Protist, Vol. 149, 29-37, February 1998 © Gustav Fischer Verlag
Protist
ORIGINAL PAPER
Protozoan Diversity: Converging Estimates
of the Global Number of Free-Living Ciliate Species
Bland
a
b
J. Finlaya,1, Genoveva F. Esteban a , and Tom Fenchel b
Institute of Freshwater Ecology, Windermere laboratory, The Ferry House, Ambleside, Cumbria LA22 alP, UK
Marine Biological laboratory (University of Copenhagen), Strandpromenaden 5, DK - 3000, Helsingm, Denmark
Submitted October 6, 1997; Accepted November 14, 1997
Monitoring Editor: Michael Melkonian
Protozoa are the most abundant phagotrophs in the biosphere, but no scientific strategy has
emerged that might allow accurate definition of the dimensions of protozoan diversity on a global
scale. We have begun this task by searching for the common ground between taxonomy and ecology.
We have used two methods - taxonomic analysis, and extrapolation from ecological datasets - to estimate the global species richness of free-living ciliated protozoa in the marine interstitial and freshwater benthos. The methods provide estimates that agree within a factor of two, and it is apparent
that the species-area curves for ciliates must be almost flat (the slope z takes the very low value of
0.043 in the equation: [number of species] = [constant][area]Z). Insofar as independent ecological
datasets can be extrapolated to show similiar, flat, species-area relations, and that these converge
with an independent estimate from taxonomic analysis, we conclude that the great majority of freeliving ciliates are ubiquitous. This strengthens our recent claim that the global species richness of
free-living ciliated protozoa is relatively low (-3000).
Introduction
It is rather difficult to provide accurate estimates for
the number of species in any of the larger taxonomic
groups (see May 1988, 1990). Furthermore, the
scale of the problem seems to be inversely related
to the size of the organisms concerned. Estimating
the global species richness of birds is probably an
achievable task (Zink 1996), but more difficult for the
insects (Gaston 1992) and, apparently, extraordinarily difficult for micro-organisms (see UNEP 1995),
where in many cases we do not even have a clear
idea of what a species is, let alone a sound strategy
for estimating global diversity.
1 Corresponding author;
fax 44-15394-46914;
e-mail [email protected]
Some of the methods used for estimating
species richness of larger organisms are inadequate when it comes to micro-organisms. For example, it may under certain circumstances be possible to extrapolate species numbers in size categories down to about 1 em, but this becomes a very
dubious procedure for size classes smaller than this
(Fenchel 1993). The main reason may be the
marked tendency towards cosmopolitanism in the
smallest organisms. For these, barriers to migration
and dispersal appear to be ineffective: thus rates of
extinction and speciation may be low, and the same
species will tend to be distributed worldwide. So
the global species richness of micro-organisms
could be relatively low, and the task of accurately
estimating the number of microbial species (includ-
30
B. J. Finlay, G. F. Esteban, and T. Fenchel
ing protozoa) may be simpler than previously
thought.
What evidence is there that protozoan species are
typically cosmopolitan and that the global number
of these species is modest? We have begun to answer this question for one large protozoan group in
particular - the ciliates. There are four main bodies
of evidence. First, and in common with most other
groups of protists, there is no good evidence that
ciliates have a biogeography (Bary 1950; Bowers
and Pratt 1995; Corliss 1974; Ekebom et al. 1996;
Kristiansen 1996; Lackey 1938; Larsen and Patterson 1990; Ogden and Hedley 1980; Patterson and
Simpson 1996; Sandon 1927; Stout 1956; Tyler
1996). On the contrary, it seems that the same ciliate
species are found wherever their preferred habitat is
found (e.g. Smith 1978). Second, enrichment culture
experiments indicate that local species richness of
ciliates is a significant proportion of the global
species richness (Fenchel et al. 1997; Finlay et al.
1996a). Third, the diversity of free-living ciliate
species described in the international literature is a
relatively small number (close to 3000, after revision), and unlikely to increase significantly in the future (Finlay et al. 1996b). Fourth, ciliates and other
protists have high absolute abundance and, in many
cases, effective passive dispersal (e.g. Maguire
1963; Parsons et al. 1966; Maguire and Belk 1967;
Schlichting and Sides 1969; Kristiansen 1996; Finlay
1997). Much evidence indicates that they are continually being distributed everywhere', and newlyformed habitats such as freshwater ponds and volcanic islands are rapidly colonised (e.g. Holmberg
and Pejler 1972; Scourfield 1944). Free-living ciliates
may, in fact, be ubiquitous.
If we take this assumption of ubiquity and use it to
extrapolate from ecological datasets for relatively
small areas to produce global estimates of the number of ciliate species, will we obtain estimates that
are similar to the global number of nominal ciliate
species? We have tested this proposition, using
large datasets for free-living ciliates in the marine interstitial and in the freshwater benthos. The category 'free-living ciliates' is here defined as all those
extant ciliates that do not live exclusively as gut
symbionts (e.g. rumen ciliates), or as parasites or
symphorionts of specific metazoans. A detailed list
of taxa considered not to be free-living is given in
Finlay et al. (1996b).
Results
The ecological data for numbers and abundance of
ciliate species in marine and freshwater sites are
summarised in Table 1. As we also have data for the
numbers of individuals of each species, the species
abundance data can be illustrated as frequency
curves. Using the original method of Preston (1948),
with log2 octaves on the abscissa (Le. each successive octave represents a doubling in abundance), we
create species curves indicating that most species
are of intermediate abundance, a few species are
very abundant, and some are very rare. A normal
curve superimposed upon the logarithmic abundance data (a 'lognormal' distribution) provides an
adequate fit (Figs. 1a, b). In this case, as is often so
with ecological data, the distribution is truncated, although nearly 'unveiled' (Le. indicating that most
species have been recorded). But this message is
misleading, for it fails to take account of the potential ciliate diversity - the true number of ciliate
species present, but not detected during the timespan of the sampling programme. Many of the cryptic
Table 1. Summary information from ecological datasets with independent estimates for the global number of
ciliate species in the marine interstitial and in the freshwater benthos
Ecological Datasets
Global Estimate Based on:
Number of
ciliates
recorded
Number of
ciliate species
recorded
Extrapolation
from ecological
datasets
Taxonomic
analysis*
Marine
Interstitial
Helsing0r Beach
All marine sites
48186
79342
85
151
597
793
Freshwater
Benthos
Esthwaite Water
All freshwater sites
20486
35837
104
125
732
1370
*Current estimated numbers for all nominal marine and non-marine free-living ciliate species are 1592 and 2152 respectively. These numbers include, for example, planktonic species, many suctorians, and those ciliates found so
far only in soil.
Protozoan Diversity
a
25
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15
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25
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31
10
10
Co
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5
1
1
2
I.
16
256
4096
2 I.
16
256
4096
Individuals per species
Individuals per species
Figures 1a, b. Lognormal distributions fitted to the ciliate species abundance data (log 2) obtained from the marine
interstitial (a) and the freshwater benthos (b). Following Preston's (1948) terminology, the constant a (related to the
logarithmic standard deviation by the equation a =(1/[202])1/2) in the fitted curves takes the value 0.22 (marine) and
0.24 (freshwater). As drawn here, the y-axis is the "veil line", to the left of which lie those hypothetically rare ciliate
species that were not observed in the sampling programme (Le. abundance <1). The bar value shown for these is
an estimate, being equivalent to half of the number of species each represented by a single individual.
(e.g. encysted) and rare species present would have
required specific conditions in order to grow, reproduce and become detectable. Over the extended
periods of the sampling programmes, some of these
would have become detectable but it is likely that
many of the species that were present would not
have been recorded. Some would never have been
numerous, and others would have remained rare because they were migrants from the surrounding area
and beyond who had been transported to a place
where they awaited the arrival of conditions suitable
for population growth. One way to find the rare
species would be to look at a larger area, for that will
probably support additional ciliate niches; so some
species that remained undetected in the original,
small area may find the conditions they require for
population growth (and detection) in the larger area.
If the ecological datasets are plotted as ranked
species abundances (logarithmic), we find that the
curves become linear (Figs. 2a,b): that is to say, the
abundances of the successively rarer species decrease logarithmically. Furthermore, the slopes of
these trends seem insensitive to the size of the
datasets. In Figure 2a for example, the slope for the
Helsing0r Beach data is roughly the same as that for
the larger dataset that includes all the marine interstitial sites. The same message is obvious in the
freshwater data. This feature is consistent with the
idea of the ubiquity of species: if the larger datasets
had included a number of species with exclusively
local distributions, their respective slopes would be
less steep than those for the smaller datasets from
smaller areas.
Now, if our datasets had been much larger, as if
we had examined much larger areas of sediment,
additional ciliate niches would have been included.
We would also have found a proportionate increase
in numbers of the more common species originally
recorded. It is reasonable therefore to extend each
terminal linear trend below an abundance of one ciliate (Figs. 2a, b) to indicate the additional species
that would be recovered by examining a larger area.
Take the example of the marine data (Fig. 2a). The
total number of ciliates found was 79342, and these
c.v
No. of ciliates
No. of ciliates
100000 .
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Figures 2a, b. Rank-abundance plots of the ecological data from the marine interstitial (a) and the freshwater benthos (b). The terminal components in
each are assumed to be linear. a: open symbols represent ciliates in Helsing0r
HelsingeJr Beach; filled symbols, all marine sites (see Table 1). b: open symbols
represent ciliates in Esthwaite Water; filled, all freshwater sites (see Table 2). See text for method of extrapolation. The number of ciliate species estimated for 1m 2 of the marine interstitial is 212 (a), and 234 for 1 m2 of freshwater benthos (b).
Protozoan Diversity
33
6
Figure 3. Species-area relation-
ships for freshwater benthic and
marine interstitial ciliates obtained
by extrapolation from the ecological datasets (upper curve "all
freshwater sites"; lower curve "all
marine sites"), plotted with global
species richness estimated independently from taxonomic analysis
(1'" freshwater benthos; A, marine
interstitial). The origins of the extrapolations are the ecological
data given in Table 1, and the
curves are polynomials (marine interstitial: y =-0.0031x2 + 0.0383x +
2.587; freshwater benthos: y = 0.0021x2 + 0.0433x + 2.669). The
linear least squares regression
computed through the combined
ciliate extrapolations is: y = 0.043x
+ 2.571 ; r2 =0.96 (Le. z =0.043). In
marked contrast, the regression
drawn for the insects (using data
for various regions of the world,
assimilated by Gaston [1992]), has
az value of 0.31.
Insects
5
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In
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-10
belonged to 151 species. This is the total ciliate
complement of 87cm 2 of sediment, and in this area,
the rarest ciliate species was represented by a single individual. Now, suppose that we could record
every ciliate in the 1 m 2 surrounding (and including)
our original 87 cm 2 and that our rare ciliate retained
the same degree of rarity within this enlarged area.
This rare species would now be represented by an
estimated 115 individuals, as illustrated in Figure 2a
by moving vertically upwards to this value. All other
ciliate species will keep the same relative abundances they had in the smaller area, so the linear
slope of the new, upwards displaced, rank-abundance plot will be the same as the original (broken
line terminating with an arrow, in Figs 2a, b). This
new theoretical plot (for 1 m2) indicates that the ciliate with an abundance of 115 individuals per 1 m2
will, when the additional species are added to the
rank abundance plot, terminate the species sequence at 212 species (Le. there are estimated to be
212 species in 1 m 2 , when the rarest species in that
area is represented by a single individual). The same
procedure can be used to extrapolate to areas on a
'global' scale (e.g. 2x106 km 2 - the area of inland
fresh waters in the world) in Figure 3, at which point
o
-5
Log Area (km
5
2
10
)
the projected total is 597 species. When the same
procedure is carried out for the freshwater benthic
ciliates, the projected total is 732 species (Table 1).
Discussion
We find that the global extrapolations are within a
factor of two of the numbers of species derived from
an analysis of species descriptions in the international published literature (Table 1). Furthermore,
there is good reason for believing that the correspondence between the two types of estimate may
be even better than this, because the number of
species estimated from taxonomic analysis is probably still too high. There is no doubt that many synonyms remain embedded in the published literature,
especially in the many crowded genera that require
taxonomic revision (see Finlay et al. 1996b). One
problem that may be unique to the ciliates (and possibly other protists) is the practice of creating new
genera to accommodate the overflow from crowded
genera. This has produced a very large number of
single-species genera (372 out of a total of 774 ciliate genera; Finlay et al. 1996b), making it even more
34
B. J. Finlay, G. F. Esteban, and T. Fenchel
laborious to discover synonyms. Another problem
that is certainly not unique to ciliates is that too
many 'new' species are still being described on the
basis of trivial differences, or in ignorance of species
descriptions that have already been published. One
likely consequence of the resolution of these problems is that our estimates of global species richness
may, in the course of time, show even better convergence than they do at present. In addition, we may
also have some tentative evidence that the extrapolations provide realistic estimates on a local scale.
We are engaged in an intensive long-term study of
the ciliate fauna in a natural, freshwater pond in England (e.g. Finlay et al. 1988; 1996a,c). The number of
ciliate species that are predicted to find suitable
habitats in one hectare (the area of the pond) is 375
(from the polynomial in Fig. 3). Our list for the pond
currently contains 244 ciliate species (only one of
which may be new to science); and although the
number continues to grow with continued sampling
effort, it is becoming noticeably more difficult to
record additional species for this water body.
We have assumed throughout that ciliates are
ubiquitous. Absolute abundance is so large, and
passive dispersal so effective, that every species
has some probability of being transported, at some
point in time, anywhere in the biosphere. Each
species will grow and reproduce where it finds a
suitable habitat, and if the habitats are found in
many different parts of the world, that species will
be considered to have a cosmopolitan distribution.
But perhaps we are mistaken - perhaps we are unable to detect subtle but important differences separating ciliates, so we identify ciliates from different
places as the same species only because we are unable to tell them apart. These separate species
could have different spatial distributions, and in an
extreme case, a ciliate referred to as a cosmopolitan
morphospecies could consist of many similar
species, each with its own geographical distribution.
There is, however, one good piece of evidence indicating that this is not usually the case. In some ciliate genera (e.g. Paramecium and Tetrahymena), a
biological species concept does apply. The different
syngens are in most cases morphologically indistinguishable, and yet they are readily identifiable using
laboratory tests of their mutual reproductive isolation. We would expect this reproductive isolation to
be correlated with geographic isolation, but the evidence is to the contrary. Most syngens in the Paramecium aurelia complex have cosmopolitan distributions (Nyberg 1988), many in the Tetrahymena
pyriformis complex have been found on two or more
continents (Nanney and McCoy 1976), and the apparent absence of species from other regions in the
world might easily be contradicted with additional
sampling effort (Corliss and Daggett 1983). It appears as if those ciliates holding the most promise of
revealing a species biogeography within a common
morphotype, fail to do just that.
A second argument against cosmopolitanism in
ciliates is fuelled by the so-called endemics. New
species do continue to be discovered. Invariably
these come from unusual or previously unexplored
habitats, such as solution lakes (Esteban et al.
1993), wetlands in tropical Africa (Dragesco and
Dragesco-Kerneis 1986 ) or Antarctic sea-ice (Petz
et al. 1995). The relevant point is that these species
are found in these places because of the habitats
that the places provide. This is graphically illustrated
by the species of sea-ice ciliates that appear to be
identical in the Arctic and in the Antarctic (Agatha et
al. 1993; Petz et al. 1995). There is also an undeniable tendency for 'endemics' to acquire a broader
geographical distribution in response to additional
sampling effort, and the true number is probably low
(Fenchel 1993; Foissner 1997). Wilbert and Kahan
(1981) described a very large and unusual ciliate
(Condylostoma reichi) from Solar Lake in Eilat. It was
subsequently found in tropical Africa (Dragesco and
Dragesco-Kerneis 1986), and a ciliate most closely
resembling C. reichi has recently been found in the
Antarctic (Petz et al. 1995). An 'endemic' of the
Hawaiian archipelago (Foissner 1994) was recently
found in wet moss by a river in central Spain (Olmo
and Tellez 1996).
The assumption of cosmopolitanism in free-living
ciliates is, in general, justified, and it may even be
true for the ciliates living in habitats that are relatively rare. These ciliates will have lower absolute
global abundances and (for purely statistical reasons) rates of dispersal that are much lower than
those of ciliates living in common habitats. Ciliates
living and growing on unusual 'islands' that are separated by large distances (e.g. the sea-ice of the
Arctic and the Antarctic) may rarely if ever be detected in intermediate regions; but the evidence
does indicate the reality of global dispersal of these
'island' species, even if the magnitude of this dispersal is small compared to that of the many common ciliate morphospecies co-occurring in common habitats in, for example, the Antarctic, Nigeria
and Scotland.
We have recently (July 1997) obtained some supporting evidence from a real 'island' - a small lake
lying in the crater of an extinct volcano in Victoria,
Australia. We are still adding species to the record
for this water body, but preliminary results indicate
that of the 80 ciliate species recorded, 79 are already known from Northern Europe. The only other
Protozoan Diversity
record for the remaining species (Oxytricha salmastraY is from tropical Africa (Dragesco and DragescoKernt3is, 1986). This directed search for 'endemics'
in a place where we might have had a realistic
chance of finding some, has so far failed to reveal
any.
Species-area relations, and extinctions
Two important features of the species-richness of
free-living ciliates become clear, and both are a consequence of their small size. First, in comparison
with macroscopic animals and plants, individuals
and species are both very densely packed in nature.
A square metre of freshwater benthos will typically
contain 2x107 ciliates represented by 234 species.
The equivalent figures for the marine interstitial are
107 ciliates and 212 species. How do so many
species manage to live in a small area? The answer
is easily explained in terms of 'fractal geometry':
that the world is equally complex at all scales, so for
example 1cm 2 of sediment could be as complex a
habitat for protozoa as a beech tree in mid-summer
is for insects. The reality of this phenomenon will of
course be obvious to anyone who has used a microscope to examine a small sediment aggregate and
found attached peritrich ciliates, Chilodonella and
Aspidisca crawling and browsing over the surface,
Spirostomum and various small scuticociliates filter
feeding in the pore volume, and the neck of an embedded Lacrymaria periodically emerging to grab
algae and other microbial food items.
The second important feature is the low rate of
species addition for increasing area. The best
known general equation for the relation is S = CN,
where S is number of species, A is area, and C and z
are constants that vary from one group of organisms
to another (MacArthur and Wilson 1967). In most
studies where the relationship has been fitted (Le.
the macroscopic flora and fauna of islands), z takes
a value in the range 0.2 to 0.35. The value is usually
smaller (0.12-0.17) when the areas are located
within continents (reflecting enhanced migration between areas); and birds (easily dispersed) have
lower values than land snails. The average slope of
the extrapolation for ciliates in Figure 3 (z = 0.043)
falls well below either of these ranges and is consistent with the high rates of dispersal assumed for ciliates. In this connection it is interesting that Dodson
(1991, 1992) also reports a low value (z = 0.05) for
another group of relatively small and easily dispersed animals - the crustacean zooplankton of European and North American lakes. He too, ascribes
the low value to high rates of immigration from
neighbouring areas.
35
One important implication of the low slope for the
ciliate species-area relationship is that the global diversity of ciliate species is largely unaffected by loss
of habitat. One can readily calculate (e.g. Wilson,
1992) that in the larger metazoans, with a typical zvalue of 0.3, a reduction in habitat area (e.g. of rainforest) to one tenth of its original size, will eventually
lead to loss of one half of the original number of
species. For ciliates (z = 0.043), the same reduction
in area would lead to a 10% reduction in species
number. But even this level of threatened extinction
is probably unrealistically severe, as a specific ciliate
habitat is unlikely to be lost simultaneously from all
places in the biosphere where it exists (and the
same ciliate species probably live in 'rainforests'
that are geographically isolated from each other).
Moreover, at a local level, habitat destruction is perhaps only rarely so thorough that it reduces the
abundance of any ciliate species-population to such
an extent that stochastic extinction becomes likely.
If our extrapolation was based on only one
dataset, the closeness of the global estimate to that
obtained by taxonomic analysis might be considered fortuitous. The fact that the two independent
data sets can each be extrapolated to show the
same general species-area relation and that these
extrapolations converge with the additional independent estimate of taxonomic analysis indicates
that our conclusions are firm: free-living ciliate
species are ubiquitous, many have cosmopolitan
distributions and their global species richness is relatively low.
Methods
Marine data: The localities, sampling techniques
and enumeration methods are described in Fenchel
(1969). Sampling was concentrated within three
main areas, and at water depths down to 22 m: in
the 0resund, the Isefjord area, and in the Baltic
south of Stockholm. The largest data set is from
Helsing0r Beach (Denmark).
Freshwater data: The largest dataset we used
was derived from a study of the benthos of a lake
(Esthwaite Water) in the UK. These data were obtained from monthly sampling in the period October
1978 to November 1981. A total of 228 Jenkin sediment cores were collected. The data from Airthrey
Loch in Scotland (UK) were obtained from examination of 92 sediment cores taken with approximately
monthly sampling at three sites in the period January 1975 to December 1976. The remainder of the
data were obtained from 18 excursions to sample
five shallow freshwater streams on the Jos Plateau
36
B. J. Finlay, G. F. Esteban, and T. Fenchel
in Nigeria, in the period December 1977 to May
1978. The enumeration methods used are described
in Finlay and Guhl (1992). Further information relating to the Airthrey and Esthwaite datasets appears
in Finlay (1980, 1982 respectively).
Taxonomic analysis: The method used in
analysing all ciliate species descriptions published
in the period 1758 to 1996, was published in Finlay
et al. (1996b). The dataset established therein has
been further analysed, with allocation of all free-living ciliate species to one of two categories: marine,
and non-marine. Some ciliates (e.g. Cyclidium
glaucoma) live in the sea and in fresh water, so
numbers of these have been divided equally between the marine and non-marine categories. The
marine category was then further divided - into
those species that are typically interstitial, and
those that are not (e.g. tintinnids and other planktonic ciliates). This procedure is not easily applied
to the freshwater ciliates, of which few can be classified as truly interstitial species. The interstitial
habitat is much rarer in the typically finely-grained
freshwater sediments, and many freshwater ciliates
perform seasonal benthic-planktonic migrations in
response to the development of deep-water anoxia
·(Finlay 1981). But many freshwater ciliates are apparently well-adapted for a permanently planktonic
lifestyle (e.g. many oligotrichs), and we finally allocated species to the freshwater benthos category if
they were not obviously planktonic, and if the
weight of evidence (our personal experience combined with that in the published literature) indicated
that the benthos provided their 'preferred' habitat.
It may be noted that some (perhaps many) 'soil ciliates' also make a living in fresh waters (Foissner
1987); especially in riverine and littoral sediments.
These species are included in our 'freshwater benthos' total in Table 1.
The species concept used throughout is the concept of 'morphospecies' as described in Finlay et al.
(1996b).
Data handling: All data handling and statistical
processes were performed using Microsoft EXCEL
(5.0).
Acknowledgements
This work was supported financially by the Centre
for Ecology and Hydrology (NERC, United Kingdom), The British Council (newIMAGES), and the
Danish Natural Science Research Council. The interim results from Australia are the product of an ongoing collaboration with Prof. PA Tyler, Deakin University, Australia.
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