Mechanisms and impact of differential fouling of the zebra mussel Dreissena polymorpha on different unionid bivalves

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The role of host specificity in explaining the invasion success of the freshwater mussel Anodonta woodiana in Europe

Several freshwater mussel species represent some of the most problematic invasive species and have considerably altered ecosystems worldwide. Their invasion potential has been partially attributed to their free-living larvae, which have a high dispersal capability. We investigated the invasion potential of Anodonta (Sinanodonta) woodiana, a species of East Asian unionid mussel established worldwide despite having an obligatory parasitic stage (glochidium), which must encyst on host fish. The invasion success of A. woodiana has been attributed to the success of worldwide introductions of its sympatric fish hosts. We experimentally found, however, that A. woodiana is a broad host generalist, which can complete its development on all eight fish species tested, both coinvasive and native. Subsequently, we used a data on the occurrence and relative abundance of potential hosts in river habitats in the Czech Republic to project scenarios of the effect of host availability on A. woodiana invasion. We found that host availability does not constitute a major limit for A. woodiana to colonise most aquatic habitats in Central Europe. In addition, we investigated seasonal dynamics of A. woodiana reproduction and did not detect any limitations of its reproduction by ambient water temperatures typical of a Central European lowland river. Consequently, we predict that A. woodiana may further increase the speed and range of its invasion and we discuss possible consequences to native habitats and communities, especially to the endangered species of unionid mussels.     

The role of local adaptation in shaping fish‐mussel coevolution

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Sympatric variability of isotopic baselines influences modeling of fish trophic patterns

Stable isotope signatures of freshwater snails and mussels have been established as a convenient baseline measurement at the primary consumer level for food-web coupling studies. We measured δ¹⁵N and δ¹³C of primary consumers, including mussels (Anodonta woodiana, Cristaria plicata, and Unio douglasiae), snails (Bellamya aeruginosa and Hippeutis sp.), and zooplankton from the same habitat within a shallow eutrophic lake. Primary consumers showed positive relationship between δ¹⁵N and δ¹³C, indicating a linkage between planktonic and benthic habitats in this system. The variation in isotope ratios was higher in short-lived primary consumers (zooplankton) compared with the long-lived primary consumers (mussels and snails), suggesting limited availability of short-lived primary consumers as isotopic baselines in aquatic food-web assessment. Significant differences in isotope ratios were also found among three species of mussels, and when using these mussels separately as pelagic baselines to calculate trophic position and contribution of planktonic and benthic sources of fishes, bias and even misestimates were observed. This finding suggests that caution is needed when multiple primary consumers coexist in the same habitat, and it is important to assess potential effects of different baselines used.     

Population-specific responses to an invasive species

Predicting the impacts of non-native species remains a challenge. As populations of a species are genetically and phenotypically variable, the impact of non-native species on local taxa could crucially depend on population-specific traits and adaptations of both native and non-native species. Bitterling fishes are brood parasites of unionid mussels and unionid mussels produce larvae that parasitize fishes. We used common garden experiments to measure three key elements in the bitterling–mussel association among two populations of an invasive mussel (Anodonta woodiana) and four populations of European bitterling (Rhodeus amarus). The impact of the invasive mussel varied between geographically distinct R. amarus lineages and between local populations within lineages. The capacity of parasitic larvae of the invasive mussel to exploit R. amarus was higher in a Danubian than in a Baltic R. amarus lineage and in allopatric than in sympatric R. amarus populations. Maladaptive oviposition by R. amarus into A. woodiana varied among populations, with significant population-specific consequences for R. amarus recruitment. We suggest that variation in coevolutionary states may predispose different populations to divergent responses. Given that coevolutionary relationships are ubiquitous, population-specific attributes of invasive and native populations may play a critical role in the outcome of invasion. We argue for a shift from a species-centred to population-centred perspective of the impacts of invasions.     

Physical forces constrain the depth distribution of the abundant native mussel Elliptio complanata in lakes

1. Unionid mussels often account for a large portion of benthic biomass and contribute to nutrient cycling and sediment processes, but are thought to be limited to shallow areas (<2–3 m). 2. The depth distribution and body size of Elliptio complanata were compared in seven Canadian Shield lake basins of different sizes to test what factors determine the upper and lower limit of their depth range. Specifically, I tested whether (i) the upper range of their distribution is limited by exposure to winds and wave action and (ii) the lower range of their distribution is limited by the depth of the thermocline or by the boundary of mud deposition. 3. The average depth distribution of E. complanata shifted to greater depths in larger lake basins. When comparing individual transects, maximum mussel density was found deeper at more exposed sites. Mussel size decreased with increasing depth and was larger, on average, in larger lake basins. These results suggest that physical forces limit the upper range of mussel distribution in lakes. 4. The maximum depth at which mussels were found in different lakes was closely related to thermocline depth. However, mussels were commonly observed below the predicted depth of the mud deposition boundary. The thermocline limits the lower range of mussel distribution in lakes, probably by limiting food availability and by determining water temperature. Substratum type does not limit the lower distribution of mussels. 5. These results suggest that unionid mussels are present in the deeper parts of the littoral zone, especially in large lakes. Therefore, comparisons of mussel populations between sites and between lakes would be biased unless the full depth distribution of these mussels is considered. These results also suggest that long‐term changes in the thermal structure of lakes could affect the range of unionid mussel populations and their functional role in littoral ecosystems.     

Potential effects on zooplankton from species shifts in planktivorous mussels: a field experiment in the St Lawrence River

1. Suspension feeding by bivalves exceeds that by other planktivores in many North American rivers, and food webs may be altered substantially by differences in feeding patterns between native unionid mussels and invading dreissenid mussels. 2. We conducted an experiment comparing zooplanktivory by one unionid and two dreissenid species that addressed several primary questions. Is benthic planktivory important in this river? Has this linkage been altered substantially by dreissenids? Do the two dreissenid species differ in planktivory, and is this ecologically important if quagga mussels extend their geographical range? 3. Our 12‐day experiment consisted of controls (no mussels) and treatments with unionid (Elliptio complanata), quagga (Dreissena bugensis) or zebra (D. polymorpha) mussels in 3500‐L, 80‐μm mesh enclosures placed in a slackwater area of the St Lawrence River. 4. The density of the most abundant calanoid copepod Eurytemora affinis increased in the presence of dreissenids, probably as an indirect food web response. By day 12, a cumulative effect was shown by the most overwhelmingly abundant rotifer, Polyarthra, whose density declined dramatically in dreissenid enclosures compared with control and unionid enclosures. Rotifer densities in unionid enclosures were not different from controls, nor were dreissenid treatments different from each other. The effects on rotifers were probably from predation, as Chl‐a did not vary among treatments. 5. We conclude that benthic‐pelagic coupling via planktivory is important in slackwater areas. Dreissenids have strengthened this linkage, but range extension of quaggas should not appreciably alter effects produced by a similar biomass of zebra mussels.     

Grazing effects of a freshwater bivalve (Corbicula leana Prime) and large zooplankton on phytoplankton communities in two Korean lakes

This study examined the effects of a freshwater filter feeding bivalve (Corbicula leana Prime) and large zooplankton (>200 μm, mostly cladocerans and copepods) on the phytoplankton communities in two lakes with contrasting trophic conditions. A controlled experiment was conducted with four treatments (control, zooplankton addition, mussel addition, and both zooplankton and mussel addition), and each established in duplicate 10-l chambers. In both lakes there were significant effects of mussel grazing on phytoplankton density and biomass. The effects were greater in mesotrophic Lake Soyang than in hypertrophic Lake Ilgam. Effects of zooplankton grazing did not differ between these lakes, and zooplankton effects on phytoplankton were much less than the effects of mussels. Although mussels exerted a varying effect on phytoplankton according to their size, mussels reduced densities of almost all phytoplankton taxa. Total mean filtering rate (FR) of mussels in Lake Soyang was significantly greater than that in Lake Ilgam (p=0.002, n=5). Carbon fluxes from phytoplankton to mussels (977–2,379 μgC l^?1d^?1) and to zooplankton (76–264 μgC l^?1 d^?1) were always greater in Lake Ilgam due to the greater phytoplankton biomass (p<0.01, n=6). Based on the C-flux to biomass ratios, the mussels consumed 170–754% (avg. 412%) of phytoplankton standing stock in Lake Soyang, and 38–164% (avg. 106%) in Lake Ilgam per day. The C-flux to biomass ratio for mussels within each lake was much greater than for large zooplankton. Mussels reduced total phosphorus concentration by 5–34%, while increasing phosphate by 30–55% relative to the control. Total nitrogen also was reduced (by 9–25%), but there was no noticeable change in nitrate among treatments. The high consumption rate of phytoplankton by Corbicula leana even in a very eutrophic lake suggests that this mussel could affect planktonic and benthic food web structure and function by preferential feeding on small seston and by nutrient recycling. Control of mussel biomass therefore might be an effective tool for management of water quality in shallow eutrophic lakes and reservoirs in Korea.     

Cadmium Accumulation and Metallothionein Biosynthesis in Cadmium-Treated Freshwater Mussel Anodonta woodiana

This study investigated the distribution of cadmium (Cd) and the protein level of metallothionein (MT) and examined the relationship of Cd accumulation and the MT concentration in different tissues of freshwater mussel Anodonta woodiana following Cd treatment. The mussels were exposed to Cd (4.21, 8.43, 16.86, 33.72 and 67.45 mg L^-1) for 24, 48, 72 and 96 h, respectively. After Cd treatment, the gills, mantle, foot, visceral mass and digestive gland tissues were collected for analysis. We found that, in the controls, Cd distributed in all tissues in the concentration order of gills>mantle>foot>visceral mass>digestive gland. Upon Cd treatment, Cd concentration significantly increased in all tissues. The highest Cd accumulation was found in the digestive gland, which was 0.142 mg g^-1 (P<0.05). MT levels in the gills and mantle of the mussels increased significantly (P<0.05), which were in positive correlation with Cd accumulation in the tissues (P<0.05). In conclusion, our results demonstrated a correlation between Cd accumulation and MT up-regulation in gills and mantle of the mussels after Cd treatment. It is suggested that the protein level of MT in gills and mantle of Anodonta woodiana is a good biomarker for Cd contamination.     

Valve movement of the freshwater mussel Anodonta anatina: a reciprocal transplant experiment between lake and river

The effects of source and caging on the valve movements of the freshwater unionid mussel (Anodonta anatina) were studied in a reciprocal transplant experiment between a lake and its outflow. Caged mussels were moved and compared with those remaining in their natural environment on the lake or river bottom. At both sites, the mussels from the study site and the transplanted mussels from the opposite site were monitored simultaneously. In river the averaged weighted valve openness was higher and the number of valve movements was lower than in the lake. The mussels monitored in the lake exhibited a diurnal rhythm of valve movements which differed between the lake-bottom and the caged animals. Caging was found to increase valve openness. On the other hand, little variation appeared in valve openness between caged and bottom animals in the river, where diurnal rhythms were almost nonexistent. In the river the valve movements were more variable in respect to time than in the lake.     

Energy exploitation in Chirocephalus croaticus (Steuer, 1899) (Crustacea: Anostraca): survival strategy in an intermittent lake

Electron transport system (ETS) activity was measured in Chirocephalus croaticus from the intermittent lake, Petelinjsko Jezero. The ETS activities were measured at 5, 10, 15, 20, and 25 °C, and were studied separately in juveniles, females and males. Juveniles had significantly higher activity than adults at a standard temperature of 20 °C. The mass-specific ETS activity decreased with increasing size of the animals; the value b was 0.787. Respiration rates (R) were determined at 20 °C and the ratio ETS/R (±standard deviation) for C. croaticus was 1.43±0.46 (n=38). ETS activity increased with temperature. Females had higher Q₁₀ than males in higher temperature range (t-test; t=2.50; d.f.=8; p<0.05). Activation energy E_a was higher for females than males (t-test; t=2.35; d.f.=8; p<0.05). Females exhibited lower ETS activity than males over the lower temperature range, but their ETS could function more efficient at higher temperature.     

Impact of Dreissena fouling on the physiological condition of native and invasive bivalves: interspecific and temporal variations

The impact of Dreissena fouling on unionids has hardly been studied in Europe, despite the fact that in some ecosystems (e.g. Lake Balaton, Hungary) infestations of several hundreds to a thousand individuals per unionid have been observed. At present, the zebra mussel Dreissena polymorpha is a dominant species in Lake Balaton and in the last decade three other invasive bivalves were introduced, potentially increasing the pressure on native unionid survival. We examined whether the fouling of dreissenids (zebra and quagga (D. rostriformis bugensis) mussels) has a negative impact on native (Anodonta anatina, Unio pictorum and U. tumidus) and invasive (Corbicula fluminea and Sinanodonta woodiana) bivalves and whether there are any interspecific and temporal variations in fouling intensity and physiological condition measured by standard condition index and glycogen content. A significant negative impact was detected on native unionids only in July and September (no impact was detected in May), when the fouling rate was high. For invasive species, a significant negative impact was detected on S. woodiana with a high level of dressenid infestation; whereas no significant impact was detected on C. fluminea. Overall, this study confirms that Dreissena may threaten unionid species including the invasive S. woodiana, although high interspecific and temporal variations were observed. This situation should be taken into account in future ecological and conservational assessments because species respond differently to Dreissena fouling and effects seem to be more pronounced in late summer/early autumn. In addition, this study provides the first evidence that the invasive C. fluminea appear to be less vulnerable to dressenid fouling.     

An indirect effect of biological invasions: the effect of zebra mussel fouling on parasitisation of unionid mussels by bitterling fish

Invasive species represent a major threat with both direct and indirect effects on natural ecosystems, including effects on established and coevolved relationships. In a series of experiments, we examined how the interaction between two native species, a unionid mussel (Unio pictorum) and the European bitterling (Rhodeus amarus), a fish that parasitises unionids, was affected by the non-native zebra mussel (Dreissena polymorpha). The zebra mussel fouls hard substrates, including shells of living unionids, and its presence is often associated with a decrease in population density of native unionid mussels. Bitterling lay their eggs into live unionids and the embryos develop inside their gills. Using a range of zebra mussel densities, we demonstrated that zebra mussel fouling had a negative effect on the number of bitterling eggs inside the mussel host, with abundances of 5–10 zebra mussels (shell size 15–25 mm) per unionid critical for bitterling ability to utilise the host. In a further experiment, we found that bitterling did not discriminate between unfouled unionids and those fouled with five zebra mussels. Most ovipositions into fouled hosts, however, were unsuccessful as eggs failed to reach the unionid gills. We discuss implications of such unsuccessful ovipositions for bitterling recruitment and population dynamics.     

Invasive zebra mussel (Dreissena polymorpha) threatens an exceptionally large population of the depressed river mussel (Pseudanodonta complanata) in a postglacial lake

1. Freshwater mussels are in decline worldwide, with the depressed river mussel Pseudanodonta complanata being one of the rarest and most endangered species in Europe. Invasive mussels are suspected to be an important factor of decline, but there is little information on their interaction with native species.
2. This study analyzed densities, depth distribution, and individual sizes and weights in one of the largest known populations of P. complanata in Europe in relation to the co‐occurring invasive zebra mussel Dreissena polymorpha and other mussel species, using a systematic transect analysis.
3. Pseudanodonta complanata was the dominant unionid species in Lake Siecino reaching densities of up to 26 ind/m², with half of the specimens found at a water depth of 2.0–4.0 m. Densities were highest on sandy substrates in areas of underwater currents. In contrast, 67% of native Unio tumidus were found at depths < 1 m, indicating different habitat preference.
4. In the study area, 91% of P. complanata, 92% of U. tumidus, and all Anodonta individuals were fouled by D. polymorpha. The dreissenid:unionid mass ratio (mean ± SD; maximum) was 0.43 ± 0.56; 4.22 and 0.86 ± 1.87; 8.76 in P. complanata and U. tumidus, respectively. Pseudanodonta complanata fouled with D. polymorpha were impaired in their anchoring capability and had shell deformations potentially affecting shell closing and filtration activity. Fouling intensity was negatively correlated with unionid density, potentially leading to accelerated population declines.
5. The observed adverse effects of invasive zebra mussels on the depressed river mussel and the difficulties in eradicating established populations of invasive mussels suggest that D. polymorpha should be considered a serious threat to P. complanata. Therefore, the further spread of zebra mussels into habitats with native unionids needs to be avoided by all means.

     

Noninvasive assessment of cardiac contractility by using (dP/dt)/P of carotid artery pulses during exercise

In earlier studies we have shown that both the pressure (P) of the carotid artery pulse (CAP) and its first derivative (CAP dP/dt) could be recorded during moderate exercise. To establish that the CAP (dP/dt)/P is a noninvasive substitute for the left ventricular (LV) value, LV (dP/dt)/P, an index of cardiac contractility, we studied CAP (dP/dt)/P under various states of activity in the autonomic nervous system in 12 healthy male subjects. Increased sympathetic nerve activities yielded by passive tilting, emotional load, or cold stress increased CAP (dP/dt)/P significantly (P< 0.05). Increased parasympathetic nerve activity by ocular compression, however, did not significantly affect the value. Moderate exercise at a heart rate of approximately 150 beats·min^–1 increased it significantly from 16.7 to 25.2·s^–1 in a supine position (P<0.001) and from 16.6 to 24.8·s^–1 in an upright position (P<0.001). It increased monotonically as heart rate increased, but the slope was steeper when the heart rate was greater than approximately 100 beats·min^–1 than it was when the rate was less than 100 beats·min^–1. In conclusion, the present study indicated that CAP (dP/dt)/P can be used as a noninvasive index of cardiac contractility even in moderate exercise.     

Analysis of VH gene diversity in rainbow trout (Oncorhynchus mykiss): both nonsynonymous and synonymous nucleotide changes are more frequent in CDRs than in FRs

 Forty-six immunoglobulin VH gene sequences of rainbow trout were compiled to analyze the extent of variations and the frequency of nucleotide changes in CDRs and FRs. The results show that the frequency of nonsynonymous (amino acid replacing) changes (Ka) are on average 4.9 times higher in complementarity determining regions (CDRs) than in FRs, thus contributing more diversity in CDRs. Unexpectedly, however, the frequency of synonymous (silent) changes (Ks) show the same tendency: it was 5.3 times higher in CDRs than in framework regions (FRs). The distribution of Ks/Ka ratios of each comparison shows no segregation between CDRs and FRs. The same analysis applied to five germline VH genes of Heterodontus francisci shows the same result as was found with the rainbow trout. In contrast, the results from mouse data show that, while the CDR/FR ratio for Ka is much higher (7.4), the CDR/FR ratio for Ks is only slightly higher (1.8). The distribution of Ks/Ka ratios in mouse indicates clear segregation between CDRs and FRs. This suggests that CDR germline diversity is largely generated by gene conversion in VHs of lower vertebrates such as rainbow trout or shark. This mechanism might be advantageous to lower vertebrates in generating V gene diversity faster than other mechanisms such as point mutation and selection. Received: 10 July 1996 / Revised: 9 September 1996     

毛状副冠对高山植物喉毛花的适应意义

高山地区生境极端,却拥有许多形态特化的植物,非生物因素在塑造花部性状及其进化过程中发挥着重要作用。该研究选取龙胆科典型高山植物喉毛花(Comastoma pulmonarium)为对象,探究其毛状副冠在多雨、强辐射的极端高山环境中的适应意义及其对植物雌雄繁殖适合度的影响。结果表明:通过比较自然状态和人工去除副冠的花,毛状副冠有效减少了雨水对花粉的冲刷(t=2.61,P0.05),提高了受精比率(t=2.05,P0.05),但是对种子的质量,即种子重量和种子萌发率的影响不显著。另外,花粉浸泡在蒸馏水中后,其萌发率显著低于蔗糖溶液中(t=30.67,P0.001),表明毛状副冠能够有效减小雨水浸泡对花粉活力的影响;同时,与自然状态相比,去除毛状副冠后的花,经太阳暴晒后,其花粉萌发率同样极显著地降低(t=9.89,P0.001),表明毛状副冠有效地避免了太阳辐射对花粉质量产生的不利影响。该研究结果表明喉毛花的毛状副冠结构是应对高山恶劣环境的一种适应策略,对植株的雌性和雄性繁殖成功都具有重要意义,从而进一步证实了非生物因素在植物花部特征演化中的重要作用。     

Growth chronologies of white sucker, Catostomuscommersoni, and lake trout, Salvelinusnamaycush: a comparison among lakes and between trophic levels

A growth chronology index was used to determine whether changes in ecosystem structure and function in lakes could be associated with fish growth histories. Growth chronologies were compared for white suckers, Catostomus commersoni, from Little Moose (oligotrophic), Oneida (eutrophic), and Cayuga (mesotrophic) lakes (New York) from opercular bone growth increments, and for lake trout, Salvelinus namaycush, from Little Moose Lake using otolith growth. The longevity of these species allowed the development of chronologies from 17 to 33 years in length using only contemporary collections. We used these chronologies to examine whether fish growth histories could be used as an index for ecosystem-scale changes. Specifically, we examined whether zebra mussel, Dreissena polymorpha, invasion in Oneida and Cayuga lakes in the early 1990s, and treatment of sewage effluent from dwellings around Little Moose Lake beginning during the late 1980s could be detected in white sucker and lake trout growth chronologies. White sucker growth in Oneida and Cayuga Lakes did not differ before and after zebra mussel invasions. Neither white sucker nor lake trout growth chronologies from Little Moose Lake reflect changes in growth expected with reduced productivity levels associated with improved sewage treatment. Growth chronologies of these two species did not detect the ecosystem-scale changes that occurred in the study lakes.     

Predation by the invasive American signal crayfish, Pacifastacus leniusculus Dana, on the invasive zebra mussel, Dreissena polymorpha Pallas: the potential for control and facilitation

Non-indigenous crayfish often have major ecological impacts on invaded water bodies, and have contributed to the decline of native crayfish species throughout Europe. The American signal crayfish, Pacifastacus leniusculus, is the most widespread invasive crayfish in Great Britain, where the zebra mussel, Dreissena polymorpha, is similarly an invasive pest species. The potential for the American signal crayfish to regulate zebra mussel populations was investigated through a series of laboratory experiments. Crayfish were found to be highly size selective, consuming significantly more of the smallest size class of zebra mussels offered (7–12 mm), over medium (16–21 mm) and large (25–30 mm). Crayfish feeding rate on zebra mussels was not altered when mussels were presented clumped together in natural druses compared with mussels in a disassembled druse. Crayfish spent significantly more time foraging when mussels were unattached, and a greater proportion of attacks were on medium and large than on small mussels (83% of attacks were on medium and large mussels when unattached as opposed to 47% when on druses). Individual crayfish feeding rate decreased significantly at densities of > ~5 crayfish m⁻². Signal crayfish are, therefore, unlikely to be able to significantly impact established populations of zebra mussels in the wild, although zebra mussels have the potential to provide crayfish with a substantial food source.