Post on 25-Apr-2023
ORIGINAL PAPER
A paradox of the ciliates? High ciliate diversity in a resource-poorenvironment
Monika Claessens • Stephen A. Wickham •
Anton F. Post • Michel Reuter
Received: 20 March 2009 / Accepted: 22 October 2009 / Published online: 10 November 2009
� Springer-Verlag 2009
Abstract Ecological theory predicts that low productivity
systems should have low biodiversity. However, despite
the oligotrophic status of the Gulf of Aqaba (Northern Red
Sea) ciliate species richness was unexpectedly high. In
addition, phytoplankton, as main ciliate prey, was made up
by only few genera, indicating a significant niche overlap
among the grazers. Up to 97% of the ciliates were from the
same taxonomic group and of the same size range,
implying very similar food niches. Ciliate diversity was
highest at times of lowest chlorophyll concentrations,
during the period of stable abiotic conditions, but relatively
high genetic diversity within the ciliate prey, notably
among the cyanobacteria Synechococcus and Prochloro-
coccus. In the absence of disturbance and with little pre-
dation pressure, the alternate explanations for the observed
ciliate diversity are either very fine niche partitioning by
the ciliates, or their competitive equivalence resulting in a
random assortment of species immigrating from a larger
metacommunity, in accordance with Hubbell’s, (The uni-
fied neutral theory of biodiversity and biogeography.
Princeton University Press, Princeton, 2001) neutral model.
While the use of species abundance distributions (SAD’s)
is far from definitive, the theoretical SAD’s that best fit the
Gulf of Aqaba ciliate data was most often not that expected
by neutral theory.
Introduction
Biological diversity has become a major issue due to
increasing concerns about the global losses of species
richness. Although the classical paradigm holds that two
species cannot coexist at equilibrium if they share a single
niche, actual diversity often exceeds the expected diversity
(Hutchinson 1961; Kneitel and Chase 2004). Attempts to
explain this phenomenon have been traditionally been
dominated by niche partitioning theories (reviewed in
Silvertown 2004), while nonequilibrium approaches have
examined the role of predation and disturbance in main-
taining diversity (Paine 1966; Connell 1978). More
recently, it has been suggested that species do not differ
substantially in their competitive abilities (and are there-
fore ‘‘neutral’’), and the species actually found in any given
community are the result of stochastic processes of immi-
gration from a larger metacommunity, speciation and local
extinction (Hubbell 2001). This so-called neutral theory of
biodiversity has been invoked to explain the species dis-
tribution patterns in tintinnid ciliates in the oligotrophic
eastern Pacific (Dolan et al. 2007). In that study, high
tintinnid diversity was found despite low chlorophyll
concentrations (B1.7 lg chlorophyll a L-1), and species
abundance pattern most often followed a log-series distri-
bution, thought to be indicative of a neutral community
Communicated by U. Sommer.
M. Claessens � S. A. Wickham (&)
Department of Organismic Biology, University Salzburg,
Hellbrunnerstrasse 34, 5020 Salzburg, Austria
e-mail: steve.wickham@sbg.ac.at
M. Claessens
e-mail: monika.claessenskenning@googlemail.com
A. F. Post
The Interuniversity Institute for Marine Sciences,
Coral Beach POB 469, 88103 Eilat, Israel
e-mail: apost@mdl.edu
M. Reuter
Department of General Ecology and Limnology,
University Cologne, Weyertal 119,
50923 Cologne, Germany
123
Mar Biol (2010) 157:483–494
DOI 10.1007/s00227-009-1334-7
model, at least in species-rich systems (Alonso and
McKane 2004; Dolan et al. 2007).
In contrast to Dolan et al. (2007), where samples were
taken once at a large spatial scale, the present study
returned repeatedly to the same sampling site over a period
of 2.5 years. Our study area was the oligotrophic (chloro-
phyll a \ 0.8 lg L-1) Gulf of Aqaba, northern Red Sea,
which is characterized by deep mixing in winter, injecting
nutrient-rich waters into the productive layers, and stable
stratification in summer, causing nutrient depletion in the
photic zone. This alternation leads to a seasonal succession
of dominance by small eukaryotic algae (winter mixing),
Synechococcus (spring) and Prochlorococcus (summer) in
the phytoplankton community (Lindell and Post 1995).
Although the relationship between productivity and species
richness remains controversial (e.g., Kondoh 2001; Mit-
telbach et al. 2001), Cadotte (2006) found that increased
resources maintained greater species richness in a micro-
bial model system. There is debate whether the produc-
tivity–diversity relationship is unimodal or linear (Chase
and Leibold 2002), but at the very low productivities typ-
ical for the Gulf of Aqaba, it seems clear that a positive
relationship between productivity and diversity is to be
expected. Therefore, we expected that the low prey bio-
mass and diversity in the Gulf would lead to low ciliate
diversity—particularly during periods of stable abiotic
conditions. The Gulf is subject to only infrequent distur-
bances in terms of temperature or turbulence. With the
onset of stratification, there were only marginal changes in
temperature or mixing, caused by weather events, which
might be a disturbance in sense of the intermediate dis-
turbance hypothesis (IDH; Connell 1978). We analyzed
ciliate diversity, in an approach connecting multiple tro-
phic levels, during winter mixing, the spring onset of
stratification and in late summer. Ciliate diversity was very
high, which cannot be explained by a high number of
available niches or high food quantity. The aim of the study
was to explain this unexpected high ciliate diversity, with
respect to the low heterogeneity and diversity within the
resource level.
Materials and methods
Sampling and study site
Samples were taken along a 600–700 m deep water column
at sampling station A (29�280N, 34�550E) in the Gulf of
Aqaba, Israel. Open waters of the Gulf have hydrographic
conditions resembling those of open ocean systems despite
their proximity to the coast, with no noticeable coastal
effects on nutrient regimes and plankton ecology (Lindell
and Post 1995). Water samples were taken toward the end
of winter mixing (March 21, 2004; March 23, 2005),
shortly after the onset of stratification (April 17, 2005) and
after approximately 4 months of stable stratification
(August 21, 2003; September 9, 2003; September 3, 2004).
Triplicate water samples taken at 2, 80, 140, 350 and
600 m were drawn from 12 L Niskin bottles mounted on a
CTD-rosette. Replicates were taken from separate Niskin
bottles, when possible from different CTD-cruises. Con-
tinuous vertical profiles data for temperature and in vivo
chlorophyll a fluorescence were collected. Water chemis-
try, chlorophyll concentrations and phytoplankton abun-
dance were determined for distinct depths. Phytoplankton
was enumerated on a FACScan flow cytometer (Becton
Dickenson) with only partial analysis of Prochlorococcus
populations due to their low autofluorescence signals. Flow
cytometry was also applied to assess bacterial abundances
after staining with SybrGreen. Nitrite, nitrate and phos-
phorus (after a 20-fold concentration by the MAGIC
method (Karl and Tien 1992) were measured colorimetri-
cally on a QuickChem 8000 flow injection autoanalyzer
(Lachat Instruments) with detection limits of 20 nmol L-1
for nitrate and nitrite and 10 nmol L-1 for phosphorus (see
Lindell et al. 2005). These analyses are part of routine
measurements in the National Monitoring Program of the
Gulf of Aqaba at The Interuniversity Institute for Marine
Science (http://www.iui-eilat.ac.il/NMP/). Ciliate samples
were fixed in Bouin‘s solution (5% f.c.) and then settled in
1 L-graduated cylinders for 5 days. The samples were
reduced to a volume of 100 mL by siphoning off the upper
900 mL. Ciliates were counted as distinct morphotypes in
settling chambers according to the Utermohl method.
Depending on ciliate abundance, the equivalent of between
100 and 500 mL was settled, with[100 cells counted in all
but the deepest samples. In addition, the Quantitative
Protagol Stain (which silver-stains nuclei and ciliary basal
bodies; Skibbe 1994) was applied to a subset of samples in
order to improve the taxonomic resolution (usually at least
to genus, and often to species). Mixotrophic species could
be identified in QPS samples by their stained algal sym-
bionts or chloroplasts. Taxonomy followed Lynn and Small
(2000), and ciliates were identified using Kofoid and
Campbell (1939), Lynn and Montagnes (1988), Lynn et al.
(1988), Lynn and Gilron (1993), Montagnes and Taylor
(1994), Agatha et al. (2005).
Statistical analysis
Species richness (the total number of species found, SR),
evenness (Shannon–Wiener Diversity divided by maximal
diversity, a diversity measure independent of the species
richness, E) and the Jaccard similarity index (the propor-
tion of shared species between two samples) were calcu-
lated to evaluate ciliate diversity. Calculations were based
484 Mar Biol (2010) 157:483–494
123
on the abundances of the morphotypes. Some of the mor-
photypes comprised of two or even three morphologically
very similar species, which could not be distinguished from
another in settled samples. Thus, diversity is underesti-
mated in some cases. Species richness and evenness
between different seasons were compared with t-tests. The
relationship between chlorophyll and ciliate abundance
was analyzed with Pearson’s correlations. To test whether
differences in Jaccard’s similarity index were more than
expected by chance, Monte Carlo simulations were run.
Expected Jaccard’s indices were calculated using the total
number of species found in the water column as the species
pool, and randomly assembled subsets of species, with the
species richness of the subsets equal to the numbers of
species found in adjacent depths. For example, if there
were a total of 40 species in the water column and 15 and
18 species in two adjacent depths, J would be calculated
100 times using groups of 15 and 18 species, randomly
drawn from the species pool of 40.
Species abundance distributions (SAD’s) were fit using
geometric, log-normal, log-series and zero-sum multi-
nomial (hereafter ‘‘zsm’’) distributions. A geometric
distribution is thought to occur when each species
monopolizes the same proportion of available resources,
but if the competitive dominant utilizes x% of the resour-
ces, then the second best competitor uses the same x% of
the remaining resource, the third best competitor x% of
the resources not used by the best two competitors, etc.
(Magurran 1988). It is thought to be most common in
species-poor and/or harsh environments where relatively
few factors determine the niche. The log-normal distribu-
tion predicts a more even distribution of resources,
typically when the niche is multi-dimensional (Magurran
1988). The log-series distribution has been used as a proxy
for a distribution consistent with the neutral model (Dolan
et al. 2007) and thought to be consistent with the neutral
community model when diversity is high (i.e. when
Hubbell’s fundamental biodiversity number, h[ 1; Alonso
and McKane 2004). However, the zsm distribution is
normally thought to be more consistent with the neutral
model, and at h\ 1, departs from the log-series distribu-
tion (Hubbell 2001; Alonso and McKane 2004). The
expected log-series distribution was calculated using May’s
(1975) approximation and an iterative half-step routine,
while the expected geometric distributions were calculated
using the formula given by Magurran (1988). Dolan et al.
(2007) argued that to calculate the expected geometric
distribution, it is more representative to use the relative
abundance of the most abundance species, rather than the
least abundant, as recommended by Magurran (1988) and
May (1975). As a result, expected distributions using both
the minimum and maximum relative abundances were
calculated and are referred to as Geomin and Geomax,
respectively. To calculate the expected log-normal distri-
bution, the mean and standard deviation of per-species
ln(abundance) in each sample was used to generate 1,000
log-normal distributions for each sample, with species
richness in each generated distribution equaling the actual
species richness in the sample. The expected abundances
were then ranked, and the average expected abundance for
each rank was calculated. The zsm distribution, along with
h and the second parameter of the neutral model, the
migration factor, m, were calculated using the untb pack-
age of the R program (specifically, the optimal.theta and
rand.neutral functions; Hankin 2009). After 1,000 distri-
butions and the subsequent relative abundances were gen-
erated, relative abundances were ranked and mean ranks
calculated. Differences between expected distributions
were tested using Chi-squared tests and were ranked using
the Akaike information criterium (AIC), calculated as in
Dolan et al. (2007). The Monte Carlo simulations, expected
SAD’s (with the exception of the zsm) and AIC’s were
calculated using SAS v.6.12.
Results
Hydrographic characteristics and chlorophyll
The typical seasonal pattern in the Gulf of Aqaba, with
stratification in spring–summer, followed by deep mixing
in fall-winter was reflected in the development of the
temperature and chlorophyll a profiles. During summer
stratification, a homogenous layer with temperatures
around 25–26�C from the surface to 40 m and a deep
chlorophyll maximum (DCM) at 80 m was found, with the
highest chlorophyll a concentration around 0.3 lg L-1.
The thermocline ran between 40 and 100 m, with a tem-
perature gradient between 25 and 22�C that was followed
by a deep, colder layer (20–21�C). The water column was
mixed from the surface down to 600 m during winter, with
homogenous temperatures (21�C) and uniform chlorophyll
a distributions (0.1–0.2 lg L-1). Sea surface warming in
spring caused the onset of stratification in April and
increased chlorophyll a values throughout the surface
mixed layer (0.4 lg L-1). Chl a was lowest in September
(200 m, 0.01 lg L-1), and the highest chlorophyll a value
was recorded in April (20 m, 0.44 lg L-1).
Phytoplankton and heterotrophic bacteria
The phytoplankton succession seen during our study was
similar to previous reports for the Gulf of Aqaba (Lindell
and Post 1995). In winter and early spring increased
numbers of small eukaryotic algae (1 9 104 cells mL-1)
were observed as long as mixing continued. With the onset
Mar Biol (2010) 157:483–494 485
123
of stratification, a shift to Synechococcus dominance began
(1.1 9 105 cells mL-1), and a Prochlorococcus bloom
was observed in summer ([105 cells mL-1). Densities of
heterotrophic bacteria were almost an order of magnitude
higher after the onset of stratification (1.9 9
106 cells mL-1) than during mixing in March and summer
stratification in August/September (5.5 9 105 and 5.3 9
105 cells mL-1, respectively). The morphological diversity
of the phytoplankton community was highest during mix-
ing, mostly among the eukaryotic algae. This diversity
declined with the onset of stratification during which per-
iod the dominant picocyanobacteria were high light (HLII)
adapted Prochlorococcus and clade III Synechococcus
(Fuller et al. 2003; Penno et al. in prep). The genotypic
diversity of Synechococcus in summer was expected to be
high, with several clades typical for this period, and the
numerical dominance of a single Prochlorococcus clade
(Penno et al. 2006).
Ciliate abundance
Ciliate abundance showed distinct seasonal differences in
the three periods: uniform, lower abundances during mix-
ing (230–885 cells L-1), followed by a order of magnitude
increase in the surface after the onset of stratification
(3,530 cells L-1) and finally reduced abundances in sum-
mer again, with a significant vertical gradient. Abundance
was always lowest in the 600 m samples. More detail about
ciliate abundance, biomass and species composition is
given in Claessens et al. (2008).
Ciliate diversity
Species richness and evenness were high given the nutri-
ent-poor nature and the very low heterogeneity of the
phytoplankton of the Gulf of Aqaba. During winter mixing,
a total of 47 and 55 ciliate species were found in the entire
water column in March 2004 and 2005, respectively, with
between 12 and 37 species found at any one depth and time
(Fig. 1). There was relatively little variance in either spe-
cies richness or evenness between the 2 years, with the
exception of 600 m where 12 species were found in 2004,
but 36 in 2005. There was no dominance of a single species
(0.8 \ E \ 0.9; Fig. 1) and on average, between 70 and
46% shared species between adjacent depths (Fig. 2). One
exception was in March 2004, where only there was only
29% species overlap between 300 and 600 m (but only 12
species in 600 m). While 29 or even 46% shared species
may seem low during a period when the water column was
mixing, Monte Carlo simulations showed that with 47 total
species, and subsamples of 35 and 12 species (the case for
the 350 and 600 m depths in March 2004), a Jaccard index
of 0.24 (i.e., 24% species overlap) could be expected by
chance. Similarly, the overlap found between other depths
during mixing was not less than expected by from a ran-
dom sample.
The onset of stratification affected the ciliate community
strongly, with a significant reduction in species richness
and the dominance of a single species in the surface layer
(t-test, P \ 0.001; and SR = 2–33, Fig. 1). In this period,
the similarity between the sampled depths declined as well.
While the upper 350 m still shared 50–64% of ciliate
species, the ciliates in the deep layer were exclusively
found there. Highest species richness was observed during
summer stratification (max. SR = 55; 80 m depth, August
21, 2003; Fig. 1) with a clear gradient over depth, but again
no dominance of a single species (average evenness:
0.78 \ E \ 0.93). As in winter, there was considerably
more variation between dates in species richness than in
evenness (Fig. 1). In summer, the similarity was lowest.
The upper layers (surface—140 m) only shared 40% of the
species and similarity declined in the deep layers to 28%.
The similarity of their ciliate community between the
sampled seasons was also low (Fig. 2). Comparing the
three seasons, the layers from surface to 80 m depth had
maximally 49% of their species in common. The 140 and
350 m layers were more similar over time, but only
between winter mixing and the onset of stratification
(Fig. 2). The deepest layer had the greatest turnover in
species over the seasons. This was true not only between
the periods of mixing and stratification, but also between
the onset of stratification and late summer.
Taxonomic composition
One group dominated the taxonomic structure of the ciliate
community in the Gulf of Aqaba, in all depths as well as in
all sampled seasons. The aloricate oligotrich ciliates (alo-
ricate members of the Choreotrichia and Oligotrichia)
represented up to 98% of total abundance and biomass,
with 45 species belonging to this group. The oligotrich
species constituted between 46 and 81% of total species
numbers, holding most species in all depth and seasons
(Fig. 3). Litostome ciliates were important regarding
abundance during mixing and tintinnids showed increased
biomass in this period, but in terms of percent on total
species number, litostome ciliates did not exceed 20%, and
the proportion of tintinnid species was even smaller
(Fig. 3). One species, Strombidium epidemum, dominated
after the onset of stratification, with 67% of total abun-
dance in the upper layer. As with the taxonomic pattern, the
size structure of the ciliate community was dominated by
one size class, the nanociliates (\20 lm). The small cili-
ates accounted for up to 88% of total abundance. Mixo-
trophy, combining heterotrophic and autotrophic modes of
nutrition, can reduce the amount of niche overlap and
486 Mar Biol (2010) 157:483–494
123
600
500
400
300
200
100
0
0 0,2 0,4 0,6 0,8 1
0 10 20 30 40 50
Dep
th (
m)
Evenness
Richness
0 0,2 0,4 0,6 0,8 1
0 10 20 30 40 50
Evenness
Species Richness
0 0,2 0,4 0,6 0,8 1
0 10 20 30 40 50
(b)(a) (c)
Fig. 1 Profiles of ciliate evenness (circles) and species richness (squares) during a the mixing period in early spring, b the onset of stratification
in April and c the summer stratification in August/September (from left to right)
(a) (b)Fig. 2 Jaccard similarity index
(J; % similarity), a between the
sampled depths for each season
(surface—80 m; 80–140 m;
140–350 m, 350–600 m),
b between the three seasons for
each sampled depth (summer
stratification—mixing,
mixing—onset of stratification,
onset of stratification—summer
stratification). The size of the
circles shows the percent
similarity, increasing similarity
with increasing circle diameter.
The numbers within the circlesshow the values of J in %
Fig. 3 Vertical profiles of the
proportion of the taxonomic
groups (oligotrichs, tintinnids,
litostomes, prostomes and
‘‘Others’’) on total species
richness during a mixing in
March, b after the onset of
stratification in April and c after
4 months of stable stratification
in August/September (left to
right)
Mar Biol (2010) 157:483–494 487
123
competition (e.g., Pitta et al. 2001; Sanders 1991) and so
might be advantageous when resources are limiting.
However, only 3 mixotrophic species were found (maxi-
mally 14% of abundance). More details about the species
composition, biomass and abundance of the Gulf of Aqaba
ciliate community are given in Claessens et al. (2008).
Diversity patterns
The relationship between productivity and diversity was
weak. We used chlorophyll fluorescence and sum of dis-
solved NO2 ? NO3 (total oxygenated nitrogen, TON) as
proxies for productivity. While the amount of available N
is known to drive phytoplankton abundance and composi-
tion in the Gulf of Aqaba and is expected to be inversely
related to chl a (Lindell and Post 1995), the correlation
between TON and chl a was weak (r = -0.28, P = 0.20).
There was a significant negative linear trend between TON
and ciliate species richness (Fig. 4a; Pearson’s r = -0.79,
P \ 0.0001), but no relationship between chlorophyll and
richness (Fig. 4b; Pearson’s r = 0.24, P = 0.29). Evenness
followed a trend opposite that of richness: this increased
with increasing TON (Fig. 4a; Pearson’s r = 0.63,
P = 0.0002), but decreased with increasing chlorophyll
(Fig. 4b; Pearson’s r = 0.72 P = 0.0002). There was an
outlier in the evenness data, as on one date and depth
(17 April 05, surface), the ciliate community was dominated
by a single species, and evenness was therefore low. This,
however, had little influence on the strength of the corre-
lations, as the nonparametric Spearman’s rho was similar to
the Pearson’s correlations (TON-Richness: Spearman’s
rho = -0.60; TON-Eveness: Spearman’s rho = 0.69) As
with richness, ciliate abundance was negatively, though
nonlinearly, related to TON (Fig. 4c; Pearson’s r = -0.45,
P = 0.015, Spearman’s rho = -0.73, P \ 0.0001). There
was also a strong positive, but log-linear relationship
between abundance and chlorophyll (Fig. 4d; log10
(abundance) - log10(chlorophyll): Pearson’s r = 0.82,
P \ 0.0001). Ciliate abundance and richness were also
positively, though nonlinearly, related (Fig. 5a). The rela-
tionship was best represented by the logarithmic function
log10 Richnessð Þ ¼ 0:34 � log10 Abundanceð Þ þ 0:56
R2 ¼ 0:66; P\0:0001
Conversely, evenness was a negative function of the
logarithm of abundance (Fig. 5b). When the sample with
the highest ciliate abundance (the surface sample from
April 17, 05, an obvious outlier) was omitted from the
regression, the function of the relationship was
Evenness ¼ �0:082 � log10 Abundanceð Þ þ 1:03
R2 ¼ 0:81; P\0:0001
Relative abundance data were fit to two versions of the
geometric distribution, the log-normal, log-series and the
(a) (b)
(c) (d)
Fig. 4 Upper panelscorrelations of species richness
(left axis) and evenness (rightaxis) against a NO3 ? NO2
(total organic nitrogen, or TON)
and b chlorophyll a, lowerpanels total ciliate abundance
(ind L-1) against NO3 ? NO2
and d chlorophyll a. A log scale
was used in d to linearize the
data
488 Mar Biol (2010) 157:483–494
123
zsm distributions for 28 of the 29 dates and depths in the
study. One sample (17 April 05, 600 m) had only 2 species
and was excluded from further analysis. The geometric
distribution, calculated using the proportion of the most
abundant species (Geomax), gave with one exception the
worse fits to the relative abundance data, as ranked by the
AIC statistic (Table 1). The Geomin distribution gave the
best fit to nine distributions, including the upper four
depths of the March 21, 2004 sampling date. The log-
normal and log-series distributions gave the best fit on 9
and 10 occasions, respectively: the log-normal predomi-
nantly during mixing and directly after the onset of strati-
fication (6 of 9 distributions), while the log-series gave the
best fit most often during the period of stratification (8 of
10 distributions, Table 1). On two occasion the zsm dis-
tribution gave the second best fit; on 25 of the 27 remaining
sampling dates, the zsm gave the worst or second worst fit
to the data (Table 1). All the theoretical distributions, with
the exception of the Geomax fit the data reasonably well,
with chi-square tests not being able to distinguish differ-
ences between the expected and observed relative abun-
dances (P [ 0.1, Fig. 6). The one exception was the
surface sample on April 17, 05, when a single species
dominated the ciliate community (Fig. 6d).
Discussion
Ciliates in the Gulf of Aqaba appear to contradict the
prevailing wisdom regarding the productivity–diversity
relationship. That the diversity was high for the produc-
tivity of the system seem clear. A total of 82 ciliate species
were found in the oligotrophic eastern Mediterranean and
Aegean Seas (when compared to 123 species in our study),
but from a greater number of samples than those taken in
our study (66 vs. 29, Pitta and Giannakorou 2000). In the
productive Long Island Sound, ciliate abundance was
[2000 cells L-1, but only 16–19 morphotypes could be
distinguished in a single sample (Doherty et al. 2007). The
same study found that genetic diversity among oligotrichs
and choreotrichs (the groups dominating the Gulf of Aqaba
ciliate community) was considerably higher that the mor-
phological diversity. If this is also the case for Gulf of
Aqaba ciliates, then the actual diversity is even higher than
what was measured in our study.
The relationship between ecosystem productivity and
diversity is usually thought to be unimodal at the local
level and monotonic at a regional scale, with disturbance
causing increased species richness at any given produc-
tivity level (Kondoh 2001; Chase and Leibold 2002).
Therefore, we expected low species richness in the study
area, the resource-poor and only marginally disturbed Gulf
of Aqaba. While we only measured proxies of productivity,
chlorophyll a and dissolved N, food resources are com-
monly used as a metric of the energy available, even in
experimental settings (e.g., Fukami and Morin 2003) There
was, however, no correlation between chlorophyll and
richness, with a positive relationship at only the lowest
chlorophyll concentrations (\0.05 lg L-1; Fig. 4b). There
was also a negative correlation between TON and species
richness, albeit over a narrow range of low TON concen-
trations (Fig. 4a). It might be expected that higher phyto-
plankton biomass would reduce dissolved N, thus resulting
in negative TON—chl a and TON—ciliate species richness
relationships. However, as neither the TON—chl a nor the
chl a—ciliate richness correlations were significant, the
negative TON—ciliate richness correlation was not simply
the result of higher productivity leading to both lower
dissolved N and higher ciliate richness. A similar trend has
recently been found for tintinnid ciliates in the Pacific,
where tintinnid diversity was unrelated to surface chloro-
phyll concentrations (Dolan et al. 2007). A negative rela-
tionship between tintinnid diversity and chlorophyll has
also been found, with a trend of lower chlorophyll and
(a) (b)
Fig. 5 a Species richness regressed against the logarithm of ciliate
abundance. The equation of the line is: Log10 Richnessð Þ ¼ 0:34 �log10 Abundanceð Þ þ 0:56: R2 = 0.66, P \ 0.0001,b species evenness
regressed against the logarithm of ciliate abundance. The equation of
the line is: Evenness ¼ �0:082 � log10 Abundanceð Þ þ 1:03: R2 = 0.81,
P \ 0.0001
Mar Biol (2010) 157:483–494 489
123
higher tintinnid species richness going from the western to
eastern Mediterranean (Dolan et al. 1999, 2002).
In our study, species richness was a positive, semi-log-
arithmic function of ciliate abundance (Fig. 5a). A possible
explanation of this positive relationship is a sampling
effect, where through random chance there is a greater
probability of finding more species in samples with more
individuals. We reduced this possibility by counting larger
sample volumes when abundances were low, and the nature
of the relationship suggests that more than simple a sam-
pling effect was occurring. A sampling effect should pro-
duce a log-linear relationship between abundance and
richness, with a slope \1, as increasing abundances are
associated with ever smaller increases in richness. This
occurred in our data (Fig. 5a, slope = 0.34), but the
regression line overestimated the actual richness at the
highest and lowest abundances. The cause for at least the
overestimation at high ciliate abundance can be seen in the
relationship between evenness and abundance (Fig. 5b). As
abundance increased, the species distribution pattern
became more uneven, with fewer species dominating the
ciliate community.
How can such a nutrient-poor system with minimal
resource heterogeneity support such high diversities and
high evenness? Niche differentiation has traditionally been
used to explain species diversity, where greater variation in
abiotic and biotic factors allows higher diversity. There is
mixed evidence for this in marine ciliates, with a positive
correlation between tintinnid diversity and chlorophyll size
or pigment diversity found in the Mediterranean, but not
the south-eastern Pacific (Dolan et al. 2002, 2007). There
was also some indication of resource partitioning in the
Gulf of Aqaba, at least when different water depths during
stratification are compared. Here, the average species
similarities between adjacent depths were 28–42%, indi-
cating considerable species turnover between depths
Table 1 Distribution rankings
according to AIC scores
Geomax is a geometric
distribution using the relative
abundance of the most abundant
species to calculate the expected
abundances, while Geomin uses
the least abundant species. The
March samples were during
water column mixing, April was
shortly after the onset of
stratification, and the August
and September samples were
taken while the water column
was stably stratified
ZSM zero-sum multinomial
distribution
Date Depth Species
richness
Geomax Geomin Log-normal Log-series ZSM
21 Mar 2004 1 32 5 1 2 3 4
80 30 5 1 2 3 4
140 37 5 1 2 3 4
300 35 5 1 2 3 4
600 12 5 3 2 1 4
23 Mar 2005 1 32 5 2 1 3 4
80 28 5 2 1 3 4
140 31 5 2 1 3 4
350 33 5 2 1 3 4
600 36 5 3 2 1 4
17 Apr 2005 1 26 5 1 3 4 2
80 33 5 2 1 3 4
140 27 5 2 1 3 4
300 25 5 1 2 3 4
600 2
21 Aug 2003 1 24 5 2 3 1 4
80 55 5 3 2 1 4
140 44 5 4 3 1 2
350 17 5 2 1 3 4
9 Sep 2003 1 34 5 3 2 1 4
80 28 5 3 2 1 4
140 21 5 3 2 1 4
350 10 5 2 3 1 4
600 5 3 1 4 2 5
3 Sep 2004 1 37 5 2 1 3 4
80 35 5 2 1 3 4
140 29 5 3 2 1 4
350 20 5 1 2 3 4
600 14 5 1 3 2 4
Times ranked first 0 9 9 10 0
490 Mar Biol (2010) 157:483–494
123
(Fig. 2a). However, in the Gulf of Aqaba, not only were
resources highly limiting, during stratification they had
very little apparent diversity, with either Synechococcus or
Prochlorococcus dominating in late spring and summer.
The ciliate community was dominated by oligotrichs and
choreotrichs\20 lm (up to 80% of the ciliate species and
up to 97% of ciliate abundance; Fig. 3), a closely related
group of ciliates with very similar food niches (Kivi and
Setala 1995). Evenness was largely independent of pro-
ductivity, with values between 0.75 and 1.0 in all but one
sample (Fig. 4b) Moreover, species richness was highest in
summer, when chlorophyll was lowest, and dominated by
Prochlorococcus. In this period, tintinnid and aloricate
oligotrich species dominated the ciliate community,
accounting for at least 50% of the species, all of them filter
feeders with the same prey size spectrum. This indicates
that the high species richness cannot be explained by high
functional diversity within the ciliate community. Not only
was algal biomass very low in the Gulf, but also it was
dominated by very few types of autotrophs resulting in
seemingly enormous niche overlap among the grazers.
Predation has the potential to increase diversity if the
effect is to reduce the abundance of a competitive domi-
nant, although if predation is nonselective, it can just as
easily reduce diversity by eliminating rare species (Paine
1966; Yodzis 1989). However, grazing by metazoans on
ciliate-sized particles in the Gulf of Aqaba has been
found to be negligible, with instantaneous grazing rates in
the range of 0.01–0.03 day-1 (Sommer et al. 2002).
Experiments conducted concurrently with the profile
(b)
(d)(c)
(a)
Fig. 6 Species abundance distributions (SAD’s) showing ciliate
relative abundance (the proportion of total abundance) against ranked
abundance for four representative samples. The circles are the actual
relative abundances, the lines are the expected abundances from four
theoretical distributions. All samples shown are surface samples aSept 3, 2004, where the log-normal distribution gave the best fit,
b Mar 21, 2004, Geomin (the geometric distribution using the smallest
relative abundance to calculate the expected abundances) gave the
best fit, c Sept 9, 2003, with the best fit given by the log-series
distribution, d April 17, 2005, where the zsm distribution gave the
best fit
Mar Biol (2010) 157:483–494 491
123
measurements reached similar conclusions (Claessens
unpublished data). Tintinnids and litostomes are known to
prey on other ciliates (e.g., Stoecker and Evans 1985), and
predation pressure on smaller ciliates could have conceiv-
ably come from these groups. While these groups were
routinely present in the Gulf of Aqaba ciliate community,
their abundance, particularly in a size range capable of
consuming other ciliates, was usually very low (Claessens
et al. 2008). Thus, it seems unlikely that predation played a
central role in structuring the ciliate community.
Mixotrophy would seem to be a potential route to
reducing niche overlap, and mixotrophic ciliates have been
found to make up an increasing proportion of total abun-
dance with decreasing productivity (Dolan et al. 1999; Pitta
et al. 2001). Mixotrophy was not a general strategy to
reduce niche overlap in the Gulf of Aqaba, as only 3
mixotrophic species were found, contributing maximally
14% to total ciliate abundance. Besides phytoplankton,
heterotrophic flagellates and bacteria generally fit the food
demands of ciliates. However, there was only one occasion
when heterotrophic bacterial abundance was above
0.6 9 106 cells mL-1, and flagellate abundance was also
proportionately low, usually \100 cells mL-1 (Claessens
et al. 2008; Claessens unpublished data). It would therefore
seem unlikely that either mixotrophy or predation on
nonautotrophic prey was viable strategy to reduce niche
overlap.
A plausible explanation for the high ciliate diversity
despite the low morphological diversity of prey may lie in
the genetic diversity of the autotroph community, and with
that, a prey diversity that might be higher than it seemed.
Ciliate diversity was generally lowest in April during the
Synechococcus bloom, when the picocyanobacterial
diversity was low with clade II Synechococcus dominating
this populations by far (Fuller et al. 2003; Penno et al.
2006). However, at least 8 different clades were identified
for the Gulf of Aqaba (Penno et al. 2006), and little is
known about their temporal and spatial distribution. Gen-
ome sequences (including two genomes of Gulf of Aqaba
strains) reveal that these clades likely represent ecotypes
and have different structural and physiological properties
(Dufresne et al. 2008). While differential use of limiting
resources can lead to coexistence of competing species
(Tilman 1985), there would need to be a remarkable degree
of specialization on very similar Synechococcus genotypes
in order to account for the 21–55 ciliates species found in
the upper 80 m of the Gulf of Aqaba in summer. This also
presumes that ciliates are selective feeders. Size-selectivity
by ciliates is a long-known phenomenon, and they can
actively reject less preferred particles after they are cap-
tured (Verity 1991 and literature therein; Strom and Lou-
kos 1998). Prey preference and possibly prey selection also
occur among ciliates feeding on marine picocyanobacteria
(Christaki et al. 1999). For the dominant ciliate group, the
oligotrich species, there is selectivity on the basis of prey
cell surface properties in addition to prey size, with cell-
surface lectin-recognition carbohydrates likely playing a
central role (Stoecker 1988; Christaki et al. 1999; Wootton
et al. 2007). Thus, niche differentiation and the diverse
Synechococcus populations in the Gulf may play a greater
than expected role in explaining high ciliate diversity at
times when the apparent prey morphological diversity is
low.
There is also some question as to exactly how ciliates
partition their niches. Recent laboratory work has demon-
strated that two bacterivorous ciliates can coexist on a
single bacterial strain, even without spatial heterogeneity
or chemically mediated interference competition (Fox and
Barreto 2006). Such results in a controlled environment
make rejecting a niche-partitioning hypothesis in field
populations somewhat problematic. Nevertheless, it is still
an open question as to whether potential selective predation
and the observed prey genetic diversity is sufficient to
explain the observed ciliate diversity in the Gulf of Aqaba.
High diversities have often been explained as the result
of disturbance in the sense of the intermediate disturbance
hypothesis (IDH) preventing a competitive dominant from
suppressing other species (Connell 1978). Disturbance
sources in aquatic systems are e.g., climatic events, tur-
bulence or mixing/stratification (Floder and Sommer 1999;
Beisner 2001; Weithoff et al. 2001). Mixing in the Gulf
regularly ends in April, and the system remains stably
stratified until fall. That the onset of stratification consti-
tutes a disturbance in sense of the IDH was clearly reflected
by the sharp break in evenness (Fig. 1). However, the onset
of stratification and nutrient depletion produced lower,
rather than higher, diversity. It was only at this time that a
single species made up more than 25% of total ciliate
abundance (Fig. 6d). Moreover, the frequency of distur-
bance has to be seen in the context of the generation time
of the organisms and the time necessary to establish
competitive exclusion. Diversity is highest when the time
between disturbances is less than the time needed to
establish competitive exclusion (Hutchinson 1961; Rey-
nolds 1988; Roxburgh et al. 2004). Stratification remained
stable for an estimated [100 generations of ciliates,
seemingly long enough for a competitive dominant to
establish itself. While the late summer ciliate community
was considerably different to that at the onset of stratifi-
cation (Fig. 2b), competitive dominance was not evident,
with average evenness during summer stratification of
0.79–0.93 (Fig. 1). Thus, it seems unlikely that disturbance
is a plausible explanation for the high diversity seen in Gulf
of Aqaba ciliates.
A third possible explanation is that Hubbell’s (2001)
neutral theory of biodiversity holds and that the observed
492 Mar Biol (2010) 157:483–494
123
species assemblage was a dynamic equilibrium due to local
extinction and immigration from a larger metacommunity.
The zsm distribution is expected when the neutral model
holds, but it has been repeatedly pointed out that theoretic
species abundance distributions (SAD’s) have multiple
theoretical causes, and that most theoretical distributions
are similarly hyperbolic (Magurran 1988; Hubbell 2001;
McGill et al. 2007). The log-series has also been cited as
expected by the neutral model, and at high diversities, there
is expected to be little difference between the log-series and
zsm distributions (Alonso and McKane 2004). Dolan et al.
(2007) found a log-series distribution to provide the best fit
to the abundance distributions of tintinnids along a broad
transect of the equatorial Pacific and suggested that the
tintinnid communities they sampled were random assem-
blage of species. While the zsm distribution gave a poor fit
to the data, log-series distributions gave the best fit to 10 of
28 samples, most often during the period of stable stratifi-
cation in late summer, the period most closely resembling
conditions in the Pacific when Dolan et al. (2007) took their
samples. During mixing and directly after the onset of
stratification (a period of rapidly declining nutrients), geo-
metric (at least the traditional version calculated using
minimum abundance) or log-normal distributions usually
gave a better fit (Table 1). While there are multiple theo-
retical causes for the same type of SAD, it would appear that
different processes are controlling ciliate species distribu-
tions during stable stratification and the rest of the year.
However, niche partitioning and neutral theories are not
mutually exclusive, but extremes on a continuum (Gravel
et al. 2006). Moreover, coexistence is enhanced when the
growth rates and carrying capacities of two species are more
similar (Leibold and McPeek 2006), a not-unlikely scenario
for the similar-sized ciliates of the Gulf of Aqaba.
What controls diversity in marine ciliate populations
remains an open, but very relevant question. Oligotrich and
tintinnid species consume particle in the size range 0.5–
20 lm, reaching from pico- to nanoplankton-sized particles
(Rassoulzadegan et al. 1988). Ciliates \20 lm, represent-
ing the most important group in the Gulf of Aqaba, were
most likely primarily picoplankton grazers, and only sec-
ondarily nanoplankton grazers, although within the oligo-
trichs there are species-specific differences in breadth of
the size spectrum grazed (Rassoulzadegan et al. 1988; Kivi
and Setala 1995). The prey size classes consumed by these
ciliates are largely too small for most metazoan grazers,
making ciliates an essential trophic link in oligotrophic
systems. Moreover, high diversity has the potential for
more complete and efficient use of resources, resulting in
higher biomass in high, compared to low, diversity systems
(Tilman et al. 1996). This was evident in the Gulf of Aq-
aba, with ciliate carbon:chlorophyll ratios up to 26, con-
siderably higher than the 2–5 normally found in marine
ciliate communities (Claessens et al. 2008; Dolan et al.
1999; Pitta et al. 2001). Thus, understanding the drivers of
ciliate diversity is essential to understanding how resources
are utilized in oligotrophic marine systems.
Acknowledgments The work was funded by the Deutsche Fors-
chungsgemeinschaft (DFG; grant WI 1623/3 to S. A. Wickham) and
Germany-Israel Foundation (grant #I-732-54_8_2002) to A. F. Post.
We are indebted to Inbal Ayalon and Amatzia Genin for providing the
phytoplankton and bacterial cell numbers, to Sabine Agatha for
helping identify some difficult ciliate species, and to John Dolan, who
helped with the geometric distributions. We are grateful to Dorit
Golan, Alexandra Pitt and Claudia Lorenz for their assistance and
fabulous organization. We thank Helmut Hillebrand and Mario Prast
for critical comments, and four anonymous reviewers for constructive
comments, which improved the manuscript.
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