Description of a new epibiotic relationship (Suctorian–Copepoda) in NE Atlantic waters: from morphological to phylogenetic analyses

Paraeuchaeta hebes is one of the most important carnivorous copepods in the coastal upwelling system off Galician waters (Ría de Vigo, NE Atlantic). A suctorian epibiont of the genus Pelagacineta was found attached to the surface of these copepods. The abundance and distribution on the copepod surface were analysed, taking into account the sex of the crustacean, revealing some preference for females and also a different attachment point in both sexes. The morphological study allowed us to identify a new species of this Suctoria epibiont as Pelagacineta hebensis. Moreover, the 18S rRNA gene was partially sequenced to inspect the phylogenetic position of Pelagacineta hebensis within the subclass Phyllopharyngea. The maximum‐likelihood (ML) tree obtained was consistent with the morphological and with previous molecular studies and showed that P. hebensis belongs to the order Endogenina, as a sister clade of the few taxa sequenced within this order. Including new genetic data to the Endogenina will allow building new hypothesis about the evolution of the most derived clade of suctorians.     

A survey of the epibiota of Eretmochelys imbricata (Testudines: Cheloniidae) of Mona Island, Puerto Rico

Epibiotic organisms inhabiting non-nesting hawksbill sea turtles, Eretmochelys imbricata (Linnaeus, 1766), are described from Mona and Monito Islands, Puerto Rico. Epibiont samples from 105 turtles of shallow (< 40 m) water foraging habitats were collected and identified to the lowest possible taxon. This epibiotic assemblage consisting of at least 4 algal functional groups and 12 animal phyla represents the greatest phylogenetic diversity for marine turtle epibiota. Six groups are considered new reports for marine turtles. Most epibiont colonization was found on posterior marginal scutes and under overlapping scutes. Ecological attributes of epibiota and their symbiosis with E. imbricata provide a tool to understand basi and epibiont populations.     

Prevalence of Colacium vesiculosum (Colaciales: Euglenophyceae) on planktonic crustaceans in a subtropical shallow lake of Argentina

Colacium vesiculosum (Euglenophyceae) is an epibiont common on planktonic microcrustaceans of continental waters. The interaction between epibionts and substrate organisms is not very well known, particularly in subtropical environments of South America. In the present work, we analyzed the prevalence, density, biomass and attachment sites of C. vesiculosum on planktonic microcrustaceans from Paiva Lake, a subtropical lake of Argentina. With the aim to evaluate whether epibionts affect the filtering rates of Notodiaptomus spiniger, the dominant planktonic crustacean, we carried out bioassays using phytoplankton < 53 microm. Crustaceans were sampled using a PVC tube (1.2m long and 10cm in diameter), filtering 50L of water through a 53 microm-mesh. Microcrustaceans were counted in Bogorov chambers under a stereoscopic microscope. The infested organisms were separated and observed with a photonic microscope to determine density and biovolume of epibionts, by analyzing their distribution on the exoskeleton. The prevalence of C. vesiculosum was higher in adult crustaceans than in their larvae and juveniles. The most infested group was that of calanoid copepods, related to their high density. The attachment sites on the exoskeleton were found to be the portions of the body which have a higher probability of encounter with epibionts during locomotion and feeding, i.e., antennae and thoracic legs in copepods, and thoracic legs and postabdomen in cladocerans. The similar values found in the filtering rate of infested and uninfested individuals of N. spiniger and the constant prevalence (< 40%) of epibiont algae, suggest that C. vesiculosum does not condition the life of planktonic crustaceans of Paiva Lake.     

The complex life-cycle of a polymorphic prokaryote epibiont of the photosynthetic bacterium Chromatium weissei

In natural populations of the anaerobic phototrophic bacterium Chromatium weissei, many cells support a prokaryotic epibiont. This epibiont appears in several forms, all from the life cycle of a single species. A typical epibiont consists of one to five flattened coccoid cells stacked one above the other, perpendicular to the C. weissei surface. The cells at the proximal and distal ends of the stack are 0.6 m in diameter and 0.8 m in length; mid-stack cells are slightly shorter. A typical three or four cell stack is 2 m in length. Small mesosome-like inclusions in the distal cell are involved in the development of droplet shaped cells which are released from the end of each stack. These specialised droplet cells probably transfer to new hosts when C. weissei cells collide, thereafter developing into new epibiont stacks. It is likely that the epibiont grows heterotrophically using the substantial production of dissolved organic carbon within the dense plates of photosynthesising C. weissei which develop naturally. Thus the epibiont uses its unusual method of growth and dispersion to maintain position in the microbial plate upon which it depends.     

Effects of hydrology on zooplankton communities in high-mountain ponds, Mount Rainier National Park, USA

Ten high-mountain ponds in Mount Rainier National Park, WashingtonState, were studied from ice-out in June through September1992to investigate the influences of fluctuating pond volumes onzooplankton communities. All of the ponds were at maximum volumeimmediately after ice-out. The temporary pond with the shortestwet phase was inhabited by rotifer taxa with short generationtimes and a crustacean taxon with the ability to encyst as drought-resistantresting bodies at immature stages of development. Dominant zooplanktontaxa in three other temporary ponds and six permanent pondswere similar. Rotifer densities typically were lower in temporaryponds relative to those in permanent ponds, although Brachionusurceolaris was abundant shortly before the temporary ponds dried.Large volume loss was associated with large declines in totalabundances of crustacean populations. Daphnia rosea was notpresent in temporary ponds following fall recharge. In deep-permanentponds, copepods had slower developmental rates, smaller temporalchanges in total abundances of crustacean populations and twoadditional large-bodied crustacean taxa were present relativeto the characteristics of crustacean communities in shallow-permanentponds. Owing to their small sizes and sensitivity to environmentalchange, collectively ponds such as these may provide an earlysignal of long-term climate change in aquatic systems.     

Spatial and temporal patterns in the occurrence of peritrich ciliates as epibionts on calanoid copepods in the Chesapeake Bay, USA

We investigated temporal and spatial patterns of distribution in two peritrich ciliates (i.e. Zoothamnium intermedium and Epistylis sp.) living as epibionts on calanoid copepods (i.e. Acartia tonsa and Eurytemora affinis) in Chesapeake Bay. Net tow samples collected along the main axis of the Bay were analyzed to estimate the occurrence of epibionts on copepods and to explore relationships among infestation prevalence, host abundance, and environmental variables. Zoothamnium intermedium and Epistylis sp. colonized populations of A. tonsa during spring and summer months, while only Z. intermedium colonized E. affinis during spring. Occurrence of epibionts on copepods showed high interannual variation, marked seasonality, and geographic heterogeneity. Extensive statistical analyses rejected simple scenarios of interactions between epibiosis, environmental variables, and host density, suggesting a more complex dynamics for the system. Analyses of epibiont colonies and zooids per host area (i.e. the sum of width and length of the body including antennae and swimming legs calculated assuming a cylindrical shape) were also performed. Overall, epibiont infestation prevalence (i.e. colonies/host area) and load (i.e. zooids/host area) were higher on copepodites than on adults for both host species, suggesting a preferential attachment to juveniles, or a higher predation pressure on adult stages. Infestation density and loads of both epibiont species were higher on the cephalothorax and abdomen of A. tonsa and E. affinis in comparison to the antennae and swimming legs, suggesting that ciliates can more easily colonize less active parts of the host.     

Biodiversity and distribution of epibiontic communities on Caridina ensifera (Crustacea,Decapoda, Atyidae) from Lake Poso: comparison with another ancient lake system of Sulawesi (Indonesia)

Fernandez‐Leborans, G. and von Rintelen, K. 2010. Biodiversity and distribution of epibiontic communities on Caridina ensifera (Crustacea, Decapoda, Atyidae) from Lake Poso: comparison with another ancient lake system of Sulawesi (Indonesia). — Acta Zoologica (Stockholm) 91 : 163–175 The epibiont communities of the shrimp Caridina ensifera, endemic to Lake Poso (Sulawesi, Indonesia), were analysed. Most of the epibiont species were ciliated protozoa belonging to three suctorian genera (Acineta, Podophrya and Spelaeophrya), three peritrich genera (Zoothamnium, Vorticella and Cothurnia), and a haptorid genus (Amphileptus). There was also a rotifer epibiont of the genus Embata. Epibionts were identified to species level. There were 14 to 1114 epibionts per shrimp. The distribution of the epibiont species on the surface of the basibiont was recorded, calculating the number on the different colonized individuals of C. ensifera. The most abundant species, Zoothamnium intermedium and Acineta sulawesiensis, were also the most widely distributed. There was a significant difference between the spatial distributions of the different epibiont species. The analysis of the number of the epibiont species throughout the anteroposterior axis of the shrimp showed a gradient from the anterior to the posterior end of the body. Data from Lake Poso were compared with those of the Malili lake system (Sulawesi), obtained from its endemic shrimp, Caridina lanceolata. Lake Poso had the highest mean diversity, while Lake Mahalona showed the highest maximum diversity. All lakes were correlated with respect to the mean number of epibionts on the anatomical units of the shrimp, which showed a similar general distribution. The distributions of the different epibiont species were compared between the lakes. The possible adaptations of the epibionts as well as the colonization patterns were discussed. From the statistical results and the analysis of the distributions, we propose that in these communities epibiont species have a pattern of colonization in which they follow a behaviour as a whole; each species has a differential distribution, with the species occupying the available substratum with the particular requirements of each functional group, but there is a trend towards maintaining an equilibrium among species and groups, compensating for diversity and number of individuals. In all lakes there was an epibiont distribution model comprising the maintenance of an anteroposterior axis gradient, which was supported by the fluctuation in diversity and number of individuals of the different functional groups of epibiont species. The functional role of the different groups of species seems to tend towards sustainability with little global variation among the lakes.     

Transmission and scanning electron microscopic studies of crustacean shell disease in fish lice of the genus Argulus (Crustacea: Branchiura)

Juvenile and adult specimens of the branchiuran crustacean parasite, Argulus foliaceus , have been found to exhibit the brown areas of damaged cuticle typical of crustacean shell disease. Transmission and scanning electron microscopy of such lesions at a variety of sites on the body surface have demonstrated that they harbour dense populations of bacteria and occasionally fungi, in zones of superficial cuticular erosion. Complete penetration of the exoskeleton was inferred in instances when circular lesions were associated with bacteraemia of underlying soft tissues.     

DISPERSAL AND COLONIZATION OF THE EPIBIONT ALGA KORSHIKOVIELLA GRACILIPES (CHLOROPHYCEAE) ON DAPHNIA PULICARIA (CLADOCERA)

The dispersal and colonization of Korshikoviella gracilipes (Lambert) Silva on Daphnia pulicaria Forbes collected from a small high mountain lake in southern Spain were investigated in a series of laboratory experiments. Results of these laboratory experiments were related to previous field data. Massive release and detachment of zoospores, which is the dispersal stage of the epibiont, occurred just before molting. A lower number of zoospores was dispersed from the discarded molts and a scant number dispersed during the intermolt period. Release of cysts, which is the overwintering stage of the epibiont, mainly occurred immediately after the molt was discarded. The production of dispersal forms (zoospores and cysts) shows precise temporal synchronization with the molting process in Daphnia. The colonization of uninfected individuals from infected molts and from infected individuals was rapid. Our results suggest that colonization of field animals in this lake is efficient and is facilitated by the coincident aggregates of substrate and epibiont.     

Non-consumptive effects of larval Salamandra on crustacean prey: can eggs detect predators?

Predators affect prey populations not only by prey consumption but also in nonconsumptive ways including modifying prey behavior. I tested the effects of fire salamander larvae (Salamandra infraimmaculata) on populations of co-occurring crustacean species in artificial outdoor pools. I also tested whether these effects were due entirely to prey consumption by Salamandra larvae or alternatively to some nonconsumptive effect. The soil (containing crustacean eggs) added to the artificial pools was collected from a dried-out temporary pool that is inhabited by Salamandra during the early part of the hydroperiod. I randomly assigned the pools to one of three treatments: control, free Salamandra, or caged Salamandra. Free salamander larvae could roam the entire pool and prey upon crustaceans. Caged salamander larvae were placed within a cage with having 250-μm mesh windows. They could not prey upon the crustaceans but could, for example, influence them by chemical cues. Densities of the three dominant crustacean species (Arctodiaptomus similis, Ceriodaphnia quadrangula and Cyzicus sp.) were drastically reduced in both salamander treatments compared to the control. Crustacean densities, however, were not significantly different between the two salamander treatments. One plausible explanation is that crustacean eggs can detect the presence of this predator via chemical cues and delay hatching. Received: 4 March 1996 / Accepted, 23 October 1996     

Effects of artificial epibionts on byssogenesis,attachment strength,and movement in two size classes of the blue mussel,Mytilus edulis

Blue mussels (Mytilus edulis) can alter the strength of byssal attachment and move between and within mussel aggregations on wave‐swept shores, but this movement ability may be limited by epibiont fouling. We quantified the effects of artificial epibiont fouling on the production of byssal threads, attachment strength, and movement in two size classes of blue mussels. In a factorial experiment, large epibiont‐covered mussels produced more functional byssal threads (i.e., those continuous from animal to substrate) after 24 h than large unfouled and small fouled mussels, but not more than small unfouled mussels. Small unfouled mussels formed and released more byssus bundles compared to any other treatment group, which indicates increased movement. Conversely, epibiont fouling resulted in decreased numbers of byssus bundles shed, and therefore reduced movement in small mussels. Epibiont‐covered mussels started producing byssal threads sooner than unfouled mussels, while small mussels began producing byssal threads earlier compared to large mussels. Mean attachment strength from both size classes increased by 9.5% when mussels were artificially fouled, and large mussels had a 34% stronger attachment compared to small mussels. On the other hand, a 2.3% decrease in attachment strength was found with increasing byssus bundles shed. Our results suggest that fouling by artificial epibionts influences byssal thread production and attachment strength in large mussels, whereas epibionts on small mussels impact their ability to move. Mussels are able to respond rapidly to fouling, which carries implications for the dynamics of mussel beds in their intertidal and subtidal habitats, especially in relation to movement of mussels within and among aggregations.     

Structure and mating system of the graminicolous fungal epibiont Echinodothis tuberiformis (Clavicipitales)

The developmental morphology and mating system of the epibiont Echinodothis tuberiformis is investigated. The structure of conidial stromata, conidia, perithecial stromata, asci, and ascospores is documented. Crosses involving transfer of conidia between stromata resulted in formation of perithecia, indicating a heterothallic mating system. Comparisons are made to other members of the Clavicipitales that are presently classified in the tribe Balansieae. It is suggested that this epibiont bears a closer relationship to the grass endophytes classified in the genus Epichloë (Fr.) Tul. than to several other members of the Balansieae.     

Sustainable control of mosquito larvae in the field by the combined actions of the biological insecticide Bti and natural competitors

Integrated management of mosquitoes is becoming increasingly important, particularly in relation to avoiding recolonization of ponds after larvicide treatment. We conducted for the first time field experiments that involved exposing natural populations of the mosquito species Culex pipiens to: a) application of the biological insecticide Bacillus thuringiensis israelensis (Bti), b) the introduction of natural competitors (a crustacean community composed mainly of Daphnia spp.), or c) a combined treatment that involved both introduction of a crustacean community and the application of Bti. The treatment that involved only the introduction of crustaceans had no significant effect on mosquito larval populations, while treatment with Bti alone caused only a significant reduction in the abundance of mosquito larvae in the short‐term (within 3–10 days after treatment). In contrast, the combined treatment rapidly reduced the abundance of mosquito larvae, which remained low throughout the entire observation period of 28 days. Growth of the introduced crustacean communities was favored by the immediate reduction in the abundance of mosquito larvae following Bti administration, thus preventing recolonization of ponds by mosquito larvae at the late period (days 14–28 after treatment). Both competition and the temporal order of establishment of different species are hence important mechanisms for efficient and sustainable mosquito control.     

经济甲壳动物实验种群的研究进展

综述了近１０年来国内外经济甲壳动物实验种群的研究进展。内容包括几种主要经济种类的生活环境条件,如水温、盐度、溶氧量、透明度、底质等;饵料方面的研究;种内关系（性别、种内竞争）;种间关系（种间竞争、捕食、混养）;甲壳动物的特征行为—自截对其自身的影响以及病害等方面的研究结果。     

Local adaptation and enhanced virulence of Nosema granulosis artificially introduced into novel populations of its crustacean host, Gammarus duebeni

Local adaptation theory predicts that, on average, most parasite species should be locally adapted to their hosts (more suited to hosts from local than distant populations). Local adaptation has been studied for many horizontally transmitted parasites, however, vertically transmitted parasites have received little attention. Here we present the first study of local adaptation in an animal/parasite system where the parasite is vertically transmitted. We investigate local adaptation and patterns of virulence in a crustacean host infected with the vertically transmitted microsporidian Nosema granulosis. Nosema granulosis is vertically transmitted to successive generations of its crustacean host, Gammarus duebeni and infects up to 46% of adult females in natural populations. We investigate local adaptation using artificial horizontal infection of different host populations in the UK. Parasites were artificially inoculated from a donor population into recipient hosts from the sympatric population and into hosts from three allopatric populations in the UK. The parasite was successfully established in hosts from all populations regardless of location, infecting 45% of the recipients. Nosema granulosis was vertically (transovarially) transmitted to 39% of the offspring of artificially infected females. Parasite burden (intensity of infection) in developing embryos differed significantly between host populations and was an order of magnitude higher in the sympatric population, suggesting some degree of host population specificity with the parasite adapted to its local host population. In contrast with natural infections, artificial infection with the parasite resulted in substantial virulence, with reduced host fecundity (24%) and survival (44%) of infected hosts from all the populations regardless of location. We discuss our findings in relation to theories of local adaptation and parasite-host coevolution.     

Epibiont protozoan communities on Caridina lanceolata (Crustacea, Decapoda) from the Malili lakes of Sulawesi (Indonesia)

The epibiont protozoan communities living on the freshwater shrimp Caridina lanceolata Woltereck, 1937a from the three major lakes (Towuti, Matano and Mahalona) of the Malili lake system (Sulawesi, Indonesia) were studied. The number of epibionts varied between 2 and 971 per shrimp. Seven protozoan ciliate species were found: Acineta sulawesiensis n. sp., Cothurnia sp., Zoothamnium sp. (in all three lakes), Vorticella sp. (Lake Mahalona and Lake Matano), Opercularia sp. (Lake Mahalona), Epistylis sp. (Lake Mahalona and Lake Matano), and Podophrya sp. (Lake Mahalona). Although these ciliates had been found previously on other crustaceans, they have not been observed as epibionts on Caridina H. Milne Edwards, 1837. The distribution of the different epibiont species on the anatomical units of the shrimp was analyzed in each lake. There is a statistical significant difference between the three lakes in respect to the number of epibionts on each anatomical unit of all analyzed shrimps. The total and mean densities of each epibiont species on the different analyzed shrimps showed a significant difference between the three lakes; i.e., the presence of each epibiont species on the population of C. lanceolata varied from one lake to another. In Lake Towuti the highest density of epibionts was found on the anterior part of the shrimp body (rostrum, antennae, antennulae and eyes) (32.41%), while in the other two lakes, the highest colonization corresponded to the maxillipeds (31.56% Lake Matano, 40.89% Lake Mahalona). In Lake Towuti the rest of epibionts colonized mainly maxillipeds and pleopods (both 45.76% of epibionts). In Lake Matano, other epibionts were distributed principally on the anterior part of the body and pleopods (in total 57.18% of epibionts). In Lake Mahalona, other epibionts were divided among the anterior part of the body, pereiopods and pleopods (in total 57.39% of the epibionts). Uropods and telson were the units less colonized in Lake Matano (3.64%) and Lake Mahalona (1.72%), while in Lake Towuti, they presented a moderate density (13.18% of the epibionts). Taking into account the distribution of epibionts along the antero-posterior axis of the shrimp, considering the different anatomical units, there was a significant correlation between the three lakes. This fact indicates that, in the three lakes, the colonization on C. lanceolata followed a similar distribution pattern, independently of the epibiont species present. The comparison between the distributions of the same epibiont species along the longitudinal axis of the shrimp on the diverse lakes showed that they correlated respect to their density values on the anatomical units of the shrimp. Diverse aspects of the colonization patterns are discussed. Morphological features, taxonomic identification, and particular distribution of the epibiont species in each lake are also included.     

Ultrastructural characterization of the prokaryotic symbiosis in "Chlorochromatium aggregatum"

The phototrophic consortium "Chlorochromatium aggregatum" currently represents the most highly developed interspecific association of bacteria and consists of green sulfur bacteria, so-called epibionts, surrounding a central, motile, chemotrophic bacterium. In order to identify subcellular structures characteristic of this symbiosis, consortia were studied by a combination of high-resolution analytical scanning electron microscopy, transmission electron microscopy, and three-dimensional reconstruction and image analyses. Epibionts are interconnected and to a lesser extent are also connected with the central bacterium, by electron-dense, hair-like filaments. In addition, numerous periplasmic tubules extend from the outer membrane of the central bacterium and are in direct contact with the outer membrane of the epibionts. In each epibiont cell, the attachment site to the central bacterium is characterized by the absence of chlorosomes and an additional 17-nm-thick layer (epibiont contact layer [ECL]) attached to the inner side of the cytoplasmic membrane. The ECL is only occasionally observed in pure cultures of the epibiont, where it occurs in about 10 to 20% of the free-living cells. A striking feature of the central bacterium is the presence of one or two hexagonally packed flat crystals (central bacterium crystal [CBC]) per cell. The CBC reaches 1 microm in length, is 35 nm thick, and consists of bilayers of subunits with a spacing of 9 nm. A detailed model for consortia is presented, summarizing our conclusions regarding (i) cohesion of the cells, (ii) common periplasmic space between the central bacterium and the epibiont, (iii) ECL as a symbiosis-specific structure, and (iv) formation of the interior paracrystalline structures, central bacterium membrane layer, and CBC.     

Direct and indirect influences of crustacean zooplankton on bacterioplankton of Lake Constance

Herbivorous crustacean zooplankton may influence bacterial populations of lakes directly by grazing on them or indirectly by grazing on algae. In Lake Constance a regularly observed decrease of bacterial density during periods of high abundance of cladocerans (clearwater phase) indicated bacterial grazing losses. However, cladoceran grazing on bacteria appeared to be less efficient than on algae. Moreover, cladocera reduced grazing pressure on bacteria by grazing on bacterivorous flagellates. Additionally, a shift of bacterial composition from an originally higher percentage of filamentous and aggregate growth forms towards a population of homogenously distributed small single celled bacteria was observed regularly at the beginning of the clearwater phase. Transient increases of bacterial abundance and productivity coinciding with the increase of cladocera at the end of the algal spring bloom were interpreted as field indications of indirect bacteria-zooplankton interactions due to crustacean grazing on phytoplankton. The release of organic carbon during grazing of crustacea on algae was considered as explanation for the observed stimulation of bacterial populations. Thereby, additional, otherwise inaccessible algal carbon would be made available to bacteria by zooplankton. Experimental support for this hypothesis was given by showing that bacteria were able to respond to crustacean grazing on algae by enhanced growth and activities. The possible impact of these direct and indirect crustacea-bacteria interactions on the abundance, activity and composition of bacterioplankton as well as on the structure and function of the total planktonic community is discussed.