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מדינת ישראלSTATE OF ISRAEL מ שרד התשתיות הלאומיותTHE MINISTRY OF NATIONAL INFRASTRUCTURES המדען הראשיOffice of the Chief Scientist Characteristics of benthic foraminifera inhabiting rocky reefs in northern Israeli Mediterranean shelf Orit Hyams-Kaphzan, Lydia Perelis Grossowicz and Ahuva Almogi-Labin The Geological Survey of Israel 20.8.20.4 GSI/36/2014 Report: ES-20-2014

Characteristics of benthic foraminifera inhabiting rocky reefs in

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STATE OF ISRAEL מדינת ישראל

THE MINISTRY OF NATIONAL INFRASTRUCTURES שרד התשתיות הלאומיותמ

Office of the Chief Scientist המדען הראשי

Characteristics of benthic foraminifera

inhabiting rocky reefs in northern Israeli

Mediterranean shelf

Orit Hyams-Kaphzan, Lydia Perelis Grossowicz and

Ahuva Almogi-Labin

The Geological Survey of Israel

20.8.20.4

GSI/36/2014 Report: ES-20-2014

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Page 3: Characteristics of benthic foraminifera inhabiting rocky reefs in

3. Recipient Accession No. 2. 1. Publication No. ES-20-14

5.Publication Date

August, 2014

4.Title: Characteristics of benthic

foraminifera inhabiting rocky reefs in

northern Israeli Mediterranean shelf

6. Performing Organiz. Code

8. Performing Organiz. Rep. No.

GSI/36/2014

7. Author (s) Orit Hyams-Kaphzan, Lydia

Perelis Grossowicz and Ahuva Almogi-Labin

10. Project/ Task / Work Unit No. 9. Performing Organization Name and Address Geological Survey of Israel, Jerusalem 95501

11. Contract No. 212-17-024

13. Type of report and period covered

Final report

12.Sponsoring Organization (s) Name and

Address The Ministry Of Energy and Water Resources

P.O.B. 36148, 9136002 Jerusalem 14. Sponsoring Organiz. Code

15. Supplementary Note: This report is part of a larger research project: חקר וניטור מדף היבשת כבסיס לקבלת החלטות בנושאי פיתוח תשתיות לאומיות כדוגמת איים מלאכותיים

16. Abstract: Hard bottom habitats common in the northern Israeli shelf constitute a highly

diverse marine ecosystem rich in macroalgae and calcareous organisms. This ecosystem suffered

during the last few decades from continuous disturbance due to anthropogenic intervention. In

order to tackle this complex ecosystem we initiated a pilot study in collaboration with IOLR,

with focus on several key faunal groups. Benthic foraminifera, known to be sensitive indicators

of this ecosystem were sampled from the rocky reefs of Akhziv (AK) and Carmel Head (CH) by

scuba diving. Different macroalgae species accommodating the live epiphytic benthic

foraminifera were sampled twice a year at AK and in each season at CH in 3 depth intervals

between 5-20 m, during 2013-4. The numerical abundance of the group ranges between 170-

3500 #/10cc (wet macroalgae volume) without any significant difference in standing stocks

within regions, water depths or macroalgae preference. In total 77 benthic foraminifera species

were identified, 71 in CH and only 43 at AK. Species richness per site varied between 3 and 42

with higher values at CH. 25% of all species were aliens, mostly Lessepsian, and comprise on

average 70% - 84% of the numerical abundance of AK and CH respectively. Cluster analysis

using benthic foraminifera relative abundance data did not correlate with the different

macroalgae species, water depths or seasonality, indicating that the foraminiferal community in

the two regions is quite homogenous. Amphistegina lobifera a Lessepsian migrant is by far the

most common species on the Israeli rocky reefs occurring in all samples and comprising 18-93%

of the foraminiferal community. Textularia agglutinans another common species occurs in

higher numbers in AK while Pararotalia calcariformata is more restricted to the CH region. In

some CH sites this species predominate the assemblage, indicating the adjustment of this species

to deeper water niches. This study indicates that Israeli rocky reefs represent a dynamic

ecosystem prone to rapid changes that needs to be monitored regularly.

17. Keywords: Benthic foraminifera, Rocky reefs, Mediterranean, alien species מינים מהגרים, ים תיכון, שוניות סלעיות, בנתוניים פורמיניפרה

20. Security Class 19. Security Class 18. Availability Statement

22. Price 21. 32 Pages

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Abstract

Hard bottom habitats common in the northern Israeli shelf constitute a highly diverse

marine ecosystem rich in macroalgae and calcareous organisms. This ecosystem suffered

during the last few decades from continuous disturbance due to anthropogenic

intervention. In order to tackle this complex ecosystem we initiated a pilot study in

collaboration with IOLR, with focus on several key faunal groups. Benthic foraminifera,

known to be sensitive indicators of this ecosystem were sampled from the rocky reefs of

Akhziv (AK) and Carmel Head (CH) by scuba diving. Different macroalgae species

accommodating the live epiphytic benthic foraminifera were sampled twice a year at AK

and in each season at CH in 3 depth intervals between 5-20 m, during 2013-4. The

numerical abundance of the group ranges between 170-3500 #/10cc (wet macroalgae

volume) without any significant difference in standing stocks within regions, water

depths or macroalgae preference. In total 77 benthic foraminifera species were identified,

71 in CH and only 43 at AK. Species richness per site varied between 3 and 42 with

higher values at CH. 25% of all species were aliens, mostly Lessepsian, and comprise on

average 70% - 84% of the numerical abundance of AK and CH respectively. Cluster

analysis using benthic foraminifera relative abundance data did not correlate with the

different macroalgae species, water depths or seasonality, indicating that the

foraminiferal community in the two regions is quite homogenous. Amphistegina lobifera

a Lessepsian migrant is by far the most common species on the Israeli rocky reefs

occurring in all samples and comprising 18-93% of the foraminiferal community.

Textularia agglutinans another common species occurs in higher numbers in AK while

Pararotalia calcariformata is more restricted to the CH region. In some CH sites this

species predominate the assemblage, indicating the adjustment of this species to deeper

water niches. This study indicates that Israeli rocky reefs represent a dynamic ecosystem

prone to rapid changes that needs to be regularly monitored.

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1. Introduction

1.1 Background

Hard bottom habitats are distributed along the Mediterranean Israeli coast from zero

down to ~100 m depth being more abundant in the northern part of the Israeli shelf

(Almagor and Hall, 1984). This marine ecosystem is highly diverse, unlike the more

common sandy soft sediment habitat, resembling in its wealth low latitudes rocky reefs

(Rilov, 2014). For many of the Mediterranean and the Atlantic-Mediterranean species the

Israeli coast represents the eastern end of distribution. In addition this region, and mainly

the rocky habitat is affected badly by invasive species that spread from the Red Sea via

the Suez Canal into our coasts and alter the community structure (Hyams et al., 2002,

Hyams-Kaphzan et al., 2008; Rilov and Galil, 2009). This complex habitat, rich in

macroalgae, micro- and macrofauna and fish is also one of the most vulnerable

ecosystems along the Israeli coast that might be affected by the rapid increase in sea

surface temperature (SST), salinity (SSS) and changes in the trophic levels (Herut et al.,

2000; Gertman and Hecht, 2002). So far, little attention was given to study this unique

and complex ecosystem. In order to be able to detect and follow changes that result from

natural variability in space and time and compared it to changes caused by anthropogenic

contamination we initiated this study on the characteristics of the foraminiferal group, an

important component of the hard bottom ecosystem of the Israeli coast (Hyams-Kaphzan

et al., 2008; Gruber, 2006; Lazar, 2007). This study, carried out in collaboration with Gil

Rilov from IOLR, is an extensive effort to establish an ecological baseline and test a

possible monitoring program of this important ecosystem. In this study the distribution of

living benthic foraminifera was investigated in two rocky regions, in different seasons,

water depths and on different macroalgae species, in order to capture the full numerical

abundance range and species diversity and assemblage composition in this highly

variable and complex ecosystem.

1.2 Benthic foraminifera

Benthic foraminifera are known as the most diverse group of microscopic organisms with

calcareous or agglutinated shell alive today (Sen Gupta, 1999). As unicellular organisms

with short reproductive cycle and fast growing rates, they show a quick response to

changes in environmental conditions and serve therefore as extremely sensitive indicators

of environmental changes due to anthropogenic contaminations and SST rise (e.g. Alve,

1995; Jorissen et al., 1995; Hyams-Kaphzan et al., 2009; Arieli et al., 2011). The main

factors determining the abundance of benthic foraminifera in the shallow water of the

Israeli Mediterranean Sea are food availability, substrate type and seasonality (Gruber,

2006; Hyams-Kaphzan et al., 2008, 2009; Arieli et al., 2011). Species diversity and

abundance is the highest at 30–40 m water depths, mainly in the carbonate-rich substrate

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(including hard substrate) and on macroalgae of the subtidal zone. The lowest values

were encountered at depths of 3–9 m, in sandy substrate where high wave energy and

lack of food resources act as limiting factors (Hyams-Kaphzan et al., 2008). In the past,

Gruber (2006) and Arieli et al. (2011) studied foraminifera living on rocky habitats of

less than 2 m water depth. These foraminifera were epiphytic, living on different

macroalgae species. “Time-averaged” death assemblages, of rocky reefs were studied

between 6-30 m water depth by Hyams et al. (2002), Lazar (2007), Hyams-Kaphzan et al.

(2008), and Avnaim-Katav et al. (2013). An important group of foraminifera that lives on

the rocky substrates off Dado and Akhziv coasts (northern Israel), are the larger

endosymbiont bearing foraminifera (LBF). Eleven species of LBF, known to inhabit

tropical/subtropical shallow water habitats occur there. Some of them are natives (Avital,

2002; Lazar, 2007) but most arrived from regions with warm winter temperatures,

extreme oligotrophic condition, and deep light penetration. Most of the alien species

migrated from the Red Sea via the Suez Canal and are known as Lessepsians invaders.

Others may reach this region by ballast water (Hyams et al., 2002; Hyams-Kaphzan et al.,

2008, 2014; Arieli et al., 2011; Zenetos et al., 2012; Avnaim-Katav et al., 2013).

2. Material and methods

2.1 Field work

Macroalgae samples were collected for studying the foraminifera from two regions on the

northern coast of Israel (Fig. 1): Carmel Head (CH) and Akhziv (AK). At each region

samples were collected at three water depth intervals: very shallow (VS, 2-6 m), shallow

(SH, 6-12 m) and intermediate (I, 12-20 m), as a part of the rocky reef benthic

community survey (Rilov, 2014). Samples were taken during summer, winter, fall and

spring 2013-2014 in CH, and during spring and fall 2013 in AK (Table 1). In order to

monitor the effect of the marine protected area (MPA) on the foraminiferal community at

the AK region (where the MPA exists for the last decade) samples were collected from

inside the Nature Reserve at Sahaf (SF) and Nahlieli (NL) islets, and outside the Nature

Reserve at Akhziv (AK) and Segavion (SG) islets at three different water depths (Table

1). In both regions, AK and CH the sampling sites were decided according to logistic

constrains and sea conditions. SCUBA divers using a 250 ml receptacle, 10 x 10 cm

quadrate and a knife collected the samples. Macroalgal collection was based on two

criteria: 1. Macroalgae with complex morphology previously found to contain large

numbers of foraminifera. 2. Macroalgae that visually looked as containing large numbers

of foraminifera (Table 1). Once a macroalgae species was chosen for collection, a diver

would place the receptacle over an attached, intact living fragment, and cut its’ holdfast

or stem from the bottom, re-suspending as little foraminifera as possible. For each site,

triplicates were collected. In AK, in two occasions, five replicates were sampled per site

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and in few other cases, only a single sample was taken (Table 1). Samples were brought

to IOLR lab and kept in -20 oC freezer.

Fig. 1. A. Study areas shown on the bathymetric, multibeam map of Sade et al. (2006).

The areas Akhziv (AK) and Carmel Head (CH) are marked by yellow ovals. Locations of

study sites are shown at right top map for Akhziv and at the bottom map for Carmel

Head.

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2.2 Laboratory work

At the Geological Survey micropaleontology lab, the volume of the wet macroalgae

sampled for this project (Table 1) was determined following the procedure suggested by

FOBIMO for determining volume of irregular sediment surface (Schönfeld et al., 2012).

Table 1. List of sites, dates, replicate numbers and macroalgae sampled for foraminifera

from rocky habitats at Akhziv (AK) and Carmel Head (CH), northern Israel. Sample

name contains site name and often water depth (at Akhziv) or macroalgae and sampling

season initial (at CH).

Sampling date Station

Qd (replicate

numbers)

Water Depth

(m) long (E) lat (N) Macroalgae Phylum

Akhziv

8.5.13 NL-VS 5 5 035˚05'38.3" 33˚04'16.7" Dictyota sp. OCHROPHYTA

12.5.13 NL-SH 1, 2, 3, 4, 5 8 035˚05'35.5" 33˚04'16.3" Jania rubens RHODOPHYTA

14.8.13 SF-VS 1, 2, 3 4 035˚05'39.1" 33˚04'28.3" Jania rubens RHODOPHYTA

14.8.13 SF-SH 1, 2, 3 11 035˚05'36.1" 33˚04'28.8" Turf

14.8.13 AK-VS 1, 2, 3 5 035˚05'08.1" 33˚02'46.1" Turf

14.8.13 AK-SH 1, 2, 3 10 035˚05'06.6" 33˚02'48.9" Turf

12.5.13 AK-I 1, 2, 3, 4, 5 15.5 035˚04'54.3" 33˚02'44.2" Jania rubens RHODOPHYTA

19.11.13 SG-VS 1, 2, 3 4 035˚04'55.3" 33˚02'31.2" Laurencia sp. RHODOPHYTA

19.11.13 SG-SH 1, 2, 3 9 035˚04'52.5" 33˚02'33.4" Laurencia sp. RHODOPHYTA

19.11.13 SG-I 1, 2, 3 18 035˚04'50.1" 33˚02'36.7" Laurencia sp. RHODOPHYTA

Carmel Head

15.8.13 SK-2 L- SM 1, 2, 3 13 034˚56'35.1" 32˚49'23.6" Laurencia sp. RHODOPHYTA

15.8.13 SP-1 G 1, 2, 3 20 034˚58'05.5" 32˚50'59.6" Galaxaura rugosa RHODOPHYTA

21.8.13 SP-1 T C 19 034˚58'05.5" 32˚50'59.6" Turf

21.8.13 SP-1 L-SM 8, 10, 11 19 034˚58'05.5" 32˚50'59.6" Laurencia sp. RHODOPHYTA

21.8.13 SK-2 G SM 2, 3, 12 11 034˚56'35.1" 32˚49'23.6" Galaxaura rugosa RHODOPHYTA

21.8.13 SK-2 T B 11 034˚56'35.1" 32˚49'23.6" Turf

21.8.13 RD-3 5, 7, 16 7 034°56'39.43" 32°50'27.65" Jania rubens RHODOPHYTA

15.10.13 SK-2 G F 1, 2, 5 12 034˚56'35.1" 32˚49'23.6" Galaxaura rugosa RHODOPHYTA

15.10.13 SP-1 C 3 20 034˚58'05.5" 32˚50'59.6" Codium sp. CHLOROPHYTA

15.10.13 SP-1 L-F 5 20 034˚58'05.5" 32˚50'59.6" Laurencia sp.

16.10.13 RD-1 J 1, 2, 3 7 034˚56'43.7" 32˚50'37.1" Jania rubens RHODOPHYTA

20.11.13 NS-9 1, 2, 3 12 034˚57'03.5" 32˚50'59.4" Laurencia sp. RHODOPHYTA

21.11.13 SK-5 1, 2, 3 2.2 034˚57'12.2" 32˚48'53.4" Galaxaura rugosa RHODOPHYTA

03.03.14 RD-1 H 1, 2, 3 7 034˚56'43.7" 32˚50'37.1" Halopteris scoparia OCHROPHYTA

04.03.14 SK-2 G W 1, 2, 3 12 034˚56'35.1" 32˚49'23.6" Galaxaura rugosa RHODOPHYTA

09.03.14 SP-1 H 1, 2, 3 18 034˚58'05.5" 32˚50'59.6" Halopteris scoparia OCHROPHYTA

Akhziv (AK): SF- Sahaf; NL = Nahlieli; AK- Akhziv; SF - Segavion; VS = 2-6 m; SH = 6-12 m; I = 12-20 m

Carmel Head (CH): SP-1 = Spartan - northern side of Carmel Head; NS-9 = Carmel Head itself; RD = Ridge - south side of Carmel Head;

SK = Shikmona (aprox. 1 mile from shore)

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The Rose-Bengal stained samples (with 2 g/l ethanol 95%) were left in the solution for

two weeks, following FOBIMO recommendation (Schönfeld et al., 2012), to ensure

coloring of the entire sample. The macroalgae were than washed over a 63 µm sieve, in

order to separate the foraminifera from the macroalgae and then the samples were dried at

room temperature. Next, the samples were examined under a stereomicroscope and only

living (stained) benthic foraminiferal specimens were picked out of the sample from the

>150 μm fraction, following previous studies in the region (Hyams et al., 2002, 2014;

Gruber, 2006; Hyams-Kaphzan et al., 2008). All stained specimens were collected either

from the entire sample or in case of split sample they were picked and counted from the

entire split. All counted foraminifera were stored in micropaleontological slides. The

stained specimens were sorted into genera based on Loeblich and Tappan (1987) and into

species level based on Sgarrella and Moncharmont Zei (1993), Loeblich and Tappan

(1987, 1994), Cimerman and Langer (1991), Hottinger et al. (1993) and Milker and

Schmiedl (2012). Foraminifera were counted in order to determine species richness and

numerical abundance (expressed as #/10 cc wet macroalgae volume) in each sample as

well as diversity indices and species evenness. Pooling of the triplicate (or other

duplication) samples (Table 1) yielded a more extended species database that

characterizes more the specific sites that were investigated.

Macroalgae containing benthic foraminifera were collected from 10 sampling sites at

Akhziv (AK), mainly in spring and summer and 14 sites at Carmel Head /Shikmona (CH)

during summer, fall and winter (Table 1). Generally, in each site only one type of

macroalgae was sampled but in several occasions up to 3 different macroalgae were

sampled at the same site, e.g., the case of the summer sampling at CH site SK-2.

Galaxaura rugosa (G) and Halopteris scoparia (H) (= Stypocaulon scoparium) were

sampled only at CH, but Jania rubens (J), Laurencia sp. (L) and Turf (T) were sampled

both in CH and AK. The sampling of the macroalgae depended on their seasonal growth

period and temporal occurrence, as shown by Rilov (2014).

A multivariate analysis was conducted using the package PRIMER v.6 of the Plymouth

Marine Laboratory, specifically in order to find groups of samples (sites), according to

their foraminiferal species abundances and other ecological variables. Cluster Analysis

dendograms were based on the Bray-Curtis similarity coefficient (Clarke and Warwick,

1994). Samples were clustered based on species relative abundances with no

transformation or with log(X+1) transformation. Significance of cluster branching was

tested using the SIMPROF test. The motivation of the analysis was to check the

similarity among the two main studied area regarding seasonality, macroalgae species,

water depths plotted as nMDS and most common foraminifera species distribution

pattern (PCA).

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3. Results and discussion

3.1 General characteristics of the benthic foraminiferal community

Benthic foraminifera are living on the rocky Mediterranean Israeli reefs in variable

numbers as shown previously (Hyams et al., 2002; Gruber, 2006; Gruber et al., 2007;

Hyams-Kaphzan et al., 2008; Arieli et al., 2011; Avnaim-Katav et al., 2013). In this

study, species richness varies considerably, being the highest at Carmel Head (CH) with

39-42 species per site, in winter samples SK-2 and SP-1 (Fig. 2, Table 2). Species

richness values exceeding 20 occur at CH also in summer and in fall, regardless of

sample size. At Akhziv (AK) species richness is higher in summer than in fall with max.

23-25 species occurring at SF sites in summer compared to max. of 14 at SG in fall (Figs.

2-5, Table 1). The lowest species richness occurred in CH site SP-1 and at AK area SG

site in fall and at CH site SK-2 in summer with 5 species per site.

Fig. 2. Species richness (S) at Akhziv islets (left) and Carmel Head (right), shown on

bathymetric, multibeam map of Sade et al. (2006).

Seasonality does not influence the highly variable numerical abundance. High numbers

occur at CH site SP-1 with 3500 #/10 cc in summer and 2900 #/10 cc in winter. The

lowest values occurred at RD-3 site with 175 #/10 cc in summer (Figs. 3-5; Table 2). At

AK site SG-SH 1650 #/10 cc occur in fall and 170 #/10cc in SF-VS site in summer.

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Table 2. Diversity indices (S = richness, N = total abundance/10 cc wet macroalgae; d=

Margalef species richness index; J’ = Pielou evenness index, Fisher = Fisher's ɑ diversity,

and Dominance) of living foraminifera for all sites (see Fig. 3).

Sites Depth Season S N d J' Fisher Dominance

Akhziv

NL-VS VS SP 6 0.739 0.403 0.869 0.70

NL-SH SH SP 7 0.684 0.151 0.775 0.93

SF-VS VS SM 25 169 3.814 0.612 5.419 0.36

SF-SH SH SM 23 750 2.673 0.476 3.263 0.50

AK-VS VS SM 12 741 1.230 0.415 1.394 0.54

AK-SH SH SM 18 574 2.010 0.447 2.370 0.70

AK-I I SP 13 1.377 0.173 1.573 0.91

SG-VS VS F 5 657 0.535 0.428 0.629 0.69

SG-SH SH F 3 1658 0.252 0.525 0.332 0.78

SG-I I F 14 376 2.157 0.331 2.798 0.77

Carmel Head / Shikmona

SK-2-L SM SH SM 8 170 1.212 0.323 1.485 0.85

SP-1 G I SM 10 724 1.206 0.232 1.404 0.89

SP-1 T I SM 8 3468 0.858 0.205 0.977 0.93

SP-1 L-SM I SM 13 1303 1.761 0.285 2.147 0.82

SK-2 G SM SH SM 21 434 2.709 0.332 3.411 0.75

SK-2 T SH SM 5 970 0.582 0.161 0.690 0.95

RD-3 VS SM 15 147 2.045 0.791 2.534 0.25

SK-2 G F SH F 25 175 3.375 0.290 4.446 0.79

SP-1 C I F 4 339 0.509 0.481 0.629 0.86

SP-1 L-F I F 5 245 0.749 0.334 0.922 0.73

RD-1 J SH F 11 400 1.274 0.370 1.474 0.67

NS-9 SH F 12 671 1.576 0.333 1.892 0.78

SK-5 VS F 12 1609 1.215 0.559 1.374 0.44

RD-1 H SH W 29 412 3.398 0.347 4.271 0.63

SK-2 G W SH W 42 461 4.718 0.303 6.102 0.66

SP-1 H I W 39 2914 4.069 0.227 5.053 0.84

vs = 2- 6 m; SH = 6-12 m; I = 12-20 m; SP=Spring, SM= Summer; F=Fall; W = Winter

Akhziv: In red - sites located within the Nature Reserve, in black, outside the reserve

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Fig. 3. Species richness (S), Numerical abundance (N #/10cc), Margalef species richness

index (d), Pielou evenness index (J’) and Dominance values (0-1) of Carmel Head and

Akhziv sites (see Table 2).

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The Margalef diversity index d is a measure of diversity that takes into account the

number of species and the abundance of each species. Seasonality does not influence the

diversity of the group in both regions. The highest values, > 3, were encountered at four

CH sites in winter and in fall. At AK it was recorded in summer. The lowest values at CH

occur in summer and fall and at AK in spring, summer and fall (Fig. 4, Table 2).

Fig. 4. Margalef diversity index (d) at Akhziv (left) and Carmel Head (right) shown on

bathymetric, multibeam map of Sade et al. (2006).

Pielou's evenness J’ index, varying between 0 and 1, expresses how uniformly

individuals are distributed among the different species and thus the extent to which the

community is dominated by a small number of species. The higher the J’ is, the more

even are the species distributed. The highest evenness values of 0.79 and 0.61 were found

in CH site RD-3 and AK site SF-VS in summer (Figs. 4-5, Table 2). Low values, ≤0.2

were found at CH sites SK-2 and SP-1, in summer, on Turf, and in AK sites NL-SH and

AK-I in spring, on Jania, indicating that seasonality as well as water depth or macroalgae

type do not influence evenness values.

In those sites that J' evenness index is the lowest the percentage of the most common

species (Dominance, Figs. 3, 6, Table 2) exceeds 90%. In many sites, the most common

species comprise 60-90% of the assemblage. Often the most common species is

Amphistegina lobifera, a Lessepsian invasive species. The lowest dominance occurred at

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CH site RD-3 with the most abundant species comprising only 25% of the community.

This site was poor in foraminifera and often differed from all other CH sites.

Fig. 5. Pielou's evenness J’ index at Akhziv (left) and Carmel Head (right), shown on

bathymetric, multibeam map of Sade et al. (2006).

The cumulative relative abundance, of all species with the most abundant species plotted

first, then each in decreasing order of abundance, in all studied sites, is shown in Fig. 6.

The dominance (Table 2, Figs. 3, 6) varies between 25% and 95% at AK and CH

regardless of water depth or macroalgae type and generally with first ranking species

being A. lobifera. The long tail appearing in many samples results from the large number

of rare species especially in CH sites. The lowest dominance, ≤50% occurs in summer.

Fig. 6. Cumulative relative abundance against

species abundance rank for all samples.

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3.2 The benthic foraminiferal community composition

77 foraminiferal species were identified: 2 agglutinants, 50 miliolids and 25 hyaline

species (Table 3). Nearly 30% of the miliolids were identified only up to the genus level.

The high species richness of this group in the southeastern Mediterranean exceeds other

parts of the Mediterranean and rareness of some of these species contributes to the partial

knowledge of this group in the Levantine Basin (cf. Cimerman and Langer, 1991; Hyams,

2000; Milker and Schmiedl, 2012).

Table 3. List of living benthic foraminifera occurring at Carmel Head and Akhziv.

Number of occurrences per site, at three water depths categories is given together with

taxa biogeographical affiliation. Alien species are highlighted.

Foraminifera taxa Atlantic Indo-Pacific

< 6 m 6-12 m >12 m < 6 m 6-12 m >12 m

Agglutinants

Textularia agglutinans (d'Orbigny, 1839) 5 17 15 10 14 8 X X

Trochammina inflata (Montagu, 1808) 1

Miliolids

Adelosina partschi (d'Orbigny, 1846) 1 X

Adelosina pulchella (d'Orbigny, 1826) 1 X

Affinetrina planciana (d'Orbigny, 1839) 6 1 1 X

Affinetrina sp. 1

Amphisorus hemprichii Ehrenberg, 1839* 1 X

Coscinospira hemprichii Ehrenberg, 1839* 1 X

Cycloforina cf. C. contorta (d'Orbigny, 1839) 2 X X

Cycloforina quinquecarinata (Collins, 1958) 2 X

Cycloforina sp. 2

Flintinoides labiosa (d'Orbigny, 1839) 1 1 X ?

Hauerina diversa Cushman, 1946 3 7 1 2 3 2 X

Lachlanella sp. 1 (=scans) 4 6 1 1 2

Miliolinella elongata Kruit, 1955 1 X

Miliolinella subrotunda (Montagu, 1803) 1 6 4 3 5 6 X X

Miliolinella spp. 4 2 2 4 3

Peneroplis pertusus (Forskål, 1775)* 4 1 5 5 X X

Peneroplis planatus (Fichtel & Moll, 1798)* 1 2 4 8 X X

Peneroplis cf. P. Planatus* 2 2

Pseudoschlumbergerina ovata (Sidebottom, 1904) 6 1 1 X

Pyrgo denticulata (Brady, 1884) 1 1 1 X X

Pyrgo striolata (Brady, 1884) 1 X

Quinqueloculina berthelotiana d'Orbigny, 1839  1 1 X

Quinqueloculina cf. Q. bradyana Cushman, 1917 1 4 2 5 1 X

Quinqueloculina compressiostoma Zheng, 1988 1 X

Quinqueloculina crassicarinata Collins, 1958 1 X

Quinqueloculina lamarckiana d'Orbigny, 1839 1 X

Quinqueloculina cf Q. mosharrafai Said, 1949 1 1 X

Quinqueloculina cf. Q. neapolitana Sgarrella &

Moncharmont Zei, 1993 1 1 X

Quinqueloculina oblonga (Montagu, 1803) 1 1 X X

provenance

Carmel Head Akhziv

1 = no. of occurrences out of the 72 studied samples; * symbiont- bearing species

Page 18: Characteristics of benthic foraminifera inhabiting rocky reefs in

14

Table 3. (cont.)

Foraminifera taxa Atlantic Indo-Pacific

< 6 m 6-12 m >12 m < 5 m 6-12 m >12 m

Quinqueloculina parvula Schlumberger, 1894 1 2 X

Quinqueloculina pygmaea Reuss, 1850 1 2 X X

Quinqueloculina seminula (Linnaeus, 1758) 1 2 X

Quinqueloculina stelligera Schlumberger, 1893 2 2 X

Quinqueloculina ungeriana d' Orbigny, 1846 2 2 1 X

Quinqueloculina viennensis Le Calvez & Le

Calvez, 1958 2 2 1 X

Quinqueloculina sp. 1 2 2 1

Quinqueloculina sp. 2 2 2

Quinqueloculina sp. 3 1

Quinqueloculina sp. 4 1

Quinqueloculina sp. 5 1

Quinqueloculina sp. 6 1

Sigmamiliolinella australis (Parr, 1932) 2 6 6 3 ? X

Sigmoilina costata Schlumberger, 1893 5 3 X

Siphonaperta distorqueata (Cushman, 1954) 9 X

Sorites orbiculus (Forskål, 1775)* 2 10 5 5 1 X X

Spiroloculina antillarum d'Orbigny, 1839 5 3 2 X X

Triloculina hybrida (Terquem, 1878) 3 6

Triloculina schreiberiana d'Orbigny, 1839 6 3 1 X

Triloculinella dilatata (d'Orbigny, 1839) 10 3 2 1 3 X

Varidentella sp. 5 3 1

Hyalines

Ammonia parkinsoniana (d'Orbigny, 1839) 1 5 3 X

Amphistegina lobifera Larsen, 1976* 6 19 15 10 14 8 X

Asterigerinata mamilla (Williamson, 1858) 5 X

Bolivina variabilis (Williamson, 1858) 4 X X

Cancris auriculus ? (Fichtel & Moll, 1798) 6 1 X X

Cibicides sp. 1 6 2

Conorbella pulvinata (Brady, 1884) 6 1 1 ? X

Cymbaloporetta sp. 8 6 1 1

Discorbis vilardeboanus (d'Orbigny, 1839) 2 1 3 X

Epistomaroides punctulata (d'Orbigny, 1826) 6 1 4 1 X

Heterostegina depressa d'Orbigny, 1826* 8 6 1 5 4 ? X

Lenticulina cultrata (Montfort, 1808) 1 X

Lobatula lobatula (Walker & Jacob, 1798) 1 1 1 1 X X

Neoconorbina sp. 1 1 1

Neoconorbina sp. 2 1

Planorbulina mediterranensis d'Orbigny, 1826 5 9 9 5 4 2 X ?

Planorbulina variabilis (d'Orbigny, 1826) 1 1 X

Pararotalia calcariformata McCulloch 1977* 6 15 10 3 1 1 X

Reussella spinulosa (Reuss, 1850) 3 4 ? X

Rosalina bradyi (Cushman, 1915) 2 1 X X

Rosalina floridana (Cushman, 1922) 2 1 3 X

Rosalina globularis (d'Orbigny, 1826) 4 8 1 4 2 X X

Rosalina macropora (Hofker, 1951) 1 1 X

Spirilina vivipara Ehrenberg 1843 1 X

Tretomphalus bulloides (d'Orbigny, 1839) 3 6 12 5 4 X X

1 = no. of occurrences out of the 72 studied samples; * symbiont- bearing species

provenance

Carmel Head Akhziv

Page 19: Characteristics of benthic foraminifera inhabiting rocky reefs in

15

Table 4. The relative abundance of the most common species comprising ≥3% of the

community in at least one site and the total numerical abundance per 10 cc. In blue AK

and in black CH sites.

The high number of miliolids species and the very low number of agglutinants agrees

with Hyams-Kaphzan et al. (2008) and Arieli et al. (2011) previous observations on the

community structure along the Israeli shelf. Out of the 31 species known to occur in the

Indo-Pacific province only 19 are aliens (marked with gray background in Table 3) and

many of them are considered as Lessepsians, entering the southeastern Mediterranean via

the Suez Canal (Hyams et al., 2002; Zenetos et al., 2010, 2012). 14 rare species, with a

single occurrence during the entire sampling period were found at CH, compared with

only 4 at AK. The sporadic occurrence of rare species more often in CH follows also the

general higher species richness in this region with 71 species (Figs. 2-3; Tables 1-2) at

Carmel Head (max. on Galaxaura) and 43 in Akhziv (max. on Jania; max. inside Nature

Reserve). The alien species comprise only a quarter of the foraminiferal community

species richness but they occur frequently in the rocky habitats. Amphistegina lobifera,

for example, is the most frequently occurring species in all studied sites (Table 4). Other

Sites T. a

gg

lutin

an

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L. "s

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M. su

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Milio

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P. p

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P. p

lan

atu

s

Q. cf. L

. b

rad

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na

S. a

ustr

alis

A. lo

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P. m

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rra

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nsis

P. ca

lca

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T. b

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To

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er

10

cc

NL-VS 27.6 0.0 0.0 0.0 0.0 0.0 0.0 0.0 70.0 0.5 0.0 0.0 0.9

NL-SH 6.9 0.0 0.1 0.0 0.0 0.2 0.1 0.0 92.5 0.1 0.1 0.0 0.0 136*

SF-VS 29.4 0.4 1.7 2.0 2.0 0.4 0.4 8.5 36.0 0.0 2.8 5.2 3.3 169

SF-SH 50.2 1.1 1.3 0.0 3.2 8.7 0.6 0.0 28.8 0.6 0.7 0.0 0.0 750

AK-SH 32.4 0.0 0.3 0.0 1.0 2.9 3.1 0.0 54.1 0.9 0.3 0.3 0.0 574

AK-VS 17.8 0.0 0.0 0.6 4.3 4.4 0.2 0.0 69.6 0.0 1.0 0.0 0.2 741

AK-I 4.0 0.0 0.3 0.1 0.0 0.0 0.1 0.0 91.4 1.0 0.0 0.0 1.4 377*

SG-VS 29.7 0.0 0.0 0.0 0.0 0.0 0.0 0.0 69.0 0.0 0.5 0.0 0.0 657

SG-SH 20.4 0.0 1.4 0.0 0.0 0.0 0.0 0.0 78.2 0.0 0.0 0.0 0.0 1658

SG-I 14.7 0.0 1.4 0.6 0.0 0.0 0.0 0.0 76.7 0.2 0.4 0.2 2.7 376

SK-2-L SM 5.9 0.0 0.0 0.0 0.3 0.0 0.0 0.0 84.5 0.0 0.6 4.6 0.9 170

SP-1 G 2.8 0.0 0.3 0.0 0.0 0.0 0.0 0.0 88.6 0.5 0.7 0.2 4.9 724

SP-1 T 0.8 0.0 0.0 0.0 0.0 0.0 0.0 0.0 93.1 1.5 0.9 0.0 0.9 3468

SP-1 L-SM 0.2 0.0 0.0 0.2 0.0 0.0 0.0 1.6 82.5 0.3 0.4 9.4 3.5 1303

SK-2 G SM 13.4 1.5 0.7 0.0 0.1 0.0 0.2 1.2 75.5 0.7 0.8 1.1 0.0 434

SK-2 T 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 95.0 0.1 1.6 0.0 0.0 970

RD-3 4.7 8.5 0.4 16.6 0.0 0.0 0.9 14.9 25.2 0.0 4.3 13.2 6.4 147

SK-2 G F 11.1 0.7 0.3 0.2 0.5 0.0 0.2 0.0 79.1 0.2 0.5 1.5 0.0 175

SP-1 C 5.6 0.0 0.0 0.0 0.0 0.0 0.0 0.0 86.1 5.9 0.0 2.4 0.0 339

SP-1 L-F 21.7 0.0 0.0 0.0 0.0 0.0 0.0 0.0 73.4 0.0 0.0 3.3 0.8 245

RD-1 J 1.1 0.0 0.0 0.0 0.2 0.0 0.0 0.0 67.0 0.5 1.2 27.6 0.0 400

NS-9 13.8 0.0 0.0 0.4 0.0 0.7 0.1 0.0 78.4 0.0 0.4 1.2 1.1 671

SK-5 29.6 1.7 0.0 0.9 0.0 0.2 0.0 0.0 17.8 0.0 0.9 44.5 0.0 1609

RD-1 H 10.6 0.1 0.0 0.0 0.1 0.0 0.0 1.4 19.2 0.0 0.7 63.4 2.8 412

SK-2 G W 23.8 0.0 3.2 0.0 0.0 0.0 0.1 0.1 66.1 0.2 0.0 0.1 0.4 461

SP-1 H 5.5 0.1 0.4 0.6 0.0 0.0 0.0 0.8 84.0 0.4 0.6 1.5 1.5 2914

* per g wet macroalgae wt., unlike all samples normalized per 10 cc volume of wet macroalgae

Page 20: Characteristics of benthic foraminifera inhabiting rocky reefs in

16

common species are Textularia agglutinans (a probable invasive species), Pararotalia

calcariformata (invasive) and Planorbulina mediterranensis (native).

Among the 77 species occurring at CH and AK only 13 comprise in at least one sample

≥3% of the community (Table 4). Amphistegina lobifera is by far the most common

species occurring in all studied samples and comprising 18-93% of the assemblage

composition (on average 68.5±23.6). Other species occurring in high relative abundance

are Textularia agglutinans with max of 50% at AK site SF-SH and Pararotalia

calcariformata with max of 63%, occurring mostly at CH (Table 4).

The majority of the common species are aliens (Fig. 7; Table 3). They comprise up to

98% of the entire assemblage. An exception appears in CH RD-3 site where aliens

comprise ~60% of the community and at AK SF sites 80%. In addition to A. lobifera, T.

agglutinans (apparently alien) and P. calcariformata, a new alien species

Sigmamiliolinella australis was identified in this survey. It appears in both regions

comprising up to 15% and 8.5% of the community at CH and AK respectively.

Epistomaroides punctulata, a Lesspesian species, first recorded on the Israeli coast in

2005 by Almogi-Labin and Hyams-Kaphzan (2012) was found also in this study at 5 sites

in CH and 3 sites in AK, comprising <1% of the assemblage.

Sorites orbiculus, a LBF recently found alive on pebbles at 0.2 m off Shikmona is quite

rare in our material comprising ≤2% at CH and ≤1% at AK. The low occurrence of this

species in our sample is related to the fact that this variant is restricted to very shallow

water not sampled in this study, and is similar to its habitat in northern Gulf of Aqaba, as

shown recently by phylogenetic analyses of Merkado et al. (2014).

3.3 Multivariate analysis of the community structure and composition

In order to test the similarity in assemblage composition between CH and AK regions a

cluster analysis based on Bray-Curtis similarity coefficient was performed on the relative

abundance database (Fig. 8). Lines marked red in the dendogram by SIMPROF test are

not different significantly (Fig. 8A). Two clusters of samples form at a similarity of 38%

and show some difference among the samples from the two studied regions.

Cluster 1 consists of three sites from CH. Cluster 2 with a similarity of 50% consists only

of AK sites while cluster 3 consists of a mixture of sites from both regions with a

similarity of 70%. The non-metrical multidimensional scaling (nMDS) is based on the

pairwise distance of the Bray-Curtis similarity coefficient. Results of cluster analysis

were superimposed on the nMDS in Fig. 8B showing the same two clustering groups. To

understand which species are responsible for the differences between the clusters a

similarity percentage analysis (SIMPER) was done. Analysis using SIMPER for all

species shows that the average similarity for AK samples is 71%. The species contributed

Page 21: Characteristics of benthic foraminifera inhabiting rocky reefs in

17

to the similarity are A. lobifera – 76% and T. agglutinans – 22% making 98% of the

similarity. The average similarity for CH is 65%, contributed by A. lobifera – 87%, T.

agglutinans – 7% and P. calcariformata – 4%. The average dissimilarity between AK

and CH samples is 35% and the species contributing to it most are A. lobifera - 12%, T.

agglutinans – 8.5% and P. calcariformata – 5.4%.

Akhziv

Carmel Head

Fig. 7. Relative abundance of alien species (see also Table 3) occurring at AK and CH

sites.

0

10

20

30

40

50

60

70

80

90

100

NL-VS NL-SH SF-VS SF-SH AK-SH AK-VS AK-I SG-VS SG-SH SG-I

T. agglutinans

S. orbiculus

S. distorqueata

S. australis

Q. crassicarinata

Q. compressiostoma

Q. cf Q. mosharrafai

P. striolata

P. ovata

P. calcariformata

H. diversa

H. depressa

E. punctulata

C. hemprichii

A. lobifera

0

10

20

30

40

50

60

70

80

90

100

T. agglutinans

S. orbiculus

S. distorqueata

S. australis

Q. crassicarinata

Q. compressiostoma

Q. cf Q. mosharrafai

P. striolata

P. ovata

P. calcariformata

H. diversa

H. depressa

E. punctulata

C. hemprichii

A. lobifera

Page 22: Characteristics of benthic foraminifera inhabiting rocky reefs in

18

Fig. 8. A. Cluster analysis of samples using species relative abundance (P<0.05). Black

lines represent signiciant differneces (SIMPROF test). B. nMDS plot of all sites based on

Bray-Curtis similarity cofficient showing two main superimposed clusters of Fig. 8A.

The ellipses circles sites with 38 % similarity. For sites locations see Table 1.

The influnce of seasonality on the foraminiferal taxonomic similairty between the AK

and CH regions was analysed on their relative abundance database with log

transformation in order to reduce the influence of the most abundant species (Fig. 9). The

nMDS plot shows high similairty for the samples from the two studied regions with no

distinct differntiation between the seasons. Still many of the fall samples from both

region are clustered in the middle part of the plot showing larger resemblence while the

A.

B.

1

2

3

Page 23: Characteristics of benthic foraminifera inhabiting rocky reefs in

19

summer samples are located at the margins with large distances between the AK, ploted

at the lower part, vs. CH sites, ploted at the upper part of the ordination.

Fig. 9. nMDS ordination of AK and CH sites. The different symbols indiacte the 4

seasons (SP= spring, SM=summer; F=fall and W=winter) and the labels are the sampling

sites.

All living foraminifera collected from the 6 different macroalgae species and the Turf

(Tables 1, 3) are epiphytic. Among the macroalgae, Codium sp., Galaxuara rugosa and

Laurencia sp. are invasive while Dictyora sp., Halopteris scoparia (= Stypacaulon

scoparium) and Jania rubens are native (Rilov, 2014). Turf was sampled only in summer

both at AK and CH. Jania and Laurencia were sampled in all seasons except winter and

Galaxaura was sampled only at CH. Testing the similarity among the % benthic

foraminifera living on the 6 different macroalgae and Turf shows two clusters composed

of a mixture of different macroalgae without any distinct pattern (Fig. 10). Site SK-2

Turf is frequently an outsider, apparently because of the high dominance of A. lobifera of

95% with a few specimens of Quinqueloculina stelligera (Tables 2, 3). Other Turf

samples, located at the margins of the large cluster, came from different water depths.

Some of the Jania samples are grouped in the left cluster with sites located at CH and AK

in 2-7 m depth. In all these sites A. lobifera occurs in low percentages (generally <40%),

unlike other, Jania samples taken at 12-20 m water depth that belong to the large cluster

and contain >80% A. lobifera. To summarize, no clear associations between % benthic

Page 24: Characteristics of benthic foraminifera inhabiting rocky reefs in

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foraminifera and different macroalgae in the two studied regions could be established

indicating the indifference of the different species relative abundance to their host.

Fig. 10. nMD plot of relative abundance of benthic foraminifera per macroalgae at AK

and CH sites. Different symbols indiacte the different macroalgae and the labels are of

the different sites. The ellipses circles sites with 50% similarity.

Fig. 11. nMD plot of % benthic foraminifera per water depth. Different symbols indiacte

the different water depths categories with VS = 2-6 m, SH = 6-12 m and I = 12-20 m. The

labels are of the different AK and CH sites. The ellipses circles sites with 50% similarity.

Page 25: Characteristics of benthic foraminifera inhabiting rocky reefs in

21

Water depth is another important ecological parameter influencing the distribution of

benthic foraminifera in rocky habitats (Reiss and Hottinger, 1984). One of the groups

most affected by the bathymetry are the larger symbiont bearing benthic foraminifera

(LBF) with distibution limited by the amount of light penetration. In the studied material

we identified 3 depth categories: VS (2-6 m), SH (6-12 m) and I (intermediate, 12-20 m).

In order to test the similarity in assemblage composition between CH and AK regions

regarding the depth categories, a cluster analysis based on Bray-Curtis similarity

coefficient was performed on the relative abundance database. The three clusters formed

at a similarity of 50% were superimposed on the nMDS in Fig. 11.

The largest cluster is composed of a mixture of samples from the three different water

depth categories with the deepest I category occurring mainly in the upper part of the plot

while SH depth category occurs more frequently in the lower part of the plot. The small

cluster on the left seems to stand by itself. It is composed of very shallow to shallow

water sites charcterized by low percentage of A. lobifera (generally <40%, Table 4) that

group together also when checked for % bentic foraminifera vs. macroalgae (Fig. 10).

The single site cluster SK-2 T is an outlier, as seen also in Fig. 10.

In order to examine the relation between the most common species (>3%, Table 4) and

the different sampling sites, a principal component analysis (PCA) was conducted (Fig.

12). The PCA plot shows the distribution of the variables in the space formed by the two

main components, which explain 74% of the variance, with PC1 explaining 45% and PC2

29%. The alien LBF Amphistegina lobifera plots most positively on PC1. Amphistegina

lobifera plots negatively to T. agglutinans on PC2 and opposite on PC1. P.

calcariformata plots negatively both on PC1 and PC2.

The distribution pattern of most common species among the different sampling sites are

presented by “bubbles” (Figs. 13-16) that show the abundance overlaid on the nMDS

ordination of per 10 cc (Fig. 3; Table 4) and the relative abundnace overlaid on Fig. 8.

Amphistegina lobifera is the most common species occurring in all samples, all seasons,

all water depths and on all macroalgae species from both regions but in different standing

stocks and percentages. Its standing stocks values range over two orders of magnitutde

(37-3200 #/10cc) comprising on average 68.5±23.6% of the community (Fig. 13). The

highest standing stocks is found at the deepest site SP-1 (20 m) both during summer and

winter, and the highest percentages (>90%) occur in spring and summer mainly on Turf

and Jania. A similar water depth range of 15-25 m was documented by Hyams-Kaphzan

et al. (2008) for A. lobifera off Dado and Akhziv. Gruber (2006) studied the distribution

of A. lobifera on Cystoseira sp. and Jania rubens off Shikmona at 1.5 m depth. She

showed large variability in standing stocks and a single reproduction period, in early

summer. In the G. Aqaba / Red Sea this species lives down to 40 m water depth (Reiss

and Hottinger, 1984) reproducing twice a year (January and June, as described by Ter

Page 26: Characteristics of benthic foraminifera inhabiting rocky reefs in

22

Kuile and Erez, 1984) unlike its Israeli Mediterranean counterpart that reproduces once a

year in early summer, apparently because minimum winter temperatures were too low

(Langer and Hottinger, 2000; Gruber, 2006; Herut et al., 2005). This species is the most

successful Lessepsian invader among the foraminiferal group, occurring in extremely

high numbers all over the eastern Mediterraenan, reaching lately Malta and Sicily coasts

(Yokes et al., 2007; Langer, 2008; Langer et al., 2012; and Caruso and Cosentino, 2014).

Fig. 12. PCA ordination of study sites with abundant(>3%) benthic foraminiferal species

vectors overlain on it. PC1 explains 45% of the variance and PC2 29%.

Pararotalia calcariformata, another symbiont bearing alien species domiantes CH sites

RD-1, RD-3 and SK-5 all from 2-7 m water depths (Figs. 12, 14), replacing apparently A.

lobifera that comprise in these sites < 40% of the assemblage. This alien species was first

documented as P. spinigera on the very shallow Israeli coast in the mid-90th

by

Reinhardt et al. (1994) and Yanko et al. (1994) and later described by Hyams-Kaphzan et

al. (2008) and Arieli et al. (2011). Recently it was reported from the southeastern coast of

Turkey by Meriç et al. (2013) as P. calcariformata. This species occurs in high numbers

on the abrasion platforms (AAL personal communication) and on algal mats growing on

beachrocks. Arieli et al. (2011) studied these beachrocks within a project aiming to study

Page 27: Characteristics of benthic foraminifera inhabiting rocky reefs in

23

the distribution of foraminifera along a temperautre gradient adjacent to Hadera Power

Plant. She indicated that P. calcariformata proliferate in summer when temperatures

exceeds 30 ºC and it survives temperutures of up to 35 ºC in the most warm stations.

This species was reported by Hyams-Kaphzan et al. (2008) mainly from the central part

of the Israeli shelf from shallow water habitats within the Nilotic province. This agrees

with our findings that this species occurs mainly in the CH sites and being quite rare at

AK sites (Table 4, Fig. 14). Moreover it occurs also in the 12-20 m depth interval, though

in lower numbers as compared to the 2-12 m sites at CH, indicating its expansion to

deeper waters.

Fig. 13. “Bubbles” showing the abundance (#/10 cc) and relative abundance overlaid on

the nMDS ordination of per 10 cc (Fig. 3; Table 4) and of percentage as in Fig. 8. The

legend is the scale of abundance (#/10 cc) top and relative abundance (bottom) for

Amphistegina lobifera. Labels mark the different sites.

# / 10cc

%

Page 28: Characteristics of benthic foraminifera inhabiting rocky reefs in

24

Textularia agglutinans predominate the shallow water AK sites from 5 to 12 m (Figs. 12,

15; Table 4). It occurs also in CH sites but in lower percentages compared to AK. Arieli

et al. (2011) showed that in the algal mats covering the beachrocks off Hadera this

species lives mainly in winter and disappears as temperature rise, being absent from the

most warm stations in summer adjacent to the Hadera Power Plant. On the abrasion

platforms it was found attached to the “roots” of Jania (AAL personal communication).

In the studied sites it occur in all seasons with high percentage in summer at AK and in

winter at CH.

Fig. 14. “Bubbles” showing the abundance and relative abundance overlaid on the nMDS

ordination of per 10 cc (Fig. 3; Table 4) and of percentage as in Fig. 8. The legend is the

scale of abundance (#/10 cc) top, and relative abundance (bottom) for Pararotalia

calcariformata. Labels mark the different sites.

%

# / 10cc

Page 29: Characteristics of benthic foraminifera inhabiting rocky reefs in

25

Tretomphalus bulloides plots close to the vector of P. calcariformata (Fig. 12) and is

more frequent at CH sites comprising up to 6% of the assemblage at site RD-3 (Table 4).

Heterostegina depressa plots on the same vector as A. lobifera. It is another Lessepsian

LBF that occurs mostly between 6-20 m with the highest relative abudance of 6% at 20 m

at CH site SP-1 C. Herut et al. (2005) recorded this species on the submerged Kurkar

ridges in Haifa Bay at 10 m water depth. In G. Aqaba this species lives between 20 and

130 m, only on hard bottoms and often occurs in shaded areas in shallower water (Reiss

and Hottinger, 1984).

Fig. 15. “Bubbles” showing the abundance and relative abundance overlaid on the nMDS

ordination of per 10 cc (Fig. 3; Table 4) and of percentage as in Fig. 8. The legend is the

scale of abundance (#/10 cc) top, and relative abundance (bottom) for Textularia

agglutinans. Labels mark the different sites.

The LBF species Peneroplis planatus and P. pertusus plot close to T. agglutinans vector

(Fig. 12). Both species are more common in AK sites, only in very shallow to shallow

# / 10cc

%

Page 30: Characteristics of benthic foraminifera inhabiting rocky reefs in

26

water depths (< 12 m) comprising up to 9% and 4 % of the assemblage repectivly (Table

4). Hyams-Kaphzan et al. (2008) showed that although those peneroplid species occurred

between 3-42 m at Akhziv, their maximum abundance was at 6 m. These two species are

natives to the Mediterranean (Cimerman and Langer, 1991).

Sigmamiliolinella australis (Parr) is a new alien species (Fig. 16; Table 3), first recorded

in this study. This species is known from the Maldives (Parker and Gischler, 2011),

Mozambique, New Caledonia and Sahul Shelf (Loeblich and Tappan, 1994). However it

is not known from the G. Aqaba / northern Red Sea (Hottinger et al., 1993). This species

was found in several CH sites in low numbers and percentages. In CH site RD-3 and in

AK site SF-VS it comprise 15% and 9%, respectively, of the assemblage composition. In

these sites it occurs generally with P. calcariformata, in a separate cluster (Figs. 8, 10-

11). The vector distribution of this species is not clear yet in this stage.

Fig. 16. “Bubbles” showing the abundance and relative abundance overlaid on the nMDS

ordination of per 10 cc (Fig. 3; Table 4) and of percentage as in Fig. 8. The legend is the

scale of abundance (#/10 cc) top, and relative abundance (bottom) for Sigmamiliolinella

australis. Labels marks the different sites.

# / 10cc

%

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27

4. Conclusions

The rocky reefs of northern Israel comprise a unique, diverse and sensitive ecosystem

with

• High benthic foraminiferal diversity and low evenness

• High dominance of epiphytic species with endosymbionts; variable dominance at

each area

• 77 species: 43 in Akhziv (max on Jania; max. inside Akhziv Nature Reserve), 71

in Carmel Head (max on Galaxaura)

• Few rare species restricted to AK (4) and much more to CH (14)

• Compared to the sandy-silty habitat, rocky reefs are hot spots for invasive species

therefore needs to be constantly monitored

5. Acknowledgments

We are grateful to Gil Rilov the head, Ohad Peleg the lab manager and the Marine

Community Ecology Lab team from IOLR for their hard and dedicated work during their

numerous scuba diving campaigns. We are also grateful for the technical help of Michael

Kitin from the Micropaleontological Lab and Ra’anan Bodzin from the SEM Lab, at the

GSI. Yael Edelman-Furstenberg from the GSI and Yael Leshno from BGU University

and GSI are acknowledged for their useful comments. We acknowledge funding by Grant

contract no. 212-17-024 of the Earth Sciences Board, Ministry of National

Infrastructures, Energy and Water Resources.

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תקציר

מ'. סביבות אלה 0-00סביבות סלעיות נפוצות מאד במדף היבשת של צפון ישראל בעיקר בעומקי מים שבין

אצות, מאקרופאונה ודגים. סביבה זו חשופה -מצטיינות במבנה מורכב, מגוון מינים גבוה ועושר רב של מאקרו

השינויים שמתרחשים בעשרות השנים האחרונות להפרעות מעשה ידי אדם. כדי שניתן יהיה לעקוב אחר

בסביבה דינמית זו יזמנו את המחקר הנוכחי בשילוב חיא"ל שבאמצעותו נבדקו מספר קבוצות מפתח מתוך

כוונה שהמידע המצטבר ישמש כבסיס לכל מחקר שיבוצע באזור זה בעתיד. במחקר זה נבדקה קבוצת

אגלוטיננטי הידועים ברגישותם הפורמיניפרה הבנתוניים, המורכבת מיצורים חד תאיים בעלי שלד גירי /

נושאי פורמיניפרה בנתוניים נדגמו Turf -מיני אצות ו 6הרבה ובתגובתם המהירה לשינויים בתנאי הסביבה.

ע"י צוות הצוללים 3002-3000באביב ובסתיו באזור אכזיב ומדי עונה בראש כרמל )כולל שקמונה( במהלך

מ'. 3-30תם העונתית ובעומקי מים בין של חיא"ל. דיגום האצות בוצע בהתאם להופע

פורמיניפרה בנתוניים נפוצים מאד בסביבה הסלעית של צפון ישראל ומספר הפרטים באזור המחקר נע בין

סמ"ק נפח אצה רטובה. מתוך בדיקת הנתונים עולה כי השינויים במספר הפרטים 00 -פרטים ל 070-2000

מיני פורמיניפרה 77הם חיים, בעומק המים או במיקום התחנות. אינו תלוי בעונתיות, במיני האצות שעליהם

2-03מינים באזור אכזיב. מספר המינים בתחנה נע בין 02בראש כרמל ו 70בנתוניים חיים זוהו בסביבה זו,

כשמספרם פר תחנה גבוה יותר לרוב בראש כרמל. גם במקרה זה לא נמצא קשר ברור בין מספר מיני

. 2%מכלל המינים נפיצותם היחסית עולה על 07%מק המים, מין האצה או עונתיות. רק הפורמיניפרה לעו

מינים מיוצגים רק ע"י פרט אחד לכל מין כשמרבית המינים הנדירים נמצאו בראש כרמל. 01לעומת זאת

בממוצע מתוך 70-10%מכלל המינים הם מהגרים, רובם לספסיים אך מבחינה מספרית הם מהווים 30%

01הפרטים של קבוצת הפורמיניפרה באכזיב ובראש כרמל בהתאמה. במילים אחרות ניתן לקבוע כי כלל

המינים המקומיים מהווים רק חלק קטן מאד מכלל פרטי הקבוצה ומספרם הולך ופוחת עם הזמן. דחיקת

המינים המקומיים היא תהליך מתמשך הדורש מעקב קבוע.

הנפוץ ביותר בסביבה הסלעית של צפון ישראל המין הוא לספסי. מהגר הוא, Amphistegina lobiferaהמין

. מין זה הולך ומתפשט ברחבי 8.5%±23.6%6מכלל מאסף הפורמיניפרה ובממוצע 01-32%והוא מהווה

מזרח הים התיכון ולאחרונה הגיע לחופי מלטה וסיציליה והוא מהווה איום על אוכלוסיית הפורמיניפרה

. מין מהגר נוסף שהולך ומתפשט בעיקר דרומה למפרץ חיפה על יצורים אחרים בסביבה זוואולי גם המקומית

שנים בחופי ישראל מופיע במספרים נמוכים 30. מין זה שזוהה לפני Pararotalia calcariformataהוא ה

ות באזור אכזיב ונמצא במספרים גבוהים יותר בתחנות הרדודות של ראש כרמל כשהוא מראה מגמת התפשט

למים עמוקים יותר.

הסביבה הסלעית של צפון ישראל פגיעה ונתונה להשפעת מעשי ידי אדם כולל כניסת מינים פולשים ודחיקת

המינים המקומיים המשנים לחלוטין את מבנה מערכת אקולוגית זו ולכן יש צורך במעקב קבוע אחר סביבה זו

שראל.שהיא מין העשירות במגוון המינים והפרטים בחופי י

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STATE OF ISRAEL מדינת ישראל

THE MINISTRY OF NATIONAL INFRASTRUCTURES שרד התשתיות הלאומיותמ

Office of the Chief Scientist המדען הראשי

פורמיניפרה בנתוניים של שוניות סלעיות במדף

בשת של צפון ישראלהי

לבין-קפצן, לידיה פרליס גרוסוביץ ואהובה אלמוגי-אורית חיימס

המכון הגיאולוגי

20.8.20.4

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