Chromosomal heteromorphism in a Japanese population of Pectinatella gelatinosa and karyotypic comparison with some other phylactolaemate bryozoans

Five different karyotypes were present in germinating statoblasts obtained from a sampling of a predominately or exclusively asexually reproducing population of Pectinatella gelatinosa from Lake Tatara-numa, Japan. Karyotypes were consistent in having 18 chromosomes, a unique telocentric, a pair of minute metacentrics, and at least one prominently secondarily constricted element. In a number of cases, a sampling of statoblasts from a single large colony yielded more than one karyotype, perhaps because there had been fusion of smaller colonies with different karyotypes. Some individual statoblasts may have been chimeric, but this was not conclusively demonstrated. The possibility of asexually-maintained permanent chimerism in phylactolacmates involving karyotypically distinct ectodermal and peritoneal cell lines is discussed. Karyotypically, P. gelatinosa is more similar to Lophopodella carteri than to Pectinatella magnifica.     

Variation in reproductive characteristics of colonies of the freshwater bryozoan Cristatella mucedo

1. We studied relationships between different forms of reproduction and local variation in the reproductive state of colonies of a common freshwater bryozoan Cristatella mucedo Cuvier (Bryozoa: Phylactolaemata). Four sampling locations in central Finland, including both lotic and lentic habitats, were sampled by scuba diving. The traits studied were occurrence of sexual larvae, colony size, number of resting stages (statoblasts) and number of zooids. 2. While 76.9% of the sampled colonies carried statoblasts at the time of sampling, only 4.5% of the colonies were brooding sexual larvae. Most of the colonies were relatively small with a mean colony size of 16.6 mm. 3. In colonies brooding larvae, the number of statoblasts was positively correlated with the number of larvae. We did not detect a colony size threshold for sexual reproduction or formation of statoblasts. Colonies carrying statoblasts had a lower number of zooids per unit dry weight. 4. We found significant variation in reproductive traits of colonies among the sampling locations, and among lotic and lentic habitats. The observed phenotypic differences may reflect broadly distributed, phenotypically plastic clones. Differences in clonal composition of local populations cannot, however, be ruled out and factors that may provide clonal diversity are discussed.     

Plumatella mukaii,a new phylactolaemate bryozoan from Asia and South America

A new freshwater bryozoan species, Plumatella mukaii, is recognized from eastern Asia and western South America. Colonies and statoblasts both bear a resemblance to P. emarginata, and have often been confused with that species, especially in Japanese studies. Floatoblasts and sessoblasts are enclosed within a tough, wrinkled, membrane which resists removal by mechanical means. Floatoblasts are generally smaller than those of P. emarginata, but display unusually high variability in their overall dimensions. The species has been reported from both lentic and lotic habitats. In Asia, the range includes Japan, Korea, China, India and Indonesia. It has most recently also been found at several sites in Chile. The recognition of P. mukaii narrows the previously reported range of P. emarginata and invites a re-inspection of that species worldwide.     

Asexual propagation in the marine bryozoan Cupuladria exfragminis

Colonies of the free-living bryozoan Cupuladria exfragminis [Herrera-Cubilla, A., Dick, M.H., Sanner, J., Jackson, J.B.C., 2006. Neogene Cupuladriidae of Tropical America. I:. Taxonomy of Recent Cupuladria from opposite sides of the Isthmus of Panama. Journal of Paleontology. 80, 245-263.] from the Gulf of Panama are observed to separate into viable fragments without external force. The process, termed autofragmentation, involves the development of distinctive morphologies designed to assist in colony division. Culturing C. exfragminis shows that fragments that are a consequence of autofragmentation are significantly better able to regenerate than fragments originating from mechanical fragmentation. However, the relative importance of auto- versus mechanical fragmentation in natural populations remains unknown. Autofragmentation in C. exfragminis is found to be stimulated by cooling waters, and analysis of growth in natural populations demonstrates that colonies undergo periodic fragmentation coincident with lowered water temperatures during seasonal upwelling in the Gulf of Panama. These observations suggest that C. exfragminis uses the drop in temperature that occurs during upwelling as a cue to indicate times of increased food availability which may assist in the successful regeneration of fragments. These results are discussed in the context of the morphological, ecological and evolutionary significance of autofragmentation as a method of asexual propagation in cupuladriids.     

Experimental cultivation of the invasive freshwater bryozoan <Emphasis Type="Italic">Pectinatella magnifica</Emphasis>

The freshwater bryozoan Pectinatella magnifica (Leidy, 1851) is an invasive species in many countries all over the world. Although native to North America, it has been found in many countries of Europe and Asia. Pectinatella magnifica forms the largest colonial masses from all recently known bryozoan species. Culturing this organism in an aquarium has never been achieved for more than few days so far. Colonies from laboratory culture are important for various studies on its biology and life cycle of this species in experimental conditions. Young colonies successfully hatched from germinating statoblasts of P. magnifica in the laboratory and were maintained over eight weeks. Moreover, this was the first time when the compound colonies of this species were carried from its natural habitat to the laboratory, into a special aquarium system, and kept alive for more than three weeks. In both experiments the physicochemical parameters of the water (temperature, concentration of dissolved oxygen, electrolytic conductivity and pH) and changes in weight of compound colonies of P. magnifica in laboratory conditions were checked. The results found in this study are essential for understanding the invasiveness of this species and identifying methods for elimination of its ecological risks because these are closely resembling those of other invasive species.     

Shallow lake sediments provide evidence for metapopulation dynamics: a pilot study

The aim of this pilot study is to test the hypotheses that sediment cores can provide evidence for metapopulation dynamics and that these can be linked with site characteristics. We focus on temporal patterns of incidence and abundance of overwintering stages (statoblasts) produced by the freshwater bryozoan Cristatella mucedo, an organism characterised by a metapopulation ecology, in sediment cores retrieved from 18 UK lakes. Runs and goodness-of-fit tests provided evidence for population instability, periods of low abundance and absence, and of asynchrony—all signatures of metapopulation dynamics. Further hypothesis testing indicated that extinction risk is greater in more isolated sites and in sites of smaller size. Absence of statoblasts from the top sections of spatially separated, replicate cores provided independent evidence for extinction in one site. Our study demonstrates how the abundances of sedimentary-bound propagules may be analysed initially for metapopulation dynamics and subsequently how this may lead to working hypotheses regarding the drivers of such dynamics. The sediment archive represents a unique historical record whose potential for characterising metapopulation dynamics has previously been untapped but is broadly relevant for understanding the population biology of freshwater organisms.     

Vegetative reproduction in the octocoral Briareumasbestinum (Pallas)

Briareum asbestinum (Pallas), a common octocoral of Caribbean reefs, produces runner-like branches which are capable of attaching to the substratum and establishing new colonies. The subsequent death of the intervening runner leaves groups of genetically identical but physiologically distinct colonies. The origin of these colonies can be deduced by the presence or absence of runners. Analysis of colonies at Marsarkantupo in the San Blas Islands, Panama and at Carrie Bow Cay, Belize indicate that 23–56% and 18–67%, respectively, of the colonies at these sites originate from vegetative runners. In both areas the distribution of colonies of larval origin is not uniform. Colonies originating from larvae are patchily distributed within habitats and are over-represented in shallow habitats. The ability of B. asbestinum to reproduce vegetatively results in the spread and development of large populations of this species in many habitats where it might otherwise be rare.     

NOR-Chromosome morphology and evidence for rDNA selection in phylactolaemates

Silver-stained chromosome spreads from the phylactolaemate ectoprocts Fredericella indica, Fredericella browni, Plumatella repens, Pectinatella magnifica and Asajirella gelatinosa show that each of these species has a single pair of NORs. In the first four species each NOR is immediately adjacent to the centromere of a large metacentric chromosome. Giemsa-stained preparations from Cristatella mucedo show centromeric gapping in a similar large metacentric, indicating the same type of NOR-chromosome. In Asajirella gelatinosa the two NORs are on a pair of smaller chromosomes, and are not immediately adjacent to a centromere. A close NOR-centromere association would inhibit meiotic crossing over in the NOR region. Since in phylactolaemates reproduction is primarily asexual, often by formation of statoblasts, there is potential intraclonal selection for favorable ribosomal DNA (rDNA) mutations, including from simultaneous germination of otherwise genetically identical statoblasts within a limited area and competition between cell lines within statoblasts. Inhibition of meiotic crossing over within the NOR would maintain its integrity during periods when intraclonal selection would not be occurring. This suggests that a more rapid rate of rDNA evolution is possible in phylactolaemates than in most other organisms, and is consistent with a derivation of this group from the morphologically similar phoronids, despite phylogenetic interpretations of rDNA sequence data that suggest the two groups are not closely related.     

Annual net production and life span of floating leaves in Nymphaea tetragona Georgi: a comparison with other floating-leaved macrophytes

Fredericella sultana (Blumenbach, 1779) has long been considered one of the few freshwater bryozoan species with a truly cosmopolitan distribution. However, chromosome spreads from European material show 2n = 16 compared to 2n = 14 in North American specimens. In laboratory rearing the two forms are morphologically indistinguishable except for the surface texture of their statoblasts. Smooth statoblasts of European colonies match early illustrations of the species, while the densely pitted statoblasts of the North American form resemble those of F. indica Annandale 1909. On the basis of these observations we tentatively designate the North American F. sultana as F. indica. The only known American species with smooth statoblasts is F. australiensis Goddard 1909, in which the 2n = 16 karyotype is similar or identical to European F. sultana; however, despite this karyotypic similarity the two species retain their distinguishing morphology when reared together in the laboratory. Two enzymes from a single specimen of European F. sultana were electrophoretically distinct from the corresponding enzymes present in samples of both F. australiensis and North American F. sultana. Four phosphoglucose isomerase alleles were present in North American F. aultana from four geographically separated collection sites, although only one genotype for this locus was observed in material from any one site. These genetic findings are consistent with a relatively short-range dispersal potential in this species as compared to Plumatella species.     

An integrative approach to reveal speciation and species richness in the genus Diasporus (Amphibia: Anura: Eleutherodactylidae) in eastern Panama

We have applied an integrative taxonomic approach, including bioacoustics, ecology, morphology, and molecular genetics (barcoding and phylogeography), to explore species richness in the genus Diasporus in eastern Panama, from where only Diasporus quidditus (Lynch, 2001) was previously known. During fieldwork in eastern Panama in 2011 and 2012 we found six additional species, four of which we are describing here as new to science, plus two species that are new for this region. We have evaluated the presence of Diasporus diastema (Cope, 1875) in eastern Panama by comparing morphological, genetic, and bioacoustic characters of specimens from near the type locality in central Panama with specimens from eastern Panama. We further describe and compare male advertisement calls of most Diasporus species. The phylogeographic analysis suggests the allopatric speciation of Diasporus species in eastern Panama following the completion of the Panamanian isthmus in the middle Miocene. Subsequent geological events concur with the vicariant evolution of different lineages in situ, suggesting eastern Panama to be a centre of endemism for this group of frogs. We present an integrative analysis of the species from eastern Panama and include an identification key for all species of the genus.     

Stereoscan studies of phylactolaemate bryozoan statoblasts including a key to the statoblasts of the British and European Phylactolaemata

The stereoscan electron microscope has been used to study morphological features of the statoblasts of nine phylactolacmate species. Pores present in the walls of annulus chambers of floating statoblasts are fully described for the first time. The taxonomic significance of surface patterning is assessed, and a key to the species found in Britain and Europe is included.     

Interpretation of bryozoan microfossils in lacustrine sediment cores

Bryozoan statoblasts were isolated from the surficial sediments of 30 Florida lakes representing a gradient of trophic conditions. A prerequisite for lake selection was a good data base for water chemistry that was collected within the past 5–10 years. A novel technique of employing 210-Pb as a dilution tracer was used to estimate sedimentation rates for each lake. The net annual accumulation rate for bryozoan statoblasts was calculated for each lake and correlated with twelve physical, chemical, and biological variables. The results suggest that bryozoan distributions are strongly controlled by the extent of the littoral zone and phytoplankton biomass. It appears that bryozoan abundance in excessively weeded lakes may be limited by phytoplankton in spite of the richly developed habitat. Separation of the importance of food requirements from habitat requirements was not possible from this initial survey.     

Bryozoan populations reflect nutrient enrichment and productivity gradients in rivers

1. The hypothesis that nutrient enrichment will affect bryozoan abundance was tested using two complementary investigations; a field‐based method determining bryozoan abundance in 20 rivers of different nutrient concentrations by deploying statoblast (dormant propagule) traps and an experimental laboratory microcosm study measuring bryozoan growth and mortality. These two methods confirmed independently that increased nutrient concentrations in water promote increases in the biomass of freshwater bryozoans. 2. Statoblasts of the genus Plumatella were recorded in all rivers, regardless of nutrient concentrations, demonstrating that freshwater bryozoans are widespread. Concentrations of Plumatella statoblasts were high in rivers with high nutrient concentrations relative to those with low to moderate nutrient concentrations. Regression analyses indicated that phosphorus concentrations, in particular, significantly influenced statoblast concentrations. 3. Concentrations of Lophopus crystallinus statoblasts were also higher in sites characterised by high nutrient concentrations. Logistic regression analysis revealed that the presence of L. crystallinus statoblasts was significantly associated with decreasing altitude and increasing phosphorus concentrations. This apparently rare species was found in nine rivers (out of 20), seven of which were new sites for L. crystallinus. 4. Growth rates of Fredericella sultana in laboratory microcosms increased with increasing nutrient concentration and high mortality rates were associated with low nutrient concentrations. 5. Our results indicate that bryozoans respond to increasing nutrient concentrations by increased growth, resulting in higher biomasses in enriched waters. We also found that an important component of bryozoan diets can derive from food items lacking chlorophyll a. Finally, bryozoans may be used as independent proxies for inferring trophic conditions, a feature that may be especially valuable in reconstructing historical environments by assessing the abundance of statoblasts in sediment cores.     

Transoceanic ships as vectors for nonindigenous freshwater bryozoans

Aim The transport of organisms in ships’ ballast tanks is a dominant vector for aquatic invasions worldwide. Until recently, efforts to manage this vector have overlooked the potential transport of invertebrate resting stages in the residual waters and sediments within emptied ballast tanks, i.e. NOBOB (‘No Ballast On Board’) tanks. The resting stages (statoblasts) of freshwater bryozoans are often buoyant and locally abundant and thus can be taken up easily during ballasting operations. They are also resistant to extreme environmental conditions and can generate new colonies after being dormant for decades; as such, they would likely remain viable propagules after lengthy transport in ship ballast tanks. This study quantified the occurrence of freshwater bryozoan statoblasts in ballast tank sediments of transoceanic ships. Location North American Great Lakes. Methods We quantified the frequency of occurrence, abundance and diversity of bryozoans (as statoblasts) in residual sediment samples taken from 51 NOBOB tanks of 33 transoceanic ships visiting the Great Lakes from 2000 to 2002. Results Our study identified 11 species, comprising nearly 12% of the total number of freshwater bryozoans known worldwide. These include two exotic species unrecorded in the Great Lakes (Fredericella sultana and Lophopus crystallinus), an exotic species already established in the region (Lophopodella carteri) and three cosmopolitan species (Plumatella casmiana, P. fungosa and P. repens). Our estimates suggest that a ship with NOBOB tanks may carry up to 10⁶ statoblasts. Main conclusions The discovery of species unrecorded in the Great Lakes and the potentially large numbers of statoblasts being transported in ship ballast tanks indicate a significant risk of new species introductions. Furthermore, the presence of cosmopolitan species and an exotic species already established in the Great Lakes suggests the strong possibility of cryptic invasions via the introduction of exotic genotypes.     

Divergence and species discrimination in freshwater bryozoans (Bryozoa: Phylactolaemata)

We explored the suitability of nuclear and mitochondrial ribosomal markers [small subunit nuclear ribosomal RNA gene, large subunit nuclear ribosomal RNA gene, and a region spanning partial small mitochondrial ribosomal RNA subunit, four transfer RNA genes, and partial large mitochondrial ribosomal RNA subunit (referred to as rrnS‐rrnL)] for resolving patterns of diversification of 27 freshwater bryozoan species (class: Phylactolaemata) and evaluated the utility of statoblast ultrastructural features and molecular phylogenies for species discrimination in the Fredericellidae and Plumatellidae. Molecular data identified Plumatella fruticosa as distinct from the rest of the plumatellids, rendering the latter polyphyletic. rrnS‐rrnL was the most suitable marker for species discrimination and identified two undescribed species of Plumatella and at least two undescribed species of Fredericella. Lack of wide dispersal by fredericellid statoblasts may underlie the observed propensity for cryptic speciation and phylogeographical structure in Fredericella. Conversely, the strong dispersal potential of plumatellid statoblasts may mediate efficient gene flow between distant populations and explain the relatively low intraspecific divergence and lack of evidence for cryptic speciation. We show that species identification based on external features of statoblasts can be problematic in both genera, including for a putatively highly invasive, biofouling species, Plumatella vaihiriae, thereby highlighting the utility of rrnS‐rrnL sequences for species barcoding. © 2013 The Linnean Society of London     

Dormant stages in freshwater bryozoans--an adaptation to transcend environmental constraints

Freshwater invertebrates often disperse between discrete habitat patches via the production of dormant propagules. Being dispersed passively by animal vectors or wind, certain adaptations for exposures to terrestrial and aerial conditions like desiccation and freezing are required. In the present study, we investigate the mechanisms of survival and physiological adaptations due to desiccation and low temperatures in the statoblasts of two populations of the freshwater bryozoan Cristatella mucedo. Our results show that both sessoblasts and floatoblasts tolerate almost complete desiccation and subzero temperatures. Trehalose, a non-reducing disaccharide which has been related to desiccation tolerance, was detected by amperometric chromatography. However, due to the low concentrations found, it is unlikely that trehalose is playing a major part in desiccation tolerance of bryozoan statoblasts. Vitrification is assumed to be important in the survival of desiccation tolerant organisms. Differential scanning calorimetry revealed thermal transitions (T_g onset around 70 °C) in desiccated statoblasts, indicating that a vitreous matrix is present. During the exposure to subzero temperatures, freeze tolerance of statoblasts was confirmed by the detection of internal ice formation, which took place at a crystallisation temperature of between −6 °C and −12 °C.     

Cryptic invaders: nonindigenous and cryptogenic freshwater Bryozoa and Entoprocta in the St. Lawrence River

The distributions of most cosmopolitan invertebrate species are assumed to result from natural processes. Cryptic invertebrates with obscure biogeographic origins are often considered native by default, resulting in potentially severe underestimation of the extent of human-assisted invasions. This problem is exemplified by freshwater Bryozoa (Ectoprocta) and Entoprocta—small and widely distributed invertebrates commonly found in lakes and rivers. A benthic survey of a thermally modified section of the St. Lawrence River revealed the presence of two nonindigenous bryozoans: Carter’s moss animal Lophopodella carteri (Hyatt) and the crystal moss animal Lophopus crystallinus Pallas. Also discovered was a cryptogenic entoproct, the goblet worm Urnatella gracilis Leidy. These species were collected as statoblasts and (in the case of U. gracilis) colonial fragments downstream of the Gentilly-2 nuclear power plant at Bécancoeur, Quebec. Local densities of both U. gracilis and L. carteri increased by an order of magnitude at sites closer to the power plant. The occurrence of Lophopus crystallinus statoblasts in St. Lawrence River sediments is the first documented physical evidence of the species in North America. Contrary to the presumed natural Holarctic distribution of L. crystallinus, our literature review found that published historical records of L. crystallinus in the United States are erroneous or unsubstantiated. We propose that L. crystallinus is a western Palearctic species recently introduced to the St. Lawrence River, most likely as statoblasts discharged with ballast water from transoceanic ships.     

Venezuelan Equine Encephalitis in Panama: Fatal Endemic Disease and Genetic Diversity of Etiologic Viral Strains

Venezuelan equine encephalitis (VEE) is a reemerging, mosquito-borne viral disease of the neotropics that is severely debilitating and sometimes fatal to humans. Periodic epidemics mediated by equine amplification have been recognized since the 1920s, but interepidemic disease is rarely recognized. We report here clinical findings and genetic characterization of 42 cases of endemic VEE detected in Panama from 1961–2004. Recent clusters of cases occurred in Darien (eastern Panama) and Panama provinces (central Panama) near rainforest and swamp habitats. Patients ranged from 10 months to 48 years of age, and the more severe cases with neurological complications, including one fatal infection, were observed in children. The VEE virus strains isolated from these cases all belonged to an enzootic, subtype ID lineage known to circulate among sylvatic vectors and rodent reservoir hosts in Panama and Peru. These findings underscore endemic VEE as an important but usually neglected arboviral disease of Latin America.