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Effect of Salinity on the Growth and Survival of the Freshwater Mussel Unio crassus in an Environmentally Disturbed River.

Byline: Ertan Ercan and Ali Serhan Tarkan

Abstract

The aim of this study was to examine the effects of salinity on the survival and growth of a freshwater mussel Unio crassus from a Mediterranean stream (Saricay Stream) in south-west Anatolia Turkey which has highly variable environmental conditions and a salinity gradient. A total of 250 similarly-sized U. crassus were collected from a stream in the species' native range and transferred in ice to Saricay Stream. The length width height and weight of each individual were measured before and after the sampling period a period of 286 days. Significant increases were detected in the height width and weight of mussels at all sampling points during the study with the exception of weight in the sampling station third with salinity of 3. Increase in mussel weight was highest at the second station (19.29%) with a moderate salinity (1.5) while that with a growth loss was observed at the third station (-1.56%) with the highest salinity concentration (3).

Survival rates over the duration of the study were 60% 56% and 66% at stations 1-3 respectively. All mussels were dead at the fourth (salinity 4.5) and fifth stations (salinity 6) at the end of the experiment.

Keywords: Freshwater mussel weight gain salinity temperature nutrient enrichment survival rate.

INTRODUCTION

Freshwater mussels are key components of freshwater ecosystems and have worldwide ecological and economic significance. Filter feeding behavior by mussels removes phytoplankton and suspended particles from the water column (Ahmed 1971; Kasprzak 1986; Kryger and Riisgaerd 1988; McMahon 1991; Welker and Walz 1998; Strayer et al. 1999). When mussel biomass is large filter feeding has a profound impact on ecological processes (Welker and Walz 1998). Mussels also have an impact on the calcium budget of freshwater systems and serve as food items for other organisms (McMahon 1991).

Despite their importance many aspects of their ecology are still unknown. In Turkey the existed information is restricted to their growth (Ercan et al. 2013a b) ontogeny (Ozdemir 1991; Sereflisan 2003; Cek and Sereflisan 2006; Ercan et al. 2013c) species description (Bascinar et al. 2003; Bilgin 1980; Cetinkaya 1996; Demirsoy 1999; Geldiay and Bilgin 1969; Oktener 2004; Ozemsi 1999; Ercan et al. 2013c) distribution (Bascinar et al. 2003; Bilgin 1980 1987; Cetinkaya 1996; Geldiay and Bilgin 1969; Oktener 2004; Ozemsi 1999; Ercan et al. 2013c d) abundance (Ercan et al. 2013e) and effects of pollution (Celiloglu-Begenirbas 2002).

Freshwater mussels are sensitive to a variety of pollutants including the impacts of salinity. Elevated salinity in freshwaters can result from land-use change pollution events drought conditions and climate change with consequences for the survival and viability of populations of freshwater mussels (Kaushal et al. 2005; Sherif and Singh 1999). Despite its potential significance the impact of elevated salinity has only recently been recognised as having a significant impact on freshwaters and attempts to understand its effects have been limited to specific taxa; insects (Hassell et al. 2006) macrophytes (James and Hart 1993) and snails (Kefford and Nugegoda 2005). Studies on salinity tolerance of freshwater mussels are limited and include experimental studies focusing on the zebra mussel Dreissena polymorpha which is considered as one of the most invasive mussel species that causes serious economic losses.

Another recent experimental study on the effects of salinity on mussels was on the multiple life stages of a common freshwater mussel Elliptio complanata which demonstrated that low levels of salinity could have a dramatic effect on the reproduction physiology and survival of this species (Blakeslee et al. 2013). An impact of salinity on the reproduction of freshwater unionids was also shown through a decrease in glochidia viability in the freshwater mussel Lampsilis fasciola (Gillis 2011).

Unio crassus Philipsson 1788 is a native mussel species in Turkish waters. It was classified as having an 'endangered' status in 1990 which was later changed in 1994 to 'threatened' by IUCN (the International Union for Conservation of Nature). Although there have been several studies on this species in Turkey (Ilhan et al. 2004; GA1/4relli and Ozbek 2012; Ercan et al. 2013ce) its distribution and population status are poorly known. In addition there have been no studies conducted on its salinity tolerance or the effects of salinity on its growth in natural conditions despite its ecological importance and endangered status.

The aim of the present study was therefore to investigate the survival and growth of U. crassus from a Mediterranean-type stream in south-west Anatolia Turkey in a highly variable environment and showing a distinct salinity gradient. Our specific goals were to find out the salinity tolerance and effects of salinity on growth of U. crassus among different stream zones with variable salinity concentrations.

MATERIALS AND METHODS

Study site

Saricay Stream is situated in the south- western region of Anatolia part of Mugla Province and drains into GA1/4llA1/4k Bay (Fig. 1). The stream has a large reservoir named the Geyik Reservoir on its course and experiences a typical Mediterranean climate with hot dry summers and mild wet winters. There are a number of human disturbances on the stream mainly river channel regulations destruction of the riparian zone water abstraction for agriculture and solid waste inputs from fish feed and yogurt industries. The influx zone of the stream has brackish water springs which makes the surrounding area suitable for earth pond marine aquaculture facilities. Salt concentrations in the water increase steadily towards the sea reaching 6 in the estuary zone. Five sites were selected on the stream that had similar physical environments but differed in their salinity regime of 0 1.5 3.0 4.5 6.0 for stations 1-5 respectively.

Three of these sites (0 1.5 3) (i.e. first three stations) were located on the stream whereas the other two sites (4.5 6.0) (i.e. the fourth and fifth stations) were located on channels connected to the stream (Fig. 1 Table I).

The study was conducted between February and November 2011. A total of 250 similarly-size U. crassus specimens was collected by hand within its native range in the Tersakan Stream (Dalaman Mugla) and transferred in ice to the Saricay Stream. Before collection all individuals were checked for eggs availability and individuals that were not carrying eggs were selected for further analyses. All individuals were measured in three dimensions (width height and length) using digital calipers to the nearest 0.1 mm and their dry weight measured on an electronic balance to the nearest 0.01 g. To avoid biased calculation in dry weight the mussels were first taken out of water and they were measured after flushing the water inside of the mussels by opening their shells. All measured mussels were placed into buckets with 5 mm mesh sizes and 50 L volume. Fifty individuals were placed in each bucket. No modifications were carried out on the mussels.

All groups were placed at each station with a 1m s-1 flow rate which was the same flow condition with the site of collection in the Tersakan Stream. Experimental mussels were checked monthly for a total of 286 days. Mussel size and weight were measured before and after the sampling period. The number of dead mussels was counted on each monthly visit. However died mussels were not included in growth calculations as all mussels were individually tagged.

The instantaneous growth rate (K) for length width height and weight was calculated by modifying the following equation for each measurement (Malouf and Bricelj 1989): K = (lnS2 lnS1)/t2-t1) where S1 S2 are respective size measurements (length L; width W; height H; weight We) at the beginning and end of the study respectively. The duration of the study (in months) is expressed by t (t2-t1). Relative growth rate (RGR %) was calculated: (W2-W1/W1) A- 100 where W2 and W1 is the final and initial weight respectively.

Survival rate (%) was estimated according to the formula; S = (Nt/N0) A- 100 where Nt is the number of live mussels removed from the buckets after t and N0 is the number of mussels at the beginning of the study.

Water samples for nutrient analyses were collected monthly at each of the study sites throughout the sampling period and analyzed by Standard Methods for the Examination of Water and Wastewater (APHA et al. 1985). Water samples for Chlorophyll-a content was filtered and extracted through ethanol. Following centrifugation absorbance was measured before and after acidification in a spectrophotometer and then estimated (Ryther and Yentsch 1957). Temperature dissolved oxygen conductivity TDS salinity and pH were measured in the field using a multi- parameter probe (YSI 556 MPS).

Differences in mean size of the mussels (length weight and height) between the beginning and end of the experiment were tested with a t-test while size variations in growth rate among the study sites were determined using a one-way ANOVA using population means for each variable. When significant differences among the sites were found a Tukey HSD test was used to determine which sites were different. Chi-squared (x2) tests were used for survival rate comparisons. P less than 0.05 was accepted as the level of significance for all analyses.

RESULTS

Survival rates in three study sites were 60% 56% and 66% respectively by the end of the study (Table I). There were no statistical differences among the study sites (2 = 0.196 Pgreater than 0.05) although mussels in station 3 had the highest survival rate. All mussels were dead in the fourth and fifth stations at the end of the first week of the experiment.

Length measurements of U. crassus at the beginning and at the end of the experiment showed no significant differences in all stations (t-tests P greater than 0.05). However there were significant increases detected in other size measurements (height width and weight) (t-tests P less than 0.05) for all study sites with the exception of weight (t-test P = 0.571) at the third station with a 3 salinity concentration (Table I Fig. 2). Growth rates measured as length (ANOVA F = 0.111 P = 0.895) width (ANOVA F = 0.248 P = 0.781) height (ANOVA F = 0.893 P = 0.413) did not differ significantly among study sites but weight showed a significant difference with the mean weight of mussels at the third station lower than the other two stations (ANOVA Tukey HSD F = 31.331 P less than 0.001). Increase in weight was highest at the second station (19.29%) with moderate salinity concentration (1.5) while there was a weight loss at station 3 (-1.56%) with a higher salinity concentration (3) (Table II).

Table I.- Differences in the number of individuals survival rates size measurements (weight length width and height) and relative growth rate as percentage of Unio crassus at the beginning and the end of the study from five sampling stations in the Saricay Stream.

###Stations

###1###2###3###4###5

Initial no of individuals###50###50###50###50###50

Final no of individuals###31###28###34###0###0

Survival rate (%)###62###56###68###0###0

Initial weight###42.924.06###46.0310.21###47.977.67###47.058.17###49.039.23

Final weight###51.296.46###58.328.18###47.375.32###-###-

Initial length###64.392.09###66.073.97###64.272.57###66.822.68###68.314.12

Final length###64.632.39###66.703.80###64.742.74###-###-

Initial width###42.411.69###42.542.43###41.481.60###43.521.82###44.211.96

Final width###44.461.71###45.122.04###44.181.65###-###-

Initial height###25.151.20###25.52.18###23.761.32###25.381.44###26.171.23

Final height###26.671.27###28.052.58###26.131.23###-###-

RGR (%)###17.38###19.29###-1.56###-###-

Table II.- The instantaneous growth rate (K) of Unio crassus for length (L) width (W) height (H) and weight (We) at study stations 1-3 on the Saricay Stream.

K###K (L)###K(W)###K (H)###K (We)

1st station###0.0006###0.005###0.005###0.010

2nd station###0.0004###0.005###0.007###0.020

3rd station###0.0007###0.004###0.007###0.001

Mean environmental parameters measured in Saricay Stream during the study period are presented in Table III. The first two stations had similar values for physico-chemical measurements showing higher temperature but lower conductivity TDS orto-phosphate and chlorophyll-a values than those at other stations (Table III). Higher TDS and conductivity values in the last two stations (fourth and fifth) are probably due to the high correlation of these variables with salinity. However both these stations along with third station had notably higher chlorophyll-a concentrations (Table III). Other chemical components which are indicative of trophic status of the water were similar among all sampling stations (Table III).

DISCUSSION

The results of the present study represent the first findings of salinity tolerances and growth responses of the freshwater mussel U. crassus and indicated that moderate salinity concentrations (1.5) supported the greatest weight increase but least survival rate among different salinity levels examined although these rates were not significantly different among the sampling sites with different salinity concentrations with the exception of 4.5 and 6 where all mussels died. This finding suggests that the salt concentrations are increasingly ideal for growth up to 1.5 for U. crassus but higher salt concentrations than 3 were lethal for this freshwater mussel species. This would be expected as elevated salinity can trigger the growth of aquatic organisms within certain limits a well-known phenomenon for several fish and mussel species (Blakeslee et al. 2013; Gonzalez 2011).

Unfortunately there were no available data on the effect of salinity on the survivorship and the growth of U. crassus from other field studies that can be used to compare with our data. Other available studies have usually been conducted on common marine mussel species such as Meretrix meretrix Katelysia opima Mytilus viridis and Mytilus edulis and freshwater species D. polymorpha E. complanata and L. fasciola (Ranade and Kulkarni 1973; Fong et al. 1995; Gillis 2011; Blakeslee et al. 2013). These studies have clearly shown profound effects of salinity on growth breeding and distribution of the mussel

Table III.- Mean environmental variables at the sampling stations on the Saricay Stream.

###Stations

###1###2###3###4###5

Number###10###10###10###1###1

Temperature (C)###215.91###20.65.40###16.91.33###18###17.5

Conductivity (S/m)###356.5100.53###384.598.07###431178.80###672###1071

TDS (mg/L)###0.240.05###0.270.06###128.0963.92###3.88###6.62

Salinity ()###0.10.04###1.50.05###30.08###4.5###6

DO (mg/L)###7.382.51###9.143.13###9.892.42###8.3###8.9

pH###7.790.95###7.220.93###7.090.66###6.78###7.06

Nitrite-N (mg/L)###0###0###0###0###0

Nitrate N (mg/L)###0.700.01###1.320.02###0.750.01###1.95###1.78

Ammonium- N (mg/L)###0.110.02###0.010.001###0.110.01###0.29###0.18

o-phosphate (mg/L)###1.050.03###0###1.990.04###2.08###1.53

Suspended solids (mg/L)###0.130.01###0.130.01###0.140.01###0.32###0.26

Cl-a (mg/m3)###10.120.21###4.180.07###21.354.98###25.16###20.56

species. Similarly the larvae of mussel species seem to be strongly influenced by salinity (Tham et al. 1972). Blakeslee et al. (2013) studied the effects of salinity on several life stages of the freshwater mussel E. complanata in experimental conditions demonstrating that salt concentrations as low as 4 resulted in mortality after only 48 hours of exposure concentrations as low as 3 disrupted reproductive success and concentrations as low as 2 significantly depressed metabolic rate.

These results are in accordance with our findings which showed the survivorship at 3 was the limit for the survival of U. crassus in nature. However it should be noted that there could be some differences between experimental and natural conditions where there are many more confounding environmental variables.

The growth of the mussels measured as mean weight or size gain may dependent on several factors. Indeed growth of U. crassus has been demonstrated as variable depending on the environment in which they live (Akyurt and Erdogan 1993; Ercan et al. 2013e). Therefore in addition to salinity it is expected that growth may vary along a gradient of ambient natural factors such as nutrient availability and water temperature. Temperature for instance is known to have a major impact on mussel growth because it affects metabolism and the timing of reproduction (McMahon 1991). In the present study the temperature was higher (215.91) in the first two stations with the second station slightly colder (20.65.40) than first station while the third station had notably lower (16.91.33) than that in other stations. This difference would explain the reduced growth of U. crassus in station 3 which had a 3 salinity concentrations.

However higher weight gain at the second station could not be attributed to temperature since the first two stations had similar mean temperatures throughout the study period.

In parallel with temperature nutrient availability had a similar role for growth variation of U. crassus among study sites which were highly variable. Despite significantly higher chlorophyll-a values at station 3 weight increase was limited. This would suggest that the growth of U. crassus was limited by salinity rather than other environmental conditions such as temperature and food availability (Ranade and Kulkarni 1973; Gillis 2011; Blakeslee et al. 2013; Ercan et al. 2013e). Increased growth of the species at a certain salinity concentrations (1.5) is indicative of importance of this variable (Ercan et al. 2013b). The study site (Saricay Stream) receives numerous inputs from agricultural industrial and municipal sources which might lead variable growth and survival patterns for mussels in different sections of the stream. However the effects of the analyzed variables for U. crassus were strongly dependent on salinity variation in the stream.

This effect can be explained by the fact that U. crassus is tolerant of relatively low water quality conditions and could be associated with nutrient-enriched waters (Ercan et al. 2013e). Alternatively this might be due to additional variables which were not revealed as key causative factors. The measurements taken in the present study were obtained from water only not sediments yet it is known that mussels receive energy from both resources (Salazar and Salazar 2001).

The low survival rate of U. crassus has been linked to nitrate concentrations between 2 and 10 mg L-1 (KAlhler 2006). This was not the case in Saricay Stream since nitrate concentrations measured at all of stations never exceed 2 mg L-1. Healthy U. crassus populations exposed to nitrate levels varying from 0.4 mg L-1 to 0.6 mg L-1 have been reported from a similar stream in northwestern Turkey (Ercan et al. 2013e). Salinity on the other hand is certainly a limiting factor for the survival of U. crassus as all mussels were dead at salinity levels of 4.5 and 6. Salinity is known as the most limiting factor for the widely-distributed mussel species D. polymorpha in European brackish waters (Strayer and Smith 1993) although reproduction of this species was reported to be possible in brackish water below 7 when mussels are acclimated to brackish water (Fong et al. 1995).

This may suggest that mechanisms may have evolved for surviving and reproducing when mussels are exposed to brackish waters. This seems to be case for U. crassus which adapt to varying salinity concentrations within certain limits in Saricay Stream. However while not examined in the present study a negative effect of increased salinity on glochidia production has been observed (Blakeslee et al. 2013). Other similar studies have also reported that 24 h of salt exposure from 0.1 to 2.0 decreased glochidia viability in several mussel species but the lethal concentrations are variable among mussel species (Bringolf et al. 2007; Cope et al. 2008; Gillis 2011). These studies clearly indicated that salinity had a dramatic effect on the reproduction of freshwater mussels by reducing successful host infestation of glochidia (Gillis 2011; Blakeslee et al. 2013).

From the results of this study which constitute the first evaluation of the effect of salinity on U. crassus under natural conditions it can be concluded that U. crassus could successfully be reared in a salinity range 0-3 ideally at 1.5. It should be noted that our results represent a long- term evaluation and should be further re-studied with short-term experiments for assessing survivorship and growth. Furthermore since the effects of salinity could differ depending on season seasonal effects should also be experimentally examined. If salinity stressors have important consequences for the reproductive success of freshwater mussels salinity is also likely to impact their population dynamics and persistence. This may become an increasingly important issue given increased worldwide salinization of freshwater ecosystems.

ACKNOWLEDGEMENTS

We thank Bahadir Onsoy Neslihan Agrali Murat Can Sunar Nildeniz Top Ugur Karakus and Sevan Agdamar for their invaluable help in sampling and water quality analyses. This study was financially supported by Mugla Sitki Kocman University Research Fund (BAP) - Project Number: 2011/35. In addition we thank the two anonymous reviewers for their useful comments to improve the paper.

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Author:Ercan, Ertan; Tarkan, Ali Serhan
Publication:Pakistan Journal of Zoology
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Date:Oct 31, 2014
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