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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