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.     

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     

Evidence of cannibalism and bentho-pelagic coupling within the life cycle of the mussel, Perna canaliculus

The feeding ecology of the green-lipped mussel, Perna canaliculus, was investigated within three intertidal mussel beds along Ninety Mile Beach, northern New Zealand, between August 2000 and March 2001. Adult mussels of different sizes (45-105 mm in shell length) were collected from the intertidal sites about 30 min after being submerged by the incoming tide for gut content analyses. Results of these analyses indicate that mussels consume a variety of phytoplankton, micro- and mesozooplankton, including mussel larvae and post-larvae. Cannibalism of juveniles of up to 620 μm was recorded for intertidal mussels, and conspecifics of up to 2.4 mm were found within the stomachs of additional mussels collected in August 2000 from a nearby subtidal site. For all three intertidal populations, mussel larvae and juveniles contribute about 70% of the food particle consumption during the spawning peak in August, while phytoplankton and other zooplankton constitute the majority of the food source (about 99%) in March, during gametogenesis. Larger intertidal mussels tended to have more food particles in their stomachs than smaller mussels within all three populations. Distinctive differences in food consumption among intertidal populations directly coincide with variations in total particulate matter (TPM), particulate organic matter (POM) and percent organic matter (OM) in the adjacent seawater.Separate experiments designed to test the feeding behavior of mussels feeding at different times during the incoming tide were conducted at one of the intertidal sites during August 2000 and March 2001. Results from these experiments indicate a marked shift in food consumption from bivalves to other mesozooplankton in August, and from phytoplankton to mesozooplankton in March. The observed combination of mussel predatory and grazing behavior over the incoming tide and through the year provides evidence for a strong food-web link between the benthic and pelagic life stages of this species. Furthermore, the high rate of cannibalism during some months of the year suggests that this source of food may significantly contribute to the energy budget of wild populations, with potential implications for evolutionary adaptive success.     

The Behavioural Responses by Larvae of the Water Mite Unionicola Foili (Acari: Unionicolidae) to Gravity, Light and Host Chemicals: Adaptations for Transmission Success?

The life cycle of the water mite Unionicola foili includes larvae that parasitize chironomid dipterans, and nymphs and adults that occur in association with the freshwater mussel Utterbackia imbecillis. The georesponses and photoresponses of larval U. foili in the presence of chemical substances from chironomids and mussels both prior to (= pre-chironomid larvae) and after their parasitism with chironomids (= post-chironomid larvae) were examined in the laboratory. The responses of larval U. foili to light and gravity changed during larval ontogeny and varied depending on the chemistry of the medium in which they were examined. Pre-chironomid larvae preferentially responded to water modified by chironomids given that negative phototaxis and positive georesponses were elicited only in the presence of water that had been modified by these hosts. Post-chironomid larvae exhibited host-induced negative phototaxis only in the presence of mussel-modified water. Post-chironomid larvae were consistently geopositive when exposed to water modified by mussels or chironomids. The pattern of responses exhibited by larval U. foili to light and gravity are interpreted as adaptations for locating potential hosts in the field.     

Annual gametogenic cycle of the freshwater pearl mussel,Lamellidens marginalis (Lamarck, 1819) collected from a perennial lentic habitat of Bangladesh

ABSTRACT

We investigated the annual gametogenic phenology of the freshwater pearl mussel, Lamellidens marginalis (Lamarck, 1819), collected from a lentic habitat at Mymensingh, Bangladesh, using biometry and histology through monthly sampling from August 2015 to July 2016. After biometric measurements, thin slices of dorso-ventral sections were cut from the middle of the mussels for histology to determine sex and level of gonadal maturation. The condition index (CI) ranged from 0.64 (March) to 0.99 (January) over the study period. The CI peaked three times (January, April and July) indicating that the mussels were ripe during these months and subsequent decreases in CI indicated spawning, which was consistent with histology. Both males and females exhibited similar patterns in terms of gonadal development, maturation and spawning activity. It was confirmed that natural populations of L. marginalis spawn throughout the year with remarkable temporal variations, except during December when the surface water temperature reaches annual minima (16.5°C). Highest spawning activity of L. marginalis was noted during February–March, May and July–November. The data obtained in the present study could be useful for the conservation managers of this commercial species by allowing harvesting of better quality mussels to be timed without interrupting major spawning activity.     

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.     

Divergence of ovipositor length and egg shape in a brood parasitic bitterling fish through the use of different mussel hosts

Bitterling fishes deposit their eggs on the gills of living mussels using a long ovipositor. We examined whether ovipositor length (OL) and egg shape correlated with differences in host mussel species in the family Unionidae among populations of the tabira bitterling (Acheilognathus tabira) in Japan. Bitterling populations that use mussels in the sub-family Anodontinae possessed longer ovipositors and more elongated eggs than those using mussels of Unioninae, as expected from the difference in host size between the sub-families (anodontine mussels are larger than unionine mussels). Based on a robust phylogeny of A. tabira populations, we demonstrated that the evolution of both OL and egg shape were correlated with host differences, but not with each other, suggesting that these traits have been selected for independently. Our study demonstrates how adaptive traits for brood parasitism may diverge with host shift due to different host availability and/or interspecific competition for hosts.     

The use of volatile cues in recognition of kin eggs by predatory mites

1. Several animal species are known to distinguish between their own eggs and eggs of unrelated conspecifics. However, the cues involved in this discrimination are often unknown. These cues were studied using the predatory mite Gynaeseius liturivorus Ehara.
2. Adult females of these predatory mites oviposit in clusters and avoid oviposition close to eggs laid by other females, resulting in reduced cannibalism between offspring. Because predatory mites are blind, it was tested whether volatiles of eggs were used as a cue for egg recognition.
3. Adult female predatory mites were offered volatile cues of their own eggs and of unrelated conspecific eggs, and females were prevented from contacting the eggs. Predatory mites oviposited closer to their own eggs than to unrelated eggs. This preference was observed even when one own and one unrelated egg were offered as a volatile source.
4. These results suggest that adult female predatory mites can determine kinship using volatiles released from the eggs.

     

High levels of multiple paternity in a spermcast mating freshwater mussel

Multiple paternity is an important characteristic of the genetic mating system and common across a wide range of taxa. Multiple paternity can increase within‐population genotypic diversity, allowing selection to act on a wider spectre of genotypes, and potentially increasing effective population size. While the genetic mating system has been studied in many species with active mating behavior, little is known about multiple paternity in sessile species releasing gametes into the water. In freshwater mussels, males release sperm into the water, while eggs are retained and fertilized inside the female (spermcast mating). Mature parasitic glochidia are released into the water and attach to the gills of fish where they are encapsulated until settling in the bottom substrate. We used 15 microsatellite markers to detect multiple paternity in a wild population of the freshwater pearl mussel (Margaritifera margaritifera). We found multiple paternity in all clutches for which more than two offspring were genotyped, and numbers of sires were extremely high. Thirty‐two sires had contributed to the largest clutch (43 offspring sampled). This study provides the first evidence of multiple paternity in the freshwater pearl mussel, a species that has experienced dramatic declines across Europe. Previous studies on other species of freshwater mussels have detected much lower numbers of sires. Multiple paternity in freshwater pearl mussels may be central for maintaining genetic variability in small and fragmented populations and for their potential to recover after habitat restoration and may also be important in the evolutionary arms race with their fish host with a much shorter generation time.     

Guild structure in water mites (Unionicola spp.) inhabiting freshwater mussels: choice,competitive exclusion and sex

Summary Unionicolid water mites inhabit freshwater unionid mussels during the nymphal and adult stages of their life-cycle. Regular sampling of mussels from two sites in St. Mark's River, Fl. established that each of four species of water mite (Unionicola abnormipes, U. fossulata, U. serrata and U. formosa) occurred mainly in one or two of the mussel species available at each site.The role of preference for particular mussel species during host location was assessed for the first three mite species by choice experiments, in which mites were offered different mussel species simultaneously. In five out of six experiments, mites entered normally unused mussels as often as they did normally used ones. Additionally, a sexual difference in choice was found for U. fossulata, with males preferring one mussel species and females showing no preference. One mussel species, (Anodonta imbecilis), normally unused but chosen by mite species during the lab. experiments, is inhabited exclusively by the fourth mite species, U. formosa, in the field. An experiment showed that U. formosa excludes other mite species aggressively from Anodonta imbecilis.The results illustrate the sometimes misleading nature of simple sampling data as an indication of host specificity or host preference in parasites. They suggest also that the population dynamics of some parasites might be more fruitfully compared to unrelated, free-living species than to other parasites.     

Recruitment of shore crabsCarcinus maenas on tidal flats: Mussel clumps as an important refuge for juveniles

During the late summer and early fall, juvenile shore crabs (Carcinus maenas L.) occurred in high abundances in mussel clumps scattered on tidal flats of the Wadden Sea. Abundances were much lower on bare tidal flats without mussel clumps and decreased substantially from July to November, whereas numbers in mussel clumps remained high. Large crabs left the tidal flats in early fall, whereas juveniles undertook tidal migrations only in the late fall. In March very few shore crabs were found in the intertidal area. The size of juvenile shore crabs living between mussels did not increase significantly during fall. On the bare tidal flats surrounding the mussels, a size increase was observed. Mussel beds and mussel clumps serve as a spatial refuge for the early benthic phases of juvenile shore crabs. Between mussels they can hide effectively from their epibenthic predators. Juvenile shore crabs do not leave the intertidal area and the mussel habitats before their major predators have left the area. Mussel clumps scattered over the tidal flats may be a critical refuge for juvenile shore crabs settling on tidal flats. Intensified efforts in mussel culturing in the European Wadden Sea during recent decades may have caused an increased abundance of mussel clumps on tidal flats, thus enhancing habitat availability for some mussel-clump inhabitants.     

Effect of the western pearlshell mussel Margaritifera falcata on Pacific lamprey Lampetra tridentata and ecosystem processes

Suspension feeders concentrate organic material from the water column and enhance deposition to the surrounding benthos. On the South Fork of the Eel River (Mendocino, California) two suspension feeders, the freshwater mussel Margaritifera falcata and Pacific lamprey larvae Lampetra tridentata, co‐occur in areas with low flow velocities and boundary sheer stresses. We investigated mussel/lamprey larvae interactions, and their impacts on nutrient and organic matter cycling, in flow‐through enclosures placed where lamprey larvae and mussels naturally occurred. Over the 80‐day study, lamprey larvae grew faster in the presence of mussels and in food addition treatments. Our results suggest that lamprey larvae benefit from native mussels, and that lamprey populations and organic matter retention in rivers may decrease with the rapid decline of native freshwater mussels.     

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.     

Life history traits and abundance can predict local colonisation and extinction rates of freshwater mussels

1. A critical need in conservation biology is to determine which species are most vulnerable to extinction. Freshwater mussels (Bivalvia: Unionacea) are one of the most imperilled faunal groups globally. Freshwater mussel larvae are ectoparasites on fish and depend on the movement of their hosts to maintain connectivity among local populations in a metapopulation. 2. I calculated local colonisation and extinction rates for 16 mussel species from 14 local populations in the Red River drainage of Oklahoma and Texas, U.S. I used general linear models and AIC comparisons to determine which mussel life history traits best predicted local colonisation and extinction rates. 3. Traits related to larval dispersal ability (host infection mode, whether a mussel species was a host generalist or specialist) were the best predictors of local colonisation. 4. Traits related to local population size (regional abundance, time spent brooding) were the best predictors of local extinction. The group of fish species used as hosts by mussels also predicted local extinction and was probably related to habitat fragmentation and host dispersal abilities. 5. Overall, local extinction rates exceeded local colonisation rates, indicating that local populations are becoming increasingly isolated and suffering an ‘extinction debt’. This study demonstrates that analysis of species traits can be used to predict local colonisation and extinction patterns and provide insight into the long‐term persistence of populations.     

RANDOM AMPLIFIED POLYMORPHIC DNA (RAPD) MARKERS REVEAL CROSS-FERTILISATION IN BIOMPHALARIA GLABRATA (PULMONATA: BASOMMATOPHORA)

The freshwater, schistosome-transmitting snail, Biomphalariaglabrata is a simultaneous hermaphrodite which can reproduceby both cross-and selffertilisation, but despite the medicalimportance of this species, little is known about the matingstrategies adopted by wild-type individuals from natural populations.The identification of cross-fertilised progeny is a prerequisitefor both evolutionary studies of the relative fitness of differentreproductive strategies, and for the production of exclusivelyoutcrossed F₁ populations for genetic mapping of biologicallyimportant phenotypes, most notably, resistance to schistosomeinfection. In this study, parents, offspring and ‘syntheticoffspring’ (controls) from four families of B. glabratarecently derived from wild populations were analysed using theRandom Amplified Polymorphic DNA (RAPD) assay. RAPDs were usedbecause they reveal more genetic variation, require less tissue(juvenile snails were only 4–5 mm diameter) than proteinelectrophoresis, are less laborious than other molecular analyses,and do not require sequence data. Seven of the 19 arbitrarysequence, oligonucleotide primers used gave bands that werepolymorophic between pairs of parent snails. Scoring the offspringfor the presence/absence of these polymorphic bands showed thatall the offspring tested were the products of cross-fertilisation.This study provides the first demonstration of the applicabilityof the RAPD technique to an analysis of fertilisation in wild-typeB. glabrata. (Received 20 December 1994; accepted 27 March 1995)     

Life History of Ilybius fenestratus (Fabricius) (Coleoptera,Dytiscidae) in a Central Norwegian Lake

The life history of Ilybius fenestratus was studied in Målsj?en, a lake in S?r-Tr?ndelag, Central Norway (63°14'N, 10°26'E), during 1971–1972. Adults and larvae were sampled in activity traps every week during March–October and every 2–3 weeks during November–February. Newly-emerged adults were generally found from mid-July to September, and after overwintering in torpidity, probably in the water, they again appeared in the second half of June to August/September. Laying of eggs took place from early/mid July to early August. Larvae occurred in the traps from late July to early May. I. fenestratus was thus found to be a semivoltine summer breeder, with overwintering larvae the first winter and overwintering adults the next. Both adults and larvae lived in large areas of the lake's littoral zone.     

Somatic and genetic factors in sun and shade population differentiation in Plantago lanceolata and Anthoxanthum odoratum

Differences between individuals collected from sun and shade populations could result from either somatic or genetic differences, particularly in populations of perennial plants. Our objective in this study was to separate somatic from genetic differences. We collected Anthoxanthum odoratum and Plantago lanceolata from sun and shade populations and made measurements on both vegetatively propagated clones and seed progeny from each clone. The parental populations differed in a wide range of physiological and morphological traits. However, only photosynthetic capacity was significantly different between both the original sun and shade populations and their seed progeny. In both species, plants from the sun population had higher photosynthetic capacities than those from the shade population when grown in a common environment. This demonstrates that there was genetic differentiation between the sun and shade populations. Photosynthetic capacity of parents and offspring also differed, suggesting a somatic effect. Since many of the original clones were virus-infected, but all but one of the offspring were virus-free, this might have been a result of virus infection. However, in spite of the fact that the parents and offspring clones were propagated vegetatively so that the plants were at the same developmental stage at the time of measurement, we cannot rule out the possibility that differences in age of cell lines could also have been a factor.     

Recolonisation of four small streams in central Scotland following drought conditions in 1984

Four streams in the Loch Ard Forest in central Scotland dried out almost completely during a drought in the summer of 1984. The recovery of the invertebrate populations in the streams was studied from September 1984 until March 1985 when most of the insect larvae and nymphs were almost full-grown.The appearance of very small larvae belonging to several insect orders within a month of the streams' filling up suggests that they had survived the drought as eggs, or eggs had been laid by adults soon after the drought ended.Statistical analysis showed that with the exception of 3 taxa there was no significant difference between the numbers of animals in November 1984 samples and in samples collected in March 1985.Comparison of samples from March 1984 and March 1985 showed significant difference in population size for a few species; with 2 exceptions the 1984 samples (ie before drought) were larger. In the long term the overall effect of the drought on the invertebrate communities seems to have been limited.     

Mussels as bioindicators of trace metal pollution in the Danube Delta of Romania

Specimens of mussels species Anodonta anatina, Unio pictorum, U. tumidus and surfical sediment samples were collected in the summers of 1994 and 1995 from twelve lakes in the Danube Delta, Romania. Whole mussel tissues were analyzed for metals (Ag, As, Cd, Co, Cu, Cr, Ni, Pb, Se and Zn), and sediment samples were subjected to weak acid extraction and to a sequential extraction procedure, and analyzed for Cr, Cu, Ni and Zn. Total mean Cu and Ag concentrations were statistically greater in Unio species than in Anodonta species, but other metal levels did not significantly differ between mussel species. There was a ten fold variation for Cd and Pb and five fold variation for Zn, Ag and Co concentrations in mussels among lakes. Mean concentrations of As, Cu, Se and Zn in mussel tissues varied two fold among lakes. Zn, Co and Cd concentrations in mussels were significantly negatively correlated with distance gradients from the origin of the Delta and with distance from main channels of the Danube. Other metal concentrations in mussels did not correlate with either distance gradient. Trace metal levels in mussel tissues were correlated with those in weak acid and in sequential extractions of sediment. Zn concentrations in the carbonate fraction was the best predictor of Zn concentrations in mussels. Cu and Ni levels in the organic matter and sulfide fraction were the best estimators of Cu and Ni concentrations in mussels. This revised version was published online in July 2006 with corrections to the Cover Date.