Unique and species-specific microbial communities in Oscarella lobularis and other Mediterranean Oscarella species (Porifera: Homoscleromorpha)

Homoscleromorph sponges such as Oscarella spp. are characterized by unique morphological features, and Homoscleromorpha were therefore recently proposed as the fourth class of sponges. The microbiology of these sponges was mainly studied by electron microscopy while molecular studies are scarce. The aim of this study was to characterize the bacteria in Oscarella sponges using molecular tools. Denaturing gradient gel electrophoresis revealed distinct bacterial profiles in five Oscarella species and several color morphs of Oscarella lobularis. These profiles are characteristic of low microbial abundance (LMA) sponges. This was further confirmed by analysis of a 16S rRNA clone library from O. lobularis that yielded a low phylum-level diversity with dominance of Alphaproteobacteria. Bacterial communities in O. lobularis were very similar among different individuals (collected at the same site and time), five different color morphs, and specimens from different depths and locations, indicating a species-specific association. These results allow novel insights into the microbiology of the first known LMA sponge genus within the new class Homoscleromorpha.     

Asexual reproduction in homoscleromorph sponges (Porifera; Homoscleromorpha)

Asexual reproduction by external budding in Homoscleromorpha is reported for the first time. Two Mediterranean sponge species were studied, Oscarella lobularis and O. tuberculata. Buds are formed in the marginal basal part of sponge. Budding takes from 1 to 4 days and is defined in three budding stages. First, small irregular protuberances, consisting of external parental tissue, are formed. Second, they elongate and acquire more regular, nipple-like shape. These protuberances are tube like, their internal cavity derived from parental exhalant canal. The wall consists of three layers: (a) external layer is flagellated exopinacoderm, (b) internal one is flagellated endopinacoderm and (c) intermediate one is a thin layer of mesohyl. Third, a spherical bud with a large central cavity is formed. During budding, we did not observe cell proliferation or transdifferentiation either in budding zone or in any special mitotically active region. The bud attached to the substrate is similar to the rhagon developing after larva metamorphosis, it has a syconoid organization. Morphogenetically, budding in Oscarella differes from that in other sponges. Occurring by epithelial morphogenesis, it is similar to morphallaxis during regeneration. The presence in Homoscleromorpha of an epithelial morphogenesis is unique among sponges. This feature is shared by Homoscleromorpha and Eumetazoa.     

Bacterial symbionts as an additional cytological marker for identification of sponges without a skeleton

Symbiotic bacteria from six Oscarella species (adults and embryos) collected in the Mediterranean Sea (O. lobularis, O. tuberculata, O. imperialis, O. microlobata, O. viridis) and the Sea of Japan (O. malakhovi) were investigated by scanning electron microscopy and transmission electron microscopy. In most cases, symbionts are rather numerous. Each sponge species has a definite set of bacterial morphological types. All bacteria are extracellular. Symbionts occupy the mesohyl of adult sponges or intercellular space in embryos and are often in contact with mesohylar filaments or cells. Bacteria of some morphotypes have characteristic blebs. Most symbionts are gram-negative, and two types of bacteria have traits of Archaea and one type of bacteria is similar to Planctomycetes. Data on morphology of bacterial symbionts can be a good additional character for identification of Oscarella species, which have no skeleton.     

Biochemical genetic divergence and systematics in sponges of the genera Corticium and Oscarella (Demospongiae: Homoscleromorpha) in the Mediterranean Sea

The sponge sub-class Homoscleromorpha is generally considered to include just two families, the Oscarellidae (without spicules) and the Plakinidae (with simple spicules). In May 1990, an unusual sponge was found deep inside a submarine cave in the western Mediterranean Sea. On the basis of externally visible characters this sponge appeared indistinguishable from the common plakinid species Corticium candelabrum Schmidt, 1862. However, on closer examination in the laboratory the new sponge proved to be devoid of spicules. Therefore, despite great morphological similarities to C. candelabrum, the new sponge should, by taxonomic convention, have been placed in the Oscarellidae. On the basis of other criteria, the similarities to C. candelabrum were great and the new sponge was at first considered to be conspecific. Thus, the taxonomic position of the new sponge and its relationship to C. candelabrum are highly confusing. It could be an aspiculate morph of C. candelabrum, or a new and undescribed related species or, lacking spicules, it could justifiably be placed in a different family (Oscarellidae). The relationship of the new sponge to C. candelabrum and also to two species of Oscarella (Oscarellidae) was assessed by the use of enzyme electrophoresis to estimate genetic divergence between species. It was found that the new sponge was reproductively isolated from sympatric C. candelabrum, with 6 of 16 loci proving diagnostic. Thus it is clear that the new sponge belongs to a different biological species. Surprisingly it was also found that, although this new species was fairly closely related to C. candelabrum (level of genetic identity, I0.47), the two Oscarella species were similarly closely related to C. candelabrum (I0.31 to 0.41) and rather less closely to the new species (I0.17 to 0.28). Indeed from genetic identity estimates, O. tuberculata is more closely related to C. candelabrum than it is to O. lobularis. It is concluded that all homoscleromorph sponges should be placed in the single family Plakinidae.     

Variability in reproductive output across a water quality gradient for a tropical marine sponge

To establish a complete understanding of reproductive variability, larval supply and ultimately population demographics of a species it is important to determine reproduction across a broad spectrum of environmental conditions. This study quantified sexual reproduction of the brooding, gonochoristic sponge Rhopaloeides odorabile from populations across the shelf reefs of the central Great Barrier Reef (GBR). Histological sections of reproductive sponges collected at increasing distances from the coast were used to determine if numbers of reproductive sponges, reproductive output (using a reproductive output index), size at sexual maturity, and sex ratios varied according to their location (distance) from the coastline and therefore from influences of terrigenous/riverine discharge. Significantly higher proportions of reproductive sponges occurred with increasing distance from the coast. The proportion of all reproductive sponges (both male and female) on offshore reefs ranged from 77 to 90%, during November and December, the peak reproductive months of this sponge, compared to 47 to 50% for sponges occurring on coastal reefs. Levels of female reproduction increased with increasing distance from the coastline on two levels. First, oocytes from offshore sponges were significantly larger than oocytes from coastal sponges. Second, sponges from offshore reefs showed a reproductive index (proportions of oocytes, embryos and larvae mm⁻²) approximately 15 times higher than coastal reef sponges. Therefore, both numbers of oocytes, embryos and larvae in conjunction with larger oocytes contribute to a higher reproductive output index for offshore sponges. The production of spermatic cysts in males was consistent across the GBR. Sex ratios for coastal reef sponges showed a male bias while offshore sponges showed approximate equal sex ratios. The effect of terrigenous riverine input from coastal fluvial plains to the inner GBR is well established and is likely to contribute to the lower levels of reproduction associated with female sponges inhabiting coastal reefs of the central GBR.     

Wide-spread genetic variability and the paradox of effective population size in the gag,Mycteroperca microlepis,along the West Florida Shelf

Wide-ranging marine species are often described as having a low effective population size (N _e) to census size (N) ratio. This genetic phenomenon is typically attributed to large variation among individuals in reproductive success because of the high mortality rates and unpredictable environments associated with larval dispersal. In this study, we examined patterns of genetic variation in gag (Mycteroperca microlepis) on the West Florida Shelf across year classes of post-settlement juveniles and spawning adults. With no significant genetic differentiation among year classes despite varying recruitment dynamics, little evidence for chaotic genetic patchiness, and no truncation of adult genetic diversity in subsequent juvenile cohorts, there was little support for large variation among individual in reproductive success contributing to a low N _e/N ratio. In fact, the consistent lack of significant differences in annual recruitment classes indicated that reproductive success among individuals was resistant to skewing. Among the various evolutionary forces that may be affecting N _e, changes to demography due to fishing pressure are posited as a likely mechanism affecting current levels of genetic variation.     

Reproductive strategies of Mycalecontarenii (Porifera: Demospongiae)

The sexual and asexual phases of the reproductive cycle of the sponge Mycalecontarenii (Martens, 1824) were studied from samples collected over a period of 2 years (June 1994 to May 1996) in a Mediterranean coastal basin (Porto Cesareo, southwestern Apulia). The species is viviparous; year round it shows a discontinuous oocyte production. No males were found, possibly owing to the very short period of spermatogenesis. M.␣contarenii produces asexual buds during autumn and winter, and this process seems to be related to changes in water temperature. Even though, at present, we cannot evaluate the incidence of larval recruitment, we postulate that asexual reproduction in M.contarenii plays a crucial role in maintaining the sponge population. Received: 8 July 1997 / Accepted: 5 November 1997     

Host specificity in sponge-encrusting zoanthidea (Anthozoa: Zoantharia) of Barbados,West Indies

Six species of common Caribbean Zoanthidea, Parazoanthus swiftii, P. parasiticus, P. catenularis, P. puertoricense, Epizoanthus cutressi, and Epizoanthus sp., are virtually restricted to living on surfaces of reef-dwelling sponges. Quantitative surveys on Barbados reefs indicate that substrate specificity is relatively high among these zoanthids with three restricted to a single primary host sponge species and three restricted to three closely related sponges. One species, P. swiftii, exhibits a broad range of acceptable secondary substrates, due to its unique ability to execute migrational spread in the adult polyp stage. Variations in substrate specificity have been noted between island populations within the extensive Caribbean range and appear to be due to different species compositions of local sponge communities and slight differences in zoanthid larval settling specificities.     

Effects of El Niño-Southern oscillation on the population dynamics of the tropical bivalve Donax dentifer from Málaga bay, Colombian Pacific

The population dynamics of a Donax dentifer (Hanley, 1843) population from Málaga bay, Colombia, was studied during two periods (August 1997–July 1998 and November 1999–February 2002) in order to investigate the effects of El Niño (EN) 1997/1998 and La Niña (LN) 1998/2000. The EN–LN cycle was strongly associated to an interannual precipitation and salinity variability in Málaga bay. Additionally, these factors were highly correlated with the reproductive cycle. Results indicate that EN had negative effects on the reproductive cycle, leading to weak, abnormal spawning events. In contrast, good spawning events were recorded during LN and post-LN. Based on these findings, an opportunistic reproductive strategy is proposed for this species. Overall growth performance (P) was higher during LN (P=4.41) than during EN and post-LN (P=4.20, P=4.28, respectively). These results indicate that D. dentifer has a higher overall growth performance compared to several tropical species reported in the literature. Total mortality rate of small individuals was higher during LN whereas that of large individuals was higher during EN. These results are best explained by recruitment variability and spatial differences between recruits and adults. Individual production and productivity were higher during LN, although annual biomass was relatively low. This, together with the results regarding growth and reproduction, suggests that food availability was higher during LN, thus positive effects under LN may be concluded. In contrast, EN seems to have negative effects on growth, reproduction and somatic production for this surf clam.     

Reproduction of sympatric populations ofHeliocidaris erythrogramma andH. tuberculata (Echinoidea) in New South Wales

Reproduction ofHeliocidaris erythrogramma (Valenciennes) andH. tuberculata (Lamarck) was compared through examination of oogenesis, spermatogenesis and monthly measurement of the gonad index. These species occur sympatrically in the Sydney region. Their reproduction was examined at two sites near Botany Bay, New South Wales, Australia, from February 1989 through January 1990.H. erythrogramma produces buoyant, 450µm-diam eggs and the sperm have a head region 10µm in length. By contrast,H. tuberculata produces negatively-buoyant, 95µm-diam eggs and the sperm have a head region 4µm in length. Histochemical examination of the gonads revealed that periodic acid Schiff-positive (PAS +) material stored in the nutritive phagocytes appears to support vitellogenesis in both species. InH. tuberculata this material is utilized in the formation of PAS + yolk oligolecithal eggs, whereas inH. erythrogramma the PAS + material appears to be converted to lipid yolk in macrolecithal eggs.H. erythrogramma had a seasonal reproductive pattern with a 3 mo summer spawning period, whereas both populations ofH. tuberculata had a 9 mo breeding period characterized by the continual presence of nutrient reserves and vitellogenic oocytes which rapidly replaced spawned ova. Spawning ceased only for 3 mo over the summer. Due to the 9 mo spawning ofH. tuberculata it is not clear what factors serve to cue reproduction in this species.     

Influence of sponges on invertebrate recruitment: A field test of allelopathy

We manipulated live sponges in Belize, Central America, Big Pine Key, Florida (USA), and Indian River lagoon, Florida (USA) in summer/autumn, 1988. At each location, live sponges of three species were placed within 0.5 cm of ceramic tiles. Tiles with synthetic sponges positioned in the same manner and tiles with no sponges served as controls. Of 26 recruiting species analyzed, only one (Sponge sp. 6 — Indian River) was inhibited by living sponges. Four species (Perophora regina — Belize;Aiptasia pallida — Big Pine Key; andCrassostrea virginica andAscidia nigra — Indian River) recruited in greater numbers in the presence of sponges, suggesting that some larvae may be attracted rather than repelled by sponge allelochemicals. Allelopathic effects were less important than small-scale flow effects and patchy larval supply in determining recruitment patterns on surfaces adjacent to sponges.     

Sexual reproduction and settlement of the coral reef spongeChalinula sp. from the Red Sea

Characteristics of the sexual reproduction and larval settlement of the haplosclerid spongeChalinula sp., which inhabits the shallow waters (1 to 6 m) of Eilat, Red Sea, were investigated from September 1985 through to November 1987. This species was found to be a simultaneous hermaphroditic brooder, hence gonochorism is not the rule in the order Haplosclerida. Brooding always takes place in special brooding chambers. While the oocytes in the brooding chambers are among the largest known in sponges (355±37µm), the spermatic cysts distributed in the choanosome are among the smallest known for this phylum (average 26±7µm).Chalinula sp. breeds throughout the year and in experiments most larvae (74%) settled within 1 to 8 h post-release, generally within 4.5 h. Metamorphosis from larval shape to a sessile sponge lasts 1 to 6 h. Thus, larvae had a short swimming period, settled fast, and metamorphosed rapidly (within 1 to 6 h). The large size of the larvae may contribute to their ability to rapidly reorganize their body shape into that of a sessile sponge. In addition, the existence of already differentiated choanocyte chambers in the larvae, facilitates fast construction of the water filtration system in the newly settled sponges. The reproductive and larval characteristics ofChalinula sp. enable the larvae to settle on any vacant space in the reef, which may explain its abundance in the Red Sea.     

Seeding phenology influences wood mouse seed choices: the overlooked role of timing in the foraging decisions by seed-dispersing rodents

Scatter-hoarding rodents influence the population dynamics of plants by acting as seed predators and dispersers. Therefore, rodent foraging preferences for certain seed traits (species, size, condition) have been extensively studied. However, to what extent these preferences are fixed or they track the temporal changes on seed characteristics due to phenological differences has been seldom explored. We studied the temporal variability in seed preferences by wood mouse (Apodemus sylvaticus), according to phenological changes in seed characteristics of two co-occurring oaks (Quercus ilex and Quercus pubescens). The phenology of acorn abundance and the acorn predation/dispersal patterns by rodents were monitored over an entire seeding season. Results revealed temporal changes in rodent preferences for acorns of the two oaks, matching their different seeding phenology (earlier in Q. pubescens and later in Q. ilex). On the other hand, whatever the species considered, rodents preferred larger and sound acorns along the entire season, although the dispersal of infested ones increased slightly during the peaks of acorn drop. The observed influence of seeding phenology on seed choices by rodents warns about inferring definite conclusions regarding their foraging behavior when arising from short-term experiments. Indeed, this study reveals that foraging preferences may be highly dynamic and context-dependent for some seed traits (e.g., species and condition), rather than fixed behavioral patterns. Plasticity in rodent foraging choices may allow them to successfully exploit different oaks with uncoupled seeding phenologies, while potentially favoring their coexistence.     

Studies on the reproductive cycles of the calcareous sponges Clathrina coriacea and C. blanca

The reproductive cycles of two closely related calcareous sponges, Clathrina coriacea (Montagu, 1818) and C. blanca (Miklucho-Maclay, 1868), were studied to determine whether they were reproductively isolated. Populations of both species were sampled at Santa Catalina Island, California, USA, for 2.5 years. The reproductive period is from July to October in C. coriacea, and from April to August in C. blanca. Seawater temperature and habitat influence reproduction in both species. Fragmentation occurs in C. coriacea in the summer, while asexual reproduction by means of budding is seen in C. blanca throughout the year. The results of the study confirm that the two sponges are separate species.     

Variable effects of symbiotic snapping shrimps on their sponge hosts

Mutualistic relationships are ubiquitous in tropical coral reefs, but the costs and benefits to partner species are often poorly known. In Caribbean coral reefs, several species of snapping shrimp (Synalpheus spp.) dwell exclusively in marine sponges, which serve as both habitat and food source. A paired experimental design was used to examine the effects of Synalpheus occupancy on predation, morphology, and growth of their sponge host Lissodendoryx colombiensis in Bocas del Toro, Panama (9.351°N, 82.258°W) in June 2009. Shrimp occupancy significantly decreased consumption of sponges by a predatory sea star (Oreaster reticulatus) and also affected sponge morphology; sponges grown without shrimps decreased in canal size, in both the laboratory and the field. Shrimp occupancy had more ambiguous effects on sponge growth. In laboratory experiments, shrimp occupancy benefited sponge growth, although all sponges experienced overall decreases in mass. In field experiments, there were no significant differences in growth between occupied and empty sponges. However, the benefits of shrimp occupancy on sponge growth were negatively correlated with overall increases in sponge size; sponges that decreased in mass during the experiment benefited more from shrimp occupancy than sponges that increased in mass. These costs and benefits suggest that Synalpheus has variable effects on sponges: positive effects on sponges in the presence of predators, and/or when sponges are decreasing in mass (e.g., during periods of physical stress), but a negative effect on sponges during periods of active sponge growth.     

Meso-scale hydrodynamic and reproductive asynchrony affects the source–sink metapopulation structure of the coastal polychaete Pectinaria koreni

The polychaete Pectinaria koreni exhibits a complex life cycle characterized by non-overlapping generations and widespread larval dispersal. To explore how “local” metapopulation genetic structure varies spatially and temporally during population turnover, we combined observations on demography, larval dispersal through hydrodynamic modelling and population genetics of successive age cohorts in the Baie de Seine (eastern English Channel, France). Mature adults (March), newly settled (July) and later-stage juveniles (September) were sampled in 2003 on the edge and in the main demes of the metapopulation. Demes displayed an asynchronous dynamics due to variations in habitat quality affecting reproductive timing (e.g. three distinct spawning events observed) and in local larval supply linked to temporal fluctuations of hydrodynamism. Two-source populations were identified among dense areas with the greatest larval retention and self-recruitment rates: one with a single recruitment event, stable temporal genetic variation and a strong spatial genetic re-homogenization during turnover, and the other with two recruitment events and significant allele frequency changes over time. Sink habitats displayed single recruitment event and experienced strong inter-generational (juveniles vs adults) genetic changes due to genetic drift associated with strong winter mortalities. Altogether, results suggested that adult spawning asynchrony and sweepstakes reproductive success, together with genetic drift, played a greater role than hydrodynamics itself in determining effective recruitment rates at some sites and generating genetic patchiness.     

Reproduction,recruitment and fragmentation in nine sympatric species of the coral genus Acropora

Multispecies assemblages of the coral genus Acropora occur commonly throughout the Indo-Pacific Ocean. Nine species from such an assemblage comprising 41 species of Acropora, at Big Broadhurst Reef on the Great Barrier Reef, were studied during 1981–1983. Similarities and differences in reproductive modes and timing, oocyte dimensions and fecundity, recruitment by larvae and by fragments, and mortality were recorded. All species had an annual gametogenic cycle, were simultaneous hermaphrodites, and had the same arrangement of gonads in polyps. In six species, most colonies released gametes on the same night of the year, in early summer, during a mass spawning event involving many coral genera. A seventh species had colonies spawning at this as well as other times of the year. Another species spawned in late summer, and gametes were not observed to mature in the last species. Eggs were very large (601 to 728 m geometric mean diameter) and fecundity of polyps low, compared with other corals; no reduction in oocyte numbers occurred during oogenesis. Reef-flat species had slightly bigger and fewer eggs than reef-slope species. All species recruited by larvae, but four also multiplied by fragmentation, either year-round or during occasional rough weather. Yearround fragmenters had few larval recruits; non-fragmenters had many, and a rough-weather fragmenter had an intermediate number of larval recruits. It was concluded that larval recruitment largely determined species composition, and that reduced larval recruitment was responsible for sparse distribution of fragmenting species. Subsequent mortality in some species and increase by fragmentation in others probably determined relative abundances.     

Dispersal and use of sponges and ascidians as camouflage by Cryptodromia hilgendorfi (Brachyura: Dromiacea)

From May 1977 to February 1979, the use of sponges and ascidians by Cryptodromia hilgendorfi was studied in Moreton Bay, Queensland, Australia. The aim was to investigate patterns of seasonal use, cap making behaviour, cap turnover, the effect of intraspecific interactions on cap life and the effect of movement of crabs between hosts on background matching. C. hilgendorfi uses 12 (of 16 available) species of sponge and 3 species of ascidians to construct caps, which are carried by the crabs using their last two pairs of legs. Cap area increases non-linearly with crab size, and caps are normally two to three times as large as the crabs. Cap making behaviour is described. It occurs during intermoult periods, with females making most of their caps at night. Caps decrease in size with time, but conceal the crabs which commonly occupy exposed sites on sponges. Cap life is independent of crab size, differs between different cap species and is influenced by the presence of other crabs who can dislodge caps through aggressive behaviour. Caps are made from the sponge Suberites carnosus more often than from other available sponges. S. carnosus caps also decay less rapidly than caps made from other sponges. Use of sponge and ascidian species varies seasonally, with Halichondria sp. and S. carnosus being used in all months. C. hilgendorfi exhibits a preference for certain sponges. The majority of crabs carried caps which matched their host sponge or ascidian, but mis-matches varied seasonally with a winter peak following the breeding season. Young C. hilgendorfi settle only on S. carnosus sponges and disperse from this host to other species in the environment. Males and females differ in their rate of discovery of new hosts. Males, despite their greater mobility, find new hosts slower than females. It is hypothesized that males occupy “home ranges” which females do not. Crabs frequently move between sponges, mostly at night. Sponges and ascidian species grow in intimate association with each other, and sponge crabs act a selective asexual propagation mechanism. Depending upon the nature of the interactions between sponge and ascidian species (co-operative or competitive) and whether competitive hierarchies or networks are involved, the sponge crabs may have either stabilizing or destabilizing effects on the sponge community.     

Biological patterns and near-bottom population characteristics of two pasiphaeid decapod crustacean species, Pasiphaea sivado and P. multidentata, in the north-western Mediterranean Sea

Biological aspects of the only two epi-/mesopelagic pasiphaeid species distributed along the continental marginof the north-western Mediterranean Sea were studied over the period 1991-1994. The annual reproductive cycle, reproductive output, sex and size distributions by depth (near-bottom distribution), and growth were analysed using 4156 specimens of Pasiphaea sivado (Risso, 1816) and 5491 specimens of P. multidentata Esmark, 1866. The reproductive cycle in the shallower-dwelling species, P. sivado, was nearly continuous, in contrast to the reproductive cycle in P. multidentata, which was markedly seasonal in nature. Both species exhibited similar size and population structure patterns with depth, with individual size increasing along the bottom depth gradient. The shallower-dwelling species had a significantly higher reproductive output level, in terms of the relative number of eggs, than the deeper-dwelling species. Biological trends for each of the species have been compared. The comparative results for these two congeneric species revealed that the biological parameters analysed were closely linked to their population structure. The slight differences in the depth range inhabited by each species have been considered the main environmental factor affecting the life histories of these two species. The data presented supported the hypothesis that depth exerted an important influence on the biological patterns of deep-water species, with the seasonality of reproductive processes increasing in deeper-dwelling species.