Host Mussels Research Articles

Seasonal change in the spatial utilization of host mussels in relation to ovipositor length by female rosy bitterling Rhodeus ocellatus kurumeus

The seasonal changes in ovipositor length and utilization patterns of mussels for oviposition in the rosy bitterling Rhodeus ocellatus kurumeus(Cyprinidae) were investigated in a field experiment and field surveys during the breeding period (April to August). The mean length of ovipositors at oviposition was short at the start (early April) and end (July) of the breeding period. Females with long ovipositor at oviposition were collected between mid‐April and June. Mark‐and‐recapture data showed that ovipositor length at oviposition changed rhythmically throughout the breeding period, shortening and lengthening as the female entered the spawning and resting phase. The density of rosy bitterling embryos in mussels increased between April and June, peaking in May, but decreasing in July. The position of eggs on mussel gills varied from close to the exhalant siphon to deeper inside the gill during April, and periodically thereafter. There was a positive correlation between ovipositor length at oviposition and the distance from exhalant siphon of mussels to eggs deposited by females, suggesting that ovipositor length at oviposition determined the position of eggs deposited on a mussel gill. Because dissolved oxygen in mussel gills decreased with the density of bitterling embryos, suitable positions for embryo survival in gills changed with embryo density. By changing ovipositor length at oviposition, females might be able to spawn their eggs in a position that maximizes embryo survival. Thus, plasticity in ovipositor length at oviposition may play an important role as an adaptation of rosy bitterling in utilizing mussels when their quality as a spawning substratum fluctuates seasonally.

Effects of epibiotic algae on the survival, biomass and recruitment of mussels, Mytilus L. (Bivalvia: Mollusca)

Habitats composed of living ‘ecosystem engineers’, such as mussels, are subject to direct and indirect interactions with organisms that live among them. These interactions may affect the presence and structure of habitat, and hence, the associated taxa. We examined the direct effects of epibiotic algae on the survival, biomass and recruitment of mussels ( Mytilus L.) on the west coast of Ireland. A field experiment showed that the presence of epibiotic fucoid algae reduced the likelihood of survival of mussels during storms. We also found that the strength of attachment of mussels did not increase in the presence of epibionts. Another in situ experiment revealed that the presence of ephemeral epibiotic algal mats had no effect on the biomass of host mussels, suggesting no effect on mussel growth or production. The abundance of small mussels (< 5 mm) covaried with cover of epibiotic algae at one location, but experimental results suggest no direct effect of the algae on recruitment unless through the action of chemical cues which linger after the removal of algae. We have identified a negative direct interaction between epibiotic algae and mussels on exposed rocky shores, which may often be characterised by bottom-up regulation. It is thought that positive interactions may be more important on more sheltered or sedimentary shores where top-down processes are more likely to dominate.

Factors affecting seasonal mortality of rosy bitterling (Rhodeus ocellatus kurumeus) embryos on the gills of their host mussel

Factors affecting seasonal mortality of rosy bitterling (<i>Rhodeus ocellatus kurumeus</i>) embryos on the gills of their host mussel

Factors affecting seasonal mortality of rosy bitterling (Rhodeus ocellatus kurumeus) embryos on the gills of their host mussel

AbstractI investigated the seasonal change in factors affecting embryonic mortality in the rosy bitterling, Rhodeus ocellatus kurumeus, a freshwater fish that spawns on the gills of living unionid mussels. Research was conducted in a small pond during 1999 and 2001 in which bitterling were provided with Anodonta sp. mussels for spawning. Bitterling spawned between April and July, peaking mid–late May. Seasonal survival rate of bitterling embryos in their mussel hosts was unimodal, with a peak between late April and mid May (about 70% of total spawnings). In mid April, survival was about 50%. The lowest survival was from late May to July (0%). Losses of bitterling embryos from mussels were identified by ejections from the mussel host. Ejections were categorized as either ejections of live embryos, or ejections of embryos that died in the mussel and were subsequently expelled from the mussel. Ejection rates of live embryos were higher in the earlier part of the spawning period (early–mid April) and dead embryo ejections in the later period (after June). The ejection rate of live embryos was higher among younger embryos earlier in the season, probably because of the incomplete development of morphological and behavioural traits associated with maintaining the embryo inside the mussel gill chambers, and as a consequence of a more protracted developmental period at low temperatures making them more susceptible to ejection. The ejection rate of dead embryos was higher in older embryos later in the season, and in larger mussels and at high embryo densities. The survival of embryos in mussels was probably related to oxygen availability, with mortalities probably caused by asphyxiation. Increased embryo mortalities may arise through competition among embryos, between embryos and mussel, and ambient dissolved oxygen levels. The optimal period for bitterling to spawn may represent a balance between two opposing factors; with positive and negative effects of a seasonal rise in temperature directly affecting embryonic growth rate and oxygen availability.

The importance of species interactions in conservation: the endangered European bitterling Rhodeus sericeus and its freshwater mussel hosts

AbstractSpecies conservation may be complicated in symbiotic interactions. Sub‐lethal impacts of human activities on one species may be lethal to other species on which they depend. We investigated the impact of two aspects of eutrophication – changes in phytoplankton and oxygen levels – on the interaction between a freshwater fish that is endangered in several countries, the European bitterling, Rhodeus sericeus, and the unionid mussel hosts that they require for spawning. Reduced concentrations of algae and oxygen each led to a greater proportion of bitterling embryos being ejected prematurely from the mussel hosts. Reduced algal concentrations also led to reductions in mussel ventilation rates and to mussels spending less time with their valves open. Bitterling mortality may have been due to three causes: direct effects of environmental conditions on embryonic survival, active expulsion by mussels when stressed and through responses by mussels that created internal conditions that bitterling embryos could not survive. Our study shows that the sub‐lethal effects of pollution on one species can have lethal effects on another species with which it interacts. Such interactions need to be considered in conservation programmes.

Environment drives physiological variability in the cold seep mussel Bathymodiolus childressi

The ability of an organism to respond to changes in its environment depends upon its short‐term physiological plasticity and the constraints of its genetic makeup. At hydrothermal vents and cold seeps, the spatially variable physiological characteristics of symbiont‐bearing animals are often assumed to reflect short‐term physiological adjustments to a patchy and dynamic chemical environment. However, the extent to which these spatially variable responses represent fixed characteristics unique to animals inhabiting the different environments (such as might arise from genetic differentiation) has not been tested. The seep mussel Bathymodiolus childressi depends upon methanotrophic bacteria for the bulk of its nutrition and inhabits a range of environments where it displays varying growth and body condition. In this study, we first investigated the multiscale environmental and physiological variability of B. childressi by measuring dissolved gas concentrations and mussel body condition in 12 mussel beds at four geographically distinct sites. Brine‐dominated seeps tended to have higher methane and sulfide concentrations and host mussels of better body condition than petroleum‐dominated sites. Then, using two transplant experiments, we evaluated whether local environmental conditions or stock effects determined the observed differences in growth and body condition of B. childressi. In all cases, mussels transplanted to new sites acquired or nearly acquired the characteristics of their host population, illustrating the primary role of the environment in determining the physiological characteristics of resident mussels. However, mussels from different sites sometimes responded differently to the same environment, suggesting stock‐related effects also play a role in the spatial variation observed in the physiology of chemosynthetic fauna.

Random amplified polymorphic DNA analysis of kinship within host-associated populations of the symbiotic water mite Unionicola foili (Acari: Unionicolidae)

Kinship relations within populations of unionicolid water mites are not well known, owing to their complex life cycles and the fact that interactions between active and resting stages for some species are transitory. A number of species of unionicolid water mites are, however, obligate symbionts of freshwater mussels and spend most of their life cycle in association with these hosts. Among these species of mites, parents and offspring are more likely to co-occur and thus provide opportunities to address questions related to the structure of the mating system. The present study employs random amplified polymorphic DNA (RAPD) analysis to address kinship within populations of Unionicola foili living in symbiotic association with the host mussel Utterbackia imbecillis. DNA was amplified from adult mites and a representative number of eggs or larvae (n = 20-30) that were removed from mussels collected on three separate occasions (July, November, and March) over a 12-month period. Parsimony analyses of the molecular data for adults and progeny collected from mussels during July, November, and March revealed distinct groupings, that for the most part, corresponded to mites collected from each of the sampling periods. Many of the genetic markers obtained for male and female U. foili were not evident among the larvae or eggs, suggesting that adults obtained from a host mussel at the time of collection were not the parents of a majority of the progeny. However, female mites and eggs collected from mussels during March and November shared more markers than did females and progeny examined during July. Furthermore, many offspring in the July sampling period were found to have one or more parents absent from the sampled population. Overall, RAPD profiling appears to have limited usage in determining kinship within populations of U. foili, due to its recruitment patterns, and the relatively large number of adults and progeny per mussel. It may, however, prove to be a useful method for assessing genetic relatedness among unionicolid mussel-mites that have substantially lower population densities.

Filial cannibalism improves survival and development of beaugregory damselfish embryos

Cannibalism of small numbers of offspring by a parent has been proposed as an adaptive parental strategy, by providing energy to support parental care. However, there are few empirical studies to support this hypothesis. We conducted field and laboratory experiments to investigate partial filial cannibalism in Stegastes leucostictus, a coral reef fish with paternal care. Partial cannibalism was shown to be common, and males were found to remove developing embryos from throughout a clutch in a random pattern, rather than in the more aggregated pattern seen during embryo predation. Males that received a diet supplement grew faster than control males, but did not engage in less cannibalism. Also, males did not concentrate cannibalism on early embryonic stages with the highest energetic value. Experimental reduction of embryo densities was found to significantly increase embryo development rate and survival from egg deposition to hatching, and experimental reduction of oxygen levels significantly increased rates of partial filial cannibalism by males. Artificial spawning sites with low oxygen levels were avoided by spawning females, and cannibalism rates by males were higher. We propose that partial filial cannibalism serves as an adaptive parental strategy to low oxygen levels in S. leucostictus by increasing the hatching success of embryos.

Seasonal dynamics of Conchophthirus acuminatus (ciliophora, conchophthiridae) infection in Dreissena polymorpha and D. bugensis (bivalvia, dreissenidae)

Summary Although considerable research has been carried out on Dreissena spp., relatively little is known about the symbiotic organisms living within them. We report a two-year study of the dynamics of infection by the commensal ciliate Conchophthirus acuminatus in D. polymorpha and D. bugensis populations in the Dnieper River in the Ukraine and in four D. polymorpha populations in Belarus. C. acuminatus was present in all samples. The moderate to high infection prevalence and moderate infection intensity that we recorded in D. polymorpha populations were in contrast to the low prevalence and very low intensity of infection observed in D. bugensis . Recording C. acuminatus in D. bugensis represents the first record of any ciliate species from this mussel and the first report of C. acuminatus in a host other than D. polymorpha . Since infection prevalence and intensity strongly correlated with the size of D. polymorpha , the presence of large, infected mussels is likely important to serve as a reservoir for maintaining infection in the overall population. To infect new host mussels, C. acuminatus must disperse into surrounding waters, and we suggest that a period of mass dispersal may be synchronized to occur when new potential hosts, i.e., juvenile mussels, become abundant.

The symbiotic water mite Unionicola formosa (Acari: Unionicolidae) ingests mucus and tissue of its molluscan host.

Unionicola formosa is a symbiotic water mite that passes most of its life cycle in the mantle cavity of freshwater mussels. Although mites of this genus are often referred to as parasitic, little is known about their nutritional biology. A few species reportedly pierce the gill of a host mussel and ingest tissue or hemolymph. The present study was undertaken to identify possible sources of nutrition for U. formosa. To determine if mites ingested particulate matter in the mucous strand produced by a mussel during feeding, mussels with resident mites were exposed to a suspension of fluorescent microspheres. There was no evidence that U. formosa ingested the beads. Histochemical staining did, however, indicate a mucous material present in the midgut of the mites. Sodium dodecyl sulfate-polyacrylamide gel electrophoretic assays revealed a high molecular weight component, consistent with a mucopolysaccharide, present both in the mussel gill and the mites. Results from western blots and an immunoaffinity binding assay with antibodies against mussel gill tissue and hemolymph also indicated that mites ingested host tissue. Whereas U. formosa probably does not ingest particulate material acquired by its host's suspension feeding, it is apparent that this mite utilizes host mucus, gill tissue, or hemolymph for at least part of its nutrition.

Rhythmicity of larval release in three species of intertidal brachyuran crabs (Crustacea: Brachyura) from Inhaca Island (Mozambique)

A study of rhythmicity of larval release in three species of intertidal brachyuran crabs, based on laboratory and field experiments, was undertaken at Inhaca Island, southern Mozambique, using Leptodius exaratus and Macrophthalmus grandidieri from December 1994 to January 1995, and Arcotheres palaensis from April to July 1995. L. exaratus and M. grandidieri showed a semi-lunar cycle in larval release. The release of larvae for L. exaratus, a species having conspicuous larvae, occurred in the first half of the night, after the post-crepuscular high tide, which suggests maximisation of protection of larvae from visual predation. The larval release activity matched the late spring and early neap tides. Results from the field were similar to those from the laboratory. M. grandidieri, having inconspicuous larvae, did not show a pattern related to the light–dark cycle and hatched during spring tides (around full and new moons) to maximise larval dispersion. A. palaensis, living inside the host mussel which inhabits the lowest section of the intertidal zone, did not show a relation with moon phase, tidal or light–dark cycles.

Lethal and sub-lethal effects of phototrophic endoliths attacking the shell of the intertidal mussel Perna perna

Animals that bore into calcareous material can cause considerable damage to molluscan shells. In contrast, smaller microbial phototrophic endoliths have until recently been thought of as relatively benign. Phototrophic endoliths (primarily cyanobacteria) infest the shells of 50 to 80% of midshore populations of the mussel Perna perna (L.) in South Africa. This infestation causes clearly visible shell degradation, and we record here ecologically important lethal and sub-lethal effects (e.g. changes in growth and reproductive output) of the endoliths on their mussel hosts. Endolith infestation reduced the strength of shells significantly and also affected shell growth. In situ marking of shells, using the fluorochrome calcein, showed that infested and non-infested mussels increased in shell length at the same rate. However, the rate of increase in shell thickness (associated with shell repair) was significantly faster in infested than in uninfested individuals. This increase in the rate of shell thickening was not sufficient to compensate for rapid endolith-induced shell degradation and, around the site of adductor muscle attachment, infested shells were thinner than their uninfested counterparts. The shells of 18% of recently dead mussels had holes induced by endolith erosion. This effect was highly size dependent, and the proportion of mortality due to endoliths rose to almost 50% for the largest mussels. The re-routing of energy due to shell repair had important sub-lethal effects on the reproductive rates of mussels. During the reproductive period, mean dried flesh mass for large (>70 mm), non-infested P. perna was substantially higher than for infested individuals. This difference was almost entirely due to differences in gonad mass, which was approximately 100% higher for non-infested mussels. We conclude that, by attacking the shell, phototrophic endoliths reduce both the longevity and reproductive output of large mussels on the midshore.

Indirect Effects of Epibiosis on Host Mortality: Seastar Predation on Differently Fouled Mussels

In situ experiments were run with the seastar Asterias rubens to investigate the influence of epibiosis on predation preferences. Mussels (Mytilus edulis) monospecifically fouled by different epibiont species (the barnacle Balanus improvisus, the red filamentous alga Ceramium strictum, the sponge Halichondria panicea and the hydrozoan Laomedea flexuosa) and macroscopically clean mussels were exposed and seastar predation was monitored by SCUBA. Asterias rubens preferred macroscopical unfouled mussels as prey. Fouling generally reduced predation pressure on the mussel hosts (associational resistance). Barnacles protected mussels less efficiently than hydrozoans or algae.We hypothesize that in top‐down controlled communities this influence of epibiosis on predation pressure should affect mussel community patterns. A survey of natural mussel‐epibiont distribution in the presence or absence of A. rubens showed that the prevalence of differently fouled mussels differed between predation‐exposed and predation‐protected habitats. Natural mussel‐epibiont associations reflected the preferential predation of the major local predators. Additionally, higher epibiotic diversity and evenness could be observed at locations accessible to benthic predators as compared with habitats protected from predation.As blue mussels and seastars are important structuring and controlling elements in the shallow water community of Kiel Fjord, major consequences of epibiosis on the entire system are discussed.

Site‐specific and ontogenetic variations in nutrition of mussels (Bathymodiolus sp.) from the Lucky Strike hydrothermal vent field, Mid‐ Atlantic Ridge

Lucky Strike mussels (Bathymodiolus sp.) support two metabolically distinct (methanotrophic and thiotrophic) prokaryotic endosymbionts in their gills. Differences in source inorganic carbon isotope ratios and in carbon fixation pathways between these two symbionts typically result in organic carbon with distinctive δ13C values. Site‐specific differences in isotopic compositions of host mussels may therefore reflect differences in sulfide and methane availability. Large differences in mean carbon and nitrogen isotopic compositions were observed in adult mussels collected from two chemically distinct vents at Lucky Strike (Sintra: d13C 5 221.3‰, δ15N 5 –4.5‰; Eiffel Tower: δ13C = –30.7‰, δ15N = –10.5‰). These values are consistent with the hypothesis that Sintra mussels are more dependent on methanotrophy than are Eiffel Tower mussels. Relative abundances of the two types of endosymbionts in mussel gill tissues (Sintra: mean = 15% methanotrophs; Eiffel Tower: mean = 6% methanotrophs) provide further support of this hypothesis, suggesting that Lucky Strike mussels express a nutritional response to environmental variations. Within sites, there were small but significant correlations between isotopic composition and mussel size over the shell lengths of 15–80 mm, but these shifts are so small that they are attributable to factors other than ontogenetic shifts in nutritional strategy. In contrast, large nitrogen isotope differences were observed between larval and adult stages. Based on δ15N values, mussel larvae appear to rely very little on photosynthetically derived organic material. Observations of the demersal nature of mussel larvae and isotopic similarities between Sintra and Eiffel Tower larvae and Sintra adults suggest that the potential of stable isotopes as useful tracers of larval sources within the Lucky Strike vent field should be considered.

Effects of phosphate on the reproductive symbiosis between bitterling and freshwater mussels: implications for conservation

Summary We examined the effects of phosphorus, an important pollutant in fresh waters, on mussels Anodonta anatina and embryos of European bitterling Rhodeus sericeus amarus. These species are involved in an unusual symbiosis, with the fish depositing eggs inside the mussels' gills, where the embryos develop for 3–6 weeks until the larvae leave the mussel. High concentrations of phosphate (500 μg L−1 and higher) caused a significant increase in the rate of premature expulsion and emergence of bitterling embryos from the mussels, with a concomitant increase in fish mortality. At concentrations of 750 μg L−1 and higher, mussels reduced their frequency of ventilation and movements through the substratum. These results have implications for understanding the nature of the symbiosis between the fish and their mussel hosts, showing that mussels have control over bitterling developing in their gills. The premature expulsion of bitterling embryos at high phosphate levels is detrimental to the fish that they harbour. Recommendations for the conservation of bitterling and species of mussels, which are threatened or endangered over parts of their ranges, include reductions in levels of phosphorus in natural habitats and the need for low levels in reintroduction sites for the fish and their mussel hosts.

Field and Laboratory Studies of Zebra Mussel (Dreissena polymorpha) Infection by the CiliateConchophthirus acuminatusin the Republic of Belarus

This study quantifies the infection prevalence and intensity of the European, commensal, host-specific ciliateConchophthirus acuminatus(Scuticociliatida: Conchophthiridae) in five zebra mussel populations within the Republic of Belarus. Laboratory and field experiments were also conducted to assess variables affecting infection.C. acuminatuswas found in zebra mussels in all five waterbodies sampled: Naroch, Myastro, and Lukomskoe Lakes, Skema Stream, and in the Svisloch River. Prevalence was always 100%, with the exception of shallow areas (≤0.5 m depth) in the Svisloch River. This was possibly the result of the elimination of the majority of infected zebra mussels each winter by a combination of factors, including ice scour, mallard duck predation, and fluctuating water levels. As a result, zebra mussels are not permanently present at shallow depths, and the mussels that we randomly sampled there during the summer were thus smaller (i.e., younger) and less infected than those present in deeper sections of the river. This is the first study to quantify the intensity ofConchophthirusinfection in zebra mussels. When infection prevalence was 100%, it was not uncommon for zebra mussels to have 500–2,000C. acuminatusin their mantle cavities, particularly those mussels ca. 15–30 mm in length. Zebra mussels, while relatively small bivalves, have one of the highest intensities ever reported for ciliates in the order Scuticociliatida. Infection intensity correlated directly with mussel length (range inr2=0.83–0.92). Transinfection of zebra mussels withC. acuminatuswas achieved both in the laboratory and field, and represented the first successful trials to initiate protozoan infection inDreissena.Laboratory experiments demonstrated thatC. acuminatusrapidly leave their dying zebra mussel hosts, and this suggested that these mussels are likely a major source for the spread ofC. acuminatusinfection. Field trials indicated that the presence of mussels with high intensity infections can cause an increase in the levels of infection (both prevalence and intensity) in other zebra mussels in their microhabitat.

Genetic Differentiation between Unionicola formosa and U. foili (Acari: Unionicolidae): Cryptic Species of Molluscan Symbionts

Genetic Differentiation between Unionicola formosa and U. foili (Acari: Unionicolidae): Cryptic Species of Molluscan Symbionts

Specificity of the host recognition behaviour of larvalUnionicola(Acari: Unionicolidae): the effects of larval ontogeny and early larval experience

The water mitesUnionicola formosaandU.foiliare obligate symbionts of the freshwater unionid musselsPyganodon cataractaandUtterbackia imbecillis, respectively. Although behavioural specificity of adultU.formosaandU.foiliis well documented, behaviour of the larvae of these species is poorly understood. The present study revealed that host-influenced behaviour of larvalU.formosaandU.foiliis highly host-specific, but changes during larval ontogeny. Larvae that had completed their parasitic phase with chironomid dipterans (=post-chironomid larvae) preferentially responded to a chemical signal from their respective host mussel, and exhibited the host-induced negative phototaxis that characterizes adult mites. Specificity of the host recognition behaviour of post-chironomid larvae was modified when larvae were exposed to water modified by a non-host mussel species early in development. The chemically mediated behaviour patterns exhibited by post-chironomid larvae were absent among mite larvae prior to parasitizing chironomids (=pre-chironomid larvae). These data suggest that parasitism of a chironomid is adaptive for the ontogeny of behaviour of these mussel-mites at specific stages in the mite's life cycle. Differences in the behaviour of pre-chironomid and post-chironomid larvae may reflect the different demands of contacting an insect host prior to establishing the symbiotic association with the final molluscan host. The behavioural preferences of larvalU.formosaandU.foilicomplement those of adult mites and suggest that host specificity is an important mechanism in maintaining reproductive isolation between these two species.

The effect of pea crabs on predation of host mussels by sea stars

Pea crabs parasitize a large proportion of mussels in Narragansett Bay, Rhode Island. Large mussels (>50 mm shell length) are more heavily parasitized than smaller mussels. Previous work on the ene...

Host-Induced Morphology in Mites: Implications for Host-Parasite Coevolution

Coevolution of parasites and their hosts is presumed if the phylogeny of a group of parasites matches that of their hosts, producing a high value of a consistency index. Such comparisons are done using relatively host specific parasite species that are usually separated only by morphological characters. Parasitic, unionicolan mites in the subgenus Unionicolides are described, from sampling data, as highly host specific and are thought to have co-speciated with their freshwater mussel hosts. However, experimental observations of Unionicola Unionicolides poundsi and U. U. lasellai were inconsistent with these mites' supposed high host specificity. A transplant experiment, in which nymphs metamorphosed in the wrong host, demonstrated that the morphological characters used to differentiate these mite species are plastic and host- determined. Hence, when taxonomists use only morphological characters and host-induced morphological variation is present, morphological variants can be elevated to the status of species. Consequently, parasites can appear to be highly host specific. If morphs are then grouped, as species, into the same taxon, phylogenetic comparisons can produce high consistency indices independently of any coevolutionary processes. The conditions under which this bias can occur are commonly true of phylogenetic comparisons. Hence, host-induced morphology is a viable, alternative explanation for high consistency indices. (Host-parasite coevolution; mites.) Coevolution between parasites and hosts