Download Ecology of the threatened thick-shelled river mussel Unio crassus

Ecology of the threatened
thick-shelled river mussel
Unio crassus (Philipsson 1788)
with focus on mussel-host interactions
Lea Dominique Schneider
Department of Biology
Introductory paper No. 11
2014
Ecology of the threatened thick-shelled river mussel Unio crassus (Philipsson 1788) with
focus on mussel-host interactions
___________________________________________________________________________
Lea D. Schneider
Department of Biology
Karlstad University
Introductory paper No. 11
2014
Contents
1.
Introduction ................................................................................................................................. 3
2.
Freshwater mussel ecology – the order Unionoida .................................................................... 5
2.1.
Sexual strategies and larval development........................................................................... 5
2.2.
The mussel – host-fish relationship ..................................................................................... 8
3.
Status and threats to freshwater bivalves................................................................................. 14
4.
Conservation strategies ............................................................................................................. 16
5.
My doctoral research ................................................................................................................ 17
6.
Acknowledgements ................................................................................................................... 19
7.
References ................................................................................................................................. 20
2
1. Introduction
Freshwater mussels (phylum Mollusca, class Bivalvia) derive from marine species and inhabit
a variety of inland waters such as rivers, streams, lakes and ponds worldwide, with the
exception of Antarctica. Generally, the most diverse mussel fauna can be found in North
America, holding one third of the world’s mussel species (Strayer 2008). Repeated invasions
of marine mussels to freshwaters have led to phylogenetically independent bivalve lineages
(Graf 2013), resulting in co-existence of non-related freshwater mussel groups such as
cyrenids (formerly the corbiculids, Bieler et al. 2010), dreissenids and unionoids (Watters
2001). Mussel colonization of different environments has induced a multitude of mussel life
history traits and physiological adaptations to various habitat conditions. The mussel
communities in large rivers, for example, are mainly represented by a variety of generalist
species that show similar patterns of adaptation to local conditions. For instance, taxa in
large rivers with hard sediments often have sculptured shells which facilitate burrowing,
while taxa living in soft substrates produce thinner and flattened shells. On the other hand,
mussels in headwater streams often have streamlined, unsculptured shells and are usually
highly habitat specific (Bauer 2001c). In addition, mussel diversity increases downstream in
watersheds, and beta diversity is greatest between headwater streams (Haag and Warren
1998).
Mussels are not only affected by habitats, but can also substantially alter the habitats they
live in. Mussels bioturbate sediments through pedal (foot) movement (Limm and Power
2011) and together with biodeposition of faeces and pseudofaeces (biodeposits) affect
nutrient dynamics and availability in freshwaters (Pusch et al. 2001). Moreover, mussel shells
increase pore space in the sediment, contributing to interstitial oxygenation as well as
sediment stabilisation. As freshwater mussels are filter feeders, they can improve water
clarity, particularly when mussels occur in high densities (Strayer et al. 1994). Furthermore,
epiphytic and epizoic organisms use mussel shells as habitat (Vaughn and Hakenkamp 2001).
Consequently, the abundance of mussels can greatly contribute to ecosystem functioning
and freshwater biodiversity (e.g. Aldridge et al. 2007, Vaughn 2010).
The high diversity of life history traits among mussels includes some specialised features. For
instance, freshwater mussels belonging to the order Unionoida have a long and complex life
cycle (usually > 10 years, Israel 1913), where most species have a larval stage that is
dependent on a fish host (Barnhart et al. 2008). The unionoid larvae attach to the gills or skin
of the fish, on which they parasitize, from a few days to around one year. After they
metamorphose to juvenile mussels they fall off the fish and sink to the sediment. They then
bury themselves into the sediment, completing development to reproducing adults within a
few to approximately 15-20 years (Fig 1). Such specialized life cycles can, although adaptive,
face a number of challenges, as both fish community structure and habitat conditions must
meet the needs of each life-cycle stage of the mussels (Strayer et al. 2004, Vaughn and
Taylor 2000, Österling et al. 2008).
3
Fig. 1 Life cycle of Unio crassus with the minnow (Phoxinus phoxinus) acting as a host fish for the
mussel larvae (glochidia). © UC4LIFE
The freshwater unionid bivalves are one of the most threatened groups of organisms on
earth. The global decline of these mussel species is probably related to both anthropogenic
activities and the complex life history traits of these mussels (Bogan 2008). For some species,
every life stage is negatively affected (Österling 2014). A lack of suitable fish hosts can impair
mussel recruitment, affecting population density, potentially leading to extinction (Zale and
Neves 1982, Arvidsson et al. 2012). Fish composition has been largely affected by
anthropogenic habitat alteration since the industrial revolution. Freshwater mussels are also
sensitive to habitat modification, water pollution, land-use change, exotic species
introductions and overharvesting (Zahner-Meike and Hanson 2001, Bauer and Wächtler
2001, Strayer et al. 2004, Österling et al. 2008, Österling et al. 2010).
Freshwater mussels have been described as keystone species in freshwater ecosystems, with
high conservation value (e.g. Vaughn and Hakenkamp 2001, Gutiérrez et al. 2003). To be
able to preserve the mussel fauna worldwide, as well as their hosts, direct conservation
strategies need to be established (Geist 2010). Therefore, knowledge about the interaction
between individual mussel species and their habitats is of utmost importance, and
particularly so the co-evolutionary link between mussels and fish hosts. Host fish assemblage
and abundance strongly determine mussel abundance and community structure (Vaughn
and Taylor 2000, Arvidsson et al. 2013). Thus, there is great need to evaluate the adaptive
mechanisms behind the parasite-host interactions, something that hitherto only has been
4
understood for a few of the thousand freshwater mussel species existing worldwide (Strayer
et al. 2004).
The objective of this introductory essay is to review the mussel – host-fish interactions of
unionoid mussels, and relate these general interactions to the threatened thick-shelled river
mussel Unio crassus (Philipsson 1788), the target species of my PhD thesis. Therefore, the
species’ life history traits are discussed in a broad context of freshwater mussel ecology. As
U. crassus is the most threatened European unionoid (Lundberg 2007), its status and threats
are summed up to be able to relate to essential research and conservation of the species. So
far, the question of the relationship between U. crassus and its hosts has only been
addressed a few times, mostly in Germany, the Czech Republic and Luxemburg. Here, the
European minnow (Phoxinus phoxinus), the European chub (Squalius cephalus) and the
bullhead (Cottus gobio) have been identified as major host fish species (e.g. Bednarczuk
1986, Maaß 1987, Hochwald 1997, Thielen 2011, Douda et al. 2012, Taeubert et al. 2012a).
However, it has also been shown that the host fish use varies between different drainage
areas and their fish populations (e.g. Hochwald and Bauer 1990, Taeubert et al. 2012a).
Wengström (2009), for example, reported on mussel population with successful recruitment
where minnow, chub and bullhead were absent. This indicates a need for further research
clarifying the relationship between mussels and fish for the entire mussel distribution area,
so that one can establish conservation strategies for mussels and fish. My doctoral research
will be presented at the end of this introductory essay.
2. Freshwater mussel ecology – the order Unionoida
In this chapter, I provide an overview of the general life cycle of freshwater mussels, along
with specifications for each life cycle stage for U. crassus. First, I discuss sexual strategies and
larval development which secondly is followed by a discussion of the mussel – host-fish
relationship.
2.1. Sexual strategies and larval development
Having derived from marine mussel species, all three freshwater mussel lineages (cyrenids,
formerly the corbiculids, Bieler et al. 2010; dreissenids and unionids) developed their mode
of reproduction from oviparous broadcast spawning towards ovoviviparity and even
euviviparity. Thus, in contrast to their marine ancestors that cast out sperms and eggs
separately in free flowing water resulting in external egg fertilization and development of
planktonic veliger larvae, freshwater mussels adopted parental care (i.e. brooding).
Accordingly, female mussels keep their eggs in the marsupium for fertilization by filtered
sperms. Egg development in euviviparous mussel species, mostly sphaeriids (227 spp., 19%
of the mussel species worldwide; order Veneroida), occurs in eggs poor in yolk where
nutrients are provided over the maternal marsupium tissue (Korniushin and Glaubrecht
2003). Here, no larval stage can be found but “crawl-away juveniles”. Most unionoids (681
5
spp., 57%) represent ovoviviparous mussel species which brood their larvae in yolk rich eggs
until transformed to larvae, which, unlike the marine veliger larvae are host fish dependent.
Particularly in streams, the abolishment of the free-swimming larvae can be regarded as an
evolutionary adaptation to lotic waters, where drift can be maladaptive (Graf 2013).
Compared to e.g. the sphaeriids that produce few offspring, the fertility of unionoids is
generally high and probably a “result of the adoption of a parasitic life style” (Watters 2001).
Thus, fertility depends on the species’ reproductive mode. Unionoid mussels that produce
small larvae (e.g. Margaritifera margaritifera, the freshwater pearl mussel, FPM), for
example, show higher fertility than mussels producing large larvae (e.g. Anodonta spp.), as
energetic trade-offs do not allow for producing large and numerous larvae (Bauer 1994).
Additionally, a general positive relation between fecundity and age/size has been found for
many mussel species (Bauer 2001). However, food supply and temperature are important
factors affecting fitness. The long-living and slowly growing headwater stream species FPM is
generally highly fecund, but shows considerable variation in larval production for all age
classes. This trait has also been observed for U. crassus, which usually occurs downstream of
FPM habitats in watersheds, albeit U. crassus produces higher developed larvae before
expulsion in free flowing water (Hochwald 1997). Variations in larval production may be
explained by the level of fitness of each individual rather than by size/age relations (Bauer
1998). Furthermore, the degree of egg fertilization can fluctuate greatly. Hochwald and
Bauer (1990) observed about 10% undeveloped eggs in gravid female U. crassus even at high
mussel density. The authors explain this as natural failure rate during egg development, or
because sperm concentration is below a critical level. Sperm provision is therefore, together
with female fertility, an important parameter for successful mussel population recruitment.
Most unionoids are diocious, i.e. the sexes are separate (Kat 1983). Nevertheless, many
species are believed to switch to hermaphroditism when population density is reduced, as
e.g. the Australasian Hyriids (Walker et al. 2001), the FPM (Bauer 1987, but see Österling
2014) and the Anodonta species (Bauer 2001d) in Europe. Representatives of strictly
diocious species are the North American Anodonta species A. corpulenta, A. gibbosa and A.
wahlamatenis (Heard. 1975) and U. crassus in Europe, where the sex ratio is described as 1:1
(Hochwald and Bauer 1990). Generally, eggs are transported from the gonads via the
oviduct, through the genital aperture into the cloaca to the gills where they get fertilized by
sperm released by male mussels situated upstream of the females in lotic freshwaters (Coker
et al. 1921).
One or both pairs of gills of female unionoids are used as breeding pouches, or marsupium,
for eggs. In gravid mussels the marsupium appears swollen (Harms 1909). Margaritiferids
hold the least developed demibranches (gill structures) among all mussel species worldwide
as they brood their eggs in all four gills (tetragenous) and consequently have reduced
filtration capacities (Bauer 2001c). Other species do not have this problem as they have their
marsupium in either the outer (ectobranchious) or the inner (endobranchious) gills.
6
Anodonta and Unio species, to which U. crassus belong, use the ectobranchious breeding
pouches whereas Etherioidea, occurring in the tropics of America and Africa, use the
endobranchious demibraches. Partial use of inner or outer gills is found in the family
Hyriidae and the genus Lampsilis which is regarded as advanced brooding strategy.
Furthermore, it seems that many unionoid mussel species (except etherioids) can vary the
amount of brood according to their level of fitness (Hochwald 2001). Thus, reduced filtration
rate due to brooding activity generally causes a challenge for energetics which, however can
be adjusted by regulating the extent of larval production.
There are two larval types within the order Unionoida, the lasidium and the glochidium. The
lasidium type of larvae is found in the superfamily Etherioidea. Lasidia development to
young mussels can either be similar to glochidia development where the egg develops to a
larva metamorphosing to a young mussel in a host cyst, or can continue through a second
larval stage, the “haustorium” which finally develops to a young mussel (Parodiz and Bonetto
1963). Additionally, some American mussel species show direct development from egg to
young mussel without any larval stage (e.g. Anodonta inbecilis) (Wächter et al. 2001). The
term “mussel larvae” will henceforth be used interchangeably with “glochidia”, while
information on lasidia will be specified explicitly. The glochidia larval type is found in the
superfamily Unionoidea (Bauer 2001a) which represents about 80% of the Unionoida
(Barnhart et al. 2008), comprising three families, the Unionidae (the largest family), the
Margaritiferidae and the Hyriidae (Strayer 2008). In Sweden, only the FPM (EN) belongs to
the Margaritiferidae, whereas three Unio spp. (U. crassus (EN), U. tumidus and U. pictorum
(NT)) and three Anodonta spp. (A. cygnea, A. anatina, Pseudanodonta complanata (NT))
belong to the family Unionidae (IUCN Red List Categories: EN, endangered; NT, near
threatened; Bjelke et al. 2010). The distribution area of Hyriids is restricted to South America
and Australasia (Bogan 2008).
Breeding strategies have been divided into long- (brachytictic) and short-term (tachtictic)
breeders (Lefevre and Curtis 1910). Long-term breeders keep their larvae in their marsupium
from fall until spring the year after (e.g. Anodonta imbecilis, Heard 1975; A. cygnea, A.
anatina, Harms 1909). This leads to relatively large (~400µm) and morphologically wellequipped triangular shaped larvae carrying a larval thread (Wächter 2001). In contrast,
short-term breeders release their small (~50µm) and less developed spherical glochidia a
few weeks after fertilization (e.g. the FPM, Wächter et al. 2001; Anodonta gibbosa (Heard
1975). Interestingly, U. crassus lies in between those two breeding strategies, with egg
fertilization in spring and release of medium-sized glochidia (~200µm) during late spring and
summer (Bednarczuk 1986). U. crassus is nevertheless regarded as a short-term breeder and
is capable of reproducing up to five times per year (Hochwald 2001) which has not been
observed in other European species. Interestingly, reduced fertility has been found for older
U. crassus females at later spawning events (Hochwald 1997). From an evolutionary
perspective, this indicates that U. crassus has developed a reproduction strategy where
7
larvae are spread over extended time periods, potentially to extend the time span for larvae
to encounter suitable host fish.
In summary, freshwater mussels evolved different sexual strategies and larval
developments, where they have maximized offspring number with the smallest energetic
cost. Which reproductive strategy the different mussel species adapted over time depends
on the freshwater habitat that was colonized. The imposed selection pressure after the
invasion of marine species to freshwaters, however, led to a shared adaptation of a parasitic
life stage on fish within the order Unionoida (Graf 2013). Despite this common adaptation,
individual interactions between fish and mussels depend on fish community structure, fish
behaviour and habitat and have led to a variety of interactions between mussel species and
their hosts.
2.2. The mussel – host-fish relationship
Mostly, unionoid mussel larvae (glochidia) are obligate parasites on host fish. Without a
suitable host, mussel larvae cannot develop and metamorphose into juvenile mussels.
Consequently, glochidia die within a few days in the absence of hosts, depending on mussel
species and temperature (Zimmerman and Neves 2002). According to Jansen et al. (2001)
the highest glochidia mortality occurs after larval release from the adult mussel. This is also
due to the fact that none of the larvae types are capable of locomotion (Lefevre and Curtis
1910), which decreases the likelihood of getting in contact with a suitable host. Also, this
excludes selective host fish choice by the larvae (Bauer 2001b). Most mussel species
compensate this dilemma by producing high numbers of larvae (Wächter et al. 2001) and/or
reproducing several times per year, releasing their larvae asynchronously within the
population, as is the case for U. crassus (Hochwald 1997). Hastie and Young (2003) state that
larval release may be triggered by environmental cues, causing synchronized events in FPM
populations. This timing may depend on temperature and follow an effect of thermal
summation. However, fish presence and odours may also be used as cues to time larval
release with host presence to increase infestation success (Jokela and Palokangas 1993).
Thus, it seems that evolutionary adaptations of mussels include both high numbers of larvae,
and larval release that is synchronised to host presence.
Host fish attraction by adult unionoid mussels is an evolutionary adaptation facilitating host
encounter, serving to decrease glochidia mortality (Strayer et al. 2004). Examples of visual
attraction include moving lures, which are modifications of the mantle margin, imitating fish
or macroinvertebrates (e.g. Lampsilis spp.), or filamentous egg conglutinates mimicking
worms. Moreover, transparent mucus structures, formed out of larvae, can look like small
fish and lure foraging fish (Wächter 2001). The above host fish attraction strategies have not
been described for European species. However, a so called spurting behaviour has been
observed for the European species Pseudanodonta complanata (Hazay 1881) in Germany
and U. crassus in Germany and Switzerland (Vicentini 2005; Beckmann 2007; Zettler and
Jueg 2007), where the adult female mussel crawls to the stream edge, adjusting its posterior
8
end above the water level so that glochidia can be ejected up to one meter over the stream
surface. Fish are probably attracted by the water splash, mistaking it for prey, and are
infected upon foraging attempts. So far, spurting behaviour has not been seen for any
Swedish freshwater mussel (personal communication Stefan Lundberg, Naturhistorska
riksmuseet Stockholm 2013). Furthermore, glochidia attachment can be improved when
larvae are equipped with an attachment thread. First, the thread reduces sinking rate of
individual glochidia by 30%, and secondly it links together multiple larvae in a line. Thus, one
larvae that attaches to a fish tow further larvae increasing infestation success (Jansen et al.
2001). Mussel species in lotic habitats are often threadless (e.g. M. margaritifera, U. crassus,
P. complanata) whereas lentic species A. anatina, U. tumidus and U. pictorum carry threads
(Wächter et al. 2001).
The position of attachment of mussel larvae on a fish is determined by extrinsic conditions
such as water current and shear stress, as well as intrinsic conditions as fish behaviour and
anatomy, but also larval morphology (Wächter et al. 2001). Hooked glochidia can attach to
gill filaments and to external parts of the fish, particularly to opercula and fins (Arey 1932b).
In spite of U. crassus glochidia having hooks, encapsulation of larvae fixed on the fish’s body
surface is rarely successful, and it leads to higher mortality than when glochidia attach to the
gills (Hochwald 1997, Engel 1990). Glochidia without hooks (e.g. FPM) are mainly gill
parasites (Harms 1907a).
The encapsulation (interchangeably with encystment) of mussel larvae that attach to fish
fins or rays has been described as wound closure, a reaction induced by lesion of blood
vessels and performed by host epithelial cells (Arey 1932a). Encapsulation speed varies
depending on mussel and fish species and fish condition, and has been estimated to take six
hours for both FPM (Scharsack 1994) and Unio glochidia (Maaß 1987). Encapsulation can
also occur if larvae attach to non-hosts, but here the cyst formation shows more
irregularities than when larvae attach to suitable hosts. Also, the glochidia can be killed due
to cellular defence, with subsequent expulsion within one day, after which a healing process
starts immediately in the fish tissue (Arey 1932a, b). Attachment of a mussel larva on a
suitable host mostly leads to encapsulation, enabling successful metamorphosis from
glochidium to juvenile mussel. The process of juvenile release from the host fish after
metamorphosis has yet to be fully clarified. Several authors propose that the juvenile mussel
mechanically releases itself by pedal movement causing cyst rupture (e.g. Lefevre and Curtis
1910, Wächter et al. 2001), whereas Dodd et al. (2005) suggest that the host fish tissue
retreat due to histolytic processes triggered by the juvenile. A search of the literature
showed that there are few studies of the encapsulation, and particularly the release process
of glochidia from fish tissue. A better understanding of the inner cellular substances
participating in these processes could help explain why successful metamorphosis mostly
occurs in fish gill tissue and fewer on fins, or why non-suitable hosts expel mussel larvae
while suitable fish tolerate glochidia infestation over different periods of time.
9
Generally, the duration of the parasitic phase varies greatly depending on mussel species
and breeding type (Bauer 2001c), but also on host fish species and quality and tissue type
(Levine et al. 2012). Taeubert et al. (2013a), for example, measured slower metamorphosis
when FPM larvae were attached to gill rakers than to gill filaments, which they ascribed to
lower nutrition supply in gill-raker tissue. Moreover, many studies have shown that water
temperature is an important parameter influencing the rate of metamorphosis (e.g. Harms
1907a, Lefevre and Curtis 1910). For U. crassus, Bednarczuk (1986) reported juvenile mussels
after a 27-28 days parasitic stage on Squalius cephalus, Scardinius erythrophtalmus and
Perca fluviatilis, without reference to water temperatures. The results of Hochwald and
Bauer (1990), however, show successful metamorphosis on fish hosts Squalius cephalus,
Phoxinus phoxinus and Cottus gobio after 28 days in 12 °C. At this temperature, U. crassus
glochidia metamorphosed within 36-52 days in the experiment of Taeubert et al. (2013b),
who tested the host Phoxinus phoxinus, at three temperatures. In their experiment,
parasitism duration decreased with increasing temperature; metamorphosis occurred
already after 11-15 days when fish were kept at 23°C. However, the lowest glochidial
mortality was reported at 17 °C (16-28 days to metamorphosis) and consequently this
temperature has been proposed as the optimum temperature for successful
metamorphosis.
Whether the term “infection” defines the parasite-host interaction for freshwater mussels
and their host fish correctly, has lately been discussed lively, mainly based on a lack of
knowledge of the harm to hosts. However the word “infection” originally was used to
describe a medical infection by bacteria, fungus or virus, “localised as in pharyngitis, or
widespread as in sepsis, and are often accompanied by fever and increased number of white
blood cells” as described by the American Heritage® Science Dictionary. As glochidial
infestations are not infectious, researchers at a symposium (International Meeting on
Biology and Conservation of Freshwater Bivalves in Bragança 2012) suggested substituting
the term “infection rate” to “encystment rate” or “attachment rate” (anonymous reviewer).
Important to mention is that fish mortality has only been observed when fish have been
subjected to large numbers of glochidia under artificial laboratory conditions, i.e. not in
nature (Lefevre and Curtis 1910, personal comment Österling 2014). However, evident harm
to fish due to overinfestation under semi-natural conditions was found in a salmon farm
located downstream of a FPM location in West Norway, where mussels occurred in high
densities. In either case, larval metamorphosis success obviously requires both nutrients and
energy, which, according to Jansen et al. (2001), suggests a negative effect of mussel larvae
on fish hosts. Thomas et al. (2013) allude to a respiratory burden for fish when glochidia
attach to gills, whereas no other serious physiological effects could be observed. However,
glochidia are equipped with a mushroom body, formed by mantle cells, which are “the
primary sites of intracellular digestion of the larval adductor muscle and host tissue during
metamorphosis” (Fisher and Dimock 2002). This indicates that host tissue digestion takes
place and cause harm to fish. Mechanical harm to hosts may also occur when glochidia grow
on the fish gills, especially if they have a long parasitic stage, e.g. as with FPM growing from
10
70 to 400-500µm during nine months of parasitism (Bauer 2001c). This is not the case for U.
crassus glochidia, as their pre-parasitic size is about 200µm and growth is only about 2.5 to
4.0% during 28 days before hatching from fish (Täubert 2012b). U. crassus is, on the other
hand, equipped with hooks that may increase the physical harm to the host.
Fish can expel glochidia that are attached to fish tissue, a reaction that has been described as
an immune response with antibody production against glochidial tissue (e.g. O’Connell and
Neves 1999). This immune response depends on fish body condition at infestation (Frost
1943) and if the fish has been infested before (Jansen et al. 2001). Details about how this
defence mechanism works from a physiological point of view are not well understood. There
seems to be two types of immunity, natural and acquired immunity (Arey 1932a). Fish
without natural immunity, or fish that have not yet acquired immunity, can be considered as
suitable hosts. It is however still unclear how the immune response is linked to the
encapsulation rate. For conservation purposes, it would be interesting to know if there is an
optimal encapsulation rate that minimises the immune response and optimises glochidial
transformation (Dodd et al. 2005). The results of Hochwald (1997), who investigated
glochidial survival of U. crassus larvae on European minnows (P. phoxinus), indicate lower
glochidial mortality when fish were highly infested. Similar results were obtained from the
common rudd (Scardinius erythropthalmus) when the fish had previously been infested with
glochidia from Anodonta anatina. This suggests that high infestation rates depress the
immune system of fish. Furthermore, many studies suggest that older fish, which are more
likely to have had a previous encounter with mussel larvae are less suitable for successful
mussel metamorphosis even though they have large surface areas where larvae can attach
(e.g. Arey 1932a, Bauer 1987, Blažek and Gelnar 2006, Strayer 2008). Hochwald (1997),
however, did not find a difference in glochidia mortality rate when comparing minnows (P.
phoxinus) that had been infested one or two times, nor was there an effect of fish size or
age. This may indicate that P. phoxinus may be an ideal host for U. crassus, albeit U. crassus
has more than one host. Taeubert et al. (2012a), for example, concluded that there are at
least three popular hosts for U. crassus in the Danube drainage: P. phoxinus, the European
chub (Squalius cephalus) and the European bullhead (Cottus gobio). Interestingly, there are
additional fish species that act as hosts for U. crassus in other drainage systems (Tab 1).
Host fish mapping is a method to describe the geographic distribution of the mussel and its
different host species. A complete host fish evaluation requires one to consider the endpoint
of metamorphosis success i.e. the proof that juvenile mussels hatched from fish. Fish should
therefore not only be caught in nature to investigate glochidia encapsulation rate, but
should also be caught and transferred to laboratories where metamorphosed juveniles can
be collected from natural and/or artificially infested fish (Taeubert et al. 2013c). Thus,
observations of natural encystment rates on “ecological hosts” in mussel streams are equally
important as lab experiments assessing “physiological hosts” (Levine et al. 2012).
11
Fish species
Alburnoides bipunctatus
Alburnus alburnus
Acipenser ruthernus
Carassius carassius
Chondrostoma nasus
Cottus gobio
Gasterosteus aculeatus
Gobio gobio
Gymnocephalus cernua
Leucaspius delineatus
Leuciscus idus
Lota lota
Neogobius melanostomus
Onchorynchus mykiss
Perca fluviatilis
Phoxinus phoxinus
Pungitius pungitius
Rhodeus serioeus
Rutilus rutilus
Salmo trutta
Scardinius
erythrophythalmus
Squalius cephalus
Tinca tinca
Suitable
W
T(+)
T(-), H, LB
T(-), E
M
M
Not suitable
T(+)
T(-)
T(-)
M
B
M
T(-)
W
T(-)
T(-), B
T(-), B, M
T(+), H, HB, M, LB
E
B, W
E
T(-)
T(-), M
T(+), M, HB
Tab. 1 Fish species tested
as hosts for U. crassus and
categorized suitable or not
suitable according to the
following authors: B,
Bednarczuk (1986); E, Engel
(1990); H, Hochwald (1997);
HB, Hochwald and Bauer
(1990); LB, Lundberg and
Bergengren (2008); M,
Maaß (1987); T, Taeubert
et al. (2012a, b); W,
Wengström (2009). (+) and
(-) indicate higher and
lower host quality
according to Taeubert
2012a, b.
T(+), M
T(+), B, E, M
B, M
The number of fish species used varies depending on whether the mussel species is a hostfish generalist or a host-fish specialist (Strayer et al. 2004). Host generalists such as the
North American mussel Cumberlandia monodonta, found in downstream parts of
watersheds, can parasitize up to 36 fish species (Strayer 2008). Host specialised mussels,
mostly occurring in headwater streams only use one or a few host species, e.g. the FPM
using only brown trout (Salmo trutta) or Atlantic salmon (Salmo salar) as hosts. Host fish
range also increases with mussel larvae size, independent of species, as large larvae often
are equipped with hooks enhancing adherence on tissue, suggesting why e.g. Anodonta spp.
with its relative large larvae use many hosts (Bauer 2001c). Non-host-specialised mussels
mostly use co-occurring, local fish species independent of fish taxonomy (Barnhart et al.
2008). U. crassus seems to be a host generalist rather than a host specialist, but could not be
accurately classified as a specialist or a generalist, as they parasitize on several but not all of
the fish species in the assemblage (Hochwald 1997). However, to be able to understand why
only certain fish species act as hosts, physiological and behavioural aspects of both the
mussel and the fish needs to be taken into account.
12
Fish behaviour plays an important role for infestation success, as some fish species remain
at mussel locations only during e.g. foraging, migration or spawning. The spawning season of
the European minnow, for example, overlaps with the reproductive timing of U. crassus
(Frost 1943). The benthic bullhead is also exposed to mussel glochidia, but seems
comparably less vulnerable to infestation, probably since the opercula cover the gills more
completely in bullheads. Bullheads may still act as important hosts for U. crassus (Lundberg
et al. 2007) as they may occur at very high densities in small streams, particularly (Mills and
Mann 1983). As bullheads have relatively small home ranges (Knaepkens et al. 2004), they
probably lead to small-scale dispersal for parasitic larvae, whereas migratory hosts such as
the European chub may transport mussel larvae to different habitats over extensive
distances. Fish behaviours contribute to mussel infestation probability and dispersal.
The main dispersal mechanism for mussels is mediated by transportation of parasitic mussel
larvae on host fish, and is even mentioned as the greatest benefit for mussel larvae in the
parasite-host relationship (Barnhart et al. 2008). Generalist mussel species, with large host
fish ranges, have potentially higher chances to be transported to different habitats, and
migratory fish can spread juvenile mussels over long distances. Downstream drift by mussel
larvae released from the maternal marsupium can also act as mussel dispersal, but the brief
life span of expelled mussel larvae limits this as an efficient dispersal mechanism. Adult
mussels can also disperse, by horizontal movement with up to 5m in 4 weeks for U. crassus,
mostly directed upstream (Körner 1998-2001). Here, higher activity has been found for adult
mussels 4 years of age in search of suitable habitats (Lang 1998). This adult movement
should constitute a minor dispersal vector compared to that of glochidia on fish.
Adult mussels are also capable of vertical movement. During winter, mussels often stay
completely buried in the sediment, or just underneath the bottom surface with only the
siphons visible (Baumgärtner and Heitz 1995). Vertical mussel distribution has been
described to occur in different layers with a tendency for larger and older mussels sitting
near the surface, above smaller and younger mussels (Trudorancea and Gruia 1968). It is
assumed that a sediment depth of 35-50cm can be reached by freshwater mussels,
particularly by younger and thus smaller individuals (Jungbluth 1993). U. crassus has been
found as low as 30cm below the sediment surface (Engel 1990). Temporal decreases in
vertical movement activity can be seen during the reproductive season of adult FPM, when
mussels can be found at the sediment surface. Particularly female mussels remain on top of
the sediment with the siphons wide open. This facilitates the intake of free-flowing sperm
needed for egg fertilization, as well as it enhances oxygen provision. In this way, female
mussels get enough oxygen even though the filtration rate is reduced due to marsupial
brooding (Harms 1907b).
Vertical movement occurs also in juvenile mussels when they migrate into the river
sediment after having fallen off their host fish. A relatively long foot enables burying and
high movement capacity. In the hyporheic interstitial zone, juveniles seek refuge from
13
predators such as fish or crayfish (Strayer 2008), and search for food such as detritus, algae
and bacteria. During the early post-parasitic stage, juveniles pedal feed as their gills have not
yet been developed (Wächter 2001). Therefore, cilia creating a water flow transporting food
items to the digestion system cover the foot. Juvenile mussels do not emerge to the
sediment surface until having fully developed into sexually mature filter feeders (Coker et al.
1921).
3. Status and threats to freshwater bivalves
Drastic habitat destruction and modification of freshwater ecosystems have followed man’s
increased economic status and standard of living since the industrial revolution in the 18 th
and 19th centuries (Bogan 2008). Freshwaters are particularly adversely affected by major
threats, including (I) destruction or degradation of habitat, (II) flow modification, (III) water
pollution, (IV) overexploitation and (V) invasive species (Dudgeon et al. 2006). Among those,
dam construction for hydroelectric power or mills represents one of the most serious threats
to lotic freshwaters, as it disrupts the four-dimensional nature of running waters (Ward
1989), and their ecological connectivity in particular (e.g. Calles and Greenberg 2005,
Mueller et al. 2011). Dams also cause changes to water levels and flow. Forestry including
clear-cutting is a wide-spread threat to running waters (Österling et al. 2008, 2010) as it
generates habitat degradation causing destabilization of bottoms, particularly in the riparian
zone, where trees and floodplains are removed. Eutrophication of whole river systems often
follows use of manure in high concentration, which cannot be buffered if floodplains are
absent. Additionally, canalization increases the access of non-buffered pollutants to
freshwaters, as well as erosion and fine sediment loads (Geist 2011), all contributing to a
global decline of freshwater molluscs, including bivalves (Lydeard et al. 2004, Österling and
Högberg 2014). According to Freyhof and Brooks (2011), many fish populations are also
threatened due to the anthropogenic land-use change, particularly due to pollution and
migration obstacles, conveying negative consequences for mussels with parasitic stages.
Furthermore, the introduction of alien species, such as the Eurasian zebra mussel (Dreissena
polymorpha) and the Asian clam (Corbicula fluminea), causes high competition between
invasive and native mussel species, with potential for extinction (Ricciardi 1998, Yeager et al.
1999). Overexploitation of mussels caused huge population declines (Strayer at al. 2004) as a
market for the mother of pearl and pearls started blooming in the 16th century (Strayer
2008). Here, decorative art and expensive pieces of jewellery were made out of the shiny
mother of pearl and pearls produced by some mussel species as a dirt-encapsulation
reaction (e.g. FPM) (Lozoya and Araujo 2011).
Prior to the 19th century, mussels (e.g. the Unio species) still occurred in such high
population densities that the mussels were fed to pigs and chickens, and shells were used as
fertiliser (Baumgärtner and Heitz 1995). Today, freshwater molluscs is the most imperilled
14
taxonomic group both in Europe (Cuttelod et al. 2011) and globally (Bogan 2008). The
reasons for the mussels’ high sensitivity to anthropogenic habitat alterations are directly
linked to their ecology, i.e. the mussels’ complex life history traits. Acute toxicity or dredging
can negatively affects all individuals in a population. Additionally, mussel larval survival
depends on availability of suitable host fish, and a lack of hosts can lead to mussel
population decline. According to Haag and Warren (1998) the variability of fish community
structure, combined with the host fish infestation strategy by mussels, can have a greater
impact on mussel community structure than habitat structure and variability. They also
conclude that mussels that are host specialists and lack fish-attraction strategies suffer most
from low host densities, in contrast to generalist mussel species with the ability to attract
hosts.
Juvenile mussels are highly sensitive to pollution, eutrophication and clogged sediments with
low oxygen concentrations (Jungbluth 1993). As juveniles are not able to choose their
habitat when hatching from hosts, they are dependent on overall good sediment quality
(Nagel and Badino 2001). High fine sediment loads in freshwaters due to e.g. agriculture,
forestry, canalization or damming can cause juvenile mortality (Österling et al. 2010).
Investigating recruitment failure for U. crassus, Hochwald and Bauer (1990) argue that high
values of nitrate that can convert to nitrite at anoxic conditions is toxic for juveniles.
Therefore, different nitrate thresholds have been prescribed for juvenile survival (Engel
1990, Hochwald and Bauer 1990), but still need to be confirmed in detail (e.g. Denic et al.
2013, Strayer 2012, 2014). Hence, the postparasitic juvenile phase may be a very critical
stage in the mussels’ life cycle (Jansen et al. 2001).
Another local threat for unionoid mussels is the muskrat (Ondatra zibethicus) predation.
Owen et al. (2006) studied the impact of this semi-aquatic rodent, native to North America,
on mussel community. They concluded that muskrats negatively affect species composition,
population size and age structure as it is mussel size and shape selective. However,
compared to southern and central Europe, where the muskrat has spread rapidly since the
early 20th century causing drastic mussel population declines, the muskrat in North America
and western Europe has natural predators such as mink (Mustela vison), bob cat (Felis rufus),
red fox (Vulpes vulpes) or coyote (Canis latrans), controlling the muskrat populations. In
these regions, the muskrat has also been hunted for its fur. In Europe, U. crassus is the
muskrats’ target mussel species, compared to e.g. Anodonta anatina and Unio pictorum
(Zahner-Maike and Hanson 2001). Even though the muskrat does not eat every individual of
a population, it may severely reduce mussel density. Together with other threats mentioned,
this can lead to allee effects in sparse populations.
Allee effects include elevated extinction probability below threshold or critical population
sizes (Vaughn 2012). As soon as the population size of mussels decreases, factors regulating
successful recruitment can be adversely affected. This may be impoverished sperm
availability in male-reduced populations as well as sperm dilution effects from low
15
population densities leading to great distances between males and females (Strayer 2008).
To counteract allee effects, mussels may aggregate, the two sexes mate and
hermaphroditism becomes common in some species (e.g. FPM). Therefore, some authors
(cited in Strayer 2008) claim that a limited population size does not affect reproduction due
to lack of sperm i.e. limited fertilization. However, Hochwald and Bauer (1990) did not
observe hermaphroditism or that males and females approached in U. crassus populations
and therefore suggest that U. crassus populations suffer severe extinction risk when the
population size falls under a certain threshold. Here, a danger of inbreeding occurs in small
populations suffering under a component allee effect that occurs when there is a positive
relationship between any measureable component of individual fitness and population size
or density (Berec et al. 2006). Thus, conservation programs for endangered mussel species
focusing on breeding and culturing of mussels should carefully take into account inter- and
intra-population genetic patterns and “maintain the genetic identity of evolutionary
significant units (ESUs) and conservation units (CUs)” (Geist 2011).
4. Conservation strategies
Ecological knowledge about mussel – host-fish interactions is of crucial importance when
working towards conservation of large freshwater mussels (Taeubert et al. 2012a). Host-fish
mapping should take into account research on the fish immune reaction due to glochidia
infestation and co-adaptation between mussels and fish (O'Connell and Neves 1999, Jansen
et al. 2001, Dodd et al. 2005). In other words, research on the relationship between mussels
and their host fish may help to adjust stream restoration incentives according to species
habitat requirements (Zale and Neves 1982), including removal of migratory obstacles for
fish (Vaughn and Taylor 2000).
Additionally, re-meandering of channelized streams including re-establishment of
floodplains is, for example, a suitable method to improve habitat quality for a variety of
freshwater organisms as it can contribute to reduced erosion, stabilization of sediments,
buffering of nutrient loads from agriculture and diversification of in-stream flow regimes, to
mention a few possible positive effects (Roni and Beechie eds. 2012). Here, specific
parameters as e.g. substrate heterogeneity or flow regime can be adjusted to meet the
needs of the mussel and host fish.
Re-introduction of mussel species in streams where populations have been extinct or where
mussel populations are decreasing can be performed by stocking of infested host fish
(Zettler and Jueg 2007). Juvenile hatching rates from infested host fish as well as mussel
survival are crucial parameters for evaluation of re-introduction efficiency. Suitable
monitoring methods are needed, and the small size of juveniles after metamorphosis,
around 200-500µm, poses serious challenges to developing such a monitoring program.
Often, one needs to wait several years before being able to evaluate the outcome of a re16
introduction by estimating the number of mussels emerging from the interstitial sediment to
the riverbed surface. As research and conservation projects rarely have time to wait so long,
captive breeding programs have been established (Lefevre and Curtis 1912). Here, juvenile
mussels, developed on artificially infested hosts, are hatched and reared in the laboratory
until the mussels reach an age and size that can be easily spotted in rivers. This has been
conducted successfully for many North American (e.g. Barnhart 2005) and two European
species (reviewed by McIvor and Aldridge 2008), and so far once for U. crassus in
Luxembourg (Eybe and Thielen 2010). The reared mussels are usually transferred to
watersheds, after marking them in the lab to enable identification in nature and evaluating
re-capture success. Marking methods like waterproof colour marking (Hochwald 1997),
engraving (Barnhart 2003), and PIT (passive integrated transponders) tagging (Hua et al.
2012) have been used. Recent development also includes fluorescent marking of juvenile
mussels. However, this technique needs to be improved as low survival prevails (Lavictoire
2012). Engel (1990) conducted a survival study using mesh-covered hole plates, later known
as “Buddensiek cages” (Buddensiek 1995), which were attached to tree roots slightly above
the stream bottom. Thus, instead of marking juveniles, the small mussels could be recaptured as they were held in individual compartments. Unfortunately, juvenile survival rate
was greatly reduced due to clogging of the mesh, in spite of repeated cleaning. In other
words, techniques for juvenile re-capture are needed as they would tremendously promote
research on juvenile mussel ecology, e.g. habitat requirement, foraging and survival.
Furthermore, research is essential for mussel conservation as mussel propagation programs
can be created more cost-effective focusing on juvenile re-introduction and reducing the
effort in captive breeding.
5. My doctoral research
The aim of my dissertation is to investigate mussel-host interactions for U. crassus,
considering the complex mussel life history traits. Few studies have hitherto been conducted
on U. crassus, particularly in Swedish rivers, in spite of that, the need to preserve this
national and pan-European endangered species is urgent, approved and prioritized. To
facilitate the development and establishment of conservation programs, I address the
following questions: (1) Which host-fish species are used by U. crassus in Sweden? (2) When
does U. crassus reproduce, and are timing and encapsulation rates linked to fish host size
and/or fish/mussel densities? (3) Is glochidia release by female U. crassus dependent on
temperature and host fish presence? (4) Does host fish suitability differ between streams
and does co-adaptation influence the juvenile metamorphosis success? (5) How high is
juvenile survival when re-introduced in natural habitats?
1. Identification of fish species used as hosts by U. crassus is an essential part of the studies
of mussel-host interactions and improves conservation actions for mussels and host fish.
17
Hence, fishing will be conducted within the species distribution area in Sweden along a
north-south gradient. Seven mussel streams located in the Region of Skåne, Blekinge,
Jönköping, Östergotland and Södermanland will be sampled during the reproduction
season of U. crassus. Preserved fish will be examined for glochidial infestation in the
laboratory wheareas ITS rDNA analyses of single glochidia will help identifying U. crassus
and separating the species from other co-occurring mussel species in the streams. This
study will be combined with investigations of excystment of juvenile mussels from
naturally infested fish enabling evaluation of fish species suitability as “ecological hosts”.
2. Assessment of the reproductive period of U. crassus will help us to understand the link
between changes in temperature, host fish presence and host infestation with mussel
spawning events. My investigations will therefore include comparisons of the
proportions of gravid mussels, their size and repeated spawning across mussel densities.
Host quality will be evaluated by means of natural encystment rates on local host fish
species electro-fished which will be referred to both host and mussel density.
Hypothetically, the temporal dynamics of natural infestations should respond to gravidity
dynamics. Moreover, fish host size-dependent capacity to carry glochidia will be
investigated.
3. Water temperature is a factor known to have an impact on the release of glochidia
larvae. An ability to sense the presence of host-fish may also be a mechanism that
triggers larval release of female mussels and result in high infestation. In my third study, I
address the question if larval release of gravid U. crassus females is affected by host-fish
presence and water temperature, or a combination of both. I will investigate the timing
of glochidia release from gravid mussels in treatments with and without fish presence at
three water temperature levels simulating cold, intermediate and warm temperatures at
the early reproduction season of U. crassus.
4. The relationship between mussels and fish will additionally be investigated by means of
artificial infestation of fish under standardized aquarium experimental conditions. Here, I
question if U. crassus is a host generalist or specialist and if host fish species suitability
varies between drainage areas. During these laboratory studies the infestation rate of
mussel larvae on fish will be followed over the parasitic stage and the juvenile
metamorphosis success quantified which enables evaluation of host functionality. Also,
by investigating infestation and survival rates of mussels on sympatric and allopatric host
fish species, common garden experiments will aim to evaluate if mussels in separate
catchments have adapted locally to catchment-specific fish host composition. Moreover,
fish that are infested with mussels under known, laboratory conditions and infestation
rates will be evaluated for re-infestation rates, where possible immune responses in fish
can reduce infestation rates in a second infestation round.
5. Studies of habitat requirements of early mussel life cycle stages such as fertilized larvae
on adult mussels, encysted larvae on host fish and free-living juvenile mussels are
18
essential prerequisites for conservation programs focusing on mussel re-introduction.
Therefore, I will conduct research in two habitat restored rivers where U. crassus shall be
re-introduced. Gravidity of re-introduced adult mussels with origin in mussel streams will
be investigated by means of standardized methods. Compatibility between the parasitic
stage of U. crassus and potential host fish species from the two rivers will be evaluated
by means of artificial infestation of fish under standardized experimental conditions.
Juveniles hatched in these laboratory experiments will be re-introduced into the restored
rivers and monitored for survival and growth. Survival and growth of juvenile mussels
introduced in their native rivers, which have recruitment of juvenile mussels, will serve
as controls.
6. Acknowledgements
My PhD research is funded by the European Commissions’ LIFE program fund and FORTUM.
I would like to thank Ivan Olsson for initiating and managing our project UnioCrassusforLIFE.
For more information, please visit: www.ucforlife.se.
19
7. References
Aldridge, D. C. et al. 2007. Freshwater mussel abundance predicts biodiversity in UK lowland
rivers. - Aquatic Conserv: Mar. Freshw. Ecosyst. 17: 554–564.
Arey, L. 1932a. A microscopical study of glochidial immunity. - Journal of Morphology 53:
367–379.
Arey, L. 1932b. The Formation and Structure of the Glochidial Cyst. - Biol Bull. 62: 212–221.
Arvidsson, B. L. et al. 2012. Recruitment of the threatened mussel Margaritifera
margaritifera in relation to mussel population size, mussel density and host density. Aquatic Conserv: Mar. Freshw. Ecosyst. 22: 526–532.
Barnhart, M. C. 2003. Marking Mussels. - Missoui Conservationist.
Barnhart, M. C. 2005. Buckets of muckets: A compact system for rearing juvenile freshwater
mussels. - Aquaculture 254: 227–233.
Barnhart, M. C. et al. 2008. Adaptations to host infection and larval parasitism in Unionoida.
- Journal of the North American Benthological Society 27: 370–394.
Bauer, G. 1987. Reproductive Strategy of the Freshwater Pearl Mussel Margaritifera
margaritifera. - Journal of Animal Ecology 56: 691–704.
Bauer, G. 1994. The Adaptive Value of Offspring Size among Freshwater Mussels (Bivalvia;
Unionoidea). - Journal of Animal Ecology 63: 933–944.
Bauer, G. 1998. Allocation policy of female freshwater pearl mussels. - Oecologia 117: 90–94.
Bauer, G. 2001a. Characterization of Unionoida (= Naiads) - In: Bauer, G. and Wächtler K.
(eds.), Ecology and Evolution of the Freshwater Mussels Unionoida. Springer-Verlag,
Berlin.
Bauer, G. 2001b. Factors Affecting Naiad Occurence and Abundance - In: Bauer, G. and
Wächtler K. (eds.), Ecology and Evolution of the Freshwater Mussels Unionoida. SpringerVerlag, Berlin.
Bauer, G. 2001c. Framework and Driving Forces for the Evolution of Naiad Life Histories - In:
Bauer, G. and Wächtler K. (eds.), Ecology and Evolution of the Freshwater Mussels
Unionoida. Springer-Verlag, Berlin.
Bauer, G. 2001d. Life-History Variation on Different Taxonomic Levels of Najads - In: Bauer,
G. and Wächtler K. (eds.), Ecology and Evolution of the Freshwater Mussels Unionoida.
Springer-Verlag, Berlin.
Bauer, G. and Wächtler, K. 2001. Environmental Relationships of Naiads: Threats, Impact on
the Ecosystem, Indicator Function - In: Bauer, G. and Wächtler K. (eds.), Ecology and
Evolution of the Freshwater Mussels Unionoida. Springer-Verlag, Berlin.
Baumgärtner, D. and Heitz, S. 1995. Großmuscheln. Lebensweise, Gefährdung und Schutz. Landesamt für Umweltschutz.
Beckmann, K.-H. 2007. Die Spritztätigkeit der Gemeinen Flussmuschel Unio crassus
PHILIPSSON, 1788 - Ein Beitrag zur Fortpflanzungsbiologie. - Club Conchylia
Informationen 38: 2–4.
20
Bednarczuk, J. 1986. Untersuchungen zu Wirtsfischspektrum und Entwicklung der
Bachmuschel Unio crassus. Dissertation, Tierärtzliche Hochschule Hanover.
Berec, L. et al. 2006. Multiple Allee effects and population management. - Trends in Ecology
& Evolution 22: 185–191.
Bieler, R. et al. 2010. Classification of bivalve families - In: Bouchet, P. et al. (eds.),
Nomenclator of Bivalve Families with a Classification of Bivalve Families. Malacologia 52,
pp. 151–338.
Bjelke, U. et al. 2010. Blötdjur - Molluscs. Mollusca - In: Gärdenfors, U. (ed.), Rödlistade arter
i Sverige 2010. ArtDatabanken SLU.
Björk, S. 1962. Investigations on Margaritifera margaritifera and Unio crassus. Limnologic
Studies in Rivers in South Sweden.
Blažek, R. and Gelnar M. 2006. Temporal and spatial distribution of glochidial larval stages of
European unionid mussels (Mollusca: Unionidae) on host fishes. - Folia Parasitologica 53:
98–106.
Boettger, C. R. 1926. Untersuchungen über die Entstehung eines Faunenbildes. Zur
Zoogeographie der Weichtiere Schlesiens. - Z. f. Morphol. u. Ökol. d. Tiere 6.
Bogan, A. E. 2008. Global diversity of freshwater mussels (Mollusca, Bivalvia) in freshwater. Hydrobiologia 595: 139–147.
Buddensiek, V. et al. 1993. Studies on the chemistry of interstitial water taken from defined
horizons in the fine sediments of bivalve habitats in several norther German lowland
waters. II: Microhabitats of Margaritifera margaritifera L., Unio crassus (PHILIPSSPON)
and Unio tumidus PHILIPSSPON. - Arch. Hydrobiol. 127: 151–166.
Buddensiek, V. 1995. The culture of juvenile freshwater pearl mussels Margaritifera
margaritifera L. in cages: A contribution to conservation programmes and the knowledge
of habitat requirements. - Biological Conservation 74: 33–40.
Calles, E. O. and Greenberg L. A. 2005. Evaluation of nature-like fishways for re-establishing
connectivity in fragmented salmonid populations in the River Emån. - River Res. Applic.
21: 951–960.
Coker, R. E. et al. 1921. Natural history and propagation of fresh-water mussels. - Bulletin of
the bureau of fisheries XXXVII: 69–187.
Cuttelod, A. et al. 2011. European Red List of Non-marine Molluscs. - Publications Office of
the European Union.
Denic, M. et al. 2013. Physicochemical assessment of Unio crassus habitat quality in a small
upland stream and implications for conservation. - Hydrobiologia.
Dodd, B. J. et al. 2005. Cross-resistance of largemouth bass to glochidia of unionid mussels. Journal of Parasitology 91: 1064–1072.
Douda, K. et al. 2012. Host limitation of the thick-shelled river mussel: identifying the threats
to declining affiliate species. - Anim Conserv 15: 536–544.
Dudgeon, D. et al. 2006. Freshwater biodiversity: importance, threats, status and
conservation challenges. - Biol. Rev. 81: 163.
Editors of the American Heritage® Dictionaries. 2014. The American Heritage® Science
Dictionary. - 2014 Houghton Mifflin Company
21
Engel, H. 1990. Untersuchungen zur Autökologie von Unio crassus (PHILIPSSON) in
Norddeutschland. Dissertation, Universität Hanhover.
Eybe, T. and Thielen, F. 2010. Restauration des populations de moules perlières en
Ardennes. Technical Report: Action A1 /D1 /F3 Mussel Rearing Station.
Fisher, G. and Dimock, R. V. 2002. Ultrastructure of the mushroom body: digestion during
metamorphosis of Utterbackia imbecillis (Bivalvia: Unionidae). - Invertebrate Biology 121:
126–135.
Freyhof, J. and Brooks, E. 2011. European Red List of Freshwater Fishes. - European Union.
Frost, W. 1943. The Natural History of the Minnow, Phoxinus phoxinus. - Journal of Animal
Ecology 12: 139–162.
Geist, J. 2010. Strategies for the conservation of endangered freshwater pearl mussels
(Margaritifera margaritifera L.): a synthesis of Conservation Genetics and Ecology. Hydrobiologia 644: 69–88.
Geist, J. 2011. Integrative freshwater ecology and biodiversity conservation. - Ecological
Indicators 11: 1507–1516.
Glöer, P. and Zettler, M. 2005. Kommentierte Artenliste der Süßwassermollusken
Deutschlands. - Malakologische Abhandlungen 23: 3–26.
Graf, D. L. 2013. Patterns of Freshwater Bivalve Global Diversity and the State of
Phylogenetic Studies on the Unionoida, Sphaeriidae, and Cyrenidae. – American
Malacological Bulletin. 31: 135-153.
Gutiérrez, J. et al. 2003. Mollusks as ecosystem engineers: the role of shell production in
aquatic habitats. - Oikos 101: 79–90.
Haag, W. and Warren, M. 1998. Role of ecological factors and reproductive strategies in
structuring freshwater mussel communities. - Can. J. Fish. Aquat. Sci. 55: 297–306.
Haas, F. 1911. Die geologische Bedeutung der rezenten Najaden. - Geologische Rundschau 2:
87–90.
Harms, W. 1907a. Über die postembryonale Entwicklung von Anodonta piscinalis. Zoologischer Anzeiger XXXI: 801–814.
Harms, W. 1907b. Zur Biologie und Entwicklungsgeschichte der Flussperlmuschel
(Margaritifera margaritifera Dupuy). - Zoologischer Anzeiger XXXI: 814–824.
Harms, W. 1909. Postembryonale Entwicklungsgeschichte der Unioniden. - Zool. Jhrb., Abt.
Anat. und Ont. 28: 325–386.
Hastie, L. C. and Young, M. R. 2003. Timing of spawning and glochidia release in Scottish
freshwater pearl mussel (Margaritifera margaritifera) populations. - Freshwater Biology
48: 2107–2117.
Hazay, J. 1881. Die Mollusken-Fauna von Budapest. Mit besonderer Rücksichtnahme auf die
embryonalen und biologischen Verhältnisse ihrer Vorkommnisse. - Theodor Fischer.
Heard, W. 1975. Sexuality and other aspects of reproduction in Anodonta (Pelecypoda:
Unionidae). - Malacologia 10: 333–353.
Hochwald, S. and Bauer G. 1990. Untersuchungen zur Populationsökologie und
Fortpflanzungsbiologie der Bachmuschel Unio crassus (PHIL.) 1788. - Schriftenreihe
Bayer. Landesamt für Umweltschutz 97.
22
Hochwald, S. 1997. Das Beziehungsgefüge innerhalb der Größenwachstums- und
Fortpflanzungsparameter bayrischer Bachmuschelpopulationen (Unio crassus Phil. 1788)
und dessen Abhängigkeit von Umweltparametern. Dissertation, Universität Bayreuth,
Bayreuth.
Hochwald, S. 2001. Plasticity of Life-History Traits in Unio crassus - In: Bauer, G. and
Wächtler K. (eds.), Ecology and Evolution of the Freshwater Mussels Unionoida. SpringerVerlag, Berlin.
Hua, D. et al. 2012. Monitoring survival and growth of laboratory-cultured endangered
mussels, Epioblasma capsaeformis and E. brevidens, released into the Powell River,
Tennessee, USA - In: Teixeira, A. et al. (eds.), Book of Abstracts. International Meeting on
Biology and Conservation of Freshwater Bivalves. Instituto Politécnico de Bragança, p. 56.
Israel, W. 1913. Biologie der europäischen Süβwassermuscheln. - K.G. Lutz Verlag Stuttgart.
Jansen, W. et al. 2001. Glochidial Mortality in Freshwater Mussels - In: Bauer, G. and
Wächtler K. (eds.), Ecology and Evolution of the Freshwater Mussels Unionoida. SpringerVerlag, Berlin.
Jokela, J. and Palokangas, P. 1993. Reproductive tactics in Anodonta clams: parental host
recognition. - Animal Behaviour 46: 618–620.
Jungbluth, J. 1993. Beiträge zur Najadenfauna in Mitteleuropa. - Arch. Moll. 122: 155–170.
Kat, P. 1983. Conchiolin layers among the Unionidae and Margaritiferidae (Bivalvia):
microstructural characteristics and taxonomic implications. - Malacologia 24: 298–311.
Källersjo, M. et al. 2005. Evaluation of ITS rDNA as a complement to mitochondrial gene
sequences for phylogenetic studies in freshwater mussels: an example using Unionidae
from north-western Europe. - Zool Scripta 34: 415–424.
Knaepkens, G. et al. 2004. Assessment of residency and movement of the endangered
bullhead (Cottus gobio) in two Flemish rivers. Short communication. - Ecology of
Freshwater Fish 13: 317–322.
Korniushin, A. V. and Glaubrecht, M. 2003. Novel reproductive modes in freshwater clams:
brooding and larval morphology in Southeast Asian taxa of Corbicula (Mollusca, Bivalvia,
Corbiculidae). - Acta Zoologica (Stockholm) 84: 291–315.
Körner, H. (ed.) 1998-2001. Mitteilungen des Badischen Landesvereins für Naturkunde und
Naturschutz e.V.
Lang, K. 1998. Die Bachmuschel Unio crassus (PHILIPSSON, 1788) im Niederbach:
Bestandssituation, Fortpflanzungsbiologie und Wanderverhalten. Dissertation,
Fachbereich Zoologie, Freiburg.
Lavictoire, L. 2012. Using a fluorescence marking technique to improve monitoring of the
critically endangered freshwater pearl mussel Margaritifera margaritifera. Final Report.
Lefevre, G. and Curtis W. C. 1910. Reproduction and parasitism in the Unionidæ. - Journal of
Experimental Zoölogy 9: 79–115.
Lefevre, G. and Curtis, W. 1912. Studies on the reproduction and artificial propagation of
fresh-water mussels. - Bull Bur Fish 30: 1–190.
23
Levine, T. D. et al. 2012. Physiological and ecological hosts of Popenaias popeii (Bivalvia:
Unionidae): laboratory studies identify more hosts than field studies. - Freshwater
Biology 57: 1854–1864.
Limm, M. P. and Power M. E. 2011. Effect of the western pearlshell mussel Margaritifera
falcata on Pacific lamprey Lampetra tridentata and ecosystem processes. - Oikos 120:
1076–1082.
Lozoya, A. V. de and Araujo, R. 2011. How the Naiad was Drawn: A Pre-Linnean Iconography
of Freshwater Mussels. - Malacologia 53: 381–402.
Lundberg, S. et al. 2007. Åtgärdsprogram för bevarande av tjockskalig målarmussla (Unio
crassus). Rapport 5658. - Naturvårdsverket.
Lundberg, S. and Bergengren J. 2008. Miljöövervakningsstrategi för stormusslor. Utveckling
av nationell miljöövervakning för sötvattenslevande stormusslor. - Naturhistoriska
riksmuseets småskriftserie. Stockholm. ISSN: 0585-3249
Lydeard, C. et al. 2004. The Global Decline of Nonmarine Mollusks. - BioScience 54: 321.
Maaß, S. 1987. Untersuchungen zur Fortpflanzungsbiologie einheimischer
Süßwassermuscheln der Gattung Unio. Dissertation, Tierärztliche Hochschule Hannover.
McIvor, A. and Aldridge D. The cultivation of the freshwater pearl mussel, Margaritifera
margaritifera.
Mills, C. and Mann, R. 1983. The bullhead Cottus gobio, a versatile and successful fish. In:
Fifty-first annual report for the year ended 31st March 1983, Ambleside, UK. - Freshwater
Biological Association: 76–88.
Mueller, M. et al. 2011. The effects of weirs on structural stream habitat and biological
communities. - Journal of Applied Ecology 48: 1450–1461.
Nagel, K.- O. and Badino G. 2001. Population Genetics and Systematics of European
Unionoidea - In: Bauer, G. and Wächtler K. (eds.), Ecology and Evolution of the
Freshwater Mussels Unionoida. Springer-Verlag, Berlin.
O'Connell, M. and Neves R. J. 1999. Evidence of Immunological Responses by a Host Fish
(Ambloplites rupestris) and Two Non-Host Fishes (Cyprinus carpio and Carassius auratus)
to Glochidia of a Freshwater Mussel (Villosa iris). - Journal of Freshwater Ecology 14: 71–
78.
Owen, C. T. et al. 2011. Muskrat predation on a diverse unionid mussel community: impacts
of prey species composition, size and shape. - Freshwater Biology 56: 554–564.
Österling, M. E. et al. 2008. Relationship of biotic and abiotic factors to recruitment patterns
in Margaritifera margaritifera. - Biological Conservation 141: 1365–1370.
Österling, M. E. et al. 2010. Habitat degradation and the decline of the threatened mussel
Margaritifera margaritifera: influence of turbidity and sedimentation on the mussel and
its host. - Journal of Applied Ecology 47: 759–768.
Österling, E. M. et al. 2014. Parasitic freshwater pearl mussel larvae (Margaritifera
margaritifera L.) reduce the drift-feeding rate of juvenile brown trout (Salmo trutta L.). Environ Biol Fish 97: 543–549.
24
Österling, M. E. and Högberg, J.- O. 2014. The impact of land use on the mussel Margaritifera
margaritifera and its host fish Salmo trutta. - Hydrobiologia 735: 213–220.
Parodiz, J. and Bonetto, A. 1963. Taxonomy and zoogeographic relationships of the South
American najades (Pelecypoda: Unionacea and Mutelacea). - Malacologia 1: 179–214.
Patzner, R. and Mueller, D. 2001. Effects of Eutrophication on Unionids - In: Bauer, G. and
Wächtler K. (eds.), Ecology and Evolution of the Freshwater Mussels Unionoida. SpringerVerlag, Berlin.
Prié, V. and Puillandre, N. 2013. Molecular phylogeny, taxonomy, and distribution of French
Unio species (Bivalvia, Unionidae). - Hydrobiologia. DOI 10.1007/s10750-013-1571-0
Pusch, M. et al. 2001. Filtration and Respiration Rates of Two Unionid Species and Their
Impact on the Water Quality of a Lowland River - In: Bauer, G. and Wächtler K. (eds.),
Ecology and Evolution of the Freshwater Mussels Unionoida. Springer-Verlag, Berlin.
Ricciardi, A. et al. 1998. Impeding extinctions of North American freshwater mussles
(Unionoida) following the zebra mussel (Dreissena polymorpha) invasion. - Journal of
Animal Ecology 67: 613–619.
Rogers, S. et al. 2001. Life history and population biology of the endangered tan riffleshell
(Epioblasma florentina walkeri) (Bivalvia: Unionidae). - Journal of the North American
Benthological Society 20: 582–594.
Roni, P. and Beechie, T. eds. 2012. Stream and Watershed Restoration: A Guide to Restoring
Riverine Processes and Habitats. Wiley-Blackwell. ISBN: 978-1-4051-9956-8.
Scharsack, G. 1994. Licht- und elektronenmikroskopische Untersuchungen an Larvalstadien
einheimischer Unionacea. Dissertation, Universität Hannover.
Sell, J. et al. 2013. Identification and Characterization of the First Microsatellite Loci for the
Thick-Shelled River Mussel Unio crassus (Bivalvia: Unionidae). - J. Exp. Zool.: 1–4.
Strayer, D. L. et al. 1994. Distribution, abundance, and roles of freshwater clams (Bivalvia,
Unionidae) in the freshwater tidal Hudson River. - Freshwater Biol 31: 239–248.
Strayer, D. L. et al. 2004. Changing Perspectives on Pearly Mussels, North America's Most
Imperiled Animals. - BioScience 54: 429–439.
Strayer, D. L. 2008. Freshwater Mussel Ecology. A Multifactor Approach to Distribution and
Abundance. - University California Press.
Strayer, D. L. 2014. Understanding how nutrient cycles and freshwater mussels (Unionoida)
affect one another. - Hydrobiologia 735: 277–292.
Strayer, D. L. and Malcom, H. 2012. Causes of recruitment failure in freshwater mussel
populations in southeastern New York. - Ecological Applications 22: 1780–1790.
Taeubert, J.- E. et al. 2012a. Host-specificity of the endangered thick-shelled river mussel
(Unio crassus, Philipsson 1788) and implications for conservation. - Aquatic Conserv: Mar.
Freshw. Ecosyst. 22: 36–46.
Taeubert, J.- E. et al. 2012b. The relationship between endangered thick-shelled river mussel
(Unio crassus) and its host fishes. - Biological Conservation 155: 94–103.
25
Taeubert, J.- E. et al. 2013a. Variable development and excystment of freshwater pearl
mussel (Margaritifera margaritifera L.) at constant temperature. - Limnologica 43: 319–
322.
Taeubert, J.- E. et al. 2013b. Effects of water temperature on the larval parasitic stage of the
thick-shelled river mussel (Unio crassus). - Aquatic Conserv: Mar. Freshw. Ecosyst. DOI:
10.1002/aqc.2385.
Taeubert, J.- E. et al. 2013c. Towards standardization of studies into host relationships of
freshwater mussels. - Biological Conservation 159: 550-551.
Thielen, F. (ed.) 2011. Rearing of unionoid mussels with special emphasis on the Freshwater
Pearl Mussel Margaritifera margaritifera. Travaux scientifiques du Musée national
d'histoire naturelle Luxembourg ISSN: 1682-5519.
Thomas, G. R. et al. 2013. Does the parasitic freshwater pearl mussel M. margaritifera harm
its host? - Hydrobiologia DOI 10.1007/s10750-013-1515-8.
Trudorancea, C. and Gruia, L. 1968. Observations on the Unio crassus Philipsson population
from the Nera river. - Trav. Mus. Hist. nat. Grigore Antipa 8: 381–394.
Vaughn, C. C. 2010. Biodiversity Losses and Ecosystem Function in Freshwaters: Emerging
Conclusions and Research Directions. - BioScience 60: 25–35.
Vaughn, C. C. 2012. Life history traits and abundance can predict local colonization and
extinction rates of freshwater mussels. - Freshwater Biology 57: 982–992.
Vaughn, C. and Hakenkamp, C. 2001. The functional role of burrowing bivalves in freshwater
ecosystems. - Freshwater Biology 46: 1431–1446.
Vaughn, C. and Taylor, C. 2000. Macroecology of a hostparasite relationship. - Ecography 23:
11–20.
Wengström, N. 2009. Samspelet mellan fiskar och stormusslor. Vilka värdfiskar utnyttjas av
den tjockskaliga målarmusslan Unio crassus? Examensarbete för naturvetenskaplig
magisterexamen i Biologi, Zoologiska institutionen, Göteborgs Universitet.
Vicentini, H. 2005. Unusual spurting behaviour of the freshwater mussel Unio crassus. Journal of Molluscan Studies 71: 409–410.
Wächter, K. et al. 2001. Larval Types and Early Postlarval Biology in Naiads (Unionoida) - In:
Bauer, G. and Wächtler K. (eds.), Ecology and Evolution of the Freshwater Mussels
Unionoida. Springer-Verlag, Berlin.
Wächter, K. 2001. Larval Types and Early Postlarval Biology in Naiads (Unionoida) - In: Bauer,
G. and Wächtler K. (eds.), Ecology and Evolution of the Freshwater Mussels Unionoida.
Springer-Verlag, Berlin.
Walker, K. et al. 2001. Freshwater Mussels (Hyriidae) of Australasia - In: Bauer, G. and
Wächtler K. (eds.), Ecology and Evolution of the Freshwater Mussels Unionoida. SpringerVerlag, Berlin, pp. 5–31.
Ward, J. 1989. The Four-Dimensional Nature of Lotic Ecosystems. - Journal of the North
American Benthological Society 8: 2–8.
26
Watters, G. 2001. The Evolution of the Unionacea in North America, and Its Implications for
the Worldwide Fauna - In: Bauer, G. and Wächtler K. (eds.), Ecology and Evolution of the
Freshwater Mussels Unionoida. Springer-Verlag, Berlin, pp. 281–307.
Yeager, M. M. et al. 1999. Competitive interactions between early life stages of Villosa iris
(Bivalvia: Unionidae) and adult Asian clams (Corbicula fluminea). - Proceedings of the
First Freshwater Mollusk Conservation Societey Symposium: 253–259.
Zahner-Meike, E. and Hanson J. M. 2001. Effect of Muskrat Predation on Naiads - In: Bauer,
G. and Wächtler K. (eds.), Ecology and Evolution of the Freshwater Mussels Unionoida.
Springer-Verlag, Berlin.
Zale, A. and Neves R. J. 1982. Fish hosts of four species of lampsiline mussels (Mollusca:
Unionidae) in Big Moccasin Creek, Virginia. - Canadian Journal of Zoology 60: 2535–2542.
Zettler, M. 2000. Weitere Bemerkungen zur Morphologie von Unio crassus PHILIPSSON 1788
aus dem nordeuropäischen Verbreitungsgebiet (Bivalivia: Unionidae). - Malakologische
Abhandlungen 20: 73–78.
Zettler, M. L. and Jueg U. 2007. The situation of the freshwater mussel Unio crassus
(Philipsson, 1788) in north-east Germany and its monitoring in terms of the EC Habitats
Directive. - Mollusca 25: 165–174.
Zieritz, A. et al. 2012. Identifying freshwater mussels (Unionoida) and parasitic glochidia
larvae from host fish gills: a molecular key to the North and Central European species. Ecology and Evolution 2: 740–750.
Zimmerman, L. and Neves R. J. 2002. Effects of temperature on duration of viability for
glochidia of freshwater mussels (Bivalvia: Unionidae). - American Malacological Bulletin
17: 31–35.
27
Introductory papers in Biology, Karlstad University:
1. Olsson, I.C. 2005. Migration av öring (Salmo trutta L.)
2. Calles, O. 2005. Fiskars migration och reproduktion i reglerade vatten –
restaureringsåtgärder och dess effekter
3. Österling, M. 2005. Begränsande faktorer för utbredning och överlevnad av
flodpärlmusslan (Margaritifera margaritifera L.)
4. Olsson, M. 2007. Infrastukturens effekter och betydelse av faunapassager
5. Gustafsson, P. 2007. Kantzonsvegetations inverkan på öring (Salmo trutta L.) i
rinnande vatten
6. Cassing, G. 2009. Löträd, landskap och viltbete – en introduktion till studier av
lövträdrekrytering och viltbete i olika rumsliga skalor
7. Enefalk, Å. 2012. Brown trout responses to woody debris in boreal streams
8. Watz, J. 2012. The foraging behaviour of steam salmonids during winter: The effects
of temperature, light intensity, and surface ice
9. Nyqvist, D. 2013. Atlantic salmon kelts – repeat spawning and downstream migration
10. Lans, L. 2013. Beteende och metabolism: Hur ämnesomsättning och beteende
påverkar viljan att migrera hos Atlantlax (Salmo salar) och öring (Salmo trutta)
11. Schneider, L. D. 2014. Ecology of the threatened thick-shelled river mussel Unio
crassus (Philipsson 1788) with focus on mussel-host interactions
28