Indigenous microflora and opportunistic pathogens of the freshwater zebra mussel, Dreissena polymorpha

Freshwater fouling invertebrate zebra mussels (Dreissena polymorpha) harbor a diverse population of microorganisms in the Great Lakes of North America. Among the indigenous microorganisms, selective species are opportunistic pathogens to zebra mussels. Pathogenicity to zebra mussels by opportunistic bacteria isolated from the mussels was investigated in this study. Among the more than 30 bacteria isolated from temperature-stressed mussels, Aeromonas media, A. veronii, A. salmonicida subsp. salmonicida, and Shewanella putrefaciens are virulent pathogens to juvenile zebra mussels. Inoculation of a bacterial concentration of A. media, A. salmonicida subsp. salmonicida and S. putrefaciens at 10⁷ cells per zebra mussel resulted in 100% mortality within 5 days, and only 64.9% for A. veronii. In contrast, mortality was less than 12.3% following inoculation of a sterile phosphate buffer solution as a control. In addition, mortality was dependent on the size of the pathogen population used in inoculation and the incubation temperature, indicating the close relationship between the bacterial population and subsequent death. On the mussel tissue, a dense microbial population was evident from the moribund mussels viewed with Scanning Electron Microscope (SEM). Opportunistic bacteria invaded and destroyed the D. polymorpha tissue after 7 days of incubation when the bacterial inoculation was larger than 10⁵ per zebra mussel. Our results suggest that mussels are reservoirs of opportunistic pathogenic microorganisms to aquatic organisms and humans and a better understanding of the microbial ecology of the mussels will provide insights to the possible health hazards from these microorganisms.     

Seston quality drives feeding,stoichiometry and excretion of zebra mussels

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Effects of β‐xylanase and 6‐phytase on digestibility,trace mineral utilisation and growth in juvenile red tilapia,Oreochromis niloticus (Linnaeus, 1758) x O. mossambicus (Peters, 1852), fed declining fishmeal diets

In response to the global sustainability drive to lower fishmeal (FM) inclusion in aquatic feeds, exogenous enzymes can improve nutrient digestibility in monogastric plant‐based diets. A 80‐day experiment was conducted to evaluate the combined effects of xylanase and phytase on digestibility, trace mineral utilisation and growth in juvenile red tilapia, Oreochromis niloticus x O. mossambicus, (48.8 g ± 13.9; μ ± STD) fed declining FM diets. Basal diets were formulated to contain 0, 3 and 5% FM with and without xylanase (0.385 g kg^?1) and phytase (0.075 g kg^?1), forming six treatments. Each treatment was randomly assigned to four replicates, 20 fish tank^?1; mean water temperature 28.98 ± 0.73°C. Although the size of the effects was modest, growth performances (feed intake, FCR, growth rate) decreased with lower FM levels (P < 0.05) but improved with enzyme supplementation. Enzyme supplementation increased P digestibility and trace mineral uptake (P < 0.05), but no effects were seen on protein digestibility and N retention. Nevertheless, tilapia fed the enzyme‐supplemented 3% FM and control 5% FM diets performed comparably (P < 0.05). This potentially justifies a 2% FM reduction for tilapia diets using exogenous xylanase and phytase without significant effects on digestibility, trace mineral utilisation and growth.     

Parasite‐induced alterations of host behaviour in a riverine fish: the effects of glochidia on host dispersal

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Sediment accumulation predicts the distribution of a unionid mussel (Elliptio complanata) in nearshore areas of a Canadian Shield lake

1. The importance of native freshwater mussels for ecosystem processes depends on their density, size distribution and activity. In lakes, many of the factors that affect mussels (fish hosts, habitat, food) could be directly or indirectly related to wind‐driven physical processes. 2. We tested whether the abundance and size of Elliptio complanata in the shallow, nearshore areas of a medium‐sized lake were related to site exposure, substratum type and fish distribution. To disentangle some of the correlated variables known to affect mussel distribution, we used paired exposed and sheltered sampling sites along the 7‐km fetch of the lake basin. 3. The distribution of sediment characteristics in nearshore areas was highly predictable. The mean depth of accumulated soft sediments decreased with increasing fetch at wind‐exposed sites, but increased with increasing fetch at sheltered sites. Sediments were deeper along the main shoreline than around islands. Deeper sediments tended to be finer and higher in silt content and organic fraction. 4. The density and proportion of juvenile mussels along the main shoreline varied in a unimodal way with sediment depth. These results suggest that wind‐driven physical forces affect the transport of young juveniles to sediment depositional areas and create sediment conditions that influence their growth and survival. In contrast, the proportion of juvenile mussels around islands was not related to sediment characteristics, but decreased with remoteness of the island, suggesting that the distribution of juvenile mussels may be limited by fish movements. These results are tentative since they do not include buried juvenile mussels. 5. We also found a unimodal relationship between total mussel density (juveniles and adults) and sediment depth but, in contrast to the relationship for juveniles only, it applied to all sites with soft sediments, including islands. We conclude that factors related to sediment depth affect the growth and survival of adult mussels around islands and that these factors are strong enough to modify the pattern of distribution established via dispersal during earlier life stages. 6. The mean shell length of adults at different sites within the lake basin ranged from 60 to 85 mm. Mussel shell length decreased with increasing fetch at sites exposed to the prevalent winds, but was relatively constant on the sheltered side of peninsulas and islands. The size of unionid mussels in different parts of the lake seems to be determined both by their exposure to physical forces and by sediments. 7. The local distribution of E. complanata is determined, directly and indirectly, by wind‐driven forces. These processes are likely to be important for other benthic organisms affected by similar habitat conditions (e.g. sediment characteristics, physical disturbance).     

Rose bitterling (Rhodeus ocellatus) embryos parasitize freshwater mussels by competing for nutrients and oxygen

Spence, R. and Smith, C. 2011. Rose bitterling (Rhodeus ocellatus) embryos parasitize freshwater mussels by competing for nutrients and oxygen. —Acta Zoologica (Stockholm) 00 : 1–6. Understanding how parasites inflict fitness costs on their hosts is a key question in host–parasite biology. Rose bitterling (Rhodeus ocellatus) are small cyprinid fish that place their eggs in the gills of living freshwater mussels. The embryos complete their development inside the mussel gill and emerge as free‐swimming larvae after approximately 4 weeks. Bitterling show a range of specialized adaptations for using mussels as a spawning substrate, and the presence of bitterling embryos has been shown to retard the growth of mussels. We compared the development and survival of embryos incubated in either mussels or Petri dishes and exposed to either nutrient‐rich or nutrient‐poor pond water. Embryonic development rate was significantly faster in Petri dishes, probably as a result of oxygen limitation in mussel gills. Embryo survival rate was significantly higher in nutrient‐rich than filtered water, suggesting that the embryos obtained a nutritional benefit prior to emergence from the host. The results imply that bitterling embryos compete for oxygen and nutrients with their host mussel, as well as each other, and in this way, impose a growth cost on mussels.     

Net cages enhance golden mussel (Limnoperna fortunei) larval density and condition factor

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Impacts of zebra mussels (Dreissena polymorpha) on isotopic niche size and niche overlap among fish species in a mesotrophic lake

Zebra mussels (Dreissena polymorpha) filter feed phytoplankton and reduce available pelagic energy, potentially driving fish to use littoral energy sources in lakes. However, changes in food webs and energy flow in complex fish communities after zebra mussel establishment are poorly known. We assessed impacts of zebra mussels on fish littoral carbon use, trophic position, isotopic niche size, and isotopic niche overlap among individual fish species using δ¹³C and δ¹⁵N data collected before (2014) and after (2019) zebra mussel establishment in Lake Ida, MN. Isotope data were collected from 11 fish species, and from zooplankton and littoral invertebrates to estimate baseline isotope values. Mixing models were used to convert fish δ¹³C and δ¹⁵N into estimates of littoral carbon and trophic position, respectively. We tested whether trophic position, littoral carbon use, isotopic niche size, and isotopic niche overlap changed from 2014 to 2019 for each fish species. We found few effects on fish trophic position, but 10 out of 11 fish species increased littoral carbon use after zebra mussel establishment, with mean littoral carbon increasing from 43% before to 67% after establishment. Average isotopic niche size of individual species increased significantly (2.1-fold) post zebra mussels, and pairwise-niche overlap between species increased significantly (1.2-fold). These results indicate zebra mussels increase littoral energy dependence in the fish community, resulting in larger individual isotopic niches and increased isotopic niche overlap. These effects may increase interspecific competition among fish species and could ultimately result in reduced abundance of species less able to utilize littoral energy sources.

     

Predation on exotic zebra mussels by native fishes: effects on predator and prey

SUMMARY 1. Exotic zebra mussels, Dreissena polymorpha, occur in southern U.S. waterways in high densities, but little is known about the interaction between native fish predators and zebra mussels. Previous studies have suggested that exotic zebra mussels are low profitability prey items and native vertebrate predators are unlikely to reduce zebra mussel densities. We tested these hypotheses by observing prey use of fishes, determining energy content of primary prey species of fishes, and conducting predator exclusion experiments in Lake Dardanelle, Arkansas. 2. Zebra mussels were the primary prey eaten by 52.9% of blue catfish, Ictalurus furcatus; 48.2% of freshwater drum, Aplodinotus grunniens; and 100% of adult redear sunfish, Lepomis microlophus. Blue catfish showed distinct seasonal prey shifts, feeding on zebra mussels in summer and shad, Dorosoma spp., during winter. Energy content (joules g⁻¹) of blue catfish prey (threadfin shad, Dorosoma petenense; gizzard shad, D. cepedianum; zebra mussels; and asiatic clams, Corbicula fluminea) showed a significant species by season interaction, but shad were always significantly greater in energy content than bivalves examined as either ash-free dry mass or whole organism dry mass. Fish predators significantly reduced densities of large zebra mussels (>5 mm length) colonising clay tiles in the summers of 1997 and 1998, but predation effects on small zebra mussels (≤5 mm length) were less clear. 3. Freshwater drum and redear sunfish process bivalve prey by crushing shells and obtain low amounts of higher-energy food (only the flesh), whereas blue catfish lack a shell-crushing apparatus and ingest large amounts of low-energy food per unit time (bivalves with their shells). Blue catfish appeared to select the abundant zebra mussel over the more energetically rich shad during summer, then shifted to shad during winter when shad experienced temperature-dependent stress and mortality. Native fish predators can suppress adult zebra mussel colonisation, but are ultimately unlikely to limit population density because of zebra mussel reproductive potential.     

Salmonella spp., Vibrio spp., Clostridium perfringens, and Plesiomonas shigelloides in Marine and Freshwater Invertebrates from Coastal California Ecosystems

The coastal ecosystems of California are highly utilized by humans and animals, but the ecology of fecal bacteria at the land–sea interface is not well understood. This study evaluated the distribution of potentially pathogenic bacteria in invertebrates from linked marine, estuarine, and freshwater ecosystems in central California. A variety of filter-feeding clams, mussels, worms, and crab tissues were selectively cultured for Salmonella spp., Campylobacter spp., Escherichia coli-O157, Clostridium perfringens, Plesiomonas shigelloides, and Vibrio spp. A longitudinal study assessed environmental risk factors for detecting these bacterial species in sentinel mussel batches. Putative risk factors included mussel collection near higher risk areas for livestock or human sewage exposure, adjacent human population density, season, recent precipitation, water temperature, water type, bivalve type, and freshwater outflow exposure. Bacteria detected in invertebrates included Salmonella spp., C. perfringens, P. shigelloides, Vibrio cholerae, Vibrio parahaemolyticus, and Vibrio alginolyticus. Overall, 80% of mussel batches were culture positive for at least one of the bacterial species, although the pathogens Campylobacter, E. coli-O157, and Salmonella were not detected. Many of the same bacterial species were also cultured from upstream estuarine and riverine invertebrates. Exposure to human sewage sources, recent precipitation, and water temperature were significant risk factors for bacterial detection in sentinel mussel batches. These findings are consistent with the hypothesis that filter-feeding invertebrates along the coast concentrate fecal bacteria flowing from land to sea and show that the relationships between anthropogenic effects on coastal ecosystems and the environmental niches of fecal bacteria are complex and dynamic.     

Effects of human chorionic gonadotropin (hCG) and handling stress on spermiation of silver perch Leiopotherapon plumbeus (Kner, 1864)

This study determined the effect of human chorionic gonadotropin (hCG) and handling stress on the spermiation and milt response of silver perch Leiopotherapon plumbeus based on the measurement of spermatocrit, sperm density, and milt production. Compared to saline‐injected fish, the mean spermatocrit (or packed sperm) of hCG‐treated fish was significantly lower at 18 h (47.9%) and 30 h (40.2%) post‐injection while mean sperm density was significantly lower at 30 h post‐injection (3.6 × 10⁶ cells μl^?1) but not at 18 h. At 18 h (1.8 μl g‐BW^?1) and 30 h (2.5 μl g‐BW^?1) post‐injection, mean milt production of hCG‐treated fish was significantly higher than in the saline group. Milt consistency was also thinner in the hCG‐treated group. Mean sperm density of handled fish (18.0 × 10⁶ cells μl^?1) was significantly lower than control fish (23.4 × 10⁶ cells μl^?1). However, mean sperm density of handled plus saline‐injected (16.2 × 10⁶ cells μl^?1) and handled plus hCG‐treated fish (8.4 × 10⁶ cells μl^?1) was significantly lower than in the control goup. Having thicker milt consistency, mean spermatocrit and milt production of handled (77.5%; 1.1 μl g‐BW^?1, respectively) and handled plus saline‐injected fish (75.4%; 1.1 μl g‐BW^?1, respectively) were not significantly different from the control fish (76.2%; 1.3 μl g‐BW^?1, respectively). Handled plus hCG‐treated fish had the lowest mean sperm density (8.4 × 10⁶ cells μl^?1) and spermatocrit (54.7%), but had the highest mean milt production (5.5 μl g‐BW^?1) among the treatment groups. These results demonstrate that the hCG injection effectively induces spermiation and milt expression and that handling‐related stress negatively affects such responses. The spermatocrit method may be used to assess the spermiation and milt response of silver perch.     

Vibrio–bivalve interactions in health and disease

In the marine environment, bivalve mollusks constitute habitats for bacteria of the Vibrionaceae family. Vibrios belong to the microbiota of healthy oysters and mussels, which have the ability to concentrate bacteria in their tissues and body fluids, including the hemolymph. Remarkably, these important aquaculture species respond differently to infectious diseases. While oysters are the subject of recurrent mass mortalities at different life stages, mussels appear rather resistant to infections. Thus, Vibrio species are associated with the main diseases affecting the worldwide oyster production. Here, we review the current knowledge on Vibrio–bivalve interaction in oysters (Crassostrea sp.) and mussels (Mytilus sp.). We discuss the transient versus stable associations of vibrios with their bivalve hosts as well as technical issues limiting the monitoring of these bacteria in bivalve health and disease. Based on the current knowledge of oyster/mussel immunity and their interactions with Vibrio species pathogenic for oyster, we discuss how differences in immune effectors could contribute to the higher resistance of mussels to infections. Finally, we review the multiple strategies evolved by pathogenic vibrios to circumvent the potent immune defences of bivalves and how key virulence mechanisms could have been positively or negatively selected in the marine environment through interactions with predators.     

The Effects of Zebra Mussels (Dreissena polymorpha) on the Foraging Success of Eurasian Perch (Perca fluviatilis) and Ruffe (Gymnocephalus cernuus)

Complex habitat structures can influence the foraging success of fish. Competition for food between fish species can therefore depend on the competitors' abilities to cope with structural complexity. In laboratory experiments, we comparatively assessed effects of zebra mussels (Dreissena polymorpha Pall .) on the foraging success of Eurasian perch (Perca fluviatilis L.) and ruffe (Gymnocephalus cernuus (L.)). In single‐species and mixed‐species experiments, the fish were fed caddisfly larvae (Tinodes waeneri (L.)) over complex (mussel‐covered stones) and less‐complex (bare stones) substrates. With intraspecific competition, food consumption by perch and ruffe decreased significantly when the complex substrate was used. With interspecific competition, food consumption by perch and ruffe did not change with substrate complexity, but perch clearly out‐competed ruffe on both substrates. Zebra mussel beds provide a refuge for macrozoobenthos against predation by ruffe and probably also by perch. (© 2004 WILEY‐VCH Verlag GmbH & Co. KGaA, Weinheim)     

Behavioral aspects of host recognition by the symbiotic water mite Unionicola formosa (Acarina,Unionicolidae)

Summary The occurrence and specificity of host recognition behavior of adult and nymphal Unionicola formosa and the capability of adult mites to recolonize various mussel species were examined. Adult U. formosa aggregated on excised tissue from their host mussel, Anodonta imbecilis, in preference to that of two other species of mussels. Nymphs also exhibited an aggregation response to host tissue. A radioisotope (⁵¹Cr) technique was used to monitor the recolonization behavior of U. formosa. Adult female mites preferentially re-entered A. imbecilis rather than the sympatric mussel A. cataracta. The specificity of this behavior parallels the distribution of this water mite among potential bivalve hosts in the southeastern U.S. Host recognition by U. formosa may contribute to re-establishing contact with a host after accidental separation and probably helps to maintain mite-mussel symbioses. Whether or not larval U. formosa employ similar host recognition behavior while selecting a potential host has not as yet been determined.     

Clumping behavior and byssus production as strategies for substrate competition in Mytilus edulis

Laboratory experiments showed that the mussel Mytilus edulis aggregated more intensely around living organisms (the bivalve Hiatella arctica and the solitary ascidian Styela rustica, which commonly co‐occur with mussels in fouling communities) than around inanimate objects. When exposed to an inanimate object, mussels attached their byssal threads primarily to the substrate, close to the object, but when exposed to a living organism, they attached their byssal threads directly to the organism. The ascidian was more intensely covered with byssal threads than was the bivalve. Mussel attachment to the ascidians was apparently determined by the physical characteristics of the tunic and to a lesser extent by the excretion‐secretion products released by S. rustica. This study indicates that mussels can use byssus threads as a means of entrapment of potential competitors for space. It remains unclear why mussels preferentially attached to ascidians compared to the bivalve. This can be explained either by competitive interactions, or by attractiveness of the ascidian tunic as an attachment substratum.     

Non‐specific immunity and disease resistance are enhanced by the polysaccharide fraction of a marine chlorophycean macroalga in Oreochromis niloticus (Linnaeus, 1758)

Polysaccharides (PF) from marine macroalgae, Caulerpa scalpelliformis were extracted and tested for its potential immunostimulatory and disease resistance properties in fish. Five groups of Nile tilapia (n = 6), Oreochromis niloticus (Linnaeus, 1758) were intraperitoneally administered with the different doses of PF (2, 20 or 200 mg/kg body weight) or with yeast‐derived commercial immunostimulant, Macrogard^? (20 mg/kg body weight), to compare the effectiveness. An untreated control group was also maintained. A total of fifteen fibre reinforced plastic tanks (150 L, ambient temperature and light conditions) were used, with triplicate tanks for each group. Only four fish per tank (totally 12 fish from a group) were taken at random and assayed. PF enhanced all the tested non‐specific serum immune responses namely lysozyme, myeloperoxidase, antiprotease, and bactericidal activities. There was an upregulation of the genes encoding IL‐1β, lysozyme and TNF‐α in the spleen of PF injected fish as compared to the control group. In order to study the overall functional immunity, disease resistance test was conducted. Another five groups of fish (n = 10) were treated by intraperitoneal injection with different doses of PF or Macrogard^? or untreated as mentioned earlier in triplicates (30 fish per group in three tanks, totally 150 fish in 15 tanks). Seven days post treatment, fish were challenged by intraperitoneal administration of live virulent Aeromonas hydrophila. PF treated fish were protected with significant reduction in the mortality and the consequent increased relative percent survival (RPS) of 92 in the least (2 mg/kg) and middle dose (20 mg/kg) groups. The disease resistance experiment was repeated again but this time, fish were challenged 21 days post treatment that resulted in RPS of 50 for the middle dose. The results clearly show that the intraperitoneal administration of the polysaccharide fraction had a stimulating effect on the non‐specific immune responses, immune gene expression and disease resistance.     

Hard rock versus soft bottom: the fauna associated with intertidal mussel beds on hard bottoms along the coast of Chile,and considerations on the functional role of mussel beds

The fauna associated with hard bottom mussel beds along the exposed Pacific coast of Chile was examined. The abundance of adult (>10 mm body length) purple mussels Perumytilus purpuratus varied between 32 and 75 individuals per 50 cm², and their biomass between 4.8 and 8.6 g AFDW per 50 cm² at eight sampling sites between Arica (18°S) and Chiloé (42°S). At all sampling sites, the associated fauna was dominated by suspension-feeding organisms (cirripeds, spionid and sabellid polychaetes, a small bivalve) followed by grazing peracarids and gastropods. Predators and scavengers also reached high abundances while deposit- and detritus-feeding organisms were of minor importance. The majority of organisms associated with these hard bottom mussel beds feed on resources obtained from the water column or growing on the mussels rather than on materials deposited by the mussels. This is in contrast to the fauna associated with mussel beds on soft bottoms, which comprises many species feeding on material accumulated by mussels (faeces and pseudofaeces) and deposited within the mussel bed. Many of the organisms dwelling between mussels both on hard bottoms and on soft bottoms have direct development, but organisms with pelagic development also occur abundantly within mussel beds. We propose that species with direct development are disproportionately favoured by the structurally complex habitat with diverse interstitial spaces between the mussels, which provides ample shelter for small organisms. We conclude that mussels on hard-bottoms primarily provide substratum for associated fauna while mussels on soft bottoms provide both substratum and food resources. Electronic Publication     

The role of local adaptation in shaping fish‐mussel coevolution

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Restoring the endangered oyster mussel (Epioblasma capsaeformis) to the upper Clinch River,Virginia: an evaluation of population restoration techniques

From 2005 to 2011, the federally endangered freshwater mussel Epioblasma capsaeformis (oyster mussel) was reintroduced at three sites in the upper Clinch River, Virginia, using four release techniques. These release techniques were (1) translocation of adults (site 1, n = 1418), (2) release of laboratory‐propagated sub‐adults (site 1, n = 2851), (3) release of 8‐week‐old laboratory‐propagated juveniles (site 2, n = 9501), and (4) release of artificially infested host fishes (site 3, n = 1116 host fishes). These restoration efforts provided a unique research opportunity to compare the effectiveness of techniques used to reestablish populations of extirpated and declining species. We evaluated the relative success of these four population restoration approaches via monitoring at each release site (2011–2012) using systematic 0.25‐m² quadrat sampling to estimate abundance and post‐release survival. Abundances of translocated adult and laboratory‐propagated sub‐adult E. capsaeformis at site 1 ranged 577–645 and 1678–1700 individuals, respectively, signifying successful settlement and high post‐release survival. Two untagged individuals (29.1 and 27.3 mm) were observed, indicating that recruitment is occurring at site 1. No E. capsaeformis were found at sites where 8‐week‐old laboratory‐propagated juveniles (site 2) and artificially infested host fishes (site 3) were released. Our results indicate that translocations of adults and releases of laboratory‐propagated sub‐adults were the most effective population restoration techniques for E. capsaeformis. We recommend that restoration efforts focus on the release of larger (>20 mm) individuals to accelerate augmenting and reintroducing populations and increase the probability for recovery of imperiled mussels.     

Age,growth and reproduction of the black sea bream Spondyliosoma cantharus (Linnaeus, ) (Sparidae) in the Gulf of Annaba (Algeria)

The objective of this study was to determine the basic population‐specific parameters necessary for fish stock assessment in the Gulf of Annaba and to compare these with data from other Mediterranean regions. Black sea bream Spondyliosoma cantharus (Linnaeus, 1758) (N = 501) were collected monthly from January to December 2008 along the Algerian eastern coasts. More than 22 fish were collected each month and ranged in size from 13.4 to 40 cm total length, weighing from 36 to 1080 g eviscerated weight. Biological sampling included weighing and measuring the fish, gonad weighing, sex and maturity stage determination, and age estimation through otolith readings. Validity of the otolith readings for estimating age and growth was supported using the back‐calculation method. Estimated parameters of the von Bertalanffy model are: L_∞ = 33.54 cm, W_∞ = 633.46 g, k = 0.52 year^?1 and t_o = ?0.04 year. The growth performance index (φ) is: 2.76. The length‐weight relationship is: EW = 4.4.10^?6 TL^3.23. The spawning period occurred from February to May, while the gamete emission peaked in April. Females reached sexual maturity at 19.3 cm (2 years) and males at 21.3 cm (3 years). Sexual inversion occurs at approximately 24.3 cm. Spondyliosoma cantharus was characterized as being a protogynic hermaphrodite.