Biological Journal of the Linnean Society, 2015, 115, 826–841. With 4 figures.
Once a land of big wild rivers: specialism is
context-dependent for riparian snails (Pulmonata:
Valloniidae) in central Europe
CRISTIAN R. ALTABA1,2*
1
Human Evolution and Cognition Group (EVOCOG), Universitat de les Illes Balears, 07122, Palma,
Balearic Islands, Spain
2
Laboratori de Natura, Museu de Ci
encies Naturals de Barcelona, Passeig Picasso s/n, 08003,
Barcelona, Catalonia, Spain
Received 3 December 2014; revised 17 February 2015; accepted for publication 18 February 2015
Specialist species may be perceived as such because of their narrow ecological requirements, but this may be
context-dependent. The genus Vallonia (Gastropoda Pulmonata: Valloniidae) includes widespread generalist
species and also two specialists endemic to Central Europe: Vallonia suevica, restricted to warm, wet meadows
and riverbanks subject to seasonal flooding; and Vallonia declivis, living only in wet to humid meadows,
riverbanks, and reedbeds. Both have experienced dramatic declines; as is the case with many land snails, their
global conservation status has been underestimated: these species are Critically Endangered. Other congenerics
are probably dispersed by birds. In contrast, the distributions of these meadow specialists appear to be the
outcome of their strictly riparian habitat coupled with dispersal by fish. Thus, they have tracked drainage
changes through the Pleistocene from their origin in the floodplain uplands of the Danube biodiversity hotspot in
the Pliocene. Natural dispersal mechanisms have been disrupted, and riparian and river ecosystems have been
destroyed throughout Europe. This has led big-river specialist molluscs and their associated fishes to the brink of
extinction. The notion of specialism thus depends on the ecological context; it is useful to stress their noninvasive character, current restriction to scarce habitats, and evolution under quite different conditions. © 2015
The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 115, 826–841.
ADDITIONAL KEYWORDS: biogeography – conservation – dispersal – endemism – evolution –
ichthyochory – Mollusca – riparian habitat – rivers – Vallonia.
INTRODUCTION
Unusual species often prove to be unusually enlightening – those most divergent from the norm within a
taxon are useful for understanding adaptation and
diversification. Indeed, specialization is favourable in
a given ecological setting but represents an increased
risk of extinction under environmental change (Futuyma & Moreno, 1988). Although generalist species
may be so considered because of incomplete knowledge of their requirements (Loxdale, Lushai &
Harvey, 2011), they often have comparatively large
distributions and thrive in various habitats. Thus,
*E-mail: [email protected]
826
divergence between specialists and generalists promotes a variety of resource consumption and life-history strategies. Most importantly, these strategies
form a continuum from generalism to specialism,
across which species may evolve in either direction
(Dennis et al., 2011). At one extreme, generalists may
readily become invasive, whilst, at the other, specialists are characteristic of isolated ecosystems (Altaba,
2014). The challenge is to determine what sets specialists apart from closely related generalists and what
ecological consequences derive from such differences.
Several generalist species are well known among
the minute land snails of the genus Vallonia Risso,
1826 (Pulmonata: Valloniidae). These species are
often abundant, have very large ranges, and have
© 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 115, 826–841
SPECIALISM OF EUROPEAN RIPARIAN SNAILS
become invasive in many regions (Sterki, 1893;
Gerber, 1996; Barker, 1999). However, the genus
also includes species that are ecologically restricted
and thus have experienced enormous range shifts
in the Quaternary (Meng, 2009a; Hors
ak et al.,
2010). Outside either type, two exceedingly rare
species are known from just a few valleys in Central Europe: Vallonia suevica Geyer, 1908 and
Vallonia declivis Sterki, 1893. These live only in
seriously threatened habitats found exclusively on
the banks of seasonally flooding rivers (Kerney,
Cameron & Jungbluth, 1983; Cuttelod, Seddon &
Neubert, 2011; R€
ahle, 2011). Herein, I address
what makes them specialists – their current and
historical distribution and habitat – with the aim
of assessing how they differ from generalist congenerics. In search of a mechanistic explanation for
their unusual biogeographical patterns, I then
develop an evidence-based hypothesis about their
origin and dispersal means. The conclusions apply
to a wide range of spatial scales and allow a reformulation of the generalist/specialist dichotomy.
This has profound consequences for biodiversity
conservation in riparian habitats and river ecosystems at the landscape level.
DISTRIBUTION OF SPECIALISTS
A DANUBIAN ENCLAVE
The Danube is the second largest of European rivers
(surpassed only by the Volga in Russia), running
along 2921 km from the Alps through the Hungarian
Plain and the southern Carpathians into the Black
Sea. Its freshwater fauna is exceptionally rich and
distinctive (Abell et al., 2008). Indeed, its main channel served as a refuge for freshwater and terrestrial
species during Pleistocene glaciations (Sommerwerk
et al., 2009). Its role in the recolonization by fishes of
rivers between the Atlantic and the Caspian Sea
allows discriminating a vast, comparatively uniform
‘Danubian Europe’ from the finely differentiated
Mediterranean drainages (Reyjol et al., 2007; Tedesco et al., 2012). A comparable pattern is found in
North America (Bernatchez & Wilson, 1998), where
glaciated areas have been recolonized mostly by generalists adapted to large rivers (Griffiths, 2010). In
contrast, terrestrial species dispersed northwards
from southern refugia (Taberlet et al., 1998; Hewitt,
1999; Schmitt, 2007), with differences in dispersal
ability and timing causing partially incongruent
recolonization patterns (Fattorini & Ulrich, 2012;
O’Meara et al., 2012; Yannic et al., 2012). In unglaciated areas, species-specific differences among fish
and amphibian species, and a long history, account
for phylogeographical patterns that are even more
827
divergent (Canestrelli, Sacco & Nascetti, 2012; Husemann et al., 2012; Lopes-Cunha et al., 2012).
The best-preserved stretch of the Danube is at
Devın Gate at the border of Slovakia and Austria
(Fig. 1). Here, the Morava (March) river inflows from
the north, passing by the southernmost tip of the
Western Carpathians range, at 158 m above sea
level. The area just north of Devın Castle is unique
in Slovakia for its xerophilous sub-Mediterranean
vegetation, with many rare or endangered species
found only there (Fer
akov
a, 1997). Below these hillside and cliff habitats, the Morava is surrounded by
one of the best-preserved floodplains in Europe, still
hosting small tracts of seasonally flooded forests and
meadows (Seffer
& Stanov
a, 1999; Oszl
any, 2001;
Ruzickov
a, Ban
asov
a & Kalivoda, 2004; Hager et al.,
2007), and now protected jointly by three countries
(Kadlecık & Janak, 2004). The extant land snail
assemblages of this floodplain are similar to those of
the Danube riverbanks, although the latter harbour
larger populations owing to shorter periods of flood
ing (Cejka,
2005). This is because of large-scale
works aimed at controlling the once-devastating
Danube floods (Rohr, 2005). Upstream of Devın, the
Danube is flanked by riparian forests, but those riverbanks were severely disturbed by the ‘Great Danube Draining and Flood Protection Program’ at the
beginning of the 20th century. They no longer harbour the once extensive wet meadows, although the
area has recently been protected in Austria as the
Danube-Auen National Park. A delicate equilibrium
is sought therein between intensive recreational use
and habitat management (Hager & Schume, 2001;
Hager et al., 2007; Sterl, Brandenburg & Arnberger,
2008), including renaturalization of riverbanks (Keckeis, 2014). However, such restoration may not be
ecologically sufficient (Bernhardt & Palmer, 2011),
especially for low-dispersing organisms, such as molluscs (Kappes & Haase, 2011). Past Devın, the Danube crosses the city of Bratislava and flows into a
subsiding basin where it forms an extensive inland
delta. This has been deeply transformed by agriculture, industry, and diversion through the last eight
t et al., 2004). Moreover, the large
centuries (Pisu
Gabcıkovo-Nagymaros hydroelectric complex, completed in 1996, has triggered enormous environmental impacts on the Slovak–Hungarian border
(Jansky, Murakami & Pachova, 2004), including the
total demise of seasonally flooded wetlands. The
stretch between Vienna (Wien) and Bratislava is the
only place where the Danube has a good ecological
and chemical status (ICPDR, 2009); natural habitats
exist only at the Morava confluence.
Among land snails collected at Devın Gate
(Supporting Information, Appendix S1), all seven
European Vallonia were found (Fig. 2, Table 1): the
© 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 115, 826–841
828
C. R. ALTABA
V. suevica; and the subfossil Vallonia tenuilabris
(Braun, 1843). This unusually rich assemblage is a
consequence of the unique, relict character of both
Devın Hill and the Danube–Morava confluence. It is
remarkable that Devın has been guarded by a fortress since prehistory. Old castle hills often host
many rare and endangered land snails in Central
Europe (Gaschott, 1922; Alexandrowicz, 1995;
Jurickov
a, 2005; Jurickov
a & Kucera, 2005a, b; Kobialka & Kappes, 2010; R€
uetschi et al., 2012).
Throughout the 20th century, the Slovak side of the
Danube at Devın was spared from massive channelization works undertaken just upstream in Austria
and just downstream throughout the inner Danube
delta in Slovakia. In addition, this site was forbidden, and thus wild, during the four decades of the
Cold War. The cliff foot at Devın has deep soil and a
humid, relatively warm, microclimate, experiences
seasonal flooding, and remained undisturbed, thus
providing an adequate refuge for thermophile wetmeadow species. This allowed the continued existence of a small stretch of pristine wet riverbank
where both V. suevica and V. declivis could survive.
Unfortunately, the narrow strip between the rocky
cliff and the river now receives a growing number of
visitors who walk through a paved path leading to
restaurants, a hotel, a memorial monument, and a
small harbour. Moreover, forecasts of climate change
in lowland Slovakia include an increase of extreme
events, including heat spells and floods (Stankoviansky et al., 2012). This refuge for rare species is a serendipitous, but fragile, combination of geography
and human history.
H ISTORICAL
Figure 1. Riparian habitats along the confluence of the
Danube and the Morava at Devı́n Gate (Slovakia):
upstream from the summit of Devın Hill (top), from the
main river (middle), and along the mouth of the Morava
(bottom). This is the only site along the whole Danube’s
main channel with good ecological status, clean water,
and natural riversides with seasonally flooded meadows.
widespread Vallonia costata (M€
uller, 1774), Vallonia pulchella (M€
uller, 1774), and Vallonia excentrica
Sterki, 1892; the rare Vallonia enniensis Gredler,
1856; the critically endangered V. declivis and
RANGES
Vallonia suevica and V. declivis appear to be highly
specialized, being among the most rare land snails in
Europe (Fig. 3, Appendix S2). Vallonia suevica
inhabits only wet meadows and riverbanks subject to
seasonal flooding in relatively warm sites in Central
Europe (Geyer, 1908; Fechter, 1989; Gerber, 1996).
It survives in, at most, a dozen sites with relatively
dry (when not flooded) meadows, mowed at most
twice a year, and spared from expanding intensive
agriculture. Vallonia declivis lives only in wet to
humid (but not permanently waterlogged) meadows,
riverbanks, and reedbeds. It may survive in just six
sites, all in Germany (Geyer, 1908; Gerber, 1996;
R€
uetschi et al., 2012).
The extent and habitat quality of north German
lowland floodplain grasslands has decreased dramatically since the 1950s (Krause et al., 2011), and the
loss of these endangered grassland habitats is ongoing throughout Germany (Ammermann, 2008; Lind
et al., 2009) and Switzerland (R€
uetschi et al., 2012).
© 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 115, 826–841
SPECIALISM OF EUROPEAN RIPARIAN SNAILS
829
Figure 2. Non-invasive Vallonia species found at Devı́n Gate. From top to bottom: Vallonia declivis, Vallonia suevica,
Vallonia enniensis, and Vallonia tenuilabris (fossil). Scale bar = 1 mm.
Furthermore, restoration of such meadows is difficult, being hampered by fragmentation and reduced
seed dispersal (Bakker & Berendse, 1999; Soomers,
2012), as well as loss of vital disturbance of soil
structure by flooding (Burmeier, 2010). Along a tributary of the Morava in Bohemia, the land snail
assemblages in the floodplain are distinct from those
on adjacent forest slopes, and connectivity among
localities appears to play a minor role in determining
k & Hors
their composition (Mysa
ak, 2011), suggesting that land snail dispersal rates are indeed low
along riverbanks. Moreover, both size and age of
habitat patches have a strong effect on habitat specialist land snails (Hors
ak et al., 2012). Unaided
recolonization by specialist species of Vallonia also
seems difficult at present, so surviving populations
are effectively residual and thus vulnerable.
The lower Morava and large parts of the Danube
have been channelled, preventing flooding of most of
the original, extensive riverbanks. This is the main
factor affecting land snail assemblages along the Slovakian Danube, causing profound alteration of riparian communities and the demise of wet-softwood
forest specialist snails (Cejka,
Hors
ak & Nemethov
a,
2008). In addition, the Danube riverbanks in Slovakia are being colonized by adventive, often invasive,
plant species, carried along by the current and shipping activities (Jehlık, Dost
alek & Zaluberov
a, 2005).
The outcome is that virtually all wet meadows and
riparian forests that once covered the inland Danube
delta have been lost, with the fragmented remnants
of natural or seminatural vegetation affected by
draining, intensive agriculture, lack of flooding, lowered phreatic levels and spread of ruderal and inva t et al., 2004, 2010). In that
sive plant species (Pisu
area, most land snail species in floodplain forests
could be assigned to distinct groups along the moisture gradient, but only two strongly hygrophilous
species are present, and the ubiquitous V. pulchella
was the only species of its genus found (Cejka
&
Hamerlık, 2009). This species occurs in a wide variety of habitats (Gerber, 1996), although at a large
spatial scale it prefers dryer grasslands and even disturbed sites (Nekola, 2003). In wetlands, it may be
quite abundant in ungrazed wet meadows subject to
flooding (Cejka,
2005). At any rate, V. pulchella is an
adaptable, weedy species that apparently substitutes
its specialized congenerics in a general process of biodiversity loss and homogenization.
It is thus relevant to assess what the strongholds
for V. suevica and V. declivis have in common. In
spite of intense human occupation, river channelization, and land-use changes, including large industries
and, more recently, habitat restoration (Albrecht
et al., 2000; Hutter, 2007), the Neckar valley bottomlands have sustained V. suevica. A probable explanation is that this river experiences huge variations in
flow, effectively sustaining small patches of seasonally flooded meadows subject to relatively warm, dry
summers (the valley slopes host the northernmost
© 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 115, 826–841
Small
Medium
Large
V. enniensis
V. tenuilabris
Large
V. declivis
V. suevica
Size
Species
Short oval
Circular,
rounded
periphery
Ovoid,
periphery
slightly
angled on top
Nearly circular,
rather solid
Shape
Slow regular
growth;
broadly
conical; last
whorl barely
widened before
aperture; deep
suture
Whorls with
comparatively
little overlap;
last 1/4 whorl
expanded
trumpet-like,
smoothly
running into
mouth edge in
top view
Regular growth;
low conical,
inflated whorls
Regular growth
Spire
Shiny with
numerous
faint and fine
riblets (about
50 on last
whorl), smooth
periostracum
in between
Dull with
numerous
(50–80)
delicate, low,
often regularly
spaced riblets
with
calcareous
base
Weakly shiny
with very fine
streaks;
embryonic
shell often
with thin
spiral lines
Almost smooth
Surface
Table 1. Diagnostic traits of non-invasive European Vallonia species
Wide, slightly
elliptical,
eccentric
Relatively
narrow,
subcircular
Narrow,
eccentric
Very wide,
eccentric
Umbilicus
Elliptical,
slightly
wider than
tall,
well inclined,
preceded by a
downward
bend
Nearly round
aperture,
preceded by a
slightly
descending
slope
Large, preceded
by a gently
descending
last
1
/6 whorl
Nearly
circular. If
strongly built,
preceded by a
suddenly
descending
slope
Aperture
Short and
sharply bent
outwards,
insertions
often wide
apart
Insertions well
separate
No real lip, only
a diffuse
thickening
Lip abruptly
enlarged,
thick, whitish
translucent,
protruding a
bit beyond
mouth edge
Roundly
protruding
over mouth
edge, not
distinctly
visible from
above and not
expanded
near upper
peristome
insertion
Not protruding
beyond mouth
edge
Insertions
wide apart
Greatly
thickened
internally
Lip
Peristome
830
C. R. ALTABA
© 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 115, 826–841
SPECIALISM OF EUROPEAN RIPARIAN SNAILS
831
Figure 3. Recorded distribution of riparian specialist Vallonia along rivers in Central Europe: Vallonia declivis (horizontal hatching) and Vallonia suevica (vertical hatching). The Danube drainage (silver) includes the Pannonian basin
(dark grey); it lost part of its headwaters (white) to neighbouring drainages (light grey) throughout the Pleistocene.
Virtually all Holocene findings were made in the last 130 years, after Europe’s rivers had been thoroughly altered but
before widespread destruction of riparian habitats. Most belong to now-extinct populations. Up to the late Middle Ages,
both species surely were abundant along all rivers shown, except deep into the Pannonian basin and (for V. suevica) the
northern reaches on the Great European Plain.
vineyards). Such habitat traits are also present
locally at the riverbank in Devın Gate.
RANGE EXPANSION AND COLLAPSE
T HE DANUBE’S HERITAGE
The ranges of V. suevica and V. declivis (Fig. 3) are
difficult to interpret taking into account the present
geography. They are circumscribed to riverside habitats and have very limited dispersal ability. However,
current drainages in Central Europe underwent major
changes caused by the Pleistocene glaciations. Stream
captures may account for the occurrence of these species in mainland drainages flowing to different seas.
Much of the upper Rhine drainage, including the Neckar and part of the Aar (Aare), belonged to the Danube
system until the Early to Middle Pleistocene (Preusser, 2008; Baier, 2009; Uehlinger et al., 2009; Mikl
os
& Neppel, 2010; Yanites et al., 2013). These stream-
capture events account for other currently disjunct
ranges. Fish distributions were greatly modified in
glaciated areas (Griffiths, 2006); fishes with low dispersal ability are found in the headwaters of different
drainages around the Alps (Winkler et al., 2011;
Lerceteau-K€
ohler et al., 2013), and others spread during the Pleistocene from the Danube into the Rhine
(Englbrecht et al., 2000; Freyhof, Kottelat & Nolte,
2005). If Vallonia alamannica, restricted to the river
valleys flanking the dry Swabian Jura (Schw€
abische
Alb), turns out to be a valid taxon, its distribution
might also be explained by Quaternary stream captures. Further east, several land snail species of Carpathian origin dispersed, following the Oder towards
the Baltic (Boettger, 1926; Schlesch, 1946). Several of
the Danube’s headwaters in the Carpathians were
captured by the Vistula drainage (Kukulak, 2007),
also carrying fish species into this northern river system (Konopinski, Amirowicz & Kukuła, 2007). Likewise, stream captures in the Dolomites (Soldati, 2010)
© 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 115, 826–841
832
C. R. ALTABA
may account for the single record of V. suevica in
northern Italy, in the Sarca (Sarchbach), now a headwater of the Po drainage. Freshwater fishes also
appear to have been carried by stream capture from
the Danube drainage into the Po headwaters (Bianco,
1995). The Boreo–Alpine vertiginid snail, Vertigo genesii (Gredler, 1856), is found in the South Tirol (Alto
Adige) but nowhere else in Italy, being tightly linked
to cool and wet, often flooded, meadows (Alzona, 1971;
Limondin, 1992; Manganelli et al., 1995). The hypothesis of one-stance dispersal of V. suevica by birds over
the Alps (Falkner, von Proschwitz & R€
uetschi, 2011)
is ad hoc and unlikely.
During the last glacial low-stand, the Rhine, Elbe,
and Thames joined before reaching the Atlantic
along the present-day English Channel (Antoine
et al., 2003; Preusser, 2008). Much of the North Sea
was dry land: a low-lying landscape now known as
Doggerland (Gaffney, Fitch & Smith, 2009). The
occurrence of V. declivis in the middle Rhine and
Elbe drainages probably reflects dispersal along
riparian corridors. In this context, riparian and riverine habitats in southern and eastern England were
colonized by species incoming from the Rhine.
The Danube harbours an unusually rich aquatic
biodiversity and it played an active role in the development of today’s freshwater faunas of Central Europe through incorporation of Miocene Paratethyan
taxa and Plio-Pleistocene stream captures (Reyjol
et al., 2007; Tedesco et al., 2012). Adequate habitats
for either V. suevica or V. declivis do not exist along
the Danube, from Hungary to the Black Sea. The big
river’s entrance into the Pannonian forest steppes of
the Great Hungarian Plain marks the eastern limits
for such wet meadow specialists. However, vegetation types in the Danube area have experienced
drastic changes throughout the Neogene, largely
because of the uplift of surrounding mountain belts
(Jimenez-Moreno et al., 2007). During the Middle
Miocene optimum, the Paratethys basin (roughly the
present middle Danube basin) had a warm, subtropical climate supporting reedbeds along with riparian,
swamp, and mixed-mesophytic forests (Kovar-Eder,
1987; Erdei et al., 2007; Utescher et al., 2008; Ivanov
et al., 2011). Late Miocene vegetation included a
mixture of swamp and riparian forests, with decreasing laurophyllous taxa, among freshwater marshes
and wet prairies (Hofmann & Zetter, 2005; Utescher
et al., 2008; Ivanov et al., 2011). In the early Pliocene, the area was uplifted, reducing the Paratethys
to the Black and Caspian seas, and by the middle
Pliocene the region had a warm, humid climate, supporting many South-East Asian faunal elements
(J
anossy, 1986; Popov et al., 2006; Van Dam, 2006;
Kov
acs et al., 2011). At the end of the Pliocene and
throughout the Pleistocene (including cold phases
and the Holocene), steppes occupied the Pannonian
basin (Magyari et al., 2010), as attested by the grassland character of fossil land snail faunas (Mitrovic,
2007). However, rivers flowing from high mountains
maintained relatively small, humid terrestrial habitats, thus providing adequate glacial refugia for several terrestrial species (Schmitt, 2007).
Before losing much of its Alpine headwaters, the
late Pliocene Danube had a much larger flow with
huge spring floods, giving rise to extensive habitats
suitable for the evolution of specialists. The origin of
V. suevica and V. declivis can be traced to the Danube biodiversity hotspot – in the Pliocene highlands
forming the early Danube upper drainage. The
occurrence of V. declivis in the Drava and Sava river
systems, which flow into the Danube deep within the
forest steppe region, is probably the result of dispersal along riverside habitats during more humid
periods. The long-distance dispersal of either species
following river drainages necessitates an efficient
mechanism of passive dispersal.
A VIOPHILIA
VS. AVIOPHOBIA
On the basis of all available evidence, I hypothesize
that the various Vallonia species differ in their dispersal strategies (Table 2). The range of V. tenuilabris has experienced enormous expansions and
contractions throughout the Quaternary; its extinction in Central Europe marks the onset of the Holocene (F}
uk€
oh, 1993, 1995). It is now restricted to very
cold regions in northern Asia, inhabiting various vegetation types, most often wet prairies (White et al.,
2008; Gerber & B€
ossneck, 2009; Meng, 2009a;
Hors
ak et al., 2010; Hoffmann et al., 2011). Indeed,
this species appears to be well suited for passive dispersal by migrating birds (Meng, 2009b), as for other
tiny grassland Boreo–Alpine snails, such as those
belonging to Vertiginidae (Meng, 2008). A comparable aviophilia may account for the wide, but markedly discontinuous, range of V. enniensis, limited to
undisturbed wet sites such as calcareous swamps
and spring-fed meadows in central Europe and the
Mediterranean region (Kerney et al., 1983; Gerber,
1996). It is unclear, however, whether such ability
for aerial dispersal is caused by any behavioural and
life-history traits of V. tenuilabris and V. enniensis
(as well as widely distributed species such as V. costata, V. pulchella, and V. excentrica) that are not
present in either V. suevica or V. declivis. At least
two types of mutually non-exclusive hypotheses can
be formulated.
Internal factors in behaviour and life history can
translate into differences in suitability for passive
dispersal. A stronger clinging ability of V. tenuilabris, which lives in windswept open habitats, would
© 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 115, 826–841
SPECIALISM OF EUROPEAN RIPARIAN SNAILS
833
Table 2. Ecological and biogeographical traits of European Vallonia species: distribution, degree of range fragmentation, type of habitat, conservation status [critically endangered (CR), endangered (EN), vulnerable (VU), and least concern (LC)], and hypothesized dispersal vectors are shown
also prevent falling off from birds. In contrast, wet
meadow specialists may have a greater tendency to
fall off if disturbed; this would be advantageous
against accidental swallowing by grazing terrestrial
herbivores. Moreover, relevant variability in life-history traits among Vallonia species can be suspected
from the common occurrence of aphallic individuals,
which opens a wide span of possible reproductive
modes (as suggested for other land snails by Riedel,
1953).
Differences in dispersal ability may be external,
related to the vectors responsible for passive dispersal. The role of vertebrates in the dispersal of
molluscs was noticed by Darwin (1859) but has long
remained anecdotal, as well as under reluctance by
most malacologists (Cameron, 2013). In temperate
lowland floodplains, dispersal on wading birds is
indeed common for gastropods (Darwin, 1859: 385;
Rees, 1965; van Leeuwen & van der Velde,
2012a2012a; van Leeuwen et al., 2013). Endozoochory by birds may also be widespread among freshwater snails, especially if ingested together with
macrophytes (van Leeuwen et al., 2012b2012b,
2012cc; Viana et al., 2013). Birds that actively store
tiny snails among their feathers to use them as food
during their long flights (Rees, 1965; Wesselingh,
Cadee & Renema, 1999) are common in Boreal and
Alpine grasslands. This aerial mechanism would
explain the enormous ranges of many tiny Boreo–
Alpine land snails, such as V. tenuilabris, as well as
their ability to track with precision the wide ecological changes triggered by glacial cycles. It is also clear
now that dispersal of land snails through endozoochory by birds may be unexpectedly common (Wada,
Kawakami & Chiba, 2012). This might explain the
invasive character of ubiquitous congenerics (V. costata, V. pulchella, and V. excentrica). In the case of
V. enniensis, whose highly fragmented distribution
appears to have been so even before the recent
reduction in available habitat, a possible vector is
the woodcock, Scolopax rusticola (Linnaeus, 1758).
This bird feeds selectively on small, terrestrial, softbodied animals in humid habitat patches (Hirons &
Johnson, 1987; Duriez et al., 2005). It also appears
to have a marked population structure (Memoli &
Paffetti, 2007) that may account for the circumscription of V. enniensis to the Western Palaearctic. In
contrast, dispersal by birds cannot account for the
geographically and ecologically limited distributions
of V. suevica and V. declivis. Waders could disperse
them along rivers, but then these snails would also
occur in habitats disconnected from streams, such as
lake shores and isolated wetlands. It appears that
these two Vallonia species have not coincided in time
and space with adequate aerial vectors (if these are
not avoided altogether), thus remaining endemic to a
comparatively small temperate continental area.
F ISH
GHOSTS
In general, propagule dispersal is determined by the
migratory strategy of the disperser, the region
through which the disperser population moves, and
the propagule characteristics (Viana et al., 2013).
Thus, nonflying vertebrate vectors moving along rivers must have acted as dispersers of V. suevica and
V. declivis because their ranges cannot be explained
by passive dispersal by water or birds or by their
exceedingly limited active dispersal ability.
Dispersal by fishes (ichthyochory) was a key process in natural European rivers. There is growing
evidence that fishes are major seed dispersers in
floodplain and riparian forests in both tropical and
temperate rivers (Reys, Sabino & Mauro Galetti,
2009; Horn et al., 2011), ensuring upstream dispersal
(Horn, 1997). This process is a generalized dispersal
system (Horn et al., 2011), involving distinct stages
that have been barely studied (Pollux, 2011). However, it is clear that big-river specialist molluscs also
benefit from dispersal by fishes in Europe. It was
© 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 115, 826–841
834
C. R. ALTABA
Figure 4. Proposed dispersal by fish (ichthyochory) of the riparian specialist Vallonia. Local populations built up in riverside meadows, which were grazed by fishes during seasonal floods. These tiny snails would become intentionally or
accidentally ingested; some could survive gut passage, providing them with the chance of being released in adequate
habitats. Migrating fish carried them over long distances, ensuring upstream recolonization. Fish depicted are Coregonus maraena (grazing) and Coregonus oxyrinchus (migrating).
first hypothesized (Altaba, 1990), and then proved
(Lopez et al., 2007), that the European sturgeon (Acipenser sturio) is a temporary host for the larvae of
the giant pearlmussel (Margaritifera auricularia).
Such a parasitic relationship is a trait of almost all
freshwater mussels (Unionida); however, in this case,
the narrow host specificity had major ecosystem-wide
consequences: this bivalve was once a common keystone element of benthic communities in big rivers
throughout western Europe and was dispersed over
large distances, even among separate drainages, by
one of the most abundant, heavy, and long-lived
fishes. The much smaller freshwater blenny (Salaria
fluviatilis) can also be a host of this pearlmussel,
accounting for short-range dispersal within southern
drainages (Lopez & Altaba, 2000, 2005).
Ichthyochory of the meadow specialist Vallonia
may have been rather generalized and similar to that
of seeds or pearlmussel larvae. In the Danube drainage, several species of fish occupy flooded meadows
(Jurajda, Ondrackov
a & Reichard, 2004). These
snails may be preyed upon or accidentally ingested
by fishes, such as Coregonus salmonids, grazing
there, and then released in other suitable habitats
(Fig. 4). Indeed, aquatic molluscs (bivalves and aquatic gastropods, even including non-operculate snails)
survive passage through the gut of benthic-feeding
Coregonus, suggesting that fish may play an important role in their dispersal within freshwater systems
(Brown, 2007). Coregonus may move up to 500 km in
one summer (Chang-Kue & Jessop, 1997), and were a
major element of the Rhine fauna (Borcherding et al.,
2014). Thus, upstream movements by fish (rheophyly)
would ensure the necessary, continuous recolonization of upstream habitats, whilst seasonal migration
of hosts would disperse the snails over large distances. Also, fishes colonizing new drainages through
stream capture would carry along the tiny snails.
Dispersal through endozoochory yields a distribution
of propagules that is clumped, nonrandom, and
highly context-dependent (Lehouck et al., 2012). In
the pristine rivers of Central Europe, ichthyochory
© 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 115, 826–841
SPECIALISM OF EUROPEAN RIPARIAN SNAILS
would have ensured an efficient mechanism to thrive
in otherwise inhospitable or unreachable habitats.
CONCLUSIONS
The biogeographical pattern of V. declivis and
V. suevica appears to be the outcome of their strictly
riparian habitat coupled with dispersal by fish over a
changing landscape. From this perspective, the
notion of specialism becomes rather questionable.
Would a naturalist travelling across Central Europe
a millennium ago, provided she was able to discriminate the various species of Vallonia, ever come up
with the idea that those thriving along all rivers were
specialists? In agreement with Loxdale et al. (2011),
the dichotomy of specialism vs. generalism may be
just a semantic artefact. Indeed, the recognition of
specialism will depend on the scale and goal of observation (Devictor et al., 2010). Besides, under the
niche paradigm (Southwood, 1977; Brouat et al.,
2004; Fried, Petit & Reboud, 2010), these imperilled
riparian species might paradoxically qualify as generalists, being adapted to environments subject to very
intense natural disturbance and having (had) an
unusually high dispersal ability. It seems reasonable
to attribute this paradox to two factors. First, to inadequate theory, at least because relative differences in
niche breadth depend critically on the variables considered (Peers, Thornton & Murray, 2012). Thus, the
concept of niche is a construct (or artefact) only valid
as a time-honoured shorthand (McInerny & Etienne,
2012) for whatever scope-delimited requirements or
interactions of species (Guisan & Thuiller, 2005;
Kearney & Porter, 2009; Kearney et al., 2010; Peterson et al., 2011). In addition, and most relevant, specialism is context-dependent in a fundamental sense
– beyond methodological and scaling considerations,
what matters is the ecological and evolutionary context in which a given species exists. In this sense,
calling both riparian Vallonia specialists is useful as
a contrasting remark. On the one hand, it shows that
they do not belong to the set of weedy, invasive congenerics, and, on the other, it highlights their current
restriction to habitats that are now scarce, impoverished, interaction-depriven, and thus dysfunctional.
Native riverine ecosystems have been destroyed,
almost completely, throughout Europe. Thus, natural
dispersal mechanisms have been disrupted, leading
big-river specialist molluscs and associated fishes to
the brink of extinction. The catastrophic decline of
freshwater and riparian molluscs is a global process
(Altaba, 2003; Lydeard et al., 2004), just older, and
thus more advanced, in Europe. All anadromous fishes
have experienced dramatic declines in the North
Atlantic (Limburg & Waldman, 2009). Freshwater
835
fishes that made massive migrations along European
rivers have also been decimated. As a case in point,
the once economically important Coregonus oxyrinchus is now extinct (Freyhof & Sch€
oter, 2005). Likewise, sturgeons, blennies, and giant pearlmussels are
nearly extinct (Altaba, 2003). The survival of V. suevica and V. declivis depends critically on ecological restoration at the drainage scale, or at least the
management of riparian habitats that may mimic the
original conditions.
Viewing ecological specialism as a context-dependent attribute may be useful for understanding complex ecosystems. An explicit recognition of context,
far from indulging in sterile relativism, widens the
boundaries of science (as postulated by Edmonds,
2013). In evolutionary ecology, context means introducing real-life variation across scales in interaction
outcome into experimental design and models, including the impact of gradients that may be spatial, abiotic, or related to the abundance of other species
(Thompson, 1988; Bronstein, 1994; Kiers et al., 2010;
Chamberlain, Bronstein & Rudgers, 2014). Thus, the
tiny, rare snails point at a much wider picture. Arguably, Europe’s wealth was triggered through harnessing and transforming its rivers. Between the
Mediterranean and Boreal regions, Europe was once
a land of big wild rivers carrying an enormous energy
load, thus being major migration pathways for plentiful wildlife and spreading seasonally over huge floodplains. Europe’s geopolitical dominance was surely
not caused by unusually efficient organization (e.g.
North & Thomas, 1973), a unique human ability or
attitude (e.g. Mead, 2008), geographical determinism
(e.g. Diamond, 1997; Shenefelt & White, 2013), or
sheer luck (e.g. Deutsch, 2011). Instead, it was a complex process based on a favourable hydrological setting – a combination of abundant fertile lands and
nearshore seas with hydraulic power available for
modern technology in societies that gradually (and
often brutally) organized in accordance. The ensuing
alteration of large-scale ecosystem processes also
resulted in massive habitat loss and stark impacts on
native biodiversity. The wet-meadow Vallonia specialists remain a vanishing witness. Improvements in
the ecological condition of Europe’s rivers and lakes
are certainly being carried on in spite of several
drawbacks (IKSR, 2009; Hering et al., 2010). However, recovering the functionality of big rivers is more
than a matter of clean water and fishways. The
extinction of native species and the spread of invasive
ones impose a heavy toll on ecological restoration
(e.g. Dubey, Leuenberger & Perrin, 2014). In my
experience, too many European freshwater ecologists
have never seen, or even conceived, a wild river with
its native fauna. As recognized by the European Commission (2012), the river basin management plans
© 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 115, 826–841
836
C. R. ALTABA
devised under the Water Framework Directive constitute largely a missed opportunity for real integrated
water management. Once revered and now thoroughly tamed, it may be time to rethink what European rivers should be. At least it seems that
understanding riverine biotas requires knowledge
about the pristine conditions where they evolved.
ACKNOWLEDGEMENTS
Lina Ponsell, Margarita Bota, and F. Javier Pomar
helped in the field in Slovakia, together with my
children Laia and Jordi. Miquel Angel
Lopez Robles
contributed shaping my perception of big-river molluscs. Jaume Belda, at Centre de Recursos per a
l’Educacio Ambiental de les Illes Balears, assisted in
finding literature. Friendly discussion of taxonomic
and biogeographical ideas with Francisco WelterSchultes was most helpful. Guido Poppe kindly provided Vallonia shells collected by Rolf Brandt.
Thoughtful comments by nine anonymous reviewers
have also been highly constructive.
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SUPPORTING INFORMATION
Additional Supporting Information may be found in the online version of this article at the publisher’s web-site:
Appendix S1. The remarkable land snail community at Devın Gate.
Appendix S2. Historical ranges of Vallonia suevica and V. declivis.
© 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 115, 826–841