Habitat Establishment, Captive Breeding and Conservation Translocation to Save Threatened Populations of the Vulnerable European Mudminnow Umbra Krameri

Habitat establishment, captive breeding and conservation translocation to save threatened populations of the Vulnerable European mudminnow Umbra krameri

S ÁNDOR T ATÁR,BÁLINT B AJOMI,ANDRÁS S PECZIÁR,BALÁZS T ÓTH M AGDOLNA M ÜLLERNÉ T RENOVSZKI,BÉLA U RBÁNYI,BÉLA C SÁNYI J ÓZSEF S ZEKERES and T AMÁS M ÜLLER

Abstract In Europe % of freshwater fish are threatened. restoration and potential areas for creation of surrogate ha- However, conservation activity is less widespread for fish bitats, and enhancing induced propagation methodology. compared to other vertebrate groups. The Vulnerable Keywords Carassius carassius, habitat loss, Hungary, European mudminnow Umbra krameri is a marshland Misgurnus fossilis, reintroduction, surrogate habitats, threa- fish endemic to the Carpathian Basin. Its range and popula- tened populations, Umbra krameri tion have declined significantly since the s. The main threats to the species are habitat loss and the invasive To view supplementary material for this article, please visit Chinese sleeper Perccottus glenii. During – a spe- https://doi.org/./S cies conservation programme was established to rescue broodstocks from threatened populations, breed them under controlled conditions, translocate both rescued fish Introduction and their laboratory-reared offspring to surrogate habitats, n their overall assessment of the European Red List of fresh- and finally reintroduce offspring to their original habitats. Iwaterfish,Freyhof&Brooks()concludedthatnearly Broodstocks from three threatened habitats were bred in %ofnativespeciesinEuropeareendemicand%are the laboratory and produced offspring appropriate for threatened, which is high compared to other taxonomic stocking. Six artificial ponds were created in the pilot groups (e.g. %ofamphibiansand% of mammals are study area according to the environmental needs of the spe- threatened; Freyhof & Brooks, ).Thereisevidencethat cies, four of which proved to be suitable surrogate habitats  fish species have already gone extinct in Europe, with five in which translocated fish survived and reproduced success- others facing impending extinction. The greatest threats to na- fully. Populations in the original habitats were supplemen- tive European fish are pollution, habitat destruction and inva- ted with fish from laboratory breeding and from the natural sive alien species (Dudgeon et al., ). The effects of climate recruitment of surrogate habitats, with special care of the change (e.g. drought) have been shown to drive the deterior- corresponding broodstocks. Future challenges include im- ation of freshwater ecosystems, and fish living in shallow proving our knowledge about the ecological processes in waters of wetlands are in particular danger (Heino et al., which the European mudminnow participates, identifying ; Pratchett et al., ; Jeppesen et al., ; Ellis et al., the most threatened populations, habitats suitable for ). Nonetheless, fish are underrepresented in the conservation literature, with a clear bias in favour of birds and mammals (Seddon et al., ;Bajomietal.,). SÁNDOR TATÁR*† Tavirózsa Association, Veresegyház, Hungary Fen habitats are particularly exposed to environmental BÁLINT BAJOMI† (Corresponding author) Faculty of Sciences, Centre for regulation by people, and in Europe their area has decreased Environmental Sciences, Eötvös Loránd University, Pázmány Péter sétány  1/A, H-1117 Budapest, Hungary. E-mail [email protected] by %to, km since the s (Rosenthal et al., ;   ANDRÁS SPECZIÁR Balaton Limnological Institute, Hungarian Academy of Joosten & Couwenberg, ; Brinson & Malvárez, ). In Sciences Centre for Ecological Research, Tihany, Hungary Hungary % of fens have been destroyed by regulation of BALÁZS TÓTH Danube-Ipoly National Park Directorate, Budapest, Hungary watercourses, draining and ploughing (Tatár, ). Small,

MAGDOLNA MÜLLERNÉ TRENOVSZKI,BÉLA URBÁNYI and TAMÁS MÜLLER† isolated remnant marshland populations are particularly Department of Aquaculture, Szent István University, Gödöllő, Hungary sensitive to environmental alterations, which often lead to BÉLA CSÁNYI and JÓZSEF SZEKERES Danube Research Institute, Hungarian a decrease in genetic diversity and an increase in mortality, Academy of Sciences Centre for Ecological Research, Budapest, Hungary as in the case of the European mudminnow Umbra krameri. *Also at: Department of Aquaculture, Szent István University, Gödöllő, Freyhof & Brooks () urged the establishment of Hungary †These authors have contributed equally to the results presented in this paper. Freshwater Key Biodiversity Areas and the development of Received  February . Revision requested  March . species protection plans for European freshwater fish spe- Accepted  May . First published online  November . cies. They also suggested establishing habitat monitoring

Oryx, 2017, 51(4), 718–729 © 2016 Fauna & Flora International doi:10.1017/S0030605316000533 Downloaded from https://www.cambridge.org/core. IP address: 170.106.33.19, on 01 Oct 2021 at 02:30:46, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0030605316000533 Saving the European mudminnow 719

and ex situ programmes, restrictions on settling of non-na- conservation of declining populations of the European mud- tive fish species, and revision of the relevant legislation. One minnow across its diminishing and fragmented range. of the most important roles of a species protection plan is to Our aim was to develop and test a comprehensive meth- identify and rectify factors that caused the initial extinction odology to promote the rescue and strengthening of popu- or decline (Fischer & Lindenmayer, ; IUCN/SSC, ; lations of European mudminnow, for which habitat loss is Cochran-Biederman et al., ). Accordingly, we summar- one of the most important threats (Sallai, ; Kuehne & ize the actions and results of our pilot conservation pro- Olden, ). Considering the decreased population size, gramme for the European mudminnow (Tatár et al., ). an important challenge is to preserve the species’ remnant The European mudminnow is small-bodied (– cm), genetic diversity, distributed across small and isolated habi- has a short lifespan ( years), is the only native representa- tat patches (Takács et al., ). Accordingly, we implemen- tive of the Umbridae family in Europe and is a relic and en- ted a pilot experiment that included: demic fish species of the Danube catchment area (Gaudant, (1) determining habitat characteristics required by the species, ). It occurs sporadically along the Danube River be- for consideration in the planning of surrogate habitats, tween Vienna and the Danube Delta. Some populations (2) creating new fen and marsh surrogate habitats to supple- live in the lower stretches of the River Dniester but the spe- ment lost native areas and harbour rescued populations cies’ main range is in the Carpathian Basin (Kottelat & (creating new self-sustaining populations in Szada Pilot Freyhof, ; Kuehne & Olden, ). The European mud- Area), minnow lives in marshes, fens, vegetated backwaters and (3) rescuing broodstocks from habitats known to be da- channels with clean water (Pekárik et al., ). The main maged or exposed to contamination, threats to the species are habitat loss as a result of dredging (4) checking the quality of the created habitats before of channels, the destruction of river and stream floodplains, stocking them with European mudminnow, the loss of fens and marshes (Wanzenböck, ; Kuehne & (5) propagating and rearing European mudminnow Olden, ) and the spread of the invasive Chinese sleeper under controlled laboratory conditions for reintroduc- Perccottus glenii. This voracious competitor and predator of tion and for the conservation of genetic diversity, and the European mudminnow is expanding its range in Eurasia (6) monitoring the quality of the created habitats after and has colonized the catchment area of the Danube and stocking. Dniester rivers (Reshetnikov & Ficetola, ; Reshetnikov, ). It is estimated that populations of European mud- Behavioural degradation could be minimized by introdu- minnow have declined by . % (Freyhof, ). The spe- cing rescued broodstock to the new surrogate habitats cies is categorized as Vulnerable on the IUCN Red List on quickly rather than holding them in the laboratory the basis of its restricted and fragmented habitat (Freyhof, (Hammer et al., ; Ellis et al., ). The key behavioural ) and it also features on the Red Lists of seven aspects for the survival of stocked fish are the ability to eat European countries (Müller et al., ). and avoid being eaten. Fish are often necessarily reared on Several successful attempts have been made to conserve artificial diets because of the cost, limited supply and poten- populations of the species, primarily by means of habitat tial disease risk of wild foods, but this potentially reduces restoration and the reintroduction of rescued stocks their foraging efficiency in the wild (Hammer et al., ). (Wanzenböck, ;Keckeis&Sehr,); for example, in We hypothesized that carefully designed artificial habitats the Slovenian Beloviči backwater populations of European wouldbeappropriatesurrogatehabitatsfortheEuropean mudminnow, as well as weatherfish Misgurnus fossilis and mudminnow to establish permanent self-sustaining stocks, crucian carp Carassius carassius, increased significantly after and that either breeding in the laboratory or reproduction of restoration of their habitat (Povž, ). European mud- broodstocks in the artificial habitats would yield enough off- minnow fry were also introduced successfully to waters in spring to reinforce threatened populations or replace extinct Austria (Benesch, ) and close to the River Morva in ones. To support the assessment of the ecological status of Slovakia, which is part of the species’ native range the created habitats, we included in the study two other threa- (Valachovič &Kováč, ). However, translocations from tened components of marshland fish assemblages, the Beloviči oxbow to a gravel pit (Povž, a) were unsuccessful. weatherfish Misgurnus fossilis and the crucian carp Carassius After the original population had gone extinct, the NGO carassius. BioticaEcologicalSocietyrestockedfry into small waterbodies in the Lower Dniester area (Aps et al., ). A successful re- ő introduction was carried out in Fert -Hanság National Park Study area (north-west Hungary) by translocating wild individuals from other areas (Ambrus & Sallai, ; A. Ambrus, pers. For habitat construction experiments we selected nine nat- comm). Although some of these trials proved to be successful ural lowland sites within Hungary’s Carpathian Basin at a local scale, there is no detailed action plan for the (Fig. ; Table ) that had existing or previously known

FIG. 1 (a) Sites of surveyed European mudminnow Umbra krameri populations and habitats (Table  and Table S) in Hungary, with numbers of caught individuals and stocked captive- bred individuals. White circles represent extinct populations. The inset shows the numbers of fish caught for propagation and stocked offspring in Illés Ponds I, III, IV, VI of Szada Pilot Area (Table ). (b) Location of natural and artificial ponds (Pócos and Illés Ponds, respectively) in Szada Pilot Area. *Parent fish were captured in Pócos Pond B (site ;  individuals) and Illés Pond IV ( individuals). The latter habitat is connected to Pócos Pond B.

populations of European mudminnow (Sallai, ). The Gőgő-Szenke Stream, which was threatened by anthropo- chosen habitats represented the environmental range occu- genic pollution, and a fen in the construction area of the pied by the species, and included fens, ponds, slow-flowing South M highway bridge (Ráckeve Danube Branch and vegetated streams, and canals. Two more sites were Natura  Site, Czuczor Island), which was about to be added subsequently because of threats to the species: filled up as part of the expansion of the highway.

Oryx TABLE 1 Fish assemblages and macrophyte coverage recorded during surveys at sites of existing or previously known populations of European mudminnow Umbra krameri in Hungary’s

07 14,718 51(4), 2017, , Carpathian Basin (Fig. ), with site number and survey date in parentheses. https://www.cambridge.org/core Still waters Watercourses

Ócsa Landscape Fen at South Császárvíz Császárvíz

– Protection Pond Farmos Lake Báb Pócos Pond Pócos Pond M0 Bridge Canal, upper Canal, lower Felső-Tápió Csaronda Gőgő-Szenke 729 Area (Site 3; (Site 5; (Site 7; A (Site 8; B (Site 9; (Site 11; 7 & section (Site 1; section (Site 2; Stream (Site 4; River (Site 6; Stream (Site 10; © . https://doi.org/10.1017/S0030605316000533 19 June 2008) 16 Nov. 2012) 2 Apr. 2010) 19 June 2008) 29 June 2009) 16 Sep. 2010) 26 June 2014) 16 Nov. 2012) 16 Nov. 2012) 2 Apr. 2010) 2 Apr. 2010) 06Fua&FoaItrainldoi:10.1017/S0030605316000533 International Flora & Fauna 2016 Abramis brama 1 Ameiurus melas2 2

. IPaddress: Blicca bjoerkna 5 Carassius 66 4 carassius1 Carassius carassius 3 170.106.33.19 × Carassius gibelio Carassius gibelio2 14 1 13 5 3 Cobitis 88 32 elongatoides , on Gobio gobio 7 01 Oct2021 at02:30:46 Lepomis gibbosus2 12 Misgurnus fossilis1 55 1 4316 Perca fluviatilis 10 Perccottus glenii2 12 8 Proterorhinus 20 1 marmoratus

, subjectto theCambridgeCore termsofuse,available at Pseudorasbora 38 17 1 parva2 Rhodeus sericeus 38 1 Rutilus rutilus 12 Squalius cephalus 28 Tinca tinca 9 Umbra krameri1 12 27 22 21 2 19 Total no. of 12 138 12 27 23 30 39 227 55 9 34 individuals Total no. of species 1 4 1 1 2 2 2 11 11 2 5 % abundance of 0.0 10.1 100.0 0.0 0.0 0.0 100.0 13.7 18.2 88.9 8.8 721 mudminnow European the Saving invasive species % invasive species 0.0 25.0 100.0 0.0 0.0 0.0 100.0 27.3 36.4 50.0 20.0 % macrophyte 60 100 100 100 8 100 5 000100 coverage (charac- (Lemnetum (Ceratophylle- (Lemnetum (Lemnetum (Lemnetum (Ceratophyll- (Lemnetum (Lemnetum teristic species/ minoris) tum minoris, minoris) minoris, etum minoris) minoris, associations)* demersi) Hydrocharis Lemna demersi, Lemna trisulca) morsus- trisulca) Lemnetum ranae) minoris, Elodea canadensis)  Protected/rare marshland fish species  Invasive species 722 S. Tatár et al.

The  ha Szada Pilot Area (Fig. ) was chosen for the Creation and monitoring of new surrogate habitats creation of new and revitalized fen and marsh habitats (Illés Ponds I–VI) based on the following criteria. Firstly, Based on a literature review and field surveys of the natural it is a drained wetland area with a few small and isolated na- habitats of the European mudminnow (Supplementary –  tive populations of European mudminnow (in Pócos Ponds Tables S S ) we designed Illés Ponds in the Szada Pilot  – A and B, sampling sites  and ; Fig. ). Secondly, the Area (Fig. ). During we established six ground- – –  groundwater level does not drop below . m even during water-fed ponds (i.e. Illés Ponds I VI; each with m –  –    droughts, thus facilitating the creation and maintenance of volume, m surface area, . and . m mean and fen and marsh habitats. Thirdly, this area is adjacent to the maximum depths, respectively) by dredging degraded ter- EU’s Natura  network of protected areas (Natura , restrial habitats dominated by the invasive plants Solidago ), and thus there should be no further risk of significant spp. Rather than creating one large lake we designed several human impact. Finally, it is close to the laboratory of Szent smaller ponds with a high shoreline-to-surface ratio, which István University (Gödöllő) where breeding took place. is important for the development of diverse and abundant macrophyte and macroinvertebrate assemblages (Gee et al., ; Cremona et al., ). To increase environmental diversity we created irregular shorelines and bottoms. Methods The ponds were created such that –% of their surface area was in the shade of the surrounding trees and shrubs Assessment of habitats and new surrogate habitats (Illés to prevent excessive warming and algal blooms, which are Ponds) not tolerated by marshland fish. Shading was increased The ecological requirements of the European mudminnow by introducing macrophytes to the ponds. Aquatic were determined based on a comprehensive literature re- vegetation also decreases the nitrate, nitrite and ammonium view and field research in native habitats. In total,  natural content of water, which also inhibits the growth of algae. We habitats of the species in the three main regions of Hungary planted the ponds with indigenous aquatic macrophytes were selected at random for surveys, from a habitat list of Ceratophyllum demersum and Lemna minor from a nearby National Parks (Fig. ). water body; the common reed Phragmites australis was Water quality analysis and botanical investigations were present in the Szada Pilot Area and colonized the littoral conducted between February and September, and hydrobio- of Illés Ponds spontaneously. As we wished to preserve logical surveys were carried out in May and June during the genetic identity of each of the rescued broodstocks, –. Dissolved oxygen, pH and conductivity were Illés Ponds were constructed in such a way as to ensure recorded using portable water quality meters (Voltcraft the isolation from each other and from the surrounding DO-,PH- ATC and LWT-, Conrad Electronic, aquatic habitats (except Illés Pond IV, which was created Hirschau, Germany) and other chemical properties of the as a refuge extension of the over-vegetated and shallow nat- water (phosphate, ammonium, nitrite and nitrate ion con- ural Pócos Pond B). Isolation of experimental ponds from centrations) were measured using a VISOCOLOR® ECO surrounding watercourses also prevents immigration of in- test kit (Macherey-Nagel, Dűren, Germany). Abundance vasive fish. and number of taxa of macroinvertebrates (i.e. food base of After their construction Illés Ponds were monitored fish) were assessed using a kick-and-sweep sampling method regularly for water chemistry, macrophytes and macroinver- –  – (mesh size  μm, frame size  ×  cm). Macroinvertebrate tebrates (Supplementary Tables S S ). Following - samples were preserved in %formaldehydeor%ethanol month colonization periods, ponds that were considered prior to identification in a laboratory. Botanical investigations to be appropriate were stocked with European mudminnow. included assessment of the macrophyte coverage and identi- After stocking, monitoring of ponds was supplemented with fication of the dominant taxa at each site. Algal or bacterial seasonal sampling of fish, applying the same method out- blooms observed were recorded. lined above for small, still water bodies. Fish assemblages were sampled during – using  electric fishing (IG , Hans Grassl, Schönau am Königssee, Saving threatened stocks, captive breeding and releases Germany) along randomly selected  m long transects. Samples were taken by wading upstream in streams and During our field trips and by maintaining contact with other canals, and covering the whole volume of small, still waters conservationists countrywide we actively searched for situa-  (i.e. ponds and fens; ,  m ). Captured fish were identi- tions where populations of European mudminnow were fied and measured immediately, counted and released. The threatened by human activities. In such cases, fish were cap- same procedure and methodology used for natural habitats tured using electric fishing, placed in a plastic barrel filled was also used to monitor the pre- and post-stocking water with oxygenated water and transported to a laboratory at quality of Illés Ponds. the Szent István University.

In the laboratory broodstocks were held in separate aqua- abundance of Prussian carp Carassius gibelio (i.e. Gőgő- ria to preserve their genetic identity for a -week acclima- Szenke Stream). In contrast, five former habitats of the tization period prior to attempted breeding using two European mudminnow where the species is no longer procedures. The first group was placed in breeding tanks present are now populated by invasive fish, including the with °C water temperature and a photoperiod similar to black bullhead Ameiurus melas, Prussian carp, that of the spawning season, in April; the bottom of the pumpkinseed Lepomis gibbosus, Chinese sleeper Perccottus tanks was covered by a green plastic net to prevent cannibal- glenii and stone moroko Pseudorasbora parva.Wefound ism of eggs and larvae. (Green netting was used for camou- only one exception; the Felső-Tápió stream harboured a flage amidst the aquatic vegetation.) The second group small number of European mudminnow as well as an received carp pituitary extract treatment to induce propaga- abundance of invasive species. The weatherfish was the tion. Larvae were then reared in aquaria and in an artificial most common native species captured over all sites.   m pond lined with foil. For more details of propagation and rearing see Müller et al. () and Demény et al. (). Captured fish, and their laboratory-reared offspring, ori- Creation and pre-stocking monitoring of surrogate habitats ginating from different populations were stocked in separate Pre-stocking water quality, macrophyte and macroinverte- – Illés Ponds. Offspring from captive breeding and from nat- brate (i.e. food base) monitoring (Supplementary Tables S  ’ ural spawning in Illés Ponds were used to supplement popu- S ) revealed that Illés Ponds I, III, IV and VI met the species lations in native habitats where the parents originated. conservation criteria following a short primary succession Laboratory-reared weatherfish and crucian carp were also period, and thus they were assigned for stocking with – stocked in Illés Ponds. European mudminnow during .InIllésPondII there were regular blooms of cyanobacteria, and proliferation of sulphur bacteria was also a common phenomenon. In  Results we observed high nitrite concentrations (Supplementary Table S) and blooms of Cladophora sp. in Illés Pond V. Consequently Illés Ponds II and V were excluded from Environmental characteristics of European mudminnow the conservation programme. habitats According to published data and the results of our surveys the physical and chemical water quality of natural habitats of the European mudminnow varies Captive breeding and saving threatened stocks In  a widely (Supplementary Table S). The species’ habitats total of  adult European mudminnow were rescued and usually have a low dissolved oxygen concentration; for transported to the laboratory from three threatened sites: example, we measured oxygen levels of . and . the Pócos Pond B (site ), which nearly dried up in that − mg l in Pócos Pond A and at Ócsa Landscape Protection year; the heavily polluted Gőgő-Szenke Stream (site ); Area, respectively. Our field surveys revealed that and the fen in the construction area of the South M macrophyte coverage in these habitats can vary widely (– Bridge (site ; Table ). Induced propagation with carp %), with a mean value of %(Table ). The European pituitary treatment was attempted three times but no mudminnow generally occurs in shallow (.–. m), larvae were hatched. In contrast, fish that did not receive shaded and often low-volume waterbodies. Data on the any treatment formed bonded pairs and laid eggs on the abundance of macroinvertebrates in samples from various bottom of the breeding tank. From this  juveniles were native habitats are summarized in Supplementary Table S. introduced to the Szada Pilot Area and the parents’ original habitat (Table ). Laboratory-reared juveniles reached a mean standard body length of . cm in aquaria by early Fish assemblages of European mudminnow habitats Of the August; they reached a mean body length of . cm and nine investigated sites where the presence of the European sexual maturity (females visibly carried developing eggs) in mudminnow had been confirmed previously, we found the an artificial pond by mid September. species only at four (Table ). We also found the species at the two additional sites threatened by anthropogenic impacts (i.e. the fen at the South M Bridge and Gőgő- Stocking surrogate habitats with marshland fish Szenke Stream). In general, fish assemblages of still-water Environmental assessment of Illés Pond I  months after habitats comprised fewer species (–) than those of its creation indicated favourable conditions for marshland streams and canals (–; Table ). There was a negative fish (Tables S &S). However, we had not yet rescued relationship between the occurrence of the European any European mudminnow at that time and therefore we mudminnow and the presence of invasive species. We stocked  one-summer-old juveniles of weatherfish and found the European mudminnow in abundance only at crucian carp in the pond in autumn .Testfishingin five sites that lacked invasive species or had a low  revealed that these fish had survived in the pond

TABLE 2 Outcome for European mudminnow saved from three sites (Fig. ), bred in the laboratory and released at three artificial ponds, with capture site, number of individuals captured, mortality during the acclimatization period, number of individuals bred in the laboratory, post-breeding mortality, number of sexually mature individuals released after laboratory breeding, and release date and location. More than half of mortalities were attributable to poor condition, age or disease.

No. of individuals No. of deaths No. of individuals No. of captured Date of during bred in deaths post No. of individuals Release Release Capture site (females, males) capture acclimatization laboratory breeding released date site Gőgő- 15 (8,7) 2 Apr. 2 13 0 13 6 Apr. Illés Szenke 2010 2010 Pond I Stream Pócos 6 (2,4) 6 Apr. 2 4 0 4 31 May Illés Pond B 2010 2010 Pond IV Fen at the 21 (9,12) 7 & 16 12 9 6 3 7 June Illés South M0 Sep. 2010 2011 Pond III Bridge

TABLE 3 Details of releases of European mudminnow offspring of captive bred and nursed stocks.

Released offspring No. of Age Standard Origin of fish Locality Date individuals (days) length (cm) Gőgő-Szenke Stream Gőgő-Szenke Stream 27 May 2010 100 39 1.5–2 Illés Pond I 31 May 2010 103 43 1.5–2 Illés Pond I 22 Sep. 2010 25 187 3–5 Gőgő-Szenke Stream 12 Oct. 2010 50 208 3–6 Pócos Pond B Illés Pond IV 31 May 2010 33 43 1.5–2 Illés Pond IV 29 May 2012 3711 55 2 Fen at the South Illés Pond VI 14 Oct. 2011 20 188 3–5 M0 Bridge Illés Pond III 10 Aug. 2011 41 123 2–3 Fen at the South M0 Bridge (Ráckeve Danube 10 Aug. 2011 1142 c. 131 2–3 Branch Natura 2000 Site, Czuczor Island) 28 Sep. 2011 1432 c. 180 2–3 Ráckeve Danube Branch Natura 2000 12 June 2012 121 429 5–7 Site (Csupics Island)3

 From laboratory breeding of  parent fish captured in Illés Pond IV on  March  and re-released into the same pond on  April   Natural offspring of saved adults released to Illés Pond III  Csupics Island is a nearby and similar natural habitat to the partially destructed fen at the South M Bridge (Czuczor Island).

(Table ). We subsequently stocked Illés Ponds I, III, IV and macroinvertebrate taxa, and macroinvertebrate abundance VI with European mudminnow. After propagation in the of these ponds are mainly within the range of natural laboratory we released a total of  saved adult European habitats. Test fishing showed that introduced fish survived mudminnow into Illés Ponds I, III and IV in spring  in their new habitats. Observed mean recapture rates were and summer  (Table ). Between spring  and % for European mudminnow, % for crucian carp and summer  we stocked Illés Ponds I, III, IV and VI with % for weatherfish (Table ). Natural reproduction of  laboratory-reared juveniles aged – days (Table ). European mudminnow was evident in the year following During – we stocked Illés Ponds III and VI with the first introductions (Table ). Recruitment was most  weatherfish and  crucian carp juveniles, respectively, abundant in the densely vegetated Illés Pond III. Although which had been bred under laboratory conditions. we released more adults into Illés Pond I (n = ) than into Illés Pond III (n = ), reproduction success was weaker in the former, probably because of the low macrophyte coverage. Post-stocking monitoring of surrogate habitats Results of water quality and macroinvertebrate assessments following the stocking of Illés Ponds I, III, IV and VI with European Reinforcement of natural European mudminnow mudminnow are in Supplementary Tables S and S. populations Given the success of our experiments we were Monitoring revealed that water quality, number of able to reinforce and reintroduce populations of European

TABLE 4 Results of monitoring in Illés Ponds (Fig. ), with numbers of European mudminnow, crucian carp and weatherfish, mean recapture rate (no. recaptured relative to no. stocked) and mean coverage of macrophytes. As Illés Pond IV is connected to Pócos Pond B to provide a refugee for natural marsh fish assemblages in dry periods, recapture rate is not relevant. In some cases low water temperature probably decreased the sampling efficiency.

Umbra Carassius Misgurnus Mean % macrophyte coverage krameri carassius fossilis (taxa) Illés Pond I (created July 2008; sampled 6 times during May 2010–Sep. 2012) No. of individuals stocked 150 50 50 No. of one-summer-old natural offspring 14 47 0 Mean recapture rate (%) 21 18 4 , 1(Utricularia vulgaris) Illés Pond III (created July 2009; sampled 7 times during Aug. 2011–Sep. 2012) No. of individuals stocked 48 200 No. of one-summer-old natural offspring 5501 02 Mean recapture rate (%)3 8 0 80 (Ceratophyllum demersum) Illés Pond IV (created July 2009; sampled 5 times during May 2010–Sep. 2012) No. of individuals stocked 407 No. of one-summer-old natural offspring 54 104 Mean recapture rate (%) 18 89 (Chara sp.) Illés Pond VI (created Sep. 2010; sampled twice during June–Sep. 2012) No. of individuals stocked 20 108 20 No. of one-summer-old natural offspring 0 0 0 Mean recapture rate (%)3 20 78 35 80 (Ceratophyllum demersum) Mean (range) of recapture rates for all 17 (8–21) 48 (18–78) 13 (0–35) ponds (%)

  captured larvae of natural progeny were used to reinforce the threatened parental population (Table ).  Weatherfish larvae released at small size (c.  cm) were probably still smaller than the mesh size.  On some occasions fish sampling was ineffective because of dense vegetation, and thus these results are incomplete.  Illés Pond IV is connected to native Pócos Pond B, and therefore the exact place of spawning cannot be identified.

mudminnow in the threatened habitats where parent fish had the European mudminnow, which uses its swim-bladder originated. Following an administrative measure to eliminate as an auxiliary breathing organ (Geyer & Mann, ). pollution we reintroduced  -day-old and  -day-old The ability to survive periods of low oxygen concentrations laboratory-reared individuals into Gőgő-Szenke Stream in confers a competitive advantage over other fish species in May and October , respectively (Table ). Laboratory- marsh and fen environments. Pekárik et al. () found reared -day-old offspring (n = ) of parents that that both the probability of the presence of European mud- originated from the fen at the South M Bridge were minnow and its abundance tend to increase with macro- introduced to a similar, nearby habitat, Ráckeve Danube phyte coverage. The mean value of macrophyte coverage Branch at Szigetcsép (Table ). Following successful was  and % (free-floating and submerged plants, respect- spawning of European mudminnow, offspring were partially ively) in the surveyed habitats, which differs from the assess- harvested from Illés Pond III and  individuals of c.  ment of Pekárik et al. (), who concluded that the and  days old were reintroduced to the preserved optimal macrophyte coverage is c.  and %. remnant of their native habitat, the fen at the South M Bridge, in August and September , respectively. The threatened population of Pócos Pond B was reinforced Current status of native European mudminnow indirectly by ensuring its connectivity with Illés Pond IV. populations

More than half (five of the nine investigated) of the previous- Discussion ly known populations were not found in our surveys, indicat- ing the species may be at considerable risk of extinction. Environmental characteristics of European mudminnow Other studies have reached similar conclusions (Sallai,   habitats ; Kuehne & Olden, ) and identified two main sources of threats. Most of the species’ habitat was lost during We recorded extremely low dissolved oxygen concentra- the extensive regulation of rivers and wetlands in the th tions in several habitats. This circumstance is tolerated by and th centuries (Takács et al., ). However, habitat

loss is ongoing, as illustrated by the case of the fen at the spider Dolomedes fimbriatus, the smooth newt Lissotriton South M Bridge, where construction work related to trans- vulgaris, the common spadefoot Pelobates fuscus, the grass port infrastructure and expansion of recreational areas are snake Natrix natrix and the European pond turtle Emys resulting in the loss of wetland habitats. orbicularis). The second evident threat is the spread of invasive fish The creation of several small habitat patches (i.e. ponds) species. Invasive species were abundant in all former habitats instead of a more extended and connected fen system has of the European mudminnow where we failed to capture any several advantages, especially in monitoring and controlling individuals. Conversely, where the European mudminnow ongoing biological and environmental processes, preventing was present invasive species were generally absent or oc- the spread of disease, and keeping invasive species out of the curred only in small numbers. The most voracious invader system. It also facilitates the preservation and maintenance in these habitats is the Chinese sleeper, which is known to of broodstocks from different populations with unique gen- have negative impacts on the European mudminnow etic pools (Marić et al., ; Takács et al., ). (Sallai, ; Reshetnikov, ). The European mudminnow Pre-stocking monitoring of created habitats is advisable, may coexist with most invasive fish species (Keresztessy, as habitat quality and prey availability influence the out- ;Povž, a) but in the long term it does not survive come of introductions of freshwater fish (Griffith et al., the settlement of the Chinese sleeper (Sallai, ; ; Ellis et al., ; Cochran-Biederman et al., ). Reshetnikov, ). Although there are signs of both compe- The unfavourable conditions in Illés Ponds II and V may tition from and predation by other invasive species (Ferincz be attributable to the soil structure and the slow flux of et al., ), the extent of these relationships has not yet been groundwater. Furthermore, shading from riparian vegeta- quantified. It is likely that, at least in some cases, invasive spe- tion could prohibit the establishment of macrophytes, cies are not the primary cause of the European mudmin- thus facilitating planktonic eutrophication. now’s population decline. The proliferation of invasive species in wetland habitats could be an indicator of environmental degradation (e.g. regulated water level, dredging of Saving fish from threatened habitats macrophytes, increased nutrient load), and thus their effect Our study targeted three threatened populations of on the European mudminnow could be considered to be in- European mudminnow: the fen at the South M Bridge con- direct. Habitats of the European mudminnow generally construction area and the Gőgő-Szenke Stream, both of which tain species-poor fish assemblages; among the most had suffered direct anthropogenic impacts, and Pócos Pond common associate species are the weatherfish and the cru- B, where habitat loss had occurred as a result of drought. We cian carp (Sallai, ; Pekárik et al., ), which are adapted believe that at least the first two might have gone extinct to survive periods of extremely low oxygen concentrations without our action. Rapid rescue and relocation of brood- and low water levels (Geyer, ;Povž, b). Habitat alter- stocks from these sites to the laboratory and to surrogate ha- ation may facilitate the establishment of other species, in- bitats created in the Szada Pilot Area ensured the survival of cluding invasive fishes and, therefore, it is important to these gene pools. conserve and restore wetland habitats in their original form. Rescuing and maintaining broodstocks from threatened Both refuge fen habitats in the Szada Pilot Area (i.e. populations is a commonly used conservation tool (Hammer Pócos Ponds A and B) contained European mudminnow et al., ;Ellisetal.,). However, captive maintenance populations and were free of invasive species, which sup- may raise problems of reduced genetic diversity given the ports the relevance of this area for a species conservation small number of parent fish (Philippart, ), and behaviour- experiment. al alterations under laboratory conditions (Philippart, ; Lynch & O’Hely, ). Nevertheless, many wild populations of European mudminnow could be small, especially during Establishment and pre-stocking monitoring of surrogate droughts. It should be emphasized that many of these isolated habitats populations may represent unique gene pools and therefore important management units (Takács et al., ). Illés Ponds, created based on our experiences studying native habitats of the European mudminnow, revealed variable environmental characteristics. Although these ponds are lo- Captive breeding cated close together in the same degraded wetland landscape, they vary in their water quality, macrophyte flora Reintroductions of threatened species depend on successful and macroinvertebrate fauna. Four of the ponds proved to captive-breeding programmes (Witzenberger & Hochkirch, be suitable for marshland fish conservation, being occupied ). The majority of freshwater fish species can be propa- by rich macroinvertebrate, amphibian and reptilian assem- gated using hormone treatments, even out of their repro- blages, including rare and protected species (e.g. the raft ductive season (Muscalu-Nagy et al., ; Zakęś et al.,

). However, all our attempts to induce controlled propa- restored habitat or in an equivalent natural or artificial sur- gation of European mudminnow failed. Despite there being rogate habitat within the range of the conservation unit no reports of successful induced propagation in this species, (Fischer & Lindenmayer, ; Olden et al., ; Ellis this outcome is still surprising, particularly as fish spawned et al., ). We deemed our efforts to save and conserve po- spontaneously in the aquaria under temperature and light pulations of European mudminnow as successful when we conditions similar to those in the spawning season. reintroduced all three threatened populations to their ori- Spontaneous spawning of European mudminnow has also ginal habitats while preserving their genetic identity. been observed by other researchers (Geyer, ;Povž, ; Bohlen, ; Kováč, ; Müller et al., ; Demény et al., ; Kucska et al., ). Consequently, la- Conclusion boratory-bred offspring may be used for species conserva- Populations of European mudminnow have declined or dis- tion purposes but their availability could be limited both appeared over most of their native range and are threatened in quantity and timing. We obtained a sufficient quantity by habitat loss and invasive species. Our pilot programme is of larvae from laboratory spawning to stock the Illés the first comprehensive species conservation programme Ponds, and the larvae were easily reared to sizes suitable that includes rescuing individuals from threatened popula- for stocking. tions, captive breeding and rearing, creation of surrogate habitats, introduction of saved and captive-bred stocks and Survival of fish in surrogate habitats reinforcement of threatened parent populations of European marshland fish. Our experience in the conservation of the The most critical measure of any surrogate habitat is European mudminnow has been positive and our results attest whether the introduced species can survive and reproduce to the wide-scale relevance of such complex approaches in there (i.e. establish a self-sustaining population; Fischer & preserving other wetland species and biodiversity. Lindenmayer, ; Cochran-Biederman et al., ). However, to facilitate larger-scale conservation actions fur- Although we only monitored a limited post-stocking period, ther research is needed to resolve the problem of reliable in- the results suggest that stocked European mudminnow, as duced propagation in this species. In addition range-wide well as weatherfish and crucian carp, survived in the four investigations are needed to improve our knowledge of the Illés Ponds that were initially determined to be suitable en- ecological processes in which the European mudminnow vironments for fish conservation. Reproductive success was participates and to identify the most threatened popula- also evident in Illés Ponds I and III. In Illés Pond IV we also tions, habitats for restoration and potential areas for cre- observed some offspring; however, as this pond is connected ation of new surrogate habitats. Conservation actions to native Pócos Pond B, the exact place of spawning could should be synchronized and a range-wide conservation not be identified. In the case of Illés Pond VI, post-stocking plan should be developed, taking into consideration the gen- monitoring did not cover a sufficiently long period to evalu- etic guide on relevant conservation and management units, ate reproductive success. However, it should be emphasized based on information about which populations may be used that in densely vegetated habitats such as Illés Ponds, fish for recruiting (i.e. serving a pool of parent fish in artificial sampling is ineffective and results are biased, as electronarco- breeding programmes) and stocking into reconstructed ha- tized individuals, especially small-bodied juveniles, remain bitats in different geographical areas, and which populations hidden among the dense macrovegetation. Furthermore, con- have the genetic integrity to be preserved without mixing sidering the small size of stocked individuals recapture rates them with other populations (Takács et al., ). probably significantly underestimated actual survival rates. Illés Ponds were designed for permanent use, with introduced broodstocks to be maintained without further disturb- Acknowledgements ance except regular monitoring. Long-term monitoring of We are grateful to Bence Balován (Tavirózsa Association), these populations will ultimately reveal whether our ex situ Zsolt Boczonádi (Szent István University), Eszter Buza conservation experiment has been successful; however, bene- (Szent István University), Ferenc Demény (Szent István fits of Illés Ponds are already apparent in that we were able to University), György Hajdú (Umbra Association), Katalin harvest offspring hatched there and reintroduce them to na- Keresztessy (Szent István University), Sándor Krenedits tive habitats. (Tavirózsa Association), David McFetridge (London School of Business and Finance), Zoltán Sallai (Hortobágy ő Reinforcement of natural populations National Park Directorate), Dávid Sz ts (Nagy Gáspár City Library), Dr Péter Takács (Balaton Limnological The ideal outcome for a conservation rescue is that threa- Institute), Dr András Takács-Sánta (Eötvös Loránd tened and rescued populations recover in their original University), László Vécsey (Municipality of Szada),

Prof. Gábor Vida (Eötvös Loránd University) and Gábor growth of the European mudminnow larvae (Umbra krameri Várbíró (Hungarian Academy of Sciences). We thank Prof. Walbaum, ) reared in controlled conditions. Bulgarian Journal  – Doug Armstrong (Massey University), Prof. Robin J. of Agricultural Science, , . DUDGEON, D., ARTHINGTON, A.H., GESSNER, M.O., KAWABATA, Z.- Pakeman (James Hutton Institute), Dr Daniel L. Jeffries I., KNOWLER, D.J., LÉVÉQUE, C. et al. () Freshwater (University of Lausanne) and Nathan Spillman (Society for biodiversity: importance, threats, status and conservation Conservation Biology) for their useful comments. challenges. Biological Reviews, , –. Support from Magyar Telekom Nyrt. helped to start the ELLIS, I.M., STOESSEL, D., HAMMER, M.P., WEDDERBURN, S.D.,  European Mudminnow Conservation Pilot Programme. SUITOR,L.&HALL,A.( ) Conservation of an inauspicious endangered freshwater fish, Murray hardyhead (Craterocephalus Our research was funded by the Hungarian Ministry of fluviatilis), during drought and competing water demands in the Environment and Water and the Hungarian Ministry of Murray-Darling Basin, Australia. Marine & Freshwater Research, Rural Development (Green Source Programme – , –. , –), the National Innovation Office, and FERINCZ, Á., STASZNY, Á., WEIPERT, A., SÜTŐ, A., SOCZÓ, G., ÁCS,A.  Research Centre of Excellence-//FEKUT. et al. ( ) Adatok a dél-balatoni berekterületek halfaunájához. Natura Somogyiensis, , –. [In Hungarian] FISCHER,J.&LINDENMAYER,D.B.() An assessment ofthe published results of animal relocations. Biological Conservation, , –. Author contributions FREYHOF,J.() Umbra krameri. The IUCN Red List of Threatened Species : e.TA. Http://dx.doi.org/./IUCN. 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() Contribution of climate change to BALÁZS TÓTH works on in situ protection and monitoring of fish. degradation and loss of critical fish habitats in Australian marine MAGDOLNA MÜLLERNÉ TRENOVSZKI,BÉLA URBÁNYI and TAMÁS and freshwater ecosystems. Marine and Freshwater Research, , MÜLLER work on the ex situ conservation of protected and threatened –. fish species. BÉLA CSÁNYI and JÓZSEF SZEKERES monitor surface RESHETNIKOV, A.N. () Spatio-temporal dynamics of the waters in light of the EU Water Framework Directive, and assess the expansion of rotan Perccottus glenii from West-Ukrainian centre of status of their macroinvertebrate, faunal and fish assemblages.