Article #156 South African Journal of Science

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21 Under 14 of the Eichhornia % was found Research Article and an average 2 hwater s T. granifera including the Kruger 5 Mytilus galloprovincialis Mytilus is of African and global may prove difficult in the in difficult prove may fre

T. granifera. S Afr J Sci (lethal salinity for 50 50 ive can cause ecological disturbances s T. granifera

T. granifera T. to salinity and temperature through the 18,19,20 is present in an increasing number of fresh C, allowing it to survive high temperature high survive to it allowing C,

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11 10 cm), which are quickly heated by the sun to may have been introduced into KwaZulu-Natal, < However, there is a lack of studies on the ecological the on studies of lack a is there However, A number of studies have assessed the effects of 5 the . T. granifera granifera,

C and 47.5 and C 16,17 º in an estuarine environment was in South Africa at the St the at Africa South in was environment estuarine an in of ABSTRACT

granifera T. granifera

INTRODUCTION Physa acuta Physa as well as invertebrates such as the mussel the as such invertebrates as well as Successful invaders progress beyond the introduction and 3 5,9,10,11,12 T. granifera T. 4,6,7 arebia C in summer. º mortality within 48 h. Snail activity also declined with increasing salinity. T The loss of water from the system has also meant a drop in water levels and

14 % and the snail the and 4 tolerance

This high surface area to volume ratio is conducive to great evaporative water losses, population. Snails acclimated to freshwater conditions and suddenly transferred to The first record of record first The is a freshwater prosobranch gastropod (family: ), originally from South-East 15 Vol. 106 No. 3/4 Page 1 ofVol. 7 13 ’s environmental tolerance and parthenogenetic characteristics are the keys to successful In South Africa, knowledge of aquatic invasive has increased over the past two 1 tropod was first recorded in an estuarine environment in the St Lucia Estuary. Its tolerance to 0 between temperatures tolerate can fish such as bass and trout, and bass as such fish s 2 Carcinus maenas Carcinus from invading. , The species has spread rapidly in recent years across a number of countries throughout tropical T. granifera 8,9 ga Tarebia graniferaTarebia granifera factors. these of manipulation experimental the through investigated was temperature and salinity granifera constitute a contribution short to medium term. The present findings to the knowledge of biological of estuarine invasions by invasions in Africa and to the understanding Invasive aquatic species, such as the gastropod and potentially reduce by displacing indigenous invertebrates. In South Africa, remarkably, More areas. altitude higher invade and snaps cold survive also may species The extremes. this snail survives high salinity for a relatively population) was long reached time, at as 30 LS psu over 65–75 days. However, the higher salinity adversely affected 30 psu experienced 100 T. granifera of management the Therefore, establishment. and introduction temperature and salinity on invasive aquatic invertebrates. interest due to its invasive ability and the potential impact on indigenous benthic communities. consequences of invasive aquatic invertebrates in freshwater and estuarine systems. These consequences consequences These systems. estuarine and freshwater in invertebrates aquatic invasive of consequences may include biotic homogenisation, competitive exclusion of indigenous species and properties of the changes invaded habitat. to the reported here will contribute to an understanding of the threat that this snail poses, and possibly also to also possibly and poses, snail this that threat the of understanding an to contribute will here reported its management in Africa and elsewhere. the formation of large areas of very shallow depth ( reach temperatures over 45 In January 2007, a dense population (over 5 000 individuals per square metre) of in a very shallow freshwater seepage zone just south of the Old Jetty in Catalina Bay and, in February 2007, it was found in similarly high densities at embayments as far south as Brodie’s Crossing (Figure 1). Salinity conditions in these embayments were brackish rather than fresh, but this did not prevent granifera Salinity and temperature are among and the distribution patterns main of factors aquatic molluscs. influencing growth, reproduction, survival study investigated the lethal tolerance limits of experimental manipulation of these factors. It provides the first experimental data on the responses of results The estuaries. of environments saline/brackish the in factors physicochemical key to invader this Asia. and subtropical areas of the World. South Africa, via the trade in the early 1990s. and brackish water bodies of Park. National KwaZulu-Natal and which environment) freshwater Mpumalanga (a Stream Nkazama the provinces, in 2005 December in found was It Estuary. Lucia flows into the eastern shore of the South Lake, 1.2 km north of Catalinaestuarine Baysystem (Figureis 1).part Theof Stthe Lucia iSimangaliso (formerly known as the Greater has Lucia St Recently, Importance. International of Wetland St Ramsar a and Site Heritage World a is This Lucia) Wetland Park. been experiencing severe freshwater starvation. The mouth closed in June 2002 and this ‘closed-mouth conditions. temperature water and salinity variable to leading 2007, March until persisted state’ normal conditions, the St Lucia estuarine system has a surface area of around 350 km depth of 0.9 m. causing some areas to become hypersaline (salinity greater than 40 psu). However, developed fresh or other brackish conditions due areas to the input of have fresh water from rivers, streams or seepage from sand dune aquifers. have been widely reported as having a negative impact on the ecology and economy of a region. hyacinth water the as such species, invasive prominent on been has focus the far, So decades. crassipes crab the Management impacts. ecological tangible have finally and habitats new in spread stages, establishment is it until noticed not is invader the cases, many in but, introduction, preventing on focus should efforts already established. Ecophysiological knowledge about the invading species is essential in considering whether, and how, to implement control measures. temperature

. 1 and

1 1 Tarebia granifera alinity S School Biological of and at: http://www.sajs.co.za Art. 7 pages. #156, DOI: 10.4102/sajs.v106i3/4.156 This article is available and temperature tolerance of the invasive freshwater gastropod S Afr J Sci. 2010;106(3/4), How to cite this article: MirandaPerissinotto NAF, R, Appleton CC. Salinity Dates: 2009 July Received: 17 2010 Accepted: Feb. 01 Published: 2010 23 Apr. mollusc; lethal tolerance; South Africa; Lucia St Estuary Durban 4000, South Africa Keywords: alien species; aquatic Conservation Sciences, University KwaZulu- of Natal, Westville campus, Private X54001, Bag [email protected] Postal address: School Biological of and Correspondence to: Nelson Miranda email: University KwaZulu- of Natal, Westvillecampus, South Africa Affiliations: 1 ConservationSciences, Authors: MirandaNelson A.F. Renzo Perissinotto Christopher C. Appleton Publishing. This work is licensed under the Creative Commons Attribution License. © 2010. The Authors. © 2010. Licensee: OpenJournals http://www.sajs.co.za Salinity and temperaturetolerance of Research Article Miranda

in these conditions for 48 h prior to the experiment and fed ad libitum on naturally occurring benthic microalgae. Suspensions of microalgae were obtained by scooping the upper few millimetres of sediment and re-suspending them through stirring, and then harvesting the supernatant. Temperature-controlled, aerated water baths were used to achieve the following treatments: 0 ºC, 5 ºC, 10 ºC, 20 ºC, 30 ºC, 40 ºC, 45 ºC, 47.5 ºC and 50 ºC. Bottles reached test temperatures within 30 min. A control water bath was placed outside and its temperature was not controlled. Six replicates (900-mL bottles with 20 live individuals each) were used per water bath. Mortality, defined as a lack of response to a mechanical stimulus (gentle prodding with a fine brush), was recorded after exposure times of 2 h, 4 h, 8 h, 16 h and 32 h. At 0 ºC, the water in some bottles froze due to their close proximity to the water bath’s cooling element. Although these treatments were not included in the data analysis, the snails retrieved from such bottles were thawed and kept at a recovering temperature of 20 ºC for 12 h, after which mortality was tested. A second stock of snails was collected from Catalina Bay on 18 July 2007 (salinity ≈ 28 psu) and this procedure was repeated at 30 ± 2 psu (diluted, sterilised sea water was used) with a freshwater control treatment. Results were expressed as per cent survival.22

Salinity tolerance The experimental procedure for salinity tolerance was similar to the above, using stock collected in July 2007. Six replicates (900-mL bottles with 20 live individuals each) were subjected to each of the following salinities: 0 ± 0.5 psu, 10 ± 2 psu, 20 ± 2 psu, 30 ± 2 psu and 40 ± 2 psu. The 40 ± 2 psu concentration was prepared by the addition of natural sea salt and measured using a water logger (YSI 6920, YSI Incorporated, Yellow Springs, OH, USA). Mortality was monitored over a period of 85 days. Dead individuals were removed immediately. T. granifera is ovoviviparous and has a brood pouch from which juveniles (shell height ≈ 1 mm) are born. Hence the presence of live juveniles in a bottle was recorded as birth. Water was changed every 5–10 days and food renewed weekly. The activity of snails in each bottle was monitored and classified according to four progressive criteria: actively moving, not moving (foot anchored), head out of shell (foot not anchored) and quiescent

Article #156 with closed. The proportions of snails in each bottle conforming to these criteria were recorded every 10 days. These data were used to calculate the distribution of snail activity for each salinity treatment over the total exposure time up to

Source: Adapted from Vrdoljak and Hart33 with permission of NISC (Pty) Ltd. 85 days. A ‘salinity shock experiment’ was also conducted, in South African Journal of Science which 12 replicates were acclimated to fresh water for a week. FIGURE 1 Map of the St Lucia estuarine system, showing Catalina Bay on the eastern Six replicates were then transferred directly to 30 ± 2 psu, with shores of South Lake the remainder serving as control. Mortality was recorded after 48 h.

MATERIALS AND METHODS Data analysis Study site Data were arcsine-transformed, following a one-sample Catalina Bay is located on a limestone flat on the eastern shore Kolmogorov–Smirnov normality test.23 Repeated measures of St Lucia’s South Lake (Figure 1). The fringing vegetation is analyses of variance (RM-ANOVA) were used where each mainly composed of Cyperus laevigatus, Juncus kraussii and 900-mL bottle containing 20 live individuals was the unit of Salicornia spp. The water in the bay is very shallow (≈ 0.5 m) and replication. Temperature tolerance data were tested using a can reach a temperature of around 50 ºC during summer. From three-way RM-ANOVA (dependent variable: survival; fixed the beginning of 2005 until the breach of the St Lucia mouth in factors: salinity, temperature, exposure time). Salinity tolerance March 2007, the average salinity (± s.d.) in this area was 16 ± 9 data were tested using a two-way RM-ANOVA (dependent psu, a reflection of the influence of the seepage of fresh water variable: survival; fixed factors: salinity and exposure time). from dune systems located to the east of Catalina Bay. Several Tukey post-hoc analyses were done on each of these two data additional freshwater seepage zones were identified south of the sets. Differences between control and experimental treatments Old Jetty at Catalina Bay. After the breach event, a large volume of the ‘salinity shock experiment’ were tested using a two- of sea water entered the system, causing an overall increase in tailed independent-samples t-test. Homogeneity and normality water levels and salinity. During the open phase the average of residuals were tested by a Levene’s test and a one-sample salinity in the bay rose to 30 ± 3 psu. Kolmogorov–Smirnov test, respectively. The statistical program SPSS-15 was used in all analyses. Temperature tolerance RESULTS T. granifera snails (mean shell height ± s.d. = 12.5 ± 2.5 mm) were collected from Catalina Bay (Figure 1) on 11 April 2007 (salinity Temperature tolerance ≈ 13 psu), transported to the laboratory, sorted into groups Survival in the control and the 0 ºC, 5 ºC, 10 ºC, 20 ºC, 30 ºC and of 20 and put into transparent plastic bottles (900 mL). These 40 ºC treatments, at both 0 psu and 30 psu, exceeded 75% for 32 were filled with fresh water≈ ( 0 psu), placed in a controlled- h (Figure 2). Snails died if the water in the bottles froze. Time

environment room at 20 ± 1 ºC with a photoperiod of 12 h of to LT50 at 45 ºC was 8 h – 16 h at 0 psu and 16 h – 32 h at 30 psu light followed by 12 h of darkness. Snails were left to acclimate (Figure 2). Mortality of 100% occurred within 2 h of exposure

S Afr J Sci Vol. 106 No. 3/4 Page 2 of 7 http://www.sajs.co.za Article #156 South African Journal of Science Research Article S Afr J Sci (± s.d.) over s.d.) (± exposure times h – 32 (2 h) FIGURE 2 Tarebia granifera Vol. 106 No. 3/4 Page 3 ofVol. 7 Percentage survival of Tarebia graniferaTarebia Survival rates were calculated at temperatures ranging from 0 ºC to 50 ºC (b–j) and ºC16 at salinities – 22 ºC. of 0 psu (white bars) and 30 psu (grey bars). control The (a) treatments were set in the open at http://www.sajs.co.za Salinity and temperaturetolerance of Research Article Miranda

TABLE 1 significance of its survival at temperatures lower than 10 ºC is that Results of a three-way RM-ANOVA performed to test for exposure time (hours), it may be able to survive cold snaps, as long as the temperature salinity and temperature effects on the survival (%) of Tarebia granifera, in which data were arcsine-transformed before analysis does not drop below zero. It may also indicate that T. granifera is able to invade areas at higher altitudes that have colder climates, Source of Sum of d.f. MS F p-level although this has not happened yet in South Africa.21 This variation squares study did not focus on sub-lethal effects of temperature on T. Exposure time (hours) 2.969 4 0.742 119.4 < 0.001 granifera. However, it is likely that this species has an optimum Salinity 0.112 1 0.112 0.4 0.528 temperature range for physiological activities around 30 ºC, Temperature 162.7 10 16.268 2616.2 < 0.001 since we observed physical activity to peak at that temperature (snails moved very fast in the bottles) and decrease in lower and Salinity – Temperature 0.395 10 0.04 6.4 < 0.001 higher temperatures (snails tended to retreat into their shells). If Exposure time (hours) 13.638 40 0.341 54.8 < 0.001 physical activity is taken to be a proxy for physiological activity, – Temperature the results are in agreement with those found by Masilamoni et Exposure time (hours) 0.073 4 0.018 2.9 0.021 al.18 for the bivalve Brachidontes striatulus, although T. granifera – Salinity has wider lethal temperature limits.18 The size of the snail was Exposure time (hours) – 1.687 40 0.042 6.8 < 0.001 not taken into account, but mortality may be assumed to be Salinity – Temperature independent of body size in this study.18 T. granifera seems to respond in similar ways to temperature under both high and low salinity, which means that further investigation is required to 45.7 ºC and 50 ºC at both 0 psu and 30 psu (Figure 2). Thus, to understand its osmoregulatory ability. the thermal tolerance range of T. granifera was determined to be between 0 ºC and 47.5 ºC. A three-way RM-ANOVA showed It is noteworthy that T. granifera was able to survive salinities no significant difference in survival between temperature from 30 psu to 40 psu for just under a month, after which time the treatments (Table 1). A Tukey post-hoc analysis showed, firstly, snails died (Figures 3d and 3e). Salinity tolerance of freshwater a significant difference in survival between the 45 ºC treatment molluscs is thought to be limited only to very dilute and stable at 0 psu and 30 psu and all other treatments (p < 0.05). Secondly, brackish conditions,26,27,28 but T. granifera survived and gave birth there were no significant differences between the 0 ºC, 5 ºC, 10 ºC, 20 ºC, 30 ºC and 40 ºC treatments (p > 0.05) and between to live juveniles at salinities of up to 20 psu. The behavioural the 47.5 ºC and 50 ºC treatments (p > 0.05) and, thirdly, the response of reducing physical activity, retreating into the shell 47.5 ºC and 50 ºC treatments were significantly different from and closing the operculum is thought to be associated with a all others (p < 0.05). reduction in physiological activity and is the strategy used in an attempt to survive until favourable conditions are re-established. Salinity tolerance When T. granifera is under stress, its impact on the environment should be reduced. Thus, T. granifera may have a greater impact Throughout the 85 days, survival remained above 75% at 0 psu, on freshwater than on brackish environments, a pattern already 10 psu and 20 psu (Figures 3a–c) and several individuals gave observed in the invasive bivalve Dreissena polymorpha.20 Unlike birth under these conditions. Time to LS50 at 30 psu was 65–75 most other freshwater invasive invertebrates in South Africa, days (Figure 3d) but 15–25 days at 40 psu (Figure 3e). No births T. granifera has a brood pouch, which provides some measure were recorded during either treatment. A two-way RM-ANOVA of protection to developing stages before birth. Further studies showed a significant difference in survival between salinity should focus on the effects of salinity and temperature on

Article #156 treatments (Table 2). A Tukey post-hoc analysis showed, firstly, reproduction. There is also a need for studies on T. granifera’s no significant differences in terms of survival between the 0 psu, 10 psu and 20 psu treatments (p > 0.05) and, secondly, the 30 psu ecological impact on freshwater and brackish environments, and the 40 psu treatments were significantly different from all and the pre-adaptation of this species to a higher salinity other treatments (p < 0.05). environment is of importance as it contributes to the invasion

South African Journal of Science process. The monitoring of snail activity revealed that T. granifera spent more time in its shell with the operculum closed at high Expected ecosystem impact of T. granifera compared to low salinity. At 0 psu, 71% of snails were actively Previous studies indicate that if T. granifera proliferates it moving, at 10 psu 52%, at 20 psu 33%, at 30 psu 13% and at 40 may displace other invertebrates, thereby causing ecological psu only 2% (Figures 3a–e). At 0 psu, 5% of snails were quiescent, disturbances and a possible reduction in biodiversity.5,10,29,30,31 at 10 psu 6%, at 20 psu 16%, at 30 psu 71% and at 40 psu 96% (Figures 3a–e). However, no ecological studies have been done on this species in South Africa and the mechanisms of impact are not understood.21 The T. granifera population in the St Lucia Estuary has become In the ‘salinity shock experiment’, LS50 at 30 psu was reached quickly, with 100% mortality after 48 h, while the control well established but high salinity certainly poses an obstacle was significantly different because all snails remained alive to its spread and subsequent impact. After a six-month period (independent-samples t-test: t = 96.831, d.f. = 10, p < 0.001). of open-mouth conditions, the St Lucia mouth closed again in August 2007. The large quantities of sea salt that entered the DISCUSSION system caused an increase in salinity over the ensuing months, Range of environmental tolerance despite the input of rain water.32 In November 2007, high mortality was becoming evident in the T. granifera population T. granifera appears to have a wider temperature tolerance at Catalina Bay (salinity ≈ 31 psu). This observation supports than previously proposed in the literature,24 but its relatively 25 the results of the salinity tolerance experiment discussed earlier high levels of tolerance are typical of tropical species. The (Figure 3d). By March 2008, most of the population had died and many empty shells littered the shore as water levels dropped. TABLE 2 In June 2008, at a recorded average salinity of 40 ± 2 psu, no Results of a two-way RM-ANOVA performed to test for exposure time (days) and salinity effects on the survival (%) of Tarebia granifera, in which data were living specimens were found in the study area. In April 2009, arcsine-transformed before analysis however, it was discovered that a portion of the population had Source of Sum of d.f. MS F p-level remained in the adjacent freshwater seepage zones together with variation squares the indigenous salt-sensitive biota.14,33 Other disturbing findings Exposure time 1755.563 8 219.445 39.9 < 0.001 made in the seepage zones a few months later (August 2009) (days) were populations of Lymnaea columella and Aplexa marmorata, both invasive species from the Americas. Salinity 8820.43 4 2205.107 400.9 < 0.001 How these invasive species were introduced and what sort of Exposure time 2088.437 32 65.264 11.8 < 0.001 impact they are having is currently unknown. What is certain is (days) – Salinity that freshwater seepage zones in coastal areas are particularly

S Afr J Sci Vol. 106 No. 3/4 Page 4 of 7 http://www.sajs.co.za Article #156 South African Journal of Science Research Article The present findings 43 S Afr J Sci can be regarded as a global invader 39,40,41,42 discovered with increasing frequency in However, so far there have been no reports 21 T. granifera are being suggest that tropical and subtropical freshwater and estuarine systems located in lowlands (altitude lower particularly than at 500 risk m) in are Africa, trade especially operates. where the aquarium of this species having spread northwards Lucia St the in recorded those to similar situations Nevertheless, from South Africa. Estuary already occur elsewhere in South Africa: populations of T. granifera other areas of the iSimangaliso Park, such as Kosi Bay and Lake Sibaya (Kyle R 2008, personal communication, July 20; Taylor R estuaries other and 26), February communication, personal 2008, suggest that invasions by this species temporarily open/closed could estuaries by be artificially breaching controlled the in mouth. However, such an action (effecting large-scale changes in order to manage a single species) may have unintended and on literature growing the in discussed as consequences, negative adaptive management. In summary, of tropical and subtropical regions. (± s.d.) over s.d.) (± exposure time (5–85 days) FIGURE 3 T. T. was Tarebia granifera Haminoea Vol. 106 No. 3/4 Page 5 ofVol. 7 T. granifera Another option

31,34 29 During this study, from an environment, Percentage survival of Tarebia graniferaTarebia 35,36,37,38 T. granifera T. granifera sp., which often dominate macrobenthic dominate often which sp., Assiminea and showed a drop in physical activity as salinity increased salinity as activity physical in drop a showed populations to gradually adapt to higher salinity as of the population has to be eliminated because of its % n order to completely purge granifera (Figure 4) and, at salinities obviously higher under stress than and 30 died psu, within 3). a snails The ‘salinity shock experiment’ showed few that were weeks (Figure very vulnerable to sudden salinity increases. These findings natalensis communities, may be adversely would be the affected. introduction of a biological control agent, but this has its own widely reported risks. parthenogenetic characteristic. The use of molluscicides in the St Lucia Estuary is not feasible at any stage, given that juveniles observation) (personal killed be not may pouch brood the within and non-target species, such as the indigenous snails Prospects for the control of I 100 vulnerable to invasion and may provide the opportunity for granifera they undergo a diffusion dispersal process. Survival rates were calculated at salinities ranging from 0 psu to 40 psu (a–e). Temperature was kept constant at 20 ºC. http://www.sajs.co.za Salinity and temperaturetolerance of Research Article Miranda Article #156 South African Journal of Science

Activity was measured over a period of 85 days and in salinities ranging from 0 psu to 40 psu (a–e). Temperature was kept constant at 20 ºC.

FIGURE 4 Average distribution of Tarebia granifera activity (%) classified into four successive criteria

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19. 18. 16. 17. 15. 13. 14. 12. 10. 11. 9. 8. 6. 7. 5. 4. 3. 1. 2. Foundation, Foundation, South (WWF). Nature for Africa, Fund Wide World the Marine and (DEAT-MCM) and Coastal Management KZN Wildlife for supporting this project. Special thanks go thanks to Special R. this project. for KZN supporting Wildlife comments valuable C. Taylor, Fox their and A. for We Myeza for assistance. their invaluable reviewers anonymous three thank also Research National the by provided was Funding suggestions. and We We dedicate this article to the Technical Assistant at Ezemvelo memory KZN Wildlife EcoAdvice since of Mr Amos Myeza, 1976. We thank the Park iSimangaliso and Authority Ezemvelo AT 2008, personal communication, August 7; MacKay F 2009, likely are discoveries Similar 24). June communication, personal in nearby Mozambique. to be made in KwaZulu-Natal, such as Nhlabane and Manzimtoti (Forbes http://www.sajs.co.za Salinity and temperaturetolerance of