Flagellar movement of the sessile flagellates Actinomonas ...
Flagellar movement of the sessile flagellates Actinomonas ...
Flagellar movement of the sessile flagellates Actinomonas ...
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<strong>Flagellar</strong> <strong>movement</strong> <strong>of</strong> <strong>the</strong> <strong>sessile</strong> <strong>flagellates</strong><br />
<strong>Actinomonas</strong>, Codonosiga, Monas,<br />
and Poteriodendron<br />
4°5<br />
By M. A. SLEIGH<br />
(From <strong>the</strong> Department <strong>of</strong> Zoology, The University, Bristol 8)<br />
Summary<br />
Water currents set up by flagellar activity are used to bring food particles to <strong>the</strong><br />
body in each <strong>of</strong> <strong>the</strong> <strong>sessile</strong> <strong>flagellates</strong> <strong>Actinomonas</strong>, Codonosiga, Monas, and Poteriodendron.<br />
The water currents produced by <strong>the</strong> 4 organisms are all somewhat different,<br />
and, while that set up by Codonosiga is in <strong>the</strong> expected direction with water flow<br />
from <strong>the</strong> flagellar base towards <strong>the</strong> tip, <strong>the</strong> currents set up by <strong>the</strong> o<strong>the</strong>r 3 forms flow<br />
from <strong>the</strong> tip towards <strong>the</strong> base. In all 4 types <strong>the</strong> flagellar <strong>movement</strong>s take <strong>the</strong> form<br />
<strong>of</strong> plane sinusoidal undulations propagated from <strong>the</strong> base <strong>of</strong> <strong>the</strong> flagellum towards<br />
its tip, but <strong>the</strong> different types show adaptive modifications according to <strong>the</strong> pattern<br />
<strong>of</strong> water currents required. The rates <strong>of</strong> beat <strong>of</strong> <strong>the</strong> flagellum (range 30 to 50 cycles/<br />
sec) and <strong>the</strong> speeds <strong>of</strong> propagation <strong>of</strong> <strong>the</strong> contraction wave (range 100 to 600 /x/sec)<br />
did not differ sufficiently to explain different current patterns. It is suggested that<br />
<strong>the</strong> 'unexpected' direction <strong>of</strong> current flow in 3 <strong>of</strong> <strong>the</strong> types may be <strong>the</strong> result <strong>of</strong> <strong>the</strong><br />
presence <strong>of</strong> flagellar mastigonemes; <strong>the</strong>se are known to be present in <strong>the</strong> chrysomonad<br />
phyt<strong>of</strong>lagellates, to which group Monas and probably also <strong>Actinomonas</strong> and Poteriodendron<br />
belong. Attention is also drawn to <strong>the</strong> peculiar mode <strong>of</strong> coiling and unrolling<br />
<strong>of</strong> <strong>the</strong> flagellum <strong>of</strong> <strong>the</strong> bicoecid Poteriodendron.<br />
Introduction<br />
THE <strong>movement</strong> <strong>of</strong> flagella has been studied in few organisms, and this lack<br />
<strong>of</strong> knowledge is reflected in <strong>the</strong> confused accounts given in textbooks. Flagella<br />
can evidently produce <strong>movement</strong> <strong>of</strong> water in a variety <strong>of</strong> ways: sometimes <strong>the</strong>y<br />
act as pushing organelles (pulsella), trailing behind <strong>the</strong> organism as it moves,<br />
and in o<strong>the</strong>r cases <strong>the</strong>y may act as pulling organelles (tractella), when <strong>the</strong>y are<br />
held in front <strong>of</strong> <strong>the</strong> organism and draw it along. The pushing action <strong>of</strong> flagella<br />
is well known, in spermatozoa for example, and has recently been described<br />
for <strong>the</strong> longitudinal flagellum <strong>of</strong> <strong>the</strong> din<strong>of</strong>lagellate Ceratium (Jahn, Harmon,<br />
and Landman, 1963), but few convincing descriptions <strong>of</strong> flagella acting as<br />
tractella have been published until recently.<br />
Both Lowndes (1941,1943) and Brown (1945) have discussed <strong>the</strong> <strong>movement</strong><br />
<strong>of</strong> <strong>the</strong> flagellum <strong>of</strong> those <strong>flagellates</strong> in which <strong>the</strong> flagellar activity causes a<br />
gyration <strong>of</strong> <strong>the</strong> anterior end <strong>of</strong> <strong>the</strong> body, which 'screws' <strong>the</strong> organism through<br />
<strong>the</strong> water. Observations on Trypanosoma by Jahn and Fonseca (1963) and on<br />
trypanosomes and Strigomonas by Holwill (1963) have shown that in <strong>the</strong>se<br />
cases <strong>the</strong> propagated wave <strong>of</strong> contraction in <strong>the</strong> flagellum travels from <strong>the</strong> tip<br />
<strong>of</strong> <strong>the</strong> flagellum towards <strong>the</strong> basal body when <strong>the</strong> organism moves with <strong>the</strong><br />
flagellum in front, so that <strong>the</strong> way in which <strong>the</strong>se flagella act as tractella is<br />
fairly obvious. The action <strong>of</strong> <strong>the</strong> flagellum <strong>of</strong> Chromulina described in a<br />
preliminary report by Jahn, Landman, and Fonseca (1963) is much less<br />
IQuart. J. micr. Sci., Vol. 105, pt. 4, pp. 405-14, 1964.]
406 Sleigh—<strong>Flagellar</strong> <strong>movement</strong> <strong>of</strong> <strong>sessile</strong> <strong>flagellates</strong><br />
obvious; high-speed cinematograph studies have shown that, although <strong>the</strong><br />
flagellum is held in front <strong>of</strong> <strong>the</strong> body as it moves, and acts as a tractellum,<br />
<strong>the</strong> waves <strong>of</strong> contraction pass from <strong>the</strong> flagellar base towards <strong>the</strong> tip. In fact, <strong>the</strong><br />
flagellum is working in a similar manner to that described by Lowndes (1944)<br />
for <strong>the</strong> longer flagellum <strong>of</strong> Monas, which was found to move particles towards<br />
<strong>the</strong> flagellar base while <strong>the</strong> waves <strong>of</strong> contraction passed along <strong>the</strong> flagellum<br />
from base to tip; Lowndes believed that <strong>the</strong> flagellum moved in a spiral, but<br />
<strong>the</strong> <strong>movement</strong> <strong>of</strong> <strong>the</strong> flagellum <strong>of</strong> Chromulina takes place in a single plane.<br />
Jahn, Landman, and Fonseca suggest that flagellar mastigonemes may play<br />
a part in producing <strong>movement</strong> in a direction opposite to that expected.<br />
Studies by high-speed cinematograph methods have shown that <strong>the</strong> <strong>movement</strong><br />
<strong>of</strong> <strong>the</strong> flagellum usually takes place in a single plane, but in <strong>the</strong> transverse<br />
flagellum <strong>of</strong> Ceratium a helical <strong>movement</strong> <strong>of</strong> <strong>the</strong> flagellum has been observed<br />
(Jahn, Harmon, and Landman, 1963). The motion <strong>of</strong> sperm tails <strong>of</strong> <strong>the</strong> sea<br />
urchin and <strong>the</strong> bull is also believed to take <strong>the</strong> form <strong>of</strong> plane sine waves (Gray,<br />
}<br />
This study concerns observations on 4 <strong>sessile</strong> <strong>flagellates</strong> in which <strong>the</strong><br />
flagellum is held extended from <strong>the</strong> body and causes water currents from which<br />
food particles are collected. The water currents caused have previously been<br />
described in some cases, and occasional attempts have been made to describe<br />
<strong>the</strong> flagellar motion. Descriptions relevant to <strong>the</strong> forms studied will be mentioned<br />
later.<br />
Materials and methods<br />
The <strong>flagellates</strong> studied here were found in moss from a fresh-water stream<br />
known as Alphin Brook, near Exeter, Devon, during June 1963, with an<br />
abundance <strong>of</strong> o<strong>the</strong>r Protozoa, both ciliates and amoebae as well as <strong>flagellates</strong>.<br />
Confirmatory observations have been made on material from <strong>the</strong> River Avon<br />
near Bristol. These organisms were studied by phase-contrast microscopy<br />
and also under dark-ground illumination in order to investigate <strong>the</strong>ir structure<br />
and <strong>the</strong> motion <strong>of</strong> <strong>the</strong> water-borne particles that indicated <strong>the</strong> effects <strong>of</strong><br />
flagellar activity. The <strong>movement</strong> <strong>of</strong> <strong>the</strong> flagella <strong>the</strong>mselves was studied under<br />
stroboscopic illumination; this permitted an examination <strong>of</strong> <strong>the</strong> form <strong>of</strong><br />
flagellar beating, measurement <strong>of</strong> <strong>the</strong> frequency <strong>of</strong> beat, and, in some cases,<br />
photography <strong>of</strong> <strong>the</strong> flagellum in action. These photographs have too little<br />
contrast for reproduction, but form <strong>the</strong> basis for <strong>the</strong> drawings in this paper<br />
and for measurements <strong>of</strong> <strong>the</strong> length <strong>of</strong> <strong>the</strong> waves <strong>of</strong> contraction.<br />
Observations<br />
The organisms are not generally very well known, and <strong>the</strong> structure <strong>of</strong> each<br />
will <strong>the</strong>refore be described as far as is relevant here; after <strong>the</strong> description in<br />
each case an account will be given <strong>of</strong> <strong>the</strong> motion <strong>of</strong> <strong>the</strong> flagellum and <strong>the</strong> water<br />
<strong>movement</strong>s that <strong>the</strong> flagellum produces. The different patterns <strong>of</strong> flagellar<br />
<strong>movement</strong> will be compared later.
<strong>Actinomonas</strong><br />
Sleigh—<strong>Flagellar</strong> <strong>movement</strong> <strong>of</strong> <strong>sessile</strong> <strong>flagellates</strong> 407<br />
This is an organism <strong>of</strong> uncertain affinities, having both heliozoan and<br />
flagellate characters. The genus was originally described by Saville Kent<br />
(1880) on <strong>the</strong> basis <strong>of</strong> two marine species, each with a single flagellum and<br />
many fine straight pseudopodia. One fresh-water species, A. vernalis, with<br />
few branched capitate pseudopodia, was described by Stokes (1888) and<br />
ano<strong>the</strong>r fresh-water type, A. radiosa, with 4 to 6 pseudopodia was described<br />
by Roskin (1931). The description <strong>of</strong><br />
A. mirabilis by Greissmann (1914) from<br />
marine collections at Rosc<strong>of</strong>f is <strong>the</strong> most<br />
complete, but refers to an organism that<br />
is ra<strong>the</strong>r smaller than Kent's species <strong>of</strong><br />
<strong>the</strong> same name and has fewer pseudopodia;<br />
it corresponds more closely with<br />
Kent's A. pusilla. The fresh-water<br />
specimens used in this investigation<br />
agree closely with Greissmann's description<br />
<strong>of</strong> A. mirabilis, though <strong>the</strong> freshwater<br />
forms have fewer pseudopodia.<br />
The genus <strong>Actinomonas</strong> is <strong>of</strong>ten included<br />
in <strong>the</strong> Order Proteomyxida (see,<br />
for example, Tregoub<strong>of</strong>f, 1953), but<br />
Pascher (1918) has suggested a relationship<br />
with <strong>the</strong> chrysomonad <strong>flagellates</strong>,<br />
since leucosin is a storage product.<br />
The form <strong>of</strong> <strong>the</strong> body and <strong>the</strong> distribution<br />
<strong>of</strong> <strong>the</strong> appendages are shown<br />
in fig. 1. The almost spherical body<br />
(diameter 8 to 10 p) carries a single flagellum<br />
(length 20 to 30 /JL) at one pole, and<br />
at <strong>the</strong> o<strong>the</strong>r pole <strong>the</strong>re is a very slender<br />
flagellum<br />
filopodia<br />
FIG. 1. <strong>Actinomonas</strong>, showing body form<br />
and <strong>the</strong> water currents caused by flagellar<br />
beating.<br />
stalk (up to at least 60 (j, long) which attaches <strong>the</strong> body to a piece <strong>of</strong> debris or<br />
plant material. This stalk is usually rigid, but is also contractile in <strong>the</strong> sense<br />
that it suddenly bends, usually near <strong>the</strong> end that is attached to <strong>the</strong> substrate,<br />
and carries <strong>the</strong> body to a new position. Contractions <strong>of</strong> <strong>the</strong> stalk were seen to<br />
be especially violent when <strong>the</strong> organism was subjected to <strong>the</strong> bright illumination<br />
required for dark-ground observations, and <strong>the</strong>y caused rapid jerky <strong>movement</strong>s<br />
<strong>of</strong> <strong>the</strong> whole body when <strong>the</strong> stalk was detached from <strong>the</strong> substrate. The<br />
very fine filopodia (length 10 to 15 fi) occur in two groups, a ring <strong>of</strong> 6 to 8<br />
around <strong>the</strong> flagellar base, and ano<strong>the</strong>r ring <strong>of</strong> about 4 above <strong>the</strong> stalk; <strong>the</strong>y<br />
are apparently straight and permanent even when food is being ingested.<br />
Both Kent and Greissmann observed that <strong>the</strong> flagellum was held out stiffly<br />
from <strong>the</strong> body and caused water <strong>movement</strong>s that can be seen in <strong>the</strong> <strong>movement</strong><br />
<strong>of</strong> particles. The water circulation caused is shown in fig. 1; currents travel
408 Sleigh—<strong>Flagellar</strong> <strong>movement</strong> <strong>of</strong> <strong>sessile</strong> <strong>flagellates</strong><br />
towards <strong>the</strong> body from <strong>the</strong> region <strong>of</strong> <strong>the</strong> flagellar tip, and food particles<br />
become entangled in <strong>the</strong> filopodia. Small amoebae were seen to be caught in<br />
this way and carried down <strong>the</strong> filopodia to be ingested in <strong>the</strong> body.<br />
The flagellar beat is rapid and regular, and under stroboscopic illumination<br />
<strong>the</strong> form <strong>of</strong> beat is seen to be a sine wave with almost constant wavelength and<br />
amplitude along its length (<strong>the</strong>re is a slight tendency to an increase in both<br />
towards <strong>the</strong> distal end). Sometimes <strong>the</strong> flagellum appears as shown in fig. i<br />
when <strong>the</strong> sine wave is seen from <strong>the</strong> side, and sometimes <strong>the</strong> flagellum appears<br />
as a straight line that is seen as a dotted line at a particular optical level, when<br />
<strong>the</strong> sine wave is seen from <strong>the</strong> edge; evidently <strong>the</strong> beat takes place in a single<br />
plane. In observations on a number <strong>of</strong> specimens <strong>the</strong> waves <strong>of</strong> bending were<br />
always seen to pass up <strong>the</strong> flagellum from base to tip; it is certain that this<br />
observation is not a stroboscopic artifact. The frequency <strong>of</strong> beat at i8° C was<br />
on average about 50 cycles/sec, and <strong>the</strong> length <strong>of</strong> <strong>the</strong> waves <strong>of</strong> contraction was<br />
about 7 to 10 JX, so that <strong>the</strong> contraction waves were propagated at about 350<br />
to 500 /x/sec.<br />
Codonosiga<br />
This organism is well known from <strong>the</strong> studies <strong>of</strong> Kent (1880) and Lapage<br />
(1925), and <strong>the</strong> species used here, C. botrytis, is a common fresh-water choan<strong>of</strong>lagellate.<br />
Lapage has thoroughly described <strong>the</strong> organism and <strong>the</strong> water<br />
currents that are produced by flagellar activity, but he did not venture to<br />
describe <strong>the</strong> <strong>movement</strong> <strong>of</strong> <strong>the</strong> flagellum in any detail because it was normally<br />
too rapid to be seen. Hollande (1952) has discussed evidence relating <strong>the</strong><br />
choan<strong>of</strong>lagellates to <strong>the</strong> chrysomonad phyt<strong>of</strong>lagellates, but found it inconclusive.<br />
The individuals observed were attached to debris or moss by slender rigid<br />
stalks up to 100 fj, or more long; frequently <strong>the</strong>re were several animals on a<br />
single stalk. Each body (about 10 /u, long) carried a single flagellum (length 25<br />
to 30 p), whose base was at <strong>the</strong> centre <strong>of</strong> a collar (about 8 to 10 JJL tall). It was<br />
long believed that <strong>the</strong> collar was a conical membrane, but electron microscope<br />
observations <strong>of</strong> Fjerdingstad (1961) have confirmed an alternative belief—that<br />
<strong>the</strong> collar is made up <strong>of</strong> a palisade <strong>of</strong> microvilli, a structure that is shared with<br />
<strong>the</strong> choanocyte cells <strong>of</strong> sponges.<br />
Particles borne by water currents can be seen to flow in a three-dimensional<br />
vortex in which <strong>the</strong> water moves in below <strong>the</strong> flagellar base and is swept away<br />
along <strong>the</strong> axis <strong>of</strong> <strong>the</strong> flagellum towards its distal end (fig. 2, A). It is believed<br />
that water passes through <strong>the</strong> meshwork <strong>of</strong> <strong>the</strong> collar, where particles are<br />
strained from <strong>the</strong> water by <strong>the</strong> microvilli and carried down to <strong>the</strong> body by<br />
protoplasmic flow, to be engulfed in food vacuoles near <strong>the</strong> base <strong>of</strong> <strong>the</strong><br />
collar.<br />
The flagellum beats about 30 times/sec at 18° C, with a wavelength <strong>of</strong> 15<br />
to 2011, giving a speed <strong>of</strong> 450 to 600 /it/sec for <strong>the</strong> propagation <strong>of</strong> <strong>the</strong> contraction<br />
waves. The waves take place in a single plane, as is evident when organisms<br />
turn so that <strong>the</strong> waves may be seen from <strong>the</strong> edge. The waves <strong>of</strong> contraction
Sleigh—<strong>Flagellar</strong> <strong>movement</strong> <strong>of</strong> <strong>sessile</strong> <strong>flagellates</strong> 409<br />
pass from <strong>the</strong> base <strong>of</strong> <strong>the</strong> flagellum to <strong>the</strong> tip, and are sinusoidal, though with<br />
perhaps some increase in amplitude <strong>of</strong> <strong>the</strong> broad waves as <strong>the</strong>y near <strong>the</strong> tip.<br />
Monas<br />
Many organisms <strong>of</strong> <strong>the</strong> ochromonad type were found in <strong>the</strong> stream water<br />
and among <strong>the</strong>se were <strong>sessile</strong> forms that lacked plastids and had <strong>the</strong> body-form<br />
shown in fig. 2, B ; <strong>the</strong>y are believed to belong to <strong>the</strong> genus Monas. The <strong>movement</strong><br />
<strong>of</strong> Monas has been discussed by Krijgsman (1925) and Lowndes (1944),<br />
FIG. 2. A, Codonosiga; B, Monas,<br />
and figures by both authors have been published in textbooks to illustrate<br />
flagellar <strong>movement</strong>. Krijgsman considered that <strong>the</strong> flagellum performed an<br />
oar-like rowing stroke, but Lowndes pointed out that this <strong>movement</strong> was<br />
unlikely to be <strong>the</strong> normal mode <strong>of</strong> progression. By <strong>the</strong> use <strong>of</strong> a stroboscope<br />
Lowndes found that <strong>the</strong> flagellar waves moved from base to tip with a frequency<br />
<strong>of</strong> about 19 cycles/sec, that <strong>the</strong> waves increased in amplitude towards<br />
<strong>the</strong> tip, and that <strong>the</strong> water current set up was in <strong>the</strong> direction from <strong>the</strong> tip <strong>of</strong><br />
<strong>the</strong> flagellum towards <strong>the</strong> base. He pointed out that <strong>the</strong> organisms on which<br />
<strong>the</strong>se observations were made were swimming at much less than maximum<br />
speed. The waves passing up <strong>the</strong> flagellum were believed to be spiral, and<br />
this helical component provided a basis for Lowndes's explanation <strong>of</strong> <strong>the</strong><br />
mechanism <strong>of</strong> <strong>movement</strong>. He believed that <strong>the</strong> organisms always swam in a
41 o Sleigh—<strong>Flagellar</strong> <strong>movement</strong> <strong>of</strong> <strong>sessile</strong> <strong>flagellates</strong><br />
spiral and that <strong>the</strong> rotation and gyration provided <strong>the</strong> forward component <strong>of</strong><br />
<strong>movement</strong>. The <strong>sessile</strong> monads studied here could not move, nor turn quickly,<br />
so that <strong>the</strong> motion <strong>of</strong> <strong>the</strong> flagellum is easily seen.<br />
The body <strong>of</strong> <strong>the</strong> organism (some 10 to 12 \x in diameter) is attached to debris<br />
or moss by a very fine strand (some 20 /J. long), which is flexible and noncontractile<br />
(fig. 2, B). The two flagella emerge close toge<strong>the</strong>r, <strong>the</strong> longer one<br />
(25 to 30 fx in length) being extended almost straight out from <strong>the</strong> body, and<br />
<strong>the</strong> shorter one (about 5 [x long) being held curved close to <strong>the</strong> body.<br />
Strong water currents reminiscent <strong>of</strong> those caused by <strong>Actinomonas</strong> flow<br />
around <strong>the</strong> active flagellum (fig. 2, B), differing slightly in that <strong>the</strong>y impinge<br />
on <strong>the</strong> surface <strong>of</strong> <strong>the</strong> body at <strong>the</strong> flagellar base. Food particles are seen to be<br />
engulfed by activity <strong>of</strong> <strong>the</strong> body surface near <strong>the</strong> flagellar base and carried<br />
down <strong>the</strong> side <strong>of</strong> <strong>the</strong> body and into vacuoles. Food objects as large as diatoms<br />
30 to 40 ix long were seen enclosed in <strong>the</strong> body; intense flagellar activity must<br />
be used to collect such large objects.<br />
When seen under <strong>the</strong> stroboscope, <strong>the</strong> longer flagellum shows a roughly<br />
sinusoidal beat, in which both <strong>the</strong> amplitude and wavelength increased<br />
markedly towards <strong>the</strong> tip. The waves travel from base to tip and are planar.<br />
The frequency <strong>of</strong> beat is about 50 beats/sec at 20 0 C, and <strong>the</strong> wavelength<br />
increases from about 6 fx at <strong>the</strong> base to 10 to 12 fx distally, so that <strong>the</strong> waves<br />
are propagated at 300 jtt/sec basally and 500 to 600 //,/sec distally.<br />
The small flagellum appeared to flicker, but its motion was not found to be<br />
regular enough for stroboscopic observation. It may be concerned with <strong>the</strong><br />
trapping and ingestion <strong>of</strong> food particles.<br />
Poteriodendron<br />
The <strong>movement</strong> <strong>of</strong> <strong>the</strong> flagellum <strong>of</strong> this colonial bicoecid has been briefly<br />
discussed by Geitler (1942), but without stroboscopic or cinematographic<br />
observations he was unable to see <strong>the</strong> true nature <strong>of</strong> <strong>the</strong> beating activity. Kent<br />
(1880) noted that free-swimming bicoecids swam with <strong>the</strong>ir flagella held in<br />
front, presumably acting as tractella. While Kent classed bicoecids with <strong>the</strong><br />
chrysomonad phyt<strong>of</strong>lagellates, Geitler believed <strong>the</strong>m to be choan<strong>of</strong>lagellates,<br />
and Grasse and Deflandre (1952) found that <strong>the</strong>ir systematic position was<br />
uncertain because <strong>of</strong> lack <strong>of</strong> knowledge <strong>of</strong> <strong>the</strong>ir structure.<br />
Individuals <strong>of</strong> Poteriodendron occupy a stalked campanulate lorica (fig. 3, A),<br />
which is attached to plant material or debris. The stalk is secreted first, and<br />
<strong>the</strong>n <strong>the</strong> lorica, which has a spiral structure (Robinow, 1956), is produced<br />
from a continuous thread <strong>of</strong> secreted material laid down by rotation <strong>of</strong> <strong>the</strong><br />
animal; in one case <strong>the</strong> animal was observed to rotate continuously clockwise<br />
during secretion <strong>of</strong> <strong>the</strong> lorica, performing one complete rotation every 7 or 8<br />
min. The fully-formed lorica is about 15 /x long at <strong>the</strong> end <strong>of</strong> a stalk 5 to 30 fx<br />
long.<br />
The animal is attached to <strong>the</strong> base <strong>of</strong> <strong>the</strong> inside <strong>of</strong> <strong>the</strong> lorica by a contractile<br />
'foot' which is said to be a modified flagellum. The body <strong>of</strong> <strong>the</strong> organism<br />
(about 8 to 12 ju, long) is held near <strong>the</strong> mouth <strong>of</strong> <strong>the</strong> lorica at <strong>the</strong> end <strong>of</strong> <strong>the</strong> foot,
Sleigh—<strong>Flagellar</strong> <strong>movement</strong> <strong>of</strong> <strong>sessile</strong> <strong>flagellates</strong> 411<br />
and from it projects <strong>the</strong> stiffly held, but slightly curved, flagellum, 25 to 40 /x<br />
long. The flagellum is attached near <strong>the</strong> end <strong>of</strong> <strong>the</strong> body, at <strong>the</strong> base <strong>of</strong> an<br />
apical bulge.<br />
<strong>Flagellar</strong> activity sets up water currents which impinge on <strong>the</strong> body surface<br />
near <strong>the</strong> base <strong>of</strong> <strong>the</strong> flagellum, in which region food particles are ingested. The<br />
currents are different from those in ei<strong>the</strong>r <strong>Actinomonas</strong> or Monas, since<br />
<strong>the</strong> water is funnelled in from a considerable distance, but only close to <strong>the</strong><br />
flagellum (fig. 3, B). Stroboscopic observations show <strong>the</strong> reason for this: <strong>the</strong><br />
amplitude <strong>of</strong> <strong>the</strong> bending waves <strong>of</strong> <strong>the</strong> flagellum is small, and <strong>the</strong> sinusoidal<br />
'/ water currents •<br />
FIG. 3. Poteriodendron. A, part <strong>of</strong> a colony; B, water currents around <strong>the</strong> flagellum; c, unrolling<br />
<strong>of</strong> <strong>the</strong> flagellum on relaxation after retraction <strong>of</strong> <strong>the</strong> animal into <strong>the</strong> lorica.<br />
waves have a small wavelength which tends to decrease distally. Examination<br />
<strong>of</strong> <strong>the</strong> animal while it is rotating during <strong>the</strong> secretion <strong>of</strong> <strong>the</strong> lorica shows<br />
alternately <strong>the</strong> edge and flat face <strong>of</strong> a plane sine wave envelope <strong>of</strong> <strong>movement</strong>,<br />
and this is especially obvious under <strong>the</strong> stroboscope. The frequency <strong>of</strong> beat<br />
is 40 to 50 cycles/sec, and <strong>the</strong> wavelength 3 to 5 fj,, so that <strong>the</strong> rate <strong>of</strong> propagation<br />
<strong>of</strong> <strong>the</strong> contraction waves from <strong>the</strong> base to <strong>the</strong> tip <strong>of</strong> <strong>the</strong> flagellum is 120<br />
to 250 /x/sec.<br />
On stimulation <strong>of</strong> <strong>the</strong> animal it was retracted to <strong>the</strong> base <strong>of</strong> <strong>the</strong> lorica by <strong>the</strong><br />
contraction <strong>of</strong> <strong>the</strong> foot, and at <strong>the</strong> same time <strong>the</strong> flagellum coiled up very<br />
rapidly to assume <strong>the</strong> shape <strong>of</strong> a watchspring. On relaxation, <strong>the</strong> animal<br />
emerged as <strong>the</strong> foot extended and <strong>the</strong> flagellum slowly uncoiled over a period<br />
<strong>of</strong> a second or two (fig. 3, c). The contraction <strong>of</strong> a flagellum into a plane spiral<br />
is most unusual, and <strong>the</strong> mechanism involved must be considerably different<br />
from that which produces normal contractile waves in <strong>the</strong> flagellum.
412 Sleigh—<strong>Flagellar</strong> <strong>movement</strong> <strong>of</strong> <strong>sessile</strong> <strong>flagellates</strong><br />
Discussion<br />
In all <strong>the</strong>se 4 <strong>flagellates</strong> <strong>the</strong> flagellum is <strong>of</strong> a similar size, and plane waves<br />
<strong>of</strong> approximately sinusoidal form are propagated from <strong>the</strong> base to <strong>the</strong> tip (fig.<br />
4), yet <strong>the</strong> results <strong>of</strong> flagellar activity are all somewhat different. From studies<br />
on <strong>the</strong> tails <strong>of</strong> spermatozoa one would expect that water currents would be<br />
set up which travel in <strong>the</strong> same direction as <strong>the</strong> propagated bending waves<br />
in <strong>the</strong> flagellum, and this is indeed what has been observed in Codonosiga. In<br />
<strong>the</strong> o<strong>the</strong>r 3 examples <strong>the</strong> water currents were observed to travel in <strong>the</strong> direction<br />
opposite to that in which <strong>the</strong> flagellar waves are propagated; this is not easily<br />
explained.<br />
<strong>Actinomonas</strong> Codonosiga. Monas Potehodendron<br />
FIG. 4. Comparison <strong>of</strong> <strong>the</strong> form <strong>of</strong> flagella during beating.<br />
At this point it is interesting to draw an analogy with <strong>the</strong> <strong>movement</strong> <strong>of</strong><br />
organisms <strong>of</strong> larger size. Comparison <strong>of</strong> <strong>the</strong> swimming <strong>of</strong> an eel with that<br />
<strong>of</strong> a polychaete worm like Nepktys is instructive. The eel propagates waves <strong>of</strong><br />
bending from <strong>the</strong> head to <strong>the</strong> tail as it moves through <strong>the</strong> water, while in<br />
Nephtys <strong>the</strong> waves <strong>of</strong> bending are propagated from <strong>the</strong> tail to <strong>the</strong> head as <strong>the</strong><br />
animal swims head-first. The difference here is <strong>the</strong> presence <strong>of</strong> <strong>the</strong> paddle-like<br />
parapodia situated in <strong>the</strong> plane <strong>of</strong> <strong>the</strong> oscillations in <strong>the</strong> polychaete, while <strong>the</strong><br />
eel is smooth-bodied. Taylor (1952) approached this problem from a ma<strong>the</strong>matical<br />
point <strong>of</strong> view, and found from <strong>the</strong>oretical calculations that, while <strong>the</strong><br />
propagation <strong>of</strong> sinusoidal waves along a smooth thin cylinder will cause<br />
<strong>movement</strong> <strong>of</strong> water in <strong>the</strong> same direction as <strong>the</strong> propagation <strong>of</strong> <strong>the</strong> waves, <strong>the</strong><br />
propagation <strong>of</strong> similar waves along a cylinder whose surface is sufficiently<br />
rough, and whose roughness has a directional character, may cause <strong>movement</strong><br />
in a direction opposite to <strong>the</strong> direction <strong>of</strong> propagation <strong>of</strong> <strong>the</strong> waves.<br />
It is possible that <strong>the</strong> flagellum <strong>of</strong> <strong>the</strong>se <strong>flagellates</strong> uses a similar mechanism.<br />
The presence <strong>of</strong> mastigonemes or flimmer filaments on many flagella is well<br />
established (see Pitelka, 1963), but <strong>the</strong>ir arrangement on <strong>the</strong> flagellar shaft is<br />
as yet unknown. Flimmer filaments appear to be <strong>of</strong> two distinct types: <strong>the</strong><br />
larger mastigoneme structures several micra long and 10 to 20 m/x in diameter,<br />
and finer filaments only 2 m/x or so in diameter. Light microscopists found that<br />
many flagella carry flimmer filaments, and Deflandre (1934) listed choan<strong>of</strong>lagellates<br />
and chrysomonad <strong>flagellates</strong> among those forms whose flagella<br />
carry lateral appendages; however, only by electron microscopy is it possible
Sleigh—<strong>Flagellar</strong> <strong>movement</strong> <strong>of</strong> <strong>sessile</strong> <strong>flagellates</strong> 413<br />
to determine <strong>the</strong> type and arrangement <strong>of</strong> <strong>the</strong> flimmer filaments adequately.<br />
The long flagellum <strong>of</strong> ochromonad <strong>flagellates</strong>, which no doubt has <strong>the</strong> same<br />
structure as that <strong>of</strong> Manas, has been found to carry both mastigonemes and<br />
fine filaments (Pitelka and Schooley, 1955), but no clear evidence is available<br />
about <strong>the</strong> o<strong>the</strong>r types studied here. Electron micrographs <strong>of</strong> Codonosiga by<br />
Petersen and Hansen (1954) show a fibrous zone around <strong>the</strong> flagellum which<br />
may represent poorly-preserved flimmer filaments, and Afzelius (1961) found<br />
that thin flimmer filaments were present in <strong>the</strong> plane <strong>of</strong> <strong>the</strong> central fibres <strong>of</strong><br />
<strong>the</strong> choanocyte flagellum <strong>of</strong> <strong>the</strong> sponge Microciona; <strong>the</strong> flimmer filaments <strong>of</strong><br />
choan<strong>of</strong>lagellates may well be <strong>of</strong> <strong>the</strong> same type. It is worth noticing that <strong>the</strong>se<br />
filaments are not situated in <strong>the</strong> presumed plane <strong>of</strong> oscillation <strong>of</strong> <strong>the</strong> sponge<br />
flagellum, but in <strong>the</strong> plane at right angles to this. It is possible that in <strong>Actinomonas</strong>,<br />
Monas, and Poteriodendron <strong>the</strong>re are mastigonemes situated in <strong>the</strong><br />
plane <strong>of</strong> <strong>the</strong> oscillations (ei<strong>the</strong>r in two rows, or all round like <strong>the</strong> hairs <strong>of</strong> a<br />
bottle brush), which may act to move water in <strong>the</strong> direction opposite to that<br />
expected, by providing <strong>the</strong> roughness mentioned in Taylor's <strong>the</strong>oretical consideration<br />
<strong>of</strong> <strong>the</strong> <strong>movement</strong> <strong>of</strong> undulating thin cylinders. These mastigonemes<br />
may perhaps be visualized as oars projecting from <strong>the</strong> flagellar shaft which row<br />
water towards <strong>the</strong> flagellar base as <strong>the</strong> crests <strong>of</strong> <strong>the</strong> waves <strong>of</strong> bending move up<br />
<strong>the</strong> flagellum.<br />
There is doubt as to <strong>the</strong> systematic position <strong>of</strong> both <strong>Actinomonas</strong> and <strong>the</strong><br />
bicoecids, but <strong>the</strong> similarity <strong>of</strong> <strong>the</strong>ir flagellar activity to that <strong>of</strong> Monas and<br />
o<strong>the</strong>r chrysomonads that I have studied suggest that <strong>the</strong>y may belong to this<br />
group; indeed Pascher has included <strong>Actinomonas</strong> with <strong>the</strong> chrysomonads for<br />
ano<strong>the</strong>r reason, and several probable bicoecids like Codonodendron are <strong>of</strong>ten<br />
placed in <strong>the</strong> same group <strong>of</strong> phyt<strong>of</strong>lagellates.<br />
It is interesting to note <strong>the</strong> adaptive modification <strong>of</strong> <strong>the</strong> form <strong>of</strong> flagellar<br />
beat in <strong>Actinomonas</strong>, Monas, and Poteriodendron. The food-catching pseudopodia<br />
<strong>of</strong> <strong>Actinomonas</strong> only require a broad stream <strong>of</strong> water-carrying particles,<br />
but in <strong>the</strong> o<strong>the</strong>r two forms <strong>the</strong> particles must hit <strong>the</strong> body near <strong>the</strong> flagellar<br />
base. In Monas this is achieved by funnelling <strong>the</strong> water current towards <strong>the</strong><br />
body by increasing <strong>the</strong> amplitude <strong>of</strong> <strong>the</strong> bending waves <strong>of</strong> <strong>the</strong> flagellum distally,<br />
and in Poteriodendron <strong>the</strong> amplitude <strong>of</strong> <strong>the</strong> waves is kept small so that <strong>the</strong><br />
main current is close to <strong>the</strong> flagellar shaft and impinges on <strong>the</strong> body surface.<br />
Evidently <strong>the</strong>re is a considerable variety <strong>of</strong> patterns <strong>of</strong> flagellar <strong>movement</strong>,<br />
and a full range <strong>of</strong> <strong>the</strong>se patterns must be studied before <strong>the</strong> mode <strong>of</strong> functioning<br />
<strong>of</strong> <strong>the</strong> contractile mechanism <strong>of</strong> <strong>the</strong> flagellum can be properly understood.<br />
The first observations were made at <strong>the</strong> University <strong>of</strong> Exeter, in <strong>the</strong> Department<br />
<strong>of</strong> Pr<strong>of</strong>essor L. A. Harvey, whom I should like to thank for his interest.<br />
I am also grateful to Pr<strong>of</strong>essor J. E. Harris, F.R.S., for reading <strong>the</strong> manuscript.
414 Sleigh—<strong>Flagellar</strong> <strong>movement</strong> <strong>of</strong> <strong>sessile</strong> <strong>flagellates</strong><br />
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