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Is Pseudanodonta Complanata the Most Vulnerable of Widespread European Species of Unionids? an Intense Stress Test Leading to a Massive Die‐Off

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Is Pseudanodonta Complanata the Most Vulnerable of Widespread European Species of Unionids? an Intense Stress Test Leading to a Massive Die‐Off Received: 17 January 2019 Revised: 24 May 2019 Accepted: 22 July 2019 DOI: 10.1002/aqc.3216 RESEARCH ARTICLE Is Pseudanodonta complanata the most vulnerable of widespread European species of unionids? An intense stress test leading to a massive die‐off Adam M. Ćmiel | Katarzyna Zając | Anna M. Lipińska | Tadeusz Zając Institute of Nature Conservation, Polish Academy of Sciences, Kraków, Poland Abstract 1. This article reports a large‐scale die‐off of approximately one‐third of the unionid Correspondence Adam M. Ćmiel, Institute of Nature mussels inhabiting a shallow, naturally eutrophic, floodplain lake (Zalew Conservation, Polish Academy of Sciences, al. Pińczowski), which took place within the space of just a few days. A. Mickiewicza 33, 31‐120, Kraków, Poland. Email: [email protected] 2. Mortality was the highest in Pseudanodonta complanata (81%), followed by Unio pictorum (58%), Anodonta cygnea (26%), Unio tumidus (15%), and Anodonta anatina Funding information Statutory funds; Subsidy for young scientists, (5%). It was significantly related to mussel size (age) only in A. cygnea, with the Grant/Award Number: 188/N/2017 mortality rate higher in smaller (young) mussels. 3. Pseudanodonta complanata was already the rarest species in the lake, and the num- ber of survivors decreased to such an extent as to trigger a possible Allee effect. 4. The most likely cause of the die‐off was a motor‐boating incident that had directly preceded the die‐off. Analysis of the water samples collected just after the die‐off revealed an extremely high concentration of phosphate (up to 0.5 mg dm−3) and nitrite (up to 0.06 mg dm−3). We suggest that the boat movements must have dis- turbed the lake sediments, thereby disrupting the mussels' physiology and causing mass mortality. 5. The high sensitivity of P. complanata to environmental stress suggests that it may be an effective umbrella species for the protection of co‐occurring mussel species in eutrophic lakes. KEYWORDS extinction, extreme disturbance, mortality, motor‐boating, nitrite, phosphate 1 | INTRODUCTION indicator (Viarengo & Canesi, 1991) and umbrella species (Geist, 2010). Freshwater mussels (Unionidae) are among the most endangered Mussel die‐offs — episodic events when hundreds to thousands of animal groups in the world (Lydeard et al., 2004), and in recent mussels die during a short period (days to weeks) — have increased in decades a growing number of studies have been conducted frequency since 1982 and exceeded the normal occurrence of isolated concerning their ecology and conservation (Lopes‐Lima et al., 2018; incidents that are part of the natural population dynamics of this fauna Sousa, Novais, Costa, & Strayer, 2014). They perform many important (Neves, 1987). The aetiology of the die‐offs remains largely unknown, functions in aquatic ecosystems, which can be framed as ecosystem and only a small number of causative factors have been identified; for services (Vaughn, 2018). Some species fulfil the criteria for example, diseases (Neves, 1987), poisoning (Fleming, Augspurger, & Aquatic Conserv: Mar Freshw Ecosyst. 2019;1–8. wileyonlinelibrary.com/journal/aqc © 2019 John Wiley & Sons, Ltd. 1 2 ĆMIEL ET AL. Alderman, 1995), flood (Hastie, Boon, Young, & Way, 2001; Sousa mussel mortality in the lake. Along the southern shore of Zalew et al., 2012), drought (Gagnon, Golladay, Michener, & Freeman, Pińczowski, five 10 m long transects were marked out perpendicu- 2004; Haag & Warren, 2008; Galbraith, Spooner, & Vaughn, 2010; larly to the shore at intervals of ~150 m (Figure 1a). The water Bódis, Tóth, & Sousa, 2014; Sousa et al., 2018), and water manage- depth and the silt layer were measured every 0.5 m along each ment (Gołąb, Lipińska, & Ćmiel, 2010). Moreover, for many species, transect. At the same points, bottom samples were collected from a major shortcoming is a lack of knowledge regarding their biology an area of 0.5 × 1 m2 using a 50 cm wide dredge rake with nylon and habitat requirements (Ferreira‐Rodríguez et al., 2019; Lopes‐Lima netting (2 mm mesh; Figure 1b). All the bottom sediment down to et al., 2018). a 20 cm depth was taken and sieved, the mussels being retained In Europe, there are at least 16 species of unionids (Lopes‐Lima in the rake netting. Dead mussels floating on the water near the et al., 2017), most of which used to be widely distributed and shore in a 20 m2 area (two 10 × 1 m2 strips, one on each side of abundant. Three of them (Margaritifera margaritifera, Margaritifera the transect; Figure 1c,d) were counted. In addition, along each auricularia, and Unio crassus) suffered a rapid decline, which suggested transect, mussels in the following categories were counted and their their great vulnerability; this led to their protection by the European shell lengths measured: moribund (half‐open shell, not adducting Habitats Directive (Council of the European Communities, 1992) and after removal from the water) and dead (evidently dead, with shell the application of active conservation measures (>€60 million spent; open to ligament resistance, or shell with fresh remnants of body Lopes‐Lima et al., 2017). However, the sparse distribution, small or adductor muscles; Figure 1e). Mussel age was determined from number of recorded populations, and low density of Pseudanodonta the number of their annual growth rings. Water temperature, complanata, which is especially rare in central and eastern Europe conductivity, oxygen content and turbidity were measured using a (Lopes‐Lima et al., 2017), raises the question of its conservation HACH HQ40D portable multimeter and a HACH 2100P portable status. Pseudanodonta complanata has only a narrow range of suitable turbidimeter at two sampling points on each transect (2 m and habitat conditions and may thus be one of the most vulnerable of the 10 m from the shore). Water samples for chemical analysis were European unionids. However, knowledge of its ecology is very limited taken at three points (see Figure 1a), stored in 0.33 dm3 plastic (Lopes‐Lima et al., 2017; McIvor & Aldridge, 2007). containers, placed in a field refrigerator and transported to the Zalew Pińczowski, a eutrophic floodplain lake, used to be inhabited laboratory, where they were analysed by a Dionex ion chromatogra- by populations of five species of European unionids, including phy system the following day. The results were compared with the P. complanata (Zając, Zając, & Ćmiel, 2016). On August 25, 2018, reference (mean) values from chemical analyses performed between shortly after a motor‐boating incident, a massive die‐off of freshwater 1999 and 2001 (Zając, 2001) and between 2013 and 2017 mussels in the lake was observed. This event can be treated as a (A. M. Ćmiel, unpublished data). natural experiment — an intense stress test, as it were, of the ecolog- To analyse the influence of the habitat parameters and body size ical stability of the most widespread species of European unionids. on mussel survival, a generalized linear (GLZ) model was constructed (binomial, logit; binomial response variable: live/dead mussel; categorical predictor: mussel species; continuous predictors: position | 2 MATERIALS AND METHODS of the transect on the shore [rank increasing from the lake to the water intake], distance of the bottom sampling site along the 2.1 | Study site transect from the shore, water depth and silt layer thickness at the sampling site, mussel shell length). GLZ models based on the ń ′ ″ ′ ″ Zalew Pi czowski (50°31 08 N, 20°30 58 E; see detailed description same scheme were constructed separately for each mussel species. ą in Zaj c et al., 2016) is a naturally eutrophic, shallow floodplain lake. It The significance of the differences in mussel length between live has an area of 11.4 ha, a mean depth of 1.4 m (maximum depth 1.5 m) and dead individuals of each species was tested using one‐way 3 and a volume of 160,000 m . Five of the six species of unionid mussels analysis of variance. present in Poland inhabit this lake: the swollen river mussel (Unio The probability that all individuals of each species occurring in a tumidus), painter's mussel (Unio pictorum), duck mussel (Anodonta given transect were of the same sex was calculated using the binomial anatina), swan mussel (Anodonta cygnea), and depressed river mussel distribution probability mass function (detailed description in the (P. complanata). As two of these species, A. cygnea and P. complanata, Supporting Information). are endangered, they are legally protected in Poland (Zając, 2004a, 2004b). Pseudanodonta complanata is considered an endangered spe- cies in many European countries, whereas the other four species are 3 | RESULTS regarded as less threatened (Lopes‐Lima et al., 2017). In total, 901 unionids (18.1 ind. m−2; standard deviation SD = 7.43) 2.2 | Sampling and data analyses were found during the sampling, of which 398 were identified as A. cygnea (7.96 ind. m−2; SD = 5.12), 224 as U. pictorum The data were collected on September 4, 2018, 12 days after a (4.88 ind. m−2; SD = 1.77), 188 as U. tumidus (3.76 ind. m−2; SD = 1.33), motor‐boating incident and 10 days after the first notification of 47 as P. complanata (0.94 ind. m−2; SD = 0.30), and 44 as A. anatina ĆMIEL ET AL. 3 FIGURE 1 General view of Zalew Pińczowski (and its location in Poland) showing (a) the transects and water sampling sites, (b) transect sampling scheme, (c,d), zone of dead mussel bodies floating in the water near the bank, and (e) a shell of a recently dead individual. White arrows indicate mussel bodies floating in the water. (0.88 ind. m−2; SD = 0.52). The total number of individuals found dead In the models constructed for each species separately, the was 284 (32%), and 19 (2%) were found moribund.
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