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Life Span Variation of the Freshwater Pearl Shell: A Model Species for Testing Longevity Mechanisms in Animals

Authors:
  • Regulatory Council of the Galician Mussel

Abstract

Only about a dozen species of animals are known to achieve maximum ages (Amax) exceeding 100 yrs, including the freshwater pearl shell (Margaritifera margaritifera). This species has a life-span of between 100–200 years depending on latitude and environmental conditions. The difference in Amax is 3–7 times when southern populations, with Amax of 28–40 yrs, are compared to northern Arctic populations, with Amax of 114–190 yrs. Evolutionary and ecological explanations for longevity in the Arctic pearl shell include adaptations to the severe, unstable climatic and hydrological conditions in rivers. Extreme longevity seems to be related not only to the low metabolic rate in the cold climate, but the species can reduce energy expenditure for growth, and can rapidly increase metabolic rate up to 130x the normal level, to regenerate damaged shell or tissue. The physiology of this species may provide valuable clues to understanding the mechanisms that sustain longevity and retard senescence.
... Velikost a dlouhověkost perlorodek se mění se zeměpisnou šířkou (Bauer 1992). Jihoevropské populace jsou krátkověké s průměrnou délkou života 35 let a jsou charakteristické vysokými přírůstky, zatímco severské a ruské populace jsou charakteristické dlouhou délkou života (100 -190 let) a malými ročními přírůstky (Ziuganov et al. 2000). Nejstarší nalezenou perlorodkou byl 280 let starý jedinec z lokality Görjean ve Švédsku (Degerman et al. 2009), i když jiní autoři tento věk považují za neprokázaný a za nejstarší publikovaný údaj je udáváno stáří 179 let (Helama & Valovitra 2008). ...
... Nicméně i dlouhověké formy jsou schopny výrazně zvýšit svoji metabolickou aktivitu, např. při regeneraci poškozených tkání nebo lastury (Ziuganov et al. 2000, Helama & Valovitra 2008. Na rozdíl od juvenilních jedinců nejsou adulti po nástupu pohlavní dospělosti tak nároční na kvalitu detritu. ...
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Action plan for freshwater pearl mussel in the Czech Republic The effort for Czech freshwater pearl mussel conservation was started in 1982. In 1993, the official ratification of conservation efforts resulted in the introduction of the action plan for freshwater pearl mussel. It is approved by the Ministry of the Environment of the Czech Republic and coordinated by Nature Conservation Agency (NCA CR). The third phase of action plan was approved in 2013. It is focused on the ecosystem-oriented conservation approach reflecting the complexity of processes in oligotrophic running waters that is a key to freshwater pearl mussel survival. The action plan for freshwater pearl mussel distinguishes among the localities according their quality and perspectives. Perspective localities are those that have sufficiently large population and their habitat is only slightly altered according to 16 hydromorphological, hydrochemical, ecological and environmental metrics (see Simon, Vaníčková, Bílý et al 2015). These localities are labelled as a category I. Altered population are those that have populations of insufficient abundance and their habitat is altered and insufficient in more metrics. These localities are labelled as a category II. Localities of a category III are likely to vanish soon due to occurrence of only individuals Margaritifera and the habitat is severely altered. Conservation efforts and active protection of habitat are mainly targeted on localities of category I and II.
... Only few microhabitats in headwaters provide sufficiently stable conditions for the survival of long-living species such as true river mussels (Unionoida). In boreal streams, pearl mussels (Margaritifera margaritifera) belong to the longest-living animals on earth, attaining more than 200 years (Ziuganov et al., 2000). Along with the "EPT taxa" (Ephemeroptera: mayflies, Plecoptera: stoneflies, Trichoptera: caddisflies), they belong to the most pollution-sensitive taxonomic groups. ...
Chapter
Benthic macroinvertebrates colonize all types of lentic and lotic inland hydrosystems. Except for few purely marine groups, almost all taxonomic groups of invertebrates occur in freshwater. Due to their size from less than 1 mm to several centimeters and the amphibious life cycle of aquatic insects as one of the main groups, they are important actors in the benthic-pelagic coupling of food webs, they connect the detritus-based food chain with the primary-production-based food chain, and provide reciprocal subsidies between aquatic and terrestrial ecosystems. Some species have been globally distributed by human activities and are now invasive neobiota. In this chapter, we address classical methods for the study of benthic macroinvertebrates, their life cycle strategies and the community-determining parameters of typical inland water habitats. In spite of their essential contribution to ecosystem processes, benthic macroinvertebrates are insufficiently considered in conservation strategies. In many countries, especially in the Tropics, there is still a great lack of knowledge of their biodiversity and their functional responses to seasonality and alterations in water quality and quantity.
... Previous work has shown that M. truncata frequently have low fecundity and a failure to recruit at the Frisian Front (a region of relatively similar latitude and temperature range to the specimens used in the present study). Furthermore, previous work has also shown that molluscs (Margaritifera margaritifera) living at high latitudes with a longer lifespans have better wound and shell-healing capacity than those living at lower latitudes (Ziuganov et al. 2000). The difference in repair capacity between high and low latitude populations of M. margaritifera was hypothesised to be due to the reduced energy expenditure for growth, and therefore greater energy availability for shell and tissue regeneration to sustain homeostasis. ...
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Acclimation, via phenotypic flexibility, is a potential means for a fast response to climate change. Understanding the molecular mechanisms underpinning phenotypic flexibility can provide a fine-scale cellular understanding of how organisms acclimate. In the last 30 years, Mya truncata populations around the UK have faced an average increase in sea surface temperature of 0.7 °C and further warming of between 1.5 and 4 °C, in all marine regions adjacent to the UK, is predicted by the end of the century. Hence, data are required on the ability of M. truncata to acclimate to physiological stresses, and most notably, chronic increases in temperature. Animals in the present study were exposed to chronic heat-stress for 2 months prior to shell damage and subsequently, only 3, out of 20 damaged individuals, were able to repair their shells within 2 weeks. Differentially expressed genes (between control and damaged animals) were functionally enriched with processes relating to cellular stress, the immune response and biomineralisation. Comparative transcriptomics highlighted genes, and more broadly molecular mechanisms, that are likely to be pivotal in this lack of acclimation. This study demonstrates that discovery-led transcriptomic profiling of animals during stress-response experiments can shed light on the complexity of biological processes and changes within organisms that can be more difficult to detect at higher levels of biological organisation. Electronic supplementary material The online version of this article (10.1007/s12192-018-0910-5) contains supplementary material, which is available to authorized users.
... The pearl mussel is a long-lived aquatic species and individuals usually have a lifespan of between 100-200 years depending on latitude and environmental conditions (Zuiganov et al 2000), but exceptionally up to 280 years in northern Sweden (Dunca and Mutvei 2009). Today, most surviving populations are found in northern European rivers and streams in partially or wholly forested catchments. ...
... Maximum and mean lifespan of ectotherms can vary dramatically between related species and populations from different climatic and environmental conditions Bluhm et al. 2001;Philipp and Abele 2010). Inter and intra-specific comparisons among marine and freshwater bivalves on biogeographic gradients indicate species/populations from colder environments to be frequently longer lived (Basova et al. 2012;Fiori and Defeo 2006;Philipp et al. 2005a;Ziuganov et al. 2000). The effect of environmental temperature on the lifespan of marine ectotherms was shown for fish (Liu and Walford 1970), nematodes (e.g. ...
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Environmental factors can affect the rate of ageing and shape the lifespan in marine ectotherms. The mechanisms and the degree of environmental influence on aging can best be studied in species with wide ranging biogeographic distribution. One of the biomarkers of physiological ageing is the fluorescent age pigment lipofuscin, which accumulates over lifetime in tissues of bivalves. We compared lipofuscin accumulation rate in muscles and respiratory tissues of the extremely long-lived bivalve Arctica islandica from five geographically distinct populations (Northern Norway, White Sea, Kiel Bay, German Bight and Iceland). Maximum investigated chronological age across different populations in the present study differed from 40 years in Kiel Bay to 192 years at Iceland. An inverse association between lipofuscin deposition rate and recorded maximum age was observed through inter-population comparisons. In most cases lipofuscin accumulated exponentially over age in a tissue-specific manner. The age-specific lipofuscin content was significantly higher in respiratory than muscles tissues in all populations. Cellular lipofuscin granule area can be used as indicator of aging across A. islandica populations with the variance in granule accumulation depending on the annual variations of salinity in different marine regions, but not on the habitat-specific thermal envelope.
... Therefore, we can consider that adult individuals observed in the field have attained maximum size. Conversely, in other species, largest differences have been found among populations located in different rivers, for instance in M. margaritifera (Bauer, 1992;Hastie et al., 2000;Ziuganov et al., 2000;San Miguel et al., 2004) and in M. laevis (Akiyama & Iwakuma, 2009). ...
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Here we analyse in detail, for the first time, the growth pattern of the endangered freshwater mussel Margaritifera auricularia in the Ebro basin, a life history trait essential for conservation purposes. We combined information on size and age from captive bred juveniles, together with growth annuli from living preadults studied in the field, and empty shells of preadult and adult individuals. We compared the fit of six types of (asymptotic and sigmoid) non-linear growth models and, in terms of residual errors and AIC values, the sigmoid ones were superior, being the Generalized von Bertalanffy and Richards models the best fitted ones. After an initial exponential growth phase in juveniles, growth rate starts to decelerate at an inflection point corresponding to an age of seven years. At an age of about 30 years, the growth rate markedly declines and attains an asymptote at c. 150 mm shell length. Global growth rate is relatively low but comparable to other members of the family, and the maximum age estimated from ring counts was 68 years. We demonstrate that the use of sigmoid models provides more accurate estimation of growth patterns in freshwater mussels, as previously observed for other bivalves.
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The freshwater pearl mussel (Margaritifera margaritifera) is one of the longest-lived invertebrate species in the world and one of the most threatened freshwater animals in Europe. Its southernmost populations, located in northwestern Spain, are in a critical conservation situation and are still understudied. Here we calibrate a non-invasive method for calculating the volume of the shell and use it to study the ontogenetic scaling of shell volume on shell length. We characterized ontogenetic growth and determined allometric relationships in 16 M. margaritifera northwestern Spain populations by using ordinary least squares regression, major axis and reduced major axis methods. We estimated topographic slopes of the sampling points using a GIS system, as a proxy of water speed. We measured 803 shells and found that the volume of the shell can precisely be estimated using three linear measurements. We found evidence for negative allometry of shell volume in the global sample and in 11 populations. We hypothesized that water speed would affect allometric patterns of local populations. Results suggest a negative relationship between the allometric slope and the topographic slope of the river section inhabited by M. margaritifera. We propose that when water speed is higher, larger mussels become proportionally flatter than in locations where water current is slower, allowing them to burrow more easily in the sediment. Our method will allow estimation of M. margaritifera biomass and ontogenetic growth without killing any specimens, which will contribute to conservation programs for this species.
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Tasas de crecimiento en dos poblaciones naturales de Gasterosteus aculeatus en el noroeste de España: relación con otros parámetros vitales Se analizaron las tasas de crecimiento de dos poblaciones naturales de Galicia (noroeste de España) del pez espinoso Gasterosteus aculeatus, cuyo ciclo biológico es estrictamente anual. Para ello, se utilizó una función no lineal para conjuntos de datos de longitud por edad: el modelo de crecimiento de von Bertalanffy. Estas poblaciones europeas periféricas tienen las tasas de crecimiento más altas (k en el modelo de von Bertalanffy > 0,4 mes–1, en promedio) conocidas para esta especie. A partir de los parámetros del modelo de von Bertalanffy, se calcularon las tasas de mortalidad instantánea y de fecundidad de cada población, y se observó que las tasas de mortalidad de las poblaciones gallegas son de 2 a 2,3 veces superiores a las observadas en general en Gasterosteidae. La combinación de la fertilidad y la mortalidad produjo diferentes valores óptimos intermedios de eficacia biológica para las hembras maduras de cada población. En términos generales, estas diferencias encontradas en rasgos vitales con respecto a otras poblaciones estudiadas de pez espinoso se pueden interpretar como adaptaciones locales a un clima de tipo mediterráneo con un valor alto de grados–día. Por tanto, estas poblaciones situadas en los límites de la zona de distribución de la especie pueden estar localmente adaptadas a condiciones ambientales muy específicas y pueden ser de interés en los ámbitos de la ecología y la conservación.
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Pleurobema riddellii is a state listed unionid in Texas, proposed for potential USFWS protections. Life history information is critical to determine whether a species warrants protection and to ensure that effective conservation measures are implemented. The Neches River is the only Texas river with substantial numbers of P. riddellii. In 2014, we selected three 25 m2 locations in the Neches River with the highest P. riddellii density and excavated those areas. All P. riddellii were collected, measured, and marked. This was repeated again in 2017. We used the inverted von Bertalanffy growth equation to create growth models for each location and an overall growth model. Models were compared to determine if there were differences between locations. The Highway 294 site had a higher growth rate and smaller individuals and was apparently a younger assemblage. To validate our models, additional P. riddellii were measured and their growth rings were counted. They were compared to the number of rings and sizes calculated by our model. Our overall growth model matched growth parameters calculated for other Pleurobema species, indicating that the model is accurately predicting P. riddellii growth. This study increases our knowledge of P. riddellii life history and can help in planning effective conservation strategies.
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• The complex life cycle of the globally threatened Margaritifera margaritifera includes a parasitic stage, where glochidia attach to the gills of fishes of the genus Salmo; however, the species of Salmo used appears to vary across its range. In previous literature the reported primary host in Scotland, home to a high proportion of the world's remaining M. margaritifera populations, is the Atlantic salmon Salmo salar, and in its absence the brown trout Salmo trutta. • In this study, the prevalence of infection in putative Salmo hosts in eight rivers in north‐west Scotland was determined. At a selected site on each river, where both S. trutta and S. salar were collected in abundance, S. trutta was the preferred host. • At sites where S. salar were abundant but S. trutta were at low density, however, S. salar showed a high prevalence of infection (with the exception of one river where neither S. salar nor S. trutta were infected). Thus, the primary host appears to be very site‐specific in the rivers sampled. • We speculate that this may be because M. margaritifera have population‐specific responses to cues for attachment to a host. Alternatively, it may be that host population‐specific immune responses mediate infections by glochidia. In addition, larger fish were less likely to be infected than smaller fish, and gills 1 and 5 were less heavily infected than gills 2–4. • One consequence of this finding, for both national and international conservation management of this globally endangered species, is that any current or future management activity must take into account local population host preferences, otherwise conservation efforts may be in vain.
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The modern data on systematics, morphology, life history, reproduction, and distribution of Margaritiferidae species are presented and analyzed. The principles of classification and phylogeny in the family, as well as the species problem are considered. The significance of pearl mussels in the waterbodies, ecological and evolutionary mechanisms of establishing "pearl mussel - salmon" symbiosis are discussed. The special attention is given to the reasons of extinction and prospects for restoration of "pearl mussel - salmon" ecosystems in various regions of Russia and the world.
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Generation time is supposed to be an important factor for the evolution of host-parasite relationships. The shorter an organism’s generation time, the faster its potential rate of evolution. Thus, short-lived hosts (the generation time is equal to or only slightly longer than that of the parasite) can be thought as being involved in an arms race where new host defences select for new parasite offences and vice versa. On the other hand, long-lived hosts are unlikely to match the faster evolving attack possibilities of parasites. Therefore the evolution of “covenants” may account for the continued persistence of such host-parasite systems (Freeland 1986).
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1. Within the distribution area of the freshwater pearl mussel (Margaritifera margaritifera L.), the maximum observed life span attained in a population varies from 30 to 132 years and the maximum shell length from 80 to 145 mm. For both life-history traits, the growth constant k is a major determinant. The growth constant describes the shape of the average individual growth curve, the lower its value, the slower is the asymptote approached. Maximum size and life span increase as the growth constant declines and the maximum age almost equals the time necessary to complete the growth pattern. 2. With increasing latitude, from North Spain up to the polar circle, the growth constant declines, whereas age and size increase. This must be attributed to the close relationship between the growth constant and metabolism. As temperature decreases (towards the north), metabolic rate declines and the rate of growth decreases; the asymptote is approached slowly and this leads to a long life. Simultaneously, there is probably a shift in the anabolic-catabolic-balance increasing the asymptotic size and hence the maximum size. 3. The growth constant and maximum life span also respond to the productivity of the habitat. There is a negative correlation between growth constant and eutrophication, and the maximum life span is reduced as the concentration of nitrate increases. 4. Implications for Bergmann's rule and for the theory of ageing are discussed. It is concluded that this variability is a case of phenotypic plasticity with no adaptive value because: (i) plasticity must be attributed to unavoidable physiological responses; (ii) between populations the relationships between maximum life span, maximum size and reproductive output are positive, whereas trade-offs would be expected if variation in life-history tactics was the source of plasticity; and (iii) the demographic consequences of plasticity may be highly disadvantageous.
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Алимов А.Ф. Функциональная экология пресноводных двустворчатых моллюсков. Л.: Наука, 1981. 248 с.
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My interest in longevity in fish arose originally from its significance in fish resource dynamics and its relationships to growth, maturation and fecundity. My first opportunity to perceive the wider implications of the phenomenon of longevity came at the 1959 Conference on Lifespan in Man and Animals sponsored by the CIBA Foundation. Holt and I (Beverton and Holt, 1959) gave a paper on life-spans of fish in relation to growth, and the contributors included the late George Sacher whose paper on mammalian size and life-span has been referred to at this conference. The present symposium in its aims and multi-disciplinary character has much in common with the 1959 CIBA Conference. I shall again approach my subject primarily from the demographic standpoint, but this time exploring certain evolutionary implications.