Download The global diversity of protozoa and other small species

International Journal for Parasitology 28 (199%) 2948
The global diversity of protozoa and other small species
B. J. Finlay*
Institute of Freshwater Ecology, Ambleside. Cumbria LA22 OLP, U.K.
Received 30 June 1997; accepted 25 July 1997
Abstract
It is widely believedthat the numberof speciesof micro-organisms
in the world isextremely large. Here, we offer the
contrastingview-that the numbermay be quite modest.Most of the work reviewedre&rs to the ciliated protozoa. As
with all microbial groups, we must define our concept of “species”, and for ciliates, the “morpbospecies”concept
appearsto be at leastasrobust asany other. Critical examinationof publisheddescriptionsof &l&es provides a “best
estimate”of 3744for the globalnumberof free-living morphospecies.
Of these,‘793areassociatedwith marinesediments,
and 1370with freshwatersediments.In an independentanalysisbasedon extrapolation (assumingthe ubiquity of
species)from ecologicaldatasets,we estimatethe numbersof qecies in marine and freshwatersedimentsa$ 597 and
732,respectively(i.e. within a factor of two of the figuresobtainedfrom taxonomic analysis).This a~entconvergence
of independentestimateswill strengthenif, asis likely, the numberof nominal speciesis further reducedby taxonomic
revision. Theserelatively low numbersof speciesare consistentwith (a) the vast amount of ~1~~
information
indicatingtypically cosmopolitandistributionsfor ciliatesand other microbes,and(b) recentexperimentitievidencethat
most free-living ciliates are rare or cryptic-seldom detectable,but present,and “waiting” for suit&le conditions to
arrive. In summary,mostciliates(and other micro-organisms)areprobably ubiquitous,endemicsare rare, global species
richnessis relatively low, and, at leastin the caseof the ciliates, most specieshave already beendiscovered.C 1998
Australian Society for Parasitology.Publishedby ElsevierScienceLtd.
Key words: &diversity;
protozoa; ciliate; micro-organisms; species richness; cosmopolitan; morphospecies; ubiquity; aggregate
It is not a simpk task to provide accurate estimates of giohal speciesrichnessin any of the larger
taxonomic groups. Even for the well-studied
insects, then? is considerable variation in published
estimates [I]; and with respect to the micro-organisms, the task is generally considered to he rather
difficult [2-l.
The fundamental problem with
micro-organisms is that in many casesthere is only
*E-mail: [email protected].
a fragile consensuson what constitutes a species,
and until that consensusis strengthened, we cannot
have a sound strategy for estimating the global
number of species.
Let us begin by looking at a specific example
within the protozoa. The rich morphofogical variety of ciliated protozoa (Fig. 1) has been investigated for more than 200years, and ciliate
morphology has provided the criteria for defining
species 18-111. However, this practice has not
always been without its prohh~~. The ccmtinuous
development of new metho& @A as E!M) for probing deeper .into the morphology
of cells has
SOO20-7519/98 %19.00+0.00 0 1998 Australian Society for Parasitology. Published by Elsevier Science Ltd. Printed in Great Britain
PII: SOO20-7519(97)00167-7
B. J. Fin&
1 International
Journal for
unravelled layers of complexity and variation that
could not have been imagined 200years ago; but
perhaps the considerable exploratory potential of
these techniques contributes more to illustrating the
fractal geometry of protozoa than to the clearer
definition of species differences. Moreover, some
investigators have better tools than others, and better tools allow more weight to be placed on specific
criteria. Some workers have broad experience of
protozoan diversity in the natural environment;
others have huge experience of variation in laboratory cultures of protozoa. All those who study
ciliates and other protozoa, like all naturalists, tend
to form a personal view of protozoan diversity.
And, like at1 other naturalists, protozoologists tend
Parasitology1
28 i 1998)
31
2948
to fall into one camp or the other--the “lumpers”
or the “splitters”.
It is, therefore, not surprising that if we try to
gain some quantitative idea of species diversity in
the ciliates, we find a rather murky picture. We
find a remarkably large number of synonyms for
nominal species, and genera that endure chaotic
cycles of expansion
and contraction,
with
occasional “revision” into extinction. Improved
clarity might be gained by adopting a more objective approach., and by focusing on specific groups
within the protozoa. Therefore, as a first step, we
have looked at those ciliates that are capable of an
independent existence in the natural environment--the free-living ciliated protozoa.
Fig. 1. A selection from the variety of morphospecies of free-living ciliates living in fresh waters. Those placed towards the top left are
typically found in the open water of lakes; those close to the centre at the base are all anaerobic. The remainder are generally found in
sediments and detritus, and attached to submerged surfaces (e.g., aquatic animals and plants). All are drawn to scale (scale bar = 1 mm).
(Adapted from Finlay et al. [12].) 1. Cinetochilum margaritaceum;
2. Halteria sp.;3. Cyclidium citrullus; 4. Urotricha
sp. 5. Thigmogaster
sp.; 6. Mesodinium
sp.; I. Philasterides
sp.; 8. Chilodonelia uncinata; 9. Litonotur uninucleatus; IO. Cyclidium plouneaurr; 11. Aspidisca
cicada: 12. Lacrymaria
sp.: 13. Halteria grandinelia;
14. Trimyema sp.; 15. Zosterodasys
sp.; 16. Glaucoma scintillans; i 7. Ctedectoma
wilberti; 18. Calyptotricba
lanuginosa;
19. Saprodinium
sp.;20. Cristigera setosa; 21. Cyctidium sp.; 22. Pseudomnicrothurax
dubius; 23.
Sathrophilus
muscorum; 24. Paranophrys
sp.; 25. Askenasia sp.; 26. Metacystis tessehta; 27. Hastatella radians; 28. Bahmanema biceps;
29. Uronema marinum; 30. Cyclidium glaucoma; 3 1. Colpoda cucullus; 32. Dexiotricha
media; 33. Colpidium campylum;
34. Ptacus iuciae:
35136. Tetrahymena
pyrijormis-complex; 37. Placus sp.; 38. Cinetochilum
margaritaceum;
39. Blepharisma
hyalinum; 40. Loxohs
SD.;
41. Paramecium aurelia-complex;
42. Lacrymaria
olor; 43. Tetrahymena
vorax; 44. Entosiphon
sp. (euglenid); 45. Spurhidium suhatum;
46. Pleuronema coronatum;
41. Chilodonella
sp.; 48. Urocentrum turbo; 49. Ileonema dispar; 50. Nassula tumida; 51. Sugittariapoltganalis;
52. Trithigmostoma
cucullulus;
53. Frontonia
leucas; 54. Lacrymaria
elegans; 55. Paramecium
caudatum;
op.; 57. Eqlotes
eienkowski:
63.
61. Gastrostyla
steinii; SK. Styloqxhia
mytilus; 69. Uroleptuspiscis;
70. Lacrymaria
olor; 11. Metopus striatus; 12. Bothrostoma
undulans; 73. Tropidoatractuc
acuminates;
74.
Metopus
sp.; 75. Brachonella spiralis; 16. Caenomorpha
sp.; 77. Caenomorpha
uniseriahs; 18. Saprodinium
dentatum;
19. tsocychdium
globosum;
80. Plagiopyla
nasuta: 81. Metopus
es; 82. Saprodinium
sp.; 83. Cvclidium porcatum;
84. Discomorphellu
pectinata;
85.
Mylestoma
uncinatum;
86. Saprodinium
diffile;
81. Trimyema
compressurn;
88. Vaginicola
crystallina;
89. Ophrydium
versatile;
90.
Trichophrya
epistylidis; 91, Vorticella
natans; 92. Acineta sp.; 93. Loxophyllum
heft*s; 94. Chikodonetla
sp.; 95. Sphaerophrya
magna; 96.
Epistylis sp.; 97. Paruroleptus
caudatus; 98. Stentor sp.; 99. Stentor polymorphus:
100. Dendrosoma
radians; 101. Stylocohz striuta; 102.
Aspidisca cosiata 103. Stentor roeseli; 104. Epistylis flavicans;
105. Nassula picta; 106. Paramecium bursaria; 107. Front&a
sp.; 108.
Deltopylum
rhabdoides;
109. Ophrydium
eichornii; 110. Loxodes striaius; 11 I. Dileptus sp.; 112. Trachelius ovum; 113. Arcuospathidium
vermiforme;
114. Epistylis plicatilis;
115. Kahlilembus
attenuatus;
116. Endosphaera
terehrans;
117. Vorticella
mayert;
118. Litonotus
Cygnus; 119. Amphileptus
sp.; 120. Litonotus Cygnus; 121. Litonotus fasciola; 122. Loxophyllum
hems; 123. Litonotuv
fi-tsriofa:
124.
Loxophyllum
sp.; 125. Hastatella
aesculacantha;
126. Hastatella
radians; 127. Phascolodon
vorticella;
128. Scrombidmm
aclox: 129.
Bursaria
truncatella;
130. Urozona bti’tsehlii; 13 1. Disematostoma
gyrans;
132. Urotricha fircata;
133. Monodinium
balbiani;
1.34.
Actinobolina
sp.; 135. Urotricha furcata; 136. Tintinnopsis sp.; 137. Bursaridium
pseudobursaria;
138. Prorodon
palurlris;
139. Histiobalantium
ma&s; 140. Balanion planctonicum;
141. Hypotrichidium
conicum; 142. Dtsematostoma
(Leurophrys)
tetraedrica:
143.
Tintinnopsis
laeustris; 144. Lembadion
sp.; 145. Enchelyomorpha
vermicularis;
146. Tintinmidium fluviatile;
147. Platynamatum
so&/e;
148. Prorodon ovum; 149. Pleuronema
sp.; 150. Urotricha sp.; 151. Halteria sp.; 152. Strombidium
sp.; 153. Strombidium
sulcatum; 154.
Coleps sp.; 155. Coleps hirtus; 156. Prorodon
discolor; 157. Codonella cratera; 158. Strombidium
viride; 159. Pro&on
sp.: 160. Promdon
sp; 161. Bursel~opsisgargamellae;
162. Frontonia
acuminata;
163. Strobilidium
adhrrens;
164. Spirosromum
sp.; 165. Spiro.~tomum minus:
I66 Homalozoon
vermiculare;
167. Vorticeffa sp.
sp.; 58. Drepanomonas
revoluta;
59. Tachysoma
sp.; 60. Tachysoma pellionella; 61. Styiomychia
Holosticha
sp.; 64. Keronopsis monilata; 65. Ancystropodium
maupasi; 66. Urosoma cienkonski;
56. Lacrymaria
putrina; 62. Urosoma
32
B. J. Finlay
1 International
Journalfor
Parasitology
2. The discovery of new ciliate species-historical
trends
Figure 2 illustrates the history of the discovery
of new free-living ciliate species, from the year 1758
until the end of 1993. These species belong to 774
genera. One genus (Spathidium) contains at least
100 species, and no fewer than 372 genera are represented by a single species. The rate of description
of new species has varied greatly over time. There
are correlations with historical events such as world
wars, and peaks of taxonomic activity can be allocated to specific individuals or groups of individuals, e.g., Ehrenberg and Dujardin around
1830-1940; Faur6Fremiet
and Penard around
1920, and massive peaks in the 1920s and 1930s
due, especially, to the efforts of Kahl. Dragesco et
al. are largely responsible for the peaks in the 1950s
and 196Os, and Foissner et al. for those in the 1980s.
The underlying rising trend in the number of species
described in the period since 1945 is about 1% per
annum.
In our analysis of this literature, we encountered
two related problems. The most obvious was duplication-the
same organism being described under
different names by different (and sometimes the
same!) taxonomist. The second problem was the
apparent lack of objective criteria for defining species-how different do two organisms have to be to
have the status of separate species? Each of these
problems, of synonyms and species concepts, is now
considered.
28 (1998)
2948
200
(4
1750
I
1800
1850
1WJO
I
1050
moo
1
(b>
L
s
4
2OOQ
g
CJ 1000
3. Synonyms and revisions
The rate of change in the number of nominal
species depends on opposing forces-the naming of
new species, and taxonomic revisions. These forces
are obviously unequal in strength, because the number of nominal species continues to rise. Of course,
genuinely new species are found, but we must also
consider the problem of ignorance of what has previously been published, with the consequence that
the same organism is described with different
names. These names may subsequently be judged
to be synonyms (see Fig. 3).
Taxonomic
revision will reduce the rate of
0
1750
I
18OQ
1850
1900
1950
2000
Year
Fig. 2. (a) The number of new species of free-living ciliates
described each year. (b) The cumulative number of new species
of free-living ciliates described in the international literature from
1758 until the end of 1993. (Adapted from Finlay et al. [12].)
l
Fig. 3. Taxonomic history of the ciliate genus Loxo&s. Arrows
are used to connect equivalent species, “forms” and “types”. We
have considered only those species that can be unambiguously
integrated into the taxonomic history of the genus. Broken lines
indicate that the connected species may not be identical. Boxes
indicate a statement by the original author that Loxodes exists
only as three conspecific “forms” or “types”.
B. J. Finlay
/ International
Journal
for Parasitology
28 (1998)
vii
“TiF
____------_-_----------------------------I
L----.i‘e-g~swwTm’
c-------___---&.;.;-,--_-___----___
-‘:
i--+; ----!qr+ -_--____-4: ----!
LA-
+&&
.“sq
qdL.
Ln!k
q*IUS
1
r-----: fk
---7-c
--------__------__
L-Qsy-
*-
A
i
29-48
34
B. .I. Finlay
/ International
Journalfor
increase in the number of new species. Consider
again the extreme example of Spathidium. The
genus has not been revised in the last 60years. It
currently contains more than 100 species, and many
are very similar to one another. How can it be
justified to squeeze more “new” ciliates into such a
genus before rationalising the existing complement
of nominal species? And if we look at the 730 “new”
ciliate species described in the period 1978-1993,
we find that many have been allocated to “old”
genera; in fact most are placed in genera that have
not benefited from revision since 1935, and some
have never been revised. More than half of the
recent increase in the number of new species is due
to species allocated to genera that are probably in
need of revision. Taxonomic revisions are a potent
force in rationalising the numbers of nominal species. In most recent, authoritative revisions, the number of nominal species has been reduced to about
half, or less, of the original number [ 121.
4. Species concepts
One factor that contributes greatly to the rising
number of new ciliate species is the lack of a solid
species concept. At present, the boundaries between
species are often unclear, and the probability of a
new species being “discovered” and described often
depends on the techniques and other resources that
are available at the time. It is abundantly clear that
we need a practicable concept of species that can
be applied throughout the whole range of the freeliving ciliates.
5. Biological species
Within many nominal species, discrete populations probably exist, between which gene flow is
restricted or non-existent.
These populations,
known as syngens, sibling species or biological species (the terms are largely interchangeable), are often
difficult, even impossible to separate on morphological grounds. Paramecium aurelia is one of
the best studied of these ciliates, and it has been
shown to comprise at least 14 sibling species [13].
But let us take a step back, and look for a moment
Parasitology
28 (1998)
2948
at the ciliates as a whole. We find that they are
remarkably diverse in the repertoire of their sexual
habits, and some manage with no sex at all. We find
outbreeders with multiple mating types, inbreeders
performing intraclonal conjugation, autogamous
ciliates practising self-fertilisation, and forms that
are apparently incapable of sex, and so permanently
asexual. Paramecium bursaria can form conjugation
triplets, with the third partner carrying out autogamy [14], and up to half of the Tetrahymenas isolated from nature were found not to have a
micronucleus [ 151, so they were asexual. Are sibling
species relevant to our quest for a practicable species concept for ciliates? The answer, I believe, is
“no”; but let us look at some of the evidence.
Paramecium caudatum consists of at least 16
sibling species, but mating is known to occur among
four of them [16]. A further complication is that
mating type is not always fixed.
The Tetrahymena pyriformis complex currently
consists of 16 sibling species [ 171. Four are amicronucleate, and thus incapable of mating. Two
others can mate with each other, with the production of viable progeny.
Valbonesi et al. [18] collected 120 strains of
Euplotes crassus, of which 38 were observed to
mate. These were placed in groups: strains in one
group could mate with those in a second group, but
not with strains in a third group. Strains in the
third group would, however, mate with those in
the second group; so genetic exchange could occur,
directly or indirectly, among all 38 strains. Such
complex mating behaviour cannot be rationalised
in terms of any practicable biological species
concept.
Although
they are undoubtedly
biologically
interesting, we might question the contribution that
biological species make to the business of characterising ciliate diversity. A biological species concept cannot be applied to sexless and inbreeding
ciliates; nor to the complex “mating continuum”
found in ciliates such as Euplotes. Mating between
sibling species can occur, and only a small fraction
of the total number of sibling species, and of the
inventiveness of their sexual exploits, is ever likely
to be known.
The diversity of cultured tetrahymenine ciliates
has also been subjected to sequence analysis of
B. J. Finlay / International Journal for Parasitology 28 ( 1998) 29-48
rRNA. Nanney et al. [19] and Jerome and Lynn
[20] found that they fell into distinct groups, or
“ribosets”. One riboset emerged with eight morphologically identical species that were “ribosomally”
identical,
and yet all were different,
biological species. So, what do these sibling species
tell us about ciliate diversity? Two morphologically
identical species can be reproductively isolated from
each other, but “ribosomally”
identical. A further
pair of morphologically
identical species can be
reproductively isolated, yet “ribosomally”
quite
different from each other. In Tetrahymena, at least,
genetic isolation and genetic divergence appear to
be poorly
correlated,
although
morphology
remains fairly constant. The most plausible explanation is that stabilising selection has preserved
the typical tetrahymenid morphological phenotype
because it probably represents some adaptive peak
[21]. In other words, evolution has preserved the
morphology
that allows representatives of the
genus Tetrahymena to continue to carry out the
same core ecological functions (e.g., bacterivory in
organically-rich particle aggregates) irrespective of
the variation that has arisen in their reproductive
behaviour and in their ribosomal DNA.
In any event, the number of sibling species
described so far is not quantitatively important.
Approximately
2000 morphological
species have
been described in the past 50 years. For sibling species in the same period, the figure is just over 100.
2.
3.
4.
5.
6. Tbe cibte mqWspecies-towards
operatioaal deSinitio0
an
In ecological studies in particular, “species diversity” of ciliates usually means diversity of form and
function [22]. For this reason, the “morphospecies”
can be used as a pragmatic definition of “species”:
a collection of forms that fit into a defined range
of morphological
variation; and, most important,
forms that apparently occupy the same ecological
niche. A ciliate morphospecies might have the following characteristics:
1. Morphospecies and the ecological niche. Form
and function are closely correlated in ciliates,
e.g., “worm-like” interstitial karyorelictids; per-
15
itrich
stalks;
the adoral
membranellar
“umbrella” in planktonic oligotrichs. If two eiliates are morphologically
identical or very nearly
so, then it is likely that they occupy identical
or very similar niches. In particular, they will
probably feed in the same way, on the same types
of food particles, in the same type of habitat.
Morphological
limits. A morphospecies can be
defined in terms of limits for various morphological characteristics (e.g., cell length, number of kineties,
argyrome
type). Some
characteristics (e.g., the number of k&reties and
the number of ciliary units they contain) may be
extremely variable and scale with cell size, clonal
age, and other factors 1231; but others will be
conservative (e.g., argyrome type, type of oral
apparatus). The morphological
limits will be
derived using data from a large number of ceils,
from a range of physiological states (see Fig. 4).
Global distribution. A morphospecies is usually
cosmopolitan in its distribution, and it will thrive
wherever it finds a suitable habitat. Variation in
some features (e.g., the continuous
morphological variation in tintinnid loricae [24])
may be correlated with geography.
Siblings selfers and sexless species. The morphospecies may consist of sibling species, amicronucleate-asexual cells, obligatory selfers, and
cells that do not or cannot mate. Crme flow may
occur between different sibling species; either
directly, or through intermediates.
Correlation with molecular characteristics. It may
be possible to divide a morphospecies into
groups, using defined molecular techniques. If
these groups cannot also be ascribed specific
morphological characteristics, there may be little
justification for referring to them as discrete
species.
7.
In many cases, the relevant features of both form
and function may have less to do with the ciliates
themselves than with functional
associations
involving ciliates and other micro-org;tnisms. Many
free-living ciliates, perhaps the majority, harbour
36
B. J. Finlay
/ International
Joumal,for
Parasitology
28 (1998)
2948
130 . .
“0
10
50
I
150
I
250
1
350
450
550
650
Cell length (urn
Fig. 4. Non-overlapping distributions of morphological characteristics (length of oral aperture and length of cell) in two species of the
genus Loxodes (L. magnus and the smaller L. striates). (Adapted from Finlay and Berninger [80].)
symbiotic micro-organisms
[25, 261 or organelles
(e.g., chloroplasts) sequestered from micro-organisms [27, 281. Most anaerobic ciliates have endosymbiotic methanogens that act as hydrogen sinks
[29]; in Paramecium, symbiotic bacteria confer killer
traits upon the host [30]. Half of the biomass of the
marine interstitial ciliate Kentrophoros consists of
ectosymbiotic sulphide-oxidising bacteria which the
ciliate farms as a food source [3 I]. An extraordinary
diversity of freshwater ciliates harbour unicellular
algae that photosynthesise inside the host ciliate
[25, 321. These associations are usually permanent
or, as in the case of sequestered chloroplasts, continuously re-formed. In all cases, two or more genomes permanently co-exist but-more
importantthe relevant phenotype is not that of the ciliate
itself, but that of the consortium. Take the example
of Euplotes daidaleos, a ciliate that contains symbiotic green algae (Chlorellae). Like many other
freshwater ciliates, E. daidaleoshas a preferred spatial niche (Figs 5 and 6)-at, or just below, the oxicanoxic boundary in the stratified water column of
a pond or lake-a place where it is largely free from
predation by aerobic metazoans. Different ciliate
species have different methods of coping with life
in a low-oxygen environment [29, 33-351. Euplotes
daidaleosmanages because it makes use of its algal
symbionts. It lives at a depth in the water column
where there is just enough light for the consortium
to carry out net photosynthesis: the symbionts provide all the oxygen required for aerobic respiration
by the ciliate, so the consortium becomes an aerobic
“island”
surrounded by anoxic water [36]. In
addition, by living where it does, the consortium is
exposed to an elevated concentration of free carbon
dioxide which diffuses from the underlying sediment. This ensures that photosynthesis by the symbionts is not carbon limited, so the ciliate can
receive part of its requirement for organic carbon
from the sugars produced and secreted by the symbionts. In this case, the ecological niche is filled not
by a ciliate, but by a symbiotic consortium that
incorporates a ciliate, and it is the phenotype of the
consortium on which evolution will operate.
B. J. Finlay
/ Iniemational
Journal
Fig. 5. The ciliate EupZotes daidaleos (length 90 pm), packed with
photosynthetic endosymbionts (zoochlorellae).
The ciliate was
retrieved from anoxic (illuminated) water in a pond. Note the
accompanying 16-41 cluster of the anaerobic, photosynthetic
bacterium Thiopedia, present at the same depth in the water
column. (Adapted from Finlay et al. [36].)
There are published reports that ciliates can lose
their symbionts when they are cultivated in the laboratory (e.g., the methanogen endosymbionts of the
anaerobic ciliate Trimyema compressurn[37]). One
possible reason is that the characteristics that contribute to fitness in nature may be rather different
to those that are relevant in laboratory cultures,
and the morphospecies that is selected for in the
laboratory may in a sense be an artefact, differing
in some important respects from its symbiont-carrying antecedents in the natural environment.
In nature, ciliates may invariably reproduce
themselves in asexual clones. Mutations in these
for Parasitology
28 (1998)
2948
37
clones may produce morphological
variants, but
these may be so minor that they do not reduce
significantly the overall fitness of the organism.
Propagation of these mutations in asexual clanes
will produce iuzdepen&nt lineages with slightly
divergent morphotypes. There are several consequences: the boundaries of the morphospecies may
become rather fuzzy; a morpbaspecies may, in the
course of time, produce enough variants to fill out
a continuum of forms; and “conservative” morphological characters may show systematic variation (e.g., in Euplotes minuta the number of
longitudinal
ciliary rows changes with clonal age
[23]). One way to handle this problem may be to
borrow and adapt a device used in plant taxonomy
[38]. (NB Higher plants, too, support a very large
number of typically asexual species-e.g., dandelions). The solution is the “aggregate”.
An aggregate is nothing more than a device of
convenience, used to group together two or more
nominal species that are morphologically
similar
and difficult to separate. In the case of ciliates, an
aggregate would have three key characteristics: (a)
it would have no formal taxonomic m;eaning, {b)
its name would be permanent, and unaffected by
translocations of the nominal species it contains,
and (c) it would have no particular phylogenetic
significance. Under what circumstances would
nominal species be grouped together in an aggregate?
1 When they cannot consistently be separated
from each other, or when they lie in a continuum
of overlapping forms (e.g., cifiates of the cirrotype 10, double argyrome [Euplotes charon]
morpbtypej.
2. When sibling species cannot be discriminated
(e.g., T. pyriformis agg. and
morphologically
Paramecium aurelia agg.).
3. When nominal species can be separated only
with molecular methods OF EM of intra-cellular
structures (e.g., mitochondria),
or on the basis
of differences in their geographic distribution.
Adopting this procedure, one can envisage that part
of a ‘%pecies” list from an ecological project in the
future would look something like the following:
38
B. J. Finlay
/ International
Journalfor
agg.
contains at least 13 overlapping nominal species [39]
Halteria viridis agg.
contains at least five (probably indistinguishable) nominal
species of Halteria and Pelagohalteria
with zoochlorellae
Loxodes magaas Stokes, 1887 (morphospecies)
Loxodes striatas (Engelmann, 1862) Penard, 1917
(morphospecies)
Metopus palaeformzs
Kahl, 1927
a morphospecies with several synonyms [40] and a polymorphic life-cycle
Paramecium
aurelia agg.
contains all sibling species (primaureiia
quadecaurelia)
Eupiotes
Parasitology
28 (1998)
29-48
9. Estimating the global number of morpbospecies
charon
From our examination of the published literature, the current best estimate for the number of
nominal free-living ciliate species is 3744. We would
expect this number to remain fairly stable in the
future, or to be reduced, possibly to around 3000,
in response to new taxonomic revisions of crowded
genera. But how good an estimate is this of the
global number of ciliate species? In order to answer
this question, we have focused on habitats that are
relativelv well-studied-the
marine interstitial and
the freshwater benthos.
0
I
Ciliates without
symbiotic algae
I
Ciliates with
symbic .calgae
Photo irradiance @mol mqs”) l
1
10
20
I
’
30
I
9
40
I
-
0, (mol m’“)
0.2
0.4
2.5
Free COS1(mol ni”)
0
Fig. 6. Vertical distribution of free-living ciliates, with and without photosynthetic endosymbionts, in the water column of a freshwater
pond. Ciliates with endosymbionts produced a distinct abundance peak at 2.6m where there was no detectable dissolved oxygen in the
water. (Adapted from Finlay et al. [36].)
B. J. Finlay / International Journalfor Parasitology 28 (1!?98) 29-48
We assume that microbes in general, including
ciliates, are ubiquitous. In some places they may be
extremely rare or present only as the occasional cyst
or other cryptic form, but there is a reasonable
chance that a species can be found, at least periodically, anywhere in the biosphere. This would be
due mainly to passive dispersal which in terms of
absolute numbers is responsible for dispersal of
phenomenally
large numbers of protozoa. The
agents involved would include hurricanes and tornadoes, convective transfer into the atmosphere
(with subsequent deposition in rainfall), transport
by flying insects and in the damp fur and feathers
of migrating animals, in ground water, in the ballast
of marine tankers, etc. There is a large literature
on this (see [41-44]). If we take the assumption of
ubiquity and use it to extrapolate from ecological
datasets which relate to relatively small areas, will
we obtain global estimates that accord with those
obtained by taxonomic analysis? We have tried to
answer this question, using large datasets for freeliving ciliates in the marine interstitial and in the
freshwater benthos. The marine sites were in Scandinavia, predominantly
Denmark. The freshwater
sites were in the United Kingdom and in Nigeria.
The summary data for the numbers of ciliates
and ciliate species recorded in these studies appear
in Table 1. If these data are then plotted as ranked
species (logarithmic) abundances, we find that the
curves have linear terminal components (Fig. 7);
that is to say, the abundances of the successively
rarer species decrease logarithmically.
Furthermore, the slopes of these trends seem fairly insensitive to the size of the datasets. The slope for the
Esthwaite Water data is roughly the same as that
39
for the larger dataset that includes all the freshwater
benthic sites. 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
would have been the case if we had examined much
larger areas of sediment, we can safely assume that
some very rare species would have been revealed.
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 to indicate the additional species that would
be recovered by examining a larger area. This process is best described with an hypothetical example,
as shown in Fig. 8. This shows an unusually simple
community of ciliates, but it serves to illustrate the
procedure. The inner circle represents 0.05cm2 of
sediment. It contains only three species, represented
by 100, 10 and 1 individuals, respectively. Now,
suppose that we could record every ciliate in an
area of sediment 10 times as large (i.e. 0.5 cm’),
surrounding and including the inner circle. Our rare
ciliate represented by only a single individual in the
smaller area would, if it retained the same degree
of rarity within the enlarged area, now be represented by an estimated 10 individuals. Moreover,
all other ciliate species will keep the same relative
abundances the:y had in the smaller area, so the
slope of the new, upwards displaced, rank-abundance plot will have the same slope as the original.
This new theore!.ical plot (for 0.5 cm’) indicates that
Table 1
Summary information for ecological datasets
-___Marine interstitial
Freshwater benthos
Number of ciliates recorded
and identified
Helsingrar Beach”
All Marine Sites”
48 186
79 342
Number of ciliate species recorded
_____....._ -...-.. ~_._-.-.. -85
151
Esthwaite Water”
All freshwater sitesb
20 486
35 837
104
125
“Fenchel[8 11.
“Finlay [82. 831; Finlay et al. [36, 841.
40
B. J. Finlay
1 International
Journalfor
Parasitology
28 (1998)
29-48
No. of ciliates
looooo
+
1000
100
10
0
20
40
60
80
100
120
140
Species sequtaee
Fig. 7. Rank abundance plots for ciliate species recorded from the sediment of a freshwater lake (Esthwaite Water, in England) over a
period of 2 years, and from a variety of lakes and rivers (“all freshwater sites”) in the U.K. and in Nigeria. See Table 1.
B. J. Finlay / International Journalfor Parasitology 28 11’998) 2948
ciliaee
41
sumber
10000 t
.'..._
t
w.
. . . . ..(f*
.....
I‘\
,
..
0.05 cm2
..,JOO
‘,..t
Al
_. -I 1*-,---&-
\
t
\
e‘,
\\
4 *\ \
\
Fig. 8. An illustration of the method of extrapolating from ecological datasets, with the assumption of the ubiquity of species, using a
hypothetical benthic ciliate community. The community is unusually simple in terms of the number of species, but overall ciliate
abundance per unit area is typical of real communities in natural sediments. The three species found in the smaller area keep the same
relative abundances in the larger area, but as area increases, additional rare species are encountered. Sampling progressively larger
areas produces parallel, upwards-displaced rank abundance plots (top right) each of which retains the key character that successively
rarer species decrease logarithmically in abundance (compare with real data in Fig. 7).
the ciliate with an abundance of 10 individuals per
0.5 cm2 will, when the additional species are added
to the rank abundance plot, terminate the species
sequence at four species (i.e. there are estimated to
be four species in 0.5 cm’, when the rarest species
in that area is represented by a singe individual).
The same procedure can be used with real data,
to extrapolate to areas on a “gfobar’ s&e (e.g.,
42
B. J. Finlay
] International
Journalfor
Parasitology
2 x lo6 km’-the
area of inland fresh waters in the
world). If we do this, the projected total is 597
species for the marine interstitial, and 732 species
of freshwater benthic ciliates.
How realistic are these extrapolations from ecological data obtained for relatively small areas? We
find that they are within a factor of two of the
numbers of species derived from an analysis of species descriptions in the international published literature (Fig. 9). Furthermore, there is good reason for
believing that the correspondence between the two
types of estimate may be even better than this,
because, as discussed above, the estimate from taxonomic analysis is probably still too high. So, our
converging estimates of global species richness may,
in the course of time, flow even closer to each other
than they do at present.
These estimates are also in line with some
published, authoritative guesses. After examining
marine interstitial ciliates in different parts of the
world, Dragesco [45] suggested that “the total number of mesopsammic ciliates must certainly exceed
600”. Some, however, may question our estimates
as being rather low (e.g., [46]), for we are saying
that there are only 1300-2200 niches for free-living
ciliates living in marine and freshwater sediments.
Unfortunately it is difficult to carry this argument
THE GLOBAL
NUMBER
28 (1998)
much further because it is even more difficult to
characterise the niches of ciliates than it is to
describe ciliate morphospecies. Moreover, a potential ciliate niche with an adequate supply of suitable
bacteria or micro-algae as food may also be a potential niche for some heterotrophic
flagellates,
gastrotrichs, rotifers, nematodes and other microfauna. Ciliates may not have unhindered access to
such a wide variety of niches as is commonly
imagined.
10. Cosmopolitanism
and endemics
We have assumed throughout that the great
majority of ciliate species probably do have cosmopolitan distributions and that as a consequence,
their global species number is limited. What evidence is there for this?
As with most protists [44,47-561, there is no good
evidence that ciliates have a biogeography. On the
contrary, it seems that the same species are found
wherever their “preferred” habitat is found (e.g.,
[571). Second, local species richness seems to be a
significant proportion of global species richness.
The number of ciliate species that can be recovered
OF FREE-LIVING
Summary information
29-48
CILIATE
SFECIES
from independent datasets
Taxonomic analysis
total piiJ
Lt
marine n1592
tit
marine
interstitial
17931
15971
t
121521 non-marine
d\
m
17821
other
marine non-marme
Other.
K
113701 ftwhwa&r
m
beathos
f
Extrapolation from
ecological datasets
Fig. 9. The convergence
of independent
estimates (from taxonomic
analysis, and by extrapolation
global number of free-living
ciliates living in the marine interstitial
and in the freshwater
benthos.
from
ecological
datasets),
for the
B. J. Finlay
/ International
Journal
from 100 cm’ of freshwater or marine sediment represents lO-20% of the global species number [58,
591. Third, the diversity of free-living species that
have been described in the international literature
is relatively small and unlikely to increase significantly in the future [12]. Fourth, ciliates and
other protists have high absolute abundance and,
in many cases, effective passive dispersal (e.g., [4,
43, 44, 60-633). They are continually being distributed “everywhere”, and newly-formed habitats
(e.g., freshwater ponds) are rapidly colonised (e.g.,
[64, 651). Protists are, in fact, ubiquitous.
But perhaps this assumption is suspect-perhaps
we are unable to detect subtle but important differences separating species, so we identify ciliates from
different places as the same species only because we
are unable to tell them apart. A “cosmopolitan
morphospecies” could consist of many similar species, each with its own geographical distribution.
There is, however, one piece of evidence indicating
that this is not usually the case. In those ciliate
genera in which reproductively isolated populations
(sibling species) are known, we might expect this
reproductive isolation to be correlated with geographic isolation, but the evidence is to the
contrary. Most sibling species in the P. aureliu complex have cosmopolitan
distributions
[66], and
many in the T. pyrifarmis complex have been found
on two or more continents [67, 681. Strains of
Stylonychia Iemnae isolated in North America conjugated with those isolated in Europe, producing
viable ex-conjugants; and the two groups of strains
were genetically very similar [69]. It appears as if
those examples holding the most promise of revealing a species biogeography within a common morphotype, fail to do just that.
A further argument against cosmopolitanism
is
fuelled by the so-called “endemics”. These tend to
be found in unusual or poorly-studied habitats,
such as solution lakes [70], wetlands in tropical
Africa [9] or sea-ice in the Antarctic [71]. But is it
not likely that “endemics” are found in these places
because of the habitats that the places provide?
Perhaps, if the habitat was found elsewhere, we
would find the same species there also. A good
example is provided by the “endemics” of Antarctic
sea-ice that were subsequently found in the Arctic
[71, 721. And there are many other examples. Wilbert and Kahan [73] described a very large and
for Parasirologv
28 ( 1998)
29-48
43
unusual ciliate (Condylostomu reicki) from Solar
Lake in Sinai. Iit was subsequently found in tropical
Africa [9], but before it could acquire the epithet of
a pantropical distribution, Petz et al. ]71] described
a Condyloston;ra in Antarctic sea-ice which, they
believed, most closely resembled C. reichi.
Endemics tend to acquire a broader geographical
distribution
in. response to additional sampling
effort.
Thus
Bryometopus
hawaiiensis,
an
“endemic” of the Hawaiian archipelago [74], was
soon found in wet moss by a river in central Spain
[75]. There are many other exmples from nonciliate protists. Among the more spectacular of
recent discoveries is the ana.e~obir
with long rod-,shaped bacteria, discovered in the
deep anoxic basin of Mariager Fjord in Denmark
and named Postgaardi ?riar@pem& (Fig. 10) [76].
The basin is separated from the sea by a 20 km-long
channel of oxygenated brackish water. 14n identical
flagellate has now been found in the anaerobic,
sulphidic zone of a meromictic lake in the Vestfold
Hills of Antarctica [77].
11. Ubiquity
Ciliate species are ubiquitous, and if they find an
appropriate habitat on different continents they will
be termed cosmopolitan. This is so, even for species
living in habitats that are relatively rare. Those
living and growing on unusual “islands’” that are
separated by large distances (e.g., the sea-ice of
the Arctic and the Antarctic) may never have been
detected in intermediate regions, but the available
evidence does indicate the reality of global dispersal
of these “island” species, even if the magt&ude of
this dispersal is small compared with that of the
many common ciliate morphospecies co-occurring
in common habitats.
But if ciliates are ubiquitous, we should, with
sufficient patience, be able to find them in any suitable sample of the natural environmeat. This is
what we have now begun to do. We simply took a
small sample of sediment from a freshwater lake
and, in a separate experiment, a small sampie of
marine sand, and manipulated them to produce a
variety of niches for the wide range of cift‘ate species
that we suspected might be present. The manipu-
44
B. J. Finlay
1 International
Journal for Parasitology
Fig. 10. The anaerobic flagellate Postgaardi mariagerensis
with
ectosymbiotic bacteria, recently found in the deep, anoxic basin
of a Danish fjord (Fenchel et al. [76] [including illustration]),
and in the sulphidic layer of a freshwater pond in the Antarctic
(Simpson et al. [77]).
lations involved treatment of sediment with various
temperatures, redox gradients, food sources, light
regimes, etc. and various combinations of these.
These simple procedures did create niches for population growth by a previously hidden diversity of
ciliate species. Although only 20 species could be
detected in a small volume of sediment freshly col-
28 (1998)
2948
lected from a small pond, subsequent manipulations encouraged the growth of a total of 135
species over a 3-month period (Fig. 11). It is likely
that with more patience, and more imaginative
manipulations
of sediment, further ciliate niches
would have been created and an even greater variety
of “ubiquitous” ciliates would have revealed themselves. The total for the pond is now (as at June
1997) 203 species, and the number continues to
increase as new micro-habitats within the pond are
examined in detail. This total, from this one small
pond, represents about 20% of the total for freshwater benthic sites worldwide, so local species richness is a significant proportion of the global species
number-as
we would expect for a group of predominantly ubiquitous organisms.
Perhaps an even more impressive example is
afforded by the representatives of the chrysomonad
genus Paruphysomonas living in the same l-hectare
pond. At present, 50 described species are known
from around the world-all
of them discriminated
on the basis of the scale morphology (incidentally,
only a single species was known until these flagellates were examined in greater detail using EMsee Andersen [78]). Recent examination of a few
millilitres from the sediment-water interface in the
pond has so far uncovered 27 of these 50 species
(KJ Clarke, personal communication).
Finally, we can illustrate just how different is
global biodiversity at the microbial level. Although
a large proportion of all microbial species can be
found in a small area, the rate of addition of new
species falls off rapidly with increasing area
sampled. The best known general equation for the
species-area relation in macroscopic animals and
plants is: S= CA”, where S is number of species, A
is area, and C and z are constants that vary from
one group of organisms to another [79]. In most
studies of the macrofauna and flora of islands and
continents, z takes a value in the range 0.12-0.35.
The value is usually lower (0.12-O. 17) for organisms
such as birds that are easily dispersed, and it is
higher for animals such as land snails living on
islands. The average slope of the species-area
relation for ciliates (z=O.O43; Fig. 12) falls well
below either of these ranges. This is consistent with
the high rates of dispersal assumed for ciliates, other
protozoa and probably all free-living micro-organisms, providing yet another illustration of the theme
B. J. Finlay / International Journal for Parasitology 28 (I1998) 29-48
45
46
B. J. Finlay
/ International
Journal for Parasilology
28 (1998)
insects
Ciliates
29-48
= 0.31
= 0.04
6
5
1
T
-10
-5
0
5
10
Log Area (km2)
Fig. 12. Species-area relationships for free-living ciliates obtained by extrapolation from two large independent ecological datasets (see
Table 1): upper curved line, freshwater benthos; lower curved line, marine interstitial. The two superimposed triangles mark the global
estimates from taxonomic analysis for freshwater benthic (open triangle) and marine interstitial (filled triangle) ciliates. The latter are
in fair agreement with the low slope extrapolated from the ecological datasets, with the assumption of species ubiquity. This is in
marked contrast to the much higher slope of the regression drawn for the insects (using data provided by Gaston [l]) which, like most
macrofauna and flora, do have a biogeography. (Adapted from Finlay et al. [85].)
that has run through this presentation: most ciliates
(and other micro-organisms) are probably ubiquitous, endemics are rare, global species richness is
relatively low and, in the case of ciliates, most species have already been discovered.
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