Trophic relationships between the larvae of two freshwater mussels and their fish hosts

Denic, Marco; Taeubert, Jens‐Eike; Geist, Juergen

doi:10.1111/ivb.12080

Cited by 30 publications

(37 citation statements)

References 31 publications

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“…A variety of aquatic parasites, such as the larvae (glochidia) of many species of unionoid mussels, attaches and encysts on the gills of fish (Crane et al 2011; Denic et al 2015; Meyers et al 1980; Young and Williams 1984). Such encystment can affect both the physiology and behaviour of the host.…”

Section: Introductionmentioning

confidence: 99%

Encystment of parasitic freshwater pearl mussel (Margaritifera margaritifera) larvae coincides with increased metabolic rate and haematocrit in juvenile brown trout (Salmo trutta)

et al. 2017

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Gill parasites on fish are likely to negatively influence their host by inhibiting respiration, oxygen transport capacity and overall fitness. The glochidia larvae of the endangered freshwater pearl mussel (FPM, Margaritifera margaritifera (Linnaeus, 1758)) are obligate parasites on the gills of juvenile salmonid fish. We investigated the effects of FPM glochidia encystment on the metabolism and haematology of brown trout (Salmo trutta Linnaeus, 1758). Specifically, we measured whole-animal oxygen uptake rates at rest and following an exhaustive exercise protocol using intermittent flow-through respirometry, as well as haematocrit, in infested and uninfested trout. Glochidia encystment significantly affected whole-animal metabolic rate, as infested trout exhibited higher standard and maximum metabolic rates. Furthermore, glochidia-infested trout also had elevated levels of haematocrit. The combination of an increased metabolism and haematocrit in infested fish indicates that glochidia encystment has a physiological effect on the trout, perhaps as a compensatory response to the potential respiratory stress caused by the glochidia. When relating glochidia load to metabolism and haematocrit, fish with low numbers of encysted glochidia were the ones with particularly elevated metabolism and haematocrit. Standard metabolic rate decreased with substantial glochidia loads towards levels similar to those of uninfested fish. This suggests that initial effects visible at low levels of encystment may be countered by additional physiological effects at high loads, e.g. potential changes in energy utilization, and also that high numbers of glochidia may restrict oxygen uptake by the gills.

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Section: Introductionmentioning

confidence: 99%

Encystment of parasitic freshwater pearl mussel (Margaritifera margaritifera) larvae coincides with increased metabolic rate and haematocrit in juvenile brown trout (Salmo trutta)

et al. 2017

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“…The initial difference in growth could occur if juveniles start their free-life in the sediments at different times. Margaritifera margaritifera ;Denic et al, 2015;Marwaha et al, 2017). Yellow perch, sunfish, and bass are the dominant nearshore fish in Sproule Bay (H. Cyr unpublished data), and they are all known hosts of E. complanata glochidia (Kneeland & Rhymer, 2008;Matteson, 1948).…”

Section: Early Juvenile Growth Declines With Agementioning

confidence: 99%

The growth of juvenile native mussels (Elliptio complanata) in lakes varies with sediment characteristics and site exposure

Cyr

2019

Freshwater Biology

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Unionid mussels are among the largest and longest‐lived freshwater invertebrates and can play an important role in these ecosystems. They are also one of the most endangered groups of organisms. The juvenile stage is a particularly vulnerable part of mussel life history and is one of the most poorly known. I compared the growth of young Elliptio complanata at 17 nearshore sites, in shallow (polymictic) and stratified lake basins, along gradients of sediment characteristics and site exposure (effective fetch). At each site, the growth of six to 14 small (20–68 mm) mussels collected on the sediment surface was measured, using internal growth lines. The growth of very young endobenthic mussels (22–40 mm) was also measured on four to six mussels at each of two sites. Juveniles spend several years in the sediments, and I found that during this period growth is not constant but declines rapidly with age. Shifts in δ15N signatures suggest that juveniles change their habitat use towards a more planktonic baseline around the time of maturation, when they reach a length of 30–50 mm. Identical δ13C signatures in juveniles and adults suggest that both rely on food of planktonic origin, whether deposited or suspended. The growth of juvenile mussels varies in a complex but predictable manner with sediment characteristics and wind‐driven physical forces. Growth was highest in fine sediments with low organic content, in highly organic but coarse sediments, and in protected nearshore areas with low effective fetch. Interestingly, I also found high growth rates at exposed nearshore areas with fine sediments, suggesting that areas where bottom topography creates a refuge from currents and waves may provide particularly good conditions for the early growth of juvenile mussels. Some parts of the shoreline may be more important than others for native mussel populations, and if we can identify those, they may warrant additional protection.

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“…The sperm is then inhaled by female mussels to fertilize the eggs in their marsupial gills. After several weeks, when the fertilized eggs have developed to round glochidium larvae of 50-70 μm diameter, the glochidia are shed into the water by the females (Young and Williams 1984a, Bauer 1987b, Pekkarinen and Valovirta 1996, Schmidt and Vandré 2010, Scheder et al 2011, Denic et al 2015, after which the glochidia have to reach and attach to appropriate host fish for further development. Unlike the glochidia of many other mussel species, which may successfully parasitize several fish species and attach either on gills, fins or skin of the host (see e.g.…”

Section: Habitat Preferences and Life Cycle Of The Freshwater Pearl Mmentioning

confidence: 99%

“…In addition to the salmonid host specificity, the long duration of the parasitic stage and the remarkable growth of glochidia during that stage distinguish FPM from many other mussel species; in the northernmost range of FPM, the glochidia remain attached on the host fish for almost a year, from early autumn to late summer of the following year (Young and Williams 1984b, Hruška 1992, Ieshko et al 2009, Schmidt and Vandré 2010, while in southern latitudes the parasitic life stage may end several months earlier (Cunjak and McGladdery 1991, Eybe et al 2015. Nevertheless, during that stage the glochidia metamorphose into slightly ovoid juvenile mussels of 400-500 μm length (Young and Williams 1984b, Bauer 1987b, 1987c, Bauer and Vogel 1987, Schmidt and Vandré 2010, Denic et al 2015, after which the juveniles leave the host and penetrate into the river bottom substratum for several years (Young and Williams 1983a, Bauer 1988, San Miguel et al 2004, Geist and Auerswald 2007, Bolland et al 2010, Ostrovsky and Popov 2011, presumably to hide from predators (see Zimmerman et al 2003). The mortality of FPM is very high during these early life stages even in optimal conditions; it is estimated that 95-99 % of glochidia shed into the water do not reach a suitable host and die, 90-95 % of the glochidia attached to a suitable host die before completing metamorphosis, and a further 95 % of young mussels are lost between detachment from the host and establishment in the bottom substratum (Young and Williams 1984a, Preston et al 2007, Schmidt and Vandré 2010.…”

Section: Habitat Preferences and Life Cycle Of The Freshwater Pearl Mmentioning

confidence: 99%

“…Furthermore, as the fish were caught in early June and the size of glochidia had also greatly increased to more than 300 μm from the initial 50-70 μm (e.g. Nezlin et al 1994, Pekkarinen and Valovirta 1996, Denic et al 2015, there is no doubt that the glochidia had been attached to the brook trout for at least 9 months. This case is, to my knowledge, the first ever confirmed successful parasitism by European FPM of this invasive salmonid, and implies that the long-run adaptation of European FPM to use brook trout as their host cannot be excluded.…”

Section: Suitability Of Brook Trout As a Host For The European Freshwmentioning

confidence: 99%

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An alien fish threatens an endangered parasitic bivalve: the relationship between brook trout (Salvelinus fontinalis) and freshwater pearl mussel (Margaritifera margaritifera) in northern Europe

Salonen

Marjomäki

Taskinen

2016

Aquatic Conservation

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Salonen, JouniThe role of salmonid fishes in conservation of the endangered freshwater pearl mussel (Margaritifera margaritifera) Jyväskylä: University of Jyväskylä, 2016, 48 The abundance of freshwater pearl mussels (Margaritifera margaritifera) has declined widely during the past century, and new conservation initiatives are needed. This thesis focused on the relationship between M. margaritifera and its salmonid host required for reproduction of this species. First, by exposing fish experimentally to glochidium larvae of M. margaritifera, different M. margaritifera populations were shown to demonstrate strong differences in their ability to parasitize different salmonid species. Atlantic salmon was clearly a better host for mussels in large river channels, whereas in small headwater tributaries brown trout was the best, or the only suitable, host. These findings provide a previously unrecognised explanation for the collapse and the lack of recruitment especially of the salmon-specific M. margaritifera populations; a high proportion of large salmon rivers were dammed for hydropower production in the 1960s, which prevented the migration of salmon and thus left M. margaritifera without the appropriate host in these rivers. Furthermore, an invasive salmonid, brook trout, was widely introduced to small tributaries above the dams in the past, but in this study was shown to be an unsuitable host for M. margaritifera. Thus, and due to the tendency of brook trout to replace native brown trout, the spread of brook trout is an additional threat to M. margaritifera. An indication of local adaptation of M. margaritifera, i.e. higher infectivity in sympatric salmonid host strain than in allopatric populations of the same species, was also detected. Finally, a new, nondestructive approach to search for M. margaritifera populations, involving electrofishing and quick visual examination of the gills of captured salmonids, revealed the occurrence of 3 previously unknown populations. The results of this thesis highlight the importance of taking into account the roles of salmonid fish in future efforts to search, protect and restore freshwater pearl mussel populations.

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Trophic relationships between the larvae of two freshwater mussels and their fish hosts

Cited by 30 publications

References 31 publications

Encystment of parasitic freshwater pearl mussel (Margaritifera margaritifera) larvae coincides with increased metabolic rate and haematocrit in juvenile brown trout (Salmo trutta)

Encystment of parasitic freshwater pearl mussel (Margaritifera margaritifera) larvae coincides with increased metabolic rate and haematocrit in juvenile brown trout (Salmo trutta)

The growth of juvenile native mussels (Elliptio complanata) in lakes varies with sediment characteristics and site exposure

An alien fish threatens an endangered parasitic bivalve: the relationship between brook trout (Salvelinus fontinalis) and freshwater pearl mussel (Margaritifera margaritifera) in northern Europe

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