalizing on divergent eukaryotic V9 hypervariable region ribosomal RNA gene targets unveiled two new genera in these lakes. A novel taxon belonging to an unknown class most closely related to Cryptocaryon irritans was also inferred from separate gene phylogenies.