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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
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
2
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.
3
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
4
(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
5
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.
6
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)
7
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).
8
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.
9
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
10
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).
11
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
12
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.
13
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
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
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
s
L. "s
eca
ns"
M. su
bro
tun
da
Milio
lin
ella
sp
p.
P. p
ert
usu
s
P. p
lan
atu
s
Q. cf. L
. b
rad
ya
na
S. a
ustr
alis
A. lo
bife
ra
H. d
ep
ressa
P. m
ed
ite
rra
ne
nsis
P. ca
lca
rifo
rma
ta
T. b
ullo
ide
s
To
tal p
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
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
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
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
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
20
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.
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
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
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
%
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
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
%
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
%
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.
6. References
Almagor, G. and Hall, J., 1984. Morphology and bathymetry of the Mediterranean
continental margin of Israel. Israel Geological Survey Bulletin, 77, 31 pp.
Almogi-Labin, A. and Hyams-Kaphzan, O., 2012. Epistomaroides punctatus (Said, 1949)
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31
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
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
GSI/36/2014 מס' דו"חES-20-2014