Persistence of host response against glochidia larvae in Micropterus salmoides

Host fish acquire resistance to the parasitic larvae (glochidia) of freshwater mussels (Unionidae). Glochidia metamorphose into juvenile mussels while encysted on host fish. We investigated the duration of acquired resistance of largemouth bass, Micropterus salmoides (Lacepède, 1802) to glochidia of the broken rays mussel, Lampsilis reeveiana (Call, 1887). Fish received three successive priming infections with glochidia to induce an immune response. Primed fish were held at 22-23 degrees C and were challenged (re-infected) at intervals after priming. Metamorphosis success was quantified as the percent of attached glochidia that metamorphosed to the juvenile stage and were recovered alive. Metamorphosis success at 3, 7, and 12 months after priming was significantly lower on primed fish (26%, 40%, and 68% respectively) than on control fish (85%, 93%, and 92% respectively). A second group of largemouth bass was similarly primed and blood was extracted. Immunoblotting was used to detect host serum antibodies to L. reeveiana glochidia proteins. Serum antibodies were evident in primed fish, but not in naive control fish. Acquired resistance of host fish potentially affects natural reproduction and artificial propagation of unionids, many of which are of conservation concern.     

Acquired resistance of bluegill sunfish Lepomis macrochirus to glochidia larvae of the freshwater mussel Utterbackia imbecillis (Bivalvia: Unionidae) after multiple infections

The effects of multiple infections on the host-parasite relationship between bluegill sunfish (Lepomis macrochirus) and parasitic glochidial larvae of the freshwater mussel Utterbackia imbecillis were examined. Na?ve, young-of-the-year bluegills were infected with glochidia and placed in individual observation chambers. Each day, water was drained from each chamber and the numbers of dead glochidia, live glochidia, partially metamorphosed glochidia, and fully metamorphosed juvenile mussels were counted. The same fishes were infected a total of 4 times. After 2 infections, the fish began to exhibit evidence of acquired resistance to glochidia. During the third and fourth infections, this resistance was clearly evidenced by the marked increase in the percentage of dead and live glochidia shed during the first 5 days of the infection and by the significant decrease in the success of metamorphosis. The total number of glochidia that successfully attached to the fish decreased significantly during the fourth infection relative to the first. The number of larvae attached to the host fish was positively correlated with the size of the fish during the first infection but was negatively correlated during all subsequent infections. Variance to mean ratios indicated that larvae were aggregated among host fishes during the infections. This study has important implications in propagation and conservation efforts of this endangered group of organisms.     

Encapsulation of attached ectoparasitic glochidia larvae of freshwater mussels by epithelial tissue on fins of naive and resistant host fish

To metamorphose into juveniles and subsequently mature into adults, the glochidia larvae of freshwater mussels in the order Unionoida must temporarily parasitize the gills, fins, or other external structures of fish. Once attached to the fish, the glochidium is encapsulated by host fish epithelial tissue. The migration of epithelial cells of the bluegill sunfish Lepomis macrochirus over glochidia of Utterbackia imbecillis was examined by time-lapse video microscopy, and the morphology was examined by scanning electron microscopy. Initially, the leading edge epithelial cells migrating over the larvae became rounded and the cells moved as a sheet until the attached glochidium was completely covered. Cyst formation on host fish that had been repeatedly exposed to mussel larvae was significantly delayed and morphologically irregular compared to that on na?ve fish. Cyst formation on other species of fish that are less successful as hosts was examined. In general, it took longer for glochidia to become encapsulated on these less suitable potential hosts. The delay and irregularities in cyst formation on resistant fish and nonhost fish species may result in increased mortality and reduced success of metamorphosis of glochidia.     

Influence of cortisol on the attachment and metamorphosis of larval Utterbackia imbecillis on bluegill sunfish (Lepomis macrochirus)

The larvae of unionid freshwater mussels (i.e., glochidia) undergo a parasitic stage requiring their attachment to the external epithelia of fish hosts, where they metamorphose into free-living juveniles. We describe the physiological effects in bluegill sunfish (Lepomis macrochirus) of infection with glochidia from the paper pondshell (Utterbackia imbecillis). Glochidia accumulation on bluegill increased dramatically at concentrations of 2000 glochidia liter(-1) and above, reaching a maximum attachment density of about 30 glochidia g(-1) fish at 4000 glochidia liter(-1). Plasma cortisol was the most sensitive indicator of biological effect to glochidial exposure, increasing significantly in hosts exposed to 2000 glochidia liter(-1) or greater. Glochidia were 31% more likely to undergo successful juvenile metamorphosis when attached to bluegill with elevated plasma cortisol, largely due to the enhanced survivorship of these larvae during the first 48 h after infection. We tested the hypothesis that glochidial attachment and juvenile metamorphosis were stimulated directly by plasma cortisol in fish hosts. Bluegill were given an intraperitoneal injection of cortisol, then infected with 1000 glochidia liter(-1) at 48 h after hormone supplementation. Cortisol-injected fish had a 42% increase in the number of attached glochidia g(-1) fish and a 28% increase in larval metamorphosis compared to sham-injected and control fish. We provide evidence that cortisol enhances glochidial metamorphosis on hosts by improving the retention of attached glochidia. This study gives insights into the influence of host physiology on glochidial attachment and juvenile mussel transformation.     

三角帆蚌钩介幼虫在两种寄主鱼上的寄生效果及其对寄主鱼血浆生化指标的影响

利用黄颡鱼(Pelteobagrus fulvldraco)、尼罗罗非鱼(Tilapia nilotica)对三角帆蚌(Hyriopsis cumingii)钩介幼虫进行了寄生实验,分析了幼虫在寄主鱼上的寄生周期和脱落数量与寄主种类、寄主鱼单尾体重的相关关系.以未寄生幼虫的罗非鱼为空白对照,测定分析了罗非鱼在幼虫寄生前、脱落后主要血浆生化指标的变化.实验结果显示:黄颡鱼、罗非鱼平均每千克体重脱落稚贝的数量分别为(26 435±6 430)只、(26 327±3 091)只,两种寄主鱼间不存在显著差异;脱落的稚贝数量随着寄主鱼体重的增加而增加,并呈显著线性相关.在水温(24±1)℃条件下,黄颡鱼组、罗非鱼组的稚贝脱落高峰分别出现在寄生后的第8 d、第7 d,罗非鱼组表现为明显的"早脱落"现象.罗非鱼在寄生前后血浆总蛋白(TP)、白蛋白(Alb)、总糖(Glu)、总胆固醇(Tc)和高密度脂蛋白(HDL)含量均未出现显著变化,而血浆甘油三酯(TG)、低密度脂蛋白(LDL)含量显著下降(P=0.001,0.020).未寄生组罗非鱼的7项指标均未出现明显变化.实验结果将为三角帆蚌钩介幼虫变态发育相关营养因子的探讨提供理论参考.     

Physiological and ecological hosts of Popenaias popeii (Bivalvia: Unionidae): laboratory studies identify more hosts than field studies

1. Freshwater mussels are critically endangered in North America, making it important to understand their environmental requirements at all life stages. As glochidia (larvae), they attach to fish hosts where they undergo substantial mortality, making this transition important in their life cycle. Larval host fish requirements have typically been described using data from laboratory infestations to determine suitable hosts. 2. Laboratory infestations circumvent many natural barriers that prevent infestation of physiologically compatible fishes by mussel larvae. While such methods are invaluable for identifying ‘physiological hosts,’ they cannot fully describe realised ‘ecological hosts’ in the field. 3. We studied Popenaias popeii in the Black River in New Mexico, because it is of conservation concern and it is the only mussel species present, facilitating identification of glochidial infestation. To explore the difference between physiological hosts and ecological hosts, we conducted a 3‐year field study of fishes infested by P. popeii glochidia. 4. Substantially fewer fish species were infested by P. popeii in the wild (10 of 20 observed) than had been identified as physiological hosts in laboratory trials (24 of 31). We combined data on fish abundance, proportion of fish hosts infested (prevalence) and the number of glochidia per fish (intensity) and identified three fish species that probably contributed substantially more to mussel recruitment by carrying more glochidia than other host species. 5. Similarities in behaviour among these fishes allowed us to hypothesise routes of infestation, such as benthos‐feeding by catostomids, that allow glochidia to infest these hosts at higher rates than other suitable hosts. Overall, this approach provides a method of quantifying the relative importance of different species of host fish in the mussel lifecycle.     

Mantle displays of freshwater mussels elicit attacks from fish

1. Gravid females of some North American freshwater mussel species (Bivalvia: Unionidae) display highly modified mantle margins and other reproductive structures which mimic small fish, terrestrial insects, or aquatic macro-invertebrates. We report the responses of fish to these lures, based on the results of laboratory encounters between the following pairs of displaying mussels and fishes: Lampsilis cardium and Micropterus coosae; L . perovalis and M . coosae; and Villosa nebulosa and Percina nigrofasciata . In all three encounters, the lures elicited attacks from fish.
2. Encounters between Lampsilis spp. and M. coosae resulted in gill infestations of the fish by larval mussels, which are obligate parasites on fish. An encounter between V . nebulosa and P . nigrofasciata did not result in infestation.
3. The use of these lures to attract fish may greatly increase the chances of parasite/host encounters and may also reduce the chances of infestation of unsuitable hosts.     

THE BITTERLING–MUSSEL COEVOLUTIONARY RELATIONSHIP IN AREAS OF RECENT AND ANCIENT SYMPATRY

Host–parasite relationships are often characterized by the rapid evolution of parasite adaptations to exploit their host, and counteradaptations in the host to avoid the costs imposed by parasitism. Hence, the current coevolutionary state between a parasite and its hosts is predicted to vary according to the history of sympatry and local abundance of interacting species. We compared a unique reciprocal coevolutionary relationship of a fish, the European bitterling (Rhodeus amarus) and freshwater mussels (Unionidae) between areas of recent (Central Europe) and ancient (Turkey) sympatry. Bitterling parasitize freshwater mussels by laying their eggs in the gills of mussel and, in turn, mussel larvae (glochidia) parasitize the fish. We found that all bitterling from both regions avoided one mussel species. Preferences among other mussel species tended to be related to local mussel abundance rather than duration of sympatry. Individual fish were not consistent in their oviposition choices, precluding the evolution of host‐specific lineages. Mussels were demonstrated to have evolved strong defenses to bitterling parasitism in the area of ancient sympatry, but have no such defenses in the large areas of Europe where bitterling are currently invasive. Bitterling avoided glochidia infection irrespective of the duration of sympatry.     

The role of local adaptation in shaping fish‐mussel coevolution

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

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Population dynamics of glochidia of the freshwater pearl mussel Margaritifera margaritifera L., parasitizing on juvenile Salmonidae fishes in northern water reservoirs

This paper presents data on the population dynamics of glochidia of the freshwater pearl mussel Margaritifera margaritifera L. (1758) (a declining species of European fauna), parasitizing on juvenile Salmonidae fishes in rivers of northern Europe. It was found that the number of glochidia parasitizing on gills of juvenile salmon and trout in explored water reservoirs are stimulated by negative binomial distribution. Estimation of the distribution parameter allows us to obtain statistically valid data on the population number of pearl mussel and to judge the stable character of interactions in the host-parasite system (balance of host specimens that are resistant and nonresistant to infection).     

Evolution of active host-attraction strategies in the freshwater mussel tribe Lampsilini (Bivalvia: Unionidae)

Most freshwater mussels (Bivalvia: Unionoida) require a host, usually a fish, to complete their life cycle. Most species of mussels show adaptations that increase the chances of glochidia larvae contacting a host. We investigated the evolutionary relationships of the freshwater mussel tribe Lampsilini including 49 of the approximately 100 extant species including 21 of the 24 recognized genera. Mitochondrial DNA sequence data (COI, 16S, and ND1) were used to create a molecular phylogeny for these species. Parsimony and Bayesian likelihood topologies revealed that the use of an active lure arose early in the evolution of the Lampsiline mussels. The mantle flap lure appears to have been the first to evolve with other lure types being derived from this condition. Apparently, lures were lost independently in several clades. Hypotheses are discussed as to how some of these lure strategies may have evolved in response to host fish prey preferences.     

Direct impact of invasive bivalve (<Emphasis Type="Italic">Sinanodonta woodiana</Emphasis>) parasitism on freshwater fish physiology: evidence and implications

Direct and potentially damaging effects of invasive alien species can remain unnoticed or insufficiently quantified, resulting in a lack of stakeholder awareness. We report for the first time that parasitic larvae (glochidia) of the invasive freshwater mussel Sinanodonta (Anodonta) woodiana (Unionidae, Bivalvia) cause an unexpected reduction in the condition factor of parasitized native fish species. The reduction in the body mass and condition factor of experimentally infested European chub (Squalius cephalus) was associated with changes in several physiological parameters measured in host fish plasma. Ion concentrations (potassium, chloride) and enzymes activities (aspartate aminotransferase, alanine aminotransferase, lactate dehydrogenase, alkaline phosphatase) were significantly affected; hence, the results reveal the complex effects of non-native glochidia on the homeostasis of the individually tested fish. Changes in host physiology and condition status were recorded also in environmentally relevant infestation intensities (mean of 3.02 ± 0.51 glochidia g^?1). Despite intensive concern regarding the negative biodiversity and ecosystem impacts of the adult stage of S. woodiana among conservationists and natural resource managers, potential effects of its larval stage have been neglected until now. Because fish hosts are an obligatory part of the reproductive cycle of the mussel and the main vector for spreading, documentation of this direct and easily quantifiable impact on fish has great potential to influence the key community of stakeholders in fisheries and aquaculture sectors and to serve as a strong motivating factor for invasive species control. We argue for more careful consideration of potential multiple life-stage effects of S. woodiana and of other invasive alien species as well, as different life stages can have highly specific impacts and corresponding relevance for key stakeholder groups.     

Review Geographic differences in host specialization between the symbiotic water mites Unionicola formosa and Unionicola foili (Acari: Unionicolidae)

The host specificity and population genetic structure of the symbiotic water mites Unionicola foili from the host mussel Utterbackia imbecillis and Unionicola formosa from the mussels Pyganodon cataracta, Pyganodon grandis and Anodonta suborbiculata were examined over a broad geographical scale in order to determine the extent to which specialization by these water mites is structured geographically. The behavioural responses of U. foili and U. formosa were highly host-species specific, with adults of both species exhibiting negative phototaxis in the presence of a chemical factor from the species of mussel with which the mites had been associated in the field. The photobehaviour of these water mites in the presence of water from a non-host mussel varied depending on the species in question. Although U. foili from U. imbecillis exhibited negative phototaxis in water modified by A. suborbiculata, mites from this latter host did not exhibit a directional response in U. imbecillis water. Unionicola foili and U. formosa from A. suborbiculata were positively phototactic when they were exposed to water modified by either species of Pyganodon. The photoresponse of U. formosa from P. cataracta and P. grandis was positive in the presence of water modified by U. imbecillis and A. suborbiculta. However, these mussel-mites showed no directional response in water modified by their alternate species of Pyganodon. Unionicola foili and the host-associated populations of U. formosa were examined for allozyme variation at eight loci to determine the pattern and degree of genetic variation. There was a high degree of genetic differentiation when mite populations from the two species of Pyganodon were compared with U. foili or U. formosa from A. suborbiculata. These populational groupings were fixed for different alleles at two enzyme loci. The results of this study indicate that populations of U. formosa from P. cataracta and P. grandis are reproductively isolated from U. foili from U. imbecillis and from U. formosa from A. suborbiculata and contend that host specificity is an important mechanism in restricting gene flow among these populational groupings. Furthermore, this study indicates that specialization among unionicolid water mites can vary geographically, owing to differences in geographic distribution of available hosts and differences in host use.Exp Appl Acarol 22: 683697 © 1998 Kluwer Academic Publishers     

GLOCHIDIA OF THE FRESHWATER MUSSEL LAMPSILIS OVERWINTERING ON FISH HOSTS

Largemouth Bass were infected with glochidia of the freshwatermussel Lampsilis cardium. Three fishes each were held at 4.5,10, and 15.5°C; five fish were held at 21°C. By 64 days,metamorphosed juveniles were found in the 15.5 and 21°Ctrials but not in the 5.5 and 10°C trials, indicating thatthe lower threshold temperature for metamorphosis was between10 and 15.5°C for the duration. In a second experiment,Largemouth Bass were infected with glochidia of L. cardium andheld at 10°C. A sample of fishes was removed monthly andbrought to 21°C. Numbers of glochidia that metamorphosedafter being warmed were compared to the number that metamorphosedwithout warming. The percentage that metamorphosed after warmingdecreased linearly with time. At one month, 100% of the glochidiametamorphosed after warming. This decreased to 80% by two months,to 30% by four months and 3% by six months. Although this post-warmingpercentage decreased with time, the total percentage of metamorphosedjuveniles (at all temperatures) was not correlated with time.Controls kept at 21°C required three weeks to reach peakmetamorphosis, but test subjects subjected to 10°C requiredless than nine days to metamorphose once warmed. Many overwinteringglochidia therefore complete a portion of their developmenton the host at winter temperatures, but stop short of excystment.Some glochidia metamorphosed without being warmed, but thisphenomenon is not understood. This study confirms that glochidiamay overwinter on hosts, with some glochidia persisting formore than six months before metamorphosing when warmer conditionsreturn. (Received 29 September 1998; accepted 18 January 1999)     

Do individual Activity Patterns of Brown Trout (Salmo trutta) alter the Exposure to Parasitic Freshwater Pearl Mussel (Margaritifera margaritifera) Larvae?

The hypothesis that interindividual differences in the activity of brown trout alter the exposure to parasitic freshwater pearl mussel glochidia was tested in a Swedish stream. Wild yearling brown trout (N = 103) were caught, individually tagged for identification and scored for open‐field activity during standardized laboratory tests in June. Fifty gravid freshwater pearl mussels were relocated to the stream, where after the trout were released back into the stream. The fish were recaptured in October (N = 35), checked for glochidia encystment (infested individuals: n = 6) and re‐scored for open‐field activity traits. Swimming velocity during the test was higher in fish infected with glochidia, suggesting that high activity could increase their exposure to glochidia. Potentially, as metabolism rate and ventilation rate typically increase with activity, elevated activity may lead to an increased likelihood of glochidia passing over the gills. This novel finding suggests that glochidia infestation is non‐random and that the behaviour of the host fish can influence the likelihood of glochidia infestation.     

The distribution of glochidia of the Swan mussel, Anodonta cygnea (Mollusca) on the Three-spined stickleback Gasterosteus aculeatus (Pisces)

The pattern of infestation by glochidia of the Swan mussel, Anodonta cygnea , on a population of the Three-spined stickleback, Gasterosteus aculeatus was studied over a period of 12 months. The results obtained are considered under the four headings of incidence, intensity, the effect of fish size and the toDoeraDhical distribution of oarasites on the host.     

Survival of glochidial larvae of the freshwater pearl mussel, Margaritifera laevis (Bivalvia: Unionoida), at different temperatures: a comparison between two populations with and without recruitment

The viability of free-living glochidia of the freshwater pearl mussel (Margaritifera laevis) was studied in the laboratory at water temperatures of 10 degrees C, 15 degrees C and 20 degrees C. To obtain glochidia, gravid female mussels were collected from the Chitose River, inhabited by adult and juvenile mussels, and from the Abira River, where only adult mussels were found. Daily survival rates of glochidia from each population at various water temperatures were significantly different, and survival time was longest at the lowest temperature in each population. Maintenance of some field mussel populations might become difficult at higher water temperatures due to the short survival time of glochidia and expected low density of host fish. Daily survival rates of glochidia were compared between the Abira population at 15 degrees C and the Chitose population at 20 degrees C, since these temperatures were close to the mean water temperature during the period of glochidial release in the respective rivers. Daily mean survival rates were significantly different between the Abira population at 15 degrees C and the Chitose population at 20 degrees C. Mean glochidial survival rate for the Chitose population changed from 85.3% to 66.2% from 9 to 13 h, whereas that for the Abira population dropped suddenly from 80.4% to 34.2% from 10 to 14 h after the initiation of experiment. Absence of juveniles in the Abira River might have been caused by the low glochidial viability. Survival times of free-living glochidia in Margaritiferidae tend to be shorter than in other families in Unionoida. A trade-off is suggested between high fertility and low glochidial survival rate in Margaritiferidae.     

Laboratory evidence suggests glochidia metamorphosis in Sinanodonta japonica (Bivalvia: Unionidae) is supported by gills,but no other tissues of the host Gymnogobius urotaenia (Perciformes: Gobiidae)

We quantitatively assessed the ability of the gills, caudal fin and scales of the floating goby Gymnogobius urotaenia (Hilgendorf, 1879) (Perciformes: Gobiidae) to serve as substrates for the larvae (glochidia) of the freshwater mussel Sinanodonta japonica (Clessin, 1874) (Unionida: Unionidae) by comparing parasitism success and metamorphosis success. We established three experimental treatments with 10 fish per treatment. Twenty glochidia were introduced onto one of the three body parts of each test fish by direct pipette infestation. Glochidia in the gill group had higher parasitism success than those in the fin and scale groups. Juvenile mussels were obtained only in the gill group. We quantitatively assessed the appropriateness of the three body parts as substrates for glochidia on the basis of three indicators: parasitism success; metamorphosis success; and parasitism and metamorphosis success. We conclude from our laboratory experiment that the artificial introduction of S. japonica glochidia onto G. urotaenia gills is a better procedure for obtaining juvenile mussels than the introduction onto fin or scales.     

Identifying freshwater mussels (Unionoida) and parasitic glochidia larvae from host fish gills: a molecular key to the North and Central European species

Freshwater mussels (order Unionoida) represent one of the most severely endangered groups of animals due to habitat destruction, introduction of nonnative species, and loss of host fishes, which their larvae (glochidia) are obligate parasites on. Conservation efforts such as habitat restoration or restocking of host populations are currently hampered by difficulties in unionoid species identification by morphological means. Here we present the first complete molecular identification key for all seven indigenous North and Central European unionoid species and the nonnative Sinanodonta woodiana, facilitating quick, low-cost, and reliable identification of adult and larval specimens. Application of this restriction fragment length polymorphisms (RFLP) key resulted in 100% accurate assignment of 90 adult specimens from across the region by digestion of partial ITS-1 (where ITS is internal transcribed spacer) polymerase chain reaction (PCR) products in two to four single digestions with five restriction endonucleases. In addition, we provide protocols for quick and reliable extraction and amplification of larval mussel DNA from complete host fish gill arches. Our results indicate that this new method can be applied on infection rates as low as three glochidia per gill arch and enables, for the first time, comprehensive, large-scale assessments of the relative importance of different host species for given unionoid populations.