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The marbled crayfish (Procambarus fallax f. virginalis) has become one of the potentially most dangerous non-indigenous crayfish species spreading in European countries and elsewhere. This taxon reproduces parthenogenetically and recently has been verified as a vector of the crayfish plague pathogen. Here, we report on two established populations of marbled crayfish in the Czech Republic. The marbled crayfish was observed during autumn 2015 in an urban pond connected by sewer piping with the Rokytka brook near its mouth to the Vltava River in Prague. Subsequently, three adult females, two of them having well-developed glair glands and oocytes, were captured in this pond during spring 2016, suggesting successful overwintering of the local population. Furthermore, four adult females were captured in an artificial pond at the Radovesická lignite spoil heap in the vicinity to the industrial conurbation of Bílina in summer 2016; one of them carried eggs. We tested these for the presence of the crayfish plague pathogen Aphanomyces astaci, with negative results. The introduction pathway for both populations is most likely a release from private aquaria, as these sites are popular for recreation activities. Our findings substantiate previous predictions that conurbations are likely to be the primary areas for marbled crayfish introductions.
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Biologia 71/12: 1380—1385, 2016
Section Zoology
DOI: 10.1515/biolog-2016-0164
Predictions of marbled crayfish establishment in conurbations
fulfilled: Evidences from the Czech Republic
Jiří Patoka1, Miloš Buřič2,Vojtˇech Kolář3,4,MartinBláha2, Miloslav Petrtýl1,
Pavel Franta2,RobertTropek3,5,LukášKalous1,AdamPetrusek5&AntonínKouba2
1Department of Zoology and Fisheries, Faculty of Agrobiology, Food and Natural Resources, Czech University of Life
Sciences Prague, Kamýcká 129,CZ-16500 Praha 6, Czech Republic; e-mail:
2Faculty of Fisheries and Protection of Waters, South Bohemian Research Center of Aquaculture and Biodiversity of Hy-
drocenoses, University of South Bohemia in České Budˇejovice, Zátiší 728/II, CZ-38925 Vodňany, Czech Republic
3Institute of Entomology, Biology Centre, Czech Academy of Science, Branišovská 31,CZ-37005 České Budˇejovice, Czech
4Department of Ecosystem Biology, Faculty of Science, University of South Bohemia, Branišovská 1760,CZ-37005 České
Budˇejovice, Czech Republic
5Department of Ecology, Faculty of Science, Charles University, Viničná 7,CZ-12844 Praha, Czech Republic
Abstract: The marbled crayfish (Procambarus fallax f. virginalis) has become one of the potentially most dangerous non-
indigenous crayfish species spreading in European countries and elsewhere. This taxon reproduces parthenogenetically and
recently has been verified as a vector of the crayfish plague pathogen. Here, we report on two established populations of
marbled crayfish in the Czech Republic. The marbled crayfish was observed during autumn 2015 in an urban pond connected
by sewer piping with the Rokytka brook near its mouth to the Vltava River in Prague. Subsequently, three adult females,
two of them having well-developed glair glands and oocytes, were captured in this pond during spring 2016, suggesting
successful overwintering of the local population. Furthermore, four adult females were captured in an artificial pond at
the Radovesická lignite spoil heap in the vicinity to the industrial conurbation of Bílina in summer 2016; one of them
carried eggs. We tested these for the presence of the crayfish plague pathogen Aphanomyces astaci, with negative results.
The introduction pathway for both populations is most likely a release from private aquaria, as these sites are popular for
recreation activities. Our findings substantiate previous predictions that conurbations are likely to be the primary areas for
marbled crayfish introductions.
Key words: Procambarus fallax f. virginalis; biological invasion; first record; pet trade; Marmorkrebs; urban pond; post-
mining site
The introduction, establishment, and subsequent
spread of non-indigenous crayfish species (NICS) are
known to constitute one of the main factors seriously
affecting abundance of European indigenous crayfish
species (Peay 2009; Gherardi et al. 2011; Perdikaris
et al. 2012; Chucholl 2014). The trade for ornamen-
tal purposes (pet trade) has been considered an impor-
tant source of new alien species introductions world-
wide (Padilla & Williams 2004; Duggan 2010; Chucholl
2013; Patoka et al. 2015a, 2016). The pet trade in im-
ported crayfish started to expand around 1995, and
consequently production of crayfish for ornamental pur-
poses developed in various countries (Vogt et al. 2004;
Faulkes 2010; Patoka et al. 2015b). Germany, currently
with 28 NICS available for sale (Chucholl & Wendler
2016), and the Czech Republic, with 27 NICS (Patoka
et al. 2014a, b), have been identified as the leading Eu-
ropean countries in this regard.
The marbled crayfish (Marmorkrebs in German)
has been identified as one of the most dangerous of or-
namental NICS from a European perspective (Scholtz
et al. 2003; Chucholl 2014; Patoka et al. 2014a; Ko-
tovska et al. 2016; Souty-Grosset et al. 2016). Although
it cannot be excluded that the origin of this triploid
parthenogenetic crayfish could have been a hybridiza-
tion between Procambarus fallax (Hagen, 1870) and
some other species of the genus Procambarus (Martin
et al. 2016), it is usually regarded as a parthenogenetic
form of the former (P.fallax forma virginalis Martin
et al., 2010). Although the native geographical distri-
bution of this form, if at all present in the wild, is still
unknown (Martin et al. 2010, 2016; Kouba et al. 2014),
the sexually reproducing P.fallax occurs in Florida and
Georgia (Taylor et al. 2007).
Populations of the marbled crayfish are exclusively
composed of females, which reproduce by obligatory
apomictic parthenogenesis. Thus, a single female can
theoretically be sufficient to establish a viable popula-
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Marbled crayfish establishment 1381
Fig. 1. Map showing the location of the Přátelství Park in Prague (A), and the Jiřina pond (B) at the Radovesická spoil heap, Czech
Republic; both indicated by white asterisks. The crayfish female on the photo was captured by funnel trapping in the Jiřina pond.
The basis for the maps are available under the Open Database License (
tion (Scholtz et al. 2003). This reproduction strategy,
together with low intraspecific aggressiveness, a gener-
ation time of only 6 months, and high fecundity, fre-
quently lead to population explosion in a very short
time (Scholtz et al. 2003; Vogt et al. 2004).
This crayfish has been recorded in the wild in sev-
eral European countries, including Croatia, Germany,
Hungary, Italy, the Netherlands, Slovakia, Sweden, and
Ukraine (Nonnis Marzano et al. 2009; Chucholl & Pfeif-
fer 2010; Janský & Mutkovič 2010; Soes & Koese 2010;
Bohman et al. 2013; Samardži´c et al. 2014; Vojkovská
et al. 2014; Weiperth et al. 2015; Lipták et al. 2016;
okk¨os et al. 2016; Novitsky & Son 2016), although
the establishment success in some of those countries
is not clear. As one of the negative effects to native
biodiversity, ornamental animals can serve as impor-
tant hosts and vectors of exotic commensals (Patoka
et al. 2015a) and pathogens (e.g., Martinez-Murcia et
al. 2008; Kalous et al. 2015). Indeed, marbled crayfish
has been recently confirmed as a vector of the crayfish
plague pathogen Aphanomyces astaci Schikora (Keller
et al. 2014; Mrugala et al. 2015), which still threat-
ens European indigenous crayfish species (Holdich et
al. 2009). Due to its invasion potential as well as dis-
ease carrier status, marbled crayfish has been recently
included, together with four other invasive crayfish of
North American origin, in the list of 37 Invasive Alien
Species of European Union Concern (EU Regulation
No. 1143/2014; Commission Implementing Regulation
No. 2016/1141).
We present here the first records of marbled cray-
fish from open waters in the Czech Republic from two
different, geographically distant sites, in which it seems
to have established populations. In an urban pond lo-
cated in the city of Prague, we could confirm a suc-
cessful overwintering of the population. In a pond on
a post-mining spoil heap close to Bílina, several adult
animals were captured, one of which carried eggs in late
summer. Perdikaris et al. (2012), Chucholl (2014), and
Souty-Grosset et al. (2016) had noted that the occur-
rence of some NICS in European waters, including the
marbled crayfish, is entirely driven by propagule pres-
sure in relation to the pet trade, and that crayfish are
usually released into the nearest ponds or streams in
the vicinity of conurbations. Our observations support
this view.
Material and methods
Study sites
The first site, Přátelství Park, is situated in the town dis-
trict Prosek, Prague, Czech Republic (GPS 500721 N,
142943 E) at the altitude 288–295 m a.s.l. (Fig. 1A). The
park was founded for recreational purposes of local inhabi-
tants. The park contains a system of small ponds connected
with cascades and channels. This system, which was reno-
vated in 2008, has a total length of 450 m and volume of
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1382 J. Patoka et al.
1800 m3. The water is circulated through the vegetation
season and kept at a low level. The majority of the system
is completely drained at the end of vegetation season, with
the exception of a pond (denoted as A in Fig. 1). In late
autumn, the water is discharged into the water sewer con-
nected with the Rokytka brook close to its confluence with
the Vltava River (Elbe basin). The bottom and banks of
ponds and channels are made from concrete, and the bot-
tom is covered by a thin layer of mud and detritus, mainly
formed by leaf litter. Aquatic macrophytes are represented
at the site by three patches of water lilies (Nymphaea alba
L.). These plants are taken out of the water over winter.
The second site, Radovesická spoil heap (Fig. 1B), is
situated in the North Bohemian lignite basin. The whole
area is heavily affected by opencast lignite mining, result-
ing also in numerous larger heaps of spoil consisted mainly
of tertiary clays. The Radovesická spoil heap is a relatively
large heap (ca 12.5 km2) formed between 1964 and 2003 in
a vicinity to the Bílina conurbation. Its majority has been
technically reclaimed with artificial creation of several pools
and ponds supplemented by numerous pools formed spon-
taneously in the terrain depressions (Harabiš et al. 2013).
The Jiřina pond (0.6 ha; GPS 503308 N, 134853 E;
altitude 340 m a.s.l.; denoted as B in Fig. 1) is a middle-
sized artificial pond created in the early 1990s for the future
recreation of Bílina inhabitants. Although still officially in-
accessible, it is already relatively popular for fishing and
swimming. It has no affluent, but there is an outlet con-
ducting water after strong rains or snowmelt to a drainage
channel system flowing into the Bílina River (Elbe basin).
The pond banks and bottom are formed by clays and are
regularly rounded and highly homogeneous. Its littoral zone
is very narrow (max. 1 m) because the bottom steeply de-
scends to the depth of over 2 m; it is dominated by dense
common reed [Phragmites australis (Cav.) Trin. ex Steud.]
and much sparser bladderwort (Utricularia sp.).
Data collection
Marbled crayfish was first observed to occur in open wa-
ters in the Czech Republic during October 2015, when
three individuals were captured in the Přátelství Park by
Jakub Friedl, a student of the Czech University of Life Sci-
ences Prague. These crayfish were photographed and subse-
quently released to the pond. On 16 March 2016, we inten-
sively sampled the pond by electrofishing, using a backpack
electroshocker (Bednář; Supplementary
sampling included small seine-netting and sweep-netting in
In the Radovesická spoil heap, the first marbled cray-
fish was recorded on 30 July 2016. A female entered one of
five funnel traps (80 ×27.5 ×27.5 cm, 0.5 cm green mesh
nylon, 3.5 cm of an entrance diameter) exposed for 24 hours
in the littoral zone for the purpose of aquatic insect moni-
toring. In the night of 3 September 2016, we exposed eight
funnel traps in the littoral zone close to the first record. We
also actively searched for crayfish by snorkelling, by sweep-
netting of detritus and littoral vegetation, and exploring
potential shelters.
All animals captured in both surveyed sites were identi-
fied immediately after their capture and subsequently, with
exception of crayfish, were returned to the pond.
The identity of crayfish specimens was verified by both mor-
phological and genetic analyses. Morphological analyses fol-
lowed Martin et al. (2010). The mitochondrial gene for the
cytochrome c oxidase subunit I (COI) from one captured fe-
male per each site was sequenced using the universal primer
pair LCO1490/HCO2198 (Folmer et al. 1994) and following
the protocols described in Mrugala et al. (2015).
Testing for the presence of the crayfish plague pathogen
As the marbled crayfish may host the crayfish plague
pathogen Aphanomyces astaci (Keller et al. 2014; Mrugala
et al. 2015), we analysed individuals captured at the
Radovesická spoil heap for the presence of its DNA, follow-
ing the protocols in Mrugala et al. (2015). We dissected the
soft abdominal cuticle and telson of each individual, and
isolated DNA from the mixed subsample of these tissues
(ca 50 mg per individual) by DNeasy tissue kit (Qiagen) to
the volume of 200 µl. Then, TaqMan minor groove binder
quantitative PCR (qPCR) assay modified from Vr˚alstad et
al. (2009), which specifically and with high sensitivity de-
tects A. astaci DNA, was run on iQ5 real-time PCR de-
tection system (Bio-Rad), using 5 µl of the DNA isolate in
25 µl reaction. Further details of the protocol are provided
in Mrugala et al. (2015) and Svoboda et al. (2014).
Three females were captured in the pond A of the Přá-
telství Park (Fig. 1A) in March 2016. The first indi-
vidual, with cephalothorax length (CL, measured from
tip of rostrum to posterior end of cephalothorax) of
35 mm and total body length (BL, measured from tip
of rostrum to posterior edge of telson) of 73 mm was
captured by electrofishing and had a carapace surface
densely covered by periphyton. The other two females
(CL/BL of 33/70 and 32/70 mm) were captured by
sweep-netting in detritus and had well-developed glair
glands and oocytes.
Four females were captured in the Jiřina pond at
the Radovesická spoil heap (Fig. 1B). In July 2016 one
individual (CL/BL of 56/115 mm) was captured by fun-
nel trapping. In September 2016, one female entered a
funnel trap at the same location as the first one, and
two females were found in shelters under a stone and a
sunken concrete block close to the pond bank (CL/BL
of 38/83, 42/90, and 42/90 mm). One of the two larger
individuals carried three eggs.
Morphological characteristics of the crayfish cor-
responded with the description given in Martin et al.
(2010). The DNA barcoding confirmed the morphologi-
cal identification of the captured crayfish as P.fallax f.
virginalis. The obtained COI fragments matched com-
pletely each other and the reference sequences for mar-
bled crayfish publicly available from GenBank (acc. nos.
KC107813, HM358011, JF438007; Filipová et al. 2011;
Martin et al. 2010; Shen et al. 2013). The qPCR assay
did not detect DNA of A. astaci in any of the tested
Fish stock captured by electroshocking and seine-
netting in the pond A of the Přáteství Park included the
following potential crayfish predators: catfish Silurus
glanis L., 1758 (2 subadults), perch Perca fluviatilis L.,
1758 (2 adults), carp Cyprinus carpio L., 1758 (1 adult).
Also, five pairs of mallard ducks (Anas platyrhynchos
L., 1758) were observed feeding at the site. In the Jiřina
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Marbled crayfish establishment 1383
pond at the Radovesická spoil heap, we have observed
several (sub)adults of eel Anguilla anguilla (L., 1758).
We discovered and subsequently surveyed two popu-
lations of marbled crayfish occurring within an urban
pond system in Prague and at a larger artificial pond
on a reclaimed spoil heap. Based on our results, we con-
sider both populations to be established. The repeated
findings of marbled crayfish in the Přátelství Park sug-
gest that the local population successfully overwintered
in the pond that had not been drained at the onset of
winter. Although the marbled crayfish has been consid-
ered a warm water taxon (Chucholl & Pfeiffer 2010),
its established populations occur in European temper-
ate zone (Chucholl et al. 2012; Lipták et al. 2016) and
tolerance to winter water temperatures was confirmed
also experimentally (Veselý et al. 2015). However, an
alternative scenario that animals found in the Přátel-
ství Park after winter originated from repeated intro-
ductions of marbled crayfish from aquaria cannot be
entirely ruled out without a continuous monitoring or
a capture-recapture study. The reproductive potential
of the local population is indicated by the fact that the
captured females had well-developed glair glands.
All females from the Radovesická spoil heap were
large adults, which are likely to reproduce in situ.One
was observed to carry a few eggs at the end of summer,
when no other crayfish species in Central Europe breed
(Reynolds 2002). We presume this was a remainder of
originally larger clutch, considering that the typical size
at maturity of this species (at least in laboratory con-
ditions) is less than half of the size of captured females,
female fecundity increases with body size, and brood
sizes even for very small females usually exceed 45 eggs
and may reach up to hundreds of eggs (Seitz et al. 2005;
Kouba et al. 2015).
At present, marbled crayfish apparently does not
reach high density in either of the studied sites. We
hypothesise that the low number of captured individu-
als in the Přátelství Park could be caused by draining
of the channels, and concentration of water only into
the pond A over the winter season. The low water level
can be very harmful for crayfish due to intensive pre-
dation pressure from mallard ducks (Malone 1965) as
well as by fish (Syväranta et al. 2010), which are abun-
dant at the location. In the Radovesická spoil heap, we
presume a strong predation pressure by the relatively
abundant European eel, which has a strong potential
to decrease the crayfish population density (Aquiloni et
al. 2010). Furthermore, the presence of these predators
likely drives the crayfish into little accessible shelters,
making the manual surveys less effective.
However, it must be underscored that without
rapid management activity focusing on extirpation or
control of these populations, we expect a substantial
potential of the spread of marbled crayfish from both
sites. In the Přátelství Park, crayfish may drift through
the water outlet to the nearby adjacent water bodies.
Although the Jiřina pond at the Radovesická spoil heap
is not permanently connected with any other waters, its
outlet is filled by water after strong rains or during a
spring melting when superfluous water flows into the
drainage system, including more artificial ponds and
finally flowing into the Bílina River. Thus, the estab-
lishment of marbled crayfish in some adjoining water
bodies is also possible. At the spoil heap, both stag-
nant (Harabiš et al. 2013; Vojar et al. 2016) and flowing
(Tichanek & Tropek 2015, 2016) waters are known to
harbour unusually rich freshwater biodiversity, which
can be potentially threatened by the expanding mar-
bled crayfish. In particular, some of the local ponds
have been recently stocked by the native noble cray-
fish Astacus astacus (L., 1758) after a rescue transfer,
as the area has been considered free of alien species
that may directly affect this protected species vulnera-
ble to crayfish plague. Although we did not detect A.
astaci in captured crayfish, the low number of tested
crayfish does not guarantee absence of the pathogen
in the studied site; furthermore, even if the population
is pathogen-free at the moment, infection by A. astaci
sometimes in the future cannot be entirely ruled out.
Both aquarium and garden fishkeeping are tradi-
tionally popular and widespread in the Czech Repub-
lic. Although the release of non-native organisms is il-
legal, irresponsible or uninformed hobbyists frequently
release their pets, including crayfish, into the wild (Pa-
toka et al. 2014b). Hence, the propagule pressure (sensu
Duggan et al. 2006) is high. As noted by Patoka et al.
(2015b), marbled crayfish originate almost exclusively
from domestic production in quantities estimated to be
as high as 100,000 individuals annually in the Czech
Republic. In comparison with recorded retail prices of
other traded crayfish species ( 2.0 to 25.92), the mar-
bled crayfish is very inexpensive and thus widely acces-
sible; the lowest recorded price was 0.55 per individ-
ual (Patoka et al. 2015b). In addition to its low price,
the species is popular, is easy to keep and breed, repro-
duces rapidly and asexually, and has a short generation
time (Faulkes 2015). These facts support the assump-
tion that the discovered population originated due to
intentional release from aquaria.
Chucholl et al. (2012) and Chucholl (2014) have
predicted that the number of established populations
within European territory will further increase due to
release by hobbyists of surplus and unwanted crayfish
at new sites near conurbations. This suggestion is sup-
ported by our both findings from Prague and the vicin-
ity of Bílina, together with other recent records of mar-
bled crayfish occurrence, such as in Budapest, Hun-
gary (Weiperth et al. 2015), and Dnepropetrovsk and
Odessa, Ukraine (Novitsky & Son 2016). Populations
established in conurbations may serve as the source
for further, spontaneous spread. The North American
NICS have been evaluated as more dangerous for na-
tive European astacofauna than traded crayfish species
originating from elsewhere in the world (Patoka et al.
2014a). In agreement with other authors (Peay 2009;
Magalh˜aes & Andrade 2014), we recommend further
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1384 J. Patoka et al.
education of the general public and sharing of infor-
mation which will improve knowledge as to how dan-
gerous are NICS and how important is conservation of
indigenous crayfish species. As both discovered Czech
populations of marbled crayfish are in isolated water
bodies, their eradication before the further expansion
of crayfish should be attempted.
The authors thank Marie Lupomˇeská (Town District Prague
9) for permission to survey the urban pond, Jakub Friedl
for reporting on the presence of crayfish in the Přátel-
ství Park, to Filip Tichánek for various information on
the Radovesická spoil heap, and to Zuzana Musilová for
help with sampling at the Radovesická spoil heap. De-
nis Copila¸s-Ciocianu, Nuria Vi˜nuela Rodríguez and Agata
Mrugala helped with laboratory analyses. The study was fi-
nancially supported by the project “CIGA” (No. 20152007),
the Czech Science Foundation (P504/12/2525), the Ministry
of Education, Youth and Sports of the Czech Republic –
projects CENAKVA (No. CZ.1.05/2.1.00/01.0024) and CE-
NAKVA II (No. LO1205 under the NPU I program), and
the University of South Bohemia (GAJU 158/2016/P). En-
glish was proofread by Gale A. Kirking at English Editorial
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... While it has been confirmed that marbled crayfish can act as A. astaci carrier, analysis of specimens of this species from the wild and from the aquarium trade have shown that the presence of A. astaci in their tissues often cannot be verified (Lipták et al., 2016(Lipták et al., , 2017Patoka et al., 2016;Pârvulescu et al., 2017;Andriantsoa et al., 2019;Ercoli et al., 2019;Lenich, 2019;own unpublished data). No infection could be confirmed in 100 tested crayfish from Madagascar (Andriantsoa et al., 2019), 67 specimens from Slovakia (Lipták et al., 2016(Lipták et al., , 2017, four specimens from Czechia (Patoka et al., 2016), nine specimens from Romania (Pârvulescu et al., 2017), six specimens from Estonia (Ercoli et al., 2019), and 20 specimens from Germany (Lenich, 2019). ...
... While it has been confirmed that marbled crayfish can act as A. astaci carrier, analysis of specimens of this species from the wild and from the aquarium trade have shown that the presence of A. astaci in their tissues often cannot be verified (Lipták et al., 2016(Lipták et al., , 2017Patoka et al., 2016;Pârvulescu et al., 2017;Andriantsoa et al., 2019;Ercoli et al., 2019;Lenich, 2019;own unpublished data). No infection could be confirmed in 100 tested crayfish from Madagascar (Andriantsoa et al., 2019), 67 specimens from Slovakia (Lipták et al., 2016(Lipták et al., , 2017, four specimens from Czechia (Patoka et al., 2016), nine specimens from Romania (Pârvulescu et al., 2017), six specimens from Estonia (Ercoli et al., 2019), and 20 specimens from Germany (Lenich, 2019). On the other hand, when marbled crayfish coexists with North American crayfish species, it is usually found to be infected. ...
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For 150 years the crayfish plague disease agent Aphanomyces astaci has been the cause of mass mortalities among native European crayfish populations. However, recently several studies have highlighted the great variability of A. astaci virulence and crayfish resistance toward the disease. The main aim of this study was to compare the response of two crayfish species, the European native noble crayfish (Astacus astacus) and the invasive alien marbled crayfish (Procambarus virginalis), to an A. astaci challenge with a highly virulent strain from haplogroup B and a lowly virulent strain from haplogroup A. In a controlled infection experiment we showed a high resistance of marbled crayfish against an A. astaci infection, with zoospores from the highly virulent haplogroup B strain being able to infect the crayfish, but unable to cause signs of disease. Furthermore, we demonstrated a reduced virulence in the A. astaci strain belonging to haplogroup A, as shown by the light symptoms and the lack of mortality in the generally susceptible noble crayfish. Interestingly, in both marbled crayfish and noble crayfish challenged with this strain, we observed a significant decrease of the detected amount of pathogen’s DNA during the experiment, suggesting that this A. astaci haplogroup A strain has a decreased ability of penetrating into the cuticle of the crayfish. Our results provide additional evidence of how drastically strains belonging to A. astaci haplogroup B and haplogroup A differ in their virulence. This study confirmed the adaptation of one specific A. astaci haplogroup A strain to their novel European hosts, supposedly due to reduced virulence. This feature might be the consequence of A. astaci’s reduced ability to penetrate into the crayfish. Finally, we experimentally showed that marbled crayfish are remarkably resistant against the crayfish plague disease and could potentially be latently infected, acting as carriers of highly virulent A. astaci strains.
... Freshwater ornamental shrimps do not pose such an invasion risk and are not released as frequently as crayfish. Thermal waters are usually popular amongst local people, above all in built-up areas, and the release of exotic crustaceans including shrimps from aquaria-and their survival-is ongoing (Patoka et al., 2016b). ...
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Ornamental aquaculture and the related pet industry are known to be important sources of non-native species worldwide. In the temperate zone, thermal waterbodies are attractive places for irresponsible owners to release unwanted freshwater pets including decapod crustaceans. Several non-native ornamental species have been reported in the thermal locality of Miskolctapolca (a suburb of Miskolc, Hungary). So we surveyed this site in March 2019–November 2021 to update local occurrence records and detect potentially newly released species. A well-established population of Neocaridina denticulata and the occurrence of Caridina cf. babaulti had previously been noted. However, for the first time at this site, we found the shrimps Atyopsis moluccensis, Caridina gracilirostris and C. multidentata, as well as the crayfish Procambarus virginalis, P. clarkii, Cherax quadricarinatus, C. boesemani and C. snowden, and several formally undescribed Cherax species originating from New Guinea. Furthermore, in most species, gravid females carrying eggs were also noticed. Three shrimps, A. moluccensis, C. gracilirostris and C. multidentata, were recorded for the first time in European wild. Further monitoring of this locality and better education of the general public regarding the risks associated with the release of non-native species are strongly recommended.
... The greatest risks related to ornamental aquaculture in Czechia are biological invasions. The risk of intentional release of unwanted aquatic ornamentals exists as confirmed by records of several fish taxa including C. auratus, L. gibbosus and P. reticulata (Koščo et al., 2010) and marbled crayfish (Procambarus virginalis) in the Czech Republic and Slovakia (Lipták et al., 2017;Patoka et al., 2016c), and by irresponsible activities of garden pond vendors (Patoka et al., 2017a). Moreover, nonornamental organisms associated with ornamental aquatic plants and both freshwater and marine animals were imported into Czechia in huge quantities (Akmal et al., 2020;Patoka et al., 2016aPatoka et al., , 2016bPatoka et al., , 2017bLožek et al., 2021;Patoka and Patoková, 2021). ...
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Ornamental aquaculture is an economically important industry with many enthusiasts worldwide. Much of the supply for the industry is provided by individuals and businesses in tropical countries because many ornamental species originated in the tropics. But Czechia, a temperate region in Central Europe, is an exception. Czech suppliers have significantly influenced the global freshwater ornamental aquaculture market for decades. Here we present and discuss the history of ornamental aquaculture in Czechia considering its geopolitical background, social status and history, pet-trade trends, overlapping to research activities, public education, and related risks and threads. We list the most traded and exported species, and list species that rarely reproduce in captivity, but that are successfully bred for commercial purposes by Czech producers globally, we introduce the term “Czech aquarium phenomenon” to describe the substantial economic and scientific importance of Czechia in ornamental aquaculture. Given that the diversity and volume of species traded are vast, we suggest the importance of this phenomenon for consideration to key stakeholders who design aquaculture policies, including the management of invasive alien species and ex-situ conservation programs for endangered species.
... Marbled crayfish is an invasive benthic actively searching omnivorous species spreading across freshwater ecosystems mainly in Europe (Patoka et al., 2016), but also emerging as a model species in various biological disciplines (Hossain et al., 2018;Vogt, 2011). ...
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Phenotypic plastic responses to temperature can modulate the kinetic effects of temperature on biological rates and traits and thus play an important role for species adaptation to climate change. However, there is little information on how these plastic responses to temperature can influence trophic interactions. Here, we conducted an experiment using marbled crayfish and their water louse prey to investigate how short‐term thermal acclimation at two temperatures (16 and 24°C) modulates the predator functional response. We found that both functional response parameters (search rate and handling time) differed between the two experimental temperatures. However, the sign and magnitudes of these differences strongly depended on acclimation time. Acclimation to 16°C increased handling time and search rate whereas acclimation to 24°C leads to the opposite effects with shorter handling time and lower search rate for acclimated predators. Moreover, the strength of these effects increased with acclimation time so that the differences in search rate and handing time between the two temperatures were reversed between the treatment without acclimation and after 24 h of acclimation. Overall, we found that the magnitude of the acclimation effects can be as strong as the direct kinetic effects of temperature. Our study highlights the importance of taking into account short‐term thermal plasticity to improve our understanding of the potential consequences of global warming on species interactions. Temperature effect on feeding rate depends on acclimation temperature and duration. Acclimation to cool temperatures decreases predation rate whereas acclimation to warmer temperature leads to opposite effects. Moreover, the magnitude of the acclimation effects can be as strong as the direct kinetic effects of temperature.
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The widespread presence of North American alien crayfish in Europe is a major driver of native crayfish population declines, mainly because they are chronic carriers of the oomycete Aphanomyces astaci responsible for crayfish plague. Screening for the crayfish plague pathogen in host populations has become a common practice across Europe, but sampling usually covers spatial but not temporal variation. Our study focuses on the current situation in Czechia, where screening for A. astaci was first conducted in the mid-2000s. We provide data about the distribution and prevalence of this pathogen at almost 50 sites with three host crayfish: the spiny-cheek crayfish Faxonius limosus, signal crayfish Pacifastacus leniusculus, and marbled crayfish Procambarus virginalis. Among these sites were 20 localities that were resampled several years (usually more than a decade) after the original screening for A. astaci. We did not detect any A. astaci infection in two studied P. virginalis populations but documented several new hotspots of highly infected P. leniusculus in Czechia, and the first site with the coexistence of the latter with F. limosus. Our data suggest that despite some fluctuations, A. astaci prevalence in North American host populations generally does not tend to change significantly over time; we only observed two cases of a significant increase and one of a significant decrease. We no longer detected A. astaci in several originally weakly infected populations, but our data suggest it likely still persists in these areas and threatens native crayfish populations. At the single known site in the country where P. leniusculus and F. limosus coexist, we documented the presence of the same A. astaci genotype group in both crayfish species, likely due to interspecific transmission of the pathogen from the former host to the latter. However, genotyping of A. astaci in infected host individuals still supported the link between specific pathogen genotypes and crayfish hosts, suggesting that assessment of sources of mass mortalities from the pathogen genotyping is feasible in European regions where the mutual contact of different American crayfish species is uncommon.
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Invasive species have long been recognized as a serious threat to freshwater ecosystems. This is especially true for invasive species in keystone positions in food webs that can cause major disruption and can lead to unexpected outcomes. Crayfish occupy a central trophic position and non-indigenous crayfish have been shown to substantially disrupt ecosystems they invade. Here, we assess eight non-indigenous crayfish to 21 freshwater ecoregions in Canada using a screening-level risk assessment. We found that ecoregions in Canada that were warmer and contained high native freshwater diversity were most at risk from crayfish invasions, particularly: the Laurentian Great Lakes, St. Lawrence, English-Winnipeg Lakes and Coastal British Columbia ecoregions. Four crayfish species consistently had higher scores: rusty (Faxonius rusticus), virile (Faxonius virilis), signal (Pacifastacus leniusculus), and red swamp (Procambarus clarkii). Of these high-risk crayfish, only the red swamp crayfish is not yet established in Canada but is present in US waters of the transboundary Great Lakes ecoregion. Our study is the first to evaluate the relative risks that non-indigenous crayfish pose to freshwater ecosystems in Canada.
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Freshwater ecosystem functioning is often thought to be dominated by fish, determining the community structure via top-down control and ecosystem engineering. However, freshwater crayfish can have an even stronger effect on food web and ecosystem functioning, operating as keystone species in a water body (Longshaw and Stebbing, 2016). As environmental engineers, crayfish have a significant impact on the biodiversity within their habitat (Souty-Grosset et al., 2006). Yet over the past 150 years freshwater crayfish in Europe have faced a novel challenge in the form of a lethal disease caused by the oomycete Aphanomyces astaci Schikora 1906, introduced by alien crayfish species of North American origin. Today, the European native crayfish population trends are in decline nearing extinction in several cases (Souty-Grosset et al., 2006; Jussila et al., 2014). The introduction of different A. astaci strains in Europe and the repeated introductions of their North American host species are a classic example of a man-made ecological disaster (Jussila et al.), stemming from the naive belief that the manipulation of an ecosystem would be straightforward. The alien crayfish species, which were supposed to replace the eradicated native stocks, not only transfer the deadly disease but in many parts of Europe also outcompete their native crayfish counterparts, because they are more aggressive giving them additional advantage regarding habitat competition in addition to higher fecundity (Alonso and Martínez, 2006). Introductions of new alien crayfish stocks and thus new A. astaci strains will inevitably lead to the total eradication of the remaining native European crayfish stocks. In this Research Topic we collected scientific work on crayfish conservation from multiple scales, ranging from molecular to species and ecosystem levels, to address the consequences of invasive crayfish and host-parasite interactions on European freshwater biodiversity and ecosystem functioning, aiding conservation and management of European freshwater crayfish to prevent them from extinction.
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• Invasive non-native species represent a leading threat to global freshwater biodiversity and non-native crayfish species frequently cause extensive ecological damage. However, the extent to which their impact: (1) depends on invader identity and (2) differs from the natural state with native crayfish remains unclear. Comparison of the functional responses of invasive and native species represents a promising approach in this regard. • Here, we explored whether four invasive crayfish species (calico crayfish Faxonius immunis, spiny-cheek crayfish Faxonius limosus, signal crayfish Pacifastacus leniusculus, and marbled crayfish Procambarus virginalis) in European freshwaters and the most widespread native species (noble crayfish Astacus astacus) overlap in function in their potential effects on key resources of benthic food webs. First, the impact on gammarids and zebra mussels was assessed by means of comparative functional response analysis using the functional response ratio as impact metric; second, the consumption of macrophytes (Chara sp.) and detritus (leaf litter) was quantified and compared using feeding experiments. • Both invader- and resource-specific effects were observed. Invasive calico crayfish and signal crayfish exhibited the strongest per capita effects on gammarids and zebra mussels, respectively, with functional response ratios being 2-fold higher than those of native noble crayfish. Marbled crayfish showed an intermediate effect on both prey species, whereas spiny-cheek crayfish had lower impacts than noble crayfish. In the feeding experiment, calico crayfish consumed the highest amount of detritus, while the consumption of macrophytes did not differ among the five crayfish species. • Our work demonstrates as-yet unrecognised differences in functional responses among the four North American crayfish invaders and the European noble crayfish. The lack of congruence across the observed impacts suggests a mostly species-specific pattern and stresses the importance of species and resource identity when considering the ecological impact of crayfish. An initial assessment of invader-specific potential impacts positions calico crayfish and signal crayfish among the most impactful invaders.
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Native European crayfish conservation was triggered by invasion of crayfish plague disease agent, Aphanomyces astaci, starting 1860s in Northern Italy. Resulting crayfish plague epidemics quickly spread over Continental Europe, then to Finland, Sweden and finally, after running amok around Europe, A. astaci was discovered also in Iberian Peninsula, Norway, Ireland, and United Kingdom in 1970s and 1980s. By that time significant proportion of native crayfish stocks had been lost, and while crayfish plague epidemics were still recorded, also industrialization and waterways construction were causing damage to remaining native crayfish stocks. While alien crayfish introductions, at least Faxonius limosus, already gave rise to first wave of crayfish plague epidemics in late 19th century, later in 1960s it was decided that introductions of alien Pacifastacus leniusculus should be initiated to replace native European crayfish populations. Decisions were based on presumed advantages for fishery, suitable habitat requirements and supposed immunity against A. astaci. Furthermore, conservation of native European crayfish species was sidelined and focus shifted toward alien crayfish stocking routine and consumption. Alien crayfish species introductions resulted in repeated waves of crayfish plague epidemics among remaining native crayfish stocks. It was soon discovered that alien crayfish of North American origin were, as suspected, permanent reservoirs for A. astaci, that some of those alien species were losing their resistance against selected strains of A. astaci and struggled in European aquatic ecosystems. In this article, we introduce numerous motives behind grand mistake of introducing alien crayfish species to Europe and then promoting their stocks instead of focusing on conservation of native crayfish species. We outline how false economical, biological and ecologic assumptions were used to justify a hasty introduction of alien crayfish, which has further devastated native crayfish and also permanently changed European aquatic ecosystems, both with disastrous consequences. Lesson to be learnt is that science-based warnings about alien species damage to native ecosystems and native crayfish must be taken with utmost caution. Protection of native European crayfish should be core issue, not commercial activities. Finally, we summarize main threats and actions needed to protect remaining native freshwater crayfish fauna in Europe.
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Citation: Sanna, D.; Azzena, I.; Scarpa, F.; Cossu, P.; Pira, A.; Gagliardi, F.; Casu, M. First Record of the Alien Species Procambarus virginalis Lyko, 2017 in Fresh Waters of Sardinia and Insight into Its Genetic Variability. Life 2021, 11, 606. Abstract: In the fresh waters of Sardinia (Italy), the non-indigenous crayfish species Procambarus clarkii has been reported from 2005, but, starting from 2019, there have been several reports of a new non-indigenous crayfish in southern and central areas of this Mediterranean island, and its morphology suggests that this species may be the marbled crayfish Procambarus virginalis. Forty-seven individuals of this putative species were analyzed, using the mitochondrial gene Cytochrome c Oxidase subunit I as molecular marker to identify this crayfish and investigate the level of genetic variability within the recently established population. Phylogenetic and phylogeographic analyses were carried out on a dataset including sequences from the Sardinian individuals and from all congenerics available in GenBank. Results showed that the new Sardinian crayfish belong to the species P. virginalis. All the sequences belonging to P. virginalis from European countries are identical, with only few exceptions found among Sardinian individuals. In conclusion, this paper highlights the occurrence of a new further alien species in the Sardinian fresh waters, which are already characterized by the high presence of non-indigenous species.
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An increasing number of non-indigenous crayfish species (NICS) of apparently pet trade origin have become established particularly in Europe. Especially alarming are recent confirmation of two distantly separated marbled crayfish Procambarus fallax f. virginalis populations in Ukraine and indications of more North American cambarids present in the local pet market. The present study aimed to investigate crayfish species availability within the Ukrainian pet trade together with the climate match and risk they represent to the freshwater ecosystems generally and indigenous crayfish species in particular. Altogether, 15 NICS belonging to all three crayfish families were detected. Considering their origin, availability, probability of establishment, invasiveness and further aspects, marbled crayfish and red swamp crayfish Procambarus clarkii appear to be potentially the most troubling. Available information obtained from the pet trade in ornamental crayfish as a whole demonstrates that the broad availability of NICS most probably overlaps the vast majority of European indigenous crayfish species distribution, including the endemic thick-clawed crayfish Astacus pachypus, which occupies only a limited area that is situated critically close to established marbled crayfish populations. Negative effects of NICS on freshwater ecosystems as a whole can be also expected.
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After interest in keeping crayfish (Crustacea, Decapoda, Astacida) in home aquaria peaked in the mid-2000s, the aquarium trade has become a novel introduction pathway for non-native crayfish species in Germany. Here, we provide an update on the ornamental crayfish trade approximately one decade after the ‘crayfish hype’ to explore the long-term implications in terms of bio-invasion risk. Specifically, species’ availability in e-commerce and potential invasiveness were assessed and compared to previous studies. Morphological and ecological traits of the offered species were compiled and related to their long-term availability (covering 2005–2015). In July 2015, a total of 31 online shops offered 28 crayfish species, which represents a decline of 24 % in species diversity compared to the late 2000s. The estimated rate of import of new species has considerably flattened and approaches pre-hype values (<1 species year⁻¹). However, the risk associated with the offered species, as assessed by a risk screening tool, has not decreased compared to the late 2000s. Long-term availability in the trade was primarily determined by bright coloration, the ability to reproduce under warm aquarium conditions, and a preference for lentic habitats. Species featuring such traits are likely to persist in the aquarium trade and include four high-risk species, most notably invasive and crayfish plague-carrying red swamp crayfish (Procambarus clarkii) and Marmorkrebs (Procambarus fallax f. virginalis). Persistent propagule pressure from aquaria has substantially contributed to the establishment of both species in Germany, stressing the need for more effective pathway management.
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The damselfly Coenagrion ornatum represents a threatened species of lowland headwater streams. Although the species is threatened in Western and Central Europe, it is known at a system of post-mining drainage ditches in the Radovesicka spoil heap (northwestern Bohemia, Czech Republic). This study aimed to estimate its population size in this post-mining stream system, and to explore habitat preferences of both its larvae and adults with respect to various environmental factors. The adults were captured-recaptured along 5.2 km of the ditches in June 2012; larvae were sampled in 64 study sites (i.e., 27-meter-long sections of the same ditches) in April 2012. The adult population size was estimated via log-linear models with the robust design on 4544 individuals (1560 ± 391 females and 2983 ± 298 males). Larvae were present in a third of the sections. GLMs revealed that both larvae and adults required emergent vegetation with a high proportion of Eleocharis spp. plants. The adults preferred the slow-flowing and shallow streams with 2-meter-high banksides covered by intermediately tall vegetation (~40 cm), whereas the larval abundance was supported by a high in-stream vegetation heterogeneity and a patchy cover of rocks on the streambeds. These results indicate that the post-mining streams could represent a valuable secondary habitat for the complete life cycle of this relatively large population of the endangered headwater specialist. Therefore, we recommend consideration of the conservation potential of such ditches during post-mining sites restoration and their subsequent management.
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In recent years, the keeping of ornamental freshwater animals and plants in garden ponds has been growing in popularity. Water hyacinth (Eichhornia crassipes) is one of the preferred macrophytes seasonally imported mainly from South-eastern Asia throughout the world. This constitutes a secondary introduction inasmuch as the species is native to South America. Although many assemblages of aquatic invertebrates have been described as associated with this plant in the wild, there has been no research focused on their potential introduction via the international plant trade. We examined 216 specimens of water hyacinths imported for ornamental purposes from Indonesia into the Czech Republic. Numerous meio- and macroinvertebrates belonging to at least 39 species were captured. On the total number of individuals, the highest prevalence was of Tubulinea and Rotifera. Most of these were still alive and vital, including a caterpillar of the Indo–Australian invasive moth Spodoptera litura. Water hyacinths are usually placed into outdoor ponds immediately after import, which facilitates the release of non-target alien species. The present paper aims to draw attention to “hitchhikers” associated with the ornamental trade.
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The marbled crayfish or Marmorkrebs, Procambarus fallax (Hagen, 1870) f. virginalis, a parthenogenetic freshwater crayfish belonging to the North American cambarids, was recorded in Hungary for the first time. Several specimens of this potentially invasive crayfish were caught at different locations in the thermal Lake Hévíz and its outflows in the western part of the country. Captured individuals covered a wide size range (5.5 to 50.5 mm carapace length) and one was carrying eggs and recently hatched offspring, which suggests that this organism has established a stable and self-sustaining population in the warm habitats of Lake Hévíz area. This finding is of great significance because these habitats belong to the catchment of the Danube River including Lake Balaton, and thus, a significant further spread of the marbled crayfish is likely to happen in Central Europe. Furthermore, the expansion of this crayfish already reached the Kis-Balaton, one of the landscape protection areas of the Balaton Uplands National Park, what could have currently yet unpredictable consequences for this unique wetland biotope.
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In this paper the first records of Marmorkrebs [Procambarus fallax (Hagen, 1870) f. virginalis] (Crustacea, Decapoda, Cambaridae) in Ukraine are given.
The ecological value and conservation potential of post-mining areas have been increasingly recognized by scientists and conservationists during recent decades. Especially valuable are sites left to spontaneous succession, which constitute habitats with high species diversity, or habitats that serve as refuges for threatened species. In contrast to several other taxa, there is a lack of such evidence for amphibians, despite the assumption that primary succession leads to a more suitable environment for amphibians than does technical reclamation. Therefore, we compared the effects of technical reclamation and spontaneous succession on amphibian presence, species richness, and abundance of the model species Rana dalmatina in technically reclaimed and unreclaimed sections of spoil banks in the Czech Republic's North Bohemian brown coal basin. We found that most recorded amphibian species, and R. dalmatina in particular, occurred predominantly within successional spoil bank sections. Apart from reclamation status, amphibians preferred partially vegetated ponds (5–75% vegetation cover) having gently sloping shores (<30°) and lower water conductivity. Mean species richness per pond (1.95 vs. 1.20), the proportion of ponds occupied by amphibians (88.5% vs. 69.4%), and the mean numbers of R. dalmatina clutches per pond (9.05 vs. 1.65) were significantly higher at unreclaimed sites compared to technically reclaimed sites. This study confirms the conservation value of post-mining sites for amphibians and evidences that sites left to spontaneous succession provide more suitable habitats for amphibians compared to technically reclaimed sites. Key habitat characteristics driving amphibian assemblages within post-mining sites are identified and guidelines for effective protection of amphibians in post-mining areas are proposed.