The effect of thermal pollution on benthic foraminiferal assemblages in the Mediterranean shoreface adjacent to Hadera power plant (Israel)

Marine Pollution Bulletin 62 (2011) 1002–1012

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The effect of thermal pollution on benthic foraminiferal assemblages in the Mediterranean shoreface adjacent to Hadera power plant (Israel) Ruthie Nina Arieli a, Ahuva Almogi-Labin b,⇑, Sigal Abramovich a, Barak Herut c a

Department of Geological and Environmental Sciences, Ben Gurion University, Israel Geological Survey of Israel, Israel c Israel Oceanographic and Limnological Research, Israel b

a r t i c l e

i n f o

Keywords: Thermal pollution SST Living benthic foraminifera Species richness East Mediterranean

a b s t r a c t The thermal pollution patch of Hadera power plant was used as a natural laboratory to evaluate the potential long-term effects of rise in Eastern Mediterranean SST on living benthic foraminifera. Their sensitivity to environmental changes makes foraminifera ideal for this study. Ten monthly sampling campaigns were performed in four stations located along a temperature gradient up to 10 °C from the discharge site of heated seawater to a control station. The SST along this transect varied between 25/ 18 °C in winter and 36/31 °C in summer. A significant negative correlation was found between SST in all stations and benthic foraminiferal abundance, species richness and diversity. The total foraminiferal abundance and species richness was particularly low at the thermally polluted stations especially during summer when SST exceeded 30 °C, but also throughout the entire year. This indicates that thermal pollution has a detrimental effect on benthic foraminifera, irrelevant to the natural seasonal changes in SST. Ó 2011 Elsevier Ltd. All rights reserved.

1. Introduction Over the past several decades public and scientific awareness to global warming has increased significantly. As of today, it is widely accepted that the upper 300 m of the world’s oceans are showing a clear multi-decadal warming signal attributed to increased global temperatures (e.g. Lyman et al., 2010; Trenberth, 2010). A currently accepted forecast for the next two decades is that ocean temperatures will rise at a rate of 0.2 °C per decade (IPCC Report, 2007). As a result, many studies have examined the potential deleterious effect of global warming on the natural environments in general and on marine environments in particular. Over the past 44 years an increase of 1.28 °C has been recorded in the Mediterranean Sea, most of which occurred since the eighties (Stips et al., 2006). The current rate of warming in the Mediterranean Sea, based on satellite data from 1990 to 2006, is 0.067 °C per year (Del Rio Vera et al., 2006). This rate is slightly more than double the current forecast for global warming which stands at 0.028 °C/ year (Stips et al., 2006). Temperature is a major factor in the metabolism of living organisms. It controls chemical reactions which affect the synthesis of enzymes which in turn determine the general state of the organism, including growth rates and reproductive success. Temperature also determines the geographical distribution of most organisms.

⇑ Corresponding author. Tel.: +972 2 5314232; fax: +972 2 5380688. E-mail address: [email protected] (A. Almogi-Labin). 0025-326X/$ - see front matter Ó 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.marpolbul.2011.02.036

The rise in the Mediterranean Sea water temperature due to global warming may give a distinct advantage to tropical invasive species originating from the Indo-Pacific, the Red Sea, and the Atlantic, over the native fauna (Galil and Zenetos, 2002; Sabatés and Lloret, 2006; Bianchi, 2007). In fact, since the opening of the Suez Canal in 1869, a large scale one-way migration began from the Red Sea to the Mediterranean (Por, 1978, 2009, 2010). Several species of benthic foraminifera also took part in this ‘‘Lessepsian Migration’’ as shown in several recent publications (Langer and Hottinger, 2000; Hyams et al., 2002; Hyams-Kaphzan et al., 2008; Langer, 2008). Foraminifera are thought to be the most diverse group of microscopic organisms with a calcareous shell alive today (Sen Gupta, 1999) and they are also prime candidates for studying the effect of anthropogenic pollution on the marine biota. As unicellular organisms with a short reproductive cycle and fast growing rates, they show a quick response to changes in environmental conditions and serve as extremely sensitive indicators of changes in nutrient abundance, salinity, irradiation, oxygen concentration, anthropogenic contaminations as well as temperature fluctuations (e.g. Alve, 1995; Jorissen et al., 1995; Alvarez Zarikian et al., 2000; Saraswat et al., 2004). Most benthic foraminiferal species, especially the larger ones, have minimum thresholds for reproduction (Murray, 2006; Langer and Hottinger, 2000). Bradshaw (1961) showed in laboratory experiments that the upper growth temperature limit for the investigated species of benthic foraminifera is 35 °C and the maximum lethal temperature is 45 °C. The main factors that determine the abundance of benthic foraminifera in

R.N. Arieli et al. / Marine Pollution Bulletin 62 (2011) 1002–1012

Temperature °C

the shallow water of the Mediterranean Sea are food availability, substrate and seasonality. Living benthic foraminiferal assemblages studied off the Mediterranean coast of Israel, at a water depth of 40 m, showed high numerical abundance during the summer and low abundance during the winter months (Jannink, 2001; Hyams-Kaphzan et al., 2009). Species diversity and abundance is the highest at 30–40 m water depths and the lowest at depths of 3–9 m, where the sandy substrate, high water energy and lack of food resources act as limiting factors (Hyams-Kaphzan et al., 2008). Some of Israel’s sandy beaches contain beachrocks adjacent to the coastline that create a line of rocks parallel to the shoreline. These rocks consist of carbonate skeletal fragments and rock fragments bound together by calcium carbonate (Ginsburg, 1953). Beachrocks provide an ideal habitat for benthic foraminifera and for a wide variety of other micro- and macro-organisms including algal mats, seaweeds, crustaceans and molluscs. Though these rocks are known for their rich biomass, increased wave force towards the coastline, may cause stress on the benthic organisms exposed to these harsh conditions (Makrykosta et al., 2006). The surface temperature in the eastern Levantine Basin varies naturally between 18 °C in winter and 30 °C in summer (Fig. 1). During the summer, the Levantine Surface Water (LSW) occupies the upper part of the water column with salinity as high as 39.7 psu and sea surface temperature (SST) of 30 °C which is the warmest SST in the entire Mediterranean Sea (Gertman and Hecht, 2002). This warm and saline seawater, together with extreme oligotrophy (Herut et al., 2000), makes the eastern Levantine basin one of the most sensitive areas to thermal pollution and an ideal location for examining the effect of the rising SST on benthic foraminifera. The Hadera power plant, active since the early eighties, is located in the eastern Levantine basin, on the northern coast of Israel (Fig. 2). Approximately 7800,000 m3 per day of sea water are pumped into the power plant year round in order to cool the turbines and then channeled back into the sea, just south of the power plant’s southern wave breaker (Klein and Lichter, 2006). The water leaving the station is up to 10 °C warmer than the water in the natural environment. This creates a quasi permanent area of unusually high temperatures extending about 1.5 km southward and 1 km westward (Fig. 2). This warm seawater discharge affects the natural seasonal changes in temperature which may have serious ramifications on marine organisms, especially during summer months when the natural water temperature can reach 30 °C. In this study, we have used the thermal pollution of the Hadera power plant (Israel) to evaluate the potential long-term effects of a

32 31 30 29 28 27 26 25 24 23 22 21 20 19 18 17

1003

rise in SST on the living benthic foraminifera. The temperature anomaly around the Hadera power plant, acts in this study as a test case of what is likely to happen to the Mediterranean Sea in the upcoming decades and centuries. It enables us to better understand how the warming of the oceans will affect marine microorganisms in general and foraminifera in particular. The large abundance of foraminifera in the shallow continental shelf of Israel and their high sensitivity to environmental changes makes them an ideal group for this study. 2. Material and methods 2.1. Field work Four sampling stations were chosen along a 1.3 km transect, extending southward the Hadera power plant (Fig. 2 and Table 1). The stations are located along the temperature gradient caused by the thermal pollution originating from the power plant. The sampling took place once a month for the duration of 1 year (February, 2007–December, 2007). The samples were taken from algal mats growing on the beachrocks at a water depth of approximately 1 m. The four sampling stations are located as follows: Station 1 is closest to the hot water source, Station 2 is about 200 m southward and Station 3 is located approximately 500 m south of Station 2. Station 4 is the southernmost station, located approximately 600 m south of Station 3, a little beyond the range of the thermal pollution, and represents the healthy control station. Sampling took place in calm sea conditions with an average wave height of 0.75 m. During each sampling campaign, measurements of temperature, conductivity and pH were taken with WTW microelectrodes. The algal mats along with sediments trapped within them, were sampled in each station in two replicates and one reference sample. The samples were separated from the rocks with a sharp flat knife and placed in plastic sampling containers. The submerged beachrocks were less common at Station 1 compared to the other three Stations 2–4 where the beachrocks create a continuous line parallel to the coast. The algal coverage and sediment content varied between the four sampling stations. The sediment content as well as the algal coverage was relatively low throughout the sampling period at Station 1, low to medium at Station 2 and medium to high at Stations 3 and 4. In order to collect from each station samples of identical volumes the collection time at Stations 1 and 2 was slightly longer than at Stations 3 and 4. The samples were then stained with Rose Bengal solution (2 g l1 ethanol 95%) in order to mark the living organisms in the sample. Representative water and sediment samples were taken from the stations in order to study their chemical composition including rare elements. 2.2. Laboratory work

Hadera 2005, 11.6m depth Satellite Avg.Temp 1

2

3

4

5

6

7

8

9

10

11

12

Month

Fig. 1. Average SST variation on the Israeli continental shelf (Herut et al., 2008; data provided by Dov Rosen, IOLR).

The samples were left in the Rose Bengal and ethanol solution for at least 48 h to ensure coloring of the entire sample. They were then washed and frozen and dried in a freeze drier in order to minimize the adhesiveness of the algae and to free the foraminifera attached to it. After they were dried the samples were weighed and then re-washed over 2 sieves, 63 lm and 1000 lm, in order to separate the sediment from the macroalgae. The separated samples were then frozen, dried and weighed once more. Next, the samples were examined under a stereomicroscope and stained benthic foraminiferal specimens were picked out of the sediment and algae. All stained specimens were collected from each aliquot until a total of 200–300 benthic foraminifera were collected per studied sample. In a few of the samples, the numbers of

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Fig. 2. (A) Location of the study area on the northern coast of Israel, eastern Levantine basin, Eastern Mediterranean. (B) The location of the sampling Stations 1–4 shown on the thermal pollution plume from Hadera Power Plant (Autumn 2007, SST at 0.5 m, modified after Glazer, 2008).

Table 1 The location of the four sampling stations, their distance from the thermal pollution source and the extent of thermal pollution as indicated by the average difference (DT) relative to ambient SST (Station 4). Station

Location

1 2 3 4

32°27.830 N 32°27.660 N 32°27.510 N 32°27.260 N

34°52.990 E 34°52.920 E 34°52.870 E 34°52.790 E

Approximate distance from thermal pollution source (m)

Average DT (relative to ambient SST)

10 200 700 1300

7 ± 2.2 4 ± 1.3 2 ± 0.6 0

living specimens were extremely low and the required minimum of foraminifera was not achieved. These samples were generally collected from Station 1, the closest to the hot water source. The benthic foraminifera collected were of three main shell types, hyaline, agglutinated or porcelaneous. The different groups were considered living under different criteria: foraminifera with hyaline shell – stained red; foraminifera with agglutinated or porcelaneous shell – dark pink to pink shell usually with the aperture stained red. The stained specimens were sorted into genera based on Loeblich and Tappan, 1987 and to species based on Loeblich and Tappan (1987, 1994), Cimerman and Langer (1991), Hottinger et al. (1993), Jones (1994) and Jannink (2001). The foraminifera were counted in order to determine species diversity and numerical abundance in each station. 2.3. Statistical analysis Several ecological indices were used in this study to describe the assemblage composition and its characteristics. The numerical

abundance was estimated by calculating the total number of individuals per gram dry sample. The same was done for each species in order to obtain the assemblage composition. The total species richness was the sum of species observed in both duplicates at each station. The species diversity was calculated according to the Fisher a diversity index (Fisher et al., 1943), that takes into account the sample size which in some cases varied significantly between the samples. In order to establish the degree of similarity between the sampling stations and sampling months, similarity analyses, ANOSIM tests, were performed using the statistical software Primer v6 (PRIMER-E Ltd., Plymouth, UK). The correlation between the SST and the assemblage characteristics was examined through regression tests, as well as by principle component analysis (PCA) preformed on XSTAT software (Addinsoft Inc.). 3. Results and discussion 3.1. Environmental conditions The main environmental factor that varies between the studied stations is the change in sea surface temperatures (SST). SST increases as the distance from the heated water source decreases (Fig. 3). The temperatures measured at Station 1 were significantly higher than the SST at the control station year round, and varied between 36.2 °C in October 2007 and 25.5 °C in April 2007. At Station 2, the temperature varied between 21.8 °C and 35.5 °C and at Station 3 it varied between 20 °C and 32.4 °C. At Station 4, the control station, the temperature varied between a minimum of 18.5 °C in April 2007 and a maximum of 31 °C in August 2007. A similar annual SST range as measured in the control Station 4 was lately

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R.N. Arieli et al. / Marine Pollution Bulletin 62 (2011) 1002–1012

Temperature °C

Station 1

Station 2

Station 3

Station 4

35 30 25 20

# Foraminifera/g

15 200 150 100 50 0

Fisher α

6 4 2

20 15 10 5

Fe b Ap r M ay Ju n Ju l Au g Se p O ct No v De c

Fe b Ap r M ay Ju n Ju l Au g Se p O ct No v De c

Fe b Ap r M ay Ju n Ju l Au g Se p O ct No v De c

0 Fe b Ap r M ay Ju n Ju l Au g Se p O ct No v De c

Species richness

0 25

Fig. 3. The SST, abundance, diversity (Fisher a) and species richness at the 4 sampling stations throughout the sampling period (February–December, 2007).

reported by Herut et al., 2008 for the Israeli coast and was also measured by satellite for the same region (Fig. 1). The temperature gradient was relatively stable during most of the year, with a DT of about 8 °C between Station 1, and the control Station 4. The weakest temperature gradient was in the summer when the DT ranged from 4 °C to 5.6 °C and the strongest gradient was in November with a DT of 10.5 °C (Fig. 4). The total dissolved solids (TDS) and conductivity (e.g. salinity) were relatively stable year round, though somewhat lower in winter, with values of 39,800–42,200 mg l1 and 54–58 mS cm1, respectively. A similar seasonal change in salinity, between 38.2 psu in winter and 40 psu in summer, was also reported lately by Hyams-Kaphzan et al. (2009) 4–5 km to the west of the Israeli coast indicating that this seasonal trend is typical for the inner shelf of Israel. The chemical concentrations of major and trace elements both in sea water and in the sediment were of normal marine values and showed no signs of any anthropogenic pollution. At the four sampling stations the sediment composition was mostly sands with an average sand fraction content (>63 lm) of 92–96% throughout most of the sampling period. An exception was in April 2007 when the fine sediment fraction (<63 lm) increased at Stations 1 and 2 to maximum values of 28.3% ± 2.3%

Fig. 4. Seasonal changes in DT (°C) between Station 1 and the control Station 4 during 2007. The lowest DT was observed in summer.

and 18.7% ± 7.4% respectively. The temporary increase in fines was attributed to winter storms that occurred shortly before the April sampling. The samples collected were composed of macroalgal mats and sandy sediments trapped within them, providing a unique habitat that resembles the rocky environment rather than the common loose-sand environment that is predominant along the Israeli coast (e.g. Einav, 2004; Hyams-Kaphzan et al., 2008). The algal mats covering the beachrocks were composed during most of the year of a complex of two genera, Polysiphonia Greville and Neosiphonia Kim and Lee that were found at all the sampling stations together with one or two additional algae, usually Centroceras Kützing, Ectocarpus Lyngbye or Bangia Lyngbye. The samples collected from October 2007 until December 2007 contained only Bangia. Several other macroalgae, such as Jania Lamouroux, Ulva Linnaeus and Ceramium Roth appeared sporadically in the samples. 3.2. SST vs. foraminiferal abundance and diversity The numerical abundance of foraminifera in Station 4 presenting the natural variability in the submerged beachrocks is characterized by distinct seasonal fluctuations. A similar seasonality was also found in the thermally polluted Stations 1–3 but with considerably lower values (Table 2). Maximum abundance during winter and spring ranged from 56.9 ± 9.4 specimens per g dry sediment at Station 1 to 155.4 ± 26.8 specimens per g dry sediment at Station 4. The lowest numbers were recorded during the summer and autumn with minimum values ranging from of 0.5 ± 0.3 at Station 1 to 21.5 ± 10.2 at Station 4 (Fig. 3 and Table 3). Thus the total numerical abundance at each of the four sampling stations was significantly different from one another at several levels of significance indicating the direct influence of the natural and the artificially elevated SST on the total benthic foraminiferal abundance.

1006 Table 2 The relative abundance of the common benthic foraminifera species comprising >1% of the assemblage in the four studied stations. Raw numbers of foraminifera (average of the two duplicates), species richness (average of the two duplicates) and Fisher a are also shown. 23-Feb-07 Station

Raw No. (avg.) Species richness (avg.) Fisher a (avg.)

5-Apr-07

2

3

1.2

4 3.5

1 1.0

3

1.5

0.4

0.4 12.8 1.2

22.0 0.9 0.4 0.4 0.4 0.4 40.5

36.0

0.4 1.6

0.2 0.2 8.2 2.3 0.5

0.2 16.6 0.5

0.5 2.1 6.9

0.8 0.8 1.4 0.5 3.5 1.5 0.8 0.3 0.5

64.6 7.7

66.7 3.6

37.0 0.5

1.5 17.8 2.3

2.9

0.4 0.9

3.7 0.2

0.5

1.8 2.6 26.4

0.9

3.1 3.1 15.4

1.8

48.2 2.1 7.5

0.3 1.0 36.3 23.3 8.8

3.1

120.0 9.5 2.46

249.0 15.0 3.67

209.0 12.0 2.8

35.5 6.5 2.44

3.1 38.0 1.2 1.9 170.5 10.0 2.53

2.1 2.3

4

1

3.7

1.2

0.7

23-Aug-07 Ammonia parkinsoniana Ammonia sp. 1 Ammonia tepida Bolivina spp. Cornuspira planorbis Cribroelphidium oceanensis Cymbaloporetta sp. 1 Elphidium cf. E. advenum Lachlanella sp. 1 Lachlanella sp. 2 Lobatula lobatula Miliolinella subrotunda Miliolinella sp. 1 Mychostomina revertens

7-May-07

2

1.4 8.7 13.0

12.7 0.5

0.4

4

0.4 0.2

0.9 1.8

1.3

0.8

0.9

0.2

4.0

42.5 1.3 1.3

73.6 9.2

65.5 1.5

49.6 0.9

0.9

0.3 0.5

4.6

8.3 1.0 0.3

0.4 0.1 0.1 15.4 2.2

8.8

1.2

1.3 1.3 26.3

1.4

0.5 0.5 16.9 9.5 5.3

22.0 41.3 13.1

1.3

86.0 7.0 1.94

116.0 12.0 3.64

354.5 10.0 1.92

59.5 8.5 3.3

1.2 0.2 0.4 0.4

2.5

3.5 3.9 4.9 0.2 0.8

8.8

271.5 12.0 2.61

7.3 1.2 0.6 0.6 1.5 7.3 1.2

0.7 0.2 0.2 0.9 1.2 14.3 9.9 11.3

204.0 16.0 4.38

309.5 13.0 2.8

22-Oct-07

0.4 0.8 37.5 6.3

61.1 10.9

0.2 71.7 4.4

4

0.7 0.7

0.7

45.4 3.7

20.5 4.8

21.0 2.8

33.2 1.3

19.8 0.4

8.2

41.3 0.2

68.7

67.8

57.3

68.1

2.1 3.3

3.8 1.3

0.2

0.7

1.3

0.4

3.3 7.1 5.0

2.5 1.3 2.5 0.6 0.6

1.1 0.4 2.8 3.2 0.6

3.6 1.2

2.8 1.4 0.7

1.0 1.3 2.9 0.7

107.5 9.0 2.6

236.0 11.0 2.4

45.0 5.0 1.48

78.5 7.5 2.11

166.5 8.5 1.93

282.0 8.5 1.67

0.2

0.8

2.3

2.2

1.3

37.5

2.9 0.8

6.3 6.3 6.3

0.8 8.5 4.0 3.18

226.0 11.0 2.95

18-Nov-07

66.1 2.5

0.2 0.2 70.7 3.1

1.9 0.2

0.2 55.6 11.1

78.3 17.4

75.9 6.1

0.7 1.5

0.2

2.9 0.2 0.2 61.8 1.8 0.2

40.7 7.4

34.5 6.9

0.4 1.3 8.7 0.6

26-Dec-07

0.5 0.2

53.7 3.7

3

0.2

1.9

43.5

2

1.3

4.3

43.2 4.2

1

0.4

0.5 0.2 0.2 0.7

4

0.4

0.3

0.2 1.7

3

0.2

0.3

2.1 0.5

1.5 66.2 4.8

11-Jul-07

2

1.2

0.2

53.0 4.3

1

1.2

1.6

0.5

74.1 3.7

3

2.5 1.3

19-Sep-07

3.7

14-Jun-07

2

0.4 0.2 0.2

0.7

61.1 9.2

40.7 4.2

0.8 1.4

0.3

2.7

33.3

0.4 16.6 1.0 0.4 0.4

0.4 0.2 1.1 21.6 0.7 0.2

R.N. Arieli et al. / Marine Pollution Bulletin 62 (2011) 1002–1012

Taxa Ammonia parkinsoniana Ammonia sp. 1 Ammonia tepida Bolivina spp. Cornuspira planorbis Cribroelphidium oceanensis Cymbaloporetta sp. 1 Elphidium cf. E. advenum Lachlanella sp. 1 Lachlanella sp. 2 Lobatula lobatula Miliolinella subrotunda Miliolinella sp. 1 Mychostomina revertens Pararotalia spinigera Planorbulina mediterranensis Quinqueloculina incisa Quinqueloculina limbata Quinqueloculina cf. Q. parvula Quinqueloculina seminula Quinqueloculina ungeriana Quinqueloculina sp. 1 Quinqueloculina sp. 2 Rosalina globularis Textularia agglutinans Tretomphalus bulloides

1

1007

260.0 13.0 2.74

1.4

36.0 6.0 2.05 18.5 3.5 1.27 305.5 13.0 2.77 267.0 13.0 2.87 15.0 3.5 1.46 4.5 2.5 2.31 238.5 11.5 2.55 198.0 6.5 1.32 13.5 4.0 2.17 273.5 12.0 2.70 259.0 10.5 2.30 87.5 6.5 1.88

0.7 1.8 2.8 0.9 7.0

13.9 18.3 0.9 3.7

20.5 3.5 1.53 Raw No. (avg.) Species richness (avg.) Fisher a (avg.)

1.3 1.1 2.0 6.4 0.4

4.3 4.3 13.0 0.2 0.2

38.5 8.0 3.83

0.8 0.6 1.1 4.0 1.1 9.3 1.9 5.6 7.4 1.9

13.0 34.8 37.7 0.2 19.8 0.2 0.9

Pararotalia spinigera Planorbulina mediterranensis Quinqueloculina incisa Quinqueloculina limbata Quinqueloculina cf. Q. parvula Quinqueloculina seminula Quinqueloculina ungeriana Quinqueloculina sp. 1 Quinqueloculina sp. 2 Rosalina globularis Textularia agglutinans Tretomphalus bulloides

14.8

2.2 0.7

1.1 0.2

11.1 0.2

23.7

17.2

22.2

11.5 2.5 0.98

0.6 7.1 3.4

227.0 12.0 2.72

13.5 3.5 1.19

3.4 3.4 0.2

0.2

2.5 8.6 4.3 0.7

3.7

48.1 16.8 0.9 5.7 0.2

263.0 8.5 1.69

0.6

0.6 0.4 0.8 0.6 2.1 9.5 0.8 0.8

2.7 32.4

2.7 0.2 0.2

1.4 5.6 2.8 27.8

0.3 1.7 3.7 3.0 0.3

0.6 0.2 0.6 6.0 2.9 3.1

1.7 0.2 0.4 1.1 0.9 8.3 0.7 0.2

57.0 0.2 64.0 26.4 59.5 41.7 0.3 0.2 51.7

12.4

233.5 16.0 3.91

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Table 3 Similarity analysis (ANOSIM) of the abundance of each of the dominant species and of the total foraminiferal numerical abundance in each of the four sampling stations.

Stations Stations Stations Stations Stations Stations

1–2 1–3 1–4 2–3 2–4 3–4

Species abundance significance P

Total abundance significance P

– – 60.1 – 60.01 60.05

60.05 60.005 60.001 60.01 60.001 60.1

The seasonal pattern typical for the submerged beachrocks with highest values recorded in winter and spring, and lowest in summer and autumn, differs from the seasonal pattern observed for foraminifera living 4–5 km to the west of the Israeli coast at 40 m water depth. At these depths the increase in abundance begins in spring and continues into the summer and sometimes early autumn (Jannink, 2001; Hyams-Kaphzan et al., 2009). In these waters there is a clear connection between the increase in chlorophyll a concentration in the top sediment layer, an increase in bottom water temperature and an increase in foraminiferal abundance (Hyams-Kaphzan et al., 2009). The shallow water in the submerged beachrocks is likely to heat up 1–2 months earlier than the water at a depth of 40 m and therefore may enable an earlier microalgal bloom facilitating an earlier peak in foraminiferal abundance. In addition to the distinct seasonality in the numerical abundance of the benthic foraminifera in the healthy station there is a sharp lateral change in the total abundance away from the source of the thermal pollution towards the healthy control station. For example during summer the numerical abundance is low at all the sampling stations and especially in the most thermally polluted Stations 1 and 2 where only a few living specimens were found. At the same time similar numerical abundance values around 50 specimens per g dry sediment occur at Stations 3 and 4. During winter the gradient from the most thermally polluted stations towards the natural healthy station is also distinct with 30% decrease in total numerical abundance at Station 3 and 70% at Stations 1 and 2 compared to the control Station 4. Since the decrease in all stations was extensive it could signify that one cause was responsible for these reductions in total abundances. A most likely cause for this decrease is the natural seasonal variations in SST, especially when considering that other environmental variables such as grain size hardly change between the stations. The shoreface, where the sampling took place, is an already extreme environment, so that in the summer months when the average surface temperature exceeds 30 °C it may become a less than amiable environment for benthic foraminifera. Species diversity (Fisher a) fluctuated throughout the sampling period a between 1 and 4 with no visible pattern (Fig. 3). At the same time species richness shows a distinct gradient from a more diverse community at the healthy station changing notably to a poorly diverse community in the most thermally polluted station. The most distinct gradient occurred during summer and fall when maximum number of species recorded was 22, at Station 4, in December 2007 and the minimum was 3, at Station 2, in October 2007. The relationship between SST of sampling Stations 1–4 and foraminiferal abundance and species diversity was examined by a series of regression tests (Table 4). The species diversity (Fisher a) showed a relatively weak negative correlation to the SST. A significant negative correlation (P 6 0.05) was observed only during 2 months (August and December 2007), and a correlation of a lower significance level (P 6 0.1), was observed in November 2007. In

R.N. Arieli et al. / Marine Pollution Bulletin 62 (2011) 1002–1012

Table 4 Regression analysis of foraminiferal abundance and Fisher a diversity index against the SST of sampling Stations 1–4 throughout the year 2007. Only significance levels of maximum P 6 0.05 and P 6 0.1 were given. Highly significant values are marked in italics. Degrees of freedom (df) for F: df within each month = 7. The ± column indicates positive or negative correlation. Temperature-abundance regression

February April May June July August September October November December

Temperature-diversity regression

R2

F

P

±

R2

F

0.390 0.444 0.540 0.875 0.595 0.915 0.842 0.561 0.582 0.341

3.844 4.794 7.056 41.883 8.813 64.634 31.925 7.675 8.346 3.107

60.1 60.1 60.05 60.001 60.05 60.001 60.001 60.05 60.05

        

0.093 0.051 0.017 0.300 0.019 0.710 0.094 0.000 0.470 0.813

0.617 0.321 0.104 2.574 0.119 14.728 0.625 0.002 5.317 26.164

P

±

A principal component analysis (PCA) was conducted in order to examine the effect of SST on each of the assemblage characteristics (Fig. 5). The PCA plot shows the distribution of the variables in the space formed by the two main components, which explain 83% of the variance. The F1 axis describes 59% of the variance and depicts a negative correlation between SST and abundance, species richness and species diversity. The PCA test clearly showed that all foraminiferal assemblage characteristics are to some degree negatively affected by the raised SST. 3.3. Benthic foraminifera species response to SST variability

60.01



60.1 60.005

 

contrast, between the SST and the foraminiferal abundance, a significant (P 6 0.05) negative correlation was observed in seven of the ten sampling months (May–November 2007) and negative correlations of lower significance levels (P 6 0.1) were observed in February and April 2007. The strongest correlation was in August 2007, indicating that the increase in SST has a negative effect on foraminiferal abundance especially during the warmer months when the natural SST is 28–30 °C. During this period the abundance decreased by 40–95% and SST rose beyond 31 °C. In winter, the abundance decreased by 50–90% when the SST rose beyond 19 °C. This strengthens the observation that the thermal pollution has a negative effect on foraminiferal abundances irrelevant of the time of year. It appears therefore, that each season may have its own temperature threshold, 19 °C in winter and 31 °C in summer, beyond which foraminiferal communities are severely damaged. These temperature thresholds are one degree above the average surface temperature over the shallow continental slope of Israel (18 °C in winter and 30 °C in summer) (Herut et al., 2000, 2008; Hyams-Kaphzan et al., 2009). This may indicate that even a rise as small as 1 °C in SST may have a detrimental effect on certain marine organisms. Station 3 depicts this most clearly since the SST at this station was only 1.5 °C above the natural SST measured at the control Station 4 and its foraminiferal assemblage differed significantly from the control station. One of the negative effects of a significant change in SST, on marine organisms, is reproductive stress. Unusually high or low temperatures can have a significant effect on life cycle length, reproduction and shell growth. A study on several microorganisms including foraminifera recognized temperatures of 33–35 °C as a thermal stress zone in which life cycles are slowed down significantly or uncompleted (Hopper et al., 1973). Studies on the effect of temperature on foraminifera show that there are three critical ranges of temperature which differ among the species. Most species will survive in a relatively large range of temperatures for example Ammonia tepida (Cushman) which is a ubiquitous species and survives at temperatures of 5–35 °C. However, foraminifera will grow within a smaller range and reproduce within an even narrower range of temperatures; A. tepida will grow from 10 to 34 °C and will reproduce only from 18 to 30 °C (Bradshaw, 1961). Within the scope of this research it is not possible to determine specifically which species reached their critical temperatures. It appears however, that in the studied environment, an increase of 1–2 °C relative to the ambient temperature may be enough to cause growth to be extremely retarded or reproduction to cease in several major species, and as a result the foraminiferal abundances decrease significantly.

Thirty-eight benthic foraminifera species were identified in the four sampling stations during the entire sampling period. Twelve of these species were common to all the stations (Table 5). The total number of species observed at each station increased along the sampling transect from north to south, with a minimum of 16 species at Station 1 and a maximum of 32 species at Stations 3 and 4. The majority of the species are epiphytes, as they were collected from algal mats and sandy sediment trapped within. It appears that in this high energy environment with mobile sands epiphytic mode of life has a clear advantage. The benthic foraminifera species in each station were ranked in descending order of relative abundance with the most abundant species plotted first and shown vs. their cumulative relative abundance (Fig. 6). The highest number of species was at the control station (Station 4) and the lowest at Station 1, the closest to the warm water source. In the thermally polluted stations, two or three species made more than 90% of the total assemblage. As a result, the corresponding curves in Fig. 6 have a much shorter asymptotic part than the curves describing the relatively unpolluted stations and during the sampling months in which the numerical abundance was low the plots fail to reach an equilibrium number of species. The thermally polluted stations have a very small number of relatively common species creating a nearly straight line. In contrast, the asymptotic part of the curves describing Station 3 and particularly Station 4, extend to include many relatively rare species that comprise approximately 75%, of the total number of species found in this study and are missing in the other two stations, indicating a healthy environment at least

Variables (axes F1 and F2: 82.27 %) 1

0.75

0.5 Abundance/g

0.25

F2 ( 22 .86 %)

1008

0 No. species

-0.25

SST

-0.5 Diversity (fisher alpha)

-0.75

-1 -1

-0.75

-0.5

-0.25

0

0.25

0.5

0.75

1

F1 (59.41 %) Fig. 5. Principle component analysis (PCA) showing the distribution of the variables analyzed in the space formed by the two main components.

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R.N. Arieli et al. / Marine Pollution Bulletin 62 (2011) 1002–1012 Table 5 List of benthic foraminifera and their distribution in the four studied stations located in the thermal patch, off Hadera Power Plant, during 2007.

Total number of species

+ + +

02/07;05/07

7

8

9

5

02/07;05/07;06/07

40

07/07

60

09/07

04/07

04/07

6

4

80

20 10 11 12 13 14 15 16 17 18 19 20 21 22

40

05/07

11/07

02/07

04/07;12/07

60

06/07;08/07

07/07

80

10/07

Station 3

100

1

Single occurrences are marked by ±.

in the control Station 4. The short tail in Stations 1 and 2 resembles the short asymptotic tail of another station on the Israeli inner shelf that suffers from pollution-induced eutrophy (e.g. Hyams-Kaphzan et al., 2009). The short tail in both cases reflects local stress: reduced oxygenation in the case of the pollutioninduced eutrophic station and SST stress in the case of the thermal patch. The most common benthic foraminifera species were Pararotalia spinigera (Le Calvez), Lachlanella sp. 1, Textularia agglutinans d’Orbigny, Rosalina globularis d’Orbigny, Tretomphalus bulloides d’Orbigny and Lachlanella sp. 2, with maximum average abundances of 72.2, 64.9, 49.4, 41.8, 14.2 and 3.9 foraminifera per g dry sediment respectively. In general, the abundance of these species is highest at the control Station 4, and higher at Station 3 than at Stations 1 and 2 (Fig. 7). The control Station 4 had notably different assemblage composition than at the thermally polluted Stations 1–3. Station 4 was different from Station 1 at significance level of P 6 0.1 and differed from Stations 2 and 3 at significance levels of P 6 0.01 and P 6 0.05 respectively. The three thermally polluted stations did not differ significantly from one another (Table 3). The numerical abundance of the six most common benthic foraminifera showed significant seasonal changes between the four sampling stations (Fig. 7). The abundance of T. agglutinans was highest during winter at Station 4, during winter and autumn

3

4

5

6

7

8

9

10 11 12 13 14 15 16 17 18 19 20 21 22

Station 4

100 80 60

12/07

32

2

02/07

32

± 16

8

11/07

24

+ + +

3

7

05/07;10/07

+

+

+ + + +

2

6

20

+

+ + + + + +

1

5

4

100

+ + + + ± + + + + + + + + + + +

+

3

08/07;09/07

+ +

+ + + + + + +

2

06/07

+ +

+ + + + +

1

04/07

+

20

+ + +

07/07

+ +

+ + + + + + +

+ + + + + + + + + + + + + + ± + + ± + +

40

08/07;12/07

+

+

09/07

+ +

+ + + +

+ ± + +

06/07;07/07

+

4

11/07

+

3

10/07

+

+ + +

10/07;11/07

60

2

Feb Apr May Jun Jul Aug 9 10 11 12 13 14 15 16 17 18 19 Sep20 21 22 Oct Station 2 Nov Dec

08/07;09/07,12/07

Stations 1

Textularia agglutinans d’Orbigny Spiroplectammina earlandi (Parker) Mychostomina revertens (Rhumbler) Cornuspira planorbis Schultze Cycloforina cf. C. rugosa (d’Orbigny) Cycloforina spp. Lachlanella sp. 1 Lachlanella sp. 2 Quinqueloculina cf. Q. bosciana d’Orbigny Quinqueloculina incisa Vella Quinqueloculina laevigata d’Orbigny Quinqueloculina limbata d’Orbigny Quinqueloculina cf. Q. parvula Schlumberger Quinqueloculina seminula (Linnaeus) Quinqueloculina ungeriana d’Orbigny Quinqueloculina sp. 1 Quinqueloculina sp. 2 Miliolinella subrotunda (Montague) Miliolinella sp. 1 Triloculina schreiberiana d’Orbigny Peneroplis planatus (Fitchel and Mall) Bolivina spp. Neoeponides bradyi (Le Calvez) Rosalina globularis d’Orbigny Tretomphalus bulloides d’Orbigny Glabratella crassa Doreen Lobatula lobatula (Walker and Jacob) Planorbulina mediterranensis d’Orbigny Cymbaloporetta sp. 1 Ammonia parkinsoniana (d’Orbigny) Ammonia tepida (Cushman) Ammonia sp. 1 Pararotalia spinigera (Le Calvez) Cribroelphidium oceanensis (d’Orbigny) Elphidium cf. E. advenum (Cushman) Elphidium cf. E. depressulum Cushman Amphistegina lobifera Larsen Unidentified sp. 1

80

% Cumulative relative abundance

Species

Station 1 100

40 20 1

2

3

4

5

6

7

8

9

10 11 12 13 14 15 16 17 18 19 20 21 22

Ranked species in descending order of abundance Fig. 6. Ranking of benthic foraminifera species in descending order of abundance vs. their cumulative relative abundance at Stations 1–4.

at Station 3, and it was nearly absent from Stations 1 and 2 year round. At Stations 1–3 the assemblage composition consisted mainly of Lachlanella sp. 1. This specie was of relatively high abundance year round except for during the winter. Lachlanella sp. 2 had relatively low abundances of 64 specimens per g dry sediment at all the stations year round. At all the sampling stations R. globularis and T. bulloides were most abundant during winter and spring and were absent from the thermally polluted stations during the summer months July–October 2007. The most common species at Stations 2, 4 was P. spinigera which in contrast to the species mentioned above, showed maximum abundances during the summer. The relative abundance of the six most common species showed clear seasonal changes as well as changes along the temperature gradient (Fig. 8). The assemblage was dominated throughout the year by two species in particular Lachlanella sp. 1 and P. spinigera. These species were in high relative abundance at Station 1 during most of the year with the exception of winter when the latter was replaced by R. globularis. At Station 2, Lachlanella sp. 1 was the most common species except in February, July and November 2007 when P. spinigera replaced this species. The same pattern was observed in Station 3 with the exception of February 2007 in which both P. spinigera and Lachlanella sp. 1 were replaced by R. globularis. At the control Station 4, where the ambient SST was undisturbed, T. agglutinans and R. globularis were the most common species in winter and spring while in summer and autumn they were replaced by Lachlanella sp. 1 and P. spinigera. When comparing the assemblage composition at the thermally polluted stations to the control station, it is apparent that at Stations 1–3 80% of the assemblage was comprised of two to three species during most of the year. In the summer however, 90% of the assemblage

R.N. Arieli et al. / Marine Pollution Bulletin 62 (2011) 1002–1012

60

Station 1

Station 2

Station 3

Station 4

40 20 0 120 80 40 0 10 5 0 60 40 20 0 30 20 10 0 100 50

Fe b Ap M r ay Ju n Ju Au l Seg p O c No t v De c

Fe b Ap M r ay Ju n Ju Au l g Se p O ct No v De c

Fe b Ap M r ay Ju n Ju Au l g Se p O c No t Dev c

0 Fe b Ap M r ay Ju n Ju Au l Se g p O c No t Dev c

Pararotalia Tretomphalus spinigera bulloides

Rosalina globularis

Lachlanella Lachlanella Textularia sp. 2 sp. 1 agglutinans

1010

Station 2

Station 3

Fe b Ap M r ay Ju n Ju Au l S eg p O c No t v De c

100

Station 1

Fe b Ap M r ay Ju n Ju Au l Seg p O c No t Dev c

Textularia agglutinans Lachlanella sp. 1

100

Rosalina globularis

100

Lachlanella sp. 2

Fig. 7. Seasonal changes in the numerical abundance (per g dry sediment) of the six most common benthic foraminifera in the four sampling stations along the thermal patch, Hadera Power Plant, 2007.

Station 4

50 0

50 0

50 0 100 50

Pararotalia spinigera

Tretomphalus bulloides

0 100 50 0 100 50

Fe b Ap M r ay Ju n Ju Au l Seg p O c No t v De c

Fe b Ap M r ay Ju n Ju Au l Seg p O c No t Dev c

0

Fig. 8. Seasonal changes in the relative abundance of the six most common benthic foraminifera in the four sampling stations along the thermal patch, Hadera Power Plant, 2007.

R.N. Arieli et al. / Marine Pollution Bulletin 62 (2011) 1002–1012

consisted of only two species. On the other hand, at Station 4 the most common species usually comprised a smaller percentage of the total assemblage. It seems that several species are more sensitive to the SST changes than others. T. agglutinans, T. bulloides and R. globularis, in decreasing order, show the highest sensitivity to raised SST out of the six common species. These species appeared in very low abundances at the thermally polluted stations (Fig. 7). T. agglutinans and T. bulloides were completely absent from Stations 1 and 2 during most of the sampling period and R. globularis also disappeared completely from Station 1 and 2 but only in the summer months. On the other hand the miliolids, Lachlanella sp. 1 and sp. 2 seem to have high tolerance to the elevated SST and even survived the most extreme summer temperatures at the thermally polluted stations. This is in accordance with Murray (1973) who found that miliolids exist in high abundances in the extremely warm lagoons of the Persian Gulf. Among the common species P. spinigera stands out as the only symbiont-bearing species. This species is the most dominant in all the stations including the thermally polluted ones in summer when SST is reaching exceptional high values of 31–36 °C and UV levels are highest. In particular, photic-stress conditions are expected to cause growth inhibition as well as other potential damage to the intercellular algae (Williams and Hallock, 2004). P. spinigera is at present a very common and successful species on the Israeli Mediterranean inner shelf and especially on rocky habitats (Reinhardt et al., 1994; Yanko et al., 1994, 1998; Bresler and Yanko, 1995). However its origin is not clear so far. It was not recorded in western Mediterranean (Cimerman and Langer, 1991) neither in the G. Aqaba (Hottinger et al., 1993) thus it is difficult to know if it a lesspsian invader or an alien from an unknown origin. This species resembles Pararotalia venusta (Brady) that was reported in the Indian Ocean by Cedhagen and Middelfart (1998), and being dispersed by attachment to gastropod veliger shells. High occurrences of T. bulloides and R. globularis in shallow water habitats in the Mediterranean were also documented by Cimerman and Langer (1991), Hyams-Kaphzan et al. (2008) and Frontalini et al. (2009). T. agglutinans is well known from the Gulf of Aqaba (Hottinger et al., 1993) and has also been spotted in the Gulf of Naples by Sgarrella and Moncharmont-Zei (1993) and in the Gulf of Lions by Mojtahid et al. (2009) and therefore though it has not been found in any fossil Holocene record of the Israeli shelf (e.g. Tapiero et al., 2003; Avital et al., 2004; Avnaim-Katav et al., 2010), its origin on the Israeli coast is not yet clear. Lachlanella sp. 1 and Lachlanella sp. 2 both are common on the Israeli inner shelf (Hyams-Kaphzan et al., 2008) but their origin is not clear as they were not recorded further to the west (e.g. Cimerman and Langer, 1991).

4. Conclusions (1) In in situ monthly monitoring of benthic foraminiferal assemblages in the thermal plume south of Hadera Power Plant, Israel, shows that they were negatively affected by the thermal pollution throughout the entire sampling period. (2) In general, the abundance, the species richness and the species diversity all decrease as the SST rises. The total foraminiferal abundance was significantly lower at the thermally polluted stations, especially during the summer, but also throughout the entire year, indicating that the thermal pollution has a detrimental effect on benthic foraminifera, irrelevant to the natural cyclic changes in SST. (3) The drastic decrease in foraminiferal abundances when SST rises above 30 °C, indicates that this temperature maybe a

1011

critical threshold above which foraminifera growth and reproduction are severely retarded. Furthermore, the significant reduction in species richness at high temperatures may signify that these temperatures may be beyond the survival range of several species. (4) The assemblage composition varies along the temperature gradient within the heat patch indicating that some species are better adapted to living in elevated SST than others. For example, T. agglutinans has very low resilience to elevated SST and was completely absent from the most thermally polluted Stations 1 and 2 during most of the sampling period. On the other hand, the miliolids in general, but especially the species Lachlanella sp. 1, seem to be particularly tolerant to increased SST and survive at the most thermally polluted stations even in the most extreme summer conditions. (5) Though the trends were the same in both the thermally polluted stations and the control station, the abundances were significantly higher in the control station. Seasonal changes have a strong effect on foraminiferal abundances, and though the thermal pollution causes a significant decrease in the abundance of the common species it still does not conceal the seasonal changes inherent in these species. Acknowledgments We are grateful for the technical help of M. Kitin from the GSI, and Gily Markado, from BGU for their assistance in field work. Alvaro Israel from IOLR is thanked for identifying the macroalgae that were collected from the sampling stations and Ofer Ovadia from BGU for helping in the statistical analysis. This study represents part of the M.Sc. thesis of the senior author at the Department of Geological and Environmental Sciences at Ben Gurion University of the Negev carried out in collaboration with the GSI and IOLR. We acknowledge funding by Grant No. 038-1727 of the Earth Sciences Board, Ministry of National Infrastructures. Editor C. Sheppard and reviewer G. Schmiedl are thanked for suggestions resulting in a significantly improved manuscript. References Alvarez Zarikian, C.A., Blackwelder, P.L., Hood, T., Nelson, T.A., Featherstone, C., 2000. Ostracods as indicators of natural and anthropogenically induced changes in coastal marine environments. In: Coasts at the Millennium, Proceedings of the 17th International Conference of the Coastal Society, Portland, OR, USA, July 9–12, pp. 896–905. Alve, E., 1995. Benthic foraminiferal responses to estuarine pollution: a review. Journal of Foraminiferal Research 25, 190–203. Avital, A., Almogi-Labin, A., Benjamini, C., 2004. The geological history of inner shelf Quaternary successions from the southeastern Mediterranean. Rapport Commission International Pour l’Exploration Scientifique de la mer Méditerranée 37, 6. Avnaim-Katav, S., Sandler, A., Almogi-Labin, A., Sivan, D., Porat, N., Ron, H., Matmon, A., 2010. Chronostratigraphy and paleoenvironments of Quaternary subsurface successions, southern Haifa Bay. In: Israel Geological Society Annual Meeting, Eilot. Bianchi, C.N., 2007. Biodiversity issues for the forthcoming tropical Mediterranean Sea. Hydrobiologia 580, 7–21. Bradshaw, J.S., 1961. Laboratory experiments on the ecology of foraminifera. Contributions of the Cushman Foundation for Foraminiferal Research 12, 87– 106. Bresler, V., Yanko, V., 1995. Chemical ecology: a new approach to the study of living benthic epiphytic foraminifera. Journal of Foraminiferal Research 25, 267–279. Cedhagen, T., Middelfart, P., 1998. Attachment to gastropod veliger shells – a possible mechanism of dispersal in benthic foraminiferans. Phuket Marine Bilological Center Special Publication 18, 117–122. Cimerman, F., Langer, M.R., 1991. Mediterranean Foraminifera. Academia Scientarium et Aritium Slovenica, Dela, Opera 30, Classis IV: Historia Naturalis. Del Rio Vera, J. et al., 2006. Mediterranean Sea level analysis from 1992 to 2005. Presented at ESA workshop, Venice, Italy. . Einav, R., 2004. Seaweeds of Eastern Mediterranean Coast. Academic Press, Bar-Ilan (Ramat Gan, in Hebrew accepted by Koeltz scientific books to be published in English).

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