Jpn. J. Protozool. Vol. 40, No. 1. (2007)

1

Review
Dispersal and Biogeography of Protists: Recent Advances
Wilhelm Foissner
Universität Salzburg, FB Organismische Biologie, Hellbrunnerstrasse 34, A-5020 Salzburg,
Austria

SUMMARY
This review summarizes recent progress inthe debate on distribution of micro-organisms,
especially protists. I present three fundamental
evidences for restricted distribution of protists,
viz., a study on global soil ciliate diversity whichshows a “meaningful” distinction of Laurasian and
Gondwanan ciliate communities; flagship and vicarious testate amoebae and ciliates which are too
conspicuous to be overlooked in Europe, if they
were there; and spore-forming cryptogams whichshow that minute sizes and high abundances do nothabitually cause cosmopolitan distribution. Regional and local protist endemism and factors restricting the distribution of micro-organisms are
discussed. The most misleading generalizations area tendency to consider protists as a homogenous
group with similar properties and high abundances.
Actually, however, protists are highly diverse andmost species have low or very low abundances, as
obvious from frequency distributions which are

Tel: +43(0)662 8044 5615; Fax:+43(0)662 8044 5698
E-mail: Wilhelm.Foissner@sbg.ac.at(Received: 18 Novenber 2006)

highly similar to those of flowering plants andanimals. The data available are consistent with the“moderate endemicity model” which suggests
about 30% of morphological and/or genetical and/or ecological protist endemics.

INTRODUCTION
The reviews by Foissner (2006), Green and
Bohannan (2006) and Martiny et al. (2006) show
biogeographic patterns in micro-organisms, disproving the famous metaphor of Beijerinck (1913)
and others “that, in micro-organisms, everything iseverywhere, the environment selects”. These reviews demonstrate also the two basic researchstrategies used in biogeographical studies. While
Foissner (2006) emphasizes morphological anddistributional data, Green and Bohannan (2006)
and Martiny et al. (2006) strengthen ecological andmolecular studies.
At first glance it appears rather academic whether
or not micro-organisms have biogeographies. However, the answer influences several basic theories
in biology and ecology, for instance, species diversity and conservation and the influence of historical contingencies (e.g., split of Pangaea) on organ-

2

原生動物学雑誌 第 40 巻 第 1 号 2007 年

ism distribution.
The cosmopolitan model, now driven mainly
by Finlay et al. (1996, 2004), proposes that microorganisms are ubiquitous and cosmopolitan because their small size and high abundance favour
global dispersal and low allopatric speciation.
Thus, they have low global but high local diversity
as well as high migration and low extinction rates.
Finlay et al. (1996, 2004) explain the lack of certain micro-organisms in certain areas as a result ofuneven sampling effort and/or misidentification of
species. The best demonstration of the cosmopolitan view is found in Finlay and Esteban (1998):“As protozoan species are probably globally ubiquitous, there is every reason to believe that all species of freshwater protozoa could eventually be
discovered in one small pond”. Such extreme opinion is hardly found in the more recent literature,
where most data and authors support a view which
I called the “moderate endemicity model” (Foissner
1999, 2004, 2006; Foissner et al. 2002; Green and
Bohannan 2006; Katz et al. 2005; Martiny et al.
2006; Scheckenbach et al. 2005). The moderateendemicity model takes into account the great differences in morphology and ecology of microorganisms by assuming that about 30% of them arehistorical (palaeoendemic; split of Pangaea), continental, regional, or local endemics. Further, it suggests that the high rates of local:global diversity
are partially caused by our ignorance of the actualglobal species number needed for the calculation;that global diversity is high because the short generation times and low extinction rates foster diversification by various modes of speciation; and thatmicro-organisms are not ubiquitous but as precisely adapted as macro-organisms to the environment (Weisse 2004a, b; Weisse et al. 2001).
Although the two models produce pronounced
differences, they agree in a fundamental matter,viz., the usually wide and even global distributionof many microbial species, likely due to their small
size, the high abundance of euryoecious species,

and the old age. Hopefully, the ongoing research
will show the reasons why part of them does notfollow this pattern. This and some recent evidences for restricted distribution of protists will be
reviewed in the present paper, emphasizing flagship species, community structures, and sporeforming cryptogams as ultimate proofs for protist
endemism.

THREE FUNDAMENTAL EVIDENCES FOR
PROTIST BIOGEOGRAPHIESIn this chapter, I summarize my most convincing evidences for protist biogeographies: (i) the
distribution of soil ciliates, (ii) flagship and vicarious species, and (iii) spore-forming cryptogams. I
am still convinced that protist biogeographies must
be shown by distinct morphospecies, as in plants
and animals, because gene analyses do not tell us
how the organisms look like. Frequently, quitedissimilar taxa have highly similar gene sequences(difference 1 % or less in, e.g., the 18S rRNA) andvice versa, that is, genes often do not adequately
represent the morphological diversity. Impressive
examples are found in ciliates from tank bromeliads (Foissner et al. 2003) and in pond ciliates from
Austria and Antarctica (Schmidt et al. 2007).
World soil ciliates
Foissner (1998) and Foissner et al. (2002) investigated ciliates in about 1000 soil samples fromall biogeographical regions. Later, unpublisheddata were added and various statistical analyses
were performed (Chao et al. 2006). The similarity
cluster resulting from the distribution of the 1136
ciliate species found clearly shows the separationof Laurasia and Gondwana (Fig. 1). This provides
convincing statistical support for the influence ofhistorical events on the distribution of soil ciliates.
The same has been shown for a flagellate flagship,Jpn. J. Protozool. Vol. 40, No. 1. (2007)

3

Figure 1. World soil ciliate species cluster based on the classic Jaccard dis-similarity index and Ward’s
error sum of squares method. From Chao et al. (2006).

viz., Hemimastix amphikineta which is fairly common in Gondwana (~ 50 records), while absent
from Laurasia (Foissner 2006).
Flagship and vicarious species
Flagship species are the “ultimate” proof of
protist endemism (Foissner 2006). However,Finlay et al. (2004) argue that flagship species “isa more-or-less convincing argument for large
mammal species, but in case of protists, it evades
the crucial question. In many cases we can confidently demonstrate that a large mammal species
does not exist outside of its endemic range, but
how are we to demonstrate that a protist species
does not exist elsewhere in the biosphere? Usingtypical sampling methods, there is no practicalmeans of doing so, and one is left wondering what
the term ‘endemic protist’ actually means”. In my
opinion, this argumentation does not hold for scientists working lifelong on a certain taxonomic

group, for instance, Penard, Kahl, Dragesco, Jung,
Bonnet, Meisterfeld, and myself. Taxonomists see
such species, simply because they stand out likeelephants from the mass of other organisms. Further, if the existence of endemic protist species
cannot be proven with the methods available, thenthe opposite is also impossible, showing that theargumentation of Finlay et al. (2004) is a circulus
vitiosus. I have seen and documented about 2000
ciliate species from habitats globally during thepast 40 years (Chao et al. 2006; Foissner 1993;
Foissner and Xu 2006, 2007; Foissner et al. 1995,
1999, 2002; Kreutz and Foissner 2006). Most ofthem, I saw only a few times, and rather many I
found only in a certain region.
I put together some of the most impressive protist flagship species previously (Foissner 2006).
Since then, several new ones have been discoveredor redescribed. They will be briefly discussed in
the following paragraphs. Unfortunately, Australia
is still almost a tabula rasa with respect to ciliates

4

原生動物学雑誌 第 40 巻 第 1 号 2007 年

and testate amoebae. It appears that quite a lot of
the large-sized testate amoebae and ciliates areabsent from this continent.
Testate amoebae
Testate amoebae provide the most convincing
evidences for protists with restricted geographic
distribution because the stable test and the rather
low diversity fostered faunistic investigations.
Foissner (2006) reviewed the biogeographic data,emphasizing species of the Nebela family, severalof which are Gondwanan relicts, e.g., Apodera vas
and Certesella certesi. Fortunately, testacean
research has been increased in Asia, showing theexistence of several Asian endemics belonging to
the Difflugia family (Yang and Shen 2005; Yanget al. 2004, 2005). Many curious testate amoebae,
including six new genera and two new families,
were recently described from rivers in Western
Azerbaijan (Snegovaya and Alekperov 2005). Unfortunately, river testaceans are poorly exploredglobally, making it impossible to estimate the geographic range of the Azerbaijan species.
Difflugia biwae Kawamura (1918) was originally described from Lake Biwa in Japan, and thenhas been considered as a local endemic for a longtime (Ichise et al. 2004). However, recently it has
been found in three lakes of China, viz., Mulan
Lake, Poyang Lake, and Qiandao Lake (Yang andShen 2005). These authors state: “Difflugia biwae
is probably endemic to East Asia because it hassuch a large size (165–306 µm) that it would havebeen easily found in Europe and North America, if
it were there”. Indeed, the distinct collar flare andthe long aboral horn set apart D. biwae from allcongeners (Fig. 2).
Difflugia tuberspinifera Hu et al. (1997), as
redescribed by Yang et al. (2004), is a highly characteristic species as yet found only in a pond andin a lake of China (Figs 6, 7). It has a moderate
size (~ 110 µm), but the conspicuous spines, themulberry-shaped wall structure, and the crenate
aperture margin make it unmistakable and easy torecognize. Interestingly, this species is abundant,emphasizing the proposed endemism.
Difflugia mulanensis Yang et al. (2005) is another flagship from the oligotrophic Lake Mulan in
China. Like D. tuberspinifera, it is a middle-sized
species (~ 110 x 70 µm), but the highly characteristic shape, viz., the widely projecting apertural
collar makes it easily recognizable (Fig. 3). The
authors suggest that “D. mulanensis might have arestricted geographical distribution with endemicareas located in East Asia, because it was notfound in Europe and North America where numerous investigations of testate amoebae fauna havebeen made”.
Two other testate amoebae with the capacity to
become holarctic endemics are Arcella formosaand Cyclopyxis acmodonta, both described by
Nicholls (2007) from a Typha-dominated wetland
in Ontario, Canada. Both are ≥ 200 µm in size anddiffer by various morphological features from thecongeners (Figs 4, 5). One of these species, viz., A.
formosa occurs also in Germany (Meisterfeld,
pers. comm.). In discussing the geographic distribution, Nicholls (2007) states: “Recognizing thatmany species of Arcella and Cyclopyxis were
known to science nearly a century ago, if A. formosa and C. acmodonta were widespread in otherhabitats on other parts of the world, they shouldhave been detected by others long ago”.
Ciliates
The richly structured ciliates offer good chance
to define flagship species very sharply. Indeed,
quite a lot are known, most defined by size and/or
colour (Chao et al. 2006; Foissner 2006). Here, I
report on three recently described species not contained in the studies just cited. Further examples
are the vicarious species discussed in the next
chapter.

Jpn. J. Protozool. Vol. 40, No. 1. (2007)

5

Figures 2–7. Endemic Asian (2, 3, 6, 7) and Holarctic (4, 5) flagship testate amoebae. 2: Difflugia biwae, average length
227 µm. Drawn from data of Yang and Shen (2005). 3: Difflugia mulanensis, average length 109 µm. Drawn from dataof Yang et al. (2005). 4, 5: Arcella formosa, ventral and lateral view, average diameter 192 µm. From Nicholls (2007). 6,
7: Difflugia tuberspinifera, ventral and lateral view, average diameter 110 µm (without spines). From Yang et al. (2004).

6

原生動物学雑誌 第 40 巻 第 1 号 2007 年

Figures 8–10. Endemic haptorid (8) and stichotrichid (9, 10) flagship ciliates from Africa. 8: Bryophyllum longisetum has an average size of 180 x 20 µm and as yet has been found only in soil from the Kilimanjaro Mountains,
Central Africa. The arrowheads mark the up to 10 µm long bristles of dorsal brush row 3, i.e., one of the most conspicuous features of this species. OB – oral bulge. From Foissner and Lei (2004). 9: Saudithrix terricola occurs insoils of Saudi Arabia and China. It is a size flagship (270 x 100 µm on average) with a highly characteristic, sickleshaped buccal lip (arrowhead) and ventral cirral pattern. From Berger et al. (2006). 10: Rigidothrix goiseri has anaverage size of 230 x 70 µm and as yet has been found only in soil from the Niger floodplain, West Africa. It is asize and shape (tail!) flagship with a highly distinct organization of body (rigid) and cirral pattern (holostichid).
From Foissner and Stoeck (2006).

Jpn. J. Protozool. Vol. 40, No. 1. (2007)

My estimation that these species have restricteddistribution is based on the investigation of over1000 soil samples collected globally and on over2000 limnetic samples from Austria and Germany.
If these species would have been present in any
other sample, I would have recognized them because all are 200 µm or larger.
Bryophyllum longisetum Foissner and Lei(2004) was discovered in soil from a cloud foreston the Kilimanjaro Mountains in Africa, about2600 m above sea-level. The understorey mainly
consists of highly conspicuous, tree-like Ericaceae.
Thus, this is a very special habitat, suggesting that
B. longisetum could be a regional endemic. Bryophyllum longisetum is a vermiform species with anaverage size of 180 x 20 µm and a distinctly
twisted oral bulge. The most conspicuous features
are the vermiform body and the up to 10 µm long
bristles of dorsal brush row 3 (Fig. 8). These andother features set widely apart B. longisetum fromall members of the family Bryophyllidae.
Saudithrix terricola was discovered by Berger
et al. (2006) in soil from a vegetable field in thesurroundings of the town of Riyadh, Saudi Arabia.
With an average size of 270 x 100 µm and a highly
characteristic, sickle-shaped buccal lip and cirral
pattern it is a flagship with respect to both, size
and morphology (Fig. 9). Thus, it was referred to a
new genus, Saudithrix. Very recently, I found S.
terricola in soil from the floodplain of the Yangtze
River in China, suggesting a palaeotropic distribution. Further, I discovered a second species in soil
from the floodplain of the Chobe River in Botswana, Africa.
Rigidothrix goiseri Foissner and Stoeck (2006)
was discovered in soil from the Niger floodplain
near to the town of Timbuktu, Republic of Mali,West Africa. It has an average size of 230 x 70 µm
and a distinct tail, making it easily recognizable(Fig. 10). This ciliate, which belongs to the stichotrichine spirotrichs (hypotrichs s.l.), has somany specific features that it was classified into a

7

new genus and family, the Rigidotrichidae. Specifically, R. goiseri has a rigid body, while thecirral pattern is like that of flexible stichotrichs.
Thus, R. goiseri breaks the flexibility-dogma in theclassification if stichotrichine spirotrichs (Berger1999).
Vicarious species
The vicarious model suggests that the components of major biota evolve together and are subject to parallel effects of geographical and climaticfluctuations, and that modern biogeographical distributions result from the division of ancestral biotas by the formation of natural barriers. In otherwords, vicariants are closely related taxa isolated
geographically from one another by a vicarianceevent, e.g., continental drift (Lincoln et al. 1982).
Thus, vicariant species verify by definition restricted geographical distribution.
In protists, the vicariance model has not yet
applied, as far as I know, although some impressive examples occur in ciliates and testate amoebae, and likely also in other groups. Here, I shallshow some examples from ciliates, while the Nebelidae provide firm evidence in testate amoebae.
Likely, the examples mentioned are basically related to continental drift.
The first example is the genus Kuehneltiella,
which belongs to the class Colpodea (Figs 11–16).
Three species are known, all living in astatic, dry
environments (Foissner 1993; Foissner et al.
2002). Kuehneltiella terricola (size 136 x 100 µm)
lives in soil of arid hummock grassland near to thetown of Alice Springs, Australia (Figs 11, 14); K.
namibiensis (180 x 120 µm) was discovered inbark from a Sterculia africana tree in Namibia,
West Africa (Figs 12, 16); and K. muscicola (84 x
63 µm) inhabits alpine mosses at the AustrianGerman border in Tyrol (Figs 13, 15). These three
species are highly similar, but differ in body size,
details of the oral structures and, especially, in the

8

原生動物学雑誌 第 40 巻 第 1 号 2007 年

Figures 11–16. Vicarious species of the colpodid genus Kuehneltiella, right side views (11–13) and resting cysts(14–16) in vivo. They differ mainly in body size and resting cyst morphology. 11, 14: Kuehneltiella terricola occurs in dry Australian soils and has an average size of 136 x 100 µm. From Foissner (1993). 12, 16: Kuehneltiellanamibiensis, which was discovered in bark of a tree in Namibia, West Africa, has an average size of 180 x 120 µm,
i.e., is a size flagship. From Foissner et al. (2002). 13, 15: Kuehneltiella muscicola occurs in German mosses andhas an average size of 84 x 63 µm. From Foissner (1993).

Jpn. J. Protozool. Vol. 40, No. 1. (2007)

Figures 17–21. Vicarious species of the peniculine genus Apofrontonia, ventral views in vivo (17) and after silver
impregnation to show the complex somatic and oral ciliary pattern (18–21). These species, which are flagships dueto the big mouth, differ from each other mainly by morphometric features, such as body size and number of vestibular ciliary rows (Table 1). 17, 18, 21: Apofrontonia lametschwandtneri occurs in mud from coastline puddles ofVenezuela and has an average size of 180 x 120 µm. Figure 21 shows the complex structure of the adoral membranelles (peniculi, P1–P3) recognizable in Fig. 18 as long, black lines at the left mouth margin. From Foissner andSong (2002). 19: Apofrontonia obtusa was discovered in a pond of Germany and has an average size of 95 x 75
µm. It has only 4–5 contractile vacuoles (CV), while the congeners have 20 or more. From Song and Wilbert(1989). 20: Apofrontonia dohrni occurs in coastline puddles of Italy and has a size of 118 x 61 µm. From Fokin etal. (2006). CV – contractile vacuoles, MA – macronucleus, PK – paroral kinety, P1–P3 – peniculi (adoral membranelles), SK – somatic kineties, VK – vestibular kineties.

9

10

原生動物学雑誌 第 40 巻 第 1 号 2007 年

Table 1. Comparison of the vicarious species Apofrontonia lametschwandtneri (A. lamet.),A. dohrni and A. obtusa, based on the original descriptions

Characteristics

A. lamet.

A. dohrni

A. obtusa

180 x 120

118 x 61

95 x 75

1.3–1.6
0.75
155

1.6–2.0
0.4–0.6
68

1.3–1.4
0.5–0.75
90

Vestibular ciliary rows, average number

13

4

9

Contractile vacuoles, average number

29

20

4–5

Habitatcoastline puddles

coastline puddles

freshwater
pondCountry

Venezuela

Italy

Germany

Reference

Foissner &Song (2002)

Fokin et al.
(2006)

Song &
Wilbert (1989)

Cell size, µm (average of prepared specimens)
Ratio body length:body width
Ratio mouth length:body length
Somatic ciliary rows, average number

structure of the resting cyst (Figs 14–16).
The second example is the genus Apofrontonia,
a relative of the widely known Paramecium (Figs
17–21, Table 1). The three species known are
fairly similar, but live in slightly different habitats(saline coastline puddles vs. freshwater ponds) andin different geographic regions (Germany, Italy,
Venezuela).
Spore-forming cryptogams
With all their theories and complex investigations, microbial biogeographers have forgotten asimple fact of paramount significance (Fig. 22):
spores, the dispersal means of macrofungi, lichens,mosses, ferns and horsetails are in the size andabundance range of trophic and cystic protists,suggesting that dispersal is subjected to similar
constraints in both groups (Foissner 2006); evensome flowering plants, for instance, many orchids
have seeds in the size of Paramecium (Fig. 22).
Further, reproduction of cryptogams is about as
simple as in protists, and the abundance of sporesis extraordinary: a single Agaricus campestris re-leases 1.6 x 1010 spores with a size of 7–10 x 5–7µm within six days (Webster 1983), which exceeds
the abundance of ciliates in a m² of forest soil byseveral orders of magnitude (Meyer et al. 1989).
There is no doubt that many cryptogams haverestricted ranges, in spite of their minute and abundant spores, although the areals are usually larger
than those of flowering plants and animals, suggesting that minuteness and high abundance of thespores facilitate dispersal, as in micro-organisms(Finlay et al. 2004; Wilkinson 2001). On the other
hand, cryptogams make clear that minute size andhigh abundance do not habitually cause cosmopolitan distribution. Other factors must be involved
and will be discussed in the last chapter.

EVIDENCES FOR REGIONAL AND LOCALPROTIST ENDEMISM“The existence of endemic morphospecies appears unlikely, since rates of global transport of
micro-organisms, although restricted, are too muchhigher than evolutionary speciation into morpho-

Jpn. J. Protozool. Vol. 40, No. 1. (2007)

Figure 22. This figure compares, at about the same magnification, trophic and cystic protists (ciliates, flagellates,
naked and testate amoebae) with spores of macrofungi (mushrooms), mosses, ferns, and the minute seed of an orchid (Vanda caerulescens). Obviously, all are of similar small size and very abundant, for instance, a single Agaricus campestris (mushroom) releases 1.6 x 1010 spores within six days (Webster 1983), which exceeds the abundanceof ciliates in a m² of forest soil by several orders of magnitude (Meyer et al. 1989). While nobody denies that mushrooms, mosses, and ferns have biogeographies, protists are widely assumed to be cosmopolitan because their small
size and high abundance (supposedly!) favour air dispersal, an opinion flawed by this figure. Further, protist cysts
lack adaptations for air dispersal, while seeds of many flowering plants have such adaptations, including the orchid
seed shown which has wings of large-sized, air-filled cells.

11

12

原生動物学雑誌 第 40 巻 第 1 号 2007 年

logically distinct organisms” (Boenigk et al. 2006).
I disagree with such statements for a simple reason: when fish in postglacial and tropical lakes(e.g. Lake Malawi) can produce dozens of distinct
species within 15 000 years (Mayr 1963; Schluter
1998), then this likely can occur also in protists,
especially, when considering their short generation
time and high diversity; further, many postglacialland plants and animals have reached an extent ofdivergence to be recognized as operational taxonomic units, i.e., morphologically distinguishable
subspecies (Mayr 1963; Schluter 1998). Thus, thisand similar generalizations by other authors, who
assume slow morphological diversification of micro-organisms due to their (supposedly!) high rates
of dispersal, would possibly apply only if allopatric speciation would be the sole speciation process. This, however, is not the case (Johnson andGullberg 1998; Schluter 1998). In protists, local
and regional endemism are difficult to prove dueto their “invisibility” and the poor state of distribution science. None the less, there are some evidences which will be discussed in the following
paragraphs.
In Lake Alatsee, a remote, alpine lake at theGerman-Austrian border, Stoeck et al. (2007) discovered an Urocentrum turbo-like ciliate, differingfrom the nominal and sole species of the genus by
the lack of functional trichocysts. Trichocysts are ahighly conspicuous feature, shaping the species’
ecology, physiology and morphology (Harumotoand Miyake 1991; Plattner 2002). Thus, the presence/absence of trichocysts has been widely usedby taxonomists to distinguish species within genera. Using this feature, the Alatsee population of
Urocentrum is a distinct species, although the
18rDNA and the ITS sequences are nearly identical to those of the nominal species.
A very similar case has been reported by
Esteban et al. (2000). These authors found a highly
distinct species of Lembadion in a remote craterlake of an extinct volcano in Tasmania. Indeed, L.

curvatum has such a distinct shape that it can beconsidered as a flagship species which would havebeen recognized at least in Europe if it were there.
A further case concerns Ophrydium versatile, aperitrich ciliate widely distributed in Eurasia. It
makes green (due to symbiotic algae) colonies up
to 15 cm across (for a review, see Foissner et al.
1999). In some pre-alpine lakes of Austria occurs
another Ophrydium, viz., O. eutrophicum, differing from O. versatile mainly by one distinct feature: it has a much longer adoral ciliary spiralcausing a conspicuous cephalisation of the anterior(peristomial) end. All my efforts to find this species elsewhere failed. However, recently it has
been reported from a Polish lake (Mieczan 2005).
Unfortunately, the author did not respond to myrequest for material so that I could not check theidentification.
A special case represents Gonostomum albicarpathicum, a stichotrich (hypotrich s.l.) ciliate recently described by Vd’ačný and Tirjaková (2006).
It is only 70 x 22 µm in size, but conspicuous inhaving four macronucleus nodules, while all congeners possess two or eight nodules. A close relative, G. affine has two nodules and is one of themost common soil ciliates globally (Foissner et al.
2002). I never saw the quadrinucleate species inover 1000 soil samples, including many from theregion (northern and eastern Austria) G. albicarpathicum occurs, suggesting that it could be a local
or Carpathian endemic.
The last example comes from a study of Kreutz
and Foissner (2006), who investigated and documented 656 species of bacteria, protists, and micro-metazoa occurring in a three hectare-sizedmoorland in southern Germany. This moorland
formed after the last (Würm) ice-age, that is, about
15 000 years ago. Thus, a considerable diversity
accumulated during this rather short period. On theother hand, some common species are lacking(e.g., the ciliate Colpidium colpoda, the euglenid
Phacus pleuronectes, and rotifers of the genera

Jpn. J. Protozool. Vol. 40, No. 1. (2007)

Proales and Floscularia) and many undescribed
species were discovered. While a mass of undescribed species is comprehensible in amoebas,
flagellates and ciliates, which are poorly researched, this is surprising in well-known groups,
such as euglenids and chrysophytes. Thus, the authors state: “We must face the possibility thatsome of the undescribed species are regional or
local endemics”.

FACTORS LIMITING DISTRIBUTION OF
MICRO-ORGANISMS
Most micro-organisms are very fragile in trophic conditions. Thus, it is reasonable to assume
that dispersal occurs mainly via the more stable
resting cysts. Certainly, there are exceptions, forinstance, Paramecium which likely lacks a cystic
stage, while Tetrahymena pyriformis GL, longconsidered as a cystless ciliate, can make restingcysts under certain conditions (Nilsson 2005). Dispersal by human activities, both in trophic (e.g.
ballast water) and cystic form is a second, often
forgotten main route (Foissner 2006). When one
experiences the masses of European tourists visiting the Titicaca Lake, then it becomes understandable why we find holarctic protists all around theworld. None the less, there are still protists withrestricted occurrence, and we have to think about
the reasons.
(i) Cyst viability is likely much more restricted
than widely assumed. Foissner (2006) presented
evidences that, e.g., cysts of soil ciliates from rain
forests are very unstable, dying under dry conditions within a few months. Likewise, most cysts
produced under laboratory conditions do not excyst, either because they are not viable or the rightconditions are not found. Certainly, there are a lotof evidences that cysts are transported by air, butvery few species have ever been identified, suggesting that most are not viable or need special

13

conditions to excyst.
(ii) Distinct geographic barriers, such as highmountains, large deserts, and specific water andwind currents. As endemics occur also in the sea(Foissner 2006), such barriers likely exist on land,
too. Unfortunately, the barrier hypothesis is difficult to prove for the reasons discussed in the foregoing paragraph.
(iii) Speciation is an ongoing process. Thus, thecommunities present are a mixture of old andyoung species, and many of the latter had not yet
time to spread globally and, especially, to establish
viable populations.

OUTLOOK
Finlay et al. (1996, 2004) and Boenigk et al.
(2006) argue that the high abundances and rates ofglobal transport make the existence of endemic
protist morphospecies unlikely. While this might
apply for some euryoecious species, it is likely
incorrect for the mass of micro-organisms most ofwhich are rare or very rare, as in flowering plants
and animals. This becomes obvious when frequency distributions or protist counts are studied.
For instance, 200 of the 365 species of soil ciliates
found in Namibia occurred at only one or two sites(Fig. 23). This has been emphasized also by Greenand Bohannan (2006). Basically, the same problem
exists with resting cysts. While some species easily encyst and excyst, the mass of species does not.
Thus, we must learn to consider micro-organisms
as highly individualized entities with very different
properties. Then, there will be place also for endemic morphospecies.

ACKNOWLEDGEMENTS
The technical assistance of Kustos Peter Gruber, Mag. Birgit Peukert and Andreas Zankl is

14

原生動物学雑誌 第 40 巻 第 1 号 2007 年

Figure 23. Frequencies of 365 ciliate species in 73 samples from terrestrial habitats ofNamibia (from Foissner et al. 2002).

greatly acknowledged. I also gratefully acknowledge financial support by the Austrian Science
Foundation (FWF-projects P-15017 and P-16796)
and the Japanese Society of Protistologists who
invited this review at occasion of a Plenary Lecture given during the annual meeting in Saga city.

REFERENCES
Beijerinck, M. W. (1913) De infusies en de ontdekking der
backteriёn. Jaarboek van de Koninklijke Akademie v.
Wetenschappen. Müller, Amsterdam.
Berger, H. (1999) Monograph of the Oxytrichidae(Ciliophora, Hypotrichia). Monographiae biol 78, i–xii, 1–1080.
Berger, H., Al-Rasheid, K.A.S and Foissner, W. (2006)
Morphology and cell division of Saudithrix terricola
n. gen., n. sp., a large, stichotrich ciliate from Saudi
Arabia. J Eukaryot Microbiol 53, 260–268.
Boenigk, J., Pfandl, K., Garstecki, T., Harms, H., Novarino, G. and Chatzinotas, A. (2006) Evidence ofgeographic isolation and signs of endemism within a
protistan morphospecies. Appl Environ Microbiol 72,
5159–5164.

Chao, A., Li, P. C., Agatha, S. and Foissner, W. (2006) A
statistical approach to estimate soil ciliate diversityand distribution based on data from five continents.
Oikos 114, 479–493.
Esteban, G. F., Finlay, B. J., Olmo, J. L. and Tyler, P. A.
(2000) Ciliated protozoa from a volcanic crater-lakein Victoria, Australia. J Nat Hist 34, 159–189.
Finlay, B. J. and Esteban, G. F. (1998) Freshwater protozoa: biodiversity and ecological function. Biodiv
Conserv 7, 1163–1186.
Finlay, B. J., Corliss, J. O., Esteban, G., Fenchel, T. (1996)
Biodiversity at the microbial level: the number offree-living ciliates in the biosphere. Q Rev Biol 71,
221–237.
Finlay, B. J., Esteban, G. F. and Fenchel, T. (2004) Protist
diversity is different? Protist 155, 15–22.
Foissner, W. (1993) Colpodea (Ciliophora). Protozoenfauna 4, i–x, 1–798.
Foissner, W. (1998) An updated compilation of world soil
ciliates (Protozoa, Ciliophora), with ecological notes,
new records, and descriptions of new species. Europ J
Protistol 34, 195–235.
Foissner, W. (1999) Protist diversity: estimates of thenear-imponderable. Protist 150, 363–368.
Foissner, W. (2004) Ubiquity and cosmopolitanism of
protists questioned. SILnews 43, 6–7.

Jpn. J. Protozool. Vol. 40, No. 1. (2007)
Foissner, W. (2006) Biogeography and dispersal of microorganisms: a review emphasizing protists. Acta Protozool 45, 111–136.
Foissner, W. and Lei, Y.-L. (2004) Morphology and ontogenesis of some soil spathidiids (Ciliophora, Haptoria). Linzer biol Beitr 36, 159–199.
Foissner, W. and Song, W. (2002) Apofrontonia lametschwandtneri nov. gen., nov. spec., a new peniculine
ciliate (Protozoa, Ciliophora) from Venezuela. Europ
J Protistol 38, 223–234.
Foissner, W. and Stoeck, T. (2006) Rigidothrix goiseri
nov. gen., nov. spec. (Rigidotrichidae nov. fam.), a
new “flagship” ciliate from the Niger floodplain
breaks the flexibility-dogma in the classification ofstichotrichine spirotrichs (Ciliophora, Spirotrichea).
Europ J Protistol 42, 249-267.
Foissner, W. and Xu, K. (2006) Monograph of the
Spathidiida (Ciliophora, Haptoria). Volume I: Protospathidiidae, Arcuospathidiidae, Apertospathulidae.
Monographiae biol 81, 1-485.
Foissner, W. and Xu, K. (2007) Monograph of the
Spathidiida (Ciliophora, Haptoria). Volume II:
Spathidiidae and Pharyngospathidiidae. Monographiae biol (in preparation).
Foissner, W., Berger, H., Blatterer, H. and Kohmann, F.
(1995) Taxonomische und ökologische Revision derCiliaten des Saprobiensystems – Band IV: Gymnostomatea, Loxodes, Suctoria. Informationsberichte
des Bayer Landesamtes für Wasserwirtschaft 1/95,
1–540.
Foissner, W., Berger, H. and Schaumburg, J. (1999) Identification and ecology of limnetic plankton ciliates.
Informationsberichte des Bayer Landesamtes fürWasserwirtschaft 3/99, 1–793.
Foissner, W., Agatha, S. and Berger, H. (2002) Soil ciliates (Protozoa, Ciliophora) from Namibia (Southwest
Africa), with emphasis on two contrasting environments, the Etosha Region and the Namib Desert.
Denisia 5, 1–1459.
Foissner, W., Strüder-Kypke, M., Van der Staay, G.W.M.,
Moon-Van der Staay, S.-Y. and Hackstein, J. H. P.
(2003) Endemic ciliates (Protozoa, Ciliophora) fromtank bromeliads: a combined morphological, molecular, and ecological study. Europ J Protistol 39, 365–
372.
Fokin, S., Andreoli I., Verni, F. and Petroni, G. (2006)
Apofrontonia dohrni sp. n. and the phylogenetic relationships within Peniculia (Protista, Ciliophora, Oligohymenophorea). Zool Scr 35, 289–300.

15

Green, J. and Bohannan, B. J. M. (2006) Spatial scaling of
microbial biodiversity. Trends in Ecol Evol 21, 501–
507.
Harumoto, T. and Miyake, A. (1991) Defensive functionof trichocysts in Paramecium. J Exp Zool 260, 84–
92.
Hu, D. L., Shen, Y. F., Gu, M. R. and Gong, X. J. (1997)
New species and new records of protozoa from Wuling Mountians Area. Pp. 40–72 in D.-X. Song, ed.
Invertebrates of Wuling Mountains Area, Southwestern China. Science Press, Bejing (in Chinese).
Ichise, S., Morita, T., Wakabayashi, T., Kusuoka, Y. andNishino, M. (2004) Disappearance and its past distribution of the endemic protista Difflugia biwae Kawamura, 1918 in Lake Biwa, Central Japan. Rep Shiga
Pref Inst Pub Hlth & Environ Sci 39, 57–63 (in Japanese).
Johnson, P. A. and Gullberg, U. (1998) Theory and models
of sympatric speciation. Pp. 79–89 in D. J. Howard
and S. H. Berlocher, eds. Endless Forms. Oxford
Univ. Press, New York and Oxford.
Katz, L. A., McManus, G. B., Snoeyenbos-West, L. O.,
Griffin, A., Pirog, K., Costas, B. and Foissner, W.
(2005) Reframing the “everything is everywhere“
debate: evidence for high gene flow and diversity inciliate morphospecies. Aquat Microb Ecol 41, 55–65.
Kawamura, T. (1918) Japanese Freshwater Biology. Syoukabou, Tokyo, Japan, pp. 113–115 (in Japanese).
Kreutz, M. and Foissner, W. (2006) The Sphagnum pondsof Simmelried in Germany: a biodiversity hot-spot
for microscopic organisms. Protozool Monogr 3, 1–
267.
Lincoln, R. J., Boxshall, G. A. and Clark, P. F. (1982) A
Dictionary of Ecology, Evolution and Systematics.
Cambridge Univ. Press, Cambridge and Sydney. 298
pp.
Martiny, J. B. H., Bohannan, B. J. M., Brown, J. H.,
Colwell, R. K., Fuhrmann, J. A., Green, J. L., HornerDevine, M. C., Kane, M., Krumins, J. A., Kuske, C.
R., Morin, P. J., Naeem, S., Øvreås, L., Reysenbach,A.-L., Smith, V. H. and Staley, J. T. (2006) Microbial
biogeography: putting microorganisms on the map.
Nature Reviews 4, 102–112.
Mayr, E. (1963) Artbegriff und Evolution. Parey, Hamburg and Berlin. 617 pp.
Meyer, E., Foissner, W. and Aescht, E. (1989) Vielfalt undLeistung der Tiere im Waldboden. Öst Forstz 3, 15–18.
Mieczan, T. (2005) Periphytic ciliates in littoral zone of

16

原生動物学雑誌 第 40 巻 第 1 号 2007 年

three lakes of different trophic status. Pol J Ecol 53,
489–502.
Nicholls, K. H. (2007) Cyclopyxis acmodonta n. sp. andArcella formosa n. sp.: two new species of testate
rhizopods (Arcellinida, Protozoa) from remnant wetlands in Ontario, Canada. Canadian Field-Naturalist
119 (in press).
Nilsson, J. R. (2005) Ethanol affects endocytosis and proliferation of Tetrahymena pyriformis GL and promotes encystment. Acta Protozool 44, 293–299.
Plattner, H. (2002) My favorite cell – Paramecium. BioEssays 24, 649–658.
Scheckenbach, F., Wylezich, C., Weitere, M., Hausmann,
K. and Arndt, H. (2005) Molecular identity of strainsof heterotrophic flagellates isolated from surface
waters and deep-sea sediments of the South Atlantic
based on SSU rDNA. Aquat Microb Ecol 38, 239–
247.
Schluter, D. (1998) Ecological causes of speciation. Pp.
114–129 in D. J. Howard and S. H. Berlocher, eds.
Endless Forms. Oxford Univ. Press, New York andOxford.
Schmidt, S. L., Bernhard, D., Schlegel, M. and Foissner,
W. (2007) Phylogeny of the Stichotrichia(Ciliophora; Spirotrichea) reconstructed with SSU
rDNA gene sequences: discrepancies and accordanceswith morphological data. J Eukaryot Microbiol (inpress).
Snegovaya, N. and Alekperov, I. (2005) Fauna of testate
amoebae of western Azerbaijan rivers. Protistology 4,
149–183.
Song, W. and Wilbert, N. (1989) Taxonomische Untersuchungen an Aufwuchsciliaten (Protozoa, Ciliophora) im Poppelsdorfer Weiher, Bonn. Lauterbornia
3, 2–221.

Stoeck, T., Bruemmer, F. and Foissner, W. (2007) Evidence for local ciliate endemism in an alpine anoxic
lake. Microb Ecol (in press).
Vd’ačný, P. and Tirjaková, E. (2006) A new soil hypotrich
ciliate (Protozoa, Ciliophora) from Slovakia:
Gonostomum albicarpathicum nov. spec. Europ J
Protistol 42, 91–96.
Webster, J. (1983) Pilze. Eine Einführung. Springer, Berlin, Heidelberg, New York.
Weisse, T. (2004a) Pelagic microbes – protozoa and themicrobial food web. Pp. 417–460 in P. O´Sullivan
and C. R. Reynolds, eds. The Lakes Handbook, Vol I.
Blackwell Science, Oxford.
Weisse, T. (2004b) Meseres corlissi: a rare oligotrich
ciliate adapted to warm water and temporary habitats.
Aquat Microb Ecol 37, 75–83.
Weisse, T., Karstens, N., Meyer, V. C. L., Janke, L., Lettner, S. and Teichgräber, K. (2001) Niche separationin common prostome freshwater ciliates: the effect offood and temperature. Aquat Microb Ecol 26, 167–
179.
Wilkinson, D. M. (2001) What is the upper size limit forcosmopolitan distribution in free-living microorganisms? J Biogeogr 28, 285–291.
Yang, J. and Shen, Y. (2005) Morphology, biometry anddistribution of Difflugia biwae Kawamura, 1918
(Protozoa: Rhizopoda). Acta Protozool 44: 103–111.
Yang, J., Beyens, L., Shen, Y. and Feng, W. (2004) Redescription of Difflugia tuberspinifera Hu, Shen, Gu et
Gong, 1997 (Protozoa: Rhizopoda: Arcellinida: Difflugiidae) from China. Acta Protozool 43, 281–289.
Yang, J., Meisterfeld, R., Zhang, W. and Shen, Y. (2005)
Difflugia mulanensis nov. spec., a freshwater testate
amoeba from Lake Mulan, China. Europ J Protistol
41, 269–276.