Orientated growth of Membranipora membranacea (L.) on the thallus of Saccorhiza polyschides (Lightf.) Batt.

Orientated growth is described in colonies of Membranipora membranacea (L.) growing on the large brown seaweed Saccorhiza polyschides (Lightf.) Batt. On average, 60% of the growth of the colonies was directed proximally along the long axis of the plant, irrespective of the region of the plant on which the colonies were growing or their proximity to its primary meristem. These results seem to rule out the possibility that orientated growth in Membranipora is a response to an age dependent polarity in the host plant, since the tissue ages in opposite directions in the lamina and stipe yet the growth of Membranipora is orientated in the same direction on both. The possibility that directional growth in this species may be a rheopositive response is discussed.     

Invasive species as a new food source: does a nudibranch predator prefer eating an invasive bryozoan?

Membranipora membranacea is an invasive bryozoan that was first found in the Gulf of Maine in 1987 and within two years became the dominant organism living on kelps. Membranipora may have become dominant so quickly because it had little competition in a relatively unoccupied niche; however, lack of predation has also probably played a major role. Where Membranipora is native, there is usually a specialist nudibranch predator that keeps the population in check. For example, in European populations, the nudibranch Polycera quadrilineata prefers Membranipora while Onchidoris muricata is known to prefer another bryozoan, Electra pilosa. Electra, Membranipora, and Onchidoris are all now found in the Gulf of Maine while Polycera is not. We tested whether Onchidoris would (1) eat Membranipora at all, (2) eat Membranipora and Electra at different rates, and (3) show a preference for eating Membranipora or Electra when given a choice. We found that Onchidoris does eat Membranipora, and it generally eats Membranipora faster than Electra. However, when given a choice, Onchidoris prefers Electra. Onchidoris typically reproduces in the spring and grows over the fall and winter, but has recently been found reproducing in the winter in New Hampshire. Although it does not survive the winter as well as Electra, Membranipora is the dominant organism living on many macroalgae in the late summer and fall. Thus, the large Membranipora food source now available in the summer and fall may allow Onchidoris to reproduce earlier.     

Resource space partitioning by the Bryozoa of a Fucus serratus L. Community

The spatial distributions of five Bryozoa species encrusting Fucus serratus L. plants in Strangford Lough, Northern Ireland, have been examined in two cross-sectional samples yielding 80 plants and 1326 sampling units drawn from 13 environmentally diverse sites. The co-occurences of Flustrellidra hispida (Fabricius), Alcyonidium hirsutum (Fleming), Electra pilosa (L.), Membranipora membranacea (L.), and Celleporella hyalina (L.) on individual Fucus serratus plants were consistent with independent settlement onto each plant, but their joint distributions within the plants were markedly non-random. Measurements of behavioural interactions between species showed that competitive abilities declined through the sequence Flustrellidra, Alcyonidium, Electra, Membranipora, which parallels the sequence of competition (Levins' α) coefficients calculated from spatial distribution data. Competitive ability varied with position on the plant. Flustrellidra and Alcyonidium reversing their relative competitive superiority between basal and distal regions of the fronds. Flustrellidra and Electra were strongly associated under all conditions. Alcyonidium was also frequently present with this pair, though its numerical abundance was inversely related to that of Flustrellidra. Celleporella tended to co-occur with Electra whilst avoiding Flustrellidra and Alcyonidium. Membranipora numbers were inversely related to those of the other species. Analyses of competition coefficients showed that Flustrellidra, Alcyonidium and Electra each peaked in competitive ability against Membranipora at different points along the frond, such that the latterwaas effectively excluded by direct as well as by diffuse competition. Membranipora populations had a greater dependence on the segment area available for colonization than had any other bryozoan species.     

Effects of the bryozoan Membranipora tuberculata (Bosc.) on the photosynthesis and growth of Gelidium rex Santelices et Abbott

Several species of Membranipora commonly occur on brown and red algae. It is currently believed that these bryozoans could affect growth of the host plant by modifying incident light. In the present study, we report on the changes that occur in both intensity and quality of light passing through colonies of M. tuberculata (Bosc.) and on the effects of bryozoans on growth of the host plant. M. tuberculata decreases photon-flux density by up to 56% of the incident light and slightly affects the quality of the incident light. Although the bryozoan reduces the photosynthetic rate of Gelidium rex Santelices et Abbott, it does not have a net effect on algal growth. It is concluded that the effects of epifauna on algal growth depend on the nature of the algal structure colonized. Therefore, it cannot be predicted a priori that encrusted thalli should grow at a slower rate than nonencrusted thalli.     

Contrasting patterns of spread in interacting invasive species: Membranipora membranacea and Codium fragile off Nova Scotia

In the Northwest Atlantic, overgrowth of the competitively dominant, native kelps by an invasive bryozoan Membranipora membranacea increases frond erosion, which has facilitated the establishment and spread of the invasive macroalga Codium fragile ssp fragile. To document the spread of both introduced species along the Atlantic coast of Nova Scotia from initial introduction points (the ‘epicentre’) southwest of Halifax, we conducted video-surveys of shallow rocky habitats along the southwestern shore of Nova Scotia (100 km linear distance, encompassing the range of M. membranacea) in 2000, and then along the entire Atlantic coast in 2007 (650 km). Membranipora membranacea was observed continuously throughout the surveyed ranges in 2000 and 2007, wherever kelps were present, suggesting natural dispersal via planktonic larvae. Codium fragile was observed along 95 km of the surveyed range in 2000 and along 445 km in 2007, with a relatively patchy distribution beyond the epicentre, suggesting a combination of natural and anthropogenic dispersal mechanisms. Rockweed-dominated (Fucus spp.) or mixed algal assemblages common outside the epicentre may alter the interaction between M. membranacea and C. fragile, since seaweeds other than kelp are not subject to defoliation by the bryozoan. Percent cover of kelp at the epicentre generally increased from 2000 to 2007, while that of C. fragile generally decreased. Codium fragile was the dominant canopy alga at 54% of sites in 2000 and at only 15% of sites in 2007. These findings indicate that, at near decadal timescales, C. fragile does not prevent re-colonization by native kelps.     

Grazing damage and encrustation by an invasive bryozoan reduce the ability of kelps to withstand breakage by waves

Increased breakage of macroalgal fronds during large wave events can significantly reduce canopy cover and biomass. We examined the effects of encrustation by the invasive bryozoan Membranipora membranacea and damage by the snail Lacuna vincta on the ability of kelp blades (Saccharina longicruris, Laminaria digitata, and Laminaria complanata) to withstand wave forces. Using standard materials testing procedures, we documented significant reductions in the maximum stress before breakage, toughness, and extensibility of blade material following bryozoan encrustation. Histological sections of blade tissue indicated a significant degradation of the outer layers of cells following prolonged encrustation by M. membranacea as a likely cause of weakening. Full-thickness perforations and partial-thickness grazing scars also reduced blade strength, suggesting that grazing damage can initiate cracks that lead to blade breakage. Our findings provide a mechanistic link between the damaging effects of mesograzers and encrusting bryozoa on their algal hosts and the export of detrital material from subtidal kelp beds.     

Density effects in a colonial monoculture: experimental studies with a marine bryozoan (Membranipora membranacea L.)

Summary Naturally occurring monocultures of plants and animals are not common, despite recent emphasis on the analysis of density effects in artificial plant monocultures. In natural populations, Membranipora membranacea, an encrusting marine bryozoan, usually forms monospecific, nearly even-aged stands on kelp blades. We experimentally manipulated the density of M. membranacea colonies and monitored the responses of individual colonies on settling panels. Colonies undergo a sub-annual cycle of growth, stasis and reproduction, shrinkage, and death. However, crowding by conspecifics accelerates the transition to stasis, triggers early onset of reproduction, and results in increased stage-specific mortality. Unlike many interactions involving colonial invertebrates, overgrowth rarely occurs at boundaries of M. membranacea colonies. Instead, colonies stop growing when they contact conspecifics; therefore more dense assemblages are populated with smaller individual colonies. At the peak in colony size during August, the mean size among colonies grown at high population densities was 300 mm² less than colonies grown at low densities or approximately 62% smaller. Mortality was concentrated in small size classes; at the end of the season colonies gradually shrank to the smallest size classes and then died. We summarized the demography of M. membranacea colonies on low- and high-density panels using size-classified transition matrices and used loglinear analysis to examine the effects of density and time on the transition patterns. As the amount of free space on panels declined, so did the frequency of upward size-class transitions. Our analysis revealed that free space declined more rapidly on panels in the high density treatment and that the transitional probabilities were sensitive to density of conspecifics and seasonal change, but only for some size classes and during some time periods.     

Observations on the ecology of Membranipora (bryozoa) and a major predator Doridella steinbergae (nudibranchiata) along the fronds of Laminaria saccharina at Friday Harbor,washington

The distribution of the bryozoan Membranipora and one of its major predators, the nudibranch Doridella steinbergae (Lance) along the fronds of Laminaria saccharina (L.) Lamour. at Friday Harbor, Washington were studied during the summer (July–August) 1975. Whilst the fronds are most heavily encrusted by the bryozoan in the middle and distal regions, settlement occurs principally in the younger more basal regions of the plants. The distribution pattern of the nudibranch closely parallels that of its prey though there is a tendency for the most distal regions, especially in older plants, to be avoided. An average density of 240 Doridella/plant was found for plants of mean length 91.0 cm. Despite the severe predation pressure imposed by this nudibranch, evidence tends to suggest that these extensive and highly productive Membranipora populations could probably support even higher densities of Doridella than those presently found — at least over that period of the year during which this investigation was made.     

The epizoic diatom community on four bryozoan species from Helgoland (German Bight, North Sea)

The composition of the diatom community on the bryozoans Electra pilosa, Membranipora membranacea, Flustra foliacea, and Alcyonidium gelatinosum from the German Bight was studied by light and scanning electron microscopy. In total, members of 26 diatom genera were found, with Cocconeis, Tabularia, Licmophora, Amphora, and Navicula being the most abundant. The amount and the composition of the diatom covering seem to be typical for single bryozoan species. Electra pilosa and Membranipora membranacea showed a rather dense covering with 71–547 cells/mm² and 77–110 cells/mm², respectively. The most prominent genus on Electra pilosa was Cocconeis, reaching up to 58% of all diatoms in one sample, followed by Navicula, Tabularia and Amphora. The most abundant genera on Membranipora membranacea were Tabularia and Licmophora, making up almost 70% of all diatoms in one sample, followed by Navicula, Cocconeis and Amphora. The diatom composition was very stable on all Electra samples, but varied on Membranipora samples. With <1–27 cells/mm², diatoms were much less abundant on Alcyonidium gelatinosum. Members of the genera Tabularia and Navicula were the most frequently found benthic diatoms, whereas the planktonic forms Coscinodiscus, Cyclotella, and Thalassiosira made up 35% of the diatoms. On Flustra foliacea, diatoms were virtually absent, with fewer than 5 cells/mm². The low diatom numbers are probably due to toxic metabolites produced by the host. The same may be true for Alcyonidium gelatinosum, but here they might also be a consequence of the surface properties of the bryozoan. Electronic Publication     

Colony Structure and Seasonal Differences in Light and Nitrogen Modify the Impact of Sessile Epifauna on the Giant Kelp Macrocystis pyrifera (L.) C Agardh

The presence of the stoloniferous hydroid Obelia geniculata (L.) had no effect on the pigment concentration or nitrogen status of underlying blade tissue of the giant kelp Macrocystis pyrifera (L.) C. Agardh. The sheet-like colonies of the bryozoan Membranipora membranacea (L.) markedly reduced the pigment concentration of colonized blade tissue, but only during winter. Reductions in pigment concentration are most likely a result of damage to underlying tissue due to some factor related to the presence of bryozoan colonies on blade surfaces. Blade tissue colonized by M. membranacea also had higher δ¹⁵N signatures than surrounding bryozoan-free tissue, possibly indicating the provision of nitrogen to M. pyrifera by bryozoan colonies. Results show that seasonal changes in nitrogen and colony size can strongly modify the effect of epifauna on macroalgae they colonize. Unlike bryozoans, hydroid colonies provided no barrier to nitrogen uptake by colonized M. pyrifera tissue and enhanced ammonium uptake was observed for tissue colonized by O. geniculata during nitrogen limitation. Epifauna with stoloniferous growth forms such as hydroids are more likely to have benign or even mutualistic relationships with macroalgae they colonize than the sheet-like colonies of bryozoans.     

Acclimation of brown seaweeds in an outdoor cultivation system and their cytokinin-like activity

Four of the most abundant intertidal eastern Mediterranean brown seaweeds were repeatedly inoculated in an outdoor cultivation system for acclimatization. Diciyopteris membranacea was best acclimated and survived for nine months in the system. D. membranacea growth rate showed a positive relationship with irradiance and temperature during nine months of cultivation. Cystoseira sp., Sargassum vulgare and Padina pavonia were not acclimated and survived for shorter times, presumably because of inadequate conditions. All four species showed a cytokinin-like activity assayed with the barley leaf senescence, and promoted radish seed germination. The cytokinin-like activity in Diciyopteris membranacea was relatively stable throughout the cultivation time, as shown by the barley leaf senescence assay, and it acted as a growth promoter of bean and lettuce seedlings. Partial fractionation of the crude seaweed extract showed an ash active component and a natural cytokinin one, which was presumably composed of minor polar and major nonpolar fractions.     

Structure and occurrence of cyphonautes larvae (bryozoa,ectoprocta)

We have studied larvae of the freshwater ctenostome Hislopia malayensis with scanning electron microscopy (SEM), confocal laser scanning microscopy (CLSM), and LM of serial sections. Some additional observations on larvae of M. membranacea using SEM and CLSM are also reported. The overall configuration of muscles, nerves, and cilia of the two larvae are identical. However, the larva of H. malayensis is much smaller than that of M. membranacea, which may explain most of the differences observed. Although all major nerves and muscle strands are present in H. malayensis, they are generally composed of fewer fibers. The H. malayensis larva lacks the anterior and posterior intervalve cilia. Its pyriform organ is unciliated with only a small central depression. The adhesive epithelium is not invaginated as an adhesive sac and lacks the large muscles interpreted as adhesive sac muscles in the M. membranacea larva. The velum carries two rows of ciliated cells, though the lower “row” consists of only one or two cells. Both rows of ciliated cells are innervated by nerves, which have not been detected in the M. membranacea larva. The ciliated ridge of H. malayensis lacks the frontal cilia. The planktotrophic cyphonautes larvae in a number of ctenostome clades and in the “basal” cheilostome clade Malacostega (and probably in the earliest cheilostomes) support the idea that the cyphonautes larva is the ancestral larval type of the Eurystomata. It may even represent the ancestral larval type of the bryozoans (= ectoprocts). J. Morphol. 271:1094‐1109, 2010. © 2010 Wiley‐Liss, Inc.     

Observations on some epibionts of gulf-weed,Sargassum natans (L.) Meyen

The succession of epibionts on gulf-weed, Sargassum natans (L.) Meyen, is described. Only the hydroid Clytia noliformis (McCrady) colonizes the newest algal growth, spreading rapidly from below towards the frond tips by means of stolons. The remaining species — the bryozoon Membranipora tuberculata (Bosc), the spirorbid Janua formosa (Bush) and the blue-green alga Calothrix crustacea Schousb. & Thurs. — establish themselves through a free-swimming phase but, instead of attaching near the meristem as is usual on other algae, the larvae and hormogonia (dispersal phase of Calothrix) settle well away from the growing tip of the Sargassum. Such behaviour is consistent with the view that tannins present in the young thallus inhibit the establishment of the surface microflora which is a pre-requisite for the settlement of larger epibionts.Janua shows a strong preference for the bladders of the Sargassum, and Calothrix for the leaflets; but Membranipora appears to settle equally well on bladders, leaflets, and stem.Observations on young colonies of Membranipora reveal that the metamorphosing larvae were orientated with respect to the axis of the Sargassum leaflets. Water flow, which has previously been considered as likely to provide a directional stimulus for such orientation, cannot be the operative factor in this case.     

EFFECTS OF THE ENCRUSTING BRYOZOAN,MEMBRANIPORA MEMBRANACEA,ON THE LOSS OF BLADES AND FRONDS BY THE GIANT KELP,MACROCYSTIS PYRIFERA (LAMINARIALES)1

Juvenile sporophytes of the giant kelp, Macrocystis pyrifera (L.) C. A. Agardh, were transplanted from local kelp beds to stations located various distances from the outfall from an electrical generating station that was known to cause an increase in the settlement of fouling organisms. Plants near the outfall became heavily fouled by the encrusting bryozoan, Membranipora membranacea (L.), and lost about one-third of their blades during the course of the experiment. Blade loss was significantly correlated with amount of fouling. To test the hypothesis that fouling causes blade loss, we paired fouled and unfouled plants of about the same age, overall length, and number of fronds and placed them at stations in nearby kelp beds and near the outfall. At the stations in the kelp beds, the fouled plants lost blades more rapidly than the unfouled controls. However, at the station near the outfall the “control” plants quickly became fouled so there was little difference in treatments and there was no significant difference in blade loss. Plants fouled by Membranipora suffered greater blade loss than clean plants probably because fouled blades are fragile and break off easily and because fish bite off chunks of blade while foraging on the attached bryozoans.     

Influence of UV radiation on growth of sporelings of three non-geniculate coralline red algae from Southern Iberian Peninsula

The effects of UV radiation (UVR) on growth of sporelings of Melobesia membranacea (Esper) Lamouroux, Lithophyllum incrustans Philippi and Mesophyllum lichenoides (Ellis) Lemoine, were investigated by culturing the algae under different doses of photosynthetically active radiation (PAR) only and PAR + UVR. Under natural conditions, the light fields occurring in the habitats of the three species differ substantially. Whereas M. lichenoides and L. incrustans inhabit sun‐exposed places in the eulittoral and upper part of the sublittoral, M. membranacea grows as an epiphyte in shady crevices in the eulittoral, where irradiance is < 10% of that in sun‐exposed places. The relative growth rate (RGR) of sporelings of these non‐geniculate coralline algae was affected by the UVR. The extent of harmful UVR effects on growth rate showed a similar increase as a function of the logarithm of the dose in the three species, inferred by a similar slope in all the linear regressions for a given action spectrum. The inhibition of growth under the PAR + UVR showed similar features in the two species of non‐geniculate coralline species from sun‐exposed places, that is, similar intercepts and slopes in the linear regressions of RGR as a function of the logarithm of the biologically effective dose.     

Appetitive Responses to Computer-Generated Visual Stimuli by Female Rhombodera basalis, Deroplatys lobata, Hierodula membranacea, and Miomantis sp. (Insecta: Mantodea)

We used computer-generated stimuli to assess the stimulus parameters eliciting prey-directed behaviors in four mantis species: Rhombodera basalis (60 mm body length), Deroplatys lobata (70 mm), Hierodula membranacea (80 mm), Miomantis sp (38 mm). All responded appetitively to erratically moving disks subtending 10° or more. R. basalis responded more consistently to checkered (versus solid black) disks; only D. lobata displayed a size preference (14–23 deg disks); Miomantis sp. struck at disks as large as did the largest species; only Miomantis sp. displayed approaching behavior. H. membranacea and R. basalis preferred black disks on a white background (versus the reverse), and red disks (versus blue or green) on a brightness-matched grey background. All preferred elongated stimuli moving parallel (versus perpendicular) to their long axes.     

Does Green Light Influence the Fluorescence Properties and Structure of Phototrophic Biofilms?

Artificial illumination can harm works of art by inducing the development of photosynthetic biofilms. With the aim of preventing biodeterioration or esthetic damage to such surfaces, we evaluated and compared the effects of illuminating biofilms formed by Gloeothece membranacea (cyanobacteria) and Chlorella sorokiniana (Chlorophyta) using exclusively white or green light.     

Global mitochondrial DNA phylogeography and biogeographic history of the antitropically and longitudinally disjunct marine bryozoan Membranipora membranacea L. (Cheilostomata): another cryptic marine sibling species complex?

The origin of disjunct distributions in high dispersal marine taxa remains an important evolutionary question as it relates to the formation of new species in an environment where barriers to gene flow are not always obvious. To reconstruct the relationships and phylogeographic history of the antitropically and longitudinally disjunct bryozoan Membranipora membranacea populations were surveyed with mtDNA cytochrome oxidase 1 (COI) sequences across its cosmopolitan range. Maximum parsimony, maximum likelihood and Bayesian genealogies revealed three deep clades in the North Pacific and one monophyletic clade each in the southeast Pacific (Chile), southwest Pacific (Australia/New Zealand), North Atlantic and southeast Atlantic (South Africa). Human-mediated dispersal has not impacted M. membranacea’s large-scale genetic structure. M. membranacea did not participate in the trans-arctic interchange. Episodic long-distance dispersal, combined with climatic vicariance can explain the disjunct distribution. Dispersal led southward across the tropics perhaps 13 mya in the East Pacific and again northwards perhaps 6 mya in the Eastern Atlantic to colonize the North Atlantic from the south, and along the West Wind Drift to colonize Australia. The clades differentiated over evolutionary time in their respective ocean region, potentially forming a sibling species complex. The taxonomic status of the clades is discussed.     

Induced changes in the proteomic profile of the phaeophyte Saccharina japonica upon colonization by the bryozoan Membranipora membranacea

The lacy crust bryozoan Membranipora membranacea frequently colonizes the late harvested blades of aquacultured Saccharina japonica. From proteomic profiles of S. japonica, 145 and 91 protein spots were detected from colonized and healthy tissues, respectively. Among them, 69 and 32 spots were significantly up- and downregulated, respectively, in expression level upon colonization. In M. membranacea colonized tissue, tripartite motif protein 2-like, microcompartments protein, carboxysome peptide shell peptide, trypsin precursor-like, transmembrane protein, two-component response regulator PilR, spermine/spermidine synthase, vanadium-dependent bromoperoxidase, peptide chain release factor 1, interaptin, 50S ribosomal protein L1P, plus agglutinin and leucine-rich repeat protein were upregulated, whereas protoporphyrinogen oxidase, PIH1 domain-containing protein 2, GTPase-activating protein alpha, cytoplasmic threonyl-tRNA synthetase, flavanone 3-hydroxylase, and eukaryotic translation initiation factor 3 proteins were downregulated. Moreover, DEAD/DEAH box helicase, glutamyl-tRNA reductase, and chaperone DnaJ protein were newly expressed in the colonized tissue. Most of the up- and downregulated proteins are known to be related to stress control, defense mechanisms, signal transduction, photosynthesis, protein metabolism, and the cytoskeleton.